Quantitative sampling of sub-tidal in the Azores J. Micael, M. J. Alves, M. B. Jones, A. C. Costa

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J. Micael, M. J. Alves, M. B. Jones, A. C. Costa. Quantitative sampling of sub-tidal echinoderms in the Azores. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 2010, pp.327-333. ￿hal-03262201￿

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Quantitative sampling of sub-tidal echinoderms in the Azores

J. Micael 1*, M. J. Alves 2, M. B. Jones 3, A. C. Costa 1 1 CIBIO-Azores, Research Center in Biodiversity and Genetic Resources, Department of Biology, University of the Azores, Campus de Ponta Delgada, 9501-801 Ponta Delgada, Portugal 2 Centro de Biologia Ambiental and Museu Bocage-Museu Nacional de História Natural, Universidade de Lisboa, Rua da Escola Politécnica, 1250-102 Lisboa, Portugal 3 Marine Institute, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK * Corresponding author: [email protected]

ROCKY-BOTTOM ECHINODERMS ABSTRACT. – This paper establishes the appropriate quadrat sample size and the minimal sam- QUADRAT SIZE ABUNDANCE pling effort to quantify the abundance and distribution of the common sub-tidal, rocky-bottom echinoderms of the Azorean Oceanic Islands. Seven (Asteroidea: glacia- lis and Ophidiaster ophidianus; Echinoidea: Arbacia lixula, and Sphaer- echinus granularis; and Holothuroidea: Holothuria tubulosa and Holothuria sanctori) were identified as the commonest echinoderms at São Miguel island. Two quadrat sizes were tested: the standard 1 m2 and a second quadrat size based on maximum organism size (one order of magnitude). While a 1 m2 quadrat was used for most species, due to the relatively large size of some seastars a 9 m2 quadrat was more appropriate. Five levels of sampling effort (based on the number of quadrats) were also tested. Depending on the species, 10, 15 or 20 quad- rats were most appropriate to represent species abundance. No previous study has determined the sampling unit size for quantification or determination of the spatial structure of an echino- derm species. Clearly the sample unit size needs to be determined in relation to the size of the target species together with the aggregative behavior of the species. These results provide key information for more detailed studies of the biology of echinoderms leading to establishing pro- tocols for their conservation and management.

INTRODUCTION est unit should be at least one order of magnitude larger than the size of the largest organism being counted. Green A wide range of quantitative methods are available for (1979) suggested a sampling size of at least 20 times the study of the sessile benthos: ranging from destructive larger than the largest organism, whereas others have rec- techniques, which require the removal of organisms, to ommended as large a sampling size as logistic and cost non-destructive ones, which do not take physical samples constraints allow (Andrew & Mapstone 1987). Despite (Bianchi et al. 2004, Parravicini et al. 2009) and are more the availability of a fair amount of literature providing related to conservation concerns such as visual inventory guidelines for sampling regimes for invertebrate species quadrats and wire frame still photography (Balduzzi et al. such as sponges and mollusks (e.g. Andrew & Mapstone 1996, Ruitton et al. 2000, Garrabou et al. 2002, Guidetti 1987, Hewitt et al. 1998, Shepard 1999, Cattaneo-Vietti et al. 2004, De Biasi et al. 2004, Bussotti et al. 2006). et al. 2002, Parravicini et al. 2009), specific informa- In both methods, differences in the size of the sampling tion for echinoderms is lacking. Most studies of echino- units are an important factor when exploring variability derm abundance and distribution are based on a standard (Andrew & Mapstone 1987, Hewitt et al. 1998, Cattaneo- quadrat size of 1 m2 (Gaymer et al. 2001, Guidetti et al. Vietti et al. 2002, Parravicini et al. 2009). If the sampling 2003, Verling et al. 2003), but even when targeting the regime is too small, statistical tests may not be adequate same species, there is no agreement about the sampling to detect a difference that in reality is there. The smaller unit size. For instance, Sala & Zabala (1996) used a 25 m2 the sample, or the smaller the true difference if it exists, transect while Guidetti et al. (2003) used 1 m2 quadrats the greater the probability of accepting a null hypothesis when targeting the same species. in error, and this probability is increased with increasing Echinoderms are an obvious component of the hard variance among the samples (Shepard 1999). In contrast bottom, marine assemblages around the Azorean Oceanic to the photographic method, visual quadrats should be pre- Islands (Morton et al. 1998) and, while their biogeograph- ferred in investigating shallow rocky reefs for their larger ical ranges are documented (e.g. Koehler 1909, Chap- size (Parravicini et al. 2009). But there is no simple rule man 1955, Marques 1983, Pereira 1997, Hansson 2001), for calculating the optimal quadrat size to use in sampling quantitative details of echinoderm distribution in Azorean (Ecoscope 2000); however, where the spatial arrangement waters are generally lacking (but see Alves et al. 2001). of the organisms is unknown or unimportant, the small- Quantifying the spatial distribution and abundance of 328 J. MICAEL, M. J. ALVES, M. B. JONES, A. C. COSTA echinoderms around the Azores is the first step in estab- lishing protocols for their conservation and management. Previously, quadrats have been used successfully around the globe to measure the abundance and distribution of echinoderms (Benedetti-Cecchi et al. 1998, Linnane et al. 2003, Verling et al. 2003, Roberts et al. 2003). How- ever, although the quadrat method defines a sample area, and is a simple way of collecting replicated data (Perry et al. 2002), the exact dimensions of the quadrat needed to ensure a representative sample for sub-tidal echino- derms have not been established from any geographical area. The aim of this study was to establish the sample size required to quantify the abundance and distribution Fig. 1. – Sampling locations in São Miguel Island: a, Baia do of sub-tidal, rocky-bottom echinoderms from the Azores Cruzeiro; b, Caloura; c, Porto de Santa Iria; and d, São Vincente Islands. da Ferraria.

