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The gametogenic cycle and life history of Nicolea uspiana (Polychaeta: Terebellidae) on the south-east coast of Brazil

Published online by Cambridge University Press:  11 March 2014

André Rinaldo Senna Garraffoni*
Affiliation:
Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, Caixa Postal 6109, 13083-970, Campinas, São Paulo, Brazil
Leonardo Querobim Yokoyama
Affiliation:
Departamento de Oceanografia Biológica, Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191, Cidade Universitária, 05508-900, São Paulo, São Paulo, Brazil
Antonia Cecília Zacagnini Amaral
Affiliation:
Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, Caixa Postal 6109, 13083-970, Campinas, São Paulo, Brazil
*
Correspondence should be addressed to: A.R.S. Garraffoni, Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, Caixa Postal 6109 13083-970, Campinas, São Paulo, Brazil (Present address: Departamento de Ciências Biológicas, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Campus II, Rodovia BR-367, 39100-000 Diamantina, Minas Gerais, Brazil) email: garraffoni@gmail.com

Abstract

The gametogenic cycle and life history of Nicolea uspiana (Nogueira, 2003) (Polychaeta: Terebellidae) was studied by taking monthly samples over a 13 month period. Each month, 10 females were sorted; 50 oocytes were removed from the coelom of each specimen, and the maximum diameter was determined. Additionally, 10 males were sorted and 100 gametes were randomly selected from each specimen to evaluate their shape and maturation stage. This species is gonochoric and exhibits slight external sexual dimorphism (in the shape of the nephridial papillae). The sex-ratio of N. uspiana was 2.4 male for each female. The initial gametic stages of both sexes are produced in special structures called nephromixia. Oogenesis is extra-ovarian, and the germ cells are clumped and surrounded by follicle cells. These cells are ovulated into the coelomic fluid, and yolk synthesis occurs in this cavity. The maximum diameter of oocytes measured, 225 µm, showed that these eggs fall into the size-range for lecithotrophy. Furthermore, N. uspiana is an iteroparous species, as the mature individuals can breed several times during their lifetime. Male gonads release germ cells early in development, and sperm maturation also occurs in the coelomic fluid. The male gametes consist of flattened plaques of germ cells attached on their anterior part by a cytophore assuming a rosette-like appearance. Following maturation of the male cells, the spermatids produce arrays of stiffly vibratile tails, assuming a morula shape. The reproductive patterns and life history of the terebellids are also discussed.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Allen, J.D. and Pernet, B. (2007) Intermediate modes of larval development: bridging the gap between planktotrophy and lecithotrophy. Evolution & Development 9, 643653.Google Scholar
Benham, W.B. (1927) External sexual differences in the terebellid worms. Proceedings of Zoological Society of London 1, 141148.CrossRefGoogle Scholar
Bhaud, M. (1988a) Change in setal pattern during early development of Eupolymnia nebolusa (Polychaeta: Terebellidae) grown in simulated natural conditions. Journal of the Marine Biological Assossiation of United Kingdom 68, 677687.CrossRefGoogle Scholar
Bhaud, M. (1988b) The two planktonic larval periods of Lanice conchilega (Pallas, 1766) Annelida Polychaeta, a peculiar example of the irreversibility of evolution. Ophelia 29, 141152.Google Scholar
Bhaud, M. (1991) Larval release from the egg mass and settlement of Eupolymniu nebulosa (Polychaeta, Terebellidae). Bulletin of Marine Science 48, 420431.Google Scholar
