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 from primary Pb emission vectors suggest that ∼48% of all Pb newly brought into use is ultimately lost to the environment (Mao et al. 2009). The second-largest loss, accounting for 21% (670,000 metric tons Pb yr⁻¹) of the annual environmental Pb deficit, is Pb dissipated following use (Mao et al. 2009). In the United States alone, >69,000 metric tons of Pb were used in the production of ammunition in 1 yr (U.S. Geological Survey 2013). Among the initial 15 countries of the European Union, ∼34,600 metric tons of Pb shot and ∼4,000 metric tons of Pb bullets and pellets are used per year (European Commission 2004). Annual estimates of Pb fishing weights sold amount to 3,977 metric tons in the United States, up to 559 metric tons in Canada, and 2,000–6,000 metric tons in Europe (Scheuhammer et al. 2003, European Commission 2004, United Nations Environment Programme 2011). Radomski et al. (2006) estimated 16 tons of Pb tackle in 5 surveyed lakes over a 20-yr period, or an average ∼320 pounds Pb lake⁻¹ yr⁻¹.

Although these estimates provide context for the raw distribution of Pb into ammunition and fishing tackle, it is important to note that they are clearly unrepresentative of the amount of Pb that is distributed and available for avian exposure (Figure 1). To appropriately estimate potential exposure coefficients, data are needed that quantify (1) the proportion of purchased ammunition and fishing tackle that is actually used; (2) the proportion of use that occurs in outdoor environments where birds can be exposed; (3) the proportion of ammunition and fishing tackle used in outdoor environments that is left in such a form or location that avian exposure is possible (i.e. bullet fragments left in carcasses); and (4) the probability that a bird will be exposed to any available Pb-based ammunition or fishing tackle (Figure 3). Although ample evidence shows considerable avian Pb exposure from ammunition and fishing tackle, we need to address these data gaps to generate ecosystem- or regional-scale estimates of potential avian Pb exposure. A distinct understanding of primary exposure pathways is important for managing scenarios where avian risk to Pb exposure is high.

FIGURE 3.

The remains of Pb and copper bullets fired into a water barrel from a .30-06 rifle. (A) Unfired Pb core bullet (with a copper alloy jacket) next to remains from a fired bullet of similar type. Tiny bullet fragments provide a great deal of surface area allowing for increased absorption of Pb once ingested by scavengers. (B) Unfired copper bullet next to the remains from a fired bullet of similar type. Photos courtesy of Clinton Epps (C. Epps and D. Sanchez personal communication).

Pathways of avian exposure

Among toxicologically significant sources (e.g., Pb-based paint, mining, smelters, and combustion residue of leaded gasoline; Blus et al. 1999, Church et al. 2006, Beyer et al. 2013), spent ammunition and lost fishing tackle are the primary exposure pathways for birds in terrestrial and aquatic systems (Kendall et al. 1996, Liu et al. 2008, Rattner et al. 2008), and these are pathways that can be controlled and managed.

The highest human-caused Pb concentrations associated with ammunition are found in and near shooting ranges (United Nations Environment Programme 2013), where patches of Pb shot may attain concentrations of 5–17 kg Pb m⁻² (Rattner et al. 2008). However, it is important to note that these values are localized extremes, and there is considerable variability in the soil Pb content in shooting ranges (Bennett et al. 2007). Nevertheless, many grit-seeking birds pick up Pb fragments at or near shooting ranges.

Conversely, traditional hunting areas may be more representative of the potential Pb exposure risk to wild birds. Although Pb densities are substantially lower than in target ranges (Ferrandis et al. 2008), the deposition of Pb pellets from historical waterfowl and contemporary Mourning Dove (Zenaida macroura) hunting provide some of the strongest examples of the amount of Pb that can be associated with hunting activities within a confined area (Box 1). During the period of Pb use for hunting migratory waterfowl, Bellrose (1959) estimated densities as high as 125,970 pellets ha⁻¹; more recently, Pain (1991) reported pellet densities of nearly 2 million pellets ha⁻¹. In managed upland dove-hunting fields where Pb shot is legal, shot densities range from tens of thousands to hundreds of thousands of pellets per hectare (Box 1 and Figure 4). However, there are differences in how long Pb pellets deposited on the landscape are available to birds, particularly between wetland and upland habitats. Flint and Schamber (2010) estimated that Pb pellets in the sediment of wetlands would be available to most species of waterfowl for ≥25 yr. If so, the risk of exposure to Pb pellets from past hunting for most waterfowl species in North America should be nearly eliminated, given that it has been 14 and 22 yr since Pb shot has been banned in Canada and the United States, respectively. However, legacy Pb exposure in some waterfowl species, such as swans, is still a concern because of the greater depths at which they forage within sediments (Smith et al. 2009). Furthermore, drying of seasonal wetlands can expose pellets that upland species (e.g., doves and pheasants) ingest.

