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Chronic stress has long been hypothesized to play a role in driving population cycles. Christian (1950) hypothesized that high population density results in chronic stress and mass "die-offs" in small mammal populations. Updated variations of this hypothesis propose that chronic stress at high population density may reduce fitness, reproduction, or program aspects of phenotype, driving population declines. We tested the effect of density on the stress axis in meadow voles (Microtus pennsylvanicus) by manipulating population density in field enclosures over three years. Using fecal corticosterone metabolites as a non-invasive measure of glucocorticoid (GC) concentrations, we found that density alone was not associated with GC differences. However, we found that the seasonal relationship of GC levels differed by density treatment, with high-density populations having elevated GC levels early in the breeding season and decreasing towards late summer. We additionally tested hippocampal glucocorticoid receptor and mineralocorticoid receptor gene expression in juvenile voles born at different densities, with the hypothesis that high density may reduce receptor expression, altering negative feedback of the stress axis. We found that females had marginally higher glucocorticoid receptor expression at high density, no effect in males, and no detectable effect of density on mineralocorticoid receptor expression in either sex. Hence, we found no evidence that high density directly impairs negative feedback in the hippocampus, but rather female offspring may be better equipped for negative feedback. We compare our findings with prior studies to attempt to disentangle the complicated relationship between density, seasonality, sex, reproduction and the stress axis., (© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Telomeres are specialized non-coding DNA sequences located at the end of chromosomes and that protect genetic information. Telomere loss over lifespan is generally viewed as a phenomenon associated with aging in animals. Recently, telomere elongation after hibernation has been described in several mammals. Whether this pattern is an adaptation to repair DNA damage caused during rewarming from torpor or if it coevolved as a mechanism to promote somatic maintenance in preparation for the upcoming reproductive effort remains unclear. In a longitudinal study measuring telomere length using buccal swabs, we tested if telomere elongation was related to reproductive success in wild adult female Columbian ground squirrels (Urocitellus columbianus) that were monitored from emergence from hibernation to the end of the reproductive season. We found three key results. First, female telomere length increased at the start of the breeding season, both in breeding and non-breeding individuals. Second, post-emergence telomere lengthening was unrelated to female future reproductive output. Third, telomere length decreased in breeding females during lactation, but remained stable in non-breeding females over a similar period. Within breeders, telomeres shortened more in females producing larger and heavier litters. We concluded that telomere lengthening after hibernation did not constrain immediate female reproductive capacities. It was more likely to be part of the body recovery process that takes place after hibernation. Telomere erosion that occurs after birth may constitute a physiological cost of female reproduction., (© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

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., (© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

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.

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.

Non-consumptive effects of predation have rarely been assessed in wildlife populations even though their impact could be as important as lethal effects. Reproduction of individuals is one of the most important demographic parameters that could be affected by predator-induced stress, which in turn can have important consequences on population dynamics. We studied non-consumptive effects of predation on the reproductive activity (i.e., mating and fertilization) of a cyclic population of brown lemmings exposed to intense summer predation in the Canadian High Arctic. Lemmings were live-trapped, their reproductive activity (i.e., testes visible in males, pregnancy/lactation in females) assessed, and predators were monitored during the summers of 2014 and 2015 within a 9 ha predator-reduction exclosure delimited by a fence and covered by a net, and on an 11 ha control area. Stress levels were quantified non-invasively with fecal corticosterone metabolites (FCM). We found that FCM levels of lemmings captured outside the predator exclosure (n = 50) were 1.6 times higher than inside (n = 51). The proportion of pregnant/lactating adult females did not differ between the two areas, nor did the proportion of adult scrotal males. We found that lemmings showed physiological stress reactions due to high predation risk, but had no sign of reduced mating activity or fertility. Thus, our results do not support the hypothesis of reproductive suppression by predator-induced stress.

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.

