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1.  Systematics within Gyps vultures: a clade at risk 
Populations of the Oriental White-backed Vulture (Gyps bengalensis) have declined by over 95% within the past decade. This decline is largely due to incidental consumption of the non-steroidal anti-inflammatory veterinary pharmaceutical diclofenac, commonly used to treat domestic livestock. The conservation status of other Gyps vultures in southern Asia is also of immediate concern, given the lack of knowledge regarding status of their populations and the continuing existence of taxonomic uncertainties. In this study, we assess phylogenetic relationships for all recognized species and the majority of subspecies within the genus Gyps. The continuing veterinary use of diclofenac is an unknown but potential risk to related species with similar feeding habits to Gyps bengalensis. Therefore, an accurate assessment of the phylogenetic relationships among Gyps vultures should aid in their conservation by clarifying taxonomic uncertainties, and enabling inference of their respective relatedness to susceptible G. bengalensis.
Phylogenetic results using mitochondrial cytB, ND2 and control region sequence data indicate a recent and rapid diversification within the genus Gyps. All recognized species formed monophyletic groups with high statistical support, with the exception of the Eurasian Vulture, for which specimens identified as subspecies G. fulvus fulvescens appear closely related to the Himalayan Vulture (G. himalayensis). In all analyses, the earliest divergence separated the Oriental White-backed Vulture from other Gyps taxa, with the next diverging taxon being either the African White-backed Vulture (G. africanus), or the Himalayan Vulture. All analyses supported a sister relationship between the Eurasian Vulture (G. f. fulvus), and Rüppell's Vulture (G. rueppellii), with this clade being sister to another consisting of the two taxa of "Long-billed" Vulture (G. indicus indicus and G. i. tenuirostris), and the Cape Vulture (G. coprotheres). These molecular phylogenies strongly support the treatment of indicus and tenuirostris as separate species, as does morphological data showing that these two taxa of similar overall size differ in proportions, especially in rostral, alar, and pedal characters. In addition, grouping of bengalensis and africanus together in the genus Pseudogyps, as historically proposed, is not upheld based on mitochondrial data.
Both molecular and morphological data provide strong support for considering the "Long-billed" Vulture to be comprised of two species (G. indicus and G. tenuirostris), and further analysis is warranted to determine the taxonomic distinctiveness of G. f. fulvescens. Our phylogenetic analyses and conservative estimates suggest the diversification of Gyps taxa to be within the past 6 million years. Diclofenac susceptibility has been previously demonstrated for four Gyps species (G. indicus, G. fulvus, G. africanus, G. bengalensis), and the phylogenetic position of these species each forming a sister relationship with at least one of the remaining species, support concern that other Gyps taxa may be susceptible as well. Determining genetic and evolutionary distinctiveness for Gyps lineages is increasingly important as a breeding program is being established to prevent extinction.
PMCID: PMC1569873
2.  Removing the Threat of Diclofenac to Critically Endangered Asian Vultures 
PLoS Biology  2006;4(3):e66.
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 genusGyps 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 captiveGyps vultures with no apparent ill effects. We then undertook a phased programme of safety testing of meloxicam on the African white-backed vultureGyps africanus, which we had previously established to be as susceptible to diclofenac poisoning as the endangered AsianGyps 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 40G. africanus. Subsequently, sixG. 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 toGyps 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.
Phased testing reveals that the anti-inflammatory drug meloxicam is less toxic to endangeredGyps vultures than diclofenac and, if used as an alternative, could potentially reverse the catastrophic decline of these species in South Asia.
PMCID: PMC1351921  PMID: 16435886
3.  Effectiveness of Action in India to Reduce Exposure of Gyps Vultures to the Toxic Veterinary Drug Diclofenac 
PLoS ONE  2011;6(5):e19069.
