Advertisement

Marine Biology

, 165:119 | Cite as

Age estimation of the oyster Ostrea puelchana determined from the hinge internal growth pattern

  • M. S. Doldan
  • M. de Rafélis
  • M. A. Kroeck
  • M. S. Pascual
  • E. M. Morsan
Original paper

Abstract

A multiproxy approach was used to analyse the internal growth pattern of Ostrea puelchana shells. Field investigations using fluorochrome stains were performed to estimate the deposition time of the lines of irregular growth. Cathodoluminescence (CL) microscopy of the hinge area and isotopic composition analyses of shells were performed. The oxygen isotopic composition of the shells showed seasonal fluctuations across the hinge. The results of CL microscopy and stable isotopes provided the first age estimations for wild specimens of O. puelchana. The maximal age of analysed oysters was 4.5 years. Shell deposition occurred at temperatures above 11 °C approximately, suggesting growth slowdown and/or cessation in winter. Lines of irregular growth showed no consistent temporal pattern; these growth structures cannot be used as sclerochronological proxies of growth season or shell age. O. puelchana is sensitive to seasonal environmental changes, which cause changes in its carbonate structure, although the pattern is not consistent, as in other species. In this study, the age of O. puelchana specimens from San Matías Gulf, Patagonia, Argentina, was estimated, providing a basis for future studies on this species.

Notes

Acknowledgements

The calcein experiment was supported by projects PICT 2007-1338 and PICT 2006-1674 from Agencia Nacional de Promoción Científica y Técnica, Argentina, and by projects M019 and M025 from Universidad Nacional del Comahue. We are grateful to CULMAR S.A. for allowing us to use the rack for the growing experiment. We offer our special thanks to Dr. Saba and UNPSJB-CENPAT at Puerto Madryn for the fluorescence microscope and also our special thanks to all colleagues at CRIAR (criadero) for their assistance with the lantern nets and tanks maintenance. MSD thanks M. Herrmann for staining advice and M. Brögger for calcein pictures. The present work was part of the PhD dissertation of MSD. Seawater samples for salinity measurement and in situ seawater temperature data were provided by the Programa de Monitoreo de calidad ambiental de las zonas de producción of CIMAS, Secretaría de Agricultura, Ganadería y Pesca of Provincia de Rio Negro, Argentina. CL and isotope analyses were performed at Laboratoire Biominéralisations et Environnements Sédimentaires de la Maître de Conférences Université Pierre et Marie Curie, Paris, France.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Research involving human participants and/or animals

