OCEANOGRAPHY and MARINE BIOLOGY AN ANNUAL REVIEW

Volume 44

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Volume 44

Editors R.N. Gibson Scottish Association for Marine Science The Dunstaffnage Marine Laboratory Oban, Argyll, Scotland [email protected] R.J.A. Atkinson University Marine Biology Station Millport University of London Isle of Cumbrae, Scotland [email protected] J.D.M. Gordon Scottish Association for Marine Science The Dunstaffnage Marine Laboratory Oban, Argyll, Scotland [email protected]

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Contents

Preface vii

Correction to Volume 43 ix

Review of three-dimensional ecological modelling related to the North Sea shelf system. Part II: model validation and data needs 1 Günther Radach & Andreas Moll

Role, routes and effects of manganese in crustaceans 61 Susanne P. Baden & Susanne P. Eriksson

Macrofaunal burrowing: the medium is the message 85 Kelly M. Dorgan, Peter A. Jumars, Bruce D. Johnson & Bernard P. Boudreau

Mediterranean coralligenous assemblages: a synthesis of present knowledge 123 Enric Ballesteros

Defensive glandular structures in opisthobranch molluscs — from histology to ecology 197 Heike Wägele, Manuel Ballesteros & Conxita Avila

Taxonomy, ecology and behaviour of the cirrate octopods 277 Martin A. Collins & Roger Villanueva

The ecology of rafting in the marine environment. III. Biogeographical and evolutionary consequences 323 Martin Thiel & Pilar A. Haye

Potential effects of climate change on marine mammals 431 J.A. Learmonth, C.D. MacLeod, M.B. Santos, G.J. Pierce, H.Q.P. Crick & R.A. Robinson

Author Index 465

Systematic Index 497

Subject Index 515

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Preface

The forty-fourth volume of this series contains eight reviews written by an international array of authors that, as usual, range widely in subject and taxonomic and geographic coverage. The editors welcome suggestions from potential authors for topics they consider could form the basis of future appropriate contributions. Because an annual publication schedule necessarily places constraints on the timetable for submission, evaluation and acceptance of manuscripts, potential contributors are advised to contact the editors at an early stage of preparation. Contact details are listed on the title page of this volume. The editors gratefully acknowledge the willingness and speed with which authors complied with the editors’ suggestions, requests and questions, and the efficiency of Taylor & Francis in ensuring the timely appearance of this volume.

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Correction to Volume 43

Carney, R.S. 2005. Zonation of deep biota on continental margins. Oceanography and Marine Biology: An Annual Review 43, 211Ð278. In reviewing various ideas put forward to explain deep benthic depth zonation (Carney 2005), the TROX, Trophic-Oxygen, model for foraminiferan distributions received special mention. This conceptual model incorporates in an easily understood manner several lines of thought concerning the importance of oxygen and labile carbon influx in controlling surficial and interstitial microhab- itats. The origin of the TROX model, however, is misattributed to Loubere and his associates (page 228). The TROX model was proposed in the context of microhabitats with Adriatic transect data used as an example by Jorissen et al. (1995). An important feature of the TROX model is the explicit link between oxygen and carbon flux, such that the ecological importance of food avail- ability changes with oxygen concentration. Given adequate oxygen, food is the primary factor. When microbial consumption of higher food levels reduces microhabitat oxygen, then low oxygen can become the primary factor. There have been other attempts to create general foraminiferan distribution models that incorporate both oxygen and carbon flux somewhat similar to TROX. An algebraically formal model of gradient distribution employing the concept of ‘r’ and ‘K’ selected species was developed by Sjoerdsma & van der Zwaan (1992) and tested with mixed success on archived distribution data from the Gulf of Mexico. Unfortunately, the geochemical relationship between oxygen and carbon flux was omitted. Bottom oxygen was estimated from water column profiles, and flux estimated only on the basis of depth. The conceptual model proposed by Loubere et al. (1993) was an assemblage model incorporating both production and taphonomy. Like the TROX model, it is an important contribution to the understanding of trophic control of geographic distribution. That mode links the geochemistry of oxygen and carbon flux. Flux was estimated from sedimentary oxygen consumption; samples were analysed from the western Gulf of Mexico.

REFERENCES

Carney, R.S. 2005. Zonation of deep biota on continental margins. Oceanography and Marine Biology: An Annual Review 43, 211Ð278. Jorissen, F.J., de Stigter, H.C. & Widmark, J.G.V. 1995. A conceptual model explaining benthic foraminiferal microhabitats. Marine Micropaleontology 26, 3Ð15. Loubere, P., Gary, A. & Lagoe, M. 1993. Generation of the benthic foraminiferal assemblage — theory and preliminary data. Marine Micropaleontology 20, 165Ð181. Sjoerdsma, P.G. & van der Zwaan, G.J. 1992. Simulating the effect of changing organic flux and oxygen content on the distribution of benthic Foraminifera. Marine Micropaleontology 19, 103Ð150.

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Oceanography and Marine Biology: An Annual Review, 2006, 44, 1-60 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis

REVIEW OF THREE-DIMENSIONAL ECOLOGICAL MODELLING RELATED TO THE NORTH SEA SHELF SYSTEM. PART II: MODEL VALIDATION AND DATA NEEDS

GÜNTHER RADACH & ANDREAS MOLL Institut für Meereskunde (IfM), Universität Hamburg (ZMK-ZMAW), Bundesstr. 53, D-20146 Hamburg, Germany E-mail: [email protected], [email protected]

Abstract The aim of this review is to provide an overview of the status of validation of eleven biogeochemical and ecological models of the greater North Sea (COHERENS, CSM-NZB, DCM- NZB, DYMONNS, ECOHAM, ELISE, ERSEM, FYFY, GHER, NORWECOM, POLCOMS- ERSEM) showing the realism achieved as well as the problems hindering a better degree of validity of the models. Several of the models were able to reproduce observations of the state variables correctly within an order of magnitude, but all models are not capable of reproducing every simulated state variable in the range of observations. None of the models can be called a valid model. Comparison of results from different models with datasets are evaluated according to the different spatial and temporal scales, for which data products were available, namely for regional distributions, annual cycles, long-term developments and events. The higher the trophic level, the greater was the discrepancy with the data. Problems still exist in determining the necessary com- plexity of the ecosystem model. More complexity in the model does not necessarily improve the simulations. Special attention should be devoted to the regeneration mechanisms in the sediments. Species’ groups have been simulated so far with rather limited success. The ecological model simulations did not reproduce fully the observed variability. Possible sources of lacking coincidence with observations originating from the spatial and temporal resolution of the internal dynamics, the trophic resolution, or the resolution of the forcing functions are discussed. Most of the models still need to be evaluated more intensively for their predictive potential to be judged. They have not yet been tested to a degree which is possible today using the various existing datasets from the northwest European shelf seas (presented in the Appendix). Common datasets for the necessary annual cycles of forcing functions are needed.

Introduction The overall aim of this review is to give an overview on the state-of-the-art biogeochemical and ecological three-dimensional modelling related to the marine ecosystem of the greater North Sea. The goal is to provide guidelines for the further development of marine ecosystem models which will be used in the future for making predictions about how the marine ecosystem of the North Sea functions and how concentrations and fluxes of biologically important elements like carbon, nitrogen, phosphorus, silicon and oxygen vary in space and time, throughout the shelf over a timescale of years, in response to physical forcing. Three-dimensional physical oceanographic modelling, which forms the basis of the ecological models, was recently reviewed by Jones (2002).

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With respect to future environmental problems occurring in the North Sea, a decadal frame has to be envisaged for modelling. Models are the only tools which can be used as a means to investigate developments of annual cycles and interannual variability in shelf sea systems to be expected in future decades, by simulating scenarios with different initial settings and boundary conditions. This review consists of two parts. Part I (Moll & Radach 2003) described the existing ecological models dealing with the greater North Sea; it characterised the complexity and the achievements of eleven ecosystem models for the whole North Sea or parts of it. Seven of these models are three- dimensional models (NORWECOM, GHER, ECOHAM, ERSEM, ELISE, COHERENS, POLCOMS-ERSEM) designed for describing the ecosystem dynamics of the North Sea, based on the physical oceanographic circulation, in more or less detail. Several of the models were used for specific applications, some of which have already been described in the literature. The information about these models and their applications from all available papers were aggregated under the heading of the names of the eleven ecological models in Moll & Radach (2003; their Table 1). This Part II provides an overview of the status of validating these models of the greater North Sea area. The term ‘status of validation’ denotes the current state of realism which a model has reached, as shown by the process of validating the model results by appropriate methods. The status of validation is considered to be a very important property of these models, because it is of great importance for simulating future scenarios that the simulations can realistically reproduce a series of observed annual cycles and especially their observed variability. The aim of this part is not only to show the realism achieved, but also to find out the problems hindering a better degree of validity of the models. The basis for both parts is the published literature on biogeochemical and ecological three- dimensional modelling related to the marine ecosystem of the greater North Sea. Although this review is concentrated on the North Sea, the problems arising in modelling other shelf seas and also the oceans in temperate climatic regions are very similar, as the corresponding literature shows. The quality of the simulations is reported on the basis of judgements of the facts given in the publication, in so far as they help to elucidate the achievements and failures of the models. Being restricted to the knowledge contained in the publications, very often questions about causes of failures must remain open. The order of the paper is as follows: after a short recapitulation of the published attempts at validating the models, the applied validation methods and the quantitative measures of the goodness of fit used for evaluating the comparison of simulations and data are briefly reported. Then the validational status of the selected models is discussed in detail with respect to defined space and timescales: The simulation results presented in the available literature are analysed with respect to regional horizontal distributions, to annual cycles and long-term developments, and also the tem- poral event scale. The discussion brings out common features of success and failure of the models and suggests measures to overcome the problems. A few important datasets available for testing the models are located and briefly described in the Appendix.

Validational efforts for ecological models for the North Sea Before presenting the validational state of the marine ecological North Sea models listed in Table 1, those publications which contain information on validational efforts are summarised. For most of the models their results were compared more or less thoroughly to observations. In a few cases comparisons to common datasets were performed. Nearly all models presented time-series of sim- ulated state variables vs. observed data in graphical form and they presented annual cycles of various state variables in comparison to either observed time-series at special locations or aggregated and averaged box data. While older simulations concentrated on the mean situation, newer papers also compared their simulations with data from actual years.

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VALIDATION OF THREE-DIMENSIONAL ECOLOGICAL MODELLING 2000, 2005) 2000, 2005) (OSPAR et al., 1998) et (OSPAR (OSPAR et al., 1998) et (OSPAR No (OSPAR et al., 1998) et (OSPAR No (OSPAR et al., 1998) et (OSPAR No et al., 1998), (OSPAR and Moll, (Skogen al., 1998) et (OSPAR (OSPAR et al., 1998), (OSPAR and Moll, (Skogen References for model quantitative comparison study No arts only arts only arts only arts only arts only Whole time P Unknown Unknown P Whole time Whole time Whole region Whole time Whole region P P Whole time Whole time Whole region P Comparison: 1. In space 2. In time Not mentioned Whole area mean None ime-series data Dutch coastal transect data only Parts PHAEOCYC reference station Whole region ICES data NERC NSP data Cruise data, E1 station data French Monitoring Network NERC NSP data, NOWESP T ECOMOD data, ICES data, Literature data Literature data (NPP only) NERC NSP data SKAGEX data SKAGEX NERC NSP data ICES data None 1985 1987 1995 NERC NSP data 1985 1988Ð1989 1955Ð1993 1985 1986 1988Ð1989 1989 1985 1988 1993 Simulation year Datasets Mean situation Graphically Mean situation Graphically Not mentioned Graphically Actual year Graphically Actual year Graphically Mean situation and actual years statistical analysis (Pätsch and Radach, 1997) Graphically, Mean situation cost function (see Moll, 2000) Graphically, Mean situation Graphically Actual year Graphically Averaged box data Averaged Mean situation and actual years 2000) cost function (see Soiland and Skogen, Graphically, Averaged box data Averaged Characteristic of validational effort: Characteristic of validational of data Type 1. 2. Actuality with citation) (if quantitative of validation Type 3. Time-series and averaged box data and averaged Time-series No validation exercise No validation Averaged box data Averaged Averaged box data Averaged Averaged box data Averaged Time-series and averaged box data and averaged Time-series Time-series alidational efforts for eleven North Sea models for eleven alidational efforts V CSM-NZB, DCM-NZB of station data Time-series MIRO POLCOMS-ERSEM box data Averaged ELISE ERSEM GHER ECOHAM NORWECOM able 1 9 8 6 COHERENS 7 5 4 2 3 1 10 FYFY 11 DYMONNS T No Model name 3

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The NORWECOM model went through consecutive validational steps. Firstly annual net primary production values were presented as tables (Skogen et al. 1995). Later a comparison of station data from the Norwegian section in the Skagerrak for nitrate and chlorophyll were displayed graphically (Skogen et al. 1998). A comparison of the horizontal distribution for long-term seasonal averages was presented by Soiland & Skogen (2000) showing the observed and modelled distri- butions, their differences, and the cost function fields for the state variables inorganic nitrogen, phosphate, silicate and chlorophyll for the surface (0Ð20 m) and for oxygen below 20 m for the whole North Sea. The validational process was continued by comparing data from the Torungen- Hirtshals section in the Skagerrak area for the years 2000 and 2001 with results from the model (Skogen et al. 2002, 2003). For the ECOHAM model the state variables phosphate and chlorophyll were compared with observed regional long-term monthly means to resolve the annual cycles (Moll 1998). Cost function values were calculated for North Sea wide chlorophyll and phosphate distributions (Moll 2000), and an evaluation of the monthly annual cycles was made for selected boxes. The seasonal dynamics of the North Sea sediments were also simulated by coupling ECOHAM to a sediment model. The evaluation of the validity of the seasonal dynamics in the water column was continued using this extended version of the model (Luff & Moll 2004), including the sediment dynamics, and also validational efforts for the state variables in the sediment were presented. ECOHAM was supple- mented by the nitrogen cycle for simulating the annual dynamics; this version was than applied to the Bohai Sea, China (Zhao et al. 2002, Wei et al. 2003). A validation exercise for dissolved inorganic nitrogen concentrations was also performed by Wei et al. (2004), comparing the simula- tion results with observations from 1998Ð1999. The model was extended by adding the full carbon cycle (Moll et al. 2003) and this new version (ECOHAM2) was compared to the previous version (ECOHAM1) to illustrate improvements for chlorophyll cycles in winter conditions in the North Sea. It is intended to run ECOHAM2 to study the zooplankton population dynamics of the single species Pseudocalanus elongatus of the North Sea with its physical and biological interactions (Andreas Moll, personal communication 2006). Several papers contributed to an intensive validational effort for the ERSEM model. Compar- isons with data exist for all macro-nutrients, silicate, phosphate, nitrate and ammonium (Baretta et al. 1995, Radach & Lenhart 1995) for almost all regions of the North Sea. A detailed comparison of annual cycles for phytoplankton groups was given by Ebenhöh et al. (1997), discriminating diatoms, flagellates and total chlorophyll. Baretta-Bekker et al. (1995, 1997) provided a comparison with data for bacteria, heterotrophic flagellates and microzooplankton annual cycles showing the improvements in process parameterisations from ERSEM-I to ERSEM-II for different coastal boxes. The diagenetic module in ERSEM simulated the nutrient regeneration in the sediments, and Ruardij & van Raaphorst (1995) compared oxygen penetration depth and nutrient profiles for the upper 10 cm for February and August. Observed benthic macrofauna was subject to a comparison by Blackford (1997). In addition to the comparison of the annual cycles of nutrients and phytoplankton with climatological data, Pätsch & Radach (1997) compared corresponding long-term time-series from Helgoland Reede from 1962Ð1993, including statistical analysis of the observed and simulated variability. ERSEM was applied to the Humber plume area (Allen 1997) with an additional validational step for the annual cycles of nutrients and plankton groups. A validation exercise for oxygen concentrations, chlorophyll and all four nutrients was also performed by Allen et al. (1998), using the results from a water column version of ERSEM for the different regime of the Adriatic Sea. ERSEM is the best studied model. The validational tests of the POLCOMS-ERSEM model presented by Allen et al. (2001) at two sites of the NERC NSP stations used the ERSEM project data for several state variables of nutrients, chlorophyll and plankton groups. This was updated by Allen et al. (2004) studying turbulence as a control parameter in a one-dimensional ERSEM setup coupled to the General Ocean Turbulence

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Model (GOTM) (Burchard et al. 1999). The POLCOMS-ERSEM model was used by Proctor et al. (2003) to simulate the seasonal cycle of nutrients (nitrate, ammonium, phosphate and silicate) and primary and secondary production for the year 1995. Also nutrient budgets were calculated and compared with previous estimates. It is intended to run POLCOMS-ERSEM for the full northwest shelf in operational mode on a supercomputer to study eutrophication of the southern North Sea on a 6 km grid (Martin Holt, personal communication 2005). Concerning the ELISE model for the English Channel region simulation results for nitrate, silicate and phytoplankton nitrogen content were compared with data on the basis of an annual cycle for distinct regions of the Channel (Menesguen & Hoch 1997). Long-term simulations were investigated for the Bay of Seine (Guillaud & Menesguen 1998, Guillaud et al. 2000). They provided a validational effort for particulate phosphorus in the sediment. For the one-dimensional version of the COHERENS model Tett & Walne (1995) attempted a validation for three NERC NSP stations over the annual cycle. Lee et al. (2002) reduced the spatial dimensions of the COHERENS model to extend and improve the benthic and pelagic biology in a one-dimensional depth-resolving version of the model (called PROWQM) by coupling the physical and microbiological processes in the water column with the sedimentation, resuspension and benthic mineralisation processes. The results were extensively compared with data and results from studies on models. The three-dimensional model results have not yet been tested against data, but several verification studies were conducted (Luyten et al. 1999). Currently a new physical-biological coupled ecosystem model called ECOSMO for the North Sea and the Baltic Sea is under development (Corinna Schrum, personal communication 2005) using the HAMSOM circulation model (Schrum & Backhaus 1999). The other two-dimensional ecological model systems (CSM/DCM-NZB, MIRO and DYMONNS), which were discussed in Moll & Radach (2003), will also be dealt with because they contributed to North Sea model validation exercises. The DCM-NZB model compared annual nutrient and chlorophyll data for the Noordwijk section and oxygen data for the Terschelling section off the Dutch coast (Peeters et al. 1995). Los & Bokhorst (1997) provided a long-term simulation for reproducing the data from the Noordwijk transect over 20 years, comparing also the mean annual cycles for all nutrients and chlorophyll. De Vries et al. (1998) extended the analysis of the coastal gradients. For the CSM-NZB model a calibration study investigated the whole North Sea simulation in comparison to observed nutrients and chlorophyll (Bokhorst & Los 1997, MARE et al. 2001). A synthesis of the validational exercises on the MIRO model was presented by Lancelot et al. (1997), where observed and predicted nutrients and phytoplankton in terms of chlorophyll and Phaeocystis cells were compared in the Dutch, Belgian and French coastal zones. Lancelot et al. (2005) gave a full representation of the 0-d MIRO model (including the equations), which was set up as a quasi-closed 3-box system. They compared annual cycles simulated under climatological forcing (1989Ð1999) with data from 1989Ð2000. The MIRO model (Lancelot et al. 2005) is cur- rently being included into a three-dimensional coupled physical-biological model (MIRO&CO-3D) using the COHERENS physical model (Geneviève Lacroix, personal communication 2005) where simulated chlorophyll is compared with ocean colour data for the year 2003. For the DYMONNS model the total pelagic dissolved nitrogen content was compared against NERC data for the southern North Sea (Kelly-Gerreyn et al. 1997). Hydes et al. (1997) compared monthly primary production values for aggregated ICES boxes. For the FYFY and GHER models there has so far been less effort to validate the models. Seven models of the North Sea ecosystem (CSM-NZB/DCM-NZB, DYMONNS, ECOHAM, ELISE, ERSEM, MIRO, NORWECOM) were compared against common datasets of observations. This model comparison study was conducted by the OSPAR Commission, in a workshop on eutrophication issues, to evaluate the agreement between the results from the models and available observations (OSPAR et al. 1998). The comparison used ‘cost functions’ as defined below in the

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section ‘Applied validation methods: Measuring the goodness of the simulations’. This model comparison exercise became a reference for further comparisons which have been mentioned already in the foregoing paragraphs and which will be reported on in the course of this review. Three aspects were investigated: (1) regional distributions, (2) annual cycles and (3) long-term developments. In fact, the available datasets dictated which comparisons between results from the model and data could be made. The following specific datasets, created by averaging observations on different spatial and temporal scales, could be used for such a comparison using cost functions:

1. The dataset for regional distributions resulted from long-term seasonal averaging (e.g., for ‘winter’, averaging data from January and February) of all available data for the whole of the North Sea on a grid of 1û longitude and 0.5û latitude. 2. The dataset for annual cycles consisted of monthly mean data derived by climatological averaging (over about three decades) for 1û longitude × 1û latitude boxes for the whole North Sea. 3. The dataset for long-term developments used time-series for up to four decades at specific stations with relatively fine temporal resolution.

These and similar datasets (see Appendix) were used in many of the comparisons between simulation results and data products, during the workshop and in later work. In summary detailed quantitative validational efforts were presented for only a few models, like NORWECOM, ECOHAM1 and ERSEM, when applied to some specific regions. These efforts used either the evaluation of a cost function as in OSPAR et al. (1998) or provided a quantitative statistical analysis of observed and simulated variability. Validational exercises were restricted by the available databases. The comparisons may build on averaged box data as climatological means, at best, when aiming at covering the whole North Sea region. However, annual cycles are resolved only by a few datasets, some of which are identified in the Appendix. Observations resolving actual years, like the NERC North Sea Project dataset (see Howarth et al. 1994) are rare. The validational efforts for ERSEM, ECOHAM and NORWECOM were the most intensive. Comparisons of datasets with the results of long-term simulations covering four decades are rarely presented, although observations at Helgoland and other stations (see Visser et al. 1996) exist. Up-to-date observations are, however, rarely obtained directly for model validation purposes.

Validational status of the ecological models for the North Sea Validation of a computational model is the process of formulating and substantiating explicit claims about the applicability and accuracy of computational results, with reference to the intended purposes of the model as well as to the natural system it represents (Lynch & Davies 1995). In this process the results provided by the simulations are tested against the available observations. The logic is as follows: The simulation model is used for reproducing a past situation (which is often called a ‘prediction’; a better term would be ‘hindcast’). The available observations for this past period of time serve as a means to judge the reliability of the simulation. The goodness of the agreement between model results and observations provides the degree of faith in the use of the simulation model for the future, for which, of course, no test against observations can be made beforehand. In a more general understanding of the whole validational process code verification and com- parison of observations vs. simulated results are only two aspects of validation, according to Dee (1995). The term ‘conceptual validation’ concerns the formulation of the reduced system of equa- tions. The objective of ‘algorithmic validation’ is to ensure that the finite set of equations was

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transformed into a valid finite-dimensional representation. ‘Software validation’ includes all activ- ities which increase confidence in the correctness of the coding. This step is often called ‘model verification’. Finally, the procedure of testing the validity of claims about the functionality of the computational model is called ‘functional validation’, in which it is shown whether or not a model is able to reproduce certain behaviour of the system modelled. The last step is often called ‘model validation’. For further discussion of a proper use of the terms ‘verification’ and ‘validation’ see Popper (1982) and Oreskes et al. (1994). In marine ecological modelling, the term ‘model validation’ is mostly used in the sense as defined above, and the term validation is associated with ‘establishing the agreement between predictions and observations’, as opposed to ‘model verification’, which tends to be used in the sense of ‘checking that the mathematical equations are being solved numerically correctly’. Soft- ware validation and functional validation are the only two steps of the several validational steps mentioned which will be discussed in the following sections in some detail. In the reviewed literature the term ‘validation’ has often been used ambiguously. Not only the process of validation (i.e., a ‘validational effort’) was called ‘validation’, but often the authors meant that the procedure in itself ensures the proof that the model is valid: The models were called ‘validated’ when the authors merely performed comparisons between simulation and observations. This rather euphemistic use of the word ‘validation’ is misleading and will not be adopted by us. Performing validational tests does not mean automatically that the tests are successful and the model is valid. The term ‘validated model’ is used for a ‘valid model’, which is a well-tested model that has proven to be realistic and which can be used with confidence in other cases where similar conditions apply (see Popper 1982). In the evaluation a strict differentiation will be made between the ‘effort of validating’ (= process of validation) a model and a possible resulting ‘valid’ model (= positive result of the process).

Model verification status Verification is done for most of the ecological North Sea models by budget calculations. The conservation of mass is taken as evidence that numerics and coding are correct. Budgets were mostly set up for nutrients, for example for total nitrogen or phosphorus in the three phases of dissolved inorganic matter (DIM), dissolved organic matter (DOM) and particulate organic matter (POM). In nearly all the recent papers on modelling statements were included that conservation of mass was achieved. Conservation of mass is only one possible test for correct numerics and coding. The reproduction of simple analytical solutions of the model equations and of laboratory experiments could provide further test cases. A specific additional verification step would be to simulate special solutions of the equations under defined forcing conditions, as is common in marine hydrodynamics. This has been done for hydrodynamic circulation models (Proctor et al. 1997, Delhez et al. 2004) and for turbulence closure models of stratified water columns (Kraus 1977, Baumert & Radach 1992, Burchard et al. 1998, Burchard & Petersen 1999, Jones 2002). There have apparently been no such attempts for the ecological models of the North Sea. It would be desirable for test cases to be developed and that specific scenarios from previous validational initiatives, as for example on eutrophication studies (OSPAR et al. 1998) or on contaminant transport (OSPAR 1998), be repeated.

Applied validation methods: measuring the goodness of the simulations In this section validation methods used for the comparison of the results of simulations of the North Sea models with observations will be presented.

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Methods of validation used for the results from ecological North Sea models are ranked from qualitative/subjective to quantitative/objective and examples are given of their appearance in the literature. Mostly measures of goodness of fit were used which show the agreement of observations and simulations at a special time instant or for an interval at a certain station or for a box by direct comparison. Statistical measures for the whole region and the whole time interval, for which the simulations were performed, are not yet common. Generally speaking, direct comparisons are used when available data are sparse, and statistical measures demand the existence of datasets which are complex in space and/or time. The most common validation procedure consists in comparing data for observed and simulated parameters directly by visual inspection; this method continues to be the standard method used in most of the papers given in Table 1. The types of the graphical representations may vary. Graphical model validation procedures promote, however, a rather subjective evaluation of the goodness of fit when showing, for example, a continuous line for the simulation and crosses for observations. This method was applied to all timescales from the simulation of time-series on the event scale of some days to weeks as, for example, Kühn & Radach (1997; their Figures 4 and 7–10), to simulations of the full annual cycle first published by Horwood (1982; his Figure 10), as well as to long-term simulations by Los & Bokhorst (1996; their Figure 5), and by Pätsch & Radach (1997; their Figures 10 and 11). For stratified areas a separation into surface and bottom layers was necessary to take account of the differences in the model performance in different depth regimes (Figure 5 in Agoumi et al. 1985). In only a few papers comparisons of vertical profiles for different seasons or regions were shown (Figures 12Ð14 in Gregg & Walsh 1992). For comparisons of the evolution of vertical profiles over the annual cycle, contour plots were provided especially at Ocean Weather Ship positions or at coastal stations with seasonal stratification. This kind of representation is still very common in one-dimensional modelling and was continuously applied to as many state variables as available, for example by Radach (1983; his Figure 8) and by Fasham et al. (1993; their Figure 8). A common method for comparing sparse observational data with the simulation is still to show a table with measured values of process rates found in different references compared to simulated values, for example for cumulated process rates like annual net primary production, sometimes accompanied by illustrations (Figure 11 with table in Moll 1998). The visual comparison of observed and simulated horizontal distributions (Figures 3 and 4 in Pätsch & Radach 1997) and of satellite-derived horizontal features with simulations (Plate 3 in Gregg & Walsh 1992) is common. Three-dimensional simulation models have to use observations which originated from many cruises. The data were usually aggregated into time and space intervals and then averaged, adding statistical information on the standard deviation and the extreme values. Vertical bars indicate monthly means and extreme values of the observations for the annual cycle of different regions (Figures 3 and 5Ð7 in Fransz & Verhagen 1985). When comprehensive datasets became available, this method became more and more common (Figures 4Ð8 in Baretta et al. 1995). Only rarely Box-Whisker plots or similar statistics were used for describing the performance of the model vs. the observations, although there should not be any problem using this method as a standard tool in validation exercises. Several statistical methods are available for measuring the goodness of fit, such as covariance analysis, regression analysis, mean square errors or cost functions. All of them are, however, based on the existence of corresponding datasets. Early attempts of validating complex models made use of methods applied in economics (Radford 1979, Baretta & Ruardij 1987). Radford (1979) made use of control charts to find extreme deviations between simulated and observed concentrations; the method of control charts was derived from manufacture control and assumed that successive deviations were statistically independent (Radford & West 1986), which may not be fulfilled for ecological simulations. The BOEDE model was evaluated by Baretta & Ruardij (1987) using the method by Stroo (1986), who defined an overall measure by using the mean square prediction error, normalised by the sum of squares of

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predicted values; he then transformed this measure into a function ranging in value between 0 (no agreement) and 1 (perfect agreement). Only a few papers used statistical methods such as regression analysis. Sometimes the temporal means and standard deviations of observed data and simulated data were compared and comple- mented by correlation coefficients and root mean square errors, for example by Ishizaka (1990), to quantify the deviation between log-transformed observations and simulated concentrations. The ‘cost function’ is a mathematical function which provides a useful means of comparing data from two different sources, for example model results and observations. The cost function gives a non- dimensional number which is indicative of the ‘goodness of fit’ between the two sets of data. Sometimes the measure is based on the sum of the absolute differences, sometimes on the squares of the differences. For comparing different models of the North Sea, as presented by OSPAR et al. (1998), the definition of a cost function was based on temporal and spatial means, calculated from both observations and results from the model in the same manner. The cost function was defined as the sum of the absolute deviations of the model values from the observations, normalised by the standard deviations of the observations in each spatial unit (box) and temporal interval (season); thus it is a standardised, relative mean error. According to this scheme two cost functions, regional and seasonal, were applied. The normalised deviation between model result and observation for each box (x) and each

season (t) (or more generally: time intervals (t)), Cx,t, was calculated as

MDxt,,− xt Cxt, = , (1) sdxt,

where Mx,t is the mean value of the model results within box x and season t, Dx,t is the mean value of the in situ data within box x and season t, and sdx,t is the standard deviation of the in situ data within box x and season t. The values Cx,t constitute a ‘cost function field (cff)’ when many locations x are given for one time t or a ‘cost function time-series (cfts)’ when many times t are given at one location x.

Then the seasonal cost function Ct for the overall mean of all boxes for one season was defined as follows:

n C ∑ xt, C = x =1 , (2) t n

where Cx,t is the normalised deviation between model and data for box x and season t, and Ct is the normalised deviation for season t, averaged over all n boxes, where data are available.

The regional cost function Cx for the overall mean for all seasons for one box was defined as follows:

m C ∑ xt, C = t =1 , (3) x m

where Cx,t is the normalised deviation between model and data for each box x per each time interval t (e.g., month), and Cx is the normalised deviation per box, averaged over time, with m being the number of time intervals t, for which observations are available. Many of the ecological North Sea models described above in the section ‘Validational efforts for ecological models for the North Sea’ were used in a comparison using these cost functions

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(OSPAR et al. 1998). Not every model could, however, deliver the same cost function application because of restrictions of model setup and performance. This comparison is a main source for judging the goodness of fit of the models. For the purpose of categorising the results, the following (subjective) interpretation of the values of the ‘cost functions (cf)’ to measure the goodness of fit between model and data will be used:

Rating Condition Very good 0 < cf < 1 Standard deviations Good 1 < cf ≤ 2 Standard deviations Reasonable 2 < cf ≤ 3 Standard deviations Poor 3 < cf Standard deviations

This rating is a sharpening of the criteria as proposed by OSPAR et al. (1998) for reasonable (2Ð3) instead of 3Ð5 and for poor (>3) instead of >5. The cost function approach should become a standard method for model validation.

Validational status of the models The evaluation of the validity of the model simulations will be performed according to different spatial and temporal scales. Such an evaluation is possible for four combinations of spatial and temporal scales: 1. For regional distributions (see section ‘Regional distributions’), described by the large- scale structure of the distributions of the state variables in the North Sea, resolved by a box structure, on temporal scales of seasons; 2. For annual cycles (see section ‘Annual cycles’) which were derived for a grid of relatively small boxes over the whole of the North Sea, from climatological averaging of available data per month; 3. For long-term developments (see ‘Long-term developments at specific stations’), for temporal scales up to decades at specific stations with relatively fine temporal resolution; 4. For events (see section ‘Events’) that use special datasets for special model applications.

Regional distributions

For validating regional distributions of phytoplankton parameters and nutrients, datasets of climato- logical seasonal or monthly means are available which are based on the order of 105Ð106 observations per parameter for the whole of the North Sea. One such dataset was provided by the International Council for the Exploration of the Sea (ICES), consisting of long-term averaged, but spatially finely resolved seasonal data (OSPAR et al. 1998); for details see Appendix under ‘ICES dataset’. The validation procedure was performed on five of the twelve models of Table 1 using the same ICES data: CSM-NZB (de Vries et al. 1998), DYMONNS (Hydes et al. 1997), ECOHAM1 (Moll 2000), ERSEM (Pätsch & Radach 1997), NORWECOM2 (Soiland & Skogen 2000). The comparisons were intended to indicate how well the models reproduced the spatial distributions and their gradients in comparison to climatological seasonal average distributions. Only four state variables (chlorophyll, phosphate, dissolved inorganic nitrogen (DIN) and silicate) could be com- pared, because either the models did not deliver other state variables or corresponding data were not available or both. The regional cost function was used for this comparison (see Equation 3); this statistical measure was defined for the entire area for which ICES data exist (see Appendix). The resulting values of the cost functions for chlorophyll and nutrients are given in Table 2.

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Table 2 Comparison of regional distributions for phosphorus, nitrogen, silicate and chlorophyll after the first model comparison study (OSPAR et al. 1998)

Winter Spring Summer Model Simulation year(s) Depth interval (JF) (MJJ) (JAS) Chlorophyll ERSEM 1985 0Ð20 m 3.98 5.27 2.93 ECOHAM1 1985 0Ð20 m 7.61 6.05 2.05 NORWECOM 1985, 1988, 1993 0Ð20 m 2.62 4.06 1.25 ERSEM 1985 20 mÐbottom 7.61 3.36 3.05 ECOHAM1 1985 20 mÐbottom 10.24 3.12 2.14 NORWECOM 1985, 1988, 1993 20 mÐbottom 5.78 2.51 1.68 DYMONNS 1988Ð1989 Depth averaged 4.72 4.84 2.31 CSM-NZB 1985 Depth averaged 5.80 3.70

Phosphorus ERSEM 1985 0Ð20 m 1.03 1.32 1.69 ECOHAM1 1985 0Ð20 m 1.03 1.51 1.90 NORWECOM 1985, 1988, 1993 0Ð20 m 1.38 2.40 3.26 ERSEM 1985 20 mÐbottom 1.09 1.18 0.90 ECOHAM1 1985 20 mÐbottom 1.04 1.99 1.85 NORWECOM 1985, 1988, 1993 20 mÐbottom 1.59 2.90 2.33 CSM-NZB 1985 Depth averaged 2.20 3.70

DIN NORWECOM 1985, 1988, 1993 0Ð20 m 2.50 11.30 23.04 NORWECOM 1985, 1988, 1993 20 mÐbottom 1.83 9.51 14.26 CSM-NZB 1985 Depth averaged 3.90 5.20

Silicate NORWECOM 1985, 1988, 1993 0Ð20 m 1.64 2.21 1.74 NORWECOM 1985, 1988, 1993 20 mÐbottom 1.25 2.64 1.46 CSM-NZB 1985 Depth averaged 1.40 3.40

Notes: The second column describes the simulated years, followed by the selected depth ranges for comparison with surface (0Ð20 m) or bottom (20 mÐbottom) observations. The last three columns describe the values of the cost function for three seasons: JF = January/February, MJJ = May/June/July, JAS = July/August/September. For explanation of the cost function see section on “Applied validation methods: Measuring the goodness of the simulations.”

For chlorophyll all models (CSM-NZB, DYMONNS, ECOHAM, ERSEM, NORWECOM) for the greater North Sea were included in the comparison. The goodness of fit in the upper layer was ‘good’ to ‘reasonable’ only for the summer period, and ‘poor’ for autumn and winter, except for NORWECOM in winter. It is remarkable that no model provided a good representation of the regional chlorophyll distribution in spring. One should consider, however, that climatological mean distributions, as represented by the data used, average out the specifics of the actual distributions (e.g., high spring blooms in different weeks of special years). Therefore, this kind of comparison must be valued with caution. The behaviour of the models could probably be much more realistic than can be seen from this comparison. Phosphorus and silicate distributions were the parameters that gave the best simulations. The goodness of fit was for all seasons ‘good’ to ‘reasonable’ for the models ECOHAM, ERSEM and

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NORWECOM. CSM-NZB provided reasonable winter distributions. Horizontal distributions of inorganic nitrogen (DIN) provided by NORWECOM and CSM-NZB were also compared to the common datasets. The fit was ‘good’ for winter bottom values from NORWECOM, however, the winter distributions in the upper layer were less satisfying for the models CSM-NZB and NORWECOM. For summer and autumn both models failed to reproduce realistic mean seasonal distributions (cf >5). Although ERSEM has the potential to simulate inorganic nitrogen nutrients and silicate, these two parameters were not included in this comparative study. Soiland & Skogen (2000) presented a repetition of the ASMO Workshop comparison (OSPAR et al. 1998) obtained with the updated version 2 of NORWECOM using the ICES dataset (see Appendix). This study provided an extended comparison of the horizontal distributions with mean seasonal long-term averages (again for the period 1980Ð1989) showing maps of the observed and modelled distributions, their differences and the cost function fields according to Equation 1 for the state variables inorganic nitrogen, phosphate, silicate, chlorophyll and oxygen for the surface (0Ð20 m) and below 20 m (Figure 1). The low cost function field values within the interval Ð1 and 1 (except for a few small areas) for predicted temperature and salinity (Figures 2 and 4 in Soiland & Skogen 2000) indicated a proper representation of the climatological mean hydrographic and circulation fields. In contrast to the results published by OSPAR et al. (1998), the surface chlorophyll cost function values (Figure 4, Table 2 in Soiland & Skogen 2000) improved (winter: 1.61, spring: 1.50, summer: 1.17) in comparison to the previous NORWECOM1 version. The chlorophyll and oxygen horizontal distributions of the cost function values exhibited many white areas due to the absence of observations (Figure 1 (B) and (C)). The areas of stronger deviation concentrated on the Dogger Bank region. Also for phosphate the horizontal distributions exhibited large areas between cost function field values of Ð1 to +1 and (small or large) islands of large cost function field values (Figure 1 (E)). Phosphate had the best cost function field values in the surface layer (winter: 0.90, spring: 1.25, summer: 1.50) and silicate followed (winter: 1.44, spring: 0.76, summer: 1.28). Areas of large deviations for the nutrients phosphate and silicate lay off the U.K. coasts and in the Skagerrak. Inorganic nitrogen failed again except for winter values (cf in winter: 1.74, spring: 9.57, summer: 13.60) and eastern North Sea coastal areas, with large discrepancies in the central and northern part of the North Sea (Figure 1 (D)). NORWECOM simulated most of the state variables with good cost function field values for most of the North Sea, but failed for the state variable inorganic nitrogen. The authors attributed the failure to the missing observations of ammonium which were responsible for the discrepancies in the comparison between the model state variable DIN and the observed nitrate, especially in summer surface layers. On a finer regional scale with a resolution of 4 km, the model NORWECOM was applied to simulate the ecosystem in the Skagerrak (OSPAR et al. 1998). The cost function field was deter- mined using data from Skagerrak sections and 25-hour averaged simulated values, interpolated on the computational grid (OSPAR et al. 1998, p. D-4). At sections F and H (for their exact positions see Skogen et al. 1998; Figure 2) the cost function values were determined (Table 3), yielding values for DIN, DIP and silicate between 1.47 and 6.03; the values for salinity and temperature were between 1.97 and 5.36, indicating, in our view, that there was a problem in correctly meeting the actual physical situation. For the ECOHAM model, Moll (2000) gave a detailed presentation of the complete results provided for the comparison during the ASMO Workshop (OSPAR et al. 1998) and presented the North Sea wide spatial variation of the cost function fields according to Equation 1 for chlorophyll and phosphate in the surface layer for the winter, spring and summer seasons. Climatological mean concentrations provided by the ERSEM II and ICES datasets (see Appendix) were compared with a single year simulation for 1985. Phosphate winter values in January and February (Figure 2) in the upper layer were in best agreement with observation (cf = 1.03), but were also good during

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Figure 1 Regional distribution of cost function field values for (A) temperature, (B) surface chlorophyll, (C) oxygen, (D) inorganic nitrogen, (E) phosphate and (F) silicate during May-June-July in the upper 20 m, except for oxygen (20 mÐbottom). The isolines of the cost function values are given for the values Ð3, Ð2, Ð1, 0, +1, +2, +3. The simulation was performed with NORWECOM for 1980Ð1989 and then the results were averaged for the season indicated. (From Soiland & Skogen 2000. With permission from Elsevier.)

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Table 3 Comparison of phosphorus, nitrogen, silicate, temperature, salinity, inorganic suspended matter and chlorophyll for different regions according to the first model comparison study (OSPAR et al. 1998)

a) Regional cost function results for the Belgian-Dutch coast: Location: Terschelling Noordwijk Model State Variable T10 T50 N10 N50 DYMONNS Chlorophyll 0.45 0.64 0.27 1.38 DIN 1.12 2.34 1.18 6.36 total N 0.88 1.61 1.01 4.95 DCM-NZB Chlorophyll 0.38 1.01 0.47 0.67 DIN 1.02 1.53 0.84 2.05 CSM-NZB Chlorophyll 0.18 0.48 0.66 0.50 DIN 0.57 0.86 1.36 1.22

b) Regional cost function results for the Belgian coast:

Model State Variable Belgian CZ MIRO Chlorophyll 0.32 Ammonium 1.49 Nitrate 0.47 Phosphate 1.04 Silicate 0.64

c) Regional cost function results for the English Channel:

Location 1 Location 2 Location 3 Location 4 Location 5 03û53′30″ W 04û5′30″ W 01û35′00″ W 00û07′30″ E 01û21′30″ E Model State Variable 48û46′50″ N 50û0′00″ N 48û41′30″ N 49û26′00″ N 50û49′00″ N ELISE Chlorophyll 0.39 0.98 0.64 0.29 0.87 DIN 0.29 0.57 0.23 0.17 DIP 0.12 0.49 1.38 0.19 Silicate 0.27 0.78 0.50 0.31 Temperature 0.09 0.09 0.11 0.07

d) Regional cost function results for two sections in the Skagerrak:

State Location ModelVariable Section F Section H NORWECOM Salinity 5.36 1.97 Temperature 4.54 3.47 DIN 2.15 6.03 DIP 2.12 2.97 Silicate 4.87 1.47

spring (cf = 1.51) and summer (cf = 1.90). During summer there was most deviation in the bottom values due to a fast remineralisation at the bottom. Chlorophyll showed good agreement only in the summer (cf = 2.05, Figure 5 in Moll 2000); it was overestimated by the simulation in coastal

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61

60

59 NORWAY SWEDEN

58

57 SCOTLAND

DENMARK 56

55

54 GERMANY

THE NETHERLANDS 53

ENGLAND 0.00 - 0.50 WALES 52 0.50 - 1.00 BELGIUM 1.00 - 1.50 51 1.50 - 2.00 2.00 - 2.50 50 FRANCE 2.50 - 3.00

Institute für Meereskund > 3.00 49 Unversitat Hamburg

-5 -4 -3 -2 -1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14

Figure 2 Absolute cost function field values of surface phosphate in January and February simulated by ECOHAM1. (From Moll 2000. With permission from Elsevier.)

areas in winter (cf = 7.61) and in the central North Sea in spring, resulting in high cost function values (cf > 6). The bloom was well simulated in the northern North Sea. The comparison between the variability of primary production estimates for 10 years from both, ECOHAM and NORWECOM (Skogen & Moll 2000, 2005) gave the important results that the variability in primary production was similar for the two models in each of the areas inspected and that the regional variations were larger than the differences between the two models (Figure 3). For the ERSEM model (130-box version) a regional comparison was performed on a decadal timescale. From the long-term simulation Pätsch & Radach (1997) derived a decadal mean of the simulation results for the period 1984Ð1993 in the same way as for observations for phosphate and nitrate in the upper 30 m. For both parameters the regional distribution of the observations (Figure 4) exhibited a higher level of concentrations, especially in the coastal areas where the rivers Rhine and Elbe enter, degrading toward the central North Sea, where the concentration levels were quite well mapped. This may indicate that either the river inputs were too low or that the conversion of the nutrients in the coastal sea was not adequately modelled.

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Figure 3 Annual mean production and its standard deviation for each individual ERSEM box, based on simulation runs with the NORWECOM and ECOHAM1 models for the years 1985Ð1994. (From Skogen & Moll 2005. With permission from Elsevier.)

In five areas of the English Channel the results of a simulation for 1980 with the ELISE model (Hoch & Garreau 1998; Figure 6) were compared to phytoplankton nitrogen observations mainly collected from 1975Ð1984. The spatial variations were reproduced as observed for the spring bloom period, but seem to be underestimated for the summer period. A comparison of the simulation from the MIRO model (Lancelot et al. 1997; Figures 6 and 7) for the French, Belgian and Dutch coastal zones showed that the observed range of concentrations of chlorophyll and the nutrients (nitrate, phosphate and silicate) between 1988 and 1993 could be reproduced grossly. The strong north-south gradient along the continental coast was well reproduced. Bokhorst & Los compared their simulation using the CSM-NZB model for winter 1985 (Figures 6.1Ð6.4 in Bokhorst & Los 1997) with the observed horizontal distributions provided by the ERSEM II dataset (see Appendix). The simulation reproduced the coastal to central North Sea gradient for all nutrients (nitrate, phosphate and silicate) in winter. The comparison for chlorophyll in May 1985 illustrated that the model was able to reproduce the high chlorophyll concentrations in the continental coastal strip, but overestimated the typically observed concentrations in the central and northern North Sea (Figure 5). The comparison of the simulation from the DCM-NZB model with long-term mean data from the Dutch monitoring programme covering the years 1975Ð1995 (de Vries et al. 1998) concentrated on the phosphate, DIN and chlorophyll along the Noordwijk transect off the Netherlands (Figure 6). The overall near-shore gradient (0Ð70 km) was reproduced well for chlorophyll, DIN and phosphate, except for phosphate and chlorophyll within the first 5 km off the coast, where the concentration of chlorophyll was overestimated and phosphate was underestimated by the simulation. For the GHER model only primary production values were compared (Delhez 1998); the right level of primary production was met in ICES box 4 (Netherlands coast); observations of primary

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(A) Hindcast: 1984 – 1993 (B) Observations: 1984 – 1993

(C) Hindcast: 1984 – 1993 (D) Observations: 1894 – 1993

Figure 4 Horizontal distributions in the surface waters (0Ð30 m) for (A) simulated and (B) observed phosphate and (C) simulated and (D) observed nitrate in winter (December, January, February) as means over the years 1984Ð1993 (in mmol mÐ3); the simulated values resulted from the 40-year long simulation with the 130-box- version of ERSEM. (From Pätsch & Radach 1997. With permission from Elsevier.)

production were underestimated in ICES boxes 1 (northern North Sea), 2b (Shetland Channel inflow area) and 5 (German Bight), and overestimated in ICES boxes 3a (Scottish coast), 3b (English coast), 7a (central North Sea) and 7b (Dogger Bank).

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(A) (B)

ERSEM130.MAP NZBLOOM.MAP >8 >8 >4 >4 >2 >2 >1 >1 >0.5 >0.5 >0.25 >0.25 >0 <=0.25 <=0

Figure 5 Comparison of (A) observed and (B) simulated chlorophyll (µg lÐ1) in May 1985; the data are part of the ERSEM dataset of climatological monthly means; the simulation was performed with the CSM-NZB model. (From Bokhorst & Los 1997.)

A series of corresponding maps was given for the southern North Sea, presenting horizontal distributions of dissolved nitrate, ammonia, oxygen and chlorophyll obtained from observations during the NERC NSP project (see Appendix) in 1988Ð1989 and from a simulation with DYMONNS by Hydes et al. (1997). Nitrate distributions resembled each other in February, but deviated grossly by May because too much nitrate was still available in the continental coastal areas. In August nitrate was rather depleted in both distributions, but built up in the simulation much faster than shown by the observations, thus yielding stronger horizontal gradients than were realistic. The observed and simulated ammonia distributions were similar to each other; the obser- vations tended to be higher than the simulations thus creating larger gradients. In November, however, the observed situation during 1988 was very different from the simulated one, showing very high concentrations of >8 µM of ammonia along the Danish coast. The chlorophyll distributions resembled each other rather well in February and May (Figure 7), when the observations were somewhat higher than simulated. In August, however, chlorophyll concentration was much too high in the Southern Bight compared to observations in 1989, but disappeared totally by November, which was different from nature. Oxygen was met by the simulation within an order of magnitude. The simulation of primary production over the year in four ICES boxes (Figure 3.3 in Hydes et al. 1997) showed that the simulated horizontal gradient differed from the observed gradients; generally the simulated primary production was too high, except for ICES box 5 (German Bight).

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50 30 ) –1 25

) 40 –1 20 30 15 20 10 10 DIN (µmol l 5 DIN:DIP (mol mol l

0 20 40 60 80 0 20 40 60 80

20 2.5 ) –1

) 2

–1 15 1.5 10 1

0.5 DIN (µmol l 5 Chlrorphyll (µg l l Chlrorphyll

0 20 40 60 80 0 20 40 60 80 Km off the coast Km off the coast

Figure 6 Comparison of long-term annual averages of DIN, DIP, DIN:DIP ratio and chlorophyll along the Noordwijk transect (dots), based on a simulation (bars) with the DCM-NZB model over the 20-year period 1975Ð1994. (From de Vries et al. 1998. With permission from Elsevier.)

The findings are summarised as follows:

1. The reproduction of the mean seasonal distributions and their horizontal gradients can be simulated for homogeneous and stratified waters in coincidence with climatological observations for many state variables, best for the nutrients phosphate and silicate, less well for nitrate and ammonia, and good to reasonable for chlorophyll. 2. Several models failed to meet the concentrations of chlorophyll for the important spring period. However, a comparison of climatological mean data with simulations of a special year implies obvious problems because of the mismatch of scales, and the models could possibly perform better than these data suggest. 3. No model achieved a good coincidence with data for the regional distributions of all state variables; in all model systems at least one state variable failed during a certain period. 4. The differing gradients in long-term averages of distributions for simulated and observed phosphate and nitrate indicated problems in modelling the dynamics in regions of direct influence of river input. 5. It became evident (what was known before) that a proper representation of the environ- mental physical situation is necessary for achieving a proper representation of the eco- system dynamics.

Annual cycles

Most work has been done on validating the annual cycles of the basic ecological state variables. Again the results from the OSPAR Workshop (OSPAR et al. 1998) are reported first, as a reference for the work building on these results. Four of the eleven models of Table 1 were used in this

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Figure 7 Comparison of simulated (left panels) and observed (right panels) chlorophyll distributions in the Southern North Sea during the months February, May, August and November; the simulation was performed with the DYMONNS model, the data are from the NERC NSP dataset. (From Hydes et al. 1997.)

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comparison: CSM-NZB (de Vries et al. 1998), DYMONNS (Hydes et al. 1997), ECOHAM1 (Moll 2000), ERSEM (Pätsch & Radach 1997). The comparison of the simulated annual cycles from several models to a common dataset was only performed for the state variable chlorophyll. The dataset used for this comparison (OSPAR et al. 1998) was the ERSEM II dataset which provided averaged values for 1¡ × 1¡ boxes as climatological monthly means for each of the 130 ERSEM boxes (Radach & Pätsch 1997); for details see under ‘ERSEM datasets’ in the Appendix. Five of these areas (boxes 21, 52, 57, 70 and 81) were selected for the comparison (OSPAR et al. 1998). For their position and the horizontal resolution see Figure 21. The resulting cost function values according to Equation 1 are illustrated for the outer German Bight and the Rhine plume areas (ERSEM boxes 70 and 81), respectively, in Figure 8. Large differences in the cost function values between Ð4 and +16 occurred for the German Bight and between Ð3 and +5 for the Rhine plume

Figure 8 Cost function values for chlorophyll simulated by the CSM-NZB, DYMONNS, ECOHAM1, ERSEM models in two areas: (A) in the outer German Bight (ERSEM box 70) and (B) off the river Rhine (ERSEM box 81), (from OSPAR et al. 1998); for the box structure see Figure 21 (ERSEM 130-box version).

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during winter time and early spring (January, February and March); for the rest of the year the range was reduced to ± 2 standard deviations. The performance of the ERSEM model turned out to be best for both regions. The DYMONNS (Hydes et al. 1997), DCM-NZB and CSM-NZB (de Vries et al. 1998) models were also tested against the dataset from the Dutch monitoring programme on the Terschelling (T10 and T50), and Noordwijk (N10 and N50) sections, each 10 and 50 km off the Dutch coast, respectively (Table 3). The DCM-NZB and CSM-NZB models were run with input for 1985 and compared to the mean annual time-series from the period 1975Ð1993. The DYMONNS model was run for the years 1988Ð1989 and was compared to data from that period. For the DCM-NZB and CSM-NZB models the cost function attained values less than 2.1 at all four stations for chlorophyll (0.18Ð1.01) and DIN (0.57Ð2.05). The DYMONNS model yielded similar values for chlorophyll, DIN and total N, except for station N50, where the fit was not satisfactory for the nitrogen compounds. The DCM-NZB and CSM-NZB models were well calibrated according to these well- established datasets and the authors used ‘own’ cost functions, which allowed them to reach lower cost function values by multiplying the cost function from Equation 3 with a factor expressing the goodness of the correlation between simulation and data (OSPAR et al. 1998). In addition to this comparison of the models and partly as a follow-up, for these four models and for most of the other models from Table 1, validational efforts concerning the annual cycles were presented in various publications. The environmental status of the Skagerrak and the North Sea for the years 2000 and 2001 was simulated with NORWECOM mostly using actual forcing data, and the results were compared to data from the Torungen-Hirtshals section from the same years (Skogen et al. 2002, 2003). At stations 230Ð235 in 2000 and 2001 observed temperature and salinity were well met by the simulations, but were less successful at the other three sections. “The results for silicate, phosphate and dissolved inorganic nitrogen vary between the different water masses” (Skogen et al. 2002). The results of the simulation coincide more or less with observations made during the annual cycle. Mostly they are highly correlated, but during 2000 there were often systematic shifts in their concentration levels, for example for DIN 1Ð3 units, for silicate 1Ð3 units, for phosphate 0.1Ð0.2 units. The deviations seemed to be more random during 2001. In a first attempt the results from the simulation using the ECOHAM model (Moll 1998) under forcing from 1986 were compared on the basis of simulated values averaged for the 15 ERSEM- I-boxes and the corresponding ERSEM I dataset (see Appendix). The high winter values of phosphate as well as its summer depletion in the stratified North Sea were very well reproduced. In coastal areas the simulated phosphate concentrations were within the band of the highly variable observations, but the model failed to reproduce the phosphate concentrations near the bottom in shallow coastal areas (ERSEM-I-boxes 8, 14, 15); there they remained too high (Figure 9A). The chlorophyll blooms were well simulated only for the northern North Sea (Figure 9B). The simulation overestimated the bloom in the central North Sea. In coastal areas the timing of the bloom was 1 month too early. Simulated primary production lay within the observed range (Figure 7 in Moll 1998). In a second attempt at a comparison, conducted at the ASMO workshop (OSPAR et al. 1998), Moll (2000) compared the annual cycles obtained from a simulation for 1985 to the corresponding data from the ERSEM II datasets, with a regional resolution of the 130 ERSEM-II- boxes (see Appendix). Phosphate winter values were in good agreement with observations (cf = 1.0Ð2.0), however, during spring and summer the bottom values were not well modelled. A remaining difficulty of the model, however, was to correctly calculate the winter and early spring chlorophyll concentrations in some of the boxes; for the remainder of the year the fit was good (see Table 2 in Moll 2000). In summary, both studies showed that phytoplankton chlorophyll, phosphate and primary production were in good agreement with climatological observations, except for phosphate in the

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Figure 9 Annual cycles simulated by the ECOHAM1 model, compared to climatological monthly mean observations (medians and 17% and 83% quantiles) from the ERSEM dataset; for (A) phosphate in all 15 boxes and (B) chlorophyll in the 10 upper ERSEM boxes. (From Moll 1998. With permission from Elsevier.)

shallow areas in late summer and early winter, due to the simple parameterisation of the regeneration of bottom detritus. It should be noted that the cost function values were lower when smaller time intervals for averaging were used (months compared to seasons).

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Luff & Moll (2004) supplemented the pelagic system model ECOHAM1 (Moll 1998) with a high-resolution diagenetic model C.CANDI for the North Sea sediments (Luff et al. 2000) and simulated the annual cycles of the pelagic variables as well as the sediment dynamics and the resulting water-sediment fluxes for the year 1986. The annual cycles of phosphate and chlorophyll (Figure 3 in Luff & Moll 2004) were only little changed, compared to the annual cycles simulated by the model ECOHAM1 including only rudimentary sediment dynamics (Moll 1998). The spring decay of phosphate was a little steeper (in box 4), depletion was a little less in summer (box 1), regeneration retarded in late summer (boxes 4 and 7) and the spring bloom was mostly shifted by 1 month into May, which was more realistic, although the magnitude of the bloom was overesti- mated. The penetration depths of oxygen and nitrate in the upper centimetres of the sediment coincided well with the very sparse observations from August 1991 and February 1992. The extension of the model did not give a better coincidence of the pelagic variables with observations, but it now allows the estimation of the sediment-water fluxes over the whole North Sea area. The ERSEM model is the most thoroughly tested ecosystem model. At first a 15-box version (see Figure 21) of the model (ERSEM I) was set up, where the boxes have dimensions of several hundred kilometers. Validation efforts for this version of the model showed deficiencies which were assessed by refining the spatial structure to a 130-box version of the model (ERSEM II), where the boxes have dimensions of 1û latitude and 1û longitude. It was clear that this model was not able to adequately map the estuaries and their inflow of nutrients from the land, and a coastal application of ERSEM was developed, called COCOA, which is a 138-box version, using smaller boxes in the southern North Sea and along the coasts. The validational efforts for these three versions are discussed below. The 15-box version of the ERSEM model, driven with forcing data from 1988Ð1989, was able to reproduce the observed annual cycles of the nutrients nitrate, phosphate and silicate within an order of magnitude, the timing of the spring bloom as well as the depletion phase (Baretta et al. 1995, Radach & Lenhart 1995). The regional differences of the annual cycles as given by the ERSEM I datasets (see Appendix) were captured quite well by the model, as the examples for phosphate and nitrate showed (Figure 10). The large ranges of variability of the climatological monthly means included the simulated annual cycles of phosphate and nitrate in many boxes for a number of months, but there were systematic features which should be noted. Winter values of phosphate in the northern and central North Sea (boxes 1,11,2,12, and 4,14,5,15) were overesti- mated, and late summer regeneration occurred too fast (boxes 3,4,5,8,15). The observed depletion of nitrate in the summer was not reached in a few regions (boxes 4,5,6,8), and possibly regeneration was too fast in some regions (boxes 3,5,10,15). In resolving the coastal gradients from the river Rhine to the central North Sea by finer than 1û boxes, the (138-box) COCOA version of the model, also driven with forcing data from 1988Ð1989, met the summer concentrations of phosphate and silicate in the southern central North Sea (Figure 11), but failed to reproduce winter concentrations further off the coast (box 82), where the simulated nutrients phosphate and nitrate were much higher than the observations. This might indicate overestimated riverine input data, which would then lead also to overestimated nutrient and chlorophyll concentrations (Lenhart et al. 1997). It is remarkable that a comparison of the annual cycles from the simulation which was driven by river load data from 1989 with monthly data from 1988Ð1989 (obtained from the NERC NSP dataset, see Appendix) instead of climatological data yielded a much better agreement for nitrate, silicate and ammonium (Baretta-Bekker et al. 1997). Chlorophyll values were simulated correctly in the Rhine area, but were underestimated in the more northerly areas of the Southern North Sea. A detailed validational test of annual cycles for phytoplankton groups was given by Ebenhöh et al. (1997; their Figure 2), discriminating diatoms, flagellates and total chlorophyll. Chlorophyll cycles were reproduced within an order of magnitude, but the comparison of simulated and observed

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ations (medians and es. (From Radach & Lenhart 1995. With permission from Elsevier.) permission With es. (From Radach & Lenhart 1995. Annual cycles simulated by the ERSEM I (15-box version) model compared to climatological monthly mean observ simulated by the ERSEM I (15-box version) Annual cycles quantiles) from the ERSEM dataset; for (A) phosphate and (B) nitrate in the 15 ERSEM box Figure 10 Figure

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GÜNTHER RADACH & ANDREAS MOLL (D) chlorophyll in the boxes (D) chlorophyll o years — 1988 and 1989 — compared to climatological monthly o years — 1988 and 1989 — compared to climatological vier.) Annual cycles simulated by the COCOA model (138-box version of ERSEM) for tw model (138-box version simulated by the COCOA Annual cycles mean observations (medians and 17% and 83% quantiles) from the ERSEM dataset; for (A) phosphate, (B) silicate, (C) nitrate and mean observations permission from Else With al. 1997. 91, 82, 64 (see Figure 21). (From Lenhart et Figure 11 Figure

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diatoms and flagellates was problematic for various reasons. The data do not show spring blooms for chlorophyll, diatoms or flagellates; this may result from the climatological averaging and shows the limitations of such a comparison. Baretta-Bekker et al. (1997; their Figure 2) compared microzooplankton and hetero-flagellates to the available data from the British Oceanographic Data Centre and found a general fit within an order of magnitude, with very large variability of the sparse observations. ERSEM was applied to the Humber plume area (Allen 1997) with a validational step at two survey sites for the annual cycles of the nutrients phosphate, nitrate and silicate, the phytoplankton groups of diatoms and flagellates, chlorophyll, suspended particulate matter and micro- and meso- zooplankton. The annual cycles of nutrients and chlorophyll were well reproduced, but diatoms, flagellates and microzooplankton were not convincing, because the simulated large spring blooms and the corresponding increases in zooplankton biomass were not seen in the data. Mesozooplankton observations exhibited a clear seasonal cycle which was well reproduced by the model. In most comparisons the simulated results and observations represent different time and space scales (e.g., simulated instantaneous values vs. climatological monthly means; simulated box means vs. point observations at a station). Pätsch & Radach (1997) compared results from a 40-year-long simulation (1955Ð1993) using ERSEM II with observations for the same scales when they averaged 40 years of simulated time-series for phosphate, nitrate, silicate and chlorophyll and all correspond- ing observations from 1955 to 1993 per box and month. The results of this procedure for a few areas (boxes 31, 46, 58, 69, 65, see Appendix) showed that the statistics for simulation and observation differed in several remarkable features (Figure 12). The simulation produced noticeable mean spring blooms in contrast to the observed means. The annual cycles of simulated phosphate showed a clear summer depletion not found in the mean observations. On the other hand, nitrate, showed a good coincidence of both means. The results provided evidence that the natural mean state and its variability were still different from the simulated states in several aspects. ERSEM I was used by Ruardij & van Raaphorst (1995) to analyse the annual cycles of the sediment dynamics of the North Sea by comparing them to sparse observations in the German Bight (box 9). The seasonal variations of the oxygen and nitrate penetration depths were reproduced in the right order of magnitude. Profiles of phosphate, ammonium and nitrate, shown for February and August, were in the right order, sometimes larger, sometimes smaller than observations in the upper few centimetres; the same applied to the nitrogen and phosphorus fluxes. Without more data a validation of the sediment module could not be done. For the POLCOMS-ERSEM model (Allen et al. 2001) the simulated results for the year 1995 were compared to observations of nitrate, phosphate and silicate at two sites of the NERC NSP project (Figure 13). Annual cycles were reproduced satisfactorily at both sites, except for the overestimation of winter nitrate and silicate concentrations at the shallow station and a decreasing silicate regeneration at the deep station. Both phosphate and silicate regeneration in summer and autumn seemed to be too weak at these stations. Chlorophyll, diatom and flagellate concentrations were in the range of observations. Higher trophic levels, however, like heterotrophic flagellates, microzooplankton and mesozooplankton exhibited severe discrepancies during spring and/or sum- mer periods. Proctor et al. (2003) simulated fluxes and budgets for the northwest European shelf using the POLCOMS-ERSEM model, for the year 1995. The simulated results were compared to estimates calculated from other models as well as observations. The estimated nutrient fluxes, using different procedures for their calculation, vary significantly. The estimates for the northern North Sea and for the Dover Strait were lower than the estimates of other authors (see Table 2 in Proctor et al. 2003). The estimates are, however, influenced by the method of flux calculation, and it is not possible to decide which estimates were more realistic; at the present time there are no ways of measuring the nutrient fluxes directly to validate the estimates from the model. Ideally, the estimates

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Figure 12 Hindcast simulation using the ERSEM II model (130-box version) for the years 1955Ð1993: observed and simulated annual cycles of (A) phosphate, (B) nitrate, (C) silicate (in mmol mÐ3) and (D) chlorophyll (in mg mÐ3) in the boxes 31, 46, 58, 69 and 65. Simulation results and data were average in the same way over each of the 12 months for all years. (From Pätsch & Radach 1997. With permission from Elsevier.)

obtained directly from the coupled simulation should be preferable, if the model was validated (e.g., by nutrient and chlorophyll distributions). The very complex POLCOMS-ERSEM model simulation needs more work to check its validity.

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Figure 13 Simulation of the annual cycles of nitrate, phosphate, silicate, diatoms, flagellates, chlorophyll, heterotrophic flagellates, microzooplankton and mesozooplankton with the POLCOMS-ERSEM model (A) at station CS (55û30′N, 0û55′E) and (B) at station AB (52û42′N, 2û25′E), compared with data from different sources. (Reproduced from Allen et al. 2001. With permission from Taylor & Francis.)

The COHERENS model was based on the water column process model by Tett & Walne (1995); only for the one-dimensional model did the authors try a validation for three stations over the annual cycle, which were measured during the NERC NSP project (see Appendix). For temperature the average deviation in summer was <2ûC; the agreement was better for stratified than for mixed areas; simulated surface temperature was generally higher than observed values. Observed attenu- ation coefficients were reproduced within an order of magnitude. The chlorophyll concentrations matched the observed bloom periods with an overestimation of the simulated spring bloom. Deficits in the physical simulation may cause the other deficits, as biological dynamics are sensitive to developments in the physical forcing, as shown by Eigenheer et al. (1996).

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Lee et al. (2002) reduced the COHERENS model to a one-dimensional version (PROWQM), then extended this version of the model by adding new pelagic and benthic components for coupling the physical and microbiological processes in the water column with sedimentation/resuspension and benthic mineralisation processes. They compared their simulations for the northern North Sea with several new and historic datasets as well as the results from models, concluding that resus- pension, pelagic and benthic mineralisation and denitrification were important processes which need further investigation before they can be properly modelled. There is no validation yet available for the three-dimensional version of the COHERENS model. The NERC NSP dataset for the southern North Sea (see Appendix) was also used for a comparison with the results from the DYMONNS model. Only very few state variables were presented by Kelly-Gerreyn et al. (1997) and Hydes et al. (1997) from a simulation for 1989. An annual cycle for total pelagic dissolved nitrogen content of the water column, without giving its location in the southern North Sea, and annual cycles of primary production in the ICES boxes 3b, 4, 5 and 7b were given (Figures 3.3 and 3.4 in Hydes et al. 1997). The spring depletion and the low summer content were reproduced, but the observed high winter content of nitrogen was not; in autumn the simulation overestimated the observations. Simulated primary production was grossly overestimated in May in all ICES boxes, resulting in annual primary production values that compare well with estimates from observations only in ICES box 4, but not in the other boxes. The same simulation was used during the ASMO workshop as reported in OSPAR et al. (1998). The cost function, which was determined at stations N10, N50 and T10, T50 (Table 3), behaved well for

chlorophyll (0.45 ≤ cf ≤ 1.38), DIN (1.12 ≤ cf ≤ 2.34, except for N50), and Ntot (0.88 ≤ cf ≤ 1.61, except for N50). Delhez (1998) gave values of annual primary production for the ICES boxes which were derived from his 10′ × 10′ resolution model; the values were in the range of results from other models, yielding a mean primary production of 150 gC mÐ2 aÐ1, which is realistic. A thorough validation still seems to be necessary. Concerning the ELISE model for the English Channel simulated results for nitrate, silicate and phytoplankton nitrogen content were tested on the basis of annual cycles for distinct regions of the Channel (Menesguen & Hoch 1997). Nutrient cycles were reproduced for all regions, with an underestimation only for shallow bays. The seasonal variations of phytoplankton were reproduced quite well, with sometimes overestimated summer concentrations. This fact holds also for an improved version by Hoch & Garreau (1998). Menesguen & Hoch (1997) gave comparisons of a simulation with the ELISE model for five areas in the English Channel (Figures 2Ð7 in Menesguen & Hoch 1997). The areas have very different characteristics, ranging from the early stratified north- western English Channel off Plymouth (A) via the deep frontal western coastal zone off Brittany (B) to the shallow coastal areas of the Normand-Breton Gulf (C) and the Bay of Seine (D), and finally the central zone of the Strait of Dover (E). The surface temperature field was met within ± 2ûC. The quality of the simulation varied with the area and differed between parameters and seasons. For inorganic nitrogen the agreement was good in region A and E; in regions C and D it was grossly underestimated in summer. The spring decrease happened rather early in region E. Silicate was simulated too low in winter in region E; it was too low all year round in region C, and in summer and autumn in region D. Phytoplankton nitrogen was well simulated in regions A, C and D; in E the spring bloom was met, but summer values were much higher than observed. For the simulation of annual cycles with ELISE (Menesguen & Hoch 1997) cost function values were given for the five areas AÐE in (OSPAR et al. 1998) in relation to available data (Table 3); the fit seems very good, showing cost function values of 0.12 (for DIP) and 0.98 (for chlorophyll) at site A off Plymouth. The modification of the model into a simplified three-dimensional model (Hoch & Garreau 1998) resulted in annual cycles of phytoplankton nitrogen which differ considerably from those shown by Menesguen & Hoch (1997); the spring bloom was met in four regions; in the Bay

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Figure 14 Simulation of the annual cycles of surface phytoplankton nitrogen by the box model ELISE (dashed line) and by the pseudo-three-dimensional model ELISE (solid line) at five stations AÐE in the English Channel, compared to data (squares). (From Hoch & Garreau 1998. With permission from Elsevier.)

of Seine the simulation of phytoplankton was better simulated by the simpler box model (Figure 14). However, the underestimation of summer phytoplankton in regions C and D and its overesti- mation in region E remained. For the MIRO model validational exercises in the Dutch, Belgian and French coastal zone were presented by Lancelot et al. (1997). Observations of nutrients, phytoplankton chlorophyll and Phaeocystis cell counts from 1988Ð1993 were compared to the results of a simulation driven by input data from 1985. Nitrate and silicate simulations met the observed concentration levels in late winter (Figures 6 and 7 in Lancelot et al. 1997). For nitrate the depletion phase was reproduced in the Dutch and French coastal zone, but not for the Belgian coastal zone. For silicate the simulated values increased too early in spring, and the summer concentration was overestimated. The phos- phate simulation was outside of the observed ranges for the whole annual cycle in the Dutch coastal box. Simulated chlorophyll reached the right magnitude and timing, except for the Dutch coastal zone, where the bloom started one month too late and where the decay of the spring bloom was lacking. The general agreement for Phaeocystis blooms was reasonable in timing and magnitude. The model did not properly predict the fast decline of the Phaeocystis blooms, especially in the Dutch part of the simulated area, where it grossly overestimated the summer concentrations.

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The results from the DCM-NZB model driven by nutrient inputs from 1987 were compared with nutrient and chlorophyll data from the Dutch monitoring programme for several annual cycles obtained at the Noordwijk section and with oxygen data for 3 years obtained at the Terschelling section off the Dutch coast (Peeters et al. 1995). The simulation met the range of the winter concentration data and reproduced the spring depletion. Chlorophyll concentrations in spring and summer were in the observed range; winter concentrations seemed to be underestimated. The annual cycle for oxygen was reproduced, with a retarded decay of oxygen in the simulation of the surface mixed layer in summer. Los & Bokhorst (1997) presented a simulation using the coastal zone version of the DCM- NZB model where the nutrients nitrate, phosphate and silicate behaved more realistically at N10 and T4 during the autumn. De Vries et al. presented results for the near shore stations up to 4 km off the coast (stations N2 and T4) where the simulation coincided well with the averaged data (Figure 12 in De Vries et al. 1998). However, at station N2 chlorophyll was lower and phosphate higher than observed. Bokhorst & Los (1997) have reported on the comparison of a simulation with the CSM-NZB model driven by nutrient inputs from 1985 with data from the Dutch monitoring programme during 1975Ð1995 at the stations of the Noordwijk (2, 10, 50 km off the Dutch coast) and Terschelling (4, 10, 50, 235, 275 km off the Dutch coast) sections. The data were compared as values of about 5-year-averages (1975Ð1980, 1981Ð1985, 1986Ð1990, 1991Ð1995). Generally, the simulation lay within the range of observed average values for the nutrients (Figures 6.7Ð6.27 in Bokhorst & Los 1997). Simulated chlorophyll was higher than that observed in summer at N10 (Figure 15A), at T235 and T275. At several stations the increase of nutrients in autumn was either underestimated (nitrate, phosphate (Figure 15B,C), silicate at N10) or overestimated (nitrate and phosphate at N50). Summarising the attempts to validate the simulated annual cycles, nearly all three-dimensional models have been tested with climatological monthly mean data, representing the annual cycle. The following conclusions can be drawn, which turn out to be almost identical to the conclusions from comparing regional distributions:

1. The comparisons of simulated and observed annual cycles showed that for the most part the nutrients phosphate and silicate were simulated best, but there was less success with nitrate or nitrogen nutrients. Chlorophyll was simulated within an order of magnitude, sometimes over-, sometimes underestimated. However, large differences between the models occurred in the cost functions (e.g., for chlorophyll) when models were compared to a common dataset. 2. The phasing of nutrients and chlorophyll showed differences compared to the data mainly at times of intense regeneration of nutrients, which has so far not been satisfactorily modelled. 3. The discrepancies between simulation and data increased with the trophic level. 4. The regional differences of the annual cycles of nutrients, chlorophyll and primary production could be reproduced quite well. 5. The quality of the simulated annual cycles varied with parameter, area and season. There is no one model for which all simulated state variables coincided with climatological monthly means in all seasons. 6. The comparisons suffered from the fact that data and results from simulations usually represented different time and space scales. This may lead to false interpretations. 7. It appears that the levels of nutrients were sometimes calibrated in favour of coastal areas vs. open sea areas, and vice versa, to meet the annual cycles in the area of interest, thereby shifting discrepancies to the areas that were not the focus of the investigation.

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(A) [ug/l] 45 40 35 30 25 20 15 10 5 0 00-01 30-01 29-02 30-03 29-04 29-05 28-06 28-07 27-08 26-09 26-102 5-11 25-12

a) CSM 1985 d) 1986 - 1990 e) 1986 - 1990 f) EUZOUT

(B) [mg/l] 1.4

1.2

1

0.8

0.6

0.4

0.2

0 00-01 30-01 29-02 30-032 9-04 29-05 28-06 28-07 27-08 26-09 26-10 25-11 25-12

a) CSM 1985 d) 1986 - 1990 e) 1991 - 1990 f) EUZOUT

(C) [mg/l] 0.16

0.14

0.12 0.1

0.08 0.06

0.04

0.02

0 00-01 30-01 29-02 30-03 29-04 29-05 28-06 28-07 27-08 26-09 26-10 25-11 25-12

a) CSM 1985 d) 1986 - 1990 e) 1991 - 1990 f) EUZOUT

Figure 15 Simulated annual cycles for (A) chlorophyll, (B) nitrate and (C) phosphate at station Noordwijk, 10 km off the Dutch coast, using the CSM-NZB model, compared to monthly averages for 5-year periods and data from the project EUZOUT. (From Bokhorst & Los 1997).

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8. The few examples where the pelagic model was extended by a benthic model showed that the extension did not necessarily substantially improve the outcome. Special attention should be devoted to the regeneration mechanisms at the bottom, especially in shallow areas, where most of the models seem to have problems in correctly describing the regeneration of nutrients. 9. There are serious data needs. Apart from the NERC North Sea Project (NSP) 1988Ð1989 data, no comprehensive datasets exist for testing the models for one specific year. Observations during full annual cycles are especially needed for validating submodules of benthic and pelagic regeneration mechanisms. Common datasets are also needed for actual annual cycles of forcing functions.

Long-term developments at specific stations

Comparisons of long-term simulations with data were performed using the ERSEM, ELISE and DCM-NZB models. For validating long-term simulations a relatively good database was provided by the EU-MAST project NOWESP (Radach et al. 1996, Visser et al. 1996), which provided time- series from coastal stations suited for such comparisons; unfortunately no offshore stations were available (see Appendix). Pätsch & Radach (1997) compared their long-term simulation (1955–1993) with the time-series of monthly means from the NOWESP datasets. They included a statistical analysis of the observed and simulated variability on several timescales (Table 7 in Moll & Radach 2003). Generally, quite a number of long-term features were reproduced. As an example, the results for Dutch coastal waters (Figure 10 in Moll & Radach 2003) and for the area around Helgoland (Figure 16) are discussed here. In both regions the long-term changes in the observations were reproduced at least qualitatively by the simulation. The visual evaluation of the comparison (Figure 16) was supported and supple- mented by a statistical analysis, which was carried out for both stations (see Tables 4–6 in Pätsch & Radach 1997, or Moll & Radach 2003), yielding the following results. Mean levels of observation were rather close to the simulated ones. The mean annual, winter and summer levels were reproduced for some, but not for all basic state variables investigated (phosphate, nitrate, ammonium, silicate, chlorophyll, diatoms, flagellates). There was, however, seasonal variation of the degree of coinci- dence. For example, the state variables yielded a good simulation for the mean annual and mean winter levels of phosphate for both regions, but this was not valid for the summer levels, where the observations showed a deeper depletion than did the simulation. For silicate and nitrate the mean annual levels were well simulated, but not the mean winter levels, which were higher or lower than observed, and the mean summer levels, which were lower than observed. Thus, for the nutrients silicate and nitrate the depletion in summer developed too strongly, and for phosphate too weakly in the simulation. The annual means of chlorophyll (NOWESP site 5-3) and diatoms (NOWESP site 6) as well as their summer levels were met by the simulation, but not the winter levels. The levels of flagellates at NOWESP site 6 were overestimated in summer and underestimated in winter. Primary production agreed with the sparse observations. The variability measured as standard deviations of annual, winter and summer levels obtained from the simulation were mostly smaller than those from observations. The interannual variability was generally underestimated, the observed variability in the nutrient observations was about twice as large as that from the simulation. There were, however, a few exceptions where the statistics of both simulated and observed values agreed well, such as for annual phosphate, silicate and chlorophyll levels at NOWESP site 5, annual and winter phosphate levels, annual and summer diatoms levels, and annual silicate level at NOWESP site 6. For more details see Pätsch & Radach (1997), especially their Tables 5 and 6. Using the ELISE model long-term simulations were run and validated for the Bay of Seine with a seven-component nitrogen-silicate version (Guillaud & Menesguen 1998) and an improved

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Figure 16 Hindcast simulation of the years 1955Ð1993: simulated (solid line) and observed (broken line) time-series of nutrients (in mmol mÐ3) and phytoplankton (in mg C mÐ3) at NOWESP site 6 in the North Sea: (A) phosphate, (B) nitrate, (C) silicate, (D) diatoms and (E) flagellates for the area around Helgoland using weighting between adjacent boxes. (From Pätsch & Radach 1997. With permission from Elsevier.)

version of the model by Guillaud et al. (2000), which added the phosphorus cycle to the nitrogen and silicate cycles. Both long-term simulations covered the years 1976Ð1984, and they were compared to — visually slightly different — datasets from station 2 of the French national monitoring system R.N.O. (Figure 17). In general, many of the simulated annual cycles showed sufficient similarity to the observed ones, but the observed variability and extreme values for nitrate, silicate, phosphate and especially chlorophyll were not reproduced. In both papers comparisons for surface DIN and silicate were shown. It is not easy to compare the two simulations because observed maxima shown in Guillaud & Menesguen (1998) no longer appeared in the paper by Guillaud et al. (2000). Simulated DIN was within an order of magnitude, yielded varying annual cycles, but failed to reproduce the low concentrations in six of nine annual cycles and missed the maxima in some years. Simulated surface silicate behaved better, but had similar structural problems with observed extreme values (Guillaud & Menesguen 1998, Guillaud et al. 2000). Chlorophyll met the observed

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Figure 17 Simulated time-series of surface (A) dissolved inorganic nitrogen, (B) silicate, (C) phosphate and (D) chlorophyll a concentrations in the Seine plume (RNO 2/box no. 3) for the period 1976Ð1984 using the ELISE model, compared to observations (Guillaud & Menesguen 1998, Guillaud et al. 2000). (From Guillaud et al. 2000. With permission from Elsevier.)

annual cycles, except for some isolated maximum observations during half of the years. In Guillaud et al. (2000) the simulation was judged to be better than that in Guillaud & Menesguen (1998), because the cost function — as a statistical measure of goodness for the whole time range — yielded the same value for silicate, but slightly better values for nitrogen and chlorophyll. From

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inspection this judgement can be confirmed for DIN, where there was better reproduction of the low summer values (1981Ð1982, 1982Ð1983). Also the summer minima of silicate were better reproduced, but sometimes (1978Ð1979) the depletion was underestimated. Maxima for DIN and silicate were still underestimated. Simulated phosphate showed rather weak annual cycles, as did the observations; the depletion phases were sometimes met (Figure 17). From this exercise one can also learn that the inclusion of a full element cycle as here for phosphorus does not necessarily substantially improve the resulting simulations. Los & Bokhorst (1997) provided a long-term simulation with the DCM-NZB model for the Dutch coastal zone over 20 years (1974Ð1994). The simulated results for phosphate, nitrate, silicate and chlorophyll were compared to the time-series of the Noordwijk station, 10 km offshore, and of the Terschelling station, 4 km offshore (Figure 18). The simulated time-series showed good agreement with observations. The annual cycles for phosphate were generally reproduced. The regeneration in summer seemed to be too weak in the model. Nitrate and silicate were well reproduced, including the depletion phase and maxima in winter. Simulated chlorophyll showed maxima which were often higher than the observations suggest. De Vries et al. (1998) extended the analysis of the coastal gradients by simulating the devel- opment in the 70 km-wide coastal strip during 1975Ð1994, using monthly riverine loads as input. They presented a comparison of simulated and observed time-series at Noordwijk (10 km and 2 km offshore) and Terschelling (4 km offshore) for DIN, DIP and chlorophyll. The simulated nutrients exhibited the same level as the observed except for DIP at Terschelling, which did not reach the observed level; but the interannual variability in the observations was not reproduced. A few river discharge events may, however, be recognised. Chlorophyll was within an order of magnitude, but satisfied only at Terschelling; at Noordwijk the simulation was rather uniform compared to the highly variable observations. To summarise, the findings from the few documented and evaluated long-term simulations which have been performed so far and which were compared to data from long-term monitoring stations in the North Sea led to the following conclusions:

1. The simulated state variables coincided within an order of magnitude with the available observations from monitoring stations. 2. The simulations were able to reproduce the overall development of the eutrophication of the continental coastal North Sea. The coincidence of simulation results with obser- vations was not a property that applied to all aspects simultaneously. Some aspects compared well, others did not. 3. In all models the interannual variability seen in the observations was not reproduced by the simulations. The simulated annual cycles were much more uniform than those observed. The simulated time-series often showed systematic time shifts. 4. The observing stations used for testing the long-term simulation are positioned in rela- tively shallow waters and have peculiarities which disturb the direct comparison with the simulations as long as the horizontal resolution of the models is in the order of 10Ð20 km and not substantially smaller. 5. More complexity in the model does not necessarily improve the simulations. 6. Clearly the quality of the forcing data for the model simulations plays a major role regarding the goodness of the long-term simulation compared to data.

Events

As shown in the preceding sections, spatial distributions as well as temporal changes on timescales of annual cycles and decades were tested mostly against climatological monthly means (Baretta

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Figure 18 Simulated time-series of (A) chlorophyll, (B) dissolved silicate, (C) nitrate and (D) phosphate for the two decades 1974Ð1994 at Terschelling station, 4 km offshore, using the DCM-NZB model, compared to data from the Dutch monitoring programme. (From Los & Bokhorst 1997.)

et al. 1995, Baretta-Bekker et al. 1997, Ebenhöh et al. 1997, Lenhart et al. 1997, Moll 1998; Pätsch & Radach 1997, Radach & Lenhart 1995). The investigation of the validity of the ecosystem models on timescales of events (days to months) needs time-series describing the events with sufficient temporal resolution, and climatological means are of restricted value for this purpose.

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Therefore, events can be studied either in comparison to some of the existing long time-series in coastal areas (see NOWESP datasets in the Appendix) or to data from ship programmes which sample the events sufficiently densely in space and time (e.g., the NERC NSP dataset in the Appendix). For testing one-dimensional models datasets obtained from single ship cruises were very frequently used (Tett & Walne 1995, Kühn & Radach 1997), but these tests have very seldom been repeated with three-dimensional models. As a rare example, the hydrographic dataset from the Fladenground Experiment 1976 in the northern North Sea was used to test a three-dimensional shelf sea circulation model (Pohlmann 1997) and several ecosystem models, one-dimensional and three-dimensional (Kühn et al. 1997). In a preliminary study Kühn et al. (1997) compared the well- observed spring plankton bloom on the Fladenground in 1976 with simulations from ERSEM, ECOHAM and the one-dimensional model by Kühn & Radach (1997), of which the latter gave by far the best coincidence with the data (Figure 19). Although the integrated primary production for

Figure 19 Comparison of the simulations of the spring phytoplankton bloom during FLEX’76 in the northern North Sea by several models (ERSEM, ECOHAM1, 1-dimensional model (Kühn & Radach 1997)), compared to observations: (A) phytoplankton carbon, (B) cumulated primary production (from Kühn et al. 1997).

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the bloom period was similar for all models, the simulations gave very different developments of the bloom. The simple three-dimensional model ECOHAM1 (with a horizontal resolution of about 20 km) gave worse results than the complex but spatially coarser ERSEM I model (with a horizontal resolution of about 100 km). More studies of this kind are urgently needed to achieve more confidence in the three-dimensional complex ecosystem models. A few examples of validational tests are given here, which make clear that the validation of simulated events is hindered by the lack of appropriate datasets. Even data from monitoring programmes, which are useful for the comparison of long-term simulations, seldom have the temporal density that is necessary for validating observed events in the simulation. As a first example, Peeters et al. (1995; their Figure 11) calibrated the simulation driven with nutrient inputs from 1987 by using data from the Dutch monitoring programme at the Noordwijk 20 km offshore station from 1980, 1985, 1987 and 1988, because the data from 1987 alone were too few. It is evident that even such an ambitious monitoring programme as the Dutch one with fortnightly sampling in summer and monthly in winter (De Vries et al. 1998) does not provide the necessary database for studying events. As a second example, Hoch & Menesguen (1997) compared their simulated annual cycles of surface phytoplankton nitrogen with data from the literature to show that the annual cycles were similar. As the data stem from a situation different from the one simulated, the data have to be understood as being representative of a normal annual cycle (e.g., climatological annual cycles) and they cannot be used for validating the specific simulated bloom on the event scale (which was not intended by the authors). In the simulation of chlorophyll by Guillard et al. (2000) the gross features of the annual plankton blooms could be reproduced by the available data, but not the short- term features within the blooms (Figure 17). As a third example, when NORWECOM was applied to simulate the situation during the SCAGEX experiment in the Skagerrak (15 MayÐ29 June 1990) (Skogen et al. 1998), the simulated time-series of salinity, nitrate, phytoplankton carbon and primary production were compared to the available measurements at station Lista during this period. The sparse nitrate and phytoplankton data were more or less met by the simulated curves, but the amount of data was not suited to address the question of whether the simulation was valid (Figure 8 in Skogen et al. 1998). One reason for the observed discrepancies may lie in the physical simulation which was the basis for the ecological one. The sensitivity of the ecological system to physical changes was demonstrated earlier (Eigenheer et al. 1996). Here the observed salinity at 10 m depth deviated substantially from the simulated salinity from 9Ð19 June. In an earlier paper Skogen et al. (1995; their Figure 8) found that the modelled and measured salinity for the whole annual cycle at Lista also differed in the vertical structure and in the temporal development to a degree that might have negatively influenced the ecological simulation. The degree to which this was true in the SCAGEX case can only be shown by appropriate sensitivity studies. To summarise, for the event scale:

1. Far too little validational work has been done at the event scale. 2. The high variability of ecosystem parameters within the annual cycles points to the great importance of single events for the overall outcome. Therefore, it is necessary to model the dynamics on the event scale correctly when simulating annual cycles. 3. Generally speaking, spring phytoplankton blooms can be simulated satisfactorily with respect to the order of magnitude and timing. However, only very few detailed compar- isons were made in the published papers to judge the realism of simulated specific spring blooms and depletion phases.

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4. Groups of phytoplankton species have been simulated with rather limited success. Mod- elling species successions could not realistically be assessed because many dynamic constants for important phytoplankton species are still lacking. 5. There is a great need for data at the event scale. To test more than the general coincidence of simulations within the range of climatological observations, datasets are needed which combine measurements of all relevant state variables on the event scale.

An historic example of such a dataset was provided by the Fladenground Experiment (Lenz et al. 1980) in spring 1976 (FLEX’76). Comparable datasets are needed which are obtained for dynamic developments like spring and autumn blooms, regeneration events, storm events and their conse- quences, overwintering and start of the new production period before the spring bloom. The datasets must have the necessary complexity which renders them suitable for hindcasts because of their completeness and consistency. More specific suggestions depend on the model under consideration.

Model-model intercomparisons and model complexity Model-model intercomparisons can help to sort out specific modelling problems and to evaluate the realism of the simulations, when also compared to data. Model comparison studies are common in other fields of science, such as the atmospheric model intercomparison project (AMIP) initiated in 1989 (Gates et al. 1999). During the end of the 1990s oceanographic-biogeochemical models were compared for the deep global ocean carbon cycle (Stephens et al. 1998) or the local plankton cycles in deep waters (Evans 1999). Comparisons of ecological models for the North Sea area exist for phytoplankton composition (Michielsen et al. 1994) and eutrophication issues (OSPAR et al. 1998). Recently a comparison for the Kattegat was initiated (Stipa et al. 2003). An additional amount of literature exists for modelling the fate of contaminants (Looise 1990, OSPAR 1998). The extension of a model to include more biology does not necessarily mean that the extended model is more realistic. For the North Sea a comparison of two very different ecological models, namely the quasi-three-dimensional box model ERSEM (Radach & Lenhart 1995) and the fully three-dimensional model ECOHAM1 (Moll 1998) gives rise to important questions about model complexity and data quality. While ECOHAM represented a model with simple biology and detailed hydrodynamical forcing, ERSEM was the most advanced North Sea ecosystem model with rela- tively coarse hydrodynamical forcing (for the box structure see Figure 21). Both models were driven by aggregated output from the same general circulation model for the North Sea (Pohlmann 1996) and the same solar radiation data (Moll & Radach 1991, Pätsch 1994). The comparison that follows is restricted to determining how well the models could reproduce the annual cycles for phosphate and phytoplankton. The two simulations of the annual cycles of phosphate in the deep North Sea appeared to be very similar (Figures 9A and 10A). ECOHAM tended to yield less depletion than ERSEM in the coastal boxes; ERSEM overestimated late winter values in the northern North Sea (boxes 1Ð5). ECOHAM overestimated the phosphate concentration in the southern central area (boxes 14, 15). In the British coastal area both simulations met the observations. The German Bight was well simulated by both models. The phytoplankton bloom occurred in ECOHAM too early in the coastal areas and a little too late in the northern area (Figure 9B). ERSEM gave the spring bloom of the northern North Sea at the correct time, but produced the bloom in the eastern part of the northern North Sea 2 months too late (not shown). In the coastal boxes the agreement with data was good, in all other boxes chlorophyll was overestimated by ERSEM. Although the models were very different in complexity, the observed annual cycles of phosphate and phytoplank- ton, described by climatological monthly means, were simulated equally well by the two models. It seems that the box model reproduced nutrient depletion a little better than the ecologically simpler

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three-dimensional ECOHAM model. An important conclusion is that the datasets available for the validation (i.e., the climatological monthly means) are not sufficient to discriminate between the two models of different complexity. Comparisons between ecological models for the same situation without any observations, called model-model intercomparisons, are performed to understand the different behaviour of the models when trying to reproduce the same shelf sea system, with the final aim to find and extinguish the causes of the different behaviours of the models. In a comparison between the NORWECOM and ECOHAM models by Skogen & Moll (2000, 2005) simulations under realistic forcing for 10 different years have been evaluated for regional and interannual variability of annual net primary production. The results from both models sug- gested that the interannual variability in the total primary production of the North Sea was around 15% of the annual mean, and that the variability can locally be higher than this. Thus, an increase in one area was often compensated for by a decrease somewhere else. It was shown that the simple ECOHAM model reproduced primary production in the same order of magnitude as NORWECOM. Again, the question is raised by these results as to what degree of complexity was adequate for an ecological model for the North Sea, when the available climatological dataset had to be used for the comparison, or seen from a different point of view, which data are necessary to discriminate between the two models? A further comparison between two models on phytoplankton species composition presented by Michielsen et al. (1994) raised similar questions. This comparison could also be looked upon as an intercalibration between the CSM-NZB/DCM-NZB model (MANS 1991, De Vries & Michielsen 1992, Peeters et al. 1995) and the FYFY model (Van den Berg et al. 1996). The objective was to compare the models with respect to conceptual framework, mathematical formulation, numerical solution and process rates by comparing the simulation results when both models were fed with similar or identical initial conditions, boundary conditions and forcing functions. In both models competition of algal species groups followed bottom-up control (nutrients and light), based on differences in a number of properties of the phytoplankton groups. In addition, the FYFY model used top-down control through selective grazing. The DCM-NZB model, developed for management purposes, described the dynamics of four phytoplankton groups (diatoms, dinoflagellates, flagellates and Phaeocystis) in the southern North Sea. The FYFY model calculated the dynamics of six phytoplankton groups (three functional groups of diatoms, N-specialist flagellates, P-specialist flagellates divided into grazed and non-grazed species) for a smaller area of the southern North Sea than the DCM-NZB model. Results stem from the simulation of the complete models, including two-dimensional water transport, river loads and solar radiation, applied to the southern North Sea. Figure 20 illustrates the comparison. Both models underestimated the concentrations of nitrate and phosphate at Terschelling station. At Noordwijk station the FYFY model did not reach the observed nitrate and phosphate concentrations, while the DCM-NZB model met the concentrations. The depletion of nutrients during spring and summer was reproduced, but the depletion of phosphate was too pronounced. The comparison for phytoplankton parameters was performed at other locations, i.e. at a deep station of 36 m depth and low turbidity (Noordwijk 70 km offshore, zone 6) and a shallow station of 15 m depth and high turbidity (Noordwijk 20 km offshore, zone 12). The chlorophyll for the shallow and deep stations simulated by the FYFY model showed a distinct spring peak in the chlorophyll concentrations, while the DCM-NZB model simulated higher concentrations all year round. The annual cycles of the daily values of primary production for the shallow and deep stations mirrored the chlorophyll cycle. Near the coast (shallow station) the diatoms in the DCM-NZB model were present from February to November with highest concentrations in March. In the FYFY model they occurred only from March to May, with a peak in April, at a lower level of

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Netherlands; middle: chlorophyll

dinoflagellates vs. N-specialist and P-specialist

Phaeocystis, agellates, al. (1994). Left: Nitrate and phosphate at two sections off the sections off al. (1994). Left: Nitrate and phosphate at two Comparison of simulations of annual cycles of nutrients and phytoplankton groups, using the DCM-NZB and FYFY models (MANS 1991, of nutrients and phytoplankton Comparison of simulations of annual cycles and primary production for two simulation areas; right: species succession for diatoms and fl and primary production for two flagellates. (From Michielsen et al. 1994.) flagellates. (From Michielsen et Figure 20 Figure al. 1995) compared by Michielsen et Michielsen 1992, Peeters et

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concentrations than in DCM-NZB model. From April to July flagellates and Phaeocystis were the main species in the DCM-NZB model, followed by a high biomass of dinoflagellates. In the FYFY model a succession was not as pronounced as in the DCM-NZB model, both for the shallow and for the deep station. Due to a lack of data, Michielsen et al. (1994) did not evaluate the models against phytoplankton observations. Nevertheless, it is obvious that the two model simulations exhibited a quite different behaviour for nutrients, phytoplankton and primary production, although they have a similar degree of complexity and were driven with the same forcing. In conclusion, the model-model intercomparisons suggest that problems still exist in determin- ing the necessary complexity of the model ecosystem:

1. Strong differences in the complexity have yielded very similar results. 2. Very similar complexity has resulted in great differences in the simulation outcome. 3. The existing database is not suitable for testing the models against each other, because the climatological monthly means are not sufficient to discriminate between the models.

Discussion and conclusions Moll & Radach (2003) showed in Part I the extent to which ecological modelling contributed to the understanding of the temporal and spatial development of the ecosystem of the North Sea. In this Part II the realism of the ecological models and their current limits when predicting the development of the coupled physical, chemical and biological North Sea system were discussed. The validational exercises reported show that several of the models were able to reproduce observations of the state variables correctly within an order of magnitude, that is the simulated time-series fall into the range of observed variability, and the state variables were close to the climatological mean situation concerning annual cycles and decadal changes. Validational exercises performed so far had to use climatological annual cycles together with the long-term variability on a monthly basis for the comparisons. The comparison of the validational efforts for the three- dimensional ecological models of the greater North Sea has shown that, at least for the time being, the ecosystem model ERSEM is the best-tested model, when considering the efforts to investigate the reaction potential of the model and the coincidence of the model results with existing data in terms of state variables, different scales and different regions. Due to the many state variables of the ERSEM model the task of validation is enormous, especially in a three-dimensional setup, but this exercise has to be done. It is of great importance not only to learn about the features which the models did reproduce, but also about those which were not reproduced. Looking closer into the behaviour of all of the ecological models investigated, several problems were apparent. The most important deficiencies were the following:

¥ No model achieved a good coincidence with data for the regional distributions of all state variables; in all model systems at least one state variable failed during a certain period. ¥ The quality of the simulated annual cycles varied with parameter, area and season. There is no one model for which all simulated state variables coincided with climatological monthly means in all seasons. ¥ In all long-term simulations the interannual variability seen in the observations was not reproduced by the simulations. The simulated annual cycles were much more uniform than the observed ones. The simulated time-series often showed systematic time shifts.

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¥ Model comparisons showed that more complexity in the model does not necessarily improve the simulations. Strong differences in the complexity have permitted very similar results, and very similar complexity has resulted in great differences in the outcome of the simulation. ¥ The existing databases are not suitable for testing the models, because the climatological monthly means are not sufficient to discriminate between different models.

Until now there has been little systematic quantitative testing, and validational efforts were differently promoted for different state variables according to the availability of data for compar- isons. Most of the models have not been evaluated sufficiently to judge their predictive potential, and they have not yet been tested to a degree which is possible using the various existing datasets that exist today from the northwest European shelf seas (see Appendix). Very rarely was one model tested with more than one dataset. Future observational and modelling needs on the basis of the existing shelf data were discussed earlier in detail by Berlamont et al. (1996). Also Baretta et al. (1998) discussed the observational requirements for validation of marine ecosystem models, based on their experiences with ERSEM for the North Sea and the Mediterranean Sea. The seven main conclusions from the evaluation of the specific ecosystem models of Table 1 investigated in this review are:

1. Strictly speaking none of the models can be called a validated model in the sense of a ‘valid model’. 2. For developing a predictive capability it is necessary to model the dynamics on the event scale correctly when simulating annual cycles. 3. For judging the capability of the model to reproduce nature in comparison to the capa- bility of other models the only way is to calculate statistical measures for coincidence and to compare these numbers for selecting the simulation model of choice. 4. In all validational efforts reported the amount of available relevant data is the limiting factor for testing the models and therefore for a faster development toward validated models. 5. For the key process complexes included in the models, field experiments are needed which provide the critical datasets for testing and discriminating the complex ecological model systems. 6. For validating ecological models field experiments have to be designed in cooperation between field oceanographers and modellers. 7. Comparisons of the different ecological models for the North Sea have to be performed, organised in workshops or projects, using the same datasets for initialisation and forcing and for testing the realism of the simulated results.

Thus, to make progress in ecological modelling of the North Sea the activity has to be directed toward several areas of research. There is no one simple pathway for modellers alone. Progress can only be achieved when modellers and field scientists cooperate intensively. In the following, the conclusions are supported by a more detailed discussion of three topics, the degree of validation with respect to temporal and spatial scales, the causes for the lack of validity and the methodology for validation.

Status of validation on different temporal scales and data needs The status of validation depends on the spatial and temporal scales investigated. Even if only the reproduction of the mean climatological situation in the range of its variability is addressed by the

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simulations, the outcome is not yet satisfactory. When the reproduction of more detailed, actual situations are the aim of the modelling, the lack of suitable data is the main obstacle for progress, because it cannot be shown how good (or bad) the model fits the data. Events At the event scale too little validational work in three-dimensional modelling has been done. Usually spring blooms and depletion phases were discussed and judged, but few detailed comparisons were made. The databases for thoroughly testing simulated events do not exist. For validating simulated events targeted process-oriented short period (of about a week) to medium period (of some months) synoptic multi-ship and multidisciplinary experiments are needed to create critical comprehensive datasets for testing key process complexes in the ecological models. For testing more than the general coincidence of a simulated event, like a phytoplankton bloom, within the range of climatological observations, datasets are needed which resemble in their spirit the dataset from the Fladenground Experiment in spring 1976 (FLEX’76) (Lenz et al. 1980) in that they describe certain dynamic developments in the necessary complexity and completeness. Such dynamic features are spring and autumn blooms, regeneration events, storm events and their consequences, overwintering and start of the new production period before the spring bloom. The ‘necessary complexity and completeness’ must be defined by the demands for testing the simulation models in a dialogue between field and modelling scientists, to enable a hindcast of the dynamic situation. Annual cycles On the seasonal scale nearly all three-dimensional models have been tested with climatological monthly mean data, representing the annual cycle. The comparisons showed that usually the best simulated nutrients were phosphate and silicate while nitrate or nitrogen was simulated with less success. Chlorophyll was simulated only within an order of magnitude, some- times over-, sometimes underestimated. The phasing of nutrients and chlorophyll showed differ- ences compared to the data which were least satisfactory at times of intense regeneration of nutrients. The discrepancies with the data increased with the trophic level. The regional differences in the annual cycles of nutrients, chlorophyll and primary production can be reproduced quite well. Regional distributions With the exception of the observations of sea surface temperature, the temporal resolution of observed spatial fields of the important state variables that can presently be used is restricted to monthly mean distributions for a climatological year. No comprehensive datasets exist, however, for testing the models for one single specific year, including the necessary forcing functions and the validational data needed for the model simulations, for the whole of the North Sea region. Therefore, basic datasets on the shelf for the most commonly measured nutrients and chlorophyll, augmented by primary production measurements, which resolve the annual cycle at least of one single year in the North Sea for all variables, are still urgently required. For the southern part of the North Sea the dataset from the NERC NSP exists (see Appendix). The validation of the models demands spatial distributions over time for the main phytoplankton groups diatoms, nanoflagellates and dinoflagellates. As long as such datasets are not available, the validation procedure will not progress substantially. Major problems for setting up models for species, size classes or functional groups are both the lack of data for the dynamic constants and of datasets from critical experiments to test the simulation model. Therefore, it is still an open question whether the approach by species, by size classes or by functional groups is the most appropriate one. Case studies are necessary where all approaches are compared, using the same datasets. Long-term developments On the decadal scale several long-term simulations have been performed which show that the state variables coincide within an order of magnitude with the available observations. For example, they were able to reproduce the overall development of the eutrophi- cation of the continental coastal North Sea. The simulated time-series which were compared to data from the few long-term monitoring stations in the North Sea (see NOWESP datasets in the

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Appendix) showed systematic time shifts during certain periods, but the reason for this cannot be attributed unambiguously without further testing of the model. One cause may lie in the fact that the stations used for testing the long-term simulations are all positioned in relatively shallow waters and have site-specific peculiarities which may disturb the direct comparison with the simulations, because the horizontal resolution of the models is in the order of 10Ð20 km and therefore the stations may not be representative for the corresponding box in the model setup. As long as there are no further time-series in open waters and regular (monthly) North Sea surveys to provide better datasets for validation of long-term simulations from three-dimensional ecological models, the same incomplete datasets, which were utilised for deriving the climatological annual cycles, have to be used. Thus, the data situation offers much more restricted possibilities for validating long-term simulations than exist for validating simulated annual cycles. For developing predictive ecological models actual distributions of observations of the main constituents of the ecosystem are necessary at least for the duration of a decade. And furthermore, long time-series of key marine parameters with high temporal resolution at key locations are necessary. The existing time-series of up to four decades are still too short for a significant analysis of decadal variability or system shifts. New positions for time-series data including phyto- and zooplankton groups and species and further ecological state variables and processes are needed in the North Sea similar to the North Atlantic BATS station (Karl et al. 2001). Stations where time- series exist must continue to be maintained. Biological sampling should be always accompanied by extensive measurements of physical and chemical parameters.

Causes for the lack of coincidence with data The causes for the lack of coincidence with data were usually not reported in the literature, presumably because they were not known. Therefore, we are limited to interpreting the deficiencies of the models which are recognisable in the papers, and hypothesise on possible causes from our modelling experience. The comparisons of the results of simulations with data have shown that ecological simulations did neither reproduce fully the observed means of the state variables nor their variability. This may have been caused by the setup of the model or by the available data or both. Possible causes of the lack of coincidence with observations will be discussed here briefly, namely (1) the spatial and temporal resolution of the internal dynamics, (2) the trophic resolution (complexity of the system’s representation) and (3) the uncertainty of the initialisation and forcing functions.

Spatial and temporal resolution of the internal dynamics

When a model is forced with space and time averaged field data, the biology will not respond on small scales, but follow the scale of the forcing. Experiments with forcing of different temporal resolution (hourly, daily, weekly) made it clear that the results of the model simulation were dependent on this resolution (Ridderinkhof 1992). It is an open question how much of the variability of the ecosystem variables will be stimulated by which temporal and spatial resolution of the forcing variables. Experiments should be performed that investigate systematically the cascade of variance from the forcing through the food web to provide the knowledge about the necessary spatial and temporal resolution in three-dimensional simulation models and to learn how temporal and spatial small-scale, meso-scale and large-scale variance can be properly modelled. Although one-dimensional models still have their specific merits for exploring in an easy way the functioning of specific parts of the marine system, unfortunately they cannot identify which of the reasons is the most important, because circulation contributes an important part to ecological variability (e.g., Skogen & Moll 2005). Three-dimensional investigations are necessary for estimating the contributions of the different

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physical and biological processes to the variability. The necessary spatial and temporal resolution for reproducing the observed variability in the simulations of the internal dynamics should be investigated in three-dimensional test cases. A further problem of scale is hidden in the data used for the comparisons. In most comparisons simulation results and observations represent different time and space scales (e.g., simulated instantaneous values vs. climatological monthly means; simulated box means vs. point observations at a station (Pätsch & Radach 1997)). This may give rise to disagreements between simulation results and observations. Procedures should be explored on how to determine comparable quantities from simulation results and available observations.

Complexity of the system’s representation

The problems associated with the trophic resolution (i.e., the complexity of the system’s represen- tation) may be the hardest to solve, because the loss of variability in the simulations compared to nature could depend on the aggregation of species. From the various studies it can be learned that the inclusion of a finer trophic resolution or of a full element cycle did not necessarily substantially improve the resulting simulations and yield ‘the best results’ (see section on ‘Model-model inter- comparisons and model complexity’). It is an open question how complex the model must be to reproduce a given dataset. This general problem should be studied to yield criteria for choosing the necessary complexity of the food web which allows the observed variability to be reproduced. One possible practical procedure may be to systematically and successively extend the range of variables and calculate the mean and variance of those variables that can be measured and predicted. Such a sequence of simulations may elucidate which mechanisms are responsible for the largest portion of the variance in the simulated time-series of the state variables that have observed counterparts. The problem is complicated, however, by the fact that the quality of the available datasets used for the comparisons is important for testing the necessary complexity. If the dataset does not sufficiently resolve the observed features, which will be modelled, in space and time, then the tests cannot give reliable information. New datasets are needed for this purpose.

Uncertainty in data for initialisation and forcing

The results from the model depend on data for initialisation and forcing. To ensure realistic simulations for the comparisons, observed and simulated data are needed that map the dynamics on the correct scales and have little uncertainty. It is well known that the circulation field provides the basic structure for the biological distributions, as expressed by the term ‘eco-hydrodynamic adjustment’ (Nihoul 1975). Hence, the dynamics and scales of the circulation models have to match those that are needed for addressing biological questions. Monthly mean driving forces are not sufficient for simulations of, for example, plankton blooms of a few days duration. The use of inappropriate forcing and initialisation yields unnecessary uncertainty in the result from the simulation. In this field many improvements could still be made which directly induce a better representation of biological dynamics. The validity of the simulations could be much improved by forcing the models with actual (observed or simulated) forcing functions, thus reducing the uncertainty for the prediction of variability. With respect to future environmental problems, which will occur in the North Sea, a decadal time frame has to be envisaged for modelling. This necessitates broadening the scope of interest from the local ecosystem dynamics to the external forcing of the system, because the forcing causes variability in the appearance of the ecosystem. The external forcing acts on the dynamics of the ecosystem in the form of an exchange of energy and matter with adjacent sea areas (Atlantic, Baltic

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Sea), with the atmosphere and as river inputs. Certainly, solar radiation acts as the main forcing for photosynthesis. For all these agents good-quality data are needed. However, the availability of data for forcing hindcasts decreases the longer the requirement for the hindcast to go back in history, and models of all sorts (e.g., circulation, atmospheric, estuarine, hydrological) must become more and more the tools for providing the forcing for ecological models. There are strong needs for enhanced information from atmospheric models or, even better, from dynamically coupled ocean- atmosphere models to improve the ‘atmospheric forcing’, like wind and sea-surface heat exchange forecasts, which are determining factors in ecological forecasting. It is necessary to make use of coupling of highly resolved regional sea and ocean models and of coupled shelf circulation- continental hydrology models, which give the inflows for fresh water and matter from land to sea, both of which are prerequisites for long-term simulations over decades. Several of the datasets presently available for the forcing of North Sea dynamics were located and discussed in detail in the Technical Report by Moll & Radach (2001). The quality of the forcing eventually determines the quality of the simulations and thus the degree to which ecological models for the North Sea can be validated. Improved common datasets of forcing functions (especially the open boundary conditions) for simulating annual cycles are needed to complement the existing validation datasets.

Methodology for validation Ecological modelling has now advanced so far that quantitative statistical measures should be applied to discriminate the acceptable models from those which need further validational efforts. For this purpose well-defined, accepted methods for validation should routinely be used. Validational concepts common in other fields of natural sciences, like meteorology and oceanography, should be considered by ecological modellers. In physical oceanography various statistical methods such as root mean square errors, regressions, the estimation of a bias and frequency dependent correlation coefficients (squared coherency) at special stations, were applied to validate hydrodynamic models. The methods were used to investigate how well the temporal and spatial variability was reproduced by the model. Spatial variability was investigated by using the technique of empirical orthogonal functions. It is suggested that such methods should also be used for validating ecological models. The application of these methods, however, demands corresponding datasets. It would be a great step forward if modelling and field oceanographers worked together to design a field experiment to obtain the data for testing the models. For testing ecological models simplified situations should be investigated for which the results are known. As an example, Sverdrup’s critical depth theory has been found to be useful as a first step in examining the general pattern of phytoplankton seasonality (Obata et al. 1996). In complex ecological models many basic mechanisms are included as several physical-biological interactions and necessary external forcing functions, and increased efforts should be made to examine whether such mechanisms were correctly represented in the models. There are quite a number of basic mechanisms which are suited for testing the behaviour of the models (steady-state equilibriums, prey-predator dynamics). In numerical weather prediction complex equations are commonly used, and the assimilation of observations into the simulations is also common. Assimilation uses the most sophisticated methods for linking meteorological simulated results and observations. Many new advances in this field for estimating statistical properties of this process can be found in meteorological journals (Dee & da Silva 1999, Dee et al. 1999). In meteorology it is acknowledged that further improvement of the forecast is best realised by improving the assimilation of observations, not by improving the quality of the atmospheric models (Prandle & Flemming 1998). Assimilation methods have as yet

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not been used very much in ecological modelling (Schartau 2001, Popova et al. 2002), but this branch of improving the performance of the models should be developed. Again, the application of such methods demands a solid database of observations, defined by the needs of the model. Comparisons should be performed where the models are driven by the same forcing functions. Comparisons are needed for all types, for example, more complex vs. less complex models, more aggregated vs. less aggregated models, box models vs. three-dimensional models, for spatially differently resolved models, and between different three-dimensional models. Observational datasets should be composed which are suited for carrying out a range of benchmark tests of the models.

Data needs As was stressed in nearly every section above, validation of the ecological models depends on the available data, and significant progress can only be expected if the database is improved. These data on their own may not have great scientific merit, but are of value when combined with ecological models. Therefore the organised cooperation of field scientists and modellers is of great importance for successful model validation. In all cases described the limited amount of relevant data or even the lack of data was the critical problem for the validation of the models and therefore for a faster development toward validated models. If field experiments were to provide the ‘critical datasets’ in the future the testing and discrimination of complex ecological model systems will make progress.

Acknowledgements Great thanks go to all the modellers across Europe who very kindly provided us with valuable information about their models and with helpful comments. We like to thank M. Kreus for technical support on the figures and C. Stegert on the literature. We thank our colleagues Dr. W. Kühn, Dr. J. Pätsch and Dr. H. Lenhart, whose criticism led to many improvements of the text. We are deeply indebted to the OMB editor, Dr. J. Gordon, for thoroughly editing and improving our manuscript. Finally, we acknowledge the support for this review which was provided by the BMBF project SYCON (03F0215A) and the project GLOBEC Germany (03F0320E).

References

Agoumi, A., Gosse, P. & Khalanski, M. 1985. Numerical modelling of the influence of the vertical thermal structure on phytoplanktonic growth in the English Channel. In Proceedings of the 19th EMBS, P.E. Gibbs (ed.), Cambridge, U.K.: Cambridge University Press, 23Ð38. Allen, J.I. 1997. A modelling study of ecosystem dynamics and nutrient cycling in the Humber plume, U.K. Journal of Sea Research 38, 333Ð359. Allen, J.I., Blackford, J., Holt, J.T., Proctor, R., Ashworth, M. & Siddorn, J. 2001. A highly spatially resolved ecosystem model for the North West European Continental Shelf. Sarsia 86, 423Ð440. Allen, J.I., Blackford, J.C. & Radford, P.J. 1998. An 1-D vertically resolved modelling study of the ecosystem dynamics of the middle and southern Adriatic Sea. Journal of Marine Systems 18, 265Ð286. Allen, J.I., Siddorn, J., Blackford, J.C. & Gilbert, F.J. 2004. Turbulence as a control on the microbial loop in a temperate seasonally stratified marine systems model. Journal of Sea Research 52, 1Ð20. Baretta, J.W., Baretta-Bekker, H.J.G. & Ruardij, P. 1998. Data needs for ecosystem modelling. ICES Journal of Marine Science 55, 756Ð766. Baretta, J.W., Ebenhöh, W. & Ruardij, P. 1995. The European Regional Seas Ecosystem Model (ERSEM), a complex marine ecosystem model. Netherlands Journal of Sea Research 33, 233Ð246.

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Baretta, J.W. & Ruardij, P. 1987. Evaluation of the Ems Estuary ecosystem model. Continental Shelf Research 7, 1471Ð1476. Baretta-Bekker, J.G., Baretta, J.W. & Ebenhöh, W. 1997. Microbial dynamics in the marine ecosystem model ERSEM II with decoupled carbon assimilation and nutrient uptake. Journal of Sea Research 38, 195Ð211. Baretta-Bekker, J.G., Baretta, J.W. & Koch Rasmussen, E. 1995. The microbial food web in the European Regional Seas Ecosystem Model. Netherlands Journal of Sea Research 33, 363Ð379. Baumert, H. & Radach, G. 1992. Hysteresis of turbulent kinetic energy in non-rotational tidal flows: a model study. Journal of Geophysical Research 97, 3669Ð3677. Berlamont, J., Radach, G., Becker, G., Colijn, F., Gekeler, J., Laane, R.W.P.M., Monbaliu, J., Prandle, D., Sündermann, J., van Raaphorst, W. & Yu, C.S. 1996. Future observational and modelling needs identified on the basis of the existing shelf data. Deutsche Hydrographische Zeitschrift 48, 421Ð436. Blackford, J.C. 1997. An analysis of benthic biological dynamics in a North Sea ecosystem model. Journal of Sea Research 38, 213Ð230. Bokhorst, M. & Los, F.J. 1997. Calibratie MANSeutro CSM-2DH. Report T1608, WL Delft Hydraulics, Delft, The Netherlands. Brockmann, U. & Topcu, D.H. 2002. North Sea Nutrient Atlas. Texte-Umwelt Bundesamt 26, 1Ð380. Burchard, H., Bolding, K. & Villareal, M.R. 1999. GOTM, a General Ocean Turbulence Model. Theory, implementation and test cases. Report EUR 18745, European Commission, Ispra, Italy. Burchard, H. & Petersen, O. 1999. Models of turbulence in the marine environment — a comparative study of two-equation turbulence models. Journal of Marine Systems 21, 29Ð53. Burchard, H., Petersen, O. & Rippeth, T.P. 1998. Comparing the performance of the Mellor-Yamada and the k-epsilon two-equation turbulence models. Journal of Geophysical Research 103, 10,543Ð10,554. Charnock, H., Dyer, K.R., Huthnance, J.M., Liss, P.S., Simpson, J.H. & Tett, P.B. (eds). 1994. Understanding the North Sea System. London: Chapman & Hall. De Vries, I., Duin, R.N.M., Peeters, J.C.H., Los, F.J., Bokhorst, M. & Laane, R.W.P.M. 1998. Patterns and trends in nutrients and phytoplankton in Dutch coastal waters: comparison of time-series analysis, ecological model simulation, and mesocosm experiments. ICES Journal of Marine Science 55, 620Ð634. De Vries, M.B. & Michielsen, B.F. 1992. Food web analysis and bioaccumulation modelling in freshwater ecosystems. Report 9.92, WL Delft Hydraulics, Delft, The Netherlands. Dee, D.P. 1995. A pragmatic approach to model validation. In Quantitative Skill Assessment for Coastal Ocean Models, D.R. Lynch & A.M. Davies (eds), Washington, D.C.: American Geophysical Union, 1Ð13. Dee, D.P. & da Silva, A.M. 1999. Maximum-likelihood estimation of forecast and observation error covariance parameters. Part I: Methodology. Monthly Weather Review 127, 1822Ð1834. Dee, D.P., Gaspari, G., Redder, C., Rukhovets, L. & da Silva, A.M. 1999. Maximum-likelihood estimation of forecast and observation error covariance parameters. Part II: Applications. Monthly Weather Review 127, 1835Ð1849. Delhez, E.J.M. 1998. Macroscale ecohydrodynamic modelling on the northwest European Continental Shelf. Journal of Marine Systems 16, 171Ð190. Delhez, E.J.M., Damm, P., de Goede, E., de Kok, J.M., Dumas, F., Gerritsen, H., Jones, J.E., Ozer, J., Pohlmann, T., Rasch, P.S., Skogen, M. & Proctor, R. 2004. Variability of shelf-seas hydrodynamic models: lessons from the NOMADS2 Project. Journal of Marine Systems 45, 39Ð53. Ebenhöh, W., Baretta-Bekker, J.G. & Baretta, J.W. 1997. The primary production module in the marine ecosystem model ERSEM II, with emphasis on the light forcing. Journal of Sea Research 38, 173Ð193. Eigenheer, A., Kühn, W. & Radach, G. 1996. On the sensitivity of ecosystem box model simulations on mixed- layer depth estimates. Deep-Sea Research I 43, 1011Ð1027. Evans, G.T. 1999. The role of local models and data sets in the Joint Global Ocean Flux Study. Deep-Sea Research I 46, 1369Ð1389. Fasham, M.J.R., Sarmiento, J.L., Slater, R.D., Ducklow, H.W. & Williams, R. 1993. Ecosystem behaviour at Bermuda station “S” and ocean weather station “India”: A general circulation model and observational analysis. Global Biogeochemical Cycles 7, 379Ð415. Fransz, H.G. & Verhagen, J.H.G. 1985. Modelling research on the production cycle of phytoplankton in the Southern Bight of the North Sea in relation to riverborne nutrient loads. Netherlands Journal of Sea Research 19, 241Ð250.

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Gates, W.L., Boyle, J.S., Covey, C., Dease, C.G., Doutriaux, C.M., Drach, R.S., Fiorino, M., Gleckler, P.J., Hnilo, J.J., Marlais, S.M., Phillips, T.J., Potter, G.L., Santer, B.D., Sperber, K.R., Taylor, K.E. & Williams, D.N. 1999. An overview of the results of the atmospheric model intercomparison project (AMIP I). Bulletin of the American Meteorological Society 80, 29Ð55. Gregg, W.W. & Walsh, J.J. 1992. Simulation of the 1979 spring bloom in the Mid-Atlantic Bight: a coupled physical-biological-optical model. Journal of Geophysical Research 97, 5723Ð5743. Guillaud, J.-F., Andrieux, F. & Menesguen, A. 2000. Biogeochemical modelling in the Bay of Seine (France): an improvement by introducing phosphorus in nutrient cycles. Journal of Marine Systems 25, 369Ð386. Guillaud, J.-F. & Menesguen, A. 1998. Modelisation sur vingt ans (1976Ð1995) de la production phytoplank- tonique en baie de Seine. Oceanologica Acta 21, 887Ð906. Hoch, T. & Garreau, P. 1998. Phytoplankton dynamics in the English Channel: a simplified three-dimensional approach. Journal of Marine Systems 16, 133Ð150. Hoch, T. & Menesguen, A. 1997. Modelling the biogeochemical cycles of elements limiting primary production in the English Channel: II. Sensitivity analyses. Marine Ecology Progress Series 146, 189Ð205. Horwood, J.W. 1982. Algal production in the west-central North Sea. Journal of Plankton Research 4, 103Ð124. Howarth, M.J., Dyer, K.R., Joint, I.R., Hydes, D.J., Purdie, D.A., Edmunds, H., Jones, J.E., Lowry, R.K., Moffat, T.J., Pomroy, A.J. & Proctor, R. 1994. Seasonal cycles and their spatial variability. In Understanding the North Sea System, H. Charnock et al. (eds), London: Chapman & Hall, 5Ð25. Hydes, D.J., Kelly-Gerreyn, B.A., Thomson, S., Proctor, R. & Prandle, D. 1997. The biogeochemistry of nitrogen in the southern North Sea: the development of a mathematical model based on the results of the NERC-North Sea Programme surveys of 1988 and 1989. Report 5, Southampton Oceanography Centre, Southampton, U.K. Ishizaka, J. 1990. Coupling of coastal zone color scanner data to a physical-biological model of the southeastern U.S. continental shelf ecosystem. 2. An Eulerian model. Journal of Geophysical Research 95, 20,183Ð20,199. Jones, J.E. 2002. Coastal and shelf-sea modelling in the European context. Oceanography and Marine Biology: An Annual Review 40, 37Ð141. Karl, D.M., Dore, J.E., Lukas, R., Michaels, A.F., Bates, N.R. & Knap, A. 2001. Building the long-term picture: the U.S. JGOFS Time-Series Programs. Oceanography 14, 6Ð17. Kelly-Gerreyn, B.A., Gellers-Barkmann, S. & Hydes, D.J. 1997. North Sea water quality modelling: a progress report on the coupling of a pelagic and benthic model DYMONNS II. Report 3, Southampton Oceanography Centre, Southampton, U.K. Kraus, E.B. (ed.). 1977. Modelling and Prediction of the Upper Layers of the Ocean. Oxford: Pergamon Press. Kühn, W., Lenhart, H.-J., Moll, A., Pätsch, J. & Radach, G. 1997. Simulating the FLEX’76 situation using different plankton models. Berichte aus dem Zentrum für Meeres- und Klimaforschung; Reihe Z: Interdisziplinäre Zentrumsberichte 2, 145Ð148. Kühn, W. & Radach, G. 1997. A one-dimensional physical-biological model study of the pelagic nitrogen cycling during the spring bloom in the northern North Sea (FLEX’76). Journal of Marine Research 55, 687Ð734. Laane, R.W.P.M., van Leussen, W., Radach, G., Berlamont, J., Sündermann, J., van Raaphorst, W. & Colijn, F. 1996. North-West European shelf programme (NOWESP): an overview. Deutsche Hydrographische Zeitschrift 48, 217Ð229. Lancelot, C., Rousseau, V., Billen, G. & van Eeckhout, D. 1997. Coastal eutrophication of the Southern Bight of the North Sea: assessment and modelling. In Sensitivity to Change: Black Sea, Baltic Sea and North Sea, E. Özsoy & A. Mikaelyan (eds), Dordrecht: Kluwer Academic Press, 439Ð453. Lancelot, C., Spitz, Y., Gypens, N., Ruddick, K., Becquevort, S., Rousseau, V., Lacroix, G. & Billen, G. 2005. Modelling diatom and Phaeocystis blooms and nutrient cycles in the Southern Bight of the North Sea: the MIRO model. Marine Ecology Progress Series 289, 63Ð78. Lee, J.-Y., Tett, P., Jones, K., Jones, S., Luyten, P., Smith, C. & Wild-Allen, K. 2002. The PROWQM physical- biological model with benthic-pelagic coupling applied to the northern North Sea. Journal of Sea Research 48, 287Ð331. Lenhart, H.-J., Radach, G. & Ruardij, P. 1997. The effects of river input on the ecosystem dynamics in the continental coastal zone of the North Sea using a box refined ecosystem model ERSEM. Journal of Sea Research 38, 249Ð274.

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Lenz, W., Ramster, J. & Weidemann, H. 1980. First steps in the realization of the Joint North Sea Data Acquisition Project for 1976 (JONSDAP’76). Meteor Forschungsergebnisse A 22, 3Ð10. Looise, B.A.S. 1990. Modelling the effects of polluting chemicals on marine ecosystems — a literature search project for the North Sea. Report 5/1990, Ministry of Housing, Physical Planning and Environment, Leidschendarm, The Netherlands. Los, F.J. & Bokhorst, M. 1996. Trend analysis Dutch coastal zone 1975Ð1994. Report Z2013, WL Delft Hydraulic, Delft, The Netherlands. Los, F.J. & Bokhorst, M. 1997. Trend analysis Dutch coastal zone 1975Ð1994. Berichte aus dem Zentrum für Meeres- und Klimaforschung; Reihe Z: Interdisziplinäre Zentrumsberichte 2, 161Ð175. Luff, R. & Moll, A. 2004. Seasonal dynamics of the North Sea sediments using a three-dimensional coupled water-sediment model system. Continental Shelf Research 24, 1099Ð1127. Luff, R., Wallmann, K., Grandel, S. & Schlüter, M. 2000. Numerical modeling of benthic processes in the deep Arabian Sea. Deep-Sea Research II 47, 3039Ð3072. Luyten, P.J., Jones, J E., Proctor, R., Tabor, A., Tett, P. & Wild-Allen, K. 1999. COHERENS Ð A Coupled Hydrodynamical-Ecological Model for Regional and Shelf Seas: User Documentation. MUMM Report, Management Unit of the Mathematical Models of the North Sea, Brussels, Belgium. Lynch, D.R. & Davies, A.M. (eds). 1995. Quantitative Skill Assessment for Coastal Ocean Models. Washington, D.C.: American Geophysical Union. MANS 1991. MANS-Management analysis of the North Sea: Scientific workshop on eutrophication models. Report GWWS 91.213, Rijkswaterstaat, Den Haag, The Netherlands. MARE Consortium, Los, H., Wijsman, J. & Tatman, S. 2001. Description and model representation. Part 2: Transport, nutrients and primary production. Report Z3030.10, WL Delft Hydraulic, Delft, The Netherlands. Menesguen, A. & Hoch, T. 1997. Modelling the biogeochemical cycles of elements limiting primary production in the English Channel: I. Role of thermohaline stratification. Marine Ecology Progress Series 146, 173Ð188. Michielsen, B., Los, H., van den Berg, A.J., Ruardij, P., Joordens, J., de Vries, I. & van der Tol, M.W.M. 1994. Comparison of models describing species group composition of marine phytoplankton. BEON Report 94-8, Rijkswaterstaat, Rijksinstituut voor Kust en Zee, Den Haag, The Netherlands. Moll, A. 1998. Regional distribution of primary production in the North Sea simulated by a three-dimensional model. Journal of Marine Systems 16, 151Ð170. Moll, A. 2000. Assessment of three-dimensional physical-biological ECOHAM1 simulations by quantified validation for the North Sea with ICES and ERSEM data. ICES Journal of Marine Science 57, 1060Ð1068. Moll, A., Pätsch, J. & Kühn, W. 2003. ECOHAM2 User Guide — The Ecological North Sea Model, Hamburg, Version 2. Technical Reports 02-2003, Institut für Meereskunde, Hamburg, Germany. Moll, A. & Radach, G. 1991. Application of Dobson and Smith’s solar radiation model to German Bight data. Quarterly Journal of the Royal Meteorological Society 117, 845Ð851. Moll, A. & Radach, G. 2001. Synthesis and new conception of North Sea Research (SYCON) — Working Group 6: review of three-dimensional ecological modelling related to the North Sea shelf. Berichte aus dem Zentrum für Meeres- und Klimaforschung; Reihe Z: Interdisziplinäre Zentrumsberichte 8, 225. Moll, A. & Radach, G. 2003. Review of three-dimensional ecological modelling related to the North Sea shelf system — Part 1: models and their results. Progress in Oceanography 57, 175Ð217. Mommaerts, J.P. 1981. Atlas of particulate primary production results from the central station during the FLEX’76 campaign as calculated with a model of photosynthesis-light relationship, Management Unit of the North Sea Model, Ministry of Public Health (IHE), Brussels. Nihoul, J.C.J. (ed.). 1975. Modelling of Marine Systems. Amsterdam: Elsevier Science Publishing Company. Obata, A., Ishizaka, J. & Endoh, M. 1996. Global verification of critical depth theory for phytoplankton bloom with climatological in situ temperature and satellite ocean color data. Journal of Geophysical Research 101, 20,657Ð20,667. Oreskes, N., Shrader-Frechette, K. & Belitz, K. 1994. Verification, validation, and confirmation of numerical models in the earth sciences. Science 263, 641Ð646.

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GÜNTHER RADACH & ANDREAS MOLL

OSPAR. 1998. Report of the ASMO workshop on modelling transport and fate of contaminants. Report for OSPAR Commission, Netherlands Institute for Coastal and Marine Management, RIKZ, The Hague, The Netherlands. OSPAR, Villars, M., de Vries, I., Bokhorst, M., Ferreira, J., Gellers-Barkman, S., Kelly-Gerreyn, B., Lancelot, C., Menesguen, A., Moll, A., Pätsch, J., Radach, G., Skogen, M., Soiland, H., Svendsen, E. & Vested, H.J. 1998. Report of the ASMO modelling workshop on eutrophication Issues, 5Ð8 November 1996, The Hague, The Netherlands. OSPAR Commission Report, Netherlands Institute for Coastal and Marine Management, RIKZ, The Hague, The Netherlands. Pätsch, J. 1994. MOCADOB a model generating synthetical time-series of solar radiation for the North Sea. Berichte aus dem Zentrum für Meeres- und Klimaforschung; Reihe B: Ozeanographie 16, 67. Pätsch, J. & Radach, G. 1997. Long-term simulation of the eutrophication of the North Sea: temporal development of nutrients, chlorophyll and primary production in comparison to observations. Journal of Sea Research 38, 275Ð310. Peeters, J.C.H., Los, F.J., Jansen, R., Haas, H.A., Peperzak, L. & de Vries, I. 1995. The oxygen dynamics of the Oyster ground, North Sea. Impact of eutrophication and environmental conditions. Ophelia 42, 257Ð288. Pohlmann, T. 1996. Predicting the thermocline in a circulation model of the North Sea — part I: model description, calibration and verification. Continental Shelf Research 16, 131Ð146. Pohlmann, T. 1997. Estimating the influence of advection during FLEX’76 by means of a three-dimensional shelf sea circulation model. Deutsche Hydrographische Zeitschrift 49, 215Ð226. Popova, E.E., Lozano, C.J., Srokosz, M.A., Fasham, M.J.R., Haley, P.J. & Robinson, A.R. 2002. Coupled 3D physical and biological modelling of the mesoscale variability observed in North-East Atlantic in spring 1997: biological processes. Deep-Sea Research I 49, 1741Ð1768. Popper, K.R. 1982. Logik der Forschung. Tübingen: J.C.B. Mohr. Prandle, D. & Flemming, N.C. 1998. The Science Base of EuroGOOS. EuroGOOS Publication 6, 58. Proctor, R., Baart, A., Berg, P., Boon, J., Deleersnijder, E., Delhez, E., Garreau, P., Gerritsen, H., Jones, J.E., de Kok, J., Lazure, P., Luyten, P., Ozer, J., Pohlmann, T., Ruddick, K., Salden, R., Salomon, J.C., Skogen, M., Tartinville, B. & Vested, H.J. 1997. NOMADS — North Sea Model Advection — Dispersion Study. Internal Document 108, Proudman Oceanographic Laboratory, Birkenhead, U.K. Proctor, R., Holt, J.T., Allen, I. & Blackford, J. 2003. Nutrient fluxes and budgets for the North West European Shelf from a three-dimensional model. The Science of the Total Environment 314–316, 769Ð785. Radach, G. 1983. Simulation of phytoplankton dynamics and their interactions with other system components during FLEX’76. In North Sea Dynamics, J. Sündermann & W. Lenz (eds), Berlin: Springer-Verlag, 584Ð610. Radach, G. & Gekeler, J. 1996. Annual cycles of horizontal distributions of temperature and salinity, and of concentrations of nutrients, suspended particulate matter and chlorophyll on the northwest European shelf. Deutsche Hydrographische Zeitschrift 48, 261Ð297. Radach, G. & Gekeler, J. 1997. Gridding of the NOWESP data sets — annual cycles of horizontal distributions of temperature and salinity, and of concentrations of nutrients, suspended particulate matter and chlorophyll on the north-west European Shelf. Berichte aus dem Zentrum für Meeres- und Klimafor- schung; Reihe B: Ozeanographie 27, 377. Radach, G., Gekeler, J., Becker, G., Bot, P., Castaing, P., Colijn, F., Damm, P., Danielssen, D., Foyn, L., Gamble, J. C., Laane, R., Mommaerts, J.P., Nehring, D., Pegler, K., van Raaphorst, W. & Wilson, J. 1996. The NOWESP Research Data Base. Deutsche Hydrographische Zeitschrift 48, 241Ð259. Radach, G. & Lenhart, H.-J. 1995. Nutrient dynamics in the North Sea: fluxes and budgets in the water column derived from ERSEM. Netherlands Journal of Sea Research 33, 301Ð335. Radach, G. & Pätsch, J. 1997. Climatological annual cycles of nutrients and chlorophyll in the North Sea. Journal of Sea Research 38, 231Ð248. Radach, G., Pätsch, J., Gekeler, J. & Herbig, K. 1995a. Annual cycles of nutrients and chlorophyll in the North Sea (Part 1). Berichte aus dem Zentrum für Meeres- und Klimaforschung; Reihe B: Ozeanog- raphie 20, 172. Radach, G., Pätsch, J., Gekeler, J. & Herbig, K. 1995b. Annual cycles of nutrients and chlorophyll in the North Sea (Part 2). Berichte aus dem Zentrum für Meeres- und Klimaforschung; Reihe B: Ozeanog- raphie 20, 173Ð371.

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Radach, G., Trahms, J. & Weber, A. 1980. The chlorophyll development at the central station during FLEX’76 — Two data sets. Proceedings of the final ICES/JONSIS Workshop on JONSDAP 76, ICES CM 1980/C:03, 3Ð21. Radford, P.J. 1979. Some aspects of an estuarine ecosystem model — GEMBASE. State-of-the-Art in Eco- logical Modelling 7, 301Ð322. Radford, P.J. & West, J. 1986. Models to minimize monitoring. Water Research 20, 1059Ð1066. Ridderinkhof, H. 1992. On the effects of variability in meteorological forcing on the vertical structure of a stratified water column. Continental Shelf Research 12, 25Ð36. Ruardij, P. & van Raaphorst, W. 1995. Benthic nutrient regeneration in the ERSEM ecosystem model of the North Sea. Netherlands Journal of Sea Research 33, 453Ð483. Schartau, M. 2001. Data-assimilation studies of marine, nitrogen based, ecosystem models in the North Atlantic Ocean, Christian-Albrechts-Universität, Kiel, 1–127. Schrum, C. & Backhaus, J.O. 1999. Sensitvity of atmosphere — ocean heat exchange and heat content in the North Sea and the Baltic Sea. Tellus 51, 526Ð549. Skogen, M.D. & Moll, A. 2000. Interannual variability of the North Sea primary production: comparison from two model studies. Continental Shelf Research 20, 129Ð151. Skogen, M.D. & Moll, A. 2005. Importance of ocean circulation in ecological modelling: an example from the North Sea. Journal of Marine Systems 57, 289Ð300. Skogen, M.D., Soiland, H. & Svendsen, E. 2003. Environmental status of the Skagerrak and North Sea 2001. Fisken og havet 2003–03, 1Ð20. Skogen, M.D., Svendsen, E., Berntsen, J., Aksnes, D.L. & Ulvestad, K.B. 1995. Modeling the primary production in the North Sea using a coupled three-dimensional physical-chemical-biological ocean model. Estuarine, Coastal and Shelf Science 41, 545Ð565. Skogen, M.D., Svendsen, E. & Ostrowski, M. 1998. Quantifying volume transports during SKAGEX with the Norwegian ecological model system. Continental Shelf Research 17, 1817Ð1837. Skogen, M.D., Svendsen, E. & Soiland, H. 2002. Environmental status of the Skagerrak and North Sea 2000. Fisken og havet 2002–03, 1Ð22. Soiland, H. & Skogen, M.D. 2000. Validation of a three-dimensional biophysical model using nutrient observations in the North Sea. ICES Journal of Marine Science 57, 816Ð823. Stephens, B.B., Keeling, R.F., Heimann, M., Six, K.D., Murnane, R. & Caldeira, K. 1998. Testing global

ocean carbon cycle models using measurements of atmospheric O2 and CO2 concentration. Global Biogeochemical Cycles 12, 213Ð230. Stipa, T., Skogen, M., Hansen, I.S., Eriksen, A., Hense, I., Kiiltomäki, A., Soiland, H. & Westerlund, A. 2003. Short-term effects of nutrient reductions in the North Sea and the Baltic Sea as seen by an ensemble of numerical models. MERI Report Series of the Finnish Institute of Marine Research 49, 43Ð70. Stroo, D. 1986. A Method for Validation. Interne Verslagen EON 1, Nederlands Instituut voor Onderzoek der Zee, NIOZ, Texel, The Netherlands. Sündermann, J., Becker, G., Damm, P., van den Eynde, D., Frohse, A., Laane, R., van Leussen, W., Pohlmann, T., van Raaphorst, W., Radach, G., Schultz, H. & Visser, M. 1996. Decadal variability on the Northwest European Shelf. Deutsche Hydrographische Zeitschrift 48, 365Ð400. Tett, P.B. & Walne, A. 1995. Observations and simulations of hydrography, nutrients and plankton in the southern North Sea. Ophelia 42, 371Ð416. Van den Berg, A.J., Ridderinkhof, H., Riegman, R., Ruardij, P. & Lenhart, H.-J. 1996. Influence of variability in water transport on phytoplankton biomass and composition in the southern North Sea: a modelling approach (FYFY). Continental Shelf Research 16, 907Ð931. Visser, M., Batten, S., Becker, G., Bot, P., Colijn, F., Damm, P., Danielssen, D., van den Eynde, D., Foyn, L., Frohse, A., Groeneveld, G., Laane, R., van Raaphorst, W., Radach, G., Schultz, H. & Sündermann, J. 1996. Time-series analysis of monthly mean data of temperature, salinity, nutrients, suspended matter, phyto- and zooplankton at eight locations on the Northwest European shelf. Deutsche Hydrog- raphische Zeitschrift 48, 299Ð323. Wei, H., Jun, S., Moll, A. & Zhao, L. 2004. Phytoplankton dynamics in the Bohai Sea — observations and modeling. Journal of Marine Systems 44, 233Ð251.

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Wei, H., Zhao, L., Yu, Z., Sun, Y., Liu, Z. & Feng, S. 2003. Variation of the phytoplankton biomass in the Bohai Sea. Journal of Ocean University of Qingdao 33, 173Ð179. Weigel, P. & Hagmeier, E. 1978. Primary production measurements and the timing of the phytoplankton spring bloom at 58û55′ N, 0û32′ E (North Sea) during Fladenground Experiments 1976 (FLEX 76), Biolo- gische Anstalt Helgoland, Technical Report Meeresstation Helgoland, Helgoland. Zhao, L., Wei, H. & Feng, S. 2002. Annual cycle and budgets of nutrients in the Bohai Sea. Journal of Ocean University of Qingdao 1, 29Ð37.

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APPENDIX

Several datasets of observations exist for the North Sea which were repeatedly used for validational efforts. The observations were usually averaged to give climatological means for spatial box structures as shown in Figure 21. The ICES dataset, the ERSEM datasets and the NOWESP datasets were derived in this manner. Long time-series were only obtained in the coastal areas of the North Sea, namely in the Dutch coastal zone, at Helgoland and at station E1 in the English Channel. In the following the datasets are described in some detail, and the locations of their availability are given.

ERSEM datasets The ERSEM datasets were originally aggregated for validating the different versions of the ERSEM ecosystem model, namely

¥ the 15-box version ERSEM I, based on a subdivision of the North Sea simulation area into 10 upper and 5 lower boxes, as shown in Figure 21A; ¥ the 130-box version ERSEM II, based on a subdivision of the North Sea into 85 upper and 45 lower boxes, as shown in Figure 21B; ¥ the 138-box version of ERSEM, called COCOA (COntinental COastal Application), based on a subdivision of the North Sea into 93 upper and 45 lower boxes, as shown in Figure 21C, with refined boxes in the southern North Sea and along the British and Danish coasts.

The upper boxes extend from the surface to 30 m, the lower boxes from 30 m to the bottom. For each box dataset products of statistical values for several state variables were derived. The major data sources of the ERSEM datasets were (a) datasets of original observations compiled in the ECOMOD database of the Institut für Meereskunde (IfM) of the University of Hamburg and (b) a dataset of monthly mean values of phosphate, nitrate, ammonium, silicate and chlorophyll, provided by the International Council for the Exploration of the Sea (ICES) for IfM. The dataset from ICES was based on data of the years 1985Ð1994 from the northwest European shelf, using a 1û × 1û resolution, as for ERSEM II (Figure 21B). ICES provided climatological arithmetic means, medians, standard deviations and quantiles for the five parameters mentioned. The two datasets had different intensities of coverage of the North Sea area. To circumvent the problem of overlapping data (which could not be solved because the basic ICES data were not available), either ECOMOD or ICES data products were used to generate the ERSEM datasets. The complicated procedure was described in detail in Radach & Pätsch (1997), where also examples of the annual cycles were presented. The complete ERSEM datasets are available from publications (Radach et al. 1995a,b) and from the Internet (http://www.ifm.uni-hamburg.de/~wwwem/dow.html (accessed 28 July 2005)). Recently, a nutrient atlas became available for the North Sea (Brockmann & Topcu 2002), which comes with a CD-ROM and has the advantage of providing nutrient datasets as cruise tracks from 1984Ð2000.

ICES dataset This dataset ICES for the comparison of eutrophication models for the North Sea (OSPAR et al. 1998, Moll 2000, Soiland & Skogen 2000). It was derived from all available data held at the ICES data centre for the years 1980Ð1989 and consists of climatological seasonal means of chlorophyll,

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(A) (B)

(C) (D)

Figure 21 Box structure for model setups and corresponding data averaging: box structure for (A) 15-box version of ERSEM I. (B) 130-box version of ERSEM II. (C) 138-box version COCOA of ERSEM. (D) ICES dataset. (From (A) Baretta et al. 1995; (B) Pätsch & Radach, 1997; (C) Lenhart et al. 1997; (D) Moll 2000. All with permission from Elsevier.)

phosphate, dissolved inorganic nitrogen, and silicate concentrations and their standard deviations; it covers the whole North Sea region. The data were averaged spatially over boxes of 0.5û longitude and 1û latitude (Figure 21D), whereby each box was subdivided into a surface layer (0Ð20 m) and

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a bottom layer (20 mÐbottom). To obtain the necessary spatial coverage the temporal averaging had to be relatively coarse and was done for three seasonal periods: JanuaryÐFebruary (JF), May, June and July (MJJ), and July, August and September (JAS). For each box and each seasonal period, the mean value and the standard deviation of the data were given. The dataset can be ordered from ICES (http://www.ices.dk (accessed 28 July 2005)) or from the same URL as above (http://www.ifm.uni-hamburg.de/~wwwem/dow.html (accessed 28 July 2005)).

NERC NSP dataset A comprehensive interdisciplinary dataset for one annual cycle was obtained by the NERC NSP (North Sea Project) during the period from August 1988ÐOctober 1989, by repeating the same cruise track in the southern North Sea at monthly intervals (Howarth et al. 1994). The measurements at over 100 locations were made during 15 consecutive months throughout the water column and near the major estuaries. The great variety of observed parameters can be seen from the publications of the results (e.g., Charnock et al. 1994). The data were partly included in the ERSEM, ICES and NOWESP dataset. The NERC NSP dataset is the only one resolving the annual cycle on a monthly basis with substantial spatial coverage of the North Sea. The datasets were issued on CD-ROM by the British Oceanographic Data Centre (BODC), which can be contacted via the internet (http://www.bodc.ac.uk (accessed 28 July 2005)).

NOWESP datasets Within the MAST project NOWESP (Laane et al. 1996) all available observations of the parameters temperature, salinity, phosphate, nitrate, nitrite, ammonium, silicate, suspended particulate matter and chlorophyll from the northwest European shelf region were compiled in a database (Radach et al. 1996). This was a follow-up of ECOMOD, and various products were derived from the original data: Annual cycles of climatological data interpolated on a 20 × 20 km grid for the shelf (Radach & Gekeler 1996, 1997) and time-series of climatological monthly means (Sündermann et al. 1996, Visser et al. 1996). In the NOWESP dataset many important survey and monitoring datasets from European insti- tutions were included: datasets from the Biologische Anstalt Helgoland (including the Helgoland Reede time-series from 1962–1995), the British NERC NSP (BODC, Bidston), the Bundesamt für Seeschifffahrt und Hydrographie in Hamburg (BSH), HELCOM, ICES in Copenhagen, the Institut für Ostseeforschung in Warnemünde (IOW), the Institute for Marine Research in Bergen (IMR), the Institut für Meereskunde at University of Hamburg (IfM), the Rijkswaterstaat (RIKZ) in Den Haag (including the Dutch monitoring data) and many others. Details of compiled data were given by Radach & Gekeler (1997). The most important time-series created for validation purposes of North Sea models were the following time-series of monthly means (Figure 22):

¥ at NOWESP site 2 based on the long time-series at station E1 in the Channel off Plymouth; ¥ at NOWESP sites 4-1, 4-2, 4-3 based on Belgian monitoring data during 1975Ð1993; ¥ at NOWESP sites 5-1, 5-2, 5-3 based on Dutch monitoring data during 1975Ð1993, including the stations on the Noordwijk and Terschelling sections;

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Figure 22 Map of the Northwest European Shelf area, defined as the area within the 200 meters depth contour. Locations of the eight boxes, where long time-series of shelf data were available: the Irish Sea (1), the Channel (2), along the east coast of Scotland (3), along the Belgian (4) and Dutch coast (5), in the German Bight (6), in the Skagerrak (7) and along the Norwegian coast (8). Positions and time-series information in Visser et al. (1996). (Map with permission from Radach et al. 1996.)

¥ at NOWESP site 6 based on German monitoring data from 1962Ð1995 which consist mainly of the time-series at Helgoland Reede from 1962Ð1993; ¥ at NOWESP sites 7-1 and 7-2 in the Skagerrak based on the long-term data from the Hirtshals-Torungen sections (1980Ð1992) and the experiment SCAGEX.

The NOWESP data products are available from the same URL as above (http://www.ifm. uni-hamburg.de/~wwwem/dow.html (accessed 28 July 2005)). The Dutch monitoring programme by Rijkswaterstaat includes two transects in the coastal zone perpendicular to the coast: the Noordwijk transect near the outflow of the rivers Rhine and Maas and the Terschelling transect to the north, with emphasis on the stations near the coast (2Ð4 km) (de Vries et al. 1998). The data are partly included in the NOWESP datasets. They were available from the Netherlands Institute for Coastal and Marine Management (RIKZ) which may be contacted via e-mail ([email protected]).

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Oceanography and Marine Biology: An Annual Review, 2006, 44, 61-83 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis

ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS

SUSANNE P. BADEN* & SUSANNE P. ERIKSSON Göteborg University, Department of Marine Ecology, Kristineberg Marine Research Station, S-450 34 Fiskebäckskil, Sweden *E-mail: [email protected]

Abstract This review provides an overview of the role, routes and effects of manganese in aquatic crustaceans. Manganese is a naturally abundant metal in marine and freshwater sediments where it is involved in a large number of chemical processes. Although sediments contain high natural concentrations of manganese, the potential danger to benthic organisms has been neglected in studies to date. Manganese bioavailability increases as the result of human impact and it accumulates in biota. Manganese may occur in toxic concentrations (10Ð20 mg lÐ1) in the bottom water of marine coastal areas after hypoxia, or more locally (e.g., close to industries) as well as in acidic lakes and aquaculture shrimp ponds. Though manganese is an essential metal, it is also an unforeseen toxic metal in the aquatic environment. Although the uptake and elimination of manganese is rapid, manganese affects processes that decrease the fitness of organisms. As manganese bioavailability increases, its uptake is predominately through the water. The midgut gland, nerve tissue, blood proteins and parts of the reproductive organs have the highest accumulation factors and are the main target tissues. The functional effects of manganese in aquatic environments are still sparsely investigated. Recent results show that the immune system, the perception of food via chemosensory organs and a normal muscle extension are affected at manganese concentrations observed in the field.

Geochemical role of manganese Manganese is the 12th most common element, the fourth most abundant metal and is universally distributed in the earth’s crust and waters (Anonymous 2005). This metal is involved in a large number of chemical processes, due mainly to its redox sensitivity. The literature on manganese (Mn) geochemistry in the aquatic environment is immense (Elderfield 1976), whereas literature on the occurrence and biological effects of manganese in aquatic animals is comparatively sparse. Man- ganese concentrations in soil vary from 0.001Ð7 mg gÐ1 dry weight (dw), averaging 0.75 mg gÐ1 dw (Saric 1986). Ocean sediment concentrations vary from approximately 1Ð50 mg gÐ1 dw (Elderfield 1976). Since the 1800s an intensive and ongoing debate has been centred on the origin and amount of the manganese flux to the oceans. Three main sources have been identified: continental weather- ing (lithogenous origin), submarine volcanism and an upward migration in porewaters as a conse- quence of sediment diagenesis (Elderfield 1976). The anthropogenic supplies of manganese to aquatic biotopes derive mainly from mine tailings and from steel manufacturing industries where approximately 90% of total manganese is used as a deoxidising and desulphurising additive and

as an alloying constituent (Saric 1986). Manganese (MnO2) is also widely used in dry cell batteries (Saric 1986), as a contrasting agent for nuclear magnetic resonance tomography, and as an agri- cultural fungicide (Gerber et al. 2002). A manganese antiknock additive (methylcyclopentadienyl manganese tricarbonyl (MMT)) was introduced to Canada in 1990 to substitute for lead in fuel,

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and since 1995 MMT has also been used in several states of the USA (Shukla & Singhal 1984, Davis 1998, Normandin et al. 2002). In the rapidly expanding shrimp farming industry of tropical regions, manganese is added to shrimp ponds in the form of potassium permanganate (KMnO4), as disinfectant, in concentrations causing potential hazards to life in the ponds and in the coastal zone close to the effluent water (Gräslund & Bengtsson 2001, Visuthismajarn et al. 2005). Manganese becomes bioavailable as Mn(II) in water when it is reduced by hypoxic/anoxic conditions in sediment. The reduction of manganese dioxides occurs during the degradation of sedimenting organic matter (Dehairs et al. 1989). The process is directly or indirectly microbially mediated but is fastest when sulphide and Fe(II) are reductants (Johnson et al. 1991). In general, the solubility (and bioavailability) of manganese increases with decreasing oxygen tension and pH, but not with increasing temperature (Wollast et al. 1979, Faust & Aly 1983). During oxic conditions in bottom water, sediment porewater may contain Mn concentrations of 0.16Ð24.0 mg lÐ1 (Canfield et al. 1993, Aller 1994, Magnusson et al. 1996), whereas bottom water concentrations are between 0.18Ð16.5 µg lÐ1 (Laslett & Balls 1995, Hall et al. 1996). During Ð1 hypoxia (O2 < 3 mg l )), the Mn(II) of the bottom water can increase by several orders of magnitude to 1.5 mg lÐ1, as in the Kiel Bight (Balzer 1982), and up to 22 mg lÐ1 in the anoxic bottom water of the Orca Basin in the Mexican Gulf (Trefry et al. 1984). This review aims to give an overview of the role of manganese in aquatic animals, its routes of uptake, and biological effects, mainly focusing on marine crustaceans living in and on the sediment. As the biological chemistry of manganese is poorly explored in invertebrates, the relevant medical and biological literature on basic processes involving Mn in vertebrates is cited.

Biological role of manganese Essentiality Manganese is an essential trace metal for metabolism belonging to the borderline elements (Mn, Fe, Co, Ni, Cu, Zn, Cd, Hg, Pb) of the periodic table. It lies between the oxygen-seeking elements of class A (Na, Mg, K and Ca being the most abundant) and the sulphur- and nitrogen-seeking elements (including heavy metals like Ag, Au and Hg) of class B, and thus exhibits aspects of both classes (Nieboer & Richardson 1980). In its divalent form, Mn(II), manganese has a relatively high affinity for sulphur or nitrogen in functional groups of proteins and other molecules, which enables Mn to interfere in a wide spectrum of biological processes (Simkiss 1979, Williams 1981). The divalent Mn(II) exchanges water and ligands rapidly and the binding constant of the metal in proteins is weak. Manganese is important as a cofactor or activator of different enzymatic reactions (e.g., electron- transfer reactions, antioxidant defences, and phosphorylation) (Simkiss & Taylor 1989). In the case of enzymes containing metal ions (mainly Mg(II), Mn(II) and Zn(II)) the metal ion itself can bind with groupings in the substrate and act as a strain-producing agent by forming a chelated interme- diary compound. At the same time the metal ion, because of its positive charge, is an efficient electrophilic agent that can act as an effective participant in the reaction (White et al. 1973). Examples of enzymatic reactions having Mn as an activator are acetyl-CoA carboxylase (the first reaction in the fatty acid formation in the endoplasmatic reticulum), pyruvate carboxylase (in the mitochondrial formation of oxaloacetate), glycylglycine dipeptidase (in the degradation of dena- tured intracellular proteins) and the well-known Mn-super oxide dismutase (Mn-SOD) (a redox enzyme in the mitochondria facilitating the production of dioxygen) (Cotzias 1958, White et al. 1973, da Silva & Williams 1991). Manganese is mainly accumulated in organelles like the mitochondria, Golgi apparatus and vesicles, whereas concentrations in the cytoplasm are relatively low. These concentration gradients are sustained by metal transporters over the membrane (e.g., Luk & Culotta 2001). The elimination

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of Mn(II) from the mitochondria is a slow, energy-requiring, Na-dependent efflux mechanism (Gavin et al. 1999). In general, those metals having an essential biochemical role, such as the metals mentioned above, are regulated at the individual level, while for non-essential metals such as mercury (Hg), cadmium (Cd) and silver (Ag) there is only weak evidence of controls on accumulation. Under constant ambient conditions, the net balance between inward and outward fluxes of metals provides the underlying control on tissue burdens and, in general, metals that exchange rapidly tend to be accumulated less efficiently than metals that exchange slowly. Accumulation may give rise to body concentrations in excess of four orders of magnitude above background in non-regulating organisms (Rainbow 1992, 1997).

Toxicity Many borderline metals are thus essential to metabolism as micronutrients but may have the potential of being toxic in high concentrations. The toxicity of manganese has been known for over 150 years after it was recognised that mine workers inhaling dust rich in Mn developed ‘manganism’ (Couper 1837). Manganism is an irreversible brain disease with prominent psychological and neurological disturbances. Such neurological responses have received close attention because they resemble several clinical disorders collectively described as ‘extra pyramidal motor system dys- function’ and in particular Parkinson’s disease. The disease is regarded as chronic and the clinical signs of intoxication include many symptoms dominated by speech disturbance, compulsive actions and motor dysfunction like tremor and stiff gait (Mena et al. 1967, Iregren 1990, Aschner & Aschner 1991). Recently, however, a manganese-induced epileptic syndrome was cured after treatment with

a chelating treatment of CaNa2EDTA (Hernandez et al. 2003). Another much debated theory connects excess Mn exposure with the initiation of transmissible spongiform encephalopathy (TSE), also called scrapie in sheep and Creutzfeldts Jacobs disease (CJD) in humans. Imbalance of Mn and Cu is established when Mn- and Cu-chelating insecticides (organo-phosphates) are taken up at the same time, giving a substitution of Cu with Mn as Mn(III) in the CNS prion protein. This substitution conforms the prions, preventing their degradation, and TSE may develop (Purdey 2000). As Mn(III), manganese is able to accumulate in the brain, likely carried through the blood- brain barrier via transferrin and receptor-mediated endocytosis (Simkiss & Taylor 1989, Aschner & Aschner 1991). Transferrin is a protein containing a Fe-cluster crucial for absorption, transport, storage and excretion of Fe in mammals and is able to cross the otherwise relatively impermeable blood-brain barrier. Manganese may mirror Fe and bind to transferrin, not necessarily replacing Fe, and in this way passes the blood-brain barrier (Aschner & Aschner 1991). Within the brain the main part of Mn(III) appears to release from transferrin and concentrate in certain parts via axonal transport (Henriksson et al. 1999). In freshwater crayfish a structural analogue to the vertebrate blood-brain barrier called the glial perineurium, has been identified. The glial perineurium ensures protection of the CNS by having a high degree of ion selectivity and regulation (Butt et al. 1990). A direct uptake from the media through the nasal chamber in rats and olfactory chamber of pike (Esox lucius) followed by axonal transport along primary and secondary neurones into the olfactory bulb has been documented (Tjälve et al. 1995, 1996). A similar uptake and transport into nerve tissue of invertebrates has not been described to date. Hydrated Mn has an ionic ratio close to that of Ca(II), and its ability to affect various aspects of neuronal transmission has been ascribed primarily to its mimicry of Ca (Aschner & Aschner 1991). Manganese ions are known to affect various steps in the chemical synapses of nerve-muscle transmission in a wide range of animal groups. At low concentrations, Mn ions have been found to pass through Ca channels in a number of different preparations, e.g., giant squid axons (Yamagishi 1973), mammalian cardiac muscle (Ochi 1970, 1975; Delahayes 1975), mouse oocytes (Okamoto et al.

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1977), starfish eggs (Hagiwara & Miyazaki 1977), larval beetle skeletal muscle fibres (Fukunda & Kawa 1977) and frog skeletal muscle fibres (Palade & Almers 1978). However, at higher concen- trations Mn ions are potent inhibitors of synaptic transmission (Katz & Miledi 1969, Ross & Stuart 1978, Xiao & Bevan 1994) and also act as competitive inhibitors of Ca ion flow through calcium channels in muscle membranes (Fatt & Ginsborg 1958, Hagiwara & Takahashi 1967, Takeda 1967, Mounier & Vassort 1975). Manganese affects not only the presynaptic site of action but also the postsynaptic site (Katz & Miledi 1969). This is consistent with earlier studies on the excitation- contraction coupling mechanisms in crustacean muscles, which indicated that Mn ions compete with Ca ions to pass through sarcolemmal calcium channels and thus affect muscle membrane depolarisation (Fatt & Ginsborg 1958, Hagiwara & Nakajima 1966, Chiarandini et al. 1970, Mounier & Vassort 1975). More recently, Hirata (2002) presented evidence that Mn(II) can induce DNA fragmentation, a biochemical hallmark for apoptosis, in neuronal cells.

Deficiency The theoretical requirement of manganese for crustaceans has been calculated to be 3.9 µg Mn g1 dw (White & Rainbow 1987). The calculation was based on the animals’ total content, thus including the exoskeleton where the majority of the manganese is incorporated into the calcareous matrix. In the literature pelagic crustaceans are reported to have an average muscle and midgut gland concentration of less than 2 µg Mn gÐ1 dw and a total manganese body concentration of 1.2Ð1.4 µg Mn gÐ1 dw (Table 1). Even the benthic lobster Nephrops norvegicus from the pristine Faeroe Islands contains very low Mn concentrations (Table 1). When excluding the exoskeleton and the stomach (which may contain sediment rich in Mn) in these animals, the rest of the body (the soft tissue) contains an Mn concentration of 2.5 µg Mn gÐ1 dw (n = 32) (S.P. Eriksson & S.P. Baden, unpublished observations). The theoretical required concentration of manganese in the soft tissue of crustaceans is thus likely to be somewhat overestimated. Since no data exist on crustacean manganese deficiency, the precise Mn requirements of Crustacea remain unresolved. It is hoped that further investigations will provide an answer. Most field-caught animals contain manganese concentrations well above the assumed basic requirements needed and manganese deficiency does not appear to pose a general threat to aquatic crustaceans (Table 1).

Manganese in Crustacea — Overview Manganese is an essential metal and is thus required in at least a minimum concentration for an animal to be able to fulfil its metabolic functions. When discussing the basic body requirements of manganese, it is, however, also important to differentiate between metabolically active soft tissues and relatively inert tissues. Each tissue is likely to have its own kinetics (reaction rate) of metal uptake and loss, the determination of which can often be valuable when interpreting the biological significance of metal burdens. The interpretation of animal kinetic data and animal metal concen- tration is potentially complicated by a combination of factors including organism condition, growth, food supply, moulting and reproduction cycles, and may also depend directly or indirectly on environmental conditions like temperature, oxygen saturation and metal concentration. Some tissue metal concentrations are maintained within a narrow range and for others there may be less tight regulation and even storage. Clearly, under such circumstances, increased metal burdens in specific tissues could easily be obscured when analysing whole organisms. The literature on background manganese concentrations in different crustaceans derives from field-collected animals from marine and freshwater environments (Table 1). Average total Mn con- centration was 63 µg Mn gÐ1 dw, with the lowest concentrations found in marine pelagic crustaceans and benthic lobsters from the pristine Faroe Islands. The highest total Mn concentration was found

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ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS Eriksson & Baden 1998 et al. 2004 Rainbow & Rainbow Blackmore 2001 Fialkowski et al. 2003 et Fialkowski Eriksson 2000a,b unpublished Martin & Ceccaldi 1976 & Depledge 2002 Weinstein et al. 1992 et Weinstein Kress et al. 1998, Drava al. 1998, Drava Kress et Baden & Childress Rainbow et al. 2002 et Rainbow Kress et al. 1998 Kress et al. 2003 Heu et Blackmore 1999, Rainbow et al. 1998, et Rainbow al. 2002 Blasco et Hendrickx et al. 1998 Hendrickx et Martin 1975, Bjerregaard Martin 1975, Bjerregaard Ovary Testes References 5.1* 0.9Ð7.4 0.4Ð0.6 4.7 1.9 5.3 25 Eriksson unpublished, 7Ð18 2.5Ð5.0 6 Martin 1974, 1975, 1976, 14Ð17 3.6Ð4.3 1.4 11 3.1 5.5 33 Eriksson & Baden 1998, 0.4Ð1.6 36Ð76 92Ð286 175Ð282 0.36Ð0.38 7.5Ð10 10Ð24 3.1Ð19 Eggs Exo. Gills Haem. Midg.gl. Muscle 53 36 10 10Ð28 7Ð42 0.2Ð0.3 8.0 3.5 11 5.9 0.12 12.3* 27.9* D,B S,B 25.2Ð97.4 D,B 32 D D D,H S,B S,B S,BD,B 74Ð206 D,B 91.7D,B 5.5Ð120 150 45 shell) S,B 6.7Ð10 Ð ( shell) S,B Ð ( Manganese concentrations found in field-caught crustaceans from pristine areas Manganese andalus borealis (Faroe islands) (Faroe alitrus saltator squamosa etraclita T Balanus crenatus T Squilla mantis eximia Acantephyra Aristeus antennatus thermydon Bythograea Callinectes sapidus Cancer irroratus maenas Carcinus vicarius Heterocarpus norvegicus Nephrops norvegicus Nephrops P able 1 T Habitat/Order/SpeciesMarine Amphipoda Subhabitat Total Stomatopoda Thoracica Decapoda

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SUSANNE P. BADEN & SUSANNE P. ERIKSSON ed in Al-Mohanna & 2001 Subrahmanyam al. 1998 Sanders et

Balkas et al. 1982, Balkas et Young & Harvey 1991 & Harvey Young Jorhem et al. 1994 Jorhem et al. 1990 Alikhan et al. 1994 Jorhem et Balkas et al. 1982 Balkas et al. 1998 Kress et al. 2003 Heu et Akyuz et al. 2001 et Akyuz Ridout et al. 1989 Ridout et al. 2002 Gherardi et al. 2002 Gherardi et Ovary Testes References 4Ð8 0.8* 3.0* 1.1Ð2.0 3.1 1.9al. 1995 et Paez-Osuna 2 6711 3.6 0.1 0.7Ð1.2* 361374 2 87 107 89al. 1994, Steenkamp et 305 3740 218 35 47 Values calculated from wet weight by using ww/dw ratio stat Values 0.6 100 0.63 102 9 23 37 ent, P-pelagic, Exo-Exoskeleton, Haem-Haemolymph and Midg.gl.-Midgut gland. 95 3 32 340 508 66Ð106 12Ð33 11 9.4Ð13 5.4Ð11 Eggs Exo. Gills Haem. Midg.gl. Muscle 52 160 239 199 34 36 847 12 29.3* dry weight tissue, except for haemolymph which is in wet weight. * dry weight tissue, except

Ð1 D,B B D S,P B P 1.2Ð4.0 S,B S,B B6 S,B S,B S,B B5 S,B g Mn g µ Manganese concentrations found in field-caught crustaceans from pristine areas Manganese

) Mean 63 22 96 Penaeus Max/min ratio (as

All values are given as are given All values athurus achypenaeus curvirostris achypenaeus ustropotamobius pallipes ustropotamobius anulirus inflatus typhlops olycheles ortunus pelagicus acifastacus leniusculus otamon fluviatile otamonautes warreni ker P Melicertus P P Tr Asellus aquaticus Astacus astacus A Cambarus bartonii virilis Orconectes P P P Larvae able 1 (continued) able 1 Euphausiacea T Habitat/Order/Species Subhabitat Total Freshwater Decapoda Notes: Decapoda, Mysidacea, the original papers. Abbreviations: S-shallow, D-deep, B-benthic, H-hydrothermal v S-shallow, Abbreviations: the original papers.

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in a freshwater crayfish (Potamonautes warreni). Highest mean tissue Mn concentration was found in the animal’s midgut gland (102 µg Mn gÐ1 dw) and the lowest concentration in the muscle tissue (average 9 µg Mn gÐ1 dw). All haemolymph values were presented as wet weight (ww) values and were thus compared as such, giving an average Mn concentration of 0.63 µg Mn gÐ1 ww. The dw/ww ratio of haemolymph equivalent to approximately 7Ð17% (S.P. Baden, unpublished observations). In general, all tissue concentrations showed a high interspecies variability, with the largest difference (almost 4000-fold) found in the midgut gland of a freshwater, benthic crayfish compared with that of a marine, pelagic crab (Table 1). Due to the high interspecies variability, and the fact that often only a few of the tissues are measured in each species, caution should be made when comparing the mean tissue concentrations at the bottom of Table 1. In two cases, sufficient data were obtained to statistically compare tissue concentrations in crustaceans of different habitats. The results showed that freshwater decapods had a significantly higher Mn concentration in the midgut gland than marine decapods (one-way ANOVA, df 10, F-value 7.4, p < 0.05), but that no difference could be observed for the Mn concentration in the exoskeleton of freshwater and marine decapods (one-way ANOVA, df 8, F-value 0.34, p > 0.05). The variability within individuals (between tissues) was in comparison lower. By ranking the tissue concentrations of Mn in Table 1 for species, where more than two tissues had been measured, the following general relationship between tissues was observed: exoskeleton, gill > egg > testes > ovary, midgut gland > muscle > haemolymph. Even when animals are exposed to elevated Mn concentrations, as in environments that are polluted (industrial waste), acidic (lakes and rivers) or hypoxic (mainly eutrophic marine areas), the relative relationship between the exoskeleton, gills, midgut gland, muscle and haemolymph holds, though concentrations are higher than in animals from pristine areas (Table 2).

The routes and effects of manganese In the following sections an up-to-date review on the routes and effects of manganese in crustaceans is presented. In Figure 1 the uptake of manganese from water is described as well as the accumu- lation and effects in separate target tissues. Existing data on elimination kinetics are described under the respective tissue section.

Uptake of manganese from water For many organisms the key determinant that influences metal accumulation from water is the speciation of the metal. Metals are usually considered more bioavailable as free ions than as complex ligands with anions. In sea water as much as 58% of the total Mn concentration is free hydrated ions whereas 37% is complexed with chloride, 4% with sulphate and 1% with carbonate (Simkiss & Taylor 1989). Hydrated ions are clearly larger than the equivalent ions in a crystal. These hydration properties of ions in aqueous solution are important in determining the permeability and selectivity of ions crossing membranes (Simkiss & Taylor 1989). Of the borderline metals, only Mn has a sufficiently low enthalpy to be able to shed its hydration and pass through membrane channels. The uptake of divalent trace metal ions occurs mainly at permeable respiratory surfaces, for example gills, and is driven by passive diffusion via ligand binding occurring through calcium channels (Rainbow 1997).

Gills

Crustaceans are relatively impermeable animals, having the main part of the body covered with a calcareous exoskeleton. The uptake of ions, including metals, dissolved in water thus occurs largely

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Table 2 Manganese concentrations in field-caught crustaceans from pristine, polluted (industrial waste), acidic (lakes and rivers) and hypoxic (eutrophic) areas

Habitat/Order/Species Tissue Pristine Polluted Acidic Hypoxic References Marine Amphipoda Talitrus saltator Total 31 105 Rainbow et al. 1998 Thoracica Tetraclita squamosa Total (Ðshell) 6.7 64 Blackmore 1999 Decapoda Callinectes sapidus Gills 56 83 Weinstein et al. 1992 Midgut gland 16 29 Weinstein et al. 1992 Muscle 4.0 6.6 Weinstein et al. 1992 Portunus pelagicus Gills 0.6 1.0 Al-Mohanna & Subrahmanyam 2001 Midgut gland 0.1 1.6 Al-Mohanna & Subrahmanyam 2001 Muscle 0.7 1.9 Balkas et al. 1982, Al-Mohanna & Subrahmanyam 2001 Nephrops norvegicus Exoskeleton 223 304 Eriksson & Baden 1998 Gills 58 1560 Eriksson & Baden 1998 Haemolymph 3.3 4.3 Eriksson & Baden 1998

Freshwater Decapoda Cambarus bartonii Total 52 68 513 Alikhan et al. 1990 Exoskeleton 32 102 248 Alikhan et al. 1990, Young & Harvey 1991 Midgut gland 11 59 337 Alikhan et al. 1990 Orconectes virilis Exoskeleton 86 106 Young & Harvey 1991 Gills 23 36 Young & Harvey 1991 Muscle 6.0 4.5 Young & Harvey 1991 Potamonautes warreni Total 239 662 Sanders et al. 1998 Exoskeleton 340 1203 Steenkamp et al. 1994 Gills 508 886 Steenkamp et al. 1994 Midgut gland 374 773 Steenkamp et al. 1994 Muscle 87 168 Steenkamp et al. 1994

Notes: All concentrations are given as mean µg Mn gÐ1 dry weight tissue, except haemolymph which is in wet weight.

through the gills (Rankin et al. 1982). The diffusion over the gill membrane is dependent on the concentration gradient of free metal ions. Crustaceans may accumulate essential as well as non- essential metals above the concentration of the medium as the metals may bind to e.g., blood proteins and thus maintain an inward flux (Baden & Neil 1998). The mean Mn concentration in animals from pristine areas is 100 µg gÐ1 dw, but varies from 0.6Ð508 µg gÐ1 dw (Table 1). During hypoxia in the SE Kattegat, Sweden, in 1995, the mean gill concentration of Mn in Norway lobster (Nephrops norvegicus) increased by 30 times to 1560 µg Mn gÐ1 (Eriksson & Baden 1998; Table 2). The fraction of absorbed and adsorbed Mn is poorly investigated. However, in the SE Kattegat, a black layer of precipitated Mn on the gills was observed indicating that large amounts of adsorbed Mn may occur in the field (Baden et al. 1990). The effects of the precipitated layer of Mn on respiration is not yet investigated but it may hamper a normal function and internal hypoxia may

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Mn (ll) Mn Mn (ll)

O2 uptake/ Gills Stomach Antennulae Immune respiration? Suppression √

No synthesis of Reduced chemo- Haemato- Haemolymph Nerve tissue Hc in hypoxia √ poetic tissue sensitivity √

Midgut Reproductive Muscle gland organs

Storage √ Reduced muscle Fertility ? Necrosis ? function √

Figure 1 Routes and effects of manganese in a crustacean. Dissolved Mn II in water may enter via the gills or antennules or get precipitated on the exoskeleton. Entrance may also occur via the food in a variety of chemical form. Octagonal boxes indicate the route and target tissues of Mn and square boxes indicate the effects of Mn exposure. Observed effects (√) and hypothetical but not yet investigated effects(?).

develop, as has been found by Spicer & Weber (1991) for crustaceans when exposed to other essential metals like Cu and Zn. Since the gills are part of the exoskeleton, changes in Mn concentration during the moult cycle follow the same pattern in these two tissues (Eriksson, 2000a). This is further discussed in the section ‘Exoskeleton’ below.

Haemolymph

Having passed the gill epithelium, Mn is transported in the haemolymph to target tissues either dissolved in the plasma or bound to the haemolymph proteins, predominantly (80Ð90%) to the respiratory protein haemocyanin (Baden & Neil 1998). Exposing N. norvegicus to realistic con- centrations of dissolved Mn (5 and 10 mg Mn lÐ1 for 2 weeks) the haemolymph plasma reaches the same concentration as the ambient water, whereas the Mn concentrations of the haemocyanin and whole haemolymph (plasma and haemocyanin) are about twelve and three times higher, respectively (Baden & Neil 1998). However, when N. norvegicus were exposed to Mn concentra- tions of 60 mg Mn lÐ1 for 2 weeks the plasma and whole haemolymph reached only 0.5 and 1.5 times the concentration of the ambient water (Selander 1997). The biological half-life for manganese accumulation in N. norvegicus during exposure to 5 and 10 mg Mn lÐ1 and elimination in undosed sea water is relatively fast in haemolymph (about 24 h for both processes) (Baden et al. 1999). As the competitive binding of metals by organic ligands (the Irving-Williams series) is stronger for Cu2+ than Mn2+ (Rainbow 1997), Mn does not replace Cu as apostethic metal in the haemocyanin, as indicated by a constant Cu concentration with increasing Mn concentration of the haemolymph (Baden & Neil 1998). Removal and displacement of Ca from haemocyanin may change the quaternary structure and thus the functional properties of the haemocyanin (Van Holde & Brenowitz 1981, Brouwer et al. 1983). The binding of Cd and Zn is stronger than Ca and has been shown to replace Ca in the haemolymph of the blue crab, Callinectes sapidus. Even though Mn binds slightly stronger than Ca,

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no change in Ca concentration of whole haemolymph was found in Nephrops norvegicus with increasing exposure to Mn of 60 mg lÐ1 (Selander 1997). This constancy in the whole haemolymph, however, does not rule out the possibility that Mn has displaced Ca from the haemocyanin to the plasma. An important source of Mn in the ocean is from hydrothermal vents. The crustaceans adapted to live close to these vents may hypothetically contain a higher concentration of Mn than non-vent crustaceans. Professor J.J. Childress from the University of California, Santa Barbara, kindly provided the authors with haemolymph from a vent crab, Bythograea thermydon, which was found to have Mn concentrations between 0.44 and 1.6 µg gÐ1 ww. These Mn concentrations are within the range of haemolymph concentration from non-vent crustaceans as seen from Table 1. The max- imum mean Mn concentrations of 7.35 µg g1 ww in a field-caught crustacean (Nephrops norvegicus) is reported from the SE Kattegat following a hypoxic period in 1995 (Eriksson & Baden 1998). The effects of manganese on haemocyanin synthesis and adaptation to hypoxia are described in a subsequent section discussing the midgut gland, as this is the primary organ for haemocyanin synthesis (Taylor & Antiss 1999). The synthesis of haemocytes takes place in the haematopoietic tissue localised as a thin sheet on the dorsal site of the stomach in crustaceans (Chaga et al. 1995). The haemocytes of crustaceans consist of hyaline, semigranular and granular cells playing an important role in, for example, the innate immune defence (Ratcliffe & Rowley 1979, Söderhäll 1981, Söderhäll & Cerenius 1992). Immunotoxicology of invertebrates is an unexplored field and as a result no early investigations can be cited. Recently, Hernroth et al. (2004) discovered that when exposed to 20 mg lÐ1 Mn for 10 days several immunological processes of N. norvegicus were affected. The number of haemocytes decreased by 60%. Despite the great loss of haemocytes, renewal through increased proliferation of the haematopoietic stem cells did not appear to occur. Additionally, maturation of the stem cells to immune-active haemocytes was inhibited in Mn-exposed lobsters (N. norvegicus). To release the prophenoloxidase system (ProPO), which is necessary for the immune defence of arthropods, the granular haemocytes must degranulate. This degranulation activity was also significantly suppressed after Mn treatment. Furthermore, the activation of ProPO by the non-self molecule, lipopolysac- caride, was blocked. Probably Mn replaces Ca and thereby inhibits protein required for mobilisation and activation of the haemocytes. Immune suppression may explain the occurrence of shell disease caused by microbial infection of the exoskeleton in blue crab, Callinectes sapidus, from North Carolina, U.S. (Weinstein et al. 1992). The infection is related to elevated Mn concentrations in the body tissues. Similar findings might explain the high frequency of the parasitic dinoflagellate Hematodinium sp. that has been found in Nephrops norvegicus from the west coast of Scotland (Field et al. 1992). In the same area high concentrations of Mn have been recorded in the tissue of this species (Baden & Neil 1998).

Midgut gland

In contrast to other target tissues, where manganese accumulation reaches an equilibrium deter- mined by the exposure concentration within 5 days, the midgut gland of N. norvegicus continuously accumulates manganese at a relatively slow rate and does not reach equilibrium after a 3-week period of exposure. This slow accumulation to the hepatopancreas has also been observed for zinc in Carcinus maenas by Chan & Rainbow (1993). The elimination rate of manganese from the midgut gland is, however, much faster. The biological half-lives for accumulation and elimination of manganese are about 4 and 1.5 days, respectively (Baden et al. 1999). Insoluble granules containing metals bound with phosphorus or sulphur have been observed in the epithelial cells of the midgut gland (or comparable organ) in many invertebrates (for review see Ahearn et al. 2004). The granules scavenge and detoxify surplus metals, and are later eliminated through exocytosis. Several marine snails have been shown to eliminate manganese this way (Simkiss 1981, Nott &

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Nicolaidou 1994). Although no such granules have yet been described in manganese-rich crustaceans, the surplus of manganese is clearly delivered to the midgut gland for net accumulation as indicated in Rainbow (1997) and Baden et al. (1999). Accumulation is also demonstrated by the relatively high levels of Mn in midgut glands from different species of crustaceans (Table 1). The highest mean tissue concentrations found in the literature are from the midgut glands of a marine hermit crab, Clibanarius erythropus (1596 µg Mn gÐ1 dw) and a freshwater crayfish, Procambarus clarkii (1677 µg Mn gÐ1 dw), both collected in areas with known anthropogenic input (Gherardi et al. 2002, Nott & Nicolaidou 1994). Unfortunately, no background data are available for either of these species which is why they have not been included in Table 2. However, unpublished data on background Mn concentrations in another marine hermit crab, Pagurus bernhardus, varied from 15Ð28 µg Mn gÐ1 dw in the midgut gland (Andersson 1993), and the highest overall midgut gland background concentration published is 374 µg Mn gÐ1 dw in a freshwater crayfish, Potamonautes warreni (Steenkamp et al. 1994; Table 1). The synthesis of haemocyanin is primarily recognised to take place in the midgut gland (Taylor & Antiss 1999, for review). In a recent study the combined and separate effects of hypoxia (2.5 mg lÐ1) and manganese (20 mg lÐ1) on the haemocyanin concentration were investigated after an exposure period of 2 weeks. Crustaceans adapt to hypoxia by increasing or decreasing (depending on the initial value) the haemocyanin concentration, presumingly to an optimal concentration (Spicer & Baden 2001). A simultaneous exposure to manganese affects this adaptation by preventing the synthesis of haemocyanin (Baden et al. 2003).

Muscle

The manganese concentration of the muscle tissue remains relatively constant throughout the moult cycle and is less dependent on the exposure concentration of Mn compared with other tissues (Bryan & Ward 1965, Baden et al. 1995, Baden & Neil 1998, Eriksson & Baden 1998, Bjerregaard & Depledge 2002). This constancy is especially interesting since the muscle is a metabolically active tissue with high mitochondrial content. Calculations indicate that an increase in Mn concentration of muscle tissue after exposure to elevated Mn concentrations can, in principle, be explained by the increase in Mn in the extracellular haemolymph of the muscle tissue (Hille 1992, Baden et al. 1995). A plausible explanation for the relatively stable concentration in the muscle cells themselves is, thus, either that turnover rates of manganese in these cells are high enough to disguise increased uptake (at least for the exposure concentrations that have so far been studied) or that the metal never enters the muscle cells but remains in the extracellular haemolymph. Normal muscle concentrations of Mn lie in the range of 0.4Ð8.0 µg Mn gÐ1 dw with the exception of the extremely high values of 24 µg Mn gÐ1 found in small Carcinus maenas by Bjerregaard & Depledge (2002) and 87 µg Mn gÐ1 found in the freshwater crayfish, Potamonautes warreni by Steenkamp et al. (1994). Many values in the literature are stated as wet weight concentrations with the primary objective being risk assessment of heavy metals in human food. Taken that the daily recommended intake for humans is 2.5Ð5 mg Mn dayÐ1, a person would have to eat ca 1 kg of crustacean meat just to fulfil the daily requirement. Manganese at natural levels in crustaceans is thus not likely to pose a threat for human consumption. When lobsters (Nephrops norvegicus) are exposed to 10 mg Mn gÐ1 their muscle extension and thus most probably (consequently) the swimming capacity is affected as will be discussed under the section ‘Nervous system’.

Exoskeleton

Due to its chemical properties, manganese is found in highest concentrations in the calcified parts of crustaceans, mainly in the exoskeleton, gills and the gastric mill of the stomach (Bryan & Ward

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1965, Baden et al. 1990, 1995, Eriksson & Baden 1998, Eriksson 2000a). Depending on the thickness of an animal’s exoskeleton the vast majority of manganese is found in this tissue, as it contains more than 98% of the total Mn content of the decapod lobsters Homarus gammarus (Bryan & Ward 1965) and Nephrops norvegicus (Baden et al. 1995). The manganese incorporated in the matrix of the exoskeleton is believed to have little effect on the animals. The manganese concentration of the exoskeleton changes during the moult cycle, and lobsters (N. norvegicus) collected in the field show a step-wise increase in average Mn concentration from postmoult, intermoult to premoult (Eriksson & Baden 1998). The crustacean moult cycle is dom- inated temporally by the intermoult phase, with brief periods of postmoult and premoult. There is, however, no correlation between the contemporary environmental Mn(II) concentration of ambient sea water and that of the exoskeleton in field-caught intermoult lobsters (Eriksson & Baden 1998). It was thus proposed that the amount of Mn found in the exoskeleton of intermoult individuals primarily depends on the Mn concentration to which the animals are exposed during the calcification process at postmoult, rather than the current ambient Mn concentrations (Eriksson & Baden 1998, Eriksson 2000a). During growth, the shell of the barnacle Balanus amphitrite has been shown to incorporate Mn in direct proportion to the concentration of the sea water (Hockett et al. 1997). Unlike most crustaceans, the calcified shells in barnacles grow more or less continuously (Bourget & Crisp 1975), thus having continuous calcification. In most crustaceans, however, calcification occurs during a short postmoult period. To test the theory, newly moulted Nephrops norvegicus were exposed to flow-through sea water with <0.06 mg Mn lÐ1 (controls) or 10 mg Mn lÐ1 for 20 days (S.P. Eriksson, unpublished observations). The animals were sacrificed and the Mn concentration was measured in the exoskeleton and in the cast exuviae (exuviae were removed immediately after

moulting, prior to Mn addition). The cast exuviae showed no difference (one factor ANOVA, F1,8 = 0.09, P = 0.77, n = 5) between the control group and the (later) Mn-exposed group; Mn concen- trations were 352 ± 70 and 326 ± 55 (mean ± SE) µg Mn gÐ1 dw, respectively. After 20 days the newly calcified intermoult exoskeletons showed significant differences between the two groups

(one factor ANOVA, F1,8 = 151, P < 0.001, n = 5). The Mn-exposed animals had exoskeletal Mn concentrations of 2524 ± 201 µg Mn gÐ1 dw (mean ± SE) whereas the control animals contained only 44 ± 8 µg Mn gÐ1 dw. In comparison, an earlier study on intermoult animals also exposed to 10 mg Mn lÐ1 dw for 20 days showed a modest increase from 200 µg Mn gÐ1 to 290 µg Mn gÐ1 dw (Baden et al. 1999). The results, though not extensive, thus appear to support the theory that intermoult exoskeleton Mn concentrations are mainly the result of prevailing Mn concentrations during the calcification process. In contrast, the increase from intermoult to premoult found in N. norvegicus is thought to be the result of exoskeletal breakdown (Eriksson 2000a). During premoult, crustaceans degrade and resorb some of the old cuticle. Cuticle components, such as calcium, are stored for later use in hardening of the new ‘shell’ (Aiken & Waddy 1992). The breakdown of the old cuticle results in a decreased dry weight/wet weight ratio which in turn also leads to an apparent increase in Mn concentration from intermoult to premoult (Eriksson 2000a). Moulting has been suggested as one possible way for decapods (Homarus gammarus, Palaemon elegans, Systellaspis debilis) to dispose of excess unwanted metals (Bryan & Ward 1965; Ward 1966; White & Rainbow 1984a,b, 1987; Swift 1992). Although crustaceans on occasion eat part or all of their cast exuviae, preliminary data on Mn uptake from food suggests that Mn incorporated in exoskeletal parts is not easily accessible when ingested, as described in the section of Mn uptake from food. Moulting might thus serve as an important regulator of the Mn content providing there are low Mn(II) concentrations in the water at the time of moult. Manganese precipitations on the hard-shelled exoskeleton are visible as persistent black dots mainly in crevices as observed after hypoxia on Nephrops norvegicus in the SE Kattegat (Baden et al. 1990). Being insoluble, the precipitation of Mn on the exoskeleton is a potential biomarker

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of exposure to Mn either from industry or hypoxia. However, the interindividual variation is high due to patchiness as shown in Baden et al. (1999). The uptake of Mn on mobile appendages of the exoskeleton is higher than on the non-mobile exoskeleton and shows less variability. Baden & Neil (2003) showed a linear time- and dose-dependent uptake of Mn and there was no elimination after 2 weeks of return to undosed sea water.

Female reproductive system and fertilized eggs

Martin (1975) showed that the manganese concentration of the ovary of the green crab (Carcinus maenas) correlated negatively with the Rapport Gonado-Somatique (RGS) gonad index (=matura- tion stage). Other studies on the lobster Nephrops norvegicus have shown that the Mn concentration of the oocytes, during maturation and throughout most of the embryogenesis, remains very stable regardless of ambient Mn concentrations. However, due to stable Mn concentrations but increase in gonad mass over the maturation period of the oocytes, the Mn load of the whole gonad increased over time (Eriksson, 2000b). Egg membranes of decapod crustaceans increase their permeability to water and minerals dramatically just before hatching (Pandian 1970a,b; Petersen & Anger 1997). This increases the internal pressure of the egg and, in combination with the weakening of the shell membrane, is believed to help the larvae to burst the eggshells and hatch. The Mn concentration of eggs from N. norvegicus is stable at around 5.5 µg gÐ1 dw eggÐ1 during the first 6 months of development. At the end of the embryonic development the Mn concentration increases dramatically so that at the time of hatching (approximately 9 months after fertilization) the eggs have reached concentrations of 120 µg gÐ1 dw egg (Table 1). At this late stage the eggshell gives no protection against external Mn, and dissolved Mn(II) passes through the eggshell where it is taken up by the embryo (Eriksson 2000b). Manganese can replace calcium at many sites (Nassrallah-Aboukais et al. 1996), and most of the Mn in aquatic crustaceans is therefore incorporated into calcified regions such as the exoskeleton and the ossicles and teeth of the gastric mill (Bryan & Ward 1965, Eriksson & Baden 1998, Eriksson 2000a, Steenkamp et al. 1994). Since the cuticle of the zoea larva has shown to be poorly calcified (Spicer & Eriksson 2003) the dramatic increase in Mn concentration found in the embryos prior to hatching would most likely not have been caused by Mn being incorporated into the animal’s cuticle (Eriksson 2000b). The hatched larva is a carnivorous zoea with a complete functional alimentary canal and it is therefore more likely that the sudden increase in egg Mn concentration might be explained by the development of the gastric mill in the embryo. Since, many crustacean embryos are brooded externally in an open clutch on the abdomen of the female, they will be exposed to prevailing benthic conditions and the Mn concentration of mature eggs may thus serve as a useful tool to indicate elevated Mn(II) concentrations in the field. This is, of course, dependent on embryonic mortality not being affected, since the female carrier removes dead eggs from the egg mass.

Male reproductive system

In astacidean crustaceans the manganese concentration in male reproductive organs (testis, vas deferens and sperm mass) is relatively high (33.2 µg gÐ1) (as found in N. norvegicus from the field that were not exposed to Mn) compared with the concentration found in other tissues (Eriksson 2000a). This finding may be explained by the large amount of acidic mucopolysaccaride (AMPS) containing condroitin sulphate (cartilage precursor) in the vas deferens (Radha & Subramoniam 1985, Subramoniam 1993). The mucopolysaccaride protects the sperm and makes the main part of the spermatophore delivered to the female spermatheca. The negative charge of this substance attracts the positive charged metals like manganese. Besides, manganese is an important factor in the production of chondroitin sulphate (Leach 1971). After in vitro exposure of N. norvegicus to

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manganese (20 mg Mn lÐ1) for 14 days the accumulation factor was highest in the testis (× 10) reaching 100 µg gÐ1 dw, whereas the concentration in the vas deferens and sperm mass increased from about 80 µg gÐ1 dw to 210 and 140 µg gÐ1 dw, respectively (Krönström 2002). During mating, the male places a spermatophore in the spermatheca (thelycum) of a newly moulted female. The gelatinous component of the spermatophore hardens, protecting the contained spermatozoa. A flap of exoskeleton covers the spermatheca and hardens with the rest of the exoskeleton following mating (Farmer 1974). After manganese exposure (20 mg Mn lÐ1 for 14 days) the spermatophore in the spermatheca showed an increase in Mn concentration from 10 to 50 µg gÐ1 dw (inner part of spermatheca) and 15 to 40 µg gÐ1 dw (outer part of spermatheca). Thus manganese may reach and hypothetically affect the sperm either from the surrounding water through the opening of the spermatheca and/or from the body of the female (Krönström 2002).

Central nervous system

A primary target tissue for Mn is the central nervous system. The accumulation of Mn in the nerve tissue and the effects therein are thus of great importance. The literature on Mn accumulation effects and toxicity in vertebrate nerve systems is extensive (see above), whereas only a few papers on this topic exist for invertebrates. The toxicity of the heavy metals Pb, Hg and Cd on synaptic transmission is reviewed for crustaceans by Devi & Fingerman (1995) and Fingerman et al. (1996). The biological half-life of Mn (after exposure to 5 & 10 ml Mn lÐ1) in the brain and ganglion of N. norvegicus is about 1 day for the accumulation of Mn and 2Ð4 days for Mn elimination, which is slowest from the brain (Baden et al. 1999). The brain and ganglionic chain may contain about 5 µg Mn gÐ1 dw when unexposed whereas the accumulation of Mn by exposed animals resulted in a four times higher concentration in the brain than in the ganglia during exposure and may reach 250 µg Mn gÐ1 dw in the brain when exposed to 10 mg Mn lÐ1 for 3 weeks (Baden & Neil 1998). In the SE Kattegat (Sweden) a concentration of 193 µg Mn gÐ1 in the brain of N. norvegicus has been reported after hypoxic events in the autumn of 1995 (Eriksson & Baden 1998). This could indicate a field exposure to at least 10 mg Mn lÐ1. Accumulated manganese has an impact on neuromuscular performance. In crustacean skeletal muscle, depolarisation involves an inflow of calcium ions rather than sodium ions across the muscle membrane (Fatt & Ginsborg 1958). Manganese ions can suppress muscle excitation (Suarez-Kurz 1979) by acting as a competitive inhibitor to calcium ion flow through calcium channels in the muscle membrane (Hagiwara & Takahashi 1967). The neuromuscular performance of N. norvegicus after manganese exposure was investigated in muscle preparations (Holmes et al. 1999) and in whole animals (Baden & Neil 1998). Low concentrations (ca 1 mg lÐ1) of manganese increased the contractile force of the abdominal superficial flexor muscle preparations whereas concentrations above 5 mg lÐ1 Mn successively decreased the contractile force until total abolition at concentrations above 320 mg lÐ1 (Holmes et al. 1999). Exposure of N. norvegicus for 3 weeks to 10 mg lÐ1 Mn affected the free tail flip swimming by reducing the postflip extension by about 40% whereas the flip flexion was unaffected. The explanation of this difference is probably that the extension involves a chemical neuromuscular synapse that is known to be affected by manganese, whereas the flexion is elicited primarily by an electrical synapse not affected by manganese (Baden & Neil 1998). In decapod crustaceans thin-walled hairs (the aesthetascs) on the first antennae (antennules) are the major chemoreceptor organs. They play a critical role in orientation toward an odour source, and are therefore important in social recognition and food search (Devine & Atema 1982). Each aesthetasc is innervated by over 300 neurones connected to the olfactory neurons of the brain as described for Homarus americanus by Shepheard (1974). The aesthetascs are very sensitive to amino acids and Pearson & Olla (1977) found that blue crabs, Callinectes sapidus, can detect clam extract in concentrations of 10Ð15 g lÐ1. The response of the aesthetasc receptor cells to changes in

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stimulus concentration is enhanced by movement of the antennules known as ‘flicking’ (Schmitt & Ache 1979). Flicking decreases the boundary layer thickness, and provides increased odour access to the receptor cells (Moore et al. 1991). The effect of Mn on chemosensitivity has been investigated in Nephrops norvegicus exposed to combinations of manganese (0, 10, 20, 40 mg Mn lÐ1) and either Ð1 Ð1 normoxia (8.9 mg O2 l ) or hypoxia (1.3 mg O2 l ) for 4 and 10 days (Engdahl 1997). Exposure length as well as Mn concentration up to 20 mg Mn lÐ1 significantly increased the mean flick frequency by about 15Ð25%, whereas the frequency decreased significantly between exposures of 20Ð40 mg Mn lÐ1. When exposed to a combination of hypoxia and increasing Mn concentrations, the flick frequency decreased significantly. It thus seems that manganese affects the perception of odour at the aesthetascs. This could be the result of either physical precipitation of Mn on the aesthetascs, or by chemical action as a neurotoxin in such a way that increasing the flick frequency may compensate for a reduced perception of the stimulus. Hypoxia or unrealistically high Mn concentration seemed to hamper this compensation of increased flicking (Engdahl 1997).

