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Nereidid polychaetes as model organisms for marine chemical ecology

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Abstract

Nereidid polychaetes and indeed many marine invertebrates use chemical signaling via sex pheromones to coordinate their reproductive behaviour. Sex pheromones attract the sexual partner and ensure the coordinated release of gametes by both sexual partners. In the current paper nereidids are used as model organisms to describe the chemical and behavioural basis of chemical communication in marine invertebrates. Structure-activity relationships can be used to chemically classify signals according to their biological function and suitable purification strategies are described. Pheromones in nereidids include diverse molecules such as volatile lipophilic 5-methyl-3-heptanone and 3,5-octadiene-2-one, uric acid and small glutathione derived peptides. A prominent question in chemical signaling is the species specificity of chemical cues and the scale of their distribution in the marine environment. This evolves when one considers the wide overlap in multispecies and multiphyla spawning such as in coral reefs. Behavioural and electrophysiological assays with several nereidid species, confirm the existence of heterospecific activity of body fluids from various phyla. The 'nuptial dance′ reproductive behaviour, as well as the release of gametes, are elicited when individuals are exposed to coelomic fluid of another nereidid species and also from lugworms, starfish, and sea urchins. The function of sex pheromones in nereidid polychaetes and their role in the timing of reproduction in relation to other environmental cues is discussed. Future research will focus on biosynthesis and reception of nereidid pheromones as well as their molecular basis and possible interactions with pollutants such as endocrine disrupters and fuel oil derivatives.

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References

  • Agosta, W. C., 1992. Chemical communication: the language of pheromones. Scientific American Library Series, New York: 1–179.

    Google Scholar 

  • Atkinson, S. & M. J. Atkinson, 1992. Detection of estradiol 17b during a mass coral spawn. Coral Reefs 11: 33–36.

    Google Scholar 

  • Atema, J., 1995. Chemical signals in the marine environment: dispersal, detection, and temporal signal analysis. Proc. nat. Acad. Sci. U.S.A. 92: 62–66.

    Google Scholar 

  • Babcock, R. C., G. D. Bull., P. L. Harrison, A. J. Heyward, J. K. Oliver, C. C. Wallace & B. L. Willis, 1986. Synchronous spawning of 105 species of scleractinian corals on the Great Barrier Reef. Mar. Biol. 90: 379–394.

    Google Scholar 

  • Babcock, R. C., C. Mundy, J. Keesing & J. Oliver, 1992. Predictable and unpredictable spawning events: in situ behavioural data from free-spawning coral reef invertebrates. Int. J. Inv. Reprod. Dev. 22: 213–228.

    Google Scholar 

  • Bamber, S. D. & E. Naylor, 1996. The mating behaviour of male Carcinus maenas in relation to a putative sex pheromone: Behavioral changes in response to antennule restriction. Mar. Biol. 483–488.

  • Bartels-Hardege, H. D., 1993. Zur Reproduktionsbiologie von Nereis diversicolor und Nereis japonica und der Rolle von Pheromonen bei der Steuerung des Reproduktionsverhaltens. Thesis, University of Oldenburg: 1–127 (in German, with English summary).

  • Bartels-Hardege H. D., J. D. Hardege, M. Beckmann & C. Müller, 1996. Sex pheromones in marine polychaetes V: Biologically active compound from the coelomic fluid of female Nereis japonica (Annelida Polychaeta). J. exp. mar. Biol. Ecol. 201: 275–284.

    Google Scholar 

  • Beckmann, M., 1996. Identifikation von Substanzen im Rohöl zur Induktion der Spermaabgabe bei Nereis succinea und Platynereis dumerilii Männchen (Polychaeta, Annelida) und Identifikation des Pheromonkomplexes zur Induktion der Eiabgabe bei Nereis succinea Weibchen. Doctoral Thesis, University of Oldenburg, Tactum Verlag, Marburg: 153 pp. (in German, with English summary).

