Skip to main content
Log in

Annual reproductive cycles of the commercial sea urchinParacentrotus lividus from an exposed intertidal and a sheltered subtidal habitat on the west coast of Ireland

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Reproduction of the commercial sea urchinParacentrotus lividus (Lamarck) from contrasting habitats on the west coast of Ireland was examined from May 1986 through August 1988. Urchins were collected intertidally from an exposed rocky shore and subtidally from a protected bay. Monthly measurements of the gonad index and histological examination of the gonads demonstrated thatP. lividus has an annual reproductive cycle. Although the two populations exhibited similar reproductive patterns over three breeding seasons, there were inter-annual and inter-population differences in the amplitude of gonadal growth and in the time when spawning started. The subtidal urchins had significantly larger gonads and exhibited a longer period of reproductive maturity compared with the intertidal urchins. This difference was also evident in the histology of the ovaries at the beginning of breeding, when most of the subtidal females contained mature ovaries, whereas most of the intertidal females contained premature ovaries. An inter-annual difference in the onset of spawning was observed, with the start of gamete release differing by as much as four weeks between years. It appears that inter-annual differences in sea temperature influence the temporal variation in spawning byP. lividus and that increasing temperature may serve as an exogenous cue for gamete release. The inter-annual variability in the onset of spawning suggests that photoperiod does not cue gamete release. Gonadal growth, on the other hand, occurs during the coldest months of the year and during the period of shortest days, suggesting that temperature and photoperiod may both influence gonadal growth during the winter. Oogenesis and spermatogenesis ofP. lividus were examined histologically. During the post-spawning recovery and growth stages, the gonads gained weight through growth of the nutritive phagocytes and the accumulation of periodic acid Schiff (PAS) + droplets by these cells. The PAS + material appears to play a nutritive role in gametogenesis. For the females, the frequencies of six ovarian maturity stages was assessed at approximately monthly intervals. Small oocytes were present throughout the year and clusters of early oocytes were most apparent during the spent and recovery stages. With the onset of vitellogenesis and subsequent accumulation of ova, the nutritive phagocytes and their PAS + droplets became depleted. The ovarian condition at the onset of breeding was variable, due to differences in the number of vitellogenic oocytes, differences in the number of ova in storage, and differences in the amount of PAS + material. In general, the nutritive phagocyte tissue is reduced by the onset of spawning and is exhausted by the termination of breeding. A similar series of events occurs during spermatogenesis. The relevance of this study for the use ofP. lividus as a brood-stock organism for mariculture is discussed.

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

Literature cited

  • Allain, J. Y. (1975). Structures des populations deParacentrotus lividus (Lamarck) (Echinodermata, Echinoidea) soumises à la pêche sur les côtes de Bretagne. Revue Trav. Inst. (scient. tech.) Pêch. marit. 39: 171–209

    Google Scholar 

  • Andrew, N. L. (1986). The interaction between diet and density in influencing reproductive output in the echinoidEvechinus chlorticus (Val.) J. exp. mar. Biol. Ecol. 97: 63–79

    Google Scholar 

  • Bay-Schmith, E., Pearse, J. S. (1987). Effect of fixed daylengths on the photoperiod regulation of gametogenesis in the sea urchinStrongylocentrotus purpuratus. Invert. Reprod. Dev. 11: 287–294

    Google Scholar 

  • Bernard, F. R. (1977). Fishery and reproductive cycle of the red sea urchinStrongylocentrotus franciscanus, in British Columbia. J. Fish. Res. Bd Can 34: 604–610

    Google Scholar 

  • Birais, D., Le Gall, P. (1986). 200 metres de toboggan pour oursins. Aqua Revue 5: 31–35

    Google Scholar 

  • Boolotian, R. A., Moore, A. R. (1956). Hermaphroditism in echinoids. Biol. Bull. mar. biol. Lab., Woods Hole 111: 328–335

    Google Scholar 

  • Chatlynne, L. G. (1969). A histochemical study of oogenesis in the sea urchinStrongylocentrotus purpuratus. Biol. Bull. mar. biol. Lab., Woods Hole 136: 167–184

    Google Scholar 

  • Chiu, S. T. (1986). Effects of the urchin fishery on the population structure ofAnthocidaris crassispina (Echinodermata: Echinoidea) in Hong Kong. In: Maclean, J. L., Dizon, L. B., Hosillos, L. V. (eds.) The First Asian Fisheries Forum. Asian Fisheries Society, Manila, Philippines, p. 361–366

