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1

1 Title

2 Catch me if you can: Species interactions and moon illumination effect on mammals of tropical

3 semi-evergreen forest of Manas National Park, Assam, India

4 Bhatt U.M1, Habib B1, Sarma H.K2 & Lyngdoh S.L*1

5 Corresponding author – [email protected]

6 Department of Animal Ecology & Conservation Biology, Wildlife Institute of India, Dehradun 248001

7 Field Director, Govt. of Assam, Barpeta Road 781315

8 Abstract

9 Species interaction plays a vital role in structuring communities by stimulating behavioral

10 responses in temporal niche affecting the sympatric associations and prey-predator

11 relationships. We studied relative abundance indices (RAI) and activity patterns of each

12 species, temporal overlap between sympatric species, and effects of moon cycle on predator-

13 prey relationships, through camera-trapping in tropical semi-evergreen forests of Manas

14 National Park. A total of 35 species were photo-captured with 16214 independent records over

15 7337 trap nights. Overall, relatively high number of photographs was obtained for large

16 herbivores (11 species, n=13669), and low number of photographs were recorded for large

17 carnivores (five species, n=657). Activity periods were classified into four categories: diurnal

18 (day-time), nocturnal (night-time), crepuscular (twilight), and cathemeral (day and night time)

19 of which 52% records were found in diurnal period followed by 37% in nocturnal phase

20 whereas only 11% photographs during twilight. Small carnivores were strictly nocturnal

21 (leopard cat and civets) or diurnal (yellow-throated marten and mongooses); whereas large

22 carnivores were cathemeral (tiger, leopard, clouded leopard and Asiatic black bear). Analysis

.CC-BY 4.0 International licensewas not certified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (whichthis version posted October 22, 2018. . https://doi.org/10.1101/449918doi: bioRxiv preprint

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23 of activity patterns throughout the 24-h cycle revealed a high degree of temporal overlap

24 (>60%) among most of the sympatric species; however, differences in the activity peaks were

25 found between most of the species pairs. Moon phase was classified according to the

26 percentage of visible moon surface as new (0-25%), waxing (25-50%), waning (50-75%) and

27 full moon (75-100%). Moon phase did not have any correlation with activity of large carnivore

28 and large prey. The large carnivore followed the feed and starve pattern of cyclic activity. The

29 activity of small carnivore was influenced negatively by moonlight (partial correlation r = -0.221,

30 p<0.01). The result suggests that large carnivores were active non-differentially across moon

31 phases; however, small carnivores showed significantly high activity in darker nights. These

32 patterns indicate that small predators may differ their activity temporally as an anti-predator

33 strategy or otherwise to increase their foraging efficiency.

34 Keywords

35 Camera-trapping, tropical forest, temporal overlap, sympatric, moon phase, prey-predator

36 relationship

37 Introduction

38 Species interactions are one of the most studied areas in community ecology, as interspecific

39 behavior can largely regulate the composition and structure of community assemblages [1].

40 There are numerous studies about coexistence and resource partitioning between carnivores in

41 tropical forests [2,3], but few focuses on activity patterns and temporal segregation. For

42 carnivores, interspecific interactions are particularly relevant because of their role in the top-

43 down control and also serve as flagship species in the conservation of biodiversity in many

44 terrestrial ecosystems [4]. Though, given the vital role of consumers and through trophic

45 cascades, changes in the environment could promote an increase of medium-sized carnivores


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46 or mesopredators, due to top predator removal [5] which can cause substantial changes in the

47 dynamics of interaction among sympatric species [6], with adverse effects on subordinate

48 species. Thus, to minimize risks, subordinate species tend to avoid encounters with dominant

49 species [7], by modifying their activity patterns according to that of the dominant species [8].

50 Often, the prey tries to avoid the times when predators are more active [9] or segregate in other

51 niche dimensions [10].

52 Moon cycle is reported to play a significant role in activity changes, and several nocturnal

53 animals can alter their activity in response to moonlight variation [11]. Animals may adapt

54 their schedules throughout the circadian cycle to increase their fitness and allow their mutual

55 co-existence [12]. The dynamics between predators and prey depend on these adaptions too,

56 leading to a balance between their activity patterns [13]. For instance, some mammals, such as

57 rodents [11,14] and bats [15] are known to reduce their activity in brighter nights, allocate it to

58 darker periods of the night [16,17] or seek for covered areas [18,14]. This behavior is thought

59 to be due to an increment of predators hunting success during these nights [15,11,14,19,20].

60 On the other hand, other species, such as some primates [21] and some nocturnal birds [22] are

61 also known to be more active in brighter nights. This increment of activity may be related to

62 both higher predator awareness and increased food uptake success [21,22,]. Amongst abiotic

63 factors, moon cycle is reported to play an essential role in niche adaptions [11,10,23]. Several

64 nocturnal animals change their activity patterns [17,24] and habitat use [18,14,25] due to

65 moonlight and the level of that response classifies species as lunarphobic [15] or lunarphilic

66 [21]. Many species’ interaction with the lunar cycles remain still unknown, however, and a

67 better perception of the responses of other small and large sized mammals to moonlight is

68 therefore required for a full understanding of its effects.


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69 The tropical forest contains some of the highest levels of species diversity and abundance, but

70 many tropical species are cryptic, shy, and secretive, which makes them notoriously difficult

71 to study and their interactions with one another, remain poorly understood [26]. Recently

72 however with camera-traps, monitoring terrestrial rare, cryptic and secretive species in tropical

73 forests has become effective [27,28]. The technique has improved our ability to study terrestrial

74 movements of Asian tropical forest fauna [29], species diversity [30], the associations among

75 species [31], and their habitats [32]. In addition to recording the presence and abundance data

76 of such taxa, date and time of the captures can help in understanding the activity patterns of

77 carnivores and other mammals [29,33,34].

