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.

When death comes: linking predator-prey activity patterns to timing of mortality to understand predation risk.

The assumption that activity and foraging are risky for prey underlies many predator-prey theories and has led to the use of predator-prey activity overlap as a proxy of predation risk. However, the simultaneous measures of prey and predator activity along with timing of predation required to test this assumption have not been available. Here, we used accelerometry data on snowshoe hares (Lepus americanus) and Canada lynx (Lynx canadensis) to determine activity patterns of prey and predators and match these to precise timing of predation. Surprisingly we found that lynx kills of hares were as likely to occur during the day when hares were inactive as at night when hares were active. We also found that activity rates of hares were not related to the chance of predation at daily and weekly scales, whereas lynx activity rates positively affected the diel pattern of lynx predation on hares and their weekly kill rates of hares. Our findings suggest that predator-prey diel activity overlap may not always be a good proxy of predation risk, and highlight a need for examining the link between predation and spatio-temporal behaviour of predator and prey to improve our understanding of how predator-prey behavioural interactions drive predation risk.

Does coat colour influence survival? A test in a cyclic population of snowshoe hares.

Some mammal species inhabiting high-latitude biomes have evolved a seasonal moulting pattern that improves camouflage via white coats in winter and brown coats in summer. In many high-latitude and high-altitude areas, the duration and depth of snow cover has been substantially reduced in the last five decades. This reduction in depth and duration of snow cover may create a mismatch between coat colour and colour of the background environment, and potentially reduce the survival rate of species that depend on crypsis. We used long-term (1977-2020) field data and capture-mark-recapture models to test the hypothesis that whiteness of the coat influences winter apparent survival in a cyclic population of snowshoe hares (Lepus americanus) at Kluane, Yukon, Canada. Whiteness of the snowshoe hare coat in autumn declined during this study, and snowshoe hares with a greater proportion of whiteness in their coats in autumn survived better during winter. However, whiteness of the coat in spring did not affect subsequent summer survival. These results are consistent with the hypothesis that the timing of coat colour change in autumn can reduce overwinter survival. Because declines in cyclic snowshoe hare populations are strongly affected by low winter survival, the timing of coat colour change may adversely affect snowshoe hare population dynamics as climate change continues.

Balancing food acquisition and predation risk drives demographic changes in snowshoe hare population cycles.

Snowshoe hare cycles are one of the most prominent phenomena in ecology. Experimental studies point to predation as the dominant driving factor, but previous experiments combining food supplementation and predator removal produced unexplained multiplicative effects on density. We examined the potential interactive effects of food limitation and predation in causing hare cycles using an individual-based food-supplementation experiment over-winter across three cycle phases that naturally varied in predation risk. Supplementation doubled over-winter survival with the largest effects occurring in the late increase phase. Although the proximate cause of mortality was predation, supplemented hares significantly decreased foraging time and selected for conifer habitat, potentially reducing their predation risk. Supplemented hares also lost less body mass which resulted in the production of larger leverets. Our results establish a mechanistic link between how foraging time, mass loss and predation risk affect survival and reproduction, potentially driving demographic changes associated with hare cycles.

Population variation alters aggression-associated oxytocin and vasopressin expressions in brains of Brandt's voles in field conditions.

Density-dependent change in aggressive behavior contributes to the population regulation of many small rodents, but the underlying neurological mechanisms have not been examined in field conditions. We hypothesized that crowding stress and aggression-associated oxytocin (OT) and arginine vasopressin (AVP) in specific regions of the brain may be closely related to aggressive behaviors and population changes of small rodents. We analyzed the association of OT and AVP expression, aggressive behavior, and population density of Brandt's voles in 24 large semi-natural enclosures (0.48 ha each) in Inner Mongolia grassland. We tested the effects of population density on the OT/AVP system and aggressive behavior by experimentally manipulating populations of Brandt's voles in the grassland enclosures. High density was positively and significantly associated with more aggressive behavior, and increased expression of mRNA and protein of AVP and its receptor, but decreased expression of mRNA and protein of OT and its receptor in specific brain regions of the voles. Our study suggests that changes in OT/AVP expression are likely a result of the increased psychosocial stress that these voles experience during overcrowding, and thus the OT/AVP system can be used as indicators of density-dependent stressors in Brandt's voles.

