Coping styles in capital breeders modulate behavioural trade-offs in time allocation: assessing fine-scale activity budgets in lactating grey seals (Halichoerus grypus) using accelerometry and heart rate variability

Abstract

Balancing time allocation among competing behaviours is an essential part of energy management for all animals. However, trade-offs in time allocation may vary according to the sex of the individual, their age, and even underlying physiology. During reproduction, higher energetic demands and constrained internal resources place greater demand on optimizing these trade-offs insofar that small adjustments in time-activity may lead to substantial effects on an individual's limited energy budget. The most extreme case is found in animals that undergo capital breeding, where individuals fast for the duration of each reproductive episode. We investigated potential underlying drivers of time-activity and describe aspects of trade-offs in time-activity in a wild, capital breeding pinniped, the grey seal Halichoerus grypus, during the lactation period. For the first time, we were able to access full 24-h activity budgets across the core duration of lactation as well as characterize how aspects of stress-coping styles influence time allocation through the use of animal-borne accelerometers and heart rate monitors in situ. We found that there was a distinct trade-off in time activity between time spent Resting and Alert (vigilance). This trade-off varied with the pup's development, date, and maternal stress-coping style as indicated by a measure of heart rate variability, rMSSD. In contrast, time spent Presenting/ Nursing did not vary across the duration of lactation given the variables tested. We suggest that while mothers balance time spent conserving resources (Resting) against time expending energy (Alert), they are also influenced by the inherent physiological drivers of stress-coping styles. Significance statement How animals apportion their time among different behaviours is key to their success. These trade-offs should be finely balanced to avoid unnecessary energy expenditure. Here, we examine how grey seal mothers balance their activity patterns during the short, but energetically demanding, period of pup-rearing. Animal-borne accelerometers provided a uniquely detailed and continuous record of activity during pup-rearing for 38 mothers. We also used heart rate monitors to provide measures of each individual's stress-coping style. We found that mothers balance time Resting against remaining Alert while time Presenting/ Nursing was largely independent of all factors measured. Stress-coping styles were found to drive the balancing and variation of all behaviours. This novel indication that differences in personality-like traits may drive whole activity budgets should be considered when assessing trade-offs in time allocation across a much wider variety of species.

An external telemetry system for recording resting heart rate variability and heart rate in free-ranging large wild mammals

“…We endeavoured to balance data collection on all instrumented seals across the time of day (daylight hours only) and the deployment period. We conducted direct behavioural observations concurrent with logging IBI data [ 38 ].…”

“…In 2015 this was based on concurrent visual behavioural observations. Across the 2016 and 2017 seasons, 29 females were additionally instrumented with tri-axial accelerometers to enable us to identify periods of inactivity without the requirement for direct visual observation [ 38 , 39 ]. Nine of these females were instrumented in both 2016 and 2017.…”

Reactive stress-coping styles show more variable reproductive expenditure and fitness outcomes

“…Each IBI in the remaining traces was matched with a behavioural state derived from in-field video footage recorded concurrently with the IBI data collection. Video footage was decoded by experienced observers (n = 4) post-field season using a focal sampling protocol 78 and a bespoke Visual Basic for Applications Macro in Microsoft Excel to record behaviours based on a pre-established ethogram 37,46,72,79 . In order to define resting HRV, (2020) 10:9550 | https://doi.org/10.1038/s41598-020-66597-3…”

“…= 0.93-0.99; comparison across four independent observers based on 17 behavioural categories, of which Resting is one). Resting behaviour is relatively easy to identify reliably and tends to comprise the bulk of a breeding grey seal's activity budget (typically over 60% 37,45,46,[79][80][81] ). Resting HRV was computed only from 300-second periods where the seal was at rest for ≥95% of the IBIs (and where the remaining time did not involve high energy behaviours such as locomotion or aggression).…”

“…We deployed specially modified heart rate monitors on lactating grey seals (Halichoerus grypus) to assess across individual variation and within individual consistency in resting HRV over successive breeding seasons. Female grey seals have been shown to exhibit consistent individual differences in behaviour 17,36 including in behavioural plasticity reflecting pro-and reactive stress-coping styles 17,37 . As coping styles represent a spectrum of approaches for dealing with life's challenges 34,38,39 , it is likely that they are associated with inter-individual differences in reproductive success.…”