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Porifera Research: Biodiversity, Innovation and Sustainability - 2007 131 Spongivory by juvenile angelfish (Pomacanthidae) in Salvador, Bahia State, Brazil Bárbara R. Andréa(1), Daniela Batista(1,2), Cláudio L.S. Sampaio(3), Guilherme Muricy(1*) Departamento de Invertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro. Quinta da Boa Vista, s/no., São Cristóvão. 20940-040 Rio de Janeiro, RJ, Brasil. [email protected] (2) Departamento de Biologia Marinha, Universidade Federal Fluminense, Niterói, Rio de Janeiro, Brasil (3) Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, João Pessoa, Brasil. (1) Abstract: Adult angelfish of the genera Pomacanthus and Holacanthus (Family Pomacanthidae) are considered the most important spongivorous fishes of the Caribbean, with sponges comprising more than 70% of their gut contents. However, despite their commercial importance as ornamental fish, little is known about the diet of juvenile angelfish, which are generally considered to be cleaners. The goal of this study was to identify through gut content analysis the sponge species eaten by juveniles of the angelfish Pomacanthus paru, Holacanthus ciliaris and Holacanthus tricolor in Salvador, Bahia state, Brazil. We also estimated the frequency of occurrence of each sponge species in the diet of juvenile angelfish, and tested the correlation between fish size and number of sponge species preyed. In Salvador, 34 species of sponges were found in the gut contents of 14 out of 16 specimens of juvenile angelfish. Twenty-two species of sponges were eaten by Holacanthus tricolor, 15 by H. ciliaris, and 14 by Pomacanthus paru. There was a significant positive correlation between fish size and number of preyed sponge species, but the coefficient of determination was low and even the smallest fishes had sponges in their gut contents. These findings indicate that juveniles of all three species of angelfish are generalists in the consumption of sponges in Brazil, a diet similar to that of the adults. The most frequent sponges in juvenile angelfish gut contents were Tedania ignis, Mycale sp., and Spirastrella sp., all with 37.5% of frequency in the 16 stomachs analyzed. Tedania ignis was not consumed by H. ciliaris in Salvador, but it was consumed by the other fish species, being the most frequent prey of H. tricolor and P. paru. Juvenile angelfish probably adapt to a cleaning behavior or to benthic feeding according to local environmental conditions. The development of sponge-based artificial foods may allow longer maintenance and reproduction of angelfish in aquaria, thus helping to protect their natural populations. Keywords: Holacanthus, Pomacanthus, Porifera, Predation, Southwestern Atlantic Introduction Sponges are important structural and functional components of coral reefs, where they participate in numerous ecological relationships such as competition, commensalism, symbiosis, bioerosion and predation (reviewed by Diaz and Rützler 2001, Wulff 2001, 2006a). Although reef sponges are abundant and many species live exposed to predators, few animals are known to feed on them, probably due to their physical (spicules) and chemical (secondary metabolites) defenses (Pawlik et al. 1995, Hill et al. 2005, Wulff 2006a, 2006b). Among invertebrates, spongivory is shown by opisthobranchs (e.g., Glossodoris pallida, Archidoris montereyensis, Peltodoris atromaculata, Tylodina perversa), sea stars (e.g., Oreaster reticulatus, Echinaster echinophorus), sea urchins (e.g., Eucidaris tribuloides and Lytechinus variegatus) and hermit crabs (Reiswig 1973, Wulff 1995, 2006b, Becerro and Paul 1998, Wadell and Pawlik 2000, Santos et al. 2002, Gemballa and Schermutzki 2004). Some associated copepods, amphipods, isopods and alpheid shrimps also consume their host sponges (Pawlik 1983, Ríos and Duffy 1999, Mariani and Uriz 2001). The main vertebrate sponge-feeders are the sea turtle Erethmochelys imbricata (Meyland 1988) and reef fishes belonging to the families Pomacanthidae, Ostraciidae, Tetraodontidae, Ephippidae and Monacanthidae. Among these, the family Pomacanthidae contains the most important sponge-feeding fishes in the Caribbean, particularly in the genera Pomacanthus and Holacanthus (Randall and Hartman 1968, Wulff 1994). The family Pomacanthidae includes 88 species distributed in all tropical seas (Allen et al. 1998, Debelius et al. 2003). Within the family there is a diverse range of feeding