BOX 1. Mourning Dove Hunting and Pb Pellet Dispersion

Declines in resident upland game-bird populations of Northern Bobwhite (Colinus virginianus; Brennan 1991) and Ring-necked Pheasant (Phasianus colchicus; Riley and Schulz 2001, Frey et al. 2003) have prompted many state and provincial resource management agencies to increase Mourning Dove shooting opportunities on public lands, especially near urban 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 and 8.9 kg ha⁻¹ among areas, and the estimated average number of no. 8 Pb pellets, which measure 2.26 mm in diameter, ranged between 35,624 and 128,632 ha yr⁻¹ among areas (Schulz et al. 2012). During 1998–1999, Pb shot deposition related to dove hunting in southern Nevada ranged from 8,970 to 22,559 pellets ha⁻¹ in fields managed primarily for dove hunting (Gerstenberger and Divine 2006). Posthunt pellet densities from 15 managed dove fields in Indiana during 1987 ranged from 2,152 to 83,928 pellets ha⁻¹ (Castrale 1989). Sampling of the upper soil layer in southeastern New Mexico during 1987 showed prehunt estimates of 167,593 pellets ha⁻¹ and posthunt estimates of 231,731 pellets ha⁻¹ (Best et al. 1992). Posthunt pellet densities in Tennessee were estimated at 107,821 pellets ha⁻¹ (Lewis and Legler 1968).

Within a national context, ∼960,000 dove hunters routinely harvest 16.6 million doves annually (Seamans et al. 2012), taking approximately 4 or 5 shots dove⁻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, especially for a suite of ground-feeding passerines (Fisher et al. 2006) and game birds (Hunter and Rosen 1965, Keel et al. 2002, Schulz et al. 2002, Potts 2005, Larsen et al. 2007, S. D. Holladay et al. 2012).

FIGURE 4.

(A) Healthy pectoralis in a Mourning Dove. (B) Eroded breast muscle due to loss of appetite and reduced physical activity following ingestion of Pb pellets (shot size no. 7.5). Muscle erosion occurred in <22 days in captive birds (Schulz et al. 2006). Photo courtesy of John Schulz.

More difficult to estimate is bullet fragment density from big-game hunting, in which Pb is associated with offal (i.e. gut piles) and carcasses. Although the densities of Pb fragments are necessarily lower than those associated with shot, they are also more localized and associated with an attractant (animal carcasses or offal) that could substantially increase the probability of avian exposure.

The density of Pb fishing tackle in aquatic environments is highly variable yet can have significant impacts on aquatic species such as loons and swans. Duerr (1999) estimated 0.01 and 0.47 sinkers m⁻² in areas of low and high fishing pressure in the United States, respectively. In the United Kingdom, estimates have ranged between 0.84 and 16.3 sinkers m⁻² along the Thames River (Sears 1988) and between 24 and 190 sinkers m⁻² in shoreline areas in Wales (Cryer et al. 1987). It is important to note that these large estimates of lost-tackle densities are from locations with exceptionally high fishing pressure and may not be representative of tackle densities in other locations. To understand subsequent risk, it is crucial to understand relative waterbird use of the high-risk zone. For example, Radomski et al. (2006) utilized creel surveys of walleye fishermen to evaluate rates of tackle loss across 5 Minnesota lakes and estimated that Pb tackle densities in 1 of these lakes was <0.002 sinkers m⁻². Across the 5 lakes, whose combined area was 267,933 ha, cumulative total estimated Pb-tackle losses were found to be >100,000 pieces, or ∼1 metric ton year⁻¹ of the study (Radomski et al. 2006). It is unclear what waterbird exposure rates might be at these Minnesota lakes; however, Pokras et al. (2009) found that 118 of 522 (23%) Common Loon (Gavia immer) carcasses from 6 New England states contained ingested Pb objects, primarily sinkers and jigs, as well as ammunition. This suggests that although overall densities may be low across entire lakes, Pb tackle may be concentrating in habitat sectors that increase exposure risk, assuming that densities of tackle in New England and Minnesota lakes are comparable.

Direct exposure

Direct exposure occurs when birds mistake Pb objects for seeds or grit and purposefully ingest them, often in areas of heavy hunting and fishing pressure or at established shooting ranges (Boxes 1 and 2). In terrestrial areas, this pathway to Pb poisoning is most relevant to seed-eating birds that obtain grit for muscular grinding of seeds in the gizzard (Fisher et al. 2006, Rattner et al. 2008). Some waterbirds also consume Pb objects for use in the gizzard and become poisoned through the same route (Smith et al. 2009) or in combination with Pb that they consume when diving (Pokras et al. 2009).

