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Foraging behavior, contaminant exposure risk, and the stress response in wild California condors (Gymnogyps californianus)

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Abstract

Wild California condors (Gymnogyps californianus) are frequently exposed to lead via lead-based ammunition ingestion, and recent studies indicate significant exposure to organochlorines (e.g. dichlorodiphenyldichloroethylene (DDE) and polychlorinated biphenyls (PCBs)) for condors feeding on beach-cast marine mammals. We investigated the influence of contaminant exposure on condor glucocorticoid response through comparisons between wild and captive populations and identified modifiers of glucocorticoid release. We assessed the glucocorticoid response to routine trapping and handling events through measurement of plasma corticosterone and urate glucocorticoid metabolites (GCM). Comparison of peak urate GCM levels showed wild condors exhibited higher responses to handling-associated stressors (2250 ± 1440 ng/g dry wt, average +/- SD, n=27) than captive condors (907 ± 489 ng/g dry wt., n=6, U = 28, p = 0.003). Multiple linear regression models and an information theoretic approach (AICc) identified several extrinsic variables (e.g., time captive in flight pen before sample collection) that were negatively associated with plasma corticosterone and urate GCM levels in wild condors, which explained ∼25% of glucocorticoid variation. When accounting for these extrinsic variables we found that behavioral variables associated with increased lead and organochlorine exposure risk were positively associated with GCM levels, explaining an additional 15% of glucocorticoid variation among wild condors. Days absent from management area, a variable associated reduced survival attributed to increased lead exposure risk, had a positive influence on plasma corticosterone levels (β = 53 ± 20 SE) and peak urate GCM levels (β = 1090 ± 586 SE). Years observed feeding on marine mammals, a variable positively associated with DDE and PCB exposure, positively influenced peak urate GCM (β = 1100 ± 520 SE) and the magnitude of GCM response (peak GCM – 1st urate GCM) (β = 1050 ± 500 SE). Our findings suggest that individual propensities for these higher risk foraging behaviors predict higher stress-induced glucocorticoid levels in wild condors, and that accounting for variables associated with trapping and handling is essential for assessing the impact of environmental stressors such as contaminants on the condor stress response. As an abnormal glucocorticoid response to stress is associated with reduced reproduction and survival in vertebrates, this work indicates the critical need for further investigations into the physiological impacts of sub-lethal contaminant exposures in scavenging species worldwide.

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... Our results support previous studies showing that GC release rates are similar between wild and captive populations of vertebrates. For example, a recent study conducted using California condors (Gymnogyps californianus) found no significant difference in plasma GC levels between wild and captive condors after routine trapping and handling procedures (Glucs et al., 2020). However, other studies have provided contradictory results; Fanson et al. (2012) showed that fecal GC metabolite concentrations were high in captive lynx (Lynx canadensis) compared to wild lynx. ...
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The hypothalamic-pituitary-adrenal (HPA) axis has been studied extensively in adults, but the HPA axis in early life is not well characterized, and there is an immense amount of unexplained variation in glucocorticoid levels during early life, especially in wild animals. To characterize population-wide natural variation in early-life HPA axis function, we compared plasma corticosterone levels (at baseline and after 30 min acute restraint-stress) from seven-day-old nestlings (n = 123) from a free-living, marked population of Savannah sparrows (Passerculus sandwichensis). We found a surprising sensitivity of the HPA axis to timing of sample collection across time scales. Even within the accepted 3-min framework to collect baseline samples, time to collect blood had a significant effect on baseline corticosterone concentrations. Daily rhythms also influenced baseline levels, which increased significantly during the relatively short window of sample collection (1100 and 1600). On a broader timeframe, there was a strong effect of hatch date (over a 2 month period) on HPA axis responsiveness, where nestlings hatched later in the breeding season had lower stress-induced corticosterone levels than those hatched earlier. The ecophysiological mechanisms and implications of these patterns warrant future investigation; meanwhile this study highlights the critical need to consider, and potentially restrict, time across scales when collecting blood samples from wild birds to assess stress physiology.
