Impacts of anthropogenic disturbance and insect abundance on Sonoran Desert bat activity

Amy Sue Law1, Khushali Shah2, Emma McAndrews3, Jess Stumpf1

1University of California, Los Angeles; 2University of California, Riverside; 3University of California, Santa Cruz

Rapid urbanization has been beneficial and detrimental to desert ecosystems. One group of organisms that are sensitive to such anthropogenic disturbance are bats. In this study, we examined bat abundance and composition in the Sonoran Desert in Southern California to assess how the bat community is affected by human disturbance and insect abundance. We observed bat calls and surveyed insect abundance at sites with high and low levels of human impact. We found that there were marginally more bats in areas of high human impact. Specifically, there were somewhat more Silver Haired and Canyon Bats in areas of high human impact. We also found that bat abundance decreased over the time of night, and that insect abundance increased over the time of night. These results provided support that the positives and negatives of anthropogenic disturbances may counteract one another and result in a slight preference by bats for areas of high human impact. Insects may have also attracted more bats to their location, causing variation in species composition and bat abundance, depending on location.

Keywords: Insectivorous bats, Sonoran Desert, anthropogenic disturbance, echolocation, Chiroptera, Echo Meter 2

INTRODUCTION offer. For example, animals like rodents or insects are often attracted to artificial Anthropogenic disturbance is a ubiquitous bodies of water that help these species phenomenon that affects biodiversity and subsist in a desert habitat (Walker 2011). In can have wide reaching impacts on desert contrast, anthropogenic influences can ecosystems (Green 2003). Disturbances present challenges to native wildlife. A such as rapid urbanization and human damaging side effect of rapid urbanization development due to tourism, mining, and and high human disturbance is habitat agriculture, have both positive and negative fragmentation (Riley et al. 2003). Habitat side effects on many ecosystems (Walker fragmentation is when large areas of 2011). As the desert becomes a more habitat are transformed into small patches appealing place for human development, of isolated land, causing ecosystem decay disturbances to the ecosystem become (Franklin et al. 2002). Habitat fragmentation more prevalent (Jenerette and Wu 2001). In is also a chain link to habitat loss and overall the desert, human-dominated ecosystems degradation of species abundance, richness, can help different species persist because of and diversity that often affects many opportunities that anthropogenic habitats organisms in desert ecosystems (Green

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2003). It is particularly important to focus As a group, bats are well adapted on how anthropogenic disturbance affects predators and are successful in the desert desert communities because of increasing environment (Nowak 1994). Bat predation urbanization in desert areas. on insects is well documented and it has Human disturbance can directly affect even been proposed that bats provide an bats, whose unique behaviors like flight and ecosystem service to human populations echolocation make them particularly because of the sheer number of insects vulnerable to disturbance (Nowak 1994). they consume (Kunz et al. 2011). Not only Bats are among the most speciose clades of do they keep the insect population under mammals and have a cosmopolitan control in their environment, they also eat distribution, occurring in a diverse range of insects that are agricultural pests, habitat types including deserts (Nowak benefiting humans (Taylor 2013). Bat 1994). Most bats are nocturnal insectivores, behavior and migratory patterns can be feeding on insects like moths or mosquitoes influenced by insect abundance (Lee and via a behavior called echolocation (Nowak McCracken 2005), and urban areas can 1994). Bats echolocate by emitting an attract high concentrations of insects, ultrasonic call through their nose or mouth, potentially increasing bat populations echoing off obstacles and prey around the (Frankie and Ehler 1978). individual, allowing them to “see” their In this study, we surveyed bat surroundings in the dark (Griffin et al. communities using the Echo Meter Touch 2 1960). Therefore, factors such as PRO Handheld Detector and its anthropogenic noise and artificial lighting corresponding application at locations with can push particularly sensitive bats away different levels of human disturbance to from urban areas. (Polak et al. 2011). While test whether there was an effect of human human development can fragment habitat development on bat abundance and species and displace bat colonies, buildings also composition. We also examined the provide homes for bats to roost (McCracken correlation between bat abundance and 1989). Bats such as Kuhl’s pipistrelle insect abundance. Because of bat sensitivity (Pipistrellus kuhlii) have been documented to anthropogenic disturbance, areas with thriving in urban environments due to their more development may have fewer bats. affinity for roosting in occupied buildings, Alternatively, we hypothesized that areas whereas high mortality rates from getting developed by humans could attract more trapped in buildings have been documented bats with artificial bodies of water and in the European free-tailed bat (Tadarida buildings that could be potential roost teniotis) (Ancillotto 2015). Like all other locations. The bats we expected to find feed desert organisms, water is of particular exclusively on insects, so we hypothesized importance to bats in the area due to its that there would be a positive correlation scarcity, and studies have shown a positive between insect and bat abundance at our correlation between the area of water survey sites. In addition, we predicted that features and bat abundance (Rabe and because of the differences in sensitivity of Rosenstock 2005). In this way, human certain species, more impacted land would development of artificial water sources can have a different species composition than provide important resources for bats. less impacted survey sites. Specifically we

