Advertisement

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

  • Patricia PradoEmail author
  • Karl B. Andree
  • Sergio Trigos
  • Noelia Carrasco
  • Nuno Caiola
  • Jose Rafael García-March
  • José Tena
  • Margarita Fernández-Tejedor
  • Francesca Carella
Primary Research Paper

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.

Keywords

Larval availability Anomalous simultaneous hermaphroditism Agricultural pollution Salinity Habitat features Parasites Western Mediterranean 

Notes

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.

References

  1. 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.CrossRefGoogle Scholar
  2. 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.PubMedCrossRefGoogle Scholar
  3. 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
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. Camp, J. & M. Delgado, 1987. Hidrografía de las bahías del delta del Ebro. Investigaciones Pesqueras 51(3): 351–369.Google Scholar
  7. 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.PubMedCrossRefGoogle Scholar
  8. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cerralbo, P., M. Espino, M. Grifoll & A. Valle-Levinson, 2019. Subtidal circulation in a microtidal Mediterranean bay. Scientia Marina 82(4): 231–243.CrossRefGoogle Scholar
  11. Chícharo, L. & M. A. Chícharo, 2001. A juvenile recruitment prediction model for Ruditapes decussatus (L.) (Bivalvia: Mollusca). Fisheries Research 53: 219–233.CrossRefGoogle Scholar
  12. Clarke, K. R. & R. N. Gorley, 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth.Google Scholar
  13. 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
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. García-March, J. R. & A. Márquez-Aliaga, 2007. Pinna nobilis L., 1758 age determination by internal shell register. Marine Biology 151: 1077–1085.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.Google Scholar
  21. Giese, A. C., 1959. Comparative physiology: annual reproductive cycles of marine invertebrates. Annual Review of Physiology 21(1): 547–576.PubMedCrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. Katsanevakis, S., 2005. Population ecology of the endangered fan mussel Pinna nobilis, in a marine lake. Endangered Species Research 1: 1–9.Google Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.Google Scholar
  31. Millot, C. & I. Taupier-Letage, 2005. Circulation in the Mediterranean sea. The Mediterranean Sea. Springer, Berlin: 29–66.CrossRefGoogle Scholar
  32. 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.Google Scholar
  33. 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
  34. 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.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. Prado, P., N. Caiola & C. Ibáñez, 2014. Habitat use by a large population of Pinna nobilis in shallow waters. Scientia Marina 78: 555–565.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. Richmond, C. E. & S. A. Woodin, 1996. Short-term fluctuations in salinity: effects on planktonic invertebrate larvae. Marine Ecology Progress Series 133: 167–177.CrossRefGoogle Scholar
  41. 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
  42. Rumrill, S. S., 1990. Natural mortality of marine invertebrate larvae. Ophelia 32(1–2): 163–198.CrossRefGoogle Scholar
  43. 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
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Patricia Prado
    • 1
    Email author
  • Karl B. Andree
    • 1
  • Sergio Trigos
    • 2
  • Noelia Carrasco
    • 1
  • Nuno Caiola
    • 1
  • Jose Rafael García-March
    • 3
  • José Tena
    • 3
  • Margarita Fernández-Tejedor
    • 1
  • Francesca Carella
    • 4
  1. 1.IRTA-Sant Carles de la RàpitaSant Carles de la RàpitaSpain
  2. 2.Innovation Network in Aquaculture Industries of the Valencian Community (RIIA-CV)ValenciaSpain
  3. 3.Institute of Environment and Marine Science Research (IMEDMAR)Universidad Católica de Valencia SVMCalpeSpain
  4. 4.Department of BiologyUniversity of Naples Federico IINaplesItaly

Personalised recommendations