Patterns of sponge distribution in Cagarras Archipelago, Rio de Janeiro, Brazil

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1 J. Mar. Biol. Ass. U.K. (2004), 84,681^687 Printed in the United Kingdom Patterns of sponge distribution in Cagarras Archipelago, Rio de Janeiro, Brazil Leandro C. Monteiro and Guilherme Muricy Departamento de InvertebradosöMuseu Nacional/UFRJ, Quinta da BoaVista s/no, Sa ocristo va o, Rio dejaneiro, Brazil. s: and The structure and distribution of the sponge community in ve sites and four habitats in Cagarras Archipelago, Rio de Janeiro, Brazil, are described. The archipelago has three major islands (Cagarra, Palmas, and Comprida), and four islets. Qualitative samples were taken by SCUBA diving in the three islands and in two islets, and quantitative samples were taken in Palmas Island only. Cluster analysis using Jaccard s coe cient on qualitative data grouped the two islets (Cagarra Bank and Cagarra Islet), which are more exposed to wave action, and the three islands formed a group of relatively sheltered sites. Cluster analysis using Bray^Curtis coe cient on quantitative data from di erent habitats in Palmas Island allowed distinction of three groups of samples: overhangs, shallow horizontal surfaces (6 m depth), and vertical walls plus deeper horizontal surfaces (17 m depth). Sponge abundance was greater in overhangs (61.2 ind m 2 ), which were dominated by Protosuberites sp. and Clathrina conifera. Abundance was reduced in vertical walls (31.1ind m 2 ) and deep horizontal surfaces (16.8 ind m 2 ). Pachychalina sp. dominated the deep horizontal surfaces and Clathrina conifera was dominant in overhangs. Values of Shannon s diversity in overhangs, vertical walls (both with H 0 ¼2.1bits ind 1 ) and deep horizontal surfaces (H 0 ¼1.7 bits ind 1 ) were moderate and similar, whereas in shallow horizontal surfaces the sponges were both less diverse (H 0 ¼0.37) and less abundant (8.5 ind m 2 ). Shallow horizontal surfaces were dominated by Hymeniacidon heliophila. The reduced species richness of the sponge community in Cagarras Archipelago when compared with other sites in Brazil and elsewhere is probably due in part to the pollution from the city of Rio de Janeiro. Wave action appears to reduce the number of sponge species at a local scale, whereas substrate inclination a ects more strongly the species composition and abundance than the diversity of sponges. INTRODUCTION Sponges are among the most important components of benthic communities in several marine environments, with wide distribution in both time and space. Due to their abundance, diversity, multiple ecological roles, and sensitivity to variations in water quality, sponges should be a major group of interest in studies of ecological biomonitoring in coral reefs and rocky shores (Alcolado & Herrera, 1987; Muricy, 1989, 1991; Muricy et al., 1991; Diaz & Ru«tzler, 2001). The distribution of sponge species is largely related to physical factors such as light, temperature, hydrodynamism, and sedimentation. Few studies however have compared the structure and composition of sponge communities in di erent habitats (e.g. Boury- Esnault, 1971; Zea, 1993); they showed signi cant di erences between shaded (vertical walls and overhangs) and exposed horizontal surfaces. Sponge communities in the Caribbean are highly diverse and abundant (Alcolado & Herrera, 1987; Alcolado, 1994; Alvarez et al., 1990; Diaz et al., 1990; Zea, 1993). In Brazil, only two studies have so far described quantitatively the structure of sponge communities, in Arraial do Cabo (Muricy, 1989) and Atol das Rocas (Moraes et al., 2003). The aim of this study was to describe qualitatively and quantitatively the structure of the sponge community of the Cagarras Archipelago in Rio de Janeiro, Brazil, and to analyse the distribution of the