Temporal correlations among demographic parameters are ubiquitous but highly variable across species.

Temporal correlations among demographic parameters can strongly influence population dynamics. Our empirical knowledge, however, is very limited regarding the direction and the magnitude of these correlations and how they vary among demographic parameters and species' life histories. Here, we use long-term demographic data from 15 bird and mammal species with contrasting pace of life to quantify correlation patterns among five key demographic parameters: juvenile and adult survival, reproductive probability, reproductive success and productivity. Correlations among demographic parameters were ubiquitous, more frequently positive than negative, but strongly differed across species. Correlations did not markedly change along the slow-fast continuum of life histories, suggesting that they were more strongly driven by ecological than evolutionary factors. As positive temporal demographic correlations decrease the mean of the long-run population growth rate, the common practice of ignoring temporal correlations in population models could lead to the underestimation of extinction risks in most species.

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.

The two oxpecker species reveal the role of movement rates and foraging intensity in species coexistence.

The two Buphagus oxpecker species are specialized passerines that forage for ticks and other food particles on the body of ungulates in the African savannahs. One of their intriguing features is their ability to coexist despite sharing the same, specialized diet. Using co-occurrence data (photographs of giraffes with oxpeckers on them) and approximate Bayesian computing, we demonstrate that yellow-billed oxpeckers changed host faster than red-billed oxpeckers and appeared to displace red-billed oxpeckers from preferred giraffe body parts. Conversely, red-billed oxpeckers exhibited a fuller use of each host and displaced yellow-billed oxpeckers from distal giraffe body parts. These findings highlight that the partition of giraffe hosts in two separate niches was only part of the coexistence story in this species pair. More precisely, the oxpeckers shared the resource by exploiting it at different rates. They engaged in different trade-offs between giving-up density, patch discovery rate and competitor displacement ability. They illustrate the importance of the time frame of interactions.

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.

Spatial memory shapes density dependence in population dynamics.

Most population dynamics studies assume that individuals use space uniformly, and thus mix well spatially. In numerous species, however, individuals do not move randomly, but use spatial memory to visit renewable resource patches repeatedly. To understand the extent to which memory-based foraging movement may affect density-dependent population dynamics through its impact on competition, we developed a spatially explicit, individual-based movement model where reproduction and death are functions of foraging efficiency. We compared the dynamics of populations of with- and without-memory individuals. We showed that memory-based movement leads to a higher population size at equilibrium, to a higher depletion of the environment, to a marked discrepancy between the global (i.e. measured at the population level) and local (i.e. measured at the individual level) intensities of competition, and to a nonlinear density dependence. These results call for a deeper investigation of the impact of individual movement strategies and cognitive abilities on population dynamics.

Mismatch between birth date and vegetation phenology slows the demography of roe deer.

Marked impacts of climate change on biodiversity have frequently been demonstrated, including temperature-related shifts in phenology and life-history traits. One potential major impact of climate change is the modification of synchronization between the phenology of different trophic levels. High phenotypic plasticity in laying date has allowed many bird species to track the increasingly early springs resulting from recent environmental change, but although changes in the timing of reproduction have been well studied in birds, these questions have only recently been addressed in mammals. To track peak resource availability, large herbivores like roe deer, with a widespread distribution across Europe, should also modify their life-history schedule in response to changes in vegetation phenology over time. In this study, we analysed the influence of climate change on the timing of roe deer births and the consequences for population demography and individual fitness. Our study provides a rare quantification of the demographic costs associated with the failure of a species to modify its phenology in response to a changing world. Given these fitness costs, the lack of response of roe deer birth dates to match the increasingly earlier onset of spring is in stark contrast with the marked phenotypic responses to climate change reported in many other mammals. We suggest that the lack of phenotypic plasticity in birth timing in roe deer is linked to its inability to track environmental cues of variation in resource availability for the timing of parturition.

Life histories and conservation of long-lived reptiles, an illustration with the American crocodile (Crocodylus acutus).