Uptake of manganese from food The ingestion of manganese could potentially be quite significant as Mn can occur in sediment concentrations of up to 80 mg gÐ1 (Elderfield 1976) and large amounts of sediment are frequently found in the stomachs of N. norvegicus (S.P. Baden, unpublished observations). The oral intake of manganese via food is sparsely investigated. Most metals including manganese are bound electro- statically to phosphate or covalently to sulphur and are thus unavailable for digestion. When feeding hermit crabs with the digestive gland of marine snails the metals of these glands were found to go straight through the gut of the hermit crab without being absorbed (Nott & Nicolaidou 1994). In a feeding experiment N. norvegicus, starved for 4 weeks, were individually fed three different diets ad libitum for 2 weeks (Norstedt 2004). The diets (shrimp muscle, shrimp muscle + exo- skeleton, shrimp muscle + sediment containing 1.4, 5.4 and 145 µg Mn gÐ1 dw, respectively) were composed to mirror the natural food selection following Baden et al. (1990). No significant differ- ence in Mn concentration was found in the lobster soft tissue despite the large difference in Mn concentration of the diets offered. The Mn concentrations obtained were normal for lobsters from reference areas and were much lower than the concentrations found in N. norvegicus following hypoxia (Table 2) (Eriksson & Baden 1998, S.P. Baden & S.P. Eriksson, unpublished observations). Uptake from water via the gills thus seems to be the most important path of Mn into aquatic crustaceans during hypoxic situations when bioavailable dissolved Mn is at high concentrations.

Excretion of manganese In aquatic environments the excretion of toxins, including metals, from organisms to the surrounding media is faster than in the terrestrial environment due in part to the large surface of the gills where an exchange occurs between the internal liquid of the haemolymph and the external water of different salinities (Rand et al. 1995). The excretion of metals including Mn from different tissues of aquatic invertebrates is reviewed by Viarengo & Nott (1993). From crustaceans, the excretion of metals to the medium may occur through antennary glands (via the urine), gills, gut and during moulting (e.g., Marsden & Rainbow 2004, for review). The rate and dominant route of excreting excess Mn depends on physical and chemical factors. Excretion of 54Mn from the lobsters Homarus gammarus (Bryan & Ward 1965) and Nephrops norvegicus (Baden et al. 1995) revealed that part of the 54Mn was excreted through the antennary glands and also in the faeces. These routes, however, only accounted for a small portion of the 54Mn lost. Bryan & Ward (1965) estimated the loss by urinary excretion to be 20Ð40%

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of the total 54Mn loss, compared with a maximum of 3% in N. norvegicus. The major portion of loss is suggested to take place via the body surface.

Conclusions Evaluating the literature on the role, routes and effects of manganese in crustaceans shows that manganese, though an essential metal, is also an unforeseen toxic metal in the marine environment. Manganese may occur in toxic concentrations in the bottom water of larger coastal areas after hypoxia or more locally close to industrial sources. Although the uptake and elimination is rapid with a half-life of a couple of days, Mn adversely affects physiological processes and can decrease fitness. Uptake from water seems to be the most important mechanism giving body concentrations above basic Mn requirements. The main target tissues and accumulation levels in different parts of the body have been investigated for many marine and freshwater species indicating that the midgut gland, nerve tissue, blood proteins and parts of the reproductive organs have the highest accumulation factors. The functional effects of manganese are, however, sparsely investigated. Recent results show that several steps in a well-functioning immune defence, the perception of food via chemosensory organs, and normal muscle extension are affected by commonly occurring concentrations of manganese. To get a more complete understanding of this metal in biological systems it is necessary to explore why Mn gets accumulated more in brain tissue than other nerve tissues, why high concentrations of Mn accumulate into the vas deferens wall and sperm mass, and

how sperm viability is affected. Is respiration affected by a precipitation of MnO2 covering the gills and by elevated Mn concentrations in the oxygen-carrying protein (haemocyanin) and does Mn induce hemocytopenia, etc.? Human concern about metals has mainly focused on highly toxic, rare and unessential heavy metals, like Pb, Hg and Cd. Due to its common occurrence and possibly also because it is essential, the potential danger of manganese has been neglected. One has to remember that any metal has the potential to cause biological damage, it is just a matter of reaching a high enough concentration. Manganese is widespread and found in very high concentrations, in particular in soft aquatic sediments. Its bioavailability increases as the result of human impact, and it can become accumu- lated in biota where it has the potential to cause damage. As more about the mechanisms underlying metal handling by animals is understood, and the details of human impact on the environment are further elucidated, more attention is likely to be given to previously overlooked metals, like manganese.

Acknowledgements We are sincerely grateful to Prof. Robert C. Aller, Prof. Helge H. Baden, Dr. Bodil Hernroth and Prof. Philip S. Rainbow for inspiration and encouragement during our work and for valuable comments on the manuscript of this review. Financial support was received from The Swedish Research Council for Environment, Agri- cultural Sciences and Spatial Planning (FORMAS no. 22.3/2001-1077) to SPB and from The Natural Swedish Research Council (VR no. 621-2001-3670) to SPE.

References

Ahearn, G.A., Mandal, P.K. & Mandal, A. 2004. Mechanisms of heavy-metal sequestration and detoxification in crustaceans: a review. Journal of Comparative Physiology B 174, 439Ð452. Aiken, D.E. & Waddy, S.L. 1992. The growth process in crayfish. Reviews in Aquatic Sciences 6, 335Ð381.

76 7044_C002.fm Page 77 Monday, April 17, 2006 1:37 PM

ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS

Akyuz, T., Erkan, B.M. & Bassari, A. 2001. Radioisotope excited X-ray flurescence analysis of Asellus aquaticus Crustacea: Isopoda from Istanbul as an indicator of environmental metal pollution. Journal of Radioanalytical and Nuclear Chemistry 249, 649Ð651. Alikhan, M.A., Bagatto, G. & Zia, S. 1990. The crayfish as a “biological indicator” of aquatic contamination by heavy metals. Water Research 24, 1069Ð1076. Aller, R.C. 1994. The sedimentary Mn cycle in Long Island Sound: its role as intermediate oxidant and the

influence of bioturbation, O2, and Corg flux on diagenetic reaction balances. Journal of Marine Research 52, 259Ð295. Al-Mohanna, S.Y. & Subrahmanyam, M.N.V. 2001. Flux of heavy metal accumulation in various organs of the intertidal marine blue crab, Portunus pelagicus L. from the Kuwait coast after the Gulf war. Environment International 27, 321Ð326. Andersson, I. 1993. Fördelning av koppar och mangan i eremitkräftan Pagurus bernhardus exponerad för syrebrist. (Distribution of copper and manganese in the hermit crab Pagurus bernhardus exposed to hypoxia). MSc Thesis, Department of Zooecology, Göteborg University, Sweden, In Swedish. Anonymous 2005. The International Manganese Institute (IMnI). Paris, France. Online. Available at www.man- ganese.org/reserves.php and www.manganese.org/intro.php (accessed 4 September 2005). Aschner, M. & Aschner, J.L. 1991. Manganese neurotoxicity: cellular effects and blood-brain barrier transport. Neuroscience and Biobehavioral Revues 15, 333Ð340. Baden, S.P., Depledge, M.H. & Hagerman, L. 1994. Glycogen depletion and altered copper and manganese handling in Nephrops norvegicus following starvation and exposure to hypoxia. Marine Ecology Progress Series 103, 65Ð72. Baden, S.P., Eriksson, S.P. & Gerhardt, L. 1999. Accumulation and elimination kinetics of manganese from different tissues of the Norway lobster Nephrops norvegicus (L.). Aquatic Toxicology 46, 127Ð137. Baden, S.P., Eriksson, S.P. & Weeks, J.M. 1995. Uptake, accumulation and regulation of manganese during experimental hypoxia and anoxia in the decapod Nephrops norvegicus (L.). Marine Pollution Bulletin 31, 93Ð102. Baden, S.P., Håkansson, C.L.J. & Spicer, J.I. 2003. Between-individual variation in haemocyanin concentra- tions in the Norway lobster Nephrops norvegicus following exposure to hypoxia and manganese. Marine Biology 143, 267Ð273. Baden, S.P. & Neil, D.M. 1998. Accumulation of manganese in the haemolymph, nerve and muscle tissue of Nephrops norvegicus (L.) and its effect on neuromuscular performance. Comparative Biochemistry and Physiology 119A, 351Ð359. Baden, S.P. & Neil, D.M. 2003. Manganese accumulation by the antennule of the Norway lobster Nephrops norvegicus (L.) as a biomarker of hypoxic events. Marine Environmental Research 55, 59Ð71. Baden, S.P., Pihl, L. & Rosenberg, R. 1990. Effects of oxygen depletion on the ecology, blood physiology and fishery of the Norway lobster, Nephrops norvegicus. Marine Ecology Progress Series 67, 141Ð155. Balkas, T.I., Tugrul, S. & Salihoglu, I. 1982. Trace metal levels in fish and Crustacea from northeastern Mediterranean coastal waters. Marine Environmental Research 6, 281Ð289. Balzer, W. 1982. On the distribution of iron and manganese at the sediment/water interface: thermodynamic versus kinetic control. Geochimica et Cosmochimica Acta 46, 1153Ð1161. Bjerregaard, P. & Depledge, M.H. 2002. Trace metal concentrations and contents in the tissue of the shore crab Carcinus maenas: effects of size and tissue hydration. Marine Biology 141, 741Ð752. Blackmore, G. 1999. Temporal and spatial biomonitoring of heavy metals in Hong Kong coastal waters using Tetraclita squamosa. Environmental Pollution 106, 273Ð283. Blasco, J., Arais, A.M. & Saenz, V. 2002. Heavy metal concentrations in Squilla mantis (L.) (Crustacea, Stomatopoda) from the Gulf of Cádiz: evaluation of the impact of the Aznalcollar mining spill. Environmental International 28, 111Ð116. Bourget, E. & Crisp, D.J. 1975. Factors affecting deposition of the shell in Balanus balanoides. Journal of the Marine Biological Association of the United Kingdom 55, 231Ð249. Brouwer, M., Bonaventura, C. & Bonaventura, J. 1983. Metal ion interactions with Limulus polyphemus and Callinectes sapidus haemocyanins: stoichiometry and structural and functional consequences of cal- cium (II), cadmium (II), zinc (II) and mercury (II). Biochemistry 22, 4713Ð4723.

77 7044_C002.fm Page 78 Monday, April 17, 2006 1:37 PM

SUSANNE P. BADEN & SUSANNE P. ERIKSSON

Bryan, G.W. & Ward, E. 1965. The absorption and loss of radioactive and non-radioactive manganese by the lobster, Homarus vulgaris. Journal of the Marine Biological Association of the United Kingdom 45, 65Ð95. Butt, A.M., Hargittai, P.T. & Lieberman, E.M. 1990. Calcium-dependent regulation of potassium permeability in the glial perineurum Blood-Brain-Barrier of the crayfish. Neuroscience 38, 175Ð185. Canfield, D.E., Thamdrup, B. & Hansen, J.W. 1993. The anaerobic degradation of organic matter in Danish coastal sediments: Fe reduction, Mn reduction, and sulfate reduction. Geochimica et Cosmochimica Acta 57, 3867Ð3884. Chaga, O., Lignell, M. & Söderhäll, K. 1995. The haemopoietic cells of the freshwater crayfish, Pacifastacus leniusculus. Animal Biology 4, 59Ð70. Chan, H.M. & Rainbow, P.S. 1993. The accumulation of dissolved zinc by the shore crab Carcinus maenas (L.) Ophelia 38, 13Ð30. Chiarandini, D.J., Reuben, J.P., Brandt, P.W. & Grundfest, H. 1970. Effects of caffeine on crayfish muscle fibres. I. Activation of contraction and induction of Ca spike electrogenesis. Journal of General Physiology 55, 640Ð664. Cotzias, J.C. 1958. Manganese in health and disease. Physiological Revue 38, 503Ð532. Couper, J. 1837. On the effects of black oxide of manganese when inhaled into the lungs. British Annals of Medicine, Pharmacy, Vital Statistics, and General Science (London) 1, 41Ð42. da Silva, J.J.R.F. & Williams, J.P. 1991. The Biological Chemistry of the Elements Ð The Inorganic Chemistry of the Elements. Oxford, England: Clarendon Press. Davis, J.M. 1998. Methylcyclopentadienylmanganese tricarbonyl: health risk uncertainties and research direc- tions. Environmental Health Perpectives 106, suppl 1, 191Ð201. Dehairs, F., Baeyens, W. & Van Gansbeke, D. 1989. Tight coupling between enrichment of iron and manganese in North Sea suspended matter and sedimentary redox processes: evidence for seasonal variability. Estuarine Coastal and Shelf Science 29, 457Ð471. Delahayes, G.F. 1975. Depolarisation-induced movement of Mn2+ across the cell membrane in the guinea-pig myocardium. Circulation Research 36, 713Ð718. Devi, M. & Fingerman, M. 1995. Inhibition of acetylcholinesterase activity in the central nervous system of the red swamp crayfish, Procambarus clarkii, by mercury, cadmium, and lead. Bulletin of Environ- mental Contamination and Toxicology 55, 746Ð750. Devine, D.V. & Atema, J. 1982. Function of chemoreceptor organs in spatial orientation of the lobster, Homarus americanus: differences and overlap. Biological Bulletin (Woods Hole) 163, 144Ð153. Drava, G., Capelli, R., Mingati, V., De Pellegrini, R., Relini, L.O. & Ivaldi, M. 2004. Trace elements in the muscle of red shrimp Aristeus antennatus, Risso, 1816 Crustacea, Decapoda from Ligurian sea NW Mediterranean: variations related to the reproductive cycle. Science of the Total Environment 321, 87Ð92. Elderfield, H. 1976. Manganese fluxes to the oceans. Marine Chemistry 4, 103Ð132. Engdahl, S. 1997. Effects of manganese and hypoxia on the chemoreception behaviour of the Norway lobster, Nephrops norvegicus. MSc Thesis in Marine Zoology, Department of Marine Ecology, Göteborg University, Sweden. Eriksson, S.P. 2000a. Temporal variations of manganese in the haemolymph and tissues of the Norway lobster, Nephrops norvegicus (L.). Aquatic Toxicology 48, 297Ð307. Eriksson, S.P. 2000b. Variations of manganese in the eggs of the Norway lobster, Nephrops norvegicus. Aquatic Toxicology 48, 291Ð295. Eriksson, S.P. & Baden, S.P. 1998. Manganese in the haemolymph and tissues of the Norway lobster, Nephrops norvegicus (L.), along the Swedish west coast, 1993Ð95. Hydrobiologia 375Ð376, 255Ð264. Farmer, A.S.D. 1974. Reproduction in Nephrops norvegicus (Decapoda: Nephropidae). Journal of Zoology 174, 161Ð183. Fatt, P. & Ginsborg, B.L. 1958. The ionic requirements for the production of action potentials in crustacean muscle fibers. The Journal of Physiology, London 142, 516Ð543. Faust, S.D. & Aly, O.M. 1983. Chemistry of Water Treatment. Boston, MA: Butterworths. Fialkowski, W., Rainbow, P.S., Smith, B.D. & Zmudzinski, L. 2003. Seasonal variation in trace metal con- centrations in three talitrid amphipods from the Gulf of Gdansk, Poland. Journal of Experimental Marine Biology and Ecology 288, 81Ð93.

78 7044_C002.fm Page 79 Monday, April 17, 2006 1:37 PM

ROLE, ROUTES AND EFFECTS OF MANGANESE IN CRUSTACEANS

Field, R.H., Chapman, C.J., Taylor, A.C., Neil, D.M. & Vickerman, K. 1992. Infection of the Norway lobster Nephrops norvegicus by a Hematodinium-like species of dinoflagellate on the west coast of Scotland. Diseases of Aquatic Organisms 13, 1Ð15. Fingerman, M., Devi, M., Reddy, P.S. & Katyayani, R. 1996. Impact of heavy metal exposure on the nervous system and endocrine-mediated processes in crustaceans. Zoological Studies 35, 1Ð8. Fukunda, J. & Kawa, K. 1977. Permeation of manganese, cadmium, zinc, beryllium through calcium channels of insect muscle membrane. Science 196, 309Ð311. Gavin, C.E., Gunter, K.K. & Gunter, T.E. 1999. Manganese and calcium transport in mitochondria implications for manganese toxicity. Neurotoxicology 20, 445Ð453. Gerber, G.B., Léonard, A. & Hantson, P. 2002. Carcinogenicity, mutagenicity and teratogenicity of manganese compounds. Critical Reviews in Oncology and Haematology 42, 25Ð34. Gherardi, F., Barbaresi, S., Vaselli, O. & Bencini, A. 2002. A comparison of trace metal accumulation in indigenous and alien freshwater macro-decapods. Marine and Freshwater Behaviour and Physiology 35, 179Ð188. Gräslund, S. & Bengtsson B.-E. 2001. Chemicals and biological products used in southeast Asian shrimp farming, and their potential impact on the environment — a review. The Science of the Total Envi- ronment 280, 93Ð131. Hagiwara, S. & Miyazaki, S. 1977. Ca and Na spikes in egg cell membrane. Progress in Clinical Biological Research 15, 147Ð158. Hagiwara, S. & Nakajima, S. 1966. Differences in Na2+ and Ca2+ spikes as examined by application of tetrodotoxin, procaine and manganese ions. Journal of General Physiology 49, 793Ð806. Hagiwara, S. & Takahashi, K. 1967. Surface density of calcium ions and calcium spikes in the barnacle muscle fibre membrane. Journal of General Physiology 50, 583Ð601. Hall, I.R., Hydes, D.J., Statham, P.J. & Overnell, J. 1996. Dissolved and particulate trace metals in a Scottish Sea Loch: an example of a pristine environment? Marine Pollution Bulletin 32, 846Ð854. Hendrickx, M.E., Paez-Osuna, F. & Zazueta-Padilla, H.M. 1998. Biology and biochemical composition of the deep-water shrimp Heterocarpus vicarius Faxon, Crustacea: Decapoda: Caridea: Pandalidae from the Southeastern gulf of California, Mexico. Bulletin of Marine Science 63, 265Ð275. Henriksson, J., Tallkvist, J. & Tjälve, H. 1999. Transport of manganese via the olfactory pathway in rats: dosage dependency of the uptake and subcellular distribution of the metal in the olfactory epithelium and the brain. Toxicology and Applied Pharmacology 156, 119Ð128. Hernandez, E.H., Discalzi, G., Dassi, P., Jarre, L. & Pira, E. 2003. Manganese intoxication: the cause of an inexplicable epileptic syndrome in a 3 year old child. Neurotoxicology 24, 633Ð639. Hernroth, B., Baden, S.P., Holm, K., Andrén, T. & Söderhäll, I. 2004. Manganese induced immunosupression of the lobster Nephrops norvegicus (L.). Aquatic Toxicology 70, 223Ð231. Heu, M.-S., Kim, J.-S. & Shahidi, F. 2003. Components and nutritional quality of shrimp processing by- products. Food Chemistry 82, 235Ð242. Hille, B. 1992. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer Associates Incorporated. Hirata, Y. 2002. Manganese-induced apoptosis in PC12 cells. Neurotoxicology and Teratology 24, 639Ð653. Hockett, D., Ingram, P. & LeFurgey, A. 1997. Strontium and manganese uptake in the barnacle shell: electron probe microanalysis imaging to attain fine temporal resolution of biomineralization activity. Marine Environmental Research 43, 131Ð143. Holmes, J.M., Gräns, A.-S., Neil, D.M., & Baden, S.P. 1999. Effects of the metal ions Mn2+ and Co2+ on muscle contraction in the Norway lobster, Nephrops norvegicus. Journal of Comparative Physiology B 169, 402Ð410. Iregren, A. 1990. Physiological test performance in foundry workers exposed to low levels of manganese. Neurotoxicology and Teratology 12, 673Ð675. Johnson, C.A., Ulrich, M., Sigg, L. & Imboden, D.M. 1991. A mathematical model of the manganese cycle in a seasonally anoxic lake. Limnology and Oceanography 7, 1415Ð1426. Jorhem, L., Engman, J., Sundstrom, B. & Thim, A.M. 1994. Trace elements in crayfish: regional differences and changes induced by cooking. Archives of Environmental Contamination and Toxicology 26, 137Ð142. Katz, B. & Miledi, R. 1969. The effect of divalent cations on transmission in the squid giant synapse. Pubblicazioni della Stazione Zoologica di Napoli 37, 303Ð310.

79 7044_C002.fm Page 80 Monday, April 17, 2006 1:37 PM

SUSANNE P. BADEN & SUSANNE P. ERIKSSON

Kress, N., Hornung, H. & Herut, B. 1998. Concentrations of Hg, Cd, Cu, Zn, Fe and Mn in deep-sea benthic fauna from the southeastern Mediterranean sea: a comparison study between fauna collected at a pristine area and at two waste disposal sites. Marine Pollution Bulletin 36, 911Ð921. Krönström, J. 2002. A study of the reproductive system in the Norway lobster, Nephrops norvegicus — Accumulation of manganese and acrosome reaction. MSc Thesis, Department of Marine Ecology, Göteborg University, Sweden. Laslett, R.E. & Balls, P.W. 1995. The behaviour of dissolved Mn, Ni and Zn in the Forth, an industrialised, partially mixed estuary. Marine Chemistry 48, 311Ð328. Leach, R.M. 1971. Role of manganese in mucopolysaccaride metabolism. Federation Proceedings 30, 991Ð994. Luk, E.E. & Culotta, V.C. 2001. Manganese superoxide dismutase in Saccaromyces cerevisiae acquires its metal co-factor through a pathway involving the Nramp metal transporter, Smf2p. Journal of Biological Chemistry 276, 47,556Ð47,562. Magnusson, K., Ekelund, R., Dave, G., Granmo, Å., Förlin, L., Wennberg, L., Samuelsson, M.-O., Berggren, M. & Brorström-Lundén, E. 1996. Contamination and correlation with toxicity of sediment samples from the Skagerrak and Kattegat. Journal of Sea Research 35, 223Ð234. Marsden, I.D. & Rainbow P.S. 2004. Does the accumulation of trace metals in crustaceans affect their ecology — the amphipod example? Journal of Experimental Marine Biology and Ecology 300, 373Ð408. Martin, J.-L.M. 1974. Metals in Cancer irroratus (Crustacea: Decapoda): concentrations, concentration factors, discrimination factors, correlations. Marine Biology 28, 245Ð251. Martin, J.-L.M. 1975. Étude comparée du métabolisme et des facteurs de concentration de Fe, Cu, Zn, Mn, Co et Mg dans l’ovaire de Carcinus maenas et Cancer irroratus durant l’ovogenése. Cahiers de Biologie Marine 16, 149Ð157. Martin, J.-L.M. 1976. Le métabolisme du manganése chez Cancer irroratus Say, 1817, Crustacé, Décapode. Cahiers de Biologie Marine 17, 359Ð373. Martin, J.-L.M. & Ceccaldi, H.J. 1976. Métabolisme de Fe, Cu, Zn, Mg, Mn et Co dans les œufs de Cancer irroratus Crustacé Décapode. Competes Rendus des Seances de la Societe Biologie et de ses Filiales 170, 157Ð162. Mena, I., Marin, O., Fuenzalida, S. & Cotzias, G.C. 1967. Chronic manganese poisoning-clinical picture and manganese turnover. Neurology 17, 128Ð136. Moore, P., Atema, J. & Gerhardt, G.A. 1991. Fluid dynamics and microscale chemical movement in the chemosensory appendages of lobster Homarus americanus. Chemical Senses 16, 663Ð674. Mounier, Y. & Vassort, G. 1975. Initial and delayed membrane currents in crab muscle fibre under voltage- clamp conditions. The Journal of Physiology, London 251, 589Ð608. Nassrallah-Aboukais, N., Boughriet, A., Fischer, J.C., Wartel, M., Langelin, H.R. & Aboukais, A. 1996. Electron paramagnetic resonance EPR study of Cu2+ and Mn2+ ions interacting as probes with calcium carbonate during the transformation of vaterite into cubic calcite. Journal of the American Chemical Society — Faraday Transactions 92, 3211Ð3216. Nieboer, E. & Richardson, D.H.S. 1980. The replacement of the nondescript “heavy metals” by a biologically and chemically significant classification of metal ions. Environmental Pollution 1B, 3Ð26. Normandin, L., Carrier, G., Gardiner, P.F., Kennedy, G., Hazell, A.S., Mergler, D., Butterworth, R.F., Philippe, S. & Zayed, J. 2002. Assessment of bioaccumulation, neuropathology, and neurobehaviour following subchronic 90 days inhalation in Sprague-Dawley rats exposed to manganese phosphate. Toxicology and Applied Pharmacology 183, 135Ð145. Norstedt, M. 2004. Uptake of manganese through experimental feeding in Norway lobster, Nephrops norveg- icus. MSc Thesis, Department of Marine Ecology, Göteborg University, Sweden. Nott, J.A. & Nicolaidou, A. 1994. Variable transfer of detoxified metals from snails to hermit crabs in marine food chains. Marine Biology 120, 369Ð377. Ochi, R. 1970. The slow inward current and the action of manganese ions in guinea-pig’s myocardium. Pflügers Archives 316, 81Ð94. Ochi, R. 1975. Manganese action potentials in mammalian cardiac muscle. Experientia 31, 1048Ð1049.

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Okamoto, H., Takahashi, K. & Yamashita, N. 1977. Ionic currents through the membrane of the mammalian oocyte and their comparison with those in the tunicate and sea urchin. The Journal of Physiology, London 267, 465Ð495. Paez-Osuna, F., Perez-Gonzalez, R., Izaguirre-Fierro, H., Zazueta-Padilla, M. & Flores-Campana, L.M. 1995. Trace metal concentrations and their distribution in the lobster Panulirus inflatus Bouvier, 1895, from the Mexican Pacific coast. Environmental Pollution 90, 163Ð170. Palade, P.T. & Almers, W. 1978. Slow Na and Ca currents across the membrane of frog skeletal muscle fibres. Biophysical Journal 21, 168a. Pandian, T.J. 1970a. Ecophysiological studies on the developing eggs and embryos of the European lobster Homarus gammarus. Marine Biology 5, 154Ð167. Pandian, T.J. 1970b. Yolk utilization and hatching time in the Canadian lobster Homarus americanus. Marine Biology 7, 249Ð254. Pearson, W.H. & Olla, B.L. 1977. Chemoreception in the blue crab, Callinectes sapidus. Biological Bulletin (Woods Hole) 153, 346Ð354. Petersen, S. & Anger, K. 1997. Chemical and physiological changes during the embryonic development of the spider crab, Hyas araneus L. Decapoda: Majidae. Comparative Biochemistry and Physiology B 117, 299Ð306. Purdey, M. 2000. Ecosystems supporting clusters of sporadic TSEs demonstrate excesses of theradical- generating divalent cation manganese and deficiencies of antioxidant cofactors Cu, Se, Fe, Zn. Medical Hypothesis 54, 278Ð306. Radha, T. & Subramoniam, T. 1985. Origin and nature of spermatophoric mass of the spiny lobster Panulirus homarus. Marine Biology 86, 13Ð19. Rainbow, P.S. 1992. The significance of accumulated heavy metal concentration in marine organisms. In Proceedings of a Bioaccumulation Workshop. A.G. Miskiewicz (ed.), Australia, Sydney: Water Board and Australian Marine Sciences Association Incorporated, 1Ð13. Rainbow, P.S. 1997. Trace metal accumulation in marine invertebrates: marine biology or marine chemistry? Journal of the Marine Biological Association of the United Kingdom 77, 195Ð210. Rainbow, P.S. & Blackmore, G. 2001. Barnacles as biomonitors of trace metal availabilities in Hong Kong coastal waters: changes in space and time. Marine Environmental Research 51, 441Ð463. Rainbow, P.S., Fialkowski, W. & Smith, B.D. 1998. The sandhopper Talitrus saltator as a trace metal biomonitor in the Gulf of Gdansk, Poland. Marine Pollution Bulletin 36, 193Ð200. Rainbow, P.S., Smith, B.D. & Lau, S.S.S. 2002. Biomonitoring of trace metal availabilities in the Thames estuary using a suite of littoral biomonitors. Journal of the Marine Biological Association of the United Kingdom 82, 793Ð799. Rand, G.M., Wells, P.G., & McCarthy, L.S. 1995. Introduction to aquatic toxicology. In Fundamentals of Aquatic Toxicology, 2nd edition, G.M. Rand & S.R.C Petrocelli (eds), Bristol (Philadelphia), PA: Taylor and Francis. Rankin, J.C., Stagg, R.M. & Bolis, L. 1982. Effects of pollutants on gills. In Gills, D.F. Houlihan et al. (eds), Cambridge (Cambridgeshire); New York: Press syndicate of the University of Cambridge, 207Ð219. Ratcliffe, N.A. & Rowley, A.R. 1979. A comparative synopsis of the structure and function of the blood cells of insects and other invertebrates. Developmental and Comparative Immunology 3, 189. Ridout, P.S., Rainbow, P.S., Roe, H.S.J. & Jones, H.R. 1989. Concentrations of V, Cr, Mn, Fe, Ni, Co, Cu, Zn, As and Cd in mesopelagic crustaceans from the North East Atlantic Ocean. Marine Biology 100, 465Ð471. Ross, W.N. & Stuart, A.E. 1978. Voltage sensitive calcium channels in the presynaptic terminals of a detri- mentally conducting photoreceptor. The Journal of Physiology, London 274, 173Ð191. Sanders, M.J., DuPreez, H.H. & VanVuren, J.H.J. 1998. The freshwater river crab, Potamonautes warreni, as a bioaccumulative indicator of iron and manganese pollution in two aquatic systems. Ecotoxicology and Environmental Safety 41, 203Ð214. Saric, M. 1986. Manganese. In Handbook on the Toxicology of Metals, Vol. 2 — Specified Metals. L. Friberg et al. (eds), Amsterdam: Elsevier, 354Ð386. Schmitt, B.C. & Ache, B.W. 1979. Olfactory: response of a decapod crustacean are enhanced by flicking. Science 205, 204Ð206.

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Selander, E. 1997. Effects of hypoxia and manganese on mortality, glycogen utilisation, and calcium homeo- stasis of Norway lobster, Nephrops norvegicus (L.) MSc Thesis, Department of Marine Ecology, Göteborg University, Sweden. Shepheard, P. 1974. Chemoreception in the antennule of the lobster, Homarus americanus. Marine and Freshwater Behaviour and Physiology 2, 262Ð273. Shukla, G.S. & Singhal, R.L. 1984. The present status of biological effects of toxic metals in the environment: lead, cadmium and manganese. Canadian Journal of Physiology and Pharmacology 62, 1015Ð1031. Simkiss, K. 1979. Metal ions in cells. Endeavour, New Series 3, 2Ð6. Simkiss, K. 1981. Cellular discrimination processes in metal accumulation cells. Journal of Experimental Biology 94, 317Ð327. Simkiss, K. & Taylor, M.G. 1989. Metal fluxes across the membranes of aquatic organisms. Aquatic Sciences 1, 173Ð188. Söderhäll, K. 1981. Fungal cell wall beta-1,3-glucans induce clotting and phenoloxidase attachment to foreign surfaces of crayfish haemocyte lysate. Developmental and Comparative Immunology 5, 565Ð573. Söderhäll, K. & Cerenius, L. 1992. Crustacean immunity. Annual Review of Fish Diseases 2, 3Ð23. Spicer, J.I. & Baden, S.P. 2001. Environmental hypoxia and haemocyanin variability in Norway lobsters Nephrops norvegicus L. Marine Biology 139, 727Ð734. Spicer, J.I. & Eriksson, S.P. 2003. Does the development of respiratory regulation always accompany the transition from pelagic larvae to benthic fossorial postlarvae in the Norway lobster Nephrops norveg- icus L. Journal of Experimental Marine Biology and Ecology 295, 219Ð243. Spicer, J.I. & Weber, R.E. 1991. Respiratory impairment in crustaceans and molluscs due to exposure to heavy-metals. Comparative Biochemistry and Physiology 100C, 339Ð342. Steenkamp, V.E., du Preez, H.H., Schoonbee, H.J. & van Eeden, P.H. 1994. Bioaccumulation of manganese in selected tissues of the freshwater crab, Potamonautes warreni (Calman), from industrial and mine- polluted freshwater ecosystems. Hydrobiologia 288, 137Ð150. Suarez-Kurz, G. 1979. The role of calcium in exitation-contraction sampling in crustacean muscle fibres. Canadian Journal of Physiology and Pharmacology 60, 446Ð458. Subramoniam, T. 1993. Spermatophores and sperm transfer in marine crustaceans. Advances in Marine Biology 29, 129Ð214. Swift, D.J. 1992. The accumulation of plutonium by the European lobster Homarus gammarus (L.). Journal of Environmental Radioactivity 16, 1Ð24. Takeda, K. 1967. Permeability changes associated with the action potential in procaine-treated crayfish abdominal muscle fibres. Journal of General Physiology 50, 1049Ð1074. Taylor, H.H. & Antiss, J.M. 1999. Copper and haemocyanin dynamics in aquatic invertebrates. Marine and Freshwater Research 50, 907Ð931. Tjälve, H., Henriksson, J., Tallkvist, J., Larsson, B.S. & Lindquist, N.G. 1996. Uptake of manganese and cadmium from the nasal mucosa into the central nervous systemvia olfactory pathways in rats. Pharmacology and Toxicology 79, 347Ð356. Tjälve, H., Mejàre, C. & Borg-Neczak, K. 1995. Uptake and transport of manganese in primary and secondary olfactory neurones in Pike. Pharmacology and Toxicology 77, 23Ð31. Trefry, J.H., Presley, B.J., Keeney-Kennicutt, W.L. & Trocine, R.P. 1984. Distribution and chemistry of manganese, iron, and suspended particulates in Orca Basin. Geo-Marine Letters 4, 125Ð130. Van Holde, K.E. & Brenowitz, M. 1981. Subunit structure and physical properties of the haemocyanin of the giant isopod Bathynomus giganteus. Biochemistry 20, 5232Ð5239. Viarengo, A. & Nott, J.A. 1993. Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comparative Biochemistry and Physiology 104C, 355Ð372. Visuthismajarn, P., Vitayavirasuk, B., Leeraphante, N. & Kietpawpan, M. 2005. Ecological risk assessment of abandoned shrimp ponds in southern Thailand. Environmental Monitoring and Assessment 104, 409Ð418. Ward, E.E. 1966. Uptake of plutonium by the lobster Homarus vulgaris. Nature 209, 625Ð626. Weinstein, J.E., West, T.L. & Bray, J.T. 1992. Shell disease and metal content of blue crabs, Callinectes sapidus, from the Albemarle-Pamlico estuarine system, North Carolina. Archives of Environmental Contamination and Toxicology 23, 355Ð362.

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White, A., Handler, P. & Smith, E.L. 1973. Principles of Biochemistry. Tokyo: McGraw-Hill Kogakusha, Ltd. Fifth edition. White, S.L. & Rainbow, P.S. 1984a. Regulation of zinc concentration by Palaemon elegans Crustacea: Decapoda: zinc flux and effects of temperature, zinc concentration and moulting. Marine Ecology Progress Series 16, 135Ð147. White, S.L. & Rainbow, P.S. 1984b. Zinc flux in Palaemon elegans (Crustacea: Decapoda): moulting, individual variation and tissue distribution. Marine Ecology Progress Series 19, 153Ð166. White, S.L. & Rainbow, P.S. 1987. Heavy metal concentrations and size effects in the mesopelagic decapod Systellaspis debilis. Marine Ecology Progress Series 37, 147Ð151. Williams, R.J.P. 1981. Natural selection of the chemical elements. Proceedings of the Royal Society of London. Biological Sciences 213, 361Ð397. Wollast, R., Billen, G. & Duinker, J.C. 1979. Behaviour of manganese in the Rhine and Scheldt estuaries. I. Physico-chemical aspects. Estuarine and Coastal Marine Science 9, 161Ð169. Xiao, X.H. & Bevan, J.A. 1994. Pharmacological evidence that flow-induced and potassium-induced contrac- tion of rabbit facial vein may involve the same calcium-entry pathway. Journal of Pharmacology and Experimental Therapeutics 268, 25Ð31. Yamagishi, S. 1973. Manganese-dependant action potentials in intracellularly perfused squid giant axons. Proceedings of the Japan Academy. Ser. B. Physical and Biological Sciences 49, 218Ð222. Young, L.B. & Harvey, H.H. 1991. Metal concentrations in crayfish tissues in relation to lake pH and metal concentrations in water and sediments. Canadian Journal of Zoology 69, 1076Ð1082.

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Oceanography and Marine Biology: An Annual Review, 2006, 44, 85-121 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis

MACROFAUNAL BURROWING: THE MEDIUM IS THE MESSAGE

KELLY M. DORGAN1, PETER A. JUMARS1, BRUCE D. JOHNSON2 & BERNARD P. BOUDREAU2 1Darling Marine Center, University of Maine, 193 Clark’s Cove Road, Walpole, Maine 04573, U.S. E-mail: [email protected]; [email protected] 2Department of Oceanography, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada E-mail: [email protected]; [email protected]

Abstract Burrowing by benthic infauna mixes both sediment grains and interstitial fluids, affect- ing sedimentary redox conditions and determining fates of organic matter and pollutants. Explicit, quantitative analyses of material properties of sediments, however, have been applied only recently to understand mechanisms of burrowing. Muds are elastic solids that fracture under small tensile forces exerted by burrowers, and are dominated by adhesive forces between sediment grains and the surrounding mucopolymeric gel and (or) by cohesion of this gel. By contrast, in clean sands behaving as granular materials, gravity is a much more significant force holding grains together than is adhesion or cohesion. Burrowers in muds have diverse structures that act as wedges to propagate cracks and elongate their burrows. In sands, increased rugosity on a small, and lique- faction on a larger scale, facilitate displacement of the grains that carry compressive forces along distinct force chains or arches. The classic dual-anchor system described for burrowers is reinter- preted as having several additional functions. The characteristic dilations or expansions function primarily as wedges that exert lateral tensile forces to propagate cracks forward, secondarily as double O-ring seals holding fluid pressure in the advancing burrow (maintaining tensile stresses needed to open a crack), and thirdly as anchors (to pull the shell along in bivalves in particular). Burrowing bivalves are wedges. In the case of burrowing gammarid amphipods, the dorsal exo- skeleton mirrors the shape of half a sedimentary bubble and constitutes a wedge. A great many anatomical features of burrowers can now be understood analogously. The identification of the mechanisms of burrowing by crack propagation suggests that a substantial revision of the previously described feeding guilds of polychaetes is required.

Introduction Roughly 70% of Earth’s surface is covered by marine sediments, and the majority are muds. This extensive biome is also one of the most poorly understood because observations are difficult in muds especially in muds underlying deep water. The relationships of animals living in this biome with their environments are particularly intimate. Not only do they move through sediments, but the vast majority subsist by eating them (i.e., by deposit feeding). This kind of intimacy leads to rich intra- and interspecific interactions (e.g., Edmonds et al. 2003).

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Burrowing deposit feeders have both global and local importance. They literally gate the burial of organic matter, controlling how much organic carbon is moved out of contact with the global ocean and atmosphere. A substantial fraction of the nutrients used in coastal ocean primary production arises from nutrient cycling within the deposit-feeder-modulated sea bed, and evidence grows that this feedback from deposited organic particles is a strongly positive one that may ‘run away’, causing coastal eutrophication and ‘dead zones’ (Grall and Chauvaud 2002). Among the subtle but important effects are those on bioavailability of nitrogen, whose remineralisation path- Ð ways (N2 vs. NO3 ) are critically determined by local redox conditions controlled by respiratory irrigation (Aller 1988). One consequence of moving and feeding is bioturbation, the mixing of sediments and their pore waters. Bioturbation is the process that in most locations limits resolution of the microfossil- based stratigraphic record. Outside areas of unusually high sedimentation rate and (or) permanent bottom-water anoxia, it is difficult or impossible to resolve ≤103 yr stratigraphically (Schiffelbein 1984). Biogenic structures produced by deposit feeders also largely control the bottom roughness of marine muds and thereby influence bottom boundary layer structure, bed shear stresses and the drag experienced by near-bed currents; these structures typically result in roughly doubled drag over a smooth-bed configuration (Nowell et al. 1981). By affecting erodibility in response to given shear stresses, deposit feeders further influence net deposition and sediment stability (e.g., Rhoads et al. 1978, Roast et al. 2004). Across ocean depths, deposit feeding is the overwhelmingly dominant strategy used by mac- roscopic marine faunas to locate and consume food, and animals that feed on sediments in turn fuel many bottom-dwelling fishes and crustaceans of commercial importance. Unfortunately, the surfactants used by deposit feeders to strip hydrophobic food from ingested particles are also effective at removing hydrophobic pollutants (e.g., Voparil et al. 2003), and the high organic concentrations reached in deposit-feeder digestive processes make them also effective at solubilising heavy metals (e.g., Chen & Mayer 1999). Thus, deposit feeders are major entry points of pollutants into marine food webs and frequently are casualties of this entry. In some cases their effects on sediment transport and deposition combine through bioturbation to exacerbate pollution problems. Witness the gradual resurfacing of massive, previously buried DDT deposits on the Palos Verdes shelf off Orange County, California (Sherwood et al. 2002). Exactly what deposit feeders do — and where on and under the sediment surface they do it — becomes extremely important to the fate and effects of the residual DDT and its breakdown products. A fundamental issue of deposit-feeder ecology is the identification of the mechanism and frequency of infaunal movement through sediments. Movement through sediments is generically referred to here as burrowing, and this movement is the subject of the present review. A review is timely for two reasons. One is simply that it has been over two decades since the topic has been systematically analysed (e.g., Trueman 1975, Trueman & Jones 1977, Elder 1980). The second and more important reason is that understanding of mechanical properties of heterogeneous materials such as sediments has increased enormously over those same two decades (e.g., Duran 2000, Torquato 2001). The goal of connecting sediment nano- and microstructure with its bulk behaviour seems nearly within reach. Moreover, parameterisation and measurement of bulk sediment prop- erties at scales relevant to burrowing has just seen dramatic advances (Johnson et al. 2002), with immediate application to burrowing mechanics (Dorgan et al. 2005). One could hardly imagine analysing how a copepod or fish swims without incorporating fluid density and dynamic viscosity, yet no prior review of burrowing has explicitly identified and quantified the mechanical properties of sediments that interact with burrowing forces. It is time to move from qualitative to quantitative description of the burrowing process. Previous burrowing studies have implicitly assumed that sediment deforms plastically around burrowing animals or that movement requires liquefaction of sediment. This assumption now is

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clearly refuted for those marine muds in which material behaviour has been quantified. These muds are solids that deform elastically and fail by fracture (Johnson et al. 2002), in stark contrast to both the granular behaviour of beach sands that was previously implicitly assumed to apply across broad sediment types and to plastic deformation. This review focuses on the physical constraints imposed by the material behaviour of sand and mud, distinguishing elastic behaviour of muds from granular mechanics of sands. Neither decapod burrowing, which has been reviewed by Atkinson & Taylor (1988), nor burying, recently reviewed by Bellwood (2002) is discussed. Similarly, the extensive literature on speed of burrowing (or burrowing rate index) vs. grain size is not reviewed in any detail. Although the scaling of burrowing rate index with body size is a clever one (Stanley 1970) that likely will find continuing applicability, grain size alone — except at the extremes — has proven to be a poor predictor of bulk sediment properties relevant to burrowing forces. Also excluded to a large extent is the extensive literature that invokes dilatancy or thixotropy (defined below) as burrowing mechanisms but does not provide further explication or quantification. Many anatomical features and behaviours of burrowing animals can be explained as mechanisms to overcome specific physical constraints of sediments. For example, anterior dilations serve to propagate a crack and elongate the burrow rather than simply to anchor animals in mud (Dorgan et al. 2005). Physical differences between sands and muds can explain morphological and behav- ioural differences among their inhabitants, while functional similarities exist across phyla with vastly different forms. Finally, implications of mechanical constraints on burrowing to distribution and biomechanics of animals in the sediment, nutrient acquisition and effects on biogeochemical cycling, bioturbation and methods of studying benthic communities are discussed. This review focuses on marine sediments, but similarities with soils necessitate some discussion of terrestrial burrowing, and many of the questions arising are relevant to both systems.

Basic terminology Because the aim is to advance the field beyond classification toward equation-level analysis and description, the terminology used is perhaps less precise than some might prefer. Namely, any method that both makes an opening and results in translation of an animal through sediments fits the generic definition of burrowing used here. In particular, excavation, in which sediment is physically removed from the direction of translation, is one method. Liquefaction is a means, particularly in media displaying granular physics, of reducing the forces needed to move forward into the liquefied region (i.e., by relieving the weight of overlying sediment and friction between grains). In either case, the resultant tunnel may be shored up by either a mucus lining or a more elaborate tube incorporating selected sediments. Movement of an animal in a pre-existing tube or burrow is not included as burrowing. The term burrowing as used here specifically includes the acts of making the opening in the substratum and moving into it. Reworking is used to mean any biogenic movement of sediment, whereas the term bioturbation refers to the detectable disturbance of the complex sedimentary medium. Bioturbation thus depends on context (e.g., whether solute or particle is treated and whether disturbance is measured by chemical assay, inspection of micro- fossils or grain-size analysis). Departure from common usage of the term ‘cohesive’ as applied to sediments is intentional because it is both chemically and mechanically misleading. Cohesive forces act between like molecules, whereas adhesive forces act between unlike molecules. Cohesive forces between sedi- ment grains can be appreciable (relative to grain weight) only for grains in the clay size range. Most natural marine sediments adhere through mucopolymers whose production and consumption are largely controlled by the billion bacteria that typically inhabit each millilitre of porewater (Schmidt et al. 1998). Sediment grains thus are surrounded by polymeric organic matter (e.g.,

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Watling 1988). Organic material associates with mineral grains differently depending on the size (and weight) of the grains. Larger sand grains are encrusted with organic material, whereas smaller silt and clay grains are almost always found in larger aggregates — effectively embedded in polymer (Johnson 1974). Johnson (1974) clearly distinguished among organic-mineral aggregates, encrusted minerals, and free mineral particles in his microscopic study of particulate matter at the sediment- water interface, and he suggested that differences in sedimentological properties likely result from these distinct particle forms. Watling (1988) showed a more continuous sedimentary matrix below the sediment surface, suggesting that at least some of the ‘aggregates’ described by Johnson (1974) were likely artifacts of putting sediment on glass slides. Sediment structure is governed by polymeric material both on a larger scale through the sedimentary matrix and on a smaller scale through the fracture of aggregates rather than individual particles from the matrix. Thus, if cohesion is important to the physical properties of sediments it is the cohesion of the mucopolymer matrix and not of the sedimentary particles above clay size.

Background solid mechanics Elasticity of mud Before considering the mechanical constraints of sediments, it is necessary to briefly summarise the relevant mechanics — starting with solid mechanics — that are relevant to muds and sandy muds. Clean, granular sands exhibit unique behaviour, resisting strain like a solid, flowing like a liquid, falling fully into neither category. Only clean, coarse-grained beach sands behave like classic granular materials, whereas adhesion among grains leads to a transition between granular behaviour and elasticity. In order to clarify the relevant variables, it is suggested that a nondimensional ‘stickiness’ marks the transition in behaviour, namely the ratio between the adhesive or cohesive forces that hold two grains together relative to grain weight. This scaling makes it clear that granular behaviour is very strongly dependent on grain size but also depends on adhesion between grains at contacts or cohesion of the polymer matrix in which grains are embedded. Solids deform under stress, and when the stress reaches a critical value, the material fails, either by fracture or plastic deformation (also called yield). Stress (σ) is defined as force per unit area, and forces can be either body forces (such as gravity), which act in the same way throughout a material, or surface forces (such as those exerted by animals) that operate either on the actual surface of the solid or on a surface defining a control volume of the solid. The stress exerted perpendicular to a surface is called normal stress, and can be either compressive or tensile, depending on its direction. Convention defines compressive stresses as negative and tensile stresses as positive. Stress exerted parallel to the surface is called shear (Figure 1). Many solids behave

A B

Figure 1 (A) Normal stress is stress exerted perpendicular to a surface; (B) Shear stress is stress exerted parallel to a surface.

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σ Y Plastic Elastic region deformation ] -2 T -1

E

W Stress (σ) [M L

Strain (ε) [dimensionless]

Figure 2 The elastic (or Young’s) modulus is the slope of the linear portion of the stress-strain curve. When

the stress exceeds the yield stress (σY), the material deforms plastically, and the deformation is no longer reversible. The work done to deform an elastic material is W = ∫σ dε, or the area under the curve. Some of the energy is stored as elastic potential energy, which is regained when the stress is removed.

elastically under small stresses, so that a deformation is reversible: when the force is removed, the solid returns to its original shape. The force resisting a deformation is called the elastic restoring

force. Yield stress (σY) defines the threshold beyond which plastic deformation occurs; as long as the stress in the material does not exceed the yield stress, the material behaves elastically. The deformation resulting from stress per unit length of the material is called strain (ε), which is dimensionless. In an element of sediment, strain can be defined relative to an initial length scale or grain-to-grain distance before deformation. Within the linear elastic range, tensile stress in a material is a linear function of strain: σ = E ε, where E is the elastic modulus (dimensions of stress, M T Ð2 LÐ1), also called Young’s modulus. The elastic modulus is experimentally determined as the slope of the stress-strain curve (Figure 2). A material with a larger elastic modulus requires more stress to reach a given displacement and has greater stiffness.

Cracks and crack propagation Tensile stresses are emphasised here because in order to make the opening, the sediment must be pushed or pulled apart, creating tension at the crack tip. Elastic solids under stress fail by fracture, which begins with some flaw or heterogeneity in the material. This material failure is success for an animal making or extending a burrow opening. An easily generalised model in fracture mechanics that proves remarkably relevant to burrowing geometries describes the behaviour of an elliptical flaw. Stress increases around the flaw, with a stress amplification factor over the far-field stress of (1 + ()ar⁄ ), where a is half the length of the flaw (the longer radius of the ellipse) and r is the radius of curvature at the tip (Anderson 1995) (Figure 3). The longer and more pointed the flaw (i.e., the more crack-shaped), the greater is the stress at the tip. At the most pointed extreme, r approaches zero and the amplification approaches infinity. Real molecular dimensions preclude this mathematical singularity in real materials, although amplification can result in stress at the crack

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A

B r

a

y

x

Figure 3 (A) If an uniaxial tensile stress in the y direction is uniformly distributed in the x direction in an elastic solid (at large distance from a crack), the stress will be concentrated in front of the crack tip because stress cannot be transmitted through the flaw. Stress is amplified at the tip of an elliptical flaw or crack. (B) The stress amplification factor over the far-field stress is (1 + ()ar⁄ ), where a is the half-length of the crack and r is the radius of curvature at the crack tip.

tip greater than the yield stress of the material. This result produces a region of plastic deformation around the crack tip (Anderson 1995). Because the amplification factor includes the radius of the elliptical flaw, causing mathematical

problems in describing cracks, a stress intensity factor for cracks (KI) is defined to describe the stress field around the crack tip in linear elastic materials. The subscript I refers to mode I fracture, in which the material is pulled apart under tension rather than sheared. Mode I is the relevant

geometry for bubbles and burrowers (cf. Anderson 1995, Johnson et al. 2002). KI is similar to the amplification around an elliptical flaw, but takes into account the small region of plastic deformation

at a pointed crack tip. KI is proportional to (σ ()πa ), where σ is the stress far away from the crack tip, and depends on the geometry of the material. When KI reaches a critical value, appropriately termed the critical stress intensity factor (KIc), the crack propagates. Plastic deformation at the crack tip requires energy, which means that when a force is exerted, some of the work that would otherwise result in strain is used instead for plastic deformation, and the stress-strain relationship is no longer linear. If the area in which plastic deformation occurs is very small, however, the material behaves linearly, and linear elastic fracture mechanics (LEFM) apply. The critical stress intensity factor is a material property describing ease of fracture and is

experimentally determined for diverse materials. A material with a higher KIc requires either more stress or a longer crack for fracture to occur than one with a lower KIc. The stress intensity factor enables comparison between cracks of different sizes under different stresses. (A smaller crack under larger stress should behave similarly to a larger crack under smaller stress.) Materials with

similar KIc have similar fracture behaviour. Another way of defining how easily a linearly elastic material fractures is the crack resistance (R), which is the rate of energy release required to propagate a crack [J mÐ2]. Crack propagation is a way of releasing energy: when a ball hits a window, kinetic energy of the moving ball is transferred to elastic potential energy stored in the glass. Crack propagation occurs when the energy available exceeds the amount of energy required for the crack to grow (R). Energy release rate (G) is a measure of the amount of energy available for crack growth, with ‘rate’ referring to a change in energy with increasing crack area rather than with time. Analogous to the stress intensity factor,

a parameter is measured (G or KI), and when that parameter exceeds a critical value that has been

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AB

Figure 4 Crack propagation in (A) a homogeneous material and (B) a heterogeneous material. The crack propagates in the direction of least resistance, which means in a heterogeneous material, the path moves stochastically around much stronger grains. The crack depicted follows grain contours, implying adhesive failure of the polymer matrix attaching to the grain. Cohesive failure may instead occur within the polymer matrix, in which case the crack would move farther from the grain surfaces.

experimentally determined for a given material (i.e., when G > R or KI > KIc), fracture occurs (Anderson 1995). Cracks propagate in the direction of least resistance. In a homogeneous, isotropic material (e.g., gelatin), a crack will propagate perpendicular to the direction in which the force is exerted. An animal burrowing by crack propagation in an elastic solid such as gelatin theoretically can make the crack turn by applying force at an angle. Heterogeneous materials (e.g., mud) exhibit small-

scale variation in material properties, such as KIc and R, which can result in stochastic changes in the direction of crack propagation (Figure 4). Excess energy can be released by crack branching, which in a heterogeneous material could be a mechanism of particle release. When a crack approaches an interface, if the adhesion at the interface is much less than the cohesion of the material, as is generally the case, the crack will follow the interface (Cook & Gordon 1964). The stress field in front of a crack pointed toward a perpendicular interface has tension pulling the material away from the interface toward the crack. This tension can result in separation at the interface before the crack reaches it, so that when the crack tip hits the interface, a crack oriented along the interface has already been formed and crack resistance is low (Figure 5). The crack preferentially follows the interface, and additional energy is required for the crack to branch away. Materials that resist crack propagation have high toughness compared with easily fractured brittle materials (Gordon 1976). Toughening mechanisms include plastic deformation, interfaces, crack bridging, and crack-tip blunting. Crack bridging is common in polymeric materials (like the mucopolymer matrix in muds) and involves fibres extending across the crack that take energy to break before the crack can propagate. Styrofoam provides a classic example of crack tip blunting: a crack in a porous foam reaches a pore and the crack tip radius is significantly increased, reducing the stress amplification factor. When the plastic zone at the crack tip is large, energy is used for plastic deformation in addition to the energy to propagate the crack. Marine muds, similar to polymer gels (because they appear to comprise grains embedded in polymer gels, cf. Watling 1988), are viscoelastic, and viscous flow or creep may be an important toughening mechanism on particular spatial and temporal scales. The behaviour of viscoelastic materials is time-dependent: under high strain rates, the material behaves elastically, whereas under low strain rates, viscous flow occurs. The dimensionless ‘Deborah number (De)’ is defined as the ratio of the time a process takes to the time required for significant plastic deformation to occur (Reiner 1964). Solids have very small values of De, fluids very large. Viscoelastic materials have

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15 15

A 20 BC 20 25

30

y 30 25 Crack 25 38 Tip x 25 35 25 D 35 30 25 20 20

15 15

Figure 5 (A) The stress field (σ x) around a crack tip. The stress in the x direction (parallel to the direction of crack propagation) relative to the far-field stress [dimensionless] is shown. Maximal stress a short distance in front of the crack is tensile, so that when the crack approaches a weak interface (B), separation occurs at the interface before the crack reaches it (C). When the crack tip reaches the interface, the crack follows the interface (D). A weak interface is one for which cohesion of the material is much greater than adhesion between the two materials at the interface. In the illustration the dark black lines represent a rigid surface, such as an aquarium wall. (From Cook & Gordon 1964. With permission from the Royal Society.)

Deborah numbers much closer to unity, falling between solids and fluids. Silly putty® (Binney & Smith, Easton, Pennsylvania, U.S.) provides a classic example of a viscoelastic material. It bounces elastically in response to the short but high strain rate of hitting the floor. When left on a table, however, the long but low strain rate of gravity results in flow. Fracture of viscoelastic materials can often be approximated using linear elastic fracture mechanics, but the approximation applies only over the limited range of strain rates and timescales under which elastic behaviour dominates viscous behaviour (Anderson 1995).

Granular materials Clean, coarse sands such as those found on wave-swept beaches behave differently from more continuous solids. Mechanical behaviour of granular materials depends on particle size, surface characteristics, heterogeneity and packing structure, as well as the viscosity of the interstitial fluid and the length scale being studied (Duran 2000, Goldenberg & Goldhirsch 2005). Extensive research on granular materials has focused on materials composed of large (e.g., 1 mm), noncohesive grains in air, for which environmental influence (e.g., viscosity of the surrounding fluid) is minimal (Duran 2000). Granular materials, when agitated at high frequency, behave like molecules in a fluid. When particles are not agitated, they can still flow under shear, but only in distinct layers lacking the smooth velocity gradient of a fluid (e.g., a snow avalanche). The stochastic behaviours of granular materials result in part from randomness in contacts between particles. In a triangular packing scheme, an individual particle contacts six other particles, but it only needs two contacts below the centre of gravity to be stable. Stress in a granular material follows random chains of particles, such that some particles bear a disproportionate fraction of the load applied to the material, while others bear little or none

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Figure 6 Light-coloured stress chains in a 2-D granular medium (of birefringent disks) visualized using photoelastic stress analysis. (A) stress resulting from gravity; (B) stress resulting from a point force on the surface; (C, D) stress resulting from a point force with stress from gravity subtracted using two different methods (From Geng et al. 2001. With permission from the American Physical Society.)

(Figure 6) (e.g., Geng et al. 2001). Stress chains form arches that can block flow of granular materials through narrow discharge orifices, causing problems for distribution of grain and gravel, for example. A vertical stress is redirected laterally to varying extents depending on packing structure, which in turn depends on size and shape distributions of grains. Granular materials exhibit a nonlinear stress-strain relationship because as stress increases, particle packing changes, resulting in more contacts and increased rigidity (Duran 2000). Under shear, tightly packed particles exhibit dilatancy. When walking on a beach, footprints appear dry, a phenomenon first identified by Reynolds. When particles are tightly packed, they fill a minimal volume. In order to deform and begin to flow under shear, particles must move to a less tightly packed configuration, increasing the volume of the material. The footprint on a beach appears dry because shear exerted by the foot causes the sand grains to separate, the volume to expand and the water to drain downward into the expanded interstices. A minimal packing density exists for dilatancy to occur; less tightly packed particles move under shear without volume expansion (Jaeger & Nagel 1992). Fracture patterns have been observed in granular materials, generally following force arches. In a falling stack of grains, fracture patterns are visible below force arches holding the overlying grains. Fractures generally begin at a wall, suggesting that friction against the wall holds the force arch in place while the underlying grains fall away. Additionally, fracture occurs around a larger grain moving upward in a bed of smaller grains by vibration (Duran 2000). Behaviours of granular materials become more complex as grain sizes decrease, viscous forces begin to become important, and adhesive and cohesive forces become relatively stronger relative to grain weight. Behaviours depend on the scale of the material as well. Bulk granular material containing a large enough number of particles can be considered a continuum, a simplification that fails on a more local level. Increased friction of grains causes granular materials to behave more

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elastically, but only on a large enough spatial scale; on a smaller scale, characteristic stress chains dominate the mechanics (Goldenberg & Goldhirsch 2005).

Bulk mechanical properties of sediments at burrowing-relevant scales Grain-scale structures of sediments have been discussed to foster some intuition about why bulk sediments behave mechanically as they do and because it is likely that bulk properties of sediments will soon be predictable from them (Torquato 2001). For the remainder of the review, however, the focus is on bulk properties. The justification again is a simple scaling argument, i.e., that the burrowers are many times the length scale of the grains. The polymeric organic material in mud, when separated from the grains, shows elastic behav- iour. Frankel & Mead (1973) separated the organic material from the grains and observed meiofauna moving through the material on a depression slide. After animals moved through the material, the clumps returned elastically to their original shapes and positions. The clump of material through which the animal was moving would commonly be moved in the direction of the animal’s motion, but more slowly than the animal. They suggest that the response of the mucilaginous material indicates both ‘viscous, and elastic’ elements, but the ‘viscous’ response is likely an artifact of detaching the material from the sediment grains and putting it in a depression slide. This elastic behaviour was recently confirmed through work on methane bubble growth and movement (Johnson et al. 2002). Bubbles injected in sediment are crack-shaped rather than spher- ical, with aspect ratios predicted by linear elastic fracture mechanics (LEFM) (Johnson et al. 2002, Boudreau et al. 2005). The small forces exerted by the surface tension and buoyancy of bubbles can propagate cracks in mud (Figure 7) (Johnson et al. 2002, Boudreau et al. 2005). The internal

pressure required for crack propagation (Pc) by a bubble of volume V depends on the critical stress intensity factor (KIc) and elastic (Young’s) modulus (E) as

1 6 4 6 5 5  1  KIc π  12 Pc = 1 1 (1) EV5 5

(Johnson et al. 2002). While KIc, the material property governing fracture, is much more important than E in determining critical pressure, the aspect ratio of the bubble (bc/ac) depends much more strongly on E, as

b K π c = Ic (2) a c Eac

Although mud is elastic on the temporal and spatial scales of bubbles, it will flow when small forces are exerted over long periods (e.g., by gravity), demonstrating viscoelastic behaviour. For forces exerted over short intervals the material behaves elastically but over longer periods, viscous properties and creep may need to be considered, particularly for high-porosity muds. If a material creeps when under constant displacement, the elastic restoring force decreases over time, resulting in loss of elastic potential energy and permanent deformation. Beyond the limit of elastic behaviour,

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Figure 7 (A, B) A high-resolution CAT-scan of a bubble injected into sediment from Cole Harbor, Nova Scotia. The bright object is the injection capillary, and the sediment has been made transparent. The bubble is about 20 mm across and 0.7 mm thick, with a resulting volume of 300 mm3. The sample is from the 25Ð35 cm depth interval of this core. (C, D) plan and cross-sectional views of a bubble rising in double- strength gelatin. The bubble is 38 mm wide and 1 mm thick. (From Boudreau et al. 2005. With permission from The Geological Society of America.)

plastic deformation occurs. Although plastic deformation is not important for bubbles, it is likely to be more important on the larger scales of animals. LEFM accurately predicts the aspect ratio of

bubbles in sediment and gelatin (a clear analogue with similar E and KIc) (Johnson et al. 2002, Boudreau et al. 2005), but some animals exert a much larger displacement than observed with bubbles. If the aspect ratio is larger than predicted by LEFM, the material is behaving nonlinearly, and significant plastic deformation or creep may occur. Marine sediments exhibit both thixotropic and dilatant properties (Chapman 1949). The term thixotropy, originally used to describe the isothermal, reversible gel-sol transition of colloids, has been generalised to include changes in load-deformation behaviour with time, specifically a decrease in viscosity with increased rate of shear or with time under a constant shear (Chapman 1949, Santamarina et al. 2001). Thixotropic behaviour results from the breakdown of the polymeric matrix among particles, but the exact mechanism is unknown. Dilatancy has been described as an increase in resistance with increased shear (Chapman 1949), but more accurately refers to an increase in volume due to expansion of pore space when particles begin to move (Duran 2000). Whereas shear decreases particle contacts, a direct pressure increases the number of grain contacts and, consequently, resistance to penetration. Thus, dilatancy is a mechanism that could be used to reduce the force required for burrowing, and exertion of shear rather than normal stress should be a more efficient burrowing mechanism in sands. Granular materials such as sands exhibit dilatant behaviour, whereas thixotropy is characteristic of viscoelas- tic materials, or muds.

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vity

Gra

Granular n

Adhesion and (Transitional) Cohesio

Elastic te

Grain size Grain ent ces nd Viscoelastic Strain-ra ear for depe sh Viscous

Porosity

Figure 8 Conceptual diagram outlining dependence of mechanical behaviour on grain size and porosity of marine sediments. The ellipse encompasses the range of grain sizes and porosities found in natural sediments. Sands behave like granular materials, muds like elastic solids, and resuspended fluid mud layers viscously. A transition zone exists between sands and muds in which gravitational forces at grain contacts are comparable with adhesive forces between the polymeric matrix and grains. Sand grains within a matrix of fine grains and polymers likely fall within this transition zone. At the other end, muds that are highly porous but not resuspended behave viscoelastically.

In muds, the polymeric matrix surrounding grains dominates mechanical behaviour. Sands on wave-swept beaches fall on the other end of the continuum, behaving like dry, granular materials. The field of granular mechanics reveals why a transition from granular mechanics to solid mechanics might be expected as grain size decreases (Figure 8). The weight of an individual large sand grain is sufficient to bring it into contact with its neighbours below, and the transmitted forces are large compared with the adhesive forces of the organic polymers connecting grains. It is not yet clear where in terms of grain size or other characteristics the transition from granular mechanics to viscoelastic mechanics occurs. What is apparent, from the limited measurements made to date (Boudreau, unpublished data), is that even fairly coarse silts with considerable sand content behave more or less elastically. That is, elastic or viscoelastic behaviour dominates below the sand-silt grain size transition (<62 µm diam), and may extend into heterogeneous fine sands as well, or even beyond. This transition zone is mechanically complex but relevant to biology, as it likely includes a range of sand-silt habitats in productive coastal areas. Granular materials show more elastic behav- iour when friction becomes more important for nonadhesive particles (Goldenberg & Goldhirsch 2005), and adhesive forces would increase friction and consequently result in more elastic behaviour. In addition, elastic behaviour is important on large spatial scales, while stress chains are important on smaller scales (Goldenberg & Goldhirsch 2005). As grains are randomly distributed, mechanical behaviour in this transition zone is likely highly heterogeneous, with small volumes of elastic behaviour around arches of sand grains. Effects of the static load of overburden are common to both muds and clean sands but differ in the manner by which the pressure is transmitted. In both cases mean total pressure at depth z equals the hydrostatic pressure at the sediment-water interface (z = 0) plus z times bulk density of the sediment above z multiplied by the acceleration of gravity. In the case of impermeable muds, this load should be effectively isotropic and add to the elastic restoring force. In the case of clean, permeable sands, force arches (Figure 6) lend some anisotropy and a great deal of grain-scale

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variation in local forces. In both materials, however, this load must be overcome to open a burrow and to keep it open. Temporary alleviation is possible through time-dependent processes such as liquefaction and grain rearrangement in general. Through feedbacks with burrowing, bulk density increases with depth in sediments as porosity decreases (Mulsow et al. 1998). Consequently, as sediment depth increases, this overburden force must add nonlinearly to the forces required for burrowing.

Burrowing in mud

Description of the mechanism Early studies of burrowing in marine sediments took a largely biological perspective, focusing on detailing muscle and appendage movements, giving little consideration to sedimentary variables. Clark (1964) described a general burrowing strategy of alternating anchors; a penetration anchor holds the body in place while the anterior end of the animal moves forward into the sediment. The anterior end then dilates to form a terminal anchor while the posterior end is pulled forward. The dual-anchor burrowing mechanism has been described across phyla and has been reviewed by several authors (Clark 1964, Trueman 1975, Trueman & Jones 1977, Elder 1980, Trueman 1983, Trueman & Brown 1992). Implicitly assumed in this mechanism is that sediment either flows or deforms plastically, is compacted around the animal, excavated or ingested, and that the movement of particles is discrete and irreversible. The polychaete Nereis has been shown to burrow by crack propagation (Dorgan et al. 2005), and preliminary observations suggest that other polychaetes, as well as Yoldia, a bivalve, use a similar mechanism (Figure 9). Anchoring is only a secondary or tertiary function of anterior

Figure 9 (A) Dorsal view of crack shape and (B) lateral oblique views of crack propagation during burrowing. Arrows extending vertically from the crack indicate forces. The worm everts its pharynx and exerts a force normal to the direction of movement (1), which causes the crack to propagate, releasing energy (2). The worm then retracts the pharynx and moves forward into the crack (3) before repeating the cycle (4). W is the longer diameter or width of the discoidal crack. Its shorter diameter matches that of the pharynx. (From Dorgan et al. 2005. With permission from the Nature Publishing Group.)

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dilations; the primary function is to exert a force perpendicular to the direction of motion. The resulting stress in the sediment is amplified at the tip of the burrow, which elongates as a propagating

crack when the critical stress intensity factor (KIc) is reached (Anderson 1995, Johnson et al. 2002, Dorgan et al. 2005). The ‘terminal anchor’ is not necessarily stationary and thus is a misnomer or at least an incomplete description. Nereis, for example, drives the everted pharynx forward as a wedge to extend the crack-shaped burrow. For ‘burrowing’ by bubbles, how to calculate net tensile force is evident, and the oblate spheroidal shape is a simple one from which to calculate that force from internal pressure (cf. Johnson et al. 2002). A natural question to ask is what shape should be assumed for an animal’s wedge and how to calculate the net force on the sediments. It is difficult to lever a crack in mud, and soft-bodied animals in general may use liquid pressure generated in front of their advance to produce an oblate spheroidal geometry and tensile stresses analogous to those in a gas bubble. Subterminal expansions thus may serve O-ring functions as well. Observers are encouraged to consider the possibility that dual expansions may comprise mechanisms that act first to wedge open a crack, second to seal and maintain fluid pressure in front of the wedge and third as an anchor to pull the remainder of the body along. Setae are used by annelids to prevent backward slip during peristalsis and for parapodial locomotion within the crack. As longitudinal muscles contract to dilate a segment, protrusion of the setae occurs; then the setae are retracted as the segment elongates and moves forward (Seymour 1969). Setae exert small, very localised forces that may displace individual grains or aggregates, potentially releasing particles from the sedimentary matrix. The friction resulting from setae explains observations that polychaetes can burrow in gelatin whereas many bivalves are unable to gain purchase and move in the low-friction medium (P.A. Jumars and K.M. Dorgan, personal observation).

Ubiquity of crack propagation The dual-anchor system of burrowing has been described for burrowers across many phyla (Clark 1964), and those descriptions are briefly reproduced here. Naticid gastropods have a wedge-shaped foot, with the propodium acting as the terminal anchor and the shell and metapodium the penetration anchor (Trueman & Brown 1992). A bivalve opens its shell to form a penetration anchor, then partially closes the valves, moving fluid into the extended foot, which dilates to form the terminal anchor (Trueman 1983). Scaphopods use a similar mechanism, with the epipodial lobes around the foot increasing the radial expansion to compensate for reduced pedal dilation compared with bivalves, which close their shells to drive more fluid into the foot (Trueman 1983). Burrowing anemones dilate the physa to form a terminal anchor, then use the dilated column as the penetration anchor (Ansell & Trueman 1968, Ansell & Peck 2000). Priapulus, the nemertean Cerebratulus, and sipunculids all have long, eversible probosces that serve as terminal anchors, while the head or anterior part of the body serves as the penetration anchor (Clark 1964, Hunter et al. 1983). The long proboscis allows these animals to move forward in large steps, progressing rapidly (Hunter et al. 1983). In Priapulus, both the longitudinal and circular muscles contract synergistically, generating high internal pressures to evert the long proboscis (Clark 1964). It is suggested that in all these cases the primary function of the subterminal expansion is a wedge to drive a crack. The polychaete Nephtys and other worms with smaller pharynges were described as using the pharynx to “excavate a hole into which the animal then crawls” (Clark 1964). Nephtys is distin- guished from worms with a larger proboscis in that it likely does not use the proboscis retractor muscles to pull the animal forward as the proboscis is retracted (Clark 1964). Similarly, Polyphysia is described to use only a penetration anchor, and to progress slowly in small steps (Hunter et al.

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1983). The echiuran Urechis and holothuroid Caudina use their proboscis and oral tentacles, respectively, to ‘scrape’ and excavate a cavity into which to move (Clark 1964). Burrowing by Nereis diversicolor has been similarly described (Trevor 1977), and we now know that the pharynx is not excavating, but exerting an outward force to propagate a crack (Dorgan et al. 2005), suggesting that these animals use crack propagation to extend their burrows, and that the ‘scraping’ releases particles, enabling surface deposit feeding from the crack wall. Clams not only use the extended foot to exert a force and propagate a crack in muddy sediment, but also are shaped like a wedge and may use the shell shape to passively exert force on the sediment for fracture and also resist the elastic restoring force. The stages of burrowing by bivalves are: (1) valves open to form a ‘penetration anchor’ while the foot probes forward; (2) valves close, moving fluid away from the body and resulting in dilation of the foot (‘terminal anchor’); and (3) retractor muscles contract, pulling the shell down toward the expanded foot (Trueman 1983). The stress exerted by the open valves in the first stage is amplified at the tip of the crack, which likely elongates under, or even before, light probing by the foot. Dilation of the foot results in a smaller deformation than the open valves, but acts like a wedge driven much closer to the crack tip. The valves are then closed as they are pulled into the crack, allowing them to fit into the narrowing crack and reducing friction as they move. Many clams exhibit a forward-backward rocking motion when burrowing, which is more common for less elongated species (disk- rather than blade-shaped; Stanley 1970). This rocking behaviour is a likely alternative for elongating a crack and moving forward, and may be more effective in muds that are more resistant to penetration. Echinoids living in muddy sediments are wedge-shaped, “push directly into the frontal sediment rather than excavating it and move through the sediment by means of a repeated rocking motion”, unlike the shapes and behaviours of more globular, excavating echinoids living in sands (Kanazawa 1992). This rocking motion, combined with transport of sediment by spines, resulted in a volume of sediment reworked by burrowing 60Ð150 times greater than that ingested by the heart urchin, Brissopsis lyrifera (Hollertz & Duchene 2001). Hollertz & Duchene (2001) observed cracks on the surface above burrowing urchins, which initially burrow into the sediment by excavating with their spines until the body angles slightly downward, and then move forward in a rocking motion. This rocking could, in addition to moving the urchin forward, exert a normal force against a burrow wall to propagate a crack. Unlike clams and worms that can expand against both walls at once, the hard test of urchins may require them to exert force against the two walls alternately. Urchins burrow relatively slowly (2Ð5 mm hÐ1 (Schinner 1993)) compared with other burrowers, possibly due to a less efficient technique of burrowing or a more efficient technique to access particles in the surrounding medium for ingestion (i.e., through manipulation with spines). Many burrowers are shaped like wedges, but even Nereis, which does not appear to have a wedge shape, uses its everted pharynx as a wedge to drive into the crack. The ultimate goal of propagating a crack allows comparisons between seemingly different anatomical features (Figure 10). For example, the ornate wedge of some trichobranchid polychaetes, large ovoid proboscis of Artacama valparaisiensis (Polychaeta: Terebellidae), and muscular anterior region of cirratulids and cossurids are all feasible crack-propagating mechanisms for worms (cf. Hartman 1955, Hartman 1958, Rozbaczylo & Mendez 1996). Magelonidae have a broad, flattened, wedge-shaped prostomium and an eversible proboscis (Jones 1968), suggesting that they, too, utilise crack propagation. Amphipod burrowing appears largely analogous with movement of bubbles. Indeed, the basic shape of a burrowing amphipod is an oblate hemispheroid, a half-bubble with legs for propulsion. The dorsal exoskeleton is the wedge, driven by the legs. If the deformation of the sediment caused by the amphipod’s body is within the elastic limit of the sediment (i.e., the sediment is linear elastic), the aspect ratio of a burrowing amphipod (Figure 11) (body width relative to its diameter) may be predictable from the Young’s modulus and the critical stress intensity factor (cf. Johnson

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Figure 10 Polychaetes with morphologies suitable for propagating cracks. (A) Many cirratulids have muscular expansions at both anterior and posterior ends that could be used to exert a force to propagate a crack (drawing from Hartman 1958, p. 201); (B) the terebellid, Artacama valparaisiensis, has a large, ovoid proboscis (drawing from Rozbaczylo & Mendez 1996, their Figure 1A); With permission from the Biological Society of Wash- ington. (C) the trichobranchid Artacamella hancocki has an ornate, wedge-shaped anterior (drawings from Hartman 1955, p. 59); (D) Magelona sp. (Magelonidae) has a broad, flattened prostomium that could be pushed forward into a crack, with an eversible proboscis to exert a lateral, wedging force (drawings from Jones 1968). With permission from Biological Bulletin (Woods Hole).

Figure 11 Lateral view of the gammaridean amphipod, Harpinia propinqua, shown with the outline of an oblate hemispheroid (From Bousfield 1973. With permission).

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et al. 2002). It is strongly suspected that this interaction with the sedimentary medium is the underlying reason for the body plan of some gammarids and may be one reason for their cuticular hydrophobicity.

Dependence on properties of mud As discussed above, the aspect ratio of bubbles in sediment has been accurately predicted using

linear elastic fracture mechanics (LEFM) and is directly proportional to KIc and inversely propor- tional to E (Johnson et al. 2002). Whereas a bubble has a constant volume, and the material properties of the sediment determine the shape, burrowers tend toward constant displacement. That displacement results in a stress determined by Young’s modulus, E, which likely varies with depth

in sediment, porosity, grain size, and organic content. KI is directly proportional to the stress, and the ease of fracture and resultant length of the crack therefore depends on both E and KIc. If E increases and KIc remains the same, a burrower will exert more stress for a given displacement, and the crack will propagate farther, resulting in a more flattened discoidal burrow shape. If KIc increases, more stress is needed to propagate the crack, and the crack will extend a shorter distance and have a larger aspect ratio.

Burrowing with a hydrostatic skeleton Many burrowers move using a hydrostatic skeleton, the physics of which has been summarised for earthworms (Quillin 1998). A hydrostatic skeleton comprises an extensible body wall containing fluid or tissue under compression against which muscles can work. The interior fluid is incompress- ible, allowing operation of antagonistic muscles, the transfer of muscle forces to the environment and maintenance of body shape (Quillin 1998). Cylindrical hydrostats of length L and radius r have a constant volume of

V=π r2 L (3)

Rearranging and differentiating this equation gives

dr −r = (4) dL 2L

For a 1% shortening of the circular muscles, which elongate the segment when contracted, there is a 2% elongation of the longitudinal muscles, which dilate the segment when contracted (Alexander 2003). For worms, the whole body comprises one or more hydrostatic skeletons used for locomotion, whereas molluscs use their hydrostatic feet in coordination with the hard shell, and amphipods and echinoids have only hard exoskeletons. Some annelids have septa that partition the fluid in segments, dividing the worm into a series of separate hydrostats. In aseptate annelids and other worm-shaped animals, the body comprises one large hydrostat. Stresses in the body wall of a thin-walled cylinder under internal pressure are

Pr Pr σ = andσ = (5) c t l 2t

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Figure 12 (A) Sections through the hydrostatic skeleton of a worm, showing circular muscles (which exert

stress, σc) and internal pressure (P) (From Quillin 1998. With permission.); (B) the same hydrostatic skeleton but dorso-ventrally compressed by the walls of the disk-shaped burrow through the elastic restoring force.

where σc is circumferential tensile stress, σl is longitudinal tensile stress, P is internal pressure, r is radius and t is body-wall thickness. These stresses are calculated by balancing the force from the internal pressure with the force exerted by the muscle, assuming that the cylinder has no other forces acting upon it (Figure 12A) (Quillin 1998). Worms that burrow in muddy sediments by crack propagation experience a force exerted by the burrow walls compressing the body dorsoventrally (Dorgan et al. 2005). Superposition of a dorsoventral force and a constant internal pressure results in an asymmetrical internal stress field, with higher stress being exerted laterally and lower stress dorsally and ventrally (Figure 12B). This internal stress asymmetry results in reduced circumferential stress on the sides of the worm extending dorsoventrally and increased circumferential stress on the dorsal and ventral sides extend- ing laterally. Similarly, the dorsoventral compression results in an elliptical rather than circular cross-section of the worm’s body. The radius of curvature of the shorter axis (the sides of the worm) is smaller than that of the longer axis, resulting in reduced lateral circumferential and longitudinal stresses from Equation 5. Scalibregma inflatum (Scalibregmatidae) is named for its balloon-like shape when removed from sediments, and sternaspids (Sternaspidae) are nearly spherical when removed from the mud. When observed burrowing in gelatin, however, they are both dorsoventrally compressed, adopting the fundamental disk shape of the crack itself (K.M. Dorgan & P.A. Jumars, unpublished observations). The polychaete Cossura sp. has longitudinal muscles, but its circular muscles are “very poorly developed” (Tzetlin 1994). Cossuridae burrow in muddy sediment (Rouse & Pleijel 2001) and may

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use the elastic restoring force of sediment to aid their circular muscles in elongating segments during peristalsis. Circular muscles are also completely absent in the burrowers Opheliidae, Sigalionidae, Nephtyidae and representatives from numerous other polychaete families, including meio- and macrofauna (Tzetlin & Filippova 2005, Tzetlin et al. 2002). Tzetlin et al. (2002) point out that circular muscles are commonly less developed in parapodia-bearing taxa, and even absence of circular muscles is not uncommon in polychaetes. In fact, Tzetlin & Filippova (2005) hypothesise that the absence of circular muscles may be the plesiomorphic state in Annelida. Tzetlin et al. (2002) suggest that circular muscles may not be necessary for polychaetes that move using parapo- dia, as the dorso-ventral, transverse, parapodial, or other longitudinal muscles can act as antagonists for longitudinal muscles, but that circular muscles are necessary for burrowers. It is suggested here that circular muscles may not be necessary for burrowing if the elastic restoring force acts as an antagonist for the longitudinal muscles, but crawling by peristalsis does require circular muscles. It would be interesting to compare burrowing and nonburrowing species that are closely related.

‘Soupy’ muds ‘Soupy’ appears to be a misnomer for deposited muds. Except for those that have very recently been resuspended, highly porous muds behave viscoelastically instead; a high strain rate results in more elastic behaviour of the sediment, whereas a low strain rate results in viscous flow. This behaviour is apparent in gelatin; gelatin ‘jiggles’ when shaken, but leave a half-eaten bowl of gelatin to respond to gravity and it flows passively. The same behaviour can be seen in some muds left in a bucket. If the strain rate at which a transition from elastic to viscous behaviour is similar to that exerted by animals, that threshold may affect animal behaviour. In this case, animals may either move quickly, heightening strain rates and invoking elastic behaviour to fracture the mud or move slowly, lowering strain rates and swimming in slow motion through a highly viscous fluid. It should be noted, however, that swimming at consequently low Reynolds numbers cannot be accomplished by reciprocating mechanisms (Purcell 1977). Viscoelastic materials experience creep, which may be important in highly porous muds. Burrowing behaviour in soft muds by Polyphysia has been described (Elder 1973), but the mechanical behaviour of the sediments is unknown. Polyphysia burrows by direct peristalsis, with both circular and longitudinal muscles contracting simultaneously, resulting in an anterior wave of short, thin segments. In septate worms, circular and longitudinal muscles work antagonistically; in Polyphysia, elastic fibres restore body shape after contraction of both sets of muscles (Elder 1973). This direct peristaltic wave displaces most of the coelomic fluid anteriorly (Elder 1973). It may be a way to build up pressures over a large enough area and to high enough levels to fracture. The anterior five segments of Polyphysia are segmented, and the head progresses continually while the rest of the body progresses in episodic waves (Elder 1973). Polyphysia moves its head from side to side while burrowing (Elder 1973, Hunter et al. 1983), a behaviour that has been observed in Scalibregma (in the same family, Scalibregmatidae, as Polyphysia) and Nereis, both burrowing in gelatin (K.M. Dorgan, personal observations). Hunter et al. (1983) suggest that Polyphysia is taking advantage of the thixotropic behaviour of mud and reducing the viscosity before moving forward. Nereis, however, which has been shown to burrow by crack propagation (Dorgan et al. 2005), exhibits the same behaviour, and preliminary observations of Scalibregma burrowing in gelatin reveal a crack-shaped burrow. Head movements of Scalibregma extend the crack tip laterally and slightly anteriorly, while the wider body holds the crack open (K.M. Dorgan, unpublished obser- vations). In this way, the head is analogous to the probing foot of a clam, while the wider body holds the crack open, as does the clam’s shell. In sediment, the head movement may additionally be used to free particles for feeding, in sensory behaviour, or as a way to mechanically ‘sample’ the resistance of sediment in different directions by driving the head into the crack.

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Priapulus caudatus also burrows in soft sediments but uses a very different mechanism. Priapulus uses simultaneous contraction of circular and longitudinal muscles to build up high internal pressures to evert a large praesoma, which has been described as a terminal anchor (Hunter et al. 1983). The praesoma is dilated to a volume greater than the volume of fluid remaining in the trunk; then a direct peristaltic wave moves the body forward as the praesoma is retracted (Hunter et al. 1983). Burrowers in high-porosity sediments use mechanisms interpreted as ways to propagate a crack in a viscoelastic solid. Although the behaviour of burrowers suggests that elastic behaviour dominates over viscous flow even in highly porous sediments, an explicit understanding of the mechanical behaviour of these sediments is still lacking. The two sediment behaviours may act largely in series (initially elastic, with creep becoming more important on longer timescales) and this series may explain the basic body plan of the burrowing polychaetes that dominate the muddy sea floor. The general body form is bilaterally symmetrical anteriorly but cylindrically symmetrical posteriorly, like that of Scalibregma or Poly- physia. It is suggested that the anterior is adapted to crack propagation and movement in the crack, whereas the hindmost cylindrical morphology is the form that will result from sediment creep reaching equilibrium with coelomic pressure. Following this reasoning, fast polychaete burrowers will lack a cylindrical region, whereas slow burrowers will lack a bilaterally symmetric region. However, to compare burrowing speeds properly, they should be normalised to the rate of sediment creep; burrowers in highly porous sediments that creep more easily may need to burrow more quickly to experience similar mechanics to a slower moving animal in stiffer sediment.

Peristalsis as a way to crack Many worms and worm-shaped burrowers move by peristalsis, which involves waves of muscular contraction travelling either anteriorly or posteriorly along the body. In direct peristalsis, the wave of contractions moves in the same direction as the animal, while in retrograde peristalsis, the wave moves in the opposite direction (Elder 1980). In general, retrograde peristalsis is utilised by animals with septa separating coelomic fluid into segments of constant volume. Direct peristalsis occurs only in animals with an open body cavity, and segments do not maintain a constant volume as the wave passes. In general, animals utilising retrograde peristalsis (e.g., earthworms) burrow in more compacted, less porous sediments. This compartmentalisation enables the animals to build up high internal pressures and exert strong forces within a small region of the body while pressures remain low elsewhere. The animal has to do less work to exert the same force at that given body location than does an animal with an open body cavity. In addition to exerting force to propagate a crack, worms dilate segments against the elastic restoring force of the sediment. It takes work to maintain body shape in the crack, and the fatter the segments and longer the dilation is held, the more work is needed. In more compact muds with a higher elastic modulus and higher restoring force, it may be more efficient to increase the volume of the body that is contained in thin segments to reduce work done against the elastic restoring force of the sediment (in other words, to let more of the body be flattened). Septa, which are present in worms that move by retrograde peristalsis, help maintain the stiffness of the body wall so less internal pressure is required to maintain body shape. The earthworm Lumbricus has septa and a particularly stiff body wall and does not need to maintain internal pressure to keep the body’s cylindrical shape against gravitational forces in air (Trueman 1975). Direct peristalsis occurs primarily in animals burrowing in high-porosity sediments, such as Polyphysia sp., Priapulus caudatus (Hunter et al. 1983, Hunter & Elder 1989), and the holothuroid Leptosynapta tenuis (Elder 1980). The thin segments in which circular muscles contract are also short, increasing the area touching the sediment and resulting in fluid displacement among segments.

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In contrast, retrograde peristalsis involves segments of a constant volume, so thin segments become longer. Elder (1980) suggests that direct peristalsis may be advantageous to these animals as it reduces the area of the thin segments and increases the anchor area, which may be beneficial in ‘soupy’ sediments that deform easily. This suggestion can be reinterpreted to explain the benefits of increasing the area exerting the stress. These high-porosity sediments deform under low stresses, prohibiting the animal from building up the higher internal pressures possible in more compacted sediments. A larger area of body wall in contact with the sediment allows the animal to exert more stress, possibly compensating for low internal pressures. The direct peristaltic wave moves coelomic fluid anteriorly in Polyphysia (Elder 1973), resulting in expansion of the anterior region and increased internal pressure. Arenicola marina also uses direct peristalsis (Elder 1980), but in this case water flow is external, and the peristaltic wave pumps water through the burrow, likely aiding in liquefaction. Even in the sand that it inhabits, however, the pressure so produced may be used to propagate a crack upward as a head shaft (S.A. Woodin, personal communication 2005). In both types of peristalsis, the thinner segments are moving while the thicker segments are stationary, the latter withstanding the elastic restoring force of the burrow wall. By analogy with

the common formulation of sliding friction, the frictional force (Ff) is directly proportional to the normal force (FN), Ff = µFN, where µ is the friction coefficient. In this case, the elastic restoring force dominates the normal force (although sediment overburden may be important as well), and most of the elastic restoring force is exerted by the sediment against the stationary, dilated segments. This conclusion suggests that frictional forces may be much less significant than inferred in previous studies in which friction has been considered important as a mechanism for particle mixing and a component of energetic calculations for burrowers (e.g., Trevor 1978).

Burrowing in sand Differentiation from mud Sand is a granular medium, in which forces distribute along stress chains; interfaces between some particles experience large stresses, while others bear little or no load (Duran 2000). To an animal burrowing in sand, some grains are easily moved, while others are part of a stress chain and are therefore much more difficult to displace. Depending on the speed of locomotion and the size of the animal, a macroscale or microscale approach to burrowing could be taken. Bulk movement of sand can be achieved by liquefaction or excavation, whereas individual grains can be moved by breaking stress chains. This section attempts to correlate observations in the literature with known behaviours of granular materials to generate hypotheses for future research. Muddy sediments are adhesive and resist deformation, so forces exerted on an animal act from any direction in which the animal exerts a force. Sand differs in that grains rest on each other, with the result that the weight of the overlying sediment exerts an important but nonuniform force on an animal, whether stationary or mobile. Sea urchins that live in sands reflect this difference with their dome shape, which is able to sustain the downward weight of the sand (Kanazawa 1992). For animals that construct more permanent burrows, mucus may serve the dual purpose of reducing friction and providing adhesion for sand grains to stick together and maintain the structure of the burrow wall. Penetrometer studies have shown that the force required to penetrate the surface of sand decreases dramatically with decreasing angle to the sand surface below 30¡. The gastropod Bullia has a disk-shaped foot, is a fast burrower, and moves by extension of the propodium, forming a terminal anchor, then drawing forward the shell and metapodium, forming a penetration anchor. B. digitalis burrows at an angle of 10Ð15¡, whereas Donax serra burrows vertically. D. serra has

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the higher energetic cost of burrowing, with a ratio of 9:1 predicted by penetrometer data (Brown & Trueman 1991). These results are unsurprising, because the upward displacement of discrete particles should be much easier than horizontal, for which tight packing resists movement. The impermeability and cohesiveness of polymers in mud suggest that the angle of penetration should have a less significant effect on ease of penetration, although there appear to be no similar studies done in muds.

Description of the mechanism Clean sands on wave-swept beaches have large, homogeneous grain sizes and are more closely mimicked by laboratory and theoretical studies on dry granular materials than are finer sands with higher organic contents. The mole crab, Emerita, burrows in sandy beaches by rapid excavation and resuspension of sand grains. Like other sandy beach burrowers (e.g., cirolanid isopods; Yan- nicelli et al. 2002), Emerita can burrow only in wet sand (Trueman 1970). It has been suggested that dry sand is too hard (Trueman 1970) or less thixotropic (Yannicelli et al. 2002), but more likely the animals are using the increased density of sea water over air to facilitate suspension of sand grains. The first three pairs of thoracic limbs move the body backward into the burrow and sand forward, while the fourth pair of limbs and the uropods excavate the burrow (Trueman 1970). Burrowing occurs much more rapidly than in the fastest bivalves studied (Trueman 1970, Lastra et al. 2002). Amphipods burrow in sands by a completely different mechanism. Setae that bend in only one direction help produce forward (and probably slightly upward) motion in sands (Nicolaisen & Kanneworf 1969). Perhaps they are driving a wedge. Mole crabs are considered generalist burrowers, in that the burrowing rate is not greatly affected by sediment grain size (Trueman 1970, Lastra et al. 2002). Burrowing rate index, defined as BRI = (mass(g))1/3/burrowing time × 100, has been used to compare burrowing speeds among animals of varying sizes (Stanley 1970). (N.B. Alexander et al. (1993) use 104 instead of 100 in their calcu- lations to give BRI values of 1.0 or greater). The burrowing rate index is generally constant throughout the size range of a species (Stanley 1970). Species for which BRI depends strongly on grain size are considered specialists, many of which burrow most quickly in fine to medium sands. Donax serra and D. sordidus show fastest burrowing times in 125–500 µm sands (Nel et al. 2001), cirolanid isopods in ‘fine’ rather than ‘coarse’ sediments (Yannicelli et al. 2002), the mysid, Gastrosaccus psammodytes, in 125–1000 µm sand (Nel et al. 1999), and many of the bivalves studied by Alexander et al. (1993) showed BRI maxima in fine to medium sands. Burrowing times increase in finer sands (Nel et al. 1999, 2001). Displacement of a single particle in a granular material requires work to overcome friction and, depending on the packing structure, work to lift overlying particles. In a loosely packed structure, a displaced particle may be moved into pre-existing void space with minimal displacement of other particles. The smaller the particle size (assuming uniform particle size distribution), the less overlying load it carries, given that it is part of a stress chain, because there are more stress chains in a given area. Stress chains are more easily broken in finer-grained granular materials: the stress chain bears less weight, and the weight is more easily redistributed along newly formed stress chains. Contacts per volume increase with decreasing grain size. Furthermore, the frictional force between two particles depends on the overlying weight and while (assuming constant void ratio) the total load is the same at a given sediment depth for smaller grains, the load is distributed over a greater area. For these reasons, smaller grains should be more easily displaced than larger grains. The fact that burrowing rates decrease in sands with grain sizes <125 µm suggests that different mechanics are at work. Changes in permeability or adhesion would affect burrowing performance. Contacts per volume also increase with decreasing sorting, although this likely leads to increased

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resistance to stress more than facilitating redistribution of stress chains, as dense packing could inhibit redistribution of grains. The features of sand burrowers that increase their rugosity may be adaptations to displace grains bearing larger loads. Examples of these features include papillae on the pharynges of worms, setae, bivalve shells with surface relief comparable in scale to grain size, and sea urchin spines.

Use of fluidisation Fluidisation entails the injection of fluid in such a manner as to eliminate a substantial proportion of grain contacts and cause the bulk material to flow as a fluid. Many clams eject water from the mantle cavity during rapid adduction of the valves; adduction also results in foot dilation (Trueman 1975, Trueman & Brown 1992). Among gastropods, Trueman & Brown (1992) compare Bullia, which burrows in sandy beaches, with natacids, which burrow deeper in muddy sediments. Bullia ejects water, helping to liquefy the sand, while natacids do not eject water, a process that would be less beneficial in low-permeability muds except to maintain pressure in the small volume of crack preceding the animal. Arenicolid polychaetes pump water down from the tail end of their J-shaped burrows toward the head. The water moves upward toward the sediment-water interface from the anterior end of the burrow within a localised area in the sediment (Timmerman et al. 2002). Although movement of fluid has been studied by several authors (Riisgård et al. 1996, Timmerman et al. 2002), explicit modeling of particle movement is lacking. Arenicola marina is assumed to use the pumped water to loosen or fluidise the sand in front of the head, feeding in this region (Trevor 1977). In order to move through sand by using pumped water to fluidise the sand, either the entire overlying bed of sand through which water passes must be fluidised, or a localised region around the head, in which case the weight of the overlying sediment must be distributed around the animal by stress chains. The upper layer of sand may be supported by stress chains arching around the small, fluid region into which the animal can move. Fluidisation may be practical only within the upper region of sand with low resistance to flow. Flow through a packed bed increases with increasing permeability and depth of sand, following Darcy’s law

k u = −∇−()pgρ (6) µ

where u is velocity, k is permeability, µ is the viscosity of the water,∇p is the pressure gradient, ρ is water density and g is gravity (Wilkes 1999). The 1-D discretised form is

kp − p  u = − 12− ρg (7) µ  L 

where L is the length of the bed, and p1 and p2 are the pressures at the bottom and top of the bed, respectively. Most of the variation results from permeability, which increases with increasing grain size, length of bed (depth in sediment), and the increase in pressure (which depends on the force with which water is forced by the animal) with depth. Fluidisation of a bed of particles occurs when the pressure drop between the bottom and top of the bed exceeds the stress caused by the weight of the particles, i.e., when

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ppgL12− = ()1− ερ 0s (8)

where ε0 is the void ratio (not to be confused with strain), and ρs is the density of the particles (Wilkes 1999). An animal burrowing at a greater depth must produce a greater increase in pressure to fluidise the bed, a depth dependence unsurprisingly similar to Darcy’s law because fluidisation occurs at a critical flow velocity. Riisgård et al. (1996) found that A. marina attains a maximum pressure head of 20 cm water, a value comparable with that needed to fluidise the bed above itself, assuming that the animal is burrowing at a depth (L) of 10Ð15 cm with a void ratio of 0.5. However, their study involved animals in glass tubes, whereas in the natural environment, pumped water may find lateral escape routes into the surrounding sand, reducing the available pressure head to fluidise the overlying sand. In addition, stress is distributed laterally over relatively large distances in granular materials, whereas the region in which fluid moves upward from the worm’s burrow is relatively small. The literature on fluidisation of beds of particles is extensive but generally considers fluidisation of the entire bed enclosed by an impermeable container with flow at a constant rate (Wilkes 1999). Burrowing animals pump water at an unsteady rate into an uncontained area, of which only a small portion is affected by the pumping. Although fluidisation of the bed is unlikely at the depth in the sediment at which Arenicola lives, the pumped water may reduce the load of the overlying sediment and reduce friction between grains, easing burrowing. Another hypothesis for the mechanism of burrowing by Arenicola is that the pumped water could be used to fracture the sand. Granular materials have been found to fracture below force arches (Duran 2000), and hydraulic fracture is an important mechanism in geological processes, including rocks and glaciers (Fountain et al. 2005). Fine sands may have enough adhesion to behave elastically, or at least to fall within the transition zone between elastic and granular behavior. Again, preliminary observations by S.A. Woodin (personal communication 2005) support this hypothesis. It is possible that the papillae of Arenicola are used to break stress chains and move grains that are not easily resuspended. However, the maldanid polychaete, Proxillella affinis pacifica, which lives in muddy sediments, has a papillated pharynx, while other sand-dwelling species of maldanids lack papillae (Kudenov 1977). In this case, the papillae may remove particles from the organic matrix and/or provide greater surface area to stick to particles and move them into the mouth.

Discussion and implications Terrestrial implications Subterminal expansions suggest that earthworms may burrow, and roots grow, by analogous mech- anisms. Roots grow axially until too much resistance is met, causing them to grow radially, creating a zone of stress relief into which axial growth extends (Figure 13) (Abdalla et al. 1969). The alternation between axial and radial growth by plant roots has been described as ‘inverse-peristaltic’ growth. This means roots can penetrate compact soils with five times the resistance that the root would be able to overcome by axial growth alone (Hettiaratchi & Ferguson 1973). Earthworms also exert radial forces, which are higher than measured axial forces (Keudel & Schrader 1999, Quillin 2000). Highest internal pressures of burrowing earthworms occur when buried segments are dilated, described as a mechanism to anchor the worm and compact the surrounding sediment (Seymour 1969). Earthworms exert stronger forces near the anterior end; a retrograde peristaltic wave is strongest when beginning at the head end and it may die out before reaching the tail (Seymour 1969). Earthworms lose coelomic fluid through dorsal pores, which are

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1234

Root cap Zone of Recycle from 2 stress relief

Figure 13 Scheme of root penetration in soil. When the root cap meets resistance (1), the root grows radially, creating a zone of stress relief (2). The root can then extend axially (3), until it again meets too much resistance (4). (From Abdalla et al. 1969. With permission from Elsevier.)

only present on posterior segments of burrowing species (Stovold et al. 2003). Anterior sections maintain internal pressures, enabling worms to exert the same radial forces even when dehydrated (Stovold et al. 2003). Although crack propagation seems a likely mechanism of burrowing in terrestrial soils, direct evidence is needed. Extensive literature on soil properties from the perspectives of civil engineers exists (e.g., Chandler 1984) but this literature has not been explicitly applied to the space and time scales of burrowing. Soils have been modelled using elastic-plastic fracture mechanics (Chandler 1984). It would be worthwhile to re-examine burrowing using a nonlinear fracture model. Previous studies of earthworm burrowing have measured forces of animals burrowing against rigid walls and, although they have yielded important ecological and ontogenetic comparisons among earth- worms (Keudel & Schrader 1999, Quillin 2000), the values measured do not represent natural conditions. Internal pressures and measured forces depend on the material against which the animal is exerting the force.

Biomechanics of burrowing While the use of a hydrostatic skeleton suggests similarities between the mechanisms of burrowing and crawling, environmental forces differ significantly. Animals burrowing in muds have two surfaces against which to push and are compressed by the elastic restoring force, resulting in different body wall stresses. Seymour (1969) measured internal pressures of earthworms burrowing and crawling and found different pressure records for the two behaviours. Crawling earthworms had maximal coelomic pressures of approximately 10 cm of water in segment 10 during circular muscle contraction (lengthening of segments), with a drop to approximately 5 cm water during segment dilation. For burrowers, coelomic pressure was higher (18Ð24 cm water) than for crawlers, and showed the reverse pattern, a reduction in coelomic pressure as segments were elongated (Seymour 1969). The two walls constrain radial expansion of the burrowing worm, requiring much higher pressures than unconstrained surface crawling. When burrowing, one direct peristaltic wave occurs at a time in Polyphysia crassa, whereas simultaneous passage of two waves occurs during crawling (Hunter et al. 1983). This difference allows higher internal pressures to build up during burrowing, even in soft muds with low resistance. Burrowing and crawling, although superficially, kinematically similar, are mechanically and dynamically different types of locomotion. Compari- sons, both within and among species, should be made with caution. A possible advantage to locomotion within an elastic solid is external storage of elastic strain energy. Elastic energy can be stored in tendons; the most common example is in kangaroos and

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wallabies (Alexander 2003). When a hopping kangaroo lands, kinetic energy is stored in a spring- like tendon and then converted back to kinetic energy as the kangaroo ascends. Whereas energy storage is common in internal elastic structures, burrowers are unique in their access to an external elastic energy storage structure. The importance, or even occurrence, of elastic energy storage by burrowers in muds is yet unknown. Terrestrial and aquatic environments differ in that terrestrial hydrostats must retain their body shapes against gravity, whereas most aquatic animals have densities close enough to the density of sea water that gravitational force is not a major concern for an animal at the sediment-water interface. Gravitational forces can, however, become significant with increasing sediment overbur- den. The cuticle and septa of Lumbricus terrestris help maintain body shape, allowing much lower resting internal pressures than in Arenicola marina, for which most of the body is aseptate (Seymour 1969). Negative pressures have been recorded in Lumbricus terrestris and have been attributed to elastic outward rebound of the body wall as circular muscles are relaxed (Seymour 1969). Burrowing has in the past been calculated to be more energetically expensive than other forms of locomotion such as flying, swimming and running (Trevor 1978, Hunter & Elder 1989). However, forces exerted by Nereis virens in gelatin are <10% of those measured with solid force transducers in Priapulus and Polyphysia (Dorgan et al. 2005, Hunter & Elder 1989). It is quite likely that burrowing is less costly than previously suggested but traditional methods of measuring energetic cost of transport are not feasible in marine sediments. Oxygen consumption rates are the standard means to calculate net cost of transport but in marine sediments no way is known to estimate individual oxygen consumption rates because of the complex three-dimensional, time-varying structure of oxygen concentration fields within and around a burrow whose geometry itself is time varying. Moreover, the uptake occurs together with that of abundantly and nonrandomly distributed smaller organisms, including bacteria at 109 cells mlÐ1 of porewater in natural sediments (Schmidt et al. 1998). Even the steady-state distribution of oxygen concentration under continuous pumping into a permanent burrow of fixed geometry is not trivial to model (Aller 1982).

Nonrandom distribution of animals Most burrowers appear to exert constant displacements on the walls of their burrows determined by the sizes of their everted pharynges, dilated feet, or other ‘terminal anchors’. The stress then exerted against the sediment depends on the elasticity of the sediment: σ = Eε. Because the elastic modulus (E) is a measure of the amount of stress required for a given strain, the elastic modulus is expected to increase with greater sediment compaction, reduced porosity and increased weight of sedimentary overburden (i.e., with depth in the sediment). A constant displacement exerted by

an animal would result in increasing stress as E increases. Stress intensity factor (KI) is proportional to stress, while the critical value at which fracture occurs (KIc) is a material property. KIc appears to increase with depth (B.D. Johnson and B.P. Boudreau, unpublished data), but similar profiles for E are lacking. Our analysis of the effects of overburden would argue for increasing E with

depth, however, but not necessarily in proportion to K1c. Changes in the relationship between E and KIc with depth would change the ease and shape of fracture and could result in layers of high burrowing activity. For example, if E increases more quickly than KIc, the higher stress will propagate the crack more easily. Because cracks propagate in the direction of least resistance, an already cracked path may become a highway for other burrowers. Similarly, methane bubbles can grow more easily in pre- existing, partially annealed cracks, as indicated by the pressure records of bubble-growth in Johnson et al. (2002). How quickly cracks anneal in sediments is unknown, but a comparison between the time of annealing and the time that elapses before another burrower encounters a crack (also

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unknown) could be used to predict the likelihood of highways forming in muds. Alternatively, cracks may be turned away from the compacted area around burrows, keeping burrowers away from recently formed burrows. Discoidal cracks can become cylindrical burrows with compacted sediment walls (e.g., Figure 4 in Shull & Yasuda 2001). These two alternatives depend in part on whether most traces left by animals are crack-shaped and close after the animal passes or are cylindrical burrows, discussed in further detail below.

Bioturbation The distribution of animals clearly has a direct effect on bioturbation. A nonrandom distribution of animals suggests a nonrandom probability of movement of particles by those animals. Perhaps more importantly, in bioturbation models, particles are considered discrete, an invalid assumption in elastic muds. Unless the polymer matrix holding grains together is broken, the movement of individual grains depends strongly on the movement of adjacent grains. The matrix is broken when a crack propagates, at which time grains may be released by crack branching or irregular crack growth resulting from sediment heterogeneity. However, release of grains from the matrix during ingestion by deposit feeders and their defaecation at another location is likely the most important mechanism of particle mixing. Results of lattice automaton models of bioturbation highlight the importance of ingestion and egestion in particle mixing (Boudreau et al. 2001). The question of how a crack becomes a permanent cylindrical burrow is important both in terms of bioturbation and interpreting the fossil record. Cylindrical burrows are clearly visible on the sediment surface and in x-radiographs and, once vacated, cave in or fill with sediment, resulting in particle movement. The presence of burrows necessitates some mechanism for transforming a crack to a cylinder, either passively resulting from sediment mechanics or by active behaviour of animals such as lining the burrow with mucus. Burrow presence does not, however, give an indication of how often this process occurs. Absence of evidence may not be evidence of absence: cylindrical burrows left in the sediment are obvious (e.g., cirratulid burrows; Shull & Yasuda 2001), but how could a crack, having closed up, be detected? It has been observed that larger macrofauna contribute disproportionately more to sediment mixing than smaller animals; for example, the volume of sediment reworked by burrowing by the heart urchin, Brissopsis lyrifera, is 60Ð150 times greater than that ingested (Hollertz & Duchene 2001), whereas ingestion contributes much more significantly to modelled mixing by small, capitellid-like deposit feeders (Boudreau et al. 2001). Whether a crack closes after an animal passes depends on a number of factors. Viscoelastic creep results in reduced elastic restoring force over time, potentially compacting burrow walls, but the temporal and spatial scales over which creep is important are unknown. The elastic limit of the sediment is clearly important, and although no data on elastic limits of muds exist, intuition suggests that more porous, fine-grained muds have lower elastic limits and flow more easily than more compacted sediments. Coarser sediments may deform plastically, more similar to terrestrial soils. Gelatin has been used to examine the mechanical effects of spicules in connective tissue of sponges and cnidarians (Koehl 1982), with obvious implications for sediment grains in a mucopolymeric matrix. Increased spicule volume fractions and surface area-to-volume ratios result in increased stiffness, a result consistent with intuition about sediment; i.e., more highly porous muds have lower stiffness. Interestingly, the spicules have a stress-softening effect on gelatin (and natural tissues) because repeated stresses are met with decreased resistance (Koehl 1982). Consider a burrower moving through a crack with repeated peristaltic contractions. The viscoelastic nature of mud suggests time dependence; the slower an animal moves, the more time is allowed for the sediment to creep. Perhaps most importantly, the size of the animal determines the deformation because a larger animal is much more likely to exceed the elastic limit and leave a permanent burrow.

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Crack propagation as a mechanism of burrowing brings into question several assumptions in bioturbation models. Meysman et al. (2003) distinguish between local and nonlocal models of bioturbation, suggesting that local models are based on the often invalid assumption that the step length of particles is much less than a length scale associated with the tracer being used, and therefore that nonlocal models are preferable in general. Local models additionally assume random particle movements (Meysman et al. 2003), a questionable assumption given the elastic property of mud. Nonlocal transition matrix models are based on the first-order Markovian assumption that displacement of a particle is independent of previous movements of that particle (Meysman et al. 2003). However, a particle moved by a burrower may be either sequestered from future movement by the compaction around the burrow or preferentially moved if another animal follows the path of least resistance. A particle’s history is also important in granular mechanics, because the friction force depends on interactions with surrounding particles (Duran 2000). This history dependence may average out over many particles and be statistically unimportant. Alternatively, it could result in preferential movement of particles that have recently been moved while other particles remain in place, leading to overestimation of total mixing. Development of the lattice-automaton bioturbation simulator (LABS) provides a mechanism- based way of studying bioturbation (Choi et al. 2002). In this computer simulation, sediment is modeled as a 2-D lattice of grains and water through which automatons, the modelled infauna, move. The automatons follow prescribed rules for movement and ingestion and egestion of particles that are designed to mimic natural behaviours of specific groups of animals (e.g., small, capitellid- like deposit feeders) (Choi et al. 2002). LABS has successfully predicted values of the biodiffusion

coefficient, DB, similar to those measured in the field with similar animal densities (Boudreau et al. 2001). These results are particularly impressive, given the lack of data on basic features of the animals being modelled (e.g., velocities) and on the mechanical interactions between the animals and the sediment. Adding realistic mechanical constraints should improve next-generation models based on the elastic properties of sediment and fracture by animals and will contribute to mechanistic understanding of bioturbation. Models of fracture in heterogeneous materials such as wood and cement may be applicable to marine muds (e.g., Schlangen & Garboczi 1996).

Feeding in a crack Because their scheme remains widely used, relevance of our new understanding of burrowing is reviewed with respect to the original feeding guild classification of Fauchald & Jumars (1979). First, it is recommended that potential users who do not resort to the primary literature update this guild classification by reference to the summaries in Rouse & Pleijel (2001). Our new understanding of burrowing by crack propagation, together with still-limited observation, suggests to us a number of changes. A clear recommendation is to be skeptical of observations made on one or a few specimens not known to be in good condition. Because animals are more easily observed at the surface, animals observed rarely there may not be performing representative behaviours when they are on the surface. Sternaspids have been considered subsurface deposit feeders, and the authors have no disagree- ment with that classification. Several workers (e.g., Day 1967, cited in Rouse & Pleijel 2001) have suggested, however, that these worms sit at the sediment surface with the rear plate and gills at the sediment surface. However, this observation may have been based on moribund individuals, much like early depictions of Yoldia feeding at the sediment-water interface (e.g., Figure 86 in Yonge & Thompson 1976). The authors have observed that Sternaspis is a vigorous subsurface burrower that rarely approaches the interface and suggest a new common name based on obvious analogy: the bubble worm. Specimens have been kept in mud in sea tables for months without any surface manifestations whatsoever (P.A. Jumars, personal observation).

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Fauchald & Jumars (1979) classified scalibregmids as subsurface deposit feeders, yet Scali- bregma appears to access surface materials quickly (Blair et al. 1996). In observations (P.A. Jumars and K.M. Dorgan, unpublished data) of Scalibregma inflatum (from Puget Sound, Washington) in laboratory microcosms, this species maintains a cylindrical surface opening, apparently for respi- ration. Such an opening may allow the animal to sense surface phytodetrital events and may serve to trap some depositing materials. A new question to which there is yet no answer is to what extent a crack-producing animal can steer its crack to the surface and take advantage of freshly deposited material there. Cossurids often show distinct subsurface depth preference in sectioned cores (e.g., Jumars 1978). Tzetlin (1994), however, drew a conceptual diagram of surface deposit feeding in one live specimen. He offered caveats about the condition of this specimen, but subsequent citations have not carried along this warning. It is strongly suspected that this specimen was moribund and that cossurids typically feed below the primary sediment-water interface in cracks of their own manu- facture. The fact that they can access surface sediments quickly (Blair et al. 1996), however, suggests that they can propagate cracks very near to or even to the sediment-water interface. Based on morphology and observation of a few individuals (P.A. Jumars, unpublished data), it may be that trichobranchids also feed similarly below the sediment-water interface. The morphology of magelonids is also strongly indicative of burrowing. Most problematic for classifiers will be cirratulids and terebellids, which certainly across, and perhaps within, species clearly span both the classical ideas of surface (sediment-water interface) deposit feeding and the newly identified guild of feeders on surfaces created below the sediment- water interface by cracking. It is suggested that the majority of bipalpate cirratulids (and at least some other cirratulids) will be found to be crack makers and feeders, with some clear exceptions that make mudballs (Levin & Edesa 1997) — and no doubt some more subtle exceptions. Cirratulids also have been seen to access fresh phytodetritus quickly (Blair et al. 1996), again suggesting that the cracks they make may come close to the surface and perhaps cause subduction of surficial materials. A number of cirratulids and cossurids show a similar body plan in which segments are many and long. These species generally have muscular expansions near both the prostomium and the pygidium. The analogy to a long train with an engine at either end is striking; it is far easier to pull from either end than to push when the burrowing direction is reversed. Burrowing by liquefaction in sands is known in terebellids (Nowell et al. 1989). Morphology will help (e.g., the Artacama illustration; Figure 10B), but in situ and laboratory observations will be needed where stronger evidence is required. The crack-utilising guild across polychaete families most commonly bears some variety of expandable wedge, gills to deal with this likely low-oxygen environment of high, unsteady oxidant demand and tentacles or spines to free particles from the matrix for ingestion. Because they had no concept of burrowing by crack propagation, Fauchald & Jumars (1979) were inclined to associate tentacles with surface deposit feeding in the absence of evidence to the contrary. No such association should be assumed. Biogeochemical implications of fracture in marine muds include potential release of macro- molecules trapped in the organic matrix and preferential access to some areas of sediment resulting from microscale differences in adhesion. Diffusion through a gel is slowed little from that through the ungelled liquid for small molecules, but molecules larger than the pore size can be trapped in the matrix. Cracks may release trapped macromolecules for consumption or for diffusion or advection through or out of the sediment. Cracks propagate in the direction of least resistance, which suggests that animals preferentially follow a path recently cracked or containing less cohesive

or adhesive material. Research on the dependence of KIc on organic content and lability of sediments could lead to predictions either of preferential ingestion of organic material or the possibility of pockets of sticky organic material sequestered from deposit feeders. The interface of a membrane-encased,

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compacted faecal pellet may cause cracks to go around the pellet, leaving it intact and the encased material unavailable to deposit feeders. Biogenic, discoidal cracks do not appear to have been reported from the fossil record (Jumars et al. 2006). Perhaps they close and anneal quickly, but given their unexpected shapes (Johnson et al. 2002) no one may have thought to link such cracks with a biogenic mechanism. The existence of this mechanism of burrowing muddies the distinction between surface and subsurface deposit feeding, particularly if cracks are found to propagate close enough to the sediment-water interface that newly deposited materials can fall in. Moreover, the mechanical similarities between feeding on the sediment-water interface and feeding on a newly created surface in a propagated crack make it very likely that many species can do both.

Methodological considerations Crack propagation is facilitated along an interface for which adhesion between the two materials is less than the cohesion in one material (Figure 5) (Cook & Gordon 1964). This phenomenon has direct relevance to marine sediments, both naturally in the presence of boulders and in observations and experimental designs involving walls in both lab and field studies. Benthic observational tools include transparent aquaria, time-lapse, sediment-profile imagery (Diaz & Cutter 2001, Solan & Kennedy 2002) and planar oxygen sensors (Koenig et al. 2001), all of which involve observing a 2-D vertical section of sediment through a rigid, glass barrier. These studies implicitly assume that the observed animals are representative of the community. However, the sediment-glass interface facilitates crack propagation along the interface, while the solid boundary allows worms to exert higher stresses with the displacement caused by pharyngeal eversion. Because of these two factors, it is likely that many burrowers in muds congregate at glass walls, resulting in overestimation of community abundance and activity in long-term studies. This increased activity may result in overestimation of bioturbation rates in laboratory studies, with wall effects increasing with decreas- ing container size. Both Nereis virens and Yoldia sp. burrowing in aquaria of gelatin tend to end up against a wall or the bottom and then follow the wall. Although gelatin makes these observations clearer, congregation near aquarium walls is frequently observed in natural sediment as well. The crack-shaped burrow extends further from Nereis burrowing against an aquarium wall than in the middle of the aquarium (8Ð10 cm from the wall) (Figure 14) (K.M. Dorgan, unpublished data). Walls may have the opposite effect on animal distributions in granular materials. Because stress chains branch with distance from a point force, the area over which the force is distributed becomes much smaller closer to a wall with fewer stress chains to bear the load. In an elastic solid, the rigidity of a solid boundary allows the animal to exert greater stress with a given displacement and

Figure 14 (A) Burrow shape of Nereis virens in gelatin 8Ð10 cm from glass wall compared with (B) against glass wall of aquarium (K.M. Dorgan, unpublished data).

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Figure 15 Light-coloured stress fields in a bounded granular medium, shown by photoelastic stress analysis (Dantu 1957).

more easily propagate a crack, but resistance to grain displacements in a granular material increases with increasing pressure, which is increased through the presence of a nearby wall (Figure 15; Dantu 1957). Animals are therefore likely to be passively directed away from rigid boundaries in sands. Size, density and food quality of particle tracers have been considered in terms of food selection by deposit feeders (Self & Jumars 1988), which affects mixing rates, but not in terms of mixing by burrowing. Granular materials separate by grain size, with larger grains moving upward during mixing (Duran 2000). In adhesive sediments, tracer particles added to the surface will behave more discretely than particles bound in the polymeric matrix, and may be preferentially moved, leading to overestimation of mixing rates in tracer studies. Surface characteristics such as roughness and hydrophobicity as well as size and density of particles affect mixing rates in sediments with both elastic and granular behaviours and thus need to be considered as potential sources of artifacts in tracer measurements.

Summary and future directions Mechanical constraints of sediments on burrowers provide new insights into the anatomy and behaviour of individuals; burrowers in mud are generally wedge-shaped or have muscular anterior regions to extend their burrows by crack propagation. This fracture may be facilitated hydraulically, with expansions serving as both wedges and O-rings to drive fluid into the crack tip. Burrowers are functionally similar across phyla with vastly different anatomies. At the same time, burrowers in mud and sand are often anatomically similar and have similar behaviours, but their physical mechanisms of burrowing differ between the two media. In this review, behaviours and anatomies of burrowing animals are correlated with physical constraints of the sediment environment, but the observations are largely qualitative, and quantitative data are lacking. For example, amphipods are bubble-shaped, but do their aspect ratios match those predicted for bubbles in sediments? To what extent can interspecific differences in body shape be explained by differences in sediment properties? Obviously, the shapes need to be measured under the conditions in the burrow, not in a specimen bottle. Clearly there are trade-offs between energetics (cost increasing with deviation from the predicted aspect ratio, but how much?) and the need for gut (and other internal organ) capacity. Furthermore, the feedback mechanisms between behaviour of burrowers and sediment properties have not been quantified. For example, an animal may passively either follow or avoid the path of another animal depending on whether the trace left

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behind is a crack that has closed but not fully annealed (facilitating propagation of another crack- shaped burrow along the same path) or a cylindrical burrow with walls of compacted sediment (turning a crack away in another direction). An explicit mechanical model for burrowing provides a framework around which to generate and test such hypotheses. Areas in which sediment mechanics should be included in benthic studies are also indicated. Most obviously, mixing of particles depends strongly on the material properties of the sediment. Particles behave discretely in granular sands, but the polymer matrix of muds holds nearby particles together, resulting in their nonindependent mixing. Key questions in furthering bioturbation research in muds are how, how often and under what conditions a crack becomes a burrow. A crack that closes after an animal passes results in minimal particle mixing, whereas vertical cylindrical burrows cave in or fill with surface sediments. Bubbles have a flattened disk shape and stay within the elastic limit of muds, but animals are much more three-dimensional. Animals may displace sediment beyond the elastic limit, resulting in permanent deformation and a cylindrical trace. Animals also actively line burrow walls with mucus, making them more permanent. The mechanical behaviour of heterogeneous, viscoelastic sediments depends on both temporal and spatial scales of deformations as well as stress history. Future research on the dependence of the stress-strain relationship on strain rate, time of deformation and stress history will enable predictions about burrow formation. Burrow formation is important in considering not only particle mixing, but also the biome- chanics of burrowing. If sediment remains predominately elastic during the passage of an animal, the burrow will remain crack-shaped and the elastic restoring force will be important. This rebound would allow energy savings by storage of elastic strain energy and a reduced need for circular muscles in peristaltic burrowing. Scaling is important not only in terms of the animal’s size, but also the animal’s size in relation to the grain size. Sediment heterogeneity is largely scale-dependent because infaunal sizes vary over orders of magnitude, and homogeneity may be largely a matter of perspective. Relative scaling of organisms and grain size becomes particularly important in the transition region between granular and elastic behaviour, and mechanical testing should be conducted on appropriate scales of both space and time. Granular materials can behave elastically on larger scales, whereas on smaller scales individual grains are important and stress chains dominate behaviour (Goldenberg & Goldhirsch 2005). Moreover, much of the extensive literature on mechanical behaviours of viscoelastic solids and granular materials focuses on vastly different temporal or spatial scales and boundary conditions than experienced by burrowers. For example, equations governing fluidised beds are presented that are useful in gaining intuition, but their application to, for example, the small-scale unsteady pumping by Arenicola is questionable at best. They need modification for biological application. In this review, we have speculated extensively about how mechanical properties of sediments may drive animal behaviour. Although it is known that burrowers in mud do propagate cracks and that cracks propagate in the direction of least resistance, it is not known whether animals necessarily move in that direction or can use sensory information and mechanical means to steer cracks. The application of a quantitative model to burrowing generates hypotheses based on predicted, ener- getically efficient behaviours. Energetic efficiency is only one component of animal fitness, and deviations from predicted behaviours suggest alternate fitness benefits. An integrated approach to studying burrowing behaviour and resultant infaunal distribution, particle mixing and geochemical profiles is essential to improving predictive capabilities. Burrowers both affect and are affected by material properties of sediments. Feedback mechanisms necessitate combining an explicit mechanical model of sediments with research on behaviour, including how closely animals follow predictions. Despite the length of this review, it has barely scraped the surface of the rich interactions that can be anticipated when realistic, quantitative descriptions of material properties of sediments are coupled with analyses of animal mechanics and behaviours.

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Acknowledgements We thank Eric Landis, Steven Vogel, Les Watling and Larry Mayer for helpful comments on the manuscript. This research was supported by an NSF Graduate Research Fellowship, an NDSEG Fellowship and ONR Grant No. N00014-02-1-0658 to Larry Mayer.

References

Abdalla, A.M., Hettiaratchi, D.R.P. & Reece, A.R. 1969. The mechanics of root growth in granular media. Journal of Agricultural Engineering Research 14, 236Ð248. Alexander, R.M. 2003. Principles of Animal Locomotion. Princeton, NJ: Princeton University Press. Alexander, R.R., Stanton Jr., RJ. & Dodd, J.R. 1993. Influence of sediment grain size on the burrowing of bivalves: correlation with distribution and statigraphic persistence of selected Neogene clams. Palaios 8, 289Ð303. Aller, R.C. 1982. The effects of macrobenthos on chemical properties of marine sediment and overlying water. In Animal-Sediment Relations, P.L. McCall & M.J.S. Tevesz (eds), New York: Plenum Press, 53Ð104. Aller, R.C. 1988. Benthic fauna and biogeochemical processes in marine sediments: the role of burrow structures. In Nitrogen Cycling in Coastal Marine Environments, T.H. Blackburn & J. Sorensen (eds), New York: Wiley, 301Ð338. Anderson, T.L. 1995. Fracture Mechanics: Fundamentals and Applications. Boca Raton, FL: CRC Press. Ansell, A.D. & Peck, L.S. 2000. Burrowing in the Antarctic anemone, Halcampoides sp., from Signy Island, Antarctica. Journal of Experimental Marine Biology and Ecology 252, 45Ð55. Ansell, A.D. & Trueman, E.R. 1968. The mechanism of burrowing in the anemone, Peachia hastata Gosse. Journal of Experimental Marine Biology and Ecology 2, 124Ð134. Atkinson, R.J.A. & Taylor, A.C. 1988. Physiological ecology of burrowing decapods. In Aspects of Decapod Crustacean Biology, A.A. Fincham & P. Rainbow (eds), Symposium of the Zoological Society of London 59, 201Ð226. Bellwood, O. 2002. The occurrence, mechanics, and significance of burying behavior in crabs (Crustacea: Brachyura). Journal of Natural History 36, 1223Ð1238. Blair, N.E., Levin, L.A., DeMaster, D.J. & Plaia, G. 1996. The short-term fate of fresh algal carbon in continental slope sediments. Limnology and Oceanography 41, 1208Ð1219. Boudreau, B.P., Algar, C., Johnson, B.D., Croudace, I., Reed, A., Furukawa, Y., Dorgan, K.M., Jumars, P.A., Grader, A.S. & Gardiner, B.S. 2005. Bubble growth and rise in soft sediments. Geology 33, 517Ð520. Boudreau, B.P., Choi, J., Meysman, F.J.R. & Francois-Carcaillet, F. 2001. Diffusion in a lattice-automaton model of bioturbation by small deposit feeders. Journal of Marine Research 59, 749Ð768. Bousfield, E.L. 1973. Shallow-Water Gammaridean Amphipoda of New England. Ithaca, NY: Comstock Publishing Associates. Brown, A.C. & Trueman, E.R. 1991. Burrowing of sandy-beach molluscs in relation to penetrability of the substratum. Journal of Molluscan Studies 57, 134Ð136. Chandler, H.W. 1984. The use of non-linear fracture mechanics to study the fracture properties of soils. Journal of Agricultural Engineering Research 29, 321Ð327. Chapman, G. 1949. The thixotropy and dilatancy of a marine soil. Journal of the Marine Biological Association of the United Kingdom 28, 123Ð140. Chen, Z. & Mayer, L.M. 1999. Sedimentary metal bioavailability determined by the digestive constraints of marine deposit feeders: gut retention time and dissolved amino acids. Marine Ecology Progress Series 176, 139Ð151. Choi, J., Francois-Carcaillet, F. & Boudreau, B.P. 2002. Lattice-automaton bioturbation simulator (LABS): implementation for small deposit feeders. Computers and Geosciences 28, 213Ð222. Clark, R.B. 1964. Dynamics in Metazoan Evolution. London: Oxford University Press. Cook, J. & Gordon, J.E. 1964. A mechanism for the control of crack propagation in all-brittle systems. Proceedings of the Royal Society Series A 252, 508Ð520.

117 7044_book.fm Page 118 Friday, April 14, 2006 1:28 PM

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Dantu, P. 1957. Contribution à l’étude mécanique et géométrique des milieux pulvérulents. Proceedings of the 4th International Conference on Soil Mechanics and Foundation Engineering, 144Ð148. Day, J.H. 1967. A Monograph on the Polychaeta of Southern Africa. Part 2. Sedentaria. London: British Museum (Natural History). Diaz, R.J. & Cutter, G.R.J. 2001. In situ measurement of organism-sediment interaction: rates of burrow formation, abandonment, and sediment oxidation, reduction. In Organism-Sediment Interactions, J.Y. Aller et al. (eds), Columbia, SC: University of South Carolina Press, 19Ð32. Dorgan, K.M., Jumars, P.A., Johnson, B.D., Boudreau, B.P. & Landis, E. 2005. Burrow elongation by crack propagation. Nature 433, 475. Duran, J. 2000. Sands, Powders, and Grains: An Introduction to the Physics of Granular Materials. New York: Springer. Edmonds, J., Cushing, J.M., Constantino, R.F., Henson, S.M., Dennis, B. & Desharnais, R.A. 2003. Park’s Tribolium competition experiments: a non-equilibrium species coexistence hypothesis. Journal of Ecology 72, 703Ð712. Elder, H.Y. 1973. Direct peristaltic progression and the functional significance of the dermal connective tissues during burrowing in the polychaete Polyphysia crassa (Oersted). Journal of Experimental Biology 58, 637Ð655. Elder, H.Y. 1980. Peristaltic mechanisms. In Aspects of Animal Movement, H.Y. Elder & E R. Trueman (eds), Cambridge: Cambridge University Press, 71Ð92. Fauchald, K. & Jumars, P.A. 1979. The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology: An Annual Review 17, 193Ð284. Fountain, A.G., Jacobel, R.W., Schlichting, R. & Jansson, P. 2005. Fractures as the main pathways of water flow in temperate glaciers. Nature 433, 618Ð621. Frankel, L. & Mead, D.J. 1973. Mucilaginous matrix of some estuarine sands in Connecticut. Journal of Sedimentary Petrology 43, 1090Ð1095. Geng, J., Howell, D., Longhi, E., Behringer, R.P., Reydellet, G., Vannel, L., Clement, E. & Luding, S. 2001. Footprints in sand: the response of a granular material to local perturbations. Physical Review Letters 87, 035506. Goldenberg, C. & Goldhirsch, I. 2005. Friction enhances elasticity in granular solids. Nature 435, 188Ð191. Gordon, J.E. 1976. The New Science of Strong Materials: or Why You Don’t Fall Through the Floor. Princeton, NJ: Princeton University Press. Grall, J. & Chauvaud, L. 2002. Marine eutrophication and benthos: the need for new approaches and concepts. Global Change Biology 8, 813Ð830. Hartman, O. 1955. Endemism in the North Pacific Ocean, with emphasis on the distribution of marine annelids, and descriptions of new or little known species. In Essays in the Natural Sciences in Honor of Captain Allan Hancock. Los Angeles: University of Southern California Press, 39Ð60. Hartman, O. 1958. Systematic account of some marine invertebrate animals from the deep basins off southern California. Allan Hancock Pacific Expeditions 22, 69Ð215. Hettiaratchi, D.R.P. & Ferguson, C.A. 1973. Stress-deformation behavior of soil in root growth mechanics. Journal of Agricultural Engineering Research 18, 309Ð320. Hollertz, K. & Duchene, J.-C. 2001. Burrowing behaviour and sediment reworking in the heart urchin Brissopsis lyrifera Forbes (Spatangoida). Marine Biology 139, 951Ð957. Hunter, R.D. & Elder, H.Y. 1989. Burrowing dynamics and energy cost of transport in the soft-bodied marine invertebrates Polyphysia crassa and Priapulus caudatus. Journal of Zoology 218, 209Ð222. Hunter, R.D., Moss, V.A. & Elder, H.Y. 1983. Image analysis of the burrowing mechanisms of Polyphysia crassa (Annelida: Polychaeta) and Priapulus caudatus (Priapulida). Journal of Zoology 199, 305Ð323. Jaeger, H.M. & Nagel, S.R. 1992. Physics of the granular state. Science 255, 1523Ð1531. Johnson, B.D., Boudreau, B.P., Gardiner, B.S. & Maass, R. 2002. Mechanical response of sediments to bubble growth. Marine Geology 187, 347Ð363. Johnson, R.G. 1974. Particulate matter at the sediment-water interface in coastal environments. Journal of Marine Research 32, 313Ð330. Jones, M.L. 1968. On the morphology, feeding, and behavior of Magelona sp. Biological Bulletin (Woods Hole) 134, 272Ð297.

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MACROFAUNAL BURROWING

Jumars, P.A. 1978. Spatial autocorrelation with RUM (Remote Underwater Manipulator): vertical and hori- zontal structure of a bathyal benthic community. Deep-Sea Research 25, 589Ð604. Jumars, P.A., Dorgan, K.M., Mayer, L.M., Boudreau, B.P. & Johnson, B.D. 2006. Material constraints on infaunal lifestyles: May the persistent and strong forces be with you. In Trace Fossils: Concepts, Problems, Prospects, W. Miller, III (ed.). Elsevier, In press. Kanazawa, K. 1992. Adaptation of test shape for burrowing and locomotion in spatangoid echinoids. Palae- ontology 35, 733Ð750. Keudel, M. & Schrader, S. 1999. Axial and radial pressure exerted by earthworms of different ecological groups. Biology and Fertility of Soils 29, 262Ð269. Koehl, M.A.R. 1982. Mechanical design of spicule-reinforced connective tissue: stiffness. Journal of Exper- imental Biology 98, 239Ð267. Koenig, B., Holst, G., Glud, R.N. & Kuehl, M. 2001. Imaging of oxygen distributions at benthic interfaces: a brief review. In Organism-Sediment Interactions, J.Y. Aller et al. (eds), Columbia, SC: University of South Carolina Press, 63Ð71. Kudenov, J.D. 1977. The functional morphology of feeding in three species of maldanid polychaetes. Zoo- logical Journal of the Linnean Society 60, 95Ð109. Lastra, M., Dugan, J.E. & Hubbard, D.M. 2002. Burrowing and swash behavior of the Pacific mole crab Hippa pacifica (Anomura, Hippidae) in tropical sandy beaches. Journal of Crustacean Biology 22, 53Ð58. Levin, L.A. & Edesa, S. 1997. The ecology of cirratulid mudballs on the Oman margin, northwest Arabian Sea. Marine Biology 128, 671Ð678. Meysman, F.J.R., Boudreau, B.P. & Middelburg, J.J. 2003. Relations between local, nonlocal, discrete and continuous models of bioturbation. Journal of Marine Research 61, 391Ð410. Mulsow, S., Boudreau, B.P. & Smith, J.N. 1998. Bioturbation and porosity gradients. Limnology and Ocean- ography 43, 1Ð9. Nel, R., McLachlan, A. & Winter, D.P.E. 1999. The effect of sand particle size on the burrowing ability of the beach mysid Gastrosaccus psammodytes Tattersall. Estuarine Coastal and Shelf Science 48, 599Ð604. Nel, R., McLachlan, A. & Winter, D.P.E. 2001. The effect of grain size on the burrowing of two Donax species. Journal of Experimental Marine Biology and Ecology 265, 219Ð238. Nicolaisen, W. & Kanneworf, E. 1969. On the burrowing and feeding habits of the amphipods Bathyporeia pilosa Lindstrom and Bathyporeia sarsi Watkin. Ophelia 6, 231Ð250. Nowell, A.R.M., Jumars, P.A. & Eckman, J.E. 1981. Effects of biological activity on the entrainment of marine sediments. Marine Geology 42, 155Ð172. Nowell, A.R.M., Jumars, P.A. & Southard, J.B. 1989. Responses of intertidal macrofauna to ripple migration in a laboratory racetrack flume. In Ecology of Marine Deposit Feeders. G.R. Lopez et al. (eds), New York: Springer-Verlag, 247Ð268. Purcell, E.M. 1977. Life at low Reynolds number. American Journal of Physics 45, 3Ð11. Quillin, K.J. 1998. Ontogenetic scaling of hydrostatic skeletons: geometric, static stress and dynamic stress scaling of the earthworm Lumbricus terrestris. Journal of Experimental Biology 201, 1871Ð1883. Quillin, K.J. 2000. Ontogenetic scaling of burrowing forces in the earthworm Lumbricus terrestris. Journal of Experimental Biology 203, 2757Ð2770. Reiner, M. 1964. The Deborah number. Physics Today 17, 62. Rhoads, D.C., McCall, P.L. & Yingst, J.Y. 1978. Disturbance and production on the estuarine seafloor. American Scientist 66, 557Ð586. Riisgård, H.U., Berntsen, I. & Tarp, B. 1996. The lugworm (Arenicola marina) pump: characteristics, mod- elling, and energy cost. Marine Ecology Progress Series 138, 149Ð156. Roast, S.D., Widdows, J., Pope, N. & Jones, M. B. 2004. Sediment-biota interactions: mysid feeding activity enhances water turbidity and sediment erodability. Marine Ecology Progress Series 281, 145Ð154. Rouse, G.W. & Pleijel, F. 2001. Polychaetes. Oxford: Oxford University Press. Rozbaczylo, N. & Mendez, M.A. 1996. Artacama valparaisiensis, a new species of Terebellidae (Annelida: Polychaeta) from subtidal soft bottoms of Valparaiso Bay, Chile. Proceedings of the Biological Society of Washington 109, 138Ð142. Santamarina, J.C., Klein, K.A. & Fam, M.A. 2001. Soils and Waves. Chichester, U.K.: John Wiley & Sons, Ltd.

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Schiffelbein, P. 1984. Effect of benthic mixing on the information content of deep-sea stratigraphical signals. Nature 311, 651Ð653. Schinner, G.O. 1993. Burrowing behavior, substratum, preference, and distribution of Schizaster canaliferus (Echinoidea: Spatangoida) in the Northern Adriatic Sea. Marine Ecology 14, 129Ð145. Schlangen, E. & Garboczi, E.J. 1996. New method for simulating fracture using an elastically uniform random geometry lattice. International Journal of Engineering Science 34, 1131Ð1144. Schmidt, J.L., Deming, J.W., Jumars, P.A. & Keil, R.G. 1998. Constancy of bacterial abundance in surficial marine sediments. Limnology and Oceanography 43, 976Ð982. Self, R.F.L. & Jumars, P.A. 1988. Cross-phyletic patterns of particle selection by deposit feeders. Journal of Marine Research 46, 119Ð143. Seymour, M.K. 1969. Locomotion and coelomic pressure in Lumbricus terrestris L. Journal of Experimental Biology 51, 47Ð58. Sherwood, C.R., Drake, D.E., Wiberg, P.L. & Wheatcroft, R.A. 2002. Prediction of the fate of DDT in sediments on the Palos Verdes margin. Continental Shelf Research 22, 1025Ð1058. Shull, D.H. & Yasuda, M. 2001. Size-selective downward particle transport by cirratulid polychaetes. Journal of Marine Research 59, 453Ð473. Solan, M. & Kennedy, R. 2002. Observation and quantification of in situ animal-sediment relations using time-lapse sediment profile imagery (t-SPI). Marine Ecology Progress Series 228, 179Ð191. Stanley, S.M. 1970. Relation of Shell Form to Life Habits of the Bivalvia (Mollusca). Boulder, CO: The Geological Society of America, Inc. Stovold, R.J., Whalley, W.R. & Harris, P.J. 2003. Dehydration does not affect the radial pressures produced by the earthworm Aporrectodea caliginosa. Biology and Fertility of Soils 37, 23Ð28. Timmerman, K., Christensen, J.H. & Banta, G.T. 2002. Modeling of advective solute transport in sandy sediments inhabited by the lugworm Arenicola marina. Journal of Marine Research 60, 151Ð169. Torquato, S. 2001. Random Heterogeneous Materials: Microstructure and Macroscopic Properties. New York: Springer. Trevor, J.H. 1977. The burrowing of Nereis diversicolor O.F. Muller, together with some observations on Arenicola marina (L.) (Annelida: Polychaeta). Journal of Experimental Marine Biology and Ecology 30, 129Ð145. Trevor, J.H. 1978. The dynamics and mechanical energy expenditure of the polychaetes Nephtys cirrosa, Nereis diversicolor, and Arenicola marina during burrowing. Estuarine and Coastal Marine Science 6, 605Ð619. Trueman, E.R. 1970. The mechanism of burrowing of the mole crab, Emerita. Journal of Experimental Biology 53, 701Ð710. Trueman, E.R. 1975. The Locomotion of Soft-bodied Animals. New York: American Elsevier Publishing Company, Inc. Trueman, E.R. 1983. Locomotion in molluscs. In The Mollusca, A.S.M. Saleuddin & K.M. Wilbur (eds), New York: Academic Press, Inc., 155Ð198. Trueman, E.R. & Brown, A. C. 1992. The burrowing habit of marine gastropods, Advances in Marine Biology 28, 389Ð431. Trueman, E.R. & Jones, H.D. 1977. Crawling and burrowing. In Mechanics and Energetics of Animal Locomotion, R.M. Alexander & G. Goldspink (eds), London: Chapman & Hall, 204Ð221. Tzetlin, A.B. 1994. Fine morphology of the feeding apparatus of Cossura sp. (Polychaeta, Cossuridae) from the White Sea. Memoires du Museum National d’Histoire Naturelle, Paris 162, 137Ð143. Tzetlin, A.B. & Filippova, A.V. 2005. Muscular system in polychaetes (Annelida). Hydrobiologia 535/536, 113Ð126. Tzetlin, A.B., Zhadan, A., Ivanov, I., Muller, M.C.M. & Purschke, G. 2002. On the absence of circular muscle elements in the body wall of Dysponetus pygmaeus (Chrysopetalidae, ‘Polychaeta’, Annelida). Acta Zoologica (Stockholm) 83, 81Ð85. Voparil, I.M., Burgess, R.M., Mayer, L.M., Tien, R., Cantwell, M.G. & Ryba, S.A. 2003. Digestive bioavail- ability to a deposit feeder (Arenicola marina) of polycyclic aromatic hydrocarbons associated with anthropogenic particles. Environmental Toxicology and Chemistry 23, 2618Ð2626.

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Watling, L. 1988. Small-scale features of marine sediments and their importance to the study of deposit feeding. Marine Ecology Progress Series 47, 135Ð144. Wilkes, J.O. 1999. Fluid Mechanics for Chemical Engineers. Upper Saddle River, NJ: Prentice-Hall PTR. Yannicelli, B., Palacios, R. & Gimenez, L. 2002. Swimming ability and burrowing time of two cirolanid isopods from different levels of exposed sandy beaches. Journal of Experimental Marine Biology and Ecology 273, 73Ð88. Yonge, C.M. & Thompson, T.E. 1976. Living Marine Molluscs. London: Collins.

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Oceanography and Marine Biology: An Annual Review, 2006, 44, 123-195 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis

MEDITERRANEAN CORALLIGENOUS ASSEMBLAGES: A SYNTHESIS OF PRESENT KNOWLEDGE

ENRIC BALLESTEROS Centre d’Estudis Avançats de Blanes — CSIC, Accés Cala Sant Francesc, 14, E-17300 Blanes, Girona, Spain E-mail: [email protected]

Abstract Coralligenous concretions, the unique calcareous formations of biogenic origin in Mediterranean benthic environments, are produced by the accumulation of encrusting algae growing in dim light conditions. This review provides an overview of the results obtained by the main studies dealing with these formations, including the environmental factors which influence the development of coralligenous communities, their distribution, types, assemblages, builders and eroders, the biotic relationships and processes that create and destroy coralligenous assemblages, their dynamics and seasonality, and the functioning of several outstanding and key species. Special attention is devoted to the biodiversity of coralligenous communities and a first estimation of the number of species reported for this habitat is provided. Major disturbances affecting coralligenous communities are discussed, ranging from large-scale events that are probably related to global environmental changes to degradation by waste water or invasive species. Degradation by fishing activities and by divers is also considered. Finally, the main gaps in current scientific knowledge of coralligenous communities are listed and some recommendations are made regarding their protection.

Introduction and description Encrusting calcareous algae are important components of benthic marine communities within the euphotic zone (Blanc & Molinier 1955, Adey & McIntyre 1973, Littler 1973a, Lebednik 1977, James et al. 1988, Dethier et al. 1991, Adey 1998) and their historical roles as reef builders have been chronicled thoroughly by Wray (1977). Coralline algae are major contributors to coral reef frameworks (Finckh 1904, Hillis-Colinvaux 1986, Littler 1972) where they usually are the dominant reef-forming organisms (Foslie 1907, Odum & Odum 1955, Lee 1967, Littler 1973b). Although encrusting corallines are adapted to grow at low light conditions (Littler et al. 1986, Vadas & Steneck 1988), coralline algal reef frameworks are usually restricted to littoral or shallow sublittoral environments throughout the marine realm (e.g., Littler 1973b, Adey & Vassar 1975, Laborel et al. 1994) because they easily withstand turbulent water motion and abrasion (Littler & Doty 1975, Adey 1978). The only known exception to this restriction is the coralligenous framework, a coralline algal concretion that thrives exclusively in Mediterranean deep waters (20Ð120 m depth). There is no real consensus among scientists studying benthic communities in the Mediterranean Sea about what a coralligenous habitat is. In this review a coralligenous habitat is considered to be a hard substratum of biogenic origin that is mainly produced by the accumulation of calcareous encrusting algae growing in dim light conditions. Algae and invertebrates growing in environments with low light levels are called sciaphilic in opposition to photophilic, that is, growing at high light levels. All plants and animals thriving in coralligenous habitats are, thus, sciaphilic. Although more

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extensive in the circalittoral zone, coralligenous habitats can also develop in the infralittoral zone, provided that light is dim enough to allow growth of the calcareous algae that produce the calcareous framework. Infralittoral coralligenous concretions always develop on almost vertical walls, in deep channels, or on overhangs, and occupy small surface areas. Communities developing in low light conditions near sea level, in sites of strong water movement and usually below the mediolittoral biogenic rim of the coralline alga Lithophyllum byssoides (Boudouresque & Cinelli 1976), are not considered in this review, even though they may exhibit small concretions of coralline algae. Other algal dominated communities thriving in the circalittoral zone, such as rhodolith beds (Basso & Tomaselli 1994) or Cystoseira zosteroides assemblages (Ballesteros 1990), are also excluded, as the coralline algal framework in these cases is reduced or almost nil. Some facies of coralligenous communities (and which are categorized as “pre-coralligenous” by several authors, e.g., Pérès & Picard 1964, Gili & Ros 1985, Ros et al. 1985) are also excluded from this review, but only if they refer to sciaphilic communities without a basal framework of coralline algae. Therefore, the main criterion used to define the coralligenous habitat is the presence of a bioherm of coralline algae grown at low irradiance levels and in relatively calm waters. This bioherm is always very complex in structure and, in fact, allows the development of several kinds of communities (Laborel 1961, Laubier 1966), including those dominated by living algae (upper part of the concretions), suspension feeders (lower part of the concretions, wall cavities and overhangs), borers (inside the concretions) and even soft-bottom fauna (in the sediment deposited in cavities and holes). Therefore, the coralligenous habitat should be considered more as a submarine landscape or community puzzle rather than a single community.

History and main studies Historical account of general and faunal studies The word ‘coralligenous’ (coralligène in French) was first used by Marion (1883) to describe the hard bottoms that fishermen from Marseilles called broundo and which are found at a depth of between 30 and 70 m, below seagrass meadows of Posidonia oceanica and above coastal muddy bottoms. Coralligène means ‘producer of coral’ and is related to the abundance of red coral (Corallium rubrum) found on this type of bottom. Marion (1883) includes long lists of fauna collected in these coralligène bottoms. Pruvot (1894, 1895) also used the word coralligène to describe similar bottoms in the Pyrenees region of the Mediterranean (Banyuls), and this terminol- ogy was included in bionomical descriptions of Mediterranean sea bottoms from the end of the nineteenth century. Feldmann (1937) subsequently described in detail the algal composition of the coralligenous assemblages from Banyuls and identified the main calcareous algae responsible for coralligenous bioherms. He also made observations of the animals contributing to the framework and of bioeroders. Pérès & Picard (1951) continued the work of Marion (1883) on coralligenous bottoms from the Marseilles region, defining the components of the coralligenous assemblages; they demonstrated their high microspatial variability and described the environmental factors which allow them to develop. Elsewhere in the Mediterranean, Bacci (1947), Tortonese (1958), Rossi (1958, 1961), Parenzan (1960) and Molinier (1960) characterized the pre-coralligenous and coralligenous bioherms in some areas of the Italian coast and Corsica and Pérès & Picard (1958) described the coralligenous communities from the northeastern Mediterranean. The last authors reported several warm-water species, as well as the absence of various species that dominate coralligenous concretions in the western Mediterranean. Laborel (1960, 1961) also expanded the study of coralligenous communities to other Mediterranean areas, including the eastern Mediterranean. He described five main coral- ligenous types (cave and overhang concretions, wall concretions, concretions at the base of submarine

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walls, concretions over flat rocky surfaces and platform coralligenous assemblages) and, in his 1960 paper, also provided the first quantified lists of algal and animal species obtained by scuba diving. In 1964 Pérès & Picard (1964) summarised existing knowledge of coralligenous communities, defining the notion of pre-coralligenous and simplifying the categories of Laborel (1961) into two coralligenous types: coralligenous assemblages over littoral rock and bank or platform coralligenous assemblages, according to the original substratum (rock or sediment) where concretion began. They proposed an evolutionary series relating the different biocenoses of the circalittoral zone in the Mediterranean and suggested that the coralligenous community was the climax biocenosis of this zone. They also used the word ‘precoralligenous’ to refer to a facies with a great development of erect, noncalcareous, sciaphilic algae and a low cover of invertebrates. An English summary of Pérès & Picard’s (1964) work can be found in Pérès (1967). At about the same time, Vaissière (1964), Fredj (1964) and Carpine (1964) made interesting contributions to the distribution and bionomic description of coralligenous concretions in the region of Nice and Monaco, east of Marseilles. Gamulin-Brida (1965) conducted the first bionomical studies of coralligenous communities in the Adriatic Sea and concluded that they are biogeographically very similar to those found in the northwestern Mediterranean, with a great abundance of large bryozoans, gorgonians and alcyonarians. Laubier (1966) made a major contribution to knowledge of invertebrates living in coralligenous assemblages, with his study based on data from the Pyrenean region of the Mediterranean. He was the first to report the high biodiversity of these substrata, he carefully studied the fauna of the concretions (particularly accurate are the studies on polychaetes, copepods and echinoderms) and defined the physico-chemical conditions allowing the coralligenous communities to develop. He was also the first to make a large number of observations related to the natural history of the species inhabiting coralligenous assemblages and, in particular, referred to the relationships of epibiosis, endobiosis, commensalism and parasitism. Subsequent to Laubier’s studies, Sarà (1968, 1969) described the coralligenous communities in the Pouilles region (Italy) and True (1970) collected quantitative samples from the coralligenous assemblages of Marseilles, providing data on the biomass of the main species of suspension feeders. Hong (1980, 1982) exhaustively described the coralligenous communities from Marseilles and the effects of sewage on their fauna. He also described the animals that contribute to these coralligenous frameworks and defined four different categories of invertebrates which can be distinguished by considering their ecological significance in the assemblages. Extensive lists of several taxonomic groups (mainly foraminiferans, sponges, molluscs, pycnogonids, amphipods and bryozoans) greatly increased the knowledge of the biodiversity of coralligenous communities. Gili & Ros (1984) reviewed the coralligenous communities of the Medes Islands, off the northeast coast of Spain, and accurately evaluated the total surface area occupied by coralligenous assemblages in this marine reserve (Gili & Ros 1985). Detailed species lists of most algal and animal groups for coralligenous communities from specific areas of the Spanish Mediterranean can also be found in Ballesteros et al. (1993) and Ballesteros & Tomas (1999). Sartoretto (1996) studied the growth rate of coralligenous buildups by radiocarbon dating and related the growth periods to different environmental conditions, mainly the eustatic water level and the transparency of the water column. He also identified the main calcareous algae that finally produce the framework and emphasised the importance of Mesophyllum alternans. The effect of sedimentation and erosion by browsers and borers was also quantified.

Algal studies Feldmann (1937) was the first to describe unequivocally the algal composition of coralligenous assemblages; he differentiated these substrata from the deep-water algal beds of Cystoseira spinosa

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and C. zosteroides, and identified the main calcareous algae responsible for coralligenous deposi- tion. The algal community growing on coralligenous assemblages was named the Pseudolitho- phyllum expansum-Lithophyllum hauckii association. Scuba diving was first used in the study of algal flora of coralligenous assemblages by Giaccone (1965), who made some species lists of coralligenous communities and described a particular plant association, the Pseudolithophyllo-Halimedetum platydiscae in the area of Palermo (Sicily). Giaccone & De Leo (1966) also used scuba diving to study the coralligenous and precoralligenous communities of the Gulf of Palermo by using the phytosociological method of Braun Blanquet. They distinguished both types of communities and referred to them as an association of Litho- phyllum expansum and Lithothamnion philippi (coralligenous) and an association of Halimeda platydisca and Udotea desfontainii (precoralligenous). The population of Laminaria rodriguezii growing over a coralligenous community at the island of Ustica was also studied by Giaccone (1967), although this endemic Mediterranean kelp is usually more abundant in deep-water rhodolith beds (fonds à pralinés) (Molinier, 1956). Boudouresque (1970) studied the macroalgal communities of coralligenous concretions as part of a detailed and exhaustive study of the sciaphilic benthic communities in the western Mediter- ranean. The accurate methodology (Boudouresque, 1971) included scuba sampling and further sorting and identification in the laboratory. Augier et al. (1971) used the same methods to study the algal sciaphilic communities around the island of Port-Cros (France). Boudouresque (1973) proposed that the terms coralligenous and precoralligenous be avoided, as they have a physiognomical value but do not refer to any bionomical or phytosociological entity; instead, he joined all the sciaphilic algal settlements under relatively sheltered conditions into one association (Peyssonnelietum rubrae), and created two subassociations, corresponding to the assem- blages developing in the infralittoral zone (Peyssonnelietum aglaothamnietosum) and the circalit- toral zone (Peyssonnelietum rodriguezelletosum). He reported the high biodiversity of these assem- blages and defined the ecological group of algae characteristic of coralligenous concretions (CC or Rodriguezellikon). Augier & Boudouresque (1975) argued that the algal composition of coralligenous communities thriving in deep water differs from that of sciaphilic assemblages from the infralittoral zone, and named it Rodriguezelletum strafforellii according to phytosociological nomenclature. Boudouresque (1980) and Coppejans & Hermy (1985) made significant contributions to the study of algal assemblages of coralligenous communities in Corsica, but Ballesteros (1991a,b,c, 1992) was the first to provide data on the dynamics and small-scale structure of algal assemblages from coralligenous communities. Giaccone et al. (1994) conducted a phytosociological review of sciaphilic assemblages described for the Mediterranean. According to this review, most phytobenthic coralligenous assem- blages should be included in the order Lithophylletalia, where two associations are distinguished: the Lithophyllo-Halimedetum tunae described by Giaccone (1965) and the Rodriguezelletum straf- forellii described by Augier & Boudouresque (1975). Phytobenthic assemblages growing in coral- ligenous concretions on vertical walls and overhangs in the infralittoral zone should be included in the order Rhodymenietalia, and mainly belong to the association Udoteo-Peyssonnelietum squamariae described by Molinier (1960) in Corsica, and which seems to be identical to the association of Peyssonnelia squamaria described by Feldmann (1937) for the Pyrenees region of the Mediterranean. Contributions by Ferdeghini et al. (2000) and Acunto et al. (2001), using photographic sampling, demonstrated the small-scale variability in algal assemblages from coralligenous communities, mainly due to the patchy distribution of calcareous algae and other dominant organisms. Recently, Piazzi et al. (2004) carefully studied the algal composition of coralligenous banks developing in three different subtidal habitats (islands, continental shores and offshore banks), and reported high spatial variability at reduced scales but no major differences between assemblages at a habitat level.

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Environmental factors and distribution Light Light is probably the most important environmental factor with respect to the distribution of benthic organisms along the rocky bottoms of the continental shelf (Ballesteros 1992, Martí et al. 2004, 2005). It is also very important for the development and growth of coralligenous frameworks, as its main builders are macroalgae which need enough light to grow but which cannot withstand high levels of irradiance (Pérès & Picard 1964, Laubier 1966). According to Ballesteros (1992), coralligenous communities are able to develop at irradiances ranging from 1.3 MJ mÐ2 yrÐ1 to 50Ð100 MJ mÐ2 yrÐ1, that is, between 0.05% and 3% of the surface irradiance. Similar ranges are reported by Ballesteros & Zabala (1993), who consider the lower light limit for the growth of Mediterranean corallines to be at around 0.05% of the surface irradiance (Figure 1). These values agree with those obtained by Laubier (1966) in the coralligenous com- munities of Banyuls, where he reported, at a depth of 32 m, light levels of 1.8Ð2.6% of surface irradiance at noon in September. However, light levels reaching different microenvironments of coralligenous communities can differ by at least two orders of magnitude. For example, Laubier (1966) reported light levels in an overhang dominated by red coral to be 17-fold lower than those recorded in an exposed, horizontal surface. Light levels reaching small holes and cavities of coralligenous banks must be almost zero, and similar to light levels reaching the bathyal zone or the innermost part of caves. The quality of light reaching coralligenous bottoms should also be taken into account. Most of the light belongs to the blue and green wavelengths, with green light dominating in relatively murky waters in winter and in coastal continental waters, and blue light dominating in summer and in offshore banks and islands (Ballesteros 1992) (Figure 2). Although most authors consider that light quantity is much more important than light quality in determining algal growth and primary production (e.g., Lüning 1981, Dring 1981), the absolute dominance of red algae in coralligenous assemblages close to their deepest distribution limit points to the ability of phyco- bilines to capture light in the ‘green window’ (Ballesteros 1992).

0 Tossa 20 Cabrera B 40

60

metres A 80

100

120 0.01 0.1 1 10 100 % surface irradiance

Figure 1 Light attenuation in the water column (circles) at two northwestern Mediterranean localities and depth ranges (bars) where coralligenous concretions develop over horizontal surfaces (A, Cabrera, oceanic waters; B, Tossa de Mar, continental coastal waters). (From data in Ballesteros 1992 and in Ballesteros & Zabala 1993.)

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A 10 0 m 5 2 3 m 1 0.5 0.2 0.1 10 m 0.05 0.02 % surface irradiance % surface 0.01 0.005 0.002 40 m 23 m 0.001

B 10 0 m 5 2 3 m 1 0.5 0.2 0.1 10 m 0.05 0.02 % surface irradiance % surface 0.01 0.005

0.002 40 m 23 m 0.001 360 400 440 480 520 560 600 640 680 λ (nm) uv v b g y r

Figure 2 Distribution by wavelength (uv: ultraviolet, v: violet, b: blue, g: green, y: yellow, r: red) of submarine irradiances relative to surface irradiance for several depths in August (A) and November (B) in waters off Tossa de Mar (northwestern Mediterranean). (From Ballesteros 1992.)

Nutrients, POC, DOC Dissolved nutrients in sea water at coralligenous depths follow the annual pattern described for coastal Mediterranean waters, with the highest values in winter and the lowest in summer. The mean annual water nitrate concentration near the coralligenous concretions at depths of 18 and 40 m at Tossa (northwestern Mediterranean) is around 0.6 µmol lÐ1, with peaks of 1.5 µmol lÐ1 in winter and undetectable levels in summer (Ballesteros 1992) (Figure 3). Similar values are reported for a station in Cabrera, at a depth of 50 m (Ballesteros & Zabala 1993). However, these values are much lower than those reported from stations situated close to river mouths, such as the coralli- genous communities around the Medes Islands, where mean annual values are close to 1 µmol lÐ1 (Garrabou 1997). Phosphate concentrations are much lower and are always below 0.1 µmol lÐ1 at

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-1 A 18 m 2.0 ) -1

1.5

1.0 0.08 0.5 0.06 Phosphates (µmol l

Nitrates, nitrites (µmol l Nitrates, 0.04

) B 40 m

-1 2.0 ) -1 1.5

1.0 0.08 0.5 0.06

0.04 Phosphates (µmol l Nitrates, nitrites (µmol l Nitrates, JF MAMJ J AS ONDJ

nitrates nitrites phosphates

Figure 3 Monthly levels of dissolved nutrient concentrations at depths of 18 and 40 m in sea water close to coralligenous concretions in Tossa de Mar (January 1983ÐJanuary 1984). (From Ballesteros 1992.)

Tossa and Cabrera (mean concentrations around 0.04 µmol lÐ1 or lower) (Ballesteros 1992, Balles- teros & Zabala 1993), and always below 0.2 µmol lÐ1 around the Medes Islands (mean concentrations around 0.13 µmol lÐ1) (Garrabou 1997) (Figure 3). Coralligenous communities seem to be adapted to these low nutrient concentrations in sea water, as increased nutrient availability greatly affects the specific composition, inhibits coralligenous construction, and increases destruction rates (Hong 1980). Mean annual particulate organic carbon (POC) rates of 387 µg C lÐ1 are reported for the near- bottom planktonic community at a depth of 15 m around the Medes Islands (Ribes et al. 1999a), although winter and spring values were much higher (500Ð800 µg C lÐ1). Dissolved organic carbon (DOC) rates, also reported by Ribes et al. (1999a) for the same site, amount to 2560 µg C lÐ1, peaking in spring and summer (Figure 4). Ribes et al. (1999a) concluded that the detrital fraction was the dominant component of total organic carbon in the near-bottom planktonic community throughout the year, which could be explained by the importance of runoff particles in the Medes Islands, but may also be due to the input of organic matter by macroalgal (and seagrass) production and the activity of benthic suspension feeders in removing microbial organisms from the plankton. However, further studies are necessary in this regard because the Medes Islands are strongly affected by continental inputs of DOC and POC, which is not usually the case for most Mediterranean coastal areas (mainly in islands or in the southern part).

Water movement Although flowing currents predominate at depths where coralligenous communities develop (Riedl, 1966), water movement generated by waves is very significant even at depths of 50 m (Ballesteros & Zabala, 1993; Garrabou, 1997) for wave heights >1 m. The year-round average of water motion Ð1 for a coralligenous community in the Medes Islands at a depth of 25Ð35 m is 40 mg CaSO4 h ,

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-1 1000 A 800

600

400

200

ive + detritic carbon (µg l ive 0

50 B )L -1 40

30

20 10 Live carbon (µg l Live 0 )

-1 6000 C 5000 4000 3000 2000 1000

0 Dissolved organic carbon (µg l Dissolved DJFMAMJJASON Time

Figure 4 Monthly averages expressed as µg C lÐ1 of live and detrital carbon (A), live carbon (B) and dissolved organic carbon (C) in waters close to coralligenous concretions around the Medes Islands (northwestern Mediterranean). (From Ribes et al. 1999a. With permission from Oxford University Press.)

that is, one order of magnitude lower than water motion at a depth of 2 m (Garrabou, 1997) (Figure 5). However, due to the intricate morphology of coralligenous frameworks, water movement can differ greatly between various microenvironments, in a similar way to that reported for light levels (Laubier, 1966).

Temperature Most of the organisms living in coralligenous communities are able to support the normal seasonal temperature range characteristic of Mediterranean waters. Although Pérès & Picard (1951) stated that coralligenous communities display a relative stenothermy, Laubier (1966) described an annual temperature range of 10Ð23ûC in the coralligenous assemblages of Banyuls. Pascual & Flos (1984)

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depth (m)

2

5

10

15

Coralligenous 20

25

30

35

0100200300 400 mg calcium sulphate dissolved h-1

Figure 5 Year-round average in water motion attenuation (mean ± SD) for a depth of between 0 and 35 m in a submarine wall at the Medes Islands. (From Garrabou 1997. With permission.)

found temperatures ranging between 12 and 20ûC at the shallowest limit of the coralligenous communities of the Medes Islands (20 m depth), although temperatures ranged from 12Ð16ûC close to their deepest limit (60 m depth) (Figure 6). Ballesteros (1992) reported more or less the same temperatures for the coralligenous assemblages developing at depths of 20 and 40 m at Tossa de Mar between the end of November and the end of June (13Ð16ûC), but differences of up to 9¼C in summer, when the thermocline is situated at a depth of around 35 m; however, peak temperatures of 22ûC were detected at the end of August at a depth of 40 m. In the Balearic Islands, where coralligenous communities are restricted to waters >40 m deep, water temperature ranges from 14.5Ð17ûC for most of the year, although occasional peaks of 22ûC are detected at the end of October, when the thermocline is at its deepest (Ballesteros & Zabala 1993). However, some organisms living in coralligenous assemblages from deep waters seem to be highly stenothermal, as they are never found in shallow waters. This is the case, for example, of the kelp Laminaria rodriguezii, which seems to be mainly restricted to depths >70 m and is seldom found between 50 and 70 m, except for in seamounts or upwelling systems (Ballesteros, unpublished data). Moreover, recent (1999) large-scale mortality events of benthic suspension feeders thriving in coralligenous communities have been attributed to unusually long-lasting periods of high temperatures during summer (Perez et al. 2000; Romano et al. 2000), although the ultimate cause of these mortalities remains unclear (possible causes include high temperatures, low food availability, pathogens and physiological stress).

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0 22 14 1618 20 21 20 19 18 17 16 14 13 10 15 17 19 21 22

20

30

40

50 depth (m) 60

70 12.5 12.513 13.51415 14 13.5 80

JFMAMJJ ASOND Time

Figure 6 Average seawater temperatures for a depth of between 0 and 80 m off the Medes Islands (July 1973ÐDecember 1977). Shaded area corresponds to depth of coralligenous outcrops. (From Pascual & Flos, 1984. With permission.)

Salinity The relatively shallow and coastal coralligenous communities of Banyuls and the Medes Islands experience salinity ranges between 37 and 38 (Laubier 1966, Pascual & Flos 1984), although salinity variations for coralligenous assemblages from insular areas should be lower.

Geographical distribution Coralligenous buildups are common all around the Mediterranean coasts, with the possible excep- tion of those of Lebanon and Israel (Laborel, 1987). According to Laborel (1961), the best developed formations are those found in the Aegean Sea, although the most widely studied banks are those of the northwestern Mediterranean; therefore, most of the data presented here come from this area.

Depth distribution The minimal depth for the formation of coralligenous frameworks depends on the amount of irradiance reaching the sea bottom. On vertical slopes in the area around Marseilles this minimal depth reaches 20 m, but it is much lower in other zones like the Gulf of Fos, where coralligenous communities are able to grow in shallower waters (12 m) because of the high turbidity of the water related to the Rhône mouth. This minimal depth is displaced to deeper waters in insular areas like Corsica or the Balearic Islands, where water transparency is very high (Ballesteros & Zabala 1993). However, coralligenous frameworks can appear in very shallow waters if light conditions are dim enough to allow a significant development of coralline algae (Laborel 1987, Sartoretto 1994) and they may even occur in the clearest waters like those around Cabrera, where they can be found at a depth of only 10 m in a cave entrance (Martí et al. 2004). The depth distribution of coralligenous assemblages in subhorizontal to horizontal bottoms for different Mediterranean areas is summarised in Table 1.

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Table 1 Depth intervals for the distribution of coralligenous outcrops in different Mediterranean areas

Region Depth (m) Reference Banyuls 20Ð40 Feldmann 1937, Laubier 1966 Marseilles 20Ð50 Laborel 1961, Hong 1980 Medes Islands 20Ð55 Gili & Ros 1984 Tossa de Mar 20Ð60 Ballesteros 1992 Naples 45Ð70 Bacci 1947 Cabrera 50Ð100 Ballesteros et al. 1993 Corsica 60Ð80 Laborel 1961 Northeastern Mediterranean 70Ð90 Laborel 1961 Aegean Islands 90Ð110 Laborel 1961 Siculo-Tunisian area 90Ð120 Laborel 1961 Southeastern Mediterranean 100Ð120 Laborel 1961

Structure Coralligenous types: structure and habitats The morphology and inner structure of coralligenous frameworks depends greatly on depth, topog- raphy, and the nature of prevailing algal builders (Laborel 1961). Two main morphologies can be distinguished (Pérès & Picard 1964, Laborel 1987): banks and rims. Banks are flat frameworks with a variable thickness that ranges from 0.5 to several (3Ð4) m. They are mainly built over more or less horizontal substrata, and have a very cavernous structure (numerous holes, Laborel 1987) that often leads to a very typical morphology (it has been compared to Gruyère cheese) (Figure 7A). These banks are sometimes surrounded by sedimentary substrata, and Pérès & Picard (1952) argued that they developed from the coalescence of rhodoliths or maërl (coralligène de plateau). However, it is highly probable that these frameworks have almost always grown upon rocky outcrops (Got & Laubier 1968, Laborel 1987) (Figure 7B). Rims develop in the outer part of marine caves and on vertical cliffs, usually in shallower waters than banks. The thickness of rims is also variable and ranges from 20Ð25 cm to >2 m; thickness increases from shallow to deep waters (Laborel 1987) (Figure 7C). In shallow water the main algal builder is Mesophyllum alternans, which builds flat or slightly rounded banks or rims with a foliaceous structure. As the water deepens, other corallines (Litho- phyllum frondosum, L. cabiochae, Neogoniolithon mamillosum) become important builders. Shal- low water banks are generally covered with populations of green algae Halimeda tuna and Flabellia petiolata (Lithophyllo-Halimedetum tunae), which can be so dense that they hide the calcareous algae. However, at greater depths the density of these erect algae decreases and corallines dominate the community (Rodriguezelletum strafforellii). Holes and cavities within the coralligenous structure always sustain a complex community dominated by suspension feeders (sponges, hydrozoans, anthozoans, bryozoans, serpulids, mol- luscs, tunicates) (Figure 7D). The smallest crevices and interstices of the coralligenous buildup have an extraordinarily rich and diverse vagile endofauna of polychaetes and crustaceans, while many attached or unattached animals cover the main macroalgae and macrofauna, swarm every- where, from the surface to the cavities or inside the main organisms, and thrive in the small patches of sediment retained by the framework.

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Figure 7 (See also Colour Figure 7 in the insert following page 276.) Types and habitats in coralligenous outcrops. (A) small coralligenous accretion apparently developed from the coalescence of rhodoliths (Tossa de Mar, NE Spain, 40 m depth); (B) coralligenous bank grown upon a rocky outcrop (Tossa de Mar, NE Spain, 25 m depth); (C) community dominated by suspension feeders in a coralligenous cavity (Cabrera, Balearic Islands, 52 m depth); (D) coralligenous rim on a vertical cliff (Gargalo, Corsica, 48 m depth). (Photos by the author.)

According to Hong (1982) four different categories of invertebrates can be distinguished with respect to their position and ecological significance in the coralligenous structure:

1. Fauna contributing to buildup, which help develop and consolidate the framework created by the calcareous algae. Several bryozoans, polychaetes (serpulids), corals and sponges constitute this category. They include 24% of the total species number. 2. Cryptofauna colonising the small holes and crevices of the coralligenous structure. They represent around 7% of the species, including different molluscs, crustaceans and polychaetes. 3. Epifauna (living over the concretions) and endofauna (living inside the sediments retained by the buildup), which represent a great number of species (nearly 67%). 4. Eroding species, accounting for only around 1%.

Algal builders Coralline algae are the main coralligenous builders (Laborel 1961, Laubier 1966, Sartoretto 1996). The taxonomy of this group of algae is very difficult to determine and the nomenclature of the

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Figure 8 (See also Colour Figure 8 in the insert.) Main red algal building species in coralligenous frameworks. (A) Mesophyllum alternans; (B) Lithophyllum frondosum; (C) Lithophyllum cabiochae; (D) Neogoniolithon mamillosum; (E) Peyssonnelia rosa-marina. (Photos by the author.)

species is constantly changing. Due to their great importance in the construction of coralligenous frameworks several issues regarding the taxonomic status and current nomenclature of the main species are considered here. The main algal building species, according to Sartoretto (1996) and several other authors (e.g., Feldmann 1937, Pérès & Picard 1964, Boudouresque 1970, Hong 1980, Ballesteros 1991b), has repeatedly been identified as Mesophyllum lichenoides (Ellis) Lemoine. However, Cabioch & Mendoza (1998) reported the most common species of the genus Mesophyllum growing in coral- ligenous assemblages to be a different species and named it Mesophyllum alternans (Foslie) Cabioch & Mendoza (Figure 8A). Although present in the Mediterranean Sea, M. lichenoides does not seem to contribute to coralligenous buildup (Cabioch & Mendoza 1998). Therefore, it is likely that some or most of the reports of M. lichenoides as a coralligenous builder actually refer to M. alternans (Cabioch & Mendoza, 1998) (Figure 8A). Pseudolithophyllum expansum (sensu Lemoine) has been identified by most authors as being the second most common coralline alga in coralligenous concretions. However, Boudouresque & Verlaque (1978) identified another species, similar to P. expansum, and described it as P. cabiochae. Later, studies by Woelkerling (1983), Athanasiadis (1987), Woerkerling et al. (1993) and Furnari

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et al. (1996) shed some light (but also added further confusion) regarding the name to be applied to the alga called P. expansum and/or P. cabiochae by Mediterranean phycologists and marine biologists. The last review by Athanasiadis (1999a) suggested that Pseudolithophyllum should not be regarded as a different genus to Lithophyllum and that the two species growing in coralligenous communities should be named Lithophyllum stictaeforme (Areschoug) Hauck [= Lithophyllum frondosum (Dufour) Furnari, Cormaci & Alongi; = Pseudolithophyllum expansum (Philippi) Lemoine; = Lithophyllum expansum sensu Lemoine] (Figure 8B) and Lithophyllum cabiochae (Boudouresque & Verlaque) Athanasiadis (Figure 8C). However, according to Marc Verlaque (personal communication), L. stictaeforme and L. frondosum are not synonyms and the species usually reported as Pseudolithophyllum expansum by Mediterranean phycologists should be named Lithophyllum frondosum. Moreover, Woelkerling (1983) recognised the lectotype of Lithophyllum expansum Philippi (non Lemoine) as a Mesophyllum and considered it to be a heterotypic synonym of M. lichenoides. However, a recent study by Cabioch & Mendoza (2003) showed that the lectotype of Lithophyllum expansum Philippi is specifically different from Mesophyllum lichenoides, M. alternans and other Mediterranean species of this genus. They named it Mesophyllum expansum (Philippi) Cabioch and Mendoza and it corresponds to the taxa usually identified as Mesophyllum lichenoides var. agariciformis (Pallas) Harvey by Mediterranean phycologists. As a result of all this confusion it is not possible to determine the extent to which M. expansum contributes to coralligenous buildup, although it is likely to make a significant contribution, at least in some places. Another species, Mesophyllum macroblastum (Foslie) Adey, has been reported for the coralligenous frameworks in Corsica (Cabioch & Mendoza 2003), and a fifth species (Mesophyllum macedonis Athanasiadis) (Athanasiadis 1999b) may also be present in the coralligenous frameworks of the Aegean Sea. According to Marc Verlaque (personal communication), three species of the genus Mesophyllum coexist in the coralligenous communities off Marseille (M. alternans, M. expansum, M. macroblas- tum), suggesting a much greater biodiversity of coralligenous coralline algae than expected. The alga identified by Feldmann (1937) as Lithophyllum hauckii (Rothpletz) Lemoine, a very common coralline in the coralligenous buildups of the Banyuls region, should be named Neogoni- olithon mamillosum (Hauck) Setchell & Mason (Hamel & Lemoine 1953, Bressan & Babbini- Benussi 1996) [= Spongites mamillosa (Hauck) Ballesteros] (Figure 8D). Although not a coralline alga, it should also be pointed out that authors prior to 1975 identified the calcareous Peyssonnelia growing in coralligenous communities as being Peyssonnelia polymor- pha (Zanardini) Schmitz. Boudouresque & Denizot (1975) described a similar species, Peyssonnelia rosa-marina (Figure 8E), that is more common than P. polymorpha and which also contributes to coralligenous frameworks. Therefore, reports of P. polymorpha prior to the description of P. rosa marina should probably be regarded as referring to this latter species or to both entities. Feldmann (1937) identified the four main calcareous algae responsible for the coralligenous frameworks in the region of Banyuls: Lithophyllum frondosum (as Pseudolithophyllum expansum), Neogoniolithon mamillosum (as Lithophyllum hauckii), Mesophyllum alternans (as M. lichenoides) and Peyssonnelia rosa-marina f. saxicola (as P. polymorpha). The same species have also been reported for coralligenous frameworks studied in several areas close to the Gulf of Lions (e.g., Boudouresque 1973, Ballesteros 1992). It seems that these species are almost always the same, with the possible exception of Lithophyllum frondosum which seems to be replaced by L. cabiochae in several areas of the Mediterranean that are warmer than the Gulf of Lions (e.g., Corsica, Balearic Islands, the eastern Mediterranean). Hong (1980) reports three species as being the main coralligenous builders in the region of Marseilles: Lithophyllum cabiochae, Mesophyllum alternans (?) and Neogoniolithon mamillosum. Peyssonnelia rosa-marina is also very abundant. Other calcareous species contributing to buildup are Archaeolithothamnion mediterraneum, Lithothamnion sonderi (?) and Peyssonnelia polymorpha.

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According to Sartoretto et al. (1996), Mesophyllum alternans (as M. lichenoides) is the main algal building species for both ancient and recent coralligenous constructions in the northwestern Med- iterranean. Mesophyllum alternans is a highly tolerant species in terms of light, temperature and hydrodynamism, and is currently the dominant species in shallow waters. In some areas, Peysson- nelia rosa-marina and P. polymorpha may also be the dominant species, and form a very cavernous, highly bioeroded coralligenous framework. In deep waters Lithophyllum cabiochae is the main calcareous alga in the region of Marseilles and Corsica, but its cover can vary from one geographical area to another. For example, the encrusting algal cover in deep-water coralligenous frameworks in Marseilles is limited to a few isolated small living thalli that seem insufficient to allow current renewal of the coralligenous construction. In contrast, these deep frameworks are luxuriant in Corsica, as evidenced by the accumulation of living thalli of L. cabiochae. The identification of the species present in the algal framework of coralligenous blocks from 7700 years ago to the present has shown that no species changes have occurred (Sartoretto et al. 1996). The study by Sartoretto et al. (1996) in the Marseilles region and Corsica identified five Corallinaceae and one Peyssonneliaceae: the nongeniculate corallines Mesophyllum alternans (as M. lichenoides), Lithophyllum sp. (as Titanoderma sp., probably Lithophyllum pustulatum v. con- finis), Lithophyllum cabiochae-frondosum (discrimination between L. cabiochae and L. frondosum is uncertain in fossil material), Lithothamnion sp., the geniculate coralline alga Amphiroa verru- culosa, and, finally, Peyssonnelia sp. Mesophyllum alternans is also the main algal builder in the coralligenous frameworks of the Mediterranean Pyrenees (Bosence, 1985), along with Lithophyllum and Titanoderma (quoted as Pseudolithophyllum and Tenarea in Bosence’s paper). Peyssonnelia polymorpha and P. rosa-marina f. saxicola may also be abundant in the coralligenous frameworks of the Mediterranean Pyrenees, the northeast coast of Spain, and the Balearic Islands (Bosence 1985, Ballesteros 1992, Ballesteros et al. 1993). However, even if Peyssonnelia is abundant as a living encrusting alga, it is almost completely absent from the fossil record (Bosence 1985, Sartoretto 1996). Carbonate content of the Peyssonnelia species is lower than the average carbonate content in corallines (Laubier 1966, Ballesteros 1992), and calcification in the form of aragonite rather than calcite prevents a good fossilization of these species (James et al. 1988). However, these and other species of Peyssonnelia usually have a basal layer of aragonite that may contribute to the consolidation of coralligenous frameworks when mixed with the physico-chemical precipitations

of CaCO3 (Sartoretto 1996).

Animal builders Coralligenous animal builders have been studied in the Marseilles region (Hong 1980) where 124 species contribute to the frameworks, and account for around 19% of the total number of species reported. The most abundant animal group are the bryozoans, accounting for 62% of species, followed by the serpulid polychaetes with 23.4%. Minor contributors are the cnidarians (4%), molluscs (4%), sponges (4%), crustaceans (1.6%) and foraminiferans (0.8%). However, Laborel (1987) considers the foraminiferan Miniacina miniacea (Figure 9A) to be the most important animal builder. Hong (1980) distinguished three different types of animal builders: those contributing directly to the framework, and which are relatively large; those with a reduced builder activity due to their small size; and those which agglomerate carbonate particles. The first group includes the bryozoans Schizomavella spp., Onychocella marioni, Cribilaria radiata, Pentapora fascialis, Enthalophoroecia deflexa, Celleporina caminata, Myriapora truncata, Brodiella armata and Turbi- cellepora coronopus (Figures 9B,C), several serpulids (Serpula vermicularis, S. concharum, Spiro- branchus polytrema) (Figure 9D), the molluscs Vermetus sp., Serpulorbis arenarius and Clavagella melitensis, and the scleractinians Hoplangia durotrix, Leptopsammia pruvoti, Caryophyllia inornata and C. smithii (Figure 9E). Among the second group, Hong (1980) reports some small bryozoans

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Figure 9 (See also Colour Figure 9 in the insert.) Some animal building species in coralligenous frameworks. (A) Miniacina miniacea; (B) Pentapora fascialis; (C) Myriapora truncata; (D) Serpula vermicularis; (E) Leptopsammia pruvoti. (Photos by the author.)

such as Crassimarginatella maderensis and Mollia patellaria, serpulids like Hydroides spp., Filogranula spp., and Spirorbis spp., the cirripedes Verruca strömia and Balanus perforatus, and the foraminiferan Miniacina miniacea. In terms of the ‘agglomerative’ animals, he reports sponges such as Geodia spp., Spongia virgultosa and Faciospongia cavernosa, the bryozoans Beania spp., and the alcyonarian Epizoanthus arenaceus.

Bioeroders Feldmann (1937) described the abundance of several organisms that erode calcareous concretions, in particular the excavating sponge Cliona viridis (Figure 10A), the bivalve Lithophaga lithophaga and several annelids. Hong (1980) listed 11 bioeroders in the coralligenous communities of Marseilles: four species of sponges of the genus Cliona, three species of molluscs, two species of polychaetes of the genus Polydora and two sipunculids. According to Sartoretto (1996), the organ- isms that erode coralligenous frameworks are similar to those eroding other marine bioherms such

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Figure 10 (See also Colour Figure 10 in the insert.) Bioeroders in coralligenous frameworks. (A) Cliona viridis; (B) Sphaerechinus granularis; (C) Echinus melo; (D) browsing marks of Sphaerechinus granularis over Lithophyllum frondosum. (Photos by the author.)

as the trottoir of Lithophyllum byssoides or the coral reefs. Three types of eroding organisms can be distinguished: browsers, microborers and macroborers. The only browsers in the coralligenous concretions are sea urchins (Laubier 1966), because the only important Mediterranean fish grazing on algae (Sarpa salpa) do not usually thrive in coralligenous communities. Sphaerechinus granularis (Figure 10B,D) is an important biological agent that substantially erodes coralligenous concretions, although local variations in sea urchin abundance and individual size greatly influence the amount of calcium carbonate eroded annually. Another sea urchin commonly found in coralligenous communities is Echinus melo (Figure 10C). The proportion of calcareous algae in its digestive content ranges from 18Ð50% of the total (Sartoretto 1996) and it preys mainly on sponges, bryozoans and serpulid polychaetes. Given the low densities of this sea urchin in coralligenous communities (1Ð3 individuals in 25 m2), Sartoretto (1996) concludes that the bioerosional role of E. melo is very limited. Microborers include blue-green algae (cyanobacteria), green algae and fungi (Hong 1980). Three green algae (Ostreobium quekettii, Phaeophila sp. and Eugomontea sp.) and four cyanobac- teria (Plectonema tenebrans, Mastigocoleus testarum, Hyella caespitosa and Calothrix sp.), together with some unidentified fungi, seem to be the main microborers in coralligenous communities. Diversity is higher in shallow waters, whereas, according to colonisation studies conducted by Sartoretto (1998), it is restricted to only one species (Ostreobium) in deep waters (>60 m). Macroborers comprise molluscs (Lithophaga lithophaga, Gastrochaena dubia, Petricola litho- phaga, Hyatella arctica), sipunculids (Aspidosiphon mülleri, Phascolosoma granulatum), polycha- etes (Dipolydora spp., Dodecaceria concharum) and several excavating sponges (Sartoretto 1996, Martin & Britayev 1998). Among perforating sponges commonly found in coralligenous commu- nities, some of them excavate mainly in Corallium rubrum and other calcareous cnidarians (Aka labyrinthica, Scantilletta levispira, Dotona pulchella spp. mediterranea, Cliona janitrix), whereas others, such as Pione vastifica, Cliona celata, C. amplicavata, C. schmidtii and C. viridis can be

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found in a wide range of calcareous substrata (coralline algae, bivalves, madreporids, etc.) (Rosell & Uriz 2002). Cliona viridis is the most powerful destructive sponge of calcareous substrata (Rosell et al. 1999), and is the most abundant excavating sponge in coralligenous communities (Uriz et al. 1992a). The encrusting sponges and the Sipunculida become more abundant in polluted corallig- enous environments (Hong 1983).

Assemblages The final result of the builders and eroders of coralligenous concretions is a very complex structure, in which several microhabitats can be distinguished (Figure 11). Environmental factors (e.g., light, water movement and sedimentation rates) can vary by one to two orders of magnitude in parts of the same concretion situated as close as one metre from each other. This great environmental heterogeneity allows several different assemblages to coexist in a reduced space. For practical purposes those situated in open waters (from horizontal to almost vertical surfaces) are distinguished here from those situated in overhangs and cavities. The assemblages of macroborers are not discussed because the only available data have already been commented on, nor are the assemblages thriving in the patches of sediment between or inside coralligenous frameworks because there are no quantitative data on them. Algae, both encrusting corallines and green algae, usually dominate in horizontal to subhorizontal surfaces (Figure 12), although their abundance decreases with depth or in dim light. Phycologists have distinguished two main communities according to the light levels reaching coralligenous frameworks. In shallower waters Mesophyllum alternans usually dominates in the basal layer and Halimeda tuna in the upper stratum, with an important coverage of other algae (Peyssonnelia spp., Flabellia petiolata) (Figure 13A). This plant association has received the name of Lithophyllo- Halimedetum tunae, and has been described in detail by Ballesteros (1991b). Algal biomass ranges between 1200 and 2100 g dry weight (dw) mÐ2, while percent cover ranges from 180Ð400%. The number of species is very high (average of 76 species in 1024 cm2) and average diversity is 2.5 bits indÐ1. Its bathymetric distribution ranges from a depth of 12Ð15 m to 30Ð35 m in the Gulf of Lions, but it can reach depths below 50 m in the clear waters of seamounts and insular territories of the western and eastern Mediterranean. This association develops at irradiances ranging from around

Figure 11 (See also Colour Figure 11 in the insert.) Diagrammatic section of a coralligenous bank, showing the high small-scale environmental heterogeneity and the different microhabitats. (Drawing by J. Corbera.)

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Figure 12 (A) Drawing of a coralligenous concretion dominated by algae in the Medes Islands (NE Spain).

2.3Ð0.3 W mÐ2, which correspond, respectively, to 3 and 0.4% of the surface irradiance. Other quantified species lists are described in Marino et al. (1998). In deeper waters or lower irradiances the density of Halimeda tuna decreases and other calcareous algae become dominant (Lithophyllum frondosum, Neogoniolithon mamillosum, Peys- sonnelia rosa-marina) (Figure 14). Other common algae are members of the family Delesseriaceae

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Figure 12 (continued) (B) Key to major species, on the left from top to bottom: Alcyonium acaule16, Crambe crambe on Spondylus gaederopus28, Cystodites dellechiajei31, Myriapora truncata23, Microcosmus sabatieri33, Hemimycale columella9, Sertularella ellisi13, Ophiothrix fragilis30, amid Halimeda tuna (a close up is shown at bottom left with, on it4, Titanoderma sp.6, Halecium halecinum14, Campanularia sp.15, Aetea truncata24, Watersipora subovoidea25 and Polycera quadrilineata26 with spawn mass27 below). At the centre and to the right, from top to bottom, and in addition to the above- mentioned species: Eunicella singularis17, Codium bursa1, Codium vermilara5, Cliona viridis10, Pentapora fascialis22, Salmacina dysteri20, Scorpaena porcus34, Sabella sp.21, Parazoanthus axinellae18, Peyssonnelia rubra2, Oscarella lobularis7, Ircinia variabilis8, Caryophyllia sp.19, Palaemon serratus29, Conger conger35, Botryllus schlosseri32, Agelas oroides12, Crambe crambe11 and Sciaena umbra36, all amid Flabellia petiolata3. (Drawing by M. Zabala in Els Sistemes Naturals de les Illes Medes, Ros et al., 1984. With permission from M. Zabala and J. Ros.)

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Figure 13 (See also Colour Figure 13 in the insert.) Different assemblages of algal-dominated coralligenous banks and rims; (A) with Halimeda tuna and Mesophyllum alternans (Tossa de Mar, NE Spain, 28 m depth); (B) with Lithophyllum frondosum (Tossa de Mar, NE Spain, 40 m depth); (C) with Peyssonnelia rosa-marina, Mesophyllum alternans, Palmophyllum crassum and Peyssonnelia squamaria (Scandola, Corsica, 50 m depth); (D) detail of C. (Photos by the author.)

and other laminar red algae (Kallymenia, Fauchea, Sebdenia, Rhodophyllis, Predaea), as well as the encrusting green alga Palmophyllum crassum. These assemblages correspond to the Rodrigu- ezelletum strafforellii of Augier & Boudouresque (1975), which may be identical to the algal assemblage described by Feldmann (1937) for coralligenous concretions from the Mediterranean Pyrenees (Figures 13B,C,D). Quantified species lists can be found in Boudouresque (1973), Augier & Boudouresque (1975), Ballesteros (1992) and Marino et al. (1998). Algal biomass averages 1600 g mÐ2 and percent cover 122%, mostly corresponding to encrusting algae and, around 90%, corre- sponding to corallines; the number of species is low (38 species in 1600 cm2 or lower) (Ballesteros 1992). Animal assemblages of these two plant associations can differ greatly from one to the other, as well as between sites and geographical areas. The abundance of suspension feeders mainly depends on average current intensity and availability of food (plankton, POC, DOC). In the richest zones (e.g., Gulf of Lions, Marseilles area) gorgonians can dominate the community (Figure 15A,B), but in very oligotrophic waters (e.g., Balearic Islands, eastern Mediterranean), sponges, bryozoans and small hexacorals are the dominant suspension feeders (Figure 15C). The only available quan- tified biomass data of invertebrate assemblages are those of True (1970) gathered from the Marseilles area, and those results are summarized below. True (1970) studied an assemblage dominated by Eunicella cavolinii. He reports a basal layer of encrusting algae accompanied by erect algae (total biomass of 163 g dw mÐ2). E. cavolinii is the most abundant species (up to 304 g dw mÐ2), followed by the bryozoans Pentapora fascialis (280.1 g dw mÐ2), Turbicellepora avicularis (49.1 g dw mÐ2), Celleporina caminata (22.3 g dw mÐ2) and Myriapora truncata (19.9 g dw mÐ2). Other less abundant species include unidentified Serpul- idae, anthozoans Parerythropodium coralloides, Alcyonium acaule, Leptopsammia pruvoti and

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Figure 14 (See also Colour Figure 14 in the insert.) (A) Drawing of a deep-water, animal-dominated, coralligenous assemblage in the Medes Islands (NE Spain).

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Figure 14 (continued) (See also Colour Figure 14 in the insert.) (B) Key to major species, left from top to bottom: Paramuricea clavata6, (and on it Halecium halecinum12, Pteria hirundo22), Aglaophenia septifera14, Cliona viridis7, Alcyonium acaule17, Acanthella acuta11, Lithophyllum frondosum1, Agelas oroides6, Palinurus elephas24, Parazoanthus axinellae19, Spirastrella cunctatrix9, Chondrosia reniformis5, Petrosia ficiformis4 (and on it Smittina cervicornis27 and Discodoris atromaculata23), Serpula vermicularis21, Caryophyllia inornata20, Halocynthia papillosa28, Clathrina coriacea3, Corallium rubrum18 and Chromis chromis.32 Right, from top to bottom (excluding the above-mentioned species): Anthias anthias31, Eunicella singularis15, Diplodus sargus29, Codium bursa8, Epinephelus marginatus30, Phyllangia mouchezii26, Galathea strigosa25, Synthecium evansi13, Dysidea avara10. (Drawing by M. Zabala & J. Corbera.)

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Figure 15 (See also Colour Figure 15 in the insert.) Different assemblages of animal-dominated coralligenous banks and rims; (A) with gorgonians Paramuricea clavata and Eunicella cavolinii but also green algae Halimeda tuna and Flabellia petiolata (Gargalo, Corsica, 45 m depth); (B) with Paramuricea clavata and encrusting sponges in deep waters (Cabrera, Balearic Islands, 65 m depth); (C) with sponges, bryozoans and anthozoans (Cabrera, Balearic Islands, 50 m depth); (D) overhangs with Corallium rubrum (Palazzu, Corsica, 35 m depth). (Photos by the author.)

Caryophyllia smithii, tunicates Microcosmus polymorphus and Halocynthia papillosa, foraminiferan Miniacina miniacea, sponges Chondrosia reniformis and Axinella damicornis and other bryozoans (Adeonella calveti, Beania hirtissima, Sertella spp., Schizomavella spp. and Cellaria salicornio- ides). The number of collected invertebrate species amounted to 146 in 7500 cm2, with a total weight of invertebrates close to 1563 g dw mÐ2. The main biomass corresponded to the phylum Bryozoa, closely followed by Cnidaria, and, with much lower values, Annelida, Porifera, Chordata (tunicates) and Mollusca. Another assemblage studied by True (1970) is that dominated by Paramuricea clavata. Popu- lations of P. clavata are abundant in steep rocky walls, but they also grow in horizontal to subhorizontal surfaces if light levels are very low. The basal layer of the community can be mainly occupied by algae (usually attributable to Rodriguezelletum strafforellii association) or by other suspension feeders (sponges and bryozoans). The lists of True (1970) do not report any algae. Paramuricea clavata has a total biomass of 746 g dw mÐ2, followed by the cnidarians Caryophyllia smithii (326.3 g dw mÐ2) and Hoplangia durotrix (188.1 g dw mÐ2), the bryozoan Celleporina caminata (119.6 g dw mÐ2), the anthozoan Leptopsammia pruvoti (54.9 g dw mÐ2), the bryozoans Adeonella calveti (32.8 g dw mÐ2) and Turbicellepora avicularis (31.4 g dw mÐ2), and red coral (Corallium rubrum, 16.9 g dw mÐ2). Other less abundant species include unidentified Serpulidae, sponges Ircinia variabilis (fasciculata in True, 1970), Spongia officinalis, Sarcotragus spinosula, Cacospongia scalaris, Petrosia ficiformis, Aplysina cavernicola, Erylus euastrum and Agelas oroi- des, the bryozoan Sertella septentrionalis, the alcyonarian Parazoanthus axinellae, molluscs Pteria hirundo, Serpulorbis arenarius, Lithophaga lithophaga and Anomia ephippium, and tunicates Microcosmus polymorphus and Polycarpa pomaria. The number of collected invertebrate species

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amounts to 111 in 7500 cm2, with a total weight of 3175 g dw mÐ2. The main biomass corresponds to the phylum Cnidaria, followed by Annelida, Bryozoa, Porifera, Mollusca and Chordata. Gili & Ballesteros (1991) described the species composition and abundance of the cnidarian populations in coralligenous concretions around the Medes Islands that are dominated by the gorgonian Paramuricea clavata. Total cnidarian biomass amounted to 430 g dw mÐ2, with 13 species of hydrozoans and 9 species of anthozoans found in an area of 5202 cm2. Species contributing the most to the total biomass of the taxocoenosis were the anthozoans Paramuricea clavata, Leptop- sammia pruvoti, Parazoanthus axinellae, Caryophyllia inornata, C. smithii, Alcyonium acaule and Parerythropodium coralloides, the hydrozoans Sertularella gaudichaudii and Halecium tenellum also being abundant. Overhangs and big cavities of coralligenous assemblages have a different species composition to that found in open waters (Figure 15D). Algae are usually completely absent because light is very reduced. However, some thalli of encrusting corallines, Peyssonnelia spp. and Palmophyllum crassum, can occasionally be found. There are no quantified species lists for this kind of habitat reported in the literature except for those of True (1970), which, in fact, do not come from a coralligenous buildup but from a semidark zone dominated by red coral in a cave (Grotte de l’Île Plane). This assemblage is worth describing as it is very similar to those that develop in the overhangs of coralligenous constructions in the northwestern Mediterranean, or in coralligenous communities situated in very deep waters. The assemblage of red coral described by True (1970) is dominated by the cnidarians Corallium rubrum (2002 g dw mÐ2), Caryophyllia smithii (303 g dw mÐ2), Hoplangia durotrix (54.1 g dw mÐ2) and Leptopsammia pruvoti (52.4 g dw mÐ2), the sponges Petrosia ficiformis (241.5 g dw mÐ2) and Aplysina cavernicola (27.9 g dw mÐ2), the bryozoan Celleporina caminata (100.5 g dw mÐ2), and unidentified Serpulidae (232.4 g dw mÐ2). Other abundant species are the sponges Ircinia variabilis, Spongia officinalis, Aaptos aaptos and Ircinia oros, the molluscs Chama gryphoides and Anomia ephippium, and several unidentified bryozoans. The total number of identified invertebrate species is 63 in 7500 cm2, with a total biomass of 3817 g dw mÐ2. The dominant phylum is largely the Cnidaria, although Porifera, Annelida and Bryozoa are also abundant. It should be remembered that most of the invertebrate data presented in this chapter, if repre- sentative at all, reflect the biomass and species composition of several assemblages of coralligenous buildups from the Gulf of Lions, which are different to those reported from other sites of the western Mediterranean (e.g., Balearic Islands; Ballesteros et al. 1993) or the eastern Mediterranean (Pérès & Picard 1958, Laborel 1960). Therefore, these data cannot be extrapolated to the whole Mediterranean.