    Google Scholar 

  • Bengtson, M., T. Lilfjors, B. S. Hansson, C. Löfstedt & S. V. Copala, 1990. Structure activity relationships for chain shortened analogs of 5-decenyl acetate, a pheromone component of the turnip moth, Agrostis segetum. J. Chem. Ecol. 16: 667–684.

    Google Scholar 

  • Bentley, M. G. & A. A. Pacey, 1992. Physiological and environmental control of reproduction in polychaetes. Oceanogr. mar. Biol. Ann. Rev. 30: 139–148.

    Google Scholar 

  • Boilly-Marer, Y., 1974. Etude expérimentale du comportement nuptial de Platynereis dumerilii Aud. et M. Edw. (Annelida, Polychaeta): chemoreception, émission des produits genitaux. Mar. Biol. 24: 167–169.

    Google Scholar 

  • Boilly-Marer, Y., 1975. Essaimage de Platynereis dumerilii (Annélide, Polychète). Comportement nuptial et chemoreception. Vidéo scientifique. Service du Film de Recherche Scientifique, Paris.

    Google Scholar 

  • Boilly-Marer, Y. & B. Lassalle, 1978. Electrophysiological responses of heteronereids stimulated with sex pheromones. J. exp. Zool. 205: 119–124.

    Google Scholar 

  • Boilly-Marer, Y. & B. Lassalle, 1980. Electrophysiological responses of the central nervous system in the presence of homospecific and heterospecific sex pheromones in nereids (Annelida, Polychaeta). J. exp. Zool. 213: 33–39.

    Google Scholar 

  • Boilly-Marer, Y. & M. F. L'Homme, 1986. Sex pheromones in the marine polychaete Platynereis dumerilii Aud. and Edw. In Porchet, M., C. Andries & A. Dhainaut (eds), Advances in Invertebrate Reproduction, Vol. 4. Elsevier, Amsterdam: 494 pp.

    Google Scholar 

  • Boland, W., P. Ney, L. Jaenicke & G. Gassmann, 1984. A ‘closed loop stripping’ technique as a versatile tool for metabolic studies of volatiles. In Schreier, P. (ed.), Anal. Volatiles: Methods. Appl. Proc. Int. Workshop (1983), W. de Gruyter, Berlin: 371–380.

    Google Scholar 

  • Bouchard, S., B. Sainte-Marie & J. N. McNeil, 1996. Indirect evidence indicates female semiochemicals release male precopulatory behaviour in the snow crab, Chinoecetes opilio (Brachyura: Majidae). Chemoecology 7: 39–44.

    Google Scholar 

  • Butenandt, A., R. Beckmann, D. Stamm & E. Hecker, 1959. Ñber den Sexuallockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z. Naturforsch. 14: 283–284.

    Google Scholar 

  • Caspers, H., 1984. Spawning periodicity and habitat of the Palolo worm Eunice viridis (Polychaeta: Eunicidae) in the Samoan islands. Mar. Biol. 79: 229–236.

    Google Scholar 

  • Christensen, T. A., H. Mustaparta & J. G. Hildebrand, 1989. Discrimination of sex pheromone blends in the olfactory system of the moth. Chem. Senses, 14: 463–477.

    Google Scholar 

  • Christofferson, J. P., 1978. Evidence for the controlled release of a crustacean sex pheromone. J. Chem. Ecol. 4: 633–639.

    Google Scholar 

  • Cowan, D. & J. Atema, 1990. Moult staggering and serial monogamy in American lobsters, Homarus americanus. Anim. Behav. 39: 1199–1206.

    Google Scholar 

  • Delaunay, H., 1931. L'excrétion azotée des invetébrés. Biol. Rev. 6: 265–301.

    Google Scholar 

  • Du, G., C. S. Ng & G. D. Prestwich, 1994. Odorant binding by a pheromone binding protein: active site mapping by photoaffinity labelling. Biochemistry, 33: 4812–4819.