Successful species conservation is dependent on adequate estimates of population dynamics, but age-specific demographics are generally lacking for many long-lived iteroparous species such as large reptiles. Accurate demographic information allows estimation of population growth rate, as well as projection of future population sizes and quantitative analyses of fitness trade-offs involved in the evolution of life-history strategies. Here, a long-term capture-recapture study was conducted from 1978 to 2014 on the American crocodile (Crocodylus acutus) in southern Florida. Over the study period, 7,427 hatchlings were marked and 380 individuals were recaptured for as many as 25 years. We estimated survival to be strongly age dependent with hatchlings having the lowest survival rates (16%) but increasing to nearly 90% at adulthood based on mark-recapture models. More than 5% of the female population were predicted to be reproductive by age 8 years; the age-specific proportion of reproductive females steadily increased until age 18 when more than 95% of females were predicted to be reproductive. Population growth rate, estimated from a Leslie-Lefkovitch stage-class model, showed a positive annual growth rate of 4% over the study period. Using a prospective sensitivity analysis, we revealed that the adult stage, as expected, was the most critical stage for population growth rate; however, the survival of younger crocodiles before they became reproductive also had a surprisingly high elasticity. We found that variation in age-specific fecundity has very limited impact on population growth rate in American crocodiles. We used a comparative approach to show that the original life-history strategy of American crocodiles is actually shared by other large, long-lived reptiles: while adult survival rates always have a large impact on population growth, this decreases with declining increasing growth rates, in favour of a higher elasticity of the juvenile stage. Crocodiles, as a long-lived and highly fecund species, deviate from the usual association of life histories of "slow" species. Current management practices are focused on nests and hatchling survival; however, protection efforts that extend to juvenile crocodiles would be most effective for conservation of the species, especially in an ever-developing landscape.

The influence of weather conditions during gestation on life histories in a wild Arctic ungulate.

The internal predictive adaptive response (internal PAR) hypothesis predicts that individuals born in poor conditions should start to reproduce earlier if they are likely to have reduced performance in later life. However, whether this is the case remains unexplored in wild populations. Here, we use longitudinal data from a long-term study of Svalbard reindeer to examine age-related changes in adult female life-history responses to environmental conditions experienced in utero as indexed by rain-on-snow (ROSutero). We show that females experiencing high ROSutero had reduced reproductive success only from 7 years of age, independent of early reproduction. These individuals were able to maintain the same annual reproductive success between 2 and 6 years as phenotypically superior conspecifics that experienced low ROSutero Young females born after high ROSutero engage in reproductive events at lower body mass (about 2.5 kg less) than those born after low ROSutero The mean fitness of females that experienced poor environmental conditions in early life was comparable with that of females exposed to good environmental conditions in early life. These results are consistent with the idea of internal PAR and suggest that the life-history responses to early-life conditions can buffer the delayed effects of weather on population dynamics.

Socially mediated effects of climate change decrease survival of hibernating Alpine marmots.

In the context of global change, an increasing challenge is to understand the interaction between weather variables and life histories. Species-specific life histories should condition the way climate influences population dynamics, particularly those that are associated with environmental constraints, such as lifestyles like hibernation and sociality. However, the influence of lifestyle in the response of organisms to climate change remains poorly understood. Based on a 23-year longitudinal study on Alpine marmots, we investigated how their lifestyle, characterized by a long hibernation and a high degree of sociality, interacts with the ongoing climate change to shape temporal variation in age-specific survival. As generally reported in other hibernating species, we expected survival of Alpine marmots to be affected by the continuous lengthening of the growing season of plants more than by changes in winter conditions. We found, however, that Alpine marmots displayed lower juvenile survival over time. Colder winters associated with a thinner snow layer lowered juvenile survival, which in turn was associated with a decrease in the relative number of helpers in groups the following years, and therefore lowered the chances of over-winter survival of juveniles born in the most recent years. Our results provide evidence that constraints on life-history traits associated with hibernation and sociality caused juvenile survival to decrease over time, which might prevent Alpine marmots coping successfully with climate change.

Early-late life trade-offs and the evolution of ageing in the wild.

