Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-04T21:33:20.321Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproductive biology of the commercial sea cucumber Athyonidium chilensis (Holothuroidea: Dendrochirotida) in southern Chile

Published online by Cambridge University Press:  09 September 2016

Josefina Peters-Didier ,
Luis Miguel Pardo ,
Orlando Garrido  and
Carlos S. Gallardo
Josefina Peters-Didier*
Affiliation:
Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile
Luis Miguel Pardo
Affiliation:
Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile Centro de Investigación de Dinámica de Ecosistemas Marinos de Altas Latitudes (IDEAL), Valdivia, Chile
Orlando Garrido
Affiliation:
Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile
Carlos S. Gallardo
Affiliation:
Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile
*
Correspondence should be addressed to:J. Peters-Didier, School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Reproductive aspects of the sea cucumber Athyonidium chilensis were studied over a year in Valdivia, Chile, through gonad index (GI) analysis, macro- and microscopic analysis of the gonads, fecundity and size at first sexual maturity estimations. We also explored the reliability of live size estimators for their use in fisheries. Athyonidium chilensis showed continuous gametogenesis and spawning individuals could be found throughout the year. However, spring was the main reproductive time, where an important GI decrease coincided with enhanced spawning activity evidenced through histology. GIs recovered in summer, and new signs of enhanced spawning activity were observed towards autumn (April 2008). GI peaks were observed in August 2007 and March 2008 for females (22.8 and 24.4% respectively) and September 2007 and March 2008 for males (31.9 and 25.9% respectively). Low mean GIs occurred in May and December 2007 for females (15.2 and 11.6% respectively) and May and October 2007 for males (12.7 and 14.1% respectively). Males reached sexual maturity at a smaller size than females (males: 21.2 g, females: 43.7 g eviscerated weight), and mature females showed a high mean absolute fecundity for a species with lecithotrophic larval development (6.31 × 105 ± 1.97 × 105 SD). For fisheries, we recommend a minimum catch size over 237.89 g drained weight to ensure that caught individuals are sexually mature. This study provides relevant information for the conservation and fishery management of A. chilensis. Continuous gametogenesis and high fecundity make this species particularly suitable for aquaculture in southern Chile.

Keywords

sea cucumberChileAthyonidium chilensisbêche-de-merfisheriesaquaculturereproductive cyclefecundityholothuroid
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 2 , March 2018 , pp. 311 - 323
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

