Abstract
Within individuals, immunity may compete with other life history traits for resources, such as energy and protein, and the damage caused by immunopathology can sometimes outweigh the protective benefits that immune responses confer. However, our understanding of the costs of immunity in the wild and how they relate to the myriad energetic demands on free-ranging organisms is limited. The endangered Galapagos sea lion (Zalophus wollebaeki) is threatened simultaneously by disease from domestic animals and rapid changes in food availability driven by unpredictable environmental variation. We made use of this unique ecology to investigate the relationship between changes in immune activity and changes in body condition. We found that during the first three months of life, changes in antibody concentration were negatively correlated with changes in mass per unit length, skinfold thickness and serum albumin concentration, but only in a sea lion colony exposed to anthropogenic environmental impacts. It has previously been shown that changes in antibody concentration during early Galapagos sea lion development were higher in a colony exposed to anthropogenic environmental impacts than in a control colony. This study allows for the possibility that these relatively large changes in antibody concentration are associated with negative impacts on fitness through an effect on body condition. Our findings suggest that energy availability and the degree of plasticity in immune investment may influence disease risk in natural populations synergistically, through a trade-off between investment in immunity and resistance to starvation. The relative benefits of such investments may change quickly and unpredictably, which allows for the possibility that individuals fine-tune their investment strategies in response to changes in environmental conditions. In addition, our results suggest that anthropogenic environmental impacts may impose subtle energetic costs on individuals, which could contribute to population declines, especially in times of energy shortage.
Highlights
Maintaining the immune system and mounting immune responses are costly activities
Disease from domestic animals is a substantial threat to wild carnivores [29,30,31], including pinnipeds [32], so Galapagos sea lion immunity may play an important role in protection against emergent pathogens [33]
Despite the agriculture and tourism on San Cristobal, there is no evidence that the levels of chemical pollutants such as polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDs), dichlorodiphenyltrichloroethane (DDT) and hydrocarbons are present in the bay at higher than background levels [28,34]
Summary
Maintaining the immune system and mounting immune responses are costly activities. The cost of immunity can be evolutionary or genetic, if immune function is selected for and covaries negatively with other fitness-enhancing traits [1]. The cost of immunity can be energetic or physiological, if an immune response consumes resources such as energy and protein that cannot be invested in other activities such as growth, or causes immunopathology [2,3,4,5]. The discipline of ecological immunology or wild immunology aims to disentangle how organisms manage this allocation problem in a variable environment, and to define immunity as a life history trait, theoretically and empirically [8,9,10] In both vertebrates and invertebrates, an experimental increase in energy expenditure on immunity can decrease investment in other life history traits [11,12,13,14]. There are relatively few studies relevant to the costs of immunity in wild mammals (but see [19,20]), so in this study we investigated whether observable patterns were consistent with a physiological cost of immunity in the endangered Galapagos sea lion, by testing for correlations between changes in immune measures with changes in body condition in known individuals over time
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