Environmental lead reduces the resilience of bald eagle populations
https://wildlife.onlinelibrary.wiley.com/doi/10.1002/jwmg.22177
Abstract
Bald eagles (Haliaeetus leucocephalus) are considered a recovery success in the United States after rebounding from near extirpation due to widespread use of the insecticide dichlorodiphenyltrichloroethane (DDT) in the twentieth century. Although abundances of bald eagles have increased since DDT was banned, other contaminants have remained in the environment with unknown influence on eagle population trends. Ingestion of spent lead (Pb) ammunition, the source of Pb most available to eagles and other scavengers in the United States, is known to kill individual eagles, but the influence of the contaminant on overall population dynamics remains unclear, resulting in longstanding controversy over the continued legality of the use of Pb in terrestrial hunting ammunition. We hypothesized that mortalities from the ingestion of Pb reduced the long-term growth rate and resiliency of bald eagles in the northeast United States over the last 3 decades. We used Holling’s definition of resilience (the ability of a system to absorb changes of state variables, driving variables, and parameters and still persist) to quantify how reduction in survival from Pb-associated mortalities reduced the likelihood of population persistence. We used a population matrix model and necropsy records gathered between 1990 and 2018 from a 7-state area to compare population dynamics under current versus hypothetical Pb-reduced and Pb-free scenarios. Despite a robust increase in eagle abundances in the northeast United States over that period, we estimated that deaths arising from ingestion of Pb was associated with a 4.2% (females) and 6.3% (males) reduction in the asymptotic long-term growth rate (lambda). Comparison between real (current) and counterfactual (Pb-reduced and Pb-free) population dynamics indicated that the deaths from acute Pb poisoning were additive because the mortality events were associated with marked reduction in annual survival performance of hatchlings and reproductive females. These shifts in survival performance were further associated with a reduction in resilience for hatchling (95.4%) and breeding (81.6%) female eagles. Counterintuitively, the current conditions produced an increase in resilience (68.9%) for immature and non-breeding female eagles over hypothetical Pb-free conditions, suggesting that the population of eagles in the northeast United States reorganized (in a population dynamics sense) to ensure population expansion despite additive mortalities associated with Pb. This study can be used by state and federal wildlife managers or non-governmental organizations to inform policy surrounding the use of lead ammunition or to educate hunters on the population-scale effects of their ammunition choices.
Wildlife populations face mounting threats to long-term viability from anthropogenic activities. Among these threats are environmental contaminants that can reduce overall population potential (Pain et al. 2009, Franson and Russell 2014, Bruggeman et al. 2018). While not directly lethal, a prime example is the contaminant dichlorodiphenyltrichloroethane (DDT), which severely affected wildlife populations across the United States. Before it was banned in the United States in 1972, DDT reduced the reproduction of several species of raptors and precipitated the rapid decline in populations of the iconic bald eagle (Haliaeetus leucocephalus) in the United States and Canada (Grier 1982, Elliott and Harris 2002). Bald eagles were included in the United States Endangered Species Act in 1973 (U.S. Fish and Wildlife Service [USFWS] 2007), and the species is now considered a model of Endangered Species Act success due to range-wide recovery and its formal delisting 2 decades later (USFWS 2007).
Despite the prohibition of DDT and the recovery of eagle abundances, eagles continue to succumb to environmental contaminants in the United States, including heavy metals (Katzner et al. 2018). One such contaminant is lead (Pb). Banned in the United States from paint in 1977, plumbing used for drinking water in 1986, and gasoline in 1996, Pb is still widely used in ammunition to hunt big game and predators in terrestrial habitats and in shot for small game and upland gamebirds (Kendall et al. 1996, Golden et al. 2016). In addition to unremedied relic deposits of Pb from once-legal (but now banned) anthropogenic activities (U.S. Geological Survey [USGS] 2005), Pb continues to be deposited into and remains in the environment through the practice of big game, pest, or predator hunting. A federal projectile ban to make the continued use of Pb ammunition illegal in terrestrial habitats does not currently exist (U.S. Department of the Interior [USDOI] 2017b).
