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

K. Woo, M. Le Vaillant, T. van Nus, and especially A. Wesphal, J. Schultner and I. Dorresteijn, assisted with field work, often under unpleasant conditions. K. Wauthier was instrumental in wrestling the gamma counter into submission. P. Redman and C. Hambly conducted the isotopic analyses. K. Scott and K. Campbell provided the FoxBox. K.H.E. benefited from a Natural Sciences and Engineering Research Council (NSERC) Vanier Scholarship, Association of Canadian Universities for Northern Studies Garfield Weston Northern Studies Award and the Arctic Institute of North America Jennifer Robinson Scholarship. Research support came from Bird Studies Canada/Society of Canadian Ornithologists James Baillie Award, Animal Behavior Society Research Grant, American Ornithologists’ Union Research Grant, Frank Chapman Research Grant, the Waterbird Society Nisbet Grant and NSERC Discovery Grants to J.F.H. and W.G.A. Any use of trade names is for descriptive purposes only and does not imply endorsement by the US Government.Peer reviewedPublisher PD

Consequences of Atlantification on a Zooplanktivorous Arctic Seabird

Global warming, combined with an increasing influence of Atlantic Waters in the European Arctic, are causing a so-called Atlantification of the Arctic. This phenomenon is affecting the plankton biomass and communities with potential consequences for the upper trophic levels. Using long-term data (2005-2020) from a high Arctic zooplanktivorous seabird, the little auk (Alle alle), we tested the hypothesis that the Atlantification affects its diet, body condition and demography. We based our study on data collected in three fjords in West Spitsbergen, Svalbard, characterized by distinct oceanographic conditions. In all three fjords, we found a positive relationship between the inflow of Atlantic Waters and the proportion of Atlantic prey, notably of the copepod Calanus finmarchicus, in the little auk chick diet. A high proportion of Atlantic prey was negatively associated with adult body mass (though the effect size was small) and with chick survival (only in one fjord where chick survival until 21 days was available). We also found a negative and marginally significant effect of the average proportion of Atlantic prey in the chick diet on chick growth rate (data were available for one fjord only). Our results suggest that there are fitness costs for the little auk associated with the Atlantification of West Spitsbergen fjords. These costs seem especially pronounced during the late phase of the chick rearing period, when the energetic needs of the chicks are the highest. Consequently, even if little auks can partly adapt their foraging behaviour to changing environmental conditions, they are negatively affected by the ongoing changes in the Arctic marine ecosystems. These results stress the importance of long-term monitoring data in the Arctic to improve our understanding of the ongoing Atlantification and highlight the relevance of using seabirds as indicators of environmental change.publishedVersio

Behavioral and energetic response of Arctic-breeding seabirds to environmental variability.

Papers number 1, 2 and 3 of the thesis are not available in Munin due to publishers' restrictions. Papers 4 and 5 are manuscripts, and not available in Munin.1. Jorg Welcker, Ann M. A. Harding, Nina J. Karnovsky, Harald Steen, Hallvard Strøm and Geir W. Gabrielsen: "Flexibility in the bimodal foraging strategy of a high Arctic alcid, the little auk Alle alle." Journal of Avian Biology 2009; 40(4): 388-399 (Wiley). Available at http://dx.doi.org/10.1111/j.1600-048X.2008.04620.x 2. Jorg Welcker, Harald Steen, Ann M. A. Harding and Geir W. Gabrielsen: "Sex-specific provisioning behaviour in a monomorphic seabird with a bimodal foraging strategy." Ibis 2009; 151(3): 502-513 (Wiley). Available at http://dx.doi.org/10.1111/j.1474-919X.2009.00931.x 3. Jorg Welcker, Ann M. A. Harding, Alexander S.Kitaysky, John R. Speakman and Geir W. Gabrielsen: "Daily energy expenditure increases in response to low nutritional stress in an Arctic-breeding seabird with no effect on mortality." Functional Ecology 2009; 23(6): 1081-1090 (Wiley). Available at http://dx.doi.org/10.1111/j.1365-2435.2009.01585.x 4. Jorg Welcker, Børge Moe, Claus Bech, Jannik Schultner, John R. Speakmana and Geir W. Gabrielsen: "Evidence for an energetic ceilinf in free-ranging kittiwakes (Rissa tridactyla)". Manuscript 5. Jannic Schultner, Jorg Welcker, John R. Speakman, Erling S. Nordøy and Geir W. Gabrielsen: "Application of the two-sample doubly-lebeled water method alters behavior and affects estimates of energy expenditure in black-legged kittiwakes". ManuscriptKnowledge about the extent to which organisms inhabitating the Arctic are able to adjust to environmental variability is essential in order to predict the impact of future climate change. In this context, the flexibility og two Acrtic-breeding seabirds, the little Auk (Alle alle) and the kittiwake (Rissa tridactyla), in foraging behavior and energy expenditure in response to environmental variability. Analysis of the foraging behavior of little auks revealed the during chick-rearing this species adopts a bimodal foraging strategy in which they alternate single foraging trips of long duration with several trips of short length. This stereotyped pattern was found to be highly flexivle and adjusted to psatial and temporal variation in foraging conditions. However, behavioral modifications led to reduced chick feeding rates and lower reproductive success, indicating the adjustments did not allow birds to fully compensate for costs incurred by unfavorable conditions. Adjustment and limitation of energy expenditure differed remarkably between the two study species. Metabolic rate in little auks was flexible and adjusted in response to variation in food availability. Birds increased energy expenditure when food was abundant. Elevated metabolism was associated with increased chick provisioning, resulting in enhanced chick surival, and increased resource allocation to self-maintenance, associated with higher body mass and a higher return rate of individuals the subsquent season. In contrast, kittiwakes did not adjust their metabolic rate in response to environmental variability. In this species, metabolic rate was similar across five study years despite large variation in foraging conditions. Instead, kittiwakes seemed to operate close to an energetic ceiling which seemed independent of extrinsic factors. This study suggested a limited ability of Arctic seabirds to compensate for large variation to environmental conditions

