Avian Urine: Its Potential as a Non-Invasive Biomonitor of Environmental Metal Exposure in Birds

Current non-invasive biomonitoring techniques to measure heavy metal exposure in free ranging birds using eggs, feathers and guano are problematic because essential metals copper (Cu) and zinc (Zn) deposited in eggs and feathers are under physiological control, feathers accumulate metals from surface contamination and guano may contain faecal metals of mixed bioavailability. This paper reports a new technique of measuring lead (Pb), Cu and Zn in avian urate spheres (AUS), the solid component of avian urine. These metal levels in AUS (theoretically representing the level of metal taken into the bloodstream, i.e. bioavailable to birds) were compared with levels in eggs (yolk and shell), feathers and whole guano from chickens (Gallus gallus domesticus) exposed to a heavy metal-contaminated soil (an allotment soil containing Pb 555 mg kg⁻¹ dry mass (dm), Cu 273 mg kg⁻¹ dm and Zn 827 mg kg⁻¹ dm). The median metal levels (n = 2) in AUS from chickens exposed to this contaminated soil were Pb 208 μg g⁻¹ uric acid, Cu 66 μg g⁻¹ uric acid and Zn: 526 μg g⁻¹ uric acid. Lead concentrations in egg yolk and shell samples (n = 3) were below the limit of detection (<2 mg kg⁻¹), while Cu and Zn were only consistently detected in the yolk, with median values of 3 and 70 mg kg⁻¹ (dm), respectively, restricting the usefulness of eggs as a biomonitor. Feathers (n = 4) had median Pb, Cu and Zn levels respectively of 15, 10 and 140 mg kg⁻¹ (dm), while whole guano samples (n = 6) were 140, 70 and 230 mg kg⁻¹ (dm). Control samples were collected from another chicken flock; however, because they had no access to soil and their diet was significantly higher in Cu and Zn, no meaningful comparison was possible. Six months after site remediation, by top soil replacement, the exposed chickens had median Pb, Cu and Zn levels respectively in whole guano (n = 6) of 30, 20 and 103 mg kg⁻¹ (dm) and in AUS (n = 4) of 147, 16 and 85 μg g⁻¹ uric acid. We suggest the persistent high Pb level in AUS was a consequence of bone mobilised for egg production, releasing chronically sequestered Pb deposits into the bloodstream. In contrast, AUS levels of Cu and Zn (metals under homeostatic control and sparingly stored) had declined, reflecting the lower current exposure. However because pre- and post-remediation samples were measured using different methods carried out at different laboratories, such comparisons should be guarded. The present study showed that metals can be measured in AUS, but no assessment could be made of availability or uptake to the birds because tissue and blood samples were not concomitantly analysed. A major short coming of the study was the inappropriate control group, having no access to uncontaminated soil and being fed a different diet to the exposed birds. Furthermore guano and urine analysis should have been carried out on samples from individual birds, so biological (rather than just technical) variation of metal levels could have been determined. Future studies into using AUS for biomonitoring environmental heavy metals must resolve such experimental design issues.