Skip to main content

Immunotoxic effects of environmental toxicants in fish — how to assess them?

Environmental Science and Pollution Research volume 19, pages 2465–2476 (2012)Cite this article

Abstract

Numerous environmental chemicals, both long-known toxicants such as persistent organic pollutants as well as emerging contaminants such as pharmaceuticals, are known to modulate immune parameters of wildlife species, what can have adverse consequences for the fitness of individuals including their capability to resist pathogen infections. Despite frequent field observations of impaired immunocompetence and increased disease incidence in contaminant-exposed wildlife populations, the potential relevance of immunotoxic effects for the ecological impact of chemicals is rarely considered in ecotoxicological risk assessment. A limiting factor in the assessment of immunotoxic effects might be the complexity of the immune system what makes it difficult (1) to select appropriate exposure and effect parameters out of the many immune parameters which could be measured, and (2) to evaluate the significance of the selected parameters for the overall fitness and immunocompetence of the organism. Here, we present — on the example of teleost fishes — a brief discussion of how to assess chemical impact on the immune system using parameters at different levels of complexity and integration: immune mediators, humoral immune effectors, cellular immune defenses, macroscopical and microscopical responses of lymphoid tissues and organs, and host resistance to pathogens. Importantly, adverse effects of chemicals on immunocompetence may be detectable only after immune system activation, e.g., after pathogen challenge, but not in the resting immune system of non-infected fish. Current limitations to further development and implementation of immunotoxicity assays and parameters in ecotoxicological risk assessment are not primarily due to technological constraints, but are related from insufficient knowledge of (1) possible modes of action in the immune system, (2) the importance of intra- and inter-species immune system variability for the response against chemical stressors, and (3) deficits in conceptual and mechanistic assessment of combination effects of chemicals and pathogens.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1

References

  • Albergoni V, Viola A (1995) Effects of cadmium on catfish, Ictalurus melas, humoral immune reponse. Fish Shellfish Immunol 5:89–95

    Article  Google Scholar 

  • Alexander JB, Ingram CA (1992) Non-cellular non-specific defense mechanisms of fish. Ann Rev Fish Dis 2:249–277

    Article  Google Scholar 

  • Arkoosh MR, Casillas E, McCain B, Varanasi U (1991) Suppression of immunological memory in juvenile Chinook salmon (Oncorhynchus tshawytscha) from an urban estuary. Fish Shellfish Immunol 1:261–277

    Article  Google Scholar 

  • Arkoosh MR, Casillas E, Huffman P, Clemons E, Evered J, Stein JE, Varanasi U (1998) Increased susceptibility of juvenile Chinook salmon from a contaminated estuary to Vibrio anguillarum. Trans Am Fish Soc 127:360–374

    Article  Google Scholar 

  • Arkoosh MR, Clemons E, Hufman P, Kagley AN (2001) Increased susceptibility of juvenile Chinook salmon to vibriosis after exposure to chlorinated and aromatic compounds found in contaminated urban estuaries. J Aquat Anim Health 13:257–268

    Article  Google Scholar 

  • Arkoosh MR, Boylen D, Stafford CC, Johnson LL, Colliert TK (2005) Use of disease challenge assays to assesss immunotoxicity of xenobiotics to fish. In: Ostrander GK (ed) Techniques in aquatic toxicology, vol 2. Taylor & Francis, New York, pp 19–35

  • Bayne CJ, Gerwick L (2001) The acute phase response and innate immunity of fish. Dev Comp Immunol 25:725–743

    Article  CAS  Google Scholar 

  • Beinecke A, Siebert U, McLachlan M, Bruhn R, Thron K, Failing K, Müller G, Baumgärtner W (2005) Investigations of the potential influence of environmental contaminants on the thymus and spleen of harbour porpoises (Phocoena phocoena). Environ Sci Technol 39:3933–3938

    Article  Google Scholar 

  • Bols NC, Brubacher JL, Ganassin RC, Lee LEJ (2001) Ecotoxicology and innate immunity in fish. Dev Comp Immunol 25:853–873

    Article  CAS  Google Scholar 

  • Burnett KG (2005) Impact of environmental toxicants and natural variables on the immune system of fishes. In: Mommsen TP, Moon TW (eds) Biochemistry and molecular biology of fishes, vol VI, Environmental toxicology. Elsevier, Amsterdam, pp 231–253

