Variation In Corticosterone Levels Research Articles

Glucocorticoids link forest type to local abundance in tropical birds

Abstract Selective logging is a major driver of environmental changes in the tropics. Recently, there has been increasing interest in understanding which traits make bird species resilient or vulnerable to such changes. Physiological stress mediated by the steroid hormone corticosterone (CORT) might underlie changes in local abundance of species because it regulates a range of body functions and behaviours to maintain homeostasis in changing environments. We conducted a 3‐year study to assess (a) the variation in CORT levels in feathers (where CORT is deposited during the moult) of 10 understorey bird species across both unlogged old‐growth forest and selectively logged forest in Borneo, (b) how this variation is associated with within‐year variation in population abundance between forest types and (c) whether the difference in feather CORT (fCORT) between co‐specific populations living in unlogged and logged forests in 1 year is related with their difference in population abundance the following year. We used effect size estimates to measure standardized magnitude and direction of fCORT changes between unlogged and selectively logged forest. We found small to large effect sizes, indicating large among‐species variation in physiological acclimatization to changes in forest conditions. In 2016 and 2018, species with relatively higher fCORT in unlogged forest were relatively more abundant in logged forest in the same year; in 2017, species with relatively higher fCORT in logged forest were relatively more abundant in logged forest. Importantly, we found that for a given species, the difference in fCORT at year (x) between unlogged and logged forests was negatively related with a difference in its local abundance between the two forest types in the following year (x + 1). Our results point to glucocorticoid hormones as potential mediators of carry‐over effects on population abundance due to direct and indirect effects of silvicultural practices in tropical forests of Borneo, suggesting fCORT as a potential marker of population changes. A free Plain Language Summary can be found within the Supporting Information of this article.

Habitat Characteristics in Created Vernal Pools Impact Spotted Salamander Water-Borne Corticosterone Levels

Spotted salamanders (Ambystoma maculatum) require vernal pools for breeding habitat. Limited protection and preservation of vernal pools makes suitable habitat creation important. Differences in corticosterone levels, a hormone associated with growth, development, and stress in amphibians, could indicate population health and habitat quality. Our objective was to determine if habitat characteristics in created vernal pools influence corticosterone levels of spotted salamander larvae. In May and June of 2015 and 2016, we sampled water-borne corticosterone levels of larval spotted salamanders in 34 created vernal pools constructed 1–5 years earlier. Using multiple regression, we determined the best model predicting corticosterone levels included larval total length, pool-water temperature, year sampled, and pool diameter. Pool-water pH, depth, and age; percent cover; and predator presence were not significant predictors. Annual variation in corticosterone levels and habitat characteristics, and positive associations with water temperature and salamander body size highlighted the importance of controlling for external influences. The negative association between pool diameter and corticosterone indicated that larvae in larger pools (up to 12.75-m maximum diameter) were less stressed and potentially healthier. These results indicate that pool diameter contributes to habitat quality and may be important when constructing vernal pools for spotted salamanders.

Seasonal changes in baseline corticosterone, association with innate immunity, and effects of confinement in free-ranging Eastern Box Turtles, Terrapene carolina carolina

Seasonal changes in glucocorticoids and their influence on the immune system are widespread in vertebrates, but whether this occurs in lesser studied taxa like turtles is unclear. The purpose of this study was to test for seasonal changes in baseline corticosterone (CORT), innate immunity, body condition, and metabolic factors (triglycerides, uric acid) in free-ranging Eastern Box Turtles (Terrapene carolina carolina), a species which is in decline across its range. In addition, the effect of handling and confinement on CORT levels was measured. In both years of the seasonal study, baseline CORT concentrations were significantly higher in fall than in spring, but summer CORT levels differed between the years. The annual variation in CORT levels may be related to weather conditions or associated with opportunistic mating. CORT levels of turtles confined for one hour were higher than turtles bled as quickly as possible, and unlike the seasonal study, females had higher baseline and post-stressor CORT levels than males. Baseline CORT levels were positively correlated with hemolysis titer, indicating a possible immunoenhancing effect of CORT. Triglycerides were positively correlated with body condition and were higher in females than males. The higher triglyceride level in females was likely associated with the energetic demands of reproduction and nesting. Males had a lower body condition in the fall than in both spring and summer, while females exhibited no seasonal differences in body condition. Uric acid and innate immunity measures failed to exhibit significant seasonal or sex related differences. Overall our findings of substantial annual, seasonal, and sexual variation in turtle physiology are consistent with the findings reported for other vertebrates and indicate the importance of incorporating these sources of variation into the design of future studies.