Contamination of their carrion food supply with the non-steroidal anti-inflammatory drug diclofenac has caused rapid population declines across the Indian subcontinent of three species of Gyps vultures endemic to South Asia. The governments of India, Pakistan and Nepal took action in 2006 to prevent the veterinary use of diclofenac on domesticated livestock, the route by which contamination occurs. We analyse data from three surveys of the prevalence and concentration of diclofenac residues in carcasses of domesticated ungulates in India, carried out before and after the implementation of a ban on veterinary use. There was little change in the prevalence and concentration of diclofenac between a survey before the ban and one conducted soon after its implementation, with the percentage of carcasses containing diclofenac in these surveys estimated at 10.8 and 10.7%, respectively. However, both the prevalence and concentration of diclofenac had fallen markedly 7–31 months after the implementation of the ban, with the true prevalence in this third survey estimated at 6.5%. Modelling of the impact of this reduction in diclofenac on the expected rate of decline of the oriental white-backed vulture (Gyps bengalensis) in India indicates that the decline rate has decreased to 40% of the rate before the ban, but is still likely to be rapid (about 18% year−1). Hence, further efforts to remove diclofenac from vulture food are still needed if the future recovery or successful reintroduction of vultures is to be feasible.
PMCID: PMC3092754  PMID: 21589920
4.  Diclofenac poisoning is widespread in declining vulture populations across the Indian subcontinent. 
Recent declines in the populations of three species of vultures in the Indian subcontinent are among the most rapid ever recorded in any bird species. Evidence from a previous study of one of these species, Gyps bengalensis, in the Punjab province of Pakistan, strongly implicates mortality caused by ingestion of residues of the veterinary non-steroidal anti-inflammatory drug diclofenac as the major cause of the decline. We show that a high proportion of Gyps bengalensis and G. indicus found dead or dying in a much larger area of India and Nepal also have residues of diclofenac and visceral gout, a post-mortem finding that is strongly associated with diclofenac contamination in both species. Hence, veterinary use of diclofenac is likely to have been the major cause of the rapid vulture population declines across the subcontinent.
PMCID: PMC1810094  PMID: 15801603
5.  Rate of Decline of the Oriental White-Backed Vulture Population in India Estimated from a Survey of Diclofenac Residues in Carcasses of Ungulates 
PLoS ONE  2007;2(8):e686.
The non-steroidal anti-inflammatory drug diclofenac is a major cause of the rapid declines in the Indian subcontinent of three species of vultures endemic to South Asia. The drug causes kidney failure and death in vultures. Exposure probably arises through vultures feeding on carcasses of domesticated ungulates treated with the drug. However, before the study reported here, it had not been established from field surveys of ungulate carcasses that a sufficient proportion was contaminated to cause the observed declines. We surveyed diclofenac concentrations in samples of liver from carcasses of domesticated ungulates in India in 2004–2005. We estimated the concentration of diclofenac in tissues available to vultures, relative to that in liver, and the proportion of vultures killed after feeding on a carcass with a known level of contamination. We assessed the impact of this mortality on vulture population trend with a population model. We expected levels of diclofenac found in ungulate carcasses in 2004–2005 to cause oriental white-backed vulture population declines of 80–99% per year, depending upon the assumptions used in the model. This compares with an observed rate of decline, from road transect counts, of 48% per year in 2000–2003. The precision of the estimate based upon carcass surveys is low and the two types of estimate were not significantly different. Our analyses indicate that the level of diclofenac contamination found in carcasses of domesticated ungulates in 2004–2005 was sufficient to account for the observed rapid decline of the oriental white-backed vulture in India. The methods we describe could be used again to assess changes in the effect on vulture population trend of diclofenac and similar drugs. In this way, the effectiveness of the recent ban in India on the manufacture and importation of diclofenac for veterinary use could be monitored.
PMCID: PMC1930156  PMID: 17668064
6.  Toxicity of diclofenac to Gyps vultures 
Biology Letters  2006;2(2):279-282.
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.
