Skip to main content

Reproductive cycle of the Manila clam (Ruditapes philippinarum): an intensively harvested invasive species in the Tagus Estuary (Portugal)

  • Paula Moura (a1), Paulo Vasconcelos (a1) (a2), Fábio Pereira (a1), Paula Chainho (a3), José Lino Costa (a3) (a4) and Miguel B. Gaspar (a1) (a5)...

The present study aimed to describe the reproductive cycle and estimate the size at sexual maturity of the Manila clam (Ruditapes philippinarum) in the Tagus Estuary (Portugal). Specimens were collected monthly from September 2013 to December 2015 during fishing surveys using bivalve dredges. The gametogenic cycle was described in detail using gonad histology and monitored throughout the study period by the monthly variation in the frequency of gonad maturation stages, mean gonadal index and mean oocyte diameter. This invasive population of R. philippinarum displayed synchronous gonadal development between sexes, with ripening occurring mainly in April and May followed by an extensive spawning period until November–December. Individuals reached the size at first sexual maturity at 29.4 mm in shell length (i.e. before 1 year old). Furthermore, the reproductive strategy, dynamics and potential were compared between the invasive R. philippinarum and the native congeneric carpet shell clam (Ruditapes decussatus). Overall, the data gathered in this study constitutes valuable baseline information to propose conservation strategies and implement management measures to minimize the harmful impacts caused by this invasive species on local ecosystems and native biodiversity, particularly over populations of autochthonous bivalves.

Corresponding author
Correspondence should be addressed to: M.B. Gaspar, Instituto Português do Mar e da Atmosfera (IPMA), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal email:
Hide All
Angert, A.L., Crozier, L.G., Rissler, L.J., Gilman, S.E., Tewksbury, J.J. and Chunco, A.J. (2011) Do species traits predict recent shifts at expanding range edges? Ecology Letters 14, 677689.
Anon. (2001) Especies de interés pesquero en el litoral de Andalucía. Vol. II – Invertebrados. Seville: Junta de Andalucía, Consejería de Agricultura y Pesca.
Banha, M. (1984) Aspectos da biologia (crescimento e reprodução) de Ruditapes decussatus Lineu, 1789 (Mollusca, Bivalvia) na Ria Formosa-Algarve. Lisbon: Relatório de estágio de licenciatura em Biologia, Faculdade de Ciências de Lisboa.
Bidegain, G., Bárcena, J.F., García, A. and Juanes, J.A. (2015) Predicting coexistence and predominance patterns between the introduced Manila clam (Ruditapes philippinarum) and the European native clam (Ruditapes decussatus). Estuarine, Coastal and Shelf Science 152, 162172.
Breber, P. (1980) Annual gonadal cycle in the carpet-shell clam Venerupis decussata in Venice Lagoon, Italy. Proceedings of the National Shellfisheries Association 70, 3135.
Breber, P. (1985) On-growing of the carpet-shell clam (Tapes decussatus (L.)): two years’ experience in Venice Lagoon. Aquaculture 44, 5156.
Cabral, H.N., Costa, M.J. and Salgado, J.P. (2001) Does the Tagus estuary fish community reflect environmental changes? Climate Research 18, 119126.
Caçador, I., Vale, C. and Catarino, F. (1996) Accumulation of Zn, Pb, Cu and Ni in sediments between roots of the Tagus estuary salt marshes, Portugal. Estuarine, Coastal and Shelf Science 42, 393403.
Caldow, R., McGrorty, S., West, A., leV. dit Durell, S.E.A., Stillman, R. and Anderson, S. (2005) Macro-invertebrate fauna in the intertidal mudflats. In Humphreys, J. and May, V. (eds) The ecology of Poole Harbour. Amsterdam: Elsevier, pp. 91108.
Carvalho, F. (2017) Current status and impacts of the Manila clam (Ruditapes philippinarum) population in the Tagus estuary. MSc thesis. Faculty of Sciences, University of Lisbon, Portugal.
