Foraging movements of Eurasian griffon vultures (Gyps fulvus): implications for supplementary feeding management

The outbreak of bovine spongiform encephalopathy provoked restrictive European sanitary legislation that forced farmers to remove livestock carcasses from the wild. This had serious repercussions for the scavenger raptor guild. Against this background, we developed a study to analyse the foraging movements of Eurasian griffon vultures (Gyps fulvus) in northern Spain. We ringed 241 griffon vultures with alphanumeric plastic rings in Biscay between 2000 and 2011 and set experimental feeding stations in 24 sites over an area of 10,614 km²; recording re-sightings of the ringed vultures between 2005 and 2012. Using these re-sighting records, we tested whether birds randomly moved long distances whilst searching for food, or if vulture re-sightings were restricted to a few feeding sites within a limited area. We summarised 329 field-work days, with an average of 2.06 ringed vultures re-sighted per day, accounting for 1,017 re-sightings. Adult vultures were detected in three separate foraging nuclei within the study area. Movements out of the main foraging nuclei were statistically less frequent than would be expected if adult vultures accessed all resources at a similar rate. Once established at breeding areas, subadult vultures behaved in the same way as adults. Our results suggest that vultures’ home ranges are largely restricted to zones close to breeding areas. This has important consequences from a conservation point of view, suggesting that management decisions should take into consideration spatial scale effects.     

Microflora and internal parasites of the digestive tract of Eurasian griffon vultures (Gyps fulvus) in Croatia

Faecal and vomit samples were collected from 12 griffon vultures (Gyps fulvus) in May 2002 and examined for bacteria, fungi and parasites. Bacteria present included Escherichia coli, Aeromonas salmonicidia, Proteus sp., Escherichia fergusonii, Providencia alcalifaciens, Micrococcus sp. and Streptococcus sp. Mycological examination revealed the presence of Candida sp., yeasts and in one case, Rhodotorula rubra. Strongyle eggs were found in several samples. In most faecal samples, ascarid eggs of Toxocara type were found. Tapeworm eggs of Moniezia type were present in one faecal sample. Both microbiologic and parasitic findings are most likely the result of the feeding habits of griffon vultures.     

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.     

Application of GPS occurrence data to understand African white‐backed vultures Gyps africanus spatial home range overlaps

Understanding key overlap zones and habitats which are intensively shared by species in space and time is crucial as it provides vital information to inform spatial conservation with maximum benefits. The advent of high‐resolution GPS technologies associated with new analytical algorithms is revolutionizing studies underpinning species spatial and social interaction patterns within ecosystems. Here, using a robust home range estimation algorithm, the autocorrelated kernel density estimator (AKDE) equipped with an equally powerful home range overlap metric, the Bhattacharyya''s coefficient (BC), we provide one of the first attempts to estimate and delineate spatial home range overlap zones for critically endangered African white‐backed vultures to inform conservation planning. Six vultures were captured in Hwange National Park using a modified cannon net system after which they were tagged and tracked with high‐resolution GPS backpacks. Overall, results suggested weaker average home range overlaps based on both the pooled data (0.38 ± 0.26), wet non‐breeding seasonal data (0.32 ± 0.23), and dry breeding season data (0.34 ± 0.28). Vultures 4, 5, and 6 consistently revealed higher home range overlaps across all the scales with values ranging between 0.60 and 0.99. Individual vultures showed consistence in space use patterns as suggested by high between‐season home range overlaps, an indication that they may be largely resident within the Hwange ecosystem. Importantly, we also demonstrate that home range overlapping geographic zones are all concentrated within the protected area of Hwange National Park. Our study provides some of the first results on African vulture home range overlaps and segregation patterns in the savanna ecosystem based on unbiased telemetry data and rigorous analytical algorithms. Such knowledge may provide vital insights for prioritizing conservation efforts of key geographic overlap zones to derive maximum conservation benefits especially when targeting wide‐ranging and critically endangered African white‐backed vultures. To this end, spatial overlap zones estimated here, although based on a small sample size, could provide a strong foundation upon which other downstream social and ecological questions can be explored further to expand our understanding on shared space use mechanisms among African vulture species.     