0.1 cm. This latter method is believed to cause minimal distur- MATERIALS AND METHODS bance to the (Barker & Nichols 1983). The most frequently cited quadrat size – the standard quad- To establish the quadrat size for quantitative sampling, three rat of 1 m2 – together with a 9 m2 quadrat size – based on one dives (May 2007) were carried out in each of the four selected order of magnitude larger than the largest organisms (see Green locations, along the coastline of São Miguel Island (Fig. 1): in 1979) – were chosen (Table I). Having established these criti- each coast (north and south), from a total of 12 possible sam- cal minimal sampling units, surveys of echinoderm abundance pling sites, one location from a moderate-wave exposure area were carried out, between July and August 2007, in the four and one location from a high-wave exposure area were random- selected locations mentioned previously (Fig. 1). Echinoderms ly selected. Each location is characterized by a mix of drained were identified in situ, and counted using the randomly selected lava and big boulders. Maximum depth considered was 15 m. In one, 10, 15, 18 and 20 sample sizes (considering each of the each of the three surveying dives (at each location), three linear two quadrat sizes) with three replicates, representing 5 levels transects of 100 m were carried out. The common echinoderm of sampling effort. The maximum sampling effort possible was species were identified and their sizes were measured (Table I). based on the time spent in manipulate the quadrats and counting Sea-star size was determined by ray length; the distance from organisms at the maximum depth of 15 m due to safe SCUBA the centre of the mouth to the tip of the longest ray (Morgan & limits. Cowles 1996). size was measured as test diameter Two-way ANOVA were used to test for differences in echi- (excluding spine length) (Sala & Zabala 1996). Traditionally, noderm species abundance in relation to sampled locations and the total length of holothurians is the criterion of size, however, sampled area (number and size of quadrat used). Following this measurement is taken after relaxation in 2.5 % MgCl2 (w/v) Duarte and Kirkman (2001), to select a quadrat number com- to overcome any error resulting from contraction and relax- bined with a quadrat size in order to obtain a minimal sampling ation of the animal’s body due to handling (Sewell 1994). As size – to reduce the sampling effort to the one necessary to this was not a feasible procedure underwater, the total length of obtain robust data – the coefficient of variation was determined each holothurian (from tip to tip) was recorded by the same indi- for each species. All analyses were carried out using the soft- vidual (J Micael) using a flexible ruler accurate to the nearest ware package STATISTIC 7 (StatSoft, Inc. 2004).

