Skip to main content
Log in

Spatial Variability in Secondary Metabolites of the Indo-Pacific Sponge Stylissa massa

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Chemical diversity represents a measure of selective pressures acting on genotypic variability. In order to understand patterns of chemical ecology and biodiversity in the environment, it is necessary to enhance our knowledge of chemical diversity within and among species. Many sponges produce variable levels of secondary metabolites in response to diverse biotic and abiotic environmental factors. This study evaluated intra-specific variability in secondary metabolites in the common Indo-Pacific sponge Stylissa massa over various geographic scales, from local to ocean basin. Several major metabolites were quantified in extracts from sponges collected in American Samoa, Pohnpei, Saipan, and at several sites and depths in Guam. Concentrations of several of these metabolites varied geographically across the Pacific basin, with American Samoa and Pohnpei exhibiting the greatest differences, and Guam and Saipan more similar to each other. There were also significant differences in concentrations among different sites and depths within Guam. The crude extract of S. massa exhibited feeding deterrence against the omnivorous pufferfish Canthigaster solandri at natural concentrations, however, none of the isolated compounds was deterrent at the maximum natural concentrations observed, nor were mixtures of these compounds, thus emphasizing the need for bioassay-guided isolation to characterize specific chemical defenses. Antibacterial activity against a panel of ecologically relevant pathogens was minimal. Depth transplants, predator exclusion, and UV protection experiments were performed, but although temporal variability in compound concentrations was observed, there was no evidence that secondary metabolite concentration in S. massa was induced by any of these factors. Although the reasons behind the variability observed in the chemical constituents of S. massa are still in question, all sponges are not created equal from a chemical standpoint, and these studies provide further insights into patterns of chemical diversity within S. massa.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abdo, D. A., Motti, C. A., Battershill, C. N., and Harvey, E. S. 2007. Temperature and spatiotemporal variability of salicylihalamide A in the sponge Haliclona sp. J. Chem. Ecol. 33:1635–1645.

    Article  PubMed  CAS  Google Scholar 

  • Amesbury, S. S. and Myers, R. F. 1982. pp. 1–141, Guide to the Coastal Resources of Guam Vol. 1. University of Guam Marine Lab Contribution No. 173, Mangilao.

    Google Scholar 

  • Assmann, M., Lichte, E., Pawlik, J. R., and Köck, M. 2000. Chemical defenses of the Caribbean sponges Agelas wiedenmayeri and Agelas conifera. Mar. Ecol. Prog. Ser. 207:255–262.

    Article  CAS  Google Scholar 

  • Bandaranayake, W. M., Bemis, J. E., and Bourne, D. J. 1996. Ultraviolet absorbing pigments from the marine sponge Dysidea herbacea: Isolation and structure of a new mycosporine. Comp. Biochem. Physiol., C: Toxicol. Pharmacol. 115:281–286.

    Google Scholar 

  • Bandaranayake, W. M., Bourne, D. J., and Sim, R. G. 1997. Chemical composition during maturing and spawning of the sponge Dysidea herbacea (Porifera: Demospongiae). Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 118:851–859.

    Article  Google Scholar 

  • Becerro, M. A. and Paul, V. J. 2004. Effects of depth and light on secondary metabolites and cyanobacterial symbionts of the sponge Dysidea granulosa. Mar. Ecol. Prog. Ser. 280:115–128.

    Article  CAS  Google Scholar 

  • Becerro, M. A., Thacker, R. W., Turon, X., Uriz, M. J., and Paul, V. J. 2003. Biogeography of sponge chemical ecology: Comparisons of tropical and temperate defenses. Oecologia 135:91–101.

    PubMed  Google Scholar 

  • Betancourt-Lozano, M., Gonzalez-Farias, F., Gonzalez-Acosta, B., Garcia-Gasca, A., and Bastida-Zavala, J. R. 1998. Variation of antimicrobial activity of the sponge Aplysina fistularis (Pallas, 1766) and its relation to associated fauna. J. Exp. Mar. Biol. Ecol. 223:1–18.

    Article  Google Scholar 

  • Blunt, J. W. and Munro, M. H. G. 2009. MarinLit. Marine Chemistry Group, Christchurch.

    Google Scholar 

  • Chanas, B., Pawlik, J. R., Lindel, T., and Fenical, W. 1996. Chemical defense of the Caribbean sponge Agelas clathrodes (Schmidt). J. Exp. Mar. Biol. Ecol. 208:185–196.