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Bagur M, Richardson CA, Gutiérrez JL, Arribas LP, Doldan MS, Palomo MG (2013) Age, growth and mortality in four populations of the boring bivalve Lithophaga patagonica from Argentina. J Sea Res 81:49–56CrossRefGoogle Scholar
  2. Barbin V (2013) Application of cathodoluminescence microscopy to recent and past biological materials: a decade of progress. Miner Petrol 107:353–362CrossRefGoogle Scholar
  3. Bougeois L, de Rafélis M, Reichart GJ, de Nooijer LJ, Nicollin F, Dupont-Nivet G (2014) A high resolution study of trace elements and stable isotopes in oyster shells to estimate Central Asian Middle Eocene seasonality. Chem Geol 363:200–212CrossRefGoogle Scholar
  4. Calvo J, Morriconi ER (1978) Epibiontie et protandrie chez Ostrea puelchana. Haliotis 9:85–88Google Scholar
  5. Campana SE (2001) Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J Fish Biol 59:197–242CrossRefGoogle Scholar
  6. Cardoso JFMF, Langlet D, Loff JF, Martins AR, Witte JIJ, Santos PT, van der Veer HW (2007) Spatial variability in growth and reproduction of the Pacific oyster Crassostrea gigas (Thunberg, 1793) along the west European coast. J Sea Res 57:303–315CrossRefGoogle Scholar
  7. Castaños C, Pascual MS, Agulleiro I, Zampatti E, Elvira M (2005) Brooding pattern and larval production in wild stocks of the puelche oyster, Ostrea puelchana D’orbigny. J Shellfish Res 24:191–196CrossRefGoogle Scholar
  8. Castellanos Z (1957) Contribución al conocimiento de las ostras del litoral Argentino (O.puelchana y O.spreta). Min Agric Gan Nac, ArgentinaGoogle Scholar
  9. Creed JC, Kinupp M (2011) Small scale change in mollusk diversity along a depth gradient in a seagrass bed off Cabo Frio (Southeast Brazil). Braz J Oceanogr 59:267–276CrossRefGoogle Scholar
  10. de Rafélis M, Renard M, Emmanuel L, Durlet C (2000) Apport de la cathodoluminiscence à la connaissance de la spéciation du manganèse dans les carbonates pélagiques. CR Acad Sci Sér 2a 330:391–398Google Scholar
  11. Doldan MS, Morsan EM, Zaidman PC, Kroeck MA (2014) Analysis of large-scale spatio-temporal trends of Ostrea puelchana beds in Northern Patagonian gulfs, Argentina. Mar Environ Res 101:196–207CrossRefPubMedGoogle Scholar
  12. Durham SR, Gillikin DP, Goodwin DH, Dietl GP (2017) Rapid determination of oyster lifespans and growth rates using LA–ICP–MS line scans of shell Mg/Ca ratios. Palaeogeogr Palaeoclimatol Palaeoecol.  https://doi.org/10.1016/j.paleo.2017.06.013 CrossRefGoogle Scholar
  13. Epstein S, Buchsbaum R, Lowenstam HA, Urey HC (1953) Revised carbonate-water isotopic temperature scale. Geol Soc Am Bull 64:1315–1326CrossRefGoogle Scholar
  14. Esteban-Delgado FJ, Harper EM, Checa AC, Rodríguez-Navarro AB (2008) Origin and expansion of foliated microstructure in Pteriomorph Bivalves. Biol Bull 214:153–165CrossRefPubMedGoogle Scholar
  15. Fan C, Koeniger P, Wang H, Frechen M (2011) Ligamental increments of the mid-Holocene Pacific oyster Crassostrea gigas are reliable independent proxies for seasonality in the western Bohai Sea, China. Palaeogeogr Palaeoclimatol Palaeoecol 299:437–448CrossRefGoogle Scholar
  16. Fernández Castro N, Bodoy A (1987) Growth of the oyster, Ostrea puelchana (D’Orbigny), at two sites of potential cultivation in Argentina. Aquaculture 65:127–140CrossRefGoogle Scholar
  17. Fernández Castro N, Lucas A (1987) Variability in the frequency of male neoteny in Ostrea puelchana (Mollusca: Bivalvia). Mar Biol 96:359–365CrossRefGoogle Scholar
  18. Gagliardini DA, Rivas AL (2004) Environmental characteristics of San Matías Gulf obtained from LANDSAT-TM and ETM + data. Gayana (Concepción) 68:186–193Google Scholar
  19. Gil MN, Sastre V, Santinelli N, Esteves JL (1989) Metal content in seston from the San José Gulf, Patagonia, Argentina. Bull Environ Contam Toxicol 43:337–341CrossRefPubMedGoogle Scholar
  20. Goodwin DH, Gillikin DP, Roopnarine PD (2013) Preliminary evaluation of potential stable isotope and trace element productivity proxies in the oyster Crassostrea gigas. Palaeogeogr Palaeoclimatol Palaeoecol 373:88–97CrossRefGoogle Scholar