2

Present address: School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand

References

REFERENCES

Abdel-Razek, F.A., Abdel-Rahman, S.H., El-Shimy, N.A. and Omar, H.A. (2005) Reproductive biology of the tropical sea cucumber Holothuria atra (Echinodermata: Holothuroidea) in the Red Sea coast of Egypt. Egyptian Journal of Aquatic Research 31, 383–402.Google Scholar
Akamine, J. (2004) The status of the sea cucumber fisheries and trade in Japan: past and present. In Lovatelli, A., Conand, C., Purcell, S., Uthicke, S., Hamel, J.F. and Mercier, A. (eds) Advances in sea cucumber aquaculture and management. FAO Fisheries and Aquaculture Technical Paper. Volume 463. Rome: FAO, pp. 39–47.Google Scholar
Anderson, S.C., Flemming, J.M., Watson, R. and Lotze, H.K. (2011) Serial exploitation of global sea cucumber fisheries. Fish and Fisheries 12, 317–339.Google Scholar
Asha, P.S. and Muthiah, P. (2008) Reproductive biology of the commercial sea cucumber Holothuria spinifera (Echinodermata: Holothuroidea) from Tuticorin, Tamil Nadu, India. Aquaculture International 16, 231–242.Google Scholar
Bell, J.D., Leber, K.M., Blankenship, H.L., Loneragan, N.R. and Masuda, R. (2008a) A new era for restocking, stock enhancement and sea ranching of coastal fisheries resources. Reviews in Fisheries Science 16, 1–9.Google Scholar
Bell, J.D., Purcell, S.W. and Nash, W.J. (2008b) Restoring small-scale fisheries for tropical sea cucumbers. Ocean and Coastal Management 51, 589–593.Google Scholar
Buckle, F., Guisado, C., Tarifeño, E., Zuleta, A., Córdova, L. and Serrano, C. (1978) Biological studies on the Chilean sea urchin Loxechinus albus (Molina) (Echinodermata: Echinoidea). IV. Maturation cycle and seasonal changes in the gonad. Ciencias Marinas Mexico 5, 1–15.Google Scholar
Caffi, M. (1981) Aspectos del ciclo reproductivo de Athyonidium chilensis (Semper, 1868) en caleta Colchogüe, Bahía de Concepción, Chile (Echinodermata: Holothuroidea). Masters equivalent thesis. Universidad de Concepción, Concepción, Chile.Google Scholar
Catalan, M.A.B. and Yamamoto, M. (1994) Annual reproductive cycle of the Japanese holothurian Eupentacta chronhjelmi . Canadian Journal of Zoology 72, 387–396.Google Scholar
Chao, S.-M., Chen, C.-P. and Alexander, P.S. (1995) Reproductive cycles of tropical sea cucumbers (Echinodermata: Holothuroidea) in southern Taiwan. Marine Biology 122, 289–295.Google Scholar
Conand, C. (1981) Sexual cycle of three commercially important holothurian species (Echinodermata) from the lagoon of New Caledonia. Bulletin of Marine Science 31, 523–543.Google Scholar
Conand, C. (1993a) Ecology and reproductive biology of Stichopus variegatus an Indo- Pacific coral reef sea cucumber (Echinodermata: Holothuroidea). Bulletin of Marine Science 52, 970–981.Google Scholar
Conand, C. (1993b) Reproductive biology of the holothurians from the major communities for the New Caledonia lagoon. Marine Biology 116, 439–450.Google Scholar
Conand, C. (2004) Present status of world sea cucumber resources and utilization: an international overview. In Lovatelli, A., Conand, C., Purcell, S., Uthicke, S., Hamel, J.-F. and Mercier, A. (eds) Advances in sea cucumber aquaculture and management. FAO Fisheries and Aquaculture Technical Paper. Volume 463. Rome: FAO, pp. 13–24.Google Scholar
Conand, C. and Byrne, M. (1993) A review of recent developments in world sea cucumber fisheries. Marine Fisheries Review 55, 1–13.Google Scholar
Costelloe, J. (1985) The annual reproductive cycle of the holothurian Aslia lefevrei (Dendrochirota: Echinodermata). Marine Biology 88, 155–165.Google Scholar
Costelloe, J. (1988) Reproductive cycle, development and recruitment of two geographically separated populations of the dendrochirote holothurian Aslia lefevrei . Marine Biology 99, 535–545.Google Scholar
