The Habitat Engineering Tunicate Microcosmus Sabatieri Roule, 1885 and Its Associated Peracarid Epifauna

Estuarine, Coastal and Shelf Science 74 (2007) 197e204 www.elsevier.com/locate/ecss

The habitat engineering tunicate Microcosmus sabatieri Roule, 1885 and its associated peracarid epifauna

Eleni Voultsiadou*, Maria-Myrto Pyrounaki, Chariton Chintiroglou

Department of Zoology, Aristotle University, School of Biology, 54124 Thessaloniki, Greece Received 19 August 2006; accepted 5 April 2007 Available online 30 May 2007

Abstract

The solitary ascidian Microcosmus sabatieri is a common ecosystem engineering species on hard bottom sublittoral communities in the East- ern Mediterranean. Peracarida are common inhabitants of biological substrata, such as algae, sponges and ascidians and have been proven to be very sensitive to changes in environmental conditions. The aim of this study was to present and analyse, for the first time, the structure of the peracarid epifaunal assemblage inhabiting this Mediterranean endemic, edible and commercially exploited species. During sampling in the North Aegean Sea, 41 specimens were collected and examined for their peracarid epifauna. Overall, 38 peracarid species were identified, a high number in comparison to those recorded in the few other relevant studies on ascidian epifauna. The great majority of the species were amphipods. By contrast, in terms of abundance, tanaidaceans was the dominant taxon, with Leptochelia savigni being by far the most dominant species. Tube-dwelling suspension-feeders dominated the peracarid epifauna of this tunicate. The suspension feeding mode of epifaunal peracarids is possibly favoured by the high filtration rate of M. sabatieri which is large sized and has an extensive branchial surface. It is suggested that the tube-dwelling habit of tanaidaceans and some amphipods offering extra protection, may further explain their dominance as elements of the epifauna, in contrast to other inquiline peracarids which prefer to search for shelter inside the canals of sponges or, in a few cases inside the mantle cavity of ascidians. Differences in peracarid abundance among the ascidian specimens were attributed to the reproductive and dispersal habits of the former. Species richness, abundance and diversity of the motile peracarid epifauna was dependent on the biomass of the ascidian, but most strongly on the biomass of the sessile epibiontic organisms, such as algae and sponges which, in some cases, had a higher biomass than the ascidian itself. Thus, M. sabatieri with its wrinkled surface usually supporting a rich sessile epiflora and epifauna provides a favourable habitat for a quite homogenous peracarid assemblage. A thorough study of the entire community associated with M. sabatieri and its comparison with that in the surrounding environment could further elucidate the role of this organism in the enrichment of local biodiversity. Ó 2007 Elsevier Ltd. All rights reserved.

Keywords: Peracarida; Microcosmus sabatieri; Ascidiacea; ecosystem engineering; epifauna; animal associations; Aegean Sea; Mediterranean Sea

1. Introduction consequently inﬂuencing local biodiversity. Their study has been recently of increasing interest due to their ecological im- Ecosystem engineering is the creation, destruction or mod- portance in structuring benthic communities. Sabellariid poly- iﬁcation of habitats by living organisms having complex con- chates (Nelson and Demetriades, 1992), bryozoans (Conradi sequences on the structure of biological communities (Jones et al., 2000), mussels (Tsuchiya and Bellan-Santini, 1989), et al., 1994; Crooks, 2002). sponges (Ribeiro et al., 2003), barnacles and ascidians (Yako- Various marine benthic animals have been considered as vis et al., 2005) have been examined for their relationships ecosystem engineers increasing habitat complexity and with associated fauna. Moreover, since some of the species belonging to the above groups are of commercial interest, their * Corresponding author. overexploitation might have serious consequences for biodi- E-mail address: [email protected] (E. Voultsiadou). versity (Coleman and Williams, 2002).

