Studies on Baltic Sea Mysids

Home , Mysis, Mysis diluviana, Mysis relicta, Mysis salemaai, Neomysis integer, Praunus

Studies on Baltic Sea mysids

Martin Ogonowski

Department of Systems Ecology Stockholm University

Doctoral thesis in Marine Ecology Martin Ogonowski, [email protected]

Department of Systems Ecology Stockholm University SE-106 91 Stockholm, Sweden

©Martin Ogonowski, Stockholm 2012

ISBN 978-91-7447-510-4

Printed in Sweden by US-AB, Stockholm 2012 Distributor: Department of Systems Ecology, Stockholm University Cover and chapter dividers: ©Ruggero Maramotti

Abstract

Mysid shrimps (Mysidacea, Crustacea) are efficient zooplanktivores in both marine and freshwater systems as well as lipid rich prey for many species of fish. Although some efforts have been made to study the role of mysids in the Baltic Sea, very few studies have been carried out in recent time and there are still knowledge gaps regarding various aspects of mysid ecology. This thesis aims to explore some of these gaps by covering a mixture of topics. Using multifrequency hydroacoustics we explored the possibility to separate mysids from fish echoes and successfully established a promising and effective method for obtaining mysid abundance/biomass estimates (paper I). An investigation of the current mysid community in a coastal area of the northern Baltic proper (paper II) demonstrated that the formerly dominant, pelagic mysid Mysis mixta had decreased substantially (~50%) in favor for phytoplanktivorous, juvenile Neomysis integer and Mysis relicta sp. By examining different aspects of mysid behavior, we studied the vertical size distribution of mysids in the field and found that size increased with depth/declining light, irrespective of temperature; indicating that their vertical size distribution primarily is a response to predation (paper II). In paper III, a combination of ecological and genetic markers was used to investigate intraspecific differences in migratory tendency. Both marker types indicated that some part of the Mysis salemaai population is sedentary on the bottom and that this strategy is a phenotypically plastic but persistent trait, analogous to the partial migrations seen in many birds and fishes. In paper IV a temperature and weight specific respiration model was developed for the littoral Praunus flexuosus. Routine respiration was moreover elevated by post-prandial effects (specific dynamic action) for longer times than previously suggested. Consequently, ignoring such effects could significantly bias respiration measurements.

Keywords: Mysids, hydroacoustics, Baltic Sea, abundance, stable isotopes, specific dynamic action (SDA), diel vertical migration, partial migration, trophic interactions, physiology, benthic-pelagic coupling, protein:DNA, C:N ratio, genetic structure. Contents

1. List of papers ...... 5 2. Contribution to papers ...... 5 3. Introduction ...... 6 3.1 Objectives ...... 7 4. Background ...... 8 4.1 Distribution and habitat choice ...... 8 4.2 Diet ...... 9 4.2.1 Mysis relicta/Mysis salemaai ...... 10 4.2.2 Mysis mixta ...... 10 4.2.3 Neomysis integer/Praunus flexuosus ...... 10 4.3 Life history and growth ...... 11 4.4 Migration patterns ...... 12 4.4.1 Effects of Light ...... 13 4.4.2 Vertical size distribution ...... 14 4.4.3 Temperature ...... 14 4.4.4 Chemical cues ...... 15 4.4.5 Niche differentiation and partial migration ...... 15 4.6 Bioenergetics ...... 16 4.7 Abundance ...... 17 4.7.1 Sampling methods ...... 18 4.7.2 Hydroacoustics ...... 18 5. Summary of papers ...... 20 6. Conclusions ...... 22 7. Acknowledgments ...... 24 8. References ...... 25

1. List of papers

I Axenrot, T., Ogonowski, M., Sandström, A. and Didrikas, T. 2009 Multifrequency discrimination of fish and mysids. ICES Journal of Marine Science 66: 1106–1110.

II Ogonowski, M., Hansson, S. and Duberg, J. 2012 Status and vertical size distributions of a pelagic mysid community in the northern Baltic proper (accepted for publication in Boreal Environment Research within a year).

III Ogonowski, M., Duberg, J., Hansson, S. and Gorokhova, E. 2012 Persistent lack of diel vertical migration in a pelagic mysid population –– a case of partial migration (Unpublished manuscript)

IV Ogonowski, M., Andersson, K. and Hansson, S. 2012 A weight and temperature dependent model of respiration in Praunus flexuosus (Crustacea, Mysidacea). (Journal of Plankton Research, in–press).

2. Contribution to papers

I I planned the study, collected field samples, and performed data analysis, all in close collaboration with the co-authors.

II I planned the study in collaboration with Sture Hansson. I collected and prepared all data except for isotopic samples (Jon Duberg). I performed all the data analyses and I wrote the manuscript in close collaboration with SH.

III I formulated the hypotheses and designed the study together with Elena Gorokhova and SH. JD and I conducted the field work. JD generated stable isotope data, EG and I performed molecular analyses. I performed statistical analyses and wrote the manuscript in close collaboration with the co-authors.

IV I designed the study together with SH and executed the experiments together with Kristoffer Andersson. I performed the data analysis and wrote the manuscript in collaboration with the co-authors.

Published and accepted papers are reprinted with kind permission from the publishers: (I, IV) Oxford University Press and (II) Boreal Environment Research.

3. Introduction

Many aquatic ecosystems have undergone considerable changes during the last century due to variations in anthropogenic and environmental factors, with eutrophication and overfishing being two of the most prominent forces. This in turn, is reflected in changed species composition at several trophic levels. In the case of the Baltic Sea, top predators such as the cod (Gadus morhua) that dominated in the 1980s have been depressed to very low levels and the system was shifted towards being dominated by planktivorous clupeids (herring (Clupea harengus membras) and sprat (Sprattus sprattus)). At the same time, the mesozooplankton community changed from being dominated by Pseudocalanus sp. to Temora longicornis and Acartia spp. (in the Gotland Basin and Gdańsk Deep). Solid explanations for these changes are lacking but the observed changes in zooplankton species composition have been linked to a deteriorating condition in herring, which is one of the most important commercial species in the Baltic Sea (Möllmann et al. 2004; Möllmann et al. 2005). Even though herring predominantly feed on different species of copepods and cladocerans, older herring consume substantial amounts of larger invertebrates, such as mysid shrimps (Mysidacea, Crustacea) (Aneer 1975), and a decrease in large prey like mysids could be one explanation to the decreased growth in herring (Arrhenius and Hansson 1993). The rapid ongoing increase in the cod stock (Cardinale and Svedang 2011) will provide good possibilities for studying and testing these and other hypotheses regarding the role of trophic interactions in the structuring of the Baltic Sea ecosystem.

Mysids are, due to their high content of polyunsaturated fatty acids (Arts and Johannsson 2003) believed to be an important part of pelagic fishes’ diet during autumn and winter when other food sources are scarce (Aneer 1980; Lankov and Kukk 2002; Posey and Hines 1991; Raid and Lankov 1995; Szypula 1985) and by that have the potential of decreasing overwintering mortality (Snyder and Hennessey 2003). Holliday et al. (1989) further proposed that a mixed diet was crucial for a good WAA (weight at age) in older herring.

Population dynamics is a cornerstone in ecology. Feeding interactions between species are often complex and cascading effects between trophic levels are common. In studies of seasonal population dynamics and trophic interactions in the Baltic pelagic system, mysids have been only vaguely considered (Möllmann et al. 2004; Möllmann et al. 2005). The reason for this is the lack of long term data on mysid abundances. Very few continuous monitoring surveys have been conducted on mysid populations in the Baltic and there is thus little information on temporal and spatial population dynamics. There is however strong evidence that mysids have an exceptional potential of structuring zooplankton communities; directly by consuming zooplankton but also indirectly by competing with herring for food. Rudstam et al. (1986) found that Mysis mixta could consume 23-51% of net annual zooplankton production in a coastal area of the Baltic proper. Mathematical models on intra guild predation (IGP) further suggest that intermediate predators like mysids must be superior competitors for a shared resource in order to persist in the system (MacLennan and Holliday 1996).

