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Turning the game around: toxicity in a nudibranch-sponge predator–prey association

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Abstract

Escalation theory proposes enemy-related selection as the most relevant factor of natural selection among individual organisms. When hazardous to predators, prey might be considered enemies that influence predator evolution. Opisthobranch molluscs that prey on chemically defended prey are an interesting study case on this subject. Predation on chemically defended species paved the way for opisthobranchs to enter in an arms race, developing means to detoxify and/or excrete harmful compounds, which led to the sequestration of those compounds and their self-defensive use, an escalation of defenses. Here we aim to understand whether the opisthobranch predator is better protected than its chemically defended prey, using as predator–prey model, a nudibranch (Hypselodoris cantabrica) and the sponge it preys upon (Dysidea fragilis), and from which it obtains deterrent chemical compounds. Specimens of both species were collected on the Portuguese coast, and their crude extracts were analyzed and used in palatability tests. Nudibranchs revealed a higher natural concentration of crude extract, probably due to a progressive accumulation of the compounds. Both predator and prey extracts revealed similar mixtures of deterrent metabolites (furanosesquiterpenes). Palatability tests revealed a more effective deterrence in the nudibranch extracts because significant rejection rates were observed at lower concentrations than those necessary for the sponge extracts to have the same effect. We concluded that the predator is chemically better protected than its prey, which suggests that its acquisition of chemical defenses reveals a defensive escalation.

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References

  • Avila C (1995) Natural products of Opisthobranch Molluscs: a biological review. Oceanogr Mar Biol Annu Rev 33:487–559

    Google Scholar 

  • Avila C, Cimino G, Fontana A, Gavagnin M, Ortea J, Trivellone E (1991) Defensive strategy of two Hypselodoris nudibranchs from Italian and Spanish coasts. J Chem Ecol 17(3):625–636

    Article  CAS  Google Scholar 

  • Brodie ED (1999) Predator–prey arms races. Bioscience 49(7):557–568

    Article  Google Scholar 

  • Carte B, Faulkner DJ (1986) Role of secondary metabolites in feeding associations between a predatory nudibranch, 2 grazing nudibranchs, and a bryozoan. J Chem Ecol 12(3):795–804

    Article  CAS  Google Scholar 

  • Cimino G, Ghiselin MT (1999) Chemical defense and evolutionary trends in biosynthetic capacity among dorid nudibranchs (Mollusca: Gastropoda: Opisthobranchia). Chemoecology 9:187–207

    Article  CAS  Google Scholar 

  • Cimino G, Derosa S, Destefano S, Sodano G, Villani G (1983) Dorid nudibranch elaborates its own chemical defense. Science 219(4589):1237–1238

    Article  PubMed  CAS  Google Scholar 

  • Cimino G, Ghiselin MT (2001) Marine natural products chemistry as an evolutionary narrative. In: McClintock JB, Baker BJ (eds) Marine chemical ecology, CRC Press LLC, pp 115–154

  • Cimino G, Ghiselin MT (2009) Chemical defense and the evolution of opisthobranch gastropods. Proc Calif Acad Sci 60(10):175–422

    Google Scholar 

  • Cimino G, Fontana A, Gimenez F, Marin A, Mollo E, Trivellone E, Zubia E (1993) Biotransformation of a dietary sesterterpenoid in the Mediterranean nudibranch Hypselodoris orsini. Experientia 49(6–7):582–586

    Article  CAS  Google Scholar 

  • Cortesi F, Cheney KL (2010) Conspicuousness is correlated with toxicity in marine opisthobranchs. J Evol Biol 23(7):1509–1518. doi:10.1111/j.1420-9101.2010.02018.x

    Article  PubMed  CAS  Google Scholar 

  • Cronin G, Hay ME, Fenical W, Lindquist N (1995) Distribution, density, and sequestration of host chemical defenses by the specialist nudibranch Tritonia hamnerorum found at high-densities on the sea fan Gorgonia ventalina. Mar Ecol Prog Ser 119(1–3):177–189

    Article  CAS  Google Scholar 

  • Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B 205(1161):489–511

    Article  PubMed  CAS  Google Scholar 

  • de Nys R, Steinberg PD, Rogers CN, Charlton TS, Duncan MW (1996) Quantitative variation of secondary metabolites in the sea hare Aplysia parvula and its host plant, Delisea pulchra. Mar Ecol Prog Ser 130(1–3):135–146

    Article  CAS  Google Scholar 

  • Dietl GP, Kelley PH (2002) The fossil record of predator–prey arms races: coevolution and escalation hypotheses. Paleontol Soc Pap 8:353–374

    Google Scholar 

  • Faulkner DJ, Ghiselin MT (1983) Chemical defense and evolutionary ecology of dorid nudibranchs and some other opisthobranch gastropods. Mar Ecol Prog Ser 13(2–3):295–301

    Article  Google Scholar 

  • Fontana A, Avila C, Martínez E, Ortea J, Trivellone E, Cimino G (1993) Defensive allomones in three species of Hypselodoris (Gastropoda: Nudibranchia) from the Cantabrian Sea. J Chem Ecol 19(2):339–356

    Article  CAS  Google Scholar 

  • García-Gómez JC, Cimino G, Medina A (1990) Studies on defensive behaviour of Hypselodoris species (Gastropoda: Nudibranchia): ultrastructure and chemical analysis of mantle dermal formations (MDFs). Mar Biol 106:245–250