  21. Guerrero E, Svendsen GM (2007) Resultados preliminares de dos campañas oceanográficas (Golfos NORPAT-2007 1 y 2) en los Golfos San Matías y San José. Informe Técnico Interno IBMP 9/07, 16 ppGoogle Scholar
  22. Hastie LC, Young MR, Boon PJ (2000) Growth characteristics of freshwater pearl mussels, Margaritifera margaritifera (L.). Freshw Biol 43:243–256CrossRefGoogle Scholar
  23. Herrmann M, Lepore ML, Laudien J, Arntz WE, Penchaszadeh PE (2009) Growth estimations of the Argentinean wedge clam Donax hanleyanus: a comparison between length-frequency distribution and size-increment analysis. J Exp Mar Bio Ecol 379:8–15CrossRefGoogle Scholar
  24. Kaehler S, Mcquaid CD (1999) Use of the fluorochrome calcein as an in situ growth marker in the internal mussel Perna perna. Mar Biol 133:455–460CrossRefGoogle Scholar
  25. Kirby M, Soniat TM, Spero HJ (1998) Stable isotope sclerochronology of Pleistocene and recent oyster shells (Crassostrea virginica). Palaios 3:560–569CrossRefGoogle Scholar
  26. Lanfredi NW, Pousa JL (1988) Mediciones de corrientes, San Antonio Oeste, Provincia de Río Negro. 13 pp. Informe Inédito, Instituto de Biología Marina y Pesquera “Almirante Storni”Google Scholar
  27. Langlet D, Alunno-Bruscia M, de Ráfelis M, Renard M, Roux M, Shein E, Buestel D (2006) Experimental and natural cathodoluminescence in the shell of Crassostrea gigas from Thau lagoon (France): ecological and environmental implications. Mar Ecol Prog Ser 317:143–156CrossRefGoogle Scholar
  28. Lartaud F, Langlet D, de Rafelis M, Emmanuel L, Renard M (2006) Mise en evidence de rythmicité saisonnière dans la coquille des huîtres fossiles Crassostrea aginensis Tournouer, 1914 (Aquitanien) et Ostrea bellovacina Lanmarck, 1806 (Thanétien). Approche par cathodoluminiscence et par sclérochronologie. Geobios 39:845–852CrossRefGoogle Scholar
  29. Lartaud F, Emmanuel L, de Ráfelis M, Ropert M, Labourdette N, Richardson CA, Renard M (2010a) A latitudinal gradient of seasonal temperature variation recorded in oyster shells from the coastal waters of France and The Netherlands. Facies 56:13–25CrossRefGoogle Scholar
  30. Lartaud F, de Rafelis M, Ropert M, Emmanuel L, Geairon P, Renard M (2010b) Mn labelling of living oysters: Artificial and natural cathodoluminescence analyses as a tool for age and growth rate determination of C.gigas (Thunberg, 1793) shells. Aquaculture 300(1–4):206–217CrossRefGoogle Scholar
  31. Le Moullac G, Soyez C, Vidal-Dupiol J, Belliard C, Fievet J, Sham-Koua M, Lo-Yat A, Saulnier D, Gaertner-Mazouni N, Gueguen Y (2016) Impact of pCO2 on the energy, reproduction and growth of the shell of the pearl oyster Pinctada margaritifera. Estuar Coast Shelf Sci 182:274–282CrossRefGoogle Scholar
  32. Márquez F, Van Der Molen S (2011) Intraspecific shell-shape variation in the razor clam Ensis macha along the Patagonian coast. J Molluscan Stud 77(2):123–128.  https://doi.org/10.1093/mollus/eyq044 CrossRefGoogle Scholar
  33. Moran AL (2000) Calcein as a marker in experimental studies newly-hatched gastropods. Mar Biol 137:893–898CrossRefGoogle Scholar
  34. Morriconi ER, Calvo J (1979) Alternative reproductive strategies of Ostrea puelchana. Hydrobiologia 185:195–203CrossRefGoogle Scholar
  35. Morsan EM, Zaidman PC, Ocampo Reinaldo M, Ciocco N (2010) Population structure, distribution and harvesting of southern geoduck, Panopea abbreviata, in San Matías Gulf (Patagonia, Argentina). Sci Mar 74:763–772CrossRefGoogle Scholar
  36. Mouchi V, de Rafelis M, Lartaud F, Fialin M, Verrecchia EP (2013) Chemical labelling of oyster shells used for time-calibrated high-resolution Mg/Ca ratios: a tool for estimation of past seasonal temperature variations. Palaeogeogr Palaeoclimatol Palaeoecol 373:66–74CrossRefGoogle Scholar
  37. Pascual MS, Bocca AH (1988) Cultivo experimental de la ostra puelche, Ostrea puelchana D’Orb., en el Golfo San Matías, Argentina. In: Verreth J, Carrillo M, Zanuy S, Huisman EA (eds) Aquaculture research in Latin America. Pudoc, Wageningen, pp 329–345Google Scholar
  38. Pascual MS, Iribarne OO, Zampatti E, Bocca AH (1989) Female-Male interaction in the breeding system of the puelche oyster Ostrea puelchana d’Orbigny. J Exp Mar Biol Ecol 132:209–219CrossRefGoogle Scholar
