Abstract

Variation in immunity is influenced by allocation trade-offs that are expected to change between age-classes as a result of the different environmental and physiological conditions that individuals encounter over their lifetime. One such trade-off occurs with carotenoids, which must be acquired with food and are involved in a variety of physiological functions. Nonetheless, relationships between immunity and carotenoids in species where these micronutrients are scarce due to diet are poorly studied. Among birds, vultures show the lowest concentrations of plasma carotenoids due to a diet based on carrion. Here, we investigated variations in the relationships between innate immunity (hemagglutination by natural antibodies and hemolysis by complement proteins), pathogen infection and plasma carotenoids in nestling and adult griffon vultures (Gyps fulvus) in the wild. Nestlings showed lower hemolysis, higher total carotenoid concentration and higher pathogen infection than adults. Hemolysis was negatively related to carotenoid concentration only in nestlings. A differential carotenoid allocation to immunity due to the incomplete development of the immune system of nestlings compared with adults is suggested linked to, or regardless of, potential differences in parasite infection, which requires experimental testing. We also found that individuals with more severe pathogen infections showed lower hemagglutination than those with a lower intensity infection irrespective of their age and carotenoid level. These results are consistent with the idea that intraspecific relationships between innate immunity and carotenoids may change across ontogeny, even in species lacking carotenoid-based coloration. Thus, even low concentrations of plasma carotenoids due to a scavenger diet can be essential to the development and activation of the immune system in growing birds.

Highlights

  • Immunity, defined as the capacity to fight or control parasitic or pathogenic infection, is one of the major physiological mechanisms regulating survival and a crucial determinant of fitness in PLOS ONE | DOI:10.1371/journal.pone.0141759 November 6, 2015Innate Immunity and Plasma Carotenoids in Vultures animals [1]

  • Our study provides an empirical evaluation of innate immunity variability in adults and nestlings in relation to the natural variation of plasma carotenoids in a large long-lived vulture

  • We found age-related differences in one component of the innate immunity, plasma carotenoid concentration and pathogen infection

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Summary

Introduction

Immunity, defined as the capacity to fight or control parasitic or pathogenic infection, is one of the major physiological mechanisms regulating survival and a crucial determinant of fitness in PLOS ONE | DOI:10.1371/journal.pone.0141759 November 6, 2015Innate Immunity and Plasma Carotenoids in Vultures animals [1]. Because optimal trade-offs can change across an individual’s lifetime as a result of variation in environmental and physiological factors, determining whether age influences the relationship of the immune system with other physiological factors can yield important insights into the mechanisms shaping immunity, and how immune responses are related to other life-history traits. Other studies found that immune activation can reduce circulating carotenoid levels in birds [11,12, 15,16,17,18,19] Taken together, these results indicate that immunity is influenced by environmental and individual physiological conditions, and that mounting an immune response can divert carotenoids from the blood stream, allowing individuals in good condition to better afford the costs of immune defense

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