Table I. – Body size of the echinoderm species (data recorded during the dives of May 2007). Minimum size Total n.º of Species (cm) Larger size (cm) individuals Asteroidea Marthasterias glacialis 13 28 13 Ophidiaster ophidianus 6 30 36 Echinoidea Arbacia lixula 3 5 27 Paracentrotus lividus 3 7 18 9 14 12 Holothuroidea Holothuria tubulosa 18 27 8 Holothuria sanctori 15 23 25

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RESULTS The two-way ANOVAs detected significant differ- ences in abundance for all echinoderm species in relation During the survey of May 2007, seven echinoderm to sampled area (Table III). Minimal sampling size for species were recorded: two from the class Asteroidea; each species was established through the identification three from the class Echinoidea and two from the class of the number of quadrat units combined with a quadrat Holothuroidea (Table I); they were the ones considered size that translated a representative mean of species abun- for the analysis. Asteroid species had the largest body dance with the lowest coefficient of variation (CV) (in sizes and echinoid species had the smallest individuals bold Table IV). As shown in Fig. 2a and b, for each asteroid species, (Table I). During the survey between July and August 2 2007, among the recorded echinoderm species, between 20 quadrats of 1 m will not be sufficient to measure abundance. For M. glacialis, 15 quadrats, each of 9 m2 241 and 251 individuals were observed at each sampling were needed to measure the abundance of this species location (Table II). Among the sampling locations, 59 (Fig. 2a). For O. ophidianus, 10 quadrats of 9 m2 (Fig. 2b) individuals of Marthasterias glacialis (Linnaeus, 1758); produced the population size. For the sea urchins A. lixula 248 individuals of Ophidiaster ophidianus (Lamarck, and P. lividus, 15 quadrats of 1 m2 (Fig. 2c and d) was the 1816); 195 individuals of Arbacia lixula (Linnaeus, appropriate sampling unit to determine abundance but for 1758); 154 individuals of Paracentrotus lividus (Lama- S. granularis 20 quadrats of 1 m2 (Fig. 2e) were needed. rck, 1816); 81 individuals of Sphaerechinus granularis As shown by Fig 2f and g, for the holothurians H. tubu- (Lamarck, 1816); 52 Holothuria sanctori (Delle Chiaje, losa and H. sanctori 10 quadrats of 1 m2 were needed. For 1823) and 188 individuals of Holothuria tubulosa (Gme- all species, there was no significant interaction between lin, 1788) were counted. Of the seven echinoderm species considered in the study three, namely O. ophidianus, A. lixula and H. tub- Table II. – Total number of individuals in each sampling loca- tions: a, Baia do Cruzeiro; b, Caloura; c, Porto de Santa Iria and ulosa showed no significant difference in abundance d, São Vincente da Ferraria. between sampling locations (Table III). M. glacialis had Location significantly higher abundances in the northern coast of Species a b c d S. Miguel Island, both in moderate and high wave expo- sure locations compared with the sampling locations from the south coast (Table II and III). A higher number of Asteroidea P. lividus was found in the high-wave exposure locations, Marthasterias glacialis 11 11 19 18 on the north and south coasts, compared with the mod- Ophidiaster ophidianus 64 64 59 61 erate-wave exposure locations (Table II and III). In con- Echinoidea trast, S. granularis had significantly higher abundances in Arbacia lixula 49 50 47 49 the moderate-wave exposure locations, on the north and Paracentrotus lividus 37 40 37 40 south coasts, in relation to the high-wave exposure loca- Sphaerechinus granularis 23 19 19 20 tions (Table II and III). Like with P. lividus, a higher num- Holothuroidea ber of H. sanctori were found in the high-wave exposure Holothuria tubulosa 12 11 13 16 locations, on the north and south coast (Table II and III). Holothuria sanctori 45 49 47 47

Table III. – Two-way ANOVA comparing echinoderm abundance at four sites and eight sampling areas (Bold, statistically significant values; * P < 0.05, ** P < 0.01). location area location*area df 3 df7 df 21 Species MS F P MS F P MS F P Asteroidea Marthasterias glacialis 56.210 5.493 0.006** 48.340 4.724 0.003** 10.230 0.182 0.994 Ophidiaster ophidianus 12.030 2.967 0.112** 1822.250 449.376 0.000** 4.060 0.337 0.945 Echinoidea Arbacia lixula 33.610 2.163 0.123** 200.820 12.920 0.000** 15.540 0.462 0.877 Paracentrotus lividus 19.110 3.419 0.040** 35.000 6.260 0.000** 5.590 0.293 0.964 Sphaerechinus granularis 30.030 6.235 0.003** 40.710 8.451 0.000** 4.820 0.160 0.997 Holothuroidea Holothuria tubulosa 7.030 2.455 0.106** 6.640 2.317 0.044** 2.860 0.407 0.909 Holothuria sanctori 12.280 4.493 0.014** 22.570 8.255 0.000** 2.730 0.223 0.986

