Skip to main content

Advertisement

Log in

Breeding, planktonic and settlement factors shape recruitment patterns of one of the last remaining major population of Pinna nobilis within Spanish waters

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The pen shell, Pinna nobilis L., is a critically endangered bivalve threatened by mass mortality events throughout the Mediterranean, but the Alfacs Bay (Ebro Delta) still hosts many healthy individuals. Herein, we study the main factors controlling recruitment patterns in this locality, including gonadal development and abundance of critical life-stages, as well as the effect of environmental factors. Growth records from empty shells suggested a single major peak of recruitment during a period of 11 years, although many juveniles were found in two very shallow sand bars possibly acting as a barrier for water circulation and as a trap for larvae. Collectors deployed outside these sand bar areas showed zero settlers, and the availability of planktonic larvae was very low. Gonadal examination evidenced breeding throughout the summer period with successive hermaphroditism, but 20% of individuals were simultaneous hermaphrodites, a condition that has been associated with environmental stress and that could lead to in-breeding depression and potentially reduced fertility. Yet, given the large size of the population and the wide breeding period observed, planktonic processes causing larval mortality such as freshwater discharges from rice locally important rice agriculture are also proposed as possible impacts accounting for patterns of low larval availability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Andree, K. B., S. Trigos, N. Vicente, N. Carrasco, F. Carella & P. Prado, 2018. Identification of potential recruitment bottlenecks in larval stages of the giant fan mussel Pinna nobilis using specific quantitative PCR. Hydrobiolgia 818: 235–247.

    Article  Google Scholar 

  • Brossa, L., R. M. Marcé, F. Borrull & E. Pocurull, 2005. Occurrence of twenty-six endocrine-disrupting compounds in environmental water samples from Catalonia, Spain. Environmental Toxicology and Chemistry 24: 261–267.

    Article  CAS  PubMed  Google Scholar 

  • Butler, A., N. Vicente & B. De Gaulejac, 1993. Ecology of de pterioid bivalves Pinna bicolor Gmelin and P. nobilis L. Marine Life 3: 37–45.

    Google Scholar 

  • Cabanellas-Reboredo, M., S. Deudero, J. Alós, J. M. Valencia, D. March, I. E. Hendriks & E. Álvarez, 2009. Recruitment of Pinna nobilis (Mollusca: Bivalvia) on artificial structures. Marine Biodiversity Records 2: e126.

    Article  Google Scholar 

  • Cabanellas-Reboredo, M., M. Vázquez-Luis, B. Mourre, et al., 2019. Tracking the dispersion of a pathogen causing mass mortality in the pen shell Pinna nobilis: a collaborative effort of scientists and citizens. Scientific Repports 9: 13355.

    Article  CAS  Google Scholar 

  • Camp, J. & M. Delgado, 1987. Hidrografía de las bahías del delta del Ebro. Investigaciones Pesqueras 51(3): 351–369.

    Google Scholar 

  • Carballal, M. J., D. Iglesias, J. Santamarina, B. Ferro-Soto & A. Villalba, 2001. Parasites and pathologic conditions of the cockle Cerastoderma edule populations of the coast of Galicia. Journal of Invertebrate Pathology 78: 87–97.

    Article  CAS  PubMed  Google Scholar 

  • Carella, F., S. Aceto, G. Pollaro, A. Micccio, N. Carrasco, P. Prado & G. De Vico, 2019. An emerging mycobacterial disease is associated with the silent mass mortality of the Pen shell Pinna nobilis along Tyrrhenian coastline of Italy. Scientific Reports 9: 2725.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Catanese, G., Grau, A., Valencia, J.M., Garcia-March, J.R., Vázquez-Luis, M., Alvarez, E., Deudero, S., Darriba, S., Carballal, M.J., Villalba, A., 2018. Haplosporidium pinnae sp. nov., a haplosporidan parasite associated with mass mortalities of the fan mussel, Pinna nobilis, in the Western Mediterranean Sea. Journal of Invertebrate Pathology 157: 9–24. https://doi.org/10.1016/j.jip.2018.07.006.

