Trade-offs between energy maximization and parental care in a central place forager, the sea otter

Thometz, Nicole M.; Staedler, Michelle M.; Tomoleoni, Joseph A.; Bodkin, James L.; Bentall, Gena B.; Tinker, M. Timothy

doi:10.1093/beheco/arw089

Cited by 33 publications

(40 citation statements)

References 91 publications

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“…While optimal foraging models do not predict a resource switch, the trip duration increase matches predictions of the marginal value theorem for central place foragers, whereby individuals forced to travel/search longer for resources spend longer foraging in selected patches (i.e. increase total foraging trip duration) (Charnov, ; Thometz et al ., ). If increased foraging trip duration of bumble bees occurs when resources are relatively more scarce, then foraging trip duration could serve as a useful proxy for resource abundance in lieu of more painstaking methods of estimating resource abundance.…”

Section: Discussionmentioning

confidence: 97%

“…() (as measured by foraging duration). Similar foraging patterns relative to resource abundance, with shorter trips that take less time when resources are locally abundant, have been observed in other taxa, including mammals (Thometz et al ., ) and birds (Tremblay et al ., ), suggesting that organisms make similar foraging decisions across diverse clades. The behavioural tracking of resource abundance is also evidence of foraging flexibility within bumble bee colonies (Spiesman & Gratton, ).…”

Section: Discussionmentioning

confidence: 99%

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Floral resource pulse decreases bumble bee foraging trip duration in central Wisconsin agroecosystem

Hemberger

Gratton

2018

Ecological Entomology

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Cranberry bloom represents a significant pulse of floral resources – increasing floral area by 400% within a 2‐km landscape, relative to the area of ambient (non‐crop) floral area before bloom. Bumble bee foraging trip duration decreases by 18% in synchrony with cranberry bloom, number of trips increase by 25%, and returning bumble bee foragers carry cranberry pollen almost exclusively. Foraging responses are consistent across individuals, colonies, landscape types (high versus low natural area), and both years of the study.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Floral resource pulse decreases bumble bee foraging trip duration in central Wisconsin agroecosystem

Hemberger

Gratton

2018

Ecological Entomology

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“…For a small marine mammal with limited energy reserves, this prolonged and sustained increase in daily metabolic demands represents an extreme energetic challenge. Despite foraging as much as 50-60% of each day (Esslinger et al, 2014;Thometz et al, 2014;Thometz et al, 2016), females are often in negative energy balance during lactation (Chinn et al, 2016). Further, any delay in independent foraging by pups can greatly increase the energetic burden on adult females during an already energetically taxing period when onboard reserves have been depleted.…”

Section: Resultsmentioning

confidence: 99%

The high cost of reproduction in sea otters necessitates unique physiological adaptations

Thometz

Kendall

Richter

et al. 2016

Journal of Experimental Biology

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Superimposed on inherently high basal metabolic demands, the additional energetic requirements of reproduction can push female sea otters beyond physiological limits. Indeed, the resulting energy imbalance contributes to disproportionately high rates of mortality at the end of lactation in this species. To examine and quantify metabolic changes associated with reproduction, we measured the resting metabolic rate (RMR) of a female sea otter across gestation, lactation and non-reproductive periods. Concurrently, measurements were made on a non-breeding control female. Our results suggest that RMR declines during gestation. Conversely, RMR increases during lactation, reaches a peak at 3-4 months postpartum, and remains elevated until weaning. Combining these direct measurements with published data, we found the cost of pup rearing to be significantly higher than previously estimated. High baseline energy demands and limited energy reserves, combined with significant lactation and pup rearing costs, appear to necessitate metabolic and thermal lability during key reproductive stages.

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“…Similarly, T 3 decreased in resource‐limited otters, suggesting downregulation of metabolism under stronger nutritional constraints. Sea otters under resource limitation stress may face intense prey competition, increased foraging effort (number of dives, dive length, and foraging bout duration), and still experience a negative energy balance (Thometz, Staedler, et al., ; Tinker et al., ). It may be adaptive for individuals under nutrient restriction to decrease thyroid levels to decrease metabolic rate, and thus energy requirements.…”

Section: Discussionmentioning

confidence: 99%

“…Respirometry studies indicate that a mother's daily energy consumption increases 85–110% over nonlactating periods (Thometz, Kendall, Richter, & Williams, ; Thometz, Tinker, Staedler, Mayer, & Williams, ). Despite increasing their foraging effort to as much as 60% of each 24‐h period (Esslinger et al., ; Thometz, Staedler, et al., ), females in resource‐limited environments are often emaciated by the end of lactation. The extreme energetic demands elicited by lactation and pup‐rearing, in addition to exogenous stressors such as resource limitation (Tinker, Doak, & Estes, ; Tinker et al., ), can increase risk of metabolic collapse and mortality, a phenomenon known as “End‐Lactation Syndrome” (ELS) (Chinn et al., ).…”

Section: Introductionmentioning

confidence: 99%

Lactation and resource limitation affect stress responses, thyroid hormones, immune function, and antioxidant capacity of sea otters (Enhydra lutris)

Chinn

Monson

Tinker

et al. 2018

Ecology and Evolution

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Lactation is the most energetically demanding stage of reproduction in female mammals. Increased energetic allocation toward current reproduction may result in fitness costs, although the mechanisms underlying these trade‐offs are not well understood. Trade‐offs during lactation may include reduced energetic allocation to cellular maintenance, immune response, and survival and may be influenced by resource limitation. As the smallest marine mammal, sea otters (Enhydra lutris) have the highest mass‐specific metabolic rate necessitating substantial energetic requirements for survival. To provide the increased energy needed for lactation, female sea otters significantly increase foraging effort, especially during late‐lactation. Caloric insufficiency during lactation is reflected in the high numbers of maternal deaths due to End‐Lactation Syndrome in the California subpopulation. We investigated the effects of lactation and resource limitation on maternal stress responses, metabolic regulation, immune function, and antioxidant capacity in two subspecies of wild sea otters (northern: E. l. nereis and southern: E. l. kenyoni) within the California, Washington, and Alaska subpopulations. Lactation and resource limitation were associated with reduced glucocorticoid responses to acute capture stress. Corticosterone release was lower in lactating otters. Cortisol release was lower under resource limitation and suppression during lactation was only evident under resource limitation. Lactation and resource limitation were associated with alterations in thyroid hormones. Immune responses and total antioxidant capacity were not reduced by lactation or resource limitation. Southern sea otters exhibited higher concentrations of antioxidants, immunoglobulins, and thyroid hormones than northern sea otters. These data provide evidence for allocation trade‐offs during reproduction and in response to nutrient limitation but suggest self‐maintenance of immune function and antioxidant defenses despite energetic constraints. Income‐breeding strategists may be especially vulnerable to the consequences of stress and modulation of thyroid function when food resources are insufficient to support successful reproduction and may come at a cost to survival, and thereby influence population trends.

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Trade-offs between energy maximization and parental care in a central place forager, the sea otter

Cited by 33 publications

References 91 publications

Floral resource pulse decreases bumble bee foraging trip duration in central Wisconsin agroecosystem

Floral resource pulse decreases bumble bee foraging trip duration in central Wisconsin agroecosystem

The high cost of reproduction in sea otters necessitates unique physiological adaptations

Lactation and resource limitation affect stress responses, thyroid hormones, immune function, and antioxidant capacity of sea otters (Enhydra lutris)

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