Empirical evidence for declines in fitness components (survival and reproductive performance) with age has recently accumulated in wild populations, highlighting that the process of senescence is nearly ubiquitous in the living world. Senescence patterns are highly variable among species and current evolutionary theories of ageing propose that such variation can be accounted for by differences in allocation to growth and reproduction during early life. Here, we compiled 26 studies of free-ranging vertebrate populations that explicitly tested for a trade-off between performance in early and late life. Our review brings overall support for the presence of early-late life trade-offs, suggesting that the limitation of available resources leads individuals to trade somatic maintenance later in life for high allocation to reproduction early in life. We discuss our results in the light of two closely related theories of ageing-the disposable soma and the antagonistic pleiotropy theories-and propose that the principle of energy allocation roots the ageing process in the evolution of life-history strategies. Finally, we outline research topics that should be investigated in future studies, including the importance of natal environmental conditions in the study of trade-offs between early- and late-life performance and the evolution of sex-differences in ageing patterns.

Sex-specific determinants of fitness in a social mammal.

Sociality should evolve when the fitness benefits of group living outweigh the costs. Theoretical models predict an optimal group size maximizing individual fitness. However, beyond the number of individuals present in a group, the characteristics of these individuals, like their sex, are likely to affect the fitness payoffs of group living. Using 20 years of individually based data on a social mammal, the Alpine marmot (Marmota marmota), we tested for the occurrence of an optimal group size and composition, and for sex-specific effects of group characteristics on fitness. Based on lifetime data of 52 males and 39 females, our findings support the existence of an optimal group size maximizing male fitness and an optimal group composition maximizing fitness of males and females. Additionally, although group characteristics (i.e., size, composition and instability) affecting male and female fitness differed, fitness depended strongly on the number of same-sex subordinates within the social group in the two sexes. By comparing multiple measures of social group characteristics and of fitness in both sexes, we highlighted the sex-specific determinants of fitness in the two sexes and revealed the crucial role of intrasexual competition in shaping social group composition.

Disentangling direct and growth-mediated influences on early survival: a mechanistic approach.

1. Early survival is a key life-history trait that often accounts for a large part of the variation in individual fitness and shapes population dynamics. The factors influencing early survival are multiple in large herbivores, including malnutrition, predation, cohort variation or maternal effects. However, the mechanistic pathways connecting these drivers to variation in early survival are much less studied. Indeed, whether these factors influence early survival directly or indirectly through early growth remains to be disentangled. 2. In this study, we used a path analysis to separate the direct and indirect (i.e. mediated by early growth) pathways through which sex, birth date, cohort and family effects influence early survival. We used a large data set of marked roe deer newborns collected from 1985 to 2010 in the intensively monitored population of Trois Fontaines (France). 3. We found that most drivers have indirect influences on early survival through early growth. Indeed, cohort effects influenced early survival through the indirect effect of precipitation around birth on early growth. Precipitation also had direct effects on early survival. Family effects indirectly influenced early survival. Twins from the same litter grew at about the same rate, so they had the same fate. Moreover, some factors, such as birth date, had both direct and indirect effects on roe deer early survival, with fawns born early in the season benefiting from high early survival both because they have more time to grow before the harsh season and because they grow faster during their first days of life than late-born fawns. 4. These findings suggest that most drivers of early survival previously identified in large mammalian herbivores may affect early survival primarily through their influence on early growth. Disentangling the direct and indirect pathways by which different factors influence early survival is of crucial importance to understand the mechanisms shaping this key component of individual fitness.

Quantifying the influence of measured and unmeasured individual differences on demography.

1. Demographic rates can vary not only with measured individual characters like age, sex and mass but also with unmeasured individual variables like behaviour, genes and health. 2. Predictions from population models that include measured individual characteristics often differ from models that exclude them. Similarly, unmeasured individual differences have the potential to impact predictions from population models. However, unmeasured individual differences are rarely included in population models. 3. We construct stage- and age-structured models (where stage is mass) of a roe deer population, which are parameterized from statistical functions that either include, or ignore, unmeasured individual differences. 4. We found that mass and age structures substantially impacted model parameters describing population dynamics, as did temporal environmental variation, while unmeasured individual differences impacted parameters describing population dynamics to a much smaller extent once individual heterogeneity related to mass and age has been included in the model. We discuss how our assumptions (unmeasured individual differences only in mean trait values) could have influenced our findings and under what circumstances unmeasured individual differences could have had a larger impact on population dynamics. 5. There are two reasons explaining the relative small influence of unmeasured individual differences on population dynamics in roe deer. First, individual body mass and age both capture a large amount of individual differences in roe deer. Second, in large populations of long-lived animals, the average quality of individuals (independent of age and mass) within the population is unlikely to show substantial variation over time, unless rapid evolution is occurring. So even though a population consisting of high-quality individuals would have much higher population growth rate than a population consisting of low-quality individuals, the probability of observing a population consisting only of high-quality individuals is small.

