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Variation in tolerance to common marine pollutants among different populations in two species of the marine copepod Tigriopus

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Geographical variation in chemical tolerance within a species can significantly influence results of whole animal bioassays, yet a literature survey showed that the majority of articles using bioassays did not provide detail on the original field collection site of their test specimens confounding the ability for accurate replication and comparison of results. Biological variation as a result of population-specific tolerance, if not addressed, can be misinterpreted as experimental error. Our studies of two marine copepod species, Tigriopus japonicus and Tigriopus californicus, found significant intra- and inter-specific variation in tolerance to copper and tributyltin. Because both species tolerate copper concentrations orders of magnitude higher than those found in coastal waters, difference in copper tolerance may be a by-product of adaptation to other stressors such as high temperature. Controlling for inter-population tolerance variation will greatly strengthen the application of bioassays in chemical toxicity tests.

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  1. Abele D, Heise K, Pörtner HO, Puntarulo S (2002) Temperature-dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. J Exp Biol 205:1831–1841

  2. Agra AR, Guilhermino L, Soares AMVM, Barata C (2009) Genetic costs of tolerance to metals in Daphnia longispina populations historically exposed to a copper mine drainage. Environ Toxicol Chem 29:939–946

  3. Berthet B, Leung KMY, Amiard-Triquet C (2011) Inter- and intraspecific variability of tolerance: implications for bioassays and biomonitoring. In: Amiard-Triquet C, Rainbow PS, Romeo M (eds) Tolerance to environmental contaminants. CRC Press, Boca Raton, pp 189–216

  4. Boone AN, Vijayan MM (2002) Constitutive heat shock protein 70 (HSC70) expression in rainbow trout hepatocytes: effect of heat shock and heavy metal exposure. Comp Biochem Physiol C Toxicol Pharmacol 132:223–233

  5. Burton ED, Phillips IR, Hawker DW (2005) In-situ partitioning of butyltin compounds in estuarine sediments. Chemosphere 59:585–592

  6. Champ MA, Seligman PF (eds) (1996) Organotin: environmental fate and effects. Chapman & Hall, London, 629 p

  7. Díez S, Ábalos M, Bayona JM (2002) Organotin contamination in sediments from the Western Mediterranean enclosures following 10 years of TBT regulation. Water Res 36:905–918

  8. Edmands S (2001) Phylogeography of the intertidal copepod Tigriopus californicus reveals substantially reduced population differentiation at northern latitudes. Mol Ecol 10:1743–1750

  9. Edmands S, Harrison JS (2003) Molecular and quantitative trait variation within and among populations of the intertidal copepod Tigriopus californicus. Evolution 57:2277–2285

  10. Gould SJ, Vrba ES (1982) Exaptation; a missing term in the science of form. Paleobiology 8:4–15

  11. Heintz RA, Rice SD, Wertheimer AC, Bradshaw RF, Thrower FP, Joyce JE, Short JW (2000) Delayed effects on growth and marine survival of pink salmon Oncorhynchus gorbuscha after exposure to crude oil during embryonic development. Mar Ecol Prog Ser 208:205–216

  12. Helmuth B, Mieszkowska N, Moore P, Hawkins SJ (2006) Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change. Annu Rev Ecol Evol Syst 37:373–404. doi:10.1146/annurev.ecolsys.37.091305.110149

  13. Ishihara Y, Kawami T, Ishida A, Yamazaki T (2012) Tributyltin induces oxidative stress and neuronal injury by inhibiting glutathione S-transferase in rat organotypic hippocampal slice cultures. Neurochem Int 60:782–790

  14. Katika MR, Hendriksen PJM, van Loveren H, Peijnenburg A (2011) Exposure of Jurkat cells to bis (tri-n-butyltin) oxide (TBTO) induces transcriptomics changes indicative for ER- and oxidative stress, T cell activation and apoptosis. Toxicol Appl Pharmacol 254:311–322

  15. Kelly MW, Sanford E, Grosberg RK (2012) Limited potential for adaptation to climate change in a broadly distributed marine crustacean. Proc R Soc B 279(1727):349–356. doi:10.1098/rspb.2011.0542

  16. Ki J-S, Lee K-W, Park HG, Chullasorn S, Dahms H-U, Lee J-S (2009) Phylogeography of the copepod Tigriopus japonicus along the Northwest Pacific rim. J Plankton Res 31:209–221

  17. Kwok KWH, Leung KMY (2005) Toxicity of antifouling biocides to the intertidal harpacticoid copepod Tigriopus japonicus (Crustacea, Copepoda): effects of temperature and salinity. Mar Pollut Bull 51:830–837

  18. Kwok KWH, Leung KMY, Bao VWW, Lee J-S (2008) Copper toxicity in the marine copepod Tigriopus japonicus: low variability and high reproducibility of repeated acute and life-cycle tests. Mar Pollut Bull 57:632–636

  19. Kwok KWH, Grist EPM, Leung KMY (2009) Acclimation effect and fitness cost of copper resistance in the marine copepod Tigriopus japonicus. Ecotoxicol Environ Saf 72:358–364

  20. Lukkari T, Taavitsainen M, Soimasuo M, Oikari A, Haimi J (2004) Biomarker responses of the earthworm Aporrectodea tuberculata to copper and zinc exposure: differences between populations with and without earlier metal exposure. Environ Pollut 129:377–386. doi:10.1016/j.envpol.2003.12.008

  21. Martins N, Lopes I, Harper RM, Ross P, Ribeiro R (2007) Differential resistance to copper and mine drainage in Daphnia longispina: relationship with allozyme genotypes. Environ Toxicol Chem 26:1904–1909. doi:10.1897/06-111R.1