    Google Scholar 

  • Burns LA, Meade BJ, Munson AE (1996) Toxic responses of the immune system. In: Klaasen CD (ed) Casarett & Doull’s Toxicology. McGraw-Hill, New York, pp 355–402

    Google Scholar 

  • Calow P, Forbes VE (2003) Does ecotoxicology inform ecological risk assessment? Environ Sci Technol 37:146A–151A

    Article  Google Scholar 

  • Carlson E, Zelikoff JT (2008) The immune system of fish: a target organ of toxicity. In: Di Giulio RT, Hinton DE (eds) The toxicology of fishes. CRC Press, Boca Raton, FL, pp 489–529

    Chapter  Google Scholar 

  • Carlson EA, Li Y, Zelikoff JT (2002) Exposure of Japanese medaka (Oryzias latipes) to benzo(a)pyrene suppresses immune function and host resistance against bacterial challenge. Aquat Toxicol 56:289–301

    Article  CAS  Google Scholar 

  • Carlson EA, Li Y, Zelikoff JT (2004) Benzo(a)pyrene-induced immunotoxicity in Japanese medaka (Oryzias latipes): relationship between lymphoid CYP1A activity and humoral immune suppression. Toxicol Appl Pharmacol 201:40–52

    Article  CAS  Google Scholar 

  • Casanova-Nakayama A, Wenger M, Burki R, Eppler E, Krasnov A, Segner H (2011) Endocrine disrupting compounds: can they target the immune system of fish? Mar Pollut Bull 63:412–416

    Article  CAS  Google Scholar 

  • Castro R, Bernard D, Lefranc MP, Six A, Benmansour A, Boudinot P (2011) T cell diversity and TcR repertoire in teleost fish. Fish Shellfish Manag 31:644–654

    Article  CAS  Google Scholar 

  • Chang YT, Kai YH, Chi SC, Song YL (2011) Cytotoxic CD8α+ leucocytes have heterogenous features in antigen recognition abd class I MHC restriction in grouper. Fish Shellfish Immunol 30:1283–1293

    Article  CAS  Google Scholar 

  • Dautremepuits C, Betoulle S, Paris-Palacios S, Vernet G (2004) Humoral immune factors modulated by copper and chitosan in healthy or parasitised carp (Cyprinus carpio L.) by Ptychobothrium sp. (Cestoda). Aquat Toxicol 68:325–338

    Article  CAS  Google Scholar 

  • Demas GE, Zysling DA, Beechler BR, Muehlenbein MP, French SS (2011) Beyond phytohaemaglutinin: assessing vertebrate immune function across ecologcial contexts. J Anim Ecol 80:710–730

    Article  Google Scholar 

  • Dietert RR (2009) Developmental immunotoxicology: focus on health risks. Chem Res Toxicol 22:17–23

    Article  CAS  Google Scholar 

  • Eder KJ, Clifford MA, Hedrick RP, Köhler HR, Werner I (2008) Expression of immune regulatory genes in juvenile Chinook salmon following exposure to pesticides and infectious hematopoietic necrosis virus (IHNV). Fish Shellfish Immunol 25:508–516

    Article  CAS  Google Scholar 

  • Evans DL, Smith EE, Brown FE (1987) Nonspecific cytotoxic cells in fish (lctalurus punctatus): VI. Flow cytometric analysis. Dev Comp Immunol 11:95–104

    Article  CAS  Google Scholar 

  • Faller P, Koble B, Peter A, Sumpter JP, Burkhardt-Holm P (2003) Stress status of gudgeon (Gobio gobio) from rivers in Switzerland with and without input of sewage treatment plant effluent. Environ Toxicol Chem 22:2063–2072

    Article  CAS  Google Scholar 

  • Fatima M, Mandiki SN, Douxfils J, Silvestre F, Coppe P, Kestemont P (2007) Combined effects of herbicides on biomarkers reflecting immune-endocrine interactions in goldfish. Immune and antioxidant effects. Aquat Toxicol 81:159–167

    Article  CAS  Google Scholar 

  • Fischer U, Utke K, Somamoto T, Köllner B, Ototake M, Nakanishi T (2006) Cytotoxic activities of fish leukocytes. Fish Shellfish Immunol 20:209–226

