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ACUTE POISONING OF RED KITES (MILVUS MILVUS) IN FRANCE:

DATA FROM THE SAGIR NETWORK

Philippe Berny1,4 and Jean-Roch Gaillet2,3

1 Toxicology Laboratory, Ecole Nationale Vétérinaire de Lyon, 1, av Bourgelat, F-69280 Marcy l’étoile, France2 Office National de la Chasse et de la Faune Sauvage, Unité de Suivi Sanitaire de la Faune, St Benoist, F-78120Auffargis, France3 Current address: DSV de Paris 20-32, rue de Bellevue, 75019 Paris, France4 Corresponding author (email: [email protected])

ABSTRACT: Red Kites (Milvus milvus) are avian scavengers limited to Europe, and they currentlyare listed as an endangered species worldwide. Accidental poisoning is often listed as one of thethreats to Red Kites throughout their range of distribution. The purpose of this article is toinvestigate the suspected poisoning cases reported to the French Wildlife Disease SurveillanceSystem. Dead animals are submitted to a local veterinary laboratory for necropsy and whenpoisoning is suspected, samples are submitted to the Toxicology Laboratory of the College ofVeterinary Medicine, Lyon, France. Over the period 1992–2002, 62 Red Kites suspected ofpoisoning were submitted, and poisoning was the confirmed cause of death for greater than 80% ofthese cases. The major toxicants found were cholinesterase inhibitors (carbamates andorganophosphate insecticides) and anticoagulant compounds. The circumstances of exposureinclude secondary poisoning after the use of anticoagulants over vast areas to control water vole(Arvicola terrestric) populations, but they also include malicious poisoning with carbamates(aldicarb and cabofuran) in meat baits. Cases of poisoning vary throughout France, with observedmortality rates ranging between 0.1/100 hundred breeding pairs/10 yr and four cases/100 hundredbreeding pairs/10 yr. Additional cases of poisoning likely go undetected, and our results suggestthat acute poisoning is not uncommon in Red Kites and that it should be considered in the currentrestoration plans.

Key words: Acute poisoning, anticoagulant, carbamate, Milvus milvus, secondary poisoning.

INTRODUCTION

The Red Kite (Milvus milvus) popula-tion in France has been considered stableto slightly declining (Sériot, 2005). Thegeographic distribution of Red Kites islimited to Europe, and the species is listedunder the Red List of the InternationalUnion for the Conservation of Nature asan endangered species, Annex II of theBern convention, and listed as a Species ofEuropean Conservation Concern (http://milan-royal.lpo.fr; Sériot, 2005). Red Kitesare scavengers; thus, they are highlysusceptible to the risk of poisoning, eitherby secondary exposure (e.g., ingestion ofcontaminated prey) or by pesticides ap-plied on meat baits (Berny et al., 1998).Among the causes of decline, habitatmodification is considered as the mostimportant factor. Elevated mortality ratesdue to human impacts are also consideredas threatening for this species, and the

conservation program for this species isspecifically focused on identifying poison-ing cases and toxicants involved (Sériot etal., 2004; Sériot, 2005).

The Toxicology Laboratory of the Col-lege of Veterinary Medicine (Lyon, France)is a member of the Wildlife DiseaseSurveillance System (SAGIR network) inFrance. Tissue samples are received dailyfor toxicologic analyses as part of theroutine diagnostic investigations of suspect-ed poisoning events. In the literature, manypapers deal with poisoning in birds of prey,especially with insecticides (Elliot et al.,1996; Fleischli et al., 2004; Wobeser et al.,2004). The main objectives of this paperwere to present data collected over 10 yr atthe Toxicology Laboratory on all toxicantsin Red Kites and to discuss the activeingredients involved, the circumstances ofexposure, and the importance of acutepoisoning in mortality rates in this uniqueEuropean species.