    Google Scholar 

  • Chiu, S. T. (1988). Reproductive biology ofAnthocidaris crassispina (Echinodermata: Echinoidea) in Hong Kong. In: Burke, R. D., Lambert, P. V., Parsley, R. L. (eds.) Echinoderm biology. Balkema, Rotterdam, p. 193–204

    Google Scholar 

  • Costelloe, J. (1988). Reproductive cycle, development and recruitment of two geographically separated populations of the dendrochirote holothurianAslia lefevrei. Mar. Biol. 99: 535–545

    Google Scholar 

  • Crapp, G. B., Willis, M. E. (1975). Age determination in the sea urchinParacentrotus lividus (Lamarck), with notes on the reproductive cycle. J. exp. mar. Biol. Ecol. 20: 157–178

    Google Scholar 

  • Czihak, G. (1971). Echinoids. In: Reverberi, G. (ed.) Experimental embryology of marine and freshwater invertebrates. North-Holland, Amsterdam, p. 363–506

    Google Scholar 

  • Denny, M. W., Daniel, T. L., Koehl, M. A. R. (1985). Mechanical limits to size in wave-swept organisms. Ecol. Monogr. 55: 69–102

    Google Scholar 

  • Dominique, F. (1973). Contribution à l'étude du cycle annuel de reproduction de deux espèces d'echinoides (echinodermata) des côtes de Bretagne. B.Sc. thesis, Université Libre de Bruxelles

  • Drzewina, A. Bohn, G. (1924). Un nouveau cas d'hermaphrodisme chez l'oursinStrongylocentrotus lividus. C.r. hebd. Séanc. Acad. Sci., Paris 178: 662–663

    Google Scholar 

  • Ebert, T. A. (1968). Growth rates of the sea urchinStrongylocentrotus purpuratus related to food availability and spine abrasion. Ecology 49: 1075–1091

    Google Scholar 

  • Fenaux, L. (1968). Maturation des gonades et cycle saisonnier des larves chezA. lixula, P. lividus etP. microtuberculatus (echinides) à Villefranche-Sur-Mer. Vie Milieu 13: 1–52

    Google Scholar 

  • Fox, H. M. (1923). Lunar periodicity in reproduction. Proc. R. Soc. (Ser. B) 95: 523–550

    Google Scholar 

  • Fox, H. M. (1924). The spawning of echinoids. Biol. Rev. 2: 71–74

    Google Scholar 

  • Fuji, A. (1960a). Studies on the biology of the sea urchin. I. Superficial and histological gonadal changes in gametogenic process of two sea urchins,Strongylocentrotus nudus andS. intermedius. Bull. Fac. Fish. Hokkaido Univ. 11: 1–14

    Google Scholar 

  • Fuji, A. (1960b). Studies on the biology of the sea urchin. III. Reproductive cycle of two sea urchins,Strongylocentrotus nudus andS. intermedius. Bull. Fac. Fish. Hokkaido Univ. 11: 49–57

    Google Scholar 

  • Giese, A. C., Kanatani, H. (1987). Maturation and spawning. In: Giese, A. C., Pearse, J. S., Pearse, V. B. (eds.) Reproduction of marine invertebrates. Vol. 9. Blackwell Scientific, Palo Alto, p. 251–329

    Google Scholar 

  • Giese, A. C., Pearse, J. S. (1974). Introduction: general principles. In: Giese, A. C., Pearse, J. S. (eds.) Reproduction of marine invertebrates. Vol. 1. Academic Press, New York, p. 1–49

    Google Scholar 

  • Gonor, J. J. (1972). Gonad growth in the sea urchinStrongylocentrotus purpuratus (Stimpson) (Echinodermata: Echinoidea) and the assumptions of the gonad index methods. J. exp. mar. Biol. Ecol. 10: 89–103

    Google Scholar 

  • Gonor, J. J. (1973a). Reproductive cycles in Oregon populations of the echinoidStrongylocentrotus purpuratus (Stimpson). I. Annual gonad growth and ovarian gametogenic cycles. J. exp. mar. Biol. Ecol. 12: 45–64

    Google Scholar 

  • Gonor, J. J. (1973b). Reproductive cycles in Oregon populations of the echinoidStrongylocentrotus purpuratus (Stimpson). II. Seasonal changes in oocyte growth and in abundance of gametogenic stages in the ovary. J. exp. mar. Biol. Ecol. 12: 65–78

