Skip to main content
Log in

Reproductive and developmental phenomena in annelids: a source of exemplary research problems

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Specific traits of reproduction, of early and postembryonic development and of sexual maturation in annelids are reported, and the existing and expected contributions to this field from the study of annelids are discussed. The study of early development, as in other spiralians, reveals the existence of canonical cleavage patterns and the combined action of antithetical principles, namely determination by stereotypic sorting-out of 'determinants′ and determination depending upon the interactions between the blastomeres. A high potential of information about the processes of metameric trunk segment formation and of segment specification has only begun to be exploited in annelids. Epitoky, the formation of a free-swimming sexual form in polychaetes, involving tissue transdifferentiation and conversion of metabolism, locomotory and sensory capacities, is discussed as a mostly one-way developmental process. The study of epitoky sheds light on the metabolic relations between soma and germ cells and on related control mechanisms. The members of epitokous species are synchronized by meteorological parameters and by pheromones and are adapted to spawn under pelagic conditions. The metameric construction of the trunk predisposes for asexual reproduction by fission into trunk fragments regenerating into complete worms. This mode of reproduction is frequent among polychaetes and oligochaetes. Trunk fission has been modified in many polychaetes: posterior fragments ('stolons′) are formed, which take over the function of pelagic, epitokous sexuals and leave behind a 'stock′ which lacks somatic sexual differentiation and can bud further stolons. Naturally occurring, as well as experimentally induced regeneration, as well as the stolonization phenomenon, reveal the existence of morphogenetic gradients and of positional information along the annelid trunk.

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.

Similar content being viewed by others

References (*asterisks: review articles)

  • Åkesson, B., 1975. Reproduction in the genus Ophryotrocha (Polychaeta, Dorvilleidae). Pubbl. Staz. Zool. Napoli 39 (Suppl): 377–398.

    Google Scholar 

  • Åkesson, B. & S. A. Rice, 1992. Two new Dorvillea species (Polychaeta, Dorvilleidae) with obligate asexual reproduction. Zool. Scr. 21: 351–362.

    Google Scholar 

  • *Anderson, D. T., 1966. The comparative embryology of the Polychaeta. Acta zool. 47: 1–42.

    Google Scholar 

  • Astrow, S., B. Holton & D. Weisblat, 1987. Centrifugation redistributes factors determining cleavage patterns in leech embryos. Dev. Biol. 120: 270–283.

    Google Scholar 

  • Bacci, G., 1978. Genetics of sex determination in Ophryotrocha (Annelida, Polychaeta). In Battaglia, B. & J. Beardmore (eds), Marine Organisms. New York, Plenum Press: 549–571.

    Google Scholar 

  • Baert, J. L. & M. C. Slomianny, 1992. Vitellin accumulation and vitellogenin synthesis in relation to oogenesis in Perinereis cultrifera (Polychaeta Annelida). Invert. Reprod. Dev. 21: 121–128.

    Google Scholar 

  • Bartels-Hardege, H. D., J. D. Hardege, E. Zeeck, C. Müller, B. L. Wu & M. Y. Zhu, 1996. Sex pheromones in marine polychaetes V: a biologically active volatile compound from the coelomic fluid of female Nereis (Neanthes) japonica (Annelida Polychaeta). J. exp. mar. Biol. Ecol. 201: 275–284.

    Google Scholar 

  • Bauchot-Boutin, M. L. & G. Bobin, 1954. Modifications hétéronéréidiennes des parapodes, des soies, et des bulbes sétigères chez Perinereis cultrifera Grube (Annélide: Polychète). Arch. Anat. micr. Morph. exp. 43: 137–162.

    Google Scholar 

  • *Bentley, M. G. & A. A. Pacey, 1992. Physiological and environmental control of reproduction in polychaetes. Oceanogr. Mar. Biol. Annu. Rev. 30: 443–481.

    Google Scholar 

  • Berrill, N. J., 1931. Regeneration in Sabella pavonina (Sav.), and other sabellid worms. J. exp. Zool. 58: 495–523.

    Google Scholar 

  • *Bissen, S. T., 1996. Developmental control of cell division in leech embryos. BioEssays 19: 201–207.

    Google Scholar 

  • Blake, J. A. & J. D. Kudenov, 1981. Larval development, larval nutrition and growth of two Boccardia species (Polychaeta: Spionidae) from Victoria, Australia. Mar. Ecol. Progr. Ser. 6:175–182.

