Destabilizing effect of climate change on the persistence of a short-lived primate.

Seasonal tropical environments are among those regions that are the most affected by shifts in temperature and rainfall regimes under climate change, with potentially severe consequences for wildlife population persistence. This persistence is ultimately determined by complex demographic responses to multiple climatic drivers, yet these complexities have been little explored in tropical mammals. We use long-term, individual-based demographic data (1994 to 2020) from a short-lived primate in western Madagascar, the gray mouse lemur (Microcebus murinus), to investigate the demographic drivers of population persistence under observed shifts in seasonal temperature and rainfall. While rainfall during the wet season has been declining over the years, dry season temperatures have been increasing, with these trends projected to continue. These environmental changes resulted in lower survival and higher recruitment rates over time for gray mouse lemurs. Although the contrasting changes have prevented the study population from collapsing, the resulting increase in life-history speed has destabilized an otherwise stable population. Population projections under more recent rainfall and temperature levels predict an increase in population fluctuations and a corresponding increase in the extinction risk over the next five decades. Our analyses show that a relatively short-lived mammal with high reproductive output, representing a life history that is expected to closely track changes in its environment, can nonetheless be threatened by climate change.

Population Dynamic Consequences of Context-Dependent Trade-Offs across Life Histories.

AbstractTrade-offs are central to life history theory and play a role in driving life history diversity. They arise from a finite amount of resources that need to be allocated among different functions by an organism. Yet covariation of demographic rates among individuals frequently do not reflect allocation trade-offs because of variation in resource acquisition. The covariation of traits among individuals can thus vary with the environment and often increases in benign environments. Surprisingly, little is known about how such context-dependent expression of trade-offs among individuals affect population dynamics across species with different life histories. To study their influence on population stability, we develop an individual-based simulation where covariation in demographic rates varies with the environment. We use it to simulate population dynamics for various life histories across the slow-fast pace-of-life continuum. We found that the population dynamics of slower life histories are relatively more sensitive to changes in covariation, regardless of the trade-off considered. Additionally, we found that the impact on population stability depends on which trade-off is considered, with opposite effects of intraindividual and intergenerational trade-offs. Last, the expression of different trade-offs can feed back to influence generation time through selection acting on individual heterogeneity within cohorts, ultimately affecting population dynamics.

Dispersal and connectivity in increasingly extreme climatic conditions.

While climate change has been shown to impact several life-history traits of wild-living animal populations, little is known about its effects on dispersal and connectivity. Here, we capitalize on the highly variable flooding regime of the Okavango Delta to investigate the impacts of changing environmental conditions on the dispersal and connectivity of the endangered African wild dog (Lycaon pictus). Based on remote sensed flood extents observed over 20 years, we derive two extreme flood scenarios: a minimum and a maximum flood extent, representative of very dry and very wet environmental periods. These conditions are akin to those anticipated under increased climatic variability, as it is expected under climate change. Using a movement model parameterized with GPS data from dispersing individuals, we simulate 12,000 individual dispersal trajectories across the ecosystem under both scenarios and investigate patterns of connectivity. Across the entire ecosystem, surface water coverage during maximum flood extent reduces dispersal success (i.e., the propensity of individuals to disperse between adjacent subpopulations) by 12% and increases dispersal durations by 17%. Locally, however, dispersal success diminishes by as much as 78%. Depending on the flood extent, alternative dispersal corridors emerge, some of which in the immediate vicinity of human-dominated landscapes. Notably, under maximum flood extent, the number of dispersing trajectories moving into human-dominated landscapes decreases by 41% at the Okavango Delta's inflow, but increases by 126% at the Delta's distal end. This may drive the amplification of human-wildlife conflict. While predicting the impacts of climate change on environmental conditions on the ground remains challenging, our results highlight that environmental change may have significant consequences for dispersal patterns and connectivity, and ultimately, population viability. Acknowledging and anticipating such impacts will be key to effective conservation strategies and to preserve vital dispersal corridors in light of climate change and other human-related landscape alterations.

Timing outweighs magnitude of rainfall in shaping population dynamics of a small mammal species in steppe grassland.

