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Oestrogenic pollutants promote the growth of a parasite in male sticklebacks

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      Highlights

      • E2 exposure had no effect on the susceptibility of sticklebacks to parasite infection.
      • E2 elevated VTG levels in males and females.
      • E2 increased the growth of parasites in male, not female, fish.
      • Parasite mass correlated with VTG levels among males, but not females.

      Abstract

      Aquatic environments are especially susceptible to anthropogenic chemical pollution. Yet although knowledge on the biological effects of pollutants on aquatic organisms is increasing, far less is known about how ecologically-important interspecific interactions are affected by chemicals. In particular, the consequences of anthropogenic pollution for the interaction of hosts and parasites are poorly understood. Here, we examine how exposure to 17β-oestradiol (E2)—a natural oestrogen and a model endocrine disrupting chemical (EDC) —affects infection susceptibility and emergent infection phenotypes in an experimental host–parasite system; three spined sticklebacks ( Gasterosteus aculeatus) infected with the common, debilitating cestode Schistocephalus solidus. We exposed individual sticklebacks to a 0 ng l −1 (control), 10 ng l −1 or 100 ng l −1 E2 treatment before feeding them infective stages of S. solidus. E2 exposure significantly elevated vitellogenin (VTG) levels—a biomarker of exposure to xenoestrogens—in both female and male fish, and reduced their body condition. Susceptibility to parasite infection was unaffected by EDC exposure; however, E2 treatment and fish sex interacted significantly to determine the growth rate of parasites, which grew quickest in male hosts held under the higher (100 ng l −1) E2 treatment. Tissue VTG levels and parasite mass correlated positively across the whole sample of experimentally infected fish, but separate regressions run on the male and female datasets demonstrated a significant relationship only among male fish. Hence, among males—but not females—elevated VTG levels elicited by E2 exposure led to more rapid parasite growth. We outline plausible physiological mechanisms that could explain these results. Our results demonstrate that oestrogenic pollutants can alter host–parasite interactions by promoting parasite growth, and that male hosts may be disproportionately affected. Because ecologically-relevant effects of infection on host antipredator responses, growth, energetics and reproductive development all depend on parasite mass in this host–parasite system, our results indicate that EDCs can mediate the ecological consequences of infections. We therefore consider the implications of our results for the ecology of hosts and parasites in polluted environments.

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      Most cited references 76

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        The stress response in teleost fish shows many similarities to that of the terrestrial vertebrates. These concern the principal messengers of the brain-sympathetic-chromaffin cell axis (equivalent of the brain-sympathetic-adrenal medulla axis) and the brain-pituitary-interrenal axis (equivalent of the brain-pituitary-adrenal axis), as well as their functions, involving stimulation of oxygen uptake and transfer, mobilization of energy substrates, reallocation of energy away from growth and reproduction, and mainly suppressive effects on immune functions. There is also growing evidence for intensive interaction between the neuroendocrine system and the immune system in fish. Conspicuous differences, however, are present, and these are primarily related to the aquatic environment of fishes. For example, stressors increase the permeability of the surface epithelia, including the gills, to water and ions, and thus induce systemic hydromineral disturbances. High circulating catecholamine levels as well as structural damage to the gills and perhaps the skin are prime causal factors. This is associated with increased cellular turnover in these organs. In fish, cortisol combines glucocorticoid and mineralocorticoid actions, with the latter being essential for the restoration of hydromineral homeostasis, in concert with hormones such as prolactin (in freshwater) and growth hormone (in seawater). Toxic stressors are part of the stress literature in fish more so than in mammals. This is mainly related to the fact that fish are exposed to aquatic pollutants via the extensive and delicate respiratory surface of the gills and, in seawater, also via drinking. The high bioavailability of many chemicals in water is an additional factor. Together with the variety of highly sensitive perceptive mechanisms in the integument, this may explain why so many pollutants evoke an integrated stress response in fish in addition to their toxic effects at the cell and tissue levels. Exposure to chemicals may also directly compromise the stress response by interfering with specific neuroendocrine control mechanisms. Because hydromineral disturbance is inherent to stress in fish, external factors such as water pH, mineral composition, and ionic calcium levels have a significant impact on stressor intensity. Although the species studied comprise a small and nonrepresentative sample of the almost 20,000 known teleost species, there are many indications that the stress response is variable and flexible in fish, in line with the great diversity of adaptations that enable these animals to live in a large variety of aquatic habitats.
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            Author and article information

            Affiliations
            [a ]Department of Neuroscience, Psychology and Behaviour, College of Medicine, Biological Sciences and Psychology, University of Leicester, Leicester LE1 7RH, UK
            [b ]Cefas Weymouth Laboratory, The Nothe, Weymouth DT4 8UB, UK
            Author notes
            [* ]Corresponding author at: Department of Neuroscience, Psychology and Behaviour, Adrian Building, University of Leicester, University Road, Leicester LE1 7RH, UK. Fax: +44 116 252 3330.Department of NeurosciencePsychology and BehaviourCollege of MedicineBiological Sciences and PsychologyUniversity of LeicesterLeicesterLE1 7RHUK ib50@ 123456le.ac.uk
            Contributors
            Journal
            Aquat Toxicol
            Aquat. Toxicol
            Aquatic Toxicology (Amsterdam, Netherlands)
            Elsevier/North Holland Biomedical Press
            0166-445X
            1879-1514
            1 May 2016
            May 2016
            : 174
            : 92-100
            26922400 4827130 S0166-445X(16)30031-5 10.1016/j.aquatox.2016.02.010
            © 2016 The Authors

            This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

            Categories
            Article

            Toxicology

            oestrogens, infection phenotype, disease, pollution, parasitism, endocrine disruption

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