    Article  Google Scholar 

  • Connolly, S. R. and Roughgarden, J. 1999. Theory of marine communities: Competition, predation, and recruitment-dependent interaction strength. Ecol. Monogr. 69:277–296.

    Article  Google Scholar 

  • Cronin, G. and Hay, M. E. 1996a. Induction of seaweed chemical defenses by amphipod grazing. Ecology 77:2287–2301.

    Article  Google Scholar 

  • Cronin, G. and Hay, M. E. 1996b. Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology 77:1531–1543.

    Article  Google Scholar 

  • Dunlap, W. C. and Shick, J. M. 1998. Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: A biochemical and environmental perspective. J. Phycol. 34:418–430.

    Article  Google Scholar 

  • Ebel, R., Brenzinger, M., Kinze, A., Gross, H. J., and Proksch, P. 1997. Wound activation of protoxins in marine sponge Aplysina aerophoba. J. Chem. Ecol. 23:1451–1462.

    Article  CAS  Google Scholar 

  • Fahey, S. J. and Garson, M. J. 2002. Geographic variation of natural products of tropical nudibranch Asteronotus cespitosus. J. Chem. Ecol. 28:1773–1785.

    Article  PubMed  CAS  Google Scholar 

  • Fielman, K. T. and Targett, N. M. 1995. Variation of 2,3,4-tribromopyrrole and its sodium sulfamate salt in the hemichordate Saccoglossus kowalevskii. Mar. Ecol. Prog. Ser. 116:125–136.

    Article  CAS  Google Scholar 

  • Gochfeld, D. J. and Aeby, G. S. 2008. Antibacterial chemical defenses in Hawaiian corals provide possible protection from disease. Mar. Ecol. Prog. Ser. 362:119–128.

    Article  Google Scholar 

  • Gochfeld, D. J., Olson, J. B., and Slattery, M. 2006. Colony versus population variation in susceptibility and resistance to dark spot syndrome in the Caribbean coral Siderastrea siderea. Dis. Aquat. Org. 69:53–65.

    Article  PubMed  Google Scholar 

  • Gochfeld D., Kamel H., Olson J., and Thacker R. 2012, this issue. Trade-offs in defensive metabolite production but not ecological function in healthy and diseased sponges. J. Chem. Ecol. doi:10.1007/s10886-012-0099-5

  • Gröniger, A., Sinha, R. P., Klisch, M., and Hader, D. P. 2000. Photoprotective compounds in cyanobacteria, phytoplankton and macroalgae—a database. J. Photochem. Photobiol. B: Biol. 58:115–122.

    Article  Google Scholar 

  • Haber, M., Carbone, M., Mollo, E., Gavagnin, M., and Ilan, M. 2011. Chemical defense against predators and bacterial fouling in the Mediterranean sponges Axinella polypoides and A. verrucosa. Mar. Ecol. Prog. Ser. 422:113–122.

    Article  CAS  Google Scholar 

  • Harvell, C. and Tollrian, R. 1999. Why inducible defenses? pp. 3–9, in R. Tollrian and C. Harvell (eds.), The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton.

    Google Scholar 

  • Hay, M. E. 1996. Marine chemical ecology: What’s known and what’s next? J. Exp. Mar. Biol. Ecol. 200(1–2):103–134.

    Article  CAS  Google Scholar 

  • Ianora, A., Boersma, M., Casotti, R., Fontana, A., Harder, J., Hoffmann, F., Pavia, H., Potin, P., Poulet, S. A., and Toth, G. 2006. New trends in marine chemical ecology. Estuar. Coasts 29:531–551.

    CAS  Google Scholar 

  • Jumaryatno, P., Stapleton, B. L., Hooper, J. N. A., Brecknell, D. J., Blanchfield, J. T., and Garson, M. J. 2007. A comparison of sesquiterpene scaffolds across different populations of the tropical marine sponge Acanthella cavernosa. J. Nat. Prod. 70:1725–1730.

    Article  PubMed  CAS  Google Scholar 

  • Karban, R. and Baldwin, I. T. 1997. Induced Response to Herbivory. University of Chicago Press, Chicago.

    Google Scholar 

  • Kelly, S. R., Jensen, P. R., Henkel, T. P., Fenical, W., and Pawlik, J. R. 2003. Effects of Caribbean sponge extracts on bacterial attachment. Aquat. Microb. Ecol. 31:175–182.