Biodiversity Coralligenous communities constitute the second most important ‘hot spot’ of species diversity in the Mediterranean, after the Posidonia oceanica meadows (Boudouresque 2004a). However, there appear to be no previous estimates of the number of species that thrive in these coralligenous assemblages. Furthermore, due to their rich fauna (Laubier 1966), complex structure (Pérès & Picard 1964, Ros et al. 1985), and the paucity of studies dealing with coralligenous biodiversity, they probably harbour more species than any other Mediterranean community. In fact, coralligenous assemblages are one of the preferred diving spots for tourists due to the great diversity of organisms (Harmelin 1993). Divers are astonished by the high number of species belonging to taxonomic groups as diverse as sponges, gorgonians, molluscs, bryozoans, tunicates, crustaceans or fishes. Moreover, there are innumerable organisms living in these coralligenous communities that cannot be observed by diving, nor without a careful sorting of samples. For example, in a sample of 370 g dw of Mesophyllum from a small coralligenous concretion in the south of Spain, García-Raso

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(1988) found 903 specimens of crustaceans, molluscs and polychaetes; other organisms from other groups (pycnogonids, nematodes, echinoderms, sipunculids, sponges, tunicates, small fishes, such as Gobiidae and Blenniidae, as well as hydrozoans and bryozoans) were also abundant, although not quantified. Laubier (1966) was the first author to emphasize the great biodiversity of coralligenous com- munities and listed 544 invertebrates from coralligenous assemblages in the region of Banyuls. Later, in an exhaustive survey of coralligenous communities around Marseilles, Hong (1980) listed a total of 682 species, while several authors (in Ros et al. 1984) report 497 species of invertebrates in the coralligenous assemblages of the Medes Islands. Estimates of the species richness found in coralligenous communities give a very conservative number of 1241 invertebrates (Table 2). Boudouresque (1973) has estimated that at least 315 species of macroalgae can thrive in Mediter- ranean sciaphilic communities (the coralligenous type being the most widespread). Finally, there are no estimates of the number of fishes that can be found in coralligenous communities, due to the high mobility of most species of this group, but estimates based on available literature regarding the biology of Mediterranean fishes (e.g., Whitehead et al. 1984Ð1986, Corbera et al. 1996, Mayol et al. 2000) range between 110 and 125 species. It is very difficult to mention all the species found to date in coralligenous communities, as the existing taxonomic literature is huge and contains many synonyms; this makes it impossible for a nonspecialist in most of the groups to come up with an accurate number of reported species. Nevertheless, an attempt is made at a first, and very conservative, estimate of the total number of species, which amounts to some 1,666 (Table 2). A first step toward increased knowledge of the biodiversity present in coralligenous communities would be to obtain a more accurate estimate of which species have been found and their number. The next section describes the main findings reported for each taxonomic group.

Taxonomic groups Algae

At least 315 species of macroalgae thrive in deep-water Mediterranean sciaphilic communities (Boudouresque 1973), and most of them are found in coralligenous concretions. The algal assem- blages found here show high biodiversity, with an average of 40 algal species in 600 cm2. Boudouresque (1973) defined the ecological group of algae characteristic of coralligenous concretions (CC or Rodriguezellikon), which (Boudouresque, 1985) comprises 28 species (e.g., Rodriguezella spp., Aeodes marginata, Fauchea repens, Chondrymenia lobata, Gulsonia nodulosa, Polysiphonia elongata, Neogoniolithon mamillosum). However, coralligenous communities are never dominated by this group of species, but rather by other species with a more depth-related widespread distribution, examples being the encrusting corallines Mesophyllum alternans, Litho- phyllum frondosum, and L. cabiochae, the green algae Palmophyllum crassum, Flabellia petiolata, Halimeda tuna and Valonia macrophysa, some brown algae such as Dictyota dichotoma, Dictyop- teris polypodioides, Spatoglossum solierii, Zonaria tournefortii, Halopteris filicina, Phyllariopsis brevipes, Zanardinia prototypus and Laminaria rodriguezii, and a large number of red algae (several species of Peyssonnelia, Kallymenia, Halymenia, Sebdenia, Predaea, Eupogodon, Myriogramme, Neurocaulon foliosum, Acrodiscus vidovichii, Osmundaria volubilis, Phyllophora crispa, Rhodymenia ardissonei, Acrosorium venulosum, Rhodophyllis divaricata, Hypoglossum hypoglossoides, Polysi- phonia banyulensis, Plocamium cartilagineum, Sphaerococcus coronopifolius, Erythroglossum san- drianum, and Aglaothamnion tripinnatum) (Boudouresque 1973, 1985, Ballesteros 1992, 1993). The algal component of coralligenous communities largely consists of Mediterranean endemics, which quantitatively represent between 33 and 48% of the total flora (Boudouresque 1985).

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Table 2 Approximate number of species reported from coralligenous communities

Group Totals References Algae 315 Boudouresque 1973 Protozoans 61 Laubier 1966, Hong 1980 Sponges 142 Laubier 1966, Hong 1980, Ros et al. 1984, Ballesteros et al. 1993, Ballesteros & Tomas 1999, Rosell & Uriz 2002 Hydrozoans 55 Laubier 1966, Ros et al. 1984, Ballesteros et al. 1993, Rosell & Uriz 2002 Anthozoans 43 Laubier 1966, Ros et al. 1984, Ballesteros et al. 1993, Ballesteros & Tomas 1999, Ballesteros, unpublished data Scyphozoans 1 Laubier 1966, Hong 1980 Turbellarians 3 Laubier 1966, Hong 1980 Nemerteans 12 Laubier 1966 Polychaetes 191 Martin 1987 Sipunculids 3 Laubier 1966, Hong 1980 Echiurids 2 Laubier 1966 Chitons 7 Hong 1980 Prosobranchs 61 Hong 1980 Opisthobranchs 33 Hong 1980 Bivalves 41 Hong 1980 Cephalopods 3 Ballesteros & Tomas 1999 Mites 6 Laubier 1966 Pycnogonids 15 Hong 1980 Copepods 54 Laubier 1966 Ostracods 10 Laubier 1966 Cirripedes 3 Laubier 1966, Hong 1980 Phyllocarids 1 Hong 1980 Mysids 7 Hong 1980 Cumaceans 3 Laubier 1966, Hong 1980 Tanaidaceans 2 Laubier 1966, Hong 1980 Isopods 14 Laubier 1966, Hong 1980 Amphipods 100 Bellan-Santini 1998 Decapods 56 García-Raso 1988, 1989 Brachiopods 8 Logan 1979 Pterobranchs 1 Laubier 1966 Bryozoans 171 Zabala 1986 Crinoids 2 Tortonese 1965 Ophiuroids 17 Laubier 1966, Tortonese 1965 Echinoids 14 Tortonese 1965, Laubier 1966, Hong 1980, Ros et al. 1984, Munar 1993, Ballesteros et al. 1993, Ballesteros & Tomas 1999 Asteroids 8 Tortonese 1965, Laubier 1966, Munar 1993 Holothurioids 9 Tortonese 1965, Laubier 1966, Hong 1980, Ros et al. 1984, Munar 1993, Ballesteros et al. 1993, Ballesteros & Tomas 1999 Tunicates 82 Ramos 1991 Fishes 110 Whitehead et al. 1984Ð1986, Ballesteros, unpublished data

Coralligenous communities are rich in algal species, although this richness is lower than that found in photophilic or moderately sciaphilic communities (Ballesteros 1992). Ballesteros (1991b) reports 90 species of macroalgae from the coralligenous assemblages of Tossa de Mar, where Mesophyllum alternans and Halimeda tuna dominate, but only 38 in the coralligenous communities from a deep water site (Ballesteros 1992). Piazzi et al. (2004) found small differences between algal assemblages of coralligenous habitats along the coast of Tuscany (Italy). However, algal

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populations in coralligenous habitats differ greatly on geographical scales across the whole Med- iterranean (Boudouresque 1973) and this is the main reason why, even if the species diversity at one site is rather constant, the overall algal richness of coralligenous habitats — on a Mediterranean- wide scale and covering all depths where they are present — can be huge.

Protozoa Fifty-four species of Foraminifera are listed by Hong (1980) in the checklist of species from the coralligenous communities of Marseilles, although none of these species seems to be characteristic of coralligenous habitats. Miniacina miniacea is the most abundant species, and other common species include Massilina secans, Planorbulina mediterranensis, Elphidium crispum and Trilocu- lina rotunda. Laubier (1966) reports six species of Folliculinidae living as epibionts of bryozoans.

Porifera Coralligenous communities are very rich in sponges, which grow mainly in the more sciaphilic environments but also in more exposed areas. There are also some species (Clionidae) that are active bioeroders and which excavate the coralline framework. The number of species reported from different well-studied areas is 26 species from Banyuls (Laubier 1966), 78 species from Marseilles (Hong 1980), 48 species from the Medes Islands (Bibiloni et al. 1984), 74 species from Cabrera (Ballesteros et al. 1993), and 24 species from Tossa (Ballesteros & Tomas 1999). The list of sponges reported in all these studies (along with those of True 1970 and Rosell & Uriz 2002) amounts to 142 different species. According to Hong (1980) the following species are characteristic of coralligenous biocoenoses: Axinella damicornis, Acanthella acuta, Hymedesmia pansa, Agelas oroides, Dictyonella pelligera, Haliclona mediterranea, Spongionella pulchella and Faciospongia cavernosa. Other abundant sponges (Laubier 1966, True 1970, Hong 1980, Bibiloni et al. 1984, Ballesteros et al. 1993, Ballesteros & Tomas 1999) are: Cliona viridis, Clathrina clathrus, Oscarella lobularis, Chondrosia reniformis, Phorbas tenacior, Geodia cydonium, Aaptos aaptos, Pleraplysilla spinifera, Dysidea avara, Terpios fugax, Spongia virgultosa, S. agaricina, S. officinalis, Ircinia variabilis, I. oros, Axinella verrucosa, A. polypoides, Diplastrella bistellata, Petrosia ficiformis, Hexadella racovitzai, Cacospongia scalaris, Dictyonella obtusa, Erylus euastrum, Hippospongia communis, Reniera cratera, R. fulva, R. mucosa, Spirastrella cunctatrix, Spongosorites intricatus and Hemimycale columella. The coralligenous communities from the eastern Mediterranean seem to be very rich in sponges (Pérès & Picard 1958) because they are almost devoid of alcyonarians and gorgonians. The most abundant species have already been cited above. Those of the genus Axinella (A. polypoides, A. damicornis, A. verrucosa), Agelas oroides and Petrosia ficiformis (Pérès & Picard 1958) are particularly common.

Hydrozoa Laubier (1966) reports 16 hydrozoans from the coralligenous communities of Banyuls but none is listed by Hong (1980). Gili et al. (1984) report 44 species of hydrozoans from the coralligenous and precoralligenous communities of the Medes Islands. According to Laubier (1966) and Gili et al. (1984, 1989) some species of hydrozoans are common on deep-water rocky bottoms and coralligenous assemblages, namely Nemertesia antennina, Eudendrium rameum, Filellum serpens, Dynamena disticha, Clytia hemisphaerica, Hebella scandens, Sertularella polyzonias, S. gayi, S. ellisi, S. crassicaulis, Laomedea angulata and Cuspidella humilis. The only detailed study of hydrozoans found on coralligenous assemblages is that of Llobet et al. (1991a), who report 35 species of hydroids living on the thalli of Halimeda tuna in the coralligenous concretions of Tossa de Mar (northwestern Mediterranean). Llobet et al. (1991a)

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classify the most abundant hydrozoans into three categories on the basis of their horizontal zonation on the thalli. The hydroids common on the proximal articles (oldest) are relatively large and present throughout the year (Eudendrium racemosum, E. capillare, Halecium tenellum and Kirchenpaueria echinulata). Those common on the medial articles (Campalecium medusiferum, Halecium pusillum, Hydranthea margarica, Phialella quadrata, Campanularia everta and Filellum serpens) are smaller and often occur in dense monospecific patches. Finally, those common on the distal articles (Campanularia raridentata, Clytia hemisphaerica, Sertularia distans, Sertularella polyzonias and Aglaophenia pluma) are present for only short periods and are highly opportunistic. This zonation seems to reflect interspecific niche selection, enabling successful competition for space with other hydroids, algae and bryozoans.

Anthozoa

Studies by Laubier (1966), True (1970), Hong (1980) and Gili et al. (1984, 1989) report several species of anthozoans from coralligenous habitats (up to 33 in Gili et al. 1984). The commonest species are Parazoanthus axinellae, Leptopsammia pruvoti, Parerythropodium coralloides, Alcyo- nium acaule, Paramuricea clavata, Eunicella singularis, E. cavolinii, Rolandia rosea, Corallium rubrum, Telmatactis elongata, Maasella edwardsii, Monomyces pygmaea, Hoplangia durotrix, Caryophyllia inornata, C. smithii, Clavularia ochracea, Cornularia cornucopiae and Epizoanthus arenaceus. Madracis pharensis is especially abundant in the coralligenous outcrops of the eastern Mediterranean (Laborel 1960).

Scyphozoa

The only species reported (Hong, 1980) is Nausitoë punctata, living inside several massive sponges.

Turbellaria

Laubier (1966) reports three turbellarians from the coralligenous communities of Banyuls, all very rare.

Nemertea

Nemerteans live endolithically in concretions. According to Pruvot (1897) and Laubier (1966), who report up to 12 species in the coralligenous communities of Banyuls, they are rather common. Drepanophorus crassus, Tetrastemma coronatum, Micrura aurantiaca and M. fasciolata are the most abundant.

Nematoda

Nematodes are the most abundant microscopic metazoans in marine sediments and are present in the sediments retained in coralligenous assemblages, as well as in the endofauna of concretions and the epifauna of algae and sessile invertebrates. However, there are no studies dealing with this group of organisms in coralligenous assemblages.

Polychaeta

Polychaetes are extremely abundant in coralligenous communities. Martin (1987) reported a total of 9195 individuals present in 20 samples of 400 cm2 collected from coralligenous communities dominated by Mesophyllum alternans and Lithophyllum frondosum from the Catalan coast (north- western Mediterranean). This means an average of 460 worms per sample and a density of more than one individual per cm2. He found 191 species, with a dominance of Syllidae (31% of the total). The number of species per sample was very high, ranging between 32 and 71 for macrofauna

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(>0.4 mm) and between 27 and 55 for microfauna (<0.04 mm). Diversity of the samples was also very high, averaging 4.54 bits indÐ1 for macrofauna and 4.34 bits indÐ1 for microfauna (Shannon- Weaver index). According to Martin (1987), coralligenous assemblages are a very suitable habitat for polychaetes because the high structural complexity of the concretions allows the coexistence of several species in a reduced space. The first checklist of polychaetes collected from coralligenous communities and studied by a specialist is that of Bellan (1964), who reported 70 species. Laubier (1966) reported 130 species in the polychaete assemblages of two coralligenous stations in the Banyuls region; Lepidasthenia elegans, Kefersteinia cirrata, Xenosyllis scabra and Typosyllis variegata were the most abundant. According to his observations, and those of Bellan (1964), the polychaetes inhabiting coralligenous concretions are mainly ubiquitous species, although he dis- tinguished two main groups: microfauna and macrofauna. Microfauna comprise three ecological groups: psammophilic species (e.g., Xenosyllis scabra, Eurysillis tuberculata, Trypanosyllis coeli- aca), limic species (e.g., Scalibregmatidae, Sclerocheilus minutus), and the strictly endogean spe- cies, which are the most ‘characteristic’ of coralligenous habitats (e.g., Pholoe minuta, Chryso- petalum caecum, Eulalia tripunctata, Sige microcephala, Opisthodonta morena, Syllides longocirrata). Among the macrofauna he distinguished four ecological groups: polychaetes living inside sponges (e.g., Lepidasthenia elegans, Eunice siciliensis, Amphitrite variabilis); species living in small crevices and holes, like most Serpulidae and Terebellidae, as well as Eunice torquata; big vagile polychaetes living over or inside coralligenous holes (e.g., Lepidonotus clava, Harmothoe aerolata, Pontogenia chrysocoma, Trypanosyllis zebra) and, finally, excavating species of the genus Dipolydora and Dodecaceria concharum. Hong (1980) reported a total of 109 species of polychaetes inhabiting the coralligenous com- munities of Marseilles, and distinguished some characteristic species such as Haplosyllis spongi- cola, Trypanosyllis coeliaca, Platynereis coccinea, Eunice torquata, Lumbrinereis coccinea and Potamilla reniformis. According to Martin (1987), who studied polychaete fauna in the corallige- nous communities from the Catalan coast, the most dominant and constant species are Filograna implexa, Spirobranchus polytrema, Polydora caeca, Pomatoceros triqueter, Nereis pelagica, Syllis truncata, S. gerlachi, Haplosyllis spongicola, Serpula concharum, Anaitides muscosa and Dode- caceria concharum. However, the most conspicuous species growing in coralligenous communities are not usually the most abundant, but rather the large and very apparent species of serpulids (True 1970) notably Salmacina dysteri, Serpula vermicularis, S. concharum, Sabella pavonina, S. spal- lanzani, Myxicola aesthetica and Protula spp. (Ballesteros & Tomas 1999).

Sipunculida Always endolithic, the most abundant species of sipunculid is Phascolosoma granulatum, which, along with Aspidosiphon mülleri, is also a very active bioeroder (Sartoretto 1996). Laubier (1966) reports a third species in the coralligenous community of Banyuls: Golfingia minuta.

Echiura Bonellia viridis, very common in coralligenous communities, is an important detritus feeder. Laubier (1966) reports another, extremely rare species from the coralligenous community of Banyuls (Thalassema sp.).

Mollusca Molluscs are extremely abundant in coralligenous communities. Martin et al. (1990) reported a total of 897 individuals in 20 samples of 400 cm2, equivalent to an average of 45 species per sample

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and more than one mollusc per 10 cm2. They report a very high number of species given the reduced area they sampled: 131. The number of species per sample ranged between 5 and 33. Average diversity for all the samples was 3 bits indÐ1 (Shannon-Weaver index). Salas & Hergueta (1986) also reported a very high diversity, with an average of 22.7 species per sample. The number of species reported in studies devoted to the coralligenous communities of a small geographic area are always high: 69 species in Banyuls (Laubier 1966), 142 species in Marseilles (Hong 1980) and 108 species in the Medes Islands (Huelin & Ros 1984). According to these authors, and to Martin et al. (1990), the most common and constant species are the chiton Callochiton achatinus; the prosobranchs Acmaea virginea, Calliostoma zizyphinum, Alvania lineata, A. cancellata, Setia semistriata, S. tenera, Chauvetia minima, C. mamillata, Hinia incrassata, Fusinus pulchellus, F. rostratus, Raphitoma linearis, Clanculus corallinus, Rissoina bruguierei, Triphora perversa, Muricopsis cristatus and Bittium reticulatum; the opisthobranchs Odostomia rissoides, Diaphorodis papillata, Limacia clavigera, Cadlina laevis, Hypselodoris fontandraui, Chromodoris luteorosea, C. purpurea, Dendrodoris grandiflora, Duvaucelia striata, Discodoris atromaculata, Glossodoris gracilis, G. tricolor, Polycera quadrilineata, Flabellina affinis and Dondice banyulensis and the bivalves Arca barbata, Striarca lactea, Musculus costulatus, Kellia suborbicularis, Lithophaga lithophaga, Coralliophaga lithophagella, Anomia ephippium, Pteria hirundo, Chlamys multistriata, Chama gryphoides, Lima lima and Hiatella arctica. Cephalopods are also present in coralligenous communities, although they are usually not reported in lists. Both Octopus vulgaris and Sepia officinalis are regularly present. Loligo vulgaris eggs are frequently seen in late winter and early spring in some coralligenous platforms.

Acari

Mites are always rare in coralligenous communities. Laubier (1966) reports six species from Banyuls.

Pycnogonida

Up to 15 species of pycnogonids occur in the coralligenous communities of Marseilles (Hong 1980). Achelia echinata, Rynchothorax mediterraneus, Tanystylum conirostre and Callipallene spectrum seem to be the most common, although they are always rare. Only one species is reported by Laubier (1966) from Banyuls, and two species by Munilla & De Haro (1984) from the Medes Islands.

Copepoda

The fauna of copepods has been carefully studied by Laubier (1966) in one station from the coralligenous communities of Banyuls. He reports up to 54 species. Ectinostoma dentatum, Har- pacticus littoralis, Tisbe furcata, Thalestris rufoviolescens, Phyllothalestris mysis, Dactylopodia tisboides, Diosaccus tenuicornis, Amphiascus minutus, A. cinctus and Laophonte cornuta are extremely abundant. There are several copepods which live as parasites of different invertebrates: polychaetes, sponges, echinoderms, molluscs, cnidarians and tunicates (Laubier 1966 and references therein).

Ostracoda

Although several species of ostracods are present in coralligenous communities (Laubier 1966, Hong 1980), no study has been devoted to this group. Laubier (1966) reports more than 10 unidentified species in the ‘endogean’ microfauna.

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Cirripedia

The barnacles Balanus perforatus and Verruca strömia, in coralligenous walls and crevices, and Acasta spongites, an endobiont of several sponges (e.g., Dysidea, Ircinia), have been identified in coralligenous communities (Laubier 1966, Hong 1980, Carbonell 1984).

Phyllocarida

Only one species has been recorded in the coralligenous communities of Marseilles (Hong 1980).

Mysidacea

Hong (1980) reports seven mysids from the coralligenous communities of Banyuls.

Cumacea

Three cumaceans are reported from coralligenous communities and are always rare (Laubier 1966, Hong 1980).

Tanaidacea

Tanais cavolini and Leptochelia savignyi are rather common among the ‘endogean’ microfauna of coralligenous frameworks (Laubier 1966, Hong 1980).

Amphipoda

A noteworthy number of amphipods have been sampled in coralligenous communities. Although Laubier (1966) only reports 12 species from the coralligenous communities of Banyuls, a list of 49 species is given by Hong (1980) in Marseilles, and 40 species are reported by Jimeno & Turon (1995) in an extensive survey of the concretions by Mesophyllum alternans along the coast of Catalonia (northwestern Mediterranean). Coralligenous assemblages harbour a certain number of amphipods from photophilic algal communities, together with rheophobic and sciaphilic species, which are linked to the presence of hydroids, sponges and bryozoans. Bellan-Santini (1998) lists 44 species from the coralligenous community (below 35 m depth), to which another 56 species collected from sciaphilic communities with Flabellia petiolata and Halimeda tuna have to be added. Therefore, a total number of 100 species is probably a good estimate of the amphipods thriving in coralligenous communities. According to the available literature, common species include Maera inaequipes, M. grossi- mana, Liljeborgia dellavallei, Leptocheirus bispinosus, Gitana sarsi, Amphilochus picadurus, Colo- mastix pusilla, Iphimedia serratipes and Stenothoe tergestina. In coralligenous communities with some erect algae, the following species are also abundant: Orchomene humilis, Leptocheirus guttatus, Stenothoe dollfusi, Leucothoe venetiarum, Pseudoprotella phasma, Cressa cristata, C. mediterranea, Caprella acanthifera, Corophium sextonae, Dexamine thea, Leucothoe euryonyx, Aora spinicornis and Elasmopus vachoni. Few species (Harpinia ala, Tryphosella simillima, Uncionella lunata) have been collected solely in coralligenous communities (Bellan-Santini 1998).

Isopoda

Laubier (1966) and Hong (1980) report 14 species from coralligenous communities. Cymodoce truncata, Jaeropsis brevicornis, Paranthura nigropunctata, Synisoma sp., Gnathia maxillaris and Paragnathia formica seem to be relatively common species.

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Decapoda

The density of decapods in coralligenous concretions is very high, the estimate being 170 individuals in 500 g dw of Mesophyllum alternans (García-Raso & Fernández Muñoz 1987). According to García-Raso et al. (1996), it is very difficult to distinguish characteristic species of the coralligenous community because the assemblages are very similar to those found in other communities where there is shelter (e.g., the rhizomes of Posidonia oceanica). Alpheus dentipes, Athanas nitescens, Pilumnus hirtellus, Pisidia longicornis, Galathea bolivari, Cestopagurus timidus and Thoralus cranchii are considered to be the characteristic decapod crus- taceans inhabiting the shallow coralligenous frameworks of Mesophyllum alternans in the south- western Mediterranean, along with, in certain areas, Porcellana platycheles, Synalpheus hululensis and Calcinus tubularis (García-Raso 1988). The three species which account for most of the biomass of the decapod crustaceans in the shallow coralligenous communities of the southwestern Medi- terranean use this environment in different ways. In Pilumnus hirtellus, the coralligenous habitat seems to be a recruitment site, where mainly juveniles are recorded. The whole life cycle of Alpheus dentipes takes place in the coralligenous concretions, whereas in Synalpheus hululensis the coral- ligenous habitat provides shelter only for reproductive individuals (García-Raso & Fernández Muñoz 1987). Other species of decapods frequently reported from coralligenous bottoms are Alpheus ruber, A. megacheles, Pilumnus spinifer, Pisa tetraodon, Galathea intermedia, Eurynome aspera, Macropodia czerniavskii, Inachus thoracicus, Processa macrophthalma, Periclimenes scriptus, Typton spongicola, Balssia gasti and Pisidia longimana (Laubier 1966, Hong 1980, Carbonell 1984, García-Raso 1988). Other large decapods that are usually found in coralligenous communities are Dromia personata, Palinurus elephas, Scyllarus arctus, Scyllarides latus and Homarus gammarus (Corbera et al. 1993). In deep waters, the decapod fauna reported by García-Raso (1989) is different from that reported from shallow water coralligenous habitats. This author found a total of 30 species, with Pilumnus inermis, Galathea nexa and Euchirograpsus liguricus being the most abundant decapods in these kinds of bottoms from the southwestern Mediterranean.

Pterobranchia

Only one pterobranch, Rhabdopleura normani, is reported by Laubier (1966) living as an epibiont of bryozoans.

Brachiopoda

Brachiopod species usually inhabit small crevices and interstices within the concretionary masses of the coralligenous assemblages. Crania anomala, Argyrotheca cistellula, A. cordata, A. cuneata, Megathiris detruncata and Lacazella mediterranea are the brachiopods most commonly reported from coralligenous communities (Laubier 1966, Logan 1979, Hong 1980). Another two species, Megerlia truncata and Platidia davidsoni, which are more typical of the bathyal zone, are seldom collected from coralligenous habitats (Vaissière & Fredj 1963, Gamulin-Brida 1967, Logan 1979).

Bryozoa

Bryozoans are very abundant in coralligenous communities: 67 species in Banyuls (Laubier 1966), 133 in Marseilles (Hong 1980), 113 in the Medes Islands (Zabala 1984) and 92 in Cabrera (Ballesteros et al. 1993). A tentative estimate of the total number of bryozoans that thrive in coralligenous bottoms according to these studies is around 170 species.

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According to Zabala (1986) four different aspects of the distribution of bryozoans can be distinguished in coralligenous communities. The main species mentioned below derive from the studies by Laubier (1966), Hong (1980), Zabala (1984, 1986) and Ballesteros et al. (1993).

1. The flat surfaces of the coralligenous platform are dominated by Pentapora fascialis and Myriapora truncata, which have Nolella spp., Aetea spp., Crisia spp., Scrupocellaria spp., Mimosella verticillata and Synnotum aegyptiacum as epibionts. Turbicellepora avicularis is very common overgrowing gorgonians, and Chorizopora brongniartii, Diplosolen obelium, Tubulipora plumosa, Puellina gattyae and Lichenopora radiata are common epibionts of other organisms. Other common species are Beania magellanica, B. hirtissima, Mollia patellaria, Schizomavella auriculata, Cellepora pumicosa, Plagio- ecia spp., Cellaria fistulosa and C. salicornioides. 2. Coralligenous walls have the species reported above but also Smittina cervicornis, Ade- onella calveti, Chartella tenella, Cribilaria innominata, Schizomavella spp., Parasmittina tropica, Sertella spp., Caberea boryi and Spiralaria gregaria. 3. Cavities and overhangs of coralligenous outcrops reveal a bryozoan fauna that is almost identical to that present in semidark caves, with several species already reported above, along with Dentiporella sardonica, Brodiella armata, Turbicellepora coronopus, Ryn- chozoon bispinosum, Schizotheca serratimargo, Escharoides coccinea, Escharina vul- garis, Callopora dumerilii, Smittoidea reticulata, Cribilaria radiata, Hippomenella mucronelliformis, Crassimarginatella maderensis, C. crassimarginata, Buskea nitida, Celleporina spp., Prenantia inerma, Diaporoecia spp., Enthalophoroecia deflexa and Idmidronea atlantica. 4. A final group is made up of species that appear mainly in deep-water coralligenous habitats, below 50 m depth, and are composed of stenotherm species that are also very resistant to sedimentation: Figularia figularis, Escharina dutertrei, E. porosa, Onycho- cella marioni, Omaloseca ramulosa, Buskea dichotoma, Escharella ventricosa, Entha- lophoroecia gracilis, Schizoporella magnifica, Mecynoecia delicatula, Idmidronea coerulea and Hornera frondiculata.

Crinoidea

Two crinoids have been reported from coralligenous habitats, the common Antedon mediterranea (Laubier 1966, Ballesteros et al. 1993) and A. bifida (Montserrat 1984).

Ophiuroidea

According to Tortonese (1965), Laubier (1966), Hong (1980) and Montserrat (1984), up to 17 species of ophiuroids have been reported from coralligenous communities. There are some species that can be considered as characteristic of these habitats, such as Ophioconis forbesii, Amphiura mediterranea and A. apicula (Tortonese 1965, Laubier 1966). Other brittlestars live entangled in gorgonians: Astropartus mediterraneus and Ophiacantha setosa. The commonest species, however, are Ophiothrix fragilis, Ophiopsila aranea, Amphiura chiajei, A. filiformis, Amphipholis squamata and Ophioderma longicaudum. Ophiocomina nigra, despite being a typical species of soft bottoms, is usually found in the small cavities containing sediment within coralligenous communities.

Asteroidea

Up to eight species of seastars have been reported from coralligenous bottoms (Tortonese 1965, Laubier 1966, Munar 1993). The most abundant species is the ubiquitous Echinaster sepositus.

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Marthasterias glacialis and Hacelia attenuata are also common, while Ophidiaster ophidianus is only found in the southern, warmer areas of the Mediterranean.

Echinoidea

Fourteen species of sea urchins are reported from coralligenous communities (Tortonese 1965, Laubier 1966, Hong 1980, Montserrat 1984, Munar 1993). The most common species is Sphaerechi- nus granularis (Sartoretto 1996), which is an important bioeroder. Also common in deep waters are Genocidaris maculata and Echinus melo. Psammechinus microtuberculatus is usually hidden inside the cavities of coralligenous outcrops. Juveniles of Paracentrotus lividus (and Arbacia lixula) are sometimes found, but are never abundant. Centrostephanus longispinus is more abundant in the warmer areas of the Mediterranean and usually lives within coralligenous crevices (Pérès & Picard 1958, Laborel 1960, Harmelin et al. 1980, Francour 1991). Finally, Echinocyamus pusillus is a ubiquitous and very small species that inhabits the small patches of sand and gravel inside the concretions.

Holothurioidea

The most commonly observed species of sea cucumber is Holothuria forskali, which can be rather abundant in some coralligenous platforms (Laubier 1966, Ballesteros & Tomas 1999). However, the genus Cucumaria has several species that live endolithically (C. saxicola, C. planci, C. kirsch- bergii, C. petiti). Another four species typical of sandy and muddy habitats have also been reported (Tortonese 1965, Laubier 1966, Montserrat 1984): Holothuria tubulosa, H. mammata, Trachytyone tergestina and Stichopus regalis.

Tunicata

Ramos (1991) describes a high species richness of ascidians in coralligenous communities, the families Didemnidae and Polyclinidae being especially present. In fact, around 70% of ascidian fauna is present in the coralligenous community (82 species). According to Ramos (1991), the most characteristic species of the coralligenous community are Cystodites dellechiajei, Ciona edwardsi and Halocynthia papillosa, although other abundant species include Diplosoma spongiforme, Dis- taplia rosea, Trididemnum cereum, T. armatum and Polycarpa gracilis. Other species that are often collected from coralligenous communities are Distomus variolosus, Didemnum maculosum, Ect- einascidia herdmanni, Clavelina nana, Polysyncraton lacazei, P. bilobatum, Polycarpa pomaria, Pyura spp., Microcosmus polymorphus, M. sabatieri, Styela partita, Eudistoma planum, E. banyule- nsis, Pseudodistoma cyrnusense, Aplidium densum and A. conicum (Laubier 1966; Hong 1980; Turon 1990, 1993). Clavelina dellavallei and Rhodosoma verecundum seem to be especially abundant in the coralligenous concretions from the eastern Mediterranean (Pérès & Picard 1958).

Pisces

The fish fauna from the coralligenous community includes many fishes covering a wide bathymetric range, such as Epinephelus marginatus, Sciaena umbra, Coris julis, Dentex dentex, Symphodus mediterraneus, S. tinca, Diplodus vulgaris, Apogon imberbis, Chromis chromis or Labrus merula. However, there is a group of species that are characteristic of coralligenous communities. Some of these, like Lappanella fasciata or Acantholabrus palloni, are species restricted to deep waters (Sartoretto et al. 1997), but others, such as Anthias anthias (Harmelin 1990), as well as (among the commonest species) Gobius vittatus, Phycis phycis and Labrus bimaculatus (Garcia-Rubies 1993, 1997), are easily observed during recreational diving. Other species are more abundant in

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coralligenous outcrops than in shallow waters, examples being Serranus cabrilla, Spondyliosoma cantharus, Diplodus puntazzo, Ctenolabrus rupestris, Spicara smaris, Scorpaena scrofa and Sym- phodus doderleini. Finally, Conger conger, Muraena helena, Zeus faber, Scorpaena notata, Scyliorhinus canicula and S. stellaris are also observed in the coralligenous habitat (Sartoretto et al. 1997, Ballesteros, personal observation). The fish fauna inhabiting the small crevices of coralligenous concretions probably consists of fishes with cave-dwelling tendencies, although data are very scarce. Hong (1980) reports juveniles of Diplecogaster bimaculata and Gobius niger. According to Patzner (1999), cryptobenthic species, such as Thorogobius ephippiatus, T. macrolepis, Corcyrogobius liechtensteinii, Gammogobius stein- itzii and Didogobius splechtnai, which are usually observed in caves, may also be present in the small holes of deep water coralligenous habitats. Odondebuenia balearica is another cryptobenthic fish that inhabits coralligenous communities but is rarely observed (Riera et al. 1993). Studies of the fish fauna of the coralligenous habitat have obtained slightly different results when performed in different areas (Bell 1983; Harmelin 1990; Garcia-Rubies 1993, 1997; Balles- teros & Tomas 1999). These differences should be related to biogeography or to differences in coralligenous rugosity. Symphodus melanocercus, for example, is a characteristic coralligenous species in Cabrera and other localities of the Balearic Islands, but it is a widespread species in terms of depth distribution in the northwestern Mediterranean (García-Rubies 1993).

Endangered species Although it is very difficult to determine the conservation status of any marine species living in the relatively deep waters where coralligenous communities develop, several approaches to endan- gered species have been taken. According to Boudouresque et al. (1990), at least eight species of macroalgae that live in coralligenous communities can be considered endangered: Chondrymenia lobata, Halarachnion ligulatum, Halymenia trigona, Platoma cyclocolpa, Nemastoma dichotomum, Ptilophora mediter- ranea, Schizymenia dubyi and Laminaria rodriguezii. However, this list can be greatly extended by adding species such as Aeodes marginata, Sphaerococcus rhizophylloides, Schmitzia neapoli- tana, Ptilocladiopsis horrida, Microcladia glandulosa, Rodriguezella bornetii, R. pinnata and Lomentaria subdichotoma (Ballesteros, unpublished data). Most of these species have coralligenous or maërl beds as their only habitats, and seem to be very sensitive to pollution and increased sedimentation rates (Boudouresque et al. 1990), two of the main threats to coralligenous assem- blages. The case of Laminaria rodriguezii is especially relevant, as this species develops best in rhodolith beds, from where it has almost disappeared due to trawling activities; coralligenous bottoms now constitute its only refuge. Several animal species in coralligenous habitats are also considered to be at risk (Boudouresque et al. 1991). Although none of them is in danger of extinction, local depletion of some species stocks may occur. Most of the endangered species have great commercial value and this is the main reason for their increased rarity. Among the anthozoans, red coral (Corallium rubrum) is exploited commercially in almost all Mediterranean countries, and its stocks have strongly declined in most areas, particularly in shallow waters (Weinberg 1991). Populations of gorgonians common in coralligenous communities but which lack commercial value, such as Paramuricea clavata, Eunicella cavolinii and E. singularis, are pulled out inadvertently by recreational divers (Coma et al. 2004). The black coral, Gerardia savaglia, is a very rare species and can be a target for collection by divers, thus making the species even scarcer (Boudouresque et al. 1991). Some species of molluscs living in coralligenous communities are also threatened. The edible rock-borer bivalve Lithophaga lithophaga is considered an endangered species (Boudouresque et al.

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1991) despite being extremely abundant. Harvesting by divers is only important in shallow waters and the reason behind calls for the species to be protected is actually an attempt to protect the shallow benthic communities in rocky shores dominated by macroalgae (Russo & Cicogna 1991, Hrs-Brenko et al. 1991), not the coralligenous bottoms themselves. Protection of the two species of fan mussels (Pinna nobilis and P. rudis) present in the Mediterranean has also been proposed (Boudouresque et al. 1991), because they have been decimated in northern Mediterranean areas by coastline modification and harvesting as souvenirs (Vicente & Moreteau 1991). P. nobilis mainly grows in seagrass meadows, and its presence in coralligenous communities is very unusual (Vicente & Moreteau 1991). However, P. rudis (= P. pernula) is frequently seen in coralligenous habitats, at least in the warmer areas of the western Mediterranean (Ballesteros 1998). According to Templado (1991), neither of the two species of the genus Charonia that occur in the Mediterranean is threatened by extinction. C. lampas is rare in the northern Mediterranean but rather common in the southwest, whilst C. tritonis variegata has been recorded in the eastern and southwestern Mediterranean. Both species are collected and used for decorative purposes but Templado (1991) argues that indirect anthropogenic pressures (coastline development) are the main reason for its increased rarity, or even local extinction. The sea urchin Centrostephanus longispinus is also considered an endangered species by Boudouresque et al. (1991), despite being a rare species in the northwestern Mediterranean, probably due to biogeographical reasons. No anthropogenic pressure has been proposed to explain its rarity. The slipper lobster, Scyllarides latus, is highly appreciated gastronomically. The high market prices it obtains have stimulated increased fishing pressure, which has led to a dramatic decline in the abundance of this species in several areas of the Mediterranean (Spanier 1991). It is more common in the warmer Mediterranean areas (e.g., eastern Mediterranean, Balearic Islands), and rarest in the colder ones. The dusky grouper, Epinephelus marginatus (= E. guaza), is the main target species in spearfish- ing activities and its abundance has greatly decreased in several Mediterranean areas, mainly in the north (Chauvet 1991). However, immature specimens and juveniles are very abundant in certain areas (e.g., Balearic Islands; Riera et al. 1998) and, therefore, the species is only threatened in those places where there is no regular recruitment (e.g., northwestern Mediterranean). Moreover, the recovery of this species in marine protected areas has repeatedly been reported (Bell 1983, Garcia- Rubies & Zabala 1990, Francour 1994, Coll et al. 1999), as has reproduction (Zabala et al. 1997a,b), suggesting that adequate management can rapidly improve its situation in those areas where stocks continue to decline. Other groupers, such as E. costae (= E. alexandrinus), Mycteroperca rubra and Polyprion americanus (Riera et al. 1998; Mayol et al. 2000), are probably in a worse situation, as their population stocks are much lower than those of the dusky grouper. Sciaena umbra and Umbrina cirrosa are the two other fish considered as endangered in the review by Boudouresque et al. (1991). Both can live in coralligenous communities, the former being more abundant. Although both species are easily spearfished, Sciaena umbra stocks readily recover after fishing prohibition (Garcia-Rubies & Zabala 1990, Francour 1994). Other species are not included in the list of Mediterranean endangered species by Boudouresque et al. (1991), although according to Mayol et al. (2000) they are exposed to major risk. This is the case of several small sharks inhabiting detritic and coralligenous habitats: Scyliorhinus stellaris, Mustelus asterias, M. mustelus, Squalus acanthias and S. blainvillei. All these species were very common in fish catches by Balearic Island fishermen at the beginning of the twentieth century, but are now extremely rare. Other species that can thrive in coralligenous communities and which are considered by Mayol et al. (2000) to be endangered are seahorses (mainly Hippocampus ramulosus), Gaidropsarus vulgaris and some cryptobenthic fishes (Didogobius splechtnai, Gammogobius stein- itzii). These are not commercial species and their increased rarity may be related to indirect effects of fishing (such as cascading effects), physical disturbances of trawling or other unknown causes.

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Biotic relationships Spatial interactions, herbivory, carnivory Biotic relationships, both trophic ones and those related to spatial interactions, are a major force in structuring all ecosystems. In fact, the whole buildup of coralligenous frameworks is affected by the interactions between encrusting corallines and other sessile, invertebrate builders (Figures 16A,B). The final result (that is, what the framework looks like) is not only related to which builder has been the most effective but also to how the borers (from sea urchins to excavating sponges and polychaetes) have subsequently changed the structure. Biotic relationships at this level are, there- fore, crucial in building coralligenous assemblages. Trophic relationships are especially interesting in coralligenous communities because the main organisms are not easily edible. Most of them have skeletons that contribute to structure but which also deter feeding (Zabala & Ballesteros 1989). Others may have chemical defences that make them unpalatable or even toxic (Martí 2002). Most of the largest sessile invertebrates living in coralligenous communities do not feed directly upon other animals from the coralligenous assem- blage but rather on the pelagic system. In fact, the largest part of the living biomass in coralligenous assemblages consists of algae and suspension feeders (True 1970, Zabala & Ballesteros 1989), which suggests that herbivory and carnivory are not as important as in other marine Mediterranean environments. The low dynamism of coralligenous habitats (Garrabou et al. 2002) also supports this suggestion.

Figure 16 (See also Colour Figure 16 in the insert.) Spatial interactions are crucial in the buildup of coral- ligenous assemblages. (A) Mesophyllum alternans overgrows Lithophyllum cabiochae which, in its turn, is epiphytised by the small green alga Halicystis parvula (above) and a tunicate (below); (B) Lithophyllum frondosum overgrows sponge Ircinia oros. Strong prey selection is present in the coralligenous community. (C) Opisthobranch Discodoris atromaculata feeds almost exclusively on sponge Petrosia ficiformis; (D) Opisthobranch Flabellina affinis feeds on hydrozoans of the genus Eudendrium. (Photos by the author.)

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However, both herbivory and carnivory are relevant to coralligenous communities. The sea urchin Sphaerechinus granularis is a major browser of encrusting corallines (Sartoretto & Francour 1997), and several invertebrates (opisthobranchs, amphipods, copepods) are able to feed on the green alga Halimeda (Ros 1978). Examples of carnivores include most of the fishes that thrive in coralligenous communities, as well as most prosobranchs, echinoderms, vagile polychaetes and crustaceans. Although feeding by most animals is not selective, there are some noteworthy examples of animals that have a strong prey selection. These include the well-known cases of the opistho- branch Discodoris atromaculata, which feeds on the sponge Petrosia ficiformis (Figure 16C), and the other opisthobranch Flabellina affinis, which feeds mainly on hydrozoans of the genus Euden- drium (Figure 16D) (Ros 1978). Other interesting examples have recently been reported for cope- pods of the genus Asterocheres, which systematically feed on both rhagons and adult sponges by sucking the material produced at the ectosome of the sponge (Mariani & Uriz 2001).

Chemical ecology The production of active substances in benthic organisms plays a major role in structuring benthic communities. Some of these substances act as a defence against consumers (e.g., unpalatable or repellent substances) while others mediate the interactions between species regarding the occupation of space (Martí 2002). Sponges, bryozoans and tunicates are the taxa with the largest number of species producing active substances (Uriz et al. 1991). The lower side of coralligenous blocks, as well as semidark caves and overhangs, exhibits the highest percentage of active species of all the Mediterranean communities sampled by Uriz et al. (1991), suggesting that investment in production of allelochemicals plays an important role in space competition in coralligenous assemblages (Figure 17A).

Epibiosis, mutualism, commensalism, parasitism There are innumerable relationships between species in coralligenous communities that can be described as ‘associations’, and these may or may not involve trophic transfer. Sometimes it is difficult to differentiate between them because the natural history of the species, or the benefits and costs of the components of the association, are unknown or not clearly understood. The purpose here is not to review these associations, nor to mention all those which have been described for coralligenous communities, but to report some examples of epibiosis, mutualism, commensalism and parasitism that can give an idea of the complexity of the coralligenous community with respect to these kinds of relationships. Epibiosis is a widespread phenomenon in benthic communities and coralligenous assemblages are an excellent example of the different strategies adopted by organisms to cope with this problem (True 1970). Some basibionts tolerate different degrees of epibiosis and even almost complete overgrowth, whilst others have developed antifouling defences to avoid overgrowth. Both types of strategies can be displayed by species from the same zoological group living in coralligenous communities. For example, the ascidians Microcosmus sabatieri and Pyura dura are usually com- pletely covered by a wide array of epibionts, whilst Halocynthia papillosa and Ciona edwardsi are always free of overgrowing organisms (Ramos 1991). Some epibionts are considered to select their hosts, whilst others are not selective. The antho- zoan Parerythropodium coralloides usually grows over the axes of gorgonians (Eunicella, Para- muricea clavata), although it can also grow over other animals and seaweeds, or be attached to rubble or any other kind of substratum (Laubier 1966, Gili 1986). The anthozoan Parazoanthus

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Figure 17 (See also Colour Figure 17 in the insert.) (A) Space competition can also be mediated by trophic depletion of the surrounding waters, or by allelochemicals. Tunicate Pseudodistoma cyrnusense inhibits growth of bryozoan Hornera frondiculata; (B) Zoantharian Parazoanthus axinellae is usually a selective epibiont of sponge Axinella damicornis; (C) Nonselective epibionts overgrow the gorgonian Paramuricea clavata: the worm Salmacina dysteri and the bryozoan Pentapora fascialis; (D) The barnacle Pyrgoma anglicum living inside the anthozoan Leptopsammia pruvoti can be considered a case of parasitism. (Photos by the author.)

axinellae prefers sponges of the genus Axinella (mainly A. damicornis) (Figure 17B), but it can also grow over other sponges or over rock or encrusting corallines (Gili 1986). The bryozoan Turbicellepora avicularis prefers the basal parts of the axes of gorgonians Paramuricea clavata and Eunicella spp. (Laubier 1966, Zabala 1986). The number of species able to act as nonselective epibionts in coralligenous communities is huge because most of the space is occupied and larvae usually have to settle on living animals or plants. Therefore, almost all sessile species can be epibionts (True 1970) (Figure 17C). Gautier (1962), for example, reviewed the epibiosis of bryozoans over bryozoans in coralligenous assem- blages, and Nikolic (1960) reported up to 18 species growing over Hippodiplosia foliacea in a coralligenous framework in the Adriatic Sea. Of particular interest are the observations by Laubier (1966) on some heterotrichs (Protozoa) of the family Folliculinidae that live close to the zooid mouth of different species of bryozoans or even inside its empty zooids. Laubier (1966) reported up to six species of Folliculinidae living as epibionts of bryozoans in the coralligenous communities of Banyuls. Mutualism has been reported, for example, in the case of the scyphozoan Nausitoë punctata and several horny sponges (Uriz et al. 1992b). Cacospongia scalaris, Dysidea avara and D. fragilis utilize the thecae of Nausitoë punctata as a substitute for skeletal fibres, presumably reducing metabolic costs associated with skeleton building. The scyphozoan should thus benefit from greater protection against predation and mechanical disturbance, trophic advantages (inhalant flow carries out small particles susceptible to capture by the scyphozoan), and chemical defence against pred- ators, as the three species of sponges exhibit toxicity (Uriz et al. 1992c). Commensalism is one of the most common relationships in coralligenous communities. Most relationships are considered as commensalism because they lack unequivocal parasitic features, as in the case of the polychaete Eunice siciliensis and the decapods Alpheus dentipes and Typton

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spongicola, which live as endobionts of the boring sponge Cliona viridis (Laubier 1966). Another well-known example is that occurring between C. viridis and the likewise boring polychaete Dipolydora rogeri (Martin 1996). The curious feature of this association is that it persists even when the sponge is massive and nonexcavating. The feeding activity of the polychaete is favoured by the inhalant flow of the sponge and, moreover, the sponge offers physical protection to the worm when they are not embedded within the calcareous algae. The ability of the worm to manipulate relatively large particles (either to feed or to build its tubes) may favour the filtering activity of the sponge by cleaning the area around the inhalant papillae, thus preventing the collapse of their orifices (Martin & Britayev 1998). Polychaetes of the genus Haplosyllis are well-known commensalists (Martin & Britayev 1998). Up to 200 specimens of Haplosyllis spongicola have been found in 1 cm2 of sponge (Bacescu 1971), and thus sponges merit the description of ‘living hotels’. Another case is the polychaete Haplosyllis depressa chamaeleon, which lives exclusively as a commensal of the sea fan Para- muricea clavata, where it crawls above the living colonies (Laubier 1960, 1966). The barnacle Acasta spongites lives inside the sponge Ircinia variabilis, as well as other sponges (Laubier 1966, Rützler 1976, Uriz et al. 1992b); it can be considered as a parasite because the cirripede settles into the inhalant oscula of the sponge, rendering it useless. Another barnacle, Pyrgoma anglicum, is quite often found living inside the anthozoan Leptopsammia pruvoti (Figure 17D). A further example of parasitism in coralligenous communities is found in the two boring spionid polychaetes Dipolydora armata and Polydora hoplura and the bryozoans Dentiporella sardonica, Porella concinna, Brodiella armata and Schizomavella auriculata (Laubier 1959a, 1959b). The bryozoans are infested throughout their basal layer and polychaetes excavate galleries that reach the surface of the colony or modify the growth form of the bryozoan in such a way that the polychaete tubes are composed of host zooids. In both cases the bryozoan is stimulated to build calcareous formations around the end of the polychaete tubes, facilitating the feeding behaviour of the worm and protecting it (Laubier 1966).

Processes Growth and age of coralligenous frameworks The mean growth rate of pillars of Mesophyllum alternans (reported as M. lichenoides) in La Ciotat (NW Mediterranean) has been estimated by radiocarbon dating to be 0.19 mm yrÐ1 (Sartoretto 1994), with a range of 0.11 to 0.26 mm yrÐ1. Similar values of 0.16 mm yrÐ1 over the last 640 yr were obtained in a coralligenous block sampled at 15 m in the Natural Reserve of Scandola (Corsica) (Sartoretto et al. 1996). Ages obtained by radiocarbon dating of coralligenous frameworks situated at depths between 10 and 60 m in the northwestern Mediterranean range from 640 ± 120 yr before the present (BP) to 7760 ± 80 yr BP (Sartoretto et al. 1996). Internal erosion surfaces within the concretions provide evidence of discontinuous development. The accumulation rate of the coralligenous constructions is very low (0.006Ð0.83 mm yrÐ1) and oscillates greatly according to depth and time period. The highest accumulation rates (0.20Ð0.83 mm yrÐ1) have been recorded for deep coralligenous frame- works and correspond to a period between 8000 and 5000 yrs BP. After 5000 yr BP, the only appreciable accumulation rates (0.11Ð0.42 mm yrÐ1) have been recorded for coralligenous frame- works situated in relatively shallow waters (10Ð35 m depth), whereas the accumulation rates of concretions below a depth of 50 m is almost nil. Thus, the development of these deep coralligenous formations occurred a long time ago, when the depth of the overlying layer of water probably did not exceed 10Ð15 m, and since their period of settlement (8500Ð7000 yr BP) the accumulation rate has progressively declined. This decrease in accumulation rates can no doubt be explained by the

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stable, but rather unfavourable, environmental conditions resulting from the decrease in irradiance related to increased water depth. It is also worth noting that the coralligenous frameworks below a depth of 30 m in the Marseilles area are today inactive and almost devoid of living coralline algae. In contrast, those present in Corsica at a depth of 50 m and below (down to 65 m) are completely covered by living corallines and are in an active period of growth; this difference must be related to the clear waters present in Corsica.

Carbonate production Although there are no specific studies on the carbonate production of the coralligenous community on a yearly basis, Canals & Ballesteros (1997) estimated the carbonate production of the phyto- benthos in the coralligenous and other communities from the continental shelf of the Balearic Islands, taking into account the standing crop of calcareous algae and their P/B ratios. The coral- ligenous community thriving in relatively shallow waters (with Mesophyllum alternans and Hal- Ð2 imeda tuna as dominant algae) was the one with the highest production (around 465 g CaCO3 m yrÐ1). Production of deep water coralligenous concretions dominated by Lithophyllum cabiochae Ð2 Ð1 was much lower (around 170 g CaCO3 m yr ), but even this rate is much higher than average Ð2 Ð1 carbonate production for the Balearic shelf as a whole (100 g CaCO3 m yr ). The contribution of suspension feeders to the total carbonate production of coralligenous communities in the Balearic shelf, as well as in other Mediterranean areas, is practically unknown. However, estimates of the animal carbonate production in deep water (25Ð50 m depth) rocky bottoms from the Alboran Sea (southwestern Mediterranean), mainly dominated by big suspension feeders with calcareous skel- etons (predominantly the coral Dendrophyllia ramea, the bryozoans Pentapora fascialis, Smittina cervicornis and Myriapora truncata, and polychaetes such as Salmacina dysteri, Protula sp. and Ð2 Ð1 other serpulids), are very high (around 660 g CaCO3 m yr ) (Cebrian et al. 2000). Although the combination of highly productive calcareous animals in these bottoms is unusual in other Medi- terranean areas, this figure can be considered as the upper limit for animal carbonate production in the coralligenous habitat.

Bioerosion The most active browser in the coralligenous community is the sea urchin Sphaerechinus granularis, which accounts for a large part of the total coralligenous erosion. Sartoretto & Francour (1997) Ð2 Ð1 calculated an erosion rate ranging between 16 and 210 g CaCO3 m yr , with higher values in shallow waters and lower values in coralligenous concretions around 50 m depth. The bioerosional role of Echinus melo cannot be measured, but it is very low. Among macroborers the spionid polychaetes Polydora spp. and the mollusc Hyatella arctica are the only macrofauna that colonise experimental blocks after 1 yr of exposure (Sartoretto 1998). In this study, the total erosion caused by annelids and molluscs increases with the number of Ð2 Ð2 individuals but does not exceed 5.73 ± 0.77 g CaCO3 m at 20 m and 1.50 ± 0.99 g CaCO3 m at 60 m after 1 yr. In natural communities macroborers are more abundant (excavating sponges, Sipunculida, perforating molluscs) and their absence in the experimental substrata may be due to their slow growth and to the high spatial and temporal variability of larval recruitment (Kleeman 1973). The comparative erosion rates produced by the three main types of eroding organisms (browsers, microborers and macroborers) have been estimated by Sartoretto (1996). Sea urchins account for

roughly 95% of the total mass of CaCO3 eroded. Bioerosion by micro- and macroborers accounts for the remaining 5%, that of microborers being very low due to the great depths at which

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coralligenous frameworks develop, and the high sedimentation rates, factors that prevent any significant development of microborers (Sartoretto 1998). Bioerosion by macroborers is probably underestimated because the studies of Sartoretto (1998) do not take into account several organisms that are common in coralligenous communities, in particular the bivalve Lithophaga lithophaga and excavating sponges (Sartoretto et al. 1996). The overall range of bioerosion observed in the Ð2 Ð1 coralligenous community is between 220 g CaCO3 m yr in relatively shallow waters and 20 g Ð2 Ð1 CaCO3 m yr at a depth of 60 m. This range is in agreement with the structure and age of coralligenous frameworks situated below 50 m depth in the region of Marseilles (Sartoretto 1996), and are at least one order of magnitude below the bioerosion experimentally estimated in coral reefs (Chazottes et al. 1995).

Sedimentation The rugosity of coralligenous frameworks promotes the deposition of particles that take part in the buildup of the coralligenous structure through complex processes of lithification (Marshall 1983). However, high sedimentation rates can be a problem because sediment particles may cover the thalli of the encrusting corallines and screen them against light (Laborel 1961), as well as prevent the recruitment of new plants (Sartoretto 1996). Not all the sediment particles deposited in the coral- ligenous structure are included in the concretion; indeed, many of them are eliminated by different browsers, while others are resuspended by currents, organisms and gravitation. The rugosity of different coralligenous types is different, as is the capacity for sediment retention. The amount of water movement is also important, and this usually decreases with depth. Studies conducted by Sartoretto (1996) in the Marseilles region conclude that around 9 kg mÐ2 yrÐ1 is retained in the coralligenous concretions situated at a depth of between 30 and 60 m, while the retention in shallow waters is much lower. However, daily sedimentation rates are extremely high in shallow waters (~500 g mÐ2) and much lower in deep waters (between 10 and 35 g mÐ2) (Sartoretto 1996). The sediment that is finally incorporated into the coralligenous framework by a process of lithification has a large calcareous component of organisms living in the coralligenous community. Major contributors are coralline algae (57%), bryozoans (19%), molluscs (16%), corals and ser- pulids (3% each) (Laubier 1966).

Dynamics and seasonality The study of dynamics for the whole coralligenous community is a very difficult task and has only very recently been undertaken. Garrabou et al. (2002) used a photographic method to look for changes occurring in two monitored areas of coralligenous concretions covering 310 cm2 over a period of 2 yr. The rate of change observed averaged 10% monthÐ1, with very low to nil seasonality. Most of the area (>70%) remained almost constant throughout the 2 yr of monitoring, showing no or few transitions, and this indicates the great persistence of the animals and plants that thrive in coralligenous communities (Figure 18). Other studies have been conducted with some components or species of coralligenous com- munities. In fact, most studies dealing with the biology of the main species in coralligenous communities (see next section) have described the effects of seasonality, when this process exists. In terms of benthic flora, Ballesteros (1991a) described the seasonal cycle of several phyto- benthic communities from the northwestern Mediterranean, making a between-community com- parison using the same variables as descriptors. The coralligenous community with Mesophyllum alternans and Halimeda tuna had the lowest seasonality of all the subtidal communities studied, this being almost constant in autumn, winter and spring, but with peak productivity in summer,

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Figure 18 (See also Colour Figure 18 in the insert.) Maps of transition intensity resulting from overlay procedures of images from the same plot (310 cm2) along a depth gradient in a vertical wall at the Medes Islands (NE Spain) during 2 yr of sampling. Patch colour denotes number of changes taking place in each patch (see legend). Coralligenous communities (14 and 20 m depth) display much lower transition rates than shallow water communities, indicating high persistence and low rates of change in the animals and plants thriving in the coralligenous communities. (From Garrabou et al. 2002. With permission from Elsevier.)

during which time there were higher biomass values than for the rest of the year. Piazzi et al. (2004) found significant seasonal differences that were mostly related to the disappearance of many turf species and the decrease in cover of most erect algae, principally foliose and corticated-terete forms, in winter. Although growth of coralline algae is almost constant throughout the year (Garrabou & Ballesteros 2000), Halimeda growth occurs mainly in summer (Ballesteros 1991c). In terms of structural changes in the community, two stages can be discerned over an annual cycle: a diversified community stage, with a reduced coverage of Halimeda and other soft algae, and a developed com- munity stage, characterized by a high coverage of Halimeda (Ballesteros 1991b). The shift from the diversified community stage to the developed community stage takes place through a production phase (early summer). A diversification phase can be distinguished in late autumn, when a sudden fall in Halimeda coverage is detected (Ballesteros 1991b) (Figure 19). Most benthic hydrozoans exhibit a seasonal pattern, with reproduction in spring or autumn and growth from autumn to spring; most of them disappear during the summer, leaving only dormant basal stolons (Boero et al. 1986). Epiphytic hydrozoans on Halimeda tuna decline in abundance in summer because of the death of old thalli of Halimeda, the growth of new thalli and apical articles on existing thalli, and possibly because of interspecific competition with epiphytic algae (Llobet et al. 1991a).

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Production phase

MME SU R

Developed community Diversified community

A

U S

T P

U

R M

I

N N G

WINTER

Diversification phase

Figure 19 Although seasonality in structural patterns is not very evident in coralligenous communities, assemblages of the green alga Halimeda tuna show high production in summer, higher biomass in autumn, low production in winter and high spatial heterogeneity in spring, going through the two stages of a diversified community (spring) and a developed community (autumn). (From Ballesteros 1991a.)

Anthozoans exhibit a marked seasonality in all activities (Coma et al. 1998a, Garrabou 1999). According to Coma et al. (2002) respiration rates of Paramuricea clavata, Dysidea avara and Halocynthia papillosa vary two- to three-fold across the annual cycle, exhibiting a marked seasonal pattern but showing no daily cycle or significant day-to-day variability within months. The respi- ration rate of Paramuricea (a passive suspension feeder) does not correlate with temperature, but that of Dysidea and Halocynthia (active suspension feeders) increases with temperature. There is a low rate of new tissue synthesis during summer, together with the contraction of polyps and a

low Q10, which explains the low respiration rates of Paramuricea observed during the period of highest temperature. These low respiration rates support the hypothesis that energy limitations may underlie summer dormancy in some benthic suspension-feeding taxa in the Mediterranean (Figure 20).

22 100

20 75 18

16 50

14

emperature (°C) emperature 25 T

12 (%) Activity rhythm

10 0 JFMAMJJASOND Time

Figure 20 Activity rhythm in the gorgonian Paramuricea clavata, estimated as a percentage of expanded colonies, displays a strong decrease in summer, in conjunction with high water temperatures. This, and other evidence of decreased activity (i.e., growth and reproduction), in Paramuricea, as well as in other suspension- feeders, prompted Coma et al. (2002) to describe summer dormancy for many Mediterranean benthic inver- tebrates. (From Coma et al. 1998a. With permission from Inter-Research.)

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There is growing evidence that seasonal patterns of activity and secondary production of suspension feeders in coralligenous assemblages are characterized by aestivation (Coma et al. 2000). Several types of resting and resistance periods have been observed in several colonial ascidians in the warm season (Turon 1992, Turon & Becerro 1992). In the case of Polysyncraton lacazei the surface of the colonies is covered by a glassy pellicle and the siphonal apertures are sealed. This state is interpreted as a rejuvenative phenomenon that extends the life span of the zooids (Turon 1992). Some sponges also go through a resting, nonfeeding period with cellular restructuring, mainly in summer. For example, some specimens of Crambe crambe appear to be covered by a glassy cuticle, obliterating the oscula and ostia after reproduction, from the end of August until the end of October (Turon et al. 1999). These authors suggest that these resting stages develop not only in response to remodelling following reproduction, but also as an effect of water temperature abnormalities. The decapod fauna also displays a certain seasonality (García-Raso & Fernández Muñoz 1987), due to the intense recruitment of several species in late summer, and a progressive decrease in the density of individuals and an increase in their size from October to June. The fish fauna of coralligenous communities is also affected by seasonality (Garcia-Rubies 1997), although its effect is of very minor importance. The number of species in fish counts along 50 m-long visual transects of the coralligenous bottoms around the Medes Islands slightly decreases in winter, and most fishes seem to be less active than in summer.

Functioning of outstanding and key species Several studies of coralligenous concretions are devoted to species that are particularly abundant, are architecturally important or are economically valuable. A compilation of the major knowledge of these species is presented here.

Coralline algae Growth dynamics of two important coralligenous builders in the northwestern Mediterranean, Mesophyllum alternans and Lithophyllum frondosum, were studied in the bioconcretions of the Medes Islands marine reserve, in a steep wall situated at a depth of between 15 and 30 m (Garrabou & Ballesteros 2000). Growth rates ranged from 0.16 monthÐ1 for Mesophyllum alternans to 0.09 monthÐ1 for Lithophyllum frondosum, with shrinkage rates being 0.09 and 0.04 monthÐ1, respectively. These growth rates are more than one order of magnitude lower than those reported for other Mediterranean and tropical coralline species, but similar to reports for crustose corallines in Arctic and temperate waters. No seasonal pattern in growth or shrinkage was found for either species, although seasonality in conceptacle occurrence was detected in Lithophyllum frondosum, with a high interannual variability. Mesophyllum alternans thalli frequently underwent fissions and fusions (almost one event during the 2-yr monitoring period for 50% of monitored plants), while they were rarely observed in Lithophyllum frondosum. These differences in growth, shrinkage, and fission and fusion events are interpreted as different growth strategies. Mesophyllum alternans has a more opportunistic strategy, growing faster and gaining area more rapidly, although it also loses area at higher rates. Lithophyllum frondosum has a more conservative strategy and is more effective in maintaining the area acquired through its reduced growth rate (Garrabou & Ballesteros 2000).

Halimeda tuna Growth and production of a Halimeda tuna population from a coralligenous community (18 m depth) in the northwestern Mediterranean was studied by Ballesteros (1991c). The production of new segments changed seasonally, being maximal in summer and minimal in winter (Figure 21),

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800 production 700 loss 600 500 400

Segments 300 200 100 0 J-F M-A M-J J-A S-O N-D Time

Figure 21 Seasonal changes in segment production and loss for a population of the green alga Halimeda tuna at 18 m depth in a coralligenous wall off Tossa de Mar (NE Spain). (From Ballesteros 1991c. With permission from Walter de Gruyter GmbH & Co. KG.)

and this suggests that growth is mainly related to temperature and irradiance. The loss of segments seemed to be related to physical disturbances (storms) and herbivory. Annual production of H. tuna Ð2 Ð2 Ð1 Ð2 was estimated at 680 g dw m , equivalent to 114 g organic C m yr and to 314 g CaCO3 m yrÐ1; the yearly P/B ratio was 1.87 yrÐ1. The epiphytic assemblage growing on the segments of H. tuna also displayed high seasonality, with a maximum biomass and species richness in early summer. Values of growth and production reported in Ballesteros (1991c) emphasize the importance of H. tuna as a producer both of organic matter and calcium carbonate in the coralligenous habitat. In fact, available data suggest that calcium carbonate production by Halimeda in shallow corallig- enous concretions is similar to that of coralline algae (Canals et al. 1988).

Porifera Garrabou & Zabala (2001) studied the growth dynamics of four demosponges (Crambe crambe and Hemimycale columella from a ‘precoralligenous’ community, and Oscarella lobularis and Chondrosia reniformis from a coralligenous community in the Medes Islands), and reported rela- tively slow growth dynamics with low growth and shrinkage rates. The coralligenous species had an average relative growth rate of 0.15 monthÐ1 (Oscarella) and 0.022 monthÐ1 (Chondrosia), with shrinkage rates of 0.12 and 0.017 monthÐ1, respectively. Interspecific differences in growth, shrink- age, division and fusion rates were interpreted as evidence of distinct biological strategies aimed at persistence and the occupation of substratum. Chondrosia reniformis is conservative, with slow growth but great resistance to damage. Crambe crambe seems to enhance its rate of space occupation by a high division rate. Hemimycale columella grows quickly and shrinks at low rates, thus spreading rapidly over the substratum. Oscarella lobularis grows and shrinks rapidly, showing great overall growth. Dysidea avara, a common sponge in coralligenous communities (Uriz et al. 1992a) obtained 85% of its ingested carbon from the fraction <5 µm (mostly procaryotes and pico- and nanoplankton) and 15% from the fraction >5 µm (mostly phytoplankton) (Ribes et al. 1999b). However, the partial contributions of the different groups varied seasonally, in accordance with the planktonic compo- sition of the water column. During winter, phytoplankton was an important component of the total uptake (26%), whereas during the rest of the year it contributed <7% of the total uptake. This trophic plasticity may represent an advantage for the species because it attenuates the effects of

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seasonal fluctuations in the planktonic community. Moreover, the water transport rates of 63 ml gÐ1 minÐ1 and the high clearance rates for particles measuring 4 µm or less observed in D. avara (Turon et al. 1997) point to a significant grazing impact of sponges on the picoplankton in communities like the coralligenous, where D. avara and other massive sponges are abundant (Laubier 1966; Bibiloni et al. 1984).

Hydrozoa The hydrozoan Orthopyxis crenata, a common hydroid growing on the alga Halimeda tuna, was most abundant from November to April, when three cohorts were identified (Llobet et al. 1991b). During the rest of the year only two cohorts were identifiable, except in June and July when there was only one (juvenile) cohort. Reproduction took place from late October to early December, with recruitment occurring at the same time. In winter, colony sizes quintupled and tripled every 15 days, living a maximum of 6 wk. The maximum abundance of hydroids in winter seems to be related to increased food availability, a decrease in competence by epiphytic algae and a decline in the turnover rate of Halimeda (Ballesteros 1991c). The strategy of Orthopyxis crenata and other hydroids is completely different to that of long-living anthozoans that are also common in coralligenous communities; the colonies survive for only a small number of weeks but asexual reproduction by the creeping stolons ensures colony survival beyond the life of Halimeda thalli, and perhaps indefinitely. Coma et al. (1992) studied the life cycle of two similar species of hydrozoans living over the thalli of H. tuna and also found that survival should be very long for each colony, due to the active asexual reproduction (by stolonisation in Halecium petrosum; by planktonic propagules in H. pusillum) that occurs throughout most of the year. Maximum life span of colonies was estimated to be only 8 wk, mean colony sizes increasing between three- and six-fold over consecutive 2-wk periods.

Corallium rubrum Red coral (Corallium rubrum) is typically associated with the animal dominated communities growing in dim light conditions and which characterize smaller cavities, vertical cliffs and overhangs present in coralligenous concretions. Although it is predominantly found in the western basin, it is also present in some areas of the eastern basin and the African-Atlantic coast (Zibrowius et al. 1984, Chintiroglou et al. 1989). Harvesting is the major source of disturbance in red coral populations (Santangelo et al. 1993, Santangelo & Abbiati 2001), although large-scale mortalities have also been documented (Arnoux et al. 1992, Garrabou et al. 2001). Recreational diving seems to have a limited impact on populations but the potential risks of poaching and mechanical disturbance will increase in the near future with the predictable increase of diving (Garrabou & Harmelin 2002). According to Garrabou & Harmelin (2002), red coral has a high survivorship, with 60% of colonies reaching 22 years of age. Mortality is higher in juveniles, but partial mortality of colonies is higher in old colonies (Garrabou & Harmelin 2002). Age at first reproduction is, on average, between 7 and 10 yr, although the reproductive effort, i.e., the percentage of gravid polyps per colony, is higher in older colonies (Torrents et al. 2005). Male gonads develop within 1 yr, whereas the maturation of female gonads takes 2 yr (Vighi 1972). Planulae emission seems to be related to water temperature and lasts from MayÐOctober, according to each geographical area (Lacaze- Duthiers 1864, Lo Bianco 1909, Cerruti 1921, Vighi 1972, Santangelo et al. 2003). There is indirect

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evidence to suggest that the larval dispersal capability of red coral is reduced (Weinberg 1979, Abbiati et al. 1993), and it seems that genetic exchange between populations is also limited, promoting the presence of several discrete and distinct populations in the Mediterranean (Abbiati et al. 1993). Recruitment, when studied in experimental panels, is usually high at the beginning, subse- quently decreasing (Garrabou & Harmelin 2002, Bramanti et al. 2005). However, differences in the results obtained by Garrabou & Harmelin (2002) and Bramanti et al. (2005) suggest there is high population variability in recruitment and colonization rates. Growth rates for red coral estimated by petrographic methods range from 1.57Ð0.91 mm yrÐ1 for basal diameter (García-Rodríguez & Massó 1986, Abbiati et al. 1992), but estimates decrease to 0.62 mm yrÐ1 in mid-term (4 yr) observations (Cerrano et al. 1999, Bramanti et al. 2005) and to 0.24 mm yrÐ1 in long-term (22 yr) studies (Garrabou & Harmelin 2002). A new technique for aging red coral developed by Marschal et al. (2005) suggests mean growth rates of around 0.35 mm yrÐ1, in close agreement with long-term observations. Growth rates in colony height have been estimated to be around 1.8 mm yrÐ1 (Garrabou & Harmelin 2002, Bramanti et al. 2005). The average branching rate for each colony is 3.4 branches in 22 yr (Garrabou & Harmelin 2002). Harvested populations show about two-fold lower values on average, and up to four-fold lower values in colony size compared with nonharvested populations. Garrabou & Harmelin (2002) provide indisputable data on the longevity of colonies and the parsimonious population dynamics of C. rubrum. Current populations have shown a dramatic shift in their size structure, characterized by the absence of large colonies (Figure 22). Full recovery of shallow-water harvested populations may take several decades or even centuries (Garrabou & Harmelin, 2002). No sign of predation has been observed in monitored colonies of C. rubrum (Garrabou & Harmelin 2002). In fact, predation appears to play a minor role in sessile, invertebrate-dominated communities as a whole (Garrabou et al. 2002).

Figure 22 (See also Colour Figure 22 in the insert.) A red coral colony (age unknown) from a pristine site (Cap Creus, 35 m) collected in 1962 (A), and a 28-year-old colony from an experimental panel (Riou Caramassaigne, 62 m) (B). (Photo and data courtesy of J.G. Harmelin.)

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60 1400 50 1200 40 1000 30 800 600 20 400 10 200 otal length (cm) T 0 0

Maximum height (cm) Maximum 151015 20 25 30 35 Age (years)

Figure 23 Predicted size of colonies using size-specific growth rates in the gorgonian Paramuricea clavata from coralligenous walls in the Medes Islands (NE Spain). Continuous line: maximum colony height; dashed line: total length. (From Coma et al. 1998b. With permission from Elsevier.)

Gorgonia Growth of Paramuricea clavata has been monitored photographically over a 2-yr period (Coma et al. 1998b). Based on growth-rate data, the largest colonies in the population (55 cm) were around 31 years old (Figure 23). On average, net production for all colonies was 75% of gross production. Gross production was 4.4 g ash free dry weight (afdw) mÐ2 yrÐ1, while the P/B value was 0.11 yrÐ1 and the turnover time was 9 yr (Coma et al. 1998a,b). Mistri & Ceccherelli (1994), in a study of P. clavata in the Straits of Messina (Italy), estimated a production of 3 g afdw mÐ2 yrÐ1, a P/B value of 0.13 yrÐ1 and a turnover rate of 7.5 yr. In Eunicella cavolinii, Weinbauer & Velimirov (1995a,b) have estimated a production of 0.3Ð7.4 g afdw mÐ2 yrÐ1, a P/B around 0.24 and 0.32 yrÐ1, and a turnover rate ranging from 3Ð4 years. Mean increase in maximum height for Paramuricea clavata ranges from 1.8Ð2.7 cm yrÐ1 (Weinberg & Weinberg 1979, Mistri & Ceccherelli 1994, Coma et al. 1998a). Similar values have been obtained for Eunicella singularis (2.2 cm yrÐ1; Weinberg & Weinberg 1979). Growth is lower in E. cavolinii (0.85Ð1.14 cm yrÐ1; Velimirov 1975, Weinbauer & Velimirov 1995a). Seasonality of growth in Paramuricea clavata requires long monitoring periods in order to be accurately detected, but available data suggest there is a high growth period in spring (Figure 24), this being consistent with the seasonal fluctuation in food sources (Coma et al. 1998b). The minimum age at first reproduction in P. clavata has been estimated to be around 7Ð13 yr on average (Coma et al. 1995a). Fecundity levels increase with colony size. Oogenesis in P. clavata lasts for 13Ð18 months and culminates with the release of mature eggs in JuneÐJuly; reproduction is synchronous each year and, as well as coinciding with increasing water temperature, it is correlated with the lunar cycle (Coma et al. 1995a). Spawned eggs adhere to the outer surfaces of female colonies through the action of a mucous coating. Embryogeny and final maturation takes place among the polyps. On leaving the surface of the colonies, larvae immediately settle on the surrounding substratum. Maintenance of the population is based on sexual reproduction (Coma et al. 1995b). Zooplankton (nauplii, copepod eggs, other invertebrate eggs, calanoid copepods) accounts for an important share of the diet. Peak prey capture levels are recorded in spring and at the end of autumn; they fall off substantially in summer, when the proportion of colonies with contracted polyps is very high. The prey capture rate extrapolated to an annual cycle suggests that gorgonians play an important role in the flow of energy from plankton to the benthos; estimates from P. clavata populations situated in the Medes Islands indicate that this species can remove the equivalent of between 12 and 85 mg C mÐ2 dayÐ1 from the zooplankton (Coma et al. 1994).

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5 )

-1 4

3

2

1 Gross growth (cm month Gross growth

0 S0NDJFMAMJJAS0NDJ FMAMJ J AS 0N 1990 1991 1992 Time

Figure 24 Available data on growth of the gorgonian Paramuricea clavata suggests a period of high growth during spring. Error bars show standard error. (From Coma et al. 1998b. With permission from Elsevier.)

However, P. clavata has a broad and heterogenous diet that ranges from nano-eukaryotes (3.8 µm) to copepods (700 µm), and includes prey as diverse as ciliates, dinoflagellates, diatoms and suspended detrital organic matter (Ribes et al. 1999c). Carbon of detrital origin accounts for roughly 48% of the total ingested carbon and shows a marked seasonal pattern, in which winter and spring are the seasons with the highest ingestion rates. The amount of carbon removed from the surrounding water is equivalent to 2.7 mg C mÐ2 dayÐ1 from the living POC (including nano- eukaryotes, diatoms, ciliates and dinoflagellates) and 28.7 mg C mÐ2 dayÐ1 from the detrital POC. No significant capture of dissolved organic matter or picoplankton has been observed. Ribes et al. (1999c) give an estimate of the partitioning of food sources that cover the energy needs of P. clavata, assuming data on ingestion rates observed in incubation chambers corrected by the effect of flow speed obtained from the literature. According to these authors, zooplankton and detrital POC make a similar contribution (about 48% each), with the living POC accounting for the remaining 4%, a figure that can probably be extrapolated to other gorgonians.

Alcyonaria The alcyonarian Alcyonium acaule has a very slow growth, which is almost undetectable over a 2-yr period (Garrabou 1999). Recruitment is very low and occurs in autumn, this being the only method of population maintenance because there is no asexual reproduction. Mortality rates average 12.7% yrÐ1, with much higher mortalities in small colonies. Contracted colonies are much more frequent in summer than in any other season (up to 80%) (Garrabou 1999, Rossi 2001). Colonies of A. acaule are usually aggregated due to the retention of eggs by the mucous strings, implying a short-range dispersal for larvae and settlement near the parental colonies (Garrabou 1999).

Zoantharia Growth and occupation of space of Parazoanthus axinellae in the coralligenous communities of the Medes Islands (northwestern Mediterranean) have been studied by Garrabou (1999). It has moderate growth dynamics (relative growth rate of 0.11 monthÐ1 and a shrinkage rate of 0.09 monthÐ1) with nonsignificant differences over time, although growth rates peak during the summer to autumn period. Fission is common, 29% of monitored colonies undergoing at least one fission

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in 2 yr. Fusion was less frequent, with only 8% of colonies undergoing fusion in 2 yr. Mortality rates average 9% yrÐ1. The occupation of space in P. axinellae seems to be based on spreading over the substrata at moderate rates, either by somatic growth or by fission. Most of the colonies (60%) were contracted in summer and mid autumn (Garrabou 1999, Rossi 2001).

Tunicata Colonies of Cystodites dellechiajei, a very common ascidian in coralligenous communities (Ramos 1991), exhibited no or only restricted growth over a 2-yr period in a vertical wall at a depth of 10Ð12 m in the northwestern Mediterranean (Turon & Becerro 1992), although one of eleven colonies was able to grow actively. According to the authors’ observations, only the individuals present in the most shaded microenvironments displayed active growth. Gonads were present in the population for most of the year. This species shows a high relative biomass per unit area, low growth rates, high survival values (Turon & Becerro 1992) and the presence of chemical defences (Uriz et al. 1991), which would seem to indicate a very conservative life strategy. Two solitary ascidian species common in coralligenous assemblages spawn in late summer and early autumn. Gamete release occurred after the period of highest temperature (SeptemberÐOctober) in Halocynthia papillosa, while for Microcosmus sabatieri it occurred in OctoberÐNovember (Becerro & Turon 1992). In order to explain the surprising fact of spawning after summer, a period of temperature and food limitation, Ribes et al. (1998) studied the natural diet and prey capture of the ascidian Halocynthia papillosa across an annual cycle. The natural diet included detrital organic matter, bacteria, Prochlorococcus and Synechococcus, protozoans and phytoplankton, with a mean size ranging from <1 µm–70 µm. One specimen of Halocynthia papillosa weighing 0.25 g afdw was estimated to ingest an annual mean of 1305 µg C g afdwÐ1 hÐ1. Carbon from detrital origin accounted for 92% of the total ingested carbon, while live carbon accounted for only 8%. Ingestion rates showed a marked seasonal pattern, with the highest ingestion of detrital particles in spring and the highest values of ingestion of live particles in summer and autumn. Ribes et al. (1998) hypothesise that live particles are of more significance in the species’ diet than are particles of detrital origin, because the seasonal variation of ingested nitrogen from live particles explained 91% of the gonadal development variance for the year. Thus, living sestonic organisms, rather than detrital carbon, may be an essential source of nitrogen and other nutrients necessary for growth and reproduction in H. papillosa.

Disturbances Large-scale events Several episodes of suspension feeder mortality have been detected in the northwestern Mediter- ranean (Rivoire 1991, Bavestrello et al. 1994, Cerrano et al. 2000, Perez et al. 2000, Garrabou et al. 2001). Here the existing data on the last large-scale mortality of suspension feeders that affected shallow water assemblages (10Ð40 m depth) eastwards from Marseilles and in some other areas of the central-western Mediterranean (Minorca; Ballesteros, unpublished data) is reported (Figure 25A,B). Owing to climatic and hydrographic anomalies in the Ligurian Sea, the characteristic summer conditions of reduced resources, high water column stability and high temperatures (normally during July and August) lasted much longer than usual in the summer of 1999. This coincided with a mass mortality of benthic suspension feeders over several hundred kilometres, affecting corallig- enous communities situated at a depth of <40 m (Figure 26), where the temperature anomaly lasted for over a month (Perez et al. 2000, Romano et al. 2000). The accumulated density decrease in

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Figure 25 (See also Colour Figure 25 in the insert.) Disturbances in coralligenous communities. (A) Mortality affecting the gorgonian Paramuricea clavata (Port-Cros, France, autumn 1999); (B) Dense carpets of alien alga Womersleyella setacea cover coralligenous assemblages; the gorgonian Eunicella singularis is also affected by previous partial mortality that occurred in summer 1999 (Minorca, Balearic Islands, summer 2000); (C) Filamentous alien alga Womersleyella setacea invades coralligenous rims dominated by Mesophyllum alternans in Cabrera (Balearic Islands, autumn 1999); (D) Partial mortality and overgrowth by filamentous algae affecting gorgonian Eunicella singularis (Minorca, Balearic Islands, summer 2000). (Photos by the author.)

Paramuricea clavata colonies 4 yr after the mass mortality accounts for around half the initial population at the Port-Cros National Park (France) (Linares et al. 2005). Red coral populations thriving above a depth of 30 m were also affected (Garrabou et al. 2001). This large-scale mortality, together with other small-scale mass mortalities (Cerrano et al. 2000) recorded during the past decade in the Mediterranean, may be related to seawater temperature increase and global warming. Some suspension feeders might be able to withstand the normal duration of adverse summer conditions but not an anomalous prolongation of these conditions (Coma et al. 2000; Coma & Ribes 2003), resulting from an energy shortage of suspension feeders related to low food availability in summer. If mass mortalities are indeed related to the global warming trend, such events might occur again and become more frequent, which would cause profound changes in the specific composition and structure of coralligenous communities. In fact, P. clavata, the suspension feeder most drasti- cally affected in the summer 1999 mortality (Perez et al. 2000), is completely absent above a depth

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100 Transect 1 Transect 2 80 Transect 3

60

40

Extent of injury (%) 20

0 15 20 25 30 35 40 45 50 Depth (m)

Figure 26 Extent of injury (mean ± SE) of Paramuricea clavata colonies along three depth transects in the summer 1999 mortality at La Gabinière (Port-Cros, France, autumn 1999). (Unpublished data, courtesy of C. Linares, R. Coma, D. Diaz, M. Zabala, B. Hereu and L. Dantart.)

of 40 m in the warm central Mediterranean waters of the Balearic Islands (Ballesteros, unpublished data), and this may be related to the longer duration of summer conditions in this area. However, the ultimate cause of these mortalities remains unclear, because the temperature anomaly can only have caused physiological stress which, in turn, has triggered the development of some pathogenic agent that would otherwise have remained nonvirulent.

Degradation by waste water Hong (1980) studied the effects of waste water along three stations situated in a gradient of multisource pollution in the Gulf of Fos (Marseilles), and in an unpolluted reference zone. Bio- diversity decreased from the reference station (310 species) to the most polluted zone (214 species), and mainly affected bryozoans, crustaceans and echinoderms; molluscs and polychaetes were largely unaffected. The number of individuals also decreased with increased pollution, as did the biomass of sponges and bryozoans, and the diversity of invertebrates. However, the density of sipunculids as well as the relative abundance of species with a wide ecological distribution was enhanced by pollution (Hong 1980, 1983). The abundances of the species responsible for accretion and those living in the coralligenous community decrease with the pollution gradient, both in terms of number and density of individuals. There are few data concerning the impact of various pollutants on the growth of coralline algae (Littler 1976), although it is known that orthophosphate ions inhibit calcification (Simkiss 1964). However, Hong (1980) observed that with increased pollution large thalli of Mesophyllum alternans are replaced by Peyssonneliaceae, which have a much lower building capacity (Sartoretto 1996). Moreover, the species that act as bioeroders are more abundant in the polluted areas (Hong 1980). Thus, all the available evidence suggests that pollution accelerates the destruction of coralligenous assemblages and inhibits building activity. Cormaci et al. (1985) studied the deep water phytobenthic communities developing over coral- ligenous concretions in the Gulf of Augusta, a site that is heavily polluted by both urban and industrial wastewater. Water turbidity seems to be the main factor causing degradation and homogenisation of the phytobenthos. There is a slight decrease in the number of species (26 algal species sampleÐ1) when compared with similar sites and depths of unpolluted areas (30Ð38 algal species sampleÐ1) (Furnari et al. 1977, Battiato et al. 1979).

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Degradation by fishing Trawling is probably the most destructive fishing method and is causing degradation of large areas of coralligenous concretions (Boudouresque et al. 1990). Trawling not only causes direct physical damage by breaking down the coralligenous structure and rolling the coralligenous blocks but also negatively affects photosynthetic production of encrusting and erect algae by increasing turbidity and sedimentation rates when applied to adjacent sedimentary bottoms (Palanques et al. 2001). Special trawling to collect precious red coral with what is known as the ‘Italian Bar’ or ‘St. Andrew Cross’ is highly destructive. Ortiz et al. (1986) reported the capture of up to 50 kg of benthic fauna (mainly gorgonians) in order to collect 15 kg of living red coral in the Alboran Sea. The abovementioned device is so effective at destroying the sea bed that it has also been used for scientific studies of fauna associated with red coral (Templado et al. 1986, Maldonado 1992). Both traditional and recreational fishing also have an effect on coralligenous communities, although they mainly affect the target species. Fishing leads to a significant decrease in mean specific number of fish species, producing changes in the composition of the community (Bell 1983, Garcia-Rubies & Zabala 1990). This effect is due not only to the nearly total absence of some fishes, demonstrated in two species (Epinephelus marginatus and Sciaena umbra) that are extremely vulnerable to spear-fishing, but also to the notable scarcity of other species (Garcia- Rubies 1999). However, depth acts as a protective factor by limiting the effects of fishing, given the inherent difficulty in locating from the surface the coralligenous bottoms that are isolated from the coast (Garcia-Rubies 1999). No cascading effects through overfishing have so far been detected in coralligenous communities, as they have been in shallow rocky bottoms (Sala et al. 1998), although they may well exist because both densities and sizes of fishes and lobsters have been greatly modified over the last 100 yr. Nevertheless, populations of groupers and other vulnerable fishes rapidly recover after fishing is prohibited (Harmelin 1991, Coll et al. 1999, Harmelin & Robert 2001) and readily exhibit normal socio-behavioural patterns and reproductive success (Zabala et al. 1997a,b).

Degradation by the activity of divers The coralligenous community is one of the most popular sites for recreational diving in the Mediterranean (Boudouresque 2004b) due to its great variety of life and great visual appeal (Harmelin 1993). Some studies have detected the direct impact of divers on the largest invertebrates of the coralligenous community. Sala et al. (1996) found that the large and fragile calcareous bryozoan Pentapora fascialis was present at all levels of exposure (from overhangs to epibiotic) in locations where diving was not allowed, whereas colonies were largely restricted to cryptic positions at diving locations in the Medes Islands marine reserve. Density, colony diameter and colony height were also significantly lower at frequented than at unfrequented sites. Densities of colonies of the bryozoan P. fascialis showed a significant decrease (50% in 1 yr) after a diving site was opened in the marine protected area of the Medes Islands (Garrabou et al. 1998). The impact was greater on boulders covered by coralligenous concretions than on vertical walls, probably as a result of the protection provided by the dense canopy of the gorgonian Paramuricea clavata. However, these high levels of recreational scuba diving (e.g., >1000 visits siteÐ1 yrÐ1) also appear to be greatly modifying the natural demographic parameters of P. clavata in the Medes Islands marine reserve and adjacent sites by means of a three-fold increase in adult mortality (Coma et al. 2004). This increase in adult mortality is due to toppling by divers, because annual mortality induced by overgrowth is almost similar in dived and undived sites, whereas annual mortality by toppling in high visitation areas ranges from 4.9Ð6.9% (1.5% in rarely visited sites). Nonintentional breaking of P. clavata has also been reported by Harmelin & Marinopoulos (1994) from the coralligenous

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communities in Port-Cros National Park (France). Anchoring of boats seems also to have a negative impact on coralligenous assemblages, although there are no studies where this has been adequately assessed. Garrabou et al. (1998) conclude that abrasion by divers may affect other organisms of the coralligenous community because it contains many sessile, long-lived organisms with fragile skeletons and slow growth rates that make them very prone to disturbance by toppling. They suggest that diving might lead the coralligenous community to be dominated by erosion-resistant species, such as encrusting and massive organisms, rather than erect, articulate and foliose species. There- fore, human activities may affect the coralligenous community as a whole. Unfortunately, the paucity of data on turnover rates for most organisms thriving on coralligenous assemblages does not allow a quantitative estimate to be made of diver carrying capacity (Sala et al. 1996).

Invasive species Some species introduced into the Mediterranean have become invasive (Boudouresque & Ribera 1994, Boudouresque & Verlaque 2002) and a number of them can thrive in, or are more or less adapted to, the coralligenous habitat. Currently, only introduced algal species are threatening the coralligenous community and then only in some areas of the Mediterranean. Probably the most dangerous alien species for the coralligenous community is the small red alga Womersleyella (Polysiphonia) setacea, which is currently distributed along most of the Mediterranean basin (see Athanasiadis 1997). This species grows abundantly in coralligenous (and other sublittoral) communities (Figure 25C,D), forming a dense carpet, 1Ð2 cm thick, over the encrusting corallines that constitute the concretion (Mesophyllum alternans, Lithophyllum cabiochae, and others) (Ball- esteros 2004). The carpet of Womersleyella setacea undoubtedly decreases light availability to the encrusting corallines (avoiding or reducing photosynthesis and growth of these algae), increases sediment trapping (Airoldi et al. 1995), excludes other macroalgae by overgrowth and pre-emption (Piazzi et al. 2002), and inhibits recruitment of corallines and other algal and animal species inhab- iting the coralligenous community (Ballesteros et al. 1998). This alga is also very successful at establishing itself and persisting from year to year (Airoldi 1998). It therefore may cause enormous damage to the entire coralligenous community. Indeed, the species richness found in sites invaded by W. setacea is lower than that observed in noncolonised sites (Piazzi et al. 2002). Another alien turf alga that is able to grow in deep waters is Acrothamnion preissii which, nevertheless, has been mainly reported from maërl beds (Ferrer et al. 1994) and the rhizomes of the seagrass Posidonia oceanica (Piazzi et al. 1996). Although present in the coralligenous com- munity of the Balearic Islands (Ballesteros, personal observation), it is never dominant in this environment and always grows together with Womersleyella setacea. Caulerpa taxifolia is another species that can threaten the coralligenous community. Although mainly found in relatively shallow waters (Meinesz & Hesse 1991), it has been recorded down to a depth of 99 m (Belsher & Meinesz 1995) and in some areas, such as Cap Martin (France), it has totally invaded the coralligenous community (Meinesz 1999). C. racemosa var. cylindracea, another invasive species that is quickly spreading in the Mediterranean (Piazzi et al. 2005), is also able to grow in deep waters where coralligenous assemblages develop (down to a depth of 55 m in the Balearic Islands; Ballesteros 2004) but no information about its impact on the coralligenous community is available. Two other species that have been reported to act as invaders in the Mediterranean are Aspar- agopsis taxiformis (Ballesteros & Rodríguez-Prieto 1996) and Lophocladia lallemandii (Patzner 1998). These two species are becoming increasingly abundant both in shallow bottoms and deep waters around the Balearic Islands. They have been found to a depth of 65 m on coralligenous bottoms with or without Womersleyella setacea (Ballesteros, personal observation).

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Conclusions regarding current knowledge of coralligenous communities The coralligenous habitat, as described here, is a typical Mediterranean underwater landscape that basically comprises coralline algae growing in dim light conditions and in relatively calm waters. Although it usually develops in the circalittoral zone it can also thrive in the lower infralittoral zone if irradiance levels are low enough to allow the growth of the encrusting corallines. Most of the available data come from studies conducted in the western Mediterranean. Almost nothing is known about eastern Mediterranean coralligenous habitats, and this may be related to both the greater depth where the coralligenous habitat develops in this area (usually beyond the normal limit of scientific scuba diving) and to the lack of traditional marine research institutes. The main distribution of coralligenous communities has been well documented on a large scale: it is common all around the Mediterranean coasts, with the possible exception of those of Lebanon and Israel. Knowledge about environmental factors is rather poor because the coralligenous habitat is a highly heterogenous system and environmental variables can differ greatly on both a geographical and a microscale. However, even though more data are necessary, basic knowledge of light (irra- diance), temperatures, nutrient concentrations and hydrodynamism is available. Irradiance seems to be the most critical factor for the development of coralligenous frameworks. Available data suggest that light levels must range between 1.3 MJ mÐ2 yrÐ1 and 50Ð100 MJ mÐ2 yrÐ1, that is, between 0.05% and 3% of the surface irradiance. Two main morphologies can be distinguished: banks, which are built over more or less hori- zontal substrata, and rims, which develop in the outer parts of marine caves and vertical cliffs. The coralligenous habitat includes several assemblages due to its great heterogeneity. Algal assemblages develop in open waters and are dominated by several species of encrusting red algae. Mesophyllum alternans dominates in relatively shallow waters while Lithophyllum frondosum, L. cabiochae and Neogoniolithon mamillosum are more abundant in deep waters. Two main algal assemblages have been distinguished. Shallow-water assemblages are rich in species of green algae, while deep-water assemblages have a poorer algal flora, with some encrusting and foliaceous red algae. Animal assemblages differ greatly among sites and geographical areas. In open areas, mixed with algae, cnidarians dominate the assemblage (mainly gorgonians) in relatively eutrophic areas, while in more oligotrophic waters sponges and bryozoans dominate. On overhangs and in large cavities the communities of suspension feeders are dominated by anthozoans, sponges and bryo- zoans. Some research has studied algal and animal builders, as well as bioeroders. However, biomass data for the species composing the assemblages are very scarce. A considerable amount of research has been done on the biodiversity of coralligenous frame- works. Much more data could probably be gathered by taking into account floristic and faunistic studies, as well as monographs from the different groups that contain comments on the ecological distribution of species. A first estimate on the number of species thriving in coralligenous commu- nities is around 1666 (315 algae, 1241 invertebrates and 110 fishes). Studies dealing with the coralligenous communities of certain areas give the number of species as ranging between 500 and 700 species of marine invertebrates. Also important is the very high density of vagile fauna that inhabit coralligenous outcrops, which can reach >3 invertebrates gÐ1 of coralligenous concretion and, for example, a density of >1 polychaete worm cmÐ2. Some endangered Mediterranean species live in the coralligenous habitat, although none is exclusive to this environment. As its diversity is so great, the coralligenous habitat reveals an intense connectivity among its inhabitants. Space competition is strong because the space is completely saturated by organisms, and epibiosis is extremely frequent. Alellochemicals must play an important role in space competition

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because coralligenous communities exhibit a very high percentage of chemically active species. Trophic relationships are also strong in coralligenous communities, particularly among vagile species because most of the sessile invertebrates have skeletons that deter feeding. Several examples of mutualism, commensalism and parasitism have been reported. Growth of coralligenous accretions, carbonate production, and bioerosion and sedimentation rates have merited very few studies, although those published have presented very valuable data. They indicate (1) very low accumulation rates which are related to water depth and light availability; (2) the important source of carbonate for the continental shelf represented by coralligenous buildups; (3) relatively low bioerosion rates, at least in deep waters where algal growth is the lowest; and (4) relatively high sedimentation rates. Accretion rates of up to 0.83 mm yrÐ1, carbonate production Ð2 Ð1 (vegetal and animal) of up to 1000 g CaCO3 m yr , and values for bioerosion of up to 220 g Ð2 Ð1 CaCO3 m year have been reported. These values are always higher in shallow than in deep waters. Large animals and plants of coralligenous assemblages are highly persistent, and show low to nil seasonality in terms of space occupation. Most of the area covered by a coralligenous community remains unchanged after, for example, 2 yr of monitoring. However, growth pulses have been detected in some organisms such as the green alga Halimeda tuna or its epiphytic hydrozoans. Vagile invertebrates and the fish fauna also show a degree of seasonality, mainly due to recruitment pulses and inactivity in winter. Several suspension feeders also exhibit some physiological season- ality, with decreased activity in summer, probably related to the low food availability and high temperatures that occur during this season. Some species inhabiting coralligenous assemblages (algae Mesophyllum alternans, Lithophyl- lum frondosum and Halimeda tuna; sponges Hemimycale columella, Crambe crambe, Chondrosia reniformis, Dysidea avara and Oscarella lobularis; hydrozoans Orthopyxis crenata, Halecium petrosum and H. pusillum; anthozoans Paramuricea clavata, Eunicella cavolinii, E. singularis, Corallium rubrum, Alcyonium acaule, Parazoanthus axinellae; tunicates Halocynthia papillosa, Cystodytes dellechiajei and Microcosmus sabatieri) have been carefully studied in order to deter- mine one or several of the following features: growth rates, population dynamics, age, carbonate production, natural diets, prey capture, reproduction, spawning and recruitment patterns. Five main causes of disturbance that affect coralligenous assemblages have been distinguished:

1. Large-scale events, involving mass mortalities of suspension feeders, seem to be related to summer high water column stability and high temperatures but their ultimate causes remain unclear. It has been suggested that they are related to the current global warming trend. 2. Waste waters profoundly affect the structure of coralligenous communities by inhibiting coralline algal growth, increasing bioerosion rates, decreasing species richness and den- sities of the largest individuals of the epifauna, eliminating some taxonomical groups (e.g., most echinoderms, bryozoans and crustaceans), and increasing the abundance of highly tolerant species. 3. Fishing is another cause of coralligenous degradation. Trawling is especially destructive, for not only does it physically destroy the coralligenous structure but it also increases turbidity and sedimentation rates, which negatively affects algal growth and suspension feeding. Traditional, as well as recreational, fishing mainly affect target species, although most of them rapidly recover after fishing prohibition or after implementation of scien- tifically guided fisheries management. However, this is not the case for the long-lived and slow-growing red coral, whose full recovery from harvesting has been estimated to take several decades or even centuries.

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4. Diver activity is another cause of recent degradation of coralligenous assemblages, although this kind of disturbance only affects, at the moment, very few areas situated at the most popular sites for recreational diving. 5. Finally, invasive alien species are another cause of concern because their numbers are increasing throughout the Mediterranean. Especially dangerous for the coralligenous communities is the red turf alga Womersleyella setacea, which forms a dense carpet over encrusting corallines, thus inhibiting photosynthesis and growth of the main coralligenous builders.

Actions Gaps in scientific knowledge In terms of the current state of scientific knowledge of the coralligenous habitat it is easy to detect several gaps that make it rather difficult to make recommendations for protecting coralligenous assemblages: 1. There is a complete lack of knowledge of the distribution of coralligenous substrata in the Mediterranean, with the exception of some extremely limited areas situated mainly in marine parks or reserves. As a minimum, approximate cartography and quantification of these bottoms is required. 2. It is highly recommended that a list of all the organisms that have been found living in coralligenous communities be drawn up, in order to have a precise idea of the amount of biodiversity contained in this environment. 3. Almost nothing is known about the coralligenous concretions from the eastern Mediter- ranean. Special efforts must be made to investigate the description and functioning of coralligenous communities in this area. 4. Further studies dealing with the processes involved in the buildup and erosion of coral- ligenous assemblages must be conducted because almost all the existing information comes from one or two localities situated in the northwestern Mediterranean. 5. An understanding of the functioning of the dominant and keystone species is essential in order to implement an adequate management strategy for the coralligenous habitat. 6. The effect of disturbances in coralligenous assemblages is poorly understood, and there are no data at all on the capacity of this environment to recover (with the exception of fish stocks after fishing prohibition). The following issues would appear to be particularly important: a. Indirect impact of trawling b. Impact of waste-water dumping c. Effects of alien species invasion d. Causes of recent large-scale mortality events

Recommendations for protecting coralligenous communities In the light of current knowledge, there are a number of recommendations that can be made in order to conserve (or even improve) coralligenous environments. Most of these recommendations concern not only the coralligenous habitat but most of the coastal benthic habitats because waste- water dumping, trawling and overfishing, and invasion by alien species are problems that affect the whole of the coastal area. Measures to reduce these impacts may improve the overall quality

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of the marine coastal environment. Specific measures aimed at protecting the coralligenous envi- ronment might include the following:

1. Waste-water dumping should be banned over coralligenous bottoms, and in their vicinity. 2. Trawling must be completely prohibited in areas with coralligenous outcrops and their vicinity, the aim being to avoid not only the physical damage caused by trawling over coralligenous assemblages but also the indirect effects due to increased turbidity and silting. 3. Any other anthropogenic activity involving an increase in water turbidity and/or sediment removal (e.g., coastline modification, beach regeneration) should be avoided in the vicinity of coralligenous outcrops. 4. Correct management of traditional and recreational fisheries must be implemented in order to prevent stock depletion of target fish and crustaceans. 5. The impact of diving must be compatible with the normal functioning and conservation of the coralligenous environment. 6. The enactment of suitable legislation concerning the introduction of alien species is urgently needed.

Acknowledgements This review was funded by the GEF Strategic Action Plan for the Conservation of Biological Diversity (SAP BIO) project, supported by the United Nations Environment Programme — Med- iterranean Action Plan (UNEP-MAP) under the responsibility of the Regional Activity Centre for Specially Protected Areas (RAC/SPA). I am indebted to Drs Joaquim Garrabou, Rafel Coma, Antoni Garcia-Rubies, Daniel Martin, Enrique Macpherson, María Jesús Uriz, Xavier Turon, Mikel Zabala and Jordi Camp for providing ecological and taxonomical advice and bibliography. Jordi Corbera and Mikel Zabala are kindly acknowledged for providing the artwork. I am also grateful to Dr. Marc Verlaque for his advice on coralline algae nomenclature, and to Dr. Jean Georges Harmelin for providing the picture and data for Figure 22.

References

Abbiati, M., Buffoni, G., Caforio, G., Di Cola, G. & Santangelo, G. 1992. Harvesting, predation and compe- tition effects on a red coral population. Netherlands Journal of Sea Research 30, 219Ð228. Abbiati, M., Santangelo, G. & Novelli, S. 1993. Genetic variation within and between two Thyrrenian populations of the Mediterranean alcyonarian Corallium rubrum. Marine Ecology Progress Series 95, 245Ð250. Acunto, S., Balata, D. & Cinelli, F. 2001. Variabilità spaziale del coralligeno e considerazione sul metodo di campionamento. Biologia Marina Mediterranea 8, 191Ð200. Adey, W.H. 1978. Coral reef morphogenesis: a multidimensional model. Science 202, 831Ð837. Adey, W.H. 1998. Coral reefs: algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. Journal of Phycology 34, 393Ð406. Adey, W.H. & McIntyre, I.G. 1973. Crustose coralline algae: a re-evaluation in the geological sciences. Geological Society of America Bulletin 84, 883Ð904. Adey, W.H. & Vassar, J.M. 1975. Colonization, succession and growth rates of tropical crustose coralline algae (Rhodophyta, Cryptonemiales). Phycologia 14, 55Ð69. Airoldi, L. 1998. Roles of disturbance, sediment stress, and substratum retention on spatial dominance in algal turf. Ecology 79, 2759Ð2770.

182 7044_C004.fm Page 183 Monday, April 17, 2006 1:38 PM

MEDITERRANEAN CORALLIGENOUS ASSEMBLAGES

Airoldi, L., Rindi, F. & Cinelli, F. 1995. Structure, seasonal dynamics and reproductive phenology of a filamentous turf assemblage on a sediment influenced, rocky subtidal shore. Botanica Marina 38, 227Ð237. Arnoux, A., Harmelin, J.G., Monod, J.L., Romaña, L.A. & Zibrowius, H. 1992. Altérations des peuplements benthiques de roches profondes en Méditerranée nord-occidentale: quelques aspects biologiques et molysmologiques. Comptes Rendus de l’Académie des Sciences de Paris Series III 314, 219Ð225. Athanasiadis, A. 1987. A Survey of the Seaweeds of the Aegean Sea with Taxonomic Studies on Species of the Tribe Antithamniae (Rhodophyta). Kungälv: Göterna. Athanasiadis, A. 1997. North Aegean marine algae. IV. Womersleyella setacea (Hollenberg) R.E. Norris (Rhodophyta, Ceramiales). Botanica Marina 40, 473Ð476. Athanasiadis, A. 1999a. The taxonomic status of Lithophyllum stictaeforme (Rhodophyta, Corallinales) and its generic position in light of phylogenetic considerations. Nordic Journal of Botany 19, 735Ð745. Athanasiadis, A. 1999b. Mesophyllum macedonis, nov. sp. (Rhodophyta, Corallinales), a putative Tethyan relic in the North Aegean Sea. European Journal of Phycology 34, 239Ð252. Augier, H. & Boudouresque, C.F. 1975. Dix ans de recherches dans la zone marine du Parc National de Port- Cros (France). Troisième partie. Annales de la Societé des Sciences Naturelles et d’Archéologie de Toulon et du Var 27, 131Ð170. Augier, H., Boudouresque, C.F. & Laborel, J. 1971. Végétation marine de l’île de Port-Cros (Parc National). VII. — Les peuplements sciaphiles profonds sur substrat dur. Bulletin du Muséum d‘Histoire Naturelle de Marseille 20, 149Ð168. Bacci, G. 1947. Ricerche sulle zoocenosi bentoniche del Golfo di Napoli, I. La secca di Benda Palumno. Pubblicazioni della Stazione Zoologica di Napoli 20, 158Ð178. Bacescu, M. 1971. Les spongiaires: un des plus intéressants biotopes benthiques marins. Rapports et Procès- Verbaux des Réunions de la Comission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 20, 239Ð241. Ballesteros, E. 1990. Structure and dynamics of the community of Cystoseira zosteroides (Turner) C. Agardh (Fucales, Phaeophyceae) in the northwestern Mediterranean. Scientia Marina 54, 217Ð229. Ballesteros, E. 1991a. Structure and dynamics of north-western Mediterranean marine communities: a con- ceptual model. Oecologia Aquatica 10, 223Ð242. Ballesteros, E. 1991b. Structure of a deep-water community of Halimeda tuna (Chlorophyceae, Caulerpales) from the northwestern Mediterranean. Collectanea Botanica 20, 5Ð21. Ballesteros, E. 1991c. Seasonality of growth and production of a deep-water population of Halimeda tuna (Chlorophyceae, Caulerpales) in the north-western Mediterranean. Botanica Marina 34, 291Ð301. Ballesteros, E. 1992. Els vegetals i la zonació litoral: espècies, comunitats i factors que influeixen en la seva distribució. Arxius Secció Ciències 101, 1–616. Barcelona: Institut d’Estudis Catalans. Ballesteros, E. 1993. Algues bentòniques i fanerògames marines. In Història Natural de l’Arxipèlag de Cabrera, J.A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 503Ð530. Ballesteros, E. 1998. Addicions a la fauna d’invertebrats bentònics de l’arxipèlag de Cabrera (Illes Balears, Mediterrània Occidental). Bolletí de la Societat d’Història Natural de les Balears 41, 41Ð48. Ballesteros, E. 2004. Espècies marines invasores: un problema ambiental emergent a les Illes Balears. In IV Jornades de Medi Ambient de les illes Balears. Ponències i Resums, G.X. Pons (ed.). Palma de Mallorca: Societat Història Natural Balears, 13–15. Ballesteros, E. & Rodríguez-Prieto, C. 1996. Presència d’Asparagopsis taxiformis (Delile) Trevisan a Balears. Bolletí de la Societat d’Història Natural de les Balears 39, 135Ð138. Ballesteros, E., Sala, E., Garrabou, J. & Zabala, M. 1998. Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the northwestern Mediterranean. European Journal of Phycology 33, 121Ð128. Ballesteros, E. & Tomas, F. 1999. Avaluació de l’estat de les comunitats bentòniques de La Roja (Tossa de Mar, Girona) en vistes a la seva declaració com a reserva marina. Blanes: Centre d’Estudis Avançats de Blanes — CSIC.

183 7044_C004.fm Page 184 Monday, April 17, 2006 1:38 PM

ENRIC BALLESTEROS

Ballesteros, E. & Zabala, M. 1993. El bentos: el marc físic. In Història Natural de l’Arxipèlag de Cabrera, J.A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 663Ð685. Ballesteros, E., Zabala, M., Uriz, M. J., Garcia-Rubies, A. & Turon, X. 1993. El bentos: les comunitats. In Història Natural de l’Arxipèlag de Cabrera, J.A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 687Ð730. Basso, D. & Tomaselli, V. 1994. Palaeoecological potentiality of rhodoliths: a Mediterranean case history. Bollettino della Societè Paleontologica Italiana, Speciale Volume 2, 17Ð27. Battiato, A., Cormaci, M., Furnari, G. & Scamacca, B. 1979. Osservazioni sulla zonazione dei popolamenti fitobentonici di substrato duro della Penisola della Maddalena (Siracusa). Thalassia Salentina 9, 19Ð25. Bavestrello, G., Bertone, S., Cattaneo-Vietti, R., Cerrano, C., Gaino, E. & Zanzi, D. 1994. Mass mortality of Paramuricea clavata (Anthozoa, Cnidaria) on Portofino Promontory cliffs, Ligurian Sea, Mediterra- nean Sea. Marine Life 4, 15Ð19. Becerro, M.A. & Turon, X. 1992. Reproductive cycles of the ascidians Microcosmus sabatieri and Halocynthia papillosa in the northwestern Mediterranean. Pubblicazioni della Stazione Zoologica di Napoli I: Marine Ecology 13, 363Ð373. Bell, J.D. 1983. Effects of depth and marine reserve fishing restrictions on the structure of a rocky fish assemblage in the north-western Mediterranean Sea. Journal of Applied Ecology 20, 357Ð369. Bellan, G. 1964. Contribution à l’étude systématique, bionomique et écologique des annélides polychètes de la Méditerranée. Thèse Doctorat. Faculté Sciences Marseille. Bellan-Santini, D. 1998. Ecology. In The Amphipoda of the Mediterranean, Part 4, S. Ruffo (ed.). Mémoires de l’Institut Océanographique (Monaco) 13, 869Ð894. Belsher, T. & Meinesz, A. 1995. Deep-water dispersal of the tropical alga Caulerpa taxifolia introduced into the Mediterranean. Aquatic Botany 51, 163Ð169. Bibiloni, M.A., Olivella, I. & Ros, J. 1984. Les esponges de les illes Medes. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds). Arxius Secció Ciències 73, Barcelona: Institut d’Estudis Catalans, 383Ð405. Blanc, J.J. & Molinier, R. 1955. Les formations organogènes construites superficielles en Méditerranée occidentale. Bulletin de l’Institut Océanographique (Monaco) 52 (1067), 1Ð26. Boero, F., Balduzzi, A., Bavestrello, G., Caffa, B. & Vieti, R. 1986. Population dynamics of Eudendrium glomeratum (Cnidaria, Anthomedusae) on the Portofino promontory (Ligurian Sea). Marine Biology 92, 81Ð85. Bosence, D.W.J. 1985. The “coralligène” of the Mediterranean — a recent analog for Tertiary coralline algal limestones. In Paleoalgology: Contemporary Research and Applications, D.F. Toomey & M.H. Nicketi (eds), Heidelberg: Springer-Verlag, 216Ð225. Boudouresque, C.F. 1970. Recherches sur bionomie analytique, structurale et expérimentale sur les peuple- ments benthiques sciaphiles en Méditerranée occidentale (fraction algale). Thèse. Université d’Aix- Marseille II. Boudouresque, C.F. 1971. Méthodes d’étude qualitative et quantitative du benthos (en particulier du phyto- benthos). Téthys 3, 79Ð104. Boudouresque, C.F. 1973. Recherches de bionomie analytique, structurale et expérimentale sur les peuplements benthiques sciaphiles de Méditerranée Occidentale (fraction algale). Les peuplements sciaphiles de mode relativement calme sur substrats durs. Bulletin du Muséum d’Histoire Naturelle de Marseille 33, 147Ð225. Boudouresque, C.F. 1980. Phytocénoses benthiques de la Réserve de Scandola. Compte-rendu de la mission rara-avis sur la façade maritime du Parc Naturel Régional de Corse. Marseille: Parc Naturel Régional de la Corse et Laboratoire Biologie Végétale Marine Luminy. Boudouresque, C.F. 1985. Groupes écologiques d’algues marines et phytocenoses benthiques en Méditerranée nord-occidentale: une revue. Giornale Botanico Italiano 118, 7Ð42. Boudouresque, C.F. 2004a. Marine biodiversity in the Mediterranean: status of species, populations and communities. Scientific Reports of Port-Cros National Park 20, 97Ð146.

184 7044_C004.fm Page 185 Monday, April 17, 2006 1:38 PM

MEDITERRANEAN CORALLIGENOUS ASSEMBLAGES

Boudouresque, C.F. 2004b. The erosion of Mediterranean biodiversity. In The Mediterranean Sea: An Overview of Its Present State and Plans for Future Protection. Lectures from the 4th International Summer School on the Environment, C. Rodríguez-Prieto & G. Pardini (eds), Girona: Universitat de Girona, 53Ð112. Boudouresque, C.F., Avon, M. & Gravez, V. (eds). 1991. Les espèces marines à protéger en Méditerranée. Marseille: GIS Posidonie. Boudouresque, C.F. & Cinelli, F. 1976. Le peuplement algal des biotopes sciaphiles superficiels de mode battu en Méditerranée Occidentale. Pubblicazione Stazione Zoologica di Napoli 40, 433Ð459. Boudouresque, C.F. & Denizot, M. 1975. Révision du genre Peyssonnelia (Rhodophyta) en Méditerranée. Bulletin Muséum d’Histoire Naturelle de Marseille 35, 7Ð92. Boudouresque, C.F., Meinesz, A., Ballesteros, E., Ben Maiz, N., Boisset, F., Cinelli, F., Cirik, S., Cormaci, M., Jeudy de Grissac, A., Laborel, J., Lanfranco, E., Lundberg, B., Mayhoub, H., Panayotidis, P., Semroud, R., Sinnassamy, J.M. & Span, A. 1990. Livre Rouge “Gérard Vuignier” des végétaux, peuplements et paysages marins menacés de Méditerranée. MAP Technical Report Series, 43. Athens: UNEP/IUCN/GIS Posidonie, 1Ð250. Boudouresque, C.F. & Ribera, M.A. 1994. Les introductions d’espèces végétales et animales en milieu marin. Conséquences écologiques et économiques et problèmes législatifs. In First International Workshop on Caulerpa taxifolia, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 29Ð102. Boudouresque, C.F. & Verlaque, M. 1978. Végétation marine de la Corse (Méditerranée). I. Documents pour la flore des algues. Botanica Marina 21, 265Ð275. Boudouresque, C.F. & Verlaque, M. 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Marine Pollution Bulletin 44, 32Ð38. Bramanti, L., Magagnini, G., De Maio, L. & Santangelo, G. 2005. Recruitment, early survival and growth of the Mediterranean red coral Corallium rubrum (L. 1758), a 4-year study. Journal of Experimental Marine Biology and Ecology 314, 69Ð78. Bressan, G. & Babbini-Benussi, L. 1996. Phytoceanographical observations on coralline algae (Corallinales) in the Mediterranean Sea. Rendiconti Lincei Scienze Fisiche e Naturali 9, 179Ð207. Cabioch, J. & Mendoza, M.L. 1998. Mesophyllum alternans (Foslie) comb. nov. (Corallinales, Rhodophyta), a mediterraneo-atlantic species, and new considerations on the Lithothamnion philippii Foslie complex. Phycologia 37, 208Ð221. Cabioch, J. & Mendoza, M.L. 2003. Mesophyllum expansum (Philippi) comb. nov. (Corallinales, Rhodophytes), et mise au point sur les Mesophyllum des mers d’Europe. Cahiers Biologie Marine 44, 257Ð273. Canals, M. & Ballesteros, E. 1997. Production of carbonate sediments by phytobenthic communities in the Mallorca-Minorca Shelf, northwestern Mediterranean Sea. Deep-Sea Research II 44, 611Ð629. Canals, M., Ballesteros, E., Serra, J., Alonso, B. & Catafau, E. 1988. The Pollensa Bay carbonate factory (Balearic islands, NW Mediterranean Sea). Rapports et Procès-Verbaux des Réunions Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 31, 298. Carbonell, J. 1984. Crustacis de les illes Medes. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds), Arxius Secció Ciències 73, 505Ð530. Carpine, C. 1964. Contribution à l’étude bionomique de la Méditerranée occidentale (côte du Var et des Alpes- Maritimes, côte occidentale de Corse). (3) La côte de l’Estérel, de la pointe des Lions à la pointe de l’Aiguille (région A2). Bulletin de l’Institut Océanographique (Monaco) 63 (1312), 1Ð52. Cebrian, E., Ballesteros, E. & Canals, M. 2000. Shallow rocky bottom benthic assemblages as calcium carbonate producers in the Alboran Sea (southwestern Mediterranean). Oceanologica Acta 23, 311Ð322. Cerrano, C. Bavestrello, G., Bianchi, C.N., Cattaneo-Vietti, R., Bava, S., Morganti, C., Morri, C., Picco, P., Sara, G., Schiaparelli, S., Siccardi, A. & Sponga, F. 2000. A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (NW Mediterranean), summer 1999. Ecology Letters 3, 284Ð293. Cerrano, C., Bavestrello, G., Cicogna, F. & Cattaneo-Vietti, R. 1999. New experiences on transplantation and red coral harvesting effects in the Ligurian Sea. In Red Coral and Other Mediterranean Octocorals, Biology and Protection, F. Cicogna & R. Cattaneo-Vietti (eds), Roma: Ministerio Politiche e Risorse Agricole Alimentari e Forestali, 62Ð67.

185 7044_C004.fm Page 186 Monday, April 17, 2006 1:38 PM

ENRIC BALLESTEROS

Cerruti, A. 1921. Ulteriori notizie biologiche riguardanti il periodo de imaturità sessuale degli animale del golfo di Napoli. Pubblicazioni della Stazione Zoologica di Napoli 3, 229Ð240. Chauvet, C. 1991. Statut d’Epinephelus guaza (Linnaeus, 1757) et éléments de dynamiques des populations méditerranéenne et atlantique. In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 255Ð275. Chazottes, V., Le Campion-Alsumard, T. & Peyrot-Clausade, M. 1995. Bioerosion rates on coral reefs: interactions between macroborers, microborers and grazers (Moorea, French Polynesia). Paleogeog- raphy Paleoclimatology Paleoecology 113, 189Ð198. Chintiroglou, H., Dounas, C. & Koukouras, A. 1989. The presence of Corallium rubrum (Linnaeus, 1758) in the eastern Mediterranean sea. Mitteilungen aus dem Zoologischen Museum Berlin 65, 145Ð149. Coll, J., Garcia-Rubies, A., Moranta, J., Stefanni, S. & Morales-Nin, B. 1999. Efectes de la prohibició de la pesca esportiva sobre l’estructura poblacional de l’anfós (Epinephelus marginatus Lowe, 1834. Pisces, Serranidae) en el Parc Nacional de Cabrera. Bolletí de la Societat d’Història Natural de les Balears 42, 125Ð138. Coma, R., Gili, J.M., Zabala, M. & Riera, T. 1994. Feeding and prey capture cycles in the aposymbiontic gorgonian Paramuricea clavata. Marine Ecology Progress Series 115, 257Ð270. Coma, R., Llobet, I., Zabala, M., Gili, J.M. & Hughes, R.G. 1992. The population dynamics of Halecium petrosum and Halecium pusillum (Hydrozoa, Cnidaria), epiphytes of Halimeda tuna in the northwest- ern Mediterranean. Scientia Marina 56, 161Ð169. Coma, R., Polà, E., Ribes, M. & Zabala, M. 2004. Long-term assessment of temperate octocoral mortality patterns, protected vs. unprotected areas. Ecological Applications 14, 1466Ð1478. Coma, R. & Ribes, M. 2003. Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization. Oikos 101, 205Ð215. Coma, R., Ribes, M., Gili, J.M. & Zabala, M. 1998a. An energetic approach to the study of life-history traits of two modular colonial benthic invertebrates. Marine Ecology Progress Series 162, 89Ð103. Coma, R., Ribes, M., Gili, J.M. & Zabala, M. 2000. Seasonality in coastal benthic ecosystems. Trends in Ecology and Evolution 15, 448Ð453. Coma, R., Ribes, M., Gili, J. M. & Zabala, M. 2002. Seasonality of in situ respiration rate in three temperate benthic suspension feeders. Limnology and Oceanography 47, 324Ð331. Coma, R., Ribes, M., Zabala, M. & Gili, J.M. 1995a. Reproduction and cycle of gonadal development in the Mediterranean gorgonian Paramuricea clavata. Marine Ecology Progress Series 117, 173Ð183. Coma, R., Ribes, M., Zabala, M. & Gili, J.M. 1998b. Growth in a modular colonial marine invertebrate. Estuarine Coastal and Shelf Science 47, 459Ð470. Coma, R., Zabala, M. & Gili, J M. 1995b. Sexual reproductive effort in the Mediterranean gorgonian Paramuricea clavata. Marine Ecology Progress Series 117, 185Ð192. Coppejans, E. & Hermy, M. 1985. L’épiflore des substrats de l’étage circalittoral dans la baie de Calvi (Corse, Méditerranée). V. Ordination et classification des données. In Progress in Belgian Oceanographic Research: Proceedings of a Symposium held at the Palace of Academies Brussels 3Ð5 March 1985, R. Van Griecken & R. Wollast (eds), Antwerpen: University of Antwerp, 430Ð441. Corbera, J., Ballesteros, E. & Garcia, L. 1993. Els crustacis decàpodes. In Història Natural de l’Arxipèlag de Cabrera, J. A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 579Ð587. Corbera, J., Sabates, A. & Garcia-Rubies, A. 1996. Peces de Mar de la Península Ibérica. Barcelona: Planeta. Cormaci, M., Furnari, G. & Scamacca, B. 1985. Osservazioni sulle fitocenosi bentoniche del golfo di Augusta (Siracusa). Bollettino dell’Accademia Gioenia Scienze Naturalli 18, 851Ð872. Dethier, M.N., Paul, K.M. & Woodbury, M.M. 1991. Distribution and thickness patterns in subtidal encrusting algae from Washington. Botanica Marina 34, 201Ð210. Dring, M.J. 1981. Chromatic adaptation of photosynthesis in benthic marine algae: an examination of its ecological significance using a theoretical model. Limnology and Oceanography 26, 271Ð284. Feldmann, J. 1937. Recherches sur la Végétation Marine de la Méditerranée: la Côte des Albères. Rouen: Wolf. Ferdeghini, F., Acunto, S., Cocito, S. & Cinelli, F. 2000. Variability at different spatial scales of a coralligenous assemblage at Giannutri island (Tuscan Archipelago, northwestern Mediterranean). Hydrobiologia 440, 27Ð36.

186 7044_C004.fm Page 187 Monday, April 17, 2006 1:38 PM

MEDITERRANEAN CORALLIGENOUS ASSEMBLAGES

Ferrer, E., Ribera, M.A. & Gómez-Garreta, A. 1994. The spread of Acrothamnion preissii (Sonder) Wollaston (Rhodophyta, Ceramiaceae) in the Mediterranean Sea: new record from the Balearic islands. Flora Mediterranea 4, 163Ð166. Finckh, A.E. 1904. Biology of the reef-forming organisms at Funafuti Atoll, Part VI. In The Atoll of Funafuti: Borings into a Coral Reef and the Results, Royal Society of London. London: Harrison & Sons, 125Ð150. Foslie, M.H. 1907. The Lithothamnia. In Reports of the Percy Sladen Trust Expedition to the Indian Ocean in 1905, J.S. Gardiner (ed.), Transactions of the Linnean Society of London, Series 2 (Zoology) 12, 177Ð192. Francour, P. 1991. Statut de Centrostephanus longispinus en Méditerranée. In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 187Ð202. Francour, P. 1994. Pluriannual analysis of the reserve effect on ichthyofauna in the Scandola natural reserve (Corsica, Northwestern Mediterranean). Oceanologica Acta 17, 309Ð317. Fredj, G. 1964. Contribution à l’étude bionomique de la Méditerranée Occidentale (côte du Var et des Alpes- Maritimes, côte occidentale de Corse). Fasc. 2. La région de Saint Tropez; du Cap Taillat au Cap de Saint Tropez (région A1). Bulletin de l’Institut Océanographique (Monaco) 63 (1311), 1Ð55. Furnari, G., Cormaci, M. & Alongi, G. 1996. Lithophyllum frondosum (Dufour) comb. nov. (Corallinaceae, Rhodophyta): the species to which Mediterranean “Pseudolithophyllum expansum” should be referred. European Journal of Phycology 31, 117Ð122. Furnari, G., Scamacca, B., Cormaci, M. & Battiato, A. 1977. Zonazione della vegetazione sommersa dell’isola Lachea (Catania). Atti XI Congresso della Società Italiana di Biologia Marina, 245Ð257. Gamulin-Brida, H. 1965. Contribution aux recherches bionomiques sur les fonds coralligènes au large de l’Adriatique moyenne. Rapports et Procés-Verbaux des Réunions Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 18 (2), 69Ð74. Gamulin-Brida, H. 1967. The benthic fauna of the Adriatic Sea. Oceanography and Marine Biology: An Annual Review 5, 535Ð568. García-Raso, J.E. 1988. Consideraciones generales sobre la taxocenosis de crustáceos decápodos de fondos de concrecionamiento calcáreo superficial del alga Mesophyllum lichenoides (Ellis & Sol.) Lemoine (Corallinaceae) del mar de Alborán. Investigación Pesquera 52, 245Ð264. García-Raso, J.E. 1989. Resultados de la segunda campaña del I.E.O. para la exploración de los fondos de coral rojo en el mar de Alborán. Crustáceos decápodos. Boletín Instituto Español de Oceanografía 5, 27Ð36. García-Raso, J.E. & Fernández-Muñoz, R. 1987. Estudio de una comunidad de crustáceos decápodos de fondos “coralígenos” del alga calcárea Mesophyllum lichenoides del sur de España. Investigación Pesquera 51 (Suplemento 1), 301Ð322. García-Raso, J.E., López de la Rosa, I. & Rosales, J.M. 1996. Decapod crustacean communities from calcareous seaweed and Posidonia oceanica (rhizome stratum) in shallow waters. Ophelia 45, 143Ð158. García-Rodríguez, M. & Massó, C. 1986. Estudio biométrico de poblaciones de coral rojo del litoral de Gerona. Boletín Instituto Español de Oceanografía 3, 65Ð74. Garcia-Rubies, A. 1993. Distribució batimètrica dels peixos litorals sobre substrat rocòs a l’illa de Cabrera. In Història Natural de l’Arxipèlag de Cabrera, J.A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 645Ð661. Garcia-Rubies, A. 1997. Estudi ecològic de les poblacions de peixos litorals sobre substrat rocòs a la Mediterrània occidental: efectes de la fondària, el substrat, l’estacionalitat i la protecció. Tesi Doctoral. Universitat de Barcelona. Garcia-Rubies, A. 1999. Effects of fishing on community structure on selected populations of Mediterranean coastal reef fish. Naturalista Siciliano 23, 59Ð81. Garcia-Rubies, A. & Zabala, M. 1990. Effects of total fishing prohibition on the rocky fish assemblages of Medes islands marine reserve. Scientia Marina 54, 317Ð328. Garrabou, J. 1997. Structure and dynamics of north-western Mediterranean rocky benthic communities along a depth gradient: a Geographical Information System (GIS) approach. PhD Thesis. University of Barcelona.

187 7044_C004.fm Page 188 Monday, April 17, 2006 1:38 PM

ENRIC BALLESTEROS

Garrabou, J. 1999. Life history traits of Alcyonium acaule and Parazoanthus axinellae (Cnidaria, Anthozoa), with emphasis on growth. Marine Ecology Progress Series 178, 193Ð204. Garrabou, J. & Ballesteros, E. 2000. Growth of Mesophyllum alternans and Lithophyllum frondosum (Coral- linaceae, Rhodophyta) in the northwestern Mediterranean. European Journal of Phycology 35, 1Ð10. Garrabou, J., Ballesteros, E. & Zabala, M. 2002. Structure and dynamics of north-western Mediterranean benthic communities along a depth gradient. Estuarine Coastal and Shelf Science 55, 493Ð508. Garrabou, J. & Harmelin, J.G. 2002. A 20-year study on life history traits of a harvested long-lived temperate coral in the NW Mediterranean: insights into conservation and management needs. Journal of Animal Ecology 71, 966Ð978. Garrabou, J., Perez, T., Sartoretto, S. & Harmelin, J.G. 2001. Mass mortality event in red coral (Corallium rubrum, Cnidaria, Anthozoa, Octocorallia) population in the Provence region (France, NW Mediter- ranean). Marine Ecology Progress Series 217, 263Ð272. Garrabou, J., Sala, E., Arcas, A. & Zabala, M. 1998. The impact of diving on rocky sublittoral communities: a case study of a bryozoan population. Conservation Biology 12, 302Ð312. Garrabou, J. & Zabala, M. 2001. Growth dynamics in four Mediterranean demosponges. Estuarine Coastal and Shelf Science 52, 293Ð303. Gautier, Y.V. 1962. Recherches écologiques sur les bryozoaires chilostomes en Méditerranée Occidentale. Recueil des Travaux de la Station Marine d’Endoume 24 (38), 1Ð434. Giaccone, G. 1965. Le fitocenosi marine nel settore rosso di Capo Zafferano (Palermo). Lavori Istituto Botanico di Palermo 22, 1Ð69. Giaccone, G. 1967. Popolamenti a Laminaria rodriguezii Bornet sul banco Apollo dell’isola di Ustica (Mar Tirreno). Nova Thalassia 3, 1Ð10. Giaccone, G., Alongi, G., Pizzuto, F. & Cossu, A. 1994. La vegetazione marina bentonica sciafila del Mediterraneo: III. Infralitorale e circalitorale. Proposte di aggiornamento. Bollettino dell’Accademia Gioenia Scienze Naturalli 27, 201Ð227. Giaccone, G. & De Leo, A. 1966. Flora e vegetazione algale del Golfo di Palermo. Lavori Istituto Botanico di Palermo 22, 251Ð317. Gili, J.M. 1986. Estudio sistemático y faunístico de los cnidarios de la costa catalana. Tesis Doctoral. Universidad Autónoma de Barcelona. Gili, J.M. & Ballesteros, E. 1991. Structure of cnidarian populations in Mediterranean sublittoral benthic communities as a result of adaptation to different environmental conditions. Oecologia Aquatica 10, 243Ð254. Gili, J.M., Garcia, A. & Colomer, P. 1984. Els cnidaris bentònics de les illes Medes. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds), Arxius Secció Ciències 73, 407Ð427. Gili, J.M., Murillo, J. & Ros, J. 1989. The distribution pattern of benthic cnidarians in the western Mediter- ranean. Scientia Marina 53, 19Ð35. Gili, J.M. & Ros, J. 1984. L’estatge circalitoral de les illes Medes: el coral·ligen. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds), Arxius Secció Ciències 73, 677Ð705. Gili, J.M. & Ros, J. 1985. Study and cartography of the benthic communities of Medes islands (NE Spain). Pubblicazzioni della Stazione Zoologica di Napoli I: Marine Ecology 6, 219Ð238. Got, H. & Laubier, L. 1968. Prospection sysmique au large des Albères: nature du substrat originel du coralligène. Vie et Milieu 19, 9Ð16. Hamel, G. & Lemoine, P. 1953. Corallinacées de France et d’Afrique du Nord. Archives du Muséum National d’Histoire Naturelle, Paris, 7 série 1, 15Ð136. Harmelin, J.G. 1990. Ichthyofaune des fonds rocheux de Méditerranée: structure du peuplement du coralligène de l’île de Port-Cros (Parc National). Mesogée 50, 23Ð30. Harmelin, J.G. 1991. Statut du corb (Sciaena umbra) en Méditerranée. In Les Espèces Marines à Protéger en Méditérranée, C. F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 219Ð227. Harmelin, J.G. 1993. Invitation sous l’écume. Cahiers Parc National Port-Cros 10, 1Ð83. Harmelin, J.G., Bouchon, C., Duval, C. & Hong, J.S. 1980. Les échinodermes des substrats durs de l’île de Port-Cros, parc national. Eléments pour un inventaire qualitatif. Travaux Scientifiques Parc National Port-Cros 6, 25Ð38.

188 7044_C004.fm Page 189 Monday, April 17, 2006 1:38 PM

MEDITERRANEAN CORALLIGENOUS ASSEMBLAGES

Harmelin, J.G. & Marinopoulos, J. 1994. Population structure and partial mortality of the gorgonian Paramuricea clavata (Risso) in the north-western Mediterranean (France, Port-Cros Island). Marine Life 4, 5Ð13. Harmelin, J.G. & Robert, P. 2001. Evolution récente de la population du mérou brun (Epinephelus marginatus) dans le Parc national de Port-Cros (France, Méditerranée). Scientific Reports Port-Cros National Park 18, 149Ð161. Hillis-Colinvaux, L. 1986. Historical perspectives on algae and reefs: have reefs been misnamed? Oceanus 29, 43Ð48. Hong, J.S. 1980. Étude faunistique d’un fond de concrétionnement de type coralligène soumis à un gradient de pollution en Méditerranée nord-occidentale (Golfe de Fos). Thèse de Doctorat. Université d’Aix- Marseille II. Hong, J S. 1982. Contribution à l’étude des peuplements d’un fond coralligène dans la région marseillaise en Méditerranée Nord-Occidentale. Bulletin of Korea Ocean Research and Development Institute 4, 27Ð51. Hong, J.S. 1983. Impact of the pollution on the benthic community: environmental impact of the pollution on the benthic coralligenous community in the Gulf of Fos, northwestern Mediterranean. Bulletin of the Korean Fisheries Society 16, 273Ð290. Hrs-Brenko, M., Zavodnik, D. & Zahtila, E. 1991. The date shell Lithophaga lithophaga Linnaeus, and its habitat calls for protection in the Adriatic sea. In Les Espèces Marines à Protéger en Méditérranée, C. F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 151Ð158. Huelin, M.F. & Ros, J. 1984. Els moláluscs marins de les illes Medes. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds), Arxius Secció Ciències 73, 457Ð504. James, N.P., Wray, J.L. & Ginsburg, R.N. 1988. Calcification of encrusting aragonitic algae (Peyssonneliaceae): implications for the origin of late Paleozoic reefs and cements. Journal of Sedimentary Petrology 58, 291Ð303. Jimeno, A. & Turon, X. 1995. Gammaridea and Caprellidae of the northeast coast of Spain: ecological distribution on different types of substrata. Polskie Archiwum Hydrobiologii 42, 495Ð516. Kleeman, K.H. 1973. Lithophaga lithophaga (L.) (Bivalvia) in different limestones. Malacologia 14, 345Ð347. Laborel, J. 1960. Contribution à l’étude directe des peuplements benthiques sciaphiles sur substrat rocheux en Méditerranée. Recueil des Travaux de la Station Marine d’Endoume 20 (33), 117Ð174. Laborel, J. 1961. Le concretionnement algal “coralligène” et son importance géomorphologique en Méditer- ranée. Recueil des Travaux de la Station Marine d’Endoume 23 (37), 37Ð60. Laborel, J. 1987. Marine biogenic constructions in the Mediterranean. Scientific Reports of Port-Cros National Park 13, 97Ð126. Laborel, J., Morhange, C., Lafont, R., Le Campion, J., Laborel-Deguen, F. & Sartoretto, S. 1994. Biological evidence of sea-level rise during the last 4500 years on the rocky coasts of continental southwestern France and Corsica. Marine Geology 120, 203Ð223. Lacaze-Duthiers, H. 1864. Histoire Naturelle du Corail. Paris: J.B. Baillière. Laubier, L. 1959a. Contribution à la faunistique du coralligène. I. Quelques particularités biologiques de Polydora armata Langerhans. Vie et Milieu 9, 412Ð415. Laubier, L. 1959b. Contribution à la faunistique du coraligène. III. Deux spionidiens inquilins sur des bryozoaires chilostomides. Vie et Milieu 10, 347Ð349. Laubier, L. 1960. Une nouvelle espèce de syllidien: Haplosyllis depressa Augener ssp. nov. chamaeleon, ectoparasite sur l’octocorallaire Muricea chamaeleon von Koch. Vie et Milieu 11, 75Ð87. Laubier, L. 1966. Le coralligène des Albères: monographie biocénotique. Annales de l’Institut Océan- ographique de Monaco 43, 139Ð316. Lebednik, P.A. 1977. The Corallinaceae of northwestern North America. I. Clathromorphum Foslie emend. Adey. Syesis 9, 59Ð112. Lee, R.K.S. 1967. Taxonomy and distribution of the melobesioid algae on Rongelap Atoll, Marshall Islands. Canadian Journal of Botany 45, 985Ð1001. Linares, C., Coma, R., Diaz, D., Zabala, M., Hereu, B. & Dantart, L. 2005. Immediate and delayed effects of mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean. Marine Ecology Progress Series 305, 127Ð137.

189 7044_C004.fm Page 190 Monday, April 17, 2006 1:38 PM

ENRIC BALLESTEROS

Littler, M.M. 1972. The crustose Corallinaceae. Oceanography and Marine Biology: An Annual Review 10, 311Ð347. Littler, M.M. 1973a. The distribution, abundance, and communities of deepwater Hawaiian crustose Coralli- naceae (Rhodophyta, Cryptonemiales). Pacific Science 27, 281Ð289. Littler, M.M. 1973b. The population and community structure of Hawaiian fringing-reef crustose Corallinaceae (Rhodophyta, Cryptonemiales). Journal of Experimental Marine Biology and Ecology 11, 103Ð120. Littler, M.M. 1976. Calcification and its role among the macroalgae. Micronesica 12, 27Ð41. Littler, M.M. & Doty, M.S. 1975. Ecological components structuring the seaward edges of tropical Pacific reefs: the distribution, communities and productivity of Porolithon. Journal of Ecology 63, 117Ð129. Littler, M.M., Littler, D.S., Blair, S.M. & Norris, J.N. 1986. Deep-water plant communities from an uncharted seamount off San Salvador Island, Bahamas: distribution, abundance, and primary productivity. Deep- Sea Research 33, 881Ð892. Lo Bianco, S. 1909. Notizie biologiche riguardanti specialmente il periodo di maturità sessuale degli animali del golfo di Napoli. Pubblicazioni della Stazione Zoologica di Napoli 19, 513Ð692. Logan, A. 1979. The recent Brachiopoda of the Mediterranean Sea. Bulletin de l’Institut Océanographique (Monaco) 72 (1434), 1Ð112. Llobet, I., Gili, J.M. & Hughes, R.G. 1991a. Horizontal, vertical and seasonal distributions of epiphytic Hydrozoa on the alga Halimeda tuna in the northwestern Mediterranean Sea. Marine Biology 110, 151Ð159. Llobet, I, Coma, R., Zabala, M., Gili, J.M. & Hughes, R.G. 1991b. The population dynamics of Orthopyxis crenata (Hartlaub, 1901) (Hydrozoa, Cnidaria), an epiphyte of Halimeda tuna in the northwestern Mediterranean. Journal of Experimental Marine Biology and Ecology 150, 283Ð292. Lüning, K. 1981. Light. In The Biology of Seaweeds, C.S. Lobban & M.J. Wynne (eds), London & Oxford: Blackwell Scientific, 326–355. Maldonado, M. 1992. Demosponges of the red coral bottoms from the Alboran Sea. Journal of Natural History 26, 1131Ð1161. Mariani, S. & Uriz, M.J. 2001. Copepods of the genus Asterocheres (Copepoda: Siphonostomatoida) feeding on sponges: behavioral and ecological traits. Invertebrate Biology 120, 269Ð277. Marino, G., Di Martino, V. & Giaccone, G. 1998. La vegetazione marina nella Penisola Maddalena (Siracusa, Sicilia SE). Bollettino dell’Accademia Gioenia Scienze Naturalli 31, 235Ð287. Marion, A.F. 1883. Esquisse d’une topographie zoologique du Golfe de Marseille. Annales Musée d’Histoire Naturelle Marseille 1, 1Ð108. Marschal, C., Garrabou, J., Harmelin, J.G. & Pichon, M. 2005. A new method for measuring growth and age in the precious red coral Corallium rubrum (L.). Coral Reefs 23, 423Ð432. Marshall, J.P. 1983. The fate of borings: relations between bioerosion, internal sediment infill and submarine cementation. In Proceedings of the Inaugural GBR Conference, J.T. Baker et al. (eds), Townsville: James Cook University Press, 129Ð234. Martí, R. 2002. Spatial and temporal variability of the natural toxicity in benthic communities of Mediterranean caves. PhD Thesis. University of Barcelona. Martí, R., Uriz, M.J., Ballesteros, E. & Turon, X. 2004. Benthic assemblages in two Mediterranean caves: species diversity and coverage as a function of abiotic parameters and geographic distance. Journal of the Marine Biological Association of the United Kingdom 84, 557Ð572. Martí, R., Uriz, M.J., Ballesteros, E. & Turon, X. 2005. Seasonal variation in structure of three algal communities under different light conditions. Estuarine Coastal and Shelf Science 64, 613Ð622. Martin, D. 1987. La comunidad de anélidos poliquetos de las concreciones de algas calcáreas del litoral catalán. Caracterización de las especies. Publicaciones del Departamento de Zoología de la Univer- sidad de Barcelona 13, 45Ð54. Martin, D. 1996. A new species of Polydora (Polychaeta, Spionidae) associated with the excavating sponge Cliona viridis (Porifera, Hadromerida) in the north-western Mediterranean Sea. Ophelia 45, 159Ð174. Martin, D. & Britayev, T.A. 1998. Symbiotic polychaetes: review of known species. Oceanography and Marine Biology: An Annual Review 36, 217Ð340. Martin, D., Dantart, L. & Ballesteros, M. 1990. Moluscos de las concreciones de algas calcáreas del litoral catalán (NE España). Lavori Società Italiana di Malacologia 23, 445Ð456.

190 7044_C004.fm Page 191 Monday, April 17, 2006 1:38 PM

MEDITERRANEAN CORALLIGENOUS ASSEMBLAGES

Mayol, J., Grau, A., Riera, F. & Oliver, J. 2000. Llista vermella dels peixos de les Balears. Quaderns de Pesca 4, 1Ð126. Meinesz, A. 1999. Killer Algae: The True Tale of a Biological Invasion. Chicago & London: University of Chicago. Meinesz, A. & Hesse, B. 1991. Introduction et invasion de l’algue tropicale Caulerpa taxifolia en Méditerranée nord-occidentale. Oceanologica Acta 14, 415Ð426. Mistri, M. & Ceccherelli, V.U. 1994. Growth and secondary production of the Mediterranean gorgonian Paramuricea clavata. Marine Ecology Progress Series 103, 291Ð296. Molinier, R. 1956. Les fonds à laminaires du Grand Banc de Centuri (Cap Corse). Comptes Rendus de l’Académie des Sciences 342, 939Ð941. Molinier, R. 1960. Étude des biocénoses marines du Cap Corse. Vegetatio 9, 212Ð312. Montserrat, A. 1984. Els equinoderms de les illes Medes. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds), Arxius Secció Ciències 73, 563Ð580. Munar, J. 1993. Els equinoderms. In Història Natural de l’Arxipèlag de Cabrera, J.A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 597Ð606. Munilla, T. & De Haro, A. 1984. Picnogònids de les illes Medes. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds), Arxius Secció Ciències 73, 531Ð536. Nikolic, M. 1960. Hippodiplosia foliacea Solander, 1876 (Bryozoa), comme centre d’association sur un fond coralligène dans l’Adriatique. Rapport et Procès Verbaux des Réunions Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 15 (2), 85Ð86. Odum, H.T. & Odum E.P. 1955. Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecological Monographs 25, 291Ð320. Ortiz, A., Massó, C., Soriano, O. & Limia, J. 1986. La barra italiana como arte de pesca del coral rojo (Corallium rubrum L.) en el mar de Alborán (SE de España). Boletín Instituto Español de Ocean- ografía 3, 83Ð92. Palanques, A., Guillén, J. & Puig, P. 2001. Impact of bottom trawling on water turbidity and muddy sediment of an unfished continental shelf. Limnology and Oceanography 46, 1100Ð1110. Parenzan, P. 1960. Aspetti biocenotici dei fondi ad alghe litoproduttrici del Mediterraneo. Rapport et Procès Verbaux des Réunions Commission Internationale pour l’Exploration Scientifique de la Mer Médi- terranée 15 (2), 87Ð107. Pascual, J. & Flos, J. 1984. Metereologia i Oceanografia. In Els Sistemes Naturals de les Illes Medes, J. Ros, I. Olivella & J.M. Gili (eds), Arxius Secció Ciències 73, 75Ð114. Patzner, R.A. 1998. The invasion of Lophocladia (Rhodomelaceae, Lophotalieae) at the northern coast of Ibiza (Western Mediterranean Sea). Bolletí de la Societat d’Història Natural de les Balears 41, 75Ð80. Patzner, R.A. 1999. Habitat utilization and depth distribution of small cryptobenthic fishes (Blenniidae, Gobiidae, Trypyterigiidae) in Ibiza (western Mediterranean Sea). Environmental Biology of Fishes 55, 207Ð214. Pérès, J. 1967. The Mediterranean benthos. Oceanography and Marine Biology: An Annual Review 5, 449Ð533. Pérès, J. & Picard, J.M. 1951. Notes sur les fonds coralligènes de la région de Marseille. Archives de Zoologie Expérimentale et Générale 88, 24Ð38. Pérès, J. & Picard, J.M. 1952. Les corniches calcaires d’origine biologique en Méditerranée Occidentale. Recueil des Travaux de la Station Marine d’Endoume 4, 2Ð33. Pérès, J. & Picard, J.M. 1958 Recherches sur les peuplements benthiques de la Méditerranée nord-orientale. Annales de l’Institut Océanographique de Monaco 34, 213Ð291. Pérès, J. & Picard, J.M. 1964. Nouveau manuel de bionomie benthique de la mer Méditerranée. Recueil des Travaux de la Station Marine d’Endoume 31(47), 1Ð131. Perez, T., Garrabou, J., Sartoretto, S., Harmelin, J.G., Francour, P. & Vacelet, J. 2000. Mortalité massive d’invertébrés marins: un événement sans précédent en Méditerranée nord-occidentale. Comptes Ren- dus de l’Académie des Sciences Série III, Life Sciences 323, 853Ð865. Piazzi, L., Balata, D., Pertusati, M. & Cinelli, F. 2004. Spatial and temporal variability of Mediterranean macroalgal coralligenous assemblages in relation to habitat and substratum inclination. Botanica Marina 47, 105Ð115.

191 7044_C004.fm Page 192 Monday, April 17, 2006 1:38 PM

ENRIC BALLESTEROS

Piazzi, L., Ceccherelli, G., Meinesz, A., Verlaque, M., Akali, B. Antolic, B., Argyrou, M., Balata, D., Balles- teros, E., Calvo, S., Cinelli, F., D’Archino, R., Djellouli, A.S., Javel, F., Mifsud, C., Pala, D., Panayotidis, P., Peirano, A., Pergent, G., Petrocelli, A., Ruitton, S. & Zuljevic, A. 2005. Invasion of Caulerpa racemosa (Caulerpales, Chlorophyta) in the Mediterranean Sea: the balance of thirteen years of spread. Cryptogamie Algologie 26, 189Ð202. Piazzi, L., Pardi, G., Balata, D., Cecchi, E. & Cinelli, F. 2002. Seasonal dynamics of a subtidal north-western Mediterranean macroalgal community in relation to depth and substrate inclination. Botanica Marina 45, 243Ð252. Piazzi, L., Pardi, G. & Cinelli, F. 1996. Ecological aspects and reproductive phenology of Acrothamnion preissii (Sonder) Wollaston (Ceramiaceae, Rhodophyta) from the Tuscan Archipelago (Western Med- iterranean). Cryptogamie Algologie 17, 35Ð43. Pruvot, G. 1894. Sur les fonds sous-marins de la région de Banyuls et du cap de Creus. Comptes Rendus de l’Académie des Sciences 118, 203Ð206. Pruvot, G. 1895. Coup d’oeil sur la distribution générale des invertébrés dans la région de Banyuls (Golfe du Lion). Archives de Zoologie Expérimentale et Générale 3, 629Ð658. Pruvot, G. 1897. Essai sur les fonds et la faune de la Manche Occidentale (côtes de Bretagne) comparées à ceux du Golfe de Lion. Archives de Zoologie Expérimentale et Générale 5, 511Ð660. Ramos, A.A. 1991. Ascidias litorales del Mediterráneo ibérico. Faunística, ecología y biogeografía. Tesis Doctoral. Universidad de Alicante. Ribes, M., Coma, R. & Gili, J.M. 1998. Seasonal variation of in situ feeding rates by the temperate ascidian Halocynthia papillosa. Marine Ecology Progress Series 175, 201Ð213. Ribes, M., Coma, R. & Gili, J.M. 1999a. Seasonal variation of particulate organic carbon, dissolved organic carbon and the contribution of microbial communities to the live particulate organic carbon in a shallow near-bottom ecosystem at the Northwestern Mediterranean Sea. Journal of Plankton Research 21, 1077Ð1100. Ribes, M., Coma, R. & Gili, J.M. 1999b. Natural diet and grazing rate of the temperate sponge Dysidea avara (Demospongiae, Dendroceratida) throughout an annual cycle. Marine Ecology Progress Series 176, 179Ð190. Ribes, M., Coma, R. & Gili, J.M. 1999c. Heterogenous feeding in benthic suspension feeders: the natural diet and grazing rate of the temperate gorgonian Paramuricea clavata (Cnidaria: Octocorallia) over a year cycle. Marine Ecology Progress Series 183, 125Ð137. Riedl, R. 1966. Biologie der Meereshöhlen. Hamburg: Paul Parey. Riera, F., Oliver, J. & Terrassa, J. 1998. Peixos de les Balears. Palma de Mallorca: Govern Balear. Riera, F., Pou, S. & Grau, A.M. 1993. La ictiofauna. In Història Natural de l’Arxipèlag de Cabrera, J. A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 623Ð644. Rivoire, G. 1991. Mortalité du corail et des gorgones en profondeur au large des côtes provençales. In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posi- donie, 53Ð59. Romano, J.C., Bensoussan, N., Younes, W.A.N. & Arlhac, D. 2000. Anomalies thermiques dans les eaux du Golfe de Marseille durant l’été 1999. Une explication partielle de la mortalité des invertébrés fixés. Comptes Rendus de l’Académie des Sciences Série III, Life Sciences 323, 853Ð865. Ros, J. 1978. La alimentación y el sustrato en los opistobranquios ibéricos. Oecologia Aquatica 3, 153Ð166. Ros, J., Olivella, I. & Gili, J.M. (eds). 1984. Els Sistemes Naturals de les Illes Medes. Arxius Secció Ciències 73, Barcelona: Institut d’Estudis Catalans. Ros, J., Romero, J., Ballesteros, E. & Gili, J.M. 1985. Diving in blue water: the benthos. In Western Mediterranean, R. Margalef (ed.), Oxford: Pergamon, 233Ð295. Rosell, D. & Uriz, M.J. 2002. Excavating and endolithic sponge species (Porifera) from the Mediterranean: species descriptions and identification key. Organisms Diversity and Evolution 2, 55Ð86. Rosell, D., Uriz, M.J. & Martin, D. 1999. Infestation by excavating sponges on the oyster (Ostrea edulis) populations of the Blanes littoral zone (northwestern Mediterranean Sea). Journal of the Marine Biological Association of the United Kingdom 79, 409Ð413.

192 7044_C004.fm Page 193 Monday, April 17, 2006 1:38 PM

MEDITERRANEAN CORALLIGENOUS ASSEMBLAGES

Rossi, L. 1958. Osservazioni sul bentos coralligeno dei dintorni di Catania. Archivi di Oceanografia e Limnologia 11, 161Ð165. Rossi, L. 1961. Sur un faciès à gorgonaires de la pointe du Mesco (Golfe de Gènes) (note préliminaire). Rapports et Procés-Verbaux des Réunions Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 16 (2), 517Ð521. Rossi, S. 2001. Environmental factors affecting the trophic ecology of benthic suspension feeders. PhD Thesis. University of Barcelona. Russo, G.F. & Cicogna, F. 1991. The date mussel (Lithophaga lithophaga), a “case” in the Gulf of Naples. In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 141Ð150. Rützler, K. 1976. Ecology of Tunisian commercial sponges. Tethys 7, 249Ð264. Sala, E., Boudouresque, C.F. & Harmelin-Vivien, M. 1998. Fishing, trophic cascades and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 82, 425Ð439. Sala, E., Garrabou, J. & Zabala, M. 1996. Effects of diver frequentation on Mediterranean sublittoral popu- lations of the bryozoan Pentapora fascialis. Marine Biology 126, 451Ð459. Salas, C. & Hergueta, E. 1986. Fauna de moluscos de las concreciones calcáreas de Mesophyllum lichenoides (Ellis) Lemoine. Estudio de la diversidad de un ciclo anual. Iberus 6, 57Ð65. Santangelo, G. & Abbiati, M. 2001. Red coral: conservation and management of an over-exploited Mediter- ranean species. Aquatic Conservation of Marine and Freshwater Ecosystems 11, 253Ð259. Santangelo, G., Abbiati, M., Giannini, F. & Cicogna, F. 1993. Red coral fishing trends in the western Mediterranean Sea during the period 1981Ð1991. Scientia Marina 57, 139Ð143. Santangelo, G., Carletti, E., Maggi, E. & Bramanti, L. 2003. Reproduction and population sexual structure of the overexploited Mediterranean red coral Corallium rubrum. Marine Ecology Progress Series 248, 99Ð108. Sarà, M. 1968. Un coralligeno di piattaforma (coralligène de plateau) lungo il littorale pugliese. Archivi di Oceanografia e Limnologia 15 (Suppl.), 139Ð150. Sarà, M. 1969. Research on coralligenous formation: problems and perspectives. Pubblicazioni della Stazione Zoologica di Napoli 37, 124Ð134. Sartoretto, S. 1994. Structure et dynamique d’un nouveau type de bioconstruction à Mesophyllum lichenoides (Ellis) Lemoine (Corallinales, Rhodophyta). Comptes Rendus de l’Académie des Sciences Série III, Life Sciences 317, 156Ð160. Sartoretto, S. 1996. Vitesse de croissance et bioérosion des concrétionnements “coralligènes” de Méditerranée nord-occidentale. Rapport avec les variations Holocènes du niveau marin. Thèse Doctorat d’Écologie, Université d’Aix-Marseille, II. Sartoretto, S. 1998. Bioérosion des concrétions coralligènes de Méditerranée par les organismes perforants: essai de quantification des processus. Comptes Rendus de l’Académie des Sciences Séries IIA, Earth and Planetary Sciences 327, 839Ð844. Sartoretto, S. & Francour, P. 1997. Quantification of bioerosion by Sphaerechinus granularis on “coralligène” concretions of the western Mediterranean. Journal of the Marine Biological Association of the United Kingdom 77, 565Ð568. Sartoretto, S., Francour, P., Harmelin, J.G. & Charbonnel, E. 1997. Observations in situ de deux Labridae profonds, Lappanella fasciata et Acantholabrus palloni, en Méditerranée nord-occidentale. Cybium 21, 37Ð44. Sartoretto, S., Verlaque, M. & Laborel, J. 1996. Age of settlement and accumulation rate of submarine “coralligène” (–10 to –60 m) of the northwestern Mediterranean Sea; relation to Holocene rise in sea level. Marine Geology 130, 317Ð331. Simkiss, K. 1964. Phosphates as crystalpoisons of calcification. Biological Reviews 39, 487Ð505. Spanier, E. 1991. Artificial reefs to insure protection of the adult Mediterranean slipper lobster, Scyllarides latus. In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 179Ð185. Templado, J. 1991. Las especies del género Charonia (Mollusca: Gastropoda) en el Mediterráneo. In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posi- donie, 133Ð140.

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Templado, J., García-Carrascosa, M., Baratech, L., Capaccioni, R., Juan, A., López-Ibor, A., Silvestre, R. & Massó, C. 1986. Estudio preliminar de la fauna asociada a los fondos coralíferos del mar de Alborán (SE de España). Boletín Instituto Español de Oceanografía 3, 93Ð104. Torrents, O., Garrabou, J., Marschal, C. & Harmelin, J.G. 2005. Age and size at first reproduction in the commercially exploited red coral Corallium rubrum (L.) in the Marseilles area (France, NW Medi- terranean). Biological Conservation 121, 391Ð397. Tortonese, E. 1958. Bionomia marina della regione costiera fra punta della Chiappa e Portofino (Riviera Ligure di Levante). Archivi di Oceanografia e Limnologia 11, 167Ð210. Tortonese, E. 1965. Fauna d’Italia. Echinodermata. Bologna: Calderini. True, M.A. 1970. Étude quantitative de quatre peuplements sciaphiles sur substrat rocheux dans la région marsellaise. Bulletin de l’Institut Océanographique (Monaco) 69 (1401), 1Ð48. Turon, X. 1990. Distribution and abundance of ascidians from a locality on the northeast coast of Spain. Pubblicazioni della Stazione Zoologoca di Napoli I: Marine Ecology 11, 291Ð308. Turon, X. 1992. Periods of non-feeding in Polysyncraton lacazei (Ascidiacea: Didemnidae): a rejuvenative process? Marine Biology 112, 647Ð655. Turon, X. 1993. Els ascidis: faunística i distribució. In Història Natural de l’Arxipèlag de Cabrera, J. A. Alcover et al. (eds), Monografies de la Societat d’Història Natural de Balears 2. Palma de Mallorca: CSIC-Ed. Moll, 607Ð621. Turon, X. & Becerro, M. 1992. Growth and survival of several ascidian species from the northwestern Mediterranean. Marine Ecology Progress Series 82, 235Ð247. Turon, X., Galera, J. & Uriz, M.J. 1997. Clearance rates and aquiferous systems in two sponges with contrasting life-history strategies. Journal of Experimental Zoology 278, 22Ð36. Turon, X., Uriz, M.J. & Willenz, P. 1999. Cuticular linings and remodelisation processes in Crambe crambe (Demospongiae: Poeciclosclerida). Memoirs of the Queensland Museum 44, 617Ð625. Uriz, M.J., Martin, D., Turon, X., Ballesteros, E., Hughes, R. & Acebal, C. 1991. An approach to the ecological significance of chemically mediated bioactivity in Mediterranean benthic communities. Marine Ecol- ogy Progress Series 70, 175Ð188. Uriz, M.J., Rosell, D. & Martin, D. 1992a. The sponge population of the Cabrera Archipelago (Balearic islands): characteristics, distribution, and abundance of the most representative species. Pubblicazioni della Stazione Zoologica di Napoli I: Marine Ecology 13, 101Ð117. Uriz, M.J., Rosell, D. & Maldonado, M. 1992b. Parasitism, commensalism or mutualism? The case of Scyphozoa (Coronatae) and horny sponges. Marine Ecology Progress Series 81, 247Ð255. Uriz, M.J., Rosell, D. & Martin, D. 1992c. Relationships of biological and taxonomic characteristics to chemically mediated bioactivity in Mediterranean littoral sponges. Marine Biology 113, 287Ð297. Vadas, R.L. & Steneck, R.S. 1988. Zonation of deep water benthic algae in the Gulf of Maine. Journal of Phycology 24, 338Ð346. Vaissière, R. 1964. Contribution à l’étude bionomique de la Méditerranée Occidentale (côte du Var et des Alpes-Maritimes, côte occidentale de Corse). Fasc. 1: Generalités. Bulletin de l’Institut Océan- ographique (Monaco) 63 (1310), 1Ð12. Vaissière, R. & Fredj, G. 1963. Contribution à l’étude de la faune benthique du plateau continental de l’Algérie. Bulletin de l’Institut Océanographique (Monaco) 60 (1272), 1Ð83. Velimirov, B. 1975. Wachstum und Altersbestimmung der Gorgonie Eunicella cavolinii. Oecologia 19, 259Ð272. Vicente, N. & Moreteau, J.C. 1991. Statut de Pinna nobilis L. en Méditerranée (Mollusque Eulamellibranche). In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 159Ð168. Vighi, M. 1972. Étude sur la reproduction du Corallium rubrum (L.). Vie et Milieu Sèries A 23, 21Ð32. Weinbauer, M.G. & Velimirov, B. 1995a. Morphological variations in the Mediterranean sea fan Eunicella cavolini (Coelenterata: Gorgonacea) in relation to exposure, colony size and colony region. Bulletin of Marine Science 56, 283Ð295. Weinbauer, M.G. & Velimirov, B. 1995b. Biomass and secondary production of the temperate gorgonian coral Eunicella cavolini (Coelenterata, Gorgonacea). Marine Ecology Progress Series 121, 211Ð216.

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Weinberg, S. 1979. The light-dependent behaviour of planulae larvae of Eunicella singularis and Corallium rubrum and its implication for octocorallian ecology. Bijdragen tot de Dierkunde 49, 16Ð30. Weinberg, S. 1991. Faut-il protéger les gorgones de Méditerranée? In Les Espèces Marines à Protéger en Méditérranée, C.F. Boudouresque et al. (eds), Marseille: GIS Posidonie, 47Ð52. Weinberg, S. & Weinberg, F. 1979. The life cycle of a gorgonian: Eunicella singularis (Esper, 1794). Bijdragen tot de Dierkunde 48, 127Ð140. Whitehead, P.J.P., Bauchot, M.L., Hureau, J.C., Nielsen, J. & Tortonese, E. (eds). 1984Ð1986. Fishes of the North-Eastern Atlantic and the Mediterranean. Vols. IÐIII. Bungay: Chaucer. Woelkerling, W.J. 1983. A taxonomic reassessment of Lithophyllum (Corallinaceae, Rhodophyta) based on studies of R.A. Philippi’s original collections. British Phycological Journal 18, 299Ð328. Woelkerling, W.J., Penrose, D. & Chamberlain, Y.M. 1993. A reassessment of type collections of non- geniculate Corallinaceae (Corallinales, Rhodophyta) described by C. Montagne and L. Dufour, and of Melobesia brassica-florida Harvey. Phycologia 32, 323Ð331. Wray, J.L. 1977. Calcareous Algae. Amsterdam: Elsevier. Zabala, M. 1984. Briozous de les illes Medes. In Els Sistemes Naturals de les Illes Medes, J. Ros et al. (eds), Arxius Secció Ciències 73, 537Ð562. Zabala, M. 1986. Fauna dels briozous dels Països Catalans. Arxius Secció Ciències 84, 1Ð833. Zabala, M. & Ballesteros, E. 1989. Surface-dependent strategies and energy flux in benthic marine communities or, why corals do not exist in the Mediterranean. Scientia Marina 53, 3Ð17. Zabala, M., Garcia-Rubies, A., Louisy, P. & Sala, E. 1997a. Spawning behaviour of the Mediterranean dusky grouper Epinephelus marginatus (Lowe, 1834) (Pisces, Serranidae) in the Medes islands Marine Reserve (NW Mediterranean, Spain). Scientia Marina 61, 65Ð77. Zabala, M., Louisy, P., Garcia-Rubies, A. & Gracia, V. 1997b. Socio-behavioural context of reproduction in the Mediterranean dusky grouper Epinephelus marginatus (Lowe, 1834) (Pisces, Serranidae) in the Medes islands Marine Reserve (NW Mediterranean, Spain). Scientia Marina 61, 79Ð89. Zibrowius, H., Monteiro-Marques, V. & Grashoff, M. 1984. La répartition du Corallium rubrum dans l’Atlan- tique (Cnidaria, Anthozoa: Gorgonaria). Téthys 11, 163Ð170.

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Oceanography and Marine Biology: An Annual Review, 2006, 44, 197-276 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS — FROM HISTOLOGY TO ECOLOGY

HEIKE WÄGELE1, MANUEL BALLESTEROS2 & CONXITA AVILA3 1Rheinische Friedrich-Wilhelms-Universität, Institut für Evolutionsbiologie, An der Immenburg 1, 53121 Bonn, Germany and Zoologisches Forschungsmuseum Koenig, Adenauer Allee 160, 53113 Bonn, Germany E-mail: [email protected] 2Facultat de Biologia, Universitat de Barcelona, Av. Diagonal 645, 08028 Barcelona, Catalunya, Spain E-mail: [email protected] 3CEAB-CSIC, c/Accés a la Cala Sant Francesc 14, 17300 Blanes, Girona, Catalunya, Spain E-mail: [email protected]

Abstract Opisthobranch molluscs are an extremely interesting group of animals, displaying a wide diversity in shape, colour and life strategies. Chemical ecology of this group is particularly appealing since most species have a reduced or absent shell and have developed chemical defences to avoid predation. New results on defensive glandular structures as well as a compilation of literature data in sea slugs (Opisthobranchia, Gastropoda, Mollusca) are presented in this review. Investigation of these structures is based on detailed analyses of the histology of many representative species of all major taxa of the Opisthobranchia. The results are correlated with previous and new findings of secondary metabolites in these animals and are set in a phylogenetic context. Addition- ally, information on food sources is given. Also, an hypothetical scenario relating chemical ecology to histology is proposed. This information will help future analyses to investigate defensive devices on a much more accurate basis and allow a better understanding of evolutionary processes, which are observed independently in many opisthobranch clades.

Introduction Defensive strategies are manifold in Opisthobranchia and comprise cryptic appearance (Edmunds 1987, Wägele & Klussmann-Kolb 2005), formation of spicules (Cattaneo-Vietti et al. 1993, 1995), uptake of nematocysts from cnidarian prey (most recent literature: Gosliner 1994a, Martin & Walther 2002, 2003, Wägele 2004), incorporation of toxic metabolites from the prey, or even de novo synthesis of chemicals. Several reviews have covered the last topic of chemical ecology in molluscs (Karuso 1987, Cimino & Sodano 1989, Faulkner 1988, 1992, 2000, 2001, Pawlik 1993, Avila 1995, 2006, Cimino & Ghiselin 1998, Cimino et al. 2000, Stachowicz 2001, Amsler et al. 2001). Furthermore, some reviews have dealt with natural products from particular groups, such as porostome nudibranchs (Gavagnin et al. 2001), dorids and sacoglossans (Cimino et al. 1999, Cimino & Ghiselin 1998, 1999), or gastropods in general (Cimino & Ghiselin 2001), incorporating

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an evolutionary perspective in their analysis. In opisthobranchs, Faulkner & Ghiselin (1983) dis- cussed the importance of the acquisition of defensive chemicals during slug evolution, thus allowing the reduction of the shell (see also Wägele & Klussmann-Kolb 2005). This may have many ecological implications, such as the advantage of searching for new food sources, the exploitation of new habitats, and the development of mantle glands or structures, among others. Cimino & Ghiselin (1999) went even further in claiming that chemical defence is the driving force of opisthobranch evolution. Chemical defence is the main topic in molluscan chemical ecology, although it is by no means the only one. The importance of correctly demonstrating in situ activity against co-occurring predators has been a subject of repeated debate (Faulkner 1992, Avila 1995). However, many compounds are still assumed to have a defensive role without the supporting evidence of reliable ecological experiments. Ecological activity of the compounds has been evaluated in situ, against co-occurring predators for only a few species (Thompson 1960, Avila & Paul 1997, Johnson & Willows 1999, Marín et al. 1999, Avila et al. 2000, Becerro et al. 2001, Gosliner 2001, Iken et al. 2002, Rogers et al. 2002, Penney 2004). The methodological difficulties in carrying out in situ experiments or using co-occuring predators are probably responsible for the scarce information available. To overcome these problems, some studies used predators that do not occur in the same habitat (e.g., Mollo et al. 2005). On the other hand, there is also some literature that deals with parasites on opisthobranchs (Edmunds 1964; Arnaud 1978; Carefoot 1987; Huys 2001; Schrödl 2002, 2003; see also Rudman 2000a) but nothing is known about possible defensive strategies against these parasites. Since the review of the natural products of opisthobranch molluscs published 10 years ago (Avila 1995), many other articles have appeared that deal with opisthobranchs and which describe new interesting aspects of their chemistry (see Faulkner 2002 and previous reports; Blunt et al. 2005). Unfortunately, they cannot all be reviewed here. The geographic variation of natural products in Asteronotus cespitosus (Fahey & Garson 2002) and in Cadlina luteomarginata (Kubanek et al. 2000) has provided new insights into the field. Kubanek et al. (2000) suggested that in some nudibranchs, de novo biosynthesis may be modulated by habitat-specific external factors, thus working only when dietary compounds are not available. The authors suggested this represents an intermediate stage in the evolution of nudibranch chemical defences, between the probably primitive chemical sequestration from diet and the more evolved processes of de novo biosynthesis. The fact that some nudibranchs may only biosynthesise when dietary compounds are not available is an open question that needs to be tested in other species. Among nudibranchs, only C. luteomarginata and Dendrodoris grandiflora seem to possess both dietary sequestered compounds and biosynthetic chemicals (Cimino et al. 1985a, Avila et al. 1991a, Kubanek et al. 2000). Regarding the origin of these compounds, the number of biosynthetic compounds, compared with those obtained from the diet, continues to increase (Garson 1993, Cimino & Sodano 1994, Avila 1995, Faulkner 2002). The sesquiterpene aldehydes of the nudibranch Acanthodoris nanaimoensis are another example of de novo biosynthesis (Graziani & Andersen, 1996). Further studies on biosynthesis include Fontana et al. (1999a, 2003) and Jansen & de Groot (2004), and others reviewed by Garson (2001) and Cimino et al. (2004). Dietary chemicals are selected by a still unknown mechanism. Faulkner (1992) proposed two different mechanisms by which the selection of chemicals could be achieved, but this was never studied in detail. The sea hare Stylocheilus striatus accumulates very different metabolites when offered artificial diets (Pennings & Paul 1993). Fontana et al. (1994b) showed that in the laboratory a chromodoridid species was able to accumulate in the mantle glands compounds from a sponge that is not usually its prey in the field. These experiments would support the idea that the initial role of accumulation structures was that of excretion or autoprotection from the dietary chemicals and evolved later into a defensive mechanism.

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The available information on location and structure of the possible storage organs for chemical defences is scarce and mainly based on literature from the nineteenth to the early twentieth centuries (e.g., Blochmann 1883, Vayssière 1885, Perrier & Fischer 1911). The older literature was reviewed by Hoffmann (1939). More recent studies including histological structures are found, for example, in Edmunds (1966a,b), Thompson & Colman (1984), Thompson (1986), Gosliner (1994a), Wägele (1997), Kolb (1998), Brodie (2005) and Wägele & Klussmann-Kolb (2005). The couple Evelyn and Ernst Marcus, to whom we owe many thorough descriptions of opisthobranchs, very often included histological investigations when describing species, but only in very few cases do these cover defensive glands (also called repugnatorial glands) and then only in a rather sketchy way (e.g., Marcus & Marcus 1955; Marcus 1957, 1958, 1959). The same holds true for many descriptions from the Danish opisthobranch scientist Rudolph Bergh, which are not included here for the same reason. Recent and more extensive investigations on defensive glands are mainly confined to the mantle dermal formations (MDFs) in the doridoidean family Chromodorididae (García-Gomez et al. 1990, 1991; Cimino et al. 1993a; Avila & Paul 1997) and the glands of sea hares (Johnson & Willows 1999). Few investigations deal with epithelial structures or other glandular structures (e.g., Marín et al. 1991, Avila & Durfort 1996, Wägele 1997, Wägele & Klussmann-Kolb 2005). MDFs are suspected to store biochemicals from sponges, the food items of chromodorids. They are discussed as important key characters in the evolution of this particular family (Gosliner & Johnson 1994, Gosliner 2001, Wägele 2004) but, in fact, it is now known that other groups of opisthobranchs that do not forage on sponges also possess MDFs (see Wägele 1997, 2004 and this study). Finding MDFs in a bryozoan-consuming nudibranch (Limacia clavigera) (Wägele 1997) and in an algae- consuming sacoglossan (Plakobranchus ocellatus (see Wägele 2004)) renders invalid all the pre- vious assumptions of the mantle glands as an exclusive characteristic of the Chromodorididae. Until now, very few attempts have been made to relate knowledge on defensive chemicals to glandular structures known from histology (e.g., Marín et al. 1991 for Tethys fimbria, Marín et al. 1999 for Cephalaspidea). Avila (1993), Fontana et al. (1994b) and Avila & Durfort (1996) showed a preliminary relationship between some defensive glands and natural products for several species of nudibranchs. Actually, all the assumptions on location of chemicals are based on dissection and separation of body parts (e.g., MDFs, mantle border, etc.), and not on cytology or cytochemistry. This is the case in most of the located compounds, such as furanosesquiterpenes of Hypselodoris and Ceratosoma species, diterpenes of Chromodoris species, sesterterpenes of Glossodoris species, or sesquiterpenes of Dendrodorididae. This study tries to fill the gap in the knowledge of the relationship between glandular structures and defensive compounds by summarising histological studies on defensive glands or structures within Opisthobranchia and by tabulating published results on their secondary metabolites. Furthermore, the development of defensive glands, which are supposed to accumulate dietary chemicals in juvenile specimens of Hypselodoris species, was studied in order to ascertain their ontogeny.

Material and methods To analyse the maximum information available on the defensive glands at histological, ecological and chemical levels, several species were selected from each group. Selection was based mainly on the availability of biological material for carrying out rigorous histological studies and also on existing data on ecology and chemistry for the species. However, this proved to be very difficult because very often data are incomplete. For example, data may be available on the chemistry but not on the histology and ecology of a species, and vice versa. Considerable effort has been made to include as many species as possible in the review so that it offers all the information available

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in the literature until June 2005. To reduce ambiguity, the taxonomic authorities of all species mentioned in the text are listed in Table 2. For histological analyses, many species were sampled during various expeditions all over the world in recent years, preserved in 4Ð6% formaldehyde/sea water and stored in 70% ethanol. After dehydration, the specimens were embedded in hydroxyethylmethacrylat (technique developed by Kulzer) (see Wägele 1997). Serial sections (2.5 µm) were stained with Toluidine blue, which specifically stains acid mucopolysaccharides red to violet, and neutral mucopolysaccharides blue. Some of the species investigated were very large and only smaller pieces could be studied histo- logically. However, this does not allow descriptions to be given of the wider occurrence of the glands, which have a very restricted distribution in the body. For comparison, a few basal pulmonate species are included. For analysis of the chemical composition of some structures (especially the mantle dermal formations), specimens of six species were embedded in Paraplast and sectioned (thickness of sections 5–6 µm). Different staining techniques were applied including two trichrome stains (Poinceau-Acidfuchsin-Azophloxin after Goldner, and Azocarmine-Aniline-Orange G after Heiden- hain) and a special staining technique for connective tissue (after Pasini). All methods are described in Böck (1989). Except where noted otherwise, staining records in the text and tables usually refer to Toluidine blue. Hypselodoris villafranca specimens for the ontogenetic studies were collected in Blanes and Tossa (Catalonia, Spain) in August 2003. Sizes of the juveniles ranged from 3Ð6 mm length. Some adults (15 mm) were also collected and studied to compare with the juveniles of the same popu- lations. They were fixed as described above.

Results Description of glands Nearly all opisthobranch and pulmonate species investigated have more glands than just the repugnatorial or defensive glands and the foot in particular is highly glandular. These latter struc- tures, and others which are more likely involved in crawling (e.g., the tubular foot gland in pulmonates and some cephalaspideans), are not listed here, only those which might be of defensive value. The glandular structures can usually be assigned to certain types, some of which are already well known, others are newly described here. Defensive glandular structures are located in different areas of the animals. They can be located in the epidermis and are therefore part of the outer epidermis. They can lie subepidermally in the notum as single glandular structures or form distinct organs. Some lie in the notum, usually forming rather large organs. In a few cases, large glands are present in the visceral cavity. Table 1 and Figure 1 to Figure 9 give an overview of the types. Table 2 lists all the species investigated during the study and lists some types of glands found in particular species. The food and the chemical structure of the known secondary metabolites from the slug are also provided (Table 2). The glands are described and listed with regard to their location in the organism. Epidermal glandular structures, subepithelial glands, glands in the notum tissue and glands in the visceral cavity are distinguished (see Table 1).

Glandular structures confined to the epidermis (Table 1, Table 2 Column 9)

Single glandular cells (Table 1) Single glandular cells are mainly located in the notum epithelium and are widely spread. The contents of the vacuoles of the cells mainly stain dark violet, indicating acid mucopolysaccharides. Although morphological and histological complexity is rather low in these

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Table 1 Overview of the different types of glandular structures arranged according to location, composition and staining properties

Staining properties Violet staining — Bluish staining indicating Nonstaining — indicating indicating acid neutral mucopolysaccharides acidic or other substances Gland type mucopolysacharides Single gland cells in Cup cells (e.g., in many Cells with a huge vacuole, Spongy glands (Figure 1C) epidermis Dendronotoidea) contents staining (Figure 1A,B) homogeneously (Dendrodorididae) (Figure 1B)

Single glands Hypobranchial gland forming a layer (Figure 1D)

Subepithelial glands Single glandular cells of ‘Cellules spéciales’ Subepithelial acid glands moderate size usually (Figure 1F,G) (Pleurobranchoidea) opening to the outside (Figure 2G) (Figure 4B at bottom) Blochmann’s glands: some Cephalaspidea Bohadsch gland or opaline (Figure 2A,B) and Anaspidea gland (Figure 2D,E) (here known as ink gland or purple gland) (Figure 2C)

Glandular organs Marginal sacs of Arminidae Dorsal notum gland Agglomeration of glandular lying in notum (Figure 4A) (Tylodinoidea) (Figure 3AÐC) cells (Thecacera, Cadlina) (Figure 4B,C) Interpallial gland (Scaphander) (Figure 3D,E) MDFs (Chromodorididae) (Figure 5AÐF, Figure MDFs (Newnesia, 6EÐG, Figure 7AÐF) Plakobranchus) (Figure 6A, 7F)

MDF-like structures (Doriopsilla, Melibe, etc.) (Figure 6BÐD, Figure 9AÐF)

Complex glands Median buccal gland lying inside the (Bourne’s gland) body (Pleurobranchoidea, Plocamopherus) (Figure 4DÐF)

kinds of cells, a typical appearance of single glandular cells was noticed in many representatives of the Dendronotoidea (Figure 1A, Marionia blainvillea; see also Table 2 Column 9). Here the cuplike glandular cells are characterised by a huge vacuole, staining homogenously dark violet, indicating acid mucopolysaccharides. In other taxa, the contents of the vacuoles may be granular or even homogenous (Figure 1B, Dendrodoris nigra, arrow). This indicates the presence of different substances in the glandular cells. In Roboastra gracilis the glandular epithelium is characterised by numerous extremely tall violet-stained mucous cells with a granular appearance. (continued on page 227)

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA Klussmann-Kolb Klussmann-Kolb 2005 1911, Hoffmann 1911, Hoffmann 1939, Wägele & Klussmann-Kolb 2005 Rudman 1972c 1939 Hoffmann Wägele & Perrier & Fischer *Rudman 1972a 12 12 histology Previous (references) 1939 Hoffmann Unknown Unknown Unknown ** Unknown Unknown Unknown Unknown 11 Natural products (references) eb site eb site eb site eb site urbellaria (Rudman W Seaslugforum) polychaetes and turbellarians (Burn & Thompson 1998) W Seaslugforum) polychaetes and turbellarians (Burn & Thompson 1998) W Seaslugforum) W Seaslugforum) Polychaeta (Rudman Congeners feed on T Congeners feed on Food (references) Food Polychaeta (Rudman Polychaeta (Rudman 10

Special defensive glands

MDF-like structures MDF-like

MDF TYPE MDF

Glandular stripe Glandular Blochmann

0000 0+00 0000 0000 0000 Spongy mantel glands mantel Spongy

456789 +0+00 Hypobranchial gland Hypobranchial 3 ++ +? ++ + ++ ++

Linneus, 1758 Baba & Abe, 1959 Baba & Baba, 1949 Risbec, 1951 Linneus, 1758 Linneus, 1758 2 Genus and species, authorities Acteon tornatilis Pupa solidula Hydatina physis inornata Chelidonura pallida Chelidonura tsurugensis Chelidonura Compilation of available data on glandular structures, food and natural products. See notes on page 226. Compilation of available Aglajidae Hydatinidae Acteonidae able 2 CEPHALASPIDEA T Column 1 Higher taxon ACTEONOIDEA

202

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS : Bulla striata Klussmann-Kolb Klussmann-Kolb 2005, 1939, *Hoffmann *Marcus 1958, *Edlinger 1982 ( discoidal glands gill, open above into mantle cavity) Wägele & *Marcus 1957 ontana et al. 2001) ** al. 2001) ontana et 1992b, 1992c, 1993, al. 1999) ** Marín et F Alvarez et al. 1998, Izzo Alvarez et al. 2000) ** MO (Spinella et al. MO (Spinella et Unknown ** Unknown Unknown ** Unknown Unknown Unknown ** Unknown SQ (Poiner et al. 1989, SQ (Poiner et OC (Spinella et al. 1998, OC (Spinella et , (Gibson &

Ulva eb site eb site eb site other haminoids, namely turfing green & algae (Burn Thompson 1998) W Seaslugforum) (Rudman Web site (Rudman Web Seaslugforum, Yonow 1992) (Rudman Web site (Rudman Web Seaslugforum) W Seaslugforum) W Seaslugforum) Cladophora Chia 1989, own Chia 1989, own studies) Probably same food as Diatoms, detritus, pieces of Green algae (Rudman Cephalaspidea Green algae (Rudman 1972d) Green algae (Rudman Green algae (Rudman * 00 000 0+00 0000 +? 0+00+ 0+000 +0+00 + +++ + + +0 ++ ++

emplado, 1987 alavera, Murillo & alavera, T T Gibson & Chia, 1989 (d’Orbigny, 1841) (d’Orbigny, smaragdinus smaragdinus (Rüppell & Leuckart 1828) (Martens, 1879) Gould, 1859 (Quoy & Gaimard, 1833) (Quoy Philinopsis cyanea Haminoea antillarum Haminoea callidegenita Haminoea cymbalum Haminoea orteai Bulla vernicosa Phanerophthalmus Bullidae Haminoeidae Smaragdinellidae

203

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA ) auriformis P. *Thompson 1960, 1986, 1988, *Rudman 1972b ( 1911, Hoffmann 1911, Hoffmann 1939 “fossette glandulare” *Guiart 1901, Perrier & Fischer 12 12 histology Previous (references) Odhner 1926, Jensen 1996 Cimino et al. 1987a, Cimino et 1989b) *** PP OC (Szabo et al. 1996) Unknown *** Unknown OC, IA? (Guiart 1901, 11 Natural products (references) Unknown Unknown oraminifera Unknown oraminifera, Annelida, (Rudman 1972d) (Cedhagen 1996) Crustacea, Mollusca, Echinodermata, site (Rudman Web Seaslugforum) Herbivore ?Foraminifera ?Foraminifera F F Food (references) Food 10

gland

Interpallial Special defensive glands MDF-like structures MDF-like

0? 0? MDF TYPE MDF

00 *

Glandular stripe Glandular Blochmann

0?00 0+0 +? Spongy mantel glands mantel Spongy

456789 +0+00 +0+2 Hypobranchial gland Hypobranchial x + 0 ? 0 0 3 + +0 ++ +0 +

Compilation of available data on glandular structures, food and natural products Compilation of available okioka & Baba, 1964 (Broderip & Sowerby (Broderip & Sowerby 1829) calyculata Mikkelsen & Mikkelsen, & Mikkelsen, Mikkelsen 1984 Thiele, 1912 Lineus, 1758 T Smith, 1902 2 Genus and species, authorities cf Smaragdinella antarctica Newnesia Philine alata Scaphander lignarius Acteocina atrata ornatum Sagaminopteron Diaphanidae Cylichnidae Philinidae able 2 (continued) T Column 1 Higher taxon

204

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS E. cauze 1966, Wägele & Klussmann-Kolb 2005 & Klussmann 2003 Klussmann-Kolb Klussmann-Kolb 2005, *Marcus 1957 *Hoffmann 1939, *Hoffmann *Fernandez- Ovies 1983 Thompson 1960, Wägele 1997 al. et Kawaguti Klussmann-Kolb Klussmann-Kolb Wägele & Hoffmann 1939 Hoffmann *Vayssiere 1883, *Vayssiere Tridachia Tridachia )) ** ** Ireland & Faulkner 1981, Ireland & Faulkner Ksebati 1985, Ksebati & Schmitz,1985, Gavagnin et al 1996, 1997a, 2000 (some as 1994c) ** al. 2000, 1979, Fu et al. 2005) Manzo et 1993, 1994c) crispata NC (Horgen et al. 2000) et NC (Horgen PP (Ireland et al., 1979, PP (Ireland et PP (Gavagnin et al. 1992, PP (Gavagnin PP (Ireland & Scheuer et DT (Gavagnin al. 1992, Unknown Unknown

, (Jensen 1993) Unknown ** sp. (Horgen sp. (Horgen

, , et al. 2000, Jensen et 1993) (Jensen 1993) (Gavagnin et al. (Gavagnin 1994c) Chaetomorpha et al 1993, Gavagnin 1994, Trowbridge, 2004) (Jensen 1993) Green algae Caulerpa, Halimeda Bryopsis Codium vermilara Bryopsis Green algae (Jensen Udotea Chlorodesmis Derbesia tenuissima Caulerpa sub- contents of subepider- mal glands epithelial glands Unusual 0? * 0+00 0+0 0+0+ 00000Many 00000Many 00000 00000 00030 00000 00 0 00 0 0 +0 + +

an Hasselt, 1824 (Montagu, 1804) Gosliner, 1989 Gosliner, quadrispinosum (Mörch, 1863) (Pease, 1861) (Swainson, 1840) (Swainson, Thompson, 1980 v (Verany, 1853) (Verany, Siphopteron Siphopteron Runcina adriatica Elysia crispata Elysia viridis ocellatus Plakobranchus Thuridilla hopei Oxynoe viridis Elysia ornata Oxynoidae Runcinidae Plakobranchidae SACOGLOSSA

205

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA 1911, *Hoffmann 1911, *Hoffmann 1939, *Morton 1972 Perrier & Fischer 1911, Klussmann-Kolb 2004 1955, Klussmann-Kolb 2004 *Perrier & Fischer 12 12 histology Previous (references) Blochmann 1883, *Marcus & Marcus Fenical et al. 1979, Fenical et Miyamoto et al. 1995, de Yamada Nys et al. 1996, & Kigoshi 1997, al. 1998, Higuchi et al. 2000a,b, Rogers et 2001, & Paul Ginsburg al. Jongaramruong et 2002) Unknown Unknown ** 11 Natural products (references) MT DT SQ (Willan 1979, MT DT SQ (Willan , , eb site ortieria hornemannii W Seaslugforum) Delisea pulchra Laurencia filiformis Laurencia P Food (references) Food Green algae (Rudman

10

Opaline gland Green and red algae, Special defensive glands

MDF-like structures MDF-like MDF TYPE MDF

00 00

Glandular stripe Glandular Blochmann

+? Spongy mantel glands mantel Spongy

456789 +++ Hypobranchial gland Hypobranchial 00 3 +

Compilation of available data on glandular structures, food and natural products Compilation of available Guilding in Mörch, 1863) (Gmelin, 1791) 2 Genus and species, authorities soluta Akera Aplysia parvula Aplysiidae Akeridae Akeridae able 2 (continued) T Column 1 Higher taxon ANASPIDEA

206

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS Hoffmann 1939, Hoffmann Wägele & Klussmann-Kolb 2005 Mazzarelli 1893, 1939, Hoffmann Merton 1920, Eales 1921, Wägele 1997, Willan Wägele & 2000, Klussmann-Kolb 2004 Hoffmann 1939 Hoffmann Blochmann 1883, 1979, Gopichand & Schmitz 1980, Schmitz et al. 1981, Cimino et al. al. 1987b, Racioppi et al. et 1990, Kawamine 1991, Scheuer 1992, al. 2002) Appleton et (Minale & Riccio 1976, (Minale & Riccio al. 1983, Castedo et al. 1986, Jiménez et al. 1989, Quiñoá et al. 1997, et Ortega al. 2002, et Butzke Findlay & Li 2002) PP (Ciavatta et al. 1996a) et PP (Ciavatta Blochmann 1883, TS (Baalsrud 1950) OC NC (Fenical et al. OC NC (Fenical et MT DT SQ TS NC OC MT DT SQ , sp. aulkner 1992) (Rudman Web site (Rudman Web Seaslugforum) (Carefoot 1967, al. 1989, Quiñoá et F Laurencia Plocamium coccineum Enteromorpha, Opaline gland Cyanobacteria Opaline gland Opaline gland 00 000 0?00 0000 +++ 0+ 0?+ 0 ++

(Phipps, 1774) Blainville, 1817 Blainville, (Cuvier, 1817) (Cuvier, Cuvier, 1803 Cuvier, Aplysia punctata leachii Bursatella dolabrifera Dolabrifera Limacina helicina THECOSOMATA

207

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA ayssiere 1885, Wägele & Klussmann-Kolb 2005 1905, Hoffmann 1905, Hoffmann 1939 Wägele & Klussmann-Kolb 2005 Klussmann-Kolb Klussmann-Kolb 2005, *Mazzarelli 1897, *MacFarland 1966 V 12 12 histology Previous (references) Meisenheimer Hoffmann 1939, Hoffmann 1939 Hoffmann Wägele & )) *** C. ), Kattner mediterraneum Fisher et al. 1956, Fisher et McClintock & Janssen et 1990, Yoshida al. al. 1995, 1995, Bryan et McClintock & Baker 1997 (some as antarctica al. et 1989a, Gavagnin 1990, De Medeiros et al. 1990, 1991 (some as U. et al. 1998) 1990b, Teeyapant et al. et 1990b, Teeyapant al. 1999, 1993, Ebel et al. 2003) Thoms et TS TT (Baalsrud 1950, TS DG (Cimino et al. 1988a, DG (Cimino et 11 Natural products (references) NC (Cimino et al 1986a, , , Porifera (Cimino et al. 1988a, 1989a) Porifera (Cimino et al. al. 1990b, Becerro et 2003) Thecosomata Food (references) Food Aplysina aerophoba Geodia cydonium 10

gland glandular cells gland

Dorsal mantle Opaline Dorsal mantle Special defensive glands

MDF-like structures MDF-like

MDF TYPE MDF

Glandular stripe Glandular

Blochmann Spongy mantel glands mantel Spongy

00000 00000 00000 456789 Hypobranchial gland Hypobranchial 0 0 3 0

Compilation of available data on glandular structures, food and natural products Compilation of available (Gmelin, 1791) (Phipps, 1774) (Lightfoot, 1786) ylodina perversa 2 Genus and species, authorities Clione limacina T umbraculum Umbraculum Tylodinidae Umbraculidae able 2 (continued) T Column 1 Higher taxon GYMNOSOMATA TYLODINOIDEA

208

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS Tsurnamal 1973, Thompson & Colman 1984, Wägele & Klussmann-Kolb 2005 *1969, Thompson & Colman 1984 Wägele & Willan Willan Wägele & 2000 Wägele 1997 Hoffmann 1939 Hoffmann Wägele 1997 Marbach & *Thompson 1960, Hoffmann 1939 Hoffmann Wägele 1997, )) B. aurantiaca vila et al. 2000) A (as Thompson, 1969, 1970, Thompson Edmunds & 1972, Marbach & Tsurnamal 1973, Thompson & Colman 1984) Thompson & Colman 1984) data) SQ (Iken et al. 1998, et SQ (Iken Unknown Unknown IA OC (Avila 1992, 1993 IA OC (Avila IA ( Franc 1968, IA (Avila 1992, 1993, IA (Avila IA (Avila, unpublished IA (Avila,

Bryozoa, Ceratoisis, Bryozoa, Crinoidea, Crustacea, Ophiuroidea Wägele (omnivore al. et 1989a,c, Avila 2000) Crinoidea, Crustacea, Ophiuroidea Wägele (omnivore 1989a,c) feeder (Hain et al. feeder (Hain et 1993) (Rudman Web site (Rudman Web Seaslugforum) site Seaslugforum) Porifera, Ceratoisis, Nonselective deposit Nonselective Porifera ?Anthozoa Porifera (Rudman Web Web Porifera (Rudman gland acid gland gland acid gland gland gland Median buccal Median buccal Subepithelial Median buccal Median buccal Subepithelial Median buccal Median buccal Median buccal Median buccal 00000 00000 00000 00000 00000 00000 00000 0 0 0 0 0 0 0

illan & Bertsch, 1987 Eliot, 1907 Thiele, 1912 (Thiele, 1912) (Vayssière, 1896) (Vayssière, (Rüppell & Leuckart 1828) W (Risso, 1826) omthompsonia antarctica Bathydoris hogdsoni Bathydoris clavigera T Berthellina edwardsii Berthellina edwardsii Berthellina citrina Bathyberthella antarctica Berthella stellata Bathydorididae Pleurobranchidae BRANCHOIDEA NUDIBRANCHIA ANTHOBRANCHIA PLEURO-

209 7044_book.fm Page 210 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA 2001 Thompson 1988, Wägele 1997, *Edmunds 1968 Thompson 1960, Wägele 1997 Wägele 1997 Wägele & Cervera Wägele & Cervera *Marcus 1959, Potts 1981, * Thompson 1960, 12 12 histology Previous (references) Clubb 1892, Edmunds 1970, 1972, Voogt 1968, 1973, Potts 1970, 1981, Thompson 1960) Unknown ** Unknown Unknown Unknown TS IA? (Herdmann & Unknown ** Unknown 11 Natural products (references) , Ircinia

Porifera, Bryozoa (McDonald & site) Web Nybakken & Nybakken Web site) Web & Nybakken & Nybakken Web site) Web & Nybakken Nybakken Web site) Web Nybakken Nybakken Web site) Web Nybakken Eudendrium, Scrupocellaria, Ascidiacea (McDonald Ascidiacea (McDonald Balanidae, Bryozoa (McDonald & Bryozoa (McDonald & Food (references) Food 10

Special defensive glands

MDF-like structures MDF-like

MDF TYPE MDF

Glandular stripe Glandular

Blochmann Spongy mantel glands mantel Spongy

00000 00000 00000 00000 00000 456789 Hypobranchial gland Hypobranchial 0 0 0 0 0 3

Compilation of available data on glandular structures, food and natural products Compilation of available apania maculata Haefelfinger, 1960 Haefelfinger, (Montagu, 1808) (Risso, 1818) (Linné, 1767) Abildgaard in Müller 1789 Tr Goniodoris nodosa Ancula gibbosa Onchidoris bilamellata Onchidoris 2 Genus and species, authorities Acanthodoris pilosa Goniodorididae Doridoidea Onchidorididae able 2 (continued) T Column 1 Higher taxon

210 7044_book.fm Page 211 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS Wägele & Willan Willan Wägele & 2000 Klussmann-Kolb Klussmann-Kolb 2005 Wägele 1997 2001, *Fischer 1892, & *MacFarland O’Donoghue 1929 Wägele 1997, Wägele 1997 Wägele & Thompson, 1960, Schrödl & Wägele Schrödl & Marcus 1959, 1998) NC (Graziani & Andersen NC (Graziani & Unknown Unknown Unknown Unknown ** Unknown Unknown Unknown ** Unknown Unknown Unknown , other Brown 1984) Brown Nybakken Web site) Web Nybakken Nybakken Web site) Web Nybakken Nybakken Web site) Web Nybakken polycerids (Pola et al. polycerids (Pola et 2005) Nybakken Web site) Web Nybakken Nybakken Web site) Web Nybakken opisthobranchs (McDonald & site) Web Nybakken Nybakken Web site) Web Nybakken Bryozoa (Thompson & Bryozoa (McDonald & Bryozoa (McDonald & Bryozoa (McDonald & Probably other Bryozoa (McDonald & Bryozoa (McDonald & Plakobranchus Bryozoa (McDonald & subepi- thelial glands, additional glands in cerata at gills glandular notum epithelium Extremely 0 * 00020 000+ 00000 00000Many 00000Many 00000 00000 00000 00000 00000 0 0 0 0 0 0 0 0 0

errill, 1880 olycerella emertoni olycerella olycera quadrilineata olycera (Müller, 1776) (Müller, MacFarland, 1905 MacFarland, Alder & Hancock, 1862 (Montagu, 1815) (Bergh, 1877) (Bergh, V (Müller, 1776) (Müller, (Eliot, 1908) Bergh, 1869 Bergh, Limacia clavigera Laila cockerelli Crimora papillata Crimora pennigera Thecacera Roboastra gracilis Roboastra P P Gymnodoris striata Corambe lucea Corambe Triophidae Polyceridae Gymnodorididae Corambidae

211 7044_book.fm Page 212 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA *Kress 1981 Potts 1981 Wägele 1997, 12 12 histology Previous (references) yama &Tanaka yama &Tanaka aulkner 1991, Avila Avila aulkner 1991, F al. et 1995, Gavagnin 1995, 1999a, 1999b, 2003a, 2003b, Iken et al. 2002) 1993b, Zubía et al. 1993, al. 1993, Soriente et al. 2000 Armstrong et 1995)) Avila (see also 1956) DG (Davies-Coleman & DG (Davies-Coleman TS TT DG (Cimino et al. TT DG (Cimino et TS NC (Carmely et al. 1989) NC (Carmely et TS (To TS Unknown Unknown 11 Natural products (references)

, spp., Cynachira barbata Cynachira Porifera (Wägele 1989a, et al. Iken 2002) Nybakken Web site) Web Nybakken Porifera (McDonald & site, Web Nybakken al. 1989) Carmely et (Wägele 1989a) Nybakken Web site) Web Nybakken Rossella Porifera (McDonald & Leucetta chagosensis, Porifera/Calcarea Bryozoa (McDonald & Food (references) Food 10

gland MDF-like structures

Median buccal Median buccal 2 types of Special defensive glands

MDF-like structures MDF-like

MDF TYPE MDF

Glandular stripe Glandular

Blochmann Spongy mantel glands mantel Spongy

????? 00000 00000 000000 000000 0000+ 456789 Hypobranchial gland Hypobranchial ? 0 0 0 0 3 0

(Bergh,

guelenensis Compilation of available data on glandular structures, food and natural products Compilation of available ker 1884) (Eliot, 1913) (Rapp, 1827) Bergh 1875 Bergh Thiele, 1912 ceylonicus 1858) (Kelaart, Austrodoris Austrodoris Archidoris pseudoargus Archidoris Actinocyclus japonicus Notodoris citrina Aegires albus Aegires 2 Genus and species, authorities Plocamopherus Dorididae Aegiridae able 2 (continued) T Column 1 Higher taxon

212 7044_book.fm Page 213 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS vila 1993, Avila Avila vila 1993, vila 1993, Avila Avila vila 1993, & Durfort 1996, Wägele 1997 *Foale & Willan Willan & *Foale 1987 A & Durfort 1996 A Wägele 1997, Edmunds 1968, TS (Voogt 1973, TS (Voogt vila 1992, 1993) vila 1995)) Castiello et al. 1978, 1980 Cimino et al. 1980b, 1981, 1982, 1985a, 1989c, 1990c A 1986b, 1988c, Porcelli al. 1989, Gavagnin et Avila et al. 1990, 1997b, al. et al. 1990a, Pani et 1992, 1993, Avila 1991, al. De Petrocellis et 1991, 1996, Granato et al. 2000, Fontana see also al. 2003 (but et A TS (Avila 1992, 1993) TS (Avila AC Unknown ** Unknown DG TS NC (Cimino et al. DG

Reniera) (Reniera) , Porifera vila et al. 1990a, vila et vila 1993) etrosia ficiformis, etrosia Nybakken Web site, Web Nybakken al. 2002) et Megina Haliclona fulva, site, Web Nybakken al. 1978, Castiello et al. 1980, Cimino et 1980b, 1982, al. et Cattaneo-Vietti Avila 1993, 2001 1993, 1995, 1996, Gemballa & Schermutzki 2004) Nybakken Web site) Web Nybakken sanguinea (McDonald & Website, Nybakken A A Bryozoa (McDonald & Porifera, Porifera (McDonald & P Porifera (McDonald & Hymeniacidon 00000 00000 00000 00000 0 0 0 0

Linné,

eltodoris atromaculata (Linneus, 1767) (Bergh, 1880) (Bergh, (Cuvier, 1804) (Cuvier, 1758 orunna tomentosa Platydoris argo P J Doris verrucosa

213 7044_book.fm Page 214 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA ) (Cadlina rumia 1987 *Marcus 1955 *Foale & Willan Willan & *Foale 12 12 histology Previous (references) ubanek et al. 1997, ubanek et ischler 1990, Faulkner ischler 1990, Faulkner ontana et al. 1995, ontana et 1981, 1982, Thompson 1981, 1982, 1982, et Walker al. 1982, al. 1985, Gustafson et Andersen Gustafson & & 1985, Tischler Andersen 1989, T et et Tischler al. 1990, al. al. et 1991, Burgoyne 1993, Dumdei 1994, F al. 1997a, Dumdei et K 1998 2000, Kubanek Avila see also (but 1995)) Anderson 1971, 1973) SQ DT ST (Hellou et al. SQ DT ST (Hellou et TT (Coulom 1966, 11 Natural products (references)

sp., , Axinella ischler & Andersen ischler & D. amblia, D. etheria, D. D. herbacea, Dysidea sp., Aplysilla glacialis, site, Web Nybakken Thompson et al. 1982, al. 1982, Hellou et T 1989) pennata site, Web Nybakken 2001) Ong & Penney, Porifera (McDonald & Dysidea fragilis, Dysidea fragilis, Porifera (McDonald & Ophlitaspongia Food (references) Food 10

tubercles

Glands in Special defensive glands

MDF-like structures MDF-like

MDF TYPE MDF

Glandular stripe Glandular

Blochmann Spongy mantel glands mantel Spongy

00010 00000 456789 Hypobranchial gland Hypobranchial 0 3 0

Compilation of available data on glandular structures, food and natural products Compilation of available MacFarland, 1905 MacFarland, MacFarland, 1905 MacFarland, 2 Cadlina marginata Genus and species, authorities Rostanga pulchra Chromodorididae able 2 (continued) T Column 1 Higher taxon

214 7044_book.fm Page 215 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS vila & Paul 1997 vila & Paul et al. 1991 & Durfort 1996, *Marcus 1955 (Glossodoris) neona) 2000 A García-Gómez Avila 1993, Avila Avila 1993, Avila Wägele & Willan Willan Wägele & vila & Paul 1997) vila & Paul vila 1992, 1993, 1995) vila 1992, 1993, 1995) 1999b) A A Cimino et al. 1990a, Cimino et al. 1992, et Gavagnin Avila al. 1992, Puliti et 1992, 1993, 1995) A 1995) ST (Gavagnin et al. 2004) et ST (Gavagnin DT (Fontana et al. 1997, et DT (Fontana ST (Rogers & Paul 1991, ST (Rogers & Paul Unknown ** Unknown Unknown ** Unknown DT (Avila et al. 1990b, et DT (Avila DT (Avila et al. 1990b, et DT (Avila DT (Avila et al. 1990b, et DT (Avila SQ, ST (Fontana et al. et SQ, ST (Fontana ST (Mollo et al. 2005) ST (Mollo et ST (Mollo et al. 2005) ST (Mollo et sp., Nybakken Web site) Web Nybakken Nybakken Web site) Web Nybakken Porifera 1997) & Paul (Avila Nybakken Web site) Web Nybakken Nybakken Web site) Web Nybakken Nybakken Web site) Web Nybakken Nybakken Web site, Web Nybakken Barbour 1979) (Mollo et al. 2005) (Mollo et (Mollo et al. 2005) (Mollo et Porifera (McDonald & Porifera (McDonald & Cacospongia Porifera (McDonald & Porifera (McDonald & Porifera (Avila 1993)Porifera (Avila 1993, 1995) DT (Avila Porifera (McDonald & Porifera (McDonald & Dysidea Dysidea ???+? ???+? ???+? 00030 00030 00030 00010 00030 00030 00030 00030 00010 ? ? ? 0 0 0 0 0 0 0 0 0 )

rufomarginata 1890) (Bergh, (Rüppel & Leuckart, 1828) atromarginata 1804) (Cuvier, westraliensis (O’Donoghue, 1925) Collingwood, 1881 Collingwood, (Laurillard, 1831) (Rapp, 1827) (Semper in Bergh, 1876 (Semper in Bergh, (Gray J.E., 1827) Ortea and Pérez, 1983 (Verany, 1846) (Verany, (Linneus, 1767) Glossodoris Glossodoris pallida Glossodoris Chromodoris Chromodoris tumulifera Chromodoris Chromodoris purpurea Chromodoris Chromodoris luteorosea Chromodoris Chromodoris krohni Chromodoris Ceratosoma gracillimum Ceratosoma Ceratosoma trilobatum Ceratosoma Chromodoris britoi Chromodoris Cadlina laevis

215 7044_book.fm Page 216 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA vila 1993, vila & Durfort vila 1993, Avila Avila vila 1993, & Durfort 1996 et al. 1990, Wägele 1997 et al. 1990, A A 1996 A García-Gómez García-Gómez 12 12 histology Previous (references) sp)) Hypselodoris ontana et al. 1993) ontana et 1993a, Avila 1992, 1993a, Avila 1993) (as F ST (Cimino et al 1982, SQ (Avila 1993) SQ (Avila SQ (Avila 1993 SQ (Avila SQ (Avila 1992, 1993, SQ (Avila Unknown Unknown 11 Natural products (references) SQ (Fontana et al. 1994b) et SQ (Fontana ,

vila 1993) ontana et al. 1993) ontana et Porifera (McDonald & site, Web Nybakken al. 1973, Cimino et 1974, 1982, 1993a, A Porifera (Avila 1993, Porifera (Avila McDonald & site) Web Nybakken Porifera (Avila, 1993) Porifera (Avila, Porifera (McDonald & site, Web Nybakken Bouchet & Ortea 1980, F Nybakken Web site) Web Nybakken Cacospongia mollior , Dysidea avara Dysidea, Dysidea fragilis, Food (references) Food Porifera (McDonald & 10

Special defensive glands

MDF-like structures MDF-like MDF TYPE MDF

+? +?

