Bioerosion rate of the sponge Cliona celata (Grant 1826) from reefs in turbid waters, north Bahia, Brazil

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1 Proceedings 9 th International Coral Reef Symposium, Bali, Indonesia October 2000 Bioerosion rate of the sponge Cliona celata (Grant 1826) from reefs in turbid waters, north Bahia, Brazil M. A. C. Reis 1 and Z. M. A. N. Leão 2 ABSTRACT The nearshore bank reefs along the north coast of Bahia, Brazil, are influenced by a continentally derived intense siliciclastic sediment influx and a nutrient enrichment. In order to estimate the degree of by the sponge Cliona celata (Grant 1826), massive colonies of the endemic coral Siderastrea stellata (Verrill 1868) were sampled from the intertidal shallow pools (0.2 to 0.6 m deep) of the emergent top of two isolated reefs, from the surface of a shallow reef (5 m), and of a 10 m deep reef. Five roughly hemispherical and partially living coral heads (10 to 20 cm diameter), were haphazardly collected from each zone. X-radiographs of sliced coral colonies were performed to estimate the percentage of skeleton removed and the rate of coral growth. The boring activity of Cliona celata in the studied corals coincides with that of worldwide investigated reefs from clear waters. It is slightly related with some characteristics of coral host, i.e. coral growth rate and density. Keywords Bioerosion, Clionidae, Coral reefs, Turbidity, North Bahia, Brazil Introduction Boring sponges of the family Clionidae (Gray 1867) are known for their capacity to bore into calcareous substrates such as corals, shells of mollusks and calcareous rock, and are a source of significant quantities of fine carbonate sediment, thus they exert an important influence on the erosion and recycling of accumulated calcium carbonate, particularly from coral reefs. Up to 50% - 90% of the amount of calcium carbonate lost from coral skeleton may be removed by sponge activity (MacGeachy and Stearn 1976). Studies from several reef areas, around the globe, having been showing that rates, in coral reefs, change with water depth (Goreau and Hartman 1963), the age of coral colonies (Kiene 1988), type of reef framework (Bromley 1978) and the water energy regime (MacGeachy and Stearn1976) and they are also associated with several other environmental parameters, among them, the available nutrients (Risk and MacGeachy 1978; Hallock 1988; Hallock et al. 1993), the rate of sedimentation and water turbidity (Tudhope and Risk 1985), as well as pollution (Risk and MacGeachy 1978; Hallock et al. 1993), and coral bleaching (Glynn 1997). Some of these environmental conditions are met in the studied reef area. This work focuses the rate of the endolithic clionid sponges from the Brazilian endemic coral Siderastrea stellata (Verrill 1868) on the reefs that are located along the north part of the coast of the State of Bahia, which are subjected to the influence of a continentally derived intense siliciclastic sediment influx and nutrient enrichment. This particular coral species was chosen because it is amply distributed along the coast of Brazil, and it is particularly abundant in the shallow parts of the coastal reefs. Fig1. Location of studied reef sites. TF= Praia do Forte reef top. TG= Guarajuba reef top. IT= Itacimirim 5m deep reef. GU = Guarajuba 10 m deep reef (data source Kikuchi 2001) 1 Universidade Santa Úrsula, ICBA, Rua Jornalista Orlando Dantas 59, Rio de Janeiro , Brazil. aliceusubr@apc.org.br 2 Universidade Federal da Bahia, IGEO, CPGG, Rua Caetano Moura 123, Federação, Salvador, Bahia, , Brazil. zelinda@ufba.br

2 Study sites The reef systems are situated between the beaches of Abaí and Praia do Forte, in the narrowest part (15 km average width) of the Eastern Brazilian Continental Shelf ( S and W) in a transition from siliciclastic to carbonate sediments (Leão et al. 1988) (Fig. 1). Two types of reefs were studied: emergent reefs, adjacent to the beaches, and submerged reefs that occur in the inner shelf. The emergent reefs are shallow (less than 6 m in the fore-reef zone), discontinuous, elongated and parallel to the coastline (50 m to 2 km long and 20 to 500 m wide). Their horizontal tops include a horizontal flat surface completely exposed during low tides. In this intertidal reef flat, where large dead coral heads truncated by erosion alternate with small pools and