Reproductive dynamics of the sympatric topshells Phorcus lineatus and Phorcus sauciatus (Gastropoda: Trochidae) on a rocky intertidal coast in southern Portugal
DOI:
https://doi.org/10.3989/scimar.05572.096Keywords:
trochid gastropods, intertidal rocky shore, gametogenesis, spawning season, mean gonadal index, shellfish harvesting, management measures, Atlantic OceanAbstract
The present study aimed to describe the reproductive cycle of the topshells Phorcus lineatus and Phorcus sauciatus from an intertidal rocky shore in the Algarve, southern Portugal. Based on two years of monthly sampling performed between January 2017 and December 2018, the study involved analyses of gonad histology and estimation of the mean gonadal index, aiming to investigate their relationship with environmental variables. Both topshell species are dioecious and showed synchrony in the reproductive dynamics between sexes. Indeed, the reproductive cycle of P. lineatus and P. sauciatus exhibited similar patterns, with scarcity of inactive gonads and prolonged periods with mature and spawning individuals. The gonadal index closely reflected the species’ reproductive cycle, which is apparently influenced by seasonal fluctuations in air and seawater temperatures. Additionally, some atmospheric and oceanographic conditions, such as daylight duration and wave height, were also correlated with gonad ripening and spawning of P. lineatus, and wind speed with gonad ripening and spawning of P. sauciatus. Overall, the present study provided valuable information to propose harvesting management measures aiming to ensure the sustainable exploitation of this shellfish resource, namely a closed season in the harvesting of both topshell species in September–October, covering their spawning peak in southern Portugal.
Downloads
References
Alfonso B., Sarabia A., Sancibrián I., et al. 2015. Efecto de la actividad humana sobre la distribución y estructura poblacional del burgado Phorcus sauciatus (Koch, 1845). Rev. Acad. Canar. Cienc. 27: 333-343.
Aranda D.A., Cárdenas E.B., Morales I.M., et al. 2003. A review of the reproductive patterns of gastropod mollusks from Mexico. Bull. Mar. Sci. 73(3): 629-641.
Aranda D.A., Oxenford H.A., Bissada C., et al. 2014. Reproductive patterns of queen conch, Strombus gigas (Mollusca, Gastropoda), across the Wider Caribbean Region. Bull. Mar. Sci. 90: 813-831. https://doi.org/10.5343/bms.2013.1072
Averbuj A., Bigatti G., Penchaszadeh P.E. 2010. Gametogenic cycle and size at first maturity of the Patagonic edible snail Buccinanops cochlidium from Argentina. Mar. Biol. 157: 2229-2240. https://doi.org/10.1007/s00227-010-1488-3
Ávila S.P., Madeira P., Rebelo A.C., et al. 2015. Phorcus sauciatus (Koch, 1845) (Gastropoda: Trochidae) in Santa Maria, Azores archipelago: The onset of a biological invasion. J. Mollus. Stud. 81: 516-521. https://doi.org/10.1093/mollus/eyv012
Baptista L., Santos A.M., Melo C.S., et al. 2021. Untangling the origin of the newcomer Phorcus sauciatus (Mollusca: Gastropoda) in a remote Atlantic archipelago. Mar. Biol. 168: 9. https://doi.org/10.1007/s00227-020-03808-5
Bertness M.D, Crain C.M, Silliman B.R., et al. 2006. The community structure of western Atlantic Patagonian rocky shores. Ecol. Monogr. 76: 439-60. https://doi.org/10.1890/0012-9615(2006)076[0439:TCSOWA]2.0.CO;2
Bigatti G., Marzinelli E.M., Penchaszadeh P.E. 2008. Seasonal reproduction and sexual maturity of Odontocymbiola magellanica (Neogastropoda: Volutidae). Invertebr. Biol. 127(3): 314-326. https://doi.org/10.1111/j.1744-7410.2008.00139.x
Bode A., Lombas I., Anadon N. 1986. Preliminary studies on the reproduction and population dynamics of Monodonta lineata and Gibbula umbilicalis (Mollusca, Gastropoda) on the central coast of Asturias (N. Spain). Hydrobiologia 142: 31-39. https://doi.org/10.1007/BF00026745
Boman E.M., de Graaf M., Nagelkerke L.A.J., et al. 2018. Variability in size at maturity and reproductive season of queen conch Lobatus gigas (Gastropoda: Strombidae) in the Wider Caribbean Region. Fish. Res. 201: 18-25. https://doi.org/10.1016/j.fishres.2017.12.016
Cabral J.P.S. 2020. Morphological variability of Phorcus lineatus (da Costa, 1778) shells along the coast of Portugal and the significance of the environment on shell morphology. Thalassas Int. J. Mar. Sci. 36: 9-22. https://doi.org/10.1007/s41208-019-00187-7
Collin R., Kerr K., Contolini G., et al. 2017. Reproductive cycles in tropical intertidal gastropods are timed around tidal amplitude cycles. Ecol. Evol. 7: 5977-5991. https://doi.org/10.1002/ece3.3166 PMid:28808559 PMCid:PMC5551088
Costa M.A. 2015. Distribution and shape analysis of Phorcus lineatus and Phorcus sauciatus along the Portuguese coast. MSc thesis, Univ. Lisboa, 68 pp.
