Skip to main content
Log in

Biogeography of sponge chemical ecology: comparisons of tropical and temperate defenses

  • Community Ecology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Examples from both marine and terrestrial systems have supported the hypothesis that predation is higher in tropical than in temperate habitats and that, as a consequence, tropical species have evolved more effective defenses to deter predators. Although this hypothesis was first proposed for marine sponges over 25 years ago, our study provides the first experimental test of latitudinal differences in the effectiveness of sponge chemical defenses. We collected 20 common sponge species belonging to 14 genera from tropical Guam and temperate Northeast Spanish coasts (Indo-Pacific and Mediterranean biogeographic areas) and conducted field-based feeding experiments with large and small fish predators in both geographic areas. We use the term global deterrence to describe the deterrent activity of a sponge extract against all of the predators used in our experiments and to test the hypothesis that sponges from Guam are chemically better defended than their Mediterranean counterparts. Sympatric and allopatric deterrence refer to the average deterrent activity of a sponge against sympatric or allopatric predators. All of the sponges investigated in this study showed deterrent properties against some predators. However, 35% of the sponge species were deterrent in at least one but not in all the experiments, supporting the idea that predators can respond to chemical defenses in a species-specific manner. Tropical and temperate sponges have comparable global, sympatric, and allopatric deterrence, suggesting not only that chemical defenses from tropical and temperate sponges are equally strong but also that they are equally effective against sympatric and allopatric predators. Rather than supporting geographic trends in the production of chemical defenses, our data suggest a recurrent selection for chemical defenses in sponges as a general life-history strategy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

References

  • Adler FR, Harvell CD (1990) Inducible defenses, phenotypic variability and biotic environments. Trends Ecol Evol 5:407–410

    Google Scholar 

  • Amesbury SS, Myers RF (1982) Guide to the coastal resources of Guam, Volume 1: The fishes. University of Guam Marine Laboratory, Mangilao, Guam

    Google Scholar 

  • Bakus GJ, Green G (1974) Toxicity in sponges and holothurians: a geographic pattern. Science 185:951–953

    Google Scholar 

  • Becerro MA, Turon X, Uriz MJ (1995) Natural variation of toxicity in the encrusting sponge Crambe crambe (Schmidt) in relation to size and environment. J Chem Ecol 21:1931–1946

    CAS  Google Scholar 

  • Becerro MA, Turon X, Uriz MJ (1997) Multiple functions for secondary metabolites in marine encrusting organisms. J Chem Ecol 23:1527–1547

    CAS  Google Scholar 

  • Becerro MA, Paul VJ, Starmer J (1998) Intraspecimen variation in chemical defenses of the sponge Cacospongia sp. and its consequences on generalist fish predators and the specialist nudibranchs predator Glossodoris pallida. Mar Ecol Prog Ser 168:187–196

    Google Scholar 

  • Berenbaum M (1983) Coumarins and caterpillars: A case for coevolution. Evolution 37:163–179

    CAS  Google Scholar 

  • Bertness MD, Garrity SD, Levings SC (1981) Predation pressure and gastropod foraging: a tropical-temperate comparison. Evolution 35:995–1007

    Google Scholar 

  • Bolser RC, Hay ME (1996) Are tropical plants better defended? Palatability and defenses of temperate vs tropical seaweeds. Ecology 77:2269–2286

    Google Scholar 

  • Boury-Esnault N, Pansini M, Uriz MJ (1994) Spongiaires bathyaux de la mer d'Alboran et du golfe ibéro-marocain. Mem Mus Natl Hist Nat Paris 160:1–174

    Google Scholar 

  • Cambie RC, Rutledge PS, Yang XS, Bergquist PR (1998) Chemistry of sponges 18. 12-desacetylfuroscalar-16-one, a new sesterterpene from a Cacospongia sp. J Nat Prod 61:1416–1417

    Article  CAS  PubMed  Google Scholar 

  • Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Monogr 56:345–365

    Google Scholar 

  • Carpenter RC (1997) Invertebrate predators and grazers. In: Birkeland C (ed) Life and death of coral reefs. Chapman and Hall, New York, pp 198–229

  • Cetrulo GL, Hay ME (2000) Activated chemical defenses in tropical versus temperate seaweeds. Mar Ecol Prog Ser 207:243–253

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Cimino G, Ghishelin MT (1998) Chemical defence and evolution in the Sacoglossa (Mollusca: Gastropoda: Opisthobranchia). Chemoecology 8:51–60

    CAS  Google Scholar 

  • Coates M (1998) A comparison of intertidal assemblages on exposed and sheltered tropical and temperate rocky shores. Global Ecol Biogeogr 7:115–124

