Divergent migration routes reveal contrasting energy-minimization strategies to deal with differing resource predictability.

BACKGROUND: Seasonal long-distance movements are a common feature in many taxa allowing animals to deal with seasonal habitats and life-history demands. Many species use different strategies to prioritize time- or energy-minimization, sometimes employing stop-over behaviours to offset the physiological burden of the directed movement associated with migratory behaviour. Migratory strategies are often limited by life-history and environmental constraints, but can also be modulated by the predictability of resources en route. While theory on population-wide strategies (e.g. energy-minimization) are well studied, there are increasing evidence for individual-level variation in movement patterns indicative of finer scale differences in migration strategies. METHODS: We aimed to explore sources of individual variation in migration strategies for long-distance migrators using satellite telemetry location data from 41 narwhal spanning a 21-year period. Specifically, we aimed to determine and define the long-distance movement strategies adopted and how environmental variables may modulate these movements. Fine-scale movement behaviours were characterized using move-persistence models, where changes in move-persistence, highlighting autocorrelation in a movement trajectory, were evaluated against potential modulating environmental covariates. Areas of low move-persistence, indicative of area-restricted search-type behaviours, were deemed to indicate evidence of stop-overs along the migratory route. RESULTS: Here, we demonstrate two divergent migratory tactics to maintain a similar overall energy-minimization strategy within a single population of narwhal. Narwhal migrating offshore exhibited more tortuous movement trajectories overall with no evidence of spatially-consistent stop-over locations across individuals. Nearshore migrating narwhal undertook more directed routes, contrasted by spatially-explicit stop-over behaviour in highly-productive fjord and canyon systems along the coast of Baffin Island for periods of several days to several weeks. CONCLUSIONS: Within a single population, divergent migratory tactics can achieve a similar overall energy-minimizing strategy within a species as a response to differing trade-offs between predictable and unpredictable resources. Our methodological approach, which revealed the modulators of fine-scale migratory movements and predicted regional stop-over sites, is widely applicable to a variety of other aquatic and terrestrial species. Quantifying marine migration strategies will be key for adaptive conservation in the face of climate change and ever increasing human pressures.

Linking movement and dive data to prey distribution models: new insights in foraging behaviour and potential pitfalls of movement analyses.

BACKGROUND: Animal movement data are regularly used to infer foraging behaviour and relationships to environmental characteristics, often to help identify critical habitat. To characterize foraging, movement models make a set of assumptions rooted in theory, for example, time spent foraging in an area increases with higher prey density. METHODS: We assessed the validity of these assumptions by associating horizontal movement and diving of satellite-telemetered ringed seals (Pusa hispida)-an opportunistic predator-in Hudson Bay, Canada, to modelled prey data and environmental proxies. RESULTS: Modelled prey biomass data performed better than their environmental proxies (e.g., sea surface temperature) for explaining seal movement; however movement was not related to foraging effort. Counter to theory, seals appeared to forage more in areas with relatively lower prey diversity and biomass, potentially due to reduced foraging efficiency in those areas. CONCLUSIONS: Our study highlights the need to validate movement analyses with prey data to effectively estimate the relationship between prey availability and foraging behaviour.

Decadal migration phenology of a long-lived Arctic icon keeps pace with climate change.

Animals migrate in response to seasonal environments, to reproduce, to benefit from resource pulses, or to avoid fluctuating hazards. Although climate change is predicted to modify migration, only a few studies to date have demonstrated phenological shifts in marine mammals. In the Arctic, marine mammals are considered among the most sensitive to ongoing climate change due to their narrow habitat preferences and long life spans. Longevity may prove an obstacle for species to evolutionarily respond. For species that exhibit high site fidelity and strong associations with migration routes, adjusting the timing of migration is one of the few recourses available to respond to a changing climate. Here, we demonstrate evidence of significant delays in the timing of narwhal autumn migrations with satellite tracking data spanning 21 y from the Canadian Arctic. Measures of migration phenology varied annually and were explained by sex and climate drivers associated with ice conditions, suggesting that narwhals are adopting strategic migration tactics. Male narwhals were found to lead the migration out of the summering areas, while females, potentially with dependent young, departed later. Narwhals are remaining longer in their summer areas at a rate of 10 d per decade, a similar rate to that observed for climate-driven sea ice loss across the region. The consequences of altered space use and timing have yet to be evaluated but will expose individuals to increasing natural changes and anthropogenic activities on the summering areas.

