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Foraging behavior, contaminant exposure risk, and the stress response in wild California condors (Gymnogyps californianus)
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.
... Condors reintroduced to Baja California may benefit from limited HOC exposure. 5,52 The nontargeted analysis presented here indicates that the largest known organic contaminant threat to coastal condors in California remains DDT and its metabolites. In 2014, ∼40% of breeding age coastal condors from central California were predicted to have levels of DDE associated with eggshell thinning. ...
... 9 Organochlorine exposure may also be related to increased glucocorticoid stress response, which can have physiological impacts on condors. 52 Furthermore, increased reintroduction to Baja California may limit lead exposure, since no condors in the BC flock have died of lead toxicosis in the last 5 years, compared to 17 coastal condors and 12 inland condors in California. 6,7,9,53−56 Although reintroduction site selection and successful condor recovery depend on multiple factors, the reduced potential for lead and HOC contamination in Baja California, compared to the California coast, highlights the value of this site. ...
Coastal reintroduction sites for California condors (Gymnogyps californianus) can lead to elevated halogenated organic compound (HOC) exposure and potential health impacts due to the consumption of scavenged marine mammals. Using nontargeted analysis based on comprehensive two-dimensional gas chromatography coupled to time-of-flight mass spectrometry (GC×GC/TOF-MS), we compared HOC profiles of plasma from inland and coastal scavenging California condors from the state of California (CA), and marine mammal blubber from CA and the Gulf of California off Baja California (BC), Mexico. We detected more HOCs in coastal condors (32 ± 5, mean number of HOCs ± SD, n = 7) than in inland condors (8 ± 1, n = 10) and in CA marine mammals (136 ± 87, n = 25) than in BC marine mammals (55 ± 46, n = 8). ∑DDT-related compounds, ∑PCBs, and total tris(chlorophenyl)methane (∑TCPM) were, respectively, ∼7, ∼3.5, and ∼148 times more abundant in CA than in BC marine mammals. The endocrine-disrupting potential of selected polychlorinated biphenyls (PCB) congeners, TCPM, and TCPMOH was determined by in vitro California condor estrogen receptor (ER) activation. The higher levels of HOCs in coastal condors compared to those in inland condors and lower levels of HOC contamination in Baja California marine mammals compared to those from the state of California are factors to consider in condor reintroduction efforts.
... 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. ...
Glucocorticoid hormones (GCs) help vertebrates maintain homeostasis during and following challenging events. Short-term elevations in GC levels are necessary for survival, whereas longer-term changes can lead to reduced reproductive output and immunosuppression. Persistent environmental contaminants (ECs) are widespread globally. Experimental exposure of individuals to ECs is associated with varying GC responses, within, and across, species and contaminants. Individuals exposed to ECs over long durations are expected to have prolonged GC elevations, which likely affect their health. We conducted a meta-analysis to test for a relationship between fish GC levels and experimental exposure to ECs, and to explore potential moderators, including duration of exposure, that could help explain the variation in effect sizes within and between studies. We report almost exclusively on cortisol responses of teleost fish to ECs. Although there was much variation in effect sizes, captive-bred fish exposed to ECs had baseline GC levels 1.5× higher than unexposed fish, and fish exposed to pharmaceuticals (estradiols and stimulants being mainly considered) had baseline GC levels approximately 2.5× higher than unexposed fish. We found that captive-bred and wild-caught fish did not differ in GC levels after exposure to the same classes of ECs - studies on captive bred fish may thus enable inferences about GC responses to ECs for wild species. Furthermore, effect sizes did not differ between baseline and challenge-induced GC measures. In different analyses, duration of exposure was negatively correlated to effect size, suggesting that the GC response may acclimate after chronic exposure to some ECs which could potentially alter the GC response of EC-exposed fish to novel stressors. Future studies should explore the effect of multiple stressors on the fish GC response and perform tests on a broader array of contaminant types and vertebrate classes.
