Quantifying energetic and fitness consequences of seasonal heterothermy in an Arctic ungulate

Desforges, Jean‐Pierre; Beest, Floris M. van; Marques, Gonçalo M.; Pedersen, Stine Højlund; Beumer, Larissa T.; Chimienti, Marianna; Schmidt, Niels Martin

doi:10.1002/ece3.7049

Cited by 8 publications

(8 citation statements)

References 60 publications

(135 reference statements)

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Section: Discussionsupporting

confidence: 76%

“…The greatest change to FE was induced by having a high T sc , which is likely an effect of the exponential relationship between T sc and DEE. Similar results have been demonstrated for musk oxen, using a process-based modelling approach, in that lower body temperatures led to reductions in the rate of body reserve depletion and to increased fitness (Desforges et al, 2021). Furthermore, Desforges et al (2021) found that initial body condition was important for determining the benefit of reducing body temperature-the greater initial body condition, the lower the benefit of reduced body temperature for overwinter survival.…”

Section: Discussionsupporting

confidence: 65%

“…Furthermore, Desforges et al. (2021) found that initial body condition was important for determining the benefit of reducing body temperature—the greater initial body condition, the lower the benefit of reduced body temperature for overwinter survival. Although we did not find any major differences in the effect of adjusting activity or T sc between individuals of different body conditions, our results do demonstrate a general benefit of combined behavioural and physiological adjustments to conserve energy in response to food scarcity.…”

Section: Discussionmentioning

confidence: 99%

“…Reductions in locomotor activity (Arnold et al., 2018), decreased endogenous heat production and an increased tolerance towards low peripheral body temperatures may further facilitate the seasonal drop in energy budgets (Arnold, 2020; Trondrud, Pigeon, Albon, et al., 2021). Individual and temporal variations in energy expenditure may therefore play an additional explanatory role in determining FE within a species (Desforges et al., 2021). Understanding the relative influence of environmental and individual variation on metabolic phenotypes and the capacity of free‐living animals to withstand food scarcity can provide potentially novel insights into the role of FE as a driver of natural selection.…”

Section: Introductionmentioning

confidence: 99%

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Fat storage influences fasting endurance more than body size in an ungulate

et al. 2021

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The fasting endurance hypothesis (FEH) predicts strong selection for large body size in mammals living in environments where food supply is interrupted over prolonged periods of time. The Arctic is a highly seasonal and food‐restricted environment, but contrary to predictions from the FEH, empirical evidence shows that Arctic mammals are often smaller than their temperate conspecifics. Intraspecific studies integrating physiology and behaviour of different‐sized individuals may shed light on this paradox. We tested the FEH in free‐living Svalbard reindeer Rangifer tarandus platyrhynchus. We measured daily energy expenditure (DEE), subcutaneous body temperature (Tsc) and activity levels during the late winter in 14 adult females with body masses ranging from 46.3 to 57.8 kg. Winter energy expenditure (WEE) and fasting endurance (FE) were modelled dynamically by combining these data with body composition measurements of culled individuals at the onset of winter (14 years, n = 140) and variation in activity level throughout winter (10 years, n = 70). Mean DEE was 6.3 ± 0.7 MJ/day. Lean mass, Tsc and activity had significantly positive effects on DEE. Across all 140 individuals, mean FE was 85 ± 17 days (range 48–137 days). In contrast to the predictions of the FEH, the dominant factor affecting FE was initial fat mass, while body mass and FE were not correlated. Furthermore, lean mass and fat mass were not correlated. FE was on average 80% (45 days) longer in fat than lean individuals of the same size. Reducing activity levels by ~16% or Tsc by ~5% increased FE by 7% and 4% respectively. Our results fail to support the FEH. Rather, we demonstrate that (a) the size of fat reserves can be independent of lean mass and body size within a species, (b) ecological and environmental variation influence FE via their effects on body composition and (c) physiological and behavioural adjustments can improve FE within individuals. Altogether, our results suggest that there is a selection in Svalbard reindeer to accumulate body fat, rather than to grow structurally large. A free Plain Language Summary can be found within the Supporting Information of this article.

