Pesticide Impacts on Bat Populations
Agricultural intensification may remove potential habitat for bats and their prey; the effects of increased agrochemical inputs, such as increased exposure and changes in prey availability, may put resident bats under further pressure.
Bats may directly consume pesticides by feeding on fruits, flowers, and arthropods exposed to chemical application. Even bats foraging outside of agricultural areas can be exposed to pesticides via biomagnification as residues are incorporated into the tissues of organisms at higher trophic levels (Bayat et al. 2014).
Investigations of exposure of bats to pesticides and its effects on physiology and mortality first appeared in the 1970s, amid a wave of growing concern regarding the effects of organochlorine pesticides (e.g., DDT, DDE, dieldrin, lindane, endosulfan, aldrin) on ecosystems and observations of declining bat populations at high-profile sites such as the Carlsbad Caverns in New Mexico, USA (Clark 1988, 2001). In some cases, DDT and other organochlorines were even applied directly to bat roosts in efforts to exterminate “vermin” (Kunz et al. 1977), and declines in high-profile bat colonies were linked to organochlorine use (Clark et al. 1978; Clark 2001). Even sublethal exposure to pesticides can have negative consequences for bats, resulting in increased metabolic rates (Swanepoel et al. 1998), and ingestion of pesticide residues on arthropods may poses a potential reproductive risk to certain bat species (Stahlschmidt and Brühl 2012).
Organochlorine residues have been documented in bats in a wide variety of both agricultural and non-agricultural landscapes, although several studies have found increased contaminant loads in bats sampled near agricultural areas (Clark and Prouty 1976; White and Krynitsky 1986) or near sites of pesticide manufacture (O'Shea et al. 2001). In some cases, temporal changes in levels of different contaminants reflect shifts in local agricultural practice as farmers adopt new pesticide regimes (Miura et al. 1978; Clark et al. 1980). Organochlorines are notorious for their persistence in ecosystems, and a variety of studies demonstrate that bats continue to harbor these contaminants in their tissues 20–30 years after the use of these pesticides was banned in sampling areas (Clawson and Clark 1989; Guillén et al. 1994; Schmidt et al. 2000; Sasse 2005). In some cases, persistence may reflect the continued use of these pesticides in lower income nations, as may be the case for the migratory Tadarida brasiliensis (Thies and Thies 1997; Bennett and Thies 2007). Investigations in India (Senthilkumar et al. 2001) and Benin (Stechert et al. 2014) have detected levels or metabolites of organochlorines in bat samples indicative of continued recent use in these regions, especially to fight against malaria. Furthermore, pesticide standards vary between different countries, application often appears to occur non-selectively, and farmers with limited training (especially in developing countries, where agricultural expansion is greatest) are likely to be unaware of the multitude of negative nontargeted environmental impacts affecting human health and biodiversity (Tilman et al. 2001; Yadav 2010).
Despite the clear negative impacts of organochlorines on bats, the effects of agrochemical classes such as pyrethroids and neonicotinoids remain largely unknown (O'Shea and Johnston 2009; Quarles 2013; Bayat et al. 2014), although recent research demonstrates a negative impact on birds (Hallmann et al. 2014). In North America, pesticide contamination has been implicated in bat mortality associated with the fungal pathogen causing white-nose syndrome (WNS), since pesticide load can lead to immunosuppression and endocrine disruption that could make bats more vulnerable to infection (Kannan et al. 2010). “Back of the envelope” calculations suggest declines in bat populations attributed to WNS could translate into an additional 1320 metric tons of insects escaping predation each year (Quarles 2013). The trickle-down impacts on agricultural production could be substantial, although quantitative evidence is lacking. The effects of GM crops incorporating insecticidal traits have been investigated largely in the context of the provisioning of predation services (Federico et al. 2008; Lopez-Hoffman et al. 2014; see next section); however, declines in pest numbers associated with the use of these crops could result in population declines of insectivorous bats (LopezHoffman et al. 2014).