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Table IV. – Descriptive statistics of the echinoderm abundance in function sample area. CV, coefficient of variation. In bold is the best combination considered between the highest mean and the smallest CV. 1 m2 quadrat 9 m2 quadrat Species 1 10 15 18 20 1 10 15 18 20 Asteroidea mean 0.0 2.7 3.0 5.0 8.0 1.0 7.7 12.7 12.7 13.3 Marthasterias glacialis CV 0.000 57.282 66.667 40.000 37.500 100.000 19.924 4.558 12.059 11.456 mean 0.0 2.7 3.0 5.0 8.0 3.0 23.0 22.3 23.0 23.0 Ophidiaster ophidianus CV 0.000 57.282 66.667 40.000 37.500 66.667 4.348 5.170 4.348 13.043 Echinoidea mean 4.7 30.3 51.4 51.3 51.3 8.3 42.0 52.3 52.7 52.7 Arbacia lixula CV 32.733 7.884 2.931 3.249 2.976 18.330 7.143 1.103 2.900 1.096 mean 7.7 24.9 35.0 35.9 35.7 11.3 29.3 35.0 35.0 34.7 Paracentrotus lividus CV 27.152 15.555 0.000 2.444 6.475 30.987 7.097 2.857 7.559 3.331 mean 1.3 7.0 13.7 11.3 20.3 4.7 13.3 16.3 17.7 20.3 Sphaerechinus granularis CV 43.301 14.286 23.521 53.913 2.839 53.927 11.456 9.352 6.536 7.512 Holothuroidea mean 4.3 14.7 14.7 14.0 15.0 5.7 14.3 14.0 14.7 14.3 Holothuria tubulosa CV 35.251 3.936 10.415 7.143 6.667 26.956 8.056 7.143 10.415 4.028 mean 3.7 26.3 26.0 25.0 25.7 5.7 25.0 25.3 24.7 24.7 Holothuria sanctori CV 31.492 2.279 3.846 4.000 5.951 26.956 8.000 6.030 6.193 2.341 minimal sampling area and sampling locations (Table trast to the southern coast. This asteroid is a major shelf III). (depths up to 180 m) predator of marine , includ- ing those of commercial importance such as Paracentro- tus lividus (Savy 1987) and barnacles (Magennis 1981). DISCUSSION No significant differences in O. ophidianus abundance were found between locations; this asteroid is a strictly Differences in the sampling unit size found in the pres- protected species in the Mediterranean Sea by the Bar- ent study derive from the differences found when analyz- celona Convention (92/43/CEE) and is also considered a ing the relationship between the number of individuals vulnerable species in Spain (Catálogo Nacional de Espe- and the number of quadrats. ANOVA tests did not detect cies Amenazadas 2007), however, there is a lack of infor- significant interactions between sample area and location, mation regarding its habitat preferences. As observed thus the sampling sizes tested did not differ in describing in previous studies (e.g. Kempf 1962, Chelazzi et al. differences among sites. Present results demonstrated that 1997, Benedetti-Cecchi et al. 1998, Bulleri et al. 1999), in five of the seven echinoderms studied it was possible although P. lividus and A. lixula often coexist, P. lividus is to use a 1m2 quadrat size to establish the abundance of generally more abundant on horizontal or gently sloping echinoderms in the Azores; however, for the larger spe- surfaces or in crevices at the bottom of rocky walls, while cies (M. glacialis and O. ophidianus), a 9 m2 quadrat A. lixula is more common on vertical substrata. Neverthe- size was more appropriate. Clearly, the choice of quadrat less, in this study, P. lividus had highest numbers in high- size has to be determined, primarily, by echinoderm size, wave exposure locations while no significant difference however, for sub-tidal sampling, there is the added com- in abundance between sites was found for A. lixula. It can plication of diving conditions. Under conditions of strong be hypothesized that differences in the abundance num- currents and limited visibility, it is easier to take a 1 m2 bers of P. lividus may be related to possible differences quadrat to ease the diver’s movement through the water. of the macrophyte structure and biomass of high-wave Statistically significant differences in species abun- exposure versus moderate-wave exposure locations. On dance between locations suggest that further studies on the other hand, these two sea urchins are known to con- spatial distribution of these specific echinoderms should trol the abundance and distribution of and can there- be directed to specific locations. For example, M. glacia- fore have a profound influence on the structure of benthic lis typically occurs amongst the rocky boulder screen on communities (Valentine et al. 1997, Alves et al. 2001). It the shallow landward side, as well as on other grade sub- is crucial to know their habitat requirements and popula- strata (Verling et al. 2003). In the present study, the high- tion dynamics to aid their conservation. Although S. gran- est densities of this species were found along the north- ularis is found from the intertidal zone to 130 m depth ern coast of S. Miguel Island and that may be related to a in a variety of habitats (Martínez-Pita et al. 2008), in this higher percentage of boulders versus drained lava in con- study it had significantly higher abundances in moderate-

