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Author's Personal Copy Author's personal copy Mar Biol (2012) 159:389–398 DOI 10.1007/s00227-011-1816-2 ORIGINAL PAPER Assessing the antipredatory defensive strategies of Caribbean non-scleractinian zoantharians (Cnidaria): is the sting the only thing? David E. Hines · Joseph R. Pawlik Received: 6 July 2011 / Accepted: 11 October 2011 / Published online: 22 October 2011 © Springer-Verlag 2011 Abstract The relative importance of chemical, nemato- and pathogens, is Wnite (Stearns 1992). The role of resource cyst, and nutritional defenses was examined for 18 species trade-oVs in ecology has been a subject of great interest to of Caribbean sea anemones (actinarians), zoanthids, and researchers for many years (reviewed by Zera and Harsh- mushroom polyps (corallimorpharians) from the Florida man 2001) and has been particularly well documented in Keys and the Bahamas Islands, 2008–2010. Feeding assays terrestrial plants (Felton and Korth 2000; Spoel et al. 2007; were performed using the Wsh Thalassoma bifasciatum with Kaplan et al. 2009). For example, trade-oVs between anti- artiWcial foods containing crude organic extracts of cnidar- herbivore defenses and fungal resistance have been ian tissues. A novel behavioral assay using brine shrimp described for the lima bean, Phaseolus lunatus, which is nauplii was used to assess nematocyst defenses. The nutri- able to resist fungal infection or produce hydrogen cyanide tional quality of cnidarian tissues was examined using to deter herbivore grazing but cannot simultaneously do bomb calorimetry and soluble protein assays. In general, both (Ballhorn et al. 2010). actinarians invested in nematocyst defenses, zoanthids in More recently, documentation of physiological resource either nematocyst or chemical defenses, and corallimorpha- trade-oVs has been extended to sessile organisms in marine rians lacked both, except for 1 of 3 species that was chemi- ecosystems. Coral reef sponges exhibit reduced healing and cally defended. Relative to other coral reef invertebrates, growth rates at the expense of producing secondary metab- cnidarian tissues had similar caloric values but lower solu- olites that deter predatory Wshes (Walters and Pawlik 2005; ble protein concentrations. Trade-oVs between chemical Leong and Pawlik 2010a). Trade-oVs between physical and and nematocyst defenses were observed for 65% of species, chemical defensive mechanisms have also been demon- while habitat and behavior provided a likely explanation for strated for hydroids (Stachowicz and Lindquist 2000). undefended species. However, physiological resource trade-oVs have not been observed in all benthic invertebrates. For example, no clear pattern between secondary metabolite and inorganic acid Introduction defenses was exhibited by ascidians (Pisut and Pawlik 2002). While some studies of sessile marine invertebrates Resource trade-oVs arise in nature because the energy have demonstrated evidence of physiological resource available to organisms for key physiological tasks, includ- trade-oVs, the importance of these trade-oVs in the ecology ing growth, reproduction, and defenses against predators of Caribbean non-scleractinian zoantharians, the sea anem- ones, zoanthids, and corallimorpharians (Phylum Cnidaria: Orders Actiniaria, Zoanthidea, and Corallimorpharia), Communicated by T. L. Goulet. remains unexplored. D. E. Hines · J. R. Pawlik (&) Non-scleractinian zoantharians can be an important Department of Biology and Marine Biology, component of the benthic community on some coral reefs Center for Marine Science, University of North Carolina (Work et al. 2008). Although coral reef ecosystems are Wilmington, 5600 Marvin Moss Lane, Wilmington, NC 28409, USA known for high levels of predation pressure (Wood 1993), e-mail: [email protected] non-scleractinian zoantharians are rarely observed to be 123 Author's personal copy 390 Mar Biol (2012) 159:389–398 consumed by generalist predators (Randall 1967), implying diVerences in predation pressure between habitats may alter the presence of defenses. Because non-scleractinian zoan- the selective pressure for producing defensive mechanisms. tharians lack a calcareous or proteinaceous endoskeleton Therefore, when considering possible trade-oVs in resource common to scleractinian and antipatharian corals, respec- investment, it is important to consider whether antipreda- tively (Daly et al. 2003), alternative defensive mechanisms tory defenses are necessary at all, given the behavior or dis- may be present. Moreover, because species within these tribution of the organism of interest relative to potential taxa may employ a variety of defensive mechanisms, non- predators. scleractinian zoantharians are a particularly relevant group In this study, we evaluated chemical, nematocyst, and