Lead (Pb) poisoning is a significant threat to Aotearoa New Zealand's endangered kea (Nestor notabilis), an avian species important to Māori. Historically, exposure was thought to be from lead‐containing building materials; however, recent field observations suggest lead‐based ammunition as an additional source. We used stable lead isotopes to investigate the sources of lead to kea. Comparing ²⁰⁷ Pb/206 Pb ratios in kea blood (n = 91) to both ammunition and building materials, we found approximately one‐third of exposed kea (blood lead > 10 µg/dL) had lead isotope ratios consistent with exposure to lead‐based ammunition. As lead ammunition is still used, including in government‐sponsored culling programs, our data indicate an urgent need to shift toward non‐lead ammunition use to prevent further poisoning and aid conservation efforts. Collaborating with tangata whenua/Māori guardians, we advocate for immediate policy changes to eliminate lead‐based ammunition in kea habitat to safeguard this endangered culturally treasured species from extinction.
Bearded vulture (Gypaetus barbatus) populations are declining worldwide primarily due to anthropogenic factors. A captive breeding program has been established in Spain, a country with one of the largest free-living populations in Europe, to further enhance the conservation efforts of this emblematic species. However, captive vulture populations can be exposed to different risks through food, such as drug residues and antimicrobial-resistant (AMR) bacteria. Health surveillance of species involved in captive breeding programs is important to face introduction of healthy animals in situ and to obtain baseline clinical data. The objective of this study was to assess the general health status of bearded vultures held in captivity in Catalonia (northeastern Spain) by carrying out hematologic, biochemical, toxicologic, and bacteriologic analyses. A total of 16 bearded vultures were sampled; the data obtained from one vulture, with a chronic tibiotarsal fracture, were excluded from the statistical analysis. Hematologic and biochemical parameters of the bearded vultures were mostly within the range of standard values as stated in previous studies. Basal feather and serum corticosterone levels were analyzed and described for the first time in this species. A total of 15 Escherichia coli isolates were obtained that were resistant to fluoroquinolones (80%), tetracycline (60%), trimethoprim and ampicillin (40%), sulfamethoxazole (33%), and colistin (20%), with 40% of them being multidrug resistant. Three of 15 isolates were carriers of the mcr-1 gene. Only the injured bird previously treated with enrofloxacin was positive for fluoroquinolone residues. Periodic monitoring for the presence of AMR bacteria would be recommended in captive breeding programs as a preventive action to establish future therapies.
The endangered California condor (Gymnogyps californianus) is negatively affected by lead poisoning from spent lead-based hunting ammunition. Because lead poisoning is the primary mortality factor affecting condors, the California Fish and Game Commission banned lead hunting ammunition during 2008 in the southern California condor range followed by a statewide ban implemented in 2019. In contrast, the Arizona Game and Fish Department instituted an outreach and awareness program encouraging voluntary use of nonlead hunting ammunition in the northern portion of the state during 2005 and a similar program was launched in Utah during 2012. The juxtaposition of policy tools provided a unique opportunity to evaluate the intended efforts to mitigate lead exposure in condors and their respective positive and negative effects. Herein we reflect upon the effectiveness of lead policy actions in the 3-state region on the basis of condor blood-lead levels, population status, and hunter awareness of the issue and use of nonlead hunting ammunition.
Lead exposure is a concern in urban ecosystems, with physiological and behavioral effects well documented in humans. Wildlife inhabiting urban ecosystems are also exposed to lead, yet little work has documented the sublethal effects of lead exposure in urban wildlife. We studied northern mockingbirds (Mimus polyglottos) in three neighborhoods of New Orleans, Louisiana, two with high soil lead and one with low soil lead, to better understand how lead exposure may influence mockingbirds' reproductive biology. We monitored nesting attempts, measured lead concentrations in blood and feathers of nestling mockingbirds, documented egg hatching and nesting success, and assessed rates of sexual promiscuity in relation to neighborhood soil lead levels. We found that nestling mockingbirds' blood and feather lead levels reflected the lead levels of their neighborhood soil lead level and nestling blood lead levels were similar to adult mockingbirds in the same neighborhoods. Nest success, as evaluated by daily survival rates, was higher in the lower lead neighborhood. Clutch sizes varied substantially across neighborhoods, but rates of unhatched eggs did not covary with neighborhood lead levels, suggesting that other drivers are influencing variation in clutch sizes and hatching success in urban habitats. At least one-third of nestling mockingbirds were sired by an extra-pair male, and there was no relationship between extra-pair paternity rates and neighborhood lead levels. This study provides insight on how lead contamination may influence reproduction in urban-dwelling wildlife and suggests that nestling birds could serve as useful bioindicators of lead levels in urban neighborhoods.