Indirect exposure

Indirect exposure to Pb occurs when predators and scavengers incidentally ingest Pb when consuming the flesh of an animal that has been shot with Pb ammunition or that ingested Pb sinkers or a soil-dwelling organism containing high Pb levels (Boxes 1, 2, and 3; Figure 4). Scavenging raptors such as eagles, vultures, and condors are typically influenced by this route of Pb poisoning (Box 2; Figures 5 and 6). They make extensive use of offal from harvested animals and from carcasses of animals that are killed for recreation (e.g., prairie dogs [Cynomys spp.]) or for animal control purposes or that are shot by hunters but cannot be retrieved (Fisher et al. 2006, Kelly et al. 2011, Bedrosian et al. 2012, Harmata and Restani 2013). Importantly, Pb bullets expand or “mushroom” and then fragment, dissipating the bullet's energy. As a result, an average of 235 (range: 15–621) and 170 (range: 85–521) Pb fragments remain in the eviscerated carcass and viscera, respectively (Hunt et al. 2007, 2009; Knott et al. 2010; Figures 5 and 6). This fragmentation increases the likelihood that multiple individuals can be exposed to Pb from a single carcass or gut pile. In addition, the small size and increased surface area of the fragments that stem from spent ammunition also increase the uptake of Pb into the bloodstream (Hunt et al. 2009). Although these exposure sources may be highly localized, the magnitude of their negative effects is increased when they are used as food resources by widely dispersing, highly social scavengers (e.g., vultures and condors). Finally, indirect exposure can also occur in ground-feeding species that rely heavily on earthworms as prey (Scheuhammer et al. 1999, 2003), such as the American Robin (Turdus migratorius; Beyer et al. 2004, 2013) and American Woodcock (Scolopax minor; Scheuhammer et al. 1999, 2003).

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) feathers in northwest Patagonia suggests that they are also being exposed to Pb from ammunition (Lambertucci et al. 2011). Other avian scavengers that share one or more of the following traits and occur in regions where Pb is available in 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.

Large size

Large avian scavengers search out food in large 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-game hunters. Their large size also means that they consume a relatively large quantity of meat at each carcass, increasing their risk of exposure to any contaminants that may be disproportionately distributed throughout the carcass.

Life-history pattern of low reproduction and high annual survival

Low reproductive output of 1 or 2 offspring every 1 or 2 yr, an extended subadult period of several years prior to recruitment into the breeding population, and a long life span of several decades or more define a life-history pattern that can be sensitive to small changes in adult survival rates (Mertz 1971, Meretsky et al. 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 that tend to roost and feed communally as an adaptation for finding resources that are large 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

A number of intrinsic factors influence species' susceptibility to Pb poisoning, including retention of Pb after ingestion versus regurgitation (Stendell 1980), nutritional status and diet, and chemical environment in the lumen (Pattee et al. 2006). Species that fail to regurgitate 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 include the spatiotemporal relationship of Pb exposures to hunting areas and season, Pb isotope ratios in feathers and blood (Scheuhammer and Templeton 1998, Church et al. 2006, Lambertucci et al. 2011), elevated copper concentrations in the kidneys of Pb-exposed eagles as an indicator of the presence of copper-jacketed Pb bullets (Cruz-Martinez et al. 2012), radiographs of Pb-exposed scavenger gastrointestinal tracts (e.g., Helander et al. 2009; Figure 6) and food items (Knopper et al. 2006, Hunt et al. 2009; Figure 5), and toxicological studies combined with direct field observations 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 levels or Pb exposure rates in avian scavengers and big-game hunting has been observed in multiple species across diverse regions of the world: Bald and Golden eagles in the upper midwestern United States (Kramer and Redig 1997, Strom et 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 southern California (Hall et al. 2007, Kelly and Johnson 2011, 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 studies have found that Pb exposures are not strictly limited to big-game hunting seasons. Furthermore, Pb pellets and .22 bullets not associated with big-game hunting have been recovered in the digestive tracts of California Condors (Rideout et al. 2012), Bald and Golden eagles (Cruz-Martinez et al. 2012), and sea eagles (Helander et al. 2009), and in the pellets of Egyptian Vultures (Neophron percnopterus; Donázar 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 simply eliminating Pb ammunition use by big-game hunters. However, these hunters remain the key to survival for most scavengers in the world (Mateo-Tomás and Olea 2010). 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.

FIGURE 5.

(A) Golden Eagle (Aquila chrysaetos) chick with a Belding's ground squirrel (Spermophilis beldingini) food source (Upper Malheur River, Harney County, May 2013). Photo courtesy of Eric Forsman. (B) Radiograph of Pb fragments in Belding's ground squirrels found dead in a field. Photo courtesy of Jeff Cooney.