    Google Scholar 

  • Boilly, B., 1974. Mode d'action du cerveau sur la régénération caudale de Nereis diversicolor (O. F. Müller). Wilhelm Roux's Arch. Entwickl. Mech. Org. 174: 195–209.

    Google Scholar 

  • Boilly-Marer, Y., 1969. Recherches expérimentales sur la danse nuptiale de Platynereis dumerilii Audouin et Milne-Edwards (Annélide: Polychète). Origine et modalités d'action de la substance excitatrice. Cah. Biol. mar. 10: 255–269.

    Google Scholar 

  • Boilly-Marer, Y., 1974. Étude expérimentale du comportement nuptial de Platynereis dumerilii (Annelida: Polychaeta): chémoréception, émission des produits génitaux. Mar. Biol. 24:167–179.

    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 nereidids. (Annelida: Polychaeta) J. exp. Zool. 213: 33–39.

    Google Scholar 

  • Brafield, A. & G. Chapman, 1967. Gametogenesis and breeding in a natural population of Nereis virens. J. mar. biol. Ass. U.K. 47:619–627.

    Google Scholar 

  • Casanova, G., 1955. Influence du prostomium sur la régénération caudale chez Platynereis massiliensis (Moquin-Tandon). C. r. Acad. Sci., Paris 241: 1814–1816.

    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 

  • Claparède, E., 1870. Les Annélides Chétopodes du Golfe de Naples (Supplément) 20: 365–542.

    Google Scholar 

  • *Clark, R. B., 1961. The origin and formation of the heteronereis. Biol. Rev. 36: 199–236.

    Google Scholar 

  • Costello, D. P., 1948. Ooplasmic segregation in relation to differentiation. Ann. N.Y. Acad. Sci. 49: 663–683.

    Google Scholar 

  • Costello, D. P. & C. Henley, 1971. Methods for obtaining and handling marine eggs and embryos, 2nd edition. Mar. Biol. Lab., Woods Hole, Mass. 249 pp.

  • Creaser, P. & D. A. Clifford, 1982. Life history studies of the sandworm, Nereis virens Sars, in the Sheepscot estuary, Maine. Fish. Bull. 80: 735–743.

    Google Scholar 

  • *Cross, N. L., 1984. Fertilization in Urechis caupo and in polychaetes. Fortschr. Zool. 29: 149–166.

    Google Scholar 

  • *Davidson, E. H., 1990. How embryos work: a comparative view of diverse modes of cell fate specification. Development 108: 365–389.

    Google Scholar 

  • Defretin, R., 1949. Recherches sur la musculature des Néréidiens au cours de l'épitoquie, sur les glandes parapodiales et sur la spermiogenèse. Ann. Inst. Oceanogr. 24: 117–257.

    Google Scholar 

  • Dorresteijn, A. W. C., 1990. Quantitative analysis of cellular differentiation during early embryogenesis of Platynereis dumerilii. Roux's Arch. Dev. Biol. 199: 14–30.

    Google Scholar 

  • *Dorresteijn, A.W. C., 1998. How do spiralian embryos accomplish cell diversity? Zoology 100: 307–319.

    Google Scholar 

  • Dorresteijn, A. W. C., H. Bornewasser & A. Fischer, 1987. A correlative study of experimentally changed first cleavage and Janus development in the trunk of Platynereis dumerilii (Annelida: Polychaeta). Roux's Arch. Dev. Biol. 196: 51–58.

    Google Scholar 

  • Dorresteijn, A.W. C. & P. Eich, 1991. Experimental change of cytoplasmic composition can convert determination of blastomeres in Platynereis dumerilii (Annelida, Polychaeta). Roux's Arch. Dev. Biol. 200: 342–351.

    Google Scholar 

  • *Dorresteijn, A. W. C. & A. Fischer, 1988. The process of early development. In Westheide, W. & C. O. Hermans (eds), The Ultrastructure of Polychaeta. Microfauna Mar. 4: 335–352.

  • Durchon, M., 1948a. Épitoquie expérimentale chez deux Polychètes: Perinereis cultrifera Grube et Nereis irrorata Malmgren. C. r. Acad. Sci., Paris 227: 157–158.

    Google Scholar 

  • Durchon, M., 1948b. Inhibition de l'épitoquie par le prostomium chez les Néréidiens (Annélides polychètes). C. r. Acad. Sci., Paris 229: 81–82.

