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1.  Building Development and Roads: Implications for the Distribution of Stone Curlews across the Brecks 
PLoS ONE  2013;8(8):e72984.
Substantial new housing and infrastructure development planned within England has the potential to conflict with the nature conservation interests of protected sites. The Breckland area of eastern England (the Brecks) is designated as a Special Protection Area for a number of bird species, including the stone curlew (for which it holds more than 60% of the UK total population). We explore the effect of buildings and roads on the spatial distribution of stone curlew nests across the Brecks in order to inform strategic development plans to avoid adverse effects on such European protected sites.
Using data across all years (and subsets of years) over the period 1988-2006 but restricted to habitat areas of arable land with suitable soils, we assessed nest density in relation to the distances to nearest settlements and to major roads. Measures of the local density of nearby buildings, roads and traffic levels were assessed using normal kernel distance-weighting functions. Quasi-Poisson generalised linear mixed models allowing for spatial auto-correlation were fitted.
Significantly lower densities of stone curlew nests were found at distances up to 1500m from settlements, and distances up to 1000m or more from major (trunk) roads. The best fitting models involved optimally distance-weighted variables for the extent of nearby buildings and the trunk road traffic levels.
The results and predictions from this study of past data suggests there is cause for concern that future housing development and associated road infrastructure within the Breckland area could have negative impacts on the nesting stone curlew population. Given the strict legal protection afforded to the SPA the planning and conservation bodies have subsequently agreed precautionary restrictions on building development within the distances identified and used the modelling predictions to agree mitigation measures for proposed trunk road developments.
PMCID: PMC3758259  PMID: 24023662
2.  Conserving the Birds of Uganda’s Banana-Coffee Arc: Land Sparing and Land Sharing Compared 
PLoS ONE  2013;8(2):e54597.
Reconciling the aims of feeding an ever more demanding human population and conserving biodiversity is a difficult challenge. Here, we explore potential solutions by assessing whether land sparing (farming for high yield, potentially enabling the protection of non-farmland habitat), land sharing (lower yielding farming with more biodiversity within farmland) or a mixed strategy would result in better bird conservation outcomes for a specified level of agricultural production. We surveyed forest and farmland study areas in southern Uganda, measuring the population density of 256 bird species and agricultural yield: food energy and gross income. Parametric non-linear functions relating density to yield were fitted. Species were identified as “winners” (total population size always at least as great with agriculture present as without it) or “losers” (total population sometimes or always reduced with agriculture present) for a range of targets for total agricultural production. For each target we determined whether each species would be predicted to have a higher total population with land sparing, land sharing or with any intermediate level of sparing at an intermediate yield. We found that most species were expected to have their highest total populations with land sparing, particularly loser species and species with small global range sizes. Hence, more species would benefit from high-yield farming if used as part of a strategy to reduce forest loss than from low-yield farming and land sharing, as has been found in Ghana and India in a previous study. We caution against advocacy for high-yield farming alone as a means to deliver land sparing if it is done without strong protection for natural habitats, other ecosystem services and social welfare. Instead, we suggest that conservationists explore how conservation and agricultural policies can be better integrated to deliver land sparing by, for example, combining land-use planning and agronomic support for small farmers.
PMCID: PMC3563584  PMID: 23390501
3.  The Population Decline of Gyps Vultures in India and Nepal Has Slowed since Veterinary Use of Diclofenac was Banned 
PLoS ONE  2012;7(11):e49118.
Populations of oriental white-backed vulture (Gyps bengalensis), long-billed vulture (Gyps indicus) and slender-billed vulture (Gyps tenuirostris) crashed during the mid-1990s throughout the Indian subcontinent. Surveys in India, initially conducted in 1991–1993 and repeated in 2000, 2002, 2003 and 2007, revealed that the population of Gyps bengalensis had fallen by 2007 to 0.1% of its numbers in the early 1990s, with the population of Gyps indicus and G. tenuirostris combined having fallen to 3.2% of its earlier level. A survey of G. bengalensis in western Nepal indicated that the size of the population in 2009 was 25% of that in 2002. In this paper, repeat surveys conducted in 2011 were analysed to estimate recent population trends. Populations of all three species of vulture remained at a low level, but the decline had slowed and may even have reversed for G. bengalensis, both in India and Nepal. However, estimates of the most recent population trends are imprecise, so it is possible that declines may be continuing, though at a significantly slower rate. The degree to which the decline of G. bengalensis in India has slowed is consistent with the expected effects on population trend of a measured change in the level of contamination of ungulate carcasses with the drug diclofenac, which is toxic to vultures, following a ban on its veterinary use in 2006. The most recent available information indicates that the elimination of diclofenac from the vultures’ food supply is incomplete, so further efforts are required to fully implement the ban.
PMCID: PMC3492300  PMID: 23145090
4.  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
5.  Potential Hazard to Human Health from Exposure to Fragments of Lead Bullets and Shot in the Tissues of Game Animals 
PLoS ONE  2010;5(4):e10315.
