Effects of developmental conditions on growth, stress and telomeres in black-legged kittiwake chicks.

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.

Adverse foraging conditions may impact body mass and survival of a high Arctic seabird.

Tradeoffs between current reproduction and future survival are widely recognized, but may only occur when food is limited: when foraging conditions are favorable, parents may be able to reproduce without compromising their own survival. We investigated these tradeoffs in the little auk (Alle alle), a small seabird with a single-egg clutch. During 2005-2007, we examined the relationship between body mass and survival of birds breeding under contrasting foraging conditions at two Arctic colonies. We used corticosterone levels of breeding adults as a physiological indicator of the foraging conditions they encountered during each reproductive season. We found that when foraging conditions were relatively poor (as reflected in elevated levels of corticosterone), parents ended the reproductive season with low body mass and suffered increased post-breeding mortality. A positive relationship between body mass and post-breeding survival was found in one study year; light birds incurred higher survival costs than heavy birds. The results of this study suggest that reproducing under poor foraging conditions may affect the post-breeding survival of long-lived little auks. They also have important demographic implications because even a small change in adult survival may have a large effect on populations of long-lived species.

Application of the two-sample doubly labelled water method alters behaviour and affects estimates of energy expenditure in black-legged kittiwakes.

Despite the widespread use of the doubly labelled water (DLW) method in energetic studies of free-ranging animals, effects of the method on study animals are rarely assessed. We studied behavioural effects of two alternative DLW protocols. During two consecutive breeding seasons, 42 parent black-legged kittiwakes received either the commonly used two-sample (TS) or the less invasive single-sample (SS) DLW treatment. A third group served as a non-treated control. We evaluated the effect of treatment with respect to the time birds took to return to their nest after treatment and recaptures, and the nest attendance during DLW measurement periods. We found that TS kittiwakes took on average 20 times longer to return to their nest than SS kittiwakes after initial treatment, and nest attendance was reduced by about 40% relative to control birds. In contrast, nest attendance did not differ between control and SS kittiwakes. Estimates of energy expenditure of SS kittiwakes exceeded those of TS kittiwakes by 15%. This difference was probably caused by TS birds remaining inactive for extended time periods while at sea. Our results demonstrate that the common assumption that the TS DLW method has little impact on the behaviour of study subjects is in some circumstances fallacious. Estimates of energy expenditure derived by the SS approach may thus more accurately reflect unbiased rates of energy expenditure. However, the choice of protocol may be a trade-off between their impact on behaviour, and hence accuracy, and their differences in precision. Adopting procedures that minimize the impact of TS protocols may be useful.

Evidence for an intrinsic energetic ceiling in free-ranging kittiwakes Rissa tridactyla.

1. The rate at which free-living animals can expend energy is limited but the causes of this limitation are not well understood. Theoretically, energy expenditure may be intrinsically limited by physiological properties of the animal constraining its capacity to process energy. Alternatively, the limitation could be set extrinsically by the amount of energy available in the environment or by a fitness trade-off in terms of reduced future survival associated with elevated metabolism. 2. We measured daily energy expenditure (DEE) using the doubly labelled water method in chick-rearing black-legged kittiwakes (Rissa tridactyla) at a study site close to the northern limit of their breeding range over 5 years. We measured breeding success, foraging trip duration and diet composition as proxies of resource availability during these years and estimated the probability of parent kittiwakes to return to the colony in relation to their energy expenditure in order to determine whether kittiwakes adjust their DEE in response to variation in prey availability and whether elevated DEE is associated with a decrease in adult survival. 3. We found that DEE was strikingly similar across all five study years. There was no evidence that energy expenditure was limited by resource availability that varied considerably among study years. Furthermore, there was no evidence of a negative effect of DEE on adult return rate, which does not support the hypothesis of a survival cost connected to elevated energy expenditure. 4. The additional lack of variation in DEE with respect to ambient temperature, brood size or between sexes suggests that kittiwakes at a time of peak energy demands may operate close to an intrinsic metabolic ceiling independent of extrinsic factors.