    Article  CAS  Google Scholar 

  • Fleeger JW, Carman KR, Nisbet RM (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317:207–233

    Article  CAS  Google Scholar 

  • Galloway TS, Depledge MH (2001) Immunotoxicity in invertebrates: measurement and ecotoxicological relevance. Ecotoxicology 10:5–23

    Article  CAS  Google Scholar 

  • Garduno RA, Kay WW (1994) Isolation and culture of head kidney macrophages. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 3, Analytical techniques. Elsevier, Amsterdam, pp 327–353

    Google Scholar 

  • Garrigues Ph, Barth H, Walker CH, Narbonne JF (eds) (2001) Biomarkers in marine organisms. A practical approach. Elsevier, Amsterdam

    Google Scholar 

  • Germolec DR, Kashon M, Nyska A, Kuper CF, Portier C, Kommimemi C, Johnson KA, Luster MI (2004) The accuracy of extended histopathology to detect immunotoxic chemicals. Toxicol Sci 82:504–514

    Article  CAS  Google Scholar 

  • Goetz FW, Planas JV, Mackenzie S (2004) Tumor necrosis factors. Dev Comp Immunol 28:487–497

    Article  CAS  Google Scholar 

  • Graham AL, Hayward AD, Watt KA, Pilkington JG, Pemberton JM, Nussey DH (2010) Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330:662–665

    Article  CAS  Google Scholar 

  • Grinwis GCM, Besselink HT, van den Brandhof EJ, Bulder AS, Engelsma MY, Kuiper RV, Wester PW, Vaal MA, Vethaak AD, Vos JG (2000) Toxicity of TCDD in European flounder (Platichthys flesus) with emphasis on histopathology and cytochrome P4501A induction in several organ systems. Aquat Toxicol 50:387–401

    Article  CAS  Google Scholar 

  • Harford AJ, O’Halloran K, Wright PF (2006) Flow cytometric analysis and optinisation for measuring phagocytosis in three Australian freshwater fish. Fish Shellfish Immunol 20:562–573

    Article  Google Scholar 

  • Harms CA, Ottinger CA, Blazer VS, Densmore CL, Pieper LH, Kennedy-Stoskopf S (2000) Quantitative polymerase chain reaction for transforming growth factor-β applied to field study of fish health in Chesapeake Bay tributaries. Environ Health Perspect 108:447–452

    CAS  Google Scholar 

  • Hinton DM (2000) US FDA “Redbook II” immunotoxicity testing guidelines and research in immunotoxicity evaluation of food chemicals and new food proteins. Toxicol Pathol 28:467–478

    Article  CAS  Google Scholar 

  • Hoeger B, Köllner B, Dietrich DR, Hitzfeld B (2005) Water-borne diclofenac affects kidney and gill integrity and selected immune parameters in brown trout (Salmo trutta f. fario). Aquat Toxicol 75:53–64

    Article  CAS  Google Scholar 

  • Hutchinson TH, Field MDR, Manning MJ (2003) Evaluation of non-specific immune functions in dab, Limanda limanda, following short-term exposure to sediments contaminated with polyaromatic hydrocarbons and/or polychlorinated biphenyls. Mar Environ Res 55:193–202

    Article  CAS  Google Scholar 

  • Iwanowicz LR, Blazer VS, McCormick SD, VanVeld PA, Ottinger CA (2009) Aroclor 1248 exposure leads to immunomodulation, decreased disease resistance and endocrine disruption in the brown bullhead, Ameiurus nebulosus. Aquat Toxicol 93:70–82

    Article  CAS  Google Scholar 

  • Jin X, Chen R, Liu W, Fu Z (2010) Effect of endocrine disrupting chemicals on the transcription of genes related to the innate immune system in the early developmental stage of zebrafish (Danio rerio). Fish Shellfish Immunol 28:854–861

    Article  CAS  Google Scholar 

  • Jovanovic B, Anastasova L, Rowe EW, Zhang Y, Clapp AR, Palic D (2011) Effects of nanosized titanium dioxide on innate immune system of fathead minnow (Pimephales promelas). Ecotoxicol Environ Saf 74:675–683

    Article  CAS  Google Scholar 

  • Kiesecker JM (2002) Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proc Natl Acad Sci U S A 99:9900–9904

