Adaptive responses to habitat change: Theory and tests with field experiments.

Habitat loss and change are often implicated as the primary causes of species extinction. Although any population can be instantly imperiled by catastrophe, most habitat loss occurs gradually, thus enabling affected individuals an adaptive advantage to occupy the best of their dwindling opportunities. I demonstrate how to infer the advantage between two habitats for any density and frequency-dependent strategy of habitat selection. I explore the concept of an Adaptive Dispersal Strategy Landscape to reveal the Evolutionarily Stable Strategy separately for ideal-free and ideal preemptive habitat selectors. Both solutions reveal an initially counterintuitive expectation that individuals living at high density gain insufficient adaptive advantage to disperse from a deteriorating habitat. Adaptive dispersal is constrained at high density because habitats of better quality are fully occupied. I test the theory with measures of movement and foraging in crossover experiments on a seminatural population of meadow voles. The experiment allowed the voles to choose among patches and between enclosures in which I differentially manipulated food and shelter. Although photographs from an infrared camera documented voles venturing from one habitat to the other, none became resident. Voles preferentially foraged in the richer of the two enclosures, even when I reversed treatments, and they foraged more in patches protected by mulched straw. The adaptive advantage of dispersal using a surrogate fitness proxy based on the voles' giving-up densities mirrored that generated by theory. The convergence between theory and experiment yields much-needed insight into our ability to test, predict, and hopefully resolve, the ecological, evolutionary, and conservation consequences of habitat loss.

Do animal personalities promote species coexistence? A test with sympatric boreal rodents.

The coexistence of competing species requires density feedbacks that have a larger effect on their own species' population growth than they do on others in the assembly. The feedbacks are often associated with behavioral tradeoffs that enable species to differentially exploit underlying axes of heterogeneity. Conjoining theories of species coexistence with foraging behavior and density-dependent habitat selection reveals that such tradeoffs impinge on invasion probabilities and equilibrium dynamics emerging from species' differences in habitat use. The resulting habitat separation promotes coexistence by reducing the overall interaction among species. Differential habitat selection depends on the behavioral abilities of organisms to identify and exploit the most profitable habitats and resource patches. One might thus expect that each species will evolve behavioral types distinct from those of other potential competitors. Accordingly, we exposed four coexisting species in four genera of boreal rodents to open-field tests. We used principal components (PC) to summarize their behaviors along three independent axes corresponding with clines of exploratory, vigilant, and apprehensive personalities. We confirmed that the axes represented repeatable behaviors (personalities) and assessed differences among species with a general linear model (GLM). The GLM revealed highly distinct differences among species, and between pairs of species, on each PC. Even so, it is difficult to infer the adaptive advantages of personality to the habitat segregation that reduces otherwise high interactions among species. Rather, personalities are best interpreted as co-adaptive behaviors reflecting the complex of morphological, physiological and behavioral attributes that dictate tradeoffs and enable coexistence.

On the effect of international human migration on nations' abilities to attain CO2 emission-reduction targets.

I merge publicly available data on CO2 emissions, with patterns of human movement, to analyze the anticipated effects of human migration on the abilities of nations to attain 2030 UNFCCC CO2 emission targets. I do so at both global (175 countries) and national (Canada and the USA) scales. The analyses reveal that mean per capita CO2 emissions are nearly three times higher in countries with net immigration than in countries with net emigration. Those differences project a cumulative migration-induced annual increase in global emissions of approximately 1.7 billion tonnes. For Canada and the United States, the projected total emissions attributable to migration from 2021 to 2030 vary between 0.7 and 0.9 billion tonnes. Although staggering, the annual and total emissions represent a small fraction of current global emissions totalling 36 billion tonnes per annum. Even so, the projected decadal immigration of nearly 4 million humans to Canada, and 10 million to the USA, represent significant additional challenges in reducing CO2 emissions. The challenges pale in comparison with poor nations that are minor contributors to climate change. Such nations face the incomprehensible burden of improving the quality of their citizens' lives without increasing global CO2 emissions. National and international strategies aimed at lowering emissions must thus acknowledge, and cooperatively address, consumptive inequities and expected increases in human population size and migration.