Stress hormones in relation to breeding status and territory location in colonial king penguin: a role for social density?

Because glucocorticoid (stress) hormones fundamentally affect various aspects of the behaviour, life history and fitness of free-living vertebrates, there is a need to understand the environmental factors shaping their variation in natural populations. Here, we examined whether spatial heterogeneity in breeding territory quality affected the stress of colonial king penguin (Aptenodytes patagonicus). We assessed the effects of local climate (wind, sun and ambient temperature) and social conditions (number of neighbours, distance to neighbours) on the baseline levels of plasma total corticosterone (CORT) in 77 incubating and 42 chick-brooding birds, breeding on territories of central or peripheral colony location. We also assessed the oxidative stress status of a sub-sample of central vs. peripheral chick-brooders to determine whether chronic stress arose from breeding on specific territories. On average, we found that brooders had 55% higher CORT levels than incubators. Regardless of breeding status, central birds experienced greater social density (higher number of neighbours, shorter distance between territories) and had higher CORT levels than peripheral birds. Increasing social density positively explained 40% of the variation in CORT levels of both incubators and brooders, but the effect was more pronounced in brooders. In contrast, climate was similar among breeding territories and did not significantly affect the CORT levels of breeding birds. In brooders, oxidative stress status was not affected by local density or weather conditions. These results highlight that local heterogeneity in breeding (including social) conditions may strongly affect the stress levels of breeding seabirds. The fitness consequences of such variation remain to be investigated.

A flexible Bayesian hierarchical approach for analyzing spatial and temporal variation in the fecal corticosterone levels in birds when there is imperfect knowledge of individual identity

Population cycles have long interested biologists. The ruffed grouse, Bonasa umbellus, is one such species whose populations cycle over most of their range. Thus, much effort has been expended to understand the mechanisms that might control cycles in this and other species. Corticosterone metabolites are widely used in studies of animals to measure physiological stress. We evaluated corticosterone metabolites in feces of territorial male grouse as a potential tool to study mechanisms governing grouse cycles. However, like most studies of corticosterone in wild animals, we did not know the identity of all individuals for which we had fecal samples. This presented an analytical problem that resulted in either pseudoreplication or confounding. Therefore, we derived an analytical approach that accommodated for uncertainty in individual identification. Because we had relatively low success capturing birds, we estimated turnover probabilities of birds on territorial display sites based on capture histories of a limited number of birds we captured. Hence, we developed a study design and modeling approach to quantify variation in corticosterone levels among individuals and through time that would be applicable to any field study of corticosterone in wild animals. Specifically, we wanted a sampling design and model that was flexible enough to partition variation among individuals, spatial units, and years, while incorporating environmental covariates that would represent potential mechanisms. We conducted our study during the decline phase of the grouse cycle and found high variation among corticosterone samples (11.33–443.92ng/g [x¯=113.99ng/g, SD=69.08, median=99.03ng/g]). However, there were relatively small differences in corticosterone levels among years, but levels declined throughout each breeding season, which was opposite our predictions for stress hormones correlating with a declining population. We partitioned the residual variation into site, bird, and repetition (i.e., multiple samples collected from the same bird on the same day). After accounting for years and three general periods within breeding seasons, 42% of the residual variation among observations was attributable to differences among individual birds. Thus, we attribute little influence of site on stress level of birds in our study, but disentangling individual from site effects is difficult because site and bird are confounded. Our model structures provided analytical approaches for studying species having different ecologies. Our approach also demonstrates that even incomplete information on individual identity of birds within samples is useful for analyzing these types of data.

