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Anti-predatory chemical defences in Antarctic benthic fauna

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Abstract

Antarctic benthic communities are largely structured by predation, which leads to the development of mechanisms of repellence. Among those mechanisms, chemical defences are quite extensive, yet poorly understood. To increase knowledge about the role of chemical defences in the Southern Ocean ecosystems, we assessed the incidence of feeding repellents in sessile and vagile invertebrates from nine phyla: Porifera, Cnidaria, Nemertea, Annelida, Mollusca, Bryozoa, Echinodermata, Hemichordata, and Tunicata (Ascidiacea). Samples were collected at depths of 120–789 m in the eastern Weddell Sea and Bouvet Island, and at depths ranging 0–100 m in the South Shetland Islands. When possible, specimens were dissected to study anatomical allocation of repellents. The common, eurybathic sea star Odontaster validus was chosen to perform feeding repellence bioassays, using diethyl ether (lipophilic) and butanol (hydrophilic) extracts from these samples. Among the 75 species tested, 52 % were studied for the first time for anti-predatory properties. Results provide further evidence of the prevalence of defensive metabolites in Antarctic organisms, with 47 % of the species exhibiting significant repellence within their lipophilic extracts. They also suggest a wider use of nonpolar defensive chemicals. Sessile taxa displayed highest repellence activities, with ascidians, cnidarians, and sponges being the most chemically protected. Overall, the present study indicates that natural products by mediating trophic interactions between prey and their potential predators play an important role in structuring Antarctic benthic ecosystems.

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References

  • Amsler CD, McClintock JB, Baker BJ (2000) Chemical defenses of Antarctic marine organisms: a reevaluation of the latitudinal hypothesis. In: Davidson W, Howard-Williams C, Broady P (eds) Antarctic ecosystems: models for wider ecological understanding. Proceedings of the 7th SCAR international biology symposium. New Zealand Natural Sciences, Christchurch, pp 158–164

  • Amsler CD, Iken KB, McClintock JB, Baker BJ (2001a) Secondary metabolites from Antarctic marine organisms and their ecological implications. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 267–300

  • Amsler CD, McClintock JB, Baker BJ (2001b) Secondary metabolites as mediators of trophic interactions among Antarctic marine organisms. Am Zool 41:17–26

    Article  CAS  Google Scholar 

  • Amsler CD, McClintock JB, Baker BJ (2014) Chemical mediation of mutualistic interactions between macroalgae and mesograzers structure unique coastal communities along the western Antarctic Peninsula. J Phycol 50:1–10

    Article  Google Scholar 

  • Arntz WE, Brey T, Gallardo A (1994) Antarctic zoobenthos. Oceanogr Mar Biol 32:241–304

    Google Scholar 

  • Avila C, Iken K, Fontana A, Cimino G (2000) Chemical ecology of the Antarctic nudibranch Bathydoris hodgsoni Eliot, 1907: defensive role and origin of its natural products. J Exp Mar Biol Ecol 252:27–44

    Article  CAS  Google Scholar 

  • Avila C, Taboada S, Núñez-Pons L (2008) Antarctic marine chemical ecology: What is next? Mar Ecol 29:1–71. doi:10.1111/j.1439-0485.2007.00215.x

    Article  CAS  Google Scholar 

  • Berne S, Sepčić K, Križaj I, Kem WR, McClintock JB, Turk T (2003) Isolation and characterisation of a cytolytic protein from mucus secretions of the Antarctic heteronemertine Parborlasia corrugatus. Toxicon 41:483–491. doi:10.1016/S0041-0101(02)00386-0

    Article  CAS  Google Scholar 

  • Bewley CA, Holland ND, Faulkner DJ (1996) Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52:716–722

    Article  CAS  Google Scholar 

  • Clarke A, Aronson RB, Crame JA, Gili JM, Blake DB (2004) Evolution and diversity of the benthic fauna of the Southern Ocean continental shelf. Antarct Sci 16:559–568