Journal of Wildlife Diseases, 44(2), 2008, pp. 417–426# Wildlife Disease Association 2008

417

MATERIALS AND METHODS

The animals included in this study werecollected by technicians from Office Nationalde la Chasse et de la Faune Sauvage (ONCFS-National Hunting and Wildlife Office) and thelocal hunting federations. The SAGIR net-work is supervised by the Office National de laChasse et de la Faune Sauvage. Hunters,technicians of the ONCFS, and the localhunting federations are responsible for thecollection of wild animals found dead andtheir submission to the local veterinarydiagnostic laboratory. As described previously(Berny et al., 1998), the network is active in allparts of France; therefore, it has a nation-widescope.

All wild animals collected within the SAGIRnetwork are necropsied by trained veterinar-ians at the local veterinary laboratory, withbacteriologic, histologic, or parasitologic ex-aminations performed as deemed necessary.Whenever acute poisoning is suspected (e.g.,sudden death of several birds, good bodycondition, recent use of pesticides in the area,presence of baits), biologic samples (e.g.,gizzard content and liver) of the dead animalsand their corresponding necropsy findings aresubmitted to the Toxicology Laboratory at theVeterinary College (Lyon, France). Eachanimal is assigned a unique identificationnumber and accompanied by a specific case-record describing the circumstances of discov-ery, and any available demographic andclinical data.

At the Toxicology Laboratory, samples areanalyzed according to internal procedures,published or official techniques for theanalysis of residues in animal tissues, or acombination (Table 1). The Toxicology Labo-ratory has developed a comprehensive ap-proach to investigate these cases (e.g., selec-tion of animal tissues, screening techniques,clinical and circumstantial evidence of expo-sure; Brown et al., 2005). However, analysesare paid for by the local hunting federations;thus, funding is usually limited to investiga-tions of wildlife poisoning incidents. Screen-ing for poisons can include insecticides (e.g.,organophosphates and carbamates, organo-chlorines, pyrethroids, imidacloprid, and fi-pronil), rodenticides, and other vertebratepoisons (e.g., anticoagulants or antivitamins K[AVKs], chloralose, crimidine, and strych-nine), molluscicides (e.g., metaldehyde andmethiocarb), herbicides (e.g., paraquat anddiquat), avicides (e.g., chloralose), and specif-ic drugs (e.g., euthanasia agents) as describedby Brown et al. (2005). Heavy metals also maybe analyzed in samples but only when clinical

evidence, exposure evidence, or both suggestthe need. The laboratory has set up a qualityassurance/quality control policy, and analyti-cal investigations include the analysis ofblanks, spiked samples, or both and calibra-tion curves. Poisoning is confirmed when theexposure information (e.g., pesticide applica-tion and baiting), clinical and necropsyfindings, and the presence and amount of agiven poison are consistent for a poisoningevent.

The information for each case submitted tothe laboratory is entered into a database forfuture reference. The laboratory database wassearched for Red Kites and Black Kites(Milvus migrans) suspected poisoning casesover the period 1992–2002 to retrieve infor-mation on the time of discovery, poisonsuspected, analytical investigations, clinicalsigns, lesions observed, or a combination.Results obtained in Red Kites were comparedwith results obtained in all wildlife species(e.g., nature of toxicant involved, circumstanc-es of poisoning, period of exposure).

Population estimates of Red Kites wereprovided by the Ligue de Protection desOiseaux (LPO-French representative of BirdLife International). Briefly, Red Kites aresurveyed by visual observation and identifica-tion of nests along road transects. A specificprotocol for bird watching has been set up,and it is available at http://milan-royal.lpo.fr/.Red Kites have been recently included in aEuropean conservation project, and annualpopulation estimates are available. Winteringpopulations are described in France, althoughto a limited extent (http://milan-royal.lpo.fr/),in most of the nesting areas, especially in thesouth of France or the Massif Central (centerof France). In our analysis of cases, it is notpossible to distinguish between wintering andnesting populations.

Anticoagulant use against water voles in thefield was computed based on the datapublished by the regional crop protectionservices in the two major regions of use inFrance (srpv; www.srpv-auvergne.com).Whenever possible, statistical tests were con-ducted. For case distributions (e.g., monthlyrepartition and proportion of various toxi-cants), chi-square tests were used, with a levelof significance P,0.05.