Climate change-induced shifts in species phenology differ widely across trophic levels, which may lead to consumer-resource mismatches with cascading population and ecosystem consequences. Here, we examined the effects of different rainfall patterns (i.e., timing and amount) on the phenological asynchrony of population of a generalist herbivore and their food sources in semiarid steppe grassland in Inner Mongolia. We conducted a 10-y (2010 to 2019) rainfall manipulation experiment in 12 0.48-ha field enclosures and found that moderate rainfall increases during the early rather than late growing season advanced the timing of peak reproduction and drove marked increases in population size through increasing the biomass of preferred plant species. By contrast, greatly increased rainfall produced no further increases in vole population growth due to the potential negative effect of the flooding of burrows. The increases in vole population size were more coupled with increased reproduction of overwintered voles and increased body mass of young-of-year than with better survival. Our results provide experimental evidence for the fitness consequences of phenological mismatches at the population level and highlight the importance of rainfall timing on the population dynamics of small herbivores in the steppe grassland environment.

Higher Mortality Is Not a Universal Cost of Dispersal: A Case Study in African Wild Dogs.

AbstractMortality is considered one of the main costs of dispersal. A reliable evaluation of mortality, however, is often hindered by a lack of information about the fate of individuals that disappear under unexplained circumstances (i.e., missing individuals). Here, we addressed this uncertainty by applying a Bayesian mortality analysis that inferred the fate of missing individuals according to information from individuals with known fate. Specifically, we tested the hypothesis that mortality during dispersal is higher than mortality among nondispersers using 32 years of mark-resighting data from a free-ranging population of the endangered African wild dog (Lycaon pictus) in northern Botswana. Contrary to expectations, we found that mortality during dispersal was lower than mortality among nondispersers, indicating that higher mortality is not a universal cost of dispersal. Our findings suggest that group living can incur costs for certain age classes, such as limited access to resources as group density increases, that exceed the mortality costs associated with dispersal. By challenging the accepted expectation of higher mortality during dispersal, we urge for further investigations of this key life history trait and propose a robust statistical approach to reduce bias in mortality estimates.

Dispersal-induced social stress prolongs gestation in wild meerkats.

In the majority of mammals, gestation length is relatively consistent and seldom varies by more than 3%. In a few species, females can adjust gestation length by delaying the development of the embryo after implantation. Delays in embryonic development allow females to defer the rising energetic costs of gestation when conditions are unfavourable, reducing the risk of embryo loss. Dispersal in mammals that breed cooperatively is a period when food intake is likely to be suppressed and stress levels are likely to be high. Here, we show that pregnant dispersing meerkats (Suricata suricatta), which have been aggressively evicted from their natal group and experience weight loss and extended periods of social stress, prolong their gestation by means of delayed embryonic development. Repeated ultrasound scans of wild, unanaesthetized females throughout their pregnancies showed that pregnancies of dispersers were on average 6.3% longer and more variable in length (52-65 days) than those of residents (54-56 days). The variation in dispersers shows that, unlike most mammals, meerkats can adapt to stress by adjusting their pregnancy length by up to 25%. By doing so, they potentially rearrange the costs of gestation during adverse conditions of dispersal and enhance offspring survival.

Contrasting effects of climate change on seasonal survival of a hibernating mammal.

Seasonal environmental conditions shape the behavior and life history of virtually all organisms. Climate change is modifying these seasonal environmental conditions, which threatens to disrupt population dynamics. It is conceivable that climatic changes may be beneficial in one season but result in detrimental conditions in another because life-history strategies vary between these time periods. We analyzed the temporal trends in seasonal survival of yellow-bellied marmots (Marmota flaviventer) and explored the environmental drivers using a 40-y dataset from the Colorado Rocky Mountains (USA). Trends in survival revealed divergent seasonal patterns, which were similar across age-classes. Marmot survival declined during winter but generally increased during summer. Interestingly, different environmental factors appeared to drive survival trends across age-classes. Winter survival was largely driven by conditions during the preceding summer and the effect of continued climate change was likely to be mainly negative, whereas the likely outcome of continued climate change on summer survival was generally positive. This study illustrates that seasonal demographic responses need disentangling to accurately forecast the impacts of climate change on animal population dynamics.

Dispersal Decreases Survival but Increases Reproductive Opportunities for Subordinates in a Cooperative Breeder.

