Detection and drivers of exposure and effects of pharmaceuticals in higher vertebrates

Abstract

Pharmaceuticals are highly bioactive compounds now known to be widespread environmental contaminants. However, research regarding exposure and possible effects in non-target higher vertebrate wildlife remains scarce. The fate and behaviour of most pharmaceuticals entering our environment via numerous pathways remain poorly characterized, and hence our conception and understanding of the risks posed to wild animals is equally constrained. The recent decimation of Asian vulture populations owing to a pharmaceutical (diclofenac) offers a notable example, because the exposure route (livestock carcasses) and the acute toxicity observed were completely unexpected. This case not only highlights the need for further research, but also the wider requirement for more considered and comprehensive ‘ecopharmacovigilance’. We discuss known and potential high risk sources and pathways in terrestrial and freshwater ecosystems where pharmaceutical exposure in higher vertebrate wildlife, principally birds and mammals, may occur. We examine whether approaches taken within existing surveillance schemes (that commonly target established classes of persistent or bioaccumulative contaminants) and the risk assessment approaches currently used for pesticides are relevant to pharmaceuticals, and we highlight where new approaches may be required to assess pharmaceutical-related risk.

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

“…anthelmintic 'worming' treatments excreted in dung and antibiotics from the aquaculture industry) and indirectly via predation or scavenging of medicated animals [12,22,[28][29][30][31][32] (figure 1). Recycled raw sewage, municipal wastewater and biosolids are also being applied increasingly to urban green spaces such as parks and golf courses, which is likely to result in increased environmental exposure to organisms occurring across a range of habitats [14,33,34]. Pharmaceuticals also have been detected at high concentrations near drug production facilities, particularly in countries with developing economies [2].…”

“…Predicting bioavailability of drugs in soils and also sediments is complicated by the fact that many compounds are ionizable and those that form cations may become bound to negatively charged clay particles [35,36]. Nevertheless, some pharmaceuticals might still be available to soil-or sediment-ingesting organisms and could potentially accumulate in terrestrial and benthic food webs (reviewed by Shore et al [14]). Consequently, wildlife across diverse ecosystems are likely to be exposed to pharmaceuticals in the environment either directly or indirectly.…”

“…The majority of exposure and uptake data are derived from laboratory organisms, while there are only a limited number of studies that quantify variation in the environmental uptake of pharmaceuticals in the wild [44]. With the aid of established environmental surveillance schemes focusing on well-characterized classes of persistent or bioaccumulative historical contaminants, Shore et al [14] examine the sources, pathways and food webs in terrestrial and freshwater systems that potentially result in the greatest exposure. Using data extrapolation, they identify the likely factors that should also mediate the degree of uptake of pharmaceuticals.…”

“…An emerging topic discussed in this issue is how the probability of exposure of wildlife to environmental contaminants can be influenced by fitnessrelated traits such as foraging range, feeding behaviour and reproductive strategy, including spawning and dispersal patterns [9,14]. Freshwater taxa have been relatively well studied in terms of exposure to pharmaceuticals [9,10,45,52,55] compared with terrestrial [14,15,[56][57][58] or marine [9,32] species. In many aquatic taxa uptake of soluble, hydrophilic compounds occurs mainly via the gills or dermally (particularly in small organisms such as larvae), whereas uptake of less soluble, hydrophobic compounds more often occurs via a dietary route [59].…”

“…This Theme Issue focuses on risks posed by pharmaceuticals (principally hydrocarbon-based small molecules, as opposed to larger biopharmaceuticals) in the environment to vertebrate wildlife which share the greatest level of orthology for mammalian drug targets important to human and veterinary medicine [7][8][9]. Both laboratory and field-based evidence of pharmaceutical exposure and effects are considered [10][11][12][13][14][15]. Some of the papers and ideas developed here derive from a Royal Society International Scientific Seminar held in April 2013, with the title 'Assessing the exposure risk and impacts of pharmaceuticals in the environment on individuals and ecosystems' [16].…”