PMCID: PMC1618889  PMID: 17148382
diclofenac; vultures; toxicity; Gyps; non-steroidal anti-inflammatory drug
7.  Toxicity of non-steroidal anti-inflammatory drugs to Gyps vultures: a new threat from ketoprofen 
Biology Letters  2009;6(3):339-341.
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.
PMCID: PMC2880042  PMID: 20007163
Gyps; vultures; toxicity; ketoprofen; diclofenac; NSAIDs
8.  Molecular sexing of threatened Gyps vultures: an important strategy for conservation breeding and ecological studies 
SpringerPlus  2012;1(1):62.
During the last two decades populations of three resident species of Gyps vulture have declined dramatically and are now threatened with extinction in South Asia. Sex identification of vultures is of key importance for the purpose of conservation breeding as it is desirable to have an equal sex ratio in these monogamous species which are housed together in large colony aviaries. Because vultures are monomorphic, with no differences in external morphology or plumage colour between the sexes, other methods are required for sex identification. Molecular methods for sex identification in birds rely on allelic length or nucleotide sequence discrimination of the chromohelicase-DNA binding (CHD) gene located on male and female chromosomes ZZ and ZW, respectively. We characterized the partial sequences of CHD alleles from Gyps indicus, Gyps bengalensis, Gyps himalayensis and Aegypius monachus and analysed the applicability of five molecular methods of sex identification of 46 individual vultures including 26 known-sex G. bengalensis and G. indicus. The results revealed that W-specific PCR in combination with ZW-common PCR is a quick, accurate and simple method, and is ideal for sex identification of vultures. The method is also suitable to augment ecological studies for identifying sex of these endangered birds during necropsy examinations especially when gonads are not apparent, possibly due to regression during non-breeding seasons.
PMCID: PMC3540358  PMID: 23316450
Molecular sex identification; Gyps vulture; Cinereous vulture; Vulture conservation; Captive breeding
9.  NSAIDs and scavenging birds: potential impacts beyond Asia's critically endangered vultures 
Biology Letters  2006;3(1):90-93.
Veterinary treatment of livestock with diclofenac, a non-steroidal anti-inflammatory drug (NSAID), has caused catastrophic declines of Gyps vultures in Asia. This has highlighted a lack of knowledge on the potential impacts of NSAIDs on scavenging birds. Surveys of veterinarians and zoos document the outcomes of the treatment of over 870 scavenging birds from 79 species. As well as diclofenac, carprofen and flunixin were associated with mortality, with deaths observed in 13 and 30% of cases, respectively. Mortality was also found following treatment with ibuprofen and phenylbutazone. NSAID toxicity was reported for raptors, storks, cranes and owls, suggesting that the potential conservation impact of NSAIDs may extend beyond Gyps vultures and could be significant for New World vultures. In contrast, there were no reported mortalities for the NSAID meloxicam, which was administered to over 700 birds from 60 species. The relative safety of meloxicam supports other studies indicating the suitability of this NSAID to replace diclofenac in Asia.
PMCID: PMC2373805  PMID: 17443974
Gyps; vultures; NSAIDs; diclofenac; meloxicam; toxicity
10.  Foraging Ranges of Immature African White-Backed Vultures (Gyps africanus) and Their Use of Protected Areas in Southern Africa 
PLoS ONE  2013;8(1):e52813.
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 km2) 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.
PMCID: PMC3559650  PMID: 23382824
11.  Modelling the effects of sanitary policies on European vulture conservation 
Scientific Reports  2012;2:753.
Biodiversity losses are increasing as a consequence of negative anthropogenic effects on ecosystem dynamics. However, the magnitude and complexity of these effects may still be greatly underestimated. Most Old World vultures have experienced rapid population declines in recent years. In Europe, their immediate conservation depends on changes in health regulations affecting the availability of food provided by domestic carcasses. Information is lacking on the effects of a hypothetical food shortage on the population dynamics of vultures, and is necessary to assess the potential impacts of policy decisions on future changes in biodiversity and ecosystem services. A novel computational model (P-systems) was used to model these effects, forecasting a rapid decline in the Eurasian griffon vulture (Gyps fulvus). By contrast, vulture species with greater plasticity in their dietary range appeared less sensitive to declining food availability. This study extends our understanding of vulture ecosystem services, which have social and economic implications.