    Google Scholar 

  • Gonor, J. J. (1973c). Sex ratio and hermaphroditism in Oregon intertidal populations of the echinoidStrongylocentrotus purpuratus. Mar. Biol. 19: 278–280

    Google Scholar 

  • Himmelman, J. H. (1975). Phytoplankton as a stimulus for spawning in three marine invertebrates. J. exp. mar. Biol. Ecol. 20: 199–214

    Google Scholar 

  • Himmelman, J. H. (1978). Reproductive cycles of the green sea urchinStrongylocentrotus droebachiensis. Can. J. Zool. 56: 1828–1836

    Google Scholar 

  • Holland, N. D. (1976). Gametogenesis during the annual reproductive cycle in a cidaroid sea urchin (Stylocidaris affinis). Biol. Bull. mar. biol. Lab., Woods Hole 133: 578–590

    Google Scholar 

  • Keats, D. W., Steele, D. H., South, G. R. (1983). Food relations and short term aquaculture potential of the green sea urchinStrongylocentrotus droebachiensis in Newfoundland. Tech. Rep. meml Univ. Newf. mar. Sci. Res. Lab. 24: 1–24

    Google Scholar 

  • Keats, D. W., Steele, D. H., South, G. R. (1984). Depth-dependent reproductive output of the green sea urchinStrongylocentrotus droebachiensis (O. F. Müller), in relation to the nature and availability of food. J. exp. mar. Biol. Ecol. 80: 71–91

    Google Scholar 

  • Kečheš, S. (1966). Lunar periodicity in sea urchins. Z. Naturf. (Abt. B) 21: 1100–1101

    Google Scholar 

  • Lane, J. M., Lawrence, J. M. (1979). Gonadal growth and gametogenesis in the sand dollarMellita quinquesperforata (Leske, 1778). J. exp. mar. Biol. Ecol. 38: 271–285

    Google Scholar 

  • Larson, B. R., Vadas, R. L., Keser, M. (1980). Feeding and nutritional ecology ofStrongylocentrotus droebachiensis in Maine, USA. Mar. Biol. 59: 49–62

    Google Scholar 

  • Lawrence, J. M. (1987). A functional biology of echinoderms. Croom Helm, London

    Google Scholar 

  • Lawrence, J. M., Lane, J. M. (1982). The utilization of nutrients by postmetamorphic echinoderms. In: Jangoux, M., Lawrence, J. M. (eds.) Echinoderm nutrition. Balkema, Rotterdam, p. 331–371

    Google Scholar 

  • McEuen, F. S. (1988). Spawning behaviors of northeast Pacific sea cucumbers (Holothuroidea: Echinodermata). Mar. Biol. 98: 565–585

    Google Scholar 

  • Miller, R. L. (1985). Demonstration of sperm chemotaxis in Echinodermata: Asteroidea, Holothuroidea, Ophiuroidea. J. exp. Zool. 234: 383–414

    Google Scholar 

  • Minchin, D. (1987). Sea-water temperature and spawning behaviour in the seastarMarthasterias glacialis. Mar. Biol. 95: 139–143

    Google Scholar 

  • Mortensen, T. (1943). A Monograph of the Echinoidea. C. A. Reitzel, Copenhagen

    Google Scholar 

  • O'Sullivan, S. (1988). Aspects of the ecology and culture of the purple sea urchinParacentrotus lividus (Lamarck). B. Sc. thesis, University College, Cork

    Google Scholar 

  • Ozaki, H., Moriya, O., Harrington, F. E. (1986). A glycoprotein in the accessory cell of the echinoid ovary and its role in vitellogenesis. Roux's Archs devl Biol. 195: 74–79

    Google Scholar 

  • Pearse, J. S. (1969). Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez. II. The echinoidEchinometra mathaei (De Blainville). Bull. mar. Sci. 19: 580–613

    Google Scholar 

  • Pearse, J. S. (1975). Lunar reproductive rhythms in sea urchins. A review. J. interdiscipl. Cycle Res. 6: 47–52

    Google Scholar 

  • Pearse, J. S. (1981). Synchronization of gametogenesis in the sea urchinsStrongylocentrotus purpuratus andS. franciscanus. In: Clark, W. H. Jr., Adams, T. S. (eds.) Advances in invertebrate reproduction. Elsevier North Holland, Amsterdam, p. 53–68