Context
Existing demographic models of California condors have not simultaneously considered individual condor movement paths, the distribution and juxtaposition of release sites, habitat components, or the spatial distribution of threats.
Objectives
Our objectives were to develop a dynamic spatially explicit and individual-based model (IBM) of California condor demography and to evaluate its ability to replicate empirical data on demography and distribution from California (1995–2019).
Methods
We built a female-only spatially explicit California condor IBM in HexSim, using a daily timestep that allowed us to simulate the foraging behavior of condors, changes in food distribution and availability, and the ephemeral threat of lead in decaying food resources.
Results
Simulated population size was highly correlated with annual population census data once the population became established with > 50 females ( r ² = 0.99). Mean simulated fecundity and mortality estimates were not significantly different from empirical trends ( p > 0.05), although empirical data had higher interannual variability. The geographic distribution of modeled condors was similar to the empirical distribution with an overall accuracy of 79%, a commission error of 27%, and an omission error of 9%. Simulated movement density corresponded moderately well to the density of observed GPS locations (weighted kappa = 0.44).
Conclusions
We developed a spatially explicit California condor IBM that is well-calibrated to empirical data from California. Given its mechanistic underpinnings and flexibility to incorporate a variety of spatial and demographic inputs, we expect our model to be useful for assessing the relative risks and benefits of future condor reintroduction and management scenarios.
Using a commercially available corticosterone I125 double-antibody radioimmunoassay, we developed and validated an assay procedure for determining corticosterone levels in small-volume (≤30 μL) avian plasma samples. We evaluated this procedure's utility by measuring plasma corticosterone levels in Indigo Buntings (Passerina cyanea), American Goldfinches (Carduelis tristis), Red-eyed Vireos (Vireo olivaceus), and Mourning Doves (Zenaida macroura). Standard biochemical validations (e.g., parallelism, recovery of exogenous corticosterone) demonstrated that the assay accurately and precisely measured corticosterone in avian plasma. We used a stress capture protocol to physiologically validate the assay's ability to determine biologically important changes in corticosterone levels. Males and females from four bird species exhibited a significant increase in plasma corticosterone in response to capture, handling, and restraint. Baseline and stress-induced corticosterone levels in our study were similar to reported values for other passerine species using other radioimmunoassay procedures. Our results suggest that this radioimmunoassay procedure is very effective for determining corticosterone levels in small-volume avian plasma samples and is sensitive enough to detect biologically important changes in the adrenocortical activity of birds. Thus, this assay has considerable utility for measuring stress levels and stress responses in small birds (<15 g), from which only small volumes of plasma (≤30 μL) can be collected.
Utilización de un Radioinmunoensayo Disponible Comercialmente para la Cuantificación de Corticosterona en el Plasma de Aves
Resumen. Desarrollamos y validamos un proceso de ensayo para determinar los niveles de corticosterona en muestras de pequeño volúmen (≤30 μL) de plasma de aves utilizando un radioinmunoensayo para corticosterona I125 de doble anticuerpo disponible comercialmente. Evaluamos este procedimiento midiendo los niveles de corticosterona en Passerina cyanea, Carduelis tristis, Vireo olivaceus y Zenaida macroura. Validaciones bioquímicas estándares (e.g., paralelismo, recuperación de corticoesteroide exógeno) demostraron que el ensayo midió de modo exacto y preciso la corticosterona en el plasma de las aves. Utilizamos un protocolo de captura que producía estrés para validar fisiológicamente la habilidad del ensayo de detectar cambios biológicamente importantes en los niveles de corticosterona. Hembras y machos de las cuatro especies de aves mostraron un incremento significativo en los niveles de corticosterona en el plasma en respuesta a la captura, manipulación y retención. Los niveles basales e inducidos por el estrés de nuestro estudio fueron similares a valores reportados para otras especies paserinas que utilizaron otros procedimientos de inmunoensayo. Nuestros resultados sugieren que este procedimiento de radioinmunoensayo es muy efectivo para determinar los niveles de corticosterona en muestras de pequeño volúmen de plasma de aves y que es suficientemente sensible como para detectar cambios biológicamente importantes en la actividad adenocortical de las aves. De esta manera, este ensayo presenta considerable utilidad para medir los niveles y respuesta al estrés en aves pequeñas (<15 g) de las cuales sólo es posible colectar pequeños volúmenes de plasma (≤30 μL).