However, recent anecdotic and indirect information suggests a significant decrease in mysid abundance compared to the 1980’s, in several parts of the Baltic Sea. A recent study by Dziaduch (2011) reported that the occurrence of mysids (primarily Mysis mixta) had decreased considerably in both herring and cod stomachs in 2007 and 2008 (southern Baltic Sea); from being a very important food item during the 1980s and early 1990s to a minor component in 2007 and 2008. Möllmann et al. (2005) also observed a steady decrease in mysid biomass in herring stomachs, during autumn, from 1987 and onwards. This observation

6 overlaps with the demise of the cod stock, the low WAA of herring and the increase in sprat stocks.

Since mysids play such a significant role in the Baltic food-web it is important to understand how, when and by which factors fish and mysids interact with each other. Despite a fair understanding of general mysid ecology, most knowledge is based on experimental studies and time series data on abundances and biomass are lacking due to sampling difficulties associated with patchy distributions and gear avoidance during day-time; thereby making it difficult to accurately assess long-term population dynamics and food-web functions.

3.1 Objectives

This thesis, aims to fill some of the current gaps in mysid ecology by covering a wide range of topics. A fundamental step towards a better understanding of food-web interactions is access to reliable data on distributions and abundances. In paper I, we investigated the possibilities of a novel technique which may provide such data efficiently; namely multifrequency hydroacoustics. Sonar technology has traditionally been used for the study of fish populations since it covers large areas effectively and is a non-invasive method, minimizing bias common to different types of towed gear.

With their swim bladder, fish are efficient reflectors of sound, but recent advances in hardware development and post-processing software have made it possible to roughly distinguish other groups of organisms aside from fish. This may be achieved by combining echoes from different frequencies, thereby producing “finger prints” of different organisms such as zooplankton, mysids and fish. The study was conducted in Lake Vättern, the second largest lake in Sweden, which hosts a similar composition of functional groups as the Baltic Sea, including mysids and planktivorous, pelagic fish.

Although this technique provides extensive improvements on biomass estimates it relies on known target strengths (the strength of the received echo, TS) of individual mysids for abundance estimation. Since TS is more or less proportional to the size of objects, it is important to understand how, when and where different sizes are distributed in the water column. For this reason, efforts were made to decipher the underlying factors that govern vertical size distributions of mysids (paper II). Moreover, since recent mysid abundance data is lacking and the Baltic Sea in many ways has changed since the last mysid investigations in the 1980s, paper II also presents new data on mysid abundances, species composition and trophic position from a formerly well studied coastal area of the northern Baltic proper.

This vertical dispersal of mysids is strongly linked to the nocturnal diel vertical migrations (DVM) from deep dark waters towards the surface at night and is performed by mysids as well as many other pelagic organisms. The behavior is generally proposed to be a trade-off between experiencing higher temperatures and food concentrations close to the surface which promote growth and reproduction at costs associated with greater predation pressure. Even though DVM generally is accepted to be working on a population level there is considerable and commonly ignored individual variation as some individuals do not seem to migrate. In paper III, we investigated whether this lack of migration is temporary or in fact stable over longer time periods and what ecological and evolutionary consequences a resident versus migratory strategy may have on ecosystem functioning.

In the last paper (paper IV) we examined the effects of fasting on respiration in a common littoral mysid species (Praunus flexuosus) and constructed a model of respiration as a function of temperature and body size. When animals are collected in the field, their feeding history is seldom known which means that basal metabolic rates may be overestimated due to elevated respiration related to what and how much they had been feeding before collection (specific dynamic action, SDA). The establishment of a precise basal metabolic rate is important in larger modeling contexts since it stands for a major part of an animal’s energy expenditure.

4. Background

4.1 Distribution and habitat choice

Opossum shrimps (Mysids) are common crustaceans in many marine and fresh water environments. They can be found all the way from shallow coastal areas down to depths of several thousand meters. Some are strictly pelagic, while others are benthic. Altogether there are more than 1000 species distributed worldwide (Mauchline 1980).

In the Baltic Sea there are 19 known species of mysids. Ten of these are restricted to the entrance region of the Baltic Sea (the Kiel and Mecklenburg bights) due to limited tolerance of low salinity water (Köhn 1992). The by far most abundant species in the Baltic proper are Mysis mixta, Mysis relicta (pelagic species), Neomysis integer and Praunus flexuosus (littoral species). Furthermore, Mysis relicta has recently been found to constitute a complex of four sibling species that hardly are distinguishable by morphology, but have genetic and life history differences (Väinolä and Vainio 1998). Two of these species are found in the Baltic Sea (M. relicta and M. salemaai) whereas the other two are restricted to North American fresh water systems (M. diluviana and M. segerstralei). In general, M. relicta prevails in coastal and peripheral areas of the Baltic whereas M. salemaai is most common in the pelagic where it coexists with M. mixta (Väinölä 1992). Unless otherwise stated, the M. relicta species complex will hence forth be referred to as M. relicta.

Mysis mixta is originally a marine species and its distribution in the Baltic is limited northwards, up to the Northern Quark area due to low salinities (Salemaa et al. 1990). The freshwater glacial relict M. relicta, on the contrary, is limited southwards by increasing salinity and does not occur where salinities are greater than 12 ppm (Ackefors 1969). The littoral N. integer and P. flexuosus are abundant all along the Baltic coasts.

Low bottom-oxygen concetrations have also been coupled with low mysid abundances (Salemaa et al. 1986; Salemaa et al. 1990). A current hypothesis is that access to bottom could be important for the maintenance of mysid populations. Avoiding predation by hiding on or in the bottom sediment could be one of the reasons for this coupling. In later studies, however, substantial mysid densities have been observed in areas with low bottom-oxygen concentrations (Välipakka 1992). These occurrences could be explained by horizontal migration/drift of animals from areas with better bottom-oxygen conditions or by the existence of strictly pelagic mysids that do not depend on benthos but rather a light refugium to avoid predation from visual predators.

4.2 Diet

Feeding of pelagic mysids is strongly connected to their pronounced, vertical migration (DVM) and feeding tends to occur on a diurnal basis with a peak during night. Light itself has been shown to reduce feeding rates for pelagic mysids (Gorokhova and Hansson 1997; Lasenby et al. 1986; Viherluoto and Viitasalo 2001a) and is most likely an anti-predator response linked to DVM (Aneer 1980; Lasenby et al. 1986). However, littoral species such as Neomysis integer and Praunus flexuosus that do not rely entirely on DVM for predator avoidance, do not display reduced feeding rates in bright conditions. This implies that neither pelagic nor littoral mysids use vision but rather mechanoreception for foraging (Viherluoto and Viitasalo 2001a).

Studies on the diet of Baltic mysids are in general few in comparison with fresh water systems such as the Laurentian Great lakes. The diet of Baltic mysids has been shown to be of a mainly omnivorous character, ranging from detritus to zooplankton (Grossnickle 1982; Rudstam and Hansson 1990; Rudstam et al. 1992; Salemaa et al. 1986; Viherluoto et al. 2000). They feed on phytoplankton and detritus by creating a suspension feeding current but can also capture prey by raptorial feeding (Grossnickle 1982; Mauchline 1980; Murtaugh 1981). The extent of raptorial feeding has been shown be positively correlated with mysid size (Grossnickle 1982; Viherluoto et al. 2000).