    Google Scholar 

  • Durchon, M., 1951. Stolonisation et hermaphroditisme successif chez Syllis amica Quatrefage. Arch. Zool. exp. gén. 88: 96–100.

    Google Scholar 

  • Durchon, M., 1952. —Recherches expérimentales sur deux aspects de la reproduction chez les Annélides Polychètes: l'épitoquie et la stolonisation. Ann. Sci. nat. (Zool. et Biol. Animale) Sér XI, 14:117–206.

    Google Scholar 

  • Durchon, M., 1955. Sur le polymorphisme présenté par quelques Néréidiens (Annélides Polychètes) au moment de la reproduction. Bull. Soc. Hist. Nat. Afr. Nord 46: 180–194.

    Google Scholar 

  • Durchon, M., 1959. Contribution à l'étude de la stolonisation chez les Syllidiens (Annélides Polychètes): I. Syllidae. Bull. biol. Fr. Belg. 93: 155–219.

    Google Scholar 

  • Durchon, M. & M. Porchet, 1971. Premières données quantitatives sur l'activité endocrine du cerveau des Néreidiens au cours de leur cycle sexuel. Gen. Comp. Endocrinol. 16: 555–565.

    Google Scholar 

  • Durchon, M. & J. C. Wissocq, 1964. Contribution a l'étude de la stolonisation chez les syllidiens (Annélides: Polychètes). Ann. Sci. nat. (Zool. et Biol. Animale) Sér XII, 6: 159–212.

    Google Scholar 

  • *Eckberg, W. R. & S. D. Hill, 1996. Chaetopterus-oocyte maturation, early development, and regeneration. Mar. Mod. Elec. Rec. [serial online; cited Sept. 23, 1997]. Available from http://www.mbl.edu/html/BB/MM ER/ECK/EckTit.html

  • Eckelbarger, K.J., 1978. Metamorphosis and settlement in the Sabellariidae. In Chia, F.-S. & S. A. Rice (eds), Settlement and Metamorphosis of Marine Invertebrate Larvae. Elsevier/North-Holland Biomedical Press: 145–164.

  • *Eckelbarger, K. J., 1992. Oogenesis. In Harrison, F. W. & S. L. Gardiner (eds), Microscopic Anatomy of Invertebrates. Vol. 7, chapter 2 (Polychaeta). Wiley-Liss. Inc., New York: 109–127.

    Google Scholar 

  • Ehlers, E., 1868. Die Borstenwürmer. Annelida Polychaeta. Vol. 2. Leipzig: Engelmann

  • Ehlers, E., 1900. Ñber Atlantischen Palolo. Nachr. K. Ges. Wiss. Göttingen, Math-phys. Kl. 397–399.

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

    Google Scholar 

  • *Fernández, J., V. Téllez & N. Olea, 1992. Hirudinea. In Harrison, F. W. & S. L. Gardiner (eds), Microscopic Anatomy of Invertebrates. Vol. 7, Wiley-Liss. Inc., New York: 323–394.

    Google Scholar 

  • *Ferraguti, M. & C. Erséus, 1999. Sperm types and their use for a phylogenetic analysis of aquatic clitellates. Hydrobiologia 402 (Dev. Hydrobiol. 142): 225–237.

    Google Scholar 

  • Fischer, A., 1963. Ñber den Bau und die Hell-Dunkel-Adaptation der Augen des Polychäten Platynereis dumerilii. Z. Zellforsch.61: 338–353.

    Google Scholar 

  • Fischer, A., 1974. Stages and stage distribution in early oogenesis in the annelid, Platynereis dumerilii. Cell Tiss. Res. 156: 35–45.

    Google Scholar 

  • Fischer, A., 1983. The earliest events in spiralian development (Platynereis, Sabellaria, Pomatoceros). Film Nr. C 1476 (en) Inst. f. d. wiss. Film, Box 2351, D-37013 Göttingen.

  • *Fischer, A., 1984. Control of oocyte differentiation in nereidids (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., 1985. Reproduction and postembryonic development of the annelid Platynereis dumerilii. Film C 1577 (en) Inst. f. d. wiss. Film, Box 2351, D-37013 Göttingen.

  • Fischer, A., 1997. Reproducing once in a lifetime: a different mode of organizing gametogenesis. J. Reprod. Devel. 43: 41–42. (Suppl).

