Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T16:33:58.716Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproductive cycle of the golden carpet shell (Polititapes aureus) in the Ria Formosa lagoon (southern Portugal)

Published online by Cambridge University Press:  16 June 2022

Paula Moura Open the ORCID record for Paula Moura [Opens in a new window] ,
Ana Margarete Matias ,
Paulo Vasconcelos Open the ORCID record for Paulo Vasconcelos [Opens in a new window] ,
Cláudia Roque ,
Sandra Joaquim ,
Domitília Matias  and
Miguel B. Gaspar
Paula Moura*
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA, I.P.), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
Ana Margarete Matias
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA, I.P.), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
Paulo Vasconcelos
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA, I.P.), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
Cláudia Roque
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA, I.P.), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
Sandra Joaquim
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA, I.P.), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
Domitília Matias
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA, I.P.), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR), Universidade do Porto, Avenida General Norton de Matos s/n, 4050-208 Matosinhos, Portugal
Miguel B. Gaspar
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA, I.P.), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal Centro de Ciências do Mar (CCMAR), Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal
*
Author for correspondence: Paula Moura, E-mail: pmoura@ipma.pt
Get access Rights & Permissions [Opens in a new window]

Abstract

The present study described the gametogenesis and assessed the pattern of energy storage throughout the reproductive cycle of the golden carpet shell (Polititapes aureus) from the Ria Formosa lagoon (southern Portugal). Monthly sampling was performed for two years (March 2016–February 2018) and the study was based on gonad histology, complemented by the estimation of the mean gonadal index, body condition index and biochemical composition. The species’ reproductive cycle presented a seasonal pattern, with a resting period mainly between October and January and gametogenesis beginning around February–March. The spawning season of P. aureus was shorter in 2016 (June–September) than in 2017 (May–October). Furthermore, ripe individuals were very scarce (1.3%) in 2017 compared with the previous year (11.4%). Mean gonadal index (GI) reflected the species’ reproductive cycle and the body condition index (CI) and biochemical composition of the individuals exhibited high variation between years. Regarding the biochemical composition, proteins ranged between 190.6 and 595.2 μg mg−1, glycogen from 5.7 to 102.6 μg mg−1 and total lipids between 31.6 and 80.7 μg mg−1. The reproduction of P. aureus was strongly influenced by fluctuations in both seawater temperature and chlorophyll a, as reflected through the temporal variation in the gonadal cycle, condition index and biochemical composition. Overall, the information gathered in this study is valuable to propose scientifically based harvesting management measures for the long-term sustainable exploitation of this shellfish resource, further reinforcing the importance of implementing adaptive fishery management strategies to cope with global climate change.

Keywords

Biochemical compositioncondition indexgametogenesisgolden carpet shellmean gonadal indexPolititapes aureusPortugalreproductive cycleRia Formosa lagoonspawning season
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 102 , Issue 1-2 , March 2022 , pp. 77 - 86
