Abstract

Despite the known deleterious effects lead exposure can have on humans, lead remains the most common type of ammunition used to harvest big game and upland game birds. We sampled wild turkey Meleagris gallopavo breast muscle shot with standard lead and copper-plated lead pellets to quantify lead residue concentrations within the wound channel, and we sampled multiple adjacent locations to measure the extent lead contamination spreads through tissue of harvested turkeys. We found that samples taken from the wound channel contained more lead (mean = 3.76 μg/g dry weight) than both samples taken adjacent to the wound channel (mean = 0.20 μg/g dry weight) and samples taken from >5 cm away (mean = 0.15 μg/g dry weight). Additionally, we found that birds harvested with standard lead ammunition did not differ in lead concentrations from those shot with copper-plated lead, suggesting that copper plating does not aid in reducing lead exposure. Our findings suggest that wild turkeys harvested with either lead or copper-plated lead shot have the potential to expose consumers, especially children due to their lower tolerance, to low levels of lead that could exceed daily consumption limits set by the Food and Drug Administration and Centers for Disease Control. However, elevated lead levels were confined to the wound channel, and thus proper preparation of game to remove tissue surrounding wound channels may eliminate or substantially reduce lead exposure from harvested game birds.

Introduction

Exposure to lead can pose a substantial risk to human and wildlife health (Campbell et al. 2005). Lead poisoning in adults can lead to increased blood pressure, decreased kidney function, and reproductive problems (EPA 2019). Elevated blood lead levels in young adults are also associated with increased odds of major depression and panic disorders (Bouchard et al. 2009). While lead is toxic to all age groups, children and pregnant women are especially susceptible to the detrimental effects of lead exposure, as blood lead levels as low as 10 μg/dL negatively affect IQ and cognitive development of children (Lanphear et al. 2005). Because of these deleterious effects, over the past 35 years, the Centers for Disease Control has decreased the maximum acceptable blood lead levels in children from 25 to 5 μg/dL (Roper et al. 1991; Baghurst et al. 1992). Hunters can be exposed to lead by consuming meat that has been contaminated with fragments from ammunition that has passed through consumable tissues during harvest (Hunt et al. 2009; Tsuji et al. 2009; Knott et al. 2010; Lindboe et al. 2012); however, more studies are needed to understand the amount of lead contamination found in hunter-harvested animals, especially birds.

Despite the known toxicity of lead, its use in ammunition has been widespread in the harvest of game. Bullets and slugs are the predominant ammunition for large game, whereas shotgun pellets are used for upland small game. Once in the environment, spent lead ammunition can have detrimental effects on wildlife that directly or indirectly consume lead fragments or pellets (Cade 2007; Craighead and Bedrosian 2008; Neumann 2009; Cruz-Martinez et al. 2012). Avian scavengers such as eagles Accipitridae spp. and vultures Cathartidae spp. are particularly susceptible to lead exposure due to consumption of offal piles containing lead bullet fragments or unrecovered carcasses (Kelly and Johnson 2011; Bedrosian et al. 2012; Cruz-Martinez et al. 2012). Waterfowl and other aquatic species are also susceptible to lead toxicosis, particularly from the ingestion of spent shot while foraging in the sediment of hunted wetlands, which led to waterfowl die-offs as early as in the 1940s (Jordan and Bellrose 1951; Olney 1960). In fact, an estimated 1.6–2.4 million waterfowl died annually from lead poisoning in the United States, before the use of lead shot was prohibited for waterfowl harvest in 1991 (Degernes 2008; Avery and Watson 2009).

Not only is spent shot a risk to wildlife, animals shot with lead ammunition may also act as vectors of exposure to human consumers. While most hunters avoid consuming lead pellets found in the muscle tissue of harvested birds, the pellets can fragment into smaller pieces and also leave behind a fine powder that may escape detection (Frank 1986). Fragments of lead bullets travel as far as 45 cm from the wound channel (Hunt et al. 2006; Cruz-Martinez et al. 2015). Fragmentation of lead ammunition is not limited to just big game and rifle bullets, as Pain et al. (2010) found shotgun pellet fragments in the carcasses of harvested game birds. Their study, along with others, found elevated lead levels in the breast muscle of birds harvested with lead-based ammunition (Johansen et al. 2001; Johansen et al. 2004; Pain et al. 2010). While no longer allowed in the hunting of waterfowl, lead-based shot is still commonly used for upland game species, such as mourning dove Zenaida macroura, ring-neck pheasant Phasianus colchicus, and wild turkey Meleagris gallopavo; thus, hunters may still be exposed to lead through consumption of these species. In fact, a study by Iqbal et al. (2009) investigated the difference in blood lead levels between consumers and nonconsumers of game meat. While none of the blood lead levels found exceeded the Centers for Disease Control and Prevention level of concern, consumers of wild game meat had blood lead levels of 0.30 μg/dl higher than people who did not consume wild game (95% confidence interval 0.16–0.44).