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Section: Discussionsupporting

confidence: 76%

Section: Discussionsupporting

confidence: 65%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Fat storage influences fasting endurance more than body size in an ungulate

et al. 2021

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“…Seasonality in muskoxen traits as they relate to their environment are known to occur and could have important implications for daily energy budgets. Muskoxen and other northern ungulates have been reported to reduce winter metabolic rates and body temperature, likely as an energy saving mechanism (Arnold et al, 2018; Desforges et al, 2020; Lawler & White, 1997; Schmidt et al, 2020). Our model does predict seasonal fluctuations in metabolic rates (Desforges et al, 2019), but the mechanism is linked to reduced feeding rates in winter and not endogenous suppression of basal metabolism.…”

Section: Discussionmentioning

confidence: 99%

Environment and physiology shape Arctic ungulate population dynamics

Desforges

Marques²,

Beumer

et al. 2021

Global Change Biology

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Species conservation in a rapidly changing world requires an improved understanding of how individuals and populations respond to changes in their environment across temporal scales. Increased warming in the Arctic puts this region at particular risk for rapid environmental change, with potentially devastating impacts on resident populations. Here, we make use of a parameterized full life cycle, individual‐based energy budget model for wild muskoxen, coupling year‐round environmental data with detailed ontogenic metabolic physiology. We show how winter food accessibility, summer food availability, and density dependence drive seasonal dynamics of energy storage and thus life history and population dynamics. Winter forage accessibility defined by snow depth, more than summer forage availability, was the primary determinant of muskox population dynamics through impacts on calf recruitment and longer term carryover effects of maternal investment. Simulations of various seasonal snow depth and plant biomass and quality profiles revealed that timing of and improved/limited winter forage accessibility had marked influence on calf recruitment (±10–80%). Impacts on recruitment were the cumulative result of condition‐driven reproductive performance at multiple time points across the reproductive period (ovulation to calf weaning) as a trade‐off between survival and reproduction. Seasonal and generational condition effects of snow‐rich winters interacted with age structure and density to cause pronounced long‐term consequences on population growth and structure, with predicted population recovery times from even moderate disturbances of 10 years or more. Our results show how alteration in winter forage accessibility, mediated by snow depth, impacts the dynamics of northern herbivore populations. Further, we present here a mechanistic and state‐based model framework to assess future scenarios of environmental change, such as increased or decreased snowfall or plant biomass and quality to impact winter and summer forage availability across the Arctic.

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Sequential analysis of δ¹⁵N in guard hair suggests late gestation is the most critical period for muskox calf recruitment

Schmidt

Michelsen

Hansen

et al. 2023

Rapid Comm Mass Spectrometry

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Rationale Analysis of stable isotopes in tissue and excreta may provide information about animal diets and their nutritional state. As body condition may have a major influence on reproduction, linking stable isotope values to animal demographic rates may help unravel the drivers behind animal population dynamics. Methods We performed sequential analysis of δ15N values in guard hair from 21 muskoxen (Ovibos moschatus) from Zackenberg in high arctic Greenland. We were able to reconstruct the dietary history for the population over a 5‐year period with contrasting environmental conditions. We examined the linkage between guard hair δ15N values in 12 three‐month periods and muskox calf recruitment to detect critical periods for muskox reproduction. Finally, we conducted similar analyses of the correlation between environmental conditions (snow depth and air temperature) and calf recruitment. Results δ15N values exhibited a clear seasonal pattern with high levels in summer and low levels in winter. However, large inter‐annual variation was found in winter values, suggesting varying levels of catabolism depending on snow conditions. In particular δ15N values during January–March were linked to muskox recruitment rates, with higher values coinciding with lower calf recruitment. δ15N values were a better predictor of muskox recruitment rates than environmental conditions. Conclusions Although environmental conditions may ultimately determine the dietary δ15N signal in muskox guard hairs, muskox calf recruitment was more strongly correlated with δ15N values than ambient snow and temperature. The period January–March, corresponding to late gestation, appears particularly critical for muskox reproduction.

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Quantifying energetic and fitness consequences of seasonal heterothermy in an Arctic ungulate

Cited by 8 publications

References 60 publications

Fat storage influences fasting endurance more than body size in an ungulate

Fat storage influences fasting endurance more than body size in an ungulate

Environment and physiology shape Arctic ungulate population dynamics

Sequential analysis of δ¹⁵N in guard hair suggests late gestation is the most critical period for muskox calf recruitment

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Quantifying energetic and fitness consequences of seasonal heterothermy in an Arctic ungulate

Cited by 8 publications

References 60 publications

Fat storage influences fasting endurance more than body size in an ungulate

Fat storage influences fasting endurance more than body size in an ungulate

Environment and physiology shape Arctic ungulate population dynamics

Sequential analysis of δ15N in guard hair suggests late gestation is the most critical period for muskox calf recruitment

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Product

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Sequential analysis of δ¹⁵N in guard hair suggests late gestation is the most critical period for muskox calf recruitment