Vie Milieu, 2010, 60 (4) QUANTIFICATION OF ROCKY-BOTTOM ECHINODERMS 331

Fig. 2. – Abundance of individuals in relation to sampling area: the x-axis represents the number of quadrats and the y-axis represents the number of infividuals; a, Marthasterias glacialis; b, Ophidiaster ophidianus; c, Arbacia lixula; d, Paracentrotus lividus; e, Sphaer- echinus granularis; f, Holothuria tubulosa; and g, Holothuria sanctori. wave exposure locations compared with high-wave expo- with the other sea urchins, to food availability in moder- sure locations. That can be related to a lesser resistance of ate-wave exposure locations versus high-wave exposure the species to higher hydrodynamic environments or, as locations.

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No significant differences in H. tubulosa abundances Benedetti-Cecchi L, Bulleri F, Cinelli F 1998. Density depend- were found between sampling locations, indicating that ent foraging of sea urchins in shallow subtidal reefs on the west coast of Italy (western Mediterranean). Mar Ecol Prog the wave-exposure degree does not influence the pres- Ser 163: 203-211. ence of the species. According to Bulteel et al. (1992), Bianchi CN, Pronzato R, Cattaneo-Vietti R, Benedetti-Cecchi individuals of H. tubulosa from the Lacco Ameno mead- L, Morri C, Pansini M, Chemello R, Milazzo M, Fraschetti ow (Ischia Island) have a well-marked size distribution S, Terlizzi A, Peirano A, Salvati E, Benzoni F, Calcinai B, related to depth, with the smallest individuals occurring in Cerrano C, Bavestrello G 2004. Mediterranean marine ben- thos: a manual of methods for its sampling and study. Hard the shallowest part of the meadow, while the largest were bottoms. Biol Mar Medit 11: 185-215. found in the deepest part. As in the present study the dives Bulleri F, Benedetti-Cecchi L, Cinelli F 1999. Grazing by the occurred only during the day, when it is more difficult sea urchins Arbacia lixula L. and Paracentrotus lividus Lam. to find and count the smaller individuals of H. tubulosa, in the Northwest Mediterranean. J Exp Mar Biol Ecol 241: probably the species was not properly sampled. 81-95. Information on H. sanctori is very scarce but it is Bulteel P, Jangoux M, Coulon P 1992. Biometry, bathymetric known that it mainly feeds at night (Pérez-Ruzafa 1984); distribution and reproductive cycle of the Holothuroid Hol- othuria tubulosa (Echinodermata) from Mediterranean Sea- in the present study, this species was found in high- grass beds. Mar Ecol 13(1): 53-62. est numbers at high-wave exposure locations which can Bussotti S, Terlizzi A, Fraschetti S, Belmonte G, Boero F 2006. probably be related with food availability. Future studies Spatial and temporal variability of sessile benthos in shallow on the spatial distribution of H. tubulosa and H. sanctori, Mediterranean marine caves. Mar Ecol Prog Ser 325: 109- need to include individual size and nocturnal activity 119. (more easy to find individuals) to establish the spatial uti- Cattaneo-Vietti R, Albertelli G, Bavestrello G, Bianchi CN, Cer- rano C, Chiantore M, Gaggero L, Morri C, Schiaparelli S lization of these species. 