Chainho, P. (2014) Report of the working group on introduction and transfers of marine organisms (WGITMO). ICES CM 2014/ACOM: 32, 259 pp.
Chainho, P., Fernandes, A., Amorim, A., Avila, S., Canning-Clode, J., Castro, J.J., Costa, A.C., Costa, J.L., Cruz, T., Gollasch, S., Grazziotin-Soares, C., Melo, R., Micael, J., Parente, M.I., Semedo, J., Silva, T., Sobral, D., Sousa, M., Torres, P., Veloso, V. and Costa, M.J. (2015) Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands. Estuarine, Coastal and Shelf Science 167, 199211.
Choi, K.H., Park, G.M. and Chung, E.Y. (2005) Ovarian maturation in female Ruditapes philippinarum on the west coast of Korea. Development and Reproduction 9, 123134.
Chung, E.Y., Chung, J.S. and Lee, K.Y. (2013) Gametogenic cycle, the spawning season, first sexual maturity, and the biological minimum size in male Ruditapes philippinarum (Bivalvia: Veneridae) in Western Korea. Journal of Life Sciences 7, 613622.
Chung, E.Y., Hur, S.B., Hur, Y.-B. and Lee, J.S. (2001) Gonad maturation and artificial spawning of the Manila clam, Ruditapes philippinarum (Bivalvia: Veneridae) in Komso Bay, Korea. Journal of Fisheries Science and Technology 4, 208218.
Chung, E.Y., Ryou, D.K. and Lee, J.H. (1994) Gonadal development, age and growth of the short necked clam, Ruditapes philippinarum (Pelecypoda: Veneridae), on the coast of Kimje, Korea. Korean Journal of Malacology 10, 3854.
Çolakoğlu, S. and Palaz, M. (2014) Some population parameters of Ruditapes philippinarum (Bivalvia, Veneridae) on the southern coast of the Marmara Sea, Turkey. Helgoland Marine Research 68, 539548.
Copp, G.H., Vilizzi, L., Tidbury, H., Stebbing, P.D., Tarkan, A.S., Miossec, L. and Goulletquer, P. (2016) Development of a generic decision-support tool for identifying potentially invasive aquatic taxa: AS-ISK. Management of Biological Invasions 7, 343350.
Cordero, D., Delgado, M., Liu, B., Ruesink, J. and Saavedra, C. (2017) Population genetics of the Manila clam (Ruditapes philippinarum) introduced in North America and Europe. Scientific Reports 7, 39745.
Cotter, J.C., Pereira, T.J., Costa, M.J. and Costa, J.L. (2013) Distribution, abundance, population structure and activity of Halobatrachus didactylus in the Tagus estuary (Portugal) and adjacent coastal waters. Journal of the Marine Biological Association of the United Kingdom 93, 405412.
Dang, C., de Montaudouin, X., Gam, M., Paroissin, C., Bru, N. and Caill-Milly, N. (2010) The Manila clam population in Arcachon Bay (SW France): can it be kept sustainable? Journal of Sea Research 63, 108118.
Delgado, M. and Pérez-Camacho, A. (2007) Comparative study of gonadal development of Ruditapes philippinarum (Adams and Reeve) and Ruditapes decussatus (L.) (Mollusca: Bivalvia): influence of temperature. Scientia Marina 71, 471484.
Delgado, M., Silva, L. and Juárez, A. (2013) Aspects of reproduction of striped venus Chamelea gallina in the Gulf of Cádiz (SW Spain): implications for fishery management. Fisheries Research 146, 8695.
de Montaudouin, X., Lucia, M., Binias, C., Lassudrie, M., Baudrimont, M., Legeay, A., Raymond, N., Jude-Lemeilleur, F., Lambert, C., Le Goïc, N., Garabetian, F., Gonzalez, P., Hégaret, H., Lassus, P., Mehdioub, W., Bourasseau, L., Daffe, G., Paul-Pont, I., Plus, M., Do, V.T., Meisterhans, G., Mesmer-Dudons, N., Caill-Milly, N., Sanchez, F. and Soudant, P. (2016) Why is Asari (=Manila) clam Ruditapes philippinarum fitness poor in Arcachon Bay: meta-analysis to answer? Estuarine, Coastal and Shelf Science 179, 226235.
