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Flushing Effects and Seasonal Changes on Corticosterone Levels in Adult Long-Eared Owls Asio otus
Abstract
Long-eared Owls Asio otus were flushed and captured from communal winter roosts and nesting seasons to assess both initial and stress-induced corticosterone concentrations. We examined blood samples from 16 males and 8 females in the winter, and 16 males and 11 females in the breeding season. Corticosterone concentrations after flushing owls in either season were not correlated with the elapsed time from initial flush to capture, suggesting that these birds did not interpret flushing as stressful. In contrast, 30 min of handling and restraint during both seasons elicited robust increases in plasma cortlcosterone concentrations that did not differ by sex. Although stress-induced corticosterone levels did not differ seasonally, baseline levels were 50% lower during the winter compared to breeding, suggesting the breeding season is a more stressful time. These results indicate that capture techniques used in this study with Long-eared Owls were only stressful when successful, and that initial corticosterone concentrations vary seasonally.
... This method is widely used and has garnered data concerning patterns of GC secretion and their various roles in wild animals (Deviche et al., 2010;French et al., 2008;Holding et al., 2014;Pereyra and Wingfield, 2003;Pravosudov et al., 2002;Refsnider et al., 2015). Many avian studies of seasonal patterns report higher CORT levels at the onset of breeding where it may serve to mobilize energy stores, and then levels declining post breeding when it may interfere with anabolic processes, such as feather molt (Foltz et al., 2015;Holding et al., 2014;Cornelius et al., 2011; DesRochers et al., 2009;Romero et al., 2009Romero et al., , 2005Pereyra and Wingfield, 2003;Raja-aho et al., 2013). In some species, plasma CORT levels are reduced during breeding when stress might interfere with limited opportunities for reproduction (e.g., a short breeding season), and thus, yearly CORT patterns often align closely with specific life-history patterns and environmental conditions (Holberton and Wingfield, 2003;Romero et al., 1997). ...
The secretion of steroids from the adrenal gland is a classic endocrine response to perturbations that can affect home-ostasis. During an acute stress response, glucocorticoids (GC), such as corticosterone (CORT), prepare the metabolic physiology and cognitive abilities of an animal in a manner that promotes survival during changing conditions. Although GC functions during stress are well established, much less is understood concerning how adrenal androgens, namely de-hydroepiandrosterone (DHEA) are influenced by stress. I conducted three field studies (one experimental and two descriptive) aimed at identifying how both CORT and DHEA secretion in free-living male northern cardinals (Cardinalis cardinalis), vary during acute stress; across different circulations (brachial vs. jugular); in response to ACTH challenge; and during the annual cycle. As predicted, restraint stress increased plasma CORT, but unexpectedly DHEA levels decreased , but the latter effect was only seen for blood sampled from the jugular vein, and not the brachial. The difference in DHEA between circulations may result from increased neural uptake of DHEA during stress. Injection with exogenous adrenocorticotropic hormone (ACTH) increased CORT concentrations, but failed to alter DHEA levels, thus suggesting ACTH is not a direct regulator of DHEA. Monthly field sampling revealed distinct seasonal patterns to both initial and restraint stress CORT and DHEA levels with distinct differences in the steroid milieu between breeding and non-breeding seasons. These data suggest that the CORT response to stress remains relatively consistent, but DHEA secretion is largely independent of the response by CORT. Although CORT functions have been well-studied in wild animals, little research exists for the role of DHEA and their variable relationship sets the stage for future experimental research addressing steroid stress responses.
Long-eared Owl Asio otus nestlings usually depart from their nests at approximately 22 days of age, and cannot fly until approximately 35 days of age. Corticosterone has been Implicated as a mechanism Influencing nest departure in many avian species. We sampled corticosterone concentrations in wild nestling and nest-departed Long-eared Owl chicks to determine if this stress hormone Influenced nest departure. Baseline corticosterone titres were found to be similar in nest-bound and nest-departed young (10.69 ± 1.37 vs. 9.29 ± 1.58 ng/ml respectively), suggesting that stress was not the trigger for nest departure. Nest-bound chicks however did show lower stress-induced titres levels than nest-departed chicks (14.62 ± 1.98 vs. 21.58 ± 2.22 ng/ml, respectively). This suggests that nest-bound chicks may have a blunted response, perhaps due to age-related developmental constraints influencing corticosterone secretion.
