Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Temporal and spatial differences in the reproductive biology of the sea urchin Arbacia dufresnii

Lucia Epherra A D , Damián G. Gil B C , Tamara Rubilar A , Soledad Perez-Gallo B C , M. Belén Reartes B C and Javier A. Tolosano B
+ Author Affiliations
- Author Affiliations

A Centro Nacional Patagónico (CENPAT – CONICET), Boulevard Brown 2915, Puerto Madryn (9120), Chubut, Argentina.

B Instituto de Desarrollo Costero, Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB), Ciudad Universitaria, Comodoro Rivadavia (9000), Chubut, Argentina.

C Departamento de Biología General, Facultad de Ciencias Naturales (FCN – UNPSJB), Ciudad Universitaria, Comodoro Rivadavia (9000), Chubut, Argentina.

D Corresponding author. Email: epherra@cenpat.edu.ar

Marine and Freshwater Research 66(4) 329-342 https://doi.org/10.1071/MF14080
Submitted: 26 March 2014  Accepted: 14 June 2014   Published: 26 November 2014

Abstract

The reproductive cycle of Arbacia dufresnii was studied in two contrasting populations on the eastern coast of Patagonia (Nuevo Gulf and San Jorge Gulf) from January 2008 to August 2010. Sea urchins from San Jorge Gulf had larger test diameter and heavier gonads than did sea urchins from Nuevo Gulf. A. dufresnii showed an annual cycle in both populations, with gametogenesis occurring mainly in the autumn and the winter. An extended spawning period took place during the spring and the summer. Sea urchins from Nuevo Gulf had a strong seasonal pattern of reproduction, with presence of gonadal stages showing re-absortion and accumulation of reserves in nutritive cells at different seasons, whereas individuals from San Jorge Gulf had mature gametes during most of the year. Interannual variation of seawater temperature affected the gamete production and spawning duration in both populations. Higher temperatures during gametogenesis enhanced gonadal growth and gametes were released early. The major population differences found in gonadal cell composition highlight the plasticity in reproductive traits of A. dufresnii, and may be responsible for the wide distribution of A. dufresnii in different environments.

Additional keywords: Echinoidea, gametogenic cycle, nutritive phagocytes, Patagonia.


References

Abramoff, M. D., Magalhaes, P. J., and Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International 11, 36–42.

Andrew, N. L. (1986). The interaction between diet and density in influencing reproductive output in the echinoid Evechinus chloroticus (Val.). Journal of Experimental Marine Biology and Ecology 97, 63–79.
The interaction between diet and density in influencing reproductive output in the echinoid Evechinus chloroticus (Val.).Crossref | GoogleScholarGoogle Scholar |

Brewin, P. E., Lamare, M. D., Keogh, J. A., and Mladenov, P. V. (2000). Reproductive variability over a four-year period in the sea urchin Evechinus chloroticus (Echinoidea: Echinodermata) from differing habitats in New Zeland. Marine Biology 137, 543–557.
Reproductive variability over a four-year period in the sea urchin Evechinus chloroticus (Echinoidea: Echinodermata) from differing habitats in New Zeland.Crossref | GoogleScholarGoogle Scholar |

Brogger, M., Martinez, M., and Penchaszadeh, P. (2010). Reproduction of the sea urchin Arbacia dufresnii (Echinoidea: Arbaciidae) from Golfo Nuevo, Argentina. Journal of the Marine Biological Association of the United Kingdom 90, 1405–1409.
Reproduction of the sea urchin Arbacia dufresnii (Echinoidea: Arbaciidae) from Golfo Nuevo, Argentina.Crossref | GoogleScholarGoogle Scholar |

Brogger, M., Gil, D. G., Rubilar, T., Martinez, M., Díaz de Vivar, M. E., Escolar, M., Epherra, L., Pérez, A., and Tablado, A. (2013). Echinoderms from Argentina: biodiversity, distribution and current state of knowledge. In ‘Latin American Echinoderms’. (Eds J. J. Alvarado and F. A. Solís-Marin.) pp. 359–402. (Springer: Berlin.)

