Abstract

Judicious management of energy can be invaluable for animal survival and reproductive success. Capital breeding mammals typically transfer energy to their young at extremely high rates while undergoing prolonged fasting, making lactation a tremendously energy demanding period. Effective management of the competing demands of the mother's energy needs and those of her offspring is presumably fundamental to maximizing lifetime reproductive success.How does the mother maximize her chances of successfully rearing her pup, by ensuring that both her pup and herself have sufficient energy during this ‘energetic fast’? While energy management models were first discussed in the 1990s, application of this analytical technique is still very much in its infancy. Recent work suggests that a broad range of species exhibits ‘energy compensation’; during periods when they expend more energy on activity, their bodies partially compensate by reducing background (basal) metabolic rate as an adaptation to limit overall energy expenditure. However, the value of energy management models in understanding animal ecology is presently unclear.We investigate whether energy management models provide insights into the breeding strategy of phocid seals. Not only do we expect lactating seals to display energy compensation because of their breeding strategy of high energy transfer while fasting, but we anticipate that mothers exhibiting a lack of energy compensation are less likely to rear offspring successfully.On the Isle of May in Scotland, we collected heart rate data as a proxy for energy expenditure in 52 known individual grey seal (Halichoerus grypus) mothers, repeatedly across 3 years of breeding. We provide evidence that grey seal mothers typically exhibit energy compensation during lactation by downregulating their background metabolic rate to limit daily energy expenditure during periods when other energy costs are relatively high. However, individuals that fail to energy compensate during the lactation period are more likely to end lactation earlier than expected.Our study is the first to demonstrate the importance of energy compensation to an animal's reproductive expenditure. Moreover, our multi‐seasonal data indicate that environmental stressors may reduce the capacity of some individuals to follow the energy compensation strategy.

Highlights

  • Lactation is an energetically demanding period for mammals

  • The demands of lactation in phocid seals typically result in a considerable increase in basal metabolic rate to well above that estimated from allometric equations (McLean & Speakman, 1999; Mellish, Iverson, & Bowen, 2000; Schweigert, 1993; Sparling, Speakman, & Fedak, 2006; Tedman & Green, 1987)

  • In terms of energy management, we might expect fasting phocid seal mothers to fit the energy compensation model, balancing energy spent on background processes, including milk production, against energy spent on activity and other auxiliary processes, in order to constrain daily energy expenditure (Mellish et al, 2000)

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Summary

| INTRODUCTION

Lactation is an energetically demanding period for mammals. Females must balance how they deploy their energy resources between maximising the relative amount of energy passed to their altricial offspring while ensuring they themselves stay alive and healthy. Some evidence suggests that daily energy expenditure is constrained, even during energetically demanding periods, and as a result, individuals tradeoff auxiliary and background costs in order to maintain a cap on daily energy expenditures over time This is known as ‘compensation energy management’ (Careau & Garland Jr., 2012; Careau et al, 2008; Halsey et al, 2019; Pontzer, 2015; Pontzer et al, 2016). In terms of energy management, we might expect fasting phocid seal mothers to fit the energy compensation model, balancing energy spent on background processes, including milk production, against energy spent on activity and other auxiliary processes, in order to constrain daily energy expenditure (Mellish et al, 2000). See Appendix S1 for more information on the tagging procedures, accelerometers, heart rate monitors and artefact filtering procedures

| MATERIALS AND METHODS
Findings
| DISCUSSION
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