    Article  CAS  Google Scholar 

  • Köllner B, Kotterba G, Fischer U (2002) Evaluation of immune functions of rainbow trout—how can environmental influences be detected? Toxicol Lett 131:83–95

    Article  Google Scholar 

  • Koskinen H, Pehkonen P, Vehniäinen E, Krasnov A, Rexroad C, Afanasyev S, Mölsa H, Oikari A (2004) Response of rainbow trout transcriptome to model chemical contaminants. Biochem Biophys Res Commun 320:745–753

    Article  CAS  Google Scholar 

  • Kreutz LC, Gil Barcellos LJ, de Faria VS, de Oliveira ST, Anziliero D, Davi dos Santos E, Pivato M, Zanatta R (2011) Altered hematological and immunological parameters in silver catfish (Rhamdia quelen) following short term exposure to sublethal concentration of glyphosate. Fish Shellfish Immunol 30:51–57

    Article  CAS  Google Scholar 

  • Lazarro BP, Little TJ (2009) Immunity in a variable world. Phil Trans R Soc B 364:15–26

    Article  Google Scholar 

  • Litman GW, Rast JP, Fugman SD (2010) The origins of vertebrate adaptive immunity. Nat Rev Immunol 10:543–552

    Article  CAS  Google Scholar 

  • Luebke RW, Hodson PV, Faisal M, Ross PJ, Grasman KA, Zelikoff J (1997) Aquatic pollution-induced immunotoxicity in wildlife species. Fundam Appl Toxicol 37:1–5

    Article  CAS  Google Scholar 

  • Luebke RW, Copeland CB, Bishop RL, Daniels MJ, Gilmour MI (2002) Mortality in dioxin-exposed mice infected with influenza-mitochondrial toxicity (Reye’s like syndrome) versus enhanced inflammation as the mode of toxic action. Toxicol Sci 69:109–116

    Article  CAS  Google Scholar 

  • MacKenzie S, Iliev D, Liarte C, Koskinen H, Planas JV, Goetz FW, Mölsä H, Krasnov A, Tort L (2006) Transcriptional analysis of LPS-stimulated activation of trout (Oncorhynchus mykiss) monocyte/macrophage cells in primary culture treated with cortisol. Mol Immunol 43:1340–1348

    Article  CAS  Google Scholar 

  • Magnadóttir I (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137–151

    Article  Google Scholar 

  • Milston RH, Fitzpatrick MS, Vella AT, Clements S, Gundersen D, Feist G, Crippen TL, Leong J, Schreck CB (2003) Short-term exposure of Chinook salmon (Oncorhynchus tshawytscha) to o, p′-DDE or DMSO during early life history stages causes long-term humoral immunosuppression. Environ Health Perspect 111:1601–1607

    Article  CAS  Google Scholar 

  • Moritomo T, Serata K, Teshirogi K, Aikawa H, Inoue Y, Itou T, Nakanishi T (2003) Flow cytometric analysis of the neutrophil respiratory burst of ayu, Plecoglossus altivelis: comparison with other fresh water fish. Fish Shellfish Immunol 15:29–38

    Article  CAS  Google Scholar 

  • Mos L, Morsey B, Jeffries SJ, Yunker MB, Raverty S, de Guise S, Ross PS (2006) Chemical and biological pollution contribute to the immunological profiles of free-ranging harbour seals. Environ Chem Toxicol 25:3110–3117

    Article  CAS  Google Scholar 

  • Mustafa A, Holladay SD, Goff M, Witowswky S, Kerr R, Reilly C, Spenenberg P, Gogal RM (2008) An enhanced postnatal autoimmune profile in 24 week old C56BL/6 mice developmentally exposed to TCDD. Toxicol Appl Pharmacol 232:51–59

    Article  CAS  Google Scholar 

  • Nakayama A, Kurokawa Y, Harino H, Kawahara E, Miyadai T, Seikai T, Kawai S (2007) Effects of tributyltin on the immune system of Japanese flounder (Paralichthys olivaceus). Aquat Toxicol 83:126–133