Hormonal manipulations with implants allow examination of the costs and benefits of behaviors and physiologic states mediated by a given hormone. As a part of ongoing research into the effects of the steroid hormone testosterone (T) in Dark-eyed Juncos (Junco hyemalis), we measured the corticosterone (B, asteroid hormone secreted by the adrenal in response to stress) response to the stress of capture and handling in males treated with T (T-males) and in control males (C-males). Although B may be essential for energy mobilization, chronic or repeated exposure to elevated levels of B can have many negative effects. Because T mediates many behaviors that may increase the likelihood that an individual will encounter stressors, we predicted that plasma B would rise more rapidly in T-males than in controls. In the first few minutes post-capture, the increase in B levels was significantly higher in T-males than in controls. B levels in samples collected 10, 30, and 60 min post-capture were consistently higher in T-males than in C-males; however, the difference was not statistically significant. Because previous work has shown that T-males reduce their parental contribution, we compared females that were mated to T-males and C-males (hereafter T- and C-females). B levels of T-females increased sharply in the first few minutes post-capture, whereas in C-females they did not; however, the responses were not statistically different. Males had higher initial levels and a greater B-response to stress than females when data were compared irrespective of treatment. Our results suggest that the behaviors or physiological changes induced by T are potentially costly and that such costs may in part be incurred through elevated B.
We used a standard handling protocol to examine the stress response of captive young western screech-owls during their active (nighttime) and inactive (daytime) periods and to compare the stress responses of captive and free-living owls. Circulating corticosterone levels were significantly higher during the inactive period than in the active period in this nocturnal species. This suggests that the daily pattern of corticosterone secretion is reversed in nocturnal birds and is correlated with activity period rather than with the light/dark cycle. Young (ca. 4-5 mo old) screech-owls of both sexes showed increases in plasma corticosterone up to 30 min after capture, followed by significant decreases at 60 min. This pattern is similar to those of other species of birds examined previously, except that decreases in corticosterone at 60 min rarely have been observed. Such decreases may be the result of physiological differences between adult and young birds, habituation to handling in captive birds, or the effects of body condition. Corticosterone levels and the response to capture and handling were comparable in captive and free-living owls, which suggests that the captive owls were not subjected to chronically high levels of stress.
The secretion of glucocorticoids (GCs) is a classic endocrine response to stress. Despite that, it remains controversial as to what purpose GCs serve at such times. One view, stretching back to the time of Hans Selye, posits that GCs help mediate the ongoing or pending stress response, either via basal levels of GCs permitting other facets of the stress response to emerge efficaciously, and/or by stress levels of GCs actively stimulating the stress response. In contrast, a revisionist viewpoint posits that GCs suppress the stress response, preventing it from being pathologically overactivated. In this review, we consider recent findings regarding GC action and, based on them, generate criteria for determining whether a particular GC action permits, stimulates, or suppresses an ongoing stress-response or, as an additional category, is preparative for a subsequent stressor. We apply these GC actions to the realms of cardiovascular function, fluid volume and hemorrhage, immunity and inflammation, metabolism, neurobiology, and reproductive physiology. We find that GC actions fall into markedly different categories, depending on the physiological endpoint in question, with evidence for mediating effects in some cases, and suppressive or preparative in others. We then attempt to assimilate these heterogeneous GC actions into a physiological whole.
Harsh weather can have devastating effects on both the survival and the breeding success of wild animals. Corticosterone, released in response to the stress caused by harsh conditions, may trigger physiological and behavioral changes that help ameliorate these effects. We examined three species of Arctic-breeding passerine birds for correlations between circulating plasma corticosterone levels and weather conditions at the time of capture. Furthermore, because persistently poor weather conditions may be required to initiate a stress response, we also looked for a relationship between corticosterone levels and weather conditions over the 24 and 72 h preceding capture. None of the three species showed substantial effects of weather on unstressed corticosterone levels during the breeding season, although one species showed a significant relationship with stress-induced corticosterone levels. In two species, however, variations in weather during molt (an energetically costly period when birds replace their feathers) explained from 35 to 88% of the individual variation in corticosterone levels. In a third molting species, weather conditions in the preceding 24 and 72 h explained between 20 and 30% of the individual variation in corticosterone levels. It thus appears that adverse weather may be a potent stimulator of corticosterone release during molt, but not during the breeding season. Although extreme weather conditions (those experienced once every few years) can disrupt breeding, since none of the birds abandoned breeding we might conclude that the storms in this study were well within the ability of the birds to cope physiologically.
Birds breeding in the Arctic must carefully balance survival and reproduction because of the often extreme environmental conditions and the very brief breeding season. Acute elevation of plasma corticosterone is one mechanism that birds apparently use to alter the balance in favor of survival at the expense of reproduction when faced with stressors such as storms, predators, or low food availability. To examine this relationship, we applied a standardized stressor, capture and handling, to four species of shorebirds (Scolopacidae) during their breeding season in the Arctic and measured the increase in corticosterone between 3 min and 30 min after capture (hereafter called the stress response). We tested two hypotheses in an effort to explain the individual variation observed in the stress response. The first hypothesis states that individuals most responsible for parental care have a lower stress response than individuals less responsible for parental care. In species with uniparental care (Pectoral Sandpiper Calidris melanotos, Red Phalarope Phalaropus fulicaria), the caregivers had a lower stress response than the opposite sex, although in the latter species the difference was not significant (P = 0.016 and P = 0.102, respectively). In a species with equal biparental care (Semipalmated Sandpiper C. pusilla), the stress response did not differ between the sexes (P = 0.99, Barrow population). In a species with unequal biparental care (Western Sandpiper C. mauri), the more parental sex (males) had a much lower stress response than the less parental sex (P = 0.002). The second hypothesis states that individuals breeding in the high Arctic have a lower stress response than individuals breeding in the low Arctic. The stress response in a low-Arctic population of Semipalmated Sandpipers (Nome) was higher than that in a high-Arctic population (Barrow, P < 0.05). Individuals at an additional high-Arctic location (Prudhoe Bay) exhibited stress responses most similar to those of the Barrow population (P > 0.05). Taken together, these results provide evidence of a mechanism that birds may use to breed in environments with a brief breeding season and under conditions that might be perceived as stressful, if not for their reduced sensitivity to potential stressors.
Corticosterone concentrations in birds usually rise in response to capture and handling, and it is often assumed that this change is predictable. We tested this assumption by leaving Gambel's White-crowned Sparrows (Zonotrichia leucophrys gambelii), House Sparrows (Passer domesticus), and Lapland Longspurs (Calcarius lapponicus) in nets or traps for 15 min following capture and comparing their corticosterone response over the next 60 min with birds removed immediately. White-crowned Sparrows and House Sparrows left in mist nets for 15 min and then bled had significantly elevated corticosterone concentrations compared to controls that were immediately removed from the net and bled. Corticosterone concentrations over the next 45 min of handling and restraint were similar between groups. In another experiment, White-crowned Sparrows and Lapland Longspurs were captured using seed-baited Potter traps. The corticosterone response of White-crowned Sparrows left in the trap for 15 min did not differ from White-crowned Sparrows removed immediately. Leaving Lapland Longspurs in the trap had no effect in the initial 10 min of handling and restraint, but at 30 and 60 min these birds had significantly lower corticosterone concentrations than longspurs removed immediately from the trap. These data indicate that failing to immediately remove birds from nets or traps can alter the corticosterone response to subsequent stressful stimuli in unpredictable ways. This result emphasizes that the elapsed time from capture is a critical variable in assessing stress responses in free-living birds.
Respuestas de los Niveles de Corticosterona en Aves Silvestres: La Importancia de un Muestreo Inicial Inmediato
Resumen. Las concentraciones de corticosterona en las aves usualmente aumentan en respuesta a la captura y manipulación, y muchas veces se supone que estos cambios son predecibles. Pusimos a prueba esta suposición reteniendo individuos de las especies Zonotrichia leucophrys gambelii, Passer domesticus y Calcarius lapponicus en redes o trampas durante los 15 minutos subsecuentes a la captura y comparamos sus respuestas en los niveles de corticosterona durante los siguientes 60 minutos con las de individuos removidos inmediatamente de las trampas y redes. Las muestras de sangre de Z. l. gambelii y P. domesticus que fueron obtenidas después de 15 minutos de retención en las redes tuvieron niveles de corticosterona significativamente más altos que las de los individuos control obtenidas inmediatamente después de la captura. Durante los 45 minutos siguientes de manipulación y captura, las concentraciones de corticosterona fueron similares entre los dos grupos. En otro experimento, Z. l. gambelii y C. lapponicus fueron capturados mediante trampas “Potter” cebadas con semillas. La respuesta en los niveles de corticosterona de Z. l. gambelii no fue diferente entre individuos retenidos en las trampas por 15 minutos e individuos removidos inmediatamente. Para individuos de C. lapponicus retenidos en las trampas no hubo un efecto durante los 10 minutos iniciales de manipulación y captura, pero a los 30 y 60 minutos estas aves tuvieron concentraciones significativamente menores que los individuos removidos inmediatamente. Estos resultados indican que al no remover inmediatamente a las aves de las redes o trampas, las respuestas en los niveles de corticosterona a estímulos estresantes pueden verse alteradas de una manera impredecible. Estos resultados enfatizan que en aves silvestres, el lapso de tiempo desde la captura es una variable crítica en la determinación de las respuestas al estrés.
