Patterns of aging in the long-lived wandering albatross

Abstract

How does an animal age in natural conditions? Given the multifaceted nature of senescence, identifying the effects of age on physiology and behavior remains challenging. We investigated the effects of age on a broad array of phenotypic traits in a wild, long-lived animal, the wandering albatross. We studied foraging behavior using satellite tracking and activity loggers in males and females (age 6-48+ years), and monitored reproductive performance and nine markers of baseline physiology known to reflect senescence in vertebrates (humoral immunity, oxidative stress, antioxidant defenses, and hormone levels). Age strongly affected foraging behavior and reproductive performance, but not baseline physiology. Consistent with results of mammal and human studies, age affected males and females differently. Overall, our findings demonstrate that age, sex, and foraging ability interact in shaping aging patterns in natural conditions. Specifically, we found an unexpected pattern of spatial segregation by age; old males foraged in remote Antarctica waters, whereas young and middle-aged males never foraged south of the Polar Front. Old males traveled a greater distance but were less active at the sea surface, and returned from sea with elevated levels of stress hormone (corticosterone), mirroring a low foraging efficiency. In contrast to findings in captive animals and short-lived birds, and consistent with disposable soma theory, we found no detectable age-related deterioration of baseline physiology in albatrosses. We propose that foraging efficiency (i.e., the ability of individuals to extract energy from their environment) might play a central role in shaping aging patterns in natural conditions.