© 2004 by The Society for Integrative and Comparative Biology
| ||||||||||||||||||||||||||||||||||||||||||||||||||||
Coping with Changing Northern Environments: The Role of the Stress Axis in Birds and Mammals1
1 Department of Life Sciences, University of Toronto at Scarborough, Scarborough, Ontario M1C 1A4, Canada
 |
SYNOPSIS |
|---|
TOP
 SYNOPSIS INTRODUCTIONTHE STRESS RESPONSEADAPTATIONS FOR SURVIVING WINTERADAPTATIONS FOR REPRODUCING IN...IMPACTS OF HUMAN ACTIVITIES...CONCLUSIONS AND NEED FOR...References |
|---|
Northern environments present ecological and physiological problems for homeotherms that require adaptations to cope with severe and less predictable physical factors while at the same time continuing to have to cope with the biological ones, such as competition and predation. The stress axis plays a central role in these adaptations and I discuss the range of solutions that birds and mammals have evolved. The stress response in these animals is not static when a challenge occurs, but may be modulated depending on the biological function during the annual cycle (breeding versus nonbreeding), either under-responding to permit reproduction (some song birds) or responding vigorously, yet not having this compromise reproduction (Arctic ground squirrels). Both may trade off survival for reproduction. In contrast, the snowshoe hare shows the expected stress response to chronic high predation risk over 2–3 years: body resources are geared to survival and reproduction is inhibited. Two long term, persistent, and pervasive changes will confront northern birds and mammals in the 21st century: global change and persistent organochlorine pollutants (POPs). These may result in either adaptations or shifts in distribution and abundance. For the former, latitudinal variation in the stress axis may help song birds respond rapidly; population variation in the stress axis response is unknown in northern mammals and relatively sedentary mammals may be unable to shift their distribution rapidly to adjust major climate shifts. For the latter, the few POPs studies that have examined the stress axis indicate marked negative effects.
|
INTRODUCTION |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE STRESS RESPONSEADAPTATIONS FOR SURVIVING WINTERADAPTATIONS FOR REPRODUCING IN...IMPACTS OF HUMAN ACTIVITIES...CONCLUSIONS AND NEED FOR...References |
|---|
The severity and unpredictably of higher latitude and alpine habitats present special challenges to birds and mammals who live out some or all of their lives there. These habitats are characterized by short summers with a burst of primary productivity separated by long winters with permanent snow cover. Habitat has been regarded as the template that constrains and shapes the evolution of successful physiological and ecology strategies (Southwood, 1988
). Though it cannot be the sole determinant for any particular suite of traits, habitat clearly plays a central role. The neuroendocrine system is a major pathway that integrates environmental change and through which life history decisions to reproduce, to grow, or to put energy into storage are implemented in the face of environmental uncertainty. It is thus a critical component adapting organisms to northern habitats and should be under strong selection pressure to evolve successful strategies which may be unique to these environments (Finch and Rose, 1995).
The limbic system (dentate gyrus and hippocampus) and the hypothalamic-pituitary-adrenocortical axis (HPA) are pivotal components of the neuroendocrine system coordinating successful adaptation to habitat for three reasons. I refer to these two components together as the stress axis as they play an integrated role through regulation and feedback (Fig. 1) that is, depending on the situation, permissive, suppressive, or stimulatory (Sapolsky et al., 2000). First, the stress axis is a critical one involved in normal day-to-day activities associated with the diurnal cycle of waking such as increased locomotion, exploratory behavior, increased appetite, and food-seeking behavior (reviewed in McEwen et al., 1988; Wingfield and Romero, 2001). Second, the stress axis permits short-term adaptation to maintain survival in the face of acute, environmental stressors. The term "stress" tends to be a vague, inclusive one, but here I use it informally as the general state of stressors that provoke a stress response (Selye, 1971; Sapolsky, 2002). The stress response is that set of responses by birds and mammals to potentially harmful environmental challenges (stressors). This response can be rapid and short-term—the classic "flight or fight" syndrome—that takes seconds to minutes to develop and is a generalized response to a wide variety of stressors. The response can also play a role coordinating longer duration responses (minutes to hours)—the emergency life history stage—that involves an interruption of the life history cycle currently underway (e.g., reproduction) and redirects physiology and behavior toward survival (Wingfield et al., 1998). The stress response can be activated by environmental stressors such as bouts of severe weather (e.g., Romero et al., 2000), by physical stressors such as attacks by a conspecific or a predator (e.g., Girolami et al., 1996; Hirschenhauser et al., 2000), or by psychological stressors such as the fear of an imminent attack (e.g., Boonstra et al., 1998; Korte, 2001). Though I focus on the stress axis here, it is only one part of the stress response and other hormones, neurotransmitters, opioid peptides, cytokines and brain functions are also rapidly called into play (Sapolsky et al., 2000). Third, the axis is central to certain long-term evolutionary adaptations to particular ecological and habitat pressures such as those encountered in the north (e.g., Boonstra et al., 2001; Wingfield and Hunt, 2002). Reproduction or survival may be maximized by evolving a stress response that is modulated by under-responding to a stressor or that is sustained chronically in spite of its negative consequences.
|
My objective in this paper is to give an overview of what is known about how environment-dependent modifications of the stress axis and its response adapt birds and mammals to survive and succeed in northern environments. Thus I will not discuss aspects of the axis that are common to all environments. The topic of stress physiology and the brain is enormous and complex, ranging from the cellular and molecular to the whole organism. For greater detail, a number of comprehensive sources can be consulted (e.g., Silverin, 1998
; Sapolsky et al., 2000; McEwen, 2001; Wingfield and Romero, 2001). I focus on species that reproduce at higher latitudes (Arctic and boreal regions) and on those that overwinter at latitudes where snowfall characterizes winter habitats (temperate, boreal, and Arctic regions). I do this for three reasons. First, the physiological adaptations of well-studied species from lower-latitude regions (temperate and boreal) may have applicability to those living further north. Second, there is a paucity of endocrinological information on how the axis functions in many northern species, even those with wide distributional ranges, and we need to highlight this gap in knowledge and redress it. Much of what we know about how the axis functions normally and in response to stressors is based on a very limited subset of mammals, especially laboratory rodents, and a slightly larger subset of birds (Romero, 2002). Third, as global climate change and the movement of persistent organic pollutants is likely to have a dominant effect on the distribution and abundance of species in the north in the 21st century we need an understanding of the current adaptations of northern species and of their capacity for change. Finally, research on the HPA axis in natural populations of birds has been much more intensive than that in mammals, particularly in the north, and it is apparent that there is extensive variation amongst species in response to similar ecological problems: more than one solution appears to work. The research documenting this complexity has been the subject of a number of recent reviews (Silverin, 1998; Wingfield and Hunt, 2002; Wingfield and Silverin, 2002), and I will discuss only some of the broad patterns for this group. |
THE STRESS RESPONSE |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE STRESS RESPONSEADAPTATIONS FOR SURVIVING WINTERADAPTATIONS FOR REPRODUCING IN...IMPACTS OF HUMAN ACTIVITIES...CONCLUSIONS AND NEED FOR...References |
|---|
An external stressor sets off a rapid cascade of responses in vertebrates to deal with the threat and then to reestablish homeostasis (Sapolsky et al., 2000
). I will discuss the major changes that occur in stress axis of mammals (Fig. 1), though that in birds is similar (Harvey et al., 1984; Silverin, 1998). Within seconds of the stressor, the sympathetic nervous system causes the adrenal medulla to release catecholamines (epinephrine and norepinephrine) into the general circulation and the paraventricular nucleus (PVN) of the hypothalamus releases primarily corticotropic releasing hormone (CRH), but also arginine vasopressin (AVP), into the portal system. These cause the anterior pituitary to release adrenocorticotropic hormone (ACTH) into the general circulation. In response to the ACTH, the adrenal cortex releases glucocorticoids (GCs) within minutes into the general circulation. In birds and some small mammals (bats, voles, and mice) the primary GC is corticosterone and in other mammals it is cortisol or a mixture of cortisol and corticosterone (e.g., hares, squirrels, primates, ungulates). The response results in mobilizing and shunting of energy to muscles by stimulation of hepatic gluconeogenesis (the production of glucose) and away from peripheral tissues not needed for short-term survival. Cardiovascular tone is increased, immune function is stimulated, inflammatory response is suppressed, pain preception is blunted, reproductive physiology and behavior inhibited, feeding and appetite is decreased, and cognition is sharpened. Under conditions where the stressor is acute, GCs exert feedback at three levels in the brain (Fig. 1) to return the body back to pre-activation state. Key to this feedback are the intracellular GC receptors (MR—mineralocorticoid receptors and GR—GC receptors) in the critical brain areas (Fig. 1) (de Kloet et al., 1999).
The stress response and the homeostatic set-point are not fixed, species-dependent characteristics, but are modified by the annual pattern of life history changes, by development, by energy reserves, and by experience. First, over the annual cycle of northern homeotherms, the requirements of reproduction, migration, and coping with winter may require that the stress axis be modulated in different ways at different times to optimize reproduction, survival, or both in the face of environmental challenges. This modulation has been referred to as allostasis (i.e., achieving stability through change—McEwen and Wingfield, 2003). Challenges that are recurrent and predictable (e.g., intense, direct male-male aggression associated with the breeding or bouts of severe weather on the breeding grounds in spring), would, if the species did not evolve a modifying solution, inhibit reproduction. Neither basal GC concentrations nor the response to stressors remain constant over the annual cycle and changes in the two are not necessarily closely correlated (e.g., baseline concentrations may be high at some times, but response to a stressor dampened—for an overview, see Romero, 2002). This is consistent with the laboratory evidence that indicates that there is differential regulation of baseline and stress GC concentrations and that these may serve different physiological and ultimately ecological functions (de Kloet et al., 1999; Sapolsky et al., 2000).
Second, during the critical pre- and postnatal periods of development, maternal effects may alter the phenotype of the progeny (Bernardo, 1996; Mousseau and Fox, 1998). This can happen in both birds (Royle et al., 2001) and mammals (e.g., Festa-Bianchet et al., 2000). In mammals, the developing stress axis is particularly vulnerable to such early experiences and can result in life-long programming of the stress response and homeostatic control (Matthews, 2002). There is also an interplay between changes in the HPA axis and the reproductive axis, which will ultimately translate in to changes in adult fitness.
Third, experience may alter the HPA axis response. This axis functions well when the stressor is of short duration (minutes to hours); thereafter the pronounced negative, inhibitory effects of chronic stress start becoming evident and intensify. Laboratory evidence in rodents indicates that the ACTH response is desensitized when the animal is repeatedly exposed to certain types of stressors (e.g., cold exposure), but not to others (e.g., footshock—Aguilera, 1998) but that entirely new stressors continue to elicit a typical stress response. Under conditions where the stressor becomes chronic (days to months), the suppressive effects of GCs grade into inhibition (Fig. 1), with the resulting impacts being potentially deleterious, affecting long-term survival and fitness through infertility, impaired resistance to disease, and inhibition of growth. Chronic stress may have two long-lasting effects that cause animals to secrete higher GC concentrations than normal in response to ACTH. First, the hippocampus affects the response of the HPA to stressors by negative feedback regulation and chronic stress will reduce this regulation by causing a down regulation of GC receptors in the hippocampus, with the effect that GC concentrations rise (e.g., Webster and Cidlowski, 1994; Meyer et al., 2001). Second, chronic stress can cause adrenal hypertrophy, increasing the productive capacity of the adrenocortical tissue (Miller and Tyrrell, 1995), resulting in an enhanced production of GC.
Methods to assess the stress axis
There are three major methods to assess the status of the stress axis in natural populations. First, GC concentrations can be determined from different categories of animals before and after the application of a stressor and their concentrations compared (e.g., before and after hunting). The results allow between category comparisons, but this gives insight only into the overall potential impact of the stressor. Second, the urine or feces of animals can be collected in the field and concentrations of GC metabolites measured (e.g., Palme et al., 1997; Teskey-Gerstl et al., 2000; Wasser et al., 2000). This simple, noninvasive method gives an integrated index of what the animals were experiencing sometime prior to defecation. However, it may be a rough index if sex, rank, and individual identification are unknown. In addition, since GC concentrations show a pronounced circadian rhythm (Dallman et al., 1990), being highest at the onset of daily activity and the lowest at the end of it, concentrations will also be affected by when they are produced in the daily cycle. Since it is usually not possible to know over what period the feces or urine were produced, this may complicate the interpretation. As well, it may not be possible to know what an animal was experiencing during the period the urine or feces were being produced (i.e., was it stressed or not, and if so, for how long). This would increase variability among samples. Thus the results may only allow one to make general statements about the stress status of entire populations. However, detailed knowledge of the individuals producing the feces or urine (i.e., through knowledge of social status, behavior, sex, etc.), calibration of fecal levels with plasma levels, and standardization of collection techniques, mitigate these limitations (Creel et al., 2002).
Third, a challenge protocol uses a standardized stressor as an index of an animal's ability to respond to natural stressors. Two basic approaches have been used—a capture-challenge protocol and a hormonal-challenge protocol. The capture-challenge protocol uses the capture of the animal as the stressor and typically proceeds as follows. Within 3 min of capture, a baseline blood sample is taken. Timing is critical as the stress response is so rapid that GC concentrations may begin to increase within 3–5 min of capture (e.g., mammals—Seggie and Brown, 1974; birds—Schoech et al., 1991). Thereafter, serial bleeds are taken at regular intervals (e.g., 5, 10, 30, 60 min). This protocol has been preferentially used in birds (see Wingfield and Silverin, 2002) though it also been used in at least one mammal (e.g., Kenagy and Place, 2000). A modification of this protocol was used by Sapolsky (1983) who darted baboons from behind and used their response to the anesthetic as the standardized stressor.
The hormonal-challenge protocol uses a standardized set of injections of hormones or analogues of them that are part of the normal stress response and measures the animal's response over a series of blood samples. This protocol is particularly useful when the techniques of capture exceed the 3 min window and the animal is already stressed. This protocol results in an integrated picture of the animal's recent physiological past (days to weeks) while at the same time overriding the immediate stress response the animal was experiencing because of the effects of capture. It does this both by assessing the responsiveness of the brain to negative feedback back regulation and the capability of the adrenals to respond to a standardized ACTH injection. It typically involves two steps: the dexamethasone suppression test (Kalin et al., 1981) followed by the adrenocorticotropic hormone (ACTH) stimulation test. The dexamethasone suppression test is a method to assess whether the brain is registering high GC concentrations correctly. Dexamethasone is an artificial GC and when injected, negative feedback on the brain should occur, causing a reduced ACTH release from the pituitary, and thus reduced GC production from the adrenals. When dexamethasone resistance occurs (i.e., GC concentrations do not decline as much as expected), it may indicate the animal has been chronically stressed (e.g., Brooke et al., 1994; Hik et al., 2001). However, certain mammal species are naturally dexamethasone resistant (prairie voles— Taymans et al., 1997; e.g., red squirrels—Boonstra and McColl, 2000). The ACTH stimulation test is a method to probe the responsiveness of adrenals directly. When greater than normal GC production occurs, it may also indicate that the animal has been chronically stressed. This protocol, or modifications of it, has been successfully applied in a wide variety of species (e.g., deer—Smith and Bubenik, 1990; sparrows—Astheimer et al., 1994; hares—Boonstra et al., 1998; mockingbirds—Sims and Holberton, 2000).
|
ADAPTATIONS FOR SURVIVING WINTER |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE STRESS RESPONSEADAPTATIONS FOR SURVIVING WINTERADAPTATIONS FOR REPRODUCING IN...IMPACTS OF HUMAN ACTIVITIES...CONCLUSIONS AND NEED FOR...References |
|---|
The modulation of the stress response, either by up-regulating it or by suppressing it, may be crucial both to preparing for and to surviving winter. Since reproduction is usually restricted to the summer, evolutionary adaptations in winter focus on those that maximize survival. The principal threats to winter survival are starvation and low temperatures, both of which may be aggravated by high predation risk. Terrestrial homeotherms have evolved five major solutions to deal with these threats and the stress axis plays a role in some of these. Though chronically high GC concentrations are generally viewed as "bad" for birds and mammals, some of these winter adaptations result in chronically moderate GC concentrations, and thus are "good" for survival. However, the pattern is not consistent across all species or groups, particularly among birds, and suggests that there may be more than one evolutionary solution.
First, the majority of northern birds migrate to either tropical regions or to subarctic and northern temperate regions (over 120 species from the Arctic alone, including all passerines and shorebirds, Boyd and Madsen, 1997; Murray, 1998), though some are permanent residents (e.g., ravens, black-capped chickadees, snowy owls). Of the terrestrial mammals, migration is an option only for the larger ones—the barrenland caribou (Rangifer tarandus) and their principal predator, the wolf (Canus lupus), but these move only to the northern boreal forests (Klein, 1999). The rest of the mammals stay put. Second, decreased metabolic expenditure through hibernation is a strategy employed by chipmunks, ground squirrels, and marmots (Mrosovsky and Sherry, 1980; Nedergaard and Cannon, 1990), coupled with internal fat storage in the last two groups. Third, some birds and mammals cache food to survive winter (Smith and Reichman, 1984). In the northern birds, chickadees, jays, and nuthatches cache seeds and insects, particularly prior to winter. Both pikas in alpine regions and red squirrels in the boreal forest and chipmunks in both alpine and forest regions cache food. The former two species remain active throughout the winter (Obbard, 1987; Dearing, 1997), the latter hibernates and periodically aroses to eat (e.g., Humphries et al., 2001). Fourth, small mammals such as the lemmings, voles, shrews, and weasels require microclimate refugia under the snow to forage and survive and hibernators require significant snow depth to insulate them in their hibernacula. Snow depth may be a critical determinant of survival (e.g., Scott, 1993; Reid and Krebs, 1996; Hubbs and Boonstra, 1997) and subsequent reproduction (e.g., Karels and Boonstra, 2000). Early or delayed onset of snowfall in autumn, snow depth in winter (too much or too little), and delayed snow melt in spring may all be detrimental (Mihok and Schwartz, 1989). Global climate change may affect any or all of these, causing a disjunct between the onset of animal activity in spring and the onset of plant growth (Inouye et al., 2000). Fifth, there can be either a seasonal long-term increase or decrease in body mass and size, as is seen in northern mammals in winter (Ashton et al., 2000) or there can be a daily increase in body mass (fat) and a nightly loss, as is seen in northern wintering birds (Holberton et al., 1999). Bergmann's rule proposes that within a genus of endothermic vertebrates, larger species are found in cooler environments. Though this rule has generated a great deal of controversy, a recent analysis (Ashton et al., 2000) finds support for it in large mammals, but not in smaller ones such as voles and shrews. The latter actually loose weight as winter approaches and maintain low mass throughout winter. The explanation in the larger mammals may be related to heat conservation (larger volume:area ratios in larger individuals), but is more likely related to their greater fasting endurance (Millar and Hickling, 1990). The explanation in smaller mammals may be related to conserving energy by optimizing the minimum body mass required to survive winter. Below I discuss how the stress axis plays a role in some of these.
Migration
Preparation for migration and for winter requires a period of hyperphagia and a laying down of fat reserves (for a review, see Holberton et al., 1999). In birds (Wingfield and Silverin, 1986; Astheimer et al., 1992) and mammals (Dallman et al., 1993), GCs play a vital role in foraging behavior and hyperphagia, with low to moderate concentrations stimulating feeding behavior. Many species of migrating birds show increased baseline concentrations of GCs but a reduced stress response (e.g., O'Reilly and Wingfield, 1995; Ramenofsky et al., 1995). An adaptive explanation for this pattern is the migration modulation hypothesis (Holberton et al., 1996, 1999). It proposes that higher concentrations of baseline GCs are expressed prior to and during migration than at other times to facilitate migratory fattening, but that the stress response is dampened when challenged so that the negative, catabolic effects of high GCs on skeletal muscle do not occur; thus critical skeletal muscles are preserved for flight during migration. This hypothesis has been validated in some studies on birds (Fig. 2A, left panel) (e.g., Holberton et al., 1996; Piersma and Ramenofsky, 1998), but not others. In white-crowned sparrows (Romero et al., 1997), baseline levels were not elevated in fall migrants nor did they show much fattening (Fig. 2A, right panel). Their stress response was similar to that in winter birds. In contrast spring migrants did show both elevated corticosterone secretion and an increase in body fat and this is congruent with the hypothesis. Thus different strategies exist to cope with the same general problem.
|
Differences in energy demand among individuals and between populations may underlie variation in corticosterone secretion during migration as well. In the hermit thrush (Caltharus guttatus), a species breeding throughout the boreal forests of North America, migrating individuals in poorer, leaner condition had elevated baseline GC concentrations and a dampened stress response, whereas those in good condition had lower baseline GC concentrations and a normal stress response (Long and Holberton, 2004). A similar relationship between energetic condition and baseline corticosterone and/or adrenocortical response has been found in other studies (e.g., Jenni et al., 2000
; but see Piersma et al., 2000; Mizrahi et al., 2001). Between-year variation in condition may directly reflect differences in either severity of the environment or of food availability. The stress response of the spring migrating semipalmated plovers (Calidris pusilla), an Arctic breeding species, varied between two years (Mizrahi et al., 2001). Though there was no relationship between baseline GC concentrations and fat levels in either year, plovers were in poorer physical condition (lower fat levels) in the year they also showed a dampened stress response to capture (see also Marra and Holberton, 1998). This may indicate a response to protect the skeletal muscle from high GC concentrations (see also Jenni et al., 2000). Thus the modulation of the stress response is clearly occurring in migrating birds but not all respond in the same way and condition and fat levels may modify the response. Different migratory strategies and other physiological constraints may be the reason for these differences.
Foraging and maintenance of optimal body mass
In winter, food intake in birds and mammals needs to be geared to prevent starvation while at the same time maintaining an optimum body mass to permit rapid escape from predators. GC concentrations may be the critical link between the size of the fat reserves and either environmental severity or predation risk. I will focus first on adaptations in birds and then in mammals.
On days with fresh snowfall, GC concentrations were higher in dark-eyed juncos (Junco hyemalis) than on days without fresh snow and fat reserves increased after these snows (Rogers et al., 1993). In England, where winter conditions are milder, great tits (Parus major—a species closely related to North American chickadees) used the daily temperature as the proximate cue to assess how much fat to accumulate—the colder the day, the greater the fat accumulated for the coming night (Gosler, 2002). However, a previous study on this species indicated that these fat reserves were not maximized and represented a tradeoff between being fat enough to avoid starvation overnight and being light enough to escape predators such as the sparrow hawk (Accipiter nisus) during the day (Gosler et al., 1995).
Body reserves of small and mid-sized mammals that remain active in winter tend to be extremely low and unlikely to be a major energy source. Northern red-backed voles (Clethrionomys rutilus) from Alaska always had <1 g of fat, with the body mass in winter being only about 1–2% fat (Zuercher et al., 1999). Snowshoe hares (Lepus americanus) in winter also tend to have very low fat levels and are subjected to intense predation pressure for parts of the 10-year cycle (Krebs et al., 2001). In the southern Yukon in February, kidney fat (fat surrounding the kidneys, a prominent storage site) constituted a trivial 0.08% ± 0.008 (1 SE, N = 226) of body mass (Boonstra, unpublished). Hares in winter have only sufficient internal reserves to survive 2–4 days without feeding (Whittaker and Thomas, 1983). Thus the voles and hares must forage daily to sustain themselves. Small mammal species at higher latitudes are short lived and in general, highly seasonal breeders. Most live considerably less than one year and virtually no vole that breeds in one year is alive the next (Boonstra, 1994). Thus, the nonbreeding young from one summer must survive winter to become the breeding adult population of the next. Since the onset of aging processes occur with the onset of maturation (Kirkwood and Austad, 2000), the nonbreeding young require adaptations to delay aging during the winter nonbreeding period. Essentially, a significant part of their neuroendocrine system in winter has to be geared to enduring and surviving an environmentally challenging period to permit an opportunity to reproduce in the next breeding season. Most small mammal species living at northern latitudes maintain lower body mass during autumn and winter than they do in summer (e.g., Iverson and Turner, 1974; Hansson, 1990). In laboratory studies, Dark et al. (1983) found that meadow voles (Microtus pennsylvanicus) lost 20% of their body mass and consumed 30% less food under short photoperiods characteristic of winter conditions. This would reduce both the energy demands and the time needed to forage for it. This lower body mass presumably represents a physiological optimum for winter survival, as voles that are either too small or too large do not survive winter (Aars and Ims, 2002).
I suggest that this winter adaptation may represent the natural equivalent of the best method known to prevent aging in mammals and to extend life in the laboratory-caloric restriction. Caloric restriction, which markedly extends lifespan in laboratory rodents (Ramsey et al., 2000) but also in a wide variety of other species, simultaneously causes a moderate hyperadrenocorticism (Sabatino et al., 1991). Evidence suggests that the latter contributes to retarded aging process (Masoro, 2000). Field evidence in meadow voles (Fig. 2B) indicates that males during the breeding season maintain significantly lower levels of corticosterone than they do during the nonbreeding season, both at baseline concentrations and when stressed by a standardized protocol. Thus, these moderate levels of glucocorticoids during winter may be one of the adaptations that small mammal species have to survive this period.
Latitudinal gradients and severity of winter
Within a bird species, there may be a latitudinal gradient in HPA sensitivity to unpredictable environmental stressors: those populations wintering further north, where climate is inherently more challenging and less predictable, should exhibit a more pronounced stress response than those living in more stable environments (Rogers et al., 1993; Wingfield et al., 1993; Holberton and Able, 2000). This would allow them to respond more rapidly to stressors such as winter storms. Though there was no difference in baseline GC concentrations between juncos (Junco hyemalis) wintering in New York (more severe winters) and those wintering in Mississippi (mild winters), those in New York were fatter and showed a greater amplitude stress response (Holberton and Able, 2000).
Fasting
Prolonged natural fasting is an adaptation by some birds and mammals to periods when food is unavailable, either because it is in short supply or because feeding would disrupt activities of greater importance (e.g., hibernation, incubation, lactation of young, molting, defence of breeding females). The ability to suppress the stress response may permit fasting animals to utilize fat stores and spare protein by preventing the catabolic, protein-mobilizing effects of GCs. King penguins in the Antaractic can fast for up to 3–4 mo while incubating and molting (Cherel et al., 1988a; Cherel et al., 1988b). Polar bears (Stirling, 2002), Svalbard reindeer (R. t. platyrhynchus) (Pond, 1998), and Svalbard ptarmigan (Lagopus mutus hyperboreus) (Blix, 1989) rely on fat reserves as energy stores during the winter period. They first prepare for the fast by a hyperphagic phase in which body fat stores increase. They then adjust to long-term fasting by mobilizing the fat stores and sparing body proteins (Bernard et al., 2003). The details of natural fasting physiology have been well worked out in male king penguins (Cherel et al., 1988a,b) and these findings may indicate the pattern in other species. Fasting is characterized by three phases. During phases I and II, first glycogen stores and then lipid stores, respectively, are the sources for energy; concentrations of corticosterone, insulin, and thyroid hormone remain low. If the fast continues until lipid stores reach some critical lower limit, the birds enter phase III when protein is no longer spared. Corticosterone and glucagon concentrations now increase markedly, and because GCs promote protein mobilization, protein now becomes the main energy source. The net result is muscle wasting. The decline in body condition of polar bears in the western Hudson Bay near Churchill, Manitoba (Stirling and Derocher, 1993; Stirling et al., 1999) over the last decade owing to the effects of global warming may be indicative of animals approaching this muscle wasting phase. When the sea ice melts and the ability to hunt seals stops, polar bears in this region spend their summers on the shore and fast. Because the sea ice is melting earlier and freezing later, the bears must fast for a longer period than they are adapted to and hence condition is declining. This decline is associated with reduced female condition and declining natality (Derocher and Stirling, 1995).
|
ADAPTATIONS FOR REPRODUCING IN NORTHERN ENVIRONMENTS |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE STRESS RESPONSEADAPTATIONS FOR SURVIVING WINTERADAPTATIONS FOR REPRODUCING IN...IMPACTS OF HUMAN ACTIVITIES...CONCLUSIONS AND NEED FOR...References |
|---|
The necessity of reproduction during a short summer places critical demands on northern birds and mammals at a time when they may simultaneously have to deal with unpredictable contingencies such as severe weather or predators that may compromise the reproduction. I will give three examples of solutions that northern species have evolved to maximize their fitness. The first, of snowshoe hares experiencing the stressor of chronic high predation risk during the decline of the 10-year cycle, reinforces the conventional understanding of how the HPA axis normally works: when animals are subjected to a chronic stressor, reproduction is inhibited or reduced. The other two examples illustrate specific adaptations of the stress axis to get around the problem of potentially being chronically stressed and yet continuing to reproduce. Some Arctic breeding birds continue to reproduce by not responding to stressors that would normally cause a strong activation of the stress response and an inhibition of reproduction. In contrast, breeding male Arctic ground squirrels continue to reproduce in spite of the fact that they are chronically stressed by the intense intrasexual competition. In the first example, animals trade off reproduction for survival; in the latter two, they may trade off survival for reproduction.
Snowshoe hares exhibit 10-year population cycles throughout the boreal forests of North America and these cycles have been occurring for at least the last 300 years (Krebs et al., 2001). During the 2–3 year period of population declines, virtually every hare that dies is killed by a predator and all the physiological evidence indicates that during this time, they are chronically stressed by the high predator threat. Using the hormonal-challenge protocol, Boonstra et al. (1998) found that in contrast to the increase phase of the population cycle, hares during the decline phase had higher concentrations of free cortisol (Fig. 3), reduced GC binding capacity (CBG—a binding carrier protein in plasma is normally present in moderate concentrations and limits the amount of free GCs in circulation), reduced testosterone response, reduced body condition, reduced white blood cell count, increased overwinter body mass loss, and increased glucose mobilization (Fig. 3). The higher concentrations of glucose released in response to the ACTH injection in decline hares indicate that they are increasing liver production and storage of glucose as glycogen in response to chronic stress by enhancing the liver's capacity for gluconeogenesis (Miller and Tyrrell, 1995). This comes at the expense of peripheral tissues by decreasing their glucose uptake and utilization, by the release of gluconeogenic substrate from peripheral tissues, and by increasing protein breakdown and decreasing protein synthesis (Fig. 1). These responses are expected of an animal under chronic stress (Sapolsky, 2002) and thus hares have not evolved a modulation of HPA axis adaptation to meet the challenge of this recurrent stressor. Thus hares appear to be making the best of a bad situation, focusing all their energies on short-term survival. However, the cost appears to be a significant reduction in reproduction to <40% of that found in increase phase (7.0 young/female/summer during the decline versus 18.9 young/female/summer during the increase—Stefan and Krebs, 2001). Thus, an attack by a predator may be one environmental factor that always requires a complete mobilization of the "flight or fight" stress response and when the frequency or threat of these attacks reaches a certain threshold, continuous activation of the stress axis precipitates the typical negative effects of chronic stress. However, in contrast to the expectation of Selye (1971) that HPA exhaustion should be the ultimate end result of chronic stress, adrenal exhaustion was never observed.
|
Birds breeding at high latitudes or at high altitudes are confronted by having to reproduce during a short growing season while at the same time having to cope with a unpredictable environment which can produce severe spring storms. The normal reaction to such weather would be a stress response, focusing body resources on survival. However, this would inhibit reproduction. Wingfield (1994)
proposed that species breeding in such environments suppress the adrenocortical response to such acute stressors, thus enhancing their chances for reproductive success. Figure 4 gives evidence to support this hypothesis: within some species, more northernly breeding populations during the breeding season respond less to the capture-stress protocol than do populations breeding further south (Romero et al., 2000; Wingfield and Hunt, 2002). Recent evidence suggests that the modulation of the stress response may occur not only between populations, but also with individuals with the strength of the response being lowered when reproductive investment or effort is greatest (Holberton and Wingfield, 2003). However, the generality of this modulation is tempered by two findings. First, if environmental conditions become chronic, the normal stress response may become activated and reproduction is traded off for survival. Astheimer et al. (1995) found that in the Lapland longspurs (Calcarius lapponicus) at Toolik Lake, Alaska a prolonged snow storm caused nest and territory abandonment and those birds recaptured subsequently had greatly increased corticosterone concentrations relative to the same birds before the storm. Second, not all species living at high latitudes show a reduced stress response during the breeding season (Wingfield et al., 1995): some species such as the rock ptarmigan (Lagopus mutus) and red phalarope (Phalaropus fulicaria), when challenged with a capture-stress protocol, showed corticosterone concentrations that were similar to those of other species at lower latitudes (though the exact stage of breeding may not have been determined in these studies). The interpretation of the response to stressors during various phases of the annual breeding cycle of northern birds may be modulated by parental effort between and within the sexes, by concentrations of the GC binding capacity (CBG—see above), and by variation in the sensitivity the HPA axis at either the level of the brain or the adrenals (e.g., Romero et al., 1998; Wingfield and Hunt, 2002).
|
Arctic ground squirrels are found throughout the tundra and alpine areas of mainland Canada, into the boreal forests of northwestern Canada, and throughout Alaska (Karels and Boonstra, 2000
). They are obligate hibernators, emerging above ground from 7–8 months of hibernation in early to mid-April, with males appearing about 1–2 weeks before females. Mating is highly synchronous, with all females being bred within 2–3 weeks of emergence. During this time, males fight intensely for the opportunity to mate, with serious injuries such as loss of eyes and gaping head wounds being frequent. Breeding males show evidence of a hormonal system geared to maximizing the chances of reproductive success irrespective of its long-term survival costs: they have the highest concentration of free cortisol (Fig. 5), the lowest GC binding capacity, the poorest ability to respond to an antigen challenge (Fig. 5), and testosterone concentrations which go up, not down, when challenged by a stressor (Boonstra et al., 2001). Normally, a stressor causes an inhibition of the gonadal axis and thus testosterone levels should decline. In contrast these increasing testosterone levels when subjected to stressors suggest that male squirrels will not back down when fighting with other males, essentially "upping the ante," and this may result in their severe injuries. About half of these males disappear during or shortly after the breeding season. Thus HPA axis and the immune response of breeding males are severely compromised relative to males at other times. Similar life history constraints (a short breeding season and low between-year survival) may select for a similar adaptive stress response in other mammals (Boonstra and Boag, 1992).
|
|
IMPACTS OF HUMAN ACTIVITIES ON THE STRESS AXIS IN WILDLIFE |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE STRESS RESPONSEADAPTATIONS FOR SURVIVING WINTERADAPTATIONS FOR REPRODUCING IN...IMPACTS OF HUMAN ACTIVITIES...CONCLUSIONS AND NEED FOR...References |
|---|
Local and regional impacts
Birds and mammals may be either directly or indirectly stressed by the local and regional activities of humans. Depending on the duration and timing of these activities (during the animal's breeding versus nonbreeding season), these stressors may have individual or population consequences. Three examples highlight the potential for stressor impacts. First, snowmobiles in winter and ATVs (all terrain vehicles) in summer are major terrestrial modes of motorized transport in the north. Wildlife exposed to the noise of these machines may be stressed by them. Creel et al. (2002)
measured fecal GC concentrations in elk (Cervus elaphus) and wolves in U.S. national parks exposed to different levels of snowmobile activity (Fig. 6). Both elk and wolf populations had higher concentrations of fecal GCs in areas and at times of heavier snowmobile use. However, Creel et al. were not able to detect any negative impact on the population dynamics of these two species from the current levels of snowmobile activity.
|
Second, activities associated with logging (felling of trees and logging truck traffic) may stress animal populations living nearby. In nesting Northern spotted owls (Strix occidentalis), an endangered species in the Pacific northwest, fecal GC concentrations in males were positively correlated with these logging practices (Wasser et al., 1997
).
Third, hunting wild game is a major activity throughout the north. Hunting may cause short-term stresses to animals in the same way that a short-duration predator attack stresses prey and elicit a short-term, acute response. However, hunts that are of long duration, occurring over many hours or longer, or to which the animal has no natural equivalent (e.g., large predators being pursued as prey animals) may be deleterious and result in chronic stress. Cougars (Puma concolor) that had been repeatedly chased by dogs over a series of weeks as part of a "nonconsumptive hunting" strategy showed a diminished response to an ACTH challenge in comparison with control animals (Harlow et al., 1992), suggesting that they were suffering from the effects of chronic stress. One of the methods of hunting red deer in Britain (Bateson and Bradshaw, 1997) and moose in Sweden (Ball et al., 1997) has involved pursuit by dogs. Relative to red deer shot without the pursuit, those hunted with dogs had cortisol concentrations up to 70% higher, disruption of muscle tissue, exhaustion of glycogen reserves, and breakdown of red blood cells (Bateson and Bradshaw, 1997). The researchers estimated that up to 8% of the deer that succeeded in escaping the pursuing dogs subsequently died from the effects of the hunt. Thus in wildlife management related to hunting or to other human activities, care should be taken to avoid activities causing chronic or extreme stresses.
Global impacts
Two long term, persistent, and pervasive changes are affecting northern environments simultaneously: global climate change and contamination of virtually all natural habitats by chemicals of anthropogenic origin (e.g., persistent organochlorine pollutants [Goldman, 1997] such as PCBs, DDT, and hexachlorocyclohexanes; polynuclear aromatic hydrocarbons; heavy metals, artificial radionuclides). Both changes may affect or compromise the HPA axis of northern birds and mammals that may then cascade into population, community, and ecosystem effects.
Climate change
Over the last 100 years, the earth's climate has warmed approximately 0.6°C and this rate of increase is the most rapid of that seen in the last 1,000 years (Climate Change, 2001). Computer model projections indicate that relative to 1990, the temperature by 2100 will increase between 1.4 and 5.8°C. Organisms could respond to this warming by changes in physiology, behavior, and morphology, by changes in population density, by shifts in range distributions either poleward or upward in elevation, by changes in the timing of life history events such as migration or initiation of breeding, and by changes in gene frequencies (Hughes, 2000; Walther et al., 2002; Root et al., 2003). Animal and plant populations have already shown marked responses to this increase in global temperature. From a meta-analysis of a large number of species or groups of species (Parmesan and Yoye, 2003), range shifts averaging 6.1 km per decade over the last 50 years toward the poles (or meters per decade upward) and advancement of spring events averaging 2.3 days per decade were found. A similar analysis found that the average shifts in spring phenology (breeding or blooming) in temperate species was 5.1 days earlier in a decade (Root et al., 2003). Given the projections of a much larger increase in temperature this century relative to the previous one and that temperature increases will be exacerbated at high latitudes (Climate Change, 2001), northern species and their environments are likely to be under severe pressure. Shifts in range distribution will be more readily accomplished for the migratory bird species (Boyd and Madsen, 1997) and some mobile groups of mammals (e.g., caribou and hares, Klein, 1999). However for mammal species that are more sedentary (e.g., Arctic ground squirrels), the rapidity of global warming may preclude or delay significant dispersal to capitalize on these changes (Peters and Lovejoy, 1992).
From the standpoint of the HPA axis, the critical question is whether northern bird and mammal species have either the phenotypic plasticity, the genotypic variability, or both to adapt to the new reality of higher temperatures or greater unpredictability caused by global warming. Realé et al. (2003) show that both act to result in earlier reproduction in Yukon red squirrels in response to earlier springs. Depending on how changes in weather translate into changes in the environment that the animals experience, the HPA axis may have a role to play in permitting them to meet this new challenge. We do not know the answer to this for most species, though we have a greater insight on this in birds than in mammals. In birds, many species exhibit between-population variation over a latitudinal cline in responsiveness to standardized stressors at certain phases of the reproductive cycle (Wingfield and Romero, 2001; Wingfield and Hunt, 2002). This variation and their ability to move large distances rapidly, may allow them to respond quickly to changes in environmental conditions. For most northern mammals, there is a paucity of even baseline endocrinological information and all studies to date have focused on within-population variation in HPA responsiveness. For example, red squirrels have an enormous distributional range throughout the length and breadth of northern and western North America, yet have been subject to only one study on the stress axis in one area (Boonstra and McColl, 2000). As well, the stress axis may play no role to permit adaptation depending on the timing of climate-induced changes. For example, reduction in winter snow cover when Arctic ground squirrels are hibernating, may both reduce female overwinter survival in alpine areas (Gillis, 2003) and reduce female reproduction in the next breeding season in the boreal forest. Karels and Boonstra (2000) found that variation in winter snow cover acted as a density independent factor: low snow cover resulted in poorer condition of females at emergence from hibernation and reduced their weaning success in late spring-early summer. Thus changes in the HPA axis will be unlikey to help these animals cope with declining conditions if the latter occur during hibernation. Finally, since the smaller mammals are reasonably sedentary, coping with climate change will depend on the speed with which it occurs relative to their speed of dispersal.
Northern contaminants
The second major factor affecting the north is the transfer to these regions of large variety of anthropogenically produced substances. Canada has been trying to understand their distribution, movement, and impact for the past decade since initiating the Canadian Northern Contaminants Program in 1991 (de March et al., 1997; de Wit et al., 2003). Many of these contaminants may be endocrine disrupting compounds (EDC). These are exogenous substances or mixtures of them that alter the function(s) of the endocrine system and consequently causes adverse health effects in an intact organism and its progeny or populations (Lister and Van der Kraak, 2001). Their modes of action are incredibly complex and diverse, with some mimicking or inhibiting the actions of hormones through interaction with hormone receptors and mechanisms of action, others altering the synthesis of a hormone or its receptor, and others altering the rate of metabolism and/or excretion of a hormone (Norris, 2000).
The major focus of research up to the present time has been on the impacts of EDCs on reproductive dysfunction and related areas (Jimenez, 1997; Crews et al., 2000; Iguchi and Sato, 2000), with relatively little attention being directed toward understanding their impact on the HPA axis. I summarize some of this search. Throughout the north, PCBs are a widespread contaminant and bioaccumulate up the food chain (Kelly and Gobas, 2001). In the field, high body burdens of PCBs and of DDT are known to be correlated with adrenal hyperplasia, necrosis, and/or hyperadrenocortism (de March et al., 1997). In the laboratory, a number of contaminants have severe effects on the HPA axis. Repeated exposure of rats to PCBs cause elevated basal corticosterone concentrations (Miller et al., 1993). The mechanism may involve the GC receptor (GR, Fig. 1), a critical component in the regulation of the limbic system and the HPA axis (Fig. 1). Methylsulfonyl PCBs will bind to the GR (Fig. 1), competing for access to the binding site with the artificial GC, dexamethasone, and thus possibly also with natural GCs (Johansson et al., 1998). Thus blocking the GR could limit the stress response to a stressor. Hyperadrenocortism occurs in Baltic seal populations and this is possibly related to the high levels of PCBs and DDT they carry (Bergman, 1999). Dioxin (2,3,7,8-tetrachlorodibenzo-p-dioxin) is another widespread environmental contaminant found in the north (de March et al., 1997) and has severe effects on the HPA axis. In laboratory cynomolgus monkeys (Macaca fascicularis), it disrupted the HPA axis by increasing levels of CRH mRNA in the hypothalamus and by increasing cortisol concentrations in plasma (Shridhar et al., 2001). In rats, it results in altered blood concentrations of ACTH (Bestervelt et al., 1998) and of corticosterone (Gorski et al., 1988).
The impact of contaminants on the inability of an organism to respond successfully to environmental stressors may only become obvious when such a challenge occurs. Thus, simply examining baseline concentrations of GCs may not be enough. The only example I can find of this comes from fish. Norris (2000) found that in wild populations of brown trout (Salmo trutta) exposed to the heavy metals zinc and cadmium (cadmium acts as an EDC in vertebrates), baseline concentrations of cortisol did not differ between exposed animals and controls. However when both groups were challenged with a stressor, exposed fish were unable to reestablish homeostasis rapidly after removal of the stressor. Thus, imposing a challenge is an effective way to assess whether contaminants have compromised the ability of the HPA axis to respond. In summary, the stress axis is clearly vulnerable to EDCs but a great deal needs to be done in both the field and laboratory to assess their impact at both the individual and population level.
|
CONCLUSIONS AND NEED FOR FUTURE STUDY |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE STRESS RESPONSEADAPTATIONS FOR SURVIVING WINTERADAPTATIONS FOR REPRODUCING IN...IMPACTS OF HUMAN ACTIVITIES...CONCLUSIONS AND NEED FOR...References |
|---|
The goal of individuals is to maximize life-time reproductive fitness and the functioning of the stress axis is key to making this happen. Coping with change is a key requirement for survival and reproduction both from both a short-term, ecological perspective and a long-term, evolutionary perspective and the stress axis is a critical one in this process. It is multi-tasking throughout the life of birds and mammals, but is subject to modification and permanent change if environmental conditions dictate. There is tendency to think of this axis only in relation to the response of the body to short-term stressors, yet it plays a key role all the time—winter and summer, in and out of breeding condition—to both carry out the daily functions of living and to cope with environmental challenges. The overview of the various solutions that birds and mammals use to deal with northern challenges high light two things. First, we have only scratched the surface in our understanding of how the stress axis functions to equip homeotherms for life in the north, with that in birds being deeper than that in mammals. Thus the broad-scale patterns are only slowly emerging. Second, the degree to which these solutions are genotypic or phenotypic and thus able to respond to long-term, directional change such as global warming, is unknown and this may limit their ability to respond. Thus studies in natural populations examining the causes of variation in the stress axis and its response to challenges are needed.
|
ACKNOWLEDGMENTS |
|---|
The Natural Sciences and Engineering Research Council of Canada supported this research. I thank J. Barker, J. Castillo, Q. Fletcher, and two incisive reviewers for comments on the manuscript, Lily Lu for assistance with the radioimmunoassays on voles, A. Hubbs, R. Manzon and A. McGreal for help with livetrapping, and the Amherst Wildlife Foundation for permission to trap voles on their property.
|
FOOTNOTES |
|---|
1 From the Symposium Biology of the Canadian Arctic: A Crucible for Change in the 21st Century presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2003, at Toronto, Canada.
2 E-mail: boonstra{at}utsc.utoronto.ca
|
References |
|---|
|
TOP
SYNOPSISINTRODUCTIONTHE STRESS RESPONSEADAPTATIONS FOR SURVIVING WINTERADAPTATIONS FOR REPRODUCING IN...IMPACTS OF HUMAN ACTIVITIES...CONCLUSIONS AND NEED FOR...References |
|---|
Aars, J., and R. A. Ims. 2002. Intrinsic and climatic determinants of population demography: The winter dynamics of tundra voles. Ecology, 83:3449-3456.[Web of Science]
Aguilera, G. 1998. Corticotropin releasing hormone, receptor regulation and the stress response. Trends Endocrinol. Metab, 9:329-336.[CrossRef][Web of Science][Medline]
Ashton, K. G., M. C. Tracy, and A. de Queiroz. 2000. Is Bergmann's rule valid for mammals? Amer. Nat, 156:390-415.[CrossRef][Web of Science]
Astheimer, L. B., W. A. Buttemer, and J. C. Wingfield. 1992. Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scand, 23:355-365.[CrossRef]
Astheimer, L. B., W. A. Buttemer, and J. C. Wingfield. 1994. Gender and seasonal differences in the adrenocortical response to ACTH challenge in an arctic passerine, Zonotrichia leucophrys gambelii. Gen. Comp. Endocrinol, 94:33-43.[CrossRef][Web of Science][Medline]
Astheimer, L. B., W. A. Buttemer, and J. C. Wingfield. 1995. Seasonal and acute changes in adrenocortical responsiveness in an arctic-breeding bird. Horn. Behav, 29:442-457.