Corticosterone (CORT) is a glucocorticoid hormone that maintains energy balance and can modulate foraging behaviors in seabirds. However, CORT responses are not always predictable under similar biophysical conditions and do not necessarily influence the same behaviors across breeding stages and species. To enhance our understanding of CORT's role as a proximate determinant of foraging behavior and energy maintenance, we examined the relationships between body condition, CORT, foraging behavior, and foraging success between two sympatric breeding albatross species with differing foraging strategies and life histories, the Campbell albatross (Thalassarache impavida) and the gray-headed albatross (Thalassarache chrysostoma), from Campbell Island, New Zealand. Pre- and postforaging CORT did not differ between species or stage, potentially as a result of behavioral plasticity or different functional roles of CORT across stages. Unexpectedly, body condition did not correlate with preforaging CORT during incubation, although a negative correlation was observed in Campbell albatrosses during the guard stage. Furthermore, CORT mediated foraging success in both species and stages, but CORT mediated foraging behavior only in incubation-stage Campbell albatrosses that had shorter foraging ranges with higher pretrip CORT. Additionally, CORT positively correlated with mass gain and the time elapsed since the last feeding event in guard-stage albatrosses. Our results highlight the complexity of CORT in mediating energy balance in free-ranging animals. Our results also support that if CORT is to be usefully interpreted, breeding stage must be considered because the physiological and behavioral functionality of CORT may differ across stages, with enhanced sensitivity to energy reserves during chick rearing.
Vertebrates respond to stressful stimuli with the secretion of glucocorticoid (GC) hormones, such as corticosterone (CORT), and measurements of these hormones in wild species can provide insight into physiological responses to environmental and human-induced stressors. California condors (Gymnogyps californianus) are a critically endangered and intensively managed avian species for which information on GC response to stress is lacking. Here we evaluated a commercially available I¹²⁵ double antibody radioimmunoassay (RIA) and an enzyme-linked immunosorbent assay (ELISA) kit for measurement of CORT and GC metabolites (GCM) in California condor plasma, urate, and feather samples. The precision and accuracy of the RIA assay outperformed the ELISA for CORT and GCM measurements, and CORT and GCM values were not comparable between the two assays for any sample type. RIA measurements of total CORT in condor plasma collected from 41 condors within 15 minutes of a handling stressor were highly variable (median = 70 ng/mL, range = 1–189 ng/mL) and significantly different between wild and captive condors (p = 0.02, two-tailed t-test, n = 10 wild and 11 captive). Urate GCM levels (median = 620 ng/g dry wt., range = 0.74–7200 ng/g dry wt., n = 216) significantly increased within 2 hr of the acute handling stressor (p = 0.032, n = 11 condors, one-tailed paired t-test), while feather section CORT concentrations (median = 18 pg/mm, range = 6.3–68 ng/g, n = 37) also varied widely within and between feathers. Comparison of multiple regression linear models shows condor age as a significant predictors of plasma CORT levels, while age, sex, and plasma CORT levels predicted GCM levels in urates collected within 30 min of the start of handling. Our findings highlight the need for validation when selecting an immunoassay for use with a new species, and suggest that non-invasively collected urates and feathers hold promise for assessing condor responses to acute or chronic environmental and human-induced stressors.
Glucocorticoid (GC) levels vary with environmental conditions, but the functional interpretation of GC variation remains contentious. A primary function is thought to be metabolic, mobilizing body reserves to match energetic demands. This view is supported by temperature-dependent GC levels, although reports of this effect show unexplained heterogeneity. We hypothesised that the temperature effect on GC concentrations will depend on food availability through its effect on the energy spent to gather the food needed for thermoregulation. We tested this hypothesis in zebra finches living in outdoor aviaries with manipulated foraging conditions (i.e. easy vs. hard), by relating within-individual differences in baseline GCs between consecutive years to differences in ambient temperature. In agreement with our hypothesis, we found the GC-temperature association to be significantly steeper in the hard foraging environment. This supports the metabolic explanation of GC variation, underlining the importance of accounting for variation in energy expenditure when interpreting GC variation.
