Volume116,2014,pp.408–428 DOI:10.1650/CONDOR-14-36.1 REVIEW The persistent problem of lead poisoning in birds from ammunition and fishing tackle Susan M. Haig,1* Jesse D’Elia,2 Collin Eagles-Smith,1 Jeanne M. Fair,3 Jennifer Gervais,4 Garth Herring,1 James W. Rivers,5 and John H. Schulz6 1 U.S.GeologicalSurvey, Forest andRangeland Ecosystem Science Center,Corvallis, Oregon, USA 2 U.S.Fishand WildlifeService, Portland, Oregon, USA 3 LosAlamos National Laboratory, Environmental Stewardship, Los Alamos, NewMexico,USA 4 OregonWildlifeInstituteand Department ofFisheriesand Wildlife,OregonState University, Corvallis, Oregon, USA 5 Department ofForest Ecosystemsand Society,Oregon StateUniversity, Corvallis, Oregon, USA 6 Department ofFisheriesand WildlifeSciences, University ofMissouri, Columbia,Missouri, USA * Correspondingauthor: [email protected] SubmittedFebruary28,2014;AcceptedApril21,2014;PublishedJuly9,2014 ABSTRACT Lead (Pb) is a metabolic poison that can negatively influence biological processes, leading to illness and mortality acrossalargespectrumofNorthAmericanavifauna(.120species)andotherorganisms.Pbpoisoningcanresultfrom numeroussources,includingingestionofbulletfragmentsandshotpelletsleftinanimalcarcasses,spentammunition leftinthefield,lostfishingtackle,Pb-basedpaints,large-scalemining,andPbsmeltingactivities.AlthoughPbshothas beenbannedforwaterfowlhuntingintheUnitedStates(since1991)andCanada(since1999),Pbexposureremainsa problem for many avian species. Despite a large body of scientific literature on exposure to Pb and its toxicological effects on birds, controversy still exists regarding its impacts at a population level. We explore these issues and highlightareasinneedofinvestigation:(1)variationinsensitivitytoPbexposureamongbirdspecies;(2)spatialextent andsourcesofPbcontaminationinhabitatsinrelationtobirdexposureinthosesamelocations;and(3)interactions between avian Pb exposure and other landscape-level stressors that synergistically affect bird demography. We explore multiple paths taken to reduce Pb exposure in birds that (1) recognize common ground among a range of affected interests; (2) have been applied at local to national scales; and (3) engage governmental agencies, interest groups,andprofessionalsocietiestocommunicatetheimpactsofPbammunitionandfishingtackle,andtodescribe approachesforreducingtheiravailabilitytobirds.Astheyhaveinprevioustimes,usersoffishandwildlifewillplaya key role in resolving the Pb poisoning issue. Keywords: birds, copper bullets, endangered species, fishing jigs, fishing sinkers, fishing tackle, lead, lead ammunition, lead poisoning Problema persistente de envenenamiento por plomo en aves debido a municiones y aparejos de pesca RESUMEN El plomo (Pb) es un veneno metabo´lico que puede influenciar negativamente los procesos biolo´gicos produciendo enfermedadesylamuertedeungranespectrodeavesdeAme´ricadelNorte(.120especies)ydeotrosorganismos.El envenenamiento por Pb puede provenir de mu´ltiples fuentes, incluyendo la ingestio´n de fragmentos de balas y perdigonesquequedanenloscada´veresdelosanimales,municionesusadasydejadasenelcampo,aparejosdepesca abandonados, pinturas a base de Pb, miner´ıa a gran escala y actividades de fundicio´n de Pb. Los disparos que contienen Pb han sido prohibidos para la caza de aves acua´ticas en Estados Unidos (desde 1991) y Canada´ (desde 1999). Sin embrago, laexposicio´n no intencional de muchas aves alPb continua. A pesar de que existe una enorme cantidad de literatura cient´ıfica sobre la exposicio´n y los efectos toxicolo´gicos del Pb en las aves, existe au´n controversia sobre losimpactos a nivel poblacional.Evaluamos estosaspectos ysubrayamos lasa´reasque necesitan investigacio´n:(1)variacio´nenlasensibilidadalaexposicio´nalPbentrelasespeciesdeaves;(2)extensio´nespacialy fuentesdecontaminacio´ndePbenlosha´bitatsenrelacio´nconlaexposicio´ndelasavesenesasmismaslocalidades;e (3)interaccionesentrelaexposicio´ndelasavesalPbyotrasfuentesdeestre´saescaladepaisajequeafectandemodo sine´rgicolademograf´ıadelasaves.Exploramosmu´ltiplesiniciativasqueapuntanalareduccio´ndelaexposicio´ndelas avesalPbque:(1)reconocenaspectoscomunesenunrangodeinteresesafectados;(2)hansidoaplicadasalaescala local y nacional; e (3) involucran agencias de gobierno, grupos de intere´s y sociedades de profesionales para comunicarlosimpactosdelasmunicionesdePbydelosaparejosdepescayparadescribirlosenfoquesparareducir sudisponibilidadparalasaves.Comohaocurridoenotrasocasiones,losusuariosconsuntivosdelospecesydelavida silvestre jugara´n un rol muy importante para resolver el tema del envenenamiento por Pb. Q2014CooperOrnithologicalSociety.ISSN0004-8038,electronicISSN1938-5129 DirectallrequeststoreproducejournalcontenttotheCentralOrnithologyPublicationOfficeataoucospubs@gmail.com S.M. Haig,J.D’Elia, C.Eagles-Smith, etal. Leadpoisoning inbirds 409 Palabras clave: aparejo de pesca, aves, balas de cobre, envenenamiento por plomo, especies en peligro, municio´n de plomo, plantillas de pesca, plomadas de pesca, plomo INTRODUCTION health, as evidenced by OSHA regulations protecting workersatshootingranges(e.g.,https://www.osha.gov/pls/ Lead (Pb) has long been recognized as an ecological and oshaweb/owadisp.show_document?p_table¼NEWS_ human health hazard becauseexposure to this cumulative RELEASES&p_id¼22524).These concerns are particularly metabolic poison has negative consequences for all applicable to birds because their mobility and diverse organisms studied (DeMichele 1984, Scheuhammer and foraging strategies contribute to potential exposure and Norris 1995, Hernberg 2000, Goddard et al. 2008,Watson