Long-term patterns in winter habitat selection, breeding and predation in a density-fluctuating, high Arctic lemming population.

Habitat selection is expected to balance benefits and costs that maximizes fitness. Using a rare data set on collared lemming (Dicrostonyx groenlandicus) winter nest location spanning more than two decades, we show that lemmings actively select for Salix snow beds, likely due to its favorable micro-climate, and that lemming habitat selection was density-dependent. Lemmings nevertheless exhibited some flexibility in their habitat selection, which appeared to be influenced by the year-to-year variation in snow conditions. The likelihood of both lemming breeding and nest predation by stoats (Mustela erminea) was not directly linked to habitat despite a delicate interplay between habitat, nest size, breeding, and predation. Hence, the larger lemming nests were found in Salix snow beds, and these were more often used for breeding, but both larger nests and nests used for breeding were also predated more often than other nests. Our study provides a clear example of how density-dependent habitat selection acts to balance fitness in the various habitats utilized by collared lemmings.

Time-averaging voles match density with long-term habitat quality.

An optimal habitat-selecting organism should use a dispersal strategy that enables occupation of the habitat yielding greatest fitness. The strategy is complicated when habitat quality varies through time. Theory predicts that the long-term distribution of individuals will match mean habitat quality while undermatching current habitat quality. I tested the prediction with experiments on controlled populations of meadow voles occupying two pairs of field enclosures. I released equal numbers, and equal sexes, of voles in each enclosure, and varied resource abundance between enclosures by supplemental feeding. I measured the voles' response with giving-up densities (GUDs) in artificial foraging patches, and with live-trapping at the end of the experiment. The data were consistent with only one of four a priori dispersal models. Giving-up densities declined with resource supply because short-term supply had no effect on population density. GUDs were invariant to the time course of the experiment because densities were proportional to each enclosure's long-term mean quality. Similar patterns in sex ratios and patterns of habitat occupation by juvenile voles born during the experiment reinforce the interpretation of time-averaged habitat matching. This study adds to the cumulating evidence that strategies of space use converge toward behavioral and evolutionary optima.

Correction to: Documenting lemming population change in the Arctic: Can we detect trends?

In the original published article, some of the symbols in figure 1A were modified incorrectly during the typesetting and publication process. The correct version of the figure is provided in this correction.

Documenting lemming population change in the Arctic: Can we detect trends?

Lemmings are a key component of tundra food webs and changes in their dynamics can affect the whole ecosystem. We present a comprehensive overview of lemming monitoring and research activities, and assess recent trends in lemming abundance across the circumpolar Arctic. Since 2000, lemmings have been monitored at 49 sites of which 38 are still active. The sites were not evenly distributed with notably Russia and high Arctic Canada underrepresented. Abundance was monitored at all sites, but methods and levels of precision varied greatly. Other important attributes such as health, genetic diversity and potential drivers of population change, were often not monitored. There was no evidence that lemming populations were decreasing in general, although a negative trend was detected for low arctic populations sympatric with voles. To keep the pace of arctic change, we recommend maintaining long-term programmes while harmonizing methods, improving spatial coverage and integrating an ecosystem perspective.

Landscapes of fear or competition? Predation did not alter habitat choice by Arctic rodents.

