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On the reproduction of the Mediterranean keystone limpet Patella rustica: histological overview

Published online by Cambridge University Press:  17 July 2014

Ivana Prusina*
Affiliation:
Department of Aquaculture, University of Dubrovnik, Ćira Carića 4, 20000Dubrovnik, Croatia
Daria Ezgeta-Balić
Affiliation:
Institute of Oceanography and Fisheries, Šetalište Ivana Meštrovića 63, 21000 Split, Croatia
Stijepo Ljubimir
Affiliation:
Institute for Marine and Coastal Research, University of Dubrovnik, Kneza Damjana Jude 12, 20000 Dubrovnik, Croatia
Tatjana Dobroslavić
Affiliation:
Department of Aquaculture, University of Dubrovnik, Ćira Carića 4, 20000Dubrovnik, Croatia
Branko Glamuzina
Affiliation:
Department of Aquaculture, University of Dubrovnik, Ćira Carića 4, 20000Dubrovnik, Croatia
*
Correspondence should be addressed to: I. Prusina, Department of Aquaculture, University of Dubrovnik, Ćira Carića 4, 20000 Dubrovnik, Croatia email: ivana.prusina@unidu.hr

Abstract

The reproductive cycle of the high shore limpet Patella rustica is described based on histological analysis as the primary method of staging gonad development. Sex-ratios, shell length at sexual maturity, gonad developmental stages, mean gonad index and oocyte size were investigated. Males and females were found to differ in size distribution, with females becoming more prevalent from ~28 mm onwards. The estimated shell length at which 50% of males were sexually mature was 13.1 mm. Patella rustica has only one reproductive cycle per year with a spawning peak between November and December for both sexes, and gonad redevelopment from January. First data on the size–frequency analysis of oocytes for this species are also presented, concurring with the qualitative analysis of the gonad developmental stages. This study presents updated information on the reproductive cycle of this keystone species and provides the first account of the reproductive biology of P. rustica in the Adriatic Sea.