subsequent toxicological impairment in a broad array of etal.2009,Centers forDisease Control 2013,Chen2013). species. Although Pb occurs naturally as a trace element of Birds are sensitive to Pb exposure, leading to apparent geological materials (Figure 1), human activities have sublethal or lethal toxic responses, and exposure has been greatly increased the distribution and abundance of Pb in documented in .120 species (reviewed by Scheuhammer the environment because it is used widely in the and Norris 1995, Fisher et al. 2006, Goddard et al. 2008, production of batteries, pigments and dyes, caulks, and Pain et al. 2009, Tranel and Kimmel 2009; Figure 2). metal alloys, as well as in aviation fuel for small piston- However, the extent of the problem is difficult to quantify engine aircraft (Rattner et al. 2008, Carr et al. 2011). The because the rapid onset of toxicity results in low physical properties of Pb (e.g., high density, low melting detectability in species that are not intensively monitored point, malleability, corrosion resistance), as well as its low and tested. Thus, the magnitude of the issue and the cost compared with alternative metals, have made it the breadthofitsconservationandhealthimplicationsremain primary metal used in the manufacturing of ammunition controversial (Bellinger et al. 2013). and fishing sinkers (Goddard et al. 2008,Thomas 2013). This review was initiated to summarize scientific Although wildlife exposure to Pb has been linked to a information pertaining to the conservation threat of Pb variety of anthropogenic sources, such as mining (Blus et ammunition and fishing tackle in birds. Our goal is to al. 1999, Henny 2003) and legacy Pb-based paint point out the broad spectrum of options that are available (Finkelstein et al. 2003), a great deal of attention is to decision-makers seeking to reduce Pb poisoning in currently focused on Pb ammunition and fishing tackle birds.These approaches are not mutually exclusive, and it because of their widespread recreational and subsistence is likely that the combination of several would most use in wildlife habitats (Rattner et al. 2008, Goddard et al. effectively reduce or eliminate Pb exposure in birds from 2008). Pb ammunition can also be a threat to human ammunition and fishing tackle. For example, in order to FIGURE1.SpatialdistributionofsoilPbconcentrations(ppmdryweight)acrossthecontinentalUnitedStates.Thesebackground levelsrangefrom50to400ppm;soilconcentrationsthatexceed~100ppmareconsideredelevated.Pblevelsinsoilnearmines, smelters, and similar sites can range upward of 12,000 ppm. Data were obtained from the USGS National Geochemical Survey database (http://mrdata.usgs.gov/geochem/). Spatial interpolation of Pb concentrations was conducted in ArcMap 10.0, based on data density ofonesample per289 km2. TheCondor:OrnithologicalApplications116:408–428,Q2014CooperOrnithologicalSociety 410 Lead poisoning inbirds S.M. Haig,J.D’Elia, C.Eagles-Smith, et al. properly address particular situations, decision-makers may need to know factors such as (1) population effects across the continuum of potentially affected species; (2) identificationofspeciesdirectlyandindirectlyaffected;(3) the degree to which other sources of Pb in the environment may be contributing to poisoning; and (4) the potential impact on human health. WebeginbyevaluatingthephysiologicaleffectsofPbin birds and critically examining the evidence of avian injury and mortality from spent ammunition and fishing tackle. We then review regulatory and voluntary approaches to reduce avian exposure to Pb and outline future directions thatcouldminimizethemagnitudeofPbimpactsonavian populations.Althoughweacknowledgethatthisisaglobal issue and cite examples from around the world (Mateo 2009, Newth et al. 2012, United Nations Environment Programme 2013), our review is primarily focused on North American birds. Pb in the Environment and Its Significance for Avian Conservation The anthropogenic Pb cycle. Pb is widely distributed across the atmosphere, lithosphere, hydrosphere, and biosphere (Figure 1). Beginning in Roman times, ~95% of Pb in the environment resulted from human activities, including mining, smelting, coal combustion, battery processing, waste incineration, and fuel additives (Alfonso et al. 2001, Goddard et al. 2008). Modeled loss estimates fromprimaryPbemissionvectorssuggestthat~48%ofall Pb newly brought into use is ultimately lost to the FIGURE 2. Black-billed Magpies (Pica hudsonia) feed on mule environment (Mao et al. 2009). The second-largest loss, deer (Odocoileus hemionus columbianus) shot near Penticton, BritishColumbia,Canada.PhotocourtesyofLaureWilsonNeish. accounting for 21% (670,000 metric tons Pb yr(cid:2)1) of the annualenvironmentalPbdeficit,isPbdissipatedfollowing use(Mao etal.2009). IntheUnitedStatesalone, .69,000 that is actually used; (2) the proportion of use that occurs metric tons of Pb were used in the production of in outdoor environments where birds can be exposed; (3) ammunitionin1yr(U.S.GeologicalSurvey2013).Among the proportion of ammunition and fishing tackle used in the initial 15 countries of the European Union, ~34,600 outdoor environments that is left in such a form or metric tons of Pb shot and ~4,000 metric tons of Pb location that avian exposure is possible (i.e. bullet bullets and pellets are used per year (European Commis- fragments left in carcasses); and (4) the probability that a sion 2004). Annual estimates of Pb fishing weights sold birdwillbeexposedtoanyavailablePb-basedammunition amount to 3,977 metric tons in the United States, up to or fishing tackle (Figure 