Deciphering the effects of climate on animal populations: diagnostic analysis provides new interpretation of Soay sheep dynamics

Soay sheep on the island of Hirta exhibit periodic population collapses that have been proposed to result from nonlinear interactions between weather, population density, and age structure. Here we employ a diagnostic approach to reanalyze the data from 1985 to 2004 and find that climate mainly affects the equilibrium population size, thus acting as a lateral perturbation. From this, we derive a simple energetic model for a population interacting with its food supply in the presence of variable winter weather. This model explains the strong nonlinearity in the Soay sheep population regulation function and provides a framework for evaluating climatic perturbations. We examined two integrative climatic indexes, one representing effects on forage production and the other representing the severity of winter weather. Results suggest that the latter has the main effect on Soay sheep population dynamics. Models incorporating this variable provided fairly accurate predictions of Soay sheep population fluctuations. The diagnostic approach offers an objective way to develop simple, nonstructured population models that are useful for understanding the causes of population fluctuations and predicting population changes, provided they are based on a careful consideration of the underlying biological and/or ecological mechanisms.     

Assessing the relative importance of intrinsic and extrinsic influence on sheep population dynamics on Hirta Island, UK

Identifying the relative importance of intrinsic factors and extrinsic environmental variations on population or ecosystem dynamics is important for ecological conservation research. Here, we use a systematic method proposed by De Menezes and Barabási [2004. Separating internal and external dynamics of complex systems. Physical Review Letters, 93, 068701] to reanalyse the long-term monitoring data of Soay sheep population fluctuations and climate variations on Hirta Island, UK. Our results indicate that the climate conditions have a higher impact than internal factors on the fluctuations of sheep population. The sheep population dynamics are internally self-regulating. The scaling relationships between sheep population and external and internal standard deviations are similar. The threshold of the sheep population on this island as determined by our study is around 1197, which is consistent with previous studies by other methods. Our study indicates that this systematic method may help to understand some of the complicated aspects of population dynamics about which detailed knowledge is limited.     

Comparative ungulate dynamics: the devil is in the detail

Attempts to relate species differences in population dynamics to variation in life histories rely on the assumption that the causes of contrasts in demography are sufficiently simple to be derived from first principles. Here, we investigate the causes of contrasts in dynamics between two ungulate populations on Hebridean islands (red deer and Soay sheep) and show that differences in stability, as well as in the effects of variation in density and climate, are related to differences in timing of reproduction relative to seasonal variation in resource abundance. In both populations, attempts to predict changes in population size sufficiently accurately for the results to be useful for management purposes require a knowledge of the responses of different age and sex categories to changes in density and climate, as well as of population structure.     

Analysis of phenotypic change in relation to climatic drivers in a population of Soay sheep Ovis aries

Climatic change has frequently been identified as a key driver of change in biological communities. These changes can take the form of alterations to population dynamics, phenotypic characters, genetics and the life history of organisms and can have impacts on entire ecosystems. This study presents a novel investigation of how changes in a large scale climatic index, the North Atlantic Oscillation (NAO) can influence population dynamics and phenotypic characters in a population of ungulates. We use an integral projection model combined with actual climate change predictions to project future body size distributions for a population of Soay sheep Ovis aries. The climate change predictions used to direct our model projections were taken from published results of climate models, covering a range of different emissions scenarios. Our model results showed that for positive changes in the mean NAO large population declines occurred simultaneously with increases in mean body weight. The exact direction and magnitude of changes to population dynamics and character distributions were dependent on the greenhouse gas emissions scenario and model used to predict the NAO. This study has demonstrated how integral projection models can use outputs of climate models to direct projections of population dynamics and phenotypic character distributions. This approach allows the results of this study to be placed within current climate change research. The nature of integral projection models means that this methodology can be easily applied to other populations. The model can also be easily updated when new climate change predictions become available, making it a useful tool for understanding potential population level responses to climatic change. Synthesis Understanding how changes in climate affect biological communities is a key component in predicting the future form of populations. Utilising a novel approach that incorporates climatic drivers (in this instance the winter North Atlantic Oscillation) into an integral projection model framework, we predict future Soay sheep dynamics under specific climate change scenarios. Tracking quantitative trait distributions and life history metrics, our results predict declining population size and increasing body weight for an increasingly positive winter North Atlantic Oscillation index, as predicted by climate models. This has important implications for future wildlife management strategies and linking demographic responses to climate change.     