FIGURE 6.

Pb poisoning in Bald Eagles following consumption of carcasses containing Pb bullet fragments. (A) Adult showing muscle degeneration, unable to stand, open-mouth breathing, weakness, and wing droop. (B) X-rays indicating location of Pb bullet fragments in coyote. (C) Pb-poisoned Bald Eagles collected in one Iowa location over 1 yr by Project SOAR. Photo courtesy of Project SOAR.

Lead impact on avian physiology

Pb ingested from Pb pellets or bullet fragments is absorbed into the circulatory system, aided by the grinding action in the gizzard; thus, diet can affect Pb uptake rates (Marn et al. 1988, Locke and Thomas 1996, Vyas et al. 2001). Once Pb is absorbed into the body, its toxicological effects are diverse. However, as is true with nearly all contaminants, interspecific variation in tolerance to Pb is considerable, which makes it difficult to assess risk solely on the basis of blood Pb levels. For example, the California Condor (Gymnogyps californianus) experiences significant mortality as a result of Pb ingestion (Finkelstein et al. 2012). Conversely, Carpenter et al. (2003) found that Turkey Vultures (Cathartes aura) repeatedly dosed with large numbers of Pb shot and constant redosing survived much longer than other species of avian scavengers, such as Bald Eagles (Haliaeetus leucocephalus), that received similar doses of Pb (Hoffman et al. 1981). These studies suggest that complex physiological processes regulate exposure and toxicity risk to Pb and vary even between close relatives. Thus, factors beyond the gross number of Pb pellets or bullet fragments ingested are important in understanding how environmental exposure is linked to toxicological responses.

At the organismal level, Pb poisoning can modify the structure and function of kidney, bone, the central nervous system, and the hematopoietic system, leading to adverse biochemical, histopathological, neurological, and reproductive effects (Boggess 1977, Nriagu 1978, DeMichele 1984, Eisler 1988, Rattner et al. 2008, Franson and Pain 2011). These effects can be observed at a very young age, as shown by studies of nestling Western Bluebirds (Sialia mexicana) and Japanese Quail (Coturnix japonica; Fair and Myers 2002, Fair and Ricklefs 2002). The range of physiological effects is mirrored by the range of potential responses to exposure. Acute poisoning may occur rapidly, without characteristic signs such as emaciation or lack of coordination (Locke and Thomas 1996). Chronic exposure results in lethargy and anorexia, breast-muscle atrophy, loss of strength and coordination, drooping wings, and changes in vocalization (see Figure 6).

Modes of action

Neurological impacts of Pb on animals are highly contingent on the chemical form of Pb, dose, and exposure duration, as well as the age, sex, and health of the bird (Müller et al. 2008). In the avian body, Pb mimics calcium and substitutes for it in many fundamental cellular processes, including nervous-system function (Simons 1993, Flora et al. 2006). For example, Pb can activate protein kinase C, which plays a critical role in the vertebrate nervous system by controlling the function of other proteins (Hwang et al. 2002). Pb poisoning also leads to anemia by reducing heme synthesis and decreasing the life span of erythrocytes (Eisler 1988, Goyer 1996). Pb affects the nervous system by changing calcium homeostasis and inhibiting cholinergic nerve cells, thus interfering with signal transmission across nerve synapses and leading to behavioral changes (Sanders et al. 2009). The cerebellum is the primary target for Pb toxicity in the brain and is the major determinant for behavioral changes (Alfano and Petit 1981). Experimental studies with environmentally relevant Pb doses in wild nestling Herring Gulls (Larus argentatus) demonstrated that Pb impairment can result in decreased health, less vigorous food-acquisition behaviors, poor coordination, and decreased survival (Burger and Gochfeld 1994).

Pb also impairs the enzymes δ-aminolevulinic acid dehydratase (δ-ALAD) and ferrochelatase, ultimately interfering with heme synthesis, and resulting in anemia if exposure is high enough (Hoffman et al. 1985). Northern Bobwhites (Colinus virginianus) dosed with a single no. 9 Pb shot (i.e. 2 mm in diameter) exhibited only 8% of normal ALAD activity 8 wk after dosing (S. D. Holladay et al. 2012). The same dose regime resulted in blood Pb levels >80 times higher than background in captive Rock Pigeons (Columba livia; J. P. Holladay et al. 2012). In wild birds, δ-ALAD and intermediary metabolites such as protoporphyrin in blood are used as biomarkers of exposure (Locke and Thomas 1996). Time for δ-ALAD recovery to normal levels is dose dependent, organ specific, and usually directly correlated with blood Pb levels.

Population-level effects of Pb

The potential effects of Pb poisoning on individual birds are clearly established. Far less clear are the population-level consequences of current rates of Pb exposure in many species. The best examples are from waterfowl, in which losses to Pb poisoning were estimated to be 2–3% overall, with an estimated 4% annual loss in Mallards (Anas platyrhynchos; Sanderson and Bellrose 1986). Similarly, Grand et al. (1998) estimated that survival rates of female Spectacled Eiders (Somateria fischeri) exposed to Pb shot from ingestion were 34% lower than those of unexposed females (77%) and suggested that Pb exposure may have been preventing local population recovery. California Condor populations appear to be at substantial risk from Pb exposure (e.g., Cade 2007, Walters et al. 2010, Finkelstein et al. 2012). Pb sinkers appear to be a regulatory factor for Common Loons in New Hampshire, where 49% of known mortalities are attributed to Pb poisoning from fishing tackle (Vogel 2013).

Significance of Pb exposure to avian conservation

Given proof that elevated Pb exposure can greatly influence the health of individual birds and can result in mortality, the environmental distribution of Pb from ammunition and fishing tackle could be an important factor influencing the conservation of avian communities. Here, we discuss (1) the apparent contradiction in results of some studies regarding avian exposure and levels of impairment caused by different contaminant concentrations; (2) unease with the implicit assumption of many published studies that Pb is the ultimate source of mortality for birds found dead with elevated Pb concentrations; and (3) lack of clarity over the relative threat of Pb to birds in comparison to other major impacts such as invasive species, habitat loss, human disturbance, domestic cats, and collisions with vehicles, power transmission lines, and buildings.

We have already presented several examples of increases in avian Pb exposure in association with ammunition and tackle. Similarly, we have outlined many instances of toxicity associated with environmental and lab-derived exposure to Pb. However, the results of other studies add a layer of ambiguity to this topic that is important to acknowledge. For example, even at relatively similar Pb exposure levels, studies have shown clear effects on blood chemistry (Kerr et al. 2010, Carpenter et al. 2003, Hoffman et al. 1981, Pattee et al. 2006), egg production (Edens and Garlich 1983), behavior (Burger and Gochfeld 1994, 2004), and survival (Schulz et al. 2006, Grand et al. 1998, Pattee et al. 2006, Rideout et al. 2012), whereas others demonstrated limited responses to many of the same endpoints (McBride et al. 2004, Schulz et al. 2007, Ferrandis et al. 2008). Although differences in methodology likely played some role, a more plausible explanation is intrinsic interindividual and interspecific variability in sensitivity to Pb. This source of variation complicates overall estimates of Pb risk to avian communities and represents a key data gap in Pb ecotoxicology.

Acute toxicity leading to mortality can often be determined from physical or behavioral cues, especially if tissues are analyzed for Pb content postmortem. But it is uncommon to encounter Pb-intoxicated birds for which this information can be obtained, which complicates attempts to estimate actual mortality due to Pb. As a result, numerous studies have reported Pb levels in tissues from dead birds, making the implicit assumption that mortality was a result of Pb exposure in those birds with elevated concentrations (Helander et al. 2009, Hernández and Margalida 2009, Kenntner et al. 2001, Wayland and Bollinger 1999). In some cases, mortality is likely due to Pb poisoning, but as we noted above, the tremendous range in sensitivities among individuals and species can make the use of tissue thresholds to infer cause of death problematic. Thus, the proportion of birds found dead with elevated Pb concentrations is often a poor and biased (under or over) estimator of mortality rates.

The cumulative body of scientific evidence unequivocally suggests that Pb exposure from ammunition and fishing tackle is directly responsible for numerous bird deaths each year and is clearly a serious threat to the population trajectory of the endangered California Condor (Franson et al. 2003, Walters et al. 2010, Finkelstein et al. 2012; Box 2). However, for many bird species, the impact of Pb exposure is much less clear given the assortment of other anthropogenic hazards and conservation threats they face. For example, >1 billion birds year⁻¹ are estimated to be killed by domestic cats in the United States (Loss et al. 2013), and millions of bird mortalities each year result from collisions with power lines, fixed objects, and vehicles (Loss et al. 2014). In addition, habitat loss and intensified land use can have an immeasurable impact on the conservation status of many bird species at global scales. However, addressing the Pb issue is tractable because it entails a relatively simple solution: replacing Pb-based ammunition and fishing tackle with non-Pb alternatives.

Proponents of this solution contend that alternatives to Pb are readily available and of comparable cost and that the costs are expected to decrease with increases in demand that accompany improved efficiencies in ballistics (Thomas 2013). Conversely, supporters of continued Pb use in ammunition and fishing tackle argue that the increased costs of non-Pb alternatives require robust and clear scientific evidence of impacts before any changes are made. However, these competing ideas are not mutually exclusive. Progress could be made in reasonably short order to reduce avian Pb exposure and increase scientific knowledge of Pb's impacts through an integrated plan of voluntary Pb replacement programs coupled with large-scale research efforts to evaluate the effects of Pb management on avian Pb exposure.

