Impact of the California lead ammunition ban on reducing lead exposure in golden eagles and turkey vultures

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.     

Lead poisoning in captive Andean condors (Vultur gryphus)

Elevated lead in the tissues of raptors, especially those that scavenge, is a common occurrence, and lead poisoning appears to be a significant problem in the ongoing recovery effort for California condors (Gymnogyps californianus). Elevated blood lead levels have been found in released birds, and a number of birds have died of lead poisoning. In earlier work, we dosed turkey vultures (Cathartes aura) with lead shot but found them to be a poor model for lead poisoning. In this study, we dosed four Andean condors (Vultur gryphus) with lead shot and found them to be quite sensitive, as two of the birds died and the other two exhibit signs of lead poisoning within 50 days. All lead-responsive parameters were affected, and regurgitation of dosed shot occurred only once. The response of the Andean condors appeared to mimic California condors, suggesting that once exposed to lead, the possibility of survival is poor. This is consistent with observations in the wild, where otherwise healthy birds exposed to metallic lead quickly succumb. At the very least, the release program has to maintain constant surveillance and an active lead monitoring program.     

Lead exposure in free-flying turkey vultures is associated with big game hunting in California

Predatory and scavenging birds are at risk of lead exposure when they feed on animals injured or killed by lead ammunition. While lead ammunition has been banned from waterfowl hunting in North America for almost two decades, lead ammunition is still widely used for hunting big game and small game animals. In this study, we evaluated the association between big game hunting and blood lead concentration in an avian scavenger species that feeds regularly on large mammals in California. We compared blood lead concentration in turkey vultures within and outside of the deer hunting season, and in areas with varying wild pig hunting intensity. Lead exposure in turkey vultures was significantly higher during the deer hunting season compared to the off-season, and blood lead concentration was positively correlated with increasing wild pig hunting intensity. Our results link lead exposure in turkey vultures to deer and wild pig hunting activity at these study sites, and we provide evidence that spent lead ammunition in carrion poses a significant risk of lead exposure to scavengers.     

Seroepidemiologic Survey of Potential Pathogens in Obligate and Facultative Scavenging Avian Species in California

Throughout the world, populations of scavenger birds are declining rapidly with some populations already on the brink of extinction. Much of the current research into the factors contributing to these declines has focused on exposure to drug residues, lead, and other toxins. Despite increased monitoring of these declining populations, little is known about infectious diseases affecting scavenger bird species. To assess potential infectious disease risks to both obligate and facultative scavenger bird species, we performed a serosurvey for eleven potential pathogens in three species of scavenging birds in California: the California condor (Gymnogyps californianus), turkey vulture (Cathartes aura) and golden eagle (Aquila chrysaetos). California condors were seropositive for avian adenovirus, infectious bronchitis virus, Mycoplasma gallisepticum, avian paramyxovirus-2, West Nile virus (WNV) and Toxoplasma gondii. Golden eagles were seropositive for avian adenovirus, Chlamydophila psittaci and Toxoplasma gondii, and turkey vultures were seropositive for avian adenovirus, Chlamydophila psittaci, avian paramyxovirus-1, Toxoplasma gondii and WNV. Risk factor analyses indicated that rearing site and original release location were significantly associated with a positive serologic titer to WNV among free-flying condors. This study provides preliminary baseline data on infectious disease exposure in these populations for aiding in early disease detection and provides potentially critical information for conservation of the endangered California condor as it continues to expand its range and encounter new infectious disease threats.     

Vulture flight behavior and implications for aircraft safety

Growing vulture populations represent increasing hazards to civil and military aircraft. To assess vulture flight behavior and activity patterns at the Marine Corps Air Station in Beaufort, South Carolina, we equipped 11 black vultures (Coragyps atratus) and 11 turkey vultures (Cathartes aura) with solar-powered Global Positioning System (GPS) satellite transmitters during a 2-year study (1 Oct 2006–30 Sep 2008). Turkey vultures had larger seasonal home ranges than did black vultures, and 2 turkey vultures made round-trips to Florida. Black vultures consistently spent less time in flight (8.4%) than did turkey vultures (18.9%), and black vultures flew at higher altitudes than did turkey vultures in all seasons except summer when altitudinal distributions (above ground level) did not differ. Although we recorded maximum altitudes of 1,578 m for black vultures and 1,378 for turkey vultures, most flights were low altitude. A matrix of vulture flight altitude versus time of day revealed that >60% of vulture flight activity occurred from 4 hr to 9 hr after sunrise at altitudes below 200 m. Continuation of aggressive harassment coupled with flexible training schedules to avoid times and altitudes of high vulture activity will decrease hazards to aircraft posed by these birds. © 2011 The Wildlife Society.     

