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Evolution of cadmium tolerance and associated costs in a Gammarus fossarum population inhabiting a low-level contaminated stream

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Abstract

Deciphering evolutionary processes occurring within long-term contaminated wild populations is essential for the ecological risk assessment of persistent chemical contaminations. Using field populations of Gammarus, a commonly-used genus in aquatic ecotoxicology, the present study sought to gain insights into the extent to which long-term exposure to metals in the field could effectively lead to shifts in toxicological sensitivities. For this, we identified a Gammarus population inhabiting a stream contaminated by cadmium (Cd). We compared the Cd-exposure and Cd-sensitivity of this population to those of five reference populations. Active biomonitoring determined in different years and seasons that significant levels of Cd were bioavailable in the contaminated site. Laboratory sensitivity tests under common garden conditions established that this long-term field exposure led to the development of a moderate Cd tolerance, which was maintained after a 3-week acclimatization in the laboratory, and transmitted to offspring produced under clean conditions. The potential physiological costs of tolerance were assessed by means of feeding rate measurements (in the laboratory and in situ). They revealed that, unlike for reference populations, the feeding activity of organisms from the tolerant population was greatly decreased when they were maintained under laboratory conditions, potentially indicating a high population vulnerability to environmental perturbations. Because dissolved Cd concentrations in water from the contaminated site were low (averaging 0.045 µg L−1) and below the current European environmental quality standard for Cd for inland surface waters (fixed at 0.08 µg L−1 in soft water environments), this case study sheds light onto the extent to which current environmental quality standards are protective against potential adverse outcomes of adaptive and micro-evolutionary processes occurring in contaminated environments.

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References

  • Agra AR, Soares AMVM, Barata C (2011) Life-history consequences of adaptation to pollution. “Daphnia longispina clones historically exposed to copper”. Ecotoxicology 20:552–562. doi:10.1007/s10646-011-0621-5

    Article  CAS  Google Scholar 

  • Amiard-Triquet C, Cossu-Leguille C, Mouneyrac C (2013) Biomarkers of defense, tolerance and ecological consequences. In: Amiard-Triquet C, Amiard JC, Rainbow PS (eds) Ecological biomarkers: indicators of ecotoxicological effects. CRC Press, Boca Raton, pp 45–72

    Google Scholar 

  • Baird DJ, Brown SS, Lagadic L, Liess M, Maltby L, Moreira-Santos M, Schulz R, Scott GI (2007) In situ-based effects measures: determining the ecological relevance of measured responses. Integr Environ Assess Manag 3:259–267. doi:10.1897/IEAM_2006-031.1

    Article  Google Scholar 

  • Besse J-P, Coquery M, Lopes C, Chaumot A, Budzinski H, Labadie P, Geffard O (2013) Caged Gammarus fossarum (Crustacea) as a robust tool for the characterization of bioavailable contamination levels in continental waters: towards the determination of threshold values. Water Res 47:650–660. doi:10.1016/j.watres.2012.10.024

    Article  CAS  Google Scholar 

  • Bickham JW (2011) The four cornerstones of evolutionary toxicology. Ecotoxicology 20:497–502. doi:10.1007/s10646-011-0636-y

    Article  CAS  Google Scholar 

  • Boets P, Lock K, Goethals PLM, Janssen CR, De Schamphelaere KAC (2012) A comparison of the short-term toxicity of cadmium to indigenous and alien gammarid species. Ecotoxicology 21:1135–1144. doi:10.1007/s10646-012-0868-5

    Article  CAS  Google Scholar 

  • Chaumot A, Gos P, Garric J, Geffard O (2009) Additive vs non-additive genetic components in lethal cadmium tolerance of Gammarus (Crustacea): novel light on the assessment of the potential for adaptation to contamination. Aquat Toxicol 94:294–299. doi:10.1016/j.aquatox.2009.07.015

    Article  CAS  Google Scholar 

  • Chiodi Boudet L, Polizzi P, Romero MB, Robles A, Gerpe M (2013) Lethal and sublethal effects of cadmium in the white shrimp Palaemonetes argentinus: a comparison between populations from contaminated and reference sites. Ecotoxicol Environ Saf 89:52–58. doi:10.1016/j.ecoenv.2012.11.008

    Article  CAS  Google Scholar 

  • Coulaud R, Geffard O, Xuereb B, Lacaze E, Quéau H, Garric J, Charles S, Chaumot A (2011) In situ feeding assay with Gammarus fossarum (Crustacea): modelling the influence of confounding factors to improve water quality biomonitoring. Water Res 45:6417–6429. doi:10.1016/j.watres.2011.09.035

