THE IMPACT OF SUPPLEMENTARY FEEDING OF PIG CARCASSES ON PLASMA VITAMIN E CONCENTRATIONS IN CAPTIVE CAPE VULTURES (GYPS COPROTHERES).

With vulture population numbers on the decline globally, many countries resort to supplementary feeding to maintain colony health. Despite what is perceived as adequate feeding in South Africa, colonies are still characterized by poor breeding success. One reason could be that supplementary sites fail to meet micronutrient needs of birds. With results from zoological gardens indicating that some carcasses are low in their vitamin E concentrations, vitamin deficiencies may be an underlying problem. For this study it was determined if the feeding of whole pig carcasses, a common food item, could have a negative effect on plasma vitamin E concentrations in a captive colony. Plasma vitamin E concentrations were 7.38 ± 2.92 and 4.51 ± 1.24 after feeding whole pig carcasses (n = 14). Behaviorally, the birds also avoided the viscera and fat when feeding. Reasons for their low vitamin E concentrations could have resulted from the birds consuming only the pork meat, which is known to be low in vitamin E, or from natural peroxidation because of the high fat content of the carcasses. The study thus highlights the need for further research to ascertain the impact of feeding pig carcasses on wild vultures feeding routinely at supplementary feeding sites and also for considerations towards vitamin E supplementation.

A utilization distribution for the global population of Cape Vultures (Gyps coprotheres) to guide wind energy development.

The rapid development of wind energy in southern Africa represents an additional threat to the already fragile populations of African vultures. The distribution of the vulnerable Cape Vulture Gyps coprotheres overlaps considerably with wind energy development areas in South Africa, creating conflicts that can hinder both vulture conservation and sustainable energy development. To help address this conflict and aid in the safe placement of wind energy facilities, we map the utilization distribution (UD) of this species across its distributional range. Using tracking data from 68 Cape Vultures collected over the last 20 years, we develop a spatially explicit habitat use model to estimate the expected UDs around known colonies. Scaling the UDs by the number of vultures expected to use each of the colonies, we estimate the Cape Vulture population utilization distribution (PUD) and determine its exposure to wind farm impacts. To complement our results, we model the probability of a vulture flying within the rotor sweep area of a wind turbine throughout the species range and use this to identify areas that are particularly prone to collisions. Overall, our estimated PUD correlates well with reporting rates of the species from the Southern African Bird Atlas Project, currently used to assess potential overlap between Cape Vultures and wind energy developments, but it adds important benefits, such as providing a spatial gradient of activity estimates over the entire species range. We illustrate the application of our maps by analyzing the exposure of Cape Vultures in the Renewable Energy Development Zones (REDZs) in South Africa. This application is a scalable procedure that can be applied at different planning phases, from strategic, nationwide planning to project-level assessments.

A multi-species evaluation of digital wildlife monitoring using the Sigfox IoT network.

Bio-telemetry from small tags attached to animals is one of the principal methods for studying the ecology and behaviour of wildlife. The field has constantly evolved over the last 80 years as technological improvement enabled a diversity of sensors to be integrated into the tags (e.g., GPS, accelerometers, etc.). However, retrieving data from tags on free-ranging animals remains a challenge since satellite and GSM networks are relatively expensive and or power hungry. Recently a new class of low-power communication networks have been developed and deployed worldwide to connect the internet of things (IoT). Here, we evaluated one of these, the Sigfox IoT network, for the potential as a real-time multi-sensor data retrieval and tag commanding system for studying fauna across a diversity of species and ecosystems. We tracked 312 individuals across 30 species (from 25 g bats to 3 t elephants) with seven different device concepts, resulting in more than 177,742 successful transmissions. We found a maximum line of sight communication distance of 280 km (on a flying cape vulture [Gyps coprotheres]), which sets a new documented record for animal-borne digital data transmission using terrestrial infrastructure. The average transmission success rate amounted to 68.3% (SD 22.1) on flying species and 54.1% (SD 27.4) on terrestrial species. In addition to GPS data, we also collected and transmitted data products from accelerometers, barometers, and thermometers. Further, we assessed the performance of Sigfox Atlas Native, a low-power method for positional estimates based on radio signal strengths and found a median accuracy of 12.89 km (MAD 5.17) on animals. We found that robust real-time communication (median message delay of 1.49 s), the extremely small size of the tags (starting at 1.28 g without GPS), and the low power demands (as low as 5.8 µAh per transmitted byte) unlock new possibilities for ecological data collection and global animal observation.

