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Assessment of swimming behavior of the Pacific oyster D-larvae (Crassostrea gigas) following exposure to model pollutants

  • Perrine Gamain
  • Alicia Roméro-Ramirez
  • Patrice Gonzalez
  • Nicolas Mazzella
  • Pierre-Yves Gourves
  • Clémence Compan
  • Bénédicte Morin
  • Jérôme CachotEmail author
Multi-Stressors in Freshwater and Transitional Environments: from Legacy Pollutants to Emerging Ones
  • 34 Downloads

Abstract

This study describes an image analysis method that has been used to analyze the swimming behavior of native oyster D-larvae (Crassostrea gigas) from the Arcachon Bay (SW, France). In a second time, this study evaluated the impact of copper and S-metolachlor pollutants on D-larvae swimming activity and the possible relationship between developmental malformations and abnormal swimming behavior. Analyses in wild and cultivated oyster D-larvae were investigated during two breeding-seasons (2014 and 2015) at different sampling sites and dates. In controlled conditions, the average speed of larvae was 144 μm s−1 and the maximum speed was 297 μm s−1 while the trajectory is mainly rectilinear. In the presence of environmental concentration of copper or S-metolachlor, no significant difference in maximum or average larval speed was observed compared to the control condition but the percentage of circular trajectory increased significantly while the rectilinear swimming larvae significantly declined. The current study demonstrates that rectilinear trajectories are positively correlated to normal larvae while larvae with shell anomalies are positively correlated to circular trajectories. This abnormal behavior could affect the survival and spread of larvae, and consequently, the recruitment and colonization of new habitats.

Keywords

Copper Early life stage Image analysis Malformations S-metolachlor Speed Trajectory 

Notes

Acknowledgments

The authors thank the Aquitaine Region (OSQUAR Project), CPER A2E, Intermunicipal Union of Arcachon Bay (SIBA) and Water Agency Adour Garonne (AEAG) for their financial support. This work was part of the LABEX COTE cluster of excellence “Continental To coastal Ecosystems: evolution, adaptability and governance”. We thank James Emery for providing English proofreading.