3). Although ample evidence 559metrictonsinCanada,and2,000–6,000metrictonsin shows considerable avian Pb exposure from ammunition Europe (Scheuhammer et al. 2003, European Commission and fishing tackle, we need to address these data gaps to 2004, United Nations Environment Programme 2011). generate ecosystem- or regional-scale estimates of poten- Radomski et al. (2006) estimated 16 tons of Pb tackle in 5 tialavianPbexposure.Adistinctunderstandingofprimary surveyed lakes over a 20-yr period, or an average ~320 exposure pathways is important for managing scenarios pounds Pb lake(cid:2)1 yr(cid:2)1. where avian risk to Pb exposure is high. Although these estimates provide context for the raw Pathways of avian exposure. Among toxicologically distributionofPbintoammunitionandfishingtackle,itis significant sources (e.g., Pb-based paint, mining, smelters, importanttonotethattheyareclearlyunrepresentativeof and combustion residue of leaded gasoline; Blus et al. theamountofPbthatisdistributedandavailableforavian 1999, Church et al. 2006, Beyer et al. 2013), spent exposure (Figure 1). To appropriately estimate potential ammunition and lost fishing tackle are the primary exposurecoefficients,dataareneededthatquantify(1)the exposure pathways for birds in terrestrial and aquatic proportion of purchased ammunition and fishing tackle systems (Kendall et al. 1996, Liu et al. 2008, Rattner et al. TheCondor:OrnithologicalApplications116:408–428,Q2014CooperOrnithologicalSociety S.M. Haig,J.D’Elia, C.Eagles-Smith, etal. Leadpoisoning inbirds 411 FIGURE3.TheremainsofPbandcopperbulletsfiredintoawaterbarrelfroma.30-06rifle.(A)UnfiredPbcorebullet(withacopper alloyjacket)nexttoremainsfromafiredbulletofsimilartype.Tinybulletfragmentsprovideagreatdealofsurfaceareaallowingfor increasedabsorptionofPbonceingestedbyscavengers.(B)Unfiredcopperbulletnexttotheremainsfromafiredbulletofsimilar type.Photos courtesy ofClintonEpps (C.Epps and D.Sanchez personal communication). 2008), and these are pathways that can be controlled and swans, is still a concern because of the greater depths at managed. which they forage within sediments (Smith et al. 2009). The highest human-caused Pb concentrations associat- Furthermore, drying of seasonal wetlands can expose edwithammunitionarefoundinandnearshootingranges pellets that upland species (e.g., doves and pheasants) (United Nations Environment Programme 2013), where ingest. patches of Pb shot may attain concentrations of 5–17 kg More difficult to estimate is bullet fragment density Pb m(cid:2)2 (Rattner et al. 2008). However, it is important to from big-game hunting, in which Pb is associated with note that these values are localized extremes, and there is offal(i.e.gutpiles)andcarcasses.Althoughthedensitiesof considerable variability in the soil Pb content in shooting Pb fragments are necessarily lower than those associated ranges (Bennett et al. 2007). Nevertheless, many grit- withshot,theyarealsomorelocalizedandassociatedwith seeking birds pick up Pb fragments at or near shooting an attractant (animal carcasses or offal) that could ranges. substantially increase the probability of avian exposure. Conversely, traditional hunting areas may be more ThedensityofPbfishingtackleinaquaticenvironments representative of the potential Pb exposure risk to wild is highly variable yet can have significant impacts on birds.AlthoughPbdensitiesaresubstantiallylowerthanin aquatic species such as loons and swans. Duerr (1999) target ranges (Ferrandis et al. 2008), the deposition of Pb estimated 0.01 and 0.47 sinkers m(cid:2)2 in areas of low and pellets from historical waterfowl and contemporary high fishing pressure in the United States, respectively. In Mourning Dove (Zenaida macroura) hunting provide the United Kingdom, estimates have ranged between 0.84 some of the strongest examples of the amount of Pb that and16.3 sinkersm(cid:2)2along theThamesRiver (Sears 1988) canbeassociatedwithhuntingactivitieswithinaconfined and between 24 and 190 sinkers m(cid:2)2 in shoreline areas in area (Box 1). During the period of Pb use for hunting Wales(Cryeretal.1987).Itisimportanttonotethatthese migratorywaterfowl,Bellrose(1959)estimateddensitiesas large estimates of lost-tackle densities are from locations high as 125,970 pellets ha(cid:2)1; more recently, Pain (1991) with exceptionally high fishing pressure and may not be reportedpelletdensitiesofnearly2millionpelletsha(cid:2)1.In representative of tackle densities in other locations. To managed upland dove-hunting fields where Pb shot is understand subsequent risk, it is crucial to understand legal, shot densities range from tens of thousands to relative waterbird use of the high-risk zone. For example, hundreds of thousands of pellets per hectare (Box 1 and Radomski et al. (2006) utilized creel surveys of walleye Figure 4). However, there are differences in how long Pb fishermen to evaluate rates of tackle loss across 5 pellets deposited on the landscape are available to birds, Minnesota lakes and estimated that Pb tackle densities in particularly between wetland and upland habitats. Flint 1 of these lakes was ,0.002 sinkers m(cid:2)2. Across the 5 and Schamber (2010) estimated that Pb pellets in the lakes, whose combined area was 267,933 ha, cumulative sedimentofwetlandswouldbeavailabletomostspeciesof total estimated Pb-tackle losses were found to be waterfowl for (cid:3)25 yr. If so, the risk of exposure to Pb .100,000 pieces, or ~1 metric ton year(cid:2)1 of the study pellets from past hunting for most waterfowl species in (Radomski et al. 2006). It is unclear what waterbird North America should be nearly eliminated, given that it exposureratesmightbeattheseMinnesotalakes;however, has been 14 and 22 yr since Pb shot has been banned in Pokrasetal.