    Google Scholar 

  • Pearse, J. S., Cameron, R. A. (in press). Echinoidea. In: Giese, A. C., Pearse, J. S., Pearse, V. B. (eds.) Reproduction of marine invertebrates. Vol. 6. Blackwell Scientific, Palo Alto

  • Pearse, J. S., McClary, D. J., Sewell, M. A., Austin, W. C., Perez-Ruzafa, A., Byrne, M. (1988). Simultaneous spawning of six species of echinoderms in Barkley Sound, British Columbia. Invert. Reprod. Dev. 14: 279–288

    Google Scholar 

  • Pearse, J. S., Pearse, V. B., Davis, K. K. (1986). Photoperiodic regulation of gametogenesis and growth in the sea urchinStrongylocentrotus purpuratus. J. exp. Zool. 237: 107–118

    Google Scholar 

  • Pennington, J. T. (1985). The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol. Bull. mar. biol. Lab., Woods Hole 169: 417–430

    Google Scholar 

  • Régis, M.-B. (1979). Analyse des fluctuations des indices physiologiques chez deux échinoides (Paracentrotus lividus (Lmck) etArbacia Lixula L.) du Golfe de Marseille. Téthys 9: 167–181

    Google Scholar 

  • Régis, M.-B. (1980). Étude des possibilités d'elevage des oursins réguliers en fonction de la valeur de certains indices physiologiques. Oceanol. Acta 3: 7–15

    Google Scholar 

  • Régis, M.-B., Pérès, J.-M. Gras, G. (1986). Données préliminaires sur l'exploitation de la ressource:Paracentrotus lividus (Lmck) dans le Quartier Maritime de Marseille. Vie mar. 7: 41–60

    Google Scholar 

  • Roden, C. M., Hensey, M., Ludgate, R. (1987). Aquaculture in Kilkieran and Bertraghbuoy Bays (Co. Galway); an atlas on environmental factors. National Board for Science and Technology, Dublin (Aquacult. tech. Bull. No. 12)

    Google Scholar 

  • Rink, T. J. (1988). Chemoattractant for sea urchin sperm. Nature, Lond. 334: p. 649

    Google Scholar 

  • Runnström, S. (1927). Über die Thermopathie der Fortpflanzung und Entwicklung mariner Tiere in Beziehung zu ihrer geographischen Verbreitung. Bergens Mus. Årb. (Naturvidens. rek.) 1927(2): 1–67

    Google Scholar 

  • Shyu, A.-B., Raff, R. A., Blumenthal, T. (1986). Expression of the vitellogenin gene in female and male sea urchin. Proc. natn. Acad. Sci. U.S.A. 83: 3865–3869

    Google Scholar 

  • Southward, A. J., Crisp, D. J. (1954). The distribution of intertidal animals around the Irish coast. Proc. R. Ir. Acad. (Ser. B) 57: 1–29

    Google Scholar 

  • Southward, A., Southward, E. (1975). Endangered urchins. New Scient. 10: 70–72

    Google Scholar 

  • Tyler, P. A., Gage, J. D. (1984). The reproductive biology of echinothuriid and cidarid sea urchins from the deep sea (Rockall Trough, North-East Atlantic Ocean). Mar. Biol. 80: 63–74

    Google Scholar 

  • Vadas, R. L. (1977). Preferential feeding: an optimization strategy in sea urchins. Ecol. Monogr. 47: 337–371

    Google Scholar 

  • Walker, C. W. (1982). Nutrition of gametes. In: Jangoux, M., Lawrence, J. M. (eds.) Echinoderm nutrition. Balkema, Rotterdam, p. 449–468

    Google Scholar 

  • Willis, M. E. (1976). Studies on the biology of the sea urchin,Paracentrotus lividus (Lamarck) in Bantry Bay, south-west Ireland. MSc. thesis, University College, Cork

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by G. F. Humphrey, Sydney

Rights and permissions

Reprints and permissions

About this article

Cite this article

Byrne, M. Annual reproductive cycles of the commercial sea urchinParacentrotus lividus from an exposed intertidal and a sheltered subtidal habitat on the west coast of Ireland. Mar. Biol. 104, 275–289 (1990). https://doi.org/10.1007/BF01313269

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01313269

Keywords

Navigation