Steller sea lion survivors: a retrospective on the impact of alternative research methods on an endangered species

Thesis (M.S.) University of Alaska Fairbanks, 2015Two novel research approaches were developed to facilitate access to wild juvenile Steller sea lions. First, the Transient Juvenile Steller sea lion Project (TJ) facilitated numerous studies of physiology, behavior, and nutrition through temporary captivity (branded TJs, n=45) over the past decade. As a complement, a control group was sampled and released during capture events (FRs, n=35). Second, the Life History Tag (LHX) project was implemented within the TJ project to implant individuals (LHX-1, n=35) with internal transmitters to detect potential causes of mortality. Our goal was to evaluate the potential for long-term impacts of these two research programs on study individuals (Chapter 1) as well as identify potential metrics of survival for use in field efforts (Chapter 2). The first chapter used open-population Cormack-Jolly-Seber (CJS) mark-recapture models to project survival from resights of branded individuals in combination with demographic covariates in program MARK. TJ and FR groups were compared to identify the potential effect of temporary captivity on survival, while LHX-1 and non-implants were compared to examine a tagging effect on survival. Overall, our results mirror previous efforts to characterize survival in sea lions and indicate minimal long-term effects on mortality from research efforts, higher survival in females than males, and increasing survival rate with age. For the second chapter, a three-tiered approach to the decade of archived physiological data attempted to build links to survival in TJs through similar CJS modeling techniques. The first two levels looked at survival in relation to observed responses of handling stress through six a priori principle blood parameters measured at entry and exit. In addition, several condition indices were also incorporated into mark-recapture models, but separately considered when measured at entry and exit due to sampling inconsistencies. The third level evaluated the efficacy of single-point sampling to project similar trends for field use. Change in mass (kg) and white blood cell count (WBC, m/mm3) had the most support in predicting survival. Mass gains over captivity and slight increases in WBC resulted in a higher averaged survival rate. Minor support was identified for exit mass and entry WBC. A higher exit mass predicted a higher survival rate, while a higher entry WBC predicted a lower survival rate and may demonstrate the efficacy of single-point sampling as a management tool

Quantifying individual variation in fine-scale time and energy trade-offs in breeding grey seals: How do differing behavioural types solve these trade-offs?

Lactation is one of the most energetically demanding periods of any female mammal’s life history, where individuals strike a balance with limited resources between their daily activity and towards the growth of their offspring, while still maintaining enough energy stores to maintain themselves in the process. Capital breeding systems mean that females must sustain themselves and their offspring while fasting exclusively on energy reserves acquired beforehand. Female phocids as a result must deal with pressures of a brief terrestrial existence where trade-offs in time, behaviour, energy, and responsiveness to the environment can have tangible consequences to short-term fitness and health. The aim of this thesis was to use new techniques, specifically animal-borne accelerometers and heart rate monitors, to track behaviour and physiology and assess the inherent trade-offs therein through the core duration of lactation in a capital breeding phocid, the grey seal (Halichoerus grypus). Female grey seals were equipped with biologging devices on the Isle of May over three consecutive breeding seasons. Using accelerometry and heart rate techniques, I aimed (1) to remotely classify behaviour using machine learning techniques, (2) to assess trade-offs in time-activity for the duration of lactation, (3) to build a holistic picture of energy allocation within the species, and (4) to develop new methods for tracking heart rate and breathing for terrestrial mammals using grey seals as a model. I also assessed the effect that consistent individual variability in behaviour, stress-coping styles, may have on the methods developed here and how they may drive behaviour and energy trade-offs over time. Accelerometers presented a useful way to remotely track several key behaviours, accurately classifying the core static behaviours over lactation. Consistent individual differences in stress-coping styles, as determined from measures of heart rate variability, modulated almost every aspect of behaviour and physiology measured in this study. More specifically, consistent trade-offs were identified for grey seal mothers between balancing time spent in a state of rest against remaining vigilant across multiple contexts, but also that these individual differences drove how individuals manage and expend that energy, ultimately resulting in differences in short-term fitness outcomes. Effort towards nursing, however, appeared to be largely fixed. Individual differences in energy management also appear to result in different levels of plasticity to environmental pressures, suggesting that future ambient conditions may not be suitable for breeding seals. This thesis also successfully detected breathing rates on land, revealing new evidence as to the energy saving and water conservation benefits of regularly engaging in periods of breath-hold while at rest. Overall, this thesis has provided new tools for exploring behaviour and physiology, and the inherent trade-offs therein, with minimal disturbance to lactating phocid seals. These differences, while minute in the scope of evolutionary constraints, may be among the most important drivers for the success and survival of populations in the face of greater environmental variability as the climate continues to change