Climate, food, density and wildlife population growth rate

1. The aim of this study was to derive and evaluate a priori models of the relationship between annual instantaneous population growth rate (r) and climate. These were derived from the numerical response of annual r and food, and the effect of climate on a parameter in the numerical response. The goodness of fit of a range of such deductive models to data on annual r of Soay sheep and red deer were evaluated using information-theoretic (AICc-based) analyses. 2. The analysis for sheep annual r showed negative effects of abundance and negative effects of the interaction of abundance and climate, measured as March rainfall (and winter NAO) in the best fitting models. The analysis for deer annual r showed a negative effect of deer abundance and a positive effect of climate measured as March rainfall (but a negative effect of winter NAO), but no interaction of abundance and climate in the best fitting models. 3. There was most support in the analysis of sheep dynamics for the ratio numerical response and the assumption that parameter J (equilibrium food per animal) was influenced by climate. In the analysis of deer dynamics there was most support for the numerical responses assuming effects of food and density (Ivlev and density, food and density, and additive responses) and slightly less support for the ratio numerical response. The evaluation of such models would be aided by the collection of and incorporation of food data into the analyses.     

Population dynamics of a South American rodent: seasonal structure interacting with climate,density dependence and predator effects

Understanding the role of interactions between intrinsic feedback loops and external climatic forces is one of the central challenges within the field of population ecology. For rodent dynamics, the seasonal structure of the environment necessitates changes between two stages: reproductive and non-reproductive. Nevertheless, the interactions between seasonality, climate, density dependence and predators have been generally ignored. We demonstrate that direct climate effects, the nonlinear effect of predators and the nonlinear first-order feedback embedded in a seasonal structure are key elements underlying the large and irregular fluctuations in population numbers exhibited by a small rodent in a semi-arid region of central Chile. We found that factors influencing population growth rates clearly differ between breeding and non-breeding seasons. In addition, we detected nonlinear density dependencies as well as nonlinear and differential effects of generalist and specialist predators. Recent climatic changes may account for dramatic perturbations of the rodent's population dynamics. Changes in the predator guild induced by climate are likely to result, through the food web, in a large impact on small rodent demography and population dynamics. Assuming such interactions to be typical of ecological systems, we conclude that appropriate predictions of the ecological consequences of climate change will depend on having an in-depth understanding of the community-weather system.     

Predator-driven component Allee effects in a wild ungulate

Negative density dependence is an important driver of population dynamics of large vertebrates. Allee effects (positive density dependence), however, can affect small populations. Allee effects can be generated by predation and recent research has revealed potentially important indirect effects of predation on population dynamics. For wild populations, however, quantification of both Allee effects and indirect effects of predation remains scarce. We monitored for 27 years a bighorn sheep (Ovis canadensis) population that declined dramatically as episodes of cougar (Puma concolor) predation depressed survival. Predation led to a positive relationship between lamb survival and population size below a threshold, and to an overall positive relationship between yearling and adult ewe survival and population size. During years of high predation, lambs also suffer mortality through reduced growth, contributing a third of the total impact of predation on lamb survival. There was no positive association between population growth and population size, probably because growth was affected by several factors other than predation, including disease. Our results support the contention that predator-driven component Allee effects may exacerbate the effects of other environmental drivers and increase the risk of extinction of small populations.     