The recent debate on the effects of toxic cyanobacteria blooms on mysids is also worth mentioning. Recently, high proportions of mysids (M. mixta and M. relicta) containing the potentially toxic Nodularia spumigena have been observed (Gorokhova 2009). The proportion of individuals ingesting cyanobacteria was however shifted towards juveniles and sub-adults. This in turn, may be explained by a higher encounter rate by smaller mysids since smaller individuals are found higher up in the water column (M. relicta: Kotta and Kotta 1999; Lasenby and Fürst 1981; Teraguchi 1969); (M. mixta: Grossnickle and Morgan 1979; Kotta and Kotta 2001; Rudstam et al. 1989; Salemaa et al. 1986; Shvetsova and Shvetsov 1990), where cyanobacterial concentration can be relatively high. Moreover, small mysids feed predominantly by suspension feeding (Lasenby and Langford 1972) which enables a high encounter rate of dominating food particles. Cyanobacteria may, however, clog the mysid’s feeding apparatus and thus have an impairing effect on feeding, resulting in a time/energy cost for cleaning the feeding apparatus (Engström et al. 2001). At high concentrations of cyanobacteria, it is possible that juvenile mysids will consume more cyanobacteria because the cost/benefit relationship makes it profitable to consume even this food of relatively poor quality compared to selecting only food that are scarce but of good quality. Even though toxic species were ingested, it has been shown that mysids actively choose other food if available (Demott 1995; Engström et al. 2001; Gorokhova and Lehtiniemi 2007). It has further been demonstrated that mysids consistently feed less on copepods when cyanobacteria are present (Engström et al. 2001). The reason for this is however unclear. Decreased feeding on high quality food could be caused either by clogged feeding appendages or a generally decreased feeding rate to reduce the intake of toxins. Nevertheless, it has been suggested that mysids, just like several cladocerans (Fulton 1988; Hanazato and Yasuno 1987; Starkweather and Kellar 1983) are tolerant to the ingested toxins produced by cyanobacteria (Engström et al. 2001) and that these phytoplankters, may be a valuable source of nitrogen during late summer; either directly as food (Gorokhova 2009) or possibly also indirecly as fuel for primary producers.

4.2.1 Mysis relicta/Mysis salemaai

Even though more studies on mysid diets have focused on M. diluviana in lakes (Boscarino et al. 2006; Boscarino et al. 2007; Bowers and Vanderploeg 1982; Johannsson et al. 2001; Johannsson et al. 1994; Lasenby and Shi 2004), some diet studies have also been conducted for its sibling species (M. relicta sp.) in the Baltic Sea. Viherluoto et al. (2000) compared the diets of M. mixta and M. relicta from the Northern Baltic proper. Their diets overlapped to a high degree (75%, Schoener's index), but M. relicta fed significantly more on benthic particles and phytoplankton than M. mixta that relied more on planktonic crustaceans. This effect could however be partly explained by interspecific size differences as M. mixta grew faster and reached a larger size than M. relicta. This in turn could be explained by copepods and cladocerans being better quality food than benthic and plant material.

4.2.2 Mysis mixta

Mysis mixta is the most studied mysid in the Baltic Sea with several reports on its feeding and diet. Salemaa et al. (1986); Rudstam and Hansson (1990); Hansson et al. (1990); Viherluoto et al. (2000) and Lehtiniemi et al. (2002) studied gut contents in wild-caught mysids. More recent papers have mainly reported results of experimental studies (Viherluoto and Viitasalo 2001a; Viherluoto and Viitasalo 2001b; Viitasalo 2007; Viitasalo and Viitasalo 2004).

Salemaa et al. (1986), Rudstam and Hansson (1990) and Hansson et al. (1990) found cladocerans (Bosmina spp. and Pleopsis spp.) and copepods (Eurytemora spp. Temora spp. Acartia spp. and Pseudocalanus spp.) to be the predominant food source (90-100% by weight) in adult M. mixta. Smaller amounts of detritus, phytoplankton and benthic copepods were however also present. A more recent experimental study also indicated a strong preference for the copepod Eurytemora affinis and cladocerans (however, to lower extent). The other abundant copepod, Acartia spp. was not readily ingested (Viherluoto et al. 2000) in contrast to the earlier findings (Hansson et al. 1990; Rudstam and Hansson 1990; Salemaa et al. 1986). The authors explain this by the fact that Acartia is a fast swimmer (Viitasalo and Rautio 1998) and thus a hard prey to capture. Even though the same is valid for Eurytemora (Viitasalo et al. 1998), there are indications that Eurytemora produces stronger hydro- mechanical signals which are more easily detected by non-visual predators like mysids. (Viherluoto pers. observation, but see also: Gorokhova et al. 2005; Gorokhova and Lehtiniemi 2007). Under experimental conditions however, Mohammadian et al. (1997) found clearly higher capture rates for Acartia than for Eurytemora.

Viherluoto and Viitasalo (2001b) further stated that prey preference was related to mysid size and prey species composition. Small mysids preferred rotifers to a high extent since they are small prey and easy to capture. As mysids grew larger, the diet composition varied more. Viherluoto and Viitasalo (2001b) suggested that larger mysids are less selective simply because their size does not limit them from capturing evasive and large prey. The switch to larger prey occurred after a threshold length of 8-11 mm.

4.2.3 Neomysis integer/Praunus flexuosus

Both Neomysis integer and Praunus flexuosus differ from Mysis spp. in habitat choice, occurring mainly in the littoral where N. integer often forms swarms in more open areas 10 whereas P. flexuosus is more closely associated with the phytobenthos. Recent studies however, show that N. integer also can be abundant in the pelagic environment (Kotta and Kotta 2001; paper II in this thesis). The diet preferences are similar to that of Mysis spp. Both species are omnivores and consume everything from detrital matter to algae and zooplankton (Bremer and Vijverberg 1982; Fockedey and Mees 1999; Lehtiniemi and Nordström 2008). Food utilization has been coupled to the availability of different food objects, e.g. phytoplankton spring bloom and zooplankton peak abundances in late summer (Lehtiniemi and Nordström 2008). Food preference is furthermore size regulated to some extent. Interestingly, small and extremely large Neomysis integer consume significantly less phytoplankton than intermediate sized animals (Lehtiniemi and Nordström 2008). It is thus attractive to hypothesize whether these diet differences are a response to predation pressure, bioenergetical needs, a result of an overlap in size distribution or a combination of these factors. Hakala et al. (1993) and Lehtiniemi and Nordström (2008) found juvenile Neomysis consuming a higher proportion of rotifers as opposed to adult animals which consumed mainly cladocerans and copepods by weight. However detrital and algal particles dominated by numbers. Similar diet preferences could be demonstrated for the pelagic M. mixta (Viherluoto et al. 2000).

4.3 Life history and growth

Many features of an organism’s biology are genetically constrained, e.g. the potential for growth, egg carrying capacity etc. Indeed, growth rates and generation times vary substantially among the dominating Baltic species. Neomysis has an asynchronous breeding season with more than one cohort annually (Mauchline 1980); whereas the pelagic M. mixta usually produces one brood per year but may supposedly reproduce a second time, one year later producing two cohorts. (Salemaa et al. 1986; Shvetsova and Shvetsov 1990). The iteroparous lifestyle described by these authors is however debated. Viherluoto et al. (2000) studied an M. mixta population throughout the growing season, from June to October. They found two distinct cohorts forming during late summer and then merging into one cohort again in late autumn. This finding could thus not be explained by a portion of the population having different generation times but rather by intra cohort differences in growth rates. Additionally, Simm and Kotta (1992) and Rudstam and Hansson (1990) found no evidence for a two year life cycle in M. mixta. Simm and Kotta (1992) explain the observations of very large, gravid females in autumn by Salemaa et al. (1986) and Shvetsova and Shvetsov (1990) by erroneous comparisons of specimens from geographically distinct areas with differing potentials for growth rather than prolonged life cycle and the authors’ understanding is that M. mixta have a one year life cycle in the Baltic and that it rarely lives longer than 16-17 months. However, aberrantly large gravid females (22-23 mm) have been found together with much smaller individuals (12-14 mm) at several localities in Stockholm archipelago during July- October, (Ogonowski, M. and Gorokhova, E. G. pers. obs.). These findings contradict the conclusions of Simm and Kotta and are not plausibly supported by the idea of different growth rates (Viherluoto et al. 2000) due to the great difference in size. Thus, there are two explanations to these findings: (i) some M. mixta grow past the first spawning season without reproducing to spawn the following winter or, (ii) they survive the act of reproduction and spawn a second time. It is thus still debatable whether M. mixta has a strict one-year life cycle in the Baltic Sea or not.