    Google Scholar 

  • Dunham, P. J., 1978. Sex pheromones in Crustacea. Biol. Rev. 53: 555–583.

    Google Scholar 

  • Dunham, P. J., 1988. Pheromones and behaviour in Crustacea. In Laufer, H. & R. Downer (eds), Endocrinology of Selected Invertebrate Types. Alan R. Liss, New York: 375–392.

    Google Scholar 

  • Eales, A. J., 1974. Sex pheromone in the shore crab Carcinus maenas, and the site of its release from females. Mar. Behav. Physiol. 2: 345–355.

    Google Scholar 

  • Edwards, P. A. & P. C. Jurs, 1989. Correlation of odor intensities with structural properties of odorants. Chem. Senses 14: 281–291.

    Google Scholar 

  • Eisner, T. & J. Meinwald, 1995. Chemical ecology. National Academy Press, Washington.

    Google Scholar 

  • Fage, L. & R. Legendre, 1927. Pêches planctonique à la lumière effectuées à Banyuls-sur-Mer et a Concarneau; Annélides polychètes. Arch. Zool. exp. gén. 67: 23–222.

    Google Scholar 

  • Fischer, A., 1984. Control of oocyte differentiation in nereids (Annelida, Polychaeta) – facts and ideas. In Fischer, A. & H. D. Pfannenstiel (eds), Polychaete Reproduction: Progress in Comparative Reproductive Biology, Fortschr. Zool. 29: 227–245.

  • Fischer, A., H. Rabien & A. E. Heacox, 1991. Specific, concentration dependant uptake of vitellin, the yolk protein of the annelid Nereis virens. Differentiation 19: 103–108.

    Google Scholar 

  • Fischer, A. & U. Hoeger, 1993. Metabolic links between sexual maturation and oogenesis in nereid annelids – a brief review. Invert. Reprod. Dev. 23: 131–138.

    Google Scholar 

  • Fischer, A., A.W. C. Dorresteijn & U. Hoeger, 1996. Metabolism of oocyte construction and the generation of histospecificity in the cleaving egg. Lessions from nereid annelids. Int. J. Dev. Biol. 40: 421–430.

    Google Scholar 

  • Foltz, K. R., 1995. Gamete recognition and egg activation in sea urchins. Am. Zool. 35: 381–390.

    Google Scholar 

  • Francke, W., 1984. Convergency and diversity in insect pheromones. In Porchet, M. (ed.), Advances in Invertebrate Reproduction 4, Elsevier, Amsterdam. 327–336.

    Google Scholar 

  • Franke, H. D., 1985. On a clocklike mechanism timing lunarrhythmic reproduction in Typosyllis prolifera (Polychaeta). J. Comp. Physiol. (Sect. A), 156: 553–561.

    Google Scholar 

  • Gleeson, R. A., 1980. Pheromone communication in the reproductive behaviour of the blue crab, Callinectes sapidus. Mar. Behav. Physiol. 7: 119–134.

    Google Scholar 

  • Goerke, H., 1979. Nereis virens (Polychaeta) in a marine pollution research: culture methods and oral administration of a polychlorinated biphenyl. Veröff. Inst. Meeresf. Bremerh. 17: 151–161.

    Google Scholar 

  • Goerke, H., 1984. Temperature-dependence of swarming in North Sea Nereidae. In Fischer, A. & H.-D. Pfannenstiel (eds), Polychaete Reproduction: Progress in Comparative Reproductive Biology, Fortschr. Zool. 29: 29–43.

  • Gomez, G. & J. Atema, 1996. Temporal resolution in olfaction: stimulus integration time of lobster chemoreceptor cells. J. exp. Biol. 199: 1771–1779.

    Google Scholar 

  • Hardege J. D., H. D. Bartels-Hardege, E. Zeeck & F. T. Grimm, 1990. Induction of swarming in Nereis succinea. Mar. Biol. 104: 291–295.

