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How life history contributes to stress response in the Manila clam Ruditapes philippinarum

  • Ika Paul-PontEmail author
  • Xavier de Montaudouin
  • Patrice Gonzalez
  • Philippe Soudant
  • Magalie Baudrimont
Research Article

Abstract

Introduction

Within the last decade, numerous studies have investigated the role of environmental history on tolerance to stress of many organisms. This study aims to assess if Manila clams Ruditapes philippinarum may react differently to cadmium exposure and trematode parasite infection (Himasthla elongata) depending on their origin and environmental history in Arcachon Bay (France).

Materials and methods

Clams were exposed to Cd (15 µg L−1) and parasites (25 cercariae per clam), alone or in combination, at 15°C under controlled laboratory conditions for 7 days. Metal accumulation and success of parasite infestation were examined, also physiological parameters such as metallothionein response and hemocyte counts and activities (phagocytosis, oxidative burst, viability, and adhesion).

Results and Discussion

Sensitivity of Manila clams to both stressors differed from one site to another, suggesting local adaptation of populations. Clams from the more parasitized site presented better resistance to trematodes than the others in terms of first line defense, i.e., avoidance of infection. On the other hand, clams that adapted to chronic Cd contamination showed better detoxification mechanisms, both in a faster transfer of metal from gills to visceral mass and in a higher metallothionein baseline, than clams which had never experienced Cd contamination. Finally, hemocyte concentration and viability differed between clam origin site, highlighting the fact that populations living in different environments may adapt their physiological and biochemical responses to environmental stressors.

Conclusion

It is therefore important to be cautious when extrapolating results from field studies of one species and one site, if the life history of the organisms is not taken into account.

Keywords

Ruditapes philippinarum Cadmium Trematode parasite Metallothionein Immunity Life history 

Notes

Acknowledgments

This work was carried out with the financial support of the “Région Aquitaine” and the French National Research Agency with the funds of the “multistress project”. The authors are grateful to sailor Francis Prince, to Pascal Lebleu, Henri Bouillard, and students Frances Haynes and Željka Trumbić, for their valuable help in the field, for their assistance in the laboratory, and for all technical support before and during the experiment.