    Article  CAS  Google Scholar 

  • Nakayama A, Riesen I, Köllner B, Eppler E, Segner H (2008a) Surface marker-defined head kidney granulocytes and B-lymphocytes of rainbow trout express benzo[a]pyrene-inducible cytochrome P4501A protein. Toxicol Sci 103:86–96

    Article  CAS  Google Scholar 

  • Nakayama K, Kitamura SI, Murakami Y, Song JY, Oh MJ, Iwata H, Tanabe S (2008b) Toxicogenomic analysis of immune system-related genes in Japanese flounder (Paralichtys oliveaceus) exposed to heavy oil. Mar Pollut Bull 57:445–452

    Article  CAS  Google Scholar 

  • Nakayama A, Segner H, Kawai SI (2009) Immunotoxic effects of organotin compounds in teleost fish. In: Arai T, Harino M, Langston WJ (eds) Ecotoxicology of antifouling biocides. Springer, Tokyo, pp 207–218

    Chapter  Google Scholar 

  • Newman MC (2001) Population ecotoxicology. John Wiley & Sons, New York

    Google Scholar 

  • Nonaka M, Smith SL (2000) Complement system of bony and cartilaginous fish. Fish Shellfish Immunol 10:215–228

    Article  CAS  Google Scholar 

  • Ottinger CA, Kaattari SL (2000) Long-term immune dysfunction in rainbow trout (Oncorhynchus mykiss) exposed as embryos to aflatoxin B1. Fish Shellfish Immunol 10:101–106

    Article  CAS  Google Scholar 

  • Owen IPF, Wilson K (1999) Immunocompetence: a neglected life history trait or conspicuous red herring? TREE 14:170–172

    Google Scholar 

  • Pedersen AB, Babayan SA (2011) Wild immunology. Mol Ecol 20:872–880

    Article  CAS  Google Scholar 

  • Prabakaran M, Binuramesh C, Steinhagen D, Michael RD (2006) Immune response and disease resistance of Oreochromis mossambicus to Aeromonas hydrophila after exposure to hexavalent chromium. Dis Aquat Organ 68:189–196

    Article  CAS  Google Scholar 

  • Press CM, Evensen O (1999) The morphology of the immune system in teleost fishes. Fish Shellfish Immunol 9:309–318

    Article  Google Scholar 

  • Quabius ES, Krupp G, Secombes CJ (2005) Polychlorinated biphenyl 126 affects expression of genes involved in stress-immune interaction in primary cultures of rainbow trout anterior kidney cells. Environ Toxicol Chem 24:3053–3060

    Article  CAS  Google Scholar 

  • Relyea R, Hoverman J (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1157–1171

    Article  Google Scholar 

  • Reynaud S, Deschaux P (2006) The effects of polycyclic aromatic hydrocarbons on the immune system of fish: a review. Aquat Toxicol 77:229–238

    Article  CAS  Google Scholar 

  • Rice CD (2001) Fish immunotoxicology: understanding mechanisms of action. In: Schlenk D, Benson WH (eds) Target organ toxicity in marine and freshwater teleosts, vol 2. Taylor & Francis, London, pp 96–138

    Chapter  Google Scholar 

  • Rice CD, Kergosien DH, Adams MS (1996) Innate immune function as a bioindicator of pollution stress in fish. Ecotoxicol Environ Saf 33:186–192

    Article  CAS  Google Scholar 

  • Rohr JR, Schotthoegr AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, Johnson VM, Lieske C, Piwoni MD, Schoff PK, Beasley VR (2008). Agrochemicals increase trematode infections in declining amphibian species. Nature 455:1235–1240

    Google Scholar 

  • Saeij JP, Stet RJ, de Vries BJ, van Muiswinkel WB, Wiegertjes GF (2003) Molecular and functional characterization of carp TNF; a link between TNF polymorphisms and trypano-tolerance? Dev Comp Immunol 27:29–41

    Article  CAS  Google Scholar 

  • Schmidt V, Zander S, Körting W, Broeg K, von Westernhagn H, Dizer H, Hansen PD, Skouras A, Steinhagen D (2003) Parasites of flounder (Paralichthys flesus) from the German Bight, North Sea, and their potential use in biological effects monitoring. Helgol Mar Res 57:262–271

    Article  Google Scholar 

  • Schulte A, Ruehl-Fehlert C (2006) Regulatory aspects of immunotoxicology. Exp Toxicol Pathol 57:385–389