Counihan R.T., McNamara D.C., Souter D.C., et al. 2001. Pattern, synchrony and predictability of spawning of the tropical abalone Haliotis asinina from Heron Reef, Australia. Mar. Ecol. Prog. Ser. 213: 193-202. https://doi.org/10.3354/meps213193
Crothers J.H. 2001. Common topshells: an introduction to the biology of Osilinus lineatus with notes on other species in the genus. Field Stud. 10: 115-160.
Cumplido M., Averbuj A., Bigatti G. 2010. Reproductive seasonality and oviposition induction in Trophon geversianus (Gastropoda: Muricidae) from Golfo Nuevo, Argentina. J. Shellfish Res. 29(2): 423-428. https://doi.org/10.2983/035.029.0219
Daguzan J. 1991. Recherches sur la croissance et l'écologie de Monodonta lineata (da Costa) Gastropoda, Prosobranchia, Trochidae) vivant sur littoral atlantique armoricain. Cah. Biol. Mar. 32: 3-22.
Desai B.N. 1966. The biology of Monodonta lineata (Da Costa). Proc. Malacol. Soc. Lond. 37: 1-17.
Di Stefano V.L., Giménez J. 2022. Gonadal morphology in the marine snail Tegula patagonica (Vetigastropoda: Tegulidae) from the intertidal area, in Patagonia, Argentina. Mar. Biodivers. 52: 6. https://doi.org/10.1007/s12526-021-01248-y
DOCAPESCA 2014. Dados relativos às vendas declaradas de caramujos nep em lota em Portugal, Docapesca, Portos e Lotas, SA, Lisboa.
D.O.G. 2012. Orden de 27 de julio de 2012. Consellería del Medio Rural y del Mar regulan los tamaños mínimos de diversos productos pesqueros en la Comunidad Autónoma de Galícia. Diario Oficial de Galícia Núm. 226, Martes, 27 de noviembre de 2012, 44545-44563 pp.
D.O.G. 2023. Orden de 21 de diciembre de 2023. Consellería del Mar aprueba el plan general de explotación marisquera para el trienio 2024-2026. Diario Oficial de Galícia Núm. 246, Viernes, 29 de diciembre de 2023, 71786-71833 pp.
Donald K.M., Preston J., Williams S.T., et al. 2012. Phylogenetic relationships elucidate colonization patterns in the intertidal grazers Osilinus Philippi, 1847 and Phorcus Risso, 1826 (Gastropoda: Trochidae) in the northeastern Atlantic Ocean and Mediterranean Sea. Mol. Phylogenet. Evol. 62(1): 35-45. https://doi.org/10.1016/j.ympev.2011.09.002 PMid:21945534
D.R. 2011. Portaria Nº 82/2011 de 22 de fevereiro que estabelece tamanhos mínimos para algumas espécies de invertebrados marinhos, aplicáveis em águas sob soberania e jurisdição nacional. Diário da República 1ª Série Nº 37: 886-887.
D.R. 2014. Portaria Nº 14/2014 de 23 de janeiro que define as artes permitidas, condicionamentos, termos do licenciamento e taxas aplicáveis ao exercício da pesca lúdica em águas oceânicas, em águas interiores marítimas ou em águas interiores não marítimas sob jurisdição da autoridade marítima. Diário da República 1ª Série Nº 16: 474-479.
Duch T.M. 1969. Spawning and development in the trochid gastropod Euchelus gemmatus (Gould, 1841) in the Hawaiian Islands. Veliger 11: 415-417.
Freije A., Al-Sayed H. 2009. Lipids and glycogen utilization in the intertidal gastropod mollusc species Turbo coronatus (Gmelin 1791). Arab Gulf J. Sci. Res. 57: 204-215.