specializations, including herbivory, planktivory, cleaning activity, and omnivory (Böhlke and Chaplin 1968, Hourigan et al. 1989, Allen et al. 1998, Deloach 1999, Bellwood et al. 2004). Ontogenetic variation in diet contents has been observed in many pomacanthids (Thresher 1980, Deloach 1999) as well as in other reef fish families such as Blenniidae, Kyphosidae and Scaridae (Bellwood 1988, Sturm and Horn 1998, Muñoz and Ojeda 2000). In the Caribbean, sponges comprise over 70% of the diet of adults of the common pomacanthid species Pomacanthus paru (French angelfish), Pomacanthus arcuatus (Gray angelfish), Holacanthus ciliaris (Queen angelfish) and Holacanthus tricolor (Rock beauty) 132 (Randall and Hartman 1968, Dunlap and Pawlik 1996). In Brazil, adults of Pomacanthus paru also feed mostly on sponges and algae, in variable proportions according to the locality studied (Batista 2006). The feeding behavior of juveniles, however, appears to be different from that of adults in these species. Juveniles of H. ciliaris, P. paru and P. arcuatus may act as cleaners until they have approximately 10-15 cm in total length (Feder 1966, Thresher 1980, Deloach 1999, Sazima et al. 1999). The primary food of P. paru and P. arcuatus juveniles was reported to be filamentous algae, with copepods picked from client fishes and few free-living copepods making up to 25% of their diet (Deloach 1999). In Abrolhos Archipelago, Brazil, juveniles of the French angelfish P. paru removed ectoparasites of 31 species of reef fishes (Sazima et al. 1999). Food items in their stomachs included caligid (15-30%) and harpaticoid copepods (5-10%), together with both red and green algae (30-70%). Juveniles of H. ciliaris also feed on algae until they reach sexual maturity (Deloach 1999). The diet of H. tricolor juveniles is largely unknown, but it is assumed that it is a combination of drifting plankton, small benthic invertebrates, and possibly the mucus and parasites of larger fishes (Thresher 1979, 1980, Gasparini and Floeter 2001). Brazil is one of the five leading exporting countries of tropical aquarium fishes in the world, and the interest in marine ornamental organisms has increased substantially from mid- to late 1990’s (Gasparini et al. 2005, Floeter et al. 2006). Juvenile angelfish are preferred over the adults for ornamental purposes due to their smaller size and beautiful color patterns. In Ceará State, NE Brazil, angelfish juveniles have been captured and exported in large numbers: 43,730 specimens of H. ciliaris, 22,969 of P. paru, and 8,757 specimens of H. tricolor between 1995 and 2000 (Monteiro-Neto et al. 2003), although these values may be overestimated (Gasparini et al. 2005). Cleaner species play an important ecological role in reef habitats, and their removal may negatively affect other fish species, including commercially important ones (Sazima et al. 1999, Monteiro-Neto et al. 2003). Therefore, knowledge about the feeding behavior of juvenile angelfish is important for the conservation of angelfish species and of coral reef communities. In this study we tested the hypothesis that sponges are an important part of the diet of juvenile angelfish, and not only of the adults. We identified the sponge species found in the gut contents of juveniles of Pomacanthus paru, Holacanthus ciliaris and H. tricolor in Salvador, Bahia state, Brazil. We also estimated the frequency of each sponge species in the gut contents of juvenile angelfish, and tested the correlation between fish size and number of prey species. Our results may aid in the development of a better diet for the growth and reproduction of angelfish in captivity, thus helping to protect angelfish species which are currently threatened by the increase of marine ornamental fish trade in Brazil. Materials and methods Sixteen specimens belonging to three species of angelfish were studied: Pomacanthus paru (n=5); Holacanthus ciliaris (n=6) and Holacanthus tricolor (n=5). Fish were collected in four locations in Salvador, Bahia state, Brazil (Fig. 1): Praia Fig. 1: Location of the study area. da Ribeira, in Todos os Santos Bay (12º54’S–38º29’W), Barra Grande, in Itaparica Island (13º03’S–38º38’W), Rio Vermelho (13º00’S–38º30’W), and Praia da Pituba (13º00’S– 38º30’W). The specimens were collected from 18/II/2003 to 10/III/2004 by commercial ornamental fisheries (Axé Online Ltd.) in shallow reefs and rocky bottoms. Only juveniles were caught, easily recognized by their special color patterns, which change