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).