    Article  Google Scholar 

  • Kinnel, R. B., Gehrken, H. P., and Scheuer, P. J. 1993. Palauamine—a cytotoxic and immunosuppresive hexacyclic bisuguanidine antibiotic from the sponge Stylotella agminata. J. Am. Chem. Soc. 115:3376–3377.

    Article  CAS  Google Scholar 

  • Kobayashi, J., Ohizumi, Y., Nakamura, H., and Hirata, Y. 1986. A novel anatagonist of serotonergic receptors, hymenidin, isolated from the okinawan marine sponge Hymeniacidon sp. Experientia 42:1176–1177.

    Article  PubMed  CAS  Google Scholar 

  • Lindel, T., Hoffmann, H., Hochgurtel, M., and Pawlik, J. R. 2000. Structure-activity relationship of inhibition of fish feeding by sponge-derived and synthetic pyrrole-imidazole alkaloids. J. Chem. Ecol. 26:1477–1496.

    Article  CAS  Google Scholar 

  • Lotze, H. K., Worm, B., Molis, M., and Wahl, M. 2002. Effects of UV radiation and consumers on recruitment and succession of a marine macrobenthic community. Mar. Ecol. Prog. Ser. 243:57–66.

    Article  Google Scholar 

  • Martí, R., Uriz, M. J., and Turon, X. 2004. Seasonal and spatial variation of species toxicity in Mediterranean seaweed communities: Correlation to biotic and abiotic factors. Mar. Ecol. Prog. Ser. 282:73–85.

    Article  Google Scholar 

  • Martí, R., Uriz, M. J., and Turon, X. 2005. Spatial and temporal variation of natural toxicity in cnidarians, bryozoans and tunicates in Mediterranean caves. Sci. Mar. 69:485–492.

    Google Scholar 

  • McClintock, J. B. and Karentz, D. 1997. Mycosporine-like amino acids in 38 species of subtidal marine organisms from McMurdo Sound, Antarctica. Antarct. Sci. 9:392–398.

    Article  Google Scholar 

  • Miner, B. G., Sultan, S. E., Morgan, S. G., Padilla, D. K., and Relyea, R. A. 2005. Ecological consequences of phenotypic plasticity. Trends Ecol. Evol. 20:685–692.

    Article  PubMed  Google Scholar 

  • Mohammed, R., Peng, J. N., Kelly, M., and Hamann, M. T. 2006. Cyclic heptapeptides from the Jamaican sponge Stylissa caribica. J. Nat. Prod. 69:1739–1744.

    Article  PubMed  CAS  Google Scholar 

  • Nunez, C. V., de Almelda, E. V. R., Granato, A. C., Marques, S. O., Santos, K. O., Pereira, F. R., Macedo, M. L., Ferreira, A. G., Hajdu, E., Pinheiro, U. S., et al. 2008. Chemical variability within the marine sponge Aplysina fulva. Biochem. Syst. Ecol. 36:283–296.

    Article  CAS  Google Scholar 

  • Page, M., West, L., Northcote, P., Battershill, C., and Kelly, M. 2005. Spatial and temporal variability of cytotoxic metabolites in populations of the New Zealand sponge Mycale hentscheli. J. Chem. Ecol. 31:1161–1174.

    Article  PubMed  CAS  Google Scholar 

  • Paul, V. J. 1992. pp. 245, Ecological Roles of Marine Natural Products. Comstock Press, Ithaca.

    Google Scholar 

  • Paul, V. J., Puglisi, M. P., and Ritson-Williams, R. 2006. Marine chemical ecology. Nat. Prod. Rep. 23:153–180.

    Article  PubMed  CAS  Google Scholar 

  • Pavia, H., Cervin, G., Lindgren, A., and Aberg, P. 1997. Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar. Ecol. Prog. Ser. 157:139–146.

    Article  CAS  Google Scholar 

  • Pawlik, J. R., Chanas, B., Toonen, R. J., and Fenical, W. 1995. Defenses of Caribbean sponges against predatory reef fish.1. Chemical deterrency. Mar. Ecol. Prog. Ser. 127:183–194.

    Article  CAS  Google Scholar 

  • Pennings, S. C., Pablo, S. R., Paul, V. J., and Duffy, J. E. 1994. Effects of sponge secondary metabolites in different diets on feeding by 3 groups of consumers. J. Exp. Mar. Biol. Ecol. 180:137–149.

    Article  Google Scholar 

  • Pigliucci, M. 2005. Evolution of phenotypic plasticity: Where are we going now? Trends Ecol. Evol. 20(9):481–486.