PMCID: PMC3475340  PMID: 23082243
12.  Antibiotics Threaten Wildlife: Circulating Quinolone Residues and Disease in Avian Scavengers 
PLoS ONE  2008;3(1):e1444.
Antibiotic residues that may be present in carcasses of medicated livestock could pass to and greatly reduce scavenger wildlife populations. We surveyed residues of the quinolones enrofloxacin and its metabolite ciprofloxacin and other antibiotics (amoxicillin and oxytetracycline) in nestling griffon Gyps fulvus, cinereous Aegypius monachus and Egyptian Neophron percnopterus vultures in central Spain. We found high concentrations of antibiotics in the plasma of many nestling cinereous (57%) and Egyptian (40%) vultures. Enrofloxacin and ciprofloxacin were also found in liver samples of all dead cinereous vultures. This is the first report of antibiotic residues in wildlife. We also provide evidence of a direct association between antibiotic residues, primarily quinolones, and severe disease due to bacterial and fungal pathogens. Our results indicate that, by damaging the liver and kidney and through the acquisition and proliferation of pathogens associated with the depletion of lymphoid organs, continuous exposure to antibiotics could increase mortality rates, at least in cinereous vultures. If antibiotics ingested with livestock carrion are clearly implicated in the decline of the vultures in central Spain then it should be considered a primary concern for conservation of their populations.
PMCID: PMC2186382  PMID: 18197254
13.  Do Power Lines and Protected Areas Present a Catch-22 Situation for Cape Vultures (Gyps coprotheres)? 
PLoS ONE  2013;8(10):e76794.
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 km2) and four immature (mean ±SD minimum convex polygon area  =  492,300±259,427 km2) 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.
PMCID: PMC3793913  PMID: 24137496
14.  African Vultures Don’t Follow Migratory Herds: Scavenger Habitat Use Is Not Mediated by Prey Abundance 
PLoS ONE  2014;9(1):e83470.
The ongoing global decline in vulture populations raises major conservation concerns, but little is known about the factors that mediate scavenger habitat use, in particular the importance of abundance of live prey versus prey mortality. We test this using data from the Serengeti-Mara ecosystem in East Africa. The two hypotheses that prey abundance or prey mortality are the main drivers of vulture habitat use provide alternative predictions. If vultures select areas based only on prey abundance, we expect tracked vultures to remain close to herds of migratory wildebeest regardless of season. However, if vultures select areas where mortality rates are greatest then we expect vultures to select the driest regions, where animals are more likely to die of starvation, and to be attracted to migratory wildebeest only during the dry season when wildebeest mortality is greatest. We used data from GSM-GPS transmitters to assess the relationship between three vulture species and migratory wildebeest in the Mara-Serengeti ecosystem. Results indicate that vultures preferentially cluster around migratory herds only during the dry season, when herds experience their highest mortality. Additionally during the wet season, Ruppell’s and Lappet-faced vultures select relatively dry areas, based on Normalized Difference Vegetation Index, whereas White-backed vultures preferred wetter areas during the wet season. Differences in habitat use among species may mediate coexistence in this scavenger guild. In general, our results suggest that prey abundance is not the primary driver of avian scavenger habitat use. The apparent reliance of vultures on non-migratory ungulates during the wet season has important conservation implications for vultures in light of on-going declines in non-migratory ungulate species and use of poisons in unprotected areas.
PMCID: PMC3885425  PMID: 24421887
15.  Levels of Polycyclic Aromatic Hydrocarbons, Polychlorinated Biphenyls, and Organochlorine Pesticides in Various Tissues of White-Backed Vulture in India 
BioMed Research International  2013;2013:190353.
