Macrofauna associated to Mycale microsigmatosa (Porifera, Demospongiae) in Rio de Janeiro State, SE Brazil

Macrofauna associated to Mycale microsigmatosa (Porifera, Demospongiae) in Rio de Janeiro State, SE Brazil

Estuarine, Coastal and Shelf Science 57 (2003) 951–959 Macrofauna associated to Mycale microsigmatosa (Porifera, Demospongiae) in Rio de Janeiro Stat...

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Estuarine, Coastal and Shelf Science 57 (2003) 951–959

Macrofauna associated to Mycale microsigmatosa (Porifera, Demospongiae) in Rio de Janeiro State, SE Brazil Suzi M. Ribeiro, Elianne P. Omena, Guilherme Muricy* Departamento de Invertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista s/n, Sa˜o Cristo´va˜o, 20940-040 Rio de Janeiro, RJ, Brazil Received 26 March 2002; accepted 21 November 2002

Abstract The macrofauna (endo- and epi-biotic) associated to the sponge Mycale (Carmia) microsigmatosa Arndt, 1927 was studied at three sites in Rio de Janeiro State, Brazil (Arraial do Cabo, Nitero´i, and Rio de Janeiro). A total of 2235 individuals (over 1 mm long) of 75 invertebrate species were found associated to 19 specimens of the sponge. The most abundant and diverse taxa were the crustaceans (83%, 31 spp.), polychetes (10%, 18 spp.), and molluscs (3.7%, 15 spp.). Cnidarians, platyhelminthes, ascidians, echinoderms, pycnogonids, bryozoans, and sponges were also represented. Amphipod crustaceans were the dominant group, comprising 61% of all individuals collected. Species richness and abundance of associated fauna were highly correlated with sponge volume, but diversity and evenness were not. The site of collection influenced the species composition of the fauna associated to M. microsigmatosa but did not change significantly its diversity, abundance, richness, and dominance patterns of higher taxa. Pregnant females and juvenile stages of 29% of the species associated, including crustaceans, molluscs, echinoderms, and pycnogonids were frequently found inside M. microsigmatosa. Although many of these organisms do occur and reproduce in other habitats outside the sponge as well, M. microsigmatosa is also important for their reproduction and survivorship, thus contributing for the maintenance of biodiversity in Southwestern Atlantic sublittoral rocky shores. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: Mycale; associated fauna; sponge; Poecilosclerida; ecology; SW Atlantic

1. Introduction Endobiosis is a common phenomenon in marine invertebrates, particularly in sponges (Saffo, 1992). Sponges are inhabited by a wide variety of organisms, most of which find shelter and food in their canal system. The fauna associated with sponges can be so rich that they have been called Ôliving hotelsÕ (Pearse, 1932, 1950), and they are considered one of the richest marine benthic biotopes after coral reefs (Bacescu, 1971). The relationships between sponges and their endobionts are of several types, including accidental or

* Corresponding author. E-mail address: [email protected] (G. Muricy). 0272-7714/03/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0272-7714(02)00425-0

intentional comensalism, predation, competition for space, mutualism, and parasitism (Long, 1968; Martin & Britayev, 1998). The fauna associated with at least 65 sponge species has been already studied, mostly in the North Atlantic (Frith, 1976; Klitgaard, 1998), Mediterranean (Koukouras, Russo, Voultsiadou-Koukoura, Dounas, & Chintiroglou, 1992; Koukouras, Voultsiadou-Koukoura, Chintiroglou, & Dounas, 1985), and Caribbean (Pearse, 1932, 1950; Villamizar & Laughlin, 1991; Westinga & Hoetjes, 1981), but also in other regions such as the Eastern Pacific (Long, 1968) and the Antarctic (Kunzmann, 1996). In the Southwestern Atlantic, the fauna of only two sponge species has been studied so far: Hymeniacidon sanguinea Grant, 1827 in Mar del Plata, Argentina (Cuartas & Excoffon, 1993), and Mycale (Aegogropila) angulosa Duchassaing and Michelotti, 1864 in Sa˜o Paulo state, Brazil (Duarte & Nalesso, 1996, as Zygomycale parishii Bowerbank, 1875).