Long-term survival effect of corticosterone manipulation in Black-legged kittiwakes.

The secretion of corticosterone in response to stress is thought to be an adaptive mechanism, which promotes immediate survival at the expense of current reproduction. However, at the individual level, the hypothesis of a corticosterone-related survival appears to be complex. In this study, we tested this hypothesis by combining for the first time an experimental manipulation of corticosterone levels and capture-mark-recapture (CMR) models. To do so, we increased corticosterone levels of chick-rearing Black-legged kittiwakes (Rissa tridactyla) via subcutaneous implants. Then, we monitored the long-term survival of kittiwakes over the 2 consecutive years. Corticosterone-implanted birds showed a significantly lower apparent annual survival than sham-implanted ones (46.9% vs 77.8%). This result is supported by the well-known deleterious effects of elevated corticosterone levels on cognitive and immune functions. Alternately and in the light of recent studies, our experimental manipulation may have down-regulated the endogenous secretion of corticosterone through a prolonged negative feedback. If so, the corticosterone-implanted kittiwakes may have failed to trigger an appropriate stress response during subsequent life-threatening perturbations, hence being unable to adjust their behavior and physiology toward immediate survival. This study highlights the complex long-term consequences of corticosterone manipulation on fitness in free-living vertebrates.

Black-legged kittiwakes as messengers of Atlantification in the Arctic.

Climate warming is rapidly altering marine ecosystems towards a more temperate state on the European side of the Arctic. However, this "Atlantification" has rarely been confirmed, as long-term datasets on Arctic marine organisms are scarce. We present a 19-year time series (1982-2016) of diet samples from black-legged kittiwakes as an indicator of the changes in a high Arctic marine ecosystem (Kongsfjorden, Svalbard). Our results highlight a shift from Arctic prey dominance until 2006 to a more mixed diet with high contribution of Atlantic fishes. Capelin, an Atlantic species, dominated the diet composition in 2007, marking a shift in the food web. The occurrence of polar cod, a key Arctic fish species, positively correlated with sea ice index, whereas Atlantic species demonstrated the opposite correlation indicating that the diet shift was likely connected with recent climate warming. Kittiwakes, which gather available fish and zooplankton near the sea surface to feed their chicks, can act as messengers of ecosystem change. Changes in their diet reveal that the Kongsfjord system has drifted in an Atlantic direction over the last decade.

Climate warming decreases the survival of the little auk (Alle alle), a high Arctic avian predator.

Delayed maturity, low fecundity, and high adult survival are traits typical for species with a long-life expectancy. For such species, even a small change in adult survival can strongly affect the population dynamics and viability. We examined the effects of both regional and local climatic variability on adult survival of the little auk, a long-lived and numerous Arctic seabird species. We conducted a mark-resighting study for a period of 8 years (2006-2013) simultaneously at three little auk breeding sites that are influenced by the West Spitsbergen Current, which is the main carrier of warm, Atlantic water into the Arctic. We found that the survival of adult little auks was negatively correlated with both the North Atlantic Oscillation (NAO) index and local summer sea surface temperature (SST), with a time lag of 2 and 1 year, respectively. The effects of NAO and SST were likely mediated through a change in food quality and/or availability: (1) reproduction, growth, and development of Arctic Calanus copepods, the main prey of little auks, are negatively influenced by a reduction in sea ice, reduced ice algal production, and an earlier but shorter lasting spring bloom, all of which result from an increased NAO; (2) a high sea surface temperature shortens the reproductive period of Arctic Calanus, decreasing the number of eggs produced. A synchronous variation in survival rates at the different colonies indicates that climatic forcing was similar throughout the study area. Our findings suggest that a predicted warmer climate in the Arctic will negatively affect the population dynamics of the little auk, a high Arctic avian predator.

Effects of food availability on yolk androgen deposition in the black-legged kittiwake (Rissa tridactyla), a seabird with facultative brood reduction.