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predicted the hoary bat (Lasiurus cinereus), November 1–4 2019. Each site was sampled Mexican free-tailed bat (Tadarida for three hours between 18:00 to 23:00. brasilensis), Yuma myotis (Myotis The sites were categorized as either “low yumanensis), and pallid bat (Antrozous impact” or “high impact,” based on their pallidus) would prefer non-developed areas amount of human foot traffic, presence of due to their propensity to be threatened by light sources, and man-made structures. human activity (Bat Conservation The “high impact” sites were Ram’s Hill Golf International 2019). For example, the Yuma Club and Borrego Springs Resort (Table 1). myotis is susceptible to pollution of their These locations each had a water source, habitat by insecticides; other similar bats 14,134 m2 and 3,613 m2 respectively, and may be similarly affected (Frick et al. 2007). were surrounded by human-introduced grass, California fan palms (Washingtonia METHODS filifera), and cement roads. The “low impact” sites were the Pupfish Pond near The Southern California Anza Borrego the Palm Canyon trailhead in Anza Borrego Desert State Park is a suitable system for State Park and the local Water Treatment observing the effects of anthropogenic Center (Table 1). The Water Treatment disturbance on bats. The Park is Center was the most remote location, and approximately 957,110 square meters of had an 8,091 m2 water source surrounded Sonoran Desert, surrounding, but not by a barbed wire fence and large honey including, a small town called Borrego mesquite trees (Prosopis glandulosa). The Springs. Localities include several golf smallest water source was the 64 m2 courses, resorts, campsites, small Pupfish Pond that experiences small businesses, and neighborhoods. The stark amounts of human impact from the difference between developed and presence of campers and hikers in the undeveloped land within the park creates general area but was relatively untouched human-wildlife interactions with by human activity. understudied impacts. We sampled four locations with water sources in the Anza Borrego Desert from

Table 1: GPS coordinates for bat call and insect count sampling locations.