Variation in Pb sensitivity

Numerous studies have evaluated toxicological responses of birds to Pb exposure (Franson and Pain 2011), but a consistent, ecologically meaningful, and standardized approach does not currently exist. This makes it challenging to prioritize how best to manage for Pb risk and makes comparative assessments across multiple taxa difficult. Thus, an important step in reducing Pb exposure in birds is the development of a standardized vulnerability assessment that considers life-history traits, exposure likelihoods, and sensitivity to the toxic effects of Pb. Of note, the concept of differential sensitivity among avian species that allows for thresholds that vary among taxa is well established for a range of contaminants (e.g., organochlorine pesticides, polychlorinated biphenyls, mercury, and selenium; Eisler 1986, Heinz et al. 2009, Blus 2011, Ohlendorf and Heinz 2011, and many others). For example, Buekers et al. (2009) summarized results of 13 repeated-dosage studies of Pb for 12 avian species. Including a range of endpoints in their analysis, they found a 50-fold range in estimates of no-observed–effect concentrations. Thus, similar Pb exposure levels will likely elicit a wide range of effects across a gradient of species. Unfortunately, few studies encompass the range of primary exposure mechanisms with similar exposure periods under standardized conditions. These estimates are important for providing context to Pb exposure across the landscape and should incorporate ecologically relevant endpoints (e.g., growth, survival, behavior, and reproduction).

Pb contamination and distribution

The spatial distribution and availability of Pb in the environment are complicated by the need to account for multiple Pb source types (Figure 1). Studies that focus on ammunition sources for birds commonly fail to account for other potential environmental Pb exposures. However, we can get a coarse estimate of Pb deposited in the environment by counting the number of harvested animals in a particular location, assuming that all were killed by Pb bullets and that offal remains were left in the field. For example, annual harvests of >200,000 white-tailed deer (Odocoileus virginianus) in Minnesota, an estimated 2 million prairie dogs in 3 U.S. states, and 3.1 million roe deer (Capreolus capreolus) in Germany, France, Austria, Poland, and the Czech Republic have been reported (cf. Thomas 2013). Recent isotopic studies, in conjunction with field studies, are now helping to disentangle exposure histories and have demonstrated that differentiating among multiple sources of Pb is possible (Church et al 2006, Finkelstein et al. 2010, Lambertucci et al. 2011). Other studies have confirmed Pb bullet fragments or fishing gear as the source of mortality through x-rays and necropsies (e.g., Pokras and Chafel 1992, Franson et al. 2003, Cruz-Martinez et al. 2012).

Pb contamination associated with hunting and recreational shooting is not homogeneous across the landscape, and the combination of seasonal hunting activity and annual variation in harvest rates among locations adds a temporal component to Pb risk across the landscape. Thus, exposure risk is likely maximized when spatial and temporal patterns of Pb availability converge in important habitats and life stages, such as in foraging ranges associated with nest sites (Walters et al. 2010) or in migration corridors for raptors (McBride et al. 2004). As a result, if managers are to identify key areas for targeting Pb reduction, there is a clear need for more robust, temporally dynamic, and higher-resolution estimates of Pb availability on the landscape that are separately associated with various sources of Pb.

Pb contamination and environmental stressors

The effects of Pb on birds are generally assessed independently of other environmental conditions. Much less is known about the extent to which sublethal Pb exposure interacts with other environmental stressors experienced by free-living birds, possibly resulting in behavioral abnormalities, decreased clutch sizes, reduced growth rates (Burger and Gochfeld 1994, 2000), reduced hematocrit levels (Redig et al. 1991), reduced δ-ALAD activity (Hoffman et al. 1985, Finkelstein et al. 2012), and impaired neural development in young birds (Dey et al. 2000). Kelly and Kelly (2005) found that Pb-intoxicated swans were more prone to collisions with power lines than non-intoxicated swans, which suggests that sublethal Pb toxicosis may indirectly elevate mortality rates. Research that can address the issue of multiple stressors under field conditions will be critical for assessing the combined and relative risks of Pb and habitat conditions on bird species.