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

Measures of heart rate variability (and heart rate more generally) are providing powerful insights into the physiological drivers of behaviour. Resting heart rate variability (HRV) can be used as an indicator of individual differences in temperament and reactivity to physical and psychological stress. There is increasing interest in deriving such measures from free ranging wild animals, where individuals are exposed to the natural and anthropogenic stressors of life. We describe a robust, externally mounted heart rate monitor for use in wild mammals, deployed here on wild breeding adult female grey seals (Halichoerus grypus), that delivers millisecond precise measures of inter beat intervals (IBIs), allowing computation of resting HRV parameters. Based on Firstbeat™ heart rate belts, our system allows for remote, continuous recording of IBI data from over 30 individuals simultaneously at ranges of up to 200m. We assessed the accuracy of the IBI data provided by the Firstbeat™ system using concurrent IBI data derived from in-field electrocardiogram (ECG) recordings. Bland-Altmann analyses demonstrated high correspondence between the two sets of IBI data, with a mean difference of 0.87±0.16ms. We used generalized additive mixed-effects models to examine the impact of the default Firstbeat™ software artefact correction procedure upon the generation of anomalous data (flats and stairs). Artefact correction and individual activity were major causes of flats and stairs. We used simulations and models to assess the impact of these errors on estimates of resting HRV and to inform criteria for subsampling relatively error free IBI traces. These analyses allowed us to establish stringent filtering procedures to remove traces with excessive numbers of artefacts, including flats and stairs. Even with strict criteria for removing potentially erroneous data, the abundance of data yielded by the Firstbeat™ system provides the potential to extract robust estimates of resting HRV. We discuss the advantages and limitations of our system for applications beyond the study system described here.

Assessing the post-release effects of capture, handling and placement of satellite telemetry devices on narwhal (Monodon monoceros) movement behaviour.

Animal-borne telemetry devices have become a popular and valuable means for studying the cryptic lives of cetaceans. Evaluating the effect of capture, handling and tagging procedures remains largely unassessed across species. Here, we examine the effect of capture, handling and tagging activities on an iconic Arctic cetacean, the narwhal (Monodon monoceros), which has previously been shown to exhibit an extreme response to extended capture and handling. Using accelerometry-derived metrics of behaviour, including activity level, energy expenditure and swimming activity, we quantify the post-release responses and time to recovery of 19 individuals following capture and tagging activities considering the intrinsic covariates of sex and individual size and the extrinsic covariates of handling time and presence of a 'bolt-on' satellite telemetry device. From accelerometer-derived behaviour, most narwhals appeared to return to mean baseline behaviour (recovery) within 24 hours after release, which was supported by longer-term measures of diving data. None of the covariates measured, however, had an effect on the time individuals took to recover following release. Using generalized additive models to describe changes in behaviour over time, we found handling time to be a significant predictor of activity levels, energy expenditure and swimming behaviour following release. Individuals held for the longest period (>40 min) were found to display the largest effect in behaviour immediately following release with respect to swimming behaviour and activity levels. We also found some support for relationships between activity levels, energy expenditure and swimming activity and two other covariates: sex and the attachment of a bolt-on configuration satellite tags. Our results indicate that narwhals recover relatively quickly following capture, handling and tagging procedures, but we suggest that researchers should minimize handling time and further investigation is needed on how to mitigate potential effects of bolt-on satellite tags in these sensitive species.

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

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.

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

Stress-coping styles dictate how individuals react to stimuli and can be measured by the integrative physiological parameter of resting heart-rate variability (HRV); low resting HRV indicating proactive coping styles, while high resting HRV typifies reactive individuals. Over 5 successive breeding seasons we measured resting HRV of 57 lactating grey seals. Mothers showed consistent individual differences in resting HRV across years. We asked whether proactive and reactive mothers differed in their patterns of maternal expenditure and short-term fitness outcomes within seasons, using maternal daily mass loss rate to indicate expenditure, and pup daily mass gain to indicate within season fitness outcomes. We found no difference in average rates of maternal daily mass loss or pup daily mass gain between proactive and reactive mothers. However, reactive mothers deviated more from the sample mean for maternal daily mass and pup daily mass gain than proactive mothers. Thus, while proactive mothers exhibit average expenditure strategies with average outcomes, expenditure varies much more among reactive mothers with more variable outcomes. Overall, however, mean fitness was equal across coping styles, providing a mechanism for maintaining coping style diversity within populations. Variability in reactive mothers' expenditures and success is likely a product of their attempts to match phenotype to prevailing environmental conditions, achieved with varying degrees of success.