References

  1. Allam B, Paillard C, Ford SE (2002) Pathogenicity of Vibrio tapetis, the etiological agent of brown ring disease. Dis Aquat Org 48:221–231CrossRefGoogle Scholar
  2. Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202CrossRefGoogle Scholar
  3. Auffret M, Oubella R (1994) Cytometric parameters of bivalve molluscs: effect of environmental factors. In: Stolen JS, Fletcher TC (eds), Models of fish immune responses. SOS Publications, Fair Haven, USA, pp 23–32Google Scholar
  4. Baudrimont M, de Montaudouin X (2007) Evidence of altered protective effect of metallothioneins after cadmium exposure in the digenean parasite-infected cockle (Cerastoderma edule). Parasitology 134:237–245CrossRefGoogle Scholar
  5. Baudrimont M, Lemaire-Gony S, Ribeyre F, Métivaud J, Boudou A (1997) Seasonal variations of metallothionein concentrations in the Asiatic clam (Corbicula fluminea). Comp Biochem Physiol—Part C Pharmacol Toxicol Endocrinol 118:361–367CrossRefGoogle Scholar
  6. Baudrimont M, Andres S, Durrieu G, Boudou A (2003) The key role of metallothioneins in the bivalve Corbicula fluminea during the depuration phase, after in situ exposure to Cd and Zn. Aquat Toxicol 63:89–102CrossRefGoogle Scholar
  7. Baudrimont M, de Montaudouin X, Palvadeau A (2006) Impact of digenean parasite infection on metallothionein synthesis by the cockle (Cerastoderma edule): a multivariate field monitoring. Mar Pollut Bull 52:494–502CrossRefGoogle Scholar
  8. Bebianno MJ, Serafim MAP, Rita MF (1994) Involvement of metallothionein in cadmium accumulation and elimination in the clam Ruditapes decussata. Bull Environ Contam Toxicol 53:726–732CrossRefGoogle Scholar
  9. Bervoets L, Voets J, Chu S, Covaci A, Schepens P, Blust R (2004) Comparison of accumulation of micropollutants between indigenous and transplanted zebra mussels (Dreissena polymorpha). Environ Toxicol Chem 23:1973–1983CrossRefGoogle Scholar
  10. Blackmore G, Wang WX (2002) Uptake and efflux of Cd and Zn by the green mussel Perna viridis after metal preexposure. Environ Sci Technol 36:989–995CrossRefGoogle Scholar
  11. Blackmore G, Wang WX (2003) Comparison of metal accumulation in mussels at different local and global scales. Environ Toxicol Chem 22:388–395CrossRefGoogle Scholar
  12. Blanchet H, de Montaudouin X, Lucas A, Chardy P (2004) Heterogeneity of macrozoobenthic assemblages within a Zostera noltii seagrass bed: diversity, abundance, biomass and structuring factors. Estuar Coast Shelf Sci 61:111–123CrossRefGoogle Scholar
  13. Blanchet H, de Montaudouin X, Chardy P, Bachelet G (2005) Structuring factors and recent changes in subtidal macrozoobenthic communities of a coastal lagoon, Arcachon Bay (France). Estuar Coast Shelf Sci 64:561–576CrossRefGoogle Scholar
  14. Boisson F, Hartl MGJ, Fowler SW, Amiard-Triquet C (1998) Influence of chronic exposure to silver and mercury in the field on the bioaccumulation potential of the bivalve Macoma balthica. Mar Environ Res 45:325–340CrossRefGoogle Scholar
  15. Bryan-Walker K, Leung TLF, Poulin R (2007) Local adaptation of immunity against a trematode parasite in marine amphipod populations. Mar Biol 152:687–695CrossRefGoogle Scholar
  16. Cajaraville MP, Olabarrieta I, Marigomez I (1996) In vitro activities in mussel hemocytes as biomarkers of environmental quality: a case study in the Abra Estuary (Biscay Bay). Ecotoxicol Environ Saf 35:253–260CrossRefGoogle Scholar
  17. Chan MK, Othman R, Zubir D, Salmijah S (2002) Induction of a putative metallothionein gene in the blood cockle, Anadara granosa, exposed to cadmium. Comp Biochem Physiol 131:123–132Google Scholar
  18. Cheng TC (1988) In vivo effects of heavy metals on cellular defense mechanisms of Crassostrea virginica: total and differential cell counts. J Invertebr Pathol 51:207–214CrossRefGoogle Scholar
  19. Cheng TC (1996) Hemocytes: forms and functions. In: Kennedy VS, Newell RIE, Eble AF (eds) The eastern oyster Crassostrea virginica by Maryland. Maryland Sea Grant, College Park, pp 299–333Google Scholar
  20. Chu F-LE (2000) Defense mechanisms of marine bivalves. Recent Adv Mar Biotech 5:1–42Google Scholar
