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Reproductive biology of Sabellaria wilsoni (Sabellariidae: Polychaeta), an important ecosystem engineer on the Amazon coast

Published online by Cambridge University Press:  23 December 2016

D. Aviz ,
A.J.A. Pinto ,
M.A.P. Ferreira ,
R.M. Rocha  and
J.S. Rosa Filho
D. Aviz*
Affiliation:
Laboratório de Oceanografia Biológica, Instituto de Geociência, Universidade Federal do Pará, Av. Augusto Corrêa s/n, Guamá, Belém, PA. CEP: 66075-110, Brazil
A.J.A. Pinto
Affiliation:
Laboratório de Oceanografia Biológica, Instituto de Geociência, Universidade Federal do Pará, Av. Augusto Corrêa s/n, Guamá, Belém, PA. CEP: 66075-110, Brazil
M.A.P. Ferreira
Affiliation:
Laboratório de Imunohistoquímica e Biologia do Desenvolvimento, Instituto de Ciências Biológicas, Universidade Federal do Pará, Rua Augusto Corrêa s/n, Guamá, Belém, PA. CEP: 66075-110, Brazil
R.M. Rocha
Affiliation:
Laboratório de Imunohistoquímica e Biologia do Desenvolvimento, Instituto de Ciências Biológicas, Universidade Federal do Pará, Rua Augusto Corrêa s/n, Guamá, Belém, PA. CEP: 66075-110, Brazil
J.S. Rosa Filho
Affiliation:
Laboratório de Bentos, Departamento de Oceanografia, Centro de Tecnologia, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, s/n. Cidade Universitária, Recife, PE. CEP: 50670-901, Brazil
*
Correspondence should be addressed to: D. Aviz, Laboratório de Oceanografia Biológica, Instituto de Geociência, Universidade Federal do Pará. Av. Augusto Corrêa s/n, Guamá, Belém, PA. CEP: 66075-110, Brazil. Email: daiane.aviz@gmail.com
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Abstract

The sabellariid worms are important ecosystem engineers in coastal zones, due to their ability to construct sand reefs, modify environments and structure biological communities. This article describes the reproductive biology of Sabellaria wilsoni on a beach of the Amazon coast. Each month between May 2008 and April 2009, specimens were collected for morphometric and histological analyses for sexing and determination of gonadal maturity. In females, the number and diameter of the oocytes at different stages of vitellogenesis were also recorded. The results showed that the species is dioecious, with sexual reproduction, females larger than males, and a female-biased sex ratio (overall, 1.6♀: 1♂). Four distinct stages of gonadal maturation were identified in the males and females – (i) initial development, (ii) maturing, (iii) mature and (iv) spawning. Sexual maturity is attained rapidly, and reproduction is continuous, with two breeding peaks, one in the dry season, related to the increased intensity of hydrodynamic conditions and reef erosion; and the other in the rainy season, when the availability of space and nutrients increases. The reproductive strategy of the species reinforces the classification of the sabellariids as r-strategists, adapted to colonize habitats with unstable environmental conditions.