    Article  CAS  PubMed  Google Scholar 

  • Cerralbo, P., M. Espino, M. Grifoll & A. Valle-Levinson, 2019. Subtidal circulation in a microtidal Mediterranean bay. Scientia Marina 82(4): 231–243.

    Article  Google Scholar 

  • Chícharo, L. & M. A. Chícharo, 2001. A juvenile recruitment prediction model for Ruditapes decussatus (L.) (Bivalvia: Mollusca). Fisheries Research 53: 219–233.

    Article  Google Scholar 

  • Clarke, K. R. & R. N. Gorley, 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth.

    Google Scholar 

  • De Gaulejac, B., 1995. Mise en évidence de l’hermaphrodisme successif à maturation asynchrone de Pinna nobilis (L.) (Bivalia: Pterioidea). Comptes rendus de l’Académie des Sciences, Sèrie 3, Sciences de la Vie 318: 99–103.

    Google Scholar 

  • De Gaulejac, B., M. Henry & N. Vicente, 1995a. An ultrastructural study of gametogenesis of the marine bivalve Pinna nobilis (Linnaeus 1758) I. Oogenesis. Journal of Molluscan Studies 61: 375–392.

    Article  Google Scholar 

  • De Gaulejac, B., M. Henry & N. Vicente, 1995b. An ultrastructural study of gametogenesis of the marine bivalve Pinna nobilis (Linnaeus 1758) II. Spermatogenesis. Journal of Molluscan Studies 61: 393–403.

    Article  Google Scholar 

  • Deudero, S., A. Grau, M. Vázquez-Luis, E. Álvarez, C. Alomar & I. E. Hendriks, 2017. Reproductive investment of the pen shell Pinna nobilis Linnaeus, 1758 in Cabrera National Park (Spain). Mediterranean Marine Science 18: 271–284.

    Article  Google Scholar 

  • García-March, J. R. & A. Márquez-Aliaga, 2007. Pinna nobilis L., 1758 age determination by internal shell register. Marine Biology 151: 1077–1085.

    Article  Google Scholar 

  • García-March, J. R., A. M. García-Carrascosa, A. L. Peña Cantero & Y. G. Wang, 2007. Population structure, mortality and growth of Pinna nobilis Linnaeus, 1758 (Mollusca, Bivalvia) at different depths in Moraira bay (Alicante, Western Mediterranean). Marine Biology 150: 861–871.

    Article  Google Scholar 

  • García-March, J. R., A. Marquez-Aliaga, Y. G. Wang, D. Surge & D. K. Kersting, 2011. Study of Pinna nobilis growth from inner record: how biased are posterior adductor muscle scars estimates? Journal of Experimental Marine Biology and Ecology 407: 337–344.

    Article  Google Scholar 

  • García-March, J. R., J. Tena-Medialdea, S. Henandis-Caballero, et al., in review. Can we save a marine species affected by a highly-infective-highly-lethal-waterborne disease from extinction? Biological Conservation.

  • Giese, A. C., 1959. Comparative physiology: annual reproductive cycles of marine invertebrates. Annual Review of Physiology 21(1): 547–576.

    Article  CAS  PubMed  Google Scholar 

  • Himmelman, J. H., 1975. Phytoplankton as a stimulus for spawning in three marine invertebrates. Journal of Experimental Marine Biology and Ecology 20(2): 199–214.

    Article  Google Scholar 

  • Katsanevakis, S., 2005. Population ecology of the endangered fan mussel Pinna nobilis, in a marine lake. Endangered Species Research 1: 1–9.

    Google Scholar 

  • Katsanevakis, S., 2007. Growth and mortality rates of the fan mussel Pinna nobilis in Lake Vouliagmeni (Korinthiakos Gulf, Greece): a generalized additive modelling approach. Marine Biology 152: 1319–1331.