Ball, J. P., G. Ericsson, and K. Wallin. 1997. Climate changes, moose and their human predators. Ecol. Bull, 47:178-187.
Bateson, P., and E. L. Bradshaw. 1997. Physiological effects of hunting red deer (Cervus elaphus). Proc. R. Soc. London B, 264:1707-1714.[Medline]
Bergman, A. 1999. Health condition of the Baltic grey seal (Halichoerus grypus) during two decades—gynaecological healthy improvement but increased prevalence of colonic cancers. Acta Path. Micro. Immuno. Scand, 107:270-272.
Bernard, S. F., M.-A. Thil, and R. Groscolas. 2003. Lipolytic and metabolic response to glucagon in fasting king penguins: Phase II vs. phase III. Am. J. Physiol, 284:R444-R454.
Bernardo, J. 1996. Maternal effects in animal ecology. Amer. Zool, 36:83-105.
Bestervelt, L. L., J. A. Pitt, C. J. Nolan, Y. Cai, D. W. Piper, J. A. Dybowski, G. A. Dayharsh, and W. N. Piper. 1998. In vitro 2,3,7,8-tetrachlorodibenzo-dioxin interference with anterior pituitary hormone adrenocorticotropin. Toxicol. Sci, 44:107-115.
Blix, A. S. 1989. Arctic resignation: Winter dormancy without hypothermia. In A. Malan and B. Canguilhem (eds.), Life in the cold, pp. 117–119. Colloque Inserm/John Libbey, Lehwald, France.
Boonstra, R. 1994. Population cycles in microtines: The senescence hypothesis. Evol. Ecol, 8:196-219.[CrossRef]
Boonstra, R., and P. T. Boag. 1992. Spring declines in Microtus pennsylvanicus and the role of steroid hormones. J. Anim. Ecol, 61:339-352.[CrossRef]
Boonstra, R., D. Hik, G. R. Singleton, and A. Tinnikov. 1998. The impact of predator—induced stress on the snowshoe hare cycle. Ecol. Monog, 68:371-394.[CrossRef]
Boonstra, R., and C. J. McColl. 2000. Contrasting stress response of male Arctic ground squirrels and red squirrels. J. Exp. Zool, 286:390-404.[CrossRef][Web of Science][Medline]
Boonstra, R., C. J. McColl, and T. J. Karels. 2001. Reproduction at all costs: The adaptive stress response of male Arctic ground squirrels. Ecology, 82:1930-1946.[CrossRef][Web of Science]
Boyd, H., and J. Madsen. 1997. Impacts of global change on Arctic-breeding bird populations and migration. In W. C. Oechel (ed.), Global change and Arctic terrestrial ecosystems, pp. 201–217. Springer.
Brooke, S. M., A. M. d. Haas-Johnson, J. R. Kaplan, S. B. Manuck, and R. M. Sapolsky. 1994. Dexamethasone resistance among nonhuman primates associated with a selective decrease of glucocorticoid receptors in the hippocampus and a history of social instability. Neuroendocrinology, 60:134-140.[CrossRef][Web of Science][Medline]
Cherel, Y., J. Leloup, and Y. L. Maho. 1988a. Fasting in king penguin. II. Hormonal and metabolic changes during molt. Am. J. Physiol, 254:R178-R184.
Cherel, Y., J. P. Robin, O. Walch, H. Karmann, P. Netchitailo, and Y. L. Maho. 1988b. Fasting in king penguin. I. Hormonal and metabolic changes during breeding. Am. J. Physiol, 254:R170-R177.
Climate Change., 2001. Third assessment report of the intergovernmental panel on climate change IPCC (WG I & II). Cambridge University Press, Cambridge.
Creel, S., J. E. Fox, A. Hardy, J. Sands, B. Garrott, and R. O. Peterson. 2002. Snowmobile activity and glucocorticoid stress responses in wolves and elk. Cons. Biol, 16:809-814.[CrossRef]
Crews, D., E. Willingham, and J. K. Skipper. 2000. Endocrine disruptors: Present issues, future directions. Q. Rev. Biol, 75:243-259.[CrossRef][Medline]
Dallman, M. F., S. F. Akana, C. S. Cascio, D. N. Darlington, L. Jacobson, and N. Levin. 1990. Regulation of ACTH Secretion: Variations on a theme of B. Rec. Prog. Horm. Res, 43:113-173.
Dallman, M. F., A. M. Strack, S. F. Akana, M. J. Bradbury, E. S. Hanson, K. A. Scribner, and M. Smith. 1993. Feast and famine: Critical role of glucocorticoids with insulin in daily energy flow. Front. Neuroendocrinol, 14:303-47.[CrossRef][Web of Science][Medline]
Dark, J., I. Zucker, and G. N. Wade. 1983. Photoperiodic regulation of body mass, food intake, and reproduction in meadow voles. Am. J. Physiol, 245:R334-338.
Dearing, M. D. 1997. The function of haypiles of pikas (Ochotona princeps). J. Mammal, 78:1156-1163.[CrossRef]
de Kloet, E. R., M. S. Oitzl, and M. Joels. 1999. Stress and cognition: Are corticosteroids good or bad guys? Trends Neurosci, 22:422-426.[CrossRef][Web of Science][Medline]
de March, B. G. E., C. A. d. Wit, and D. C. G. Muir. 1997. Persistent organic pollutants. In A. M. A. Project (ed.), Arctic assessment report, pp. 183–372. Oslo, Norway.
Derocher, A. E., and I. Stirling. 1995. Temporal variations in reproduction and body mass of polar bears in western Hudson Bay. Can. J. Zool, 73:1657-1665.
de Wit, C. A., A. Fisk, K. Hobbs, D. Muir, G. Gabrielson, R. Kallenborn, M. Krahn, R. Norstrom, and J. Skaare. 2003. AMAP II persistent organic pollutants report. In A. T. F. C. A. de Wit, K. E. Hobbs, and D. C. G. Muir (ed.), AMAP assessment report II. Chr. Hendriksen & Son, Viborg. (In press).
Festa-Bianchet, M., J. T. Jorgenson, and D. Réale. 2000. Early development, adult mass, and reproductive success in bighorn sheep. Behav. Ecol, 11:633-639.
Finch, C. E., and M. R. Rose. 1995. Hormones and the physiological architecture of life history evolution. Q. Rev. Biol, 70:1-52.[CrossRef][Medline]
Girolami, L., G. Fontani, L. Lodi, and C. Lupo. 1996. Hippocampal cholineacetyl transferase activity, agonistic behavior and social stress in male rabbits. Behav. Proc, 36:77-84.
Gillis, E. A. 2003. Breeding dispersal, male malting tactics, and population dynamics of arctic ground squirrels. Ph.D. Thesis, University of British Columbia, Vancouver, B.C.
Goldman, L. R. 1997. New approaches for assessing the etiology and risks of developmental abnormalities from chemical exposure. Reprod. Toxicol, 11:443-451.[CrossRef][Web of Science][Medline]
Gorski, J. R., G. Muzi, L. W. Weber, D. W. Pereira, M. J. Iatropoulos, and K. Rozman. 1988. Elevated plasma corticosterone levels and histopathology of the adrenals and thymuses in 2,3,7,8-Tetrachlorodibenzo-p-dioxin in the rat. Toxicology, 53:19-32.[CrossRef][Web of Science][Medline]
Gosler, A. G. 2002. Strategy and constraint in the winter fattening response to temperature in the great tit Parus major. J. Anim. Ecol, 71:771-779.[CrossRef]
Gosler, A. G., J. J. D. Greenwood, and C. Perrins. 1995. Predation risk and the cost of being fat. Nature, 377:621-623.[CrossRef]
Hansson, L. 1990. Ultimate factors in the winter weight depression of small mammals. Mammalia, 54:397-404.
Harlow, H. J., F. G. Lindzey, W. D. V. Sickle, and W. A. Gern. 1992. Stress response of cougars to nonlethal pursuit by hunters. Can. J. Zool, 70:136-139.
Harvey, S., J. G. Phillips, A. Rees, and T. R. Hall. 1984. Stress and adrenal function. J. Exp. Zool, 232:633-645.[CrossRef][Web of Science][Medline]
Hik, D., C. J. McColl, and R. Boonstra. 2001. Why are Arctic ground squirrels more stressed in the boreal forest than in alpine meadows? Ecoscience, 8:275-288.[Web of Science]
Hirschenhauser, K., E. Mostl, B. Wallner, J. Dittami, and K. Kotrschal. 2000. Endocrine and behavioural responses of male greylag geese (Anser anser) to pairbond challenges during the reproductive season. Ethology, 106:63-77.[CrossRef]
Holberton, R. L., and K. P. Able. 2000. Differential migration and an endocrine response to stress in wintering dark-eyed juncos (Junco hyemalis). Proc. Roy. Soc. London B, 267:1889-1896.[Medline]
Holberton, R. L., P. P. Marra, and F. R. Moore. 1999. Endocrine aspects of physiological condition, weather and habitat quality in landbird migrants during the non-breeding period. In N. J. Adams and R. H. Slotow (eds.), Proc. 22nd International Ornithological Congress, pp. 847–866. BirdLife South Africa, Johannesburg, South Africa.
Holberton, R. L., J. D. Parrish, and J. C. Wingfield. 1996. Modulation of the adrenocortical stress response in Neotropical migrants during autumn migration. Auk, 113:558-564.[Web of Science]
Holberton, R. L., and J. C. Wingfield. 2003. Modulating the corticosterone stress response: A mechanism for balancing individual risk and reproductive success in Arctic-breeding sparrows? Auk, 120:1140-1150.[CrossRef][Web of Science]
Hubbs, A. H., and R. Boonstra. 1997. Population limitation in Arctic ground squirrels: Effects of food and predation. J. Anim. Ecol, 66:527-541.[CrossRef]
Hughes, L. 2000. Biological consequences of global warming: Is the signal already apparent? Trends Ecol. Evol, 15:56-61.[CrossRef][Medline]
Humphries, M. M., D. W. Thomas, and D. L. Kramer. 2001. Torpor and digestion in food-storing hiberators. Physiol. Biochem. Zool, 74:283-292.[CrossRef][Web of Science][Medline]
Iguchi, T., and T. Sato. 2000. Endocrine disruption and developmental abnormalities of female reproduction. Amer. Zool, 40:402-411.[CrossRef]
Inouye, D. W., B. Barr, K. B. Armitage, and B. D. Inouye. 2000. Climate change is affecting altitudinal migrants and hibernating species. PNAS, 97:1630-1633.
Iverson, S. L., and B. N. Turner. 1974. Winter weight dynamics in Microtus pennsylvanicus. Ecology, 55:1030-1041.[CrossRef][Web of Science]
Jenni, L., S. Jenni-Eiermann, F. Spina, and H. Schwabl. 2000. Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight. Amer. J. Physiol, 278:R1182-1189.
Jimenez, B. 1997. Environmental effects of endocrine disruptors and current methodologies for assessing wildlife health effects. Trends Anal. Chem, 16:596-606.[CrossRef]
Johansson, M., S. Nilsson, and B.-O. Lund. 1998. Interactions between methylsulfonyl PCBs and the glucocorticoid receptor. Environ. Health Perspect, 106:217-222.[Web of Science][Medline]
Kalin, N. H., R. M. Cohen, G. W. Kraemer, S. C. Risch, S. Shelton, M. Cohen, W. T. McKinney, and D. L. Murphy. 1981. The dexamethasone suppression test as a measure of hypothalamic-pituitary feedback sensitivity and its relationship to behavioral arousal. Neuroendocrinology, 32:92-95.[Web of Science][Medline]
Karels, T. J., and R. Boonstra. 2000. Concurrent density dependence and independence in populations of Arctic ground squirrels. Nature, 408:460-463.[CrossRef][Medline]
Kelly, B. C., and F. A. P. C. Gobas. 2001. Bioaccumulation of persistent organic pollutants in lichen-caribou-wolf food chains of Canada's central and western Arctic. Environ. Sci. Tech, 35:325-334.[Medline]
Kenagy, G. J., and N. J. Place. 2000. Seasonal changes in plasma glucocorticosteroids of free-living female yellow-pine chipmunks: Effects of reproduction and capture and handling. Gen. Comp. Endocrinol, 117:189-199.[CrossRef][Web of Science][Medline]
Kirkwood, T. B. L., and S. N. Austad. 2000. Why do we age? Nature, 408:233-238.[CrossRef][Medline]
Klein, D. R. 1999. The roles of climate and insularity in establishment and persistence of Rangifer tarundus populations in the high Arctic. Ecol. Bull, 47:96-104.
Korte, S. M. 2001. Corticosteroids in relation to fear, anxiety, and psychopathology. Neurosci. Biobehav. Rev, 2:117-142.
Krebs, C. J., R. Boonstra, S. Boutin, and A. R. E. Sinclair. 2001. What drives the ten-year cycle of snowshoe hares? Bioscience, 51:25-35.[CrossRef][Web of Science]
Lister, A. L., and G. J. Van der Kraak. 2001. Endocrine disruption: Why is it so complicated? Water Qual. Res. J. Canada, 36:175-190.
Long, J. A., and R. L. Holberton. 2004. Corticosterone secretion, energetic condition, and a test of the migration modulation hypothesis in a neotropical migrant, the hermit thrush. Auk 121. (In press).
Marra, P. P., and R. L. Holberton. 1998. Corticosterone levels as indicators of habitat quality: Effects of habitat segregation in a migratory bird during the non-breeding season. Oecologia, 116:284-292.[CrossRef][Web of Science]
Masoro, E. J. 2000. Caloric restriction and aging: An update. Exp. Gerontol, 35:299-305.[CrossRef][Web of Science][Medline]
Matthews, S. G. 2002. Early programming of the hypothalamo— pituitary—adrenal axis. Trends Endocrinol. Metab, 13:373-380.[CrossRef][Web of Science][Medline]
McEwen, B. S.(ed.) 2001. Coping with the environment: Neural and endocrine mechanisms. Oxford University Press, Inc, New York.
McEwen, B. S., R. W. Brinton, and R. M. Sapolsky. 1988. Glucocorticoid receptors and behavior: Implications for the stress response. Adv. Exp. Med. Biol, 245:35-45.[Medline]
McEwen, B. S., and J. C. Wingfield. 2003. The concept of allostasis in biology and biomedicine. Horm. Behav, 43:2-15.[CrossRef][Medline]
Meyer, U., M. v. Kampen, E. Isovich, G. Flugge, and E. Fuchs. 2001. Chronic psychossocial stress regulated the expression of both GR and Mr mRNA in the hippocampal formation of tree shrews. Hippocampus, 11:329-336.[CrossRef][Web of Science][Medline]
Mihok, S., and B. Schwartz. 1989. Anemia at the onset of winter in the meadow vole (Microtus pennsylvanicus). Comp. Biochem. Pysiol, 94:289-304.
Millar, J. S., and G. J. Hickling. 1990. Fasting endurance and the evolution of mammalian body size. Funct. Ecol, 4:5-12.
Miller, D. B., L. E. Gray, J. E. Andrews, R. W. Luebke, and R. J. Smialowicz. 1993. Repeated exposure to the polychlorinated biphenyl (Aroclor 1254) elevates the basal serum levels of corticosterone but does not affect the stress-induced rise. Toxicology, 81:217-222.[CrossRef][Web of Science][Medline]
Miller, W. L., and J. B. Tyrrell. 1995. The adrenal cortex. In P. Felig, J. D. Baxter, and L. A. Frohman (eds.), Endocrinology and metabolism, pp. 555–711. McGraw-Hill Inc., New York.
Mizrahi, D. S., R. L. Holberton, and J. S. A. Gauthreaux. 2001. Patterns of corticosterone secretion in migrating semipalmated sandpipers at a major spring stopover site. Auk, 79:79-91.[CrossRef]
Mousseau, T. A., and C. W. Fox. 1998. The adaptive significance of maternal effects. Trends Ecol. Evol, 13:403-407.[CrossRef]
Mrosovsky, N., and D. F. Sherry. 1980. Animal anorexias. Science, 207:837-842.
Murray, J. L. 1998. Ecological characteristics of the Arctic. In AMAP (ed.), AMAP assessment report: Arctic pollution issues: Arctic monitoring and assessment programme (AMAP), pp. 117–140. Oslo, Norway.
Nedergaard, H., and B. Cannon. 1990. Mammalian hibernation. Phil. Trans. Roy. Soc. London Ser. B, 326:669-685.
Norris, D. O. 2000. Endocrine disruptors of the stress axis in natural populations: How can we tell? Amer. Zool, 40:393-401.[CrossRef]
Obbard, M. E. 1987. Red squirrel. In M. Novak, J. A. Baker, M. E. Obbard, and B. Malloch (eds.), Wild furbearer management and conservation in North America, pp. 265–281. Ontario Trappers Association; Ministry of Natural Resources,Toronto, Ontario.
O'Reilly, K. M., and J. C. Wingfield. 1995. Spring and Autumn migration in Acrtic shorebirds: Same distance, different strategies. Amer. Zool, 35:222-233.
Palme, R., C. Bobia, S. Messman, and E. Mostl. 1997. Measuring faecal cortisol metabolites: A non-invasive tool to evaluate adrenocortical activity in mammals. Adv. Ethol, 33:27-46.
Parmesan, C., and G. Yoye. 2003. A globablly coherent fingerprint of climate change impacts across natural systems. Nature, 421:37-42.[CrossRef][Medline]
Peters, R. L., and T. E. Lovejoy. 1992. Global warming and biological diversity. Yale University Press, New Haven.
Piersma, T., and M. Ramenofsky. 1998. Long term decreases of corticosterone in captive migrant shorebirds that maintain seasonal mass and molt cycles. J. Avian Biol, 29:97-104.[CrossRef]
Piersma, T., J. Reneerkens, and M. Ramenofsky. 2000. Baseline corticosterone peaks in shorebirds with maximal energy stores for migration: A general preparatory mechanism for rapid behavioral and metabolic transitions? Gen. Comp. Endocrinol, 120:118-126.[CrossRef][Web of Science][Medline]
Pond, C. M. 1998. The fats of life. Cambridge University Press, Cambridge, UK.
Ramenofsky, M., T. Piersma, and J. Jukema. 1995. Plasma corticosterone in Bar-tailed Godwits at a major stop-over site during spring migration. Condor, 97:580-584.
Ramsey, J. J., M. E. Harper, and R. Weindruch. 2000. Restriction of energy intake, energy expenditure, and aging. Free Radical Biol. Med, 29:946-968.
Realé, D., A. G. McAdam, S. Boutin, and D. Berteaux. 2003. Genetic and plastic responses of a northern mammal to climate change. Proc. Roy. Soci. London B, 270:591-596.
Reid, D. G., and C. J. Krebs. 1996. Limitations to collared lemming population growth in winter. Can. J. Zool, 74:1284-1291.