Plasma corticosterone levels in laying hens from three different housing systems: preliminary results

Adrenocortical and thyroidal hormones are physiological indicators of various forms of stress in the fowl. In order to establish possible variations in corticosterone levels, blood samples were collected from ISA Brown hens reared in three different housing systems (cage, floor and organic way). Results showed that corticosterone concentrations were highest in caged hens, intermediate in organic reared hens and lowest in floor reared hens. It could be assumed that in the last one system birds have an adequate space in controlled environment that permits them to satisfy, though partially, their behavioural needs without the presence of different chronic stress factors acting in the other systems.

Moderate differences in circulating corticosterone alter receptor-mediated regulation of 5-hydroxytryptamine neuronal activity

Circulating glucocorticoid levels vary with stress and psychiatric illness and play a potentially important role in regulating transmitter systems that regulate mood. To determine whether chronic variation in corticosterone levels within the normal diurnal range altered the control of 5-hydroxytryptamine (5-HT) neuronal activity, male rats were adrenalectomized and implanted with either a 2% or 70% corticosterone/cholesterol pellet (100 mg). Two weeks later, the regulation of 5-HT neuronal activity in the dorsal raphe nucleus was studied by in vitro electrophysiology. At this time, serum corticosterone levels approximated the low-point (2%) and mid-point (70%) of the diurnal range. The excitatory response of 5-HT neurones to the alpha1-adrenoceptor agonist phenylephrine (1-11 microM) was significantly greater in the 2% group compared to the 70% group. By contrast, the inhibitory response to 5-HT (10-50 microM) was significantly lower in the 2% group compared to the 70% group. Thus, chronic variation in circulating corticosterone over a narrow part of the normal diurnal range causes a shift in the balance of positive and negative regulation of 5-HT neurones, with increased alpha 1-adrenoceptor-mediated excitation and reduced 5-HT-mediated autoinhibition at lower corticosterone levels. This shift would have a major impact on control of 5-HT neuronal activity.

Moderate differences in circulating corticosterone alter receptor-mediated regulation of 5-hydroxytryptamine neuronal activity

Circulating glucocorticoid levels vary with stress and psychiatric illness and play a potentially important role in regulating transmitter systems that regulate mood. To determine whether chronic variation in corticosterone levels within the normal diurnal range altered the control of 5-hydroxytryptamine (5-HT) neuronal activity, male rats were adrenalectomized and implanted with either a 2% or 70% corticosterone/cholesterol pellet (100 mg). Two weeks later, the regulation of 5-HT neuronal activity in the dorsal raphe nucleus was studied by in vitro electrophysiology. At this time, serum corticosterone levels approximated the low-point (2%) and mid-point (70%) of the diurnal range. The excitatory response of 5-HT neurones to the α1-adrenoceptor agonist phenylephrine (1-11 μM) was significantly greater in the 2% group compared to the 70% group. By contrast, the inhibitory response to 5-HT (10-50 μM) was significantly lower in the 2% group compared to the 70% group. Thus, chronic variation in circulating corticosterone over a narrow part of the normal diurnal range causes a shift in the balance of positive and negative regulation of 5-HT neurones, with increased α1-adrenoceptor-mediated excitation and reduced 5-HT-mediated autoinhibition at lower corticosterone levels. This shift would have a major impact on control of 5-HT neuronal activity.

P.1.15 GABA receptor modulation of 5-HT neuronal firing in the dorsal raphe nucleus and its sensitivity to moderate variations in corticosterone levels

P.1.15 GABA receptor modulation of 5-HT neuronal firing in the dorsal raphe nucleus and its sensitivity to moderate variations in corticosterone levels

Variation within and between Birds in Corticosterone Responses of Great Tits (Parus major)