Gram-negative, aerobic, enteric pathogens among intestinal microflora of wild turkey vultures (Cathartes aura) in west central Texas.

The prevalence of gram-negative bacterial species in the intestines of 20 apparently healthy turkey vultures (Cathartes aura) was determined. Edwardsiella tarda, Plesiomonas shigelloides, Salmonella, and Arizona hinshawii (Salmonella arizonae) were each recovered from 15% of these birds. Turkey vultures may be important reservoirs of these bacterial pathogens.     

Acute oral toxicity of sodium cyanide in birds

Sensitivities of six avian species, black vulture (Coragyps atratus), American kestrel (Falco sparverius), Japanese quail (Coturnix japonica), domestic chicken (Gallus domesticus), eastern screech-owl (Otus asio), and European starling (Sturnus vulgaris), to acute poisoning by sodium cyanide (NaCN) were compared by single dose LD50's. Three species, domestic chickens, black vultures, and turkey vultures (Cathartes aura), were dosed with NaCN to determine cyanide residues in those that died and also in survivors, in addition to postmortem fate. Three flesh-eating species (black vulture, American kestrel, and eastern screech-owl; LD50's 4.0-8.6 mg/kg) were more sensitive to NaCN than three species (Japanese quail, domestic chicken, and European starling; LD50's 9.4-21 mg/kg) that fed predominantly on plant material. Elevated concentrations of cyanide were found in the blood of birds that died of cyanide poisoning; however, concentrations in birds that died overlapped those in survivors. Blood was superior to liver as the tissue of choice for detecting cyanide exposure. No gross pathological changes related to dosing were observed at necropsy.     

Hematozoa and a new haemoproteid species from Cathartidae (New World vulture) in South Carolina

A survey of turkey vultures (Cathartes aura) in South Carolina revealed the presence of a novel haemoproteid. Haemoproteus catharti n. sp. is described from the slides developed from the blood of this vulture. The new species is a thick, halteridial form with complete margins, and is considered distinct from the other recognized haemoproteids from the diurnal raptors in shape, pigment number, parasite outline, and host-family specificity. While reviewing blood films, a series of unusual immature schizonts of Plasmodium sp. were also observed, and these are illustrated, along with another distinct haemoproteid from old slides of poor quality produced from turkey vulture blood.     

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.     

Antibodies to Clostridium botulinum toxins in free-living birds and mammals.

Naturally-occuring antibodies against Clostridium botulinum toxins were found in Cathartes aura (turkey vultures), Canis latrans (coyotes) and Corvus brachyrhynchos (crows) by the passive hemagglutination (PHA) test and verified by the serum neutralization (SN) test. The prevalence of IHA antibodies was 18 of 20 vultures (90%), 5 of 12 crows (42%) and 25 to 110 coyotes (23%). Vultures and coyotes were seropositive by the PHA test against A, B, C, D, and F toxins. The highest antibody titer 1:8192 was in vulture serum against type C. In descending order, the highest antibody levels were against type C, D, F, E, A and B toxins.     

Environmental drivers of variability in the movement ecology of turkey vultures (Cathartes aura) in North and South America

Variation is key to the adaptability of species and their ability to survive changes to the Earth''s climate and habitats. Plasticity in movement strategies allows a species to better track spatial dynamics of habitat quality. We describe the mechanisms that shape the movement of a long-distance migrant bird (turkey vulture, Cathartes aura) across two continents using satellite tracking coupled with remote-sensing science. Using nearly 10 years of data from 24 satellite-tracked vultures in four distinct populations, we describe an enormous amount of variation in their movement patterns. We related vulture movement to environmental conditions and found important correlations explaining how far they need to move to find food (indexed by the Normalized Difference Vegetation Index) and how fast they can move based on the prevalence of thermals and temperature. We conclude that the extensive variability in the movement ecology of turkey vultures, facilitated by their energetically efficient thermal soaring, suggests that this species is likely to do well across periods of modest climate change. The large scale and sample sizes needed for such analysis in a widespread migrant emphasizes the need for integrated and collaborative efforts to obtain tracking data and for policies, tools and open datasets to encourage such collaborations and data sharing.     