    Google Scholar 

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

    Google Scholar 

  • Fischer, A. & U. Fischer,1995. On the life-style and life-cycle of the luminescent polychaete Odontosyllis enopla (Annelida: Polychaeta). Invert. Biol. 114: 236–247.

    Google Scholar 

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

    Google Scholar 

  • Fischer, A., K. Mewes & H. D. Franke, 1992. Stolonisation and mating behavior of Autolytus prolifer (Polychaeta). Film C 1799 (en) Inst. f. d. wiss. Film, Box 2351, D-37013 Göttingen.

  • *Fischer, A. & H. D. Pfannenstiel (eds), 1984. Polychaete Reproduction. Progress in Comparative Reproductive Biology. Fortschr. Zool. 29: 341 pp.

  • Fong, P. P & J. S. Pearse, 1992. Photoperiodic regulation of parturition in the self-fertilizing viviparous polychaete Neanthes limnicola from central California. Mar. Biol. 112: 81–89.

    Google Scholar 

  • Franke, H. D., 1980. Zur Determination der zeitlichen Verteilung von Fortpflanzungsprozessen in Laborkulturen des Polychaeten Typosyllis prolifera. Helgoländer Meeresunters. 34: 61–84.

    Google Scholar 

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

    Google Scholar 

  • *Franke, H. D., 1986a. The role of light and endogenous factors in the timing of the reproductive cycle of Typosyllis prolifera and some other polychaetes. Am. Zool. 26: 433–445.

    Google Scholar 

  • Franke, H. D., 1986b. Sex ratio and sex change in wild and laboratory populations of Typosyllis prolifera (Polychaeta). Mar. Biol.90: 197–208.

    Google Scholar 

  • *Franke, H. D. & H. D. Pfannenstiel, 1984. Some aspects of endocrine control of polychaete reproduction. Fortschr. Zool. 29:53–72.

    Google Scholar 

  • Freeman, G. & J. W. Lundelius, 1992. Evolutionary implications of the mode of D quadrant specification in coelomates with spiral cleavage. J. evol. Biol. 5: 205–247.

    Google Scholar 

  • Galloway, T. W. & P. S. Welch, 1911. Studies on a phosphorescent Bermudan annelid, Odontosyllis enopla Verrill. Trans. am. Microsc. Soc. 30: 13–39.

    Google Scholar 

  • Garwood, P. R., 1991. Reproduction and classification of the family Syllidae (Polychaeta). In Petersen, M. E. & J. B. Kirkegaard (eds), Proc. 2nd Int. Polychaete Conf. Copenhagen1986. Ophelia Suppl 5: 81–87.

  • George, J. D. & M. E. Peterson, 1991. The validity of the genus Zeppelina Vaillant (Polychaeta: Ctenodrilidae). In Petersen, M. E. & J. B. Kirkegaard (eds), Proc. 2nd Int. Polychaete Conf. Copenhagen 1986. Ophelia Suppl. 5: 89–100.

  • Gibson, G. D., 1997. Variable development in the spionid Boccardia proboscidea (Polychaeta) is linked to nurse egg production and larval trophic mode. Invert. Biol. 116: 213–226.

    Google Scholar 

  • Gibson, P. H. & R. B. Clark, 1976. Reproduction of Dodecaceria caulleryi (Polychaeta: Cirratulidae). J. mar. biol. Ass. UK. 56:649–674.

    Google Scholar 

  • Gidholm, L., 1965. On the morphology of the sexual stages, mating and egg-laying in Autolytus (Polychaeta). Zool. Bidr. Upps. 37:1–44.

    Google Scholar 

  • Goerke, H., 1984. Temperature-dependence of swarming in North Sea Nereidae. Fortschr. Zool. 29: 39–43.

    Google Scholar 

  • Golding, D. W., 1967. Endocrinology, regeneration and maturation in Nereis. Biol. Bull. 133: 567–577.

    Google Scholar 

  • Golding, D. W., 1983. Endocrine programmed development and reproduction in Nereis. Gen. Comp. Endocrinol. 52: 456–466.

    Google Scholar 

  • Gravier, D. & J. L. Dantan 1928. Pêches nocturnes à la lumière dans la Baie d'Alger. Annélides polychètes. Ann. Inst. Oceanogr. (Paris) 5: 1–187.