    Google Scholar 

  • Hardege J. D., H. D. Bartels-Hardege, Y. Yu, M. Y. Zhu, B. L. Wu & E. Zeeck, 1994. Environmental control of reproduction of Perinereis nuntia var. brevicirrus. J. mar. biol. Ass. U.K. 74: 903–918.

    Google Scholar 

  • Hardege, J. D., 1992. Verhaltensmodifizierende Naturstoffe (Pheromone) bei der Fortpflanzung von Nereiden (Annelida, Polychaeta), University of Oldenburg, Doctoral Thesis. 1–186 (in German, with English summary).

  • Hardege, J. D., M. Beckmann & C. Müller, 1997. A waterborne female sex pheromone in the ragworm, Nereis succinea (Annelida, Polychaeta). Polychaete Research 17:18–21

    Google Scholar 

  • Hardege, J. D., H. D. Bartels-Hardege, C. T. Müller, M. Beckmann, S. J. Harrison, G. Watson & M. G. Bentley, 1998a. Epidemic spawning in marine invertebrates (submitted).

  • Hardege, J. D., C. T. Müller, M. Beckmann, H. D. Bartels-Hardege & M. G. Bentley, 1998b. Timing of reproduction in marine polychaetes: The role of sex pheromones, Ecoscience, 5: 395–404.

    Google Scholar 

  • Hauenschild, C., 1956. Neue experimentelle Untersuchungen zum Problem der Lunarperiodizität. Naturwissenschaften 16: 361–363.

    Google Scholar 

  • Hauenschild, C. & A. Fischer, 1969. Platynereis dumerilii. Mikroskopische Anatomie, Fortpflanzung, Entwicklung. Großes Zoologisches Praktikum, 10 b, Gustav Fischer Verlag, Stuttgart.

    Google Scholar 

  • Himmelman, J., 1981. Synchronization of spawning of marine invertebrates by phytoplankton. In Clark, W. J. Jr. & T. S. Adamson (eds), Advances in Invertebrate Reproduction. Elsevier North Holland, Amsterdam: 1–19.

    Google Scholar 

  • Hoegh-Guldberg, O. & J. S. Pearse, 1995. Temperature, food availability and the development of marine invertebrate larvae. Am. Zool. 35: 415–425.

    Google Scholar 

  • Holland, D. L., J. East, K. H. Gibson, E. Clayton & A. Old-field, 1985. Identification of the hatching factor of the barnacle Balanus balanoides as the novel eicosanoid 10,11,12-trihydroxy-5,8,14,17-eicostetraenoic acid. Prostaglandins 29: 1021–1030.

    Google Scholar 

  • Howie, N. R. & Y. M. Sheikh, 1975. Anthopleurine: a sea anemone alarm pheromone. Science 189: 386–388.

    Google Scholar 

  • Jaenicke, L. & W. Boland, 1982. Signalstoffe und ihre Rezeption im Sexualzyklus mariner Braunalgen. Angew. Chemie 94: 655–724.

    Google Scholar 

  • Karlson, P. & M. Lüscher, 1959. Pheromone, ein Nomenklatur-Vorschlag für eine Wirkstoffklasse. Naturwissenschaften 46: 63–64.

    Google Scholar 

  • Kittredge, J. S., M. Terry & F. T. Takahashi, 1971. Sex pheromone activity of the moulting hormone crustecdysone on male crabs (Pachygrapsus crassipes, Cancer antennarius and Cancer anthonyi). Fish. Bull. 69: 337–343.

    Google Scholar 

  • Lillie, F. R. & E. F. Just, 1913. Breeding habits of the heteronereis form of Nereis limbata at Whitstable Mass. Biol. Bull. 24: 147–160.

