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, longlived 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 shortlived 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. senescence | foraging | immunity | oxidative stress | sex S enescence, a decline in fitness with advancing age, has been documented across a wide range of wild animals (1-3). There is an ongoing debate in the literature regarding the proximate mechanisms underpinning senescence. Age-associated immune dysfunction (referred to as immunosenescence) and increased susceptibility to oxidative stress are strong candidates as the major driving forces behind senescence in humans and laboratory animal models (4-6), but their relevance in natural populations remains unclear. Because of their generally longer lifespan compared with mammals, birds have emerged as predominant models for studying aging (7,8). The first studies on senescence were restricted almost entirely to investigations of age-dependent mortality or breeding performance (1). More recent pioneering studies that focused on proximal physiological patterns of aging in free-living birds yielded contrasting results; senescence was linked with decreased humoral immune response (9), increased oxidative stress (10), altered plasma levels of some hormones (refs. 2, 11; but see ref. 12), and decreased metabolic rate (ref. 13, but see ref. 14).Foraging behavior, the set of processes by which organisms acquire energy and nutrients (15), merits specific attention, because it may play a k...

Senescence rates and late adulthood reproductive success are strongly influenced by personality in a long-lived seabird

“…Male wandering albatrosses are known to forage further south with increasing age [24,29], and here we can suggest that these changes in foraging behaviour are driven predominantly by bolder individuals making longer foraging trips in later adulthood. Boldness is often correlated with explorative behaviour [9] and superficial exploration [11,36] and so bolder individuals may be more likely to explore further from the colony when ageing.…”

“…We combine these data with foraging measures from 205 individuals, across 307 trips, to examine whether boldness is linked to changes in foraging behaviour and efficiency with age. As previous work has found stronger senescence in reproductive success in males of this species [21,24], we extend these analyses to consider sexually antagonistic effects. If males demonstrate greater changes in foraging behaviour and reproductive success with age, we suggest that the interaction with personality may be stronger in this sex.…”

“…Boldness has previously been shown to be repeatable and heritable in this species [22], and albatrosses show strong age-specific variation in life-history traits such as senescence in reproductive success [19 -21,23] and changes in foraging behaviour with age [24], all of which are found predominantly in males. Furthermore, in a closely related species, the black browed albatross (Thalassarche melanophrys), personality has been shown to have sexually antagonistic effects on fitness, mediated by environmental conditions [25], but age effects were unexplored.…”

Demographic consequences of heavy metals and persistent organic pollutants in a vulnerable long-lived bird, the wandering albatross

“…However, in this population, fecundity declined in the oldest individuals (35þ years old [24,38]), while Hg levels tended to decrease with age [16] and POP levels were unrelated to age (data not shown). Moreover, age (6 -48þ years old) did not affect humoural immunity, oxidative stress, antioxidant defences or hormone levels in wandering albatrosses [38]. Hence, it is unlikely that age was a confounding factor in the correlation between contaminants and physiological mechanisms underlying breeding performance.…”

Life-History Differences in Age-Dependent Expressions of Multiple Ornaments and Behaviors in a Lekking Bird

“…Moreover, many previous studies have focused on single sexually selected traits (e.g., antler size [Nussey et al 2009] and tail feather length [Balbontín et al 2011]). However, sexual selection is clearly a multifaceted process, so investigating multiple traits simultaneously is needed to unravel the constraints and trade-offs acting on these traits (Evans et al 2011) and to accurately quantify the overall fitness costs of trait expression (Kotiaho 2001;Lecomte et al 2010). Finally, age-dependent expressions of sexual traits has not yet been quantified in relation to temporal scheduling of individual reproductive effort, where peak reproductive effort is expected to differ among individuals depending on their current body condition and, hence, may be the only opportunity during which all traits are expressed at their maximum.…”