Short CommunicationCompleting a worldwide picture: preliminary evidence of lead exposure in a scavenging bird from mainland Australia
Graphical abstract
Introduction
There is growing worldwide recognition of the threat posed by toxic lead-based ammunition for scavenging wildlife (Pain et al., 2019). Lead exposure can cause harm to animals through lethal effects (mortality) and nonlethal effects (morbidity) such as inhibited spatial movements (Ecke et al., 2017). Harmful lead levels have been found in a multitude of scavenging species associated with lead-based ammunition but little attention has been devoted to this issue in Australia (Hampton et al., 2018). This is a worldwide phenomenon, with harmful lead exposure from bullet-derived lead having been reported from numerous scavenging bird species in North America (Bakker et al., 2017; Church et al., 2006), Europe (Ecke et al., 2017; Helander et al., 2009) Asia (Isomursu et al., 2018; Kenny et al., 2015), South America (Lambertucci et al., 2011; Wiemeyer et al., 2017) and Africa (Garbett et al., 2018; van den Heever et al., 2019). We are unaware of any such published studies on wild Australian species. However, recent studies have demonstrated that harmful lead exposure can affect mammalian scavengers in Australia such as captive Tasmanian devils (Sarcophilus harrisii) exposed to lead-based bullet fragments (Hivert et al., 2018). To our knowledge, this is the first study to assess lead levels in a scavenging bird from mainland Australia.
Our study species was the wedge-tailed eagle (Aquila audax), Australia's largest raptor. Wedge-tailed eagles are distributed throughout mainland Australia and Tasmania, with some contention surrounding taxonomy of sub-species (Olsen, 2005). A recent study demonstrated elevated lead levels in the Tasmanian subspecies of the wedge-tailed eagle (Aquila audax fleayi) (Pay, 2019). Wedge-tailed eagles are known to scavenge extensively, both on roadkill as well as shot wildlife (Brooker and Ridpath, 1980; Olsen, 2005). Breeding adult wedge-tailed eagles are territorial, with territory sizes typically around 20–50 km2 in temperate areas and larger in arid areas, while non-breeding birds are highly nomadic (Brooker, 1974; Cherriman, 2007, Cherriman, 2013; Dennis, 2006; Leopold and Wolfe, 1970; Ridpath and Brooker, 1987). Wedge-tailed eagles have been observed to scavenge on several species of shot wildlife including introduced deer subjected to recreational hunting (Forsyth et al., 2014) and commercially harvested native marsupials (Hampton et al., 2018). The risk that lead from ammunition poses to this species is exemplified by findings of adult kangaroo skulls in nests of wedge-tailed eagles at times when commercial kangaroo harvesting was in operation (Brooker and Ridpath, 1980).
Investigations of lead toxicity in wildlife should ultimately be directed towards identifying the potential sources of lead in the environment as source attribution can provide valuable information directing policy and management around lead use (Church et al., 2006; Sriram et al., 2018). Lead stable isotope analysis is increasingly used in wildlife ecotoxicological studies to trace pathways of lead exposure (Lambertucci et al., 2011; Sriram et al., 2018). There are four main naturally occurring isotopes of lead (204Pb, 206Pb, 207Pb and 208Pb), and the composition of these isotopes can vary between sources. Resulting variability in ratios between these isotopes (e.g. 207Pb/206Pb ratio) creates a “fingerprint”, allowing for the differentiation between sources of lead in the environment; both anthropogenic and environmental in origin (Gulson et al., 2018). Isotope ratios have been shown to differ between ammunition and other sources and thus have been used to distinguish between different sources of lead (Finkelstein et al., 2010; Sriram et al., 2018).
Section snippets
Study areas
Samples were collected from two sites in south-western Australia: the Perth Hills and Matuwa Indigenous Protected Area (IPA). These sites are approximately 800 km apart (Fig. 1). The Perth Hills are a peri-urban area of dry sclerophyll forest east of the Darling Range (elevation c. 300 m), comprising mostly forest and woodlands of tall Eucalyptus species, much of which is water catchment, with mixed private land use including orchards, livestock grazing and urban development (Rycken et al., 2019
Specimen collection
Bone and eggshell samples were collected from all dead birds and empty shells found during inspections of eagle nests for an ecological research project (Cherriman, 2013). We chose bone and eggshell as our target sample types due to their ease of collection long after birds had died or hatched. Bone is commonly used in similar studies (Specht et al., 2018; van den Heever et al., 2019; Wayland et al., 1999) while testing of eggshell is less commonly reported. However, avian eggshells are
Laboratory analyses
Laboratory methods utilized inductively coupled plasma mass spectrometry (ICP-MS) to quantify lead levels following protocols very similar to those used by many other authors (van den Heever et al., 2019; Warner et al., 2014). Testing was performed at the School of Sciences Analytical Facility laboratory at Edith Cowan University, in Perth, Australia.
Bones and eggshells were dried to a constant weight. Samples first underwent acid digestion using a microwave digestion system. Lead
Statistical analysis and interpretation of results
Initially, we used the arbitrarily defined threshold for greater-than-background bone lead levels as >6.75 ppm from published literature which examined congeneric eagle species from the northern hemisphere (Clark and Scheuhammer, 2003; Madry et al., 2015). Subsequently, we examined previously studied isotope ratios from the four lead isotopes, as per Gulson et al. (2018) to identify eagles for whom lead exposure may have been attributed to ammunition. We used a self-starting non-linear model
Lead assays
From 11 bone samples, the mean lead concentration was 3.14 ppm (Table 1). Five bone samples demonstrated lead levels >1.5 ppm and three bone samples demonstrated lead levels >6.75 ppm. All three of these birds were all from the Perth Hills site. For 36 eggshell samples, the mean lead concentration was 0.13 and no samples had lead levels >0.5 ppm (Table 1). No bone or eggshell samples revealed lead levels traditionally considered to cause severe clinical effects (>20 ppm) (Franson and Pain, 2011
Discussion
To our knowledge, this is the first evidence of environmental lead contamination in scavenging birds from mainland Australia. Lead levels in bone were moderate while lead levels in eggshell were uniformly low. The disparity between bone and eggshell lead levels may suggest some limitations for this matrix as an indicator of harmful lead exposure. Low lead levels in eggshell may also reflect seasonality in lead exposure in wedge-tailed eagles. The lead levels observed in bone samples from adult
Conclusions
Our preliminary study into lead exposure in scavenging birds in mainland Australia confirms that this is a truly global phenomenon, with Australia representing the final inhabited continent to reveal evidence of this process. We contend that our results have some positive implications in that they suggest that lead exposure may not be currently severely harmful in peri-urban and remote sparsely-inhabited portions of the continent. However, we suggest that land management agencies heed the
Funding
This project was funded by the Department of Conservation, Biodiversity and Attractions. through the Barrow Island threatened and priority species translocation program.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We appreciate the input of Jon Arnemo, Todd Katzner, Dave Kenny, Tom Newsome, James Pay, Mark Pokras, and Mel Snape to this research. We acknowledge the Noongar and Wiluna Martu peoples, who are the traditional custodians of the study sites, and appreciate the input of TMPAC, and members of the Matuwa Kurrara Kurrara IPA Management Team. We appreciate the constructive comments of three reviewers.
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