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Carry-over effects in migratory birds are likely mediated by physiological processes that are activated in response to environmental variation. Such processes affect body condition and/or reproductive success, and can include corticosterone (CORT) because this hormone responds to environmental stressors and influences energy balance. Few studies have considered how CORT levels during non-breeding relate to a broader physiological profile during subsequent breeding, and fewer still have considered measures other than body condition. To explore CORT's potential role in carry-over effects, we investigated the relationship between CORT and foraging ecology of northern gannets (Morus bassanus) during the non-breeding period, and tested for associations between these factors and variation in a suite of physiological and biochemical metrics during subsequent breeding. Northern gannets are the largest seabird top predator in the North Atlantic and were among the hardest hit by the Deepwater Horizon oil blowout in the Gulf of Mexico in 2010. We used light-level geolocators to confirm winter origins of individuals in our study. No interrelationships were found among levels of CORT from feathers grown during non-breeding (CORTf) and variation in foraging ecology, measured by stable isotopes of carbon (δ¹³C) and nitrogen (δ¹⁵N) from the same feathers. CORTf was correlated negatively with hematocrit and positively with triglyceride measured during subsequent incubation, and explained more variation in these variables than did body mass during incubation. These findings provide support for the hypothesis that energy management, measured using CORTf, during non-breeding carries over to influence physiological measures other than body condition. Gannets that previously wintered within the Gulf of Mexico in the years following the Deepwater Horizon oil blowout had higher levels of CORTf compared to birds that wintered along the Atlantic coast, suggesting an increased energetic cost associated with visiting the Gulf of Mexico. Our results indicate that CORT during non-breeding is associated with a broader physiological profile during subsequent breeding than previously reported in birds.
Article
Glucocorticoid hormones facilitate responses to environmental challenges by mediating diverse physiological and behavioral changes, including resource mobilization and altered reproductive effort. Elevated glucocorticoids might indicate that an individual is facing high levels of environmental challenges and thus, elevated concentrations might be associated with reduced fitness (CORT-fitness hypothesis). Alternatively, the energetic demands of reproduction might be a challenge that requires elevated glucocorticoids to mobilize resources to support reproductive effort, ultimately increasing reproductive investment and fitness (CORT-adaptation hypothesis). Investigations of glucocorticoid-fitness relationships have yielded mixed results. Variation in the direction of this relationship could be caused in part by differences in the contexts in which the relationship was assessed. Incorporating context, such as life history stage, could be key to understanding the role of glucocorticoids in influencing fitness outcomes. We investigated the relationship between corticosterone and reproductive effort and success within a single life history stage: incubation of eggs. In an observational study, we measured baseline corticosterone in incubating female red-winged blackbirds (Agelaius phoeniceus), monitored incubation behavior, and determined hatching success for each nest. Incubating birds with higher baseline corticosterone concentrations had more frequent, shorter incubation bouts and spent less time overall incubating their clutches of eggs than birds with lower corticosterone concentrations. Elevated corticosterone was also associated with lower clutch mass, but neither corticosterone nor incubation effort were correlated with hatching success. Although experimental tests are needed to establish causation, these results suggest that during the incubation period, corticosterone might shift resource investment towards self-maintenance, and away from current reproductive effort.
Article
Translocation is an increasingly important tool for managing endangered species, but factors influencing the survival of translocated individuals are not well understood. Here we examine intrinsic and extrinsic drivers of survival for critically endangered California condors (Gymnogyps californianus) whose wild population recovery is reliant upon releases of captively bred stock. We used known fate models and information-theoretic methods to compare the ability of hypothesized covariates, most of which serve as proxies for lead exposure risk, to predict survival rates of condors in California. Our best supported model included the following predictors of survival: age of the recovery program, precipitation, proportion of days observed feeding on proffered carcasses, maximum blood lead concentration over the preceding 18 months, and time since release. We found that as flocks have increased in size and age, condors are increasingly likely to range more widely and less likely to be observed feeding on proffered food, and these “wilder” behaviors were associated with lower survival. After accounting for these behaviors, we found a positive survival trend, which we attribute to ongoing improvements in management. Our findings illustrate that the survival of translocated animals, such as highly social California condors, is influenced by behaviors that change through time.
