A comparison of two methods to establish the prevalence of lead shot ingestion in mallards (Anas platyrhynchos) from The Netherlands

Two collection methods for screening the mallard (Anas platyrhynchos) population in the Netherlands for the ingestion of spent lead shot were compared. One method consisted of examination of gizzards from mallards shot by hunters (n = 2,859) and the other method consisted of examination of gizzards from mallards caught in duck traps (n = 865). The 95% confidence interval of lead shot ingestion in the mallard population estimated by the first method was 1.7 to 2.9% and by the second method 1.1 to 3.1%. These values were not significantly different. From the numbers of lead pellets embedded in the gizzard wall in hunter-killed and trapped mallards it was estimated that at least 22 to 68% of the trapped ducks had been hit by lead shot previously, but survived. Furthermore, this study shows that it is reasonable to assume that a substantial part of the pellets which are identified (in this study and other studies) as ingested, may well have been shot into the gizzard lumen at some time before the birds were actually killed. To avoid lead poisoning in mallards and in raptors depredating waterfowl hit by lead shot, a change to steel shot is advocated.     

The role of lead in a syndrome of clenched claw paralysis and leg paresis in Swamp Harriers (Circus approximans)

We investigated the hypothesis that lead poisoning was the cause of the clinical syndrome of clenched feet paralysis and leg paresis in wild raptors. Swamp Harriers (Circus approximans) are one of three extant native raptor species in New Zealand. Harriers with the syndrome were found to have statistically significantly higher blood lead concentrations than those without clenched feet (t-test; t=-4.06, df=5, P=0.01). However, elevated blood lead concentrations were also present in 60% of wild harriers without the clinical syndrome of clenched feet paralysis and leg paresis. There were features of the response to chelation treatment, electroneurodiagnostics, and pathology that were inconsistent with lead poisoning as reported in other birds of prey. We conclude that lead may be a factor in the expression of this clinical syndrome of clenched claw paralysis but that other factors not identified in our study play a role in the expression of the disease.     

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.     

The link between feeding ecology and lead poisoning in white-tailed eagles

Lead poisoning affects numerous threatened raptors and is a major cause of death in white-tailed eagles (Haliaeetus albicilla). A major reason for intoxication is assumed to be lead fragments ingested while feeding on game animals killed by lead-based projectiles. However, empirical evidence on the relevance of carrion in raptor diets remains scarce. We therefore investigated the link between raptor feeding ecology and lead poisoning, with white-tailed eagles as a model species for scavenging birds. We collected data on seasonal diet composition and food availability of 7 territorial white-tailed eagle pairs in northeastern Germany. We also analyzed stomach contents (SCs) of 126 eagles found dead from 1996 to 2008 throughout Germany. Multiple regression models revealed that fish were the primary prey for eagles, and waterfowl and carcasses of game mammals comprised a large portion of alternative diet components. Eagles used individual foraging tactics, adjusted to local food supply, to maximize profitability. They showed a type II functional response to fish availability. When fish availability sharply declined, eagles switched to waterfowl and carrion. The consumption of game mammal carrion increased over autumn and winter and was positively correlated with a concomitant seasonal increase in the incidence of lead poisoning in eagles throughout Germany. The stomachs of lead-poisoned eagles predominantly contained game ungulate remains. These results indicate that carcasses of game mammals were the major sources of lead fragments. The link between raptor feeding ecology and lead poisoning is the specific functional response of raptors to changing food availability or poor habitat quality, leading to scavenging on lead-contaminated carrion. This shows that carrion constitutes a considerable threat to white-tailed eagles and other birds with similar feeding habits as long as it contains lead bullet fragments. Conservation management of scavenging birds would be substantially improved if carrion was free of lead bullet fragments. One method to achieve this is the widespread introduction of lead-free ammunition. © 2012 The Wildlife Society.     

