Defenses of Caribbean sponges against predatory ... - Inter Research

Vol. 127: 183-194.1995

MARINE ECOLOGY PROGRESS SERIES Mar Ecol Prog Ser

Published November 2

Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency Joseph R. Pawlikl,*,Brian Chanasl, Robert J. ~ o o n e n 'William , ~enical~ 'Biological Sciences and Center for Marine Science Research. University of North Carolina at Wilmington, Wilmington, North Carolina 28403-3297, USA 2 ~ n i v e r s i t yof California, San Diego, Scripps Institution of Oceanography, La Jolla. California 92093-0236. USA

ABSTRACT: Laboratory feeding assays employing the common Canbbean wrasse Thalassoma bifasciatum were undertaken to determine the palatability of food pellets containing natural concentrations of crude organic extracts of 7 1 species of Caribbean demosponges from reef, mangrove, and grassbed habitats. The majority of sponge species (69%) yielded deterrent extracts, but there was considerable inter- and intraspecific vanability in deterrency. Most of the sponges of the aspiculate orders Verongida and Dictyoceratida yielded highly deterrent extracts, as did all the species in the orders Homosclerophorida and Axinellida. Palatable extracts were common among species in the orders Hadromerida, Poecilosclerida and Haplosclerida. Intraspecific variability was evident, suggesting that, for some species, some individuals (or portions thereof) may be chemically undefended. Reef sponges generally yielded more deterrent extracts than sponges from mangrove or grassbed habitats, but 4 of the 10 most common sponges on reefs yielded palatable extracts (Callyspongia vaginalis, Mycale laevis, Niphates erecta, Iotrochota birotulata), including those most commonly eaten by sponge-eating reef fish. The presence of symbiotic zoanthid cnidarians of the genus Parazoanthus in the tissues of otherwise palatable sponges had little effect on the deterrency of tissue extracts, indicating that these commensal polyps do not confer a chemical defense by association There was no relationship between sponge color and deterrency, suggesting that sponges are not aposematic and that color variation is the result of other factors. There was also no relationship between the toxicity of sponge extracts (as determined in previous studies) and deterrency, confirming the invalidity of previous assessments of chemical defense based on toxicity. Although chemical antipredatory defenses are important strategies for most Caribbean sponges, some common species appear to rely on other tactics. KEY WORDS: Sponge - Chemical defense . Caribbean. Coral reef. Predation . Aposematism . Zoanthid

INTRODUCTION Since the Cambrian, sponges have been conspicuous members of the marine biota (Finks 1970), and remain integral constituents in benthic communities ranging from polar seas (Dayton e t al. 1974, McClintock 1987) to temperate and tropical waters (Reiswig 1973, Riitzler 1978, Wenner et al. 1983, Suchanek e t al. 1985). Sponges are particularly prominent on coral reefs (most are members of the class Demospongiae) where they often rival scleractinian and alcyonarian corals in diversity and abundance (Targett & Schmahl 1984,

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Suchanek et al. 1985).Quantitative assessments of reef sponge populations have been rare in the past, largely because of taxonomic problems (Riitzler 1978), but more recent studies have begun to determine the distributions and abundances of sponges, particularly on Caribbean reefs (Alcolado 1991, Alvarez et al. 1991, Diaz e t al. 1991). For example, Schmahl (1991) reports transect means of 10.45 species and 17.45 individual sponges m-2 on a 20 m deep reef off the Florida Keys, USA. Sponges are important to the overall ecology of coral reefs for many reasons. From a trophodynamic standpoint, they are very efficient filter feeders (Reiswig 1981), they appear to be capable of absorbing dissolved organic carbon as a food source (Reiswig 1974,