  21. Coles JA, Pipe RK (1994) Phenoloxidase activity in the haemolymph and haemocytes of the marine mussel Mytilus edulis. Fish Shellfish Immunol 4:337–352CrossRefGoogle Scholar
  22. Dang C (2009) Dynamique des populations de palourdes japonaises (Ruditapes philippinarum) dans le bassin d'Arcachon—Conséquences sur la gestion des stocks exploités. Ph.D. thesis, University Bordeaux 1Google Scholar
  23. Dang C, De Montaudouin X, Gonzalez P, Mesmer-Dudons N, Caill-Milly N (2008) Brown muscle disease (BMD), an emergent pathology affecting Manila clam Ruditapes philippinarum in Arcachon Bay (SW France). Dis Aquat Org 80:219–228CrossRefGoogle Scholar
  24. Dang C, De Montaudouin X, Bald J, Jude F, Raymond N, Lanceleur L, Paul-Pont I, Caill-Milly N (2009a) Testing the enemy release hypothesis: trematode parasites in the non indigenous Manila clam Ruditapes philippinarum. Hydrobiologia 630:139–148CrossRefGoogle Scholar
  25. Dang C, Sauriau P-G, Savoye N, Caill-Milly N, Martinez P, Millaret C, Haure J, de Montaudouin X (2009b) Determination of diet in Manila clams by spatial analysis of stable isotopes. Mar Ecol Prog Ser 387:167–177Google Scholar
  26. Delaporte M, Soudant P, Moal J, Lambert C, Quéré C, Miner P, Choquet G, Paillard C, Samain J-F (2003) Effect of a mono-specific algal diet on immune functions in two bivalve species Crassostrea gigas and Ruditapes philippinarum. J Exp Biol 206(17):3053–3064CrossRefGoogle Scholar
  27. De Montaudouin X, Thieltges DW, Gam M, Krakau M, Pina S, Bazaïri H, Dabouineau L, Russell-Pinto F, Jensen KT (2009) Review—Digenean trematode species in the cockle Cerastoderma edule: identification key and distribution along the North-East Atlantic shoreline. J Mar Biol Ass UK 80:543–556CrossRefGoogle Scholar
  28. Desclaux C (2003) Interactions hôtes-parasites : diversité, mécanismes d'infestation et impact des trématodes digènes sur les coques Cerastoderma edule (mollusque bivalve) en milieu lagunaire macrotidal. Ph.D. thesis, University Bordeaux 1Google Scholar
  29. Desclaux C, de Montaudouin X, Bachelet G (2004) Cockle (Cerastoderma edule) population mortality: the role of the digenean parasite Himasthla quissetensis. Mar Ecol Prog Ser 279:141–150CrossRefGoogle Scholar
  30. Donaghy L, Lambert C, Choi K-S, Soudant P (2009) Hemocytes of the carpet shell clam (Ruditapes decussatus) and the Manila clam (Ruditapes philippinarum): current knowledge and future prospects. Aquaculture 297(1–4):10–24Google Scholar
  31. Dutton MD, Stephenson M, Klaverkamp JF (1993) A mercury saturation assay for measuring metallothioneins in fish. Environ Toxicol Chem 12:1193–1202CrossRefGoogle Scholar
  32. Eränen JK (2006) Local adaptation of mountain birch to heavy metals in subarctic industrial barrens. For Snow Land Res 80:161–167Google Scholar
  33. Fisher WS, Oliver LM, Walker WW, Manning CS, Lytle TF (1999) Decreased resistance of eastern oysters (Crassostrea virginica) to a protozoan pathogen (Perkinsus marinus) after sublethal exposure to tributyltin oxide. Mar Environ Res 47:185–201CrossRefGoogle Scholar
  34. Fraysse B, Geffard O, Berthet B, Quéau H, Biagianti-Risbourg S, Geffard A (2006) Importance of metallothioneins in the cadmium detoxification process in Daphnia magna. Comp Biochem Physiol—C Toxicol Pharmacol 144:286–293CrossRefGoogle Scholar
  35. Gagné F, Blaise C, Pellerin J, André C (2007) Neuroendocrine disruption in Mya arenaria clams during gametogenesis at sites under pollution stress. Mar Environ Res 64:87–107CrossRefGoogle Scholar
  36. Gam M, de Montaudouin X, Bazaïri H (2009) Do trematode parasites affect cockle (Cerastoderma edule) secondary production and elimination? J Mar Biol Ass UK 89:1395–1402Google Scholar
  37. Géret F, Serafim A, Barreira L, Bebianno MJ (2002) Effect of cadmium on antioxidant enzyme activities and lipid peroxidation in the gills of the clam Ruditapes decussatus. Biomarkers 7:242–256CrossRefGoogle Scholar
  38. Géret F, Serafim A, Bebianno MJ (2003) Antioxidant enzyme activities, metallothioneins and lipid peroxidation as biomarkers in Ruditapes decussatus? Ecotoxicology 12:417–426CrossRefGoogle Scholar