Establishment of selected baseline blood chemistry and hematologic parameters in captive and wild-caught African white-backed vultures (Gyps africanus)

Despite the devastating collapse of three vulture populations on the Asian subcontinent as a result of their exposure to diclofenac, there is little available information on the normal physiology of many vulture species, including the African White-backed Vulture (Gyps africanus). Such information is needed to fully understand mechanisms for toxicity and to identify and prevent future health problems. The aim of this study was to establish baseline parameters for hematologic and selected serum chemistry parameters for this model species for further studies into the toxicity of diclofenac. Captive nonreleasable and wild African White-backed Vultures were used to determine reference values. For hematology, erythrocyte counts, hemoglobin concentration, hematocrit, packed cell volume, mean corpuscular volume, mean corpuscular hemoglobin concentration, and total and differential leukocyte counts were measured. Chemical analytes measured included sodium, potassium, calcium, albumin, and globulin concentrations, aspartate aminotransferase, creatine kinase, and alanine aminotransferase activities. Uric acid and urea concentrations and the urea:uric acid ratio also were evaluated. Values are presented as means, standard deviations, and reference intervals. The serum chemistry parameters selected may provide a starting point for the evaluation of changes in renal and hepatic function; these organ systems are most severely affected by diclofenac. Results were also compared with values reported for G. africanus nestlings, and from these results it is evident that the clinical pathologic parameters are age related. This indicates that the use of nestling values for the evaluation of clinical pathologic findings in adults may be unreliable and could lead to incorrect assumptions.     

The evolutionary pathway to obligate scavenging in Gyps vultures

The evolutionary pathway to obligate scavenging in Gyps vultures remains unclear. We propose that communal roosting plays a central role in setting up the information transfer network critical for obligate scavengers in ephemeral environments and that the formation of a flotilla-like foraging group is a likely strategy for foraging Gyps vultures. Using a spatial, individual-based, optimisation model we find that the communal roost is critical for establishing the information network that enables information transfer owing to the spatial-concentration of foragers close to the roost. There is also strong selection pressure for grouping behaviour owing to the importance of maintaining network integrity and hence information transfer during foraging. We present a simple mechanism for grouping, common in many animal species, which has the added implication that it negates the requirement for roost-centric information transfer. The formation of a flotilla-like foraging group also improves foraging efficiency through the reduction of overlapping search paths. Finally, we highlight the importance of consideration of information transfer mechanisms in order to maximise the success of vulture reintroduction programmes.     

Visual fields,foraging and collision vulnerability in Gyps vultures

The visual fields of vultures contain a small binocular region and large blind areas above, below and behind the head. Head positions typically adopted by foraging vultures suggest that these visual fields provide comprehensive visual coverage of the ground below, prohibit the eyes from imaging the sun and provide extensive visual coverage laterally. However, vultures will often be blind in the direction of travel. We conclude that by erecting structures such as wind turbines, which extend into open airspace, humans have provided a perceptual challenge that the vision of foraging vultures cannot overcome.     

Allozyme variation in four populations of African whitebacked vultures (Gyps africanus) and phylogenetic relationships between four vulture species from southern Africa

Genetic variation detected by protein electrophoresis at 41 presumptive gene loci was assayed in four populations of Gyps africanus and compared to values previously obtained for Gyps coprotheres. Values calculated for percentage of polymorphic loci (P=34.15%, 0.99 criterion) and average heterozygosity (&Hmacr;=0.108, +/-0.032) in G. africanus, confirm low levels of genetic variation as reported for G. coprotheres. Allele frequency data, assessed at 19 loci, were obtained to evaluate genetic differentiation among four vulture species. Six (31.58%) of the 19 shared loci were polymorphic. Values of 1.26 (+/-0.1), 26.32% and 0.076 (+/-0.047) for G. africanus, 1.21 (+/-0.1), 21.05% and 0.097 (+/-0.045) for Torgos tracheliotus, 1.11 (+/-0.7), 21.05% and 0.053 (+/-0.053) for Neophron percnopterus and 1.05 (+/-0.5), 5.26% and 0.044 (+/-0.047) for G. coprotheres were obtained for the mean number of alleles per locus, P and &Hmacr;, respectively. An average between-population fixation index (F(ST)) value of 0.322 was obtained, which is indicative of significant (P<0.01) differentiation between the four accipitrid species studied. Considerable concordance was obtained between dendograms produced from different analyses, pointing to the distinctiveness of N. percnopterus, which has evolved along a separate lineage as G. africanus, G. coprotheres and T. tracheliotus. Along the latter lineage G. africanus is clustered together with G. coprotheres which is consistent with the morphological similarities of these species.     

