Energetic limits: Defining the bounds and trade-offs of successful energy management in a capital breeder

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.

Keywords: capital breeding; energy management; grey seal; lactation; reproductive success.

FIGURE 1

Heart rate monitor attached to a study female during the 2017 season, pictured here resting with her pup in view. Each heart rate monitor consisted of a central transmitter located dorsally with two electrode leads extending down each flank and attaching behind the fore‐flippers (demonstrated on one side of female pictured here; Photo: CR Shuert)

FIGURE 2

Grey seal energy management over lactation. Across‐individual relationships between daily values of mean‐f_H (daily energy expenditure) against daily values of min‐f_H (daily background energy). Relationships estimated using ordinary least squares (OLS; black line), ranged major axis (RMA; grey line) and standard major axis (SMA; yellow line) regression methods, illustrating varying degrees of regression dilution. OLS regression regularly appears to underestimate the true relationships between these variables since error likely exists in both sets of variables. As a population, a slope of <1 was found for each season of study indicating a compensation energy management strategy

FIGURE 3

Envelopes of energy management. Broken black lines represent the 95th quantile regression (τ = 0.95) fitted for each year of study, representing the limits to energy compensation across the population between years, based on f_H as an energy expenditure proxy. The solid black line represents the line of unity, indicating that daily energy expenditure (daily mean‐f_H, beats/min) is solely contributed to by background energy expenditure (daily min‐f_H, beats/min; as in Figure 2). Coloured lines represent the several females that were study subjects in all 3 years of study. These individuals (unique colours) occupy similar spaces within the envelope of energy management each breeding season as a result of relatively consistent background energy expenditure across seasons

FIGURE 4

Within‐individual energy management strategy as a predictor of normal lactation behaviour. Individuals with slopes relating background (min‐f_H) and daily energy expenditure (mean‐f_H) approaching and surpassing 1 were statistically more likely to end lactation early compared to those with a slope of <1. The logistic regression is represented by the thick black line (with 95% confidence intervals in grey around), as a function of the individual data as black dots. Across‐individual slope (see Table 1) values are included for reference as vertical lines for each season (2015: yellow, 2016: grey, 2017: black)