A single climate driver has direct and indirect effects on insect population dynamics

Weather drives population dynamics directly, through effects on vital rates, or indirectly, through effects on the population's competitors, predators or prey and thence on vital rates. Indirect effects may include non-additive interactions with density dependence. Detection of climate drivers is critical to predicting climate change effects, but identification of potential drivers may depend on knowing the underlying mechanisms. For the butterfly Speyeria mormonia, one climate driver, snow melt date, has multiple effects on population growth. Snow melt date in year t has density-dependent indirect effects. Through frost effects, early snow melt decreases floral resources, thence per-capita nectar availability, which determines fecundity in the lab. Snow melt date in year t?+?1 has density-independent direct effects. These effects explain 84% of the variation in population growth rate. One climate parameter thus has multiple effects on the dynamics of a species with non-overlapping generations, with one effect not detectable without understanding the underlying mechanism.     

Bayesian Inference on the Effect of Density Dependence and Weather on a Guanaco Population from Chile

Understanding the mechanisms that drive population dynamics is fundamental for management of wild populations. The guanaco (Lama guanicoe) is one of two wild camelid species in South America. We evaluated the effects of density dependence and weather variables on population regulation based on a time series of 36 years of population sampling of guanacos in Tierra del Fuego, Chile. The population density varied between 2.7 and 30.7 guanaco/km², with an apparent monotonic growth during the first 25 years; however, in the last 10 years the population has shown large fluctuations, suggesting that it might have reached its carrying capacity. We used a Bayesian state-space framework and model selection to determine the effect of density and environmental variables on guanaco population dynamics. Our results show that the population is under density dependent regulation and that it is currently fluctuating around an average carrying capacity of 45,000 guanacos. We also found a significant positive effect of previous winter temperature while sheep density has a strong negative effect on the guanaco population growth. We conclude that there are significant density dependent processes and that climate as well as competition with domestic species have important effects determining the population size of guanacos, with important implications for management and conservation.     

The population growth consequences of variation in individual heterozygosity

Heterozygosity has been associated with components of fitness in numerous studies across a wide range of taxa. Because heterozygosity is associated with individual performance it is also expected to be associated with population dynamics. However, investigations into the association between heterozygosity and population dynamics have been rare because of difficulties in linking evolutionary and ecological processes. The choice of heterozygosity measure is a further issue confounding such studies as it can be biased by individual differences in the frequencies of the alleles studied, the number of alleles at each locus as well as the total number of loci typed. In this study, we first examine the differences between the principal metrics used to calculate heterozygosity using long-term data from a marked population of Soay sheep (Ovis aries). Next, by means of statistical transformation of the homozygosity weighted by loci index, we determine how heterozygosity contributes to population growth in Soay sheep by modelling individual contributions to population growth (p(t(i))) as a function of several covariates, including sex, weight and faecal egg count--a surrogate of parasitic nematode burden in the gut. We demonstrate that although heterozygosity is associated with some components of fitness, most notably adult male reproductive success, in general it is only weakly associated with population growth.     

Decomposing variation in population growth into contributions from environment and phenotypes in an age-structured population

Evaluating the relative importance of ecological drivers responsible for natural population fluctuations in size is challenging. Longitudinal studies where most individuals are monitored from birth to death and where environmental conditions are known provide a valuable resource to characterize complex ecological interactions. We used a recently developed approach to decompose the observed fluctuation in population growth of the red deer population on the Isle of Rum into contributions from climate, density and their interaction and to quantify their relative importance. We also quantified the contribution of individual covariates, including phenotypic and life-history traits, to population growth. Fluctuations in composition in age and sex classes ((st)age structure) of the population contributed substantially to the population dynamics. Density, climate, birth weight and reproductive status contributed less and approximately equally to the population growth. Our results support the contention that fluctuations in the population's (st)age structure have important consequences for population dynamics and underline the importance of including information on population composition to understand the effect of human-driven changes on population performance of long-lived species.     

Climate change: is the dark Soay sheep endangered?

