A Summer Heat Wave Reduced Activity, Heart Rate, and Autumn Body Mass in a Cold-Adapted Ungulate.

AbstractHeat waves are becoming more frequent across the globe and may impose severe thermoregulatory challenges for endotherms. Heat stress can induce both behavioral and physiological responses, which may result in energy deficits with potential fitness consequences. We studied the responses of reindeer (Rangifer tarandus tarandus), a cold-adapted ungulate, to a record-breaking heat wave in northern Finland. Activity, heart rate, subcutaneous body temperature, and body mass data were collected for 14 adult females. The post-heat wave autumn body masses were then analyzed against longitudinal body mass records for the herd from 1990 to 2021. With increasing air temperature during the day, reindeer became less active and had reduced heart rate and increased body temperature, reflecting both behavioral and physiological responses to heat stress. Although they increased activity in the late afternoon, they failed to compensate for lost foraging time on the hottest days (daily mean temperature ≥20°C), and total time active was reduced by 9%. After the heat wave, the mean September body mass of herd females (69.7±6.6 kg, n=52) was on average 16.4% ± 4.8% lower than predicted (83.4±6.0 kg). Among focal females, individuals with the lowest levels of activity during the heat wave had the greatest mass loss during summer. We show how heat waves impose a thermoregulatory challenge on endotherms, resulting in mass loss, potentially as a result of the loss of foraging time. While it is well known that environmental conditions affect large herbivore fitness indirectly through decreased forage quality and limited water supply, direct effects of heat may be increasingly common in a warming climate.

Post-weaning survival in kangaroos is high and constant until senescence: Implications for population dynamics.

Large herbivores typically have consistently high prime-aged adult survival and lower, more variable, juvenile, and senescent survival. Many kangaroo populations undergo greater fluctuations in density compared with other large herbivores, but age- and sex-specific survival of kangaroos and their response to environmental variation remain poorly estimated. We used long-term capture-mark-recapture data on 920 individuals to investigate the survival component of eastern grey kangaroo (Macropus giganteus) population dynamics. Forage availability and population density were monitored quarterly and included as predictors of survival in Bayesian Cormack-Jolly-Seber models. Annual survival probabilities were estimated for five age classes: 0 years (juveniles), 1-2 years (subadults), 3-6 years (prime-aged adults), 7-9 years (presenescent adults), and ≥10 years (senescent adults). Survival of juveniles varied widely during our 12-year study, ranging from 0.07 to 0.90 for females and 0.05-0.92 for males. Subadult survival was 0.80-0.93 for females and 0.75-0.85 for males, while that of prime-aged adults was ≥0.94 for females and ≥0.83 for males, despite large fluctuations in forage and density. The survival of presenescent adults spanned 0.86-0.93 for females and 0.60-0.86 for males. Senescent survival was variable, at 0.49-0.90 for females and 0.49-0.80 for males. Male survival was significantly lower than female survival in prime-aged and presenescent adults, but not in other age classes. Although most of the models supported by Watanabe-Akaike Information Criterion selection included at least one environmental covariate, none of these covariates individually had a discernible effect on survival. Temporal variability in overall survival appeared mostly due to changes in the survival of juvenile and senescent kangaroos. Kangaroo survival patterns are similar to those of ungulates, suggesting a strong role of sex-age structure on population dynamics.

Different proxies, different stories? Imperfect correlations and different determinants of fitness in bighorn sheep.

Measuring individual fitness empirically is required to assess selective pressures and predicts evolutionary changes in nature. There is, however, little consensus on how fitness should be empirically estimated. As fitness proxies vary in their underlying assumptions, their relative sensitivity to individual, environmental, and demographic factors may also vary. Here, using a long-term study, we aimed at identifying the determinants of individual fitness in bighorn sheep (Ovis canadensis) using seven fitness proxies. Specifically, we compared four-lifetime fitness proxies: lifetime breeding success, lifetime reproductive success, individual growth rate, individual contribution to population growth, and three multi-generational proxies: number of granddaughters, individual descendance in the next generation, and relative genetic contribution to the next generation. We found that all proxies were positively correlated, but the magnitude of the correlations varied substantially. Longevity was the main determinant of most fitness proxies. Individual fitness calculated over more than one generation was also affected by population density and growth rate. Because they are affected by contrasting factors, our study suggests that different fitness proxies should not be used interchangeably as they may convey different information about selective pressures and lead to divergent evolutionary predictions. Uncovering the mechanisms underlying variation in individual fitness and improving our ability to predict evolutionary change might require the use of several, rather than one, the proxy of individual fitness.