    Google Scholar 

  • Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–233

    Google Scholar 

  • Coley PD, Aide TM (1991) Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 25–49

    Google Scholar 

  • Crawley MJ (1983) Herbivory: the dynamics of animal-plant interactions. Blackwell, Oxford

  • Cronin G, Hay ME (1996) Within-plant variance in seaweed chemical defenses: Optimal defense theory versus the growth-differentiation hypothesis. Oecologia 105:361–368

    Google Scholar 

  • Cronin G, Paul VJ, Hay ME, Fenical W (1997) Are tropical herbivores more resistant than temperate herbivores to seaweed chemical defenses? Diterpenoid metabolites from Dictyota acutiloba as feeding deterrents for tropical versus temperate fishes and urchins. J Chem Ecol 23:289–302

    CAS  Google Scholar 

  • Davidson BS (1993) Variation in the secondary metabolites of the sponge Dysidea cf. avara. M.S. thesis, University of Guam

  • Dimock EJ II, Silen RR, Allen VE (1976) Genetic resistance in Douglas-fir to damage by snowshoe hare and black-tailed deer. For Sci 22:106–121

    Google Scholar 

  • Dobzhansky T (1950) Evolution in the tropics. Am Sci 38:208–221

    Google Scholar 

  • Faulkner DJ (1984) Marine Natural Products: metabolites of marine algae and herbivorous marine mollusks. Nat Prod Rep 1:251–280

    CAS  Google Scholar 

  • Faulkner DJ (2000) Marine Natural Products. Nat Prod Rep 17:7–55

    CAS  PubMed  Google Scholar 

  • Feeny P (1991) Chemical constraints on the evolution of swallowtail butterflies. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 315–340

    Google Scholar 

  • Fenical W (1980) Distributional and taxonomic features of toxin-producing marine algae. In: Abbott IA, Foster MS, Eklund LF (eds) Pacific Seaweed Aquaculture. California Sea Grant College Program, Institute of Marine Resources, University of California, La Jolla, Calif., pp 144–151

  • Green G (1977) Ecology of toxicity in marine sponges. Mar Biol 40:207–215

    Google Scholar 

  • Harvell CD (1990) The ecology and evolution of inducible defenses. Q Rev Biol 65:323–341

    CAS  PubMed  Google Scholar 

  • Harvell CD, Fenical W, Roussis V, Ruesink JL, Griggs CC, Greene CH (1993) Local and geographic variation in the defensive chemistry of a West Indian gorgonian coral (Briaerum asbestinum). Mar Ecol Prog Ser 93:165–173

    CAS  Google Scholar 

  • Hay ME (1991) Fish-seaweed interactions on coral reefs: effects of herbivorous fishes and adaptations of their prey. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic, San Diego, pp 96–119

  • Hay ME (1996) Marine chemical ecology: what's known and what's next? J Exp Mar Biol Ecol 200:103–134

    CAS  Google Scholar 

  • Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145

    Article  Google Scholar 

  • Hiatt RW, Strasburg DW (1960) Ecological relationships of the fish fauna on coral reefs of the Marshall Islands. Ecol Monogr 30:65–127

    Google Scholar 

  • Hixon MA (1997) Effects of reef fishes on corals and algae. In: Birkeland C (ed) Life and death of coral reefs. Chapman and Hall, New York, pp 230–248

  • Huston M (1979) A general hypothesis of species diversity. Am Nat 113:81–101

    Article  Google Scholar 

  • Jares-Erijman EA, Ingrum AL, Carney JR, Rinehart KL, Sakai R (1993) Polycyclic guanidine-containing compounds from the Mediterranean sponge Crambe crambe: the structure of 13, 14, 15-isocrambescidin 800 and the absolute stereochemistry of the pentacyclic guanidine moieties of the crambescidins. J Org Chem 58:4805–4808

    CAS  Google Scholar 

  • Kelly M, Hooper JNA, Paul VJ, Paulay G, van Soest RWM, de Weerdt W (2000) Taxonomic inventory of sponges (Porifera) of the Mariana Islands. Micronesica (in press)

  • Kinnel RB, Gehrken HP, Swali R, Skoropowski G, Scheuer PJ (1998) Palau'amine and its congeners: a family of bioactive bisguanidines from the marine sponge Stylotella aurantium. J Org Chem 63:3281–3286

    Article  CAS  Google Scholar 

  • Levin DA, York BM (1978) The toxicity of plant alkaloids: an ecographic perspective. Biochem Syst Ecol 6:61–76

    CAS  Google Scholar 

  • Lubchenco J, Gaines SD (1981) A unified approach to marine plant-herbivore interactions. I. populations and communities. Annu Rev Ecol Syst 12:405–437