References

  1. AFNOR XP T90-382 (2009) Qualité de l'eau - Bio indicateur de la toxicité potentielle de milieux aqueux - Détermination de la toxicité potentielle d'échantillons aqueux sur le développement embryo-larvaire de bivalve. p. 19Google Scholar
  2. Auby I, Bocquene G, Quiniou F, Dreno JP (2007) Etat de la contamination du Bassin d’Arcachon par les insecticides et les herbicides sur la période 2005-2006. Impact Environn 24:108 http://archimer.ifremer.fr/doc/00000/2398/ Google Scholar
  3. Auby I, Maurer D, Passoni S, Heroin D, Rigouin L, Méteigner C, Perrière-Rumèbe M, Tournaire M-P (2014) Reproduction de l’huître creuse dans le Bassin d'Arcachon Année 2014. Ifremer 55. https://www.researchgate.net/publication/271765196
  4. Caldwell CA, Jacobi GZ, Anderson MC, Parmenter RR, McGann J, Gould WR, DuBey R, Jacobi MD (2013) Prescribed-fire effects on an aquatic community of a Southwest Montane Grassland System. N Am J Fish Manag 33(5):1049–1062CrossRefGoogle Scholar
  5. Chevalier J, Harscoët E, Keller M, Pandard P, Cachot J, Grote M (2015) Exploration of Daphnia behavioral effect profiles induced by a broad range of toxicants with different modes of action. Environ Toxicol Chem 34:1760–1769CrossRefGoogle Scholar
  6. Faimali M, Gambardella C, Costa E, Piazza V, Morgana S, Estevez-Calvar N, Garaventa F (2017) Old model organisms and new behavioral end-points: swimming alteration as an ecotoxicological response. Mar Environ Res 128:36–45CrossRefGoogle Scholar
  7. FAO (2019) Fisheries and aquaculture Department. Fish Stat Crassostrea gigas (Thunberg, 1793). http://www.fao.org/fishery/species/3514/
  8. Festa RA, Thiele DJ (2011) Copper: an essential metal in biology. Curr Biol 21:R877–R883CrossRefGoogle Scholar
  9. Flemming CA, Trevors JT (1989) Copper toxicity and chemistry in the environment: a review. Water Air Soil Pollut 44:143–158CrossRefGoogle Scholar
  10. Gamain P, Gonzalez P, Cachot J, Pardon P, Tapie N, Gourves PY, Budzinski H, Morin B (2016) Combined effects of pollutants and salinity on embryo-larval development of the Pacific oyster, Crassostrea gigas. Mar Environ Res 113:31–38CrossRefGoogle Scholar
  11. Gamain P, Gonzalez P, Cachot J, Clérandeau C, Mazzella N, Gourves P-Y, Morin B (2017a) Combined effects of temperature and copper and S-metolachlor on embryo-larval development of the Pacific oyster, Crassostrea gigas. Mar Pollut Bull 115:201–210CrossRefGoogle Scholar
  12. Gamain P, Cachot J, Gonzalez P, Budzinski H, Gourves P-Y, Morin B (2017b) Do temporal and spatial parameters or lifestyle of the Pacific oyster Crasssostrea gigas affect pollutant bioaccumulation, offspring development and tolerance to pollutants? Front Mar Sci 4:58.  https://doi.org/10.3389/fmars.2017.00058 CrossRefGoogle Scholar
  13. Garaventa F, Gambardella C, Di Fino A, Pittore M, Faimali M (2010) Swimming speed alteration of Artemia sp. and Brachionus plicatilis as a sub-lethal behavioural end-point for ecotoxicological survey. Ecotoxicology 19:512–519CrossRefGoogle Scholar
  14. Handy RD, Sims DW, Giles A, Campbell HA, Musonda MM (1999) Metabolic trade-off between locomotion and detoxification for maintenance of blood chemistry and growth parameters by rainbow trout (Oncorhynchus mykiss) during chronic dietary exposure to copper. Aquat Toxicol 47:23–41CrossRefGoogle Scholar
  15. His E, Beiras R, Seaman MNL (1999) The assessment of marine pollution bioassays with bivalve embryos and larvae. Adv Mar Biol 37:1–178CrossRefGoogle Scholar
  16. Horiguchi T, Imai T, Cho HS, Shiraishi H, Shibata Y, Morita M, Shimizu M (1998) Acute toxicity of organotin compounds to the larvae of the rock shell, Thais clavigera, the disk abalone, Haliotis discus discus and the giant abalone, Haliotis madaka. Mar Environ Res 46:469–473CrossRefGoogle Scholar
  17. Kapur JN, Sahoo PK, Wong AKC (1985) A new method for gray-level picture thresholding using the entropy of the histogram. Computer Vis Graph Image Process 29:273–285Google Scholar
  18. Kazlauskiene N, Svecevičius G, Petrauskiene L, Vosyliene MZ (2010) Behavioural responses of medicinal leech and rainbow trout exposed to crude oil and heavy fuel oil in ontogenesis. Pol J Environ Stud 19:429–433Google Scholar
  19. Kokkali V, Katramados I, Newman JD (2011) Monitoring the effect of metal ions on the mobility of Artemia salina Nauplii. Biosensors 1:36–45CrossRefGoogle Scholar
  20. Kwok CK, Ang PO (2013) Inhibition of larval swimming activity of the coral (Platygyra acuta) by interactive thermal and chemical stresses. Mar Pollut Bull 74:264–273Google Scholar
  21. LaBreche TMC, Dietrich AM, Gallagher DL, Shepherd N (2002) Copper toxicity to larval Mercenaria mercenaria (hard clam). Environ Toxicol Chem 21:760–766CrossRefGoogle Scholar