Plasma levels of luteinizing hormone (LH), testosterone, and corticosterone were measured in relation to periods of inclement versus fair weather during the reproductive season of the Puget Sound White-crowned Sparrow (Zonotrichia leucophrys pugetensis). In 1974, cool stormy weather in spring delayed the onset of breeding by one month and also prolonged the period of elevated circulating levels of LH and testosterone, compared with the fair spring of 1975. Inclement weather in 1974 did not appear to be stressful, as indicated by body weights and plasma levels of corticosterone. In late May 1980, however, a storm occurred after nesting activities had begun and all pairs sampled were feeding young. In this case, plasma levels of corticosterone were greatly elevated above those of birds sampled at the same time in the warm spring of 1979 and also above those of birds sampled in spring of both 1974 and 1975. In addition, fat depots were virtually exhausted in birds sampled during the storm of 1980, suggesting that these birds were stressed. Most pairs lost their brood in May 1980, presumably to starvation, and renested after amelioration of environmental conditions in June.
These data suggest that although storms may modify the onset and temporal progression of the reproductive cycle, they are stressful to adults only when the nesting phase is in progress. Thus, the underlying mechanisms by which inclement weather delays the onset of breeding or disrupts the nesting once underway are likely to have different endocrine bases.
In North America, 13 of 20 breeding season studies reporting on Long-eared Owl (Asio otus) reproduction were conducted in open country habitats, four in woodland or edge habitats and three in predominantly woodland habitat. Sixteen of 22 nonbreeding season studies that reported communal roost sites were located in forest/edge habitats, five reported locations in open space and one was found within forest habitat. There is currently little data to indicate either a negative or positive effect of forest-management practices on this species. Although there appears to be some evidence of population declines in specific geographic areas, these impacts have been attributed to loss of riparian vegetation, conversion of foraging areas to agricultural fields and reforestation of open habitats. The Long-eared Owl's ecomorphology is suggestive of a species that inhabits open country. Additionally, its primary food is small mammals (e.g., microtine and heteromyid rodents) which inhabit open country. Should the Long-eared Owl be considered a forest owl? Research data would suggest no; however, studies from extensive deciduous and coniferous woodlands are needed.
A wide range of stressor stimuli activate the hypothalamo-adenohypophyseal-adrenal axis, resulting in a rapid rise of glucocorticosteroid secretion. Most studies on this subject have involved captive subjects and artificial stresses. Very few investigations have shown that stressful stimuli under natural conditions can have similar, rapid effects on the adrenal cortex. In this study, free-living common diving petrels, Pelecanoides urinatrix, captured at sea off South Georgia Island, showed highly significant elevations of circulating corticosterone levels after capture and handling stress. Plasma concentrations of corticosterone rose from a baseline of about 10 ng/mL immediately after capture to a peak of circa 40 ng/ mL within 30 min. There were no apparent differences between the sexes. During a severe storm on July 5, 1991 (with high winds, heavy snowfall, and near-zero visibility), birds had significantly elevated levels of circulating corticosterone immediately after capture. There was no further increase in plasma levels of corticosterone (for the 1-h period of sample collection), which suggests that these birds were already maximally stressed when captured. Body mass of birds captured during the storm was lower than during calm weather. In calm weather there was a significant negative relationship of maximum corticosterone level generated during capture stress to the ratio of body mass to wing chord cubed (a measure of body condition). No such relationship was observed during stormy weather.
