Lead poisoning of raptors: state of the science and cross-discipline mitigation options for a global problem.

Lead poisoning is an important global conservation problem for many species of wildlife, especially raptors. Despite the increasing number of individual studies and regional reviews of lead poisoning of raptors, it has been over a decade since this information has been compiled into a comprehensive global review. Here, we summarize the state of knowledge of lead poisoning of raptors, we review developments in manufacturing of non-lead ammunition, the use of which can reduce the most pervasive source of lead these birds encounter, and we compile data on voluntary and regulatory mitigation options and their associated sociological context. We support our literature review with case studies of mitigation actions, largely provided by the conservation practitioners who study or manage these efforts. Our review illustrates the growing awareness and understanding of lead exposure of raptors, and it shows that the science underpinning this understanding has expanded considerably in recent years. We also show that the political and social appetite for managing lead ammunition appears to vary substantially across administrative regions, countries, and continents. Improved understanding of the drivers of this variation could support more effective mitigation of lead exposure of wildlife. This review also shows that mitigation strategies are likely to be most effective when they are outcome driven, consider behavioural theory, local cultures, and environmental conditions, effectively monitor participation, compliance, and levels of raptor exposure, and support both environmental and human health.

Chlamydia psittaci Screening of Animal Workers from Argentina Exposed to Carrier Birds.

Different syndromes are involved in human psittacosis (flu-like syndrome, atypical pneumonia up to lacrimal gland lymphoma). Diagnostic methods include serology, culture, and PCR. The rate of Chlamydia psittaci (Cp) positive tests among exposed workers is still unknown. Our study aimed to assess the rate of positive tests among workers who have contact with carrier birds in natural reserves from Buenos Aires, Argentina. Secondary aims were to analyze risk factors linked to these outcomes and the occurrence of signs that suggest psittacosis. Nasopharyngeal swabs and serum pairs were collected from employees who had interacted with confirmed carrier birds. Those with detectable DNA of Cp and/or anti-Chlamydia spp. antibody baseline titer ≥ 160 mUI/ml, or at least quadruplicating, were considered positive. Activities performed with or near birds, personal protective equipment use, and previous chronic conditions were assessed. Possible Cp-related pathologies were evaluated during follow-up. A total of 63 exposed workers (71.4% men) with a median age of 35.7 years (IQR 26-39) were evaluated to detect 28.6% positives. Respiratory chronic conditions were the unique factor associated with positive tests (OR 5.2 [1.5-18.5] p < .05). Surprisingly, about a third of the workers resulted positive and all responded to medical treatment, none developing an acute atypical pneumonia syndrome associated with classical presentation of psittacosis. Active testing for early diagnosis and proper treatment in zoological workers exposed to carrier or potentially carrier birds is strongly suggested as part of zoonotic diseases preventive measures.

Neutralization of "Chaco eagle" (Buteogallus coronatus) serum on some activities of Bothrops spp. venoms.

Several species of reptiles and mammals have components in their sera that can neutralize toxic components present in snake venoms. In this manuscript, we studied the neutralizing capacity of Chaco eagle's (Buteogallus coronatus) serum. This South American bird of prey eats snakes as a regular part of its diet and has anatomical features that protect from snakes' bites. The neutralizing potency of the Chaco eagle's serum was tested on lethal, hemorrhagic, procoagulant, and phospholipase activities of the venom of "yarará grande" (Bothrops alternatus) and on phospholipase activity of "yarará ñata" (Bothrops ammodytoides) venom; both snakes are known to be the prey of Chaco eagle. Sera of crested caracara (Caracara plancus-a scavenger, omnivorous pan-American bird of prey), secretary bird (Saggitarius serpentarius-an omnivorous bird of prey from Africa that can include venomous snakes in its diet), common hen (Gallus gallus), rat (Rattus norvegicus), mouse (Mus musculus), horse (Equus caballus), and dog (Canis lupus familiaris) were also tested to compare the inhibitory capacity of neutralization. To test isologous and xenologous neutralization, sera from Bothrops alternatus and white-eared opossum (Didelphis albiventris), respectively, were used due to their known inhibitory activity on Bothrops venoms. As a control for the neutralization activity, antibothropic antivenom was used. Chaco eagle's serum neutralized hemorrhagic and phospholipasic activity and slightly neutralized the coagulation and the lethal activity of Bothrops spp. venom. The neutralizing capacity was present in the non-immunoglobulin fraction of the serum, which showed components of acidic characteristics and lower molecular weight than IgY, in correspondence with the characteristics of PLA2s and SVMPs inhibitors described in sera from some snakes and mammals. These studies showed that Chaco eagle's serum neutralizes all toxic activities tested at a higher level than sera from animal species in which inhibitors of snake venoms have not been described (p < 0.05), while it is lower or similar in neutralizing capacity to white-eared opossum and B. alternatus sera.