DeRivera, C.E., Ruiz, G.M., Hines, A.H. and Jivoff, P. (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86, 33643376.
Drummond, L., Mulcahy, M. and Culloty, S. (2006) The reproductive biology of the Manila clam, Ruditapes philippinarum, from the north-west of Ireland. Aquaculture 254, 326340.
França, S., Vinagre, C., Caçador, I. and Cabral, H.N. (2005) Heavy metal concentrations in sediment, benthic invertebrates and fish in three salt marsh areas subjected to different pollution loads in the Tagus Estuary (Portugal). Marine Pollution Bulletin 50, 9931018.
Gaspar, M.B. (2010) Distribuição, abundância e estrutura demográfica da amêijoa-japonesa (Ruditapes philippinarum) no Rio Tejo. Relatório do IPIMAR, Lisbon, 6 pp.
Gaspar, M.B., Chainho, P. and Costa, J.L. (2014) Distribuição, abundância e estrutura demográfica da amêijoa-japonesa (Ruditapes philippinarum) no Rio Tejo. Lisbon: Relatório de campanha de pesca, 18 pp.
Gaspar, M.B. and Monteiro, C.C. (1998) Reproductive cycles of the razor clam Ensis siliqua and the clam Venus striatula off Vilamoura, southern Portugal. Journal of the Marine Biological Association of the United Kingdom 78, 12471258.
Genez, P., Önal, U. and Gezen, M.R. (2015) Comparison of gametogenic cycles of the endemic European carpet shell clam (Ruditapes decussatus) and the introduced Manila clam (Ruditapes philippinarum) from a temperate coastal Mediterranean lagoon in the Dardanelles, Turkey. Journal of Shellfish Research 34, 337345.
Goulletquer, P. (1997) A bibliography of the Manila clam Tapes philippinarum. IFREMER, RIDRV-97.02/RA/LA. La Tremblade: IFREMER, 122 pp.
Goulletquer, P. (2015) Ruditapes philippinarum (Adams & Reeve, 1850). In FAO (ed.) Cultured aquatic species information programme, 2005–2015. Rome: FAO Fisheries and Aquaculture Department.
Goulletquer, P. and Héral, M. (1997) Marine molluscan production trends in France: from fisheries to aquaculture. NOAA Technical Report NMFS, 129, pp. 137–164.
Gozler, A.M. and Tartan, A.N. (2000) Reproductive biology of Ruditapes decussatus (Linnaeus, 1758) in Çardak Lagoon, Dardanelles Strait. Turkish Journal of Marine Sciences 6, 175198.
Harding, J.M., Mann, R. and Kilduff, C.W. (2008) Influence of environmental factors and female size on reproductive output in an invasive temperate marine gastropod Rapana venosa (Muricidae). Marine Biology 155, 571581.
Hesselman, L.D., Barber, B.J. and Blake, N.J. (1989) The reproductive cycle of adult hard clam, Mercenaria spp. in the Indian River Lagoon, Florida. Journal of Shellfish Research 8, 4349.
Holland, D.A. and Chew, K.K. (1974) Reproductive cycle of the Manila clam (Venerupis japonica) from Hood Canal, Washington. Proceedings of the National Shellfisheries Association 64, 5358.
Hotchkiss, A.K., Sternberg, R.M. and LeBlanc, G.A. (2008) Environmental cues trigger seasonal regression of primary and accessory sex organs of the mud snail, Ilyanassa obsoleta. Journal of Molluscan Studies 74, 301303.
Humphreys, J., Richard, W., Caldow, G., McGrorty, S., West, A.D. and Jensen, A.C. (2007) Population dynamics of naturalized Manila clams Ruditapes philippinarum in British coastal waters. Marine Biology 151, 22552270.