Changes in fatty acid composition of lipids from birds, rodents, and preschool children exposed to lead

Chronic treatment with inorganic lead (Pb) has been shown to increase the proportion of arachidonic acid (ArA), as well as the arachidonate/linoleate (ArA/LA) ratio, in the fatty acids of lipids from a variety of avian tissues. Changes in two fatty acid-mediated phenomena, peroxidation of membrane lipids and synthesis of eicosanoid cytokines, are associated with this enhanced ArA content. The authors are not aware of any reports in the literature in which these effects of Pb have been described for any animals other than birds. In the current study, the authors investigated the effect of Pb on lipid metabolism in three species: avian, rodent, and human. The group of children identified as suffering environmental Pb exposure were from a Pb-surveillance program and had blood Pb concentrations (PbB) averaging 23 μg/dL. Turkey poults fed 100 ppm dietary Pb as Pb acetate-trihydrate for 19 d had a PbB of 46 μg/dL. Gastric intubation of rats with 80 mg Pb/kg/d for 10 d resulted in a PbB of 74 μg/dL. We analyzed fatty acid composition of whole blood from children, poults, and virgin rats. Low-dose (nongrowth inhibitory) Pb exposure resulted in significantly increased ArA concentration and ArA/LA ratio in blood from all species. Also analyzed were plasma and liver of poults, virgin rats, and pregnant rats and their fetuses. In plasma and liver from Pb-treated poults and virgin rats, ArA and the ArA/LA ratio were again enhanced. Pb intoxication also affected ω3 composition, increasing the concentrations of all long-chain ω3 fatty acids of fetuses from Pb-treated pregnant dams. The authors propose that altered fatty acid metabolism may be responsible for some indications of Pb poisoning. Possible consequences mediated through lipid peroxidation and production of ArA-derivative eicosanoids are considered.     

Spatial and temporal variation in lead levels related to body condition in the Mississippi Valley population of Canada geese

Concern over lead poisoning led to progressive prohibition of toxic shot to harvest waterfowl in the 1980's. Nevertheless, waterfowl remain susceptible to ingestion of lead shot because illegal use continues and spent shot persists in soil and wetland substrates. While mortality due to lead toxicosis has subsided, sublethal effects may still affect survival and reproduction. We measured liver lead levels and body condition in 732 Canada geese (Branta canadensis interior) during July 1984 to April 1989 in southern Illinois (USA), east-central Wisconsin (USA), and northern Ontario (Canada). Although we sampled only individuals that were visibly healthy, 55 of 732 (7.5%) geese had elevated liver lead levels (> 2 ppm). Lead levels of 46 (6.3%) geese indicated subclinical poisoning (2-6 ppm) and 9 (1.2%) geese had lead levels indicative of clinical poisoning (> 6 ppm). A greater proportion of juveniles (14.3%) had elevated lead levels than did adults (6.0%), but there was no difference between genders. Lead levels were highest in autumn and winter in southern Illinois, but were low during nesting and summer, despite legal use of lead shot in northern Ontario during our study. Lead poisoning (> or = 5% of the population) was still evident during all seasons in juveniles, and during autumn and winter in adults, 5 to 10 yr after toxic shot was banned from areas where we collected geese during migration and winter. Elevated lead levels did not affect total body mass, lipid reserves, or mineral levels of geese we collected. Protein levels also were unaffected below 10 ppm, but there was evidence of decline at higher concentrations. Thus, it seems unlikely that lead exposure currently affects survival or reproduction of Mississippi Valley Population (MVP) geese via body condition, although other sublethal effects cannot be discounted.     

Lead poisoning in wild waterfowl in Japan

We collected 430 harvested ducks (Anas sp. and Aythya sp.) from nine prefectures in Japan between 1994 and 1997. Fifteen (4%) of 363 birds harvested during and after hunting seasons had one lead pellet each in the proventriculus and gizzard. In addition, 32 (34%) of 93 swans (Cygnus sp.) and two of 14 geese (Anser sp.) found dead from various wetlands had lesions consistent with lead poisoning. One to nine swans suspected of having toxicosis from ingestion of lead shot were found dead each year. Twenty-seven (84%) of the 32 lead-exposured swans were found in Hokkaido Prefecture. We concluded that lead poisoning is still a serious threat to waterfowl in Japan and that there is considerable need for environmental improvement concerning this problem.     

