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Allelochemical inhibition of recruitment in a sedimentary assemblage

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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.

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References

  • 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 

  • 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 

  • Ashworth, R.B., andCormier, M.J. 1967. Isolation of 2,6-dibromophenol from the marine hemichordateBalanoglossus biminiensis.Science 155:1558–1559.

    Google Scholar 

  • Braekman, J.C., andDaloze, D. 1986. Chemical defence in sponges.Pure Appl. Chem. 58:357–364.

    Google Scholar 

  • Buhr, K.-J. 1976. Suspension-feeding and assimilation efficiency inLanice conchilega (Polychaeta).Mar. Biol. 38:373–383.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • Emerson, S., Jahnke, R., andHeggie, D. 1984. Sediment-water exchange in shallow water estuarine sediments.J. Mar. Res. 42:709–730.

    Google Scholar 

  • Emrich, R., Weyland, H., andWeber, K. 1990. 2,3,4-Tribromopyrrole from the marine polychaetePolyphysia crass.J. Nat. Prod. 53:703–705.

    Google Scholar 

  • Faulker, D.J. 1984. Marine natural products: metabolites of marine algae and herbivorous molluscs.Nat. Prod. Rep. 1:251–280.

    Google Scholar 

  • Feeny, P. 1976. Plant apparency and chemical defense.Recent Adv. Phytochem. 10:1–40.

    Google Scholar 

  • 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 

  • 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 

  • Grosberg, R.K. 1981. Competitive ability influences habitat choice in marine invertebrates.Nature 290:700–702.

    Google Scholar 

  • 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 

  • Hadfield, M.G. 1984. Settlement requirements of molluscan larvae: New data on chemical and genetic roles.Aquaculture 39:283–298.

    Google Scholar 

  • 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 

  • Hay, M.E., andFenical, W. 1988. Marine plant-herbivore interactions: The ecology of chemical defense.Annu. Rev. Ecol. Syst. 19:111–145.

    Google Scholar 

  • Higa, T., andScheuer, P.J. 1975. Constituents of the marine annelidThelepus setosus.Tetrahedron 31:2379–2381.

    Google Scholar 

  • 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 

  • Higa, T., Fujiyama, T., andScheuer, P.J. 1980. Halogenated phenol and indole constituents of acorn worms.Comp. Biochem. Physiol. 65B:525–530.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Johnson, M.W. 1943. Studies on the life history of the marine annelidNereis vexillosa.Biol. Bull. 84:106–114.

    Google Scholar 

  • King, G.M. 1986. Inhibition of microbial activity in marine sediments by a bromophenol from a hemichordate.Nature 323:257–259.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Paul, V.J. 1987. Feeding deterrent effects of algal natural products.Bull. Mar. Sci. 41:514–522.

    Google Scholar 

  • 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 

  • 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.

  • 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 

  • 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 

  • 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 

  • Rosenthal, G.A., andBerenbaum, M.R. 1991. Herbivores. Their Interactions with Secondary Plant Metabolites, 2nd ed. Academic Press, San Diego.

    Google Scholar 

  • Roughgarden, J., Gaines, S.D., andPossingham, H.P. 1988. Recruitment dynamics in complex life cycles.Science 241:1460–1466.

    Google Scholar 

  • 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 

  • Steinberg, P.D. 1985. Feeding preferences ofTegula funebralis and chemical defenses of marine brown algae.Ecol. Monogr. 55:333–349.

    Google Scholar 

  • Strathmann, M.F. 1987. Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast. University of Washington Press, Seattle.

    Google Scholar 

  • 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 

  • 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 

  • Tjossem, S.F. 1990. Effects of fish chemical cues on vertical migration behavior ofChaoborus.Limnol. Oceanogr. 35:1456–1468.

    Google Scholar 

  • 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 

  • Weber, K., andErnst, W. 1978. Occurrence of brominated phenols in the marine polychaeteLanice conchilega.Naturwissenschaften 65:262.

    Google Scholar 

  • Woodin, S.A. 1991. Recruitment of infauna: Positive or negative cues.Am. Tool. 31:797–807.

    Google Scholar 

  • 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 

  • 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 

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Woodin, S.A., Marinelli, R.L. & Lincoln, D.E. Allelochemical inhibition of recruitment in a sedimentary assemblage. J Chem Ecol 19, 517–530 (1993). https://doi.org/10.1007/BF00994322

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