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Several factors such as the size of the sponge (Frith, 1976; Pearse, 1932), internal and external morphology (Klitgaard, 1998; Koukouras et al., 1985), tissue texture (Kunzmann, 1996), habitat (Pearse, 1950), and depth of collection (Pearse, 1950; Peattie & Hoare, 1981) are known to influence the composition of the fauna associated with sponges. Seasonal fluctuations seem not to change the dominance of taxonomic groups, although it may influence the number of associated individuals (Cuartas & Excoffon, 1993; Duarte & Nalesso, 1996). The effect of geographic location on the composition of the associated fauna was non-significant in the Caribbean sponge Spheciospongia vesparia Lamarck, 1814 (cf. Westinga & Hoetjes, 1981), and was not tested statistically in Brazilian Mycale angulosa (Duarte & Nalesso, 1996). The goal of this study was to describe the species composition and the abundance of the fauna associated with the common Western Atlantic demosponge Mycale (Carmia) microsigmatosa Arndt, 1927 in three different sites in Rio de Janeiro state, SE Brazil. This species is highly abundant and widely distributed in the Central and SW Atlantic (Hadju & Boury-Esnault, 1991; Soest, 1984), it is tolerant to pollution (Muricy, 1989), and its associated fauna has never been studied before. We aimed at testing the influence of sponge volume and collection site on species diversity, evenness, richness, abundance, and composition of the macrofauna associated to M. microsigmatosa in the SW Atlantic.

2. Materials and methods Mycale microsigmatosa is a red encrusting sponge, usually less than 5 mm thick but some massive specimens up to 40 mm thick, with oscules and canals up to 5 mm in diameter. The species is well characterized by its spiculation of subtylostyles, sigmas, and rare anisochelae, all in a single size category (Hadju & BouryEsnault, 1991; van Soest, 1984). Sponge samples were collected in three localities in Rio de Janeiro state, SE Brazil: Rio de Janeiro, Nitero´i, and Arraial do Cabo (Fig. 1). Praia Vermelha, in Rio de Janeiro (22 579S– 43 099W; Fig. 1(A)), is a small (100 m long), sheltered beach delimited by shallow rocky shores, under strong influence of the polluted waters of Guanabara Bay. This pollution includes large quantities of domestic wastes, oil, and heavy metals (Bidone & Lacerda, 2002). Itaipu Beach in Nitero´i (22 589S–43 049W; Fig. 1(B)) is located 40 km east from Praia Vermelha. It is also sheltered and shallow, but it suffers less influence from the polluted Guanabara Bay than Praia Vermelha. Arraial do Cabo (23 599S, 42 009W) is located 170 km east from Rio de Janeiro. All three collection sites in Arraial do Cabo (Forno Beach, Pedra Vermelha and Island Beach; Fig. 1(C–E)) are sheltered, shallow and unpolluted. Arraial do Cabo is under strong influence of cold, nutrient-rich

upwelling waters (Valentin, 1984), and has a rich benthic fauna. Nineteen individuals of Mycale microsigmatosa were collected through free and scuba diving (1–5 m depth) from February to July 1999. Before collection, the sponges were covered with a plastic bag to avoid escape of the fast-moving associates (mainly crustaceans). The seawater in the bags was filtered in a sieve with a mesh size of 1 mm, and the sponges with their associated fauna were fixed in 70% ethanol. In the laboratory, the sponges were macerated carefully under a stereomicroscope to remove the associated organisms. Identification of sponge associates was made with the help of specialists and through comparison with the relevant literature (Amaral & Nonato, 1996; Barnard & Karaman, 1991; Melo, 1999; Rios, 1994). Voucher specimens were deposited in the collections of Museu Nacional, in Rio de Janeiro. The volume of each sponge sample was measured by fluid displacement. For each sponge we recorded the number of associated individuals of each species and calculated Shannon–Wiener diversity H9 and Pielou’s evenness J (Ludwig & Reynolds, 1988). Correlations between sponge volume and number of individuals, number of species, diversity, and evenness of the associated macrofauna were calculated with STATISTICAä software (http://www.statsoft.com), using Pearson’s correlation coefficient (Ludwig & Reynolds, 1988). One-way ANOVA was used to compare the mean number of species, number of individuals, diversity, and evenness among the three sites. All variables were divided by the volume of the sponges in ml, and the data were tested for normality and heteroscedasity prior to ANOVA. An overall comparison of the family-level composition of the associated fauna among sponge individuals was made through cluster analysis using Bray–Curtis dissimilarity index with the proportional weights method (WPGMA). Only families with a density greater than 0.1 ind. ml1 were used in this analysis.