A rich macro-invertebrate fauna has been found living in the commercially exploited; (3) the rich cover of this ascidian crevices and interstices between the individuals of ascidian spe- by sessile epibionts, i.e. algae, sponges and bryozoans, could cies forming dense beds or matrices, such as those of the genus possibly provide an extra complex habitat favouring the settle- Pyura living in intertidal communities (Fielding et al., 1994; ment of motile macro-invertebrates; and (4) Peracarida are Cerda and Castilla, 2001; Monteiro et al., 2002; Sepu´lveda reckoned among the most diverse and abundant members of et al., 2003; Castilla et al., 2004). Ascidians provide a complex the community associated with living substrata in the Aegean substratum for their epibionts, and are preferably inhabited Sea, i.e. corals and sponges (see Koukouras et al., 1985, 1998), by suspension feeding macro-invertebrates which may utilize and they have been proven to be very sensitive to environmen- the abundant suspended material available in their vicinity tal conditions (Conradi et al., 1997) and changes induced by (Sepu´lveda et al., 2003). On the other hand, like other sessile human activities (Baxevanis and Chintiroglou, 2000). macro-invertebrates, i.e. sponges and bryozoans, they produce On the basis of the above considerations, the aim of the antifouling substances (e.g. Teo and Ryland, 1994), which present work was to investigate, describe and analyse the might reduce the abundance of some associated organisms. structure of the peracarid epifaunal community inhabiting Peracarida have been studied as common inhabitants of this common Aegean tunicate. This was accomplished primar- living substrata, such as algae, sponges, corals, polychaetes, ily through the estimation of faunal composition, species rich- mollusks and bryozoans (Stachowitsch, 1980; Koukouras ness, abundance of individuals, dominance and diversity of the et al., 1985; Costello and Myers, 1987; Nelson and Deme- peracarid epifauna associated with numerous specimens of triades, 1992; Conradi and Cervera, 1995; Koukouras et al., Microcosmus sabatieri found at a selected site in the North 1998; Serejo, 1998; Conradi et al., 2000; Thiel and Va´squez, Aegean. Furthermore, in order to test the general hypothesis 2000; Broyer et al., 2001; Cinar et al., 2002; etc.). However, that the structure of the peracarid epifaunal community may the peracarid epifauna associated with ascidians has been the be dependant on the structure of its habitat, in our case a soli- subject of a restricted number of studies: Monniot (1965a) tary tunicate, the above parameters were correlated with the gave information on the epifauna of Microcosmus species morphometric characteristics of the ascidian and the sessile forming blocks in the muddy bottoms of the western Mediter- epibiontic cover. Specific issues examined were: (1) the simi- ranean. Vader (1984) noted some amphipod species associated larity among the ascidian individuals studied on the basis of with tunicates in the Norwegian waters. Finally, a few species their peracarid epifauna in order to test whether the latter of this group have been recorded as epibionts of Pyura in the forms a homogenous assemblage; (2) the relationship between literature mentioned above (for an exception see Sepu´lveda the ascidian length and biomass and the peracarid species rich- et al., 2003). ness, abundance of individuals and diversity; (3) the possible Microcosmus sabatieri is a solitary ascidian living attached effect of the sessile epiflora and epifauna on the peracarid on various hard substrata in the Mediterranean infralitoral community; (4) the possible dominance of certain taxonomic zone, on both muddy and rocky bottoms. In contradiction to or functional groups, such as the suspension-feeders in the the ascidians of the genus Pyura, this species does not form community; and (5) the possibility to predict species richness, dense beds, but it is one of the most conspicuous and abundant which is considered as a very good surrogate for biodiversity megabenthic species in this area (Antoniadou et al., 2006). It (Gaston