Journal of Chemical Ecology

, Volume 19, Issue 3, pp 517–530 | Cite as

Allelochemical inhibition of recruitment in a sedimentary assemblage

  • Sarah A. Woodin
  • Roberta L. Marinelli
  • David E. Lincoln
Article

Abstract

Chemical signals affect recruitment of organisms in many habitats. Most of the described biogenic chemical moieties in marine environments elicit specific positive responses, for example, of predators to prey or of conspecific larvae to suitable habitats. However, organisms also release noxious chemicals that may elicit negative responses from neighboring members of the assemblage. Herein we measured the effect on recruitment of the release of such compounds (halogenated aromatics) into sediments. The common, sediment-dwelling, terebellid polychaeteThelepus crispus contains brominated aromatic metabolites and contaminates the sediments surrounding its tube with these compounds. Sediments so contaminated are actively rejected by recruitingNereis vexillosa (Nereidae: Polychaeta). Interestingly, many of these noxious biogenic compounds have low solubility in water and, therefore, potentially long residence times in sedimentary environments. The negative response of larvae to sediment contaminated with them is a novel, potentially common, and very important mechanism in which sediment-dwelling organisms release haloaromatic compounds and thus impose a recruitment filter on their community.

Key Words

Infauna polychaete halogenated aromatic recruitment allelochemical negative cue sediments Thelepus Nereis allelopathy 

