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Durham University

Department of Biosciences

News

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

(16 June 2020)

Mother (right foreground) starts to react as her pup strays too close to a neighbour (left foreground); a ‘normal’, everyday stress for a breeding female grey seal at the Isle of May (Photo: S. Twiss)

Authors: Sean D. Twiss 1*, Courtney R. Shuert 1, Naomi Brannan1+3, Amanda M. Bishop 2, Patrick. P. Pomeroy 4

Sean Twiss: s.d.twiss@durham.ac.uk (orcid.org/0000-0002-1923-8874)

Courtney Shuert: cshuert@gmail.com (orcid.org/0000-0002-3202-4897)

Naomi Brannan: nb@smruhk.com (orcid.org/0000-0002-3939-5017)

Amanda Bishop: amybi@alaskasealife.org (orcid.org/0000-0002-0568-454X)

Patrick Pomeroy: pp6@st-andrews.ac.uk (orcid.org/0000-0003-1603-5630)

1. Department of Biosciences, Durham University, Durham, UK, DH1 3LE

2. Alaska SeaLife Center, P.O. Box 1329, 301 Railway Ave, Seward, AK 99664.

3. SMRU (Hong Kong), University of St Andrews, 1802 One Midtown, 11 Hoi Shing Road, Hong Kong Special Administrative Region

4. Sea Mammal Research Unit, University of St. Andrews, St. Andrews, UK, KY16 8LB

Twiss group research theme: Integrating physiology, behaviour and ecology to understand the causes and consequences of individual differences in stress reactivity in wild grey seals (Halichoerus grypus).

Background: Within animal populations individuals differ in their ability to cope with stress. Most wild animal populations are subject to increasing anthropogenic stressors. Even non-consumptive activities, such as the rapidly expanding ecotourism industry, can add stressors to animals. Quantitatively assessing how individual animals react to, and cope with, stress is critical in determining ‘acceptable’ levels of disturbance in situations where human-wildlife interactions are inevitable. However, behavioural measures can be misleading or difficult to interpret in terms of how stressed an individual actually is, for example, is an individual that is totally stationary at rest, or literally ‘scared stiff’? One way around this is to use physiological measures to provide evidence of when stress becomes distress, but gaining such measures, especially in wild, free ranging animals can be difficult!

Our previous work has shown that adult female grey seals exhibit consistent individual differences in behaviour (behavioural types or ‘personalities’) during the breeding season, suggesting that some mothers showing high levels of responsiveness to stressors while others show little response relative to normal, undisturbed behaviour. We wanted to investigate these behavioural differences more thoroughly by looking for a physiological indicator of an individuals’ tendency to react to, or ignore, potentially stressful stimuli in their natural environment. 

In this new paper we investigate the physiological underpinnings of the behavioural types we had previously observed. We achieved this by the attaching heart rate data-loggers to individually identified seals during the breeding season to identify individual differences in stress-coping style. Coping-styles are individually consistent suites of behavioural and physiological traits that dictate how individuals react to stimuli. Physiological and consequently behavioural flexibility is a key component of coping-styles, with proactive individuals exhibiting limited flexibility compared to reactive individuals. Coping-style can be measured using the physiological parameter of resting heart-rate variability (rHRV); the amount of variation in the time between successive heart beats that an individual exhibits while at rest and unstressed. Low rHRV indicates proactive individuals, high rHRV indicates reactive individuals. Over five successive breeding seasons we measured rHRV of 57 grey seal mothers during the time when they were raising their pup. 

Mothers showed consistent individual differences in rHRV across years meaning that an individual’s coping style (whether reactive or proactive) is a fixed characteristic of that individual and dictates how she responds to stimuli. We also show that there are subtle differences in the patterns of reproductive performance between reactive and proactive mothers. Although we found no difference in average measures of maternal daily expenditure on her pup (basically how much ‘milk energy’ she manages to transfer to the pup), and the consequent growth rate of her pup, we did find that reactive mothers deviated more from the average daily expenditure, and consequent pup growth rate, compared to proactive mothers. Therefore, within seasons proactive mothers exhibit average expenditures with average outcomes (pup growth rate), while reactive mothers vary significantly more in their expenditures and the resulting short-term fitness outcomes. Essentially, proactive mothers exhibit less flexible expenditure strategies, basically a ‘one size fits all’ approach that they adopt come what may. Reactive mothers however, attempt to match their expenditure to their local social and physical environment depending on what is going on around them; sometimes succeeding and achieving greater than average outcomes, but at other times failing and suffering below average outcomes. Despite their greater variability in reproductive expenditure and outcomes, average success for reactive mothers remains similar to that of proactive mothers, providing a mechanism that can maintain coping-style diversity within natural populations in the wild.

The index we used for individual coping style, resting HRV, is based on a physiological system that underpins behavioural patterns and is highly conserved across vertebrates, and so our findings are applicable to a wide range of other species. It is probable that the behavioural and physiological distinctions between pro- and reactive types represent a fundamental biological pattern that can be observed in many vertebrate species. Coping styles are linked to the degree of behavioural flexibility that individuals are able to express, therefore our results and their implications are particularly pertinent in the context of current rapid environmental change, particularly the increased unpredictability of local weather patterns. Our previous work has shown that grey seal behaviour and success on the breeding colony are very much influenced by weather, with higher temperatures and lower rainfall causing increased stress. However, grey seals are not alone in being subjected to ever more variable and unpredictable conditions during key phases of their lifecycles. Such changing environmental patterns will inevitably impact differentially upon proactive and reactive individuals within populations because of their different approaches to dealing with stress. Therefore, assessing the extent of variation in coping styles within wild populations and their responses to changing environmental conditions is a vital step in understanding species resilience to rapid environmental change.

This exciting study is published here: https://www.nature.com/articles/s41598-020-66597-3

More details are also available on the group's wider research in their blog: https://sealbehaviour.wordpress.com/