Status and structure of the griffon vulture (Gyps fulvus) population in Crete

Griffon vulture (Gyps fulvus) population surveys were conducted during 1996–2002 in the island of Crete (Greece) to document population status and structure. Fieldwork was carried out during the breeding period when birds could be monitored in their colonies. Total population size was estimated at 379 individuals (range = 341–417) with adult birds comprising 63%. The breeding population was estimated at 141 pairs, which were distributed on an average in 23 colonies per year (range = 16–30) while the mean number of breeding pairs that laid eggs was 98 (range= 64–126). Crete thus supports the largest insular population of the species in the world and hosts 70–80% of the breeding population of the species in Greece. Population density was estimated at 6.9 individuals/100 km², 2.6 breeding pairs/100 km² and 1.8 nesting pairs/100 km². The average home range of an occupied colony (i.e., breeding group) was estimated at ca. 204 km² producing a theoretical foraging range of 8 km radius around the breeding cliff. No trends in the total number of individuals and breeding pairs appeared to exist, although significant differences in population size of individual colonies occurred between the years. The majority of the population was concentrated in small-sized colonies, which showed a low occupancy rate. The number of abandoned sites and the colonization of new ones could represent a shift of breeding pairs to alternative colonies provoked by local food abundance and conspesific attraction.     

The effect of food quality on breeding strategy in Griffon vultures (Gyps spp.)

Griffon vultures feed from the soft tissues of large mammal carcasses: a diet which contains very little calcium. Comparatively large amounts of calcium are required in order to breed, first for eggshell formation and then for bone mineralization of the chick. These requirements are estimated. Adults were not found to supply the chick with a mineral-rich crop secretion during rearing, but they must feed the young with calcium-rich food items, such as bone fragments. These are not abundant, and it is suggested that the mineral requirements for breeding have determined certain features of the breeding strategy in these birds—such as laying a single egg and having a prolonged rearing period.     

High altitude and hemoglobin function in the vultures Gyps rueppellii and Aegypius monachus

Functional characteristics of the stripped composite hemoglobins (Hbs) of the vultures Gyps rueppellii and Aegypius monachus that can fly at extremely high altitudes, and of component Hbs of G. rueppellii are reported, in relation to influences of pH, temperature and inositol hexaphosphate. G. rueppellii Hbs A, A' and D represent a sequence of increasing oxygen affinity, which is opposite to earlier results on avian Hb components, but correlates with two alpha-chain substitutions that predictably affect oxygen affinity. The homo- and heterotropic interactions in oxygen binding are related to primary structures of the constituent polypeptide chains to trace molecular adaptations to high-altitude respiration, and to physiological factors (pulmonary hypoxia and hypocapnia, body temperature shifts, and lung and nasal gas and heat exchange) to discern their possible survival value at altitudes of 11,300 m.     

The role of cryoprotective agents as hydroxyl radical scavengers

The classic cryoprotective agents dimethylsulfoxide and glycerol are hydroxyl radical scavengers. In addition the cryoprotective agents tetramethylurea, dimethylformide, dimethylurea and monomethylurea act as hydroxyl radical scavengers as shown by the inhibition of ethylene production from methional and the inhibition of methane production from dimethylsulfoxide. Both cryoprotection and scavenger efficiency decrease in the same order within a homologous series: tetramethylurea > dimethylurea > monomethylurea. Urea does not act as a hydroxyl radical scavenger and urea is not a cryoprotective agent. Thus cryoprotection may involve scavengers in the prevention of membrane damage by hydroxyl radicals.     

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.     

Nesting habitat preference of the African White-backed Vulture Gyps africanus and the effects of anthropogenic disturbance

The African White-backed Vulture Gyps africanus is widely distributed across sub-Saharan Africa but populations are in decline. Loss of suitable habitat for foraging and breeding are among the most important causes, and future conservation will require identification of suitable remaining habitat and the threats to it and to the vultures in it. Like many large raptors, African White-backed Vultures have a long breeding cycle and thus spend much of each year near their nest site, but ecological correlates of nest sites have not been quantified for any African vulture species. We use nest-site data for African White-backed Vultures collected during aerial and ground surveys and habitat data derived from a GIS to develop statistical models that estimate the probability of nest presence in relation to habitat characteristics, and test these models against an independent dataset. The models predicted that both direct and indirect disturbance by humans limit the potential distribution. Suitable habitat needs to be identified and receive adequate protection from poaching. Poaching of vultures is thought to be mainly for use in traditional medicine and does not target any particular species, so all vulture species can be considered equally at risk. We predict the likelihood of individuals nesting in currently unprotected areas should they become protected. These predictions show that readily available GIS data combined with relatively simple statistical modelling can provide meaningful large-scale predictions of habitat availability.     