Glandular stripe Glandular

Blochmann Spongy mantel glands mantel Spongy

???+? ??? ??? 00020 00000 00030 456789 Hypobranchial gland Hypobranchial ? ? ? 0 0 0 3

Compilation of available data on glandular structures, food and natural products Compilation of available Ortea, 1996 (Verany, 1846) (Verany, (Pruvot-Fol, 1951) (Pruvot-Fol, Bouchet & Ortea, 1980 (Marcus & Marcus, 1967) (Pruvot-Fol, 1953) (Pruvot-Fol, Hypselodoris gasconi Hypselodoris orsinii Hypselodoris fontandraui 2 Hypselodoris cantabrica Genus and species, authorities Hypselodoris bayeri Hypselodoris bilineata able 2 (continued) T Column 1 Higher taxon

216 7044_book.fm Page 217 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS ) ), ) ), H. webbi vila 1993, vila & Durfort vila 1993, Avila Avila vila 1993, (Noumea decussata Klussmann-Kolb 2005 & Durfort 1996 et al. 1991, Wägele 1997, Willan Wägele & 2000 et al. 1990 (as et H. webbi García-Gómez al. 1991 (as et H. elegans A A 1996 (as *Risbec 1953 Wägele & A García-Gómez García-Gómez )) H. webbi vila 1992, 1993, vila 1992, 1993, Avila Avila vila 1992, 1993, vila et al. 1990b, 1991b, ontana et al. 1993) ontana et ontana et al. 1993, ontana et ontana et al. 1994a, b ontana et 1982, Avila 1992, 1993, Avila 1982, Cimino & Sodano 1989, A F A F 1994b) Cimino & Sodano 1989, A al. 1990b, 1991b, et F (some as Unknown Unknown SQ (Cimino et al. 1980b, SQ (Cimino et SQ (Cimino et al. 1982, SQ (Cimino et SQ (Cimino et al. 1982, SQ (Cimino et , , , Porifera vila et al. 1990b, vila et vila 1993, Fontana vila 1993, Fontana ontana et al. 1994a,b) Nybakken Web site) Web Nybakken Porifera (McDonald & site, Web Nybakken Cimino & Sodano 1993, 1989, Avila A 1991b) Porifera (McDonald & site, Web Nybakken A et al. 1993) (Avila 1993, Cimino & (Avila Avila Sodano 1989, al. 1990b, 1991b, et F Fasciospongia Fasciospongia cavernosa, (= Microciona toxystila), Pleraplysilla spinifera, Porifera (McDonald & Dysidea fragilis Dysidea fragilis Dysidea fragilis 0? ??? 00030 00020 00030 00030 ? 0 0 0 0

crocea cf. Rudman, 1986 (Garrett, 1873) (Risso, 1818) (Cantraine, 1835) (Schultz, 1836) Noumea Risbecia tryoni Hypselodoris villafranca Hypselodoris tricolor Hypselodoris picta

217 7044_book.fm Page 218 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA vila 1993, Avila Avila vila 1993, Wägele et al. Wägele et 1999 & Durfort 1996 A *Brodie 2005 12 12 histology Previous (references) vila et al. 1991a, vila et ontana et al. 1999a, ontana et 1982, 1983, 1985b, Avila 1986a, 1988b, al. et Avila 1992, 1993, al. et 1991a, Fontana 1999a, 2000) et al. 1980b, 1982, et 1985a, 1986a, 1988b, 1992, 1993, Avila 1990b, A F 2000) SQ (Okuda et al. 1983)SQ (Okuda et Wägele 1997, ** Unknown SQ (Cimino et al 1981, SQ ST MO OC (Cimino 11 Natural products (references) Porifera Nybakken Web site) Web Nybakken Nybakken Web site) Web Nybakken Fasciospongia Fasciospongia cavernosa (= Microciona toxystila), Spongia officinalis, (McDonald & site, Web Nybakken al. 1975, Cimino et 1980b, 1982, 1985a, 1986a, 1990b) Porifera (McDonald & Porifera (McDonald & Ircinia fasciculata, Ircinia Food (references) Food 10

Special defensive glands

MDF-like structures MDF-like

MDF TYPE MDF

Glandular stripe Glandular

Blochmann Spongy mantel glands mantel Spongy

0000+ 00000 00000 00000 456789 Hypobranchial gland Hypobranchial 0 0 0 3 0

Compilation of available data on glandular structures, food and natural products Compilation of available Gosliner, Schaefer & Gosliner, Millen, 1999 (Stimpson, 1855) (Cuvier, 1804) (Cuvier, (Rapp, 1827) Doriopsilla gemela nigra Dendrodoris 2 Dendrodoris limbata Dendrodoris Genus and species, authorities grandiflora Dendrodoris Dendrodorididae able 2 (continued) T Column 1 Higher taxon

218 7044_book.fm Page 219 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS ) australis Klussmann-Kolb Klussmann-Kolb 2005 *Marcus 1959 (as T. Wägele & *Thompson 1960, Hoffmann 1939 Hoffmann Wägele 1997 ) pulitzeri P. 1953) 1986a (as Avila see also (but 1995)) ** Kassühlke et al. 1991, et Kassühlke al. 1991, Fusetani et 1992, Okino et al. 1996, al. 1998, Hirota et al. 1997b, Dumdei et al. 1997, Simpson et al. 2000, Garson et Wright 2003, Manzo et al. 2004) Unknown Unknown Vevers & NC (Kennedy Unknown Unknown Unknown SQ (Cimino et al. 1982, SQ (Cimino et SQ, DT (Karuso 1987, , cf , sp., (McDonald & site) Web Nybakken (McDonald & site) Web Nybakken (McDonald & site) Web Nybakken Porifera (Cimino et al. 1982, unpublished data of HW) Halichondria lendenfeldi, Phakellia carduus al. 1991, Kassühlke et al. 1991, Dumdei et et al. 1997b, Wright 2003) (Karuso 1987, Fusetani Octocorallia Octocorallia Octocorallia Axinella Acanthella cavernosa Densa iolet glands iolet glands iolet glands iolet glands in epidermis in epidermis in epidermis grouped and into sunken notum 0?00 0?00V ????? 00000 00000V 00000V 00000V 00000 ? 0 0 0 0 00 00 0

ritonia antarctica ritonia plebeia ritonia festiva ritonia challengeriana Pfeffer in Martens & Pfeffer 1886 Pfeffer, (Risso, 1818) Johnston, 1828 (Stearns, 1873) (Cuvier, 1804) (Cuvier, Bergh, 1899 Bergh, Bergh, 1884 Bergh, Aradas, 1847 T T Marionia blainvillea T T Phyllidiella pustulosa Doridoxa ingolfiana Phyllidia flava Dendronotoidea Tritoniidae Doridoxidae (1) Phyllidiidae CLADOBRANCHIA DEXIARCHIA

219 7044_book.fm Page 220 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA Wägele 1997 Vayssière 1888, Vayssière Wägele 1997 Wägele 1997 12 12 histology Previous (references) Manukhin,1962, Voogt Manukhin,1962, Voogt 1970, 1972, 1973) 1994, Bryan et al. 1998) 1994, Bryan et Unknown Unknown Unknown TS (Buznikov & TS (Buznikov Unknown Unknown Unknown OC (McClintock et al. OC (McClintock et Unknown 11 Natural products (references) xacorallia & Nybakken Web site) Web & Nybakken & Nybakken Web site) Web & Nybakken & Nybakken Web site) Web & Nybakken (McDonald & site) Web Nybakken (McDonald & site) Web Nybakken & Nybakken Web site) Web & Nybakken Synascidia (McDonald site) Web & Nybakken (McDonald & site) Web Nybakken Hydrozoa (McDonald Hydrozoa (McDonald He Hydrozoa (McDonald Hydrozoa, Octocorallia, Bryozoa Hexacorallia, Hydrozoa (McDonald Octocorallia, Food (references) Food Octocorallia 10

iolet glands iolet glands iolet glands iolet glands iolet glands in epidermis in epidermis in epidermis in epidermis in epidermis

Special defensive glands MDF-like structures MDF-like

0V 0V 0V

MDF TYPE MDF

Glandular stripe Glandular Blochmann

0+0 0+0 0+0 Spongy mantel glands mantel Spongy

00000V 00000 00000V 00000 00000 456789 Hypobranchial gland Hypobranchial 0 00 0 00 0 00 0 3 0

Compilation of available data on glandular structures, food and natural products Compilation of available ritoniella belli ritonia vorax (Adams & Reeve in (Adams & Reeve Adams, 1848) Johnson, 1984 Cooper, 1863 Cooper, (Gmelin, 1791) (Ascanius, 1774) Eliot, 1908 Eliot, 1907 Odhner, 1926 Odhner, Bornella stellifer Bornella anguilla Dendronotus iris Dendronotus Lomanotus vermiformis Doto coronata Dendronotus frondosus Dendronotus 2 T Genus and species, authorities T Bornellidae Lomanotidae Dotidae Dendronotidae able 2 (continued) T Column 1 Higher taxon

220 7044_book.fm Page 221 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS H. ) ), 1997 ) olb 1998, *Bergh olb 1998, *Bergh 1866 1995a, Willan Wägele & 2000 Hoffmann 1939 Hoffmann Crampton 1984 (M. fimbriata 2000 (H. burni ryrca K Kolb 1998 Kolb Wägele et al. Wägele et *Thompson & Willan & *Wägele Born 1910, *Thompson 1972 *Marcus 1957 ( 1988, 1990) 1983, Gustafson & Andersen 1985, Barsby et al. 2002) Unknown DT (Guerriero et al. 1987, Unknown Unknown Unknown MT TS (Ayer & Andersen & TS (Ayer MT Unknown Unknown Unknown Unknown Wägele Unknown Unknown

etillum cynomorium, (Rudman Web (Rudman Web site Seaslugforum) Octocorallia (McDonald & site, Web Nybakken al. 1987, Guerriero et 1988, 1990) Bullough 1996) (McDonald & site) Web Nybakken Appendicularia (McDonald & site) Web Nybakken (McDonald & site) Web Nybakken & Nybakken Web site) Web & Nybakken Ver Hydrozoa Bryozoa (Barnes & Crustacea larvae Crustacea larvae Medusae of Hydrozoa, Hydrozoa (McDonald ferent ginal sacs ginal sacs ginal sacs Octocorallia ginal sacs Unknown ginal sacs MDF-like MDF-like structures 0+00 0+00 00000Mar 0000+Two dif 0000+Two 0000+ 00000Mar 00000Mar 00000Mar 00000Mar 00000 0 0 0 0 0 00 0 0 00

sp. 0

ayssière, 1906 Rafinesque, 1814 (Gould, 1853) Eliot, 1903 (Delle Chiaje, 1824) Rafinesque, 1814 V semistriatus Baba, 1949 Peron & Lesueur, 1810 Peron & Lesueur, (Hesse, 1872) Armina maculata Armina neapolitana Melibe leonina Armina tigrina Crosslandia viridis Crosslandia Dermatobranchus Charcotia granulosa Charcotia Dermatobranchus Dermatobranchus Hancockia uncinata Hancockia Phylliroe bucephala Phylliroe ethydidae Arminoidea Arminidae T Scyllaeidae Charcotiidae Hancockiidae Phylliroidae

221 7044_book.fm Page 222 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA ) ) Telarma Telarma rinchese 1881, (M. sanguinea Hoffmann 1939 Hoffmann antarctica (as Wägele 1997 *Baba 1935 T Wägele 1997 Wägele 1991, Wägele 1991 12 12 histology Previous (references) 1986, Cimino et al. 1986, Cimino et al. 1986a, Giordano et 2000) Unknown Unknown NC (Sodano & Spinella Unknown Unknown Unknown Unknown Unknown 11 Natural products (references) (Wägele 1990) Nybakken Web site) Web Nybakken Nybakken Web site) Web Nybakken site) Web Nybakken Nybakken Web site) Web Nybakken 1996) (Barnes & Bullough Actiniaria Bryozoa (McDonald & Bryozoa (McDonald & Bryozoa (McDonald & Bryozoa (McDonald & Bryozoa Unknown Unknown Bryozoa Unknown Food (references) Food 10

Special defensive glands

MDF-like structures MDF-like

MDF TYPE MDF

Glandular stripe Glandular Blochmann

0+00 0+00 0?00 0+00 0+00 0+00 0+00 Spongy mantel glands mantel Spongy

00000 00000 456789 Hypobranchial gland Hypobranchial 00 00 0 0 00 00 00 00 3 00

Compilation of available data on glandular structures, food and natural products Compilation of available Eliot, 1907 Alder & Hancock, 1864 (Delle Chiaje, 1841) Miller & Willan, 1986 Willan, Miller & Bergh, 1907 Bergh, MacFarland, 1912 MacFarland, quadrangularis Thiele, 1912 gracilidens 1944 Odhner, (Odhner, 1934) (Odhner, anolus cristatus anolus mokohinau anolus capensis Madrella ferruginosa Madrella J Notaeolidia depressa J J Dirona albolineata Dirona Pseudotritonia Pseudotritonia 2 Genus and species, authorities Pseudotritonia antarctica Madrellidae Aeolidoidea Notaeolidiidae Zephyrinidae Dironidae able 2 (continued) T Column 1 Higher taxon

222 7044_book.fm Page 223 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Streble 1968 Schulze & Wägele 1998 *Trinchese 1881 *Trinchese (several Flabellina species), *Marcus du Bois- 1970 Reymond 1995b Wägele 1997 Hoffmann 1939, Hoffmann Evans 1922 Evans Wägele 1997, Wägele 1997 Wägele 1997, Wägele et al. Wägele et Howe & Harris 1978) Howe 1980a,b) Unknown OC (Rogers, 1977, Unknown Unknown Unknown Unknown Unknown Unknown TS (Cimino et al. TS (Cimino et Unknown Unknown and other

sp., xacorallia & Nybakken Web site) Web & Nybakken (McDonald & site) Web Nybakken (Calado & Urgorri (Calado & Urgorri 2001) ?Octocorallia (McDonald & site) Web Nybakken hydrozoans (Thompson & Brown 1984) & Nybakken Web site) Web & Nybakken & Nybakken Web site) Web & Nybakken & Nybakken Web site, Web & Nybakken Cimino et al. 1980a, b) (Wägele 1990) Nybakken Web site) Web Nybakken Hydrozoa (McDonald He Probably unknown Unknown Eggs of blenniid fish Hydrozoa, Eudendrium Hydrozoa (McDonald Hydrozoa (McDonald Eudendrium Hydrozoa (McDonald Actiniaria Octocorallia (McDonald & 0+00 0+00 0+00 0+00 0+00 0+00 0+00 0+00 0+00 00000 00000 00000 0 0 0 00 00 00 00 00 00 00 00 00

Burn, 1966 (Linneus, 1761) 1905 Bergh, (Alder & Hancock, 1854) (Verany, 1846) (Verany, (Montagu, 1815) Eliot, 1907 (Alder & Hancock, 1844) Schmekel, 1973 Schmekel, (Gmelin, 1791) Wägele, 1990 Eliot, 1905 Protaeolidiella juliae Protaeolidiella Aeolidia papillosa Cerberilla amboinensis Calma glaucoides Calmella cavolinii Flabellina pedata Flabellina falklandica Flabellina gracilis Flabellina affinis Flabellina babai Notaeolidia schmekelae Notaeolidia gigas Aeolidiidae Calmidae Flabellinidae

223 7044_book.fm Page 224 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA ) indica P. vila et al. 1998 vila et A *Rudman 1981b (as Wägele 1997, Wägele 1997, Wägele 1997 12 12 histology Previous (references) Slattery et al. 1998) Slattery et 1980a,b, Ciavatta et al. et 1980a,b, Ciavatta 1996b) Unknown DT (Avila et al. 1998, et DT (Avila Unknown Unknown TS (Cimino et al. et TS (Cimino 11 Natural products (references) , (Xenia) sp., sp., , Octocorallia 2004) Sinularia et al. 1998, (Avila al. 1998, Slattery et McDonald & site) Web Nybakken (McDonald & site, Web Nybakken al. 2005) et Burghardt & Nybakken Web site) Web & Nybakken Hydrozoa (McDonald site, Web & Nybakken Cimino et al. 1980a, b) S. polydactyla, Octocorallia Wägele & (Burghardt Sinularia maxima Octocorallia Briareum Hydrozoa (McDonald Eudendrium Food (references) Food 10

Special defensive glands

MDF-like structures MDF-like

MDF TYPE MDF

Glandular stripe Glandular Blochmann

0+00 0+00 Spongy mantel glands mantel Spongy

00000 456789 Hypobranchial gland Hypobranchial 00 000?00 000?00 0 00 3

Compilation of available data on glandular structures, food and natural products Compilation of available vila et al., 1998 vila et jakobsenae Wägele, & Burghardt 2004 A (Bergh, 1896) (Bergh, (D«Orbigny, 1847) (D«Orbigny, (Gmelin, 1791) Phyllodesmium Phyllodesmium guamensis Phyllodesmium briareum Phidiana lottini 2 peregrina Cratena Genus and species, authorities Facelinidae able 2 (continued) T Column 1 Higher taxon

224 7044_book.fm Page 225 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS eiss & Wägele eiss & eiss & Wägele eiss & oung et al. 1986, oung et Reymond 1971 Reymond W 1998 Reymond 1979 Reymond species), (several W 1998 Wägele 1997 *Rudman 1981a Edmunds 1966a Wägele 1997 *Marcus du Bois- Y Marcus du Bois- Trinchese 1877, Trinchese *Edmunds 1966a, Hoffmann 1939, Hoffmann Rudman 1982, )) Trinchesia Arimoto et al. 1990, Arimoto et 1993) Abramson et al. 1989) Abramson et (as Unknown ** Unknown PP (Ireland et al. 1984, PP (Ireland et OC ** (Young et al. 1986, OC ** (Young Unknown ** Unknown Unknown TT (Bürgin-Wyss 1961 TT (Bürgin-Wyss Unknown Unknown Unknown Unknown (www.hku.hk/ecology/ porcupine/por28/ 28-glance-siphonaria. htm#index2) (Stanisic 1998) (Stanisic 1998) bacteria (Stanisic 1998) marine-education/ onchidella.htm & Nybakken Web site) Web & Nybakken & Brown 1984, & Brown McDonald & site) Web Nybakken & Nybakken Web site) Web & Nybakken Siphonophora (McDonald & site) Web Nybakken & Nybakken Web site) Web & Nybakken & Nybakken Web site) Web & Nybakken Cyanobacteria Live algae algae Live Live algae Live Live algae algae Live Diatoms, detritus, www.seanature.co.uk/ Hydrozoa (McDonald Hydrozoa (Thompson Hydrozoa (McDonald Hydrozoa, Hydrozoa (McDonald Octocorallia Hydrozoa (McDonald repugna- torial glands 0+00 0+00 0?00 0000+ 00000 0000+Many 0000+Many 0000+ 00000 00000 00000 0 0 0 0 00 0 00 00 0 0

gipes tergipes orster, 1777 orster, (Lamarck 1819) (Cuvier, 1830) (Cuvier, Dall, 1871 (Cuvier, 1817) (Cuvier, (Forskål, 1771) (Forskål, (Montagu, 1804) (Alder & Hancock, 1848) F (Vicente, 1975) (Vicente, (Angas, 1865) Siphonaria javanica Onchidium verruculatum Onchidium Onchidella borealis Onchidella Onchidella celtica Onchidella Ter Cuthona caerulea Eubranchus exiguus Eubranchus Glaucus atlanticus Piseinotecus gabinieri Pteraeolidia ianthina Pteraeolidia gipedidae Siphonariidae Onchidiidae Ter Eubranchidae Glaucidae Piseinotecidae PULMONATA

225 7044_book.fm Page 226 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA Wise 1996 Wise 12 12 histology Previous (references) do not produce an acid secretion (Avila,

s, DT diterpenes, SQ sesquiterpenes, ST a few species have been investigated. For a For been investigated. species have a few the substance is given, instead of the names of the substance is given, Unknown 11 Natural products (references) one to four MDF-like structures were observed.

of data, due to inappropriate histological slides or and eicosanoids, PP polyproprionates. ** indicates

ence. Very often, only the general groups of prey are Very ence. gory of Umbraculum umbraculum Umbraculum and arious polychaetes, ectoparasites on v and other bivalves gastropods (Ponder & 1998) de Keyzer Pyramidellids are Food (references) Food 10 able 3. A question mark indicates lack able 3.

Scaphander lignarius

Special defensive glands

MDF-like structures MDF-like MDF TYPE MDF o MFDs were found. Column 8: * indicates that only

vestigations and pictures on probably defensive glandular structures. *indicates that other species of the glandular and pictures on probably defensive vestigations

xcept for the members of the Chromodorididae, where only

Glandular stripe Glandular Philine alata,

ganic acids, MO compounds with mixed origin, MT monoterpene

Blochmann

Spongy mantel glands mantel Spongy The cate natural products. Column 11: summarises known ven.

00000 456789 Hypobranchial gland Hypobranchial 3 +

Compilation of available data on glandular structures, food and natural products Compilation of available Adams, 1854 2 Genus and species, authorities sulcata Pyramidella All species listed have been re-investigated by histological means, e been re-investigated All species listed have

Pyramidellidae able 2 (continued) BRANCHIA that other species of the same genus have been chemically studied. *** that other species of the same genus have Column 9: indicates special glandular structures, which are typical of only a small group. Column 10: indicates the food prefer possible, details of genera or species are gi Whenever known. the products, as follows: AC acetylenes, DG diacylglycerols, IA inor acetylenes, DG diacylglycerols, AC the products, as follows: TT tetraterpenes, NC nitrogenated compounds, OC other compounds, PG prostaglandins TS triterpenes and steroids, sesterterpenes, compilation of all available data on presence or absence of MDFs in Chromodorididae see T compilation of all available because of lack of literature data. Column 7: * indicates that only one or tw same genus are described. unpublished data). Column 12: References including previous histological in unpublished data). Column 12: References including previous T Column 1 Higher taxon HETERO- Notes:

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Figure 1 Histological sections of opisthobranch epidermal and subepithelial glands. (A) Marionia blainvillea epidermis. (B) Dendrodoris nigra epidermis; Arrow: single glands with acid mucopolysaccharides, asterisk: homogenously light blue stained glandular cell. (C) Acteon tornatilis spongy glands, note the invagination of the epithelium. (D) Chelidonura ornata, hypobranchial gland (arrow) and spongy tissue (asterisk). (E) Thu- ridilla hopei subepithelial glands with crystalline structures. (F) Chelidonura pallida glandular stripe, note the duct of one of the cells (arrow). (G) Akera soluta glandular stripe, note the small duct (arrow). Scale bars in µm.

In a few species, cells are present which have a large vacuole with homogenously staining light blue contents (Figure 1B, Dendrodoris nigra, asterisk). Spongy glands at mantle rim. (Table 1, Table 2 Column 4) This gland is also called “Mantelrand- drüsen” (Hoffmann 1939), or “glande semi-lunaire” (Pelseneer 1888, 1894). Several members of the Opisthobranchia, belonging to many different groups, show these spongelike vacuolated cells. The cells are very large, with a tiny nucleus. The single large vacuole does not stain (Figure 1C, Acteon tornatilis). The cells are actually epithelial cells but, due to their size, they can come to lie subepthelial in comparison with the other epithelial cells. Due to invagination of the epidermis, the glandular cells lie in saclike depressions. In many species, these glands are located near to the mantle edge and can be clearly identified by their kind of pores, which are formed by the invagi- nation of the epidermis. This glandular epithelium is restricted to the mantle rim in members of

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

the Acteonoidea, Cephalaspidea sensu stricto and Anaspidea. Some dorids, like Trapania and Polycera have an outer epithelium, which seems to be spongy, but the size of the glandular cells is smaller, and the contents are stained lightly bluish. In several opisthobranchs (Chelidonura, Ancula) the notum beneath the epithelium appears spongy due to large cells with a tiny nucleus and a huge nonstaining vacuole (Figure 1D, Chelidonura ornata, asterisk). In these cases, however, no openings through the epidermis could be observed. Therefore, this type of cell is not considered to be homologous with the spongy glandular epithelium shown in Figure 1C. Hypobranchial gland. (Table 1, Table 2 Column 3) This gland consists of elongate epidermal cells which stain light violet to red. They form a compact layer, with tiny supporting cells interspersed (Figure 1D, Chelidonura inornata, arrow). In some cephalaspidean species, this gland is voluminous and secretes copious amounts of mucus (e.g., in Haminoea callidegenita). Sometimes, this glandular layer is reduced to few cells interspersed with ordinary epithelial cells. When the locality and staining properties of these few cells are identical to the typical hypobranchial gland in other opisthobranchs, these glandular cells are considered to be a hypobranchial gland. This gland is mainly found in species which still have a mantle cavity (e.g., many Cephalaspidea). Subepithelial glands (Table 1) Subepithelial single glands producing acid mucopolysaccharides (staining violet to red). (Table 1) The single cells have a drop-like structure with their duct-like part running between the epidermal cells and opening to the outside. The cells stain violet. These glands are widespread in many Opisthobranchia and probably are one of the major glandular structures (Figure 4B, Thecacera pennigera). Some species (e.g. Elysia crispata) are completely covered by this type of gland. In Thuridilla hopei, the contents of the cells resemble small globular crystals (Figure 1E). This is rather unusual and was observed only in this species. Opaline gland (gland of Bohadsch, grape-shaped gland) (Table 1, Table 2 Column 9) The opaline gland lies beneath the ventral floor of the mantle cavity. The cells are considerably larger than the normal subepithelial cells and open to the outside with a small pore each. They also have a large nucleus (Figure 2D arrow, Bursatella leachii). In a few aplysiids only, the single glandular cells open into a common duct, which leads to the outside. The opaline gland is considered to be present only in Anaspidea. Similar glands have been detected in members of the Gymnosomata (Figure 2E arrow, Clione limacina). They are also considered to be opaline glands. Supepithelial single gland cells staining bluish (cellules spéciales, glandular stripe) (Table 1, Table 2 Column 6 as glandular stripe). The contents of these cells stain bluish, the nucleus is of moderate size (Figure 1F, G). Sometimes a duct leading to the outside can be observed (Figure 1F, G arrows). These supepithelial glandular cells are widespread in some taxa (e.g., Anaspidea, Cladobranchia) but are missing in others (e.g., Doridoidea). In gill-bearing opisthobranchs, like cephalaspids and anaspids, the position of the glandular cells is related to the gill. The glands are usually found in the hyponotum, the ventral side of the notum covering and protecting the gill. In gill-less species (mainly the Cladobranchia) the glandular cells are arranged into a longitudinal stripe starting behind the genital papilla on the right side and running to the end of the lateral mantle side. In some species (e.g., Dirona) the glands are also located in a stripe on the left side. In some cerata-bearing animals, the glandular cells can be found at the base of the cerata (Doto, Eubranchus). Blochmann’s glands and ink gland (purple gland) (Table 1, Table 2 Column 5) Blochmann’s gland is a large single glandular cell lying subepithelially and characterised by a big nucleus. The contents hardly stain. The single gland has a duct composed of small cuboidal cells leading to the outside. The glandular cell is surrounded by muscle fibres. This glandular type is only present in some members of the Cephalaspidea (e.g., Figure 2A, Haminoea antillarum, Figure 2B, Bulla vernicosa) and Anaspidea. In Anaspidea this gland is called the ink gland and is composed of many Blochmann’s

228 7044_book.fm Page 229 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Figure 2 Histological sections of opisthobranch subepithelial glands. (A) Haminoea antillarum Blochmann’s gland with duct composed of cuboidal small cells. (B) Bulla vernicosa Blochmann’s gland. (C) Aplysia parvula ink gland (composed of Blochmann’s glands). (D) Bursatella leachii opaline gland (gland of Bohadsch), note the large nucleus (arrow). (E) Clione limacina opaline glands (gland of Bohadsch), note the large nucleus (arrow). (F) Cadlina laevis compound glands lying in notum with outleading duct. (G) Berthellina edwardsii acid glands in notum with opening to the outside. Scale bars in µm.

glands lying close together in the dorsal mantle cavity and opening above the gill (Figure 2C, Aplysia parvula). The ink gland exudes whitish or purple secretions. The ink gland is considered to be only present in Anaspidea, but it is difficult to differentiate between the ink gland in the Anaspidea and the presence of the Blochmann’s glands in several members of the Cephalaspidea. Subepithelial acid glands (Table 1, Table 2 Column 6) Huge subepithelial acid glands are present in some members of the Pleurobranchoidea (Berthellina). These structures can have a diameter of ~500 µm. The glands are composed of very few cells and lead to the outside (Figure 2G). Their contents do not stain, or only small pale patches are present.

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Other subepithelial glands composed of several cells These compound glands have larger vacuoles with granular and bluish stained contents. They have been observed in several species, e.g., Cadlina luteomarginata and C. laevis (Figure 2F). In the latter species, the glands are sunk deeply in the notum, and could also be assigned to the notum glands (see below). Glandular organs lying in the notum (Table 1, Table 2 Column 9) Dorsal mantle gland This gland is present in members of the Tylodinoidea. Although the position is similar in the two investigated species, Tylodina perversa and Umbraculum umbraculum, the morphology and histology are different. In both species, the gland is located in the dorsal notum tissue and it opens to the outside above the mouth area. U. umbraculum (Figure 3A) has a highly branched system of many tubules. Glandular tissue is only present in the finer tubules (Figure 3A, arrows). These connect to bigger tubules, which are surrounded by flat to cuboidal cells with no glandular vacuoles (Figure 3A, asterisks). The whole gland opens above the mouth in the mantle rim via one or two openings. Tylodina perversa (Figure 3B, C) has huge glandular follicles which stain grainy and in a greyish colour (asterisks). They seem to fuse in the anterior part of the mantle rim and form a large reservoir of secretion. Part of the gland has bigger cells with uniform violet contents (arrows). These areas are more confined to the dorsal part of the mantle and form several distinct ducts which open separately to the outside. Interpalleal gland The interpalleal gland in the genus Scaphander is roundish in its general appear- ance (Figure 3D). It is composed of many tiny tubules. These run together into a common duct, which opens in the outer part of the dorsal mantle cavity (Figure 3D and E, arrows). The cells lining the tubules are small, with a large vacuole. Their rather transparent contents stain light bluish. Marginal sacs of Arminidae These glandular and saclike structures are very conspicuous and arranged in the mantle rim of the animals. The glands are large (up to 1 mm), globular and composed of many cells which more or less stretch from the margin to the middle of the globes. The single vacuole contains a homogenously dark violet-stained substance. Nuclei are not visible in mature marginal sacs. The sacs are surrounded by a thin layer of muscular tissue (Figure 4A, Dermato- branchus semistriatus). These glandular structures only occur in members of the Arminidae and their staining properties are listed in Table 4 (see page 245). Agglomeration of glandular cells in ceratal processes or tubercles. Thecacera pennigera (Figure 4B) and Cadlina luteomarginata (Figure 4C) have glandular tissues, which are characterised by nonstaining vacuolated cells. These glands, which can easily be overlooked, are probably not homologous. In Thecacera pennigera the glands are arranged like a flower and were only observed in the ceratal processes next to the gill. In Cadlina luteomarginata the glandular tissue is located in the apical parts of the tubercles. Mantle dermal formations (MDF types) (Table 1, Table 2 Column 7, Table 3 and Table 4) Basically, MDFs are globular structures of usually >300 µm and are composed of many cells, each with a single large vacuole. Very often, especially within the Chromodorididae, these vacuoles do not stain with toluidine blue. The whole organ can be surrounded by a thin or rather thick layer of muscles (Table 3). MDFs are widely distributed in members of the doridoidean family Chromodorididae, but are also observed in members of other opisthobranch taxa (Table 2 Column 7). Whereas some of these taxa have MDFs rather regularly arranged (Chromodorididae, Limacia clavigera, Plako- branchus ocellatus), some seem to have only a few irregularly arranged MDFs (Newnesia antarctica, Elysia ornata, Haminoea orteai). Their appearance can vary to a great extent even within the same genus. At least three different types can be distinguished. Type 1 (Figure 5A, B) is characterised by the presence of a duct which leads to the outside. It is present in Cadlina luteomarginata, which has a specialised duct (Figure 5B) and in Chromodoris

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Figure 3 Histological sections of opisthobranch glands lying in the notum. (A) Umbraculum umbraculum cross section of anterior part of body with dorsal mantle glands. To the left more fine tubules with dark violet staining glandular cells are visible (arrows), whereas to the right, ducts with a wide lumen are more common (asterisks). (B) Tylodina citrina cross section through frontal part with the dorsal mantle separated from the underlaying body wall. Dorsal mantle glands with glandular ducts leading separately to the outside (arrow); greyish part of gland, which is connected to the glandular ducts marked with an asterisk. (C) Detail of Tylodina citrina dorsal mantle glands. Connection between greyish staining part (asterisk) to the violet staining part (arrow). (D) Scaphander lignarius interpalleal gland with main collecting duct, which leads to the outside (arrow) at the ventral part of dorsal notum. (E) Scaphander lignarius detail of interpalleal glands. Arrows indicate small ducts leading into main duct. Scale bars in µm.

tumulifera (Figure 5A), where the MDF is located beneath the epidermis and the vacuoles reach the outside. Type 2 (Figure 5CÐF, Figure 6A) is characterised by a muscular clot which connects the MDF to the outside (see Table 3, e.g., Hypselodoris orsinii, Limacia clavigera). The clot is composed of muscle fibres which are arranged parallel to the epidermis and the MDF (Figure 5C, D, F).

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Figure 4 Histological sections of opisthobranch glands lying in the notum. (A) Dermatobranchus semistriatus marginal sac. Note the orientation of the cell vacuoles to the centre of the globe. (B) Thecacera pennigera glandular agglomerations in ceratal processes next to gills (arrows). At bottom of picture, subepithelial glands staining dark violet visible. (C) Cadlina luteomarginata glandular agglomerations in the apical parts of tubercles. (D) Bathyberthella antarctica acid glands. Note the tubular structure. (E) Plocamopherus ceylonicus acid glands in visceral cavity. Note the tubular structure and similar size as in Bathyberthella antarctica. (F) Plocamopherus ceylonicus acid glands in visceral cavity. Scale bars in µm.

Newnesia antarctica also has MDFs in its mantle, although these are not regularly arranged along a rim, but are rather clumped together. Nevertheless, these MDFs also show a muscular clot, with fibres arranged parallel to the epidermis (Figure 6A). Type 3 (Figure 6G, Figure 7AÐF) seems to be independent of the outer epithelium and most of the MDFs investigated here were of this type. The density of the vacuoles may differ greatly, as does the muscle layer surrounding the MDF in the species investigated. For example, the density

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of vacuoles is very low in Glossodoris atromarginata (Figure 7D) and Plakobranchus ocellatus (Figure 7F) and there is nearly no muscle layer around their MDFs. Between the vacuolated cells, connective tissue is present. In contrast, the vacuoles are packed very densely in Hypselodoris tricolor (Figure 6G) and Risbecia tryoni (Figure 7C) and the muscle layer surrounding the MDF is very thick (40 µm, see Table 3). The MDF of Chromodoris westraliensis (Figure 7A) is peculiar because it does not show a muscular layer but a homogenously stained layer of unknown contents. The MDFs in C. westraliensis were the only ones with a flattened appearance. Vacuolated cells are rather sparse and arranged along the periphery. These cells are connected with the surrounding layer (Figure 7A, asterisk). MDFs in Laila cockerelli (Figure 7B) are rare and located in the cerata- like structures of the notum rim. Only two were recognised in the specimen investigated. The distribution of the MDFs in the organism is also variable between species and the difference in distribution in adult specimens of several species is shown in Figure 8. The main areas covered in most species are the mantle border, or especially near gills and rhinophores. However, Limacia clavigera has MDFs in all processes except those next to the gills. Histochemical analysis showed some differences in the MDFs of five chromodorid species investigated (Table 4). Even applying different staining techniques, the contents of the vacuoles never stained, whereas the surrounding layers of Chromodoris westraliensis, Hypselodoris tricolor and Limacia clavigera stain similarly as connective tissue (green in trichrome after Goldner and blue in trichrome Azan after Heidenhain), but not as muscles (which in both methods stain red). Unfortunately no information is available for the muscular clot. Table 2 contains additional information on the presence of MDFs taken from the literature combined with data obtained by the authors, although information on the size and description of MDFs is lacking for most species. Also, for these species no information on the presence of ducts leading to the outside, or on muscular clots was available and so the presence of these structure is only noted with a +. Similarly, for those species possessing MDFs, data on the presence and thickness of a muscular layer, and the presence or absence of a muscular clot, for example, are lacking (Table 3), because notes on MDFs are frequently not accompanied by any description or morphometrical data. As far as it is known, all the available data on presence/absence or descriptive details of MDFs are included in Table 2 and Table 3. MDF-like structures (Table 1, Table 2, Column 8) (Figure 6B, D, Figure 9AÐF) There are several other glands similar to the MDFs but they differ in the number of cells, size and/or staining properties. The structures observed in Doriopsilla gemela (Figure 6B) are quite similar to true MDFs in having a muscular layer surrounding the vacuole cells but the number of the cells is small, and the contents of the vacuole usually stains bluish or sometimes violet. The homogeneity of the contents also varies. It can be granular or homogenous. The diameters of the structures are ~100 µm and a duct leading to the outside can be observed. Melibe leonina also shows globular structures containing vacuole cells which stain bluish or do not stain at all. These structures lack a muscular layer and a duct leading to the outside (Figure 9D). In addition to these MDF-like structures, Melibe also possesses agglomerations of cells with a large nonstaining vacuole (Figure 6C). The size of these agglomerations comes close to that of real MDFs. The cells are loosely connected by connective tissue in an almost tissue-free notum. This unusual type of gland is listed with the MDF- like structures. Several species show larger globular structures sometimes even surrounded by muscle fibres and therefore resembling MDFs, but their general appearance differs. Plocamopherus ceylonicus even shows two different types, one with a duct leading to the outside and filled with small, rodlike structures (Figure 9A, arrow), and one type without a duct and composed of several globular subunits (Figure 9B). These subunits are composed of vacuoles of different sizes, the smaller ones filled with homogenously dark bluish stained contents, the larger being lighter in colour. These

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Table 3 Details of MDFs, when known, from literature or own studies. See notes on page 240.

Maximum Muscular size Thickness structure (including of muscle connecting MDF MDFs present Type layer), µm layer, µm Opening to epidermis References Sacoglossa Plakobranchus ocellatus 3 500 Absent Absent Absent Present work van Hasselt, 1824 Elysia ornata 2? ?? ? Horgen et al. (Swainson 1840) 2000

Cephalaspidea Newnesia antarctica 2? ? Absent Absent Present work Smith, 1902

Nudibranchia Doridoidea Cadlina laevis 1 450 Absent See figures for Absent Present work (Linnaeus, 1767) possible extrusions Cadlina luarna ?+ ?? ?Valdés & (Marcus & Marcus, 1967) Campillo 2000 Cadlina marginata 1 700 Absent With channel- Absent Present work MacFarland, 1905 like exit (= C. luteomarginata) Cadlinella hirsuta ?+ ?? ? Rudman 1995 Rudman, 1995 Ceratosoma alleni ?+ ?? ? Gosliner 1996 Gosliner, 1996 Ceratosoma gracillimum ?+ ?? ? Gosliner 1996 Ceratosoma ingozi ?+ ?? ? Gosliner 1996 Gosliner, 1996 Ceratosoma tenue ?+ ?? ? Gosliner 1996 Abraham, 1876 Ceratosoma trilobatum ?+ ?? ? Gosliner 1996 (J.E. Gray, 1827) Chromodoris africana ?+ ?? ? Gosliner & Eliot, 1904 Behrens 1998 Chromodoris annae ?+ ?? ? Gosliner & Bergh, 1877 Behrens 1998 Chromodoris britoi 3 360 Absent ? ? Present work, (Ortea & Pérez, 1983) García-Gómez et al. 1991, Avila 1993, Avila & Durfort 1996 Chromodoris buchananae ?+ ?? ? Gosliner & Gosliner & Behrens, 2000 Behrens 2000 Chromodoris elisabethina ?+ ?? ? Gosliner & Bergh, 1877 Behrens 1998 Chromodoris dianae ?+ ?? ? Gosliner & Gosliner & Behrens, 1998 Behrens 1998 Chromodoris goslineri Absent Absent Absent Absent Absent Ortea et al. 1996 Ortea & Valdés, 1996

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Table 3 (continued) Details of MDFs, when known, from literature or own studies

Maximum Muscular size Thickness structure (including of muscle connecting MDF MDFs present Type layer), µm layer, µm Opening to epidermis References Chromodoris hamiltoni ?+ ?? ? Gosliner & Rudman, 1977 Behrens 1998 Chromodoris heatherae ?+ ?? ? Gosliner 1994b Gosliner, 1994 Chromodoris hintuanensis ?+ ?? ? Gosliner & Gosliner & Behrens, 1998 Behrens 1998 Chromodoris joshi ?+ ?? ? Gosliner & Gosliner & Behrens, 1998 Behrens 1998 Chromodoris kitae ?+ ?? ? Gosliner 1994b Gosliner, 1994 Chromodoris krohni 3? ? Absent Absent Present work, (Vérany, 1846) García-Gómez et al. 1991, Avila 1993 Chromodoris lochi ?+ ?? ? Gosliner & Rudman, 1982 Behrens 1998 Chromodoris ?+ ?? ? García-Gómez luteopunctata et al. 1991 (Gantés, 1962) Chromodoris luteorosea 3? ? Absent ? Present work, (Rapp, 1827) García-Gómez et al. 1991, Avila 1993 Chromodoris magnifica ?+ ?? ? Gosliner & (Quoy & Gaimard, 1832) Behrens 1998 Chromodoris ?+ ?? ?Valdés et al. mandapamensis 1999 Valdés, Mollo & Ortea, 1999 Chromodoris michaeli ?+ ?? ? Gosliner & Gosliner & Behrens, 1998 Behrens 1998 Chromodoris naiki Valdés, ?+ ?? ?Valdés et al. Mollo & Ortea, 1999 1999 Chromodoris purpurea 3? Absent Absent ? Present work, (Laurillard, 1831) García-Gómez et al. 1991, Avila 1993 Chromodoris loboi ?+ ?? ? Gosliner & Gosliner & Behrens, 1998 Behrens 1998 Chromodoris strigata ?+ ?? ? Gosliner & Rudman, 1982 Behrens 1998 Chromodoris trimarginata ?+ ?? ?Valdés et al. (Winckworth, 1946) 1999 Chromodoris tumulifera 1 350 Absent Whole Absent Present work Collingwood, 1881 vacuoles (see Figure 5A)

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Table 3 (continued) Details of MDFs, when known, from literature or own studies

Maximum Muscular size Thickness structure (including of muscle connecting MDF MDFs present Type layer), µm layer, µm Opening to epidermis References Chromodoris westraliensis 3 450 Homogeno Absent Absent Present work (O’Donoghue, 1924) us layer (5Ð10) Chromodoris willani ?+ ?? ? Gosliner & Rudman, 1982 Behrens 1998 Doriopsilla gemela 160< 5Opening to Absent Present work Gosliner, Schaefer & exterior Millen, 1999 Durvilledoris albofimbriae ? Single ?? ? Rudman 1995 Rudman, 1995 spheres Glossodoris atromarginata 3 100 Absent Absent Absent Present work (Cuvier, 1804) Glossodoris aureola ? Large & ?? ? Rudman 1995 Rudman, 1995 spherical Glossodoris edmundsi ?+ ?? ? Ortea et al. 1996 Cervera et al. 1989 Glossodoris pallida ?+ ?? ?Avila & Paul (Rüppert & Leuckart, 1997 1828) Glossodoris rufomarginata 3 555 Absent Absent Absent Present work (Bergh, 1890) Gymnodoris aurita ?+ ?? ? Gosliner & (Gould, 1852) Tubes Behrens 1997 network Hypselodoris acriba ?+ ?? ? Ortea et al. 1996 Marcus & Marcus, 1967 Hypselodoris agassizii ?+ ?? ? Gosliner & (Bergh 1894) Johnson 1999 Hypselodoris ?+ ?? ? Gosliner & alboterminata Johnson 1999 Gosliner & Johnson, 1999 Hypselodoris andersoni ?+ ?? ? Gosliner & Bertsch & Gosliner, 1989 Johnson 1999 Hypselodoris babai ?+ ?? ? Gosliner & Gosliner & Behrens, 2000 Behrens 2000 Hypselodoris bayeri ?+ ?? ? Ortea et al. 1996 (Marcus & Marcus, 1967) Hypselodoris benetti ?+ ?? ? Gosliner & (Angas, 1864) Johnson 1999 Hypselodoris bertschi ?+ ?? ? Gosliner & Gosliner & Johnson, 1999 Johnson 1999 Hypselodoris bilineata 1 450 ? ? ? Present work, (Pruvot-Fol, 1953) García-Gómez et al. 1991, Avila 1993 Hypselodoris bollandi ?+ ?? ? Gosliner & Gosliner & Johnson, 1999 Johnson 1999

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Table 3 (continued) Details of MDFs, when known, from literature or own studies

Maximum Muscular size Thickness structure (including of muscle connecting MDF MDFs present Type layer), µm layer, µm Opening to epidermis References Hypselodoris ?+ ?? ? Gosliner & californiensis Johnson 1999 (Bergh, 1879) Hypselodoris cantabrica 3 3600 8 Absent ? Present work, (Bouchet & Ortea, 1980) García-Gómez et al. 1991, Avila 1993, Avila & Durfort 1996 Hypselodoris capensis ?+ ?? ? Gosliner & (Barnard, 1927) Johnson 1999 Hypselodoris carnea ?+ ?? ? Gosliner & (Bergh, 1889) Johnson 1999 Hypselodoris ciminoi Absent Absent Absent Absent Absent Ortea et al. 1996 Ortea & Valdes, 1996 Hypselodoris dollfusi ?+ ?? ? Gosliner & (Pruvot-Fol, 1933) Behrens 2000 Hypselodoris emma ?+ ?? ? Gosliner & Rudman, 1977 Johnson 1999 Hypselodoris espinosai ?+ ?? ? Ortea et al. 1996 Ortea & Valdés, 1996 Hypselodoris festiva ?+ ?? ? Gosliner & (Adams, 1861) Johnson 1999 Hypselodoris ?+ ?? ? Rudman 1995 flavomarginata Rudman, 1995 Hypselodoris fontandraui Absent Absent Absent Absent Absent Present work, (Pruvot-Fol, 1951) Avila 1993 Hypselodoris fucata ?+ ?? ? Gosliner & Gosliner & Johnson, 1999 Johnson 1999 Hypselodoris gasconi ?+ ?? ?Avila 1993 (as Ortea, 1996 Hypselodoris sp.) Hypselodoris ghiselini ?+ ?? ? Gosliner & Bertsch, 1978 Johnson 1999 Hypselodoris gofasi Absent Absent Absent Absent Absent Ortea et al. 1996 Ortea & Valdés, 1996 Hypselodoris iacula ?+ ?? ? Gosliner & Gosliner & Johnson, 1999 Johnson 1999 Hypselodoris infucata ?+ ?? ? Gosliner & (Rüppert & Leuckart, Johnson 1999 1828) Hypselodoris insulana ?+ ?? ? Gosliner & Gosliner & Johnson, 1999 Johnson 1999 Hypselodoris kaname ?+ ?? ? Gosliner & Baba, 1994 Johnson 1999

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Table 3 (continued) Details of MDFs, when known, from literature or own studies

Maximum Muscular size Thickness structure (including of muscle connecting MDF MDFs present Type layer), µm layer, µm Opening to epidermis References Hypselodoris kanga ?+ ?? ? Gosliner & Rudman, 1977 Johnson 1999 Hypselodoris koumacensis ?+ ?? ? Rudman 1995 Rudman, 1995 Hypselodoris krakatoa ?+ ?? ? Gosliner & Gosliner & Johnson, 1999 Johnson 1999 Hypselodoris lapislazuli ?+ ?? ? Gosliner & (Bertsch & Ferreira, Johnson 1999 1974) Hypselodoris maculosa ?+ ?? ? Gosliner & (Pease, 1871) Johnson 1999 Hypselodoris malacitana ?+ ?? ? Ortea et al.1996 Luque, 1986 Hypselodoris marci ?+ ?? ? Ortea et al., Marcus, 1970 1996 Hypselodoris maridadilus ?+ ?? ? Gosliner & Rudman, 1977 Johnson 1999 Hypselodoris maritima ?+ ?? ? Gosliner & (Baba, 1949) Johnson 1999 Hypselodoris midatlantica ?+ ?? ? Gosliner & Gosliner, 1990 Johnson 1999 Hypselodoris muniani ?+ ?? ? Ortea et al. 1996 Ortea & Valdés, 1996 Hypselodoris nigrolineata ?+ ?? ? Gosliner & (Eliot, 1904) Johnson 1999 Hypselodoris orsinii 2 650 3 Absent Present Present work, (Vérany, 1846) García-Gómez et al. 1991, Avila 1993, Avila & Durfort 1996 Hypselodoris paulinae ?+ ?? ? Gosliner & Gosliner & Johnson, 1999 Johnson 1999 Hypselodoris picta 3 3000 ? ? ? Present work, (Schultz, 1836) García-Gómez et al. 1991, Avila 1993, Avila & Durfort 1996 Hypselodoris pinna ?+ ?? ? Ortea et al. 1996 Ortea, 1988 Hypselodoris punicea Absent Absent Absent Absent Absent Rudman 1995 Rudman, 1995 Hypselodoris ?+ ?? ? Gosliner & purpureomaculosa Johnson 1999 Hamatani, 1995

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Table 3 (continued) Details of MDFs, when known, from literature or own studies

Maximum Muscular size Thickness structure (including of muscle connecting MDF MDFs present Type layer), µm layer, µm Opening to epidermis References Hypselodoris regina ?+ ?? ? Gosliner & Marcus & Marcus, 1970 Johnson 1999 Hypselodoris reidi ?+ ?? ? Gosliner & Gosliner & Johnson, 1999 Johnson 1999 Hypselodoris rudmani ?+ ?? ? Gosliner & Gosliner & Johnson, 1999 Very large Johnson 1999 Hypselodoris ruthae ?+ ?? ? Ortea et al. Marcus & Hughes, 1974 1996, Gosliner & Johnson 1999 Hypselodoris sagamiensis Absent Absent Absent Absent Absent Gosliner & (Baba, 1949) Johnson 1999 Hypselodoris ?+ ?? ? Gosliner & shimodaensis Johnson 1999 Baba, 1994 Hypselodoris tricolor 3 750 3 Absent Absent Present work, (Cantraine, 1835) García-Gómez et al. 1991, Avila 1993 Hypselodoris villafranca 280~ 5Absent Present Present work (Risso, 1818) 3 mm Hypselodoris villafranca 294~ 5Absent Absent* Present work (Risso, 1818) 3.5 mm Hypselodoris villafranca 2 115 5 Absent Absent* Present work (Risso, 1818) 4 mm Hypselodoris villafranca 2 165 8 Absent Absent* Present work (Risso, 1818) 6 mm Hypselodoris villafranca 2 700 13 Absent Present Present work, (Risso, 1818) adult García-Gómez et al. 1991, Avila 1993, Avila & Durfort 1996, Gosliner & Johnson 1999 Hypselodoris ?+ ?? ? Gosliner & violabranchia Johnson 1999 Gosliner & Johnson, 1999 Hypselodoris xicoi ?+ ?? ? Ortea et al. 1996 Ortea & Valdés, 1996 Hypselodoris whitei ?+ ?? ? Gosliner & (Adams & Reeve, 1850) Johnson 1999 Hypselodoris zebra ?+ ?? ? Gosliner & (Heilprin, 1888) Johnson 1999 Hypselodoris zephyra ?+ ?? ? Gosliner & Gosliner & Johnson, 1999 Johnson 1999

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Table 3 (continued) Details of MDFs, when known, from literature or own studies

Maximum Muscular size Thickness structure (including of muscle connecting MDF MDFs present Type layer), µm layer, µm Opening to epidermis References Laila cockerelli 3 140 Absent Absent Absent Present work (MacFarland, 1905) Limacia clavigera 2 400 13 Absent Present Present work, (Müller, 1776) Wägele 1997 Mexichromis francoisae ?+ ?? ? Ortea et al. 1996 (Bouchet in Bouchet & Ortea, 1980) Mexichromis molloi ?+ ?? ? Ortea et al. 1996 Ortea & Valdés, 1996 Noumea verconiforma ?+ ?? ? Rudman 1995 Rudman, 1995 Large opaque spheres Pectenodoris aurora ?+ ?? ? Johnson & Johnson & Gosliner, 1998 Gosliner 1998 Pectenodoris trilineata ?+ ?? ? Johnson & (Adams & Peeve, 1850) Gosliner 1998 Risbecia nyalya ?+ ?? ? Ortea et al. 1996 (Marcus & Marcus, 1967) Risbecia tryoni 3 650 40 Absent Absent Present work (Garrett, 1873) Thorunna kahuna ?+ ?? ? Johnson & Johnson & Gosliner, 2001 Gosliner 2001 Thorunna montroucieri ?+?? ?? Rudman 1995 Rudman, 1995 Thorunna punicea Absent Absent Absent Absent Absent Gosliner & (Rudman, 1995) Johnson 1999 Tyrinna nobilis 3 2000 Very thin Absent Absent Muniaín et al. Bergh, 1898 Spherical 1996, Schrödl & Millen 2001 Tyrinna evelinae 3 700 Very thin Absent Absent Muniaín et al. Marcus, 1958 1996 (and references therein, some as Cadlina)

Notes: ? = unknown; + = present but size not known; * juvenile Hypselodoris villafranca are assumed to develop muscular clots during ontogeny, because this clot was already present in one 3 mm specimen, as well as in all MDFs of the adult.

glandular balls lie in the dorsal appendages of the mantle rim. Elysia ornata (Figure 9C) has very few MDF-like structures (two to three) lying in the parapodia. They are not surrounded by muscle tissue. The dense core of the MDFs (Figure 9C, arrow), which could not be identified, is peculiar. It stains bluish and, at least on the periphery, small nuclei can be observed. Haminoea orteai (Figure 9D) has an MDF with a more typical appearance, but the glandular cells stain with a tinge to violet. MDF-like structures are also very rare in this species. Siphonaria javanica (Pulmonata)

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Figure 5 Histological sections of opisthobranch glands: MDFs of type 1 and type 2. (A) Chromodoris tumulifera. Note the opening to the outside. (B) Cadlina luteomarginata MFDs with outleading ducts. (C) Hypselodoris villafranca. Only a small section of the whole MDF is visible with the muscular clot. (D) Hypselodoris orsinii. Part of the MDF visible with muscular clot. Note the outer epithelium invaginating in the area of the muscle clot. (E) Hypselodoris orsinii with two MDFs, one showing a muscular clot. (F) Limacia clavigera. MDF in one of the dorsal processes. Note the muscular clot. Scale bars in µm.

has large glands with a duct leading to the outside and a muscle layer surrounding the gland. The contents of the vacuoles stain violet, but many cells seemed to have exuded their vacuoles’ contents (Figure 9E). To a certain extent, the gland resembles the subepithelial glands mentioned above, but their size is much bigger. The same applies to the glandular structures observed in Onchidella species (Figure 9F, Onchidella borealis). The gland is composed of large cells with a staining vacuole. There is a long and narrow duct that connects this gland with the exterior.

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Figure 6 Histological sections of opisthobranch glands: MDFs and MFD-like structures: (A) Newnesia antarctica. The MDF does not show the distinct habitus of chromodorid MDFs. Nevertheless, a muscular clot is present (arrow). (B) Doriopsilla gemela with two MDF-like structures. Note the duct leading outwards and the muscular layer around the structure, which is considerably smaller than the MDFs shown in Figure 5. Asterisks denote spicules. (C) Melibe leonina. Agglomeration of glandular cells. (D) Melibe leonina MDF- like structure. (E) Hypselodoris villafranca. MDFs of type 3 (without muscular clot) in an early ontogenetic state. Size of animal: 3 mm, one of the smallest MDFs observed (about 40 µm). (F) H. villafranca. Size of animal: 3 mm, one of the largest MDFs observed (about 200 µm). (G) H. tricolor with MDF of type 3. Scale bars in µm.

Glands in the visceral cavity (Table 1, Table 2 Column 9)

Median buccal gland This gland is present in members of the Pleurobranchoidea (Figure 4D, Bathyberthella antarctica) and in one doridoidean species: Plocamopherus ceylonicus (Figure 4E, F). The gland is tubular in structure (e.g., Bathyberthella antarctica and Plocamopherus) or may ramify greatly (in many other Pleurobranchoidea). It opens into the oral tube. The gland can fill most of the lumen of the visceral cavity. The glandular cells are very large and surround the central lumen of the glandular tube in one layer. Each cell contains a huge vacuole with nonstaining contents.

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Figure 7 Histological sections of opisthobranch glands: MDFs Type 3. (A) Chromodoris westraliensis. Note the homogenously stained surrounding area of the MDF, as well as the connection to the vacuolated cells (next to the asterisk). (B) Laila cockerelli. One of the very few MDFs detected in this species. (C) Risbecia tryoni. (D) Glossodoris atromaculata. Note the loosely distributed vacuolated cells with connective tissue in between. (E) Hypselodoris orsinii MDFs sectioned in different areas. (F) Plakobranchus ocellatus. Note the loosely distributed vacuolated cells. Scale bars in µm.

Ontogenetic studies of MDFs in Hypselodoris villafranca Juvenile specimens of Hypselodoris villafranca were studied to gain a better understanding of the formation of MDFs. Serial sections of juvenile animals of a size between 3 and 6 mm, as well as an adult specimen of 15 mm length were analysed and MDF sizes recorded. Figure 10 gives an indication where MDFs were found in the different sized animals from 3 to 6 mm. There seems to be no direct relation between the number and size of MDFs in these juveniles. The minimum number of MDFs (4) was counted in one 6 mm animal, the highest number (8) in an animal of 4 mm length. Out of the six MDFs noted in one of the smallest animals (3 mm), the smallest MDF measured ~55 µm (Figure 6E), the largest 200 µm (Figure 6F). In the largest juvenile (6 mm), out of the seven MDFs, the smallest measured 35 µm, and the largest 150 µm. The only difference between the 3 mm animals and the 6 mm animals is the presence of a muscular clot in one of the MDFs in the largest juvenile. Adult H. villafranca of 15 mm length have ~14 MDFs with a maximum

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(A) (B) (C) (D)

(E) (F) (G) (H)

(I) (J) (K)

Figure 8 Distribution of MDFs in various members of opisthobranchs. Doridoidea A-J, Sacoglossa K. (A) Cadlina laevis. (B) Cadlina luteomarginata. (C) Hypselodoris tricolor. (D) Hypselodoris villafranca. (H. orsinii has the same distribution as the other Hypselodoris species). (E) Glossodoris atromarginata. (F) Glossodoris rufomarginata. (G) Chromodoris tumulifera. (H) Chromodoris westraliensis. (I) Risbecia tryoni. (J) Limacia clavigera. (K) Plakobranchus ocellatus.

size of 700 µm (Table 3, Figure 8). The muscle layer increased in thickness from ~5 µm in the 3 mm specimens and 8 µm in the 6 mm specimen to 13 µm in the adult (Table 3).

Discussion Gastropods are known for their ‘slimy’ habits, and therefore the presence in this taxon of glandular cells with a high diversity in shape is to be expected, although they have been only poorly described (see authors listed in Table 2 Column 12). The glandular cells have very different tasks. Glands in

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Table 4 Histochemical studies of MDFs in selected species. Staining methods and names (Goldner, Azan, Pasini) are given according to Böck (1989).

Capsule of MDF Contents of vacuoles Species Goldner Azan Pasini Goldner Azan Pasini Chromodoris westraliensis Green Blue Blue 0 0 0 Glossodoris atromarginata 000000 Hypselodoris tricolor Green Blue Blue 0 0 0 Cadlina laevis 000000 Limacia clavigera Green Blue Blue 0 0 0 Dermatobranchus semistriatus 000Red Red Red to violet

Note: Connective tissues stain green in Goldner, blue in Azan and Pasini, whereas muscles stain red in all three methods.

the foot are mainly involved in gliding over the ground or in adherence to substrata. These glands are not considered further here. Glands on the surface (single epidermal or subepidermal glands) are involved in cleaning the epidermis from micro-organisms by producing a slime cover, which has to be renewed occasionally. They probably also repel parasites, but this function has never been investigated. Infection by certain parasites especially of the copepod family Splanchnotrophidae seems to be very species-specific in parasites as well as hosts (Haumayr & Schrödl 2003). Glands within the mantle cavity of pulmonates and basal opisthobranchs (e.g., hypobranchial gland) also have cleaning tasks and transport debris, and probably microorganisms, which are inhaled with the respiration stream, from the cavity. This function has been demonstrated for the hypobranchial gland in prosobranchs (Voltzow 1994). Whether the substances exuded from the glands have antibiotic functions has never been tested, although it is likely. This comparative study of the many glands throughout the Opisthobranchia has shown not only the high diversity of glandular structures, but also the occurrence of some definable types. However, glands were also found that are difficult to assign to known structures. Because only one or two specimens of the same species were studied, hardly anything is known about the intraspecific variability of all these glandular structures. This lack of knowledge renders it impossible to homologise the glands described in this study.

Glandular structures confined to the epidermis Single glandular cells

Epithelial and single subepithelial glands staining violet and indicating acid mucopolysaccharides are widely spread in Opisthobranchia and also marine Pulmonata. These glands may have the function of cleaning the outer surface of the animals from bacteria and other small organisms. The quantity of glands present may be related to special circumstances in the respective habitats, but the relationship is difficult to understand at the moment due to lack of biological information. It is not clear why, for example, Elysia crispata from the upper sublittoral in the Caribbean is characterised by a huge amount of subepithelial glands (see figure in Wägele & Klussmann-Kolb 2005), whereas E. viridis from same depths in the Mediterranean Sea has many fewer glands. On the other hand, the presence of a large quantity of homogeneously staining violet glands in nearly all members of the Dendronotoidea may be a characteristic feature of the whole taxon, irrespective of their habitat. The glands are only missing in the pelagic members, which could be an adaptation to this special environment. Thompson (1960) referred to this gland as type 2.

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Figure 9 Histological sections of opisthobranch glands: MDF-like structures. (A) Plocamopherus ceylonicus. MDF-like structure located at the base of ceratal processes. (Arrow indicates duct leading to the outside). (B) Plocamopherus ceylonicus. MDF-like structures located at the tip of ceratal processes next to the gills. Several globular structures can be distinguished. (C) Elysia ornata. One of the very few MDF-like glands found in the parapodia of this species. Note the dense core (arrow). (D) Haminoea orteai. One of the rare MDF-like structures found in this species. (E) Siphonaria javanica. Several cells with violet staining contents are present. Note the duct leading to the outside. (F) Onchidella borealis showing similar cells to Siphonaria javanica. Scale bars in µm.

The epidermis of Dendrodoris nigra is characterised by large vacuolised cells. Avila & Durfort (1996) described macrovacuolated cells especially in the mantle border and the gills of D. limbata. According to the authors’ results presented here, in D. nigra large vacuole cells are distributed all over the mantle. Whether they contain natural products has yet to be investigated.

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3 mm

4 mm

6 mm

Figure 10 Distribution of MDFs in ontogenetically different stages of Hypselodoris villafranca. Two animals investigated per size and indicated in the figure. Note the different numbers of MDFs even in same-sized animals.

Spongy glands at mantle rim (see Table 2 Column 4)

The cells of the ‘spongy’ glands in the notum present in the Acteonoidea and several Cephalaspidea are similar in their appearance to those found in the median buccal gland of Pleurobranchoidea and, to a certain extent, to the subepithelial acid glands (see below). They are rather large and do not stain, therefore the production of acids by these glands seems very likely, although this remains to be tested. Hoffmann (1939) described and illustrated this type as ‘Mantelranddrüsen’. The presence of these epithelial glands is confined to members of the Opisthobranchia which still have a mantle cavity (Acteonoidea, many Cephalaspidea and Anaspidea). These glands are usually situated at the entrance of the mantle cavity in the dorsal area and perhaps an acid secretion would deter small invertebrates from entering the cavity. Although the epithelial glands in Dendrodoris appear similar to the spongy glands (Brodie 2005), they clearly differ by staining bluish, and by not secreting acids (see Avila & Durfort 1996).

Hypobranchial gland (see Table 2 Column 3)

According to the results presented in Table 2, the presence of a hypobranchial gland is confined to species which still have a mantle cavity. Therefore, many species which have a spongy gland also have a hypobranchial gland. Only some members of the Anaspidea still having a mantle cavity lack the the hypobranchial gland, although the spongy gland is present. A hypobranchial gland is also present in Prosobranchia (e.g., Fretter & Graham 1962, Voltzow 1994). The Prosobranchia have a shell and are well protected by it. Therefore, it may be assumed that the hypobranchial

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gland does not have a defensive task against predators, but is involved in cleaning the mantle cavity (see Voltzow 1994), including preventing the intrusion of parasites.

Subepithelial glands, lying in the notum tissue Subepithelial single glands producing acid mucopolysaccharides (staining violet to red)

These glands are widespread in Opisthobranchia (e.g., Hoffmann 1939, Edmunds 1966a). They are probably one of the major glandular structures but their role in defence is not clear. Even after analysing nearly 200 species of opisthobranchs, bacteria, protists or other organisms (excluding parasitic copepods) were never found on the surface of these animals. Therefore, some kind of antifouling function of these glands can be assumed. The density and size of the glands may be related to ecological conditions; a relationship which as yet we do not understand. It is of interest, however, that, in contrast to whole animals, opisthobranch egg clutches are very often contaminated with bacteria, algae or nematodes (Wägele 1989b, author’s unpublished data).

Supepithelial single gland cells staining bluish (cellules spéciales, glandular stripe) (see Column 6 in Table 2: glandular stripe)

These single glands have been described in the past under different names. Edmunds (1966a) described these cells for several members of the Aeolidoidea in detail as “cellules spéciales” and showed that their size differs intraspecifically. He suggested that the cells store substances which are exuded only occasionally, because the presence of ducts was not observed in all specimens investigated. He thought that the function of the glandular cells was not related to protection. According to his results, these cells synthesise proteins or have a function in metabolism. Wägele (1997) described these cells for many Cladobranchia in the ‘glandular stripe’. She suspected that these glands were homologous with similar glands described in Anaspidea where the cells have been found in the mantle roof mainly above the gill. They are widespread amongst the Cephalaspidea and Anaspidea (see Table 2 Column 6), usually assigned to the right side, even if the mantle cavity is reduced. In Cladobranchia, they also lie mainly on the right side. If they function as defensive glands, a regular distribution all over the body would be expected, at least in shell-less opistho- branchs. This is not the case in Cladobranchia. Wägele (1997) assumed they have a function in reproductive behaviour, because the glands were only present in the adults of species of Notaeolidia and absent in the juveniles (Wägele 1990, 1997). She assumed that they may produce pheromones for mate attraction and mating.

Blochmann’s glands and ink gland (purple gland) (see Table 2 Column 5)

Blochmann’s glands generally do not stain with toluidine-blue, although in some anaspideans they show a tinge to blue. Their morphology and ontogeny have already been described in detail by Blochmann (1883, after Hoffmann 1939) and Perrier & Fischer (1911). According to these authors, the Blochmann gland starts as a single cell, which may even lie in the epidermis. Later, this cell and its nucleus grow and then the duct is formed by several small cells. According to Hoffmann (1939), the single glands above the gills in Anaspidea (described in this study under single sub- epithelial glands, ‘cellules spéciales’ or ‘glandular stripe’ — see also Wägele 1997) are immature Blochmann’s glands. It was not possible to verify these assumptions and therefore it is not consid- ered that these glands are Blochmann’s glands. They represent an additional type of gland at the same position above the gills. The function of the Blochmann’s glands is unknown. These glands can be scarce and not related to the mantle cavity in some cephalaspideans, e.g., in Scaphander lignarius, but are somewhat

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concentrated in the mantle fold above the gill in other Cephalaspidea (e.g., Bulla vernicosa) and in Anaspidea. In the latter taxon, the agglomeration is then called an ‘ink gland’ (see below). The glands described here for B. vernicosa are probably those mentioned by Marín et al. (1999) in B. striata and B. gouldiana, although they did not describe the morphology of the glands. These authors only mentioned the presence of ‘defensive glands’ — white spots in a white gland along the mantle margin. Johnson & Willows (1999) summarised the different roles described for the ink gland in anaspideans, which is considered to be homologous with Blochmann’s glands (see Hoffmann 1939). Although their morphological appearance is similar to the Blochmann’s glands in Cephalaspidea, the contents stain in all members of Anaspidea investigated here. A change in function can therefore be assumed. Nearly every role has been considered for these glands including camouflage, pheromone production and protection against predators (see Johnson & Willows 1999). These authors also included the hypothesis of bile excretion, because this would explain the evolutionary trait from an excretory organ to a defensive one. The chemistry of the gland has been examined by several workers (see summary in Johnson & Willows 1999). The secretion is formed by two different substances; a red algal-derived pigment (mainly phycoerythrin) and proteins.

Opaline gland (gland of Bohadsch, grape-shaped gland)

Until now, this gland has only been described from members of the Aplysiidae. Hoffmann (1939) reviewed the work of Blochmann (1883) and Perrier & Fischer (1911) and he affirmed their conclusion that the opaline gland of the Anaspidea is also homologous with Blochmann’s glands. Klussmann-Kolb (2004) followed their assumptions. According to the present authors’ results, the opaline gland in the investigated aplysiids differs considerably from the Blochmann’s glands, not only in shape but also in staining properties. The opaline gland always stained violet, whereas Blochmann’s glands stain only light bluish, or were transparent. Furthermore, no duct composed of cells and connected to a single glandular cell could be found in the opaline gland. A thorough reinvestigation based on ultrastructure is needed. Glands similar to the opaline gland in anaspideans have been found in members of a planktonic group (the Gymnosomata) but here, the glands can be found beneath the exterior notum. The relationship of this group within the Opisthobranchia is still unknown.

Subepithelial acid glands

Glandular cells containing acids usually do not stain. Thompson & Slinn (1959) investigated the secretion of acid in Pleurobranchus membranaceus and demonstrated that the exudate contains choride and sulphate ions, but not nitrite, nitrate, oxalate, tartrate and citrate, or any proteins. The lack of any proteins explains the nonstaining properties of most of the cells. In a few cases, however, a light bluish-stained fluid was observed, indicating further (probably protein) ingredients. The pH value measured by Thompson & Slinn (1959) was in the region of 1, and the acid is stored in the cells (Thompson, 1969, 1983, 1986). Sulphuric acid secretions from subepthelial glands lying in the notum are known from several different and unrelated opisthobranchs (Pleurobranchoidea, Philine, Discodoris, Onchidoris, Anisodoris and others) (Edmunds 1968; Thompson 1960; 1983, 1986, 1988; Gillete et al. 1991), as well as from prosobranchs (e.g., Thompson 1983). The inves- tigation of the epidermis and notum of Onchidoris bilamellata and Peltodoris atromaculata did not reveal large cells with a nonstaining vacuole, although Thompson (1988) demonstrated the presence of sulphate ions in Onchidoris and Discodoris. In some members of the Opisthobranchia, however, large cells with a nonstaining vacuole were observed beneath the epidermis (e.g., Cheli- donura inornata, Figure 1D, asterisk). Further analysis of acid secretion in these opisthobranchs is needed. Philine alata has subepithelial cells similar to those of P. aperta where acidic secretions

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were demonstrated by Thompson (1986). It seemed likely that they also produce sulphuric acid, but this has been denied by preliminary and unpublished studies of one of the authors (CA). The presence of acid glands in the notum cannot be generalised for whole groups. For example, large acid glands were present in Berthellina edwardsii, but were missing in Berthella stellata. Further studies are needed to ascertain whether the gland is present in some genera and missing in others, or whether it is species-specific. It cannot be excluded that the subepithelial acid glands are homologous with the spongy glands in the epithelium. An invagination of formerly epithelial glands, as discussed above, seems probable. Pleurobranchoidea and also the dorid Plocamopherus ceyloni- cus have evolved internal tubular acid glands opening into the oral tube (see below). In 1976, Thompson described the dislike of fish for acid compounds. Therefore, a defensive function is certain.

Subepithelial glands composed of several cells

These glands, composed of several cells, have large vacuoles with staining contents. Here they are described for Cadlina luteomarginata and C. laevis. In the latter species, the glands are sunk deeply in the notum and could be assigned to the notum glands (see below). This gland type shows the particular problems encountered in defining types because these composite glands are similar to MDF-like structures as described in Siphonaria and Doriopsilla, for example. The main difference is the presence of a muscle-like tissue around the structures in Siphonaria and Doriopsilla, which is missing in the Cadlina species.

Glandular organs lying in the notum Dorsal mantle gland

This gland, which is unique to the Tylodinoidea, was described by Moquin-Tandon (1870) and Vayssière (1885) for the genus Umbraculum, although they misinterpreted the kidney as part of this gland (Wägele & Klussmann-Kolb 2005, Wägele et al. 2006). Morphology and staining prop- erties of the dorsal mantle gland differs considerably in the two genera. Nevertheless, Wägele et al. (2006) assume a homology due to the same position in the body. Nothing is known about the function of these glands. Investigation of chemical products in Tylodina perversa (Ebel et al. 1999, Thoms et al. 2003) revealed the presence of brominated alkaloids, which are sequestered while feeding on the sponge Aplysina aerophoba, in the mantle tissue, mucus and eggs. Becerro et al. (2003) were able to show that Tylodina perversa prefers sponges with a high content of cyanobacteria, although these do not seem to be responsible for the high content of natural products in Aplysina aerophoba (Turón et al., 2000). It is not possible to ascertain any relationship between the mantle gland and the presence of these chemicals at present.

Interpalleal gland

This gland was described for the first time by Perrier & Fischer (1911) and is only known from the genus Scaphander. The gland lies in the dorsal mantle rim, in the middle of the entrance into the mantle cavity. The drawings of this gland in Perrier & Fischer (1911) give the impression that it is very similar to the dorsal mantle gland in Umbraculum, but histology (morphology and staining properties of cells) and the position of the gland differ considerably and homology is therefore very unlikely. Marín et al. (1999) mentioned that the alarm pheromones lignarenone-A and lignarenone-B were located in the interpalleal gland of Scaphander lignarius. This has been proven to be erroneous since the lignarenones are secreted by the glands situated along the mantle border (unpublished results of A. Domènech; Fontana et al. 2004).

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Marginal sacs of Arminidae

This glandular structure is unique within the Opisthobranchia and an autapomorphy of the Armin- idae (Kolb & Wägele 1998). Its defensive role is not known, although suspected by several authors (Hoffmann 1939, Thompson & Brown 1984). Histochemical investigation (see Table 4) has shown that the consistency of these glandular structures is completely different to the MDFs described below (see Böck 1989). At the moment, it can only be assumed that they have a defensive role. Arminidae feed on octocorals but because the distribution of their chemical compounds has hardly been studied, it is not known whether the marginal sacs contain the defensive metabolites or not.

Glands in ceratal processes or tubercles

These different glandular structures described here for certain species (e.g., Plocamopherus cey- lonicus, Thecacera pennigera) have to be considered as a starting point for extensive further research. The structures are new to science and special investigations on natural products of these species have yet to be performed.

Mantle dermal formations (MDFs) (see Table 1ÐTable 4)

The best-known defensive glands are the mantle dermal formations (MDFs) of Chromodorididae (García-Gómez et al. 1990, 1991, Gosliner 1994a, Avila 1995, Avila & Paul 1997, Wägele 1997, Mollo et al. 2005, and others). Avila & Paul (1997) convincingly showed that individuals of Glossodoris pallida were much more attractive to fishes when the mantle margin with the MDFs was removed. Rudman (1984), Gosliner (1994a) and Gosliner & Johnson (1994) considered the presence of MDFs as a synapomorphy uniting the family Chromodorididae. Wägele (1997) figured an MDF in Limacia clavigera, with very similar structural details to the MDFs of Hypselodoris villafranca, including a muscular clot. In Limacia clavigera, these MDFs are present in all dorsal processes, except of those next to the gills. Most recently, Wägele (2004) described and figured MDFs of the sacoglossan Plakobranchus ocellatus. These findings are confirmed here. The occur- rence of other MDFs or MDF-like structures in completely unrelated opisthobranchs, which has never been reported before (Newnesia antarctica, Haminoea orteai, Elysia ornata, Plocamopherus ceylonicus), indicate that there seem to be constraints in the structure for storing secondary metab- olites. There are always tiny differences between the kinds of MDFs so that creating a terminology for these different structures is not sensible. The mechanism for exudation of the vacuoles’ contents is not yet clear. The presence of a muscular clot in a few species with MDFs is noteworthy. These species (Newnesia antarctica, Limacia clavigera, Hypselodoris villafranca and H. orsinii) are not closely related (see Wägele & Klussmann-Kolb 2005). Little is known about the kind of secondary metabolites stored in some of these species. H. villafranca and H. orsinii are known to store sesquiterpenes (e.g., Avila 1993, 1995) and Limacia clavigera possesses nitrogenated compounds (Graziani & Andersen 1998). Chemicals similar in size and type to those in Hypselodoris mentioned here are also known from many other chromodorids, and also from opisthobranchs without any MDFs (e.g., Haminoea cymbalum, Aplysia parvula; see Avila 1995). When a muscular clot is present, it is always composed of muscle fibres running parallel to the epidermis and the outer layer of the MDF. Its function is not yet understood. In the authors’opinion, a contraction of the fibres would not actually push out the whole MDF, as might be expected. It seems more likely that a contraction disrupts the vacuoles and enables the exudation of their contents. The results on the staining properties of the ‘muscular layer’ around the MDFs are peculiar because, according to the results presented in Table 4, the fibres consist of connective tissue and not real muscle cells. These findings should be investigated again on a broader base, especially because many staining techniques are based on vertebrate rather

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than invertebrate cells (see Böck 1989). In the present study, it was recognised, that several typical muscles in the foot, for example, did not stain apropriate to their function. Therefore the term ‘muscular layer’ is still used here for delineating the capsule around the MDF. The term ‘MDF-like’ is used for another round structure, which is smaller but nevertheless shows the huge vacuoles characteristic of the MDFs described above. Additionally, these structures are surrounded by muscle fibres. These MDF-like structures are present in completely different taxa. Doriopsilla is a doridoidean sponge eater, whereas Melibe feeds on crustaceans, larvae and other small invertebrates, and Crosslandia feeds on Hydrozoa. Thompson & Crampton (1984) and Marín et al. (1991) described the histology of the cerata of Tethys fimbria, a close relative of Melibe. Only Thompson & Crampton (1984: 119) mentioned “conspicuous subepidermal defensive glands” of multicellular character with a strong muscle coat. These glands are distributed all over the cerata and the buccal hood. The authors have also found these glands along the mantle of the body. The two different MDF-like structures in the doridoidean Plocamopherus ceylonicus are also peculiar. One type lies in the notum, under the epidermis, with an opening to the outside, similar to the structures described for Cadlina species although the contents look like bacteria. The other MDF-like structures fill the dorsal appendages and are composed of subunits, which partly stain bluish, the bigger vacuoles only showing bluish patches. Probably the smaller, staining parts represent ‘immature’ cell vacuoles. Plocamopherus is described as possessing organs of lumines- cence located in the lateral processes next to the gills (Okada & Baba 1938, Rudman 1984, Rudman & Darvell 1990, Rudman 2000b). Okada & Baba (1938) investigated the luminous organs in P. tilesii by histological means. In this species, the subunits are more separate and do not form a typical MDF-like structure although the histological properties are quite similar. A second type of MDF as is observed in P. ceylonicus has not been fully described. Further research is also needed on these structures.

Glands in the visceral cavity Median buccal gland

The first description of this gland was given by Schulz (1905). Thompson & Slinn (1959) analysed the secretion of the buccal gland in Pleurobranchus membranaceus, which is sulphuric acid, similar to the subepithelial glands described above. Thompson (1976) mentioned that Pleurobranchoidea can expel a larger dose of sulphuric acid from this gland through the mouth when the animal is threatened. The morphology of the gland coincides with that of the subepithelial acid glands described above. Whether this gland also has a task while feeding is not known. The authors have been able to show that another species not belonging to the Pleurobranchoidea, namely Plocamopherus ceylonicus (Nudibranchia, Doridoidea), also has a buccal gland which very likely produces acid. This species feeds on bryozoans, a prey which is not known within the diet of the Pleurobranchoidea.

Ontogenetic studies of MDFs in Hypselodoris villafranca This review contains the first report of the number and size of MDFs for several ontogenetic stages of a member of the Chromodorididae. In general, the size of the MDFs is smaller than in the adults, and the number may be lower in smaller specimens but there is a certain range of numbers and MDF sizes even within same-sized animals. It is evident from the authors’ studies that these defensive devices are developed very early in the ontogeny of this species. Because the small animals were collected from their sponge prey organisms, it seems likely that growth of MDFs is induced while feeding on the sponges. It is also noteworthy that the muscular clot is formed later in the ontogeny of the MDFs.

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Correlation of chemical ecology with histological structures Shelled molluscs are usually assumed to be mechanically protected by the shell, and therefore few efforts have been made to study their natural products. However, many of these molluscs possess glands, some of them with defensive secretions. Bryan et al. (1997) reviewed molluscs with secretions which may have a defensive role. Among them, the prosobranch Calliostoma canalicu- latum secretes a yellow exudate from the mantle containing chemical defences against sympatric seastars (Bryan et al. 1997). Secretions in pulmonates and opisthobranchs have been reviewed by Faulkner (1992), Avila (1995, 2006), Cimino & Ghiselin (2001). As mentioned above, the hypobranchial gland is only found in shelled opisthobranchs (Acteonoidea, Cephalaspidea, Sacoglossa, Thecosomata) and heterobranchs (Table 2). Spongy mantle glands are present in Acteonoidea, Cephalaspidea, Anaspidea and Thecosomata, while the Blochmann gland is only found in Cephalaspidea and Anaspidea (Table 2). Whether the chemical products described in these species are related to the glands present remains to be further investi- gated. At the present there seems to be insufficient evidence to correlate the presence of particular glands with specific natural products. Also, as discussed above, acid secretions are stored in nonstaining vacuoles of large cells, such as those in spongy mantle glands, subepidermal acid glands and the median buccal gland. A glandular stripe is present in many groups (Cephalaspidea, Sacoglossa, Anaspidea, Dendronotoidea, Arminoidea and Aeolidoidea) but again, the relationship with the natural products described is uncertain (Table 2). The Chromodorididae do not possess any of the above mentioned glands and seem to have evolved a series of specific (but not exclusive) massive glands, the MDFs. In fact, MDFs and MDF- like structures are present in many species of Doridoidea, as well as in some Cephalaspidea, Sacoglossa, Dendronotoidea and even Pulmonata (Table 2). Analysing the data presented in Table 2, it is evident that most doridoidean species possessing dietary terpenes or polypropionates (Figure 11) possess either MDFs or MDF-like structures. This condition could be related to the potential toxicity of the sequestered chemicals, thus providing protection to the slugs by concentrating the compounds in specific structures, and simultaneously, the animals will benefit by effectively using this concentrated area for defence (Avila & Paul 1997). Nevertheless, similar compounds are also found in species without MDFs. Polyproprionates are also recorded from the sacoglossans Elysia crispata and E. viridis, but only Plakobranchus ocellatus has many MDFs. Within the Nudibranchia, a group of Antobranchia species which do not seem to possess any large glands but possess interesting natural products (terpenes and/or diacylglycerids), includes Bathydoris and several dorids such as Austrodoris, Archidoris, Doris and Platydoris, and ‘Poro- stomata’ such as Dendrodoris, Phyllidia and Phyllidiella. These compounds are often very active as chemical defences (Figure 12; see references in Table 2). A shared trend between all these species is that they have been proven or suggested to have biosynthetic natural compounds. Thus, it can be tentatively stated that, in general, opisthobranchs possessing dietary terpenes or polypropionates store them in special glands (MDFs or similar structures), while biosynthetic chemicals are stored differently, probably at the cellular level. These would suggest a hypothetical scenario as shown in Figure 13. However, more data on the localisation of chemicals are needed in other species to further demonstrate this theory. From the current data, it seems that special accumulation structures are not present when chemical defences are biosynthesised, and instead single glandular cells could be responsible for the storage of the compounds (as suggested, for example, for macrovacuolated cells in Dendrodoris; Avila & Durfort 1996). Possible exceptions, although not in the Nudibranchia, seem to be Haminoea species and Elysia viridis, which possess other kinds of glands (Table 2). Furthermore, MDFs are not uniformly structured in all groups and a classification of MDFs into three different types is proposed here. Type 1 (with a duct leading to the exterior) is present only in Doridoidea accumulating dietary terpenes (Table 2). Type 2 (with a muscular clot) is

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O

H O

O 2,6-dimethyl-5-heptenal O OCOCH3

Luteorosin

AcO CHO

O CHO O Longifolin

Scalaradial

O OMe

O 9, 10-deoxytridachione

Figure 11 Chemical structure of some terpenes from opisthobranchs possessing MDFs or MDF-like glands: 2,6-dimethyl-5-heptenal (monoterpene from Melibe leonina), luteorosin (diterpene from Chromodoris lutero- sea), longifolin (sesquiterpene from Hypselodoris picta), scalaradial (sesterterpene from Glossodoris pallida) and 9-10-deoxytridachione (polypropionate from Plakobranchus ocellatus).

AcO O OAc AcO CHO

OAc H Olepupuane Hodgsonal

Figure 12 Chemical structure of some sesquiterpene compounds from opisthobranchs without accumulating glands: olepupuane (biosynthesised by Dendrodoris limbata) and hodgsonal (probably biosynthesised by Bathydoris hodgsoni).

observed in Cephalaspidea and Doridoidea with different kinds of dietary products (nitrogenated compounds or sesquiterpenes). Finally, Type 3 with the most common distribution is found in Sacoglossa and many Doridoidea. As indicated in Table 2, many species possess MDFs which cannot yet be assigned to any of the types, due to a lack of information. Further research is needed to complete this partial information. As mentioned above, the fact that dietary chemicals have to be stored in special glands, isolated from the rest of the body, may indicate the need of the organism to be protected from the sequestered chemicals. Therefore, all these data would support the hypothesis that the initial role of accumulation structures was that of excretion or autoprotection from the dietary chemicals, but later evolved into a defensive mechanism.

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HYPOTHETICAL SCENARIO FOR CHEMICAL DEFENCE IN OPISTHOBRANCH MOLLUSCS

Dietary compounds Biosynthetic Inorganic acids

Accumulating glands: large, Biosynthetic cells: small, Several types restricted distribution in wide distribution in mantle of acid glands mantle

PROTECTION AND EFFECTIVE USE OF DEFENCES

Figure 13 Hypothetical scheme of chemical ecology of opisthobranch molluscs describing the relationship between defence and histology.

In recent years, an effort has been made to locate the chemicals in the animal’s body (e.g., Avila 1995, Avila & Durfort 1996, Avila & Paul 1997, Cimino et al. 1999, Kubanek et al. 2000, Thoms et al. 2003). Location is important not only to know where the compounds are stored, transformed or biosynthesised, but also to ascertain their ecological role. Understanding the evo- lution of shell-less opisthobranchs is tightly coupled with the evolution of defensive products. However, the relationship between location of natural products in these molluscs and their ecological significance has only been addressed in a few cases (Cronin et al. 1995, Avila & Paul 1997). The data reported here show that more opisthobranch groups possess structures similar to MDFs than initially thought. In fact, even the more typical MDFs can show many differences at histological and cytological levels. The location of the natural products at the cellular level is so far very problematic and has been investigated mainly within plants and only a few marine organisms (see e.g., Gillor et al. 2000, Sakai et al. in press). The present authors have also tried to use immunocytological methods, although the trials to create antibodies for longifolin have produced no positive results so far (M. Preisfeld, C. Avila & H. Wägele, unpublished results). A new methodology, the use of oligonucle- otide aptamers (Famulok 1999) also seems to be difficult to apply in tracing these kinds of compounds (M. Famulok, personal communication 2005). According to the histological results, glandular structures are numerous in opisthobranch taxa, even within one and the same specimen. Often they are intermingled and cannot be separated by sectioning. Therefore, analysing parts of the body only give an indirect indication of where the substance might not be located. Localisation at the cellular level (or at least the organ level) is therefore badly needed. If one or another of these techniques is successful, these methods would allow us not only to detect known compounds at histological and cytological levels but also, simultaneously, to locate the site of biosynthesis, if the compound is biosynthesised, or alternatively, if the compound is from dietary origin, the transpor- tation pathway from the digestive gland to the accumulating structures. This is a topic that deserves extensive studies in the near future for a better understanding of the evolution of the Opisthobranchia. Although it is not the subject of this review, it should be mentioned here that some metabolites are located in the egg masses. Dolabellanins of sea hares in reproductive organs and eggs seem to be involved in antimicrobial protection for the egg masses (Iijima et al. 2003). In many cases the

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location of chemicals in the egg ribbons has a yet unknown function (Thoms et al. 2003), although Benkendorff et al. (2001) have demonstrated antibacterial activity in several molluscan egg masses. Another interesting topic is the possibility that symbionts may be related to the presence of some chemicals. There is, in fact, increasing evidence in marine invertebrates that symbionts, like Cyanobacteria, Prochloron or even Symbiodinium, may play an important role in producing bio- active chemicals or precursors within the hosts (Proksch et al. 2002, Hentschel et al. 2002, Con- stantino et al. 2004, G. König personal communication 2005). Perhaps in the future molluscs will also be a good source of micro-organisms that produce interesting compounds (see Armstrong et al. 2000 for an example). In fact, symbiotic bacteria have been described in molluscs (Klussmann- Kolb & Brodie 1999) and are somehow involved in reproduction and egg-laying processes. These bacteria do not seem to have any relationship with the natural products of the molluscs, because as far as is known, in Dendrodoris species, the bacteria described are not located in the same place as the natural products (Avila et al. 1991a). In Tylodina perversa, sequestration of dietary chemicals is not related to the presence of sponge symbionts and the symbionts of the sponge are not present in the molluscs (Thoms et al. 2003). Finally, it is worth mentioning that endosymbiosis in photo- synthetic slugs (Symbiodinium sp. in Cladobranchia, chloroplasts in Sacoglossa) is well documented (see Rumpho et al. 2000 for older literature, Wägele & Johnsen 2001, Wägele 2004), although, again, there seem to be no relation with the presence of secondary metabolites. A very peculiar case is that of Melibe pilosa, in which sterols are produced by incorporated zooxanthellae (Sym- biodinium sp.) (Whiters et al. 1982). Zooxanthellae are also incorporated in Phyllodesmium species, but Avila et al. (1998) and Slattery et al. (1998) detected diterpenes in P. guamensis that are obtained from its diet and do not seem to be related to the zooxanthellae.

Correlation of histology with taxonomy and phylogeny Recently, some authors have tried to interpret the possible phylogeny of opisthobranchs by creating an evolutionary scenario based on the findings of defensive systems and secondary metabolites (Cimino & Ghiselin 1998, Cimino et al. 1999, Cimino & Ghiselin 1999, Marín & Ros 2004) in an attempt to put their results into an evolutionary context (see e.g., Mollo et al. 2005). Investigations and publications on phylogeny of opisthobranchs and its subgroups based on morphological and histological characters, or on genes, are increasing. Nevertheless, these investigations in most cases are preliminary and very often contradict each other, regardless of whether they are based on morphological or molecular data (Wollscheid-Lengeling et al. 2001, Dayrat & Tillier 2002, Wägele et al. 2003, Grande et al. 2004, Vonnemann et al. 2005, Wägele & Klussmann-Kolb 2005, H. Wägele personal observation). Therefore, we still lack information on relationships of the major opistho- branch taxa which would enable our knowledge on histology and biochemistry presented here to be discussed in a phylogenetic context or even in an evolutionary context. Nevertheless, some findings can be discussed with regard to the taxonomy of the major clades. Contrary to the situation within the Opisthobranchia, the monophyly of the groups that are well known is supported in many analyses (see Wägele & Klussmann-Kolb 2005).

Blochmann’s glands

These glands are only present in members of the Cephalaspidea sensu stricto (after Mikkelsen 1996) and Anaspidea, two groups which have recently been brought into a closer relationship by several authors (Wollscheid-Lengeling et al. 2001, Dayrat & Tillier 2002, 2003, Wägele et al. 2003, Vonnemann et al. 2005, H. Wägele personal observation). This type of gland could have evolved in the common ancestor of these two groups. Spongy mantle glands also occur in these two groups but also in the Thecosomata and the Acteonoidea. Thecosomates are discussed as a possible offshoot

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of the Anaspidea by Dayrat & Tillier (2003) and the presence of these glands in the thecosomates would support their assumptions. The position of the Acteonoidea is very controversial. Whereas Mikkelsen (1996, 2002) excluded Acteon from the Opisthobranchia on a morphological basis and put the other members at the base of the Opisthobranchia, the molecular data indicate a closer relationship to the Nudipleura (Grande et al. 2004, Vonnemann et al. 2005). In the analysis of Wägele & Klussmann-Kolb (2005) the whole taxon Acteonoidea is excluded from the Opistho- branchia. In all these hypotheses it has to be assumed that the spongy gland has evolved very early in opisthobranch evolution and has been lost in more highly evolved ones, where shell and mantle cavity are reduced. As reviewed and discussed by Klussmann-Kolb (2004), the Bohadsch gland is a synapomorphy of the Aplysiidae, but not for all Anaspidea because it is lacking in Akera. It is difficult to interpret the glands in the gymnosomate Clione as Bohadsch glands because their morphology differs to some extent. If they are homologous, then this would support the results of Dayrat & Tillier (2003) which indicate that the Gymnosomata are closely related to aplysiids.

Dorsal mantle gland

This gland, with a typical position in the anterior mantle tissue and with ducts leading to the frontal mantle margin, is found only in members of the Tylodinoidea. The monophyly of this group has never been challenged (see Willan 1987) and the gland represents a further synapomorphy, despite the fact that the morphology of the glands differs in Tylodina and Umbraculum.

Median buccal gland

A gland producing sulphuric acid and opening into the oral tube is a synapomorphy of the Pleurobranchoidea and is only missing in the monotypic Tomthompsonia antarctica. Recent phy- logenetic investigations revealed contradictory results concerning the position of Tomthompsonia (Mikkelsen 2002, Vonnemann et al. 2005, Wägele & Klussmann-Kolb 2005) and so it is not known whether this gland is primarily absent or secondarily reduced in this species. The buccal gland in Plocamopherus ceylonicus seems to have evolved separately from the Pleurobranchoidea.

MDFs

From the data on histology and characteristics of the MDFs reported here, it can be said that they have evolved separately many times. Nevertheless, results on the phylogeny of Chromodorididae (Gosliner & Johnson 1999) allow the assumption that a rather typical MDF was present at the base of the Chromodorididae (Cadlina excluded) and this was the basis for the future evolution of MDFs.

Conclusions It will be apparent from this review that many aspects of chemical ecology and histology of opisthobranch molluscs remain unclear and most of the questions raised here deserve further research. Many glandular structures need to be analysed further at the histological and cytological level before wider conclusions can be drawn. Major questions that still require answers are the linkage of certain secondary metabolites with particular morphological and/or cellular structures, and whether these substances impose constraints on the cellular structures of the organs involved. This question also touches on evolutionary processes, inasmuch as we know little about the homology of all the different glandular types. Answering these questions would help in identifying the change of function of some of these glands. Further questions, so far hardly addressed at all, are the transportation of the chemicals to the glands, the biosynthetic sites, the duration of these

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substances in the organs, and whether or how often they have to be replaced. Investigation of ontogenetic processes, beginning with the egg and continuing into the larval and juvenile stages, will provide evidence for possible parental care and a possible starting point of de novo biosynthesis. Finally, we know little about the linkage of the toxicity of slugs to their (aposematic?) colouration and the effects on possible predators. Elucidating this linkage also requires further knowledge of the toxicity (bioactivity) of the substances involved, which are currently considered to have effects that range from antibacterial to the repellence of larger predators. Hopefully, this study will stimulate researchers to develop these topics in the near future.

Acknowledgements This study is the result of a long-term research programme on opisthobranchs. Many colleagues have contributed material or helped in collecting it and we apologise if we have forgotten to mention anyone: Gilianne Brodie, Ingo Burghardt, Katrin Iken, Lucas Cervera, F. Javier Cristobo, Stefan Hain, Annette Klussmann-Kolb, Katrin Linse, Nico Michiels, Paula Mikkelsen, Sandra Millen, Brian Penney, Luise Schmekel, Michael Schrödl, Gerhard Steiner, Gabi Strieso, Victoriano Urgorri, Leonard, Richard and Wolfgang Wägele, Richard Willan and Peter Wirtz. Thanks go also to Martina Maierl-Nebe, Annette Schletz and Petra Wahl for help in preparing histological slides and to Sergi Taboada for his help with the bibliography. Special gratitude goes to those organisations which have supported our research for several years: the German Science Foundation (DFG) with projects (Wa 618/3 to 618/8) to H.W., the German Academic Exchange Service (DAAD, Acciones Integradas Hispano-Alemanas 2003/2004), and the Ministry of Education and Science in Spain to C.A. and M.B. (ECOQUIM projects: REN2003-00545, REN2002-12006-E ANT, CGL2004-03356/ANT, and Acciones Integradas HA2002-0070).

References

Abramson, S.N., Radic, Z., Manker, D., Faulkner, D.J. & Taylor, P. 1989. Onchidal: a naturally occurring irreversible inhibitor of acetylcholinesterase with a novel mechanism of action. Molecular Pharma- cology 36, 349Ð354. Alvarez, R., Herrero, M., Lopez, S. & De Lera, A.R. 1998. Stereoselective synthesis of polyenic alarm pheromones of cephalaspidean molluscs. Tetrahedron 54, 6793Ð6810. Amsler, C.D., Iken, K.B., McClintock, J.B. & Baker, B.J. 2001. Secondary metabolites from Antarctic marine organisms and their ecological implications In Marine Chemical Ecology, J.B. McClintock & B.J. Baker (eds). Boca Raton, FL: CRC Press, 267Ð300. Anderson, E.S. 1973. The association of the nudibranch Rostanga pulchra MacFarland, 1905 with the sponges Ophlitaspongia pennata, Esperiopsis originalis and Plocamia karykina. Dissertation Abstracts Inter- national B 33, 5668. Anderson, G.B. 1971. A contribution to the biology of Doridella steinbergae and Corambe pacifica, MA Thesis, California State College, Hayward. Appleton, D.R., Sewell, M.A., Berridge, M.V. & Copp, B.R. 2002. A new biologically active malyngamide from a New Zealand collection of the sea hare Bursatella leachii. Journal of Natural Products 65, 630Ð631. Arimoto, H., Cheng, J.F., Nishiyama, S. & Yamamura, S. 1993. Synthetic studies on fully substituted gamma- pyrone-containing natural products: the absolute configurations of ilkonapyrone and peroniatriols I and II. Tetrahedron Letters 34, 5781Ð5784. Arimoto, H., Nishiyama, S. & Yamamura, S. 1990. Synthetic studies on fully substituted gamma-pyrone containing natural products: synthesis of gamma-pyrone derivatives obtained by decomposition of peroniatriols. Tetrahedron Letters 31, 5491Ð5494.

258 7044_book.fm Page 259 Friday, April 14, 2006 1:28 PM

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Armstrong, E., Boyd, K.G., Pisacane, A., Peppiatt, C.J. & Burgess, J.G. 2000. Marine microbial natural products in antifouling coatings. Biofouling 16, 215Ð225. Arnaud, F. 1978. A new species of Ascorhynchus (Pycnogonida) found parasitic on an opisthobranch mollusc. Zoological Journal of the Linnean Society 63, 99Ð104. Avila, C. 1992. A preliminary catalogue of natural substances of opisthobranch molluscs from Western Mediterranean and near Atlantic. Scientia Marina 56, 373Ð382. Avila, C. 1993. Sustancias naturales de moluscos opistobranquios: estudio de su estructura, origen y función en ecosistemas bentónicos. PhD Thesis, University of Barcelona, Spain. Avila, C. 1995. Natural products of opisthobranch molluscs: a biological review. Oceanography and Marine Biology: An Annual Review 33, 487Ð559. Avila, C. 1996. The growth of Peltodoris atromaculata Bergh, 1880 (Gastropoda: Nudibranchia) in the laboratory. Journal of Molluscan Studies 62, 151Ð157. Avila, C. 2006. Molluscan natural products as biological models: chemical ecology, histology and laboratory culture. In Molluscs. From Chemo-ecological Study to Biotechnological Application, G. Cimino & M. Gavagnin (eds). [subseries Marine Molecular Biotechnology, Vol. 2, W.E.G. Muller (ed.); Series Progress in Molecular and Subcellular Biology, Volume 43]. Berlin, Heidelberg: Springer-Verlag, 1Ð23. Avila, C., Ballesteros, M., Cimino, G., Crispino, A., Gavagnin, M. & Sodano, G. 1990a. Biosynthetic origin and anatomical distribution of the main secondary metabolites in the nudibranch mollusc Doris verrucosa. Comparative Biochemistry and Physiology 97B, 363Ð368. Avila, C., Ballesteros, M., Slattery, M., Starmer, J. & Paul, V.J. 1998. Phyllodesmium guamensis (Nudibranchia: Aeolidoidea), a new species from Guam (Micronesia). Journal of Molluscan Studies 64,147Ð160. Avila, C., Cimino, G., Crispino, A., Fontana, A., Gavagnin, M. Ortea, J. & Vardaro R.R. 1990b. Defensive strategies of Chromodorididae nudibranchs: origins, anatomical distribution and role of selected chemicals. Abstracts 25th European Marine Biology Symposium, Ferrara, Italy. Avila, C., Cimino, G. Crispino, A. & Spinella, A. 1991a. Drimane sesquiterpenoids in Mediterranean Den- drodoris nudibranchs: anatomical distribution and biological role. Experientia 47, 306Ð310. Avila, C., Cimino, G., Fontana, A., Gavagnin, M., Ortea, J. & Trivellone, E. 1991b. Defensive strategy of two Hypselodoris nudibranchs from Italian and Spanish coasts. Journal of Chemical Ecology 17, 625Ð636. Avila, C. & Durfort, M. 1996. Histology of epithelia and mantle glands of selected species of doridacean mollusks with chemical defensive strategies. The Veliger 39, 148Ð163. Avila, C., Iken, K., Fontana, A. & Cimino, G. 2000. Chemical ecology of the Antarctic nudibranch Bathydoris hodgsoni Eliot, 1907: defensive role and origin of its natural products. Journal of Experimental Marine Biology and Ecology 252, 27Ð44. Avila, C. & Paul, V.J. 1997. Chemical ecology of the nudibranch Glossodoris pallida: is the location of diet- derived metabolites important for defence? Marine Ecology Progress Series 150, 171Ð180. Ayer, S.W. & Andersen, R.J. 1983. Degraded monoterpenes from the opisthobranch mollusc Melibe leonina. Experientia 39, 255Ð256. Baalsrud, K. 1950. Chemical investigations on Pteropoda: isolation of a new sterol, pteropodasterol. Acta Chemica Scandinavica 4, 512Ð517. Baba, K. 1935. Notes on a nudibranch, Madrella sanguinea (Angas), with reference to its papillary glands. Venus 5, 181Ð187. Barbour, M.A. 1979. A note on the distribution and food preference of Cadlina laevis (Nudibranchia: Chro- modoriade). The Nautilus 93, 61Ð62. Barnes, D.K.A. & Bullough, L.W. 1996. Some observations on the diet and distribution of nudibranchs at Signy Island, Antarctica. Journal of Molluscan Studies 62, 281Ð287. Barsby, T., Linington, R.G. & Andersen, R.J. 2002. De novo terpenoid biosynthesis by the dendronotid nudibranch Melibe leonina. Chemoecology 12, 199Ð202. Becerro, M.A., Goetz, G., Paul, V.J. & Scheuer, P.J. 2001. Chemical defences of the sacoglossan mollusk Elysia rufescens and its host alga Bryopsis sp. Journal of Chemical Ecology 27, 2287Ð2299. Becerro, M.A., Turon, X., Uriz, M.J. & Templado, J. 2003. Can a sponge feeder be a herbivore?: Tylodina perversa (Gastropoda) feeding on Aplysina aerophoba (Demospongiae). Biological Journal of the Linnean Society 78, 429Ð438.

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Benkendorff, K., Davis, A.R. & Bremer, J.B. 2001. Chemical defence in the egg masses of benthic inverte- brates: an assessment of antibacterial activity in 39 mollusks and 4 polychaetes. Journal of Invertebrate Pathology 78, 109Ð118. Bergh, R. 1866. Bidrag til en Monographi af Pleurophyllidierne, en Familie af de gastropode Mollusker. Naturhistorisk Tidsskrift Stiftet af Henrik Kroyer 4, 207Ð380. Blochmann, F. 1883. Über die Drüsen im Mantelrand der Aplysien und verwandten Formen. Zeitschrift für Wissenschaftliche Zoologie 38, 411Ð418. Blunt, J.W., Copp, B.R., Munro, M.H.G., Northcote, P.T. & Prinsep, M.R. 2005. Marine natural products. Natural Products Reports 22, 15Ð61. Böck, P. 1989. Romeis Mikroskopische Technik. München: Urban & Schwarzenberg, 17th edition. Born, E. 1910. Beiträge zur feineren Anatomie der Phyllirhoe bucephala. Zeitschrift für Wissenschaftliche Zoologie 97, 105Ð197. Bouchet, P. & Ortea, J. 1980. Quelques Chromodorididae bleus (Mollusca, Gastropoda, Nudibranchiata) de l’Atlantique oriental. Annales de l’Institute Océanographique Paris 56, 117Ð125. Brodie, G.B. 2005. Redescription of the Australian endemic nudibranch Dendrodoris maugeana Burn, 1962 (Gastropoda: Opisthobranchia, Doridoidea) new and reviewed features important for future phyloge- netic analyses of porostomes. Molluscan Research 25, 37Ð46. Bryan, P.J., McClintock, J.B. & Baker, B.J. 1998. Population biology and antipredator defences of the shallow- water Antarctic nudibranch Tritoniella belli. Marine Biology 132, 259Ð265. Bryan, P.J., McClintock, J.B. & Hamann, M. 1997. Behavioral and chemical defenses of marine prosobranch gastropod Calliostoma canaliculatum in response to sympatric seastars. Journal of Chemical Ecology 23, 645Ð658. Bryan, P.J., Yoshida, W.Y., McClintock, J.B. & Baker, B.J. 1995. Ecological role for pteroenone, a novel antifeedant from the conspicuous Antarctic pteropod Clione antarctica (Gymnosomata: Gastropoda). Marine Biology 122, 271Ð277. Burghardt, I., Evertsen J., Johnsen, G. & Wägele, H. 2005. Mutualistic symbiosis of aeolid Nudibranchia (Mollusca, Gastropoda, Opisthobranchia) with zooxanthellae of the genus Symbiodinium. Symbiosis 38, 227Ð250. Burghardt, I. & Wägele, H. 2004. A new solar powered species of the genus Phyllodesmium Ehrenberg, 1831 (Mollusca: Nudibranchia: Aeolidoidea) from Indonesia with analysis of its photosynthetic activity and notes on biology. Zootaxa 596, 1Ð18. Bürgin-Wyss, K. 1961. Die Rückenanhänge von Trinchesia coerulea (Montague). Revue Suisse de Zoologie 68, 461Ð582. Burgoyne, D.L., Dumdei, E. J. & Andersen, R. J. 1993. Acanthenes a to c: a chloro, isothiocyanate, formamide sesquiterpene triad isolated from the northeastern Pacific marine sponge Acanthella sp. and the dorid nudibranch Cadlina luteomarginata. Tetrahedron 49, 4503Ð4510. Burn, R. & Thompson, T.E. 1998. Order Cephalaspidea. In Mollusca: The Southern Synthesis. Fauna of Australia. Vol. 5. P.R. Beesley et al. (eds). Melbourne: CSIRO Publishing, 943Ð959. Butzke, D., Machuy, N., Rudel, T. & Meyer, T.F. 2002. Identification of a new cytotoxic activity from the ink of Aplysia punctata (CA136:322390). Patent Cooperation Treaty, International Application, 1Ð87. Buznikov, G.A. & Manukhin, B.N. 1962. The blocking substance of mollusc embryos and its role in regulation of embryonic motor activity. Chemical Abstracts 57, 17228g. Calado, G. & Urgorri, V. 2001. Feeding habits of Calma glaucoides (Alder & Hancock, 1854): its adaptive structures and behaviour. Bollettino Malacologico 37, 177Ð180. Carefoot, T.H. 1967. Growth and nutrition of Aplysia punctata feeding on a variety of marine algae. Journal of the Marine Biological Association of the United Kingdom 47, 565Ð589. Carefoot, T.H. 1987. Aplysia: its biology and ecology. Oceanography and Marine Biology: An Annual Review 25, 167Ð284. Carmely, S., Ilan, M. & Kashman, Y. 1989. 2-Imidazole alkaloids from the marine sponge Leucetta chagosensis. Tetrahedron 45, 2193Ð2212. Castedo, L., Quiñoá, E. & Riguera, R. 1983. Sterol peroxides from Aplysia punctata. Anales de Quimica Serie C 79, 454Ð455.

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Castiello, D., Cimino, G., De Rosa, S., De Stefano, S., Izzo, G. & Sodano, G. 1978. Studies on the chemistry of the relationship between the opisthobranch Peltodoris atromaculata and the sponge Petrosia ficiformis. Colloques Internationaux du Centre National de la Recherche Scientifique 291, 413Ð416. Castiello, D., Cimino, G., De Rosa S., De Stefano, S. & Sodano, G. 1980. High molecular weight poly- acetylenes from the nudibranch Peltodoris atromaculata and the sponge Petrosia ficiformis. Tetrahe- dron Letters 21, 5047Ð5050. Cattaneo-Vietti, R., Angelini, S. & Bavestrello, G. 1993. Skin and gut spicules in Discodoris atromaculata (Bergh, 1880) (Mollusca: Nudibranchia). Bolletino Malacologico 29, 173Ð180. Cattaneo-Vietti, R., Angelini, S., Gaggero, L. & Lucchetti, G. 1995. Mineral composition of nudibranch spicules. Journal of Molluscan Studies 61, 331Ð337. Cattaneo-Vietti, R., Schiaparelli, S. & Chiantore, M. 2001. Food availability and trophic needs of Peltodoris atromaculata (Mollusca: Doridacea). Bollettino Malacologico 37, 77Ð80. Cedhagen, T. 1996. Foraminiferans as food for cephalaspideans (Gastropoda: Opisthobranchia) with notes on secondary tesks around calcareous foraminiferans. Phuket Marine Biological Center Special Publi- cations 16, 279Ð290. Ciavatta, M.L., Gavagnin, M., Puliti, R., Cimino, G., Martinez, E., Ortea, J. & Mattia, C.A. 1996a. Dolabriferol: a new polypropionate from the skin of the anaspidean mollusc Dolabrifera dolabrifera. Tetrahedron 52, 12831Ð12838. Ciavatta, M.L., Trivellone, E., Villani, G. & Cimino, G. 1996b. Prenylphenols from the skin of the aeolid mollusc Cratena peregrina. Gazetta Chimica Italiana 126, 707Ð710. Cimino, G., Ciavatta, M.L., Fontana, A. & Gavagnin, M. 2000. Metabolites of marine opisthobranchs: chemistry and biological activity. In Bioactive Natural Products, C. Tringali (ed.). London: Taylor and Francis Ltd, 577Ð637. Cimino, G., Crispino, A., De Stefano, S., Gavagnin M. & Sodano, G. 1986b. A naturally-occurring analog of methylthioadenosine (MTA) from the nudibranch mollusc Doris verrucosa. Experientia 42, 1301Ð1302. Cimino, G.A., Crispino, A., Gavagnin, M. & Sodano, G. 1990a. Diterpenes from the nudibranch Chromodoris luteorosea. Journal of Natural Products 53, 102Ð106. Cimino, G., Crispino, A., Gavagnin, M., Trivellone, E. & Zubía, E. 1993b. Archidorin: a new ichthyotoxic diacylglycerol from the Atlantic dorid nudibranch Archidoris tuberculata. Journal of Natural Products 56, 1642Ð1646. Cimino, G.A., Crispino, A., Sodano, G. & Spinella, A. 1987a. Alchilpiridine ed alchilbenzeni da Opisthobran- chi Bullomorfi: composti relazionati ai feromoni d’allarme del Navanax inermis. Atti del XVII Con- vegno Nazionale della Divisione di Chimica Organica, Società Chimica Italiana. Cimino, G.A., Crispino, A., Spinella, A. & Sodano, G. 1988a. Two ichthyotoxic diacylglycerols from the opisthobranch mollusc Umbraculum mediterraneum. Tetrahedron Letters 29, 3613Ð3616. Cimino, G., De Giulio, A., De Rosa, S. & Di Marzo, V. 1989c. High molecular weight polyacetylenes from Petrosia ficiformis: further structural analysis and biological activity. Tetrahedron Letters 30, 3563Ð3566. Cimino, G., De Giulio, A., De Rosa, S. & Di Marzo, V. 1990c. Minor bioactive polyacetylenes from Petrosia ficiformis. Journal of Natural Products 30, 3563Ð3566. Cimino, G., De Rosa, S., De Stefano, S., Morrone, S, R. & Sodano, G. 1985a. The chemical defense of nudibranch molluscs; structure, biosynthetic origin and defensive properties of terpenoids from the dorid nudibranch Dendrodoris grandiflora. Tetrahedron 41, 1093Ð1100. Cimino, G., De Rosa, S., De Stefano, S. & Sodano, G. 1980a. Cholesten-4-en-4,16B,18,22R-tetrol-3-one 16,18-diacetate, a novel polyhydroxylated steroid from the hydroid Eudendrium sp. Tetrahedron Letters 21, 3303Ð3304. Cimino, G., De Rosa, S., De Stefano, S. & Sodano, G. 1981. Novel sesquiterpenoid esters from the nudibranch Dendrodoris limbata. Tetrahedron Letters 22, 1271Ð1272. Cimino, G., De Rosa, S., De Stefano, S. & Sodano, G. 1982. The chemical defense of four Mediterranean nudibranchs. Comparative Biochemistry and Physiology 73B, 471Ð474. Cimino, G., De Rosa, S., De Stefano, S. & Sodano, G. 1985b. Observations on the toxicity and metabolic relationships of polygodial, the chemical defense of the nudibranch Dendrodoris limbata. Experientia 41, 1335Ð1336.

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HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Cimino, G., De Rosa, S., De Stefano, S. & Sodano, G. 1986a. Marine natural products: new results from Mediterranean invertebrates. Pure and Applied Chemistry 58, 375Ð386. Cimino, G., De Rosa, S., De Stefano, S., Sodano, G. & Villani, G., 1983. Dorid nudibranch elaborates its own chemical defence. Science 219, 1237Ð1238. Cimino, G., De Stefano, S., De Rosa, S., Sodano, G. & Villani, G. 1980b. Novel metabolites from some predator-prey pairs. Bulletin des Societés Chimiques Belges 89, 1069Ð1073. Cimino, G., De Stefano, S., Guerriero, A. & Minale, L. 1975. Furanosesquiterpenoids in sponges. IV. Micro- cionins from Microciona toxystila. Tetrahedron Letters 43, 3723Ð3726. Cimino, G., De Stefano, S. & Minale, L. 1973. Deoxoscalarin, a further sesterterpene with the unusual tetracyclic carbon skeleton of scalarin, from Spongia officinalis. Experientia 29, 934Ð936. Cimino, G., De Stefano, S. & Minale, L. 1974. Scalaradial, a third sesterterpene with the tetracarbocyclic skeleton of scalarin from the sponge Caccospongia mollior. Experientia 30, 846Ð747. Cimino, G., Fontana, A. & Gavagnin, M. 1999. Marine opisthobranch molluscs: chemistry and ecology in sacoglossans and dorids. Current Organic Chemistry 3, 327Ð372. Cimino, G., Fontana, A. & Gavagnin, M. 2004. Biosynthesis in opisthobranch molluscs: general outline in the light of recent use of stable isotopes. Phytochemistry Reviews 3, 285Ð307. Cimino, G., Fontana, A., Giménez, F., Marín, A., Mollo, E., Trivellone, E. & Zubía, E. 1993a. Biotransfor- mation of a dietary sesterterpenoid in the Mediterranean nudibranch Hypselodoris orsini. Experientia 49, 582Ð586. Cimino, G., Gavagnin, M., Sodano, G., Puliti, R., Mattia, C.A. & Mazzarella, L. 1988c. Verrucosin-A and -B, ichthyotoxic diterpenoic acid glycerides with a new carbon skeleton from the dorid nudibranch Doris verrucosa. Tetrahedron 44, 2301Ð2310. Cimino, G., Gavagnin, M., Sodano, G., Spinella, A., Strazzullo, G., Schmitz, F.J. & Yalamanchili, G. 1987b. Revised structure of bursatellin. Journal of Organic Chemistry 52, 2301Ð2303. Cimino, G. & Ghiselin, M.T. 1998. Chemical defence and evolution in Sacoglossa (Mollusca: Gastropoda: Opisthobranchia). Chemoecology 8, 51Ð60. Cimino, G. & Ghiselin, M.T. 1999. Chemical defence and evolutionary trends in biosynthetic capacity among dorid nudibranchs (Mollusca: Gastropoda: Opisthobranchia). Chemoecology 9, 187Ð207. Cimino, G. & Ghiselin, M.T. 2001. Marine natural products chemistry as an evolutionary narrative. In McClintock, J.B. & Baker, B.J. (eds). Marine Chemical Ecology, Boca Raton, FL: CRC Press, 115Ð154. Cimino, G. & Sodano, G. 1989. The chemical ecology of Mediterranean opisthobranchs. Chemica Scripta 29, 389Ð394. Cimino, G. & Sodano, G. 1994. Transfer of sponge secondary metabolites to predators. In Sponges in Time and Space, R.W.M. Van Soest et al. (eds). Rotterdam: Balkema, 459Ð472. Cimino, G., Sodano, G. & Spinella, A. 1988b. Occurrence of olepupuane in two Mediterranean nudibranchs: a protected form of polygodial. Journal of Natural Products 51, 1010Ð1011. Cimino, G., Sodano, G. & Villani, G. 1990b. Studio su basi chimiche dei comportamnti biologici dei molluschi Opistobranchi. Atti Congresso Sorrento. Lavori Società Italiana di Malacologia 23, 229Ð240. Cimino, G.A., Spinella, A., Scopa, A. & Sodano, G. 1989a. Umbraculumin b an unusual 3 hydroxybutyric acid ester from the opisthobranch mollusc Umbraculum mediterraneum. Tetrahedron Letters 30, 1147Ð1148. Cimino, G., Spinella, A. & Sodano, G. 1989b. Potential alarm pheromones from the Mediterranean opisthobanch Scaphander lignarius. Tetrahedron Letters 30, 5003Ð5004. Constantino, V., Fattorusso, E., Menna, M. & Taglialatela-Scafati, O. 2004. Chemical diversity of bioactive marine natural products: an illustrative case study. Current Medical Chemistry 11, 1671Ð1692. Coulom, C. 1966. Senior Honor’s Report, University of California (USA). As reported in Harris (1973). [Referred to as: “Cullon, C. (1966)” in Harris (1971)]. Cronin, G., Hay, M.E., Fenical, W. & Lindquist, N. 1995. Distribution, density and sequestration of host chemical defenses by the specialist nudibranch Tritonia hamnerorum found at high densities on the sea fan Gorgonia ventalina. Marine Ecology Progress Series 119, 177Ð189. Davies-Coleman, M.T. & Faulkner, D.J., 1991. New diterpenoic acid glycerides from the Antarctic nudibranch Austrodoris kerguelensis. Tetrahedron 47, 9743Ð9750.

262 7044_book.fm Page 263 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Dayrat, B. & Tillier, S. 2002. Evolutionary relationships of euthyneuran gastropods (Mollusca): a cladistic re- evaluation of morphological characters. Zoological Journal of the Linnean Society 135, 403Ð470. Dayrat, B. & Tillier, S. 2003. Goals and limits of phylogenetics. The euthyneuran gastropods. In Molecular Systematics and Phylogeography of Mollusks, C. Lydeard & D. Lindberg (eds). Washington, London: Smithsonian Books, 161Ð184. De Medeiros, E.F., Herbert, J.M. & Taylor, R.J.K. 1990. The synthesis and absolute configuration of the novel ichthyotoxic diacyglycerol, umbraculumin A. Tetrahedron Letters 31, 5843Ð5844. De Medeiros, E.F. Herbert, J.M. & Taylor, R.J.K. 1991. The synthesis and absolute configuration of the novel ichthyotoxic diacylglycerols, umbraculumin A and umbraculumin C. Journal of the Chemical Society Perkin Transactions 10, 2725Ð2730. de Nys, R., Steinberg, P.D., Rogers, C.N., Charlton, T.S. & Duncan, M.W. 1996. Quantitative variation of secondary metabolites in the sea hare Aplysia parvula and its host plant, Delisea pulchra. Marine Ecology Progress Series 130, 135Ð146. De Petrocellis, L., Di Marzo, V., Arca, B., Gavagnin, M., Minei, R. & Cimino, G. 1991. The effect of diterpenoidic diacylglycerols on tentacle regeneration in Hydra vulgaris. Comparative Biochemistry & Physiology 100C, 603Ð608. De Petrocellis, L., Orlando, P., Gavagnin, M., Ventriglia, M., Cimino, G. & Di Marzo, V. 1996. Novel diterpenoid diacylglycerols from marine molluscs: potent morphogens and protein kinase C activators. Experientia 52, 874Ð877. Dumdei, E.J. 1994. Terpenoid metabolites from three dorid nudibranchs and a new bromotryptamine derivative from the northeast Pacific sponge Plocamissa igzo. Dissertation Abstracts International B 54, 4128. Dumdei, E.J., Flowers, A.E., Garson, M.J. & Moore, C.J. 1997b. The biosynthesis of sesquiterpene isocyanides and isothiocyanates in the marine sponge Acanthella cavernosa (Dendy); evidence for dietary transfer to the dorid nudibranch Phyllidiella pustulosa. Comparative Biochemistry and Physiology 113A, 1385Ð1392. Dumdei, E.J., Kubanek, J., Coleman, J.E., Pika, J., Andersen, R.J., Steiner, J.R. & Clardy, J. 1997a. New terpenoid metabolites from the skin extracts, an egg mass, and dietary sponges of the northeastern Pacific dorid nudibranch Cadlina luteomarginata. Canadian Journal of Chemistry 75, 773Ð789. Eales, N.B. 1921. Aplysia. Liverpool Marine Biological Committee Memoirs 24, 1Ð84. Ebel, R., Marín, A., & Proksch, P. 1999. Organspecific distribution of dietary alkaloids in the marine opistho- branch Tylodina perversa. Biochemical Systematics and Ecology 27, 769Ð777. Edlinger, K. 1982. On sense physiology and ultrastructure of the unspecialised epidermis of Haminea navicula (Da Costa, 1778) (Mollusca Ð Opisthobranchia). Zoologischer Anzeiger Jena 209, 345Ð361. Edmunds, M. 1964. Eolid Mollusca from Jamaica, with descriptions of two new genera and three new species. Bulletin of Marine Science of the Gulf and Carribean 14, 1Ð32. Edmunds, M. 1966a. Protective mechanisms in the Eolidacea (Mollusca Nudibranchia). Journal of the Linnean Society of London Zoology 46, 27Ð71. Edmunds, M. 1966b. Defensive adaptations of Stiliger vanellus Marcus, with a discussion on the evolution of “nudibranch” mollusks. Proceedings of the Malacological Society of London 37, 73Ð81. Edmunds, M. 1968. Acid secretion in some species of Doridacea (Mollusca, Nudibranchia). Proceedings of the Malacological Society of London 38, 121Ð133. Edmunds, M. 1987. Color in opisthobranchs. American Malacological Bulletin 5, 185Ð196. Edmunds, M. & Thompson, T.E. 1972. Opisthobranchiate Mollusca from Tanzania IV. Pleurobranchomorpha, Dendronotoidea and Arminoidea. Proceedings of the Malacological Society of London 40, 219Ð234. Evans, T.J. 1922. Calma glaucoides. A study in adaptation. Quarterly Journal of Microscopical Science 66, 439Ð455. Fahey, S.J. & Garson, M.J. 2002. Geographic variation of natural products of tropical nudibranch Asteronotus cespitosus. Journal of Chemical Ecology 28, 1773Ð1785. Famulok, M. 1999. Oligonucleotide aptamers that recognize small molecules. Current Opinion in Structural Biology 9, 324Ð329. Faulkner, D.J. 1988. Feeding deterrents in mollucsc. In Biomedical Importance of Marine Organisms, D.G. Fautin (ed.). Memoirs of the California Academy of Sciences 13, 29Ð36.

263 7044_book.fm Page 264 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Faulkner, D.J. 1992. Chemical defenses of marine molluscs. In Ecological Roles of Marine Natural Products, V.J. Paul (ed.). Ithaca: Comstock Publishing Assoc, 119Ð163. Faulkner, D.J. 2000. Highlights of marine natural products chemistry (1972Ð1999). Natural Products Reports 17, 1Ð6. Faulkner, D.J. 2001. Marine natural products. Natural Products Reports 18, 1Ð49. Faulkner, D.J. 2002. Marine natural products. Natural Products Reports 19, 1Ð48. Faulkner, D.J. & Ghiselin, M.T. 1983. Chemical defence and evolutionary ecology of dorid nudibranchs and some other opisthobranch gastropods. Marine Ecology Progress Series 13, 295Ð301. Faulkner, D.J., Molinski, T.F., Andersen, R.J., Dumdei, E.J. & de Silva, E.D. 1990. Geographical variation in defensive chemicals from Pacific coast dorid nudibranchs and some related marine molluscs. Com- parative Biochemistry and Physiology 97C, 233Ð240. Fenical, W., Sleeper, H.L., Paul, V.J., Stallard, M.O. & Sun, H.H. 1979. Defensive chemistry of Navanax and related opisthobranch molluscs. Pure and Applied Chemistry 51, 1865Ð1874. Fernandez-Ovies, C.L. 1983. Notas sobre la anatomia e histologia de un ejemplar de Runcina ferruginea Kress, 1977 (Opisthobranchia: Runcinacea) recolectado en Asturias. Boletim Ciencias Naturales 31, 153Ð168. Findlay, J.A. & Li, G.Q. 2002. Novel terpenoids from the sea hare Aplysia punctata. Canadian Journal of Chemistry 80, 1697Ð1707. Fischer, H. 1892. Recherches sur la morphologie du foie des gastéropodes. Bulletin Scientifique de la France et de la Belgique Paris 24, 260Ð346. Fisher, L.R., Kon, S.K. & Thompson, S.Y. 1956. Vitamin A and carotenoids in certain invertebrates. IV. Mollusca: Loricata, Lamellibranchiata and Gastropoda. Journal of the Marine Biological Association of the United Kingdom 35, 41Ð46. Foale, S.J. & Willan, R.C. 1987. Scanning and transmission electron microscope study of specialized mantle structures in dorid nudibranchs (Gastropoda: Opisthobranchia: Anthobranchia). Marine Biology 95, 547Ð557. Fontana, A., Ávila, C., Martinez, E., Ortea, J.A., Trivellone, E. & Cimino, G. 1993. Defensive allomones in three species of Hypselodoris (Gastropoda, Nudibranchia) from the Cantabrian Sea. Journal of Chem- ical Ecology 19, 339Ð356. Fontana, A., Cavaliere, P., Ungur, N., D’Souza, L., Parameswaram, P.S. & Cimino, G. 1999b. New scalaranes from the nudibranch Glossodoris atromarginata and its sponge prey. Journal of Natural Products 62, 1367Ð1370. Fontana, A., Ciavatta, M.L., D’Souza, M.L., Mollo, E., Naik, C.G., Parameswaran, P.S., Wahidulla, S. & Cimino, G. 2001. Selected chemo-ecological studies of marine opisthobranchs from Indian coasts. Journal of the Indian Institute of Science 81, 403Ð415. Fontana, A., Ciavatta, M.L., Miyamoto, T., Spinella, A. & Cimino, G. 1999a. Biosynthesis of drimane terpenoids in dorid molluscs: pivotal role of 7-deacetoxyolepupuane in two species of Dendrodoris nudibranchs. Tetrahedron 55, 5937Ð5946. Fontana, A., Cutignano, A., Cimino, G., Domènech, A., Ballesteros, M., Calabrese. G., Della Sala, G. & Spinella, A. 2004. Isolation, structure determination and synthesis of new metabolites from the marine mollusc Scaphander lignarius. Abstracts of the XI International Symposium on Marine Natural Products. Sorrento (Italy). Fontana, A., Gavagnin, M., Mollo, E., Trivellone, E., Ortea, J.A. & Cimino, G. 1995. Chemical studies of Cadlina molluscs from the Cantabrian Sea (Atlantic Ocean). Comparative Biochemistry and Physi- ology 111B, 283Ð290. Fontana, A., Gimenez, F., Marin, A., Mollo, E. & Cimino, G. 1994b. Transfer of secondary metabolites from the sponges Dysidea fragilis and Pleraplysilla spinifera to the mantle dermal formations MDFs of the nudibranch Hypselodoris webbi. Experientia 50, 510Ð516. Fontana, A., Mollo, E., Ricciardi, D., Fakhr, I. & Cimino, G. 1997. Chemical studies of Egyptian opistobranchs: spongian diterpenoids from Glossodoris atromarginata. Journal of Natural Products 60, 444Ð448. Fontana, A., Tramice, A., Cutignano, A., d’Ippolito, G., Renzulli, L. & Cimino, G. 2003. Studies of the biogenesis of verrucosins, toxic diterpenoid glycerides of the Mediterranean mollusc Doris verrucosa. European Journal of Organic Chemistry 16, 3104Ð3108.

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Fontana, A., Trivellone, E., Mollo, E., Cimino, G., Avila, C., Martinez, E. & Ortea, J. 1994a. Further chemical studies of Mediterranean and Atlantic Hypselodoris nudibranchs — a new furanosesquiterpenoid from Hypselodoris webbi. Journal of Natural Products (Lloydia) 57, 510Ð513. Fontana, A., Villani, G. & Cimino, G. 2000. Terpene biosynthesis in marine molluscs: incorporation of glucose in drimane eaters of Dendrodoris nudibranchs via classical mevalonate pathway. Tetrahedron Letters 41, 2429Ð2433. Franc, A. 1968. Sous-classe des opisthobranches. In Traité de Zoologie, Anatomie, Systematique, Biologie. Tome V, Mollusques Gasteropodes et Scaphopodes. E. Fischer et al. (eds). Paris: Masson & Cie, 608Ð893. Fretter, V. & Graham, A. 1962. British Prosobranch Molluscs. London: The Ray Society. Fu, X., Hong, E.P. & Schmitz, F.J. 2000. New polypropionate pyrones from the Philippine sacoglossan mollusc Placobranchus ocellatus. Tetrahedron 56, 8989Ð8993. Fusetani, N., Wolstenhome, H.J., Matsunaga, S. & Hirota, H. 1991. Two new sesquiterpene isonitriles from the nudibranch Phyllidia pustulosa. Tetrahedron Letters 32, 7291Ð7294. Fusetani, N., Wolstenholme, H. J., Shinoda, K., Asai, N., Matsunaga, S., Onuki, H. & Hirota, H. 1992. Two sesquiterpene isocyanides and a sesquiterpene thiocyanate from the marine sponge Acanthella cf. cavernosa and the nudibranch Phyllidia ocellata. Tetrahedron Letters 33, 6823Ð6826. García-Gómez, J.C., Cimino, G. & Medina, A. 1990. Studies on the defensive behaviour of Hypselodoris species (Gastropoda: Nudibranchia): ultrastructure and chemical analysis of mantle dermal formations (MDFs). Marine Biology 106, 245Ð250. García-Gómez, J.C., Medina, A. & Coveñas, R. 1991. Study of the anatomy and histology of the mantle dermal formations (MDFs) of Chromodoris and Hypselodoris (Opisthobranchia: Chromodorididae). Malacologia 32, 233Ð240. Garson, M.J. 1993. The biosynthesis of marine natural products. Chemical Reviews 93, 1699Ð1733. Garson, M.J. 2001. Ecological perspectives on marine natural product biosynthesis. In Marine Chemical Ecology, J.B. McClintock & B.J. Baker (eds). Boca Raton, FL: CRC Press, 71Ð114. Garson, M.J., Simpson, J.S., Flowers, A.E. & Dumdei, E.J. 2000. Cyanide and thiocyanate-derived function- ality in marine organisms — structures, biosynthesis and ecology. Studies of Natural Products and Chemicals 21, 329Ð372. Gavagnin, M., Carbone, M., Mollo, E. & Cimino, G. 2003a. Further chemical studies on the Antarctic nudibranch Austrodoris kerguelenensis: new terpenoid acylglycerols and revision of the previous stereochemistry. Tetrahedron 59, 5579Ð5583. Gavagnin, M., Carbone, M., Mollo, E. & Cimino, G. 2003b. Austrodoral and austrodoric acid: nor-sesquiterpenes with a new carbon skeleton from the Antarctic nudibranch Austrodoris kerguelenensis. Tetrahedron Letters 44, 1495Ð1498. Gavagnin, M., De Napoli, A., Castelluccio, F. & Cimino, G. 1999b. Austrodorin-A and -B: first tricyclic diterpenoid 2′-monoglyceryl esters from an Antarctic nudibranch. Tetrahedron Letters 40, 8471Ð8475. Gavagnin, M., De Napoli, A., Cimino, G., Iken, K., Avila, C. & García, F.J. 1999a. Absolute stereochemistry of diterpenoid diacylglycerols from the Antarctic nudibranch Austrodoris kerguelenensis. Tetrahedron Asymmetry 10, 2647Ð2650. Gavagnin, M., Marín, A., Mollo, E., Crispino, A., Villani, G. & Cimino, G. 1994. Secondary metabolites from Mediterranean Elysioidea: origin and biological role. Comparative Biochemistry and Physiology 108B, 107Ð115. Gavagnin, M., Mollo, E., Calado, G., Fahey S., Ghiselin M., Ortea, J. & Cimino, G. 2001. Chemical studies of porostome nudibranchs: comparative and ecological aspects. Chemoecology 11, 131Ð136. Gavagnin, M., Mollo, E., Castelluccio, F., Montanaro, D., Ortea, J. & Cimino, G. 1997a. A novel dietary sesquiterpene from the marine sacoglossan Tridachia crispata. Natural Products Letters 10, 151Ð156. Gavagnin, M., Mollo, E. & Cimino, G. 1996. A new gamma-dihydropyrone-propionate from the Caribbean sacoglossan Tridachia crispata. Tetrahedron Letters 37, 4259Ð4262. Gavagnin, M., Mollo, E., Docimo, T., Guo, Y.W. & Cimino, G. 2004. Scalarane metabolites of the nudibranch Glossodoris rufomarginata and its dietary sponge from the South China Sea. Journal of Natural Products 67, 2104Ð2107.

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Gavagnin, M., Mollo, E., Montanaro, D., Ortea, J. & Cimino, G. 2000. Chemical studies of Caribbean sacoglossans: dietary relationships with green algae and ecological implications. Journal of Chemical Ecology 26, 1563Ð1578. Gavagnin, M., Spinella, A., Cimino, G. & Sodano, G. 1990. Stereochemistry of ichthyotoxic diacyglycerols from opisthobranch molluscs. Tetrahedron Letters 31, 6093Ð6094. Gavagnin, M., Spinella, A., Crispino, A., De Almeida-Epifanio, A., Marin, A. & Cimino, G. 1993. Chemical components from the Mediterranean ascoglossan Thuridilla hopei. Gazzetta Chimica Italiana 123, 205Ð208. Gavagnin, M., Trivellone, E., Castelluccio, F., Cimino, G. & Cattaneo-Vietti, R. 1995. Glyceryl ester of a new halimane diterpenoic acid from the skin of the Antarctic nudibranch Austrodoris kerguelenensis. Tetrahedron Letters 36, 7319Ð7322. Gavagnin, M., Ungur, N., Castelluccio, F. & Cimino, G. 1997b. Novel verrucosins from the skin of the Mediterranean nudibranch Doris verrucosa. Tetrahedron 52, 1491Ð1504. Gavagnin, M., Vardaro, R.R., Ávila, C., Cimino, G. & Ortea, J.A. 1992. Ichthyotoxic diterpenoids from the Cantabrian nudibranch Chromodoris luteorosea. Journal of Natural Products 55, 368Ð371. Gemballa, S. & Schermutzki, F. 2004. Cytotoxic haplosclerid sponges preferred: a field study on the diet of the dotted sea slug Peltodoris atromaculata (Doridoidea: Nudibranchia). Marine Biology 144, 1213Ð1222. Gibson, G.D. & Chia, F.S. 1989. Description of a new species of Haminoea, Haminoea callidegenita (Mollusca: Opithobranchia), with a comparison with two other Haminoea species found in the northeast Pacific. Canadian Journal of Zoology 67, 914Ð922. Gillete, R., Saeki, M. & Huang, R.C. 1991. Defensive mechanisms in notaspid snails: acid humor and evasiveness. Journal of Experimental Biology 156, 335Ð347. Gillor, O., Carmeli, S., Rahamim, Y., Fishelson, Z. & Ilan, M. 2000. Immunolocalization of the toxin latrunculin B within the Red Sea sponge Negombata magnifica (Demospongiae, Latrunculidae). Marine Biotech- nology 2, 213Ð223. Ginsburg, D.W. & Paul, V.J. 2001. Chemical defences in the sea hare Aplysia parvula: importance of diet and sequestration of algal secondary metabolites. Marine Ecology Progress Series 215, 261Ð274. Giordano, A., Monica, C.D., Landi, F., Spinella, A. & Sodano, G. 2000. Stereochemistry and total synthesis of janolusimide, a tripeptide marine toxin Tetrahedron Letters 41, 3979Ð3982. Gopichand, Y. & Schmitz, F.J. 1980. Bursatellin, a new diol dinitrile from the sea hare Bursatella leachii pleii. Journal of Organic Chemistry 45, 5383Ð5385. Gosliner, T.M. 1994a. Gastropoda: Opisthobranchia. Chapter 5, In Microscopic Anatomy of Invertebrates Volume 5: Mollusca I. F.W. Harrison & A.J. Kohn (eds). New York: Wiley-Liss. Inc., 253Ð355. Gosliner, T.M. 1994b. New species of Chromodoris and Noumea (Nudibranchia: Chromodorididae) from the western Indian Ocean and Southern Africa. Proceedings of the California Academy of Sciences 48, 239Ð252. Gosliner, T.M. 1996. Phylogeny of Ceratosoma (Nudibranchia: Chromodorididae), with descriptions of two new species. Proceedings of the California Academy of Sciences 49, 115Ð126. Gosliner T.M. 2001. Aposematic coloration and mimicry in opisthobranch molluscs: new phylogenetic and experimental data. Bolletino Malacologico 37, 163Ð170. Gosliner, T.M. & Behrens, D.W. 1997. Description of four new species of phanerobranch dorids (Mollusca: Nudibranchia) from the Indo-Pacific, with a redescription of Gymnodoris aurita (Gould, 1852). Proceedings of the California Academy of Sciences 49, 287Ð308. Gosliner, T.M. & Behrens, D.W. 1998. Five new species of Chromodoris (Mollusca: Nudibranchia: Chromo- dorididae) from the tropical Indo-Pacific Ocean. Proceedings of the California Academy of Sciences 50, 139Ð165. Gosliner, T.M. & Behrens, D.W. 2000. Two new species of Chromodorididae (Mollusca: Nudibranchia) from the tropical Indo-Pacific, with a redescription of Hypselodoris dollfisi (Pruvot-Fol, 1933). Proceedings of the California Academy of Sciences 52, 111Ð124. Gosliner, T.M. & Johnson, R.F. 1999. Phylogeny or Hypselodoris (Nudibranchia: Chromodorididae) with a review of the monophyletic clade of Indo-Pacific species, including descriptions of twelve new species. Zoological Journal of the Linnean Society 125, 1Ð114.

266 7044_book.fm Page 267 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Gosliner, T.M. & Johnson, S. 1994. Review of the genus Hallaxa (Nudibranchia, Actinocyclidea) with descriptions of nine new species. Veliger 37, 155Ð191. Granato, A.C., Berlinck, R.G.S., Magalhaes, A., Schefer, A.B., Ferreira, A.G., De Sanctis, B., De Freitas, J.C., Hajdu, E. & Migotto, A.E. 2000. Natural products from the marine sponges Aaptos sp. and Hymeni- acidon aff. heliophila, and from the nudibranch Doris aff. verrucosa. Quimica Nova 23, 594Ð599. Grande, C., Templado, J., Cervera, J.L. & Zardoya, R. 2004. Phylogenetic relationships among Opisthobranchia (Mollusca: Gastropoda) based on mitochondrial cox 1, trnV, and rrnL genes. Molecular Phylogenetics and Evolution 33, 378Ð388. Graziani, E.I. & Andersen, R.J. 1996. Investigations of sesquiterpenoid biosynthesis by the dorid nudibranch Acanthodoris nanaimoensis. Journal of the American Chemical Society 118, 4701Ð4702. Graziani, E.I. & Andersen, R.J. 1998. Limaciamine, a new diacylguanidine isolated from the North Sea nudibranch Limacia clavigera. Journal of Natural Products 61, 285Ð286. Guerriero, A., D’Ambrosio, M. & Pietra, F. 1987. Verecynarmin A, a novel briarane diterpenoid isolated from both the Mediterranean nudibranch mollusc Armina maculata and its prey, the pennatulacean octocoral Veretillum cynomorium. Helvetica Chimica Acta 70, 984Ð991. Guerriero, A., D’Ambrosio, M. & Pietra, F. 1988. Slowly interconverting conformers of the briarane diterpe- noidsverecynarmin B, C, and D, isolated from the nudibranch mollusc Armina maculata and the pennat- ulacean octocoral Veretillum cynomorium of east Pyrenean waters. Helvetica Chimica Acta 71, 472Ð485. Guerriero, A., D’Ambrosio, M. & Pietra, F. 1990. Isolation of the cembranoid preverecynarmin alongside some briaranes, the verecynarmins, from both the nudibranch mollusc Armina maculata and the octocoral Veretillum cynomorium of the east Pyrenean Mediterranean Sea. Helvetica Chimica Acta 73, 277Ð283. Guiart, J. 1901. Contribution à l’étude des gastéropodes opisthobranches et en particulier des céphalaspidés. Mémoires de la Société Zoologique de France 14, 1Ð219. Gustafson, K. & Andersen, R.J. 1985. Chemical studies of British Columbia nudibranchs. Tetrahedron 41, 1101Ð1108. Gustafson, K., Andersen, R.J., Cun-heng, H. & Clardy, J. 1985. Marginatafuran; a furanoditerpene with a new carbon skeleton from dorid nudibranch Cadlina luteomarginata. Tetrahedron Letters 26, 2521Ð2524. Hain, S., Wägele, H. & Willan, R.C. 1993. Tomthompsonia spiroconchalis Wägele & Hain, 1991 (Opitho- branchia: Notaspidea): a junior synonym of Adeorbis antarcticus Thiele, 1912 (Prosobranchia: Trun- catelloidea) with notes on diet and histology. Journal of Molluscan Studies 59, 366Ð368. Haumayr, U. & Schrödl, M. 2003. Revision of the endoparasitic copepod genus Ismaila Bergh, 1867, with description of eight new species. Spixiana 26, 1Ð33. Hellou, J., Andersen, R.J., Rafii, S., Arnold, E. & Clardy, J. 1981. Luteone, a twenty-three carbon terpenoid from the dorid nudibranch Cadlina luteomarginata. Tetrahedron Letters 22, 4173Ð4176. Hellou, J., Andersen R.J. &. Thompson, J.E. 1982. Terpenoids from the dorid nudibranch Cadlina luteomar- ginata. Tetrahedron 38, 1875Ð1879. Hentschel, U., Hopke, J., Horn, M., Friedrich, A.B., Wagner, M., Hacker, J. & Moore, B.S. 2002. Molecular evidence for a uniform microbial community in sponges from different oceans. Applied and Environ- mental Microbiology 68, 4431Ð4440. Herdman, W.A. & Clubb, J.A. 1892. Third report on the Nudibranchiata of the LMBC district. Proceedings of the Biological Society of Liverpool 3, 131Ð169. Higuchi, R., Miyamoto, T., Yamada, K. & Komori, T. 1998. Cytotoxic and ichthyotoxic compounds from marine Opisthobranchia and soft coral. Toxicon 36, 1703Ð1705. Hirota, H., Okino, T., Yoshimura, E. & Fusetani, N. 1998. Five new antifouling sesquiterpenes from two marine sponges of the genus Axinyssa and the nudibranch Phyllidia pustulosa. Tetrahedron 12, 13971Ð13980. Hoffmann, H. 1939. Opisthobranchia. In Klassen und Ordnungen des Tierreichs. 3. Band: Mollusca, II. Abteilung: Gastropoda. 3. Buch: Opisthobranchia, H.G. Bronn, (ed.). Leipzig: Akademische Verlags- gesellschaft, 1Ð1247. Horgen, F.D., De los Santos, D.B., Goetz, G., Sakamoto, B., Kan, Y., Nagai, H. & Scheuer, P.J. 2000. A new depsipeptide from the sacoglossan mollusk Elysia ornata and the green alga Bryopsis species. Journal of Natural Products 63, 152Ð154.

267 7044_book.fm Page 268 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Howe, N.H. & Harris, L.G. 1978. Transfer of the sea anemone pheromone, anthopleurine, by the nudibranch Aeolidida papillosa. Journal of Chemical Ecology 4, 551Ð561. Huys, R. 2001. Splanchnotrophid systematics: a case of polyphyly and taxonomic myopia. Journal of Crus- tacean Biology 21, 106Ð156. Iijima, R., Kisugi, J. & Yamazaki, M. 2003. L-amino acid oxidase activity of an antineoplastic factor of a marine mollusk and its relationship to cytotoxicity. Developmental and Comparative Immunology 27, 505Ð512. Iken, K., Avila, C., Ciavatta, M.L., Fontana, A. & Cimino, G. 1998. Hodgsonal, a new drimane sesquiterpene from the mantle of the Antarctic nudibranch Bathydoris hodgsoni. Tetrahedron Letters 39, 5635Ð5638. Iken, K., Avila, C., Fontana, A. & Gavagnin, M. 2002. Chemical ecology and origin of defensive compounds in the Antarctic nudibranch Austrodoris kerguelenensis (Opisthobranchia: Gastropoda). Marine Biology 141, 101Ð109. Ireland, C., Biskupiak, J.E., Hite, G.J., Rapposch, M., Scheuer, P.J. & Ruble, J.R. 1984. Ilikonapyrone esters: likely defense allomones of the mollusc Onchidium verruculatum. Journal of Organic Chemistry 49, 559Ð561. Ireland, C. & Faulkner, D.J. 1981. The metabolites of the marine molluscs Tridachiella diomedea and Tridachia crispata. Tetrahedron 37, 233Ð240. Ireland, C., Faulkner, D.J., Finer, J.S. & Clardy, J. 1979. Crispatone, a metabolite of the opisthobranch mollusc Tridachia crispata. Journal of the American Chemical Society 101, 1275Ð1276. Ireland, C. & Scheuer, P.J. 1979. Photosynthetic marine mollusks: in vivo 14C incorporation into metabolites of the sacoglossan Placobranchus ocellatus. Science 205, 922Ð923. Izzo, I., De Caro, S., De Riccardis, F. & Spinella, A. 2000. Synthesis of alkylphenols and alkylcatechols from the marine mollusc Haminoea callidegenita. Tetrahedron Letters 41, 3975Ð3978. Jansen, B.J.M. & de Groot, A. 2004. Occurrence, biological activity and synthesis of drimane sesquiterpenoids. Natural Products Report 21, 449Ð477. Jensen, K. 1993. Morphological adaptations and plasticity of radular teeth of the Sacoglossa (=Ascoglossa) (Mollusca: Opisthobranchia) in relation to their food plants. Biological Journal of the Linnean Society 48, 135Ð155. Jensen, K. 1996. The Diaphanidae as a possible sister group of the Sacoglossa (Gastropoda, Opisthobranchia). In Origin and Evolutionary Radiation of the Mollusca, J. Taylor (ed.). Oxford: Oxford University Press, 231Ð247. Jiménez, C., Quínoa, E., Castedo, L. & Riguera, R. 1986. Epidioxy sterols from the tunicates Dendrodoa grossularia and Ascidiella aspersa and the gastropods Aplysia depilans and Aplysia punctata. Journal of Natural Products 49, 905Ð909. Johnson, P.M. & Willows, A.O.D. 1999. Defence in sea hares (Gastropoda, Opisthobranchia, Anaspidea): multiple layers of protection from egg to adult. Marine and Freshwater Behaviour and Physiology 32, 147Ð180. Johnson, R.F. & Gosliner, T.M. 1998. The genus Pectenodoris (Nudibranchia: Chromodorididae) from the Indo-Pacific, with the description of a new species. Proceedings of the California Academy of Sciences 50, 295Ð306. Johnson, R.F. & Gosliner, T.M. 2001. Two new species of Thorunna Bergh, 1878 (Mollusca: Nudibranchia: Chromodorididae) from the Indo-Pacific. Bollettino Malacologico 37, 143Ð150. Jongaramruong, J., Blackman, A.J., Skelton, B.W. & White, A.H. 2002. Chemical relationships between the sea hare Aplysia parvula and the red seaweed Laurencia filiformis from Tasmania. Australian Journal of Chemistry 55, 275Ð280. Karuso, P. 1987. Chemical ecology of the nudibranchs. In Scheuer, P.J. (ed.). Bioorganic Marine Chemistry, Berlin: Springer Verlag, 31Ð60. Kassühlke, K.E., Potts, B.C.M. & Faulkner, D.J. 1991. New nitrogenous sesquiterpenes from two Philippine nudibranchs, Phyllidia pustulosa and P. varicosa, and from a Palauan sponge, Halichondria cf. lendenfeldi. Journal of Organic Chemistry 56, 3747Ð3750. Kattner, G., Hagen, W., Graeve, M., Albers, C. (1998). Exceptional lipids and fatty acids in the pteropod Clione limacina (Gastropoda) from both polar oceans. Marine Chemistry 61, 219Ð228.

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Kawaguti, S., Kamishima, Y. & Nakamura, A. 1966. Electron microscopy on the pigment and mucous cells in an opisthobranchiate mollusk. Biological Journal of Okayama University 12, 23Ð34. Kawamine, K., Takeuchi, R., Miyashita, M., Irie, H., Shimamoto, K. & Ohfune, Y. 1991. A synthesis of (-)-bursatellin. Chemical and Pharmaceutical Bulletin 39, 3170Ð3171. Kennedy, G.Y. & Vevers, H.G. 1953. The occurrence of porphyrins in certain marine invertebrates. Journal of the Marine Biological Association of the United Kingdom. 33, 663Ð676. Klussmann-Kolb, A. 2004. Phylogeny of the Aplysiidae (Gastropoda, Opisthobranchia) with new aspects of the evolution of seahares. Zoologica Scripta 33, 439Ð462. Klussmann-Kolb, A. & Brodie G.D. 1999. Internal storage and production of symbiotic bacteria in the reproductive system of a tropical marine gastropod. Marine Biology 133, 443Ð447. Klussmann-Kolb, A. & Klussmann, A. 2003. A new species of Gastropteridae (Gastropoda, Opisthobranchia, Cephalaspidea) from tropical northeast Australia. Zootaxa 156, 1Ð12. Kolb, A. 1998. Morphology, anatomy and histology of four species of Armina Rafinesque, 1814 (Nudibranchia, Arminoidea, Arminidae) from the Mediterranean Sea and the Atlantic Ocean. Journal of Molluscan Studies 64, 355Ð386. Kolb, A. & Wägele, H. 1998. On the phylogeny of the Arminidae (Gastropoda, Opisthobranchia, Nudibranchia) with considerations of biogeography. Journal of Zoological Systematic and Evolution Research 36, 53Ð64. Kress, A. 1981. A scanning electron microscope study of notum structures in some dorid nudibranchs (Gastropoda: Opisthobranchia). Journal of the Marine Biological Association of the United Kingdom 61, 177Ð191. Ksebati, M.B. 1985. Natural products chemistry of soft coral Asteriospicularia sp. and the gorgonian Lep- togorgia sp. and the nudibranch Tridachia sp. Dissertation Abstracts International B 45, 2159Ð2160. Ksebati, M.B. & Schmitz, F.J. 1985. Tridachiapyrones: propionate-derived metabolites from the sacoglossan mollusc Tridachia crispata. Journal of Organic Chemistry 50, 5637Ð5642. Kubanek, J.M. 1998. Chemical studies on the origin of secondary metabolites in selected marine invertebrates. Dissertation Abstracts International B, 2204. Kubanek, J., Faulkner, D.J. & Andersen, R.J. 2000. Geographic variation and tissue distribution of endogenous terpenoids in the northeastern Pacific Ocean dorid nudibranch Cadlina luteomarginata: implications for the regulation of de novo biosynthesis. Journal of Chemical Ecology 26, 377Ð389. Kubanek, J., Graziani, E.I. &. Andersen, R.J. 1997. Investigations of terpenoid biosynthesis by the dorid nudibranch Cadlina luteomarginata. Journal of Organic Chemistry 62, 7239Ð7246. MacFarland, F. 1966. Studies of opisthobranchiate molluscs of the Pacific coast of North America. Memoirs of the California Academy of Sciences VI, 1Ð546. MacFarland, F. & O’Donoghue, C.O. 1929. A new species of Corambe from the Pacific coast of North America. Proceedings of the California Academy of Sciences 18, 1Ð26. Manzo, E., Ciavatta, M.L., Gavagnin, M., Mollo, E., Guo, Y.W. & Cimino, G. 2004. Isocyanide terpene metabolites of Phyllidiella pustulosa, a nudibranch (Mollusca: Gasteropoda) from the South China Sea. Journal of Natural Products 67, 1701Ð1704. Manzo, E., Ciavatta, M.L., Gavagnin, M., Mollo, E.,Wahidulla, S. & Cimino, G. 2005. New γ-pyrone propi- onates from the Indian Ocean sacoglossan Placobranchus ocellatus. Tetrahedron Letters 46, 465Ð468. Marbach, A. & Tsurnamal, M. 1973. On the biology of Berthellina citrina (Gastropoda: Opisthobranchia) and its defensive acid secretion. Marine Biology 21, 331Ð339. Marcus, E. 1955. Opisthobranchs from Brazil. Boletim da Faculdade de Filosofia, Ciencias e Letras, Univer- sidade de Sao Paulo, Zoologia 20, 89Ð262. Marcus, E. 1957. On Opisthobranchia from Brazil (2). Journal of the Linnean Society London 43, 390Ð486. Marcus, E. 1958. Notes on Opisthobranchia. Boletim Instituto Oceanografico Sao Paulo 7, 31Ð78. Marcus, E. 1959. Lamellariacea and Opisthobranchia. Reports of the Lund University Chile Expedition, 1948Ð1949. Lunds Universitets Arsskrift Avd. 2 55, 1Ð133. Marcus, E. & Marcus, E. 1955. Sea-hares and side-gilled slugs from Brazil. Boletim do Instituto Oceanografico Universidad de Sao Paulo 6, 3Ð33. Marcus du Bois-Reymond, E. 1970. On some opisthobranchs from Cananeia, Brazil. Boletim da Faculdade de Filosofia, Ciencias e Letras Universidad de Sao Paulo, Zoologia 27, 207Ð228.

269 7044_book.fm Page 270 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Marcus du Bois-Reymond, E. 1971. On some euthyneuran gastropods from the Indian and Pacific Oceans. Proceedings of the Malacological Society of London 39, 355Ð369. Marcus du Bois-Reymond, E. 1979. The Atlantic species of Onchidella (Gastropoda Pulmonata) Part 2. Boletim de Zoologia Universidade de Sao Paulo 4, 1Ð38. Marín, A., Alvarez, L.A., Cimino, G. & Spinella, A. 1999. Chemical defence in cephalaspidean gastropods: origin anatomical location and ecological roles. Journal of Molluscan Studies 65, 121Ð131. Marín, A., Di Marzo, V. & Cimino, G. 1991. A histological and chemical study of the cerata of the opistho- branch mollusc Tethys fimbria. Marine Biology 111, 353Ð358. Marín, A. & Ros, J. 2004. Chemical defences in sacoglossan opisthobranchs: taxonomic trends and evolutive implications. Scientia Marina 68, 227Ð241. Martin, R. & Walther, P. 2002. Effects of discharging nematocysts when an eolid nudibranch feeds on a hydroid. Journal of the Marine Biological Association of the United Kingdom 82, 455Ð462. Martin, R. & Walther, P. 2003. Protective mechanisms agains the action of nematocysts in the epidermis of Cratena peregrina and Flabellina affinis. Zoomorphology 122, 25Ð35. Mazzarelli, G. 1893. Monografia delle Aplysiidae del Golfo di Napoli. Memorie della Societa Italiana delle Scienze 9, 1Ð222. Mazzarelli, G. 1897. Contributo all conoscenza delle Tylodinidae, nuova Famiglia del gruppo dei molluschi tectibranchi. Zoologische Jahrbücher, Abteilung Systematik, Geographie, Biologie 10, 596Ð608. McClintock, J.B. & Baker, B.J. 1997. A review of the chemical ecology of Antarctic marine invertebrates. American Zoologist 37, 329Ð342. McClintock, J.B., Baker, B.J., Slattery, M., Heine, J.N., Bryan, P.J., Yoshida, W., Davies-Coleman, M.T. & Faulkner. D.J. 1994. Chemical defence of the common Antarctic shallow-water nudibranch Tritoniella belli (Mollusca: Tritonidae) and its prey, Clavularia frankliniana Rouel (Cnidaria: Octocorallia). Journal of Chemical Ecolology 20, 3361Ð3372. McClintock, J.B. & Janssen, J. 1990. Pteropod abduction as a chemical defence in a pelagic Antarctic amphipod. Nature 346, 462Ð464. McDonald, G.R. & Nybakken, J.W. Online. A list of the worldwide food habits of nudibranchs. Available HTTP: http://people.ucsc.edu/~mcduck/nudifood.htm (accessed 20 June 2005). Megina, C., Carballo, J.L., Cervera, J.L. & García-Gómez, J.C. 2002. The diet of Platydoris argo (Gastropoda: Nudibranchia) and the dietary specialization of sponge eating dorids. Journal of Molluscan Studies 68, 173Ð179. Meisenheimer, J. 1905. Die arktischen Pteropoden. Fauna Arktica 4, 407Ð430. Merton, H. 1920. Untersuchungen über die Hautsinnesorgane der Mollusken. I. Opisthobranchia. Abhandlun- gen herausgegeben von der Senckenbergischen Naturforschenden Gesellschaft 36, 447Ð473. Mikkelsen, P.M. 1996. The evolutionary relationship of Cephalaspidea s.l. (Gastropoda: Opisthobranchia): a phylogenetic analysis. Malacologia 37, 375Ð442. Mikkelsen, P.M. 2002. Shelled opisthobranchs. Advances in Marine Biology 42, 67Ð136. Minale, L. & Riccio, R. 1976. Constituents of the digestive gland of the molluscs of the genus Aplysia. I. Novel diterpenes from Aplysia depilans. Tetrahedron Letters 31, 2711Ð2714. Miyamoto, T., Ebisawa, Y. & Higuchi, R. 1995. Aplyparvunin, a bioactive acetogenin from the sea hare Aplysia parvula. Tetrahedron Letters 36, 6073Ð6074. Mollo, E., Gavagnin, M., Carbone, M., Guo, Y.-W. & Cimino, G. 2005. Chemical studies on Indopacific Ceratosoma nudibranchs illuminate the protective role of their dorsal horn. Chemoecology 15, 31Ð36. Moquin-Tandon, G. 1870. Recherches anatomiques sur l’ombrelle de la Méditeranée. Annales des Sciences Naturelles Zoologie 14, 1Ð73. Morton, J.E. 1972. The form and functioning of the pallial organs in the opisthobranch Akera bullata with a discussion on the nature of the gill in Notaspidea and other tectibranchs. The Veliger 14, 337Ð349. Muniaín, C., Valdés, A. & Ortea J. 1996. Redescription of Tyrinna nobilis Bergh, 1898 (Opisthobranchia: Chromodorididae) from Patagonia, Argentina. Journal of Molluscan Studies 62, 265Ð273. Odhner, N.H. 1926. Die Opisthobranchien. Further Zoological Results on the Swedish Antarctic Expedition 1901Ð1903 2(1), 1Ð100. Okada, Y. & Baba, K. 1938. On the luminous organs of a nudibranch Placomopherus tilesii Bergh. Annotationes Zoologicae Japonenses 17, 276Ð281.

270 7044_book.fm Page 271 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Okino, T., Yoshimura, E. & Hirota, H. 1996. New antifouling sesquiterpenes from four nudibranchs of the family Phyllidiidae. Tetrahedron 52, 9447Ð9454. Okuda, R.K., Scheuer, P.J., Hochlowski, J.E., Walker, R.P. & Faulkner, D.J. 1983. Sesquiterpenoid constituents of eight porostome nudibranchs. Journal of Organic Chemistry 48, 1866Ð1869. Ong, S. & Penney, B.K. 2001. Non-polar components of prey sponge extract attract Rostanga pulchra (Nudibranchia: Doridacea). The Veliger 44, 99Ð107. Ortea, J., Valdés, A. & García-Gómez, J.C. 1996. Revisión de las especies atlánticas de la familia Chromo- dorididae (Mollusca: Nudibranchia) del grupo cromático azul. Avicennia Suplemento 1, 1Ð165. Ortega, M.J., Zubia, E. & Salva, J. 1997. New polyhalogenated monoterpenes from the sea hare Aplysia punctata. Journal of Natural Products 60, 482Ð484. Pani, A., Marongiu, M.E., Obino, P., Gavagnin, M. & La Colla, P. 1991. Antimicrobial and antiviral activity of xylosyl-methylthio-adenosine, a naturally occuring analogue of methylthio-adenosine from Doris verrucosa. Experientia 47, 1228Ð1229. Pawlik, J.R. 1993. Marine invertebrate chemical defenses. Chemical Reviews 93, 1911Ð1922. Pelseneer, P. 1888. Report on the Pteropoda collected by H.M.S. “Challenger” during the years 1873–1876. Part III. Anatomy. Report of the Scientific Results of the Voyage with H.M.S. ”Challenger” 1873–1876. Zoology 23(2), 1Ð97. Pelseneer, P. 1894. Recherches sur divers opisthobranches. Mémoires Couronné de l’Academie Royal des Sciences de Belgique 53, 1Ð157. Penney, B.K. 2004. Individual selection and the evolution of chemical defence in nudibranchs: experiments with whole Cadlina luteomarginata (Nudibranchia: Doridina). Journal of Molluscan Studies Research Notes 70, 399Ð400. Pennings, S.C. & Paul, V.J. 1993. Sequistration of dietary secondary metabolites by three species of sea hares: location, specificity and dynamics. Marine Biology 117, 535Ð546. Perrier, R. & Fischer, H. 1911. Recherches anatomiques et histologiques sur la cavité palléale et ses dépen- dances chez les bulléens. Annales des Sciences Naturelles Zoologie 9, 1Ð181. Poiner, A., Paul, V.J. & Scheuer, P.J. 1989. Kumepaloxane, a rearranged trisnor sesquiterterpine from the bubble shell Haminoea cymbalum. Tetrahedron 45, 617Ð622. Pola, M., Cervera, J.L. & Gosliner, T.M. 2005. Review of the systematics of the genus Roboastra Bergh, 1877 (Nudibranchia, Polyceridae, Nembrothinae) with the description of a new species from the Galápagos Islands. Zoological Journal of the Linnean Society 144, 167Ð189. Ponder, W.F. & de Keyzer, R.G. 1998. Superfamily Pyramidelloidea. In Mollusca: The Southern Synthesis. Fauna of Australia. Vol. 5. P.R. Beesleyet al. (eds). Melbourne: CSIRO Publishing, 865Ð869. Porcelli, M., Cacciapuotti, G., Cimino, G., Gavagnin, M., Sodano, G. & Zappia, V. 1989. Biosynthesis and metabolism of 9-[5’-deoxy-5’-(methylthio)-b-D-xylofuranosyl]adenine, a novel natural analogue of methylthioadenosine. Biochemical Journal 263, 635Ð640. Potts, G.W. 1970. The ecology of Onchidoris fusca (Nudibranchia). Journal of the Marine Biological Asso- ciation of the United Kingdom 50, 269Ð292. Potts, G.W. 1981. The anatomy of respiratory structures in the dorid nudibranchs, Onchidoris bilamellata and Archidoris pseudoargus, with details on the epidermal glands. Journal of the Marine Biological Association of the United Kingdom 61, 959Ð982. Proksch, P., Edrada, R.A. & Ebel, R. 2002. Drugs from the seas — current status and microbiological implications. Applied Microbiology and Biotechnology 59, 125Ð134. Puliti, R., Gavagnin, M., Cimino, G., Mattia, C.A. & Mazzarella, L. 1992. Structure of chelonaplysin C: a spongian diterpenoid from nudibranch Chromodoris luteorosea. Acta Crystallographica C 48, 2145Ð2147. Quiñoá, E., Castedo, L. & Riguera, R. 1989. The halogenated monoterpenes of Aplysia punctata: a comparative study. Comparative Biochemistry and Physiology 92B, 99Ð102. Racioppi, R., Gavagnin, M., Strazzullo, G. & Sodano, G. 1990. Stereochemistry and synthesis of bursatellin from chloramphenicol. Tetrahedron Letters 31, 573Ð574. Risbec, J. 1953. Mollusques Nudibranches de la Nouvelle-Calédonie. Faune de l’Union Française Paris, Libraire Larose, Paris 15, 1Ð189. Rogers, C.N., De Nys, R., Charlton, T.S. & Steinberg, P.D. 2000a. Dynamics of algal secondary metabolites in two species of sea hare. Journal of Chemical Ecology 26, 721Ð744.

271 7044_book.fm Page 272 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Rogers, C.N., De Nys, R. & Steinberg, P.D. 2000b. Predation on juvenile Aplysia parvula and other small anaspidean, ascoglossan and nudibranch gastropods by pycnogonids. Veliger 43, 330Ð337. Rogers, C.N., De Nys, R, & Steinberg, P.D. 2002. Effects of algal diet on the performance and susceptibility to predation of the sea hare Aplysia parvula. Marine Ecology Progress Series 236, 241Ð254. Rogers, D.J. 1977. Antibody-like substances in marine organisms. In Marine Natural Products Chemistry, D.J. Faulkner & W.H. Fenical (eds). New York: Plenum Press, 311Ð327. Rogers, S.D. & Paul, V.J. 1991. Chemical defenses of three Glossodoris nudibranchs and their dietary Hyrtios sponges. Marine Ecology Progress Series 77, 221Ð232. Rudman, W.B. 1972a. A study of the anatomy of Pupa and Maxacteon (Acteonidae, Opisthobranchia), with an account of the breeding cycle of Pupa kirki. Journal of Natural History 6, 603Ð619. Rudman, W.B. 1972b. The genus Philine (Opisthobranchia, Gastropoda). Proceedings of the Malacological Society London 40, 171Ð187. Rudman, W.B. 1972c. The anatomy of the opisthobranch genus Hydatina and the functioning of the mantle cavity and alimentary canal. Zoological Journal of the Linnean Society 51, 121Ð139. Rudman, W.B., 1972d. The herbivorous opisthobranch genera Phanerophthalmus A. Adams and Smaragdinella A. Adams. Journal of Natural History, 5, 647Ð675. Rudman, W.B. 1981a. Further studies on the anatomy and ecology of opisthobranch molluscs feeding on the scleractinian coral Porites. Zoological Journal of the Linnean Society 71, 373Ð412. Rudman, W.B. 1981b. The anatomy and biology of alcyonarian feeding aeolid opisthobranch molluscs and their development of symbiosis with zooxanthellae. Zoological Journal of the Linnean Society 72, 219Ð262. Rudman, W.B. 1982. The taxonomy and biology of further aeolidacean and arminacean nudibranch molluscs with symbiotic zooxanthellae. Zoological Journal of the Linnean Society 74, 147Ð196. Rudman, W.B. 1984. The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: a review of the genera. Zoological Journal of the Linnean Society 81, 115Ð273. Rudman, W.B. 1995. The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: further species from New Caledonia and the Noumea romeri colour group. Molluscan Research 16, 1Ð43. Rudman, W.B. Seaslugforum. Online, Available HTTP: http://www.seaslugforum.net/. Rudman, W.B. & Darvell, B.W. 1990. Opisthobranch molluscs of Hong Kong: Part 1. Goniodorididae, Onchidorididae, Triophidae, Gymnodorididae, Chromodorididae (Nudibranchia). Asian Marine Biology 7, 31Ð79. Rumpho, M.E., Summer, E.J. & Manhart, J.R. 2000. Solar-powered sea slugs: mollusc/algal chloroplast symbiosis. Plant Physiology 123, 29Ð38. Sakai, R., Minato, S., Koike, K., Koike, K., Jimbo, M., Kamiya, H. 2005. Cellular and subcellular localization of kainic acid in the marine red alga Digenea simplex. Cell and Tissue Research 322, 491Ð502. Scheuer, P.J. 1992. Isocyanides and cyanides as natural products. Accounts of Chemical Research 25, 433Ð439. Schmitz, F.J., Gopichand, Y., Michaud, D., Prasad, R.S., Remaley, S., Hossain, M.B., Rahman, A., Sengupta, P.K. & Van Der Helm, D. 1981. Recent developments in research on metabolites from Caribbean marine invertebrates. Pure and Applied Chemistry 53, 853Ð865. Schrödl, M. 2002. Heavy infestation by endoparasitic copepod crustaceans (Poecilostomatoidea: Splanch- notrophidae) in Chilean opisthobranch gastropods, with aspects of splanchnotrophid evolution. Organ- isms Diversity and Evolution 2, 19Ð26. Schrödl, M. (ed.) 2003. Sea Slugs of Southern South America. Hackenheim: ConchBooks. Schrödl, M. & Millen, S.V. 2001. Revision of the nudibranch gastropod genus Tyrinna Bergh, 1898 (Doridoidea: Chromodorididae). Journal of Natural History 35, 1143Ð1171. Schrödl, M. & Wägele, H. 2001. Anatomy and histology of Corambe lucea Marcus, 1959 (Gastropoda, Nudibranchia, Doridoidea), with a discussion of the systematic position of Corambidae. Organisms Diversity and Evolution 1, 3Ð16. Schulz, F.N. 1905. Der histologische Bau der Säuredrüse von Pleurobranchaea meckelii. Verhandlungen der Gesellschaft Deutscher Naturforscher und Ärzte 76, 487Ð489. Schulze, A. & Wägele, H. 1998. Morphology, anatomy and histology of Flabellina affinis (Gmelin, 1791) (Nudibranchia, Aeolidoidea, Flabellinidae) and its relation to other Mediterranean Flabellina species. Journal of Molluscan Studies 64, 195Ð214.

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DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Simpson, J.S., Garson, M.J., Hooper, J.N.A., Cline, E.I. & Angerhofer, C.K. 1997. Terpene metabolites from the tropical marine sponge Axinyssa sp. nov. Astralian Journal of Chemistry 50, 1123Ð1127. Slattery, M., Avila, C., Starmer, J. & Paul, V.J. 1998. A sequestered soft coral diterpene in the aeolid nudibranch Phyllodesmium guamensis Avila, Ballesteros, Slattery, Starmer & Paul. Journal of Experimental Marine Biology and Ecology 226, 33Ð49. Sodano, G. & Spinella, A. 1986. Janolusimide: a lipophilic tripeptide toxin from the nudibranch mollusc Janolus cristatus. Tetrahedron Letters 27, 2505Ð2508. Soriente, A., Sodano, G., Reed, K.C. & Todd, C. 1993. A new ichthyotoxic diacylglycerol from the nudibranch Archidoris pseudoargus. Natural Products Letters 3, 31Ð35. Spinella, A., Alvarez, L.A. & Cimino, G. 1998. Alkylphenols from the cephalaspidean mollusc Haminoea callidegenita. Tetrahedron Letters 39, 2005Ð2008. Spinella, A., Alvarez, L.A., Cimino, G., Crispino, A., Fenical, W., Marín, A., Passeggio, A. & Villani, G. 1992b. Semiochemicals from some cephalaspidean molluscs. C21. Proceedings 7th International Symposium on Marine Natural Products, Capri, Naples, Italy. Spinella, A., Alvarez, L.A., Crispino, A., Marín, A., Villani, G. & Cimino, G. 1992c. Chemical signals in some cephalaspidean molluscs. Abstracts 11th International Malacological Congress, Siena, Italy, F. Giusti & G. Manganelli (eds). Unitas Malacologia: Siena, 289Ð290. Spinella, A. Alvarez, L.A., Passeggio, A. & Cimino, G. 1993. New 3-alkylpyridines from three Mediterranean cephalaspidean molluscs: structure, ecological role and taxonomic relevance. Tetrahedron 49, 1307Ð1314. Stachowicz, J.J. 2001. Chemical ecology of mobile benthic invertebrates: predators and prey, allies and competitors. In Marine Chemical Ecology, J.B. McClintock & B.J. Baker (eds). Boca Raton, FL: CRC Press, 157Ð194. Stanisic, J. 1998. Order Systellommatophora. In Mollusca: The Southern Synthesis. Fauna of Australia. Vol. 5. P.R. Beesley et al. (eds). Melbourne: CSIRO Publishing, 1060Ð1067. Streble, H. 1968. Bau und Bedeutung der Nesselsäcke von Aeolidia papillosa L., der Breitwarzigen Faden- schnecke (Gastropoda, Opisthobranchia). Zoologischer Anzeiger 180, 356Ð372. Szabo, C.M., Nakao, Y., Yoshida, W.Y. & Scheuer, P.J. 1996. Two diverse constituents of the cephalaspidean mollusk Smaragdinella calyculata. Tetrahedron 52, 9681Ð9686. Teeyapant, R., Kreis, P., Wray, V., Witte, L. & Proksch, P. 1993. Brominated secondary compounds from the marine sponge Verongia aerophoba and the sponge feeding gastropod Tylodina perversa. Zeitschrift fur Naturforschung C 48, 640Ð644. Thompson, J.E., Walker, R.P., Wratten, S.J. & Faulkner, D.J. 1982. A chemical defense mechanism for the nudibranch Cadlina luteomarginata. Tetrahedron 38, 1865Ð1873. Thompson, T.E. 1960. Defensive adaptations in opisthobranchs. Journal of the Marine Biological Association of the United Kingdom 39, 123Ð134. Thompson, T.E. 1969. Acid secretion in Pacific Ocean gastropods. Australian Journal of Zoology 17, 755Ð764. Thompson, T.E. 1970. Eastern Australian Pleurobranchomorpha (Gastrooda, Opisthobranchia). Journal of Zoology (London) 160, 173Ð198. Thompson, T.E. 1972. Eastern Australian Dendronotoidea (Gastropoda: Opisthobranchia). Zoological Journal of the Linnean Society 51, 63Ð77. Thompson, T.E. 1976. Biology of Opisthobranch Molluscs Volume 1. London: Ray Society. Thompson, T.E. 1983. Detection of epithelial acid secretions in marine molluscs: review of techniques and new analytical methods. Comparative Biochemistry and Physiology 74A, 615Ð621. Thompson, T.E. 1986. Investigation of the acidic allomone of the gastropod mollusc Philine aperta by means of ion chromatography and histochemical localisation of sulphate and chloride ions. Journal of Molluscan Studies 52, 38Ð44. Thompson, T.E. 1988. Acidic allomones in marine organisms. Journal of the Marine Biological Association of the United Kingdom 68, 499Ð517. Thompson, T.E. & Brown, G.H. 1984. Biology of Opisthobranch Molluscs. Volume 2. London: Ray Society. Thompson, T.E. & Colman, J.G. 1984. Histology of acid glands in Pleurobranchomorpha. Journal of Molluscan Studies 50, 66Ð67.

273 7044_book.fm Page 274 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Thompson, T.E. & Crampton, D.M. 1984. Biology of Melibe fimbriata, a conspicuous opisthobranch mollusc of the Indian Ocean, which has now invaded the Mediterranean Sea. Journal of Molluscan Studies 50, 113Ð121. Thompson T.E. & Slinn, D.J. 1959. On the biology of the opisthobranch Pleurobranchus membranaceus. Journal of the Marine Biological Association of the United Kingdom 38, 507Ð524. Thoms, C., Ebel, R., Hentschel, U. & Proksch, P. 2003. Sequestration of dietary alkaloids by the spongivorous marine mollusc Tylodina perversa. Zeitschrift fur Naturforschung 58, 426Ð432. Tischler, M. 1990. Terpenoids from the marine sponge Aplysilla glacialis and the nudibranch Cadlina luteo- marginata. Dissertations Abstract International B 52, 5280. Tischler, M. & Andersen, R.J. 1989. Glaciolide, a degraded diterpenoid with a new carbon skeleton from the nudibranch Cadlina luteomarginata and the sponge Aplysilla glacialis. Tetrahedron Letters 30, 5717Ð5720. Tischler, M., Andersen, R.J., Choudhary, M.I. & Clardy, J. 1991. Terpenoids of the sponge Aplysilla glacialis and specimens of the nudibranch Cadlina luteomarginata found on the sponge. Journal of Organic Chemistry 56, 42Ð47. Toyama, Y. & Tanaka, T. 1956. XIV. Fatty oils from a holothurian, nine gastropods and two anthozoans. Memoirs of the Faculty of Engineering Nagoya University 8, 40Ð44. Trinchese, S. 1877. Nota sulla struttura dell’uovo dei mammiferi e dei molluschi. Rendiconto delle Sessioni dell Accademia delle Scienze dell Instituto di Bologna 1876Ð1877, 36Ð37. Trinchese, S. 1881. Aeolididae e famiglie affini del Porto die Genova II. Part 2. Anatomia, fisiologia, embri- ologia delle Phyllobranchideae, Heraeidae, Aeolididae, Proctonotidae, Dotonidae del Porto Genova. Memorie della Classe di Scienze Fisiche Matematiche e Naturali 3, 1Ð142. Trowbridge, C.D. 2004. Emerging associations on marine rocky shores: specialist herbivores on introduced macroalgae. Journal of Animal Ecology 73, 294Ð308. Turón, X., Becerro, M.A. & Uriz, M.J. 2000. Distribution of brominated compounds within the sponge Aplysina aerophoba: coupling of X-ray microanalysis with cryofixation techniques. Cell and Tissue Reserach 301, 311Ð322. Valdés, A., Mollo, E. & Ortea, J.A. 1999. Two new species of Chromodoris (Mollusca: Nudibranchia, Chromodorididae) from Southern India, with a redescription of Chromodoris trimarginata (Winck- worth, 1946). Proceedings of the California Academy of Sciences 51, 461Ð472. Valdés, A. & Campillo, O.A. 2000. Redescription and reasessment of Cadlina luarna (Ev. Marcus & Er. Marcus, 1967), comb. nov. (Mollusca, Opisthobranchia, Doridina). Proceedings of the California Academy of Sciences 52, 77Ð85. Vayssière, A.J.B.M. 1883. Recherches anatomiques sur les genres Pelta (Runcina) et Tylodina. Annales des Sciences Naturelles Zoologie 15, 1Ð46. Vayssière, A.J.B.M. 1885. Recherches zoologiques et anatomiques sur les mollusques opisthobranches du Golfe de Marseille. 1er partie. Tectibranches. Annales de Musée Histoire Naturelle Marseille 2, 1Ð181. Vayssière, A.J.B.M. 1888. Recherches zoologiques et anatomiques sur les mollusques opisthobranches du Golfe de Marseille. 2me partie. Nudibranches et ascoglosses. Annales de Musée Histoire Naturelle Marseille 3, 1Ð160. Voltzow, J. 1994. Gastropoda: Prosobranchia. In Microscopic Anatomy of Invertebrates Volume 5: Mollusca I, F.W. Harrison & A.J. Kohn (eds). New York: Wiley-Liss. Inc., 111Ð252. Vonnemann, V., Schrödl, M., Klussmann-Kolb, A. & Wägele, H. 2005. Reconstruction of the phylogeny of the Opisthobranchia (Mollusca, Gastropoda) by means of 18S and 28S rDNA sequences. Journal of Molluscan Studies 71, 113Ð125. Voogt, P.A. 1970. Investigations into the capacity of synthesizing sterols and into sterol composition in the phyllum Mollusca. PhD Thesis, University of Utrecht (as reported in Voogt, 1972). Voogt, P.A. 1972. Lipid and sterol components and metabolism in Mollusca. In Chemical Zoology, Volume VII, Mollusca, M. Florkin & B.T. Scheer (eds). New York: Academic Press, 245Ð300. Voogt, P.A. 1973. Investigations of the capacity of synthesizing 3-sterols in mollusca. XI. Biosynthesis and composition of 3-sterols in some Acoela (Opisthobranchia). International Journal of Biochemistry 4, 479Ð488.