Fitness consequences of environmental conditions at different life stages in a long-lived vertebrate.

The predictive adaptive response (PAR) hypothesis proposes that animals adjust their physiology and developmental trajectory during early life in anticipation of their future environments. Accordingly, when environmental conditions in early life match environmental conditions during adulthood, individual fitness should be greater. Here, we test this hypothesis in a long-lived mammal, the roe deer, using data from two contrasting populations, intensively monitored for more than 35 years. In the highly productive site, the fitness of female roe deer increased with the quality of environment during adulthood and, contrary to predictions of PAR, individuals born in good conditions always outperformed those born under poor conditions. In the resource-limited site, the fitness of female roe deer born in poor years was better than those born in good conditions in poor years when the animals were adult, but not in good years. Although consistent with predictions of PAR, we showed that this pattern is likely to be a consequence of increased viability selection during the juvenile stage for animals born in poor years. While PARs are often advanced in evolutionary medicine, our findings suggest that detailed biological processes should be investigated before drawing conclusions about the existence of this phenomenon.

A one night stand? Reproductive excursions of female roe deer as a breeding dispersal tactic.

Breeding dispersal, defined as the net movement between successive breeding sites, remains a poorly understood and seldom reported phenomenon in mammals, despite its importance for population dynamics and genetics. In large herbivores, females may be more mobile during the breeding season, undertaking short-term trips (excursions) outside their normal home range. If fertilisation occurs, leading to gene flow of the male genome, this behaviour could be considered a form of breeding dispersal from a genetic point of view. Here, we investigated ranging behaviour of 235 adult roe deer using intensive GPS monitoring in six populations across Europe within the EURODEER initiative. We show that excursions are common from June to August among females, with 41.8% (vs. 18.1% of males) making at least one excursion. Most individuals performed only one excursion per season and departure dates for females were concentrated in time, centred on the rutting period, suggesting a link with reproduction. The distance females travelled during excursions was significantly greater than the site-specific average diameter of a male home range, while travel speed decreased once they progressed beyond this diameter, indicating search behaviour or interaction with other male(s) outside the resident male's territory. Because adults are normally highly sedentary, the potential for mating with relatives is substantial; hence, we conclude that rut excursions could be an alternative tactic enabling females to avoid mating with a closely related male. To understand better the ultimate drivers at play, it will be crucial to explore the genetic causes and consequences of this behaviour.

How does climate change influence demographic processes of widespread species? Lessons from the comparative analysis of contrasted populations of roe deer.

How populations respond to climate change depends on the interplay between life history, resource availability, and the intensity of the change. Roe deer are income breeders, with high levels of allocation to reproduction, and are hence strongly constrained by the availability of high quality resources during spring. We investigated how recent climate change has influenced demographic processes in two populations of this widespread species. Spring began increasingly earlier over the study, allowing us to identify 2 periods with contrasting onset of spring. Both populations grew more slowly when spring was early. As expected for a long-lived and iteroparous species, adult survival had the greatest potential impact on population growth. Using perturbation analyses, we measured the relative contribution of the demographic parameters to observed variation in population growth, both within and between periods and populations. Within periods, the identity of the critical parameter depended on the variance in growth rate, but variation in recruitment was the main driver of observed demographic change between periods of contrasting spring earliness. Our results indicate that roe deer in forest habitats cannot currently cope with increasingly early springs. We hypothesise that they should shift their distribution to richer, more heterogeneous landscapes to offset energetic requirements during the critical rearing stage.

Decreasing litter size of marmots over time: a life history response to climate change?