RESULTS

Over the study period, 4,323 suspectedpoisoning cases of wildlife were investi-gated at the toxicology laboratory. Amongthem, Eurasian Buzzards (Buteo buteo)

418 JOURNAL OF WILDLIFE DISEASES, VOL. 44, NO. 2, APRIL 2008

were the most common birds of preyreceived (314 cases). Red Kites (62 cases)were the second major bird of prey,followed by Black Kites (40 cases).

There is no statistical difference be-tween monthly distribution of Red Kitecases and other wildlife cases (chi-squaretest, P50.21, df523). Most cases weresubmitted during autumn and spring, witha limited number of cases submittedduring summer (Fig. 1). The proportionof confirmed poisoning cases was signifi-cantly higher in Red Kites (82%) com-pared with other wildlife species (54%)(binomial test, P,0.01). The number ofconfirmed Red Kite poisoning cases forgroups of pesticides is given in Figure 2;most cases were associated with AVK andinsecticide poisoning. Among AVKs (27confirmed cases), bromadiolone (0.2–5.6 mg/g wet weight) was detected in 24cases and chlorophacinone (0.9–5.2 mg/gwet weight) in three cases. Among cholin-esterase inhibitors (21 confirmed cases),

carbofuran was detected in 14 cases,mevinphos in five cases, and aldicarb intwo cases. The other products detectedwere a-chloralose (four cases), imidaclo-prid (one case), lindane (one case), andlead (one case). There was no evidence ofpoisoning with herbicides, drugs for eutha-nasia, or any other pesticide.

Geographic distribution of poisoningcases and of Red Kites is depicted inFigure 3. There were a few individualcases reported from neighboring areasoutside of the known distribution of RedKite populations (Fig. 3b). Mortality ratesbased on population data (Fig. 3b) andidentified poisoning cases vary between0.1/100 hundred breeding pairs/10 yr tofour cases/100 hundred breeding pairs/10 yr. No statistical comparison betweenareas could be conducted due to thelimited number of cases. There is evi-dence, from both maps, that AVKs arewidely used in some areas (Fig. 3a), withsome differences: scattered use in central

TABLE 1. Analytical techniques used for toxicology screening at the College of Veterinary MedicineToxicology Laboratory (and published references).

Group Compound Detectiona Confirmation Referenceb LOD (mg/g or mg/l)c

Anticoagulant 8 HPTLC-UV HPLC-UV/Fluo

Berny et al.(1995, 2006)

0.05 (L)0.01 (Pl)

Carbamate/ 5 compounds HPTLC-UV HPLC-UV Berny et al. (1999) 1 (GC, L)Organophosphate 15 compounds HPTLC-UV GC-MS AFSSA 0.001 (GC, L)Organochlorine 12 compounds GC-ECD GC-MS AFSSA 0.0001 (GC, L)Pyrethroid 5 GC-ECD GC-MS AFSSA 0.001 (GC, L)Fipronil HPLC-UV GC-MS Jennings et al. (2002) 0.01Convulsant Strychnine

CrimidineHPTLC-UV GC-MS Braselton and

Johnson (2003)0.1 (GC)

Molluscicide Metaldehyde Colorimetric GC-MS 1 (GC)Herbicide Paraquat UV HPLC-UV Blake et al. (2002) 0.1 (GC, K)Euthanasia Pentobarbital

T61HGC-MS Hooijerink et al. (1998) 0.1 (Pl)

Avicide a-Chloralose Colorimetric GC-ECD Brown (1996, 2005) 1 (GC)Heavy metal Pb, Cd, Cu AAS AFSSA 0.001 (L, K)

Hg Cold vapor 0.005 (Pl)As AAS AFSSA (L, K)

(GC, L, K)

a AAS 5 atomic absorption spectrometry; ECD 5 electron capture detection; Fluo 5 fluorescence detection; GC 5 gaschromatography; HPLC 5 high-performance liquid chromatography; HPTLC 5 high-performance-thin layerchromatography; MS 5 mass spectrometry; UV 5 ultraviolet.

b AFSSA 5 official method developed by the French Agency for Food Safety.c LOD 5 limit of detection; L 5 liver; Pl 5 plasma; Bl 5 blood; GC 5 gizzard content; K 5 kidney.