species within di erent islands and habitats. Our goals were to demonstrate some basic principles of sponge distribution on a local scale, and to generate data for future biomonitoring of the archipelago, which has been recently proposed to be designated as a Marine Protected Area by the Brazilian environmental agency (IBAMA). MATERIALS AND METHODS Study area Cagarras Archipelago is located 5 km south of Ipanema Beach, Rio de Janeiro, south-eastern Brazil ( W S), and occupies an area of 2 km 2. It is an important area for sheries and tourism, and is subjected to upwelling of cold waters during summer. The water quality is relatively poor due to the waste waters of Rio de Janeiro city disposed nearby. The archipelago is composed of three major islands, namely, Palmas, Comprida and Cagarra, and four islets. Sampling sites Site 1: Palmas Island, south shore: this is the island closest to the shoreline. The average inclination of the rocky shore is approximately 458, and small caves are common. Maximum depth of rocky substrates is 22 m,

2 682 L.C. Monteiro and G. Muricy Sponge distribution in Cagarras Archipelago Table 1. Presence (+) and absence (7) of sponges in ve islands of Cagarras Archipelago, Rio de Janeiro, south-eastern Brazil. Species Palmas Island Comprida Island Cagarra Island Cagarra Bank Cagarra Islet Aplysilla rosea (Barrois, 1876) Callyspongia sp Chondrilla a. nucula Schimdt, Chondrosia sp Clathria sp Clathrina aurea Sole -Cava et al., Clathrina conifera Klautau & Borojevic, Cliona a. celata Grant, Darwinella sp Dragmacidon reticulatus (Ridley & Dendy, 1886) Dysidea etheria (de Laubenfels, 1936) Euryspongia rosea de Laubenfels, Geodia corticostylifera Hajdu et al., Guitarra sepia Lerner et al., Haliclona (Reniera) sp Hemimycale sp Hymedesmia sp Hymeniacidon heliophila (Parker, 1910) Mycale microsigmatosa Arndt, Oceanapia nodosa (George & Wilson, 1919) Pachychalina sp Paraleucilla sp Petromica citrina Muricy et al., Polymastia janeirensis (Boury-Esnault, 1973) Protosuberites sp Scopalina ruetzleri (Wiedenmayer, 1977) Suberites sp Tedania ignis (Duchassaing & Michelotti, 1864) Terpios fugax Duchassaing & Michelotti, Timea sp Total with sandy substrates below that depth. The south shore is exposed only to strong swell from the south-west in storms. Site 2: Comprida Island, north shore: located approximately 500 m south of Palmas Island, its shores are very similar to those of that island with the exception that caves are more rare and it is sheltered from direct wave impact. Maximum depth sampled 20 m. Site 3: Cagarra Island, north shore: the shore is characterized by a relatively sheltered, very smooth vertical rocky wall and horizontal surfaces at 23 m depth; caves are absent. Site 4: Cagarra Bank, north-eastern shore: this is the sampling site furthest from the coast, and it is very exposed to wave action. The rocky shore is made of large rocks, and small caves are common. Maximum depth 20 m. Site 5: Cagarra Islet, north-eastern shore: located immediately south of Cagarra Island, forming with it a canal with intense currents, it is also subjected to strong wave action. Small caves are common. Maximum depth 16 m. Qualitative sampling Visual censuses were made by SCUBA diving in Palmas Island, Cagarra Island, Comprida Island, and Cagarras Bank in January^February 2001, and in Cagarra Islet in February Each census was composed of a single 50 min dive by three divers, who noted every species observed. Whenever there was any doubt about the identity of a sponge it was collected for identi cation in the laboratory. Before collection, specimens were photographed in situ with a Nikonos-V camera. The specimens collected were xed and preserved in alcohol 70%, and deposited in the Porifera collection of the Museu Nacional, Universidade Federal do Rio de Janeiro (MNRJ). Quantitative