    Article  CAS  Google Scholar 

  • Coulaud R, Geffard O, Vigneron A, Quéau H, François A, Chaumot A (2015) Linking feeding inhibition with reproductive impairment in Gammarus confirms the ecological relevance of feeding assays in environmental monitoring. Environ Toxicol Chem. 34:1031–1038. doi:10.1002/etc.2886

    Article  CAS  Google Scholar 

  • Coutellec M-A, Barata C (2011) An introduction to evolutionary processes in ecotoxicology. Ecotoxicology 20:493–496. doi:10.1007/s10646-011-0637-x

    Article  CAS  Google Scholar 

  • Coutellec M-A, Barata C (2013) Special issue on long-term ecotoxicological effects: an introduction. Ecotoxicology 22:763–766. doi:10.1007/s10646-013-1092-7

    Article  CAS  Google Scholar 

  • De Coninck DI, Janssen CR, De Schamphelaere KA (2014) An approach to assess the regulatory relevance of microevolutionary effects in ecological risk assessment of chemicals: a case study with cadmium. Environ Toxicol Chem 33:453–457. doi:10.1002/etc.2434

    Article  Google Scholar 

  • European Parliament, Council of the European Union (2013) Directive 2013/39/EU of the European Parliament and of the Council of 12 August 2013 amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy. Off J Eur Union L 226:1–17

    Google Scholar 

  • Feckler A, Thielsch A, Schwenk K, Schulz R, Bundschuh M (2012) Differences in the sensitivity among cryptic lineages of the Gammarus fossarum complex. Sci Total Environ 439:158–164. doi:10.1016/j.scitotenv.2012.09.003

    Article  CAS  Google Scholar 

  • Forrow DM, Maltby L (2000) Toward a mechanistic understanding of contaminant-induced changes in detritus processing in streams: direct and indirect effects on detritivore feeding. Environ Toxicol Chem 19:2100–2106. doi:10.1002/etc.5620190820

    Article  CAS  Google Scholar 

  • Geffard O, Xuereb B, Chaumot A, Geffard A, Biagianti S, Noël C, Abbaci K, Garric J, Charmantier G, Charmantier-Daures M (2010) Ovarian cycle and embryonic development in Gammarus fossarum: application for reproductive toxicity assessment. Environ Toxicol Chem 29:2249–2259. doi:10.1002/etc.268

    Article  CAS  Google Scholar 

  • Khan AT, Weis JS, D’Andrea L (1988) Studies of cadmium tolerance in two populations of grass shrimp, Palaemonetes pugio. Bull Environ Contam Toxicol 40:30–34. doi:10.1007/BF01689382

    Article  CAS  Google Scholar 

  • Khan FR, Irving JR, Bury NR, Hogstrand C (2011) Differential tolerance of two Gammarus pulex populations transplanted from different metallogenic regions to a polymetal gradient. Aquat Toxicol 102:95–103. doi:10.1016/j.aquatox.2011.01.001

    Article  CAS  Google Scholar 

  • Klerks PL, Lentz SA (1998) Resistance to lead and zinc in the western mosquito fish Gambusia affinis inhabiting contaminated Bayou Trepagnier. Ecotoxicology 7:11–17. doi:10.1023/A:1008851516544

    Article  CAS  Google Scholar 

  • Klerks PL, Weis JS (1987) Genetic adaptation to heavy metals in aquatic organisms: a review. Environ Pollut 45:173–205. doi:10.1016/0269-7491(87)90057-1

    Article  CAS  Google Scholar 

  • Klerks PL, Xie L, Levinton JS (2011) Quantitative genetics approaches to study evolutionary processes in ecotoxicology; a perspective from research on the evolution of resistance. Ecotoxicology 20:513–523. doi:10.1007/s10646-011-0640-2

    Article  CAS  Google Scholar 

  • Maltby L (1999) Studying stress: the importance of organism-level responses. Ecol Appl 9:431–440. doi:10.1890/1051-0761(1999)009[0431:SSTIOO]2.0.CO;2

    Article  Google Scholar 

  • Maltby L, Crane M (1994) Responses of Gammarus pulex (amphipoda, crustacea) to metalliferous effluents: identification of toxic components and the importance of interpopulation variation. Environ Pollut 84:45–52. doi:10.1016/0269-7491(94)90069-8