Byrne, M., Andrew, N. L., Worthington, D. G., and Brett, P. A. (1998). Reproduction in the diadematoid sea urchin Centrostephanus rodgersii in contrasting habitats along the coast of New South Wales, Australia. Marine Biology 132, 305–318.
Reproduction in the diadematoid sea urchin Centrostephanus rodgersii in contrasting habitats along the coast of New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |

Casas, G. N., Piriz, M. L., and Scrosati, R. (2004). The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biological Invasions 6, 411–416.
The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina).Crossref | GoogleScholarGoogle Scholar |

Casas, G. N., Piriz, M. L., and Parodi, E. R. (2008). Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae: Laminariales) in Nuevo Gulf (Patagonia, Argentina). Journal of the Marine Biological Association of the United Kingdom 88, 21–28.
Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae: Laminariales) in Nuevo Gulf (Patagonia, Argentina).Crossref | GoogleScholarGoogle Scholar |

Ernest, R. G., and Blake, N. J. (1981). Reproductive patterns within sub-populations of Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea). Journal of Experimental Marine Biology and Ecology 55, 25–37.
Reproductive patterns within sub-populations of Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea).Crossref | GoogleScholarGoogle Scholar |

Fernandez, C., and Boudouresque, C. F. (1997). Phenotypic plasticity of Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Marine Ecology Progress Series 152, 145–154.
Phenotypic plasticity of Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment.Crossref | GoogleScholarGoogle Scholar |

Garrido, C. L., and Barber, B. J. (2001). Effects of temperature and food ratio on gonad growth and oogenesis of the green sea urchin, Strongylocentrotus droebachiensis. Marine Biology 138, 447–456.
Effects of temperature and food ratio on gonad growth and oogenesis of the green sea urchin, Strongylocentrotus droebachiensis.Crossref | GoogleScholarGoogle Scholar |

Gaudette, J., Whale, R. A., and Himmelman, J. H. (2006). Spawning events in small and large populations of the green sea urchin Strongylocentrotus droebachiensis as recorded using fertilization assays. Limnology and Oceanography 51, 1485–1496.
Spawning events in small and large populations of the green sea urchin Strongylocentrotus droebachiensis as recorded using fertilization assays.Crossref | GoogleScholarGoogle Scholar |

Gil, D. G., Zaixso, H. E., and Tolosano, J. A. (2009). Brooding of the sub-Antarctic heart urchin, Abatus cavernosus (Spatangoida: Schizasteridae), in southern Patagonia. Marine Biology 156, 1647–1657.
Brooding of the sub-Antarctic heart urchin, Abatus cavernosus (Spatangoida: Schizasteridae), in southern Patagonia.Crossref | GoogleScholarGoogle Scholar |

Heflin, L. E., Gibbs, V. K., Powell, M. L., Makowsky, R., Lawrence, A. L., and Lawrence, J. M. (2012). Effect of diet quality on nutrient allocation to the test and Aristotle’s lantern in the sea urchin Lytechinus variegatus (Lamarck, 1816). Journal of Shellfish Research 31, 867–874.
Effect of diet quality on nutrient allocation to the test and Aristotle’s lantern in the sea urchin Lytechinus variegatus (Lamarck, 1816).Crossref | GoogleScholarGoogle Scholar |

Hernández, J. C., Clemente, S., and Brito, A. (2011). Effects of seasonality on the reproductive cycle of Diadema aff. antillarum in two contrasting habitats: implications for the establishment of a sea urchin fishery. Marine Biology 158, 2603–2615.
Effects of seasonality on the reproductive cycle of Diadema aff. antillarum in two contrasting habitats: implications for the establishment of a sea urchin fishery.Crossref | GoogleScholarGoogle Scholar |

Irigoyen, A. J., Trobbiani, G., Sgarlatta, M. P., and Raffo, M. P. (2011). Effects of the alien algae Undaria pinnatifida (Phaeophyceae, Laminariales) on the diversity and abundance of benthic macrofauna in Golfo Nuevo (Patagonia, Argentina): potential implications for local food webs. Biological Invasions 13, 1521–1532.
Effects of the alien algae Undaria pinnatifida (Phaeophyceae, Laminariales) on the diversity and abundance of benthic macrofauna in Golfo Nuevo (Patagonia, Argentina): potential implications for local food webs.Crossref | GoogleScholarGoogle Scholar |

Isla, F. I., Iantanos, N., and Estrada, E. (2002). Playas reflectivas y disipativas macromareales del Golfo San Jorge, Chubut. Revista de la Asociación Argentina de Sedimentología 9, 155–164.

Kino, S. (2010). Reproduction and early life history of sea urchins, Arbacia dufresnei and Pseudechinus magellanicus, in Chiloe Island and Reloncavi Sound, Chile. Aquaculture Science 58, 65–73.

Laegdsgaard, P., Byrne, M., and Anderson, D. T. (1991). Reproduction of sympatric populations of Heliocidaris erythrogramma and H. tuberculata (Echinoidea) in New South Wales. Marine Biology 110, 359–374.
Reproduction of sympatric populations of Heliocidaris erythrogramma and H. tuberculata (Echinoidea) in New South Wales.Crossref | GoogleScholarGoogle Scholar |

Lawrence, J. M. (1975). On the relationships between marine plants and sea urchin. Oceanography and Marine Biology – an Annual Review 13, 213–286.