Keywords

Reproductionbiogenic reef-forming wormsabellariidsAmazon beachBrazil
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 4 , June 2018 , pp. 743 - 754
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Ataide, M.B., Venekey, V., Filho, J.S.R. and dos Santos, P.J.P. (2014) Sandy reefs of Sabellaria wilsoni (Polychaeta: Sabellariidae) as ecosystem engineers for meiofauna in the Amazon coastal region, Brazil. Marine Biodiversity 44, 403–413.Google Scholar
Barry, J.P. (1989) Reproductive response of a marine annelid to winter storms – an analog to fire adaptation in plants. Marine Ecology Progress Series 54, 99–107.CrossRefGoogle Scholar
Berglund, A. (1986) Sex change by a polychaete: effects of social and reproductive costs. Ecology 67, 837–845.CrossRefGoogle Scholar
Bhaud, M. (1972) Quelques données sur le déterminisme ecologique de la reproduction des annélides polychètes. Marine Biology 17, 115–136.CrossRefGoogle Scholar
Britayev, T.A. and Fauchald, K. (2005) New species of symbiotic scaleworms Asterophilia (Polychaeta, Polynoidae) from Vietnam. Invertebrate Zoology 2, 20–28.Google Scholar
Britayev, T.A. and Zamishliak, E.A. (1996) Association of the commensal scaleworm Gastrolepidia clavigera (Polychaeta: Polynoidae) with holothurians near the coast of SouthVietnam. Ophelia 45, 175–190.Google Scholar
Capa, M., Hutchings, P. and Peart, R. (2012) Systematic revision of Sabellariidae (Polychaeta) and their relationships with other polychaetes using morphological and DNA sequence data. Zoological Journal of the Linnean Society 164, 245–284.Google Scholar
Charnov, E.L. and Bull, J.J. (1989) The primary sex ratio under environmental sex determination. Journal of Theoretical Biology 139, 431–436.CrossRefGoogle ScholarPubMed
Cotter, E., O'Riordan, R.M. and Myers, A.A. (2003) A histological study of reproduction in the serpulids Pomatoceros triqueter and Pomatoceros lamarckii (Annelida: Polychaeta). Marine Biology 142, 905–914.Google Scholar
Culloty, S.C., Favier, E., Ni Riada, M., Ramsay, N.F. and O'Riordan, R.M. (2010) Reproduction of the biogenic reef-forming honeycomb worm Sabellaria alveolata in Ireland. Journal of the Marine Biological Association of the United Kingdom 90, 503–507.CrossRefGoogle Scholar
Curtis, L.A. (1978) Aspects of the population dynamics of the polychaete Sabellaria vulgaris Verrill, in the Delaware Bay. Estuaries 1, 73–84.Google Scholar
da Costa, V.B., de Sousa, E.B., Pinheiro, S.C.C., Pereira, L.C.C. and da Costa, R.M. (2011) Effects of a high energy coastal environment on the structure and dynamics of phytoplankton communities (Brazilian Amazon littoral). Journal of Coastal Research SI 64, 354–358.Google Scholar
Desroy, N., Dubois, S.F., Fournier, J., Ricquiers, L., Le Mao, P., Guerin, L., Gerla, D., Rougerie, M. and Legendre, A. (2011) The conservation status of Sabellaria alveolata (L.) (Polychaeta: Sabellariidae) reefs in the Bay of Mont-Saint-Michel. Aquatic Conservation – Marine and Freshwater Ecosystems 21, 462–471.CrossRefGoogle Scholar
DHN-Brasil (2008) Tábuas de maré para o fundeadouro de Salinópolis (Estado do Pará). Brasil: Diretoria de Hidrografia e Navegação.Google Scholar
Dias, A.S. and Paula, J. (2001) Associated fauna of Sabellaria alveolata colonies on the central coast of Portugal. Journal of the Marine Biological Association of the United Kingdom 81, 169–170.CrossRefGoogle Scholar
Dubois, S., Comtet, T., Retière, C. and Thiébaut, E. (2007) Distribution and retention of Sabellaria alveolata larvae (Polychaeta: Sabellariidae) in the Bay of Mont-Saint-Michel, France. Marine Ecology Progress Series 346, 243–254.Google Scholar
Eckelbarger, K.J. (1976) Larval development and population aspects of the reef-building polychaete Phragmatopoma lapidosa from the east coast of Florida. Bulletin of Marine Science 26, 117–132.Google Scholar