Article
Stress hormones (i.e., glucocorticoids such as corticosterone and cortisol) have been widely proposed as biomarkers of habitat quality and disturbance. However, there is growing evidence that baseline glucocorticoid (GC) levels are highly context-dependent, potentially confounding their utility for inferring population-level disturbance depending on the life history stage and the duration, severity, and type of environmental change being measured. Determining which aspects of an organism's environment are consistently reflected by baseline GC levels is therefore of paramount importance to establishing how they may be best suited to conservation monitoring goals. We investigated the relationship between baseline GC levels and three extrinsic (food availability, inter-specific nest competition, intra-specific competition) and two intrinsic (reproductive investment, body condition) environmental contexts in breeding female tree swallows (Tachycineta bicolor) at two reproductive stages. We combined this with a manipulation of energetic demand (i.e., a decrease in foraging profitability) to determine whether baseline GCs reflect the extrinsic or intrinsic environment when females are faced with an unexpected disturbance. Baseline GC levels were not reflective of any environmental component in control females, regardless of reproductive stage. However, levels increased and were reflective of a decrease in body mass when females were challenged during the offspring provisioning period. Our findings suggest that baseline GCs may not always be indicative of the environmental contexts we associate with variation in habitat quality, particularly when individuals are operating within their expected energetic demand. In a conservation sense, baseline GCs may be more valuable in reflecting unexpected perturbations, which could limit their applicability as sensitive, predictive biomarkers across a diversity of systems.
Article
As use of Akaike's Information Criterion (AIC) for model selection has become increasingly common, so has a mistake involving interpretation of models that are within 2 AIC units (ΔAIC ≤ 2) of the top-supported model. Such models are <2 ΔAIC units because the penalty for one additional parameter is 2 AIC units, but model deviance is not reduced by an amount sufficient to overcome the 2-unit penalty and, hence, the additional parameter provides no net reduction in AIC. Simply put, the uninformative parameter does not explain enough variation to justify its inclusion in the model and it should not be interpreted as having any ecological effect. Models with uninformative parameters are frequently presented as being competitive in the Journal of Wildlife Management, including 72 of all AIC-based papers in 2008, and authors and readers need to be more aware of this problem and take appropriate steps to eliminate misinterpretation. I reviewed 5 potential solutions to this problem: 1) report all models but ignore or dismiss those with uninformative parameters, 2) use model averaging to ameliorate the effect of uninformative parameters, 3) use 95 confidence intervals to identify uninformative parameters, 4) perform all-possible subsets regression and use weight-of-evidence approaches to discriminate useful from uninformative parameters, or 5) adopt a methodological approach that allows models containing uninformative parameters to be culled from reported model sets. The first approach is preferable for small sets of a priori models, whereas the last 2 approaches should be used for large model sets or exploratory modeling.
Article
Lead is a prominent and highly toxic contaminant with important impacts to wildlife. To understand the degree to which wildlife populations are chronically exposed, we quantified lead levels within American black vultures (Coragyps atratus; BLVU) and turkey vultures (Cathartes aura; TUVU), two species that are useful as environmental sentinels in eastern North America. Every individual sampled (n=108) had bone lead levels indicative of chronic exposure to anthropogenic lead (BLVU: x¯=36.99±55.21mg Pb/kg tissue (±SD); TUVU: x¯=23.02±18.77mg/kg). Only a few showed evidence of recent lead exposure (BLVU liver: x¯=0.78±0.93mg/kg; TUVU liver: x¯=0.55±0.34mg/kg). Isotopic ratios suggested multiple potential sources of lead including ammunition, gasoline, coal-fired power plants, and zinc smelting. Black and turkey vultures range across eastern North America, from Quebec to Florida and individuals may traverse thousands of kilometers annually. The extent to which vultures are exposed suggests that anthropogenic lead permeates eastern North American ecosystems to a previously unrecognized degree. Discovery of an epidemic of chronic lead exposure in such widespread and common species and the failure of soft-tissue sampling to diagnose this pattern has dramatic implications for understanding modern wildlife and human health concerns. Copyright © 2015 Elsevier Ltd. All rights reserved.