Stress responses to repeated captures in a wild ungulate.

While capture-mark-recapture studies provide essential individual-level data in ecology, repeated captures and handling may impact animal welfare and cause scientific bias. Evaluating the consequences of invasive methodologies should be an integral part of any study involving capture of live animals. We investigated short- and long-term stress responses to repeated captures within a winter on the physiology, behaviour, and reproductive success of female Svalbard reindeer (Rangifer tarandus platyrhynchus). Short-term responses were evaluated using serum concentrations of glucocorticoids and catecholamines during handling, and post-release recovery times in heart rate and activity levels. Repeated captures were associated with an increase in measured catecholamines and glucocorticoids, except cortisone, and delayed recovery in heart rate but not activity. Four months later, in summer, individuals captured repeatedly in winter exhibited a small increase in behavioural response to human disturbance and had a lower probability of being observed with a calf, compared to animals not captured, or captured only once. Our findings imply that single annual capture events have no significant negative consequences for Svalbard reindeer, but repeated captures within a season may impact offspring survival in the same year. Such unanticipated side effects highlight the importance of addressing multiple indicators of animal responses to repeated captures.

Context-dependent fitness costs of reproduction despite stable body mass costs in an Arctic herbivore.

The cost of reproduction on demographic rates is often assumed to operate through changing body condition. Several studies have found that reproduction depresses body mass more if the current conditions are severe, such as high population densities or adverse weather, than under benign environmental conditions. However, few studies have investigated the association between the fitness components and body mass costs of reproduction. Using 25 years of individual-based capture-recapture data from Svalbard reindeer Rangifer tarandus platyrhynchus, we built a novel Bayesian state-space model that jointly estimated interannual change in mass, annual reproductive success and survival, while accounting for incomplete observations. The model allowed us to partition the differential effects of intrinsic and extrinsic factors on both non-reproductive mass change and the body mass cost of reproduction, and to quantify their consequences on demographic rates. Contrary to our expectation, the body mass cost of reproduction (mean = -5.8 kg) varied little between years (CV = 0.08), whereas the between-year variation in body mass changes, that were independent of the previous year's reproductive state, varied substantially (CV = 0.4) in relation to autumn temperature and the amount of rain-on-snow in winter. This body mass loss led to a cost of reproduction on the next reproduction, which was amplified by the same environmental covariates, from a 10% reduction in reproductive success in benign years, to a 50% reduction in harsh years. The reproductive mass loss also resulted in a small reduction in survival. Our results show how demographic costs of reproduction, driven by interannual fluctuations in individual body condition, result from the balance between body mass costs of reproduction and body mass changes that are independent of previous reproductive state. We illustrate how a strong context-dependent fitness cost of reproduction can occur, despite a relatively fixed body mass cost of reproduction. This suggests that female reindeer display a very conservative energy allocation strategy, either aborting their reproductive attempt at an early stage or weaning at a relatively constant cost. Such a strategy might be common in species living in a highly stochastic and food limited environment.

Do Early-Life Conditions Drive Variation in Senescence of Female Bighorn Sheep?

The rate of senescence may vary among individuals of a species according to individual life histories and environmental conditions. According to the principle of allocation, changes in mortality driven by environmental conditions influence how organisms allocate resources among costly functions. In several vertebrates, environmental conditions during early life impose trade-offs in allocation between early reproduction and maintenance. The effects of conditions experienced during early life on senescence, however, remain poorly documented in wild populations. We examined how several early-life environmental conditions affected reproductive and survival senescence in wild bighorn sheep. We found long-term effects of high population density at birth, precipitations during the winter before birth, and temperature during the winter following birth that decreased survival after 7 years of age. High temperature during the first summer and autumn of life and high Pacific decadal oscillation decreased reproductive success at old ages. However, harsh early-life environment did not influence the rate of senescence in either survival or reproduction. Contrary to our expectation, we found no trade-off between reproductive allocation prior to senescence and senescence. Our results do show that early-life environmental conditions are important drivers of later survival and reproductive success and contribute to intra-specific variation in late-life fitness, but not aging patterns. These conditions should therefore be considered when studying the mechanisms of senescence and the determinants of variation in both survival and reproductive senescence at older ages.

Determinants of heart rate in Svalbard reindeer reveal mechanisms of seasonal energy management.