BERNY AND GAILLET—POISONING IN RED KITES IN FRANCE 419

France and continuous use in easternFrance. Most AVK poisoning cases occurin the eastern France (Fig. 3b), althoughthe local population of Red Kites is lower.

DISCUSSION

The number of wildlife cases submittedto the Toxicology Laboratory is substantial

FIGURE 1. Monthly distribution of suspected poisoning cases in Red Kites (Milvus milvus) and in wildlife(less red kites) in general between 1992 and 2002 in France.

FIGURE 2. Toxic compounds detected in Red Kites (Milvus milvus, n562) and in wildlife (less Red Kites,n54,326) in general (number of cases) between 1992 and 2002 in France (n 5 number of cases submitted).


FIGURE 3. Geographical distribution of (a) major areas (green areas) treated with bromadiolone againstfield voles (Arvicola terrestris) and (b) Red Kite (Milvus milvus) population and poisoning cases between 1992and 2002 in France. Population data were obtained from Ligue de Protection des Oiseaux (French section ofBirdlife International) (www.milan-royal.lpo.fr).


(400–450/yr), and it provides a reasonabledatabase on poisoning cases in wildmammals and birds. As stated previously(Berny et al., 1998), the French networkrelies primarily on hunters for casesubmission, and analyses are paid for byhunting associations; thus, most speciessubmitted for investigation are gamespecies. As a comparison, in the WildlifeIncident Investigation Scheme (WIIS)reports in the United Kingdom, birds ofprey are very commonly sent to the lab forinvestigation (WIIS, 2003; www.defra.gov.uk), with an average of 20–22 Red Kites/yr(versus six in France); there are approxi-mately 370–380 breeding pairs in GreatBritain, which is approximately 10 timesless than reported in France in 2000(Sériot, 2005; http://milan-royal.lpo.fr/).In the UK, the system does not rely onprivate funding; thus, there is an obviousbias in case collection in France. Never-theless, the case-series described in thisarticle provides some valuable data on anendangered species for which there areonly a few published toxicologic investiga-tions. The majority of cases occur duringearly spring and autumn; therefore, win-tering kites may be exposed as well. It ispossible that in early spring, snow coverlimits food in the areas where Red Kitesare found. Considering the importance ofAVK poisoning, the monthly distributionof poisoning cases is also driven by the useof bromadiolone against Arvicola terrestrisat that time of the year, especially inautumn and early spring (Berny et al.,1997).

Investigation of suspected poisoningcases in wildlife may be complex andtime-consuming. The strategy developedby the WIIS in the UK, for example, isbased on necropsy, with a wide multi-residue chemical analysis (Brown et al.,1996, 2005). Although this approach mayyield many interesting results, it is expen-sive and time-consuming. In the Frenchsystem, necropsy is performed locally tobe conducted as soon as possible aftercollection, and appropriate samples may

be kept frozen and submitted to thetoxicology laboratory for chemical investi-gations. Clinical (when possible) andnecropsy findings may suggest a specificpesticide poisoning. As stated by Fair-brother (1996), acute exposure to carba-mate/organophosphate pesticides is usual-ly suggested by the discovery of deadanimals in good condition (e.g., adequatebody mass and fat), with signs of convul-sions (e.g., tightened claws), pulmonaryedema, and diarrhea. Because of the delaybetween body collection, necropsy andsubmission to the toxicology laboratory,investigation of acetylcholinesterase inhi-bition is no longer considered, although itis commonly used in other case series(Eliott et al., 1996; Wobeser et al., 2004).Spontaneous reversal, as commonly de-scribed with carbamates, and lack ofinhibition in the brain in case of suddendeath (Wobeser et al., 2004) are alsopitfalls of the cholinesterase inhibitionmethod, resulting in a high proportion offalse negative cases: these authors foundfour negative cases out of seven withconfirmed exposure (carbouran identifiedin the gizzard). For example, Guitart et al.(1999) describe a case of death withaldicarb, in which the bait was found inthe esophagus only, confirming the hightoxicity and rapid onset of signs. There-fore, identification of suspected poisoningcases relies on chromatographic determi-nation of carbamates and organophos-phates as described above, with cholines-terase inhibition on a thin layerchromatography plate to confirm theactivity of the compound identified (Bernyet al., 1999).