In birds with facultative brood reduction, survival of the junior chick is thought to be regulated primarily by food availability. In black-legged kittiwakes (Rissa tridactyla) where parents and chicks are provided with unlimited access to supplemental food during the breeding season, brood reduction still occurs and varies interannually. Survival of the junior chick is therefore affected by factors in addition to the amount of food directly available to them. Maternally deposited yolk androgens affect competitive dynamics within a brood, and may be one of the mechanisms by which mothers mediate brood reduction in response to a suite of environmental and physiological cues. The goal of this study was to determine whether food supplementation during the pre-lay period affected patterns of yolk androgen deposition in free-living kittiwakes in two years (2003 and 2004) that varied in natural food availability. Chick survival was measured concurrently in other nests where eggs were not collected. In both years, supplemental feeding increased female investment in eggs by increasing egg mass. First-laid ("A") eggs were heavier but contained less testosterone and androstenedione than second-laid ("B") eggs across years and treatments. Yolk testosterone was higher in 2003 (the year with higher B chick survival) across treatments. The difference in yolk testosterone levels between eggs within a clutch varied among years and treatments such that it was relatively small when B chick experienced the lowest and the highest survival probabilities, and increased with intermediate B chick survival probabilities. The magnitude of testosterone asymmetry in a clutch may allow females to optimize fitness by either predisposing a brood for reduction or facilitating survival of younger chicks.

Thyroid hormones correlate with basal metabolic rate but not field metabolic rate in a wild bird species.

Thyroid hormones (TH) are known to stimulate in vitro oxygen consumption of tissues in mammals and birds. Hence, in many laboratory studies a positive relationship between TH concentrations and basal metabolic rate (BMR) has been demonstrated whereas evidence from species in the wild is scarce. Even though basal and field metabolic rates (FMR) are often thought to be intrinsically linked it is still unknown whether a relationship between TH and FMR exists. Here we determine the relationship between the primary thyroid hormone triiodothyronine (T3) with both BMR and FMR in a wild bird species, the black-legged kittiwake (Rissa tridactyla). As predicted we found a strong and positive relationship between plasma concentrations of T3 and both BMR and mass-independent BMR with coefficients of determination ranging from 0.36 to 0.60. In contrast there was no association of T3 levels with either whole-body or mass-independent FMR (R(2) =0.06 and 0.02, respectively). In accordance with in vitro studies our data suggests that TH play an important role in modulating BMR and may serve as a proxy for basal metabolism in wild birds. However, the lack of a relationship between TH and FMR indicates that levels of physical activity in kittiwakes are largely independent of TH concentrations and support recent studies that cast doubt on a direct linkage between BMR and FMR.

Thyroid hormones correlate with resting metabolic rate, not daily energy expenditure, in two charadriiform seabirds.

Thyroid hormones affect in vitro metabolic intensity, increase basal metabolic rate (BMR) in the lab, and are sometimes correlated with basal and/or resting metabolic rate (RMR) in a field environment. Given the difficulty of measuring metabolic rate in the field-and the likelihood that capture and long-term restraint necessary to measure metabolic rate in the field jeopardizes other measurements-we examined the possibility that circulating thyroid hormone levels were correlated with RMR in two free-ranging bird species with high levels of energy expenditure (the black-legged kittiwake, Rissa tridactyla, and thick-billed murre, Uria lomvia). Because BMR and daily energy expenditure (DEE) are purported to be linked, we also tested for a correlation between thyroid hormones and DEE. We examined the relationships between free and bound levels of the thyroid hormones thyroxine (T4) and triiodothyronine (T3) with DEE and with 4-hour long measurements of post-absorptive and thermoneutral resting metabolism (resting metabolic rate; RMR). RMR but not DEE increased with T3 in both species; both metabolic rates were independent of T4. T3 and T4 were not correlated with one another. DEE correlated with body mass in kittiwakes but not in murres, presumably owing to the larger coefficient of variation in body mass during chick rearing for the more sexually dimorphic kittiwakes. We suggest T3 provides a good proxy for resting metabolism but not DEE in these seabird species.