The non-steroidal anti-inflammatory drug nimesulide kills Gyps vultures at concentrations found in the muscle of treated cattle.

Throughout South Asia, cattle are regularly treated with non-steroidal anti-inflammatory drugs (NSAIDs) and their carcasses are left for scavengers to consume. Residues of the NSAID diclofenac in cattle carcasses caused widespread mortality and catastrophic population declines in three species of Gyps vulture during the 1990s and 2000s. Diclofenac is now banned, but other NSAIDs are used in its place. Different lines of evidence, including safety testing in Gyps vultures, have shown that some of these other NSAIDs are toxic, or probably toxic, to vultures. The NSAID nimesulide is widely available and commonly used, and has been found in dead vultures with signs of renal failure (i.e. visceral gout) and without the presence of diclofenac and/or other vulture-toxic NSAIDs. Nimesulide is therefore probably toxic to vultures. Here, we report safety testing of nimesulide in Gyps vultures. In a controlled toxicity experiment, we gave two vultures the maximum likely exposure (MLE) of nimesulide calculated from initial pharmacokinetic and residue experiments in cattle. Two other control birds were given an oral dose of water. Both vultures dosed with nimesulide died within 30 h, after showing outward signs of toxicity and increases in biochemical indicators of renal failure. Post-mortem examinations found extensive visceral gout in both vultures. Both control vultures survived without biochemical indicators of renal failure. With this evidence, we call for an immediate and comprehensive ban of nimesulide throughout South Asia to ensure the survival of the region's Critically Endangered vultures. More generally, testing the impacts of drugs on non-target species should be the responsibility of the pharmaceutical industry, before their veterinary use is licensed.

Does the renal portal valve exist in a raptor species? A study aimed at further evaluating the mechanism of toxicity of diclofenac in vultures.

Diclofenac has been responsible for the deaths of millions of vultures on the Asian subcontinent. While the pathology of toxicity is well described, the mechanism of toxicity remains elusive. However, it was postulated that toxicity could be related to the unique avian renal vascular structure known as the renal portal valve and that that diclofenac altered valve functionality with subsequent renal ischaemia. While plausible, the valva renalis portalis has only been described in a small number of other bird species such as the chicken (Gallus domesticus), the domestic duck (Anas platyrhynchos domesticus) and ostrich (Struthio camelus) but not a raptor. The aim of this study was to evaluate the renal anatomy and related vasculature of the Cape griffon vulture (Gyps coprotheres) (CGV), a species sensitive to the toxic effects of diclofenac, using gross anatomy, histology and vascular casting. The vasculature of the vulture was found to be almost identical to that of the domestic chicken with the valva renalis portalis present in the v. iliaca externa between the v. renalis renalis cranialis and the v. renalis caudalus. The valve was ring-shaped with finger-like processes and histologically was composed of smooth muscle. The valve was also well vascularized and was associated with a nerve plexus. Based on the findings of this study, the proposed mechanism of toxicity is anatomically possible.

Percentage of faecal excretion of meloxicam in the Cape vultures (Gyps corprotheres).

Asian Gyps vulture species are gradually recovering from the devastating effect of diclofenac being present in contaminated carcasses. This drug was responsible for the death of over 10 million vultures in India, Nepal and Pakistan. To prevent the extinction of vultures, meloxicam was introduced after the ban of veterinary diclofenac. Meloxicam's safety in vultures was attributed to its short elimination half-life in contrast with diclofenac. The reason for the rapid elimination of meloxicam is yet to be explained. The aim of this study was to evaluate the role of biotransformation in the elimination of meloxicam. Six Cape griffon vultures (Gyps coprotheres) were treated with 2 mg/kg meloxicam intramuscularly for faecal and plasma quantification of meloxicam concentration over time. In the plasma meloxicam was characterised by a half-life, mean residence time, clearance and volume of distribution at steady state of 0.37 ±â€¯0.10 h, 0.90 ±â€¯0.12 h, 0.02 ±â€¯0.00 l/h kg and 0.02 ±â€¯0.00 l/kg respectively (presented as geometric mean). Over the 24 h monitoring period, the total non-metabolised meloxicam in the faeces was 1.35 ±â€¯0.71% of the total concentration in the plasma. Based on the short meloxicam elimination half-life and low cumulative concentration of total faecal meloxicam over a period in excess of 10 half-lives, this study indicates that Cape griffon vultures are efficient metaboliser of meloxicam, which is suggestive of different set of cytochrome enzymes being involved in the metabolism to that for diclofenac in this species. Identification of orthologous human CYP2C9 and CYP3A4 enzyme families in vultures will be an important further step in explaining the differences in the metabolic pathway(s) of meloxicam and diclofenac for the species.