2002. Can rock composition affect sublittoral epibenthic To our knowledge no previous study has determined communities? PSZN: Mar Ecol 23: 65-77. the sampling unit size for quantification or determina- Chapman G 1955. Aspects of the Fauna and Flora of the Azores. tion of the spatial structure of an echinoderm species; this IV. Echinodermata. Ann Mag Nat Hist 12(7): 338-400. study clearly demonstrated that the sample unit size needs Chelazzi G, Serra G, Bucciarelli G 1997. Zonal recovery after to be determined in relation to the size of the target spe- experimental displacement in two sea urchins co-occurring cies. The results obtained represent key information for in the Mediterranean. J Exp Mar Biol Ecol 212: 1-7. further studies to determine seasonal spatial distribution De Biasi AM, Bianchi CN, Aliani S, Cocito S, Peirano A, Dando P, Morri C 2004. Epibenthic communities in a marine shal- of echinoderms. Such information is essential for the con- low area with hydrothermal vents. Chem Ecol 20: 89-105. servation of echinoderms, many of which have a specific Duarte CM, Kirkman H 2001. Methods for measurement of sea- habitat preference and are slow moving, restricting their grass abundance and depth distribution. In Short FT, Coles distribution and making them particularly vulnerable to RG eds, Global Research Methods. Amsterdam, local extinction. Elsevier: 146-149. Ecoscope 2000. A species and habitats monitoring handbook. Acknowledgements . – We thank Dr J Borg (University of Vol 2: Habitats. Research, Survey and Monitoring Review Malta) for constructive comments on an early draft of the manu- No. [xx]. Scottish Natural Heritage, Edinburgh: 24 p. script, Master P Rodrigues (University of Azores) and J Brum Garrabou J, Ballesteros E, Zabala M 2002. Structure and dynam- (University of Azores) for field support. This work was support- ics of northwestern Mediterranean rocky benthic communi- ed by the Portuguese Foundation for Science and Technology ties along a depth gradient. Estuar Coast Shelf Sci 55: 493- (FCT) (PhD grant SFRH/BD/27550/2006 to J Micael). 508. Gaymer C, Himmelman J, Johnson L 2001. Distribution and feeding ecology of the seastars Leptasterias polaris and Aste- rias vulgaris in the northern Gulf of St. Lawrence. J Mar REFERENCES Biol Ass UK 81: 827-843. Green R 1979. Sampling design and statistical methods for envi- Alves F, Chicharo L, Serrao E, Abreu A 2001. Algal cover and ronmental biologists. John Wiley & Sons, New York: 257 p. sea-urchin spatial distribution at Island (NE Atlan- Guidetti P, Fraschetti S, Terlizzi A, Boero F 2003. Distribution tic). Sci Mar 65(4): 383-392. patterns of sea urchins and barrens in shallow Mediterranean Andrew N, Mapstone B 1987. Sampling and the description of rocky reefs impacted by the illegal fishery of the rock-boring spatial pattern in marine ecology. Oceanogr Mar Biol 25: mollusc Lithophaga lithophaga. Mar Biol 143: 1135-1142. 2539-2590. Guidetti P, Bianchi CN, Chiantore M, Schiaparelli S, Morri C, Balduzzi A, Bianchi CN, Burlando B, Cattaneo-Vietti R, Man- Cattaneo-Vietti R 2004. Living on the rocks: substrate min- coni R, Morri C, Pansini M, Pronzato R, Sarà M 1996. Zoo- eralogy and the structure of subtidal rocky substrate commu- benthos di substrato duro delle isole di Capraia e del Giglio nities in the Mediterranean Sea. Mar Ecol Prog Ser 274: (Arcipelago Toscano). Atti Soc Toscana Sci Nat 102: 124- 57-68. 135. Hansson H 2001. Echinodermata. In Costello MJ, Emblow CS, Barker M, Nichols D 1983. Reproduction, recruitment and juve- White R eds, European Register of Marine Species. A check- nile ecology of the Asterias rubens and Marthaste- list of the marine species in Europe and a bibliography of rias glacialis. J Mar Bio Ass UK 63: 745-765. guides to their identification. Patrimoines Nat 50: 336-351.