and Spicer, 2004), of the epibiontic Peracarida using is a Mediterranean endemic recorded from the Aegean Sea the abundance of individuals. (Koukouras et al., 1995), edible, and of commercial interest in several Mediterranean countries (Monniot and Monniot, 1987). It reaches a large size, sometimes passing 20 cm in 2. Materials and methods height, and its wrinkled tunic, characteristic of the family Pyuridae, is often covered with numerous epibiontic organisms, Sampling was carried out by SCUBA diving at Porto and accounts for the genus name given by Cuvier in 1815 Koufo, a small, deep bay located on the extreme end of Si- (micros ¼ small þ cosmos ¼ world) (Monniot, 1965a). thonia Peninsula, in the North Aegean Sea (395703400N, This work is part of a broad study on the epifauna associ- 235501800E). In total, 41 Microcosmus sabatieri individuals ated with Microcosmus sabatieri living on the rocky bottoms growing on large rocks were collected in June 1994, at of the Aegean Sea, Eastern Mediterranean. Main reasons for depths of 5e12 m and in a total area of 500 m2. The ascid- studying this specific community were the following: (1) the ians were covered with a plastic bag before being removed ascidian M. sabatieri seems to be an important habitat builder from the rock surface. Samples, preserved in 10% formalin, in the Aegean Sea, where other living substrata, such as were washed over a 0.5 mm mesh sieve in the laboratory. For sponges and corals have been studied for their associated each specimen, the total wet weight was measured. Before fauna, as mentioned above; the contribution of this ascidian being weighed the ascidians were cut with a knife in order to the benthic community structure, especially in an impover- to loose all the formalin kept inside the tunic and they ished ecosystem such as the South Aegean, (see Voultsiadou, were carefully folded for a while in blotting paper. Then, ep- 2005) might be significant; (2) it is necessary to first describe iflora and sessile epifauna (sponges, cnidarians, etc.) were the fauna associated with this habitat forming species in order separated and their wet weight determined. Additionally, to be able to predict how changes to the habitat may affect ma- maximum length of the ascidians, from the base of attach- rine diversity in the area, given that M. sabatieri is ment to the base of the oral siphon, was measured. Mobile E. Voultsiadou et al. / Estuarine, Coastal and Shelf Science 74 (2007) 197e204 199 epifauna was sorted, and the peracarid material was identi- analysis and Spearman rank correlation were used. Faunal fied to species level. similarity among ascidian specimens was calculated using Common biocoenotic methods were employed to analyse hierarchical clustering based on Bray-Curtis similarity and the data (Bellan-Santini, 1981). Five community parameters non-metric multidimensional scaling ordination, with the were calculated: mean abundance (mA), the mean number of Primer package (Clarke and Warwick, 1994). individuals of a peracarid species per ascidian specimen; presence (P), the number of ascidian specimens on which each 3. Results peracarid species occurred; frequency of appearance (F ), the percentage presence; and mean dominance (mD), the percent- Overall 38 peracarid species were found to live on the 41 as- age abundance of peracarid species in relation to the total per- cidian specimens collected. The taxonomic composition of the acarid abundance on each ascidian specimen. peracarid epifauna was: 25 species of amphipods, 5 isopods, 6 Peracarid diversity was calculated using the Shannon- tanaidaceans and 2 cumaceans (Table 1). A total of 2177 indi- Wiener (H ), Margalef (d ) and eveness (J ) indices (Dajet, viduals were counted, the great majority of which (1415) were 1979). In order to estimate the relationships between the tanaidaceans, followed by 497 amphipods, 231 isopods and 34 morphometric characteristics of the ascidians and peracarid cumaceans. The most abundant species identified was the abundance, species richness and diversity, linear regression tanaidacean Leptochelia savigni (mean Dominance w43%)

