The Dilemma of Foraging Herbivores: Dealing with Food and Fear

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

Equipped for Life in the Boreal Forest: The Role of the Stress Axis in Mammals

The hypothalamic-pituitary-adrenal axis (stress axis) plays a central role in equipping mammals to succeed in the challenging environment of the boreal forest. Over the last 20 years, we have tackled a broad range of topics to understand how the stress axis functions in four key herbivore species. The central challenge for snowshoe hares is coping with their predators, whereas for the others, it is primarily coping with each other (especially during reproduction) and with their physical environment. Hares are severely stressed by their predators during the population decline. The predator threat causes major changes in the stress axis of hares and reduces their reproduction; in addition, acting through maternal programming, it is the most plausible explanation for the extended period of low numbers following the population decline. Arctic ground squirrel males have an intense breeding season for two to three weeks in early spring, after which many of them die. The functioning of their stress axis changes markedly and is key in meeting their energy demands during this period. In contrast, red-backed vole males, though also short-lived, breed repeatedly only in the summer of their life, and their stress axis shows no change in function. However, their reproductive effort negatively affects their long-term survival. Territorial red squirrels experience marked interannual fluctuations in their major food source (white spruce seed), resulting in major fluctuations in their densities and consequently in the intensity of territorial competition. Changes in the densities of red squirrels also alter maternal stress hormone levels, inducing adaptive plasticity in offspring postnatal growth rates that prepares offspring for the environment they will encounter at independence. To survive winter, red squirrels need to defend their territories year-round, and the basis of this defense appears to be adrenal dehydroepiandrosterone, which has the benefits, but not the costs, of gonadal steroids. Arctic ground squirrels survive winter by hibernating in deeply frozen ground. Unlike all other hibernators, they have evolved a unique adaptation: high levels of adrenal androgens in summer to accumulate protein reserves that they then burn in winter. With a rapidly changing climate, the stress axis will play a key role in permitting northern animals to adapt, but the linkages between the changes in the abiotic and biotic components of the boreal forest and the phenotypic plasticity in the stress response of its inhabitants are not well understood for these or any other herbivore species.L’axe hypothalamo-hypophyso-surrénalien (l’axe du stress) joue un rôle central pour aider les mammifères à réussir dans l’environnement difficile de la forêt boréale. Ces 20 dernières années, nous nous sommes penchés sur une vaste gamme de sujets afin de comprendre comment fonctionne l’axe du stress chez quatre grandes espèces herbivores. Pour le lièvre d’Amérique, le défi central consiste à faire face à ses prédateurs, tandis que pour les autres espèces, ce défi consiste à se faire face mutuellement (surtout pendant la reproduction) de même qu’à faire face à leur environnement physique. Les lièvres subissent beaucoup de stress de la part de leurs prédateurs pendant la diminution de la population. La menace des prédateurs est la cause de changements majeurs sur l’axe du stress des lièvres, ce qui a pour effet de réduire leur reproduction. De plus, en raison de leur programmation maternelle, il s’agit de l’explication la plus plausible justifiant la période prolongée de leur faible nombre suivant la diminution de la population. Le spermophile arctique mâle a une période de reproduction intense pendant deux à trois semaines au début du printemps et après cela, un grand nombre d’entre eux meurent. Le fonctionnement de son axe de stress change de façon marquée, ce qui est essentiel à sa demande en énergie pendant cette période. Par contraste, le campagnol à dos roux mâle, même s’il ne vit également pas longtemps, se reproduit à répétition seulement pendant l’été de sa vie, et le fonctionnement de son axe de stress ne montre aucun changement. Cependant, ses efforts de reproduction ont des incidences négatives sur sa survie à long terme. Pour sa part, la principale source d’alimentation (les graines d’épinette blanche) de l’écureuil roux territorial connaît des fluctuations interannuelles marquées, ce qui se traduit par une fluctuation majeure en matière de densité de cette espèce animale et, par conséquent, en matière d’intensité de la concurrence pour le territoire. Les changements de densité d’écureuils roux exercent également une influence sur les taux d’hormone maternelle de stress, ce qui donne lieu à une plasticité adaptative des taux de croissance postnatale de la progéniture qui prépare la progéniture pour faire face à l’environnement dans lequel ils évolueront au stade de l’indépendance. Pour survivre à l’hiver, l’écureuil roux doit défendre son territoire à l’année et pour y parvenir, il se sert de la déhydroépiandrostérone surrénalienne, qui comporte les avantages des stéroïdes gonades, sans les coûts. Le spermophile arctique survit à l’hiver en hibernant dans le sol gelé en profondeur. Contrairement à tous les autres hibernateurs, il s’est développé une adaptation unique en son genre, soit des taux élevés d’androgènes surrénaliens en été qui lui permettent d’accumuler les réserves de protéines qu’il brûle ensuite pendant l’hiver. À la lumière du changement climatique rapide, l’axe de stress jouera un rôle-clé pour permettre aux animaux du Nord de s’adapter, mais les liens entre les changements des composantes abiotiques et biotiques de la forêt boréale et la plasticité phénotypique de la réaction de stress de ses habitants ne sont pas bien compris dans le cas de ces espèces herbivores ou de toute autre espèce herbivore

