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

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

The Evolution of the Stress Axis in Ground Squirrels

The hypothalamic-pituitary-adrenal (HPA) axis, or stress axis, is a key physiological system that mediates the relationship of the organism with its environment. Because activation of the HPA axis mobilizes energy stores for immediate use, but sustained activation can have deleterious effects on survival, the HPA axis has been implicated in the tradeoff between reproduction and survival. In this thesis, I investigate whether there is an association between one life history trait, reproductive lifespan, and the functioning of the HPA axis as predicted by the “adaptive stress hypothesis”. The adaptive stress hypothesis predicts that species adopting life history strategies characterized by short lifespans and early reproduction should maximize the energy available for reproduction through high levels of circulating glucocorticoids caused by the dysregulation of the HPA axis in the breeding season, whereas those characterized by long lifespans and extended reproduction should maintain a functioning HPA axis with low levels of glucocorticoids throughout life. To test this hypothesis, I studied five species of ground squirrels that vary dramatically in male reproductive lifespan: arctic, Richardson’s, Columbian, thirteen-lined, and Franklin’s ground squirrels (Urocitellus parryii, U. richardsonii, U. columbianus, Ictidomys tridecemlineatus, and Poliocitellus franklinii). I used a stress profile to characterize the HPA axis of male ground squirrels immediately before and immediately after the breeding season. The stress profile included measures of plasma glucocorticoid concentrations, determinants of plasma glucocorticoid concentrations (corticosteroid binding globulin levels, adrenal sensitivity/capacity, negative feedback, and intrinsic restraint), and markers of the biological effects of glucocorticoids (energy mobilization, health, and immune function). Contrary to the adaptive stress hypothesis, I found no relationship between reproductive lifespan and postbreeding glucocorticoid levels. Species also varied significantly and unexpectedly in how determinants of glucocorticoid levels changed over the breeding season, and in how glucocorticoids levels translated into biological effects. I also observed unexpected patterns of individual variation within species. Thus, life history alone did not predict HPA axis functioning. My results suggest that the HPA axis is so flexible in its functioning, that we will need to adopt a much more detailed model of the HPA axis in order to fully understand the relationship between the HPA axis and life history variation.Ph

Effects of food addition on a population of grey jays

Grey jays (Perisoreus canadensis). in the southwest Yukon were provided with supplemental food on three study areas to study the effects of food on territoriality and foraging strategies. Territory sizes and overlap were measured in 1993 and 1994. Territories of food addition grids were 3 0% smaller than those on grids without access to added food. There was only slightly more overlap between territories on food addition grids compared to controls, and the difference was not statistically significant. Time spent foraging, the rate at which jays made caches, and the weights of jays were measured. These data were used to test four hypotheses about the factors that limit overwinter body masses of jays. Birds on food addition grids made three times as many caches as control birds in a similar amount of time spent foraging. In winter, grey jays with added food spent less time foraging, yet they were able to maintain higher body condition than control birds. These results were consistent with the hypothesis that overwinter weights are limited by both a food shortage and by costs associated with increasing weight. Seasonal trends in body condition differed between birds on food addition grids and those without supplemental food. Birds with added food were in better condition year round, and were able to increase in weight between summer and fall. Control birds lost weight between summer and fall, but then increased dramatically in winter. These different weight trends may represent different caching or cache retrieval strategies.Science, Faculty ofZoology, Department ofGraduat

Preparing for hibernation in ground squirrels: Adrenal androgen production in summer linked to environmental severity in winter

1. At high latitudes, evolutionary adaptations focus on those that maximize survival, with hibernation being a major one used by many smaller mammals. Typically, mammalian hibernators overwinter in sites that are approximate to 0 degrees C. However, in arctic regions, such sites do not exist, necessitating hibernation at sites well below 0 degrees C. Lipid, the normal fuel of most hibernators, may not provide sufficient glucose needed by certain tissues to permit survival, with muscle breakdown being required. Critical to enhancing muscle stores are high concentrations of anabolic androgens prior to hibernation when the gonads are inactive

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

ABSTRACT. The hypothalamic-pituitary-adrenal axis (stress axis) plays a central role in equipping mammals to succeed in the challenging environment of the boreal forest. Over the last 20 years, we have tackled a broad range of topics to understand how the stress axis functions in four key herbivore species. The central challenge for snowshoe hares is coping with their predators, whereas for the others, it is primarily coping with each other (especially during reproduction) and with their physical environment. Hares are severely stressed by their predators during the population decline. The predator threat causes major changes in the stress axis of hares and reduces their reproduction; in addition, acting through maternal programming, it is the most plausible explanation for the extended period of low numbers following the population decline. Arctic ground squirrel males have an intense breeding season for two to three weeks in early spring, after which many of them die. The functioning of their stress axis changes markedly and is key in meeting their energy demands during this period. In contrast, red-backed vole males, though also short-lived, breed repeatedly only in the summer of their life, and their stress axis shows no change in function. However, their reproductive effort negatively affects their long-term survival. Territorial red squirrels experience marked interannual fluctuations in their major food source (white spruce seed), resulting in major fluctuations in their densities and consequently in the intensity of territorial competition. Changes in the densities of red squirrels also alter maternal stress hormone levels, inducing adaptive plasticity in offspring postnatal growth rates that prepares offspring for the environment they will encounter at independence. To survive winter, red squirrels need to defend their territories year-round, and the basi

Life history and the ecology of stress: how do glucocorticoid hormones influence life‐history variation in animals?

Summary Glucocorticoids hormones (GCs) are intuitively important for mediation of age‐dependent vertebrate life‐history transitions through their effects on ontogeny alongside underpinning variation in life‐history traits and trade‐offs in vertebrates. These concepts largely derive from the ability of GCs to alter energy allocation, physiology and behaviour that influences key life‐history traits involving age‐specific life‐history transitions, reproduction and survival. Studies across vertebrates have shown that the neuroendocrine stress axis plays a role in the developmental processes that lead up to age‐specific early life‐history transitions. While environmental sensitivity of the stress axis allows for it to modulate the timing of these transitions within species, little is known as to how variation in stress axis function has been adapted to produce interspecific variation in the timing of life‐history transitions. Our assessment of the literature confirms that of previous reviews that there is only equivocal evidence for correlative or direct functional relationships between GCs and variation in reproduction and survival. We conclude that the relationships between GCs and life‐history traits are complex and general patterns cannot be easily discerned with current research approaches and experimental designs. We identify several future research directions including: (i) integration of proximate and ultimate measures, including longitudinal studies that measure effects of GCs on more than one life‐history trait or in multiple environmental contexts, to test explicit hypotheses about how GCs and life‐history variation are related and (ii) the measurement of additional factors that modulate the effects of GCs on life‐history traits (e.g. GC receptors and binding protein levels) to better infer neurendocrine stress axis actions. Conceptual models of HPA/I axis actions, such as allostatic load and reactive scope, to some extent explicitly predict the role of GCs in a life‐history context, but are descriptive in nature. We propose that GC effects on life‐history transitions, survival probabilities and fecundity can be modelled in existing quantitative demographic frameworks to improve our understanding of how GC variation influences life‐history evolution and GC‐mediated effects on population dynamics Lay Summar

Investigation of the Link between Per- and Polyfluoroalkyl Substances and Stress Biomarkers in Bottlenose Dolphins (Tursiops truncatus)

Bottlenose dolphins (Tursiops truncatus) are keystone and sentinel species in the world's oceans. We studied correlations between per- and polyfluoroalkyl substances (PFAS) and their stress axis. We investigated associations between plasma biomarkers of 12 different PFAS variants and three cortisol pools (total, bound, and free) in wild T. truncatus from estuarine waters of Charleston, South Carolina (n = 115) and Indian River Lagoon, Florida (n = 178) from 2003 to 2006, 2010-2013, and 2015. All PFAS and total cortisol levels for these dolphins were previously reported; bound cortisol levels and free cortisol calculations have not been previously reported. We tested null hypotheses that levels of each PFAS were not correlated with those of each cortisol pool. Free cortisol levels were lower when PFOS, PFOA, and PFHxS biomarker levels were higher, but free cortisol levels were higher when PFTriA was higher. Bound cortisol levels were higher when there were higher PFDA, PFDoDA, PFDS, PFTeA, and PFUnDA biomarkers. Total cortisol was higher when PFOA was lower, but total cortisol was higher when PFDA, PFDoDA, PFTeA, and PFTriA were higher. Additional analyses indicated sex and age trends, as well as heterogeneity of effects from the covariates carbon chain length and PFAS class. Although this is a cross-sectional observational study and, therefore, could reflect cortisol impacts on PFAS toxicokinetics, these correlations are suggestive that PFAS impacts the stress axis in T. truncatus. However, if PFAS do impact the stress axis of dolphins, it is specific to the chemical structure, and could affect the individual pools of cortisol differently. It is critical to conduct long-term studies on these dolphins and to compare them to populations that have no or little expose to PFAS

Social, not genetic, programming of development and stress physiology of a colonial seabird

International audiencePhenotypic differences often stem from genetic/maternal differences and/or early-life adaptations to local environmental conditions. In colonial animals, little is known on how variation in the social environment is embedded into individual phenotypes, nor what the consequences are on individual fitness. We conducted an experimental cross-fostering study on king penguins (Aptenodytes patagonicus), exchanging eggs among 134 pairs breeding in high-density (67 pairs) or low-density (67 pairs) areas of the same breeding colony. We investigated differences in parent and chick phenotypes and survival in relation to the density of their origin and foster environment. Adults breeding in colony areas of high density exhibited decreased resting behavior and increased aggression and vigilance, increased hypometabolism during incubation fasts, and more moderate CORT responses to chronic stressors (e.g., constant aggression by neighbors). Chick phenotypes were more influenced by the environment in which they were reared than their genetic/maternal origin. Chicks reared in high-density colonial environments showed enhanced weight gain and survival rates regardless of the density of their genetic parents' breeding areas. Our study experimentally shows advantages to breeding in colonial areas of higher breeder densities in king penguins, and highlights the importance of social settings in shaping phenotype expression in colonial seabirds.</div