274 7044_book.fm Page 275 Friday, April 14, 2006 1:28 PM

DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS

Wägele, H. 1989a. Diet of some Antarctic nudibranchs (Gastropoda, Opisthobranchia, Nudibranchia). Marine Biology 100, 439Ð441. Wägele, H. 1989b. Über die Morphologie und Feinstruktur einiger Eigelege antarktischer Nudibranchia (Gastropoda, Mollusca). Zoologischer Anzeiger 222, 225Ð243. Wägele, H. 1989c. Revision of the Antarctic species of Bathydoris Bergh, 1884 and comparison with other known bathydorids (Opisthobranchia, Nudibranchia). Journal of Molluscan Studies 55, 343Ð364. Wägele, H. 1990. Revision of the Antarctic genus Notaeolidia Eliot, 1905 (Gastropoda, Nudibranchia) with a description of a new species. Zoologica Scripta 19, 309Ð330. Wägele, H. 1991. Studies on the morphology and anatomy of the Antarctic genera Pseudotritonia Thiele, 1912 and Telarma Odhner, 1934 with a discussion of the family Charcotiidae Odhner, 1926 (Nudi- branchia, Opisthobranchia). Zoological Journal of the Linnean Society 101, 359Ð389. Wägele, H. 1997. Histological investigation of some organs and specialized cellular structures in Opistho- branchia (Gastropoda) with the potential to yield phylogenetically significant characters. Zoologischer Anzeiger 236, 119Ð131. Wägele, H. 2004. Potential key characters in Opisthobranchia (Gastropoda, Mollusca) enhancing adaptive radiation. Organisms Diversity and Evolution 4, 175Ð188. Wägele, H., Barnes, D.K.A. & Bullough, L.W. 1995a. Redescription of Charcotia granulosa (Nudibranchia: Arminoidea: Charcotiidae) from Signy Island, Antarctica. Journal of Molluscan Studies 61, 197Ð207. Wägele, H., Brodie, G. & Klussmann-Kolb, A. 1999. Histological investigations on Dendrodoris nigra (Stimpson, 1855) (Gastropoda, Nudibranchia, Dendrodorididae). Molluscan Research 20, 79Ð94. Wägele, H., Bullough, L.W. & Barnes, D.K.A. 1995b. Anatomy of Pseudotritionia Thiele, 1912 and Notae- olidia Eliot, 1905 (Gastropoda: Opisthobranchia: Nudibranchia) from Signy Island, Antarctica. Journal of Molluscan Studies 61, 209Ð213. Wägele, H. & Cervera, J.L. 2001. Histological study of Goniodoris castanea (Alder and Hancock, 1845 (Nudibranchia, Doridoidea, Goniodorididae). Journal of Morphology 250, 61Ð69. Wägele, H. & Johnsen, G. 2001. Observations on the histology and photosynthetic performance of “solar- powered” opisthobranchs (Mollusca, Gastropoda) containing symbiotic chloroplasts or zooxanthellae. Organisms Diversity and Evolution 1, 193Ð210. Wägele, H. & Klussmann-Kolb, A. 2005. Opisthobranchia (Mollusca, Gastropoda) — more than just slimy slugs: shell reduction and it implications on defence and foraging. Frontiers in Zoology 2, 1Ð18. Wägele, H., Vonnemann, V. & Rudman, W.B. 2006. Umbraculum umbraculum (Lightfoot, 1786) (Gastropoda, Opisthobranchia, Tylodinoidea) and the synonymy of U. mediterraneum (Lamarck, 1812). Records of the Western Australian Museum, Supplement 69. Wägele H, Vonnemann, V. & Wägele, J.W. 2003. Toward a phylogeny of the Opisthobranchia. In Molecular Systematics and Phylogeography of Mollusks, C. Lydeard & D. Lindberg (eds). Washington and London: Smithsonian Institution Press, 185Ð228. Wägele, H. & Willan, R.C. 2000. Phylogeny of the Nudibranchia. Zoological Journal of the Linnean Society 130, 83Ð181. Walker, R.P. 1982. The chemical ecology of some sponges and nudibranchs from San Diego. Dissertation Abstracts International B42, 3698. Weiss, K. & Wägele, H. 1998. On the morphology, anatomy and histology of three Onchidella-species (Gastropoda, Gymnomorpha, Onchidiida). Archiv für Molluskenkunde 127, 69Ð91. Whiters, N.W., Kokke, W.C.M.C., Fenical, W. & Djerassi, C. 1982. Sterol patterns of cultured zooxanthellae isolated from marine invertebrates: synthesis of gorgosterol and 23-desmethylgorgosterol by aposym- biotic algae. Proceedings of the National Academy of Sciences of the United States of America 79, 3764Ð3768. Willan, R.C. 1979. PhD Thesis. University of Auckland, New Zealand. (As reported in Carefoot, 1987). Willan, R.C. 1987. Phylogenetic systematics of the Notaspidea (Opisthobranchia) with reappraisal of families and genera. American Malacological Bulletin 5, 215Ð241. Wise, J.B. 1996. Morphology and phylogenetic relationship of certain pyramidellid taxa (Heterobranchia). Malacologia 37, 443Ð551.

275 7044_book.fm Page 276 Friday, April 14, 2006 1:28 PM

HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA

Wollscheid-Lengeling, E., Boore, J., Brown, W. & Wägele, H. 2001. The phylogeny of Nudibranchia (Opistho- branchia, Gastropoda, Mollusca) reconstructed by three molecular markers. Organisms Diversity and Evolution 1, 241Ð256. Wright, A.D. 2003. GC-MS and NMR analysis of Phyllidiella pustulosa and one of its dietary sources, the sponge Phakellia carduus. Comparative Biochemistry and Physiology 134A, 307Ð313. Yamada, K. & Kigoshi, H. 1997. Bioactive compounds from the sea hares of two genera Aplysia and Dolabella. Bulletin of the Chemical Society of Japan 70, 1479Ð1489. Yonow, N. 1992. Observations on the diet of Philinopsis cyanea (Martens) (Cephalaspidea: Aglajidae). Journal of Conchology 34, 199Ð204. Yoshida, W.Y., Bryan, P.J., Baker, B.J. & McClintock, J.B. 1995. Pteroenone: a defensive metabolite of the abducted Antarctic pteropod Clione antarctica. Journal of Organic Chemistry 60, 780Ð782. Young, C.M., Greenwood, P.G. & Powell, C.J. 1986. The ecological role of defensive secretions in the intertidal pulmonate Onchidella borealis. Biological Bulletin (Woods Hole) 171, 391Ð404. Zubía, E., Gavagnin, M., Crispino, A., Martínez, E., Ortea, J. & Cimino, G. 1993. Diasteroisomeric ichthyo- toxic acylglycerols from the dorsum of two geographically distinct populations of Archidoris nudi- branchs. Experientia 49, 268Ð271.

Electronic references

www.hku.hk/ecology/porcupine/por28/28-glance-siphonaria.htm#index2 (accessed 24 June 2005, food of Siphonaria). www.seanature.co.uk/marine-education/onchidella.htm (accessed 24 June 2005, food of Onchidella)

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Oceanography and Marine Biology: An Annual Review, 2006, 44, 277-322 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis

TAXONOMY, ECOLOGY AND BEHAVIOUR OF THE CIRRATE OCTOPODS

MARTIN A. COLLINS1 & ROGER VILLANUEVA2 1British Antarctic Survey, Natural Environmental Research Council, High Cross, Madingley Road, Cambridge, CB3 0ET, U.K. E-mail: [email protected] 2Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC), Passeig Marítim de la Barceloneta 37-49, E-08003 Barcelona, Spain E-mail: [email protected]

Abstract The cirrate octopods are deep-sea, cold-adapted cephalopod molluscs that are found throughout the world’s oceans, usually at depths in excess of 300 m, but shallower in cold water at high latitudes. The gelatinous bodies of the cirrates, which deform when preserved, coupled with low capture rates have caused considerable confusion in the systematics of the group. The taxo- nomically relevant morphological features are briefly reviewed and the taxonomy revised. On the basis of morphological and molecular information the cirrates are divided into four families, the Cirroteuthidae (including the genera Cirroteuthis, Cirrothauma and Stauroteuthis), Cirroctopodidae (Cirroctopus), Grimpoteuthidae (Cryptoteuthis, Grimpoteuthis and Luteuthis) and Opisthoteuthidae (Opisthoteuthis). A total of 45 species are recognised. The opisthoteuthids are primarily benthic animals, the grimpoteuthids and cirroctopodids benthopelagic and the cirroteuthids essentially pelagic, but generally close to the sea floor. With the exception of two common, shallow, Opistho- teuthis species, the biology of the cirrates is poorly studied. The data on reproductive biology indicate that spawning is extended, with growth continuing during a reproductive period that probably occupies much of the life cycle, an unusual strategy in cephalopods. Diet studies suggest that benthic cirrates feed on small-sized organisms with low swimming speeds and the main prey are amphipods and polychaetes. Cirrate predators include sharks, teleost fishes, fur seals and sperm whales. Behav- ioural observations, based on underwater photographs, submersible observations and aquarium studies, show a range of postures, modes of locomotion and responses to disturbance that differ between the families. Behavioural observations also help interpret the unusual morphology and physiology of the cirrates, such as the use of cirri, fins, secondary web and bioluminescent emissions.

Introduction The cirrate octopods are deep-sea cephalopod molluscs, possessing a semigelatinous body, paired fins, well-developed web, a large internal shell and paired cirri between a single row of suckers. The morphology of the cirrates indicates that the group are relatively primitive, with similarities to ancestral octopods (Young et al. 1998). However, molecular studies of cephalopod evolution have produced mixed results, with no clear monophyly in the Octopoda (incirrates and cirrates) and the suggestion of polyphyly in the cirrates (Carlini et al. 2001, Lindgren et al. 2004). The cirrates are known from all oceans, typically at depths of 300Ð7000 m, but are found shallower in cold waters at high latitudes (Voss 1967, 1988a) and include some of the largest

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invertebrates in the deep sea. They are usually caught in small numbers, are extremely fragile and easily damaged on capture, and often distort during preservation. Many of the early descriptions of species, genera and families were based on small numbers (often one) of badly damaged and poorly preserved specimens (e.g., Cirroteuthis muelleri (Eschricht 1836), Cirrothauma magna (Hoyle 1885), Grimpoteuthis umbellata (Fischer 1883), Opisthoteuthis massyae (Grimpe 1920)). These factors have led to considerable confusion in the taxonomy of the group, with debate about which characters should be used to separate genera and families and consequently the classification of the cirrates has been in an almost constant state of flux, with species being moved between genera and genera between families (e.g., Robson 1930, Nesis 1987, Voss 1988a, Sweeney & Roper 1998). Studies of the morphology of the cirrates have, with a small number of exceptions (Meyer 1906, Ebersbach 1915, Robson 1932, Aldred et al. 1983), been limited to brief taxonomic descrip- tions and some of the early detailed studies have been confounded by confusion over the definition of structures and of the species being examined. The development of new technology, allowing access to the deep sea (e.g.. Roper & Brundage 1972, Villanueva et al. 1997) and the extension of commercial fishing into deeper water (Boyle et al. 1998), has stimulated renewed interest in this enigmatic group in the last 20 yr. Much of the recent work has focused on taxonomy and distribution (e.g., O’Shea 1999, Collins et al. 2001a, Villanueva et al. 2002, Collins 2003), ecology of the relatively shallow species (e.g., Villanueva & Guerra 1991, Boyle & Daly 2000) and in situ behavioural observations from submersibles (Vec- chione & Young 1997, Villanueva et al. 1997, Johnsen et al. 1999a,b). Correct identification is important to all studies, but taxonomic work has been handicapped by the poor state of type specimens, rather confused literature and problems with definitions of anatomical structures. Ecological studies of the cirrates have, largely through lack of specimens, been limited to shallow species of the Opisthoteuthis genus, which have been caught as by-catch of commercial fisheries (Cupka 1970, Vecchione 1987, Villanueva & Guerra 1991, Villanueva 1992a, Boyle et al. 1998, Laptikhovsky 1999, Daly et al. 1998, Boyle & Daly 2000), but little or no ecological work has been undertaken on the deeper species. The existing data indicate important differences in reproduction between the cirrate and incirrate octopods, notably in lack of seasonality associated with spawning and the continuous production of eggs and spermatophores in adult individuals of the species studied to date. During recent years in situ and aquaria observations of live cirrates have dramatically changed our understanding of how these animals use their fins and web to swim and respond to external disturbance (e.g., Boletzky et al. 1992, Vecchione & Young 1997, Villanueva et al. 1997, Villanueva 2000). These behavioural observations have been indispensable in interpreting the morphological characteristics of the cirrates, such as the delicate secondary web and the bioluminescent capabilities (Johnsen et al. 1999a,b), and suggest that future observations on live specimens will produce new findings and help explain the function of other unusual morphological features such as the areolar spots and mantle ‘windows’. Here the taxonomy of the group is reviewed and updated and the limited data on ecology and behaviour summarised. To underpin the taxonomic review, the first section briefly compares the anatomy of the different genera and families.

Comparative anatomy This section is intended to provide the reader with details of the comparative anatomy of the cirrates to facilitate identification and taxonomic descriptions. For a detailed study of the anatomy of a cirrate (Cirrothauma murrayi) the reader is referred to Aldred et al. (1983). The cirrates are essentially deep-water forms, and exhibit a number of characteristics that are considered modifications to deep-sea life (reduction or loss of radula and posterior salivary glands;

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loss of ink sac; reduction of gills; narrowing of funnel aperture; large eggs), which are shared by deep incirrate species (Robson 1925, Voss 1988b). The gelatinous nature and few hard parts of the cirrates mean that preservation can dramatically change the form of the animal, and this has been clearly demonstrated with whole animals (e.g., Luteuthis shuishi (O’Shea & Lu 2002) and Cryptoteuthis brevibracchiata (Collins 2004) where comparisons of fresh and preserved specimens are illustrated). Different preservatives will cause different types of distortion, with considerable shrinkage of Cirro- teuthis, Cirrothauma and Stauroteuthis in alcohol. Freezing may also cause distortion, notably to the internal shell (Collins 2003) and possibly spermatophores (Villanueva et al. 2002). Guidelines for dealing with captured specimens were produced at a workshop in 2000 (Vecchione & Collins 2002).

External Externally the cirrates are characterised by the possession of lateral to terminal fins and paired cirri, which are interspersed between a single row of suckers that are highly variable in form. The body is semigelatinous and varies from an extended bell-shape with long arms (Cirroteuthidae) through bell-shaped forms with moderate arms (Grimpoteuthidae) to the ovoid shaped Opistho- teuthis (Figure 1 and Figure 2). Fin size varies from large in Cirroctopus, Cirroteuthis and Cirrothauma through moderate (Grimpoteuthis, Luteuthis and Stauroteuthis) to small (Cryptoteuthis and Opisthoteuthis). The fins are generally larger in juvenile cirrates than in adults (Figure 2G).

Figure 1 Ventral view of basic body form in the cirrate octopods. (A) Cirroteuthis muelleri, (B) Cirrothauma murrayi, (C) Stauroteuthis syrtensis, (D) Grimpoteuthis discoveryi, (E) Opisthoteuthis massyae, (F) Cirroc- topus glacialis. Sources (with permission where required): (A, B, F) Collins unpublished; (C) from Collins & Henriques (2000); (D) from Collins (2003); (E) from Villanueva et al. (2002). Scale bars = 100 mm.

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Figure 2 (See also Colour Figure 2 in the insert following page 276.) Photographs of cirrate octopods. (A) dorsal view of Opisthoteuthis massyae (fresh specimen), (B) ventral view of Cryptoteuthis brevibracchiata (fresh specimen), (C) dorso-posterior view of Cirroctopus glacialis (fresh specimen), (D) ventral view of Grimpoteuthis discoveryi (formalin-preserved specimen), (E) ventral view of Cirrothauma murrayi (fresh specimen), (F) oral view of male Stauroteuthis syrtensis (formalin-preserved specimen), (G) Juvenile specimen of Opisthoteuthis calypso, note the relatively large fins and funnel in comparison with the adult Opisthoteuthis in (A). Sources (with permission where required): (A) Collins unpublished; (B) from Collins (2004); (C) Mike Vecchione unpublished; (D) from Collins (2003); (E) from Aldred et al. (1983); (F) from Collins & Henriques (2000); (G) L. Dantart. Scale bars: (AÐF) = 100 mm; (G) = 10 mm.

The cirrates lack the innervated chromatophores that are found in shallow-water cephalopods (Aldred et al. 1983, Nesis 1987), and are therefore not capable of colour change. In most species the skin is pigmented and is an orange/red/purple colour in fresh specimens of Opisthoteuthis,

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Grimpoteuthis, Luteuthis, Cryptoteuthis and Cirroctopus. In the Cirroteuthidae the oral surface of the arms is usually deep purple in colour, with the rest of the body pale or unpigmented, although in situ photographs do show cirroteuthids with purple, red and/or brown colour in both oral and dorsal surfaces. Although much of the external tissue of Stauroteuthis is translucent, the internal organs are surrounded by a pigmented membrane, which has a ‘window’ of unknown function in the area of the accessory glands in males and oviducal glands in females (Collins & Henriques 2000). In Cirrothauma murrayi the pigmentation occurs in two layers: an outer layer that contains many small granules and an inner layer containing spherical clusters of pigment granules (Aldred et al. 1983). Pigment-free (areolar) spots are seen on some species of Opisthoteuthis and Cirroctopus (Vecchione et al. 1998, Villanueva et al. 2002), and Vecchione et al. (1998) speculated that the pigment-free spots in Cirroctopus glacialis gather and channel light. The arms vary in length from short to moderate in Opisthoteuthis and Cryptoteuthis, moderate in Grimpoteuthis, Luteuthis and Cirroctopus and long in Cirroteuthis, Stauroteuthis and Cirrothauma. In many species the arms are of approximately the same length, and if there are differences, it is usually the dorsal arms that are the longest. In at least two species of Opisthoteuthis (O. massyae and O. hardyi) the dorsal arms of the mature males are considerably thicker than the other arms (see Villanueva et al. 2002). The function of the thickened arms is not known. The cirrates do not possess a hectocotylus (the modified arm of male incirrate octopods, used to transfer spermatophores to the female). In all cirrates the arms are connected by a deep web, which occurs in two forms. In Opistho- teuthidae, Grimpoteuthidae and Cirroctopodidae the arms are directly connected to the web (Figure 3B), whilst in Cirroteuthidae each arm is independent of the primary web and is connected to it by a single, delicate vertical membrane (the intermediate or secondary web) that is attached along the dorsum of the arm (Figure 3A; see Vecchione & Young 1997). The secondary web of the Cirroteuthidae may allow greater flexing in the web, and therefore greater locomotory capacity (see section on behaviour, p. 310). The web is particularly thin and delicate in the Cirroteuthidae, but thicker and tougher in the other families. In Cirroteuthis muelleri and many Grimpoteuthis species (Voss & Pearcy 1990, Collins 2003) the web is supported by a single fleshy nodule at the

Figure 3 Cross section of the arm and web of (A) Stauroteuthis syrtensis and (B) Cirroctopus glacialis contrasting the complex web (secondary web) of S. syrtensis with the simple web form of C. glacialis. From Vecchione & Young (1997). With permission.

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web margin on the ventral side of each arm (see Figure 4E). Opisthoteuthis species lack these single fleshy nodules, but instead the web is supported, in some species at least, by multiple, thin, web supports also placed at the web margin (Figure 4D). In Cirrothauma murrayi the web extends right to the arm tips (Aldred et al. 1983). The arms carry a single row of suckers of highly variable form (Figure 4), with distinct sexual dimorphism in many species. In Opisthoteuthis the suckers are embedded in the arms, with two distinct enlarged fields in mature males, the proximal enlarged field typically occupies suckers 3Ð8, whilst the location, number and degree of enlargement of the distal field is generally species specific, with gross enlargement in some species (e.g., O. calypso, see Villanueva et al. 2002). In females the suckers increase gradually in size to a single maximum. In Grimpoteuthis and Cirroctopus the suckers increase to reach a single maximum, somewhere between sucker 8 and the web margin. In many Grimpoteuthis species the suckers also show sexual dimorphism, with suckers larger in males than females but in G. tuftsi and G. challengeri there is no apparent sexual dimorphism. In mature specimens of Grimpoteuthidae and Opisthoteuthidae total sucker counts vary between 50 and 120 suckers. Sucker form is either barrel-shaped or cylindrical in Grimpoteuthis and distinctly barrel-shaped in Opisthoteuthis and Cirroctopus. The suckers of Opisthoteuthis have a distinct peduncle, with the infundibulum composed of radially arranged cushions similar to incirrate octopods (Villanueva & Guerra 1991) (Figure 5A,B) and the suckers of the other Opisthoteuthidae and Grimpoteuthidae appear similar in basic structure. The suckers of the Cirroteuthidae are highly modified. In Stauroteuthis syrtensis the suckers are highly sexually dimorphic, with very small suckers in the females (maximum sucker diameter (MSD) = 2.2 mm), but considerably larger in the males (MSD = 6.5 mm; Collins & Henriques 2000) (Figure 5E). In both sexes the first 5–6 (oral) suckers are close together, then 7Ð23 are spaced out, with maximum intersucker distance between suckers 13 and 14, with the distal suckers small and closely packed (Figure 4GÐI). From behavioural, anatomical and ultrastructural examination, Johnsen et al. (1999a,b) considered the suckers of S. syrtensis to be photophores, not true octopodan suckers. These suckerlike photophores have the capability for bioluminescent emission, but it is not clear if the suckers of both males and females produce light (Collins & Henriques 2000). These findings suggest that careful observations of living material and ultrastructural examination may be useful in other species of cirrates. The function of the light could be to attract either food or mates. In S. gilchristi there is no dimorphism in sucker form, and the bioluminescent capability is not known. In Cirrothauma murrayi the first 5–6 (oral) suckers are small, rounded and closely packed, and somewhat similar to the oral suckers of Stauroteuthis, but the remaining suckers are borne on long, conspicuous, fleshy peduncles (see Figures 4J,K; 5D,E; Aldred et al. 1983). The oral suckers have a small orifice in the infundibulum, but lack a suction chamber. There is no orifice in the distal suckers, with the infundibulum resembling a small cap (Figure 5C,D). It has been suggested that there is a possible light organ at the base of the fleshy peducle of the distal suckers (Chun 1913; Aldred et al. 1982, 1983), but this has not been confirmed (Aldred et al. 1984). In Cirroteuthis muelleri the oral suckers (1Ð8) are the largest and are tightly packed, cup-shaped and raised on broad heavy pads (Voss & Pearcy 1990). The distal suckers appear nonfunctional (as adhesive suckers) and are raised on fluid filled peduncles, similar in form to those of Cirrothauma murrayi, but they stop at the web margin (Voss & Pearcy 1990). Three types of suckers are found on the arms of Cirrothauma magna (Guerra et al. 1998): the oral suckers are small, closely packed and cylindrical, mounted on a stout stalk; mid-arm suckers have a long stalk and an inflatable acetabulum chamber; distal suckers are bowl-like with a rigid muscular base. The cirri are thought to have a sensory function (Aldred et al. 1983) and vary in length, arrangement and internal structure between genera. In the Cirroteuthidae the cirri are extremely long, particularly on the midsection of the arms (approximately 50% of mantle length (ML) in

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CIRRATE OCTOPODS (M) arm, Cryptoteuthis brevibracchiata: Cryptoteuthis brevibracchiata: : (G) arm, (H, I) male suckers and cirri from : (G) arm, (H, I) male suckers (L) arm. : (A) arm, (B) enlarged male suckers and cirri, (C) female male suckers : (A) arm, (B) enlarged Stauroteuthis syrtensis Stauroteuthis Cirroctopus glacialis: Cirroctopus Opisthoteuthis agassizii Villanueva et al. 2002; (EÐF) from Collins 2003; (G) from Collins & Henriques al. 2002; (EÐF) from Collins 2003; (G) et Villanueva : (E) arm, (F) suckers and cirri. : (E) arm, (F) suckers : (J) arm, (K) suckers and cirri. : (J) arm, (K) suckers Grimpoteuthis boylei Cirrothauma murrayi Cirrothauma Illustrations of the arms, suckers and cirri form in the cirrate octopods. Illustrations of the arms, suckers suckers and cirri, (D) web supports. suckers (H) oral and (I) mid-arm sections. (H) Figure 4 Figure (N) suckers and cirri. Sources (with permission where required): (AÐD) from (N) suckers scale bars = 10 mm. 2000; (HÐL) Collins, unpublished; (M-N) from Collins 2004. Unmarked

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Figure 5 Detail of suckers and cirri. (A, B) Scanning electron micrographs of suckers of Opisthoteuthis calypso (sp, sucker peduncle; inf, sucker infundibulum), (C) Section of mid-arm sucker of male Stauroteuthis syrtensis, (D) Scanning electron micrograph of Cirrothauma murrayi sucker, (E) Sagital section of stalked sucker of Cirrothauma murrayi, (F) Scanning electron micrograph of cirrus of Opisthoteuthis calypso, (G) longitudinal section of Cirrothauma murrayi cirrus (sep = septum). Sources (with permission where required): (A, B, F) from Villanueva & Guerra (1991); (C) Collins unpublished; (E, D, G) from Aldred et al. (1983). Scale bars: (A, B, C, E, F, G) = 0.5 mm; (D) = 2 mm.

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Stauroteuthis; Collins & Henriques 2000). In Stauroteuthis, Cirroteuthis and Cirrothauma magna the cirri are absent from the distal parts of the arms, stopping at the web margin. In Cirrothauma murrayi, both the web and cirri extend to the distal ends of the arms. In the other families the cirri continue to the arm tips and are of moderate length in the Grimpoteuthidae but typically short and stubby in Opisthoteuthidae and Cirroctopus. Cirri are usually absent between some of the oral suckers, but the location of the first (oral) cirrus varies between species. In Cirrothauma murrayi the long cirri are divided internally by transverse septa (Figure 5G; Aldred et al. 1983), but these septa were not seen in the shorter cirri of Opisthoteuthis massyae (Villanueva & Guerra 1991). In O. massyae, the cirri are composed of sensory tissue surrounded by muscle (Villanueva & Guerra 1991), similar in structure to O. depressa (Meyer 1906). Hochberg et al. (1992) reported that cirri are absent in early juvenile forms of some Opisthoteuthis sp., however juvenile Opisthoteuthis calypso have well-developed cirri, that are relatively longer (in relation to sucker diameter) than adults (Villanueva unpublished). Early juveniles of Cirrothauma murrayi also possess well-developed cirri (Aldred et al. 1983). The funnel form is variable, being extremely long in Cirrothauma, but relatively short in the other genera. The mantle aperture is reduced, probably associated with the reduction or lack of jet propulsion. In Stauroteuthis it is extremely reduced, such that on preservation it appears as a small pore in the mantle, with the funnel often contracted inside. The funnel organ, which is a useful taxonomic character in the incirrate octopods, is rather indistinct in the cirrates, but in those species for which it has been described, it is an inverted V-shape (e.g., Berry 1918, Voss & Pearcy 1990, Collins 2003). The eyes are large in all but Cirrothauma, which has greatly reduced eyes that lack an iris and lens (see Aldred et al. 1983). Rounded, prominent olfactory organs are found within the mantle aperture and either side of the funnel in all cirrate species. They are served by a complex nerve net, but their supposed chemosensory function has not been established.

Internal The arrangement of organs in the mantle cavity is similar in all cirrates (Figure 6), but the structure of the gills and the digestive system is variable. The gills of the cirrates are of two basic forms, the sepioid form is found in the Cirroteuthidae and the half-orange or modified half-orange form in the other families (Figure 6). The gills are divided into a series of lamellae, which in the sepioid form are arranged linearly, whist in the half-orange form they are grouped like segments of an orange. Opisthoteuthidae, Grimpoteuthidae and Cirroctopus and have the half-orange form, but the number and form of the lamellae varies between species. In Grimpoteuthis, G. challengeri and G. tuftsi possess very fine lamellae and small gills, but the other species have broad lamellae and larger gills. Associated with each gill is a branchial heart, which leads to the systemic heart. A detailed description of the circulatory system of Stauroteuthis syrtensis and Grimpoteuthis is given by Ebersbach (1915), and Aldred et al. (1983) describe interspecific differences in the structure of the cirrate heart. The internal shell is distinct in each of the genera (Figure 7; see Bizikov 2004 for detail of the form and evolution of the shell). The vacuolated cartilage of the shell becomes distorted during freezing, so caution should be exercised when examining frozen material. In Cirroteuthis muelleri the shell is saddle-shaped, with large ‘wings’ associated with the large fin muscles. Cirrothauma magna and C. murrayi possess a butterfly-shaped shell, a character that unites these species in Cirrothauma (see O’Shea 1999). In Stauroteuthis the shell is a simple U-shape. The shell of Cirroctopus is V-shaped, whilst those of Grimpoteuthis, Opisthoteuthis and Cryptoteuthis are U-shaped. The shells of Opisthoteuthis and Cirroctopus have lateral walls that taper to fine points, whilst those of Grimpoteuthis and Cryptoteuthis either end bluntly or in two lobes. Luteuthis has

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Figure 6 Internal anatomy of (A) female Grimpoteuthis wuelkeri and (B) male Stauroteuthis syrtensis illus- trating the gill form and location of internal organs. Sources (with permission where required): (A) from Collins (2003); (B) Collins unpublished. Scale bars = 25 mm.

a distinctly W-shaped shell. The shell is tightly bound in the shell sac, to which the fins adhere. The fins, which contain the most robust muscle in the cirrate octopods (Vecchione & Young 1997), are divided into distinct proximal and distal regions (Figure 8). The proximal region has a central cartilaginous core, which is covered by thick bundles of muscle fibres, parallel to the fin axis, that insert on the shell sac or on the cartilaginous core. The distal region lacks the cartilaginous core of the proximal region, consisting of two layers of thin muscles that are oriented transversely to the fin plane. The digestive system is similar in all the cirrates (Figure 9) consisting of buccal mass and beaks, radula (in some species), anterior and posterior (reduced or absent) salivary glands, oesoph- agus, stomach, caecum, digestive gland and intestine. The beak form varies between the genera (Figure 10), with Stauroteuthis possessing a particularly distinct beak, although insufficient material has been examined to distinguish interspecific variability. A radula is only found in some species of Grimpoteuthis (Figure 11) and in Luteuthis, but in a highly reduced monodont form (Voss & Pearcy 1990, O’Shea 1999, Collins 2003). Anterior salivary glands are present in all species, but posterior salivary glands are only reported in two species of Grimpoteuthis, where they are small (Collins 2003). Aldred et al. (1983) did report a single posterior salivary gland in Cirrothauma, but the location of the single gland is different to Grimpoteuthis and incirrate octopods and is possibly not an analagous structure. The oesophagus, stomach and intestine are a deeply pigmented purple colour that may be associated with the consumption of bioluminescent prey (Vecchione & Young 1997). A swelling of the oesophagus (crop?) has been reported for some species, but is rather indistinct. The stomach, which lies in a groove in the digestive gland, is lined with a thick cuticle and leads, via a narrow duct, to the caecum, which typically has a single turn and is connected to the digestive gland by two digestive ducts. The digestive gland consists of a single lobe in most species but is bilobed (two discrete lobes) in some Opisthoteuthis species and in Luteuthis. The intestine is straight (uncoiled) in Cirroteuthis, Stauroteuthis and Cirrothauma but slightly coiled in the other genera. The basic form of the nervous system is similar for all the cirrates and is described in detail for Cirrothauma murrayi by Aldred et al. (1983). A major difference between the cirrates and incirrates is the form of the central ganglia, which in cirrates consist of two rings surrounding the

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Figure 7 Shell form in the cirrate octopods. (A) Cirrothauma murrayi, (B) Cirroteuthis muelleri, (C) Stau- roteuthis syrtensis, (D) Cirroctopus glacialis, (E) Grimpoteuthis discoveryi, (F) Opisthoteuthis agassizii, (G) Cryptoteuthis brevibracchiata. Sources (with permission where required): (A, B, C, D) Collins, unpub- lished; (E) from Collins 2003; (F) from Villanueva et al. 2002; (G) from Collins 2004. Scale bars = 10 mm.

oesophagus (Figure 12), somewhat similar to that of Nautilus (Aldred et al. 1983). The eyes are directed laterally with long optic nerves passing through a large ‘white body’, which varies in colour between species. The form of the optic nerve is an important taxonomic character: in the Cirroteuthidae and Grimpoteuthidae the optic nerve passes through the white body as a single bundle of fibres (Figure 13), whilst in Opisthoteuthidae there are two to four bundles of nerve fibres and in Cirroctopodidae there are eight or nine bundles. The form of the stellate ganglion and epistellar body has also been used as a taxonomic character (e.g.. Robson 1932, Voss & Pearcy 1990) and the epistellar body is particularly well developed in the cirrates (Aldred et al. 1983), although its function is not known.

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Figure 8 The structure of the shell, fin cartilage and fin muscles of (A, B) Cirroctopus glacialis and (C, D) Stauroteuthis syrtenis. (B) and (D) are schematic sections through the long axis of the fins. Modified from Vecchione & Young (1997). With permission.

Figure 9 Digestive system of (A) Opisthoteuthis massyae, (B) Grimpoteuthis wuelkeri (with detail of posterior salivary glands) and (C) Stauroteuthis syrtensis. Sources (with permission where required): (A) from Villanueva et al. (2002); (B) from Collins (2003); (C) from Collins & Henriques (2000). Scale bars = 10 mm.

The female reproductive system is similar in all the cirrates consisting of ovary, thin-walled proximal oviduct (left only), oviducal gland and a fleshy distal oviduct (Figures 14, 15; see Boyle & Daly 2000, Villanueva 1992a). For all species studied the ovaries contain a wide range of egg sizes and developmental stages (see section on reproduction, p. 302). The oviducal gland consists of two sections, both striated, but differing distinctly in colour. The proximal section, which is usually lighter in colour functions as a spermatheca (Aldred et al. 1983) and is the presumed location of fertilisation, whilst the distal section is responsible for providing the tough egg case. The male reproductive system is more variable, consisting of testes, seminal vesicle, accessory gland(s) and terminal organ (or penis) (Figure 14). The testis is located posteriorly in the mantle cavity, and leads via the vas deferens to the seminal vesicle, which passes through the accessory gland(s) to the terminal organ. The number and size of the accessory glands vary between genera and species. In the Cirroteuthidae there is a single accessory gland (Aldred et al. 1983, Voss & Pearcy 1990, Collins & Henriques 2000), whilst in Opisthoteuthis, Cirroctopus and Grimpoteuthis there are multiple accessory glands (Voss & Pearcy 1990, O’Shea 1999, Villanueva et al. 2002, Collins 2003). In mature males the spermatophores (‘sperm packets’) are unlike those of incirrate

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Figure 10 Lower and upper beaks of (A) Opisthoteuthis agassizii, (B) Grimpoteuthis wuelkeri, (C) Stauro- teuthis syrtensis and (D) Cirrothauma magna. Sources (with permission where required): (A) from Villanueva et al. (2002); (B) from Collins (2003); (C) from Collins & Henriques (2000); (D) Collins unpublished. Scale bars = 5 mm.

Figure 11 Scanning electron micrographs of the radula of Grimpoteuthis wuelkeri. Modified from Collins (2003). With permission. Scale bars = 1 mm.

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Figure 12 Eye, central nervous system and statocyst of Cirrothauma murrayi. Modified from Aldred et al. (1983). With permission.

Figure 13 Optic nerve configuration in the cirrate octopods. (A) Opisthoteuthis, (B) Grimpoteuthis, (C) Stauroteuthis, (D) Cirroctopus. Sources (with permission where required): (A) from Villanueva et al. (2002); (B) from Collins (2003); (C) from Collins & Henriques (2000); (D) Collins unpublished. Scale bars = 10 mm.

octopods, being ovoid in shape (approximately 2Ð3 × 1Ð1.5 mm) embedded in gelatinous material (in preserved specimens) and located in the seminal vesicle and terminal organ. The spermatophores of Opisthoteuthis hardyi appear disc-shaped (Villanueva et al. 2002), but this may be a consequence of distortion due to freezing prior to fixation. Detailed examination of the spermatophores of

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Figure 14 Reproductive system of cirrate octopods. (A) Female reproductive system of Grimpoteuthis boylei, male reproductive system of (B) Grimpoteuthis boylei and (C) Stauroteuthis syrtensis. Sources (with permis- sion): (A, B) from Collins (2003); (C) from Collins & Henriques (2000). Scale bars = 20 mm.

Figure 15 (A) Section of ovary of Opisthoteuthis massyae, showing maturing eggs and convoluted follicular epithelium which secretes yolk into the lumen of the ovum, (B) dissected ovary of O. massyae showing distribution and size range of maturing eggs, (C) section of mature ovarian egg showing formed chorion and outer sheath layer, (D) general view of released eggs among remaining maturing eggs of various sizes. From Boyle & Daly (2000). With permission. Scale bars: (A, C, D) = 500 µm; (B) = 20 mm.

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Figure 16 (A) Diagram of a spermatophore from Opisthoteuthis calypso, (B) scanning electron micrograph of a spermatophore of O. massyae, (C) spermatozoa of O. calypso (left) and O. massyae, (D, E) scanning electron micrographs of the inside wall of the spermatophores of (D) Stauroteuthis syrtensis and (E) O. grimaldii showing the form of the spermatozoa. Sources (with permission where required): (A, C) from Villanueva 1992a; (B, E) Collins unpublished; (D) from Collins & Henriques 2000. Scale bars: (A, B) = 1 mm; (C, D, E) = 3 µm.

O. calypso (Figure 16A) shows them to possess pores at each end, which are covered with a hinged opercular structure (Villanueva 1992a), although these have not been found in other species (Figure 16B, Villanueva et al. 2002). The spermatophores function as a sperm reservoir, and sections through the spermatophores show aggregations of spermatozoids, with the heads oriented toward the walls and tails in the centre (Figure 16D,E; Aldred et al. 1983, Guerra et al. 1998, Collins & Henriques 2000). Healy (1993) compared mature spermatozoa from Opisthoteuthis persephone with those of Octopus and Vampyromorpha and found them to be similar to those of Octopus species, consisting of an elongate, solid acrosome; a straight, rodlike nucleus; a short midsection with a post mitochondrial

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skirt and a long flagellum. The form of sperm in Opisthoteuthis massyae (Villanueva 1992a), O. grimaldii and Stauroteuthis (Collins & Henriques 2000) is similar (Figure 16C,D,E), although Opisthoteuthis calypso has a broader, more oval nuclear section (Figure 16C; Villanueva 1992a).

Systematics In his review of the deep-sea octopods Voss (1988a) recognised 24 cirrate species in three families (Opisthoteuthidae, Stauroteuthidae and Cirroteuthidae), with 21 species in the Opisthoteuthidae. Recent work (Voss & Pearcy 1990, O’Shea 1999, Villanueva et al. 2002, Collins 2003) has increased the number of species considerably, with 45 species now recognised. Based on studies of the New Zealand fauna, O’Shea (1999) split the Opisthoteuthidae, adding the families Grimpoteuthidae and Luteuthidae. Recently, in a molecular study using sequences of the 16s gene, Piertney et al. (2003) suggested a division into four families, with Stauroteuthis, Cirroteuthis and Cirrothauma united in the Cirroteuthidae; Opisthoteuthis in the Opisthoteuthidae; Grimpoteuthis, Luteuthis and Enigma- titeuthis in the Grimpoteuthidae and a new family to include the genus Cirroctopus. The division into four families proposed by Piertney et al. (2003) is in general agreement with the morphological data and is followed here. Class Cephalopoda Cuvier, 1797 Order Octopoda Leach, 1818 Suborder Cirrata Grimpe, 1916 Family Cirroteuthidae Keferstein, 1866 Diagnosis Small-to-large cirrates, with extended bell-shaped body. Web complex, with secondary web linking arms to primary web. Digestive gland entire. Cirri long. Radula and posterior salivary glands absent. Gill form sepioid. Comments The family is represented by four genera (Table 1) and characterised by the possession of a secondary web (Figure 2) and extremely long cirri. Previous taxonomic organisations included Stauroteuthis in a separate family (Stauroteuthidae, Grimpe 1916), but a recent molecular study supports inclusion in the Cirroteuthidae (Piertney et al. 2003).

Genus Cirroteuthis Eschricht, 1836

Diagnosis Small-to-medium sized cirroteuthids, with large fins, saddle-shaped shell and long cirri. Cirri absent from distal section of arms. One recognised species. Type species Cirroteuthis muelleri (Eschricht 1836). Comments The genus previously included species that have since been moved to other genera or are considered nomen dubium (Table 1). Cirroteuthis muelleri was the first described cirrate (Eschricht 1836) and was redescribed by Voss & Pearcy (1990). It is benthopelagic and has a circum- Arctic distribution extending into the northern basins of the Pacific and Atlantic Oceans (Voss & Pearcy 1990, Nesis 2001, Collins et al. 2001a, Collins 2002). It occurs from near the surface in the high Arctic to 4500 m in the ocean basins, with distribution probably limited by temperature rather than depth. A specimen tentatively attributed to this species was caught off New Zealand but may represent a new species (O’Shea 1999). Cirroteuthis hoylei was described from a single specimen caught during the Challenger Expe- dition (Station 298) and was originally identified as C. magna by Hoyle (1885a). The specimen is small and badly damaged, but Robson (1932) considered that it represented a new species, which

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Table 1 Family Cirroteuthidae: distribution of recognised species

Species Distribution Comments References Cirroteuthis muelleri North Atlantic and North = Sciadophorus Reinhardt Eschricht 1836, Reinhardt & Eschricht, 1836 Pacific, possibly continuous & Prosch 1846 Prosch 1846, Voss & Pearcy through Arctic Ocean. Also 1990, O’Shea 1999, Collins reported from SW Pacific et al. 2001a, Collins 2002, Knudsen & Roeleveld 2002 Cirroteuthis hoylei SE Pacific 2225 fathoms Only known from type, Robson 1932, Guerra et al. nomen dubium (4070 m) (Robson 1932) which is small and 1998 damaged, but clearly a Cirroteuthis Cirrothauma magna Southern Indian Ocean; Only known from four Hoyle 1885a,b, Guerra et al. Hoyle, 1885 Atlantic Ocean specimens 1998, Collins et al. 2001b (1300Ð3351 m) Cirrothauma murrayi Worldwide at bathyal to Worldwide distribution Chun 1911, Aldred et al. Chun, 1911 abyssal depths requires critical review to 1983, Roper & Brundage determine differences 1972, Collins et al. 2001a Stauroteuthis gilchristi South Atlantic (900Ð2604 m) = Cirroteuthis gilchristi Robson 1924a, b, 1930, Robson, 1924 Collins & Henriques 2000, Collins et al. 2004 Stauroteuthis syrtensis North Atlantic at = Chunioteuthis Verrill 1879, Grimpe 1916, Verrill, 1879 1500Ð2500 m, shallower in ebersbachi Collins & Henriques 2000, Arctic waters Collins et al. 2001a Froekenia clara Equatorial Pacific (1015 m) Only known from type Hoyle 1904, Nesis 1986, nomen dubium (Hoyle 1904) specimen, which is now 1987, 1993, Voss 1988a, lost Guerra et al. 1998

he called Cirroteuthis (?) hoylei. The presence of a saddle-shaped shell indicates that it is a Cirroteuthis (Guerra et al. 1998), but it should be considered as Cirroteuthis sp. Cirroteuthis hoylei is thus nomen dubium.

Genus Cirrothauma Chun, 1911

Diagnosis Large-sized cirroteuthids with butterfly-shaped shell, large fins, extremely long cirri, distal suckers stalked and highly modified. Two species. Type species: Cirrothauma murrayi (Chun 1911). Comments The genus includes two recognised species, C. murrayi and C. magna (see Table 1). C. murrayi, which lacks lens and iris and has been called the ‘blind octopus’, appears to have a worldwide distribution, with specimens reported from the North Atlantic (Chun 1911, 1913, Aldred et al. 1983, Collins et al. 2001a), south Atlantic (Roper & Brundage 1972) and Pacific Oceans (see Aldred et al. 1983). However, geographic variability in these specimens has not been critically reviewed. Recent captures in the northeast Atlantic have been taken in bottom trawls at depths from 3900Ð4800 m (Aldred et al. 1983, Collins et al. 2001a), but other specimens (including the type) have been captured in midwater, usually over deep water. A specimen has also been captured with a dip net in the Arctic (Voss 1967). There are only four records of C. magna, from the Atlantic and Indian Oceans (Hoyle 1885a,b, Guerra et al. 1998, Collins et al. 2001b). This species grows to a large size and is probably the largest of the cirrates (Collins et al. 2001b). It was previously included in the genus Cirroteuthis, but the form of the shell, long arms and extremely large fins indicate it should be included in Cirrothauma (see O’Shea 1999).

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Genus Stauroteuthis Verrill, 1879

Diagnosis Large-sized cirroteuthids with moderate fins and U-shaped shell. Arms long with extremely long cirri on midsection. Cirri absent from distal section of arms. Two species. Type species: Stauroteuthis syrtensis (Verrill 1879). Comments The genus Stauroteuthis has previously been included in its own family (Stau- roreuthidae, Grimpe 1916), but has also been included in the Cirroteuthidae (see Nesis 1987). The presence of a secondary web suggests that it is closely related to Cirroteuthis and Cirrothauma, and molecular analysis also supports its inclusion in Cirroteuthidae (Piertney et al. 2003). The genus includes two species, Stauroteuthis syrtensis and S. gilchristi. S. syrtensis is distributed in the North Atlantic at depths of 200Ð3000 m (Verrill 1879, Grimpe 1916, Collins & Henriques 2000, Collins et al. 2001a, Collins 2002). Males and females are sexually dimorphic, notably in the form of the suckers, which was partly responsible for the confusion regarding Chunioteuthis ebersbachi (a junior synonym), which was originally described by Grimpe (1916) from a male specimen, whilst Stauroteuthis syrtensis was described by Verrill (1879) from a female. Johnsen et al. (1999a,b) demonstrated the bioluminescent capacity of the suckers. However, given the sexual dimorphism, it is not clear if both sexes are capable of producing light. It may be that the highly reduced suckers of the females produce light, perhaps to attract males. S. gilchristi is known from the type location, off the South African coast (Robson 1924a,b) and from the Atlantic sector of the Southern Ocean (Collins & Henriques 2000, Collins et al. 2004). It is morphologically similar to S. syrtensis, but there is no sexual dimorphism in the suckers. It is possible that the Southern Ocean specimens are different from the type material, but the poor condition of the two South African specimens prevented proper comparison (Collins & Henriques 2000).

Genus Froekenia Hoyle, 1904

Comments The genus was described from the single specimen of Froekenia clara caught at 555 fathoms (~1015 m) in the Pacific (Hoyle 1904). The species is unusual in, apparently, lacking a web between the arms. The type specimen has been lost (Sweeney & Roper 1998) and the species is considered nomen dubium (Voss 1988a). However, Nesis (1986, 1993) reported that new spec- imens, attributable to a new species of Froekenia, have been found at 500Ð810 m at the Error Seamount, Indian Ocean. To date the specimens have not been formally described and the status of the genus remains in doubt.

Family Opisthoteuthidae Verrill, 1896 Diagnosis Moderate-sized cirrates with small, subterminal fins. Shell a flaring U-shape, lateral walls tapering to fine points. Optic nerves pass through white body in two to four bundles. Two fields of enlarged suckers in mature males. Digestive gland entire or bilobed. Radula and posterior salivary glands absent. Web deep, single. Gills of ‘half-orange’ form. Single genus. Comments Includes the genus Opisthoteuthis. Various divisions of the cirrates have been proposed, with Grimpoteuthis included either in Opisthoteuthidae or Cirroteuthidae. O’Shea (1999) proposed a new family to accommodate Grimpoteuthis, but included Cirroctopus in the Opisthoteuthidae. However, recent molecular evidence (Piertney et al. 2003) indicates that Cirroctopus is sufficiently distinct from the other genera to warrant a separate family. Generally Opisthoteuthidae is the shallowest of the cirrate families, typically found at depths from 300Ð2200 m.

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Genus Opisthoteuthis Verrill, 1883

Diagnosis As family. Nineteen species. Type species Opisthoteuthis agassizii Verrill, 1883. Comments The 19 species occur throughout the world’s oceans (Table 2), with new species recently described from Atlantic and New Zealand waters. O. brunni is included in this genus rather than Grimpoteuthis (see Collins 2003). O’Shea (1999) separated the genus into three types based on the form of the digestive gland (bilobed or entire), shell, enlarged suckers and male accessory glands, but that organisation is not followed here. Six species are reported in the Atlantic, and the confusion surrounding the identification of these species has been addressed by Villanueva et al. (2002), with O. borealis subsequently described from the coast of Greenland (Collins 2005). O. agassizii is found only in the western Atlantic and reports of this species in the eastern Atlantic and Mediterranean are erroneous (e.g., Chun 1913; Bruun 1945; Adam 1962; Villanueva & Guerra 1991; Villanueva 1992a,b). O. massyae (= O. vossi, in part) was originally described as Cirroteuthis (Cirroteuthopsis) massyae by Grimpe (1920) from a single specimen caught off Ireland. It is a large species found at depths of 600Ð1500 m from the west coast of the British Isles to the Namibian coast in the southeast Atlantic. O. grimaldii has a similar geographic range to O. massyae, but appears to live slightly deeper (<2200 m) and may also occur in the northwest Atlantic (Villanueva et al. 2002). O. calypso is a small species, characterised by extreme enlargement in the distal sucker field in mature males, it is found in the eastern Atlantic from the coast of Namibia in the south to the southwest of Ireland in the north and in the Mediterranean. O. hardyi is only known from a single (male) specimen caught near South Georgia (~1000 m), but a female, probably attributable to this species has been taken off the Falkland Islands. Three species, O. phillipi, O. medusoides and O. extensa were described from the Indian Ocean (Table 2), but little is known about the distribution of any of them. Four species (O. albatrossi, O. californiana, O. depressa and O. japonica) are known from the North Pacific and their status is unclear. O. albatrossi was originally described (from south of the Aleutian Islands) as Stauro- teuthis (Sasaki 1920), and has recently been considered a Grimpoteuthis (Voss 1988a). Although the holotype (male) is in poor condition, it is clear from the original illustration that the body shape and pattern of greatly enlarged suckers at the web margin are characteristic of Opisthoteuthis. The sucker pattern of males is very similar to that of O. californiana, suggesting that an updated classification of the Opisthoteuthis in the North Pacific is needed. O. brunni is distributed in the east Pacific, off the central American coast (Voss 1982). O’Shea (1999) described three new species from New Zealand waters: O. mero occurs at depths of 360Ð1000 m around New Zealand; O. chathamensis is slightly deeper (900Ð1438 m) off the northeast coast of New Zealand with O. robsoni deeper again (1178Ð1723 m) off the east coast of the south island. In addition, O. persephone and O. pluto are described from the south of Australia.

Family Grimpoteuthidae O’Shea, 1999 Diagnosis Medium-to-large sized, bell-shaped cirrates with lateral fins. Web deep and simple. Shell U-shaped, with lateral walls parallel. Optic nerve passes though white body in single bundle. Radula reduced or absent. Posterior salivary glands reduced or absent. Cirri of short to moderate length. Gills of ‘half-orange’ form. Three genera: Grimpoteuthis, Cryptoteuthis and Luteuthis. Comments O’Shea (1999) split the Family Opisthoteuthidae and created two new families Grim- poteuthidae and Luteuthidae. O’Shea (1999) proposed that Grimpoteuthidae include Grimpoteuthis and a new genus Enigmatiteuthis. The family Luteuthidae was proposed to include a single species, Luteuthis dentatus (from a single specimen). However, whilst Grimpoteuthis is distinct from

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Table 2 Family Opisthoteuthidae: recognised species and distribution

Species Distribution Comments References Opisthoteuthis agassizii NW Atlantic (227Ð1935 m) Restricted to western Villanueva et al. 2002 Verrill, 1883 Atlantic, reports from E Atlantic are misidentifications. Opisthoteuthis Group 1 of O’Shea (1999) Opisthoteuthis albatrossi Off Japan, NW Pacific Four specimens; Sasaki 1920, 1929 (Sasaki, 1920) (486Ð1679 m) Opisthoteuthis Group 2 of O’Shea (1999) Opisthoteuthis borealis N Atlantic off Greenland Similar to O. grimaldii, but Collins 2005 Collins, 2005 (957Ð1321 m) digestive gland entire Opisthoteuthis brunni East Pacific off the coast of Originally described as a Voss 1982, Collins 2003 (Voss, 1982) Peru Grimpoteuthis Opisthoteuthis californiana North Pacific (320–620 m) Similar to O. albatrossi Berry 1949, Berry, 1949 Laptikhovsky 1999 Opisthoteuthis calypso NE Atlantic from SW Previously misidentified as Villanueva et al. 2002, Villanueva et al., 2002 Ireland to South Africa O. agassizii Villanueva 1992b and Mediterranean (365Ð2208 m) Opisthoteuthis chathamensis Off New Zealand Opisthoteuthis Group 2 of O’Shea 1999 O’Shea, 1999 (850Ð1500 m) O’Shea (1999) Opisthoteuthis depressa N Pacific, off Japanese coast Ijima & Ikeda 1895 Ijema & Ikeda, 1895 Opisthoteuthis extensa Indian Ocean, SW of Opisthoteuthis Group 1 of Thiele in Chun 1915 Thiele, 1915 Sumatra O’Shea (1999) Opisthoteuthis grimaldii NE Atlantic (1135Ð2287 m) Only known from male Joubin 1903, (Joubin, 1903) specimens, no confirmed Villanueva et al., 2002 females Opisthoteuthis hardyi Off South Georgia, Southern Single male specimen only Villanueva et al. 2002 Villanueva et al., 2002 Ocean (800Ð1100 m) Opisthoteuthis japonica Off Japan, West Pacific Two specimens; similar to Taki 1962, 1963 Taki, 1962 (152 m) O. albatrossi Opisthoteuthis massyae NE Atlantic, from Rockall = Cirroteuthopsis massyae Villanueva et al. 2002, (Grimpe, 1920) Trough to Namibia Grimpe 1920 Boyle et al. 1998, (778Ð1450 m) = Opisthoteuthis vossi Collins et al. 2001a Sanchez & Guerra 1989 Opisthoteuthis medusoides Off east African coast, Thiele in Chun 1915 Thiele, 1915 Indian Ocean (400 m) Opisthoteuthis mero Off New Zealand Opisthoteuthis Group 1 of O’Shea 1999 O’Shea, 1999 (360Ð1000 m) O’Shea (1999) Opisthoteuthis persephone Off South Australian coast Opisthoteuthis Group 1 of Berry 1918, Healy 1993 Berry, 1918 (270Ð540 m) O’Shea (1999) Opisthoteuthis phillipi Indian Ocean, off SW India Opisthoteuthis Group 1 of Oommen 1976 Oommen, 1976 O’Shea (1999) Opisthoteuthis pluto Off South Australian coast Opisthoteuthis Group 2 of Berry 1918 Berry, 1918 (270Ð810 m) O’Shea (1999) Opisthoteuthis robsoni Off east coast of New Four specimens only; O’Shea 1999 O’Shea, 1999 Zealand (1178Ð1723 m) Opisthoteuthis Group 3 of O’Shea (1999)

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Opisthoteuthis and there is molecular support for separating the two families, there is little support for the separation of Luteuthis from Grimpoteuthis at the familial level. Furthermore, the ‘true’ form of Grimpoteuthis remains unknown because the type species G. umbellata remains poorly described and is known only from the type, which is in extremely poor condition (see Collins 2003). Therefore, until new material is found from the type locality and G. umbellata is redescribed it is inappropriate to split Grimpoteuthis. For these reasons Luteuthis should remain in the family Grimpoteuthidae.

Genus Grimpoteuthis Robson, 1932

Diagnosis Small-to-large grimpoteuthids with medium-to-large lateral fins, each with a distinct lobe near the anterior fin insertion. Shell vestige U-shaped; lateral sides parallel, not tapered to fine points. Radula monodont or absent. Posterior salivary glands small or absent. Web supported by single fleshy nodules on the ventral side of the arms. Digestive gland entire (single lobe). Sucker sexual dimorphism present in some species, but with single enlarged field. Fourteen species. Type species: Grimpoteuthis umbellata (Fischer 1883). Comments The type species, G. umbellata, is known only from a single, badly damaged specimen caught near the Azores (2235 m) (see Collins 2003). It is possible that G. wuelkeri, G. plena or G. discoveryi are synonymous with G. umbellata, but this cannot be resolved until new material has been examined from the type locality. Of the seven Atlantic species (see Table 3), G. wuelkeri (Grimpe 1920) was described (as Stauroteuthis wuelkeri) from a single specimen caught off the Moroccan coast. It is found at depths of 1500Ð2100 m in the North Atlantic, and has recently been redescribed (Collins 2003). Piatkowski & Dieckmann (2005) reported a specimen of Grimpoteuthis wuelkeri from 5430 m in the Angola Basin, but this is considerably deeper than other records of this species and may be attributable to one of the deeper Grimpoteuthis species. G. boylei and G. challengeri are both large- sized abyssal species currently known from the northeast Atlantic, whilst G. discoveryi is a smaller species found throughout the North Atlantic (2600Ð4870 m). G. megaptera was described from five specimens from the northwest Atlantic. Of the five specimens that Verrill (1885) attributed to this species, four are now lost and the small damaged specimen is actually a Cirrothauma murrayi. Of the four lost specimens, three were caught at abyssal depths (4594Ð4708 m), with the fourth taken considerably shallower (1928 m) and, given what is known about the depth ranges of other Grimpoteuthis, it is unlikely that the shallow specimen is conspecific with the other three. The larger specimen (4708 m), which was illustrated by Verrill (1885; his Plate XLIII), is clearly a Grimpoteuthis, but new material is required from the type locality to redescribe G. megaptera. G. plena is known from a single, small and damaged specimen from the northwest Atlantic (1963 m). The poor condition of the G. plena type makes comparison difficult but it is somewhat similar to G. wuelkeri, which is found at equivalent depths in the North Atlantic. Seven species are known from the Indo-Pacific region (Table 3), but three of them, G. pacifica, G. meangensis and G. hippocrepium, were described from single specimens caught in the late nineteenth and early twentieth centuries and only in G. meangensis (one additional specimen) has new material been found. G. tuftsi and G. bathynectes were described from the northeast Pacific by Voss & Pearcy (1990). G. tuftsi was described from seven specimens caught on the Tufts Abyssal Plain at 3585Ð3900 m and is similar to the Atlantic abyssal species, G. challengeri, in possessing a (reduced) radula, fine lamellae on the gills, long cirri and with MSD at the web margin. The two species (G. tuftsi and G. challengeri) are clearly closely related. G. bathynectes was described from thirteen specimens caught on both the Tufts and Cascadia Abyssal Plains. G. abyssicola is only known from a single specimen caught between Australia and New Zealand (O’Shea 1999).

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Table 3 Family Grimpoteuthidae: recognised species and distribution

Species Distribution Comments References Grimpoteuthis umbellata Azores, NE Atlantic Type (and only) specimen Fischer 1883, Fischer & (Fischer, 1883) (2235 m) in poor condition, making Joubin 1907, Collins et al. comparisons difficult 2001a, Collins 2003 Grimpoteuthis abyssicola Tasman Sea, SW Pacific Single specimen O’Shea 1999 O’Shea, 1999 (4660 m) Grimpoteuthis bathynectes NE Pacific (2816–3932 m) Voss & Pearcy 1990 Voss & Pearcy, 1990 Grimpoteuthis boylei NE Atlantic (4000Ð4900 m) Large species Collins et al. 2001a, Collins, 2003 Collins 2003 Grimpoteuthis challengeri NE Atlantic (4800Ð4850 m) Large; possesses radula; Collins et al. 2001a, Collins, 2003 allied to G. tuftsi Collins 2003 Grimpoteuthis discoveryi N Atlantic (2600Ð4870 m) Small species Collins et al. 2001a, Collins, 2003 Collins 2003 Grimpoteuthis hippocrepium East Pacific (3334 m) Single damaged specimen Hoyle 1904, Voss & Pearcy (Hoyle, 1904) 1990 Grimpoteuthis inominata Chatham Rise, SW Pacific Two specimens only; O’Shea 1999, Collins 2003 (O’Shea, 1999) (1705Ð2002 m) originally described as Enigmatiteuthis inominata Grimpoteuthis meangensis North of Celebes, W Pacific Known only from two Hoyle 1885a,b, 1886 (Hoyle, 1885) (1100 m); Kermadec specimens described by Island, SW Pacific (915 m) Hoyle; generic status uncertain Grimpoteuthis megaptera NW Atlantic Known only from type Verrill 1885, Collins 2003 (Verrill, 1885) material, now lost Grimpoteuthis pacifica Coral Sea, north of Australia Single specimen only Hoyle 1885a (Hoyle, 1885) Grimpoteuthis plena NW Atlantic (1963 m) Single small specimen; Verrill 1885, Collins 2003 (Verrill, 1885) similar to G. wuelkeri Grimpoteuthis tuftsi NE Pacific (3585–3900 m) Large species; possesses Voss & Pearcy 1990 Voss & Pearcy, 1990 radula; allied to G. challengeri Grimpoteuthis wuelkeri N Atlantic (1500Ð2500 m) Similar to G. plena Grimpe 1920, Collins 2003 (Grimpe, 1920) Luteuthis dentatus Tasman Sea, SW Pacific Single specimen O’Shea 1999 O’Shea, 1999 (991 m) Luteuthis shuishi South China Sea Single specimen O’Shea & Lu 2002 O’Shea, & Lu 2002 (754Ð767 m) Cryptoteuthis NE Atlantic (2274Ð2300 m) Single specimen Collins 2004 brevibracchiata Collins, 2004

G. inominata was described (as Enigmatiteuthis inominata) from two specimens caught at depths of 1705–2002 m on the Chatham Rise (O’Shea 1999). O’Shea (1999) suggested that other Grim- poteuthis species (G. bathynectes, G. meangensis, G. pacifica and G. wuelkeri) be included in Enigmatiteuthis but Collins (2003) considered that all should be retained in Grimpoteuthis until the type species of this genus is described in detail.

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Genus Cryptoteuthis Collins, 2004

Diagnosis Bell-shaped grimpoteuthids, with small fins and short arms. Gills with seven broad lamellae. Suckers broad, cirri moderate in length. Shell U-shaped, with parallel lateral walls terminating in two lobes. Posterior salivary glands absent. Radula absent. Digestive gland entire. One species. Type species: Cryptoteuthis brevibracchiata (Collins 2004). Comments The genus Cryptoteuthis was described from a single specimen (C. brevibracchiata) caught from 2274Ð2300 m in the Porcupine Seabight, northeast Atlantic (Collins 2004). The species possesses characters of both Opisthoteuthis and Grimpoteuthis, with the body shape and short fins characteristic of Opisthoteuthis whilst the form of the shell, optic nerve configuration and the size and shape of suckers and cirri resemble Grimpoteuthis. There is a superficial resemblance to Luteuthis shuishi, but Cryptoteuthis brevibracchiata possesses an entire digestive gland, U-shaped shell, cirri of moderate length and lacks a radula. In a molecular study Cryptoteuthis was found to differ from both Grimpoteuthis and Opisthoteuthis, although it appeared more closely allied to Grimpoteuthis (Piertney et al. 2003), which supports inclusion in the family Grimpoteuthidae.

Genus Luteuthis O’Shea, 1999

Diagnosis Grimpoteuthids with moderate-sized fins, short cirri (<2% ML) and a bilobed digestive gland. Shell W-shaped with lateral wings tapering to acute, offset points. Radula well developed. Male accessory glands in linear sequence. Web supporting nodules absent. Two species. Type species: Luteuthis dentatus (O’Shea 1999). Comments The genus Luteuthis was described by O’Shea (1999) to accommodate a single spec- imen that differed from other described cirrates in possessing a radula, a bilobed digestive gland and a unique W-shaped internal shell. O’Shea (1999) included it in a novel family (Luteuthidae), but molecular evidence suggests it is closely allied to Grimpoteuthis (Piertney et al. 2003) and should be included in the Grimpoteuthidae. O’Shea (1999) and O’Shea & Lu (2002) suggested that G. tuftsi should also be included in Luteuthis, although it is probably better retained in Grimpoteuthis until a full evaluation of the genus is undertaken. The single Luteuthis dentatus specimen was caught at 991 m in the Tasman Sea (Table 3; O’Shea 1999). A second species, L. shuishi, was described from the South China Sea (O’Shea & Lu 2002) and the authors illustrate the dramatic effects of preservation on the form of cirrates, with the fins appearing considerably larger in the preserved specimen, when the gelatinous tissue of the mantle has shrunk.

Family Cirroctopodidae n. fam. Diagnosis Large cirrates with large, paddlelike and broad-based fins. Secondary web absent, shell V-shaped with lateral walls spikelike. Optic nerve passes though white body in 8Ð9 bundles. Radula absent. Posterior salivary glands absent. Digestive gland entire. Cirri of moderate length, approx- imately equal to maximum sucker diameter, commence between suckers 1 and 2. Gills of ‘half- orange’ form. Single genus. Comments The genus Cirroctopus was proposed by Naef (1923) to accommodate C. mawsoni, which was originally described as Stauroteuthis mawsoni (Berry 1917). Robson (1932) included both mawsoni and glacialis in his new genus Grimpoteuthis and this generic placement was followed (e.g., Nesis 1987, Voss 1988a) until the genus was removed from synonymy by O’Shea (1999). O’Shea (1999) included Cirroctopus within the Opisthoteuthidae and although Cirroctopus shares some characters with both Grimpoteuthis and Opisthoteuthis, the form of the shell, the fin shape

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Table 4 Family Cirroctopodidae: recognised species and distribution

Species Distribution Comments References Cirroctopus mawsoni Southern Ocean, south of Type species of genus, Berry 1917, (Berry, 1917) Australia and in the Indian originally described as Naef 1923, Ocean sector (526Ð911 m) Stauroteuthis mawsoni O’Shea 1999 Cirroctopus glacialis Antarctic Peninsula, Deception = Cirroteuthis glacialis Robson 1930, (Robson, 1930) Island (333-914 m) Robson 1930 Vecchione et al. 1998 Cirroctopus antarctica Southern Ocean, 62¡S in the Possibly a junior synonym of Kubodera & (Kubodera & Okutani, 1986) Pacific Sector (509–804 m) C. glacialis (see O’Shea 1999) Okutani 1986 Cirroctopus hochbergi Off New Zealand only, Similar to C. mawsoni O’Shea 1999 O’Shea, 1999 750Ð1200 m

and the arrangement of optic nerves are unique and warrant inclusion in a separate family. This separation is supported by the molecular data of Piertney et al. (2003).

Genus Cirroctopus Naef 1923

Diagnosis As family. Four species. Type species: Cirroctopus mawsoni (Berry 1917). Comments The genus is restricted to the southern hemisphere (Table 4). C. glacialis was described from a single specimen trawled near Deception Island (Robson 1930), but has subsequently been found abundantly around the Antarctic Peninsula (Vecchione et al. 1998). The status of C. antarc- tica, which was described from 62ûS in the Pacific Sector (Kubodera & Okutani 1986), is unclear. O’Shea (1999) considered it a junior synonym of C. glacialis, but the description of the beaks differs from those of C. glacialis (Vecchione et al. 1998). C. mawsoni is recorded from the Indian Ocean sector (see O’Shea 1999) and C. hochbergi was described from off New Zealand. Voss (1988a) mentioned, without describing, another Cirroctopus species from Walther Herwig collec- tions in the Scotia Sea. Bizikov (2004) considers that the shell of Cirroctopus represents a transi- tional form between the U-shaped shell of Grimpoteuthis and Opisthoteuthis and the paired stylets of incirrate octopods.

Ecology Habitat Evidence from behavioural studies, diet, underwater observations, net catches and interpretation of morphology suggests that the Opisthoteuthidae are primarily benthic, Cirroctopodidae and Grim- poteuthidae demersal and Cirroteuthidae benthopelagic. Little is known about habitat preferences. Most samples are collected from bottom trawls, a selective method that works only on deep-sea soft sediments and may bias our perspective of the cirrate habitat and distribution toward this type of substratum. In fact, deep-sea photographic surveys and observations from submersibles showed cirroteuthids (Roper & Brundage 1972) and Grimpoteuthis (Villanueva et al. 1997) associated with both soft and rocky bottoms.

Distribution patterns The cirrates are generally considered a deep-sea group usually found at depths in excess of 300 m, but have been reported from shallower depths close to the poles, where water temperature remains

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cool (Voss 1988a) and as an extreme example, a Cirrothauma murrayi specimen was captured with a dip net from an ice hole in the Arctic Ocean (86ûN, 173ûE) (Voss 1967). At lower latitudes Opisthoteuthis is generally the shallowest genus, with O. californiana reported from as shallow as 125 m (Pereyra 1965), and Opisthoteuthis sp. occasionally consumed by fur seals, which have limited diving capability (Gales et al. 1993, see Trophic ecology section, p. 307). The bathymetric distribution of species varies geographically, for instance, Stauroteuthis syrtensis occurs much shallower in waters around Greenland (Collins 2002) than it does to the west and southwest of the British Isles (Collins et al. 2001a) and is likely to be influenced by factors such as temperature, food availability and dissolved oxygen concentration. Cupka (1970) suggested that the distribution of Opisthoteuthis agassizii in the DeSoto Canyon (Gulf of Mexico) is influenced by oxygen con- centration. In the canyon an oxygen minimum occurs between 400 and 500 m, below which concentration increases with depth and O. agassizii only occurred below 500 m, with the smaller individuals, which have relatively larger gills, at the shallower depths. In a given location there is likely to be a distinct bathymetric succession of cirrate species and Collins et al. (2001a) showed distinct depth-related patterns in the cirrate fauna of the northeast Atlantic. In the Porcupine Seabight (northeast Atlantic) Opisthoteuthis is the shallowest genus (877Ð2287 m), with a succession of Grimpoteuthis species extending from 1775 m to abyssal depths. Stauroteuthis syrtensis is caught at 1425Ð3100 m, with Cirrothauma murrayi and Cirro- teuthis muelleri occurring at abyssal depth. The type specimen of Cryptoteuthis brevibracchiata was also caught in the Porcupine Seabight from 2250 m (Collins 2004). Observations from photo- graphic (Jahn 1971, Roper & Brundage 1972, Pearcy & Beal 1973) and submersible surveys (Vecchione & Roper 1991, Vecchione & Young 1997, Villanueva et al. 1997, Johnsen et al. 1999a,b) suggest that cirrates are generally solitary individuals, with no evidence of schooling. However, abundance estimates from photo surveys have been reported as high as 2000 individuals kmÐ2 in the Arctic and from trawl surveys of up to 500 individuals kmÐ2 (see Table 5).

Reproduction Characters of sexual maturity

Quantitative studies on cirrate octopod reproduction have only been made for Opisthoteuthis species, a group where males are usually larger than females. Males of this genus have enlarged, modified suckers of unknown function, in one or two fields of one to all arm pairs, a character absent in females (see Figure 4). As an external sexual character, the enlarged sucker diameter clearly discriminates sexually immature and mature males (Villanueva 1992a). Sucker diameter also dis- criminates males and females in Stauroteuthis syrtensis (Collins & Henriques 2000), where suckers are capable of light emission (Johnsen et al. 1999a,b), and in some species of Grimpoteuthis (Collins 2003). There is a large difference in investment in gonad tissue between sexes, with relative gonad size approximately 10 times greater in females than in males of equivalent body size in Opistho- teuthis massyae (Daly et al. 1998). Males produce small spermatophores (or ‘sperm packets’) characteristic of cirrates (see Figure 16), located in the seminal vesicle and terminal organ, with up to 196 found in Cirrothauma magna (Guerra et al. 1998), ca. 100 in Stauroteuthis syrtensis (Collins & Henriques 2000), 15Ð103 (mean: 42) in Opisthoteuthis calypso, and 2Ð172 (mean: 72) in O. massyae (Villanueva 1992a). The biochemical composition of the mature male gonad of Opisthoteuthis sp. shows low protein (50.6 % dry weight) and total amino acid (protein-bound + free amino acids: 46.6 % dry weight) content and high lipid (11.4%) and cholesterol (2.3%) values (Rosa et al. 2005). In O. massyae, the genital complex in mature females constituted a mean of 2.6% (range 1.5Ð7%) of the total body mass (Boyle & Daly 2000). This reproductive investment

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Table 5 Abundance estimates of cirrate octopods

Density Species Gear Depth (m) (ind km-2) Location References Cirroteuthis muelleri Bottom trawl 2001Ð4850 1.4Ð6.2 Porcupine Seabight and Collins et al. 2001a Abysal Plain, NE Atlantic Cirrothauma Bottom trawl 2001Ð4850 1.2Ð6.2 Porcupine Seabight and Collins et a.l 2001a murrayi Abysal Plain, NE Atlantic Stauroteuthis Bottom trawl 1001Ð2000 8.5Ð8.9 Porcupine Seabight, NE Collins et al. 2001a syrtensis Atlantic Grimpoteuthis Bottom trawl 1501Ð2000 2.7 Porcupine Seabight, NE Collins et al. 2001a wuelkeri Atlantic Grimpoteuthis sp.* Bottom trawl 2001Ð4850 1.3Ð25 Porcupine Seabight and Collins et al. 2001a Abysal Plain, NE Atlantic Opisthoteuthis Bottom trawl 686Ð823 1** Off Columbia River, NE Pereyra 1965 californiana Pacific Opisthoteuthis Bottom trawl 483Ð490 6Ð23 Off Namibia, SE Atlantic Villanueva & calypso Guerra 1991 Opisthoteuthis Bottom trawl 829Ð836 202Ð499 Off Namibia, SE Atlantic Villanueva & massyae Guerra 1991 Bottom trawl 750Ð1500 1.5Ð5.7 Porcupine Seabight and Collins et al. 2001a Abysal Plain, NE Atlantic Unidentified cirrates Bottom trawl 1093Ð5043 0.3Ð3.3** Bahamas Islands, NW Vecchione 1987 Atlantic Unidentified cirrates Photographic 2360Ð3786 2000 Arctic Ocean Pearcy & Beal 1973 survey Unidentified cirrates Photographic 3900 (average) 98 Virgin Island Basin, NW Roper & Brundage survey 5000 (average) 32 Atlantic 1972 4300 (average) 1.1 Blake Basin, NW Atlantic 2500 (average) 1.3 Bermuda, NW Atlantic Northeast Channel, NE Atlantic

Note: * mixture of Grimpoteuthis boylei, G. challengeri and G. discoveryi; ** density in ind hÐ1.

is very low compared with incirrate octopods, such as Eledone cirrhosa, which reaches 19% (Boyle & Knoblock 1983) and reflects the cirrate spawning strategy, in which reproductive invest- ment is spread over an extended period, with eggs maturing and being released one or two at a time. An interesting feature recorded in the ovary of cirrates is the formation of a follicular sheath around each maturing egg that remains attached to the ovary after mature eggs are released into the proximal oviduct. First described in Opisthoteuthis massyae (Daly et al. 1998, Boyle & Daly 2000), these sheaths were also observed in Stauroteuthis syrtensis (Collins & Henriques 2000) and probably exist in other genera (see Figure 15D). The number of empty follicular sheaths increases linearly with body size and represents an estimation of the egg-laying record over the female’s lifetime. The number of eggs in the ovary and oviducts plus the number of empty follicular sheaths, provides an accurate estimation of the absolute fecundity, which for Opisthoteuthis massyae was 1396 eggs (mean), with an individual maximum of 3202 eggs (Boyle & Daly 2000). This novel

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approach indicates that previous studies on Opisthoteuthis reproduction probably underestimated fecundity. This is the case for O. californiana, with 225Ð475 eggs (Pereyra 1965), and 1400Ð2381 eggs (Laptikhovsky 1999); O. agassizii, 320 eggs (Cupka 1970); O. calypso, 209Ð833, mean 648 eggs; and O. massyae from the southeast Atlantic, 621Ð1735, mean 934 eggs (Villanueva 1992a). Fertilisation in cirrates is internal and probably takes place in the proximal section of the oviducal gland, where spermatophores have been observed in Cirrothauma murrayi (Aldred et al. 1983) but the location has not been confirmed for other cirrates. Single (e.g., Opisthoteuthis massyae) or two (e.g., O. calypso) encapsulated eggs are often present in the distal oviduct of mature females, apparently ready to be released. These eggs from the distal oviduct have an outer, rigid egg capsule, sometimes with rudiments of an egg shell stalk. This hard egg capsule is produced by the oviducal gland and, in Opisthoteuthis, its mineral composition includes 27Ð32% sulphur (Villanueva 1992a). The egg capsule may be smooth or sculptured with considerable interspecific variation, with longitudinal striations in O. agassizii and O. massyae, circular lines and ridges in O. chathamensis and Cirroctopus hochbergi and irregular shapes in Opisthoteuthis calypso, O. chathamensis and Cirroctopus hochbergi. Eggs coated by the egg shell in the distal oviduct are presumably fertilised so the female carries the early developing embryo for an unknown period of time until it is released.

Reproductive strategy

Considerable growth takes place in both sexes after the onset of the sexual maturity and no seasonality has been observed in spawning of Opisthoteuthis, the only cirrate genus in which reproduction has been quantified. Analysis of the ovarian oocyte size frequency is consistent with continuous egg production and the relationships between total body weight and number of sper- matophores in males or number of eggs in the oviducts of females, are uncorrelated, indicating a continuous production and release of spermatophores and eggs over the adult life-span (Villanueva 1992a, Daly et al. 1998, Laptikhovsky 1999, Boyle & Daly 2000). A number of other studies, mostly taxonomic with small sample sizes, show similar characteristics of the mature female reproductive tract, with a few eggs of large size in the oviducts, indicating that a single, extended and continuous period of egg maturation and spawning is a common trend in the reproductive strategy of cirrate octopods (Table 6). This reproductive pattern differs notably from incirrate octopods. Coastal incirrate octopods of the family Octopodidae (e.g., Octopus vulgaris) are characterised by decreasing feeding activity and growth as spawning approaches, which eventually ceases during spawning and brooding (Mangold 1983). An exception is O. chierchiae, which, in captivity, feeds and grows in between laying multiple egg batches (Rodaniche 1984). Pelagic incirrate octopods of the genus Argonauta and Ocythoe spawn over a prolonged period (Laptikhovsky & Salman 2003), continuing to feed and grow while spawning. However, this strategy differs from the cirrate octopods because spawning takes place at the end of the life cycle and is essentially an extended terminal spawning (Figure 17). Mating behaviour in cirrates is unknown. Males lack the hectocotylus, which is used as an intromittent organ in incirrate octopods, and no copulatory organs have been described. It is suggested that the long funnel of Cirrothauma murrayi males may be used to transfer spermato- phores to the female mantle cavity (Aldred et al. 1983). Females, however, also have a long funnel. In Cirroctopus glacialis (see Figure 2 in Vecchione et al. 1998), Opisthoteuthis calypso and O. massyae (Villanueva et al. 2002), the terminal end of both the distal oviduct in females and terminal organ in males are slightly pigmented. These areas of pigmented skin may indicate organ surfaces that are sometimes exposed outside the mantle cavity, for example during spawning and/or mating. Cirrate females are not thought to brood their eggs, instead eggs are released singly on the sea floor. Spawning areas, which have been described from submersibles for deep-sea incirrate octopods

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Table 6 Egg size in cirrate octopods from different developmental stages: ovary, oviducal gland, oviducts or spawned

Ovarian Species egg size (mm) Development References Cirroteuthis muelleri 10.4 × 9.3 Ovarian Voss & Pearcy 1990 10-11 Oviduct Eschricht 1836 Cirrothauma magna 11.3 Ovarian Guerra et al. 1998 14.5 Ovarian Collins et al. 2001b 12.5 Oviduct Collins et al. 2001b Cirrothauma murrayi 13.8 × 8.4 Oviduct Aldred et al. 1983 14 × 8.9 Oviduct Aldred et al. 1983 15.5 ? Voss 1988a Stauroteuthis gilchristi 9.5 Ovarian Collins & Henriques 2000 Stauroteuthis syrtensis 11 × 6 Oviduct Robson 1932 9Ovarian Collins & Henriques 2000 11 × 6.5 Oviducal Collins & Henriques 2000 Grimpoteuthis abyssicola 17.8 × 7Ovarian? O’Shea 1999 Grimpoteuthis boylei 18Ð20* Oviduct Collins 2003 Grimpoteuthis challengeri 13 Oviduct Collins 2003 Grimpoteuthis discoveryi 10Ð11 Oviducal Collins 2003 Grimpoteuthis meangensis 12.2 × 6? Robson 1932 Grimpoteuthis wuelkeri 12Ð13 Ovarian Collins 2003 14.0 Oviduct Grimpoteuthis sp. 12.5 × 7 Oviduct Voss 1955, reported as G. umbellata Luteuthis shuishi 17.8 × 11** O’Shea & Lu 2002 Cirroctopus glacialis 16 × 10 Oviduct Vecchione et al. 1998, reported as Grimpoteuthis 22 × 14* Oviduct Grimpoteuthis antarctica 10 × 7 Oviduct Kubodera & Okutani 1986 Cirroctopus hochbergi to 15.8 × 10** O’Shea 1999 Opisthoteuthis albatrossi 10 × 7Ovarian Sasaki 1920, 1929 Opisthoteuthis agassizii 7.7Ð10.2 × 5.8Ð7.7 Oviduct Cupka 1970 Opisthoteuthis californiana 9 × 5Ovarian Berry 1949 11 × 6 Oviduct Pereyra 1965 10 × 5Ovarian Laptikhovsky 1999 Opisthoteuthis calypso 5.1Ð7.5 × 3.6Ð4 Oviduct Villanueva 1992a, reported as O. agassizii Opisthoteuthis chathamensis 7.9 × 4.0 Oviduct O’Shea 1999 Opisthoteuthis massyae 9.9 Ovarian Sánchez & Guerra 1989, reported as O. vossi 10 Ovarian Boyle & Daly 2000; reported as O. grimaldii 10.4 × 5 Oviduct Villanueva 1992a; reported as O. vossi 12 Oviduct Daly et al. 1998; reported as Opisthoteuthis sp. 12 Oviduct Boyle & Daly 2000; reported as O. grimaldii Opisthoteuthis mero 7.2 × 4.9 Ovarian O’Shea 1999 Opisthoteuthis sp. 7 × 4 Oviduct Hochberg et al. 1992, NE Pacific Unidentified cirrate 15Ð16 × 11Ð12 Spawned Verrill 1885 Unidentified cirrates 12 × 15; 12 × 9; Spawned Boletzky 1982 A, B, C, D, E, F 24 × 11; 12.5 × 8; ~ 12; ~16 × 9

Note: *includes shell, **eggs free in mantle cavity

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Figure 17 Schematic representation of somatic growth versus spawning mode in different octopods (note that the growth curves are unrealistic). Sources of information: Boyle & Daly (2000) and Villanueva (1992a) for cirrate octopods; Laptikhovsky & Salman (2003) for the Argonautidae; Rodaniche (1984) for Octopus chierchiae and Mangold (1983) for Octopus vulgaris.

such as Graneledone and Benthoctopus (Voight & Grehan 2000, Drazen et al. 2003), are unknown for cirrates. The few illustrations of the spawned cirrate eggs that exist show different sizes and sculpture of the egg shell (Boletzky 1982, Norman 2000). Boletzky (1982) described six large eggs and embryos of unidentified cirrates (see Table 6, Figure 18). The eggs possessed different colouration (beige or brown) and patterns of sculpture (irregular, longitudinal or hexagonal ridge pattern). The embryos have an early differentiation of very large fins, but lack the cirri on the arms, that are characteristic of the group. The large eggs of the cirrates suggest direct developing juveniles. Spawned eggs of unidentified cirrates have been collected attached to gorgonians (Verrill 1885) and it can be expected that mature females will be associated with areas rich in hard substrata where they can attach their eggs. The fact that females are less abundant than males in trawl samples that usually operate on soft, deep-sea muddy bottoms, seems to corroborate this hypothesis. From trawl samples, males are more abundant than females in Opisthoteuthis massyae from the northeast Atlantic (1.5:1, Boyle & Daly 2000), and southeast Atlantic (1.6:1, Villanueva 1992a), in O. calypso (1.7:1, Villanueva 1992a), O. californiana (2.4:1, Laptikhovsky 1999; 1.8:1, Pereyra 1965), and Cirroctopus glacialis (2.4:1, Vecchione et al. 1998). The low proportion of females could be a consequence of different factors, but may suggest that mature females of these species associate with rocky areas to spawn, and are inaccessible to trawls. The duration of the embryonic development in cirrates is unknown. As egg size and water temperature are primary determinants of the duration of embryonic development in cephalopods, it can reasonably be expected that cirrate embryos will take a long time to develop, probably comparable with shark eggs (Boletzky 1982, 1994). From models using egg size and incubation temperature, Laptikhovsky (1999) estimated the embryonic development of Opisthoteuthis califor- niana in the northwest Bering Sea as 1.4 yr at 4ûC, and Nesis (1999) estimated 2.6 yr for the development of Cirroteuthis muelleri at Ð0.8ûC in the Central Polar Basin and a 2.5 yr development

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Figure 18 Unidentified eggs and embryos of cirrate octopods. (A) Egg capsule (16 mm capsule length (CL)), (B) same with shell removed to expose chorion and embryo, (C) egg capsule (24 mm CL), (D) same with shell removed to expose chorion and embryo, (E) ventral and (F) dorsal views of embryo from (B). Modified with permission from Boletzky (1982).

time for the Antarctic Cirroctopus glacialis at 0.5ûC. Posthatching life in cirrates is also unknown, but is probably very long. Assuming that most of the ovarian oocytes will grow and are then released one by one, and considering the decline in metabolic rates of deep-sea cephalopods living at low temperatures (Seibel et al. 1997), the life cycle of cirrate octopods is likely to last many years.

Trophic ecology Diet and prey capture

In comparison with incirrate octopods, cirrates generally appear to feed on smaller prey. A study of the diet of Opisthoteuthis calypso and O. massyae showed that both species are epibenthic or suprabenthic feeders with benthic gammarid amphipods and polychaetes the major prey categories, and a variety of small crustaceans ranging from 1Ð8 mm in length, including tanaids, cumaceans, mysids, ostracods, decapods and copepods also taken (Villanueva & Guerra 1991). A number of other studies have reported on the diet of small numbers of specimens, indicating a common trend in cirrates of feeding on small-sized organisms with low swimming speeds (Table 7). Suckers and cirri seem to play an important role in chemo- and mechanoreception in Opisthoteuthis (Villanueva & Guerra 1991), with small, unmodified suckers (1Ð3 mm in diameter), adapted to handling small

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Table 7 Main prey recorded from stomach contents in cirrate octopods

Sample Species Main Prey Size References Stauroteuthis syrtensis Crustacea, mostly copepods 1 Vecchione & Young 1997 Opisthoteuthis Amphipods, mysids and polychaetes 1 Voss 1956 agassizii Polychaetes, cumaceans, amphipods, calanoid Several Cupka 1970 copepods and decapod crustaceans Decapod crustaceans, octopod beaks and 2 Lipka 1975 foraminiferans Opisthoteuthis Copepods, isopods, amphipods, mysids, crangonid 8 Pereyra 1965 californiana or hippolytid shrimp and sand Opisthoteuthis calypso Crustacea: Macrura Natantia and Reptantia, 5 Alcazar & Ortea 1981 amphipods and isopods reported as O. agassizii Mostly polychaetes, gammarid amphipods, mysids 125 Villanueva & Guerra and decapods, also tanaids, ostracods, copepods, 1991, reported as isopods, bivalves and cumaceans O. agassizii Opisthoteuthis Crustaceans, shrimps and fishes 1 Meyer 1906 depressa Opisthoteuthis Mostly gammarid amphipods, polychaetes, isopods 93 Villanueva & Guerra massyae and decapods, also mysids, ostracods, copepods, 1991, reported as tanaids, gastropods and bivalves O. vossi Opisthoteuthis robsoni Large amphipods 1 O’Shea 1999 Opisthoteuthis sp. Nauplii and adult Artemia (in aquaria) 1 Hunt 1999 reported as Polychaetes (in the field) 1 Grimpoteuthis sp. Grimpoteuthis boylei Polychaetes, calanoid copepods, amphipods and 1 Collins 2003 isopods Grimpoteuthis Isopods, amphipods, copepods 1 Scott 1910 hippocrepium Grimpoteuthis Small crustaceans 1 Ebersbach 1915 wuelkeri Cirroctopus glacialis Polychaetes 1 Robson 1930 Unidentified cirrates Benthopelagic copepods 5 Vecchione 1987

prey. In addition to the sensory role, a functional role of the cirri to assist in prey capture and transport to the mouth has been observed in aquaria for Opisthoteuthis sp. (Hunt 1999), probably a common trait for other cirrates. Nothing is known about the diet of the pelagic Cirroteuthidae. The pumping behaviour observed in a cirroteuthid, swimming close to the sea bottom (Villanueva et al. 1997; Figure 19) indicates that, in addition to planktonic prey, suprabenthic prey can also be expected in their diets. Based on the presence of buccal secretory glands in Stauroteuthis syrtensis, Vecchione & Young (1997) suggested that this species may feed by entrapping prey in a mucus web handled by the long cirri. Johnsen et al. (1999b) suggest that given the oral position of the photophores of S. syrtensis, and

the wavelength of peak emission (λmax = 470 nm), the moderately bright, blue-green biolumines- cence may function as a light lure to attract prey. The deeply pigmented digestive system of cirrates suggests feeding on bioluminescent prey (Vecchione & Young 1997), but the stomachs of Opistho- teuthis analysed did not, with the possible exception of the copepod Oncaea conifera, include bioluminescent species (Villanueva & Guerra 1991). Cirrate eyes are large compared with the body, but it is unknown how important they are for prey and/or predator detection and no studies on their retinal structure and visual capabilities have

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Figure 19 Pumping locomotion in Cirroteuthidae close to the seafloor. Line drawings based on video record- ings taken from the manned submersible NAUTILE. Reproduced with permission from Villanueva et al. (1997).

been published. An exception is Cirrothauma murrayi whose eye is a simple cup with a cornea and large pupil but with no iris, ciliary muscles or lens and with small, relatively simply, optic lobes (Aldred et al. 1983). Despite their small size, the eyes of C. murrayi are probably sufficient to detect the bioluminescence produced by other animals and the wide aperture of the cornea allows for detection of flashes over wide angles and for greater sensitivity (Aldred et al. 1983, Warrant & Locket 2004).

Predators

Few predators of the cirrates have been described, but this lack of information is probably a consequence of difficulties in distinguishing the beaks and the lack of studies of bathyal and abyssal predators. The existing information comes from beaks and whole specimens collected in stomach contents of fishes, sharks and sperm whales and in the faeces of fur seals. The Patagonian toothfish (Dissostichus eleginoides) seems to be an active predator on cirrate octopods. This species is primarily ichthyophagous, preying secondarily on a large diversity of cephalopods (Xavier et al. 2002). Patagonian toothfish have been reported to prey on unidentified cirrate octopods around Macquarie Island, South Pacific, at depths of 500–1290 m, where cirrates represented 0.7 % of the total biomass consumed and cephalopods reach 32% of the total prey biomass (Goldsworthy et al. 2002). Stomach contents of the Patagonian toothfish collected from 520–1930 m near the Crozet Islands in the Southern Indian Ocean showed that Stauroteuthis gilchristi, Opisthoteuthis sp. and other unidentified cirrates, represented 8% of the total cephalopod biomass consumed (Cherel et al. 2004). An unidentified large cirrate was collected in stomach contents of the sleeper shark (Som- niosus cf. microcephalus) caught between 350 and 763 m near the Kerguelen Islands, Indian Ocean

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(Cherel & Duhamel 2004). Smale & Cliff (1998) recorded a possible Grimpoteuthis from the stomach contents of the scalloped hammerhead shark Sphyrna lewini collected off KwaZulu-Natal, South Africa. Marine mammals also feed on opisthoteuthids, the shallowest group of cirrates. Gales et al. (1993) reported Opisthoteuthis sp. from the diet of the Australian fur seal (Arctocephalus pusillus doriferus) in Pedra Branca, southern Tasmania, where the cirrates appeared in 4.2% of the samples. Three Opisthoteuthis mero specimens of 46Ð55 mm ML have been reported in sperm whale stomach contents collected off New Zealand, southeast Pacific (O’Shea 1999). It is unknown how cirrates interact or escape from their possible predators. Behavioural responses to disturbance, such as ballooning and web inversion, can be expected (see next section).

Behaviour The behavioural implications of low levels of ambient light in the deep sea have long been recognised for many organisms (Herring et al. 1990, Warrant & Locket 2004). Seibel et al. (2000a) pointed out that the reduction in predator-prey detection distances associated with low light levels in the deep sea influences reproduction, metabolism and behaviour of deep-sea cephalopods. Studies by Seibel and colleagues (Seibel et al. 1997, 1998, 2000b, Hunt & Seibel 2000, Seibel & Childress 2000) have demonstrated that in the deep sea, where high speeds are not strongly selected, the use of fins and arms for locomotion in cephalopods reduces the cost for transport in comparison with the energetically expensive jet propulsion mode, used by coastal and oceanic species of cephalopods (O’Dor & Webber 1986, Wells 1990, Wells & Clarke 1996). In situ video recordings of cirrates obtained from submersibles support this hypothesis, as jet propulsion has not been observed (Vecchione & Roper 1991, Vecchione & Young 1997, Villanueva et al. 1997). However, it is possible that jet propulsion of unknown, presumable low intensity can exist during burst swimming and during ventilation of the mantle cavity to oxygenate the gills.

Behavioural and physiological adaptions to the deep sea Compared with the muscular, high-protein coastal cephalopods, the gelatinous musculature of the cirrates is significantly lower in nitrogen and carbon compound contents. The biochemical com- position of the muscle in Opisthoteuthis sp. (Rosa et al. 2005) is relatively low in protein (53% dry weight) and lipid (3.4%) reflecting a mode of life where high speeds and high metabolic rates are not required. The different cirrate families use different behaviours and modes of locomotion according to their mode of life (benthic or benthopelagic), which is reflected in their morphology and physiology. External and internal morphology of the four cirrate families show characters that indicates the different adaptations, ranging from the pelagic Cirroteuthidae to the seabed associated Opisthoteuthidae (see Figure 1, Figure 2, Figure 3, Figure 7 and Figure 10). In Cirroteuthidae, the long body, the presence of the thin and well-developed primary and secondary webs, and the large fins supported by a large internal shell (except in Stauroteuthis) reflect adaptions to the predominant use of fin and web swimming. On the other hand, the morphology of the Opisthoteuthidae, with ovoid body shape, thick web and small fins supported by a thin internal shell, indicates the predominant use of their relatively robust arms for locomotion. The bell-shaped Grimpoteuthidae and Cirroctopodidae show intermediate characters, probably reflecting their association with the sea bed as well as their capacity for fin swimming. Studies on cirrate aerobic and anaerobic metabolism support these behavioural differences between families. Enzyme activities of citrate synthase and octopine dehydrogenase measured in fin, mantle and arm tissue of Cirrothauma murrayi are consistent with predominant use of fin swimming, while those of Opisthoteuthis californiana suggest the predominant use of arms for locomotion (Seibel et al. 1998).

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Attitudes and modes of locomotion Descriptions of the attitudes, modes of locomotion, responses to high disturbance and feeding behaviour observed in cirrate octopods are given below. It should be borne in mind however that all of these behaviours are influenced by human disturbance (presence of the submersible, flashes, postcapture stress and/or captivity conditions) that influence in some degree the unmodified natural behaviour.

Bottom resting

In this posture, octopods are apparently resting, with their oral surface on the bottom. The mantle is erect and pointed posteriorly, with the web and arms spread out with distal ends curved inward, toward the oral surface, and fins extended parallel to the bottom. Prey searching on the epibenthic fauna cannot be ruled out using this posture. This posture has been observed from submersibles in Opisthoteuthis agassizii (Vecchione & Roper 1991) and Grimpoteuthis sp. (Vecchione & Young 1997, Villanueva et al. 1997) (Figure 20A).

Crawling

The octopod starts from a bottom-resting posture and moves backward supported mainly by its ventral and ventrolateral arms, with the dorsal and dorsolateral arms pulled in at each stroke of the former, moving the left and right arms symmetrically. Displacements in directions other than backward are possible, but have not been recorded. This behaviour has been observed in Grimpo- teuthis sp. (Villanueva et al. 1997) (Figure 20B, C).

Take-off

This mode of locomotion takes place from the bottom-resting, crawling and umbrella-style modes. Just before take-off, the distal tips of the arms are curved slightly back upon their aboral sufaces. Take-off is a single, strong pulsation generated by contraction of the brachial crown, sometimes accompanied by a forceful stroke of both fins, pulling the octopod body into a fusiform shape before fin-swimming starts. Take-off has been observed in Grimpoteuthis sp. and Cirroteuthidae (Villanueva et al. 1997) (Figure 20E).

Umbrella-style drifting

Individuals have arms and web outspread with the distal ends slightly curved toward the aboral surface. The fins are usually folded in against the mantle with the cirri erect. No active motion appears to be generated by the octopods, which seem to take advantage of the water currents and drift passively. This mode of locomotion requires little energy and may be extremely useful in deep-sea regions where energy-transfer rates are low. It has only been observed in cirroteuthid octopods (Roper & Brundage 1972, Villanueva et al. 1997) and Stauroteuthis syrtensis (Johnsen et al. 1999b) (Figure 20D, J).

Bell-like posture

Individuals drift with the anterior-posterior axis of the body horizontal, usually parallel to the sea bed, and the web inflated into a bell shape with the arms separated from the primary web by the membranes of the secondary web. The posture and movement is maintained by the use of the fins. This posture is only known for S. syrtensis (Nesis 1987 p. 66, Vecchione & Young 1997, Johnsen et al. 1999a) (Figure 21A).

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Figure 20 (See also Colour Figure 20 in the insert.) Photographs of cirrate octopods taken from the manned submersible NAUTILE at the mid-Atlantic Ridge, illustrating behaviour. Grimpoteuthis sp.: (A) bottom resting and (B, C) crawling. Cirroteuthidae: (D) drifting in umbrella style, (E) during take off and (F) fin-swimming. Grim- poteuthis sp.: (G-I) fin-swimming. Cirroteuthidae: (J) umbrella drifting, (K, L) taking off after touching submers- ible and displaying long cirri, (M, N) swimming by pumping. (O) Cirrothauma magna being manoeuvered into a sample box, showing ballooning response in three web sectors. (From Villanueva et al. (1997). With permission.)

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Figure 21 Line drawings based on in situ images of Stauroteuthis syrtensis illustrating (A, B) the bell posture and (C, D) different phases of the ballooning response. Sources: (A, B) redrawn from Vecchione & Young (1997); (C, D) redrawn from Johnsen et al. (1999b).

Fin swimming

In fin swimming, the near symmetrical movements of the fins result in a backward motion with the cirrate taking on a fusiform shape. The fin stroke begins with a rise starting in the posterior margin of the fins. The fins are then pushed vigorously downward, moving ventrally until they nearly cross beneath the ventral region of the mantle. Stroke cycles range from 4Ð30 minÐ1. Observed in Cirrothauma murrayi (Aldred et al. 1983), C. magna and Cirroteuthidae (Villanueva et al. 1997) and Grimpoteuthis sp. (Vecchione & Young 1997, Villanueva et al. 1997) (Figure 20GÐI).

Pumping

During this locomotion mode the mantle is erect, with arms and web outspread and the octopod pumps water by means of peristaltic waves running from the proximal interumbrellar region to the margin of the web, apparently using both the primary and secondary webs. The motion is slow and gentle, water waves take 11Ð18 s to reach the edge of the web, propelling the octopod in a placid movement in the opposite direction. Observed in Cirroteuthidae (Villanueva et al. 1997) (Figure 19 and Figure 20 M, N).

Arm-web contractions

The principal means of locomotion in Opisthoteuthis sp. observed over 2 months in the laboratory was arm-web, medusoid contractions (Hunt 1999). Contractions occurred at a rate of about 1.2 sÐ1 and the fins moved with simultaneous beats of 2 to 3 fin strokes for every web pulse. The fins also moved independently to control attitude and direction during swimming or passive sinking to the bottom of the tank. Arm-web pulses have been reported for other cirrates in the field such as O. agassizii (Vecchione & Roper 1991), Stauroteuthis syrtensis (Vecchione & Young 1997), and in aquaria for Opisthoteuthis californiana (Pereyra 1965) and Grimpoteuthis sp. (Vecchione & Young 1997).

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Responses to disturbance Ballooning response

Cirrate octopods react to disturbance by changing the curvature of the arms inward and fully expanding the web. The arm crown increases greatly in volume and the web sectors between the arms bulge out strongly, adopting a form similar to the segment of an orange, with just the distal part of the arms and web curved inward. This extravagant posture might have a stunning or disorienting effect on a potential predator (Boletzky et al. 1992) and it has also been hypothesised that the large acoustic size gained by a transition into a spherical shape from the normal flat posture (low acoustic reflection) may confuse a possible predator (Hovland 1992). This response, first described in a cirroteuthid (Boletzky et al. 1992), was also observed in the field for Stauroteuthis syrtensis (Vecchione & Young 1997, Johnsen et al. 1999b) (Figure 21C, D) and Cirrothauma magna (Villanueva et al. 1997) (Colour Figure 20O) and also in shipboard aquaria for Opisthoteuthis massyae (Villanueva 2000).

Web inversion

During web inversion the arms and web are upturned, with oral surface facing outward, completely covering the mantle, head and fins (Figure 22A,B). The distal portion of the arms remains highly curled. This response has been observed in Grimpoteuthis sp. in the field (Nesis 1987, p. 10) and shipboard aquaria (Vecchione & Young 1997) and in Opisthoteuthis massyae (Villanueva 2000). This behaviour is comparable with the defensive pattern described for Octopus by Packard & Sanders (1971) and also observed in Vampyroteuthis infernalis (de Gruy & Brown 1995).

Emission of bioluminescence

Emission from all the suckerlike structures arranged along the arms has been observed in shipboard aquaria when Stauroteuthis syrtensis specimens were gently prodded to induce bioluminescence (Johnsen et al. 1999a,b). Individual photophores glowed dimly and continuously or flashed on and off more brightly with a period of 1Ð2 s and, under continuous stimulation, photophores produces light for up to 5 min.

Figure 22 Line drawings illustrating (A) oral and (B) lateral views of web inversion in Opisthoteuthis massyae. Redrawn from photographs taken in a shipboard aquarium in Villanueva (2000).

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Feeding behaviour Hunt’s (1999) observations of 14 displays of feeding on Artemia nauplii and adults, by a mature female of Opisthoteuthis sp. (reported originally as Grimpoteuthis sp.) maintained in captivity for nearly 2 months, is the only existing knowledge of feeding behaviour in cirrates. The specimen exhibited three distinct feeding modes as follows:

Envelopment

When live prey was offered as food, the octopod opened its arms and web and enveloped dense groups of nauplii near the surface of the tank. The enclosed volume proceeded to shrink in size, first distally, working the prey toward the mouth. As water slowly escapes through the small aperture created by the arm tips, it appears there is some mechanism preventing the prey from escaping with the water, probably involving the cirri and suckers (Figure 23A).

Entrapment

The octopod extended its arms near the surface of the tank, keeping arm tips directed downward and descending, due to its slightly negative buoyancy, through the water column to the tank floor, trapping prey against the bottom by the oral side of the web. When the octopod settled, it forced prey and water toward its mouth by slow arm contractions and the enclosed volume become progressively smaller. Again, cirri and suckers are thought to play a functional role (Figure 23B).

Cirri-generated current feeding

When the octopod was on the bottom, coordinated cirral movements in metachronic waves toward the mouth generated slow currents of water that helped collect prey. Individual prey was observed being drawn into the oral cavity by these waves that had a periodicity of 1 sÐ1 (Figure 23C).

Figure 23 Feeding behaviour of Opisthoteuthis sp. in aquaria showing (A) envelopment, (B) entrapment and (C) cirri-generated current feeding. Reproduced with permission from Hunt (1999).

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It is not known how much time cirrates spend on different behaviours such as resting, swimming or feeding in the wild. In the southeastern Atlantic, O. massyae has been shown to undergo significant diel changes in abundance, with trawls indicating densities of 202Ð337 ind kmÐ2 during the day and 256Ð499 ind kmÐ2 during the night (Villanueva & Guerra 1991). There is no evidence of daily feeding patterns, so the higher abundances recorded at night could indicate a change in feeding method or activities independent of feeding (Villanueva & Guerra 1991). Under laboratory conditions, a mature female of Opisthoteuthis sp. spent most of its time resting on the bottom of the tank, swimming once or twice per hour to the surface (Hunt 1999). To date, all images collected from Cirroteuthidae species in the field showed animals in motion by fin swimming, pumping or drifting in different postures but never resting or crawling on the sea bottom. This is not the case for the species of Opisthoteuthidae and Grimpoteuthidae that, in addition to fin swimming, have been photographed and filmed resting and crawling (Vecchione & Roper 1991, Roux 1994, Vecchione & Young 1997, Villanueva et al. 1997). It should be noted that most observations on live cirrate octopods come from subadult and/or adult individuals. Younger cirrates have proportionally larger fins (see review of Hochberg et al. 1992) indicating that fin swimming is more important in the early life stages. Further behavioural research using both in situ video recordings and aquaria-maintained specimens (under suitable conditions of darkness and low temperature) is required to determine the behaviour of juveniles, sexual behaviour and mating in adults and to understand how cirrates utilise bioluminescence.

Conclusions Our understanding and interpretation of cirrate anatomy and taxonomy has advanced considerably in recent years and with improved identification it should be possible to conduct ecological and behavioural studies with greater confidence. Nearly half of the known cirrate species belong to the Opisthoteuthidae, the shallower group, and new taxa are likely to be found as scientific work continues in the deep sea, the largest ecosystem of the world. There are large areas of deep sea that remain unsampled and because cirrates have very large eggs, direct developing juveniles and a relatively low energy lifestyle, high levels of dispersion appear unlikely. Considerable problems remain with the existing taxonomy. Cirroteuthis muelleri and Cirroth- auma murrayi have apparent worldwide patterns of distribution, but specimens from a number of distant localities need to be critically reviewed to confirm this pattern. In the North Pacific region, the Opisthoteuthidae (Opisthoteuthis albatrossi, O. californiana, O. depressa, O. japonica) are in need of revision, with potential synonyms examined in detail. A key problem in the Grimpoteuthidae is the lack of a good description of the type species (Grimpoteuthis umbellata) and new material is required from the type locality and depth (Azores, 2235 m) for it to be resolved. It is possible that G. plena, G. wuelkeri or one of the recently described Atlantic species of Grimpoteuthis is a junior synonym of G. umbellata. With the exception of one or two species of Opisthoteuthis the ecology of the cirrates is poorly known, but this situation is unlikely to be easily resolved because the capture rate of the deeper species is very low and so samples are likely to be small. The reproductive strategy of cirrates is clearly different from other cephalopods, with eggs released individually over an extended period, during which time the animal continues to grow. Reproductive behaviour is not known, fertilisation is thought to occur in the oviducal gland, but how spermatophores are transferred is not known. Embryonic life also remains a mystery, and it can reasonably be expected that cirrate embryos will take >1 yr to develop individually on the sea floor. Longevity and growth are also major unknowns in the biology of the cirrates. Based on predicted development times and the relatively low productivity of the deep sea, it is likely that cirrates are long-lived compared with other cephalopods, but this assumption cannot be confirmed. Statoliths are

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now used routinely to age squid (see Jereb et al. 1991), and daily growth increments are found in most species studied, but they cannot be used in octopods. Growth increments have been identified in the stylets (equivalent to the shell) of incirrate octopods (Reis & Fernandes 2002), but their rate of deposition has not been validated. It is possible that growth increments will be found in the shell of cirrates, but direct validation requires maintenance of animals in aquaria and/or mark and recapture in the field, which is not a straightforward procedure for cirrates. The trophic ecology of the cirrates remains poorly understood and determining the diet of cirrates is likely to be hampered by small sample sizes; even less is known about foraging behaviour. Cirrate predators include marine mammals for shallow benthic species, indicating an energy transfer from the deep sea to the surface channelled by cirrates. Determining the predators of cirrates will be aided by a good knowledge of the fauna in predator foraging areas and by a detailed study of beak form and reference collections of beaks. The beaks of Stauroteuthis appear distinct from the other cirrates (see Figure 10) but the other genera are not so easily distinguished. Behavioural observations should yield more valuable information on cirrates. The observations of the bioluminescent suckers in Stauroteuthis syrtensis illustrate the value of live observations, because it would be difficult to determine the presence of light organs from anatomical studies alone (Chun 1913, Aldred et al. 1982, 1984). Bioluminescence is suspected in other cirrates and future research is needed in this intriguing field. Finally, it is worth noting that while the extension of commercial fishing into deeper waters has yielded many specimens for studies of taxonomy, ecology and distribution of cirrates, the consequences of fishing mortality on these potentially long-lived cephalopods is unknown and may already have significantly reduced population sizes in certain areas.

Acknowledgements Thanks to Ian Rendall, Liz White and Juliette Corley for providing many of the illustrations and to Mike Vecchione and Louise Allcock for providing photographs. Thanks to Eric Hochberg for inspiring discussions of cirrate biology. RV was supported by the Programa para Movilidad de Investigadores of the Spanish Ministry of Science.

References

Adam, W. 1962. Céphalopodes de l’archipiel du Cap-Vert, de l’Angola et du Mozambique. Memorias da Junta de Investigacoes do Ultramar 33, 9Ð64. Alcazar, J. & Ortea, J. 1981. Comentarios sobre Opisthoteuthis agassizi Verrill, 1883 (Cephalopoda: Octopoda) en el mar Cantábrico. Cuadernos del Crinas 6, 29Ð37. Aldred, R.G., Nixon, M. & Young, J.Z. 1982. Possible light organs in finned octopods. Journal of Molluscan Studies 48, 100Ð101. Aldred, R.G., Nixon, M. & Young, J.Z. 1983. Cirrothauma murrayi, a finned octopod. Philosophical Trans- actions of the Royal Society of London B 301, 1Ð54. Aldred, R.G., Nixon, M. & Young, J.Z. 1984. Ganglia not light organs in the sucker of octopods. Journal of Molluscan Studies 50, 67Ð69. Berry, S.S. 1917. Cephalopoda. Scientific Reports of the Australasian Antarctic Expedition 1911Ð1914 14, 1Ð39. Berry, S.S. 1918. Report on the Cephalopoda obtained by the F.I.S. “Endeavour” in the Great Australian Bight and other southern Australian localities. Biological Results of the Fishing Experiments Carried out by the F.I.S. “Endeavour”, 1909–14 4, 201Ð298. Berry, S.S. 1949. A new Opisthoteuthis from the eastern Pacific. Leaflets in Malacology 1, 23Ð26. Bizikov, V.A. 2004. The shell in Vampyropoda (Cephalopoda): morphology, functional role and evolution. Ruthenica, Supplement 3, 1Ð88.

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Boletzky, S.v. 1982. On eggs and embryos of cirromorph octopods. Malacologia 22, 197Ð204. Boletzky, S.v. 1994. Embryonic development of cephalopods at low temperatures. Antarctic Science 6, 139Ð142. Boletzky, S.v., Rio, M. & Roux, M. 1992. Octopod “ballooning” response. Nature 356, 199. Boyle, P.R., Collins, M.A. & Williamson, G.R. 1998. The cephalopod by-catch of deep-water trawling on the Hebrides slope. Journal of the Marine Biological Association of the United Kingdom 78, 1023Ð1026. Boyle, P.R. & Daly, H.I. 2000. Fecundity and spawning in a deep-water cirromorph octopus. Marine Biology 137, 317Ð324. Boyle, P.R. & Knoblock, D. 1983. The female reproductive cycle of the octopus, Eledone cirrhosa. Journal of the Marine Biological Association of the United Kingdom 63, 71Ð83. Bruun, A.F. 1945. Cephalopoda. Zoologica Iceland 4, 1Ð15. Carlini, D.B., Young, R.E. & Vecchione, M. 2001. A molecular phylogeny of the Octopoda (Mollusca: Cephalopoda) evaluated in light of morphological evidence. Molecular Phylogenetics and Evolution 21, 388Ð397. Cherel, Y. & Duhamel, G. 2004. Antarctic jaws: cephalopod prey of sharks in Kerguelen waters. Deep-Sea Research I 51, 17Ð31. Cherel, Y., Duhamel, G. & Gasco, N. 2004. Cephalopod fauna of subantarctic islands: new information from predators. Marine Ecology Progress Series 266, 143Ð156. Chun, C. 1911. Cirrothauma, ein blinder Cephalopod. Philosophiae Doctores Dissertation, University of Leipzig. Chun, C. 1913. Cephalopoda from the “Michael Sars” north Atlantic deep-sea expedition 1910. In Report of the Scientific Results of the “Michael Sars” North Atlantic Deep-sea Expedition 1910, Zoology, J. Murray & J. Hjort (eds). Bergen, Norway: Bergen Museum. Chun, C. 1915. Die Cephalopoden. Myopsida, Octopoda. Wissenschaftliche Ergebnisse der Deutschen Tiefsee Expedition auf dem Dampfer “Valdivia” 1898–1899 18, 405Ð552. Collins, M.A. 2002. Cirrate octopods from Greenland and Iceland waters. Journal of the Marine Biological Association of the United Kingdom 82, 1035Ð1036. Collins, M.A. 2003. The genus Grimpoteuthis (Octopoda: Grimpoteuthidae) in the north-east Atlantic, with descriptions of three new species. Zoological Journal of the Linnean Society 139, 93Ð127. Collins, M.A. 2004. Cryptoteuthis brevibracchiata: a new species and genus of cirrate octopod (Octopoda: Cirrata). Journal of Molluscan Studies 70, 263Ð267. Collins, M.A. 2005. Opisthoteuthis borealis: A new species of cirrate octopod from Greenland waters. Journal of the Marine Biological Association of the United Kingdom 85, 1475Ð1479. Collins, M.A., Allcock, A.L. & Belchier M. 2004. Cephalopods of the South Georgia slope. Journal of the Marine Biological Association of the United Kingdom 84, 415Ð419. Collins M.A. & Henriques, C. 2000. A revision of the family Stauroteuthidae (Octopoda: Cirrata) with redescriptions of Stauroteuthis syrtensis and S. gilchristi. Journal of the Marine Biological Association of the United Kingdom 80, 685Ð697. Collins, M.A., O’Dea, M. & Henriques, C. 2001b. A large Cirroteuthis magna (Cephalopoda: Cirrata) caught on the Cape Verde Terrace (North Atlantic). Journal of the Marine Biological Association of the United Kingdom 81, 357Ð358. Collins, M.A., Yau, C., Allcock, A.L. & Thurston, M.H. 2001a. Distribution of deep water benthic and bentho- pelagic cephalopods from the NE Atlantic. Journal of the Marine Biological Association of the United Kingdom 81, 105Ð117. Cupka, D.M. 1970. Observations on the biology and bathymetric distribution of the bathybenthic octopod Opisthoteuthis agassizii (Mollusca: Cephalopoda). MSc Thesis, Florida State University, Tallahassee, Florida. Daly, H.I., Boyle, P.R. & Collins, M.A. 1998. Reproductive status of Opisthoteuthis sp. over an annual cycle. South African Journal of Marine Science 20, 187Ð192. de Gruy, M. & Brown, R. 1995. Incredible Suckers. Oxford: Oxford Scientific Films. Drazen, J.C., Goffredi, S.K., Schlining, B. & Stakes, D.S. 2003. Aggregations of egg-brooding deep-sea fish and cephalopods on the Gorda Escarpment: a reproductive hot spot. Biological Bulletin (Woods Hole) 205, 1Ð7.

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Ebersbach, A. 1915. Zur Anatomie von Cirroteuthis umbellata Fischer und Stauroteuthis sp. Zeitschrift für Wissenschaftliche Zoologie 113, 361Ð483. Eschricht, D.F. 1836. Cirroteuthis mulleri, eine neue Gattung der Cephalopoden bildend. Academiae Caesareae Leopoldino-Carolinae Naturae Curiosorum 18, 627Ð634. Fischer, H. & Joubin, L. 1907. Cephalopodes. Expeditions Scientifiques du Travailleur et du Talisman 8, 313Ð353. Fischer, P. 1883. Note preliminaire sur une nouvelle espece du genre Cirroteuthis. Jounal de Conchyologie 31, 402Ð404. Gales, R., Pemberton, D., Lu, C.C. & Clarke, M.R. 1993. Cephalopod diet of the Australian fur seal: variation due to location, season and sample type. Australian Journal of Marine and Freshwater Research 44, 657Ð671. Goldsworthy, S.L., Williams, M., He, X., Young, J.W. & van den Hoff, J. 2002. Diet of Patagonian toothfish (Dissostichus eleginoides) around Macquire Island, South Pacific Ocean. Marine and Freshwater Research 53, 49Ð57. Grimpe, G. 1916. Chunioteuthis- Eine neue Cephalopodengattung. Zoologische Anzeiger 46, 349Ð359. Grimpe, G. 1920. Teuthologische Mitteilungen V. Zwei neue Cirraten-Arten. Zoologische Anzeiger 51, 230Ð243. Guerra, A., Villanueva, R., Nesis, K.N. & Bedoya, J. 1998. Redescription of the deep-sea cirrate octopod Cirroteuthis magna Hoyle 1885, and considerations on the genus Cirroteuthis (Mollusca: Cepha- lopoda). Bulletin of Marine Science 63, 51Ð81. Healy, J.M. 1993. Sperm and spermiogenesis in Opisthoteuthis persephone (Octopoda: Cirrata): Ultrastructure, comparison with other cephalopods and evolutionary significance. Journal of Molluscan Studies 59, 105Ð115. Herring, P.J., Campbell, A.K., Whitfield, M. & Maddock, L. 1990. Light and Life in the Sea. Cambridge: Cambridge University Press. Hochberg, F.G., Nixon, M. & Toll, R.B. 1992. Order Octopoda Leach, 1818. In “Larval” and Juvenile Cephalopods: A manual for their identification, M. J. Sweeney et al. (eds). Smithsonian Contributions to Zoology 513, 213Ð280. Washington, D.C.: Smithsonian Institution Press. Hovland, M. 1992. Balloon response explanation? Nature 357, 119. Hoyle, W.E. 1885a. Diagnosis of new species of Cephalopoda collected during the cruise of H.M.S. “Chal- lenger” — I. The Octopoda. Annals and Magazine of Natural History 15, 222Ð236. Hoyle, W.E. 1885b. Preliminary report on the Cephalopoda collected during the cruise of H.M.S. “Challenger” Part I. The Octopoda. Proceedings of the Royal Society of Edinburgh 13, 94Ð114. Hoyle, W.E. 1886. Report on cephalopods collected by HMS Challenger during the years 1873Ð1876. Report of the Scientific Results of the Voyage of HMS Challenger during the Years 1873Ð76 (Zoology) 16, 1Ð245. Hoyle, W.E. 1904. Reports on the Cephalopoda. Bulletin of the Museum of Comparative Zoology, Harvard 43, 1Ð72. Hunt, J.C. 1999. Laboratory observations of the feeding behaviour of the cirrate octopod, Grimpoteuthis sp.: one use of cirri. The Veliger 42, 152Ð156. Hunt, J.C. & Seibel, B.A. 2000. Life history of Gonatus onyx (Cephalopoda: Teuthoidea): ontogenetic changes in habitat, behavior and physiology. Marine Biology 136, 543Ð552. Ijima, I. & Ikeda, S. 1895. Description of Opisthoteuthis depressa n. sp. Journal of the College of Science, Imperial University, Tokyo 8, 323Ð337. Jahn, W. 1971. Deepest photographic evidence of an abyssal cephalopod. Nature 232, 487. Jereb, P., Ragonese, S. & Boletzky, S.v. (eds) (1991). Squid Age Determination Using Statoliths. Proceedings of the International Workshop held in the Institute de Tecnologia de la Pesca e del pescato (I.T.P.P.ÐC.N.R.), Mazara del Vallo, Italy. N.T.R., I.T.P.P. Special Publication No. 1. Johnsen, S., Balser, E.J. Fisher, E.C. & Widder, E.A. 1999b. Bioluminescence in the deep-sea cirrate octopod Stauroteuthis syrtensis Verrill (Mollusca: Cephalopoda). Biological Bulletin (Woods Hole) 197, 26Ð39. Johnsen, S., Balser, E.J. & Widder, E.A. 1999a. Light-emitting suckers in an octopus. Nature 398, 113Ð114. Joubin, L. 1903. Sur quelques céphalopodes recueillis pendant les dernieres campagnes de S.A.S. le Prince de Monaco (1901Ð1902). Comptes Rendus des Séances de l’Academie des Sciences 136, 100Ð102. Knudsen, J. & Roeleveld, M.A.C. 2002. J.T. Reinhardt and V. Prosch (1846): On Sciadephorus mulleri (Eschr.) — A translation into English. Bulletin of Marine Science 71, 421Ð447.

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Kubodera, T. & Okutani, T. 1986. New and rare cephalopods from the Antarctic waters. Memoirs of the National Institute of Polar Research Special Edition 44, 129Ð143. Laptikhovsky, V.V. 1999. Fecundity and reproductive strategy of three species of octopods from the north- western Bering Sea. Biologiya Morya (Vladivostok) 25, 342Ð346. Laptikhovsky, V.V. & Salman, A. 2003. On reproductive strategies of the epipelagic octopods of the superfamily Argonautoidea (Cephalopoda: Octopoda). Marine Biology 142, 321Ð326. Lindgren, A.R., Giribet, G. & Nishiguchi, M.K. 2004. A combined approach to the phylogeny of Cephalopoda (Mollusca). Cladistics 20, 454Ð486. Lipka, D.A. 1975. The systematics and zoogeography of cephalopods from the Gulf of Mexico. PhD Thesis, Texas A&M University. Mangold, K. 1983. Octopus vulgaris. In Cephalopod Life Cycles, Volume I: Species Accounts, P.R. Boyle (ed.), London: Academic Press, 335Ð364. Meyer, W.T. 1906. Die Anatomie von Opisthoteuthis depressa (Ijima und Ikeda). Zeitschrift für Wissenschaft- liche Zoologie 85, 183Ð269. Naef, A. 1923. Die Cephalopoden. Fauna e Flora de Golfo di Napoli, Monograph 35, 1 (part 2): 149Ð863. Nesis, K.N. 1986. Cephalopods from the seamounts of the western Indian Ocean. Okeanologia 26, 123Ð130 (In Russian with English summary). Nesis, K.N. 1987. Cephalopods of the World. New York and London: T.N.P Publications. Nesis, K.N. 1993. Cephalopods of seamounts and submarine ridges. In Recent Advances in Cephalopod Fisheries Biology, T. Okutani et al. (eds) Tokyo: Tokai University Press, 365Ð373. Nesis, K.N. 1999. The duration of egg incubation in high-latitude and deep-water cephalopods: estimation and ecological consequences. Biologiya Morya (Vladivostok) 25, 499Ð506. Nesis, K.N. 2001. West-Arctic and east-Arctic distributional ranges of cephalopods. Sarsia 86, 1Ð11. Norman, M.D. 2000. Cephalopods: a World Guide. Hachenheim: ConchBooks. O’Dor, R.K. & Webber, D.M. 1986. The constraints on cephalopods — why squid aren’t fish. Canadian Journal of Zoology 64, 1591Ð1605. Oommen, V.P. 1976. A new species of the genus Opisthoteuthis Verrill, 1883 (Cephalopoda: Mollusca) from the Southwest coast of India. Journal of the Marine Biological Association of India 18, 368Ð374. O’Shea S. 1999. The marine fauna of New Zealand: Octopoda (Mollusca: Cepahlopoda). NIWA Biodiversity Memoir, 112. Wellington: NIWA Research. O’Shea, S. & Lu, C.C. 2002. A new species of Luteuthis (Mollusca: Cephalopoda: Octopoda: Cirrata) from the South China Sea. Zoological Studies 41, 119Ð126. Packard, A. & Sanders, G.D. 1971. Body patterns of Octopus vulgaris and maturation of response to distur- bance. Animal Behaviour 19, 780Ð790. Pearcy, W.G. & Beal, A. 1973. Deep-sea cirromorphs (Cephalopoda) photographed in the Arctic Ocean. Deep- Sea Research 20, 107Ð108. Pereyra, W.T. 1965. New records and observations on the flapjack devilfish, Opisthoteuthis californiana Berry. Pacific Science 19, 427Ð441. Piatkowski, U. & Dieckmann, R. 2005. A short note on the cephalopods sampled in the Angola Basin during the DIVA-1 expedition. Organisms Diversity and Evolution 5, 227Ð230. Piertney, S.B., Huedelot, C., Hochberg, F.G. & Collins, M.A. 2003. Phylogenetic relationships among cirrate octopods (Mollusca: Cephalopoda) resolved using mitochondrial 16S ribosomal DNA sequences. Molecular Phylogenetics and Evolution 27, 348Ð353. Reinhardt, J.T. & Prosch,V. 1846. Om Sciadephorus mulleri (Eschr.). Det Kongelige Danske Videnskabernes Selskabs Naturvidenskabelige og Mathematiske Afhandlinger 12, 185Ð224. Reis, C.S. & Fernandes, R. 2002. Growth observations on Octopus vulgaris Cuvier, 1797 from the Portuguese waters: growth lines in the vestigial shell as possible tools for age determination. Bulletin of Marine Science 71, 1099Ð1103. Robson, G.C. 1924a. On new species of Octopoda from South Africa. Annals and Magazine of Natural History 13, 202Ð210. Robson, G.C. 1924b. On the Cephalopoda obtained in South African waters by Dr. J.D.F. Gilchrist in 1920Ð21. Proceedings of the Zoological Society of London 39, 589Ð686.

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Robson, G.C. 1925. The deep-sea Octopoda. Proceedings of the Zoological Society of London, 1925, 1323Ð1356. Robson, G.C. 1930. Cephalopoda, I. Octopoda. Discovery Reports 2, 371Ð401. Robson, G.C. 1932. A Monograph of Recent Cephalopoda. Part II. The Octopoda (excluding the Octopodinae). London: British Museum. Rodaniche, A.F. 1984. Iteroparity in the lesser Pacific striped octopus Octopus chierchiae (Jatta, 1889). Bulletin of Marine Science 35, 99Ð104. Roper, C.F.E. & Brundage, W.L. 1972. Cirrate octopods with associated deep sea organisms: new biological data based on deep benthic photographs (Cephalopoda). Smithsonian Contributions to Zoology 121, 1Ð46. Rosa, R., Pereira, J. & Nunes, M.L. 2005. Biochemical composition of cephalopods with different life strategies, with special reference to a giant squid, Architeuthis sp. Marine Biology 146, 739Ð751. Roux, M. 1994. The CALSUB cruise on the bathyal slopes off New Caledonia. In Résultats des Campagnes MUSORSTOM. Vol. 12, A. Crosnier (ed.). Memoires du Museum National d’Histoire Naturelle, Paris 161, 9Ð47. Sanchez, P. & Guerra, A. 1989. A new species of cirrate octopod Opisthoteuthis vossi from the southeast Atlantic (Cephalopoda: Octopoda). Bulletin of Marine Science 44, 1159Ð1165. Sasaki, M. 1920. Report on cephalopods collected during 1906 by the United States Bureau of Fisheries steamer “Albatross” in the northwestern Pacific. Proceedings of the United States National Museum 57, 163Ð203. Sasaki, M. 1929. A monograph of the dibranchiate cephalopods of the Japanese and adjacent waters. Journal of the College of Agriculture Hokkaido Imperial University, 20 (Supplement), 1Ð357. Scott, T. 1910. Notes on crustaceans found in the gizzard of a deep sea cephalopod. Annals and Magazine of Natural History 5, 51Ð54. Seibel, B.A. & Childress, J.J. 2000. Metabolism of benthic octopods (Cephalopoda) as a function of habitat depth and oxygen concentration. Deep-Sea Research I 47, 1247Ð1260. Seibel, B.A., Hochberg, F.G. & Carlini, D.B. 2000b. Life history of Gonatus onyx (Cephalopoda: Teuthoidea): deep-sea spawning and post-spawning egg care. Marine Biology 137, 519Ð526. Seibel, B.A., Thuesen, E.V. & Childress, J.J. 1998. Flight of the vampire: ontogenetic gait-transition in Vampy- roteuthis infernalis (Cephalopoda: Vampyromorpha). Journal of Experimental Biology 201, 2413Ð2424. Seibel, B.A., Thuesen, E.V. & Childress, J.J. 2000a. Light-limitation on predator-prey interactions: conse- quences for metabolism and locomotion of deep-sea cephalopods. Biological Bulletin (Woods Hole) 198, 284Ð298. Seibel, B.A., Thuesen, E.V., Childress, J.J. & Gorodezky, L.A. 1997. Decline in pelagic cephalopod metabolism with habitat depth reflects differences in locomotory efficiency. Biological Bulletin (Woods Hole) 192, 262Ð278. Smale, M.J. & Cliff, G. 1998. Cephalopods in the diets of four shark species (Galeocerdo cuvier, Shyrna lewini, S. zygaena and S. mokarran) from KwaZulu-Natal, South Africa. South African Journal of Marine Science 20, 241Ð253. Sweeney, M.J. &. Roper, C.F.E. 1998. Classification, type localities and type repositories of recent Cepha- lopoda. In Systematics and Biogeography of Cephalopods, N.A. Voss et al. (eds) Smithsonian Con- tributions to Zoology 586, 561Ð599. Taki, I. 1962. On species newly added to the fauna of Japanese Cephalopoda. Dobutsu-Gaku Zasshi [Zoological Magazine Tokyo] 71, 397Ð398 (in Japanese). Taki, I. 1963. On four newly known species of Octopoda from Japan. Journal of the Faculty of Fisheries and Animal Husbandry Hiroshima University 5, 57Ð93. Vecchione, M. 1987. A multispecies aggregation of cirrate octopods trawled from North of the Bahamas. Bulletin of Marine Science 40, 78Ð84. Vecchione, M. & Collins, M.A. 2002. Systematics, ecology and biology of cirrate octopods: workshop report. Bulletin of Marine Science 71, 79Ð96. Vecchione, M., Piatkowski, U. & Allcock, A.L. 1998. Biology of the cirrate octopod Grimpoteuthis glacialis (Cephalopoda: Opisthoteuthidae) in the South Shetland Islands, Antarctica. South African Journal of Marine Science 20, 421Ð428.

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Vecchione, M. & Roper, C.F.E. 1991. Cephalopods observed from submersibles in the Western North Atlantic. Bulletin of Marine Science 49, 433Ð445. Vecchione M. & Young, R.E. 1997. Aspects of the functional morphology of cirrate octopods: Locomotion and feeding. Vie et Milieu-Life and Environment 47, 101Ð110. Verrill, A.E. 1879. Notice of recent additions to the marine fauna of the eastern coast of North America, No. 7. American Journal of Science and Arts 18, 468Ð470. Verrill, A.E. 1883. Supplementary report on the “Blake” cephalopods. Bulletin of the Museum of Comparative Zoology 11, 105Ð115. Verrill A.E. 1885. Third catalogue of Mollusca recently added to the fauna of the New England coast and the adjacent parts of the Atlantic, consisting mostly of deep-sea species with notes on others previously recorded. Transactions of the Connecticut Academy of Science 6, 395Ð452. Villanueva, R. 1992a. Continuous spawning in the cirrate octopods Opisthoteuthis agassizii and O. vossi: features of sexual maturation defining a reproductive strategy in cephalopods. Marine Biology 114, 265Ð275. Villanueva, R. 1992b. Deep-sea cephalopods of the north-western Mediterranean: indications of up-slope ontogenetic migration in two bathybenthic species. Journal of Zoology London 227, 267Ð276. Villanueva, R. 2000. Observations on the behaviour of the cirrate octopod Opisthoteuthis grimaldii (Mollusca, Cephalopoda). Journal of the Marine Biological Association of the United Kingdom 80, 555Ð556. Villanueva, R., Collins, M.A., Sanchez, P. & Voss, N.A. 2002. Systematics, distribution and biology of the cirrate octopods of the genus Opisthoteuthis (Mollusca, Cephalopoda) in the Atlantic Ocean, with description of two new species. Bulletin of Marine Science 71, 933Ð985. Villanueva, R. & Guerra, A. 1991. Food and prey detection in two deep-sea cephalopods: Opisthoteuthis agassizii and O. vossi (Octopoda: Cirrata). Bulletin of Marine Science 49, 288Ð299. Villanueva, R., Segonzac, M. & Guerra, A. 1997. Locomotion modes of deep-sea cirrate octopods (Cepha- lopoda) based on observations from video recordings on the Mid-Atlantic Ridge. Marine Biology 129, 113Ð122. Voight, J.R. & Grehan, A.J. 2000. Egg brooding by deep-sea octopuses in the North Pacific Ocean. Biological Bulletin (Woods Hole) 198, 94Ð100. Voss, G.L. 1955. The Cephalopoda obtained by the Harvard-Havana expedition off the coast of Cuba in 1938Ð39. Bulletin of Marine Science of the Gulf and Caribbean 5, 81Ð115. Voss, G.L. 1956. A review of the cephalopods of the Gulf of Mexico. Bulletin of Marine Science of the Gulf and Caribbean 6, 1Ð178. Voss, G.L. 1967. The biology and bathymetric distribution of deep-sea cephalopods. Studies in Tropical Oceanography 5, 511Ð535. Voss, G.L. 1982. Grimpoteuthis brunni, a new species of finned octopod (Octopoda: Cirrata) from the southern Pacific. Bulletin of Marine Science 32, 426Ð433. Voss, G.L. 1988a. The biogeography of the deep-sea Octopoda. Malacologia 29, 295Ð307. Voss, G.L. 1988b. Evolution and phylogenetic relationships of deep-sea octopods (Cirrata and Incirrata). In The Mollusca, Volume 12, Paleontology and Neontology of Cephalopoda, M.R. Clarke & E.R. Trueman (eds). San Diego, CA: Academic Press, 253Ð276. Voss, G.L. & Pearcy, W.G. 1990. Deep-water octopods (Mollusca; Cephalopoda) of the northeastern Pacific. Proceedings of the California Academy of Sciences 47, 47Ð94. Warrant, E.J. & Locket, N.A. 2004. Vision in the deep sea. Biological Reviews 79, 671Ð712. Wells, M.J. 1990. Oxygen extraction and jet propulsion in cephalopods. Canadian Journal of Zoology 68, 815Ð824. Wells, M.J. & Clarke, A. 1996. Energetics: the costs of living and reproducing for an individual cephalopod. Philosophical Transactions of the Royal Society of London Series B 351, 1083Ð1104. Xavier, J.C., Rodhouse, P.G., Purves, M.G., Daw, T.M., Arata, J. & Pilling, G.M. 2002. Distribution of cephalopods recorded in the diet of the Patagonian toothfish (Dissostichus eleginoides) around South Georgia. Polar Biology 25, 323Ð330. Young, R.E., Vecchione, M. & Donovan, D.T. 1998. The evolution of coleoid cephalopods and their present biodiversity and ecology. South African Journal of Marine Science 20, 393Ð420.

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Oceanography and Marine Biology: An Annual Review, 2006, 44, 323-429 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis

THE ECOLOGY OF RAFTING IN THE MARINE ENVIRONMENT. III. BIOGEOGRAPHICAL AND EVOLUTIONARY CONSEQUENCES

MARTIN THIEL1,2* & PILAR A. HAYE1,2 1Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile E-mail: [email protected]; Fax: ++ 56 51 209 812 2Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Coquimbo, Chile *Author for correspondence

Abstract Rafting of marine and terrestrial organisms has important ecological, biogeographical and evolutionary implications. Herein the general principles of rafting are described and how they contribute to population connectivity. Rafting dispersal has particular characteristics, which may differ substantially from those of species with planktonic larval dispersal. Dispersal distances achieved via rafting can vary considerably: journeys may be very short or in some cases extremely long, depending on currents and wind. Accumulation of rafts in convergence zones facilitates cohesion of travelling groups, possibly reducing the risk of founder populations being very small. This becomes particularly important over long distances where singular founder events could provoke strong reduction of the genetic variability in the founded population. The frequency of transport affects the degree of connectivity between local populations. Three important rafting routes are distinguished: frequent, intermittent and episodic. Frequent rafting routes are found in bays, lagoons and estuaries, and they are typically facilitated by substrata of biotic origin (seagrass, saltmarsh vegetation, intermediate-sized algae and mangroves). Intermittent rafting routes are found along temperate continental shores where they are facilitated primarily by giant kelps. In the subtropics and the Arctic intermittent rafting routes facilitated by wood are particularly important. Episodic rafting routes, which often cross vast areas of open ocean (biogeographic barriers), are facilitated by volcanic pumice, floating trees and occasionally by giant kelps when these are pushed beyond intermittent routes by strong winds or currents. Dispersal events occur in a highly sporadic manner in this latter category of rafting route, but when they happen, large amounts of floating substrata and rafters may be dispersed simultaneously. Intervals between events can be decades, centuries or even millennia, and consequently populations resulting from these events may be isolated from each other for long time periods. Population connectivity on frequent, intermittent and episodic rafting routes is high, intermediate and low, respectively. Genetic studies support these predictions, and furthermore underline that rafting may contribute to population connectivity over a wide range of geographic scales, from <100 km up to >5000 km. Rafting also has a strong effect on evolutionary processes of the organisms dispersed by this means. It is suggested that local recruitment (consequence of direct development) contributes to enhanced rates of population diver- gence among local populations of common rafters, but occasionally high genetic diversity may result from secondary admixture. Isolation of colonisers after singular episodic rafting events facilitates allopatric speciation. Through these processes rafting dispersal may support local species richness and thus have an influence on local biogeography and biodiversity. Human activities affect rafting connections in the oceans either by reducing or enhancing the possibility of transport and

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landfall. In many cases it cannot be safely decided whether the appearance of a species in a new habitat is due to rafting or to other transport mechanisms, and genetic studies can help to identify the most likely causes. Future field and laboratory studies on the ecology of potential rafters in combination with genetic studies on different spatial and temporal scales will contribute to a better understanding of the mechanisms of rafting dispersal, consideration of which is crucial in devel- oping efficient conservation measures in the marine environment.

Introduction

The existence of the Plagusia tomentosa [=P. chabrus Linnaeus 1758] at the southern extremity of Africa, in New Zealand, and on the Chilian coasts, may perhaps be due to migration, and especially as it is a southern species, and each of these localities is within the subtemperate region. We are not ready however to assert, that such journeys as this range of migration implies are possible. The oceanic currents of this region are in the right direction to carry the species eastward, except that there is no passage into this western current from Cape Horn, through the Lagulhas current, which flows the other way. It appears to be rather a violent assumption, that an individual or more of this species could reach the western current from the coast on which it might have lived; or could have survived the boisterous passage, and finally have had a safe landing on the foreign shore. The distance from New Zealand to South America is five thousand miles, and there is at present not an island between.

Dana (1856) reporting on the geographical distribution of Crustacea

The riddle of Plagusia chabrus still is not resolved. It is well known that this species is widely distributed in the southern oceans, but it is not clear whether the individuals from New Zealand, South America and South Africa indeed represent the same species or not (C. Schubart, personal communication). Most likely it will be necessary to await molecular studies to show whether the populations from those distant regions were separated a long time ago, or whether exchange between them still exists. In case these studies show actual gene flow, Dana (1856) already offered a possible explanation of how this could be achieved over such long distances: “They may cling to any floating log and range the seas wherever the currents drift the rude craft”. While he did not have the insights of post-Darwinian biologists and the tools of modern science, Dana (1856) had already recognised the importance of the interaction between dispersal and allopatric speciation. The questions that fascinated Dana and his contemporaries 150 years ago continue to move scientists today. However, despite the enormous scientific progress since then, dispersal remains an important incognitum to biologists. In particular, marine biologists are faced with the problem that many of the species of interest are difficult or impossible to track during their boisterous journeys in the oceans. Many marine organisms are small, and following them in the vast realms of open water is unfeasible. This is especially true for those species that have planktonic larvae. Yet scientists have managed with admirable effort to follow tiny larvae during their planktonic journey and to obtain reliable estimates of effective dispersal distances (e.g., Young 1986; Stoner 1990, 1992), but only for short- lived larvae (a few hours). For most species with longer-lived larval stages no or only approximate estimates are available. This is even more true for invertebrate species without larval stages. Many of these latter species rely on other dispersal mechanisms (e.g., rafting) but very little is known about the distances they may achieve during these voyages, let alone actual exchange between distant populations. In general, it had been assumed for a long time that the dispersal potential of species with planktonic larvae would be relatively high while that of species without planktonic larvae would be limited. Results that did not coincide with this general perception have increasingly puzzled

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marine biologists during the past 20 years. When Johannesson (1988) found abundant populations of the directly developing gastropod Littorina saxatilis but not of L. littorea, a species with a planktonic larva, on a remote island in the North Atlantic she formulated the ‘Paradox of Rockall’. More recently, Colson & Hughes (2004) observed fast recolonisation of remote sites by another directly developing gastropod, Nucella lapillus, and furthermore they revealed continuous genetic population structure across the British Isles. The authors of these (and other) studies inferred that, in the absence of pelagic larvae, dispersal could be achieved via rafting on floating substrata (Edmands & Potts 1997, Hoskin 1997, Arndt & Smith 1998, De Matthaeis et al. 2000, Collin 2001, Porter et al. 2002, Sponer & Roy 2002, Colson & Hughes 2004, Waters & Roy 2004a, Baratti et al. 2005, Lourie et al. 2005). Indication that rafting dispersal may be important for a wide diversity of species is continuously increasing with evidence coming from small unicellular organisms, invertebrates and even large terrestrial invertebrates (Masó et al. 2003, Waters & Roy 2004a, Glor et al. 2005). Thus, it appears that the wide distribution of some species with direct development is no longer a paradox; dispersal of these species may be much more efficient and common than previously assumed. Rafting can thus transport organisms to distant habitats, but how much exchange is there between populations and what does it depend on? Exchange processes between habitats and populations occur over many different scales in the marine environment (Carr et al. 2003). For example, ecologists recognised early on that high temporal and spatial variability in recruitment intensity often depends on supply and exchange between neighbouring populations. Important trophic fluxes between habitats further underline the fact that many marine systems exchange biomass (and living organisms) with neighbouring systems. With the advent of molecular techniques an increasing number of genetic studies offered important insights into the connectivity (extent to which populations are linked by exchange of propagules, i.e., dispersing eggs, larvae, recruits, juveniles or adults) of local populations of marine organisms. In some cases these studies have revealed high connectivity between distant local populations (e.g., Johnson & Black 1984a,b; Hellberg 1996; Ayre & Hughes 2000; Kyle & Boulding 2000; Lessios et al. 2001; Pfeiler et al. 2005), while in others they have identified almost complete lack of exchange between neighbouring populations (e.g., Ayre & Dufty 1994, McFadden 1997, Ayre & Hughes 2000). Conservation biologists are keenly aware of the fact that population connectivity is a crucial variable when designing networks of marine-protected areas (see Palumbi 2003, Grantham et al. 2003, Baums et al. 2005, Kinlan et al. 2005). The degree of population connectivity depends on (i) the distances between habitats, (ii) the prevalent current patterns, (iii) supply of propagules, (iv) the dispersal capability and (v) the colonisation potential of the organisms under consideration. Dispersal capabilities of marine organ- isms vary substantially depending on their sizes, morphology, behaviour and life histories. Dispersal can be achieved by planktonic larvae or swimming adult stages that are capable of maintaining themselves in the water column, thereby facilitating transport via currents. In this case, dispersal distances are largely determined by currents and by the swimming ability of the respective organisms (either larvae or swimming adults) (e.g., Shanks et al. 2003). Estimates of potential dispersal distances can be obtained by combining current velocities and larval life span for species with planktonic larvae (Siegel et al. 2003, Kinlan et al. 2005). Species without planktonic larvae or with adults that lack efficient swimming capability depend on other dispersal mechanisms, usually aided by a dispersal agent, for example birds (Green & Figuerola 2005), fish (Domaneschi et al. 2002), humans (Wonham & Carlton 2005) or floating substrata (Thiel & Gutow 2005a,b). In general, distances between habitats, currents and propagule supply are the main factors that influence the degree of population connectivity in species with autonomous dispersal stages and those dependent on dispersal agents. However, population connectivity potential differs between these two groups in that the latter additionally depends on the characteristics of the dispersal agent, here floating substrata.

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Transport across inhospitable areas Anthropogenic transfer Crossing biogeographic barriers Immigration to new habitats Range extension Rafting

Reproduction & Dispersal Larvae

Mucus-floating Habitat change Predator escape Swimming Resource exploitation Crawling

0.0001 0.01 1 100 10,000 Distances (km)

Figure 1 Schematic relationship between geographical distance and biologically relevant movements indi- cating the principal dispersal mechanisms on each scale.

A diverse armada of floating objects is continuously underway in the world’s oceans, the most important being macroalgae, wood, volcanic pumice and increasing amounts of plastics (Thiel & Gutow 2005a). These floating objects differ substantially in their suitability for rafting organisms, in particular in food value and longevity. In addition, in most regions the abundance, drift direction and velocity of floating objects depend on unpredictable events (for example storms), thereby introducing additional uncertainty when estimating population connectivity via rafting dispersal. Perhaps it is due to the stochastic nature of rafting dispersal that most recent efforts in estimating population connectivity in the marine realm have focused on organisms with autonomous dispersal stages (Gerber et al. 2005), even though there are many reported cases of organisms without pelagic larval stages, which depend on rafting (or other mechanisms) for dispersal (Thiel & Gutow 2005b). While it is increasingly known and widely accepted among ecologists that rafting dispersal occurs, relatively little is known about its significance in marine (and terrestrial) communities. Organisms are dispersed via diverse mechanisms in the sea (Figure 1). Most of these mechanisms are of great importance at certain life history stages and are most effective over a particular range of distances. For example, walking and crawling may be important on the scale of cm or several m, depending on the size and characteristics of a species. Swimming organisms may move over hundreds of metres up to several kilometres. Planktonic larvae are dispersed over a wide range of distances from a few metres up to hundreds of kilometres. Rafting is effective over similar distances but there is indication that some rafters may be carried over thousands of kilometres, distances rarely achieved by planktonic larvae. Anthropogenic transport of marine organisms (for example through ballast waters) extends over similar distances as rafting. However, unlike rafting dispersal, human activities may carry marine organisms over very large distances, across regions that exceed the physiological limits of many organisms (Carlton & Geller 1993). This can occur when organisms are enclosed in spaces maintaining favourable environmental conditions during transport (ballast water tanks in ships, or coolers for aquaculture purposes). Thus, as a natural process, rafting operates at spatial scales also covered by other dispersal mechanisms in the sea. However, it appears to be particularly effective over distances where other mechanisms lose importance (Figure 1).

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ECOLOGY EVOLUTION

Population biology Food web interactions Biodiversity

Biomass export/import

Resource exploitation

Local population dynamics

Metapopulation dynamics Connectivity

Bottlenecks and Founder effects

Allopatric speciation

frequentintermittent episodic Rafting routes

Rafting distances short intermediate long (<100 km) (<5,000 km)

Figure 2 Schematic relationship between frequency/distance of rafting events/routes and the degree of con- nectivity between local populations. Important ecological and evolutionary processes affected by this relation- ship are also indicated. The shaded area indicates that the number of species and individuals expected to successfully disperse by rafting decreases with increasing rafting distances.

Rafting may transport a wide variety of organisms (Thiel & Gutow 2005b) but this process is only of evolutionary or ecological significance if the journey leads them to sites beyond their neigh- bourhood area and if rafters can disembark and establish in coastal marine or terrestrial habitats. Depending on the frequency and intensity of transport, one can hypothesise that there should be three principal temporal and spatial scales over which rafting acts (Figure 2). Frequency of transport is also related to transport distances since many of the most common floating substrata persist only for limited time periods at the sea surface (non-lignified vascular plants, seagrasses, small algae), while substrata that become available less frequently (large trees, calcareous skeletons, volcanic pumice) have a very high longevity (Thiel & Gutow 2005a). At very high rafting frequencies, organisms utilise rafting to reach resource patches within habitats, and abundant rafting events also facilitate export and import of organisms to and from neighbouring habitats. This will also lead to effective mixing of individuals between resource patches, thereby reducing the probability of deme formation. At intermediate rafting frequencies, rafting events are sufficiently common to permit efficient exchange between and within local populations, affecting the dynamics of metapopulations and local populations. Depending on the frequency and intensity of the connectivity, local popu- lations will display varying degrees of genetic relatedness. At low rafting frequency, dispersal events are so rare that a species (group) that is successfully transported will not experience the arrival of

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additional conspecifics over many generations, allowing for genetic differentiation and eventually even allopatric speciation. It is important to keep in mind that these categories are arbitrary, but that they reflect the three principal temporal and spatial scales over which rafting dispersal operates. In general, it can be hypothesised that at high rafting frequencies, ecological and microevolu- tionary processes should be dominating, while at low rafting frequencies cladogenetic events (e.g., allopatric speciation) will gain importance. Given the fact that rafting frequency depends, among other things, on the availability and longevity of floating substrata, and that not all organisms are adapted to survive for long time periods as rafters, it can furthermore be expected that different taxa are differentially adapted to be dispersed via rafting. For example, few organisms may be able to survive long-lasting journeys, and consequently only a specific subset of organisms may expe- rience long-distance dispersal via rafting permitting colonisation of new habitats. Likewise, only some organisms are capable of using rafts as short-term floats, allowing them to move between local habitats or exploit ephemeral resource patches. In this review, the ecological, biogeographical and evolutionary implications of rafting dispersal in the marine environment will be addressed. The review is concerned with the consequences of rafting on a variety of scales. Based on published case studies, the account will explore whether predictions based on longstanding assumptions of marine dispersal are valid, and if so, for which organisms. Furthermore, future study topics will be suggested, addressing important questions that need to be answered in order to better understand rafting dispersal. Finally, it will be pointed out where, why and how rafting-mediated connectivity needs to be considered in the design of areas protecting coastal marine environments.

Dispersal in the sea General considerations In general, dispersal is what maintains and expands the geographic range of species and as such it determines the degree of genetic connectivity between local populations of a species (Palumbi 2003). Dispersal can be active (autochrony: swimming, crawling) or passive (rafting, human- mediated) and it may be by diffusion from the home range or by long-distance dispersal (also called jump dispersal). Long-distance dispersal (LDD) can be defined relative to some ecologically significant scale that sets the limits of the local population or the mean dispersal distance for the metapopulation (Kinlan et al. 2005). It is important to consider that LDD and the absence of dispersal represent extremes along a dispersal scale continuum (Bradbury & Snelgrove 2001, Mora & Sale 2002, Kinlan & Gaines 2003, Shanks et al. 2003, Kinlan et al. 2005). Both organisms with a planktonic larva and organisms with direct development (brooders) may have high potential for LDD. For brooders, LDD is probably achieved via rafting of non-larval individuals (Highsmith 1985, Jackson 1986, Johannesson 1988, Ó Foighil 1989, Ó Foighil et al. 1999, Helmuth et al. 1994). In the context of the present review, it will be examined under which conditions rafting can be an effective dispersal mechanism resulting in successful LDD and colonisation of new habitats or to the maintenance of population connectivity over time. Many biotic and abiotic factors determine the potential for dispersal of a species, and the effects of these factors are variable among taxonomic groups and localities (Scheltema 1988, Shanks et al. 2003, Kinlan et al. 2005). Effective marine dispersal distances are distributed over a wide continuum of spatial scales (Underwood & Chapman 1996, Bradbury & Snelgrove 2001, Mora & Sale 2002, Kinlan & Gaines 2003, Shanks et al. 2003, Kinlan et al. 2005), and even within a species it may vary at different locations in space and time (Cowen et al. 2003, Sotka et al. 2004). At one extreme of this continuum, populations are considered closed because local recruitment is the result of local propagule production (e.g., Taylor & Hellberg 2003). At the other extreme, open populations are

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broadly connected at larger spatial scales and the arrival of propagules to the population contributes substantially to local recruitment (Caley et al. 1996). Thus, depending on the spatial scale consid- ered, species differ in the extent to which local recruitment depends on local propagule production (Kinlan et al. 2005). Even though most marine systems are thought to be more open than terrestrial systems (Roughgarden et al. 1988, Underwood & Fairweather 1989, Gaines & Bertness 1992, Caley et al. 1996, Carr et al. 2003), there is accumulated evidence from plankton distribution (Grantham 1997), local larval retention (Swearer et al. 1999) and genetic connectivity (Palumbi 2003), among others, that many marine species have restricted dispersal, suggesting that their populations might not be demographically open or that dispersal distances of many marine organisms may be shorter than expected (Jones et al. 1999; Swearer et al. 1999, 2002; Palumbi 2004; Sotka et al. 2004, Baums et al. 2005). On the other hand, there is a growing number of reports of species with a much wider geographic distribution than can be explained by their autonomous dispersal capabilities (Johan- nesson 1989, Castilla & Guiñez 2000). These considerations underline the importance of taking a close look at all aspects of the dispersal behaviour of the species under consideration. For marine organisms, life history traits, habitat and oceanographic conditions are the most important factors affecting their dispersal poten- tial (Mileikovsky 1971, Jablonski 1986, Scheltema 1986, Strathmann 1987, Sponaugle et al. 2002, Grantham et al. 2003, Muñiz-Salazar et al. 2005). Marine communities contain taxa with varying reproductive patterns (Thorson 1950, Levin 1984, Strathmann 1987, Pechenik 1999, Grantham et al. 2003) that are thought to influence their dispersal potential (Mileikovsky 1971, Jablonski 1986). While for many species larval dispersal together with biotic and abiotic factors determines their geographic range (Thorson 1950, Mileikovsky 1971, Strathmann 1974, Jablonski & Lutz 1983, Scheltema 1986, Díaz 1995, Underwood & Chapman 1996, Watts et al. 1998), several observations have supported a more open view of marine dispersal that examines dispersal potential beyond the presence of a larval stage (Levin & Bridges 1995, Palumbi 1995, Ayre & Hughes 2000, Grantham et al. 2003). Larval dispersal is often considered as active dispersal since some larvae are known to have specific active behaviours that enhance the probabilities of either being trans- ported by currents or of being retained in certain regions (Havenhand 1995, Shanks 1995). Larvae, juveniles and adults may accomplish dispersal by active behaviours such as swimming and crawling. For many benthic marine invertebrates, though, these latter mechanisms only account for movement within the local range (local movement) and not for diffusion or LDD. The dispersal mode of marine species may also be passive (such as rafting) and may happen at one or more of the above life stages. Rafting differs from larval dispersal in not (in most cases) being restricted to a particular life stage, and not being limited by the duration of a stage (as it does not depend on it) but rather on external factors such as raft availability, the capability of organisms to persist on the raft during the journey and colonisation success (Thiel & Gutow 2005b). Even though there is a general lack of direct evidence for rafting dispersal occurring in benthic marine invertebrates (but see Worcester 1994), there has been increasing awareness that rafting might be an important dispersal mechanism that plays a significant role in determining the geographic range of distribution of many species (Sterrer 1973; Johannesson 1988; Ó Foighil 1989; Ó Foighil et al. 1999; Castilla & Guiñez 2000; Sponer & Roy 2002; Waters & Roy 2003, 2004a; de Queiroz 2005; Kinlan et al. 2005). This is also supported by the fact that many species with direct development have wider geographic distributions than congeners with a planktonic larval stage (e.g., Johannesson 1988, Ó Foighil 1989).

Rafting dispersal Many organisms (even those with pelagic larvae) can potentially accomplish connectivity among localities through rafting. Species that usually inhabit benthic coastal habitats are often found on

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ice Pum

Duration of Wood rafting journey

Macroalgae clonal

internal Seag rass ms eder direct osit fe n Dep

Detritus feeder Sexual syste

Grazer opment Suspension feeder sexual Fertilizatio /Predator ex ger ternal Scaven Devel pelagi c

Figure 3 Schematic relationship between feeding and reproductive biology of rafters and duration of rafting journeys. The number of rafting species decreases with length of the journey and only selected groups achieve very long journeys. Main substrata and their relative importance are also indicated.

rafts. Based on an extensive review, it has been argued that rafting is very common in certain regions and that some organisms are well adapted for rafting (Thiel & Gutow 2005b). The rafting voyage is a selective process that favours travellers with certain adaptations. Organisms need to maintain themselves on the raft, feed (depending on the length of the voyage), grow and reproduce. The most important selective pressure that rafters experience during the voyage depends on the floating substrata (Figure 3). These not only differ in their availability but also in their quality as a raft for associated organisms (Thiel & Gutow 2005a). Substrata of biotic origin (floating animal and plant material) have a high food value for organisms but their longevity generally is limited (e.g., Hobday 2000a), while substrata of abiotic origin (volcanic pumice and plastics) have no food value but float for long time periods, often >1 yr (Jokiel 1989, Bryan et al. 2004, Barnes & Milner 2005). Since raft longevity in combination with current velocities and/or prevailing winds determine dispersal distances, organisms that live on biotic substrata have a lower dispersal potential than organisms that can settle and survive on abiotic substrata. In general, suspension feeders abound among the rafting fauna because they do not depend on the raft for nourishment. On biotic substrata a high diversity of grazers and predators/scavengers is also frequently found. Differences in species composition between rafts may also be due to competitive interactions that are commonly reported from rafting communities (Thiel & Gutow 2005b). Interspecific competition may lead to the eradication of inferior species (Gutow & Franke 2003). Dominant competitors capable of proliferating during rafting journeys will slowly but steadily monopolise resources on a raft (Stevens et al. 1996, Tsikhon-Lukanina et al. 2001). Rafting communities that are underway for long time periods may therefore be impoverished in species. If organisms reproduce during the voyage, individuals that reach new habitats may be offspring of

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original travellers. Intraspecific competition, strong selective processes and genetic drift may thus lead to proliferation of particular lineages within a species during long-lasting rafting journeys. Successful dispersal not only depends on the transport direction and velocity of floating items, but also on their total abundance in a particular region. In contrast to organisms that are dispersing in the water column (larvae), rafting organisms are being dispersed in a two-dimensional space (sea surface). Additionally, floating items are not homogeneously or randomly distributed on the sea surface, but rather clumped due to accumulation in convergence zones. Occasionally strong wind and waves may disperse floating items, but during calm weather they will be accumulated in convergence zones again. This facilitates interactions (positive: reproduction and protection; neg- ative: competition and predation) among rafters from different floating items. If many floating items are underway in the same current system, mobile organisms may switch between rafts to avoid drowning on deteriorating rafts, escape from dominant competitors or predators, or associate with conspecifics for the purpose of reproduction. A comparatively large proportion of successful rafters are hermaphrodites or proliferate asex- ually (Thiel & Gutow 2005b). There are also many gonochoric and sexually reproducing species with a very short planktonic larval stage or which lack a planktonic larva. The latter species produce fully developed offspring that may recruit directly on the maternal raft, thereby allowing the persistence of a species during prolonged journeys (Figure 3). Initially, any organism that can hold onto a floating substratum may be dispersed over short distances, but LDD is only achieved by species capable of feeding and reproducing during the journey. In consequence, suspension feeders and organisms with local recruitment are favoured for LDD via rafting. In summary, the quality of floating substrata exerts a strong selection on the pool of potential rafting organisms, and selective pressures increase during prolonged journeys (Figure 3). These processes (selection, local recruit- ment, inbreeding and genetic drift) may also have important consequences for the genetic structure of rafting demes.

Colonisation and establishment of local populations When dense assemblages of floating items are transported together in nearshore convergence zones, there is a high probability that many rafting conspecifics will get ashore simultaneously. Clearly, arrival of many floating items with an armada of conspecific rafters increases the probability of successful reproduction in new habitats. Additionally, the number of conspecifics that arrive simul- taneously has important effects on the potential persistence of a new population, because if too few individuals colonise, founder effects can be drastic and the genetic variability may be imperilled. This, of course, is less important if rafting is frequent, and multiple colonisers arrive during repeated arrival events. Since dispersal stages of many marine organisms have only limited autonomous swimming capabilities, they must be delivered directly to benthic habitats in order to settle successfully. Larvae of many marine invertebrates have evolved diverse behaviours that ensure delivery to suitable habitats (see, e.g., contributions in McEdward 1995). For example, many species exhibit vertical migrations in the water column in order to enter favourable currents to reach open water for larval development or to return to benthic habitats for settlement (Young 1995). Floating substrata remain at the water surface where they are at the mercy of wind and surface currents. Thus, in contrast to many species with pelagic larvae, rafting organisms have little or no chance of influencing the direction of transport during the journey. However, being limited to a two-dimensional space also presents advantages because it facilitates cohesion of propagule clouds (see above). Once arriving near potential new habitats, rafting organisms face the problem of moving from the raft to benthic habitats. While final stages of many planktonic larvae are adapted to actively select settlement substratum, most rafting organisms have little opportunity for selection. In many

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cases, arrival appears to be a chance process. When reaching coastal habitats, sessile organisms may either grow over onto benthic substrata (Worcester 1994), be scraped off by hard-bottom substrata (Jokiel 1989), or they may release spores or larvae (Keough & Chernoff 1987). Semisessile and mobile organisms such as gastropods, crustaceans and echinoderms, can also actively abandon rafts and reattach or crawl over to benthic substrata (Thiel & Gutow 2005b). It is during arrival that floating substrata exert a final selective influence on rafting organisms. Complex floating items (seagrass shoots, macroalgae, trees) may entangle in benthic habitats such as rocky shores, seagrass beds, kelp or mangrove forests. It can be hypothesised that mobile organisms that raft on these substrata, have higher probabilities of going ashore successfully than other organisms. Following arrival in a new habitat, successful colonisation can occur only if species reproduce effectively. Here the reproductive biology of an organism gains extraordinary importance. In particular when few individuals arrive in new habitats, similar reproductive traits as those selected for during long rafting journeys are advantageous (i.e., capability of establishing local populations). Species with asexual reproduction or self-fertilising hermaphrodites are favoured since they do not depend on the presence of conspecifics — at least in some taxa the consequences of reduced genetic diversity do not appear to impede establishment (e.g., Jackson 1986). In species that require cross- fertilisation, the presence and abundance of mating partners is crucial. At low densities of potential mates, the species with internal fertilisation may be favoured over external fertilisers, which usually form aggregations or spawn synchronously in order to achieve high concentrations of gametes. When few conspecifics are present, gamete concentrations may be too low for successful fertilisation in broadcast spawners. In species with internal fertilisation, efficient searching or courtship behav- iours may facilitate association of mating partners in benthic habitats, thereby ensuring successful fertilisation. Once fertilisation has happened, the developmental mode of species furthermore becomes critical. Williams & Reid (2004) discussed this for littorinid snails: “establishment of a self-sustaining population at such a distance [1400 km] must be very much rarer, because the founding population should be of sufficient density to ensure that mates can be found and to overcome the dilution of the resulting progeny during their own pelagic phase”. It is here that direct developers are at an advantage, because in many cases their offspring are retained in close vicinity, facilitating coherence of the founder population and future reproduction. In particular, when propagules are transported over long distances and few individuals arrive in new habitats, rafting organisms have a higher probability of successfully colonising than species with planktonic larvae because in the former reproductive traits have been selected that favour colonisation (Figure 4). The positive relationship between raft size and number of travellers (Thiel & Gutow 2005b) may not only have effects on the persistence of a species on the raft (reproduction during the journey) but also on the colonisation success after arrival (reproduction in new habitats). Single travellers (on small rafts) may have a lower likelihood of finding mates, impeding successful establishment in new habitats, and even if they reproduce and form small populations, their sustainability may be limited due to the fitness consequences resulting from strong founder effects. If competent and sufficient individuals arrive, rafting may lead to founding of a new population (Johannesson 1988, Castilla & Guiñez 2000, Colson & Hughes 2004) or be a means that contributes to connectivity among populations (Grosberg & Cunningham 2001, Hellberg et al. 2002, Palumbi 2003), but its importance in population maintenance remains unexplored (Martel & Chia 1991, Grantham et al. 2003). Dispersal sets a tradeoff between the probability of extinction and local adaptation (Jablonski & Lutz 1983) that is likely to impact the evolution of dispersal patterns (Grantham et al. 2003). The reproductive traits that are selected during prolonged rafting journeys and at establishment in new coastal habitats (asexual reproduction, internal fertilisation and direct development) will have important consequences for local population structure. While these traits favour cohesion and sus- tainability of founding groups, they also result in a high degree of inbreeding and genetic relatedness.

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planktonic Colonisation success

rafting

short intermediate long Dispersal distances

Rafting routes frequentintermediate episodic

Figure 4 Schematic relationship between rafting routes (distances) and the colonisation success of rafting organisms, compared with that of planktonic organisms. At very long dispersal distances, rafting organisms have a higher likelihood of successful colonisation (due to their reproductive biology) than planktonic organisms.

Rafters achieving LDD may be pre-adapted to establish local populations, but these will be at a high risk of extinction. Rafting can thus be considered a selective process that has strong implications for the biogeography and evolution of marine species, in particular for the many marine benthic invertebrate species that lack a planktonic dispersal stage and thus depend on rafting for dispersal. Since rafting organisms have no influence on the direction and velocity of transport they may frequently be carried to marginal or even inhospitable environments. A patch of floating algae (originally growing in hard-bottom habitats) thrown onto a sandy beach is a vivid example for the latter (inset in Figure 5). It can be expected that the probabilities of reaching suitable habitats depend on transport distances (Figure 5). Rafts travelling over short distances may have a high likelihood of intercepting habitat patches similar to those where travellers went onboard. For example, most seagrass shoots or mangroves detached from their native habitat in a bay or estuary may be retained in adjacent seagrass or mangrove patches. In contrast, rafts carried out of a bay and travelling over farther distances will have a low probability of reconnecting with habitats sharing the characteristics of their sites of origin. The distributional range of marine organisms depends on a variety of factors, the most important being the availability of suitable habitat (including abiotic factors such as temperature, salinity, light and oxygen), food supply and biotic interactions. Outside the physiological limits of a species, metabolic costs of individuals are too high for these species to persist or to reproduce successfully (Pörtner 2002). Establishment or maintenance of viable populations within the ecological range of a species is only possible if production and survival of propagules is assured. When organisms are

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MARTIN THIEL & PILAR A. HAYE Colonisation success Successful arrival in suitable habitats frequent intermittent episodic Rafting routes

Figure 5 Schematic relationship between rafting routes and the probability of successful arrival in suitable habitats. Between categories of rafting routes the probabilities decrease in a stepwise manner. For example, organisms travelling on frequent rafting routes within bays or estuaries may have a high probability of reconnecting with suitable habitats within bays, but once flushed out to the outer coast, the probability of returning to a bay with suitable habitats diminishes substantially. Insert shows an individual of the floating kelp Durvillaea antarctica, commonly growing on exposed hard bottoms, washed up on a sandy beach (reaching unsuitable habitat for most species that live and raft on this macroalga).

carried into regions that are close or even outside their ecological range their reproductive potential may be strongly reduced (due to physiological constraints and low densities), and local populations may not be self-sustainable, endangering their persistence. Individuals may temporarily survive and even reproduce successfully, but local populations might rapidly disappear, for example during seasonal changes. Local populations may be exposed to recurrent colonisation and extinction events (Marko 2005). This appears to be the case in the obligate rafter Idotea metallica, which regularly is transported into the North Sea, but apparently is eradicated in this region during harsh winter conditions (Gutow & Franke 2001). Castilla & Guiñez (2000) discussed the case of a local population of the gastropod species Concholepas concholepas (native to the Pacific coast of South America) in South Africa, which established and became extinct during the Pliocene/Holocene. They suggested that this population might have arrived via rafting, but reasons for extinction are not known. Since the environmental conditions in the Benguela Current are similar to those in the Humboldt Current region, extinction may not have been due to physiological reasons but was possibly caused by limited reproductive potential of a small local population or by the negative consequences of a strong founder effect.

Metapopulation structure and processes Floating substrata can transport rafting organisms to new habitats and may allow their immigration to other populations of conspecifics. The frequency of rafting events along a route affects the

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possibility of successful colonisation or the degree of connectivity between local populations. Colonisation and connectivity achieved via these rafting routes maintains uni- or bidirectional migration among local populations. This kind of population structure (i.e., with many local popu- lations that interact through gene flow) is referred to as a metapopulation. Grimm et al. (2003) identified the characteristics of a metapopulation as: (a) a system of local populations having their own dynamics, (b) some local populations are so small that they face risk of extinction, (c) local populations interact via propagules and (d) dispersers are able to establish new local populations in empty patches. Local populations occupy an area that reflects the mobility and habitat require- ments of the organisms (Camus & Lima 2002). Many marine benthic invertebrates, in particular those dispersed by rafting, seem to fit a metapopulation model, particularly because of the frag- mented nature of marine benthic environments. Strong gene flow among populations prevents differentiation of local populations by mixing gene pools and preventing local effects of genetic drift. Conversely, restricted gene flow among local populations reduces the effective population size, leading to decreased genetic variability within local populations. The effects of genetic drift and localised selection are stronger for populations with restricted gene flow. The gene flow patterns of marine metapopulations are not straightforward. Most populations are not characterised by constant and bidirectional gene flow among all local populations, suggesting that more complex patterns of dispersal are imposed by the intrinsic characteristics of marine environments and species. The direction of exchange between local populations will have important consequences for the dynamics of the metapopulation of a species. Cook & Crisp (2005) emphasised, albeit not in the context of rafting, that increasing strength in directionality of dispersal increases the frequency of multiple dispersal events in one direction relative to the other. In the case of rafting, the main source population of a rafting species may be a single interbreeding population that changes over time and produces enough propagules for their own persistence as well as for export to other sink areas. Over time there may be multiple colonisations in a sink area due to settlement and establishment of propagules that reach the area by directional rafting on an intermittent or frequent rafting route. Metapopulation structure changes with the number of local populations and the degree and direction of gene flow among them. Different degrees of connectivity lead to variable genetic differentiation between the populations of a species that are connected by a rafting route, and thus differing metapopulation structures (see how metapopulation dynamics span across all rafting frequencies in Figure 2). It has been argued that a single migrant per generation is sufficient to prevent genetic differentiation of populations (Wright 1951). When levels of gene flow are lower, populations may share many alleles due to common ancestry, but their frequencies will change due to genetic drift and local selective pressures, leading populations to genetically differentiate over time. Gene flow is a force that acts against the development of new lineages as it prevents differentiation and speciation. Consequently, if popu- lations are isolated, for example after being established from a single rafting colonisation event, they will accumulate genetic differences over time. In contrast, populations that are connected by frequent rafting events (and thus maintaining high gene flow with source population) will tend toward homogenisation over time. Just as the theory of island biogeography of MacArthur & Wilson (1967) predicts that species diversity is a balance between arrival of species through migration and the loss through extinction, the genetic diversity of a population is a balance between the arrival of new alleles (gene flow) and the loss of alleles due to genetic drift (island model of genetic diversity of Wright 1940; see also Vellend 2003). Genetic drift is mostly the product of the random sampling of gametes that occurs in every generation and causes a change in the allelic frequencies of the population from one generation to the next. Genetic drift usually has no detectable effect on populations that are large enough such that the sampling of gametes does not change the frequency of alleles in the population. However, if populations are small, like the ones found on a raft or those originating

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from rafting-mediated colonisation events, genetic drift may cause perceptible changes in allele frequencies or cause some alleles to completely disappear and the population will lose genetic variation. Two highly documented genetic drift events are bottlenecks and founder effects. These two events have identical genetic architecture as they result from evolution in small populations, but their originating mechanisms differ. Bottlenecks are drastic reductions in population size (and genetic variability), triggered by a change in the biotic or abiotic conditions, while founder effects refer to the result of the founding of a new population by only a few individuals. Because the founding population is small (for example, the colonisers that arrive on a raft), it contains only part of the genetic diversity present in the source population. The population starts with the little genetic diversity present in the founder population, and over time may gain new genetic diversity. If the new diversity arises solely by mutation, then the differences between source and founded populations will be detectable with genetic markers. But if the new diversity were to arise by continual migration from the source population, then it would not be detectable, especially if gene flow is high. An episodic rafting route (less frequent and with long-distance trajectories) may result in a founder effect if few individuals of a species colonise the arrival area. Frequent and intermittent routes have relatively high connectivity between localities, decreasing the probability of a single founder effect and leading to multiple ones that, depending on the amount of source populations, will have varying effects on the genetic structure of the populations. Chambers et al. (1998) explained that low levels of gene flow in combination with direct development cause small-scale founder effects in subpopulations that increase the overall genetic diversity of the whole meta- population. This latter scenario of genetic structure may prove common in brooders that disperse via rafting. Connectivity is a measure of the strength of the connections between local populations. It depends mainly on the dispersal of individuals (carriers of genes) and in particular on the number and origin of immigrants to local populations, and has important consequences for the genetic structure of metapopulations. Gene flow estimates are quantifications of the connections in terms of amounts of individuals that migrate (and effectively reproduce) in each generation. Gene flow is often reported as Nm, a measure that is based on both effective population size (N) and migration rate (m). Depending on the levels of relatedness among populations, inferences can be made about the realised dispersal of propagules over time. Genetic data allow for inferences of real rather than potential dispersal distances (Hunt 1993). Realised dispersal is determined by many parameters, including mode of development, oceanographic conditions, history of populations and others that may influence the pattern of migration among populations. For many species, rafting must be assumed to increase their dispersal potential (even enabling them to achieve LDD) and the con- nectivity between local populations.

Dispersal patterns Gene flow patterns among local populations may resemble more or less the proposed models of dispersal. The basic dispersal model that is the underlying model assumed in many commonly used analytical tools is the island model of Wright (1931), in which several local populations are connected by random migration from a common pool, and mating is more frequent within than between populations. In this case, the metapopulation will eventually reach genetic drift/migration equilibrium. This model is appropriate for two-population cases or for equally spaced oceanic islands, but may not accurately describe the structure of marine species distributed along a coastline (Hellberg et al. 2002). Slatkin (1977) proposed the propagule- and migrant-pool models. The propagule-pool model is like the island model as there is only one population that serves as the source of migrants. In the migrant-pool model, instead, migration is random and gene flow occurs

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among all local populations. An alternative metapopulation model is the stepping-stone model (Kimura & Weiss 1964, Maruyama & Kimura 1980) that has been increasingly applied to examine the structure of marine metapopulations (Slatkin 1993, Hellberg et al. 2002). Under this model, population differentiation increases with increasing geographic distance between local populations. The resulting pattern is known as isolation by distance (IBD) (Wright 1943, Slatkin 1993). In the stepping-stone model, gene flow occurs among local neighbours in a continuously distributed population (i.e., no extreme LDD). For a population to be continuously distributed the habitat has to be continuous and a series of conditions need to be met (e.g., oceanographic conditions do not isolate populations, selection does not interfere with the pattern, populations are not at genetic equilibrium). Many studies have concluded that marine populations conform with IBD patterns, while other studies have found that other more general metapopulation models are more accurate. Even though many marine populations show a pattern of IBD, high dispersal potential (e.g., through larvae or rafting) sometimes leads to genetic homogenisation of populations or to a population differentiation not following a distance pattern. Rafting may have a strong effect on the local dynamics by providing a means of propagule input to a local population. Additionally, it may have a strong impact on the migration patterns among local populations, especially for organisms that lack other means of dispersal. The frequency of dispersal opportunities over variable spatial scales leads to different dispersal scenarios. At a micro- to mesogeographic scale (i.e., within a patch of habitat, for example, a bay) frequent rafting opportunities are more common and could lead to genetic homogenisation if exchange is abundant and follows a migrant-pool model. Less frequent or restricted gene flow among local subpopulations within the patch of habitat will lead to genetic differentiation at a microspatial scale, leading to high population fragmentation and extinction risk. At a broader geographic scale, local populations may be more or less connected by a rafting route (e.g., with populations outside of a bay). If propagules come from one or few source populations, small founder effects will accelerate genetic drift and reduce the genetic variation within and among populations (Harrison & Hastings 1996, but see Wares et al. 2005). Instead, if propagules come from many sources, small founder effects may increase local genetic diversity. Thus, the genetic structure will depend on both the local gene flow dynamics and on the connectivity with populations outside of the patch. The genetic differentiation of populations from different habitat patches may follow contrasting patterns depending on the kind of rafting route and its characteristics. For example, a rafting route with regular supply of floating substrata (= dispersal opportunities) following a unidirectional current could lead to a pattern of IBD along the coast. However, this is only likely if the rafting route links a series of local populations that receive propagules only from up-current populations. The stretch over which populations may display IBD will depend on the local hydrography. If the current direction is not strongly defined (i.e., is bi- or multidirectional) or when it is not temporally stable, so that it sometimes reverses, there will be no IBD pattern and instead the population may present a migrant-pool model of colonisation. There may be areas where currents converge and redirect offshore posing a gene-flow barrier to many rafters. At either side of the barrier the populations may be structured following an IBD pattern, while being strongly differentiated from the populations from the other side of the barrier. The absence of an IBD pattern of differentiation could be associated with medium-distance or LDD dispersal events, either through larvae or in the case of direct developers, through rafting (e.g., Colson & Hughes 2004). However, both organisms with direct and planktonic larval development can be dispersed over long distances by rafting (see below). Some studies have shown that dispersal is directional among populations of marine species (Wares et al. 2001, Waters & Roy 2004a). Oceanographic and climatic conditions are probably the main factors determining the directionality of a rafting route in the ocean (Gaines et al. 2003,

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Muñiz-Salazar et al. 2005). Cook & Crisp (2005) state that successful LDD depends on a number of variables that have a “strong directional component” such as the dispersal ability of the organisms or their propagules, favourable environmental conditions for dispersal (currents, location of raft sources) and a suitable habitat for establishment. If currents are persistent, transport will be highly directional. Dispersal of organisms (gene flow) and oceanic currents match closely in these regions, enabling the persistence of downcurrent populations through metapopulation effects. If a close match is found for species without a pelagic dispersal stage, rafting is often inferred as the most likely dispersal mechanism. An example for this are local populations of terrestrial lizards Anolis sagrei on the Bahama Islands, where these lizards are supposed to be dispersed over-water after hurricane events (Calsbeek & Smith 2003): “We found directionality of gene flow that is congruent in all cases with the prevailing direction of ocean currents, including the exceptional case in which currents adjacent to Florida drive gene flow south from Bimini to Andros Islands”. Similar direc- tional source-sink connections are hypothesised for many other organisms and regions. For the North Atlantic, Wares & Cunningham (2001) inferred that recent (re)colonisation of areas in the northwest Atlantic has occurred from source populations in the northeast Atlantic. They based this suggestion on the higher genetic diversity in European compared with North American populations, making it most likely that the direction of colonisation was from east to west. In the southern oceans, many authors have suggested that transport of propagules follows the direction of the West Wind Drift (e.g., Ó Foighil et al. 1999, Donald et al. 2005). Waters & Roy 2004a observed para- phyletic lineages of a brooding seastar (Patiriella exigua) in South Africa while they found mono- phyletic lineages in the Australian region (i.e., in down-current direction in the West Wind Drift). Based on these results, they inferred that the populations in the Australian region had developed from a singular dispersal event, most likely via rafting. It is not always easy to identify the direction of connectivity between local populations, mostly because methodologies like F-statistics do not account for directionality (for alternative approach see Wares et al. 2001). Knowledge of the prevailing current regime in a region may also help to interpret phylogenetic trees by aiding in the identification of the gene flow direction (see e.g., Carranza et al. 2000).

Rafting dispersal pathways Rafting, as most other dispersal mechanisms, occurs over a wide variety of temporal and spatial scales. Terrestrial biogeographers commonly distinguish three types of dispersal pathways that connect two (or more) localities: corridor, filter and sweepstake routes. A corridor is a route that is defined as part of the same landmass with a similar habitat to the two localities being connected, and that allows most organisms to cross it. A filter or filter bridge is an interconnecting region that has more restrictive habitat characteristics than a corridor, and only some organisms are capable of crossing it. Finally, a sweepstakes route has completely different habitat characteristics than the areas it is connecting such that dispersal events are rare across the barrier, most of them being considered to be accidental. The biota found on a sweepstakes route is considered disharmonic, as it is not a representative sample of the ecologically integrated and balanced biota that is being connected by the route (Cox & Moore, 1993). Because the three types of route imply different probabilities of successful dispersal, they result in different degrees of similarity (community and lineage composition) between the biota connected by the route. In the terrestrial environment, corridors are common dispersal routes, while sweepstakes routes, as their name indicates, are rare events or events that rarely result in successful dispersal. In the sea, the distinction between corridors, filter and sweepstakes routes is also applicable but harder to envision than for terrestrial environments. Herein, three main types of rafting routes (frequent, intermittent and episodic — see also Figure 2) are distinguished, analogous to the

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dispersal routes described for terrestrial environments. Rafting routes can be classified according to the frequency of rafting events, which depend on environmental conditions favouring availability of floating items, their persistence and the length of the journey. Just as there is a continuum in populations from being demographically open to closed, there is also a continuum in rafting dispersal potential. High frequency rafting routes connecting two or more areas, typically of distances <100 km, will be referred to herein as frequent rafting routes. On these frequent rafting routes, floating substrata are available in large quantities and any organism capable of holding onto the substratum can migrate via rafting. Rafting distances and duration usually are short, and thus there is no need for organisms to feed during transport, similar to the situation in terrestrial corridor routes. Voyages on intermittent rafting routes extend over greater distances (100Ð5000 km) and last longer, requiring that travellers feed or at least use body reserves during transport. This means that the pool of species capable of travelling on these intermittent routes is more eclectic. Organisms unable to fulfil their metabolic requirements or to survive conditions on a raft will not usually be transported on intermittent rafting routes. Dispersal on frequent and intermittent rafting routes commonly occurs on substrata derived from the natural habitats of rafting organisms, thus resem- bling a dispersal corridor in terrestrial environments. However, the duration of the voyage and the need to satisfy metabolic requirements on intermittent rafting routes produces a filter effect, only permitting successful dispersal of certain organisms. If rafting is extremely rare, so that it does not represent a permanent or semipermanent connection between populations or regions, it will be considered an episodic rafting route. Episodic routes result from random and independent events that for a short ecological timescale provide abundant floating substrata, establishing a route of rafting dispersal that allows colonisation of faraway sites. These routes are expected to occur at distances >5000 km and because rafting episodes are so rare it could be predicted that in many cases it results in allopatric speciation. Examples will be presented from the literature in order to elucidate the processes acting on frequent, intermittent and episodic rafting routes and how these affect ecological, biogeographic and evolutionary consequences. These rafting routes have strong implications for the exchange of rafters and the consequences vary from trophic dynamics (frequent routes), to metapopulations with more or less connectivity among local populations (frequent and intermittent routes) and allopatric speciation (episodic routes) (Figure 2).

The rafting routes Floating substrata are most abundant in those regions where they are supplied and their routes of dispersion are driven by oceanic currents and wind. There exist important regional differences in abundance and supply of floating substrata, and consequently, rafting opportunities and dynamics are also variable. The three rafting routes identified above can also be distinguished according to the temporal and spatial scales over which rafting opportunities arise (Thiel & Gutow 2005a). Frequent routes are found where substrata are supplied in great quantities and continuously (or at least every year) with a high degree of predictability. They occur in bays, lagoons and estuaries along coastlines of many regions of the world. On intermittent rafting routes, substrata are available on a regular basis, but supply and dispersal scale can vary on an annual basis. Episodic rafting routes only receive a very sporadic input of floating substrata (e.g., following volcanic eruptions, hurricanes or tsunamis). Instantaneous local supply, regardless of the frequency of occurrence (frequent, intermittent or episodic), can be very high on all three rafting routes. The substratum characteristics also vary in accordance with their frequency of supply. Inter- estingly, there is a tendency that many of the frequently supplied substrata have a limited longevity. For example, seagrass shoots (occurring on frequent rafting routes) usually float for a few days, and the maximum longevity recorded at the sea surface is 2 weeks (Harwell & Orth 2002). At the

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other extreme, volcanic pumice is only available very sporadically, but may float for several years (Frick & Kent 1984, Jokiel & Cox 2003, Bryan et al. 2004). These characteristics, in particular supply and longevity, affect the consequences of rafting, in particular the number of rafters and the potential dispersal distances. Herein, for each rafting route specific predictions will be made with respect to their ecological and evolutionary consequences, and it will then be examined whether or not there is support for these predictions. There are, however, also unpredictable events (storms or intense floods) that change the relatively stable direction and frequency of a dispersal route. These events may interrupt frequent rafting routes (disconnecting areas) or push floating substrata to areas off the trodden paths (episodic rafting route). It should thus always be kept in mind that there is overlap between the three rafting routes. Many of the dispersal mechanisms and particular floating substrata that will be discussed below are most relevant at one scale of dispersal (i.e., rafting route, but they may also operate across rafting routes). In general, most of the various natural floating substrata appear to fit one of these three scales relatively well (see also below). However, anthropogenic substrata (plastics and tar lumps) are present and potentially important on all three rafting routes. Plastics have caused substantial concern as potential rafting substrata for three main reasons: i) they are ubiquitous and continuously introduced to the oceans, ii) the amounts of plastics have been increasing dramatically during the last century and iii) they have a high longevity, possibly facilitating LDD (Winston et al. 1997, Barnes 2002, Barnes & Milner 2005). These anthropogenic substrata led to new, artificial, rafting routes that are a relatively new phenomenon. Due to their different characteristics and potential impact, these artificial rafting routes will be briefly dealt with in a separate subsection, outlining the temporal and spatial scales covered by these routes.

Frequent natural rafting routes Continuous supply of floating substrata on frequent rafting routes

In some areas of the world oceans, large quantities of floating materials are continuously supplied, offering abundant possibilities for organisms to be dispersed via rafting. This situation is the case in temperate coastal ecosystems, where every spring and summer large quantities of plants and algae are produced in estuaries, coastal lagoons and shallow waters along the continental shelf. These floating substrata are dispersed by tidal currents and, when carried into offshore waters, by coastal currents. Most of these substrata (seagrasses, marshgrasses, macroalgae, mangrove wood) are already colonised by a diverse biota at the moment of going afloat. Within estuaries, bays or lagoons, these substrata and associated rafters are transported throughout the system leading to efficient exchange between neighbouring habitats. Similarly efficient exchange might also be expected around island shores. If rafting frequencies are very high, some organisms may even utilise this process to exploit resource patches within these ecosystems. Furthermore, at very high frequency of production and transport of floating items, biomass of floating substrata (and associated organisms) can be exported to neighbouring habitats within bays. These exchanges result in very efficient trophic and genetic connections between habitats and local populations. Multiple examples are known for rafting transport on floating plants and macroalgae via these common rafting routes. Here, examples for biomass transport, resource exploitation, and exchange of rafting colonisers within estuaries, lagoons and bays are presented. Since in these systems floating substrata are most abundantly available, it could be expected that frequent rafting routes occur therein. When a raft is carried out of these systems, the probability of reconnecting to suitable habitats decreases (see also Figure 5).

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Frequent rafting route; no exchange out of bay Frequent rafting route; high exchange out of bay

A B

High within-connectivity: lower genetic diversity High within-and between-connectivity: higher genetic diversity

Figure 6 Scheme showing the two extreme situations on frequent rafting routes and the expected genetic consequences. (A) shows a frequent rafting route in a bay without any out-of-bay connection, while (B) shows a frequent rafting route with relatively strong out-of-bay connections. Genetic diversity is expected to be lower in (A) showing a closed metapopulation than in (B) representing an open metapopulation, due to the genetic input from external sources in (B).

On most frequent rafting routes, it is expected that connectivity is high within estuaries, bays or lagoons. This will lead to panmictic populations within these systems. Genetic diversity will depend on the size of populations within bay systems and on the degree of exchange with popu- lations from other bays. If within-bay populations are virtually isolated and receive no immigrants, their genetic diversity is expected to be lower than in situations where bay populations occasionally obtain input from outside sources (Figure 6).

Examples of frequent rafting routes

Seagrass beds During their annual growth season, seagrasses produce large quantities of above- ground biomass (Alongi 1998), parts of which are continuously sloughed off (e.g., Flindt et al. 2004). Large proportions of the above-ground production are prone to be exported from the system (Cebrian & Duarte 2001). Depending on the buoyancy of detached blades and shoots, export occurs via the sea surface or via bedload transport (see also Alongi 1998). The transport mechanism (sea surface or bedload) will have strong effects on export distances, and it can be expected that positively buoyant species are transported substantially farther than negatively buoyant species. Consequently, positively buoyant seagrasses may reach neighbouring seagrass patches and thereby contribute to the connectivity between habitats and populations. However, surprisingly little information is available about the buoyancy properties of seagrasses. There are anecdotal reports that some species are negatively buoyant (Thalassia testudinum, Flindt et al. 2004; Posidonia oceanica, J. Cebrian, personal communication), while others are known to be positively buoyant (Zostera marina, Bach et al. 1986, Harwell & Orth 2002; Syringodium filiforme, Flindt et al. 2004; S. isoetifolium, Alongi 1998; Cymodocea nodosa, J. Cebrian personal communication; Heterozostera tasmanica, personal observation). In particular blades and shoots of Zostera marina are highly buoyant and may persist for >2 weeks at the sea surface when they can be dispersed considerable distances within bay systems (Harwell & Orth 2002). Senescent blades of the seagrass Z. marina are frequently sloughed off during the growth season, and they are widely transported by currents within an enclosed lagoon (Flindt et al. 2004). Those authors observed that the vast majority of detached blades of Z. marina floated at or near the sea surface (Figure 7). They suggested that this transport represents an important component

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Figure 7 Dynamics on frequent rafting routes supported by seagrass as rafting substrata. (A) Detached blades or shoots float to the sea surface and are dispersed by currents. (B) Export of parts of Zostera sp. at different heights above the bottom; upper height represents sea surface; after Flindt et al. (2004). (C) Annual pattern of biomass export (in ash-free dry weight AFDW) from a Z. marina bed in North Carolina; after Bach et al. (1986). (D) Density of epiphytes on blades of Z. marina in a Danish estuary; Five blades (1Ð5) are shown with different segments starting at the base (a) and ending at the tip of the blade; after Borum (1985).

of biomass transfer within lagoonal ecosystems. Bach et al. (1986) revealed that export from a seagrass bed in an enclosed estuary reached levels of >20% of the monthly production. They estimated seasonal transport of blades along the sea surface and found that export is highest during late summer, but there may be high interannual variation in production and export (Figure 7). They also reported that floating blades still contained epiphytes, but since their study focused on trophic dynamics, they did not mention the fate of these (and other organisms). It is well known that old seagrass blades usually are overgrown by a diverse biota including algae, hydrozoans, bryozoans, ascidians, and others (e.g., Borum 1985, Borowitzka & Lethbridge 1989) (Figure 7). Since epibionts may constitute a large proportion of total biomass (Borowitzka & Lethbridge 1989), substantial export of associated organisms may occur together with export of floating seagrass blades. These can be deposited in close vicinity of the seagrass beds or at far distances offshore, depending on the buoyancy and longevity of detached seagrass blades or shoots. High production and export of above-ground biomass along the sea surface will also lead to efficient dispersal of seagrasses and associated organisms within estuaries, lagoons or coastal bays. Evidence for high connectivity between local seagrass populations within bays or lagoons comes from genetic studies of seagrasses themselves. No significant genetic differentiation between populations

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of Z. marina was found at distances of 54 km in the European Wadden Sea and 33 km in the Baltic Sea (Reusch 2002). Similarly, Olsen et al. (2004) found little genetic variation in populations of Z. marina within neighbouring bay systems, and they suggested that this might be due to efficient exchange via rafting (see also Figure 8). Examining floating shoots, Reusch (2002) suggested that at least 10% of the shoots arriving at a seagrass bed were immigrants from other populations — to the present authors’ knowledge this is the only study investigating the genetic relatedness between benthic and rafting populations. For Z. noltii, Coyer et al. (2004) revealed that “substantial gene flow among intertidal and subtidal populations occurs at the level of tens of km”, and they emphasised the importance of dispersal of floating shoots along the sea surface. Serving as floating substrata for other organisms, seagrasses may also facilitate the connectivity between local populations of common seagrass inhabitants. Indication for the relatively short distances covered by floating seagrasses (i.e., within bay systems) comes from a study by Collin (2001) who, referring to a species of Crepidula, discussed that “the high levels of population structure in C. convexa suggest that rafting on seagrass could only be a significant cause of among- population gene flow over short distances”. Direct evidence of dispersal on floating seagrass comes from a study by Worcester (1994) who observed that colonial ascidians Botrylloides sp. rafting on blades of Zostera marina are efficiently dispersed within an estuary. The high frequency of rafting and successful colonisation observed by the author suggests that benthic populations of this species in that bay are not limited by dispersal. Similar effects can be expected in other estuarine, lagoonal or bay systems with abundant seagrass populations. Boström & Bonsdorff (2000) observed high individual turnover of species inhabiting a seagrass bed in the northern Baltic Sea and they suggested moving algae (albeit benthic drift algae) as a potential dispersal vector (see also Brooks & Bell 2001). Thus, it can be hypothesised that eventual genetic differences between subpopulations within local populations of many seagrass epibionts are not a consequence of restricted dispersal, but rather of environmental factors. Salt marshes Intertidal salt marshes have a high primary production, generating plant biomass of >1 kg dry weight (DW) mÐ2 yÐ1 (Bouchard & Lefeuvre 2000). Toward the end of the growth season, above-ground parts of many saltmarsh plants die back, and during storms or spring tides, these may be transported away (Figure 9). Export from salt marshes into nearby coastal habitats has been well known for decades (Teal 1962) and a large proportion of this export may be via the sea surface. It has been reported that dead or living parts of some saltmarsh plants are positively buoyant (Thiel & Gutow 2005b) but it is not well known how long these can persist at the sea surface. Dalby (1963) reported that seed-containing fragments of Salicornia pusilla may float for up to 3 months. Whole branches with fruits of the coastal plant Crambe maritima were found on beaches of the North Sea and it has been estimated that these may have come from source populations at least 7 km upcurrent (Cadée 2005). Most of these floating materials may be washed up in the flotsam in close vicinity of their sites of origin within the salt marsh: “Macrodetritus moved by tides from the production site in the low marsh accumulate in drift lines in the middle and high marshes, which act as sinks of organic matter” (Bouchard & Lefeuvre 2000). However, some of this dead organic matter may also be carried greater distances (Bouchard et al. 1998). Bart & Hartman (2003) suggested that during storm and hurricane events entire patches of saltmarsh vegetation can be eroded. Positively buoyant peat patches containing rhizomes may then be carried to other neigh- bouring salt marshes in a bay or estuary. Connectivity between populations of saltmarsh plants themselves is achieved via floating propagules of either vegetative (roots and rhizomes, e.g., Proffitt et al. 2003, Travis et al. 2004) or sexual origin (seeds and fruits, e.g., Huiskes et al. 1995). Potential dispersal distances of roots and rhizomes are not well known, but fruits and seeds have been reported to disperse at least over distances of 60 km via tidal currents (Koutstaal et al. 1987). Few studies are available on rafting

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Figure 8 Genetic relationships between populations of Zostera noltii from W Iberia. (A) Study sites along the Atlantic coast of Portugal and S Spain. (B) Neighbour-joining tree based on pairwise Reynold’s distances (using microsatellites). The northern populations and the southern populations are monophyletic and form sister clades. (C) Isolation by distance based on pairwise comparisons of genetic and geographic distance among eight populations. IBD pattern among all populations was significant (Mantel test, p < 0.016), but no significant IBD was found for the southern populations (p < 0.549), suggesting a high degree of connectivity between them. Figures modified after Diekmann et al. (2005).

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Figure 9 Dynamics on frequent rafting routes supported by saltmarsh vegetation. (A) Detached shoots, senescent plants or patches with rhizomes floating to the sea surface and that are dispersed by currents. (B) Plants of Spartina sp. during high tide with entangled seagrass shoots. (C) Annual pattern of biomass export from a salt marsh on the French Atlantic coast; after Bouchard & Lefeuvre (2000). (D) Proportion of macrofaunal groups found in larval collectors (L.C.) and on floating rafts in a restored salt marsh in California; after Moseman et al. (2004).

transport of organisms associated with saltmarsh plants, but it is known that gastropods climb up the stem of marsh grasses and diverse insects feed on and reproduce in saltmarsh plants. A diverse fauna inhabits the rhizome mats of salt marshes, and several recent studies indicate that saltmarsh plants and algae serve as dispersal vectors for these organisms within bay systems. In a restored salt marsh, Moseman et al. (2004) observed diverse organisms, including polychaetes, turbellarians, molluscs, crustaceans and insects arriving on algal rafts (Figure 9), and they concluded that rafting transport contributes large numbers of colonisers to salt marshes. Levin & Talley (2002) made similar observations at another restoration site: all initial colonisers arrived via rafting (on sea- grasses, saltmarsh vegetation and macroalgae), and most of them included macrofauna with mobile adults and without planktonic larval stages (for example the amphipods Hyale frequens, Pontogeneia rostrata and Jassa falcata, the tanaid Leptochelia dubia, the gastropods Barleeia subtenuis and Cerithidea californica, and several annelids). Those authors also noticed abundant rafting dispersal in a neighbouring undisturbed salt marsh, emphasising that “rafting of macrofauna is also common in undisturbed settings”. They concluded that the high rates of recolonisation are partly made possible by the high degree of connectivity between saltmarsh patches within bay systems.

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Figure 10 (A) Adult of the beetle Agapanthia villosoviridescens (photo courtesy of Per H. Olsen). (B) Dry weight of the larvae of A. villosoviridescens collected in flotsam and in standing saltmarsh plants at different sites in the estuary; the large size of larvae found in down-estuary flotsam suggest up-estuary sources. (C) Cumulative emergence of larvae of A. villosoviridescens from flotsam, and from standing plants at the presumed site of origin (Soeftinge) and another site (Ellewoutsdijk); the similarity of emergence-pattern between down-estuary flotsam and up-estuary plants suggests up-estuary sources. (D) Sites in the Wester- schelde estuary where larvae were collected in flotsam and in standing saltmarsh vegetation. Figures (BÐD) modified after Hemminga et al. (1990).