    Article  Google Scholar 

  • Kersting, D. K. & J. R. García-March, 2017. Long-term assessment of recruitment, early stages and population dynamics of the endangered Mediterranean fan mussel Pinna nobilis in the Columbretes Islands (NW Mediterranean). Marine Environmental Research 130: 282–292.

    Article  CAS  PubMed  Google Scholar 

  • Köck-Schulmeyer, M., M. L. de Alda, E. Martínez, M. Farré, A. Navarro, A. Ginebreda & D. Barceló, 2010. Pesticides at the Ebro River delta: occurrence and toxicity in water and biota. In Barceló, D. & M. Petrovis (eds), The Ebro River Basin. Springer, Berlin: 259–274.

    Chapter  Google Scholar 

  • Llebot, C., J. Solé, M. Delgado, M. Fernández-Tejedor, J. Camp & M. Estrada, 2011. Hydrographical forcing and phytoplankton variability in two semi-enclosed estuarine bays. Journal of Marine Systems 86(3–4): 69–86.

    Article  Google Scholar 

  • Llebot, C., F. J. Rueda, J. Solé, M. L. Artigas & M. Estrada, 2014. Hydrodynamic states in a wind-driven microtidal estuary (Alfacs Bay). Journal of Sea Research 85: 263–276.

    Article  Google Scholar 

  • Lough, R. G. & J. J. Gonor, 1971. Early embryonic stages of Adula californiensis (Pelecypoda: Mytilidae) and the effect of temperature and salinity on developmental rate. Marine Biology 8(2): 118–125.

    Article  Google Scholar 

  • Malchus, N., Sartori, A.F., 2013. The early shell: ontogeny, features, and evolution. In: Treatise Online, Part N, Revised, Vol 1, Chapter 4, pp 1–114.

  • Millot, C. & I. Taupier-Letage, 2005. Circulation in the Mediterranean sea. The Mediterranean Sea. Springer, Berlin: 29–66.

    Chapter  Google Scholar 

  • Nebot, E., M., Vázquez, E., Boissin, C., Peyran, S., Deudero & S. Planes, 2019. Inferred family structure of an endangered species, Pinna nobilis, using molecular analyses: implications of connectivity for conservation. Book of Abstracts, XX Iberian Symposium of Marine Biology (SIEBM). Braga, Portugal, 9–12 September.

  • Pekkarinen, M., 1991. Notes on the general condition of Mytilus edulis L. of the Southwestern coast of Finland. Bivalve Studies in Finland 1: 20–40.

    Google Scholar 

  • Pineda, J., F. Porri, V. Starczak & J. Blythe, 2010. Causes of decoupling between larval supply and settlement and consequences for understanding recruitment and population connectivity. Journal of Experimental Marine Bioloy and Ecology 392: 9–21.

    Article  Google Scholar 

  • Porri, F., T. Jordaan & C. D. McQuaid, 2008. Does cannibalism of larvae by adults affect settlement and connectivity of mussel populations? Estuarine Coastal and Shelf Science 79: 687–693.

    Article  Google Scholar 

  • Prado, P., 2018. Seagrass epiphytic assemblages are strong indicators of agricultural discharge but weak indicators of host features. Estuarine Coastal and Shelf Science 204: 140–148.

    Article  Google Scholar 

  • Prado, P., N. Caiola & C. Ibáñez, 2014. Habitat use by a large population of Pinna nobilis in shallow waters. Scientia Marina 78: 555–565.

    Article  Google Scholar 

  • Richardson, C. A., H. Kennedy, C. M. Duarte, D. P. Kennedy & S. V. Proud, 1999. Age and growth of the fan mussel Pinna nobilis from south-east Spanish Mediterranean seagrass (Posidonia oceanica) meadows. Marine Biology 133: 205–212.