3. Results 3.1. Associated macrofauna The macrofauna associated to 19 specimens of Mycale microsigmatosa in Rio de Janeiro state was moderately diverse, with 75 species representing nine invertebrate phyla (Table 1). The crustaceans were the most diverse group with 31 spp., followed by polychetes with 18, and molluscs with 15 spp. (Table 1). Species diversity and evenness of all 19 samples together irrespectively of collection site were H9 ¼ 3:0 and J ¼ 0:7. A total of 2235 individuals over 1 mm long was found associated to Mycale microsigmatosa. The most abundant taxa were the crustaceans (83% of the individuals), polychetes (10%), and molluscs (3.7%). Cnidarians,

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Fig. 1. Location of the collection sites in Rio de Janeiro State: (A) Praia Vermelha, (B) Itaipu´ Beach, (C) Forno Beach, (D) Pedra Vermelha, and (E) Island Beach.

platyhelminthes, ascidians, echinoderms, pycnogonids, bryozoans, and sponges were also represented (all below 1%, 1–3 species each). Amphipod crustaceans were the single dominant group, comprising 61% of all associates individuals. 3.2. Correlations with sponge volume Species diversity (H9) and evenness (J) were only slightly correlated with sponge volume (evenness negatively correlated), and both correlations had low levels of significance (respectively r ¼ 0:52, p ¼ 0:02310 and r ¼ 0:41, p ¼ 0:08118; Fig. 2A, B). In contrast, the number of associated species (r ¼ 0:80, p ¼ 0:00008; Fig. 2C) and of associated individuals (r ¼ 0:84, p ¼ 0:00001; Fig. 2D) were both highly correlated with sponge volume, and with high significance levels.

3.3. Influence of collection site When summed up for all samples from each site, the associates of sponges collected in Nitero´i had the largest number of individuals associated (1363 in five sponges), and those collected in Rio de Janeiro had slightly higher

Shannon’s diversity ðH9 ¼ 3:0Þ, evenness ðJ ¼ 0:8Þ, and number of species (50) of the three sites. The sponges from Rio de Janeiro were however, generally bigger than those from the other two sites. Since it was demonstrated that the volume has a moderate to high influence in all these variables (Fig. 2), particularly in the number of species and number of individuals, we averaged each variable per volume of sponge (in ml) per specimen. The differences in diversity, evenness, richness, and abundance among the three sites were then non-significant at p < 0:05 (Table 2; Fig. 3). The dominance (in number of individuals) and the number of species of the major taxonomic groups showed no significant variation; in all three sites the crustaceans were the dominant and most diverse group, followed by polychetes and molluscs (Table 3; Fig. 4(A)). The other groups were much less diverse (0–3 species). Among the crustaceans, amphipods dominated in Nitero´i and Rio de Janeiro, and barnacles were dominant in Arraial do Cabo (Fig. 4(B)). Cluster analysis of family-level composition of the 19 samples of Mycale microsigmatosa (Fig. 5) showed three major groups: group A is a heterogeneous group with sponges from Arraial do Cabo and Rio de Janeiro, characterized by the abundance of syllid polychetes; group B is formed by all sponges from Nitero´i plus one

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Table 1 Density and frequency of the invertebrates associated to M. microsigmatosa Taxon Crustacea Cirripedia