Poisoning by AVKs is also easily sug-gested by severe hemorrhagic lesions andlack of clotting. Because the network isonly dealing with spontaneous submissionof dead animals, the number of poisoningcases should not be compared withprevalence or incidence of poisoning.The high proportion of confirmed poison-ing among the suspected cases indicatesthat the selection process is relevant and


effective; toxicants not detected in thecases submitted to the Toxicology Labo-ratory represent less than 20% of thesubmitted cases. To have a reasonableidea of the importance of poisoning amongthe various causes of death, systematicinvestigations should be conducted in birdpopulations, as reported by Wendell et al.(2002) for raptors admitted at the Color-ado State Veterinary Teaching Hospital.Wendell et al. (2002) identified toxicosis asthe primary cause of death in about 2% ofthe birds, which is fairly consistent withdata published by the SAGIR networkregarding game species (Lamarque et al.,1999). In White-tailed Sea Eagles (Ha-liaeetus alvicilla) in Greenland, one case oflead poisoning was identified among 12reported deaths (Krone et al., 2004).Considering the limited number of birdsincluded in this series, the proportion ofpoisoning cases (8%) may not be signifi-cant.

Among the toxicants found in Red Kitesin this study, cholinesterase inhibitors (21cases) and anticoagulant rodenticides (27cases) were predominant, findings thatcorresponded to a previous survey in birdsof prey (Berny et al., 1998). Both toxicantgroups are reported as major toxicants inbirds of prey, although seldom in the samestudy. For example, Fleischli et al. (2004)reported investigations of 355 anticholin-esterase poisoning cases from more than35,000 wildlife deaths in the UnitedStates, with fanfur and carbofuran asprimary toxicants. In New York, Stone etal. (2003) reported only on anticoagulantpoisoning in raptors. In the UK, WIIS(2003) reports indicate that insecticidesare commonly detected in raptors, withcarbofuran, mevinphos, and aldicarb asthe most common compounds. In France,we found a similar pattern for toxicants,which may reflect the European homolo-gations of pesticides. These insecticidesare highly toxic to birds of prey (toxicdoses ,10 mg/kg), and they are availableas concentrated formulations. Indeed,they are available as micropellets for soil

treatment at 5% or 10% active ingredient,or as a liquid concentrate (mevinphos)(ACTA, 2005). Despite strict regulationson the sale and use of such pesticides, theycan be easily purchased. There is evidencethat most cases reported in this article areillicit poisoning cases (Berny et al., 1998),as often reported elsewhere in the world(Elliott et al., 1996; Wobeser et al., 2004),and even in Red Kites in Spain (Sergio etal., 2005). Reports from European surveyson pesticide incidents in wildlife alsodescribe deliberate abuse as the majorcause of pesticide poisoning in mostspecies (de Snoo et al., 1999; Van Oerset al., 2005). Birds of prey, especiallyscavengers, suffer from a bad reputation,and they are often incorrectly associatedwith negative events in game speciespopulations. As described by Villafuerteet al. (1998), major population decreasesdue to infectious diseases (in hares in theirstudy) may be falsely attributed to preda-tion by Red Kites; this may result in illicithunting and poisoning of birds of prey.Because these raptors are scavengers, theyare easily poisoned by meat baits contain-ing insecticides, and because carbamatesand organophosphates may be highlypersistent in the environment, poisoningwith baits may be possible over severaldays (Wilson et al., 2002). As suggested bySergio et al. (2005), predators and scav-engers are often poisoned by huntersbecause they are considered to be com-petitors. Population management strate-gies should also include, as they suggest,information and implication of inhabitantsand hunters to understand the benefits ofscavengers.