Fretter V., Graham A. 1977. The Prosobranch Molluscs of Britain and Ireland Part 2 - Trochacea. J. Mollus. Stud. 3: 1-64.
Garwood P.R., Kendall M.A. 1985. The reproductive cycles of Monodonta lineata and Gibbula umbilicalis on the coast of Mid-Wales. J. Mar. Biol. Assoc. U.K. 65: 933-1008. https://doi.org/10.1017/S0025315400019470
Gharsallah I.H., Vasconcelos P., Zamouri-Langar N., et al. 2010. Reproductive cycle and biochemical composition of Hexaplex trunculus (Gastropoda: Muricidae) from Bizerte lagoon, northern Tunisia. Aquat. Biol. 10: 155-166. https://doi.org/10.3354/ab00275
Grange K.R. 1976. Rough water as a spawning stimulus in some trochid and turbinid gastropods. N.Z.J. Mar. Freshw. Res. 10: 203-216. https://doi.org/10.1080/00288330.1976.9515607
Gyory J., Pineda J. 2011. High-frequency observations of early-stage larval abundance: Do storms trigger synchronous larval release in Semibalanus balanoides? Mar. Biol. 158: 1581-1589. https://doi.org/10.1007/s00227-011-1671-1
Herbert D.G. 1992. Revision of the Umboniinae (Mollusca: Prosobranchia: Trochidae) in southern Africa and Mozambique. Ann. Natal Mus. 33: 379-459.
Hickman C.S., McLean J.H. 1990. Systematic revision and suprageneric classification of trochacean gastropods. Science Series of Natural History Museum of Los Angeles County, Los Angeles, 35: 1-169.
Himmelman J. H. 1999. Spawning, marine invertebrates. In: Knobil E., Neill J.D. (eds), Encyclopedia of reproduction, vol. 4. New York, Academic Press, pp. 524-533.
I.H. 2020. Dados de temperatura da água e altura da onda registados na boia oceanográfica costeira de Faro (2016-2018). Lisboa: Instituto Hidrográfico (IH).
Joll L.M. 1980. Reproductive biology of two species of Turbinidae (Mollusca: Gastropoda). Aust. J. Mar. Freshwater Res. 31: 319-336. https://doi.org/10.1071/MF9800319
Joska M.A.P., Branch G.M. 1993. The reproductive cycle of the trochid gastropod Oxystele variegata (Anton, 1839). Veliger 26: 47-51.
Kendall, M.A. 1987. The age and size structure of some northern populations of the trochid gastropod Monodonta lineata. J. Mollus. Stud. 53: 213-222. https://doi.org/10.1093/mollus/53.2.213
Kendall M.A., Williamson P., Garwood P.R. 1987. Annual variation in recruitment and population structure of Monodonta lineata and Gibbula umbilicalis populations at Aberaeron. Mid-Wales Estuar. Coast. Shelf. Sci. 24(4): 499-511. https://doi.org/10.1016/0272-7714(87)90130-2
Knox G.A. 2000. The ecology of seashores. CRC Press, Boca Raton, Florida, 576 pp. https://doi.org/10.1201/9781420042634
Lasiak T. 1987. The reproductive cycles of three trochid gastropods from the Transkei coast, southern Africa. J. Moll. Stud. 53: 24-32. https://doi.org/10.1093/mollus/53.1.24
Macedo M.C.C., Macedo M.I.C., Borges J.P. 1999. Conchas marinhas de Portugal. Editorial Verbo, Lisboa, 516 pp.
Melchior M., Clearwater S.J., Collier K.J. 2023. Reproductive phenology and the influence of temperature in two sympatric New Zealand freshwater mussel species. Mar. Freshw. Res. 74: 1478-1491. https://doi.org/10.1071/MF23072
Mieszkowska N. 2005. Changes in the biogeographic distribution of the trochidae gastropods Osilinus lineatus (da Costa) and Gibbula umbilicalis (da Costa) in response to global climate change: range dynamics and physiological mechanisms. PhD thesis, Univ. Plymouth, 188 pp. https://pearl.plymouth.ac.uk/bms-theses/124/
Mora J.P.R., Mancera-Pineda J.E., Vargas L.A.G. 2017. Population ecology of Cittarium pica (Gastropoda: Trochidae) of San Andrés Island, International Biosphere Reserve, Seaflower. Rev. Biol. Trop. 65(4): 1496-1506. https://doi.org/10.15517/rbt.v65i4.26208
Nieto-Vilela R.A., Cumplido M., Zabala S., et al. 2021. Biochemical composition during the reproductive cycle of a novel gastropod resource from Atlantic Patagonia. Mar. Freshw. Res. 73(3): 388-397. https://doi.org/10.1071/MF21208
Noke R. 2016. What is driving the range extension of Gibbula umbilicalis (Gastropoda, Trochidae) in the eastern English Channel? MSc thesis, Bournemouth Univ., UK, 84 pp.