    Article  Google Scholar 

  • Cutignano A, Zhang W, Avila C, Cimino G, Fontana A (2011) Intrapopulation variability in the terpene metabolism of the Antarctic opisthobranch mollusc Austrodoris kerguelenensis. Eur J Org Chem 2011:5383–5389. doi:10.1002/ejoc.201100552

    Article  CAS  Google Scholar 

  • Cutignano A, De Palma R, Fontana A (2012) A chemical investigation of the Antarctic sponge Lyssodendoryx flabellata. Nat Prod Lett 26:1240–1248. doi:10.1080/14786419.2011.561493

    Article  CAS  Google Scholar 

  • Davies-Coleman MT (2006) Secondary metabolites from the marine gastropod molluscs of Antarctica, Southern Africa and South America. In: Cimino G, Gavagnin M (eds) Molluscs: from chemo-ecological study to biotechnological application, vol 43., Series: progress in molecular and subcellular biology. Subseries: marine molecular biotechnology. Springer, Berlin/Heidelberg, pp 133–157

    Chapter  Google Scholar 

  • Dayton PK, Robilliard GA, Paine RT, Dayton LB (1974) Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecol Monogr 44:105–128

    Article  Google Scholar 

  • Dayton PK, Mordida BJ, Bacon F (1994) Polar marine communities. Am Zool 34:90–99

    Google Scholar 

  • Dearborn JH (1973) Ecological studies of echinoderms and general marine collecting along the Antarctic Peninsula. Antarct J US 8:206–208

    Google Scholar 

  • Dearborn JH (1977) Foods and feeding characteristics of Antarctic asteroids and ophiuroids. In: Llano GA (ed) Adaptations within Antarctic Ecosystems. Smithsonian, Washington DC, pp 293–327

    Google Scholar 

  • Dilly PN (1988) Tube building by Cephalodiscus gracilis. J Zoo 216:465–468

    Article  Google Scholar 

  • Duffy JE, Paul AV (1992) Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333–339

    Article  Google Scholar 

  • Fairhead VA, Amsler CD, McClintock JB, Baker BJ (2005) Within-thallus variation in chemical and physical defences in two species of ecologically dominant brown macroalgae from the Antarctic Peninsula. J Exp Mar Biol Ecol 322:1–12. doi:10.1016/j.jembe.2005.01.010

    Article  CAS  Google Scholar 

  • Figuerola B, Núñez-Pons L, Moles J, Avila C (2013a) Feeding repellence in Antarctic bryozoans. Naturwissenschaften 100:1069–1081. doi:10.1007/s00114-013-1112-8

    Article  CAS  Google Scholar 

  • Figuerola B, Taboada S, Monleón-Getino T, Vázquez J, Avila C (2013b) Cytotoxic activity of Antarctic benthic organisms against the common sea urchin Sterechinus neumayeri. Oceanography 1:107. doi:10.4172/2332-2632.1000107

    Google Scholar 

  • Fontana A, Ciavatta ML, Amodeo P, Cimino G (1999) Single solution phase conformation of new antiproliferative Cembranes. Tetrahedron 55:1143–1152

    Article  CAS  Google Scholar 

  • Furrow FB, Amsler CD, McClintock JB, Baker BJ (2003) Surface sequestration of chemical feeding deterrents in the Antarctic sponge Latrunculia apicalis as an optimal defense against sea star spongivory. Mar Biol 143:443–449. doi:10.1007/s00227-003-1109-5

    Article  Google Scholar 

  • Gili JM, Arntz WE, Palanques A, Orejas C, Clarke A, Dayton PK, Isla E, Teixidó N, Rossi S, López-González PJ (2006) A unique assemblage of epibenthic sessile suspension feeders with archaic features in the high-Antarctic. Deep Sea Res Part II 53:1029–1052. doi:10.1016/j.dsr2.2005.10.021

    Article  Google Scholar 

  • Gutt J, Schickan T (1998) Epibiotic relationships in the Antarctic benthos. Antarct Sci 10:398–405. doi:10.1017/S0954102098000480

    Article  Google Scholar 

  • Hayward P (1995) Antarctic cheilostomatous bryozoa. Oxford University Press, Oxford