Article
Glucocorticoid (GC) hormones, i.e. corticosterone (CORT) in birds, support physiological homeostasis and facilitate adaptations to stressful situations. However, maintaining high GC levels are energetically costly and interfere with other physiological processes. To keep the balance of costs and benefits of GC hormones, various mechanisms act to adapt GC levels to environmental conditions on different timescales, i.e. over generations, between parents and their offspring and within the life-time of a single individual. We elucidated whether two strains (domesticated and wild) of grey partridges (Perdix perdix) differed in the developmental trajectories of baseline and stress response CORT throughout the first 80 days of life. We also explored the potential of prenatal and postnatal factors, e.g. parental origin, predictable vs. unpredictable food treatments, individual and social factors to modify these trajectories. Baseline CORT was similar between strains and unaffected by perinatal food treatments. It was negatively related to body size and body condition. Conversely, the CORT stress response was not markedly affected by physiological condition. It was stronger in wild than in domesticated birds and it increased with age. Birds subjected to prenatal unpredictable food supply exhibited an accelerated development of the CORT stress response which could reflect an adaptive maternal effect. We conclude that the vital role of baseline CORT may allow little adaptive scope since changes can quickly become detrimental. In contrast, the CORT stress response may show considerable adaptive potential which might ultimately support homeostasis in a changing environment.
Article
From 1997 through 2010, in collaboration with the National Park Service, we released 84 captive-reared California Condors (Gymnogyps californianus) to the wild in central California; from 2006 through 2010 we recorded 16 nestings by nine pairs and recovered eggs or eggshell fragments from 12 nests. Mean thickness of shell fragments, without membrane, was 0.46 mm, 34% lower than the average thickness of 0.70 mm of fragments recovered from nine successful nests in interior southern California, 2007–2009. Hatching success in central California was 20–40%, significantly lower than the 70–80% recorded in southern California. The outer crystalline layer was absent or greatly reduced, as in thin-shelled condor eggs laid in southern California in the 1960s. Shell thickness was not related to egg size. Weight/water loss during incubation in the wild averaged three times greater than the normal rate associated with successful hatching; the rate of loss increased significantly with decreasing shell thickness. At least four failures, three from death of the embryo, we attribute to excessive weight/water loss; two other eggs losing substantial weight hatched successfully after artificial incubation at elevated humidities. DDT/DDE from wastes of a DDT factory discharged into the Southern California Bight had previously caused extensive eggshell thinning and reproductive failures of fish-eating and raptorial birds. Feeding on carcasses of California sea lions (Zalophus californianus), reintroduced condors now occupy a higher level of the food web. Like that of other species previously affected, the thickness of condor eggshells should recover as DDE contamination continues to decline. Desde 1997 hasta 2010, en colaboración con el Servicio de Parques Nacionales de los Estados Unidos, liberamos 84 individuos criados en cautiverio de Gymnogyps californianus en ambientes silvestres en el centro de California; desde 2006 al 2010 registramos 16 anidaciones por parte de nueve parejas y recuperamos huevos o fragmentos de cáscara de 12 nidos. El espesor medio de los fragmentos de la cáscara, sin la membrana, fue de 0.46 mm, 34% menos que el espesor medio de 0.70 mm de fragmentos recuperados de nueve nidos exitosos en el interior del sur de California, entre 2007 y 2009. El éxito de eclosión en el centro de California fue 20–40%, significativamente menor que el 70–80% registrado en el sur de California. La capa exterior cristalina estuvo ausente o muy reducida, como en los huevos de cóndor de cáscara fina puestos en el sur de California en los 1960s. El espesor de la cáscara no estuvo relacionado al tamaño del huevo. La relación peso/pérdida de agua durante la incubación en estado silvestre promedió tres veces más que la tasa normal asociada con el éxito de eclosión; la tasa de pérdida aumentó significativamente con la disminución del espesor de la cáscara. Al menos cuatro fracasos, tres debidos a la muerte del embrión, los atribuimos al exceso de peso/pérdida de agua; otros dos huevos que perdieron un peso substancial eclosionaron exitosamente luego de la incubación artificial realizada a humedades elevadas. DDT/DDE proveniente de desechos de una fábrica de DDT descargado en la Ensenada Sur de California había causado anteriormente el adelgazamiento generalizado de la cáscara del huevo y fracasos reproductivos de rapaces y aves alimentadas con peces. A partir de la ingestión de cadáveres de leones marinos de California (Zalophus californianus), los cóndores reintroducidos ocupan ahora un nivel más elevado en la red trófica. Al igual que el de otras especies afectadas previamente, el espesor de la cáscara de los huevos de cóndor debería recuperarse a medida que la contaminación con DDE continúa disminuyendo.