Penchaszadeh P.E., Antelo C.S., Zabala S., et al. 2009 Reproduction and imposex in the edible snail Adelomelon ancilla from northern Patagonia, Argentina. Mar. Biol. 156: 1929-1939 https://doi.org/10.1007/s00227-009-1225-y
Perry R.I., Walters C.J., Boutillier J.A. 1999. A framework for providing scientific advice for the management of new and developing invertebrate fisheries. Rev. Fish. Biol. Fisher. 9: 125-150. https://doi.org/10.1023/A:1008946522213
R Core Team 2024. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Raffaelli D., Hawkins S.J. 1999. Intertidal ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands, 356 pp.
Ramesh R., Ravichandran S., Kumaravel K. 2010. Annual cycle of reproduction in Turbo brunneus, from Tuticorin South East Coast of India. World J. Fish Mar. Sci. 2: 14-20.
Ramírez R., Tuya F., Sánchez-Jerez P., et al. 2005. Population structure and spatial distribution of the gastropod molluscs Osilinus atrata and Osilinus sauciatus in the rocky intertidal zone of the Canary Islands (Central East Atlantic). Cienc. Mar. 31(4): 697-706. https://doi.org/10.7773/cm.v31i4.35
Romero Bastías M.S. 2014. Spawning and larval development of Tegula euryomphala (Jones, 1844) (Trochoidea: Tegulidae) from La Herradura Bay, Chile. Invertebr. Reprod. Dev. 58(4): 278-283. https://doi.org/10.1080/07924259.2014.920423
Rubal M., Veiga P., Moreira J., et al. 2014. The gastropod Phorcus sauciatus (Koch, 1845) along the north-west Iberian Peninsula: filling historical gaps. Helgol. Mar. Res. 68: 169-177. https://doi.org/10.1007/s10152-014-0379-2
Seed R. 1976. Ecology. In: Bayne B.L. (ed) Marine Mussels: Their ecology and physiology. Cambridge University Press, Cambridge pp. 13-65.
Seinor K., Purcell S.W., Malcom H., et al. 2023. Extended and spatially asynchronous reproductive periodicity in a harvested, warm-temperate rocky-reef gastropod (Turbinidae). Fish. Oceanogr. 33(1):1-12. https://doi.org/10.1111/fog.12653
Shanks A.L. 1997. Apparent oceanographic triggers to the spawning of the limpet Lottia digitalis. J. Exp. Mar. Biol. Ecol. 222: 31-42. https://doi.org/10.1016/S0022-0981(97)00135-4
Shanks A.L., Rasmuson L.K., Valley J.R., et al. 2020. Marine heat waves, climate change, and failed spawning by coastal invertebrates. Limnol. Oceanogr. 65: 627-36. https://doi.org/10.1002/lno.11331
Shin S.R., Kim H.J., Lee D.H., et al. 2020. Gonadal maturation and main spawning period of Haliotis gigantea (Gastropoda: Haliotidae). Dev. Reprod. 24: 79-88. https://doi.org/10.12717/DR.2020.24.2.79 PMid:32734125 PMCid:PMC7375981
Simpson R.D. 1977. The reproduction of some littoral molluscs from Macquarie Island (Sub-Antarctic). Mar. Biol. 44: 125-142. https://doi.org/10.1007/BF00386953
Sousa R. 2019. Key exploited species as surrogates for coastal conservation in an oceanic archipelago: Insights from topshells and limpets from Madeira (NE Atlantic Ocean). Ph.D. thesis, Univ. Madeira, 279 pp.