AbstractIn most socially structured populations, the formation of new groups depends on the survival and reproduction of dispersing individuals. Quantifying vital rates in dispersers, however, is difficult because of the logistic challenges of following wide-ranging animals. Here, using data from free-ranging meerkats (Suricata suricatta), we estimate survival and reproduction of dispersing females and compare these estimates to data for established residents. Meerkat groups consist of a dominant pair and several subordinate helpers. Female helpers are evicted from their resident groups by the dominant female, allowing her to monopolize reproduction, and evicted females may form small dispersing coalitions. We show that, as in established resident groups, one female is behaviorally dominant in parties of dispersing females. During dispersal and the first 4 months after new group formation, survival is lower for all females compared with established resident groups. At the same time, subordinates in disperser groups have higher birth rates than those in established groups, which rarely breed successfully. This may partly offset the survival costs of dispersal to subordinate females. Further studies of dispersal based on direct observation of dispersing animals are needed to explore the costs and benefits of dispersal in species with contrasting breeding systems.

A Trade-Off between Robustness to Environmental Fluctuations and Speed of Evolution.

AbstractUnderstanding how a species' life history affects its capacity to cope with environmental changes is important in the context of rapid climate changes. Reinterpreting previous results from a well-developed theoretical framework, we show that a trade-off exists between a species' ability to genetically adapt to long-term gradual environmental changes and its ability to demographically resist short-term environmental perturbations, causing variation in its vital rates. Surprisingly, this important insight has not been made formally explicit before. Choosing archetypal life histories along the fast-slow pace-of-life continuum and modeling their eco-evolutionary dynamics, we further show that long-lived species have larger demographic robustness to interannual fluctuations but limited trait evolutionary responses in gradually changing environments. In contrast, short-lived species had larger evolvability but reduced demographic robustness. This trade-off bears heavily on extinction probabilities of populations tracking fast trait changes in stochastic environments. Faster trait evolution in short-lived species came at the expense of their higher sensitivity to short-term fluctuations, causing higher extinction rates than for long-lived species. Long-lived species persisted better on short timescales but built maladaptation and an extinction debt over time. This work shows how modeling species' eco-evolutionary dynamics can help to assess species vulnerability to environmental changes.

Distinct body-size responses to warming climate in three rodent species.

In mammals, body-size responses to warming climates are diverse, and the mechanisms underlying these different responses have been little investigated. Using temporal and spatial datasets of three rodent species distributed across different climatic zones in China, we investigated temporal and spatial trends of body size (length and mass), identified the critical drivers of these trends, and inferred the potential causes underlying the distinct body-size responses to the critical drivers. We found that body mass of all species remained stable over time and across space. Body length, however, increased in one species over time and in two species across space. Generally, body-length variation was predicted best by minimum ambient temperature. Moreover, in two species, body length changed linearly with temperature differences between ancestral and colonization areas. These distinct temperature-length patterns may jointly be caused by species-specific temperature sensitivities and experienced magnitudes of warming. We hypothesize that species or populations distributed across distinct temperature gradients evolved different intrinsic temperature sensitivities, which affect how their body sizes respond to warming climates. Our results suggest that size trends associated with climate change should be explored at higher temporal and spatial resolutions, and include clades of species with similar distributions.

Community structure determines the predictability of population collapse.

Early warning signals (EWS) are phenomenological tools that have been proposed as predictors of the collapse of biological systems. Although a growing body of work has shown the utility of EWS based on either statistics derived from abundance data or shifts in phenotypic traits such as body size, so far this work has largely focused on single species populations. However, to predict reliably the future state of ecological systems, which inherently could consist of multiple species, understanding how reliable such signals are in a community context is critical. Here, reconciling quantitative trait evolution and Lotka-Volterra equations, which allow us to track both abundance and mean traits, we simulate the collapse of populations embedded in mutualistic and multi-trophic predator-prey communities. Using these simulations and warning signals derived from both population- and community-level data, we showed the utility of abundance-based EWS, as well as metrics derived from stability-landscape theory (e.g. width and depth of the basin of attraction), were fundamentally linked. Thus, the depth and width of such stability-landscape curves could be used to identify which species should exhibit the strongest EWS of collapse. The probability a species displays both trait and abundance-based EWS was dependent on its position in a community, with some species able to act as indicator species. In addition, our results also demonstrated that in general trait-based EWS were less reliable in comparison with abundance-based EWS in forecasting species collapses in our simulated communities. Furthermore, community-level abundance-based EWS were fairly reliable in comparison with their species-level counterparts in forecasting species-level collapses. Our study suggests a holistic framework that combines abundance-based EWS and metrics derived from stability-landscape theory that may help in forecasting species loss in a community context.

