Telomeres are highly conserved regions of DNA that protect the ends of linear chromosomes. The loss of telomeres can signal an irreversible change to a cell's state, including cellular senescence. Senescent cells no longer divide and can damage nearby healthy cells, thus potentially placing them at the crossroads of cancer and ageing. While the epidemiology, cellular and molecular biology of telomeres are well studied, a newer field exploring telomere biology in the context of ecology and evolution is just emerging. With work to date focusing on how telomere shortening relates to individual mortality, less is known about how telomeres relate to ageing rates across species. Here, we investigated telomere length in cross-sectional samples from 19 bird species to determine how rates of telomere loss relate to interspecific variation in maximum lifespan. We found that bird species with longer lifespans lose fewer telomeric repeats each year compared with species with shorter lifespans. In addition, phylogenetic analysis revealed that the rate of telomere loss is evolutionarily conserved within bird families. This suggests that the physiological causes of telomere shortening, or the ability to maintain telomeres, are features that may be responsible for, or co-evolved with, different lifespans observed across species.This article is part of the theme issue ‘Understanding diversity in telomere dynamics'.
a b s t r a c tCentral place foragers, such as breeding seabirds, need to commute between their nests and foraging grounds, thus close proximity of the breeding colony to productive oceanographic features might be beneficial for seabird reproduction. We tested this hypothesis by investigating the at-sea foraging and breeding behavior of thick-billed murres (Uria lomvia) nesting at three colonies (Bogoslof, St. Paul, and St. George Islands) in the Bering Sea located at different distances from the productive continental shelf-break. We found that distances to feeding areas differed only during night trips among colonies. St. Paul murres foraged entirely on the shelf, whereas St. George murres commuted to the continental shelf-break at night and foraged on the shelf during the day. Bogoslof murres foraged in oceanic waters in close proximity to the colony. Murres breeding at the both Pribilof colonies spent less time attending nests and had higher levels of stress hormone corticosterone compared to murres breeding at Bogoslof, although chick-provisioning rates and fledging success were similar among the three colonies. Lower nest attendance and higher corticosterone suggest lower food availability in the Pribilof domain compared to the Bogoslof region. Murres breeding at the Pribilofs used different foraging strategies to buffer effects of food shortages on their reproduction: flight costs associated with longer distance night trips at St. George were presumably balanced by benefits of higher density and/or more lipid rich prey in the continental shelf-break regions, whereas the additional distance of St. Paul from the continental shelf-break may have outweighed any energetic gain. Murres exhibited a remarkable degree of plasticity of foraging strategies in response to changes in their food availability, but the breeding success of murres did not reflect either food limitations or the colony proximity to productive oceanographic features.
As central-place foragers, seabirds from colonies located close to multiple and/or productive marine habitats might experience increased foraging opportunities and enhanced resilience to food shortages. We tested whether this hypothesis might explain divergent trends in 3 populations of black-legged kittiwakes Rissa tridactyla, a surface-feeding piscivore, in the eastern Bering Sea. We simultaneously studied the foraging behavior, diet, nutritional stress, and breeding performance of chick-rearing kittiwakes from 2 continental shelf colonies (St. Paul and St. George) and an oceanic colony (Bogoslof). Although shelf-based forage fishes were rare or absent in bird diets during the cold study year, not all kittiwakes from the 3 colonies concentrated foraging along the productive shelf break habitats. Compared to the oceanic colony, birds from both shelf-located colonies had lower chick provisioning rates, higher levels of nutritional stress, and lower breeding performance. Although birds from both shelf-based colonies foraged in nearby neritic habitats during daytime, birds from St. George, a stable population located closest to the continental shelf break, also conducted long overnight trips to the ocean basin to feed on lipid-rich myctophids. In contrast, birds from St. Paul, a declining population located farthest from shelf break/oceanic habitats, fed exclusively over the shelf and obtained less high-energy food. Birds from Bogoslof, an increasing population, foraged mainly on myctophids close to the colony in the oceanic basin and Aleutian coast habitats. Our study suggests that proximity to multiple foraging habitats may explain divergent population trends among colonies of kittiwakes in the southeastern Bering Sea.
Early-life conditions can drive ageing patterns and life history strategies throughout the lifespan. Certain social, genetic and nutritional developmental conditions are more likely to produce high-quality offspring: those with good likelihood of recruitment and productivity. Here, we call such conditions "favoured states" and explore their relationship with physiological variables during development in a long-lived seabird, the black-legged kittiwake (Rissa tridactyla). Two favoured states were experimentally generated by manipulation of food availability and brood size, while hatching order and sex were also explored as naturally generating favoured states. Thus, the favoured states we explored were high food availability, lower levels of sibling competition, hatching first and male sex. We tested the effects of favoured developmental conditions on growth, stress, telomere length (a molecular marker associated with lifespan) and nestling survival. Generation of favoured states through manipulation of both the nutritional and social environments furthered our understanding of their relative contributions to development and phenotype: increased food availability led to larger body size, reduced stress and higher antioxidant status, while lower sibling competition (social environment) led to lower telomere loss and longer telomere lengths in fledglings. Telomere length predicted nestling survival, and wing growth was also positively correlated with telomere length, supporting the idea that telomeres may indicate individual quality, mediated by favoured states.