meandering channels, small colonies of living corals occur along with other reef organisms. Typical reef lagoons do not exist and the back-reef zone is adjacent to the quartz-sandy beaches. The submerged reefs, almost parallel to the coastline, are located in depths from 5 to 20 m (Nolasco and Leão 1986). Corals, millepores and coralline algae build the rigid frame of the reefs. The coral fauna has a very low diversity with numerous endemic species. The endemic coral Siderastrea stellata forms massive colonies similar to the Caribbean species, although it has larger calyces, a more delicate columella and wider interseptal spaces (Laborel 1969). Physical setting This part of the Brazilian coast has a tropical humid climate, with average air temperatures ranging between 23 C in winter and 28 C in summer (Nimer 1989). Dominant winds blows from the NE in the summer, and from the E in the winter, southeastern winds occur during winter storms. Depths around the nearshore reef area do not exceed 10 m, and the shelf edge, which lies at 15 km off the coastline, is about 70 m deep. Water temperature, measured during this study, ranged from 28 C to 30 C, salinity from 35 to 39 ppt and ph between 8.2 and 8.7. Material and methods Field survey Five roughly hemispherical and partially living coral colonies of the massive coral Siderastrea stellata (Verrill 1868), with diameters ranging from about 10 to 20 cm, were haphazardly collected from four different reef sites: the intertidal shallow pools (0.2 to 0.6 m deep) from the top of two emergent isolated reefs (Guarajuba reef top = TG, and Praia do Forte reef top = TF), the surface of a reef 5 m deep (Itacimirim reef = IT), and of a reef located at depths around 10 m (Guarajuba reef = GU) (Fig. 1). Laboratory techniques From the center of each coral colony, three serial slabs (5 mm thick) were cut parallel to the axis of maximum coral growth. From each one of these coral slabs, X- radiographs were made in order to identify all types of boring organisms and to determine the rate of coral growth. The boreholes were described from the slabs and from the X-radiographs. To quantify the boring activity, the AutoCAD R14 computer program was used. Identification of sponge species was done according to the spiculation method proposed by Rützler and Boury- Esnault (1997) and confirmed by polymorphic DNA sequences analyses. The DNA sequence was measured in the variable regions of the two Internal Transcribed Spacers (ITS-1 and ITS-2) of the eukaryotic nuclear ribosomal DNA (rdna) genes by PCR amplification, using primers based on the alignment of 18S, 5.8S and 28S conserved sequences (Mansure et al. 2000). Results Boring sponges The analyzed specimens of the coral Siderastrea stellata are significantly eroded by a diverse suite of endolithic fauna that was identified according shape, texture and size of the borings as sponges, bivalves and worms (sipunculans and polychaetes). Most boreholes occur mainly below the dead surfaces of the slabs and have, in general, no consistent preferred orientation. Sponges are the most abundant borers in the samples from three sites, being the dominant group in the Guarajuba reef top (TG, 40%), in the Praia do Forte reef top (TF, 48.7%) and in the Guarajuba 10 m deep reef (GU, 90.1%) (Fig. 2). 100% 80% 60% 40% 20% 0% TG TF IT GU Worm Bivalve Sponge Fig. 2 Relative abundance of major bioeroders detected on studied reef sites. TG=Guarajuba reef top; TF=Praia do Forte reef top; IT=Itacimirim 5 m deep reef; GU=Guarajuba 10 m deep reef. Data showed in cumulative percentages These boring sponges were identified as belonging to the cosmopolitan species Cliona celata (Grant 1826). The alpha stage of C. celata has a thickly oval shape encrusted on fragments of dead corals and coralline algae