ICES (2008) Report of the working group on introductions and transfers of marine organisms (WGITMO). ICES CM 2008/ACOM 52, 130 pp.
Jensen, A., Humphreys, J., Caldow, R. and Cesar, C. (2005) The Manila clam in Poole Harbour. In Humphreys, J. and May, V. (eds) The ecology of Poole Harbour. Amsterdam: Elsevier, pp. 163173.
Jensen, A.C., Humphreys, J., Caldow, R.W.G., Grisley, C. and Dyrynda, P.E.J. (2004) Naturalization of the Manila clam (Tapes philippinarum), an alien species, and establishment of a clam fishery within Poole Harbour, Dorset. Journal of the Marine Biological Association of the United Kingdom 84, 10691073.
Joaquim, S., Matias, D., Matias, A.M., Moura, P., Arnold, W.S., Chícharo, L. and Gaspar, M.B. (2011) Reproductive activity and biochemical composition of the pullet carpet shell Venerupis senegalensis (Gmelin, 1791) (Mollusca: Bivalvia) from Ria de Aveiro (northwestern coast of Portugal). Scientia Marina 75, 217226.
Juanes, J.A., Bidegain, G., Echavarri-Erasun, B., Puente, A., García, A., García, A., Bárcena, J.F., Álvarez, C. and García-Castillo, G. (2012) Differential distribution pattern of native Ruditapes decussatus and introduced Ruditapes phillippinarum clam populations in the Bay of Santander (Gulf of Biscay): considerations for fisheries management. Ocean and Coastal Management 69, 316326.
King, M. (1995) Fisheries biology, assessment and management. Oxford: Fishing News Books.
Kolar, C.S. and Lodge, D.M. (2001) Progress in invasion biology: predicting invaders. Trends in Ecology and Evolution 16, 199204.
Langston, W.J., Chesman, B.S., Burt, G.R., Hawkins, S.J., Readman, J. and Worsfold, P. (2003) Characterisation of the south west European marine sites: Poole Harbour SPA. Occasional Publication no. 12. Plymouth: Marine Biological Association of the United Kingdom, 163 pp.
Laruelle, F., Guillou, J. and Paulet, Y.M. (1994) Reproductive pattern of the clams, Ruditapes decussatus and R. philippinarum on intertidal flats in Brittany. Journal of the Marine Biological Association of the United Kingdom 74, 351366.
Machado, D.T.S. (2015a) Reproductive cycle of the population of European clam, Ruditapes decussatus, from Lagoa de Óbidos, Leiria, Portugal. MSc thesis in Aquaculture. Escola Superior de Turismo e Tecnologia do Mar, Instituto Politécnico de Leiria, Portugal.
Machado, M. (2015b) Effects of the non-indigenous bivalve Ruditapes philippinarum on meiofaunal communities of the Tagus estuary. MSc thesis in Conservation Biology. Department of Biology, University of Évora, Portugal.
Maia, F. and Gaspar, M.B. (2014) Case study – clam harvesting in the Ria de Aveiro. Biology and management of bivalve harvesting in Ria de Aveiro. GEPETO Report, 23 pp.
Mann, R. (1979) Some biochemical and physiological aspects of growth and gametogenesis in Crasssotrea gigas and Ostrea edulis grown at sustained elevated temperatures. Journal of the Marine Biological Association of the United Kingdom 59, 95110.
Matias, D., Joaquim, S., Matias, A.M., Moura, P., Teixeira de Sousa, J., Sobral, P. and Leitão, A. (2013) The reproductive cycle of the European clam Ruditapes decussatus (L., 1758) in two Portuguese populations: implications for management and aquaculture programs. Aquaculture 406/407, 5261.
Meneghetti, F., Moschino, V. and Da Ros, L. (2004) Gametogenic cycle and variations in oocyte size of Tapes philippinarum form Lagoon of Venice. Aquaculture 240, 473488.
Moschino, V., Delaney, E. and Da Ros, L. (2012) Assessing the significance of Ruditapes philippinarum as a sentinel for sediment pollution: bioaccumulation and biomarker responses. Environmental Pollution 171, 5260.