Occurrence of mycoplasmas in free-ranging birds of prey in Germany

Mycoplasmas are well-known avian pathogens of poultry and some passerines. Although reported in birds of prey, their role as pathogens is still unclear. Healthy, free-ranging raptor nestlings sampled during a routine ringing (banding) program, and birds of prey from rehabilitation centers, tested positive for Mycoplasma spp. by culture and a genus-specific polymerase chain reaction (PCR). Given the lack of clinical signs and disease, we suggest that mycoplasmas in raptors may be commensal rather than pathogenic. Using immunobinding assay and species-specific PCR tests, Mycoplasma buteonis, M. falconis, and M. gypis were identified; M. falconis was only detected in falcons. Additionally, some isolates could not be identified. This is the first report of Mycoplasma spp. isolations from Western Marsh Harriers (Circus aeroginosus), a Eurasian Hobby (Falco subbuteo), and a Barn Owl (Tyto alba).     

Causes of mortality in the Mute swan Cygnus olor on the River Thames

Over the last 20 years there has been an unprecedented decline of the Mute swan on the River Thames. Between August 1979 and October 1981 a systematic attempt was made to collect as many swan corpses as possible. Of 94 swan corpses examined at post-mortem 57% died from lead poisoning due to ingestion of anglers' weights. Birds dying from lead poisoning had significantly higher liver and kidney lead levels. Kidney proved to be the most useful indicator tissue, the median lead level in birds with lead weights in their gizzard was 908 μg/g DM compared to 8 μg/g DM in birds without weights. More immature birds die from lead poisoning than other factors and significantly more corpses were found between the months of July-October.
Ultra-structure examinations revealed electron dense intra-nuclear inclusions in the cells of proximal convulated tubules of the kidney and X-ray analysis confirmed that these structures consisted of lead.     

Diagnosing the environmental causes of the decline in Grey Partridge Perdix perdix survival in France

We studied Grey Partridge Perdix perdix mortality during breeding to identify the environmental causes of a long‐term decline in adult survival. We radiotagged and monitored daily from mid‐March to mid‐September 1009 females on ten contrasting study sites in 1995‐97. Simultaneously, we recorded habitat features and estimated the abundance of Hen and Marsh Harriers Circus cyaneus and C. aeruginosus Red Fox Vulpes vulpes and mustelids. We experimentally tested whether scavenging could have biased predation rates. We also examined, through the necropsy of 80 carcasses of Grey Partridge, whether disease, parasites or poisoning could have been ultimate causes of high predation rates. The survival rate of radiotagged females during spring and summer ranged from 0.25 to 0.65 across study areas. Mortality peaked in May, June and July when females were laying and incubating. The direct negative impact of farming practices was low (6%). Predation was the main proximate cause of female mortality during breeding (73%) and determined the survival rate, suggesting no compensation by other causes of mortality. Ground carnivores were responsible for 64% of predation cases, and raptors for 29%, but this proportion varied across study sites. Disease and poisoning did not appear to favour predation, and scavenging was not likely to have substantially overestimated predation rates. The predation rate on breeding females was positively correlated with the abundance of Hen and Marsh Harriers, suggesting an additional mortality in areas where harriers were abundant. The proportion of raptor predation was linearly related to harrier abundance. The predation rate was not correlated with the abundance of the Red Fox and mustelids. A potential density‐dependent effect on the predation rate was confounded by the abundance of harriers. We found no convincing relationship between the predation rate and habitat features, but we observed a positive relationship between the abundance of Hen and Marsh Harriers and the mean field size. This suggested that habitat characteristics may contribute to high predation rates through predator abundance or habitat‐dependent predation.     

