The physiological declines associated with senescence, including declines in both innate and acquired immune defenses against parasites and pathogenic microorganisms, have been thoroughly documented in laboratory animals and humans (Wollscheid-Lengeling, 2004). But the fitness deficits associated with advancing age in the wild, where animals experience a full range of natural hazards, stresses and diseases, are far less well understood (Miller, 1996). Recently, reliable aging-related declines in aspects of either cellular or humoral immunity have been reported in wild populations of several bird species, including barn swallows (Hirundo rustica), collared flycatchers (Ficedula hypoleuca), and ruffs (Philomachus pugnax) (Saino et al., 2003; Cichon et al., 2003; Lozano and Lank, 2003).
Lozano and Lank measured cell-mediated immunity in the ruff, a shorebird, using a measure of delayed hypersensitivity to phytohemagglutinin, a nonspecific mitogen foreign to the avian immune system. Males showed a marginally significant age-related decline in cellular immune response; this effect was more pronounced in nonbreeding than in breeding males, which probably expend significant amounts of energy defending territories. In a study focusing on the humoral immune response of barn swallows by Saino et al. (2003), banded swallows were immunized repeatedly against Newcastle disease virus. Breeding individuals showed declining antibody responses with advancing age (barn swallows live 5 to 7 years in the wild), and this trend was more likely to be statistically significant for females. Secondary humoral responses were considerably lower overall in females than males, as were initial antibody titers prior to secondary vaccination. This finding is consistent with the greater parental investment typical of females in this species. Cichon et al. (2003) challenged the immune systems of nesting female flycatchers with sheep red blood cells, another nonspecific antigen. Older females mounted an antibody response only about half that shown by younger breeders. This result was correlated with a trend for older females to fledge offspring of lower body mass than those of young and middle-aged birds.
It remains unclear what contribution such age-related changes in immune responses actually make to senescence-related mortality in the wild, where environmental factors may be more important physiological stressors than the effects of aging. Studies like these, however, represent an exciting effort by ecologists and field zoologists to begin incorporating reliable biomarkers of aging into studies of population biology and mating systems, life-history evolution, or other aspects of avian behavioral ecology.
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