Table 1 Community parameters for the peracarid epifauna of Microcosmus sabatieri. t, Tanaidacea; a, Amphipoda; i, Isopoda; c, Cumacea; T, tube-builder; S, suspension- feeder; P, predator; G, grazer; D, detritivore; O, omnivore; C, commensal Peracarida species Order Feeding mode Presence Frequency % Mean abundance Mean Cumulative & life habit dominance % dominance % Leptochelia savignyi (Kroyer, 1842) tS, T 40 97.56 22.878 43.08 43.08 Pseudoparatanais batei (Sars, 1882) tS, T 37 90.24 7.560 14.24 57.32 Microdeutopus anomalus (Rathke, 1843) aS, T 31 75.61 4.512 8.50 65.82 Janira maculosa (Leach, 1814) iS 24 58.54 3.829 7.21 73.03 Tanais dulongii (Audouin, 1826) tS, T 13 31.71 2.463 4.64 77.67 Hyale camptonyx (Heller, 1866) aG 16 39.02 2.390 4.50 82.17 Apseudes intermedius (Hansen, 1895) tS 20 48.78 1.560 2.94 85.11 Paranthura nigropunctata (Lucas, 1849) i ? 18 43.90 1.122 2.11 87.22 Cumella limicola (Sars, 1879) cG, S 14 34.15 0.805 1.51 88.73 Dexamine spinosa (Montagu, 1813) aG, S 21 51.22 0.756 1.42 90.15 Leucothoe spinicarpa (Abildgaard, 1789) aS, C 8 19.51 0.634 1.19 91.34 Lysianassa costae (Milne-Edwards, 1830) aP 18 43.90 0.560 1.06 92.40 Guernea coalita (Norman, 1868) aS 13 31.71 0.536 1.01 93.41 Stenothoe monoculoides (Montagu, 1813) aO 13 31.71 0.512 0.96 94.37 Gnathia vorax (Lucas, 1849) iG 13 31.71 0.512 0.96 95.33 Orchomene grimaldii (Chevreux, 1890) aP 12 29.27 0.488 0.92 96.25 Corophium acherusicum (Costa, 1851) aS, T 10 24.39 0.439 0.83 97.08 Orchomene humilis (Costa, 1853) aP 6 14.63 0.244 0.46 97.54 Colomastix pusilla (Grube, 1861) aP, C 7 17.07 0.195 0.37 97.91 Dexamine spiniventris (Costa, 1853) aG, S 6 14.63 0.170 0.32 98.23 Munna kroyeri (Goodsir, 1842) i ? 5 12.20 0.146 0.27 98.50 Synchelidium longidigitatum (Ruffo, 1947) aO 4 9.76 0.122 0.23 98.73 Elasmopus pocillimanus (Bate, 1862) aG 3 7.32 0.097 0.18 98.91 Ampelisca ledoyeri (Bellan-Santini and aT, S 3 7.32 0.073 0.14 99.05 Kaim- Malka, 1977) Coboldus nitior (Krapp-Schickel, 1974) a ? 3 7.32 0.073 0.14 99.19 Phtisica marina (Slabber, 1769) aP 1 2.44 0.073 0.14 99.33 Caprella acanthifera (Leach, 1814) aO 1 2.44 0.049 0.09 99.42 Gitana sarsi (Boeck, 1871) a ? 2 4.88 0.049 0.09 99.50 Gammarella fucicola (Leach, 1814) aD 1 2.44 0.024 0.05 99.55 Leucothoe richiardii (Lessona, 1865) aS 1 2.44 0.024 0.05 99.60 Metaphoxus fultoni (Scott, 1890) a ? 1 2.44 0.024 0.05 99.65 Perioculodes aequimanus (Kossmann, 1880) a ? 1 2.44 0.024 0.05 99.70 Pseudoprotella phasma (Montagu, 1804) aO 1 2.44 0.024 0.05 99.75 Tritaeta gibbosa (Bate, 1862) aO, C 1 2.44 0.024 0.05 99.80 Dynamene torelliae (Holdich, 1968) iG 1 2.44 0.024 0.05 99.85 Apseudes latreillii mediterraneus tS 1 2.44 0.024 0.05 99.90 (Bacescu, 1965) Pseudoleptochelia anomala (Sars, 1882) tT, S 1 2.44 0.024 0.05 99.95 Iphinoe rhodaniensis (Ledoyer, 1965) cP 1 2.44 0.024 0.05 100.00 200 E. Voultsiadou et al. / Estuarine, Coastal and Shelf Science 74 (2007) 197e204 with 938 individuals, constituting 66% of the tanaidacean abun- n ¼ 41). Furthermore, a comparatively strong correlation dance and 43% of the total peracarid abundance. The 10 most was found between peracarid species richness (S ) and abun- common species, 4 tanaidaceans (Leptochelia savigni, Pseudo- dance of individuals (N ) in the different ascidian specimens paratanais batei, Tanais dulongii, Apseudes intermedius), 3 am- (Rs ¼ 0.719, p < 0.01, n ¼ 41) (Fig. 3), with the exception phipods (Microdeutopus anomalus, Hyale camptonyx, of two specimens, one of which had extreme numbers of spe- Dexamine spinosa), 2 isopods (Janira maculosa, Paranthura cies and the other of individuals. nigropunctata) and 1 cumacean (Cumella limicola) were re- sponsible for 90% of the cumulative dominance of the total per- 4. Discussion acarid epifauna, appearing in the ascidian specimens with a frequency varying between 31% and 98% (Table 1). The solitary ascidian Microcosmus sabatieri is a very com- Species richness, abundance of individuals and diversity in- mon inhabitant of hard bottom sublittoral communities (Anto- dices of peracarid epifauna varied among individual ascidians, niadou et al., 2006) with densities reaching 10 indiv. m2 in as seen from the statistics presented in Table 