Gymnogyps californianus - Journal of Wildlife Diseases

DOI: 10.7589/2014-10-253

Journal of Wildlife Diseases, 51(4), 2015, pp. 901–906 # Wildlife Disease Association 2015

Lead Exposure Risk from Trash Ingestion by the Endangered California Condor (Gymnogyps californianus) Myra E. Finkelstein,1,7 Joseph Brandt,2 Estelle Sandhaus,3,4 Jesse Grantham,2 Allan Mee,5,6 Patricia Jill Schuppert,1 and Donald R. Smith1 1Microbiology and Environmental Toxicology Department, University of California, 1156 High St., Santa Cruz, California 95064, USA; 2US Fish and Wildlife Service, 2493 Portola Rd. Suite B, Ventura, California 93003, USA; 3Center for Conservation and Behavior, Georgia Institute of Technology and Department of Conservation and Research, 654 Cherry Street, Atlanta, Georgia 30332, USA; 4 Department of Conservation and Research, Santa Barbara Zoo, 500 Nin˜os Drive Santa Barbara, California 93103, USA; 5San Diego Zoo Global, 15600 San Pasqual Valley Road, Escondido, California 92027, USA; 6 Golden Eagle Trust Ltd., 22 Fitzwilliam Square, Dublin 2, D02 FH68, Ireland; 7Corresponding author (email: [email protected])

Arizona (n573), and Baja California, Mexico (n529; US Fish and Wildlife Service [USFWS] unpubl. data). Currently, wild California Condors face multiple threats to their recovery, including lead poisoning and trash ingestion (Mee and Snyder 2007; Finkelstein et al. 2012; Rideout et al. 2012). Although there is clear evidence that ingestion of spent lead ammunition from feeding on carcasses is the principal source of lead exposure to condors (Parish et al. 2009; Finkelstein et al. 2012) other sources, such as trash ingestion, may also be an exposure risk (Walters et al. 2010). Trash ingestion is well-documented in California Condors, particularly those nesting in southern California (Mee et al. 2007a, b). We use the term “trash” to describe the broad category of small nonfood items, including glass and plastic debris, bottle caps, and spent ammunition casings, which condors ingest or transport back to nest sites (Mee et al. 2007b). Although injury and death from physical obstruction due to trash ingestion occurs (Rideout et al. 2012), the risk of lead poisoning from trash ingestion is unknown, although it has been suggested as a potential source of lead exposure to condors (Walters et al. 2010). Fifty-four sets of trash samples containing 1,413 items were collected by USFWS Condor Recovery Program personnel between 2002 and 2008. Samples were

ABSTRACT: Lead poisoning from ingestion of spent lead ammunition is one of the greatest threats to the recovery of California Condors (Gymnogyps californianus) in the wild. Trash ingestion by condors is well documented, yet the extent that trash presents a lead exposure risk is unknown. We evaluated 1,413 trash items collected from condor nest areas and nestlings in the Transverse Range of Ventura County, California, US, from 2002 to 2008, for their potential as a lead exposure risk to condors. We visually identified 71 items suspected to contain sufficient lead to be of toxicologic concern. These items were leached with weak acid and analyzed for lead. Twentyseven of the 71 leached items (,2% of the 1,413 items) were “lead containing” based on criteria of a leachate lead concentration .1 mg/ mL, with the majority of these items (22; 81% of the 27 lead items) being ammunition related (e.g., spent bullet casings and jacketed bullets). Only three of the 1,413 items collected were lead containing but were clearly not ammunition related; the other two lead-containing items were unidentified. Our results suggest that trash ingestion of nonammunition items does not pose a significant lead exposure risk to the California Condor population in California. Key words: Ammunition, California Condor, exposure risk, lead, trash, vulture.