Eckelbarger, K.J. (1977) Larval development of Sabellaria floridensis from Florida and Phragmatopoma californica from southern California (Polychaeta: Sabellariidae), with a key to the sabellariid larvae of Florida and a review of development in the family. Bulletin of Marine Science 27, 241–255.Google Scholar
Eckelbarger, K.J. (1978a) Metamorphosis and settlement in the Sabellariidae. In Rice, M.E. and Chia, F.S. (eds) Settlement and metamorphosis of marine invertebrate larvae. Amsterdam: Elsevier B.V., pp. 145–164.Google Scholar
Eckelbarger, K.J. (1978b) Oogenesis in the polychaete Phragmatopoma lapidosa: a unique mode of yolk formation in a spiralian. American Zoologist 18, 646.Google Scholar
Eckelbarger, K.J. (1979) Ultrastructural evidence for both autosynthetic and heterosynthetic yolk formation in the oocytes of an annelid (Phragmatopoma lapidosa, Polychaeta). Tissue and Cell 11, 425–443.Google Scholar
Eckelbarger, K.J. (1984) Ultrastructure of spermatogenesis in the reef-building polychaete Phragmatopoma lapidosa (Sabellariidae) with special reference to acrosome morphogenesis. Journal of Ultrastructure Research 89, 146–164.CrossRefGoogle Scholar
Faroni-Perez, L. (2014) Variação sazonal no recrutamento de Phragmatopoma caudata (Polychaeta, Sabellariidae) na costa sudeste do Brasil: biometria e validação de metodologia para categorização de classes etárias. Iheringia, Série Zoologia 104, 5–13.Google Scholar
Faroni-Perez, L. and Zara, F.J. (2014) Oogenesis in Phragmatopoma (Polychaeta: Sabellariidae): evidence for morphological distinction among geographically remote populations. Memoirs of Museum Victoria 71, 53–65.Google Scholar
Fauré-Frémiet, E. (1924) L'oeuf de Sabellaria alveolata L. Archives d'Anatomie Microscopique 20, 211–342.Google Scholar
Giangrande, A. (1990) Distribution and reproduction of syllids (Annelida, Polychaeta) along a vertical cliff (West Mediterranean). Oebalia 16, 69–86.Google Scholar
Giangrande, A. (1997) Polychaete reproductive patterns, life cycles and life histories: an overview. Oceanography and Marine Biology: An Annual Review 35, 323–386.Google Scholar
Giese, A.C. and Kanatani, H. (1987) Maturation and spawning. In Giese, A.C., Pearse, J.S. and Pearse, V.B. (eds) Reproduction of marine invertebrates, IX. Palo Alto, CA: Blackwell Scientific Publishers, pp. 252–313.Google Scholar
Gore, R.H., Scotto, L.E. and Becker, L.J. (1978) Community composition, stability, and trophic partitioning in decapod crustaceans inhabiting some subtropical sabellariid worm reefs. Studies on decapod Crustacea from the Indian River region of Florida. IV. Bulletin of Marine Science 28, 221–248.Google Scholar
Gram, R. (1968) A Florida Sabellariidae reef and its effect on sediment distribution. Journal of Sedimentary Petrology 38, 863–868.Google Scholar
Gruet, Y. (1971) Morphologie, croissance et faune associée des récifs de Sabellaria alveolata (Linné) de la Bernerie-en-Retz (Loire Atlantique). Tethys 3, 321–380.Google Scholar
Gruet, Y. (1986) Spatio-temporal changes of sabellarian reefs built by the sedentary polychaete Sabellaria alveolata (Linné). Marine Ecology–Pubblicazioni Della Stazione Zoologica Di Napoli I 7, 303–319.Google Scholar
Gruet, Y. and Lassus, P. (1983) Contribution à l’étude de la biologie reproductive d'une population naturelle de l'annélide polychète Sabellaria alveolata (Linné). Annales de l'Institut Océanographique de Paris 59, 127–140.Google Scholar
Jollivet, D., Empis, A., Baker, M.C., Hourdez, S., Comtet, T., Jouin-Toulmond, C., Desbruyeres, D. and Tyler, P.A. (2000) Reproductive biology, sexual dimorphism, and population structure of the deep sea hydrothermal vent scale-worm, Branchiplynoee seepensis (Polychaeta: Polynoidae). Journal of the Marine Biological Association of the United Kingdom 80, 55–68.Google Scholar
