Abstract
The relative importance of chemical, nematocyst, and nutritional defenses was examined for 18 species of Caribbean sea anemones (actinarians), zoanthids, and mushroom polyps (corallimorpharians) from the Florida Keys and the Bahamas Islands, 2008–2010. Feeding assays were performed using the fish Thalassoma bifasciatum with artificial foods containing crude organic extracts of cnidarian tissues. A novel behavioral assay using brine shrimp nauplii was used to assess nematocyst defenses. The nutritional quality of cnidarian tissues was examined using bomb calorimetry and soluble protein assays. In general, actinarians invested in nematocyst defenses, zoanthids in either nematocyst or chemical defenses, and corallimorpharians lacked both, except for 1 of 3 species that was chemically defended. Relative to other coral reef invertebrates, cnidarian tissues had similar caloric values but lower soluble protein concentrations. Trade-offs between chemical and nematocyst defenses were observed for 65% of species, while habitat and behavior provided a likely explanation for undefended species.
Similar content being viewed by others
References
Alvarez C, Macheno JM, Martinez D, Tejuca M, Pazos F, Lanio ME (2009) Sticholysins, two pore-forming toxins produced by the Caribbean Sea anemone Stichodactyla helianthus: their interaction with membranes. Toxicon 54:1135–1147
Anderluh G, Maček P (2002) Cytolytic peptide and protein toxins from sea anemones (Anthozoa: Actiniaria). Toxicon 40:111–124
Ballhorn DJ, Pietrowski A, Lieberei R (2010) Direct trade-off between cyanogenesis and resistance to a fungal pathogen in lima bean (Phaseolus lunatus L.). J Ecol 98:226–236
Basulto A, Perez VM, Noa Y, Varela C, Otero AJ, Pico MC (2006) Immunohistochemical targeting of sea anemone cytolysins on tentacles, mesenteric filaments and isolated nematocysts of Stichodactyla helianthus. J Exp Zool 305A:253–258
Chanas B, Pawlik JR (1995) Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Mar Ecol Prog Ser 127:195–211
Daly M, Fautin DG, Cappola VA (2003) Systematics of the hexacorallia (Cnidaria: Anthozoa). Zool J Linn Soc Lond 139:419–437
Duffy JE, Paul VY (1992) Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333–339
Dunlap M, Pawlik JR (1996) Video-monitored predation by Caribbean reef fishes on an array of mangrove and reef sponges. Mar Biol 126:117–123
Dunlap M, Pawlik JR (1998) Spongivory by parrotfish in Florida mangrove and reef habitats. Mar Ecol PSZNI 19:325–337
Dunn DF (1982) Sexual reproduction of two intertidal sea anemones (Coelenterata: Actiniaria) in Malaysia. Biotropica 14:262–271
England KW (1991) Nematocysts of sea anemones (Actiniaria, Ceriantharia and Corallimorpharia: Cnidaria): nomenclature. Hydrobiologia 216:691–697
Fautin DG (1988) Importance of nematocysts to Actinian taxonomy. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press Inc, London, pp 487–500
Fautin DG (2009) Structural diversity, systematics, and evolution of cnidae. Toxicon 54:1054–1064
Felton GW, Korth KL (2000) Trade-offs between pathogen and herbivore resistance. Curr Opin Plant Biol 3:309–314
Ford CE (1964) Reproduction in the aggregating sea anemone, Anthopleura elegantissima. Pac Sci 18:138–145
Hamner WM, Dunn DF (1980) Tropical corallimorpharia (Ceolenterata: Anthozao): feeding by envelopment. Micronesica Ser 16:34–41
Harborne AR, Renaud RG, Tyler EHM, Mumby PJ (2009) Reduced density of the herbivorous urchin Diadema antillarum inside a Caribbean marine reserve linked to increased predation pressure by fishes. Coral Reefs 28:783–791
Hill MS (1998) Spongivory on Caribbean reefs releases corals from competition with sponges. Oecologia 117:143–150
Humann P, DeLoach N (2002) Phylum Cnidaria. In: Delaoch N (ed) Reef creature identification Florida Caribbean Bahamas. New World Publishing Inc, pp 62–125
Kaplan I, Dively GP, Denno RF (2009) The costs of anti-herbivore defense traits in agricultural crop plants: a case study involving leafhoppers and trichomes. Ecol Appl 19:864–872
León YM, Bjorndal KA (2002) Selective feeding in the hawksbill turtle, an important predator in coral reef ecosystems. Mar Ecol Prog Ser 245:249–258
Leong W, Pawlik JR (2010a) Evidence of a resource trade-off between growth and chemical defenses among Caribbean coral reef sponges. Mar Ecol Prog Ser 406:71–78
Leong W, Pawlik JR (2010b) Fragments or propagules? Reproductive tradeoffs among Callyspongia spp. from Florida coral reefs. Oikos 119:1417–1422
Loh T, Pawlik JR (2009) Bitten down to size: fish predation determines growth form of the Caribbean coral reef sponge Mycale laevis. J Exp Mar Biol Ecol 374:45–50
Mariscal RN (1974) Nematocysts. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology: reviews and new perspectives. Academic Press, New York, pp 129–178