3 with a diameter of 6 cm and height of 2 cm. The conical papillae processes attain height about 2-4 mm. In life the color is sulfur-yellow and preserved papillae present a dark brown color. The specimens carry only an unique type of spicule, tylostyles, straight or slightly curved, with a pointed end and bilobed and spherical head. Their length (263 μm 349 μm), and width (7 μm 10 μm) does not differ from the tylostyles reported in the literature. The analyses of DNA sequences revealed a closer relationship between the populations of the species of Cliona celata already identified compared to other sponge species (Cliona varians and Cliona dioryssa) (Mansure et al. 2000). The sponge borings, which penetrate to a maximum depth of 2 cm to the substrate, are small (diameter from 0.50 to 1.25 mm) with irregular camerate forms and are usually concentrated at the slab s base and periphery. Bioerosion rates Combining the amount of material removed from the coral skeleton with the age of the animal colony, gives the rate of, which in turns points to the amount of carbonate sediment produced by the macroborers. The numbers shown in table 1 indicate that the Itacimirim 5 m deep reef (IT) has the highest rate of either from all bioeroders (3.66 kg m -2 y -1 ) as well as from the boring sponges (mean 1.0 kg m -2 y -1 ). The shallow reef site ( m) of the top of the Guarajuba Reef (TG) has the second highest rate of from all bioeroder (3.33 kg m -2 y -1 ) and from the sponges (average of 0.99 kg m -2 y -1 ), followed by the also shallow ( m deep) Praia do Forte reef top (TF), with an average of total rate of 2.99 kg m -2 y -1 and of 0.98 kg m -2 y -1 from the boring sponges; the lowest rate of 1.55 kg m -2 y -1 from all bioeroders, and of 0.96 kg m -2 y -1 from the sponges is found on the Guarajuba 10 m deep reef (GU). Table 1 Rate of in the studied reef sites. TG=Guarajuba reef top; TF=Praia do Forte reef top; IT=Itacimirim 5 m deep reef; GU=Guarajuba 10 m deep reef. n=number of colonies x 3 coral slabs. Reef site Depth ( m ) Total (mean) ( kg m -2 y -1 ) TG (n=5) TF (n=5) IT (n=5) GU (n=5) Rate of sponge (range - mean) ( kg m -2 y -1 ) Discussion and conclusion Sponge In the area studied, among all identified bioeroders, sponges represent the dominant bioeroding component, with percentages ranging from 35.3% to 90.1% in the sampled sites. Such figures concur favorably with data reported from other modern reef areas (Table 2), e.g. Becker and Reaka-Kudla (1997) for the Bahamas (86.5%); Bak (1976) for Curaçao (97%); Highsmith et al. (1983) for Belize (84% %); MacGeachy and Stearn (1976) for Barbados (90%); Perry (1998) for Jamaica (81.5%); Risk and Sammarco (1982) and Sammarco and Risk (1990) for some areas of the Great Barrier Reef ( %) and Highsmith (1981) for Enewetak ( %). Within individual reef sites an increase of the relative abundance of sponge excavation becomes obvious from the shallower Praia do Forte reef ( m deep) (TF, 35.3%) to the deepest Guarajuba 10 m deep reef (GU, 90.1%). Similar findings are described in reefs with depths varying between 0 30 m, where relative abundance of sponge boring increases with increasing water depths (Kiene and Hutchings 1994). Factors controlling Bioerosion studies carried out worldwide have shown that different factors influence the degree of borer infestation. The boring activity can be related either to coral host characteristics and/or to environmental parameters. With respect to coral host characteristics, i.e., coral structure, age, growth rate and density, in our study variations of these factors between reef sites are rather small. A correlation between the rate of sponge with these parameters is found only when we do not consider the samples from the Guarajuba 10 m deep reef (GU) that is a somewhat small (202.9 cm -3 ) and young (17 y) sample to be compared with the others ones (873.2 cm -3 to cm -3 and 29 y to 39.8 y) (Table 3). In the other three reef sites TG ( m deep), TF ( m deep) and IT (5 m deep), the increase of sponge rate (from 0.98 to 1.00 kg m -2 y -1 ) is positively correlated with coral growth rate (from 2.18 to 2.82 mm y -1 ), which, conversely, means that it is favored by a coral less dense skeleton (from 1.90 to 1.76 g -1 cm -3 ). Similarly the substrate porosity in other reef areas has been found to favor both the degree of bioeroders infestation (Neumann 1966, Sammarco and Risk 1990) and the growth rate of corals (Holmes 1997), an inverse relationship, however, was found by Highsmith et al. (1983). Relative to environmental parameters, the sponge rate has been shown to decrease with water depth (Kobluk and Kozelj 1985) or not to be related with depths at all (MacGeachy and Stearn 1976). In this study the sponge rate does not show a regular trend related with water depths (Table 3), although the smallest number is seen in the Guarajuba 10 m deep reef. This probably reflects the limited depth range in which our sampling was conducted.