Lawrence, J. M. (1987) A functional biology of Echinoderms. In ‘Functional Biology Series’. (Ed P. Calow.). pp. 332–340. (Croom Helm: London.)

Lawrence, J. M., and Lane, P. (1982). The utilization of nutrients by post-metamorphic echinoderms. In ‘Echinoderm Nutrition’. (Eds M. Jangoux and J. M. Lawrence.) pp. 331–372. (Balkema: Rotterdam, the Netherlands.)

Lessios, H. A. (1981). Reproductive periodicity of the echinoids Diadema and Echinometra on the two coasts of Panama. Journal of Experimental Marine Biology and Ecology 50, 47–61.
Reproductive periodicity of the echinoids Diadema and Echinometra on the two coasts of Panama.Crossref | GoogleScholarGoogle Scholar |

Lessios, H. A., Lockhart, S., Collin, R., Sotil, G., Sanchez-Jerez, P., Zigler, K., Pérez, A., Garrido, M., Geyer, L., and Bernardi, G. (2012). Phylogeography and bindin evolution in Arbacia, a sea urchin genus with an unusual distribution. Molecular Ecology 21, 130–144.
Phylogeography and bindin evolution in Arbacia, a sea urchin genus with an unusual distribution.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC387nsVGmtA%3D%3D&md5=5a1370b8bcb80527f585ff4eb23960f4CAS | 21981354PubMed |

Levitan, D. R. (1988). Density-dependent size regulation and negative growth in the sea urchin Diadema antillarum Philippi. Oecologia 76, 621–629.

Levitan, D. R. (1989). Density-dependent size regulation in Diadema antillarum: effects on fecundity and survivorship. Ecology 70, 1414–1424.
Density-dependent size regulation in Diadema antillarum: effects on fecundity and survivorship.Crossref | GoogleScholarGoogle Scholar |

Levitan, D. R. (1991). Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate. The Biological Bulletin 181, 261–268.
Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate.Crossref | GoogleScholarGoogle Scholar |

Levitan, D. R. (1995). The ecology of fertilization in free-spawning invertebrates. In ‘Ecology of Marine Invertebrate Larvae’. (Ed. L. R. McEdward.) pp. 123–156. (CRC Marine Science Series: Boca Raton, FL.)

Levitan, D. R. (1998). Sperm limitation, gamete competition, and sexual selection in external fertilizers. In ‘Sperm Competition and Sexual Selection’. (Eds T. R. Birkhead and A. P. Moller.) pp. 175–206. (Academic Press: San Diego, CA.)

Levitan, D. R., and Young, C. M. (1995). Reproductive success in large populations: empirical measures and theoretical predictions of fertilization in the sea biscuit Clypeaster rosaceus. Journal of Experimental Marine Biology and Ecology 190, 221–241.
Reproductive success in large populations: empirical measures and theoretical predictions of fertilization in the sea biscuit Clypeaster rosaceus.Crossref | GoogleScholarGoogle Scholar |

Levitan, D. R., Sewell, M. A., and Chia, F. S. (1992). How distribution and abundance influence fertilization success in the sea urchin Strongylocentotus franciscanus. Ecology 73, 248–254.
How distribution and abundance influence fertilization success in the sea urchin Strongylocentotus franciscanus.Crossref | GoogleScholarGoogle Scholar |

Lozano, J., Galera, J., López, S., Turon, X., Palacín, C., and Morera, G. (1995). Biological cycles and recruitment of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Marine Ecology Progress Series 122, 179–191.
Biological cycles and recruitment of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats.Crossref | GoogleScholarGoogle Scholar |

Magniez, P. (1983). Reproductive cycle of the brooding echinoid Abatus cordatus (Echinodermata) in Kerguelen (Antarctic Ocean): changes in the organ indices, biochemical composition and caloric content of the gonads. Marine Biology 74, 55–64.
Reproductive cycle of the brooding echinoid Abatus cordatus (Echinodermata) in Kerguelen (Antarctic Ocean): changes in the organ indices, biochemical composition and caloric content of the gonads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhsVKgtLk%3D&md5=5f698dbf9b655b7858df316d16a6a067CAS |

Marsh, A. G., and Watts, S. A. (2007). Biochemical and energy requirements of gonad development. In ‘Edible Sea Urchins: Biology and Ecology’. (Ed. J. M. Lawrence). pp. 35–53. (Elsevier: Amsterdam.)

