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First observations of hermaphroditism in the patellid limpet Patella piperata Gould, 1846

Published online by Cambridge University Press:  18 June 2019

Ricardo Sousa ,
Paulo Henriques ,
Joana Vasconcelos ,
Graça Faria ,
Rodrigo Riera ,
Ana Rita Pinto ,
João Delgado  and
Stephen J. Hawkins
Ricardo Sousa
Affiliation:
Observatório Oceânico da Madeira, Agência Regional para o Desenvolvimento da Investigação Tecnologia e Inovação (OOM/ARDITI) – Edifício Madeira Tecnopolo, Funchal, Madeira, Portugal Direção de Serviços de Investigação (DSI) – Direção Regional das Pescas, Estrada da Pontinha, Funchal, Madeira, Portugal
Paulo Henriques
Affiliation:
Faculdade da Ciências da Vida, Universidade da Madeira, Campus da Penteada, Funchal, Madeira, Portugal
Joana Vasconcelos*
Affiliation:
Secretaria Regional de Educação, Edifício do Governo Regional, Funchal, Madeira, Portugal Departamento de Ecología, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile Centro de Ciências do Mar e do Ambiente (MARE), Quinta do Lorde Marina, Sítio da Piedade Caniçal, Madeira, Portugal
Graça Faria
Affiliation:
Direção de Serviços de Investigação (DSI) – Direção Regional das Pescas, Estrada da Pontinha, Funchal, Madeira, Portugal
Rodrigo Riera
Affiliation:
Departamento de Ecología, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile
Ana Rita Pinto
Affiliation:
Direção de Serviços de Investigação (DSI) – Direção Regional das Pescas, Estrada da Pontinha, Funchal, Madeira, Portugal
João Delgado
Affiliation:
Direção de Serviços de Investigação (DSI) – Direção Regional das Pescas, Estrada da Pontinha, Funchal, Madeira, Portugal
Stephen J. Hawkins
Affiliation:
Ocean and Earth Science, University of Southampton, National Oceanography Centre Southampton, Southampton S014 3ZH, UK The Marine Biological Association of the UK, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK
*
Author for correspondence: Joana Vasconcelos, E-mail: joana.pr.vasconcelos@madeira.gov.pt
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Abstract

Hermaphroditism is thought to be an advantageous strategy common in marine molluscs that exhibit simultaneous, sequential or alternating hermaphroditism. Several species of patellid limpets have previously been shown to be protandrous hermaphrodites. The present study aimed to confirm whether this phenomenon occurs in Patella piperata. Transitional forms of simultaneous protandrous hermaphroditism were found in intermediate size classes of P. piperata, in Madeira (North-eastern Atlantic). Sequential hermaphroditism was confirmed after histological analysis. The overall sex-ratio was biased towards females but approached similar proportions in the larger size classes. Analysis of size at sex change showed that at a shell length of 36 mm 50% of the population probably have changed sex. The results reported confirm the occurrence of sequential hermaphroditism. These findings are of utmost importance to the understanding of the reproductive biology of this species with direct effect on management and conservation of this traditionally harvested limpet.

Keywords

Atlantic OceanintertidalMadeiraMolluscaPatellogastropodasex change
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 7 , November 2019 , pp. 1615 - 1620
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