    Article  Google Scholar 

  • Richardson, C. A., M. Peharda, H. Kennedy, P. Kennedy & V. Onofri, 2004. Age, growth rate and season of recruitment of Pinna nobilis (L) in the Croatian Adriatic determined from Mg: Ca and Sr: Ca shell profiles. Journal of Experimental Marine Biology and Ecology 299(1): 1–16.

    Article  CAS  Google Scholar 

  • Richmond, C. E. & S. A. Woodin, 1996. Short-term fluctuations in salinity: effects on planktonic invertebrate larvae. Marine Ecology Progress Series 133: 167–177.

    Article  Google Scholar 

  • Rouanet, E., S. Trigos & N. Vicente, 2015. From youth to death of old age: the 50-year story of a Pinna nobilis fan mussel population at Port-Cros Island (Port-Cros National Park, Provence, Mediterranean Sea). Scientific Reports of the Port-Cros National Park 29: 209–222.

    Google Scholar 

  • Rumrill, S. S., 1990. Natural mortality of marine invertebrate larvae. Ophelia 32(1–2): 163–198.

    Article  Google Scholar 

  • Syasina, I. G., M. A. Vashchenco, P. M. Zhadan & E. M. Kareseva, 1996. State of the gonads and development of offspring of the scallop Mizuhopecten yessoensis from polluted areas in Peter the Great Bay, the Sea of Japan. Russian Journal of Marine Biology 22: 233–240.

    Google Scholar 

  • Theodorou, J. A., R. James, I. Tzovenis & C. Hellio, 2015. The recruitment of the endangered fan mussel Pinna nobilis (Linnaeus, 1758) on the ropes of a Mediterranean mussel long line farm. Journal of Shellfish Research 4: 409–414.

    Article  Google Scholar 

  • Trigos, S., N. Vicente, P. Prado & F. J. Espinós, 2018. Adult spawning and early larval development of the endangered bivalve Pinna nobilis. Aquaculture 483: 102–110.

    Article  Google Scholar 

  • Wesselmann, M., M. González-Wangüemert, E. A. Serrão, A. H. Engelen, L. Renault, J. R. García-March, C. M. Duarte & I. E. Hendriks, 2018. Genetic and oceanographic tools reveal high population connectivity and diversity in the endangered pen shell Pinna nobilis. Scientific Reports 8(1): 4770.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Whyte, S. K., R. J. Cawthorn & S. E. McGladdery, 1994. Co-infection of bay scallops Argopecten irradians with Perkinsus karlssoni (Apicomplexa, Perkinsea) and an unidentified coccidian parasite. Diseases of Aquatic Organisms 18: 53–62.

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the Zoo Barcelona Foundation for an Antoni Jonch grant 2015. JR García-March and J Tena were funded by the Albert II of Monaco Foundation to develop the age study within the project “The study, protection and possible breeding of the pen shell (P. nobilis) in the Boka Kotorska Bay”. Additional funding was obtained from a 2017 INIA Grant for project EMERGER (E-RTA2015-00004-00-00). We thank Department of Territory and Sustainability for granting us a permit for the collection of P. nobilis (Ref.: SF/030). Environmental factors were obtained from the project “Programa de seguiment de la qualitat de les aigües, mol·luscs i fitoplancton toxic les zones de producció de marics del litoral català de la DGPAM”. IRTA acknowledges support from the CERCA Program from the Catalonian Government. Authors thank Dr. Miguel Alonso García-Amilivia for help with the separation of bivalve larvae, and Pep Cabanes, Lluis Jornet, and Jose Luis Costa for fieldwork assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patricia Prado.

Additional information

Handling editor: Manuel Lopes Lima

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prado, P., Andree, K.B., Trigos, S. et al. Breeding, planktonic and settlement factors shape recruitment patterns of one of the last remaining major population of Pinna nobilis within Spanish waters. Hydrobiologia 847, 771–786 (2020). https://doi.org/10.1007/s10750-019-04137-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-04137-5

Keywords

Navigation