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Immunotoxic Effects of Environmental Toxicants in Fish — How to Assess Them?

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Immunotoxic Effects of Environmental Toxicants in Fish — How to Assess Them? View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by RERO DOC Digital Library Environ Sci Pollut Res (2012) 19:2465–2476 DOI 10.1007/s11356-012-0978-x 15TH INTERNATIONAL SYMPOSIUM ON TOXICITY ASSESSMENT Immunotoxic effects of environmental toxicants in fish — how to assess them? Helmut Segner & Michael Wenger & Anja Maria Möller & Bernd Köllner & Ayako Casanova-Nakayama Received: 3 December 2011 /Accepted: 9 May 2012 # Springer-Verlag 2012 Abstract Numerous environmental chemicals, both long- assess chemical impact on the immune system using param- known toxicants such as persistent organic pollutants as eters at different levels of complexity and integration: im- well as emerging contaminants such as pharmaceuticals, mune mediators, humoral immune effectors, cellular are known to modulate immune parameters of wildlife spe- immune defenses, macroscopical and microscopical cies, what can have adverse consequences for the fitness of responses of lymphoid tissues and organs, and host resis- individuals including their capability to resist pathogen tance to pathogens. Importantly, adverse effects of chemi- infections. Despite frequent field observations of impaired cals on immunocompetence may be detectable only after immunocompetence and increased disease incidence in immune system activation, e.g., after pathogen challenge, contaminant-exposed wildlife populations, the potential rel- but not in the resting immune system of non-infected fish. evance of immunotoxic effects for the ecological impact of Current limitations to further development and implementa- chemicals is rarely considered in ecotoxicological risk as- tion of immunotoxicity assays and parameters in ecotoxico- sessment. A limiting factor in the assessment of immuno- logical risk assessment are not primarily due to technological toxic effects might be the complexity of the immune system constraints, but are related from insufficient knowledge of (1) what makes it difficult (1) to select appropriate exposure and possible modes of action in the immune system, (2) the effect parameters out of the many immune parameters which importance of intra- and inter-species immune system vari- could be measured, and (2) to evaluate the significance of ability for the response against chemical stressors, and (3) the selected parameters for the overall fitness and immuno- deficits in conceptual and mechanistic assessment of combi- competence of the organism. Here, we present — on the nation effects of chemicals and pathogens. example of teleost fishes — a brief discussion of how to Keywords Immunotoxicity . immune system . Responsible editor: Philippe Garrigues ecotoxicological risk assessment . ecotoxicology . H. Segner (*) : A. M. Möller : A. Casanova-Nakayama ecoimmunology . fish Centre for Fish and Wildlife Health, Vetsuisse Faculty, University of Bern, Laenggass-Strasse 122, Introduction 3012 Bern, Switzerland e-mail: [email protected] Ecology investigates the processes that keep ecological sys- M. Wenger tems functioning. Ecotoxicology deals with the risk of toxic Neuroendocrine Immune Interactions Research Group, chemicals to disrupt the functioning of ecological systems. Institute of Anatomy, University of Zurich, Winterthurerstrasse 190, Traditionally, ecotoxicology assesses the ecological impact 8057 Zurich, Switzerland of environmental toxicants by determining chemical effects on growth and reproduction of species, as changes of these B. Köllner parameters may translate into altered population density, Institute of Infectiology, Friedrich-Loeffler-Institute, Federal Research Institute for Animal Health, although this translation is not a linear, deterministic process 17493 Greifswald-Insel Riems, Germany but is influenced by a number of extrinsic and intrinsic 2466 Environ Sci Pollut Res (2012) 19:2465–2476 processes (Newman 2001; Calow and Forbes 2003; Segner Chemicals impair the immunocompetence of exposed 2007, 2011a). Toxicant-induced alterations of population organisms through a variety of mechanisms, including in- density are not only relevant for the directly impacted spe- terference with signalling pathways in immune cells, sup- cies but can indirectly affect other species. For instance, if a pressing immune functions such as oxidative burst activity, toxic chemical is lethal to a predator species, this will induction of apoptosis (Bols et al. 2001; Köllner et al. 2002; directly affect predator density, and indirectly prey species Reynaud and Deschaux 2006; Nakayama et al. 2009), but density (e.g., Fleeger et al. 2003). Importantly, species inter- also through trade-offs between energetically costly immune actions are