The California Condor (Gymnogyps californianus) approached extinction in the 1980s before an intensive captive breeding and management program led to a steady increase in the population. As of 31 December 2014, there were 423 California Condors, approximately half of which were free flying and associated with release programs in California (n5128), 901

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recovered from the digestive tract of condor nestlings during necropsies, sifted from the nest substrate, or the immediate environs of eight nest sites monitored by the Hopper Mountain National Wildlife Refuge Complex. Between 2002 and 2006, trash samples were collected following the methods of Mee et al. (2007b). In 2007 and 2008, under a new protocol, trash samples were collected from active nest sites approximately every 30 d (USFWS 2012). Survey data indicate the number of trash items recovered has not changed significantly since the study period (annual number of trash items recovered [average6SD]: 2002–0852376156; 2009– 1351856166; USFWS unpubl. data). Although biologists believe the majority of trash items were brought to the nest area intentionally by adult condors, some items may have been ingested while a bird was foraging remote from the nest site and later regurgitated to the nestling or onto the nest site surface. Of the 1,413 items evaluated, we visually categorized 328 as “metal” (clearly containing some metal). These metal items were sorted into 1) items judged not to be of toxicologic concern for lead (e.g., bottle caps, coins, washers, bolts; n5257) and 2) items that may contain sufficient lead to be of toxicologic concern if ingested, such as ammunition-related items, electronics, and metal wire (n571; see Supplementary Material Fig. S1). Ammunition-related items were those clearly identifiable as such (e.g., spent bullet casing or jacketed bullet, shotgun shell casing; see Supplementary Material Fig. S2), and these categorizations were verified by two individuals with a combined 48 yr of firearm and wildlife game warden–related experience. The 71 metal-containing items identified to possibly contain lead of toxicologic concern were individually cleaned by rinsing with acetone and then deionized water, dried at 65 C overnight, leached in 4 mL 1% trace metal-grade HNO3 for 1 min, and the leachate filtered through

a 0.5-mm Teflon filter. The leaching procedure was intended to remove chemically labile (i.e., readily leachable) surface lead, not to leach lead from within the solid matrix of the objects or quantify the biological availability of lead associated with the objects if ingested (Finkelstein et al. 2012, 2014). Leachates were analyzed for lead and 10 other metals (antimony, bismuth, cadmium, chromium, copper, iron, nickel, silver, tin, and zinc) by optical emission spectrometry (PerkinElmer Optima 4300 DV, Waltham, Massachusetts, USA), to characterize the elemental composition of items that were a potential lead exposure risk. Analytical limits of quantitation (LOQ; reported here as 103 the standard deviation of three blank samples in micrograms per milliliter) were 0.066 (lead), 0.710 (antimony), 0.530 (bismuth), 0.012 (cadmium), 0.004 (chromium), 0.012 (copper), 0.180 (iron), 0.004 (nickel), 0.007 (silver), 0.051 (tin), and 0.220 (zinc). All leachate samples for antimony and bismuth were below the LOQ. Items with a leachate lead concentration .1 mg/mL were classified as containing sufficient lead to be of potential toxicologic concern and henceforth referred to as “lead containing.” This criterion was based on the lead concentration in separate leachates from two lead bullets (31 mg/mL and 40 mg/mL, referred to as “Reference bullets” in Table 1) obtained through a hunter exchange program (Finkelstein et al. 2012). Thus, our .1-mg/mL leachate threshold criteria for a lead-containing item is ,30-fold lower than levels measured in lead bullet leachates and a conservative threshold to assess if an item could be a significant source of lead exposure to condors if ingested. From a visual assessment of 1,413 individual trash items, the majority were classified as glass (,45%), plastic (,27%), metal containing (,23%), organic (,4%), or ceramic (,1%; see Supplementary Material Fig. S3A). Of the 328 metal-containing items

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TABLE 1. Metal concentrations in leachates (mg/mL) of trash samples (see Supplementary Material Fig. S1) collected from eight California Condor (Gymnogyps californianus) nest areas and opportunistically from condor nestlings between 2002 and 2008 from the Transverse Range of Ventura County, California, USA. Descriptive statistics reflect only the number of samples above the limit of quantitation (LOQ; see methods) for each metal. If the number of samples within a category above the LOQ was ,3, concentrations for each sample are reported individually. — 5 no sample leachates were above the LOQ for that category. Reference bulletsa

ng 2 Lead 31, 40 Median — Mean6SD — Range — No. of samples.LOQ — Silver — Median — No. of samples.LOQ — Cadmium — Median — Mean6SD — Range — No. of samples.LOQ — Chromium — Median — Mean6SD — Range — No. of samples.LOQ — Copper 0.082, 0.053 Median — Mean6SD — Range — No. of samples.LOQ — Iron — Median — Mean6SD — Range — No. of samples.LOQ — Nickel — Median — Mean6SD — Range — No. of samples.LOQ — Tin — Median — Mean6SD — Range — No. of samples.LOQ — Zinc — Median — Mean6SD — Range — No. of samples.LOQ — a

