Abstract

Waterfowl managers first recognized the problem of lead poisoning in ducks from the ingestion of spent lead shot (pellets) over 100 years ago. The phaseout of lead shot for waterfowl hunting began in the Atlantic Flyway in the 1970s. Lead shot was subsequently banned throughout the United States and Canada prior to 2000. We compared blood lead levels in American black ducks Anas rubripes wintering in coastal New Jersey in 1978, prior to the lead ban, and in 2017, about 39 years after lead shot was first banned for use in Atlantic coastal marshes and 27 years after it was banned for waterfowl hunting in New Jersey. The prevalence of blood lead >0.2 ppm, a level commonly used to indicate lead exposure, declined nearly fourfold from 1978 (79%) to 2017 (20%). We found no significant differences in the prevalence of birds with blood lead levels >0.2 ppm between sexes in either year or between age classes in 2017. The prevalence of ducks with blood lead levels >1.0 ppm, considered clinically evident toxicity, declined from 19% in 1978 to 1% in 2017. Our study provides further evidence that the ban on the use of lead shot over 20 years ago throughout North America has resulted in lower blood lead levels in waterfowl. Notwithstanding, we still found evidence of lead exposure in black ducks in 2017, which warrants further investigation.

Introduction

Lead poisoning in waterfowl from ingestion of lead shot (pellets) along with grit and food has been an issue in the United States as far back as the late 1870s (Bellrose 1959; Beyer et al.1998; Stevenson et al. 2005; Pain et al. 2009; Kanstrup et al. 2019). A study conducted by the Illinois Natural History Survey in 1959 concluded that approximately 2% to 3% of the North American waterfowl population died annually from lead toxicity during 1938–1954 (Stevenson et al. 2005). In response to increasing mortality caused by lead poisoning in waterfowl and predatory birds, particularly bald eagles Haliaeetus leucocephalus, the U.S. Fish and Wildlife Service issued a nationwide lead ammunition ban for waterfowl hunting in 1991 (Friend 2009). Canada implemented a complete ban of all lead ammunition use near wetlands in 1999 (Avery and Watson 2009). By 2009, 29 countries had issued bans on lead ammunition for hunting (Lahner and Franson 2009). Following the lead ban, several studies have shown significant declines in the prevalence of blood lead in waterfowl (Anderson et al. 1987; Anderson et al. 2000; Samuel and Bowers 2000).

Waterfowl hunting continues to be common in Atlantic coastal marshes in New Jersey, where nearly all marshes are public land open to hunting. The number of waterfowl hunters in New Jersey peaked in the 1970s with 25 500 active hunters annually (Serie and Raftovich 2003). Beginning in 1976, the U.S. Department of the Interior phased in steel shot zones in key waterfowl wintering areas of the United States (U.S. Department of the Interior 1976), including coastal Atlantic County, New Jersey, a core wintering area for American black ducks Anas rubripes (hereafter, black duck) in the Atlantic Flyway. Federally mandated, plus state-imposed, steel shot zones were expanded through the state up until 1990 when nontoxic shot was required for all waterfowl hunting in New Jersey. In addition, New Jersey has a rich rail hunting tradition (Dunne 1997). Both clapper rail Rallus crepitans and sora rail Porzana carolina hunting occurs during September and October prior to the waterfowl season. Although Federal regulations allowed the use of lead ammunition for rail hunting prior to the waterfowl season, New Jersey implemented a nontoxic shot requirement for all rail hunting beginning in 2004. This essentially eliminated all sources of lead shot deposition from hunting in tidal marshes in the state.

Investigators have used several techniques to document lead exposure in waterfowl, with the presence of ingested shot, collected mostly from waterfowl hunting specimens, being the most common method (Bellrose 1959; Sanderson and Bellrose 1986). Although lead exposure estimation by counting ingested shot is a cost-effective technique, authors have acknowledged the possible bias introduced, since birds weakened by ingested shot might be more vulnerable to hunting (Bellrose 1959; Sanderson and Bellrose 1986; DeStefano et al. 1995). Blood lead levels from live-captured waterfowl are a better metric of exposure to the amount of lead absorbed, since these levels have been correlated to various physiological effects (Anderson and Havera 1985). Pain (1996) and Friend et al. (2009) provided guidance for interpreting background, elevated, and clinically toxic levels of lead in tissues and blood of waterfowl based on a review of laboratory and field investigations. They defined blood lead levels <0.2 ppm as background, levels between 0.2 and 0.5 ppm as elevated, and levels >1.0 ppm as clinical toxicity.