Article
Many scavenging bird populations have experienced abrupt declines across the globe, and intensive recovery activities have been necessary to sustain several species, including the critically endangered California condor (Gymnogyps californianus). Exposure to lead from lead-based ammunition is widespread in condors and lead toxicosis presents an immediate threat to condor recovery, accounting for the highest proportion of adult mortality. Lead contamination of carcasses across the landscape remains a serious threat to the health and sustainability of scavenging birds, and here we summarize recent evidence for exposure to lead-based ammunition and health implications across many species. California condors and other scavenging species are sensitive indicators of the occurrence of lead contaminated carcasses in the environment. Transdisciplinary science-based approaches have been critical to managing lead exposure in California condors and paving the way for use of non-lead ammunition in California. Similar transdisciplinary approaches are now needed to translate the science informing on this issue and establish education and outreach efforts that focus on concerns brought forth by key stakeholders.
Article
Birds of prey occupy high trophic levels and can consequently bioaccumulate high levels of environmental contaminants. To evaluate exposure to past- and current-use pollutants, we measured legacy contaminants (i.e., polychlorinated biphenyls [PCBs]; organochlorine pesticides, e.g., DDT), contaminants of emerging concern (polybrominated diphenyl ethers [PBDEs]; perfluorinated compounds [PFCs]), and stable isotopes (δ(13)C, δ(15)N) in 26 birds of prey (10 species) from coastal South Carolina (USA) sampled in 2009 and 2010. Nitrogen isotope ratios (δ(15)N) ranged from 5.2% to 13.7%, indicating the birds of prey spanned two to three trophic levels. Legacy contaminant levels were highly variable but generally comparable to levels reported previously for birds of prey in the southeast US, suggesting exposure has not declined substantially over the past 40 yr. Despite their status as newly emerging environmental contaminants, PFC levels were within the same order of magnitude as legacy contaminants. Although PBDEs were less prevalent, levels were among the greatest observed in wildlife to date (∑PBDEs max. 200 μg/g lipid). Relative contaminant profiles also varied between birds of prey utilizing low and high trophic levels; specifically PFCs contributed to a larger proportion of the contaminant burden in birds utilizing high trophic levels, whereas the legacy pesticide mirex was a larger contributor in low-trophic-level birds, indicating that relative exposure is in part dependent on foraging ecology. This study demonstrates that birds of prey continue to face exposure to legacy contaminants as well as newly emerging contaminants at levels of concern.