Wilhelmsen (1999) revealed a high degree of connectivity between local populations of Littorina saxatilis and she suggested that dispersal may occur via floating marsh grass or seagrass shoots. Strong evidence for efficient dispersal of insects via saltmarsh vegetation comes from a study by Hemminga et al. (1990). Those authors collected large numbers of viable larvae of the beetle (Agapanthia villosoviridescens) in dead stems of Aster tripolium that had accumulated in flotsam of the Schelde Estuary (NL). Based on morphological evidence and of accompanying saltmarsh vegetation in flotsam, the authors concluded that these larvae had rafted to the collecting sites from upstream source populations (Figure 10). This transport mechanism appears to be important since adults of this beetle “rarely seem to fly”. Hemminga et al. (1990) also observed other species in the hollow stems and they suggested that “tidal transport of insects [via rafting] between isolated estuarine salt marshes is an actual process and probably is more common than is apparent until now”. Many insects overwinter as larval or pupal stages in senescent saltmarsh vegetation (Denno 1977, Denno et al. 1981), which during winter storms may become detached and dispersed with tidal currents, thereby contributing to connectivity between subpopulations within estuaries. In this

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context it appears interesting that Peterson et al. (2001) revealed strong gene flow between local populations in a predominantly flightless plant hopper (Tumidagena minuta), which lives under the layer of plant debris accumulating in the high salt marsh. Possibly, dispersal of this species is achieved when detritus in the upper marsh goes afloat during strong winter storms. Shallow-water macroalgal belt The intertidal belt and shallow subtidal waters of temperate regions in both hemispheres are colonised by lush populations of intermediate-sized macroalgae. Many of these algae possess gas-filled structures providing positive buoyancy to these species (e.g., Ascophyllum spp., Fucus spp., Sargassum spp.) (Thiel & Gutow 2005a). Thalli or whole individuals of these algae are frequently detached due to grazer-activity or wave-induced failure and may then float away. There are abundant reports of these algae encountered on sandy beaches (e.g., Stegenga & Mol 1983), yet surprisingly little is known about their arrival on rocky shores or in other subtidal habitats. Also, no data on quantity and direction of export fluxes of these intermediate- sized algae are available. However, based on anecdotal accounts it appears safe to assume that much of the ungrazed annual production of the buoyant algae in these algal belts will be exported via the sea surface to surrounding areas or regions. As a result of their intermediate longevity these algae may be efficiently moved around within estuaries, lagoons or bays, but they may also be frequently exported from these systems (see also below). Dense patches of these algae have been reported from large marine systems such as the North Sea (Franke et al. 1999, Gutow & Franke 2003, Vandendriessche et al. 2006), the Irish Sea (Davenport & Rees 1993), the British Channel and the Baltic Sea (M. Thiel, personal observations), the Gulf of Maine (Locke & Corey 1989), the Strait of Juan de Fuca (Shaffer et al. 1995), and the Japan Sea (Segawa et al. 1964). Many species of these intermediate-sized algae are colonised by a diverse biota including mobile and sessile species (Mukai 1971, Norton & Benson 1983, Kitching 1987, Ingólfsson 1998, Fre- driksen et al. 2005, Buschbaum et al. 2006). Mobile grazers such as isopods from the genus Idotea are commonly found on floating Fucus vesiculosus and Ascophyllum nodosum (Gutow 2003). In laboratory experiments, it could be shown that Idotea baltica rapidly consumes its floating sub- stratum (Gutow & Franke 2003). Since this species is restricted to coastal areas, the author suggested that, after exploiting a patch of floating algae, these highly mobile isopods (see Orav-Kotta & Kotta 2004) may return to benthic populations or search for new floating patches (Gutow & Franke 2003). Thus, I. baltica appears to be capable of exploiting floating patches as food resources. Similar relationships can be expected for other mobile crustaceans such as palaemonid or hippolytid shrimp. Common decomposers of detached algae such as amphipods from the genus Orchestia or isopods from the genus Ligia have also been found on floating algae in estuaries (Wildish 1970). Juvenile stages of many fish species associate with floating algae, where they forage on associated rafters (e.g., Shaffer et al. 1995, Ingólfsson & Kristjánsson 2002). In addition to mobile species, many sessile organisms are found on these algae, including spirorbid polychaetes, hydrozoans, bryozoans and ascidians. Due to the small size of the holdfasts of these intermediate-sized algae, most organisms grow on their blades. The high abundance and intermediate longevity of these floating algae facilitate not only temporary exploitation of these ephemeral habitats, but also efficient dispersal of associated organisms within bays, and occasionally even between bays along the outer coast. Some indication for connectivity among populations, both within and between bays, on rela- tively small spatial scales comes from a study by Engelen et al. (2001) on floating algae. They suggested some connectivity between bays via rafting individuals but they also noted local differ- entiation (Figure 11). For two common epibionts on fucoid algae, rafting has also been inferred to contribute to population connectivity (for the nudibranch Adalaria proxima Ð Todd et al. 1998 and for the bryozoan Alcyonidium gelatinosum Ð Porter et al. 2002). Similarly, the gastropod Littorina saxatilis may also be dispersed on floating fucoids (Johannesson & Warmoes 1990).

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Figure 11 Genetic population structure of Sargassum polyceratium on the Caribbean island of Curaçao. (A) Neighbour-joining diagrams for pairwise genetic distances (using RAPD data) of populations from shallow water sites — two distinct clusters, one in the north and one in the south can be distinguished. (B) Typical current and wind patterns around Curaçao. Figures modified after Engelen et al. (2001).

Mangrove forests Mangroves produce a wide variety of detritus that is positively buoyant, includ- ing wood (Si et al. 2000) and leaves (e.g., Wehrtmann & Dittel 1990). While substantial research has been conducted on the fate of fallen leaves in mangrove forests (Lee 1999, Jennerjahn & Ittekkot 2002, Alongi et al. 2004), surprisingly little information is available on the amounts and charac- teristics of fallen wood: “Despite considerable research interest in the ecology of mangrove forests, there is a surprising paucity of information concerning the role of wood in these systems” (Romero et al. 2005). Leaves and small twigs become available every year with seasonal peaks at the end of the summer/fall (Mfilinge et al. 2005), while large pieces of wood only are supplied to the aquatic system following episodic events, such as hurricanes (Krauss et al. 2005). A large proportion of this detritus is exported to nearby coastal habitats (Odum & Heald 1975) as has been demonstrated by numerous studies on trophic links in mangrove systems (Marchand et al. 2003, Alongi et al. 2004), but little information is available about the transport mechanisms. Fallen leaves and twigs of many species are positively buoyant (see, e.g., photograph in Stieglitz & Ridd 2001) and they may locally be very abundant: “Remarkable concentrations of floating debris, especially of man- grove leaves, were at several tidal fronts” (Wehrtmann & Dittel 1990). In general, it appears safe to assume that leaves of most species have only a limited survival time (days) at the sea surface

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(see Kathiresan & Bingham 2001). Seeds of mangroves may have higher longevities, i.e., several weeks (Steinke & Ward 2003). No information is available about the buoyancy of mangrove wood and its longevity at the sea surface. This makes it difficult to estimate potential transport distances within estuaries and bays. Since mangrove leaves, twigs and seeds are not in contact with sea water before entering the rafting circuit, they may serve as rafts for terrestrial organisms. It is considered likely that terrestrial arthropods or their developmental stages, which are inquilines in leaves, leaf-stems, twigs or seeds (Feller & Mathis 1997), are dispersed within and between neighbouring mangrove forests, similar to what has been shown by Hemminga et al. (1990) for insects in saltmarsh vegetation (see above). Feller & McKee (1999) mentioned for the wood-boring beetle Elaphidion mimeticum, that “dis- persal of this species from the mainland to the offshore mangrove islands probably occurred via rafting in wood”. Even though aerial parts of mangroves are only of limited value as dispersal vector to marine organisms, some highly mobile ephemeral rafters such as megalopae or juveniles of decapod crustaceans, and also peracarid crustaceans, are known to utilise them as transport vehicles (Wehrtmann & Dittel 1990). Parts of mangroves that are exposed to sea water before going afloat may be more important as substratum for potential marine rafters. For example, submerged aerial roots of the red mangrove Rhizophora mangle are colonised by a diverse biota, mostly composed of sessile suspension feeders (Bingham & Young 1995). These organisms may be transported to new sites, when roots break off. This is facilitated by boring organisms, such as teredinid bivalves or sphaeromatid isopods. In particular, isopod borers have been held responsible for breakage of mangrove roots, and subsequent loss of mangrove trees (Rehm & Humm 1973, Svavarsson et al. 2002). Thus, with their boring activity, isopods may indirectly facilitate dispersal of the biota growing on/in aerial roots of mangroves. Indeed, Brooks (2004) suggested that Sphaeroma terebrans may be dispersed with the roots of Rhizophora mangle. Detached roots may float for up to 2 months (Estevez 1978, cited in Brooks 2004) and thus they may be efficiently dispersed by tidal currents within mangrove forests and lagoons. There is some indication that population connectivity of Sphaeroma terebrans within enclosed bays is high. Baratti et al. (2005) observed little genetic variation among individuals collected within each of four sites in Kenya (two sites), Tanzania and Florida, but they revealed substantial differences between sites (Figure 12). They also reported a limited degree of connectivity between the East African populations, and they suggested occasional rafting dispersal with floating mangrove wood. Reid (2002) also mentioned that littorinid gastropods that inhabit mangrove fringes may be dispersed via rafting (possibly on floating wood). Local populations of boring isopods and other root biota appear not to be dispersal-limited, and their distribution within bays and lagoons may rather be influenced by abiotic factors such as temperature, salinity, tidal level or seston load (Brooks 2004).

Dispersal dynamics on frequent rafting routes

Supply of floating substrata in seagrass beds, salt marshes, macroalgal belts and in mangroves is highly predictable. In some of these environments, substrata are supplied continuously, but with some seasonal variation in abundance and size of floating items. Most of these substrata have a limited survival time at the sea surface (days), but occasionally they may float for several weeks. Longevity of substrata appears sufficient to guarantee efficient dispersal within estuaries, lagoons and bays. In these systems, organisms that already grow on these substrata at the moment of detachment or that are capable of holding onto them may become efficiently dispersed. Since many of the habitats discussed above intercept the sea surface at some time during the tidal cycle or generate layers with reduced flow above them (Dame et al. 2000), they are also very efficient in retaining floating substrata. Thus, rafting dispersal may be an important component of the population dynamics of

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Figure 12 Dynamics on frequent rafting routes supported by mangroves. (A) Detached roots, branches or leaves float at the sea surface and are dispersed by currents. (B) Dense meshwork of aerial roots of the red mangrove Rhizophora mangle (photo courtesy of Ingo Wehrtmann, Universidad de Costa Rica, Costa Rica). (C) Global distribution of the isopod Sphaeroma terebrans, which excavates burrows in aerial roots of R. mangle, and map of study sites along the coast of E Africa. (D) Haplotype minimum spanning network of partial sequence of mitochondrial cytochrome oxidase I gene from different populations of S. terebrans, size of ovals (haplotypes) and squares (haplotype with highest outgroup probability) represent the frequency of haplotypes; after Baratti et al. (2005).

organisms living in these habitats. Colonisation of habitat patches may proceed rapidly and via multiple immigration events. In dense subpopulations, emigration events may commonly occur, resulting in rapid spreading of individuals from local populations within estuaries, lagoons and bays, permitting efficient exploitation of resources. The realised geographic distribution of these species within bays will thus depend on environmental factors (both biotic and abiotic), rather than on dispersal supply as long as source populations persist within bays or estuaries (see also Wildish 1970). If subpopulations are effectively connected within a bay, but without input from local popula- tions in adjacent bays, loss of genetic diversity could be expected (see Figure 6). Some indication for this comes from a study by Hoagland (1985) who observed absence of rare alleles in a small introduced population of the gastropod Crepidula fornicata in southern England. When input from neighbouring populations occurs, genetic diversity may increase. Dupont et al. (2003) suggested that jump-dispersal (in that case mediated by human transfer) between local populations in neigh- bouring bays may be responsible for the high genetic diversity observed in French populations.

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This indirectly confirms the expectation of high genetic diversity in local populations of rafters on frequent rafting routes that occasionally receive inputs from external populations (see Figure 6). Based on the high predictability of rafting opportunities, it can be hypothesised that some species may have evolved particular morphological and behavioural adaptations, allowing them to exploit the opportunities offered by these substrata. Mobile species able to cling efficiently to floating substrata and to swim rapidly in search of new rafts or benthic habitats appear to be pre- adapted to exploit opportunities for rafting dispersal. Seagrass- and algal-dwelling isopods from the genera Cleantis, Erichsonella and Idotea, amphipods and hippolytid shrimp seem to be the most likely candidates. They are frequently found on floating seagrass blades (M. Thiel, personal observation), but presently it is not known whether these are accidental rafters or whether, under certain conditions, some individuals actively seek out floating blades in order to be transported to other parts of a seagrass bed or even to neighbouring habitat patches. Occasionally floating items may also be flushed out of estuaries or bays. Baratti et al. (2005) suggested that strong ebbing currents could eject floating mangrove parts into coastal waters, where they may then be transported over greater distances. Snyder & Gooch (1973) mentioned that (rafting) “snails [Littorina saxatilis] may occasionally be swept offshore during violent storms and be deposited at new sites”. Hemminga et al. (1990) also remarked that saltmarsh vegetation may occasionally leave estuaries. Once carried out of estuaries, lagoons or bay systems into coastal offshore waters, the probability of successful transport to suitable habitats will decrease substan- tially, because in addition to estuarine shores (seagrasses, salt marshes, macroalgal belt, mangrove forests), many of these floating substrata may end up on inhospitable shores (sandy beaches, exposed rocky shores, etc.). Dispersal dynamics of floating substrata from frequent rafting routes that are carried into offshore waters are expected to be more similar to those on intermittent rafting routes. Local populations of organisms rafting on intermediate-sized algae and on floating mangrove debris may thus exhibit connectivity that is characteristic of the frequent rafting routes within bays, but the metapopulation connectivity of these species outside of bays may resemble that typical for organisms dispersed on intermittent rafting routes.

Intermittent natural rafting routes Regular supply of floating substrata on intermittent rafting routes

As already outlined in the previous section there may exist substantial overlap between frequent and intermittent routes. The main difference between them is the spatial scale at which they occur. While frequent rafting routes occur within bays or adjacent or continuous patches of habitat, intermittent routes connect different bays or non-adjacent patches of habitat. Since intermittent routes encompass a longer voyage, they present a more selective filter for species, and thus, for many species the likelihood of successful rafting may be lower than on frequent rafting routes. In coastal offshore waters, floating substrata may be available on a regular basis, but abundance and floating direction can vary substantially between years. Substrata are supplied from coastal sources (e.g., kelp forests or rivers). These floating substrata are dispersed within alongshore coastal currents or with major oceanic currents. Strong winds may also influence the floating direction and velocity of these substrata (Harrold & Lisin 1989, Johansen 1999). In the case of giant kelps, these are already inhabited by a wide variety of species before becoming detached, while wood may or may not be colonised when entering offshore waters, depending on its origin and residence time in nearshore coastal waters. Both substrata have intermediate longevities, and can thus travel over intermediate distances throughout biogeographic regions. In addition to the giant kelps, interme- diate-sized macroalgae are available on a regular basis in coastal waters, and these can also transport organisms within offshore currents (see above). Many observations of these substrata in coastal

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currents and in the open ocean are available (for summary see Thiel & Gutow 2005a), but surpris- ingly little is known about the local populations connected via these substrata. Given that floating substrata are common on intermittent rafting routes, it can be predicted that these routes may lead to high-to-intermediate levels of population connectivity. Since distances connected by intermittent routes are relatively large (100Ð5000 km), not all local populations will be continuously connected via this rafting route. Small local populations may be temporarily isolated, possibly resulting in founder effects. Also, as a consequence of comparatively large distances over which intermittent rafting routes are effective, IBD may increasingly gain in impor- tance if hydrographic conditions regularly result in the same rafting trajectory. Under these condi- tions, the relatedness of neighbouring local populations will depend to a high degree on current velocity and directions. Stepping-stone dispersal is expected to be a predominant pattern on inter- mittent rafting routes that have a fixed route. This usually leads to colonisation of neighbouring local populations, and thus, distant local populations may only be connected via intermediate local populations (Figure 13). However, since floating substrata on intermittent rafting routes have a

ABIntermittent rafting route; alongshore convergent currents Intermittent rafting route; alongshore divergent currents

Intermediate connectivity: Disrupted IBD Intermediate connectivity: Disrupted IBD

CDIntermittent rafting route; alongshore directional currents Intermittent rafting route; alongshore directional current

Intermediate connectivity: Stepping-stone with IBD Intermediate connectivity: Leapfrog dispersal, no IBD

Figure 13 Scheme showing four possible scenarios on intermittent rafting routes and the expected genetic consequences. (A) shows an intermittent rafting route with convergent currents, while (B) shows a route with divergent currents; in both cases the alongshore populations are not expected to show an IBD pattern because not all local populations are connected by currents. (C) shows an intermittent rafting route with consistent alongshore currents resulting in local populations being connected in a stepping-stone manner and in an IBD pattern of genetic differentiation. (D) shows an intermittent rafting route with consistent alongshore currents where rafters may occasionally be transported over long distances jumping over adjacent local populations, which results in lack of IBD.

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relatively high longevity, gene flow in an alongshore direction may not occur in a stepping-stone fashion (or other dispersal/colonisation mechanisms that may ultimately lead to IBD), but rather in a leapfrog fashion where propagules may leap over immediately neighbouring populations and immigrate into distant populations (Figure 13). In these situations, the pattern of genetic structure of the metapopulation should not be IBD. It is important to characterise this specific form of jump- dispersal, because a particular pattern in genetic population structure might result from leapfrog dispersal, namely that distant populations are more similar than adjacent local populations. Leapfrog dispersal may occur at all scales, because there exists a high variability in individual dispersal distances among rafters. Genetic diversity of many species connected via intermittent rafting routes can be expected to be structured as a metapopulation with varying degrees of connectivity among local populations. Local populations will be more or less both temporarily isolated and connected, such that in some cases gene flow obscures the effects of genetic drift (either in the form of bottlenecks or founder effects), which would be reflected in a low genetic differentiation among local populations. At the other extreme, intermittent routes may sometimes act as a strong filter that results in a lower probability of successful colonisation by rafters, but that is still frequent enough to prevent speci- ation. In these cases, genetic differentiation among local populations will be higher.

Examples of intermittent rafting routes

Kelp forests In temperate regions of the Pacific and of the Southern Ocean, giant kelps grow between ca latitudes 30û and 60û in both hemispheres (Steneck et al. 2002). These kelp forests contain many species that are positively buoyant thanks to gas-filled structures. Detachment of these kelps may be caused by strong wave action (Dayton & Tegner 1984), by high grazer activity (e.g., Tegner et al. 1995), or a combination of both (Barrales & Lobban 1975). Following detachment, kelp with floating structures rise to the sea surface (Kingsford & Choat 1985, Kingsford 1992) where they are transported with major currents or pushed by prevailing winds (Harrold & Lisin 1989). Some authors reported that the abundances of floating kelp increased during late summer/ early fall (e.g., Kingsford 1992), while other studies revealed no clear seasonal trend (Hobday 2000b). Kelp forests grow in nearshore coastal habitats, and consequently detached individuals may be exported immediately onto nearby beaches where they constitute an important subsidy to the community of sandy beach detritivores (Orr et al. 2005). Kelp species with limited buoyancy or those that have lost buoyancy due to degradation processes may also sink to the sea floor, where they accumulate in submarine canyons constituting an important food source for benthic organisms (Vetter & Dayton 1999). However, abundant reports of floating kelps at far distances from the nearest source populations also indicate that they can potentially travel substantial distances while afloat (Helmuth et al. 1994, Kingsford 1995, Hobday 2000b, Smith 2002, Macaya et al. 2005). During offshore voyages, these kelps may carry a diverse community of associated organisms, which, upon landfall, may colonise benthic habitats. Large kelp from the genera Macrocystis, Nereocystis, Pelagophycus and Durvillaea possess a large and structurally complex holdfast, which is inhabited by a wide diversity of organisms (e.g., Ojeda & Santelices 1984, Smith & Simpson 1995, Adami & Gordillo 1999, Thiel & Vásquez 2000). Depending on their biology and on the structure of the holdfast, these organisms may persist in the holdfast after detachment. For example, many inhabitants of holdfasts of Macrocystis pyrifera survived for several months in detached holdfasts (Edgar 1987, Vásquez 1993). Connectivity between neighbouring kelp forests is hypothesised to be high. Some indication for this comes from genetic studies on positively buoyant kelp species. For the elk kelp Pelagophycus porra, Miller et al. (2000) revealed that individuals from several Channel Islands off southern California were too similar to represent different species, but they observed a trend of isolation.

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Figure 14 Dynamics on intermittent rafting routes supported by giant kelps. (A) Detached blades, branches or whole individuals float at the sea surface and are dispersed by currents. (B) Floating giant kelp Macrocystis pyrifera along the SE Pacific coast of Chile. (C) Phylogram based on nuclear ITS2 sequences of populations of M. pyrifera, indicating the close relationship of populations from the southern and northern hemisphere; after Coyer et al. (2001).

Interestingly, in a subsequent ‘distance network analysis’ some individuals from different islands clustered together, and even though they observed floating sporophytes, the authors did not mention rafting dispersal as a potential explanation. Using rDNA, Coyer et al. (2001) examined the genetic relatedness among four putative species of Macrocystis (Figure 14), and their results led them to suggest that “Macrocystis may be a monospecific genus (M. pyrifera)”. They furthermore noted high “intra-individual variability” in the samples from the northern hemisphere (in particular those from the Channel Islands). Inferring rafting dispersal of fertile sporophytes, they hypothesised that “southern genotypes ‘hybridize’ with northern genotypes in intermediate areas such as Santa Catalina Island” (Coyer et al. 2001). This scenario would fit the hypothesised gene flow on regular rafting routes with alongshore convergent currents (Figure 13). Another indication of efficient dispersal via floating kelps comes from the wide geographic distribution of some common kelp inhabitants. Despite lacking a pelagic dispersal stage, the kelp- boring isopod Limnoria chilensis is found in kelp holdfasts extending over a wide geographic range of >4000 km between 20 and 55ûS (Thiel 2003a). Other kelp inhabitants with direct development also have wide geographic distributions (Knight-Jones & Knight-Jones 1984, Helmuth et al. 1994). This evidence for rafting dispersal admittedly is circumstantial, and it is emphasised that future studies on the population connectivity of organisms associated with giant kelp are highly desirable. Intermediate-sized algae (Ascophyllum spp., Fucus spp., Sargassum spp.) are also frequently found in coastal currents (Thiel & Gutow 2005a), which they may have reached after detachment from sheltered bays or from outer-coast rocky shores. These algae can also contribute to population

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connectivity within these systems via effective transport of organisms without planktonic larval stages (e.g., Littorina sitkana, Kyle & Boulding 2000; Amphipholis squamata, Sponer & Roy 2002; Nucella lapillus, Colson & Hughes 2004). The relatively high abundance of floating giant kelp in temperate coastal currents, and their intermediate longevity of several months (Thiel & Gutow 2005a), suggest that these are efficient dispersal vectors within biogeographic regions. Recolonisation of disturbed patches may proceed relatively slowly over several years. In particular toward the limits of the distributional ranges, where extinctions can occur relatively frequently, impoverished genetic diversity can be expected. Floating trees Rivers regularly transport large amounts of floating wood to the sea. In the northern hemisphere, north of ca 60°N, this occurs every year in the spring following snow melt (Maser & Sedell 1994, Johansen 1999). At low latitudes, around the equator, wood becomes available on a less regular basis, with relatively high interannual variation in abundances (Solana-Sansores 2001, Castro et al. 2002). If floating wood is immediately pushed into offshore waters, colonisation by marine organisms will occur during the journey (i.e., in the pelagic environment without direct contact with benthic communities). Wood may also be retained in or close to benthic nearshore communities (e.g., in salt marshes, kelp forests or in mangrove systems), and during this time become colonised by common coastal organisms. While wood may serve as the dispersal vehicle for many different marine organisms, its utility for terrestrial organisms is relatively limited. Only species which are not directly exposed to saltwater (e.g., in self-excavated burrows), or which resist immersion in saltwater (e.g., dormant stages), may survive extensive trips on floating wood. After reaching offshore waters, floating wood is presumed to follow a similar fate as kelp rafts. A large proportion of the total pool of floating wood may be thrown onto beaches during onshore storms, while the other fraction will sink to the sea floor where they sustain a diverse community of wood- boring organisms (Distel et al. 2000). There are surprisingly few studies on population connectivity via floating wood, despite the fact that this substratum is relatively abundant in some regions. In the Arctic Ocean, the distribution of some coastal plant species is assumed to be the result of seed dispersal via rafting (Johansen & Hytteborn 2001) (Figure 15). Baratti et al. (2005) inferred limited exchange between local bay populations of the boring isopod Sphaeroma terebrans along the outer East African coast (see Figure 12). They suggested that isopod-bearing roots may occasionally be flushed out of bays into offshore waters. Lapègue et al. (2002) demonstrated close genetic relationships between mangrove oysters from West Africa and eastern South America and they suggested rafting (possibly on mangrove wood?) (Figure 15). In the Caribbean, there is an indication that population connectivity between island population of lizards may be achieved via rafting (Calsbeek & Smith 2003). Wood may be the primary rafting substratum for lizards as underlined by a direct observation of a group of iguanas that arrived on the Caribbean island Anguilla on a tree-raft (Censky et al. 1998). Insects were found on driftwood stranded on sandy beaches (Wheeler 1916) or floating in the sea (Heatwole & Levins 1972). Several other authors had suggested wood as dispersal substratum connecting insect populations of island groups in archipelagos and between islands off continental coasts (Abe 1984, Niedbala 1998, Coulson et al. 2002). Most of these observations are from subtropical and tropical areas, underlining the importance of floating wood as connecting vector in these regions.

Dispersal dynamics on intermittent rafting routes

While floating items (kelp and wood) can be underway in large quantities on intermittent rafting routes, the strength of the connectivity between local populations in general is lower than on frequent routes, primarily because transport distances are farther and local populations are more dispersed, diminishing the probability of landfall in suitable habitats. Nevertheless, fast recolonisation

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Figure 15 Intermittent rafting routes supported by floating trees. (A) Distribution pattern of Potentilla stip- ularis from Arctic coasts and predominant current patterns in the Arctic Ocean; modified after Johansen & Hytteborn (2001). (B) Distribution of 16S mtDNA haplotypes of mangrove oysters from W Africa and eastern S America and predominant current patterns in the S Atlantic; modified after Lapègue et al. (2002).

of unpopulated areas (Colson & Hughes 2004), and high genetic relatedness among distant local populations of some species, show that rafting dispersal on these intermittent rafting routes can be effective. Gene flow can be directional when alongshore currents are highly persistent, but there are also apparent examples of gene flow in variable directions. Dispersal via rafting often seems not to proceed in a stepping-stone fashion, commonly resulting in lack of IBD. A pattern of leapfrog migration, where travelling individuals are passing adjacent local populations and reach distant locations, appears to be a recurrent observation on intermittent rafting routes, irrespective of the floating substratum. The first example for this was found in one of the earliest studies on the genetic

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Figure 16 Relationships between local populations of an intertidal gastropod and a saltmarsh plant, assumed to being dispersed along intermittent rafting routes. (A) Sampling sites of local populations of the gastropod Nucella lapillus in SW England, and genetic cluster membership (based on microsatellites) of individuals collected at each site; the two most distant populations (1 and 10) show strongest similarities; modified after Colson & Hughes (2004). (B) Sampling sites of Elymus athericus from salt marshes on the SE coasts of the

North Sea, and pairwise FST (based on microsatellites) plotted against geographic distance showing IBD pattern for the sampled populations; the local population from Helmsand (HS) is as closely related to a distant population (Sch) as to two adjacent populations (WH and SNK); modified after Bockelmann et al. (2003).

population structure of a marine invertebrate, the intertidal snail Littorina saxatilis (Snyder & Gooch 1973). These authors observed that “significant population differentiation may occur over distances of as little as 2 km, while widely separated populations may be nearly identical”. Colson & Hughes (2004) reported a similar pattern for local populations of Nucella lapillus: “The similarity between SW1 (St Agnes in North Cornwall) and SW10 (Stoke Beach in South Devon) is remarkable, considering the geographical distance between the two populations”, and they suggested “that the major dispersal routes involve relatively long-distance exchanges between open sea sites, bypassing Plymouth Sound” (Figure 16). In a study on the genetic population structure of the saltmarsh plant Elymus athericus, Bockelmann et al. (2003) also observed that distant populations were more similar than immediately adjacent populations: “Surprisingly, the Helmsand [HS] population was more similar to the populations on Schiermonikoog [Sch], although it is situated in a clayey mainland marsh in the northeastern Wadden Sea such as Sönke-Nissen-Koog Vorland [SNK] and Westerhever [WH]” (Figure 16). For the seagrass Thalassia testudinum, Waycott & Barnes (2001) revealed high levels

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of gene flow over distances of >2500 km (between Panama and Bermuda), and they suggested long-distance movements of vegetative fragments (possibly via rafting) as the principal explanation for the same clone being present in Panama and at Bermuda. Indication for the high floating potential of T. testudinum also comes from the finding of fragments of this seagrass in the deep sea off the Caribbean coasts (Wolff 1979), even though Flindt et al. (2004) assigned this species a low floating potential. It is suggested that many of these cases could be the result of leapfrog dispersal, where travellers jumped over long distances, leaving nearby populations out of the loop. For several rafting species, though, there is an indication of decreasing genetic diversity toward the limits of their biogeographic distribution (Marko 2004, 2005), suggesting that dispersal may occur along a chain of stepping stones. The reasons for decreasing genetic diversity toward range limits are primarily four-fold, namely (i) lack of suitable dispersal opportunities, (ii) limited propagule production, (iii) rapid range extension via few founding individuals or (iv) differential natural selection, which permits survival of different genotypes in source and sink regions. These factors may act in combination or separately — if they act in unison, their impacts might be enhanced. Toward the down-current end of intermittent rafting routes, dispersal may taper out and the frequency of events may take on a sporadic character similar to that on episodic rafting routes (see below). Based on global patterns of substratum supply, several intermittent rafting routes can be identified (Figure 17). Important intermittent rafting routes are known in the boundary currents of the Pacific, on the coasts of the North Atlantic, probably in the boundary currents of the South Atlantic (little is known from these regions), around southern New Zealand, also along the coasts around the equator, but at lower frequency than on the other intermittent rafting routes (Figure 17). In some of these regions (e.g., in the Humboldt and California Currents) during ENSO events, large-scale regional extinctions may occur. Rafting can contribute to a rapid recolonisation after such events, albeit possibly with few colonisers resulting in low genetic diversity (for algae see Martínez et al. 2003, for invertebrates Marko 2004).

Figure 17 Global distribution of important intermittent (shaded areas) and episodic (dotted lines) rafting routes. Regions with high abundances of floating wood and floating macroalgae indicated by dark and light shading, respectively.

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Episodic natural rafting routes Sporadic supply of floating substrata on episodic rafting routes

In many regions of the world, for most of the time floating items may be virtually absent on the sea surface. However, after certain events, large numbers of these items suddenly become available as rafting substrata. This is, for example, the case with volcanic pumice, which may be supplied in large quantities after volcanic eruptions (Sutherland 1965; Jokiel 1989, 1990a; Bryan et al. 2004). Similarly, after cyclones, flood events or tsunamis enormous quantities of terrestrial debris may reach the oceans (Carey et al. 2001). Following these events, huge armadas of floating substrata may be transported with the predominant current systems, offering abundant rafting opportunities for potential travellers. Many of the substrata that become available episodically have very high longevities since they are either of abiotic origin (volcanic pumice) or consist of inorganic materials (skeletons) that are resistant to decay processes. Also terrestrial debris (e.g., large trees or processed wood) may survive for a relatively long time at the sea surface. Consequently, many of the floating items that are supplied sporadically may be transported over relatively large distances. Due to their origin either in terrestrial environments or in the open ocean, most of these substrata will only be colonised after starting their journey at the sea surface. The frequencies and localities at which these substrata are supplied to the ocean are difficult to predict. In general, volcanic pumice is most common in regions with high volcanic activity (e.g., the Pacific Ocean and the Mediterranean). Important volcanic eruptions, during which large quantities of volcanic pumice are released, appear to occur on a timescale of the order of several decades or centuries. For example surface eruptions were recorded in 1883 in Krakatau (Thornton 1997, Jokiel & Cox 2003) and in 1952 on San Benedicto (Richards 1958). Underwater eruptions producing buoyant pumice appear to take place over similar timescales (Sutherland 1965, Frick & Kent 1984, Fushimi et al. 1991, Bryan et al. 2004), in particular in the Pacific Ocean. Throughout a region with high tectonic activity, tsunamis may also wash terrestrial debris into the sea along wide stretches of impacted coastlines. Along the Pacific Rim, tsunami events are recorded to occur at a frequency of tens to hundreds of years (Witter et al. 2001, Pinegina et al. 2003, Kulikov et al. 2005). Similar frequencies are reported from other active margins (e.g., in parts of the Mediterranean (Altinok & Ersoy 2000)). In the tropics, large quantities of terrestrial debris may also be flushed out to sea after passage of hurricanes and typhoons. These tropical cyclones recur each year (e.g., Chan & Liu 2004), but their pathways and the input sites of terrestrial debris are highly unpredictable (Landsea et al. 1996, Weber 2005). Their frequency of occurrence in a given locality may be on the order of decades or centuries. Buoyant skeletal materials of marine organisms (floating corals, cephalopod shells, egg cases) only become available episodically, but then may be very abundant (Kornicker & Squires 1962, DeVantier 1992, Cadée 2002). In addition to these sporadically supplied substrata, some of the regularly available items such as floating macroalgae or wood may occasionally also travel on episodic rafting routes (e.g., during particular climatic or ocean- ographic events such as ENSO). In general, the temporal pattern of travel opportunities on these episodic rafting routes depends on the frequency of events that supply floating substrata. The unpredictability of most of these events makes it difficult (in many cases impossible) to provide estimates of the time intervals between subsequent rafting episodes. However, despite these uncertainties some simple statements can be made. In most cases, episodic events occur at intervals of many years, often decades or even centuries. It can thus be safely stated that the generation times of most small, coastal or terrestrial organisms are substantially shorter than the time intervals between supply events. Consequently, individuals supplying propagules to a given rafting episode will be descendents of several generations

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of residents that arrived after previous rafting events. In contrast, in clonal organisms, generation times may be of a similar magnitude as the intervals between rafting episodes. Individuals that established after one episode may be the same ones providing propagules for a subsequent rafting episode. As a consequence of the relationships between generation time and dispersal events, small sexually reproducing species with short lifetimes may reproduce over many generations without any (or with very little) exchange via rafting. During these time periods, dispersal will depend primarily on autonomous dispersal capabilities of organisms. This may lead to small effective population sizes of these organisms (i.e., on islands or in relatively isolated bays), with a high likelihood of founder effects to occur. In general, the degree of isolation of local populations will be negatively correlated with the potential for autonomous dispersal of a species (unless the episodic event has transported colonists into an area with frequent or intermittent rafting routes). Species with direct development can be expected to be most affected by periods of isolation of local populations. Interestingly, once rafting opportunities arise, some of these species are particularly well adapted for LDD and successful colonisation of new habitats (Thiel & Gutow 2005b). As a result of relatively long periods of isolation, local populations may diverge or even go extinct. Consequently, organisms that are transported during episodic rafting events may arrive in areas where conspecifics have experienced substantial genetic changes or are completely absent. Even when some degree of divergence has occurred or the new colonisers come into secondary contact with incipient species that derived from a common ancestral lineage, hybridisation may take place. If genetic changes have not yet led to reproductive barriers, genetic diversity of the metapopulation may reach high levels. In contrast, if allopatric evolution has led to reproductive isolation or if conspecifics are absent, founding populations may become established as a new species to the area. The genetic diversity of these local populations will depend on their history of isolation and the number and gene pool of arriving individuals. Since founding populations of direct developers on episodic rafting routes usually are small, genetic diversity of these may be relatively low. Thus, the dispersal dynamics on episodic rafting routes may lead to contrasting scenarios in the population biology of sexually reproducing organisms with short generation times. Genetic diversity in local populations may either show high or low levels, depending on whether arriving individuals can interbreed with local residents or not (Figure 18). In general, it can be predicted that the evolutionary consequences of episodic rafting routes depend on the relationship between generation times of rafting organisms and the time interval between subsequent rafting episodes.

Examples of episodic rafting routes

Volcanic pumice During volcanic eruptions enormous quantities of positively buoyant pumice can be released (e.g., Sutherland 1965, Jokiel 1990a, Bryan et al. 2004). Pieces of pumice usually are relatively small (several millimetres in diameter), but may occasionally be larger, reaching fist size — even pieces of >0.5 m diameter have been reported (Jokiel & Cox 2003). Pumice that is supplied to the sea may originate from island volcanoes (Richards 1958, Thornton 1997), or also from eruptions of underwater volcanoes (e.g., Coombs & Landis 1966, Fushimi et al. 1991, Bryan et al. 2004). Pumice pieces can float for many months and even years before disintegrating or washing ashore. During this time, the pumice and rafting organisms may be distributed throughout all major ocean basins (Frick & Kent 1984, Jokiel & Cox 2003, Bryan et al. 2004) (Figure 19). Diverse marine organisms are known to be transported with volcanic pumice. Algae, sponges, corals, polychaetes and bivalves have been found growing on volcanic pumice (Jokiel 1984, 1989; Bryan et al. 2004). How these organisms colonise the floating pumice in the first place is not well known. Pumice, as most other floating substrata on episodic rafting routes, enters the sea in a clean

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A Episodic rafting route; singular dispersal eventB Episodic rafting route; repeated dispersal events One source region

Founder effect: reduced genetic diversity High population connectivity: similar genetic diversity

C Episodic rafting route; repeated dispersal eventsD Episodic rafting route; historic dispersal events Multiple source regions Multiple source regions

Mya Kya

High population connectivity: higher genetic diversity No connectivity: allopatric speciation

Figure 18 Scheme showing four possible scenarios on episodic rafting routes and the expected genetic and biogeographic consequences. (A) showing a local island population arising from a singular dispersal event, where founder effects lead to a strong reduction in genetic diversity in the sink population. (B) showing a local island population supported by repeated dispersal events from a particular source region, resulting in close similarity between source and sink populations. (C) showing a local population supported by repeated dispersal events from several source regions, resulting in a high genetic diversity in the sink population. (D) showing a situation with several historic dispersal events, where local populations in the sink region have diverged significantly after the first dispersal event and could not anymore interbreed with subsequent colonists, leading to the establishment of two different species in the sink region.

state. Thus, it is most likely that pumice is colonised while floating, probably via planktonic (larval) stages. Many corals found on pumice have planktonic larval stages (Jokiel 1989), which is also true for other organisms reported from pumice, such as, for example, bivalves or stalked barnacles. In a laboratory experiment, Jokiel & Cox (2003) showed that similar numbers of planula larvae of Pocillopora damicornis settled and developed into juvenile colonies on volcanic pumice as on calcareous rock. They emphasised that P. damicornis produces larvae throughout the year, poten- tially permitting continuous colonisation of floating pumice. Bryan et al. (2004) remarked on the temporal coincidence between a pumice supply event and a spawning event: “It is noteworthy that the eruption and generation of the pumice rafts in this instance just preceded late spring coral spawning events in the southwest Pacific”. The necessity for close temporal overlap between pumice availability and propagule supply in a given locality enhances the sporadic character of dispersal on these episodic rafting routes. Several studies provide indication that volcanic pumice may serve as a dispersal vector with the potential of connecting distant populations. Strongest evidence comes from the studies by Jokiel

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Figure 19 Origins of volcanic pumice found on beaches on Hawaii and Christmas islands, and major ocean- ographic currents assumed to transport floating pumice from the different source regions; modified after Jokiel & Cox 2003. Shadings in map indicate sources of origin shown in the pie diagrams.

(1984, 1989, 1990a,b), who sampled volcanic pumice throughout the equatorial Pacific. His studies revealed that some species (e.g., P. damicornis) are frequently dispersed via pumice (Jokiel 1984, 1990b), though he remarked that organic substrata such as wood and seeds might be “far more important than pumice rafts in establishment of new populations of corals”, because rafting colonies are easily shed from these organic substrata when scratching over the reef (Jokiel 1989). Regardless of the floating substratum, rafting appears to be an important dispersal mechanism for some coral species. Observations of rafted colonies can be compared with studies on the geographic distribution or genetic diversity of these corals. Pocillopora damicornis is distributed throughout the tropical Pacific and Indic oceans and there is relatively good indication that distant populations may be episodically connected (e.g., during El Niño events) (Glynn & Ault 2000). However, populations from the East Pacific are spawners whereas those from the West Pacific are brooders (Glynn & Ault 2000), suggesting that connectivity between distant populations could be limited and might already have led to cryptic allopatric speciation. Ayre & Hughes (2004) revealed gene flow over large distances for P. damicornis and other corals along the Great Barrier Reef, but they did not specify whether dispersal might be achieved via larvae or via rafting. They did, however, emphasise that genetic exchange between distant populations is a highly episodic event: “Long-distance dispersal by corals to geographically isolated reefs cannot be achieved incrementally and is likely to be very rare” (Ayre & Hughes 2004). Interestingly, for this region, several reports of pumice-rafted

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Figure 20 (A) A small colony of the coral Pocillopora damicornis, growing on an algae-covered piece of volcanic pumice (photo courtesy of Scott Bryan, Yale University, U.S.) (diameter of coin is 16 mm), and (B) map of the SW Pacific indicating the inferred rafting routes of floating pumice originating from an eruption in the Tonga-Kermadec arc; modified after Bryan et al. (2004). (C) Estimates of gene flow (Nm) for two coral species from the Great Barrier Reef, one of which (P. damicornis) is very commonly reported as a rafter on volcanic pumice; modified after Ayre & Hughes (2004).

corals (including P. damicornis, Seriatopora sp. and Styllophora sp.) have been published (Jokiel 1990b, Bryan et al. 2004), suggesting that gene flow could indeed be achieved via rafting of adult colonies (Figure 20). Even though Ayre & Hughes (2004) do not discuss rafting, their results of gene flow on different spatial scales closely matches the predictions for processes on episodic rafting routes made above: “While long-distance gene flow over multiple generations is sufficient to limit genetic differentiation along the length of the Great Barrier Reef, most recruitment by corals on ecological time frames is decidedly local”. Results from a study by Wörheide et al. 2002 reported similar scales of connectivity for the tropical sponge Leucetta ‘chagosensis’ (Figure 21). They suggested that “small-distance dispersal was involved in the range expansion of clade 3Ð1, whereas some long-distance movements may be inferred for clade 3–4”, but they did not mention how LDD was achieved (possibly via pumice?). Little is known about dispersal and population connectivity via floating pumice for other organisms. This probably is due to the fact, that dispersal events are rare and that many other organisms (e.g., algae or bivalves) may quickly fall off pumice pieces after stranding (Jokiel 1990a). Ó Foighil et al. (1999) reported the presence of Ostrea chilensis in New Zealand and in Chile separated by >5000 km of open ocean (Figure 21). Since this species features direct development,

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Figure 21 (A) Distribution of the principal clades revealed for the tropical sponge Leucetta ‘chagosensis’ throughout its distribution range in the Indo-Pacific, and (B) distribution of the two clades found on the Great Barrier Reef; modified after Wörheide et al. (2002). (C) Unrooted phylogram based on mtDNA Cytochrome Oxidase I sequences depicting relationships between three populations of Ostrea chilensis (two from New Zealand and one from Chile) and two other species of the genus, and map of the Southern Ocean indicating the current direction of the West Wind Drift; modified after Ó Foighil et al. (1999).

these authors suggested that the trans-Pacific distribution pattern of O. chilensis may be the result of pumice-rafting. Empirical evidence for this transport mechanism and for continuing gene flow between New Zealand and Chilean populations, however, is not available at present. Terrestrial debris (after flood events, cyclones or tsunamis) Supply frequencies of terrestrial debris are similar to that of volcanic pumice. However, terrestrial debris supplied during episodic events comprises a heterogeneous assemblage of different substrata, from fragments of annual plants to entire trees. While it is well known that large amounts of floating substrata are travelling in adjacent seas after these events, little is known about the quantities and temporal dynamics. Tropical cyclones occur every year in the western parts of the central Pacific and the central Atlantic, but storm tracks vary substantially among years. A synthesis of the data provided by Landsea et al. (1996) shows that the hitpoints of hurricanes (where hurricane tracks and shorelines cross) vary substantially between years (Figure 22). Consequently, dispersal export from particular localities (e.g., islands) via terrestrial debris will occur only episodically. Storm and rain events were identified as main causes for interannual variation in abundance of floating terrestrial debris (Heatwole & Levins 1972, Zarate-Villafranco & Ortega-García 2000).

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Figure 22 Tracks of intense hurricanes in the W Atlantic over the eight-year period 1987Ð1995, showing that annual sites of hurricane landfall (star symbols) (and subsequent production of sporadic rafting opportunities) are spread throughout the region; modified after Landsea et al. (1996).

The importance of hurricane and storm events for episodic appearance of rafting opportunities is well known. For example, Simberloff & Wilson (1969), who studied the colonisation patterns on small mangrove islands in Florida Bay, noted that rafting dispersal may usually be of minor importance, because “except during hurricanes, there is very little floating debris”. In general, these events appear to have particular importance in the tropics where flood events, cyclones and tsunamis are most effective in transporting terrestrial debris to the sea. In the case of cyclone-related supply this is explainable by the fact that these phenomena occur mainly in the tropics. In the case of flood events and tsunamis these may achieve particular significance in the tropics due to the concentration of (a) many large and unregulated rivers in these areas, and (b) low-lying coral islands with little protection against tsunami or cyclone waves. Organisms found on this debris include terrestrial species such as insects and reptiles (Wheeler 1916, Heatwole & Levins 1972, Censky et al. 1998), but also marine organisms. Due to the singularity of events, little is known about connectivity between local populations via rafting on terrestrial debris. The strongest indication that terrestrial debris (in particular trees) may aid in transport of organisms comes from terrestrial vertebrates (reptiles). Supporting evidence comes from observations of individuals on rafts and from phylogeographic studies. Disembarkation of reptiles from rafts of terrestrial debris has been observed by Barbour (1916) and Censky et al. (1998). Several phylogeographic studies suggest over-water dispersal of terrestrial vertebrates, and in many of these cases, authors suggested rafting on terrestrial debris (Raxworthy et al. 2002, Calsbeek & Smith 2003, Carranza & Arnold 2003, Glor et al. 2005) (Figure 23). Yoder et al. (2003) suggested that Carnivora on Madagascar originated from one single dispersal event (Figure 23). They also emphasised that those groups that colonised feature ecophysiological specialisations that may have allowed relatively long trips in an unhospitable environment (e.g., a raft in the open ocean). Clearly, evidence for rafting dispersal via terrestrial debris supplied by episodic events is circumstantial. However, independent molecular studies provide increasing indication that this process may occasionally have led to successful colonisation and that it may be of major importance for the biodiversity of remote locations. Giant kelp and other substrata Due to the sporadic character of dispersal events and the fact that they may have happened far back in the past, often it is difficult or impossible to know the floating

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MARTIN THIEL & PILAR A. HAYE Anolis rent A data of the diffe adagascar; genetic data suggest that taxa found on African predecessor; modified after Yoder et al. (2003). et Yoder African predecessor; modified after al. (2005). (C) Proposed biogeography of carnivores from Africa and M from al. (2005). (C) Proposed biogeography of carnivores lizards from Caribbean islands, and (B) cladogram showing the phylogenetic relationships inferred from mtDN lizards from Caribbean islands, and (B) cladogram showing

Anolis (A) Sampling sites of species from the Caribbean islands; modified after Glor et Madagascar have originated from a single dispersal event from an originated from a single dispersal event Madagascar have Figure 23 Figure

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substratum on which organisms have been dispersed. Some authors have used life history of present day organisms to infer potential substrata, while others have simply suggested rafting without venturing into the characteristics of rafts. Some substrata that usually travel on intermittent rafting routes (giant kelp and wood) may also sporadically be transported over distances more characteristic of episodic rafting routes. This may occur when storms or other climatic events push these substrata out of their common routes or accelerate transport velocities. During these occasions, substrata may become transported to localities that they would not normally reach. For example, giant kelp, thought to survive for several months at the sea surface, may not be capable of bridging the enormous distances of open ocean between South Africa and Australia or between New Zealand and South America. There is, however, both distributional and genetic evidence for occasional connections via floating substrata. Many coastal species are found on distant subantarctic islands and rafting on floating kelp is commonly inferred (Davenport & Stevenson 1998, Edgar & Burton 2000). A study by Waters & Roy (2004a) indicated that colonisation of Australia by the seastar Patiriella exigua resulted from a singular dispersal event from African source populations (Figure 24). This seastar also is found in the holdfasts of giant kelp, and Mortensen (1933) had suggested that dispersal of this species may occur via floating kelp. Based on phylogeographic relationships of topshell gastropods with short-lived larvae, Donald et al. (2005) suggested that repeated LDD events via rafting had occurred during the evolutionary history of these species. In the case of the species Diloma nigerrima a dispersal event between New Zealand and Chile was dated to have happened approximately 0.6 Mya, apparently too short for significant genetic divergence to take place (Figure 25). Episodic dispersal on large floating macroalgae may also play a role in the northern North Atlantic. Based on historical analyses and on the present-day distribution of important rocky-shore

Figure 24 Episodic rafting route in the West Wind Drift between Africa and Australia, possibly supported via floating giant kelp. (A) Sampling sites of different populations of Patiriella exigua; insert shows the seastar Patiriella exigua (which reproduces via benthic crawl-away larvae) from S Africa (photo courtesy of Eliecer Diaz, Rhodes University, S Africa). (B) Phylogram based on mtDNA Cytochrome Oxidase I (CO I) sequences; modified after Waters & Roy (2004a).

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Figure 25 Episodic rafting route in the West Wind Drift between New Zealand and S America, possibly supported via floating bullkelp Durvillaea antarctica. (A) Sampling sites of different gastropod species from the family Trochidae; geographic distribution of bullkelp D. antarctica indicated by light shading. (B) Phy- logenetic tree based on mtDNA 16S, COI and nuclear DNA actin sequences for selected species from the S Pacific; modified after Donald et al. (2005).

organisms, Ingólfsson (1992) inferred a rafting route between northern Norway and Newfoundland and Nova Scotia on the western side of the North Atlantic, with Iceland and southern Greenland serving as intermediate stepping stones. Wares & Cunningham (2001) supported this suggestion via genetic studies. For example, they found genetic connectivity between North American and European populations of Idotea baltica (Figure 26), a species commonly found on floating algae (Ingólfsson 1995, Gutow & Franke 2003). They also revealed that the North American populations of Nucella lapillus and Littorina obtusata, with benthic crawling progeny, had originated from European populations (Wares & Cunningham 2001). In all cases rafting transport on floating algae appears to be the most likely dispersal mechanism. Ó Foighil & Jozefowicz (1999) reported phylogenetic relationships between clades of Lasaea from Florida and Bermuda on the western side of the North Atlantic and between clades from the Azores and the Iberian peninsula on the eastern side of the North Atlantic, which was confirmed in a later more extensive study (Ó Foighil et al. 2001) (Figure 27). They suggested rafting but did not mention the substrata on which these bivalves may have been transported. Regardless of whether dispersal has occurred on floating kelp, wood or other substrata, most of these studies underline the importance of episodic rafting events and subsequent periods of isolation.

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Figure 26 (A) The isopod Idotea baltica, which releases fully developed juveniles, on fucoid algae (photo courtesy of Veijo Jormalainen, University of Turku, Finland). (B) Map of the N Atlantic with sampling sites: M Ð Maine, NS Ð Nova Scotia, Ic Ð Iceland, No Ð Norway, Ir Ð Ireland, Fr Ð France. (C) Haplotype networks (based on mtDNA COI sequences) for populations of Idotea baltica (direct development), Nucella lapillus and Littorina obtusata (crawl-away progeny) from the N Atlantic; modified after Wares & Cunningham (2001).

Dispersal dynamics on episodic rafting routes

Based on the examples presented, it appears that episodic rafting routes are most important in the tropics and in subpolar regions (Figure 17). While in the tropics these rafting routes are constituted by episodic supply of floating substrata (pumice and terrestrial debris), in subpolar regions they may represent episodic extensions of intermittent rafting routes (supported by giant kelps and wood). Interestingly, the three main substrata mentioned herein (pumice, terrestrial debris, giant kelps) appear to transport different groups or organisms. Volcanic pumice and calcareous animal skeletons are usually only colonised after starting their pelagic voyage (i.e., by marine organisms that have (short-lived) planktonic larvae). Also terrestrial debris is colonised by marine organisms while afloat, but trees or other terrestrial vegetation may additionally carry many initial terrestrial colonists such as insects, spiders or vertebrates with them to sea. In contrast, large kelps, which are colonised while growing in benthic habitats, appear to have been mainly responsible for dispersal of various marine organisms with direct development. These observations underline the importance of sub- stratum origin and characteristics, in particular for rafting over long distances. Many authors discussed the relationship between connectivity and the possibility of population divergence. For example, Ayre & Hughes (2004) remarked on low levels of gene flow between distant local populations of corals, just sufficient to counteract genetic divergence (see above). In this context, Bryan et al. (2004) suggested pumice rafting as an important connecting process: “Speciation events and volcanicity may be linked such that the periodic development of globalism

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Figure 27 (A) Nest of an unidentified Lasaea species from Chile, and adult brooding juveniles. (B) Study regions of populations of Lasaea spp. in the western and eastern N Atlantic; map modified after Ó Foighil & Jozefowicz (1999). (C) The unrooted phylogram (based on mtDNA 16S sequences) showing the genetic relationships of the N Atlantic clades of Lasaea, which suggests a western and an eastern clade in the N Atlantic. Six different dispersal events were inferred between the Azores and the Iberian Peninsula (for sampling sites of eastern N Atlantic populations see detailed map); modified after Ó Foighil et al. (2001).

for some taxa (e.g., corals, gastropods, bryozoans) may correlate in time and/or space with particular igneous events”. If gene flow is insufficient, speciation processes may occur: “Species that have a capacity for sporadic dispersal may undergo dramatic range expansions followed by isolation, genetic divergence, and possible speciation” (Waters & Roy 2004a). Other authors reached similar conclusions: “…The foregoing leads to the expectation that endemism through founder speciation is most likely for organisms that rarely enter the transport medium but survive well in it” (Paulay & Meyer 2002). These authors went on to say: “Organisms that rarely enter the dispersal medium but survive well there are the most likely to undergo founder speciation. The high levels of endemicity observed in rafted, direct developing marine mollusks, and bird- and raft-dispersed terrestrial organisms support this hypothesis”. Additionally, many rafting species that survive LDD via rafting are also pre-adapted to become successful colonisers after making landfall (see Thiel & Gutow 2005b). Occasionally, rafting organisms on episodic rafting routes may even cross biogeo- graphic borders or barriers: “The several months of transportation time provides the opportunity for biogeographic exchange, and it may be a mechanism by which biogeographic mixing in the marine realm occurs naturally” (Bryan et al. 2004). If this is followed by successful colonisation, it will lead to an enrichment of the local biota, thereby increasing local biodiversity. In general, connectivity between populations is very low on episodic rafting routes. This may, in extreme cases, lead to singular colonisation by few individuals, resulting in a founder effect. This may facilitate allopatric speciation, in particular in sexually reproducing organisms with short

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generation times. Furthermore, since episodic rafting routes often are supported by floating substrata of high longevity (volcanic pumice, calcareous skeletons, large trees), they may often result in LDD, transporting rafters to new habitats. Here these organisms may be confronted with established communities and conditions, exposing colonists to a selective environment different from their source regions. Thus, for several reasons dispersal via episodic rafting routes may result in rapid evolutionary changes in rafting organisms. Interrupting the sporadic pattern of these episodic rafting events may have important consequences for biodiversity.

Artificial rafting routes In this review artificial rafting routes are considered to be those sustained by floating substrata of anthropogenic origin, in particular plastics. These have gained increasing attention in recent years (Winston 1982, Barnes 2002), because supply has increased during the past century, and plastics are now present throughout the world oceans. For two main reasons, plastics do not fit the natural rafting routes discussed above: (a) they are delivered to the oceans almost anywhere, in estuaries, bays and in the open ocean, albeit with regional differences in intensity and (b) some of them are extremely long-lived and can therefore be transported over very long distances. They share some features with substrata found on frequent rafting routes (abundant supply), but they differ in other features (plastics offer no food value and are highly persistent). Similarly, some of their characteristics resemble those of substrata on episodic rafting routes (low food value and high longevity), but other char- acteristics are very different (plastics are supplied relatively consistently). Plastics are present on all previously described natural rafting routes, but they may gain particular importance on the intermittent and in particular on the episodic rafting routes. As outlined above, organisms on frequent rafting routes have abundant dispersal opportunities on natural floating substrata, because these are usually available in large quantities. Some of these organisms may also hitch a ride on floating plastics, but given the high connectivity between local populations already achieved via natural substrata, this may be relatively unimportant. In contrast, on intermittent and episodic rafting routes, plastics (and other anthropogenic debris) may lead to a dramatic increase in dispersal opportunities and due to their continuous supply may disrupt the sporadic character of natural dispersal events. Previous authors have suggested that episodic rafting routes, for example those sustained by volcanic pumice, may permit “periodic globalism” of some organisms (sensu Bryan et al. 2004). Chronic supply of plastics may enhance the risk of globalisation of these species and homogenisation of the species biodiversity, in particular in regions where episodic rafting events have predominated in the past, for example in the Southern Ocean (Barnes & Fraser 2003). Rafting organisms found on plastics are diverse and they include, among others, sponges, hydrozoans, bryozoans, ascidians, polychaetes, bivalves and crustaceans (Thiel & Gutow 2005b). Interestingly, corals have also been found on floating plastics or glass, including species from the genus Pocillopora, commonly reported from floating pumice (Jokiel 1984, 1989; Winston et al. 1997). This indeed indicates that plastics may serve as alternative rafting substratum for the same organisms usually transported by pumice or other sporadically supplied substrata. Floating plastics are occasionally suggested as dispersal agents connecting localities. For example, Aliani & Molcard (2003) discussed that many organisms found on floating plastics in the western Mediterranean can become widely dispersed along shorelines of this region. Winston et al. (1997) expressed similar concerns for the western South Pacific. Stevens et al. (1996) found many bryozoan species, which are usually growing on natural buoyant substrata, also on floating plastics — some rafting colonies were even sexually mature, leading the authors to infer that these species “could adapt to a pseudoplanktonic lifestyle”. Such an adaptation would then facilitate LDD. Due to their relatively recent appearance in the world oceans, no molecular study has yet identified floating plastics as potential dispersal vectors. However, given the ubiquity of plastics and other

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anthropogenic floating substrata and their diverse assemblage of rafters, it is considered highly likely that these may serve as connecting agents.

Rafting dispersal Marine connectivity Marine benthic invertebrates inhabit patchy environments. As described above, patches harbour local populations that may be connected by dispersal, either through larvae, rafting or other mechanisms. Connectivity among local populations of rafters will largely depend on the environ- mental conditions of the place they inhabit. The genetic structure of local populations is determined in part by the direction, magnitude, and frequency of dispersal among local populations. Just as it has been widely demonstrated for species with planktonic developmental stages (Palumbi 1995, Bohonak 1999), oceanographic, ecological, behavioural and historic factors may limit rafting dispersal as well. All of these factors determine the relationships between local populations and the magnitude of the effects of deterministic and random evolutionary forces (i.e., natural selection and genetic drift, respectively). Since there are several factors that, in combination, affect the dispersal potential of a species and it cannot be inferred from a single element (i.e., mode of development, Colson & Hughes 2004), estimates of gene flow have been used to understand the factors that shape connectivity among local populations. Gene flow can be indirectly estimated from population differentiation data, and represents a measure of realised dispersal potential. Gene flow estimates for a number of benthic marine invertebrates have indicated that both organisms with planktonic and direct development can achieve LDD. Larval dispersal is assumed to be the major means of dispersal for organisms with planktonic development, while rafting is considered to promote the dispersal of organisms with direct development (e.g., Johannesson 1988, Ó Foighil 1989, Davenport & Stevenson 1998). Organisms with planktonic development, too, may be dis- persed through rafting, which is, however, hard to demonstrate since rafting is an explanation that often is supported indirectly by the rejection of alternative hypotheses, such as vicariance, anthro- pogenic and larval dispersal (e.g., Castilla & Guiñez 2000, Waters & Roy 2004a, Donald et al. 2005). Several studies stress the importance of considering the biology of a species beyond its developmental mode in order to predict its dispersal potential (e.g., Colson & Hughes 2004). While species with planktonic larvae may disperse over much shorter distances than expected from their larval lifetime, those with direct development may be transported distances far exceeding what would be expected based on their autonomous dispersal potential. Evidence is mounting that rafting can have a strong impact on the genetic structure and geographic range of distribution of some species, particularly of those with direct development. It thus may be timely not only to abolish the Rockall Paradox but also to go a step further and consider rafting as an important mechanism for the connectivity of marine communities.

Use of genetic data to estimate gene flow

Molecular genetic tools allow for studying the allele frequencies of populations and inferring their demographic history. There is a diversity of molecular markers, among which proteins, mitochon- drial DNA (mtDNA), microsatellites and fingerprinting methods (e.g., RFLP, RAPDS) are preferred for studies on the population level (Parker et al. 1998, Sunnucks 2000, Hellberg et al. 2002, Féral et al. 2003). MtDNA has been extensively used to reveal phylogeographic patterns and population structure of a wide diversity of marine taxa (e.g., Palumbi et al. 1997, Avise 2000, Wilke & Davis 2000, Collin 2001, Breton et al. 2003, Waters & Roy 2004b). Microsatellites, proteins, and finger- printing methods have been widely used to infer population structure often at more than one

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geographic scale (e.g., Edmands & Potts 1997; Ayre & Hughes 2000, 2004; Goldson et al. 2001; Colson & Hughes 2004). Many of these studies include estimates of population differentiation that also allow for estimating gene flow as the number of migrants per generation among local popu- lations (e.g., Ayre et al. 1997, Ayre & Hughes 2000, De Matthaeis et al. 2000, Vianna et al. 2003). The genetic structure of a metapopulation depends on local dispersal dynamics influenced by both the migration rate (m) and the effective population size (N) of the metapopulation (Hellberg

et al. 2002). A commonly reported measure of population differentiation is the fixation index, FST, developed by Wright (1931, 1965) that refers specifically to the differentiation among subpopula- tions (S) of the total population (T) and allows for the estimation of Nm (the product of effective population size and migration rate). Nm is interpreted as the number of migrants per generation,

and can be calculated from FST -values by the following relationship: FST = 1/(1 + 4Nm) (Wright 1969). Generally, FST-values smaller than 0.2 (Nm = 1) represent less than one individual migrant per generation, which is considered insufficient to prevent population differentiation. Values of Nm greater than 1, corresponding to slightly higher levels of gene flow, are high enough to prevent differential fixation of alleles in different subpopulations (Wright 1969). Since many studies have

reported FST values at a wide variety of spatial scales, it is used in the present analysis as a measure for comparison of genetic differentiation data from the literature. FST is a powerful tool to estimate genetic differentiation among populations. Populations at or close to equilibrium conditions will

behave somewhat like the model underlying the FST coefficient and thus its value will be biologically meaningful. Caution needs to be used, though, because FST values could be misleading and in particular for populations, which commonly deviate from equilibrium assumptions underlying the

mathematical model that FST is based on (see Grosberg & Cunningham 2001). Whitlock & McCauley (1999) address the general limitations of the model and its unrealistic biological assumptions that may affect the meaningfulness of the numerical value. Based on their analysis, they suggest that “comparisons of large groups of species are likely to be more informative, as many of the differences may average out” (see also Neigel 1997, 2002). In the present review, such an analysis is undertaken,

and genetic structure data are compiled and analysed for a large group of marine invertebrates. FST approaches have revealed patterns of genetic structure over a wide range of biological scenarios and have indicated that the genetic structure of populations is shaped by several factors, including gene flow barriers that are thought to be due to environmental factors (see below). Data should be carefully interpreted; in some cases genetic differentiation of populations may be reflecting historic rather than ongoing events. For example, gastropod species of the genus Nucella with similar dispersal potentials (they lay egg capsules from which juveniles emerge) display extremely different patterns of population structure across the same geographic range (Marko 2004). Usually these differences have been attributed to dispersal potential, but in this case, the species have similar dispersal potentials based on their developmental mode. The results of that study address the importance of

ecological and historical differences for the genetic structure of populations. FST cannot detect gene flow asymmetry as it only shows a measure of total differentiation among populations without considering independently the contribution of each of the compared populations to the differenti- ation among them. Measures of asymmetric gene flow are particularly desirable in the context of rafting, and can be predicted by some alternative means, although these are scarce in the literature. An example is given by Wares et al. (2001) who used a cladistic analysis to detect asymmetrical migrations. They studied genetic differentiation of two barnacle species and a sea urchin across Point Conception in California, which had been suggested as a strong barrier to gene flow. The cladistic approach allowed them to determine that there was an excess of southward migration events across Point Conception. In the context of rafting it is desirable to have estimates of magnitude and direction of dispersal among local populations of potential rafters to better under- stand the dynamics of rafting routes. In cases of unique rafting events that lead to allopatric speciation (on episodic routes), the direction of the dispersal route can be detected with phylogenetic

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analyses. Intermittent and frequent rafting routes, however, prevent speciation by maintaining sufficient connectivity among local populations. In these cases, the genetic structure of populations will depend on the magnitude and direction of migration, even though asymmetrical gene flow is

not often detected, total gene flow estimates (Nm) can be inferred (from FST values) and are likely to reflect the summed contributions of populations or groups of populations to the total exchange among them. There exists a variety of other measures of population differentiation that alleviate

many of the problems associated with FST, but most are scarcely reported in marine population genetic studies and thus are not useful for comparison of a large number of studies. The numerous

reports of FST-like values allow estimation of realised dispersal of many marine taxa (Neigel 1997, Bohonak 1999) and will be used herein to make broad comparisons of the dispersal potential of benthic marine invertebrate taxa.

Genetic homogeneity vs. genetic structure of populations

Even though marine environments seem to lack apparent barriers to gene flow, populations only sometimes show panmixia and genetic differentiation exists even when wide dispersal is predicted based on larval developmental mode. Marine populations usually show reduced heterozygosity (e.g., Ayre & Hughes 2000), explained largely by the restricted dispersal of marine organisms and consequent effects of inbreeding and local population differentiation, which can generate a Wahlund effect (i.e., decreased heterozygosities resulting from the sampling of subdivided populations) (e.g., Johnson & Black 1984a). Planktonically developing taxa intrinsically provide good models to study the potentially restricting effects of the environment on gene flow. Several factors such as ocean- ographic conditions, physical barriers, life-history features, historic demography and ecological or behavioural barriers can hinder the realised dispersal of marine taxa (Hedgecock 1986, Palumbi 1994). The same barriers that have been described for species with planktonic dispersal should apply to dispersal through rafting, too. Many studies have detected limited gene flow in species that presumably have a high potential for dispersal. There are many factors that can act as gene flow barriers and that promote geographic differentiation. Gene flow barriers can be inferred from genetic structure and population differen- tiation data. For example, Sköld et al. (2003) found that genetic differentiation of populations of the widely dispersing seastar Coscinasterias muricata in the New Zealand fjords is not correlated with geographic distance. They suggested that recent colonisation and isolation from open coasts explain the apparent island model of the population. Perrin et al. (2004) also studied population differentiation of this species along the New Zealand fjords and found that at a macrogeographical scale (>1000 km) there was restricted gene flow between the North and South Island. At a mesogeographical scale (tens to hundreds of km) there was significant population differentiation among fjords and the open coast. The pattern among fjords suggests that populations from the north and the south meet in what appears to be a secondary contact zone. For this species, distance alone does not explain population differentiation and it is likely that hydrography prevents mixing of propagules and contributes to isolation of local populations. Local populations seem to have expanded recently and subsequently differentiated as a consequence of isolation. Perrin et al. (2004) suggest that once the larvae of C. muricata “are transported out of the fjord, the likelihood of entering another fjord is less than being transported further along the open coast. For this species, the fjords might act as barriers to dispersal of differing strength, facilitating genetic drift within fjord populations.” Along the New Zealand coast, Waters & Roy (2004b) found that upwelling in the central regions blocks gene flow and leads to genetic differentiation between the populations of the seastar Patiriella regularis from the north and south that are subject to different oceanographic conditions. Just as upwelling can transport propagules away from coastal systems, it may bring propagules toward the coast when it reverses its direction (Palumbi 2003). It is likely that if an

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upwelling zone poses a barrier to gene flow in species with planktonic development, it will also affect the connectivity of populations of rafters. Habitat structure may highly influence population structure, sometimes because different hab- itats may differ in the rafting opportunities they offer (see above). Johannesson & Tatarenkov (1997) found that the population structure of the brooding gastropod Littorina saxatilis on islands of the Swedish coast was highly related to habitat structure. Similarly, Johannesson et al. (2004) reported that genetic structure among L. saxatilis on high rocky shores was different from the ones on low rocky shores. Populations on high rocky shores appear to be more isolated which, as stated by the authors, “might be true if the main mechanism of dispersal among islands is by rafting”. Some studies show the prevailing pattern, namely that populations of organisms with extensive planktonic larval stages are not genetically subdivided. For example, the marine bryozoan Mem- branipora membranacea does not show genetic differentiation among populations across the Atlan- tic Ocean, even though there is morphological variation caused by phenotypic plasticity (Schwaninger 1999). Surprisingly, this species seems to maintain gene flow over long geographic stretches, which could be due to rafting (it has been reported on floating substrata, see Aliani & Molcard 2003) or other mechanisms (e.g., human transport). Conversely, other studies have shown that species with direct development tend to be highly structured due to restricted gene flow (e.g., Hellberg 1994, Ayre et al. 1997, McFadden 1997). This seems to be the case in the gorgonian coral Pseudopterogorgia elisabethae, which has restricted dispersal potential (larvae live less than two days) and shows high genetic differentiation among populations following an IBD pattern (Gutiér- rez-Rodríguez & Lasker 2004). Contrary to expectations based on developmental mode alone, there are examples of directly developing species that show that LDD has taken place or that there is little differentiation among populations. For example, the direct developers Littorina sitkana and Nucella lapillus display high levels of gene flow over relatively wide geographic scales (>1500 km) (Kyle & Boulding 2000, Colson & Hughes 2004) (Figure 16). Based on the above, it becomes evident that connectivity cannot be predicted solely on the basis of mode of development (see also Ó Foighil et al. 1999, Colson & Hughes 2004).

Rafting-mediated gene flow In the past, dispersal rates have been frequently inferred based on presence/absence and duration of a planktonic dispersal stage. However, there are many examples of organisms with planktonic development that, based on population differentiation, have restricted dispersal among local pop- ulations (e.g., Barber et al. 2000, McCartney et al. 2000). On the other end of the scale, species that lack a planktonic dispersal stage may disperse long distances by alternative means such as rafting. Comparisons of gene flow estimates from a wide variety of benthic marine taxa clearly show that populations of organisms with contrasting modes of dispersal can achieve comparable levels of gene flow and that rafting is a significant means of dispersal at more than one spatial scale, particularly for species with direct development (see below). Rafting has been inferred for 33 out of 124 marine invertebrate species for which genetic differentiation data are available (Table 1). In many of the studies, rafting was inferred because realised gene flow strongly exceeded the expectations based on life history characteristics (i.e., absence of a planktonic larval stage), or because of the absence of IBD in brooders suggested the existence of LDD. For 113 of the 124 reviewed species data were reported that allowed an examination of realised gene flow over variable spatial scales (from metres to global distribution)

(Table 1). Only reports that include FST-like values have been incorporated in this analysis. From the FST-like values given, gene flow (Nm; number of migrants per generation) was estimated according to the equation of Wright (1969) (Table 1). Whenever possible, genetic differentiation data for more than one geographic scale were recorded for each species (see Table 1). Values of

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MARTIN THIEL & PILAR A. HAYE yre & Hughes 2000 yre & Hughes 2004 yre & Hughes 2000 yre & Hughes 2000 yre & Hughes 2000 yre & Hughes 2000 yre & Hughes 2000 2005 Whalan et al. 2005 Whalan et Duran et al. 2004a Duran et & Hughes 2000 Ayre Mackenzie et al. 2004 et Mackenzie al. 2005 Baums et Ayre & Hughes 2004 Ayre Govindarajan et al. et Govindarajan Duran et al. 2004b Duran et al. 2004c Duran et A A A A & Hughes 2000 Ayre A & Hughes 2000 Ayre A & Hughes 2000 Ayre A seaweeds Rafting inferred Reference No No No No No No Yes Yes No No data No No No No data No Yes Yes No No No No No No No No No 1.14 0.19 7.1 9.75 12.25 2.53 6.69 6 7.56 0.61 2.87 4.75 1.42 8.08 2.89 4.75 3.32 24.75 2.25 = 0.565 = 0.26 0.71 No data on Yes, = 0.034 = 0.025 = 0.153 = 0.221 = 0.150

= 0.121 1.82 No data No = 0.02 = 0.09 = 0.04 = 0.032 = 0.29 = 0.08 = 0.05 = 0.15 = 0.18 = 0.036 = 0.03 = 0.08 = 0.05 = 0.07 = 0.01 = 0.1 ST ST ST ST ST ST ST

F θ F θ θ θ R θ R θ θ θ θ θ = 9.78 % var F θ R θ θ θ θ θ θ F 400 8 2400 1700 1200 8 Spatial scale (km) Genetic structure3000 3000 Nm3000 IBD >3000 1800 840 8 8 8 500 35 and Lord Howe and Lord Howe Island Madeira and Canary Islands Bahamas GBR N Atlantic 5000 Geographic location Mediterranean, NE Australia, and ncDNA mtDNA Allozymes E Australia, GBR ncDNA mtDNA Microsatellites Caribbean and Allozymes E Australia, GBR 1200 Allozymes E Australia, GBR 1200 Allozymes E Australia, GBR 1200 P D Allozymes E Australia, GBR1200D AllozymesAustralia, E D Dev. Genetic system L Microsatellites P P P P P Microsatellites Genetic structure of populations of several marine invertebrate taxa reported in the literature marine invertebrate Genetic structure of populations of several sp. D Allozymes SW Australia

able 1 Hydrozoa Obelia geniculata A. palifera Anthozoa cuneata Acropora Haliclona T Species Porifera crambe Crambe A. palmata A. cytherea A. hyacinthus A. millepora A. nasuta

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RAFTING AND MARINE BIODIVERSITY ianna et al. 2003 ianna et al. 2003 ianna et yre & Hughes 2004 yre & Hughes 2000 yre & Hughes 2000 1996 Billingham & Ayre Ayre Billingham & Hunt & Ayre 1989 Ayre Hunt & 1996 Hellberg Ayre et al. 1991 et Ayre 1997 McFadden al. 1994 Russo et al. 2002 Bastidas et Edmands & Potts 1997 Ayre & Hughes 2004 Ayre Edmands & Potts 1997 Edmands & Potts 1997 Edmands & Potts 1997 V V al. 1994 Russo et Hellberg 1994 Hellberg 1996 Hellberg A A A es, on or algae or algae or algae or algae macroalgae (Bushing 1994) No No No No sY Ye No data No data No No Yes Yes No No YesNo No No Yes No No No ery large 1.31 No Infoeelgrass on Yes, 0.61 No No 0.53 No Infoeelgrass on Yes, 0.64 0.87 1.03 8.23 55.31 v 63.25 0.33 0.94 2.33 0.58 0.49 0.61 1.54 No dataeelgrass on Yes, 2.53 1.62 1.07 0.44 No Infoeelgrass on Yes, 0.94 6.33 12.25 0.64 0.0295 0.0045 = 0.434 = 0.21 = 0.262 = 0.375 0.42 No No = 0.042 5.7 = = = 0.16 = 0.29 = 0.32 = 0.28 = 0.22 = 0.195 = 0 = 0.004 = 0.3 = 0.34 = 0.29 = 0.14 = 0.09 = 0.134 = 0.189 = 0.36 = 0.21 = 0.038 = 0.02 = 0.28 ST ST ST ST ST ST ST

F θ θ θ θ θ θ F θ θ F F F θ θ θ θ θ θ θ θ F θ θ θ θ F 3000 1000 1150 0.024 1000 100 100 600 50 1000 30 4 2500 1700 1200 8 4000 2000 1150 GBR and Lord Howe and Lord Howe Island Brazil Brazil Allozymes SE Australia 735 Allozymes NE Pacific 1800 Allozymes SE Australia 930 Allozymes NE Pacific 1800 Allozymes SE Australia 1050 AllozymesAllozymes NE Pacific NE Pacific 1100 1800 AllozymesAllozymes NE Australia, NE Pacific 1800 Allozymes E Australia, GBR Allozymes Bermuda and P D P D D Allozymes California P Allozymes California P D P D D P Allozymes Brazil P D acyathus albocincta elegans stearnsii elegantissima koellikeri caissarum bermudensis Oulactis muscosa E. ritteri Anthothoe E. prolifera Balanophyllia Par A. tenebrosa Alcyonium rudyi Anthopleura Clavularia Epiactis lisbethae Bunodosoma A. valida Actinia

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MARTIN THIEL & PILAR A. HAYE gilio & Abbiati gilio & yre & Hughes 2004 yre & Hughes 2000 yre & Hughes 2000 yre & Hughes 2004 yre & Hughes 2000 yre & Hughes 2000 yre & Dufty 1994 yre & Hughes 2004 yre & Hughes 2000 yre & Hughes 2000 & Lasker 2004 & Lasker 2004 Gutiérrez-Rodríguez Jolly et al. 2003a Jolly et Ayre & Hughes 2004 Ayre Magalon et al. 2005 Magalon et A A A Stoddart 1984 A A A A al. 2001 Bastidas et & Hughes 2004 Ayre A A A al. 2003 Breton et Breton et al. 2003 Breton et Vir es, on pumice (Jokiel & Cox 2003) Rafting inferred Reference Y No No No sNo Ye Yes No No No No No Yes Yes No No No No data No No Yes No No No No data Yes No No data No 0.27 Yes No 4.21 12.91 1.42 24.75 (31) 6 1.27 1.067 0.84 1.42 0.64 0.33 38.21 9.37 5.85 1.42 9.37 2.53 1.14 0.47 2.33 0.165 0.04 6 = 0.43 = = = 0.48 = 0.19 = 0.23 = 0.15 = 0.28 = 0.056 = 0.019 = 0.15 = 0.01 = 0.04 = 0.0065 = 0.026 = 0.041 = 0.15 = 0.026 = 0.09 = 0.18 = 0.347 = 0.097 ST ST ST

θ θ θ θ θ F θ θ θ θ θ F θ θ θ θ θ θ θ % var = 45.3 % var θ θ F 450 2400 1700 1200 8 90 7.5 Spatial scale (km)2400 Genetic structure1200 8 Nm400 IBD 1300 30 4 2400 1700 1200 8 5500 2500 175 200 >30,000 = 0 % var and Lord Howe and Lord Howe Island GBR and Lord Howe and Lord Howe Island Mediterranean English Channel NW Atlantic, N Sea W Pacific, NE and W Pacific, GBR Geographic location SW Australia N Atlantic and Allozymes E Australia, GBR Microsatellites Indo-W Pacific 2000 Allozymes NE Australia, Allozymes E Australia, GBR Allozymes Microsatellites British coasts and mtDNA Genetic structure of populations of several marine invertebrate taxa reported in the literature marine invertebrate Genetic structure of populations of several P s.l. Microsatellites Bahamas D P Dev.GBR Genetic system D AllozymesAustralia, E P D D mtDNA P P meandrina able 1 (continued) ectinaria koreni elisabethae damicornis pistillata diversicolor Pseudopterogorgia Pseudopterogorgia Seriatopora hystrix Seriatopora P. T Species Pocillopora Sinularia flexibilis Styllophora Styllophora Polychaeta Hediste P Neanthes virens

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RAFTING AND MARINE BIODIVERSITY Wares et al. 2001 et Wares Duffy 1993 Duffy Wares et al. 2001 et Wares al. 2005 Pfeiler et Duda & Palumbi 1999 Duda & Palumbi 2002 Vannini Fratini & 1993 Duffy Ball & Chapman 2003 Barber et al. 2002 Barber et al. 1998 Zane et al. 1997 et Wilson Costa et al. 2004 Costa et al. 2002 Coelho et Jolly et al. 2003b Jolly et Sotka et al. 2004 Sotka et es, on macroalgae macroalage Y No weak No data No No data No No No No data No data 1.54 No data No 5.31 (*7.35) 0.41 largevery No No 3.08 0.25 0.38 0.21 No data No 1.27 4.14 = 0.38 = 0.87 0.037= 0 = 0.021 No 11.65 No No data No = 0.205 0.97 No No = 0.02= 0.075 = 0.505 12.25= 0.398 = 0.04 Yes, 6 = 0.074 = 0.057 = 0.164 1.27 No data on Yes,

= 0.14 = 0.54 = 0.045 5.31 (*1.9) No data No = 0.045 ST ST ST ST ST ST ST ST ST ST ST ST ST

Φ Φ θ Φ Φ F F F F θ F F F F θ θ Φ 500 4800 4800 800 100 8000 2000 >7500 >7500 4700 1500 600 lagoons and Red Sea and W Pacific Gulf of Mexico Indo-W Pacific 5000 E Pacific Circumantarctic >7000 E Indian Ocean California Gulf of Maine 160 W Indian Ocean Portugal California 1600 ncDNA RAPD mtDNA Allozymes SE British coastal mtDNA ncDNA mtDNA Microsatellites W Atlantic and Allozymes mtDNA and mtDNA D P mtDNA P Allozymes Caribbean P D P D Allozymes Caribbean P P P D RAPD P mtDNA P mtDNA enaeus monodon volutator pulchella bellicosus setiferus Peracarida Corophium Euphausia superba S. pectiniger Hoplocarida Haptosquilla Idotea chelipes Scylla serrata Synalpheus brooksi P Eucarida Callinectes Lithopenaeus Gammarus locusta Chthamalus fissus Cirripedia Balanus glandula

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MARTIN THIEL & PILAR A. HAYE 2000 1997 1994 1997 1997 1997 1997 1997 1997 2000 2000 Stevens & Hogg 2004 Stevens Stevens & Hogg 2004 Stevens Carvalho & Piertney & Piertney Carvalho & Piertney Carvalho & Piertney Carvalho & Piertney Carvalho De Matthaeis et al. De Matthaeis et Carvalho & Piertney & Piertney Carvalho & Carvalho Piertney & Piertney Carvalho & Piertney Carvalho De Matthaeis et al. De Matthaeis et al. De Matthaeis et macroalgae macroalgae macroalgae Rafting inferred Reference No No No weak No data No data No data No No data No No data No No data No 1.82 2.76 7.56 2.53 4.21 5.07 27.53 3.99 4.85 22.48 3 4.75 8.67 0.96 1.19 7.33 = 0.121 = 0.032 = 0.09 = 0.056 = 0.047 = 0.009 = 0.059 = 0.049 = 0.011 = 0.077 = 0.050 = 0.028 = 0.207 = 0.174 = 0.033 = 0.083 = 0.7= 0.66 0.11 0.13 Yes but Yes, No

= 0.071 3.27 No on Yes, = 0.198= 0.452 1.01 0.30 Yes No on Yes, on Yes, PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT ST ST ST

G F θ G F G G G G G G G G G G G G θ θ F G 100 0.06 100 0.06 100 0.06 100 0.06 Spatial scale (km)200 Genetic structure100 Nm100 IBD 0.06 Geographic location South Wales UK Anglesey, Allozymes Zealand New 1600 Allozymes UK Anglesey, 200 AllozymesAllozymes UK Anglesey, 200 Allozymes UK Anglesey, 200 UK Anglesey, 200 Allozymes Zealand New 1600 Allozymes UK Anglesey, Genetic structure of populations of several marine invertebrate taxa reported in the literature marine invertebrate Genetic structure of populations of several D D Allozymes Mediterranean >3000 D D D D DD AllozymesD Allozymes Mediterranean Mediterranean >3000 >3000 Dev. Genetic system D acorophium acorophium lucasi forsmani ischiosetosa nordmanni praehirsuta able 1 (continued) platensis montagui excavatum aera albifrons aera P. Platorchestia Platorchestia J. J. J. J. Orchestia O. stephenseni Par T Species J

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RAFTING AND MARINE BIODIVERSITY Gofas 1999 Gofas 1999 Gofas 2000 Collin 2001 Collin 2001 Collin 2001 Collin 2001 Hoskin 1997 & Boisselier-Dubayle & Boisselier-Dubayle Hoskin 1997 al. 2003 Andrade et 2000 & Davis Wilke 2000 & Davis Wilke Baratti et al. 2005 Baratti et al. De Matthaeis et al. 2003 Andrade et mangrove mangrove woods macroalgae mangrove trees (David Reid, pers. comm.) Yes No YesYes seagrass on Yes, Collin 2001 NoNo No No No on Yes, No on Yes, 0.04 0.18 = 0.85 = 0.58 = 0.14= 0.582 1.54= 0.158 0.18= 0.52 May be 1.33 Yes No data 0.23 No No data No May be Yes = 0.054= 0.25 4.38= 0.41 0.75 Yes= 0.185 0.36 No No 1.1 Yes Yes Yes

= 0.843 0.05 Yes on Yes, ST ST ST ST ST ST ST ST ST ST

F F θ F F F F F F F F 4000 4000 162 180 6000 6000 30,000 500 coast coast coasts coasts and Mediterranean Florida USA NW AtlanticNW 1300 APV= 54.3 NW European NW European NW AtlanticNW AtlanticNW 1300AtlanticNW 4500 APV= 76.1 AtlanticNW 1300 APV= 87.2 2600 APV= -7,4 APV= 22.1 E Africa and mtDNA mtDNA mtDNA mtDNA mtDNA mtDNA mtDNA mtDNA PCJ Allozymes Allozymes Mediterranean SE Australian 1750 D Allozymes Mediterranean >3000 CJ Allozymes SE Australian D Allozymes MediterraneanD 1750 P D D Allozymes Brazil D L P P P Allozymes Brazil D lineolata lividulum atrasolea angulifera Northern species Southern species lineolata** terebrans alitrus saltator C. vulgatum Cominella T Prosobranchia hanleyi Bedeva Cerithium Crepidula ulvae Hydrobia H. ventrosa Littoraria C. convexa C. convexa C. convexa C. depressa C. fornicata Echinolittorina Sphaeroma Sphaeroma

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MARTIN THIEL & PILAR A. HAYE atarenkov 1997 atarenkov yle & Boulding 2000 T Kyle & Boulding 2000 Boulding & Kyle Waters et al. 2005 et Waters Kyle & Boulding 2000 Kyle Johnson & Black 1998 Hoskin 1997 Kyle & Boulding 2000 Kyle Marko 2004 Marko Janson 1987a K Andrade et al. 2003 Andrade et Janson 1987a Janson 1987b Johannesson & al. 2004 Johannesson et ) intertidal rockweeds (Fucus distichus mangrove mangrove trunks (David Reid, pers. comm.) (Johannesson et al. 2004) Rafting inferred Reference No Yes Yes sNo No No No No No No Yes Ye Yes No data Yes Yes Very largeVery largeVery No No No on Yes, 7.81 11.66 18.98 2.96 2.38 2.88 = 0.065 3.6 = 0 = 0 = 0.12 1.83 Yes No = 0.021= 0.078 11.66= 0.095 No No = 0.008 = 0.028 8.68= 0.031 = 0.021 Yes= 0.013 on Yes, = 0.017 14.46 May be Yes

ST ST ST ST PT PT PT ST ST ST ST ST ST G Φ G F F F = 0.11 % var F G G Φ F Φ % var = 8.6 % var Φ 4000 300 300 75 150 1120 160 2000 = 0.84 % var 162 Spatial scale (km) Genetic structure Nm IBD asmania and Australia, oster archipelago T Zealand New coast NE Pacific 3600 NE Pacific 245 NE Pacific 745 NE Pacific 3600 W Swedish coast K W Swedish coast W Swedish coast NW Pacific 5000 = 0.06 % var Geographic location RAPD mtDNA Allozymes Swedish coast 300 Allozymes NW Australia 1500 S mtDNA haplot. mtDNA seq. mtDNA Allozymes SE Australian mtDNA mtDNA mtDNA Genetic structure of populations of several marine invertebrate taxa reported in the literature marine invertebrate Genetic structure of populations of several D Allozymes D P P P D P P Dev. Genetic system P Allozymes Brazil P D able 1 (continued) marginalba L. saxatilis L. sitkana L. littorea Littorina cingulata Nerita atramentosa Nucella lamellosa Morula L. plena T Species L. flava L. scutulata L. subrotundata

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RAFTING AND MARINE BIODIVERSITY odd et al. 1998, odd et 1984a,b al. 2003 Lambert et Lambert et al. 2003 Lambert et 1997 2003 2004 1997 Johnson & Black Allcock et al. 1997 Allcock et Todd et al. 1998, et Todd Murray-Jones & Ayre Ayre Murray-Jones & al. Luttikhuizen et Hare & Weinberg 2005 Weinberg Hare & Benzie 1999 Colson & Hughes Marko 2004 Marko Benzie & Williams Williams Benzie & T (Todd et al. et (Todd 1998) No sNo one of the 4 loci Ye Only No on fucoids Yes, No Yes No No No data No 6.89 0.67 227.02 138.64 131.33 77.87 57.89 0.22 No data No 0.58 1 largevery No No 2.02 3.92 1.35 2.73 83.08 0.0090.669 27.53 0.12 No No data No No = 0.338 0.49 No No = 0.0011 = 0.0018 = 0.0019 = 0.0032 = 0.0043

= = = 0.035 = 0.273 = 0.54 = 0.3 = 0.2 = 0 = 0.11 = 0.06 = 0.156 = 0.084 < 0.003 ST ST ST ST ST ST ST ST

θ θ F F F F θ θ θ θ F F Φ θ = 7.31 % var θ = 5.44 % var F % var = 0.08 % var θ θ θ 700 10,000 26 18,000 0.15 500 50 10 0.05 2600 <700 Indian Oceans, GBR Alaska N Europe and NW Atlantic 4500 NW Pacific 5000 = 0.05 % var Allozymes and E Pacific AllozymesAllozymes British Isles British Isles 1600 1600 Allozymes SE Australia 1200 mtDNA mtDNA Microsatellites British coasts 1600 Allozymes W Australia 2500 mtDNA haplot. mtDNA seq. mtDNA Allozymes Indo-W Pacific >5000 P D AllozymesGeorgia South 0.15 L P P P P D P D P eledone turqueti ridacna maxima solidissima Asteroidea Acanthaster planci T Opisthobranchia Adalaria proxima Goniodoris nodosa Bivalvia Donax deltoides Macoma balthica Spisula s. N. lapillus Siphonaria jeanae N. ostrina Cephalopoda Par

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MARTIN THIEL & PILAR A. HAYE illiams & Benzie aters & Roy 2004a aters & Roy 1998 1996 Lessios et al. 2001 Lessios et al. 2001 Lessios et Williams & Benzie Williams Hunt 1993 Waters & Roy 2004b & Roy Waters al. 2001 Lessios et al. 2001 Lessios et Baus et al. 2005 Baus et W W Hunt 1993 Perrin et al. 2004 Perrin et al. 2003 Sköld et es, on es (Waters & es (Waters comments by R. Emson macroalgae or wood Roy 2003) Roy Rafting inferred Reference No No Y sY No Yes Yes No Ye No data No No data No 3.92 No No 6 2.25 0.96 (1.9) 0.87 (1.7) 124.75 1.4 3.85 9.75 0.15 0.29 12.25 largevery No No = 0.152 = 0.224 = 0.395 0.38= 0.061 = 0.025 Yes personal (Yes), = 0.072 3.22 Yes No

= 0.06 = 0.04 = 0.1 = 0.002 = 0.62 = 0.46 = 0.02 = 0 = 0.0008 312.25= 0.462 No 0.29 No = 0.206 ST ST ST ST ST ST

θ θ θ F θ Φ F θ θ θ θ θ = 0.9 % div = 1.8 % div = 3.2 % div θ F θ Φ F 35,000 12,000 2500 >1000 2000 270 10,000 5000 7000 600 1900 3800 230 1400 12,500 10,500 12,500 Spatial scale (km)1000 Genetic structure Nm IBD W and C Pacific W Oceans fiords Galápagos Australia and Tasmania coasts coasts and Mediterranean Pacific and Indian Pacific E Pacific, E Pacific, Indian Ocean, New Zealand New W and E Atlantic W and E 14,000 New Zealand New S Africa, S Indian Ocean Indo-W Pacific Geographic location NW European mtDNA mtDNA Allozymes mtDNA mtDNA Allozymes SE AustraliaAllozymes 230 mtDNA Allozymes Genetic structure of populations of several marine invertebrate taxa reported in the literature marine invertebrate Genetic structure of populations of several P P P mtDNA P P P D mtDNA P P RFLP Dev. Genetic system CJ AFLP gularis xigua re able 1 (continued) atiriella calcar muricata antillarum P. e D. savignyi D. paucispinum Coscinasterias Echinoidea Diadema D. mexicanum P. P Linckia laevigata Linckia T Species Asterina gibbosa

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RAFTING AND MARINE BIODIVERSITY McMillan et al. 1992 McMillan et Lessios et al. 1998 Lessios et al. 2000 et McCartney al. 1997 et Palumbi al. 1997 et Palumbi al. 2000 et McCartney al. 2000 et McCartney al. 2004d Duran et Arndt & Smith 1998 McMillan et al. 1992 McMillan et Arndt & Smith 1998 Edmands et al. 1996 Edmands et 2002 Sponer & Roy al. 2001 Féral et es, on grass Phyllospadix scouleri (Hobday 2000a) macroalgae or debris (Sponer 2002) & Roy Y es, but es, but low No data No Y No data on algae Yes, al. 2002 Porter et No No data No 3.66 24.75 11 0.31 1.42 0.15 0.49 = 0.05= 0.97 4.75 (10) 0.01 (0.017) No data No data No on surf Yes, = 0.62 = 0.34 = 0.12 1.83 No data No = 0.064 = 0.01 = 0.022 = 0.261= 0.389 0.71= 0.306= 0.057 0.39= 0.361 0.57 No data 4.14 No 0.44 Yes= 0.01 Yes No data No = 0.03 No data No No 24.75 No 8.08 No No data No on algae Yes, = 0.15 = 0.077 3

= 0.45 ST ST ST ST ST ST ST ST ST ST ST ST ST ST ST ST ST F Φ F F F F F F F G F Φ F Φ F F G G 2600 870 1600 0.003 10,000 3400 1500 >5000 >5000 2000 4700 Brazil Tasmania Islands NE PacificNE 2350 Indo-W PacificIndo-W PacificE Pacific >10,000 >10,000 NE Pacific 2300 Caribbean and Caribbean SW Europe 5000 New Zealand New W Mediterranean Australia and California IslesBritish 800 N Pacific Ocean N Pacific mtDNA RFLP and mtDNA RAPD mtDNA mtDNA mtDNA mtDNA Allozymes and mtDNA Allozymes and mtDNA mtDNA D P P P P PP s.l. RFLP mtDNA P P mtDNA L RAPD D P P P RFLP Australia E 3400 acentrotus acentrotus squamata lucunter erythrogramma purpuratus gelatinosum diadema lividus Ophiuroidea Amphipholis Echinometra Echinometra E. mathaei E. oblonga E. vanbrunti E. viridis Heliocidaris Strongylocentrotus Holothuroidea Cucumaria miniata (Bryozoa) Ectoprocta Alcyonidium C. pseudocurata Echinothrix Echinothrix Par H. tuberculata

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MARTIN THIEL & PILAR A. HAYE lecular marker Goldson et al. 2001 Goldson et Porter et al. 2002 Porter et al. 1997 et Ayre al. 1997 et Ayre al. 1997 et Ayre Schwaninger 1999 Schwaninger Goldson et al. 2001 Goldson et en by authors is presented), velopment, mo velopment, gence; APV = among population gence; ver ae; CJ = crawling juveniles; s.l. = short juveniles; ae; CJ = crawling (Aliani & Molcard 2003) (Vallentin (Vallentin 1895, Todd et al. 1998) Rafting inferred Reference Yes No No data on plastic Yes, No on algae Yes, differ from those calculated by us are given in parentheses. from those calculated by us are given differ f the genetic studies from which population differentiation netic differentiation data are available (most were calculated netic differentiation data are available 0.09 12.91 17.61 = coefficient of gene differentiation between populations; * = CME or cladistic of gene differentiation = coefficient

PT G = 0.105 2.13 No data No = 0.202= 0.002 0.99= 0.210 124.75 Yes 0.94 No No No Yes No

= 0.726 = 0.019 = 0.014 ST ST ST ST

F F F θ θ θ F ferentiation (genetic structure) among populations (original parameter giv 14,000 4600 2200 Spatial scale (km) Genetic structure Nm IBD velopment; L = short-lived lecitotrophic larvae; CL = crawling larv CL = crawling lecitotrophic larvae; L = short-lived velopment; A; % var = percentage of molecular variance; % div = percentage sequence di % div = percentage of molecular variance; A; % var ferent name. Wright (1969) (see text). Values of Nm provided by the authors that of Nm provided Values Wright (1969) (see text). and NW Atlantic and NW North WalesNorth 10 = 5.29 % var Geographic location British Isles 1500 North WalesNorth 10 = 0 % var (Excoffier et al. 1992); AGD= average genetic diversity; genetic diversity; average AGD= al. 1992); et (Excoffier

-like measure of population genetic differentiation. For each species information is included about its mode of de For measure of population genetic differentiation. -like ST ST F F RAPD AllozymesAllozymes SE Australia SE Australia 215 140 RAPD Allozymes SE Australia 190 Allozymes NE NE Pacific, RAPD Genetic structure of populations of several marine invertebrate taxa reported in the literature marine invertebrate Genetic structure of populations of several L P D P D P Dev. Genetic system P Most studies provided an Most studies provided

able 1 (continued) hyalina gibbosa magnicoecum membranacea ariance; approximately equal to Celleporella Celleporella gibbosa Pyura Stolonica australis Electra pilosa Electra v Tunicata Botrylloides Membranipora Membranipora T Species A. mytili Notes: **species reported by author under a dif migration events; presence or absence of an isolation by distance pattern (IBD), whether rafting has been inferred for the taxon and references o obtained. Nm was calculated using the equation of data was (genetic system) used to infer population structure, geographic location of the studies, spatial scales for which population ge in the literature), estimates of genetic dif from maps or coordinates provided Dev. = mode of development; P = planktonic development; D = direct de P = planktonic development; = mode of development; Dev. = nuclear DN ncDNA = mitochondrial DNA; mtDNA lived;

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Nm and geographic scale for which differentiation values where available were classified by mode of development of the studied species. The direct development categories included all organisms that brood their progeny up to a juvenile or crawl-away stage or that have very short-lived larvae (<2 days). All others were classified as organisms with planktonic larval development. Both broad developmental mode categories were further subdivided into organisms for which rafting is not known (No Rafting) and those organisms for which rafting has been reported in the literature or inferred based on available knowledge (Rafting). Log-scatter plots of Nm vs. geographic scale of the studies show that all categories of organisms (combinations of Direct/Planktonic development and Rafting/No Rafting) are highly variable in the degree of connectivity between distant popula- tions and that they can achieve extensive gene flow (Figure 28). As expected, most of the species with high realised gene flow over the greatest distances have planktonic larval stages (both rafters and non-rafters). However, contrary to classical expectations, several direct-developing species were also found to show high connectivity at intermediate-to-long distances. Thus, rafting is an important

100 Planktonic-Rafting Direct-Rafting Planktonic-No Rafting Direct-No Rafting

10 Nm

1

0.1 0110 100 1,000 10,000 100,000 Log geographic scale (km)

Figure 28 Relationship between the geographical scale and migration rate calculated as Nm according to

Wright (1969) for the species shown in Table 1 for which FST-like genetic measures were available. FST-like values that resulted in Nm values greater than 100 were all left at 100 migrants per generation. Horizontal dashed lines mark the limit between arbitrarily defined low (<1), medium (1Ð10) and high (>10 migrants per generation) levels of genetic connectivity. It is important to note that the geographical scale does not necessarily relate to the geographic range of distribution of species and that it corresponds to the scale at which population genetic differentiation values were available. The scatter plot shows that rafting leads to low-to-moderate and sometimes high levels of genetic connectivity at a broad range of geographic scales. The oval groups Nm values of most rafters with direct development (33 of 37 reports; 89.2%) and shows that rafting has a strong impact on connectivity of direct-developing species between 10 and up to almost 10,000 km, leading to medium Nm values. The triangle groups all 12 reports (100%) of rafters with planktonic development. There is an area of overlap between the oval and the triangle and then the triangle also encompasses an area of medium to high connectivity from 100 to almost 10,000 km.

387

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MARTIN THIEL & PILAR A. HAYE

Planktonic-Rafting Geographic scale (km) Direct-Rafting Planktonic-No Rafting 0-100 100-1,000 1,000-5,000 >5,000 Direct-No Rafting 6 10 16 3

High Nm (>10)

21 21 35 4

Medium Nm (1-10) Connectivity (Nm)

4 12 26 12

Low Nm (<1)

Figure 29 Contribution of rafting to genetic connectivity at different geographical scales. Values of Nm for different species shown in scatter plot (Figure 28) were classified according to level of connectivity and geographic scale. Levels of connectivity estimated as number of migrants per generations were low (<1), medium (1Ð10) and high (>10). The pie charts within each cell represent the proportion of organisms in each of the four categories of organisms (Rafting/No rafting and Direct/Planktonic development) that are charac- terised by low, intermediate and high migration rates (Nm). Numbers in the upper left corners indicate the total number of species for which population differentiation data were available at each geographical scale; note that for some species data were available for more than one geographical scale, so the total adds up to more than 113. When more than one Nm value was available for the same geographical scale and species, the Nm was recalculated from the average genetic differentiation.

means of dispersal for many brooders at different geographic scales (Figure 28). The impact of rafting on migration rates of marine invertebrates at different spatial scales (0Ð100, 100Ð1000, 1000Ð5000, and >5000 km) can be further explored in Figure 29 where data are presented as the number of species of each of the four broad categories that achieve high (>10), intermediate (1Ð10) and low (<1) levels of gene flow measured as Nm at the different spatial scales. While most direct developers were reported to have low levels of gene flow (35 of all 81 species that have direct development), there are several reports of moderate to high levels of gene flow among direct developers at intermediate distances (1000Ð5000 km) (17 out of 51 species), and many of these are species for which rafting has been inferred (8 out of 17 species). It is important to acknowledge that rafting may be unrecognised as a dispersal means for many species and its contribution is likely to be underestimated. A detailed overview of the studies that have reported population genetic differentiation for species for which rafting has been inferred (Table 1) will now be given. The examples presented are partitioned according to the four geographic scales previously defined (Figure 29). It is worth noting that the scale at which a species is described herein reflects the spatial scale used in the respective study and it does not necessarily correspond with its entire geographic range of distri- bution. The geographical scale at which rafting has important effects on population connectivity will depend on local conditions and the species considered. As shown in Figure 1 and Figure 2, rafting may be an important factor to consider at varying levels of a continuum of biological processes from local population dynamics to cladogenesis.

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Rafting-mediated connectivity at the geographic scale of 0Ð100 km

Rafting has been invoked as a means of dispersal at this geographic scale only for direct developers, including the anthozoans Balanophyllia elegans from California (Bushing 1994, Hellberg 1996) and Pocillopora damicornis from the Great Barrier Reef (GBR) in eastern Australia (Ayre & Hughes 2000, Jokiel & Cox 2003), the mesogastropod Littorina saxatilis from the western Swedish coasts (Johannesson & Tatarenkov 1997), the neogastropod Nucella lapillus from the British coasts (Colson & Hughes 2004), the nudibranch Adalaria proxima from the northeastern Atlantic (Todd et al. 1998), the isopod Idotea chelipes from southeastern British coastal lagoons (Jolly et al. 2003b), and the brittle star Amphipholis squamata from the western Mediterranean (Féral et al. 2003). Balanophyllia elegans, commonly known as the orange cup coral, has direct development and has been reported rafting on macroalgae on the coast of California (Bushing 1994). Gene flow between populations of B. elegans separated by approximately 100 km is sufficient to prevent local genetic differentiation (Nm = 1.03) (Hellberg 1996), while at greater distances (1000Ð5000 km) gene flow is slightly lower (see below). According to Ayre & Hughes (2000) both restricted dispersal among populations and inbreeding contribute to the fine-scale genetic structure in Pocillopora damicornis from the GBR (Ayre & Hughes 2000), a brooding coral that is presumed to have high dispersal potential through rafting on pumice (e.g., Jokiel & Cox 2003) (Figure 20). Over a local scale of 8 km along the GBR, the genetic differentiation data of P. damicornis do not demonstrate an IBD pattern and translate to high gene flow (Nm ~ 6; Ayre & Hughes 2000). In both these anthozoans, frequent rafting routes may be contributing to population connectivity at a local spatial scale, counteracting the effects of genetic drift, and thus becoming an important evolutionary agent at this spatial scale. For the direct-developing rough periwinkle, Littorina saxatilis, Johannesson & Tatarenkov (1997) reported genetic differentiation values at the scale of 75 km for western Sweden, consistent with two to five migrants per generation. Johannesson et al. (2004) suggested that rafting may be a means of dispersal for this species. Colson and Hughes (2004) found that the egg-laying dog whelk Nucella lapillus of the British coasts lacks a pattern of IBD and that medium distance movements (10Ð150 km) are relatively common (Figure 20). Rafting is considered to be contributing to the high levels of gene flow among populations of this direct developer. The nudibranch Adalaria proxima may occasionally be dispersing by rafting on fucoids, either as adults or as egg-masses (Todd et al. 1998). Populations of A. proxima separated by 26 km display sufficient gene flow to prevent population differentiation (Nm = 1; Todd et al. 1998, Lambert et al. 2003). However, the authors observed a significant IBD pattern, possibly because at this scale dispersal is mostly via the larval stage and “the larvae are behaviourally constrained from becoming pelagic, or remain epibenthic, and thereby are subject to only restricted dispersal” (Todd et al. 1998). At this geographic scale, populations of the isopod Idotea chelipes from British coastal lagoons show gene flow levels of 1.27 migrants per generation (Jolly et al. 2003b). The authors suggested that the outer coast may act as a barrier to gene flow between bays leading to the observed genetic differentiation. They recognised rafting as a possible means for LDD, but since lagoons are the typical habitat of I. chelipes along the British coast and are discontinuously distributed, the likeli- hood to reach suitable habitats through rafting once leaving the lagoon is low (Jolly et al. 2003b). All the examples given above fit well with connectivity levels resulting from dispersal through frequent rafting routes (or possibly strong intermittent routes), that as defined were predominant at distances of 0Ð100 km. Contrary to this, the brooding brittle-star Amphipholis squamata has very low gene flow at this geographic scale. Rafting has been inferred for this species (on macroalgae or debris, see Sponer & Roy 2002), even though for a very small scale of 3 m local gene flow is very low (Nm = 1.42). Thus, rafting does not seem to be considerably affecting population structure of A. squamata at a microgeographic scale, possibly due to the fact that the rafting routes of the

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MARTIN THIEL & PILAR A. HAYE

species may be episodic, and thus be contributing to the worldwide distribution of the species and speciation (see below). It is possible that many more direct developers than reported are also dispersing via rafting at this geographic scale. In the previous section, it was argued that at a small geographic scale, frequent rafting routes could lead to high connectivity among local populations for example within a bay or a system of bays. It is likely that many more brooders than presently reported use frequent rafting routes to disperse at distances under 100 km (e.g., within bays or estuaries) and that rafting accounts for most of the connectivity among populations of benthic marine brooders at this geographic scale.

Rafting-mediated connectivity at the geographic scale of 100Ð1000 km

The levels of gene flow of the orange cup coral, Balanophyllia elegans, at a scale of 1000 km are sufficiently low to allow population differentiation (Nm = 0.87). Pocillopora damicornis, the brooding coral from the GBR also mentioned in the previous section as having high gene flow at a microgeographic scale, maintains connectivity presumably through rafting on pumice with at least one migrant per generation at a scale of 400 km (Stoddart 1984) (Figure 20), which is sufficient to prevent significant genetic differentiation. Intermittent rafting routes are probably ensuring genetic connectedness among populations located 400 km apart, and thus, it is up to this scale or further that rafting is affecting the metapopulation structure of P. damicornis. Additionally, Stoddart (1984) did not find a significant association between genetic and geographic distance for this species (i.e., no IBD). This pattern might be the consequence of LDD of individuals via an intermittent rafting route in a leapfrog fashion (Figure 13). Colonies of the bryozoan Alcyonidium gelatinosum from the British Isles have been found on Fucus serratus and presumably have the potential for rafting on this or other macroalgae (Porter et al. 2002). This species has a short-lived lecitotrophic larva that probably only allows for home range dispersal. At the spatial scale of 800 km this bryozoan displays levels of genetic differentiation consistent with an average gene flow of three migrants per generation. This value is comparable to the migration rate of a sympatric congener with planktonic development (Porter et al. 2002). Rafting has also been invoked at this geographic scale for several gastropods. The gastropods Bedeva hanleyi and Cominella lineolata from the coast of southeastern Australia have crawling larvae with very restricted dispersal and are thought to disperse via plankton or by rafting on substrata such as logs and algae (Hoskin 1997). The Nm of Bedeva hanleyi is 1.54 at 180 km, while Cominella lineolata only has an Nm of 0.23 at a similar spatial scale. It may be that Bedeva hanleyi is a better rafter and can make better use of intermittent rafting routes for dispersal than Cominella lineolata, achieving sufficient gene flow at a scale of 180 km, to prevent genetic differentiation. Estimated gene flow for the direct developing Littorina saxatilis over 300 km of the Swedish west coast and in the Koster Archipelago is approximately 2.67 migrants per generation (Janson 1987a,b). The isopod Sphaeroma terebrans shows relatively low levels of gene flow over 500 km along the East African coast (Nm = 0.18; Baratti et al. 2005). These isopods spend most of their lives in mangrove roots and they are presumed to raft when roots break off and float away. In spite of this, populations of S. terebrans appear to comprise ancient lineages with restricted dispersal, as evi- denced by their strong genetic differentiation (Baratti et al. 2005) (Figure 12). Successful rafting dispersal on this geographic scale may be limited in this species by the low probability of reaching suitable environments via rafting along the outer coast on detached mangrove roots (Figure 5). Along a stretch of 500 km of the Portuguese coast, populations of the amphipod Gammarus locusta show low population differentiation, attributable to relatively high levels of gene flow in the area (Coelho et al. 2002, Costa et al. 2004). This is a direct-developing species associated with

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macroalgae and “loose-lying bunches of drift-macroalgae” (Costa et al. 2004), and the low genetic differentiation could indicate that G. locusta achieves gene flow (between 3.13 and 4.14 migrants per generation) through rafting. According to the authors “drifting attached to macroalgae is probably an important means of dispersal for this species” (Costa et al. 2004). The seastar Asterina gibbosa releases crawling juveniles with low dispersal potential, although it has been inferred to raft occasionally (Baus et al. 2005, R. Emson personal communication). At a scale of 1000 km it exhibits low levels of connectivity (Nm = 0.38) (Baus et al. 2005). All the examples given above fit the predictions of intermittent rafting routes, allowing more or less connectivity at this mesogeographic scale depending on the strength and frequency of the rafting connection. Weak intermittent or episodic rafting routes seem to be the cause of low levels of connectivity (0.29 migrants per generation) (Hunt 1993) of populations of the brooding starfish Patiriella exigua along 230 km of the southeastern Australian coasts. Even though it is thought to disperse via rafting on macroalgae or wood (Waters & Roy 2004a), the levels of connectivity are low but sufficient to maintain the geographic range of distribution, yet possibly contribute to speciation in the long term (see section on episodic rafting routes). The high genetic structure found for P. exigua that is not clearly associated to geographic distance (Hunt 1993) is consistent with rafting dispersal, although not very frequent, as has been suggested by Waters & Roy (2004a). As can be observed in Figure 28 and Figure 29, around 100Ð1000 km there are many brooders that achieve intermediate-to-high levels of gene flow, some of which have not been inferred as rafters. It is likely that many more direct-developing species than those that have so far been reported disperse via intermittent rafting routes at this spatial scale. Species with planktonic development that are thought to raft (based on non-genetic data) may also be achieving high gene flow via rafting at this scale. For example, the rafting gastropod Morula marginalba from southeastern Australia has high gene flow (Nm = 14.46) at a scale of 160 km (Hoskin 1997). The urchin Strongylocentrotus purpuratus, which also has been found on floating algae on the coasts of California (Hobday 2000c), exchanges at least 8 migrants per generation at a scale of 870 km (Edmands et al. 1996). Finally the seastar Coscinasterias muricata achieves a connectivity of 9.75 migrants per generation along the New Zealand fjords (Sköld et al. 2003). For all these species, rafting through intermittent routes probably represents an additional means of dispersal that may ensure connectivity even when environmental conditions do not allow for successful larval-mediated dispersal and in these cases the rafters are most likely the juveniles or adults.

Rafting-mediated connectivity at the geographic scale of 1000Ð5000 km

There are many examples of direct-developing species, which presumably are dispersed by rafting at this geographic scale, including bryozoans (Hellberg 1994), anthozoans (Hellberg 1994, 1996; Ayre & Hughes 2004; Govindarajan et al. 2005), actiniarians (Edmands & Potts 1997), gastropods (Kyle & Boulding 2000, Andrade et al. 2003, Colson & Hughes 2004), peracarids (De Matthaeis et al. 2000, Stevens & Hogg 2004), holothurians (Arndt & Smith 1998), asteroids (Baus et al. 2005) and ophiurids (Sponer & Roy 2002). At a scale of 3000 km the orange cup coral Balanophyllia elegans has lower values of Nm (= 0.64) than those reported for shorter distances (Hellberg 1994). Rafting may have similar effects at this spatial scale to what was described at the scale of 1000 km for this species (i.e., intermittent rafting routes may allow for gene flow, albeit low, among distant populations). The brooding coral Pocillopora damicornis from the GBR has an Nm of 1.42 (only slight levels of genetic differenti- ation) at a scale of 2400 km (Ayre & Hughes 2004), which possibly is a consequence of pumice rafting given the geographic distance (see also above) (Figure 20). This species has high levels of gene flow at the scale of 0Ð100 km, which decreases at the scale of 1200Ð3000 km, but were still slightly sufficient to prevent significant genetic differentiation. The directly developing anemones

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of the genus Epiactis from the coasts of British Columbia to Southern California show a lower connectivity among populations at this geographic scale. With only 0.44Ð1.31 migrants per gener- ation on average, at the scale of 1800 km these species show overall low levels of migration (Edmands & Potts 1997). However, some LDD dispersal is expected, especially for E. ritteri that has the highest Nm value (sufficient to prevent genetic differentiation), which may be achieved through rafting on algae. Littorina sitkana, which also has been inferred to raft at this spatial scale (3600 km), has a

very high Nm (FST = 0) (Kyle & Boulding 2000). The authors suggested that in the northeast Pacific “rafting of egg masses or adults on floating rockweed may account for long-range gene flow between populations after winter storms, which dislodge the rockweed”. They also discuss that there may have been severe bottlenecks or local extinctions and recolonisations, which could account for the low intra- and high interpopulation variation (Kyle & Boulding 2000). Indeed rafting may lead to repeated colonisations that could be followed by founder effects, reducing within-population dif- ferentiation (see Harrison & Hastings 1996). Andrade et al. (2003) found that the ovoviviparous gastropod Littoraria angulifera from man- groves and rocky shores of the Brazilian coast does not show a significant correlation between geographic and genetic distances within a 4000 km stretch of coast. The levels of gene flow are sufficient to prevent differentiation, accounting for 1.1 migrants per generation on average (Andrade et al. 2003). The authors conclude that there is random geographic dispersal of individuals but that the lack of IBD could also be due to a strong effect of genetic drift in addition to the effects of gene flow (Andrade et al. 2003). Dispersal of L. angulifera could be achieved through rafting: “Littoraria angulifera is an ovoviviparous species that inhabits trunks, branches and leaves of mangrove trees, and it therefore is likely to raft on driftwood or even floating foliage” (David Reid, personal communication). Given the reported connectivity among populations of L. angulifera from Brazilian mangroves (preventing significant genetic differentiation), it could be inferred that rafting routes, which may not be very strong or permanent, connect these populations. Possibly, climatic oscillations could favour temporary formation of strong intermittent rafting routes, leading to the low but detectable differentiation levels. The previously mentioned study of Nucella lapillus from the British coasts also revealed a lack of IBD at the scale of 1600 km, suggesting considerable gene flow (Nm = 2; Colson & Hughes 2004) (Figure 16). The authors state that “populations of N. lapillus seem to fit a migrant model (with high numbers of colonists from several source populations) of dispersal rather than a stepping- stone”. Rafting was suggested as a mechanism of dispersal for this brooding gastropod, and based on genetic diversity it could be predicted that there is not a single but rather many source populations. This is likely to be the case with intermittent rafting routes that could allow connectivity among populations, maybe seasonally or permanently. The nudibranch Adalaria proxima, which exhibits IBD at a scale of 26 km, shows a lower connectivity at a scale of 1600 km around the British Isles (Nm = 0.58), but nevertheless sufficient to prevent very high levels of differentiation among distant populations (Todd et al. 1998). Possibly, over these distances, rafting dispersal gains in importance over larval dispersal, which seems to dominate the population dynamics at smaller spatial scales (see above). De Matthaeis et al. (2000) reported differentiation data for four species of amphipod peracarids at a geographic scale of 3000 km along the Mediterranean coast and suggested that for these species rafting may occur via floating wracks. Of the four, Orchestia montagui and Talitrus saltator have a genetic differentiation following an IBD pattern, while the other two, Orchestia stephenseni and Platorchestia platensis do not display a significant association between genetic differentiation and geographic distance at the studied spatial scale. The last species shows the greatest Nm value (3.27). Consequently, dispersal of P. platensis may be through strong intermittent and frequent rafting routes.

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The brooding holothuroid Cucumaria pseudocurata has been found on clumps of surf grass of Phyllospadix scouleri (Arndt & Smith 1998) and might sporadically disperse by rafting. However, over approximately 2300 km of the Pacific coast of North America, Arndt & Smith (1998) found a genetic differentiation consistent with very low dispersal (Nm = 0.17). If this species is dispersing by rafting, the rate of dispersal is very low compared to the generational time. Thus, populations feature high genetic differentiation but maintain widespread populations over time, even though some of the local populations may eventually speciate. The rafting routes connecting distant populations may be highly unstable and only establish when a series of favourable conditions are met. Similarly, Sponer & Roy (2002) proposed that the cosmopolitan brooding brittle-star Amphiph- olis squamata effectively disperses by rafting on macroalgae. They reported low gene flow (Nm = 0.31) at a scale of 1600 km along the coast of New Zealand, and conclude that epiplanktonic transport is an important dispersal mechanism for A. squamata in New Zealand, which may account for the widespread distribution of lineages. Results from Le Gac et al. (2004) challenge the rafting hypothesis proposed by Sponer & Roy (2002) and conclude that the “worldwide distribution of some clades only reflects the antiquity of clades, which are composed of several species”. However, paleo-rafting and current rafting may still be the means of dispersal for this species that could have promoted its widespread distribution. Episodic rafting routes could allow sporadic or singular connectivity events that maintain the geographic range of distribution of lineages or lead to the divergence of lineages in isolation. A similar scenario could be inferred for Patiriella exigua. Waters & Roy (2004a) suggested that P. exigua could have dispersed from South Africa eastward across the Indian Ocean rafting on macroalgae or wood with assistance of the West Wind Drift (Figure 24). They found that the DNA sequences of individuals in South Africa are paraphyletic (suggested as the source population) while the Australian are monophyletic. Additional evidence of LDD comes from the Amsterdam Island population that is isolated (>3000 km) and whose haplotypes are more divergent than the ones from closer islands. Even though episodic rafting- mediated gene flow is inferred for this species, local levels of connectivity are low enough to allow genetic differentiation (Colgan et al. 2005). Indeed, “the population structure of P. exigua indicates that effective recent migration between New South Wales, Tasmania and South Australia has been so low that complete lineage sorting of haplotypes to regions has occurred” (Colgan et al. 2005). There are also a few species with planktonic development that are inferred to raft, and where rafting may contribute to connectivity at this scale. For example, the actiniarian Anthopleura elegantissima, distributed from British Columbia to Southern California, is suggested to raft on eelgrass or algae and 1.54 migrants per generation are inferred from genetic differentiation data (Edmands & Potts 1997). The bryozoan Membranipora membranacea, frequently found growing on positively buoyant kelp and plastics, exchanges more than 15 individuals per generation at a scale >3000 km. The snail Littoraria flava may disperse by rafting at this geographic scale as it lives on mangrove trunks (as well as rocks) (David Reid, personal communication) and high connectivity among populations located 4000 km apart corresponds to 8.68 migrants per generation (Andrade et al. 2003). Rafting may also contribute to the connectivity of the populations of the seastar Coscinasterias muricata at this geographic scale (Waters & Roy 2003). Distances involved (1000Ð5000 km) may be extensive requiring long voyages (possibly exceeding the lifetime of planktonic larvae of many species), and rafting may permit some connectivity among their popu- lations at these geographic distances. Particularly interesting is the case of the widely distributed hydrozoan Obelia geniculata. This species has a relatively short-lived lecitotrophic planula larvae and the asexually produced medusa lives for approximately 1 month (Stepanjants et al. 1993, cited in Slobodov & Marfenin 2004). At least for the White Sea, these medusae are expected to disperse only for about 3Ð4 km, but the dispersal distance will depend on the speed and direction of the currents (Sergei Slobodov, personal

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communication). The hydroids grow on various substrata, including macroalgae, offering the possibility for rafting. In fact, O. geniculata has been inferred as a rafter in many regions of the world (see references in Thiel & Gutow 2005b). Within the North Atlantic and based on genetic data, Govindarajan et al. (2005) proposed as the most likely scenario that populations from Canada and Iceland had been sheltered in northern glacial refugia, and subsequently expanded southward. In general they found high genetic differentiation among the four North Atlantic populations studied (Massachusetts, New Brunswick, Iceland and France), with the exception of the New Brunswick and Iceland populations, which also share many unique haplotypes (Figure 30). This further supports the suggestion of a rafting route connecting the North American and Icelandic populations (see also Ingólfsson 1992, Wares & Cunningham 2001). The Massachusetts population, on the other hand, only has haplotypes shared with New Brunswick, suggesting recent southern expansion of the New Brunswick population (Govindarajan et al. 2005), possibly also achieved through rafting. In summary, rafting has been invoked as an important means of dispersal for many species at the geographic scale of 1000Ð5000 km, showing an impact on the realised dispersal among populations of directly developing species (Figure 28 and Figure 29). Most of the examples given above correspond well with the predictions of intermittent rafting routes, bearing in mind that some of these routes may be stronger or more permanent in time than others and that this leads to varying levels of connectivity among populations at this geographic scale. These rafting routes are crucial for direct-developing species whose metapopulation structure is controlled by migration at this macrogeographic scale.

Rafting-mediated connectivity at the geographic scale >5000 km

At a wider geographic range (>5000 km), rafting does not seem to be a prevalent mechanism of dispersal, and when inferred it only contributes with low levels of gene flow, presumably through episodic rafting routes that may sometimes connect distant populations while others found new populations, thus expanding the geographic range of distribution or contributing to allopatric speciation. The small but existent migration among populations of the isopod Sphaeroma terebrans across oceans might be achieved through rafting, and as stated by the authors, “In spite of the low vagility of S. terebrans, mechanisms of passive dispersal, probably through floating mangrove woods, could be responsible for the worldwide distribution of the taxon, which is until now considered cosmo- politan” (Baratti et al. 2005). They conclude that current patterns also affect “mangrove fragments with animals on board” resulting in genetic differentiation patterns, and that their reproductive strategy “is not sufficient to produce a high level of reproductive isolation between S. terebrans populations since passive dispersal through floating mangrove wood transported by currents could maintain a certain degree of gene flow between populations” (Baratti et al. 2005) (Figure 12). However, it cannot be excluded that this wood-boring isopod may not also be transported via anthropogenic vectors (e.g., on wooden ships). Rafting has been suggested as a means of dispersal at a scale over 6000 km for two gastropod species of the genus Hydrobia from the European coasts with contrasting modes of development. Hydrobia ventrosa is a direct developer that exchanges approximately 0.36 migrants per generation at this spatial scale. Considering the continuum between intermittent and episodic rafting routes, these populations may be sufficiently connected via rafting to prevent allopatric speciation but not local population differentiation. The species with planktonic development, H. ulvae, does not show a pattern of IBD and gene flow corresponds to 0.75 migrants every generation as inferred from genetic differentiation data, which led the authors to conclude that rafting is a possible means of LDD dispersal for the species (Wilke & Davis 2000). Finally, the bryozoan Membranipora membranacea with planktonic development shows low but detectable levels of gene flow (Nm = 0.09) at distances >10,000 km (Schwaninger 1999). Since

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O. geniculata from the N Atlantic that shows that the Massachusetts Atlantic that shows from the N

O. geniculata : JP Ð Japan, NZ Ð New Zealand, MA Ð Massachusetts, NB Ð New: JP Ð Japan, NZ Ð New Brunswick, yletic (e.g., NB). Figures modified after Govindarajan et al. (2005). yletic (e.g., NB). Figures modified et Govindarajan after Obelia geniculata ylogram based on same data for the populations of A sequence data for populations of (A) Global distribution and sampling sites of the hydrozoan(A) Global distribution genus population (MA) shares all haplotypes with New Brunswick (NB). (C) Ph the N Atlantic. This tree shows that within the N Atlantic many populations are paraph that within the N This tree shows Atlantic. the N Figure 30 Figure IC Ð Iceland, FR Ð France. (B) Haplotype network of mtDN

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distances considered here are extremely large for larval dispersal, episodic rafting routes mediated on plastic substrata (Aliani & Molcard 2003) could account for the cosmopolitan distribution of the species and the low but persistent gene flow that prevents allopatric speciation. At this geographic scale and mostly toward 10,000 km, actual dispersal may be mostly human- mediated, but it cannot be excluded that rafting has occurred on isolated occasions in the evolu- tionary past. Rafting events may be so rare at this scale (e.g., one event every million years, episodic rafting routes) that populations have diverged significantly leading to allopatric speciation, and the observed genetic signals could be indicative of different species. Exemplifying this are the three deeply divergent clades (possibly cryptic species) of Obelia geniculata from Japan, New Zealand and the North Atlantic (Figure 30), which are thought to have originated >3 Mya. Rafting may have played a role in dispersing the ancestors of the populations from the different oceans (Govin- darajan et al. 2005). Phylogeographic analysis of closely related species may be most suitable to reveal historic rafting events at this scale.

Gene flow patterns and contrasting developmental modes In general, brooders show higher levels of genetic differentiation among local populations than species with planktonic larval development (McMillan et al. 1992, Duffy 1993, Hunt 1993, Edmands & Potts 1997, Arndt & Smith 1998, Chambers et al. 1998, Todd et al. 1998, Boisselier- Dubayle & Gofas 1999, Kyle & Boulding 2000, Wilke & Davis 2000, Collin 2001, Andrade et al. 2003) (Figure 29). In situations where gene flow is indeed low for direct-developing species, they usually show increasing genetic isolation with increasing geographic distance (IBD) (e.g., Hellberg 1994, Ayre et al. 1997, Wilke & Davis 2000, Collin 2001, Goldson et al. 2001, Vianna et al. 2003). Several studies have compared genetic structure in taxa with different modes of development and have shown that sympatric sessile or semi-sessile species with contrasting modes of develop- ment often have similar genetic structure. Gene flow of sympatric species that are closely related (not necessarily congeners) may be constrained by similar dispersal barriers. The genetic differen- tiation values that have been reported among congeneric sympatric species with contrasting modes of development indicate that taxa with direct development generally display higher levels of genetic structure and IBD. Ayre et al. (1997) studied the genetic population structure of ascidians and corals from southeastern Australia, distinguishing solitary and colonial forms with high and limited dispersal potential, respectively. They found that solitary corals display little variation among local populations while local populations of colonial corals are highly differentiated. Comparison with data from other species inhabiting the same region confirmed their results (Hunt & Ayre 1989, Ayre et al. 1991, Hunt 1993, Billingham & Ayre 1996, Ayre et al. 1997, Hoskin 1997, Murray-Jones & Ayre 1997). The authors conclude that “even in a region where current flow is expected to be erratic, there is a clear contrast between the level of differentiation of broadcast-spawning and brooding species, and that for broadcast-spawning species the East Australian current is able to maintain high levels of gene flow and produce effectively panmictic breeding populations within the central and southern coasts of New South Wales” (Ayre et al. 1997). Particularly interesting are studies of congeners that differ in their dispersal potential based on developmental mode alone. Many of these studies conclude that direct-developing species have highly structured populations and a more robust pattern of IBD than species with planktonic larval development (see Table 2). Rafting can be invoked in cases where the phylogenetic and habitat characteristics of popula- tions of species with contrasting modes of development are similar and the directly developing species lacks sufficient differentiation with respect to expectations (or does not fit an IBD pattern). For example, Ayre & Hughes (2000, 2004) have presented interesting results on the genetic divergence of populations of corals of the genus Acropora from the GBR in eastern Australia. In

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Table 2 Comparison of population genetic differentiation values among congeners with different modes of development

Direct Planktonic Taxon Genus development development Reference Anthozoa Acropora θ = *0.035 θ = *0.03 Ayre & Hughes 2000 Nm = 6.89 Nm = 8.08 1200 km 1200 km

Acropora FST = 0.29 FST = 0.21 Ayre & Hughes 2004 Nm = 0.61 Nm = 0.94 2400 km 2500 km

Actinia FST = 0.262 FST = 0.375 Ayre et al. 1991, Vianna et al. 2003 Nm = 2.33 Nm = 0.42 1150 km 1050 km Pocillopora θ = 0.15 θ = 0.056 Ayre & Hughes 2004, Magalon et al. 2005 Nm = 1.42 Nm = 4.21 2400 km 2000 km Eucarida Synalpheus θ = 0.54 θ = 0.14 Duffy 1993 Nm = 0.21 Nm = 1.54 4800 km 4800 km

Prosobranchia Cerithium FST = 0.58 FST = 0.158 Boisselier-Dubayle & Gofas 1999 Nm = 0.18 Nm = 1.33 1750 km 1750 km Crepidula APV = *65.2 APV = Ð7.4 Collin 2001 1300 km 1300 km

Hydrobia FST = 0.41 FST = 0.25 Wilke & Davis 2000 Nm = 0.36 Nm = 0.75 6000 km 6000 km

Littoraria FST = 0.185 FST = 0.028 Andrade et al. 2003 Nm = 1.1 Nm = 8.68 4000 km 4000 km

Littorina ΦST = *0.06 ΦST = *0.03 Kyle & Boulding 2000 Nm = 3.9 Nm = 8 3600 km 250Ð750 km

Asteroidea Patiriella FST = 0.462 FST = 0.0008 Hunt 1993 Nm = 0.29 Nm = 312.25 230 km 230 km

Echinoidea Heliocidaris GST = 0.62 GST = 0.12 McMillan et al. 1992 Nm = 0.15 Nm = 1.83 3400 km 3400 km

Holothuroidea Cucumaria ΦST = 0.97 ΦST = 0.05 Arndt & Smith 1998 Nm = 0.01 Nm = 4.75 2300 km 2350 km

Ectoprocta Alcyonidium FST = 0.077 FST = 0.105 Porter et al. 2002 (Bryozoa) Nm = 3 Nm = 2.13 800 km 1500 km

Notes: For each genus we present estimates of genetic differentiation among populations (or their averages) for species with differing modes of development at similar spatial scales. Nm values were calculated according to Wright (1969). Genera in bold indicate that the species with direct development has been inferred to raft.

* Average value, details in Table 1.

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their first study conducted at a scale of 1200 km they found that species with both direct and planktonic larval development were effectively panmictic (Ayre & Hughes 2000). Indeed all studied species display low genetic differentiation and relatively high number of migrants per generation. Subsequently they expanded the geographic scale of their study and found that at a scale of 2400 km, species with direct and planktonic larval development show similar genetic differentiation (Ayre & Hughes 2004). The above results suggest that corals with different developmental modes in the GBR have similar realised dispersal distances and frequencies. Some coral species of the genus Acropora are known to raft on pumice (Jokiel 1990a), and even though it is not direct evidence that the species included in the genetic studies (Ayre & Hughes 2000, 2004) is a rafter, it is possible that rafting mediated connectivity prevents genetic differentiation among populations of the direct- developing Acropora cuneata. Another example is provided by the comparison of the genetic differentiation in sea anemones provided by the studies of Vianna et al. (2003) and Ayre et al. (1991). They studied genetic differentiation in species of the genus Actinia with direct development from the coast of Bermuda and Brazil and with planktonic development from southeastern Australia, respectively. Interestingly, the direct-developing species displays lower genetic differentiation at a scale of 1150 km (Nm = 2.33) than the species with planktonic development at a similar scale (1050 km) (Nm = 0.42). Rafting has not been inferred for any of the two studied species of Actinia, but according to these data, the direct-developing Actinia bermudensis is achieving LDD by some means. Another example that involves greater gene flow for direct-developing species than for species with planktonic development is seen in bryozoans of the genus Alcyonidium, but opposed to the examples given above, the species with short-lived lecitotrophic larvae (restricted potential for autonomous dispersal), Alcyonidium gelatinosum, has the potential for rafting on algae (Porter et al. 2002). These authors found that bryozoan species from the British Isles with direct development

have less genetic differentiation at a scale of 800 km (FST = 0.077) than bryozoans with planktonic larval dispersal at a scale of 1500 km (FST = 0.105), which is likely due to rafting-mediated connectivity for the species with short-lived larvae. Gastropods from the genus Littorina have been widely studied and compared with respect to their genetic structure and modes of development (Janson 1987a,b; Johannesson & Tatarenkov 1997; Johnson & Black 1998; Kyle & Boulding 2000; Andrade et al. 2003; Johannesson et al. 2004). Kyle & Boulding (2000) found that the direct-developing L. sitkana shows no genetic

differentiation at the scale of >3000 km (FST = 0), and suggested that rafting has played an important role (see above). In general, species of Littorina that have planktonic larval development show similar or slightly less genetic differentiation at comparable scales than species with direct development. All the above leads to the conclusion that rafting is an important means of dispersal at different spatial scales and as previously emphasised, dispersal potential cannot be inferred from develop- mental mode alone. From small to large spatial scales, connectivity achieved through rafting (as reported above), matches closely the described rafting routes, from frequent, to intermittent and episodic.

Rafting dispersal and evolution Arrival in new habitats often leads to evolutionary change (Holt et al. 2005). This may be particularly true for species that have arrived on rafts as will be argued in the following subsections. One of the main differences between dispersal via rafting and planktonic larvae is that rafting, as opposed to larval dispersal, is usually not restricted to a particular ontogenetic stage. This may allow rafters to establish local populations during the rafting voyage (Thiel & Gutow 2005b). There are specific characteristics of the life history of many brooders that give additional evidence that they are particularly well adapted to colonise and persist after arriving in new habitats. Herein, genetic

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evidence will be reviewed that characterises the population structure of direct developers, and there will be discussion of the impact of rafting dispersal on (i) local recruitment and deme formation, (ii) colonisation across environmental gradients and (iii) the interplay between isolation and sec- ondary admixture.

Local recruitment and deme formation

Rafting provides an effective means of dispersal for many brooders, particularly those that are likely to be found on floating substrata. Even though brooders may successfully achieve LDD through rafting, within a limited geographic area it has been observed that they show high levels of genetic differentiation (i.e., that they are highly microspatially structured) (Lessios et al. 1994, Johnson & Black 1995, Hoskin 1997). Organisms with direct development show distributions with greater patchiness than species with planktonic larval stages and within a patch they may contribute significantly to species diversity: “The fine scale spatial structure of direct-developing species was reflected in higher average species diversity within quadrats” (Johnson et al. 2001). Peracarids are common rafters and display life-history characteristics that may enhance their probabilities of successful dispersal through rafting. They brood their eggs up to a crawl-away stage and in many species offspring recruit in close proximity to their parents (Flach 1992, Thiel et al. 1997, Thiel 1999). In the marine environment, some peracarids may live in algae and have a relatively high potential for passive dispersal by rafting. Thiel & Vásquez (2000) found that algal holdfast communities are characterised by dense aggregations of single peracarid species that do not correlate with holdfast size, suggesting that local recruitment of these species occurred within the holdfast. Juveniles often excavate their galleries as offshoots of the maternal gallery (Menzies 1957, Jones 1971, Conlan & Chess 1992, Thiel 2003a), as a consequence of extended parental care (for review see Thiel 2003b). Consequently, populations of brooders often show differentiation at a microgeographic spatial scale. For example, the isopod Jaera albifrons shows differentiation over a scale of a few metres, consistent with deme formation (Piertney & Carvalho 1994, 1995; Carvalho & Piertney 1997). Similarly, Lessios et al. (1994) identified differentiation at the scale of hundreds of metres in the isopod Excirolana braziliensis, and populations of the amphipod Coroph- ium volutator show significant differentiation within the Bay of Fundy (Wilson et al. 1997). Thus, peracarids often exhibit microscale genetic structure consistent with local recruitment resulting in deme formation. Johnson & Black (1995) studied the gene flow patterns in the brooding intertidal snail Bemb- icium vittatum in the Albrolhos Islands using direct and indirect methods. They found that along a continuous habitat there was a pattern of IBD that was absent in discontinuous habitats. Their results emphasise the importance of gene flow barriers on the genetic structure of species, partic- ularly those with direct development. The recruitment pattern of these species, leading to deme formation within a microhabitat, could lead to high localised inbreeding (and potentially reduction in individual fitness) and divergence through genetic drift and localised selection (Piertney & Carvalho 1994, 1995). Deme formation appears to be common among species with direct devel- opment that inhabit patchy microhabitats (Piertney & Carvalho 1994, Sponer & Roy 2002, Colgan et al. 2005). However, Piertney & Carvalho 1995, found that the levels of genetic differentiation in Jaera albifrons resemble those found in other species with similar developmental modes that do not display deme formation, and thus, they concluded that “the ephemeral nature of some micro- habitats may result in inbreeding being restricted to within one generation, reducing the overall effects of inbreeding depression and loss of heterozygosity in the localized population”. For brooders, local recruitment may represent an extreme advantage that enables them for LDD through rafting, as they may establish viable populations during the journey as well as during colonisation. In addition to local recruitment leading to deme formation, there are several other

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advantages that predispose direct developers for LDD; among the most important is their ability to disperse at any life stage (i.e., they are not restricted to the temporal duration of a particular ontogenetic stage in order to disperse).

Transport and colonisation across environmental gradients

On the microscale, rafting may occasionally transport organisms into habitats that are quite different from their native habitats. For example, this can happen across an intertidal gradient, where organisms from lower-shore habitats may be deposited on the higher shore. Due to their high colonisation potential, these rafting colonists may establish local populations, even in habitats with a new selective regime. Possibly this is occurring in species of Littorina from the North Pacific and North Atlantic, which are found both in the low and high intertidal zone. For the eastern North Atlantic, Panova & Johannesson (2004) reported divergent genetic adaptations between local populations of L. saxatilis from the lower and upper shore, which are in accordance with the respective selective pressures in either zone. Snyder & Gooch (1973) who studied this species in the western North Atlantic have discussed that “population isolation, with subsequent reduction in population size, promotes random drift and ultimate fixation of alleles. Shifting modes of natural selection over an ecologically heterogeneous area lead to genetic differences”. Based on ecological responses of L. saxatilis from the low and high intertidal zone, Pardo & Johnson (2005) also suggested that “selection may favour genotypes with low growth potential in lower zones and those with high growth potential in higher zones”. Cruz et al. (2004) suggested that divergence of ecotypes of L. saxatilis, which differ in size due to different selective environments, is enhanced by size- assortative mating patterns. Sokolova & Boulding (2004) studied ‘ecotypes’ from the open shore and from salt marshes in two species of Littorina from the eastern North Pacific with consistent physiological differences. They suggested “that phenotypic differentiation in direct-developing species with limited dispersal is strongly affected by local adaptation and natural selection in heterogeneous habitats, and that strong local adaptation in the same type of habitat may result in convergent evolution producing superficially similar phenotypes”. At least one of the species they studied (L. sitkana) is also thought to disperse frequently via rafting (Behrens Yamada 1989, Kyle & Boulding 2000). Estevez (1994) reported isopods Sphaeroma terebrans, which usually bore into mangrove roots and wood, from rhizomes of saltmarsh plants. They suggested that isopods had arrived in the salt marsh on floating driftwood. Possibly, original founders colonised rhizomes due to lack of other suitable habitats. Nothing is known at present about the genetic relationship of rhizome populations and wood populations of S. terebrans. For the saltmarsh plant Elymus athericus, Bockelmann et al. (2003) also reported that within- site populations from high and low shore differ more than between-site populations. They suggested “that markedly different selection regimes between these habitats, in particular intraspecific com- petition and herbivory, result in habitat adaptation and restricted gene flow over distances as small as 80 m”. Billard et al. (2005) revealed that Brittany populations of Fucus vesiculosus from the outer coast differed from those in bays. The authors suggested that this differentiation could be due to dispersal restrictions between bay and coastal populations. This is surprising since F. vesiculosus is probably the species from the genus Fucus, which is best adapted to float over considerable distances, and is commonly reported as floating in coastal waters of northwestern Europe (Tully & Ó Céidigh 1986, Davenport & Rees 1993, Franke et al. 1999, Vandendriessche et al., 2006). The possibility of differential selective pressures was not excluded by Billard et al. (2005): “Local popu- lation acclimation or adaptation to specific habitats causing lower establishment success between habitats cannot be ruled out as an additional explanation for this population differentiation”.

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The selective environments in the low and high intertidal zone or on the open shore and in sheltered bays are substantially different and this could result in genetic divergence of local populations across these gradients. For all of the species discussed above, rafting dispersal has been inferred or appears likely. However, why should these species be more prone to selective divergence across these gradients than other species? As mentioned above, rafting organisms have very little influence on selecting particular sites during the arrival process, and consequently they may be deposited over a wide range of ecological gradients. In contrast, planktonic larvae show diverse adaptations to select suitable habitats during settlement. They may settle only in a very restricted range across a gradient. Additionally, small, recently metamorphosed individuals may be highly susceptible to adverse environmental conditions. Rafting organisms, many of which feature direct development, release advanced developmental stages that may also survive in less favourable conditions. Consequently, rafters may initially survive over a wider range of environmental gradients than species with planktonic larvae. During subsequent population establishment, diverging selec- tive pressures may result in genetic divergence of local populations, which is further enhanced by retention of lineages with favoured genes due to local recruitment of direct developers. Johannesson (2003) emphasised that: “The absence of pelagic larvae prevents rapid colonisation of habitats, but promotes local adaptation by subpopulations living generation after generation in the same habitat”. In her excellent review on evolutionary processes in littorinid snails she concluded that “we have evidence both from morphological and molecular traits that directional selection can produce rapid evolutionary changes. If such changes create reproductive barriers either directly or as secondary effects, reproductive isolation (and thus speciation) might appear more or less instanta- neously upon an ecological shift of a population”. Interestingly, these rapid changes are most pronounced in those species with direct development, and rafting contributes to these microevolu- tionary processes. The interaction between rafting and direct development appears to play an important role in these processes, and it is suggested that future studies should a priori focus on this interaction. For species with planktonic larvae, Havenhand (1995) had stated: “Because the capacity for gene-flow between populations is frequently related to the dispersal potential of the larvae, the degree of larval dispersal may strongly mediate rates of evolution in marine species”. Rates of evolution in some rafting-dispersed direct developers may be particularly fast due to the reasons discussed.

Isolation and secondary admixture

As emphasised above, LDD via rafting may often result in isolated local populations. In particular in populations established on episodic rafting routes, periods of isolation may be sufficiently long to result in significant population divergence. There are abundant examples in the literature sug- gesting isolated dispersal events (see above) that resulted in allopatric speciation. For example, for littorinid snails, Williams et al. (2003) suggested dispersal of ancestors of recent species from the genus Austrolittorina in the Southern Ocean between New Zealand and South America about 15Ð30 Mya, and due to the long distance and intermediate larval lifetime they invoked rafting as a potential dispersal mechanism. Williams & Reid (2004) also suggested transatlantic dispersal in the equatorial current system starting around 20 Mya ago, when oceanic currents became stronger. They inferred that dispersal has primarily taken place in an easterly direction, but they did not discuss the dispersal mechanism. Based on the phylogeography of the species-rich genus Echino- littorina they emphasised that “speciation may be predominantly allopatric in each case, but on long coastlines allopatry is more likely to be transient, because of greater opportunities for post- speciation range extension, whereas geographical isolation should be more complete in island settings” (Williams & Reid 2004). Donald et al. (2005) inferred rafting events to have played an important role in the phylogenetic evolution of snails from the family Trochidae. In a phylogenetic

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analysis of marine bivalves from the genus Lasaea, Ó Foighil et al. (2001) also suggested that rafting followed by isolation has repeatedly influenced evolutionary processes. Rafting may also affect evolution in species with planktonic larvae. For example, Waters & Roy (2003) stated with respect to a widespread seastar genus with planktonic larval development “that both rare dispersal (e.g., rafting) and recent vicariance (e.g., formation of the Benguela Current) may have promoted allopatric divergence and speciation in Coscinasterias”. Rafting dispersal followed by isolation has also led to allopatric speciation in many terrestrial species. Most recent evidence comes from phylogenetic studies on reptiles. Carranza et al. (2000) inferred that geckos from the genus Neotarentula colonised Cuba up to 23 Mya, coming from North Africa, most likely rafting in the North Equatorial Current. Glor et al. (2005) reported that Caribbean species from the genus Anolis have diverged on different islands following overwater dispersal (via rafting). If isolation has not yet led to reproductive barriers, secondary contact via rafting may allow hybridisation of diverging clades. In general, founder effects, genetic bottlenecks, long periods of isolation and secondary admixture may result in a complex genetic pattern among local populations of many species. Possibly, the high degree of polymorphism among species commonly known as rafters is a consequence of various combinations of these processes. Occasional hybridisation between the different ecotypes of Littorina saxatilis may result in the observed polymorphism in this species (Pérez-Figueroa et al. 2005). Rafting may also allow exchange of similar ecotypes from different localities, further enhancing polymorphism in L. saxatilis. Another example might be found among the species of caprellid amphipods, which are commonly reported as rafters (Thiel & Gutow 2005b). Many of these species feature highly variable morphotypes (known as smooth and spinose forms). This group (and other peracarids) may prove in the future to be an excellent model to study evolutionary processes among common rafters with direct development. Evolutionary processes influenced by rafting represent an exciting challenge for marine biol- ogists. Rafting-mediated evolution shows some particularities that are the result of the fact that this dispersal process usually transports a limited number of individuals, which nevertheless have a high likelihood of successfully establishing populations in new habitats. This increases the proba- bility of founder effects and population persistence, even in isolation from other populations. While this may also increase the risk of extinction (due to inbreeding and low genetic diversity), there is ample indication that many founder populations have persisted and spread successfully in new habitats. Arrival of conspecifics (or congeners) long after the arrival of early colonists may lead either to secondary admixture or to sympatric coexistence of closely related species. In summary, evolutionary processes mediated by rafting can lead to species divergence, either in sympatry or in allopatry. Rafting thus contributes to local biodiversity, not only by importing colonisers to marine communities but also by facilitating speciation.

Implications for conservation of marine biodiversity Connectivity and conservation In accordance with conservation strategies applied in terrestrial systems, protected areas have been recognised as a powerful conservation tool in the marine environment also (Carr et al. 2003). Marine protected areas (MPA) and marine reserves are increasingly created in many regions of the world in order to provide refuges for over-exploited species or to protect biodiversity in general (Lubchenco et al. 2003, Palumbi 2004). Building on the metapopulation concept, it has been recognised that a single isolated MPA has only a limited potential for the protection of endangered species (Gerber et al. 2003). Isolated populations depend exclusively on local recruitment, making a population vul- nerable to extinction if unpredictable climatic variations affect reproduction or survival (Figure 31).

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Local Local Local recruitment recruitment recruitment only + Larval + immigration Larval + immigration Rafting immigration

Openness of populations

low high

Figure 31 Relationship between the connectivity of local populations (via different mechanisms) and the sensitivity to disturbance. The openness or closed nature of populations makes them more or less dependent on local recruitment. Absolute dependence on local recruitment (closed population) leads to a high sensitivity to local disturbance, while populations open to the input of larval and/or rafting dispersal will be less sensitive to local disturbance.

Ensuring connectivity with other populations and immigration of propagules from other areas will alleviate failures in local recruitment and avoid extinctions of populations in an isolated reserve area. Consequently, networks of MPAs encompassing multiple local populations are required, because connected local populations are less vulnerable to local catastrophes (Figure 31). Resilience of a population to environmental changes can be expected to increase with the number of populations to which it is connected, because more connections result in a higher probability that at least some of the connections are not interrupted by environmental disturbances. Similarly, the larger the total area of a network, the higher is the probability that at least some of the local populations are not affected by local disturbances and maintain their function as a donor of individuals for affected populations (Allison et al. 2003, Halpern 2003). Rafting connections occur on a variety of spatial scales, and in particular those routes that connect local populations (frequent and intermittent rafting routes) need to be taken into account in the design of MPA networks. The major challenge in the development of MPA networks is the appropriate spacing of the subunits of a network in order to allow for sufficient connectivity between local populations (Shanks et al. 2003). Consequently, the creation of efficient MPA networks requires detailed knowledge of the dispersal capacities of the species under protection. To date, most efforts have focused on species with planktonic larvae (e.g., Guichard et al. 2004) and/or active migration (e.g., swimming) (e.g., Rakitin & Kramer 1996). Even though empirical data for dispersal distances of commonly rafting organisms are rare, there is growing indication that this might substantially contribute to the connectivity among local populations (see above). In many regions, rafting and other alternative dispersal mechanisms may contribute to the connectivity among populations that appeared to be

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unconnected when accounting only for larval dispersal or active migration. Considering all relevant aspects in the assessment of the dispersal capacity of a species (including the possibility of rafting) will allow for an accurate estimate of the connectivity of populations, the relative importance of local recruitment vs. immigration processes, and the vulnerability of a population toward environ- mental variability (see, e.g., Gerber et al. 2005). The development of efficient MPA networks requires a quantification of exchange processes of individuals between local populations. Even though complex behaviour (Yeung & Lee 2002) and physiological constraints of larvae (Anger 2003) complicate the modelling of dispersal, rafting dispersal is even more difficult to apprehend because it depends on multiple external variables and requires extensive empirical information from field investigations. The importance of external factors such as availability, quality, and longevity of rafts decreases the relative importance of intrinsic features of the organisms making exclusive laboratory investigations (as used for estimating the duration of larval development — see, e.g., Goffredo & Zaccanti 2004) insufficient in order to obtain reasonable estimates of rafting processes. The quantification of rafting opportunities and the assessment of the directionality of transport processes are basic aspects in the evaluation of the importance of rafting for the connectivity of populations in a given region. In addition to the extrinsic factors depending on currents and floating substrata, the life history of organisms needs to be taken into account. For many of the taxa that have been found on floating substrata, relatively little is known about their population connectivity (Table 3). For example, even though amphipods are among the most abundant rafting species, only for very few species are data available about population connectivity. Despite this general lack of knowledge about rafting organisms, it can be mentioned that many species feature particular life-history characteristics. Many common rafting species are small, have a limited reproductive potential (individual clutch sizes usually <100 offspring) and feature direct development. Due to these characteristics, the inclusion of these organisms in effective conservation measures and the design of MPA networks require particular considerations. Rafting connectivity is achieved via three important steps: (i) going onboard, (ii) surviving the voyage and (iii) disembarking and establishment. Only when all these steps are successfully completed can rafting be an efficient dispersal mechanism. The first two steps depend on both the organisms and the floating substrata, while the last step also depends to a high degree on the characteristics of the sink regions. Human activities are affecting the first two steps by changing the availability of floating substrata and the last step by modifying the characteristics of potential arrival sites.

Changes in rafting opportunities In many regions of the world the frequency of rafting opportunities has changed significantly, often as a consequence of human activities affecting the spatial and temporal distribution of floating items. The introduction of large amounts of floating debris into the marine environment over the last decades has increased rafting opportunities (Winston 1982, Winston et al. 1997, Barnes 2002, Aliani & Molcard 2003, Masó et al. 2003) and, thus, is likely to have contributed to population connectivity for those species capable of rafting on artificial substrata. Even though floating anthropogenic debris might enhance population persistence by supporting species transport, its chronic presence may superimpose on natural dispersal patterns. The high longevity of plastics in the marine environment might result in transport of associated organisms over large distances, similar to that on pumice or other natural substrata that are available only sporadically. The ubiquitous and continuous presence of plastics may change the episodic character of LDD via rafting, thereby enhancing the frequency of rafting dispersal of many organisms across biogeo- graphic barriers. This could lead to an enhanced globalisation of species transported on these long- lived substrata by raising the risk of species introductions (Barnes 2002). The introduction of

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Table 3 Number of marine invertebrate species that have been reported or inferred as rafting in a previous review (Thiel & Gutow 2005b), and species for which data on the genetic population connectivity are available (see Table 1)

Sum of species with Sum of data for genetic Taxon rafting species population connectivity Porifera 3 2 Cnidaria Hydrozoa 102 1 Anthozoa 28 27 Annelida Polychaeta 79 3 Arthropoda Cirripedia 22 2 Copepoda (Harpacticoida) 72 0 Hoplocarida 0 1 Eucarida 96 7 Peracarida (Amphipoda) 108 8 Peracarida (Isopoda) 38 7 Mollusca Gastropoda (Prosobranchia) 72 27 Gastropoda (Opisthobranchia) 44 2 Bivalvia 51 4 Cephalopoda 11 1 Echinodermata Asteroidea 16 7 Echinoidea 7 14 Holothuroidea 6 2 Ophiuroidea 11 1 Ectoprocta (Bryozoa) 96 5 Chordata Tunicata 11 3

Total 873 124

non-indigenous species into new regions has been recognised as a major threat to biodiversity (Carlton & Geller 1993). Especially polar regions, which are thought to be particularly vulnerable to the harmful effects of bioinvasions due to their high degree of endemism (Barnes & Fraser 2003), are expected to be threatened by an increasing amount of floating debris in the world’s oceans (Barnes 2002). However, the role of plastics in the ‘ecological roulette’ of bioinvasions is discussed controversially and some scientists believe that the role of plastic rafting may be overestimated. In order to evaluate risks created by these substrata, the global distribution pattern of floating anthro- pogenic material has to be taken into consideration. In coastal waters near the centres of human activity at low and mid latitudes, floating marine debris is highly abundant (Thiel & Gutow 2005a), possibly contributing significantly to the transport of species (e.g., Winston et al. 1997, Masó et al. 2003, Aliani & Molcard 2003). At high latitudes, however, where densities of floating plastics are lower, the contribution of these items to the overall transport of marine species has not yet been evaluated thoroughly. Based on the finding of plastic-rafted organisms, Barnes & Fraser (2003) confirmed that some species could be successfully dispersed by rafting in Antarctic and subantarctic

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waters. Lewis et al. (2005) agree that floating plastics provide artificial surfaces for settlement of organisms but they consider fouling on ship hulls as a more imminent threat to polar biodiversity. Furthermore, due to the low abundances of floating plastics in polar waters, compared to naturally occurring substrata such as pumice or floating macroalgae, the authors expect floating plastics to simply supplement already existing natural pathways in Antarctic waters but produce no significant effects on biodiversity (Lewis et al. 2005). At lower latitudes, however, there is some indication that rafting on anthropogenic floating substrata has already led to significant niche expansions or to the spread of species into areas previously not colonised by them. Winston (1982) described how an increasing amount of floating plastics can facilitate the proliferation of species. The bryozoan Electra tenella was rare at the Atlantic coast of Florida, but its ability to colonise artificial substrata enabled this species to establish in the region and to persist in competition with indigenous species such as the bryozoan Membranipora tuberculata, usually competitively superior in the natural benthic envi- ronment. Similarly, range expansion via rafting has also been inferred for the Pacific oyster Lopha cristagalli, formerly known only from northernmost New Zealand. Individuals of this species have been found on stranded rope masses on a remote beach of the South Island of New Zealand (Winston et al. 1997). These examples indicate that an increasing amount of floating debris in the world’s oceans results in an intensified transport of organisms potentially beyond existing distributional limits. In addition to contributing directly to bioinvasions, rafting can also facilitate the local or regional spread of a non-indigenous species after these have been introduced by alternative dispersal mechanisms. The barnacle Elminius modestus was brought to European waters in the 1950s on ship hulls from the South Pacific (Crisp 1958). Within a few decades this species spread rapidly throughout the coastal regions of northwestern Europe. Rafting has never been discussed as a potential mechanism for regional dispersal of this species in European waters. Recent reports of E. modestus from floating debris in the North Atlantic (Barnes & Milner 2005) indicate that rafting on anthropogenic rafts cannot categorically be excluded as a possible mechanism for the extensive spread of this species in its new environment. Rafting has also been discussed as a possible mechanism for regional spread of the skeleton shrimp Caprella mutica in the North Sea where the species was co-introduced with the pacific oyster Crassostrea gigas (Buschbaum & Gutow 2005). These examples indicate the potential of persistent anthropogenic rafts in facilitating species invasions that might be less likely under natural conditions of raft availability and quality. While the availability of anthropogenic flotsam has increased, naturally occurring types have, in turn, decreased in abundance in the marine environment, at least regionally. Logging activities have changed the supply of floating wood in many areas of the world during the past centuries (Maser & Sedell 1994). Damming of rivers has led to retention of floating wood, which is no longer delivered to the sea during flood events. Similarly, shoreline stabilisations such as dikings and embankments prevent seasonal flooding of coastal lowlands. Terrestrial plant material usually washed out during these events is retained and, consequently, not available for important seasonal dispersal events.

Modern coastlines and connectivity There are numerous factors that influence the arrival process of rafters (Thiel & Gutow 2005b). Human activities may affect this process in two important ways, namely by modifying the filter efficiency of many habitats and the retention efficiency of coastlines. The filter effect refers to the structure of many habitats where vascular plants or algae extend across the sea surface, effectively filtering out most floating substrata preventing these from being washed onto inhospitable beaches or higher shores. This filter effect is vividly described by Simberloff & Wilson (1969) for small mangrove islands: “Drifting wood usually hits an island, gets trapped temporarily among roots, and eventually floats away”. Similar observations were made for kelp forests, where floating algae frequently entangle in kelp forests (Zobell 1971, Dayton et al.

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Figure 32 Grazing has an important effect on the filter efficiency of salt marshes. (A) Ungrazed salt marsh showing that large quantities of floating debris are filtered out by the vegetation, and (B) grazed salt marsh showing that plant debris passes the salt marsh without being filtered out before ending up on the dike (photos courtesy of Martin Stock, Nationalparkamt Schleswig-Holsteinisches Wattenmeer, Germany).

1984, Dayton 1985). Any activity that leads to an elimination or length reduction in the plants/algae that constitute the filter will also reduce their efficiency in filtering out floating substrata at the sea surface. For example, mangrove clear-cutting, in particular on the seaward edge of mangrove forests, leads to a reduction of roots intersecting the sea surface. Similarly, industrial-scale kelp harvesting removes a large proportion of the surface canopy (California Department of Fish and Game 2000, Casas et al. 2003), reducing the filter efficiency of kelp beds. Intensive grazing of saltmarsh vegetation produces a very short lawn unable to filter floating detritus during high tides (Figure 32). These effects may cause most floating materials to end up directly on the high shore where living conditions are unsuitable for most marine rafters. The retention efficiency of coastal areas depends on the geomorphology of the shore. Highly fragmented coastlines with many semienclosed bays and inlets facilitate the retention of floating items within such bays. Turbulent current and front systems and coastal eddies, characteristic for many irregular coastal areas, might prevent floating items from escaping to offshore waters (Largier 2003) and, thus, increase the probability of successful disembarking of rafting organisms. Harrold & Lisin (1989), for example, observed that the majority of Macrocystis pyrifera rafts in Monterey Bay (California) remained within the bay as a consequence of local current and wind conditions. This process is supported by internal waves and surface slicks that often transport floating objects toward the shore (Kingsford & Choat 1986, Shanks 2002). These coastlines thus provide ample opportunities for rafting organisms to disembark from floating items. In contrast, linear coastlines have only a limited retention efficiency because water movements are intensified along the entire shore. Human activities in many of the densely inhabited coastal regions of the world have significantly modified coastlines during the past centuries. For example, until the late 1700s, the North Sea coast of Germany was highly fragmented with long-stretching estuaries where tidal currents reached far inland (Figure 33). As a consequence of extensive diking during the past centuries, the shape of the coastline has been smoothed dramatically, and many of the smaller estuaries are now cut off from tidal influence. Canalisation of larger estuaries and intensified river runoff might lead to stronger seaward-directed currents preventing the arrival of rafts in up-estuary habitats. Consequences of all these changes are similar to those of the filter effect. Floating substrata are no longer retained in shallow waters but rather end up on inhospitable dikes. Coastlines of many tropical and subtropical regions have experienced similar modifications. For example, the Atlantic coast of Florida, which until the beginning of the twentieth century was highly fragmented, was artificially remodelled by raising the height of supratidal areas and simultaneously deepening

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Figure 33 Maps of the North Sea coast of N Germany in the sixteenth century (A) and at present (B), showing the high degree of fragmentation in the sixteenth century and the rectilinear coastlines predominating since the twentieth century. Land (white), intertidal flats (shading) and subtidal streams and rivers (black) are shown.

shallow subtidal areas. The reduced extension of intertidal and low supratidal areas may have compromised the retention efficiency in many of these coastal regions. These changes usually lead to enhanced flow speeds in the remaining coastal waters. Davis et al. (2002) remarked that in highly modified bays “nutrients, food, and larvae in this water have a greater open-coast signal”. While these modifications enhance exchange of water masses and thereby the transport of planktonic organisms (and larvae), they may result in a reduced connectivity via rafting dispersal. To the present authors’ knowledge rafting-mediated dispersal has never been addressed in studies con- cerned with the modifications of coastlines. It is apparent that in addition to the loss of habitat and biodiversity, changes in the rafting dispersal processes and connectivity may be important secondary consequences of these human interventions of coastlines. Other human activities may lead to enhanced population connectivity via rafting in coastal waters. Artificial hard substrata such as harbours, aquaculture installations, navigation buoys, platforms, wind energy towers or piers constitute settlement substrata for a great diversity of organisms (Davis et al. 2002, Bram et al. 2005). All these constructions intercept the sea surface and thus may also retain floating substrata. In fact, cleaning of entangled floating algae has been reported to produce major costs to aquaculture installations in Australia (Hodson et al. 1997). Other anthropogenic structures are also assumed to retain floating items. Already established algal com- munities on breakwaters, jetties and piers may filter out floating items from the sea surface, thereby facilitating successful arrival of rafting organisms. Johannesson & Warmoes (1990) reported rapid colonisation of breakwaters on the Belgian coast (where natural hard substrata are lacking) by Littorina saxatilis, which most likely had arrived via rafting. Similarly, Dethier et al. (2003) remarked that direct development and the lack of an autonomous dispersal stage is no impediment to successful colonisation of a rock jetty at considerable distance (>40 km) from potential source populations. These examples demonstrate that artificial structures can serve as intermediate stepping stones, not only for species with planktonic larvae, but also for those that are thought to arrive as rafters. Anthropogenic structures may not only act as filters for floating substrata, but also as retention areas. For example, harbour basins often represent zones of reduced current velocities (Bulleri & Chapman 2004), where floating items might linger for longer time periods increasing the probability of successful disembarkation of associated rafters. In addition to their action in filtering out or retaining floating items, anthropogenic structures may also serve as important

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stepping stones, leading to a higher connectivity among local populations. In this context, Pinn et al. (2005) remarked that artificial hard substrata may “influence the dispersal of sessile organisms, allowing species that are poor dispersers to cover greater distances by using these structures as stepping stones” (see also Thompson et al. 2002). In general, human activities affect various stages of rafting journeys. Some activities may enhance connectivity between populations (introduction of plastics, construction of artificial filters and stepping stones), while others lead to a decreasing connectivity (retention of riverwood, elimination of filter habitats, coastline construction). Species that depend almost exclusively on rafting for dispersal can be expected to be most affected by these changes.

Outlook Some of the expressions most commonly used in this review are ‘may be’ or ‘suggest’. This demonstrates the high degree of uncertainty with respect to rafting as a dispersal process in the sea. However, the abundance of cases where authors are left with rafting as the only reasonable explanation for a certain pattern, is giving a clear signal. Rafting does occur and it connects populations of many species, or it transports organisms to new habitats where they may establish new populations. Based on the accumulated evidence the present authors believe that it is high time to move beyond the suggestive phase. Rafting plays an important role over most spatial and temporal scales operating in present-day oceans. The urgent need for effective and representative conservation measures in the marine environment requires that rafting be taken into account. The directionality of rafting dispersal, similar to the situation for larval dispersal, is crucial for the spatial arrangement of marine reserve networks. Accordingly, marine network reserves need to consider connectivity including rafting-mediated dispersal, which requires understanding the rafting dynamics of marine metapopulations (i.e., source-sink dynamics, sources of floating substrata). For example, if populations persist in a source-sink system with down-current sink populations being supplied from a large up-current source population, it is important to define adequate up-current reserve areas. The up-current area must not only provide supply of individuals but also sufficient rafts necessary for appropriate transport of organisms. The identification of relevant natural raft sources such as macroalgal belts, mangrove forests, salt marshes, or seagrass beds (see above) are, thus, obligatory for the development of efficient management programmes. Recognition of source areas might be complicated when rafts originate from distant sources without any obvious spatial relation to the actual conservation area. Rafts themselves (or the rafting organisms) may carry signals that allow the identification of source areas. Jokiel (1989), for example, collected rafting colonies of corals from floating pumice at Hawaii: the chemical composition of pumice can be utilised to identify source regions (Frick & Kent 1984, Jokiel & Cox 2003). Other characteristics of floating items (or size of rafting organisms) could also be used to infer their origin. Some of the most powerful tools to identify potential source regions are the genetic signals of the organisms themselves as has been demonstrated by several of the studies presented herein. Rafting not only poses challenges to conservation biologists, it also offers opportunities. One of the main questions in the study of marine reserve design is the question for source and sink regions: where do the organisms living in a marine reserve actually come from? Also one of the principal questions related to rafters observed on the high seas (or arriving in coastal habitats) is, where do they come from? Rafters can be traced back to the source regions by a variety of methods (see above). However, in contrast to tiny planktonic larvae, where evidence for source regions usually is inferential (e.g., Becker et al. 2005, Zacherl 2005), rafts can also be followed at sea and tracked during the rafting journey. Following dispersing organisms would also provide an under- standing of the processes leading to the survival or demise of rafters. In a previous review (Thiel & Gutow 2005b), it was argued that long-distance rafters may reproduce during the journey, and in

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the present review it is suggested that this may lead to founder effects within rafts. These processes may also influence the viability and genetic structure of groups of colonisers in new habitats. In order to understand these processes satisfactorily it is necessary not only to examine populations in source and sink regions, but also groups of travellers. It is therefore suggested that molecular studies that examine the population connectivity of coastal organisms should also incorporate rafting individuals whenever possible and feasible. It appears that the study by Reusch (2002) is the only one that sampled rafting individuals in an attempt to identify their source of origin with the aid of molecular markers. While rafting on the one hand offers unique opportunities in tracking organisms, on the other hand, direct testimony of arrival is much less likely than for species with planktonic larvae. Numerous studies have examined settlement in planktonic larvae, and many more have monitored recruitment events (for synthesis see, e.g., Eckert 2003). In contrast, very few investigators were actually present during the arrival of rafters. Successful colonisations by rafters are often only detected a long time after the arrival event. This is not very different from the arrival of species transported by other dispersal agents (e.g., birds, fish or humans). In these cases, the appearance of invaders often is noticed many years or decades after the first arrival. Not surprisingly, very little is known about the arrival process and initial colonisation in both categories. Consequently, in many cases it is difficult to infer whether an organism has arrived in a new area via rafting or via other agent-mediated transport mechanisms. Molecular studies can help to answer this question, because they permit an estimation of whether arrival has happened very recently or far back in time. For example, in a series of studies Duran et al. (2004a,b,c) have examined the present geographic distribution of the marine sponge Crambe crambe (which has short-lived lecitotrophic larvae) around the coasts of the Mediterranean and the North Atlantic (Madeira and Canary islands). At a scale of 3000 km, Duran et al. (2004a,b) found high genetic structure of populations following an IBD pattern based on microsatellites and nuclear DNA. The shallow divergence among sequence types in this study, led the authors to propose that C. crambe either is a young species (with no time to generate large sequence divergence) or an old species that has suffered demographic changes or a low mutation rate (Duran et al. 2004b). Duran et al. (2004b) elaborated on potential demographic changes as being “a strong recent bottleneck that has reduced its former genetic diversity, followed by a new expansion and accumulation of new mutations”. The authors offered human-mediated dispersal as the most likely explanation for recent exchange among populations of C. crambe, but they did not completely discount rafting as a possibility, which could result in a similar genetic pattern. Molecular studies have also helped to reveal that the present-day distribution of many organisms is due to historic dispersal events, most likely via rafting. In the wake of these studies it has been increasingly recognised that rafting may have contributed significantly to the species succession and biodiversity of coastal ecosystems and island communities. More species may have reached these habitats via rafting than previously assumed. For example, in an extensive review (Thiel & Gutow 2005b) reported a total of 17 invertebrate species for which rafting was inferred based on genetic data. Twelve of these species have never been observed on or near a raft, but based on all available evidence the authors of the respective studies offered rafting as the most probable explanation for the observed genetic patterns. It is likely that in the future the number of species for which rafting is inferred based on genetic evidence will be increasing. Extensive evidence has been provided that rafting is an important mechanism that affects biodiversity at a local and global level. From frequent to episodic rafting routes there exists a continuum of rafting intensity, distance and selective pressures (= filters) posed to rafters, which influences processes from population dynamics to allopatric speciation. It has been shown that different rafting routes provide varying degrees of connectivity for populations. Also, that organisms with direct development can achieve LDD via rafting and that the Rockall Paradox is no longer a

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paradox. Based on the evidence and examples presented herein, it becomes clear that rafting- mediated dispersal of organisms is yet another process that needs to be taken into account when studying and interpreting the biogeography and evolution of coastal organisms.

Acknowledgements This final part of a series of reviews on the ecology of rafting was originally planned and designed together with Lars Gutow. For work-related reasons Lars finally could not be part of this endeavour. He has contributed enormously to our ideas and concepts about rafting and we are extremely thankful for his unconditional support. Christian Buschbaum, Larry Harris, Irv Kornfield and Peter Smith accepted the challenge to read large parts or the entire version of a preliminary draft. Their thoughtful and constructive comments are deeply appreciated. This manuscript would not have seen the light of day without the enormous help of Ivan Hinojosa who shepherded the literature and of Erasmo Macaya who skilfully prepared many of the figures. We thank them whole-heartedly for their efforts. Any mistakes or misinterpretations are entirely our own responsibility. Funding during the writing of this manuscript was through FONDECYT 1010356 (MT) and 1051076 (PH, MT). MT once more acknowledges a generous invitation by the Alfred Wegener Institute for Polar and Marine Research during the writing phase of this review.

References

Abe, T. 1984. Colonization of the Krakatau Islands by termites (Insecta: Isoptera). Physiology and Ecology Japan 21, 63Ð88. Adami, M.L. & Gordillo, S. 1999. Structure and dynamics of the biota associated with Macrocystis pyrifera (Phaeophyta) from the Beagle Channel, Tierra del Fuego. Scientia Marina 63, 183Ð191. Aliani, S. & Molcard, A. 2003. Hitch-hiking on floating marine debris: macrobenthic species in the Western Mediterranean Sea. Hydrobiologia 503, 59Ð67. Allcock, A.L., Brierley, A.S., Thorpe, J.P. & Rodhouse, P.G. 1997. Restricted gene flow and evolutionary divergence between geographically separated populations of the Antarctic octopus Pareledone turqueti. Marine Biology 129, 97Ð102. Allison, G.W., Gaines, S.D., Lubchenco, J. & Possingham, H.P. 2003. Ensuring persistence of marine reserves: catastrophes require adopting an insurance factor. Ecological Applications 13, S8ÐS24. Alongi, D.M. 1998. Coastal Ecosystem Processes. Boca Raton, FL: CRC Press. Alongi, D.M., Sasekumar, A., Chong, V.C., Pfitzner, J., Trott, L.A., Tirendi, F., Dixon, P. & Brunskill, G.J. 2004. Sediment accumulation and organic material flux in a managed mangrove ecosystem: estimates of land-ocean-atmosphere exchange in peninsular Malaysia. Marine Geology 208, 383Ð402. Altinok, Y. & Ersoy, S. 2000. Tsunamis observed on and near the Turkish coast. Natural Hazards 21, 185Ð205. Andrade, S.C.S., Magalhaes, C.A. & Solferini, V.N. 2003. Patterns of genetic variability in Brazilian Littorinids (Mollusca): a macrogeographic approach. Journal of Zoological Systematic and Evolutionary Research 41, 249Ð255. Anger, K. 2003. Salinity as a key parameter in the larval biology of decapod crustaceans. Invertebrate Reproduction & Development 43, 29Ð45. Arndt, A. & Smith, M.J. 1998. Genetic diversity and population structure in two species of sea cucumber: differing patterns according to mode of development. Molecular Ecology 7, 1053Ð1064. Avise, J.C. 2000. Phylogeography: The History and Formation of Species. Cambridge, MA: Harvard University Press. Ayre, D.J., Davis, A.R., Billingham, M., Llorens, T. & Styan, C. 1997. Genetic evidence for contrasting patterns of dispersal in solitary and colonial ascidians. Marine Biology 130, 51Ð61. Ayre, D.J. & Dufty, S.L. 1994. Evidence for restricted gene flow in the viviparous coral Seriatopora hystrix on Australia Great-Barrier-Reef. Evolution 48, 1183Ð1201.

411 7044_C007.fm Page 412 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

Ayre, D.J. & Hughes, T.P. 2000. Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54, 1590Ð1605. Ayre, D.J. & Hughes, T.P. 2004. Climate change, genotypic diversity and gene flow in reef-building corals. Ecology Letters 7, 273Ð278. Ayre, D.J., Read, J. & Wishart, J. 1991. Genetic subdivision within the Eastern Australian population of the sea-anemone Actinia tenebrosa. Marine Biology 109, 379Ð390. Bach, S., Thayer, G. & LaCroix, M. 1986. Export of detritus from eelgrass (Zostera marina) beds near Beaufort, North Carolina, USA. Marine Ecology Progress Series 28, 265Ð278. Ball, A.O. & Chapman, R.W. 2003. Population genetic analysis of white shrimp, Litopenaeus setiferus, using microsatellite genetic markers. Molecular Ecology 12, 2319Ð2330. Baratti, M., Goti, E. & Messana, G. 2005. High level of genetic differentiation in the marine isopod Sphaeroma terebrans (Crustacea, Isopoda, Sphaeromatidae) as inferred by mitochondrial DNA analysis. Journal of Experimental Marine Biology and Ecology 315, 225Ð234. Barber, P.H., Palumbi, S.R., Erdmann, M.V. & Moosa, M.K. 2000. A marine Wallace’s line? Nature 406, 692Ð693. Barber, P.H., Palumbi, S.R., Erdmann, M.V. & Moosa, M.K. 2002. Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences. Molecular Ecology 11, 659Ð674. Barbour, T. 1916. Some remarks upon Matthew’s “Climate and Evolution”. Annals of the New York Academy of Sciences 27, 1Ð10. Barnes, D.K.A. 2002. Biodiversity: invasions by marine life on plastic debris. Nature 416, 808Ð809. Barnes, D.K.A. & Fraser, K.P.P. 2003. Rafting by five phyla on man-made flotsam in the Southern Ocean. Marine Ecology Progress Series 262, 289Ð291. Barnes, D.K.A. & Milner, P. 2005. Drifting plastic and its consequences for sessile organism dispersal in the Atlantic Ocean. Marine Biology 146, 815Ð825. Barrales, H.L. & Lobban, C.S. 1975. The comparative ecology of Macrocystis pyrifera, with emphasis on the forests of Chubut, Argentina. The Journal of Ecology 63, 657Ð677. Bart, D. & Hartman, J.M. 2003. The role of large rhizome dispersal and low salinity windows in the establishment of common reed, Phragmites australis, in salt marshes: new links to human activities. Estuaries 26, 436Ð443. Bastidas, C., Benzie, J.A.H. & Fabricius, K.E. 2002. Genetic differentiation among populations of the brooding soft coral Clavularia koellikeri on the Great Barrier Reef. Coral Reefs 21, 233Ð241. Bastidas, C., Benzie, J.A.H., Uthicke, S. & Fabricius, K.E. 2001. Genetic differentiation among populations of a broadcast spawning soft coral, Sinularia flexibilis, on the Great Barrier Reef. Marine Biology 138, 517Ð525. Baums, I.B., Miller, M.W. & Hellberg, M.E. 2005. Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Molecular Ecology 14, 1377Ð1390. Baus, E., Darrock, D.J. & Bruford, M.W. 2005. Gene-flow patterns in Atlantic and Mediterranean populations of the Lusitanian sea star Asterina gibbosa. Molecular Ecology 14, 3373Ð3382. Becker, B.J., Fodrie, F.J., McMillan, P.A. & Levin, L.A. 2005. Spatial and temporal variation in trace elemental fingerprints of mytilid mussel shells: a precursor to invertebrate larval tracking. Limnology and Oceanography 50, 48Ð61. Behrens Yamada, S. 1989. Are direct developers more locally adapted than planktonic developers? Marine Biology 103, 403Ð411. Benzie, J.A.H. 1999. Major genetic differences between crown-of-thorns starfish (Acanthaster planci) popu- lations in the Indian and Pacific Oceans. Evolution 53, 1782Ð1795. Benzie, J.A.H. & Williams, S.T. 1997. Genetic structure of giant clam (Tridacna maxima) populations in the West Pacific is not consistent with dispersal by present-day ocean currents. Evolution 51, 768Ð783. Billard, E., Daguin, C., Pearson, G., Serrão, E., Engel, C. & Valero, M. 2005. Genetic isolation between three closely related taxa: Fucus vesiculosus, F. spiralis, and F. ceranoides (Phaophyceae). Journal of Phycology 41, 900Ð905. Billingham, M. & Ayre, D.J. 1996. Genetic subdivision in the subtidal, clonal sea anemone Anthothoe albocincta. Marine Biology 125, 153Ð163.

412 7044_C007.fm Page 413 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

Bingham, B.L. & Young, C.M. 1995. Stochastic events and dynamics of a mangrove root epifaunal community. Pubblicazioni della Stazione Zoologica di Napoli I Marine Ecology 16, 145Ð163. Bockelmann, A.C., Reusch, T.B.H., Bijlsma, R. & Bakker, J.P. 2003. Habitat differentiation vs. isolation-by- distance: the genetic population structure of Elymus athericus in European salt marshes. Molecular Ecology 12, 505Ð515. Bohonak, A.J. 1999. Dispersal, gene flow, and population structure. Quarterly Review of Biology 74, 21Ð45. Boisselier-Dubayle, M.C. & Gofas, S. 1999. Genetic relationships between marine and marginal-marine populations of Cerithium species from the Mediterranean Sea. Marine Biology 135, 671Ð682. Borowitzka, M.A. & Lethbridge, R.C. 1989. Seagrass epiphytes. In Biology of Seagrasses, A.W.D. Larkum et al. (eds). Amsterdam: Elsevier, 458Ð499. Borum, J. 1985. Development of epiphytic communities on eelgrass (Zostera marina L.) along a nutrient gradient in a Danish Estuary. Marine Biology 87, 211Ð218. Böstrom, C. & Bonsdorff, E. 2000. Zoobenthic community establishment and habitat complexity — the importance of seagrass shoot-density, morphology and physical disturbance for faunal recruitment. Marine Ecology Progress Series 205, 123Ð138. Bouchard, V., Creach, V., Lefeuvre, J.C., Bertru, G. & Mariotti, A. 1998. Fate of plant detritus in a European salt marsh dominated by Atriplex portulacoides (L.) Aellen. Hydrobiologia 374, 75Ð87. Bouchard, V. & Lefeuvre, J.C. 2000. Primary production and macro-detritus dynamics in a European salt marsh: carbon and nitrogen budgets. Aquatic Botany 67, 23Ð42. Bradbury, I.R. & Snelgrove, P.V.R. 2001. Contrasting larval transport in demersal fish and benthic invertebrates: the roles of behaviour and advective processes in determining spatial pattern. Canadian Journal of Fisheries and Aquatic Sciences 58, 811Ð823. Bram, J.B., Page, H.M. & Dugan, J.E. 2005. Spatial and temporal variability in early successional patterns of an invertebrate assemblage at an offshore oil platform. Journal of Experimental Marine Biology and Ecology 317, 223Ð237. Breton, S., Dufresne, F., Desrosiers, G. & Blier, P.U. 2003. Population structure of two northern hemisphere polychaetes, Neanthes virens and Hediste diversicolor (Nereididae), with different life-history traits. Marine Biology 142, 707Ð715. Brooks, R.A. 2004. Discovery of Sphaeroma terebrans, a wood-boring isopod, in the red mangrove, Rhizo- phora mangle, habitat of northern Florida Bay. Ambio 33, 171Ð173. Brooks, R.A. & Bell, S.S. 2001. Mobile corridors in marine landscapes: enhancement of faunal exchange at seagrass/sand ecotones. Journal of Experimental Marine Biology and Ecology 264, 67Ð84. Bryan, S.E., Cook, A., Evans, J.P., Colls, P.W., Wells, M.G., Lawrence, M.G., Jell, J.S., Greig, A. & Leslie, R. 2004. Pumice rafting and faunal dispersion during 2001Ð2002 in the Southwest Pacific: record of a dacitic submarine explosive eruption from Tonga. Earth and Planetary Science Letters 227, 135Ð154. Bulleri, F. & Chapman, M.G. 2004. Intertidal assemblages on artificial and natural habitats in marinas on the north-west coast of Italy. Marine Biology 145, 381Ð391. Buschbaum, C., Chapman, A.S. & Saier, B. 2006. How an introduced seaweed can affect epibiota diversity in different coastal systems. Marine Biology 148, 743Ð754. Buschbaum, C. & Gutow, L. 2005. Mass occurrence of an introduced crustacean (Caprella cf. mutica) in the south-eastern North Sea. Helgoland Marine Research 59, 252Ð253. Bushing, W.W. 1994. Biogeographic and ecological implications of kelp rafting as a dispersal vector for marine invertebrates. In Proceedings of the Fourth California Islands Symposium: Update on the Status of Resources, March 22Ð25, 1994, W.L. Halvorson & G.J. Maender (eds). Santa Barbara, CA: Santa Barbara Museum of Natural History, 103Ð110. Cadée, G.C. 2002. Mass stranding of cuttlebones of Sepia orbignyana Férussac, 1826, on Texel, the Nether- lands, in July 2002 (Cephalopoda, Decapoda, Sepiidae). Basteria 66, 113Ð120. Cadée, G.C. 2005. Drifting branches of Crambe maritima L. with fruits. Cahiers de Biologie Marine 46, 217Ð219. Caley, M.J., Carr, M.H., Hixon, M.A., Hughes, T.P., Jones, G.P. & Menge, B.A. 1996. Recruitment and the local dynamics of open marine populations. Annual Review in Ecology and Systematics 27, 477Ð500. California Department of Fish and Game 2000. Giant and bull kelp. Commercial and sport fishing regulations. Unpublished report, Marine Region Kelp Management Team La Jolla, CA.

413 7044_C007.fm Page 414 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

Calsbeek, R. & Smith, T.B. 2003. Ocean currents mediate evolution in island lizards. Nature 426, 552Ð555. Camus, P.A. & Lima, M. 2002. Populations, metapopulations, and the open-closed dilemma: the conflict between operational and natural population concepts. Oikos 97, 433Ð438. Carey, S., Morelli, D., Sigurdsson, H. & Bronto, S. 2001. Tsunami deposits from major explosive eruptions: an example from the 1883 eruption of Krakatau. Geology 29, 347Ð350. Carlton, J.T. & Geller, J.B. 1993. Ecological roulette: the global transport of nonindigenous marine organisms. Science 261, 78Ð82. Carr, M.H., Neigel, J.E., Estes, J.A., Andelmann, S., Warner, R.R. & Largier, J.L. 2003. Comparing marine and terrestrial ecosystems: implications for the design of coastal marine reserves. Ecological Appli- cations 13, S90ÐS107. Carranza, S. & Arnold, E.N. 2003. Investigating the origin of transoceanic distributions: mtDNA shows Mabuya lizards (Reptilia, Scincidae) crossed the Atlantic twice. Systematics and Biodiversity 1, 275Ð282. Carranza, S., Arnold, E.N., Mateo, J.A. & Lopez-Jurado, L.F. 2000. Long-distance colonization and radiation in gekkonid lizards, Tarentola (Reptilia: Gekkonidae), revealed by mitochondrial DNA sequences. Proceedings of the Royal Society Series B Biological Sciences 267, 637Ð649. Carvalho, G.R. & Piertney, S.B. 1997. Interspecific comparisons of genetic population structure in members of the Jaera albifrons species complex. Journal of the Marine Biological Association of the United Kingdom 77, 77Ð93. Casas, V.M., Zaragoza, E.S., Belda, D.L., Marcos, R. & Ramirez, R.A. 2003. Effect of climatic change on the harvest of the kelp Macrocystis pyrifera on the Mexican Pacific Coast. Bulletin of Marine Science 73, 545Ð556. Castilla, J.C. & Guiñez, R. 2000. Disjoint geographical distribution of intertidal and nearshore benthic invertebrates in the southern hemisphere. Revista Chilena de Historia Natural 73, 585Ð603. Castro, J.J., Santiago, J.A. & Santana-Ortega, A.T. 2002. A general theory on fish aggregation to floating objects: an alternative to the meeting point hypothesis. Reviews in Fish Biology and Fisheries 11, 255Ð277. Cebrian, J. & Duarte, C.M. 2001. Detrital stocks and dynamics of the seagrass Posidonia oceanica (L.) Delile in the Spanish Mediterranean. Aquatic Botany 70, 295Ð309. Censky, E.J., Hodge, K. & Dudley, J. 1998. Over-water dispersal of lizards due to hurricanes. Nature 395, 556. Chambers, R.J., McQuaid, C.D. & Kirby, R. 1998. The use of randomly amplified polymorphic DNA to analyze the genetic diversity, the systematic relationships and the evolution of intertidal limpets, Siphonaria spp. (Pulmonata: Gastropoda), with different reproductive modes. Journal of Experimental Marine Biology and Ecology 227, 49Ð66. Chan, J.C.L. & Liu, K.S. 2004. Global warming and western North Pacific typhoon activity from an obser- vational perspective. Journal of Climate 17, 4590Ð4602. Coelho, H., Costa, F.O., Costa, M.H. & Coelho, M.M. 2002. Low genetic variability of the widespread amphipod Gammarus locusta, as evidenced by allozyme electrophoresis of southern European pop- ulations. Crustaceana 75, 1335Ð1348. Colgan, D.J., Byrne, M., Rickard, E. & Castro, L.R. 2005. Limited nucleotide divergence over large spatial scales in the asterinid sea star Patiriella exigua. Marine Biology 146, 263Ð270. Collin, R. 2001. The effects of mode of development on phylogeography and population structure of North Atlantic Crepidula (Gastropoda: Calyptraeidae). Molecular Ecology 10, 2249Ð2262. Colson, I. & Hughes, R.N. 2004. Rapid recovery of genetic diversity of dogwhelk (Nucella lapillus L.) populations after local extinction and recolonization contradicts predictions from life-history charac- teristics. Molecular Ecology 13, 2223Ð2233. Conlan, K.E. & Chess, J.R. 1992. Phylogeny and ecology of a kelp-boring amphipod, Peramphithoe stypo- trupetes, new Species (Corophioidea — Ampithoidae). Journal of Crustacean Biology 12, 410Ð422. Cook, L.G. & Crisp, M.D. 2005. Directional asymmetry of long-distance dispersal and colonization could mislead reconstructions of biogeography. Journal of Biogeography 32, 741Ð754. Coombs, D.S. & Landis, C.S. 1966. Pumice from the South Sandwich eruption of March 1962, reaches New Zealand. Nature 209, 289Ð290.

414 7044_C007.fm Page 415 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

Costa, F.O., Neuparth, T., Theodorakis, C.W., Costa, M.H. & Shugart, L.R. 2004. RAPD analysis of southern populations of Gammarus locusta: comparison with allozyme data and ecological inferences. Marine Ecology Progress Series 277, 197Ð207. Coulson, S.J., Hodkinson, I.D., Webb, N.R. & Harrison, J.A. 2002. Survival of terrestrial soil-dwelling arthropods on and in seawater: implications for trans-oceanic dispersal. Functional Ecology 16, 353Ð356. Cowen, R.K., Paris, C.B., Olson, D.B. & Fortuna, J.L. 2003. The role of long distance dispersal versus local retention in replenishing marine populations. Gulf and Caribbean Research 14, 129Ð137. Cox, C.B. & Moore, P.D. 1993. Biogeography: An Ecological and Evolutionary Approach. Oxford, Blackwell Science. Coyer, J.A., Smith, G.J. & Andersen, R.A. 2001. Evolution of Macrocystis spp. (Phaeophyceae) as determined by ITS1 and ITS2 sequences. Journal of Phycology 37, 574Ð585. Coyer, J.A., Diekmann, O.E., Serrão, E.A., Procaccini, G., Milchakova, N., Pearson, G.A., Stam, W.T. & Olsen, J.L. 2004. Population genetics of dwarf eelgrass Zostera noltii throughout its biogeographic range. Marine Ecology Progress Series 281, 51Ð62. Crisp, D.J. 1958. The spread of Elminius modestus Darwin in North-West Europe. Journal of the Marine Biological Association of the United Kingdom 37, 483Ð520. Cruz, R., Carballo, M., Conde-Padín, P. & Rolán-Alvarez, E. 2004. Testing alternative models for sexual isolation in natural populations of Littorina saxatilis: indirect support for by-product ecological speciation? Journal of Evolutionary Biology 17, 288Ð293. Dalby, D.H. 1963. Seed dispersal in Salicornia pusilla. Nature 199, 197Ð198. Dame, R.F., Koepfler, E. & Gregory, L. 2000. Benthic-pelagic coupling in marsh-estuarine ecosystems. In Concepts and Controversies in Tidal Marsh Ecology, M.P. Weinstein & D.A. Kreeger (eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, 369Ð390. Dana, J.D. 1856. On the origin of the geographical distribution of Crustacea. Annals and Magazine of Natural History 17, 42Ð51. Davenport, J. & Rees, E.I.S. 1993. Observations on neuston and floating weed patches in the Irish Sea. Estuarine Coastal and Shelf Science 36, 395Ð411. Davenport, J. & Stevenson, T.D.I. 1998. Intertidal colonization rates. A matched latitude, north v. south, remote v. near shore island experiment. Diversity and Distributions 4, 87Ð92. Davis, J.L.D., Levin, L.A. & Walther, S.M. 2002. Artificial armored shorelines: sites for open-coast species in a southern California bay. Marine Biology 140, 1249Ð1262. Dayton, P.K. 1985. Ecology of kelp communities. Annual Review of Ecology and Systematics 16, 215Ð245. Dayton, P.K., Currie, V., Gerrodette, T., Keller, B.D., Rosenthal, R. & Ven Tresca, D. 1984. Patch dynamics and stability of some California kelp communities. Ecological Monographs 54, 253Ð289. Dayton, P.K. & Tegner, M.J. 1984. Catastrophic storms, El Niño, and patch stability in a southern California kelp community. Science 71, 776Ð787. De Matthaeis, E., Davolos, D., Cobolli, M. & Ketmaier, V. 2000. Isolation by distance in equilibrium and nonequilibrium populations of four talitrid species in the Mediterranean Sea. Evolution 54, 1606Ð1613. Denno, R.F. 1977. Comparison of the assemblages of sap-feeding insects (Homoptera-Hemiptera) inhabiting two structurally different salt marsh grasses in the genus Spartina. Environmental Entomology 6, 359Ð371. Denno, R.F., Raupp, M.J. & Tallamy, D.W. 1981. Organization of a guild of sap-feeding insect: equilibrium vs. nonequilibrium coexistence. In Insect Life History Patterns: Habitat and Geographic Variation, R.F. Denno & H. Dingle (eds). New York: Springer-Verlag, 151Ð181. de Queiroz, A. 2005. The resurrection of oceanic dispersal in historical biogeography. Trends in Ecology and Evolution 20, 68Ð73. Dethier, M.N., McDonald, K. & Strathmann, R.R. 2003. Colonization and connectivity of habitat patches for coastal marine species distant from source populations. Conservation Biology 17, 1024Ð1035. DeVantier, L.M. 1992. Rafting of tropical marine organisms on buoyant coralla. Marine Ecology Progress Series 86, 301Ð302. Diaz, J.M. 1995. Zoogeography of marine gastropods in the southern Caribbean: a new look at provinciality. Carribbean Journal of Science 31, 104Ð121.

415 7044_C007.fm Page 416 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

Diekmann, O.E., Coyer, J.A., Ferreira, J., Olsen, J.L., Stam, W.T., Pearson, G.A. & Serrão, E.A. 2005. Population genetics of Zostera noltii along the west Iberian coast: consequences of small population size, habitat discontinuity and near-shore currents. Marine Ecology Progress Series 290, 89Ð96. Distel, D.L., Baco, A.R., Chuang, E., Morrill, W., Cavanaugh, C. & Smith, C.R. 2000. Do mussels take wooden steps to deep-sea vents? Nature 403, 725Ð726. Domaneschi, O., da Silva, J., Neto, L. & Passos, F. 2002. New perspectives on the dispersal mechanisms of the Antarctic brooding bivalve Mysella charcoti (Lamy, 1906). Polar Biology 25, 538Ð541. Donald, K.M., Kennedy, M. & Spencer, H.G. 2005. Cladogenesis as the result of long-distance rafting events in South Pacific topshells (Gastropoda, Trochidae). Evolution 59, 1701Ð1711. Duda, T.F. & Palumbi, S.R. 1999. Population structure of the black tiger prawn, Penaeus monodon, among western Indian Ocean and western Pacific populations. Marine Biology 134, 705Ð710. Duffy, J.E. 1993. Genetic population structure in two tropical sponge-dwelling shrimps that differ in dispersal potential. Marine Biology 116, 459Ð470. Dupont, L., Jollivet, D. & Viard, F. 2003. High genetic diversity and ephemeral drift effects in a successful introduced mollusc (Crepidula fornicata: Gastropoda). Marine Ecology Progress Series 253, 183Ð195. Duran, S., Giribet, G. & Turon, X. 2004b. Phylogeographical history of the sponge Crambe crambe (Porifera, Poecilosclerida): range expansion and recent invasion of the Macaronesian islands from the Mediter- ranean Sea. Molecular Ecology 13, 109Ð122. Duran, S., Palacin, C., Becerro, M.A., Turon, X. & Giribet, G. 2004d. Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Molec- ular Ecology 13, 3317Ð3328. Duran, S., Pascual, M., Estoup, A. & Turon, X. 2004a. Strong population structure in the marine sponge Crambe crambe (Poecilosclerida) as revealed by microsatellite markers. Molecular Ecology 13, 511Ð522. Duran, S., Pascual, M. & Turon, X. 2004c. Low levels of genetic variation in mtDNA sequences over the western Mediterranean and Atlantic range of the sponge Crambe crambe (Poecilosclerida). Marine Biology 144, 31Ð35. Eckert, G.L. 2003. Effects of the planktonic period on marine population fluctuations. Ecology 84, 372Ð383. Edgar, G.J. 1987. Dispersal of faunal and floral propagules associated with drifting Macrocystis pyrifera plants. Marine Biology 95, 599Ð610. Edgar, G.J. & Burton, H.R. 2000. The biogeography of shallow-water macrofauna at Heard Island. Papers and Proceedings of the Royal Society of Tasmania 133, 23Ð26. Edmands, S. & Potts, D.C. 1997. Population genetic structure in brooding sea anemones (Epiactis spp.) with contrasting reproductive modes. Marine Biology 127, 485Ð498. Edmands, S., Moberg, P.E. & Burton, R.S. 1996. Allozyme and mitochondrial DNA evidence of population subdivision in the purple sea urchin Strongylocentrotus purpuratus. Marine Biology 126, 443Ð450. Engelen, A.H., Olsen, J.L., Breeman, A.M. & Stam, W.T. 2001. Genetic differentiation in Sargassum polyc- eratium (Fucales: Phaeophyceae) around the island of Curaçao (Netherlands Antilles). Marine Biology 139, 267Ð277. Estevez, E.D. 1978. Ecology of Sphaeroma terebrans Bate, a wood boring isopod, in a Florida mangrove forest. PhD Dissertation University of South Florida. Estevez, E.D. 1994. Inhabitation of tidal salt marshes by the estuarine wood-boring isopod Sphaeroma terebrans in Florida. In Recent Developments in Biofouling Control, M.-F. Thompson et al. (eds). New Delhi: Oxford & IBH Publishing Co. Pvt. Ltd., 97Ð105. Feller, I.C. & Mathis, W.N. 1997. Primary herbivory by wood-boring insects along an architectural gradient of Rhizophora mangle. Biotropica 29, 440Ð451. Feller, I.C. & McKee, K.L. 1999. Small gap creation in Belizean mangrove forests by a wood-boring insect. Biotropica 31, 607Ð617. Féral, J.P., Barré, N., Villard, A.M. & Chenuil, A. 2003. What is the smallest distance of genetic structuring in the brooding ophiuroid Amphipholis squamata from the Western Mediterranean? In Echinoderm Research 2001: Proceedings of the 6th European Conference on Echinoderm Research, Banyuls-sur- Mer, 3Ð7 September 2001, J.P. Féral & B. David (eds). Lisse, NL: Swets & Zeitlinger Publishers, 23Ð27.