The critically endangered California condor (Gymnogyps californianus) has relied intermittently on dead-stranded marine mammals since the Pleistocene and this food source is considered important for their current recovery. However, contemporary marine mammals contain persistent organic pollutants that could threaten condor health. We used stable carbon and nitrogen isotope, contaminant, and behavioral data in coastal versus non-coastal condors to quantify contaminant transfer from marine mammals and created simulation models to predict the risk of reproductive impairment for condors from exposure to DDE (p,p'-DDE), a major metabolite of the chlorinated pesticide DDT. Coastal condors had higher whole blood isotope values and 12 to 100-fold greater mean concentrations of contaminants associated with marine mammals, including mercury (whole blood), sum chlorinated pesticides (comprised of ~95% DDE) (plasma), sum polychlorinated biphenyls (PCBs) (plasma), and sum polybrominated diphenyl ethers (PBDEs) (plasma), than non-coastal condors. The mean plasma DDE concentration for coastal condors was 500±670SD (n=22) versus 25±23SD (n=8) ng/g wet weight for non-coastal condors and simulations predicted ~40% of breeding-age coastal condors have DDE levels associated with eggshell thinning in other avian species. Our analyses demonstrate potentially harmful levels of marine contaminant transfer to California condors, which could hinder the recovery of this terrestrial species.
Researchers typically study "acute" activation of the hypothalamic-pituitary-adrenal (HPA) axis by measuring levels of circulating glucocorticoids in animals that have been exposed to a predator, a cue from a predator (e.g., odor), or have experienced a standardized capture-and-restraint protocol, all of which are many minutes in duration. However, exposure to predators in the "wild" either as the subject of an attack or as a witness to an attack, is generally much shorter as most depredation attempts upon free-living animals last <5s. Yet, whether a stimulus lasting only seconds can activate the HPA axis is unknown. To determine if a stimulus of a few seconds triggers a glucocorticoid response, we measured levels of corticosterone (CORT; the primary avian glucocorticoid) in wild-caught European starlings (Sturnus vulgaris) after they witnessed a brief (< 2-8s) raptor attack upon a conspecific, a human "attack" (i.e., a researcher handling a conspecific), and an undisturbed control. Witnesses of a raptor attack responded with CORT levels comparable to that induced by a standardized capture-and-restraint protocol. Glucocorticoid levels of individuals following the control treatment were similar to baseline levels, and those that witnessed a human "attack" had intermediate levels. Our results demonstrate that witnessing a predator attack of very brief duration triggers a profound adrenocortical stress response. Given the considerable evidence of a role for glucocorticoids in learning and memory, such a response may affect how individuals learn to recognize and appropriately react to predators.
Lead poisoning is a primary factor impeding the survival and recovery of the critically endangered California Condor (Gymnogyps californianus). However, the frequency and magnitude of lead exposure in condors is not well-known in part because most blood lead monitoring occurs biannually, and biannual blood samples capture only 10% of a bird’s annual exposure history. We investigated the use of growing feathers from free-flying condors in California to establish a bird’s lead exposure history. We show that lead concentration and stable lead isotopic composition analyses of sequential feather sections and concurrently collected blood samples provided a comprehensive history of lead exposure over the 2−4 month period of feather growth. Feather analyses identified exposure events not evident from blood monitoring efforts, and by fitting an empirically derived timeline to actively growing feathers, we were able to estimate the time frame for specific lead exposure events. Our results demonstrate the utility of using sequentially sampled feathers to reconstruct lead exposure history. Since exposure risk in individuals is one determinant of population health, our findings should increase the understanding of population-level effects from lead poisoning in condors; this information may also be helpful for other avian species potentially impacted by lead poisoning.