The M. relicta species-complex on the other hand is known to have a varying life cycle. Populations with differing generation times have been identified in the Baltic and vary with a

12, 18 or 24 month life cycle (Hakala 1979; Välipakka 1990). It has been proposed that this variation may be due to variable food quality and primary production in different areas, where availability of good quality food is positively correlated with shorter generation times. The oligotrophic Lake Tahoe in California, for example, harbors an introduced population of M. diluviana, which has a generation time of at least four years, whereas an isolated much more productive bay of the same lake holds mysids with a one year life cycle (Morgan 1980). Life history differences of the sub-populations do not seem to be effects of evolutionary adaptation but rather plasticity since both groups in Lake Tahoe stem from the same ancestral population. Moreover, mysids preferred the same temperature strata in both areas indicating that temperature was of little importance for the reported differences in generation times. In the Baltic, similar patterns have been observed. In the Bothnian bay, M. relicta and M. salemaai are sympatric and both are winter-breeders, with a two year life cycle. Southwards however, where productivity is substantially higher (Samuelsson et al. 2006), one year life cycles predominate and M. salemaai breeding occurs throughout the year in the Gulf of Finland (Väinolä and Vainio 1998; Välipakka 1990; see also: Hessle and Vallin 1934; Shvetsova and Davidyuk 1987; Teraguchi 1969) but probably not in the northern Baltic proper (pers. obs, paper II and III in this thesis).

Shvetsova et al. (1992) followed the population dynamics of two generations of M. mixta during a year in the Gulf of Riga. Their calculations indicate that the mysid mortality rate was at its highest during September-December, coinciding with a diet shift in herring (Aneer 1975; Rudstam et al. 1992) This further indicates that as mysids compete with herring for zooplankton during the summer months, they also become the prey for older herring in the autumn and predation pressure on the shared resource progressively decreases when predation on mysids increases (Rudstam et al. 1992).

4.4 Migration patterns

Nocturnal diel vertical migration (DVM) is a well-known phenomenon performed by many invertebrates in both freshwater and marine ecosystems. It is a widespread behavior and is manifested by feeding in the surface waters (epilimnion) at night and then inhabiting deeper and darker waters (hypolimnion) in daytime. This behavior reduces the risk of being eaten by visual predators like fish (Lampert 1989; Lampert 1993).

However, not all pelagic mysids migrate. Rudstam (1989) (Mysis mixta), Bowers (1988) and Morgan, (1980) (Mysis relicta) all found mysids residing on or close above the bottom during night. Until recently, it has been unknown whether these mysids ever migrate or not. Ogonowski et al. (Paper III), found that Mysis salemaai caught on the bottom at night had a significantly different isotope signature in muscle tissue from pelagic mysids collected at the same date and site (coastal northern Baltic Proper). These findings indicate that the food ingested by these two groups of mysids differs and that pelagic mysids may have a higher proportion of zooplankton in their diet, indicated by a higher 15N:14N ratio.

The vertical migration of mysids (M. relicta, in particular) has been studied extensively (Ackefors 1969; Beeton 1960; Boscarino et al. 2006; Boscarino et al. 2007; Debus et al. 1992; Lasenby and Langford 1972; Teraguchi 1969) because of their important role, both as food for many fish species and also because of their potentially high predation on other zooplankton species (Mauchline 1980). Mysid DVM has mainly been studied in pelagic systems but is evident in littoral species as well, even though the extent of vertical migration

12 in this habitat may be just in the range of 3-25 m (Kotta and Kotta 2001), while it can be >100 m in pelagic species. In pelagic systems, downward migration is believed to provide a darkness refuge that helps them avoid fish predation. In littoral systems, this explanation does not seem to be adequate, since light extinction does not change to the same magnitude as in the pelagic. Littoral downward migration during daytime could be coupled to a refuge in form of dense macrophyte coverage and/or association to benthic substrate.

Littoral mysids, such as Neomysis integer, also perform horizontal migrations. Intense schooling (up to 50 000 ind.·m-2) in the littoral during day (Rasmussen 1973) and dispersed individuals in offshore areas during night have been observed (Debus et al. 1992). One to two hours prior to sunrise, these mysids seemed to return to the littoral. At such high mysid densities, it is possible that food resources become locally depleted in the littoral, thereby forcing mysids to expand their feeding grounds to the pelagic environment during night when predation pressure relaxes. Horizontal migrations were also observed in another littoral mysid, Paramysis lacustris, and the pelagic Mysis relicta. These migrations were however not performed on a diurnal basis, but rather on a seasonal. Paramysis and juvenile Mysis relicta migrated into coastal areas during autumn when decaying plant material was abundant providing a food source (Beeton and Bowers 1982; Lesutiene et al. 2008; Morgan and Threlkeld 1982). In the case of juvenile Mysis relicta, migration to shallower waters could in addition be an escape reaction from predation by adult mysids that prefer deeper waters (Morgan and Threlkeld 1982; Quirt and Lasenby 2002). However, such active horizontal translocations are, to my knowledge, not known to occur in the Baltic Sea for neither M. relicta nor M. mixta. This could, in contrast to Morgan and Threlkelds’ situation be explained by the presence of other, adult littoral mysid species posing a threat to juveniles.

4.4.1 Effects of Light

The questions concerning the mechanisms behind DVM, and the variables that govern it, have been investigated by several authors. Lasenby and Fürst (1981) studied mysids in situ with a high frequency echosounder. They observed mysids to avoid migration into the densest zooplankton layer during full moon and speculated that mysid feeding may be inhibited by light (see also: Debus et al. 1992). Several authors suggested light intensity to be the principal variable governing DVM in pelagic mysids (Boscarino et al. 2009; Bremer and Vijverberg 1982; Rudstam et al. 1989; Salemaa et al. 1986). Rudstam and Hansson (1990) observed M. mixta to avoid light levels above 10-4 lux, whereas for M. diluviana, these levels were variable from 10-6 lux (Boscarino et al. 2009) to 0.02–0.05 lux (Teraguchi et al. 1975). In the Baltic proper, the light preferences for M. relicta remain unknown, but recent observations indicate that M. relicta in pelagic water increased with depth and dominated at depths exceeding 150 m (pers. obs.) thus indicating that M. relicta could be more light sensitive than M. mixta; dissimilarities in light tolerance may however be attributable to the different subspecies of M. relicta (Audzijonyte et al. 2005; Pahlberg et al. 2005). Similar observations have also been reported by Ojaveer et al. (1999). Consequently, these observations suggest that M. relicta in the Baltic Sea may have a lower tolerance to light than M. mixta; alternatively the partial, vertical separation is a response to lower food availability potentially driven by competition.

Wiebe et al. (1996) investigated the effect of light on M. diluviana DVM and realized that standard light measuring equipment could be inadequate due to the fact that “lux” is a scale measure related to the visual spectrum of the human eye. M. relicta eye sensitivity has different spectral optima, ranging from 505-570 nm (Dontsov et al. 1999; Jokela-Maeaettae et

13 al. 2005; Lindström and Nilsson 1988). Dontsov et al. (1999) further demonstrated similar peak sensitivities for M. salemaai and M. mixta. Lindström et al. (2000), Dontsov et al. (1999) and Wiebe et al. (1996), concluded that peak sensitivity may vary among populations of a single species due to adaptations to specific optical environments. Moreover, Beeton (1959) and Jokela-Maeaettae et al. (2005) observed that juveniles are much less sensitive to light, which might explain their vertical separation from adults during day time. This feature could be an adaptation to (1) avoid cannibalism, (2) stay higher in the water column and feed on small sized phytoplankton, (3) encounter higher temperature that promotes growth; a combination of these factors is also likely.