The impact of variable predation risk on stress in snowshoe hares over the cycle in North America's boreal forest: adjusting to change.

The boreal forest is one of the world's ecosystems most affected by global climate warming. The snowshoe hare, its predators, and their population dynamics dominate the mammalian component of the North American boreal forest. Our past research has shown the 9-11-year hare cycle to be predator driven, both directly as virtually all hares that die are killed by their predators, and indirectly through sublethal risk effects on hare stress physiology, behavior, and reproduction. We replicated this research over the entire cycle by measuring changes in predation risk expected to drive changes in chronic stress. We examined changes in hare condition and stress axis function using a hormonal challenge protocol in the late winter of 7 years-spanning all phases of the cycle from the increase through to the low (2014-2020). We simultaneously monitored changes in hare abundance as well as those of their primary predators, lynx and coyotes. Despite observing the expected changes in hare-predator numbers over the cycle, we did not see the predicted changes in chronic stress metrics in the peak and decline phases. Thus, the comprehensive physiological signature indicative of chronic predator-induced stress seen from our previous work was not present in this current cycle. We postulate that hares may now be increasingly showing behavior-mediated rather than stress-mediated responses to their predators. We present evidence that increases in primary productivity have affected boreal community structure and function. We speculate that climate change has caused this major shift in the indirect effects of predation on hares.

Contribution of late-litter juveniles to the population dynamics of snowshoe hares.

Determining the factors driving cyclic dynamics in species has been a primary focus of ecology. For snowshoe hares (Lepus americanus), explanations of their 10-year population cycles most commonly feature direct predation during the peak and decline, in combination with their curtailment in reproduction. Hares are thought to stop producing third and fourth litters during the cyclic decline and do not recover reproductive output for several years. The demographic effects of these reproductive changes depend on the consistency of this pattern across cycles, and the relative contribution to population change of late-litter versus early litter juveniles. We used monitoring data on snowshoe hares in Yukon, Canada, to examine the contribution of late-litter juveniles to the demography of their cycles, by assigning litter group for individuals caught in autumn based on body size and capture date. We found that fourth-litter juveniles occur consistently during the increase phase of each cycle, but are rare and have low over-winter survival (0.05) suggesting that population increase is unlikely to be caused by their occurrence. The proportion of third-litter juveniles captured in the autumn remains relatively constant across cycle phases, while over-winter survival rates varies particularly for earlier-litter juveniles (0.14-0.39). Juvenile survival from all litters is higher during the population increase and peak, relative to the low and decline. Overall, these results suggest that the transition from low phase to population growth may stem in large part from changes in juvenile survival as opposed to increased reproductive output through the presence of a 4th litter.

Prey availability and ambient temperature influence carrion persistence in the boreal forest.

Scavenging by vertebrates can have important impacts on food web stability and persistence, and can alter the distribution of nutrients throughout the landscape. However, scavenging communities have been understudied in most regions around the globe, and we lack understanding of the biotic drivers of vertebrate scavenging dynamics. In this paper, we examined how changes in prey density and carrion biomass caused by population cycles of a primary prey species, the snowshoe hare Lepus americanus, influence scavenging communities in the northern boreal forest. We further examined the impact of habitat and temperature on scavenging dynamics. We monitored the persistence time, time until first scavenger, and number of species scavenging experimentally-placed hare carcasses over four consecutive years in the southwestern Yukon. We simultaneously monitored hare density and carrion biomass to examine their influence relative to temperature, habitat, and seasonal effects. For the primary scavengers, we developed species-specific scavenging models to determine variation on the effects of these factors across species, and determine which species may be driving temporal patterns in the entire community. We found that the efficiency of the scavenging community was affected by hare density, with carcass persistence decreasing when snowshoe hare densities declined, mainly due to increased scavenging rates by Canada lynx Lynx canadensis. However, prey density did not influence the number of species scavenging a given carcass, suggesting prey abundance affects carrion recycling but not necessarily the number of connections in the food web. In addition, scavenging rates increased in warmer temperatures, and there were strong seasonal effects on the richness of the vertebrate scavenging community. Our results demonstrate that vertebrate scavenging communities are sensitive to changes in species' demography and environmental change, and that future assessments of food web dynamics should consider links established through scavenging.