416 7044_C007.fm Page 417 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

Féral, J.P., Villard, A.M., Dupont, S. & Mallefet, J. 2001. Morphological, physiological and genetic variability of the ophiuroid Amphipholis squamata from the lagoon system of Oliveri-Tindari (Sicily). In Proc 10th Int Echinoderm Conf, Echinoderm 2000, Dunedin, NZ, M. Barrer (ed.). Lisse, NL: Swets & Zeitlinger Publishers, 261Ð266. Flach, E.C. 1992. The influence of four macrozoobenthic species on the abundance of the amphipod Corophium volutator on tidal flats of the Wadden Sea. Netherlands Journal of Sea Research 29, 379Ð394. Flindt, M.R., Neto, J., Amos, C.L., Pardal, M.A., Bergamasco, A., Pedersen, C.B. & Andersen, F.¯. 2004. Plant bound nutrient transport. Mass transport in estuaries and lagoons. In Estuarine Nutrient Cycling: The Influence of Primary Producers, S. Nielsen et al. (eds). Dordrecht, The Netherlands: Kluwer Academis Publichers, 93Ð128. Franke, H.-D., Gutow, L. & Janke, M. 1999. The recent arrival of the oceanic isopod Idotea metallica Bosc off Helgoland (German Bight, North Sea): an indication of a warming trend in the North Sea? Helgoländer Meeresuntersuchungen 52, 347Ð357. Fratini, S. & Vannini, M. 2002. Genetic differentiation in the mud crab Scylla serrata (Decapoda : Portunidae) within the Indian Ocean. Journal of Experimental Marine Biology and Ecology 272, 103Ð116. Fredriksen, S., Christie, H. & Saethre, B.A. 2005. Species richness in macroalgae and macrofauna assemblages on Fucus serratus L. (Phaeophyceae) and Zostera marina L. (Angiospermae) in Skagerrak, Norway. Marine Biology Research 1, 2Ð19. Frick, C. & Kent, L.E. 1984. Drift pumice in the Indian and South Atlantic Oceans. Transactions of the Geological Society of South Africa 87, 19Ð33. Fushimi, K., Nishikawa, M. & Mitsuda, H. 1991. Floating pumices in the western North Pacific. Oceanogr. Mag./Kishocho Obun Kaiyo Hokoku. 41, 59Ð74. Gaines, S.D. & Bertness, M.D. 1992. Dispersal of juveniles and variable recruitment in sessile marine species. Nature 360, 579Ð580. Gaines, S.D., Gaylord, B. & Largier, J.L. 2003. Avoiding current oversights in marine reserve design. Eco- logical Applications 13, S32ÐS46. Gerber, L.R., Heppell, S.S., Ballantyne, F. & Sala, E. 2005. The role of dispersal and demography in determining the efficacy of marine reserves. Canadian Journal of Fisheries and Aquatic Sciences 62, 863Ð871. Gerber, L.R., Botsford, L.W., Hastings, A., Possingham, H.P., Gaines, S.D., Palumbi, S.R. & Andelman, S. 2003. Population models for marine reserve design: a retrospective and prospective synthesis. Eco- logical Applications 13, S47ÐS64. Glor, R.E., Losos, J.B. & Larson, A. 2005. Out of Cuba: overwater dispersal and speciation among lizards in the Anolis carolinensis subgroup. Molecular Ecology 14, 2419Ð2432. Glynn, P.W. & Ault, J.S. 2000. A biogeographic analysis and review of the far eastern Pacific coral reef region. Coral Reefs 19, 1Ð23. Goffredo, S. & Zaccanti, F. 2004. Laboratory observations of larval behavior and metamorphosis in the Mediterranean solitary coral Balanophyllia europaea (Scleractinia, Dendrophylliidae). Bulletin of Marine Science 74, 449Ð457. Goldson, A.J., Hughes, R.N. & Gliddon, C.J. 2001. Population genetic consequences of larval dispersal mode and hydrography: a case study with bryozoans. Marine Biology 138, 1037Ð1042. Govindarajan, A.F., Halanych, K.K. & Cunningham, C.W. 2005. Mitochondrial evolution and phylogeography in the hydrozoan Obelia geniculata (Cnidaria). Marine Biology 146, 213Ð222. Grantham, B.A. 1997. Coastal upwelling, larval recruitment and the dynamics of intertidal barnacle commu- nities. PhD Thesis, Stanford University, CA, U.S. Grantham, B.A., Eckert, G.L. & Shanks, A.L. 2003. Dispersal potential of marine invertebrates in diverse habitats. Ecological Applications 13, S108ÐS116. Green, A.J. & Figuerola, J. 2005. Recent advances in the study of long-distance dispersal of aquatic inverte- brates via birds. Diversity and Distributions 11, 149Ð156. Grimm, V., Reise, K. & Strasser, M. 2003. Marine metapopulations: a useful concept? Helgoland Marine Research 56, 222Ð228.

417 7044_C007.fm Page 418 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

Grosberg, R.K. & Cunningham, C.W. 2001. Genetic structure in the sea: from populations to communities. In Marine Community Ecology, M.D. Bertness et al. (eds). Sunderland, MA: Sinauer Associates Inc., 61Ð84. Guichard, F., Levin, S.A., Hastings, A. & Siegel, D. 2004. Toward a dynamic metacommunity approach to marine reserve theory. Bioscience 54, 1003Ð1011. Gutiérrez-Rodríguez, C. & Lasker, H.R. 2004. Microsatellite variation reveals high levels of genetic variability and population structure in the gorgonian coral Pseudopterogorgia elisabethae across the Bahamas. Molecular Ecology 13, 2211Ð2221. Gutow, L. 2003. Local population persistence as a pre-condition for large scale dispersal of Idotea metallica (Crustacea: Isopoda) on drifting habitat patches. Hydrobiologia 503, 45Ð48. Gutow, L. & Franke, H.-D. 2001. On the current and possible future status of the neustonic isopod Idotea metallica Bosc in the North Sea: a laboratory study. Journal of Sea Research 45, 37Ð44. Gutow, L. & Franke, H.-D. 2003. Metapopulation structure of the marine isopod Idotea metallica, a species associated with drifting habitat patches. Helgoland Marine Research 56, 259Ð264. Halpern, B.S. 2003. The impact of marine reserves: do reserves work and does reserve size matter? Ecological Applications 13, S117ÐS137. Hare, M.P. & Weinberg, J.R. 2005. Phylogeography of surfclams, Spisula solidissima, in the western North Atlantic based on mitochondrial and nuclear DNA sequences. Marine Biology 146, 707Ð716. Harrison, S. & Hastings, A. 1996. Genetic and evolutionary consequences of metapopulation structure. Trends in Ecology & Evolution 11, 180Ð183. Harrold, C. & Lisin, S. 1989. Radio-tracking rafts of giant kelp: local production and regional transport. Journal of Experimental Marine Biology and Ecology 130, 237Ð251. Harwell, M.C. & Orth, R.J. 2002. Long-distance dispersal potential in a marine macrophyte. Ecology 83, 3319Ð3330. Havenhand, J.N. 1995. Evolutionary ecology of larval types. In Ecology of Marine Invertebrate Larvae, L.R. McEdward (ed.). Boca Raton, FL: CRC Press, 79Ð122. Heatwole, H. & Levins, R. 1972. Biogeography of the Puerto Rican Bank: flotsam transport of terrestrial animals. Ecology 53, 112Ð117. Hedgecock, D. 1986. Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bulletin of Marine Science 39, 550Ð564. Hellberg, M.E. 1994. Relationships between inferred levels of gene flow and geographic distance in a philopatric coral, Balanophyllia elegans. Evolution 48, 1829Ð1854. Hellberg, M.E. 1996. Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution 50, 1167Ð1175. Hellberg, M.E., Burton, R.S., Neigel, J.E. & Palumbi, S.R. 2002. Genetic assessment of connectivity among marine populations. Bulletin of Marine Science 70, 273Ð290. Helmuth, B., Veit, R.R. & Holberton, R. 1994. Long-distance dispersal of a sub-antarctic brooding bivalve (Gaimardia trapesina) by kelp-rafting. Marine Biology 120, 421Ð426. Hemminga, M.A., van Soelen, J. & Koutstaal, B.P. 1990. Tidal dispersal of salt marsh insect larvae within the Westerschelde estuary. Holarctic Ecology 13, 308Ð315. Highsmith, R.C. 1985. Floating and algal rafting as potential dispersal mechanisms in brooding invertebrates. Marine Ecology Progress Series 25, 169Ð179. Hoagland, K.E. 1985. Genetic relationships between one British and several North American populations of Crepidula fornicata based on allozyme studies (Gastropoda: Calyptraeidae). Journal of Molluscan Studies 51, 177Ð182. Hobday, A.J. 2000a. Age of drifting Macrocystis pyrifera (L.) C. Agardh rafts in the Southern California Bight. Journal of Experimental Marine Biology and Ecology 253, 97Ð114. Hobday, A.J. 2000b. Abundance and dispersal of drifting kelp Macrocystis pyrifera rafts in the Southern California Bight. Marine Ecology Progress Series 195, 101Ð116. Hobday, A.J. 2000c. Persistence and transport of fauna on drifting kelp (Macrocystis pyrifera (L.) C. Agardh) rafts in the Southern California Bight. Journal of Experimental Marine Biology and Ecology 253, 75Ð96.

418 7044_C007.fm Page 419 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

Hodson, S.L., Lewis, T.E. & Burke, C.M. 1997. Biofouling of fish-cage netting: efficacy and problems of in situ cleaning. Aquaculture 152, 77Ð90. Holt, R.D., Barfield, M. & Gomulkiewicz, R. 2005. Theories of niche conservatism and evolution: could exotic species be potential tests? In Species Invasions: Insights into Ecology, Evolution, and Biogeography. D.F. Sax et al. (eds). Sunderland, MA: Sinauer Associates Inc., 259Ð290. Hoskin, M.G. 1997. Effects of contrasting modes of larval development on the genetic structures of populations of three species of prosobranch gastropods. Marine Biology 127, 647Ð656. Huiskes, A.H.L., Koutstaal, B.P., Herman, P.M.J., Beeftink, W.G., Markusse, M.M. & Demunck, W. 1995. Seed dispersal of halophytes in tidal salt marshes. Journal of Ecology 83, 559Ð567. Hunt, A. 1993. Effects of contrasting patterns of larval dispersal on the genetic connectedness of local populations of two intertidal starfish, Patiriella calcar and P. exigua. Marine Ecology Progress Series 92, 179Ð186. Hunt, A. & Ayre, D.J. 1989. Population structure in the sexually reproducing sea anemone Oulactis muscosa. Marine Biology 102, 537Ð544. Ingólfsson, A. 1992. The origin of the rocky shore fauna of Iceland and the Canadian Maritimes. Journal of Biogeography 19, 705Ð712. Ingólfsson, A. 1995. Floating clumps of seaweed around Iceland: natural microcosms and a means of dispersal for shore fauna. Marine Biology 122, 13Ð21. Ingólfsson, A. 1998. Dynamics of macrofaunal communities of floating seaweed clumps off western Iceland: a study of patches on the surface of the sea. Journal of Experimental Marine Biology and Ecology 231, 119Ð137. Ingólfsson, A. & Kristjánsson, B.K. 2002. Diet of juvenile lumpsucker Cyclopterus lumpus (Cyclopteridae) in floating seaweed: effects of ontogeny and prey availability. Copeia 2002, 472Ð476. Jablonski, D. 1986. Larval ecology and macroevolution in marine invertebrates. Bulletin of Marine Science 39, 565Ð587. Jablonski, D. & Lutz, R.A. 1983. Larval ecology of marine benthic invertebrates: paleobiological implications. Biological Review 58, 21Ð89. Jackson, J.B.C. 1986. Modes of dispersal of clonal benthic invertebrates: consequences for species’ distribu- tions and genetic structure of local populations. Bulletin of Marine Science 39, 588Ð606. Janson, K. 1987a. Allozyme and shell variation in two marine snails (Littorina, Prosobranchia) with different dispersal abilities. Biological Journal of the Linnean Society 30, 245Ð257. Janson, K. 1987b. Genetic drift in small and recently founded populations of the marine snail Littorina saxatilis. Heredity 58, 31Ð37. Jennerjahn, T.C. & Ittekkot, V. 2002. Relevance of mangroves for the production and deposition of organic matter along tropical continental margins. Naturwissenschaften 89, 23Ð30. Johannesson, K. 1988. The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more wide- spread than one having a planktonic larval dispersal stage (L. littorea)? Marine Biology 99, 507Ð513. Johannesson, K. 1989. The bare zone of Swedish rocky shores: why is it there. Oikos 54, 77Ð86. Johannesson, K. 2003. Evolution in Littorina: ecology matters. Journal of Sea Research 49, 107Ð117. Johannesson, K., Lundberg, J., Andre, C. & Nilsson, P.G. 2004. Island isolation and habitat heterogeneity correlate with DNA variation in a marine snail (Littorina saxatilis). Biological Journal of the Linnean Society 82, 377Ð384. Johannesson, K. & Tatarenkov, A. 1997. Allozyme variation in a snail (Littorina saxatilis) — deconfounding the effects of microhabitat and gene flow. Evolution 51, 402Ð409. Johannesson, K. & Warmoes, T. 1990. Rapid colonization of Belgian breakwaters by the direct developer, Littorina saxatilis (Olivi) (Prosobranchia, Mollusca), 99Ð108. Johansen, S. 1999. Origin of driftwood in north Norway and its relevance for transport routes of drift ice and pollution to the Barents Sea. Science of the Total Environment 231, 201Ð225. Johansen, S. & Hytteborn, H. 2001. A contribution to the discussion of biota dispersal with drift ice and driftwood in the North Atlantic. Journal of Biogeography 28, 105Ð115. Johnson, M.P., Allcock, A.L., Pye, S.E., Chambers, S.J. & Fitton, D.M. 2001. The effects of dispersal mode on the spatial distribution patterns of intertidal molluscs. Journal of Animal Ecology 70, 641Ð649.

419 7044_C007.fm Page 420 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

Johnson, M.S. & Black, R. 1984a. The Wahlund effect and the geographical scale of variation in the intertidal limpet Siphonaria sp. Marine Biology 79, 295Ð302. Johnson, M.S. & Black, R. 1984b. Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 38, 1371Ð1383. Johnson, M.S. & Black, R. 1995. Neighbourhood size and the importance of barriers to gene flow in an intertidal snail. Heredity 75, 142Ð154. Johnson, M.S. & Black, R. 1998. Effects of isolation by distance and geographical discontinuity on genetic subdivision of Littoraria cingulata. Marine Biology 132, 295Ð303. Jokiel, P.L. 1984. Long distance dispersal of reef corals by rafting. Coral Reefs 3, 113Ð116. Jokiel, P.L. 1989. Rafting of reef corals and other organisms at Kwajalein Atoll. Marine Biology 101, 483Ð493. Jokiel, P.L. 1990a. Long-distance dispersal by rafting: reemergence of an old hypothesis. Endeavour 14, 66Ð73. Jokiel, P.L. 1990b. Transport of reef corals into the Great Barrier Reef. Nature 347, 665Ð667. Jokiel, P.L. & Cox, E.F. 2003. Drift pumice at Christmas Island and Hawaii: evidence of oceanic dispersal patterns. Marine Geology 202, 121Ð133. Jolly, M.T., Rogers, A.D. & Sheader, M. 2003b. Microgeographic genetic variation of populations of Idotea chelipes (Crustacea: Isopoda) in lagoons of the southern English coast. Cahiers de Biologie Marine 44, 319Ð327. Jolly, M.T., Viard, F., Weinmayr, G., Gentil, F., Thiebaut, E. & Jollivet, D. 2003a. Does the genetic structure of Pectinaria koreni (Polychaeta: Pectinariidae) conform to a source-sink metapopulation model at the scale of the Baie de Seine? Helgoland Marine Research 56, 238Ð246. Jones, G.P., Milicich, M.J., Emslie, M.J. & Lunow, C. 1999. Self-recruitment in a coral reef fish population. Nature 402, 802Ð804. Jones, L.G. 1971. Studies on selected small herbivorous invertebrates inhabiting Macrocystis canopies and holdfasts in southern California kelp beds. Beiheft Nova Hedwigia 32, 343Ð367. Kathiresan, K. & Bingham, B.L. 2001. Biology of mangroves and mangrove ecosystems. Advances in Marine Biology 40, 81Ð251. Keough, M.J. & Chernoff, H. 1987. Dispersal and population variation in the bryozoan Bugula neritina. Ecology 68, 199Ð210. Kimura, M. & Weiss, G.H. 1964. The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49, 561Ð576. Kingsford, M.J. 1992. Drift algae and small fish in coastal waters of northeastern New Zealand. Marine Ecology Progress Series 80, 41Ð55. Kingsford, M.J. 1995. Drift algae: a contribution to near-shore habitat complexity in the pelagic environment and an attractant for fish. Marine Ecology Progress Series 116, 297Ð301. Kingsford, M.J. & Choat, J.H. 1985. The fauna associated with drift algae captured with a plankton-mesh purse seine net. Limnology and Oceanography 30, 618Ð630. Kingsford, M.J. & Choat, J.H. 1986. Influence of surface slicks on the distribution and onshore movements of small fish. Marine Biology 91, 161Ð171. Kinlan, B.P. & Gaines, S.D. 2003. Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 94, 2007Ð2020. Kinlan, B.P., Gaines, S.D. & Lester, S.E. 2005. Propagule dispersal and the scales of marine community process. Diversity and Distributions 11, 139Ð148. Kitching, J.A. 1987. The flora and fauna associated with Himanthalia elongata (L.) S. F. Gray in relation to water current and wave action in the Lough Hyne Marine Nature Reserve. Estuarine and Costal Shelf Science 25, 663Ð676. Knight-Jones, P. & Knight-Jones, E.W. 1984. Systematics, ecology and distribution of Southern Hemisphere spirorbids. In Proceedings of the First International Polychaete Conference, P.A. Hutchings (ed.). Sydney, N.S.W.: Linnean Society, 196Ð210. Kornicker, L.S. & Squires, D.F. 1962. Floating corals: a possible source of erroneous distribution data. Limnology and Oceanography 7, 447Ð452. Koutstaal, B.P., Markusse, M.M. & de Munck, W. 1987. Aspects of seed dispersal by tidal movements. In Vegetation between Land and Sea, A.H.L. Huiskes et al. (eds). Dordrecht, The Netherlands: Dr. W. Junk Publishers, 226Ð233.

420 7044_C007.fm Page 421 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

Krauss, K.W., Doyle, T.W., Twilley, R.R., Smith, T.J., Whelan, K.R.T. & Sullivan, J.K. 2005. Woody debris in the mangrove forests of South Florida. Biotropica 37, 9Ð15. Kulikov, E.A., Rabinovich, A.B. & Thomson, R.E. 2005. Estimation of tsunami risk for the coasts of Peru and northern Chile. Natural Hazards 35, 185Ð209. Kyle, C.J. & Boulding, E.G. 2000. Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Marine Biology 137, 835Ð845. Lambert, W.J., Todd, C.D. & Thorpe, J.P. 2003. Genetic population structure of two intertidal nudibranch molluscs with contrasting larval types: temporal variation and transplant experiments. Marine Biology 142, 461Ð471. Landsea, C.W., Nicholls, N., Gray, W.M. & Avila, L.A. 1996. Downward trends in the frequency of intense Atlantic hurricanes during the past five decades. Geophysical Research Letters 23, 1697Ð1700. Lapègue, S., Boutet, I., Leitão, A., Heurtebise, S., Garcia, P., Thiriot-Quiévreux, C. & Boudry, P. 2002. Trans- Atlantic distribution of a mangrove oyster species revealed by 16S mtDNA and karyological analyses. Biological Bulletin (Woods Hole) 202, 232Ð242. Largier, J.L. 2003. Considerations in estimating larval dispersal distances from oceanographic data. Ecological Applications 13, S71ÐS89. Le Gac, M., Féral, J.-P., Poulin, E., Veyret, M. & Chenuil, A. 2004. Identification of allopatric clades in the cosmopolitan ophiurid species complex Amphipholis squamata (Echinodermata). The end of a para- dox? Marine Ecology Progress Series 278, 171Ð178. Lee, S.Y. 1999. The effect of mangrove leaf litter enrichment on macrobenthic colonization of defaunated sandy substrates. Estuarine Coastal and Shelf Science 49, 703Ð712. Lessios, H.A., Kessing, B.D. & Robertson, D.R. 1998. Massive gene flow across the world’s most potent marine biogeographic barrier. Proceedings of the Royal Society Series B Biological Sciences 265, 583Ð588. Lessios, H.A., Kessing, B.D. & Pearse, J.S. 2001. Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55, 955Ð975. Lessios, H.A., Weinberg, J.R. & Starczak, V.R. 1994. Temporal variation in populations of the marine isopod Excirolana — how stable are gene-frequencies and morphology. Evolution 48, 549Ð563. Levin, L.A. 1984. Life history and dispersal patterns in a dense infaunal polychaete assemblage: community structure and response to disturbance. Ecology 65, 1185Ð1200. Levin, L.A. & Bridges, T.S. 1995. Pattern and diversity in reproduction and Development. In Ecology of Marine Invertebrate Larvae, L.R. McEdward (ed.). Boca Raton, FL: CRC Press, 1Ð48. Levin, L.A. & Talley, T.S. 2002. Natural and manipulated sources of heterogeneity controlling early faunal development of a salt marsh. Ecological Applications 12, 1785Ð1802. Lewis, P.N., Riddle, M.J. & Smith, S.D.A. 2005. Assisted passage or passive drift: a comparison of alternative transport mechanisms for non-indigenous coastal species into the Southern Ocean. Antarctic Science 17, 183Ð191. Locke, A. & Corey, S. 1989. Amphipods, isopods and surface currents: a case for passive dispersal in the Bay of Fundy, Canada. Journal of Plankton Research 11, 419Ð430. Lourie, S.A., Green, D.M. & Vincent, A.C.J. 2005. Dispersal, habitat differences, and comparative phylogeog- raphy of Southeast Asian seahorses (Syngnathidae: Hippocampus). Molecular Ecology 14, 1073Ð1094. Lubchenco, J., Palumbi, S.R., Gaines, S.D. & Andelman, S. 2003. Plugging a hole in the ocean: the emerging science of marine reserves. Ecological Applications 13, S3ÐS7. Luttikhuizen, P.C., Drent, J. & Baker, A.J. 2003. Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal. Molecular Ecology 12, 2215Ð2229. MacArthur, R.H. & Wilson, E.O. 1967. The Theory of Island Biogeography. New York: Princeton University Press. Macaya, E.C., Boltaña, S., Hinojosa, I.A., Macchiavello, J.E., Valdivia, N.A., Vásquez, N.R., Buschmann, A.H., Vásquez, J.A., Vega, J.M.A. & Thiel, M. 2005. Presence of sporophylls in floating kelp rafts of Macrocystis spp. (Phaeophyceae) along the Chilean Pacific Coast. Journal of Phycology 41, 913Ð922. Mackenzie, J.B., Munday, P.L., Willis, B.L., Miller, D.J. & van Oppen, M.J.H. 2004. Unexpected patterns of genetic structuring among locations but not colour morphs in Acropora nasuta (Cnidaria; Scleractinia). Molecular Ecology 13, 9Ð20.

421 7044_C007.fm Page 422 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

Magalon, H., Adjeroud, M. & Veuille, M. 2005. Patterns of genetic variation do not correlate with geographical distance in the reef-building coral Pocillopora meandrina in the South Pacific. Molecular Ecology 14, 1861Ð1868. Marchand, C., Lallier-Verges, E. & Baltzer, F. 2003. The composition of sedimentary organic matter in relation to the dynamic features of a mangrove-fringed coast in French Guiana. Estuarine Coastal and Shelf Science 56, 119Ð130. Marko, P.B. 2004. ‘What’s larvae got to do with it?’ Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential. Molecular Ecology 13, 597Ð611. Marko, P.B. 2005. An intraspecific comparative analysis of character divergence between sympatric species. Evolution 59, 554Ð564. Martel, A. & Chia, F.-S. 1991. Drifting and dispersal of small bivalves and gastropods with direct development. Journal of Experimental Marine Biology and Ecology 150, 131Ð147. Martínez, E.A., Cardenas, L. & Pinto, R. 2003. Recovery and genetic diversity of the intertidal kelp Lessonia nigrescens 20 years after El Niño 1982/83. Journal of Phycology 39, 504Ð508. Maruyama, T. & Kimura, M. 1980. Genetic variability and effective population size when local extinction and recolonization of subpopulations are frequent. Proceedings of the National Academy of Sciences, USA 77, 6710Ð6714. Maser, C. & Sedell, J.R. 1994. From the Forest to the Sea. The Ecology of Wood in Streams, Rivers, Estuaries, and Oceans. Delray Beach, FL: St. Lucie Press. Masó, M., Garces, E., Pages, F. & Camp, J. 2003. Drifting plastic debris as a potential vector for dispersing Harmful Algal Bloom (HAB) species. Scientia Marina 67, 107Ð111. McCartney, M.A., Keller, G. & Lessios, H.A. 2000. Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Molecular Ecology 9, 1391Ð1400. McEdward, L.R. 1995. Ecology of Marine Invertebrate Larvae. Boca Raton, FL: CRC Press. McFadden, C.S. 1997. Contributions of sexual and asexual reproduction to population structure in the clonal soft coral, Alcyonium rudyi. Evolution 51, 112Ð126. McMillan, W.O., Raff, R.A. & Palumbi, S.R. 1992. Population genetic consequences of developmental evolution in sea-urchins (Genus Heliocidaris). Evolution 46, 1299Ð1312. Menzies, R.J. 1957. The marine borer family Limnoriidae (Crustacea, Isopoda). Part I: Northern and Central America: systematics, distribution and ecology. Bulletin of Marine Science of the Gulf and Caribbean 7, 101Ð200. Mfilinge, P.L., Meziane, T., Bachok, Z. & Tsuchiya, M. 2005. Litter dynamics and particulate organic matter outwelling from a subtropical mangrove in Okinawa Island, South Japan. Estuarine Coastal and Shelf Science 63, 301Ð313. Mileikovsky, S.A. 1971. Types of larval development in marine bottom invertebrates, their distribution and ecological significance: a reevaluation. Marine Biology 10, 193Ð213. Miller, K.A., Olsen, J.L. & Stam, W.T. 2000. Genetic divergence correlated with morphological and ecological subdivision in the deep-water elk kelp, Pelagophycus porra (Phaeophyceae). Journal of Phycology 36, 862Ð870. Mora, C. & Sale, P.F. 2002. Are populations of coral reef fish open or closed? Trends in Ecology & Evolution 17, 422Ð428. Mortensen, T. 1933. Papers from Dr. Th. Mortensen’s Pacific Expedition 1914–16. LXVI. The echinoderms of St. Helena (other than Crinoids). Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kj¿benhavn 93, 401Ð473. Moseman, S.M., Levin, L.A., Currin, C. & Forder, C. 2004. Colonization, succession, and nutrition of macrobenthic assemblages in a restored wetland at Tijuana Estuary, California. Estuarine Coastal and Shelf Science 60, 755Ð770. Mukai, H. 1971. The phytal animals on the thalli of Sargassum serratifolium in the Sargassum region, with reference to their seasonal fluctuations. Marine Biology 8, 170Ð182. Muñiz-Salazar, R., Talbot, S.L., Sage, G.K., Ward, D.H. & Cabello-Pasini, A. 2005. Population genetic structure of annual and perennial populations of Zostera marina L. along the Pacific coast of Baja California and the Gulf of California. Molecular Ecology 14, 711Ð722.

422 7044_C007.fm Page 423 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

Murray-Jones, S.E. & Ayre, D.J. 1997. High levels of gene flow in the surf bivalve Donax deltoides (Bivalvia: Donacidae) on the east coast of Australia. Marine Biology 128, 83Ð89. Neigel, J.E. 1997. A comparison of alternative strategies for estimating gene flow from genetic markers. Annual Review of Ecology and Systematics 28, 105Ð128.

Neigel, J.E. 2002. Is FST obsolete? Conservation Genetics 3, 167Ð173. Niedbala, W. 1998. Ptyctimous mites of the Pacific Islands. Recent knowledge, origin, descriptions, redescrip- tions, diagnoses and zoogeography (Acari: Oribatida). Genus 9, 431Ð458. Norton, T.A. & Benson, M.R. 1983. Ecological interactions between the brown seaweed Sargassum muticum and its associated fauna. Marine Biology 75, 169Ð177. Ó Foighil, D. 1989. Planktotrophic larval development is associated with a restricted geographic range in Lasaea, a genus of brooding, hermaphroditic bivalves. Marine Biology 103, 349Ð358. Ó Foighil, D., Jennings, R., Park, J.K. & Merriwether, D.A. 2001. Phylogenetic relationships of mid-oceanic ridge and continental lineages of Lasaea spp. (Mollusca: Bivalvia) in the northeastern Atlantic. Marine Ecology Progress Series 213, 165Ð175. Ó Foighil, D. & Jozefowicz, C.J. 1999. Amphi-Atlantic phylogeography of direct-developing lineages of Lasaea, a genus of brooding bivalves. Marine Biology 135, 115Ð122. Ó Foighil, D., Marshall, B.A., Hilbish, T.J. & Pino, M.A. 1999. Trans-Pacific range extension by rafting is inferred for the flat oyster Ostrea chilensis. Biological Bulletin (Woods Hole) 196, 122Ð126. Odum, E.P. & Heald, E.J. 1975. The detritus based food web of an estuarine mangrove community. In Estuarine Research, L.E. Cronin (ed.). New York: Academic Press, 265Ð286. Ojeda, F.P. & Santelices, B. 1984. Invertebrate communities in holdfasts of the kelp Macrocystis pyrifera from southern Chile. Marine Ecology Progress Series 16, 65Ð73. Olsen, J.L., Stam, W.T., Coyer, J.A., Reusch, T.B.H., Billingham, M., Bostrom, C., Calvert, E., Christie, H., Granger, S., La Lumiere, R., Milchakova, N., Oudot-Le Secq, M.P., Procaccini, G., Sanjabi, B., Serrão, E., Veldsink, J., Widdicombe, S. & Wyllie-Echeverria, S. 2004. North Atlantic phylogeography and large- scale population differentiation of the seagrass Zostera marina L. Molecular Ecology 13, 1923Ð1941. Orav-Kotta, H. & Kotta, J. 2004. Food and habitat choice of the isopod Idotea baltica in the northeastern Baltic Sea. Hydrobiologia 514, 79Ð85. Orr, M., Zimmer, M., Jelinski, D.E. & Mews, M. 2005. Wrack deposition on different beach types: spatial and temporal variation in the pattern of subsidy. Ecology 86, 1496Ð1507. Palumbi, S.R. 1994. Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics 25, 547Ð572. Palumbi, S.R. 1995. Using genetics as an indirect estimator of larval dispersal. In Ecology of Marine Inver- tebrate Larvae, L.R. McEdward (ed.). Boca Raton, FL: CRC Press, 323Ð367. Palumbi, S.R. 2003. Population genetics, demographic connectivity, and the design of marine reserves. Ecological Applications 13, S159ÐS169. Palumbi, S.R. 2004. Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annual Review of Environment and Resources 29, 31Ð68. Palumbi, S.R., Grabowsky, G., Duda, T., Geyer, L. & Tachino, N. 1997. Speciation and population genetic structure in tropical Pacific Sea urchins. Evolution 51, 1506Ð1517. Panova, M. & Johannesson, K. 2004. Microscale variation in Aat (aspartate aminotransferase) is supported by activity differences between upper and lower shore allozymes of Littorina saxatilis. Marine Biology 144, 1157Ð1164. Pardo, L.M. & Johnson, L.E. 2005. Explaining variation in life-history traits: growth rate, size, and fecundity in a marine snail across an environmental gradient lacking predators. Marine Ecology Progress Series 296, 229Ð239. Parker, P.G., Snow, A.A., Schug, M.D., Booton, G.C. & Fuerst, P.A. 1998. What molecules can tell us about populations: choosing and using a molecular marker. Ecology 79, 361Ð382. Paulay, G. & Meyer, C. 2002. Diversification in the tropical Pacific: comparisons between marine and terrestrial systems and the importance of founder speciation. Integrative and Comparative Biology 42, 922Ð934. Pechenik, J.A. 1999. On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Marine Ecology Progress Series 177, 269Ð297.

423 7044_C007.fm Page 424 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

Pérez-Figueroa, A., Cruz, F., Carvajal-Rodriguez, A., Rolán-Alvarez, E. & Caballero, A. 2005. The evolution- ary forces maintaining a wild polymorphism of Littorina saxatilis: model selection by computer simulations. Journal of Evolutionary Biology 18, 191Ð202. Perrin, C., Wing, S.R. & Roy, M.S. 2004. Effects of hydrographic barriers on population genetic structure of the sea star Coscinasterias muricata (Echinodermata, Asteroidea) in the New Zealand fiords. Molec- ular Ecology 13, 2183Ð2195. Peterson, M.A., Denno, R.F. & Robinson, L. 2001. Apparent widespread gene flow in the predominantly flightless planthopper Tumidagena minuta. Ecological Entomology 26, 629Ð637. Pfeiler, E., Hurtado, L.A., Knowles, L.L., Torre-Cosio, J., Bourillon-Moreno, L., Marquez-Farias, J.F. & Montemayor-Lopez, G. 2005. Population genetics of the swimming crab Callinectes bellicosus (Brachyura: Portunidae) from the eastern Pacific Ocean. Marine Biology 146, 559Ð569. Piertney, S.B. & Carvalho, G.R. 1994. Microgeographic genetic differentiation in the intertidal isopod Jaera albifrons Leach.1. spatial-distribution of allozyme variation. Proceedings of the Royal Society Series B Biological Sciences 256, 195Ð201. Piertney, S.B. & Carvalho, G.R. 1995. Detection of high levels of genetic relatedness in rock-populations of an intertidal isopod using DNA fingerprinting. Journal of the Marine Biological Association of the United Kingdom 75, 967Ð976. Pinegina, T.K., Bourgeois, J., Bazanova, L.I., Melekestsev, I.V. & Braitseva, O.A. 2003. A millennial-scale record of holocene tsunamis on the Kronotskiy Bay coast, Kamchatka, Russia. Quaternary Research 59, 36Ð47. Pinn, E.H., Mitchell, K. & Corkill, J. 2005. The assemblages of groynes in relation to substratum age, aspect and microhabitat. Estuarine Coastal and Shelf Science 62, 271Ð282. Porter, J.S., Ryland, J.S. & Carvalho, G.R. 2002. Micro- and macrogeographic genetic structure in bryozoans with different larval strategies. Journal of Experimental Marine Biology and Ecology 272, 119Ð130. Pörtner, H.O. 2002. Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology Part A 132, 739Ð761. Proffitt, C.E., Travis, S.E. & Edwards, K.R. 2003. Genotype and elevation influence Spartina alterniflora colonization and growth in a created salt marsh. Ecological Applications 13, 180Ð192. Rakitin, A. & Kramer, D.L. 1996. Effect of a marine reserve on the distribution of coral reef fishes in Barbados. Marine Ecology Progress Series 131, 97Ð113. Raxworthy, C.J., Forstner, M.R. & Nussbaum, R.A. 2002. Chameleon radiation by oceanic dispersal. Nature 415, 784Ð787. Rehm, A.E. & Humm, H.J. 1973. Sphaeroma terebrans: a threat to the mangroves of south-western Florida. Science 182, 173Ð174. Reid, D.G. 2002. The Genus Nodilittorina von Martens, 1897 (Gastropoda: Littorinidae) in the Eastern Pacific Ocean, with a discussion of biogeographic provinces of the rocky-shore fauna. Veliger 45, 85Ð170. Reusch, T.B.H. 2002. Microsatellites reveal high population connectivity in eelgrass (Zostera marina) in two contrasting coastal areas. Limnology and Oceanography 47, 78Ð85. Richards, A.F. 1958. Transpacific distribution of floating pumice from Isla San Benedicto, Mexico. Deep-Sea Research 5, 29Ð35. Romero, L.M., Smith, T.J. & Fourqurean, J.W. 2005. Changes in mass and nutrient content of wood during decomposition in a south Florida mangrove forest. Journal of Ecology 93, 618Ð631. Roughgarden, J., Gaines, S. & Possingham, H. 1988. Recruitment dynamics in complex life-cycles. Science 241, 1460Ð1466. Russo, C.A.M., Sole-Cava, A.M. & Thorpe, J.P. 1994. Population structure and genetic variation in two tropical sea anemones (Cnidaria, Actinidae) with different reproductive strategies. Marine Biology 119, 267Ð276. Scheltema, R.S. 1986. On dispersal and planktonic larvae of benthic invertebrates: an eclectic overview and summary of problems. Bulletin of Marine Science 39, 290Ð322. Scheltema, R.S. 1988. Initial evidence for the transport of teleplanic larvae of benthic invertebrates across the East Pacific barrier. Biological Bulletin (Woods Hole) 174, 145Ð152.

424 7044_C007.fm Page 425 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

Schwaninger, H.R. 1999. Population structure of the widely dispersing marine bryozoan Membranipora membranacea (Cheilostomata): implications for population history, biogeography, and taxonomy. Marine Biology 135, 411Ð423. Segawa, S., Sawada, T. & Yoshida, T. 1964. Studies on the floating seaweeds. IX. The floating seaweeds found on the sea around Japan. Science Bulletin of the Faculty of Agriculture, Kyushu University 21, 111Ð115. Shaffer, J.A., Doty, D.C., Buckley, R.M. & West, J.E. 1995. Crustacean community composition and trophic use of the drift vegetation habitat by juvenile splitnose rockfish Sebastes diploproa. Marine Ecology Progress Series 123, 13Ð21. Shanks, A.L. 1995. Orientated swimming by megalopae of several eastern North Pacific crab species and its potential role in their onshore migration. Journal of Experimental Marine Biology and Ecology 186, 1Ð16. Shanks, A.L. 2002. Internal tides and the biology of continental shelf waters. In The Oceanography and Ecology of the Nearshore and Bays in Chile. Proceeding of the International Symposium on Linkages and Dynamics of Coastal System: Open Coasts and Embayments, Santiago, Chile, 2000, J.C. Castilla & J.L. Largier (eds). Santiago, Chile: Ediciones Universidad Católica de Chile, 3–27. Shanks, A.L., Grantham, B.A. & Carr, M.H. 2003. Propagule dispersal distance and the size and spacing of marine reserves. Ecological Applications 13, S159ÐS169. Si, A., Alexander, C.G. & Bellwood, O. 2000. Habitat partitioning by two wood-boring invertebrates in a mangrove system in tropical Australia. Journal of the Marine Biological Association of the United Kingdom 80, 1131Ð1132. Siegel, D.A., Kinlan, B.P., Gaylord, B. & Gaines, S.D. 2003. Lagrangian descriptions of marine larval dispersion. Marine Ecology Progress Series 260, 83Ð96. Simberloff, D.S. & Wilson, E.O. 1969. Experimental zoogeography of islands: the colonization of empty islands. Ecology 50, 278Ð296. Sköld, M., Wing, S.R. & Mladenov, P.V. 2003. Genetic subdivision of a sea star with high dispersal capability in relation to physical barriers in a fjordic seascape. Marine Ecology Progress Series 250, 163Ð174. Slatkin, M. 1977. Genetic flow and genetic drift in a species at frequent local extinctions. Theoretical Population Biology 12, 253Ð263. Slatkin, M. 1993. Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47, 264Ð279. Slobodov, S.A. & Marfenin, N.N. 2004. Reproduction of the colonial hydroid Obelia geniculata (L., 1758) (Cnidaria, Hydrozoa) in the White Sea. Hydrobiologia 530Ð31, 383Ð388. Smith, S.D.A. 2002. Kelp rafts in the Southern Ocean. Global Ecology and Biogeography 11, 67Ð69. Smith, S.D.A. & Simpson, R.D. 1995. Effects of the Nella Dan oil spill on the fauna of Durvillaea antarctica holdfasts. Marine Ecology Progress Series 121, 73Ð89. Snyder, T.P. & Gooch, J.L. 1973. Genetic differentiation in Littorina saxatilis (Gastropoda). Marine Biology 22, 177Ð182. Sokolova, I.M. & Boulding, E.G. 2004. A neutral DNA marker suggests that parallel physiological adaptations to open shore and salt marsh habitats have evolved more than once within two different species of gastropods. Marine Biology 145, 133Ð147. Solana-Sansores, R. 2001. Floating objects of the Eastern Pacific: types, spatial distribution and temporal changes. Ciencias Marinas 27, 423Ð443. Sotka, E.E., Wares, J.P., Barth, J.A., Grosberg, R.K. & Palumbi, S.R. 2004. Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Molecular Ecology 13, 2143Ð2156. Sponaugle, S., Cowen, R.K., Shanks, A., Morgan, S.G., Leis, J.M., Pineda, J.S., Boehlert, G.W., Kingsford, M.J., Lindeman, K.C., Grimes, C. & Munro, J.L. 2002. Predicting self-recruitment in marine popu- lations: biophysical correlates and mechanisms. Bulletin of Marine Science 70, 341Ð375. Sponer, R. & Roy, M.S. 2002. Phylogeographic analysis of the brooding brittle star Amphipholis squamata (Echinodermata) along the coast of New Zealand reveals high cryptic genetic variation and cryptic dispersal potential. Evolution 56, 1954Ð1967. Stegenga, H. & Mol, I. 1983. Flora van de Nederlandse Zeewieren. Amsterdam, Koninklijke Nederlandse Natuurhistorische Vereniging.

425 7044_C007.fm Page 426 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

Steinke, T.D. & Ward, C.J. 2003. Use of plastic drift cards as indicators of possible dispersal of propagules of the mangrove Avicennia marina by ocean currents. African Journal of Marine Science 25, 169Ð176. Steneck, R.S., Graham, M.H., Bourque, B.J., Corbett, D., Erlandson, J.M., Estes, J.A. & Tegner, M.J. 2002. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation 29, 436Ð459. Stepanjants, S.D., Panteleeva, N.N. & Belousova, N.P. 1993. Obelia longissima (Pallas, 1766) (Hydrozoa, Thecaphora, Campanulariidae) life history. The Barents Sea medusae development in laboratory conditions. In Marine Plankton. Taxonomy, Ecology, Distribution. II., S.D. Stepanjants (ed.). Trudi Zoologicheskogo Instituta, St. Petersburg, 106Ð130. Sterrer, W. 1973. Plate tectonics as a mechanism for dispersal and speciation in interstitial sand fauna. Netherlands Journal of Sea Research 7, 200Ð222. Stevens, L.M., Gregory, M.R. & Foster, B.A. 1996. Fouling bryozoans on pelagic and moored plastics from northern New Zealand. In Bryozoans in Space and Time, D.P. Gordon et al. (eds). Wellington, New Zealand: NIWA, 321Ð340. Stevens, M.I. & Hogg, I.D. 2004. Population genetic structure of New Zealand’s endemic corophiid amphipods: evidence for allopatric speciation. Biological Journal of the Linnean Society 81, 119Ð133. Stieglitz, T. & Ridd, P.V. 2001. Trapping of mangrove propagules due to density-driven secondary circulation in the Normanby River estuary, NE Australia. Marine Ecology Progress Series 211, 131Ð142. Stoddart, J.A. 1984. Genetic differentiation amongst populations of the coral Pocillopora damicornis off Southwestern Australia. Coral Reefs 3, 149Ð156. Stoner, D.S. 1990. Recruitment of a tropical colonial ascidian: relative importance of presettlement vs. postsettlement processes. Ecology 71, 1682Ð1690. Stoner, D.S. 1992. Vertical distribution of a colonial ascidian on a coral-reef: the roles of larval dispersal and life-history variation. American Naturalist 139, 802Ð824. Strathmann, M.F. 1987. Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast. Seattle, WA: University of Washington Press. Strathmann, R.R. 1974. The spread of sibling larvae of sedentary marine invertebrates. American Naturalist 108, 29Ð44. Sunnucks, P. 2000. Efficient genetic markers for population biology. Trends in Ecology & Evolution 15, 199Ð203. Sutherland, F.L. 1965. Dispersal of pumice, supposedly from the 1962 South Sandwich Island eruption, on southern Australian shores. Nature 207, 1332Ð1335. Svavarsson, J., Osore, M.K.W. & Ólafsson, E. 2002. Does the wood-borer Sphaeroma terebrans (Crustacea) shape the distribution of the mangrove Rhizophora mucronata. Ambio 31, 574Ð579. Swearer, S.E., Caselle, J.E., Lea, D.W. & Warner, R.R. 1999. Larval retention and recruitment in an island population of a coral-reef fish. Nature 402, 799Ð802. Swearer, S.E., Shima, J.S., Hellberg, M.E., Thorrold, S.R., Jones, G.P., Robertson, D.R., Morgan, S.G., Selkoe, K.A., Ruiz, G.M. & Warner, R.R. 2002. Evidence of self-recruitment in demersal marine populations. Bulletin of Marine Science 70, 251Ð271. Taylor, M.S. & Hellberg, M.E. 2003. Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299, 107Ð109. Teal, J.M. 1962. Energy flow in the salt marsh ecosystem of Georgia. Ecology 43, 614Ð624. Tegner, M.J., Dayton, P.K., Edwards, P.B. & Riser, K.L. 1995. Sea urchin cavitation of giant kelp (Macrocystis pyrifera C. Agardh) holdfasts and its effects on kelp mortality across a large California forest. Journal of Experimental Marine Biology and Ecology 191, 83Ð99. Thiel, M. 1999. Duration of extended parental care in marine amphipods. Journal of Crustacean Biology 19, 60Ð71. Thiel, M. 2003a. Reproductive biology of Limnoria chilensis: another boring peracarid species with extended parental care. Journal of Natural History 37, 1713Ð1726. Thiel, M. 2003b. Extended parental care in crustaceans — an update. Revista Chilena de Historia Natural 76, 205Ð218. Thiel, M. & Gutow, L. 2005a. The ecology of rafting in the marine environment. I. The floating substrata. Oceanography and Marine Biology: An Annual Review. 42, 181Ð263.

426 7044_C007.fm Page 427 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

Thiel, M. & Gutow, L. 2005b. The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanography and Marine Biology: An Annual Review 43, 279Ð418. Thiel, M., Sampson, S. & Watling, L. 1997. Extended parental care in two endobenthic amphipods. Journal of Natural History 31, 713Ð725. Thiel, M. & Vásquez, J.A. 2000. Are kelp holdfasts islands on the ocean floor? — indication for temporarily closed aggregations of peracarid crustaceans. Hydrobiologia 440, 45Ð54. Thompson, R.C., Crowe, T.P. & Hawkins, S.J. 2002. Rocky intertidal communities: past environmental changes, present status and predictions for the next 25 years. Environmental Conservation 29, 168Ð191. Thornton, I.W.B. 1997. Krakatau: The Destruction and Reassembly of an Island Ecosystem. Cambridge, MA: Harvard University Press. Thorson, G. 1950. Reproductive and larval ecology of marine invertebrates. Biological Reviews of the Cam- bridge Philosophical Society 25, 1Ð45. Todd, C.D., Lambert, W.J. & Thorpe, J.P. 1998. The genetic structure of intertidal populations of two species of nudibranch molluscs with planktotrophic and pelagic lecithotrophic larval stages: are pelagic larvae “for” dispersal? Journal of Experimental Marine Biology and Ecology 228, 1Ð28. Travis, S.E., Proffitt, C.E. & Ritland, K. 2004. Population structure and inbreeding vary with successional stage in created Spartina alterniflora marshes. Ecological Applications 14, 1189Ð1202. Tsikhon-Lukanina, E.A., Reznichenko, O.G. & Nikolaeva, G.G. 2001. Ecology of invertebrates on the oceanic floating substrata in the Northwest Pacific Ocean. Russian Academy of Sciences. Oceanology 41, 525Ð530. Tully, O. & Ó Céidigh, P. 1986. The ecology of Idotea species (Isopoda) and Gammarus locusta (Amphipoda) on surface driftweed in Galway Bay (West of Ireland). Journal of the Marine Biological Association of the United Kingdom 66, 931Ð942. Underwood, A.J. & Chapman, M.G. 1996. Scales of spatial patterns of distribution of intertidal invertebrates. Oecologia 107, 212Ð224. Underwood, A.J. & Fairweather, P.G. 1989. Supply-side ecology and benthic marine assemblages. Trends in Ecology & Evolution 4, 16Ð20. Vallentin, R. 1895. Some remarks on the dispersal of marine animals by means of seaweeds. The Annals and Magazine of Natural History, Zoology, Botany and Geology 16, 418Ð423. Vandendriessche, S., Vincx, M. & Degraer, S. 2006. Floating seaweed in the neustonic environment: A case study from Belgian coastal waters. Journal of Sea Research 55, 103Ð112. Vásquez, J.A. 1993. Effects on the animal community of dislodgment of holdfasts of Macrocystis pyrifera. Pacific Science 47, 180Ð184. Vellend, M. 2003. Island biogeography of genes and species. American Naturalist 162, 358Ð365. Vetter, E.W. & Dayton, P.K. 1999. Organic enrichment by macrophyte detritus, and abundance patterns of megafaunal populations in submarine canyons. Marine Ecology Progress Series 186, 137Ð148. Vianna, P., Schama, R. & Russo, C.A.M. 2003. Genetic divergence and isolation by distance in the West Atlantic sea anemone Actinia bermudensis (McMurrich, 1889). Journal of Experimental Marine Biology and Ecology 297, 19Ð30. Virgilio, M. & Abbiati, M. 2004. Habitat discontinuity and genetic structure in populations of the estuarine species Hediste diversicolor (Polychaeta: Nereididae). Estuarine Coastal and Shelf Science 61, 361Ð367. Wares, J.P. & Cunningham, C.W. 2001. Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55, 2455Ð2469. Wares, J.P., Gaines, S.D. & Cunningham, C.W. 2001. A comparative study of asymmetric migration events across a marine biogeographic boundary. Evolution 55, 295Ð306. Wares, J.P., Hughes, A.R. & Grosberg, R.K. 2005. Species introductions and invasions: insights into the mechanisms that drive evolutionary change. In Species Invasions: Insights into Ecology, Evolution, and Biogeography, D.F. Sax et al. (eds). Sunderland, MA: Sinauer Associates Inc., 229Ð257. Waters, J.M., King, T.M., O’Loughlin, P.M. & Spencer, H.G. 2005. Phylogeographical disjunction in abundant high-dispersal littoral gastropods. Molecular Ecology 14, 2789Ð2802. Waters, J.M. & Roy, M.S. 2003. Global phylogeography of the fissiparous sea-star genus Coscinasterias. Marine Biology 142, 185Ð191.

427 7044_C007.fm Page 428 Tuesday, April 25, 2006 1:08 PM

MARTIN THIEL & PILAR A. HAYE

Waters, J.M. & Roy, M.S. 2004a. Out of Africa: the slow train to Australasia. Systematic Biology 53, 18Ð24. Waters, J.M. & Roy, M.S. 2004b. Phylogeography of a high-dispersal New Zealand sea-star: does upwelling block gene-flow? Molecular Ecology 13, 2797Ð2806. Watts, P.C., Thorpe, J.P. & Taylor, P.D. 1998. Natural and anthropogenic dispersal mechanisms in the marine environment: a study using cheilostome Bryozoa. Philosophical Transactions of the Royal Society Series B Biological Sciences 353, 453Ð464. Waycott, M. & Barnes, P.A.G. 2001. AFLP diversity within and between populations of the Caribbean seagrass Thalassia testudinum (Hydrocharitaceae). Marine Biology 139, 1021Ð1028. Weber, H.C. 2005. Probabilistic prediction of tropical cyclones. Part I: Position. Monthly Weather Review 133, 1840Ð1852. Wehrtmann, I.S. & Dittel, A.I. 1990. Utilization of floating mangrove leaves as a transport mechanism of estuarine organisms, with emphasis on decapod Crustacea. Marine Ecology Progress Series 60, 67Ð73. Whalan, S., Johnson, M.S., Harvey, E. & Battershill, C. 2005. Mode of reproduction, recruitment, and genetic subdivision in the brooding sponge Haliclona sp. Marine Biology 146, 425Ð433. Wheeler, W.M. 1916. Ants carried in a floating log from the Brazilian coast to San Sebastian Island. Psyche 23, 180Ð183.

Whitlock, M.C. & McCauley, D.E. 1999. Indirect measures of gene flow and migration: FST not equal 1/(4Nm+1). Heredity 82, 117Ð125. Wildish, D.J. 1970. Some factors affecting the distribution of Orchestia Leach in estuaries. Journal of Experimental Marine Biology and Ecology 5, 276Ð284. Wilhelmsen, U. 1999. Rapid colonization of new habitats in the Wadden Sea by the ovoviviparous Littorina saxatilis (Olivi). Helgoländer Meeresuntersuchungen 52, 325Ð335. Wilke, T. & Davis, G.M. 2000. Intraspecific mitochondrial sequence diversity in Hydrobia ulvae and Hydrobia ventrosa (Hydrobiidae: Rissooidea: Gastropoda): do their different life histories affect biogeographic patterns and gene flow? Biological Journal of the Linnean Society 70, 89Ð105. Williams, S.T. & Benzie, J.A.H. 1996. Genetic uniformity of widely separated populations of the coral reef starfish Linckia laevigata from the East Indian and West Pacific Oceans, revealed by allozyme electrophoresis. Marine Biology 126, 99Ð107. Williams, S.T. & Benzie, J.A.H. 1998. Evidence of a biogeographic break between populations of a high dispersal starfish: congruent regions within the Indo-West Pacific defined by color morphs, mtDNA, and allozyme data. Evolution 52, 87Ð99. Williams, S.T. & Reid, D.G. 2004. Speciation and diversity on tropical rocky shores: a global phylogeny of snails of the genus Echinolittorina. Evolution 58, 2227Ð2251. Williams, S.T., Reid, D.G. & Littlewood, D.T.J. 2003. A molecular phylogeny of the Littorininae (Gastropoda: Littorinidae): unequal evolutionary rates, morphological parallelism, and biogeography of the Southern Ocean. Molecular Phylogenetics and Evolution 28, 60Ð86. Wilson, A.B., Boates, J.S. & Snyder, M. 1997. Genetic isolation of populations of the gammaridean amphipod, Corophium volutator, in the Bay of Fundy, Canada. Molecular Ecology 6, 917Ð923. Winston, J.E. 1982. Drift plastic — an expanding niche for a marine invertebrate. Marine Pollution Bulletin 13, 348Ð351. Winston, J.E., Gregory, M.R. & Stevens, L.M. 1997. Encrusters, epibionts, and other biota associated with pelagic plastics: a review of biogeographical, environmental, and conservation issues. In Marine Debris: Sources, Impacts, and Solution, J.M. Coe & D.B. Rogers (eds). New York: Springer, 81Ð97. Witter, R.C., Kelsey, H.M. & Hemphill-Haley, E. 2001. Pacific storms, El Niño and tsunamis: competing mechanisms for sand deposition in a coastal marsh, Euchre Creek, Oregon. Journal of Coastal Research 17, 563Ð583. Wolff, T. 1979. Macrofaunal utilization of plant remains in the deep sea. Sarsia 64, 117Ð136. Wonham, M.J. & Carlton, J.T. 2005. Trends in marine biological invasions at local and regional scales: the Northeast Pacific Ocean as a model system. Biological Invasions 7, 369Ð392. Worcester, S.E. 1994. Adult rafting versus larval swimming — dispersal and recruitment of a botryllid ascidian on eelgrass. Marine Biology 121, 309Ð317.

428 7044_C007.fm Page 429 Tuesday, April 25, 2006 1:08 PM

RAFTING AND MARINE BIODIVERSITY

Wörheide, G., Hooper, J.N.A. & Degnan, B.M. 2002. Phylogeography of western Pacific Leucetta ‘chagosen- sis’ (Porifera: Calcarea) from ribosomal DNA sequences: implications for population history and conservation of the Great Barrier Reef World Heritage Area (Australia). Molecular Ecology 11, 1753Ð1768. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16, 97Ð159. Wright, S. 1940. Breeding structure of populations in relation to speciation. American Naturalist 74, 232Ð248. Wright, S. 1943. Isolation by distance under diverse systems of mating. Genetics 28, 114Ð138. Wright, S. 1951. The genetical structure of populations. Annals of Eugenics 15, 323Ð353. Wright, S. 1965. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19, 395Ð420. Wright, S. 1969. Evolution and the Genetics of Populations, Vol. 2: The Theory of Gene Frequencies. Chicago, IL: University of Chicago Press. Yeung, C. & Lee, T.N. 2002. Larval transport and retention of the spiny lobster, Panulirus argus, in the coastal zone of the Florida Keys, USA. Fisheries Oceanography 11, 286Ð309. Yoder, A.D., Burns, M.M., Zehr, S., Delefosse, T., Veron, G., Goodman, S.M. & Flynn, J.J. 2003. Single origin of Malagasy Carnivora from an African ancestor. Nature 421, 734Ð737. Young, C.M. 1986. Direct observations of field swimming behavior in larvae of the colonial ascidian Ectein- ascidia turbinata. Bulletin of Marine Science 39, 279Ð289. Young, C.M. 1995. Behavior and locomotion during the dispersal phase of larval life. In Ecology of Marine Invertebrate Larvae, L.R. McEdward (ed.). Boca Raton, FL: CRC Press, 249Ð277. Zacherl, D.C. 2005. Spatial and temporal variation in statolith and protoconch trace elements as natural tags to track larval dispersal. Marine Ecology Progress Series 290, 145Ð163. Zane, L., Ostellari, L., Maccatrozzo, L., Bargelloni, L., Battaglia, B. & Patarnello, T. 1998. Molecular evidence for genetic subdivision of Antarctic krill (Euphausia superba Dana) populations. Proceedings of the Royal Society Series B Biological Sciences 265, 2387Ð2391. Zarate-Villafranco, A. & Ortega-García, S. 2000. Spatial and seasonal distribution of the tuna catch on floating objects in the eastern Pacific Ocean during 1992–1993. Marine and Freshwater Behaviour and Physiology 34, 53Ð72. Zobell, C.E. 1971. Drift seaweeds on San Diego county beaches. Nova Hedwigia (Suppl.) 32, 269Ð314.

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POTENTIAL EFFECTS OF CLIMATE CHANGE ON MARINE MAMMALS

J.A. LEARMONTH1, C.D. MACLEOD1, M.B. SANTOS1,2, G.J. PIERCE1, H.Q.P. CRICK3 & R.A. ROBINSON3 1School of Biological Sciences [Zoology], University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, U.K. E-mail: [email protected] 2Instituto Español de Oceanografía, Centro Costero de Vigo, Cabo Estay, Canido, 36200 Vigo, Spain 3British Trust for Ornithology, The Nunnery, Thetford, IP24 2PU, U.K.

Abstract Predicted impacts of climate change on the marine environment include an increase in temperature, a rise in sea levels and a decrease in sea-ice cover. These impacts will occur at local, regional and larger scales. The potential impacts of climate change on marine mammals can be direct, such as the effects of reduced sea ice and rising sea levels on seal haul-out sites, or species tracking a specific range of water temperatures in which they can physically survive. Indirect effects of climate change include changes in prey availability affecting distribution, abundance and migra- tion patterns, community structure, susceptibility to disease and contaminants. Ultimately, these will impact on the reproductive success and survival of marine mammals and, hence, have conse- quences for populations. Marine mammal species, which have restricted geographical distributions with little or no opportunity for range expansion in response to climate change, may be particularly vulnerable to the effects of climate change. The potential effects of climate change on marine mammals have a number of implications for their conservation and highlight several areas requiring further research.

Introduction The Earth’s climate is changing (IPCC 2001a). The global average land and sea surface temperature has increased over the twentieth century and precipitation has increased over the same period, particularly over mid- and high-latitudes. These changes have had secondary impacts. For example, as temperatures have increased the extent of ice cover has decreased and global sea level has risen. Such changes are evident from the global network of climate instruments and, over a longer timescale, from the use of historical proxies such as tree rings or ice cores. The causes of such changes are open to debate, but most of the observed warming over the last 50 yr has probably

been due to increased CO2 emissions, and these increases are likely to continue (e.g., Hulme et al. 2002, EEA 2004). Global climate change will affect the physical, biological and biogeochemical characteristics of the oceans and coasts. Known or predicted large-scale and regional impacts of climate change on the marine environment include an increase in temperature, a rise in sea levels, and changes in

ocean circulation, sea-ice cover, salinity, CO2 concentrations, pH, rainfall patterns, storm frequency, wind speed, wave conditions and climate patterns (FRS 1998, Hansen et al. 2001, IPCC 2001a, Sear et al. 2001, Hulme et al. 2002, FRS 2003, ICES 2004).

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Climate change is likely to present a major challenge to the world’s wildlife, and to impact overall levels of biodiversity. Changing climate has already had a number of impacts on wildlife, across a range of taxa, and these impacts are set to increase unless suitable mitigation measures are taken (Walther et al. 2002, Parmesan & Yohe 2003, Root et al. 2003, EEA 2004, Parmesan & Galbraith 2004). The effect of climate change on the marine environment has the potential to have, and in some cases has already had, a considerable impact on marine ecosystems and species. These effects could include changes in abundance, distribution, timing and range of migration, community structure, the presence and species composition of competitors and/or predators, prey availability and distri- bution, timing of breeding, reproductive success and, ultimately, survival (IWC 1997, Tynan & DeMaster 1997, Harwood 2001, Würsig et al. 2002). While some species may increase in abundance or range, climate change will increase the risk of extinction of other more vulnerable species. The geographical extent of the damage or loss, and the number of systems affected, will increase with the magnitude and rate of climate change (IPCC 2001a). Uncertainties about the nature and degree of future climate change make it impossible to know exactly how weather, ocean circulation and biological productivity will be affected (for example, Weaver & Zwiers 2000). Effects on the marine environment are especially difficult to predict because of the complex interactions between ocean processes and climate and will vary greatly between areas. Therefore, predictions of the effects on species and populations are highly speculative (Würsig et al. 2002). The impacts of climate change will reflect the timing and geographic scale of the changes, as well as on the longevity, generation time and geographic distribution of the species (Würsig et al. 2002). For example, large but ‘slow’ (in the order of decades or centuries) shifts in the climate have occurred throughout the Earth’s history, and these have driven the evolution of adaptive character- istics, within-species variations, population discreteness and extinctions (Würsig et al. 2002). There have been several recent papers linking the effects of climate change to marine mammals (e.g., Ferguson et al. 2005, MacLeod et al. 2005). The present paper reviews current information on the observed and predicted changes in climate and their potential impacts, direct and indirect, on marine mammals. Examples of observed effects are given for mysticetes (baleen whales), odonto- cetes (toothed whales, dolphins and porpoises), pinnipeds (seals, sea lions and walruses), sirenians (manatee and dugong) and the polar bear (Ursus maritimus), based on published accounts and reports. Many of the indirect effects of climate change on marine mammals will be through changes in prey availability; therefore potential effects of climate change on prey species, such as fish, cephalopods and plankton are also reviewed.

Range of marine mammals Marine mammals are found in just about all ocean habitats, as well as several rivers and inland seas. In the open ocean, marine mammals may be thought of as ‘surface dwellers’, that spend most of their lives within about 200 m of the surface, ‘deep divers’, that routinely dive to depths below 500 m for short periods of time, or ‘deep dwellers’ that spend much of their time at depths below 500 m. Several species are semipelagic; occurring in areas between shallow and deep water, often at the edge of the continental shelf or some other underwater feature. Many marine mammals are coastal, with baleen whales, odontocetes, pinnipeds and sirenians all having coastal representatives (Würsig 2002). A species’ distribution is affected by a combination of demographic, evolutionary, ecological, habitat-related and anthropogenic factors although, in general, prey availability is likely to be particularly critical (Forcada 2002). Species habitat preferences are generally thought to be related to the distribution of preferred prey, which in turn are often determined by physical oceanographic features. Therefore, the habitat preferences of marine mammals are often defined by physical and chemical characteristics of the water, which define water masses and current boundaries where

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prey accumulates. For example some species, such as Heaviside’s (Cephalorhynchus heavisidii), Commerson’s (C. commersonii) and Peale’s (Lagenorhynchus australis) dolphins, are associated with cold-water currents, and blue whales (Balaenoptera musculus) are often found in areas of cool upwelling waters (Forcada 2002, LeDuc 2002). Therefore, although marine mammals are observed widely across the world’s oceans, distribution within the overall range is often patchy, with some areas being used more frequently than others. These ‘preferred’ areas or ‘critical habitats’ are probably particularly important for survival and reproduction, and it is changes to these areas that are most likely to affect the distribution and abundance of marine mammals (Harwood 2001). While the fine-scale distribution of marine mammal species may be related to oceanographic features and conditions through their effects on prey distribution, the regional or global ranges of marine mammal species are often related to water temperature (Table 1). For example, bowhead whales (Balaena mysticetus) and narwhals (Monodon monoceros) are found only in Arctic waters, Atlantic white-beaked dolphins (Lagenorhynchus albirostris) are only found in cold temperate waters, and species such as spinner (Stenella longirostris) and pantropical spotted (S. attenuata) dolphins are restricted to tropical waters (Mann et al. 2000). A species’ range may be limited in some cases because it is not adapted for living in certain environments. For example, tropical delphinids may not range into higher latitudes due to limitations on their abilities to thermoregulate in colder water or find food in different habitats. Competition, either from closely related species or from ecologically similar species, may also exclude a species from a particular region in which it could otherwise survive (i.e., competitive exclusion) (Forcada 2002). However, whether the relationship between the range of many marine mammal species and water temperature is direct, with species only being able to survive within specific temperature ranges, or indirect with tem- perature affecting competitive abilities of ecologically similar species, is unknown in most cases. Within a species range, there may be regular changes in areas of occurrence as their biological and ecological requirements change (Forcada 2002). Of these changes, the most common are seasonal migrations. Migration can be described as “the seasonal movement between two geo- graphic locations that is related to the reproductive cycle, changes in temperature, and prey avail- ability” (Forcada 2002) or “the persistent movement between two destinations” (Cockeron & Connor 1999). The Bonn Convention on the Conservation of Migratory Species of Wild Animals (1979) (CMS) is an important instrument in the management of migratory species. It defines a migratory species as “the entire population or any geographically separate part of the population of any species or lower taxon of wild animals, a significant proportion of whose members cyclically and predictably cross one or more national jurisdictional boundaries”. The basic driving forces for migration are ecological and biogeographic factors, like seasonality, spatiotemporal distributions of resources, habitats, predation and competition (Alerstam et al. 2003). The triggers for migration may relate to changes in day length but, as the timing of migrations can vary from year to year, prey abundance may also be an important factor, and temperature and sea- ice formation can also be influential (Stern 2002). Most baleen whales (mysticetes), such as blue, grey (Eschrichtius robustus), fin (Balaenoptera physalus), sei (B. borealis), northern and southern right whales (Balaena glacialis and B. australis) and humpback whales (Megaptera novaeangliae), undertake long seasonal migrations between tropical calving grounds in winter and high latitude feeding grounds in summer. For example, grey whales are highly migratory with an annual migration covering up to 15,000Ð20,000 km between summer feeding grounds in Arctic or subarctic waters and winter breeding grounds in temperate or subtropical southern waters (Jones & Swartz 2002). Bowhead whales also migrate but their longitudinal movements are equal to or greater than their latitudinal movements and they never leave Arctic waters. The migration or seasonal movements of Bryde’s (Balaenoptera edeni) and minke whales (B. acutorostrata) are often less well defined and less predictable than those of other migratory baleen whales (Forcada 2002).

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Table 1 Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species

Potential effects Family and Species range IUCN of climate change species name Common name (breeding site for pinnipeds) status on species range Mysticeti Baleen Whales Balaenidae Balaena mysticetus Bowhead whale N Hemisphere: Arctic waters, LR:cd ↓ circumpolar Balaena glacialis Northern right N Atlantic & Pacific: subpolar to EN (D) ?↓ whale tropical Balaena australis Southern right S Hemisphere: Antarctic to LR:cd ?↓ whale temperate

Neobalaenidae Caperea marginata Pygmy right whale S Hemisphere: circumpolar, ?↓ cold temperate

Eschrichtiidae Eschrichtius robustus Grey whale N Pacific: warm temperate to LR:cd ? arctic

Balaenopteridae Megaptera novaeangliae Humpback whale Worldwide: cold VA (A) ? temperate/polar to tropical Balaenoptera acutorostrata Minke whale1 Worldwide: polar to tropical LR:nt ? Balaenoptera bonaerensis Antarctic minke S Hemisphere: polar to tropical LR:cd ? whale1 Balaenoptera edeni/brydei Bryde’s whale Worldwide: warm temperate to DD tropical Balaenoptera borealis Sei whale Worldwide: cold temperate to EN (A) ? tropical Balaenoptera physalus Fin whale Worldwide: polar to tropical EN (A) ? Balaenoptera musculus Blue whale Worldwide: polar to tropical EN (A) ?

Odontoceti Toothed Whales Physeteridae Physeter macrocephalus Sperm whale Worldwide: polar to tropical VU (A) ?

Kogiidae Kogia breviceps Pygmy sperm Worldwide: warm temperate to DD ↑ whale tropical Kogia sima Dwarf sperm whale Worldwide: warm temperate to ↑ tropical

Ziphiidae Ziphius cavirostris Cuvier’s beaked Worldwide: cold temperate to DD ? whale tropical Berardius arnuxii Arnoux’s beaked S Hemisphere: circumpolar, LR:cd ? whale polar to subtropical Berardius bairdii Baird’s beaked N Pacific: polar to subtropical LR:cd ? whale

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species

Potential effects Family and Species range IUCN of climate change species name Common name (breeding site for pinnipeds) status on species range Tasmacetus shepherdi Shepherd’s beaked S Hemisphere: warm temperate DD ? whale to subpolar Indopacetus pacificus Longman’s beaked Indian Ocean and Pacific: DD ? whale tropical waters Hyperoodon ampullatus Northern N Atlantic: arctic to cold LR:cd ↓ bottlenose whale temperate waters Hyperoodon planiforms Southern S Hemisphere: circumpolar, LR:cd ? bottlenose whale Antarctic to temperate Mesoplodon hectori Hector’s beaked S Hemisphere: cold temperate to DD ? whale subtropical Mesoplodon mirus True’s beaked Worldwide: warm temperate to DD ?↑ whale subtropical Mesoplodon europaeus Gervais’ beaked Atlantic: warm temperate to DD ?↑ whale tropical Mesoplodon bidens Sowerby’s beaked N Atlantic: subpolar to warm DD ? whale temperate Mesoplodon grayi Gray’s beaked S Hemisphere: cold to warm DD ? whale temperate Mesoplodon peruvianus Pygmy beaked SE and NE Pacific: cold DD ? whale temperate to tropical Mesoplodon bowdoini Andrew’s beaked S Hemisphere: cold temperate to DD ? whale subtropical Mesoplodon carlhubbsi Hubbs’ beaked N Pacific: cold temperate to DD ? whale subtropical Mesoplodon ginkgodens Ginko-toothed N Pacific and Indian Ocean: DD ? beaked whale temperate to tropical Mesoplodon stejnegeri Stejneger’s beaked N Pacific: warm temperate to DD ? whale subpolar Mesoplodon layardii Strap-toothed S Hemisphere: polar to DD ? beaked whale subtropical Mesoplodon densirostris Blainville’s beaked Worldwide: warm temperate to DD ? whale tropical Mesoplodon traversii Spade-toothed Unknown possibly S Pacific: ?↑ whale cold temperate to subtropical Mesoplodon perrini Perrin’s beaked Unknown possibly NE Pacific: ? whale warm temperate to subtropical

Platanistidae Platanista gangetica Ganges river India, Nepal, Bhutan and EN (A) ↓ dolphin Bangladesh: freshwater only

Iniidae Inia geoffrensis Boto Peru, Ecuador, Brazil, Bolivia, VU (A) ↓ Venézuela, Colombia: freshwater only

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species

Potential effects Family and Species range IUCN of climate change species name Common name (breeding site for pinnipeds) status on species range Lipotidae Lipotes vexillifer Baiji China: freshwater only CR ↓ (ACD)

Pontoporiidae Pontoporia blainvillei Franciscana Brazil to Argentina: coastal DD ↓ waters from Doce River

Monodontidae Delphinapterus leucas Beluga or white Circumpolar in arctic seas: arctic VU (A) ↓ whale to cold temperate Monodon monoceros Narwhal Arctic Ocean DD ↓

Delphinidae Cephalorhynchus Commerson’s S America, Falkland and DD ↓ commersonii dolphin Kerguelen islands: coastal, subpolar to cold temperate Cephalorhynchus eutropia Chilean dolphin S South America: coastal, DD ? subpolar to warm temperate Cephalorhynchus heavisidii Heaviside’s SW Africa: cold to warm DD ? dolphin temperate Cephalorhynchus hectori Hector’s dolphin New Zealand: coastal waters, EN ↓ cold to warm temperate (AC) Steno bredanensis Rough-toothed Worldwide: warm temperate to DD ? dolphin tropical Sousa teuszii Atlantic hump- SE Atlantic: coastal and river DD ? backed dolphin mouths, subtropical to tropical Sousa plumbea Indian hump- Indian Ocean: coastal, ? backed dolphin subtropical to tropical Sousa chinensis Indo-pacific hump- Indian Ocean: coastal and rivers, DD ? backed dolphin tropical Sotalia fluviatilis Tucuxi SW Atlantic: coastal, estuaries DD ↓ and rivers, tropical Tursiops aduncus Bottlenose dolphin Indian and Pacific Ocean: DD ? coastal, tropical Tursiops truncatus Bottlenose dolphin Worldwide: cold temperate to DD ↑ tropical Stenella attenuata Pantropical spotted Worldwide: tropical LR:cd ?↑ dolphin Stenella frontalis Atlantic spotted Atlantic Ocean: subtropical to DD ?↑ dolphin tropical Stenella longirostris Spinner dolphin Worldwide: tropical LR:cd ?↑ Stenella clymene Clymene dolphin Atlantic Ocean: tropical DD ? Stenella coeruleoalba Striped dolphin Worldwide: cold temperate to LR:cd ?↑ tropical

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species

Potential effects Family and Species range IUCN of climate change species name Common name (breeding site for pinnipeds) status on species range Delphinus delphis Short-beaked Worldwide: temperate and ?↑ common dolphin2 tropical Delphinus capensis Long-beaked Worldwide: subtropical ?↑ common dolphin2 Delphinus tropicalis Arabian common Arabian Sea: coastal waters, ? dolphin2 tropical Lagenodelphis hosei Fraser’s dolphin Worldwide: warm temperate to DD ?↑ tropical Lagenorhynchus albirostris White-beaked N Atlantic: cold temperate dolphin Lagenorhynchus acutus Atlantic white- N Atlantic: subpolar to warm ?↓ sided dolphin temperate Lagenorhynchus Pacific white-sided N Pacific: cold temperate to ?↓ obliquidens dolphin subtropical Lagenorhynchus obscurus Dusky dolphin S Hemisphere: cold to warm DD ?↓ temperate Lagenorhynchus australis Peale’s dolphin S America: subpolar to warm DD ? temperate Lagenorhynchus cruiger Hourglass dolphin S Hemisphere: polar to warm ?↓ temperate Lissodelphis borealis N. right whale N Pacific: subpolar to ? dolphin subtropical Lissodelphis peronii S. right whale S Hemisphere: polar to DD ? dolphin subtropical Grampus griseus Risso’s dolphin Worldwide: cold temperate to DD ? tropical Peponocephala electra Melon-headed Worldwide: tropical ?↑ whale Feresa attenuata Pygmy killer whale Worldwide: tropical to warm ?↑ temperate Pseudorca crassidens False killer whale Worldwide: warm temperate to ?↑ tropical Orcinus orca Killer whale, orca Worldwide: polar to tropical LR:cd ? Globicephala melas Long-finned pilot Worldwide (ex N Pacific): polar ? whale to warm temperate Globicephala Short-finned pilot Worldwide: tropical to LR:cd ?↑ macrorhynchus whale subtropical Orcaella brevirostris Irrawaddy dolphin SE Asia, N Australia and Papua DD ↓ New Guinea: tropical coastal waters and estuaries

Phocoenidae Neophocaena phocaenoides Finless porpoise Indo-Pacific: warm temperate to DD ? tropical Phocoena phocoena Harbour porpoise N Pacific and N Atlantic: VU (A) ?↓ subpolar to cold temperate

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species

Potential effects Family and Species range IUCN of climate change species name Common name (breeding site for pinnipeds) status on species range Phocoena sinus Vaquita Gulf of California: subtropical CR (C) ↓ Phocoena spinipinnis Burmeister S America: coastal cold DD ? porpoise temperate to subtropical Phocoena dioptrica Spectacled S Hemisphere: polar to cold DD ?↓ porpoise temperate Phocoenoides dalli Dall’s porpoise N Pacific: subpolar to temperate LR:cd ?

Otariidae Artocephalus pusillus Cape fur seal S Africa and S Australia: warm ? temperate (land) Artocephalus gazelle Antarctic fur seal S Hemisphere (excluding SE ?↓ Pacific): polar to subpolar Artocephalus tropicalis Subantarctic fur S Hemisphere (excluding SE ? seal Pacific): high temperate Artocephalus townsendi Guadalupe fur sea NE Pacific: warm temperate to VU (D) ? tropical (land) Artocephalus philippii Juan Fernández fur- West coast of South America, VU (D) ? seal Chile: temperate (land) Artocephalus forsteri New Zealand fur S Australia and New Zealand: ? seal temperate (land) Artocephalus australis South American fur S America and Falklands: ? seal subpolar to temperate (land) Artocephalus Galápagos fur seal Galápagos Islands: equatorial VU (A) ?↓ galapagoensis (land) Callorhinus ursinus Northern fur seal N Pacific and Bering Sea: VU (A) ? subpolar to temperate (land) Zalophus californianus California sea lion NE Pacific: warm temperate to ? tropical (land) Zalophus wollebaeki Galápagos sea lion Galápagos Islands: equatorial VU (A) ?↓ (land) Eumetopias jubatus Steller sea lion N Pacific: subpolar to cold EN (A) ?↓ temperate (land) Neophoca cinera Australian sea lion SE Indian Ocean, S and SW ? Australia: temperate (land) Phocarctos hookeri New Zealand sea SW Pacific, NZ: subpolar to cold VU (D) ? lion temperate (land) Otaria flavescens South American S America and Falklands: polar ? sea lion to subtropical (land)

Odobenidae Odobenus rosmarus Walrus Arctic Ocean and adjoining seas ?↓

Phocidae Ergnathus barbatus Bearded seal Arctic (pack ice) ?↓ Phoca vitulina Harbour seal N Hemisphere: subpolar to ? warm temperate (land)

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species

Potential effects Family and Species range IUCN of climate change species name Common name (breeding site for pinnipeds) status on species range Phoca largha Spotted seal N Pacific, Chukchi Sea: polar ?↓ (pack ice) Pusa hispida Ringed seal Arctic regions, Baltic Sea: (fast ?↓ ice) Pusa caspica Caspian seal Caspian Sea: polar to subpolar VU (B) ?↓ (fast ice) Pusa sibirica Baikal seal Lake Baikal, Siberia: polar to LR:nt ?↓ subpolar (fast ice) Halichoerus grypus Grey seal N Atlantic: subpolar to cold ?↓ temperate (land, ice) Histriophoca fasciata Ribbon seal N Pacific: polar (pack ice) ?↓ Pagophilus groenlandicus Harp seal N Atlantic: polar to cold ?↓ temperate (pack ice) Cystophora cristata Hooded seal N Atlantic: polar to cold ?↓ temperate (pack ice) Monachus monachus Mediterranean Med. Sea, Black Sea, NW CR (C) ?↓ monk seal African coast: subtropical (land) Monachus schauinslandi Hawaiian monk Hawaiian Islands: tropical (land) EN (C) ? seal Mirounga leonina Southern elephant Subantarctic, Antarctic, ?↓ seal southern S. America (land) Mirounga angustirostris Northern elephant N Pacific: subpolar to ?↓ seal subtropical (land) Leptonychotes weddellii Weddell seal Antarctic (fast ice) ?↓ Ommatophoca rossii Ross seal Antarctic (fast ice) ?↓ Lobodon carcinophaga Crabeater seal Antarctic (pack ice) ?↓ Hydrurga leptonyx Leopard seal Antarctic (pack ice) ?

Trichechidae Trichechus manatus Caribbean manatee Florida, Caribbean (marine and VU (A) ?↑ freshwater) T. m. latirostris Florida manatee Florida peninsula, occasionally as far south as Bahamas T. m. manatus Antillean manatee Mainland coast from Mexico to Venezuela, and Brazil including the Greater and Lesser Antilles Trichechus senegalensis African manatee West Africa (marine and VU (A) ? freshwater) Trichechus inunguis Amazon manatee Amazon river (marine and VU (A) ? freshwater)

Dugongidae Dugong dugon Dugong Indian and western Pacific VU (A) ? oceans (marine)

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Table 1 (continued) Species range (breeding site for pinnipeds), IUCN status and potential effects of climate change on the range of cetaceans, pinnipeds, sirenians and other marine mammal species

Potential effects Family and Species range IUCN of climate change species name Common name (breeding site for pinnipeds) status on species range

Ursidae Ursus maritimus Polar bear Arctic LR:cd ?↓

Mustelidae Enhydra lutris Sea otter Canada, U.S., Mexico, Japan, EN (A) ? Russian Federation (terrestrial, marine) Lontra felina Marine otter Argentina, Chile, Peru EN (A) ? (terrestrial, freshwater, marine) Lutra lutra Common otter Worldwide (terrestrial, NT ? freshwater, marine)

Notes: ↑ indicates a possible increase in range, ↓ indicates a possible decrease in range and ? indicates effects on range are unknown.

IUCN status: (CR = critically endangered; EN = endangered; VU = vulnerable; A = declining population, B = small distribution and decline or fluctuation, C = small population size and decline, D = very small or restricted); NT = near threatened; LR:cd = low risk, conservation dependent; LR:nt = low risk, near threatened; DD = data deficient.

1. Minke whale: several authors refer to two species of minke whale — the Antarctic minke whale (B. bonaerensis) and the dwarf minke whale (B. acutorostrata) — however, in the context of this review both are referred to as minke whales. 2. Common dolphins: three species of common dolphins have been identified — the short-beaked common dolphin (D. delphis), the long-beaked common dolphin (D. capensis) and the Arabian common dolphin (D. tropicalis) — however, in the context of this review all are referred to as common dolphins due to the overlap in distribution of D. delphis and D. capensis.

Source: Based on Ridgeway & Harrison 1985, Rice 1998, Mann et al. 2000, Perrin et al. 2002, Reid et al. 2003b, IUCN 2004, Kaschner 2004.

Baleen whale migrations have generally been regarded as a response to the need to feed in colder waters and reproduce in warmer waters. Explanations for such long-range migrations have included (i) direct benefits to the calf, for example, increase in survival in calm, warm waters, (ii) relict from times when continents were closer together, (iii) the possible ability of some species to supplement their food supply with plankton encountered on migration or on calving grounds, (iv) reducing the risk of killer whale predation of new born calves in low latitudes and (v) species with a large body size (and lower mass specific metabolic rates) are able to make the long migrations that allow them to take advantage of warmer, and predator-free, waters (Bannister 2002, Stern 2002). The movements of odontocetes (toothed whales) vary more in scale depending on geographic range and species. For example, some sperm whales (Physeter macrocephalus) undertake long seasonal migrations similar to those of baleen whales, between high-latitude feeding grounds and warmer water breeding areas, although this is probably quite unusual in odontocetes (Whitehead 2002). Large seasonal movements often occur in oceanic odontocetes, for example, Stenella species and common dolphins (Delphinus delphis). Coastal bottlenose dolphins (Tursiops truncatus) exhibit

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a full spectrum of movements, including seasonal migrations, year-round home ranges, periodic residency and occasional long-range movements (Wells & Scott 2002). Bottlenose dolphins living at the high-latitude or cold-water extremes of the species’ range may migrate seasonally, for example, along the Atlantic coast of the U.S. (Wells & Scott 2002). North-south and inshore- offshore seasonal movements have been observed in several odontocete species, including harbour porpoise (Phocoena phocoena) (Northridge et al. 1995, Anderson et al. 2001, Bj¿rge & Tolley 2002). Dispersal and migration is common in several pinniped species. Sea lion species, such as the California sea lion (Zalophus californianus), tend to live in warmer areas where food resources are more constant and there is less dispersal from breeding sites. However, Phocidae species (true seals) that live in higher latitudes, which are more dependent on ice cover and/or seasonally changing prey, tend to have a wider dispersal. For example, northern and southern elephant seals (Mirounga angustirostris and M. leonina) spend between 8 and 10 months at sea each year, with long-distance migrations from breeding and moulting sites to feeding areas (Forcada 2002). Polar bears undertake seasonal migrations, and these long-range movements are generally related to ice cover and seal distribution (Forcada 2002). Sirenians, such as manatees (Trichechus manatus), also embark on seasonal movements. For example in Florida, where water temperature is a major determinant factor (Reynolds & Powell 2002). Migration and the range of marine mammal species have evolved within constantly changing environmental conditions. Species have adapted to historic changes in climate. However, many of these changes, such as the retreat of the polar front in the Pleistocene, occurred at a rate that allowed species to adapt. Although marine mammals are capable of adapting to environmental changes, it is unclear if they will be able to adapt at the rate of climate change predicted in the near future (Stern 2002). Wild species have three basic possible responses to climate change: (i) change geographical distribution to track environmental changes; (ii) remain in the same place but change to match the new environment, through either plastic response, such as shifts in phenology (for example timing of growth, breeding, etc.) or genetic response, such as an increase in the proportion of heat tolerant individuals; or (iii) extinction (IPCC 2001a).

Climate change Future changes in the global climate are difficult to predict. The climate system is made up of a number of components: the atmosphere, oceans, land surface, cryosphere (ice areas) and biosphere (including human influences). Each of these systems is the result of a large array of drivers and climate is a result of complex interactions between each of the components. The only way to make quantitative predictions about future changes in climate is through the use of Global Climate Models (GCM) which simulate future climates given an emissions scenario and a mathematical represen- tation of climate processes. Currently, there are hundreds of climate scenarios described in the literature. These scenarios, which cover both global and regional areas, have been developed for a variety of purposes and consider a large range of possible emission levels and other factors. Currently, the most extensively used scenarios, and those referred to in this review, are compiled by the Intergovernmental Panel on Climate Change (IPCC) in its Third Assessment Report (IPCC 2001b). The observed and predicted effects of global climate change vary between areas. Examples from the U.K. and surrounding waters have been included as an indication of these changes, as there is a long-time series for climate data and there have been intense efforts to predict future changes. The predicted changes for the U.K. are based on the U.K. Climate Impacts Program (UKCIP) scenarios, which provide the most comprehensive assessment of climate change impacts in the U.K. (Hulme et al. 2002).

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Changes in temperature Globally the average surface temperature (the average of near surface air temperature over land and sea surface temperature) has increased over the twentieth century by 0.6 ± 0.2ûC, with an increase of 0.4Ð0.7ûC in marine air temperature and a 0.4Ð0.8ûC increase in sea-surface temperature since the late-nineteenth century (IPCC 2001b). The global ocean heat content has increased significantly since the late 1950s, with more than half of the increase occurring in the upper 300 m of the ocean, this is equivalent to a rate of temperature increase in this layer of about 0.04ûC/decade (IPCC 2001b). The globally averaged surface (sea and land) temperature is projected to increase by 1.4Ð5.8ûC over the period 1990Ð2100 (IPCC 2001b). Projections indicate that the warming would vary by region (IPCC 2001a). In most areas of the North Atlantic during 2003, temperature in the upper water layers remained higher than the long-term average, with new records set in several regions (ICES 2004). Over the northern North Sea, average air temperatures have risen by 0.8ûC since 1960. Since 1995, winter sea temperatures in Scottish coastal waters have been warming faster than summer ones, resulting in a smaller annual range each year. Winter seabed temperatures at fishing grounds in the North Sea show a long-term warming trend since the 1970s. Over the last 30 yr, Scottish offshore waters have also warmed by between 1 and 1.5ûC. In oceanic waters at the edge of the U.K.’s continental shelf there has been a steady rise in temperature over the past 100 yr (FRS 1998, 2003). There has been an overall warming of U.K. coastal waters, with an increase in annually averaged temperature of about 0.6ûC over the past 70Ð100 years, with a substantial increase over the last 20 yr (Hulme et al. 2002). Climate change scenarios for the U.K. predict that the annual temperature across the U.K. may rise by between 2 and 3.5ûC by the 2080s. The temperature of U.K. coastal waters will also increase, although not as rapidly as over land. Offshore waters in the English Channel may warm in summer by between 2 and 4ûC over the same period (Hulme et al. 2002).

Changes in sea levels Tide gauge data show that global average sea level rose between 0.1 and 0.2 m during the twentieth century (IPCC 2001b). Global mean sea level is projected to rise by 0.09Ð0.88 m between 1990 and 2100. The geographical distribution of sea-level changes results from interactions between factors such as the geographical variation in thermal expansion, and changes in salinity, winds and ocean circulation. Therefore the range of regional variation is substantial compared with the global average sea level rise (IPCC 2001b). Climate change scenarios for the U.K. predict that by the 2080s sea levels may be between 2 cm below and 58 cm above the current level in western Scotland and between 26 and 86 cm above the current level in southeast England, depending on the climate change scenario and effects of land movements. Extreme sea levels, occurring through combinations of high tides, sea-level rise and changes in winds, are also predicted to become more frequent at many U.K. coastal locations (Hulme et al. 2002). A rise in sea level is likely to affect most coastal habitats, although the extent will vary with location and type of coastal habitat. Many coastal areas are already experiencing increased levels of sea flooding, accelerated coastal erosion and seawater intrusion into freshwater sources and these processes will increase with climate change and rises in sea levels (IPCC 2001a). Low-latitude tropical and subtropical coastlines are highly susceptible to climate change impacts (IPCC 2001a).

Changes in ocean circulation In the Arctic, as temperature increases, more freshwater from melting snow and ice will be released into the North Atlantic, through the Fram Strait between northeastern Greenland and Svalbard. This

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could exert a strong influence on salinity in the North Atlantic, shift the Gulf Stream current, and even affect upwelling related to the Great Ocean Conveyor Belt current system (Tynan & DeMaster 1997, Marotzke 2000). Most models show a weakening of the ocean thermohaline circulation, which will lead to a reduction of heat transport into high latitudes of the Northern Hemisphere. The current projections using climate models do not exhibit a complete shutdown of the thermohaline circulation by 2100. Beyond 2100, the thermohaline circulation could completely, and possibly irreversibly, shut down in either hemisphere (IPCC 2001b). Climate change scenarios predict a weakening of the Gulf Stream during the twenty-first century, perhaps by as much as 25% by 2100, although a shutdown of the Gulf Stream is not predicted in any climate models (Hulme et al. 2002). Shifts in the locations of fronts and upwellings are also expected as the climate changes, but are difficult to predict.

Changes in sea-ice extent There has been a retreat of sea-ice extent in the Arctic spring and summer by about 10Ð15% since the 1950s. It is likely that there has been about a 40% decline in Arctic sea-ice thickness during the late summer to early autumn in recent decades and a slower decline in winter sea-ice thickness (IPCC 2001b). In the Northern Hemisphere snow cover and sea-ice extent are projected to decrease further (IPCC 2001b). Over the past 100Ð150 yr, observations show that there has probably been a reduction of about two weeks in the annual duration of lake and river ice in the mid to high latitudes of the Northern Hemisphere (IPCC 2001b). The sea-ice extent in Antarctica appears to be more stable, with no readily apparent relationship between decadal changes in Antarctic tem- peratures and sea-ice extent since 1973 (IPCC 2001b). However, the Antarctic Peninsula ice shelves have retreated over the last century, resulting in the collapse of the Prince Gustav and parts of the Larsen ice shelves in 1995 (Vaughan & Doake 1996, IPCC 2001b).

Changes in salinity Changes in salinity may occur as a result of increased evaporation with increased temperature and changes in ocean circulation. There may also be more localised changes in salinity as a result of changes in precipitation and associated river input and land run-off or the melting of ice sheets. In most areas of the North Atlantic during 2003, salinity in the upper layers remained higher than the long-term average, with new records set in several regions (ICES 2004). The salinity of Scottish oceanic waters has generally increased, with values approaching the highest recorded over the past 100 yr. This may indicate the arrival of warmer, more saline waters from further south in the Atlantic (FRS 1998). In southern North Sea fishing areas (e.g., German Bight), there is an apparent trend of decreasing salinity at the sea bed in winter, which may be linked to freshwater inputs from rivers around the coast (FRS 2003). Inshore waters off the northeast of Scotland have experienced a decrease in salinity in the past 5 yr (FRS 2003).

Changes in CO2 concentrations and pH

The atmospheric concentration of carbon dioxide (CO2) has increased by 31% since 1750. The rate of increase over the past century is unprecedented during the past 20,000 yr, with the present

atmospheric CO2 increase being caused by anthropogenic emissions of CO2 (IPCC 2001b). The oceans absorb CO2 from the atmosphere and in the past 200 yr the oceans have absorbed approx- imately half of the CO2 produced by fossil fuel burning and cement production (Royal Society 2005). The uptake of anthropogenic CO2 by the oceans will continue to increase with increasing atmospheric CO2 concentrations. However, warming will reduce the solubility of CO2 and increased

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temperatures will also increase vertical stratification (decreasing mixing between ocean layers),

which will also reduce CO2 uptake by the oceans (IPCC 2001b, Royal Society 2005). Increasing atmospheric CO2 concentration has no significant fertilisation effect on marine biological productivity, but it decreases pH (IPCC 2001b). It is estimated that this uptake of CO2 has led to a reduction in the pH of surface waters by 0.1 units, which is the equivalent to a 30% increase in the concentration of hydrogen ions. Surface waters (<100 m) which are slightly alkaline (average pH is about 8.2) are becoming more acidic (Royal Society 2005). The average pH of the oceans is estimated to fall by 0.5 units (equivalent to a three-fold increase in the concentration of

hydrogen ions) by the year 2100 if global emissions of CO2 continue to rise at current levels (Royal Society 2005). The scale of the changes may vary regionally, affecting the magnitude of biological effects (Royal Society 2005).

Changes in rainfall patterns In the Northern Hemisphere it is very likely that precipitation has increased by 0.5Ð1% per decade in the twentieth century over most mid and high latitude land areas, and it is likely that rainfall has increased by 0.2Ð0.3% per decade over the tropical land areas (10ûNÐ10ûS) (IPCC 2001b). In the mid and high latitudes of the Northern Hemisphere over the latter half of the twentieth century, there has probably been a 2Ð4% increase in the frequency of heavy precipitation events (IPCC 2001b). Global average precipitation is projected to increase during the twenty-first century, with regional increases and decreases (IPCC 2001b). More intense precipitation events are very likely over many areas (IPCC 2001b). For example, throughout the U.K., winters over the last 200 yr have become wetter relative to summers, with a larger proportion of winter precipitation in all regions falling on heavy rainfall days compared to 50 yr ago (Hulme et al. 2002). Climate change scenarios for the U.K. predict that winter precipitation will increase, with increases ranging from 10Ð35% by the 2080s. The pattern for summer precipitation is reversed, with almost the whole of the U.K. becoming drier (Hulme et al. 2002).

Changes in storm frequency, wind speed and wave conditions Climate change is likely to affect local weather conditions in a number of ways. For example, there is a greater frequency in the formation of hurricanes and typhoons when water temperatures are 28ûC or above, and so the general warming of oceans may lead to changes in the frequency or strength of such weather events (IPCC 2001a). Climate change may also affect local weather in general rather than just the occurrence of specific types of weather events. For example, over the northern North Sea average wind speeds have become 2 knots faster since 1960 (FRS 1998). Waves in the North Sea have increased in size, by about 20 cm every 10 yr, as a result of increase in the average wind speed (FRS 1998). Around the U.K. coastline there was an apparent increase in average wave height of 10Ð15% between the 1980s and 1990s. The roughening wave climate over the last 40 yr is likely to result from a change in the strength of the North Atlantic Oscillation (NAO) (Hulme et al. 2002). In the last decade the U.K. has also experienced an increase in the frequency of gales, although this is not unprecedented in the historic record as gale frequencies are also related to the NAO (Hulme et al. 2002).

Changes in climate patterns Large-scale patterns of climate variability, such as the El Niño-Southern Oscillation (ENSO) and the NAO, account for major variations in weather and climate around the world and have been

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shown to affect marine species and fish stocks, through both direct and indirect pathways (Stenseth et al. 2002). The effects of short-term events such as El Niño and NAO can provide valuable insight into the potential effects of climate change.

The El Niño-Southern Oscillation (ENSO) Fluctuations in tropical Pacific sea-surface temperature are related to the occurrence of El Niño events, during which the equatorial surface waters warm considerably from the International Date Line to the west coast of South America. The Southern Oscillation is a global-scale ‘see-saw’ in atmospheric mass, involving exchanges of air between the Eastern and Western hemispheres centred in tropical and subtropical latitudes. Warm ENSO events are those in which both a negative Southern Oscillation and an El Niño occur together. Different phases of the ENSO shift the location of the heaviest tropical rainfall, and these changes in the heating of the atmosphere distort the flow of air over thousands of kilometres, producing anomalous cold and warm regions (Stenseth et al. 2002). Warm episodes of the ENSO phenomenon (which affects regional variations of precipitation and temperature over much of the tropics, subtropics and some mid-latitude areas and can affect the incidence and severity of hurricanes and typhoons) have been more frequent, persistent and intense since the mid-1970s, compared with the previous 100 yr (IPCC 2001b). Even with little or no change in El Niño amplitude, global warming is likely to lead to greater extremes of drying and heavy rainfall and to increase the risk of droughts and floods that occur with El Niño events in many different regions (IPCC 2001b). It is possible that overall climate change will have some similar effects to short-term El Niño events, although the effects of global climate change could be more gradual and more subtle. Potential changes in the frequency, intensity and persistence of climate extremes (e.g., heat waves, heavy precipitation and drought) associated with the ENSO could emerge as key determinants of future impacts and vulnerability (IPCC 2001a).

The North Atlantic Oscillation (NAO) The North Atlantic Oscillation is a north-south alteration in atmospheric mass between the sub- tropical atmospheric high-pressure centre over the Azores and the atmospheric subpolar low- pressure centre over Iceland. It determines the strength of the westerly winds blowing across the North Atlantic Ocean between 40 and 60ûN. Variability in the direction and magnitude of the westerlies is responsible for fluctuations in winter temperatures and the balance of precipitation and evaporation across the Atlantic and the adjoining landmasses. During positive phases of the NAO, the westerly winds are strengthened and moved northward, causing increased precipitation and temperatures over northern Europe and the southeastern U.S. and dry anomalies in the Mediterranean region (Planque & Taylor 1998, Stenseth et al. 2002). Climate change scenarios suggest the North Atlantic Oscillation will tend to become more positive in the future, resulting in more wet, windy, mild winters (Hulme et al. 2002).

Impacts of climate change on marine mammals The potential impacts of climate change on marine mammals can be (i) direct, such as the effects of reduced sea ice and rising sea levels on seal haul-out sites or a species tracking a specific range of water temperatures in which they can physically survive, and (ii) indirect, such as the potential impacts on reproductive success through effects on the distribution and abundance of prey or the structure of prey communities at specific locations.

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Effects of changes in temperature Direct effects

The most likely direct effects of changes in water temperature on marine mammals are shifts in species ranges as species track preferred or required temperature conditions. Baleen whales are less likely to be directly affected by changes in temperature, compared to other marine mammals, because of their mobility and thermoregulatory ability, although calves may be more susceptible than adults (IWC 1997). The majority of baleen whales, such as the blue, grey, humpback and fin whales, migrate large distances and experience temperature variations between their polar feeding grounds and tropical breeding grounds. However, several species have a more restricted distribution, for example, bowhead whales which are found only in the polar waters of the Arctic and may be uniquely heat intolerant (IWC 1997, Bannister 2002). Toothed whales (odontocetes) are more likely to be directly affected by changes in water temperature than baleen whales, as in general they are much smaller and several species are limited in the range of water temperatures that they inhabit. For example, belugas (Delphinapterus leucas) are restricted to polar and cold temperate waters in Arctic seas. As water temperatures change, species that inhabit specific ranges of water temperature would be expected to shift their geographic ranges to track preferred or required temperature conditions. However, for several species there may be physical limits to their ability to change their geographic range. For example, the endangered vaquita (Phocoena sinus), whose distribution is limited to the warm waters at the northern end of the Gulf of California, and river dolphins, baiji (Lipotes vexillifer), Ganges river dolphin (Platanista gangetica), Boto (Inia geoffrensis) and tucuxi (Sotalia fluviatilis), may be particularly vulnerable. Some individuals within a population may also be more susceptible than others, for example finless porpoise (Neophocaena phocaenoides) calves (IWC 1997). Increased variation in sea temperature, especially in coastal areas, may also be important: for example, a mass mortality of bottlenose dolphins in the Gulf of Mexico has been linked to an unusual cold-water event (IWC 1997). Changes in water temperature will also directly affect pinnipeds and sirenians. For example, the distribution of the manatee is influenced by temperature, with waters colder than 20ûC increasing the manatees’ susceptibility to cold stress and cold-induced mortality. Therefore an increase in sea temperature (i.e., extension of 20ûC isotherm) could lead to a possible increase in range directly related to changes in temperature (Reynolds & Powell 2002, Würsig et al. 2002).

Indirect effects

The direct and indirect effects of climate change on prey species can in turn have several indirect effects on marine mammals, including changes in distribution, abundance and migration, commu- nity structure, susceptibility to disease and contaminants, and reproductive success. Climate change may also indirectly affect marine mammal species through competition with other marine mammals.

Changes in distribution, abundance and migration

Marine mammals in general and baleen whales in particular, require dense patches of prey, such as crustaceans (copepods, euphausiids or krill, amphipods, shrimp), cephalopods (squid) and schooling fish. Therefore, the distribution, abundance and migration of baleen whales reflects the distribution, abundance and movements of these dense prey patches, which have in turn been linked to oceano- graphic features including fronts, eddies and primary productivity. These features, and hence the formation of dense prey patches, can be affected by several factors including temperature. Thus, the distribution of feeding whales, such as North Atlantic right whales, can be predicted from surface temperature and bathymetric variables, such as depth and slope, due to their effects on prey distribution.

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Changes in plankton distribution, abundance and composition are related to ocean climate, including temperature (Southward et al. 1995; Planque & Taylor 1998; Ducrotoy 1999; Heath et al. 1999a,b; Edwards et al. 2001, 2002; Beare et al. 2002; Beaugrand 2003; Reid et al. 2003a; Edwards & Richardson 2004; Moline et al. 2004). For example, in the northeastern North Atlantic Ocean and adjacent seas there have been recent shifts in all copepod assemblages, with a northward extension of more than 10û in latitude of warm-water species associated with a decrease in the number of colder-water species. These changes reflect regional increases in sea-surface temperature (Beaugrand & Reid 2003). Therefore marine mammals and their prey that depend on plankton species may be affected by these shifts in distribution. The distribution, abundance and migration of odontocetes are also strongly influenced by prey distribution, for example, in the Gulf of Maine/Georges Bank, northeast America, shifts in cetacean distributions and abundance relate to trends in fish abundance (Kenney et al. 1996). In the Faroe Islands where there is a long history (catch statistics are available for almost 300 yr) of traditional drive harvest of long-finned pilot whales (Globicephala melas), peaks in catch rates are correlated with periods of warmer temperatures and the occurrence of their main prey, the pelagic squid Todarodes sagittatus. The occurrence of pelagic squid may be influenced by temperature directly, or indirectly through effects on hydrography or productivity, which in turn, influences the distribution and abundance of the pilot whales (Bj¿rge 2002). Temperature can directly affect the embryonic development, age of sexual maturity, timing of spawning, growth and survival of most fish and cephalopod species (for example, Boyle 1983). The distribution, abundance and migration of several fish and cephalopod species are also related to temperature, including whiting (Merlangius merlangus), herring (Clupea harengus), veined squid (Loligo forbesi) and Patagonian long-fin squid (L. gahi) (Sims et al. 2001, Zheng et al. 2002, Pierce & Boyle 2003, Arkhipkin et al. 2004, Sissener & Bj¿rndal 2005). The distributions of both exploited species, such as Atlantic cod (Gadus morhua) and common sole (Solea solea), and nonexploited species in the North Sea have responded markedly to recent increases in sea temper- ature, with distributions of nearly two-thirds of species shifting in mean latitude and/or depth over the past 25 yr (Perry et al. 2005). An increase in the abundance of several warm-water species, including anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) in the North Sea and North Atlantic, also correspond to recent increases in temperature (Stebbing et al. 2002, Beare et al. 2004a,b). These shifts in prey species are likely to affect the distribution of marine mammal species. For example, changes in species distribution have been related to increases in temperature indirectly through the effects on prey. During the 1982–83 El Niño event, near-shore bottlenose dolphins expanded their range from southern to central California and have stayed in the new northern range well after the warming event subsided in the mid-1980s. It is believed that movement of prey, rather than water temperature itself, may have caused the range expansion (Wells et al. 1990, Wells & Scott 2002). Bottlenose dolphins off the northeast coast of Scotland are at the northern limit of their distribution. There is evidence of a recent range expansion, the causes of which are unknown, but may be related to changes in prey abundance and/or distribution (Wilson et al. 2004). A recent expansion in range of fur seals in the subantarctic Indian Ocean has been related to climate and its effects on prey. For example, the re-establishment of Antarctic fur seals (Artocephalus gazelle) on Heard Island in the past 50 yr coincides with warmer temperature, glacier recession and hypothesised improved food supplies (Shaughnessy & Green 1998).

Changes in community structure

Shifts in the range of a species may be a response to climate change directly or indirectly as a result of changes in prey distribution or availability, and/or interactions with other species (Davis et al. 1998). Changes in the cetacean community of northwest Scotland have been related to recent

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ocean warming. There has been a decline in the relative frequencies of strandings and sightings of white-beaked dolphins, a colder-water species and a relative increase in strandings and sightings of common dolphins, a warmer-water species (MacLeod et al. 2005). These results suggest a possible range expansion of common dolphins and a decrease in range of white-beaked dolphins, which may be due to the direct effects of changes in temperature or indirect effects, such as competitive exclusion. This has potentially serious implications for white-beaked dolphins, which are generally found in cold water less than 200 m deep around northwest Europe, as their ability to respond to climate change by tracking suitable habitat may be restricted, due to the lack of suitable shelf waters further north. This may lead to a decline in abundance or its distribution becoming fragmented (MacLeod et al. 2005). Climate-related changes in cetacean community structure have also been associated with El Niño events. During the 1982–83 El Niño, near-bottom spawning market squid (Loligo opale- scens) and short-finned pilot whales (Globicephala macrorhynchus), which normally feed on the squid, were absent from the southern California area (Shane 1994). The absence of pilot whales was followed several years later by an influx of Risso’s dolphins (Grampus griseus) feeding on the returned market squid. The Risso’s dolphins may have taken advantage of the temporarily vacant niche left by the pilot whales, apparently as a result of the El Niño event (Shane 1995).

Effects on reproductive success

Changes in temperature, through the effects on prey availability, can have potentially serious impacts on the reproductive success of marine mammals. For example, a decrease in North Atlantic right whale calf survival has been related to the effects of climate variability on prey abundance (Greene & Pershing 2004). Female fin whales, in years of great food abundance at the summer feeding grounds, might produce a calf in consecutive years, whereas in poor years the cycle can be extended to 3 yr. In female fin whales, there appears to be a close correlation between food abundance, body fat condition and fecundity (Lockyer 1986). It is thought that ovulation is suppressed if a certain threshold level of body weight or fat is not attained (Boyd et al. 1999). Similar strategies have also been observed in terrestrial animals, for example red deer (Cervus elaphus) (e.g., Hamilton & Blaxter 1980). Calving intervals and the sex ratios of calves of humpback whales have been related to maternal condition: females in a ‘superior’ condition had a calving interval of 3 or more years and the sex ratio of their calves was biased toward males (Wiley & Clapham 1993). Observations of sea-surface temperature and the abundance of sperm whale calves near the Galapagos Islands suggest that females have a lower rate of conception after periods of warm sea- surface temperature, usually caused by ENSO events. Although the relationship between increased sea-surface temperature and the abundance of calves is tentative, it is supported by poor foraging success of females and immature sperm whales during warm conditions when primary productivity is suppressed (Whitehead 1997). Therefore, any increase in temperature as a result of global warming and/or the frequency and duration of El Niño events could have serious implications for populations such as sperm whales in the Galápagos Islands (Whitehead 1997). Differences in reproductive success have also been related to prey availability in odontocetes, pinnipeds and sirenians. For example, in harbour porpoise from the Bay of Fundy, changes in the growth and age of sexual maturity have been linked to changes in prey availability (Read & Gaskin 1990). In Antarctic fur seals the duration of pregnancy is longer and birth takes place later in years associated with reduced prey availability (Boyd 1996). Reproductive failure, especially in the form of high juvenile mortality, affected several seal colonies, including Galápagos fur seals (Artoceph- alus galapagoensis), during the major El Niño year of 1982. This massive recruitment failure was attributed to shifts in prey distribution, as at least some lethal and sublethal effects were linked to starvation (Würsig et al. 2002). In sirenians there appears to be considerable potential plasticity of

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life-history parameters in response to food availability, with food shortages probably causing sirenians to reproduce later and less often (Boyd et al. 1999). Breeding in many species may be timed to coincide with maximum abundance of suitable prey, either for the lactating mother or the calf at weaning, so that any changes in the environmental conditions which determine prey abundance may cause a mismatch in synchrony between predator and prey, either in time or location. Migratory species that travel long distances between feeding and breeding areas may be particularly vulnerable to mismatching. The uncoupling of phenological relationships has important implications for trophic interac- tions, altering food-web structures and leading to changes in the ecosystem. The recruitment success of higher marine trophic levels is highly dependent on synchronization with plankton production. Observations indicate that the marine pelagic community responds to climate changes, and that the level of response differs throughout the community and seasonal cycle. These differences in response have led to a mismatch between successive trophic levels and a change in synchrony of timing between primary, secondary and tertiary production (Edwards & Richardson 2004). The link between climate change and the cascade effects on trophic levels has been observed in phytoplankton, zooplankton and salmon (Salmo salar) in the northeast Atlantic, with predicted temperature increases expected to result in a decline in the abundance of salmon returning to home waters (Beaugrand & Reid 2003). The growth and survival of cod larvae (Gadus morhua) depends on synchronous production with their main prey, the early stages of zooplankton (Stenseth et al. 2002). The decline in cod recruitment in the North Sea has been linked to rising temperatures affecting the plankton ecosystem (O’Brien et al. 2000, Beaugrand et al. 2003). Changes due to mismatches in the food chain and the effects on prey species are likely to have serious implications for marine mammals.

Increased susceptibility to disease, contaminants and other potential causes of death

Increased susceptibility to disease, starvation and the exposure to contaminants have been related to changes in prey type or reduced prey availability (Thompson et al. 1997, Geraci et al. 1999, Geraci & Lounsbury 2002, Würsig et al. 2002). For example, marked interannual variations in food availability, diet composition and body condition of harbour seals (Phoca vitulina) were associated with physiological responses, such as differences in haematological parameters. Differences observed in leukocyte counts could have resulted from immuno-suppression, for example because of differences in prey nutrient or contaminant levels (Thompson et al. 1997). Insufficient prey availability results in the use of blubber reserves and the associated mobili- sation of any accumulated contaminants, such as organochlorines, organobromines and polyaro- matic hydrocarbons (Aguilar et al. 1999, Reijinders & Aguilar 2002). The majority of persistent organic pollutants and toxic elements have the potential to cause immune, reproductive and endo- crine disrupting effects (Helle et al. 1976, Fuller & Hobson 1986, Reijnders 1986, Aguilar & Borrell 1994, de Swart et al. 1994, Kuiken et al. 1994, Jepson et al. 1999, Ross et al. 2000, Hoffman et al. 2001). The frequency and severity of toxic algal blooms are likely to increase as a result of nutrient enrichment (increased rainfall and runoff) and increased temperature. Fatal poisonings have occurred in cetaceans, pinnipeds and manatees (Geraci et al. 1989, 1999; Hernández et al. 1998; Scholin et al. 2000; Domingo et al. 2002; Geraci & Lounsbury 2002; Gilmartin & Forcada 2002). Changes in

precipitation, pH, water temperature, wind, dissolved CO2 and salinity can affect water quality in estuarine and marine waters and some marine disease organisms and algal species are strongly influenced by one or more of these factors. Climate change has the potential to increase pathogen development and survival rates, disease transmission, and host susceptibility (Harvell et al. 2002). Higher temperatures may also stress organisms, increasing their susceptibility to some diseases, especially if they are at the upper end of their thermal tolerance (Lafferty et al. 2004). Climate

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change is expected to affect the range and migratory patterns of many marine mammals, which in turn could lead to a spread of viruses and the introduction of novel pathogens. In the past two decades there has been an apparent increase in large-scale mortality events such as morbillivirus infections, which caused massive die-offs of striped dolphins (Stenella coeruleoalba) in the Med- iterranean Sea and seals in Europe, although the actual causes are not fully understood (Kennedy et al. 1992, Aguilar & Raga 1993, Cebrian 1995, Kennedy 1996, Geraci et al. 1999, Harvell et al. 1999, Kennedy 1999, Van Bressem et al. 2001, Domingo et al. 2002, Geraci & Lounsbury 2002).

Effects of rising sea levels Direct effects

Cetaceans, both baleen whales and odontocetes, are unlikely to be directly affected by rises in sea levels, although important habitats for coastal species and species that require coastal bays and lagoons for breeding, such as grey and humpback whales, could be affected (IWC 1997). Pinniped haul-out sites for breeding, nurseries and resting are likely to be directly affected. For example, rising sea levels could eliminate already scarce haul-out sites of the Mediterranean monk seal (Monachus monachus), especially by the flooding of caves that provide the only refuges for some groups (Harwood 2001, Würsig et al. 2002).

Indirect effects

The construction of sea-wall defences and protective measures for coastal habitats against increasing sea levels could potentially impact coastal marine species and possibly interfere with migration routes. For example, in Florida between 1974 and 1996 about 4% of manatee deaths were due to crushing and drowning in flood gates or canal locks (Reynolds & Powell 2002). Dams and other structures have also obstructed the normal migration routes of manatees along rivers in South America and West Africa (Reynolds & Powell 2002).

Effects of changes in ocean currents Direct effects

The range of marine mammals that are associated with oceanic fronts, such as the Antarctic convergence in the Southern Ocean, could be directly affected by changes in ocean currents and the positions of associated fronts. In the Southern Ocean, the Antarctic convergence, an oceanic front between cold southern polar waters and northern temperate waters, is an important physical feature that defines the normal southern extent of the distributions of most tropical and temperate marine mammals. The ocean temperature can change by as much as 10ûC across the Antarctic convergence, which may only be a few miles across (Boyd 2002). The segregation of male and female sperm whales is associated with the Antarctic convergence, with only male sperm whales found within the Southern Ocean during summer, and females and young males remaining north of the polar front throughout the year (Boyd 2002).

Indirect effects

Changes in ocean mixing, deep water production and coastal upwelling will have profound impacts on the status, sustainability, productivity and biodiversity of the coastal zone and marine ecosystem (IPCC 2001a). Changes in ocean currents will directly affect the distribution, abundance and migration of plankton, many fish and cephalopod species (for example, Planque & Taylor 1998, Waluda et al. 2001, Walther et al. 2002), which in turn will affect marine mammals. For example, in the Barents

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Sea fluctuations in the influx of Atlantic water affects the location of the polar front and water temperature. This influences the distribution and species composition of the primary and secondary production, with subsequent effects on the distribution and diet of minke whales (Bj¿rge 2002).

Effects of a decrease in sea-ice cover Direct effects

Seals that rely on ice for breeding are likely to suffer considerable habitat loss with a decrease in sea-ice extent. Particularly vulnerable may be species that are confined to inland seas and lakes, such as the Caspian seal (Phoca caspica), the Baikal seal (Phoca siberica), and subspecies of the ringed seal (Phoca hispida lagodensis and P. h. saimensis), which will be limited in their ability to track the receding ice cover (Harwood 2001). During the breeding season, the ice on which pinnipeds haul out must be thick enough and persist long enough for completion of the critical stages of birth, feeding of the pups, and in many cases, completion of their annual moult (Burns 2002). Ice characteristics can affect the distribution and activity patterns of pinnipeds, with pack ice (i.e., large pieces of ice, which vary from a few metres to several hundred metres in diameter, that are not attached to land) offering a more constant substratum than fast ice (i.e., ice that is attached to the land), which is highly variable with season (breeding sites of pinnipeds are given in Table 1). For pinnipeds that reproduce on fast ice, the duration of lactation and rearing of their young strongly depends on ice conditions (Forcada 2002). Ringed seals, bearded seals (Ergnathus barbatus) and walruses (Odobenus rosmarus), which rely on suitable ice substrate for resting, pupping and moulting, may be particularly vulnerable to changes in sea-ice extent (Tynan & DeMaster 1997). For example, earlier spring breakup of ice together with lower snow depths suggest a continued low pup survival of ringed seals in western Hudson Bay (Ferguson et al. 2005). Polar bears require ice as a solid substratum on which to hunt and rear their offspring. The distribution of polar bears is probably a function of the distribution of ice conditions that allow them to hunt and travel most efficiently, especially in areas of ice floes, between foraging areas and areas where they give birth and rear their young. Therefore, any changes in the extent and type of ice cover are expected to affect the distributions, foraging and reproductive success of polar bears (Tynan & DeMaster 1997, Forcada 2002). In western Hudson Bay there has been a significant decline in the condition of adult male and female polar bears, along with an overall decline in the proportion of independent yearling cubs between 1981 and 1998, during which period the breakup of the sea ice had been occurring earlier, causing the bears to come ashore in poorer condition (Stirling et al. 1999). Open-water areas, such as annual recurring polynyas (areas within the pack ice that are almost always clear of ice), driven by upwelling or wind, variable shore leads or cracks, or tidal- and wind-driven openings in the sea ice, are critical for several marine mammal species, such as walrus, belugas, narwhals and bowhead whales (Heide-J¿rgensen & Laidre 2004). Although global warming has reduced sea-ice formation in the Arctic this trend is not uniform and any changes in the timing and distribution of these important open water areas will have direct and severe implications for the marine mammals dependent on them (Tynan & DeMaster 1997, Heide-J¿rgensen & Laidre 2004, Laidre & Heide-J¿rgensen 2005).

Indirect effects

Changes in the extent and concentration of sea ice may alter the seasonal distribution, geographic ranges, patterns of migration, nutritional status, reproductive success, and ultimately the abundance and stock structure of species associated with the ice edge, such as plankton, fish, crustaceans and marine mammals (Tynan & DeMaster 1997). Melting ice sheets in the Arctic will reduce ocean

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salinities, which in turn may cause highly variable shifts in the distribution and biomass of major constituents of Arctic food webs. These changes in the distribution and abundance of prey will affect more mobile species such as the bowhead whales, belugas and narwhals, as well as resident or sedentary species, such as pinnipeds and polar bears (Tynan & DeMaster 1997, Laidre et al. 2004). For example, periods of decline in the production of ringed seals, and consequently polar bears, have been linked with ice conditions, possibly as a result of a reduction in regional produc- tivity causing poor nutritional condition in the seals (Tynan & DeMaster 1997). Large baleen whale species that undertake long distance migrations from tropical breeding grounds to high-latitude feeding grounds close to the ice edge may be at risk as the polar ice caps retreat. The longer migration paths that will be required will increase the costs of movement and reduce the duration of the feeding season (Stern 2002). Species, such as the grey whale, that use the Arctic for summer feeding grounds are likely to experience disruptions in the timing and distribution of their food sources (Tynan & DeMaster 1997). Migratory species within the Arctic will also be affected, for example, the migration of belugas and narwhals is linked to the spring production of ice algae and ice-edge productivity (Tynan & DeMaster 1997). Warming in the Arctic will cause changes in species compositions, with a tendency for poleward shifts in species assem- blages and loss of some polar species (Tynan & DeMaster 1997). In the Southern Ocean, climate change is likely to produce long-term, perhaps irreversible, changes in the physical oceanography and ecology. Projected reductions in sea-ice extent will alter under-ice biota and the spring bloom in the sea-ice marginal zone and will cause profound impacts to all levels in the food chain, from algae to krill to whales (e.g., Fraser & Hofmann 2003). Marine mammals which have life histories that tie them to specific breeding sites, such as Weddell (Lep- tonychotes weddellii), Ross (Ommatophoca rossii) and crabeater (Lobodon carcinophaga) seals, will be severely affected by shifts in their foraging habitats and migration of prey species associated with a decrease in sea-ice extent. For example, growth and survival of seal pups are directly influenced by krill abundance. Warming could reduce the extent of pack ice in the Antarctic and thus affect the distribution and abundance of krill. Declining krill abundance in the region of the Antarctic Peninsula during the 1990s has been linked to low winter sea-ice extent (Boyd 2002, Fraser & Hofmann 2003).

Effects of changes in salinity Direct effects

The salinity of the surface waters of the open ocean varies between 32 practical salinity units (psu) in the subarctic Pacific to 37 psu in subtropical gyres. At the coastal and polar limits of the ocean and in marginal seas, processes such as local precipitation and evaporation, river runoff and ice formation can result in salinities of less than 10 and greater than 40 psu. Many marine mammals have adapted to tolerate variations in salinity (Fiedler 2002). However, populations of bottlenose dolphins from areas of low water temperature and low salinity have been found to exhibit higher skin lesion prevalence and severity. It is thought that such conditions may impact on the epidermal integrity or produce more general physiological stress, potentially making the animals more vulnerable to natural infections or anthropogenic factors (Wilson et al. 1999). This indicates that variations in environmental factors can have an important effect on disease in marine mammals.

Indirect effects

Changes in salinity, for example, with changes in river inputs/runoff and melting ice, will influence the distribution and abundance of prey through effects on stratification of the water column and circulation and possibly also due to limited salinity tolerance. For example, most cephalopods are

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particularly sensitive to changes in salinity (Boyle 1983, Fiedler 2002). Shifts in the phytoplankton community structure, from diatoms to cryptophytes, in the near-shore coastal waters along the Antarctic Peninsula have been linked to glacial melt-water runoff and reduced surface water salinity. This shift in phytoplankton community structure directly affects the zooplankton assemblage. Antarctic krill do not graze efficiently on cryptophytes due to their small size, and an increase in the relative abundance of cryptophytes will cause a shift in the spatial distribution of krill. This in turn will affect higher trophic levels in the food web as krill is an important prey for several seabird and marine mammal species (Moline et al. 2004).

Effects of changes in CO2 concentrations and pH Direct effects

Carbon dioxide accumulating in the atmosphere permeates into ocean surface layers, where it may

impact on marine animals (Pörtner et al. 2004). The direct effects of increased CO2 concentrations and associated decrease in pH on marine mammals are unknown.

Indirect effects

Increased levels of CO2 have important implications for large marine animals that do not breathe air (i.e., the prey of marine mammals) as increased CO2 will acidify the body tissues and fluids (hypercapnia) and affect the ability of blood to carry oxygen. Changes in CO2 levels and pH are likely to affect metabolic function and therefore growth and reproduction of water breathing animals (Pörtner et al. 2004, Royal Society 2005). Sensitivity is highest in ommastrephid squids, such as Illex illecebrosus, which are characterised by a high metabolic rate and extremely pH-sensitive

blood oxygen transportation. In comparison to squid, fish are better protected from CO2 effects as they have a lower metabolic rates and higher capacities to compensate for CO2-induced pH disturbances (Pörtner et al. 2004). In general, the number of species suffering from acute CO2 toxicity will be limited. However, although individuals in a population may be tolerant over a short

period, it is impossible to determine the long-term effects of changes in CO2 levels and pH on individuals and populations (Pörtner et al. 2004).

Effects of changes in rainfall patterns Direct effects

More intense precipitation events and flash floods will result in increased runoff. Thus, increased nutrient inputs into coastal waters, combined with an increase in water temperatures could cause an increase in toxic algal blooms and eutrophication (see section above on increased susceptibility to diseases and other causes of death).

Indirect effects

The effects of eutrophication play an important role in phytoplankton seasonal and community dynamics in the southern North Sea (Edwards et al. 2001). Changes associated with changes in rainfall patterns, for example, a decrease in salinity in coastal waters, will affect the distribution and abundance of prey species. Increased runoff as a result of increased precipitation may also cause an increase in inputs of pollutants, including sewage, with potential effects on coastal marine mammal and prey species.

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Changes in rainfall patterns are likely to lead to an increased demand for fresh water in some areas, resulting in the regulation of water flow through the use of dams and dredging. These are major barriers to the migration of river dolphins. Such activities have already created small isolated populations and rendered some areas of otherwise suitable habitat completely inaccessible. Flood control will result in loss of shallow water habitats that are often used extensively during rainy seasons (Harwood 2001).

Effects of changes in storm frequency, wind speed and wave conditions Direct effects

Changes in prevailing ocean wave height and directions and storm waves and surges can be expected to have serious impacts on coasts as they will be superimposed on increasing sea levels (IPCC 2001a). Pinniped haul-out sites for breeding and nurseries are likely to be vulnerable to any changes in storm frequency and wave conditions, for example, the Mediterranean monk seal, which is reliant on a small number of caves or narrow beaches for breeding (Harwood 2001, Würsig et al. 2002).

Indirect effects

Coastal ecosystems such as coral reefs and atolls, salt marshes and mangrove forests, and submerged aquatic vegetation will be directly impacted by any changes in storm frequency and intensity (IPCC 2001a). These areas are important nursery grounds for many fish and invertebrate species, and therefore the prey of marine mammals.

Effects of changes in climate patterns Direct effects

Changes in climate patterns, such as El Niño events, have been linked directly and indirectly to massive die-offs and shifts in distribution of plankton, fishes (such as anchovy), seabirds and marine mammals (Stenseth et al. 2002).

Indirect effects

The predicted increase in frequency of warm events associated with the ENSO, would result in a decline in plankton biomass and fish larvae abundance, adversely impacting fish recruitment patterns and spatial distribution of fish stocks, with subsequent effects on marine mammals, seabirds and ocean biodiversity (IPCC 2001a, Stenseth et al. 2002). The indirect effects associated with El Niño events on marine mammal species are mostly related to changes in prey availability and include (i) changes in community structure, for example, after the 1982–83 El Niño short-finned pilot whales appeared to be replaced by Risso’s dolphins (Shane 1994, 1995), (ii) changes in species ranges, for example, the range expansion of bottlenose dolphins along the Californian coast during and after the 1982–83 El Niño event (Wells et al. 1990), and (iii) effects on reproduction, for example, reduced fecundity or calf survival in sperm whales of the eastern tropical Pacific during and after an El Niño event in the late 1980s (Whitehead 1997), and high juvenile mortality in seal colonies, such as Galapagos fur seals during the El Niño year of 1982 (Würsig et al. 2002). There is also some indirect evidence for environmental effects on reproduction in female dusky dolphins (Lagenorhynchus obscurus) during the 1982–83 El Niño event off Peru. The deposition of poorly calcified dentinal growth layer groups in the teeth of

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pregnant and lactating females during the period of El Niño and reduced prey availability, indicated nutritional stress (Manzanilla 1989, Boyd et al. 1999). The NAO can influence, directly and indirectly, the recruitment, growth, distribution, abundance and survival of several fish, cephalopod and plankton species (Stenseth et al. 2002). For example, changes in sea temperatures driven by NAO variations have been linked to cod recruitment off Labrador and Newfoundland, and in the Barents Sea (Stenseth et al. 2002). The temporal and spatial population dynamics of Calanus finmarchicus and C. helgolandicus have been linked to the NAO (Planque & Taylor 1998, Beare et al. 2002, Stenseth et al. 2002, Beaugrand & Ibanez 2004). Early stages of Calanus species are the main prey for larvae and early juveniles of many fish species throughout the North Atlantic and thus influence fish recruitment success and consequently the size of fish populations (Stenseth et al. 2002, Walther et al. 2002). These changes in prey abundance and distribution as a result of the NAO are likely to have direct and indirect effects on marine mammal species in the North Atlantic. In addition to ENSO and NAO variability, the persistence of multi-year climate-ocean regimes and switches from one regime to another have been recognised, with changes in recruitment patterns of fish populations linked to such switches (IPCC 2001a). Similarly, survival of marine mammals and seabirds is also affected by interannual and longer-term variability in several oceanographic and atmospheric properties and processes, especially in high latitudes (IPCC 2001a).

Conservation and legislation related to marine mammals The conservation status of marine mammals is provided by the World Conservation Union (IUCN), which maintains a red list of threatened species and provides advice to organisations such as International Whaling Commission (IWC) and Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). In the most recent Red List (IUCN 2004) (listed in Table 1), six of the 28 cetacean species for which sufficient data were available are considered endangered, five species are listed as vulnerable and two species, the vaquita and baiji, are critically endangered; 14 of the 15 species that are listed as low risk are conservation dependent and one is listed as near threatened. Nearly 60% of the 67 cetacean species included in the IUCN red list are classed as being ‘data deficient’, indicating that a lack of scientific knowledge is a major barrier to the conservation of cetacean populations. Seven of the 11 pinniped species listed in the IUCN red list are classed as vulnerable, two as endangered and one, the Mediterranean monk seal, as critically endangered. All four sirenian species are listed as vulnerable, both the sea otter and marine otter are endangered and polar bears are conservation dependent. Marine mammals are subjected to various threats and pressures throughout their range, including incidental catch in fisheries, boat strikes, prey depletion, pollution (including heavy metals, orga- nochlorine compounds, oil and sewage), habitat disturbance and degradation; algal blooms, noise pollution, introduction of exotic species and pathogens, marine debris and climate change (Perrin et al. 2002, Evans & Raga 2001). International conservation conventions and institutions that relate to marine mammals include the IWC, which was created in 1946 following the International Convention for the Regulation of Whaling. Formerly devoted to the regulation of whaling, the IWC has increasing become involved in the preservation and recovery of cetacean populations. In 1996 the IWC sponsored a workshop on climate change and cetaceans (IWC 1997). The Convention on the Conservation of Migratory Species of Wild Animals (CMS or Bonn Convention) is an international treaty that provides a mechanism for regional conservation agree- ments. This has led to the Agreement on the Conservation of Small Cetaceans of the Baltic and North Sea (ASCOBANS) and the Agreement on the Conservation of Small Cetaceans of the Black Sea, Mediterranean Sea and Contiguous Atlantic Area (ASCOBAMS). ASCOBANS carried out a

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multinational abundance survey of cetaceans in 1994 throughout the Baltic and North Sea (Ham- mond et al. 2002) and another survey was carried out in 2005. Marine mammals are also protected under conservation acts such as the Marine Mammal Protection Act in the U.S. and the Convention on the Conservation of European Wildlife and Natural Habitats (Bern Convention). Protected or management areas intended, at least in part, to benefit marine mammals have been established in several areas, for example, the Biosphere Reserve in the upper Gulf of Mexico to protect the vaquita and the Hawaiian Island Humpback Whale Sanctuary (for further examples see Reeves 2002).

Implications of climate change for the management and conservation of marine mammals Management and conservation measures need to take into account the potential changes in range and changing requirements of marine mammals. The adverse effects on breeding habitat may be reduced by creating protected areas for the remaining habitat, if this can be identified. However, the main method for adapting to change in the wider environment will be to manage human impacts on the resources required by marine mammal species through some form of ecosystem-based management. The European Marine Strategy proposes the management of all human activities in the sea based on three central features: an Ecosystem Approach, Integrated Management and a Regional Focus for the coordination and delivery of management programmes. One way to protect marine mammals would be to designate marine protected areas (‘no-take zones’) for the prey of marine mammals as well as marine mammal species. However, the ideal location of such areas is likely to change over time, and this will require different legislation than currently used. For example, there needs to be a degree of flexibility in the establishment of protected areas for marine mammals, such as Special Areas of Conservation (SAC), to take into account the potential shift in range and needs of marine mammals resulting from climate change (e.g., Wilson et al. 2004 and MacLeod et al. 2005). However, protective and conservation measures will not be able to solve many of the problems faced by marine mammals as a result of climate change and therefore the mitigation of greenhouse gases to prevent temperature increase and the associated changes in climate may be the only solution.

Knowledge gaps and future research Marine mammals are large, long-lived warm-blooded animals that show considerable behavioural plasticity. This plasticity allows many species to respond to environmental changes within a single generation and these species are unlikely to be affected physiologically by moderate changes in the physical characteristics of their environment. Their apparent reliance on behavioural responses to environmental changes, some of which can be transmitted culturally, means that low genetic diversity, which has been demonstrated for some species, does not necessarily affect their ability to respond to such changes. However, the limits to this plasticity are not known. One of the greatest threats to marine mammals probably comes from changes in their food resources, as a result of climate change. Many prey species such as fish, cephalopods and plankton appear to rely on, and are influenced by, particular sets of environmental conditions. Any changes in the geographic distribution of these conditions as a result of climate change will affect the abundance and distribution of prey species. This will ultimately affect the availability of these prey to marine mammals, which in turn would affect their distribution and migration, and could have serious consequences for reproduction and survival. More information is required to determine the potential impact of climate change on the timing and extent of population movements, distribution,

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abundance, recruitment, and species composition of prey. The theoretical basis for identifying and tracking areas where the prey of marine mammals should be protected is limited, and more information is required on the factors affecting prey availability and prey quality. Future data needs include the continued monitoring or establishment of long-term stranding and sightings records of marine mammals, especially in areas at the northern and southern limits of the range of the species. The range of migratory and resident species can be very sensitive to climate and individuals can show an immediate response, for example, in their migratory destina- tions. Therefore, as with climatic data, a long time series is required to distinguish year-to-year variation from long-term trends (IPCC 2001a, Walther et al. 2002). These data are needed to (i) detect changes in the community structure, abundance or distribution of species, (ii) compare with long-term records of other marine species such as plankton, fish, cephalopods and environmental variables and (iii) detect any changes in cause of death (i.e., the presence of ‘new’ diseases, etc.). The establishment of regular marine mammal monitoring programmes in areas where infor- mation is limited, especially areas that are known or thought to be important for breeding and/or feeding and on migration routes, is essential. The regionally distinctive effects of climate change make it difficult to predict the potential impacts on most species; therefore more information is required on a regional scale to determine critical habitat and diet. This is especially true for populations that are already under threat: those with reduced abundance due to past whaling, by- catch and/or pollutants and restricted to a limited distribution and/or dependent on critical habitats for breeding or feeding. More information is required for species, such as beaked whales (Ziphiidae), for which very little is known about their distribution, abundance, migration and diet, and for which, therefore, the potential effects of climate change or any other potential threat are difficult to predict. In general, more information and research is needed on the direct effects of temperature change

on marine mammals; the potential impacts of changes in salinity, pH and CO2; habitat use and requirements for almost all species; competitive interactions between marine mammal species, and the effects of climate change on the spread and prevalence of diseases. The effects of climate change are unlikely to be isolated and therefore further information is required on the potential effects of synergetic interactions, for example, the effects of changes in prey availability combined with the effects of increased stress due to changes in temperature, etc. To understand the impacts of climate change on marine mammal species and populations, we also need to take into account other threats and pressures, such as habitat degradation/destruction, by-catch, pollution, noise, etc., already faced by many marine mammals. Currently there has been very little done to model/predict future climate change scenarios in relation to their potential effects and impacts on marine mammals.

Summary of the potential effects of climate change on marine mammals Direct effects of changes in temperature include shifts in species ranges; some may expand and some may contract. However, species with restricted ranges, for example, polar species, the vaquita and river dolphins, may be particularly vulnerable. More information is needed on potential direct physiological effects of increased temperature on marine mammals and the possible implications. Indirect effects of changes in temperature include the effects of climate change on prey availability affecting the distribution, abundance and migration, community structure, susceptibility to disease and contaminants, reproductive success, and, ultimately, the survival of marine mammal species. Changes in the range and abundance of competitors and predators will also affect marine mammals to varying degrees depending on the species and location. Management and conservation measures need to take into account the potential changes in species’ range by creating protected areas for the remaining and predicted habitat.

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Rising sea levels will directly affect pinniped haul-out sites. The Mediterranean monk seal may be particularly vulnerable as it is reliant on a small number of caves or narrow beaches for breeding and these sites could easily be destroyed or rendered unusable by rising sea levels and increased storm frequency. Remaining breeding sites, as well as potentially suitable breeding sites as condi- tions change, need to be protected. The construction of protective barriers for coastal habitats, against rising sea levels, could have several implications for coastal marine mammals, including habitat degradation, effects on prey, direct mortality and obstruction to migration. Detailed envi- ronmental impact assessments are required that take into account the current and possible future impacts on marine mammals. Changes in ocean currents, upwellings and fronts could affect the distribution of marine mammals either directly, especially if the limits to their range are defined by the boundary between two water masses, or indirectly as a result of changes in the distribution and occurrence of prey associated with currents, upwellings and fronts. Protective measures could include flexible no-take zones that follow changes in prey distribution rather than fixed areas. Marine mammals, particularly those that rely on ice or the environment close to the ice edge, are vulnerable to the direct effects of a decrease in sea-ice cover. Seals and polar bears that rely on ice for breeding are likely to suffer considerable habitat loss. Large baleen whale species that undertake long-distance migrations from tropical breeding grounds to high-latitude feeding grounds close to the ice edge may be at risk as the polar ice caps retreat. The longer migration paths that will be required will increase the costs of movement and reduce the duration of the feeding season. Changes in sea extent and salinity will affect all species associated with the ice edge, either directly or indirectly through spatial and/or temporal changes in prey availability.

The potential effects and impacts of changes in salinity, pH and CO2 on marine mammals are not fully understood and require further research, although prey species — especially cephalopods — may be particularly sensitive. Changes in rainfall patterns and increased runoff, as well as changes

in temperature, salinity, pH and CO2, could increase toxic algal blooms. Fatalities due to toxic algal blooms have occurred in cetacean, pinniped and manatee species. Improving water management and control of discharges could help to elevate the potential risks of increased eutrophication and toxic algal blooms. The greatest threat to marine mammals probably comes from changes in their food resources as a result of climate change. For example, many species appear to rely on particular sets of environmental conditions to concentrate their prey. If climate change affects the geographic distri- bution of these oceanographic conditions, this could ultimately have serious consequences for marine mammal reproduction and survival. For populations that are already under threat (e.g., from low numbers due to past whaling, severely affected by by-catch and/or pollutants, restricted to a limited distribution dependent on critical habitats for breeding or feeding), the effects (direct and/or indirect) of climate change may be more important.

Acknowledgements The work for this review was carried out as part of the Climate Change and Migratory Species Report for DEFRA Research Contract CR0302. Thanks also go to John Harwood (SMRU) who provided useful comments and suggestions on an early draft of the report and to other colleagues who participated in discussions on the effects of climate change at the project workshop in Cambridge, 2005.

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References

Aguilar, A. & Borrell, A. 1994. Abnormally high polychlorinated biphenyl levels in striped dolphins (Stenella coeruleoalba) affected by the 1990Ð1992 Mediterranean epizootic. The Science of the Total Environ- ment 154, 237Ð247. Aguilar, A., Borrell, A. & Pastor, T. 1999. Biological factors affecting variability of persistent pollutant levels in cetaceans. In Chemical Pollutants and Cetaceans, Special Issue 1, P.J.H. Reijnders et al. (eds). Cambridge: International Whaling Commission, 83Ð116. Aguilar, A. & Raga, J.A. 1993. The striped dolphin epizootic in the Mediterranean Sea. Ambio 22, 524Ð528. Alerstam, T., Hedenström, A. & Åkesson, S. 2003. Long-distance migration: evolution and determinants. Oikos 103, 247Ð260. Anderson, L.W., Ruzzante, D.E., Walton, M., Berggren, P., Bj¿rge, A. & Lockyer, C.H. 2001. Conservation genetics of harbour porpoises, Phocoena phocoena, in eastern and central North Atlantic. Conservation Genetics 2, 309Ð324. Arkhipkin, A.I., Grzebielec, R., Sirota, A M., Remeslo, A.V., Polishchuk, I.A. & Middleton, D.A.J. 2004. The influence of seasonal environmental changes on the ontogenetic migrations of the squid Loligo gahi on the Falkland shelf. Fisheries Oceanography 13, 1Ð9. Bannister, J.L. 2002. Baleen whales. In Encyclopedia of Marine Mammals, W.F., Perrin et al. (eds). San Diego: Academic Press, 62Ð72. Beare, D.J., Batten, S., Edwards, M. & Reid, D.G. 2002. Prevalence of boreal Atlantic, temperate Atlantic and neritic zooplankton in the North Sea between 1958 and 1998 in relation to temperature, salinity, stratification intensity and Atlantic inflow. Journal of Sea Research 48, 29Ð49. Beare, D.J., Burns, F., Greig, T., Jones, E.G., Peach, K., Kienzle, M., McKenzie, E. & Reid, D.G. 2004a. Long-term increases in prevalence of North Sea fishes having southern biogeographic affinities. Marine Ecology Progress Series 284, 269Ð278. Beare, D.J., Burns, F., Jones, E., Peach, K., Portilla, E., Greig, T., McKenzie, E. & Reid, D.G. 2004b. An increase in the abundance of anchovies and sardines in the north-western North Sea since 1995. Global Change Biology 10, 1209Ð1213. Beaugrand, G. 2003. Long-term changes in copepod abundance and diversity in the north-east Atlantic in relation to fluctuations in the hydroclimatic environment. Fisheries Oceanography 12, 270Ð283. Beaugrand, G., Brander, K.M., Lindley, J.A., Souissi, S. & Reid, P.C. 2003. Plankton effect on cod recruitment in the North Sea. Nature 426, 661Ð664. Beaugrand, G. & Ibanez, F. 2004. Monitoring marine plankton ecosystems II: long-term changes in North Sea calanoid copepods in relation to hydro-climatic variability. Marine Ecology Progress Series 284, 35Ð47. Beaugrand, G. & Reid, P.C. 2003. Long-term changes in phytoplankton, zooplankton and salmon related to climate. Global Change Biology 9, 801Ð817. Bj¿rge, A. 2002. How persistent are marine mammal habitats in an ocean of variability? In Marine Mammals: Biology and Conservation, P.G.H. Evans & J.A. Raga (eds). New York: Kluwer Academic/Plenum Publishers, 63Ð91. Bj¿rge, A. & Tolley, K.A. 2002. Harbour Porpoise. In Encyclopedia of Marine Mammals, W.F. Perrin et al. (eds). San Diego: Academic Press, 549Ð551. Boyd, I.L. 1996. Individual variation in the duration of pregnancy and birth date in Antarctic fur seals: the role of environment, age, and sex of foetus. Journal of Mammalogy 77, 124Ð133. Boyd, I.L. 2002. Antarctic marine mammals. In Encyclopedia of Marine Mammals, W.F. Perrin et al. (eds). San Diego: Academic Press, 30Ð36. Boyd, I.L., Lockyer, C. & Marsh, H.D. 1999. Reproduction in marine mammals. In Biology of Marine Mammals, J.E. Reynolds III. & S.A. Rommel (eds). Washington, D.C.: Smithsonian Institute Press, 218Ð286. Boyle, P.R. (ed.). 1983. Cephalopod Life Cycles. London: Academic Press. Burns, J.J. 2002. Arctic marine mammals. In Encyclopedia of Marine Mammals, W.F. Perrin. et al. (eds). San Diego: Academic Press, 39Ð45. Cebrian, D. 1995. The striped dolphin Stenella coeruleoalba epizootic in Greece, 1991Ð1992. Biological Conservation 74, 143Ð145.

459 7044_C008.fm Page 460 Tuesday, April 25, 2006 1:04 PM

J.A. LEARMONTH, C.D. MACLEOD, M.B. SANTOS, G.J. PIERCE, H.Q.P. CRICK & R.A. ROBINSON

Cockeron, P.J. & Connor, R.C. 1999. Why do baleen whales migrate? Marine Mammal Science 15, 1228Ð1245. Davis, A.J., Jenkinson, L.S., Lawton, J.H., Shorrocks, B. & Wood, S. 1998. Making mistakes when predicting shifts in species range in response to global warming. Nature 391, 783Ð786. de Swart, R.L., Ross, P.S., Vedder, L.J., Timmerman, H.H., Heisterkamp, S., Van Loveren, H., Vos, J.G., Reijnders, P.J.H. & Osterhaus, A.D.M.E. 1994. Impairment of immune function in harbour seals (Phoca vitulina) feeding on fish from polluted water. Ambio 23, 155Ð159. Domingo, M., Kennedy, S. & Van Bressem, M. 2002. Marine mammal mass mortalities. In Marine Mammals: Biology and Conservation, P.G.H. Evans & J.A. Raga (eds). New York: Kluwer Academic/Plenum Publishers, 425Ð456. Ducrotoy, J.P. 1999. Indications of change in the marine flora of the North Sea in the 1990s. Marine Pollution Bulletin 38, 646Ð654. Edwards, M., Beaugrand, G., Reid, P.C., Rowden, A.A. & Jones, M.B. 2002. Ocean climate anomalies and the ecology of the North Sea. Marine Ecology Progress Series 239, 1Ð10. Edwards, M., Reid, P. & Planque, B. 2001. Long-term and regional variability of phytoplankton biomass in the Northeast Atlantic (1960Ð1995). ICES Journal of Marine Science 58, 39Ð49. Edwards, M. & Richardson, A.J. 2004. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881Ð884. EEA. 2004. Impacts of Europe’s changing climate. Copenhagen: European Environment Agency. Evans, P.G.H. & Raga, J.A. (eds). 2001. Marine Mammals Biology and Conservation. New York: Kluwer Academic/Plenum Publishers, 630 pp. Ferguson, S.H., Stirling, I. & McLoughlin, P. 2005. Climate change and ringed seals (Phoca hispida) recruit- ment in western Hudson Bay. Marine Mammal Science 21, 121Ð135. Fiedler, P.C. 2002. Ocean Environment. In Encyclopedia of Marine Mammals, W.F. Perrin et al. (eds). San Diego: Academic Press, 824Ð830. Forcada, J. 2002. Distribution. In Encyclopedia of Marine Mammals, W.F. Perrin et al. (eds). San Diego: Academic Press, 327Ð333. Fraser, W.R. & Hofmann, E.E. 2003. A predator’s perspective on causal links between climate change, physical forcing and ecosystem response. Marine Ecology Progress Series 265, 1Ð15. FRS 1998. Scottish Ocean Climate Status Report 1998. Report No. 9/99. Aberdeen, U.K.: Fisheries Research Services, 11 pp. FRS 2003. Scottish Ocean Climate Status Report 2000Ð2001. Report No. 05/03. Aberdeen, U.K.: Fisheries Research Services, 20 pp. Fuller, G.B. & Hobson, W.C. 1986. Effects of PCBs on reproduction in mammals. In PCBs and the Environ- ment, II, J.S. Waid (ed.). Boca Raton, FL: CRC Press, 101Ð125. Geraci, J.R., Andersen, D.M., Timperi, R.J., St. Aubin, D.J., Early, G.A., Prescott, J.H. & Mayo, C.A. 1989. Humpback whales fatally poisoned by dinoflagellate toxin. Canadian Journal of Fisheries and Aquatic Sciences. 46, 1895Ð1898. Geraci, J.R., Harwood, J. & Lounsbury, V.J. 1999. Marine mammal die-offs. In Conservation and Management of Marine Mammals, J.R. Twiss Jr. & R.R. Reeves (eds). Washington, D.C.: Smithsonian Institution Press, 367Ð395. Geraci, J.R. & Lounsbury, V. 2002. Marine mammal health: holding the balance in an ever changing sea. In Marine Mammals: Biology and Conservation, P.G.H. Evans & J.A. Raga (eds). New York: Kluwer Academic/Plenum Publishers, 365Ð384. Gilmartin, W.G. & Forcada, J. 2002. Monk seals. In Encyclopedia of Marine Mammals, W.F. Perrin. et al. (eds). San Diego: Academic Press, 756Ð759. Greene, C.H. & Pershing, A.J. 2004. Climate and the conservation biology of North Atlantic right whales: the right whale at the wrong time? Frontiers in Ecology and the Environment 2, 29Ð34. Hamilton, W.J. & Blaxter, K.L. 1980. Reproduction in farmed red deer 1: hind and stag fertility. Journal of Agricultural Science 95, 261Ð273. Hammond, P.S., Berggren, P., Benke, H., Borchers, D.L., Collet, A., Heide-Jorgensen, M.P., Heimlich, S., Hiby, A.R., Leopold, M.F. & Oien, N. 2002. Abundance of harbour porpoise and other cetaceans in the North Sea and adjacent waters. Journal of Applied Ecology 39, 361Ð376.

460 7044_C008.fm Page 461 Tuesday, April 25, 2006 1:04 PM

POTENTIAL EFFECTS OF CLIMATE CHANGE ON MARINE MAMMALS

Hansen, B., Turrell, W.R. & ¯sterhus, S. 2001. Decreasing overflow from the Nordic seas into the Atlantic Ocean through the Faroe Bank channel since 1950. Nature 411, 927Ð930. Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J., Hofmann, E.E., Lipp, E.K., Osterhaus, A D.M.E., Overstreet, R.M., Porter, J.W., Smith, G.W. & Vasta, G.R. 1999. Emerging marine diseases — climate links and anthropogenic factors. Science 285, 1503Ð1510. Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P., Ostfeld, R.S. & Samuel, M.D. 2002. Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158Ð2162. Harwood, J. 2001. Marine mammals and their environment in the twenty-first century. Journal of Mammalogy 82, 630Ð640. Heath, M.R., Adams, R.D., Brown, F., Dunn, J., Fraser, S., Hay, S.J., Kelly, M.C., Macdonald, E.M., Robertson, M. R., Robertson, S. & Wilson, C. 1999a. Plankton monitoring off the east coast of Scotland in 1997 and 1998. Report No. 13/99. Aberdeen, U.K.: Fisheries Research Services, 32 pp. Heath, M.R., Beare, D.J., Dunn, J., Fraser, J.G., Hay, S.J. & Turrell, W.R. 1999b. Monitoring the effects of climate change — overwintering abundance of Calanus finmarchicus in the Faroe-Shetland Channel. Report No. 14/99. Aberdeen, U.K.: Fisheries Research Services, 24 pp. Heide-J¿rgensen, M.P. & Laidre, K.L. 2004. Declining extent of open-water refugia for top predators in Baffin Bay and adjacent waters. Ambio 33, 487Ð494. Helle, E., Olsson, M. & Jensen, S. 1976. PCB levels correlated with pathological changes in seal uteri. Ambio 5, 261Ð263. Hernández, M., Robinson, I., Aguilar, A., González, L.M., López-Jurado, L.F., Reyero, M.I., Cacho, E., Franco, J., López-Rodas, V. & Costas, E. 1998. Did algal toxins cause monk seal mortality? Nature 393, 28. Hoffman, D., Rattner, B. A., Scheunert, I. & Korte, F. 2001. Environmental Contaminants. In Ecotoxicology of Wild Mammals, R.F. Shore & B.A. Rattner (eds), Chichester, England: John Wiley & Sons Ltd., 1Ð48. Hulme, M., Jenkins, G.J., Lu, X., Turnpenny, J.R., Mitchell, T.D., Jones, R.G., Lowe, J., Murphy, J.M., Hassell, D., Boorman, P., McDonald, R. & Hill, S. 2002. Climate change scenarios for the United Kingdom: the UKCIP02 scientific report. Norwich: Tyndall Centre for Climate Change Research, 120 pp. ICES. 2004. The Annual ICES Ocean Climate Status Summary 2003/2004. Report No. 269. Copenhagen: International Council for the Exploration of the Sea, 32 pp. IPCC. 2001a. Climate Change 2001: Impacts, Adaptation and Vulnerability. Cambridge: Cambridge University Press, 1032 pp. IPCC. 2001b. Climate Change 2001: The Scientific Basis. Cambridge: Cambridge University Press, 881 pp. IUCN. 2004. Red list of threatened species. www.redlist.org. [Date accessed: December 2004] IWC. 1997. Report of the IWC workshop on climate change and cetaceans. Report of the International Whaling Commission 47, 293Ð313. Jepson, P.D., Bennett, P.M., Allchin, C.R., Law, R.J., Kuiken, T., Baker, J.R., Rogan, E. & Kirkwood, J.K. 1999. Investigating potential associations between chronic exposure to polychlorinated biphenyls and infectious disease mortality in harbour porpoises from England and Wales. The Science of the Total Environment 243/244, 339Ð348. Jones, M.L. & Swartz, S.L. 2002. Gray whale. In Encyclopedia of Marine Mammals, W.F. Perrin et al. (eds). San Diego: Academic Press, 524Ð536. Kaschner, K. 2004. Modelling and mapping resource overlap between marine mammals and fisheries on a global scale. PhD, Alber-Lubwigs-Universitat, Freiburg, Germany. Kennedy, S. 1996. Infectious diseases of cetacean populations. In The Conservation of Whales and Dolphins, M.P. Simmonds & J.D. Hutchinson (eds). Chichester, U.K.: John Wiley & Sons, 333Ð353. Kennedy, S. 1999. Morbilliviral infections in marine mammals. In Chemical Pollutants and Cetaceans, Special Issue 1, P.J.H. Reijnders et al. (eds). Cambridge: International Whaling Commission, 267Ð273. Kennedy, S., Kuiken, T., Ross, H.M., McAliskey, M., Moffett, D., McNiven, C.M. & Carole, M. 1992. Morbillivirus infection in two common porpoises (Phocoena phocoena) from the coasts of England and Scotland. Veterinary Record 131, 286Ð290. Kenney, R.D., Payne, M., Heinemann, D.W. & Winn, H.E. 1996. Shifts in Northeast shelf cetacean distributions relative to trends in Gulf of Maine/Georges Bank finfish abundance. In The Northeast Shelf Ecosystem: Assessment, Sustainability and Management, K. Sherman et al. (eds). Cambridge, MA: Blackwell Science, 169Ð196.

461 7044_C008.fm Page 462 Tuesday, April 25, 2006 1:04 PM

J.A. LEARMONTH, C.D. MACLEOD, M.B. SANTOS, G.J. PIERCE, H.Q.P. CRICK & R.A. ROBINSON

Kuiken, T., Bennett, M.E., Allchin, C.R., Kirkwood, J.K., Baker, J., Lockyer, C., Walton, M. & Sheldrick, M.C. 1994. PCBs, cause of death and body condition in harbour porpoises (Phocoena phocoena) from British waters. Aquatic Toxicology 28, 13Ð28. Lafferty, K.D., Porter, J.W. & Ford, S.E. 2004. Are diseases increasing in the ocean? Annual Review of Ecology and Systematics. 35, 31Ð54. Laidre, K.L. & Heide-J¿rgensen, M.P. 2005. Arctic sea ice trends and narwhal vulnerability. Biological Conservation 121, 509Ð517. Laidre, K.L., Heide-J¿rgensen, M.P., Logdson, M.L., Hobbs, R.C., Heagerty, P., Dietz, R., J¿rgensen, O.A. & Treble, M.A. 2004. Seasonal narwhal habitat associations in the high Arctic. Marine Biology 145, 821Ð831. LeDuc, R. 2002. Biogeography. In Encyclopedia of Marine Mammals, W.F. Perrin. et al. (eds). San Diego: Academic Press, 99Ð103. Lockyer, C.H. 1986. Body fat condition in Northeast Atlantic fin whales, Balaenoptera physalus, and its relationship with reproduction and food resource. Canadian Journal of Fisheries and Aquatic Sciences 43, 142Ð147. MacLeod, C.D., Bannon, S.M., Pierce, G.J., Schweder, C.S., Learmonth, J.A., Herman, J.S. & Reid, R.J. 2005. Climate change and the cetacean community of north-west Scotland. Biological Conservation 124, 477Ð483. Mann, J., Connor, R.C., Tyack, P.L. & Whitehead, H. (eds). 2000. In Cetacean Societies: Field Studies of Dolphins and Whales. Chicago: The University of Chicago Press, 415 pp. Manzanilla, S.R. 1989. The 1982Ð1983 El Nino event recorded in dentinal growth layers in teeth of Peruvian dusky dolphins (Lagenorhynchus obscurus). Canadian Journal of Zoology 67, 2120Ð2125. Marotzke, J. 2000. Abrupt climate change and thermohaline circulation: mechanisms and predictability. Proceedings of the National Academy of Sciences of the United States of America 97, 1347Ð1350. Moline, M.A., Claustre, H., Frazer, T.K., Schofields, O. & Vernet, M. 2004. Alterations of the food web along the Antarctic Peninsula in response to a regional warming trend. Global Change Biology 10, 1973Ð1980. Northridge, S.P., Tasker, M.L., Webb, A. & Williams, J.M. 1995. Distribution and relative abundance of harbour porpoises (Phocoena phocoena), white-beaked dolphins (Lagenorhynchus albirostris) and minke whales (Balaenoptera acutorostrata) around the British Isles. ICES Journal of Marine Science 52, 55Ð66. O’Brien, C.M., Fox, C.J., Planque, B. & Casey, J. 2000. Climate variability and North Sea cod. Nature 404, 142. Parmesan, C. & Galbraith, H. 2004. Observed impacts of global climate change in the U.S. Arlington, VA: Pew Center on Global Climate Change. Parmesan, C. & Yohe, G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37Ð42. Perrin, W.F., Würsig, B. & Thewissen, J.G.M. (eds). 2002. Encyclopedia of Marine Mammals. San Diego: Academic Press, 1414 pp. Perry, A.L., Low, P.J., Ellis, J.R. & Reynolds, J.D. 2005. Climate change and distribution shifts in marine fishes. Science 308, 937. Planque, B. & Taylor, A.H. 1998. Long-term changes in zooplankton and the climate of the North Atlantic. ICES Journal of Marine Science 55, 644Ð654.

Pörtner, H.O., Langenbuch, M. & Reipschläger, A. 2004. Biological impact of elevated ocean CO2 concen- trations: lessons from animal physiology and earth history. Journal of Oceanography 60, 705Ð718. Read, A. & Gaskin, D.E. 1990. Changes in growth and reproduction of Harbour porpoises, Phocoena phocoena, from the Bay of Fundy. Canadian Journal of Fisheries and Aquatic Sciences 47, 2158Ð2163. Reeves, R.R. 2002. Conservation efforts. In Encyclopedia of Marine Mammals, W.F. Perrin. et al. (eds). San Diego: Academic Press, 276Ð297. Reid, D.G., Edwards, M., Beaugrand, G., Skogen, M. & Stevens, D. 2003a. Periodic changes in the zooplankton of the North Sea during the twentieth century linked to oceanic inflow. Fisheries Oceanography 12, 260Ð269. Reid, J.B., Evans, P.G.H. & Northridge, S.P. (eds). 2003b. Atlas of Cetacean Distribution in North-west European Waters. Peterborough: Joint Nature Conservation Committee, 75 pp.

462 7044_C008.fm Page 463 Tuesday, April 25, 2006 1:04 PM

POTENTIAL EFFECTS OF CLIMATE CHANGE ON MARINE MAMMALS

Reijinders, P.J.H. & Aguilar, A. 2002. Pollution and marine mammals. In Encyclopedia of Marine Mammals, W.F. Perrin. et al. (eds). San Diego: Academic Press, 948Ð957. Reijnders, P.J.H. 1986. Reproductive failure in common seals feeding on fish from polluted coastal waters. Nature 324, 456Ð467. Reynolds, J.E. & Powell, J.A. 2002. Manatees. In Encyclopedia of Marine Mammals, W.F. Perrin et al. (eds). San Diego: Academic Press, 709Ð720. Rice, D.W. 1998. Marine Mammals of the World: Systematics and Distribution. The Society of Marine Mammalogy, Special Publication No. 4. Ridgeway, S.H. & Harrison, R. (eds). 1985. Handbook of Marine Mammals. Volume 3: The Sirenians and Baleen Whales. London: Academic Press. Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosenzweig, C. & Pounds, J.A. 2003. Fingerprints of global warming on plants and animals. Nature 421, 57Ð60. Ross, P.S., Vos, J.G., Birnbaum, L.S. & Osterhaus, A.D.M.E. 2000. PCBs are a health risk for humans and wildlife. Science 289, 1878Ð1879. Royal Society. 2005. Ocean acidification due to increasing atmospheric carbon dioxide. Policy Document 12/05. London: The Royal Society, 60 pp. Scholin, C.A., Gulland, F., Doucette, G.J., Benson, S., Busman, M., Chavez, F.P., Cordaro, J., DeLong, R., De Vogelaere, A., Harvey, J., Haulena, M., Lefebvre, K., Lipscomb, T., Loscutoff, S., Lowenstine, L.J., Marin III, R., Miller, P.E., McLellan, W.A., Moeller, P.D.R., Powell, C.L., Rowles, T., Silvagni, P., Silver, M., Spraker, T., Trainer, V. & Van Dolah, F.M. 2000. Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature 403, 80Ð84. Sear, C., Hulme, M., Adger, N. & Brown, K. 2001. The impacts of global climate change of the UK overseas territories. Norwich: Tyndall Centre for Climate Change Research, 49 pp. Shane, S.H. 1994. Occurrence and habitat use of marine mammals at Santa Catalina Island, California from 1983Ð91. Bulletin Southern California Academy of Sciences 93, 13Ð29. Shane, S.H. 1995. Relationship between pilot whales and Risso’s dolphins at Santa Catalina Island, California, USA. Marine Ecology Progress Series 123, 5Ð11. Shaughnessy, P.D. & Green, K. 1998. Continued increase in the population of Antarctic fur seals, Arctocephalus gazella, at Heard Island, Southern Ocean. Marine Mammal Science 14, 384Ð389. Sims, D.W., Genner, M.J., Southward, A.J. & Hawkins, S.J. 2001. Timing of squid migration reflects North Atlantic climate variability. Proceedings of the Royal Society of London, B Biological Sciences 268, 2607Ð2611. Sissener, E.H. & Bj¿rndal, T. 2005. Climate change and the migratory pattern for Norwegian spring-spawning herring — implications for management. Marine Policy 29, 299Ð309. Southward, A.J., Hawkins, S.J. & Burrows, M.T. 1995. Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. Journal of Thermal Biology 20, 127Ð155. Stebbing, A.R.D., Turk, S.M.T., Wheeler, A. & Clarke, K.R. 2002. Immigration of southern fish species to south-west England linked to warming of the North Atlantic (1960Ð2001). Journal of the Marine Biological Association of the United Kingdom 82, 177Ð180. Stenseth, N., Mysterud, A., Ottersen, G., Hurrell, J. W., Chan, K.-S. & Lima, M. 2002. Ecological effects of climate fluctuations. Science 297, 1292Ð1296. Stern, S.J. 2002. Migration and movement patterns. In Encyclopedia of Marine Mammals, W.F. Perrin et al. (eds). San Diego: Academic Press, 742Ð750. Stirling, I., Lunn, N.J. & Iacozza, J. 1999. Long-term trends in the population ecology of polar bears in western Hudson Bay in relation to climate change. Arctic 52, 294Ð306. Thompson, P.M., Tollit, D.J., Corpe, H.M., Reid, R.J. & Ross, H.M. 1997. Changes in haematological parameters in relation to prey switching in a wild population of harbour seals. Functional Ecology 11, 743Ð750. Tynan, C.T. & DeMaster, D.P. 1997. Observations and predictions of Arctic climatic change: potential effects on marine mammals. Arctic 50, 308Ð322.

463 7044_C008.fm Page 464 Tuesday, April 25, 2006 1:04 PM

J.A. LEARMONTH, C.D. MACLEOD, M.B. SANTOS, G.J. PIERCE, H.Q.P. CRICK & R.A. ROBINSON

Van Bressem, M.F., Van Waerebeek, K., Jepson, P.D., Raga, J.A., Duignan, P.J., Nielsen, O., Di Beneditto, A.P., Siciliano, S., Ramos, R., Kant, W., Peddemors, V., Kinoshita, R., Ross, P.S., López-Fernandez, A., Evans, K., Crespo, E. & Barrett, T. 2001. An insight into the epidemiology of dolphin morbillivirus worldwide. Veterinary Microbiology 81, 287Ð304. Vaughan, D.G. & Doake, C.S.M. 1996. Recent atmospheric warming and retreat of ice shelves on the Antarctic Peninsula. Nature 379, 328Ð331. Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.-M., Hoegh- Guldberg, O. & Bairlein, F. 2002. Ecological responses to recent climate change. Nature 416, 389Ð395. Waluda, C.M., Rodhouse, P.G., Podestá, G.P., Trathan, P.N. & Pierce, G.J. 2001. Surface oceanography of the inferred hatching grounds of Illex argentinus (Cephalopoda: Ommastrephidae) and influences on recruitment variability. Marine Biology 139, 671Ð679. Weaver, A.J. & Zwiers, F.W. 2000. Uncertainty in climate change. Nature 407, 571Ð572. Wells, R.S., Hansen, L.J., Baldridge, A., Dohl, T.P., Kelly, D.L. & Defran, R.H. 1990. Northward extension of the range of bottlenose dolphins along the California coast. In The Bottlenose Dolphin, S. Leather- wood & R.R. Reeves (eds). San Diego: Academic Press, 421Ð431. Wells, R.S. & Scott, M.D. 2002. Bottlenose dolphins. In Encyclopedia of Marine Mammals, W.F. Perrin et al. (eds). San Diego: Academic Press, 122Ð128. Whitehead, H. 1997. Sea surface temperature and the abundance of sperm whale calves off the Galápagos Islands: implications for the effects of global warming. Report of the International Whaling Commis- sion 47, 941Ð944. Whitehead, H. 2002. Sperm whale. In Encyclopedia of Marine Mammals, W.F. Perrin et al. (eds). San Diego, Academic Press, 1165Ð1172. Wiley, D.N. & Clapham, P.J. 1993. Does maternal condition affect the sex ratio of offspring in humpback whales? Animal Behaviour 46, 321Ð324. Wilson, B., Arnold, H., Bearzi, G., Fortuna, C.M., Gaspar, R., Ingram, S., Liret, C., Pribanic, S., Read, A.J., Ridoux, V., Schneider, K., Urian, K.W., Wells, R.S., Wood, C., Thompson, P.M. & Hammond, P.S. 1999. Epidermal diseases in bottlenose dolphins: impacts of natural and anthropogenic factors. Pro- ceedings of the Royal Society of London, B Biological Sciences 266, 1077Ð1083. Wilson, B., Reid, R. J., Grellier, K., Thompson, P.M. & Hammond, P.S. 2004. Considering the temporal when managing the spatial: a population range expansion impacts protected areas-based management for bottlenose dolphins. Animal Conservation 7, 331Ð338. Würsig, B. 2002. Ecology, Overview. In Encyclopedia of Marine Mammals, W.F. Perrin et al. (eds). San Diego: Academic Press, 367Ð370. Würsig, B., Reeves, R.R. & Ortega-Ortiz, J.G. 2002. Global climate change and marine mammals. In Marine Mammals: Biology and Conservation, P.G.H. Evans & J.A. Raga (eds). New York: Kluwer Aca- demic/Plenum Publishers, 589Ð608. Zheng, X., Pierce, G.J., Reid, D.G. & Jolliffe, I.T. 2002. Does the North Atlantic current affect spatial distribution of whiting? Testing environmental hypotheses using statistical and GIS techniques. ICES Journal of Marine Science 59, 239Ð253.

464

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AUTHOR INDEX

References to complete articles are given in bold type, references to bibliographic lists are in normal type.