Amphipoda

Isopoda

Tanaidacea Decapoda

Species Balanus trigonus Darwin, 1854 Megabalanus coccopoma Darwin, 1854 Amphilocus neapolitanus Della Vale, 1893 Ampithoe kava Myers, 1985 Ampithoe ramondi Audoin, 1826a Ampithoe sp. Aora sp. Aoridae sp. Audulla sp. Caprellidae sp.a Corophium sp. Elasmopus pectenicrus Bate, 1862 Ericthonius brasiliensis Dana, 1853 Gamaropsis sp. Hyale nigra Haswell, 1879 Isaeidae sp. Jassa sp. Leucothoe sp. Leucothoe spinicarpa Abildgaard, 1789 Photis longicaudata Bate and Westwood, 1862 Podocerus brasiliensis Dana, 1853a Podocerus fissipes Serejo, 1998a Anthuridae sp.a Joeropsis sp. Paranthura sp. Sphaeromatidae sp. Unidentifieda,b Alpheidae sp.a Diogenidae sp. Porcellanidae sp.b Xantiidae sp.a

Density (ind. l1)

Taxon

Frequency (%)

32 01

47.37 5.26

<01

5.26

<01 20

5.26 31.58

01 <01 11 <01 05 04 65

10.53 5.26 21.05 5.26 31.58 36.84 57.89

63

36.84

18 01 09 03 49 26

15.79 10.53 10.53 10.53 31.58 56.84

02

10.53

27

52.63

18

42.10

11 08 01 01 138 12 <01 12 13

31.58 42.11 5.26 5.26 84.21 42.11 5.26 36.84 52.63

06 <01 01

21.05 5.26 5.26

01

5.26

Polychaeta Cirratulidae sp. Cirriformia sp. Eunice australis Quatretages, 1865 Halosydnella brasiliensis Kinberg, 1858 Hydroides norvegica Gunnerus, 1768 Hydroides sp. ?Marphysa sp. Nereididae sp. Perinereis anderssoni Kinberg, 1866 Pista sp. Polydora sp. Polydora spongicola Berkeley and Berkeley, 1950 Polynoidae sp. Sabella sp.

Table 1 (continued )

Mollusca Gastropoda

Bivalvia

Cnidaria Anthozoa Hydrozoa

5.26

01 <01 02 <01

10.53 5.26 21.05 5.26

<01 <01 20

5.26 10.53 21.05

<01 03

5.26 15.79

Density (ind. l1)

Frequency (%)

Sabellidae sp. Spionidae sp. Syllidae sp. Typosyllis sp.

<01 04 34 20

5.26 15.79 73.68 21.05

02 02

10.53 26.32

<01 01

5.26 5.26

<01 <01

5.26 5.26

10

57.89

<01 07 <01 <01

5.26 26.32 5.26 5.26

<01 01

10.53 10.53

08 01

42.11 10.53

04 01

21.05 5.26

<01

5.26

<01

5.26

03

10.53

01 <01

10.53 5.26

02

15.79

02

15.79

03

21.05

05

36.84

Bitium varium Pfeiffer, 1840 Crepidula aculeata Gmelin, 1791b Fissurellidae sp.b Parviturboides interruptus Adams, 1850 Pyramidellidae sp. Hiatella arctica Linnaeus, 1767b Isognomum alatus Gmelin, 1791b Limidae sp. Modiolus sp.b Mytilidae sp. Mytilus edulis Linnaeus, 1758b Ostrea sp.b Papyridea soleniformis Bruguie`re, 1789b Perna perna Linnaeus, 1758b Pinctada imbricata Ro¨ding, 1798b Unidentified Clytia hemisphaerica Linnaeus, 1767 ?Nemalecium sp.