Vie Milieu, 2010, 60 (4) QUANTIFICATION OF ROCKY-BOTTOM ECHINODERMS 333

Hewitt JE, Thrush SF, Cummings VJ, Turner SJ 1998. The effect Pérez-Ruzafa A 1984. Estudio sistemático, ecoiógico y biogeo- of changing sampling scales on our ability to detect effects of grafico de la Clase Holothurioidea (Echinodermata) en las large-scale processes on communities. J Exp Mar Biol Ecol islas Canarias. First degree thesis, Univ Laguna. 227: 251-264. Perry J, Liebhold A, Rosenberg M, Dungan J, Miriti M, Jako- Kempf M 1962. Recherches d’écologie comparée sur Paracen- mulska A, Citron-Pousty S, 2002. Illustrations and guidelines trotus lividus et Arbacia lixula. Recl Trav Stn Mar Endoume for selecting statistical methods for quantifying spatial pat- 25: 47-116. tern in ecological data. Ecography 25: 578-600. Koehler R 1909. Echinodermes provenant des campagnes du Roberts C, Branch G, Bustamante R, Castilla J, Dugan J, Hal- yacht Princesse-Alice (Astéries, Ophiures, Echinides et Cri- pern B, Leslie H, Lafferty K, Lubchenco J, McArdle D, Pos- noides). Résultats Campagnes scientifiques accomplies sur singham H, Ruckleshaus M, Warner R 2003. Application of son yacht par Albert I Prince Souverain de Monaco. Fasc ecological criteria in selecting marine reserves and develop- XXXIV, 317 p., 32 pls. ing reserve networks. J Appl Ecol 13: 215-228. Linnane A, Ball B, Munday B, Browne R, Mercer J 2003. Fau- Ruitton S, Francour P, Boudouresque CF 2000. Relationships nal description of an Irish cobble site using airlift suction between algae, benthic herbivorous invertebrates and fishes sampling. Biol Environ 103(1): 41-48. in rocky sublittoral communities of a temperate sea (Medi- Magennis B 1981. Feeding habits of Marthasterias glacialis. J terranean). Estuar Coast Shelf Sci 50: 217-230. Sherkin Isl 1: 36-49. Sala E, Zabala M 1996. Fish and the structure of the Marques V 1983. Peuplements benthiques des Açores. I. Echi- sea urchin Paracentrotus lividus population in the NW Medi- nodermes. Arquiv Mus Bocage 2(1): 1-12. terranean. Mar Ecol Prog Ser 140: 71-81. Martínez-Pita I, Sánchez-España AI, García FJ 2008. Gonadal Savy S 1987. Activity pattern of the sea star, Marthasterias gla- growth and reproduction in the sea urchin Sphaerechinus cialis in Port-Cros Bay (France, Mediterranean Coast). Mar granularis (Lamarck 1816) (Echinodermata: Echinoidea) in Ecol 8: 97-106. southern Spain. Sci Mar 72(3): 603-611. Sewell M 1994. Small size, brooding, and protandry in the apo- Morgan M, Cowles D 1996. The effects of temperature on the did sea cucumber Leptosynapta clarki. Biol Bull 187: 112- behavior and physiology of Phataria unifascialis Gray (Echi- 123. nodermata, Asteroidea): Implications for the species’ distri- Sheppard CRC 1999. How large should my sample be? Some bution in the Gulf of California, Mexico. J Exp Mar Biol quick guides to sample size and the power of the test. Mar Ecol 208: 13-27. Pollut Bull 38: 439-447. Morton B, Briton J, Martins AF 1998. Coastal Ecology of the StatSoft, Inc 2004. STATISTICA (data analysis software sys- Azores. Sociedade Afonso de Chaves e Direcção Regional tem), version 7. www.statsoft.com. da Cultura, Ponta Delgada, Portugal: 249 p. Valentine JF, Heck Jr KL, Busby J, Webb D 1997. Experimental Parravicini V, Morri C, Ciribilli G, Montefalcone M, Albertelli evidence that herbivory can increase habitat complexity and G, Bianchi CN 2009. Size matters more than method: Visual flowering in a subtropical turtlegrass (Thalassia testudinum) quadrat vs photography in measuring human impact on Med- meadow. Oecologia 112: 193-200. iterranean rocky reef communities. Estuar Coast Shelf Sci Verling E, Crook A, Barnes D, Harrison S 2003. Structural 81: 359-367. dynamics of a sea-star (Marthasterias glacialis) population. Pereira M 1997. Checklist of the littoral echinoderms of the J Mar Biol Ass UK 83: 583-592. Azores. Açoreana 8(3): 331-337. Received November 3, 2010 Accepted January 11, 2011 Associate Editor: A Chenuil

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