    Google Scholar 

  • Heine JN, McClintock JB, Slattery M, Weston J (1991) Energetic composition, biomass, and chemical defense in the common antarctic nemertean Parborlasia corrugatus Mclntosh. J Exp Mar Biol Ecol 153:15–25

    Article  Google Scholar 

  • Hines DE, Pawlik JR (2012) Assessing the antipredatory defensive strategies of Caribbean non-scleractinian zoantharians (Cnidaria): Is the sting the only thing? Mar Biol 159:389–398. doi:10.1007/s00227-011-1816-2

    Article  Google Scholar 

  • Hyman L (1955) The invertebrates: Echinodermata. McGraw-Hill, New York

    Google Scholar 

  • Janosik AM, Mahon AR, Halanych KM (2011) Evolutionary history of Southern Ocean Odontaster sea star species (Odontasteridae; Asteroidea). Polar Biol 34:575–586. doi:10.1007/s00300-010-0916-7

    Article  Google Scholar 

  • Koplovitz G, McClintock J, Amsler C, Baker B (2009) Palatability and chemical anti-predatory defenses in common ascidians from the Antarctic Peninsula. Aquat Biol 7:81–92. doi:10.3354/ab00188

    Article  Google Scholar 

  • Lebar MD, Heimbegner JL, Baker BJ (2007) Cold-water marine natural products. Nat Prod Rep 24:774–797. doi:10.1039/b516240h

    Article  CAS  Google Scholar 

  • Lindquist N, Hay ME, Fenical W (1992) Defense of ascidians and their conspicuous larvae: adult vs. larval chemical defenses. Ecol Monogr 62:547–568

    Article  Google Scholar 

  • Loh T-L, Pawlik JR (2014) Chemical defenses and resource trade-offs structure sponge communities on Caribbean coral reefs. Proc Natl Acad Sci USA 111:4151–4156. doi:10.1073/pnas.1321626111

    Article  CAS  Google Scholar 

  • López-Legentil S, Dieckmann R, Bontemps-Subielos N, Turon X, Banaigs B (2005) Qualitative variation of alkaloids in color morphs of Cystodytes (Ascidiacea). Biochem Syst Ecol 33:1107–1119. doi:10.1016/j.bse.2005.03.011

    Article  Google Scholar 

  • McClintock JB (1989) Toxicity of shallow-water Antarctic echinoderms. Polar Biol 9:461–465. doi:10.1007/BF00443234

    Article  Google Scholar 

  • McClintock JB (1994) Trophic biology of antarctic shallow-water echinoderms. Mar Ecol Prog Ser 111:191–202

    Article  Google Scholar 

  • McClintock JB, Baker BJ (1997) A review of the chemical ecology of Antarctic marine invertebrates. Integr Comp Biol 37:329–342. doi:10.1093/icb/37.4.329

    Article  CAS  Google Scholar 

  • McClintock JB, Pearse JS, Bosch I (1988) Population structure and energetics of the shallow-water antarctic sea star Odontaster validus in contrasting habitats. Mar Biol 99:235–246

    Article  Google Scholar 

  • McClintock JB, Heine J, Slattery M, Weston J (1990) Chemical bioactivity in common shallow-water Antarctic marine invertebrates. Antarct J US 25:204–206

    Google Scholar 

  • McClintock JB, Heine J, Slattery M, Weston J (1991) Biochemical and energetic composition, population biology, and chemical defense of the antarctic ascidian Cnemidocarpa verrucosa Lesson. J Exp Mar Biol Ecol 147:163–175. doi:10.1016/0022-0981(91)90180-5

    Article  CAS  Google Scholar 

  • McClintock JB, Slattery M, Baker BJ, Heine JN (1993) Chemical ecology of antarctic sponges from McMurdo Sound, Antarctica: ecological aspects. Antarct J US 28:134–135

    Google Scholar 

  • McClintock JB, Baker BJ, Slattery M, Heine JN, Bryan PJ, Jayatilake GS, Moon BH (1994) Chemotactic tube-foot responses of a spongivorous sea star Perknaster fuscus to organic extracts from Antarctic sponges. J Chem Ecol 20:859–870