The present study investigated inter- and intraindividual variation of the stress response (in terms of plasma levels of corticosterone) to handling in birds. Individual captive great tits (Parus major) were exposed to a standardised capture and handling protocol three times at about 2-week intervals. Mean plasma corticosterone levels were low (<5 ng/ml) when the birds were first sampled and increased in all birds 10 min after handling (mean levels on each sampling occasion 14 to 22 ng/ml). Levels in some birds then continued to increase, whereas in other birds levels remained relatively constant or had declined 30 min after handling began. Corticosterone responses were measured three times in each bird so that variation in plasma corticosterone levels could be defined. The area under the corticosterone response curve was defined as the integrated corticosterone response and was calculated for each response curve. Variation between birds was quantified by comparing mean values of corticosterone levels and integrated corticosterone responses between birds, then calculating a coefficient of variation for the mean of the individual bird means for each corticosterone parameter. Variation within birds was quantified by calculating the mean of the coefficients of variation for each bird for each corticosterone parameter. Variation in corticosterone levels in the first blood samples at 0 min (coefficient of variation (CV) 84.0%) was greater than variation in peak levels at 10 min (CV 35.1%) and in integrated corticosterone responses (CV 31.9%), indicating that corticosterone responses were more consistent between birds than were basal corticosterone levels. This study has demonstrated that corticosterone responses to a stressor tend to be repeatable in individual great tits, and has provided a method for quantifying variation in corticosterone responses for comparison with other birds in the future.

Chronic iodine deprivation attenuates stress-induced and diurnal variation in corticosterone secretion in female Wistar rats.

Many millions of people throughout the world are at risk of developing iodine deficiency-associated disorders. The underlying effects of iodine deficiency on neuroendocrine function are poorly defined. We have studied stress-induced and diurnal variation in corticosterone secretion in female rats rendered chronically hypothyroid by feeding them an iodine-free diet for 6 months. Corticosterone secretory responses in iodine deficient animals were compared to those seen in animals rendered hypothyroid with propylthiouracil and untreated controls. By using a well-validated, automated blood sampling system to collect small samples of blood over the complete daily cycle in unrestrained animals, we have demonstrated for the first time that the normal diurnal rhythm of corticosterone secretion is lost in chronic iodine deficiency and that the corticosterone secretory response to the psychological stress of 10 min exposure to white noise is attenuated. Despite restoration of circulating triiodothyronine and thyrotropin releasing hormone- and thyroid stimulating hormone beta-transcript prevalence in the hypothalamus and pituitary, respectively, 1 month after restoration of normal iodine-containing diet both the diurnal variation in corticosterone levels and the corticosterone secretory response to the noise stress remained reduced in amplitude compared to control animals. Thus, chronic hypothyroidism induced by iodine deficiency significantly attenuates hypothalamo-pituitary-adrenal axis activity, an effect that persists after functional recovery of the thyroid axis.

Effects of Weather on Corticosterone Responses in Wild Free-Living Passerine Birds

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.

Susceptibility to autoimmune disease and drug addiction in inbred rats. Are there mechanistic factors in common related to abnormalities in hypothalamic-pituitary-adrenal axis and stress response function?

DA and LEW inbred rats are extraordinarily susceptible to a wide range of experimental autoimmune diseases. These diseases include rheumatoid arthritis models such as collagen-induced arthritis (CIA) and adjuvant-induced arthritis (AIA), multiple sclerosis models such as myelin-basic-protein (MBP)-induced experimental autoimmune encephalomyelitis (MBP-EAE), and autoimmune uveitis models such as retinal S antigen (SAG) and interphotoreceptor-retinoid-binding-protein (IRBP)-induced experimental autoimmune uveitis (SAG-EAU and IRBP-EAU, respectively). DA and LEW rats are also addiction-prone to various drugs of abuse, such as cocaine. Moreover, they exhibit a variety of behavioral and biochemical characteristics that appear to be related to their susceptibility to addiction. By contrast, F344 and BN rats show quite different phenotypes. They are relatively resistant to CIA, AIA, MBP-EAE, SAG-EAU, and IRBP-EAU, and they are relatively resistant to addiction. Interestingly, both DA and LEW rats, in contrast to F344 and BN rats, have abnormalities in hypothalamic-pituitary-adrenal (HPA) axis function. For example, circadian production of corticosteroids is very abnormal in DA and LEW rats; that is, they exhibit minimal circadian variation in corticosterone levels. Since corticosteroids potentially have significant influences on immune function and autoimmune disease susceptibility and may also influence sensitivity to drugs of abuse, we have begun to dissect genetic control of these various phenotypic differences, focusing initially on the regulation of autoimmune disease expression. Using genomewide scanning techniques involving F2 crosses of DA x F344 (CIA and AIA), DA x BN (CIA), and LEW x F344 [IRBP-EAU and streptococcal-cell-wall arthritis (SCWA)], we have identified, to date, 14 genomic regions [quantitative trait loci (QTL)] that regulate disease expression in these crosses. Development and analysis of QTL-congenic rats involving these loci are in progress and should permit us to address the relationships among autoimmune disease susceptibility, drug addiction, and HPA axis and stress response function. These initial data, however, indicate that the genetic control of the autoimmune disease traits is highly complex.

Dark Agouti and Fischer 344 rats: differential behavioral responses to morphine and biochemical differences in the ventral tegmental area

We sought to identify behavioral and biochemical differences between Dark Agouti and Fischer 344 inbred rat strains to assess whether they could serve as a model of genetically determined differences in sensitivity to drugs of abuse. We compared the strains for the following traits: morphine-induced locomotor activity and sensitization; circadian variation in plasma levels of corticosterone, a hormone reported to affect sensitivity to drugs of abuse; and several biochemical parameters in the ventral tegmental area and nucleus accumbens, brain regions implicated in the locomotor activating and reinforcing actions of drugs of abuse. Fischer 344 rats exhibited greater initial locomotor responses to morphine but, unlike Dark Agouti rats, did not develop sensitization to a second morphine exposure. Fischer 344 rats displayed a marked rise in basal plasma corticosterone levels in the late light phase and early dark phase, whereas Dark Agouti rats showed no significant circadian variation in corticosterone levels. Relative to drug-naive Fischer 344 rats, drug-naive Dark Agouti rats showed higher levels of tyrosine hydroxylase and glial fibrillary acidic protein, and lower levels of neurofilament proteins, in the ventral tegmental area. In contrast, no strain differences were found in levels of tyrosine hydroxylase, specific G protein subunits or protein kinase A in the nucleus accumbens. Together, these results demonstrate that Dark Agouti rats and Fischer 344 rats exhibit differences in specific behavioral, endocrine and biochemical parameters related to sensitivity to drugs of abuse.

Perinatal hormone exposure alters the expression of selective affiliative preferences in prairie voles.

In the present study, perinatal administration of corticosterone and testosterone significantly influenced affiliative preferences only in females. Despite the very high levels of steroids given, no significant differences were noted among treated and untreated groups of males. Prairie voles apparently are uniquely adapted to tolerate high levels of endogenous steroids. However, females of this species may be capable of exploiting variations in corticosterone levels to regulate sexually dimorphic traits, including social behaviors, in adulthood. Perinatal responsivity to adrenal hormones could allow animals to adapt their social behaviors, including traits that have been used to characterize monogamy and/or communal breeding, to environmental demands.

Sex differences in adrenal function in the lizard Cnemidophorus sexlineatus: I. Seasonal variation in the field.

In order to document sex differences in adrenal function and how this relates to gonadal function during the period of seasonal activity, blood samples from male and female six-lined racerunners, Cnemidophorus sexlineatus, were taken immediately after capture in the field for determination of plasma corticosterone and gonadal steroid concentrations. Plasma testosterone and dihydrotestosterone levels for males, and 17 beta-estradiol and progesterone levels for females, were measured. Trends in the concentration of plasma corticosterone differed significantly between males and females. In males the highest concentrations of corticosterone were measured in late spring and the lowest concentrations were measured in late summer. Whereas half of the variation in corticosterone levels among males could be explained as seasonal change, less than 1% of the variation among females could be explained as seasonal change. In males plasma corticosterone and androgens exhibited similar seasonal decreases. Corticosterone levels for females were not correlated with progesterone or 17 beta-estradiol levels. Sex differences in seasonal variation in plasma corticosterone concentrations suggest that corticosterone may be involved in the different reproductive strategies and energy requirements of males and females during the seasonal period of activity.