    Google Scholar 

  • Margalef R (1985) Key environments: Western Mediterranean. Pergamon, Oxford

    Google Scholar 

  • Martin TE (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecol Monogr 65:101–127

    Google Scholar 

  • McCaffrey EJ, Endean R (1985) Antimicrobial activity of tropical and subtropical sponges. Mar Biol 89:1–8

    Google Scholar 

  • McClintock JB (1987) Investigation of the relationships between invertebrate predation and biochemical composition, energy content, spicule armament, and toxicity of benthic sponges at McMurdo Sound, Antarctica. Mar Biol 94:479–487

    CAS  Google Scholar 

  • McClintock JB, Baker BJ (2001) Marine Chemical Ecology. CRC, Boca Raton, Fla

  • Meekan MG, Choat JH (1997) Latitudinal variation in abundance of herbivorous fishes: a comparison of temperate and tropical reefs. Mar Biol 128:373–383

    Article  Google Scholar 

  • Menge BA, Lubchenco J (1981) Community organization in temperate and tropical rocky intertidal habitats: prey refuges in relation to consumer pressure gradients. Ecol Monogr 51:429–450

    Google Scholar 

  • Meyer KD, Paul VJ (1992) Intraplant variation in secondary metabolite concentration in three species of Caulerpa (Chlorophyta: Caulerpales) and its effects on herbivorous fishes. Mar Ecol Prog Ser 82:249–257

    CAS  Google Scholar 

  • Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75

    Article  Google Scholar 

  • Paine RT (1994) Marine rocky shores and community ecology: an experimentalist's perspective. Ecology Institute, Oldendorf/Luhe, Germany

    Google Scholar 

  • Palmer AR (1978) Fish predation and the evolution of gastropod shell sculpture: experimental and geographic evidence. Evolution 33:697–713

    Google Scholar 

  • Paul VJ (1992) Ecological roles of marine natural products. Comstock, Ithaca, N.Y.

  • Paulay G (1997) Diversity and distribution of reef organisms. In: Birkeland C (ed) Life and death of coral reefs. Chapman and Hall, New York, pp 298–353

  • 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

    CAS  Google Scholar 

  • Pennings SC, Paul VJ (1992) Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia. Ecology 73:1606–1619

    Google Scholar 

  • Pennings SC, Pablo SR, Paul VJ, Duffy JE (1994) Effects of sponge secondary metabolites in different diets on feeding by three groups of consumers. J Exp Mar Biol Ecol 180:137–149

    Google Scholar 

  • Pennings SC, Siska EL, Bertness MD (2001) Latitudinal differences in plant palatability in Atlantic coast salt marshes. Ecology 82:1344–1359

    Google Scholar 

  • Pianka ER (1966) Latitudinal gradients in species diversity: a review of concepts. Am Nat 100:33–46

    Article  Google Scholar 

  • Porter JW, Targett NM (1988) Allelochemical interactions between sponges and corals. Biol Bull 175:230–239

    Google Scholar 

  • Potvin C, Roff DA (1993) Distribution-free and robust statistical methods: viable alternatives to parametric statistics. Ecology 74:1617–1628

    Google Scholar 

  • Pulitzer-Finàli G (1983) A collection of Mediterranean Demospongiae (Porifera) with, in appendix, a list from the Mediterranean Sea. Ann Mus Civ Hist Nat Genova 84:445–621

    Google Scholar 

  • Randall JE, Hartman WD (1968) Sponge feeding fishes of the West-Indies. Mar Biol 1:216–225

    Google Scholar 

  • Rhoades DF (1983) Herbivore population dynamics and plant chemistry. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic, New York, pp 155–220

  • Rousi M, Tahvanainen J, Uotila I (1991) Mechanism of resistance to hare browsing in winter-dormant silver birch (Betula pendula). Am Nat 137:64–82

    Article  Google Scholar 

  • Rueda A, Zubia E, Ortega MJ, Carballo JL, Salvá J (1997) New cytotoxic metabolites from the sponge Cacospongia scalaris. J Org Chem 62:1481–1485

    Article  CAS  Google Scholar 

  • Sammarco PW, Carletton JH, Risk MJ (1986) Effects of grazing and damselfish territoriality on bioerosion of dead corals: direct effects. J Exp Mar Biol Ecol 98:1–19

    Google Scholar 

  • Sara M, Vacelet J (1973) Écologie des Démosponges. In: Grasse PP (ed) Traité de zoologie (anatomie, systematique, biologie). Masson, Paris, pp 462–576

  • Schmitt TM, Hay ME, Lindquist N (1995) Constraints on chemically mediated coevolution: multiple functions of seaweed secondary metabolites. Ecology 6:107–123

    Google Scholar 

  • Schupp PJ, Paul VJ (1994) Calcification and secondary metabolites in tropical seaweeds: variable effects on herbivorous fishes. Ecology 75:1172–1185

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. State University of New York at Stony Brook, New York, N.Y.