sampling Quanti cation of the sponge community was made by SCUBA diving in Site 1 (Palmas Island) in January ^ February Four di erent habitats were distinguished and sampled separately: shallow horizontal surfaces (inclination 0^308, 6 m depth); deep horizontal surfaces (17 m depth); vertical walls (inclination 70^1108) 6^17 m depth; and roofs of small caves (overhangs, inclination 1508^1808) 6^17 m depth. The number of specimens of each species was counted in quadrats of 0.25 m 2. The number of quadrats in each habitat was determined by a species ^area curve and varied from 8^15, summing up 51 quadrats. Quadrat placement in shallow and deep horizontal surfaces was determined through random points marked in a 10 m transect parallel to the shore. In vertical and overhang habitats, quadrat placement was determined by swimming

3 Sponge distribution in Cagarras Archipelago L.C. Monteiro and G. Muricy 683 Table 2. Abundance (mean individuals m 2 ) of each species and community parameters of sponges in four habitats in Palmas Island, Cagarras Archipelago. Species Shallow horizontal (6 m) Deep horizontal (17 m) Vertical walls (6^17 m) Overhangs (6^17 m) Aplysilla rosea (Barrois, 1876) ^ 0.1 ^ Chondrosia sp. ^ ^ ^ 2.4 Clathria sp. ^ ^ Clathrina aurea Sole -Cava et al., 1991 ^ Clathrina conifera Klautau & Borojevic, 2001 ^ Cliona a. celata Grant, 1926 ^ ^ Darwinella sp. ^ ^ Dysidea etheria (de Laubenfels, 1936) ^ ^ ^ 1.1 Guitarra sepia Lerner et al., 2003 ^ ^ Haliclona (Halichoclona) sp. ^ ^ ^ 0.4 Haliclona (Haliclona) sp. ^ ^ 0.4 ^ Haliclona (Reniera) sp.1 ^ ^ Haliclona (Reniera) sp.2 ^ ^ 0.6 ^ Haliclona (Reniera) sp.3 ^ ^ ^ 0.5 Haliclona (Soestella) sp. ^ ^ ^ 1.8 Hemymicale sp. ^ Hymedesmia sp. ^ ^ 2.2 ^ Hymeniacidon heliophila (Parker, 1910) ^ Hymeniacidon sp. ^ 0.1 ^ ^ Monanchora arbuscula (Duchassaing & Michelotti, 1864) ^ ^ 0.1 ^ Mycale microsigmatosa Arndt, Mycale sp. ^ ^ ^ 0.5 Oceanapia nodosa (George & Wilson, 1919) ^ ^ Pachychalina sp. ^ Paraleucilla sp Protosuberites sp. ^ ^ Scopalina ruetzleri (Wiedenmayer, 1977) ^ ^ ^ 1.1 Suberites sp. ^ 0.3 ^ ^ Sycon sp. ^ 0.1 ^ ^ Tedania ignis (Duchassaing & Michelotti, 1864) ^ ^ Terpios fugax Duchassaing & Michelotti, 1864 ^ ^ Timea sp.1 ^ 0.5 ^ ^ Timea sp.2 ^ 0.2 ^ ^ Number of samples (0.25 m 2 quadrats) Total abundance (number of individuals in all quadrats) Relative abundance (ind. m 72 ) Number of species Shannon s diversity Pielou s evenness in random directions from a prede ned place in the centre of the sampled area, when an area with suitable inclination was found, the quadrat was placed in its centre. Statistical analysis The data obtained were analysed using the software Multivariate Statistical Package (MVSP; kovcomp.com). Species richness was determined in ve sites and in four habitats in Palmas Island (6 m depth horizontal surfaces, 17 m depth horizontal surfaces, vertical walls, and overhangs). In each habitat we calculated Shannon s species diversity (H 0 ¼ P p i log 2 p i ), Pielou s evenness (J¼H 0 /H 0 max), and the abundance and relative frequency of each species. Jaccard s binary coe cient of similarity was used to compare the species composition of the ve sites. The Bray^Curtis distance index was used to compare the composition of the di erent habitats in Palmas Island. The unweighted pair group method with arithmetic mean (UPGMA) was used in both cases. RESULTS Forty species of sponges were found in Cagarras Archipelago, with 30 in qualitative samples (Table1) and 33 in quantitative samples (Table 2). In Palmas Island, total Shannon s diversity and Pielou s evenness in the four habitats considered together were H 0 ¼1.67 and J¼0.67, respectively. Total sponge abundance was 32.1ind m 2. Variation between sites Species richness in the ve sites studied varied from 14 species in Cagarras Island to 23 in Palmas Island (Table 1).