Veterinary pharmaceuticals as a threat to endangered taxa: Mitigation action for vulture conservation.

Overuse and misapplication of veterinary pharmaceuticals affect the ecosystem, even at low concentrations. Vultures are mainly exposed to these compounds when feeding on improperly disposed carcasses from animals treated before death. This produces diverse negative impacts on vulture health and populations, even leading to death. Using the available bibliography we determined which veterinary pharmaceuticals vultures are exposed to worldwide and assessed the potential consequences for these species. Based on the responsibilities of the different stakeholders, we also propose action to mitigate this problem. Of 104 articles addressing vulture exposure to veterinary pharmaceuticals, most came from Asia, Europe and Africa; almost no information was available on the Americas. Vultures were reported as being exposed to non-steroidal anti-inflammatory drugs (NSAIDs), antibiotics, anti-parasitic and euthanizing agents. Most available information is related to the catastrophic effect of the NSAID diclofenac in South Asia. Vultures are particularly exposed to veterinary drugs when ingesting carcasses from intensive livestock production, but other potential pathways (e.g., discards from salmon farms or fisheries) have not yet been properly evaluated. It is essential to improve scientific information on this topic - increasing the range of drugs and geographical areas studied - in order to implement sustainable conservation action for these birds. A combination of strategies could prove effective in reducing the impact of pharmaceuticals on the environment and non-target species. To mitigate this conservation problem, a set of multilateral actions should therefore be implemented, involving diverse stakeholders such as government representatives, pharmaceutical companies, veterinary practitioners, scientists and conservation agents, and local communities.

Pharmacokinetic Behaviour of Enrofloxacin after Single Intramuscular Dosage in American Black Vultures (Coragyps atratus).

The aim of the study was to investigate the intramuscular pharmacokinetics of enrofloxacin in black vultures (Coragyps atratus). The pharmacokinetics of a single intramuscular dose (10 mg/kg) of enrofloxacin was studied in six vultures. Plasma concentrations of enrofloxacin and its active metabolite, ciprofloxacin, were determined by high-performance liquid chromatography (HPLCuv). Pharmacokinetic parameters were estimated using non-compartmental and compartmental analysis. After intramuscular administration, enrofloxacin showed a rapid and complete absorption, reaching a Cmax value of 3.26 ± 0.23 µg/mL at 1.75 ± 0.53 h. A long terminal half-life of 19.58 h has been observed. Using previously published MIC values to perform a PK/PD analysis, cumulative fraction responses obtained after Monte Carlo simulation for AUC/MIC > 30, 50 and 125 were 72.93%, 72.34% and 30.86% for E. coli and 89.29%, 88.89% and 58.57% for Mycoplasma synoviae, respectively. Cumulative fraction responses obtained for Cmax/MIC index were 33.93% and 40.18% for E. coli and M. synoviae, respectively. The intramuscular administration of 10 mg/kg could be appropriate to treat infectious diseases caused by gram-positive bacteria with MIC value lower than 1 µg/mL; however, although enrofloxacin showed a slow elimination in black vultures, plasma concentrations were insufficient to reach the gram-negative stablished breakpoints.