Article
ABSTRACT The scientific evidence that California condors (Gymnogyps californianus) are frequently sickened and killed by lead poisoning from spent ammunition supports the conclusion that current levels of lead exposure are too high to allow reintroduced condors to develop self-sustaining populations in the wild in Arizona and, by inference, in California. The evidence for lead poisoning and its source comes from the following sorts of data: 1) 18 clinical necropsies revealing high levels of lead in body tissues and (or) presence of lead shotgun pellets and bullet fragments in digestive tracts; 2) moribund condors showing crop paralysis and impending starvation with toxic levels of lead in their blood; 3) widespread lead exposure among free-flying condors, many with clinically exposed or acute levels; 4) temporal and spatial correlations between big game hunting seasons and elevated lead levels in condors; and 5) lead isotope ratios from exposed condors showing close similarity to isotope ratios of ammunition lead but isotope ratios in less exposed condors being similar to environmental background sources, which are different from ammunition lead. Simple population models reveal harmful demographic impacts of unnatural mortality from lead on population trajectories of reintroduced condors. Recent innovations in the manufacture of nonlead shotgun pellets and bullets with superior ballistics now provide for a simple solution to the problem of lead ingestion by condors, many other species of wildlife, and human beings: substitute nontoxic forms of ammunition for traditional lead-based ammunition. The substitution of nontoxic ammunition would be highly efficacious for hunting, economically feasible, and the right thing to do.
Article
Herbivore damage is generally detrimental to plant fitness, and the evolu- tionary response of plant populations to damage can involve either increased resistance or increased tolerance. While characters that contribute to resistance, such as secondary chem- icals and trichomes, are relatively well understood, characters that contribute to a plant's ability to tolerate damage have received much less attention. Using Helianthus annuus (wild sunflower) and simulated damage of Haplorhynchites aeneus (head-clipping weevil) as a model system, we examined morphological characters and developmental processes that contribute to compensatory ability. We performed a factorial experiment that included three levels of damage (none, the first two, or the first four inflorescences were clipped with scissors) and eight sires each mated to four dams. We found that plants compensated fully for simulated head-clipper damage and that there was no variation among plant families in compensatory ability: seed production and mean seed mass did not vary among treat- ments, and sire X treatment interactions were not significant. Plants used four mechanisms to compensate for damage: (1) Clipped plants produced significantly more inflorescences than unclipped plants. Plants produced these additional inflorescences on higher order branches at the end of the flowering season. (2) Clipped plants filled significantly more seeds in their remaining heads than did unclipped plants. (3) Clipped plants, because they effectively flowered later than unclipped plants, were less susceptible to damage by seed- feeding herbivores other than Haplorhynchites. (4) In later heads, seed size was greater on clipped plants, which allowed mean seed size to be maintained in clipped plants. Although there was genetic variation among the families used in this experiment for most of the characters associated with compensation for damage (seed number, mean seed size, mean flowering date, length of the flowering period, and branching morphology), in analyses of these characters, no sire X treatment interactions were significant indicating that all of the families relied on similar mechanisms to compensate for damage.
Article
We document causes of death in free-ranging California Condors (Gymnogyps californianus) from the inception of the reintroduction program in 1992 through December 2009 to identify current and historic mortality factors that might interfere with establishment of self-sustaining populations in the wild. A total of 135 deaths occurred from October 1992 (the first post-release death) through December 2009, from a maximum population-at-risk of 352 birds, for a cumulative crude mortality rate of 38%. A definitive cause of death was determined for 76 of the 98 submitted cases, 70% (53/76) of which were attributed to anthropogenic causes. Trash ingestion was the most important mortality factor in nestlings (proportional mortality rate [PMR] 73%; 8/11), while lead toxicosis was the most important factor in juveniles (PMR 26%; 13/50) and adults (PMR 67%; 10/15). These results demonstrate that the leading causes of death at all California Condor release sites are anthropogenic. The mortality factors thought to be important in the decline of the historic California Condor population, particularly lead poisoning, remain the most important documented mortality factors today. Without effective mitigation, these factors can be expected to have the same effects on the sustainability of the wild populations as they have in the past.
Article
In physiological studies of free-living species, it is essential to consider the context of the life history stage at which an individual was observed in order to link measures of physiology with ecological parameters. One such measure that is important to consider is the age of an individual. We tested whether baseline or stress-induced corticosterone levels vary with age in free-living Florida scrub-jays (Aphelocoma coerulescens) during the pre-breeding period. Corticosterone (CORT), the primary avian stress hormone, is released in response to stressful stimuli, and stimulates gluconeogenesis; however, it also serves as a chemical messenger that can influence other physiological processes, reproduction, and behavior. We monitored both baseline CORT levels longitudinally throughout a five-year period and stress-induced CORT responses over a shorter two-year period. We predicted that older jays would have lower baseline CORT levels and a dampened stress response compared to younger birds, as has been shown in other avian species. We found no significant differences in baseline CORT levels with age. We found a decrease in total corticosterone responses to a stressor with age, however, the oldest birds in the population showed greater total corticosterone responses to a stressor. These results may be a product of age-related changes in physiological processes related to the stress response or a result of selection acting on the population, resulting in only the most responsive individuals surviving to old age.