4 684 L.C. Monteiro and G. Muricy Sponge distribution in Cagarras Archipelago Cluster analysis using Jaccard s coe cient on qualitative (presence/absence) data grouped the two islets (Cagarra Bank and Cagarra Islet), which are more exposed to wave action, and the three islands formed a group of sheltered sites (Figure 1). The two islets are poorer in number of species than two of the islands (Palmas and Comprida), but are slightly richer than Cagarra Island. In general, the islands have relatively conspicuous and abundant species which are absent in the islets: Clathrina aurea, Geodia corticostylifera, Petromica citrina, Polymastia janeirensis, and Oceanapia nodosa (Table 1). Most of these species are associated to overhangs (Clathrina aurea) or to the sandy/ rocky substrates interface (sensu Muricy et al., 1991; e.g. Geodia corticostylifera, Petromica citrina, Polymastia janeirensis), which are absent from the small islets. Figure 1. Cluster analysis of ve sampling sites in Cagarras Archipelago using Jaccard s similarity coe cient on binary data. Variation between habitats The species ^area curves of each habitat studied showed two general shapes: a low pro le curve in shallow horizontal surfaces (6 m depth), which quickly (1.5 m 2 ) reached a maximum of three species (Figure 2); and a high pro le curve at deep horizontal surfaces (17 m depth), vertical walls and overhangs, which reached stability only around 3 m 2 (at between 16 and 22 species; Figure 2). Among the three richest habitats, the walls had the greatest species richness (22 species; Table 2). In shallow horizontal surfaces the distribution of species abundances evidenced the low species richness Figure 2. Species^area curves of the sponge community in four habitats in Palmas Island.

5 Sponge distribution in Cagarras Archipelago L.C. Monteiro and G. Muricy 685 Figure 3. Rank-frequency diagrams of sponges from four di erent habitats in Palmas Island. Figure 4. Cluster analysis of four di erent habitats in Palmas Island using Bray^Curtis dissimilarity coe cient on quantitative (abundance) data. and high dominance of two species, Hymeniacidon heliophila (70% of the sponge specimens) and Paraleucilla sp. (25% of the specimens; Figure 3). In vertical walls the curve is smoother, and the dominant species reached only 20% of dominance (Clathrina conifera; Figure 3). In the other habitats the number of species is higher, but there was a single dominant species in deep horizontal surfaces (Pachychalina sp., 43%; Figure 3) and two dominant species in overhangs (Protosuberites sp.with 34%,and Clathrina conifera with 23%; Figure 3). The same trend is shown by Shannon s diversity: it was similar in overhangs (H 0 ¼2.12 bits ind 1 ), vertical walls (H 0 ¼2.12 bits ind 1 ) and deep horizontal surfaces (H 0 ¼1.73 bits ind 1 ), whereas in shallow horizontal surfaces the sponges were much less diverse (H 0 ¼0.37 bits ind 1 ;Table2). Sponge abundance was greater in overhangs (61.2 ind m 2 ), which were dominated by Protosuberites sp. (33% of the sponge individuals in this habitat) and Clathrina conifera (23%). Abundance was reduced in vertical walls (31.1ind m 2 ) and deep horizontal surfaces (16.8 ind m 2 ). Pachychalina sp. dominated the deep horizontal surfaces (43%), whereas Clathrina conifera dominated in the overhangs (19%; Table 2). Sponges were less abundant in shallow horizontal surfaces (8.5 ind m 2 ), which were dominated by Hymeniacidon heliophila (70%). Cluster analysis using Bray ^ Curtis coe cient on quantitative data in Palmas Island allowed distinction of three groups of samples: overhangs, shallow horizontal surfaces (6 m depth), and vertical walls plus deeper horizontal surfaces (Figure 4). DISCUSSION The sponge community of Cagarras Archipelago has intermediate to low species richness (with 40 species) and