Demographic effects

Ascribing a direct link between Pb and population trajectories (λ) is exceedingly difficult (Kendall et al. 1996) because it requires estimates of cause-specific mortality rates that can be obtained only through intensive sampling efforts combined with necropsies and toxicological investigations. Projections have been made under varying exposure scenarios for such intensively managed species as the California Condor (Finkelstein et al. 2012), in which all individuals in the population are closely monitored and the cause of every known death is investigated. For other species, targeted and robust estimates of the influence of Pb on key demographic parameters (e.g., adult and juvenile mortality, fecundity) would be useful but generally do not exist. For example, Grand et al. (1998) found that survival of female Spectacled Eiders exposed to Pb from ingesting spent shot were substantially lower than those of unexposed females (77% vs. 44%), which may have made it difficult for some local populations to recover. Such an approach could facilitate a better understanding of Pb effects on key demographic parameters that may go into later population estimates and projections

Ammunition

Many countries have banned Pb shot for waterfowl hunting, yet only Sweden and Denmark have banned Pb ammunition for all forms of hunting (Avery and Watson 2009). The U.S. and Canadian governments banned Pb ammunition for waterfowl hunting in 1991 and 1999, respectively, using their jurisdictional authority under the Migratory Bird Treaty Act. Studies conducted after this ban found a substantial decline in Pb shot exposure in waterfowl (Anderson et al. 2000, Stevenson et al. 2005), resulting in a 64% decline in annual Pb poisoning in Mallards (Anderson et al. 2000). Currently, U.S. and Canadian migratory bird regulations prohibit hunting waterfowl and American Coots (Fulica americana) with Pb shot; all other hunted migratory birds can still be shot with Pb (D. J. Case and Associates 2006; Environment Canada:  http://www.ec.gc.ca/regeng.html). The U.S. National Wildlife Refuge System requires that hunters possess and use only approved nontoxic ammunition while hunting on Waterfowl Production Areas (50 CFR 32.2(k)). Individual refuges have adopted specific rules that require the use of nontoxic ammunition outside of these areas for hunting waterfowl, upland game birds, Mourning Doves, red foxes (Vulpes vulpes), and coyotes (Canis latrans; 50 CFR 32.20–32.70). U.S. National Park Service personnel have used non-PB ammunition since 2008 (Ross-Winslow and Teel 2011). Further, the U.S. Army will issue a new Pb-free version of the 7.62-mm rounds fired from the M-14 to troops in 2014 ( http://www.army.mil/article/106710/Picatinny_ammo_goes_from_regular_to_unleaded).

Fishing tackle

In the most sweeping reform, the European Union is on track to ban Pb in fishing tackle by June 2015 (European Fishing Tackle Trade Association;  http://www.eftta.com/english/news_indepth.html?cart=&SKU=2047259450). All Pb fishing tackle has been banned in Denmark since 2002, and Pb tackle (0.6–28.4 g) has been banned in the United Kingdom since 1987 (United Nations Environment Programme 2013). It is illegal to use Pb fishing sinkers and jigs weighing <50 g in National Parks and National Wildlife Areas in Canada (SOR 96–313, 23.4 17(h)). There are some restrictions on the use of Pb fishing gear in U.S. national wildlife refuges and national parks, but these decisions have been made at the level of the individual refuge or park (50 CFR 32.20–32.70). For example, Yellowstone National Park banned most Pb tackle because of concerns regarding “alarmingly low populations” of Trumpeter Swans (Cygnus buccinator) and loons ( http://www.nps.gov/yell/planyourvisit/upload/14FishReg.pdf). The park continues to allow Pb-core line and heavy (>2 kg) downrigger weights used to fish for deep-dwelling lake trout, with the rationale that these weights are too large to be ingested by waterfowl.

Alternatives to Pb

An increasing number of Pb-free ammunition options are available for hunters and recreational shooters. A recent study of 37 corporations that produce non-Pb bullets and shot for the international market found no major difference in the retail price of equivalent Pb-free and Pb-core ammunition for many popular rifle calibers and shotgun gauges (Thomas 2013). Further, the study found that there were a minimum of 35 calibers and 51 rifle-cartridge configurations available. One caveat to the use of non-Pb ammunition is that manufacturers currently produce smaller quantities of these ammunition types compared with Pb-based ammunition, so availability may limit access to these alternatives unless production volume is increased. To explore this, we conducted an Internet market search of the 3 major resale distributers in the United States for each of the non-Pb centerfire bullets and shotgun slugs identified in Thomas (2013). In October 2013, only 18%, 27%, and 10% of the Pb-free options were available from Cabela's ( http://www.cabelas.com), Cheaper Than Dirt ( http://www.cheaperthandirt.com), and Bass Pro Shops ( http://www.basspro.com), respectively. This general lack of availability could hamper efforts to transition to Pb-free ammunition. However, it is not clear whether the lack of Pb-free options results from lack of market demand or lack of production by ammunition manufacturers.