The Neurological Ecology of Fear: Insights Neuroscientists and Ecologists Have to Offer one Another

That the fear and stress of life-threatening experiences can leave an indelible trace on the brain is most clearly exemplified by post-traumatic stress disorder (PTSD). Many researchers studying the animal model of PTSD have adopted utilizing exposure to a predator as a life-threatening psychological stressor, to emulate the experience in humans, and the resulting body of literature has demonstrated numerous long-lasting neurological effects paralleling those in PTSD patients. Even though much more extreme, predator-induced fear and stress in animals in the wild was, until the 1990s, not thought to have any lasting effects, whereas recent experiments have demonstrated that the effects on free-living animals are sufficiently long-lasting to even affect reproduction, though the lasting neurological effects remain unexplored. We suggest neuroscientists and ecologists both have much to gain from collaborating in studying the neurological effects of predator-induced fear and stress in animals in the wild. We outline the approaches taken in the lab that appear most readily translatable to the field, and detail the advantages that studying animals in the wild can offer researchers investigating the “predator model of PTSD.

Stress triangle: do introduced predators exert indirect costs on native predators and prey?

Non-consumptive effects of predators on each other and on prey populations often exceed the effects of direct predation. These effects can arise from fear responses elevating glucocorticoid (GC) hormone levels (predator stress hypothesis) or from increased vigilance that reduces foraging efficiency and body condition (predator sensitive foraging hypothesis); both responses can lead to immunosuppression and increased parasite loads. Non-consumptive effects of invasive predators have been little studied, even though their direct impacts on local species are usually greater than those of their native counterparts. To address this issue, we explored the non-consumptive effects of the invasive red fox Vulpes vulpes on two native species in eastern Australia: a reptilian predator, the lace monitor Varanus varius and a marsupial, the ringtail possum Pseudocheirus peregrinus. In particular, we tested predictions derived from the above two hypotheses by comparing the basal glucocorticoid levels, foraging behaviour, body condition and haemoparasite loads of both native species in areas with and without fox suppression. Lace monitors showed no GC response or differences in haemoparasite loads but were more likely to trade safety for higher food rewards, and had higher body condition, in areas of fox suppression than in areas where foxes remained abundant. In contrast, ringtails showed no physiological or behavioural differences between fox-suppressed and control areas. Predator sensitive foraging is a non-consumptive cost for lace monitors in the presence of the fox and most likely represents a response to competition. The ringtail\u27s lack of response to the fox potentially represents complete naiveté or strong and rapid selection to the invasive predator. We suggest evolutionary responses are often overlooked in interactions between native and introduced species, but must be incorporated if we are to understand the suite of forces that shape community assembly and function in the wake of biological invasions