Moura, P., Garaulet, L.L., Vasconcelos, P., Chainho, P., Costa, J.L. and Gaspar, M.B. (2017) Age and growth of a highly successful invasive species: the Manila clam Ruditapes philippinarum (Adams & Reeve, 1850) in the Tagus Estuary (Portugal). Aquatic Invasions 12, 133146.
Moura, P., Gaspar, M.B. and Monteiro, C.C. (2008) Gametogenic cycle of the smooth clam Callista chione on the south-western coast of Portugal. Journal of the Marine Biological Association of the United Kingdom 88, 161167.
Occhipinti-Ambrogi, A. (2000) Biotic invasions in a Mediterranean lagoon. Biological Invasions 2, 165176.
Ohba, S. (1959) Ecological studies in the natural population of a clam, Tapes japonica, with special reference to seasonal variations in the size and structure of the population and to individual growth. Biological Journal of Okayama University 5, 1343.
Ojea, J., Martínez, D., Novoa, S. and Cerviño-Otero, A. (2005) Ciclo gametogénico de una población de almeja japonesa Ruditapes philippinarum (Adams & Reeve, 1850) en la ría de Camariñas (noroeste de España) y relación con la composición bioquímica mayoritaria. Boletín del Instituto Español de Oceanografía 21, 337342.
Ojea, J., Pazos, A.J., Martínez, D., Novoa, S., Sánchez, J.L. and Abad, M. (2004) Seasonal variation in weight and biochemical composition of the tissues of Ruditapes decussatus in relation to the gametogenic cycle. Aquaculture 238, 451468.
Otero, M., Cebrian, E., Francour, P., Galil, B. and Savini, D. (2013) Monitoring marine invasive species in Mediterranean Marine Protected Areas (MPAs): a strategy and practical guide for managers. Malaga: IUCN.
Paesanti, F. and Pellizzato, M. (2000) Tapes philippinarum. Manuale di divulgazione. Serie acquacoltura. Padova: Veneto Agricoltura.
Pellizzato, M. and Da Ros, L. (2005) Clam farming quality as a management tool: a proposal based on recent studies in Northern Adriatic lagoons. Aquaculture International 13, 5766.
Ponurovsky, S.K. and Yakovlev, Y.M. (1992) The reproductive biology of the Japanese littleneck, Tapes philippinarum (Adams and Reeve, 1850) (Bivalvia: Veneridae). Journal of Shellfish Research 11, 265277.
Pranovi, F., Franceschini, G., Casale, M., Zucchetta, M., Torricelli, P. and Giovanardi, O. (2006) An ecological imbalance induced by a non-native species: the Manila clam in the Venice Lagoon. Biological Invasions 8, 595609.
Ramajal, J., Picard, D., Costa, J.L., Carvalho, F.B., Gaspar, M.B. and Chainho, P. (2016) Amêijoa-japonesa, uma nova realidade no estuário do Rio Tejo: pesca e pressão social versus impacto ambiental. In Cancela da Fonseca, L., Garcia, A.C., Pereira, S.D. and Rodrigues, M.A.C. (eds) Entre Rios e Mares: um Património de Ambientes, História e Saberes. Tomo V. Rio de Janeiro: Rede BrasPor, pp. 1730.
Rodríguez-Moscoso, E. and Arnaíz, R. (1998) Gametogenesis and energy storage in a population of the grooved carpet-shell clam, Tapes decussatus (Linne, 1787) in northwest Spain. Aquaculture 162, 125139.
Rodríguez-Moscoso, E., Pazo, J.P., García, A. and Fernández-Cortés, F. (1992) Reproductive cycle of Manila clam Ruditapes philippinarum (Adams & Reeve, 1850) in Ria of Vigo (NW Spain). Scientia Marina 56, 6167.
Ruiz, G.M., Carlton, J.T., Grosholz, E.D. and Hines, A.H. (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. American Zoologist 37, 621632.