The way that plants and animals respond to climate change varies widely among species, but the biological features underlying their actual response remains largely unknown. Here, from a 20-year monitoring study, we document a continuous decrease in litter size of the Alpine marmot (Marmota marmota) since 1990. To cope with harsh winters, Alpine marmots hibernate in burrows and their reproductive output should depend more on spring conditions compared to animals that are active year-round. However, we show that litter size decreased over time because of the general thinning of winter snow cover that has been repeatedly reported to occur in the Alps over the same period, despite a positive effect of an earlier snowmelt in spring. Our results contrast markedly with a recent study on North American yellow-bellied marmots, suggesting that between-species differences in life histories can lead to opposite responses to climate change, even between closely related species. Our case study therefore demonstrates the idiosyncratic nature of the response to climate change and emphasizes, even for related species with similar ecological niches, that it may be hazardous to extrapolate life history responses to climate change from one species to another.

Variation in adult body mass of roe deer: early environmental conditions influence early and late body growth of females.

There is increasing evidence that environmental conditions experienced early in life can markedly affect an organism's life history, but the pathways by which early environment influences adult phenotype are poorly known. We used long-term data from two roe deer (Capreolus capreolus) populations (Chizé and Trois-Fontaines, France) to investigate the direct and indirect (operating through fawn body mass) effects of environmental conditions during early life on adult body mass. We found that environmental conditions (population size and spring temperatures) around birth influenced body mass of adult females through both direct and indirect effects in both populations. The occurrence of direct effects means that, for a given fawn body mass, adult female mass decreases with adverse conditions in early life. In contrast, we found no evidence for direct effects of early-life conditions on adult body mass of males, suggesting the existence of sex-specific long-term responses of body mass to stressful early conditions. Our results provide evidence that early environmental conditions influence the adult phenotype through persistent effects over the body development in wild mammal populations.

Seasonality, weather and climate affect home range size in roe deer across a wide latitudinal gradient within Europe.

1. Because many large mammal species have wide geographical ranges, spatially distant populations may be confronted with different sets of environmental conditions. Investigating how home range (HR) size varies across environmental gradients should yield a better understanding of the factors affecting large mammal ecology. 2. We evaluated how HR size of a large herbivore, the roe deer (Capreolus capreolus), varies in relation to seasonality, latitude (climate), weather, plant productivity and landscape features across its geographical range in Western Europe. As roe deer are income breeders, expected to adjust HR size continuously to temporal variation in food resources and energetic requirements, our baseline prediction was for HR size to decrease with proxies of resource availability. 3. We used GPS locations of roe deer collected from seven study sites (EURODEER collaborative project) to estimate fixed-kernel HR size at weekly and monthly temporal scales. We performed an unusually comprehensive analysis of variation in HR size among and within populations over time across the geographical range of a single species using generalized additive mixed models and linear mixed models, respectively. 4. Among populations, HR size decreased with increasing values for proxies of forage abundance, but increased with increases in seasonality, stochastic variation of temperature, latitude and snow cover. Within populations, roe deer HR size varied over time in relation to seasonality and proxies of forage abundance in a consistent way across the seven populations. Thus, our findings were broadly consistent across the distributional range of this species, demonstrating a strong and ubiquitous link between the amplitude and timing of environmental seasonality and HR size at the continental scale. 5. Overall, the variability in average HR size of roe deer across Europe reflects the interaction among local weather, climate and seasonality, providing valuable insight into the limiting factors affecting this large herbivore under contrasting conditions. The complexity of the relationships suggests that predicting ranging behaviour of large herbivores in relation to current and future climate change will require detailed knowledge not only about predicted increases in temperature, but also how this interacts with factors such as day length and climate predictability.

Parturition date for a given female is highly repeatable within five roe deer populations.

Births are highly synchronized among females in many mammal populations in temperate areas. Although laying date for a given female is also repeatable within populations of birds, limited evidence suggests low repeatability of parturition date for individual females in mammals, and between-population variability in repeatability has never, to our knowledge, been assessed. We quantified the repeatability of parturition date for individual females in five populations of roe deer, which we found to vary between 0.54 and 0.93. Each year, some females gave birth consistently earlier in the year, whereas others gave birth consistently later. In addition, all females followed the same lifetime trajectory for parturition date, giving birth progressively earlier as they aged. Giving birth early should allow mothers to increase offspring survival, although few females managed to do so. The marked repeatability of parturition date in roe deer females is the highest ever reported for a mammal, suggesting low phenotypic plasticity in this trait.