Exposure to Anthropogenic Areas May Influence Colonization by Zoonotic Microorganisms in Scavenging Birds.

Wild bird species have commonly been implicated as potential vectors of pathogens to other species, humans included. However, the habitat where birds live could influence the probability to acquire these pathogens. Here, we evaluated if the characteristics of the environment used by obligate scavenging birds (vultures) influence their colonization by zoonotic pathogens. For this, we particularly focused on Salmonella spp., a zoonotic pathogen commonly present in bird species. The occurrence of this bacteria was evaluated in free ranging Andean condors (Vultur gryphus) using natural environments from Argentina and compared with those obtained from condors under human care. In addition, we compared our results with those reported for other wild vultures using natural and anthropized environments at a global scale. We did not find Salmonella spp. in samples of wild condors. Captive condor samples presented Salmonella spp. with an occurrence of 2.8%, and one isolate of Meticilin Resistant Staphylococcus aureus, among other potential pathogenic microorganisms. Moreover, some species of free ranging vultures from diverse geographical areas using anthropized environments tend to present higher occurrences of Salmonella spp. These results highlight the importance of pristine ecosystems to protect vultures' health toward pathogenic microorganisms that can produce disease in these birds, but also in other species. We call for more studies evaluating differences in occurrence of zoonotic pathogens in vultures according to the quality of the environment they use. Even when vultures have not been implicated in zoonotic pathogen spread, our results add information to evaluate potential events of pathogen spillover between vultures and from these birds to other species.

Plasma carotenoids and immunity in a despotic avian scavenger.

Carotenoids are pigmented compounds acquired through diet that have important functions as antioxidants and immune modulators. We studied the association between immunity and circulating carotenoids in Andean condors (Vultur gryphus). We evaluated the relationship between α-, ß-, and γ-globulin blood concentrations and different circulating carotenoids in two groups of Andean condors that differ in their mean health status, rehabilitating (suffering different pathologies), and wild individuals (trapped when displaying their physiological behavior). In rehabilitating individuals, α-, ß-, and γ-globulin concentrations were higher than in wild individuals. This shows that rehabilitating individuals were developing an immune response associated with the pathologies that they were suffering at the time of sampling. In addition, circulating carotenoids were lower in rehabilitating than in wild individuals. We found negative correlations between α-, ß-, and γ-globulins and different circulating carotenoids in rehabilitating individuals, but not in wild condors. Xanthophylls were strongly related to α-, ß-, and γ-globulin blood concentrations in rehabilitating, but not in wild condors. Our results suggest that there is a potential relationship between circulating carotenoids and immunity in the Andean condor. Given that this species may display a carotenoid-based pigmentation, our results could suggest that a trade-off between the immune system and external coloration could operate in this species, which may have implications in their access to food resources and mate selection and, thus, in their conservation.

Protein electrophoresis in Andean condors (Vultur gryphus): Reference values and differences between wild and rehabilitating individuals.

The study of wildlife health greatly contributes to understanding population dynamics and detecting conservation threats. The determination of the different fractions of plasma proteins (proteinogram) is an important laboratory tool to study wildlife health. The aim of this study was to characterize protein electrophoresis in wild Andean condors (Vultur gryphus) from north-western Patagonia and to evaluate differences according to age and sex classes. Once reference values of wild, apparently healthy individuals, were established, we compared these values to those of individuals received at the Buenos Aires Zoo in Argentina for rehabilitation due to various health problems. Reference proteinograms from wild Andean condors differed only in the α 1 and ß 2-fractions between sex categories. Males showed higher concentrations of these protein fractions than females. We found clear differences between wild birds and rehabilitating individuals. Total proteins, globulins, α 1-globulins, total α-globulins, ß 2-globulins, total ß-globulins, and γ-globulins were significantly higher in rehabilitating than in wild individuals, whereas albumin, α 2, and ß1-globulins were similar between these groups. The albumin/globulin ratio, as a general indicator of health, was significantly lower in rehabilitating than in wild individuals. The results indicate the effects on different protein fractions of pathologic processes occurring in individuals undergoing rehabilitation. Our results provide useful insights, contributing to improving diagnoses and prognoses in this species. This information may also be useful to assess the health status of Andean condors in studies of wild populations and for comparisons with other bird species.