In systems where predation plays a key role in the dynamics of prey populations, such as in Arctic rodents, it is reasonable to assume that differential patterns of habitat use by prey species represent adaptive responses to spatial variation in predation. However, habitat selection by collared (Dicrostonyx groenlandicus) and brown (Lemmus trimucronatus) lemmings depends on intra- and inter-specific densities, and there has been little agreement on the respective influences of food abundance, predators, and competition for habitat on lemming dynamics. Thus, we investigated whether predation affected selection of sedge-meadow versus upland tundra by collared lemmings in the central Canadian Arctic. We first controlled for the effects of competition on lemming habitat selection. We then searched for an additional signal of predation by comparing habitat selection patterns between 12 control plots and one large grid where lemmings were protected from predators by fencing in 1996 and 1997, but not during 5 subsequent years when we monitored habitat use in the grid as well as in the control plots. Dicrostonyx used upland preferentially over meadows and was more numerous in 1996 and 2011 than in other sample years. Lemmus was also more abundant in 1996 than in subsequent years, but its abundance was too low in the exclosure to assess whether exclusion of predators influenced its habitat selection. Contrary to the effects of competition, predation had a negligible impact on the spatial dynamics of Dicrostonyx, at least during summer. These results suggest that any differences in predation risk between the two habitats have little direct influence on the temporal dynamics of Dicrostonyx even if induced through predator-prey cycles.

Can rare positive interactions become common when large carnivores consume livestock?

Livestock populations in protected areas are viewed negatively because of their interaction with native ungulates through direct competition for food resources. However, livestock and native prey can also interact indirectly through their shared predator. Indirect interactions between two prey species occur when one prey modifies either the functional or numerical responses of a shared predator. This interaction is often manifested as negative effects (apparent competition) on one or both prey species through increased predation risk. But indirect interactions can also yield positive effects on a focal prey if the shared predator modifies its functional response toward increased consumption of an abundant and higher-quality alternative prey. Such a phenomenon between two prey species is underappreciated and overlooked in nature. Positive indirect effects can be expected to occur in livestock-dominated wildlife reserves containing large carnivores. We searched for such positive effects in Acacia-Zizhypus forests of India's Gir sanctuary where livestock (Bubalus bubalis and Bos indicus) and a coexisting native prey (chital deer, Axis axis) are consumed by Asiatic lions (Panthera leo persica). Chital vigilance was higher in areas with low livestock density than in areas with high livestock density. This positive indirect effect occurred because lion predation rates on livestock were twice as great where livestock were abundant than where livestock density was low. Positive indirect interactions mediated by shared predators may be more common than generally thought with rather major consequences for ecological understanding and conservation. We encourage further studies to understand outcomes of indirect interactions on long-term predator-prey dynamics in livestock-dominated protected areas.

Adaptation and habitat selection in the eco-evolutionary process.

The struggle for existence occurs through the vital rates of population growth. This basic fact demonstrates the tight connection between ecology and evolution that defines the emerging field of eco-evolutionary dynamics. An effective synthesis of the interdependencies between ecology and evolution is grounded in six principles. The mechanics of evolution specifies the origin and rules governing traits and evolutionary strategies. Traits and evolutionary strategies achieve their selective value through their functional relationships with fitness. Function depends on the underlying structure of variation and the temporal, spatial and organizational scales of evolution. An understanding of how changes in traits and strategies occur requires conjoining ecological and evolutionary dynamics. Adaptation merges these five pillars to achieve a comprehensive understanding of ecological and evolutionary change. I demonstrate the value of this world-view with reference to the theory and practice of habitat selection. The theory allows us to assess evolutionarily stable strategies and states of habitat selection, and to draw the adaptive landscapes for habitat-selecting species. The landscapes can then be used to forecast future evolution under a variety of climate change and other scenarios.

Active density-dependent habitat selection in a controlled population of small mammals.

Density-dependent habitat selection has numerous and far-reaching implications to population dynamics and evolutionary processes. Although several studies suggest that organisms choose and occupy high-quality habitats over poorer ones, definitive experiments demonstrating active selection, by the same individuals at the appropriate population scale, are lacking. We conducted a reciprocal food supplementation experiment to assess whether voles would first occupy a habitat receiving extra food, then change their preference to track food supplements moved to another habitat. Meadow voles, as predicted, were more abundant in food-supplemented habitat than in others. Density declined when food supplements ceased because the voles moved to the new habitat receiving extra food. Although males and females appeared to follow different strategies, meadow-vole densities reflected habitat quality because voles actively selected the best habitat available. It is thus clear that behavioral decisions on habitat use can motivate patterns of abundance, frequency, and gene flow that have widespread effects on subsequent evolution.