Dissanayake, D.C.T. and Stefansson, G. (2010) Reproductive biology of the commercial sea cucumber Holothuria atra (Holothuroidea: Aspidochirotida) in the northwestern coastal waters of Sri Lanka. Invertebrate Reproduction and Development 54, 65–76.Google Scholar
Eriksson, H. and Byrne, M. (2013) The sea cucumber fishery in Australia's Great Barrier Reef Marine Park follows global patterns of serial exploitation. Fish and Fisheries 16, 329–341.Google Scholar
Fajardo-León, M.C., Suárez-Higuera, M.C.L., del Valle-Manríquez, A. and Hernández-López, A. (2008) Reproductive biology of the sea cucumber Parastichopus parvimensis (Echinodermata: Holothuroidea) at Isla Natividad and Bahía Tortugas, Baja California Sur, Mexico. Ciencias Marinas 34, 165–177.Google Scholar
Fernández, M. and Castilla, J.C. (2005) Marine conservation in Chile: historical perspective, lessons, and challenges. Conservation Biology 19, 1752–1762.CrossRefGoogle Scholar
Foster, G.G. and Hodgson, A.N. (1995) Annual reproductive cycles of three sympatric species of intertidal holothurians (Echinodermata) from the coast of the Eastern Cape Province of South Africa. Invertebrate Reproduction and Development 27, 49–59.CrossRefGoogle Scholar
Gelcich, S., Godoy, N., Prado, L. and Castilla, J.C. (2008) Add-on conservation benefits of marine territorial user rights fishery policies in central Chile. Ecological Applications 18, 273–281.Google Scholar
Gelcich, S., Hughes, T.P., Olsson, P., Folke, C., Defeo, O., Fernández, M., Foale, S., Gunderson, L.H., Rodríguez-Sickert, C., Scheffer, M., Steneck, R.S. and Castilla, J.C. (2010) Navigating transformations in governance of Chilean marine coastal resources. Proceedings of the National Academy of Sciences USA 107, 16794–16799.Google Scholar
Guisado, C., Carrasco, S.A., Díaz-Guisado, D., Maltrain, R. and Rojas, H. (2012) Embryonic development, larval morphology and juvenile growth of the sea cucumber Athyonidium chilensis (Holothuroidea: Dendrochirotida). Revista de Biología Marina y Oceanografía 47, 65–73.Google Scholar
Guzmán, H.M., Guevara, C.A. and Hernández, I.C. (2003) Reproductive cycle of two commercial species of sea cucumber (Echinodermata: Holothuroidea) from Caribbean Panama. Marine Biology 142, 271–279.Google Scholar
Hamel, J.F., Himmelman, J.H. and Dufresne, L. (1993) Gametogenesis and spawning of the sea cucumber Psolus fabricii (Duben and Koren). Biological Bulletin 184, 125–143.CrossRefGoogle ScholarPubMed
Hamel, J.-F. and Mercier, A. (1996a) Studies on the reproductive biology of the Atlantic sea cucumber Cucumaria frondosa . SPC bêche-de-mer Information Bulletin 8, 22–33.Google Scholar
Hamel, J.F. and Mercier, A. (1996b) Evidence of chemical communication during the gametogenesis of holothuroids. Ecology 77, 1600–1616.Google Scholar
Harriott, V.J. (1985) Reproductive biology of three congeneric sea cucumber species, Holothuria atra, H. impatiens and H. edulis, at Heron Reef, Great Barrier Reef. Marine and Freshwater Research 36, 51–57.Google Scholar
Herrero-Pérezrul, M.D. and Reyes-Bonilla, H. (2008) Weight-length relationship and relative condition of the holothurian Isostichopus fuscus at Espíritu Santo Island, Gulf of California, México. Revista de Biologia Tropical 56, 273–280.Google Scholar
Hewatt, W.G. (1943) A method for narcotizing holothurians. Science 97, 588.Google Scholar
Kazanidis, G., Antoniadou, C., Lolas, A.P., Neofitou, N., Vafidis, D., Chintiroglou, C. and Neofitou, C. (2010) Population dynamics and reproduction of Holothuria tubulosa (Holothuroidea: Echinodermata) in the Aegean Sea. Journal of the Marine Biological Association of the United Kingdom 90, 895–901.Google Scholar
Larraín, A. (1995) Biodiversidad de equinodermos Chilenos: Estado actual del conocimiento y sinopsis biosistemática. Gayana Zoología 59, 73–96.Google Scholar