after sexual maturity is reached (Böhlke and Chaplin 1968, Thresher 1980). Specimen size varied between 5.0-14.5 cm in H. ciliaris, 5.0-14.0 cm in H. tricolor, and 3.0-14.5 cm in P. paru. The stomachs were removed and their contents were separated based on color, texture and consistency. Only the sponge fragments were identified to lower rank taxons, and no attempts were made to quantify the abundance of each species consumed in the gut contents of the 16 angelfish specimens analyzed. The sponge fragments were dehydrated in an alcohol series (50-100%) with a final xylene step and included in paraffin. Transverse sections were mounted on microscope slides for identification. Free spicules were not considered as evidence of predation, only fragments large enough to be sectioned and in which the skeleton could be observed. Sponges were deposited in the sponge collection of Museu Nacional, Universidade Federal do Rio de Janeiro, Brazil. A linear regression between fish size (standard length SL) and number of prey species was calculated online (http:// faculty.vassar.edu/lowry/VassarStats.htm). 133 Results Sponges comprised more than 90% of the gut contents of juvenile angelfish in Salvador, together with a few unidentified filamentous algae (< 10%). The guts of two juveniles of H. ciliaris were empty. A total of 34 sponge species were found in the diet of angelfish in Salvador (Table 1). The greatest species richness was observed in gut contents of Holacanthus tricolor (22 sponge species), followed by H. ciliaris and Pomacanthus paru (15 and 14 sponge species, respectively). Twelve sponge species were only predated by H. tricolor: Acanthanchora sp., Coelosphaeridae unidentified, Desmapsamma anchorata, Lissodendoryx sp., Microcionidae unidentified 1, Microcionidae unidentified 2, Monanchora sp., Myxillina unidentified, Pachastrellidae unidentified, Phellodermidae unidentified, Plakinastrella sp., and Timea sp. Only three species were predated exclusively by Holacanthus ciliaris: Artemisina sp., Chalinidae unidentified, and Tethya sp. Six species were eaten exclusively by P. paru: Chondrilla nucula complex, Cyamon sp., Mycale laxissima, Niphatidae unidentified, Raspaciona sp., and Tetillidae unidentified (Table 1). As a whole, the sponge species most frequently predated by pomacanthids in Salvador were Tedania ignis, Mycale sp., and Spirastrella sp., all present in 37.5% of the 16 specimens analyzed. Although Tedania ignis was not consumed by H. ciliaris, it was very frequent in the gut contents of P. paru (80% of the specimens examined) and common in H. tricolor (40%; Table 1). The number of sponge species per stomach varied from 4-9 in H. tricolor, from 1-7 in P. paru, and from 0-8 in H. ciliaris. The curves of accumulated richness of sponge species in angelfish diet did not reach stabilization with the small sample sizes studied here, neither with each fish species considered separately nor when they were considered together (Fig. 2). This indicates that the real number of sponge species in the diet of juvenile angelfish in Salvador is probably much higher than that shown by our results. There was a significant positive correlation (p<0.05) between fish size and number of sponge species in gut contents, although with a low coefficient of determination (r2 = 0.465; Fig. 3). The single smallest fish (3 cm SL) had only one sponge species in its stomach, and three of the five smallest fishes (3.0-5.5 cm SL) fed on few sponge species (15 species per stomach). Table 1: Frequency of occurrence of sponge species in gut contents of juvenile angelfish in Salvador, Brazil (in %). Combined = frequency in all species pooled together (n=16). Sponge species Acanthanchora sp. Acervochalina sp. Artemisina sp. Chalinidae unidentified Chondrilla nucula complex Clathria sp. 1 Clathria sp. 2 Coelosphaeridae unidentified Cyamon sp. Desmapsamma anchorata Halichondriidae unidentified Haplosclerida unidentified Lissodendoryx sp. Microcionidae unidentified 1 Microcionidae unidentified 2 Mycale laxissima Mycale sp. Mycalidae unidentified Myxillina unidentified Monanchora sp. Niphatidae unidentified Pachastrellidae unidentified Phellodermidae unidentified Plakinastrella sp. Raspaciona sp. Spirastrella sp. Stelleta sp. 1 Stelleta sp. 2 Strongylacidon sp. Suberitidae unidentified Tedania ignis Tethya sp. Tetillidae unidentified Timea sp. Species richness P. paru 20 20 40 20 20 40 20 40 20 20 60 20 80 20 14 H. tricolor 20 40 20 20 40 20 20 20 20 20 60 40 40 