Sarasquete, M.C., Gimeno, S. and Gonzalez de Canales, M.L. (1990) Cycle reproducteur de la palourde Ruditapes philippinarum (Adams & Reeve, 1850) de la côte sud ouest atlantique (Espagne). Revue Internationale d'Océanographie Médicale 97, 9099.
Sastry, A.N. (1975) Pelecypoda (excluding Ostreidae). In Giese, A.C. and Pearse, J.S. (eds) Reproduction of marine invertebrates. New York, NY: Academic Press, pp. 113292.
Savini, D., Occhipinti-Ambrogi, A., Marchini, A., Tricarico, E., Gherardi, F., Olenin, S. and Gollasch, S. (2010) The top 27 animal alien species introduced into Europe for aquaculture and related activities. Journal of Applied Ichthyology 26, 17.
Seed, R. (1976) Ecology. In Bayne, B.L. (ed.) Marine mussels: their ecology and physiology. Cambridge: Cambridge University Press, pp. 1365.
Serdar, S. and Lök, A. (2009) Gametogenic cycle and biochemical composition of the transplanted carpet shell clam tapes decussatus, Linnaeus 1758 in Sufa (Homa) Lagoon, Izmir, Turkey. Aquaculture 293, 8188.
Sorokin, Y.I. and Giovanardi, O. (1995) Trophic characteristics of the Manila clam (Ruditapes philippinarum Adams & Reeve, 1850). ICES Journal of Marine Science 52, 835862.
Sousa, R., Gutiérrez, J.L. and Aldridge, D.C. (2009) Non-indigenous invasive bivalves as ecosystem engineers. Biological Invasions 11, 23672385.
Sternberg, R.M., Gooding, M.P., Hotchkiss, A.K. and Leblanc, G.A. (2010) Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin-induced imposex in prosobranchs. Ecotoxicology 19, 423.
Thatje, S., Lovrich, G.A. and Anger, K. (2004) Egg production, hatching rates, and abbreviated larval development of Campylonotus vegans Bate, 1888 (Crustacea: Decapoda: Caridea), in subantarctic waters. Journal of Experimental Marine Biology and Ecology 301, 1527.
Thorsen, A., Witthames, P.R., Marteinsdóttir, G., Nash, R.D.M. and Kjesbu, O.S. (2010) Fecundity and growth of Atlantic cod (Gadus morhua L.) along a latitudinal gradient. Fisheries Research 104, 4555.
Velez, C., Figueira, E., Soares, A. and Freitas, R. (2015a) Spatial distribution and bioaccumulation patterns in three clam populations from a low contaminated ecosystem. Estuarine, Coastal and Shelf Science 155, 114125.
Velez, C., Leandro, S., Figueira, E., Soares, A. and Freitas, R. (2015b) Biochemical performance of native and introduced clam species living in sympatry: the role of elements accumulation and partitioning. Marine Environmental Research 109, 8194.
Ward, P. and Hirst, A.G. (2007) Oithona similis in a high latitude ecosystem: abundance, distribution and temperature limitation of fecundity rates in a sac spawning copepod. Marine Biology 151, 10991110.
Wayne, N.L. (2001) Regulation of seasonal reproduction in mollusks. Journal of Biological Rhythms 16, 391402.
Xie, Q. and Burnell, G.M. (1994) A comparative study of the gametogenic cycles of the clams Tapes philippinarum (Adams & Reeve 1850) and Tapes decussatus (Linnaeus) on the south coast of Ireland. Journal of Shellfish Research 13, 467472.
Yamamoto, K. and Iawata, F. (1956) Studies on the bivalve Venerupis japonica, in Akkleshi Lake: II. Growth rate and biological minimum size. Bulletin of the Hokkaido Regional Fisheries Research Laboratory 14, 5763.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of the Marine Biological Association of the United Kingdom
  • ISSN: 0025-3154
  • EISSN: 1469-7769
  • URL: /core/journals/journal-of-the-marine-biological-association-of-the-united-kingdom
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed