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.