Experimental increase in predation risk causes a cascading stress response in free-ranging snowshoe hares.

Extensive research confirms that environmental stressors like predation risk can profoundly affect animal condition and physiology. However, there is a lack of experimental research assessing the suite of physiological responses to risk that may arise under realistic field conditions, leaving a fragmented picture of risk-related physiological change and potential downstream consequences on individuals. We increased predation risk in free-ranging snowshoe hares (Lepus americanus) during two consecutive summers by simulating natural chases using a model predator and monitored hares intensively via radio-telemetry and physiological assays, including measures designed to assess changes in stress physiology and overall condition. Compared to controls, risk-augmented hares had 25.8% higher free plasma cortisol, 15.9% lower cortisol-binding capacity, a greater neutrophil:lymphocyte skew, and a 10.4% increase in glucose. Despite these changes, intra-annual changes in two distinct condition indices, were unaffected by risk exposure. We infer risk-augmented hares compensated for changes in their stress physiology through either compensatory foraging and/or metabolic changes, which allowed them to have comparable condition to controls. Although differences between controls and risk-augmented hares were consistent each year, both groups had heightened stress measures during the second summer, likely reflecting an increase in natural stressors (i.e., predators) in the environment. We show that increased predation risk in free-ranging animals can profoundly alter stress physiology and that compensatory responses may contribute to limiting effects of such changes on condition. Ultimately, our results also highlight the importance of biologically relevant experimental risk manipulations in the wild as a means of assessing physiological responses to natural stressors.

Using experimentation to understand the 10-year snowshoe hare cycle in the boreal forest of North America.

Population cycles have long fascinated ecologists from the time of Charles Elton in the 1920s. The discovery of large population fluctuations in undisturbed ecosystems challenged the idea that pristine nature was in a state of balance. The 10-year cycle of snowshoe hares (Lepus americanus Erxleben) across the boreal forests of Canada and Alaska is a classic cycle, recognized by fur traders for more than 300 years. Since the 1930s, ecologists have investigated the mechanisms that might cause these cycles. Proposed causal mechanisms have varied from sunspots to food supplies, parasites, diseases, predation and social behaviour. Both the birth rate and the death rate change dramatically over the cycle. Social behaviour was eliminated as a possible cause because snowshoe hares are not territorial and do not commit infanticide. Since the 1960s, large-scale manipulative experiments have been used to discover the major limiting factors. Food supply and predation quickly became recognized as potential key factors causing the cycle. Experiments adding food and restricting predator access to field populations have been decisive in pinpointing predation as the key mechanism causing these fluctuations. The immediate cause of death of most snowshoe hares is predation by a variety of predators, including the Canada lynx (Lynx canadensis Kerr). The collapse in the reproductive rate is not due to food shortage as was originally thought, but is a result of chronic stress from predator chases. Five major issues remain unresolved. First, what is the nature of the predator-induced memory that results in the prolonged low phase of the cycle? Second, why do hare cycles form a travelling wave, starting in the centre of the boreal forest in Saskatchewan and travelling across western Canada and Alaska? Third, why does the amplitude of the cycle vary greatly from one cycle to the next in the same area? Fourth, do the same mechanisms of population limitation apply to snowshoe hares in eastern North American or in similar ecosystems across Siberia? Finally, what effect will climatic warming have on all the above issues? The answers to these questions remain for future generations of biologists to determine.