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

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References

REFERENCES

Bacci, G. (1947) Sex reversal in Patella coerulea L. and Diodora gibberula (Lam). Nature 160, 9495.Google Scholar
Belkhodja, H., Jaafoura, M.H., Missaoui, H. and Romdhane, M.S. (2011) Histological investigation of the reproductive cycle of the limpet Patella caerulea Linnaeus, 1758. Cahiers de Biologie Marine 52, 279290.Google Scholar
Blackmore, D.T. (1969) Studies of Patella vulgata L. I. Growth, reproduction and zonal distribution. Journal of Experimental Marine Biology and Ecology 3, 200213.CrossRefGoogle Scholar
Bowman, R.S. (1985) The biology of the limpet Patella vulgata L. in the British Isles: spawning time as a factor determining recruitment success. In Moore, P.G. and Seed, R. (eds) The ecology of rocky coasts. London: Hodder and Stoughton Press, pp. 178193.Google Scholar
Bowman, R.S. and Lewis, J.R. (1986) Geographical variation in the breeding cycles and recruitment of Patella spp. Hydrobiologia 142, 4156.Google Scholar
Branch, G.M. (1974) The ecology of Patella Linnaeus from the Cape peninsula, South Africa. II. Reproductive cycles. Transactions of the Royal Society of South Africa 41, 111160.CrossRefGoogle Scholar
Branch, G.M. (1981) The biology of limpets: physical factors, energy flow, and ecological interactions. Oceanography and Marine Biology: an Annual Review 19, 235379.Google Scholar
Brazão, S., Boaventura, D., Morais, S., Narciso, L. and , P. (2003) Reproduction of Patella depressa Pennant, 1777 on the central Portuguese coast. Boletín Instituto Español de Oceanografía 19, 453460.Google Scholar
Brêthes, J.C., Ferreyra, G. and de la Vega, S. (1994) Distribution, growth and reproduction of the limpet Nacella (Patinigera) concinna (Strebel 1908) in relation to potential food availability, in Esperanza Bay (Antarctic Peninsula). Polar Biology 14, 161170.Google Scholar
Coleman, R.A., Underwood, A.J., Benedetti-Cecchi, L., Åberg, P., Arensa, F., Arrontes, J., Castro, J., Hartnoll, R.G., Jenkins, S.R., Paula, J., Della Santina, P. and Hawkins, S.J. (2006) A continental scale evaluation of the role of limpet grazing on rocky shores. Oecologia 147, 556564.Google Scholar
Delany, J., McGrath, D., O'Riordan, R. and Myers, A.A. (2002) Reproduction in the intertidal limpets Patella vulgata and Patella ulyssiponensis. In Myers, A. (ed.) New Survey of Clare Island, Volume 3, Marine intertidal ecology. Dublin: Royal Irish Academy, pp. 91116.Google Scholar
Della Santina, P., Sonni, C., Sartoni, G. and Chelazzi, G. (1993) Food availability and diet composition of three coexisting Mediterranean limpets (Patella spp.). Marine Biology 116, 8795.Google Scholar
Espinosa, F., Guerra-García, J.M., Fa, D. and García-Gómez, J.C. (2006) Aspects of reproduction and their implications for the conservation of the endangered limpet, Patella ferruginea. Invertebrate Reproduction and Development 49, 8592.CrossRefGoogle Scholar
Espinosa, F. and Ozawa, T. (2006) Population genetics of the endangered limpet Patella ferruginea (Gastropoda: Patellidae): taxonomic, conservation and evolutionary considerations. Journal of Zoological Systematics and Evolutionary Research 44, 816.Google Scholar
Espinosa, F., Rivera-Ingraham, G.A., Fa, D. and García-Gómez, J.C. (2009) Effect of human pressure on population size structures of the endangered ferruginean limpet: toward future management measures. Journal of Coastal Research 25, 857863.Google Scholar
Evans, R.G. (1953) Studies on the biology of the British limpets—the genus Patella on the south coast of England. Proceedings of the Zoological Society of London 123, 357376.CrossRefGoogle Scholar
Frenkiel, L. (1975) Contribution à l'étude des cycles de reproduction des Patellidae en Algèrie. Marine Ecology—Pubblicazioni della Stazione Zoologica di Napoli 39, 153189.Google Scholar
Fretter, V. and Graham, A. (1976) The prosobranch molluscs of Britain and Denmark. I. Pleurotomariacea, Fissurellacea and Patellacea. Journal of Molluscan Studies 1, 137.Google Scholar
Gosling, E. (2003) Bivalve molluscs: biology, ecology and culture. Oxford: Blackwell.Google Scholar