Article
The endangered, endemic Yellow-eyed penguin (Megadyptes antipodes) is one of the flagship species for New Zealand's wildlife tourism, and recently concern has been raised that tourism-related pressures may be becoming too great. We compared two neighbouring breeding areas exposed to different levels of human disturbance. Penguins at the site exposed to unregulated tourism showed significantly lower breeding success and fledging weights than those in an area visited infrequently for monitoring purposes only. High parental baseline corticosterone concentrations correlated with lower fledgling weights at both sites. Stress-induced corticosterone concentrations were significantly higher at the tourist-exposed site, suggesting birds have been sensitized by frequent disturbance. Consequences are likely to include reduced juvenile survival and recruitment to the tourist site, while the changed hormonal stress responses may ultimately have an effect on adult fitness and survival. For maintenance of attractive Yellow-eyed penguin-viewing destinations we recommend that tourists stay out of breeding areas and disturbance at penguin landing beaches is reduced.
Article
The diversity and specificity of glucocorticoid effects are dependent on cell-specific receptor mechanisms. Three known corticosteroid receptors mediate tissue effects of glucocorticoids in vertebrates: two intracellular receptors that act primarily as ligand-activated transcription factors, and a membrane-associated receptor. The intracellular receptor sub-types have been well characterized in mammals, however relatively little is known about them across non-mammalian vertebrates. The membrane-associated receptors are poorly characterized in most vertebrate taxa. To explore the basis for glucocorticoid action in birds, we pharmacologically characterized the three putative corticosteroid receptors in the brain, as well as a plasma corticosterone binding globulin, in the house sparrow (Passer domesticus). We found that house sparrow brain cytosol contained two distinguishable binding sites for corticosterone. A high affinity, mineralocorticoid-like receptor had subnanomolar affinity for corticosterone (K(d) approximately 0.2 nM). However, this 'MR-like' high-affinity receptor did not bind RU28318 or canrenoic acid, two compounds that bind mammalian MR with high affinity. A lower-affinity, glucocorticoid-like receptor in brain cytosol bound corticosterone with an average K(d)=5.61 nM. This GR-like receptor showed subnanomolar affinity for RU 486. MR- and GR-like receptors were found in equal numbers in whole brain assays (average B(max)=69 and 62 fmol/mg protein, respectively). House sparrow brain membranes contain a single binding site specific for glucocorticoids, with characteristics consistent with a steroid/receptor interaction. Corticosterone affinity for this putative membrane receptor was approximately 24 nM, with apparent B(max)=177 fmol/mg protein. House sparrow plasma contained a single binding site for [(3)H]corticosterone. Specific binding to plasma sites was inhibited by glucocorticoids, progesterone, and testosterone. Testosterone binding to this corticosteroid binding globulin is noteworthy as sex steroid-specific binding globulins have not been identified in birds. Taken together, these data extend our ability to evaluate the comparative actions of glucocorticoids, increase our understanding of mechanisms behind the tissue specificity of glucocorticoid action, and offer insight into the evolution of glucocorticoid action in vertebrates.
