Molly J. Dickens

The Reactive Scope Model - a new model integrating homeostasis, allostasis, and stress.

Allostasis, the concept of maintaining stability through change, has been proposed as a term and a model to replace the ambiguous term of stress, the concept of adequately or inadequately coping with threatening or unpredictable environmental stimuli. However, both the term allostasis and its underlying model have generated criticism. Here we propose the Reactive Scope Model, an alternate graphical model that builds on the strengths of allostasis and traditional concepts of stress yet addresses many of the criticisms. The basic model proposes divergent effects in four ranges for the concentrations or levels of various physiological mediators involved in responding to stress. (1) Predictive Homeostasis is the range encompassing circadian and seasonal variation - the concentrations/levels needed to respond to predictable environmental changes. (2) Reactive Homeostasis is the range of the mediator needed to respond to unpredictable or threatening environmental changes. Together, Predictive and Reactive Homeostasis comprise the normal reactive scope of the mediator for that individual. Concentrations/levels above the Reactive Homeostasis range is (3) Homeostatic Overload, and concentrations/levels below the Predictive Homeostasis range is (4) Homeostatic Failure. These two ranges represent concentrations/levels with pathological effects and are not compatible with long-term (Homeostatic Overload) or short-term (Homeostatic Failure) health. Wear and tear is the concept that there is a cost to maintaining physiological systems in the Reactive Homeostasis range, so that over time these systems gradually lose their ability to counteract threatening and unpredictable stimuli. Wear and tear can be modeled by a decrease in the threshold between Reactive Homeostasis and Homeostatic Overload, i.e. a decrease in reactive scope. This basic model can then be modified by altering the threshold between Reactive Homeostasis and Homeostatic Overload to help understand how an individuals response to environmental stressors can differ depending upon factors such as prior stressors, dominance status, and early life experience. We illustrate the benefits of the Reactive Scope Model and contrast it with the traditional model and with allostasis in the context of chronic malnutrition, changes in social status, and changes in stress responses due to early life experiences. The Reactive Scope Model, as an extension of allostasis, should be useful to both biomedical researchers studying laboratory animals and humans, as well as ecologists studying stress in free-living animals.

Stress and translocation: alterations in the stress physiology of translocated birds

Translocation and reintroduction have become major conservation actions in attempts to create self-sustaining wild populations of threatened species. However, avian translocations have a high failure rate and causes for failure are poorly understood. While ‘stress’ is often cited as an important factor in translocation failure, empirical evidence of physiological stress is lacking. Here we show that experimental translocation leads to changes in the physiological stress response in chukar partridge, Alectoris chukar. We found that capture alone significantly decreased the acute glucocorticoid (corticosterone, CORT) response, but adding exposure to captivity and transport further altered the stress response axis (the hypothalamic–pituitary–adrenal axis) as evident from a decreased sensitivity of the negative feedback system. Animals that were exposed to the entire translocation procedure, in addition to the reduced acute stress response and disrupted negative feedback, had significantly lower baseline CORT concentrations and significantly reduced body weight. These data indicate that translocation alters stress physiology and that chronic stress is potentially a major factor in translocation failure. Under current practices, the restoration of threatened species through translocation may unwittingly depend on the success of chronically stressed individuals. This conclusion emphasizes the need for understanding and alleviating translocation-induced chronic stress in order to use most effectively this important conservation tool.

Chronic Stress Alters Glucocorticoid Receptor and Mineralocorticoid Receptor mRNA Expression in the European Starling (Sturnus vulgaris) Brain

Although the glucocorticoid response to acute short‐term stress is an adaptive physiological mechanism that aids in the response to and survival of noxious stimuli, chronic stress is associated with a negative impact on health. In wild‐caught European starlings (Sturnus vulgaris), chronic stress alters the responsiveness of hypothalamic‐pituitary‐adrenal (HPA) axis as measured by the acute corticosterone response. In the present study, we investigated potential underlying neuroendocrine mechanisms by comparing glucocorticoid receptor and mineralocorticoid receptor mRNA expression in the brains of chronically and nonchronically‐stressed starlings. Hypothalamic paraventricular nucleus, but not hippocampal, glucocorticoid receptor mRNA expression in chronically‐stressed birds was significantly lower compared to controls, suggesting changes in the efficacy of corticosterone negative feedback. In addition, chronically‐stressed birds showed a significant decrease in hippocampal MR mRNA expression. Together, these results suggest that chronic stress changes the brain physiology of wild birds and provides important information for the understanding of the underlying mechanisms that result in dysregulation of the HPA axis in wild animals by chronic stress.

Heart Rate and Heart‐Rate Variability Responses to Acute and Chronic Stress in a Wild‐Caught Passerine Bird

The cardiovascular‐stress response has been studied extensively in laboratory animals but has been poorly studied in naturally selected species. We determined the relative roles of the sympathetic nervous system (SNS) and the parasympathetic nervous system (PNS) in regulating stress‐induced changes in heart rate (HR) in wild‐caught European starlings (Sturnus vulgaris). In both heart‐rate variability (HRV) analysis and receptor blockade (atropine and propranolol) experiments, baseline HR was controlled predominantly by the PNS, whereas the increase in HR resulting from acute restraint stress was controlled predominantly by the SNS. These results indicate similar cardiac control of baseline and acute‐stress‐induced HR in wild‐caught starlings and mammals. We further investigated HR responses during chronic stress. Driven primarily by changes in PNS regulation, baseline HR increased during the day but decreased at night. In addition, elevated HRs during acute restraint stress were attenuated throughout chronic stress and were accompanied by decreased HRV. This suggested that increased SNS drive elevated HR, but the attenuated HR response combined with resistance to the SNS blocker propranolol suggested that the sympathetic signal was less effective during chronic stress. Overall, chronic stress in wild‐caught starlings elicited profound changes in cardiac function that were primarily regulated by changes in the PNS.

Wild European Starlings (Sturnus vulgaris) Adjust to Captivity with Sustained Sympathetic Nervous System Drive and a Reduced Fight‐or‐Flight Response

Although research on wild species typically involves capture, handling, and some degree of captivity, few studies examine how these actions affect and/or alter the animal’s underlying stress physiology. Furthermore, we poorly understand the immediate changes that occur as wild animals adjust to captive conditions. Most studies to date have investigated relatively long‐term changes in the glucocorticoid response to an acute stressor, but immediate changes in the fight‐or‐flight response are relatively understudied in wild‐caught species. In this study, we investigated changes to the cardiovascular stress response during the first 10 d of captivity of freshly captured wild European starlings (Sturnus vulgaris). We demonstrated that (1) baseline heart rate (HR) remains elevated for several days following transport into captivity, (2) the normal balance between sympathetic nervous system (SNS) and parasympathetic nervous system regulation of HR is disrupted, with the SNS exerting relatively greater control over baseline HR for the first days of captivity, and (3) the HR response to startle, a mild stressor, becomes significantly reduced compared to that of starlings maintained in captivity for several months and remains below the control response for at least 10 d. These data are the first to show that successive acute stressors and introduction to a captive setting significantly alter the physiology and responsiveness of the cardiovascular stress response system.

Captive European starlings (Sturnus vulgaris) in breeding condition show an increased cardiovascular stress response to intruders.

European starlings (Sturnus vulgaris) alter their physiology and behavior between seasons, becoming territorial during the spring/summer and flocking during the fall/winter. We used captive male starlings in breeding (photostimulated to 18L:6D) and nonbreeding (11L:13D) conditions to determine whether changing physiology and behavior alters their reaction to crowding. One or five intruders entered a resident’s cage without human disturbance. A subcutaneous heart rate transmitter recorded cardiovascular output in residents. Corticosterone and testosterone were measured in plasma samples taken before and after the intrusion. While corticosterone concentrations did not change, heart rate changed significantly, indicating that these responses can be regulated independently. Long‐day birds showed a significantly elevated heart rate response to the single‐bird intrusion compared to short‐day birds. Whereas five intruders elicited an identical peak response in both groups, long‐day birds also demonstrated an equivalent response to one intruder. In addition, one intruder induced longer elevation in heart rate for long‐day birds. Male starlings in breeding condition, therefore, demonstrate an increased sensitivity to additional conspecifics. This seasonal shift in response suggests that a higher tolerance for intrusion (i.e., considering a nearby starling as less stressful) may facilitate flocking behavior, while a lower tolerance may aid in territoriality.

Combined effects of molt and chronic stress on heart rate, heart rate variability, and glucocorticoid physiology in European Starlings

Molt is an important life-history stage in avian species, but little is known about the effects of chronic stress during this period. Three weeks after the onset of molt, captive European starlings (Sturnus vulgaris) were exposed to 18 days of chronic stress, induced with four 30-minute randomized stressors presented daily. Birds showed no chronic-stress-induced changes in heart rate or heart rate variability when measured either during the middle of the day or at night. These data suggest that chronic stress did not alter the balance between sympathetic and parasympathetic nervous system regulation of cardiovascular function, which contrasts with data from an earlier study indicating that chronic stress profoundly alters cardiovascular function in non-molting starlings. Additionally, there was a significant increase in restraint-induced corticosterone secretion the first week of chronic stress that subsequently returned to pre-chronic-stress levels by the second week of exposure. The attenuated corticosterone response again contrasts with data from non-molting starlings that showed significant decreases in corticosterone responses. Consequently, the resistance to cardiovascular and corticosterone changes indicates that the physiological changes induced by chronic stress are greatly attenuated in molting birds. Overall, the data suggest that molt requires a degree of physiological stability that must be protected, so that if a bird is exposed to chronic stress during this life-history stage, molt takes priority.

Stress responsiveness decreases with age in precocial, juvenile Chukar.

Abstract Development of the hypothalamic-pituitary-adrenal (HPA) axis and subsequent corticosterone (CORT) release in newly hatched birds is a balance between limiting exposure to the detrimental effects of CORT on growth and development, and the necessity of mounting an acute stress response. We measured the stress responsiveness of juvenile Chukar (Alectoris chukar) 20 to 60 days post-hatch prior to molting into full adult plumage. The integrated CORT response during 60 min of restraint in these individuals decreased with age. Comparisons to mean adult integrated CORT values imply the youngest juveniles have greater responses than adults while the oldest juveniles have reduced CORT responses. This pattern is currently an anomaly within the altricial-precocial range and suggests specific tradeoffs, such as molting into adult plumage, may affect timing of HPA suppression during development.

Acute Corticosterone Stress Response to Handling in Four Captive Gopher Tortoises (Gopherus polyphemus)

ABSTRACT Corticosterone is the primary glucocorticoid hormone produced by reptiles in response to stressful stimuli. Evaluating hormone responses to stress in reptiles relies on acquiring baseline corticosterone levels; however, the stress associated with restraint needed to collect blood samples from animals can affect the results. Therefore, it is important to obtain a blood sample in a relatively short time after the capture of an animal. In some avian and reptilian species, a “3 min rule” has been determined, suggesting that blood samples collected within 3 min of capture are more likely to represent baseline corticosterone levels. The purpose of this study was to determine a time limit for collection of blood samples to evaluate baseline corticosterone concentrations in captive gopher tortoises, Gopherus polyphemus. Four nonreleasable, adult gopher tortoises were used for this study. All tortoises were acclimated to their captive environment for 10 months. Each tortoise was then manually restrained f...