Hematozoa from Southern African vultures, with a description of Haemoproteus janovyi sp. n.

This study represents the first major survey of avian hematozoa from southern Africa and the only one dealing with blood parasites of vultures. Blood smears from 506 Rhodesian, Botswanan and South African vultures (Hooded, White-headed, Lappetfaced, Cape Griffon and Whitebacked Vultures) were examined for hematozoa. Haemoproteus janovyi sp. n. was observed in 35.2% of the vultures, Leucocytozoon toddi in 0.8%, Plasmodium fallax in 0.6%, Atoxoplasma sp. in 1.4% and microfilariae in 0.2%. Hematozoan prevalence increased with age of the vultures. Only 2 of 133 nestlings sampled during the dry season had patent parasitemias (L. toddi). Haemoproteid prevalence in immature vultures was depressed during the dry season, whereas it was stable throughout the year in adults. The only species which nests on cliffs (the Cape Griffon Vulture) did not harbor hematozoa whereas the other species which nest and roost in trees were infected with at least one hematozoan species.     

Testing the importance of individual nest-site selection for a social and group-living vulture

Nest-site selection by species is expected to be adaptive and lead to improved breeding productivity, but in some settings, there exist mismatches between preferred nesting habitat and breeding productivity. We tested the expectation that nest-site selection is adaptive in a sample of 63 nests of a long-lived social species that breeds and forages in groups: the critically endangered white-backed vulture (Gyps africanus). By studying breeding groups in the same area, we controlled for landscape-level effects on habitat selection and investigated how fine-scale nest-site characteristics affect breeding productivity. We developed models to assess how nine characteristics of nest sites selected by breeding vultures compared with 70 random trees and tested associations between these characteristics and breeding productivity. White-backed vultures selected nest sites in taller trees (>7 m), but neither tree height nor any other nest-site characteristics had a clear effect on breeding productivity. Vultures selected nest trees closer to each other than random trees, and the associations between nest density, nearest neighbour distance and breeding success were all positive. These positive associations and the absence of an observable effect between nest-site characteristics and breeding productivity suggest that for this semi-colonial breeder, the social imperative of proximity to conspecifics (i.e., nesting near other vultures and group foraging) may be more important than individual nest-site selection.     

Characteristics of Mycoplasma meleagridis sp. n., Isolated from Turkeys.

Yamamoto, R. (University of California, Davis), C. H. Bigland, and H. B. Ortmayer. Characteristics of Mycoplasma meleagridis sp. n., isolated from turkeys. J. Bacteriol. 90:47-49. 1965.-A designation is proposed for a pathogenic Mycoplasma species isolated from turkeys. The organism originally was recovered from the air-sac lesion of a turkey poult in 1957, and was designated the "N" strain. Mycoplasma species with identical characteristics have since been recovered from the sinus, trachea, oviduct, vagina, semen, and bursa of Fabricius of turkeys. The organism has been recovered from many turkey flocks throughout the country. Many investigators have confirmed the original finding that this organism is antigenically distinct from other known serotypes of Mycoplasma found in poultry. The species proposed is Mycoplasma meleagridis sp. n.     

NSAIDs and scavenging birds: potential impacts beyond Asia's critically endangered vultures

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.     

Estimating updraft velocity components over large spatial scales: contrasting migration strategies of golden eagles and turkey vultures

Soaring birds migrate in massive numbers worldwide. These migrations are complex and dynamic phenomena, strongly influenced by meteorological conditions that produce thermal and orographic uplift as the birds traverse the landscape. Herein we report on how methods were developed to estimate the strength of thermal and orographic uplift using publicly available digital weather and topography datasets at continental scale. We apply these methods to contrast flight strategies of two morphologically similar but behaviourally different species: golden eagle, Aquila chrysaetos, and turkey vulture, Cathartes aura, during autumn migration across eastern North America tracked using GPS tags. We show that turkey vultures nearly exclusively used thermal lift, whereas golden eagles primarily use orographic lift during migration. It has not been shown previously that migration tracks are affected by species-specific specialisation to a particular uplift mode. The methods introduced herein to estimate uplift components and test for differences in weather use can be applied to study movement of any soaring species.     