Seed-predator satiation and Janzen-Connell effects vary with spatial scales for seed-feeding insects.

BACKGROUND AND AIMS: The Janzen-Connell model predicts that common species suffer high seed predation from specialized natural enemies as a function of distance from parent trees, and consequently as a function of conspecific density, whereas the predator satiation hypothesis predicts that seed attack is reduced due to predator satiation at high seed densities. Pre-dispersal predation by insects was studied while seeds are still on parent trees, which represents a frequently overlooked stage in which seed predation occurs. METHODS: Reproductive tree density and seed production were investigated from ten Quercus serrata populations located in south-west China, quantifying density-dependent pre-dispersal seed predation over two years by three insect groups. KEY RESULTS: Acorn infestation was nearly twice as high in the low-seed year as that in the high-seed year, with considerable spatio-temporal variation in the direction and magnitude of density-dependent pre-dispersal seed predation evident. Across whole populations of trees, a high density of reproductive trees caused predator satiation and reduced insect attack in the high-seed year. Within individual trees, and consistent with the Janzen-Connell model, overall insect seed predation was positively correlated with seed production in the low-seed year. In addition, there was variation among insect taxa, with positive density-dependent seed predation by Curculio weevils in the high-seed year and moths in the low-seed year, but apparent density independence by Cyllorhynchites weevils in both years. CONCLUSIONS: The overall trend of negative density-dependent, pre-dispersal seed predation suggests that predator satiation limited the occurrence of Janzen-Connell effects across Q. serrata populations. Such effects may have large impacts on plant population dynamics and tree diversity, depending on the extent to which they are reduced by counteracting positive density-dependent predation for seeds on individual trees and other factors affecting successful recruitment.

Why Do the Boreal Forest Ecosystems of Northwestern Europe Differ from Those of Western North America?

The boreal forest is one of the largest terrestrial biomes on Earth. Conifers normally dominate the tree layer across the biome, but other aspects of ecosystem structure and dynamics vary geographically. The cause of the conspicuous differences in the understory vegetation and the herbivore-predator cycles between northwestern Europe and western North America presents an enigma. Ericaceous dwarf shrubs and 3- to 4-year vole-mustelid cycles characterize the European boreal forests, whereas tall deciduous shrubs and 10-year snowshoe hare-lynx cycles characterize the North American ones. We discuss plausible explanations for this difference and conclude that it is bottom-up: Winter climate is the key determinant of the dominant understory vegetation that then determines the herbivore-predator food-web interactions. The crucial unknown for the twenty-first century is how climate change and increasing instability will affect these forests, both with respect to the dynamics of individual plant and animal species and to their community interactions.

Successive sheep grazing reduces population density of Brandt's voles in steppe grassland by altering food resources: a large manipulative experiment.

Livestock grazing has shaped grassland ecosystems around the world. Previous studies indicated grazing showed various impacts on small rodents; however, most studies were conducted over 1-2 years without controlling for confounding factors such as immigration/emigration and predation in rodents. Brandt's voles (Lasiopodomys brandtii) are generally recognized as pests because of food overlap with domestic herbivores, but are also important for biodiversity conservation because they provide nests or food to many birds. Fully understanding the ecological relationship between domestic herbivores and small mammals is essential to making ecosystem management decisions. To address these needs, we carried out a field experiment during the period 2010-2013 to assess the effects of sheep grazing on vegetation and the population density of Brandt's voles along a gradient of three grazing intensities by using 12 large-scale enclosures. Responses of Brandt's voles to livestock grazing varied with grazing intensity and year. As compared to the control group, sheep grazing had no effect on vole abundance in the first year but an overall negative effect on vole abundance in the following 3 years. Successive grazing caused decreases in survival and male body mass of voles, but had no significant effect on fecundity. Negative effects of grazing were associated with a grazing-induced deterioration in both food quantity (reflected by biomass and cover of less-preferred plants), and food quality (measured by tannin and total phenol content). Our findings highlight the urgent need for more flexible management of yearly rotational grazing to optimize livestock production while maintaining species diversity and ecosystem health.