4.4.2 Vertical size distribution

Predation risk by visual predators like herring reasonably increases with light intensity. It would be expected, however, that small, less conspicuous mysids are more difficult for fish to detect and that they may migrate higher up in the water column in search for high quality food and at the same time escape predation from conspecifics (Brooks and Dodson 1965; Rajasilta and Vuorinen 1983). Rudstam et al. (1989) found small, juvenile Baltic M. mixta higher up in the water column than large individuals. Similar observations have been made by Hessle and Vallin (1934); Salemaa et al. (1986); Kotta and Kotta (1999) (M.mixta); Grossnickle and Morgan (1979); Teraguchi (1969) and Bowers (1988) (M. relicta). The mechanisms behind this behavior are however not clear. If the behavior is a result of predation avoidance from visual predators, then a vertical separation between sexes should also be prominent, since egg/embryo carrying females are far more conspicuous than males. However, no such differences have been found (Teraguchi 1969).

Although observations regarding the more extensive DVM of juvenile mysids, indicating vertical size differences are well described in the literature, few attempts have been made to study vertical size distribution explicitly. We need to know under which circumstances and how different sizes of mysids disperse in order to accurately be able to incorporate them into bioenergetical models and energy budgets. Consequently, a detailed knowledge of vertical migration and size distribution is of importance for understanding the energy flows between trophic levels in pelagic ecosystems and benthic-pelagic coupling.

4.4.3 Temperature

Although light intensity has been proven an important factor restricting mysid migration to top surface layers, limits in terms of temperature also seem to be present and some authors have considered temperature to be the primary underlying factor governing the extent of DVM in mysids (Lampert 1989; Maurer and Wigley 1982). In a study by Salemaa et al. (1986), most M. mixta were caught below the thermocline and rarely passed into warmer water than 10°C. Other studies though, have found mysids well above the thermocline (Grabe and Hatch 1982; Kotta and Kotta 1999; McLaren 1963; Teraguchi 1969). Rudstam et al. (1989) noted that mysids that migrated and passed the thermocline primarily were small juveniles. An absence of juveniles in the collections of Salemaa et al. (1986) could explain why they suggested that mysids do not pass the 10°C boundary. Strong temperature gradients have been proposed to limit the DVM in mysids. Beeton (1960) found mysids avoiding passage through temperature gradients of 2°C · m-1. When the thermocline was weak or disrupted, mysids were distributed throughout the water column. However, in a more recent

14 study by Boscarino et al. (2007), M. diluviana from Lake Ontario showed strong preference for 6–8°C and did not seem to be affected by temperature gradients although absolute temperatures limited mysid vertical migration. Consequently, the effects of temperature on mysid behavior manifest some degree of variation and the ways it affects mysid migrations are not clear.

4.4.4 Chemical cues

While DVM in zooplankton has received much attention in the past, (e.g. Hays 2003; Hutchinson 1967; Lampert 1989) focus has been on the behavior of the average population on exogenous stimuli. Since predation by visual predators most probably occurs at the boundaries of a DVM-prey’s distribution (Boscarino et al. 2007), other means have to be employed in order for these effects to be studied.

The presence of chemical substances from fish (kairomones) has shown to further increase the migration of zooplankton and mysids away from fish (Boscarino et al. 2007; Cohen and Ritz 2003; Dodson 1988; Loose and Dawidowicz 1994; Loose et al. 1993). In the absence of such chemical cues, zooplankton, usually stay in the epilimnion/metalimnion continuously. Chemical cues from fish have also shown to affect mysids on another level. Hamrén and Hansson (1999) and Lehtiniemi and Lindén (2006) observed that M. mixta and M. relicta changed their feeding rates when exposed to fish scented water. Mysids ate less and were less selective to prey items in order to decrease their conspicuousness to predators. However, a similar study on littoral mysids Neomysis integer and Praunus flexuosus (Lindén et al. 2003) did not yield lower feeding rates. Instead, more time was attributed to hiding in the provided macrophyte refuge in the presence of fish kairomones. These differences could be explained by the very different environments that littoral and pelagic mysids live in. As pelagic mysids do not have any structural refuge in open water, decreased feeding and thus swimming may be ways of decreasing conspicuousness (see Gerritsen 1984; Savino and Stein 1989). Littoral mysids on the other hand are closely associated with the macrophyte coverage and use a different strategy to avoid predators (Lindén et al. 2003).

Mysids may also display behavioral responses to cannibalism by conspecifics (Clutter 1969) which manifests itself in terms of ontogenetic niche separation. Juvenile and subadult mysids usually migrate higher up in the water column during night (Grossnickle and Morgan 1979; Rudstam et al. 1989) and besides possible effects of light and temperature (see above) this may be attributable to chemical cues from adult mysids (Quirt and Lasenby 2002).

4.4.5 Niche differentiation and partial migration

Even though diel vertical migration commonly is accepted as being a prominent part of zooplankton and mysid behavior, it is generally treated as a population level trait, i.e. individual variation is disregarded. However, several authors have reported a bimodal nighttime vertical distribution in mysid populations (North American lakes: Morgan (1980), Bowers (1988); the Baltic Sea: Rudstam et al. (1989)), with part of the population close to the bottom even at night, suggesting that some individuals may be sedentary. Morgan (1980) assumed this group to consist mostly of recently moulted gravid females, although this was later rejected by Bowers (1988) who observed that the demographic structure of the benthic part of the population generally was representative of the entire population. These

15 observations thus raise some interesting questions regarding the nature of this behavior. Are mysids polymorphic in respect to habitat choice and resource use or can there be other factors explaining these observations?

A division into pelagic and benthic forms is actually not uncommon in nature, especially among fishes (Robinson and Wilson 1994; Skúlason and Smith 1995) and the cause for such segregation has been proposed to be a release from competition promoted by the discrete nature of benthic and pelagic habitats. Although niche differentiation of this form often is related to intraspecific morphological differences, it is sometimes only expressed as an intraspecific behavioral difference without any noticeable morphological or genetic discrepancies (behavioral plasticity) (Bolnick et al. 2003). As niche partitioning often is discussed in the context of persistent traits where species, early in life diverge into different forms to specialize in specific habitats, temporary competitive release may be achieved by a part of the population migrating to other habitats on a seasonal basis.

This phenomenon is termed partial migration. Stemming from the avian literature (Lundberg 1988), it has been described in a wide array of taxa and can often be coupled to intrinsic conditional states (e.g. sex, age or ontogeny) or extrinsic plastic traits such as physical condition and dominance (Lundberg 1988). In the case of DVM-performing animals that have regular and frequent migrations, very little is known in terms of persistent life history strategies, even though bimodal vertical distributions regularly are observed in both fish and zooplankton (see Pearre 2003 for review). In fact, Mehner and Kasprzak (2011) where the first to propose that the absence of DVM in fish could be a manifestation of partial migration (sensu Lundberg (1988)). Although some fish were found to be “resident”, the duration of residency was not established and thus neither the potential magnitude of trophic interactions. The problem of tracking individuals makes it difficult to say whether the “resident” part of the population is resident over some considerable time period or if individuals change strategy on e.g. a nightly, daily or weekly basis (asynchronous migration).

The third paper in this thesis addresses this problem by using stable isotope and genetic markers to elucidate the persistence of “residency” in Mysis salemaai, providing the first line of evidence for persistent partial migration in mysids.