Echinodermata Ophiuroidea Amphiolis squamata Delle Chiaje, 1828b Ophiactis savigny Mu¨ller and Troschel, 1842b Porifera Calcarea Leucilla sp. Leucosolenia sp. Pycnogonida Unidentifieda Bryozoa Unidentified Ascidiascea Unidentified Platyhelminthes Unidentified a b

<01

Species

Including pregnant females. Including juveniles.

specimen from Rio de Janeiro, dominated by podocerid amphipods; and group C has four samples from Arraial do Cabo, which was the site geographically more distant from the others. Group C was characterized mainly by the abundance of balanid cirripedians. Twenty-two out of 75 associated species (29.3%) were found incubating eggs or embryos or in juvenile stages. This included 10 species of molluscs, nine crustaceans, two echinoderms, and one pycnogonid (Table 1).

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Fig. 2. Correlation between sponge volume (in ml) and (A) diversity, (B) evenness, (C) number of species, and (D) number of individuals of the fauna associated to Mycale microsigmatosa.

4. Discussion 4.1. Composition of the associated macrofauna Mycale microsigmatosa has a moderately rich associated macrofauna in Rio de Janeiro state (75 spp. belonging to nine invertebrate phyla). If organisms smaller than 1 mm were considered, the number of species associated would increase through the inclusion of several species of copepods, ostracods, and foraminiferans. Some sponges have a very poor associated macrofauna, whereas others harbor a rich fauna. One specimen of Aulospongus schoemus de Laubenfels, 1936 harbored only three associated individuals, a crab and two annelids (Pearse, 1950). Mycale angulosa from Sa˜o Paulo state, Brazil harbored 92 spp. in 25 samples (Duarte & Nalesso, 1996). Aplysina lacunosa Pallas, 1766 from the Caribbean was colonized by 139 associated species larger than 0.5 mm in 100 samples (Villamizar & Laughlin, 1991). Crustaceans are the single dominant taxa in most sponge species, but in a few cases they were not among the three dominant groups (e.g. in Geodia barretti, Stryphnus ponderosus, and Phakelia robusta from Faroe Islands; Klitgaard, 1998). This discrepancy may be due to differences in collection methods, since the dredging used by Klitgaard (1998), contrary to the collection with scuba diving and plastic bags more commonly used, allows the escape of the most mobile associated animals, especially the crustaceans. Among the crustaceans, the amphipods

dominated in M. microsigmatosa. Amphipods were also abundant in the partially sympatric (in Arraial do Cabo) sponge Dysidea robusta Vilanova and Muricy, 2001 (Serejo, 1998, as Dysidea fragilis). Alpheideans are more often dominant in other sponges (Koukouras et al., 1992; Westinga & Hoetjes, 1981); they were frequent but not abundant in M. microsigmatosa. Polychetes are usually one of the three dominant taxa in sponges—most often second or third. Molluscs dominate more rarely (e.g. in Ircinia variabilis Schmidt, 1864 and Spongia officinalis from Greece (Koukouras et al., 1992, 1985). Taxa with lower abundance such as plathyhelminthes, pycnogonids, sponges, ascidians, and bryozoans are usually poorly represented in other sponges too. Cnidarians and echinoderms, uncommon in Mycale microsigmatosa, can dominate in other poecilosclerids (Bakus, 1966; Duarte & Nalesso, 1996). The Table 2 Summary of ANOVA comparing the diversity, evenness, number of species, and number of individuals (meanstandard deviation) of the associated fauna of Mycale microsigmatosa in three sites in Rio de Janeiro state Parameter

AC

Diversity Evenness Number of species Number of individuals

0.894  1.23 0.139  0.13 3.968  5.44

NT

RJ

F

p-Level

0.202  0.15 0.208  0.22 1.77 0.2 0.067  0.06 0.345  0.52 1.96 0.17 1.614  0.69 1.427  1.13 1.15 0.34

9.681  12.27 11.586  4.02 4.799  2.84 1.20 0.32

AC, Arraial do Cabo; NT, Nitero´i; RJ, Rio de Janeiro.