This study provides information on the current status of contamination by polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), and organochlorine pesticides (OCPs) in the tissues of endangered White-backed Vulture Gyps bengalensis in India. Chemical analyses revealed detectable amounts of PAHs, PCBs, and OCPs. Concentration ranges of ∑PAHs, ∑PCBs, and ∑OCPs in tissues were 60–2037 ng/g, 30–5790 ng/g, and 3.2–5836 ng/g wet weight, respectively. 1,1-Dichloro-2,2-bis(p-chlorophenyl)ethylene (p,p′-DDE) concentrations ranged from below detectable level to 599 ng/g wet weight, representing more than 90% of the total dichlorodiphenyltrichloroethane (DDT). Among the various OCPs analyzed, p,p′-DDE was detected most frequently. All the contaminants recorded show higher accumulation in liver than other tissues. Levels of contaminants measured in the tissues of vulture are comparable with the levels documented in a number of avian species and are lower than those reported to have caused deleterious effects. Although no threat is expected from the current level of contamination, the presence of varying levels of contaminants and their additive or synergistic toxicity is a cause of concern to vultures. Values reported in this study can serve as guideline for future research.
PMCID: PMC3830878  PMID: 24288666
16.  The effect of social facilitation on foraging success in vultures: a modelling study 
Biology Letters  2008;4(3):311-313.
The status of many Gyps vulture populations are of acute conservation concern as several show marked and rapid decline. Vultures rely heavily on cues from conspecifics to locate carcasses via local enhancement. A simulation model is developed to explore the roles vulture and carcass densities play in this system, where information transfer plays a key role in locating food. We find a sigmoid relationship describing the probability of vultures finding food as a function of vulture density in the habitat. This relationship suggests a threshold density below which the foraging efficiency of the vulture population will drop rapidly towards zero. Management strategies should closely study this foraging system in order to maintain effective foraging densities.
PMCID: PMC2610049  PMID: 18364309
local enhancement; Allee effect; food finding; scavenging; scrounging; social facilitation
17.  Can Wild Ungulate Carcasses Provide Enough Biomass to Maintain Avian Scavenger Populations? An Empirical Assessment Using a Bio-Inspired Computational Model 
PLoS ONE  2011;6(5):e20248.
The reduction in the amount of food available for European avian scavengers as a consequence of restrictive public health policies is a concern for managers and conservationists. Since 2002, the application of several sanitary regulations has limited the availability of feeding resources provided by domestic carcasses, but theoretical studies assessing whether the availability of food resources provided by wild ungulates are enough to cover energetic requirements are lacking.
We assessed food provided by a wild ungulate population in two areas of NE Spain inhabited by three vulture species and developed a P System computational model to assess the effects of the carrion resources provided on their population dynamics. We compared the real population trend with to a hypothetical scenario in which only food provided by wild ungulates was available. Simulation testing of the model suggests that wild ungulates constitute an important food resource in the Pyrenees and the vulture population inhabiting this area could grow if only the food provided by wild ungulates would be available. On the contrary, in the Pre-Pyrenees there is insufficient food to cover the energy requirements of avian scavenger guilds, declining sharply if biomass from domestic animals would not be available.
Our results suggest that public health legislation can modify scavenger population trends if a large number of domestic ungulate carcasses disappear from the mountains. In this case, food provided by wild ungulates could be not enough and supplementary feeding could be necessary if other alternative food resources are not available (i.e. the reintroduction of wild ungulates), preferably in European Mediterranean scenarios sharing similar and socio-economic conditions where there are low densities of wild ungulates. Managers should anticipate the conservation actions required by assessing food availability and the possible scenarios in order to make the most suitable decisions.
PMCID: PMC3101228  PMID: 21629647
18.  How Predictability of Feeding Patches Affects Home Range and Foraging Habitat Selection in Avian Social Scavengers? 
PLoS ONE  2013;8(1):e53077.