6 686 L.C. Monteiro and G. Muricy Sponge distribution in Cagarras Archipelago diversity (H 0 ¼1.67, J¼0.67) when compared with similar areas in Brazil and elsewhere. There are some hot-spots of sponge diversity such as sub-rubble communities in Curac ao and Bonaire, with 159 and 199 species respectively (Meesters et al., 1991), or sublittoral rocky shores in Sa o Sebastia o, south-eastern Brazil, with 145 species (Hajdu et al., 1999). Most western Atlantic sponge communities, however, range from 36 to 84 species, with a minimum of 30 species in the Itacolomis Reefs, Bahia State (G. Muricy, unpublished data). Cagarras Archipelago is thus in the lowest part of this range. Shannon s diversity has been calculated in fewer sites in the Atlantic; it varies widely from H 0 ¼0.8 to 3.5 bits ind 1 (Muricy, 1989; Diaz et al., 1990; Alvarez et al., 1990; Alcolado, 1994; Moraes et al., 2003). The relative poverty of Cagarras Archipelago may be in part related to pollution. The archipelago has been subjected since 1975 to direct discharge of untreated sewage from the sewerage outfall of Ipanema, which is located approximately 1.5 km west of the archipelago; it throws an average of 5.8 m 3 of sewerage per second (Britto et al., 1978). The polluted waters of Guanabara Bay may also in uence the archipelago. This heavy organic and inorganic pollution load might reduce species diversity in the archipelago as in Cuba (Alcolado & Herrera, 1987), Arraial do Cabo (Muricy, 1989; Muricy et al., 1991), and Marseilles (Muricy, 1991). In contrast, however, organic pollution appears to increase cover and abundance of sponges in Colombia (Zea, 1994). A negative in uence of pollution in Cagarras Archipelago is also supported by the shape of the rank-frequency diagrams (Figure 2), with the typical dominance of few species, common in impacted environments (e.g. Muricy, 1991). There are, however, no data on sponge abundance in the archipelago available before this study for objective comparisons. The two adjacent areas with reduced pollution levels that could be compared with the archipelago are Arraial do Cabo to the east and Ilha Grande to the west, both of which have di erent species composition from Cagarras Archipelago (Muricy et al., 1991, and author s unpublished observations). Both areas have more sponge species than Cagarras Archipelago (more than 60 species in Arraial do Cabo; Muricy et al., 1991). The sponge faunas of Rasa and Redonda islands, located close to Cagarras Archipelago but more distant from the sewerage outfall, are still unexplored; they would probably be the best control ( clean ) areas to study the e ects of pollution in Cagarras Archipelago. Our quantitative data provide a baseline that can be used for comparison with other areas and with the same area in the future. Variation in species richness between the ve sampling sites appears to be related to two main factors, wave action and availability of cryptic substrata. Wave action is greater in the two exposed islets (Cagarras Bank and Cagarras Islet), which had low numbers of species (16 and 17 respectively). Cagarras Island, which had the lowest diversity with 14 species, is sheltered from direct wave impact, but it lacks crevices and overhangs which harbour many sponge species in the other sites. Wave action is also clearly acting to reduce the richness, diversity, and abundance of sponges in the shallow horizontal surfaces (6 m depth) when compared with the other three habitats studied. Although other factors such as competition with algae and sedimentation may also be harmful to sponges in shallow horizontal substrates, ultraviolet radiation from direct sunlight and wave action are probably more important in the reduction of their diversity. Sedimentation does not seem to be very important in a ecting sponges in Palmas Island, since deep horizontal substrates (17 m depth) are almost as rich and diverse in sponges as the vertical walls and cave ceilings, which are subjected to much less sedimentation. Although there are no measurements of sedimentation rates in Cagarras Archipelago, the long distance from the coast (5 km) reduces the in uence of terrigenous sediments on the sponge community of the islands, with the exception of the solid residues of the sewerage outfall. As in the western Mediterranean (Boury-Esnault, 1973) and the Caribbean (Zea, 1993), vertical walls were the richest and most diverse habitat. However, in Cagarras Archipelago sponge abundance increased geometrically from exposed to shaded habitats: 8.5 : 16.8 : 31.1 : 61.2 ind m 2, respectively in shallow horizontal substrates (6 m), deep horizontal surfaces (17 m), vertical walls, and cave ceilings. The composition of the sponge