  39. Glé C (2007) Structure et dynamique des communautés microbiennes autotrophes et production primaire planctonique dans une lagune côtière macrotidale, le Bassin d'Arcachon. Facteurs de contrôle de type bottom-up. Ph.D. thesis, University Bordeaux 1Google Scholar
  40. Griscom SB, Fisher NS (2004) Bioavailability of sediment-bound metals to marine bivalve molluscs: an overview. Estuaries 27:826–838CrossRefGoogle Scholar
  41. Hégaret H, Wikfors GH (2005) Effects of natural and field-simulated blooms of the dinoflagellate Prorocentrum minimum upon hemocytes of eastern oysters, Crassostrea virginica, from two different populations. Harmful Algae 4:201–209CrossRefGoogle Scholar
  42. Kim Y, Powell EN (2007) Distribution of parasites and pathologies in sentinel bivalves: NOAA status and trends “Mussel Watch” program. J Shellfish Res 26:1115–1151CrossRefGoogle Scholar
  43. Klerks PL, Weis JS (1987) Genetic adaptation to heavy metals in aquatic organisms: a review. Environ Pollut 45:173–205CrossRefGoogle Scholar
  44. Lambert C, Soudant P, Choquet G, Paillard C (2003) Measurement of Crassostrea gigas hemocytes oxidative metabolism by flow cytometry and the inhibiting capacity of pathogenic vibrios. Fish Shellfish Immunol 15(3):224–240CrossRefGoogle Scholar
  45. Langston W, Bebianno MJ, Burt GR (1998) Metal handling strategies in molluscs. In: Langston WJ, Bebianno MJ (eds) Metal metabolism in aquatic environments, Chapman and Hall, London, pp 219–284Google Scholar
  46. Lapanje A, Drobne D, Nolde N, Valant J, Muscet B, Leser V, Rupnik M (2008) Long-term Hg pollution induced Hg tolerance in the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Environ Pollut 153:537–547CrossRefGoogle Scholar
  47. Lassalle G, de Montaudouin X, Soudant P, Paillard C (2007) Parasite co-infection of two sympatric bivalves, the Manila clam (Ruditapes philippinarum) and the cockle (Cerastoderma edule) along a latitudinal gradient. Aquat Living Resour 20:33–42CrossRefGoogle Scholar
  48. Lee M-K, Cho B-Y, Lee SJ, Kang J-Y, Jeong HD, Huh SH, Huh M-D (2001) Histopathological lesions of Manila clam, Tapes philippinarum, from Hadong and Namhae coastal areas of Korea. Aquaculture 201:199–209CrossRefGoogle Scholar
  49. MacKenzie K, Williams HH, Williams B, McVicar AH, Siddall R (1995) Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Adv Parasitol 35:85–144CrossRefGoogle Scholar
  50. Morley NJ, Irwin SWB, Lewis JW (2003a) Pollution toxicity to the transmission of larval digeneans through their molluscan hosts. Parasitology 126:S5–S26CrossRefGoogle Scholar
  51. Morley NJ, Crane M, Lewis JW (2003b) Effects of cadmium and zinc toxicity on orientation behaviour of Echinoparyphium recurvatum (Digenea: Echinostomatidae) cercariae. Dis Aquat Org 56:89–92CrossRefGoogle Scholar
  52. Morley NJ, Crane M, Lewis JW (2004) Influence of cadmium exposure on the incidence of first intermediate host encystment by Echinoparyphium recurvatum cercariae in Lymnaea peregra. J Helminthol 78:329–332CrossRefGoogle Scholar
  53. Morley NJ, Crane M, Lewis JW (2005) Changes in survival characteristics of Diplostomum spathaceum cercariae emerged from cadmium-exposed Lymnaea stagnalis. J Helminthol 79:55–59CrossRefGoogle Scholar
  54. Nacci DE, Champlin D, Coiro L, McKinney R, Jayaraman S (2002) Predicting the occurrence of genetic adaptation to dioxinlike compounds in populations of the estuarine fish Fundulus heteroclitus. Environ Toxicol Chem 21:1525–1532Google Scholar
  55. Ng TY-T, Wang W-X (2004) Detoxification and effects of Ag, Cd, and Zn pre-exposure on metal uptake kinetics in the clams Ruditapes philippinarum. Mar Ecol Prog Ser 268:161–172CrossRefGoogle Scholar
  56. Ngo TTT, Choi K-S (2004) Seasonal changes of Perkinsus and Cercaria infections in the Manila clam Ruditapes philippinarum from Jeju, Korea. Aquaculture 239:57–68CrossRefGoogle Scholar
  57. Ownby DR, Newman MC, Mulvey M, Vogelbein WK, Unger MA, Arzayus LF (2002) Fish (Fundulus heteroclitus) populations with different exposure histories differ in tolerance of creosote-contaminated sediments. Environ Toxicol Chem 21:1897–1902Google Scholar
  58. Piola RF, Johnston EL (2006) Differential tolerance to metals among populations of the introduced bryozoan Bugula neritina. Mar Biol 148:997–1010CrossRefGoogle Scholar