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, SC, Lotze, HK and Shackell, NL (2008) Evaluating the knowledge base for expanding low-trophic-level fisheries in Atlantic Canada. Canadian Journal of Fisheries and Aquatic Sciences 65, 2553–2571.CrossRefGoogle Scholar
Anderson, SC, Mills Flemming, J, Watson, R and Lotze, HK (2011) Rapid global expansion of invertebrate fisheries: trends, drivers, and ecosystem effects. PLoS ONE 6, e14735.CrossRefGoogle ScholarPubMed
Avendaño, M and Le Pennec, M (1997) Intraspecific variation in gametogenesis in two populations of the Chilean molluscan bivalve, Argopecten purpuratus (Lamarck). Aquaculture Research 28, 175–182.CrossRefGoogle Scholar
Bayne, BL and Newell, RC (1983) Physiological energetics of marine molluscs. In Salenium, ASM and Wilbur, KM (eds) The Mollusca, vol. 4. New York, NY: Academic Press, pp. 407–515.Google Scholar
Beninger, PG and Lucas, A (1984) Seasonal variations in condition, reproductive activity, and gross biochemical composition of two species of adult clam reared in a common habitat: Tapes decussatus (L.) (Jeffreys) and Tapes philippinarum (Adam & Reeve). Journal of Experimental Marine Biology and Ecology 79, 19–37.CrossRefGoogle Scholar
Berkes, F, Hughes, TP, Steneck, RS, Wilson, JA, Bellwood, DR, Crona, B, Folke, C, Gunderson, LH, Leslie, HM, Norberg, J, Nyström, M, Olsson, P, Österblom, H, Scheffer, M and Worm, B (2006) Globalization, roving bandits, and marine resources. Science 311, 1557–1558.CrossRefGoogle ScholarPubMed
Beukema, JJ and De Bruin, W (1979) Calorific values of the soft parts of the tellinid bivalve Macoma balthica (L.) as determined by two methods. Journal of Experimental Marine Biology and Ecology 37, 19–30.CrossRefGoogle Scholar
Borges, PAV, Costa, A, Cunha, R, Gabriel, R, Gonçalves, V, Martins, AF, Melo, I, Parente, M, Raposeiro, P, Rodrigues, P, Santos, RS, Silva, L, Vieira, P and Vieira, V (2010) A List of the Terrestrial and Marine Biota From the Azores. Oeiras: Princípia.Google Scholar
Carballal, MJ, Iglesias, D, Díaz, S and Villalba, A (2013) Disseminated neoplasia in clams Venerupis aurea from Galicia (NW Spain): histopathology, ultrastructure and ploidy of the neoplastic cells, and comparison of diagnostic procedures. Journal of Invertebrate Pathology 112, 16–19.CrossRefGoogle ScholarPubMed
Carpenter, KE and De Angelis, N (2016) The Living Marine Resources of the Eastern Central Atlantic. Volume 2. Bivalves, Gastropods, Hagfishes, Sharks, Batoid Fishes, and Chimaeras. FAO Identification Guide for Fishery Purposes. Rome: Food and Agriculture Organisation of the United Nations.Google Scholar
Clarke, A (1987) Temperature, latitude and reproductive effort. Marine Ecology Progress Series 38, 89–99.CrossRefGoogle Scholar
Costa, DP (2018) Ensaios para cultivo de amêijoa-macha Venerupis corrugata (Gmelin, 1791) e amêijoa-cão Polititapes aureus (Gmelin, 1791) em aquacultura. MSc thesis. Escola Superior de Turismo e Tecnologia do Mar. Instituto Politécnico de Leiria, Leiria, Portugal.Google Scholar
da Costa, F, Aranda-Burgos, JA, Cerviño-Otero, A, Fernández-Pardo, A, Louzán, A, Nóvoa, S, Ojea, J and Martínez-Patiño, D (2012) Clam reproduction. In da Costa, F (ed.), Clam Fisheries and Aquaculture. Lugo: Centro de Cultivos Marinos de Ribadeo, CIMA, Muelle de Porcillán, pp. 45–72.Google Scholar
Derbali, A and Jarboui, O (2021) Stock mapping, size structure and biological parameters of the clam Polititapes aureus in the shellfish production area of the southern Tunisian waters (Central Mediterranean). International Journal of Oceanography and Hydrology 50, 128–136.Google Scholar
Di Bella, G, Turco, VL, Potortì, AG, Rando, R, Licata, P and Dugo, G (2013) Statistical analysis of heavy metals in Cerastoderma edule glaucum and Venerupis aurea laeta from Ganzirri Lake, Messina (Italy). Environmental Monitoring and Assessment 185, 7517–7525.CrossRefGoogle Scholar