    Google Scholar 

  • Hamond, R., 1974. The culture, experimental taxonomy, and comparative morphology of the planktonic stages of Norfolk autolytoids (Polychaeta: Syllidae: Autolytinae). Zool. J. Linn. Soc. 54:299–320.

    Google Scholar 

  • Hartmann, M. & W. Huth, 1936. Untersuchungen über Geschlechtsbestimmung und Geschlechtsumwandlung bei Ophryotrocha puerilis. Zool. Jahrb. Physiol. 56: 389–439.

    Google Scholar 

  • Hauenschild, C., 1951. Nachweis der sog. atoken Geschlechtsform des Polychaeten Platynereis dumerilii als eigene Art auf Grund von Zuchtversuchen. Zool. Jahrb. Physiol. 63: 107–127.

    Google Scholar 

  • Hauenschild, C., 1953. Die phänotypische Geschlechtsbestimmung bei Grubea clavata (Annel. Polych.) und vergleichende Beobachtungen an anderen Sylliden. Zool. Jahrb. Physiol. 64:15–52.

    Google Scholar 

  • Hauenschild, C., 1956. Hormonale Hemmung der Geschlechtsreife und Metamorphose bei dem Polychaeten Platynereis dumerilii. Z. Naturforsch. 11b: 125–132.

    Google Scholar 

  • Hauenschild, C., 1966. Der hormonale Einfluß des Gehirns auf die sexuelle Entwicklung bei dem Polychaeten Platynereis dumerilii. Gen. Comp. Endocrinol. 6: 26–73.

    Google Scholar 

  • Hauenschild, C. & A. Fischer, 1969. Platynereis dumerilii. Grosses Zoologisches Praktikum, Heft 10b. Gustav Fischer Verlag, Stuttgart.55 pp.

  • Hauenschild, C., A. Fischer & D. K. Hofmann, 1968. Untersuchungen am pazifischen Palolowurm Eunice viridis (Polychaeta) in Samoa. Helgoländer wiss. Meeresunters. 18: 254–295.

    Google Scholar 

  • Hauenschild, A. & C. Hauenschild, 1951. Untersuchungen über die stoffliche Koordination der Paarung des Polychäten Grubea clavata. Zool. Jahrb. Physiol. 62: 429–440.

    Google Scholar 

  • Heacox, A. E., A. Fischer & H. R. Frangenberg, 1983. Development of a medium for in vitro culture of oocytes from the polychaete Nereis virens. In Vitro 19: 825–832.

    Google Scholar 

  • Heil, P., 1995. Die Bereitstellung von Vitellogenin durch die Elaeocyten im Wachstumsverlauf der Oocyten durch Nereis virens. Thesis, Univ. of Mainz

  • Heimann, C. & A. W. C. Dorresteijn, 1999. Molecular control of cleavage cycles in the embryos of Platynereis dumerilii (Annelida: Polychaeta). II. m-RNA-sequence for a Wee1-like kinase (Abstr.). Zoology 102 Suppl. (DZG 92.1):22.

    Google Scholar 

  • Hempelmann, F., 1911. Zur Naturgeschichte von Nereis dumerilii. Zoologica 62: 1–132.

    Google Scholar 

  • Herpin, R., 1926. Recherches biologiques sur la reproduction et le développement de quelques Annélides Polychètes. Bull. Soc. Sci. Nat. l'Ouest Fr. Sér. 4, 5: 1–250.

    Google Scholar 

  • *Hoagland, K. E. & R. Robertson 1988. An assessment of poecilogony in marine invertebrates: Phenomenon or fantasy? Biol. Bull. 174: 109–125.

    Google Scholar 

  • Hoeger, U., C. Märker & G. Geier, 1996. Adenylate storage, metabolism and utilization in coelomic cells of the polychaete Nereis virens (Annelida, Polychaeta). Experientia 52: 481–486.

    Google Scholar 

  • Hoeger, U., N. Rebscher & G. Geier, 1999. Metabolite supply in oocytes of Nereis virens: role of nucleosides. Hydrobiologia 402 (Dev. Hydrobiol. 142): 163–174.

    Google Scholar 

  • Hofmann, D. K., 1966. Untersuchungen zur Regeneration des Hinterendes bei Platynereis dumerilii (Audouin et Milne-Edwards) (Annelida Polychaeta). Zool. Jb. Physiol. 72: 374–430.