Mar Ecol Prog Ser 127:183-194, 1995

1981), and their bodies provide shelter for large numbers of invertebrates and fish (Tyler & Bohlke 1972, Riitzler 1976. Westinga & Hoetjes 1981, Pawlik 1983, Duffy 1992). Moreover, sponge tissues often harbor carbon- and nitrogen-fixing symbionts (e.g. Riitzler 1981, Wilkinson 1983) to the extent that sponges constitute a significant source of nutrients to primary producers in oligotrophic tropical waters (Schubauer et al. 1991). Sponges are aggressive competitors for space (Targett & Schmahl 1984, Suchanek et al. 1985), and often form complex epizoic associations with one another to maximize use of this limited resource (Riitzler 1970, Sara 1970). In addition, boring sponges are primary agents of carbonate bioerosion on coral reefs (Goreau & Hartman 1963, Riitzler & Rieger 1973). What factors limit the distributions of sponges on coral reefs? Abiotic factors appear to play a major role in shallow water, particularly wave stress and UVradiation (Jokiel 1980, Schubauer et al. 1991). Current velocity (Vogel 1977) and turbidity (Gerrodette & Flechsig 1979) can affect sponge pumping rates and may limit growth. Space is certainly a limiting resource, but sponges are often competitively dominant over other invertebrate species (Suchanek et al. 1985). Strangely, the biotic factors that structure reef sponge populations are poorly known. Predation appears to be of minor importance to most species (Randall & Hartman 1968), which is surprising in an environment noted for high levels of predation and nutrient scarcity (Grigg et al. 1984, Huston 1985). Predation on coral reef sponges is limited to a few vertebrate predators that feed on a diversity of sponge species (Randall & Hartman 1968, Meylan 1988, Wulff 1994),and a group of molluscs that specialize on one or a few species (Thompson 1976). In addition, there is a diversity of sponge-dwelling invertebrates that consume small amounts of sponge tissue, but these appear to do little damage to the sponge host (Westinga & Hoetjes 1981, Patvlik 1983). On Caribbean reefs, the primary vertebrate predators are angel-, file-, spade-, and puffer-fish (Randall & Hartman 1968) and hawksbill turtles (Meylan 1988). Of the 212 species of Caribbean fish surveyed by Randall & Hartman (1968) only 11 had sponge remains that comprised 6 % or more of their gut contents, with 5 species in the genera Holacanthus, Pomacanthus and Cantherhines having guts containing >50% sponge tissue. The authors believed that predation by these fish did little to control sponge populations, because only a few, highly specialized fish 'spread their predatory activities over a wide variety of sponge species.' Sponges of relatively few species comprised >95% of the diet of the hawksbill turtle Eretmochelys imbricata (Meylan 1988), but this turtle is so rare that it has been listed as a n endangered species. Among invertebrates, dorid nudibranch

molluscs are specialist predators on sponges (Thompson 1976), however these animals are also uncommon in the Caribbean, and their feeding likely results in minimal localized damage. Why should reef sponges have so few predators? It may be that the presence of a mineral or organic skeleton, or low food value per unit tissue, protects sponges from generalist predatory fish. Hypotheses regarding physical defenses and nutritional quality are considered in the next paper (Chanas & Pawlik 1995, this issue). By far, the most common explanation for the lack of predation on reef sponges is that they are distasteful to potential predators, a result of unusual chemical compounds in their tissues (Pawlik 1993). Of all invertebrates, demosponges have yielded the largest number and greatest diversity of secondary metabolites that have been isolated and described by marine natural products chemists (Faulkner 1994, and previous reviews cited therein). Many of these compounds have potent pharmacological activities, including anti-tumor, anti-fungal, anti-viral, and anti-bacterial effects (e.g. Schmitz & Gopichand 1978, Stonard & Andersen 1980, Kashman et al. 1989). Although the synthesis of these unusual compounds may ultimately be traced to endosymbiotic microorganisms for some sponge species (e.g. Unson & Faulkner 1993), the presence of certain classes of compounds is sufficiently conservative within other groups of sponges as to represent a basis for taxonomic assignment (Bergquist & Wells 1983, Braekman et al. 1992). Despite decades of natural products isolation work and pharmacological assays, little is known about the functions of sponge secondary metabolites in ecological interactions. Because these compounds are often structurally complex or present at high concentrations in sponge tissues, they are likely to be metabolically expensive for sponges that make and store them; therefore, it stands to reason that these metabolites should have some adaptive purpose. By far, the most commonly hypothesized role for these compounds is that of predator deterrence, but antifouling, anti-overgrowth and UV-protective functions have also been proposed (Paul 2992, Pawlik 1992, 1993). rn addition to the possibility that demosponges thwart predators with structural or chemical defenses, some species may deter predation by association with zoanthid cnidarians. Several species of Caribbean reef sponges have tissues that are often infused with commensal colonies of the genera Parazoanthus and Epizoanthus, with the polyps of these anthozoans visible on the sponge surface (Crocker & Reiswig 1981, Lewis 1982). Other species of zoanthids produce potent toxins, including palytoxin (Moore & Scheuer 1971). Zoanthids may provide an associational defense to undefended sponges that bear them by (1) stinging