Seasonal energetic challenges may constrain an animal's ability to respond to changing individual and environmental conditions. Here, we investigated variation in heart rate, a well-established proxy for metabolic rate, in Svalbard reindeer (Rangifer tarandus platyrhynchus), a species with strong seasonal changes in foraging and metabolic activity. In 19 adult females, we recorded heart rate, subcutaneous temperature and activity using biologgers. Mean heart rate more than doubled from winter to summer. Typical drivers of energy expenditure, such as reproduction and activity, explained a relatively limited amount of variation (2-6% in winter and 16-24% in summer) compared to seasonality, which explained 75% of annual variation in heart rate. The relationship between heart rate and subcutaneous temperature depended on individual state via body mass, age and reproductive status, and the results suggested that peripheral heterothermy is an important pathway of energy management in both winter and summer. While the seasonal plasticity in energetics makes Svalbard reindeer well-adapted to their highly seasonal environment, intraseasonal constraints on modulation of their heart rate may limit their ability to respond to severe environmental change. This study emphasizes the importance of encompassing individual state and seasonal context when studying energetics in free-living animals. This article is part of the theme issue 'Measuring physiology in free-living animals (Part II)'.

The neglected season: Warmer autumns counteract harsher winters and promote population growth in Arctic reindeer.

Arctic ungulates are experiencing the most rapid climate warming on Earth. While concerns have been raised that more frequent icing events may cause die-offs, and earlier springs may generate a trophic mismatch in phenology, the effects of warming autumns have been largely neglected. We used 25 years of individual-based data from a growing population of wild Svalbard reindeer, to test how warmer autumns enhance population growth. Delayed plant senescence had no effect, but a six-week delay in snow-onset (the observed data range) was estimated to increase late winter body mass by 10%. Because average late winter body mass explains 90% of the variation in population growth rates, such a delay in winter-onset would enable a population growth of r = 0.20, sufficient to counteract all but the most extreme icing events. This study provides novel mechanistic insights into the consequences of climate change for Arctic herbivores, highlighting the positive impact of warming autumns on population viability, offsetting the impacts of harsher winters. Thus, the future for Arctic herbivores facing climate change may be brighter than the prevailing view.

Silver spoon effects are constrained under extreme adult environmental conditions.

Early-life environmental conditions may generate cohort differences in individual fitness, subsequently affecting population growth rates. Three, nonmutually exclusive hypotheses predict the nature of these fitness differences: (1) silver spoon effects, where individuals born in good conditions perform better across the range of adult environments; (2) the "environmental saturation" hypothesis, where fitness differences only occur in intermediate adult environmental conditions; and (3) the "environmental matching" or "predictive adaptive response" (PAR) hypothesis, where fitness is highest when adult environmental conditions match those experienced in early life. We quantified the context-dependent effect of early-life environment on subsequent reproductive success, survival, and population growth rate (λ) of Svalbard reindeer, and explored how well it was explained by the three hypotheses. We found that good early-life conditions increased reproductive success compared to poor early-life conditions, but only when experiencing intermediate adult environmental conditions. This is the first example of what appears to be both "beneficial" and "detrimental environmental saturation" in a natural system. Despite weak early-life effects on survival, cohorts experiencing good early-life conditions contributed to higher population growth rates, when simulating realistic variation in adult environmental conditions. Our results show how the combination of a highly variable environment and biological constraints on fitness components can suppress silver spoon effects at both extremes of the adult environmental gradient.

Antler growth as a cost of reproduction in female reindeer.

The costs of reproduction are important in shaping individual life histories, and hence population dynamics, but the mechanistic pathways of such costs are often unknown. Female reindeer have evolved antlers possibly due to interference competition on winter-feeding grounds. Here, we investigate if variation in antler size explains part of the cost of reproduction in late winter mass of female reindeer. We captured 440 individual Svalbard reindeer a total of 1426 times over 16 years and measured antler size and body mass in late winter, while presence of a 'calf-at-heel' was observed in summer. We found that reproductive females grew smaller antlers and weighed 4.3 kg less than non-reproductive females. Path analyses revealed that 14% of this cost of reproduction in body mass was caused by the reduced antler size. Our study is therefore consistent with the hypothesis that antlers in female Rangifer have evolved due to interference competition and provides evidence for antler growth as a cost of reproduction in females. Antler growth was constrained more by life history events than by variation in the environment, which contrasts markedly with studies on male antlers and horns, and hence increases our understanding of constraints on ornamentation and life history trade-offs.

Biased estimation of trends in cohort effects: the problems with age-period-cohort models in ecology.