A Alongi, G. See Furnari, G., 187 See Giaccone, G., 188 Abbiati, M., 182 Alonso, B. See Canals, M., 185 See Santangelo, G., 193 Altinok, Y., 411 See Virgilio, M., 427 Altizer, S. See Harvell, C.D., 461 Abdalla, A.M., 117 Alvarez, L.A. See Marín, A., 270 Abe, T., 411 See Spinella, A., 273 Aboukais, A. See Nassrallah-Aboukais, N., 80 Alvarez, R., 258 Abramson, S.N., 258 Aly, O.M. See Faust, S.D., 78 Acebal, C. See Uriz, M. J., 194 Amos, C.L. See Flindt, M.R., 417 Ache, B.W. See Schmitt, B.C., 81 Amsler, C.D., 258 Acunto, S., 182 Andelman, S. See Gerber, L.R., 417 See Ferdeghini, F., 186 See Lubchenco, J., 421 Adam, W., 317 Andelmann, S. See Carr, M.H., 414 Adami, M.L., 411 Andersen, D.M. See Geraci, J.R., 460 Adams, R.D. See Heath, M.R., 461 Andersen, F.¯. See Flindt, M.R., 417 Adey, W.H., 182 Andersen, R.A. See Coyer, J.A., 415 Adger, N. See Sear, C., 463 Andersen, R.J. See Ayer, S.W., 259 Adjeroud, M. See Magalon, H., 422 See Barsby, T., 259 Agoumi, A., 50 Andersen, R.J. See Burgoyne, D. L., 260 Aguilar, A., 459 See Dumdei, E.J., 263 See Hernández, M., 461, See Faulkner, D.J., 264 See Reijnders, P.J.H., 463 See Graziani, E.I., 267 Ahearn, G.A., 76 See Gustafson, K., 267 See Aiken, D.E., 76 Hellou, J., 267 See Kubanek, J., 269 Airoldi, L., 182, 183 See Tischler, M., 274 Akali, B. See Piazzi, L., 192 Anderson, E.S., 258 Åkesson, S. See Alerstam, T., 459 Anderson, G.B., 258 Aksnes, D.L. See Skogen, M.D., 55 Anderson, L.W., 459 Akyuz, T., 77 Anderson, T.L., 117 Albers, C. See Kattner, G., 268 Andersson, I., 77 Alcazar, J., 317 Andrade, S.C.S., 411 Aldred, R.G., 317 Andre, C. See Johannesson, K., 419 Alerstam, T., 459 Andrén, T. See Hernroth, B., 79 Alexander, C.G. See Si, A., 425 Andrieux, F. See Guillaud, J.-F., 52 Alexander, R.M., 117 Angelini, S. See Cattaneo-Vietti, R., 261 Alexander, R.R., 117 Anger, K., 411 Algar, C. See Boudreau, B.P., 117 See Petersen, S., 81 Aliani, S., 411 Angerhofer, C.K. See Simpson, J.S., 273 Alikhan, M.A., 77 Anonymous, 77 Allchin, C.R. See Jepson, P.D., 461 Ansell, A.D., 117 See Kuiken, T., 462 Antiss, J.M. See Taylor, H.H., 82 Allcock, A.L., 411 Antolic, B. See Piazzi, L., 192 See Collins, M.A., 318 Appleton, D.R., 258 See Johnson, M.P., 419 Arais, A.M. See Blasco, J., 77 See Vecchione, M., 321 Arata, J. See Xavier, J.C., 322 Allen, I. See Proctor, R., 54 Arca, B. See De Petrocellis, L., 263 Allen, J.I., 50 Arcas, A. See Garrabou, J., 188 Aller, R.C., 77, 117 Argyrou, M. See Piazzi, L., 192 Allison, G.W., 411 Arimoto, H., 258 Almers, W. See Palade, P.T., 81 Arkhipkin, A.I., 459 Al-Mohanna, S.Y., 77 Arlhac, D. See Romano, J. C., 192 Alongi, D.M., 411 Armstrong, E., 259

465

7044_Idx.fm Page 466 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Arnaud, F., 259 Baker, J.R. See Jepson, P.D., 461 Arndt, A., 411 Bakker, J.P. See Bockelmann, A.C., 413 Arnold, E. See Hellou, J., 267 Balata, D. See Acunto, S., 182 Arnold, E.N. See Carranza, S., 414 See Piazzi, L., 191, 192 Arnold, H. See, Wilson, B., 464, Baldridge, A. See Wells, R.S., 464 Arnoux, A., 183 Balduzzi, A. See Boero, F., 184 Asai, N. See Fusetani, N., 265 Balkas, T.I., 77 Aschner, J.L. See Aschner, M., 77 Ball, A.O., 412 Aschner, M., 77 Ballantyne, F. See Gerber, L.R., 417 Ashworth, M. See Allen, J.I., 50 Ballesteros, E., 123Ð195, 183, 184 Atema, J. See Devine, D.V., 78 See Boudouresque, C.F., 185 See Moore, P., 80 See Canals, M., 185 Athanasiadis, A., 183 See Cebrian, E., 185 Atkinson, R.J.A., 117 See Corbera, J., 186 Augier, H., 183 See Garrabou, J., 188 Ault, J.S. See Glynn, P.W., 417 See Gili, J.M., 188 Avila, C., 259 See Martí, R., 190 See Fontana, A., 264, 265 See Piazzi, L., 192 See Gavagnin, M., 265, 266 See Ros, J., 192 See Iken, K., 268 See Uriz, M. J., 194 See Slattery, M., 273 See Zabala, M., 195 See Wägele, H., 197Ð276 Ballesteros, M. See Avila, C.,259 Avila, L.A. See Landsea, C.W., 421 See Fontana, A., 264 Avise, J.C., 411 See Martin, D., 190 Avon, M. See Boudouresque, C.F., 185 See Wägele, H. 197Ð276 Ayer, S.W., 259 Balls, P.W. See Laslett, R.E., 80 Ayre, D.J., 411, 412 Balser, E.J. See Johnsen, S., 319 See Billingham, M., 412 Baltzer, F. See Marchand, C., 422 See Hunt, A., 419 Balzer, W., 77 See Murray-Jones, S.E., 423 Bannister, J.L., 459 Bannon, S.M. See MacLeod, C.D., 462 Banta, G.T. See Timmerman, K., 120 B Baratech, L. See Templado, J., 194 Baratti, M., 412 Baalsrud, K., 259 Barbaresi, S. See Gherardi, F., 79 Baart, A. See Proctor, R., 54 Barber, P.H., 412 Baba, K., 259 Barbour, M.A., 259 See Okada, Y., 270 Barbour, T., 412 Babbini-Benussi, L. See Bressan, G., 185 Baretta, J.W., 50, 51 Bacci, G., 183 See Ebenhöh, W., 51 Bacescu, M., 183 See Baretta-Bekker, J.G., 51 Bach, S., 412 Baretta-Bekker, J.G., 51 Bachok, Z. See Mfilinge, P.L., 422 See Baretta, J.W., 50 Backhaus, J.O. See Schrum, C., 55 See Ebenhöh, W., 51 Baco, A.R. See Distel, D.L., 416 Barfield, M. See Holt, R.D., 419 Baden, S.P., 61Ð83, 77 Bargelloni, L. See Zane, L., 429 See Eriksson, S.P., 78 Barnes, D.K.A., 259, 412 See Hernroth, B., 79 See Wägele, H., 275 See Holmes, J.M., 79 Barnes, P.A.G. See Waycott, M., 428 See Spicer, J.I., 82 Barrales, H.L., 412 Baeyens, W. See Dehairs, F., 78 Barré, N. See Féral, J.P., 416 Bagatto, G. See Alikhan, M.A., 77 Barrett, T. See Van Bressem, M.F., 464 Bairlein, F. See Walther, G.-R., 464 Barsby, T., 259 Baker, A.J. See Luttikhuizen, P.C., 421 Bart, D., 412 Baker, B.J. See Amsler, C.D., 258 Barth, J.A. See Sotka, E.E., 425 See Bryan, P.J., 260 Bassari, A. See Akyuz, T., 77 See McClintock, J.B., 270 Basso, D., 184 See Yoshida, W.Y., 276 Bastidas, C., 412 Baker, J. See Kuiken, T., 462, Bates, N.R. See Karl, D.M., 52

466 7044_Idx.fm Page 467 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Battaglia, B. See Zane, L., 429 Bensoussan, N. See Romano, J. C., 192 Batten, S. See Beare, D.J., 459 Benzie, J.A.H., 412 See Visser, M., 55 See Bastidas, C., 412 Battershill, C. See Whalan, S., 428 See Williams, S.T., 428 Battiato, A., 184 Berg, P. See Proctor, R., 54 See Furnari, G., 187 Bergamasco, A. See Flindt, M.R., 417 Bauchot, M.L. See Whitehead, P.J.P., 195 Berggren, M. See Magnusson, K., 80 Baumert, H., 51 Berggren, P., See Hammond, P.S., 460 Baums, I.B., 412 See Anderson, L.W., 459 Baus, E., 412 Bergh, R., 260 Bava, S. See Cerrano, C., 185 Berlamont, J., 51 Bavestrello, G., 184 See Laane, R.W.P.M., 52 See Boero, F., 184 Berlinck, R.G.S. See Granato, A.C., 267 See Cattaneo-Vietti, R., 261 Berntsen, I. See Riisgård, H.U., 119 See Cerrano, C., 185 Berntsen, J. See Skogen, M.D., 55 Bazanova, L.I. See Pinegina, T.K., 424 Berridge, M.V. See Appleton, D.R., 258 Beal, A. See Pearcy, W.G., 320 Berry, S.S., 317 Beare, D.J., 459 Bertness, M.D. See Gaines, S.D., 417 See Heath, M.R., 461 Bertone, S. See Bavestrello, G., 184 Bearzi, G. See Wilson, B., 464 Bertru, G. See Bouchard, V., 413 Beaugrand, G., 459 Bevan, J.A. See Xiao, X.H., 83 See Edwards, M., 460 Bianchi, C.N. See Cerrano, C., 185 See Reid, D.G., 462 Bibiloni, M.A., 184 Becerro, M. See Turon, X., 194 Bijlsma, R. See Bockelmann, A.C., 413 Becerro, M.A., 184, 259 Billard, E., 412 See Duran, S., 416 Billen, G. See Lancelot, C., 52 See Turón, X., 274 See Wollast, R., 83 Becker, B.J., 412 Billingham, M., 412 Becker, G., See Radach, G., 54 See Ayre, D.J., 411 See Berlamont, J., 51 See Olsen, J.L., 423 See Sündermann, J., 55 Bingham, B.L., 413 See Visser, M., 55 See Kathiresan, K., 420 Becquevort, S. See Lancelot, C., 52 Birnbaum, L.S. See Ross, P.S., 463 Bedoya, J. See Guerra, A., 319 Biskupiak, J.E. See Ireland, C. 268 Beebee,T.J.C. See Walther, G.-R.,464 Bizikov, V.A., 317 Beeftink, W.G. See Huiskes, A.H.L., 419 Bjerregaard, P., 77 Behrens, D.W. See Gosliner, T.M., 266 Bj¿rge, A., 459 Behrens Yamada, S., 412 See Anderson, L.W., 459 Behringer, R.P. See Geng, J., 118 Bj¿rndal, T. See Sissener, E.H., 463 Belchier M. See Collins, M.A., 318 Black, R. See Johnson, M.S., 420 Belda, D.L. See Casas, V.M., 414 Blackford, J. See Allen, J.I., 50 Belitz, K. See Oreskes, N., 53 See Proctor, R., 54 Bell, J.D., 184 Blackford, J.C., 51 Bell, S.S. See Brooks, R.A., 413 See Allen, J.I., 50 Bellan, G., 184 Blackman, A.J. See Jongaramruong, J., 268 Bellan-Santini, D., 184 Blackmore, G., 77 Bellwood, O., 117 See Rainbow, P.S., 81 See Si, A., 425 Blair, N.E., 117 Belousova, N.P. See Stepanjants, S.D., 426 Blair, S.M. See Littler, M.M., 190 Belsher, T., 184 Blanc, J.J., 184 Ben Maiz, N. See Boudouresque, C.F., 185 Blasco, J., 77 Bencini, A. See Gherardi, F., 79 Blaxter, K.L. See Hamilton, W.J., 460 Bengtsson, B.-E. See Gräslund, S., 79 Blier, P.U. See Breton, S., 413 Benke, H. See Hammond, P.S., 460 Blochmann, F., 260 Benkendorff, K., 260 Blunt, J.W., 260 Bennett, M.E. See Kuiken, T., 462 Boates, J.S. See Wilson, A.B., 428 Bennett, P.M. See Jepson, P.D., 461 Böck, P., 260 Benson, M.R. See Norton, T.A., 423 Bockelmann, A.C., 413 Benson, S. See Scholin, C.A., 463 Boehlert, G.W. See Sponaugle, S., 425

467 7044_Idx.fm Page 468 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Boero, F., 184 Boyle, P.R., 318, 459 Bohonak, A.J., 413 See Daly, H.I., 318 Boisselier-Dubayle, M.C., 413 Bradbury, I.R., 413 Boisset, F. See Boudouresque, C.F., 185 Braitseva, O.A. See Pinegina, T.K., 424 Bokhorst, M., 51 Bram, J.B., 413 See de Vries, I., 51 Bramanti, L., 185 See Los, F.J., 53 See Santangelo, G., 193 See OSPAR, 54 Brander, K.M. See Beaugrand, G., 459 Bolding, K. See Burchard, H., 51 Brandt, P.W. See Chiarandini, D.J., 78 Boletzky, S.v., 318 Bray, J.T. See Weinstein, J.E., 82 See Jereb, P., 319 Breeman, A.M. See Engelen, A.H., 416 Bolis, L. See Rankin, J.C., 81 Bremer, J.B. See Benkendorff, K., 260 Boltaña, S. See Macaya, E.C., 421 Brenowitz, M. See Van Holde, K.E., 82 Bonaventura, C. See Bourget, E., 77 Bressan, G., 185 Bonaventura, J. See Bourget, E., 77 Breton, S., 413 Bonsdorff, E. See Böstrom, C., 413 Bridges, T.S. See Levin, L.A., 421 Boon, J. See Proctor, R., 54 Brierley, A.S. See Allcock, A.L., 411 Boore, J. See Wollscheid-Lengeling, E., 276 Britayev, T.A. See Martin, D., 190 Boorman, P. See Hulme, M., 461 Brockmann, U., 51 Booton, G.C. See Parker, P.G., 423 Brodie, G. See Wägele, H., 275 Borchers, D.L. See Hammond, P.S., 460 Brodie, G.B., 260 Borg-Neczak, K. See Tjälve, H., 82 Brodie G.D. See Klussmann-Kolb, A., 269 Born, E., 260 Bronto, S. See Carey, S., 414 Brooks, R.A., 413 Borowitzka, M.A., 413 Brorström-Lundén, E. See Magnusson, K., 80 Borrell, A. See Aguilar, A., 459 Brouwer, M., 77 Borum, J., 413 Brown, A.C., 117 Bosence, D.W.J., 184 See Trueman, E.R., 120 Böstrom, C., 413 Brown, F. See Heath, M.R., 461 See Olsen, J.L., 423 Brown, G.H. See Thompson, T.E., 273 Bot, P. See Radach, G., 54 Brown, K. See Sear, C., 463 See Visser, M., 55, Brown, R. See de Gruy, M., 318 Botsford, L.W. See Gerber, L.R., 417 Brown, W. Wollscheid-Lengeling, E., 276 Bouchard, V., 413 Bruford, M.W. See Baus, E., 412 Bouchet, P., 260 Brundage, W.L. See Roper, C.F.E., 321 Bouchon, C. See Harmelin, J.G., 188 Brunskill, G.J. See Alongi, D.M., 411 Boudouresque, C.F., 184, 185 Bruun, A.F., 318 See Augier, H., 183 Bryan, G.W., 78 See Sala, E., 193 Bryan, P.J., 260 Boudreau, B.P., 117 See McClintock, J.B., 270 See Choi, J., 117 See Yoshida, W.Y., 276 See Dorgan, K.M., 85Ð121, 118 Bryan, S.E., 413 See Johnson, B.D., 118 Buckley, R.M. See Shaffer, J.A., 425 See Jumars, P.A., 119 Buffoni, G. See Abbiati, M., 182 See Meysman, F.J.R., 119 Bulleri, F., 413 See Mulsow, S., 119 Bullough, L.W. See Barnes, D.K.A., 259 Boudry, P. See Lapègue, S., 421 See Wägele, H., 275 Boughriet, A. See Nassrallah-Aboukais, N., 80 Burchard, H., 51 Boulding, E.G. See Kyle, C.J., 421 Burgess, J.G. See Armstrong, E., 259 See Snyder, T.P., 425 Burgess, R.M. See Voparil, I.M., 120 Bourgeois, J. See Pinegina, T.K., 424 Burghardt, I., 260 Bourget, E., 77 Bürgin-Wyss, K., 260 Bourillon-Moreno, L. See Pfeiler, E., 424 Burgoyne, D. L., 260 Bourque, B.J. See Steneck, R.S., 426 Burke, C.M. See Hodson, S.L., 419 Bousfield, E.L., 117 Burkholder, J.M. See Harvell, C.D., 461 Boutet, I. See Lapègue, S., 421 Burn, R., 260 Boyd, I.L, 459 Burns, F. See Beare, D.J., 459 Boyd, K.G. See Armstrong, E., 359 Burns, J.J. 459 Boyle, J.S. See Gates, W.L., 52 Burns, M.M. See Yoder, A.D., 429

468 7044_Idx.fm Page 469 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Burrows, M.T. See Southward, A.J., 463 Carpine, C., 185 Burton, H.R. See Edgar, G.J., 416 Carr, M.H., 414 Burton, R.S. See Edmands, S., 416 See Caley, M.J., 413 See Hellberg, M.E., 418 See Shanks, A.L., 425 Buschbaum, C., 413 Carranza, S., 414 Buschmann, A.H. See Macaya, E.C., 421 Carrier, G. See Normandin, L., 80 Bushing, W.W., 413 Carvajal-Rodriguez, A. See Pérez-Figueroa, A., 424 Busman, M. See Scholin, C.A., 463 Carvalho, G.R., 414 Butt, A.M., 78 See Piertney, S.B., 424 Butterworth, R.F. See Normandin, L., 80 See Porter, J.S., 424 Butzke, D., 260 Casas, V.M., 414 Buznikov, G.A., 260 Caselle, J.E. See Swearer, S.E., 426 Byrne, M. See, Colgan, D.J., 414 Casey, J. See O'Brien, C.M., 462 Castaing, P. See Radach, G., 54 C Castedo, L., 260 See Jiménez, C., 268 Caballero, A. See Pérez-Figueroa, A., 424 See Quiñoá, E., 271 Cabello-Pasini, A. See Muñiz-Salazar, R., 422 Castelluccio, F. See Gavagnin, M., 265, 266 Cabioch, J., 185 Castiello, D., 261 Cacciapuotti, G. See Porcelli, M., 271 Castilla, J.C., 414 Cacho, E. See Hernández, M., 461 Castro, J.J., 414 Cadée, G.C., 413 Castro, L.R. See Colgan, D.J., 414 Caffa, B. See Boero, F., 184 Catafau, E. See Canals, M., 185 Caforio, G. See Abbiati, M., 182 Cattaneo-Vietti, R., 261 Calabrese. G. See Fontana, A., 264 See Bavestrello, G., 184 Calado, G., 260 See Cerrano, C., 185 See Gavagnin, M., 265 See Gavagnin, M., 266 Caldeira, K. See Stephens, B.B., 55 Cavaliere, P. See Fontana, A., 264 Caley, M.J., 413 Cavanaugh, C. See Distel, D.L., 416 California Department of Fish and Game, 413 Cebrian, D., 459 Calsbeek, R., 414 Cebrian, E., 185 Calvert, E. See Olsen, J.L., 423 Cebrian, J., 414 Calvo, S. See Piazzi, L., 192 Ceccaldi, H.J. See Martin, J.-L.M., 80 Camp, J. See Masó, M., 422 Ceccherelli, G. See Piazzi, L., 192 Campbell, A.K. See Herring, P.J., 319 Ceccherelli, V.U. See Mistri, M., 191 Campillo, O.A. See Valdés, A., 274 Cecchi, E. See Piazzi, L., 192 Camus, P.A., 414 Cedhagen, T., 261 Canals, M., 185 Censky, E.J., 414 See Cebrian, E., 185 Cerenius, L. See Söderhäll, K., 82 Canfield, D.E., 78 Cerrano, C., 185 Cantwell, M.G. See Voparil, I.M., 120 See Bavestrello, G., 184 Capaccioni, R. See Templado, J., 194 Cerruti, A., 186 Capelli, R. See Drava, G., 78 Cervera, J.L. See Grande, C., 267 Carballo, J.L. See Megina, C., 270 See Megina, C., 270 Carballo, M. See Cruz, R., 415 See Pola, M., 271 Carbone, M. See Gavagnin, M., 265 See Wägele, H., 275 See Mollo, E., 270 Chaga, O., 78 Carbonell, J., 185 Chamberlain, Y.M. See Woelkerling, W.J., 195 Cardenas, L. See Martinez, E.A., 422 Chambers, R.J., 414 Carefoot, T.H., 260 Chambers, S.J. See Johnson, M.P., 419 Carey, S., 414 Chan, H.M., 78 Carletti, E. See Santangelo, G., 193 Chan, J.C.L., 414 Carlini, D.B., 318 Chan, K.-S. See Stenseth, N., 463 See Seibel, B.A., 321 Chandler, H.W., 117 Carlton, J.T., 414 Chapman, A.S. See Buschbaum, C., 413 See Wonham, M.J., 428 Chapman, C.J. See Field, R.H., 79 Carmeli, S. See Gillor, O., 266 Chapman, G., 117 Carmely, S., 260 See Bulleri, F., 413 Carole, M. See Kennedy, S., 461 See Underwood, A.J., 427

469 7044_Idx.fm Page 470 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Chapman, R.W. See Ball, A.O., 412 See Ferdeghini, F., 186 Charbonnel, E. See Sartoretto, S., 193 See Piazzi, L., 191, 192 Charlton, T.S. See De Nys, R., 263 Cirik, S. See Boudouresque, C.F., 185 See Rogers, C.N., 271 Clapham, P.J. See Wiley, D.N., 464 Charnock, H., 51 Clardy, J. See Dumdei, E.J., 263 Chauvaud, L. See Grall, J., 118 See Gustafson, K., 267 Chauvet, C., 186 See Hellou, J., 267 Chavez, F.P. See Scholin, C.A., 463 See Ireland, C., 268 Chazottes, V., 186 See Tischler, M., 274 Chen, Z., 117 Clark, R.B., 117 Cheng, J.F. See Arimoto, H., 258 Clarke, A. See Wells, M. J., 322 Chenuil, A. See Féral, J.P., 416 Clarke, K.R. See Stebbing, A.R.D., 463 See Le Gac, M., 421 Clarke, M.R. See Gales, R., 319 Cherel, Y., 318 Claustre, H. See Moline, M.A., 462 Chernoff, H. See Keough, M.J., 420 Clement, E. See Geng, J., 118 Chess, J.R. See Conlan, K.E., 414 Cliff, G. See Smale, M.J., 321 Chia, F.S. See Gibson, G.D., 266 Cline, E.I. Simpson, J.S., 273 See Martel, A., 422 Clubb, J.A. See Herdman, W.A., 267 Chiantore, M. See Cattaneo-Vietti, R., 261 Cobolli, M. See De Matthaeis, E., 415 Chiarandini, D.J., 78 Cocito, S. See Ferdeghini, F., 186 Childress, J.J. See Seibel, B.A., 321 Cockeron, P.J., 460 Chintiroglou, H., 186 Coelho, H., 414 Choat, J.H. See Kingsford, M.J., 420 Coelho, M.M. See Coelho, H., 414 Choi, J., 117 Coleman, J.E. See Dumdei, E.J., 263 See Boudreau, B.P., 117 Colgan, D.J., 414 Chong, V.C. See Alongi, D.M., 411 Colijn, F. See Berlamont, J., 51 Choudhary, M.I. See Tischler, M., 274 See Laane, R.W.P.M., 52 Christensen, J.H. See Timmerman, K., 120 See Radach, G., 54 Christie, H. See Fredriksen, S., 417 See Visser, M., 55 See Olsen, J.L., 423 Coll, J., 186 Chuang, E. See Distel, D.L., 416 Collet, A. See Hammond, P.S., 460 Chun, C., 318 Collin, R., 414 Ciavatta, M.L., 261 Collins, M.A., 277Ð322, 318 See Cimino, G., 261 See Boyle, P.R., 318 See Fontana, A., 264 See Daly, H.I., 318 See Iken, K., 268 See Manzo, E., 269 See Piertney, S.B., 320 Cicogna, F. See Cerrano, C., 185 See Vecchione, M., 321 See Russo, G.F., 193 See Villanueva, R., 322 See Santangelo, G., 193 Colls, P.W. See Bryan, S.E., 413 Cimino, G., 261, 262 Colman, J.G. See Thompson, T.E., 273 See Avila, C., 259 Colomer, P. See Gili, J.M., 188 See Castiello, D., 261 Colson, I., 414 See Ciavatta, M.L., 261 Colwell, R.R. See Harvell, C.D., 461 See De Petrocellis, L., 263 Coma, R., 186 See Fontana, A., 264, 265 See Linares, C., 189 See García-Gómez, J.C., 265 See Llobet, I., 190 See Gavagnin, M., 265, 266 See Ribes, M., 192 See Iken, K., 268 Conde-Padín, P. See Cruz, R., 415 See Manzo, E., 269 Conlan, K.E., 414 See Marín, A., 270 Connor, R.C. See Cockeron, P.J., 460 See Mollo, E., 270 See Mann, J., 462 See Porcelli, M., 271 Constantino, R.F. See Edmonds, J., 118 See Puliti, R., 271 Constantino, V., 262 See Spinella, A., 273 Convey, P. See Walther, G.-R., 464 See Zubía, E., 276 Cook, A. See Bryan, S.E., 413 Cinelli, F. See Acunto, S., 182 Cook, J., 117 See Airoldi, L., 183 Cook, L.G., 414 See Boudouresque, C.F., 185 Coombs, D.S., 414

470 7044_Idx.fm Page 471 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Copp, B.R. See Appleton, D.R., 258 Cushing, J.M. See Edmonds, J., 118 See Blunt, J.W., 260 Cutter, G.R.J. See Diaz, R.J., 118Cutignano, A. See Coppejans, E., 186 Fontana, A., 264 Corbera, J., 186 Corbett, D. See Steneck, R.S., 426 Cordaro, J. See Scholin, C.A., 463 D Corey, S. See Locke, A., 421 Corkill, J. See Pinn, E.H., 424 Daguin, C. See Billard, E., 412 Cormaci, M., 186 Dalby, D.H., 415 See Battiato, A., 184 Daly, H.I., 318 See Boudouresque, C.F., 185 See Boyle, P.R., 318 See Furnari, G., 187 D'Ambrosio, M. See Guerriero, A., 267 Corpe, H.M. See Thompson, P.M., 463 Dame, R.F., 415 See Cossu, A. See Giaccone, G., 188 Damm, P. Delhez, E.J.M., 51 See Radach, G., 54 Costa, F.O., 415 See Sündermann, J., 55 See Coelho, H., 414 See Visser, M., 55 Costa, M.H. See Coelho, H., 414 Dana, J.D., 415 See Costa, F.O., 415 Danielssen, D. See Radach, G., 54 Costas, E. See Hernández, M., 461 See Visser, M., 55 Cotzias, G.C. See Mena, I., 80 Dantart, L. See Linares, C., 189 Cotzias, J.C., 78 See Martin, D., 190 Coulom, C., 262 Dantu, P., 118 Coulson, S.J., 415 D'Archino, R. See Piazzi, L., 192 Couper, J., 78 Darrock, D.J. See Baus, E., 412 Coveñas, R. See García-Gómez, J.C., 265 Darvell, B.W. See Rudman, W.B., 272 Covey, C. See Gates, W.L., 52 da Silva, A.M. See Dee, D.P., 51 Cowen, R.K., 415 da Silva, J. See Domaneschi, O., 416 See Sponaugle, S., 425 da Silva, J.J.R.F., 78 Cox, C.B., 415 Dassi, P. See Hernandez, E.H., 79 Cox, E.F. See Jokiel, P.L., 420 Dave, G. See Magnusson, K., 80 Coyer, J.A., 415 Davenport, J., 415 See Diekmann, O.E., 416 Davies, A.M. See Lynch, D.R., 53 See Olsen, J.L., 423 Davies-Coleman, M.T., 262 Crampton, D.M. See Thompson, T.E., 274 See McClintock, J.B., 270 Creach, V. See Bouchard, V., 413 Davis, A.J. 460, Crespo, E. See Van Bressem, M.F., 464 Davis, A.R. See Ayre, D.J., 411 Crick, H.Q.P. See Learmonth, J.A., 431Ð464 See Benkendorff, K., 260 Crisp, D.J., 415 Davis, G.M. See Wilke, T., 428 See Bourget, E., 77 Davis, J.L.D., 415 Crisp, M.D. See Cook, L.G., 414 Davis, J.M., 78 Crispino, A. See Avila, C., 259 Davolos, D. See De Matthaeis, E., 415 See Cimino, G., 261 Daw, T.M. See Xavier, J.C., 322 See Gavagnin, M., 265, 266 Day, J.H., 118 See Spinella, A., 273 Dayrat, B., 263 See Zubía, E., 276 Dayton, P.K., 415 Cronin, G., 262 See Tegner, M.J., 426 Croudace, I. See Boudreau, B.P., 117 See Vetter, E.W., 427 Crowe, T.P. See Thompson, R.C., 427 Dease, C.G. See Gates, W.L., 52 Cruz, F. See Pérez-Figueroa, A., 424 De Almeida-Epifanio, A. See Gavagnin, M., 266 Cruz, R., 415 De Caro, S. See Izzo, I., 268 Culotta, V.C. See Luk, E.E., 80 Dee, D.P., 51 Cun-heng, H. See Gustafson, K., 267 Defran, R.H. See Wells, R.S., 464 Cunningham, C.W. See Govindarajan, A.F., 417 De Freitas, J.C. See Granato, A.C., 267 See Grosberg, R.K., 418 De Giulio, A. See Cimino, G., 261 See Wares, J.P., 427 Degnan, B.M. See Wörheide, G., 429 Cupka, D.M., 318 de Goede, E. See Delhez, E.J.M., 51 Currie, V. See Dayton, P.K., 415 Degraer, S. See Vandendriessche, S., 427 Currin, C. See Moseman, S.M., 422 de Groot, A. See Jansen, B.J.M., 268

471 7044_Idx.fm Page 472 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

de Gruy, M., 318 Diaz, R.J., 118 Dehairs, F., 78 Di Beneditto, A..P. See Van Bressem, M.F., 464 De Haro, A. See Munilla, T., 191 Di Cola, G. See Abbiati, M., 182 de Keyzer, R.G. See Ponder, W.F., 271 Dieckmann, R. See Piatkowski, U., 320 de Kok, J. See Proctor, R., 54 Diekmann, O.E., 416 de Kok, J.M., See Delhez, E.J.M., 51 See Coyer, J.A., 415 Delahayes, G. F., 78 Dietz, R. See Laidre, K.L., 462 Deleersnijder, E. See Proctor, R., 54 d'Ippolito, G. See Fontana, A., 264 Delefosse, T. See Yoder, A.D., 429 Di Martino, V. See Marino, G., 190 De Leo, A. See Giaccone, G., 188 Di Marzo, V. See Cimino, G., 261 De Lera, A.R. See Alvarez, R., 258 See De Petrocellis, L., 263 Delhez, E. See Proctor, R., 54 See Marín, A., 270 Delhez, E.J.M., 51 Discalzi, G. See Hernandez, E.H., 79 Della Sala, G. See Fontana, A., 264 Distel, D.L., 416 DeLong, R. See Scholin, C.A., 463 Dittel, A.I. See Wehrtmann, I.S., 428 De los Santos, D.B. See Horgen, F.D., 267 Dixon, P. See Alongi, D.M., 411 De Maio, L. See Bramanti, L., 185 Djellouli, A.S. See Piazzi, L., 192 DeMaster, D.J. See Blair, N.E., 117 Djerassi, C. See Whiters, N.W., 275 DeMaster, D.P. See Tynan, C.T., 463 Doake, C.S.M. See Vaughan, D.G., 464 De Matthaeis, E., 415 Dobson, A.P. See Harvell, C.D., 461 De Medeiros, E.F., 263 Docimo, T. See Gavagnin, M., 265 Deming, J.W. See Schmidt, J.L., 120 Dodd, J.R. See Alexander, R.R., 117 Demunck, W. See Huiskes, A.H.L., 419 Dohl, T.P. See Wells, R.S., 464 de Munck, W. See Koutstaal, B.P., 420 Domaneschi, O., 416 De Napoli, A. See Gavagnin, M., 265 Domènech, A. See Fontana, A., 264 Denizot, M. See Boudouresque, C.F., 185 Domingo, M., 460 Dennis, B. See Edmonds, J., 118 Donald, K.M., 416 Denno, R.F., 415 Donovan, D.T. See Young, R.E., 322 See Peterson, M.A., 424 Dore, J.E. See Karl, D.M., 52 De Nys, R., 263 Dorgan, K.M., 85Ð121, 118 See Rogers, C.N., 271, 272 See Boudreau, B.P., 117 De Pellegrini, R. See Drava, G., 78 See Jumars, P.A., 119 De Petrocellis, L., 263 Doty, D.C. See Shaffer, J.A., 425 Depledge, M.H. See Baden, S.P., 77 Doty, M.S. See Littler, M.M., 190 See Bjerregaard, P., 77 Doucette, G.J. See Scholin, C.A., 463 de Queiroz, A., 415 Dounas, C. See Chintiroglou, H., 186 De Riccardis, F. See Izzo, I., 268 Doutriaux, C.M. See Gates, W.L., 52 De Rosa, S. See Castiello, D., 261 Doyle, T.W. See Krauss, K.W., 421 See Cimino, G., 261, 262 Drach, R.S. See Gates, W.L., 52 De Sanctis, B. See Granato, A.C., 267 Drake, D.E. See Sherwood, C.R., 120 de Silva, E.D. See Faulkner, D.J., 264 Drava, G., 78 Desharnais, R.A. See Edmonds, J., 118 Drazen, J.C., 318 De Stefano, S. See Castiello, D., 261 Drent, J. See Luttikhuizen, P.C., 421 See Cimino, G., 261, 262 Dring, M.J., 186 Desrosiers, G. See Breton, S., 413 D'Souza, L. See Fontana, A., 264 de Swart, R.L., 460 Duarte, C.M. See Cebrian, J., 414 Dethier, M.N., 186, 415 Duchene, J.-C. See Hollertz, K., 118 DeVantier, L.M., 415 Ducklow, H.W. See Fasham, M.J.R., 51 Devi, M., 78 Ducrotoy, J.P., 469 See Fingerman, M., 79 Duda, T. See Palumbi, S.R., 423 Devine, D.V., 78 Duda, T.F., 416 De Vogelaere, A. See Scholin, C.A., 463 Dudley, J. See Censky, E.J., 414 de Vries, I., 51 Duffy, J.E., 416 See Michielsen, B., 53 Dufresne, F. See Breton, S., 413 See OSPAR, 54 Dufty, S. See Ayre, D.J., 411 See Peeters, J.C.H., 54 Dugan, J.E. See Bram, J.B., 413 de Vries, M.B., 51 See Lastra, M., 119 Diaz, D. See Linares, C., 189 Duhamel, G. See Cherel, Y., 318 Diaz, J.M., 415 Duignan, P.J. See Van Bressem, M.F., 464

472 7044_Idx.fm Page 473 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Duin, R.N.M. See de Vries, I., 51 Engel, C. See Billard, E., 412 Duinker, J.C. See Wollast, R., 83 Engelen, A.H., 416 Dumas, F. See Delhez, E.J.M., 51 Engman, J. See Jorhem, L., 79 Dumdei, E.J., 263 Epstein, P.R., See Harvell, C.D., 461 See Burgoyne, D. L., 260 Erdmann, M.V. See Barber, P.H., 412 See Faulkner, D.J., 264 Eriksen, A. See Stipa, T., 55 See Garson, M.J., 265 Eriksson, S.P., 78 Duncan, M.W. See De Nys, R., 263 See Baden, S.P., 61Ð83, 77 Dunn, J. See Heath, M.R., 461 See Spicer, J.I., 82 Dupont, L., 416 Erkan, B.M. See Akyuz, T., 77 Dupont, S. See Féral, J.P., 417 Erlandson, J.M. See Steneck, R.S., 426 DuPreez, H.H. See Sanders, M.J., 81 Ersoy, S. See Altinok, Y., 411 du Preez, H.H. See Steenkamp, V.E., 82 Eschricht, D.F., 319 Duran, J., 118 Estes, J.A. See Carr, M.H., 414 Duran, S., 416 See Steneck, R.S., 426 Durfort, M. See Avila, C., 259 Estevez, E.D., 416 Duval, C. See Harmelin, J.G., 188 Estoup, A. See Duran, S., 416 Dyer, K.R. See Charnock, H., 51 Evans, G.T., 51 See Howarth, M.J., 52 Evans, J.P. See Bryan, S.E., 413 Evans, K. See Van Bressem, M.F., 464 Evans, P.G.H., 460 E See Reid, J.B., 462 Evans, T.J., 263 Eales, N.B., 263 Evertsen J. See Burghardt, I., 260 Early, G.A. See Geraci, J.R., 460 Ebel, R., 263 See Proksch, P., 271 F See Thoms, C., 274 Ebenhöh, W., 51 Fabricius, K.E. See Bastidas, C., 412 See Baretta, J.W., 50 Fahey S. See Gavagnin, M., 265 See Baretta-Bekker, J.G., 51 Fahey, S.J., 263 Ebersbach, A., 319 Fairweather, P.G. See Underwood, A.J., 427 Ebisawa, Y. See Miyamoto, T., 270 Fakhr, I. See Fontana, A., 264 Eckert, G.L., 416 Fam, M.A. See Santamarina, J.C., 119 See Grantham, B.A., 417 Famulok, M., 263, 264 Eckman, J.E. See Nowell, A.R.M., 119 Farmer, A.S.D., 78 Edesa, S. See Levin, L.A., 119 Fasham, M.J.R., 51 Edgar, G.J., 416 See Popova, E.E., 54 Edlinger, K., 263 Fatt, P., 78 Edmands, S., 416 Fattorusso, E. See Constantino, V., 262 Edmonds, J., 118 Fauchald, K., 118 Edmunds, H. See Howarth, M.J., 52 Faulkner, D.J., 263 Edmunds, M., 263 See Abramson, S.N., 258 Edrada, R.A. See Proksch, P., 271 See Davies-Coleman, M.T., 262 Edwards, K.R. See Proffitt, C.E., 424 See Ireland, C., 268 Edwards, M., 460 See Kassühlke, K.E., 268 See Beare, D.J., 459 See Kubanek, J., 269 See Reid, D.G., 462 See McClintock, J.B., 270 Edwards, P.B. See Tegner, M.J., 426 See Okuda, R.K., 271 EEA, 460 See Thompson, J.E., 273 Eigenheer, A., 51 Faust, S.D., 78 Ekelund, R. See Magnusson, K., 80 Feldmann, J., 186 Elder, H.Y., 118 Feller, I.C., 416 See Hunter, R.D., 118 Feng, S., Zhao, L., 56 Elderfield, H., 78 See Wei, H., 56 Ellis, J.R. See Perry, A.L., 462 Fenical, W., 264 Emslie, M.J. See Jones, G.P., 420 See Cronin, G., 262 Endoh, M. See Obata, A., 53 See Spinella, A., 273 Engdahl, S., 78 See Whiters, N.W., 275

473 7044_Idx.fm Page 474 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Féral, J.P., 416, 417 Foyn, L. See Radach, G., 54 See Le Gac, M., 421 See Visser, M., 55 Ferdeghini, F., 186 Franc, A., 265 Ferguson, C.A. See Hettiaratchi, D.R.P., 118 Franco, J. See Hernández, M., 461 Ferguson, S.H., 460 Francois-Carcaillet, F. See Boudreau, B.P., 117 Fernandes, R. See Reis, C.S., 320 See Choi, J., 117 Fernandez Ovies, C.L., 264 Francour, P., 187 Fernández-Muñoz, R. See García-Raso, J.E., 187 See Perez, T., 191 Ferreira, A.G. See Granato, A.C., 267 See Sartoretto, S., 193 Ferreira, J. See Diekmann, O.E., 416 Franke, H.-D., 417 See OSPAR, 54 See Gutow, L., 418 Ferrer, E., 187 Frankel, L., 118 Fialkowski, W., 78 Fransz, H.G., 51 See Rainbow, P.S., 81 Fraser, J.G. See Heath, M.R., 461 Fiedler, P.C., 460 Fraser, K.P.P. See Barnes, D.K.A., 412 Field, R.H., 79 Fraser, S. See Heath, M.R., 461 Figuerola, J. See Green, A.J., 417 Fraser, W.R., 460 Filippova, A.V. See Tzetlin, A.B., 120 Fratini, S., 417 Finckh, A.E., 187 Frazer, T.K. See Moline, M.A., 462 Findlay, J.A., 264 Fredj, G., 187 Finer, J.S. See Ireland, C., 268 See Vaissière, R., 194 Fingerman, M., 79 Fredriksen, S., 417 See Devi, M., 78 Fretter, V., 265 Fiorino, M. See Gates, W.L., 52 Frick, C., 417 Fischer, H., 264, 319 Friedrich, A.B. See Hentschel, U., 267 See Perrier, R., 271 Frohse, A. See Sündermann, J., 55 Fischer, J.C. See Nassrallah-Aboukais, N., 80 See Visser, M., 55 Fischer, P., 319 Fromentin, J.-M. See Walther, G.-R., 464 Fishelson, Z. See Gillor, O., 266 FRS, 460 Fisher, E.C. See Johnsen, S., 319 Fu, X., 265 Fisher, L. R., 264 Fuenzalida, S. See Mena, I., 80 Fitton, D.M. See Johnson, M.P., 419 Fuerst, P.A. See Parker, P.G., 423 Flach, E.C., 417 Fukunda, J., 79 Flemming, N.C. See Prandle, D., 54 Fuller, G.B., 460 Flindt, M.R., 417 Furnari, G., 187 Flores-Campana, L.M. See Paez-Osuna, F., 81 See Battiato, A., 184 Flos, J. See Pascual, J., 191 See Cormaci, M., 186 Flowers, A.E. See Dumdei, E.J., 263 Furukawa, Y. See Boudreau, B.P., 117 See Garson, M.J., 265 Fusetani, N., 265 Flynn, J.J. See Yoder, A.D., 429 See Hirota, H., 267 Foale, S.J., 264 Fushimi, K., 417 Fodrie, F.J. See Becker, B.J., 412 Fontana, A., 264, 265 See Avila, C., 259 G See Cimino, G., 261, 262 See Iken, K., 268 Gaggero, L. See Cattaneo-Vietti, R., 261 Forcada, J. 460 Gaines, S. See Roughgarden, J., 424 See Gilmartin, W.G., 460 Gaines, S.D., 417 Ford, S.E. See Lafferty, K.D., 462 See Allison, G.W., 411 Forder, C. See Moseman, S.M., 422 See Gerber, L.R., 417 Förlin, L. See Magnusson, K., 80 See Kinlan, B.P., 420 Forstner, M.R. See Raxworthy, C.J., 424 See Lubchenco, J., 421 Fortuna, C.M. See, Wilson, B., 464 See Siegel, D.A., 425 Fortuna, J.L. See Cowen, R.K., 415 Gaino, E. See Bavestrello, G., 184 Foslie, M.H., 187 Galbraith, H. See Parmesan, C. 462 Foster, B.A. See Stevens, L.M., 426 Galera, J. See Turon, X., 194 Fountain, A.G., 118 Gales, R., 319 Fourqurean, J.W. See Romero, L.M., 424 Gamble, J.C. See Radach, G., 54 Fox, C.J. See O'Brien, C.M., 462 Gamulin-Brida, H., 187

474 7044_Idx.fm Page 475 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Garboczi, E.J. See Schlangen, E., 120 Gellers-Barkman, S. See OSPAR, 54 Garces, E. See Masó, M., 422 See Kelly-Gerreyn, B.A., 52 Garcia, A. See Gili, J.M., 188 Gemballa, S., 266 Garcia, L. See Corbera, J., 186 Geng, J., 118 Garcia, P. See Lapègue, S., 421 Genner, M.J. See Sims, D.W., 463 García, F.J. See Gavagnin, M., 265 Gentil, F. See Jolly, M.T., 420 García-Carrascosa, M. See Templado, J., 194 Geraci, J.R., 460 García-Gómez, J.C., 265 Gerber, G.B., 79 See Megina, C., 270 Gerber, L.R., 417 See Ortea, J., 271 Gerhardt, G.A. See Moore, P., 80 García-Raso, J.E., 187 Gerhardt, L. See Baden, S.P., 77 García-Rodríguez, M., 187 Gerritsen, H. See Delhez, E.J.M., 51 Garcia-Rubies, A., 187 See Proctor, R., 54 See Ballesteros, E., 184 Gerrodette, T. See Dayton, P.K., 415 See Coll, J., 186 Geyer, L. See Palumbi, S.R., 423 See Corbera, J., 186 Gherardi, F., 79 See Zabala, M., 195 Ghiselin, M. See Gavagnin, M., 265 Gardiner, B.S. See Boudreau, B.P., 117 Ghiselin, M.T. See Cimino, G., 262 See Johnson, B.D., 118 See Faulkner, D.J., 264 Gardiner, P.F. See Normandin, L., 80 Giaccone, G., 188 Garrabou, J., 187, 188 See Marino, G., 190 See Ballesteros, E., 183 Giannini, F. See Santangelo, G., 193 See Marschal, C., 190 Gibson, G.D., 266 Gilbert, F.J. See Allen, J.I., 50 See Perez, T., 191 Gili, J.M., 188 See Sala, E., 193 See Coma, R., 186 See Torrents, O., 194 See Llobet, I., 190 Garreau, P. See Hoch, T., 52 See Ribes, M., 192 See Proctor, R., 54 See Ros, J., 192 Garson, M.J., 265 Gillete, R., 266 See Dumdei, E.J., 263 Gillor, O., 266 See Fahey, S.J., 263 Gilmartin, W.G., 460 See Simpson, J.S., 273 Gimenez, F. See Fontana, A., 264 Gasco, N. See Cherel, Y., 318 See Cimino, G., 262 Gaskin, D.E. See Read, A.,462, Gimenez, L. See Yannicelli, B., 121 Gaspar, R. See Wilson, B., 464 Ginsborg, B.L. See Fatt, P., 78 Gaspari, G. See Dee, D.P., 51 Ginsburg, D.W., 266 Gates, W.L., 52 Ginsburg, R.N. See James, N.P., 189 Gautier, Y.V., 188 Giordano, A., 266 Gavagnin, M., 265, 266 Giribet, G. See Duran, S., 416 See Avila, C., 259 See Lindgren, A.R., 320 See Ciavatta, M.L., 261 Gleckler, P.J. See Gates, W.L., 52 See Cimino, G., 261, 262 Gliddon, C.J. See Goldson, A.J., 417 See De Petrocellis, L., 263 Glor, R.E., 417 See Fontana, A., 264 Glud, R.N. See Koenig, B., 119 See Iken, K., 268 Glynn, P.W., 417 See Manzo, E., 269 Goetz, G. See Becerro, M.A., 259 See Mollo, E., 270 See Horgen, F.D., 267 See Pani, A., 271 Gofas, S. See Boisselier-Dubayle, M.C., 413 See Porcelli, M., 271 Goffredi, S.K. See Drazen, J.C., 318 See Puliti, R., 271 Goffredo, S., 417 See Racioppi, R., 271 Goldenberg, C., 118 See Zubía, E., 276 Goldhirsch, I. See Goldenberg, C., 118 Gavin, C.E., 79 Goldson, A.J., 417 Gaylord, B. See Gaines, S.D., 417 Goldsworthy, S.L., 319 See Siegel, D.A., 425 Gómez-Garreta, A. See Ferrer, E., 187 Gekeler, J. See Berlamont, J., 51 Gomulkiewicz, R. See Holt, R.D., 419 See Radach, G., 54 González, L.M. See Hernández, M., 461 Geller, J.B. See Carlton, J.T., 414 Gooch, J.L. See Snyder, T.P., 425

475 7044_Idx.fm Page 476 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Goodman, S.M. See Yoder, A.D., 429 Grzebielec, R. See Arkhipkin, A.I., 459 Gopichand, Y., 266 Guerra, A., 319 See Schmitz, F.J., 272 See Sanchez, P., 321 Gordillo, S. See Adami, M.L., 411 See Villanueva, R., 322 Gordon, J.E., 118 Guerriero, A., 267 See Cook, J., 117 See Cimino, G., 262 Gorodezky, L.A. See Seibel, B.A., 321 Guiart, J., 267 Gosliner, T.M., 266, 267 Guichard, F., 418 See Johnson, R.F., 268 Guillaud, J.-F., 52 See Pola, M., 271 Guillén, J. See Palanques, A., 191 Gosse, P. See Agoumi, A., 50 Guiñez, R. See Castilla, J.C., 414 Got, H., 188 Gulland, F. See Scholin, C.A., 463 Goti, E. See Baratti, M., 412 Gunter, K.K. See Gavin, C.E., 79 Govindarajan, A.F., 417 Gunter, T.E. See Gavin, C.E., 79 Grabowsky, G. See Palumbi, S.R., 423 Guo, Y.W. See Gavagnin, M., 265 Gracia, V. See Zabala, M., 195 See Manzo, E., 269 Grader, A.S. See Boudreau, B.P., 117 See Mollo, E., 270 Graeve, M. See Kattner, G., 268 Gustafson, K., 267 Graham, A. See Fretter, V., 265 Gutiérrez-Rodríguez, C., 418 Graham, M.H. See Steneck, R.S., 426 Gutow, L., 418 Grall, J., 118 See Buschbaum, C., 413 Granato, A.C., 267 See Franke, H.-D., 417 Grande, C., 267 See Thiel, M., 426, 427 Grandel, S. See Luff, R., 53 Gypens, N. See Lancelot, C., 52 Granger, S. See Olsen, J.L., 423 Granmo, Å. See Magnusson, K., 80 Gräns, A.-S. See Holmes, J.M., 79 H Grantham, B.A., 417 See Shanks, A.L., 425 Haas, H.A. See Peeters, J.C.H., 54 Grashoff, M. See Zibrowius, H., 195 Hacker, J. See Hentschel, U., 267 Gräslund, S., 79 Hagen, W. See Kattner, G., 268 Grau, A. See Mayol, J., 191 Hagerman, L. See Baden, S.P., 77 Grau, A.M. See Riera, F., 192 Hagiwara, S., 79 Gravez, V. See Boudouresque, C.F., 185 Hagmeier, E. See Weigel, P., 56 Gray, W.M. See Landsea, C.W., 421 Hain, S., 267 Graziani, E.I., 267 Hajdu, E. See Granato, A.C., 267 See Kubanek, J., 269 Håkansson, C.L.J. See Baden, S.P., 77 Green, A.J., 417 Halanych, K.K. See Govindarajan, A.F., 417 Green, D.M. See Lourie, S.A., 421 Haley, P. J. See Popova, E.E., 54 Green, K. See Shaughnessy, P.D., 463 Hall, I.R., 79 Greene, C.H., 460 Hall, K.R. See Root, T.L., 463 Greenwood, P.G. See Young, C.M., 276 Halpern, B.S., 418 Gregg, W.W., 52 Hamann, M. See Bryan, P.J., 260 Gregory, L. See Dame, R.F., 415 Hamel, G., 188 Gregory, M.R. See Stevens, L.M., 426 Hamilton, W.J., 460 See Winston, J.E., 428 Hammond, P.S., 460 Grehan, A.J. See Voight, J.R., 322 See Wilson, B., 464 Greig, A. See Bryan, S.E., 413 Handler, P. See White, A., 83 Greig, T. See Beare, D.J., 459 Hansen, B., 461 Grellier, K. See, Wilson, B., 464 Hansen, I.S. See Stipa, T., 55 Grimes, C. See Sponaugle, S., 425 Hansen, J.W. See Canfield, D.E., 78 Grimes, D.J. See Harvell, C.D., 461 Hansen, L.J. See Wells, R.S., 464 Grimm, V., 417 Hantson, P. See Gerber, G.B., 79 Grimpe, G., 319 Hare, M.P., 418 Groeneveld, G. See Visser, M., 55 Hargittai, P.T. See Butt, A.M., 78 Grosberg, R.K., 418 Harmelin, J.G., 188, 189 See Sotka, E.E., 425 See Arnoux, A., 183 See Wares, J.P., 427 See Garrabou, J., 188 Grundfest, H. See Chiarandini, D.J., 78 See Marschal, C., 190

476 7044_Idx.fm Page 477 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

See Perez, T., 191 Henriksson, J., 79 See Sartoretto, S., 193 See Tjälve, H., 82 See Torrents, O., 194 Henriques, C. See Collins, M.A., 318 Harmelin-Vivien, M. See Sala, E., 193 Hense, I. See Stipa, T., 55 Harris, L.G. See Howe, N.H., 268 Henson, S.M. See Edmonds, J., 118 Harris, P.J. See Stovold, R.J., 120 Hentschel, U., 267 Harrison, J.A. See Coulson, S.J., 415 Heppel, S.S. See Gerber, L.R., 417 Harrison, R. See Ridgeway, S.H., 463 Herbert, J.M. See De Medeiros, E.F., 263 Harrison, S., 418 Herbig, K. See Radach, G., 54 Harrold, C., 418 Herdman, W.A., 267 Hartman, J.M. See Bart, D., 412 Hereu, B. See Linares, C., 189 Hartman, O., 118 Hergueta, E. See Salas, C., 193 Harvell, C.D., 461 Herman, J.S. See MacLeod, C.D., 462 Harvey, E. See Whalan, S., 428 Herman, P.M.J. See Huiskes, A.H.L., 419 Harvey, H.H. See Young, L.B., 83 Hermy, M. See Coppejans, E., 186 Harvey, J., See Scholin, C.A., 463 Hernandez, E.H., 79 Harwell, M.C., 418 Hernández, M., 461 Harwood, J., 461 Hernroth, B., 79 See Geraci, J.R., 460 Herrero, M. See Alvarez, R., 258 Hassell, D. See Hulme, M., 461 Herring, P.J., 319 Hastings, A. See Gerber, L.R., 417 Herut, B. See Kress, N., 80 See Guichard, F., 418 Hesse, B. See Meinesz, A., 191 See Harrison, S., 418 Hettiaratchi, D.R.P., 118 Haulena, M. See Scholin, C.A., 463 See Abdalla, A.M., 117 Haumayr, U., 267 Heu, M.-S., 79 Havenhand, J.N., 418 Heurtebise, S. See Lapègue, S., 421 Hawkins, S.J. See Sims, D.W., 463 Hiby, A.R. See Hammond, P.S., 460 See Southward, A.J., 463 Highsmith, R.C., 418 See Thompson, R.C., 427 Higuchi, R., 267 Hay, M.E. See Cronin, G., 262 See Miyamoto, T., 270 Hay, S.J. See Heath, M.R., 461 Hilbish, T.J. See Ó Foighil, D., 423 Haye, P.A. See Thiel, M., 323Ð429 Hill, S. See Hulme, M., 461 Hazell, A.S. See Normandin, L., 80 Hille, B., 79 He, X. See Goldsworthy, S.L., 319 Hillis-Colinvaux, L., 189 Heagerty, P. See Laidre, K.L., 462 Hinojosa, I.A. See Macaya, E.C., 421 Heald, E.J. See Odum, E.P., 423 Hirata, Y., 79 Healy, J.M., 319 Hirota, H., 267 Heath, M.R., 461 See Fusetani, N., 265 Heatwole, H., 418 See Okino, T., 271 Hedenström, A. See Alerstam, T., 459 Hite, G.J. See Ireland, C., 268 Hedgecock, D., 418 Hixon, M.A. See Caley, M.J., 413 Heide-Jorgensen, M.P., 461 Hnilo, J.J. See Gates, W.L., 52 See Hammond, P.S., 460 Hoagland, K.E., 418 See Laidre, K.L., 462 Hobbs, R.C. See Laidre, K.L., 462 Heimann, M. See Stephens, B.B., 55 Hobday, A.J., 418 Heimlich, S. See Hammond, P.S., 460 Hobson, W.C. See Fuller, G.B., 460 Heine, J.N. See McClintock, J.B., 270 Hoch, T., 52 Heinemann, D.W. See Kenney, R.D., 461 See Menesguen, A., 53 Heisterkamp, S. See de Swart, R.L., 460 Hochberg, F.G., 319 Hellberg, M.E., 418 See Piertney, S.B., 320 See Baums, I.B., 412 See Seibel, B.A., 321 See Swearer, S.E., 426 Hochlowski, J.E. See Okuda, R.K., 271 See Taylor, M.S., 426 Hockett, D., 79 Helle, E., 461 Hodge, K. See Censky, E.J., 414 Hellou, J., 267 Hodkinson, I.D. See Coulson, S.J., 415 Helmuth, B., 418 Hodson, S.L., 419 Hemminga, M.A., 418 Hoffman, D., 461,Hoegh-Guldberg, O. See Walther, G.-R., Hemphill-Haley, E. See Witter, R.C., 428 464 Hendrickx, M.E., 79 Hoffmann, H., 267

477 7044_Idx.fm Page 478 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Hofmann, E.E. See Fraser, W.R., 460 I See Harvell, C.D., 461 Hogg, I.D. See Stevens, M.I., 426 Iacozza, J. See Stirling, I., 463 Holberton, R. See Helmuth, B., 418 Ibanez, F. See Beaugrand, G., 459 Hollertz, K., 118 ICES, 461 Holm, K. See Hernroth, B., 79 Iijima, R., 268 Holmes, J.M., 79 Ijima, I., 319 Holst, G. See Koenig, B., 119 Ikeda, S. See Ijima, I., 319 Holt, J.T. See Proctor, R., 54 Iken, K., 268 See Allen, J.I., 50 See Avila, C., 259 Holt, R.D., 419 See Gavagnin, M., 265 Hong, E.P. See Fu, X., 265 Iken, K.B. See Amsler, C.D., 258 Hong, J.S., 189 Ilan, M. See Gillor, O., 266 See Harmelin, J.G., 188 See Carmely, S., 260 Hooper, J.N.A. See Wörheide, G., 429 Imboden, D.M. See Johnson, C.A., 79 Simpson, J.S., 273 Ingólfsson, A., 419 Hopke, J. See Hentschel, U., 267 Ingram, P. See Hockett, D., 79 Horgen, F.D., 267 Ingram, S. See Wilson, B., 464 Horn, M. See Hentschel, U., 267 IPCC, 461 Hornung, H. See Kress, N., 80 Iregren, A., 79 Horwood, J.W., 52 Ireland, C., 268 Hoskin, M.G., 419 Irie, H. See Kawamine, K., 269 Hossain, M.B. See Schmitz, F.J., 272 Ishizaka, J., 52 Hovland, M., 319 See Obata, A., 53 Howarth, M.J., 52 Ittekkot, V. See Jennerjahn, T.C., 419 Howe, N.H., 268 IUCN, 461 Howell, D. See Geng, J., 118 Ivaldi, M. See Drava, G., 78 Hoyle, W.E., 319 Ivanov, I. See Tzetlin, A.B., 120 Hrs-Brenko, M., 189 IWC, 461 Huang, R.C. See Gillete, R., 266 Izaguirre-Fierro, H. See Paez-Osuna, F., 81 Hubbard, D.M. See Lastra, M., 119 Izzo, G. See Castiello, D., 261 Huedelot, C. See Piertney, S.B., 320 Izzo, I., 268 Huelin, M.F., 189 Hughes, A.R. See Wares, J.P., 427 Hughes, R. See Uriz, M. J., 194 J Hughes, R.G. See Coma, R., 186 See Llobet, I., 190 Jablonski, D., 419 Hughes, R.N. See Colson, I., 414 Jackson, J.B.C., 419 See Goldson, A.J., 417 Jacobel, R.W. See Fountain, A.G., 118 Hughes, T.P. See Ayre, D.J., 412 Jaeger, H.M., 118 See Caley, M.J., 413 Jahn, W., 319 Huiskes, A.H.L., 419 James, N.P., 189 Hulme, M., 461 Janke, M. See Franke, H.-D., 417 See Sear, C., 463 Jansen, B.J.M., 268 Humm, H.J. See Raxworthy, C.J., 424 Jansen, R. See Peeters, J.C.H., 54 Hunt, A., 419 Janson, K., 419 Hunt, J.C., 319 Janssen, J. See McClintock, J.B., 270 Hunter, R.D., 118 Jansson, P. See Fountain, A.G., 118 Hureau, J.C. See Whitehead, P.J.P., 195 Jarre, L. See Hernandez, E.H., 79 Hurrell, J.W. See Stenseth, N., 463 Javel, F. See Piazzi, L., 192 Hurtado, L.A. See Pfeiler, E., 424 Jelinski, D.E. See Orr, M., 423 Huthnance, J.M. See Charnock, H., 51 Jell, J.S. See Bryan, S.E., 413 Huys, R., 268 Jenkins, G.J. See Hulme, M., 461 Hydes, D.J., 52 Jenkinson, L.S. See Davis, A.J., 460 See Hall, I.R., 79 Jennerjahn, T.C., 419 See Howarth, M.J., 52 Jennings, R. See Ó Foighil, D., 423 See Kelly-Gerreyn, B.A., 52 Jensen, K., 268 Hytteborn, H. See Johansen, S., 419 Jensen, S. See Helle, E., 461

478 7044_Idx.fm Page 479 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Jepson, P.D., 461 Juan, A. See Templado, J., 194 See Van Bressem, M.F., 464 Jumars, P.A., 119 Jereb, P., 319 See Dorgan, K.M., 85Ð121, 118 Jeudy de Grissac, A. See Boudouresque, C.F., 185 See Fauchald, K., 118 Jimbo, M. See Sakai, R., 272 See Nowell, A.R.M., 119 Jiménez, C., 268 See Schmidt, J.L., 120 Jimeno, A., 189 See Self, R.F.L., 120 Johannesson, K., 419 Jun, S. See Wei, H., 55 See Panova, M., 423 Johansen, S., 419 Johnsen, G. See Burghardt, I., 260 K See Wägele, H., 275 Johnsen, S., 319 Kamishima, Y. See Kawaguti, S. 269 Johnson, B.D., 118 Kamiya, H. See Sakai, R., 272 See Boudreau, B.P., 117 Kan, Y. See Horgen, F.D., 267 See Dorgan, K.M., 85Ð121, 118 Kanazawa, K., 119 See Jumars, P.A., 119 Kanneworf, E. See Nicolaisen, W., 119 Johnson, C.A., 79 Kant, W. See Van Bressem, M.F., 464 Johnson, L.E. See Pardo, L.M., 423 Karl, D.M., 52 Johnson, M.P., 419 Karuso, P., 268 Johnson, M.S., 420 Kaschner, K., 461 See Whalan, S., 428 Kashman, Y. See Carmely, S., 260 Johnson, P.M., 268 Kassühlke, K.E., 268 Johnson, R.F., 268 Kathiresan, K., 420 See Gosliner, T.M., 266 Kattner, G., 268 Johnson, R.G., 118 Katyayani, R. See Fingerman, M., 79 Johnson, S. See Gosliner, T.M., 267 Katz, B., 79 Joint, I.R. See Howarth, M.J., 52 Kawa, K. See Fukunda, J., 79 Jokiel, P.L., 420 Kawaguti, S., 269 Jolliffe, I.T. See Zheng, X., 464 Kawamine, K., 269 Jollivet, D. See Dupont, L., 416 Keeling, R.F. See Stephens, B.B., 55 Jollivet, D.S. See Jolly, M.T., 420 Keeney-Kennicutt, W.L. See Trefry, J.H., 82 Jolly, M.T., 420 Keil, R.G. See Schmidt, J.L., 120 Jones, E. See Beare, D.J., 459 Keller, B.D. See Dayton, P.K., 415 Jones, E.G., See Beare, D.J., 459, Keller, G. See McCartney, M.A., 422 Jones, G.P., 420 Kelly, D.L. See Wells, R.S., 464 See Caley, M.J., 413 Kelly, M.C. See Heath, M.R., 461 See Swearer, S.E., 426 Kelly-Gerreyn, B. See OSPAR, 54 Jones, H.D. See Trueman, E.R., 120 Kelly-Gerreyn, B.A., 52 Jones, H.R. See Ridout, P.S., 81 See Hydes, D.J., 52 Jones, J.E., 52 Kelsey, H.M. See Witter, R.C., 428 See Delhez, E.J.M., 51 Kennedy, G. See Normandin, L., 80 See Howarth, M.J., 52 Kennedy, G.Y., 269 See Luyten, P.J., 53 Kennedy, M. See Donald, K.M., 416 See Proctor, R., 54 Kennedy, R. See Solan, M., 120 Jones, K. See Lee, J.-Y., 52 Kennedy, S., 461 Jones, L.G., 420 See Domingo, M., 460 Jones, M.B. See Edwards, M., 460, Kenney, R.D., 461 See Roast, S.D., 119 Kent, L.E. See Frick, C., 417 Jones, M.L., 118, 461 Keough, M.J., 420 Jones, R.G. See Hulme, M., 461 Kessing, B.D. See Lessios, H.A., 421 Jones, S. See Lee, J.-Y., 52 Ketmaier, V. See De Matthaeis, E., 415 Jongaramruong, J., 268 Keudel, M., 119 Joordens, J. See Michielsen, B., 53 Khalanski, M. See Agoumi, A., 50 J¿rgensen, O.A., See Laidre, K.L., 462 Kienzle, M. See Beare, D.J., 459 Jorhem, L., 79 Kietpawpan, M. See Visuthismajarn, P., 82 Joubin, L., 319 Kigoshi, H. See Yamada, K., 276 See Fischer, H., 319 Kiiltomäki, A. See Stipa, T., 55 Jozefowicz, C.J. See Ó Foighil, D., 423 Kim, J.-S. See Heu, M.-S., 79

479 7044_Idx.fm Page 480 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Kim, K. See Harvell, C.D., 461 Kuiken, T., 462 Kimura, M., 420 See Jepson, P.D., 461 See Maruyama, T., 422 See Kennedy, S., 461 King, T.M. See Waters, J.M., 427 Kulikov, E.A., 421 Kingsford, M.J., 420 Kyle, C.J., 421 See Sponaugle, S., 425 Kinlan, B.P., 420 See Siegel, D.A., 425 L Kinoshita, R. See Bressem, M.F., 464 Kirby, R. See Chambers, R.J., 414 Laane, R. See Radach, G., 54 Kirkwood, J.K. See Jepson, P.D., 461 See Sündermann, J., 55 See Kuiken, T., 462 See Visser, M., 55 Kisugi, J. See Iijima, R., 268 Laane, R.W.P.M., 52 Kitching, J.A., 420 See Berlamont, J., 51 Kleeman, K.H., 189 See de Vries, I., 51 Klein, K.A. See Santamarina, J.C., 119 Laborel, J., 189 Klussmann, A. See Klussmann-Kolb, A., 269 See Augier, H., 183 Klussmann-Kolb, A., 269 See Boudouresque, C.F., 185 See Vonnemann, V., 274 See Sartoretto, S., 193 See Wägele, H., 275 Laborel-Deguen, F. See Laborel, J., 189 Knap, A. See Karl, D.M., 52 Lacaze-Duthiers, H., 189 Knight-Jones, E.W. See Knight-Jones, P., 420 La Colla, P. See Pani, A., 271 Knight-Jones, P., 420 Lacroix, G. See Lancelot, C., 52 Knoblock, D. See Boyle, P.R., 318 LaCroix, M. See Bach, S., 412 Knowles, L.L. See Pfeiler, E., 424 Lafferty, K.D., 462 Knudsen, J., 319 Lafont, R. See Laborel, J., 189 Koch Rasmussen, E. See Baretta-Bekker, J.G., 51 Laidre, K.L., 462 Koehl, M.A.R., 119 See Heide-Jorgensen, M.P., 461 Koenig, B., 119 Lallier-Verges, E. See Marchand, C., 422 Koepfler, E. See Dame, R.F., 415 La Lumiere, R. See Olsen, J.L., 423 Koike, K. See Sakai, R., 272 Lambert, W.J., 421 Kokke, W.C.M.C. See Whiters, N.W., 275 See Todd, C.D., 427 Kolb, A., 269 Lancelot, C., 52 Komori, T. See Higuchi, R., 267 See OSPAR, 54, Kon, S.K. See Fisher, L. R., 264 Landi, F. See Giordano, A., 266 Kornicker, L.S., 420 Landis, C.S. See Coombs, D.S., 414 Korte, F. See Hoffman, D., 461 Landis, E. See Dorgan, K.M., 118 Kotta, J. See Orav-Kotta, H., 423 Landsea, C.W., 421 Koukouras, A. See Chintiroglou, H., 186 Lanfranco, E. See Boudouresque, C.F., 185 Koutstaal, B.P., 420 Langelin, H.R. See Nassrallah-Aboukais, N., 80 See Hemminga, M.A., 418 Langenbuch, M. See Pörtner, H.O., 462 See Huiskes, A.H.L., 419 Lapègue, S., 421 Kramer, D.L. See Rakitin, A., 424 Laptikhovsky, V.V., 320 Kraus, E.B., 52 Largier, J.L., 421 Krauss, K.W., 420 See Carr, M.H., 414 Kreis, P. See Teeyapant, R., 273 See Gaines, S.D., 417 Kress, A., 269 Larson, A. See Glor, R.E., 417 Kress, N., 80 Larsson, B.S. See Tjälve, H., 82 Kristjánsson, B.K. See Ingólfsson, A., 419 Lasker, H.R. See Gutiérrez-Rodríguez, C., 418 Krönström, J., 80 Laslett, R.E., 80 Ksebati, M.B., 269 Lastra, M., 119 Kubanek, J., 269 Lau, S.S.S. See Rainbow, P.S., 81 See Dumdei, E.J., 263 Laubier, L., 189 Kubodera, T., 320 See Got, H., 188 Kudenov, J.D., 119 Law, R.J. See Jepson, P.D., 461 Kuehl, M. See Koenig, B., 119 Lawrence, M.G. See Bryan, S.E., 413 Kühn, W., 52 Lawton, J.H. See Davis, A.J.,460 See Eigenheer, A., 51 Lazure, P. See Proctor, R., 54 See Moll, A., 53 Lea, D.W. See Swearer, S.E., 426

480 7044_Idx.fm Page 481 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Leach, R.M., 80 Littler, D.S. See Littler, M.M., 190 Learmonth, J.A., 431Ð464 Littler, M.M., 190 See MacLeod, C.D., 462 Littlewood, D.T.J. See Williams, S.T., 428 Lebednik, P.A., 189 Liu, K.S. See Chan, J.C.L., 414 Le Campion, J. See Laborel, J., 189 Liu, Z. See Wei, H., 56 Le Campion-Alsumard, T. See Chazottes, V., 186 Llobet, I., 190 LeDuc, R., 462 See Coma, R., 186 Lee, J.-Y., 52 Llorens, T. See Ayre, D.J., 411 Lee, R.K.S., 189 Lobban, C.S. See Barnes, D.K.A., 412 Lee, S.Y., 421 Lo Bianco, S., 190 Lee, T.N. See Yeung, C., 429 Locke, A., 421 Leeraphante, N. See Visuthismajarn, P., 82 Locket, N.A. See Warrant, E.J., 322 Lefebvre, K. See Scholin, C.A., 463 Lockyer, C. See Boyd, I.L., 459 Lefeuvre, J.C. See Bouchard, V., 413 See Kuiken, T., 462 LeFurgey, A. See Hockett, D., 79 Lockyer, C.H., 462 Le Gac, M., 421 See Anderson, L.W., 459 Leis, J.M. See Sponaugle, S., 425 Logan, A., 190 Leitão, A. See Lapègue, S., 421 Logdson, M.L. See Laidre, K.L., 462 Lemoine, P. See Hamel, G., 188 Longhi, E. See Geng, J., 118 Lenhart, H.-J., 52 Looise, B.A.S., 53 See Kühn, W., 52 Lopez, S. See Alvarez, R., 258 See Radach, G., 54 López de la Rosa, I. See García-Raso, J.E., 187 See van den Berg, A.J., 55 López-Fernandez, A. See Van Bressem, M.F., 464 Lenz, W., 53 López-Ibor, A. See Templado, J., 194 Léonard, A. See Gerber, G.B., 79 Lopez-Jurado, L.F. See Carranza, S., 414 Leopold, M.F. See Hammond, P.S., 460 See Hernández, M., 461 Leslie, R. See Bryan, S.E., 413 López-Rodas, V. See Hernández, M., 461 Lessios, H.A., 421 Los, F.J., 53 See McCartney, M.A., 422 See Bokhorst, M., 51 Lester, S.E. See Kinlan, B.P., 420 See de Vries, I., 51 Lethbridge, R.C. See Borowitzka, M.A., 413 See Peeters, J.C.H., 54 Levin, L.A., 119, 421 See MARE Consortium, 53 See Becker, B.J., 412 See Michielsen, B., 53 See Blair, N.E., 117 Loscutoff, S. See Scholin, C.A., 463 See Davis, J.L.D., 415 Losos, J.B. See Glor, R.E., 417 See Moseman, S.M., 422 Louisy, P. See Zabala, M., 195 Levin, S.A. See Guichard, F., 418 Lounsbury, V. See Geraci, J.R., 460 Levins, R. See Heatwole, H., 418 See Geraci, J.R., 460 Lewis, P.N., 421 Lourie, S.A., 421 Lewis, T.E. See Hodson, S.L., 419 Low, P.J. See Perry, A.L., 462 Li, G.Q. See Findlay, J.A., 264 Lowe, J. See Hulme, M., 461 Lieberman, E.M. See Butt, A.M., 78 Lowenstine, L.J. See Scholin, C.A., 463 Lignell, M. See Chaga, O., 78 Lowry, R.K. See Howarth, M.J., 52 Lima, M. See Camus, P.A., 414 Lozano, C.J. See Popova, E.E., 54 See Stenseth, N., 463 Lu, C.C. See Gales, R., 319 Limia, J. See Ortiz, A., 191 See O'Shea, S., 319 Linares, C., 189 Lu, X. See Hulme, M., 461 Lindeman, K.C. See Sponaugle, S., 425 Lubchenco, J., 421 Lindgren, A.R., 320 See Allison, G.W., 411 Lindley, J.A. See Beaugrand, G., 459 Lucchetti, G. See Cattaneo-Vietti, R., 261 Lindquist, N. See Cronin, G., 262 Luding, S. See Geng, J., 118 Lindquist, N.G. See Tjälve, H., 82 Luff, R., 53 Linington, R.G. See Barsby, T., 259 Luk, E.E., 80 Lipka, D.A., 320 Lukas, R. See Karl, D.M., 52 Lipp, E.K. See Harvell, C.D., 461 Lundberg, B. See Boudouresque, C.F., 185 Lipscomb, T. See Scholin, C.A., 463 Lundberg, J. See Johannesson, K., 419 Liret, C. See Wilson, B., 464 Lüning, K., 190 Lisin, S. See Harrold, C., 418 Lunn, N.J. See Stirling, I., 463 Liss, P.S. See Charnock, H., 51 Lunow, C. See Jones, G.P., 420

481 7044_Idx.fm Page 482 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Luttikhuizen, P.C., 421 Marion, A.F., 190 Lutz, R.A. See Jablonski, D., 419 Mariotti, A. See Bouchard, V., 413 Luyten, P. See Lee, J.-Y., 52 Marko, P.B., 422 See Proctor, R., 54 Markusse, M.M. See Huiskes, A.H.L., 419 Luyten, P.J., 53 See Koutstaal, B.P., 420 Lynch, D.R., 53 Marlais, S.M., See Gates, W.L., 52 Marongiu, M.E. See Pani, A., 271 Marotzke, J., 462 M Marquez-Farias, J.F. See Pfeiler, E., 424 Marschal, C., 190 Maass, R. See Johnson, B.D., 118 See Torrents, O., 194 MacArthur, R.H., 421 Marsden, I.D., 80 Macaya, E.C., 421 Marsh, H.D. See Boyd, I.L., 459 Maccatrozzo, L. See Zane, L., 429 Marshall, B.A. See Ó Foighil, D., 423 Macchiavello, J.E. See Macaya, E.C., 421 Marshall, J.P., 190 Macdonald, E.M. See Heath, M.R., 461 Martel, A., 422 MacFarland, F., 269 Martí, R., 190 Machuy, N. See Butzke, D., 260 Martin, D., 190 Mackenzie, J.B., 421 See Rosell, D., 192 MacLeod, C.D., 462 See Uriz, M. J., 194 See Learmonth, J.A., 431Ð464 Martin, J.-L.M., 80 Maddock, L. See Herring, P.J., 319 Martin, R., 270 Magagnini, G. See Bramanti, L., 185 Martinez, E.A., 422 Magalhaes, A. See Granato, A.C., 267 Martínez, E. See Ciavatta, M.L., 261 Magalhaes, C.A. See Andrade, S.C.S., 411 See Zubía, E.,276 Magalon, H., 422 See Fontana, A., 264, 265 Maggi, E. See Santangelo, G., 193 Maruyama, T., 422 Magnusson, K., 80 Maser, C., 422 Maldonado, M., 190 Masó, M., 422 See Uriz, M. J., 194 Massó, C. See García-Rodríguez, M., 187 Mallefet, J. See Féral, J.P., 417 See Ortiz, A., 191 Mandal, A. See Ahearn, G.A., 76 See Templado, J., 194 Mandal, P.K. See Ahearn, G.A., 76 Mateo, J.A. See Carranza, S., 414 Mangold, K., 320 Mathis, W.N. See Feller, I.C., 416 Manhart, J.R. See Rumpho, M.E., 272 Matsunaga, S. See Fusetani, N., 265 Manker, D. See Abramson, S.N., 258 Mattia, C.A. See Ciavatta, M.L., 261 Mann, J., 462 See Cimino, G., 262 MANS, 53 See Puliti, R., 271 Manukhin, B.N. See Buznikov, G.A., 260 Mayer, L.M. See Jumars, P.A., 119 Manzanilla, S.R., 462 See Voparil, I.M., 120 Manzo, E., 269 See Chen, Z., 117 Marbach, A., 269 Mayhoub, H. See Boudouresque, C.F., 185 Marchand, C., 422 Mayo, C.A. See Geraci, J.R., 460 Marcos, R. See Casas, V.M., 414 Mayol, J., 191 Marcus, E., 269 Mazzarella, L. See Cimino, G., 262 Marcus du Bois-Reymond, E., 269, 270 See Puliti, R., 271 MARE Consortium, 53 Mazzarelli, G., 270 Marfenin, N.N. See Slobodov, S.A., 425 McAliskey, M. See Kennedy, S., 461 Mariani, S., 190 McCall, P.L. See Rhoads, D.C., 119 Marín, A., 270 McCarthy, L.S. See Rand, G.M., 81 Cimino, G., 262 McCartney, M.A., 422 See Ebel, R., 263 McCauley, D.E. See Whitlock, M.C., 428 See Fontana, A., 264 McClintock, J.B., 270 See Gavagnin, M., 265, 266 See Amsler, C.D., 258 See Spinella, A., 273 See Bryan, P.J., 260 Marín, O. See Mena, I., 80 See Yoshida, W.Y., 276 Marin III, R. See Scholin, C.A., 463 McDonald, G.R., 270 Marino, G., 190 McDonald, K. See Dethier, M.N., 415 Marinopoulos, J. See Harmelin, J.G., 189 McDonald, R. See Hulme, M., 461

482 7044_Idx.fm Page 483 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

McEdward, L.R., 422 Millen, S.V. See Schrödl, M., 272 McFadden, C.S., 422 Miller, D.J. See Mackenzie, J.B., 421 McIntyre, I.G. See Adey, W.H., 182 Miller, K.A., 422 McKee, K.L. See Feller, I.C., 416 Miller, M.W. See Baums, I.B., 412 McKenzie, E. See Beare, D.J., 459 Miller, P.E. See Scholin, C.A., 463 McLachlan, A. See Nel, R., 119 Milner, P. See Barnes, D.K.A., 412 McLellan, W.A. See Scholin, C.A., 463 Minale, L., 270 McLoughlin, P. See Ferguson, S.H., 460 See Cimino, G., 262 McMillan, P.A. See Becker, B.J., 412 Minato, S. See Sakai, R., 272 McMillan, W.O., 422 Minei, R. See De Petrocellis, L., 263 McNiven, C.M. See Kennedy, S., 461 Mingati, V. See Drava, G., 78 McQuaid, C.D. See Chambers, R.J., 414 Mistri, M., 191 Mead, D.J. See Frankel, L., 118 Mitchell, C.E. See Harvell, C.D., 461 Medina, A. See García-Gómez, J.C., 265 Mitchell, K. See Pinn, E.H., 424 Megina, C., 270 Mitchell, T.D. See Hulme, M., 461 Meinesz, A., 191 Mitsuda, H. See Fushimi, K., 417 See Belsher, T., 184 Miyamoto, T., 270 See Boudouresque, C.F., 185 See Fontana, A., 264 See Piazzi, L., 192 See Higuchi, R., 267 Meisenheimer, J., 270 Miyashita, M. See Kawamine, K., 269 Mejàre, C. See Tjälve, H., 82 Miyazaki, S. See Hagiwara, S., 79 Melekestsev, I.V. See Pinegina, T.K., 424 Mladenov, P.V. See Sköld, M., 425 Mena, I., 80 Moberg, P.E. See Edmands, S., 416 Mendez, M.A. See Rozbaczylo, N., 119 Moeller, P.D.R. See Scholin, C.A., 463 Mendoza, M.L. See Cabioch, J., 185 Moffat, T.J. See Howarth, M.J., 52 Menesguen, A., 53 Moffett, D. See Kennedy, S., 461 See Guillaud, J.-F., 52 Mol, I. See Stegenga, H., 425 See Hoch, T., 52 Molcard, A. See Aliani, S., 411 See OSPAR, 54 Moline, M.A., 462 Menge, B.A. See Caley, M.J., 413 Molinier, R., 191 Menna, M. See Constantino, V., 262 See Blanc, J.J., 184 Menzel, A. See Walther, G.-R., 464 Molinski, T.F. See Faulkner, D.J., 264 Menzies, R.J., 422 Moll, A., 53 Mergler, D. See Normandin, L., 80 See Kühn, W., 52 Merriwether, D.A. See Ó Foighil, D., 423 See Luff, R., 53 Merton, H., 270 See OSPAR, 54 Messana, G. See Baratti, M., 412 See Radach, G., 1Ð60 Mews, M. See Orr, M., 423 See Skogen, M.D., 55 Meyer, C. See Paulay, G., 423 See Wei, H., 55 Meyer, T.F. See Butzke, D., 260 Mollo, E., 270 Meyer, W.T., 320 See Cimino, G., 262 Meysman, F.J.R., 119 See Fontana, A., 264, 265 See Boudreau, B.P., 117 See Gavagnin, M., 265, 266 Meziane, T. See Mfilinge, P.L., 422 See Manzo, E., 269 Mfilinge, P.L., 422 See Valdés, A., 274 Michaels, A.F. See Karl, D.M., 52 Mommaerts, J.P., 53 Michaud, D. See Schmitz, F.J., 272 See Radach, G., 54 Michielsen, B., 53 Monbaliu, J. See Berlamont, J., 51 Michielsen, B.F. See de Vries, M.B., 51 Monica, C.D. See Giordano, A., 266 Middelburg, J.J. See Meysman, F.J.R., 119 Monod, J.L. See Arnoux, A., 183 Middleton, D.A.J., See Arkhipkin, A.I., 459 Montanaro, D. See Gavagnin, M., 265, 266 Mifsud, C. See Piazzi, L., 192 Monteiro-Marques, V. See Zibrowius, H., 195 Migotto, A.E. See Granato, A.C., 267 Montemayor-Lopez, G. See Pfeiler, E., 424 Mikkelsen, P.M., 270 Montserrat, A., 191 Milchakova, N. See Coyer, J.A., 415 Moore, B.S. See Hentschel, U., 267 See Olsen, J.L., 423 Moore, C.J. See Dumdei, E.J., 263 Miledi, R. See Katz, B., 79 Moore, P., 80 Mileikovsky, S.A., 422 Moore, P.D. See Cox, C.B., 415 Milicich, M.J. See Jones, G.P., 420 Moosa, M.K. See Barber, P.H., 412

483 7044_Idx.fm Page 484 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Moquin-Tandon, G., 270 Nicolaidou, A. See Nott, J.A., 80 Mora, C., 422 Nicolaisen, W., 119 Morales-Nin, B. See Coll, J., 186 Nieboer, E., 80 Moranta, J. See Coll, J., 186 Niedbala, W., 423 Morelli, D. See Carey, S., 414 Nielsen, J. See Whitehead, P.J.P., 195 Moreteau, J.C. See Vicente, N., 194 Nielsen, O. See Van Bressem, M.F., 464 Morgan, S.G. See Sponaugle, S., 425 Nihoul, J.C.J., 53 See Swearer, S.E., 426 Nikolaeva, G.G. See Tsikhon-Lukanina, E.A., 427 Morganti, C. See Cerrano, C., 185 Nikolic, M., 191 Morhange, C. See Laborel, J., 189 Nilsson, P.G. See Johannesson, K., 419 Morri, C. See Cerrano, C., 185 Nishiguchi, M.K. See Lindgren, A.R., 320 Morrill, W. See Distel, D.L., 416 Nishikawa, M. See Fushimi, K., 417 Morrone, S.R. See Cimino, G., 261 Nishiyama, S. See Arimoto, H., 258 Mortensen, T., 422 Nixon, M. See Aldred, R.G., 317 Morton, J.E., 270 See Hochberg, F.G., 319 Moseman, S.M., 422 Norman, M.D., 320 Moss, V.A. See Hunter, R.D. 118 Normandin, L., 80 Mounier, Y., 80 Norris, J.N. See Littler, M.M., 190 Mukai, H., 422 Norstedt, M., 80 Muller, M.C.M. See Tzetlin, A.B., 120 Northcote, P.T. See Blunt, J.W., 260 Mulsow, S., 119 Northridge, S.P., 462 Munar, J., 191 See Reid, J.B., 462 Munday, P.L. See Mackenzie, J.B., 421 Norton, T.A., 423 Muniaín, C., 270 Nott, J.A., 80 Munilla, T., 191 See Viarengo, A., 82 Muñiz-Salazar, R., 422 Novelli, S. See Abbiati, M., 182 Munro, J.L. See Sponaugle, S., 425 Nowell, A.R.M., 119 Munro, M.H.G. See Blunt, J.W., 260 Nunes, M.L. See Rosa, R., 321 Murillo, J. See Gili, J.M., 188 Nussbaum, R.A. See Raxworthy, C.J., 424 Murnane, R. See Stephens, B.B., 55 Nybakken, J.W. See McDonald, G.R., 270 Murphy, J.M. See Hulme, M., 461 Murray-Jones, S.E., 423 Mysterud, A. See Stenseth, N., 463 O

Obata, A., 53 N Obino, P. See Pani, A., 271 O'Brien, C.M., 462 Naef, A., 320 Ó Céidigh, P. See Tully, O., 427 Nagai, H. See Horgen, F.D., 267 Ochi, R., 80 Nagel, S.R. See Jaeger, H.M., 118 O’Dea, M. See Collins, M.A., 318 Naik, C.G. See Fontana, A., 264 Odhner, N.H., 270 Nakajima, S. See Hagiwara, S., 79 O’Donoghue, C.O. See MacFarland, F., 269 Nakamura, A. See Kawaguti, S., 269 O’Dor, R.K., 320 Nakao, Y. See Szabo, C.M., 273 Odum, E.P., 423 Nassrallah-Aboukais, N., 80 See Odum, H.T., 191 Nehring, D. See Radach, G., 54 Odum, H.T., 191 Neigel, J.E., 423 Ó Foighil, D., 423 See Carr, M.H., 414 Ohfune, Y. See Kawamine, K., 269 Neil, D.M. See Baden, S.P., 77 Oien, N. See Hammond, P.S., 460 See Hellberg, M.E., 418 Ojeda, F.P., 423 See Field, R.H., 79 Okada, Y., 270 See Holmes, J.M., 79 Okamoto, H., 81 Nel, R., 119 Okino, T., 271 Nesis, K.N., 320 See Hirota, H., 267 See Guerra, A., 319 Okuda, R.K., 271 Neto, J. See Flindt, M.R., 417 Okutani, T. See Kubodera, T., 320 Neto, L. See Domaneschi, O., 416 Ólafsson, E. See Svavarsson, J., 426 Neuparth, T. See Costa, F.O., 415 Olivella, I. See Bibiloni, M.A., 184 Nicholls, N. See Landsea, C.W., 421 See Ros, J., 192

484 7044_Idx.fm Page 485 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Oliver, J. See Mayol, J., 191 Palacin, C. See Duran, S., 416 See Riera, F., 192 Palacios, R. See Yannicelli, B., 121 Olla, B.L. See Pearson, W.H., 81 Palade, P.T., 81 O'Loughlin, P.M. See Waters, J.M., 427 Palanques, A., 191 Olsen, J.L., 423 Palumbi, S.R., 423 See Coyer, J.A., 415 See Barber, P.H., 412 See Diekmann, O.E., 416 See Duda, T.F., 416 See Engelen, A.H., 416 See Gerber, L.R., 417 See Miller, K.A., 422 See Hellberg, M.E., 418 Olson, D.B. See Cowen, R.K., 415 See Lubchenco, J., 421 Olsson, M. See Helle, E., 461 See McMillan, W.O., 422 Ong, S., 271 See Sotka, E.E., 425 Onuki, H. See Fusetani, N., 265 Panayotidis, P. See Boudouresque, C.F., 185 Oommen, V.P., 320 See Piazzi, L., 192 Orav-Kotta, H., 423 Pandian, T.J., 81 Oreskes, N., 53 Pani, A., 271 Orlando, P. See De Petrocellis, L., 263 Panova, M., 423 Orr, M., 423 Panteleeva, N.N. See Stepanjants, S.D., 426 Ortea, J., 271 Parameswaram, P.S. See Fontana, A., 264 See Alcazar, J., 317 Pardal, M.A. See Flindt, M.R., 417 See Avila, C., 259 Pardi, G. See Piazzi, L., 192 See Bouchet, P., 260 Pardo, L.M., 423 See Ciavatta, M.L., 261 Parenzan, P., 191 See Gavagnin, M., 265, 266 Paris, C.B. See Cowen, R.K., 415 See Muniaín, C., 270 Park, J.K. See Ó Foighil, D., 423 See Zubía, E., 276 Parker, P.G., 423 Ortea, J.A. See Fontana, A., 264, 265 Parmesan, C. 462 See Valdés, A., 274 See Walther, G.-R., 464 Ortega, M.J., 271 Pascual, J., 191 Ortega-García, S. See Zarate-Villafranco, A., 429 Pascual, M. See Duran, S., 416 Ortega-Ortiz, J.G. See Würsig, B., 464 Passeggio, A. See Spinella, A., 273 Orth, R.J. See Harwell, M.C., 418 Passos, F. See Domaneschi, O., 416 Ortiz, A., 191 Pastor, T. See Aguilar, A., 459 O’Shea, S., 320 Patarnello, T. See Zane, L., 429 Osore, M.K.W. See Svavarsson, J., 426 Pätsch, J., 54 OSPAR, 54 See Kühn, W., 52 Ostellari, L. See Zane, L., 429 See Moll, A., 53 Osterhaus, A D.M.E. See Harvell, C.D., 461 See OSPAR, 54 See de Swart, R.L., 460 See Radach, G., 54 See Ross, P.S., 463 Patzner, R.A. 191 ¯sterhus, S. See Hansen, B., 461 Paul, K.M. See Dethier, M.N., 186 Ostfeld, R.S. See Harvell, C.D., 461 Paul, V.J. See Avila, C., 259 Ostrowski, M. See Skogen, M.D., 55 See Becerro, M.A., 259 Ottersen, G. See Stenseth, N., 463 See Fenical, W., 264 Oudot-Le Secq, M.P. See Olsen, J.L., 423 See Ginsburg, D.W., 266 Overnell, J. See Hall, I.R., 79 See Pennings, S.C., 271 Overstreet, R.M. See Harvell, C.D., 461 See Poiner, A., 271 Ozer, J. See Delhez, E.J.M., 51 See Rogers, S.D., 272 See Proctor, R., 54 See Slattery, M., 273 Paulay, G., 423 Pawlik, J.R., 271 P Payne, M. See Kenney, R.D., 461 Peach, K. See Beare, D.J., 459 Packard, A., 320 Pearcy, W.G., 320 Paez-Osuna, F., 81 See Voss, G.L., 322 See Hendrickx, M.E., 79 Pearse, J.S. See Lessios, H.A., 421 Page, H.M. See Bram, J.B., 413 Pearson, G. See Billard, E., 412 Pages, F. See Masó, M., 422 Pearson, G.A. See Coyer, J.A., 415 Pala, D. See Piazzi, L., 192 See Diekmann, O.E., 416

485 7044_Idx.fm Page 486 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Pearson, W.H., 81 Pinn, E.H., 424 Pechenik, J.A., 423 Pino, M.A. See Ó Foighil, D., 423 Peck, L S. See Ansell, A.D., 117 Pinto, R. See Martinez, E.A., 422 Peddemors, V. See Van Bressem, M.F., 464 Pira, E. See Hernandez, E.H., 79 Pedersen, C.B. See Flindt, M.R., 417 Pisacane, A. See Armstrong, E., 259 Peeters, J.C.H., 54 Pizzuto, F. See Giaccone, G., 188 See de Vries, I., 51 Plaia, G. See Blair, N.E., 117 Pegler, K. See Radach, G., 54 Planque, B., 462 Peirano, A. See Piazzi, L., 192 See Edwards, M., 460 Pelseneer, P., 271 See O'Brien, C.M., 462 Pemberton, D. See Gales, R., 319 Pleijel, F. See Rouse, G.W., 119 Penney, B.K., 271 Podestá, G.P. See Waluda, C.M., 464 See Ong, S., 271 Pohlmann, T., 54 Pennings, S.C., 271 See Delhez, E.J.M., 51 Penrose, D. See Woelkerling, W.J., 195 See Proctor, R., 54 Peperzak, L. See Peeters, J.C.H., 54 See Sündermann, J., 55 Peppiatt, C.J. See Armstrong, E., 259 Poiner, A., 271 Pereira, J. See Rosa, R. 321 Pola, M., 271 Pérès, J., 191 Polà, E. See Coma, R., 186 Pereyra, W.T., 320 Polishchuk, I.A. See Arkhipkin, A.I., 459 Perez, T., 191 Pomroy, A.J. See Howarth, M.J., 52 See Garrabou, J., 188 Ponder, W.F., 271 Pérez-Figueroa, A., 424 Pope, N. See Roast, S.D., 119 Perez-Gonzalez, R. See Paez-Osuna, F., 81 Popova, E.E., 54 Pergent, G. See Piazzi, L., 192 Popper, K.R., 54 Perrier, R., 271 Porcelli, M., 271 Perrin, C., 424 Porter, J.S., 424 Perrin, W.F., 462 Porter, J.W. See Harvell, C.D., 461 Perry, A.L., 462 See Lafferty, K.D., 462 Pershing, A.J. See Greene, C.H., 460 Portilla, E. See Beare, D.J., 462 Pertusati, M. See Piazzi, L., 191 Pörtner, H.O., 424, 462 Petersen, O. See Burchard, H., 51 Possingham, H. See Roughgarden, J., 424 Petersen, S., 81 Possingham, H.P. See Allison, G.W., 411 Peterson, M.A., 424 See Gerber, L.R., 417 Petrocelli, A. See Piazzi, L., 192 Post, E. See Walther, G.-R., 462 Peyrot-Clausade, M. See Chazottes, V., 186 Potter, G.L. See Gates, W.L., 52 Pfeiler, E., 424 Potts, B.C.M. See Kassühlke, K.E., 268 Pfitzner, J. See Alongi, D.M., 411 Potts, D.C. See Edgar, G.J., 416 Philippe, S. See Normandin, L., 80 Potts, G.W., 271 Phillips, T.J. See Gates, W.L., 52 Pou, S. See Riera, F., 192 Piatkowski, U., 320 Poulin, E. See Le Gac, M., 421 See Vecchione, M., 321 Pounds, J.A. See Root, T.L., 463 Piazzi, L., 191, 192 Powell, C.J. See Young, C.M., 276 Picard, J.M. See Pérès, J., 191 Powell, C.L. See Scholin, C.A., 463 Picco, P. See Cerrano, C., 185 Powell, J.A. See Reynolds, J.E., 463 Pichon, M. See Marschal, C., 190 Prandle, D., 54 Pierce, G.J. See Learmonth, J.A., 431Ð464 See Berlamont, J., 51 See MacLeod, C.D., 462 See Hydes, D.J., 52 See Waluda, C.M., 464 Prasad, R.S. See Schmitz, F.J., 272 See Zheng, X., 464 Prescott, J.H. See Geraci, J.R., 460 Piertney, S.B., 320 Presley, B.J. See Trefry, J.H., 82 424 Pribanic, S. See Wilson, B., 464 See Carvalho, G.R., 414 Price, J.T. See Root, T.L., 463 Pietra, F. Ee Guerriero, A., 267 Prinsep, M.R. See Blunt, J.W., 260 Pihl, L. See Baden, S.P., 77 Procaccini, G. See Coyer, J.A., 415 Pika, J. See Dumdei, E.J., 263 See Olsen, J.L., 423 Pilling, G.M. See Xavier, J.C., 322 Proctor, R., 54 Pineda, J.S. See Sponaugle, S., 425 See Allen, J.I., 50 Pinegina, T.K., 424 See Delhez, E.J.M., 51

486 7044_Idx.fm Page 487 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

See Howarth, M.J., 52 Rainbow, P.S., 81 See Hydes, D.J., 52 See Chan, H.M., 78 See Luyten, P.J., 53 See Fialkowski, W., 78 Proffitt, C.E., 424 See Marsden, I.D., 80 See Travis, S.E., 427 See Ridout, P.S., 81 Proksch, P., 271 See White, S.L., 83 See Ebel, R., 263 Rakitin, A., 424 See Teeyapant, R., 273 Ramirez, R.A. See Casas, V.M., 414 See Thoms, C., 274 Ramos, A.A., 192 Prosch,V. See Reinhardt, J.T., 320 Ramos, R., See Van Bressem, M.F., 464 Pruvot, G., 192 Ramster, J. See Lenz, W., 53 Puig, P. See Palanques, A., 191 Rand, G.M., 81 Puliti, R., 271 Rankin, J.C., 81 See Ciavatta, M.L., 261 Rapposch, M. See Ireland, C., 268 See Cimino, G., 262 Rasch, P.S. See Delhez, E.J.M., 51 Purcell, E.M., 119 Ratcliffe, N.A., 81 Purdey, M., 81 Rattner, B.A. See Hoffman, D., 461 Purdie, D.A. See Howarth, M.J., 52 Raupp, M.J. See Denno, R.F., 415 Purschke, G. See Tzetlin, A.B., 120 Raxworthy, C.J., 424 Purves, M.G. See Xavier, J.C., 322 Read, A., 462 Pye, S.E. See Johnson, M.P., 419 Read, A.J., See Wilson, B., 464 Read, J. See Ayre, D.J., 412 Redder, C. See Dee, D.P., 51 Q Reddy, P.S. See Fingerman, M., 79 Reece, A.R. See Abdalla, A.M., 117 Quillin, K.J., 119 Reed, A. See Boudreau, B.P., 117 Quiñoá, E., 271 Reed, K.C. See Soriente, A., 273 See Castedo, L., 260 Rees, E.I.S. See Davenport, J., 415 See Jiménez, C., 268 Reeves, R.R., 462 See Würsig, B., 464 Rehm, A.E., 424 R Reid, D.G., 424, 462 See Beare, D.J., 459 Rabinovich, A.B. See Kulikov, E.A., 421 See Williams, S.T., 428 Racioppi, R., 271 See Zheng, X., 464 Radach, G., 1Ð60, 54, 55 Reid, J.B., 462 See Berlamont, J., 51 Reid, P. See Edwards, M., 460 See Baumert, H., 51 Reid, P.C. See Beaugrand, G., 459 See Eigenheer, A., 51 See Edwards, M., 460 See Kühn, W., 52 Reid, R.J. See MacLeod, C.D., 462 See Laane, R.W.P.M., 52 See Thompson, P.M., 463, See Lenhart, H.-J., 52 See Wilson, B., 464 See Moll, A., 53 Reijinders, P.J.H., 463 See OSPAR, 54 See de Swart, R.L., 460 See Pätsch, J., 54 Reiner, M., 119 See Sündermann, J., 55 Reinhardt, J.T., 320 See Visser, M., 55 Reipschläger, A. See Pörtner, H.O., 462 Radford, P.J. 55 Reis, C.S., 320 See Allen, J.I., 50 Reise, K. See Grimm, V., 417 Radha, T., 81 Relini, L.O. See Drava, G., 78 Radic, Z. See Abramson, S.N., 258 Remaley, S. See Schmitz, F.J., 272 Raff, R.A. See McMillan, W.O., 422 Remeslo, A.V. See Arkhipkin, A.I., 459 Rafii, S. See Hellou, J., 267 Renzulli, L. See Fontana, A., 264 Raga, J.A. See Aguilar, A., 459 Reuben, J.P. See Chiarandini, D.J., 78 See Evans, P.G.H., 460 Reusch, T.B.H., 424 See Van Bressem, M.F., 464 See Bockelmann, A.C., 413 Ragonese, S. See Jereb, P., 319 See Olsen, J.L., 423 Rahamim, Y. See Gillor, O., 266 Reydellet, G. See Geng, J., 118 Rahman, A. See Schmitz, F.J., 272 Reyero, M.I. See Hernández, M., 461

487 7044_Idx.fm Page 488 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Reynolds, J.D. See Perry, A.L., 462 Rogers, C.N., 271, 272 Reynolds, J.E., 463 See De Nys, R., 263 Reznichenko, O.G. See Tsikhon-Lukanina, E.A., 427 Rogers, D.J., 272 Rhoads, D.C., 119 Rogers, S.D., 272 Ribera, M.A. See Boudouresque, C.F. 185 Rolán-Alvarez, E. See Cruz, R., 415 See Ferrer, E., 187 See Pérez-Figueroa, A., 424 Ribes, M., 192 Romaña, L.A. See Arnoux, A., 183 See Coma, R., 186 Romano, J. C., 192 Ricciardi, D. See Fontana, A., 264 Romero, J. See Ros, J., 192 Riccio, R. See Minale, L., 270 Romero, L.M., 424 Rice, D.W., 463 Root, T.L., 463 Richards, A.F., 424 Roper, C.F.E., 321 Richardson, A.J. See Edwards, M., 460 See Sweeney, M.J., 321 Richardson, D.H.S. See Nieboer, E., 80 See Vecchione, M., 322 Rickard, E. See Colgan, D.J., 414 Ros, J., 192 Ridd, P.V. See Stieglitz, T., 426 See Bibiloni, M.A., 184 Ridderinkhof, H., 55 See Gili, J.M., 188 See van den Berg, A.J., 55 See Huelin, M.F., 189 Riddle, M.J. See Lewis, P.N., 421 See Marín, A., 270 Ridgeway, S.H., 463 Rosa, R., 321 Ridout, P.S., 81 Rosales, J.M. See García-Raso, J.E., 187 Ridoux, V. See, Wilson, B., 464 Rosell, D., 192 Riedl, R., 192 See Uriz, M. J., 194 Rosenberg, R. See Baden, S.P., 77 Riegman, R. See van den Berg, A.J.,55 Rosenthal, R. See Dayton, P.K., 415 Riera, F., 192 Rosenzweig, C., See Root, T.L., 463 See Mayol, J., 191 Ross, H.M. See Kennedy, S., 461 Riera, T. See Coma, R., 186 See Thompson, P.M., 463 Riguera, R. See Castedo, L., 260 Ross, P.S., 463 See Jiménez, C., 268 See de Swart, R.L., 460 See Quiñoá, E., 271 See van Bressem, M.F., 464 Riisgård, H.U., 119 Ross, W.N., 81 Rindi, F. See Airoldi, L., 183 Rossi, L., 193 Rio, M. See Boletzky, S.v., 318 Rossi, S., 193 Rippeth, T.P. See Burchard, H., 51 Roughgarden, J., 424 Risbec, J., 271 Rouse, G.W., 119 Riser, K.L. See Tegner, M.J., 426 Rousseau, V. See Lancelot, C., 52 Ritland, K. See Travis, S.E., 427 Roux, M., 321 Rivoire, G., 192 See Boletzky, S.v., 318 Roast, S.D., 119 Rowden, A.A. See Edwards, M., 460 Robert, P. See Harmelin, J.G., 189 Rowles, T. See Scholin, C.A., 463 Robertson, D.R. See Lessios, H.A., 421 Rowley, A.R. See Ratcliffe, N.A., 81 See Swearer, S.E., 426 Roy, M.S. See Perrin, C., 424 Robertson, M.R. See Heath, M.R., 461 See Sponer, R., 425 Robertson, S. See Heath, M.R., 461 See Waters, J.M., 427, 428 Robinson, A.R. See Popova, E.E., 54 Royal Society, 463 Robinson, I. See Hernández, M., 461 Rozbaczylo, N., 119 Robinson, L. See Peterson, M.A., 424 Ruardij, P., 55 Robinson, R.A. See Learmonth, J.A., 431Ð464 See Baretta, J.W., 50, 51 Robson, G.C., 320, 321 See Lenhart, H.-J., 52 Rodaniche, A.F., 321 See Michielsen, B., 53 Rodhouse, P.G. See Allcock, A.L., 411 See van den Berg, A.J., 55 See Waluda, C.M., 464 Ruble, J.R. See Ireland, C., 268 See Xavier, J.C., 322 Ruddick, K. See Lancelot, C., 52 Rodríguez-Prieto, C. See Ballesteros, E., 183 See Proctor, R., 54 Roe, H.S.J. See Ridout, P.S., 81 Rudel, T. See Butzke, D., 260 Roeleveld, M.A.C. See Knudsen, J., 319 Rudman, W.B., 272 Rogan, E. See Jepson, P.D., 461 See Wägele, H., 275 Rogers, A.D. See Jolly, M.T., 420 Ruitton, S. See Piazzi, L., 192

488 7044_Idx.fm Page 489 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Ruiz, G.M. See Swearer, S.E., 426 Sasaki, M., 321 Rukhovets, L. See Dee, D.P., 51 Sasekumar, A. See Alongi, D.M., 411 Rumpho, M.E., 272 Sawada, T. See Segawa, S., 425 Russo, C.A.M., 424 Scamacca, B. See Battiato, A., 184 See Vianna, P., 427 See Cormaci, M., 186 Russo, G.F., 193 See Furnari, G., 187 Rützler, K., 193 Schama, R. See Vianna, P., 427 Ruzzante, D.E. See Anderson, L.W., 459 Schartau, M., 55 Ryba, S.A. See Voparil, I.M., 120 Schefer, A.B. See Granato, A.C., 267 Ryland, J.S. See Porter, J.S., 424 Scheltema, R.S., 424 Schermutzki, F. See Gemballa, S., 266 Scheuer, P.J., 272 S See Becerro, M.A., 259 See Horgen, F.D., 267 Sabates, A. See Corbera, J., 186 See Ireland, C., 268 Saeki, M. See Gillete, R., 266 See Okuda, R.K., 271 Saenz, V. See Blasco, J., 77 See Poiner, A., 271 Saethre, B.A. See Fredriksen, S., 417 See Szabo, C.M., 273 Sage, G.K. See Muñiz-Salazar, R., 422 Scheunert, I., Hoffman, D., 461 Saier, B. See Buschbaum, C., 413 Schiaparelli, S. See Cattaneo-Vietti, R., 261 Sakai, R., 272 See Cerrano, C., 185 Sakamoto, B. See Horgen, F.D., 267 Schiffelbein, P., 120 Sala, E., 193 Schinner, G.O., 120 See Ballesteros, E., 183 Schlangen, E., 120 See Garrabou, J., 188 Schlichting, R. See Fountain, A.G., 118 See Gerber, L.R., 417 Schlining, B. See Drazen, J.C., 318 See Zabala, M., 195 Schlüter, M. See Luff, R., 53 Salas, C., 193 Schmidt, J.L., 120 Salden, R. See Proctor, R., 54 Schmitt, B.C., 81 Sale, P.F. See Mora, C., 422 Salihoglu, I. See Balkas, T.I., 77 Schmitz, F.J., 272 Salman, A. See Laptikhovsky, V., 320 See Cimino, G., 262 Salomon, J.C. See Proctor, R., 54 See Fu, X., 265 Salva, J. See Ortega, M.J., 271 See Gopichand, Y., 266 Sampson, S. See Thiel, M., 427 See Ksebati, M.B., 269 Samuel, M.D. See Harvell, C.D., 461 Schneider, K. See, Wilson, B., 464 Samuelsson, M.-O. See Magnusson, K., 80 Schneider, S.H. See Root, T.L., 463 Sanchez, P., 321 Schofields, O. See Moline, M.A., 462 See Villanueva, R., 322 Scholin, C.A., 463 Sanders, G.D. See Packard, A., 320 Schoonbee, H.J. See Steenkamp, V.E., 82 Sanders, M.J., 81 Schrader, S. See Keudel, M., 119 Sanjabi, B. See Olsen, J.L., 423 Schrödl, M., 272 Santamarina, J.C., 119 See Haumayr, U., 267 Santana-Ortega, A.T. See Castro, J.J., 414 See Vonnemann, V., 274 Santangelo, G., 193 Schrum, C., 55 See Abbiati, M., 182 Schug, M.D. See Parker, P.G., 423 See Bramanti, L., 185 Schultz, H. See Sündermann, J., 55 Santelices, B. See Ojeda, F.P., 423 See Visser, M., 55 Santer, B.D. See Gates, W.L., 52 Schulz, F.N., 272 Santiago, J.A. See Castro, J.J., 414 Schulze, A., 272 Santos, M.B. See Learmonth, J.A., 431Ð464 Schwaninger, H.R., 425 Sara, G. See Cerrano, C., 185 Schweder, C.S. See MacLeod, C.D., 462 Sarà, M., 193 Scopa, A. See Cimino, G., 262 Saric, M., 81 Scott, M.D. See Wells, R.S., 464 Sarmiento, J.L. See Fasham, M.J.R., 51 Scott, T., 321 Sartoretto, S., 193 Sear, C., 463 See Garrabou, J., 188 Sedell, J.R. See Maser, C., 422 See Laborel, J., 189 Segawa, S., 425 See Perez, T., 191 Segonzac, M. See Villanueva, R., 322

489 7044_Idx.fm Page 490 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Seibel, B.A., 321 See Proctor, R., 54 See Hunt, J.C., 319 See Delhez, E.J.M., 51 Selander, E., 82 See Reid, D.G., 462 Self, R.F.L., 120 See Stipa, T., 55 Selkoe, K.A. See Swearer, S.E., 426 Skogen, M.D., 55 Semroud, R. See Boudouresque, C.F., 185 See Soiland, H., 55 Sengupta, P.K. See Schmitz, F.J., 272 Sköld, M., 425 Serra, J. See Canals, M., 185 Slater, R.D. See Fasham, M.J.R., 51 Serrão, E. See Billard, E., 412 Slatkin, M., 425 See Olsen, J.L., 423 Slattery, M., 273 Serrão, E.A. See Coyer, J.A., 415 See Avila, C., 259 See Diekmann, O.E., 416 See McClintock, J.B., 270 Sewell, M.A. See Appleton, D.R., 258 Sleeper, H.L. See Fenical, W., 264 Seymour, M.K., 120 Slinn, D.J. See Thompson, T.E., 274 Shaffer, J.A., 425 Slobodov, S.A., 425 Shahidi, F. See Heu, M.-S., 79 Smale, M.J., 321 Shane, S.H., 463 Smith, B.D. See Fialkowski, W., 78 Shanks, A. See Sponaugle, S., 425 See Rainbow, P.S., 81 Shanks, A.L., 425 Smith, C. See Lee, J.-Y., 52 See Grantham, B.A., 417 Smith, C.R. See Distel, D.L., 416 Shaughnessy, P.D., 463 Smith, E.L. See White, A., 83 Sheader, M. See Jolly, M.T., 420 Smith, G.J. See Coyer, J.A., 415 Sheldrick, M.C. See Kuiken, T., 462 Smith, G.W. See Harvell, C.D., 461 Smith, J.N. See Mulsow, S., 119 Shepheard, P., 82 Smith, M.J. See Arndt, A., 411 Sherwood, C.R., 120 Smith, S.D.A., 425 Shima, J.S. See Swearer, S.E., 426 See Lewis, P.N., 421 Shimamoto, K. See Kawamine, K., 269 Smith, T.B. See Calsbeek, R., 414 Shinoda, K. See Fusetani, N., 265 Smith, T.J. See Krauss, K.W., 421 Shorrocks, B. See Davis, A.J., 460 See Romero, L.M., 424 Shrader-Frechette, K. See Oreskes, N., 53 Snelgrove, P.V.R. See Bradbury, I.R., 413 Shugart, L.R. See Costa, F.O., 415 Snow, A.A. See Parker, P.G., 423 Shukla, G.S., 82 Snyder, M. See Wilson, A.B., 428 Shull, D.H., 120 Snyder, T.P., 425 Si, A., 425 Sodano, G., 273 Siccardi, A. See Cerrano, C., 185 See Avila, C., 259 Siciliano, S. See Van Bressem, M.F., 464 See Castiello, D., 261 Siddorn, J. See Allen, J.I., 50 See Cimino, G., 261, 262 Siegel, D. See Guichard, F., 418 See Gavagnin, M., 266 Siegel, D.A., 425 See Giordano, A., 266 Sigg, L. See Johnson, C.A., 79 See Porcelli, M., 271 Sigurdsson, H. See Carey, S., 414 See Racioppi, R., 271 Silvagni, P. See Scholin, C.A., 463 See Soriente, A., 273 Silver, M. See Scholin, C.A., 463 Söderhäll, I. See Hernroth, B., 79 Silvestre, R. See Templado, J., 194 Söderhäll, K., 82 Simberloff, D.S., 425 See Chaga, O., 78 Simkiss, K., 82, 193 Soiland, H., 55 Simpson, J.H. See Charnock, H., 51 See OSPAR, 54 Simpson, J.S., 273 See Skogen, M.D., 55 See Garson, M.J., 265 See Stipa, T., 55 Simpson, R.D. See Smith, S.D.A., 425 Sokolova, I.M., 425 Sims, D.W. 463 Solana-Sansores, R., 425Solan, M., 120 Singhal, R.L. See Shukla, G.S., 82 Sole-Cava, A.M. See Russo, C.A.M., 424 Sinnassamy, J.M. See Boudouresque, C.F., 185 Solferini, V.N. See Andrade, S.C.S., 411 Sirota, A M. See Arkhipkin, A.I., 459 Soriano, O. See Ortiz, A., 191 Sissener, E.H., 463 Soriente, A., 273 Six, K. D. See Stephens, B.B., 55 Sotka, E.E., 425 Skelton, B.W. See Jongaramruong, J., 268 Souissi, S. See Beaugrand, G., 459 Skogen, M., See OSPAR, 54 Southard, J.B. See Nowell, A.R.M., 119

490 7044_Idx.fm Page 491 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Southward, A.J., 463 Stevens, L.M., 426 See Sims, D.W., 463 See Winston, J.E., 428 Span, A. See Boudouresque, C.F., 185 Stevens, M.I., 426 Spanier, E., 193 Stevenson, T.D.I. See Davenport, J., 415 Spencer, H.G. See Donald, K.M., 416 Stieglitz, T., 426 See Waters, J.M., 427 Stipa, T., 55 Sperber, K.R. See Gates, W.L., 52 Stirling, I., 463 Spicer, J.I., 82 See Ferguson, S.H., 460 See Baden, S.P., 77 Stoddart, J.A., 426 Spinella, A., 273 Stoner, D.S., 426 See Avila, C. 259 Stovold, R.J., 120 See Cimino, G., 261, 262 Strasser, M. See Grimm, V., 417 See Fontana, A., 264 Strathmann, M.F., 426 See Gavagnin, M., 266 Strathmann, R.R., 426 See Giordano, A., 266 See Dethier, M.N., 415 See Izzo, I., 268 Strazzullo, G. See Cimino, G., 262 See Marín, A., 270 See Racioppi, R., 271 See Sodano, G., 273 Streble, H., 273 Spitz, Y. See Lancelot, C., 52 Stroo, D., 55 Sponaugle, S., 425 Stuart, A.E. See Ross, W.N., 81 Sponer, R., 425 Styan, C. See Ayre, D.J., 411 Sponga, F. See Cerrano, C., 185 Suarez-Kurz, G., 82 Spraker, T. See Scholin, C.A., 463 Subrahmanyam, M.N.V. See Al-Mohanna, S.Y., 77 Squires, D.F. See Kornicker, L.S., 420 Subramoniam, T., 82 Srokosz, M.A. See Popova, E.E., 54 See Radha, T., 81 St. Aubin, D.J. See Geraci, J.R., 460 Sullivan, J.K. See Krauss, K.W., 421 Stachowicz, J.J., 273 Summer, E.J. See Rumpho, M.E., 272 Stagg, R.M. See Rankin, J.C., 81 Sun, H.H. See Fenical, W., 264 Stakes, D.S. See Drazen, J.C., 318 Sun, Y. See Wei, H., 56 Sündermann, J., 55 Stallard, M.O. See Fenical, W., 264 See Berlamont, J., 51 Stam, W.T. See Coyer, J.A., 415 See Laane, R.W.P.M., 52 See Diekmann, O.E., 416 See Visser, M., 55 See Engelen, A.H., 416 Sundstrom, B. See Jorhem, L., 79 See Miller, K.A., 422 Sunnucks, P., 426 See Olsen, J.L., 423 Sutherland, F.L., 426 Stanisic, J., 273 Svavarsson, J., 426 Stanley, S.M., 120 Svendsen, E. See OSPAR, 54 Stanton, R.J., Jr. See Alexander, R.R., 117 See Skogen, M.D., 55 Starczak, V.R. See Lessios, H.A., 421 Swartz, S.L. See Jones, M.L., 461 Starmer, J. See Avila, C., 259 Swearer, S.E., 426 See Slattery, M., 273 Sweeney, M.J., 321 Statham, P.J. See Hall, I.R., 79 Swift, D.J., 82 Stebbing, A.R.D., 463 Szabo, C.M., 273 Steenkamp, V.E., 82 Stefanni, S. See Coll, J., 186 Stegenga, H., 425 T Steinberg, P.D. See De Nys, R., 263 See Rogers, C.N., 271, 272 Tabor, A. See Luyten, P.J., 53 Steiner, J.R. See Dumdei, E.J., 263 Tachino, N. See Palumbi, S.R., 423 Steinke, T.D., 426 Taglialatela-Scafati, O. See Constantino, V., 262 Steneck, R.S., 426 Takahashi, K. See Hagiwara, S., 79 See Vadas, R.L., 194 See Okamoto, H., 81 Stenseth, N., 463 Takeda, K., 82 Stepanjants, S.D., 426 Takeuchi, R. See Kawamine, K., 269 Stephens, B.B., 55 Taki, I., 321 Stern, S. J., 463 Talbot, S.L. See Muñiz-Salazar, R., 422 Sterrer, W., 426 Tallamy, D.W. See Denno, R.F., 415 Stevens, D. See Reid, D.G., 462 Talley, T.S. See Levin, L.A., 421

491 7044_Idx.fm Page 492 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Tallkvist, J. See Henriksson, J., 79 Thorrold, S.R. See Swearer, S.E., 426 See Tjälve, H., 82 Thorson, G., 427 Tanaka, T. See Toyama, Y., 274 Thuesen, E.V. See Seibel, B.A., 321 Tarp, B. See Riisgård, H.U., 119 Thurston, M.H. See Collins, M.A., 318 Tartinville, B. See Proctor, R., 54 Tien, R. See Voparil, I.M., 120 Tasker, M.L. See Northridge, S.P., 462 Tillier, S. See Dayrat, B., 262 Tatarenkov, A. See Johannesson, K., 419 Timmerman, H.H. See de Swart, R.L., 460 Tatman, S. See MARE Consortium, 53 Timmerman, K., 120 Taylor, A.C. See Atkinson, R.J.A., 117 Timperi, R.J. See Geraci, J.R., 460 See Field, R.H., 79 Tirendi, F. See Alongi, D.M., 411 Taylor, A.H. See Planque, B., 462 Tischler, M., 274 Taylor, H.H., 82 Tjälve, H., 82 Taylor, K.E. See Gates, W.L., 52 See Henriksson, J., 79 Taylor, M.G. See Simkiss, K., 82 Todd, C. See Soriente, A., 273 Taylor, M.S., 426 Todd, C.D., 427 Taylor, P. See Abramson, S.N., 258 See Lambert, W.J., 421 Taylor, P.D. See Watts, P.C., 428 Toll, R.B. See Hochberg, F.G., 319 Taylor, R.J.K. See De Medeiros, E.F., 263 Tolley, K.A. See Bj¿rge, A., 459 Teal, J.M., 426 Tollit, D.J. See Thompson, P.M., 463 Teeyapant, R., 273 Tomas, F. See Ballesteros, E., 183 Tegner, M.J., 426 Tomaselli, V. See Basso, D., 184 See Dayton, P.K., 415 Topcu, D.H. See Brockmann, U., 51 See Steneck, R.S., 426 Torquato, S., 120 Templado, J., 193, 194 Torre-Cosio, J. See Pfeiler, E., 424 See Becerro, M.A., 259 Torrents, O., 194 See Grande, C., 267 Tortonese, E., 194 Terrassa, J. See Riera, F., 192 See Whitehead, P.J.P., 195 Tett, P. See Lee, J.-Y., 52 Toyama, Y., 274 See Luyten, P.J., 53 Trahms, J. See Radach, G., 55 Tett, P.B., 55 Trainer, V. See Scholin, C.A., 463 See Charnock, H., 51 Tramice, A. See Fontana, A., 264 Thamdrup, B. See Canfield, D.E., 78 Trathan, P.N. See Waluda, C.M., 464 Thayer, G. See Bach, S., 412 Travis, S.E., 427 Theodorakis, C.W. See Costa, F.O., 415 See Proffitt, C.E., 424 Thewissen, J.G.M. See Perrin, W.F., 462 Treble, M.A. See Laidre, K.L., 462 Thiebaut, E. See Jolly, M.T., 420 Thiel, M., 323Ð429, 426, 427 Trefry, J.H., 82 See Macaya, E.C., 421 Trevor, J.H., 120 Thim, A.M. See Jorhem, L., 79 Trinchese, S., 274 Thiriot-Quiévreux, C. See Lapègue, S., 421 Trivellone, E. See Avila, C., 259 Thompson, J.E., 273 See Ciavatta, M.L., 261 See Hellou, J., 267 See Cimino, G., 262 Thompson, P.M., 463 See Fontana, A., 264, 265 See Wilson, B., 464 See Gavagnin, M., 266 Thompson, R.C., 427 Trocine, R.P. See Trefry, J.H., 82 Thompson, S.Y. See Fisher, L. R., 264 Trott, L.A. See Alongi, D.M., 411 Thompson, T.E., 273, 274 Trowbridge, C.D., 274 See Burn, R., 260 True, M.A., 194 See Edmunds, M., 263 Trueman, E.R., 120 See Yonge, C.M., 121 See Ansell, A.D., 117 Thoms, C., 274 See Brown, A.C., 117 Thomson, R.E. See Kulikov, E.A., 421 Tsikhon-Lukanina, E.A., 427 Thomson, S. See Hydes, D.J., 52 Tsuchiya, M. See Mfilinge, P.L., 422 Thornton, I.W.B., 427 Tsurnamal, M. See Marbach, A., 269 Thorpe, J.P. See Allcock, A.L., 411 Tugrul, S. See Balkas, T.I., 77 See Lambert, W.J., 421 Tully, O., 427 See Russo, C.A.M., 424 Turk, S.M.T. See Stebbing, A.R.D., 463 See Todd, C.D., 427 Turnpenny, J.R. See Hulme, M., 461 See Watts, P.C., 428 Turon, X., 194, 274

492 7044_Idx.fm Page 493 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

See Ballesteros, E., 184 van Leussen, W. See Laane, R.W.P.M., 52 See Becerro, M.A., 184, 259 See Sündermann, J., 55 See Duran, S., 416 Van Loveren, H. See de Swart, R.L., 460 See Jimeno, A., 189 Vannel, L. See Geng, J., 118 See Martí, R., 190 Vannini, M. See Fratini, S. 417 See Uriz, M.J., 194 van Oppen, M.J.H. See Mackenzie, J.B., 421 Turrell, W.R. See Hansen, B., 461 van Raaphorst, W. See Berlamont, J., 51 See Heath, M.R., 461 See Laane, R.W.P.M., 52 Twilley, R.R. See Krauss, K.W., 421 See Radach, G., 54 Tyack, P.I. See Mann, J., 462 See Ruardij, P., 55 Tynan, C.T., 463 See Sündermann, J., 55 Tzetlin, A.B., 120 See Visser, M., 55 van Soelen, J. See Hemminga, M.A., 418 VanVuren, J.H.J. See Sanders, M.J., 81 U Van Waerebeek, K. See Van Bressem, M.F., 464 Vardaro, R.R. See Avila, C. 259 Ulrich, M. See Johnson, C.A., 79 See Gavagnin, M., 266 Ulvestad, K.B. See Skogen, M.D., 55 Vaselli, O. See Gherardi, F., 79 Underwood, A.J., 427 Vásquez, J.A., 427 Ungur, N. See Fontana, A., 264 See Macaya, E.C., 421 See Gavagnin, M., 266 See Thiel, M., 427 Urgorri, V. See Calado, G., 260 Vásquez, N.R. See Macaya, E.C., 421 Urian, K.W. See Wilson, B., 464 Vassar, J.M. See Adey, W.H., 182 Uriz, M.J., 194 Vassort, G. See Mounier, Y., 80 See Ballesteros, E., 184 Vasta, G.R. See Harvell, C.D., 461 See Becerro, M.A., 259 Vaughan, D.G., 464 See Mariani, S., 190 Vayssière, A.J.B.M., 274 See Martí, R., 190 Vecchione, M., 321, 322 See Rosell, D., 192 See Carlini, D.B., 318 See Turon, X., 194, 274 See Young, R.E., 322 Uthicke, S. See Bastidas, C., 412 Vedder, L.J. See de Swart, R.L., 460 Vega, J.M.A. See Macaya, E.C., 421 V Veit, R.R. See Helmuth, B., 418 Veldsink, J. See Olsen, J.L., 423 Vacelet, J. See Perez, T., 191 Velimirov, B., 194 Vadas, R.L., 194 See Weinbauer, M.G., 194 Vaissière, R., 194 Vellend, M., 427 Valdés, A., 274 Ven Tresca, D. See Dayton, P.K., 415 See Muniaín, C., 270 Ventriglia, M. See De Petrocellis, L., 263 See Ortea, J., 271 Verhagen, J.H.G. See Fransz, H.G, 51 Valdivia, N.A. See Macaya, E.C., 421 Verlaque, M. See Boudouresque, C.F., 185 Valero, M. See Billard, E., 412 See Piazzi, L., 192 Vallentin, R., 427 See Sartoretto, S., 193 Van Bressem, M. See Domingo, M., 460 Vernet, M. See Moline, M.A., 462 Van Bressem, M.F., 464 Veron, G. See Yoder, A.D., 429 van den Berg, A.J., 55 Verrill, A.E., 322 See Michielsen, B.,53 Vested, H.J. See OSPAR, 54 van den Eynde, D. See Sündermann, J., 55 See Proctor, R., 54 See Visser, M., 55 Vetter, E.W., 427 van den Hoff, J. See Goldsworthy, S.L., 319 Veuille, M. See Magalon, H., 422 Vandendriessche, S., 427 Vevers, H.G. See Kennedy, G.Y., 269 Van Der Helm, D. See Schmitz, F.J., 272 Veyret, M. See Le Gac, M., 421 van der Tol, M.W.M. See Michielsen, B., 53 Vianna, P., 427 Van Dolah, F.M. See Scholin, C.A., 463 Viard, F. See Dupont, L., 416 van Eeckhout, D. See Lancelot, C., 52 See Jolly, M.T., 420 van Eeden, P.H. See Steenkamp, V.E., 82 Viarengo, A., 82 Van Gansbeke, D. See Dehairs, F., 78 Vicente, N., 194 Van Holde, K.E., 82 Vickerman, K. See Field, R.H., 79

493 7044_Idx.fm Page 494 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Vieti, R. See Boero, F., 184 Waluda, C.M., 464 Vighi, M., 194 Ward, C.J. See Steinke, T.D., 426 Villani, G. See Ciavatta, M.L., 261 Ward, D.H. See Muñiz-Salazar, R., 422 See Cimino, G., 262 Ward, E. See Bryan, G.W., 78 See Fontana, A., 265 Ward, E.E., 82 See Gavagnin, M., 265 Ward, J.R. See Harvell, C.D., 461 See Spinella, A., 273 Wares, J.P., 427 Villanueva, R., 322 See Sotka, E.E., 425 See Collins M.A., 277Ð322 Warmoes, T. See Johannesson, K., 419 See Guerra, A., 319 Warner, R.R. See Carr, M.H., 414 Villard, A.M. See Féral, J.P., 416, 417 See Swearer, S.E., 426 Villareal, M.R. See Burchard, H., 51 Warrant, E.J., 322 Villars, M. See OSPAR, 53 Wartel, M. See Nassrallah-Aboukais, N., 80 Vincent, A.C.J. See Lourie, S.A., 421 Waters, J.M., 427, 428 Vincx, M. See Vandendriessche, S., 427 Watling, L., 121 Virgilio, M., 427 See Thiel, M., 427 Visser, M., 55 Watts, P.C., 428 See Sündermann, J., 55 Waycott, M., 428 Visuthismajarn, P., 82 Weaver, A.J., 464 Vitayavirasuk, B. See Visuthismajarn, P., 82 Webb, A., Northridge, S.P., 462 Voight, J.R., 322 Webb, N.R. See Coulson, S.J., 415 Voltzow, J., 274 Webber, D.M. See O'Dor, R.K., 320 Vonnemann, V., 274 Weber, A. See Radach, G., 55 See Wägele, H., 275 Weber, H.C., 428 Voogt, P.A., 274 Weber, R.E. See Spicer, J.I., 82 Voparil, I.M., 120 Weeks, J.M. See Baden, S.P., 77 Vos, J.G. See de Swart, R.L., 460 Wehrtmann, I.S., 428 See Ross, P.S., 463 Wei, H., 55, 56 Voss, G.L., 322 See Zhao, L., 56 Voss, N.A. See Villanueva, R., 322 Weidemann, H. See Lenz, W., 53 Weigel, P., 56 Weinbauer, M.G., 194 W Weinberg, F. See Weinberg, S., 195 Weinberg, J.R. See Hare, M.P., 418 Waddy, S.L. See Aiken, D.E., 76 See Lessios, H.A., 421 Wägele, H., 197Ð276, 275 Weinberg, S., 195 See Burghardt, I., 260 Weinmayr, G. See Jolly, M.T., 420 See Hain, S., 267 Weinstein, J.E., 82 See Kolb, A., 269 Weiss, G.H. See Kimura, M., 420 See Schrödl, M., 272 Weiss, K., 275 See Schulze, A., 272 Wells, M.J., 322 See Vonnemann, V., 274 Wells, M.G. See Bryan, S.E., 413 See Weiss, K., 275 Wells, P.G. See Rand, G.M., 81 See Wollscheid-Lengeling, E., 276 Wells, R.S., 464 Wägele, J.W. See Wägele, H., 275 See Wilson, B., 464 Wagner, M. See Hentschel, U., 267 Wennberg, L. See Magnusson, K., 80 Wahidulla, S. See Fontana, A., 264 West, J. See Radford, P. J., 55 See Manzo, E., 269 West, J.E. See Shaffer, J.A., 425 Walker, R.P., 275 West, T.L. See Weinstein, J.E., 82 See Okuda, R.K., 271 Westerlund, A. See Stipa, T., 55 See Thompson, J.E., 273 Whalan, S., 428 Wallmann, K. See Luff, R., 53 Whalley, W.R. See Stovold, R.J., 120 Walne, A. See Tett, P.B., 55 Wheatcroft, R.A. See Sherwood, C.R., 120 Walsh, J.J. See Gregg, W.W. 52 Wheeler, A. See Stebbing, A.R.D., 463 Walther, G.-R., 464 Wheeler, W.M., 428 Walther, P. See Martin, R., 270 Whelan, K.R.T. See Krauss, K.W., 421 Walther, S.M. See Davis, J.L.D., 415 White, A., 83 Walton, M. See Anderson, L.W., 459 White, A.H. See Jongaramruong, J., 268 See Kuiken, T., 462 White, S.L., 83

494 7044_Idx.fm Page 495 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

Whitehead, H., 464 Wörheide, G., 429 See Mann, J., 462 Wratten, S.J. See Thompson, J.E., 273 Whitehead, P.J.P., 195 Wray, J.L., 195 Whiters, N.W., 275 See James, N.P., 189 Whitfield, M. See Herring, P.J., 319 Wray, V. See Teeyapant, R., 273 Whitlock, M.C., 428 Wright, A.D., 276 Wiberg, P.L. See Sherwood, C.R., 120 Wright, S., 429 Widder, E.A. See Johnsen, S., 319 Wursig, B., 464 Widdicombe, S. See Olsen, J.L., 423 See Perrin, W.F., 462 Widdows, J. See Roast, S.D., 119 Wyllie-Echeverria, S. See Olsen, J.L., 423 Wijsman, J. See MARE Consortium, 53 Wild-Allen, K. See Lee, J.-Y., 52 X See Luyten, P.J., 53 Wildish, D.J., 428 Xavier, J.C., 322 Wiley, D.N., 464 Xiao, X.H., 83 Wilhelmsen, U., 428 Wilke, T., 428 Y Wilkes, J.O., 121 Willan, R.C., 275 Yalamanchili, G. See Cimino, G., 262 See Foale, S.J., 264 Yamada, K., 276 See Hain, S., 267 See Higuchi, R., 267 See Wägele, H., 275 Yamagishi, S., 83 Willenz, P. See Turon, X., 194 Yamamura, S. See Arimoto, H., 258 Williams, D.N. See Gates, W.L., 52 Yamashita, N. See Okamoto, H., 81 Williams, J.M., Northridge, S.P., 462 Yamazaki, M. See Iijima, R., 268 Williams, J.P. See da Silva, J.J.R.F., 78 Yannicelli, B., 121 Williams, M. See Goldsworthy, S.L., 319 Yasuda, M. See Shull, D.H., 120 Williams, R. See Fasham, M.J.R., 51 Yau, C. See Collins, M.A., 318 Williams, R.J.P., 83 Yeung, C., 429 Williams, S.T., 428 Yingst, J.Y. See Rhoads, D.C., 119 See Benzie, J.A.H., 412 Yoder, A.D., 429 Williamson, G.R. See Boyle, P.R., 318 Yohe, G., Parmesan, C., 462 Willis, B.L. See Mackenzie, J.B., 421 Yonge, C.M., 121 Willows, A.O.D. See Johnson, P.M., 268 Yonow, N., 276 Wilson, A.B., 428 Yoshida, T. See Segawa, S., 425 Wilson, B., 464 Yoshida, W. See McClintock, J.B., 270 Wilson, C. See Heath, M.R., 461 Yoshida, W.Y., 276 Wilson, E.O. See MacArthur, R.H., 421 See Bryan, P.J., 260 See Simberloff, D.S., 425 See Szabo, C.M., 273 Wilson, J. See Radach, G., 54 Yoshimura, E. See Hirota, H., 267 Wing, S.R. See Perrin, C., 424 See Okino, T., 271 See Sköld, M., 425 Younes, W.A.N. See Romano, J. C., 192 Winn, H.E. See Kenney, R.D., 461 Young, C.M., 276, 429 Winston, J.E., 428 See Bingham, B.L., 413 Winter, D.P.E. See Nel, R., 119 Young, J.W. See Goldsworthy, S.L., 319 Wise, J.B., 275 Young, J.Z. See Aldred, R.G., 317 Wishart, J. See Ayre, D.J., 412 Young, L.B., 83 Witte, L. See Teeyapant, R., 273 Young, R.E., 322 Witter, R.C., 428 See Carlini, D.B., 318 Woelkerling, W.J., 195 See Vecchione, M., 322 Wolff, T., 428 Yu, C.S. See Berlamont, J., 56 Wollast, R., 83 Yu, Z. See Wei, H., 56 Wollscheid-Lengeling, E., 276 Wolstenhome, H.J. See Fusetani, N., 265 Z Wonham, M.J., 428 Wood, C. See, Wilson, B., 464 Zabala, M., 195 Wood, S. See Davis, A.J., 460 See Ballesteros, E., 183, 184 Woodbury, M.M. See Dethier, M.N., 186 See Coma, R., 186 Worcester, S.E., 428 See Garcia-Rubies, A., 187

495 7044_Idx.fm Page 496 Tuesday, April 25, 2006 1:43 PM

AUTHOR INDEX

See Garrabou, J., 188 Zehr, S. See Yoder, A.D., 429 See Linares, C., 189 Zhadan, A. See Tzetlin, A.B., 120 See Llobet, I., 190 Zhao, L., 56 See Sala, E., 193 See Wei, H., 55, 56 Zaccanti, F. See Goffredo, S., 417 Zheng, X., 464 Zacherl, D.C., 429 Zia, S. See Alikhan, M.A., 77 Zahtila, E. See Hrs-Brenko, M., 189 Zibrowius, H., 195 Zane, L., 429 See Arnoux, A., 183 Zanzi, D. See Bavestrello, G., 184 Zimmer, M. See Orr, M., 423 Zappia, V. See Porcelli, M., 271 See Zaragoza, E.S. See Casas, V.M., 414 Zmudzinski, L. Fialkowski, W., 78 Zarate-Villafranco, A., 429 Zobell, C.E., 429 Zardoya, R. See Grande, C., 267 Zubía, E., 276 Zavodnik, D. See Hrs-Brenko, M., 189 See Cimino, G., 261, 262 Zayed, J. See Normandin, L., 80 See Ortega, M.J., 271 Zazueta-Padilla, H.M. See Hendrickx, M.E., 79 Zuljevic, A. See Piazzi, L., 192 See Paez-Osuna, F., 81 Zwiers, F.W. See Weaver, A.J., 464

496 7044_Idx.fm Page 497 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

References to sections of articles are given in italics, references to pages are given in normal type. An asterisk (*) indicates a taxon mentioned in the colour insert.

A Akera, 257 soluta , 206, 227 Aaptos aaptos, 147, 150 Akeridae, 206 Acantephyra eximia, 65 Alcyonaria, 173 Acanthaster planci, 383 Alcyonidium, 397, 398 Acanthella acuta, *, 145, 150 gelatinosum, 347, 385, 390, 398 cavernosa, 219 mytili, 386 Acanthodoris nanaimoensis, 198 Alcyonium acaule, *, 142, 143, 145, 147, 151, 173, 180 pilosa, 210 rudyi, 377 Acantholabrus palloni, 157 Alpheus dentipes, 155, 162 Acari, 153 megacheles, 155 Acasta spongites, 154 ruber, 155 Achelia echinata, 153 Alvania cancellata, 153 Acmaea virginea, 153 lineata, 153 Acrodiscus vidovichii, 148 Amphiascus cinctus, 153 Acropora, 396, 397, 398 minutus, 153 cuneata, 376, 398 Amphilochus picadurus, 154 cytherea, 376 Amphipholis squamata, 156, 355, 385, 389, 393 hyacinthus, 376 Amphipoda, 65, 68, 154, 405, millepora, 376 Amphiroa verruculosa, 137 nasuta, 376 Amphitrite variabilis, 152 palifera, 376 Amphiura apicula, 156 palmata, 376 chiajei, 156 Acropora valida, 363, 377 filiformis, 156 Acrosorium venulosum, 148 mediterranea, 156 Acrothamnion preissii, 178 Anaitides muscosa, 152 Acteocina atrata, 204 Anaspidea, 201, 206, 228, 229, 247, 248, 253, 256, 257 Acteon, 257 Ancula, 228 tornatilis, 202, 227 gibbosa , 210 Acteonidae, 202 Anisodoris, 249 Acteonoidea, 202, 228, 247, 253, 256, 257 Annelida, 103, 146, 147, 204, 405 Actinia, 397, 398 Anolis, 366, 402 bermudensis, 377, 398 allisoni, 366 tenebrosa, 377 allisoni A. porcatus hybrid, 366 Actiniaria, 222, 223 brunneus, 366 Actinocyclus japonicus, 212 carolinensis, 366 Adalaria proxima, 347, 383, 389, 392 longiceps, 366 Adeonella calveti, 146, 156 maynardi, 366 Aegires albus, 212 porcatus, 366 Aegiridae, 212 sagrei, 338 Aeodes marginata, 148, 158 smaragdinus, 366 Aeolidia papillosa, 223 smaragdinus lerneri, 366 Aeolidiidae, 223 smaragdinus smaragdinus, 366 Aeolidoidea, 222, 248, 253 Anomia ephippium, 146, 147, 153 Aetea, 156 Antedon bifida, 156 truncata, *, 142 mediterranea, 156 Agapanthia villosoviridescens, 346 Anthias anthias, *, 145, 157 Agelas oroides, *, 142, 145, 146, 150 Anthobranchia, 209 Aglajidae, 202 Anthopleura elegantissima, 377, 393 Aglaophenia pluma, 151 Anthothoe albocincta, 377 septifera, *, 145 Anthozoa, 151, 209, 376, 397, 405 Aglaothamnion tripinnatum, 148 Aora spinicornis, 154 Aka labyrinthica, 139 Apendicularia, 221

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SYSTEMATIC INDEX

Aplidium conicum, 157 Axinella, 150, 162, 214, 219 densum, 157 damicornis, *, 146, 150, 162 Aplysia parvula, 206, 229, 251 polypoides,150 punctata, 207 verrucosa, 150 Aplysiidae, 206, 249, 257 Aplysilla glacialis, 214 aerophoba, 208, 250 B Aplysina cavernicola, 146, 147 Apogon imberbis, 157 Balaena australis, 433, 434 Arbacia lixula, 157 glacialis, 433, 434 Arca barbata, 153 mysticetus, 433, 434 Archaeolithothamnion mediterraneum, 136 Balaenidae, 434 Archidoris, 253 Balaenoptera acutorostrata, 433, 434, 440 pseudoargus, 212 bonaerensis, 434, 440 Arctocephalus pusillus doriferus, 310 borealis, 433, 434 Arenicola, 108, 116 edeni, 433 marina, 105, 107, 108, 110 edeni/brydei, 434 Argonauta, 304 musculus, 433, 434 Argyrotheca cistellula, 155 physalus, 433, 434 cordata, 155 Balaenopteridae, 434 cuneata, 155 Balanidae, 210 Aristeus antennatus, 65 Balanophyllia elegans, 377, 389, 390, 391 Armina maculata, 221 Balanus amphitrite, 72 neapolitana, 221 crenatus, 65 tigrina, 224 glandula, 379 Arminidae, 201, 221, 230, 251 perforatus, 138, 154 Arminoidea, 221, 253 Balssia gasti, 155 Artacama, 113 Barleeia subtenuis, 345 valparaisiensis, 99, 100 Bathyberthella antarctica, 209, 232, 242 Artacamella hancocki, 100 Bathydorididae, 209 Artemia, 315 Bathydoris, 253 Arthropoda, 405 clavigera, 209 Artocephalus australis, 438 hogdsoni, 209, 254 forsteri, 438 Beania, 138 galapagoensis, 438, 448 hirtissima, 146, 156 gazelle, 438, 447 magellanica, 156 philippii, 438 Bedeva hanleyi, 381, 390 pusillus, 438 Bembicium vittatum, 399 townsendi, 438 Benthoctopus, 306 tropicalis, 438 Berardius arnuxii, 434 Ascidiacea, 210 bairdii, 434, Ascophyllum 347, 354 Berthella stellata, 209, 250 nodosum, 347 Berthellina, 229 Asellus aquaticus, 66 aurantiaca, 209 Asparagopsis taxiformis, 178 citrina, 209 Aspidosiphon mülleri, 139, 152 edwardsii, 209, 229, 250 Astacus astacus, 66 Bittium reticulatum, 153 Aster tripolium, 346 Bivalvia, 383, 405 Asterina gibbosa, 384, 391 Blenniidae, 148 Asterocheres, 161 Bonellia viridis, 152 Asteroidea, 156Ð157, 383, 397, 405 Bornella anguilla, 220 Asteronotus cespitosus, 198 stellifer, 220 Astropartus mediterraneus, 156 Bornellidae, 220 Athanas nitescens, 155 Botrylloides, 343 Austrocochlea concmerata, 368 magnicoecum, 386 Austrodoris, 253 Botryllus schlosseri, *, 142 kerguelenensis, 212 Brachiopoda, 155 Austrolittorina, 401 Briareum, 224 Austropotamobius pallipes, 66 Brissopsis lyrifera, 99, 111

498 7044_Idx.fm Page 499 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

Brodiella armata, 137, 156, 163 inornata, *, 137, 145, 147, 151 Bryopsis, 205 smithii, 137, 146, 147, 151 Bryozoa, 146, 147, 155Ð156, 209, 210, 211, 212, 213, 220, Caudina, 99 221, 222, 385, 397, 405 Caulerpa, 205 Bulla gouldiana, 249 racemosa var. cylindracea, 178 striata, 249 taxifolia, 178 vernicosa, 203, 228, 229, 249 Cellaria fistulosa, 156 Bullia, 105, 107 salicornioides, 146, 156 digitalis, 105 Cellepora pumicosa, 156 Bullidae, 203 Celleporella hyalina, 386 Bunodosoma caissarum, 377 Celleporina, 156 Bursatella leachii, 207, 228, 229 caminata, 137, 143, 146, 147 Buskea dichotoma, 156 Centrostephanus longispinus, 157, 159 nitida, 156 Cephalaspidea, 199, 201, 202, 203, 228, 229, 234, 247, Bythograea thermydon, 65, 70 248, 249, 253, 254, 256 Cephalopoda, 293, 383, 405 Cephalorhynchus commersonii, 433, 436 C eutropia, 436 heavisidii, 433, 436 Caberea boryi, 156 hectori, 436 Cacospongia, 215 Ceratoisis, 209 mollior, 216 Ceratosoma, 199 scalaris, 146, 150, 162 alleni, 234 Cadlina, 201, 250, 252, 257 gracillimum, 215, 234 laevis, 153, 215, 229, 230, 232, 234, 241, 244, ingozi, 234 250 tenue, 234 luarna, 234 trilobatum,215 234 luteomarginata, 198, 230, 232, 234, 241, 244, 250 Cerberilla amboinensis, 223 marginata, 214, 234 Cerebratulus, 98 rumia, 214 Cerithidea californica, 345 Cadlinella hirsuta, 234 Cerithium, 397 Calanus, 455 lividulum, 381 finmarchicus, 455 vulgatum, 381 helgolandicus, 455 Cervus elaphus, 448 Calcinus tubularis, 155 Cestopagurus timidus, 155 Callinectes bellicosus, 379 Chaetomorpha, 205 sapidus, 65, 68, 69, 70, 74 Chama gryphoides, 147, 153 Calliostoma canaliculatum, 253 Charcotia granulosa, 221 zizyphinum, 153 Charcotiidae, 221 Callipallene spectrum, 153 Charonia, 159 Callochiton achatinus, 153 lampas, 159 Callopora dumerilii, 156 tritonis variegata, 159 Callorhinus ursinus, 438 Chartella tenella, 156 Calma glaucoides, 223 Chauvetia mamillata, 153 Calmella cavolinii, 223 minima, 153 Calmidae, 223 Chelidonura, 228 Calothrix, 139 inornata, 202, 228, 249 Cambarus bartonii, 66, 68 ornata, 227, 228 Campalecium medusiferum, 151 pallida, 202, 227 Campanularia, *, 142 tsurugensis, 202 everta, 151 Chlamys multistriata, 153 raridentata, 151 Chlorodesmis, 205 Cancer irroratus, 65 Chondrosia, 169 Caperea marginata, 434 reniformis, *, 145, 146, 150, 169, 180 Caprella acanthifera, 154 Chondrymenia lobata, 148, 158 mutica, 406 Chordata, 146, 147, 405 Carcinus maenas, 65, 70, 71, 73 Chorizopora brongniartii, 156 Carnivora, 365 Chromis chromis, *, 145, 147 Caryophyllia, 142 Chromodorididae, 199, 201, 214, 226, 230, 251, 253, 257

499 7044_Idx.fm Page 500 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

Chromodoris, 199 murrayi, *, 278, 279, 280, 281, 282, 283, 284, 285, 286, africana, 234 287, 290, 294, 298, 302, 303, 304, 305, 309, 310, 313, annae, 234 316 britoi, 234 Cladobranchia, 219, 228, 248, 256 buchananae, 234 Cladophora, 203 dianae, 234 Clanculus corallinus, 153 elisabethina, 234 Clathrina clathrus, 150 goslineri, 234 coriacea, *, 145 hamiltoni, 235 Clavagella melitensis, 137 heatherae, 235 Clavelina dellavallei, 157 nana, 157 hintuanensis, 235 Clavularia koellikeri, 377 joshi, 234, 235 ochracea, 151 kitae, 235 Cleantis, 351 krohni, 215, 235 Clibanarius erythropus, 71 loboi, 235 Cliona, 138 lochi, 235 amplicavata, 139 luteopunctata, 235 celata, 139 luteorosea, 153, 215, 235, 254 janitrix, 139 magnifica, 235 schmidtii, 139 mandapamensis, 235 viridis, *, 138, 139, 140, 142, 145, 150, 163 michaeli, 235 Clione, 208, 228, 229, 257 naiki, 235 antarctica, 208 purpurea, 153, 215, 235 limacina, 208, 228, 229 strigata, 235 Clupea harengus, 447 trimarginata, 230, 235 Clytia hemisphaerica, 150, 151 tumulifera, 215, 235, 241, 244 Cnidaria, 146, 147, 405 westraliensis, 215, 233, 236, 243, 244, 245 Codium bursa, *, 142, 145 willani, 236 vermilara, *, 142, 205 Chrysopetalum caecum, 152 Colomastix pusilla, 142 Chthamalus fissus, 379 Cominella lineolata, 381, 390 Chunioteuthis ebersbachi, 294, 295 Concholepas concholepas, 334 Ciona edwardsi, 157, 161 Conger conger, *, 142, 158 Cirrata, 293 Copepoda, 153, 405 Cirripedia, 154, 379, 405 Coralliophaga lithophagella, 153 Cirroctopodidae, 277, 281, 287, 300Ð301, 310 Corallium rubrum, *, 124, 139, 145, 146, 147, 151, 158, 170Ð171, 180 Cirroctopus, 277, 279, 281, 282, 285, 288, 290, 293, 295, Corambe lucea, 211 300, 301 Corambidae, 211 antarctica, 301 Corcyrogobius liechtensteinii, 158 glacialis, *, 279, 280, 281, 283, 287, 288, 301, 304, Coris julis, 157 305, 3006, 307, 308 Cornularia cornucopiae, 151 hochbergi, 301, 304, 305 Corophium sextonae, 154 mawsoni, 300, 301 volutator, 379, 399 Cirroteuthidae, *, 277, 279, 281, 282, 285, 287, 288, 293, Coscinasterias, 402 293Ð295 , 296, 301, 308, 309, 310, 311, 312, 313, 316 muricata, 374, 384, 391, 393 Cirroteuthis, 277, 279, 281, 285, 286, 293, 294, 295 Cossura, 102 gilchristi, 294 Cossuridae, 102 glacialis, 310 Crambe crambe, *, 142, 168, 169, 180, 376, 410 hoylei, 293, 294 maritima, 343 magna, 293 Crania anomala, 155 massyae, 296, 297 Crassimarginatella crassimarginata, 156 muelleri, 278, 279, 281, 282, 285, 287, 293, 294, 302, maderensis, 138, 156 303, 305, 306, 316 Crassostrea gigas, 406 Cirroteuthopsis massyae, 296, 297 Cratena peregrina, 224 Cirrothauma, 277, 279, 281, 285, 286, 293, 294, 295 Crepidula, 343, 397 magna, *, 278, 282, 285, 289, 294, 302, 305, 312, 313, atrasolea, 381 314, 316 convexa, 343, 381

500 7044_Idx.fm Page 501 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

depressa, 381 Densa, 219 fornicata, 350, 381 Dentex dentex, 157 Cressa cristata, 154 Dentiporella sardonica, 156, 163 mediterranea, 154 Derbesia tenuissima, 205 Cribilaria innominata, 156 Dermatobranchus, 221 radiata, 137, 156 semistriatus, 221, 230, 232, 245 Crimora papillata, 211 Dexamine thea, 154 Crinoidea, 156, 209 Dexiarchia, 219 Crisia, 156 Diadema antillarum, 384 Crosslandia, 252 mexicanum, 384 viridis, 221 paucispinum, 384 Crustacea, 64, 294, 209, 324 savignyi, 384 Cryptoprocta, 366 Diaphanidae, 204 Cryptoteuthis, 277, 279, 281, 285, 296, 300 Diaphorodis papillata, 153 brevibracchiata, *, 279, 280, 283, 287, 299, 300, 302 Diaporoecia, 156 Ctenolabrus rupestris, 158 Dictyonella obtusa, 150 Cucumaria, 157, 397 pelligera, 150 kirschbergii, 157 Dictyopteris polypodioides, 148 miniata, 385 Dictyota dichotoma, 148 petiti, 157 Didemnidae,157 planci, 157 Didemnum maculosum, 157 pseudocurata, 385, 393 Didogobius splechtnai, 159 saxicola, 157 Diloma arida, 368 Cumacea, 154 bicanaliculata, 368 Cuspidella humilis, 150 coracina, 368 Cuthona coerulea, 225 crusoeana, 368 Cyanobacteria, 207, 225, 250, 256 nigerrima, 367 Cylichnidae, 204 subrostrata, 368 Cymodoce truncata, 154 zelandica, 368 Cymodocea nodosa, 341 Diosaccus tenuicornis, 153 Cynachira barbata, 212 Diplastrella bistellata, 150 Cystodites dellechiajei, *, 142, 157, 174, 180 Diplecogaster bimaculata, 158 Cystophora cristata, 439 Diplodus puntazzo, 158 Cystoseira spinosa, 125 sargus, *, 145 zosteroides, 124, 126 vulgaris, 157 Diplosolen obelium, 156 Diplosoma spongiforme, 157 D Dipolydora, 139, 152 armata, 163 Dactylopodia tisboides, 153 rogeri, 163 Decapoda, 65, 66, 68, 155 Dirona, 228 Delesseriaceae, 141 albolineata, 222 Delisea pulchra, 206 Dironidae, 222 Delphinapterus leucas, 436, 446 Discodoris, 249 Delphinidae, 436 atromaculata, *, 145, 153. 160, 161 Delphinus capensis, 437, 440 Dissostichus eleginoides, 309 delphis, 437, 440 Distaplia rosea, 157 tropicalis, 437, 440 Distomus variolosus, 157 Dendrodorididae, 199, 201, 217 Dodecaceria concharum, 139, 152 Dendrodoris, 247, 253, 256 Dolabrifera dolabrifera, 207 grandiflora, 153, 198, 218 Donax serra, 105, 106 limbata, 218, 246, 254 deltoides, 383 nigra, 201, 218, 227, 246 sordidus, 106 Dendronotidae, 220 Dondice banyulensis, 153 Dendronotoidea, 201, 219, 253 Dorididae, 212 Dendronotus frondosus, 220 Doridoidea, 210, 228, 234, 252, 253, 254 iris, 220 Doridoxa ingolfiana, 219 Dendrophyllia ramea, 164 Doridoxidae, 219

501 7044_Idx.fm Page 502 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

Doriopsilla, 201, 250, 252 Enhydra lutris, 440 gemela, 218, 233, 236, 242 Enigmatiteuthis, 293, 296 Doris, 253 inominata, 299 verrucosa, 213 Enteromorpha, 207 Dotidae, 220 Enthalophoroecia deflexa, 137, 156 Doto, 228 gracilis, 156 coronata, 220 Epiactis, 392 Dotona pulchella ssp. mediterranea, 139 lisbethae, 377 Drepanophorus crassus, 151 prolifera, 377 Dromia personata, 155 ritteri, 377, 392 Dugong dugon, 439 Epinephelus alexandrinus, 159 Dugongidae, 439 costae, 159 Durvillaea, 353 guaza, 159 antarctica, 334, 368 marginatus, *,145, 157, 159, 177 Durvilledoris albofimbriae, 236 Epizoanthus arenaceus, 138, 151 Duvaucelia striata, 153 Ergnathus barbatus, 438, 451 Dynamena disticha, 150 Erichsonella, 351 Dysidea, 154, 167, 214, 215, 216 Erylus euastrum, 146, 150 amblia, 214 Erythroglossum sandrianum, 148 avara, *, 145, 150, 162, 167, 169, 170, 180, 216 Escharella ventricosa, 156 etheria, 214 Escharina dutertre, 156 fragilis, 162, 214, 216, 219 porosa, 156 herbacea, 214 vulgaris, 156 Escharoides coccinea, 156 Eschrichtiidae, 434 E Eschrichtius robustus, 433, 434 Esox lucius, 63 Echinaster sepositus, 156 Eubranchidae, 225 Echinocyamus pusillus, 157 Eubranchus, 228 Echinodermata, 204, 405 exiguus, 225 Echinoidea, 157, 384, 397, 405 Eucarida, 379, 397, 405 Echinolittorina, 401 Euchirograpsus liguricus, 155 lineolata, 381 Eudendrium, *, 160, 161, 210, 223, 224 Echinometra lucunter, 385 capillare, 151 mathaei, 385 racemosum, 151 oblonga, 385 rameum, 150 vanbrunti, 385 Eudistoma banyulensis, 157 viridis, 385 planum, 157 Echinothrix diadema, 385 Eugomontea, 139 Echinus melo, 139, 157, 164 Eulalia tripunctata, 152 Echiura, 152 Eumetopias jubatus, 438 Ecteinascidia herdmanni, 157 Eunice siciliensis, 152, 162 Ectinostoma dentatum, 153 torquata¸152 Ectoprocta, 385, 397, 405 Eunicella, 161, 162 Elaphidion mimeticum, 349 cavolinii, *, 143, 146, 151, 158, 172, 180 Elasmopus vachoni, 154 singularis, *, 142, 143, 151, 158, 172, 175, 180 Electra pilosa, 386 Euphausiacea, 66 tenella, 406 Euphausia superba, 379 Eledone cirrhosa, 303 Eupogodon, 148 Elminius modestus, 406 Eurynome aspera, 155 Elphidium crispum, 150 Eurysillis tuberculata, 152 Elymus athericus, 357, 400 Excirolana braziliensis, 399 Elysia cauze, 205 crispata, 205, 228, 245, 253 ornata, 205, 230, 234, 240, 246, 251 F viridis, 205, 245, 253 Emerita, 106 Facelinidae, 224 Engraulis encrasicholus, 447 Faciospongia cavernosa, 138, 150, 217, 218

502 7044_Idx.fm Page 503 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

Fauchea, 143 Gnathia maxillaris, 154 repens, 148 Gobiidae, 148 Feresa attenuata, 437 Gobius niger, 158 Figularia figularis, 156 vittatus, 157 Filellum serpens, 150, 151 Golfingia minuta, 152 Filograna implexa, 152 Goniodorididae, 210 Filogranula, 138 Goniodoris nodosa, 210, 383 Flabellia petiolata, *, 133, 140, 142, 145, 148, 154 Gorgonia, 172Ð173 Flabellina, 223 Grampus griseus, 437, 448 affinis, *, 153, 160, 161, 223 Graneledone, 306 babai, 223 Grimpoteuthidae, 277, 279, 281, 282, 285, 287, 293, falklandica, 223 296Ð300, 301, 310, 316 gracilis, 223 Grimpoteuthis, 277, 279, 281. 282, 285, 286, 287, 288, 290, pedata, 223 293, 295, 296, 298, 299, 300, 301, 302, 303, 305, 308, Flabellinidae, 223 310, 311, 312, 313, 314, 315, 316 Folliculinidae, 150, 162 abyssicola, 298, 299, 305 Foraminifera, 204 antarctica, 305 Fossa, 366 bathynectes, 298, 299 Froekenia, 295 boylei, 283, 291, 298, 299, 303, 305, 308 clara, 294, 295 challengeri, 282, 285, 298, 299, 303, 305 Fucus, 347, 354, 400 discoveryi, *, 279, 280, 287, 298, 299, 303, 305 distichus, 382 glacialis, 300 serratus, 390 hippocrepium, 298, 299, 308 vesiculosus, 347, 400 inominata, 299 Fusinus pulchellus, 153 meangensis, 298, 299, 305 rostratus, 153 megaptera, 298, 299 pacifica, 298, 299 plena, 298, 299, 316 G tuftsi, 282, 285, 298, 299, 300 umbellata, 278, 298, 299, 305, 316 Gadus morhua, 447, 449 wuelkeri, 286, 288, 289, 298, 299, 303, 305, 308, 316 Gaidropsarus vulgaris, 158 Gulsonia nodulosa, 148 Galathea bolivari, 155 Gymnodorididae, 210, 211 intermedia, 155 Gymnodoris aurita, 236 nexa, 155 striata, 211 strigosa, *, 145 Gymnosomata, 208, 228, 249, 257 Gammarus locusta, 379, 390, 391 Gymnoteuthis plena, 298, 299 Gammogobius steinitzii, 158, 159 Gastrochaena dubia, 139 Gastropoda, 197, 405 H Gastrosaccus psammodytes, 106 Genocidaris maculata, 157 Hacelia attenuata, 157 Geodia, 138 Halarachnion ligulatum, 158 cydonium, 150, 208 Halecium halecinum, *, 142, 145 Gerardia savaglia, 158 petrosum, 170, 180 Gitana sarsi, 154 pusillum, 151, 170, 180 Glaucidae, 225 tenellum, 147, 151 Glaucus atlanticus, 225 Halichoerus grypus, 439 Globicephala macrorhynchus, 437, 448 Halichondria cf lendenfeldi, 219 melas, 437, 447 Haliclona, 376 Glossodoris, 199 mediterranea, 150 atromarginata, 215, 233, 236, 243, 244, 245 (Reniera) fulva, 213 aureola, 236 Halicystis parvula, *, 160 edmundsi, 236 Halimeda, 161, 166, 170, 205 gracilis, 153 platydisca, 126 neona, 215 tuna, *, 133, 140, 141, 142, 143, 145, 148, 149, 150, pallida, 215, 236, 251, 254 154, 164, 165, 167, 168Ð169, 170, 180 rufomarginata, 215, 236, 244 Halocynthia, 167 tricolor, 153 papillosa, *, 145, 146, 157, 161, 167, 174, 180

503 7044_Idx.fm Page 504 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

Halopteris filicina, 148 Hydrozoa, 150Ð151, 170, 220, 221, 223, 224, 225, 252, Halymenia, 148 376, 405 trigona, 158 Hydrurga leptonyx, 439 Haminoea, 253 Hyella caespitosa, 139 antillarum, 203, 228, 229 Hymedesmia pansa, 150 callidegenita, 203, 228 Hymeniacidon sanguinea, 213 cymbalum, 203, 251 Hyperoodon ampullatus, 435 orteai, 203, 230, 240, 246, 251 planiforms, 435 Haminoeidae, 203 Hypoglossum hypoglossoides, 148 Hancockia burni, 221 Hypselodoris, 199, 216, 244, 251 ryrca, 221 acriba, 236 uncinata, 221 agassizii, 236 Hancockiidae, 221 alboterminata, 236 Haplosyllis, 163 babai, 236 andersoni, 236 depressa chamaeleon, 163 bayeri, 236 spongicola, 152, 163 benetti, 236 Haptosquilla pulchella, 379 bertschi, 236 Harmothoe aerolata, 152 bilineata, 216, 236 Harpacticoida, 405 bollandi, 236 Harpacticus littoralis, 153 californiensis, 237 Harpinia ala, 154 cantabrica, 216, 237 propinqua, 100 capensis, 237 Hebella scandens, 150 carnea, 237 Hediste diversicolor, 378 ciminoi, 237 Heliocidaris, 397 dollfusi, 237 tuberculata, 385 emma, 237 erythrogramma, 385 espinosai, 237 Hematodinium, 70 festiva, 237 Hemimycale columella, *, 142, 150, 169, 180 flavomarginata, 237 Heterobranchia, 226 fontandraui, 153, 216, 237 Heterocarpus vicarius, 65 fucata, 237 Heterozostera tasmanica, 341 gasconi, 216, 237 Hexacorallia, 220, 223 ghiselini, 237 Hexadella racovitzai, 150 gofasi, 237 Hiatella arctica, 153 iacula, 237 Hinia incrassata, 153 infucata, 237 Hippocampus ramulosus, 159 insulana, 237 Hippodiplosia foliacea, 162 kaname, 237 Hippomenella mucronelliformis, 156 kanga, 238 Hippospongia communis, 150 koumacensis, 238 Histriophoca fasciata, 439 krakatoa, 238 Holothuria forskalis, 157 lapislazuli, 238 mammata, 157 maculosa, 238 tubulosa, 157 malacitana, 238 Holothurioidea, 157, 385, 397, 405 marci, 238 Homarus americanus, 74 maridadilus, 238 gammarus, 155, 72, 75 maritima, 238 Hoplangia durotrix, 137, 146, 147, 151 midatlantica, 238 Hoplocarida, 379, 405 muniani, 238 Hornera frondiculata, *, 156, 162 nigrolineata, 238 Hyale frequens, 345 orsinii, 216, 231, 238, 241, 243, 244, 251 Hyatella arctica, 139, 164 paulinae, 238 Hydatina physis, 202 picta, 217, 238, 254 Hydatinidae, 202 pinna, , 238 Hydranthea margarica, 151 punicea, 238 Hydrobia, 394, 397 purpureomaculosa, 238 ulvae, 381, 394 regina, 239 ventrosa, 381, 394 reidi, 239 Hydroides, 138 rudmani, 239

504 7044_Idx.fm Page 505 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

ruthae, 239 L sagamiensis, 239 shimodaensis, 239 Labrus bimaculatus, 157 tricolor, 217, 233, 239, 244, 245 merula, 157 villafranca, 200, 217, 239, 240, 241, 242, 243, 244, Lacazella mediterranea, 155 247, 251 Lagenodelphis hosei, 437 violabranchia, 239 Lagenorhynchus acutus, 437 webbi, 217 albirostris, 433, 437 whitei, 239 australis, 433, 437 xicoi, 239 cruiger, 437 zebra, 239 obscurus, 437, 454 zephyra, 239 obliquidens, 437 Laila cockerelli, 211, 233, 240, 243 Laminaria rodriguezii, 126, 131, 148, 158 I Laomedea angulata, 150 Laophonte cornuta, 153 Idmidronea atlantica, 156 Lappanella fasciata, 157 coerulea, 156 Lasaea, 368, 370, 402 Idotea, 347, 351 Laurencia, 207 baltica, 347, 368, 369 filiformis, 206 chelipes, 379, 389 Lepidasthenia elegans, 152 metallica, 344 Lepidonotus clava, 152 Illex illecebrosus, 453 Leptocheirus bispinosus, 154 Inachus thoracicus, 155 guttatus, 154 Indopacetus pacificus, 435 Leptochelia dubia, 345 Inia geoffrensis, 435, 446 savignyi, 154 , Iniidae 435 Leptonychotes weddellii, 439, 452 Iphimedia serratipes, 154 Leptopsammia pruvoti, *, 137, 138, 143, 146, 147, 151, Ircinia , 154, 210 162, 163 fasciculata , 146, 218 Leptosynapta tenuis, 104 oros, *, 147, 150, 160 Leucetta chagosensis, 212, 363, 364 variabilis, *, 142, 146, 147, 150, 163 Leucothoe euryonyx, 154 Isopoda, 154, 405 venetiarum, 154 Lichenopora radiata, 156 Ligia, 347 J Liljeborgia dellavallei, 154 Jaera albifrons, 380, 399 Lima lima, 153 forsmani, 380 Limacia clavigera, 153, 199, 211, 230, 231, 233, 240, 241, ischiosetosa, 380 244, 245, 251 nordmanni, 380 Limacina helicina, 207 praehirsuta, 380 Limnoria chilensis, 354 Jaeropsis brevicornis, 154 Linckia laevigata, 384 Janolus capensis, 222 Lipotes vexillifer, 436, 446 cristatus, 222 Lipotidae, 436 mokohinau, 222 Lissodelphis borealis, 437 Jassa falcata, 345 peronii, 437 Jorunna tomentosa, 213 Lithopenaeus setiferus, 379 Lithophaga lithophaga, 138, 139, 146, 153, 158, 165 Lithophylletalia, 126 K Lithophyllo-Halimedetum tunae, 126, 133, 140 Lithophyllum, 136, 137 Kallymenia, 143, 148 byssoides, 124, 139 Kefersteinia cirrata, 152 cabiochae, *, 133, 136, 137, 148, 160, 164, 178, 179 Kellia suborbicularis, 153 cabiochae-frondosum, 137 Kirchenpaueria echinulata, 151 expansum, 126, 136 Kogia breviceps, 434 frondosum, *, 133, 1136, 137, 139, 141, 143, 145, 151, sima, 434 160, 168, 179, 180 Kogiidae, 434 hauckii, 136

505 7044_Idx.fm Page 506 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

pustulatum v. confinis, 137 Mecynoecia delicatula, 156 stictaeforme, 136 Megaptera novaeangliae, 433, 434 Lithothamnion, 137 Megathiris detruncata, 155 philippi, 126 Megerlia truncata, 155 sonderi, 136 Melagraphia aethiops, 368 Littoraria, 397 Melibe, 201, 233, 252 angulifera, 381, 392 fimbriata, 221 flava, 382, 393 leonina, 221233, 242, 254 Littorina, 397, 398, 400 pilosa, 256 cingulata, 382 Melicertus kerathurus, 66 littorea, 325, 382 Membranipora membranacea, 375, 386, 393, 394 obtusata, 368, 369 tuberculata, 406 plena, 382 Merlangius merlangus, 447 saxatilis, 325, 346, 347, 351, 357, 375, 382, 389, 390, Mesophyllum, 135, 136, 147 400, 402, 408 alternans, *, 125, 133, 135, 236, 137, 140, 143, 148, scutulata, 382 149, 151, 154, 155, 160, 164, 165, 168, 175, 176, 178, sitkana, 355, 375, 382, 392, 398 179, 180 subrotundata, 382 expansum, 136 Lobodon carcinophaga, 439, 452 lichenoides, 135, 136, 137, 163 lichenoides var. agariciformis, 136 Loligo forbesi, 447 macedonis, 136 gahi, 447 macroblastum, 136 opalescens, 448 Mesoplodon bidens, 435 vulgaris, 153 bowdoini, 435 Lomanotidae, 220 carlhubbsi, 435 Lomanotus vermiformis, 220 densirostris, 435 Lomentaria subdichotoma, 158 europaeus, 435 Lontra felina, 440 ginkgodens, 435 Lopha cristagalli, 406 grayi, 435 Lophocladia lallemandii, 178 hectori, 435 Lumbricus, 104 layardii, 435 terrestris, 110 mirus, 435 Lumbrinereis coccinea, 152 perrini, 435 Luteuthidae, 293, 296, 300 peruvianus, 435 Luteuthis, 277, 279, 281, 285, 286, 293, 296, 298, 300 stejnegeri, 435 dentatus, 296, 299, 300 traversii, 435 shuishi, 279, 299, 300, 305 Mexichromis francoisae, 240 Lutra lutra, 440 molloi, 240 Microciona toxystila, 217, 218 Microcladia glandulosa, 158 M Microcosmus polymorphus, 146, 157 sabatieri, *, 142, 157, 161, 174, 180 Maasella edwardsii, 151 Micrura aurantiaca, 151 Macoma balthica, 383 fasciolata, 151 Macrocystis, 353, 354 Mimosella verticillata, 156 pyrifera, 353, 354, 407 Miniacina miniacea, 137, 138, 146, 150 Macropodia czerniavski, 155 Mirounga angustirostris, 439, 441 Madracis pharensis, 151 leonina, 439, 441 Madrella ferruginosa, 222 Mollia patellaria, 138, 156 Madrellidae, 222 Mollusca, 146, 147, 152Ð153, 204, 405 Maera grossimana, 154 Monachus monachus, 439, 450 inaequipes, 154 schauinslandi, 439 Magelona, 100 Monodon monoceros, 433, 436 Magelonidae, 99, 100 Monodontidae, 436 Mandinia, 366 Monomyces pygmaea, 151 Marionia blainvillea, 201, 219, 227 Morula marginalba, 382, 391 Marthasterias glacialis, 157 Muraena helena, 158 Massilina secans, 150 Muricopsis cristatus, 153 Mastigocoleus testarum, 139 Musculus costulatus, 153

506 7044_Idx.fm Page 507 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

Mustelidae, 440 Octopoda, 293 Mustelus asterias, 159 Octopodidae, 304 mustelus, 159 Octopus, 292 Mycteroperca rubra, 159 chierchiae, 304, 306 Myriapora truncata, *, 137, 138, 142, 143, 156, 164 vulgaris, 153, 304, 306 Myriogramme, 148 Ocythoe, 304 Mysidacea, 66, 154 Odobenidae, 438 Mysticeti, 434 Odobenus rosmarus, 438, 451 Myxicola aesthetica, 152 Odondebuenia balearica, 158 Odontoceti, 434 Odostomia rissoides, 153 N Omaloseca ramulosa, 156 Ommatophoca rossii, 439, 452 Nausitoë punctata, 151, 162 Oncaea conifera, 308 Nautilus, 287 Onchidella, 241 Neanthes virens, 378 borealis, 225, 241, 246 Nemastoma dichotomum, 158 celtica, 225 Nematoda, 151 Onchidiidae, 225 Nemertea, 151 Onchidium verruculatum, 225 Nemertesia antennina, 150 Onchidorididae, 210 Neobalaenidae, 434 Onchidoris, 249 Neogoniolithon mamillosum, 133, 135, 136, 141, 148, 179 bilamellata, 210, 249 Neophoca cinera, 438 Onychocella marioni, 137, 156 Neophocaena phocaenoides, 437, 446 Opheliidae, 103 Neotarentula, 402 Ophiacantha setosa, 156 Nephrops norvegicus, 64, 65, 68, 69, 70, 71, 72, 73, 74, 75, 76 Ophidiaster ophidianus, 157 Nephtyidae, 103 Ophiocomina nigra, 156 Nephtys, 99 Ophioconis forbesii, 156 Nereis, 97, 98, 99, 103, 114 Ophioderma longicaudum, 156 diversicolor, 99 Ophiopsila aranea, 156 pelagica, 152 Ophiothrix fragilis, *, 142, 156 virens, 110, 114 Ophiuroidea, 156, 209, 385, 405 Nereocystis, 353 Ophlitaspongia pennata, 214 Nerita atramentosa, 382 Opisthobranchia, 228, 245, 247, 249, 251, 255, 256, 257, Neurocaulon foliosum, 148 383, 405 Newnesia, 201 Opisthodonta morena, 152 antarctica, 204, 230, 232, 234, 242, 251 Opisthoteuthidae, 281 282, 285, 287, 293, 295Ð296, 297, Nolella, 156 300, 301, 310, 316 Notaeolidia, 248 Opisthoteuthis, 277, 278, 279, 280, 281, 282, 285, 286, depressa, 222 288, 290, 293, 295, 296, 297, 298, 300, 301, 302, 304, gigas, 223 305, 307, 308, 309, 310, 313, 315, 316 schmekelae, 223 agassizii, 283, 287, 289, 296, 297, 302, 304, 305, 308, Notaeolidiidae, 222 311, 313 Notodoris citrina, 212 albatrossi, 296, 297, 305, 316 Noumea cf. crocea, 217 borealis, 296, 297 decussata, 217 brunni, 296, 297 verconiforma, 240 californiana, 296, 297, 302, 303, 304, 305, 306, 307, Nucella, 373 308, 313, 316 lamellosa, 382 calypso, *, 280, 282, 284, 285, 292, 293, 296, 297, 302, lapillus, 325, 355, 357, 368, 369, 375, 383, 389, 392 303, 304, 305, 306, 307, 308 ostrina, 383 chathamensis, 296, 297, 304, 305 Nudibranchia, 209, 234, 252 depressa, 285, 296, 297, 308, 316 Nudipleura, 257 extensa, 296, 297 grimaldii, 292, 293, 296, 297, 305 hardyi, 281, 290, 296, 297 O japonica, 296, 297, 316 massyae, *, 278, 279, 280, 281, 285, 288, 291, 292, Obelia geniculata, 376, 393, 394, 395, 396 293, 296, 297, 302, 303, 304, 305, 306, 307, 308, 314, Octocorallia, 219, 220, 221, 223, 224, 225 316

507 7044_Idx.fm Page 508 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

medusoides, 296, 297 calcar, 384 mero, 296, 297, 305, 310 exigua, 338, 367, 384, 391, 393 persephone, 292, 296, 297 regularis, 374 phillipi, 296, 297 Pectenodoris aurora, 240 pluto, 296, 297 trilineata, 240 robsoni, 297, 308 Pectinaria koreni, 378 vossi, 296, 297 Pelagophycus, 353 Orcaella brevirostris, 437 porra, 353 Orchestia, 347 Peltodoris atromaculata, 213, 249 montagui, 380, 392 Penaeus kerathurus, 66 stephenseni, 380, 392 monodon, 379 Orchomene humilis, 154 Pentapora fascialis, *, 8, 137, 138, 142, 143, 156, 162, 164, Orcinus orca, 437 177 Orconectes virilis, 66, 68 Peponocephala electra, 437 Orthopyxis crenata, 170, 180 Peracarida, 379, 405 Oscarella, 169 Periclimenes scriptus, 155 lobularis, *, 142, 150, 169, 180 Petricola lithophaga, 139 Osmundaria volubilis, 148 Petrosia ficiformis, *, 145, 146, 147, 150, 160, 161, 213 Ostracoda, 153 Peyssonnelia, 136, 137, 140, 147, 148 Ostrea angasi, 364 polymorpha, 136, 137 aupouria, 364 rosa-marina, 135, 136, 141, 143 chilensis, 363, 364 rosa-marina f. saxicola, *, 136, 137 Ostreobium, 139 rubra, *, 142 quekettii, 139 squamaria, *, 126, 143 Otaria flavescens, 438 Peyssonneliaceae, 176 Otariidae, 437 Peyssonnelietum aglaothamnietosum, 126 Oulactis muscosa, 377 rodriguezelletosum, 126 Oxynoe viridis, 205 rubrae, 126 Oxynoidae, 205 Phaeocystis, 5, 31, 42, 43, 44 Phaeophila, 139 Phakellia carduusi, 219 P Phanerophthalmus smaragdinus, 203 Phascolosoma granulatum, 139, 152 Pacifastacus leniusculus, 66 Phialella quadrata, 151 Pagophilus groenlandicus, 439 Phidiana indica, 224 Pagurus bernhardus, 71 lottini, 224 Palaemon elegans, 72 Philine, 249 serratus, *, 142 alata, 204, 226, 249 Palinurus elephas, *, 145, 155 aperta, 249 Palmophyllum crassum, *, 143, 147, 148 auriformis, 204 Pandalus borealis, 65 Philinidae, 219 Panulirus inflatus, 66 Philinopsis cyanea, 203 Paracentrotus lividus, 157, 385 Phoca caspica, 451 Paracorophium excavatum, 380 hispida lagodensis, 451 lucasi, 380 hispida saimensis, 451 Paracyathus stearnsii, 377 largha, 439 Paragnathia formica, 154 siberica, 451 Paramuricea, 167, 172 vitulina, 438, 449 clavata, 145, 146, 147, 151, 158, 161, 162, 163, 167, Phocarctos hookeri, 438 172, 173, 175, 176, 177, 180 Phocidae, 438, 441 Paranthura nigropunctata, 154 Phocoena dioptrica, 438 Parasmittina tropica, 156 phocoena, 437, 441 Parazoanthus axinellae, *, 142, 145, 146, 147, 151, 161, sinus, 438, 446 162, 173, 174, 180 spinipinnis, 438 Pareledone turqueti, 383 Phocoenidae, 437 Parerythropodium coralloides, 143, 147, 151, 161 Phocoenoides dalli, 438 Patiriella, 397 Pholoe minutia, 152

508 7044_Idx.fm Page 509 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

Phorbas tenacior, 150 Plocamopherus, 201, 242, 252 Phycis phycis, 157 ceylonicus, 212, 232, 233, 242, 246, 250, 251, 152, 257 Phyllangia mouchezii, *, 145 tilesii, 252 Phyllariopsis brevipes, 148 Pocillopora, 371, 397 Phyllidia, 253 damicornis, 361, 362, 363, 378, 389, 390, 391 flava, 219 meandrina, 378 Phyllidiella, 253 Polycarpa gracilis, 157 pustulosa, 219 pomaria, 146, 157 Phyllidiidae, 219 Polycera, 228 Phylliroe bucephala, 221 quadrilineata, *, 142, 153, 211 Phylliroidae, 221 Polycerella emertoni, 211 Phyllocarida, 154 Polyceridae, 211 Phyllodesmium, 256 Polychaeta, 99, 151Ð152, 202, 378, 405 briareum, 224 Polycheles typhlops, 66 jakobsenae, 224 Polyclinidae, 157 Phyllophora crispa, 148 Polydora, 138, 164 Phyllospadix scouleri, 385, 393 caeca, 152 Phyllothalestris mysis, 153 hoplura, 163 Physeter macrocephalus, 434, 440 Polyphysia, 98, 103, 104, 105, 110 Physeteridae, 434 crassa, 109 Pilumnus hirtellus, 155 Polyprion americanus, 159 inermis, 155 Polysiphonia banyulensis, 148 spinifer, 155 elongata, 148 Pinna nobilis, 159 Polysyncraton bilobatum, 157, 168 pernula, 159 lacazei, 157 rudis, 159 Pomatoceros triqueter, 152 Pione vastifica, 139 Pontogeneia rostrata, 345 Pisa tetraodon, 155 chrysocoma, 152 Pisces, 157Ð158 Pontoporia blainvillei, 436 Piseinotecidae,225 Pontoporiidae, 436 Piseinotecus gabinieri, 225 Porcellana platycheles, 155 Pisidia longicornis, 155 Porella concinna, 163 longimana, 155 Porifera, 146, 147, 150, 169Ð170, 208, 209, 210, 212, 213, Plagioecia, 156 214, 215, 216, 217, 218, 219, 376, 405 Plagusia chabrus, 324 Porostomata, 253 tomentosa, 324 Portieria hornemannii, 206 Plakobranchidae, 205 Portunus pelagicus, 66, 68 Plakobranchus, 201, 211 Posidonia oceanica, 124, 147, 178, 341 ocellatus, 199, 205, 230, 233, 234, 243, 244, 251, 253, Potamilla reniformis, 152 254 Potamon fluviatile, 66 Planorbulina mediterranensis, 150 Potamonautes warreni, 66, 67, 68, 71 Platanista gangetica, 435, 446 Potentilla stipularis, 356 Platanistidae, 435 Predaea, 143, 148 Platidia davidsoni, 155 Prenantia inerma, 156 Platoma cyclocolpa, 158 Priapulus, 98, 104, 110 Platorchestia platensis, 380, 392 caudatus, 104, 105 Platydoris, 253 Procambarus clarkii, 71 argo, 213 Processa macrophthalma, 155 Platynereis coccinea, 152 Prochlorococcus, 174 Plectonema tenebrans, 139 Prochloron, 256 Pleraplysilla spinifera, 150, 217 Prosobranchia, 247, 381, 397, 405 Pleurobranchidae, 209 Protaeolidiella juliae, 223 Pleurobranchoidea, 201, 209, 229, 242, 247, 249, 250, 252, Protozoa, 162 257 Protula, 152, 164 Pleurobranchus membranaceus, 249, 252 Proxillella affinis pacifica, 108 Plocamium cartilagineum, 148 Psammechinus microtuberculatus, 157 coccineum, 207 Pseudocalanus elongatus, 4

509 7044_Idx.fm Page 510 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

Pseudodistoma cyrnusense, *, 157, 162 Rynchothorax mediterraneus, 153 Pseudolithophyllo-Halimedetum platydiscae, 126 Rynchozoon bispinosum, 156 Pseudolithophyllum 136, 137 cabiochae, 135, 136 expansum, 135, 136 S expansum-Lithophyllum hauckii association, 126 Pseudoprotella phasma, 154 Sabella, *, 142 Pseudopterogorgia elisabethae, 375, 378 pavonina, 152 Pseudorca crassidens, 437 spallanzani, 152 Pseudotritonia antarctica, 222 Sacoglossa, 205, 234, 253, 254, 256 gracilidens, 222 Sagaminopteron ornatum, 204 quadrangularis, 222 Salicornia pusilla, 343 Pteraeolidia ianthina, 225 Salmacina dysteri, *, 142, 152, 162, 164 Pteria hirundo, *, 145, 146, 153 Salmo salar, 449 Pterobranchia, 155 Sarcotragus spinosula, 146 Ptilocladiopsis horrida, 158 Sardina pilchardus, 447 Ptilophora mediterranea, 158 Sargassum, 347, 354 Puellina gattyae, 156 polyceratium, 348 Pulmonata, 225, 240, 245, 253 Sarpa salpa, 139 Pupa solidula, 202 Scalibregma, 103, 104, 113 Pusa caspica, 439 inflatum, 102, 113 hispida, 439 Scalibregmatidae, 102, 103, 152 sibirica, 439 Scantilletta levispira, 139 Pycnogonida, 153 Scaphander, 201, 230, 250 Pyramidella sulcata, 226 lignarius, 204, 226, 231, 248, 250 Pyramidellidae, 226 Schizomavella, 137, 146, 156 Pyrgoma anglicum, 162, 163 auriculata, 156, 163 Pyura, 157 Schizoporella magnifica, 156 dura, 161 Schizotheca serratimargo, 156 gibbosa gibbosa, 386 Schizymenia dubyi, 158 Schmitzia neapolitana, 158 Sciadophorus, 294 R Sciaena umbra, *, 142, 157, 159, 177 Sclerocheilus minutus, 152 Raphitoma linearis, 153 Scorpaena notata, 158 Reniera cratera, 150 porcus, *, 142 fulva, 150 scrofa, 158 mucosa, 150 Scrupocellaria, 156, 210 Rhabdopleura normani, 155 Scyliorhinus canicula, 158 Rhizophora mangle, 349, 350 stellaris, 159 Rhodophyllis, 143 Scylla serrata, 379 divaricata, 148 Scyllaeidae, 221 Rhodosoma verecundum, 157 Scyllarides latus, 155, 159 Rhodymenia ardissonei, 148 Scyllarus arctus, 155 Rhodymenietalia, 126 Scyphozoa, 151 Risbecia nyalya, 240 Sebdenia, 143, 148 tryoni, 217, 233, 240, 244 Sepia officinalis, 153 Rissoina bruguierei, 153 Seriatopora, 363 Roboastra gracilis, 201, 211 hystrix, 378 Rodriguezella, 148 Serpula concharum, 137, 152 bornetii, 158 vermicularis, *, 137, 138, 145, 152 pinnata, 158 Serpulidae, 146, 147, 152 Rodriguezelletum strafforellii, 126, 133, 143, 146 Serpulorbis arenarius, 137, 146 Rodriguezellikon, 126, 148 Serranus cabrilla, 158 Rolandia rosea, 151 Sertella, 146, 156 Rossella, 212 septentrionalis, 146 Rostanga pulchra, 214 Sertularella crassicaulis, 150 Runcina adriatica, 205 ellisi, *, 142, 150 Runcinidae, 205 gaudichaudii, 147

510 7044_Idx.fm Page 511 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

gayi, 150 syrtensis, 279, 280, 281, 282, 283, 284, 285, 286, 287, polyzonias, 150, 151 288, 289, 291, 292, 294, 295, 302, 303, 305, 308, 311, Sertularia distans, 151 313, 314, 317 Setia semistriata, 153 wuelkeri, 298 tenera, 154 Stenella, 440 Sigalonidae, 103 attenuata, 433, 436 Sige microcephala, 152 clymene, 436 Sinularia, 224 coeruleoalba, 436, 450 flexibilis, 378 frontalis, 436 maxima, 224 longirostris, 433, 436 polydactyla, 224 Steno bredanensis, 436 Siphonaria, 250 Stenothoe dollfusi, 154 tergestina javanica, 225, 240, 246 , 154 Sternaspidae, 102 jeanae, 383 Sternaspis, 112 Siphonariidae, 225 Stichopus regalis, 157 Siphopteron quadrispinosum, 205 Stolonica australis, 386 Sipunculida, 152 Stomatopoda, 65 Smaragdinella cf calyculata, 204 Striarca lactea, 153 Smaragdinellidae, 203 Strongylocentrotus purpuratus, 385, 391 Smittina cervicoris, *, 145, 156, 164 Styela partita, 157 Smittoidea reticulata, 156 Styllophora, 363 Solea solea, 447 pistillata, 378 Somniosus cf. microcephalus, 309 Stylocheilus striatus, 198 Sotalia fluviatilis, 436, 446 Syllidae, 151 Sousa chinensis, 436 Syllides longocirrata, 152 plumbea, 436 Syllis gerlachi, 152 teuszii, 436 truncata, 152 Spartina, 345 Symbiodinium, 256 Spatoglossum solierii, 148 Symphodus doderleini, 158 Sphaerechinus granularis, 139, 157, 161, 164 mediterraneus, 157 coronopifolius, 148 melanocercus, 158 rhizophylloides, 158 tinca, 157 Sphaeroma terebrans, 349, 350, 355, 381, 390, 394, 400 Synalpheus, 397 Sphyrna lewini, 310 pectiniger, 379 Spicara smaris, 158 brooksi, 379 Spiralaria gregaria, 156 hululensis, 155 Spirastrella cunctatrix, *, 145, 150 Synascidia, 220 Spirobranchus polytrema, 137, 152 Synechococcus, 174 Spirorbis, 138 Synisoma, 154 Spisula s. solidissima, 383 Synnotum aegyptiacum, 156 Splanchnotrophidae, 245 Synthecium evansii, *, 145 Spondyliosoma cantharus, Syringodium filiforme, 341 Spondylus gaederopus, *, 142 isoetifolium, 341 Systellaspis debilis, 72 Spongia agaricina, 150 officinalis, 146, 147, 150, 218 virgultosa, 138, 150 Spongionella pulchella, 150 T Spongites mamillosa, 136 Talitrus saltator, 65, 68, 381, 392 Spongosorites intricatus, 150 Tanaidacea, 154 Squalus acanthias, 159 Tanais cavolini, 154 blainvilleii, 159 Tanystylum conirostre, 153 Squilla mantis, 65 Tasmacetus shepherdi, 435 Stauroteuthidae, 293, Telarma antarctica, 222 Stauroteuthis, 277, 279, 281, 282, 285, 286, 290, 293, 295, Telmatactis elongata, 151 296, 310, 317 Tenarea, 137 gilchristi, 282, 294, 295, 305, 309 Terebellidae, 99, 152 mawsoni, 300 Tergipedidae, 225

511 7044_Idx.fm Page 512 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

Tergipes tergipes, 225 Turbicellepora avicularis, 143, 146, 156, 162 Terpios fugax, 150 coronopus, 137, 156 Tethydidae, 221 Tursiops aduncus, 436 Tethys fimbria, 199, 252 truncatus, 436, 440 Tetraclita squamosa, 65, 68 Tylodina, 257 Tetrastemma coronatum, 151 citrina, 231 Thalassema, 152 perversa, 208, 230, 250, 256 Thalassia testudinum, 341, 357, 358 Tylodinidae, 208 Thalestris rufoviolescens, 153 Tylodinoidea, 201, 208, 230, 250, 257 Thecacera, 201 Typosyllis variegata, 152 pennigera, 211, 228, 230, 232, 251 Typton spongicola, 155, 162 Thecosomata, 207, 208, 253, 256 Tyrinna evelinae, 240 Thoracica, 65, 68 Tyrinna nobilis, 240 Thoralus cranchii, 155 Thorogobius ephippiatus, 158 macrolepis, 158 U Thorunna kahuna, 240 montroucieri, 240 Udotea, 205 punicea, 240 desfontainii, 126 Thuridilla hopei, 205, 227, 228 Udoteo-Peyssonnelietum squamariae, 126 Tisbe furcata, 153 Ulva, 203 Todarodes sagittatus, 447 Umbraculidae, 208 Titanoderma, *, 137, 142 Umbraculum, 250, 257 Tomthompsonia, 257 mediterraneum, 208 antarctica, 209, 257 umbraculum, 208, 226, 230, 231 Trachypenaeus curvirostris, 66 Umbrina cirrosa, 159 Trachytyone tergestina, 157 Uncionella lunata, 154 Trapania, 228 Urechis, 99 maculata, 210 Ursidae, 440 Trichechidae, 439 Ursus maritimus, 440 Trichechus inunguis, 439, manatus, 439, 441 manatus manatus, 439, 441 manatus latirostris, 439 V senegalensis, 439 Valonia macrophysa, 148 Tridachia crispata, 205 Vampyromorpha, 292 Tridacna maxima , 383 Vampyroteuthis infernalis, 314 Trididemnum armatum, 157 Veretillum cynomorium, 221 cereum, 157 Vermetus, 137 Triloculina rotunda, 150 Verruca strömia, 138, 154 Triophidae, 211 Triphora perversa, 153 Tritonia antarctica, 219 australis, 219 W challengeriana, 219 Watersipora subovoidea, *, 142 festiva, 219 Womersleyella (Polysiphonia) setacea, 178 plebeia, 219 setacea, 175, 178, 181 vorax, 220 Tritoniella belli, 220 Tritoniidae, 219 X Trochidae, 401 Trypanosyllis coeliaca, 152 Xenia, 224 zebra, 152 Xenosyllis scabra, 152 Tryphosella simillima, 154 Tubulipora plumosa, 156 Tumidagena minuta, 347 Y Tunicata, 157, 174, 386, 405 Turbellaria, 151, 202 Yoldia, 97, 112, 114

512 7044_Idx.fm Page 513 Tuesday, April 25, 2006 1:43 PM

SYSTEMATIC INDEX

Z Ziphiidae, 434 Ziphius cavirostris, 434 Zalophus californianus, 438, 441 Zoantharia, 173Ð174 wollebaeki, 438 Zonaria tournefortii, 148 Zanardinia prototypus, 148 Zostera, 342 Zephyrinidae, 222 marina, 341, 342, 343 Zeus faber, 158 noltii, 343, 344

513 7044_Idx.fm Page 514 Tuesday, April 25, 2006 1:43 PM 7044_Idx.fm Page 515 Tuesday, April 25, 2006 1:43 PM

SUBJECT INDEX

References to complete articles are given in bold type, references to sections of articles are given in italics, references to pages are given in normal type.

A external, 279Ð285 internal, 285Ð293 Algae, in coralligenous assemblages, 123, 124, 125, 126, conclusions, 316Ð317 127, 132, 133, 134, 136, 139, 140, 141, 143, ecology, 301Ð310 146, 147, 148, 149, 151, 154 160, 163, 164, distribution patterns, 301Ð302 165, 166, 68, 169, 170, 175, 176, 177, 178, habitat, 301 179, 180 reproduction, 302Ð307 Algal blooms, 449, 453, 455, 458 reproductive strategy, 304Ð307 Allozymes, 376, 377, 378, 379, 380, 381, 382, 383, 384, sexual characters, 302Ð304 385, 386 trophic ecology, 307Ð310 Aquaculture, 326, 408 diet and prey capture, 307Ð309 ASMO workshop, 12, 22, 30 predators, 309Ð310 systematics, 293Ð301 Climate change and marine mammals, 431Ð464 B climate change, 441Ð445 climate patterns, 444Ð445 Bacteria, in opisthobranchs, 225, 245, 248, 252, 256 CO concentration and pH, 443Ð444 Ballast water, 326 2 ENSO, 445 Behaviour, of cirrate octopods, 310Ð316 NAO, 445 Biodiversity, in coralligenous assemblages, 147Ð158 ocean circulation, 442Ð443 Bioerosion, in coralligenous assemblages, 139, 164Ð165 rainfall patterns, 444 Bioluminescence, in cirrate octopods, 277, 278, 282, 295, salinity, 443 308, 314, 316, 317 sea level, 442 Biomechanics, of burrowing, 109Ð110 sea-ice extent, 443 Biosynthesis, in opisthobranchs, 198, 253, 254, 255, 258 storms, wind, waves, 444 Biotic relationships, in coralligenous assemblages, temperature, 442 159Ð163 conservation and legislation, 455Ð456 Bioturbation, 111Ð112 impacts of, 445Ð455 Bonn Convention on the Conservation of Migratory Species climate patterns, 454 of Wild Animals (CMS), 433, 455 CO concentration and pH, 453 Bottlenecks, 327, 336, 353, 392, 402, 410, 2 decrease in ice cover, 451Ð452 Burrowing of macrofauna, 85Ð121 ocean currents, 450 in mud, 97Ð105 rainfall patterns, 453Ð454 in sand, 105Ð108 rising sea levels, 450 salinity, 452Ð453 C storms, wind, waves, 454 temperature, 446Ð450 Carbonate production, in coralligenous assemblages, 164 community structure, 447Ð448 Central nervous system, uptake of manganese, 74Ð75 direct, 446 Chemical defence, in opisthobranchs, 197, 198, 199, 253, distribution, abundance, migration, 446Ð447 255 increased susceptibility, 449Ð450 Chemical ecology, in coralligenous assemblages, 161 indirect, 446 of opisthobranchs, 197, 198, 253Ð256, 257 reproductive success, 448Ð449 Chlorophyll, 4, 5, 10, 11, 12, 13, 14, 16, 18, 19, 20, 21, implications for management and conservation, 456 22, 23, 24, 26, 27, 28, 29, 20, 21, 32, 33, 34, knowledge gaps and future research, 456Ð457 35, 36, 37, 38, 40, 41, 42, 43, 46 range of marine mammals, 432Ð441 Cirrate octopods, taxonomy, ecology, behaviour, 277Ð322 summary, 457Ð458 behaviour, 310Ð316 Climate Models (GCM), 441, 443 deep-sea adaptations, 310 COHERENS model, 1, 2, 3, 5, 29, 30 feeding, 315Ð316 Colonisation, 325, 328, 329, 331Ð334, 335, 336, 337, 338, locomotion, 311Ð313 339, 343, 345, 349, 352, 353, 355, 358, 360, responses to disturbance, 314 361, 365, 367, 370, 374, 392, 399, 400, 401, comparative anatomy, 278Ð293 408, 410

515 7044_Idx.fm Page 516 Tuesday, April 25, 2006 1:43 PM

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Commensalism, in coralligenous assemblages, 125, 161, correlation of chemical ecology with histology, 162, 163, 180 253Ð256 Comparative anatomy, of cirrate octopods, 278Ð293 correlation of histology with taxonomy and Connectivity, 323, 325, 326, 327, 328, 329, 332, 335, 336, phylogeny, 337, 338, 339, 341, 342, 343, 344, 345, 346, Blochmann's glands, 256Ð257 347, 349, 351, 352, 353, 354, 355, 361, 362, dorsal mantle gland, 257 363, 365, 368, 369, 370, 371, 372Ð375, 387, MDFs, 257 388, 389Ð396, 398, 402Ð404, 405, 406Ð409, median buccal gland, 257 410 glands in the visceral cavity, 252 Conservation and legislation, marine mammals, 455Ð456 median buccal gland, 252 Conservation, implications of rafting for, 402Ð409 glandular organs in the notum, 250Ð252 Contaminants, in marine mammals, 431, 446, 449, 457 dorsal mantle gland, 250 Convention on the Trade in Endangered Species (CITES), glands in ceratal processes or tubules, 251 455 interpalleal gland, 250 Coral, 359, 360, 361, 362, 363, 365, 369, 370, 371, 375, marginal sacs, 251 389, 390, 391, 396, 398, 409 MDFs, 251Ð252 Coral, red, 124, 127, 146, 147, 158, 171, 175, 177, 180 glandular structures confined to the epidermis, Coralligenous assemblages, Mediterranean, 123Ð195 245Ð248 Crack propagation, 84, 89Ð92, 94, 97, 98Ð101, 102, 103, hypobranchial gland, 247Ð248 104, 109, 112, 113, 114, 115 single glandular cells, 245Ð246 CSM-NZB model, 1, 5, 10, 11, 12, 14, 16, 18, 21, 22, 32, spongy glands, 247 33, 42 ontogenetic studies of MDFs, 252 Cyanobacteria, in opisthobranchs, 207, 225, 250, 256 subepithelial glands, 248Ð250 acid glands, 249Ð250 Blochmann's and ink glands, 248Ð249 D multicellular glands, 250 opaline gland, 249 Datasets, for North Sea models, 1, 2, 3, 5, 6, 8, 10, 13, 21, single glands, 248 22, 24, 30, 34, 35, 39, 40 41, 42, 45, 46, 47, material and methods, 199Ð200 48, 49, 50 ontogenetic studies of MDFs, 243Ð244 DCM-NZB model, 1, 3, 5, 14, 16, 19, 22, 32, 34, 37, 38, Deposit feeding, 85, 86, 99, 111, 112, 113, 114, 115, 330 42, 44 Dilatancy, of sediments, 87, 93, 95 Deep-sea adaptations, of cirrate octopods, 310 Diseases, marine mammals, 431, 446, 449, 452, 453, 457 Defensive glandular structures in opisthobranch molluscs, Dispersal, 328Ð339 197Ð276 colonisation and establishment, 331Ð334 conclusions, 257Ð258 pathways, 338Ð339 description of glands, 200Ð242 patterns, 336Ð338 glands in the visceral cavity, 242 general considerations, 328Ð329 median buccal gland, 242 metapopulation structure and processes, 334Ð336 glandular organs in the notum, 230Ð242 rafting dispersal, 329Ð331 dorsal mantle gland, 230 Dispersal, and evolution, 398Ð402 glands in ceratal processes or tubules,230 Disturbance, in coralligenous assemblages, 174Ð178 Diver activity, in coralligenous assemblages, 177Ð178 interpalleal gland, 230 Diversity, genetic, 323, 332, 335, 336, 337, 338, 341, 350, marginal sacs, 230 351, 353, 355, 358, 360, 361, 362, 386, 392, MDF-like structures, 233Ð242 402, 410 MDFs, 230Ð233 species, 335, 399 glandular structures confined to the epidermis, DNA, 354,356, 364, 366, 367, 368, 369, 370, 372, 376, 200Ð228 378, 379, 381, 382, 383, 384, 385, 386, 393, hypobranchial gland, 228 395, 410 single glands, 200Ð227 DYMONNS model, 1, 3, 5, 10, 11, 14, 18, 20, 21, 22, 30 spongy glands, 227Ð228 subepithelial glands, 228Ð230 acid glands, 229 E Blochmann's and ink glands, 228Ð229 multicellular glands, 230 ECOHAM model, 1, 2, 3, 4, 5, 6, 10, 11, 12, 15, 16, 21, opaline gland, 228 22, 23, 24, 39, 40, 41, 42 single glands, 228 Ecological modelling of North Sea shelf system, 1Ð60 discussion, 244Ð257 discussion and conclusions, 44Ð50

516 7044_Idx.fm Page 517 Tuesday, April 25, 2006 1:43 PM

SUBJECT INDEX

causes for lack of coincidence with data, 47Ð49 terrestrial debris, 364Ð365 complexity of system's representation, 48 volcanic pumice, 360Ð364 spatial and temporal resolution of dynamics, frequent natural, 340Ð351 47Ð48 continuous supply of substrata, 340 uncertainty in initialisation and forcing data, dispersal dynamics, 349Ð351 48Ð49 macroalgal belts 347Ð248 data needs, 50 mangroves, 348Ð349 methodology for validation, 49Ð50 salt marshes, 343Ð347 status of validation and data needs, 45Ð47 seagrass beds, 341Ð343 annual cycles, 46 intermittent natural, 351Ð358 events, 46 dispersal dynamics, 355Ð358 long-term developments, 46Ð47 kelp forests, 353Ð355 regional distributions, 46 regular supply of substrata, 351Ð353 model comparisons and complexity, 41Ð44 trees, 355 validational efforts, 2Ð6 Ecology, of cirrate octopods, 301Ð310 validational status, 6Ð41 El Niño, 444, 445, 447, 448, 454, 455 applied validation methods, 7Ð10 status of models, 10Ð41 El Niño-Southern Oscillation (ENSO), 445 annual cycles, 19Ð34 Elastic behaviour, sediments, 87, 92, 94, 96, 103, 104, 116 events, 37Ð41 Elasticity of mud, 88Ð89, 110 long-term developments, 34Ð37 ELISE model, 1, 2, 3, 5, 14, 16, 30, 31, 34, 36 regional distributions, 10Ð19 Endangered species, 158Ð159, 434, 435, 436, 438, 439, verification status, 7 440, 446, 455 Ecology of rafting, 323Ð429 Endosymbiosis, in opisthobranchs, 256 dispersal in the sea, 328Ð339 ENSO, 358, 359 colonisation and establishment, 331Ð334 Epibiosis, in coralligenous assemblages, 125, 161, 162, 179 dispersal pathways, 338Ð339 ERSEM model, 1, 2, 3, 4, 5, 6, 10, 11, 12, 15, 16, 17, 18, dispersal patterns, 336Ð338 21, 22, 23, 24, 25, 26, 27, 28, 29, 34, 39, 40, general considerations, 328Ð329 41, 44, 45 metapopulation structure and processes, 334Ð336 Excretion, of manganese, 75Ð76 rafting dispersal, 329Ð331 Exoskeleton, uptake of manganese, 71Ð73 implications for conservation, 402Ð409 changes in rafting opportunities, 404Ð406 connectivity and conservation, 402Ð404 F modern coastlines and connectivity, 406Ð409 outlook, 409Ð411 Feeding, of cirrate octopods, 315Ð316 rafting dispersal, 372Ð402 of macrofauna in cracks, 112Ð114 dispersal and evolution, 398Ð402 Fishing, in coralligenous assemblages, 177

isolation and secondary admixture, 401Ð402 Fixation index (FST), 373, 374, 375, 376, 377, 378, 379 380, local recruitment and deme formation, 398Ð400 381, 382, 383, 384, 385, 386, 387, 392, 397, transport and colonisation, 400Ð401 398 gene flow patterns and developmental mode, Fluidisation, of sediments, 107Ð108 396Ð398 Founder effects, 327, 331, 332, 334, 336, 337, 352, 353, marine connectivity, 372Ð375 360, 361, 370, 392, 402, 410 genetic homogeneity and structure, 374Ð375 FYFY model, 1, 3, 5, 42, 43, 44 use of genetic data, 372Ð374 rafting-mediated connectivity, 389Ð396 0-100km, 389Ð390 G 100-1000km, 390Ð391 1000-5000km, 391Ð394 Gene flow, 375Ð388 >5000km, 394Ð396 pools, 335, 360 rafting-mediated gene flow, 375Ð388 Genetic structure, marine invertebrate populations, routes, 339Ð372 374Ð375 artificial, 371Ð372 GHER model, 1, 2, 3, 5, 16 episodic natural, 358Ð371 Gills, uptake of manganese, 67Ð69 dispersal dynamics, 369Ð371 Glands, in opisthobranchs, 200Ð242, 245Ð252 giant kelp and other substrata, 365Ð369 Great Barrier Reef (GBR), 373, 377, 378, 383, 389, 390, sporadic supply of substrata, 358Ð360 391, 396, 398

517 7044_Idx.fm Page 518 Tuesday, April 25, 2006 1:43 PM

SUBJECT INDEX

H biomechanics of burrowing, 109Ð110 bioturbation, 111Ð112 Haemolymph, uptake of manganese, 69Ð70 feeding in a crack, 112Ð114 Histology, correlation with taxonomy and phylogeny, methodological considerations, 114Ð115 256Ð257 nonrandom distribution of animals, 110Ð111 Hydrostatic skeleton, of burrowers, 101Ð103, 109 summary and future directions, 115Ð116 terrestrial implications, 108Ð109 Management and conservation, of marine mammals, 456 I Manganese in crustaceans, role, routes and effects, 61Ð83 biological role, 62Ð64 ICES boxes, 5, 12, 16, 17, 18, 30 deficiency, 64 data, 10, 12 essentiality, 62Ð63 Intergovernmental Panel on Climate Change (IPCC), 441 toxicity, 63Ð64 International Whaling Commission (IWC), 455 conclusions, 76 Invasive species, in coralligenous assemblages, 178 geochemical role, 61Ð62 Island biogeography, 335 overview, 64Ð67 routes and effects, 67Ð76 excretion, 75Ð76 K uptake from food, 75 uptake from water, 67Ð75 Kelp, 323, 332, 334, 351, 353Ð355, 365, 368, 369, 393, central nervous system, 74Ð75 406, 407 exoskeleton, 71Ð73 Key species, in coralligenous assemblages, 168Ð174 female reproductive system, eggs, 73 Krill, 446, 452, 453 gills, 67Ð69 haemolymph, 69Ð70 L male reproductive system, 73Ð74 midgut gland, 70Ð71 Life history characteristics, 375, 399, 404 muscle, 71 Light, affecting distribution of coralligenous assemblages, Mangroves, 323, 332, 333, 340, 348Ð349, 351, 355, 356, 126Ð128 365, 381, 382, 390, 392, 393, 394, 400, 406, Locomotion, of cirrate octopods, 311Ð313 407, 409 Marine mammals, effects of climate change on, 431Ð464 Marine protected areas (MPA), 402, 403, 404 M Mediterranean coralligenous assemblages, 123Ð195 actions, 181Ð182 Macroalgae, in rafting, 326, 330, 332, 340, 345, 347Ð348, gaps in knowledge, 181 351, 358, 359, 367, 377, 379, 380, 381, 384, recommendations for protection, 181Ð182 385, 389, 390, 391, 393, 394, 406 biodiversity, 147Ð158 Macrofaunal burrowing, 85Ð121 taxonomic groups, 148Ð158 background solid mechanics, 88Ð94 biotic relationships, 159Ð163 cracks and crack propagation, 89Ð92 chemical ecology, 161 elasticity of mud, 88Ð89 epibiosis, mutualism, commensalism, parasitism, granular materials, 92Ð94 161Ð163 basic terminology, 87Ð88 spatial interactions, herbivory, carnivory, 159Ð161 bulk mechanical properties of sediments, 94Ð97 conclusions on current knowledge, 179Ð181 burrowing in mud, 97Ð105 description, 123Ð124 burrowing with a hydrostatic skeleton, 101Ð103 disturbances, 174Ð178 dependence on mud properties,101 degradation, by diver activity, 177Ð178 mechanism, 97Ð98 by fishing, 177 peristalsis as a way to crack, 104Ð105 by waste water, 176 soupy muds, 103Ð104 invasive species, 178 ubiquity of crack propagation, 98Ð101 large-scale events, 174Ð176 burrowing in sand, 105Ð108 dynamics and seasonality, 165Ð168 differentiation from mud, 105Ð106 endangered species, 158Ð159 mechanism, 106Ð107 environmental factors and distribution, 126Ð133 use of fluidisation, 107Ð108 depth, 132Ð133 discussion and implications, 108Ð115 geographical distribution, 132

518 7044_Idx.fm Page 519 Tuesday, April 25, 2006 1:43 PM

SUBJECT INDEX

light, 126Ð128 NORWECOM model, 1, 2, 3, 4, 5, 6, 10, 11, 12, 13, 14, nutrients, POC, DOC, 128Ð129 15, 16, 22, 40, 42 salinity, 132 Nurtients, affecting distribution of coralligenous temperature, 130Ð132 assemblages, 128Ð129 water movement, 129Ð130 functioning of outstanding and key species, 168Ð174 Alcyonaria, 173 O coralline algae, 168 Ocean circulation, 442Ð443 Corallium rubrum, 170Ð171 Ocean weather ship, 8 Gorgonia, 172Ð173 OSPAR Commission, 5 Halimeda tuna, 168Ð169 OSPAR workshop, 19 Hydrozoa, 170 Porifera,169Ð170 Tunicata, 174 P Zoantharia, 173Ð174 Parasitism, in coralligenous assemblages, 125, 153, 161, history and main studies, 124Ð126 162, 163, 180 algal studies, 125Ð126 Peristalsis, of burrowers, 98, 103, 104Ð105 historical account, fauna, 124Ð125 Phytoplankton, 449, 453 processes, 163Ð165 Plastics, 326, 330, 340, 371, 386, 393, 396, 404, 405, 406, 409 bioerosion, 164Ð165 POLCOMS-ERSEM model, 1, 2, 3, 4, 5 carbonate production, 164 Predators, of cirrate octopods, 309Ð310 growth and age, 163Ð164 Protection, of coralligenous assemblages, 181Ð182 sedimentation, 165 Pumice, 323, 326, 327, 330, 340, 359, 360Ð364, 369, 371, structure, 133Ð147 378, 389, 390, 391, 398, 404, 406, 409 algal builders, 134Ð137 animal builders, 137Ð138 assemblages, 140Ð147 R bioeroders, 138Ð140 Rafting, ecology of, 323Ð429 coralligenous types, 133Ð134 Rainfall patterns, 444, 453Ð454 Metapopulation structure and processes, 334Ð336 Reproduction, of cirrate octopods, 302Ð307 Microsatellites, 344, 357, 372, 376, 378, 379, 383, 410 Reproductive strategy, of cirrate octopods, 304Ð307 Midgut gland, uptake of manganese, 70Ð71 system, of cirrate octopods, 288, 291 Migration, by rafting, 324, 326, 331, 335, 336, 337, 350, uptake of manganese, 73Ð74 356, 373, 374, 386, 387, 388, 390, 392, 393, 394, 403, 404 marine mammals, 431, 432, 433, 440, 441, 446, 447, S 450, 451, 452, 454, 456, 457, 458 Salt marshes, 343Ð347, 349, 351, 355, 357, 400, 407, 409 Modelling, of North Sea shelf system, 1Ð60 Sea ice, cover, 451Ð452 Moulting, in crustaceans, 64, 69, 71, 72, 75 extent, 443 Mucopolymers, 85, 87, 91, 111 Sea level, 442, 450 Mucopolysaccharides, 200, 201, 228, 245, 248 Seagrass, 323, 330, 332, 333, 339, 341Ð343, 345, 346, 349, Muscle, uptake of manganese, 71 351, 357, 358, 381, 409 Mutualism, in coralligenous assemblages, 161,162, 180 Sedimentation, in coralligenous assemblages, 125, 140, 156, 158, 165, 177, 180 in North Sea, 5, 30 N Sediments, mechanical properties of, 94Ð97 Sequestration, of chemicals in opisthobranchs, 198, 250, Natural products, in opisthobranchs, 202Ð226, 250, 251, 253, 254, 256 253, 255, 256 Spermatophores, of cirrate octopods, 278, 279, 281, 288, Nervous system, of cirrate octopods, 286, 290 290, 292, 302, 304, 316 North Atlantic Oscillation (NAO), 445 Solid mechanics, as background to burrowing, 88Ð94 North Sea shelf system, ecological modelling of, 1Ð60 Storms, wind, waves, 444, 454 North Sea, climate change, 442, 443, 444, 447, 449, 453, Suspension feeders, 330, 331, 349 455, 456 Symbionts, in opisthobranchs, 256 rafting in, 334, 343, 347, 357, 406, 407, 408 Systematics, of cirrate octopods, 293Ð301

519 7044_Idx.fm Page 520 Tuesday, April 25, 2006 1:43 PM

SUBJECT INDEX

T W

Thixotropy, of sediments, 87, 95 Water movement, affecting distribution of coralligenous Toxicity, of manganese, 63Ð64 assemblages, 129Ð130 Trees, 323, 327, 332, 349, 355, 356, 359, 364, 365, 369, Weather prediction, 49 371, 381, 392 World Conservation Union (IUCN), 455 Trophic ecology, of cirrate octopods, 307Ð310 Tsunamis, 339, 359, 363Ð365 Z V Zooplankton, 449, 453 Validation, of North Sea models, 1Ð60 Zooxanthellae, in opisthobranchs, 256

520

7044_C009.fm Page 521 Wednesday, April 26, 2006 9:11 AM

Colour Figure 7 (Ballesteros) Types and habitats in coralligenous outcrops. (A) small coralligenous accretion apparently developed from the coalescence of rhodoliths (Tossa de Mar, NE Spain, 40 m depth); (B) coralligenous bank grown upon a rocky outcrop (Tossa de Mar, NE Spain, 25 m depth); (C) community dominated by suspension feeders in a coralligenous cavity (Cabrera, Balearic Islands, 52 m depth); (D) coralligenous rim on a vertical cliff (Gargalo, Corsica, 48 m depth). (Photos by the author.)

Colour Figure 8 (Ballesteros) Main red algal building species in coralligenous frameworks. (A) Mesophyllum alternans; (B) Lithophyllum frondosum; (C) Lithophyllum cabiochae; (D) Neogoniolithon mamillosum; (E) Peyssonnelia rosa-marina. (Photos by the author.)

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Colour Figure 9 (Ballesteros) Some animal building species in coralligenous frameworks. (A) Miniacina miniacea; (B) Pentapora fascialis; (C) Myriapora truncata; (D) Serpula vermicularis; (E) Leptopsammia pruvoti. (Photos by the author.)

Colour Figure 10 (Ballesteros) Bioeroders in coralligenous frameworks. (A) Cliona viridis; (B) Sphaerechi- nus granularis; (C) Echinus melo; (D) browsing marks of Sphaerechinus granularis over Lithophyllum frondosum. (Photos by the author.)

7044_C009.fm Page 523 Wednesday, April 26, 2006 9:11 AM

Colour Figure 11 (Ballesteros) Diagrammatic section of a coralligenous bank, showing the high small-scale environmental heterogeneity and the different microhabitats. (Drawing by J. Corbera.)

Colour Figure 13 (Ballesteros) Different assemblages of algal-dominated coralligenous banks and rims; (A) with Halimeda tuna and Mesophyllum alternans (Tossa de Mar, NE Spain, 28 m depth); (B) with Litho- phyllum frondosum (Tossa de Mar, NE Spain, 40 m depth); (C) with Peyssonnelia rosa marina, Mesophyllum alternans, Palmophyllum crassum and Peyssonnelia squamaria (Scandola, Corsica, 50 m depth); (D) detail of C. (Photos by the author.)

7044_C009.fm Page 524 Wednesday, April 26, 2006 9:11 AM , , 14 19 Serpula ), 23 Epinephelus

, 8 Right, from top

32 azoanthus axinellae Aglaophenia septifera Par ),

, 22 24 Codium bursa

, 29 Chromis chromis. Chromis Discodoris atromaculata and 18 Pteria hirundo

and , 27 12 alinurus elephas P

(Drawing by M. Zabala & J. Corbera.) (Drawing ,

6 Diplodus sargus .

10 , 15 Corallium rubrum Corallium

, 3 Agelas oroides Agelas

, Smittina cervicornis Halecium halecinum Dysidea avara 1

, 13 Eunicella singularis

, (and on it

31 (and on it , 6

4 Clathrina coriacea

, 28 Synthecium evansi

, 25 Lithophyllum frondosum

, Anthias anthias 11 amuricea clavata etrosia ficiformis etrosia P

Par , 5 Halocynthia papillosa

, Galathea strigosa

20 , Acanthella acuta

26 , 17 (A) Drawing of a deep-water, animal-dominated, coralligenous assemblage in the Medes Islands (NE Spain). of a deep-water, (A) Drawing

Chondrosia reniformis Chondrosia

, 9 Alcyonium acaule Caryophyllia inornata

, , Phyllangia mouchezii 7

, 21 30 vermicularis Colour Figure 14 (Ballesteros) Colour Figure Cliona viridis cunctatrix Spirastrella marginatus (B) to major species, left from top to bottom: Key to bottom (excluding the above-mentioned species): the above-mentioned to bottom (excluding

7044_C009.fm Page 525 Wednesday, April 26, 2006 9:11 AM

Colour Figure 15 (Ballesteros) Different assemblages of animal-dominated coralligenous banks and rims; (A) with gorgonians Paramuricea clavata and Eunicella cavolinii but also green algae Halimeda tuna and Flabellia petiolata (Gargalo, Corsica, 45 m depth); (B) with Paramuricea clavata and encrusting sponges in deep waters (Cabrera, Balearic Islands, 65 m depth); (C) with sponges, bryozoans and anthozoans (Cabrera, Balearic Islands, 50 m depth); (D) overhangs with Corallium rubrum (Palazzu, Corsica, 35 m depth). (Photos by the author.)

Colour Figure 16 (Ballesteros) Spatial interactions are crucial in the buildup of coralligenous assemblages. (A) Mesophyllum alternans overgrows Lithophyllum cabiochae which, in its turn, is epiphytised by the small green alga Halicystis parvula (above) and a tunicate (below); (B) Lithophyllum frondosum overgrows sponge Ircinia oros. Strong prey selection is present in the coralligenous community. (C) Opisthobranch Discodoris atromaculata feeds almost exclusively on sponge Petrosia ficiformis; (D) Opisthobranch Flabellina affinis feeds on hydrozoans of the genus Eudendrium. (Photos by the author.)

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Colour Figure 17 (Ballesteros) (A) Space competition can also be mediated by trophic depletion of the surrounding waters, or by allelochemicals. Tunicate Pseudodistoma cyrnusense inhibits growth of bryozoan Hornera frondiculata; (B) Zoantharian Parazoanthus axinellae is usually a selective epibiont of sponge Axinella damicornis; (C) Nonselective epibionts overgrow the gorgonian Paramuricea clavata: the worm Salmacina dysteri and the bryozoan Pentapora fascialis; (D) The barnacle Pyrgoma anglicum living inside the anthozoan Leptopsammia pruvoti can be considered a case of parasitism. (Photos by the author.)

2

5

10

15

20

Coralligenous 25

30

35

Colour Figure 18 (Ballesteros) Maps of transition intensity resulting from overlay procedures of images from the same plot (310 cm2) along a depth gradient in a vertical wall at the Medes Islands (NE Spain) during 2 yr of sampling. Patch colour denotes number of changes taking place in each patch (see legend). Corallig- enous communities (14 and 20 m depth) display much lower transition rates than shallow water communities, indicating high persistence and low rates of change in the animals and plants thriving in the coralligenous communities. (From Garrabou et al. 2002. With permission from Elsevier.)

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Colour Figure 22 (Ballesteros) A red coral colony (age unknown) from a pristine site (Cap Creus, 35 m) collected in 1962 (A), and a 28-year-old colony from an experimental panel (Riou Caramassaigne, 62 m) (B). (Photo and data courtesy of J.G. Harmelin.)

Colour Figure 25 (Ballesteros) Disturbances in coralligenous communities. (A) Mortality affecting the gorgonian Paramuricea clavata (Port-Cros, France, autumn 1999); (B) Dense carpets of alien alga Womers- leyella setacea cover coralligenous assemblages; the gorgonian Eunicella singularis is also affected by previous partial mortality that occurred in summer 1999 (Minorca, Balearic Islands, summer 2000); (C) Filamentous alien alga Womersleyella setacea invades coralligenous rims dominated by Mesophyllum alternans in Cabrera (Balearic Islands, autumn 1999); (D) Partial mortality and overgrowth by filamentous algae affecting gorgonian Eunicella singularis (Minorca, Balearic Islands, summer 2000). (Photos by the author.)

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Colour Figure 2 (Collins & Villanueva) Photographs of cirrate octopods. (A) dorsal view of Opisthoteuthis massyae (fresh specimen), (B) ventral view of Crypto- teuthis brevibracchiata (fresh specimen), (C) dorso- posterior view of Cirroctopus glacialis (fresh specimen), (D) ventral view of Grimpoteuthis discoveryi (formalin- preserved specimen), (E) ventral view of Cirrothauma murrayi (fresh specimen), (F) oral view of male Stauro- teuthis syrtensis (formalin-preserved specimen), (G) Juvenile specimen of Opisthoteuthis calypso, note the relatively large fins and funnel in comparison with the adult Opisthoteuthis in (A). Sources (with permission where required): (A) Collins unpublished; (B) from Col- lins (2004); (C) Mike Vecchione unpublished; (D) from Collins (2003); (E) from Aldred et al. (1983); (F) from Collins & Henriques (2000); (G) L. Dantart. Scale bars: (AÐF) = 100 mm; (G) = 10 mm.

Colour Figure 20 (Collins & Villa- nueva) Photographs of cirrate octopods taken from the manned submersible NAUTILE at the mid-Atlantic Ridge, illustrating behaviour. Grimpoteuthis sp.: (A) bottom resting and (B, C) crawling. Cirroteuthidae: (D) drifting in umbrella style, (E) during take off and (F) fin-swimming. Grimpoteuthis sp.: (G-I) fin-swimming. Cirro- teuthidae: (J) umbrella drifting, (K, L) taking off after touching submersible and displaying long cirri, (M, N) swim- ming by pumping. (O) Cirrothauma magna being manoeuvered into a sam- ple box, showing ballooning response in three web sectors. (From Villanueva et al. (1997). With permission.)