Serum and Plasma Cholinesterase Activity in the Cape Griffon Vulture (Gyps coprotheres).

Vulture (Accipitridae) poisonings are a concern in South Africa, with hundreds of birds dying annually. Although some of these poisonings are accidental, there has been an increase in the number of intentional baiting of poached rhinoceros (Rhinocerotidae) and elephant (Elephantidae) carcasses to kill vultures that alert officials to poaching sites by circling overhead. The primary chemicals implicated are the organophosphorous and carbamate compounds. Although most poisoning events can be identified by dead vultures surrounding the scavenged carcass, weak birds are occasionally found and brought to rehabilitation centers for treatment. The treating veterinarian needs to make an informed decision on the cause of illness or poisoning prior to treatment. We established the reference interval for serum and plasma cholinesterase activity in the Cape Griffon Vulture ( Gyps coprotheres ) as 591.58-1,528.26 U/L, providing a clinical assay for determining potential exposure to cholinesterase-depressing pesticides. Both manual and automated samplers were used with the butyrylthiocholine method. Species reference intervals for both serum and plasma cholinesterase showed good correlation and manual and automated measurements yielded similar results.

The Safety and Pharmacokinetics of Carprofen, Flunixin and Phenylbutazone in the Cape Vulture (Gyps coprotheres) following Oral Exposure.

The following study evaluates the overt toxic potential of carprofen (CRP), flunixin (FXN) and phenylbutazone (PBZ) in Old world vultures in relation to historic toxicity data for diclofenac and ketoprofen, with the Cape vulture (Gyps coprotheres) being the indicator species. The toxic potential of a single oral dose of CRP (11.5 mg/kg), FXN (1 mg/kg),PBZ (1.7 mg/kg) or water was evaluated by means of a four-way parallel study (n = 2), as means of ascertaining if these drugs were as toxic as diclofenac in the vulture. No unscheduled deaths or pathological lesions were noted following exposure. Clinical signs of lethargy and depression were, however, noted in one CRP, two FXN and one PBZ treated birds. Mild reversible inhibition of UA excretion was evident in all three groups, although UA remained within the population reference interval in contrast to the effects previously described for diclofenac and ketoprofen. All treatment groups had a drug concentration responsive increase in alanine transferase activity. CRP, FXN and PBZ were characterised by a maximum plasma concentration (Cmax) of 1051.8 ± 620.7 ng/ml, 335.9 ± 36.3 ng/ml and 11150 ± 2474.9 ng/ml at 4 ± 4.3, 0.45 ± 0.02 and 5.3 ± 5.2 hours (Tmax) respectively and a half-life of elimination of 13.3 ±5, 1.8±1 and 18.7 ±11.4 hours respectively. While we could not demonstrate a lethal effect of the tested substances, the presence of toxic clinical signs, clinical pathological changes and/or long half-lives of elimination suggests that all three drugs have a potential for toxicity in a larger population or on repeat administration. In conclusion while the studied substances were not as overtly toxic as diclofenac, they are of safety concern.

Do power lines and protected areas present a catch-22 situation for Cape vultures (Gyps coprotheres)?

