Avian scavengers and the threat from veterinary pharmaceuticals

Abstract

Veterinary use of the non-steroidal anti-inflammatory drug diclofenac on domesticated ungulates caused populations of resident Gyps vultures in the Indian sub-continent to collapse. The birds died when they fed on carrion from treated animals. Veterinary diclofenac was banned in 2006 and meloxicam was advocated as a ‘vulture-safe’ alternative. We examine the effectiveness of the 2006 ban, whether meloxicam has replaced diclofenac, and the impact of these changes on vultures. Drug residue data from liver samples collected from ungulate carcasses in India since 2004 demonstrate that the prevalence of diclofenac in carcasses in 2009 was half of that before the ban and meloxicam prevalence increased by 44%. The expected vulture death rate from diclofenac per meal in 2009 was one-third of that before the ban. Surveys at veterinary clinics show that diclofenac use in India began in 1994, coinciding with the onset of rapid Gyps declines ascertained from measured rates of declines. Our study shows that one pharmaceutical product has had a devastating impact on Asia's vultures. Large-scale research and survey were needed to detect, diagnose and quantify the problem and measure the response to remedial actions. Given these difficulties, other effects of pharmaceuticals in the environment may remain undetected.

Medicating the environment: assessing risks of pharmaceuticals to wildlife and ecosystems

“…There are fewer data concerning subsequent Phase II and III metabolism of drugs in non-target organisms, but zero-order metabolism and consequent increased susceptibility to harmful pharmaceutical effects, or side effects, have been shown for the non-steroidal anti-inflammatory drug (NSAID) diclofenac in raptors [12,49]). …”

“…For example, residues of barbiturates in carrion of euthanized pets have been found to exceed the lethal dose for a spectrum of scavengers and there have been reports of secondary barbiturate poisoning [14]. The foraging mode of Asian vultures and their sensitivity to certain NSAIDs resulted in the near extinction of three keystone species [12,49]. The management of both species important for conservation (e.g.…”

“…Another reason why some non-target species might be particularly susceptible to pharmaceuticals is if they do not possess the metabolic, excretory or detoxification systems present in the, primarily mammalian, target species, including humans; the physiology and anatomy of renal systems in Gyps vultures and cats, for example, appear to be particularly susceptible to accumulation of uric acid and occurrence of visceral gout, following exposure to diclofenac [12,49]. Genetic variation among populations of the same species might also incorporate the loss of polymorphisms or allozymes associated with altered drug target sensitivity or increased uptake versus loss rate of environmental chemicals, including pharmaceuticals, in a range of wildlife, humans and model species (reviewed in [71]).…”

“…Cuthbert et al [12] present data on the effectiveness of mitigation measures mediated by conservation organizations and the Indian government designed to reverse the dramatic declines in populations of scavenging raptors. Fundamental to this has been to understand why the LD 50 of diclofenac to vultures is 0.1 mg kg 21 [74] compared with 9.8 mg kg 21 for the domestic chicken [75] and up to 1500 mg kg 21 for some mammals [76] (which also highlights the taxonomic diversity in responses to pharmaceuticals).…”

Assessing variation in the potential susceptibility of fish to pharmaceuticals, considering evolutionary differences in their physiology and ecology

“…This has been shown to cause population-level declines, and even localized extinctions, in three Asian vulture species (Gyps sp.) scavenging on the carcasses of treated cattle [10,11]. In another case, the contraceptive oestrogen 17a-ethinyloestradiol (EE2) has been linked directly with population-level risks in wild fish, owing to feminization in males and reduced fertility in both sexes of several fish species [12][13][14][15].…”