    Google Scholar 

  • Hofmann, D. K. & I. Schiedges, 1984. Brain hormone levels and feedback regulation during gametogenesis, metamorphosis and regeneration in Platynereis dumerilii – An experimental approach. Fortschr. Zool. 29: 73–79.

    Google Scholar 

  • *Irvine, S. M. & M. Q. Martindale, 1996. Cellular and molecular mechanisms of segmentation in annelids. Semin. Dev. Biol. 7:593–604.

    Google Scholar 

  • Irvine, S. M., S. A. Warinner, J. D. Hunter & M. Q. Martindale,1997. A survey of homeobox genes in Chaetopterus variopedatus and analysis of polychaete homeodomains. Mol. Phyl. Evol. 7: 331–345.

    Google Scholar 

  • Ishimoto, K., K. Maekawa & N. Sawada, 1968. Jelly substance extruded from eggs of Nereis japonica Izuka. Ehime Daigaku, Matsuyama, Japan. Mem. Sec. 6. Agriculture 13: 1–13.

    Google Scholar 

  • *Jamieson, B. G. M., 1992. Oligochaeta. In Harrison, F. W. & S. L. Gardiner (eds), Microscopic Anatomy of Intertebrates. Vol. 7. Wiley-Liss Inc., New York: 272–322.

    Google Scholar 

  • Kluge, B., M. Lehmann-Greif & A. Fischer, 1995. Long-lasting exocytosis and massive structural reorganization in the egg periphery during cortical reaction in Platynereis dumerilii (Annelida: Polychaeta). Zygote 3: 141–156.

    Google Scholar 

  • Korschelt, E., 1942.Weiteres über die Dauer der ungeschlechtlichen Fortpflanzung der Ctenodrilus monostylus. Zool. Anz. 137: 162–166.

    Google Scholar 

  • *Levin, L. A. & T. S. Bridges,1994. Control and consequences of alternative developmental modes in a poecilogonous polychaete. Am. Zool. 34: 323–332.

    Google Scholar 

  • Levin, L. A., J. Zhu & E. Creed, 1991. The genetic basis of lifehistory characters in a polychaete exhibiting planktotrophy and lecithotrophy. Evolution 45: 380–397.

    Google Scholar 

  • Lillie, F. R., 1906. Observations and experiments concerning the elementary phenomena of embryonic development in Chaetopterus. J. exp. Zool. 3: 153–268.

    Google Scholar 

  • Lillie, F. R., 1911. Studies on fertilization in Nereis. I. The cortical changes in the egg. II. Partial fertilization. J. Morph. 22: 361–393.

    Google Scholar 

  • Lillie, F. R. & E. Just, 1913. Breeding habits of the heteronereis form of Nereis limbata. Biol. Bull. 24: 147–168.

    Google Scholar 

  • Malaquin, A., 1893. Recherches sur les Syllidiens Morphologie, Anatomie, Reproduction, Développement. Mém. Soc. Sci. Arts. Lille, Sér. 4, 18: 1–477.

    Google Scholar 

  • Malmgren, A. J., 1867. Annulata Polychaeta Spetsbergiae, Groenlandiae, Islandiae et Scandinaviae hactenus cognita. Oefv. K. Vetensk. Akad. Stockholm Forh. 24: 127–235.

    Google Scholar 

  • Markert, R. E., B. J. Markert & N. J. Vertrees, 1961. Lunar periodicity in spawning and luminescence in Odontosyllis enopla. Ecology 42: 414–415.

    Google Scholar 

  • Morgan, T. H., 1910. The effects of altering the position of the cleavage planes in eggs with precocious specification. Arch. Entwicklungsmech. Organ. 29: 205–224.

    Google Scholar 

  • Okada, Y. K., 1937. La stolonisation et les caractères sexuels du stolon chez les Syllidiens Polychètes (Études sur les Syllidiens III). Japan. J. Zool. 7: 441–490.

    Google Scholar 

  • *Olive, P. J.W. & R. B. Clark, 1978. Physiology of reproduction. In Mill, P. J. (ed.), Physiology of Annelids. 271–368.

  • Peaucellier, G., P. Guerrier & J. Bergerard, 1974. Effects of cytochalasin B on meiosis and development of fertilized and activated eggs of Sabellaria alveolata L. (Polychaete Annelid). J. Embryol. exp. Morph. 31: 61–74.

    Google Scholar 

  • Penners, A., 1922. Die Furchung von Tubifex rivulorum. Zool. Jb. Anat. 43: 323–367.