Environmental variation can generate life-long similarities among individuals born in the same breeding event, so-called cohort effects. Studies of cohort effects have to account for the potentially confounding effects of current conditions (observation year) and age of individuals. However, estimation of such models is hampered by inherent collinearity, as age is the difference between observation year (period) and cohort year. The difficulties of separating linear trends in any of the three variables in Age-Period-Cohort (APC) models are the subject of ongoing debate in social sciences and medicine but have remained unnoticed in ecology. After reviewing the use of APC models, we investigate the consequences of model specification on the estimation of cohort effects, using both simulated data and empirical data from a long-term individual-based study of reindeer in Svalbard. We demonstrate that APC models are highly sensitive to the model's treatment of age, period and cohort, which may generate spurious temporal trends in cohort effects. Avoiding grouping ages and using environmental covariates believed to be drivers of temporal variation reduces the APC identification problem. Nonetheless, ecologists should use caution, given that the specification issues in APC models may have substantial impacts on estimated effect sizes and therefore conclusions.

Hunting regulation favors slow life histories in a large carnivore.

As an important extrinsic source of mortality, harvest should select for fast reproduction and accelerated life histories. However, if vulnerability to harvest depends upon female reproductive status, patterns of selectivity could diverge and favor alternative reproductive behaviors. Here, using more than 20 years of detailed data on survival and reproduction in a hunted large carnivore population, we show that protecting females with dependent young, a widespread hunting regulation, provides a survival benefit to females providing longer maternal care. This survival gain compensates for the females' reduced reproductive output, especially at high hunting pressure, where the fitness benefit of prolonged periods of maternal care outweighs that of shorter maternal care. Our study shows that hunting regulation can indirectly promote slower life histories by modulating the fitness benefit of maternal care tactics. We provide empirical evidence that harvest regulation can induce artificial selection on female life history traits and affect demographic processes.

Into the wild-WAMBAM goes to Canada.

The sixth Wild Animal Models Bi-Annual Meeting was held in July 2017 in Québec, with 42 participants. This report documents the evolution of questions asked and approaches used in evolutionary quantitative genetic studies of wild populations in recent decades, and how these questions and approaches were represented at the recent meeting. We explore how ideas from previous meetings in this series have developed to their present states, and consider how the format of the meetings may be particularly useful at fostering the rapid development and proliferation of ideas and approaches.

Direct and indirect effects of early-life environment on lifetime fitness of bighorn ewes.

Cohort effects, when a common environment affects long-term performance, can have a major impact on population dynamics. Very few studies of wild animals have obtained the necessary data to study the mechanisms leading to cohort effects. We exploited 42 years of individual-based data on bighorn sheep to test for causal links between birth density, body mass, age at first reproduction (AFR), longevity and lifetime reproductive success (LRS) using path analysis. Specifically, we investigated whether the effect of early-life environment on lifetime fitness was the result of indirect effects through body mass or direct effects of early-life environment on fitness. Additionally, we evaluated whether the effects of early-life environment were dependant on the environment experienced during adulthood. Contrary to expectation, the effect on LRS mediated through body mass was weak compared to the effects found via a delay in AFR, reduced longevity and the direct effect of birth density. Birth density also had an important indirect effect on LRS through reduced longevity, but only when adult density was high. Our results show that the potential long-term consequences of a harsh early-life environment on fitness are likely to be underestimated if investigations are limited to body mass instead of fitness at several life stages, or if the interactions between past and present environment are ignored.

Eco-evolutionary dynamics in a contemporary human population.

Recent studies of the joint dynamics of ecological and evolutionary processes show that changes in genotype or phenotype distributions can affect population, community and ecosystem processes. Such eco-evolutionary dynamics are likely to occur in modern humans and may influence population dynamics. Here, we study contributions to population growth from detailed genealogical records of a contemporary human population. We show that evolutionary changes in women's age at first reproduction can affect population growth: 15.9% of variation in individual contribution to population growth over 108 years is explained by mean age at first reproduction and at least one-third of this variation (6.1%) is attributed to the genetic basis of this trait, which showed an evolutionary response to selection during the period studied. Our study suggests that eco-evolutionary processes have modulated the growth of contemporary human populations.

Fluctuating effects of genetic and plastic changes in body mass on population dynamics in a large herbivore.