community was most di erent between shallow horizontal substrates and cave ceilings; conversely, there was little distinction between deep horizontal and vertical substrates (Figure 3). In vertical walls the richness is greater, probably because they are colonized by both photophilic and sciaphilic species; in overhangs the number of species is slightly reduced through the elimination of photophilic species; the abundance of some species is very high, particularly Protosuberites sp., Clathrina conifera, and Clathrina aurea. The long-term stability of the overhangs may be a factor leading to the monopolization of the substrate by these species. Due to their higher diversity and reduced in uence of physical factors (light, wave action, sedimentation), overhangs and vertical walls are the most suitable habitats for the biomonitoring of sponge communities. We thank Fernando Moraes, Eduardo Vilanova, and Eduardo Hajdu (Universidade Federal do Rio de Janeiro) for help in collections. Michelle Klautau (Universidade Federal do Rio de Janeiro) helped in the identi cation of calcareous sponges. This work was supported by grants and fellowships from Conselho Nacional de Desenvolvimento Cient co e Tecnolo gico (CNPq), Fundac a o Carlos Chagas Filho de Amparo a' Pesquisa do Estado do Rio de Janeiro (FAPERJ), and Fundac a o Universita ria Jose Bonifa cio (FUJB). REFERENCES Alcolado, P.M., General trends in coral reef sponge communities of Cuba. In Sponges in time and space (ed. R.W.M. van Soest et al.), pp. 251^255. Rotterdam: A.A. Balkema. Alcolado, P.M. & Herrera, A., Efectos de la contaminacio n sobre las comunidades de esponjas en el litoral de la Habana, Cuba. Reporte de Investigacio n del Instituto de Oceanologia de Cuba, 68,1^17. Alvarez, B., Diaz, M.C. & Laughlin, R.A., The sponge fauna on a fringing coral reef in Venezuela, I: composition, distribution, and abundance. In New perspectives in sponge biology (ed. K. Ru«tzler), pp. 358^366. Washington DC: Smithsonian Institution Press.

7 Sponge distribution in Cagarras Archipelago L.C. Monteiro and G. Muricy 687 Britto, E.R., Machado, E., Semeraro, J. & Montenegro, M.A., Monitoragem do emissa rio submarino de esgotos de Ipanema. Rio de Janeiro: SEMA/CEDAE. Boury-Esnault, N., Spongiaires de la zone rocheuse littorale de Banyuls-sur-Mer. 1öe cologie et re partition. Vie et Milieu, 22, 159^192. Diaz, M.C., Alvarez, B. & Laughlin, R.A., The sponge fauna on a fringing coral reef in Venezuela, II: community structure. Proceedings of the Third International Sponge Conference, 367^375. Diaz, M.C.& Ru«tzler, K., Sponges: an essential component of Caribbean coral reefs. Bulletin of Marine Science, 69, 535^546. Hajdu, E., Berlinck, R.G.S. & Freitas, J.C. de, Porifera. In Biodiversidade do Estado de Sa o Paulo: S ntese do Conhecimento ao Final do Se culo XX (ser. ed. C.A. Joly and C.E.M. Bicudo), vol. 3, Invertebrados Marinhos (ed. A.E. Migotto and C.G. Thiago), pp. 20^30. Sa o Paulo: Fapesp. Meesters, E., Knijn, R., Willemsen, P., Pennartz, R., Roebers, G. & Soest, R.W.M. van, Sub-rubble communities of Curac ao and Bonaire coral reefs. Coral Reefs, 10,189^197. Moraes, F.C., Vilanova, E.P. & Muricy, G., Distribuic a o das Esponjas (Porifera) na Reserva Biolo gica do Atol das Rocas, Nordeste do Brasil. Arquivos do Museu Nacional, 61,13^22. Muricy, G., Sponges as pollution-biomonitors at Arraial do Cabo, Southeastern Brazil. Revista Brasileira de Biologia, 49, 347^354. Muricy, G., Structure des peuplements de spongiaires autour de l e gout de Cortiou (Marseille, France). Vie et Milieu, 41, 205^221. Muricy, G., Hajdu, E., Custo dio, M., Klautau, M., Russo, C. & Peixinho, S., Sponge distribution at Arraial do Cabo, SE Brazil. In Proceedings of the VII Symposium on Coastal and Oceanic Management: Coastal Zone 91 (ed. O.T. Magoon et al.), pp. 1183^ Long Beach: ASCE Publications. Zea, S., Cover of sponges and other sessile organisms in rocky and coral reef habitats of Santa Marta, Colombian Caribbean Sea. CaribbeanJournal of Science, 29, 75^88. Zea, S., Patterns of coral and sponge abundance in stressed coral reefs at Santa Marta, Colombian Caribbean. In Sponges in time and space (ed. R.W.M. van Soest et al.), pp. 257^264. Rotterdam: A.A. Balkema. Submitted 12 January Accepted 3 April 2004.