Rudy Boonstra

Impact of food and predation on the snowshoe hare cycle.

Snowshoe hare populations in the boreal forests of North America go through 10-year cycles. Supplemental food and mammalian predator abundance were manipulated in a factorial design on 1-square-kilometer areas for 8 years in the Yukon. Two blocks of forest were fertilized to test for nutrient effects. Predator exclosure doubled and food addition tripled hare density during the cyclic peak and decline. Predator exclosure combined with food addition increased density 11-fold. Added nutrients increased plant growth but not hare density. Food and predation together had a more than additive effect, which suggests that a three-trophic-level interaction generates hare cycles.

Measuring stress in wildlife: techniques for quantifying glucocorticoids

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.

The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares

1. Prey responses to high predation risk can be morphological or behavioural and ultimately come at the cost of survival, growth, body condition, or reproduction. These sub-lethal predator effects have been shown to be mediated by physiological stress. We tested the hypothesis that elevated glucocorticoid concentrations directly cause a decline in reproduction in individual free-ranging female snowshoe hares, Lepus americanus. We measured the cortisol concentration from each dam (using a faecal analysis enzyme immunoassay) and her reproductive output (litter size, offspring birth mass, offspring right hind foot (RHF) length) 30 h after birth. 2. In a natural monitoring study, we monitored hares during the first and second litter from the population peak (2006) to the second year of the decline (2008). We found that faecal cortisol metabolite (FCM) concentration in dams decreased 52% from the first to the second litter. From the first to the second litter, litter size increased 122%, offspring body mass increased 130%, and offspring RHF length increased 112%. Dam FCM concentrations were inversely related to litter size (r(2) = 0.19), to offspring birth mass (r(2) = 0.32), and to offspring RHF length (r(2) = 0.64). 3. In an experimental manipulation, we assigned wild-caught, pregnant hares to a control and a stressed group and held them in pens. Hares in the stressed group were exposed to a dog 1-2 min every other day before parturition to simulate high predation risk. At parturition, unsuccessful-stressed dams (those that failed to give birth to live young) and stressed dams had 837% and 214%, respectively, higher FCM concentrations than control dams. Of those females that gave birth, litter size was similar between control and stressed dams. However, offspring from stressed dams were 37% lighter and 16% smaller than offspring from control dams. Increasing FCM concentration in dams caused the decline of offspring body mass (r(2) = 0.57) and RHF (r(2) = 0.52). 4. This is the first study in a free-ranging population of mammals to show that elevated, predator-induced, glucocorticoid concentrations in individual dams caused a decline in their reproductive output measured both by number and quality of offspring. Thus, we provide evidence that any stressor, not just predation, which increases glucocorticoid concentrations will result in a decrease in reproductive output.

What Drives the 10-year Cycle of Snowshoe Hares?

n 1831 the manager of a Hudson’s Bay Company post in northern Ontario wrote to the head office in London. The local Ojibway Indians were starving, he reported, because of a scarcity of “rabbits,” and they were unable to trap for furs because they spent all their time fishing for food (Winterhalder 1980). These shortages of so-called rabbits, which apparently occurred approximately every 10 years, are regularly mentioned in Canadian historical documents from the 18th and 19th centuries. Those rabbits were in fact snowshoe hares (Lepus americanus), and their 10-year cycle is one of the most intriguing features of the ecology of the boreal forest. Ten-year cycles were first analyzed quantitatively when wildlife biologists began to plot the fur trading records of Hudson’s Bay Company during the early 1900s. The Hudson’s Bay Company, established in 1671, kept meticulous records of the numbers of furs traded from different posts spread across Canada. The most famous time series drawn together from those records was that of Canada lynx (Elton and Nicholson 1942; Figure 1). The lynx is a specialist predator of snowshoe hares, and the rise and fall in lynx numbers mirrors, with a slight time lag, the rise and fall of snowshoe hare populations across the boreal region. The spectacular cycles of snowshoe hares and their predators have captured the attention of biologists as well as historians. These cycles are highlighted in virtually all ecology texts and are often cited as one of the few examples of Lotka-Volterra predator‐prey equations, a simple model which shows never-ending oscillations in the numbers of predators and their prey. Cycles seem to violate the implicit assumption of many ecologists that there is a balance in nature, and anyone living in the boreal forest would be hard pressed to recognize a balance among the boom and bust in nature’s economy. The challenge to biologists has been to understand the mechanisms behind these cycles, which has not been easy. One cycle lasts 10 years, and few PhD students or researchers wish to take 10 years to obtain n = 1. Fortunately,

Balancing food and predator pressure induces chronic stress in songbirds

The never–ending tension between finding food and avoiding predators may be the most universal natural stressor wild animals experience. The ‘chronic stress’ hypothesis predicts: (i) an animals stress profile will be a simultaneous function of food and predator pressures given the aforesaid tension; and (ii) these inseparable effects on physiology will produce inseparable effects on demography because of the resulting adverse health effects. This hypothesis was originally proposed to explain synergistic (inseparable) food and predator effects on demography in snowshoe hares (Lepus americanus). We conducted a 2 × 2, manipulative food addition plus natural predator reduction experiment on song sparrows (Melospiza melodia) that was, to our knowledge, the first to demonstrate comparable synergistic effects in a bird: added food and lower predator pressure in combination produced an increase in annual reproductive success almost double that expected from an additive model. Here we report the predicted simultaneous food and predator effects on measures of chronic stress in the context of the same experiment: birds at unfed, high predator pressure (HPP) sites had the highest stress levels; those at either unfed or HPP sites showed intermediate levels; and fed birds at low predator pressure sites had the lowest stress levels.

Reality as the leading cause of stress: rethinking the impact of chronic stress in nature

Summary Chronic activation of the stress axis caused by long-term uncontrollable and unpredictable factors in the environment has been regarded as causing maladaptive and/or pathological effects, both by those studying animals in the laboratory and in nature. While pathology may apply to the former, I argue that it does not apply to the latter. Our thinking on the role of chronic stress in animals in nature has been heavily influenced by biomedical research, but much less so by the ecological and evolutionary context within which animals actually function. I argue that when such stressors occur (e.g. periods of high predation risk, food limitation, prolonged severe weather, social conflict, etc.), although the animal may be chronically stressed, its responses are adaptive and continue to promote fitness. Chronic stressors in nature can be subdivided into whether they are reactive (direct physiological challenges threatening homeostasis and not requiring cognitive processing – for example, food limitation) or anticipatory (perceived to be threatening and requiring cognitive processing – for example, high predation risk). For anticipatory stressors, their impact on the animal should not be based on their absolute duration (they may be acute), but rather by the duration of their physiological consequences. The anticipatory stressor of persistent high predation risk does not elicit chronic stress in all prey classes. Cyclic snowshoe hare and arctic ground squirrels exhibit evidence of chronic stress when predator numbers are high, but cyclic vole and noncyclic elk populations do not. I suggest that chronic stress has evolved to benefit the fitness of the former and not the later, with the key factors being lifespan and life history. I propose that chronic stress evolves in a species only if it is adaptive.

POPULATION CYCLES IN SMALL MAMMALS: THE PROBLEM OF EXPLAINING THE LOW PHASE

Cycles characterize the demography of many populations of microtine rodents and snowshoe hares. A phase of low numbers often follows the decline and introduces a lag that lengthens the cycle. This low can last 1–3 yr in microtines and 2–4 yr in hares. Understanding the low phase is critical in explaining population cycles. Two major classes of hypotheses try to account for the low phase. The first proposes that something may be “wrong” with the extrinsic environment. The most promising of these extrinsic explanations is that predation, acting either directly or indirectly, has delayed density-dependent effects on prey populations during the low phase. The second class of hypotheses proposes that something may be “wrong” with the animals themselves. The most likely intrinsic factors are maternal effects or age effects on fitness during the low phase. Experimental tests for each of these sets of hypotheses are needed, and we suggest replicated experiments on focal species in two continents to resolve these ...

Population changes of the vertebrate community during a snowshoe hare cycle in Canada’s boreal forest

We measured the density changes of 22 species of vertebrates during a snowshoe cycle in northern Canada. Hares were the dominant herbivore in the system and changes in their numbers were correlated with changes in numbers of arctic ground squirrel, spruce grouse, ptarmigan, lynx, coyote, great horned owl, goshawk, raven and hawk owl. Hare numbers were not correlated with numbers of red-backed vole which showed peaks during the low, increase, and early decline phases of the hare cycle. Hawk owls were the only predator whose numbers correlated with changes in red-backed voles while boreal owls and weasels were correlated with densities of Microtus. Red squirrel, American kestrel, red-tailed hawk, northern harrier, wolverine, magpie, and gray jay showed no correlation with hare or vole numbers. We conclude that species in the boreal forests of Canada do not exhibit the strong synchrony found between voles and other members of the vertebrate community in northern Fennoscandia. We discuss some of the possible reasons for these differences.

EQUIPPED FOR LIFE: THE ADAPTIVE ROLE OF THE STRESS AXIS IN MALE MAMMALS

Abstract Habitat constrains and shapes successful ecological and physiological strategies and thus provides the context for the evolution of life-history traits. The stress axis plays a vital role in the endocrine system and is a critical component adapting mammals to particular habitat pressures. It is subject to both individual activational and organizational plasticity as well as to evolutionary modification. To illustrate, I examine the suite of traits of the stress axis associated with breeding frequency in male mammals, which varies in a continuum from semelparity to iteroparity. During the breeding season, males in species at the semelparous end of the continuum exhibit high concentrations of free corticosteroids, low concentrations of glucocorticoid-binding protein, a failure of the negative feedback system, a gonadal axis that is not inhibited by high corticosteroid concentrations, and immunosuppression. Iteroparous species exhibit the opposite traits. The evolutionary constraints selecting for the former may partially be related to phylogeny (in marsupials) as well as to an interaction of the restrictions imposed by the environment on female reproduction, the mating system, the high costs of reproduction, and the low adult survival during the nonbreeding season.

Population cycles in microtines: The senescence hypothesis

SummaryThe 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 towards 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. Although 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. Six testable predictions are made that can falsify this hypothesis.