H. ciliaris 17 17 17 33 17 50 17 50 17 20 20 20 20 20 20 20 40 33 17 17 17 17 17 20 22 15 Combined 6.25 12.50 6.25 6.25 6.25 25.00 25.00 6.25 6.25 12.50 12.50 31.25 6.25 12.50 6.25 6.25 37.50 25.00 12.50 12.50 6.25 6.25 6.25 6.25 6.25 37.50 12.50 12.50 12.50 12.50 37.50 6.25 6.25 6.25 34 134 Fig. 2: Curves of accumulated richness of sponge prey species in juvenile angelfish gut contents. A, Holacanthus tricolor; B, Holacanthus ciliaris; C, Pomacanthus paru; D, all species pooled together. Discussion Juvenile angelfish fed largely on sponges in Salvador (> 90%), and only a few filamentous algae were also found in their gut contents. These figures are similar to those of adult angelfish diet in the Caribbean, where sponges comprised 74.8% to 97.1% of the diet of Pomacanthus paru and Holacanthus ciliaris, respectively (Randall and Hartman 1968). Algae were also the second most common item in the diet of adult pomacanthids in the Caribbean, varying from 0.8% to 13.4% of the diet of H. tricolor and P. paru, respectively (Randall and Hartman 1968). Other food items common in Caribbean adults such as tunicates, hydroids, zoantharians, and bryozoans were not found in juveniles from Salvador. Fourteen out of 16 fishes (87.5%) collected in one year had sponge remains in their stomachs, indicating that spongivory is not occasional, but frequent and widespread in the juvenile angelfish population in Salvador. Adult angelfish appear to have a more varied diet, at least in the Caribbean, where sponges were found in only 12 of 23 stomachs of P. paru (52.1%) and 18 out of 34 specimens of P. arcuatus (52.2%). Adults of H. tricolor are more specialized in sponges, with sponge remains in 22 of 24 specimens (91.7%; Randall and Hartman 1968). The diet of juvenile angelfish in Salvador includes at least 34 sponge species. All three angelfish species studied here, Pomacanthus paru, Holacanthus ciliaris, and H. tricolor were generalists in the consumption of sponges, eating 14 to 22 different species each. The real number of sponge species consumed by these angelfish is probably higher than that, as indicated by the shape of the accumulated richness curves (Fig. 2). Although there was a significant positive correlation between fish size and number of preyed sponge species (Fig. 3), the coefficient of determination was low and even the smallest fishes had sponges in their gut contents. Part of this correlation may reflect greater gut volume in larger fish individuals, allowing them to have more bites (and therefore more species) in their guts at the time they were collected. The diet of pomacanthid juveniles in Salvador is very similar to that of the adults, both in the Caribbean and in Brazil: they are “smorgasbord-feeding sponge specialists”, consuming a variety of benthic invertebrates and algae, apparently chosen according partly to prey palatability and partly to prey availability in the environment (Randall and Hartman 1968, Hourigan et al. 1989, Wulff 2006a, Batista 2006). This is at odds with some studies which suggest that juveniles of H. ciliaris and P. paru are cleaners until they have approximately 10-15 cm in total length, when they change to benthic feeding of a mainly sponge and algae diet (Feder 1966, Böhlke and Chaplin 1968, Hourigan et al. 1989, Sazima et al. 1999). Other studies however found little cleaning activity in juveniles of P. paru (Wicksten 1995, 1998). Among Tropical Western Atlantic angelfish, juveniles of P. paru seem to be the most specialized as cleaners, with P. arcuatus and H. ciliaris having a mixed diet composed mostly of algae and detritus 135 Fig. 3: Linear regression between fish size (standard length in cm) and the number of sponge species in gut contents of juvenile angelfish. Slope = 1.1173, intercept = 5.0347, Standard error of the estimate = 3.169. and being only occasional cleaners (Thresher 1980, Deloach 1999). The diet of H. tricolor juveniles was hitherto poorly known, although cleaning activity has been reported in a few other studies (Thresher 1979, 1980, Gasparini and Floeter 2001). The method of study employed by each author is important to explain such disagreements. When only direct underwater observation is considered (e.g., counting the bites given in each prey species), there is a trend to increase the relative importance of algae and of cleaning activity in the diet of pomacanthids (Böhlke and Chaplin 1968, Thresher 1980, Hourigan et al. 1989, Sazima et al. 1999, Batista 2006). Juveniles of