Black ducks have been a species of conservation concern since population declines began in the 1950s (Rusch et al. 1989; Conroy et al. 2002). New Jersey remains a key wintering area for black ducks, annually wintering 92 000 birds or about 42% of the black ducks in the U.S. portion of the Atlantic Flyway during 1995–2015 (Roberts 2017). Our objective in this study was to compare black duck blood lead levels in New Jersey from 1978, prior to the lead ammunition ban for use in waterfowl hunting, to contemporary (2017) blood lead levels following nearly 40-y and 20-y periods of nontoxic shot requirements in coastal New Jersey and North America, respectively.

Study site

Wintering black ducks occur throughout New Jersey, but are most abundant in tidal marshes of the Atlantic Coast and Delaware Bay. Atlantic Coast tidal marshes span 150 km from Manasquan to Cape May and are about 5 km wide, contained between the upland edge on the mainland and narrow, mostly developed, barrier islands. Coastal salt marshes are an interspersion of shallow tidal bays, creeks, and mudflats dominated by cord grass Spartina alterniflora and salt hay S. patens, but also include patches of other graminoids and forbs (Tiner 1985) on deep organic and coastal plain sandy soils. Salinities are 20–30 ppt, with a tidal amplitude of 1.3 m (Tiner 1985).

We captured black ducks in Cape May County, New Jersey, at four locations in 1978, spanning 30 km of coastal marshes, and one location in 2017, 7 km inland at Hanson Sand Pit (hereafter Hanson) (Figure 1). Hanson was a relatively sterile, 75-ha freshwater pond resulting from groundwater filling a surface sand-mining operation that had been out of operation for 10 y. It had steep banks and was mostly >8 m deep, providing almost no foraging habitat for dabbling ducks. Since Hanson was closed to hunting and all public access, black ducks used it as a refugium from hunting and other disturbance. We began operating Hanson as a winter banding station in 2014 and, during the 3 y preceding this study, we generally observed 2 000–7 000 black ducks using the site daily. Black ducks consistently left Hanson at dusk on a daily basis, generally flying to the east presumably to forage in nearby coastal marshes, with the birds returning at dawn. Sampling locations from 1978 were 7 km east to 30 km south of Hanson (Figure 1).

Figure 1.

American black duck Anas rubripes blood-lead sampling locations in Cape May County, New Jersey, USA, 1978 and 2017.

Figure 1.

American black duck Anas rubripes blood-lead sampling locations in Cape May County, New Jersey, USA, 1978 and 2017.

Methods

Sample collection

From 3–6 February 1978, we captured 176 black ducks in welded wire, walk-in traps, baited with whole corn that were set in marshes adjacent to groundwater-fed tidal creeks (North American Banding Council 2017). We trapped birds using four trapping stations (Figure 1) at Jarvis Sound (n = 31), Townsend-Stites (n = 3), Corson-Ludlam (n = 79), and Great Sound (n = 63). We collected blood from all specimens and determined sex by cloacal exam for all but one specimen, but we did not determine age. From 14–19 January 2017, we captured 80 black ducks at Hanson with a rocket net (Dill and Thornsberry 1950) on the shoreline using cracked corn for bait. We determined the sex of ducks by cloacal exam and age as second-year or after-second-year using wing feather criteria (Ashley et al. 2006). We then collected a 0.75–1.0-mL blood sample from the ulnar vein of each bird using a sterile 22-gauge, 2.54-cm heparinized needle attached to a 3-mL sterile syringe. We immediately transferred the blood to sterile EDTA vacutainers, gently inverted them 8–10 times for thorough mixing, and stored the samples in an insulated cooler with ice packs prior to refrigeration.