    Article  CAS  Google Scholar 

  • Meyran JC (1997) Impact of water calcium on the phenotypic diversity of alpine populations of Gammarus fossarum. Ecology 78:1579–1587. doi:10.1890/0012-9658(1997)078[1579:IOWCOT]2.0.CO;2

    Article  Google Scholar 

  • Plautz SC, Salice CJ (2013) Plasticity in offspring contaminant tolerance traits: developmental cadmium exposure trumps parental effects. Ecotoxicology 22:847–853. doi:10.1007/s10646-013-1076-7

    Article  CAS  Google Scholar 

  • Posthuma L, Van Straalen NM (1993) Heavy-metal adaptation in terrestrial invertebrates: a review of occurrence, genetics, physiology and ecological consequences. Comp Biochem Phys C 106:11–38. doi:10.1016/0742-8413(93)90251-F

    Google Scholar 

  • Postma JF, van Kleunen A, Admiraal W (1995) Alterations in life-history traits of Chironomus riparius (diptera) obtained from metal contaminated rivers. Arch Environ Contam Toxicol 29:469–475. doi:10.1007/BF00208376

    Article  CAS  Google Scholar 

  • Salice CJ, Anderson TA, Roesijadi G (2010) Adaptive responses and latent costs of multigeneration cadmium exposure in parasite resistant and susceptible strains of a freshwater snail. Ecotoxicology 19:1466–1475. doi:10.1007/s10646-010-0532-x

    Article  CAS  Google Scholar 

  • Shirley MDF, Sibly RM (1999) Genetic basis of a between-environment trade-off involving resistance to Cadmium in Drosophila melanogaster. Evolution 53:826–836. doi:10.2307/2640722

    Article  Google Scholar 

  • Spicer JI, Morritt D, Maltby L (1998) Effect of water-borne zinc on osmoregulation in the freshwater amphipod Gammarus pulex (L.) from populations that differ in their sensitivity to metal stress. Funct Ecol 12:242–247. doi:10.1046/j.1365-2435.1998.00177.x

    Article  Google Scholar 

  • Stuhlbacher A, Maltby L (1992) Cadmium resistance in Gammarus pulex (L.). Arch Environ Contam Toxicol 22:319–324. doi:10.1007/BF00212093

    Article  CAS  Google Scholar 

  • R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/

  • van Straalen NM, Timmermans MJTN (2002) Genetic variation in toxicant-stressed populations: an evaluation of the “genetic erosion” hypothesis. Hum Ecol Risk Assess 8:983–1002. doi:10.1080/1080-700291905783

    Article  Google Scholar 

  • Weston DP, Poynton HC, Wellborn GA, Lydy MJ, Blalock BJ, Sepulveda MS, Colbourne JK (2013) Multiple origins of pyrethroid insecticide resistance across the species complex of a nontarget aquatic crustacean, Hyalella azteca. PNAS 110:16532–16537. doi:10.1073/pnas.1302023110

    Article  CAS  Google Scholar 

  • Xie L, Klerks PL (2004) Fitness cost of resistance to cadmium in the least killifish (Heterandria formosa). Environ Toxicol Chem 23:1499–1503. doi:10.1897/03-96

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank for financial Grants the ANR (Agence Nationale de la Recherche) CESA program GAMMA 021 02 “Variability-adaptation-diversity and Ecotoxicology in gammarids” (2012–2015), and ONEMA (the French National Agency for Water and Aquatic Ecosystems) for its financial support. The authors also thank technical staff of the “Ecotoxicology laboratory” and the “Aquatic chemistry laboratory” of Irstea in Lyon, especially R. Recoura-Massaquant, G. Jubeaux, A. Larrose, J Gahou and L Dherret, for their assistance in the field experiments and for analyses of trace elements.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Irstea, UR MALY Milieux aquatiques, écologie et pollutions, Centre de Lyon-Villeurbanne, 5 rue de la doua – CS70077, 69626, Villeurbanne, France

    A. Vigneron, O. Geffard, M. Coquery, A. François, H. Quéau & A. Chaumot

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  1. A. Vigneron
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  2. O. Geffard
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  3. M. Coquery
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  4. A. François
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  5. H. Quéau
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  6. A. Chaumot
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Correspondence to A. Chaumot.

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Vigneron, A., Geffard, O., Coquery, M. et al. Evolution of cadmium tolerance and associated costs in a Gammarus fossarum population inhabiting a low-level contaminated stream. Ecotoxicology 24, 1239–1249 (2015). https://doi.org/10.1007/s10646-015-1491-z

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