Ammunitionleadb

Ammunitionnonleadc

22 — 48 1706290 1.1–1,300 22 — — — — 0.019 0.02360.009 0.017–0.033 3 — 0.007 0.01160.011 0.005–0.039 9 — 17 41680 0.054–370 22 — 2.3 2.661.9 0.60–6.0 16 — 0.034 0.04260.036 0.007–0.16 21 — 2.6 2.461.7 0.12–4.3 4 — 3.5 7.2610 0.32–41 19

30 — 0.29 0.3160.18 0.081–0.96 29 — 0.008 1 — 0.014 0.01660.003 0.013–0.020 3 — 0.02 0.02560.019 0.005–0.061 14 — 39 43632 0.076–120 30 — 9.1 1369.6 1.5–29 15 — 0.043 1.264.6 0.019–24 30 — 0.078, 0.096 — — 2 — 19 17612 0.43–45 29

Otherleadd

Other-nonleade

3 13 — — 3.5 0.27 5.265.2 0.3260.24 1.1–11 0.099–0.70 3 6 — — — — — — — — — — — — — — — — — — 0.054 0.029 — 0.03560.027 — 0.008–0.075 1 5 — — 16 0.52 36649 8.1620 0.91–92 0.032–71 3 13 — — 0.84 6.4 — 7.968.4 — 0.50–24 1 7 — — 0.015, 38 0.042 — 1.764.6 — 0.005–16 2 13 — — — — 0.18 0.33 — — 1 1 — — 0.32, 1.6 0.85 — 1.963.0 — 0.28–8.0 2 6

Unknownf

3 — 1.2 1.060.83 0.13–1.8 3 — — — — — — — — — 0.096 — — 1 — 0.24 1.361.9 0.071–3.5 3 — 12 1063.8 6.0–13 3 — 0.44 5.569.0 0.035–16 3 — — — — — — 0.96, 1.2 — — 2

Reference bullets 5 lead-based bullets obtained through a hunter exchange program (Finkelstein et al. 2012). Ammunition-lead 5 samples that contained lead (leachate .1 mg/mL) and were clearly ammunition related. c Ammunition-nonlead 5 samples that did not contain lead (leachate ,1 mg/mL) and were clearly ammunition related. d Other-lead 5 samples that contained lead (leachate .1 mg/mL) and were clearly not ammunition related. e Other-nonlead 5 samples that did not contain lead (leachate ,1 mg/mL) and were clearly not ammunition related. f Unknown 5 samples that were unable to be classified as ammunition related or not. g n 5 number of samples in each category. b

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(items containing visible metal), 257 were judged not to be of toxicologic concern for lead (e.g., bottle caps, coins, washers, bolts), with over 70% of these items (n5186) consisting of bottle caps. The remaining 71 metal-containing items were further classified as a clearly identified component of ammunition (n552), unknown (n53), or other (n516; see Supplementary Material Figs. S2 and S3B). Lead concentrations in the leachates from the 71 metal-containing items ranged from below the LOQ (,0.066 mg/mL) to 1,300 mg/mL (Table 1). Twenty-seven items were lead containing based on a leachate leadconcentration .1 mg/mL (Table 1). Of these 27 items, 22 (,81%) were visually classified as ammunition related (e.g., spent bullet casings and jacketed bullet fragments; Table 1, Ammunition-lead category), two items were classified as “unknown” but were possibly ammunition related (Table 1, Unknown category), with the remaining three items (Table 1, Other-lead category) described as a 231-cm piece of sheet metal–like material, a 2.531-cm piece of circuit board electronics, and a ,2-cm-diameter dial (see Supplementary Material Figs. S2 and S3C). The 15 items with the highest lead concentrations (median5110; range527–1,300 mg/mL) were ammunition related. Leachate concentrations for metals other than lead were generally very low. Concentrations of silver, cadmium, and chromium were ,0.1 mg/mL; concentrations of tin were ,0.5 mg/mL for all trash categories except the Ammunition-lead category, which had tin leachate concentrations up to 4.3 mg/mL (Table 1). Nickel and iron concentrations were higher (up to 29 mg/mL), while copper and zinc concentrations ranged up to 370 mg/mL and 45 mg/mL, respectively (Table 1). Of the 1,413 trash items evaluated, only 27 (2%) exceeded our leachate lead concentration threshold (.1 mg/mL) for classification as lead containing and a potential lead exposure source to condors. Further, less