Lana, P.C. and Bremec, C.S. (1994) Sabellariidae (Annelida, Polychaeta) from South America. In Dauvin, J.C., Laubier, L. and Reish, D.J. (eds) Conférence Internationale des Polychètes, Volume 162. Paris: Mémoires du Muséum National d´Histoire Naturelle, pp. 211–222.Google Scholar
Lana, P.D. and Gruet, Y. (1989) Sabellaria wilsoni sp.n. (Polychaeta, Sabellariidae) from the southeast coast of Brazil. Zoologica Scripta 18, 239–244.Google Scholar
Lomônaco, C., Santos, A.S. and Christoffersen, M.L. (2012) Effects of local hydrodynamic regime on the individual's size in intertidal Sabellaria (Annelida: Polychaeta: Sabellariidae) and associated fauna at Cabo Branco beach, north-east Brazil. Marine Biodiversity Records 4, 1–7.Google Scholar
Longhurst, A. and Pauly, D. (1987) Ecology of tropical oceans. San Diego, CA: Academic Press.Google Scholar
Martorano, L.G., Pereira, L.C., Cézar, E.G.M. and Pereira, I.C.B. (1993) Estudos climáticos do Estado do Pará: classificação climática (Köppen) e deficiência hídrica (Thornthwaite, Mather). Belém: Sudam/Embrapa/SNLCS.Google Scholar
Mauro, N.A. (1975) The premetamorphic developmental rate of Phragmatopoma lapidosa Kinberg, 1867, compared with that in temperate sabellariids (Polychaeta: Sabellariidae). Bulletin of Marine Science 25, 387–392.Google Scholar
McCarthy, D.A., Young, C.M. and Emson, R.H. (2003) Influence of wave-induced disturbance on seasonal spawning patterns in the sabellariid polychaete Phragmatonoma lapidosa. Marine Ecology Progress Series 256, 123–133.CrossRefGoogle Scholar
Moraes, B.C., Costa, J.M.N., Costa, A.C.L. and Costa, M.H. (2005) Variação espacial e temporal da precipitação no Estado do Pará. Acta Amazonica 35, 207–214.Google Scholar
Pawlik, J.R. (1988) Larval settlement and metamorphosis of two gregarious sabellariid polychaetes: Sabellaria alveolata compared with Phragmatopoma californica. Journal of the Marine Biological Association of the United Kingdom 68, 101–124.Google Scholar
Pawlik, J.R. and Butman, C.A. (1993) Settlement of a marine tube worm as a function of current velocity – interacting effects of hydrodynamics and behavior. Limnology and Oceanography 38, 1730–1740.Google Scholar
Pawlik, J.R. and Chia, F.S. (1991) Larval settlement of Sabellaria cementarium Moore, and comparisons with other species of sabellariid polychaetes. Canadian Journal of Zoology – Revue Canadienne de Zoologie 69, 765–770.Google Scholar
Peaucellier, G. (1984) Ultrastructural study of oocyte maturation in the polychaete annelid Sabellaria alveolata. International Journal of Invertebrate Reproduction and Development 7, 33–42.Google Scholar
Pereira, L.C.C., Mendes, C.M., Monteiro, M.D.C. and Asp, N.E. (2009) Morphological and sedimentological changes in a macrotidal sand beach in the Amazon Littoral (Vila Dos Pescadores, Pará, Brazil). Journal of Coastal Research SI 56, 113–117.Google Scholar
Pereira, L.C.C., Sozinho da Silva, N.I., da Costa, R.M., Asp, N.E., da Costa, K.G. and Vila-Concejo, A. (2012) Seasonal changes in oceanographic processes at an equatorial macrotidal beach in northern Brazil. Continental Shelf Research 43, 95–106.Google Scholar
Porras, R., Bataller, J.V., Murgui, E. and Torregrosa, M.T. (1996) Trophic structure and community composition of polychaetes inhabiting some Sabellaria alveolata (L) reefs along the Valencia Gulf Coast, Western Mediterranean. Marine Ecology-Pubblicazioni della Stazione Zoologica di Napoli I 17, 583–602.Google Scholar
Premoli, M.C. and Sella, G. (1995) Sex economy in benthic polychaetes. Ethology Ecology and Evolution 7, 27–48.Google Scholar