(2009) foundthat 118of522 (23%) Common Canada and the United States, respectively. However, Loon (Gaviaimmer)carcassesfrom 6New England states legacy Pb exposure in some waterfowl species, such as containedingestedPbobjects,primarilysinkersandjigs,as TheCondor:OrnithologicalApplications116:408–428,Q2014CooperOrnithologicalSociety 412 Lead poisoning inbirds S.M. Haig,J.D’Elia, C.Eagles-Smith, et al. BOX 1. Mourning Dove Hunting and Pb Pellet Dispersion Declinesinresidentuplandgame-birdpopulationsofNorthernBobwhite(Colinusvirginianus;Brennan1991)andRing- neckedPheasant(Phasianuscolchicus;RileyandSchulz2001,Freyetal.2003)havepromptedmanystateandprovincial resourcemanagementagenciestoincreaseMourningDoveshootingopportunitiesonpubliclands,especiallynearurban population centers, by creating attractive feeding spots (Schulz et al. 2003; Figure 4). However, Pb pellet deposition accumulates on fields managed for dove hunting. For example, on 5 public hunting areas managed for dove hunting in Missouri during 2005–2011, the average amount of traditional Pb ammunition deposited per year ranged between 2.5 and8.9kgha(cid:2)1amongareas,andtheestimatedaveragenumberofno.8Pbpellets,whichmeasure2.26mmindiameter, ranged between 35,624 and 128,632 ha yr(cid:2)1 among areas (Schulz et al. 2012). During 1998–1999, Pb shot deposition relatedtodovehuntinginsouthernNevadarangedfrom8,970to22,559pelletsha(cid:2)1infieldsmanagedprimarilyfordove hunting(GerstenbergerandDivine2006).Posthuntpelletdensitiesfrom15manageddovefieldsinIndianaduring1987 ranged from 2,152 to 83,928 pellets ha(cid:2)1 (Castrale 1989). Sampling of the upper soil layer in southeastern New Mexico during1987showedprehuntestimatesof167,593pelletsha(cid:2)1andposthuntestimatesof231,731pelletsha(cid:2)1(Bestetal. 1992). Posthunt pellet densities inTennessee were estimated at 107,821 pellets ha(cid:2)1 (Lewis and Legler 1968). Withinanationalcontext,~960,000dovehuntersroutinelyharvest16.6milliondovesannually(Seamansetal.2012), taking approximately 4 or 5 shots dove(cid:2)1 (Schulz et al. 2012) and potentially depositing 1,900–2,400 metric tons of Pb shot on publicly owned wildlife habitat across the country. Thus, reducing the deposition of Pb shot resulting from Mourning Dove hunting on public areas has the potential to substantially reduce Pb exposure in terrestrial wildlife, especiallyforasuiteofground-feedingpasserines(Fisheretal.2006)andgamebirds(HunterandRosen1965,Keeletal. 2002, Schulz et al. 2002, Potts 2005, Larsen et al. 2007, S. D. Holladay et al. 2012). FIGURE4.(A)HealthypectoralisinaMourningDove.(B)Erodedbreastmuscleduetolossofappetiteandreducedphysicalactivity followingingestionofPbpellets(shotsizeno.7.5).Muscleerosionoccurredin,22daysincaptivebirds(Schulzetal.2006).Photo courtesy ofJohnSchulz. well as ammunition. This suggests that although overall terrestrial areas, this pathway to Pb poisoning is most densities may be low across entire lakes, Pb tackle may be relevant to seed-eating birds that obtain grit for muscular concentrating in habitat sectors that increase exposure grindingofseedsinthegizzard(Fisheretal.2006,Rattner risk,assumingthatdensitiesoftackleinNewEnglandand et al. 2008). Some waterbirds also consume Pb objects for Minnesota lakes are comparable. useinthegizzardandbecomepoisonedthroughthesame Direct exposure. Direct exposure occurs when birds route (Smith et al. 2009) or in combination with Pb that mistakePbobjectsforseedsorgritandpurposefullyingest they consume when diving (Pokras et al. 2009). them, ofteninareas ofheavyhuntingand fishing pressure Indirect exposure. Indirect exposure to Pb occurs or at established shooting ranges (Boxes 1 and 2). In when predators and scavengers incidentally ingest Pb TheCondor:OrnithologicalApplications116:408–428,Q2014CooperOrnithologicalSociety S.M. Haig,J.D’Elia, C.Eagles-Smith, etal. Leadpoisoning inbirds 413 whenconsumingthefleshofananimalthathasbeenshot understanding how environmental exposure is linked to with Pbammunition or that ingestedPbsinkersorasoil- toxicological responses. dwelling organism containing high Pb levels (Boxes 1, 2, At the organismal level, Pb poisoning can modify the and 3; Figure 4). Scavenging raptors such as eagles, structureandfunctionofkidney,bone,thecentralnervous vultures,andcondorsaretypicallyinfluencedbythisroute system, and the hematopoietic system, leading to adverse of Pb poisoning (Box 2; Figures 5 and 6). They make biochemical, histopathological, neurological, and repro- extensive use of offal from harvested animals and from ductive effects (Boggess 1977, Nriagu 1978, DeMichele carcasses of animals that are killed for recreation (e.g., 1984, Eisler 1988, Rattner et al. 2008, Franson and Pain prairie dogs [Cynomys spp.]) or for animal control 2011).Theseeffectscanbeobservedataveryyoungage,as purposes or that are shot by hunters but cannot be shown by studies of nestling Western Bluebirds (Sialia retrieved(Fisheretal.2006,Kellyetal.2011,Bedrosianet mexicana)andJapaneseQuail(Coturnixjaponica;Fairand al. 2012, Harmata and Restani 2013). Importantly, Pb Myers 2002, Fair and Ricklefs 2002). The range of bullets expand or ‘‘mushroom’’ and then fragment, physiological effects is mirrored by the range of potential dissipating the bullet’s energy. As a result, an average of responsestoexposure.Acutepoisoningmayoccurrapidly, 235 (range: 15–621) and 170 (range: 85–521) Pb without characteristic signs such as emaciation or lack of fragments remain in the eviscerated carcass and viscera, coordination(LockeandThomas1996).Chronicexposure respectively (Hunt et al. 2007, 2009; Knott et al. 2010; results in lethargy and anorexia, breast-muscle atrophy, Figures 5 and 6). This fragmentation increases the loss of strength and coordination, drooping wings, and likelihood that multiple individuals can be exposed to changes in vocalization (see Figure 6). Pbfromasinglecarcassorgutpile.Inaddition,thesmall Modes of action. Neurological impacts of Pb on sizeandincreasedsurfaceareaofthefragmentsthatstem animals are highly contingent on the chemical form of from spent ammunition also increase the uptake of Pb Pb, dose, and exposure duration, as well as the age, sex, into the bloodstream (Hunt et al. 2009). Although these and health of the bird (Mu¨ller et al. 2008). In the avian exposure sources may be highly localized, the magnitude body, Pb mimics calcium and substitutes for it in many oftheirnegativeeffectsisincreasedwhentheyareusedas fundamental cellular processes, including nervous-system food resources by widely dispersing, highly social scaven- function(Simons1993,Floraetal.2006).Forexample,Pb gers(e.g.,vulturesandcondors).Finally,indirectexposure canactivateprotein kinaseC,whichplaysacriticalrolein can also occur in ground-feeding species that rely heavily the vertebrate nervous system by controlling the function on earthworms as prey (Scheuhammer et al. 1999, 2003), of other proteins (Hwang et al. 2002). Pb poisoning also suchastheAmericanRobin(Turdusmigratorius;Beyeret leads to anemia by reducing heme synthesis and decreas- al.2004,2013)andAmericanWoodcock(Scolopaxminor; ing thelifespan oferythrocytes (Eisler 1988, Goyer1996). Scheuhammer et al. 1999, 2003). Pb affects the nervous system by changing calcium Leadimpactonavianphysiology.PbingestedfromPb homeostasis and inhibiting cholinergic nerve cells, thus pelletsorbulletfragmentsisabsorbedintothecirculatory interfering with signal transmission across nerve synapses system, aided by the grinding action in the gizzard; thus, and leading to behavioral changes (Sanders et al. 2009). diet can affect Pb uptake rates (Marn et al. 1988, Locke Thecerebellumistheprimary targetforPbtoxicityinthe and Thomas 1996,Vyas et al. 2001). Once Pb is absorbed brainandisthemajordeterminantforbehavioralchanges into the body, its toxicological effects are diverse. (Alfano and Petit 1981). Experimental studies with However, as is true with nearly all contaminants, environmentallyrelevantPbdosesinwildnestlingHerring interspecific variation in tolerance to Pb is considerable, Gulls(Larusargentatus)demonstratedthatPbimpairment whichmakesitdifficulttoassessrisksolelyonthebasisof can result in decreased health, less vigorous food- blood Pb levels. For example, the California Condor acquisition behaviors, poor coordination, and decreased (Gymnogyps californianus) experiences significant mor- survival (Burger and Gochfeld 1994). tality as a result of Pb ingestion (Finkelstein et al. 2012). Pb also impairs the enzymes d-aminolevulinic acid Conversely, Carpenter et al. (2003) found that Turkey dehydratase (d-ALAD) and ferrochelatase, ultimately Vultures (Cathartes aura) repeatedly dosed with large interfering with heme synthesis, and resulting in anemia numbersofPbshotandconstantredosingsurvivedmuch ifexposureishighenough(Hoffmanetal.1985).Northern longerthanotherspeciesofavianscavengers,suchasBald Bobwhites (Colinus virginianus) dosed with a single no. 9 Eagles (Haliaeetus leucocephalus), that received similar Pb shot (i.e. 2 mm in diameter) exhibited only 8% of doses of Pb (Hoffman et al. 1981). These studies suggest normalALADactivity8wkafterdosing(S.D.Holladayet that complex physiological processes regulate exposure al.2012).ThesamedoseregimeresultedinbloodPblevels and toxicity risk to Pb and vary even between close .80 times higher than background in captive Rock relatives. Thus, factors beyond the gross number of Pb Pigeons (Columba livia; J. P. Holladay et al. 2012). In wild pellets or bullet fragments ingested are important in birds, d-ALAD and intermediary metabolites such as TheCondor:OrnithologicalApplications116:408–428,Q2014CooperOrnithologicalSociety 414 Lead poisoning inbirds S.M. Haig,J.D’Elia, C.Eagles-Smith, et al. BOX 2. Demographic Effects of Pb Ingestion on California Condors and Other Avian Scavengers California Condors were nearly driven to extinction in the 1980s, and the cause of their decline was unknown at that time (Snyder and Snyder 2000, Walters et al. 2010, D’Elia and Haig 2013). Substantial evidence now points to ingestion of Pb ammunition in carcasses as the primary factor preventing California Condors from achieving self-sustaining populations (Church et al. 2006,Walters et al. 2010, Finkelstein et al. 2012). A related study of Pb isotopes in Andean Condor (Vultur gryphus)feathersinnorthwestPatagoniasuggeststhattheyarealsobeingexposedtoPbfromammunition(Lambertucciet al.2011).OtheravianscavengersthatshareoneormoreofthefollowingtraitsandoccurinregionswherePbisavailablein gut piles or dead animals may also be at elevated risk of adverse effects. Obligate scavenger. Obligate scavengers represent an extreme specialization in the animal kingdom, being completely reliant on other agents to kill their food. These species are limited to the condors and vultures (Ruxton and Houston 2004). Their inability to procure live prey places them at greater risk of exposure to Pb shot from animals left in the field or offal from harvested animals. Largesize.Largeavianscavengerssearchoutfoodinlarge quantities to meet their energy requirements (Ruxton and Houston 2004). This preference for larger food items may increase their exposure to Pb in areas frequented by big- gamehunters.Theirlargesizealsomeansthattheyconsume arelativelylargequantityofmeatateachcarcass,increasing their risk of exposure to any contaminants that may be disproportionatelydistributedthroughoutthecarcass. Life-history pattern of low reproduction and high an- nual survival. Low reproductive output of 1 or 2 offspring every 1 or2yr,an extended subadult period ofseveralyears priortorecruitmentintothebreedingpopulation,andalong life span of several decades or more define a life-history pattern that can be sensitive to small changes in adult survival rates(Mertz1971,Meretskyetal.2000).Long-lived species are also at greater risk of multiple exposures and, thus, at greater risk of sublethal effects (Hunt 2012). Social foraging.Species thattend toroost andfeedcom- munallyasanadaptationforfindingresourcesthatarelarge and ephemeral are at greater risk than species whose individuals roost and forage alone (Dermody et al. 2011). Social behavior such as communal roosting and sharing of food resources may increase the risk that a single contaminated carcass can poison a large number of individuals in the same feeding. Physiological factors. Anumberofintrinsicfactorsinflu- ence species’ susceptibility to Pb poisoning, including retention of Pb after ingestion versus regurgitation (Stendell 1980), nutritional status and diet, and chemical environment inthelumen(Patteeetal.2006).Speciesthatfailtoregurgitate ingested Pb fragments are likely to suffer greater exposure. Multiple lines of evidence point to Pb ammunition as the primary source of Pb poisoning in avian scavengers. These FIGURE 5. (A) Golden Eagle (Aquila chrysaetos) chick with a include the spatiotemporal relationship of Pb exposures to Belding’s ground squirrel (Spermophilis beldingini) food source hunting areas and season, Pb isotope ratios in feathers and (Upper Malheur River, Harney County, May 2013). Photo blood (Scheuhammer and Templeton 1998, Church et al. courtesy of Eric Forsman. (B) Radiograph of Pb fragments in 2006, Lambertucci et al. 2011), elevated copper concentra- Belding’sgroundsquirrelsfounddeadinafield.Photocourtesy tions in the kidneys of Pb-exposed eagles as an indicator of ofJeffCooney. TheCondor:OrnithologicalApplications116:408–428,Q2014CooperOrnithologicalSociety S.M. Haig,J.D’Elia, C.Eagles-Smith, etal. Leadpoisoning inbirds 415 thepresenceofcopper-jacketedPbbullets(Cruz-Martinezet al. 2012), radiographs of Pb-exposed scavenger gastrointes- tinal tracts (e.g., Helander et al. 2009; Figure 6) and food items (Knopper et al. 2006, Hunt et al. 2009; Figure 5), and toxicologicalstudiescombinedwithdirectfieldobservations and necropsies (e.g., Finkelstein et al. 2012).Taken together, and without a reasonable alternative hypothesis, these studies collectively provide a compelling indication that ammunition is the predominant source of Pb poisoning in scavenging birds. The association in time and space between elevated Pb levelsorPbexposureratesinavianscavengersandbig-game huntinghasbeenobservedinmultiplespeciesacrossdiverse regions of the world: Bald and Golden eagles in the upper midwesternUnitedStates(KramerandRedig1997,Stromet al. 2009, Cruz-Martinez et al. 2012); Bald Eagles and Common Ravens (Corvus corax) in the Rocky Mountains (Craighead and Bedrosian 2008, Bedrosian et al. 2012); Golden Eagles, Turkey Vultures, and California Condors in southernCalifornia(Halletal.2007,KellyandJohnson2011, Kelly et al. 2011); California Condors in Arizona and Utah (Hunt et al. 2007); and Steller’s Sea Eagles (Haliaeetus pelagicus) and White-tailed Sea Eagles (H. albicilla) in Hokkaido, Japan (Saito 2009).These findings are consistent with the hypothesis that scavengers are consuming Pb in carcasses from hunting. Not all studies have found a significant relationship between Pb concentrations or Pb exposure rates and big- game hunting seasons (Martina et al. 2008, Stauber et al. 2010) and, even where significant correlations exist, many studieshavefoundthatPbexposuresarenotstrictly limited tobig-gamehuntingseasons.Furthermore,Pbpelletsand.22 bullets not associated with big-game hunting have been recovered in the digestive tracts of California Condors (Rideoutetal.2012),BaldandGoldeneagles(Cruz-Martinez etal.2012),andseaeagles(Helanderetal.2009),andinthe pellets of EgyptianVultures (Neophron percnopterus; Dona´- zar et al. 2002). The fact that ammunition can be delivered via multiple sources to avian scavengers means that in many areas, effective treatment of this threat will require more than simplyeliminatingPbammunitionusebybig-gamehunters. However, these hunters remain the key to survival for most scavengersintheworld(Mateo-Toma´sandOlea2010).They are now the top predator in modern ecosystems, and the remnants of hunting are a more important wildlife food source now than at any other time in history. weakness, and wing droop. (B) X-rays indicating location of Pb FIGURE 6. Pb poisoning in Bald Eagles following consumption bullet fragments in coyote. (C) Pb-poisoned Bald Eagles of carcasses containing Pb bullet fragments. (A) Adult showing collectedinoneIowalocationover1yrbyProjectSOAR.Photo muscle degeneration, unable to stand, open-mouth breathing, courtesy ofProjectSOAR. TheCondor:OrnithologicalApplications116:408–428,Q2014CooperOrnithologicalSociety 416 Lead poisoning inbirds S.M. Haig,J.D’Elia, C.Eagles-Smith, et al. protoporphyrin in blood are used as biomarkers of et al. 2004, Schulz et al. 2007, Ferrandis et al. 2008). exposure (Locke and Thomas 1996). Time for d-ALAD Although differences in methodology likely played some recoverytonormallevelsisdosedependent,organspecific, role, a more plausibleexplanation isintrinsicinterindivid- and usually directly correlated with blood Pb levels. ual and interspecific variability in sensitivity to Pb. This Population-level effects of Pb.The potential effects of sourceofvariationcomplicatesoverallestimatesofPbrisk Pb poisoning on individual birds are clearly established. to avian communities and represents a key data gap in Pb Far less clear are the population-level consequences of ecotoxicology. current rates of Pb exposure in many species. The best Acute toxicity leading to mortality can often be examples are from waterfowl, in which losses to Pb determined from physical or behavioral cues, especially if poisoning were estimated to be 2–3% overall, with an tissues are analyzed for Pb content postmortem. But it is estimated4%annuallossinMallards(Anasplatyrhynchos; uncommon to encounter Pb-intoxicated birds for which Sanderson and Bellrose 1986). Similarly, Grand et al. this information can be obtained, which complicates (1998) estimated that survival rates of female Spectacled attempts to estimate actual mortality due to Pb. As a Eiders (Somateria fischeri) exposed to Pb shot from result,numerousstudieshavereportedPblevelsintissues ingestionwere34%lowerthanthoseofunexposedfemales from dead birds, making the implicit assumption that (77%) and suggested that Pb exposure may have been mortality was a result of Pb exposure in those birds with preventing local population recovery. California Condor elevated concentrations (Helander et al. 2009, Herna´ndez populations appear to be at substantial risk from Pb and Margalida 2009, Kenntner et al. 2001, Wayland and exposure (e.g., Cade 2007,Walters et al. 2010, Finkelstein Bollinger1999).Insomecases,mortalityislikelyduetoPb etal.2012).Pbsinkersappeartobearegulatoryfactorfor poisoning,butaswenotedabove,thetremendousrangein Common Loons in New Hampshire, where 49% of known sensitivities among individuals and species can make the mortalities are attributed to Pb poisoning from fishing use of tissue thresholds to infer cause of death problem- tackle (Vogel 2013). atic. Thus, the proportion of birds found dead with Significance of Pb exposure to avian conservation. elevated Pb concentrations is often a poor and biased Given proof that elevated Pb exposure can greatly (under or over) estimator of mortality rates. influence the health of individual birds and can result in The cumulative body of scientific evidence unequivo- mortality, the environmental distribution of Pb from cally suggests that Pb exposure from ammunition and ammunition and fishing tackle could be an important fishing tackle is directly responsible for numerous bird factor influencing the conservation of avian communities. deaths each year and is clearly a serious threat to the Here, we discuss (1) the apparent contradiction in results populationtrajectoryoftheendangeredCaliforniaCondor of some studies regarding avian exposure and levels of (Franson et al. 2003,Walters et al. 2010, Finkelstein et al. impairment caused by different contaminant concentra- 2012; Box 2). However, for many bird species, the impact tions; (2) unease with the implicit assumption of many of Pb exposure is much less clear given the assortment of published studies that Pb is the ultimate source of otheranthropogenichazardsandconservationthreatsthey mortality for birds found dead with elevated Pb concen- face.Forexample,.1billionbirdsyear(cid:2)1are estimated to trations;and(3)lackofclarityovertherelativethreatofPb be killed by domestic cats in the United States (Loss et al. to birds in comparison to other major impacts such as 2013), and millions of bird mortalities each year result invasivespecies,habitatloss,humandisturbance,domestic fromcollisionswithpowerlines,fixedobjects,andvehicles cats,andcollisionswithvehicles,powertransmissionlines, (Loss et al. 2014). In addition, habitat loss and intensified and buildings. land use can have an immeasurable impact on the Wehavealreadypresentedseveralexamplesofincreases conservation status of many bird species at global scales. in avian Pb exposure in association with ammunition and However, addressing the Pb issue is tractable because it tackle. Similarly, we have outlined many instances of entails a relatively simple solution: replacing Pb-based toxicity associated with environmental and lab-derived ammunition and fishing tackle with non-Pb alternatives. exposuretoPb.However,theresultsofotherstudiesadda Proponents of this solution contend that alternatives to layer of ambiguity to this topic that is important to Pb are readily available and of comparable cost and that acknowledge. For example, even at relatively similar Pb the costs are expected to decrease with increases in exposure levels, studies have shown clear effects on blood demandthataccompanyimprovedefficienciesinballistics chemistry(Kerretal.2010,Carpenteretal.2003,Hoffman (Thomas 2013). Conversely, supporters of continued Pb et al. 1981, Pattee et al. 2006), egg production (Edens and use in ammunition and fishing tackle argue that the Garlich1983),behavior(BurgerandGochfeld1994,2004), increased costs of non-Pb alternatives require robust and andsurvival(Schulzetal.2006,Grandetal.1998,Patteeet clearscientificevidenceofimpacts beforeanychangesare al.2006,Rideoutetal.2012),whereasothersdemonstrated made. However, these competing ideas are not mutually limitedresponsestomanyofthesameendpoints(McBride exclusive. Progress could be made in reasonably short