Feeding stations are commonly used to sustain conservation programs of scavengers but their impact on behaviour is still debated. They increase the temporal and spatial predictability of food resources while scavengers have supposedly evolved to search for unpredictable resources. In the Grands Causses (France), a reintroduced population of Griffon vultures Gyps fulvus can find carcasses at three types of sites: 1. “light feeding stations”, where farmers can drop carcasses at their farm (spatially predictable), 2. “heavy feeding stations”, where carcasses from nearby farms are concentrated (spatially and temporally predictable) and 3. open grasslands, where resources are randomly distributed (unpredictable). The impact of feeding stations on vulture’s foraging behaviour was investigated using 28 GPS-tracked vultures. The average home range size was maximal in spring (1272±752 km2) and minimal in winter (473±237 km2) and was highly variable among individuals. Analyses of home range characteristics and feeding habitat selection via compositional analysis showed that feeding stations were always preferred compared to the rest of the habitat where vultures can find unpredictable resources. Feeding stations were particularly used when resources were scarce (summer) or when flight conditions were poor (winter), limiting long-ranging movements. However, when flight conditions were optimal, home ranges also encompassed large areas of grassland where vultures could find unpredictable resources, suggesting that vultures did not lose their natural ability to forage on unpredictable resources, even when feeding stations were available. However during seasons when food abundance and flight conditions were not limited, vultures seemed to favour light over heavy feeding stations, probably because of the reduced intraspecific competition and a pattern closer to the natural dispersion of resources in the landscape. Light feeding stations are interesting tools for managing food resources, but don’t prevent vultures to feed at other places with possibly high risk of intoxication (poison).
PMCID: PMC3536817  PMID: 23301024
19.  Cellular and humoral immunodepression in vultures feeding upon medicated livestock carrion 
Veterinary pharmaceuticals contained in dead livestock may be ingested by avian scavengers and negatively affect their health and consequently their population dynamics and conservation. We evaluated the potential role of antibiotics as immunodepressors using multiple parameters measuring the condition of the cellular and humoral immune system in griffon (Gyps fulvus), cinereous (Aegypius monachus) and Egyptian vultures (Neophron percnopterus). We confirmed the presence of circulating antimicrobial residues, especially quinolones, in nestlings of the three vulture species breeding in central Spain. Individuals ingesting antibiotics showed clearly depressed cellular and humoral immune systems compared with nestlings from the control areas, which did not ingest antibiotics. Within central Spain, we found that individuals with circulating antibiotics showed depressed cellular (especially CD4+and CD8+T-lymphocyte subsets) and humoral (especially acellular APV complement and IL8-like) immune systems compared with nestlings without circulating antibiotics. This suggests that ingestion of antibiotics together with food may depress the immune system of developing nestlings, temporarily reducing their resistance to opportunistic pathogens, which require experimental confirmation. Medicated livestock carrion should be considered inadequate food for vultures due to their detrimental consequences on health derived from the ingestion and potential effects of the veterinary drugs contained in them and for this reason rejected as a management tool in conservation programmes.
PMCID: PMC2677603  PMID: 19324751
carcass; disease; immune system; quinolones; livestock; vultures
20.  Anticipating Knowledge to Inform Species Management: Predicting Spatially Explicit Habitat Suitability of a Colonial Vulture Spreading Its Range 
PLoS ONE  2010;5(8):e12374.
The knowledge of both potential distribution and habitat suitability is fundamental in spreading species to inform in advance management and conservation planning. After a severe decline in the past decades, the griffon vulture (Gyps fulvus) is now spreading its breeding range towards the northwest in Spain and Europe. Because of its key ecological function, anticipated spatial knowledge is required to inform appropriately both vulture and ecosystem management.