Blood lead analysis

In 1978, researchers at the Rutgers Medical School (Newark, NJ) analyzed samples by using flame atomic absorption spectrometry Delves cup method, as described by Delves and Campbell (1988). Researchers at the University of Pennsylvania Toxicological Laboratory (New Bolton Center, Kennett Square, PA) analyzed the 2017 samples for total blood lead analysis using a Nexion MS 300 D inductively coupled plasma source mass spectrometer (Perkin Elmer, Shelton, CT) using the following methodology. They prepared a calibration blank and lead standards (SCP Science, Champlain, NY) in 2% nitric acid using concentrated nitric acid (Fisher Scientific, Fair Lawn, NJ) and performed all dilutions using in-house Millipore (EMD Millipore Corporation, Billerica, MA) deionized water with conductivity ≥18 MΩ. The researchers then placed a 0.5-g aliquot of each sample into a Teflon PFA vial (Savillex Eden Prairie, MN) and digested the sample with 1 mL of concentrated nitric acid overnight in a 70°C oven. At the end of the digestion period, they cooled the samples to room temperature and diluted them with Millipore deionized water to a final volume of 5.0 mL after addition of the internal standard at the final concentration of 20 ppb (159 terbium). They reported all lead concentrations in parts per million. The method detection limit for blood samples was 0.01 ppm.

Statistical analysis

Following Friend et al. (2009), we assumed that blood lead values >0.2 ppm were indicative of exposure above normal background levels and considered birds with values >1.0 ppm to have clinically evident toxicity. We organized the data using Microsoft Excel and conducted analyses using Stata 12.1 (Data S1, Supplemental Material). To determine if there was a difference between the four 1978 sampling sites, we compared the prevalence of blood lead >0.2 ppm and >1.0 ppm between sites using a χ2 test. We found no significant difference (P > 0.05), so we pooled the 1978 data (before ban) and compared the prevalence of blood lead >0.2 ppm and >1.0 ppm to 2017 data (after ban) using a χ2 statistic. We also calculated the prevalence of birds with blood lead levels >0.2 ppm for both sexes (in both years) and age classes (2017 only) and used a logistic regression model to determine if significant differences occurred between sexes in both sampling years and between age classes in 2017. We also calculated an overall prevalence for blood lead levels >1.0 ppm for both years. Due to the testing method, 1978 samples had blood lead levels truncated at 1.0 ppm for values that were potentially >1.0 ppm. We therefore substituted a value of 1.0 ppm for 1978 values that were potentially >1.0 ppm when calculating means.

Results

Blood lead levels >0.2 ppm declined from 79% in 1978 to 20% in 2017. We found a significant difference (χ2 = 80.09; P ≤ 0.05) in the prevalence of ducks with blood lead levels >0.2 ppm between sampling periods (Figure 2). For the 1978 samples, there was no significant difference (P = 0.966) in the proportion of males (79%) with blood lead levels >0.2 ppm compared with females (79%). We observed a similar result in 2017, with no significant difference (P = 0.058) in the proportion of males (27%) with blood lead levels >0.2 ppm compared with females (9%) (Table 1). In addition, we found no significant difference (P = 0.355) in the proportion of birds with blood lead levels >0.2 ppm between second-year (25%) and after-second-year (17%) birds (Table 1). Blood lead levels >1.0 ppm declined from 19% in 1978 to 1% in 2017 (Table 1). We found a significant difference (χ2 = 14.63; P ≤ 0.05) in the prevalence of ducks with blood lead levels >1.0 ppm between sampling periods.

Figure 2.

Blood lead levels (ppm) for individual American black duck Anas rubripes specimens sampled in Cape May County, New Jersey, USA, 1978 and 2017.

Figure 2.

Blood lead levels (ppm) for individual American black duck Anas rubripes specimens sampled in Cape May County, New Jersey, USA, 1978 and 2017.

Table 1.

Total samples (n), number of males and females with blood lead levels >0.2 ppm (No./n), blood lead prevalence (pooled ages and sexes; %) at >0.2 ppm and >1.0 ppm, number of juvenile (SY) and adult (ASY) birds with blood lead levels >0.2 ppm (No./n), mean, standard error (SE), and range of blood lead levels (ppm) in American black ducks Anas rubripes in Cape May County, New Jersey, USA, 1978 and 2017.

Total samples (n), number of males and females with blood lead levels >0.2 ppm (No./n), blood lead prevalence (pooled ages and sexes; %) at >0.2 ppm and >1.0 ppm, number of juvenile (SY) and adult (ASY) birds with blood lead levels >0.2 ppm (No./n), mean, standard error (SE), and range of blood lead levels (ppm) in American black ducks Anas rubripes in Cape May County, New Jersey, USA, 1978 and 2017.
Total samples (n), number of males and females with blood lead levels >0.2 ppm (No./n), blood lead prevalence (pooled ages and sexes; %) at >0.2 ppm and >1.0 ppm, number of juvenile (SY) and adult (ASY) birds with blood lead levels >0.2 ppm (No./n), mean, standard error (SE), and range of blood lead levels (ppm) in American black ducks Anas rubripes in Cape May County, New Jersey, USA, 1978 and 2017.

Discussion

We found a decline in blood lead levels in black ducks following the ban on lead shot for waterfowl hunting that is consistent with other studies. Samuel and Bowers (2000) found a 44% decline in black duck blood lead levels in Tennessee less than a decade after the lead shot ban in the United States, although they found the reduction was more pronounced in adults than in juveniles. Samuel et al. (1992) also found that adults had a higher prevalence of blood lead >0.2 ppm than juveniles. We did not detect a difference in blood lead levels by age based on 2017 data, which may have been due to the small sample size. Also, similar to findings by Samuel et al. (1992) and Samuel and Bowers (2000), we did not find a difference in blood lead levels between sexes.

Although we used different analytical methods between the two study years, both methods have been commonly used to measure blood lead. The inductively coupled plasma source mass spectrometer (0.1 μg/dL), however, has a significantly improved detection limit compared with the Delves cup flame atomic absorption spectrometry method (10 μg/dL) (WHO 2011). Delves and Campbell (1988) found excellent agreement between the flame atomic absorption spectrometry and inductively coupled plasma source mass spectrometer methods (r = 0.994, where r = 1 would mean 100% agreement). Therefore, we believe that the results from the two sampling years can be confidently compared.

Although the study sites between 1978 and 2017 were not identical, we believe black ducks sampled at these sites represented the same population of birds wintering in the tidal marshes of Cape May County, New Jersey, between years. Black ducks are known to prefer habitats free from disturbance (Morton et al. 1989a; Longcore et al. 2000) similar to the 2017 Hanson study site. Several studies (Albright et al. 1983; Conroy et al. 1986; Morton et al. 1989a, 1989b) have reported nocturnal flights by black ducks from refugia to feeding areas, similar to what we observed at Hanson. Jones et al. (2014) found that wintering black ducks in coastal New Jersey spent more time foraging during the nocturnal period than during the diurnal period, further supporting this phenomenon. In addition, Ringelman et al. (2015) determined the mean home ranges of 181 black ducks wintering in five Atlantic Flyway states, including New Jersey, to be 1 082 ± 120 ha. Tidal marsh was the only habitat type surrounding (e.g., within 10 km) Hanson that could sustain the thousands of black ducks that used Hanson, since remaining areas were predominantly forest or human development. Legagneux et al. (2009) found that roosting or loafing areas were frequently on the edge of ducks' home range, and several studies have found that dabbling ducks travel >10 km from roosting to feeding sites (Jorde et al. 1983; Cox and Afton 1996). Presuming that black ducks at Hanson also fit these patterns, then these birds would be expected to move to the coastal tidal marsh to forage, overlapping several of the 1978 study sites. During other banding operations in the 2010s, we commonly recaptured live black ducks during the same month in wire traps at nearby (∼7 km) coastal marshes (e.g., near the Corson-Ludlam 1978 site) that had been banded at Hanson, providing further evidence that these birds moved to at least one of the 1978 study areas to forage (T.C. Nichols, personal observation). There is always uncertainty in the origin of blood lead in migratory ducks sampled in wintering areas. However, Ringelman et al. (2018) found that peak black duck arrival at Forsythe National Wildlife Refuge in New Jersey (40 km north of our study area) was in mid-December. Given that black ducks in our study were sampled in mid-January and February and that lead remains in blood for about 45 d after exposure (Franson et al. 1986), it is likely that the majority of black ducks we tested were exposed to lead in or near our study area.