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Using the Echo Meter Touch 2 PRO “low impact.” Additionally, we used a chi- Application and Handheld Detector, square test to see if there was a difference manufactured by Wildlife Acoustics between “high impact” and “low impact” Bioacoustics Monitoring Systems, we locations in species composition. We also detected and recorded ultrasonic calls from used an ANOVA to see if the six most bats by walking a 50 meter transect parallel abundant species, which each had greater to the longest side of the water source. The than 50 calls, were more likely to be found app identified the potential bat species that at either “high impact” or “low impact” sites. was making each vocalization observed. Each recorded call was a proxy for an RESULTS individual bat observation, figuring that the two would be linearly related if all the bats In total, we sampled 20 time periods over were calling at the same rate. After the four nights. The multiple linear collecting the bat vocalization data, we regression showed that bat abundance cross referenced the calls using the decreased over time at night but had a positive relationship to the number of Montana Natural Heritage Program Bat Call 2 Identification PowerPoint, which had insects (n = 20, pfull model = 0.002, r = 0.50, example spectrograms of frequencies and ptime = 0.014, pinsects = 0.005; Figure 1). There shapes of the calls (Maxell et al. 2011). was a marginal effect of human impact level We collected data on insects at the site to on bat call abundance per time interval, explore the correlation between bat and indicating that there were marginally more bats in the “high impact” locations than the insect abundance. We hung up two 1 x 1.25 2 m2 white sheets with two flashlights and “low impact” locations (n = 20, r = 0.41, F = two blacklights pointed at one side to 14.30, p = 0.06; Figure 2). There was an attract insects. The number of insects on effect of human impact level on the species each sheet was counted every 30 minutes, that were present, which indicated that “high impact” sites had different species which gave five insect counts over the 2 period of observation. To align the bat present than “low impact” sites (n = 550, � observations with five insect counts, we = 154.48, p < 0.0001; Figure 3). When we categorized the bat calls based on time into examined at the six most abundant bat five equal intervals of 36 minutes each. species, only the silver-haired bat All statistical tests were conducted using (Lasionycteris noctivagans) (n = 20, F = JMP Statistical Software 14.0.0. We used a 15.38, p = 0.059) and canyon bat multiple linear regression to test if there (Pipistrellus hesperus) (n = 20, F = 12.46, p = was an effect of time of night and number 0.07) showed a marginal preference for the of insects on the number of bat calls. A “high impact” sites while western red bat mixed model ANOVA was used to look at (Lasirurus blossevillii) (n = 20, F = 3.24, p = the effect of human impact on the 0.21), Mexican free-tailed bat (n = 20, F = abundance of bats per time interval. This 0.069, p = 0.81), hoary bat (n = 20, F = 0.29, test accounted for the random effect p = 0.64), and Yuma myotis (n = 20, F = 6.00, location nested within “high impact” and p = 0.13) had no preference based on level of impact.

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Figure 1. Number of bat calls by number of insects and time. The linear regressions show the two components of the multiple linear regression for time and insects versus number of bat calls. As the number of insects increased, so did the number of bat calls. As the night went on at each of the study sites, fewer bats were observed (n = 20, 2 pfull model = 0.002, r = 0.50, ptime = 0.014, pinsects = 0.005).

Figure 2. Average calls per time interval by human Figure 3. Bat call frequency by species across high impact level. Bars represent the average number of and low impact sites. The total number of calls per bat calls per 36-minute time interval. More calls species over four days of research show different were heard in areas of high human impact than species compositions at high impact versus low impact areas of low human impact. High-impact locations locations (n = 550, �2 = 154.4832, p < 0.0001). Dark (Borrego Springs Resort, Rams Hill Golf Club) are grey bars show high impact sites; light grey bars shown in shades of blue; low-impact locations show low impact sites. Only silver-haired bats (n = (Pupfish Pond, Water Treatment Center) are shown 20, F = 15.38, p = 0.059) and canyon bats (n = 20, F = in shades of red (n = 20, r2 = 0.41, F = 14.30, p = 12.46, p = 0.07) showed marginal preferences for 0.06). high impact sites.

