**3. Chiropteran life history, ecology, and physiological adaptations**

### **3.1 Overview of bat diversity and ecological services**

The order Chiroptera contains more than 1400 species—equating to over 1 in every 5 mammals is a bat [20]. Chiropteran species were previously divided into two suborders, Megachiroptera and Microchiroptera based upon morphological and behavior data. The suborder Megachiroptera consists of approximately 166 species, all belonging to the family Pteropodidae, whose diet consist of fruit, nectar, or pollen [20]. Seventeen other families compose the suborder Microchiroptera, the majority of which consume insects [20]. These suborders are still routinely used by some scientists and biologists. However, new molecular biology findings combined with morphological and behavior data have led researchers to propose two new suborders of bats, Yinpterochiroptera and Yangochiroptera, which do not coincide with the previous subordinal classification [21].

Chiroptera are critical to ecosystem health as they provide critical ecosystem services such as arthropod suppression, seed dispersal, and pollination on every continent except Antarctica [20, 22]. However, some ecosystems are at risk of degradation due to more than a quarter of the world's bat species facing the threat of extinction [23]. Additionally, over half of the species are facing population declines or have unknown population statuses further jeopardizing ecosystem health [23, 24].

Bat population declines are frequently attributed to habitat loss, White-nose Syndrome, wind energy, and more recently climate change [23, 25]. Pesticide exposure and pollutants are less recognized for causing population declines due to the lack of Chiropteran specific ecotoxicological studies. The few studies that are published directly link population declines to dermal contact and oral ingestion of pesticides [26–30].

#### **3.2 Foraging ecology and diet**

Nearly all bat species are nocturnal, with dusk and a few hours before dawn being their most active foraging times. Foraging strategies are diverse and are dependent upon the diet and the individual species morphological characteristics. The feeding behavior of bats who consume primarily fruit, frugivorous bats, are based upon their body size, dentition, and skull/jaw morphology [31]. Nectivorous bats, those whose diet consumes of primarily nectar, select flowers based upon their digestive capacity, lingual (tongue) morphology, and possibly metabolic rate [32, 33]. Relatively little is known about fishing bats, or piscivorous bats, who consume fish prey. It has been suggested that skull morphology, body size, wing morphology, and acoustic properties dictate piscivorous bats dietary niche partitioning [34, 35]. There is a lack of information on dietary morphological adaptations for the 3 sanguinivorous bat species who are obligate blood feeders.

Most is known about insectivorous bat species, those who consume insects, because most Chiropteran species fall within this category. Wing morphology, body size, and echolocation strategies influence which insect species are preyed upon [36]. For example, the aerial hawking species botta's serotine (*Eptesicus bottae*) have an average body mass of 8.9 ± 1.3 grams (adult males and nonreproductive females), broad wings with an average wingspan of 27.3 ± 1.8 mm and an average wing area of 12.6 ± 6.7 cm<sup>2</sup> [37, 38]. *E. bottae* fly around 5.7 meters per second and their echolocation calls allow them to detect large prey up to 21 meters away with an echo delay of one wing beat [38]. With these morphological characteristics helping to dictate their diet, DNA metabarcoding studies have revealed they consume primarily insects from the orders Auchenorrhyncha, Coleoptera, Lepidoptera, Heteroptera, and Hymenoptera [37].

By consuming agricultural pests as part of their diet, insectivorous bats are highly valued by farmers. Presently there is no worldwide estimate of the economic value of the ecological services provided by bats; however, researchers in the US have estimated that insectivorous bats provide roughly \$22.9 billion dollars per year in natural pest control services to US crops [39]. Due to the high foraging activity around agricultural areas and active consumption of pests that are targeted by insecticides, nearly all of the Chiropteran ecotoxicology studies focus on insectivorous species [30].

The majority of bat species in agricultural areas actively forage over fields at night with an increase in activity at dusk or dawn due to the increased activity of crepuscular insects [40]. Due to the recognition of pesticides affecting bee health, current guidelines for pesticide applicators are to apply pesticides at dusk, dawn and late at night while pollinator activity is low to non-existent in order to avoid pollinator mortality [41].

The application of pesticides at the height of bat activity, directly increase the risk of inhalation exposure of the droplets and vapors created during pesticide applications [7]. By flying through the spray clouds when foraging over agricultural fields or the vapors along the field margins, there is an increased risk of dermal exposure as well as an increased risk of oral exposure through the consumption of prey coated during the application process. Additionally, the lights used during dusk or night application may increase bat activity of non-light aversive species due to the attraction of insects to the lights [42].