Recent studies suggest that evolutionary changes can occur on a contemporary time scale. Hence, evolution can influence ecology and vice-versa. To understand the importance of eco-evolutionary dynamics in population dynamics, we must quantify the relative contribution of ecological and evolutionary changes to population growth and other ecological processes. To date, however, most eco-evolutionary dynamics studies have not partitioned the relative contribution of plastic and evolutionary changes in traits on population, community, and ecosystem processes. Here, we quantify the effects of heritable and non-heritable changes in body mass distribution on survival, recruitment, and population growth in wild bighorn sheep (Ovis canadensis) and compare their importance to the effects of changes in age structure, population density, and weather. We applied a combination of a pedigree-based quantitative genetics model, statistical analyses of demography, and a new statistical decomposition technique, the Geber method, to a long-term data set of bighorn sheep on Ram Mountain (Canada), monitored individually from 1975 to 2012. We show three main results: (1) The relative importance of heritable change in mass, non-heritable change in mass, age structure, density, and climate on population growth rate changed substantially over time. (2) An increase in body mass was accompanied by an increase in population growth through higher survival and recruitment rate. (3) Over the entire study period, changes in the body mass distribution of ewes, mostly through non-heritable changes, affected population growth to a similar extent as changes in age structure or in density. The importance of evolutionary changes was small compared to that of other drivers of changes in population growth but increased with time as evolutionary changes accumulated. Evolutionary changes became increasingly important for population growth as the length of the study period considered increased. Our results highlight the complex ways in which ecological and evolutionary changes can affect population dynamics and illustrate the large potential effect of trait changes on population processes.

Long-term fitness consequences of early environment in a long-lived ungulate.

Cohort effects can be a major source of heterogeneity and play an important role in population dynamics. Silver-spoon effects, when environmental quality at birth improves future performance regardless of the adult environment, can induce strong lagged responses on population growth. Alternatively, the external predictive adaptive response (PAR) hypothesis predicts that organisms will adjust their developmental trajectory and physiology during early life in anticipation of expected adult conditions but has rarely been assessed in wild species. We used over 40 years of detailed individual monitoring of bighorn ewes (Ovis canadensis) to quantify long-term cohort effects on survival and reproduction. We then tested both the silver-spoon and the PAR hypotheses. Cohort effects involved a strong interaction between birth and current environments: reproduction and survival were lowest for ewes that were born and lived at high population densities. This interaction, however, does not support the PAR hypothesis because individuals with matching high-density birth and adult environments had reduced fitness. Instead, individuals born at high density had overall lower lifetime fitness suggesting a silver-spoon effect. Early-life conditions can induce long-term changes in fitness components, and their effects on cohort fitness vary according to adult environment.

Intense selective hunting leads to artificial evolution in horn size.

The potential for selective harvests to induce rapid evolutionary change is an important question for conservation and evolutionary biology, with numerous biological, social and economic implications. We analyze 39 years of phenotypic data on horn size in bighorn sheep (Ovis canadensis) subject to intense trophy hunting for 23 years, after which harvests nearly ceased. Our analyses revealed a significant decline in genetic value for horn length of rams, consistent with an evolutionary response to artificial selection on this trait. The probability that the observed change in male horn length was due solely to drift is 9.9%. Female horn length and male horn base, traits genetically correlated to the trait under selection, showed weak declining trends. There was no temporal trend in genetic value for female horn base circumference, a trait not directly targeted by selective hunting and not genetically correlated with male horn length. The decline in genetic value for male horn length stopped, but was not reversed, when hunting pressure was drastically reduced. Our analysis provides support for the contention that selective hunting led to a reduction in horn length through evolutionary change. It also confirms that after artificial selection stops, recovery through natural selection is slow.

Ecological immunology in a fluctuating environment: an integrative analysis of tree swallow nestling immune defense.

Evolutionary ecologists have long been interested by the link between different immune defenses and fitness. Given the importance of a proper immune defense for survival, it is important to understand how its numerous components are affected by environmental heterogeneity. Previous studies targeting this question have rarely considered more than two immune markers. In this study, we measured seven immune markers (response to phytohemagglutinin (PHA), hemolysis capacity, hemagglutination capacity, plasma bactericidal capacity, percentage of lymphocytes, percentage of heterophils, and percentage of eosinophils) in tree swallow (Tachycineta bicolor) nestlings raised in two types of agro-ecosystems of contrasted quality and over 2 years. First, we assessed the effect of environmental heterogeneity (spatial and temporal) on the strength and direction of correlations between immune measures. Second, we investigated the effect of an immune score integrating information from several immune markers on individual performance (including growth, mass at fledging and parasite burden). Both a multivariate and a pair-wise approach showed variation in relationships between immune measures across years and habitats. We also found a weak association between the integrated score of nestling immune function and individual performance, but only under certain environmental conditions. We conclude that the ecological context can strongly affect the interpretation of immune defenses in the wild. Given that spatiotemporal variations are likely to affect individual immune defenses, great caution should be used when generalizing conclusions to other study systems.