    Article  CAS  Google Scholar 

  • McClintock JB, Baker BJ, Amsler CD, Barlow TL (2000) Chemotactic tube-foot responses of the spongivorous sea star Perknaster fuscus to organic extracts of sponges from McMurdo Sound, Antarctica. Antarct Sci 12:41–46

    Article  Google Scholar 

  • McClintock JB, Amsler CD, Baker BJ (2010) Overview of the chemical ecology of benthic marine invertebrates along the western Antarctic Peninsula. Integr Comp Biol 50:967–980. doi:10.1093/icb/icq035

    Article  Google Scholar 

  • Moles J, Figuerola B, Campanyà-Llovet N, Monleón-Getino T, Taboada S, Avila C (2015) Distribution patterns in Antarctic and Subantarctic echinoderms. Polar Biol 38:799–813. doi:10.1007/s00300-014-1640-5

    Article  Google Scholar 

  • Mortensen T (1936) Echinoidea and Ophiuroidea. Discovery Reports, vol 12. National Institute of Oceanography Cambridge, pp 199–348

  • Núñez-Pons L, Avila C (2014a) Defensive metabolites from Antarctic invertebrates: Does energetic content interfere with feeding repellence? Mar Drugs 12:3770–3791. doi:10.3390/md12063770

    Article  Google Scholar 

  • Núñez-Pons L, Avila C (2014b) Deterrent activities in the crude lipophilic fractions of Antarctic benthic organisms: chemical defences against keystone predators. Polar Res 33:21624

    Article  Google Scholar 

  • Núñez-Pons L, Avila C (2015) Natural products mediating ecological interactions in Antarctic benthic communities: a mini-review of the known molecules. Nat Prod Rep 32:1114–1130. doi:10.1039/C4NP00150H

    Article  Google Scholar 

  • Núñez-Pons L, Forestieri R, Nieto RM, Varela M, Nappo M, Rodríguez J, Jiménez C, Castelluccio F, Carbone M, Ramos-Esplà A, Gavagnin M, Avila C (2010) Chemical defenses of tunicates of the genus Aplidium from the Weddell Sea (Antarctica). Polar Biol 33:1319–1329. doi:10.1007/s00300-010-0819-7

    Article  Google Scholar 

  • Núñez-Pons L, Carbone M, Paris D, Melck D, Ríos P, Cristobo J, Castelluccio F, Gavagnin M, Avila C (2012a) Chemo-ecological studies on hexactinellid sponges from the Southern Ocean. Naturwissenschaften 99:353–368. doi:10.1007/s00114-012-0907-3

    Article  Google Scholar 

  • Núñez-Pons L, Carbone M, Vázquez J, Rodríguez J, Nieto RM, Varela MM, Gavagnin M, Avila C (2012b) Natural products from Antarctic colonial ascidians of the genera Aplidium and Synoicum: variability and defensive role. Mar Drugs 10:1741–1764. doi:10.3390/md10081741

    Article  Google Scholar 

  • Núñez-Pons L, Rodríguez-Arias M, Gómez-Garreta A, Ribera-Siguán A, Avila C (2012c) Feeding deterrence in Antarctic marine organisms: bioassays with the omnivore amphipod Cheirimedon femoratus. Mar Ecol Prog Ser 462:163–174. doi:10.3354/meps09840

    Article  Google Scholar 

  • Pawlik JR (2012) Antipredatory defensive roles of natural products from marine invertebrates. In: Fattorusso E, Gerwick WH, Taglialatela-Scafati O (eds) Handbook of marine natural products. Springer, Netherlands, Dordrecht, pp 677–710

    Chapter  Google Scholar 

  • Peters KJ, Amsler CD, McClintock JB, van Soest RWM, Baker BJ (2009) Palatability and chemical defenses of sponges from the western Antarctic Peninsula. Mar Ecol Prog Ser 385:77–85. doi:10.3354/meps08026