Endangered species recovery programs seek to restore populations to self-sustaining levels. Nonetheless, many recovering species require continuing management to compensate for persistent threats in their environment. Judging true recovery in the face of this management is often difficult, impeding thorough analysis of the success of conservation programs. We illustrate these challenges with a multidisciplinary study of one of the world's rarest birds-the California condor (Gymnogyps californianus). California condors were brought to the brink of extinction, in part, because of lead poisoning, and lead poisoning remains a significant threat today. We evaluated individual lead-related health effects, the efficacy of current efforts to prevent lead-caused deaths, and the consequences of any reduction in currently intensive management actions. Our results show that condors in California remain chronically exposed to harmful levels of lead; 30% of the annual blood samples collected from condors indicate lead exposure (blood lead ≥ 200 ng/mL) that causes significant subclinical health effects, measured as >60% inhibition of the heme biosynthetic enzyme δ-aminolevulinic acid dehydratase. Furthermore, each year, ∼20% of free-flying birds have blood lead levels (≥450 ng/mL) that indicate the need for clinical intervention to avert morbidity and mortality. Lead isotopic analysis shows that lead-based ammunition is the principle source of lead poisoning in condors. Finally, population models based on condor demographic data show that the condor's apparent recovery is solely because of intensive ongoing management, with the only hope of achieving true recovery dependent on the elimination or substantial reduction of lead poisoning rates.
In situations where limited knowledge of a system exists and the ratio of data points to variables is small, variable selection
methods can often be misleading. Freedman (Am Stat 37:152–155, 1983) demonstrated how common it is to select completely unrelated
variables as highly “significant” when the number of data points is similar in magnitude to the number of variables. A new
type of model averaging estimator based on model selection with Akaike’s AIC is used with linear regression to investigate
the problems of likely inclusion of spurious effects and model selection bias, the bias introduced while using the data to
select a single seemingly “best” model from a (often large) set of models employing many predictor variables. The new model
averaging estimator helps reduce these problems and provides confidence interval coverage at the nominal level while traditional
stepwise selection has poor inferential properties.
The relationship between stress and disease is thought to be unambiguous: chronic stress induces immunosuppression, which likely increases the risk of infection. However, this link has not been firmly established in wild animals, particularly whether stress hormones affect host responses to zoonotic pathogens, which can be transmitted to domesticated animal, wildlife and human populations. Due to the dynamic effects of stress hormones on immune functions, stress hormones may make hosts better or poorer amplifying hosts for a pathogen contingent on context and the host species evaluated. Using an important zoonotic pathogen, West Nile virus (WNV) and a competent host, the Northern Cardinal (Cardinalis cardinalis), we tested the effects of exogenous corticosterone on response to WNV infection. Corticosterone was administered at levels that individuals enduring chronic stressors (i.e., long-term inclement weather, food shortage, anthropogenic pollution) might experience in the wild. Corticosterone greatly impacted mortality: half of the corticosterone-implanted cardinals died between five - 11 days post-inoculation whereas only one of nine empty-implanted (control) birds died. No differences were found in viral titer between corticosterone- and empty-implanted birds. However, cardinals that survived infections had significantly higher average body temperatures during peak infection than individuals that died. In sum, this study indicates that elevated corticosterone could affect the survival of WNV-infected wild birds, suggesting that populations may be disproportionately at-risk to disease in stressful environments.
In addition to seasonal changes in morphology, physiology and behavior that occur in predictable annual cycles, there are facultative responses to unpredictable events known as labile (i.e., short-lived) perturbation factors (LPFs). These rapid behavioral and physiological changes have been termed the "emergency" life history stage (ELHS) and serve to enhance life-time fitness. Glucocorticosteroids interacting with other hormones in the hypothalamo-pituitary-adrenal (HPA) cascade, initiate and orchestrate the ELHS within minutes to hours. Components of the ELHS include: redirection of behavior from a normal life history stage to increased foraging, irruptive-type migration during the day, enhanced restfulness at night, elevated gluconeogenesis and recovery once the perturbation passes. These physiological and behavioral changes allow an individual to avoid potential deleterious effects of stress that may result from chronically elevated levels of circulating glucocorticosteroids over days and weeks. In other words, acute rises in glucocorticosteroids following perturbations of the environment may actually avoid chronic stress and serve primarily as "anti-stress" hormones. Several field studies in diverse habitats indicate that free-living populations have elevated circulating levels of corticosteroids when in an ELHS. However, expression of an ELHS may not always be advantageous and there is accumulating evidence from birds that the adrenocortical responses to LPFs are modulated both on seasonal and individual levels. These data suggest that glucocorticosteroid secretions in response to LPFs not only trigger physiological and behavioral responses but also allow flexibility so that the response is integrated in relation to time of year (normal LHS) as well as individual differences owing to body condition, disease and social status.