2. Speciﬁcally, the Aegean Sea (Antoniadou et al., 2004). The Peracarida is the values of ascidian biomass, biomass of sessile organisms a major faunal element, in terms of species richness, next to and abundance of peracarid individuals were widely scattered. polychates and gastropods, of the same habitat in the Eastern In order to check whether the peracarid assemblage living Mediterranean (Antoniadou and Chintiroglou, 2005). Thus, it on the ascidian individuals was homogenous, the ascidians was not surprising that the peracarid epifauna found on M. sa- were compared on the basis of the extent to which they shared batieri specimens collected during the present study formed particular peracarid species. Both hierarchical clustering and a rich species assemblage, comprising 38 species. This number non-metric multidimensional scaling ordination applied on is high compared to the few existing records of peracarid spe- non-transformed data (not presented here) did not reveal any cies richness associated with ascidians: 4 species by Monniot grouping: ascidian specimens were arranged mostly according (1965b) on Microcosmus species (qualitative data), 14 by to the number of peracaridan species and individuals (stress Fielding et al. (1994) on Pyura stolonifera (size of sampling value 0.1). Some specimens were separated because of the ex- quadrates selected so that >90% of the total number of species tremely high or low number of species and individuals. The found were present), 24 by Sepu´lveda et al. (2003) on Pyura length and the coverage of the individual ascidians did not chilensis (55 ascidian individuals examined) and 9 species seem to induce any differentiation in the peracarid species by Castilla et al. (2004) on Pyura praeputialis (28 samples composition among pairs of ascidian individuals. with an estimated optimum plot size of 35 35 cm). The spe- The estimation of relationships between the peracarid species of the genus Pyura usually form dense beds with crevices cies richness (S ), abundance of individuals (N ) and diversity and interstices between individuals, thus providing a safe and (d, H0) on one hand and the ascidian length (L) and biomass stable habitat for benthic invertebrates, comparable to mussel (Ba) on the other, resulted in stronger or weaker positive cor- beds (Fielding et al., 1994; Castilla et al., 2004). Microcosmus relations in almost all cases, with Spearman’s coefﬁcient sabatieri also proved to be a suitable habitat for epifauna, reaching 0.649 for the pair peracarid abundance-ascidian bio- although its solitary individuals live well separated from one mass (Fig. 1B) and 0.600 for species richness-ascidian bio- another on the rocky substratum. Monniot (1965b) claimed mass (Fig. 1A) ( p < 0.01, n ¼ 41). The number of both that Microcosmus individuals on a rocky coast can be totally peracarid species and individuals were weakly positively cor- covered with epibionts and this epibiontic coverage is some- related with the length of the ascidians (Rs ¼ 0.395, and 0.345 times in continuity with that of the surrounding hard substra- respectively, p < 0.05, n ¼ 41) and the same was true for Mar- tum. The ascidian provides a favorable substratum for sessile galef’s diversity (Rs ¼ 0.300, p < 0.05 and 0.378 p < 0.01 re- organisms such as algae, sponges, hydrozoans, bryozoans, spectively). Shannon diversity index hardly varied with the which in their turn form a complex habitat for small-sized per- above ascidian variables (Rs ¼ 0.107 and 0.210 respectively). acarids, thus contributing to the maintenance of their diversity A positive correlation existed as well between all the above in sublittoral rocky shores, as Ribeiro et al. (2003) have stated peracarid parameters, and the biomass of the ascidian sessile for sponges. The high species richness of the motile peracarid epibionts (Bs): Rs ¼ 0.712 for peracarid species richness community seems to be strongly affected by the dense cover of (Fig. 2A), 0.564 for peracarid abundance (Fig. 2B), and sessile epibionts which, in some cases, was found to have 0.568 for Margelef’s diversity index (Fig. 2C) ( p < 0.01, a higher biomass value than the ascidian itself. This is shown

