Few studies have explicitly examined the effects of lunar cycle on temperate bats in North America (Hecker, Brigham, 1999, Baerwald, Barclay, 2011, Arndt et al., 2018, Negraeff, Brigham, 1995, Whiting et al., 2021). Herein we not only examined lunar cycle, but also the effect and masking interaction of ALAN. We found that five bat species (eastern red bat, hoary bat, silver-haired bat, southeastern myotis, and evening bat) had lower acoustic activity when the amount of moon illumination increased in the environment without ALAN pollution. Two of these species, the hoary bat and silver-haired bat, were examined in previous studies (Hecker, Brigham, 1999, Baerwald, Barclay, 2011). Contrary to our results, these studies did not find that the amount of moon illumination affected bat acoustic activity (Hecker, Brigham, 1999, Baerwald, Barclay, 2011) or emergence time (Arndt et al., 2018, Whiting et al., 2021). One major difference between our study and others is that we used data from year-round monitoring for over a decade whereas previous studies had only a few months of data, primarily in the summer. The difference in sampling scope might affect the ability to detect a quantitative pattern. Additionally, our large dataset allowed us to limit our investigation to nights with a cloudless sky, potentially removing the masking effect of clouds, which most previous studies did not do. Lastly, all previous studies examining the effects of moonlight on temperate bats in North America were conducted at more northern latitudes, and a global meta-analysis of bat lunar phobia suggests that lunar phobia is less likely to be detected as absolute latitude increases (Saldaña-Vázquez, Munguía-Rosas, 2013).
The global meta-analysis also suggests that species-specific foraging habitat preferences can affect how bats respond to lunar cycles (Saldaña-Vázquez, Munguía-Rosas, 2013). Bats foraging over water are more likely to be affected by moonlight due to high risks of being preyed upon (Saldaña-Vázquez, Munguía-Rosas, 2013). Several of our long term monitoring sites were established over water bodies (Parker et al., 2020), which might explain lunar phobia detected in our study. A few recent studies in South America also reported species-specific responses to lunar cycles (Appel et al., 2017, 2019, Vásquez et al., 2020, Gomes et al., 2020). Fast-flying species with long, narrow wings such as the Mexican free-tailed bat might be less likely to respond to lunar cycle than slow-flying species with short, broad wings due to the ability of escaping from predators (Appel et al., 2017, 2019, Vásquez et al., 2020). Our results on the Mexican free-tailed bat supported previous studies. However, our results on the hoary bat, an open space forager (Blakey et al., 2019), showed lunar phobia, which is contradictory to existing knowledge that open space foraging species are not likely to respond to lunar cycle (Musila et al., 2019, Saldaña-Vázquez, Munguía-Rosas, 2013). Such contradiction highlights the need to further investigate the mechanism of bats’ responses to lunar cycle.
Regarding how bat activity patterns within a night varied with lunar cycle, we found that bat activity was delayed when more moonlight was present in the ALAN absent environment, which is consistent with previous studies (Appel et al., 2017, Vásquez et al., 2020). The eastern red bat, hoary bat, silver-haired bat, evening bat, tricolored bat, and Mexican free-tailed bat showed increased activity in the second half of the night on full moons when compared to new moons. The big brown bat, evening bat, and tricolored bat showed increased activity in the second half of the night on waxing moons compared to waning moons. These results support bat lunar phobia in the ALAN absent environment. Species-specific diel activity pattern has been recognized a long time ago and explained by niche partitioning (Kunz, 1973). Recent studies found that such overnight patterns could be affected by urbanization and related anthropogenic disturbances (Schimpp et al., 2018, Li et al., 2020), which is one of the sources of ALAN.
The intensity of ALAN is at least 10 times stronger than the most intense moonlight and masks any effect of moonlight (Davies et al., 2013). To our knowledge, only one study (Mariton et al., 2022) has explicitly examined how bat activity patterns within a night differed among moon phases under the effects of ALAN pollution. In our study, we found robust evidence of ALAN altering bat lunar relationships, masking the effects of lunar cycle on nightly and within-night bat activity patterns. Across nights, we found that the eastern red bat, hoary bat, southeastern myotis, and evening bat no longer responded to varying moonlight intensity with ALAN presence. We also found that the big brown bat showed an increase in activity at ALAN present sites as the moonlight intensity increased across nights. Within a night, the delayed activity pattern on full moon or waxing moon nights disappeared in the big brown bat, hoary bat, evening bat, and tri-colored bat when ALAN was present. This is consistent with the only study that showed ALAN masking the delaying effect of moonlight within a night in the Serotine bat (Eptesicus serotinus, Mariton et al., 2022).
Not all bat lunar relationships identified in our study were affected by ALAN pollution. For nightly response to the amount of moon illumination, the silver-haired bat displayed lunar phobia independent from the ALAN condition. For the delayed activity within a night on a full or waxing moon, several species showed a delayed activity pattern at the ALAN present sites. The primary explanation for bat lunar relationships is that moonlight could alter the perceived predation risk for bats, their prey, and their predators (Saldaña-Vázquez, Munguía-Rosas, 2013, Lima, O’Keefe, 2013). Several empirical studies have demonstrated how insects responded to lunar cycles thus affecting food availability for bats (Lang et al., 2006, Kolkert et al., 2020). However, studies on the activity in relation to moonlight of bats’ nighttime aerial predators, such as owls and other birds of prey, are still lacking. Furthermore, the underlying physiological and behavioral mechanism of bat lunar relationships is unclear. It is unknown whether bats use moonlight as a visual cue or a circadian clock is involved as suggested in other animals responding to lunar cycle (Kronfeld-Schor et al., 2013). Since we found varying effects of ALAN on bat lunar relationships, we speculate that different species might have different mechanisms for lunar cycle responses or that intrinsic mechanisms differentially interact with light levels. To investigate mechanisms, studies should use both field methods to monitor bat predators and laboratory methods to simulate light conditions (Tidau et al., 2022).