Considering ecological dynamics in resource selection functions.

1. Describing distribution and abundance is requisite to exploring interactions between organisms and their environment. Recently, the resource selection function (RSF) has emerged to replace many of the statistical procedures used to quantify resource selection by animals. 2. A RSF is defined by characteristics measured on resource units such that its value for a unit is proportional to the probability of that unit being used by an organism. It is solved using a variety of techniques, particularly the binomial generalized linear model. 3. Observing dynamics in a RSF - obtaining substantially different functions at different times or places for the same species - alerts us to the varying ecological processes that underlie resource selection. 4. We believe that there is a need for us to reacquaint ourselves with ecological theory when interpreting RSF models. We outline a suite of factors likely to govern ecologically based variation in a RSF. In particular, we draw attention to competition and density-dependent habitat selection, the role of predation, longitudinal changes in resource availability and functional responses in resource use. 5. How best to incorporate governing factors in a RSF is currently in a state of development; however, we see promise in the inclusion of random as well as fixed effects in resource selection models, and matched case-control logistic regression. 6. Investigating the basis of ecological dynamics in a RSF will allow us to develop more robust models when applied to forecasting the spatial distribution of animals. It may also further our understanding of the relative importance of ecological interactions on the distribution and abundance of species.

Behavioral indicators for conserving mammal diversity.

Mammals are threatened with population decline and extinction. Numerous species require immediate conservation intervention. But our ability to identify species on the brink of decline, and to intervene successfully, depends on developing reliable leading indicators of population, community, and environmental change. Classic approaches, such as population and life history assessment, as well as indicator species, trail environmental change. Adaptive behaviors honed by natural selection to respond quickly to environmental changes represent true leading indicators that we can learn to apply to conservation and management. Excellent examples of useful behaviors for conservation include foraging behavior, patch use, and habitat selection. Comparisons among giving-up densities collected in artificial resource patches can effectively indicate the forager's predation costs, its habitat quality, mechanisms of coexistence, and environmental richness. Patterns of adaptive habitat use can similarly reveal the relative value of different types of habitat, the location, and amounts of source versus sink habitat in a landscape, the effects of human disturbance, and projections on future extinction risk. Each behavior is likely to change more quickly than population size. As useful as these and related indicators may be to managers and conservationists, similar behaviors can emerge from different causes, and immediate returns of behavior to fitness may cause rapid evolution of associated morphological and physiological traits. Conservation strategies will thereby often be most effective if they build on research programs targeting the processes influencing adaptive behaviors and that assess whether wild-type or novel behaviors are most likely to sustain populations into the future.

Can we measure carrying capacity with foraging behavior?

Carrying capacity is one of the most important, yet least understood and rarely estimated, parameters in population management and modeling. A simple behavioral metric of carrying capacity would advance theory, conservation, and management of biological populations. Such a metric should be possible because behavior is finely attuned to variation in environment including population density. We connect optimal foraging theory with population dynamics and life history to develop a simple model that predicts this sort of adaptive density-dependent change in food consumption. We then confirm the model's unexpected and manifold predictions with field experiments. The theory predicts reproductive thresholds that alter the marginal value of energy as well as the value of time. Both effects cause a pronounced discontinuity in quitting-harvest rate that we revealed with foraging experiments. Red-backed voles maintained across a range of high densities foraged at a lower density-dependent rate than the same animals exposed to low-density treatments. The change in harvest rate is diagnostic of populations that exceed their carrying capacity. Ecologists, conservation biologists, and wildlife managers may thus be able to use simple and efficient foraging experiments to estimate carrying capacity and habitat quality.

Toward an ecological synthesis: a case for habitat selection.