    Article  PubMed  Google Scholar 

  • Puglisi, M. P., Paul, V. J., and Slattery, M. 2000. Biogeographic comparisons of chemical and structural defenses of the Pacific gorgonians Annella mollis and A. reticulata. Mar. Ecol. Prog. Ser. 207:263–272.

    Article  Google Scholar 

  • Putz, A., Kloeppel, A., Pfannkuchen, M., Brummer, F., and Proksch, P. 2009. Depth-related alkaloid variation in mediterranean aplysina sponges. Z. Naturforsch. Sect. C 64:279–287.

    CAS  Google Scholar 

  • Richelle-Maurer, E., De Klujiver, M. J., Feio, S., Gaudencio, S., Gaspar, H., Gomez, R., Tavares, R., Van De Vyver, G., and Van Soest, R. W. M. 2003. Localization and ecological significance of oroidin and sceptrin in the Caribbean sponge Agelas conifera. Biochem. Syst. Ecol. 31:1073–1091.

    Article  CAS  Google Scholar 

  • Rohde, S. and Schupp, P. J. 2011. Allocation of chemical and structural defenses in the sponge Melophlus sarasinorum. J. Exp. Mar. Biol. Ecol. 399:76–83.

    Article  PubMed  CAS  Google Scholar 

  • Rohde, S., Molis, M., and Wahl, M. 2004. Regulation of anti-herbivore defence by Fucus vesiculosus in response to various cues. J. Ecol. 92:1011–1018.

    Article  Google Scholar 

  • Sacristan-Soriano, O., Banaigs, B., and Becerro, M. A. 2011. Relevant spatial scales of chemical variation in Aplysina aerophoba. Mar. Drugs 9:2499–2513.

    Article  PubMed  CAS  Google Scholar 

  • Shick, J. M., Romaine-Lioud, S., Ferrier-Pages, C., and Gattuso, J. P. 1999. Ultraviolet-B radiation stimulates shikimate pathway-dependent accumulation of mycosporine-like amino acids in the coral Stylophora pistillata despite decreases in its population of symbiotic dinoflagellates. Limnol. Oceanogr. 44:1667–1682.

    Article  CAS  Google Scholar 

  • Slattery M. and Gochfeld D. J. 2012. Chemical interactions among marine competitors, and host-pathogens, in: E. Fattorusso, W. H. Gerwick, O. Taglialatela-Scafati (eds.), Handbook of Marine Natural Products: Springer.

  • Slattery, M. and Paul, V. J. 2008. Indirect effects of bleaching on predator deterrence in the tropical Pacific soft coral Sinularia maxima. Mar. Ecol. Prog. Ser. 354:169–179.

    Article  Google Scholar 

  • Slattery, M., Avila, C., Starmer, J., and Paul, V. J. 1998. A sequestered soft coral diterpene in the aeolid nudibranch Phyllodesmium guamensis. J. Exp. Mar. Biol. Ecol. 226:33–49.

    Article  CAS  Google Scholar 

  • Slattery, M., Starmer, J., and Paul, V. J. 2001. Temporal and spatial variation in defensive metabolites of the tropical Pacific soft corals Sinularia maxima and S. polydactyla. Mar. Biol. 138:1183–1193.

    Article  CAS  Google Scholar 

  • Slattery, M., Kamel, H. N., Ankisetty, S., Gochfeld, D. J., Hoover, C. A., and Thacker, R. W. 2008. Hybrid vigor in a tropical Pacific soft-coral community. Ecol. Monogr. 78:423–443.

    Article  Google Scholar 

  • Stachowicz, J. J. and Lindquist, N. 1997. Chemical defense among hydroids on pelagic Sargassum: Predator deterrence and absorption of solar UV radiation by secondary metabolites. Mar. Ecol. Prog. Ser. 155:115–126.

    Article  CAS  Google Scholar 

  • Steindler, L., Beer, S., and Ilan, M. 2002. Photosymbiosis in intertidal and subtidal tropical sponges. Symbiosis 33:263–273.

    Google Scholar 

  • Supriyono, A., Schwarz, B., Wray, V., Witte, L., Muller, W. E. G., Vansoest, R., Sumaryono, W., and Proksch, P. 1995. Bioactive alkaloids from the tropical marine sponge Axinella carteri. Z. Naturforsch. Sect. C 50:669–674.