Cape vulture Gyps coprotheres populations have declined across their range due to multiple anthropogenic threats. Their susceptibility to fatal collisions with the expanding power line network and the prevalence of carcasses contaminated with illegal poisons and other threats outside protected areas are thought to be the primary drivers of declines in southern Africa. We used GPS-GSM units to track the movements and delineate the home ranges of five adult (mean ±SD minimum convex polygon area = 121,655±90,845 km(2)) and four immature (mean ±SD minimum convex polygon area = 492,300±259,427 km(2)) Cape vultures to investigate the influence of power lines and their use of protected areas. The vultures travelled more than 1,000 km from the capture site and collectively entered five different countries in southern Africa. Their movement patterns and core foraging ranges were closely associated with the spatial distribution of transmission power lines and we present evidence that the construction of power lines has allowed the species to extend its range to areas previously devoid of suitable perches. The distribution of locations of known Cape vulture mortalities caused by interactions with power lines corresponded to the core ranges of the tracked vultures. Although some of the vultures regularly roosted at breeding colonies located inside protected areas the majority of foraging activity took place on unprotected farmland. Their ability to travel vast distances very quickly and the high proportion of time they spend in the vicinity of power lines and outside protected areas make Cape vultures especially vulnerable to negative interactions with the expanding power line network and the full range of threats across the region. Co-ordinated cross-border conservation strategies beyond the protected area network will therefore be necessary to ensure the future survival of threatened vultures in Africa.

Foraging ranges of immature African white-backed vultures (Gyps africanus) and their use of protected areas in southern Africa.

Vultures in the Gyps genus are declining globally. Multiple threats related to human activity have caused widespread declines of vulture populations in Africa, especially outside protected areas. Addressing such threats requires the estimation of foraging ranges yet such estimates are lacking, even for widespread (but declining) species such as the African white-backed vulture (Gyps africanus). We tracked six immature African white-backed vultures in South Africa using GPS-GSM units to study their movement patterns, their use of protected areas and the time they spent in the vicinity of supplementary feeding sites. All individuals foraged widely; their combined foraging ranges extended into six countries in southern Africa (mean (± SE) minimum convex polygon area =269,103±197,187 km(2)) and three of the vultures travelled more than 900 km from the capture site. All six vultures spent the majority of their tracking periods outside protected areas. South African protected areas were very rarely visited whereas protected areas in northern Botswana and Zimbabwe were used more frequently. Two of the vultures visited supplementary feeding sites regularly, with consequent reduced ranging behaviour, suggesting that individuals could alter their foraging behaviour in response to such sites. We show that immature African white-backed vultures are capable of travelling throughout southern Africa, yet use protected areas to only a limited extent, making them susceptible to the full range of threats in the region. The standard approach of designating protected areas to conserve species is unlikely to ensure the protection of such wide-ranging species against threats in the wider landscape.

Lead toxicity: consequences and interventions in an intensively managed (Gyps coprotheres) vulture colony.

The National Zoological Gardens of South Africa (NZG) is involved in the ex situ conservation of Gyps coprotheres, the Cape Griffon vulture (CGV) and houses 24 birds in a 100-yr-old aviary. Following the death of one vulture with high liver lead concentrations, an investigation was launched to ascertain the source(s) and consequences of lead toxicity in this breeding colony. Whole blood from 24 CGV, paint from the enclosure, water, and soil sampled at various locations within the enclosure were evaluated for their lead concentration, and data were gathered from NZG's medical records. The lead concentration in the paint, water, and enclosure soil was 5,100 microg/g, 0.5 microg/dl, and 72.48 +/- 21.83 microg/g, respectively. The whole-blood lead concentrations were 56.58 +/- 11 microg/dl. The breeding history of six pairs within the contaminated enclosure since 2002 showed 45 eggs laid, of which 44% were infertile and 24% successfully reared. The medical records revealed evidence of osteodystrophy despite adequate nutrition. As intervention measures, six birds were treated with Ca2+EDTA and the topsoil inside the enclosure was replaced. As a result, the lead concentration in the enclosure soil dropped to 14.74 +/- 14.39 microg/g, and the whole-blood lead concentrations declined to 42.75 +/- 11.64 microg/dl. It was concluded that lead concentrations in whole blood in excess of 100 microg/dl leads to clinical signs of lead toxicity in the CGV. Lower levels appear to interfere mainly with reproductive potential.

Toxicity of non-steroidal anti-inflammatory drugs to Gyps vultures: a new threat from ketoprofen.