Bhaud, M. and Grémare, A. (1988) Larval development of the terebellid polychaete Eupolymnia nebulosa (Montagu) in the Mediterranean Sea. Zoologica Scripta 17, 347356.Google Scholar
Blake, J.A. (1991) Larval development of Polychaeta from the Northern California coast V. Ramex californiensis Hartman (Polychaeta: Terebellidae). Bulletin of Marine Science 48, 448460.Google Scholar
Blake, E.A. and Van Dover, C.L. (2005) The reproductive biology of Amathys lutzi, an ampharetid polychaete from hydrothermal vents on the Mid-Atlantic Ridge. Invertebrate Biology 124, 254264.Google Scholar
Blankensteyn, A. and Moreno, T.R. (1999) Nova ocorrência de Nicolea venustula (Montagu) (Polychaeta, Terebellidae) na costa sul do Brasil. Revista Brasileira de Zoologia 16, 319320.Google Scholar
Christie, G. (1986) Observations on the reproductive biology of Trichobranchus glacialis Malmgren, 1866 (Polychaeta: Trichobranchidae). Sarsia 71, 259263.Google Scholar
Duchêne, J.C. (1979) Premiéres donnèes sur la reproduction et la croissance de la polychète Thelepus setosus (Terebellidae) en province subantarctique. Annales de l'Institut Océanographique 55, 145154.Google Scholar
Duchêne, J.C. (1980) Premiéres donnèes sur la reproduction at la croissance de la polychète Neoleprea streptochaeta (Terebellidae) em province subantarctique. Annales de l'Institut Océanographique 56, 109115.Google Scholar
Duchêne, J.C. (1991) Growth rate, fecundity and spawning in two subantarctic populations of Thelepus setosus (Quatrefages) (Polychaeta: Terebellidae). Ophelia 5, 313320.Google Scholar
Eckelharger, K.J. (1974) Population biology and larval development of the terebellid polychaete Nicoleu zostericola. Marine Biology 27, 101113.Google Scholar
Eckelharger, K.J. (1975) A light and electron microscope investigation of gametogenesis in Nicolea zostericola (Polychaeta: Terebellidae). Marine Biology 30, 353370.Google Scholar
Eckelbarger, K.J. (1976) Origin and development of the amoebocytes of Nicolea zostericola (Polychaeta: Terebellidae) with a discussion of their possible role in oogenesis. Marine Biology 36, 169182.Google Scholar
Fauchald, K. (1983) Life diagram patterns in benthic polychaetes. Proceedings of the Biological Society of Washington 96, 160177.Google Scholar
Franzén, Å. (1956) On spermiogenesis, morphology of the spermatozoon and biology of fertilization among invertebrates. Zoologiska Bidrag från Uppsala 31, 355482.Google Scholar
Garraffoni, A.R.S. and Amaral, A.C.Z. (2009) Postlarval development of Nicolea uspiana (Polychaeta: Terebellidae). Zoologia 26, 6166.Google Scholar
Garraffoni, A.R.S. and Lana, P.C. (2008) Phylogenetic relationships within Terebellidae (Polychaeta: Terebelomorpha) based on morphological characters. Invertebrate Systematics 22, 605626.Google Scholar
Garraffoni, A.R.S., Nihei, S.S. and Lana, P.C. (2006) Distribution patterns of Terebellidae (Annelida: Polychaeta): an application of Parsimony Analysis of Endemicity (PAE). Scientia Marina 70S3, 269276.Google Scholar
Garraffoni, A.R.S., Yokoyama, L.Q. and Amaral, A.C.Z. (2010) Allometry and population structure of Nicolea uspiana (Polychaeta: Terebellidae). Journal of the Marine Biological Association of the United Kingdom 90, 877883.Google Scholar
Giangrande, A. (1997) Polychaeta reproductive patterns, life cycles and life histories: an overview. Oceanography and Marine Biology: an Annual Review 35, 323386.Google Scholar
Giangrande, A.G., Belmonte, G. and Geraci, S. (1994) Life cycle and life history traits diversity in marine invertebrates and implications in community dynamics. Oceanography and Marine Biology: an Annual Review 32, 305333.Google Scholar