Trophic Dynamics of the Boreal Forests of the Kluane Region

The trophic dynamics of the Yukon boreal forest have been under investigation at the Kluane Lake Research Station since 1973. We monitored and conducted experiments on the major species in this ecosystem, except the large mammals (for logistic reasons). The central problem has been to determine the causes of the 9 – 10 year cycle of snowshoe hares, and to achieve this we carried out several large-scale experiments manipulating food supplies, predator pressure, and soil nutrient availability to test hypotheses that food, predation, or habitat quality regulate populations. The hare cycle is driven top-down by predators, and most hares die because they are killed by predators. Predators also cause stress in female hares, and the stress response seems to be responsible for the loss of reproductive potential in the decline and low phases of the hare cycle. Many of the specialist predators and some herbivores in this ecosystem fluctuate with the hare cycle. Arctic ground squirrels do, but red squirrels do not, being linked closely to white spruce seed masting years. Small rodents fluctuate in numbers in two patterns. Red-backed voles and four species of Microtus voles have a 3 – 4 year cycle that seems to be driven by food supplies and social behaviour. Deer mice, in contrast, have fluctuated dramatically in the 38 years we have monitored them, but not cyclically. White spruce seed production varies with temperature and rainfall, but was not affected by adding nutrients in fertilizer. Global warming and reduced hare browsing in the last 20 years have helped to increase the abundance of shrubs in these forests. It will be challenging to predict how this system will change as climatic warming proceeds, because even closely related species in the same trophic level respond differently to perturbations. We recommend continued monitoring of the major species in these boreal forests.La dynamique trophique de la forêt boréale du Yukon fait l’objet d’une étude à la station de recherche du lac Kluane depuis 1973. Nous avons fait des expériences et surveillé les espèces importantes de cet écosystème, sauf en ce qui a trait aux principaux mammifères (pour des raisons de logistique). Le problème central a consisté à déterminer les causes du cycle de 9 à 10 ans du lièvre d’Amérique. Pour ce faire, nous avons effectué plusieurs expériences à grande échelle dans le cadre desquelles nous avons manipulé les disponibilités alimentaires, la pression exercée par les prédateurs et la disponibilité en nutriments dans le sol afin de mettre à l’épreuve les hypothèses selon lesquelles la nourriture, la prédation ou la qualité de l’habitat régularisent les populations. Le cycle du lièvre est dicté par les prédateurs de haut en bas, et la plupart des lièvres meurent parce qu’ils sont tués par les prédateurs. Par ailleurs, les prédateurs sont une source de stress chez les lièvres femelles, et la réaction au stress semble responsable de la perte de capacité de reproduction dans la phase du déclin et la phase basse du cycle du lièvre. Grand nombre des prédateurs spécialistes et certains herbivores de cet écosystème fluctuent en fonction du cycle du lièvre. C’est le cas du spermophile arctique, mais ce n’est pas le cas de l’écureuil roux, car il est étroitement lié aux années de paisson de graines d’épinette blanche. Le nombre de petits rongeurs fluctue en fonction de deux modèles. Le campagnol à dos roux et quatre espèces de campagnols Microtus ont un cycle de trois à quatre ans qui semble dicté par les disponibilités alimentaires et le comportement social, tandis que la souris sylvestre a connu d’énormes fluctuations pendant les 38 années qui ont fait l’objet d’une surveillance, sans toutefois afficher de cycles. La production de graines d’épinette blanche varie en fonction des températures et des chutes de pluie, mais n’a pas été influencée par l’ajout de nutriments au fertilisant. Le réchauffement planétaire et le broutage réduit des lièvres ces 20 dernières années ont aidé à accroître l’abondance d’arbustes dans ces forêts. Il sera difficile de prévoir comment ce système changera au fur et à mesure du réchauffement climatique, car même les espèces étroitement liées du même niveau trophique réagissent aux perturbations de manière différente. Nous recommandons la surveillance continue des principales espèces de ces forêts boréales

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

Use of Acceleration and Acoustics to Classify Behavior, Generate Time Budgets, and Evaluate Responses to Moonlight in Free-Ranging Snowshoe Hares