Incidence of ingested lead gunshot in wild grey partridges (Perdix perdix) from the UK

From 1947 to 1992, successive pathologists at The Game Conservancy Trust carried out 1,318 post-mortems on adult wild grey partridges found dead in the UK. During a study of chick food from 1968 to 1978 on the Sussex Downs, the gizzards of 29 wild chicks aged up to 6 weeks were also examined. This paper reports the incidence of lead gunshot ingestion in these two groups of birds. On the assumption that there is no temporal bias, the incidence of lead poisoning increased from 1947–1958 to 1963–1992. During 1963–1992, the incidence of lead gunshot ingestion was 4.5±1.0% in adults and 6.9±4.7% in chicks. The weights of individual lead shot in the chick gizzards showed a rapid rate of erosion, indicating a short retention time in the gizzard, as also reported for adult waterfowl and game birds. The incidence rates in grey partridge and waterfowl found dead can therefore be compared. From 1963 to 1992, the overall incidence of ingested lead gunshot in the grey partridge in the UK was 52% of that of waterfowl (Anatidae excluding mute swan), significantly lower.     

Body frontal area in passerine birds

Projected body frontal area is used when estimating the parasite drag of bird flight. We investigated the relationship between projected frontal area and body mass among passerine birds, and compared it with an equation based on waterfowl and raptors, which is used as default procedure in a widespread software package for flight performance calculations. The allometric equation based on waterfowl/raptors underestimates the frontal area compared to the passerine equation presented here. Consequently, revising the actual frontal areas of small birds will concomitantly change the values of the parasite drag coefficient. We suggest that the new equation     (m²) where m _B is body mass (kg) should be used when a value of frontal area is needed for passerines.     

Evidence of High Tolerance to Ecologically Relevant Lead Shot Pellet Exposures by an Upland Bird

Upland birds that display grit ingestion behavior are potentially at risk of detrimental effects and death from lead poisoning at trap and skeet ranges and other areas where vast quantities of spent lead shot pellets abound. Because commonly cited force-feeding pellet exposure studies deviate from true field conditions, their results may not reflect true risks faced by upland birds. In particular, studies that use new shot pellets and administer more pellets than would be reasonably ingested, critically interfere with the understanding of actualized pellet exposures. In this study, northern bobwhites (Colinus virginianus), a frequent test species in shot pellet research, were dosed in an ecologically-relevant manner (i.e., with spent shot and with no more than three pellets). Notably, the 56-day post-dosing observation period, during which a battery of physiological measures were recorded, exceeded that of related studies. Despite a sustained suppression of a lead poisoning indicator, the data suggest upland birds can withstand spent shot pellet exposures. Data detected a survivorship ≥95%, absence of illness, demonstrated tolerance for extremely high blood lead concentrations, and unaffected blood parameters. In conjunction with ecological considerations (e.g., spatial scale and animal behavior), concern about bird population losses from the incidental ingestion of spent shot pellets is potentially overstated.     

Embedded lead shot in European starlings Sturnus vulgaris: an underestimated hazard for humans and birds of prey

The poisoning of wild animals by lead (Pb) ammunition fired by hunters has been known for many decades, especially in the case of waterbirds. More recently, it has been demonstrated that raptors are also exposed to the risk of plumbism when feeding on unretrieved quarry that was wounded or killed by hunters. Further studies reveal that even humans can be subject to a significant Pb dose while consuming game animals killed by traditional ammunition. Given the relevance of this issue, several pieces of research have been carried out to assess frequency, dimension, and the number of Pb fragments embedded in the carcasses of ungulates, partridges, ducks, and other birds to evaluate the risk related to the consumption of game meat. In spite of their great importance as quarry species across southern Europe, until now, no data have been available on small passerines. To assess the quantity and type of Pb embedded in songbirds, we x-rayed 196 starlings shot in Italy and found Pb pellets and/or visible fragments in 118 carcasses (60.2 %). We counted 128 shotgun pellets in 85 carcasses. In 28 birds, we detected both whole pellets and lead fragments; in 33, we found only small fragments. By excising and weighing a sample of 20 shotgun pellets (diameter 1.35–1.99 mm), we calculated a Pb load of 3.75 g in the whole sample of 196 starlings, corresponding to an average of 27.32 mg/100 g of body weight. This is a conservative estimation, because fragments were not considered. Compared to game birds of a larger size, the starlings in our study had a lower amount of embedded Pb, but the shot pellets and fragments embedded in their tissues were abundant and tiny. Given the results of previous studies, the quantity and level of fragmentation suggest that the risk of Pb poisoning cannot be ruled out for humans and birds of prey consuming the meat from songbirds killed with traditional ammunition.     