Assessing the utility and limitations of accelerometers and machine learning approaches in classifying behaviour during lactation in a phocid seal

Background Classifying behaviour with animal-borne accelerometers is quickly becoming a popular tool for remotely observing behavioural states in a variety of species. Most accelerometry work in pinnipeds has focused on classifying behaviour at sea often quantifying behavioural trade-offs associated with foraging and diving in income breeders. Very little work to date has been done to resolve behaviour during the critical period of lactation in a capital breeder. Capital breeding phocids possess finite reserves that they must allocate appropriately to maintain themselves and their new offspring during their brief nursing period. Within this short time, fine-scale behavioural trade-offs can have significant fitness consequences for mother and offspring and must be carefully managed. Here, we present a case study in extracting and classifying lactation behaviours in a wild, breeding pinniped, the grey seal (Halichoerus grypus). Results Using random forest models, we were able to resolve 4 behavioural states that constitute the majority of a female grey seals’ activity budget during lactation. Resting, alert, nursing, and a form of pup interaction were extracted and classified reliably. For the first time, we quantified the potential confounding variance associated with individual differences in a wild context as well as differences due to sampling location in a largely inactive model species. Conclusions At this stage, the majority of a female grey seal’s activity budget was classified well using accelerometers, but some rare and context-dependent behaviours were not well captured. While we did find significant variation between individuals in behavioural mechanics, individuals did not differ significantly within themselves; inter-individual variability should be an important consideration in future efforts. These methods can be extended to other efforts to study grey seals and other pinnipeds who exhibit a capital breeding system. Using accelerometers to classify behaviour during lactation allows for fine-scale assessments of time and energy trade-offs for species with fixed stores

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

The Effect of Novel Research Activities on Long-term Survival of Temporarily Captive Steller Sea Lions (<i>Eumetopias jubatus</i>)

<div><p>Two novel research approaches were developed to facilitate controlled access to, and long-term monitoring of, juvenile Steller sea lions for periods longer than typically afforded by traditional fieldwork. The Transient Juvenile Steller sea lion Project at the Alaska SeaLife Center facilitated nutritional, physiological, and behavioral studies on the platform of temporary captivity. Temporarily captive sea lions (TJs, <i>n</i> = 35) were studied, and were intraperitoneally implanted with Life History Transmitters (LHX tags) to determine causes of mortality post-release. Our goal was to evaluate the potential for long-term impacts of temporary captivity and telemetry implants on the survival of study individuals. A simple open-population Cormack-Jolly-Seber mark-recapture model was built in program MARK, incorporating resightings of uniquely branded study individuals gathered by several contributing institutions. <i>A priori</i> models were developed to weigh the evidence of effects of experimental treatment on survival with covariates of sex, age, capture age, cohort, and age class. We compared survival of experimental treatment to a control group of <i>n</i> = 27 free-ranging animals (FRs) that were sampled during capture events and immediately released. Sex has previously been show to differentially affect juvenile survival in Steller sea lions. Therefore, sex was included in all models to account for unbalanced sex ratios within the experimental group. Considerable support was identified for the effects of sex, accounting for over 71% of total weight for all <i>a priori</i> models with delta AICc <5, and over 91% of model weight after removal of pretending variables. Overall, most support was found for the most parsimonious model based on sex and excluding experimental treatment. Models including experimental treatment were not supported after <i>post-hoc</i> considerations of model selection criteria. However, given the limited sample size, alternate models including effects of experimental treatments remain possible and effects may yet become apparent in larger sample sizes.</p></div

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

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

Final model results for the apparent survival of juvenile Steller sea lions (<i>Eumetopias jubatus</i>).

<p>Final model results for the apparent survival of juvenile Steller sea lions (<i>Eumetopias jubatus</i>).</p

Resighting probabilities for temporarily captive juvenile Steller sea lions (<i>Eumetopias jubatus</i>).

<p>Resighting probabilities for temporarily captive juvenile Steller sea lions (<i>Eumetopias jubatus</i>).</p

Model-averaged apparent survival rates from top Cormack-Jolly-Seber models predicting long-term survival in juvenile Steller sea lions (<i>Eumetopias jubatus</i>).

<p>Model-averaged apparent survival rates from top Cormack-Jolly-Seber models predicting long-term survival in juvenile Steller sea lions (<i>Eumetopias jubatus</i>).</p