Mercier, A., and Hamel, J. F. (2009). Introduction. Advances in Marine Biology 55, 1–6.
Introduction.Crossref | GoogleScholarGoogle Scholar |

Newcombe, E., Cárdenas, C., and Geange, S. (2012). Green sea urchins structure invertebrate and macroalgal communities in the Magellan Strait, southern Chile. Aquatic Biology 15, 135–144.
Green sea urchins structure invertebrate and macroalgal communities in the Magellan Strait, southern Chile.Crossref | GoogleScholarGoogle Scholar |

Packard, G. C., and Boardman, T. J. (1999). The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort? Comparative Biochemistry and Physiology Part A 122, 37–44.
The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort?Crossref | GoogleScholarGoogle Scholar |

Pearse, J. S. (1968). Patterns of reproductive periodicities in four species of indo-pacific echinoderms. Proceedings of the Indiana Academy of Sciences 67, 247–279.

Pearse, J. S. (1970). Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez. III. The echinoid Diadema setosum (Leske). Bulletin of Marine Science 20, 697–720.

Pearse, J. S., and Cameron, R. A. (1991). Echinodermata: Echinoidea. In ‘Reproduction of Marine Invertebrates VI: Echinoderms and Lophophorates’. (Eds A. C. Giese, J. S. Pearse and V. B. Pearse.) (The Boxwood Press: Pacific Grove, CA.)

Penchaszadeh, P., and Lawrence, J. M. (1999). Arbacia dufresnei (Echinodermata: Echinoidea): a carnivore in Argentinian waters. In ‘Echinoderm Research’. (Eds M. D. Candia Carnevali and F. Bonasoro.) pp. 525–530. (Balkema: Rotterdarm, the Netherlands.)

Pérez, A. F., Boy, C., Morriconi, E., and Calvo, J. (2010). Reproductive cycle and reproductive output of the sea urchin Loxechinus albus (Echinodermata: Echinoidea) from Beagle Channel, Tierra del Fuego, Argentina. Polar Biology 33, 271–280.
Reproductive cycle and reproductive output of the sea urchin Loxechinus albus (Echinodermata: Echinoidea) from Beagle Channel, Tierra del Fuego, Argentina.Crossref | GoogleScholarGoogle Scholar |

Piriz, M. L., Eyras, M. C., and Rostagno, C. M. (2003). Changes in biomass and botanical composition of beach-cast seaweeds in a disturbed coastal area from Argentine Patagonia. Journal of Applied Phycology 15, 67–74.
Changes in biomass and botanical composition of beach-cast seaweeds in a disturbed coastal area from Argentine Patagonia.Crossref | GoogleScholarGoogle Scholar |

Reuter, K. E., and Levitan, D. R. (2010). Influence of sperm and phytoplankton on spawning in the echinoid Lytechinus variegatus. The Biological Bulletin 219, 198–206.
| 21183441PubMed |

Rivas, A. L., and Ripa, P. (1989). Variación estacional de la estructura termo-halina de golfo Nuevo, Argentina. Geofísica Internacional 28, 3–24.

Schuhbauer, A., Brickle, P., and Arkhipkin, A. (2010). Growth and reproduction of Loxechinus albus (Echinodermata: Echinoidea) at the southerly peripheries of their species range, Falkland Islands (South Atlantic). Marine Biology 157, 1837–1847.
Growth and reproduction of Loxechinus albus (Echinodermata: Echinoidea) at the southerly peripheries of their species range, Falkland Islands (South Atlantic).Crossref | GoogleScholarGoogle Scholar |

Siegel, S., and Castellan, N. J. (1988). ‘Nonparametric Statistics for the Behavioral Sciences.’ (McGraw-Hill Book Company: New York.)

Siikavuopio, S. I., Dale, T., and Mortensen, A. (2007). The effects of stocking density on gonad growth, survival and feed intake of adult green sea urchin (Strongylocentrotus droebachiensis). Aquaculture 262, 78–85.
The effects of stocking density on gonad growth, survival and feed intake of adult green sea urchin (Strongylocentrotus droebachiensis).Crossref | GoogleScholarGoogle Scholar |

Sokal, R. R., and Rohlf, F. J. (1995). ‘Biometry: the Principles and Practice of Statistics in Biological Research.’ 3rd edn. (W. H. Freeman: New York.)