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References

Allsop, DJ and West, SA (2003) Constant relative age and size at sex change in sequentially hermaphroditic fish. Journal of Evolutionary Biology 16, 921–929. https://doi.org/10.1046/j.1420-9101.2003.00590.x.Google Scholar
Allsop, DJ and West, SA (2004) Sex-ratio evolution in sex-changing animals. Evolution 58, 1019–1027.Google Scholar
Bacci, G (1947) L'inversione del sesso ed il ciclo stagionale della gonade in Patella coerulea L [Sex reversal and seasonal cycle of the gonad in Patella coerulea L]. Pubblicazioni della Stazione Zoologica di Napoli 21, 183–217.Google Scholar
Bergasa, O, Ramírez, R, Collado, C, Hernández, J, Gelado-Caballero, M, Haroun, R and Rodriguez, M (2007) Study of metals concentration levels in Patella piperata throughout the Canary Islands, Spain. Environmental Monitoring and Assessment 127, 127–133. https://doi.org/10.1007/s10661-006-9266-x.Google Scholar
Borges, CDG, Doncaster, CP, Maclean, MA and Hawkins, SJ (2015) Broad-scale patterns of sex ratios in Patella spp.: a comparison of range edge and central range populations in the British Isles and Portugal. Journal of the Marine Biological Association of the United Kingdom 95, 1141–1153. http://dx.doi.org/10.1017/S0025315415000417.Google Scholar
Boukhicha, J, Kalthoum, O, Hassine, B and Tlig-Zouari, S (2013) Morphological evidence for adaptive diversification of sympatric Mediterranean Patella limpets. Rapport Commission International Mer Méditerranée 40, 686.Google Scholar
Bowman, RS and Lewis, JR (1986) Geographical variation in the breeding cycles and recruitment of Patella spp. Hydrobiologia 142, 41–56. https://doi.org/10.1007/BF00026746.Google Scholar
Branch, GM (1974) Ecology of Patella Linnaeus from Cape Peninsula, South Africa. 2. Reproductive cycles. Transactions of the Royal Society of South Africa 41, 111–160. https://doi.org/10.1080/00359197409520068.Google Scholar
Branch, GM (1981) The biology of limpets: physical factors, energy flow and ecological interactions. Oceanography and Marine Biology – An Annual Review 19, 235–380.Google Scholar
Charnov, EL (1979) Natural selection and sex change in Pandalid shrimp: test of a life history theory. American Naturalist 113, 715–734.Google Scholar
Christiaens, J (1973) Révision du genre Patella (Mollusca, Gastropoda). Bulletin du Muséum National d'Histoire Naturelle 3, 1305–1392.Google Scholar
Côrte-Real, HBSM, Hawkins, S and Thorpe, JP (1996) An interpretation of the taxonomic relationship between the limpets Patella rustica and P. piperata. Journal of the Marine Biological Association of the United Kingdom 76, 717–732. https://doi.org/10.1017/S0025315400031416.Google Scholar
Creese, RG (1980) Reproductive cycles and fecundities of four common eastern Australian archaeogastropod limpets. Australian Journal of Marine and Freshwater Research 31, 49–59.Google Scholar
Creese, RG, Schiel, DR and Kingsford, MJ (1990) Sex change in a giant endemic limpet Patella kermadecensis, from the Kermedec Islands. Marine Biology 104, 419–426.Google Scholar
Cunha, L, Martins, GM, Amaral, A and Rodrigues, A (2007) A case of simultaneous hermaphroditism in the Azorean endemic limpet Patella candei gomesii (Mollusca: Patellogastropoda), a gonochoristic species. Invertebrate Reproduction and Development 50, 203–205. https://doi.org/10.1080/07924259.2007.9652247.Google Scholar
Davies, PS (1969) Effect of environment on metabolic activity and morphology of Mediterranean and British species of Patella. Pubblicazioni della Stazione Zoologica di Napoli 37, 641–656.Google Scholar
Dodd, JM (1956) Studies on the biology of limpets: III. Hermaphroditism in the three British species of Patella. Journal of the Marine Biological Association of the United Kingdom 2, 327–340. https://doi.org/10.1017/S002531540001016X.Google Scholar
Espinosa, F, Guerra-García, JM, Fa, D and García-Gómez, JC (2006) Aspects of reproduction and their implications for the conservation of the endangered limpet, Patella ferruginea. Invertebrate Reproduction and Development 49, 85–92.Google Scholar