    Article  CAS  Google Scholar 

  • Pisut DP, Pawlik JR (2002) Anti-predatory chemical defenses of ascidians: Secondary metabolites or inorganic acids? J Exp Mar Biol Ecol 270:203–214. doi:10.1016/S0022-0981(02)00023-0

    Article  CAS  Google Scholar 

  • Puglisi MP, Sneed JM, Sharp KH, Ritson-Williams R, Paul VJ (2014) Marine chemical ecology in benthic environments. Nat Prod Rep 28:345–387. doi:10.1039/c0np00040j

    Google Scholar 

  • Rhoades D (1979) Evolution of plant chemical defenses against herbivores. In: Rosenthal G (ed) Herbivores: their interaction with secondary plant metabolites. Academic Press, Orlando, pp 4–55

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. Freeman WH, New York

    Google Scholar 

  • Sotka EE, Forbey J, Horn M, Poore AGB, Raubenheimer D, Whalen KE (2009) The emerging role of pharmacology in understanding consumer-prey interactions in marine and freshwater systems. Integr Comp Biol 49:291–313. doi:10.1093/icb/icp049

    Article  CAS  Google Scholar 

  • Taboada S, Núñez-Pons L, Avila C (2013) Feeding repellence of Antarctic and sub-Antarctic benthic invertebrates against the omnivorous sea star Odontaster validus. Polar Biol 36:13–25. doi:10.1007/s00300-012-1234-z

    Article  Google Scholar 

  • Thompson TE (1960) Defensive acid-secretion in marine gastropods. J Mar Biol Assoc UK 39:115–122

    Article  Google Scholar 

  • Torssel KGB (1983) Natural product chemistry. A mechanistic and biosynthetic approach to secondary metabolism. Wiley, New York

    Google Scholar 

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Acknowledgments

We thank Prof W. Arntz, T. Brey, and the crew of the R/V Polarstern for allowing our participation in the Antarctic cruises ANT XV/3 and XXI/2 (AWI, Bremerhaven, Germany). Special thanks are given to C. Angulo, M. Bas, A. Riesgo, and J. Vázquez for laboratory and field support. Also, thanks are due to M. Ballesteros, P. Ríos, M. Varela, M. Edo, N. Anadón, and A. A. Ramos-Esplá for help with the taxonomical identification of the samples. Thanks are also due to the Unidad de Tecnología Marina (CSIC), as well as the “Bentart Project” (IEO) team, the BIO-Las Palmas and the BIO-Hespérides crews, and the “Gabriel de Castilla” Spanish Antarctic Base for providing logistic support during the Antarctic cruises. We are also thankful to the editor and reviewers for their suggestions to improve the paper. Funding was provided by the Spanish government through the ECOQUIM and ACTIQUIM Projects (REN2003-00545, REN2002-12006EANT, CGL2004-03356/ANT, CGL2007-65453, and CTM2010-17415/ANT). J.M. was supported by a Grant of the Spanish Government (MEC; BES-2011-045325).

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Authors and Affiliations

  1. Department of Animal Biology (Invertebrates) and Biodiversity Research Institute (IrBIO), Faculty of Biology, University of Barcelona, Av. Diagonal 643, 08028, Barcelona, Spain

    Juan Moles, Laura Núñez-Pons, Sergi Taboada, Blanca Figuerola & Conxita Avila

  2. Hawai’i Institute of Marine Biology, University of Hawaii, 46-007 Lilipuna Rd., Kaneohe, HI, 96744, USA

    Laura Núñez-Pons

  3. Spanish Institute of Oceanography (IEO), Oceanographic Centre of Gijón, Av. Príncipe de Asturias 70 bis, 33212, Gijón, Spain

    Javier Cristobo

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  1. Juan Moles
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Correspondence to Juan Moles.

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Communicated by P. Gagnon.

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Moles, J., Núñez-Pons, L., Taboada, S. et al. Anti-predatory chemical defences in Antarctic benthic fauna. Mar Biol 162, 1813–1821 (2015). https://doi.org/10.1007/s00227-015-2714-9

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