Predators, energetics and fitness drive neonatal reproductive failure in red squirrels.

Neonatal reproductive failure should occur when energetic costs of parental investment outweigh fitness benefits. However, little is known about the drivers of neonatal reproductive failure in free-ranging species experiencing continuous natural variation in predator abundance and in the energetic and fitness costs and benefits associated with parental investment. Long-term comprehensive studies are required to better understand how biotic, abiotic and life-history conditions interact to drive occurrences of reproductive failure in the wild. Using 24 years (1987-2011) of reproductive data from a northern boreal population of North American red squirrels in south-western Yukon, we examined the effects of predator abundance, energetics (resource availability, ambient temperature and litter size) and fitness benefits (probability of overwinter juvenile survival and maternal age) on occurrences of neonatal reproductive failure (494/2670 reproductive attempts; 18·5%). Neonatal reproductive failure was driven by a combination of predator abundance, and the energetic and fitness costs and benefits of parental investment. The abundance of mustelids and maternal age was positively related to the occurrence of neonatal reproductive failure. High energy costs associated with a combination of low resource availability and cold ambient temperatures or large litters, corresponded to increased occurrences of neonatal reproductive failure. However, the strength of these relationships was influenced by variation in juvenile overwinter survival (i.e. fitness benefits). We provide evidence that predation pressure is an important driver of neonatal reproductive failure. In addition, we found a trade-off occurs between resource-dependent energetic and fitness costs and benefits of raising the current litter to independence.

Impact of high predation risk on genome-wide hippocampal gene expression in snowshoe hares.

The population dynamics of snowshoe hares (Lepus americanus) are fundamental to the ecosystem dynamics of Canada's boreal forest. During the 8- to 11-year population cycle, hare densities can fluctuate up to 40-fold. Predators in this system (lynx, coyotes, great-horned owls) affect population numbers not only through direct mortality but also through sublethal effects. The chronic stress hypothesis posits that high predation risk during the decline severely stresses hares, leading to greater stress responses, heightened ability to mobilize cortisol and energy, and a poorer body condition. These effects may result in, or be mediated by, differential gene expression. We used an oligonucleotide microarray designed for a closely-related species, the European rabbit (Oryctolagus cuniculus), to characterize differences in genome-wide hippocampal RNA transcript abundance in wild hares from the Yukon during peak and decline phases of a single cycle. A total of 106 genes were differentially regulated between phases. Array results were validated with quantitative real-time PCR, and mammalian protein sequence similarity was used to infer gene function. In comparison to hares from the peak, decline phase hares showed increased expression of genes involved in metabolic processes and hormone response, and decreased expression of immune response and blood cell formation genes. We found evidence for predation risk effects on the expression of genes whose putative functions correspond with physiological impacts known to be induced by predation risk in snowshoe hares. This study shows, for the first time, a link between changes in demography and alterations in neural RNA transcript abundance in a natural population.

Newly discovered landscape traps produce regime shifts in wet forests.

We describe the "landscape trap" concept, whereby entire landscapes are shifted into, and then maintained (trapped) in, a highly compromised structural and functional state as the result of multiple temporal and spatial feedbacks between human and natural disturbance regimes. The landscape trap concept builds on ideas like stable alternative states and other relevant concepts, but it substantively expands the conceptual thinking in a number of unique ways. In this paper, we (i) review the literature to develop the concept of landscape traps, including their general features; (ii) provide a case study as an example of a landscape trap from the mountain ash (Eucalyptus regnans) forests of southeastern Australia; (iii) suggest how landscape traps can be detected before they are irrevocably established; and (iv) present evidence of the generality of landscape traps in different ecosystems worldwide.

Population and community ecology: past progress and future directions.