It was recently reported that the proportion of dark-coloured Soay sheep (Ovis aries) in the Hebrides has decreased, despite the fact that dark sheep tend to be larger than lighter sheep, and there exists a selective advantage to large body size. It was concluded that an apparent genetic linkage between loci for the coat colour polymorphism and loci with antagonistic effects on body size explained the decrease. Those results explain why the proportion of dark animals is not increasing, but not why it is decreasing. Between 1985 and 2005 there was a significant increase in mean ambient temperature near the islands. We suggest that, while in the past a dark coat has offset the metabolic costs of thermoregulation by absorbing solar radiation, the selective advantage of a dark coat may be waning as the climate warms in the North Atlantic. In parallel, Bergman''s rule may be operating, reducing the selective advantage of large body size in the cold. Either or both of these mechanisms can explain the decrease in the proportion of dark-coloured larger sheep in this population in which smaller (and light-coloured) sheep should be favoured by their lower gross energy demand. If environmental effects are the cause of the decline, then we can expect the proportion of dark-coloured Soay sheep to decrease further.     

Dynamics of an introduced population of mouflon Ovis aries on the sub‐Antarctic archipelago of Kerguelen

A commonly reported pattern in large herbivores is their propensity to irrupt and crash when colonizing new areas. However, the relative role of density‐dependence, climate, and cohort effects on demographic rates in accounting for the irruptive dynamics of large herbivores remains unclear. Using a 37‐yr time series of abundance in a mouflon Ovis aries population located on Haute Island, a sub‐Antarctic island of Kerguelen, 1) we investigated if irruptive dynamics occurred and 2) we quantified the relative effects of density and climate on mouflon population dynamics. Being released in a new environment, we expected mouflon to show rapid growth and marked over‐compensation. In support of this prediction, we found a two‐phase dynamics, the first phase being characterised by an irruptive pattern best described by the θ‐Caughley model. Parameter estimates were r_m=0.29±0.005(maximum growth rate), K=473±45 (carrying capacity) and S=2903±396 (surplus) mouflon. With a θ=3.18±0.69 our model also supported the hypothesis that density dependence is strongest at high density in large herbivores. The second phase was characterised by an unstable dynamics where growth rate was negatively affected by population abundance and winter precipitation. Climate, however, did not trigger population crashes and our model suggested that lagged density‐dependence and over‐grazing were the probable causes of mouflon irruptive dynamics. We compare our results with those of Soay sheep and discuss the possibility of a reversible alteration of the island carrying capacity after the initial over‐grazing period.     

Population dynamics can be more important than physiological limits for determining range shifts under climate change

Evidence is accumulating that species' responses to climate changes are best predicted by modelling the interaction of physiological limits, biotic processes and the effects of dispersal‐limitation. Using commercially harvested blacklip (Haliotis rubra) and greenlip abalone (Haliotis laevigata) as case studies, we determine the relative importance of accounting for interactions among physiology, metapopulation dynamics and exploitation in predictions of range (geographical occupancy) and abundance (spatially explicit density) under various climate change scenarios. Traditional correlative ecological niche models (ENM) predict that climate change will benefit the commercial exploitation of abalone by promoting increased abundances without any reduction in range size. However, models that account simultaneously for demographic processes and physiological responses to climate‐related factors result in future (and present) estimates of area of occupancy (AOO) and abundance that differ from those generated by ENMs alone. Range expansion and population growth are unlikely for blacklip abalone because of important interactions between climate‐dependent mortality and metapopulation processes; in contrast, greenlip abalone should increase in abundance despite a contraction in AOO. The strongly non‐linear relationship between abalone population size and AOO has important ramifications for the use of ENM predictions that rely on metrics describing change in habitat area as proxies for extinction risk. These results show that predicting species' responses to climate change often require physiological information to understand climatic range determinants, and a metapopulation model that can make full use of this data to more realistically account for processes such as local extirpation, demographic rescue, source‐sink dynamics and dispersal‐limitation.     