Why disease ecology needs life-history theory: a host perspective.

When facing an emerging infectious disease of conservation concern, we often have little information on the nature of the host-parasite interaction to inform management decisions. However, it is becoming increasingly clear that the life-history strategies of host species can be predictive of individual- and population-level responses to infectious disease, even without detailed knowledge on the specifics of the host-parasite interaction. Here, we argue that a deeper integration of life-history theory into disease ecology is timely and necessary to improve our capacity to understand, predict and mitigate the impact of endemic and emerging infectious diseases in wild populations. Using wild vertebrates as an example, we show that host life-history characteristics influence host responses to parasitism at different levels of organisation, from individuals to communities. We also highlight knowledge gaps and future directions for the study of life-history and host responses to parasitism. We conclude by illustrating how this theoretical insight can inform the monitoring and control of infectious diseases in wildlife.

Proximity to humans affects local social structure in a giraffe metapopulation.

Experimental laboratory evidence suggests that animals with disrupted social systems express weakened relationship strengths and have more exclusive social associations, and that these changes have functional consequences. A key question is whether anthropogenic pressures have a similar impact on the social structure of wild animal communities. We addressed this question by constructing a social network from 6 years of systematically collected photographic capture-recapture data spanning 1,139 individual adult female Masai giraffes inhabiting a large, unfenced, heterogeneous landscape in northern Tanzania. We then used the social network to identify distinct social communities, and tested whether social or anthropogenic and other environmental factors predicted differences in social structure among these communities. We reveal that giraffes have a multilevel social structure. Local preferences in associations among individuals scale up to a number of distinct, but spatially overlapping, social communities, that can be viewed as a large interconnected metapopulation. We then find that communities that are closer to traditional compounds of Indigenous Masai people express weaker relationship strengths and the giraffes in these communities are more exclusive in their associations. The patterns we characterize in response to proximity to humans reflect the predictions of disrupted social systems. Near bomas, fuelwood cutting can reduce food resources, and groups of giraffes are more likely to encounter livestock and humans on foot, thus disrupting the social associations among group members. Our results suggest that human presence could potentially be playing an important role in determining the conservation future of this megaherbivore.

Behavioural change during dispersal and its relationship to survival and reproduction in a cooperative breeder.

The ability of dispersing individuals to adjust their behaviour to changing conditions is instrumental in overcoming challenges and reducing dispersal costs, consequently increasing overall dispersal success. Understanding how dispersers' behaviour and physiology change during the dispersal process, and how they differ from resident individuals, can shed light on the mechanisms by which dispersers increase survival and maximise reproduction. By analysing individual behaviour and concentrations of faecal glucocorticoid metabolites (fGCM), a stress-associated biomarker, we sought to identify the proximate causes behind differences in survival and reproduction between dispersing and resident meerkats Suricata suricatta. We used data collected on 67 dispersing and 108 resident females to investigate (a) which individual, social and environmental factors are correlated to foraging and vigilance, and whether the role of such factors differs among dispersal phases, and between dispersers and residents; (b) how time allocated to either foraging or vigilance correlated to survival in dispersers and residents and (c) the link between aggression and change in fGCM concentration, and their relationship with reproductive rates in dispersing groups and resident groups with either long-established or newly established dominant females. Time allocated to foraging increased across dispersal phases, whereas time allocated to vigilance decreased. Time allocated to foraging and vigilance correlated positively and negatively, respectively, with dispersers' group size. We did not find a group size effect for residents. High proportions of time allocated to foraging correlated with high survival, and more so in dispersers, suggesting that maintaining good physical condition may reduce mortality during dispersal. Furthermore, while subordinate individuals rarely reproduced in resident groups, the conception rate of subordinates in newly formed dispersing groups was equal to that of their dominant individuals. Mirroring conception rates, in resident groups, fGCM concentrations were lower in subordinates than in dominants, whereas in disperser groups, fGCM concentrations did not differ between subordinates and dominants. Our results, which highlight the relationship between behavioural and physiological factors and demographic rates, provide insights into some of the mechanisms that individuals of a cooperative species can use to increase overall dispersal success.