4 Table 2 Relative percentage of sponge according different studies. Reef sites Coral species Depth Relative (m) percentages References Bahamas Montastrea annularis 86.5 Becker and Reaka-Kudla 1997 Curaçao M. annularis Bak 1976 Belize M. annularis 2 to Highsmith et al Belize M. cavernosa 2 to 7 93 Highsmith et al Belize Porites astreoides 2 to 7 84 Highsmith et al Barbados M. annularis 0 to MacGeachy and Stearn 1976 Jamaica M. annularis 1 to Perry 1998 Britomart Reef Acropora Risk and Sammarco 1982 Britomart Reef Porites lobata 7 to 9 40 Sammarco and Risk 1990 Orpheus Island Porites lobata 7 to Sammarco and Risk 1990 Rib Reef Porites lobata 7 to 9 67 Sammarco and Risk 1990 Davies Reef Porites lobata 7 to 9 69 Sammarco and Risk 1990 Myrmidon Reef Porites lobata 7 to 9 40 Sammarco and Risk 1990 Enewetak G. retiformis 0 to Highsmith 1981 Enewetak Porites lutea 0 to Highsmith 1981 Enewetak Favia pallida 0 to Highsmith 1981 North Bahia S. stellata 0.2 to This study Table 3 Means (± standard deviation) of results obtained from the coral colonies sampled in each reef site: TG = Guarajuba reef top; TF = Praia do Forte reef top; IT = Itacimirim 5 m deep reef; GU = Guarajuba 10 m deep reef, n = number of colonies x 3 coral slabs. Reef site Depth ( m ) Coral age ( y ) Volume (cm 3 ) Density ( g -1 cm -3 ) Coral growth rate ( mm -1 y -1 ) Rate of sponge ( kg -1 m -2 y -1 ) TG (n=5) TF (n=5) IT (n=5) 5 GU (n=5) ±19.9 ± ±0,09 ±0.23 ± ±22.53 ± ±0.09 ±0.11 ± ±14.19 ± ±0.14 ±0.2 ± ±5.38 ± ±0.12 ±0.28 ±1.17 The emergent reefs, adjacent to the coastline (TG and TF), are submitted to an intense sediment influx carried from land, due to beach erosion and/or river input (Kikuchi 2001). This factor is considered detrimental to the sponge growth (Reiswig 1971). These reefs should then present a much lower rate of sponge compared with that of the reefs located off the coast, the 5 m and 10 m deep reefs, which are surrounded by less turbid waters (Kikuchi 2001), but this does not occur. Because the shallow emergent reefs are, also, under the influence of an enrichment of nutrient levels, due to the groundwater contamination by domestic sewage (Costa et al. 2000), this might overcompensate the negative effects of sediment load. Thus, it is apparent that the rates of sponge found in the studied reefs do not have a direct relationship between environmental parameters and the different reef sites. In the overall the results found in our work are comparable to the rates found in some reefs within pure carbonate settings and clear water (Table 4).