Espinosa, F, Guerra-García, JM, Fa, D and García-Gómez, JC (2009) Gonochorism or protandrous hermaphroditism? Evidence of sex change in the endangered limpet Patella ferruginea. Marine Biology Research 2, e153. https://doi.org/10.1017/S1755267209990790.Google Scholar
Fenberg, PB and Roy, B (2008) Ecological and evolutionary consequences of size-selective harvesting: how much do we know? Molecular Ecology 17, 209–220. https://doi.org/10.1111/j.1365-294X.2007.03522.x.Google Scholar
Firth, LB, Grant, LM, Crowe, TP, Ellis, JS, Wiler, C, Convery, C and O'Connor, NE (2017) Factors affecting the prevalence of the trematode parasite Echinostephilla patellae (Lebour, 1911) in the limpet Patella vulgata (L.). Journal of Experimental Marine Biology and Ecology 492, 99–104. https://doi.org/10.1016/j.jembe.2017.01.026.Google Scholar
Fretter, V, Graham, A, Ponder, WF and Lindberg, DR (1998) Prosobranchia Introduction. In Beesley, PL, Ross, GJB and Wells, A (eds) Mollusca, the Southern Synthesis. Part B. Fauna of Australia, vol. 5. Melbourne: CSIRO, pp. 605–638.Google Scholar
Ghiselin, MT (1987) Evolutionary aspects of marine invertebrate reproduction. In Giese, AC, Pearse, JS and Pearse, VB (eds) Reproduction of Marine Invertebrates, vol. 9. Palo Alto, California: Blackwell Scientific Publications, pp. 609–666.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 & Development 57, 247–253. https://doi.org/10.1080/07924259.2012.754794.Google Scholar
Guerra, MT and Gaudêncio, MJ (1986) Aspects of the ecology of Patella spp. on the Portuguese coast. Hydrobiologia 142, 57–69.Google Scholar
Harley, CDG, Denny, MW, Mach, KJ and Miller, LP (2009) Thermal stress and morphological adaptations in limpets. Functional Ecology 23, 292–301. https://doi.org/10.1111/j.1365-2435.2008.01496.x.Google Scholar
Heller, J (1993) Hermaphroditism in molluscs. Biology Journal of Linnean Society 48, 19–42. https://doi.org/10.1111/j.1095-8312.1993.tb00874.x.Google Scholar
Henninger, TO and Hodgson, AN (2001) The reproductive cycle of Helcion pruinosus (Patellogastropoda) on two South African boulder shores. Journal of Molluscan Studies 67, 385–394. https://doi.org/10.1093/mollus/67.3.385.Google Scholar
Henriques, P, Delgado, J and Sousa, R (2017) Patellid limpets: an overview of the biology and conservation of keystone species of the rocky shores. In Ray, S (ed.) Organismal and Molecular Malacology. Croatia: Intech, pp. 71–95. https://doi.org/10.5772/67862.Google Scholar
Hoagland, KE (1978) Protandry and evolution of environmentally mediated sex change: a study of the Mollusca. Malacologia 17, 365–391.Google Scholar
Hoagland, KE (1984) Use of terms protandry, protogyny, and hermaphroditism in malacology. American Malacological Bulletin 3, 85–88.Google Scholar
IBM Corp. (2016) IBM SPSS Statistics for Windows. Version 24.0. Armonk, NY: IBM Corp.Google Scholar
Le Quesne, WJF and Hawkins, SJ (2006) Direct observations of protandrous sex change in the patellid limpet Patella vulgata. Journal of the Marine Biological Association of the United Kingdom 86, 161–162. https://doi.org/10.1017/S0025315406012975.Google Scholar
Lewis, JR (1986) Latitudinal trends in reproduction, recruitment and population characteristics of some rocky littoral molluscs and cirripedes. Hydrobiologia 142, 1–13. https://doi.org/10.1007/BF00026742.Google Scholar
Lindberg, DR (2007) Reproduction, ecology, and evolution of the Indo-pacific limpet Scutellastra flexuosa. Bulletin of Marine Science 81, 219–234.Google Scholar
Martins, GM, Borges, CDG, Vale, M, Ribeiro, PA, Ferraz, RR, Martins, HR, Santos, RS and Hawkins, SJ (2017) Exploitation promotes earlier sex changes in a protandrous patellid limpet, Patella aspera Röding, 1798. Ecology and Evolution 7, 3616–3622. https://doi.org/10.1002-ecs3.2925.Google Scholar
