Blood Lead Concentrations of Free-Ranging North Florida Raptors: 2008–17

Exposure to lead is a well-described cause of morbidity and mortality in raptors, primarily eagles (Kramer and Redig 1997; Ecke et al. 2017) and vultures (Behmke et al. 2017). It has been hypothesized that the main source is from the remains of large game animals killed by lead ammunition (Behmke et al. 2015). Our study aimed to determine the relative prevalence of detectable blood lead concentrations (BLCs) in native North Florida, US, raptors, evaluate concentrations for clinical significance, and determine whether there was a possible species, seasonal, or geographic relationship to exposure. We hypothesized that foraging ecology, season of discovery, and geographic location would have a significant effect on the birds' BLCs.

Blood samples were collected from wild raptors admitted to the Zoological Medicine Service at the University of Florida between 1 January 2008 and 31 December 2017. Raptor species with ≥15 individual samples were included in this retrospective study: Bald Eagles (Haliaeetus leucocephalus, n=72), Ospreys (Pandion haliaetus, n=18), Black (Coragyps atratus, n=40) and Turkey (Cathartes aura, n=25) Vultures, Barred (Strix varia, n=129) and Great Horned (Bubo virginianus, n=20) Owls, and Red-tailed (Buteo jamaicensis, n=48) and Red-shouldered (Buteo lineatus, n=89) Hawks.

Whole blood was collected as part of the initial clinical assessment. Samples were processed within 1 h. All lead measurements were performed with the LeadCare II Point-of-Care Blood Lead Testing System (Magellan Diagnostics Inc., Billerica, Massachusetts, USA), which assays whole blood samples (50 µL) by anodic stripping voltammetry. Whole red blood cells are lysed with a dilute hydrochloric acid solution and transferred to a chamber in which an electrical potential induces any lead to collect on a sensor; with lower and upper limits of detection of 3.3 and 65 µg/dL, respectively. This method had been evaluated for accuracy in Golden Eagles and other wildlife by inductively coupled plasma-mass spectrometry (Domenech and Langner 2009; Langner et al. 2015) and in cattle by graphite-furnace atomic absorption spectrometry as comparisons (Bischoff et al. 2010); the LeadCare II system results correlated well with the other methods.

Statistical analyses were performed by Statistix 10 (Analytical Software, Tallahassee, Florida, USA). Kruskal-Wallis one-way nonparametric analysis of variance was used to compare the whole BLC between species, season, and the county in which each bird was found. Seasons were defined as Spring (March–May), Summer (June–August), Fall (September–November), and Winter (December–February). The findings of each category were then compared by Dunn's all-pairwise comparison test. We coded BLC of <3.3 µg/dL as 3.2 µg/dL; concentrations >65 µg/dL were assigned 65.1 µg/dL. A P≤0.05 was considered statistically significant for all tests.

Between 2008 and 2017, 441 BLCs were determined for eight raptor species from 23 Florida counties (Tables 1, 2). Of the birds sampled, 142 (33%) had detectable blood lead concentrations (>3.3 µg/dL). Most (95 of 142) detectable BLCs were from the two vulture species (33%) and Bald Eagles (34%), with much of the remainder being found in diurnal raptors (18%).

Owls, hawks, and Ospreys had median BLCs of <3.3 µg/dL (undetectable), with no statistical difference between these species (Table 1). Although 18% of detectable BLCs were from diurnal raptors, the median value was <3.3 µg/dL.

Grouping species with high versus low BLC (Table 1), the vulture species and Bald Eagles showed high BLCs, with no interspecies difference in BLC between vultures and eagles; they were placed in group 2. Blood lead concentrations of the species in group 1, owls, hawks, and Osprey (median 32 µg/dL), were significantly lower than those in group 2, (median 6.6–8.1 µg/dL; Table 1). A large proportion of samples from several species was found to have no detectable BLC: Great Horned Owls 20/21, Barred Owls 112/129, Red-tailed Hawks 44/48, Red-shouldered Hawks 67/89, Ospreys 16/18, Bald Eagles 11/72, Turkey Vultures 4/25, and Black Vultures 11/40.

Dunn's all-pairwise comparison test showed spring and fall were statistically similar groups, with no statistical difference when compared other seasons (groups AB; Table 3). Winter (group A; Table 3) had significantly higher BLC than summer (group B; Table 3). Blood lead concentrations were not significantly different among the 23 counties assessed (Table 2).

Finkelstein et al. (2012) found BLCs of 20 µg/dL in California Condors (Gymnogyps californianus) resulted in subclinical health effects, measured as >60% inhibition of the heme biosynthetic enzyme δ-aminolevulinic acid dehydratase, whereas BLC>45 µg/dL required clinical intervention. We found values within the range of concern mainly in vultures and Bald Eagles; only four samples >20 µg/dL came from other species (one Strix varia, three Buteo lineatus).