Gray, D.R. and Hodgson, A.N. (2003) Growth and reproduction in the high-shore South African limpet Helcion pectunculus (Mollusca: Patellogastropoda). Journal of African Zoology 38, 371386.Google Scholar
Guallart, J., Calvo, M., Acevedo, I. and Templado, J. (2013) Two-way sex change in the endangered limpet Patella ferruginea (Mollusca, Gastropoda). Invertebrate Reproduction and Development 57, 247253.Google Scholar
Guerra, M.T. and Gaudêncio, M.J. (1986) Aspects of the ecology of Patella spp. on the Portuguese coast. Hydrobiologia 142, 5769.Google Scholar
Hadfield, M.G., Strathmann, M.F. and Strathmann, R.R. (1997) Ciliary currents of non-feeding veligers in putative basal clades of gastropods. Invertebrate Biology 116, 313321.CrossRefGoogle Scholar
Hawkins, S.J., Corte-Real, H.B.S.M., Pannacciulli, F.G., Weber, L.C. and Bishop, J.D.D. (2000) Thoughts on the ecology and evolution of the intertidal biota of the Azores and other Atlantic islands. Hydrobiologia 440, 317.CrossRefGoogle Scholar
Hawkins, S.J., Hartnoll, R.G., Kain, J.M. and Norton, T.A. (1992) Plant–animal interactions on hard substrata in the north-east Atlantic. In John, D.M., Hawkins, S.J., Price, J.H. (eds) Plant–animal interactions in the marine benthos. Systematics Association Special, Volume 46. Oxford: Clarendon Press, pp. 132.Google Scholar
Hoagland, K.E. (1978) Protandry and the evolution of environmentally-mediated sex-change: a study of the mollusca. Malacologia 17, 365391.Google Scholar
Jeffrey, S.W. and Welschmeyer, N.A. (1997) Spectrophotometric and fluorometric equations in common use in oceanography. In Jeffrey, S.W., Mantoura, R.F.C. and Wright, S.W. (eds) Phytoplankton pigments in oceanography: guidelines to modern methods. Paris: UNESCO Publishing, pp. 597615.Google Scholar
Jenkins, S.R., Coleman, R.A., Burrows, M.T., Hartnoll, R.G. and Hawkins, S.J. (2005) Regional scale differences in determinism of limpet grazing effects. Marine Ecology Progress Series 287, 7786.Google Scholar
Katsanevakis, S., Lefkaditou, E., Galinou-Mitsoudi, S., Koutsoubas, D. and Zenetos, A. (2008) Molluscan species of minor commercial interest in Hellenic seas: distribution, exploitation and conservation status. Mediterranean Marine Science 9, 77118.Google Scholar
Kido, J.S. and Murray, S.N. (2003) Variation in owl limpet Lottia gigantea population structures, growth rates, and gonadal production on southern California rocky shores. Marine Ecology Progress Series 257, 111124.Google Scholar
Le Quesne, J.F. and Hawkins, S.J. (2006) Direct observations of protandrous sex change in the patellid limpet Patella vulgata. Journal of the Marine Biological Association of the United Kingdom 86, 161162.Google Scholar
Lima, F.P., Queiroz, N., Ribeiro, P.A., Hawkins, S.J. and Santos, A.M. (2006) Recent changes in the distribution of a marine gastropod, Patella rustica Linnaeus, 1758, and their relationship to unusual climatic events. Journal of Biogeography 33, 812822.Google Scholar
Lindberg, D.R. and Wright, W.G. (1985) Patterns of sex change of the protandric patellacean limpet Lottia gigantea (Mollusca: Gastropoda). Veliger 27, 261265.Google Scholar
Mauro, A., Arculeo, M. and Parrinello, N. (2003) Morphological and molecular tools in identifying the Mediterranean limpets Patella caerulea, Patella aspera and Patella rustica. Journal of Experimental Marine Biology and Ecology 295, 131143.Google Scholar
McCarthy, M., Woosnam, P. and Culloty, S.C. (2008) Histological investigation of the reproductive cycles of the limpets Patella vulgata and Patella ulyssiponensis. Marine Biology 153, 871877.Google Scholar
Moore, P., Thompson, R.C. and Hawkins, S.J. (2007) Effects of grazer identity on the probability of escapes by a canopy-forming macroalga. Journal of Experimental Marine Biology and Ecology 344, 170180.Google Scholar
Morriconi, E. (1999) Reproductive biology of the limpet Nacella (P.) deaurata (Gmelin, 1971) in Bahia Lapataia (Beagle Channel). Scientia Marina 63, 417426.Google Scholar
Navarro, P.G., Ramirez, R., Tuya, F., Fernandez-Gil, C., Sanchez-Jerez, P. and Haroun, R.J. (2004) Hierarchical analysis of spatial distribution patterns of patellid limpets in the Canary islands. Journal of Molluscan Studies 71, 6773.Google Scholar
Orton, J.H. and Southward, A.J. (1961) Studies on the biology of limpets. IV. The breeding of Patella depressa Pennant on the north Cornish coast. Journal of the Marine Biological Association of the United Kingdom 41, 653662.Google Scholar