Three Gyps vulture species are on the brink of extinction in South Asia owing to the veterinary non-steroidal anti-inflammatory drug (NSAID) diclofenac. Carcasses of domesticated ungulates are the main food source for Asia's vultures and birds die from kidney failure after consuming diclofenac-contaminated tissues. Here, we report on the safety testing of the NSAID ketoprofen, which was not reported to cause mortality in clinical treatment of scavenging birds and is rapidly eliminated from livestock tissues. Safety testing was undertaken using captive non-releasable Cape griffon vultures (Gyps coprotheres) and wild-caught African white-backed vultures (G. africanus), both previously identified as susceptible to diclofenac and suitable surrogates. Ketoprofen doses ranged from 0.5 to 5 mg kg(-1) vulture body weight, based upon recommended veterinary guidelines and maximum levels of exposure for wild vultures (estimated as 1.54 mg kg(-1)). Doses were administered by oral gavage or through feeding tissues from cattle dosed with ketoprofen at 6 mg kg(-1) cattle body weight, before slaughter. Mortalities occurred at dose levels of 1.5 and 5 mg kg(-1) vulture body weight (within the range recommended for clinical treatment) with the same clinical signs as observed for diclofenac. Surveys of livestock carcasses in India indicate that toxic levels of residual ketoprofen are already present in vulture food supplies. Consequently, we strongly recommend that ketoprofen is not used for veterinary treatment of livestock in Asia and in other regions of the world where vultures access livestock carcasses. The only alternative to diclofenac that should be promoted as safe for vultures is the NSAID meloxicam.

Toxicity of diclofenac to Gyps vultures.

Three endemic vulture species Gyps bengalensis, Gyps indicus and Gyps tenuirostris are critically endangered following dramatic declines in South Asia resulting from exposure to diclofenac, a veterinary drug present in the livestock carcasses that they scavenge. Diclofenac is widely used globally and could present a risk to Gyps species from other regions. In this study, we test the toxicity of diclofenac to a Eurasian (Gyps fulvus) and an African (Gyps africanus) species, neither of which is threatened. A dose of 0.8 mg kg(-1) of diclofenac was highly toxic to both species, indicating that they are at least as sensitive to diclofenac as G. bengalensis, for which we estimate an LD50 of 0.1-0.2 mg kg(-1). We suggest that diclofenac is likely to be toxic to all eight Gyps species, and that G. africanus, which is phylogenetically close to G. bengalensis, would be a suitable surrogate for the safety testing of alternative drugs to diclofenac.

Removing the threat of diclofenac to critically endangered Asian vultures.

Veterinary use of the nonsteroidal anti-inflammatory (NSAID) drug diclofenac in South Asia has resulted in the collapse of populations of three vulture species of the genus Gyps to the most severe category of global extinction risk. Vultures are exposed to diclofenac when scavenging on livestock treated with the drug shortly before death. Diclofenac causes kidney damage, increased serum uric acid concentrations, visceral gout, and death. Concern about this issue led the Indian Government to announce its intention to ban the veterinary use of diclofenac by September 2005. Implementation of a ban is still in progress late in 2005, and to facilitate this we sought potential alternative NSAIDs by obtaining information from captive bird collections worldwide. We found that the NSAID meloxicam had been administered to 35 captive Gyps vultures with no apparent ill effects. We then undertook a phased programme of safety testing of meloxicam on the African white-backed vulture Gyps africanus, which we had previously established to be as susceptible to diclofenac poisoning as the endangered Asian Gyps vultures. We estimated the likely maximum level of exposure (MLE) of wild vultures and dosed birds by gavage (oral administration) with increasing quantities of the drug until the likely MLE was exceeded in a sample of 40 G. africanus. Subsequently, six G. africanus were fed tissues from cattle which had been treated with a higher than standard veterinary course of meloxicam prior to death. In the final phase, ten Asian vultures of two of the endangered species (Gyps bengalensis, Gyps indicus) were dosed with meloxicam by gavage; five of them at more than the likely MLE dosage. All meloxicam-treated birds survived all treatments, and none suffered any obvious clinical effects. Serum uric acid concentrations remained within the normal limits throughout, and were significantly lower than those from birds treated with diclofenac in other studies. We conclude that meloxicam is of low toxicity to Gyps vultures and that its use in place of diclofenac would reduce vulture mortality substantially in the Indian subcontinent. Meloxicam is already available for veterinary use in India.