Table 2 Statistics of the morphometric parameters, peracarid species richness, abundance and diversity indices for the individual specimens of Microcosmus sabatieri. L, total length in cm; Ba, ascidian wet weight in g; Bs, wet weight of the sessile epibionts in g; S, peracarid species richness; N, peracarid abundance; H, Shannon- Wiener diversity index; d, Margalef’s richness; J, Pielou’s evenness Statistics L Ba Bs SN HdJ Mean 7.7512 58.9373 43.7225 9.0732 53.0976 2.2771 2.1797 0.7580 Minimum 4.50 11.36 7.97 2.00 2.00 1.00 0.87 0.43 Maximum 11.70 190.00 219.50 24.00 309.00 3.35 4.20 1.00 Std. Deviation 1.82004 45.42587 40.45905 3.95847 57.26421 0.55359 0.68785 0.11967 E. Voultsiadou et al. / Estuarine, Coastal and Shelf Science 74 (2007) 197e204 201

30 A S = 0.0702Ba+5.1191 30 S = 0.0483N +6.5076 Rs = 0.600, p<0.01 Rs = 0.719, p<0.01 25 25

20 20

15 15

10 10

5 5 Peracarid species richness 0 Peracarid species richness 0 0 50 100 150 200 0 50 100 150 200 250 300 350 Peracarid abundance 30 B N = 0.0524Ba +6.1824 Fig. 3. Peracarid species richness (S ) e abundance (N ) correlation. 25 Rs = 0.649, p<0.01 20 15 assemblage associated with M. sabatieri was quite homoge- 10 nous among the individual ascidians all over the studied 5 area, without any differentiations in its composition.

Peracarid abundance Many of the peracarids found during this study, at least the 0 0 50 100 150 200 most dominant species (e.g. the tanaidaceans Leptochelia Ascidian biomass savigni, Pseudoparatanais batei, Tanais dulongi and the amphipod Microdeutopus anomalus), are tube-dwelling suspen- Fig. 1. Correlation of peracarid species richness (S ) and abundance (N ) with sion-feeders (see Table 1). Tube dwelling peracarids possibly ascidian biomass (Ba). find both shelter and food in this microhabitat, thus having lit- by the significant positive correlation found between the pera- tle need to change their location, as Thiel and Va´squez (2000) carid species richness and the biomass of the sessile epifauna, proposed for kelp holdfasts. Moreover, the suspension-feeding which was even stronger than the one between species rich- type is dominant among peracarids associated with ascidians, ness and the ascidian biomass. However, the peracarid which form a beneficial substratum for suspension-feeding fauna; the latter may utilize the abundant suspended material 30 available in their vicinity (Sepu´lveda et al., 2003). It is worth A S=0.0591Bs+6.4881 25 Rs=0.712, p<0.01 mentioning that Microcosmus sabatieri has a high filtration 20 rate in comparison to other ascidian species due to its large 15 size and its extensive branchial surface (Fiala-Medioni, 1974). Suspension-feeding macro-invertebrates have been re- 10 ported to live in large numbers and high biomass in association 5 with ascidians (Fielding et al., 1994). Sepu´lveda et al. (2003) 0