Efforts have been made to limit hunter exposure to lead via the production of “nontoxic” ammunition. Metals such as steel, nickel, and copper are used in place of lead or to coat lead pellets, but widespread acceptance of these alternatives has been challenging due to hunter concerns over price and efficacy of lead-free ammunition (Schulz et al. 2007). Although lead pellets coated with copper or other metals are often marketed for increased performance rather than as a nontoxic substitute for lead ammunition, they also have the potential to reduce lead exposure in consumers of harvested game. However, to our knowledge there have been no published studies investigating the effectiveness of nontoxic coatings of lead pellets at reducing lead contamination in the muscle of harvested game.

Our objective was to test the efficacy of copper-plated shot at reducing lead contamination in muscle tissue. Using wild turkeys (hereafter “turkeys”) as a model species, we tested the hypothesis that lead contamination would vary by shot type and predicted that higher levels of lead residues would be detected in turkeys shot with standard lead shot than in turkeys harvested with copper-plated lead ammunition; however, we predicted that elevated lead levels would be limited to the wound channel and not to the adjacent muscle tissue. We also compared observed lead contamination levels to Environmental Protection Agency standards to understand risks with using both types of ammunition. As copper can also be toxic when consumed at high doses, we also tested copper concentrations in the muscle samples of birds harvested with copper-plated lead shot to determine if copper levels exceeded Environmental Protection Agency thresholds.

Study Area

We harvested all turkeys on the Savannah River Site (SRS), a ∼78 000-ha tract of land owned by the U.S. Department of Energy. The SRS is located in the upper Atlantic Coastal Plain in South Carolina; the Savannah River forms its western border. The site was created in 1951, transforming the ∼40 000 ha of agricultural fields into slash Pinus elliottii, loblolly P. taeda, and longleaf pine P. palustris forests (White and Gaines 2000). In addition to these planted pines, oak Quercus spp. forests border most riparian areas, and bald cypress–water tupelo Taxodium distichumNyssa aquatica swamps are scattered throughout the site.

The SRS has a history of radionuclide and trace element contamination release into the surrounding environment due to anthropogenic activities. While wildlife inhabiting the site have been found to contain elevated concentrations of many of these contaminants, elevated lead concentrations have not been found in any of the biota inhabiting the site (Burger et al. 2002; Oldenkamp et al. 2017; Borchert et al. 2019). Thus, we have no reason to believe the contaminants on site would have any effect on our results.

Methods

Sample collection

We harvested male wild turkeys on the SRS during the spring of 2018, with both standard lead and copper-plated lead pellets. We used size five shot for both ammunition types to standardize variation in lead concentration due to pellet size. We shot all birds twice, first in the head/neck area to ensure rapid euthanasia and second, into the middle of the body from ∼20 m away within 30 s of the first shot to ensure multiple pellets impacted the breast muscle. While this second shot is not common among turkey hunters, because of the wide spread of shotgun patterns, it is common for multiple pellets to impact the breast muscle of turkeys during the first shot aimed at the head/neck area. After harvest, we placed each bird in a freezer until we could take samples. To facilitate sample collection, we thawed each bird for 1–2 d at 5°C and partially skinned it to reveal the breast muscle. Once a pellet wound was located, we extracted a muscle plug centered on the wound channel using a 1.25-cm diameter piece of stainless steel conduit, resulting in a ∼5-cm long cylinder of muscle tissue. We extracted a second sample immediately adjacent to the wound channel sample and a reference sample from at least 5 cm from any sign of a pellet wound. We took two to three wound channel and adjacent samples from each turkey as well as two references samples. We removed all pellets detected in each sample during processing. We thoroughly cleaned conduit pieces between uses and stored samples in separate Whirl Paks (Nasco, Janesville, WI) to prevent cross-contamination.

Sample analysis.

We conducted trace element analysis on muscle samples to determine lead and copper concentrations. We weighed the samples, freeze-dried them, and then weighed the samples again to calculate moisture content. We subsequently ground and homogenized the samples into a powder. We then microwave digested 250 mg of the dry, homogenized tissue (MARSX Xpress, CEM Corporation, Matthews, NC) with 10 ml of trace metal-grade nitric acid (70% HNO3). Following digestion, we diluted samples with 5 ml of Milli-Q water (18 MΩ; Millipore, Billerica, MA). As a final step, we further diluted the sample 1:10 by taking 1 ml of the digested sample and diluting it in 9 ml of Milli-Q water before analysis with inductively coupled plasma mass spectroscopy (Nexlon 300X ICP-MS; Perkin Elmer, Norwalk, CT). Every 20 samples, we included at least 1 sample of certified reference material (TORT-3 lobster hepatopancreas; National Research Council, Ottawa, ON) and a sample duplicate as a quality check. Percent recoveries ranged from 96 to 116%. For analyses, we used values of estimated lead concentration (micrograms per gram) provided by these procedures. However, for values not exceeding the minimum detectable limit (MDL) for lead (0.065 μg/g), we set the concentration value to 50% of the MDL (∼0.033 μg/g). All copper concentrations were above the MDL for copper (0.057 μg/g).