To our knowledge, only 2 peer-reviewed studies have assessed the effectiveness of non-Pb ammunition under traditional hunting conditions. Trinogga et al. (2012) assessed wound size and morphology between Pb-free and Pb-core rifle cartridges. In that study, wild ungulates (n = 34) were shot, and the authors found that the killing potential assessed via wound diameters and maximum cross-sectional area were similar between Pb-core and Pb-free bullets. Similarly, Knott et al. (2009) shot ungulates (n = 153) using Pb-core and Pb-free bullets and assessed the lethality of the bullets on the basis of accuracy and killing power, finding no difference in either assessment between bullet types. Although these studies indicate that the use of non-Pb ammunition is unlikely to affect hunting success, additional peer-reviewed research is needed to more fully explore non-Pb ammunition performance across a range of hunting applications.

Anglers can use a variety of materials for non-Pb fishing weights and sinkers, including bismuth, tin, tungsten, steel, and brass ( http://water.epa.gov/scitech/swguidance/fishshellfish/animals.cfm). Natural stone is also an option for some fishing applications ( http://www.recycledfish.org). We have not found a formal review of the effectiveness of various types of fishing tackle or comparisons among Pb and non-Pb weights and sinkers. Given that these materials vary in density, malleability, and cost, a careful review of the performance of these materials in different fishing applications would be helpful.

Federal, provincial, and state leadership

U.S. and Canadian federally mandated removal of Pb from ammunition used to hunt waterfowl resulted in a significant and rapid reduction in Pb exposure in waterfowl and prevented the loss of birds to Pb poisoning (U.S. Fish and Wildlife Service 1976, 1986, 1988, Anderson et al. 2000, Samuel and Bowers 2000, Stevenson et al. 2005), thus demonstrating the efficacy of legal restrictions on the use of Pb ammunition for hunting. For example, by 1996–1997, only 1.1% of 1,318 ducks collected on the Mississippi flyway had apparently been shot using Pb ammunition (Anderson et al. 2000).

The efficacy of laws restricting the use of Pb tackle has not been well tested because there are few and they are relatively new. However, analyses comparing pre- and post-restriction (1989–1999 vs. 2000–2011) mortality in New Hampshire loons found that the rate of Pb fishing-tackle mortalities fell marginally by 3% (preban adult mortality [± SE] = 12.5% ± 1.7; postban mortality = 9.5% ± 1.2; Grade 2011, Vogel 2013). Vogel considers the estimates of mortality to be conservative and concludes that Pb sinkers are a major cause (49% of known deaths) of mortality for Common Loons in New Hampshire.

Voluntary approaches

Some advocates, managers, and decision-makers have chosen to expand voluntary programs in lieu of regulatory approaches, or recommend such programs as interim steps to generate enough support for passage of a Pb ban. The National Park Service and some states have already implemented these measures (Ross-Winslow and Teel 2001, Epps 2014). The Association of Fish and Wildlife Agencies, led by the directors of state agencies, has formed a “Lead and Fish and Wildlife Health” Working Group and is an important leader on this issue. Their positions and initiatives reflect responsiveness to public sentiment and the missions of member agencies to manage for conservation, hunting, and fishing. Further, some federal, provincial, and state agencies are voluntarily switching to use of nontoxic ammunition and fishing tackle in the course of their duties (e.g., dispatching sick or wounded animals or shooting animals for depredating crops or livestock).

Non-Pb ammunition and tackle giveaways or exchanges in key areas

Hunters have participated in non-Pb ammunition exchange or giveaway programs in California, Utah, Wyoming, and Arizona in an effort to help conserve the California Condor and reduce Pb poisoning in wild birds (Sieg et al. 2009, Southwest Condor Review Team 2012, Ventana Wildlife Society 2012). Anglers have participated in similar programs in Maine, Massachusetts, New Hampshire, New York, and Vermont to aid waterbird conservation (Ross-Winslow and Teel 2011). Exchanges and giveaways can also serve as an important communication tool by educating hunters and anglers on the hazards of using Pb ammunition and fishing tackle and explaining the benefits of switching to nontoxic alternatives.

Outreach and communication

Informing decision-makers, hunters, anglers, and the general public about Pb poisoning resulting from spent ammunition and lost fishing tackle may increase support for the use of non-Pb ammunition and tackle. The utility of outreach efforts alone has been questioned (Thomas 2011; but see Sieg et al. 2009, Schroeder et al. 2012). However, from research designed to investigate which communication strategies might increase support for restrictions on Pb ammunition, Schroeder et al. (2012) suggested that messages addressing the key beliefs dividing those who support Pb restrictions from those who do not are most likely to be successful. Social scientists would be key allies in helping to define the role of education and outreach efforts and aid in crafting key messages to eliminate the use of Pb-based ammunition and fishing tackle while maintaining hunting and fishing opportunities (Ross-Winslow and Teel 2011).