We were encouraged that lead exposure had declined significantly in black ducks since the 1970s; however, the lead levels found in 2017 were still cause for concern. Although several studies suggest that bait-trapped birds may have a sampling or poor-condition bias (Weatherhead and Ankney 1984; Wheeler and Gates 1999), the 2017 lead levels in the black ducks we examined (20% prevalence > 0.2 ppm) were more than three times higher than the level seen in black ducks in Tennessee (6.5% prevalence > 0.2 ppm) in the late 1990s (Samuel and Bowers 2000), which implies that there are still sources of lead in the local environment.

Many studies have examined lead isotopes to determine the source of lead in the environment (Behmke et al. 2015; Sriram et al. 2018; Arrondo et al. 2020; Gorski et al. 2021). Investigating lead isotopes in our samples to determine the potential sources of lead was beyond the scope of our study. However, given our results of continued lead exposure, determining the source of lead contamination in New Jersey through evaluation of lead isotopes warrants further consideration. Stevenson et al. (2005) suggested three main reasons for continued lead exposure in waterfowl, including 1) some noncompliance with nontoxic shot regulations, 2) remaining lead shot in the environment from decades ago are still available for ingestion by waterfowl, and 3) other sources of environmental lead present, including mining and smelting operations and lead fishing tackle.

Noncompliance is unlikely to be a concern in New Jersey coastal marshes. The transition from lead shot to steel shot between 1970 and 1980 was initially contentious (Sanderson and Bellrose 1986; Anderson and Havera 1989); however, the requirement to use nontoxic shot for waterfowl hunting in contemporary times is generally accepted, and compliance is high (Havera et al. 1994). The reason for this is likely due to hunter demographics. During the early 2010s, the mean age of New Jersey migratory bird hunters was 40 y (Nichols and Clark 2017). Assuming these individuals began hunting at age 15 y, most New Jersey waterfowl hunters have pursued ducks with nontoxic shot during their entire hunting careers.

Several studies have found that lead shot can persist in the environment for decades (Flint 1998; Flint and Schamber 2010; Kanstrup et al. 2020). In Denmark, Kanstrup et al. (2020) found similar amounts of lead shot in the environment 33 y after the lead shot ban in 1986. Further, Kanstrup et al. (2020) suggested that lead can remain for hundreds to even tens of thousands of years in sediment. Given the popularity of waterfowl hunting in New Jersey prior to the lead shot ban, the amount and distribution of remaining lead shot in local salt marshes is worth further study.

There are other potential sources that may explain the lead levels we observed in the 2017 samples. Our study area did not have mining and smelting activities that could contribute to elevated lead levels. However, an additional source could come from lost lead fishing tackle (Pokras et al. 1992; Grade et al. 2018; Grade et al. 2019). More than 30 avian species have been documented to ingest lead fishing tackle (Grade et al. 2019). Pokras et al. (1992) found ingestion of lead fishing sinkers in New England to be the leading cause of mortality in the common loon Gavia immer. Saltwater fishing in back bays and marshes in our study area is extremely popular, and New Jersey did not have any regulations prohibiting lead fishing weights or tackle, suggesting lost tackle could be an important source of lead contamination and, therefore, would be an important area to examine in future studies.

Supplemental Material

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.

Data S1. All data used for the analysis are contained in the attached comma delineated file (Data S1.csv) and includes age class, sex, location, weight, and blood lead levels for all American black ducks Anas rubripes sampled in 1978 and 2017.

Found at DOI: https://doi.org/10.3996/FWM-20-044.S1 (14 KB CSV).

Reference S1. Conroy MJ, Costanzo GR, Stotts DB. 1986. Winter movements of American black ducks in relation to natural and impounded wetlands in New Jersey. Pages 31–45 in Whitman WR, Meredith WH, editors. Waterfowl and wetlands symposium: proceedings of a symposium on waterfowl and wetlands management in the coastal zone of the Atlantic Flyway. [unpublished]. Located at Dover, Delaware: Delaware Department of Natural Resources and Environmental Control.

