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Parasites suppress immune-enhancing effect of methionine in nestling great tits

Abstract

After birth, an organism needs to invest both in somatic growth and in the development of efficient immune functions to counter the effects of pathogens, and hence an investment trade-off is predicted. To explore this trade-off, we simultaneously exposed nestling great tits (Parus major) to a common ectoparasite, while stimulating immune function. Using a 2 × 2 experimental design, we first infested half of the nests with hen fleas (Ceratophyllus gallinae) on day 3 post-hatch and later, on day 9–13 post-hatch, and then supplemented half of the nestlings within each nest with an immuno-enhancing amino acid (methionine). We then assessed the non-specific immune response by measuring both the inflammatory response to a lipopolysaccharide (LPS) and assessing the levels of acute phase proteins (APP). In parasite-infested nestlings, methionine had a negative effect on body mass close to fledging. Methionine had an immune-enhancing effect in the absence of ectoparasites only. The inflammatory response to LPS was significantly lower in nestlings infested with fleas and was also lower in nestlings supplemented with methionine. These patterns of immune responses suggest an immunosuppressive effect of ectoparasites that could neutralise the immune-enhancing effect of methionine. Our study thus suggests that the trade-off between investment in life history traits and immune function is only partly dependent on available resources, but shows that parasites may influence this trade-off in a more complex way, by also inhibiting important physiological functions.

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Acknowledgments

We thank Viviana Marri and Yaëlle Bouquet for their assistance in the field, and Verena Saladin for sexing the nestlings with molecular methods. Furthermore, we thank Prof. Bruno Gottstein for comments and discussion. The study was financially supported by the Swiss National Science Foundation and conducted under the permit provided by the Ethical Committee of the Office of Agriculture of the Canton of Bern, Switzerland.

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Correspondence to Michèle Wegmann.

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Communicated by Indrikis Krams.

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Wegmann, M., Voegeli, B. & Richner, H. Parasites suppress immune-enhancing effect of methionine in nestling great tits. Oecologia 177, 213–221 (2015). https://doi.org/10.1007/s00442-014-3138-9

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  • DOI: https://doi.org/10.1007/s00442-014-3138-9

Keywords

  • Acute phase proteins
  • Flea infestation
  • Haptoglobin
  • LPS
  • Methionine supplementation