Sousa R., Delgado J., González J.A., et al. 2018. Marine snails of the genus Phorcus: Biology and ecology of sentinel species for human impacts on the rocky shores. In: Ray, S. (ed), Biological resources of water. IntechOpen, Rijeka. pp. 141-167. https://doi.org/10.5772/intechopen.71614
Sousa R., Vasconcelos J., Delgado J., et al. 2019. Filling biological information gaps of the marine topshell Phorcus sauciatus (Gastropoda: Trochidae) to ensure its sustainable exploitation. J. Mar. Biol. Assoc. U. K. 99: 841-849. https://doi.org/10.1017/S0025315418001054
Sousa R., Vasconcelos J., Riera R. 2020. Unravelling the effects of exploitation on the size-structure of the intertidal topshell Phorcus sauciatus in harvested and non-harvested Atlantic regions. Reg. Stud. Mar. Sci. 30: 104273. https://doi.org/10.1016/j.rsma.2020.101387
Sukhan Z.P., Cho Y., Sharker M.R., et al. 2021. Effective accumulative temperature affects gonadal maturation by controlling expression of GnRH, GnRH receptor, serotonin receptor and APGWamide gene in Pacific abalone, Haliotis discus hannai during broodstock conditioning in hatcheries. J. Therm. Biol. 100: 103037. https://doi.org/10.1016/j.jtherbio.2021.103037 PMid:34503784
Tuya F., García-Diez C., Espino F., et al. 2006. Assessment of the effectiveness of two marine reserves in the Canary Islands (eastern Atlantic). Cienc. Mar. 32(3): 505-522. https://doi.org/10.7773/cm.v32i3.1133
Underwood A.J. 1972. Observations on the reproductive cycles of Monodonta lineata, Gibbula umbilicalis and Gibbula cineraria. Mar. Biol. 17: 333-340. https://doi.org/10.1007/BF00366744
Underwood A.J. 1974a. On models for reproductive strategies in marine benthic invertebrates. Am. Nat. 108(964): 874-878. https://doi.org/10.1086/282962
Underwood A.J. 1974b. The reproductive cycles and geographical distribution of some common Eastern Australian prosobranchs (Mollusca: Gastropoda). Aust. J. Mar. Freshwater Res. 25: 63-88. https://doi.org/10.1071/MF9740063
Underwood A.J. 1979. The ecology of intertidal gastropods. Adv. Mar. Biol. 16: 111-210. https://doi.org/10.1016/S0065-2881(08)60293-X
Vasconcelos P., Lopes B., Castro M., et al. 2008. Gametogenic cycle of Hexaplex (Trunculariopsis) trunculus (Gastropoda: Muricidae) in the Ria Formosa lagoon (Algarve coast, southern Portugal). J. Mar. Biol. Assoc. U. K. 82: 321-329. https://doi.org/10.1017/S0025315408000593
Vasconcelos P., Moura P., Barroso C.M., et al. 2012. Reproductive cycle of Bolinus brandaris (Gastropoda: Muricidae) in the Ria Formosa lagoon (southern Portugal). Aquat. Biol. 16: 69-83. https://doi.org/10.3354/ab00434
Vasconcelos P., Santos A.C.N., Pereira F., et al. 2022. Shell morphology, morphometric relationships and relative growth of three topshell species (Gastropoda: Trochidae) from the Algarve coast (southern Portugal). Thalassas 38, 665-674. https://doi.org/10.1007/s41208-021-00351-y
Vélez-Arellano N., Del Próo S.G., Ordoñez E.O. 2009. Gonadal cycle of Tegula eiseni (Jordan 1936) (Mollusca: Gastropoda) in Bahia Asunción, Baja California Sur, Mexico. J. Shellfish Res. 28(3): 577-580. https://doi.org/10.2983/035.028.0321
Ward D.W., Davis A. R. 2002. Reproduction of the turban shell Turbo torquatus Gmelin 1791 (Mollusca: Gastropoda), in New South Wales, Australia. Mar. Freshw. Res. 53: 85-91. https://doi.org/10.1071/MF00066
Weather Underground 2024. "Weather History for Faro Airport Station, Faro, Portugal: Daily observations between January 2017 and December 2018." Last modified April 15, 2024. https://www.wunderground.com/history/monthly/pt/montenegro/LPFR/date/2017-1 .
Williams E.E. 1965. The growth and distribution of Monodonta lineata (da Costa) on a rocky shore in Wales. Field Stud. 2: 189-198.
Published
How to Cite
Issue
Section
License
Copyright (c) 2025 Consejo Superior de Investigaciones Científicas (CSIC)

This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the print and online versions of this journal are the property of the Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a Creative Commons Attribution 4.0 International (CC BY 4.0) licence. You may read the basic information and the legal text of the licence. The indication of the CC BY 4.0 licence must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the final version of the work produced by the publisher, is not allowed.
Funding data
European Maritime and Fisheries Fund
Grant numbers EMFF 2014-2020;MAR-01.03.02-FEAMP-0021