    Google Scholar 

  • Pfannenstiel, H. D., 1984a. The ventral nerve cord signals positional information during segment formation in an annelid (Ophryotrocha puerilis, Polychaeta). Roux's Arch. Dev. Biol.194: 32–36.

    Google Scholar 

  • *Pfannenstiel, H. D., 1984b. Sex-determination and intersexuality in polychaetes. Fortschr. Zool. 29: 81–98.

    Google Scholar 

  • *Porchet, M., 1984. Biochemistry of oocyte differentiation in nereidids. Fortschr. Zool. 29: 207–225.

    Google Scholar 

  • Premoli, M. C. & G. Sella, 1995. Sex economy in benthic polychaetes. Ethol. Ecol. Evol. 7: 27–48.

    Google Scholar 

  • Render, J. A., 1983. The second polar lobe of the Sabellaria cementarium embryo plays an inhibitory role in apical tuft formation. Roux's Arch. Dev. Biol. 192: 120–129.

    Google Scholar 

  • *Reverberi, G., 1971. Annelids. In Reverberi, G. (ed.), Experimental Embryology of Marine and Fresh-Water Invertebrates. North-Holland Publ. Co: 126–163.

  • *Rice, S. A., 1992. Spermatogenesis and spermiogenesis. In Harrison, F. W. & S. L. Gardiner (eds), Microscopic Anatomy of Invertebrates. Vol. 7, chapt. 2 (Polychaeta) Wiley-Liss Inc. New York: 129–151.

    Google Scholar 

  • Sato, M., 1999. Divergence of reproductive and developmental characteristics in Hediste (Polychaeta: Nereididae). Hydrobiologia402 (Dev. Hydrobiol. 142): 131–143.

    Google Scholar 

  • Sato, M. & M. Ikeda, 1992. Chromosomal complements of two forms of Neanthes japonica (Polychaeta, Nereididae) with evidence of male-heterogametic sex chromosomes. Mar. Biol. 112:299–307.

    Google Scholar 

  • Sato, M. & M. Tsuchiya, 1987. Reproductive behavior and salinity favorable for early development in two types of the brackishwater polychaete Neanthes japonica (Izuka). Bull. jap. Assoc. Benthology 31: 29–42.

    Google Scholar 

  • Sato, M. & M. Tsuchiya, 1991. Two patterns of early development in nereidid polychaetes keying out to Neanthes japonica (Izuka). Ophelia Suppl. 5: 371–382.

    Google Scholar 

  • Schiedges, K. L., 1979. Reproductive biology and ontogenesis in the polychaete genus Autolytus (Annelida: Syllidae): Observations on laboratory-cultured individuals. Mar. Biol. 54: 239–250.

    Google Scholar 

  • Schierwater, B. & C. Hauenschild, 1990. A photoperiod determined life-cycle in an oligochaete worm. Biol. Bull. 178: 111–117.

    Google Scholar 

  • Schleip, W., 1914. Die Furchung des Eies der Rüsselegel. Zool. Jb. Anat. 37: 313–368.

    Google Scholar 

  • Schneider, S., A. Fischer & A. W. C. Dorresteijn, 1992. A morphometric comparison of dissimilar early development in sibling species of Platynereis (Annelida, Polychaeta). Roux's Arch. Dev. Biol. 201: 243–256.

    Google Scholar 

  • Schöttler, U., 1989. Changes in the intermediary metabolism after transition from the atokous to the epitokous stage. Investigations on Nereis virens. Verh. dt. zool. Ges. 82:306–307.

    Google Scholar 

  • Schroeder, P. C., 1967. Morphogenesis of epitokous setae during normal and induced metamorphosis in the polychaete annelid Nereis grubei (Kinberg). Biol. Bull. 133: 426–437.

    Google Scholar 

  • *Schroeder, P. C., 1987. Endogenous control of gametogenesis. In Giese, A. C. & J. S. Pearse (eds), Reproduction of Marine Invertebrates. Vol 9, Blackwell Sci Publ, Palo Alto, Calif. and The Boxwood Press, Pacific Grove, Calif.: 179–248.

    Google Scholar 

  • *Schroeder, P. C. & C. O. Hermans, 1975. Annelida: Polychaeta. In Giese, A. C. & J. S. Pearse (eds), Reproduction of Marine Invertebrates. Vol 3, Academic Press: 1–213.