Early growth and sucking behaviour of Soay sheep in a fluctuating population

Annual variation in growth rate and sucking behaviour of lambs was studied in a fluctuating population of Soay sheep on Hirta, St. Kilda. Growth rates during the summer declined with increasing population size in the previous autumn despite an increase in time spent sucking in the first six weeks of life. The increase in time spent sucking was due largely to an increase in sucking frequency and, since a higher proportion of sucking attempts were rejected, probably reflected that lambs obtain little milk as a result of poor maternal condition following winters at high population density. After accounting for the density dependent variation, annual differences in lamb growth rates were positively related to the increase in biomass of live grasses and forbs between spring and summer. Since food availability was influenced strongly by the numbers surviving the winter, lambs born after the very high mortality at peak population density were able to compensate to some extent for their poor initial growth. However, improved food availability was never sufficient to facilitate complete catch-up growth and may permanently influence adult size and reproduction.     

Climate and spatio-temporal variation in the population dynamics of a long distance migrant, the white stork

1. A central question in ecology is to separate the relative contribution of density dependence and stochastic influences to annual fluctuations in population size. Here we estimate the deterministic and stochastic components of the dynamics of different European populations of white stork Ciconia ciconia. We then examined whether annual changes in population size was related to the climate during the breeding period (the 'tap hypothesis' sensu Saether, Sutherland & Engen (2004, Advances in Ecological Research, 35, 185 209) or during the nonbreeding period, especially in the winter areas in Africa (the 'tube hypothesis'). 2. A general characteristic of the population dynamics of this long-distance migrant is small environmental stochasticity and strong density regulation around the carrying capacity with short return times to equilibrium. 3. Annual changes in the size of the eastern European populations were correlated by rainfall in the wintering areas in Africa as well as local weather in the breeding areas just before arrival and in the later part of the breeding season and regional climate variation (North Atlantic Oscillation). This indicates that weather influences the population fluctuations of white storks through losses of sexually mature individuals as well as through an effect on the number of individuals that manages to establish themselves in the breeding population. Thus, both the tap and tube hypothesis explains climate influences on white stork population dynamics. 4. The spatial scale of environmental noise after accounting for the local dynamics was 67 km, suggesting that the strong density dependence reduces the synchronizing effects of climate variation on the population dynamics of white stork. 5. Several climate variables reduced the synchrony of the residual variation in population size after accounting for density dependence and demographic stochasticity, indicating that these climate variables had a synchronizing effect on the population fluctuations. In contrast, other climatic variables acted as desynchronizing agents. 6. Our results illustrate that evaluating the effects of common environmental variables on the spatio-temporal variation in population dynamics require estimates and modelling of their influence on the local dynamics.     

Climate variation and regional gradients in population dynamics of two hole-nesting passerines

Latitudinal gradients in population dynamics can arise through regional variation in the deterministic components of the population dynamics and the stochastic factors. Here, we demonstrate an increase with latitude in the contribution of a large-scale climate pattern, the North Atlantic Oscillation (NAO), to the fluctuations in size of populations of two European hole-nesting passerine species. However, this influence of climate induced different latitudinal gradients in the population dynamics of the two species. In the great tit the proportion of the variability in the population fluctuations explained by the NAO increased with latitude, showing a larger impact of climate on the population fluctuations of this species at higher latitudes. In contrast, no latitudinal gradient was found in the relative contribution of climate to the variability of the pied flycatcher populations because the total environmental stochasticity increased with latitude. This shows that the population ecological consequences of an expected climate change will depend on how climate affects the environmental stochasticity in the population process. In both species, the effects will be larger in those parts of Europe where large changes in climate are expected.     