Statistical analysis

We compared lead concentrations (dry weight) taken from the wound channel of turkeys shot with standard lead pellets to those shot with copper-plated lead pellets (Table S1, Supplemental Material). We also compared copper concentrations (dry weight) between breast sample locations for birds shot with copper-plated lead pellets. We tested lead concentrations for normality using the Shapiro–Wilks test and subsequently log transformed the data. Due to numerous concentrations below the MDL, we conducted a censored regression using the censReg function in R to test for differences in lead concentration between shot type and sample location (Helsel 2012; Tisdale et al. 2020). For copper concentrations, we conducted an analysis of variance using linear mixed-effects models with the “lme” function in the nlme package in R to explore differences in lead levels between turkeys shot with each shot type. To calculate degrees of freedom for each test, we used the Welch–Satterthwaite method. In addition, we used the “multcomp” package to determine whether any differences in copper concentrations existed between sample locations. We used mixed-effect models to allow for the random effect of bird identity because multiple tissue samples at each location were taken from each bird.

Results

We harvested 17 male wild turkeys from the SRS, 9 of which were shot with copper-plated lead pellets, and the remaining 8 were shot with standard lead pellets. We sampled two to three wound channels as well as an adjacent sample for every wound channel sample and two reference samples from each bird. Lead concentrations were below the MDL for ≥50% of reference and adjacent samples for both shot types, whereas 29% of wound channel samples were below the MDL for copper-plated shot, and only 8% of wound channel samples were below the MDL for turkeys shot with standard lead pellets. Given the large proportion of samples in the adjacent and reference locations with concentrations below the MDL, we tested for differences between the wound channel and the pooled reference and adjacent locations but not between the adjacent and reference locations.

Lead concentrations in the wound channels of turkeys harvested with copper-plated lead shot did not differ from lead concentrations in wound channels caused by standard lead shot (t = −0.131, df = 3, P = 0.90; Figure 1). Hence, we pooled both shot types together for further analyses. Using these combined data, we found a difference in lead concentration between locations (t = −6.45, df = 3, P < 0.001), where tissue inside the wound channel contained greater lead concentrations than both the adjacent and reference locations. All samples taken from birds shot with copper-plated lead pellets had copper concentrations greater than the MDL for copper. Due to budget constraints, we did not test the turkeys harvested with standard lead shot for copper concentrations. Our linear mixed-effects model analysis revealed a difference in copper concentration between sampling locations (F2,54 = 17.79, P < 0.001; Figure 2). Post hoc analysis revealed that the wound channel location contained greater copper concentrations than both the adjacent and reference locations but that copper concentrations did not differ between the adjacent and reference sample locations.

As shown by the standard deviations, lead and copper levels tended to be highly variable, even within locations. Also, due to the skewed nature of the data and outliers within the dataset, the means were skewed toward larger averages (Tables 1 and 2). As such, we used the proportion of wound channel samples that exceeded consumption limits set by the Food and Drug Administration and Centers for Disease Control for addressing consumer risk.

Discussion

We found that lead concentrations did not differ between shot types and were largely confined within the wound channel. None of the samples collected outside of the wound channel exceeded consumption limits set by the Food and Drug Administration and Centers for Disease Control for adults (12.5 μg/d), and only 2.2% of samples (1 of 46) that we collected immediately adjacent to the wound channel exceeded the daily consumption limit for children (3 μg/d); however, if not properly discarded while cleaning game, a single wound channel contained enough lead to put a child over this limit in 28.3% (13 of 46) of wound channel samples. For adults, a single wound channel exceeded their daily consumption limit in 8.7% (4 of 46) of samples. This suggests that upland game bird hunters are likely exposed to lead from lead-based ammunition, but given that most hunters only consume a low number of small game meals per year (Smith et al. 2017), average monthly or annual exposure to lead from harvested small game is likely low.