Article
Maintaining wild animals in captivity has long been used for conservation and research. While often suggested that captivity causes chronic stress, impacts on the underlying stress physiology are poorly understood. We used wild-caught chukar (Alectoris chukar) as a model avian species to assess how the initial 10 days of captivity alters the corticosterone (CORT) secretory pathway. In the first few days of captivity, birds lost weight, had lower hematocrit and demonstrated changes in CORT concentrations. Both baseline and restraint-stress-induced CORT concentrations decreased by days 3-5 of captivity and remained significantly lower throughout the 10 days although stress-induced concentrations began to recover by day 9. To delineate potential mechanisms underlying these CORT changes, we evaluated alterations to the hypothalamic-pituitary-adrenal (HPA) axis. Although chukar appear to be resistant to arginine vasotocin's (AVT) effects on CORT release, adrenocorticotropin hormone (ACTH) stimulated CORT release; however, ACTH stimulation did not differ during the 10 days of captivity. In contrast, negative feedback axis sensitivity, as determined by both dexamethasone suppression as well as endogenous negative feedback, decreased by day 5 but was regained by day 9. In addition, the combined stressors of capture and long distance transport eliminated the animals' ability to mount an acute CORT response on the day following the move. Therefore, introduction into captivity appeared to shift the chukar into a temporary state of chronic stress that began to recover within 9days. The duration of these alterations likely varies due to differences in capture techniques, transport distance, and species studied.
Article
Combined exposures to maternal lead (Pb) and prenatal stress (PS) can act synergistically to enhance behavioral and neurochemical toxicity in offspring. Maternal Pb itself causes permanent dysfunction of the body's major stress system, the hypothalamic pituitary adrenal (HPA) axis. The current study sought to determine the potential involvement of altered negative glucocorticoid feedback as a mechanistic basis of the effects in rats of maternal Pb (0, 50 or 150 ppm in drinking water beginning 2 mo prior to breeding), prenatal stress (PS; restraint on gestational days 16-17) and combined maternal Pb+PS in 8 mo old male and female offspring. Corticosterone changes were measured over 24 h following an i.p. injection stress containing vehicle or 100 or 300 microg/kg (females) or 100 or 150 microg/kg (males) dexamethasone (DEX). Both Pb and PS prolonged the time course of corticosterone reduction following vehicle injection stress. Pb effects were non-monotonic, with a greater impact at 50 vs. 150 ppm, particularly in males, where further enhancement occurred with PS. In accord with these findings, the efficacy of DEX in suppressing corticosterone was reduced by Pb and Pb+PS in both genders, with Pb efficacy enhanced by PS in females, over the first 6 h post-administration. A marked prolongation of DEX effects was found in males. Thus, Pb, PS and Pb+PS, sometimes additively, produced hypercortisolism in both genders, followed by hypocortisolism in males, consistent with HPA axis dysfunction. These findings may provide a plausible unifying biological mechanism for the reported links between Pb exposure and stress-associated diseases and disorders mediated via the HPA axis, including obesity, hypertension, diabetes, anxiety, schizophrenia and depression. They also suggest broadening of Pb screening programs to pregnant women in high stress environments.
Article
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.
Article
In recent years, the noninvasive monitoring of steroid hormone metabolites in feces of mammals and droppings of birds has become an increasingly popular technique. It offers several advantages and has been applied to a variety of species under various settings. However, using this technique to reliably assess an animal's adrenocortical activity is not that simple and straightforward to apply. Because clear differences regarding the metabolism and excretion of glucocorticoid metabolites (GCMs) exist, a careful validation for each species and sex investigated is obligatory. In this review, general analytical issues regarding sample storage, extraction procedures, and immunoassays are briefly discussed, but the main focus lies on experiments and recommendations addressing the validation of fecal GCM measurements in mammals and birds. The crucial importance of scrutinizing the physiological and biological validity of fecal GCM analyses in a given species is stressed. In particular, the relevance of the technique to detect biologically meaningful alterations in adrenocortical activity must be shown. Furthermore, significant effects of the animals' sex, the time of day, season, and different life history stages are discussed, bringing about the necessity to seriously consider possible sex differences as well as diurnal and seasonal variations. Thus, comprehensive information on the animals' biology and stress physiology should be carefully taken into account. Together with an extensive physiological and biological validation, this will ensure that the measurement of fecal GCMs can be used as a powerful tool to assess adrenocortical activity in diverse investigations on laboratory, companion, farm, zoo, and wild animals.