Evaluation of allometric scaling as a tool for extrapolation of the enrofloxacin dose in American black vultures (Coragyps atratus).

OBJECTIVE: To determine the pharmacokinetics of enrofloxacin after IV administration in American black vultures (Coragyps atratus), to compare clearance of enrofloxacin in American black vultures with clearance of this fluoroquinolone in other avian species, and to evaluate whether allometric scaling is an appropriate tool for dose extrapolation in avian species. ANIMALS: 6 healthy adult American black vultures. PROCEDURES: Enrofloxacin concentrations were quantified by use of high-performance liquid chromatography. Pharmacokinetics of enrofloxacin was determined in American black vultures after IV administration. Pharmacokinetic parameters for 12 avian species obtained from 24 pharmacokinetic studies were used. Allometric analysis of enrofloxacin pharmacokinetic parameters was performed. RESULTS: Volume of distribution at steady state for enrofloxacin was 3.47 L/kg, clearance was 0.147 L/h·kg, and elimination half-life was 18.3 hours. Comparisons among avian species revealed that American black vultures had the lowest extraction ratio for enrofloxacin (1.04%). Only the volume of distribution at steady state and clearance had a good allometric fit. Goodness of fit was improved when ratites were not included in the analysis. CONCLUSIONS AND CLINICAL RELEVANCE: Results suggested that the use of allometric scaling for the prediction of volume of distribution at steady state could provide a suitable method for extrapolation of enrofloxacin doses among avian species; however, allometric scaling could not be used to adequately predict the clearance of enrofloxacin.

Tracking data and retrospective analyses of diet reveal the consequences of loss of marine subsidies for an obligate scavenger, the Andean condor.

Over the last century, marine mammals have been dramatically reduced in the world's oceans. We examined evidence that this change caused dietary and foraging pattern shifts of the Andean condor (Vultur gryphus) in Patagonia. We hypothesized that, after the decrease in marine mammals and the increase in human use of coastlines, condor diet changed to a more terrestrial diet, which in turn influenced their foraging patterns. We evaluated the diet by means of stable isotope analysis (δ13C, δ15N and δ34S) of current (last decade) and historical (1841-1933) feathers. We further evaluated the movement patterns of 23 condors using satellite tracking of individuals. Condors reduced their use of marine-derived prey in recent compared with historical times from 33 ± 13% to less than 8 ± 3% respectively; however, they still breed close to the coast. The average distance between the coast and nests was 62.5 km, but some nests were located close to the sea (less than 5 km). Therefore, some birds must travel up to 86 km from nesting sites, crossing over the mountain range to find food. The worldwide reduction in marine mammal carcasses, especially whales, may have major consequences on the foraging ecology of scavengers, as well as on the flux of marine inputs within terrestrial ecosystems.

Repeated conservation threats across the Americas: High levels of blood and bone lead in the Andean Condor widen the problem to a continental scale.