Corticosterone concentrations in birds usually rise in response to capture and handling, and it is often assumed that this change is predictable. We tested this assumption by leaving Gambel's White-crowned Sparrows (Zonotrichia leucophrys gambelii), House Sparrows (Passer domesticus), and Lapland Longspurs (Calcarius lapponicus) in nets or traps for 15 rain following capture and comparing their corticosterone response over the next 60 min with birds removed immediately. White-crowned Sparrows and House Sparrows left in mist nets for 15 min and then bled had significantly elevated corticosterone concentrations compared to controls that were immediately removed from the net and bled. Corticosterone concentrations over the next 45 min of handling and restraint were similar between groups. In another experiment, White-crowned Sparrows and Lapland Longspurs were captured using seed-baited Potter traps. The corticosterone response of White-crowned Sparrows left in the trap for 15 min did not differ from White-crowned Sparrows removed immediately. Leaving Lapland Longspurs in the trap had no effect in the initial 10 min of handling and restraint, but at 30 and 60 min these birds had significantly lower corticosterone concentrations than longspurs removed immediately from the trap. These data indicate that failing to immediately remove birds from nets or traps can alter the corticosterone response to subsequent stressful stimuli in unpredictable ways. This result emphasizes that the elapsed time from capture is a critical variable in assessing stress responses in free-living birds.
There are more CRH-like immunoreactive neurons in the preoptic nucleus and nucleus lateralis tuberis in the brain of feral brown trout,Salmo trutta,living in cadmium- and zinc-contaminated regions of the Eagle River than in fish from an uncontaminated control site. Histological analyses revealed that interrenal cells are more stimulated (exhibiting both hypertrophy and hyperplasia) in fish living in contaminated sites than interrenal cells of fish at the control site. These results suggest that the hypothalamo-pituitary-interrenal (HPI) axis of fish living in the metal-contaminated water shows evidence of chronic stimulation. We suggest that assessment of these parameters of the HPI axis may be useful indices of chronic environmental stress in trout.
Male and female redpolls (Acanthis flammea) showed marked increases in circulating corticosterone up to 1 hour after exposure to a common stress - capture, handling and restraint - indicating that their hypothalamo-pituitary-adrenal axis responded to acute stress in a manner similar to that of other vertebrates. We used this protocol as a measure of responsiveness of the adrenocortical cells to acute stress in general and for comparison with gender and across seasons. In both sexes the adrenocortical response to stress was reduced in January (at Fairbanks, 64°N) and maximal when birds were breeding in June at Toolik Lake (69°N). The elevation of circulating corticosterone following capture and handling in breeding males at Barrow (71°N) was significantly less than in breeding males at Toolik Lake. There were also considerable variations among individuals in the intensity of the adrenocortical responses, particularly in the maximum levels of corticosterone attained. This individual variation correlated significantly with fat score and/or body mass in both sexes only in breeding birds at Barrow. This difference may be explained by generally lower, and thus reduced variability in body fat and mass in birds sampled in the warmer climate of Toolik Lake. A similar trend was seen in non-breeding birds, but this was not significant. Additionally, in January, baseline cortisterone levels in males were correlated with body mass, although this relationship did not hold when both sexes were considered. Body mass and fat score in winter were similar to those of redpolls sampled at Barrow in June. These data suggest that redpolls may be able to adjust their responsiveness to acute stresses in relation to fat stores. Those with greater fat depots had reduced responsiveness to stress.
Many avian species of the North American Sonoran desert, e.g., the black-throated sparrow, Amphispiza bilineata, cactus wren, Campylorhynchus brunneicapillus, and curve-billed thrasher, Toxostoma curvirostre, can potentially breed from March/April to August. It is possible that, at least in summer, intense heat and aridity may have inhibitory effects on breeding by precipitating a stress response. Stress typically results in a rise in secretion of adrenocorticosteroid hormones that then inhibit reproduction by suppressing release of gonadal hormones. However, we found that plasma levels of corticosterone were not higher during summer, compared with winter, even in 1989 when summer temperatures were higher than normal. In June 1990, temperatures were also above normal and soared to the highest level recorded in Arizona (50 degrees C). Plasma levels of corticosterone during June were high in black-throated sparrows, but less so in two other species (Abert's towhee, Pipilo aberti, and Inca dove, Scardafella inca) found in more shady riparian and suburban habitat with constant access to water. The adrenocortical response to stress (as measured by the rate of corticosterone increase following capture) was reduced in the hottest summer months in black-throated sparrows, cactus wrens, and curve-billed thrashers, but less so in Abert's towhee an Inca dove. These data suggest that at least some birds breeding in the open desert with restricted access to water are able to suppress the classical adrenocortical response to stress. The response is then reactivated in winter after breeding has ceased. It is possible that this stress modulation may allow breeding to continue despite severe heat. Analysis of plasma from these species indicated that the apparent modulation of the adrenocortical response to stress was not an artifact of reduced affinity or capacity of corticosterone binding proteins.
