, Volume 23, Issue 8, pp 1564–1573 | Cite as

Temperature-dependent toxicities of four common chemical pollutants to the marine medaka fish, copepod and rotifer

  • Adela J. Li
  • Priscilla T. Y. Leung
  • Vivien W. W. Bao
  • Andy X. L. Yi
  • Kenneth M. Y. Leung


We hypothesize that chemical toxicity to marine ectotherms is the lowest at an optimum temperature (OT) and it exacerbates with increasing or decreasing temperature from the OT. This study aimed to verify this hypothetical temperature-dependent chemical toxicity (TDCT) model through laboratory experiments. Acute toxicity over a range of temperatures was tested on four commonly used chemicals to three marine ectotherms. Our results confirmed that toxicities, in terms of 96-h LC50 (median lethal concentration; for the marine medaka fish Oryzias melastigma and the copepod Tigriopus japonicus) and 24-h LC50 (for the rotifer Brachionus koreanus), were highly temperature-dependent, and varied between test species and between study chemicals. The LC50 value of the fish peaked at 20 °C for copper (II) sulphate pentahydrate and triphenyltin chloride, and at 25 °C for dichlorophenyltrichloroethane and copper pyrithione, and decreased with temperature increase or decrease from the peak (i.e., OT). However, LC50 values of the copepod and the rotifer generally showed a negative relationship with temperature across all test chemicals. Both copepod and rotifer entered dormancy at the lowest temperature of 4 °C. Such metabolic depression responses in these zooplanktons could reduce their uptake of the chemical and hence minimize the chemical toxicity at low temperatures. Our TDCT model is supported by the fish data only, whereas a simple linear model fits better to the zooplankton data. Such species-specific TDCT patterns may be jointly ascribed to temperature-mediated changes in (1) the physiological response and susceptibility of the marine ectotherms to the chemical, (2) speciation and bioavailability of the chemical, and (3) toxicokinetics of the chemical in the organisms.


Temperature Copper DDT Triphenyltin Pyrithione Marine organisms 



This work is substantially funded by the Research Grants Council through a General Research Fund (Project No. HKU 703511P). Adela J. Li is partially supported by the HKU via a postgraduate studentship. The authors thank Helen Leung and Cecily Law for their technical support, and Dr. Stephen Cartwright of the Hong Kong Baptist University for proofreading a draft of this manuscript. The authors are very grateful to Professor Allen Burton, University of Michigan for introducing us about the early work of Professor John Cairns Jr. on studying the effect of temperature on chemical toxicity to freshwater organisms. The authors also thank the two anonymous reviewers for offering their valuable comments.

Conflict of interest

The authors declare that there is no conflict of interest.


The experiments comply with the current laws of Hong Kong in which they were performed. The manuscript contains experiments using fish, for which permission of Department of Health the Government of the Hong Kong Special Administration Region have been obtained (Ref No. (10-147) in DH/HA&P/8/2/3 Pt. 19).

Supplementary material

10646_2014_1297_MOESM1_ESM.docx (17 kb)
Supplementary material 1 (DOCX 18 kb)