Citation: Barger, C. P., R. C. Young, A. Will, M. Ito, and A. S. Kitaysky. 2016. Resource partitioning between sympatric seabird species increases during chick-rearing. Ecosphere 7(9):e01447. 10. 1002/ecs2.1447 Abstract. Partitioning of resources by competing species of seabirds may increase during periods of food shortages and elevated energy demands. Here, we examined whether food resource partitioning (differential use of foraging habitat or the consumption of different prey species) between common murres (COMU, Uria aalge) and thick-billed murres (TBMU, U. lomvia) breeding on the same colony in the Bering Sea increases with a predictable increase in energy demands between the incubation and chick-rearing stages of reproduction. We assessed the seasonal dynamics of food availability via corticosterone (CORT) levels and examined adult diet (via stable isotope analysis of nitrogen and carbon, SI) and chick diets (based on nest observations). We compared chick provisioning patterns and examined the characteristics of parental foraging habitat via deployment of bird-borne temperature-depth recorders. We found that CORT levels remained low and similar between the species and reproductive stages, reflecting relatively stable and favorable foraging conditions for both murre species during the study period. Comparisons of SI between murres and their potential prey indicated that diets were similar between the species during incubation and diverged during chick-rearing. Chick-rearing common and thick-billed murres also used different foraging habitats, as reflected in travel distances to foraging areas and sea surface temperature distributions of their foraging dives. TBMUs performed shorter foraging trips, deeper dives and delivered squid to their chicks, while COMUs foraged farther from the colony, performed shallower dives, and delivered fish species to their chicks. These results suggest that food resource partitioning between murre species increased during chick-rearing under favorable foraging conditions. Whether the dietary segregation reflected species-specific differences in adults' foraging efficiency, differences in chicks' dietary requirements, or was a way of reducing competition remains unknown. Regardless of the causal mechanism(s), food resource partitioning might ameliorate interspecific competition between sympatrically breeding birds during periods of increased energy demands.
The examination of telomere dynamics is a recent technique in ecology for assessing physiological state and age-related traits from individuals of unknown age. Telomeres shorten with age in most species and are expected to reflect physiological state, reproductive investment, and chronological age. Loss of telomere length is used as an indicator of biological aging, as this detrimental deterioration is associated with lowered survival. Lifespan dimorphism and more rapid senescence in the larger, shorter-lived sex are predicted in species with sexual size dimorphism, however, little is known about the effects of behavioral dimorphism on senescence and life history traits in species with sexual monomorphism. Here we compare telomere dynamics of thick-billed murres ( Uria lomvia ), a species with male-biased parental care, in two ways: 1) cross-sectionally in birds of known-age (0-28 years) from one colony and 2) longitudinally in birds from four colonies. Telomere dynamics are compared using three measures: the telomere restriction fragment (TRF), a lower window of TRF (TOE), and qPCR. All showed age-related shortening of telomeres, but the TRF measure also indicated that adult female murres have shorter telomere length than adult males, consistent with sex-specific patterns of ageing. Adult males had longer telomeres than adult females on all colonies examined, but chick telomere length did not differ by sex. Additionally, inter-annual telomere changes may be related to environmental conditions; birds from a potentially low quality colony lost telomeres, while those at more hospitable colonies maintained telomere length. We conclude that sex-specific patterns of telomere loss exist in the sexually monomorphic thick-billed murre but are likely to occur between fledging and recruitment. Longer telomeres in males may be related to their homogamous sex chromosomes (ZZ) or to selection for longer life in the care-giving sex. Environmental conditions appeared to be the primary drivers of annual changes in adult birds.
We hypothesized that changes in southeastern Bering Sea foraging conditions for black-legged kittiwakes (Rissa tridactyla) have caused shifts in habitat use with direct implications for population trends. To test this, we compared at-sea distribution, breeding performance, and nutritional stress of kittiwakes in three years (2008–2010) at two sites in the Pribilof Islands, where the population has either declined (St. Paul) or remained stable (St. George). Foraging conditions were assessed from changes in (1) bird diets, (2) the biomass and distribution of juvenile pollock (Theragra chalcogramma) in 2008 and 2009, and (3) eddy kinetic energy (EKE; considered to be a proxy for oceanic prey availability). In years when biomass of juvenile pollock was low and patchily distributed in shelf regions, kittiwake diets included little or no neritic prey and a much higher occurrence of oceanic prey (e.g. myctophids). Birds from both islands foraged on the nearby shelves, or made substantially longer-distance trips overnight to the basin. Here, feeding was more nocturnal and crepuscular than on the shelf, and often occurred near anticyclonic, or inside cyclonic eddies. As expected from colony location, birds from St. Paul used neritic waters more frequently, whereas birds from St. George typically foraged in oceanic waters. Despite these distinctive foraging patterns, there were no significant differences between colonies in chick feeding rates or fledging success. High EKE in 2010 coincided with a 63% increase in use of the basin by birds from St. Paul compared with 2008 when EKE was low. Nonetheless, adult nutritional stress, which was relatively high across years at both colonies, peaked in birds from St. Paul in 2010. Diminishing food resources in nearby shelf habitats may have contributed to kittiwake population declines at St Paul, possibly driven by increased adult mortality or breeding desertion due to high foraging effort and nutritional stress.
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