Heimler, W. (1981) Untersuchungen zur Larvalentwicklung von Lanice conchilega (Pallas) 1766 (Polychaeta, Terebellomorpha). Teil II: Bau und Ultrastruktur der Trochophora-Larve. Zoologische Jahrbücher Anatomie und Ontogenie der Tiere 106, 236277.Google Scholar
Hutchings, P. (2000) Family Trichobranchidae. In Beesley, P.L., Ross, G.L.B. and Glasby, C. J. (eds) Polychaeta & allies: the southern synthesis. Fauna of Australia. Volume 4a Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula. Melbourne: CSIRO, pp. 232235.Google Scholar
Hutchings, P.A. and Glasby, C.J. (1988) The Amphitritinae (Polychaeta: Terebellidae) from Australia. Records of the Australian Museum 40, 160.Google Scholar
Jamieson, B.G.M. and Rouse, G.W. (1989) The spermatozoa of the Polychaeta (Annelida): an ultrastructural review. Biological Reviews 64, 93157.Google Scholar
Jeffery, C.H. and Emlet, R.B. (2003) Macroevolutionary consequences of developmental mode in temnopleurid echinoids from the Tertiary of Southern Australia. Evolution 57, 10311048.Google Scholar
Marcano, G. and Bhaud, M. (1995) New observations on the terebellid (Polychaeta) aulophore larvae on the French coast. Ophelia 43, 229244.Google Scholar
Marshall, D.J. and Keough, M.J. (2007) The evolutionary ecology of offspring size in marine invertebrates. Advances in Marine Biology 53, 160.Google Scholar
McHugh, D. (1993) A comparative study of reproduction and development in the Polychaeta family Terebellidae. Biological Bulletin. Marine Biological Laboratory, Woods Hole 185, 153167.Google Scholar
McHugh, D. (1995) Phylogenetic analysis of the Amphitritinae (Polychaeta: Terebellidae). Zoological Journal of the Linnean Society 114, 405429.Google Scholar
McHugh, D. and Fong, P.P. (2002) Do life history traits account for diversity of polychaete annelids? Invertebrate Biology 121, 325338.Google Scholar
McHugh, D. and Rouse, G.W. (1998) Life history evolution of marine invertebrates: new views from phylogenetic systematics. Trends in Ecology and Evolution 13, 182186.Google Scholar
Moran, A.L. And McAlister, J.S. (2009) Egg size as a life history character of marine invertebrates: is it all it's cracked up to be? Biollogical Bulletin. Marine Biological Laboratory, Woods Hole 216, 226242.Google Scholar
Nogueira, J.M.M. (2003) A new species of Paraeupolymnia Young and Kritzler, 1986 (Polychaeta, Terebellidae, Terebellinae) from Brazil. Scientia Marina 67, 407413.Google Scholar
Nogueira, J.M.M., Hutchings, P.A. and Fukuda, M.V. (2010) Morphology of terebelliform polychaetes (Annelida: Polychaeta: Terebelliformia), with a focus on Terebellidae. Zootaxa 2460, 1185.CrossRefGoogle Scholar
Nylin, S. and Gotthar, K. (1998) Plasticity in life-history traits. Annual Revision of Entomology 43, 6383.Google Scholar
Qian, P.Y. and Dahms, H.U. (2006) Larval ecology of the Annelida. In Rouse, G.W. and Pleijel, F. (eds) Reproductive biology and phylogeny of Annelida. Enfield, NH: Science Publishers, pp. 179232.Google Scholar
Ramirez-Llodra, E.R. (2002) Fecundity and life-history strategies in marine invertebrates. Advances in Marine Biology 43, 87170.Google Scholar
Rouse, G.W. (2001) Family Terebellidae. In Rouse, G.W. and Pleijel, F. (eds) Polychaetes. Oxford: Oxford University Press, pp. 246250.Google Scholar
Rouse, G.W. (2005) Annelid sperm and fertilization biology. Hydrobiologia 535/536, 167178Google Scholar
Rouse, G.W. and Fauchald, K. (1997) Cladistics and polychaetes. Zoologica Scripta 26, 269301.CrossRefGoogle Scholar
Rouse, G.W. and Fitzhugh, J.K. (1994) Broadcasting fables: is external fertilization really primitive? Sex, size, and larvae in sabellid polychaetes. Zoologica Scripta 23, 271312.Google Scholar