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Fig. 3. Variation of: (A) diversity, (B) evenness, (C) number of species, and (D) number of individuals of the fauna associated to Mycale microsigmatosa in three sites in Rio de Janeiro state. AC, Arraial do Cabo; RJ, Rio de Janeiro; NT, Nitero´i. All variables were calculated for each sponge and divided by its volume in ml.

dominance of ophiuroids in the congeneric species Mycale angulosa from an adjacent area (Sa˜o Paulo state, Brazil; Duarte & Nalesso, 1996) suggests that the taxonomic composition of the associated fauna is rather species-specific, and not related to the taxonomic affinity of the sponges.

associated macrofauna are positively correlated with sponge volume, there are some exceptions to this rule, such as Ircinia fasciculata Pallas, 1766, Petrosia ficiformis Poirel, 1789, and Agelas oroides Schmidt, 1864 in Greece (Koukouras et al., 1985). 4.3. Influence of collection site

4.2. Correlations with sponge volume The internal space of the sponges, represented by their canal system and often reflected by their total volume, is an important factor for their occupation by associated organisms (Bakus, 1966; Duarte & Nalesso, 1996; Pansini, 1970). Total sponge volume is often positively correlated with both species richness and abundance of the associated macrofauna, as in Mycale microsigmatosa, M. angulosa (Duarte & Nalesso, 1996), and Spheciospongia vesparia (Westinga & Hoetjes, 1981). In S. vesparia this correlation only happened in sponges smaller than 1 l; over that volume the associated fauna remained constant (Westinga & Hoetjes, 1981). In contrast to S. vesparia, M. microsigmatosa is usually encrusting, and the samples studied here were always smaller than 100 ml; their diversity, richness, and abundance were not established up to this size. Although it is to be expected that both diversity and abundance of the

In general, the dominance of the different taxonomic groups was not influenced by the collection site, at least Table 3 Number of species associated to Mycale microsigmatosa per taxon and total in three sites on Rio de Janeiro state coast Taxon

NT

RJ

AC

Ascidiacea Bryozoa Cnidaria Crustacea Echinodermata Mollusca Plathyelminthes Polycheta Porifera Pycnogonida

3 1 1 14 0 7 1 7 2 0

2 1 2 23 1 10 1 8 1 1

0 2 1 12 2 6 0 5 0 1

Total

36

50

29

RJ, Rio de Janeiro; NT, Nitero´i; AC, Arraial do Cabo.

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Fig. 4. Composition (in number of individuals) of the macrofauna associated to Mycale microsigmatosa in Rio de Janeiro state. (A) Total fauna. (B) Crustacean fauna. Crust, crustaceans; Poly, polychetes; Moll, molluscs; Pycno, pycnogonids; Cnid, cnidarians; Plathy, plathyhelminthes; ÔOthersÕ include bryozoans, cnidarians, ascidians, echinoderms, pycnogonids, and sponges. Amphi, amphipods; Cirrip, cirripedians; Decap, decapods; Isop, isopods; Tanaid, tanaidaceans.

in the scale of 200–500 km: in Mycale microsigmatosa the crustaceans always dominated, followed by polychetes and molluscs. Among the crustaceans, amphipods dominated in Nitero´i and Rio de Janeiro, whereas barnacles were dominant in Arraial do Cabo. The abundance, diversity, richness, and composition of associated spe-

cies did not vary significantly among collection sites in our study. Variation in the composition of the associated fauna among collection sites was also non-significant in the Caribbean sponge Spheciospongia vesparia (Westinga & Hoetjes, 1981). Some variation in a similar scale in both species composition and diversity was

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Fig. 5. Cluster analysis of similarity among samples of Mycale microsigmatosa based on the family-level quantitative composition of the associated fauna, using Bray–Curtis distance with the proportional weights method (WPGMA). AC, Arraial do Cabo; NT, Nitero´i; RJ, Rio de Janeiro. A, B, and C are the major groups recognized (see text).

found in M. angulosa from Sa˜o Paulo state (Duarte & Nalesso, 1996), but its significance was not tested statistically.