Habitat selection, and its associated density and frequency-dependent evolution, has a profound influence on such vital phenomena as population regulation, species interactions, the assembly of ecological communities, and the origin and maintenance of biodiversity. Different strategies of habitat selection, and their importance in ecology and evolution, can often be revealed simply by plots of density in adjacent habitats. For individual species, the strategies are closely intertwined with mechanisms of population regulation, and with the persistence of populations through time. For interacting species, strategies of habitat selection are not only responsible for species coexistence, but provide one of the most convenient mechanisms for measuring competition, and the various community structures caused by competitive interactions. Other kinds of interactions, such as those between predators and prey, demonstrate that an understanding of the coevolution of habitat-selection strategies among strongly interacting species is essential to properly interpret their spatial and temporal dynamics. At the evolutionary scale, the frequency dependence associated with habitat selection may often allow populations to diverge and diversify into separate species. Habitat selection thereby demonstrates how we can map microevolutionary strategies in behavior onto their population and community consequences, and from there, onto macroevolutionary patterns of speciation and adaptive radiation. We can anticipate that future studies of habitat selection will not only help us complete those maps, but that they will also continue to enrich the panoply of ideas that shape evolutionary ecology.

OPTIMUM BROOD SIZE: TESTS OF ALTERNATIVE HYPOTHESES.

The most productive litter size (five) was not as common as expected in a free-living population of white-footed mice. I evaluated four competing hypotheses that can explain this pattern. Reproductive costs and annual variation in recruitment appear to be insufficient explanations for the empirical distribution of litter size. Optimal investment of reproductive resources that vary among parents is supported by some tests, but not by all. The abundance of litters less than the apparent optimum is at least partially explained by asymmetric survival in large litters (the cliff-edge hypothesis). Hypotheses that explain the empirical distribution of brood size are not mutually exclusive. Several mechanisms can act alone, or interact, to create an average brood size less than that which appears to produce the greatest number of descendants.

PROXIMATE AND ULTIMATE CONTROLS ON LIFE-HISTORY VARIATION: THE EVOLUTION OF LITTER SIZE IN WHITE-FOOTED MICE (PEROMYSCUS LEUCOPUS).

Recruitment of litter-mates of nest-box-inhabiting white-footed mice was monitored to study the evolution of litter size. The frequency distribution of litter sizes was nonsymmetrical, and the most frequent litter size was less than the optimum. This was not the result of differential parental survival, which was independent of litter size produced. Recruitment remained constant or increased slightly to a peak in litters of five young, and then dropped precipitously for larger litters. The single optimum litter size of five did not appear to have any physiological correlates. Instead, the equally low probability of successful recruitment of any young from any given litter may have given rise to a bet-hedging strategy of frequent iterated reproductions. A theoretical analysis of optimal parental investment in offspring was initiated under the assumption that optimal brood size represents a maximization of differences between age-specific costs and benefits of reproduction, both of which should be measured in constant currency of inclusive fitness. In the past, benefit has been measured by current fecundity, and cost by residual reproductive value. However, reproductive value is an appropriate estimate of inclusive fitness only for organisms in which parental investment has little effect on the subsequent survival of offspring to reproductive age. Reproductive value weighted by offspring survival and devalued by the degree of genetic relatedness defines a new currency, replacement value, which is more appropriate for evaluating the costs and benefits of parent-offspring conflict over parental investment in current as opposed to future young. Total parent-offspring conflict intensifies with increases in current brood size. For species with severe reproductive constraints, such as post-partum estrus in white-footed mice, such conflict may force parents to curtail investment in current offspring at or near parturition of subsequent litters, even if that means reducing the survival of current young.

Rodent population cycles: life history adjustments to age-specific dispersal strategies and intrinsic time lags.

Multi-annual population cycles can be generated by life history responses to density dependent changes in adult and pre-reproductive survival. The proximate mechanism linking population dynamics and demography of cycling rodents appears to be high pre-reproductive dispersal at peak density, or during periods of population increase. This model is similar to the Chitty hypothesis which can best be viewed as a special case of demographic control on population size. Normally, this control should be selfreinforcing and lead to damped oscillations toward a stable population density. Intrinsic time lags induced by variation in the length of the breeding season modify the dependence of demography on population size, and enable the cycles to persist.