Energetic demands of immature sea otters from birth to weaning: implications for maternal costs, reproductive behavior and population-level trends

Thometz, Nicole M.; Tinker, M. Tim; Staedler, Michelle M.; Mayer, Karl A.; Williams, Terrie M.

doi:10.1242/jeb.099739

Cited by 68 publications

(72 citation statements)

References 49 publications

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“…This likely reflects the high metabolic load that lactation imposes on nursing dams, and is consistent with the general observation that lactation is the most energetically demanding period across all mammalian species (Millar 1977;Thometz et al 2014). In contrast, males accumulated body reserves prior to the breeding season, but subsequently lost body mass during the peak mating season (March and April), likely due to territory defence, courtship and lost foraging opportunities (Welbergen 2011).…”

Section: Temporal Variationssupporting

confidence: 78%

Physiological biomarkers of Hendra virus infection in Australian Flying-foxes (Pteropus spp.)

McMichael¹

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Since 1994 when the disease was first described, there have been over 50 Hendra virus incidents involving more than 90 confirmed or possible equine cases, and 7 associated human cases, with case fatality rates approaching 90% and 60%respectively. Epidemiological studies suggest that flying-foxes, in particular the Black flying-fox (Pteropus alecto) and the closely related Spectacled flying-fox (P.conspicillatus) are the primary natural reservoir hosts. This research project investigates a hypothesised causal association between ecological and/or physiological stress and Hendra virus infection in Pteropus species.During a 12-month study of flying-foxes in Southeast Queensland (SEQ), samples were collected from 446 captured wild P. alecto for analysis of 18 hematologic, 22 biochemical and 8 urinary biomarkers, establishing normal reference ranges and temporal changes for this suite of biomarkers. The population demonstrated statistically significant temporal variation in some biomarkers consistent with life cycle events. In Hendra virus RNA-positive animals all biomarker mean values were within established normal ranges, but some were significantly different compared to Hendra virus RNA-negative animals, notably, increased lymphocyte percent, decreased neutrophil percent, decreased plasma triglyceride levels, increased plasma alkaline phosphatase levels and increased urinary protein levels. The study demonstrated that Hendra virus infection in P. alecto was sub-clinical, and that there was no apparent relationship with nutritional stress, reproductive stress or extreme metabolic demand, which would have caused substantial changes to biomarker values. The relationship between increased urinary protein levels, decreased triglyceride levels and Hendra virus infection is of interest, and may support the premise of urinary tract association and physiological demand with Hendra virus infection of P. alecto.In a second study, a method of collection and assay of urinary cortisol to measure physiological stress in roosting flying-foxes was validated. Differences between the four mainland flying-fox species (P. alecto, P. poliocephalus, P. scapulatus, P. conspicillatus) were established through collection of urine samples from a wide geographic range throughout Queensland and New South Wales from single species roosts. Then, over a three-year study, population urinary cortisol and Hendra virus 3 urinary excretion prevalence was measured from a total of 2208 pooled urine samples from mixed species roosts of flying-foxes from two geographically distinct regions, subtropical SEQ and tropical Far North Queensland (FNQ). An autumn elevation in urinary cortisol in the FNQ population was detected, but no significant seasonal fluctuations in Hendra virus excretion prevalence were found. Urinary cortisol was significantly elevated in both autumn and winter in the SEQ population, the latter temporally associated with a significant winter elevation in Hendra virus excretion prevalence. There was also a strong correlation betwe...

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Section: Temporal Variationssupporting

confidence: 78%

Physiological biomarkers of Hendra virus infection in Australian Flying-foxes (Pteropus spp.)

McMichael¹

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“…An open-flow respirometry system designed for aquatic mammals was used to determine VȮ 2 for each individual (Thometz et al, 2014;Williams et al, 2004). Air was pulled through the metabolic dome at 150 l min −1 by a mass flow controller (Flow kit 500H, Sable Systems, Henderson, NV, USA).…”

Section: Metabolic Measurementsmentioning

confidence: 99%

“…Sea otters (Enhydra lutris) are extreme income breeders (Stearns, 1992;Thometz et al, 2014). High baseline energy demands and minimal energy reserves require females to forage throughout lactation to meet their own caloric needs as well as the energy demands of a dependent pup (Kenyon, 1969;Payne and Jameson, 1984;Thometz et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…High baseline energy demands and minimal energy reserves require females to forage throughout lactation to meet their own caloric needs as well as the energy demands of a dependent pup (Kenyon, 1969;Payne and Jameson, 1984;Thometz et al, 2014). Although increasing onboard fat reserves generally improve the body condition of female sea otters over the course of gestation (Chinn et al, 2016), these reserves are minimal in comparison to other marine mammals, which can utilize large energy-rich blubber stores (Costa and Williams, 1999).…”

Section: Introductionmentioning

confidence: 99%

“…Thus, there appears to be a direct link between reproductive costs in this species and population-level trends. The first study to estimate pup rearing costs in sea otters suggested that female energy demands reach twice prepartum levels by the time a pup nears weaning (Thometz et al, 2014); however, this study only examined the metabolic needs of pups and could not account for the energetic cost of milk production. In general, terrestrial mammals exhibit increased resting metabolic rate (RMR) during lactation, although the extent and duration of this increase are highly variable among species (Brockway et al, 1963;Fleming et al, 1981;Garton et al, 1994;Hammond and Diamond, 1992;Harder et al, 1996;Król et al, 2003;Poppitt et al, 1994;Prentice et al, 1989;Spaaij et al, 1994;Speakman and Mcqueenie, 1996;Stephenson and Racey, 1993a,b;Thompson and Nicoll, 1986).…”

Section: Introductionmentioning

confidence: 99%

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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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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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Energetic demands of immature sea otters from birth to weaning: implications for maternal costs, reproductive behavior and population-level trends

Cited by 68 publications

References 49 publications

Physiological biomarkers of Hendra virus infection in Australian Flying-foxes (Pteropus spp.)

Physiological biomarkers of Hendra virus infection in Australian Flying-foxes (Pteropus spp.)

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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