Rouse, G.W. and Jamieson, B.G.M. (1987) An ultrastructural study of the spermatozoa of the polychaetes Eurythoe complantata (Amphinomidae), Clymenella sp. and Micromaldane sp. (Maldanidae), with definition of sperm types in relation to reproductive biology. Journal of Submicroscopic Cytology 19, 573584.Google Scholar
Rouse, G.W. and McHugh, D. (1994) Ultrastructure of spermatids and spermatozoa in Ramex californiensis and Nicolea zostericola (Terebellidae; Polycheata). Ophelia 39, 225238.Google Scholar
Santos, A.S., Nogueira, J.M.M., Fukuda, M.V. And Christoffersen, M.L. (2010) New terebellids (Polychaeta: Terebellidae) from northeastern Brazil. Zootaxa 2389, 146.Google Scholar
Schroeder, P.C. and Hermans, C.O. (1975) Annellida: Polychaeta. In Giese, A.C. and Pearse, J.R. (eds) Reproduction of marine invertebrate, Volume 3. New York: Academic Press, pp 1123.Google Scholar
Scott, J.W. (1909) Some egg-laying habits of Amphitrite ornata Verrill. Biological Bulletin. Marine Biological Laboratory, Woods Hole 17, 327340.Google Scholar
Scott, J.W. (1910) Further experiments on the methods of egg-laying in Amphitrite. Biological Bulletin. Marine Biological Laboratory, Woods Hole 20, 252265.Google Scholar
Seitz, R.D. and Schaffner, L.C. (1995) Population ecology and secondary production of the polychaete Loimia medusa (Terebellidae). Marine Biology 121, 701711.CrossRefGoogle Scholar
Smith, R.I. (1989a) Observations on spawning behavior of Eupolymnia nebulosa, and comparisons with Lanice conchilega (Annelida, Polychaeta, Terebellidae). Bulletin of Marine Science 45, 406414.Google Scholar
Smith, R.I. (1989b) Notes on gamete production in Lanice conchilega (Annelida, Polychaeta, Terebellidae). Invertebrate Reproduction and Development 15, 712.Google Scholar
Smith, R.I. (1992) Three nephromixial patterns in Polychaeta species currently assigned to the genus Pista (Annelida, Terebellidae). Journal of Morphology 213, 365393.Google Scholar
Smith, R.I. (1994) A systematic problem of inter- and intra-generic variation in nephromixia of Terebellidae. Memoires du Muséum Naturelle d'Histoire 162, 287289.Google Scholar
Strathmann, R.R. (1985) Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Annual Reviews in Ecology and Systematics 16, 339361.Google Scholar
Strathmann, R.R. (1993) Hypotheses on the origins of marine larvae. Annual Reviews in Ecology and Systematics 24, 89117.Google Scholar
Thorson, G. (1946) Reproduction and larval development of Danish marine bottom invertebrates, with special reference to the planktonic larvae in the Sound (Oresund). Meddelelser fra Kommissionen forDanmarks Fiskeri- Og Havundersøgelser, Serie: Plankton 4, 1523.Google Scholar
Thorson, G. (1950) Reproductive and larval ecology of marine invertebrates. Biological Review 25, 145.Google Scholar
Wilson, D.P. (1928) Post-larval development of Loimia medusa Sav. Journal of the Marine Biological Assossiation of United Kingdom 15, 129149.Google Scholar
Wilson, W.H. (1991) Sexual reproductive modes in polychaetes: classification and diversity. Bulletin of Marine Science 48, 500516.Google Scholar
Wray, G.A. and Raff, R.A. (1991) Rapid evolution of gastrulation mechanisms in a sea urchin with lecithotrophic larvae. Evolution 45, 17411750.Google Scholar
Zhadan, A.E. and Tzetlin, B. (2002) Comparative morphology of the feeding apparatus in the Terebellida (Annelida: Polychaeta). Cahiers de Biologie Marine 43, 149164.Google Scholar
Willemoës-Suhm, R. von (1871) Biologische Beobachtungen über niedere Meeresthiere. Zeitschrift für wissenschaftliche Zoologie 21, 380396.Google Scholar