ABSTRACT
The circadian rhythm is an adaptive biological process, allows organisms to anticipate daily environmental changes and implement appropriate strategies. Circadian rhythms play a crucial role in the health and survival of organisms. However, little is known concerning how intrinsic and extrinsic factors affect animal daily rhythms in the field, especially in nocturnal animals. Here, we investigated the emergence and return times of Vesperilio sinensis , and also integrated environmental conditions (temperature, humidity and light intensity) and biotic factors (reproductive status and predation risk) to determine causes of variation in the activity rhythms of the bats. We found that variation in the first emergence time, the mid-emergence time, and the final return time were distinct. The results demonstrated that the emergence and return times of bats were affected by light intensity, reproductive status, and predation risk in a relatively complex pattern. Light intensity had the greatest contribution to activity rhythms. Moreover, we first investigated the effects of actual predators on the activity rhythms of bats; the results showed that the mid-emergence time of bats was earlier as predators were hunting, but the final return time was later when predators were present. This challenges the traditional view that high predation risk leads to later emergence and earlier return. Finally, our results also highlighted the importance of higher energy demands during the lactation period in bats to variation in activity rhythms. These results improve our understanding of the patterns and causes of variation in activity rhythms in bats and other nocturnal animals.
Keywords: circadian rhythm, abiotic factors, biotic factors, reproduction status, predation, bats
INTRODUCTION
Circadian rhythms are endogenous patterns in the activity of organisms over periods of about 24 h, and they are universal, from prokaryotes to eukaryotes (Bell-Pedersen et al., 2005; McClung, 2000). It is commonly considered that circadian rhythms are adaptive biological processes that are crucial to the health and survival of organisms, as they allow organisms to anticipate the daily environmental changes and implement appropriate strategies (Caravaggi et al., 2018; Yerushalmi & Green, 2009). It is well known that global climate change has disrupted the activity rhythms of many animals (Levy, Dayan, Porter, & Kronfeld-Schor, 2018). Environmental conditions and biotic factors have been considered drivers of variation in the circadian activity rhythms of many vertebrates (Pita, Mira, & Beja, 2011). However, little is known concerning how intrinsic and extrinsic factors influence animal daily rhythms in the field (Quaglietta, Mira, & Boitani, 2018).
Activity rhythms are influenced by many abiotic and biotic factors, including light, moon phase, temperature, humidity, reproductive status, and predation risk (Tester & Figala, 1990). Light is an important modulator of organisms’ circadian rhythms (LeGates, Fernandez, & Hattar, 2014). Bright light conditions may present a dangerous situation for nocturnal animals, and the opposite would hold for day-active animals. For example, some nocturnal animals may decrease their activity during a full moon; this is known as “lunar phobia” (Mougeot & Bretagnolle, 2000; R. A. Saldaña-Vázquez & Munguía-Rosas, 2013). Extreme weather conditions could affect animals’ activity patterns to avoid overheating or hyperthermia, causing animals to reduce their activity during high- or low-temperature conditions (Foà & Bertolucci, 2001; Frick et al., 2012; Speakman, Hays, & Webb, 1994). Additionally, drought could affect animal and plant populations and constrain the activity of prey, thereby increasing the competition for food (Frick et al., 2012).
In addition to abiotic factors, biotic factors such as predation risk and reproductive status also may influence animals’ activity rhythms (Svensson et al, 2018). Predation risk is a strong selection pressure affecting activity rhythms, and predator avoidance is a major topic in animal evolution (John, 2013; Lima & O’Keefe, 2013). Animals face a tradeoff between predation risk and energy requirements when they decide to initiate activity during the period of day-to-night transition, especially for female animals during lactation, an energetically demanding period (Arndt., O’Keefe., Mitchell., Holmes., & Lima., 2018; Shiel & Fairley, 1999; Shuert, Halsey, Pomeroy, & Twiss, 2020). Females must balance increases in foraging time while maximizing food availability and minimizing the possibility of being captured by predators (Caro, 2005). In general, an earlier start to foraging activity may be beneficial (Pavey, Burwell, Grunwald, Marshall, & Neuweiler, 2001), but may also expose animals to a higher predation risk (Fenton et al., 1994; Jones & Rydell, 1994). Thus, a successful strategy requires the optimal adjustment between predation pressure and foraging activity in order to maximize energy intake (Caro, 2005). However, it remains unclear how animals adjust activity rhythms based on predation risk and energy requirement, especially during the lactation period.
Bats are an excellent system for investigating questions concerning the effects of abiotic and biotic factors on activity rhythms for the following reasons. First, as one of the most abundant mammal groups in terms of species and ecological diversity, bats are active almost exclusively during the night (Rydell & Speakman, 1995; Speakman, 1991). In this case, bats are sensitive to environmental changes, especially to light (Voigt & Kingston, 2016). Second, bats normally start nighttime activity for foraging after sunset, but not in total darkness (Lee & McCracken, 2001; Pavey et al., 2001). Like other animals, bats would benefit from an earlier emergence that would allow the bats to follow the activity peaks of some insects (i.e., Nematocera and other small flies) during dusk (Rydell, Entwistle, & Racey, 1996). Moreover, although earlier onset of activity would increase the amount of foraging time at dusk and dawn (Pavey et al., 2001), it would increase the chance of bats encountering diurnal predators that remain active around sunset, or even during dusk (Fenton et al., 1994; Lima & O’Keefe, 2013). However, this view was proposed based on an estimate of predation risk without actual predators. Thus, it is necessary to clarify the effects of natural predation and energy requirements for reproduction on the activity rhythms of bats. Finally, previous studies have focused on the effects of environmental factors such as temperature (Arndt. et al., 2018; Irwin & Speakman, 2003), cloud cover (Arndt. et al., 2018; Lee & McCracken, 2001; McAney & Fairley, 1988), heavy rain (McAney & Fairley, 1988) and light (Russo, LucaCistrone, & GarethJones, 2007) on the emergence of bats, but little is known concerning the impact factors affecting the return times of bats, or how interactions of abiotic and biotic factors influence the activity rhythms of bats.
In this study we monitored the emergence and return times of Asian particolored bats (Vesperilio sinensis ), and integrated environmental conditions (temperature, humidity and light intensity) and biotic factors (reproductive status and predation risk) to determine the sources of variation in activity rhythms of bats. We tested three hypotheses. First, we hypothesized that light intensity may play a pivotal role in influencing the emergence and return times of V. sinensis. Second, since bats during the lactation period have greater energy requirements, we hypothesized that V. sinensis would depart from the roost earlier during the lactation period than during the post- lactation period. Third, since bats should avoid predators, we hypothesized that V. sinensis would depart from the roost at dusk later, but return to the roost earlier at dawn in the presence of diurnal predators (e.g., falcons).