Rogers, C. M., M. Ramenofsky, E. D. Ketterson, V. J. Nolan, and J. C. Wingfield. 1993. Plasma corticosterone, adrenal mass, winter weather, and season in nonbreeding populations of Dark-eyed Juncos (Junco hyemalis hyemalis). Auk, 110:279-285.
Romero, L. M. 2002. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen. Comp. Endocrinol, 128:1-24.[CrossRef][Web of Science][Medline]
Romero, L. M., M. Ramenofsky, and J. C. Wingfield. 1997. Season and migration alters the corticosterone response to capture and handling in an Arctic migrant, the White-crowned sparrow, Zonotrichia leucophyrys gambelli. Comp. Biochem. Physiol, 116:171-177.
Romero, L. M., J. M. Reed, and J. C. Wingfield. 2000. Effects of weather on corticosterone responses in wild free-living passerine birds. Gen. Comp. Endocrinol, 118:113-122.[CrossRef][Web of Science][Medline]
Romero, L. M., K. K. Soma, and J. C. Wingfield. 1998. Hypothalamic-pituitary-adrenal axis changes allow seasonal modulation of corticosterone in a bird. Amer. J. Physiol, 274:1338-1344.
Root, T. L., J. T. Price, K. R. Hall, S. H. Schneider, C. Rosenzweig, and J. A. Pounds. 2003. Fingerprints of global warming on wild animals and plants. Nature, 421:57-60.[CrossRef][Medline]
Royle, N. J., P. F. Surai, and I. R. Hartley. 2001. Maternally derived androgens and antioxidants in bird eggs: Complementary but opposing effects? Behav. Ecol, 12:381-385.
Sabatino, F., E. J. Masoro, C. A. McMahan, and R. W. Kuhn. 1991. Assessment of the role of the glucocorticoid system in aging processes and in the action of food restriction. J. Gerontol, 46:B171-8179.[Abstract]
Sapolsky, R. M. 1983. Individual differences in cortisol secretory patterns in the wild baboon: Role of negative feedback sensitivity. Endocrinology, 113:2263-2267.
Sapolsky, R. M. 2002. Endocrinology of the stress-response. In J. B. Becker, S. M. Breedlove, D. Crews, and M. M. McCarthy (eds.), Behavioral endocrinology, pp. 409–450. MIT Press, Cambridge.
Sapolsky, R. M., L. M. Romero, and A. U. Munck. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev, 21:55-89.
Schoech, S. J., R. L. Mumme, and M. C. Moore. 1991. Reproductive endocrinology and mechanisms of breeding inhibition in cooperatively breeding Florida srub jays (Aphelocoma c. coerulescens). Condor, 93:354-64.[CrossRef][Web of Science]
Scott, P. A. 1993. Relationship between the onset of winter and collared lemming abundance at Churchill, Manitoba, Canada: 1932–90. Arctic, 46:293-296.
Seggie, J. A., and G. M. Brown. 1974. Stress response patterns of plasma corticosterone, prolactin, and growth hormone in the rat, following handling or exposure to novel environment. Can. J. Physiol. Pharmacol, 53:629-637.
Selye, H. 1971. Hormones and resistance. J. Pharm. Sci, 60:1-28.[CrossRef][Web of Science][Medline]
Shridhar, S., A. Farley, R. L. Reid, W. G. Foster, and D. A. V. Vugt. 2001. The effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on corticotrophin-releasing hormone, arginine vasopressin, and pro-opiomelanocortin mrna levels in the hypothalamus of the Cynomolgus monkey. Toxicol. Sci, 63:181-188.
Silverin, B. 1998. Stress responses in birds. Poultry Avian Biol. Rev, 9:153-168.
Silverin, B., B. Arvidsson, and J. Wingfield. 1997. The adrenocortical responses to stress in breeding willow warblers Phylloscopus trochilus in Sweden: Effects of latitude and gender. Funct. Ecol, 11:376-384.[CrossRef]
Sims, C. G., and R. L. Holberton. 2000. Development of the corticosterone stress response in young mockingbirds, Mimus polyglottos. Gen. Comp. Endocrinol, 119:193-201.[CrossRef][Web of Science][Medline]
Smith, C. C., and O. J. Reichman. 1984. The evolution of food caching by birds and mammals. Ann. Rev. Ecol. Syst, 15:329-351.[CrossRef][Web of Science]
Smith, J. H., and G. A. Bubenik. 1990. Plasma concentrations of glucocorticoids in white-tailed deer: The effect of acute ACTH and dexamethasone administration. Can. J. Zool, 68:2123-2129.
Southwood, T. R. E. 1988. Tactics, strategies and templets. Oikos, 52:3-18.
Stefan, C. I., and C. J. Krebs. 2001. Reproductive changes in a cyclic population of snowshoe hares. Can. J. Zool, 79:2101-2108.[CrossRef]
Stirling, I. 2002. Polar bears and seals in the eastern Beaufort Sea and Amundsen Gulf: A synthesis of populations over three decades. Arctic, 55:(Suppl)59-76.
Stirling, I., and A. E. Derocher. 1993. Possible impacts of climatic warming on polar bears. Arctic, 46:240-245.[Web of Science]
Stirling, I., N. J. Lunn, and J. Iacozza. 1999. Long-term trends in the population ecology of polar bears in western Hudson Bay in relation to climatic change. Arctic, 52:294-306.
Taymans, S. E., A. C. Devries, M. B. Devries, R. J. Nelson, T. C. Friedman, M. Castro, S. Deterawadleigh, C. S. Carter, and G. P. Chrousos. 1997. The hypothalamic-pituitary-adrenal axis of prairie voles (Microtus ochrogaster): Evidence for target tissue glucocorticoid resistance. Gen. Comp. Endocrinol, 106:48-61.[CrossRef][Web of Science][Medline]
Teskey-Gerstl, A., E. Bamberg, T. Steineck, and R. Palme. 2000. Excretion of corticosteroids in urine and faeces of hares (Lepus europaeus). J. Comp. Physiol. B, 170:163-168.[CrossRef][Medline]
Walther, G.-R., E. Post, P. Convey, A. Menzel, C. Parmesan, T. J. C. Beebee, J.-M. Fromentin, O. Hoegh-Guldberg, and F. Bairlein. 2002. Ecological responses to recent climate change. Nature, 416:389-395.[CrossRef][Medline]
Wasser, S. K., K. Bevis, G. King, and E. Hanson. 1997. Non-invasive physiological measures of disturbance in the Northern spotted-owl. Cons. Biol, 11:1019-1022.[CrossRef]
Wasser, S. K., K. E. Hunt, J. L. Brown, K. Cooper, C. M. Crockett, U. Bechert, J. J. Millspaugh, S. Larson, and S. L. Monfort. 2000. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen. Comp. Endocrinol, 120:260-275.[CrossRef][Web of Science][Medline]
Webster, J. C., and J. A. Cidlowski. 1994. Downregulation of the glucocorticoid receptor: A mechanism for physiological adaptation to hormones. Ann. N. Y. Acad. Sci, 746:216-220.[Web of Science][Medline]
Whittaker, M. E., and V. G. Thomas. 1983. Seasonal levels of fat and protein reserves of snowshoe hares in Ontario. Can. J. Zool, 61:1339-1345.
Wingfield, J. C. 1994. Modulation of the adrenocortical response to stress in birds. In K. G. Davey, R. E. Peter, and S. S. Tobe (ed.), Perspectives in comparative endocrinology, pp. 520–528. National Research Council of Canada, Ottawa, Toronto.
Wingfield, J. C., P. Deviche, S. Sharbaugh, L. B. Astheimer, R. Holberton, R. Suydam, and K. Hunt. 1994. Seasonal changes of the adrenocortical responses to stress in redpolls, Acanthis flammea, in Alaska. J. Exp. Zool, 270:372-380.[CrossRef][Web of Science]
Wingfield, J. C., and K. E. Hunt. 2002. Arctic spring: Hormone-behavior interactions in a severe environment. Comp Biochem Physiol B, 132:275-286.[CrossRef][Medline]
Wingfield, J. C., D. L. Maney, C. W. Breuner, J. D. Jacobs, S. Lynn, M. Ramenofsky, and R. D. Richardson. 1998. Ecological bases of hormone-behavior interactions: The "emergency life history stage.". Amer. Zool, 38:191-206.
Wingfield, J. C., M. C. Moore, and D. S. Farner. 1993. Endocrine responses to inclement weather in naturally breeding populations of White-crowned sparrows, Zoootrichia leucophrys pugetensis. Auk, 100:56-62.
Wingfield, J. C., K. M. O'Reilly, and L. B. Astheimer. 1995. Modulation of the adrenocortical responses to acute stress in Arctic birds: A possible ecological basis. Amer. Zool, 35:285-294.
Wingfield, J. C., and L. M. Romero. 2001. Adrenocortical responses to stress and their modulation in free-living vertebrates. In B. S. McEwen (ed.), Coping with the environment: Neural and endocrine mechanisms, pp. 211–236. Oxford University Press, Inc, New York.
Wingfield, J. C., and B. Silverin. 1986. Effects of corticosterone on territorial behavior of free-living male song sparrows Melospiza melodia. Horm. Behav, 20:405-417.[CrossRef][Medline]
Wingfield, J. C., and B. Silverin. 2002. Ecophysiological studies of hormone-behavior relations in birds. Horm. Brain Behav, 2:587-647.
Zuercher, G. L., D. D. Roby, and E. A. Rexstad. 1999. Seasonal changes in body mass, composition, and organs of northern red backed voles in interior Alaska. J. Mammal, 80:443-459.[CrossRef]
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||