It is plausible that frugivorous and nectivorous bat species also experience a similar increase in risk to pesticide exposure especially in intensively managed orchards. Because there is only a single study documenting organochlorine pesticide in a nectivorous bat species, the lesser long-nosed bat (*Leptonycteris sanborni*), [43] and no studies, other than manipulative experimental exposure studies, on frugivorous bats [30] it is difficult to assess their exposure risk. Whereas there are numerous records of organochlorine, organophosphate, and other pesticide residues found in deceased insectivorous species indicating that pesticide exposure is occurring and can be linked to mortality [30].

#### **3.3 Roosting ecology**

Due to recent estimates of the economic value insectivorous bats (e.g. see [39]), the agricultural industry and general public have begun recognizing the valuable natural pest control services provided by insectivorous bats. This recognition has resulted in some farmers attempting to attract bats by placing bat houses near fields or leaving untouched treelines with adequate roosting structures such as tree cavities or flaking bark [7, 44, 45].

Depending upon the species, some bats may also use farmland buildings such as barns or stables, or even roost on farm homes made of brick that contain shallow cracks [46] or under shutters based upon the authors' personal observations. With

*Pesticide Exposure Risks to Chiropteran Species and the Impacts on Emerging Zoonotic Diseases DOI: http://dx.doi.org/10.5772/intechopen.100643*

roost locations located within or adjacent to crops where pesticides are applied, bats within these roosts are at increased risk of inhalation and dermal exposure from pesticide drift [47] especially those roosting on exterior walls of buildings.

While bats are within their day roosts, they exhibit a variety of activities (e.g. parturition, nursing, torpor, and grooming) depending upon the sex and season. All these activities increase the risk of exposure. For instance, grooming could result in the increased risk of oral exposure if the roost is contaminated through pesticide drift or if bats where in direct contact with the pesticides during the application process. These roosts tend to be continuously habited for weeks to months and many are reutilized each year [48] leading to the potential for continuous long-term exposure if the roosts are contaminated. Bats also utilize night roosts in order to conserve energy, avoid predators, digest consumed food, to exchange information and for social interactions [49]. These night roosts have similar increased risks if they are in areas exposed to pesticide drift.

Some species select caves to roost for hibernation or may utilize them throughout the year. By crawling on cave walls and drinking from underground water sources, they are at risk of dermal and oral exposure because cave sediments, groundwater, and drip water samples in surveyed areas have all been reported to contain a variety of organochlorines and other pesticide metabolites [50–53].

#### **3.4 Drinking**

Bats are unable to obtain enough water through their diet, and so must rely upon drinking to meet daily needs. In addition to drinking potentially contaminated karst water, bats also drink from tailing ponds which can be high in cyanide, heavy metals, and occasionally pesticides depending upon the location of the mining operation [53]. Within the agricultural setting, bats have been observed to drink from irrigation canals, small ponds, and water troughs with the latter two often containing pesticides from overland flow [53] and thereby increasing the risk of oral exposure.

#### **3.5 Reproduction**

It is generally believed that bats reproduce once per year with most species giving birth to 1 pup or occasionally twins (e.g. big brown bat, *Eptesicus fuscus*) [54]. The exception to this is bats belonging to the genus Lasiurus who can give birth to up to four pups. For more detailed information on the reproductive biology of bats see [54].

Actual pesticide exposure risks to pups is difficult to assess. Two older studies assessing banned organochlorine pesticides such as DDE documented maternal transfer and resulted in offspring mortality [55, 56]. There is only a single study assessing reproductive effects for a commercially available fungicide, tebuconazole. This study coated papaya with the manufacturer's recommended application concentration of tebuconazole. When great fruit-eating bats (*Artibeus lituratus*) consumed the fruit, testicular and epididymal histomorphological changes were observed, suggesting that the fungicide tebuconazole may impact reproductive capacities in males [57]. Unfortunately, reproductive females were not evaluated.

Despite the lack of studies on contaminants in actively reproducing female bats and/or their offspring, it is probable that pups can be exposed in utero based upon numerous studies in humans and other mammals documenting placental transfer of commonly sold pesticides including neonicotinoids [58–60]. Furthermore, because pesticides and their metabolites are often detected in mammalian milk [61–63], pups are likely exposed to pesticides for approximately 3–4 weeks after birth while nursing.