    Article  Google Scholar 

  • Secombes CJ, Cunningham C (2004) Cytokines: an evolutionary perspective. Dev Comp Immunol 28:373–384

    Article  Google Scholar 

  • Segner H (2007) Ecotoxicology—how to asses the impact of toxicants in a multifactorial environment? In: Mothersill C, Mosse I, Seymour C (eds) Multiple stressors: a challenge for the future. NATO Advanced Workshop. Environmental security. Springer, Heidelberg, pp 39–56

    Chapter  Google Scholar 

  • Segner H (2011a) Moving beyond a descriptive aquatic toxicology: the value of biological process and trait information. Aquat Toxicol, in press

  • Segner H (2011b) Reproductive and developmental toxicity in fishes. In: Gupta RC (ed) Reproductive and developmental toxicology. Elsevier, Amsterdam, pp 1145–1166

    Chapter  Google Scholar 

  • Segner H, Möller AM, Wenger M, Casanova-Nakayama A (2011). Fish immunotoxicology: research at the crossroads of immunology, ecology and toxicology. In: Hirawa A (ed) Interdisciplinary studies in environmental chemistry, vol 6. Terra Scientific Publishing Company, Tokyo, pp 1–15

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. TREE 11:317–321

    CAS  Google Scholar 

  • Shen LL, Stuge TB, Zhou H, Khayat M, Barker KS (2002) Channel catfish cytotoxic cells: a mini-review. Dev Comp Immunol 26:141–149

    Article  CAS  Google Scholar 

  • Siwicki AK, Anderson DP (1993) An easy spectrophotometric assay for determining total protein and immunoglobulin levels in fish sera: correlation to fish health. In: Stolen JS, Fletcher TC, Anderson DP, Kaattari SL, Rowley AF (eds) Techniques in fish immunology. SOS Publications, Fair Haven, NJ, pp 23–30

    Google Scholar 

  • Skouras A, Broeg K, Dizer H, von Westernhagen H, Hansen PD, Steinhagen D (2003) The use of innate immune responses as biomarkers in a programme of integrated biological effects monitoring on flounder (Platichthys flesus) from the southern North Sea. Helgol Mar Res 57:190–198

    Article  Google Scholar 

  • Smialowicz RJ, Burgin DE, Williams WC, Diliberto JJ, Setzer RW, Birnbaum LS (2004) CYP1A2 is not required for 2,3,7,8-tetrachlorodibenzo-p-dioxin-indiuced immunosuppression. Toxicology 197:15–22

    Article  CAS  Google Scholar 

  • Song JY, Nakayama K, Murakami Y, Jung SJ, Oh MJ, Matuoka S, Kawakami H, Kitamura SI (2008) Does heavy oil pollution induce bacterial diseases in Japanese flounder, Paralichthys oliveaceus? Mar Pollut Bull 57:889–894

    Article  CAS  Google Scholar 

  • Song JY, Nakayama K, Murakami Y, Kitamura SI (2011) Heavy oil exposure induces high mortalities in virus carrier Japanese flounder, Paralichthys oliveaceus. Mar Pollut Bull 63:362–365

    Article  CAS  Google Scholar 

  • Spitsbergen JM, Blazer VS, Bowser PR, Cheng KC, Cooper KR, Cooper TK, Fraser S, Groman DB, Harper CM, Law JM, Marty GD, Smolowitz RM, St. Leger M, Wolf DC, Wolf JC (2009) Finfish and aquatic invertebrate pathology resources for now and the future. Comp Biochem Physiol 149C:249–257

  • Springman KR, Kurath G, Anderson JJ, Emlen JM (2005) Contaminants as viral cofactors: assessing indirect population effects. Aquat Toxicol 71:13–23

    Article  CAS  Google Scholar 

  • Spromberg JA, Mador JP (2005) Relating results of chronic toxicity responses to population-level effects: modeling effects on wild Chinook salmon populations. Integr Environ Assess Manag 1:9–21

    Article  CAS  Google Scholar 

  • Sunyer JO, Zarkadi IK, Sahu A, Lambris JD (1996) Multiple forms of complement C3 in trout that differ in binding to complement activators. Proc Natl Acad Sci U S A 93:8456–8551