Lead is highly toxic to animals. Humans eating game killed using lead ammunition generally avoid swallowing shot or bullets and dietary lead exposure from this source has been considered low. Recent evidence illustrates that lead bullets fragment on impact, leaving small lead particles widely distributed in game tissues. Our paper asks whether lead gunshot pellets also fragment upon impact, and whether lead derived from spent gunshot and bullets in the tissues of game animals could pose a threat to human health.
Methodology/Principal Findings
Wild-shot gamebirds (6 species) obtained in the UK were X-rayed to determine the number of shot and shot fragments present, and cooked using typical methods. Shot were then removed to simulate realistic practice before consumption, and lead concentrations determined. Data from the Veterinary Medicines Directorate Statutory Surveillance Programme documenting lead levels in raw tissues of wild gamebirds and deer, without shot being removed, are also presented. Gamebirds containing ≥5 shot had high tissue lead concentrations, but some with fewer or no shot also had high lead concentrations, confirming X-ray results indicating that small lead fragments remain in the flesh of birds even when the shot exits the body. A high proportion of samples from both surveys had lead concentrations exceeding the European Union Maximum Level of 100 ppb w.w. (0.1 mg kg−1 w.w.) for meat from bovine animals, sheep, pigs and poultry (no level is set for game meat), some by several orders of magnitude. High, but feasible, levels of consumption of some species could result in the current FAO/WHO Provisional Weekly Tolerable Intake of lead being exceeded.
The potential health hazard from lead ingested in the meat of game animals may be larger than previous risk assessments indicated, especially for vulnerable groups, such as children, and those consuming large amounts of game.
PMCID: PMC2859935  PMID: 20436670
6.  Performance of climate envelope models in retrodicting recent changes in bird population size from observed climatic change 
Biology Letters  2008;4(5):599-602.
Twenty-five-year population trends of 42 bird species rare as breeders in the UK were examined in relation to changes in climatic suitability simulated using climatic envelope models. The effects of a series of potential ‘nuisance’ variables were also assessed. A statistically significant positive correlation was found across species between population trend and climate suitability trend. The demonstration that climate envelope models are able to retrodict species' population trends provides a valuable validation of their use in studies of the potential impacts of future climatic changes.
PMCID: PMC2610063  PMID: 18664422
Rare Breeding Birds Panel; climate envelope models; climate response surface models; population trends; climate suitability
7.  Demographic mechanism of a historical bird population collapse reconstructed using museum specimens 
Long-term studies of demographic rates provide clues about the external causes of animal population declines, but systematic monitoring is rarely in place until after the decline has occurred. This study evaluates alternative hypotheses about the demographic mechanisms underlying the historical collapse of corncrake (Crex crex) populations in Britain and Ireland in the late nineteenth and early twentieth centuries using characteristics of museum specimens. The proportion of adult corncrakes that are 1-year old was estimated from feather characteristics of birds collected before, during and after the population decline and showed a marked transitory reduction during the decline. This pattern would be expected if the decline was caused by a large reduction in the recruitment of young birds to the breeding population and is the opposite of what would be expected if a change in adult survival had caused the decline. These results are consistent with previous suggestions that the corncrake population decline was caused by adverse effects on breeding productivity caused by the mechanization of the harvesting of hay crops.
PMCID: PMC2603222  PMID: 18628123
corncrake; demographic rate; population model; age structure; agriculture
8.  An Indicator of the Impact of Climatic Change on European Bird Populations 
PLoS ONE  2009;4(3):e4678.
Rapid climatic change poses a threat to global biodiversity. There is extensive evidence that recent climatic change has affected animal and plant populations, but no indicators exist that summarise impacts over many species and large areas. We use data on long-term population trends of European birds to develop such an indicator. We find a significant relationship between interspecific variation in population trend and the change in potential range extent between the late 20th and late 21st centuries, forecasted by climatic envelope models. Our indicator measures divergence in population trend between bird species predicted by climatic envelope models to be favourably affected by climatic change and those adversely affected. The indicator shows a rapid increase in the past twenty years, coinciding with a period of rapid warming.
PMCID: PMC2649536  PMID: 19259270
9.  Effectiveness of Action to Reduce Exposure of Free-Ranging California Condors in Arizona and Utah to Lead from Spent Ammunition 
PLoS ONE  2008;3(12):e4022.
California condors (Gymnogyps californianus) released into the wild in Arizona ranged widely in Arizona and Utah. Previous studies have shown that the blood lead concentrations of many of the birds rise because of ingestion of spent lead ammunition. Condors were routinely recaptured and treated to reduce their lead levels as necessary but, even so, several died from lead poisoning. We used tracking data from VHF and satellite tags, together with the results of routine testing of blood lead concentrations, to estimate daily changes in blood lead level in relation to the location of each bird. The mean daily increment in blood lead concentration depended upon both the location of the bird and the time of year. Birds that spent time during the deer hunting season in two areas in which deer were shot with lead ammunition (Kaibab Plateau (Arizona) and Zion (Utah)) were especially likely to have high blood lead levels. The influence upon blood lead level of presence in a particular area declined with time elapsed since the bird was last there. We estimated the daily blood lead level for each bird and its influence upon daily mortality rate from lead poisoning. Condors with high blood lead over a protracted period were much more likely to die than birds with low blood lead or short-term elevation. We simulated the effect of ending the existing lead exposure reduction measures at Kaibab Plateau, which encourage the voluntary use of non-lead ammunition and removal of gut piles of deer and elk killed using lead ammunition. The estimated mortality rate due to lead in the absence of this program was sufficiently high that the condor population would be expected to decline rapidly. The extension of the existing lead reduction program to cover Zion (Utah), as well as the Kaibab plateau, would be expected to reduce mortality caused by lead substantially and allow the condor population to increase.