Premoli, M.C., Sella, G. and Berra, G.P. (1996) Heritable variation of sex ratio in a polychaete worm. Journal of Evolutionary Biology 9, 845–854.Google Scholar
Rosa Filho, J.S., Gomes, T.P., Almeida, M.F. and Silva, R.F. (2011) Benthic fauna of macrotidal sandy beaches along a small-scale morphodynamic gradient on the Amazon coast (Algodoal Island, Brazil). Journal of Coastal Research SI 64, 435–439.Google Scholar
Shuker, D.M., Moynihan, A.M. and Ross, L. (2009) Sexual conflict, sex allocation and the genetic system. Biology Letters 5, 682–685.Google Scholar
Silva, D.E.A. (2015) Os recifes arenosos de Sabellaria wilsoni (Polychaeta: Sabellariidae) na Ilha de Maiandeua-Algodoal, Pará: dinâmica dos construtores e da macrofauna bentônica associada. PhD thesis. Universidade Federal do Pará, Belém, Brazil.Google Scholar
Silva, N.I.S., Pereira, L.C.C., Gorayeb, A., Vila-Concejo, A., Sousa, R.C., Asp, N.E. and Costa, R.M. (2011) Natural and social conditions of Princesa, a macrotidal sandy beach on the Amazon Coast of Brazil. Journal of Coastal Research SI 64, 1979–1983.Google Scholar
Smith, P.R. and Chia, F.S. (1985) Larval development and metamorphosis of Sabellaria cementarium Moore, 1906 (Polychaeta: Sabellariidae). Canadian Journal of Zoology – Revue Canadienne de Zoologie 63, 1037–1049.Google Scholar
Sousa, W.P. (2001) Natural disturbance and the dynamics of marine benthic communities. In Bertness, M.D., Gaines, S.D. and Hay, M.E. (eds) Marine community ecology. Sunderland, MA: Sinauer Associates Inc., pp. 85–130.Google Scholar
Van Dover, C.L., Trask, J., Gross, J. and Knowlton, A. (1999) Reproductive biology of free-living and commensal polynoid polychaetes at the Lucky Strike hydrothermal vent field (Mid-Atlantic Ridge). Marine Ecology Progress Series 181, 201–214.Google Scholar
Vovelle, J. (1965) Le tube de Sabellaria alveolata (L.) – Annélide polychète Hermellidae – et son ciment. Étude écologique, expérimentale, histologique et histochimique. Archives de Zoologie Expérimentale et Générale 106, 1–187.Google Scholar
Waterman, A.J. (1934) Observations on reproduction, prematuration and fertilization in Sabellaria vulgaris. Biological Bulletin 67, 97–114.Google Scholar
Werren, J.H. and Charnov, E.L. (1978) Facultative sex rations and population dynamics. Nature 272, 349–350.Google Scholar
Werren, J.H. and Taylor, P.D. (1984) The effects of population recruitment on sex-ratio selection. American Naturalist 124, 143–148.Google Scholar
Wilson, D.P. (1968a) Settlement behaviour of larvae of Sabellaria alveolata (L.). Journal of the Marine Biological Association of the United Kingdom 48, 387–435.Google Scholar
Wilson, D.P. (1968b) Some aspects of the development of eggs and larvae of Sabellaria alveolata (L.). Journal of the Marine Biological Association of the United Kingdom 48, 367–386.Google Scholar
Wilson, D.P. (1970a) Additional observations on larval growth and settlement of Sabellaria alveolata. Journal of the Marine Biological Association of the United Kingdom 50, 1–31.Google Scholar
Wilson, D.P. (1970b) Larvae of Sabellaria spinulosa and their settlement behaviour. Journal of the Marine Biological Association of the United Kingdom 50, 33–52.CrossRefGoogle Scholar
Wilson, D.P. (1971) Sabellaria colonies at Duckpool, North Cornwall, 1961–1970. Journal of the Marine Biological Association of the United Kingdom 51, 509–580.Google Scholar
Wilson, D.P. (1974) Sabellaria alveolata (L.) at Duckpool, North Cornwall, 1971–1972, with a note for May 1973. Journal of the Marine Biological Association of the United Kingdom 54, 393–436.Google Scholar
Zajac, R.N. (1991) Population ecology of Polydora ligni (Polychaeta, Spionidae). I. Seasonal variation in population characteristics and reproductive activity. Marine Ecology Progress Series 77, 197–206.Google Scholar