than 0.3% of the clearly nonammunitionrelated items (3 of 1,358) were classified as lead containing. Our findings indicate that ingestion of nonammunition-related trash does not pose a significant lead exposure risk to California Condors nesting in southern California. Lead has been shown to be the leading cause of mortality in juvenile and adult free-flying condors (Rideout et al. 2012). Zinc and copper are essential elements, yet high tissue levels of these metals can cause adverse health effects. Of the subset of trash items selected for elemental analysis because they were judged to potentially contain sufficient lead to be of toxicologic concern (see Supplementary Material Fig. S1), a few had relatively high copper and zinc concentrations in their leachates (Table 1). Zinc toxicosis associated with trash ingestion was diagnosed as the immediate cause of death for one California Condor nestling, and two other nestlings that died of trash ingestion had elevated liver copper concentrations, although no cases of copper-associated morbidity or mortality have been reported in California Condors (Rideout et al. 2012). Why condors or other vultures ingest trash is unclear (Mee et al. 2007b). Some have suggested that it may be a behavioral response to a calcium (Richardson et al. 1986) or other nutritional need when food sources are scarce (Benson et al. 2004), which would suggest that the trash items are mistaken for items of nutritional value. Houston et al. (2007) considered these hypotheses but also suggested that condors may consume nondigestible items to aid in gastric pellet formation. For condor nestlings, trash ingestion and subsequent gastrointestinal impaction is the primary cause of mortality (Rideout et al. 2012) and has resulted in the establishment of intensive nest monitoring practices (e.g., removal of trash from and around nests and examinations of nestlings for signs of trash impaction). Behavioral observations associated with this intensive management, aided in part by daily location

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monitoring with radio or satellite telemetry, provided no evidence that condors visited municipal dumps or trash dumpsters; rather, “trash sites” where condors have been observed ingesting items were locations such as mountain road pull outs, rural residential areas, and oil field pads. Exposure to lead ammunition via ingestion of spent ammunition fragments embedded in carcasses is the primary risk factor for lead poisoning in California Condors (e.g., Finkelstein et al. 2012), but our results also suggest that ingestion of lead ammunition–related trash may also be an important, albeit much less frequent, source of lead exposure. Thus, our findings suggest that trash ingestion is not a significant contributor to the epidemic lead poisoning rates observed in California Condors (Finkelstein et al. 2012), but ingestion of ammunition-related trash could be of concern and efforts to minimize a condor’s exposure to ammunition-related trash are warranted. We thank R. Franks, E. Hiolski, G. Kouklis, Z. Kuspa, and the US Fish and Wildlife Condor Recovery Program for their contribution to this work. Special thanks to J. Hamber at the Santa Barbara Museum of Natural History for assistance with sample storage and sorting and J. Nores and C. Babich for verification of trash items as ammunition related or not. The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the US Fish and Wildlife Service (USFWS). This project was supported by the USFWS Endangered Species Cooperative Conservation Fund, Santa Barbara Zoo, Zoos and Aquariums Committing to Conservation, Santa Barbara Auto Group and Land Rover of Santa Barbara, and the San Diego Zoo Global. None of the funders of this research had any influence on the content of the submitted or published manuscript, and none of the funders required approval of the final manuscript to be published.

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SUPPLEMENTARY MATERIAL

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Submitted for publication 24 October 2014. Accepted 28 March 2015.