Pawlik et al.. Defenses of sponges. I. Chemical

potential predators with cnides, (2) rendering the comingled sponge and zoanthid tissue unpalatable because of secondary metabolites produced by the zoanthids, or (3) both mechanisms. Defense by association has been documented for several crustaceans that live in chemically defended macroalgae (Hay et al. 1989, 1990). In the study reported herein, we tested the hypothesis that sponge secondary metabolites confer a defense against predation by surveying the palatability of crude organic extracts of 71 species of Caribbean demosponges using a common generalist predatory reef fish in aquarium assays. Specifically, we addressed the following questions: (1) Do organic extracts of sponges deter feeding by the reef fish Thalassoma bifasciatum? (2) What inter- and intraspecific patterns of deterrency exist? (3) Does the presence of commensal zoanthids in sponge tissue confer an associational chemical defense? (4) How do patterns of deterrency compare with sponge habitat (reef vs mangrove and grassbed), relative abundance, or color? (5) How do patterns of deterrency compare with patterns of sponge toxicity that have been reported in past studies? In the companion paper that follows, we also consider the importance of structural components and nutritional quality in deterring predation by generalist predators (Chanas & Pawlik 1995). In a subsequent study, we will consider predation by fish that feed primarily or exclusively on sponges.

MATERIALS AND METHODS Sponge collection and identification. This study was conducted over the course of 5 research expeditions: 3 on board the RV 'Columbus Iselin' to Belize in June 1991, and to the Bahamas Islands in July 1992 and again in August 1993, and 2 at the National Undersea Research Program facility in Key Largo, Florida, USA, in December 1992 and again in May 1994. Portions of sponges were collected by gentle tearing, or by cutting the tissue with a sharp knife. Sponges were collected from reef, mangrove, and grassbed habitats. For each species, replicate collections were taken from distant sites to avoid collecting asexually produced clones. Sponges were identified on the basis of spicule and tissue preparations (DeLaubenfels 1936, Wiedenmayer 1977, Rutzler 1986, Zea 1987, Kelly-Borges & Pomponi 1992, R. W. M. VanSoest unpubl.). Extraction and isolation. Freshly collected tissue from individual sponge specimens was used for each replicate. For large sponge specimens, only surface tissues (to 1 cm depth) were used. Only sponges that were free of epibionts were chosen for extraction, except for assays to determine whether the presence of

commensal zoanthids conferred a chemical defense by association; for these experiments, sponge specimens were chosen that were partially colonized by zoanthids, and surface tissues from the colonized and uncolonized portions of the specimen were extracted and assayed separately. Sponge tissues were chopped into small pieces and added to 40 m1 of a 1 : l mixture of dichloromethane and methanol in a graduated centrifuge tube to a final volume of 50 ml. Capped tubes were inverted, agitated repeatedly, and kept chilled at 4OC during a 24 h extraction period. During this period, water combined with the methanol and the resulting methano1:water phase separated from the dichloromethane phase. Therefore, the sponge tissue was alternately exposed to dichloromethane and methanohvater as the tubes were inverted. After extraction, both phases were filtered through celite, the dichloromethane extract was evaporated to dryness on a rotary evaporator using low heat (