  39. Pascual MS, Zampatti E, Iribarne O (2001) Population structure and demography of the puelche oyster (Ostrea puelchana, D’Orbigny, 1841) grounds in Northern Patagonia, Argentina. J Shellfish Res 20:1003–1010Google Scholar
  40. Piola AR, Scasso LM (1988) Circulación en el Golfo San Matías. Geoacta 15:33–51Google Scholar
  41. Powell EN, Morson JM, Ashton-Alcox KA, Kim Y (2013) Accommodation of the sex-ratio in eastern oysters Crassostrea virginica to variation in growth and mortality across the estuarine salinity gradient. J Mar Biol Assoc UK 93:533–555CrossRefGoogle Scholar
  42. Rasband W (1997–2016) ImageJ, U.S. National Institutes of Health, Bethesda, Maryland, USA. https://imagej.nih.gov/ij/
  43. Rhoads DC, Lutz RA (1980) Skeletal growth of aquatic organisms. Plenum, New YorkCrossRefGoogle Scholar
  44. Riascos J, Guzmán N, Laudien J, Heilmayer O, Oliva M (2007) Suitability of three stains to mark shells of Concholepas concholepas (Gastropoda) and Mesodesma donacium (Bivalvia). J Shellfish Res 26:43–49CrossRefGoogle Scholar
  45. Richardson CA (1990) Tidal rhythms in the shell secretion of living Bivalves. In: Brosche P, Sündermann J (eds) Earth’s rotation from Eons to Days. Springer, Berlin, HeidelbergGoogle Scholar
  46. Richardson CA (2001) Molluscs as archives of environmental change. Oceanogr Mar Biol 39:103–164Google Scholar
  47. Richardson CA, Collis SA, Ekaratne K, Dare P, Key D (1993) The age determination and growth rate of the European flat oyster, Ostrea edulis, in British waters determined from acetate peels of umbo growth lines. ICES J Mar Sci 50:493–500CrossRefGoogle Scholar
  48. Rivas A, Beier E (1990) Temperature and salinity fields in the Northpatagonic Gulfs. Oceanol Acta 13:15–20Google Scholar
  49. Sælen G, Lunde IL, Porten KW, Braga JC, Dundas SH, Ninnemann US, Ronen Y, Talbot MR (2016) Oyster Shells as recorders of short-term oscillations of salinity and temperature during deposition of coral bioherms and reefs in the Miocene Lorca Basin, SE Spain. J Sediment Res 86:637–667CrossRefGoogle Scholar
  50. Schöne BR (2008) The curse of physiology challenges and opportunities in the interpretation of geochemical data from mollusk shells. Geo Mar Lett 28:269–285CrossRefGoogle Scholar
  51. Shilts MH, Pascual MS, Foighil DÓ (2007) Systematic, taxonomic and biogeographic relationships of Argentine flat oysters. Mol Phylogenet Evol 44:467–473CrossRefPubMedGoogle Scholar
  52. Stenzel HB (1971) Oysters. In: Moore RC (ed) Treatise on invertebrate paleontology, Part N, Bivalvia. Geological Society of America, Boulder, pp N953–N1224Google Scholar
  53. Surge D, Lohmann KC, Dettman DL (2001) Controls on isotropic chemistry of the American oyster, Crassostrea virginica: implications for growth patterns. Palaeogeogr Palaeoclimatol Palaeoecol 172:283–296CrossRefGoogle Scholar
  54. Ullmann CV, Wiechert U, Korte C (2010) Oxygen isotope fluctuations in a modern North Sea oyster (Crassostrea gigas) compared with annual variations in seawater temperature: implications for palaeoclimate studies. Chem Geol 277:160–166CrossRefGoogle Scholar
  55. Zampatti E, Pascual MS (1989) Larval rearing, nursery growing and implantation at oyster parks of the Argentinian oyster, Ostrea puelchana D’Orb. Laboratoire de Pathologie et de Génétique des Invertébrés Marine. Technical report. IFREMER. La Tremblade. FranceGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • M. S. Doldan
    • 1
    • 2
    • 3
  • M. de Rafélis
    • 4
  • M. A. Kroeck
    • 2
    • 3
  • M. S. Pascual
    • 2
    • 3
  • E. M. Morsan
    • 3
  1. 1.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Ciudad Autónoma de Buenos AiresArgentina
  2. 2.Centro de Investigación Aplicada y Transferencia Tecnológica en Recursos Marinos “Almirante Storni” (CIMAS)Universidad Nacional del ComahueSan Antonio OesteArgentina
  3. 3.Escuela Superior de Ciencias MarinasUniversidad Nacional del ComahueSan Antonio OesteArgentina
  4. 4.Géosciences Environnement Toulouse, Université Paul Sabatier (UT 3)ToulouseFrance

Personalised recommendations