angelfish such as H. tricolor dwell mostly in cryptic habitats inaccessible for divers (Thresher 1980). These habitats are often dominated by sponges (Sarà and Vacelet 1973). Other species of angelfish, including adult specimens, also use small caves and reef crevices for sheltering and foraging, biasing the direct observation of preyed items towards more exposed organisms such as algae and gorgonians (Thresher 1980, Batista 2006). When only gut contents are analyzed, the relative importance of spongivory seems to increase, both in proportion to algae and benthic invertebrates and in number of species (e.g., Randall and Hartman 1968, Deloach 1999). It is possible that sponge fragments remain recognizable in the guts of angelfish longer than copepods and filamentous algae, due to their high collagen and spicule content (Chanas and Pawlik 1995). This would artificially increase the proportion of spongivory in studies based only in gut contents and without direct observations, such as the present one (see also Randall and Hartman 1968). The complementary use of both field observations and gut content analysis allows a better understanding of pomacanthid feeding habits (Hourigan et al. 1989, Sazima et al. 1999, Batista 2006, Wulff 1994, 2006a). It is possible therefore that juvenile angelfish in Salvador are not almost exclusively sponge-eaters as shown by our results, but might also consume other benthic organisms and act as cleaners occasionally. This issue can only be solved through systematic direct observations on juvenile angelfish, which could not be carried out in this study. Another explanation for the variation in the diet of pomacanthid juveniles in different studies is a high dietary plasticity of pomacanthid species. Allopatric angelfish populations may specialize to use different resources, depending on their availability in each locality. For example, the abundance of reef fish in general is greater in the Abrolhos National Marine Park, which is a protected area, than in Salvador, which has been subject to heavy fishing (Gasparini et al. 2005, Floeter et al. 2006). It may thus be easier for juveniles of pomacanthids such as P. paru to establish a cleaning station in Abrolhos than in Salvador, where they have to adapt their diet to the available resources, mainly sponges and algae. The presence of a suitable habitat for juveniles close to a reef fish community also helps to explain the intense cleaning activity of P. paru juveniles in Abrolhos reefs (Sazima et al. 1999). Although always composed mostly of sponges, the specific composition of the diet of adult angelfish varied strongly in different localities such as the Bahamas, Virgin Islands, and Panama in the Caribbean (Randall and Hartman 1968, Feddern 1968, Hourigan et al. 1989, Wulff 1994), and Atol das Rocas, Abrolhos and Ilha Grande in Brazil (Batista 2006), irrespective of the study method. In all these locations and in Salvador, each species of angelfish fed on a diverse array of sponge species, ranging from 12 in P. paru to 40 in H. ciliaris, both in the U.S. Virgin Islands (Randall and Hartman 1968, Hourigan et al. 1989). Together, Pomacanthus paru and P. arcuatus ate 64 sponge species in Panama (Wulff 1994). The only exception was H. tricolor, which was observed feeding on a single sponge species in Panama and was therefore considered a possible specialist (Wulff 1994). However, adults of H. tricolor are known to fed on 14 to 28 different sponge species in the U.S. Virgin Islands and Puerto Rico (Randall and Hartman 1968, Hourigan et al. 1989), and juveniles in Salvador fed on 22 sponge species. This indicates that H. tricolor is also a generalist in the consumption of sponges, like most other pomacanthids. The number of sponge species eaten by each individual fish in Salvador varied from 0-9 (average 4.5). This tolerance to predate upon diverse sponge species may be a strategy of angelfish to overcome the effects of sponge toxins by eating small amounts of each toxic substance from many different sponge species (Wulff 1994). It has also be suggested as an adaptation of benthic fish species with pelagic larvae such as angelfish to increase their chances of survival in areas with different availability of specific food items (Hourigan et al. 1989). The similarity between gut contents of different but co-specific specimens was low in Salvador (maximum 0.273 between two specimens of H. tricolor; data not shown), indicating that individual fish choose their