The myriad of complex demographic responses of terrestrial mammals to climate change and gaps of knowledge: A global analysis.

Approximately 25% of mammals are currently threatened with extinction, a risk that is amplified under climate change. Species persistence under climate change is determined by the combined effects of climatic factors on multiple demographic rates (survival, development and reproduction), and hence, population dynamics. Thus, to quantify which species and regions on Earth are most vulnerable to climate-driven extinction, a global understanding of how different demographic rates respond to climate is urgently needed. Here, we perform a systematic review of literature on demographic responses to climate, focusing on terrestrial mammals, for which extensive demographic data are available. To assess the full spectrum of responses, we synthesize information from studies that quantitatively link climate to multiple demographic rates. We find only 106 such studies, corresponding to 87 mammal species. These 87 species constitute <1% of all terrestrial mammals. Our synthesis reveals a strong mismatch between the locations of demographic studies and the regions and taxa currently recognized as most vulnerable to climate change. Surprisingly, for most mammals and regions sensitive to climate change, holistic demographic responses to climate remain unknown. At the same time, we reveal that filling this knowledge gap is critical as the effects of climate change will operate via complex demographic mechanisms: a vast majority of mammal populations display projected increases in some demographic rates but declines in others, often depending on the specific environmental context, complicating simple projections of population fates. Assessments of population viability under climate change are in critical need to gather data that account for multiple demographic responses, and coordinated actions to assess demography holistically should be prioritized for mammals and other taxa.

Forest management affects seasonal source-sink dynamics in a territorial, group-living bird.

The persistence of wildlife populations is under threat as a consequence of human activities, which are degrading natural ecosystems. Commercial forestry is the greatest threat to biodiversity in boreal forests. Forestry practices have degraded most available habitat, threatening the persistence of natural populations. Understanding population responses is, therefore, critical for their conservation. Population viability analyses are effective tools to predict population persistence under forestry management. However, quantifying the mechanisms driving population responses is complex as population dynamics vary temporally and spatially. Metapopulation dynamics are governed by local dynamics and spatial factors, potentially mediating the impacts of forestry e.g., through dispersal. Here, we performed a seasonal, spatially explicit population viability analysis, using long-term data from a group-living territorial bird (Siberian jay, Perisoreus infaustus). We quantified the effects of forest management on metapopulation dynamics, via forest type-specific demography and spatially explicit dispersal, and how forestry impacted the stability of metapopulation dynamics. Forestry reduced metapopulation growth and stability, through negative effects on reproduction and survival. Territories in higher quality natural forest contributed more to metapopulation dynamics than managed forests, largely through demographic processes rather than dispersal. Metapopulation dynamics in managed forest were also less resilient to disturbances and consequently, may be more vulnerable to environmental change. Seasonal differences in source-sink dynamics observed in managed forest, but not natural forests, were caused by associated seasonal differences in dispersal. As shown here, capturing seasonal source-sink dynamics allows us to predict population persistence under human disturbance and to provide targeted conservation recommendations.

Assessing seasonal demographic covariation to understand environmental-change impacts on a hibernating mammal.

Natural populations are exposed to seasonal variation in environmental factors that simultaneously affect several demographic rates (survival, development and reproduction). The resulting covariation in these rates determines population dynamics, but accounting for its numerous biotic and abiotic drivers is a significant challenge. Here, we use a factor-analytic approach to capture partially unobserved drivers of seasonal population dynamics. We use 40 years of individual-based demography from yellow-bellied marmots (Marmota flaviventer) to fit and project population models that account for seasonal demographic covariation using a latent variable. We show that this latent variable, by producing positive covariation among winter demographic rates, depicts a measure of environmental quality. Simultaneously, negative responses of winter survival and reproductive-status change to declining environmental quality result in a higher risk of population quasi-extinction, regardless of summer demography where recruitment takes place. We demonstrate how complex environmental processes can be summarized to understand population persistence in seasonal environments.