    Article  Google Scholar 

  • Thilagam H, Gopalokrishnan S, Bo J, Wang KJ (2009) Effect of 17β-estradiol on the immunocompetence of Japanese sea bass (Lateolabrax japonicus). Environ Toxicol Chem 28:1722–1731

    Article  CAS  Google Scholar 

  • Trowsdale J, Parham P (2004) Defense strategies and immunity-related genes. Eur J Immunol 34:7–17

    Article  CAS  Google Scholar 

  • Valdez Domingos FX, Oliveira Ribeiro CA, Pelletier E, Rouleau C (2011) Tissue distribution and depuration kinetics of waterborne 14C-labeled light PAHs in mummichog (Fundulus heteroclitus). Environ Sci Technol 45:2684–2690

    Article  CAS  Google Scholar 

  • Warr GW (1983) Immunogloblin of the toadfish, Spheroides glaber. Comp Biochem Physiol B 76:507–514

    Article  CAS  Google Scholar 

  • Weis JS, Smith G, Zou T, Santiago-Bass C, Weis P (2001) Effects of contaminants on behaviour: biochemical mechanisms and ecological consequences. Bioscience 51:209v217

    Google Scholar 

  • Wenger M, Sattler U, Goldschmidt-Clermont E, Segner H (2011) 17beta-Estradiol affects complement components and survival of rainbow trout (Oncorhynchus mykiss) challenged by bacterial (Yersinia ruckeri) infection. Fish Shellfish Immunol 31:90–97

    Article  CAS  Google Scholar 

  • Winans B, Humble MC, Lawrence BP (2011) Environmental toxicants and the developing immune system: a missing link in the global battle against infectious diseases? Repro Toxicol 31:327–336

    Article  CAS  Google Scholar 

  • Yano T (1993) Assays of hemolytic complement activity. In: Stolen JS, Fletcher TC, Kaattari SL, Rowley AF (eds) Techniques in Fish Immunology. SOS Publications, Fair Haven, NJ, pp 131–141

    Google Scholar 

  • Yano T (1996) The nonspecific immune system: humoral defense. In: Iwama G, Nakanishi T (eds) The fish immune system. Fish physiology, vol 15. Academic Press, San Diego, pp 106–157

    Google Scholar 

  • Zapata AG, Chiba A, Varas A (1996) Cells and tissues of the immune system of fish. In: Iwama G, Nakanihi T (eds) The fish immune system: Organism, pathogen and the environment. Academic Press, New York, pp 1–62

    Google Scholar 

  • Zeeman MG, Brindley WA (1981) Effects of toxic agents upon fish immune systems. A review. In: Sharma RP (ed) Immunologic considerations in toxicology. CRC Press, Boca Raton, FL, pp 3–60

    Google Scholar 

  • Zelikoff JT, Raymond A, Carlson E, Li Y, Beaman JR, Anderson M (2000) Biomarkers of immunotoxicity in fish: from the lab to the ocean. Toxicol Lett 112(113):325–331

    Article  Google Scholar 

Download references

Acknowledgment

This study was financially supported in part by the Swiss National Research Foundation, SNF (No. 31003A-130640) to HS.

Author information

Affiliations

  1. Centre for Fish and Wildlife Health, Vetsuisse Faculty, University of Bern, Laenggass-Strasse 122, 3012, Bern, Switzerland

    Helmut Segner, Anja Maria Möller & Ayako Casanova-Nakayama

  2. Neuroendocrine Immune Interactions Research Group, Institute of Anatomy, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland

    Michael Wenger

  3. Institute of Infectiology, Friedrich-Loeffler-Institute, Federal Research Institute for Animal Health, 17493, Greifswald-Insel Riems, Germany

    Bernd Köllner

Authors
  1. Helmut Segner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Wenger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anja Maria Möller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bernd Köllner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ayako Casanova-Nakayama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Helmut Segner.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Segner, H., Wenger, M., Möller, A.M. et al. Immunotoxic effects of environmental toxicants in fish — how to assess them?. Environ Sci Pollut Res 19, 2465–2476 (2012). https://doi.org/10.1007/s11356-012-0978-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-012-0978-x

Keywords

  • Immunotoxicity
  • immune system
  • ecotoxicological risk assessment
  • ecotoxicology
  • ecoimmunology
  • fish