Peracarid species richness 0 50 100 150 200 250 suggested that filter-feeding peracarids live with these tunicates because the latter grow at sites favorable for organisms 350 B N=0.6329Bs+25.426 of this feeding-type. It seems that the spatial distribution of 300 Rs=0.564, p<0.01 peracarids belonging to this functional group is most affected 250 by the availability of the habitat engineered by the ascidians. 200 Thus, their study could provide interesting information regard- 150 ing the mechanisms by which habitat engineering organisms 100 contribute to the increase of species richness at a landscape 50 scale (Castilla et al., 2004). Peracarid abundance 0 As in all previous studies on ascidian- or sponge-associated fauna (Koukouras et al., 1985; Fielding et al., 1994; Cinar 5 C d=0.0089Bs+1.7896 et al., 2002; Sepu´lveda et al., 2003; Castilla et al., 2004), Rs=0.568, p<0.01 4 amphipods were richest in species among Peracarida (twice 3 as many as the species in all other groups). However, for the first time, a significant dominance of tanaidaceans over 2 amphipods in terms of abundance is reported: the mean dom- 1 inance of the 6 tanaidacean species was 65% of the total, Margalef’s diversity 0 versus 22.8% of amphipods, 10.6 of isopods and 1.6 of cu- 0 50 100 150 200 250 maceans. It is remarkable that in sponges living at the Biomass of sessile organisms same ecological zone and geographic area, amphipods have Fig. 2. Correlation of peracarid species richness (S ), abundance (N ) and diver- been found in much higher abundances than tanaidaceans sity (d ) with the biomass of the ascidian sessile epibionts (Bs). (Koukouras et al., 1985; Voultsiadou-Koukoura et al., 202 E. Voultsiadou et al. / Estuarine, Coastal and Shelf Science 74 (2007) 197e204