    Google Scholar 

  • McKenna, M. P., D. S. Hekmat-Scafe, P. Gaines & J. R. Carlson, 1994 Putative Drosophila pheromone binding protein expressed in a subregion of the olfactory system. J. Biol. Chem. 269: 16340–16347.

    Google Scholar 

  • Mill, J. P., 1978. Physiology of annelids. Academic Press, London.

    Google Scholar 

  • Minchin, D., 1992. Multiple species, mass spawning events in an Irish sea lough: the effect of temperature on spawning and recruitment of invertebrates. Invert. Reprod. Dev. 22: 229–238.

    Google Scholar 

  • Müller, D. G., 1976. Quantitative evaluation of sexual chemotaxis in two marine brown algae. Z. Pflanzenphys. 80: 120–130.

    Google Scholar 

  • Müller, C., 1995. Isolation und Identifikation eines Sexualpheromons bei Nereis succinea. Doctoral Thesis, Univ. of Oldenburg (in German, with English summary).

  • Murata, M., K. Miyagawa-Kohshima, K. Nakanishi & Y. Naya, 1986. Characterization of compounds that induce symbiosis between sea anemone and anemone fish. Science 234: 585–587.

    Google Scholar 

  • Olive, P. J. W., 1997. 5. Annelida-Polychaeta. In Adiyodi, K. G., R. G. Adiyodi & T. S. Adams (eds), Reproductive Biology of Invertebrates. Oxford & IBH Publ. Co. PVT. Ltd., New Delhi: 153–189.

    Google Scholar 

  • Painter, S. D., 1992. Coordination of reproductive activity in Aplysia: peptide neurohormones, neurotransmitters, and pheromones encoded by the egg-laying hormone family of genes. Biol. Bull. 183: 165–172.

    Google Scholar 

  • Pettis, R. J., B. W. Erickson, R. B. Forward & D. Rittschoff, 1993. Superpotent synthetic tripeptide mimics of the mud-crab pumping pheromone. Int. J. Peptide Protein Res. 42: 312–319.

    Google Scholar 

  • Rasmussen, E., 1973. Systematics and ecology of the Isefjord marine fauna (Denmark). Ophelia 11: 1–507.

    Google Scholar 

  • Rittschoff, D., 1990. Peptide-mediated behaviors in marine organisms. J. Chem. Ecol. 16: 261–272.

    Google Scholar 

  • Rodríguez, S. R., F. P. Ojeda & N. C. Inestrosa, 1993. Settlement of benthic marine invertebrates. Mar. Ecol. Progr. Ser. 97: 193–207.

    Google Scholar 

  • Ryan, E. P., 1966. Pheromone: evidence in decapod Crustacea. Science 151: 340–341.

    Google Scholar 

  • Schleicher, S., Boeckhoff, I. & H. Breer, 1994. Pheromone-induced phosphorylation of antennal proteins from insects. J.Comp. Physiol. B. 164: 76–80.

    Google Scholar 

  • Schneider, D., 1957. Elektrophysiologische Untersuchungen von Chemo-und Mechanorezeptoren der Antenne des Seidenspinners Bombyx mori. Z. vergl. Physiol. 40: 9–41.

    Google Scholar 

  • Seifert, P., 1982. Studies on the sex pheromone of the shore crab, Carcinus maenas, with special regard to ecdysone excretion. Ophelia 21: 147–158.

    Google Scholar 

  • Smith, J. R. & D. R. Strehlow, 1983. Algal-induced spawning in the marine mussel Mytilus californicanus. Invert. Reprod. Dev. 6: 129–133.

    Google Scholar 

  • Shorey, H. H., 1977. Animal Communication by Pheromones. Academic Press, New York.

    Google Scholar 

  • Starr, M., J. H. Himmelmann & J. C. Therriault, 1990. Direct coupling of marine invertebrate spawning with phytoplankton blooms. Science 247: 1071–1074.