Here we used maximum entropy (Maxent) models to determine the habitat suitability of potential and current breeding distribution of the griffon vulture using presence-only data (N = 124 colonies) in north-western Spain. The most relevant ecological factors shaping this habitat suitability were also identified. The resulting model had a high predictive performance and was able to predict species' historical distribution. 7.5% (∼1,850 km2) of the study area resulted to be suitable breeding habitat, most of which (∼70%) is already occupied by the species. Cliff availability and livestock density, especially of sheep and goats, around 10 km of the colonies were the fundamental factors determining breeding habitat suitability for this species.
Griffon vultures could still spread 50–60 km towards the west, increasing their breeding range in 1,782 km2. According to our results, 7.22% of the area suitable for griffon vulture will be affected by wind farms, so our results could help to better plan wind farm locations. The approach here developed could be useful to inform management of reintroductions and recovery programmes currently being implemented for both the griffon vulture and other threatened vulture species.
PMCID: PMC2928263  PMID: 20811501
21.  Seropositivity and Risk Factors Associated with Toxoplasma gondii Infection in Wild Birds from Spain 
PLoS ONE  2011;6(12):e29549.
Toxoplasma gondii is a zoonotic intracellular protozoan parasite of worldwide distribution that infects many species of warm-blooded animals, including birds. To date, there is scant information about the seropositivity of T. gondii and the risk factors associated with T. gondii infection in wild bird populations. In the present study, T. gondii infection was evaluated on sera obtained from 1079 wild birds belonging to 56 species (including Falconiformes (n = 610), Strigiformes (n = 260), Ciconiiformes (n = 156), Gruiformes (n = 21), and other orders (n = 32), from different areas of Spain. Antibodies to T. gondii (modified agglutination test, MAT titer ≥1∶25) were found in 282 (26.1%, IC95%:23.5–28.7) of the 1079 birds. This study constitute the first extensive survey in wild birds species in Spain and reports for the first time T. gondii antibodies in the griffon vulture (Gyps fulvus), short-toed snake-eagle (Circaetus gallicus), Bonelli's eagle (Aquila fasciata), golden eagle (Aquila chrysaetos), bearded vulture (Gypaetus barbatus), osprey (Pandion haliaetus), Montagu's harrier (Circus pygargus), Western marsh-harrier (Circus aeruginosus), peregrine falcon (Falco peregrinus), long-eared owl (Asio otus), common scops owl (Otus scops), Eurasian spoonbill (Platalea leucorodia), white stork (Ciconia ciconia), grey heron (Ardea cinerea), common moorhen (Gallinula chloropus); in the International Union for Conservation of Nature (IUCN) “vulnerable” Spanish imperial eagle (Aquila adalberti), lesser kestrel (Falco naumanni) and great bustard (Otis tarda); and in the IUCN “near threatened” red kite (Milvus milvus). The highest seropositivity by species was observed in the Eurasian eagle owl (Bubo bubo) (68.1%, 98 of 144). The main risk factors associated with T. gondii seropositivity in wild birds were age and diet, with the highest exposure in older animals and in carnivorous wild birds. The results showed that T. gondii infection is widespread and can be at a high level in many wild birds in Spain, most likely related to their feeding behaviour.
PMCID: PMC3245288  PMID: 22216311
22.  Impact of the California Lead Ammunition Ban on Reducing Lead Exposure in Golden Eagles and Turkey Vultures 
PLoS ONE  2011;6(4):e17656.
Predatory and scavenging birds may be exposed to high levels of lead when they ingest shot or bullet fragments embedded in the tissues of animals injured or killed with lead ammunition. Lead poisoning was a contributing factor in the decline of the endangered California condor population in the 1980s, and remains one of the primary factors threatening species recovery. In response to this threat, a ban on the use of lead ammunition for most hunting activities in the range of the condor in California was implemented in 2008. Monitoring of lead exposure in predatory and scavenging birds is essential for assessing the effectiveness of the lead ammunition ban in reducing lead exposure in these species. In this study, we assessed the effectiveness of the regulation in decreasing blood lead concentration in two avian sentinels, golden eagles and turkey vultures, within the condor range in California. We compared blood lead concentration in golden eagles and turkey vultures prior to the lead ammunition ban and one year following implementation of the ban. Lead exposure in both golden eagles and turkey vultures declined significantly post-ban. Our findings provide evidence that hunter compliance with lead ammunition regulations was sufficient to reduce lead exposure in predatory and scavenging birds at our study sites.