food independently. This may be related to the very small home range of angelfish juveniles (around 1-2 m2), much smaller than that of the adults (up to 2,300 m2 in P. paru; Thresher 1980, Hourigan et al. 1989). All specimens studied here came from the same general region in Salvador, but dietary similarity between the three species was low (maximum 0.296 between H. ciliaris and H. 136 tricolor; data not shown) and in the same range of intraspecific similarity. Most of the interspecific variation found in angelfish diet in Salvador thus appears to be random, and due to the sum of independent choices of individual fishes of the three different species studied. As most fishes, spongivores have great plasticity in their feeding behavior. This variability could have influence from food availability, fish size, species and other temporal and spatial factors. However, part of the differences in dietary composition between sympatric species is probably due to an active choice of preys, possibly restrained by the physiological tolerance of each fish species to the prey’s toxins. A certain degree of choice in pomacanthids is supported by observations of predation upon relatively rare sponge species (Hourigan et al. 1989, Wulff 1994). Holacanthus passer often feeds on plankton and fish faeces in the water column in the eastern Pacific (Aburto-Oropeza et al. 2000); there are few exposed sponges on coral reefs there, but when cryptic sponges were exposed the angelfish quickly swam down out of the water column to feed on them (Wulff 1997). Caribbean angelfish also prefer to eat mangrove or cryptic sponge species whenever they are made available in the reefs (Dunlap and Pawlik 1996, Wulff 2005). In general, spongivorous fish tend to choose the most palatable or undefended prey species available in a given locality (Dunlap and Pawlik 1996), although which prey is more palatable varies according to the predator species (Wulff 2006a). For instance, the fire-sponge Tedania ignis is commonly eaten by H. tricolor and P. paru, but apparently not by H. ciliaris, both in Brazil and in the Caribbean (Table 1; see also Randall and Hartman 1968). The starfish Oreaster reticulatus also feeds on Tedania ignis in Belize, but not on the sibling species T. klausi (Wulff 2006b). Also, the dietary similarity between congeneric species of both Pomacanthus and Holacanthus is greater than between species from different genera (Table 1; see also Hourigan et al. 1989). Whether this truly represents a species-specific choice of prey by pomacanthids remains to be experimentally demonstrated. Both adult and juvenile angelfish present high plasticity, tolerance, and a certain degree of choice in their smorgasbord sponge-feeding specialized strategy. This appears to be a highly derived feeding strategy, which is coupled with morpho-functional modifications in the teeth, jaws, and gill rakers that make pomacanthids (especially Holacanthus and Pomacanthus) more apt to feed on structurally resilient and firmly attached benthic prey such as sponges, gorgonians and tunicates (Hourigan et al. 1989, Bellwood et al. 2004; Konow and Bellwood 2005). Sponges have been evolving during at least 580 MY (Li et al. 1998), and they developed chemical and physical defenses so effective that only very specialized predators such as angelfish and opisthobranchs are able to feed on them. This may help to explain why there are so few predators of sponges, despite their great abundance in coral reefs. Angelfish are threatened by marine ornamental fish trade in Brazil, and juveniles are the targets preferred by aquarists (Gasparini et al. 2005, Floeter et al. 2006). The maintenance of angelfish in aquaria is difficult due to their aggressiveness and their diet made up mostly of sponges (Thresher 1980). The development of artificial food based on the sponge species found in this study to be eaten by angelfish juveniles in the field might help their reproduction and survival in captivity, allowing aquarists to enjoy angelfish in their saltwater tanks without eliminating them from coral reefs, where they play important ecological roles. Acknowledgements We thank José de Anchieta Nunes, Camilo Ferreira and Ericka Coni for laboratory assistance. We are also grateful to Samuele Clerici of Axé Online Fishes for the kind donation of specimens for study. We thank the two anonymous reviewers for their comments, which greatly improved the manuscript. 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