For foraging herbivores, both food quality and predation risk vary across the landscape. Animals should avoid low-quality food patches in favour of high-quality ones, and seek safe patches while avoiding risky ones. Herbivores often face the foraging dilemma, however, of choosing between high-quality food in risky places or low-quality food in safe places. Here, we explore how and why the interaction between food quality and predation risk affects foraging decisions of mammalian herbivores, focusing on browsers confronting plant toxins in a landscape of fear. We draw together themes of plant-herbivore and predator-prey interactions, and the roles of animal ecophysiology, behaviour and personality. The response of herbivores to the dual costs of food and fear depends on the interplay of physiology and behaviour. We discuss detoxification physiology in dealing with plant toxins, and stress physiology associated with perceived predation risk. We argue that behaviour is the interface enabling herbivores to stay or quit food patches in response to their physiological tolerance to these risks. We hypothesise that generalist and specialist herbivores perceive the relative costs of plant defence and predation risk differently and intra-specifically, individuals with different personalities and physiologies should do so too, creating individualised landscapes of food and fear. We explore the ecological significance and emergent impacts of these individual-based foraging outcomes on populations and communities, and offer predictions that can be clearly tested. In doing so, we provide an integrated platform advancing herbivore foraging theory with food quality and predation risk at its core.

We review the population dynamics of red-backed voles (Myodes species) in North America, the main deciduous and coniferous forest-dwelling microtines on this continent, and compare and contrast their pattern with that of the same or similar species in Eurasia. We identify 7 long-term studies of population changes in Myodes in North America. Using autoregressive and spectral analysis, we found that only 2 of the 7 show 3- to 5-year cycles like those found in some Eurasian populations. There was no relationship between latitude and cycling. The general lack of cyclicity is associated with two key aspects of their demography that act in tandem: first, poor overwinter survival in most years; second, chronically low densities, with irregular outbreak years. Eight factors might explain why some Myodes populations fluctuate in cycles and others fluctuate irregularly, and we review the evidence for each factor: food supplies, nutrients, predation, interspecific competition, disease, weather, spacing behavior and interactive effects. Of these eight, only food supplies appear to be sufficient to explain the differences between cyclic and non-cyclic populations. Irregular fluctuations are the result of pulsed food supplies in the form of berry crops (M. rutilus) or tree seeds (M. gapperi) linked to weather patterns. We argue that, to understand the cause for the patterns in the respective hemispheres, we must know the mechanism(s) driving population change and this must be linked to rigorous field tests. We suggest that a large-scale, year-round feeding experiment should improve overwintering survival, increase standing densities, and flip non-cyclic Myodes populations into cyclic dynamics that would mimic the patterns seen in the cyclic populations found in parts of Eurasia.

Stress responses play a key role in allowing animals to cope with change and challenge in the face of both environmental certainty and uncertainty. Measurement of glucocorticoid levels, key elements in the neuroendocrine stress axis, can give insight into an animal's well-being and can aid understanding ecological and evolutionary processes as well as conservation and management issues. We give an overview of the four main biological samples that have been utilized [blood, saliva, excreta (feces and urine), and integumentary structures (hair and feathers)], their advantages and disadvantages for use with wildlife, and some of the background and pitfalls that users must consider in interpreting their results. The matrix of choice will depend on the nature of the study and of the species, on whether one is examining the impact of acute versus chronic stressors, and on the degree of invasiveness that is possible or desirable. In some cases, more than one matrix can be measured to achieve the same ends. All require a significant degree of expertise, sometimes in obtaining the sample and always in extracting and analyzing the glucocorticoid or its metabolites. Glucocorticoid measurement is proving to be a powerful integrator of environmental stressors and of an animal's condition.

Predation is a central organizing process affecting populations and communities. Traditionally, ecologists have focused on the direct effects of predation--the killing of prey. However, predators also have significant sublethal effects on prey populations. We investigated how fluctuating predation risk affected the stress physiology of a cyclic population of snowshoe hares (Lepus americanus) in the Yukon, finding that they are extremely sensitive to the fluctuating risk of predation. In years of high predator numbers, hares had greater plasma cortisol levels at capture, greater fecal cortisol metabolite levels, a greater plasma cortisol response to a hormone challenge, a greater ability to mobilize energy and poorer body condition. These indices of stress had the same pattern within years, during the winter and over the breeding season when the hare:lynx ratio was lowest and the food availability the worst. Previously we have shown that predator-induced maternal stress lowers reproduction and compromises offspring's stress axis. We propose that predator-induced changes in hare stress physiology affect their demography through negative impacts on reproduction and that the low phase of cyclic populations may be the result of predator-induced maternal stress reducing the fitness of progeny. The hare population cycle has far reaching ramifications on predators, alternate prey, and vegetation. Thus, predation is the predominant organizing process for much of the North American boreal forest community, with its indirect signature--stress in hares--producing a pattern of hormonal changes that provides a sensitive reflection of fluctuating predator pressure that may have long-term demographic consequences.