  1. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267Google Scholar
  2. ASTM (2012) Standard guide for acute toxicity test with the Rotifer Branchionus. doi: 10.1520/E1440-91R12
  3. Bao VWW, Koutsaftis A, Leung KMY (2008a) Temperature-dependent toxicities of chlorothalonil and copper pyrithione to the marine copepod Tigriopus japonicus and dinoflagellate Pyrocystis lunula. Australas J Ecotoxicol 14:45–54Google Scholar
  4. Bao VWW, Leung KMY, Kwok KWH, Zhang AQ, Lui GCS (2008b) Synergistic toxic effects of zinc pyrithione and copper to three marine species: implications on setting appropriate water quality criteria. Mar Pollut Bull 57:616–623CrossRefGoogle Scholar
  5. Barnett TP, Pierce DW, AchutaRao KM, Gleckler PJ, Santer BD, Gregory JM, Washington WM (2005) Penetration of human-induced warming into the world’s oceans. Science 309:284–287CrossRefGoogle Scholar
  6. Boeckman CJ, Bidwell JR (2006) The effects of temperature, suspended solids, and organic carbon on copper toxicity to two aquatic invertebrates. Water Air Soil Pollut 171:185–202CrossRefGoogle Scholar
  7. Cairns J Jr, Heath AG, Parker BC (1975) The effects of temperature upon the toxicity of chemicals to aquatic organisms. Hydrobiologia 47:135–171CrossRefGoogle Scholar
  8. Cairns J Jr, Buikema A Jr, Heath AG, Parker BC (1978) Effects of temperature on aquatic organism sensitivity to selected chemicals. Virginia Water Resour Res Center Bull 106:1–90Google Scholar
  9. Chan BKK (2000) Diurnal physico-chemical variations in Hong Kong rock pools. Asian Mar Biol 17:43–54Google Scholar
  10. Chan BKK, Morritt D, De Pirro M, Leung KMY, Williams GA (2006) Summer mortality: effects on the distribution and abundance of the acorn barnacle Tetraclita japonica on tropical shores. Mar Ecol Prog Ser 328:195–204CrossRefGoogle Scholar
  11. Cornish AS, Ng WC, Ho VCM, Wong HL, Lam JCW, Lam PKS, Leung KMY (2007) Trace metals and organochlorines in the bamboo shark Chiloscyllium plagiosum from the southern waters of Hong Kong, China. Sci Total Environ 376:335–345CrossRefGoogle Scholar
  12. Deane EE, Woo NYS (2005) Cloning and characterization of the hsp70 multigene family from silver sea bream: modulated gene expression between warm and cold temperature acclimation. Biochem Biophys Res Commun 330:776–783CrossRefGoogle Scholar
  13. Demas GE, Adamo SA, French SS (2011) Neuroendocrine-immune crosstalk in vertebrates and invertebrates: implications for host defence. Funct Ecol 25:29–39CrossRefGoogle Scholar
  14. Donelson JM, Munday PL, McCormick MI, Nilsson GE (2011) Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish. Global Change Biol 17:1712–1719CrossRefGoogle Scholar
  15. Furuta T, Iwata N, Kikuchhi K (2007) Effects of fish size and water temperature on the acute toxicity of boron to Japanese flounder Paralichthys olivaceus and red sea bream Pagrus major. Fish Sci 73:356–363CrossRefGoogle Scholar
  16. Gama-Flores JL, Sarma SSS, Nandini S (2005) Interaction among copper toxicity, temperature and salinity on the population dynamics of Brachionus rotundiformis (Rotifera). Hydrobiologia 546:559–568CrossRefGoogle Scholar
  17. Greco WR, Bravo G, Parsons JC (1995) The research for synergy: a critical review from a response surface perspective. Pharmacol Rev 47:331–385Google Scholar
  18. Hernandez PP, Undurraga C, Gallardo VE, Mackenzie N, Allende ML, Reyes AE (2011) Sublethal concentrations of waterborne copper induce cellular stress and cell death in zebrafish embryos and larvae. Biol Res 44:7–15CrossRefGoogle Scholar
  19. Heugens EHW, Hendriks AJ, Dekker T, van Straalen NM, Admiraal W (2001) A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Crit Rev Toxicol 31:247–284CrossRefGoogle Scholar