Recreational Shooting of Prairie Dogs: A Portal for Lead Entering Wildlife Food Chains

Abstract: Although lead shot has been banned for waterfowl hunting in North America, some predators continue to exhibit elevated lead burdens, which has been attributed to ingesting metallic lead from other projectiles. Few studies have investigated residual lead fragments in hunted upland animals. Therefore, specific portals for lead entering wildlife food chains remain largely unknown. Prairie dogs (Cynomys spp.) are shot for recreation with minimal regulation in western North America. Because recreational shooters mostly use expanding bullets and rarely remove or bury carcasses, shot prairie dogs could make lead accessible to predators and scavengers. To determine whether and to what degree shot prairie dogs carry lead fragments, we analyzed carcasses shot by recreational shooters with 2 bullet types. Bullet type influenced the probability of bullet fragments being retained in carcasses; 87% of prairie dogs shot with expanding bullets contained bullet fragments, whereas 7% of carcasses shot with non-expanding bullets did. The amount of bullet fragments per carcass also differed between bullet types; carcasses shot with expanding bullets contained a mean of 228.4 mg of the lead-containing bullet core and 74.4 mg of the copper-alloy jacket, whereas carcasses shot with non-expanding bullets averaged only 19.8 mg of the core and 23.2 mg of the jacket. Lead fragments in carcasses shot with expanding bullets were small in size; 73% of all lead mass in each carcass was from fragments that weighed <25 mg each, small enough to be easily ingested and absorbed by secondary consumers. The amount of lead in a single prairie dog carcass shot with an expanding bullet is potentially sufficient to acutely poison scavengers or predators. Therefore, shot prairie dogs may provide an important portal for lead entering wildlife food chains and may pose risks to raptors and carnivores. Managers should consider measures, such as using non-expanding or lead-free ammunition, to reduce the likelihood of lead consumption and poisoning in upland wildlife.     

Interspecific and intraspecific differences in habitat use and their conservation implications for Palaearctic harriers on Sahelian wintering grounds

The floodplains of the West‐African Sahel region have experienced extensive habitat transformation during the past four decades, coinciding with an impoverishment of raptor populations. We investigated foraging patterns of Palaearctic migratory Eurasian Marsh Harriers Circus aeruginosus, Pallid Harriers C. macrourus and Montagu’s Harriers C. pygargus on a floodplain system in northern Cameroon to assess species, sex‐ and age‐related habitat preferences. Sex and age have rarely been incorporated into general studies of raptor habitat associations, despite clear evidence of intrasexual and age‐related differences in foraging strategies and diet composition, potentially carrying strong conservation implications. We found evidence of sexual differences in foraging preference related to land use, particularly in the most sexually dimorphic Pallid Harrier, and evidence that juveniles used different habitats to adults. This constitutes the first quantitative documentation of such differentiation by Palaearctic raptors on African wintering grounds, indicating that general patterns of habitat use in wintering raptors may obscure sex‐ and age‐specific preferences. Contrary to expectations, we found limited evidence for interspecific foraging segregation. Food partitioning by prey mass was related to harrier body mass and facilitated by a diverse availability of prey on human‐transformed floodplains. Anticipated further large‐scale conversion of floodplain habitat into predominantly desiccated grasslands raises concerns about the survival of wintering harriers.     

Food niches of sympatric Marsh Harriers Circus aeruginosas and Hen Harriers C. cyaneus on the Dutch coast in winter

Analysis of pellets collected from adjacent communal winter roosts of Marsh Harriers Circus aeruginosus and Hen Harriers C. cyaneus on an extensive saltmarsh in the southwest Netherlands showed highly significant differences between the diets of the two species. Marsh Harrier diet showed no change throughout January, February and March. They specialized on ducks, which were about half of their prey numerically and more important by weight. Although Marsh Harriers sampled other prey, this remained at a low level and showed no seasonal response to the availability of young lagomorphs. Hen Harriers occupied the niche of a generalist predator, having a broader diet and responding to the presumed changes in availability of prey with diet shifts. In November, about half of their prey items were passerines but these declined in importance in December, and small mammals rose. The proportions of both small mammals and birds fell in February and March, due to increasing dependence on young lagomorphs. Diet overlap between the two species was greatest in January and declined in February and March.     