  59. Pipe RK, Coles JA (1995) Environmental contaminants influencing immunefunction in marine bivalve molluscs. Fish Shellfish Immunol 5:581–595CrossRefGoogle Scholar
  60. Reid HI, Soudant P, Lambert C, Paillard C, Birkbeck TH (2003) Salinity effects on immune parameters of Ruditapes philippinarum challenged with Vibrio tapetis. Dis Aquat Org 56:249–258CrossRefGoogle Scholar
  61. Ross K, Cooper N, Bidwell JR, Elder J (2002) Genetic diversity and metal tolerance of two marine species: a comparison between populations from contaminated and reference sites. Mar Pollut Bull 44:671–679CrossRefGoogle Scholar
  62. Serafim MA, Company RM, Bebianno MJ, Langston WJ (2002) Effect of temperature and size on metallothionein synthesis in the gill of Mytilus galloprovincialis exposed to cadmium. Mar Environ Res 54:361–5CrossRefGoogle Scholar
  63. Shirley MDF, Sibly RM (1999) Genetic basis of a between-environment trade-off involving resistance to cadmium in Drosophila melanogaster. Evolution 53:826–836CrossRefGoogle Scholar
  64. Shi D, Wang WX (2004) Understanding the differences in Cd and Zn bioaccumulation and subcellular storage among different populations of marine clams. Environ Sci Technol 38:449–456CrossRefGoogle Scholar
  65. Shi DL, Wang W-X (2005) Uptake of aqueous and dietary metals by mussel Perna viridis with different Cd exposure histories. Environ Sci Tech 39:9363–9369CrossRefGoogle Scholar
  66. Shi D, Blackmore G, Wang WX (2003) Effects of aqueous and dietary preexposure and resulting body burden on silver biokinetics in the green mussel Perna viridis. Environ Sci Technol 37:936–943CrossRefGoogle Scholar
  67. Smaoui-Damak W, Hamza-Chaffai A, Bebianno MJ, Amiard JC (2004) Variation of metallothioneins in gills of the clam Ruditapes decussatus from the Gulf of Gabès (Tunisia). Comp Biochem Physiol—C Toxicol Pharmacol 139:181–188CrossRefGoogle Scholar
  68. Smaoui-Damak W, Berthet B, Hamza-Chaffai A (2009) In situ potential use of metallothionein as a biomarker of cadmium contamination in Ruditapes decussatus. Ecotoxicol Environ Saf 72:1489–1498CrossRefGoogle Scholar
  69. Soudant P, Paillard C, Choquet G, Lambert C, Reid HI, Marhic A, Donaghy L, Birkbeck TH (2004) Impact of season and rearing site on the physiological and immunological parameters of the Manila clam Venerupis (=Tapes, =Ruditapes) philippinarum. Aquaculture 229:401–418CrossRefGoogle Scholar
  70. Sures B (2008) Environmental parasitology. Interactions between parasites and pollutants in the aquatic environment. Parasite 15:434–438Google Scholar
  71. Valtonen ET, Holmes JC, Koskivaara M (1997) Eutrophication, pollution, and fragmentation: effects on parasite communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in central Finland. Can J Fish Aquat Sci 54:572–585CrossRefGoogle Scholar
  72. Viarengo A (1989) Heavy metals in marine invertebrates: mechanisms of regulation and toxicity at the cellular level. Aquat Sci 1:295–317Google Scholar
  73. Walne PR, Mann R (1975) Growth and biogeochemical composition in Ostrea edulis and Crassostrea gigas. In: Barnes H (ed) 9th European marine biology symposium. Aberdeen University Press, Aberdeen, pp 587–607Google Scholar
  74. Wang WX, Rainbow PS (2005) Influence of metal exposure history on trace metal uptake and accumulation by marine invertebrates. Ecotoxicol Environ Saf 61:145–159CrossRefGoogle Scholar
  75. Wegeberg AM, de Montaudouin X, Jensen KT (1999) Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of three Himasthla species (Echinostomatidae, Trematoda). J Exp Mar Biol Ecol 238:259–269CrossRefGoogle Scholar
  76. Werding B (1969) Morphologie, Entwicklung und Ökologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Mar Biol 3:306–333CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Ika Paul-Pont
    • 1
    Email author
  • Xavier de Montaudouin
    • 1
  • Patrice Gonzalez
    • 1
  • Philippe Soudant
    • 2
  • Magalie Baudrimont
    • 1
  1. 1.UMR 5805 CNRS, Station Marine d’ArcachonUniversité Bordeaux 1ArcachonFrance
  2. 2.IUEM, LEMAR UMR 6539 CNRSUniversité de Bretagne OccidentalePlouzanéFrance

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