4.6 Bioenergetics

Knowing how much animals eat is important for our understanding of trophic dynamics. Estimating consumption is however not trivial, especially for small omnivores like mysids that depend on a wide variety of small prey, making it difficult to estimate consuption directly. Thus, indirect methods are usually applied.

Bioenergetic models are a way of estimating consumption by using a fairly straight forward energy budget approach, using knowledge of basic physiological demands, growth and temperature preferences. Generally, an energy budget can be stated in the following terms:

Energy consumed = Respiration + Waste + Growth

Although bioenergetic models have been used successfully among a variety of taxa, relatively little has been presented for mysids. Rudstam (1989) estimated the consumption of Mysis mixta with a bioenergetic model using physiological parameters mainly derived from

16 measurements on Mysis diluviana. Validations of this model produced realistic results for both species (M. diluviana: Chipps and Bennett (2002), M. mixta: Gorokhova (1998)) although some improvements to the model were made by Gorokhova (1998). It is not surprising that one model performed well for both of these species as both M. mixta and M. diluviana have similar temperature preferences, behavior and life-history-traits. Regarding littoral mysids in the northern Baltic Proper, bioenergetic approaches have only been published for Neomysis integer (Maciejewska and Opalinski 2002) and it is questionable whether a Neomysis-model could be applied to P. flexuosus since these species have different lifestyles. N. integer aggregates in swarms which decreases respiration (Ritz et al. 2001) and probably has a lower temperature tolerance than P. flexuosus; N. integer often migrate into the pelagic during summer when temperatures become too high (Debus et al. 1992) whereas such migrations have not been reported for P. flexuosus.

Since temperature has such a strong effect on biochemical and metabolic processes (Gillooly et al. 2001; Winberg 1956) and respiration accounts for approximately 50% of an animals total energy expenditure, it is crucial from a bioenergetics perspective, to know the relationship between temperature and respiration.

Another important aspect in this context is the basal respratory rate (routine metabolic rate, RMR), i.e. the level of respiration that is used to sustain basic metabolic processes. Although such parameters are available in the litterature, there is a need for caution, since this rate will be influenced by an energy expenditure related to the processing of food (specific dynamic action, SDA), possibly introducing bias to the bioenergetic model. Because SDA is dependent on how much and which food has been consumed, and we seldom know the feeding history of animals collected in the wild, we need to know the duration of SDA or the magnitude of SDA itself. The duration of SDA as well as SDA-values for mysids are at this point unavailable.

Rudstam et al. (1989) assumed a value of 18% of assimilated food which is in the range of SDA-values reported for other zooplankton. Chipps and Bennet (2002) later performed a sensitivity analysis showing that parameters most sensitive to Rudtsam’s bioenergetic output were related to respiration, i.e. SDA, routine metabolic rate or a combination of both. Assuming that RMR paramters were correct in the model, SDA could have been erroneously estimated by 50-70%. Regarding the duration of SDA, it has been assumed that this effect would be exhausted after just a few hours post-feeding (Kiørboe et al. 1985). Paper IV in this thesis however, shows that this is not the case and that postfeeding effects may be much more extended (>30 hours) than previously expected. Ultimately this means that there may be some bias associated with currently available respiration parameters.

4.7 Abundance

Due to patchy distributions and diel vertical migrations, quantification of mysids is in general difficult, expensive and time consuming and no standardized methods have been developed. Few such attempts have however been made in the Baltic Sea where most of the studies have been conducted in the Gulf of Riga (Kotta and Kotta 1999; Kotta 1984), Gulf of Finland- Bothnian Sea (Salemaa et al. 1986; Salemaa et al. 1990; Simm and Kotta 1992) and inner and outer areas of the Stockholm archipelago (Rudstam and Hansson 1990; Rudstam et al. 1986). To date, there have only been two large scale attempts to assess mysid abundances in the Baltic Sea. Shvetsova et al. (1992) conducted a survey covering the eastern parts of the Baltic proper southwards to the Polish coast. Salemaa et al. (1990) concentrated most of their efforts

17 to the Gulf of Finland and the Bothnian Sea. Although the survey of Shvetsova et al. (1992) provides good spatial and temporal resolution, there is one fundamental problem; abundances were estimated over varying depths, from 20-100 m. thus expressing abundances in volumetric units. Mysids perform diel vertical migrations and are rarely evenly distributed in the water column. It is therefore much more rational to express densities on an areal rather than a volumetric scale. Further problems arise when results from different studies are compared. Since there are no standardized methods for mysids sampling, nearly all reported mysid abundances are based on different gears, and sampling efficiencies of these are generally lacking.

4.7.1 Sampling methods

Mysids are agile and quick animals and sustained swimming speeds up to 10 body lengths·s-1 are common, with bursts of up to 20 body lengths·s-1 reported for several species (Mauchline 1980). Indeed, mysids have been shown to actively avoid sampling gears through means of intra-school communication (Clutter and Anraku 1968; Lasenby and Sherman 1991) especially at daylight (Fleminger and Clutter 1965). The reasons for lower sampling efficiency at daylight are not clear. One possibility is the gear avoidance described above and another is the pronounced patchy and concentrated distribution under bright conditions. Data on sampling efficiency of different gears is in most cases unavailable when it comes to mysids and the need for several types of gears due to ontogenetic habitat separation and possible schooling, further complicates abundance measurements. Eleftheriou and Holme (1984) and Carleton and Hamner (1987) for instance, suggested sampling efficiencies of 1-10% in epibenthic sleds. This is problematic and indicates that traditional sampling for mysids infers gross underestimations of abundances. Large mesh nets, with high filtering efficiency, usually miss small mysids, whereas use of smaller mesh sizes result in lower efficiency, low towing speeds and thus higher avoidance (Jumars 2007). Consequently, both large and small mesh sizes will tend to underestimate mysid abundances. Either by omitting juveniles in large meshes or by higher avoidance of large individuals in small mesh sizes. Smaller mesh sizes will additionally bias the catch towards smaller individuals.

4.7.2 Hydroacoustics

Hydroacoustics is an alternative strategy for abundance estimation and is a non-invasive method, which omits the problem of avoidance and is vastly more efficient when it comes to spatial coverage.

Since the development of the sonar, hydroacoustics has been used extensively in ecological studies. The ability to study marine organisms in situ and possibility to cover large volumes of water has come to be the most important feature of this technique. Although extensively used in fisheries biology (Simmonds and MacLennan 2005), hydroacoustics has also been found effective in studies of much smaller organisms, such as plankton and pelagic invertebrates (Boswell and Wilson 2004; Gal et al. 2004; Gonzalez Chavez and Arenas Fuentes 2003; Holbrook et al. 2006; Johnson et al. 2004).

Despite of its many advantages, species determination still has to rely on complementary trawls or net catches and information about the studied organism’s distribution patterns and biology is needed for a correct interpretation of the echograms. The advances made with multi

18 frequency techniques, however, allow to coarsely distinguish between organisms with different acoustical properties, resulting in minimized physical sampling (Korneliussen and Ona 2003).

The backscattering properties, i.e. the acoustic signature of the received echo of aquatic organisms may vary considerably. The amount of backscattered energy depends on the difference in density between water and the target. Although all tissues and bones in fish reflect sound, the by far most significant source of reflection is the swim bladder. About 90- 95% of the backscattering can be attributed to the gas-filled swim bladder (Foote 1980). Since mysids lack this organ, their echo strength is much lower than that of fish making them more difficult to detect. Additionally, the target strength (TS) of most organisms is affected by its tilt angle. Boscarino et al. (2007) observed that mysids instantaneously disappear from an echogram whenever an artificial light source is pointed at the water surface during night. They concluded that this phenomenon was due to a change in tilt angle in response to light avoidance, i.e. mysids turned their heads down in order to avoid the light which drastically decreased TS.

