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

Abstract

Sea otters (Enhydra lutris) have the highest mass-specific metabolic rate of any marine mammal, which is superimposed on the inherently high costs of reproduction and lactation in adult females. These combined energetic demands have been implicated in the poor body condition and increased mortality of female sea otters nearing the end of lactation along the central California coast. However, the cost of lactation is unknown and currently cannot be directly measured for this marine species in the wild. Here, we quantified the energetic demands of immature sea otters across five developmental stages as a means of assessing the underlying energetic challenges associated with pup rearing that may contribute to poor maternal condition. Activity-specific metabolic rates, daily activity budgets and field metabolic rates (FMR) were determined for each developmental stage. Mean FMR of pre-molt pups was 2.29±0.81 MJ day −1 and increased to 6.16±2.46 and 7.41±3.17 MJ day −1 in post-molt pups and dependent immature animals, respectively. Consequently, daily energy demands of adult females increase 17% by 3 weeks postpartum and continue increasing to 96% above pre-pregnancy levels by the average age of weaning. Our results suggest that the energetics of pup rearing superimposed on small body size, marine living and limited on-board energetic reserves conspire to make female sea otters exceptionally vulnerable to energetic shortfalls. By controlling individual fitness, maternal behavior and pup provisioning strategies, this underlying metabolic challenge appears to be a major factor influencing current population trends in southern sea otters (Enhydra lutris nereis).

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

“…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).…”

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

“…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).…”

“…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).…”

“…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).…”

“…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).…”