not only affected through chemical-induced defenses and the energy demands of the toxicant defense (cf. changes in species density but also through effects on spe- Segner et al. 2011). In ecology, the importance of the im- cies traits (Relyea and Hoverman 2006). Particularly sub- mune system in an organism’s evolutionary, ecological and lethal concentrations of toxicants which remain without life history context is well recognized (Sheldon and Verhulst overt effects on the density-related parameters, survival 1996; Demas et al. 2011), while in ecotoxicology there and reproduction, still may have consequences for species exists no corresponding awareness of the importance of a interactions by inducing changes of behavioural or physio- functional immune system for survival in a polluted logical traits. An example of a trait-mediated effect would environment. be chemical-induced altered foraging behaviour of a preda- Assessing immunotoxic effects is not straightforward, as tor species which will then lead to altered density of the prey the immune system is complex and multifaceted. This species (Weis et al. 2001;RelyeaandHoverman2006). means that the chemicals can affect immunocompetence Another example of trait-mediated effects on species inter- through a wide range of mechanisms and via diverse targets. actions are the effects of chemicals on host–pathogen sys- Also, to establish the relevance of a toxicant-induced change tems: Exposure to toxic chemicals can impair the in a selected immune parameter for the overall immune immunocompetence of the host species, so that the adverse status of the organism is a difficult task, since the overall ecological outcome results not from the chemical toxicity immunocompetence of the individual is more than the sum per se, but from the indirect effect of the chemical on the of the individual parts. It is the aim of the present commu- capacity of the host species to interact with and to resist to nication to briefly discuss several aspects that can be of the pathogen. For assessing the consequences of chemical relevance in designing an immunotoxicological study. contamination for ecological systems, we have to consider In particular, we will address which immune parameters both density- and trait-mediated toxic impacts (Relyea and might be selected at different levels of complexity, from Hoverman 2006). simple indicative responses to the evaluation of altered A number of field studies have shown that the impact of immunocompetence, and how the response of immune chemical contamination on the immunocompetence on parameters to chemical impact varies with the activation wildlife species bears ecological relevance (Luebke et al. status of the immune system. For this discussion, we 1997). Prominent examples come from studies on the causes will focus on teleostean fishes, because (1) they are an of the global decline in amphibian populations, which important animal group in ecotoxicology, (2) knowledge showed that exposure to pollutants can lead to compromised on the fish immune system has impressively grown over immune function and increased infection rate with parasites the last decades what opens new avenues and possibil- (Kiesecker 2002; Rohr et al. 2008). Other examples include ities to the study of immunotoxic effects, and (3) there the outbreak of distemper virus in PCB-contaminated har- exists a reasonably good body of both laboratory and bour seals and harbour porpoises (Beinecke et al. 2005; Mos field observations on immmunotoxic effects in this an- et al. 2006) or the increased disease susceptibility and inci- imal group. It is not the aim of this work to provide an dence in fishes from the polyaromatic hydrocarbon (PAH)- comprehensive review on fish immunotoxicology, as contaminated Puget Sound (Arkoosh et al. 1998, 2001). there are several recent reviewss available (Rice 2001; Also for invertebrate species, there exist a number of reports Burnett 2005; Carlson and Zelikoff 2008), but to high- of increased disease incidence in populations from contam- light specificities that have to be considered in assessing inated environments (Galloway and Depledge 2001). immunotoxicity. Good immunocompetence is a critical fitness determi- nant, as in their natural environment organisms are constant- ly exposed to pathogens (Graham et al. 2010). The threat The immune system of teleost fish — a starter which pathogens impose on host species is evident from the fact that host–pathogen interactions are a major driver in the In general, the immune system protects organism homeosta- evolution of life histories. Good immunocompetence ena- sis and integrity by monitoring any alteration of cells and bles the individual to maintain good health so as to mini- tissues caused either by internal (age, neoplastic prolifera- mize the fitness costs of infection (Owen and Wilson
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