  20. Heugens EHW, Jager T, Creyghton R, Kraak MHS, Hendriks AJ, van Straalen NM, Admiraal W (2003) Temperature-dependent effects of cadmium on Daphnia magna: accumulation versus sensitivity. Environ Sci Technol 37:2145–2151CrossRefGoogle Scholar
  21. IPCC (2013) Climate change 2013—the Physical Science Basis: the fifth assessment report of the intergovernmental panel on climate change (IPCC). Accessed 15 Nov 2013
  22. Jiang ZB, Huang YJ, Chen QZ, Zeng JN, Xu XQ (2012) Acute toxicity of crude oil water accommodated fraction on marine copepods: the relative importance of acclimatization temperature and body size. Mar Environ Res 81:12–17CrossRefGoogle Scholar
  23. 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 51:830–837CrossRefGoogle Scholar
  24. Kyprianou TD, Pörtner HO, Anestis A, Kostoglou B, Feidantsis K, Michaelidis B (2010) Metabolic and molecular stress responses of gilthead seam bream Sparus aurata during exposure to low ambient temperature: an analysis of mechanisms underlying the winter syndrome. J Comp Physiol B 180:1005–1018CrossRefGoogle Scholar
  25. Lagadic L, Caquet T (1998) Invertebrates in testing of environmental chemicals: are they alternatives? Environ Health Perspect 106:593–611CrossRefGoogle Scholar
  26. Larrain A, Soto E, Silva J, Bay-Schmith E (1998) Sensitivity of the meiofaunal copepod Tisbe longicornis to K2Cr2O7 under varying temperature regimes. Bull Environ Contam Toxicol 61:391–396CrossRefGoogle Scholar
  27. Lau ETC, Yung MMN, Karraker NE, Leung KMY (2014) Is an assessment factor of 10 appropriate to account for the variation in chemical toxicity to freshwater ectotherms under different thermal conditions? Environ Sci Pollut Res 21:95–104CrossRefGoogle Scholar
  28. Leung KMY, Taylor AC, Furness RW (2000) Temperature-dependent physiological responses of the dogwhelk Nucella lapillus to cadmium exposure. J Mar Biol Assoc UK 80:647–660CrossRefGoogle Scholar
  29. Li C, Sun S, Wang R, Wang X (2004) Feeding and respiration rates of a planktonic copepod (Calanus sinicus) oversummering in Yellow Sea cold bottom waters. Mar Biol 145:149–157CrossRefGoogle Scholar
  30. Marcial HS, Hagiwara A, Snell TW (2005) Effect of some pesticides on reproduction of rotifer Brachionus plicatilis Müller. Hydrobiologia 546:569–575CrossRefGoogle Scholar
  31. McAllen R, Taylor AC, Davenport J (1999) The effects of temperature and oxygen partial pressure on the rate of oxygen consumption of the high-shore rock pool copepod Tigriopus brevicornis. Comp Biochem Physiol A 123:195–202CrossRefGoogle Scholar
  32. OECD (1992) Fish, acute toxicity test (test no. 203). OECD Guidelines for the Testing of Chemicals, Section 2 Effects on Biotic Systems. The Organization for Economic Cooperation and Development. doi: 10.1787/20745761
  33. OECD (2007) Validation report of the full life-cycle test with the harpacticoid copepods Nitocra spinipes and Amphiascus tenuiremis and the calanoid copepod Acartia tonsa. Phase 1. Environmental Health and Safety Publications. Series on Testing and Assessment No. 79. ENV/JM/MONO (2007) 26Google Scholar
  34. OECD (2011) Report of progress on the interlaboratory validation of the OECD harpacticoid copepod development and reproduction test. Environmental Health and Safety Publications. Series on Testing and Assessment No. 158. ENV/JM/MONO (2011) 38Google Scholar
  35. Osterauer R, Köhler HR (2008) Temperature-dependent effects of the pesticides thiacloprid and diazinon on the embryonic development of zebrafish (Danio rerio). Aquat Toxicol 86:485–494CrossRefGoogle Scholar
