Abstract

The efficiency with which individuals extract energy from their environment defines their survival and reproductive success, and thus their selective contribution to the population. Individuals that forage more efficiently (i.e., when energy gained exceeds energy expended) are likely to be more successful at raising viable offspring than individuals that forage less efficiently. Our goal was to test this prediction in large long-lived mammals under free-ranging conditions. To do so, we equipped 20 lactating Antarctic fur seals (Arctocephalus gazella) breeding on Kerguelen Island in the Southern Ocean with tags that recorded GPS locations, depth and tri-axial acceleration to determine at-sea behaviours and detailed time-activity budgets during their foraging trips. We also simultaneously measured energy spent at sea using the doubly-labeled water (DLW) method, and estimated the energy acquired while foraging from 1) type and energy content of prey species present in scat remains, and 2) numbers of prey capture attempts determined from head acceleration. Finally, we followed the growth of 36 pups from birth until weaning (of which 20 were the offspring of our 20 tracked mothers), and used the relative differences in body mass of pups at weaning as an index of first year survival and thus the reproductive success of their mothers. Our results show that females with greater foraging efficiencies produced relatively bigger pups at weaning. These mothers achieved greater foraging efficiency by extracting more energy per minute of diving rather than by reducing energy expenditure. This strategy also resulted in the females spending less time diving and less time overall at sea, which allowed them to deliver higher quality milk to their pups, or allowed their pups to suckle more frequently, or both. The linkage we demonstrate between reproductive success and the quality of individuals as foragers provides an individual-based quantitative framework to investigate how changes in the availability and accessibility of prey can affect fitness of animals.

Highlights

  • Optimal Foraging theory assumes that natural selection favours animals that forage more efficiently, with foraging efficiency defined as the ratio of energy gained to energy expended to acquire food [1,2,3]

  • Fitness of an animal in its evolutionary sense should be assessed over its lifetime, but we only looked at the link between foraging efficiency and an index of reproductive success over a single reproduction cycle

  • The quantitative measures of maternal foraging efficiencies and offspring growth rates we found in free-ranging Antarctic fur seals provides empirical support that greater foraging efficiency of individual favors their reproduction success which is partly assumed in the Optimal Foraging theory

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Summary

Introduction

Optimal Foraging theory assumes that natural selection favours animals that forage more efficiently, with foraging efficiency defined as the ratio of energy gained to energy expended to acquire food [1,2,3] This implies that energy gained in excess of maintenance requirements can be allocated to reproduction, survival and growth [4]. Validating the theory in the wild is more complicated because of the difficulty of simultaneously measuring the energy intake and output of free-ranging individuals, as well as their reproductive success This is true for marine mammals that are long-lived and inhabit environments where direct observation of foraging is impossible. There is a need to link reproductive success with measures of foraging efficiency, which would allow predictions to be made about how the individual fitness and population trends of top predators are affected by changes in prey availability and foraging behaviours

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