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References

  1. Aller, R.C., 1982. The effects of macrobenthos on chemical properties of marine sediment and overlying water, pp. 53–102,in P.L. McCall and M.J.S. Tevesz (eds.). Animal-Sediment Relations. Plenum Press, New York.Google Scholar
  2. Aller, R.C., andYingst, J.Y. 1985. Effects of the marine deposit-feedersHeteromastus filiformis (Polychaeta),Macoma balthica (Bivalvia) andTellina texana (Bivalvia) on averaged sedimentary solute transport, reaction rates and microbial distributions.J. Mar. Res. 43:615–645.Google Scholar
  3. Ashworth, R.B., andCormier, M.J. 1967. Isolation of 2,6-dibromophenol from the marine hemichordateBalanoglossus biminiensis.Science 155:1558–1559.Google Scholar
  4. Braekman, J.C., andDaloze, D. 1986. Chemical defence in sponges.Pure Appl. Chem. 58:357–364.Google Scholar
  5. Buhr, K.-J. 1976. Suspension-feeding and assimilation efficiency inLanice conchilega (Polychaeta).Mar. Biol. 38:373–383.Google Scholar
  6. Butman, C.A. 1987. Larval settlement of soft-sediment invertebrates: The spatial scales of pattern explained by active habitat selection and the emerging role of hydrodynamical processes.Oceanogr. Mar. Biol Annu. Rev. 24:113–165.Google Scholar
  7. Chen, Y.P., Lincoln, D.E., Woodin, S.A., andLovell, C.R. 1991. Purification and properties of a unique flavin-containing chloroperoxidase from the capitellid polychaeteNotomastus lobatus.J. Biol. Chem. 266:23909–23915.Google Scholar
  8. Davis, A.R., Targett, N.M., McConnel, O.G., andYoung, C.M. 1989. Epibiosis of marine algae and benthic invertebrates: Natural products chemistry and other mechanisms inhibiting settlement and overgrowth, pp. 85–114,in P.J. Scheuer (ed.). Bioorganic Marine Chemistry, Vol. 3. Springer-Verlag, Berlin.Google Scholar
  9. Dawidowicz, P., Pijanowska, J., andCiechomski, K. 1990. Vertical migration ofChaoborus larvae is induced by the presence of fish.Limnol. Oceanogr. 35:1631–1636.Google Scholar
  10. Emerson, S., Jahnke, R., andHeggie, D. 1984. Sediment-water exchange in shallow water estuarine sediments.J. Mar. Res. 42:709–730.Google Scholar
  11. Emrich, R., Weyland, H., andWeber, K. 1990. 2,3,4-Tribromopyrrole from the marine polychaetePolyphysia crass.J. Nat. Prod. 53:703–705.Google Scholar
  12. Faulker, D.J. 1984. Marine natural products: metabolites of marine algae and herbivorous molluscs.Nat. Prod. Rep. 1:251–280.Google Scholar
  13. Feeny, P. 1976. Plant apparency and chemical defense.Recent Adv. Phytochem. 10:1–40.Google Scholar
  14. Goerke, H., andWeber, K. 1991. Bromophenols inLanice conchilega (Polychaeta, Terebellidae): The influence of sex, weight and season.Bull. Mar. Sci. 48:517–523.Google Scholar
  15. Goerke, H., Emrich, R., Weber, K., andDuchene, J.-C. 1991. Concentrations and localization of brominated metabolites in the genusThelepus (Polychaeta: Terrebellidae).Comp. Biochem. Physiol. 99B:302–206.Google Scholar
  16. Grosberg, R.K. 1981. Competitive ability influences habitat choice in marine invertebrates.Nature 290:700–702.Google Scholar
  17. Gust, G., andHarrison, J.T. 1981. Biological pumps at the sediment-water interface: mechanistic evaluation of the Alpheid shrimpAlpheus mackayi and its irrigation pattern.Mar. Biol. 64:71–78.Google Scholar
  18. Hadfield, M.G. 1984. Settlement requirements of molluscan larvae: New data on chemical and genetic roles.Aquaculture 39:283–298.Google Scholar
  19. Hanazato, T. 1991. Effects of aChaoborus-released chemical onDaphnia ambigua: Reduction in the tolerance of theDaphnia to summer water temperature.Limnol. Oceanogr. 36:165–171.Google Scholar
  20. Hay, M.E., andFenical, W. 1988. Marine plant-herbivore interactions: The ecology of chemical defense.Annu. Rev. Ecol. Syst. 19:111–145.Google Scholar
  21. Higa, T., andScheuer, P.J. 1975. Constituents of the marine annelidThelepus setosus.Tetrahedron 31:2379–2381.Google Scholar
  22. Higa, T., andScheuer, P.J. 1977. Constituents of the hemichordatePtychodera flava laysanica, pp. 35–43,in D.J. Faulkner and W.H. Fenical (eds.). Marine Natural Products Chemistry. Plenum Press, New York.Google Scholar
  23. Higa, T., Fujiyama, T., andScheuer, P.J. 1980. Halogenated phenol and indole constituents of acorn worms.Comp. Biochem. Physiol. 65B:525–530.Google Scholar
  24. Higa, T., Okuda, R.K., Severns, R.M., Scheuer, P.J., He, C.-H., Changfu, X., andClardy, J. 1987. Unprecedented constituents of a new species of acorn worm.Tetrahedron 43:1063–1070.Google Scholar
  25. Highsmith, R.C. 1982. Induced settlement and metamorphosis of sand dollar (Dendraster excentricus) larvae in predator-free sites: Adult sand dollar beds.Ecology 63:329–337.Google Scholar
  26. Johnson, L.E., andStrathmann, R.R. 1989. Settling barnacle larvae avoid substrata previously occupied by a mobile predator.J. Exp. Mar. Biol. Ecol. 128:87–103.Google Scholar
  27. Johnson, M.W. 1943. Studies on the life history of the marine annelidNereis vexillosa.Biol. Bull. 84:106–114.Google Scholar