    Google Scholar 

  • Steinberg PD (1989) Biogeographic variation in brown algal polyphenolics and other secondary metabolites: comparison between temperate Australasia and North America. Oecologia 78:374–383

    Google Scholar 

  • Steinberg PD, Paul VJ (1990) Fish feeding and chemical defenses of tropical brown algae in Western Australia. Mar Ecol Prog Ser 58:253–259

    Google Scholar 

  • Steinberg PD, van Altena IA (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222

    Google Scholar 

  • Steinberg PD, Edyvane K, de Nys R, Birdsey D, van Altena IA (1991) Lack of avoidance of phenolic-rich algae by tropical herbivorous fishes. Mar Biol 68:299–319

    Google Scholar 

  • Targett NM, Arnold TM (1998) Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34:195–205

    CAS  Google Scholar 

  • Targett NM, Coen LD, Boettcher AA, Tanner CE (1992) Biogeographic comparisons of marine algal polyphenolics: evidence against a latitudinal trend. Oecologia 89:464–470

    Google Scholar 

  • Thacker RW, Becerro MA, Lumbang WA, Paul VJ (1998) Allelopathic interactions between sponges on a tropical reef. Ecology 79:1740–1750

    Google Scholar 

  • Uriz MJ, Martin D, Turon X, Ballesteros E, Hughes R, Acebal C (1991) An approach to the ecological significance of chemically mediated bioactivity in Mediterranean benthic communities. Mar Ecol Prog Ser 113:287–297

    Google Scholar 

  • Uriz MJ, Martin D, Rosell D (1992a) Relationship of biological and taxonomic characteristics to chemically mediated bioactivity in Mediterranean littoral sponges. Mar Biol 113:287–297

    Google Scholar 

  • Uriz MJ, Rosell D, Martin D (1992b) The sponge population of the Cabrera Archipelago (Balearic Islands): characteristics, distribution, and abundance of the most representative species. Mar Ecol PSZNI 13:101–117

    Google Scholar 

  • Uriz MJ, Turon X, Galera J, Tur JM (1996) New light on the cell location of avarol within the sponge Dysidea avara (Dendroceratida). Cell Tissue Res 285:519–527

    Article  Google Scholar 

  • Vacelet J (1979) La place des spongiaires dans les systems trophiques marins. Coll Int CNRS 291:259–270

    Google Scholar 

  • Van Alstyne KL, Paul VJ (1990) The biogeography of polyphenolic compounds in marine macroalgae: temperate brown algal defenses deter feeding by tropical herbivorous fishes. Oecologia 84:158–163

    Google Scholar 

  • Van Alstyne KL, McCarthy JJ III, Hustead CL, Duggins DO (1999) Geographic variation in polyphenolic levels of Northeastern Pacific kelps and rockweeds. Mar Biol 133:371–379

    Article  Google Scholar 

  • Van der Vyver G, Huysecom J, Braekman JC, Daloze D (1990) Screening and bioassays for toxic substances in sponges from western Mediterranean Sea and North Brittany. Vie Milieu 40:285–292

    Google Scholar 

  • Vermeij GJ (1978) Biogeography and adaptation: patterns of marine life. Harvard University Press, Cambridge, Mass.

    Google Scholar 

  • Warren PH, Gaston KJ (1992) Predator-prey ratios: a special case of a general pattern? Philos Trans R Soc B 338:113–130

    Google Scholar 

  • Williams CB (1964) Patterns in the balance of nature. Academic Press, New York

Download references

Acknowledgements

We sincerely thank Maria Garcia and Ramon Alos not only for providing the schooner Rael but also for making us feel at home aboard. Gemma Agell, Dave Ginsburg, and Ruth Marti helped with sampling and extraction procedures. Many other people from the UOGML and the CEAB provided assistance in the field and in the laboratory. Comments from two anonymous reviewers improved the manuscript. The U.S.-Spain Joint Commission on Scientific and Technological Cooperation funded this collaborative project between the UOGML and the CEAB. This is contribution number 528 of the University of Guam Marine Laboratory.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mikel A. Becerro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Becerro, M.A., Thacker, R.W., Turon, X. et al. Biogeography of sponge chemical ecology: comparisons of tropical and temperate defenses. Oecologia 135, 91–101 (2003). https://doi.org/10.1007/s00442-002-1138-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-002-1138-7

Keywords

Navigation