5 Table 4 Rate of sponge in various reef sites Sponge rates Reef sites References (kg -1 m -2 y -1 ) 0.26 Bermuda Rützler (1975) Barbados Stearn & Scoffin (1977) 1.35 Barbados Scoffin et al. (1980) Curaçao Bak (1976) Jamaica Moore & Shedd (1977) 8.0 Grand Cayman Acker & Risk (1985) 0.17 Florida Hein & Risk (1975) Florida Hudson (1977) North Bahia This study Acknowledgments The authors are grateful to the University of Santa Úrsula (R.J.), Federal University of Bahia (CPGG/LEC/IGEO), Bahia State Government (CADCT) and the Federal Agency CNPq, for the support provided for this research. References Bak RPM (1976) The growth of coral colonies and the importance of crustose coralline algae and burrowing sponges in relation with carbonate accumulation. Netherlands Journal of Sea Research 10: Becker LC, Reaka-Kudla ML (1997) The use of tomography in assessing in corals. Proceedings of the Eighth International Coral Reef Symposium, Panama 2 : Bromley RG (1978) Bioerosion of Bermuda reefs. Paleogeography, Paleoclimatology, Paleoecology 23 (3-4) : Costa Jr OS, Leão ZMAN, Nimmo M, Attrill MJ (2000) Nutrification impacts on coral reefs from northern Bahia, Brazil. Hydrobiologia 440 : Glynn PW (1997) Bioerosion and coral reef growth: a dynamic balance. In: Birkeland, C. (ed.) Life and Death of Coral Reefs. Chapman & Hall, New York: Goreau TF, Hartman WD (1963) Boring sponges as controlling factors in the formation and maintenance of coral reefs. In: R.F. Sognnaes (ed.). Mechanisms of Hard Tissue Destruction. American Association for the Advancement of Science Publications 75 :25-54 Hallock P (1988) The role of nutrient availability in : consequences to carbonate buildups. Palaeogeography,Palaeoclimatology,Palaeoecology 63 (1-3) : Hallock P, Müller-Karger FE, Halas JC (1993) Coral Reef decline. National Geographic Research & Exploration 9 (3) : Highsmith RC (1981) Coral at Enewetak: agents and dynamics. Internationale Revue der Gesamten Hydrobiologie 66 (3) : Highsmith RC, Lueptow RL, Schonberg SC (1983) Growth and of three massive corals on the Belize barrier reef. Marine Ecology Progress Series 13 : Holmes KE (1997) Eutrophication and its effect on bioeroding sponge communities. Proceedings of the Eighth International Coral Reef Symposium, Panama, 2 : Kiene WE (1988) A model of on the Great Barrier Reef. Proceedings of the Sixth International Coral Reef Symposium, Townsville 3 : Kiene WE, Hutchings PA (1994) Bioerosion experiments at Lizard Island, Great Barrier Reef. Coral Reefs 13 (2) :91-98 Kikuchi RKP (2001) Evolução dos recifes e das comunidades de corais hermatípicos da platafroma continental norte da Bahia, durante o Holoceno. Tese de Doutorado, Instituto de Geociências, Universidade Federal da Bahia, Salvador: 152 pp Kobluk DR, Kozelj M (1985) Recognition of a relationship between depth and macroboring distribution in growth framework reef cavities, Bonaire, Netherlands Antilles. Bulletin of Canadian Petroleum 33 : Laborel JL (1969) Madreporaires et hydrocoralliaires récifaux des côtes brésiliennes. Systematique, ecologie, repartition verticale et geographie. Annales de le Institute Oceanographique de Paris 47 : Leão ZMAN, Araujo TMF, Nolasco MC (1988) The coral reefs off the coast of eastern Brazil. In: J. H. Choat et al. (eds). Proceedings of the Sixth International Coral Reef Symposium, Townsville 3: Mansure JJ, Reis, MAC, Albano, RM, Lôbo-Hajdu G (2000) Molecular characterization of Cliona species (Porifera) using polymorphisms in the nuclear ribosomal ITS sequences. Genetics and Molecular Biology 23 (3) : McGeachy JK, Stearn CW (1976) Boring by macroorganisms in the coral Montastrea annularis on Barbados reefs. Internationale Revue der Gesamten Hydrobiologie 61 : Neumann AC (1966) Observations on coral erosion in Bermuda and measurements of the boring rate of the sponge Cliona lampa. Limnology and Oceanography 11 : Nimer E (1989) Climatologia do Brasil. Rio de Janeiro, Editora do Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro: 421 pp Nolasco MC, Leão ZMAN (1986) The carbonate buildups along the northern coast of the State of Bahia, Brazil. In: J. Rabassa (ed.). Quaternary of South America and Antartic Peninsula. Balkema, Roterdam 4 : Perry T (1998) Macroborers within coral framework at Discovery Bay, north Jamaica: species distribution and abundance, and effects on coral preservation. Coral Reefs 17 : Reiswig HM (1971) Particle feeding in natural populations of three marine demosponges. Biological Bulletin of the Marine Biology Laboratory, Woods Hole, 41 :

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