Mau, A, Fox, K and Bingham, JP (2017) The reported occurrence of hermaphroditism in the yellowfoot limpet (Cellana sandwicensis Pease, 1981). Annals of Aquaculture and Research 4, 1045.Google Scholar
Montalenti, G (1958) Perspectives of research on sex problems in marine organisms. In Buzzati-Travesso, AA (ed.) Perspectives in Marine Biology. Berkeley, CA: University of California Press, pp. 589–602.Google Scholar
Moore, PJ, Thompson, RC and Hawkins, SJ (2011) Phenological changes in intertidal con-specific gastropods in response to climate warming. Global Change Biology 17, 709–719. https://doi.org/10.1111/j.1365-2486.2010.02270.x.Google Scholar
Moro, L and Herrera, R (2000) Las lapas, un recurso en extinción. Revista de Medio Ambiente – Gobierno de Canarias 16, 1–3.Google Scholar
Munday, PL, Buston, PM and Warner, RR (2006) Diversity and flexibility of sex-change strategies in animals. Trends in Ecology and Evolution 21, 89–95. https://doi.org/10.1016/j.tree.2005.10.020.Google Scholar
Orton, JH (1919) Sex-phenomena in the common limpet (Patella vulgata). Nature 104, 374. https://doi.org/10.1038/104373a0.Google Scholar
Orton, JH (1928) Observations on Patella vulgata. Part I. Sex phenomena, breeding and shell-growth. Journal of the Marine Biological Association of the United Kingdom 15, 851–862.Google Scholar
Orton, JH and Southward, AJ (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, 653–662.Google Scholar
Orton, JH, Southward, AJ and Dodd, JM (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, 149–176. https://doi.org/10.1017/S0025315400009036.Google Scholar
Pal, P and Hodgson, AN (2005) Reproductive seasonality and simultaneous hermaphroditism in two species of Siphonaria (Gastropoda: Pulmonata) from the southeast coast of South Africa. Journal of Molluscan Studies 71, 33–40. https://doi.org/10.1093/mollus/eyi003.Google Scholar
Prusina, I, Ezgeta-balic, D, Ljubimir, S, Dobroslavic, T and Glamuzina, B (2014) On the reproduction of the Mediterranean keystone limpet Patella rustica: histological overview. Journal of the Marine Biological Association of the United Kingdom 94, 1651–1660. https://doi.org/10.1017/S0025315414000976.Google Scholar
Rivera-Ingraham, GA, Espinosa, F and García-Gómez, JC (2011) Environmentally mediated sex change in the endangered limpet Patella ferruginea (Gastropoda: Patellidae). Journal of Molluscan Studies 77, 226–231. https://doi.org/10.1093/mollus/eyr007.Google Scholar
Sá-Pinto, A, Branco, M, Harris, J and Alexandrino, P (2005) Phylogeny and phylogeography of the genus Patella based on mitochondrial DNA sequence data. Journal of Experimental Marine Biology and Ecology 325, 95–110.Google Scholar
Sousa, R, Delgado, J, Pinto, AR and Henriques, P (2017) Growth and reproduction of the northeastern Atlantic keystone species Patella aspera (Mollusca: Patellogastropoda). Helgoland Marine Research 71, 1–13. https://doi.org/10.1186/s10152-017-0488-9.Google Scholar
Thompson, GB (1979) Distribution and population – dynamics of the limpet Patella aspera (Lamarck) in Bantry Bay. Journal of Experimental Marine Biology and Ecology 40, 115–135. https://doi.org/10.1016/0022-0981(79)90039-X.Google Scholar
Vasconcelos, J (2017). Estrutura Populacional do Chicharro, Trachurus picturatus do Atlântico Nordeste (PhD thesis). University of Madeira, Funchal, Portugal.Google Scholar
Warner, RR (1988) Sex change and size-advantage model. Trends in Ecology and Evolution 3, 133–136. https://doi.org/10.1016/0169-5347(88)90176-0.Google Scholar
Warner, RR, Fitch, DL and Standish, JD (1996) Social control of sex change in the shelf limpet, Crepidula norrisiarum: size-specific responses to local group composition. Journal of Experimental Marine Biology and Ecology 204, 155–167. https://doi.org/10.1016/0022-0981(96)02582-8.Google Scholar
WoRMS (2018). World Register of Marine Species. http://www.marinespecies.org.Google Scholar
Wright, WG (1989). Intraspecific density mediates sex-change in the territorial patellacean limpet Lottia gigantea. Marine Biology 100, 353–364. https://doi.org/10.1007/BF00391151.Google Scholar