Introduction
Worldwide, 69 % of mammals are nocturnal while 20% are exhibiting more
diurnal activity patterns (Bennie et al., 2014), and this phenomena is
an ancestral character stemming from the ‘nocturnal bottleneck’ in the
early evolution of the clade (Hut et al., 2012). Although synapsids
invaded the nocturnal niche 100 million years prior to mammals, recent
studies support the essential nocturnality of ancestral mammals, by way
of selection for dim-light vision (“night vision”), endothermy, and
loss of UV protection (Angielczyk and Schmitz, 2014, Wu et al., 2017).
The time it takes for the moon to complete one revolution around the
earth relative to the sun (29.5 days) is known as the synodic period or
lunar month (Häfker and Tessmar-Raible, 2020). The familiar cycle of
lunar phases is affected by alterations in the visible portion of the
moon illuminated by the sun (Andreatta and Tessmar-Raible, 2020), with
the intensity of lunar illumination on the Earth’s surface at night
varying by three orders of magnitude over a full lunar cycle (Kyba et
al., 2017). Moreover, other factors such as topography, cloud cover,
latitude, and distance from the moon, each play a role in influencing
the intensity of lunar illumination in any given space. Nocturnal
organisms can react directly to changes in lunar illumination as the
moon cycles through the phases, and they can also anticipate variations
that go along with the lunar cycle by means of an endogenous oscillator
(“clock”) synchronized to the 29.5 day circalunar rhythm (Raible et
al., 2017).
The primary environmental cue that changes with the lunar cycle is
moonlight intensity (Andreatta and Tessmar-Raible, 2020, Häfker and
Tessmar-Raible, 2020), and these cues (or ‘zeitgebers’) act on
endogenous oscillators to adjust biological processes such as mating,
feeding, activity, predator avoidance and many others (Andreatta and
Tessmar-Raible, 2020). The idea that being afraid of the dark is an
adaptation to dodge predation has a long history (Darwin, 1871), and
moonlight cycles as a cue for predation risk was first studied in
nocturnal desert rodents several decades ago (Lockard and Owings, 1974).
Animals’ circadian activity patterns are influenced by evolution (Halle,
2000) and physiology (Heurich et al., 2014), and we find that prey
species with powerful tapeta (and therefore, have superior night vision)
tend to be lunar philic (light lovers) whereas species deficient a
tapetum lucidum (i.e., have poor night vision) are more lunar phobic
(light avoiding) or uninfluenced by lunar phase (Prugh and Golden,
2014). According to the ‘predation risk hypothesis’ (Huck et al., 2017),
if predators are more successful at chasing under bright moonlight, prey
species will alter activity to become “lunar phobic” or avoid brighter
moon phases. On the contrary, the ‘visual acuity hypothesis’ (Huck et
al., 2017, Pratas‐Santiago et al., 2017) states that the brightness of a
full moon provides “visually-oriented” prey species heightened chance
to forage and/or detect danger, with the result that they are expected
to be more active during the full moon, showing “lunar philic”
activity, in other words preferring brighter moon phases.
Besides lunar illumination, the activity patterns of large carnivores,
such as felids, are also influenced by anthropogenic disturbances
(Gaynor et al., 2018, Van Cleave et al., 2018). For example, studies
have shown that leopards (Panthera pardus ) in Thailand
(Ngoprasert et al., 2007) and Amur tigers (Panthera tigris
altaica ) and leopards (Panthera pardus orientalis ) in China
(Yang et al., 2018b, Zhao et al., 2020) shift their activity patterns
under the effect of human disturbance to become more nocturnal or
crepuscular and avoid human activity across spatiotemporal scales to
decrease the risk of conflict with humans (Treves and Karanth, 2003,
Wang et al., 2019).
Furthermore, the landscape of fear created by predator may linked to
prey behavioral resource depression and their changing in temporal
foraging movement (Bischof et al., 2014). Further to temporal activity
patterns also altering in habitat resources selection into different
seasons (Ramesh et al., 2012, Yang et al., 2018b), hence spatial
separation is another strategy for the coexistence of sympatric species
(Yang et al., 2018b, Zhao et al., 2020, Davis et al., 2018).
The North China leopard (P. p. japonensis ), hereafter leopard,
their distribution and ecology is very scarce or unidentified and also
has been classified as Critically Endangered on the IUCN Red List
(Jacobson et al., 2016). Basic information about how various ecological
factors influence leopard and prey species co-occurrence under different
lunar phases is still unknown in China and the current research aims to
fill this gap. The aims of the current study were to examine the
temporal activity patterns of leopards, prey species and human-related
activities or habitat factors and the influence of lunar illumination.
Specifically, we tested the following three hypotheses: 1) the effects
of different moon phases on nocturnal spatio- temporal overlap intensity
will be distinct among different predator-prey pairs; 2) habitat factors
influence the activity response of prey to leopards during the four moon
phases, and; 3) predator and prey species shift their temporal activity
patterns during the full moon higher activity during the day time to
counter the brightness of the moon at night time.