Some terrestrial hunting practices involve discarding the carcass, parts, or viscera in the field for scavengers to consume (Pain et al. 2019). But Pb-based rifle bullets used for hunting expand when striking the target animal and can leave tens to hundreds of very small Pb fragments throughout the discarded tissues (Hunt et al. 2009). Indeed, the ingestion of Pb by scavenging wildlife has been reported for over a century, as have reports of mortalities of Pb toxicosis in non-target wildlife species wherever Pb ammunition is used (Rattner et al. 2008). As such, continued legal use of Pb ammunition in terrestrial habitats presents an ongoing hazard to non-target migratory birds and other scavenging species (Kendall et al. 1996, Golden et al. 2016).
Despite the Eagle Act rendering the direct take of a bald eagle illegal in the United States (USFWS 1940), veterinary records from necropsies on bald eagles collected in the wild by state wildlife agency biologists and their partners show that ingestion of discarded tissues containing spent Pb ammunition fragments is a widespread source of morbidity and mortality to eagles (Katzner et al. 2018). Ingestion of Pb fragments by wild scavenging eagles can cause acute or chronic morbidity and mortality, dependent on the quantity of Pb ingested in the contaminated tissues of the scavenged meal (Stansley and Murphy 2011, Franson and Russell 2014, Bruggeman et al. 2018). Despite the steady increase in eagle abundances in the northeast United States in recent years (USFWS 2007, Hanley et al. 2019), wildlife rehabilitators, veterinarians, and pathologists in the northeast United States continue to report eagle morbidities and mortalities from ingested Pb (Avian Haven Wild Bird Rehabilitation Center 2021, Cummings School of Veterinary Medicine 2021, University of New Hampshire 2021, USGS National Wildlife Health Center 2021, Wildlife Health Center of Virginia 2021), spawning regional and national controversy among wildlife managers, resource regulators, and the public on whether Pb ammunition should be banned outright (USDOI 2017a, b).
Population matrix models are used to link properties of individuals to population-scale processes (Tuljapurkar 1990, Caswell 2001), making them crucial analytical tools for translating the information contained in necropsy data sets to their corresponding effects at the population scale. A fundamental measure arising from a population matrix model is the long-term growth rate (lambda), which is the summary of intrinsic performance and long-term viability of the population (Caswell 2001, Koons et al. 2007). This rate has been used to measure the population-scale consequences of a perturbation to the life cycle (de Kroon et al. 2000, Caswell 2001), making it key in summarizing the overall effects to the population from the presence of a contaminant. Alternatively, the stochastic growth rate measures population performance by merging intrinsic growth (or decline) with the net effects of gains or losses through dispersal (Tuljapurkar 1990), making this rate key in identifying whether dispersal has played a role in empirical population performance. In a long-lived species such as the bald eagle, the survival rates of the age classes and the age at first reproduction are influential factors to the long-term growth rate. Similarly, in an open population (one that experiences gains and losses through dispersal), net differences between emigration and immigration are influential to the stochastic growth rate. Both growth rates summarize (in different ways) the performance of the population and pinpoint the biological threshold differentiating a population that is expected to persist and one expected to decline.
Our objectives were to explore if documented mortalities of eagles from the ingestion of Pb altered the population scale dynamics of the wild eagle population in the northeast United States between 1990 and 2018, and if so, estimate the degree to which these mortalities altered growth rates, annual survival rates of eagles in each life stage, or the resilience of the population to absorb additional mortalities. We hypothesized that mortalities arising from the ingestion of Pb reduced the long-term growth rate and resiliency of bald eagles in the northeast United States between 1990 and 2018. We further hypothesized that average annual survival rates of eagles in the 3 life stages (hatchling, non-breeding, and breeding) were reduced as a result of mortalities associated with the ingestion of Pb.
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