    Article  Google Scholar 

  • García-Gómez JC, Medina A, Covenas R (1991) Study of the anatomy and histology of the mantle dermal formations (Mdfs) of Chromodoris and Hypselodoris (Opisthobranchia, Chromodorididae). Malacologia 32(2):233–240

    Google Scholar 

  • Ginsburg DW, Paul VJ (2001) Chemical defenses in the sea hare Aplysia parvula: importance of diet and sequestration of algal secondary metabolites. Mar Ecol Prog Ser 215:261–274

    Article  CAS  Google Scholar 

  • Gosliner T (2001) Aposematic coloration and mimicry in opistobranch mollusks: new phylogenetic and experimental data. Boll Malacol 37(5–8):163–170

    Google Scholar 

  • Gould SJ, Vrba ES (1982) Exaptation: a missing term in the science of form. Paleobiology 8(1):4–15

    Google Scholar 

  • Haber M, Cerfeda S, Carbone M, Calado G, Gaspar H, Neves R, Maharajan V, Cimino G, Gavagnin M, Ghiselin MT, Mollo E (2010) Coloration and defense in the nudibranch gastropod Hypselodoris fontandraui. Biol Bull (Woods Hole) 218(2):181–188

    Google Scholar 

  • Henry LA, Hart M (2005) Regeneration from injury and resource allocation in sponges and corals: a review. Int Rev of Hydrobiol 90(2):125–158. doi:10.1002/iroh.200410759

    Article  Google Scholar 

  • Marin A, Lopez D, Esteban MA, Meseguer J, Munoz J, Fontana A (1998) Anatomical and ultrastructural studies of chemical defence in the sponge Dysidea fragilis. Mar Biol 131(4):639–645

    Article  CAS  Google Scholar 

  • Mollo E, Gavagnin M, Carbone M, Castelluccio F, Pozone F, Roussis V, Templado J, Ghiselin MT, Cimino G (2008) Factors promoting marine invasions: A chemoecological approach. Proc Natl Acad Sci USA 105(12):4582–4586

    Article  PubMed  CAS  Google Scholar 

  • Opitz SEW, Muller C (2009) Plant chemistry and insect sequestration. Chemoecology 19(3):117–154. doi:10.1007/s00049-009-0018-6

    Article  CAS  Google Scholar 

  • Pawlik JR, Kernan MR, Molinski TF, Harper MK, Faulkner DJ (1988) Defensive chemicals of the Spanish dancer nudibranch Hexabranchus sanguineus and its egg ribbons: macrolides derived from a sponge diet. J Exp Mar Biol Ecol 119(2):99–109

    Article  CAS  Google Scholar 

  • Ros J (1976) Sistemas de defensa en los opistobranquios. Oecol Aquat 2:41–77

    Google Scholar 

  • Ros J (1977) La defensa en los opistobranquios. Investigación y Ciencia 12:48–60

    Google Scholar 

  • Rudman WB (1991) Purpose in pattern: the evolution of colour in chromodorid nudibranchs. J Molluscan Stud 57:5–21

    Google Scholar 

  • Rudman WB, Bergquist PR (2007) A review of feeding specificity in the sponge-feeding Chromodorididae (Nudibranchia : Mollusca). Molluscan Res 27(2):60–88

    Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack, the evolutionary ecology of crypsis, warning signals and mimicry, 1st edn. Oxford University Press, New York

    Google Scholar 

  • Schulte G, Scheuer PJ (1980) Two furanosesquiterpene marine metabolites with antifeedant properties. Helv Chim Acta 63(8):2159–2167

    Article  CAS  Google Scholar 

  • Thompson TE (1960) Defensive adaptations in opistobranchs. J Mar Biol Ass UK 39(1):123–134

    Article  Google Scholar 

  • Vermeij GJ (1987) Evolution and escalation: an ecological history of life. Princeton University Press, New Jersey

    Google Scholar 

  • Vermeij GJ (1994) The evolutionary interaction among species: selection, escalation, and coevolution. Annu Rev Ecol Syst 25:219–236

    Article  Google Scholar 

  • Wagele H, Klussmann-Kolb A (2005) Opisthobranchia (Mollusca, Gastropoda): more than just slimy slugs. Shell reduction and its implications on defence and foraging. Front Zool 2:3

    Article  PubMed  Google Scholar 

  • Wagele H, Ballesteros M, Avila C (2006) Defensive glandular structures in opisthobranch molluscs—From histology to ecology. Oceanogr Mar Biol Annu Rev 44:197–276

    Google Scholar 

  • Zar J (1999) Biostatistical analysis, 4th edn. Prentice Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

The authors thank the technical support of Laboratório Nacional de Energia e Geologia staff, especially Filomena Costa. The authors also thank Sasha Vasconcelos, for the English review and an anonymous reviewer who made several suggestions that improved the manuscript. This study was developed under the Fundação para a Ciência e Tecnologia project PTDC/MAR/65854/2006 and the Fundação para a Ciência e Tecnologia/Consiglio Nazionale delle Ricerche bilateral project FCUL-ICB 2009/2010.

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Correspondence to João Filipe da Cruz.

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da Cruz, J.F., Gaspar, H. & Calado, G. Turning the game around: toxicity in a nudibranch-sponge predator–prey association. Chemoecology 22, 47–53 (2012). https://doi.org/10.1007/s00049-011-0097-z

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