Corticosterone, progesterone, estradiol-17 beta, and estrone were quantified in plasma collected weekly (April-September) from renesting and nonlaying female American kestrels (Falco sparverius) paired with males in captivity. Hormone levels and body weights for laying females were maximal during courtship and egg-laying periods, while those for non-layers showed no such distinct peaks. This demonstrated that these profiles were not controlled solely by photoperiod. Plasma corticosterone levels were elevated in all females during August and September when kestrels are preparing for migration. For laying females, body weight was positively correlated with plasma estrogen levels. A low spring body weight gain, and not stress, may have prevented the females from breeding in captivity. The photoperiodic control of molt did not appear to be mediated directly by the hormones studied, since there were no changes in hormone levels associated with the onset of molt.
Daily variations in concentrations of plasma corticosterone were found in pigeons maintained on 12-hr and 16-hr daily photoperiods. Rapid increases occurred within a few hours after the onset of the dark period, reaching peak values in 4–8 hr. There was a gradual reduction in concentrations during the light except for a small secondary peak late in the day in the pigeons adapted to a 16-hr daily photoperiod. The rhythms are lost in pigeons that are kept in continuous light for 15 days. The function of daily rhythms of corticosterone are discussed in terms of their role in regulating daily rhythms of cropsac responses to prolactin.
The Lapland longspur, Calcarius lapponicus, times its breeding season so that chicks hatch coincident with the brief period of food abundance in the high arctic. This synchronization requires that all reproductive activities occur in over a much shorter period than at lower latitudes. Because of the known influence of stress hormones on delaying breeding in temperate-zone birds and the detrimental effects of such delays in the arctic, we expected the performance of the hypothalamic-pituitary-adrenal (HPA) axis of arctic-breeding birds to show less sensitivity to environmental stress than their mid-latitude counterparts. We found that adrenocortical responsiveness to the standardized stress of capture and handling, measured by taking five serial blood samples for corticosterone during the course of a 1-hr period, was similar to many temperate passerines and was also similar both between male and female longspurs and between the migratory and reproductive phases. However, the profile of plasma corticosterone during capture stress was significantly damped in longspurs sampled as they began their postnuptial molt. In addition, we had the opportunity to examine endocrine responses to a natural environmental stress in 1989 during a 3-day snowstorm which concealed available food resources. During this storm longspurs formed progressively larger flocks each day, with females abandoning incubation duties by the third day. Birds captured during the storm showed highly significant increases in both the rate of plasma corticosterone increase during capture and the peak postcapture level compared with birds sampled before the storm. This increased adrenal potential suggests increased activity of the HPA axis in response to severe conditions and is reminiscent of the response to fasting. Although the storm occurred during incubation, and reproductive hormone levels had begun to decline, we measured significant reductions in luteinizing hormone in both males and a subset of females captured during the storm.
The Gambel's race of white-crowned sparrow (Zonotrichia leucophrys gambelii) migrates each year from their wintering grounds in the Southwestern United States to the Arctic to breed. Associated with this migration is a change in both the nonstressed and the stress-induced levels of circulating plasma corticosterone. Birds were captured at two sites on their wintering grounds (New Mexico and Arizona). Although stress-induced corticosterone levels were elevated at each site compared to nonstressed levels, there were no differences between wintering sites. These were also similar to levels in birds caught in Washington state during fall migration. In contrast, nonstressed corticosterone values were greatly elevated in birds on their breeding grounds in Alaska and similar to stress-induced levels in wintering birds. Corticosterone levels rose even further in response to the stress of capture and handling in breeding birds. These augmented corticosterone levels during breeding were not associated with weather. Both nonstressed and stress-induced corticosterone levels were similar in birds caught on their breeding grounds on two different years, one with temperatures during mid-May of approximately 0 degree C during a snow storm and the other with temperatures in the mid-20s. These results suggest that seasonal physiological changes, and not local conditions, underlie seasonal changes in corticosterone levels. Furthermore, birds caught in Washington state during spring migration had intermediate levels of both nonstressed and stress-induced corticosterone. Corticosterone release may function differently during spring and fall migrations.
This study describes an interrenal stress response in adult toads, Bufo terrestris, after exposure to coal combustion waste (characterized by a variety of trace elements). In the first portion of this study, free-ranging male toads captured at the coal ash polluted site exhibited significantly higher circulating levels of corticosterone (B) in both June/July and August than conspecifics captured at uncontaminated sites. In addition, both calling and noncalling males from the polluted site had higher B levels than conspecifics engaged in the same behaviors at reference sites. Testosterone levels were elevated in toads from the polluted site, regardless of capture month or behavioral state, suggesting altered androgen production, utilization, and/or clearance. In the second portion of this study, male toads from reference sites were transplanted to enclosures at the polluted site or an uncontaminated site. Toads held at the polluted site exhibited significant increases in B after 10 days of exposure compared to toads held at the reference site. B levels remained significantly elevated in toads transplanted to the polluted site after 12 weeks. We hypothesize that high concentrations of various trace elements in the polluted site are responsible for these hormonal responses.
I investigated the effects of high plasma levels of corticosterone in male pied flycatchers, Ficedula hypoleuca, during the period of territorial establishment and the nestling period. In a second experiment males were exposed to a territorial intruder, a great spotted woodpecker model and a weasel model during the nest-building and nestling periods and their behavioural and hormonal reactions studied. Males were also exposed to handling stress (hormonal study) during these periods. During the period of territorial establishment, corticosterone-treated males, as well as control males, abandoned the territory in which they were captured; however, males in both groups very soon established new territories. During the nestling period, corticosterone-treated males, but not control males, abandoned their nests. During the nest-building period, intact males frequently attacked the territorial intruder but corticosterone-treated males never did; the woodpecker was only rarely attacked by intact males, and the weasel never. During the nestling period, the weasel was not attacked and territorial intruders only rarely; but woodpeckers were frequently attacked. With the progress of the breeding season, male flycatchers significantly reduced their sensitivity, in terms of the adrenocortical response, to all stressors tested. During the nest-building period, corticosterone levels were significantly higher in males exposed to handling, a weasel and a territorial intruder than in unmanipulated males; corticosterone levels in males exposed to a woodpecker did not differ from those in unmanipulated males; and testosterone levels were significantly elevated in males exposed to a woodpecker and to an intruder, but were reduced in males exposed to a weasel. Handling did not affect the testosterone level. During the nestling period, all groups showed low testosterone levels, and only exposure to a weasel and to handling increased corticosterone levels significantly. The results indicate that environmentally induced changes in testosterone and corticosterone secretion can be affected independently from one another, and that there are ecological bases for the differentiated hormonal responses to stress. Copyright 1998 The Association for the Study of Animal Behaviour. Copyright 1998 The Association for the Study of Animal Behaviour.
Glucocorticoids have a wide array of actions in vertebrates. Daily fluctuations in basal levels of glucocorticoids are thought to regulate homeostatic mechanisms. In contrast, elevated levels secreted in response to stress stimulate changes in physiology and behavior. These changes are thought to aid an animal in avoiding chronic stress or death. Twenty-four-hour rhythms in basal and stress-induced glucocorticoids have been detected in laboratory mammals, but studies in wild, seasonal vertebrates are rare. Identification of plasticity in hormone secretion in wild vertebrates is critical to understanding the effects of hormones on physiology and behavior, and therefore the success of an animal in its natural environment. In the present study, we characterized diel patterns of basal and stress-induced corticosterone (the avian glucocorticoid) under two photoperiods in Gambel's white-crowned sparrow (Zonotrichia leucophrys gambelii). In contrast to previous findings in the white-crowned sparrow, we demonstrated a robust rhythm in basal corticosterone secretion, in which corticosterone reaches peak levels at the end of the inactive period, and has returned to trough levels just after the active period has begun. We also demonstrated a diel rhythm in secretion of corticosterone in response to a stressor, showing the greatest response at the beginning of the active period. Patterns of CORT secretion were similar under both photoperiods. These patterns show interesting similarities and differences to classical mammalian rhythms.
Captive starlings were used to examine daily and seasonal changes in basal and stress-induced corticosterone levels. Birds were bled at 4 times during the daily cycle and during three different simulated seasons: under a short-day photoperiod (mimicking winter), under a long-day photoperiod (mimicking summer), and while undergoing a prebasic molt. Basal corticosterone samples were assayed from blood collected within 3 min of disturbance and corticosterone increases in response to handling and restraint were monitored in blood taken at 15, 30, and 45 min postdisturbance. Handling and restraint elicited robust increases in corticosterone at all times of the day and during all three seasons. Both basal and stress-induced levels varied with the time of day (with the exception of basal samples during molt). Levels were higher at night, during the bird's inactive period, and decreased during the day. These data indicate that starlings have daily rhythms in both basal corticosterone levels and in their response to stress, with more corticosterone released during the night in response to identical stimuli. Starlings also show pronounced seasonal variation in both basal and stress-induced corticosterone levels. Although birds held on short and long days had equivalent corticosterone levels, both basal and stress-induced levels were lower during molt. This parallels data from free-living birds and provides a laboratory model for studying seasonal corticosterone regulation.