FAO (2009) The State of Food and Agriculture. Technical report. Rome: Food and Agriculture Organization of the United Nations, 166 pp.Google Scholar
Fariña, PA (2005) Dinámica reproductora de dos especies de almejas autóctonas de las Rías Gallegas, Venerupis aurea (Gmelin, 1790) y Venerupis pullastra (Montagu, 1803); estudio histológico, histoquímico y estereológico. PhD thesis. Universidade de Santiago de Compustela, Spain.Google Scholar
Folch, J, Less, M and Stanley, GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497–509.CrossRefGoogle ScholarPubMed
Fouda, MM and Abou-Zied, MM (1990) Bivalves of the Suez Canal lakes. Proceedings of Zoological Society, Egypt 21, 231–240.Google Scholar
François, F, Dalègre, K, Gilbert, F and Stora, G (1999) Specific variability within functional groups. Study of the sediment reworking of two Veneridae bivalves, Ruditapes decussatus and Venerupis aurea. Comptes Rendus de l'Académie des Sciences Series III Sciences de la Vie 322, 339–345.Google Scholar
Gabbott, PA (1976) Energy metabolism. In Bayne, BL (ed.), Marine Mussels: Their Ecology and Physiology. Cambridge: Cambridge University Press, pp. 293–357.Google Scholar
Gallois, D (1977) Sur la reproduction des palourdes, Venerupis decussata (Linné) et des clovisses, Venerupis aurea (Gmelin) de l’étang de Thau (Hérault). Vie et Milieu 27, 233–254.Google Scholar
Gaspar, MB, Barracha, I, Carvalho, S and Vasconcelos, P (2013) Clam fisheries worldwide: main species, harvesting methods and fishing impacts. In Costa, F (ed.), Clam Fisheries and Aquaculture. New York, NY: Nova Science Publishers, pp. 291–327.Google Scholar
Gaspar, MB and Monteiro, CC (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, 1247–1258.Google Scholar
Howard, DW, Lewis, EJ, Keller, BJ and Smith, CS (2004) Histological Techniques for Marine Bivalve Mollusks and Crustaceans. NOAA Technical Memorandum NOS NCCOS 5. Oxford, MD: NCCOS, 218 pp.Google Scholar
Iglesias, JIP, Camacho, C, Navarro, E, Labarta, U, Beiras, R, Hawkins, AJS and Widdows, J (1996) Microgeographic variability in feeding, absorption and condition of mussels (Mytilus galloprovincialis Lmk): a transplant experiment. Journal of Shellfish Research 15, 673–680.Google Scholar
Iglesias, D, Carballal, MJ and Villalba, A (2007) An epizootic proliferative disorder detected in a natural population of the clam Venerupis aurea in Galicia (NW Spain). 13th International Conference of the EAFP, 17–21 September 2007. Grado, Italy, p. 184.Google Scholar
IH (2020) Dados de temperatura da água registados na boia oceanográfica costeira de Faro (2016–2018). Lisboa: Instituto Hidrográfico (IH).Google Scholar
Joaquim, S, Matias, D, Matias, AM, Moura, P, Arnold, WS, Chícharo, L and Gaspar, MB (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, 217–226.CrossRefGoogle Scholar
Joaquim, S, Matias, D, Matias, AM, Moura, P, Roque, C, Chícharo, L and Gaspar, MB (2014) Biochemical and energy dynamics throughout the reproductive cycle of the striped venus Chamelea gallina (Mollusca, Bivalvia). Invertebrate Reproduction & Development 58, 284–293.CrossRefGoogle Scholar
Kandeel, KE (1992) Biological studies on the reproduction of some bivalves in Lake Timsah (MSc thesis). University of Suez Canal, Ismailia, Egypt.Google Scholar
Kandeel, KE (2002) Ecological and biological studies on some bivalves in Lake Timsah and the Bitter Lakes. Unpublished PhD thesis. University of Suez Canal, Ismailia, Egypt.Google Scholar
Kandeel, KE (2006) Quantitative assessment of gamete production in two commercially harvested clams, Venerupis aurea and Tapes decussata (Bivalvia: Veneridae) in Lake Timsah, Suez Canal, Egypt. Catrina 1, 41–52.Google Scholar
Kandeel, KE (2008) Length-weight relationships and monthly variations in body weights and condition indices of two clam's species; Venerupis aurea and Tapes decussata in Lake Timsah, Egypt. Catrina 3, 111–124.Google Scholar