Evaluating corticosterone (CORT) responses to stress in free-living vertebrates requires knowing the unstressed titers prior to capture. Based upon laboratory data, the assumption has been that samples collected in less than 3 min of capture will reflect these unstressed concentrations. This assumption was tested for six species using samples collected from 945 individuals at 0-6 min after capture. Samples were from five avian species trapped at multiple times of year and one reptilian species, comprising a total of 14 different data sets for comparisons. For seven of 14 data sets, including five species, there was no significant increase in corticosterone titers within 3 min of capture. In six of the 14 data sets, corticosterone titers increased significantly after 2 min, and in one data set, the increase started at 1.5 min. In all seven of the cases showing an increase before 3 min, however, corticosterone titers from the time of increase to 3 min were significantly lower than titers after 30 min of restraint stress. These results indicate a high degree of confidence for these species that samples collected in less than 2 min reflect unstressed (baseline) concentrations, and that samples collected from 2-3 min also will likely reflect baseline concentrations but at worst are near baseline.
Ecotourism is increasing worldwide; hence, it is important to know how wildlife are affected behaviorally and physiologically by human visitation. We studied the effects of human visitation on the Magellanic Penguins (Spheniscus magellanicus) at Punta Tombo, Argentina, by monitoring changes in defensive head turns and plasma corticosterone (a hormone secreted in response to stress) for penguins with and without a history of tourist visitation. Habituation to human visitation was rapid. In penguins with no previous exposure to tourists, the number of defensive head turns and level of plasma corticosterone decreased significantly within 5 days of one 15-minute visit/day. Penguins living in tourist-visited and undisturbed areas secreted more corticosterone when captured and restrained than penguins visited by a person. Penguins in tourist areas, however did not show as strong a corticosterone response to capture and restraint as did penguins in areas without tourists. This difference was due to a decreased capability of the adrenocortical tissue to secrete corticosterone in tourist-visited birds. Although our data show no direct negative effects of tourism on Magellanic Penguins at Punta Tombo, consequences of a modification of physiological capabilities (e.g., adrenocortical function) may not become apparent until much later in life. The physiological differences between tourist-visited and undisturbed groups of Magellanic Penguins emphasize the importance of monitoring the effects of anthropogenic disturbances on wildlife at multiple levels.
Endocrine parameters have proven useful in the detection of early or low-level responses to pollutants. Although most of the studies on endocrine modulation have been focused on processes involving gonadal steroids, contaminants may target other parts of the endocrine system as well. In this study we examined the adrenocortical stress response and thyroid hormone status in free-living nestling white storks (Ciconia ciconia) in relation to heavy metals (zinc, lead, copper, cadmium) and arsenic levels in blood.
Fieldwork was conducted in an area polluted by the Aznalcóllar mine accident (southwestern Spain) and in a reference site. We used a standardized capture, handling, and restraint protocol to determine both baseline and maximum plasma corticosterone. Circulating levels of thyroxine (T4) and triiodothyronine (T3) were also measured.
No effects of metals or As were found on baseline corticosterone, but maximum levels of corticosterone were positively related to Pb in both locations. This relationship was stronger in single nestlings than in birds from multiple-chick broods, which suggests a greater impact of Pb on more stressed individuals. Metal pollution did not affect plasma T4 or T3 levels, although thyroid status differed with location.
Because a compromised hypothalamus-pituitary-adrenal (HPA) function can have far-reaching consequences in terms of altered behavioral and metabolic processes necessary for survival, our results suggest that birds exposed to sublethal Pb levels may be at risk through an altered adrenocortical stress response, and further support the idea that HPA axis-related end points might be useful indicators of metal exposure and potential toxicity in wild animals.