  22. Mouneyrac C, Leung PTY, Leung KMY (2011) Cost of tolerance. In: Amiard-Triquet C, Rainbow PS, Romeo M (eds) Tolerance to environmental contaminants. CRC Press, Boca Raton, pp 265–297

  23. Peterson DL, Kubow KB, Connolly MJ, Kaplan LR, Wetkowski MM, Leong W, Phillips BC, Edmands S (2013) Reproductive and phylogenetic divergence of tidepool copepod populations across a narrow geographical boundary in Baja California. J Biogeogr 40:1664–1675. doi:10.1111/jbi.12107

  24. Philips DJH, Rainbow PS (1993) Biomonitoring of trace aquatic contaminants. Springer, London, 371 p

  25. Qiu J-W, Qian PY (1999) Tolerance of the barnacle Balanus amphitrite amphitrite to salinity and temperature stress: effects of previous experience. Mar Ecol Prog Ser 188:123–132

  26. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL

  27. Raisuddin S, Kwok KWH, Leung KMY, Schlenk D, Lee J-S (2007) The copepod Tigriopus: a promising marine model organism for ecotoxicology and environmental genomics. Aquat Toxicol 83:161–173

  28. Rhee J-S, Raisuddin S, Lee K-W, Seo JS, Ki J-S, Kim I-C, Park HG, Lee J-S (2009) Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants. Comp Biochem Physiol C Toxicol Pharmacol 149:104–112

  29. Rhee J-S, Yu IT, Kim B-M, Jeong C-B, Lee K-W, Kim M-J, Lee S-J, Park GS, Lee J-S (2013) Copper induces apoptotic cell death through reactive oxygen species-triggered oxidative stress in the intertidal copepod Tigriopus japonicus. Aquat Toxicol 132–133:182–189

  30. Santos DM, dos Sant’Anna BS, Sandron DC, Cardoso de Souza S, Cristale J, de Marchi MRR, Turra A (2010) Occurrence and behavior of butyltins in intertidal and shallow subtidal surface sediments of an estuarine beach under different sampling conditions. Estuar Coast Shelf Sci 88:322–328

  31. Sarabia R, Del RJ, Varo I, Díaz-Mayans J, Torreblanca A (2002) Comparing the acute response to cadmium toxicity of nauplii from different populations of Artemia. Environ Toxicol Chem 21:437–444

  32. Schoville SD, Barreto FS, Moy GW, Wolff A, Burton RS (2012) Investigating the molecular basis of local adaptation to thermal stress: population differences in gene expression across the transcriptome of the copepod Tigriopus californicus. BMC Evol Biol 12:170

  33. Smail EA, Webb EA, Franks RP, Bruland KW, Sanudo-Wilhelmy SA (2012) Status of metal contamination in surface waters of the coastal ocean off Los Angeles, California since the implementation of the Clean Water Act. Environ Sci Technol 46:4304–4311

  34. Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine “winners” and “losers”. J Exp Biol 213:912–920. doi:10.1242/jeb.037473

  35. Sun PY, Foley HB, Handschumacher L, Suzuki A, Karamanukyan T, Edmands S (2014) Acclimation and adaptation to common marine pollutants in the copepod Tigriopus californicus. Chemosphere 112:465–471

  36. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York. ISBN 0-387-95457-0

  37. Wang D, Lin W, Yang X, Zhai W, Dai M, Chen AC-T (2012) Occurrences of dissolved trace metals (Cu, Cd, and Mn) in the Pearl River Estuary (China), a large river-groundwater-estuary system. Cont Shelf Res 50–51:54–63

  38. Weis JS (2014) Delayed behavioral effects of early life toxicant exposures in aquatic biota. Toxics 2(2):165–187

  39. Wen L-S, Jiann K-T, Santschi PH (2006) Physicochemical speciation of bioactive trace metals (Cd, Cu, Fe, Ni) in the oligotrophic South China Sea. Mar Chem 101:104–129

  40. Wheeler MW, Park RM, Bailer AJ (2006) Comparing median lethal concentration values using confidence interval overlap or ratio tests. Environ Toxicol Chem 25:1441–1444

  41. Willett CS (2010) Potential fitness trade-offs for thermal tolerance in the intertidal copepod Tigriopus californicus. Evolution 64:2521–2534

  42. Winner RW, Farrell MP (1976) Acute and Chronic Toxicity of Copper to Four Species of Daphnia. J Fish Res Bd Can 33:1685–1691. doi:10.1139/f76-215

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The authors thank the editor and three anonymous reviewers for their assistance in strengthening the manuscript. This study was primarily supported by Sea Grant (NA10OAR417005) to SE and partially supported by the Research Grants Council of the Hong Kong SAR Government via a General Research Fund (HKU703511P) to KMYL. The authors wish to acknowledge use of the Maptool program for generating the maps in this paper. Maptool is a product of SEATURTLE.ORG (information is available at The authors would also like to thank Shiven Chaudhry and Jennifer Ko for their assistance with acute toxicity tests.

Compliance with ethical standards

The authors assure that all procedures were performed in compliance with national and institutional guidelines for the protection of animal welfare.

Conflict of interest

The authors declare that there is no conflict of interest.

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Correspondence to Patrick Y. Sun.

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Responsible editor: Cinta Porte

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Sun, P.Y., Foley, H.B., Bao, V.W.W. et al. Variation in tolerance to common marine pollutants among different populations in two species of the marine copepod Tigriopus . Environ Sci Pollut Res 22, 16143–16152 (2015).

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  • Copper
  • Tributyltin
  • Tigriopus japonicus
  • Tigriopus californicus
  • Bioassay