  • Schulz, G., K. P. Ulbrich, C. Hauenschild & H. D. Pfannenstiel,1989. The atokous-epitokous border is determined before the onset of heteronereidid development in Platynereis dumerilii (Annelida: Polychaeta). Roux's Arch. Dev. Biol. 198: 29–33.

    Google Scholar 

  • Shimizu, T., 1982a. Ooplasmic segregation in the Tubifex egg: Mode of pole plasm accumulation and possible involvement of microfilaments. Roux's Arch. Dev. Biol. 191: 246–256.

    Google Scholar 

  • *Shimizu, T., 1982b. Development in the freshwater oligochaete Tubifex. In Harison, F.W. & R. R. Cowden (eds), Developmental Biology of Freshwater Invertebrates. A. R. Liss, Inc., New York:283–316.

    Google Scholar 

  • Spek, J., 1930. Zustandsänderungen der Plasmakolloide bei Befruchtung und Entwicklung des Nereis Eies. Protoplasma 9:370–427.

    Google Scholar 

  • Symes, K. & D. A. Weisblat, 1992. An investigation of the specification of unequal cleavages in leech embryos. Dev. Biol. 150:203–218.

    Google Scholar 

  • *van den Biggelaar, J. A. M. & G. Haszprunar, 1996. Cleavage patterns and mesentoblast formation in the Gastropoda: an evolutionary perspective. Evolution 50: 1520–1540.

    Google Scholar 

  • Weinberg, J. R., V. R. Starczak, C. Mueller, G. C. Pesch & S. M. Lindsay, 1990. Divergence between populations of a monogamous polychaete with male parental care: premating isolation and chromosome variation. Mar. Biol. 107: 205–213.

    Google Scholar 

  • Weisblat, D. A. & M. Shankland, 1985. Cell lineage and segmentation in the leech. Phil. Trans. r. Soc. Lond. B 312: 39–56.

    Google Scholar 

  • Westheide, W., 1980. Erpobdella octoculata (Hirudinea) – Spermatophorenübertragung, Kokonablage, Schlüpfen der Jungtiere. Film E 2562. Inst. f. d. wiss. Film, Box 2351, D-37013 Göttingen

  • *Westheide, W., 1984. The concept of reproduction in polychaetes with small body size: adaptations in interstitial species. Fortschr. Zool. 29: 265–287.

    Google Scholar 

  • *Westheide, W., 1988. Genital organs. In W. Westheide, W. & C.O. Hermans (eds), The Ultrastructure of Polychaeta. Microfauna Mar. 4: 263–279.

  • Westheide, W., G. Purschke & W. Mangerich, 1994. Sinohesione genitaliphora gen.et.sp.n. (Polychaeta, Hesionidae), an interstitial annelid with unique dimorphous external genital organs. Zool. Scr. 23: 95–105.

    Google Scholar 

  • Whitman, C. O., 1878. The embryology of Clepsine. Q. J. micr. Sci.18: 215–315.

    Google Scholar 

  • Wilson, E. B., 1892. The cell lineage of Nereis. A contribution to the cytogeny of the annelid body. J. Morph. 6: 361–480.

    Google Scholar 

  • Wissocq, J. C., 1963–1964. Nouveaux cas d'inversion sexuelle chez les Syllidiens (Annélides, Polychètes). Mém. Soc. Sci. Nat. Math. Cherbourg 51, 6. Sér., 1: 105–109.

    Google Scholar 

  • Wissocq, J. C., 1970. Évolution de la musculature longitudinale dorsale et ventrale au cours de la stolonisation de Syllis amica Quatr. (Annélide Polychète). II La dédifferentiation. J. Microscopie 9:1049–1074.

    Google Scholar 

  • Wissocq, J. C., 1977. —Évolution de la musculature des Néréidiens (Annélides polychètes) au cours de l'épitoquie. Wilhelm Roux's Arch. 182: 227–253.

    Google Scholar 

  • Zeeck, E., J. 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., T. Harder & M. Beckmann, 1998. Uric acid: The sperm release pheromone of the marine polychaete Platynereis dumerilii. J. chem. Ecol. 24: 13–22.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fischer, A. Reproductive and developmental phenomena in annelids: a source of exemplary research problems. Hydrobiologia 402, 1–20 (1999). https://doi.org/10.1023/A:1003719906378

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1003719906378

Navigation