Can Ingestion of Lead Shot and Poisons Change Population Trends of Three European Birds: Grey Partridge,Common Buzzard,and Red Kite?

Little is known about the magnitude of the effects of lead shot ingestion alone or combined with poisons (e.g., in bait or seeds/granules containing pesticides) on population size, growth, and extinction of non-waterbird avian species that ingest these substances. We used population models to create example scenarios demonstrating how changes in these parameters might affect three susceptible species: grey partridge (Perdix perdix), common buzzard (Buteo buteo), and red kite (Milvus milvus). We added or subtracted estimates of mortality due to lead shot ingestion (4–16% of mortality, depending on species) and poisons (4–46% of mortality) reported in the UK or France to observed mortality of studied populations after models were calibrated to observed population trends. Observed trends were decreasing for partridge (in continental Europe), stable for buzzard (in Germany), and increasing for red kite (in Wales). Although lead shot ingestion and poison at modeled levels did not change the trend direction for the three species, they reduced population size and slowed population growth. Lead shot ingestion at modeled rates reduced population size of partridges by 10%, and when combined with bait and pesticide poisons, by 18%. For buzzards, decrease in mean population size by lead shot and poisons combined was much smaller (≤ 1%). The red kite population has been recovering; however, modeled lead shot ingestion reduced its annual growth rate from 6.5% to 4%, slowing recovery. If mortality from poisoned baits could be removed, the kite population could potentially increase at a rapid annual rate of 12%. The effects are somewhat higher if ingestion of these substances additionally causes sublethal reproductive impairment. These results have uncertainty but suggest that declining or recovering populations are most sensitive to lead shot or poison ingestion, and removal of poisoned baits can have a positive impact on recovering raptor populations that frequently feed on carrion.     

Long-Term Temporal and Spatial Fluctuations of Soft Bottom Infaunal Invertebrates Associated with an Ocean Outfall from the San Pedro Shelf,California

Temporal (annual) and spatial fluctuations of soft-bottom invertebrates from 1977 to 1988 were reviewed and analyzed from an ocean outfall area on the San Pedro Shelf, California. Several dominant species which occurred throughout the monitoring period provide continuity between early sampling efforts and recent ones. Annual fluctuations in the mean number of species, abundance, diversity and biomass were generally conservative compared to spatial fluctuations. Temporal changes of note include a marked reduction in abundance and biomass between 1981 and 1984 and another decline in biomass in 1988. The former was associated with conditions of the 1982–1983 El Niño, and the latter with a shift in population dominance from a bivalve to a polychaete. Mean abundance and biomass were enhanced by the outfall without a significant reduction in number of species. The response of the biota to the outfall extended further upcoast (northwest) than downcoast. Several hypotheses were posed and briefly examined. These include the effects of total suspended solids generated from the outfall, and the role of the “Three Little Pigs” (bivalve-Parvilucina tenuisculpta CARPENTER , ostracod-Euphilomedes carcharodonta (SMITH ), polychaete-Capitella capitata (FABRICIUS )) in influencing benthic community structure. Finally, measures of infauna from the San Pedro Shelf were, except for abundance, very similar to those reported from other California shelf areas. Through time and space the outfall has had limited negative effect on infaunal community structure.     

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.     

A Global Review of Causes of Morbidity and Mortality in Free-Living Vultures

Vulture species worldwide play a key role in ecosystems as obligate scavengers, and several populations have had precipitous declines. Research on vulture health is critical to conservation efforts including free-living vultures and captive breeding programs, but is limited to date. In this systematic review, we determined the reported causes of free-living vulture species morbidity and mortality worldwide. The most commonly reported cause of mortality was from toxins (60%), especially lead and pesticides, followed by traumatic injury (49%), including collisions with urban infrastructure and gunshot. Neglected areas of research in free-living vulture health include infectious diseases (16%), endocrine and nutritional disorders (6%), and neoplasia (<?1%). Almost half of the studies included in the review were conducted in either Spain or the USA, with a paucity of studies conducted in South America and sub-Saharan Africa. The highest number of studies was on Griffon (Gyps fulvus) (24%) and Egyptian vultures (Neophron percnopterus) (19%), while half of all vulture species had five or fewer studies. Future investigations on free-living vulture health should focus on neglected areas of research, such as infectious diseases, and areas with gaps in the current literature, such as South America, sub-Saharan Africa, and under-studied vulture species.