Ageing gracefully: physiology but not behaviour declines with age in a diving seabird

Abstract

Summary 1.A higher proportion of long-lived animals die from senescence than short-lived animals, yet many long-lived homeotherms show few signs of physiological ageing in the wild. This may, however, differ in long-lived diving homeotherms that frequently encounter hypoxic conditions and have very high metabolic rates. 2. To examine ageing within a long-lived diving homeotherm, we studied resting metabolism and thyroid hormones (N = 43), blood oxygen stores (N = 93) and foraging behaviour (N = 230) of thick-billed murres (Uria lomvia). Because murres dive exceptionally deep for their size and have a very high metabolism, we expected that ageing murres would show signs of physiological senescence. We paid particular attention to resting metabolism as we argue that these maintenance costs reflect those experienced during deep dives. 3. Blood oxygen stores (haematocrit), resting metabolic rate and thyroid hormone levels all declined significantly with age in incubating murres 3-30 years of age. In birds measured longitudinally 3 years apart, thyroid hormone levels and haematocrit were both significantly lower, suggesting progressive changes within individuals rather than selective disappearance of individuals with high metabolic rates. Within our longitudinal data set, we found no effect of age on dive depth, dive shape or behavioural aerobic dive limit. 4. A meta-analysis of changes in resting metabolism with age across 15 animal species demonstrated that such declines are pervasive across most of the kingdom. The rate of decline was highest in species with high energy expenditure supporting a linkage between metabolism and senescence. 5. Physiological changes occurred in tandem with advancing age in murres, but offset each other such that there was no detectable decline in behavioural performance.Key-words: basal metabolic rate, behavioural senescence, cost of hypoxia, diving, physiological senescence, rate of living theory, resting metabolic rate, thick-billed murre

Telomere length is a strong predictor of foraging behavior in a long‐lived seabird

“…Previous work has shown that murre behavior is relatively constant throughout the lifespan, while physiological parameters change with age (Elliott et al 2014). Some behavioral parameters did not change with telomere length in our study, yet others were strongly related to this telomeric parameter of physiological aging.…”

“…Elliott et al (2014) found that thyroid hormones, hematocrit, and metabolic rate all declined with age while diving and flying patterns remained the same. In our previous work (Young et al, unpublished manuscript) we found that under good conditions stress levels increased with telomere degradation, but attendance at the nest and rate of chickprovisioning trips did not.…”

“…Telomere length and spatial habitat choice Previous work with murres has shown that they make physiological trade-offs rather than compromise parental and foraging behaviors as they age chronologically or through telomere degradation (Elliott et al 2014;Young et al, unpublished manuscript). Elliott et al (2014) found that thyroid hormones, hematocrit, and metabolic rate all declined with age while diving and flying patterns remained the same.…”

“…Lowered metabolic rates in older birds (Elliott et al 2014) might have inhibited diving ability. The ability to maintain diving depth while expressing a physiologically deteriorated phenotype is yet more evidence that behavior is maintained while physiology declines in murres (Elliott et al 2014). At the same time, birds with longer telomeres dove less efficiently than those with short telomeres.…”

“…It is also possible that the differences in stable isotope signatures indicated that birds differing in telomere length may also differ in isotopic turnover rates. Declines in isotopic turnover may be age-related, as older murres have a lower metabolic rate (Elliott et al 2014) or could be making seasonal shifts in diet later or more slowly than younger birds. Diet composition shifts as birds move from incubation to chickrearing (Williams et al 2008), and although the process of turnover is not important to this study, it is a potential explanation of the differences in stable isotope signatures.…”