Due to their small size and often high densities, TS estimation of single individual mysids becomes practically impossible. Echo integration however is a way to obtain estimates of biomass and is often referred to as the Mean Volume Backscattering Strength (MVBS or Sv). Even though single echo detections (SED) and TS are difficult to obtain from mysids, it is possible to back-calculate a mean TS-value to length relationship. This relationship, combined with data on the mysid’s actual size distribution, can sequentially be used to derive abundance estimates from recorded Sv values (Gal et al. 1999).

The acoustic backscatter from zooplankton, including mysids and krill has shown to be more intense when using higher frequency echosounders, while the opposite relationship is valid for fish (Brierley et al. 2004; Gorska et al. 2005; Jech 2006; Knudsen et al. 2006; Korneliussen et al. 2008; Korneliussen and Ona 2003). Based on this knowledge, signals from fish, which are the strongest scatterers, can be filtered out from acoustic data by combining the information from several, simultaneously run frequencies (Knudsen et al. 2006). Quantification of M. relicta by multifrequency acoustics has been evaluated by Gal et al. (1999) and seems to give reasonably good results. They calculated the average TS for M. relicta in Lake Ontario based on in situ data for different frequencies and concluded that their results did not differ greatly from theoretical models (e.g. Foote 1990; Stanton et al. 1993). Their experiments were however conducted in a fairly simple ecosystem from an acoustic point of view, a system with few acoustically similar organisms.

Since mysids are not easily distinguished from other similarly-sized invertebrates, this means that good knowledge of the organisms constituting the ecosystem of interest is fundamental for the data interpretation. By knowing the acoustic properties of different organisms and how environmental factors affect migration patterns and behavior, errors in acoustic interpretation may be minimized.

5. Summary of papers

Paper I

Multifrequency discrimination of fish and mysids

We investigated the possibility of estimating mysid abundances and biomass by the use of multifrequency hydroacoustics. Fish compared to other objects, displayed different frequency responses and could therefore be removed by masking (Korneliussen et al. 2008; Korneliussen and Ona 2003). We found a strong, positive relationship between mysid biomass and filtered echo-data. However, daytime data showed considerable acoustic backscatter in the epilimnion, resulting not from mysids but from a dense layer of the fresh water cladoceran Leptodora kindtii. This illustrates that for accurate estimates with this technique, good knowledge is needed on distributions in relation to biotic and abiotic factors, both for mysids and other large zooplankton.

Paper II

Status and vertical size distributions of a pelagic mysid community in the northern Baltic proper

In the second paper, we compared historical, mysid abundance data from the 1980s (Rudstam et al. 1986) from a coastal area of the northern Baltic proper with recent data from 2008. The trophic position of three common mysids (Mysis mixta, Mysis relicta and Neomysis integer) was investigated by stable isotope analysis of N and C in muscle tissue. We also examined the vertical size distribution of these species in relation to light and temperature using linear mixed models (LME). Our data indicate a significant decrease in M. mixta abundance compared to historical data which also translates to significantly lower total mysid biomass in the area. No clear differences in abundance of M. relicta or N. integer were noticeable although their proportions relative M. mixta have increased significantly. Stable isotope analysis indicated that Neomysis integer feeds on a lower trophic level than Mysis spp. and that the diet consists mainly of phytoplankton, but the difference could be related to a smaller average size of Neomysis, and not species specific diet differences. However, the fact that juvenile Neomysis now are abundant in pelagic surface waters should make them attractive food items for larger clupeids and possibly also lead to a decreased predation pressure on Mysis spp. M. relicta displayed slightly higher 15N enrichment than M. mixta. This could be an effect of a more pronounced DVM by M. mixta and by that, possibly a higher intake of 15N depleted material associated with cyanobacterial occurrence (Gorokhova 2009), thus leading to a relatively lower nitrogen signal. The vertical size distribution of mysids displayed a significant size increase with depth and in situ light for N. integer but not for Mysis spp. The vertical size increase in Neomysis correlated negatively with temperature to some extent but the smallest juveniles were always caught higher in the water column than larger specimens even during isothermal conditions, indicating that the vertical size distribution probably is a response to predation more than size related temperature preferences. The lack of vertical size differences in Mysis spp. was probably caused by very low variation in size, restricted vertical distribution and fewer observations compared to Neomysis integer. Moreover, Mysis spp. were almost exclusively found below the light threshold needed for visual feeding by herring (10-4 lux) thus making any anti-predatory behavior coupled to vision such as reduction of conspicuousness obsolete.

Paper III

Persistent lack of diel vertical migration in a pelagic mysid population –– a case of partial migration

The possibility of a persistent partial diel vertical migration in Mysis salemaai was evaluated by a combination of ecological (stable isotopes as a proxy for diet, C:N ratio as a proxy for lipid accumulation and protein:DNA ratio as a proxy for growth) and genetic markers (mitochondrial DNA, cytochrome oxidase I gene).

Stable isotope analysis indicated that there were significant differences between benthic and pelagic mysids with pelagic individuals being slightly more carnivorous. This was evident both over a longer (muscle tissue) and shorter (chitin) temporal resolution indicating that differences in diets should persisted at least during the growth period (spring—summer). Genetic analysis revealed a fine-scale genetic structure between the two stations and between the benthic samples indicating that bottom-dwelling mysids were less mobile than pelagic ones. We did however not find any differences in C:N or protein:DNA ratio between groups which indicates that despite differences in diet and behavior, either strategy seems to convey equal fitness benefits in terms of growth and lipid stores which is in line with current understandings of partial migration theory.

In conclusion, our results indicate that partial diel vertical migration is a phenotypically plastic trait and since mysids in the Baltic Sea have been shown to be food limited large parts of the year (Mohammadian et al. 1997) it is plausible that the “choice” for a resident strategy is induced by intraspecific competition for pelagic zooplankton.

Paper IV

A weight and temperature dependent model of respiration in Praunus flexuosus (Crustacea, Mysidacea)

Respiration is a major component of an animal’s energy expenditure and precise measurements of this parameter are important in modelling contexts, which is why we measured and monitored oxygen consumption of previously fed mysids (Praunus flexuosus) over a period of > 30 hours. Moreover as temperature and size have been shown to influence respiration significantly we wanted to establish a temperature and weight-dependent model of respiration which could be used in a more complex modelling framework.

We found that post-feeding digestive processes had a significant and positive influence on metabolic rate (specific dynamic action, SDA) and that this effect was detectable over a long period of time (over the entire course of the experimental period and much longer after food had been evacuated from the guts). This indicates that basal metabolic rates may be overestimated without a proper pre-examination of SDA-effects. The temperature and weight- dependent model explained a high degree of variation (r2 = 0.87) and is to our knowledge the first one presented for this species.

6. Conclusions

The recent decreased condition of herring and sprat and also local recruitment problems of littoral fish such as perch (Perca fluviatilis L.) and pike (Esox lucius L.) have raised questions concerning food-limitation and lack of top-down regulation by large predatory fish such as cod (Nilsson et al. 2004). Despite of the fact that mysids are known to be very effective zooplanktivores (Hansson et al. 1990), they are rarely mentioned in such contexts. The results of paper I show that echosounding for mysids could be a successful way of gathering abundance and biomass estimations by covering large volumes of water, thereby reducing bias caused by patchy distributions. However, there is a case for caution since dense aggregations of large zooplankton may be falsely interpreted as mysids. It is therefore important to understand the mechanisms governing the distribution of organisms in order to make accurate interpretations of echo data. Moreover, because this technique involves exclusion of fish echoes on a two dimensional plane, it also means that high densities of fish may mask echoes from mysids. This was evident during a pilot study in a coastal area of the northern Baltic proper in 2008 (author’s unpublished) where a dense layer of fish was present from the surface down to below the thermocline where most mysids were concentrated, thus making quantification difficult. The technique could however work more successfully in deeper areas where mysids would be separated from most of the fish for longer periods of time due to lower spatial overlap. Investigating the deeper areas of the Baltic would also be advantageous for two reasons:

i.) Depths >30 meters are more representative of the Baltic as a whole than coastal areas. ii.) Pelagic mysids usually occur at depths > 30 meters.