None of the samples collected in this study exceeded the reference consumption limit for copper (700 μg/d for the average adult), suggesting that copper exposure from the residue of copper-plated ammunition is minimal; however, copper-plated lead shot surprisingly did not reduce concentrations of lead in the wound channel. This indicates that the copper plating on pellets is likely not robust enough to contain the lead after being fired. In fact, following a further inspection of the pellets found during dissection of the harvested turkeys, we observed large areas of copper plating wiped clean off of the pellets. Interestingly, the wound channel samples that we harvested with copper-plated lead shot had much higher variability in lead concentration than that of the lead shot-harvested samples, including a few outliers (71.29, 22.27 μg/g). These high values suggest that small lead fragments likely were present in the sample that escaped detection during initial laboratory dissection. Due to these fragments escaping detection during a thorough dissection, it is likely that they would not have been found by hunters while preparing and cooking meat and thus could potentially be ingested by consumers. Another possible source of this lead is from the vaporization of the gunpowder upon the gun being fired. To test for this, a completely lead-free pellet type would need to be used in future studies.

Previous studies have radiographed birds harvested with various types of shot and found fragments of pellets throughout the body (Pain et al. 2010). However, in these studies, fragments were generally clustered around bone, likely due to pellets fragmenting when impacting the bone. As we were sampling the wound channel through breast muscle, we were less likely to sample the areas of increased pellet fragmentation near bones, as observed in previous studies (Pain et al. 2010).

We did not attempt to clean or cook the muscle tissue, both of which have the potential to alter lead concentrations before consumption. However, Grund et al. (2010) found that rinsing carcasses of domestic sheep Ovis aries shot with lead bullets spread the lead to other areas, making contamination harder to avoid. Also, multiple studies have found elevated levels of lead in the tissue of cooked game meat harvested with lead shot (Johansen et al. 2001; Johansen et al. 2004; Pain et al. 2010). However, these studies did not test lead levels before preparation, so it is unknown what effect cooking may have on contamination levels and requires further study. It is also important to note that we shot turkeys an additional time in the breast during harvest, which is uncommon among normal turkey-hunting practices. However, while hunters typically only shoot turkeys in the head/neck area (Keck and Langston 1992), due to the spread of a shotgun pattern (Arslan et al. 2011), multiple pellets often unintentionally impact the breast muscle tissue. Further, most other species of game birds are harvested while flying and are much smaller than wild turkeys, making it common for multiple pellets to impact the breast muscle (Burger et al. 1998; Johansen et al. 2001). Thus, lead residues in other game birds may differ from levels reported here, warranting further study. In addition, hunters use varying shot sizes to harvest game, which may influence lead residues and fragmentation rates.

Collectively, our results suggest that wild turkeys harvested with either lead or copper-plated lead shot may expose consumers to small amounts of lead, but the lead contamination does not spread extensively beyond the wound channel. This suggests that if proper precautions are taken, such as removing the muscle tissue surrounding the wound channel, most of the lead contamination can be avoided. However, given the lead concentrations we found, only one pellet passing through muscle tissue has the potential to expose consumers, especially children, to amounts of lead exceeding consumption limits due to their lower threshold. Thus, the extent of lead exposure is highly influenced by the number of pellets impacting the breast upon harvest as well as the extent to which care is taken to avoid consuming meat surrounding wound channel locations. To minimize potential lead exposure from consuming game birds harvested with lead-based ammunition, hunters need to avoid eating muscle immediately surrounding the wound channel or use nontoxic shot types.

Supplemental Materials

Please note: The Journal of Fish and Wildlife Management is not responsible for the content or functionality of any supplemental material. Queries should be directed to the corresponding author for the article.

Table S1. Raw lead and copper concentrations found in the muscle tissue of wild turkeys Meleagris gallopavo harvested on the Savannah River Site in the spring of 2019.

Found at DOI: https://doi.org/10.3996/JFWM-20-084.S1 (54 KB DOCX).

Acknowledgments

We thank A. Lindell for aiding in the processing and testing of all samples collected as well as O. Rhodes, J. Cumbee, J. Kilgo, T. Mims, M. Larsen, and M. Vukovich for aiding in the harvest of wild turkeys. We would also like to thank C. Moore and M. Chamberlain for their help in the preparation of this manuscript. We also thank the reviewers and Associate Editor for helping us improve upon this manuscript to prepare it for publication. Funding for this study was provided by the U.S. Department of Energy to the University of Georgia Research Foundation (award no. DE-EM0004391).

Disclaimer: This manuscript was prepared as an account of work sponsored by an agency of the U.S. government. Neither the U.S. government nor any agency thereof, nor any of their employees, makes any warranty, express or implied, or assumes any legal liability or responsibility for the accuracy, completeness, or usefulness of any information disclosed, or represents that its use not infringe privately owned rights. The views and opinions of the authors expressed herein do not necessarily state or reflect those of the U.S. government or any agency thereof.

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The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

Author notes

Citation: Tisdale CA, Martin JA, Beasley JC. 2021. Lead contamination differences in the muscle of wild turkeys harvested with lead and copper-plated lead shot. Journal of Fish and Wildlife Management 12(1):250–256; e1944-687X. https://doi.org/10.3996/JFWM-20-084

Supplemental Material