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DISCUSSION and trees, like golf courses and resorts (Bat Conservation International 2019). Canyon Overall, there were marginally more bats bats are characterized as very social and in areas of high human impact. The species may interact with humans, which may composition differed between high and low explain why they were not averse to being impact sites; specifically, there were in areas with high human impact. They’re marginally more silver-haired bats and also sensitive to dehydration, so being close canyon bats in areas of high human to the larger water sources, even man- disturbance. Bat abundance decreased as made ones, may be an advantage. (Bat the night went on, but increased with the Conservation International 2019). number of insects present. The slight difference in bat species Our finding that there was marginally diversity may have been due to the greater bat abundance in areas of high different life history requirements of each human impact contradicted our hypothesis species. Some species, such as the hoary that human impact would reduce bat bat are more sensitive to human impact abundance. We may have found a slightly than other species and may be more likely greater bat abundance in areas of higher to be harmed by human disturbances human impact because of the resources because of their long-distance migratory that rapid urbanization can provide. For lifestyle (Kunz et al. 2007). Depending on example, man-made structures and water the resources they rely on, bats could be features can provide roosting spots and helped or hurt by human presence in the resources for bats in more developed areas. desert. On one hand, humans can These opportunities, when matched with exterminate natural flora; on the other high levels of noise and light pollution, hand, they can bring water into the middle which can interrupt bat echolocation, could of the arid landscape (Walker 2011). This neutralize one another (Schaub 2008). Our ability to tolerate human development of result that there were marginally more land may depend on the life history silver-haired and canyon bats in areas of qualities of a species (Ancillotto 2015). “high impact”, did not support our The correlation between insect and bat hypothesis that there would be fewer abundance could be explained by the hoary, Mexican free-tailed, pallid, and insectivorous habits of the bats we studied. canyon bats in areas of “low impact.” The As all species present were insectivores, occurrence of marginally more silver-haired these bats may have been following their and canyon bats in areas of “high impact” food source (Lee et al. 2005). The may be explained by their life histories. correlation between insect and bat While silver-haired bats winter in Southern abundance may imply bottom up control in California, they may be drawn to human- this food web, as the number of bats developed areas because of the presence of increased with the number of insects (Lee introduced non-native palm trees that may and McCracken 2005). provide roosting locations (Izor 1979). As humans continue to encroach upon These bats are also generally found in old desert habitat, it becomes increasingly growth forests and are known to feed in necessary to investigate how organisms like highly developed areas with water sources bats are affected by anthropogenic

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disturbance. Although our findings show 10.21973/N3Q94F. Special thanks to Anza that many bats seem to be more common Borrego Desert State Park, Ram’s Hill Golf in highly human impacted areas, it is Club, and Borrego Springs Resort. All the unclear as to whether bats that tend to love to our amazing instructors Tim Miller, prefer human impacted areas will continue Krikor Andonian, and Reina Heinz. Thanks to do so as rapid urbanization continues bats! and their available natural habitat is altered. As new resources are provided to REFERENCES bats by human development, it could be Ancillotto, L. 2015. Sensitivity of bats to important to study how their behavior urbanization: a review. Mammalian Biology 80(3): changes. For example, if bats prefer 205–212. developed land like golf courses, golf course management could cater to bat Baerwald, E. F., & Barclay, R. M. R. 2011. Patterns of conservation by creating quiet hours near activity and fatality of migratory bats at a wind energy facility in Alberta, Canada. The Journal of ponds and avoiding the use of insecticides. Wildlife Management 75(5):1103–1114. Areas for further study could include the investigation of the extremes of human Barclay, R. M. R., Faure, P. A., & Farr, D. R. 1988. activity and development, such as light Roosting behavior and roost selection by pollution and noise levels, and how they migrating silver-haired bats (Lasionycteris noctivagans). Journal of Mammalogy 69(4):821– may individually impact specific bat species. 825. A more comprehensive study could be developed in order to gauge the impacts of Bat Conservation International. 2019. Retrieved different levels of human disturbance on October 11, 2019, from batcon.org bat community dynamics, specifically in the Carrete, M., Tella, J. L., Blanco, G., & Bertellotti, M. light and noise pollution disturbances, 2009. Effects of habitat degradation on the because studies show that these two abundance, richness and diversity of raptors factors threaten bats (Stone et al. 2009). In across Neotropical biomes. Biological order to confirm the association between Conservation 142(10):2002–2011. insect abundance and heavily impacted Cross, S. P. 1965. Roosting Habits of Pipistrellus urban areas, a study could examine this hesperus. Journal of Mammalogy 46(2):270. relationship in order to inform why bats may prefer more developed areas. These Frankie, G. W., & Ehler, L. E. 1978. Ecology of insects areas for further study could enhance our in urban environments. Annual Review of knowledge on the effect of anthropogenic Entomology 23(1):367–387. disturbance on bat activity as related to Franklin, A. B., Noon, B. R., & George, T. L. 2002. insects, to better assess the overall impact What is habitat fragmentation? Studies in Avian on biodiversity in other ecosystems. Biology 25:20–29.

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