Dynamics of a harvested moose population in a variable environment

1. Population size, calves per female, female mean age and adult sex ratio of a moose ( Alces alces ) population in Vefsn, northern Norway were reconstructed from 1967 to 1993 using cohort analysis and catch-at-age data from 96% (6752) of all individuals harvested.
2. The dynamics of the population were influenced mainly by density-dependent harvesting, stochastic variation in climate and intrinsic variation in the age-structure of the female segment of the population.
3. A time delay in the assignment of hunting permits in relation to population size increased fluctuations in population size.
4. Selective harvesting of calves and yearlings increased the mean age of adult females in the population, and, because fecundity in moose is strongly age-specific, the number of calves per female concordantly increased. However, after years with high recruitment, the adult mean age decreased as large cohorts entered the adult age-groups. This age-structure effect generated cycles in the rate of recruitment to the population and fluctuations introduced time-lags in the population dynamics.
5. An inverse relationship between recruitment rate and population density, mediated by a density-dependent decrease in female body condition, could potentially have constituted a regulatory mechanism in the dynamics of the population, but this effect was counteracted by a density-dependent increase in the mean age of adult females.
6. Stochastic variation in winter snow depth and summer temperature had delayed effects on recruitment rate and in turn population growth rate, apparently through effects on female body condition before conception.     

Patterns and processes of population dynamics with fluctuating habitat size: a case study of a marine copepod inhabiting tide pools

The logistic model is a fundamental population model often used as the basis for analyzing wildlife population dynamics. In the classic logistic model, however, population dynamics may be difficult to characterize if habitat size is temporally variable because population density can vary at a constant abundance, which results in variable strength of density‐dependent feedback for a given population size. To incorporate habitat size variability, we developed a general population model in which changes in population abundance, density, and habitat size are taken into account. From this model, we deduced several predictions for patterns and processes of population dynamics: 1) patterns of fluctuation in population abundance and density can diverge, with respect of their correlation and relative variability; and 2) along with density dependence, habitat size fluctuation can affect population growth with a time lag because changes in habitat size result in changes in population density. In order to test these predictions, we applied our model to population dynamics data of 36 populations of Tigriopus japonicus, a marine copepod inhabiting tide pools of variable sizes caused by weather processes. As expected, we found a significant difference in the fluctuation patterns of population abundance and density of T. japonicus populations with respect to the correlation between abundance and density and their relative variability, which correlates positively with the variability of habitat size. In addition, we found direct and lagged‐indirect effects of weather processes on population growth, which were associated with density dependence and impose regulatory forces on local and regional population dynamics. These results illustrate how changes in habitat size can have an impact on patterns and processes of wildlife population dynamics. We suggest that without knowledge of habitat size fluctuation, measures of population size and its variability as well as inferences about the processes of population dynamics may be misleading.     

The extended Moran effect and large-scale synchronous fluctuations in the size of great tit and blue tit populations

1. Synchronous fluctuations of geographically separated populations are in general explained by the Moran effect, i.e. a common influence on the local population dynamics of environmental variables that are correlated in space. Empirical support for such a Moran effect has been difficult to provide, mainly due to problems separating out effects of local population dynamics, demographic stochasticity and dispersal that also influence the spatial scaling of population processes. Here we generalize the Moran effect by decomposing the spatial autocorrelation function for fluctuations in the size of great tit Parus major and blue tit Cyanistes caeruleus populations into components due to spatial correlations in the environmental noise, local differences in the strength of density regulation and the effects of demographic stochasticity. 2. Differences between localities in the strength of density dependence and nonlinearity in the density regulation had a small effect on population synchrony, whereas demographic stochasticity reduced the effects of the spatial correlation in environmental noise on the spatial correlations in population size by 21.7% and 23.3% in the great tit and blue tit, respectively. 3. Different environmental variables, such as beech mast and climate, induce a common environmental forcing on the dynamics of central European great and blue tit populations. This generates synchronous fluctuations in the size of populations located several hundred kilometres apart. 4. Although these environmental variables were autocorrelated over large areas, their contribution to the spatial synchrony in the population fluctuations differed, dependent on the spatial scaling of their effects on the local population dynamics. We also demonstrate that this effect can lead to the paradoxical result that a common environmental variable can induce spatial desynchronization of the population fluctuations. 5. This demonstrates that a proper understanding of the ecological consequences of environmental changes, especially those that occur simultaneously over large areas, will require information about the spatial scaling of their effects on local population dynamics.