Found at DOI: https://doi.org/10.3996/JFWM-20-044.S2 (923 KB PDF).

Reference S2. Lahner LL, Franson JC. 2009. Lead poisoning in wild birds. Madison, Wisconsin: U.S. Geological Society National Wildlife Health Center. Fact Sheet 2009-3051.

Found at DOI: https://doi.org/10.3996/JFWM-20-044.S3 (1.39 MB PDF); also available at https://pubs.usgs.gov/fs/2009/3051.

Reference S3.North American Banding Council. 2017. The North American Banders' manual for waterfowl (Family–Anatidae). Laurel, Maryland: U.S. Fish and Wildlife Service, Patuxent Wildlife Research Center.

Found at DOI: https://doi.org/10.3996/JFWM-20-044.S4 (2.82 MB PDF); also available at http://www.nabanding.net/wp-content/uploads/2012/04/North-American-Banders-Manual-for-Waterfowl.pdf.

Reference S4. Roberts AJ. 2017. Waterfowl harvest and population survey data. Laurel, Maryland: U.S. Fish and Wildlife Service, Division of Migratory Bird Management, U.S. Department of Interior.

Found at DOI: https://doi.org/10.3996/JFWM-20-044.S5 (2.77 MB PDF); also available at https://www.fws.gov/migratorybirds/pdf/surveys-and-data/DataBooks/AtlanticFlywayDatabook.pdf.

Reference S5. Sanderson GC, Bellrose FC. 1986. A review of the problem of lead poisoning in waterfowl. Illinois Natural History Survey, Special Publication 4. Champaign, Illinois: Illinois Natural History Survey.

Found at DOI: https://doi.org/10.3996/JFWM-20-044.S6 (2.7 MB PDF).

Reference S6. Serie J, Raftovich R. 2003. Final compilation estimates of harvest, hunter activity, and success based on the U.S. Fish and Wildlife Service's mail questionnaire survey, 1961–2001. Laurel, Maryland: U.S. Fish and Wildlife Service, Division of Migratory Bird Management, U.S. Department of Interior.

Found at DOI: https://doi.org/10.3996/JFWM-20-044.S7 (426 KB PDF).

Reference S7. Tiner RW. 1985. Wetlands of New Jersey. Pages 54–79 in U.S. Fish and Wildlife Service, National Wetlands Inventory. Newton Corner, Massachusetts: USFWS.

Found at DOI: https://doi.org/10.3996/JFWM-20-044.S8 (9.86 MB PDF); also available at https://www.fws.gov/wetlands/Documents/Wetlands-of-New-Jersey.pdf.

Reference S8.U.S. Department of the Interior. 1976. Final environmental assessment. Proposed use of steel shot for hunting waterfowl in the United States. Washington, DC: U.S. Fish Wildlife Service.

Found at DOI: https://doi.org/10.3996/JFWM-20-044.S9 (15.74 MB PDF).

Reference S9.World Health Organization. 2011. Brief guide to analytical methods for measuring lead in blood. Geneva: WHO.

Found at DOI: https://doi.org/10.3996/JFWM-20-044.S10 (201 KB PDF); also available at https://www.who.int/ipcs/assessment/public_health/lead_blood.pdf?ua=1.

Acknowledgments

We thank former biologists, particularly L. Widjeskog and F. Ferrigno who collected data in 1978 and former wildlife toxicologist W. Stansley for his insight into the 1978 testing protocol. A. Damminger produced Figure 1. We thank the reviewers for providing comments to improve this manuscript. Funding was provided by the Wildlife and Sportfish Restoration Funds FW-69-R and W-68-R and the New Jersey Division of Fish and Wildlife Hunter and Angler Fund.

Any use of trade, product, website, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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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: Lewis NL, Nichols TC, Lilley C, Roscoe DE, Lovy J. 2021. Blood lead declines in wintering American black ducks in New Jersey following the lead shot ban. Journal of Fish and Wildlife Management 12(1):174–182; e1944-687X. https://doi.org/10.3996/JFWM-20-044

Supplementary data