Corticosterone concentrations were measured in captive house sparrows (Passer domesticus) and found to vary both daily and with different photoperiods. Basal corticosterone was highest during the dark hours of the daily cycle and lowest during the light hours. This trend remained constant when the birds were held on short-day and long-day light cycles, and while the birds were undergoing a prebasic molt. At all times, corticosterone concentrations significantly increased in response to the stress of handling and restraint. Stress-induced corticosterone concentrations, however, only reflected a daily rhythm when the birds were held on short-days. Furthermore, even though mean basal corticosterone concentrations were equivalent over the short-day, long-day, and molt, total corticosterone output in response to stress was lower in molting birds, especially at night. Therefore, these data indicate that captive house sparrows modulate corticosterone in daily cycles that change in response to photoperiod.
The vertebrate stress response helps animals respond to environmental dangers such as predators or storms. An important component of the stress response is glucocorticoid (GC) release, resulting from activation of the hypothalamic-pituitary-adrenal axis. After release, GCs induce a variety of behavioral and physiological changes that presumably help the animal respond appropriately to the situation. Consequently, GC secretion is often considered an obligatory response to stressful situations. Evidence now indicates, however, that free-living species from many taxa can seasonally modulate GC release. In other words, the magnitudes of both unstressed and stressed GC concentrations change depending upon the time of year. This review examines the growing evidence that GC concentrations in free-living reptiles, amphibians, and birds, but not mammals, are commonly elevated during the breeding season. This evidence is then used to test three hypotheses with different focuses on GC's energetic or behavioral effects, as well as on GC's role in preparing the animal for subsequent stressors. These hypotheses attempt to place annual GC rhythms into a physiological or behavioral context. Integrating seasonal differences in GC concentrations with either different physiological states or different life history stages provides clues to a new understanding of how GCs actually help in survival during stress. Consequently, understanding seasonal modulation of GC release has far-reaching importance for both the physiology of the stress response and the short-term survival of individual animals.
Long-eared Owl (Asio otus) The Birds of North America, no. 133. Academy of Natural Sciences Philadelphia, Immunocytochemical and histological differences in the interrenal axis of feral brown trout, Salmo trutta, in metal-contaminated waters
- J S Marks
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- D W Holt
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- D O Norris
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- J D Woodling
Marks J.S., Evans D.L. & Holt D.W. 1994. Long-eared Owl (Asio otus). In: Poole A. & Gill F. (eds) The Birds of North America, no. 133. Academy of Natural Sciences Philadelphia, and AOU, Washington, D.C. Norris D.O., Felt S.B., Woodling J.D. & Dores R.M. 1997. Immunocytochemical and histological differences in the interrenal axis of feral brown trout, Salmo trutta, in metal-contaminated waters. Gen. Comp. Endocrinol. 108: 343–351.
Strigidae species accounts
- D W Holt
- R Berkley
- C Deppe
- P L Enriguez-Rocha
- P D Olsen
- J L Petersen
- J L Rangel-Salazar
- K P Segars
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Holt D.W., Berkley R., Deppe C., Enriguez-Rocha P.L., Olsen P.D.,
Petersen J.L., Rangel-Salazar J.L., Segars K.P. & Wood K.L.
1999. Strigidae species accounts. In: del Hoyo J., Elliot A. &
Sargatal J. (eds) Handbook of birds of the world, Vol. 5.
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Adrenocortical responses to stress and their modulation in free-living vertebrates Handbook of physiol-ogy; Section 7: The endocrine system; Volume IV: Coping with the Environment: Neural and Endocrine Mechanisms
- J C Wingfield
- L M Romero
Wingfield J.C. & Romero L.M. 2001. Adrenocortical responses to stress and their modulation in free-living vertebrates. In: McEwen B.S. & Goodman H.M. (eds) Handbook of physiol-ogy; Section 7: The endocrine system; Volume IV: Coping with the Environment: Neural and Endocrine Mechanisms. Oxford University Press, New York, pp. 211–234.