Out of thin air: surveying tropical bat roosts through air sampling of eDNA

Abstract

Understanding roosting behaviour is essential to bat conservation and biomonitoring, often providing the most accurate methods of assessing bat population size and health. However, roosts can be challenging to survey, e.g., physically impossible to access or presenting risks for researchers. Disturbance during monitoring can also disrupt natural bat behaviour and present material risks to the population such as disrupting hibernation cycles. One solution to this is the use of non-invasive monitoring approaches. Environmental (e)DNA has proven especially effective at detecting rare and elusive species particularly in hard-to-reach locations. It has recently been demonstrated that eDNA from vertebrates is carried in air. When collected in semi-confined spaces, this airborne eDNA can provide remarkably accurate profiles of biodiversity, even in complex tropical communities. In this study, we deploy novel airborne eDNA collection for the first time in a natural setting and use this approach to survey difficult to access potential roosts in the neotropics. Using airborne eDNA, we confirmed the presence of bats in nine out of 12 roosts. The identified species matched previous records of roost use obtained from photographic and live capture methods, thus demonstrating the utility of this approach. We also detected the presence of the white-winged vampire bat (Diaemus youngi) which had never been confirmed in the area but was long suspected based on range maps. In addition to the bats, we detected several non-bat vertebrates, including the big-eared climbing rat (Ototylomys phyllotis), which has previously been observed in and around bat roosts in our study area. We also detected eDNA from other local species known to be in the vicinity. Using airborne eDNA to detect new roosts and monitor known populations, particularly when species turnover is rapid, could maximize efficiency for surveyors while minimizing disturbance to the animals. This study presents the first applied use of airborne eDNA collection for ecological analysis moving beyond proof of concept to demonstrate a clear utility for this technology in the wild.

Using eDNA for mammal inventories still needs naturalist expertise, a meta‐analysis

“…On the way around, low detection overlaps highlight the need to use both types of methods to increase the overall success of mammalian inventories, and this is particularly the case for bats (Figure 2). The use of air filter to gather bat DNA is promising and could greatly complement mist netting (Garrett et al, 2023;Johnson et al, 2023). In the same way, the ease of sampling and high DNA yield from leaf swabs seems a promising technique for eDNA capture (Lynggaard et al, 2023), which predicts a bright future for eDNA biodiversity assessments.…”

“…Second, if a particular taxon is targeted, a combination of both DNA and trapping can maximize detection. For example, airDNA has been shown to be a promising way of detecting bat species (Garrett et al., 2023), which is completely noninvasive, and coupled with mist net surveys, to cross‐validate metabarcoding results. The “tangible proofs” coming from direct observations of specimens is still important because it is not possible to ignore the presence of eDNA in the absence of living target and the absence of eDNA in the presence of the living target without actual field surveys (Beng & Corlett, 2020).…”

“…In the case of vertebrates, many different substrates have been used to establish species inventories and can be grouped into three classes. First, the eDNA group, using substrates from the animal's environment such as water (seawater, freshwater, Ficetola et al., 2008; Foote et al., 2012), soil (Andersen et al., 2012; Taberlet et al., 2012), sediments (McDonald et al., 2023; Ryan et al., 2022), and air through filters (Garrett et al., 2023; Lynggaard et al., 2022). Another type of substrate can be considered eDNA traps, as they allow DNA concentration due to their intrinsic properties, such as feces (Van Der Heyde et al., 2021; Walker et al., 2019, hair (Croose et al., 2023; Lee et al., 2016), saliva bait (Nichols et al., 2015; Piaggio et al., 2019); saltlicks (Ishige et al., 2017), vegetation (Allen et al., 2023; Van Der Heyde et al., 2021) and even spider webs (Gregorič et al., 2022).…”

“…We argue that the amount of DNA shed by those taxa would be in lesser amount compared to large ungulates and carnivores. Although bat DNA captured through air filters seems a promising strategy, its utilization is still at the infancy level and studies did not meet our selection criteria (Garrett et al., 2023; Johnson et al., 2023). Moreover, we hypothesized that eDNA from soil was less efficient than originating from freshwater due to the patchy distribution of mammals on land (Seeber & Epp, 2022).…”

Emerging use of air eDNA and its application to forensic investigations – A review

“…The authors noted that air sampling was adopted from fungal collection methods and resulted in lower DNA concentrations when used to detect bats, identifying a need for method optimization for bat species by increasing the volume of air sampled. Garrett et al [86] used air eDNA sampling to investigate roosting behaviour of bats for conservation and biomonitoring purposes. Authors sampled various locations, including natural caves and tree hollows, and were able to identify currently occupied habitats, detecting 23 taxa, including bats, co-habiting mammals and other local animals.…”