Decreased Precipitation Predictability Negatively Affects Population Growth through Differences in Adult Survival.

Global climate change is leading to decreased climatic predictability. Theoretical work indicates that changes in the climate's intrinsic predictability will affect population dynamics and extinction, but experimental evidence is scarce. Here, we experimentally tested whether differences in intrinsic precipitation predictability affect population dynamics of the European common lizard (Zootoca vivipara) by simulating more predictable (MP) and less predictable (LP) precipitation in 12 seminatural populations over 3 years and measuring different vital rates. A seasonal age-structured matrix model was parametrized to assess treatment effects on vital rates and asymptotic population growth (λ). There was a nonsignificant trend for survival being higher in MP than in LP precipitation, and no differences existed in reproductive rates. Small nonsignificant survival differences in adults explained changes in λ, and survival differences among age classes were in line with predictions from cohort resonance. As a result, λ was significantly higher in MP than in LP precipitation. This experimentally shows that small effects have major consequences on λ, that forecasted decreases in precipitation predictability are likely to exacerbate the current rate of population decline and extinction, and that stage-structured matrix models are required to unravel the aftermath of climate change.

Eco-evolutionary processes underlying early warning signals of population declines.

Environmental change can impact the stability of ecological systems and cause rapid declines in populations. Abundance-based early warning signals have been shown to precede such declines, but detection prior to wild population collapses has had limited success, leading to the development of warning signals based on shifts in distribution of fitness-related traits such as body size. The dynamics of population abundances and traits in response to external environmental perturbations are controlled by a range of underlying factors such as reproductive rate, genetic variation and plasticity. However, it remains unknown how such ecological and evolutionary factors affect the stability landscape of populations and the detectability of abundance and trait-based early warning signals. Here, we apply a trait-based demographic approach and investigate both trait and population dynamics in response to gradual and increasing changes in the environment. We explore a range of ecological and evolutionary constraints under which stability of a population may be affected. We show both analytically and with simulations that strength of abundance- and trait-based warning signals are affected by ecological and evolutionary factors. Finally, we show that combining trait- and abundance-based information improves our ability to predict population declines. Our study suggests that the inclusion of trait dynamic information alongside generic warning signals should provide more accurate forecasts of the future state of biological systems.

When to stay and when to leave? Proximate causes of dispersal in an endangered social carnivore.

Reliable estimates of birth, death, emigration and immigration rates are fundamental to understanding and predicting the dynamics of wild populations and, consequently, inform appropriate management actions. However, when individuals disappear from a focal population, inference on their fate is often challenging. Here we used 30 years of individual-based mark-recapture data from a population of free-ranging African wild dogs Lycaon pictus in Botswana and a suite of individual, social and environmental predictors to investigate factors affecting the decision to emigrate from the pack. We subsequently used this information to assign an emigration probability to those individuals that were no longer sighted within their pack (i.e. missing individuals). Natal dispersal (i.e. emigration from the natal pack) showed seasonal patterns with female dispersal peaking prior to the mating season and male dispersal peaking at the beginning of the wet season. For both sexes, natal dispersal rate increased in the absence of unrelated individuals of the opposite sex in the pack. Male natal dispersal decreased with increasing number of pups in the pack and increased in larger packs. Female natal dispersal decreased with increasing number of pups in larger packs, but increased with increasing number of pups in smaller packs. Individuals of both sexes were less likely to exhibit secondary dispersal (i.e. emigration from a pack other than the natal pack) if they were dominant and if many pups were present in the pack. Our models predicted that 18% and 25% of missing females and males, respectively, had likely dispersed from the natal pack, rather than having died. A misclassification of this order of magnitude between dispersal and mortality can have far-reaching consequences in the evaluation and prediction of population dynamics and persistence, and potentially mislead conservation actions. Our study showed that the decision to disperse is context-dependent and that the effect of individual, social and environmental predictors differs between males and females and between natal and secondary dispersal related to different direct and indirect fitness consequences. Furthermore, we demonstrated how a thorough understanding of the proximate causes of dispersal can be used to assign a dispersal probability to missing individuals. Knowledge of causes of dispersal can then be used within an integrated framework to more reliably estimate mortality rates.