Blood lead concentrations were higher in birds of prey that are classically considered primary scavengers. Winter in North Florida is the hunting season for migratory waterfowl (Florida Fish and Wildlife Conservation Commission 2018b), as well as deer, turkey, quail, and bobcats, which may contribute to the exposure of these raptors to lead from hunting (Florida Fish and Wildlife Conservation Commission 2018a). Our findings are consistent with previous seasonal patterns of BLCs in avian scavengers. Kramer and Redig (1997) found that the BLCs of wintering eagles brought to the Raptor Center at the University of Minnesota were increased compared with samples collected in other seasons. Cruz-Martinez et al. (2012) showed markedly elevated concentrations of lead in Bald Eagles in the Midwest during their deer hunting season in the late fall–early winter. Our study supports these findings, indicating that lead from hunting is still probably a prominent issue despite a lack of substantial large game in this location. Additionally, our study indicates that these trends are still evident in a more temperate climate, not unique to the mid-northwest US.

Most studies have been in areas with state regulations of lead projectiles for hunting. Our study was in a state with, during the study period, no regulations for hunting with lead, other than the national ban on the use of lead ammunition in waterfowl from 1991 (Florida Statutes 2018). Combined with the seasonal increase in lead concentrations correlating to gun hunting seasons, it is highly suggestive that lead used in hunting may be a large source of blood lead contamination of native wild raptors.

Other sources of lead for wildlife include lead-based fishing tackle, often considered to be the cause of increased blood lead concentrations in waterfowl and piscivorous birds (Scheuhammer and Norris 1996). The species in our study most likely to encounter this source of lead would be Ospreys and Bald Eagles, both known to consume moderate amounts of fish. Bald Eagles are generally recognized to consume carrion more readily than Ospreys, which, rather than lead fishing tackle, could be a contributing factor in the disparity of detectable blood lead concentrations between these two species.

As expected on the basis of foraging ecology, both owl species had low to no detectable blood lead concentrations, with no samples within the range recommended for treatment. This result is similar to the findings of Liebeziet and Sheaffer (2014). In comparison, Behmke et al. (2015) found 100% of vultures had evidence of long-term exposure to lead and deemed these “sentinel species” for indicating lead increases in a particular ecosystem.

It is important to note that hunting and fishing are not the only possible sources of lead contamination, as illustrated by Bruggeman et al. (2018), who demonstrated increased lead concentrations in nestling Bald Eagles associated with local aquatic lead contamination. Similarly, in studies finding notable increases in BLC in nonscavenging raptor species (hawks, falcons, and owls), these have been secondary to diffuse environmental contamination with lead associated with mining and smelting sites (e.g., Henny et al. 1994). This kind of contamination is unlikely in the population of this study, given the lack of lead in samples from nonscavenging raptor species.

Our study also assessed the distribution of BLC geographically, which was found to lack statistical power. Historic evidence has suggested increased lead concentrations in raptors from rural areas (Liebezeit and Sheaffer 2014), but we could not confirm this.

Our study often found similar percentages of increased BLC within a given species, as seen in other studies. Stauber et al. (2010) found Bald Eagles in Washington and Idaho had a similar distribution of individuals in the testing population with >20 µg/dL as in our study (30–45%), whereas Kelly and Johnson (2011) found that 48% of Turkey Vultures in California had >10 µg/dL lead in their samples, comparable to 40% in our population.

One of the primarily limitations of our study is the sensitivity of the LeadCare II analysis for blood lead concentrations <3.3 µg/dL or >65 µg/dL, although it does provide a realistic view of the clinical assessment that is most likely to occur for these species, because this portable machine is very frequently used in the field and clinical settings. It would be beneficial in the future to evaluate samples with >65 µg/dL with additional testing strategies or compare BLC to tissue concentrations if the patient is euthanized, to truly assess the maximum lead concentrations being detected.

Statistics were completed on this data set despite limitations on the upper and lower end of analysis with the LeadCare II. These limited results, coded as 3.2 and 65.1 µg/dL, respectively, thus utilizing single imputation, may lead to biased data. Values below 3.3 µg/ dL are not considered clinically significant, but this possible bias is acknowledged.

In conclusion, lead exposure is common in vultures and Bald Eagles in North Florida. We found the highest BLC during winter, and the most likely source is contaminated remains from hunting. Our study, and others, reiterate that increased BLC is probably a problem wherever hunting with lead ammunition occurs, not exclusive to areas with harsh winters or large game hunting, where this concern has previously been most frequently evaluated. Further research is necessary to directly link the lead used in hunting with that found in birds. Various ammunition alternatives are available, and there is evidence supporting that a history of statewide bans has significantly lowered BLC in native species with previously high values (Kelly et al. 2011).

We thank the Batchelor Wildlife Endowment, University of Florida, for providing financial support for the treatment of injured wildlife including the research described here.