PMCID: PMC2603582  PMID: 19107211
10.  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
11.  Potential Impacts of Climatic Change on European Breeding Birds 
PLoS ONE  2008;3(1):e1439.
Climatic change is expected to lead to changes in species' geographical ranges. Adaptation strategies for biodiversity conservation require quantitative estimates of the magnitude, direction and rates of these potential changes. Such estimates are of greatest value when they are made for large ensembles of species and for extensive (sub-continental or continental) regions.
Methodology/Principal Findings
For six climate scenarios for 2070–99 changes have been estimated for 431 European breeding bird species using models relating species' distributions in Europe to climate. Mean range centroid potentially shifted 258–882 km in a direction between 341° (NNW) and 45° (NE), depending upon the climate scenario considered. Potential future range extent averaged 72–89% of the present range, and overlapped the present range by an average of 31–53% of the extent of the present range. Even if potential range changes were realised, the average number of species breeding per 50×50 km grid square would decrease by 6·8–23·2%. Many species endemic or near-endemic to Europe have little or no overlap between their present and potential future ranges; such species face an enhanced extinction risk as a consequence of climatic change.
Although many human activities exert pressures upon wildlife, the magnitude of the potential impacts estimated for European breeding birds emphasises the importance of climatic change. The development of adaptation strategies for biodiversity conservation in the face of climatic change is an urgent need; such strategies must take into account quantitative evidence of potential climatic change impacts such as is presented here.
PMCID: PMC2186378  PMID: 18197250
12.  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
13.  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
14.  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
15.  The Living Planet Index: using species population time series to track trends in biodiversity 
The Living Planet Index was developed to measure the changing state of the world's biodiversity over time. It uses time-series data to calculate average rates of change in a large number of populations of terrestrial, freshwater and marine vertebrate species. The dataset contains about 3000 population time series for over 1100 species. Two methods of calculating the index are outlined: the chain method and a method based on linear modelling of log-transformed data. The dataset is analysed to compare the relative representation of biogeographic realms, ecoregional biomes, threat status and taxonomic groups among species contributing to the index.
The two methods show very similar results: terrestrial species declined on average by 25% from 1970 to 2000. Birds and mammals are over-represented in comparison with other vertebrate classes, and temperate species are over-represented compared with tropical species, but there is little difference in representation between threatened and non-threatened species. Some of the problems arising from over-representation are reduced by the way in which the index is calculated. It may be possible to reduce this further by post-stratification and weighting, but new information would first need to be collected for data-poor classes, realms and biomes.
PMCID: PMC1569448  PMID: 15814346
Living Planet Index; biodiversity indicator; species population trends; representation; 2010 target
16.  The 2010 challenge: data availability, information needs and extraterrestrial insights 
At the 2002 Johannesburg World Summit on Sustainable Development, 190 countries endorsed a commitment to achieve, by 2010, a significant reduction of the current rate of biodiversity loss at the global, regional and national levels. A wide range of approaches is available to the monitoring of progress towards this objective. The strengths and weaknesses of many of these approaches are considered, with special attention being given to the proposed and existing indicators described in the other papers in this issue. Recommendations are made about the development of indicators. Most existing and proposed indicators use data collected for other purposes, which may be unrepresentative. In the short term, much remains to be done in expanding the databases and improving the statistical techniques that underpin these indicators to minimize potential biases. In the longer term, indicators based on unrepresentative data should be replaced with equivalents based on carefully designed sampling programmes. Many proposed and existing indicators do not connect clearly with human welfare and they are unlikely to engage the interest of governments, businesses and the public until they do so. The extent to which the indicators already proposed by parties to the Convention on Biological Diversity are sufficient is explored by reference to the advice an imaginary scientific consultant from another planet might give. This exercise reveals that the range of taxa and biomes covered by existing indicators is incomplete compared with the knowledge we need to protect our interests. More fundamentally, our understanding of the mechanisms linking together the status of biodiversity, Earth system processes, human decisions and actions, and ecosystem services impacting human welfare is still too crude to allow us to infer reliably that actions taken to conserve biodiversity and protect ecosystem services are well chosen and effectively implemented. The involvement of social and Earth system scientists, as well as biologists, in collaborative research programmes to build and parameterize models of the Earth system to elucidate these mechanisms is a high priority.
PMCID: PMC1569447  PMID: 15814341
2010 target; biodiversity loss; monitoring; indicator; wild nature
17.  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

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