Food-niche differentiation in sympatric Hen Circus cyaneus and Montagu's Harriers Circus pygargus

Hen Harriers Circus cyaneus and Montagu's Harriers Circus pygargus are medium-sized raptors that differ in size (Hen Harrier being slightly bigger than Montagu's Harrier) and breeding system (Montagu's Harriers are semi-colonial and Hen Harriers defend nesting–hunting territories). In contrast, the diets of the two species when in sympatry are very similar. We evaluated food-niche differentiation among these coexisting raptor species and how between-species differences in body size and social system influence interspecific relationships. We present data from a study conducted in 1997 and 1998 in northeastern Madrid province (central Spain). Diet of the two species largely overlapped (55–95%) during the breeding season, but Hen Harriers preyed more often on larger species. This segregation was observed both in the average size of the primary prey (lagomorphs) and in the alternative prey (birds for Hen Harriers vs. insects for Montagu's Harriers), and was particularly apparent late in the season. Accordingly, feeding frequency of Montagu's Harriers, but not of Hen Harriers, increased later in the season. Size differences between species in prey brought to the nest were apparent for both males and females. Foraging behaviour also differed, as Hen Harriers spent more time hunting close to the nest than did Montagu's Harriers. This implies that segregation in foraging areas may also exist. Observed niche partitioning may relax the potential for competition between these species.     

Feeding behaviour and diet composition of Marsh Harriers Circus aeruginosus in agricultural landscapes

Capsule Diet composition and feeding behaviour of breeding birds differed between areas of high and low agricultural intensification.

Aims To analyze diet composition and feeding behaviour of Marsh Harriers Circus aeruginosus in agricultural landscapes with different degrees of agricultural intensification.

Methods Diet composition and feeding behaviour was assessed by focal observations at nests during breeding seasons in 2001–03 in two agricultural areas within the eastern Ebro Basin (on the northern Iberian Peninsula) which differed in their degree of agricultural intensification: a traditional non-irrigated and non-intensively managed farmland area; and an irrigated and intensively managed farmland area.

Results Marsh Harriers in the intensively managed area took higher percentages of small mammals than harriers in the traditional area managed at low-intensity, where they also had a more diverse diet. Male delivery rates increased throughout the breeding season in the intensively managed area. On the contrary, no significant trend in delivery rates was observed in the traditional area, where harriers turned to larger prey late in the season.

Conclusion Marsh Harriers probably took advantage of different prey types in intensively managed and traditional farmland according to prey availability. Differences in diet composition seem to be related to different foraging strategies adopted by harriers in traditional and intensively managed farmlands. In the traditionally managed farmlands, harriers responded to increases in the energy requirements of the brood over the course of the breeding season by taking larger prey, whereas in the intensively managed farmlands harriers increased feeding rates.     

Comparative breeding ecology and hybridization of Eastern and Western Marsh Harriers Circus spilonotus and C. aeruginosusin the Baikal region of Eastern Siberia

New information on the breeding ecology and inter-breeding of Western Circus aeruginosus and Eastern C. spilonotus Marsh Harriers in the Baikal region of Eastern Siberia is presented. Hybridization is relatively common (one of the parents was not 'pure' C. spilonotus in six out of 28 nesting cases) in the Irkutsk area, where nests of a mixed pair were found with chicks in 1999 and 2000. Eastern Marsh Harriers are more similar to Western in size, biology and coloration of young birds, but to the Australasian C. approximans in their displays and mating system, and intermediate between C. aeruginosus and C. approximans in the plumage coloration of females. The systematic status (species' or 'subspecies') of the Western and Eastern Marsh Harriers depends on the systematic approach taken, and existing data seem to be inadequate to resolve this. The Siberian Mongolian zone of contact of these marsh harriers is unique as other marsh harriers of the world are allopatric. More research on ecology, behaviour and molecular systematics is necessary to resolve the situation.