A dead giveaway: Foraging vultures and other avian scavengers respond to auditory cues

Carrion represents an unpredictable and widely distributed primary food source for vultures and other avian scavengers. Avian scavengers in African savanna ecosystems are reported to rely exclusively on visual stimuli to locate carcasses. However, carnivores’ predation of large mammalian herbivores and subsequent competition for access to the carcass can result in considerable noise, often audible over long distances and for prolonged periods. Vultures and other avian scavengers may therefore detect and respond to these auditory cues, as do the mammalian carnivores alongside which vultures have coevolved, but this has not been investigated to date. Working in the Serengeti ecosystem, Tanzania, we used diurnal auditory broadcasts to simulate predation and competitive carnivore feeding interactions. Based on the current understanding of avian scavenger ecology, we hypothesized that avian responses to call‐in stations would be evoked exclusively by visual, rather than auditory, cues. We therefore predicted that (a) the arrival of avian scavengers at call‐in stations should be preceded and facilitated by mammalian carnivores and that (b) the arrival of avian scavengers would be positively correlated with the number of mammalian scavengers present, which would increase detectability. We recorded 482 birds during 122 separate playback events. In 22% of these instances, avian scavengers arrived first, ruling out responses based exclusively on visual observations of mammalian carnivores, thereby contradicting our first prediction. Furthermore, the first avian arrivals at survey sessions were inversely related to the number of hyenas and jackals present, contradicting our second prediction. Since no bait or carcasses were used during the experiments, these responses are indicative of the birds’ ability to detect and respond to audio stimuli. Our findings challenge the current consensus of sensory perception and foraging in these species and provide evidence that avian scavengers have the ability to use sound to locate food resources.     

Breeding site selection by bearded vulture (Gypaetus barbatus) and Eurasian griffon (Gyps fulvus) in the Caucasus

Occupied and unoccupied sites of bearded vulture Gypaetus barbatus and Eurasian griffon Gyps fulvus were located in the Caucasus (mainly Georgia). Habitat variables related to nest-site characteristics, climate, terrain, human disturbance and food availability were used to construct predictive models of vulture breeding site selection by using a geographic information system (GIS), logistic regression and Bayesian statistical inference. The probability of bearded vulture occupancy of a cliff ledge that was safe from climatic adversity, human disturbance and predation was positively correlated with the following variables measured within a 20-km radius of the ledge: mean elevation, mean slope, the percentage of open areas, mean distance to roads, number of globally threatened wild goats Capra cylindricornis, C. caucasica and C. aegargus , and annual biomass of dead livestock. The probability of such a cliff ledge being occupied by Eurasian griffon was negatively correlated with annual rainfall at the ledge and positively correlated with the percentage of open areas and annual biomass of dead livestock within 20 km of the ledge. Provided that GIS coverage of the habitat variables is available, these models can be of help in various areas of the Caucasus and elsewhere to predict possible nest occurrence areas, and highlight sites where vultures may occur in the future if the population grows because of conservation or other activities.     

Pathology and proposed pathophysiology of diclofenac poisoning in free-living and experimentally exposed oriental white-backed vultures (Gyps bengalensis)

Oriental white-backed vultures (Gyps bengalensis; OWBVs) died of renal failure when they ingested diclofenac, a nonsteroidal anti-inflammatory drug (NSAID), in tissues of domestic livestock. Acute necrosis of proximal convoluted tubules in these vultures was severe. Glomeruli, distal convoluted tubules, and collecting tubules were relatively spared in the vultures that had early lesions. In most vultures, however, lesions became extensive with large urate aggregates obscuring renal architecture. Inflammation was minimal. Extensive urate precipitation on the surface and within organ parenchyma (visceral gout) was consistently found in vultures with renal failure. Very little is known about the physiologic effect of NSAIDs in birds. Research in mammals has shown that diclofenac inhibits formation of prostaglandins. We propose that the mechanism by which diclofenac induces renal failure in the OWBV is through the inhibition of the modulating effect of prostaglandin on angiotensin II-mediated adrenergic stimulation. Renal portal valves open in response to adrenergic stimulation, redirecting portal blood to the caudal vena cava and bypassing the kidney. If diclofenac removes a modulating effect of prostaglandins on the renal portal valves, indiscriminant activation of these valves would redirect the primary nutrient blood supply away from the renal cortex. Resulting ischemic necrosis of the cortical proximal convoluted tubules would be consistent with our histologic findings in these OWBVs.