Technological miniaturization is driving a biologging revolution that is producing detailed and sophisticated techniques of assessing individual behavioral responses to environmental conditions. Among the many advancements this revolution has brought is an ability to record behavioral responses of nocturnal, free-ranging species. Here, we combine captive validations of acceleration signatures with acoustic recordings from free-ranging individuals to classify behavior at two resolutions. Combining these classifications with ~2 month-long recordings, we describe winter time budgets, and responses of free-ranging snowshoe hares to changing moonlight. We successfully classified snowshoe hare behavior into four categories (not moving, foraging, hopping, and sprinting) using low frequency accelerometry, with an overall model accuracy of 88%, and acoustic recordings to three categories (silence, hopping, and chewing) with an accuracy of 94%. Broad-scale accelerometer-classified categories were composed of multiple fine-scale behavioral states with the composition varying between individuals and across the day. Time budgets revealed that hares spent ~50% of their time foraging and ~50% not moving, with most foraging and feeding occurring at night. We found that hares adjusted timing of activity in response to moon phase, with a 6% reduction in foraging and 30% reduction in traveling during the night when the moon was full. Hares compensated for this lost foraging time by extending foraging into the morning hours of the following day. Using two biologging technologies to identify behavior, we demonstrate the possibility of combining multiple devices when documenting behavior of cryptic species

Cyclic dynamics drive summer movement ecology of snowshoe hares (Lepus americanus)

Animals exhibit dynamic movement and activity in response to environmental variation including changes in reproductive opportunities, predation risk, or food availability. Yet, it remains unclear which factors are primary in affecting animal movement, and whether the relative importance of these factors are consistent through time. We tracked snowshoe hares (Lepus americanus) using GPS telemetry during eight summers spanning a hare population cycle (2015–2022) in southwestern Yukon, Canada, to determine associations between environmental variation and hare movement and home range size. Hare density varied 25-fold during the study and home range size increased markedly during low hare density, especially for males. Both sexes retained similar core space use and linearity of movements, but at low densities males had greater and more variable movement rates and time spent travelling. Trail cameras revealed that annual changes in hare movement were also correlated with relative abundance of lynx (Lynx canadensis) and coyotes (Canis latrans). However, hare detection rates within a season were not closely associated with seasonal variation in predator detection. Observed differences between male and female hares in some metrics highlighted that different life histories and reproductive behavior are likely the main drivers of hare movement dynamics. Therefore, fitness rewards associated with successful mate search and reproduction appear to outweigh risks associated with increased movement, even in highly variable environments where costs of prioritizing reproduction-related activities are notably high and variable

Demography of Microtus pennsylvanicus in southern Ontario: enumeration versus Jolly-Seber estimation compared

A meadow vole population near Toronto went through a cycle in numbers from July 1978 to May 1982. The population never reached a density less than 96 voles/ha or greater than 630 voles/ha. Jolly-Seber estimates differed from total enumeration counts by an average of 10.6% in population size and by less than 0.03 per 2 weeks in survival rates for almost all periods. Sharp spring declines occurred in both sexes in both the increase and the peak years, but only among females in the decline year. Dispersal occurred more frequently during the spring of the increase and peak than of the decline, was associated with maturation, and was biased towards males. The breeding season lasted 9 months in the increase and decline but only 5 months in the peak. Survival of adults during the decline summer was no different from that in other years. Survival of young during the increase and peak was moderately high, but was extremely poor during the decline. Since most young failed to be captured in either pitfalls or live-traps, I conclude that they died shortly before or after weaning and suggest that maternal condition was impaired by prior events in the peak and that this may apply to other cyclic microtine populations

Populations cycles in microtines: the senescence hypothesis

The cause of population cycles in microtines (voles and lemmings) remains an enigma. I propose a new solution to this problem based on a crucial feature of microtine biology, shifts in age structure, that has been ignored until now. Empirical evidence indicates that age structure must shift markedly toward older animals during declines because of three characteristics of the previous peak year: a shortened breeding season, total replacement of the breeding population from peak to decline, and density-dependent social inhibition of maturation of young. Declines become inevitable as populations composed of older animals survive and reproduce poorly because of the effects of senescence, possibly interacting with the experiences of peak density, and I present both theoretical and empirical evidence for this hypothesis. Though a variety of physiological systems deteriorate with aging, I focus on a crucial one - the inability of older animals to effectively maintain homeostasis in the face of environmental challenges because of a progressive deterioration in the endocrine feedback mechanisms involved in the hippocampal-hypothalamic-pituitary-adrenal axis. Microtine populations will not exhibit cycles where age structure shifts are prevented owing to extrinsic factors such as intense predation. Five testable predictions are made that can falsify this hypothesis