Orton, J.H., Southward, A.J. and Dodd, J.M. (1956) Studies on the biology of limpets II. The breeding of Patella vulgata L. in Britain. Journal of the Marine Biological Association of the United Kingdom 35, 149176.CrossRefGoogle Scholar
Othaitz, J.P. (1994) Estudio de los ciclos reproductores de cuatro species de lapas y dos de tróquidos (Gastropoda, Prosobranchia) del piso intermareal de la costa Vasca. PhD thesis. Universidad Autónoma de Madrid, Spain.Google Scholar
Paine, R.T. (2002) Trophic control of production in a rocky intertidal community. Science 296, 736739.Google Scholar
Power, M.E., Tilman, D., Estes, J.A., Menge, B.A., Bond, W.J., Mills, L.S., Gretchen, D., Castilla, J.C., Lubchenco, J. and Paine, R.T. (1996) Challenges in the quest for keystones. BioScience 46, 609620.Google Scholar
Prusina, I. (2013) Growth and reproduction of the limpet Patella rustica Linnaeus, 1758 and heat stress physiology of the Mediterranean patellid limpets. PhD thesis. University of Split, Croatia.Google Scholar
Ribeiro, P.A., Xavier, R., Santos, A.M. and Hawkins, S.J. (2009) Reproductive cycles of four species of Patella (Mollusca: Gastropoda) on the northern and central Portuguese coast. Journal of the Marine Biological Association of the United Kingdom 89, 12151221.Google Scholar
Ridgway, S.A., Reid, D.G., Taylor, J.D., Branch, G.M. and Hodgson, A.N. (1998) A cladistic phylogeny of the family Patellidae (Mollusca: Gastropoda). Philosophical Transactions of the Royal Society, B 353, 16451671.Google Scholar
Rivera-Ingraham, G.A., Espinosa, F. and García-Gómez, J.C. (2011a) Environmentally mediated sex change in the endangered limpet Patella ferruginea (Gastropoda: Patellidae). Journal of Molluscan Studies 77, 226231.Google Scholar
Rivera-Ingraham, G.A., Espinosa, F. and García-Gómez, J.C. (2011b) Conservation status and updated census of Patella ferruginea (Gastropoda, Patellidae) in Ceuta: distribution patterns and new evidence of the effects of environmental parameters on population structure. Animal Biodiversity and Conservation 34.1, 8399.Google Scholar
Sella, G., Robotti, C.A. and Biglione, V. (1993) Genetic divergence among three sympatric species of Mediterranean Patella (Archaeogastropoda). Marine Biology 115, 401405.Google Scholar
Shanks, A.L. (1998) Apparent oceanographic triggers to the spawning of the limpet Lottia digitalis (Rathke). Journal of Experimental Marine Biology and Ecology 222, 3141.Google Scholar
Šimunović, A. (1995) Ecological study of Prosobranchiata (Gastropoda) in the eastern part of the Adriatic Sea and their relationship to benthic biocenosis. Acta Adriatica 36, 3162.Google Scholar
Sousa, L.L., Seabra, R., Wethey, D.S., Xavier, R., Queiroz, N., Zenboudji, S. and Lima, F.P. (2012) Fate of a climate-driven colonisation: demography of newly established populations of the limpet Patella rustica Linnaeus, 1758, in northern Portugal. Journal of Experimental Marine Biology and Ecology 438, 6875.Google Scholar
Sparre, P. and Venema, S.C. (1998) Introduction to tropical fish stock assessment. Part 1, Manual. FAO Fisheries Technical Paper, No. 306/1, Rev. 2, 407 pp.Google Scholar
Templado, J., Calvo, M., Garvía, A., Luque, A.A., Maldonado, M. and Moro, L. (2004) Guía de invertebrados y peces marinos protegidos por la legislación nacional e internacional. Naturaleza y Parques nacionales. Serie técnica: Organismo Autónomo Parques Nacionales (Ministerio de Medio Ambiente), 214 pp.Google Scholar
Thompson, G.B. (1979) Distribution and population dynamics of the limpet Patella aspera (Lamarck) in Bantry Bay. Journal of Experimental Marine Biology and Ecology 40, 115135.Google Scholar
Thompson, G.B. (1980) Distribution and population dynamics of the limpet Patella vulgata in Bantry Bay. Journal of Experimental Marine Biology and Ecology 45, 173217.Google Scholar
Vat, L.S. (2000) The growth and reproduction of Patella granularis (Mollusca: Patellogastropoda) on the southeast coast of South Africa. PhD thesis. Rhodes University, South Africa.Google Scholar
Zavodnik, D. and Kovačić, M. (2000) Index of marine fauna in Rijeka Bay (Adriatic Sea, Croatia). Natura Croatica 9, 297379.Google Scholar