This means that by studying the true pelagic, we would gain valuable information on the bulk of pelagic mysid abundance in a representative environment. Additionally, the hydroacoustic recordings would provide information on the behavior and relation of mysids to areas of deep water hypoxia/anoxia, which have become an area of great concern in recent years.

The current abundances of Mysis mixta presented in paper II, are clearly lower compared to historical data from the 1980’s. It is however impossible to tell whether current abundances are at a ‘normal’ state or not since there are considerable gaps between surveys. What can be said however, is that M. mixta was the dominant pelagic mysid in 1993-1996 (collections for experiments; Gorokhova and Hansson 2000; Hamrén and Hansson 1999; Mohammadian et al. 1997), clearly after a supposed Baltic Sea regime shift (Alheit et al. 2005) in the end of the 1980’s. In our study, M. mixta was no longer the dominant pelagic mysid and the reason for this decrease in is not known but the general decline is supported by indirect observations even in the southern Baltic (Dziaduch 2011) indicating that the decrease probably is not a local phenomenon. Conversely abundances of Neomysis now show tendencies of increase even though they sporadically were high during autumns in 1983-1985 (Rudstam et al. 1986). As the bulk of individuals were small juveniles feeding on phytoplankton we would expect a low degree of niche overlap between Neomysis and Mysis spp. This combined with high abundances of Neomysis in the surface layers would further decrease predation pressure on Mysis spp. in favor for predation on Neomysis. Altogether, this makes it even more difficult to understand the decrease of Mysis mixta.

Advances in understanding the mechanisms behind the vertical migration of mysids have also been made recently (Boscarino et al. 2006; Boscarino et al. 2007; Gal et al. 2004). However,

22 the aspect of size as well as size specific interactions of mysids and fish have generally been underappreciated in vertical migration models. This implies, that models like those described by Boscarino et al. (2007) would produce false predictions of mysid DVM if temperature and light preferences would be linked to size; which also was acknowledged by Boscarino (2009). An optimization of current mysid DVM models by including aspects of vertical size distribution would provide means to create more precise bioenergetics models, both for fish and mysids, and thus aid in the construction of more accurate, large-scale food-web models. Our efforts to disentangle the relative importance of light and temperature as cues driving the vertical size distribution (Paper II) revealed that in situ light is more important than temperature as mysid size increased linearly with light levels throughout the sampled temperature gradient. Even though the smallest individuals potentially aggregated in warmer surface waters to optimize their scope for growth, mysids still displayed an increasing size with depth (i.e. with decreasing light levels) within that homothermal layer. Ultimately, this indicates that there is a trade-off between occupying warmer waters where food and growth conditions are favorable and avoiding predation and that predation avoidance is the primary factor driving mysid vertical size distributions. The existence of mysids with divergent migration strategies (paper III) further illustrates an aspect of DVM which has been overseen in the past. Both ecological and genetic markers indicate that a division into benthic and pelagic forms, i.e. resident and migrating individuals is an environmentally induced plastic trait. We do not yet know which factors actually induce these different behaviors or whether they are reversible or not, but buy looking at previous studies on partial migration in e.g. fishes, we may suspect that some form of conditional cues like growth rate and food availability may be responsible (Brönmark et al. 2008; Skov et al. 2010).

As mysids in the Baltic Sea have been shown to be food limited large parts of the year (Mohammadian et al. 1997) and niche partitioning (via partial migration) is a way to decrease competition, it is plausible that the observed benthic and pelagic forms of mysids may be prevalent during times of low zooplankton availability. Consequently, we would expect the proportion of migrants/residents to vary with food availability which in turn may affect trophic dynamics. A recent paper by Brodersen and colleagues (2012) demonstrated that seasonal partial migration by roach (Rutilus rutilus), i.e. a temporary migration away from their natal habitat, induced a trophic cascade whereby zooplankton size and abundance increased as a direct consequence of decreased zooplankton predation by roach. If partial DVM in mysids has the same effect on trophic dynamics in the Baltic as in lakes, it will become even more important to understand the circumstances under which alternative migration strategies are formed and maintained as well as the quantification of migrants and residents. Not only do our results put DVM of mysids in a new perspective but also in a more general context as these findings open up for the possibility of partial migration being an inherent life-history strategy in omnivorous diel vertical migrators per se.

Finally, paper IV presents the first model of respiration for a littoral mysid (Praunus flexuosus) that despite its commonness and probable importance in Baltic coastal communities has received undeservedly little attention in comparison to other species. The study also demonstrates that the energy required for the processing of food (SDA) may be present and reflected in respiration over a long period of time (duration and amplitude depending on what and how much has been ingested) which may bias respiration values unless accounted for. In the end, biased basal respiration rates will influence bioenergetics model performance in a negative way (Chipps and Bennett 2002).

In conclusion, this thesis has covered many aspects of mysid biology and ecology. Behavior, physiology, sampling methodology, and monitoring, which are all important factors for a better understanding of mysids as integral components in the Baltic Sea ecosystem.

7. Acknowledgments

First of all, I would like to thank my wonderful supervisors, Sture Hansson, Elena Gorokhova and Tomas Didrikas without whom I surely would have been lost. Sture, you have always been there for me when things where rough, when echosounders were failing and data was messy. Your positive spirit and great enthusiasm always kept me going. Thank you for inspiring me and for introducing me to the world of science. Had it not been for that fisheries biology course in 2002, I would probably have been doing something completely different right now. I am still looking forward to that remote controlled airship project with mounted lasers . We should do something about that Sture! Elena, I don’t know what kind of batteries you are on but I sure would like to have some of them. I am still amazed by how you manage to be “on-line” 24-7. No matter where you are and no matter what time, you always take your time to help me and you always seem to have a brilliant idea in your pocket. The trip to Chile was amazing and we should definitely go on more conferences together. Tomas, sorry for all the late night calls during the hydroacoustic surveys. I was really going mad with all the malfunctions and you really helped me out countless times. I have learnt so much from working with you all and I hope that it won’t end here. So thank you for being such great supervisors and most of all, wonderful friends!

Hedvig, what would I have done without you? Your super-memory kept me away from calendars which I greatly appreciate because I never seem capable of using them anyway. I feel privileged to have been able to share the office with you and having interesting discussions not only about science but also about philosophy, art, your floating sauna projects and Guinea fowl farms . The trips we made with Pelle and Ida through deserts and Rocky Mountains, spiritual encounters with Cherokee cowboys, mountain lions and wild caught rainbow trout sushi on the banks of the Dolores river…the climbing of an active volcano in Chile, chasing rare frogs in the cloudy rainforest…those are the things that I always will remember and keep close to my heart. Thank you guys for sharing these adventures with me. To Jon, Annica, Maria, Micke and all the other colleagues at the department, thanks for making my time here so much more pleasant and fun.

Thanks also to Ragnar Elmgren for being the open library that you are and for all the interesting papers you put in my mailbox over the years, the staff at SMF Askö field station (Suss, Mattias, Eva and Eddie) for all the late night cruises and help during the field work.

To my beloved family: Mamma, Pappa, Sandra, thank you for always believing in me and supporting me throughout the years. I feel fortunate to have such a wonderful and loving family and I couldn’t have done this without you! Jasmin my love, thank you for your understanding, your love, and support! ♥.

The work in this thesis was funded by the Department of Systems Ecology, Stockholm University, Stockholm Marine Research Centre (SMF) and the former Swedish Board of Fisheries (Fiskeriverket).

8. References

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