1987). This can be understood if the associates of the two have no free-living larval stage, their development is direct above animal substrata are considered not as taxonomical and the fully developed juveniles emerging from the female’s but as functional groups. It seems that the tube-dwelling, sus- marsupium recruit into the immediate vicinity of their parents pension-feeding mode of the tanaidaceans permits these ani- (Poore et al., 2000). As Thiel and Va´squez (2000) proposed, mals to live safely as epibionts, while inquilines such as organisms like algae, sponges and ascidians can be considered Leucothoe spinicarpa, Colomastix pusilla or Tritaeta gibbosa as patches on the sea bottom with island-like features. These tend to aggregate in high abundances inside the canals of the isolated patches may serve as a centre for aggregation of con- sponges in the same geographic area (Koukouras et al., 1985; specific individuals, where they can find food and shelter, thus Cinar et al., 2002). Notice that L. spinicarpa, which has having little need to change their location (Thiel and Va´squez, evolved adaptations to life inside the sponge aquiferous sys- 2000). These aggregations and the restricted tendency of per- tem (Ribeiro et al., 2003), has been commonly found inside acarid individuals for emigration from one ascidian to the the tunic of ascidians as well (Vader, 1984; Thiel, 1999, other may explain the great fluctuation of the diversity indices. 2000). Moreover, the tube-building amphipod Microdeutopus Similarly, aggregations of macrofaunal species at small spatial anomalus, the third dominant species in our material, was scales due to differences in their reproduction and dispersal also a dominant epibiont on the sponges Halichondria pani- strategies have been reported from other habitat building or- cea and Hymeniacidon sanguinea living on small cracks and ganisms, such as algae, by Tanaka and Leite (2003). Notice depressions of sponge surface (Frith, 1976; Costello and however, that in the present study, the epibiontic organisms Myers, 1987). Much work needs to be done in order to inves- of the ascidians were treated as a total cover, providing shelter tigate species interactions within such assemblages. to motile epifauna. A detailed study of the different kinds of All peracarid species recorded in this study have been pre- epibionts (i.e. sponges, algae, compound ascidians, bryozoans, viously reported from the Aegean Sea (Kocatas, 1976; Stefa- etc.) could possibly lead to specific explanations for the differ- nidou and Voultsiadou-Koukoura, 1995; Koukouras et al., ences in species richness and abundance of the epibiontic 1996; Antoniadou, 2004; Kirkim et al., 2005) and most of Peracarida. them are well known inhabitants of the sublitoral rocky sub- Ecosystem-engineering species merit increased scientific strata and specifically of the photophilic algae community and conservation emphasis, because of the fundamental role (Antoniadou and Chintiroglou, 2005). No host-specific species that they play in shaping habitat and the dependant communi- were found. According to our results, 43% of the total abun- ties (Coleman and Williams, 2002; Crooks, 2002). Several dance is contributed by the dominant species, Leptochelia sa- ascidian species of the family Pyuridae, providing an impor- vigni, which was present in all individual ascidians with high tant habitat for many organisms, are used as food and bait abundances. Relatively high abundances contributed by few for fishing (Monteiro et al., 2002); Microcosmus sabatieri is tanaidacean or amphipod species were found also on the ascid- an intensely harvested species at several locations of the Ae- ian Pyura chilensis by Sepu´lveda et al. (2003). Leptochelia gean Sea (Antoniadou et al., 2004) and besides the direct savigni is a cosmopolitan species that is common in the Ae- loss, its commercial exploitation could have cascade effects gean in association with various living substrata, such as algae, on its associated community and the rest of the ecosystem. sponges and mussel beds (Koukouras et al., 1996; Cinar et al., In order to predict the effects of such disturbances, it is neces- 2002; Chintiroglou et al., 2004). Its high dominance among sary to understand the relationship between the structure of the the peracarid epifauna does not necessarily mean a special re- habitat provided by these ascidians and their associated assem- lationship between this crustacean and the ascidian, since the blages (Monteiro et al., 2002). Moreover, a thorough study of former has been reported with high abundances from the the entire community associated with M. sabatieri and its com- deeper (15e40 m) rocky substrata of the same area (Antonia- parison with that in the surrounding environment could further dou and Chintiroglou, 2005), as well as from artificial sub- elucidate the role of this organism in the enrichment of local strata in adjacent ports (Baxevanis and Chintiroglou, 2000). biodiversity. The amphipods Microdeutopus anomalus and Dexamine spinosa and the cumacean Cumella limicola, which are among Acknowledgements the 10 dominant species on Microcosmus sabatieri, were also found in high abundances in adjacent areas according to We are grateful to Martin Thiel and two anonymous re- the same authors. However, the similarity of the peracarid viewers for providing useful comments and suggestions that fauna living on M. sabatieri with that living on the rocky sub- upgraded the manuscript. stratum of the same area needs to be further investigated. Ya- kovis et al. (2005) studying patches of ascidians and barnacles showed that motile fauna is strongly dependent on the sessile References one and differs from the surrounding assemblage. Strong differences were observed in peracarid abundances Antoniadou, C., 2004. Crustacean distribution pattern on vertical cliffs in the between Microcosmus sabatieri individuals. The number of in- Northern Aegean (Eastern Mediterranean). Fresenius Environmental Bulletin 13, 726e732. dividuals varied from a minimum of 2 in some specimens to Antoniadou, C., Chintiroglou, C., 2005. Biodiversity of zoobenthic hard- a maximum of 309 in others (see Table 2). This is possibly substrate sublittoral communities in the eastern Mediterranean (North Ae- a consequence of the peracarid reproductive habit. Peracarids gean Sea). Estuarine, Coastal and Shelf Science 62, 637e653. E. Voultsiadou et al. / Estuarine, Coastal and Shelf Science 74 (2007) 197e204 203

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