  22. Le Bihanic F, Sommard V, de Lansalut P, Anaïk P, Grasset J, Berrada S, Budzinski H, Cousin X, Morin B, Cachot J (2015) Environmental concentrations of benz[a]anthracene induce developmental defects and DNA damage and impair photomotor response in Japanese medaka larvae. Ecotox Environ Safe 113:321–328Google Scholar
  23. Legendre P, Legendre L (1998) Numerical ecology. Transformation:1–4Google Scholar
  24. Lissalde S, Mazzella N, Fauvelle V, Delmas F, Mazellier P, Legube B (2011) Liquid chromatography coupled with tandem mass spectrometry method for thirty-three pesticides in natural water and comparison of performance between classical solid phase extraction and passive sampling approaches. J Chromatogr A 1218(11):1492–1502CrossRefGoogle Scholar
  25. Lv Z, Tek A, Da Silva F, Empereur-mot C, Chavent M, Baaden M (2013) Game on, science - how video game technology may help biologists tackle visualization challenges. Plos One.  https://doi.org/10.1371/journal.pone.0057990
  26. Mai H, Cachot J, Brune J, Geffard O, Belles A, Budzinski H, Morin B (2012) Embryotoxic and genotoxic effects of heavy metals and pesticides on early life stages of Pacific oyster (Crassostrea gigas). Mar Pollut Bull 64:2663–2670CrossRefGoogle Scholar
  27. Mai H, Morin B, Pardon P, Gonzalez P, Budzinski H, Cachot J (2013) Environmental concentrations of irgarol, diuron and S-metolachlor induce deleterious effects on gametes and embryos of the Pacific oyster, Crassostrea gigas. Mar Environ Res 89:1–8CrossRefGoogle Scholar
  28. Martin JM, Saaristo M, Bertram MG, Lewis PJ, Coggan TL, Clarke BO, Wong BBM (2017) The psychoactive pollutant fluoxetine compromises antipredator behaviour in fish. Environ Pollut 222:592–599CrossRefGoogle Scholar
  29. McCallum ES, Krutzelmann E, Brodin T, Fick J, Sundelin A, Balshine S (2017) Exposure to wastewater effluent affects fish behaviour and tissue-specific uptake of pharmaceuticals. Sci Total Environ 605-606:578–588CrossRefGoogle Scholar
  30. Melvin SD, Wilson SP (2013) The utility of behavioral studies for aquatic toxicology testing: a meta-analysis. Chemosphere 93:2217–2223CrossRefGoogle Scholar
  31. Mileikovsky SA (1973) Speed of active movement of pelagic larvae of marine bottom invertebrates and their ability to regulate their vertical position. Mar Biol 23:11–17CrossRefGoogle Scholar
  32. Morgana S, Gambardella C, Falugi C, Pronzato R, Garaventa F, Faimali M (2016) Swimming speed alteration in the early developmental stages of Paracentrotus lividus sea urchin as ecotoxicological endpoint. Mar Environ Res 115:11–19CrossRefGoogle Scholar
  33. Nussbaum-Krammer CI, Neto MF, Brielmann RM, Pedersen JS, Morimoto RI (2015) Investigating the spreading and toxicity of prion-like proteins using the metazoan model organism C. elegans. J Vis Exp (95):e52321Google Scholar
  34. Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68:369–392CrossRefGoogle Scholar
  35. Sommers F, Mudrock E, Labenia J, Baldwin D (2016) Effects of salinity on olfactory toxicity and behavioral responses of juvenile salmonids from copper. Aquat Toxicol 175:260–268CrossRefGoogle Scholar
  36. Suquet M, Le Mercier A, Rimon F, Mingant C, Haffray P, Labbe C (2012) Setting tools for the early assessment of the quality of thawed Pacific oyster (Crassostrea gigas) D-larvae. Theriogenology 78:462–467CrossRefGoogle Scholar
  37. Suquet M, Rimond F, Cosson J, Wilson-Leedy J, Lebrun L, Queau I, Mingant C, Fauve C (2013) Effect of age and environmental conditions on the movement characteristics of Pacific oyster (Crassostrea gigas) trochophores. J Appl Ichthyol 29:1145–1148CrossRefGoogle Scholar
  38. Tapie N, Chevance DL, Budzinski H (2017) Repar pesticides : quantification de la présence dans les eaux, année 2012, 22 p. https://www.siba-bassin-arcachon.fr/actions-environnementales/bibliotheque-environnementale/repar-quantification-de-la-presence-dans-les-eaux
  39. Troost K, Veldhuizen R, Stamhuis EJ, Wolff WJ (2008) Can bivalve veligers escape feeding currents of adult bivalves? J Exp Mar Biol Ecol 358:185–196CrossRefGoogle Scholar
  40. Turner A (2010) Marine pollution from antifouling paint particles. Mar Pollut Bull 60:159–171CrossRefGoogle Scholar
  41. Van der Schalie WH, Shedd TR, Knechtges PL, Widder MW (2001) Using higher organisms in biological early warning systems for real-time toxicity detection. Biosens Bioelectron 16:457–465CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Perrine Gamain
    • 1
  • Alicia Roméro-Ramirez
    • 1
  • Patrice Gonzalez
    • 1
  • Nicolas Mazzella
    • 2
  • Pierre-Yves Gourves
    • 1
  • Clémence Compan
    • 1
  • Bénédicte Morin
    • 1
  • Jérôme Cachot
    • 1
    Email author
  1. 1.Univ. Bordeaux, EPOCPessacFrance
  2. 2.IRSTEA, UR EABX (Water Research Unit)Cestas CedexFrance

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