TheCondor:OrnithologicalApplications116:408–428,Q2014CooperOrnithologicalSociety S.M. Haig,J.D’Elia, C.Eagles-Smith, etal. Leadpoisoning inbirds 417 order to reduce avian Pb exposure and increase scientific knowledge of Pb’s impacts through an integrated plan of BOX 3. Recreational Shooting of Ground Squirrels voluntary Pb replacement programs coupled with large- One component of the environmental distribution of Pb- scale research efforts to evaluate the effects of Pb based ammunition thatispoorly understood but that may management on avian Pb exposure. beanimportantsourceofPbexposureforavianscavenger species is the recreational shooting of ground squirrels Priority Research Directions such as Belding’s ground squirrel, California ground Results from countless studies have concluded that Pb squirrel (S. beecheyi), and Richardson’s ground squirrel continues to be introduced into the environment through (S. richardsonii) (Knopper et al. 2006, Pauli and Buskirk Pbammunitionandfishingtackle,andthattheseformsof 2007). Ground-squirrel shooting is generally unregulated, Pb are being ingested by a wide diversity of avian taxa, individual squirrels are commonly not retrieved, and causing illnessandmortality.Thereare additionalareasof recreational shooters almost exclusively use expandable investigation that might identify key areas to target Pb Pb bullets that result in hundreds of Pb fragments in reduction and could inform priorities for broader Pb- ground-squirrel carcasses (Pauli and Buskirk 2007). reduction programs in the future. Thus, we identify four Further, it is not uncommon for individual recreational futureresearchquestionstoimproveourunderstandingof shooterstoshoot.170squirrelsinasingleday(Pauliand the threat posed by Pb poisoning: (1) What factors are Buskirk 2007). Across large portions of avian habitats, the responsible for interspecific variation in sensitivity to Pb total number of available Pb-laced squirrel carcasses is exposure? (2) What is the spatial extent of Pb contami- difficult to estimate, and they are likely very patchily nation in habitats, and how is this linked to bird exposure distributed, given land-ownership patterns and squirrel in those same locations? (3) How does the interaction of densities. However, Reeve and Vosburgh (2005) reported Pb exposure and landscape-level or environmental stress- that .1.1 million ground squirrels were shot over a 1-yr orsaffectbirdsatthepopulationlevel?And(4)whatisthe period (2000) in South Dakota. Moreover, Pauli and influence of Pb on key demographic parameters (e.g., Buskirk(2007)demonstratedthatingroundsquirrelsshot survival) in relation to other causes of morbidity and with expandable Pb-based bullets, ~70% of the fragments mortality? remaining in the carcass were small (,25 mg). Smaller Variation in Pb sensitivity. Numerous studies have fragments are more easily ingested than large ones, and evaluated toxicological responses of birds to Pb exposure smaller fragments present relatively greater surface area, (Franson and Pain 2011), but a consistent, ecologically increasing the rate of Pb absorption into the bloodstream meaningful,andstandardizedapproachdoesnotcurrently of the scavenger. Further, Pauli and Buskirk (2007) found exist. This makes it challenging to prioritize how best to that47%ofallprairiedogsshotwithexpandablePb-based manage for Pb risk and makes comparative assessments bulletshadsufficientquantitiesofPbinasinglecarcassto across multiple taxa difficult. Thus, an important step in result in mortality of nestling raptors. There are (cid:3)13 reducing Pb exposure in birds is the development of a species of birds that regularly scavenge dead ground squirrels,includingBaldEagles,FerruginousHawks(Buteo standardized vulnerability assessment that considers life- regalis), Golden Eagles, and Swainson’s Hawks (Buteo history traits, exposure likelihoods, and sensitivity to the swainsoni;Schmutzetal.1989,HarmataandRestani1995, toxic effects of Pb. Of note, the concept of differential Hoogland 2003). Given the degree to which Pb-laced sensitivity among avian species that allows for thresholds ground-squirrel carcasses may be available to avian that vary among taxa is well established for a range of scavengers, particularly raptor scavengers whose popula- contaminants (e.g., organochlorine pesticides, polychlori- tions are decreasing, such as Swainson’s Hawk, there is an natedbiphenyls,mercury,andselenium;Eisler1986,Heinz immediate need for information to better understand the et al. 2009, Blus 2011, Ohlendorf and Heinz 2011, and spatial and temporal risks associated with contamination many others). For example, Buekers et al. (2009) by Pb bullet fragments. summarized results of 13 repeated-dosage studies of Pb for12avianspecies.Includingarangeofendpointsintheir analysis, they found a 50-fold range in estimates of no- observed–effectconcentrations.Thus,similarPbexposure levels will likely elicit a wide range of effects across a ecologically relevant endpoints (e.g., growth, survival, gradient of species. Unfortunately, few studies encompass behavior, and reproduction). the range of primary exposure mechanisms with similar Pb contamination and distribution. The spatial exposure periods under standardized conditions. These distribution and availability of Pb in the environment are estimates are important for providing context to Pb complicated by the need toaccount formultiplePbsource exposure across the landscape and should incorporate types (Figure 1). Studiesthatfocusonammunitionsources TheCondor:OrnithologicalApplications116:408–428,Q2014CooperOrnithologicalSociety