Independent from lunar chronobiology, our study also examined the effects of ALAN on bat acoustic activity. Surprisingly, nine out of ten species showed higher acoustic activity at the ALAN absent sites than at the ALAN present sites. The most extreme example is the northern long-eared bat, a forest interior species and slow flyer, which was never recorded at any ALAN bright sites. Only a few studies have examined the effect of ALAN on North American temperate bats. Two separate field experiments artificially lit naturally dark areas, and both found that big brown and little brown bats avoided lit sites (Seewagen, Adams, 2021, Cravens, Boyles, 2019). Additionally, one of the studies also found the silver-haired bat to avoid lit sites (Seewagen, Adams, 2021). No effect of ALAN was found on the eastern red bat, hoary bat, evening bat, or tricolored bat in these studies (Seewagen, Adams, 2021, Cravens, Boyles, 2019). In a study focusing on urban bats that might have somewhat adapted to ALAN in the city, scientists found that the big brown bat, eastern red bat, and silver-haired bat showed higher levels of activity at brighter sites in response to increased insect availability (Li, Wilkins, 2022). However, their activity was still limited by the spatial clutter, which affected foraging habitat suitability (Li, Wilkins, 2022).
No regional multiple-landscape scale study has explicitly examined the effect of ALAN across different light conditions on North American temperate bats. Generally, ALAN is associated with urban environments (Davies et al., 2013, Falchi et al., 2011, Doll et al., 2006, Falchi et al., 2016). Two regional multiple-landscape scale studies on bats and urbanization showed that the big brown bat, silver-haired bat, and Mexican free-tailed bat had higher levels of activity as the degree of urbanization increased (Li, Kalcounis-Rueppell, 2018, Li et al., 2019). However, both of those studies used the mobile transect survey technique to monitor bats right after sunset and did not compare the bat activity throughout a whole night. It is possible that urban dwelling bats were only active in the city immediately after sunset and would leave the city to forage in more natural conditions (Schimpp et al., 2018, Aguiar et al., 2021). Our results demonstrate that ALAN is likely to negatively affect bats at the regional multiple-landscape spatial scale and reduce habitat quality even for species that might be somewhat light tolerant, echoing recent findings on European bats (Russo et al., 2019, Mariton et al., 2022, Straka et al., 2021).
It is worth noting that we found the little brown bat to be lunar-philic regardless of the ALAN condition and the big brown bat to be lunar-philic at ALAN present sites. Similar lunar philia has been reported in South American bats, such as Tadarida brasiliensis in central Chile (Vásquez et al., 2020) and Molossus molossus in French Guiana (Gomes et al., 2020). We suspect that such results might come from interspecific competition among bats. In-flight social interactions, such as making competition warning calls has been documented in the big brown bat, evening bat, and Mexican free-tailed bat when multiple species were present at a quality foraging site (Springall et al., 2019). When a site changes from dark to bright temporarily due to the lunar cycle or permanently due to ALAN pollution, the bat community structure might change accordingly by limiting light-sensitive specie from accessing the site (Willems et al., 2022, Russo et al., 2019). Competitive interactions among bats should be emphasized in future studies on ALAN or lunar chronobiology.
We were unable to assess whether bats may have switched from echolocation to vision in the presence of light in our study. Using vision for foraging when sufficient illumination is available has been documented in bats (Eklöf, Jones, 2003, Gutierrez et al., 2014, Danilovich et al., 2015). Bats may also be silent or reduce acoustic activity in other behavioral processes since echolocation production is energy demanding (Currie et al., 2020, Corcoran et al., 2021). Our study used acoustic methods alone and therefore we cannot assess scenarios where bats alter their acoustic behaviors when light is present; rather we assume that lower calls mean less activity. Future studies should consider using other monitoring techniques such as video recording in combination with acoustic monitoring to investigate the effects of ALAN or lunar cycle on bats, ideally in a controlled experimental setting.
In the ALAN absent environment, any reduced bat foraging success (regardless of mechanism) on bright nights of full moon, can be compensated for by higher foraging activities on dark nights of new moon. In contrast, ALAN associated with human settlements is generally constant and relatively permanent. There is the need to further investigate the long term physiological consequences of ALAN exposure and examine health conditions of ALAN impacted bats. As urbanization accelerates worldwide (United Nations, 2019), conservation actions towards ALAN are needed. Efforts can be made to alter the ALAN spectrum (Lewanzik, Voigt, 2017, Spoelstra et al., 2017) or improve urban forestry (Straka et al., 2019, Li et al., 2020). However, attention should also be paid to anthropogenic environments that are traditionally dark, such as agricultural lands.
Temperate bats provide tremendous benefits of ecosystem services via pest control in agricultural environments (Boyles et al., 2011). Due to climate change and socioeconomics, there is a trend of increased agricultural activities including harvesting, equipment transportation and set up, field prep and maintenance, irrigation, and pesticide applications at night. Even though there is no governmental data or scientific research to document how many growers have adopted nighttime farming, legislation has been made to require sufficient illumination for worker safety (e.g., DIR, California, 2020). Such farming practices might change ALAN conditions in agricultural environments, reducing bat activity and ecosystem service in these areas.