    CAS  Google Scholar 

  • Targett, N. M., Coen, L. D., Boettcher, A. A., and Tanner, C. E. 1992. Biogeographic comparisons of marine algal polyphenolics—evidence against a latitudinal trend. Oecologia 89:464–470.

    Google Scholar 

  • Tasdemir, D., Mallon, R., Greenstein, M., Feldberg, L. R., Kim, S. C., Collins, K., Wojciechowicz, D., Mangalindan, G. C., Concepcion, G. P., Harper, M. K., et al. 2002. Aldisine alkaloids from the Philippine sponge Stylissa massa are potent inhibitors of mitogen-activated protein kinase kinase-1 (MEK-1). J. Med. Chem. 45:529–532.

    Article  PubMed  CAS  Google Scholar 

  • Teeyapant, R. and Proksch, P. 1993. Biotransformation of brominated compounds in the marine sponge Verongia aerophoba—Evidence for an induced chemical defense. Naturwissenschaften 80:369–370.

    Article  CAS  Google Scholar 

  • Thompson, J. E., Murphy, P. T., Bergquist, P. R., and Evans, E. A. 1987. Environmentally induced variation in diterpene composition of the marine sponge Rhopaleides odorabile. Biochem. Syst. Ecol. 15:595–606.

    Article  CAS  Google Scholar 

  • Thoms, C., Horn, M., Wagner, M., Hentschel, U., and Proksch, P. 2003. Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Mar. Biol. 142:685–692.

    CAS  Google Scholar 

  • Turon, X., Becerro, M. A., and Uriz, M. J. 1996. Seasonal patterns of toxicity in benthic invertebrates: The encrusting sponge Crambe crambe (Poecilosclerida). Oikos 75:33–40.

    Article  Google Scholar 

  • Turon, X., Marti, R., and Uriz, M. J. 2009. Chemical bioactivity of sponges along an environmental gradient in a Mediterranean cave. Sci. Mar. 73:387–397.

    Article  CAS  Google Scholar 

  • Uriz, M. J., Turon, X., Becerro, M. A., Galera, J., and Lozano, J. 1995. Patterns of resource allocation to somatic, defensive and reproductive functions in the mediterranean encrusting sponge Crambe crambe (Demospongiae, Poecilosclerida). Mar. Ecol. Prog. Ser. 124:159–170.

    Article  Google Scholar 

  • Van Soest R. W. M., Boury-Esnault N., Hooper J. N. A., Rützler K., De Voogd N. J., Alvarez De Glasby B., Hajdu E., Pisera A. B., Manconi R., Schoenberg C., et al. 2010. World Porifera database. http://www.marinespecies.org/porifera.

  • Verschoor, A. M., Vos, M., and van der Stap, I. 2004. Inducible defences prevent strong population fluctuations in bi- and tritrophic food chains. Ecol. Lett. 7:1143–1148.

    Article  Google Scholar 

  • Wahl, M. 1989. Marine epibiosis.1. Fouling and antifouling—some basic aspects. Mar. Ecol. Prog. Ser. 58:175–189.

    Article  Google Scholar 

  • Wright, J. T., de Nys, R., and Steinberg, P. D. 2000. Geographic variation in halogenated furanones from the red alga Delisea pulchra and associated herbivores and epiphytes. Mar. Ecol. Prog. Ser. 207:227–241.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Katerina Pappas, Mallory de Johnson, Sylvester Lee, and Dr. Haidy Kamel for their help in the laboratory. Funding was provided by a NOAA/NIUST grant #NA16RU1496 to MS and by NIH MBRS SCORE grant S06-GM-44796 to PJS. SR was supported by a fellowship within the Postdoc-Program of the German Academic Exchange Service (DAAD). Field support was provided by the University of Guam Marine Laboratory, American Samoa Department of Marine and Wildlife Resources, Saipan Division of Coastal Resources Management, and Pohnpei Department of Marine Development. Samples were collected under permits from the Guam Department of Agriculture, American Samoa Department of Marine and Wildlife Resources, Commonwealth of the Northern Mariana Islands Division of Fish and Wildlife, and Pohnpei Department of Marine Development.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sven Rohde.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rohde, S., Gochfeld, D.J., Ankisetty, S. et al. Spatial Variability in Secondary Metabolites of the Indo-Pacific Sponge Stylissa massa . J Chem Ecol 38, 463–475 (2012). https://doi.org/10.1007/s10886-012-0124-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0124-8

Keywords

Navigation