Kandeel, KE (2013) Recruitment pattern of commercially harvested clam, Venerupis aurea (Bivalvia: Veneridae) at the southern region of Lake Timsah, Suez Canal, Egypt. Thalassia Salentina 35, 11–28.Google Scholar
Kandeel, KE (2017 a) Invasion dynamics of a non-indigenous bivalve clam; Venerupis aurea (Gmelin, 1791), in Lake Qarun, Egypt. Journal of Advances in Biology 10, 2056–2066.Google Scholar
Kandeel, KE (2017 b) Size at the onset of sexual maturity in 7 bivalve species in Egyptian waters. Thalassia Salentina 39, 123–136.Google Scholar
Kandeel, KE (2018) Population dynamics of Venerupis aurea (Bivalvia: Veneridae) in two different clam's beds in Lake Timsah, Suez Canal, Egypt. Thalassia Salentina 40, 67–94.Google Scholar
Lotze, HK, Lenihan, HS, Bourque, BJ, Bradbury, RH, Cooke, RG, Kay, MC, Kidwell, SM, Kirby, MX, Peterson, CH and Jackson, JBC (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312, 1806–1809.CrossRefGoogle ScholarPubMed
Machado, D, Baptista, T, Joaquim, S, Anjos, C, Mendes, S, Matias, AM and Matias, D (2018) Reproductive cycle of the European clam Ruditapes decussatus from Óbidos Lagoon, Leiria, Portugal. Invertebrate Reproduction & Development 62, 179–190.CrossRefGoogle Scholar
Maia, F, Sobral, MP and Gaspar, M (2006) Ciclo reprodutivo e primeira maturação de Solen marginatus e Venerupis pullastra na Ria de Aveiro. Bases científicas para a gestão destes recursos. Relatórios científicos e técnicos IPIMAR, série digital, no. 30, 35 pp.Google Scholar
Marsh, JB and Weinstein, DB (1966) Simple charring method for determination of lipids. Journal of Lipid Research 7, 574–576.CrossRefGoogle ScholarPubMed
Matias, D, Joaquim, S, Matias, AM, 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, 52–61.CrossRefGoogle Scholar
Mohammad, SH (2002) Ecological and biological studies on the bivalves, Cerastoderma glaucum and Papyridae papyracea, in Lake Timsah, Suez Canal. PhD thesis. University of Suez Canal, Ismailia, Egypt.Google Scholar
Mohammad, SH, Belal, AAM and Hassan, SSZ (2014) Growth, age and reproduction of the commercially clams Venerupis aurea and Ruditapes decussatus in Timsah Lake, Suez Canal, Egypt. Indian Journal of Geo-Marine Sciences 43, 589–600.Google Scholar
Morton, B and Leung, PTY (2018) The discovery and identification of Ruditapes aureus (Gmelin, 1791) (Bivalvia: Veneridae: Tapetinae) introduced alongside an earlier alien venerid, R. decussatus (Linnaeus, 1758), into the lagoon of Fajã de Santo Cristo, São Jorge, Açores. Açoreana 11, 205–225.Google Scholar
Moura, P, Gaspar, MB and Monteiro, CC (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, 161–167.CrossRefGoogle Scholar
Navas, JI, Castillo, MC, Vera, P and Ruíz-Rico, M (1992) Principal parasites observed in clams, Ruditapes decussatus (L.), Ruditapes philippinarum (Adams et Reeve), Venerupis pullastra (Montagu) and Venerupis aureus (Gmelin), from the Huelva coast (S.W. Spain). Aquaculture 107, 193–199.CrossRefGoogle Scholar
Oyarzún, P, Toro, J, Garcés-Vargas, J, Alvarado, C, Guiñez, R, Jaramillo, R, Briones, C and Campos, B (2018) Reproductive patterns of mussel Perumytilus purpuratus (Bivalvia: Mytilidae), along the Chilean coast: effects caused by climate change? Journal of the Marine Biological Association of the United Kingdom 98, 375–385.CrossRefGoogle Scholar
Paine, RT (1971) The measurement and application of the calorie to ecological problems. Annual Review of Ecology, Evolution and Systematics 2, 145–164.Google Scholar
Pereira, N (2011) Avaliação do Potencial Aquícola da População de Amêijoas Venerupis aurea (Gmelin, 1791) da Ilha de S. Jorge (Açores). MSc thesis. Universidade do Porto, Portugal.Google Scholar