Persistent organic pollutants (POPs) have the potential to impair the endocrine regulation of organisms and alter their ability to respond to environmental changes. We studied whether polychlorinated biphenyls
(PCBs) and organochlorine pesticides (OCPs) affected the endocrine regulation of free-living and captive red kites (Milvus milvus) through studying the dynamics of corticosterone (CORT) and dehydroepiandrosterone (DHEA). We sampled migratory free-living kites coming from northern Europe and captive kites born in a rehabilitation center in Spain. We used body feathers from the interscapular region as a minimally-invasive and integrative matrix. The most abundant compound detected in freeliving kites was 4,40-dichlorodiphenyldichloroethylene (4,40-DDE; 6.10 ± 1.56 ng g-1 dw feather) followed by CB-153 (3.10 ± 0.63 ng g-1 dw feather) and CB-180 (2.43 ± 1.08 ng g-1 dw feather). In captive kites, the most abundant compounds were 4,40-dichlorodyphenyltrichloroethane (4,40-DDT; 2.38 ± 1.30 ng g-1 dw feather), CB-153 (2.15 ± 0.47 ng g-1 dw feather) and hexachlorobenzene (HCB; 2.03 ± 0.45 ng g-1 dw feather) at similar concentrations. Free-living kites showed higher levels of 4,40-DDE and CB-180 in comparison to captive kites. Age influenced HCB and CB-101 levels, whereas body mass was inversely related to CB-180 and 4,40-DDT. Interestingly, captive kites showed a ratio DDT/DDE higher than 1 suggesting a relatively recent exposure of DDT, in contrast to free-living kites. Regarding hormonal levels, free-living kites showed higher levels of CORT (3.30 ± 0.22 pg mm-1 feather) than captive (2.40 ± 0.16 pg mm-1 feather), reflecting higher allostatic load. In addition, a positive association between PCBs and DDTs and adrenal hormones was found in free-living kites, suggesting an increase of CORT as a response of the endocrine system to cope with stressors and a subsequent elevation of DHEA to ameliorate the potential negative effects that high CORT levels could cause to the organism.
Increased glucocorticoids cause a characteristic stress leukogram in mammalian taxa. It is assumed that avians exhibit a similar response, but to date, there have been no controlled studies to correlate serial endogenous corticosterone levels to hematologic values. An established flock of 18 Hispaniolan Amazon parrots ( Amazona ventralis) was used as a model in a crossover study. The treatment group was subjected to the stress of transport, restraint, and common clinical procedures with serial blood samples collected at 20-min intervals for hematology and corticosterone levels; the control group was sampled at the same intervals. Longitudinal data analysis was performed with linear mixed modeling. For all hematologic analytes, the baseline value had a significant positive effect on subsequent values (all P < 0.001). The white blood cell, heterophil, and eosinophil counts and heterophil to lymphocyte ratio increased over time in the treatment group, whereas it remained stable in the control group ( P = 0.016, P < 0.001, P < 0.001, P = 0.02, respectively, for the time*treatment effect). Lymphocyte absolute counts decreased over time, although not significantly; the decrease was significant for the relative lymphocyte count in the treatment group. Monocytes and basophils were not significantly altered. The treatment group had a higher mean corticosterone level overall than the control group by approximately 60% ( P = 0.008). The mean corticosterone level also increased over time in both groups by three- to fourfold ( P < 0.001) by 20 min then plateaued. These results demonstrate that some significant hematologic changes may arise with routine handling and transportation of birds and should be accounted for in hematologic interpretation of cell counts.
People living a subsistence lifestyle in the Arctic are highly exposed to persistent organic pollutants, including polychlorinated biphenyls (PCBs). Formerly Used Defense (FUD) sites are point sources of PCB pollution; the Arctic contains thousands of FUD sites, many co-located with indigenous villages. We investigated PCB profiles and biological effects in freshwater fish (Alaska blackfish [Dallia pectoralis] and ninespine stickleback [Pungitius pungitius]) living upstream and downstream of the Northeast Cape FUD site on St. Lawrence Island in the Bering Sea. Despite extensive site remediation, fish remained contaminated with PCBs. Vitellogenin concentrations in males indicated exposure to estrogenic contaminants, and some fish were hypothyroid. Downstream fish showed altered DNA methylation in gonads and altered gene expression related to DNA replication, response to DNA damage, and cell signaling. This study demonstrates that, even after site remediation, contaminants from Cold War FUD sites in remote regions of the Arctic remain a potential health threat to local residents - in this case, Yupik people who had no influence over site selection and use by the United States military.
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.
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.
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.
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.
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.
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.
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.
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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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.