    Google Scholar 

  • Starr, M., J. H. Himmelmann & J. C. Therriault, 1991. Coupling of nauplii release in barnacles with phytoplankton blooms: a parallel strategy to that of spawning in urchins and mussels. J. Plankton Res. 13: 561–571.

    Google Scholar 

  • Starr, M., J. H. Himmelmann & J. C. Therriault, 1992. Isolation and properties of a substance from the diatom Phaeodactylum tricornutum which induces spawning in the sea urchin Strongylocentrotus droebachiensis. Mar. Ecol. Progr. Ser. 79: 275–287.

    Google Scholar 

  • Strunk, C., 1930. Excretionsphysiologische Studien an den Polychäten Polymnia nebulosa und Lanice conchilega. Zool. Jb. 48: 385–398.

    Google Scholar 

  • Townsend, G., 1939. On the nature of the material elaborated by fertiliziable Nereis eggs inducing spawning of the male. Biol. Bull. 77: 306–307.

    Google Scholar 

  • Wilber, C. G., 1948. Uric acid in marine invertebrates. J. cell. comp. Physiol. 31: 107–110.

    Google Scholar 

  • Withers, P. C., 1992. Comparative Animal Physiology. Saunders College Publishing, Fort Worth, U.S.A.

    Google Scholar 

  • Wu, B. L., R. P. Sun & D. L. Yang, 1984. The Nereidae (Polychaetous Annelids) of the Chinese Coast, China Ocean Press, Springer, Beijing, 234 pp..

    Google Scholar 

  • Zeeck, E., J. D. Hardege, H. Bartels-Hardege & G. Wesselmann, 1988. Sex pheromone in a marine polychaete: determination of the chemical structure. J. exp. Zool. 246: 285–292.

    Google Scholar 

  • Zeeck E., J. D. Hardege & H. D. Bartels-Hardege, 1990. Sex pheromones and reproductive isolation in two nereid species, Nereis succinea and Platynereis dumerilii. Mar. Ecol. Progr. Ser. 67: 183–188.

    Google Scholar 

  • Zeeck, E. & J. D. Hardege, 1990. Sex pheromones in nereids: volatile compounds of the coelomic fluid of Nereis virens, Z. Naturforsch. 45c: 924–925.

    Google Scholar 

  • Zeeck E., J. D. Hardege, H. D. Bartels-Hardege, A. Willig & G. Wesselmann, 1991. Sex pheromones in amarine polychaete: biological active compounds from Platynereis dumerilii females. J. exp. Zool. 260: 93–98.

    Google Scholar 

  • Zeeck, E., J. D. Hardege, A. Willig, R. Krebber & W. A. König, 1992. Preparative separation of enantiomeric polychaete sex pheromones. Naturwissenschaften 79: 182–183.

    Google Scholar 

  • Zeeck, E., J. D. Hardege, N. Ikekawa & Y. Fujimoto, 1994. Sex pheromones in marine polychaetes: Steroids from ripe Nereis succinea. Steroids 59: 341–344.

    Google Scholar 

  • Zeeck, E., T. Harder, M. Beckmann & C. T. Müller, 1996. Marine gamete-release pheromones. Nature 382: 214.

    Google Scholar 

  • Zeeck, E., T. Harder & M. Beckmann, 1998a. Uric acid – the sperm release pheromone of the marine polychaete Platynereis dumerilii. J. Chem. Ecol. 24: 13–23.

    Google Scholar 

  • Zeeck, E., C. T. Müller, M. Beckmann, J. D. Hardege, U. Papke, V. Sinnwell, F. C. Schröder & W. Francke, 1998b. Cysteineglutathione disulfide, the sperm-release pheromone of the marine polychaete Nereis succinea (Annelida: Polychaeta). Chemoecology 8: 33–38

    Google Scholar 

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Hardege, J.D. Nereidid polychaetes as model organisms for marine chemical ecology. Hydrobiologia 402, 145–161 (1999). https://doi.org/10.1023/A:1003740509104

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