Pérez-Camacho, A, Delgado, M, Fernández-Reiriz, MJ and Labarta, U (2003) Energy balance, gonad development and biochemical composition in the clam Ruditapes decussatus. Marine Ecology Progress Series 258, 133–145.CrossRefGoogle Scholar
Poppe, GT and Goto, Y (1993) European seashells, Vol. 2. Scaphopoda, Bivalvia, Cephalopoda. Wiesbaden: Verlag Christa Hemmen.Google Scholar
Rand, WM (1973) A stochastic model of the temporal aspect of breeding strategies. Journal of Theoretical Biology 40, 337–351.CrossRefGoogle ScholarPubMed
Sastry, AN (1979) Pelecypoda (excluding Ostreidae). In Giese, AC and Pearse, JS (eds) Reproduction of Marine Invertebrates, Vol. V. Molluscs: Pelecypods and Lesser Classes. New York, Boston: Academic Press, pp. 113–292.Google Scholar
Sathyendranath, S, Brewin, RJW, Brockmann, C, Brotas, V, Calton, B, Chuprin, A, Cipollini, P, Couto, AB, Dingle, J, Doerffer, R, Donlon, C, Dowell, M, Farman, A, Grant, M, Groom, S, Horseman, A, Jackson, T, Krasemann, H, Lavender, S, Martinez-Vicente, V, Mazeran, C, Mélin, F, Moore, TS, Müller, D, Regner, P, Roy, S, Steele, CJ, Steinmetz, F, Swinton, J, Taberner, M, Thompson, A, Valente, A, Zühlke, M, Brando, VE, Feng, H, Feldman, G, Franz, BA, Frouin, R, Gould, RW Jr, Hooker, SB, Kahru, M, Kratzer, S, Mitchell, BG, Muller-Karger, F, Sosik, HM, Voss, KJ, Werdell, J and Platt, T (2019) An ocean-colour time series for use in climate studies: the experience of the Ocean-Colour Climate Change Initiative (OC-CCI). Sensors 19, 4285. Available at https://www.oceancolour.org/portal/ Accessed online 6 March 2021.CrossRefGoogle ScholarPubMed
Seed, R (1976) Ecology. In Bayne, BL (ed.), Marine Mussels: Their Ecology and Physiology. Cambridge: Cambridge University Press, pp. 13–65.Google Scholar
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, 81–88.Google Scholar
Shafee, MS and Daoudi, M (1991) Gametogenesis and spawning in the carpet-shell clam, Ruditapes decussatus (L.) (Mollusca: Bivalvia), from the Atlantic coast of Morocco. Aquaculture and Fisheries Management 22, 203–216.Google Scholar
Shakir, FK, Audilet, D, Drake, AJ 3rd and Shakir, MM (1994) A rapid protein determination by modification of the Lowry Procedure. Analytical Biochemistry 216, 232–233.CrossRefGoogle ScholarPubMed
Tebble, N (1966) British Bivalve Seashells. A Handbook for Identification. London: Trustees of the British Museum (Natural History).Google Scholar
Tirado, C, Rodríguez, FA, Bruzón, MA, López, JI, Salas, C and Márquez, I (2002) La reproducción de bivalvos y gasterópodos de interés pesquero en Andalucía. Huelva: Junta de Andalucía, Consejería de Agricultura y Pesca.Google Scholar
Trigui El Menif, N, Le Pennec, M and Maamouri, F (1995) Reproduction of the European clam Ruditapes decussatus (mollusc, bivalve) along the Tunisian coasts. Marine Life 5, 35–42.Google Scholar
Ubertini, M, Lagarde, F, Mortreux, S, Le Gall, P, Chiantella, C, Fiandrino, A, Bernard, I, Pouvreau, S and d'Orbcastel, ER (2017) Gametogenesis, spawning behavior and larval abundance of the Pacific oyster Crassostrea gigas in the Thau lagoon: evidence of an environment-dependent strategy. Aquaculture 473, 51–61.CrossRefGoogle Scholar
Viles, FJ and Silverman, L (1949) Determination of starch and cellulose with anthrone. Journal Analytical Chemistry 21, 950–953.CrossRefGoogle Scholar
Walne, P and Mann, R (1975) Growth and biochemical composition in Ostrea edulis and Crassostrea gigas. Proceedings of the 9th European marine biology symposium, the Dunstaffnage marine research laboratory, Oban, Scotland, UK, 2–8 October 1974. In Barnes, H (ed.), The Biochemistry, Physiology and Behaviour of Marine Organisms in Relation to Their Ecology. Aberdeen: Aberdeen University Press, pp. 587–607.Google Scholar
Yassien, MH, El-Ganainy, AA and Sallam, WS (2009) Age, growth and mortality rates of the venerid clam Venerupis aurea in Timsah Lake, Suez Canal, Egypt. Egyptian Journal of Aquatic Research 35, 317–324.Google Scholar