Anticoagulant poisoning is also com-monly described in birds of prey, as aresult of secondary poisoning, but mostlyin nocturnal birds such as owls (Newton etal., 1990, 1999). This is especially true forsecond-generation products, such as bro-difacoum or bromadiolone (Eason et al.,2002; Erickson and Urban, 2002). Usually,animals poisoned by AVKs die several daysafter exposure; thus, studies relying on


animal carcasses may be biased andunderestimate the true proportion ofdeath due to AVKs poisoning (Newton etal., 1990, 1999; Erickson and Urban, 2002;Shore et al., 2003). In France, bromadio-lone is widely used against field voles(Arvicola terrestris), coypu (Myocastorcoypu) and musk rat (Ondathra zibethi-cus). There is evidence that the use ofbromadiolone is associated with exposureor poisoning of predators and scavengersin the same environment (Berny et al.,1997; Fournier-Chambrillon et al., 2004).Shore et al. (2003) also showed that manymustelids found dead had detectableresidues of anticoagulants, although deathcould be attributed to another cause.

In this study, we observed an associa-tion between AVK poisoning and its use.For example, bromadiolone is applied onmany scattered areas in the center ofFrance, but over a vast, contiguous area ineastern France. As a result, bromadiolonepoisoning of Red Kites in eastern Franceis much more pronounced. It has alsobeen shown recently (Giraudoux et al.,2006) that field voles store wheat bait andthat they may consume it several days orweeks after use; hence the proportion ofvoles caught with high residues of broma-diolone is almost 100% for over 10 daysafter field application, thereby exposingRed Kites for prolonged periods. Thesedata indicate that there is some concernabout the widespread use of AVKs andtheir potential side effects on nontargetspecies. For an endangered species, this iseven more of a concern. Our data suggestthat if AVKs have to be used, they shouldbe applied on small dispersed areas toavoid contamination of an entire popula-tion of voles and consequently, repeatedpoisoning of scavengers feeding on poi-soned rodents.

The other toxicants we measured ac-count for only a few percent of thepoisoning cases. Only a-chloralose result-ed in several poisoning cases, but muchless than reported in the UK (WIIS, 2003).a-Chloralose is commonly used in France

as a bird control product (ACTA, 2005).Its toxicity is important in many birdspecies, but it is not labeled for use againstbirds of prey. Because it is only sold as acereal-based bait, exposure of birds ofprey should not occur often (ACTA, 2005).There is no evidence that this compoundaccumulates in the food chain (Brown etal., 1996). Secondary poisoning may occurwhen scavengers eat rodents or birdskilled by chloralose poisoning, by directingestion of the gizzard content. It is ourhypothesis that illicit meat baits were alsoprepared with this product and ingestedby Red Kites. There was also one case ofacute exposure to imidacloprid. This is, toour knowledge, the first report of exposureof a bird of prey to this insecticide. We donot have any information on the toxicity ofimidacloprid in birds of prey, and, in otherbird species, it may vary greatly with acuteoral lethal dose 50 from 14.5 mg/kg to152 mg/kg (www.inra.fr/agritox).

In the cases investigated, there was noheavy metal poisoning case reported,although heavy metals are commonlysuggested as potentially toxic to Red Kites,especially due to the consumption ofbullet fragments in prey (Mateo et al.,2003). As stated herein, the policy is toinvestigate the cause of death and not todetermine whether the birds were ex-posed to a given toxicant. Based onnecropsy findings, lead poisoning, forexample, is not often suspected, and heavymetal residues are not determined sys-tematically because of limited funding.

In conclusion, it seems that poisoning isa common feature in Red Kites, with twomajor groups of compounds involved:cholinesterase inhibitors and anticoagu-lant rodenticides. It is difficult to deter-mine the impact of poisoning on thepopulation. Based on our data, mortalitydue to acute poisoning may reach a fewindividuals per thousand, but we suspectthis number is underestimated. Acutepoisoning remains a potential threat on aweakened population, especially whenAVKs are used on large areas or as a


result of illicit poisoning. It would certain-ly be extremely valuable to develop aspecific monitoring system for this endan-gered species, because it is already under-going a restoration program in France.

ACKNOWLEDGMENTS

We thank J. Sinardet and D. Vey for excellenttechnical assistance in the laboratory; ONCFSand Hunting federations, who provided fund-ing for the analyses reported here; and Ligue deProtection des Oiseaux (French representativeof Birdlife International) (Mionnet), who pro-vided the data on Red Kite population statusover the study period.

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Received for publication 31 July 2006.


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