Martinez D, Morera V, Alvarez C, Tejuca M, Pazos F, Garcia Y, Raida M, Padron G, Lanio ME (2002) Identity between cytolysins purified from two morphos of the Caribbean sea anemone Stichodactyla helianthus. Toxicon 40:1219–1221
Millikin MR (1982) Qualitative and quantitative nutrient requirements of reef fishes. Fish B-NOAA 80:655–686
Moore RE, Scheuer PJ (1971) Palytoxin: a new marine toxin from a coelenterate. Science 172:495–498
O’Neal W, Pawlik JR (2002) A reappraisal of the chemical and physical defenses of Caribbean gorgonian corals against predatory fishes. Mar Ecol Prog Ser 240:117–126
Parker GM (1984) Dispersal of zooxanthellae on coral reefs by predators on cnidarians. Biol Bull 167:159–167
Pawlik JR (1998) Coral reef sponges: do predatory fishes affect their distribution? Limnol Oceanogr 46:1396–1399
Pawlik JR (2011) Antipredatory defensive roles of natural products from marine invertebrates. In: Fattorusso E, Gerwick W, Taglialatella-Scafati O (eds) Handbook of marine natural products. CRC Press, Boca Raton
Pawlik JR, Burch MT, Fenical W (1987) Patterns of chemical defense among Caribbean gorgonian corals: a preliminary survey. J Exp Mar Biol Ecol 108:55–66
Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar Ecol Prog Ser 127:183–194
Pawlik JR, Henkel TP, McMurray SE, Lopez-Legentil S, Loh T-L, Rohde S (2008) Patterns of sponge recruitment and growth on a shipwreck corroborate chemical defense resource trade-off. Mar Ecol Prog Ser 268:137–143
Penny BK (2002) Lowered nutritional quality supplements nudibranch chemical defense. Oecologia 132:411–418
Pisut DP, Pawlik JR (2002) Anti-predatory chemical defenses of ascidians: secondary metabolites or inorganic acids. J Exp Mar Biol Ecol 270:203–214
Randall JE (1967) Food habits of reef fishes of the West Indies. Stud Trop Oceanogr 5:665–847
Rupert EE, Fox RS, Barns RD (2004) Cnidaria. In: Rupert EE, Fox RS, Barns RD (eds) Invertebrate zoology: a functional evolutionary approach, 7th edn. Thompson Brooks/Cole, London, pp 111–176
Sloan NA (1980) Aspects of the feeding biology of asteroids. Oceanogr Mar Biol Annu Rev 18:57–124
Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA 104:18842–18847
Stachowicz JJ, Lindquist N (2000) Hydroid defenses against predators: the importance of secondary metabolites versus nematocysts. Oecologia 124:280–288
Stampar SN, da Silva PF, Luiz OJ (2007) Predation on the Zoanthid Palythoa caribaeorum (Anthozoa, Cnidaria) by a hawksbill turtle (Eretmochelys imbricata) in Southeastern Brazil. Mar Turtle Newslett 117:3–5
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Thorington GU, Hessinger DA (1996) Efferent mechanisms of discharging cnidae: I. measurements of intrinsic adherence of cnidae discharged from tentacles of the sea anemone, Aiptasia pallida. Biol Bull 190:125–138
Thorington GU, Hessinger DA (1998) Efferent mechanisms of discharging cnidae: II. A nematocyst release response in the sea anemone tentacle. Biol Bull 195:145–155
Van der Mejden E, van Bemmelen M, Kooi R, Post BJ (1984) Nutritional quality and chemical defence in the ragwort-cinnabar moth interaction. J Anim Ecol 53:443–453
Walters KD, Pawlik JR (2005) Is there a trade-off between wound-healing and chemical defenses among Caribbean reef sponges? Integr Comp Biol 45:352–358
Watson GM, Mire P, Hudson RR (1998) Frequency specificity of vibration dependent discharge of nematocysts in sea anemones. J Exp Zool 281:582–593
Wood R (1993) Nutrients, predation and the history of reef-building. Palaios 8:526–554
Work TM, Aeby GS, Maragos JE (2008) Phase shift from a coral to a corallimorph-dominated reef associated with a shipwreck on Palmyra Atoll. PLoS one 3:e2989
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall Inc, Englewood Cliffs, pp 224–225
Zera AJ, Harshman LG (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32:95–126
Acknowledgments
This study was funded by grants from the National Undersea Research Program at UNCW (NOAA NA96RU-0260) and from the National Science Foundation Biological Oceanography Program (OCE-0550468, OCE-1029515), as well as the UNCW Brauer Fellowship Award. Thanks to Michael Echevarria, Tim Henkel, Wai Leong, Tiffany Lewis, Tse-Lynn Loh, Dr. Susanna López-Legentil, Steven McMurray, Andrew Miller, Jan Vicente, and Colin Foord for assistance in collecting specimens. We would also like to thank the anonymous reviewers who helped to improve this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by T. L. Goulet.
Rights and permissions
About this article
Cite this article
Hines, D.E., Pawlik, J.R. Assessing the antipredatory defensive strategies of Caribbean non-scleractinian zoantharians (Cnidaria): is the sting the only thing?. Mar Biol 159, 389–398 (2012). https://doi.org/10.1007/s00227-011-1816-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-011-1816-2