  28. King, G.M. 1986. Inhibition of microbial activity in marine sediments by a bromophenol from a hemichordate.Nature 323:257–259.Google Scholar
  29. Knox, G.A. 1977. The role of polychaetes in benthic soft-bottom communities, pp. 547–604,in D.J. Reish and K. Fauchald (eds.). Essays on Polychaetous Annelids. Allan Hancock Foundation, University of Southern California, Los Angeles.Google Scholar
  30. Meyers, M.B., Fossing, H., andPowell, E.N. 1987. Microdistribution of interstitial meiofauna, oxygen and suicide gradients, and the tubes of macro-infauna.Mar. Ecol. Prog. Ser. 35:223–241.Google Scholar
  31. Morse, A.N.C., andMorse, D. 1984. Recruitment and metamorphosis ofHaliotis larvae induced by molecules uniquely available at the surfaces of crustose red alga.J. Exp. Mar. Biol. Ecol. 65:191–215.Google Scholar
  32. Paul, V.J. 1987. Feeding deterrent effects of algal natural products.Bull. Mar. Sci. 41:514–522.Google Scholar
  33. Pawlik, J.R., Butman, C.A., andStarczak, V.R. 1990. Hydrodynamic facilitation of gregarious settlement of a reef-building tube worm.Science 251:421–424.Google Scholar
  34. Peterson, C.H., andPeterson, N.M. 1979. The Ecology of Intertidal Flats of North Carolina: A Community Profile. Fish and Wildlife Service, Office of Biological Services. FWS/OBS-79/ 39, 73 pp.Google Scholar
  35. Rhoads, D.C., andBoyer, L.F. 1982. The effects of marine benthos on physical -properties of sediments: a successful perspective, pp. 3–52,in P.L. McCall and M.J.S. Tevesz (eds.). Animal-Sediment Relations, The Biogenic Alteration of Sediments. Plenum Press, New York.Google Scholar
  36. Rice, D.L. 1986. Early diagenesis in bioadvective sediments: relationships between the diagenesis of beryllium-7, sediment reworking rates and the abundance of conveyor-belt deposit feeders.J. Mar. Res. 44:149–184.Google Scholar
  37. Roe, P. 1975. Aspects of life history and of territorial behavior in young individuals ofPlatynereis bicanaliculata andNereis vexillosa (Annelida, Polychaeta).Pac. Sci. 29:341–348.Google Scholar
  38. Rosenthal, G.A., andBerenbaum, M.R. 1991. Herbivores. Their Interactions with Secondary Plant Metabolites, 2nd ed. Academic Press, San Diego.Google Scholar
  39. Roughgarden, J., Gaines, S.D., andPossingham, H.P. 1988. Recruitment dynamics in complex life cycles.Science 241:1460–1466.Google Scholar
  40. Sheikh, Y.M., andDjerassi, C. 1975. 2,6-Dibromophenol and 2,4,6-tribromophenols-antiseptic secondary metabolites ofPhoronopsis vendis.Experientia 31:265–266.Google Scholar
  41. Steinberg, P.D. 1985. Feeding preferences ofTegula funebralis and chemical defenses of marine brown algae.Ecol. Monogr. 55:333–349.Google Scholar
  42. Strathmann, M.F. 1987. Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast. University of Washington Press, Seattle.Google Scholar
  43. Suer, A.L., andPhillips, D.W. 1983. Rapid, gregarious settlement of the larvae of the marine echiuranUrechis caupo Fisher and MacGinitie 1928.J. Exp. Mar. Biol. Ecol. 67:243–259.Google Scholar
  44. Thayer, C.W. 1983. Sediment-mediated biological disturbance and the evolution of marine benthos, pp. 480–625,in M.J.S. Tevesz and P.L. McCall (eds.). Biotic Interactions in Recent and Fossil Benthic Communities. Plenum Press, New York.Google Scholar
  45. Tjossem, S.F. 1990. Effects of fish chemical cues on vertical migration behavior ofChaoborus.Limnol. Oceanogr. 35:1456–1468.Google Scholar
  46. Underwood, A.J., andDenley, E.J. 1984. Paradigms, explanations, and generalizations in models for the structure of intertidal communities on rocky shores, pp. 151–180,in D.R. Strong, Jr., and D. Simberloff, L.G. Abele, and A.B. Thistle (eds.). Ecological Communities: Conceptual Issues and the Evidence. Princeton University Press, Princeton, New Jersey.Google Scholar
  47. Weber, K., andErnst, W. 1978. Occurrence of brominated phenols in the marine polychaeteLanice conchilega.Naturwissenschaften 65:262.Google Scholar
  48. Woodin, S.A. 1991. Recruitment of infauna: Positive or negative cues.Am. Tool. 31:797–807.Google Scholar
  49. Woodin, S.A., andMarinelu, R.L. 1991. Biogenic habitat modification in marine sediments: The importance of species composition and activity, pp. 231–250,in P.S. Meadows and A. Tufail (eds.). The Environmental Impact of Burrowing Animals and Animal Burrows. Zoological Society, London, No. 63.Google Scholar
  50. Woodin, S.A., Walla, M.D., andLincoln, D.E. 1987. Occurrence of brominated compounds in soft-bottom benthic organisms.J. Exp. Mar. Biol. Ecol. 107:209–217.Google Scholar

Copyright information

© Plenum Publishing Corporation 1993

Authors and Affiliations

  • Sarah A. Woodin
    • 1
    • 2
  • Roberta L. Marinelli
    • 2
  • David E. Lincoln
    • 1
  1. 1.Department of Biological SciencesUniversity of South CarolinaColumbia
  2. 2.Marine Science ProgramUniversity of South CarolinaColumbia
  3. 3.Department of OceanographyDalhousie UniversityHalifaxCanada

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