Population and community ecology as a science are about 100 years old, and we discuss here our opinion of what approaches have progressed well and which point to possible future directions. The three major threads within population and community ecology are theoretical ecology, statistical tests and models, and experimental ecology. We suggest that our major objective is to understand what factors determine the distribution and abundance of organisms within populations and communities, and we evaluate these threads against this major objective. Theoretical ecology is elegant and compelling and has laid the groundwork for achieving our overall objectives with useful simple models. Statistics and statistical models have contributed informative methods to analyze quantitatively our understanding of distribution and abundance for future research. Population ecology is difficult to carry out in the field, even though we may have all the statistical methods and models needed to achieve results. Community ecology is growing rapidly with much description but less understanding of why changes occur. Biodiversity science cuts across all these subdivisions but rarely digs into the necessary population and community science that might solve conservation problems. Climate change affects all aspects of ecology but to assume that everything in population and community ecology is driven by climate change is oversimplified. We make recommendations on how to advance the field with advice for present and future generations of population and community ecologists.

Long-term monitoring of cycles in Clethrionomys rutilus in the Yukon boreal forest.

Baseline studies of small rodent populations in undisturbed ecosystems are rare. We report here 50 years of monitoring and experimentation in Yukon of a dominant rodent species in the North American boreal forest, the red-backed vole Clethrionomys rutilus. These voles breed in summer, weigh 20-25 g, and reach a maximum density of 20 to 25 per ha. Their populations have shown consistent 3-4-year cycles for the last 50 years with the only change being that peak densities averaged 8/ha until 2000 and 18/ha since that year. During the last 25 years, we have measured food resources, predator numbers, and winter weather, and for 1-year social interactions, to estimate their contribution to changes in the rate of summer increase and the rate of overwinter decline. All these potential limiting factors could contribute to changes in density, and we measured their relative contributions statistically with multiple regressions. The rate of winter decline in density was related to both food supply and winter severity. The rate of summer increase was related to summer berry crops and white spruce cone production. No measure of predator numbers was related to winter or summer changes in vole abundance. There was a large signal of climate change effects in these populations. There is no density dependence in summer population growth and only a weak one in winter population declines. None of our results provide a clear understanding of what generates 3-4-year cycles in these voles, and the major missing piece may be an understanding of social interactions at high density.

Linking climate change to population cycles of hares and lynx.

The classic 10-year population cycle of snowshoe hares (Lepus americanus, Erxleben 1777) and Canada lynx (Lynx canadensis, Kerr 1792) in the boreal forests of North America has drawn much attention from both population and community ecologists worldwide; however, the ecological mechanisms driving the 10-year cyclic dynamic pattern are not fully revealed yet. In this study, by the use of historic fur harvest data, we constructed a series of generalized additive models to study the effects of density dependence, predation, and climate (both global climate indices of North Atlantic Oscillation index (NAO), Southern Oscillation index (SOI) and northern hemispheric temperature (NHT) and local weather data including temperature, rainfall, and snow). We identified several key pathways from global and local climate to lynx with various time lags: rainfall shows a negative, and snow shows a positive effect on lynx; NHT and NAO negatively affect lynx through their positive effect on rainfall and negative effect on snow; SOI positively affects lynx through its negative effect on rainfall. Direct or delayed density dependency effects, the prey effect of hare on lynx and a 2-year delayed negative effect of lynx on hare (defined as asymmetric predation) were found. The simulated population dynamics is well fitted to the observed long-term fluctuations of hare and lynx populations. Through simulation, we find density dependency and asymmetric predation, only producing damped oscillation, are necessary but not sufficient factors in causing the observed 10-year cycles; while extrinsic climate factors are important in producing and modifying the sustained cycles. Two recent population declines of lynx (1940-1955 and after 1980) were likely caused by ongoing climate warming indirectly. Our results provide an alternative explanation to the mechanism of the 10-year cycles, and there is a need for further investigation on links between disappearance of population cycles and global warming in hare-lynx system.