Fat or lean : Adjustment of endogenous energy stores to predictable and unpredictable changes in allostatic load

The ability to store energy endogenously is an important ecological mechanism that allows animals to buffer predictable and unpredictable variation in allostatic load. The secretion of glucocorticoids, which reflects changes in allostatic load, is suggested to play a major role in the adjustment of endogenous stores to these varying conditions. Although crucially important, the relationship between allostatic load and energy stores remains largely unexplorTwo contrasting hypotheses describe how stores may be adjusted: animals may use low allostatic loads to increase stores to a maximum possible ('fat and fit'), or they can attain a lean physique due to fitness advantages of a low body mass ('lean and fit'). We compiled observational and experimental data available for a long-lived seabird to examine the relationship between glucocorticoids and stored energy at two life history stages (incubation and chick-rearing). Data were collected across multiple years and colonies in the North Pacific, thereby reflecting the wide range of environmental conditions birds' encounter in the marine environment. During experimental manipulations, allostatic load was minimized by supplementing food to free-living birds. We found that the relationship between allostatic load and energy stores was clearly curvilinear at both life history stages. Observational data suggested that energy stores remained relatively stable under low allostatic load and decreased under high loads. Experimental data showed that birds did not maximize energy stores under favourable conditions but maintained energy stores below a physiologically attainable level. Energy stores remained consistently lower during chick-rearing compared to incubation across the wide range of variations in allostatic load suggesting that stage-specific trade-offs limit the accumulation of energy during favourable environmental conditions. Secretion of glucocorticoids did not appear to mediate this shift in energy stores between the life history stages. Overall, results of this study support the 'lean and fit' hypothesis. We conclude that increased energy stores may not necessarily reflect better environmental conditions experienced by individuals or predict their higher fitness. A major advantage of adopting a lean physique when environmental conditions allow may be the avoidance of additional energetic costs for moving a heavy body. In breeding seabirds, this advantage may be more important during chick-rearing. In the focal species, the secretion of glucocorticoids might be involved in regulation of energy stores within a life history stage but does not appear to mediate an adaptive shift in energy stores between the incubating and chick-rearing stages of reproduction

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.publishedVersio

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

Data from: Resting and daily energy expenditures during reproduction are adjusted in opposite directions in free-living birds

1. Reproduction is energetically expensive, and daily energy expenditure (DEE) often peaks during the period of rearing young. The “potentiation” hypothesis predicts that high DEE needs to be sustained by a corresponding up-regulation of metabolic machinery, thus a concomitant increase of the resting metabolic rate (RMR) is expected. Alternatively, the “compensation” hypothesis predicts that DEE and RMR are regulated independently and animals may maintain low RMR to maximize the energy available for reproduction. This might particularly be the case if DEE was limited, e.g. by extrinsic food supply or intrinsic physiological factors. 2. We tested these hypotheses in free-living seabirds by manipulating their energy demands (experimentally reduced or increased brood size) and supplies (providing supplemental food), and simultaneously measuring their DEE and RMR (by the doubly-labeled water method and an indirect hormonal proxy, respectively). 3. In support of the ‘compensation’ hypothesis, metabolic rates were adjusted independently and in opposite directions with an increase of DEE and a decrease of the hormonal proxy for RMR in individuals rearing young compared to birds with removed broods. Energy expenditure of unfed birds with chicks appeared to be limited as experimental brood enlargement did not cause an increase in DEE. Supplemental feeding did not allow DEE to exceed this apparent limitation. 4. We propose that a reduction of the resting metabolism is a strategy to increase allocation of energy to reproduction when DEE is constrained, and that this constraint is unlikely to be related to food supply

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