Leahy, P.S., Hough-Evans, B.R., Britten, R.J. and Davidson, E.H. (1981) Synchrony of oogenesis in laboratory-maintained and wild populations of the purple sea urchin (Stronglyocentrotus purpuratus). Journal of Experimental Zoology 215, 7–22.Google Scholar
Martinez, M.I., Giménez, J. and Penchaszadeh, P.E. (2011) Reproductive cycle of the sea cucumber Psolus patagonicus Ekman 1925, off Mar del Plata, Buenos Aires, Argentina. Invertebrate Reproduction and Development 55, 124–130.Google Scholar
Moreno, C. (2002) Aspectos reproductivos de Athyonidium chilensis (Semper, 1868) (Echinodermata: Holothuroidea) en la playa El Francés, IV Región, Chile. Masters equivalent thesis. Universidad Católica del Norte, Coquimbo, Chile.Google Scholar
Morgan, A. and Neal, L. (2012) Aspects of reproductive ecology and benthic-pelagic coupling in the sub-antarctic sea cucumber Pseudostichopus mollis (Theel). Continental Shelf Research 43, 36–42.Google Scholar
Murdoch, J.H. (1984) Breeding patterns of two species of North Western Atlantic sea cucumbers (Echinodermata: Holothuroidea). Honours thesis. Mount Allison University, New Brunswick, Canada.Google Scholar
Muthiga, N.A. (2006) The reproductive biology of a new species of sea cucumber, Holothuria (Mertensiothuria) arenacava in a Kenyan marine protected area: the possible role of light and temperature on gametogenesis and spawning. Marine Biology 149, 585–593.Google Scholar
Muthiga, N.A., Kawaka, J.A. and Ndirangu, S. (2009) The timing and reproductive output of the commercial sea cucumber Holothuria scabra on the Kenyan coast. Estuarine, Coastal and Shelf Science 84, 353–360.Google Scholar
Navarro, P.G., García-Sanz, S. and Tuya, F. (2012) Reproductive biology of the sea cucumber Holothuria sanctori (Echinodermata: Holothuroidea). Scientia Marina 76, 741–752.Google Scholar
Pawson, D.L. (1964) The Holothuroidea collected by the Royal Society Expedition to Southern Chile, 1958–1959. Pacific Science 18, 435–470.Google Scholar
Pawson, D.L. (1969) Holothuroidea from Chile – Report No. 46 of the Lund University Chile Expedition 1948–1949. Sarsia 38, 121–145.Google Scholar
Pérez, L.V. (2005) Desarrollo embrionario y larval del pepino de mar Athyonidium chilensis (Semper, 1868) (Echinodermata: Holothuroidea). Masters equivalent thesis. Universidad Católica del Norte, Coquimbo, Chile.Google Scholar
Purcell, S.W. (2010) Managing sea cucumber fisheries with an ecosystem approach. In Lovatelli, A., Vasconcellos, M. and Yimin, Y. (eds) FAO Fisheries and Aquaculture Technical Paper. Volume 520. Rome: FAO.Google Scholar
Purcell, S.W. (2014) Value, market preferences and trade of bêche-de-mer from Pacific Island Sea cucumbers. PLoS ONE 9, 1–8.Google Scholar
Purcell, S.W. and Agudo, N.S. (2013) Optimisation of mesh enclosures for nursery rearing of juvenile sea cucumbers. PLoS ONE 8, 1–10.Google Scholar
Purcell, S.W., Mercier, A., Conand, C., Hamel, J.-F., Toral-Granda, M.V., Lovatelli, A. and Uthicke, S. (2013) Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish and Fisheries 14, 34–59.CrossRefGoogle Scholar
Quinn, G.P. and Keough, M.J. (2002) Experimental design and data analysis for biologists. New York, NY: Cambridge University Press.Google Scholar
Ramofafia, C., Battaglene, S.C., Bell, J.D. and Byrne, M. (2000) Reproductive biology of the commercial sea cucumber Holothuria fuscogilva in the Solomon Islands. Marine Biology 136, 1045–1056.Google Scholar
Ramofafia, C., Byrne, M. and Battaglene, C.S. (2003) Reproduction of the commercial sea cucumber Holothuria scabra (Echinodermata: Holothuroidea) in the Solomon Islands. Marine Biology 142, 281–288.Google Scholar
Ramofafia, C., Byrne, M. and Battaglene, S. (2001) Reproductive biology of the intertidal sea cucumber Actinopyga mauritiana in the Solomon Islands. Journal of the Marine Biological Association of the United Kingdom 81, 523–531.Google Scholar
RStudio Team (2015) RStudio: integrated development for R. Boston, MA: RStudio, Inc.Google Scholar
