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Marine Biology

, Volume 159, Issue 2, pp 389–398 | Cite as

Assessing the antipredatory defensive strategies of Caribbean non-scleractinian zoantharians (Cnidaria): is the sting the only thing?

  • David E. Hines
  • Joseph R. Pawlik
Original Paper

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.

Keywords

Coral Reef Reef Fish Chemical Defense Soluble Protein Content Defensive Mechanism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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.

References

  1. 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 54:1135–1147CrossRefGoogle Scholar
  2. Anderluh G, Maček P (2002) Cytolytic peptide and protein toxins from sea anemones (Anthozoa: Actiniaria). Toxicon 40:111–124CrossRefGoogle Scholar
  3. 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 98:226–236CrossRefGoogle Scholar
  4. 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:253–258CrossRefGoogle Scholar
  5. Chanas B, Pawlik JR (1995) Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Mar Ecol Prog Ser 127:195–211CrossRefGoogle Scholar
  6. Daly M, Fautin DG, Cappola VA (2003) Systematics of the hexacorallia (Cnidaria: Anthozoa). Zool J Linn Soc Lond 139:419–437CrossRefGoogle Scholar
  7. Duffy JE, Paul VY (1992) Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333–339CrossRefGoogle Scholar
  8. Dunlap M, Pawlik JR (1996) Video-monitored predation by Caribbean reef fishes on an array of mangrove and reef sponges. Mar Biol 126:117–123CrossRefGoogle Scholar
  9. Dunlap M, Pawlik JR (1998) Spongivory by parrotfish in Florida mangrove and reef habitats. Mar Ecol PSZNI 19:325–337CrossRefGoogle Scholar
  10. Dunn DF (1982) Sexual reproduction of two intertidal sea anemones (Coelenterata: Actiniaria) in Malaysia. Biotropica 14:262–271CrossRefGoogle Scholar
  11. England KW (1991) Nematocysts of sea anemones (Actiniaria, Ceriantharia and Corallimorpharia: Cnidaria): nomenclature. Hydrobiologia 216:691–697CrossRefGoogle Scholar
  12. Fautin DG (1988) Importance of nematocysts to Actinian taxonomy. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press Inc, London, pp 487–500Google Scholar
  13. Fautin DG (2009) Structural diversity, systematics, and evolution of cnidae. Toxicon 54:1054–1064CrossRefGoogle Scholar
  14. Felton GW, Korth KL (2000) Trade-offs between pathogen and herbivore resistance. Curr Opin Plant Biol 3:309–314CrossRefGoogle Scholar
  15. Ford CE (1964) Reproduction in the aggregating sea anemone, Anthopleura elegantissima. Pac Sci 18:138–145Google Scholar
  16. Hamner WM, Dunn DF (1980) Tropical corallimorpharia (Ceolenterata: Anthozao): feeding by envelopment. Micronesica Ser 16:34–41Google Scholar
  17. 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 28:783–791CrossRefGoogle Scholar
  18. Hill MS (1998) Spongivory on Caribbean reefs releases corals from competition with sponges. Oecologia 117:143–150CrossRefGoogle Scholar
  19. Humann P, DeLoach N (2002) Phylum Cnidaria. In: Delaoch N (ed) Reef creature identification Florida Caribbean Bahamas. New World Publishing Inc, pp 62–125Google Scholar
  20. 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 19:864–872CrossRefGoogle Scholar
  21. León YM, Bjorndal KA (2002) Selective feeding in the hawksbill turtle, an important predator in coral reef ecosystems. Mar Ecol Prog Ser 245:249–258CrossRefGoogle Scholar
  22. 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 406:71–78CrossRefGoogle Scholar
  23. Leong W, Pawlik JR (2010b) Fragments or propagules? Reproductive tradeoffs among Callyspongia spp. from Florida coral reefs. Oikos 119:1417–1422CrossRefGoogle Scholar
  24. 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 374:45–50CrossRefGoogle Scholar
  25. Mariscal RN (1974) Nematocysts. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology: reviews and new perspectives. Academic Press, New York, pp 129–178Google Scholar
  26. 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 40:1219–1221CrossRefGoogle Scholar
  27. Millikin MR (1982) Qualitative and quantitative nutrient requirements of reef fishes. Fish B-NOAA 80:655–686Google Scholar
  28. Moore RE, Scheuer PJ (1971) Palytoxin: a new marine toxin from a coelenterate. Science 172:495–498CrossRefGoogle Scholar
  29. 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 240:117–126CrossRefGoogle Scholar
  30. Parker GM (1984) Dispersal of zooxanthellae on coral reefs by predators on cnidarians. Biol Bull 167:159–167CrossRefGoogle Scholar
  31. Pawlik JR (1998) Coral reef sponges: do predatory fishes affect their distribution? Limnol Oceanogr 46:1396–1399CrossRefGoogle Scholar
  32. 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 RatonGoogle Scholar
  33. Pawlik JR, Burch MT, Fenical W (1987) Patterns of chemical defense among Caribbean gorgonian corals: a preliminary survey. J Exp Mar Biol Ecol 108:55–66CrossRefGoogle Scholar
  34. Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar Ecol Prog Ser 127:183–194CrossRefGoogle Scholar
  35. 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 268:137–143CrossRefGoogle Scholar
  36. Penny BK (2002) Lowered nutritional quality supplements nudibranch chemical defense. Oecologia 132:411–418CrossRefGoogle Scholar
  37. Pisut DP, Pawlik JR (2002) Anti-predatory chemical defenses of ascidians: secondary metabolites or inorganic acids. J Exp Mar Biol Ecol 270:203–214CrossRefGoogle Scholar
  38. Randall JE (1967) Food habits of reef fishes of the West Indies. Stud Trop Oceanogr 5:665–847Google Scholar
  39. 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 111–176Google Scholar
  40. Sloan NA (1980) Aspects of the feeding biology of asteroids. Oceanogr Mar Biol Annu Rev 18:57–124Google Scholar
  41. Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA 104:18842–18847CrossRefGoogle Scholar
  42. Stachowicz JJ, Lindquist N (2000) Hydroid defenses against predators: the importance of secondary metabolites versus nematocysts. Oecologia 124:280–288CrossRefGoogle Scholar
  43. 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 117:3–5Google Scholar
  44. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  45. 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 190:125–138CrossRefGoogle Scholar
  46. Thorington GU, Hessinger DA (1998) Efferent mechanisms of discharging cnidae: II. A nematocyst release response in the sea anemone tentacle. Biol Bull 195:145–155CrossRefGoogle Scholar
  47. 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 53:443–453CrossRefGoogle Scholar
  48. Walters KD, Pawlik JR (2005) Is there a trade-off between wound-healing and chemical defenses among Caribbean reef sponges? Integr Comp Biol 45:352–358CrossRefGoogle Scholar
  49. Watson GM, Mire P, Hudson RR (1998) Frequency specificity of vibration dependent discharge of nematocysts in sea anemones. J Exp Zool 281:582–593CrossRefGoogle Scholar
  50. Wood R (1993) Nutrients, predation and the history of reef-building. Palaios 8:526–554CrossRefGoogle Scholar
  51. 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:e2989CrossRefGoogle Scholar
  52. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall Inc, Englewood Cliffs, pp 224–225Google Scholar
  53. Zera AJ, Harshman LG (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32:95–126CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Biology and Marine Biology, Center for Marine ScienceUniversity of North Carolina WilmingtonWilmingtonUSA

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