PMCID: PMC3071804  PMID: 21494329
23.  Identification of a Novel Mycoplasma Species from an Oriental White-Backed Vulture (Gyps bengalensis) 
Journal of Clinical Microbiology  2004;42(12):5909-5912.
An intracellular organism was isolated from the tissues of an Oriental white-backed vulture (Gyps bengalensis) in chicken embryo fibroblast cell cultures. Biochemical and physical properties, ultrastructural features, and 16S ribosomal DNA sequencing classified this organism as a new taxon of mycoplasma, for which the name “Mycoplasma vulturii” is proposed.
PMCID: PMC535302  PMID: 15583338
24.  Testing the Goodness of Supplementary Feeding to Enhance Population Viability in an Endangered Vulture 
PLoS ONE  2008;3(12):e4084.
Human-predator conflicts are directly or indirectly threatening many species with extinction. Thus, biologists are urged to find simple solutions to complex situations while avoiding unforeseen conservation outcomes. The provision of supplementary food at artificial feeding sites (AFS) is frequently used in the conservation of scavenger bird populations currently suffering from indirect poisoning, although no scientific studies on its effectiveness have been conducted.
Methodology/Principal Findings
We used a long-term data set of 95 individually marked birds from the largest European core of the endangered bearded vulture (Gypaetus barbatus) to test the long-term effects of specific AFS for bearded vultures on their survival rates (by CMR models) and population dynamics (by Monte Carlo simulations) in an area where fatalities derived from illegal poisoning and the use of other toxics like veterinary drugs have increased over the last several years. Our data support the positive relationship between the use of AFS and survival. However, contrary to theoretical predictions (e.g. high and more stable adult survival among long-lived species), the use of AFS increased only survival of pre-adults. Moreover, AFS buffered the effects of illegal poisoning on this age-class, while adult survival decreased over years. Our simulations predicted a maximum value of extinction probability over a time horizon of 50 years. Population projections run with survival rates expected in scenarios without poisoning predicted the situation of least conservation concern, while including only AFS can maintain a large floater surplus that may delay population decline but fails to reduce poisoning risk among adults.
Although AFS are not effective to save bearded vultures from an expected population decline, they delay population extinction and can be a useful tool for prolonging population viability while combating illegal and indirect poisoning. The eradication of different sources of poisoning is of top priority to ensure the long-term viability of this and many other species.
PMCID: PMC2605265  PMID: 19115009
25.  Vultures acquire information on carcass location from scavenging eagles 
Vultures are recognized as the scroungers of the natural world, owing to their ecological role as obligate scavengers. While it is well known that vultures use intraspecific social information as they forage, the possibility of inter-guild social information transfer and the resulting multi-species social dilemmas has not been explored. Here, we use data on arrival times at carcasses to show that such social information transfer occurs, with raptors acting as producers of information and vultures acting as scroungers of information. We develop a game-theoretic model to show that competitive asymmetry, whereby vultures dominate raptors at carcasses, predicts this evolutionary outcome. We support this theoretical prediction using empirical data from competitive interactions at carcasses. Finally, we use an individual-based model to show that these producer–scrounger dynamics lead to vultures being vulnerable to declines in raptor populations. Our results show that social information transfer can lead to important non-trophic interactions among species and highlight important potential links among social evolution, community ecology and conservation biology. With vulture populations suffering global declines, our study underscores the importance of ecosystem-based management for these endangered keystone species.
PMCID: PMC4173674  PMID: 25209935
inter-guild interactions; producer–scrounger game; scavengers; social information; vultures

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