Rutherford, J.C. (1973) Reproduction, growth and mortality of the holothurian Cucumaria pseudocurata . Marine Biology 22, 167–176.Google Scholar
Sernapesca (2013) Anuario estadístico de pesca (1998–2013). Available at http://www.sernapesca.cl.Google Scholar
Sewell, M.A. (1990) Aspects of the ecology of Stichopus mollis (Echinodermata: Holothuroidea) in northeastern New Zealand. New Zealand Journal of Marine and Freshwater Research 24, 97–103.Google Scholar
Sewell, M.A. (1992) Reproduction of the temperate Aspidochirote Stichopus mollis (Echinodermata: Holothuroidea) in New Zealand. Ophelia 25, 103–121.Google Scholar
Sewell, M.A. and Bergquist, P.R. (1990) Variability in the reproductive cycle of Stichopus mollis (Echinodermata: Holothuroidea). Invertebrate Reproduction and Development 17, 1–7.Google Scholar
Sewell, M.A., Tyler, P.A., Young, C.M. and Conand, C. (1997) Ovarian development in the class Holothuroidea: a reassessment of the “Tubule Recruitment Model”. Biological Bulletin 192, 17–26.Google Scholar
Shiell, G.R. and Uthicke, S. (2006) Reproduction of the commercial sea cucumber Holothuria whitmaei [Holothuroidea: Aspidochirotida] in the Indian and Pacific Ocean regions of Australia. Marine Biology 148, 973–986.Google Scholar
Singh, R., MacDonald, B.A., Lawton, P. and Thomas, M.L.H. (2001) The reproductive biology of the dendrochirote sea cucumber Cucumaria frondosa (Echinodermata: Holothuriodea) using new quantitative methods. Invertebrate Reproduction and Development 40, 125–141.Google Scholar
Smiley, S. (1988) The dynamics of oogenesis and the annual ovarian cycle of Stichopus californicus (Echinodermata: Holothuroidea). Biological Bulletin 175, 79–93.Google Scholar
Smiley, S., McEwen, F.S., Chafee, C. and Krishnan, S. (1991) Echinodermata: Holothuroidea. In Giese, A.C., Pearse, J.S. and Pearse, V.B. (eds) Reproduction of marine invertebrates. Volume VI. Pacific Grove, CA: Boxwood Press, pp. 663–750.Google Scholar
Stotz, W. (2007) Criterios de explotación de recursos bentónicos Secundarios en Áreas de Manejo. Informe final proyecto FIP 2005-42. Chile: Universidad Católica del Norte, 424 pp.Google Scholar
Thorson, G. (1950) Reproductive and larval ecology of marine bottom invertebrates. Biological Reviews 25, 1–45.Google Scholar
Toral-Granda, M.V., Lovatelli, A. and Vasconcellos, M. (2008) Sea cucumbers: a global review of fisheries and trade. FAO Fisheries and Aquaculture Technical Paper no. 516. Rome: FAO.Google Scholar
Toral-Granda, M.V. and Martínez, P.C. (2007) Reproductive biology and population structure of the sea cucumber Isostichopus fuscus (Ludwig, 1875) (holothuroidea) in Caamaño, Galápagos Islands, Ecuador. Marine Biology 151, 2091–2098.Google Scholar
Tyler, P.A. and Gage, J.D. (1983) The reproductive biology of Ypsilothuria talismani (Holothuroidea: Dendrochirota) from the NE Atlantic. Journal of the Marine Biological Association of the United Kingdom 63, 609–616.Google Scholar
Vannuccini, S. (2004) Sea cucumbers: a compendium of fishery statistics . In Lovatelli, A., Conand, C., Purcell, S., Uthicke, S., Hamel, J.-F. and Mercier, A. (eds) Advances in sea cucumber aquaculture and management. FAO Fisheries Technical Paper. Volume 463. Rome: FAO, pp. 399–412.Google Scholar
Vásquez, J.A. (2001) Ecology of Loxechinus albus . Developments in Aquaculture and Fisheries Science 32, 161–175.Google Scholar
Zamora, L.N., Yuan, X., Carton, A.G. and Slater, M.J. (2016) Role of deposit-feeding sea cucumbers in integrated multitrophic aquaculture: progress, problems, potential and future challenges. Reviews in Aquaculture.Google Scholar
Zamora, S. and Stotz, W. (1992) Ciclo reproductivo de Loxechinus albus (Molina 1782) (Echinodermata: Echinoidea) en Punta Lagunillas, IV Región, Coquimbo, Chile. Revista Chilena de Historia Natural 65, 121–133.Google Scholar