  36. Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A 132:739–761CrossRefGoogle Scholar
  37. Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97CrossRefGoogle Scholar
  38. Powell JH, Fielder DR (1982) Temperature and toxicity of DDT to sea mullet (Mugil cephalus L.). Mar Pollut Bull 13:228–230CrossRefGoogle Scholar
  39. Raisuddin S, Kwok KWH, Leung KMY, Schlenk D, Lee JS (2007) The copepod Tigriopus: a promising marine model organism for ecotoxicology and environmental genomics. Aquat Toxicol 83:161–173CrossRefGoogle Scholar
  40. Rhee JS, Raisuddin S, Lee KW, Seo JS, Ki JS, Kim IC, Park HG, Lee JS (2009) Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants. Comp Biochem Physiol C 149:104–112Google Scholar
  41. Rhee JS, Kim RO, Choi HG, Lee J, Lee YM, Lee JS (2011) Molecular and biochemical modulation of heat shock protein 20 (Hsp20) gene by temperature stress and hydrogen peroxide (H2O2) in the monogonont rotifer, Brachionus sp. Comp Biochem Physiol C 154:19–27Google Scholar
  42. Simonich SL, Hites RA (1995) Global distribution of persistent organochlorine compounds. Science 269:1851–1854CrossRefGoogle Scholar
  43. Smith HA, Burns AR, Shearer TL, Snell TW (2012) Three heat shock proteins are essential for rotifer thermotolerance. J Exp Mar Biol Ecol 413:1–6CrossRefGoogle Scholar
  44. Snell TW, Persoone G (1989) Acute toxicity bioassays using rotifers. I. A test for brackish and marine environments with Brachionus plicatilis. Aquat Toxicol 14:65–80CrossRefGoogle Scholar
  45. Srinivasan M, Swain GW (2007) Managing the use of copper-based antifouling paints. Environ Manage 39:423–441CrossRefGoogle Scholar
  46. Terblanche JS, Hoffmann AA, Mitchell KA, Rako L, le Roux PC, Chown SL (2011) Review: ecologically relevant measures of tolerance to potentially lethal temperatures. J Exp Biol 214:3713–3725CrossRefGoogle Scholar
  47. Wang Z, Kwok KWH, Lui GCS, Zhou GJ, Lee JS, Lam MHW, Leung KMY (2014) The difference between temperate and tropical saltwater species’ acute sensitivity to chemicals is relatively small. Chemosphere 105:31–43CrossRefGoogle Scholar
  48. Williams GA (1994) The relationship between shade and molluscan grazing in structuring communities on a moderately-exposed tropical rocky shore. J Exp Mar Biol Ecol 178:79–95CrossRefGoogle Scholar
  49. Wong SWY, Leung KMY (2014) Temperature-dependent toxicities of nano zinc oxide to marine diatom, amphipod and fish in relation to its aggregation size and ion dissolution. Nanotoxicology. doi: 10.3109/17435390.2013.848949
  50. Yebra DM, Kiil S, Dam-Johansen KD (2004) Antifouling technology-past, present and future steps towards efficient and environmental friendly antifouling coatings. Prog Org Coat 50:75–104CrossRefGoogle Scholar
  51. Yi AXL, Leung KMY, Lam MHW, Lee JS, Geisy JP (2012) Review of measured concentrations of triphenyltin compounds in marine ecosystems and meta-analysis of their risks to humans and the environment. Chemosphere 89:1015–1025CrossRefGoogle Scholar
  52. Yu HY, Shen RL, Liang Y, Cheng HF, Zeng EY (2011) Inputs of antifouling paint-derived dichlorodiphenyltrichloroethanes (DDTs) to a typical mariculture zone (South China): potential impact on aquafarming environment. Environ Pollut 159:3700–3705CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Adela J. Li
    • 1
  • Priscilla T. Y. Leung
    • 1
  • Vivien W. W. Bao
    • 1
  • Andy X. L. Yi
    • 1
  • Kenneth M. Y. Leung
    • 1
  1. 1.The Swire Institute of Marine Science and School of Biological SciencesThe University of Hong KongPokfulamPeople’s Republic of China

Personalised recommendations