Starr, M., Himmelman, J. H., and Therriault, J.-C. (1991). Isolation and properties of a substance from the diatom Phaeodactylum tricornutum which induces spawning in the sea urchin Strongylocentrotus droebachiensis. Marine Ecology Progress Series 79, 275–287.
Isolation and properties of a substance from the diatom Phaeodactylum tricornutum which induces spawning in the sea urchin Strongylocentrotus droebachiensis.Crossref | GoogleScholarGoogle Scholar |

Styan, C. A. (1997). Inexpensive and portable sampler for collecting eggs of free-spawning marine invertebrates underwater. Marine Ecology Progress Series 150, 293–296.
Inexpensive and portable sampler for collecting eggs of free-spawning marine invertebrates underwater.Crossref | GoogleScholarGoogle Scholar |

Tavares, Y. A. G. (2004). Biologia reprodutiva dos equinóides Echinometra lucunter (Linnaeus, 1758) e Arbacia lixula (Linnaeus, 1758) na Ilha da Galheta, litoral paranaense, Brasil. Ph.D. Thesis, Universidade Federal do Paraná, Brazil.

Tomas, F., Romero, J., and Turon, X. (2005). Experimental evidence that intra-specific competition in seagrass meadows reduces reproductive potential in the sea urchin Paracentrotus lividus (Lamarck). Scientia Marina 69, 475–484.
Experimental evidence that intra-specific competition in seagrass meadows reduces reproductive potential in the sea urchin Paracentrotus lividus (Lamarck).Crossref | GoogleScholarGoogle Scholar |

Turon, X., Giribet, S., López, S., and Palacín, C. (1995). Growth and population structure of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Marine Ecology Progress Series 122, 193–204.
Growth and population structure of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats.Crossref | GoogleScholarGoogle Scholar |

Vinuesa, J. H., Varisco, M. A., and Balzi, P. (2013). Feeding strategy of early juvenile stages of the southern king crab Lithodes santolla in the San Jorge Gulf, Argentina. Revista de Biología Marina y Oceanografía 48, 353–363.
Feeding strategy of early juvenile stages of the southern king crab Lithodes santolla in the San Jorge Gulf, Argentina.Crossref | GoogleScholarGoogle Scholar |

Wahle, R., and Peckham, S. (1999). Density-related reproductive trade-offs in the green sea urchin, Strongylocentrotus droebachiensis. Marine Biology 134, 127–137.
Density-related reproductive trade-offs in the green sea urchin, Strongylocentrotus droebachiensis.Crossref | GoogleScholarGoogle Scholar |

Walker, C. W. (1982). Nutrition of gametes. In ‘Echinoderm Nutrition’. (Eds M. Jangoux and J. M. Lawrence.) pp. 449–468. (Balkema: Rotterdam, the Netherlands.)

Walker, C. W., Unuma, T., and Lesser, M. P. (2007). Gametogenesis and reproduction of sea urchins. In ‘Edible Sea Urchins: Biology and Ecology’. (Ed. J. M. Lawrence.) pp. 11–33. (Elsevier: Amsterdam.)

Wangensteen, O. S. (2013). Biology and phylogeography of the black sea urchin Arbacia lixula (Echinoidea: Arbacioida). Ph.D. Thesis, Universitat de Barcelona, Spain.

Wangensteen, O. S., Turon, X., Casso, M., and Palacín, C. (2013). The reproductive cycle of the sea urchin Arbacia lixula in northwest Mediterranean: potential influence of temperature and photoperiod. Marine Biology 160, 3157–3168.
The reproductive cycle of the sea urchin Arbacia lixula in northwest Mediterranean: potential influence of temperature and photoperiod.Crossref | GoogleScholarGoogle Scholar |

Yund, P. O. (2000). How severe is sperm limitation in natural populations of marine free-spawners? Trends in Ecology & Evolution 15, 10–13.
How severe is sperm limitation in natural populations of marine free-spawners?Crossref | GoogleScholarGoogle Scholar |

Zaixso, H. E., and Lizarralde, Z. I. (2000). Distribución de equinodermos en el golfo San José y sur del golfo San Matías (Chubut, Argentina). Revista de Biología Marina y Oceanografía 35, 127–145.
Distribución de equinodermos en el golfo San José y sur del golfo San Matías (Chubut, Argentina).Crossref | GoogleScholarGoogle Scholar |

Zaixso, H. E., Boraso de Zaixso, A. L., Pastor de Ward, C. T., Lizarralde, Z. I., Dadón, J., and Galván, D. E. (in press). El bentos costero patagónico. In ‘La zona costera patagónica Argentina’. (Ed. H. E. Zaixso.) (Editorial Universitaria Patagónica: Comodoro Rivadavia, Argentina.)

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.

Zamora, S., and Stotz, W. (1993). Variabilidad reproductiva del erizo negro Tetrapygus niger (Molina 1782) en dos localidades del norte de Chile: implicancias a nivel individual y poblacional. Revista Chilena de Historia Natural 66, 171–176.