for testing resource allocation theory. Historically, it has nutritional defenses of 18 species of non-scleractinian been presumed that many cnidarians rely on specialized zoantharians from the Florida Keys and the Bahamas stinging structures called nematocysts (a type of cnida) to Islands with the objective of determining whether resource inject venom as a defense against predation (Mariscal 1974; trade-oVs exist among these defensive mechanisms. In Basulto et al. 2006). Highly toxic compounds including addition to performing relevant assays to assess defensive actinoporins, equinatoxins, and sticholysins have been iso- capabilities, the habitats of each species were observed and lated and chemically characterized from inside the nemat- recorded. Under the assumption that resources are limited ocysts of some non-scleractinian zoantharians in the and both chemical and nematocyst defensive mechanisms families Aiptasiidae, Actiniidae, Stichodactylidae, and are similarly eVective, we hypothesized an inverse relation- Metridiidae (Anderluh and Macek 2002; Martinez et al. ship between nematocyst and chemical defenses in Carib- 2002; Alvarez et al. 2009). However, other toxic com- bean non-scleractinian zoantharians. In accord with other pounds, most notably palytoxin, have been isolated from studies (Penny 2002), we hypothesized no relationship outside the nematocysts (Moore and Scheuer 1971; Fautin between nutritional quality and defensive strategies, as low- 2009), suggesting that their function is not linked to nema- ered food value has been hypothesized to contribute to tocyst Wring. Furthermore, some cnidarians, such as gorgo- other defensive mechanisms rather than supplant them. nians, rarely possess a heavy armament of nematocysts and rely instead on chemical defenses to deter predation (Paw- lik et al.1987; O’Neal and Pawlik 2002). Some non-sclerac- Materials and methods tinian zoantharians can incorporate inorganic material such as sand into their bodies, but these structures likely provide Cnidarian collections little protection against predation because similar structures in sponges and gorgonians have little eVect on predation Specimens of 18 species of non-scleractinian zoantharians (Chanas and Pawlik 1995; O’Neal and Pawlik 2002). As a were collected from shallow reefs and mangroves during result of the types of defensive mechanisms available to six expeditions to the Florida Keys and the Bahamas non-scleractinian zoantharians, these cnidarians may rely Islands between June 2008 and July 2010 (Table 1). All on chemical or nematocyst defenses, or a combination of species that were encountered during sampling, and could both types of defense. be positively identiWed according to the guidelines Another possible defensive strategy for non-scleractin- described in Humann and DeLoach (2002), were included ian zoantharians is low nutritional quality. Poor food value in this study. Samples from the Florida Keys were collected has been proposed as a defensive mechanism in both plants at Bird Sanctuary (N 25°1Ј58.54Љ W 080°30Ј19.09Љ), and animals (Van der Mejden et al. 1984; DuVy and Paul Carysfort Reef (N 25°14Ј54.72Љ W 080°11Ј47.46Љ), Conch 1992). For example, it has been proposed that the percent- Reef (N 24°56Ј59.76Љ W 080°27Ј13.38Љ), Harry Harris age of digestible tissue in some nudibranchs is lower than Park (N 25°1Ј25.36Љ W 080°29Ј35.99Љ), JewWsh Creek (N that of shelled mollusks of similar size, enhancing their 25°10Ј58.59Љ W 080°23Ј25.99Љ), North Dry Rocks (N chemical defense (Penny 2002). If the nutritional value of a 25°7Ј51.00Љ W 080°17Ј31.26Љ), and Thurmond Street prey species is very low, as in some gelatinous inverte- (N 25°5Ј22.62Љ W 080°26Ј59.36Љ). Collection sites in the brates, generalist predators may choose other prey items. Bahamas were Bimini (N 25°42Ј52.86Љ W 079°17Ј36.90Љ), As a result of these considerations, inclusion of nutritional Cat Cay (N 25°31Ј51.30Љ W 079°16Ј16.62Љ), Compass Cay analyses into studies of defensive strategies has become (N 24°16Ј17.46Љ W 076°30Ј20.22Љ), Little San Salvador (N standard in recent years (Pawlik 2011). 24°34Ј16.85Љ W 075°55Ј57.77Љ), Northern Exumas (N Finally, both behavior and distribution may inXuence the 24°46Ј27.60Љ W 076°49Ј2.76Љ), San Salvador (N 24° defensive strategies used by non-scleractinian zoantharians. 9Ј4.66Љ W 074°28Ј25.94Љ), Stirrups Cay (N 25°49Ј45.51Љ Unlike some sessile organisms, soft-bodied, benthic cnidar- W 077°54Ј49.80Љ), and Sweetings Cay (N 26°33Ј39.84Љ W ians may be able to avoid predation by holding themselves 077°52Ј32.28Љ). Careful records were kept of the habitats in close to the substratum (Rupert et al. 2004). Furthermore, which species were collected, speciWcally regarding the 123 Author's personal copy Mar Biol (2012) 159:389–398
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