Predator-induced changes in the glucocorticoid responses of prey have been proposed to mediate indirect predator effects on prey demography. Ambiguities exist, however, as to whether differences in predation threat in the environment at large affect the mean glucocorticoid response in wild birds and mammals, and whether this is likely to affect reproduction. Most studies to date that have examined glucocorticoid responses to environmental variation in predation threat have evaluated just one of the several potential measures of the glucocorticoid response, and this may be the source of many ambiguities. We evaluated multiple measures of the glucocorticoid response [plasma total CORTicosterone, corticosteroid binding globulin (CBG) and free CORT] in male and female song sparrows (Melospiza melodia) sampled at locations differing in predation threat in the environment at large, where we have previously reported reproductive differences suggestive of indirect predator effects. Total CORT varied markedly with predation threat in males but not females whereas the opposite was true for CBG, and both sexes demonstrated the same moderately significant free CORT response. Considering all three indices, a glucocorticoid response to environmental variation in predation threat was evident in both sexes, whereas there were ambiguities considering each index singly. We conclude that collecting multiple physiological measures and conducting multivariate analyses may provide a preferable means of assessing glucocorticoid responses to environmental variation in predation threat, and so help clarify whether such glucocorticoid changes affect reproduction in wild birds and mammals.

From 1987 to 1989 we monitored population changes during summer of the collared lemming (Dicrostonyx groenlandicus) and the tundra vole (Microtus oeconomus) at Pearce Point, Northwest Territories, Canada (69° 48' N, 122° 40' W). Populations on four study areas did not cycle but remained at low density (<3/ha) each year and continued at low numbers for the following 3 years (Reid et al. 1995). Lemming numbers often declined throghout the summer in spite of continous reproduction, and population recovery occurred overwinter. Heavy predation losses of radio-collared lemmings occurred each summer and this lemming population may be trapped in a predator-pit. Collared lemmings breed in winter and only because of winter population growth do these populations persist. Tundra vole numbers increased rapidly in most summers but usually declined overwinter. Tundra voles do not seem able to sustain winter reproduction in this extreme environment and this prevents them from reaching high density because of the short summer. Population growth in both these rodents could be prevented by poor food or by predation losses, and landscape patchiness may also help to prevent population growth. For lemmings we do not think that a shortage of shelter or intrinsic limitations could be restricting population increase at Pearce Point. This is the first detailed study of a non-cyclic collared lemming population.

We tested the hypothesis that populations composed of unrelated animals should perform worse than those composed of related animals by setting up two moderatedly dense field populations in adjacent enclosures: one was composed of related females and one of unrelated females; both had unrelated males. The survival and reproductive success of a number of litters located by spooling were determined. Final population size, pregnancy success, number of young recruited per pregnancy, and survival were similar in both populations. Thus, differences in relatedness produced no differences in demography. We conclude that the Charnov-Finerty Hypothesis in unlikely to be an explanation for microtine population fluctuations.

To test the hypothesis that the incidence of infanticide should increase as population density increases in microtines (Mallory and Brooks, 1978), an index of pregnancy success was developed. There was no negative correlation between population density and pregnancy success in four species of Microtus and thus the hypothesis is refuted. There was a positive correlation between instantaneous growth rate and pregnancy success in M. pennsylvanicus and M. townsendii.

Field evidence indicates that adult microtines, especially females, may be a major cause of poor juvenile survival and this may be instrumental in their population regulation. This suggests that males and females behave differently towards young animals. To examine how adult males, nonlactating females, and lactating females behave towards strange young, I introduced young animals into the home cage of the adults. Lactating females were most aggressive towards young; most males investigated them; most nonlactating females ignored them. However, discriminant function analysis indicated a great deal of overlap in the behavior of the classes. None of the classes behaved differently towards young of either sex. Females did not vary their behavior during lactation. Behavior varied among lactating females, with 55% showing little aggression and 20% showing a great deal. Most lactating females showed similar behavior in each of their bouts: docile females remained docile, aggressive females remained aggressive. I conclude that lactating females are most aggressive towards strange young. These results are consistent with the field evidence, which suggests that adult females depress juvenile survival and recruitment and that the main culprits are breeding females.