parts. Their color may also vary according to that of the host (Ortiz, 1975). Leucothoe spinicarpa is considered a parasite of sponges (Connes, 1967; Ortiz, 1975). Caprellids and pycnogonids have been found eating directly on the sponge surface (Cuartas & Excoffon, 1993). Many associates were found incubating eggs and embryos or in juvenile stages (Table 1), indicating that Mycale microsigmatosa is a breeding ground for these species. Although there is no information available about the reproduction of some of these associates (e.g. Amphitae ramondi, Podocerus fissipes), and many of the remaining forms were not identified to species, it is clear that at least some of the associates also reproduce in other habitats outside M. microsigmatosa. Juveniles of Podocerus brasiliensis and Mytilus edulis were found associated respectively to Perna perna (cf. Jacobi, 1987) and algae (Seed, 1969). Juveniles of Hiatella arctica and Crepidula aculeata were found associated to the calcareous algae Amphiroa beauvoisii Lamouroux, 1816 in Sa˜o Paulo state (cf. Masunari, 1982). M. microsigmatosa is therefore not essential for the reproduction of these organisms. Nevertheless, the species is important for the maintenance of the biodiversity of the benthic community in SW Atlantic rocky shores, not only by harboring adults of 75 spp. of invertebrates, but also by providing another safe environment for their reproduction.

4.4. Nature of the association Most organisms associated to sponges are accidental epi- and endo-bionts, having no specificity to their hosts. Bivalves such as Mytilus edulis and Perna perna and the ophiuroid Ophiactis savigny are very common in Brazilian rocky shores. The amphipod Erichtonius brasiliensis is common in other sponges, corals, ascidians, and calcareous algae (Masunari, 1982; Moreno, 1998; Serejo, 1998; Wendt, Van Dolah, & O’Rourke, 1985). Photis longicaudata is also found in ceriantharians (Moore & Cameron, 1999). Leucothoe spinicarpa was found associated to polychetes, algae, bivalves, and ascidians (Lewis, 1987; Nalesso, Duarte, Pierozzi, & Enumo, 1995; Thiel, 1999). Other amphipods and alpheideans however, show a clear preference for sponges (Ortiz, 1975; Peattie & Hoare, 1981; Serejo, 1998). Some amphipods are chemically attracted to the sponge Halichondria panicea Pallas, 1766 (Peattie & Hoare, 1981). Many alpheideans and polychetes are considered obligatory endobionts of sponges (Koukouras et al., 1985; Martin & Britayev, 1998). Sponges offer to potential associates food from their internal currents or from their own tissue, and protection against wave action and predation (Frith, 1976; Green, 1977). The amphipods from the families Amphilochidae, Stenothoidae, and Leucothoidae found in Mycale microsigmatosa have adaptations to life inside the sponge aquiferous system such as smooth, elongate body with rounded extremities, and modified mouth

Acknowledgements We thank Thaı´ s Hokoc¸ and Renato Ventura (Echinodermata), Cristiana Serejo (Amphipoda), Carla Barros (Isopoda), Paulo S. Young (Cirripedia and Decapoda), Norma Salgado and Ju´lio Ce´sar Monteiro (Mollusca), Michelle Klautau (Porifera, Calcarea) (all from Universidade Federal do Rio de Janeiro), and A´lvaro Migotto (Hydrozoa—Universidade de Sa˜o Paulo) for help in the identification of the associated fauna. This work was supported by grants and fellowships from Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq) and Fundac¸a˜o Carlos Chagas Filho de Amparo a` Pesquisa do Estado do Rio de Janeiro (FAPERJ). References Amaral, A. C. Z., & Nonato, E. F. (1996). Annelida polychaeta— Caracterı´sticas, glossa´rio e chaves para famı´lias e geˆneros da costa brasileira (194 pp.). Campinas: Editora da Universidade Estadual de Campinas. Bacescu, M. (1971). Les Spongiaires: un des plus inte´ressants biotopes benthiques marins. Rapports de la Commission International de la Mer Me´diterrane´e 20, 239–241. Bakus, G. L. (1966). Marine poeciloscleridan sponges of the San Juan Archipelago, Washington. Journal of Zoology 149, 415–531. Barnard, J. L., & Karaman, G. S. (1991). The families and genera of marine gammaridean Amphipoda. Parts 1 and 2. Records of the Australian Museum 13, 1–866.

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