Wildlife lead exposure is an increasing conservation threat that is being widely investigated. However, for some areas of the world (e.g., South America) and certain species, research on this subject is still scarce or only local information is available. We analyzed the extent and intensity of lead exposure for a widely distributed threatened species, the Andean Condor (Vultur gryphus). We conducted the study at two different scales: 1) sampling of birds received for rehabilitation or necropsy in Argentina, and 2) bibliographic review and extensive survey considering exposure event for the species' distribution in South America. Wild condors from Argentina (n = 76) presented high lead levels consistent with both recent and previous exposure (up to 104 µg/dL blood level, mean 15.47 ± 21.21 µg/dL and up to 148.20 ppm bone level, mean 23.08 ± 31.39 ppm). In contrast, captive bred individuals -not exposed to lead contamination- had much lower lead levels (mean blood level 5.63 ± 3.08 µg/dL, and mean bone level 2.76 ± 3.06 ppm). Condors were exposed to lead throughout their entire range in continental Argentina, which represents almost sixty percent (>4000 km) of their geographical distribution. We also present evidence of lead exposure events in Chile, Ecuador, and Peru. Lead poisoning is a widespread major conservation threat for the Andean Condor, and probably other sympatric carnivores from South America. The high number and wide range of Andean Condors with lead values complement the results for the California Condor and other scavengers in North America suggesting lead poisoning is a continental threat. Urgent actions are needed to reduce this poison in the wild.

Need and seek for dietary micronutrients: endogenous regulation, external signalling and food sources of carotenoids in new world vultures.

Among birds, vultures show low concentrations of plasma carotenoids due to the combination of their large size, general dull colouration and a diet based on carrion. We recorded the concentration of each carotenoid type present in plasma of the Andean condor (Vultur gryphus) according to age and sex, that determine colour signalling and dominance hierarchies in the carcasses. We compared the carotenoid profile in wild condors with that of captive condors fed with a controlled diet of flesh to test the hypothesis that wild individuals could acquire extra carotenoids from vegetal matter contained in carcass viscera and fresh vegetation. Wild American black vultures (Coragyps atratus) were also sampled to evaluate the potential influence of colouration in the integument on absorption and accumulation patterns of plasma carotenoids. A remarkably higher concentration of lutein than ß-carotene was found in wild condors, while the contrary pattern was recorded in American black vultures and captive condors. We found a consistent decrease in all plasma carotenoids with age, and a lower concentration of most xanthophylls in male compared to female wild condors. Positive correlations of all carotenoids indicated general common absorption and accumulation strategies or a single dietary source containing all pigments found in plasma. The comparatively low total concentration of carotenoids, and especially of lutein rather than ß-carotene, found in captive condors fed with a diet restricted to flesh supports the hypothesis that Andean condors can efficiently acquire carotenoids from vegetal matter in the wild. Andean condors seem to be physiologically more competent in the uptake or accumulation of xanthophylls than American black vultures, which agrees with the use of colour-signalling strategies in sexual and competitive contexts in the Andean condor. This study suggests that vultures may use dietary vegetal supplements that provide pigments and micronutrients that are scarce or missing in carrion.

Electrocardiography in conscious releasable Andean condors (Vultur gryphus): reference panel and unusual findings.

Electrocardiography is a useful tool when included in healthcare protocols and is increasingly utilized for monitoring wild birds. However, the lack of reference data for many species is limiting the clinical value of this technique. In this study 26 Andean condors (Vultur gryphus) coming from rehabilitation and captive breeding programs were examined to determine electrocardiographic references prior to being released. Standard bipolar (I, II, and III) and augmented unipolar limb (aVR, aVL, and aVF) leads were recorded with birds under physical restraint. Five beats were analyzed on Lead II at 50 mm/sec and 1 cm = 1 mV to determine QRS complex morphology, cardiac rhythm, heart rate, P, PR, R, S, QRS, T, QT, and ST amplitude and/or duration. P and T wave configuration was determined for all leads, and Mean Electrical Axis (MEA) in the frontal plane was determined using leads I and III. Cardiac rhythm corresponded to regular sinus rhythm in 42% of the birds, with a relevant rate of sinus arrhythmia in 58%, and rS as the most common pattern (42%) for QRS complex in lead II. We found an influence of age and heart rate but not of sex on several ECG waves and intervals. Relevant ECG findings for studied Andean condors include a high rate of T(a), R', and U wave detection. Waves T(a) and R' were considered non-pathological, while the significance of U waves remains unclear. Our results provide a useful reference to improve clinical interpretation of full electrocardiographic examination in Andean condors.