78 In the current study, we examine activity rhythms and effect of the moon cycle on mammals in

79 the semi-evergreen forest of Manas National Park, India, using camera traps. Objectives of the

80 study were to: 1) determine relative abundance indices (RAI) and species assemblage of MNP;

81 2) determine activity periods of each species; 3) quantify temporal overlap patterns between

82 species; and 4) investigate moonlight effect on the activity of sympatric species. Such data can

83 be used to study processes shaping ecological communities, especially whether potentially

84 competing species overlap or avoid each other temporally, and how larger species might

85 influence activity of their smaller cohorts in the same habitat. This information contributes to

86 an understanding of species interactions in tropical forests and should assist in developing more

87 suitable management and conservation strategies for forest communities in the Himalayan

88 foothills.

89 Materials and Methods

90 Study Area


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91 The study was carried out within the 500 km2 of Manas National Park (MNP) (26°35' - 26°50'

92 N, 90°45' - 91°15' E), a UNESCO World Heritage Site, in the state of Assam, India. Manas lies

93 on the borders of the Indo-Gangetic and Indo-Malayan biogeographical realms on a gentle

94 alluvial slope in the foothills of the Himalayas, where wooded hills give way to grasslands and

95 tropical forest. The elevation ranges between 40-170 m moll with an average of 85 m [35]; the

96 monsoon brings extremely heavy rainfall to this region, reaching up to 3,300 mm annually and

97 temperature ranges between 6-37 0C [35]. The park is home to a variety of important mammal

98 species, including the tiger, pygmy hog, hispid hare and Asian elephant [36] and also it supports

99 22 of India’s most threatened mammal species, as listed in Schedule-I of the Wildlife

100 (Protection) Act of India [37]. Together with the Royal Manas National Park in Bhutan, the

101 park forms one of the largest areas for conservation significance in South Asia, representing

102 the full range of habitats from the subtropical plains to the alpine zone [38]. MNP acquires a

103 special place from conservation aspect owing to its tropical forests, endemism and a long

104 history of social and political conflict [39]. The national park experienced a fifteen-year-long

105 ethnic and political battle starting in the mid-1980s until fledgling peace was restored in 2003

106 [40]. The violence during the conflict that followed caused large-scale damages to Manas and

107 left the park vulnerable to logging, local hunting, and poaching of important fauna, causing

108 habitat degradation and rapid loss of wildlife [41,42].

109 Methods

110 1. Field sampling design

111 Data on RAI and species assemblage was collected by deploying camera-traps (n=241) during

112 two sample periods: April 2017 to June 2017 (n=112) and December 2017 to May 2018

113 (n=129), with the whole area divided into a grid system of size 1×1 sq. km (Fig 1). The camera-


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114 trap locations were selected based on the presence of carnivore sign, accessibility, terrain

115 features, animal trails and nallahs (seasonal drainages). At each location, a single Cuddeback-

116 color™ digital camera was set by affixing it to trees at the height of approximately 30-45 cm

117 to above the ground. The cameras were triggered by motion sensor within a range of a conical

118 infrared beam and time lag of approximately 1s between the animal detection. Relative

119 abundance index (RAI) was calculated as the sum of all detections for each species for all

120 camera traps over all days, divided by the total number of camera trap nights, and then

121 multiplied by 100 [43]. To maintain statistical independence and to reduce bias caused by

122 repeated detections of the same species, one record of each species per half an hour per hours

123 per camera-trap site was considered as an independent detection and subsequent records were

124 removed [44]. No bait was used, to avoid disproportionate increases in the frequency of some

125 species [45].

126 Fig 1. Map of the study area (MNP) showing locations of camera traps (n = 241), grids,

127 drainage and forest cover.

128 2. Activity periods

129 The date and time printed on the photographs were used to describe diel activity periods of

130 each species. The assumption was made that the number of camera trap records taken at various

131 times is correlated with the daily activity patterns of mammals. The date and time printed on

132 the photographs were used to describe the daily activity patterns of the species. As some species

133 may be partly arboreal, and the camera-traps only recorded activity at ground-level, it is not

134 possible to assess arboreal activity. The observations were classified as diurnal, nocturnal,

135 cathemeral or crepuscular. Photos that captured an hour before and after sunrise and sunset

136 were defined as crepuscular [46]. Sunset and sunrise hours were determined using geographical

137 coordinates of the study area and the Moonphase SH software (version 3.3; Henrik Tingstrom,


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138 Kalmar, Sweden). Species were classified as diurnal (<10% of observations in the dark),

139 nocturnal (<90% of observations in the dark), mostly diurnal (between 10-30% of observations

140 in the dark), mostly nocturnal (between 70-90% of observations in the dark) and crepuscular

141 (50% of observations during the crepuscular phase), the rest of the species were classified as

142 cathemeral [47].

143 3. Activity analysis

144 Kernel density estimation curves were used to describe the activity patterns of each species; a

145 non-parametric way to estimate the probability density function of a distribution of records

146 which assumes that an animal is equally likely to be captured at any time as long as it is active

147 [47]. Overlap coefficients among the daily activity patterns of sympatric carnivores and

148 potential prey were estimated using Overlap package [47] for R-software version 3.1.2 (R

149 Development Core Team, 2011). Overlap coefficients (∆) is defined as the area under the curve

150 that is formed by taking the minimum of the two density functions at each time point ranging

151 from 0 (no overlap), if species have no common active period, to 1 (complete overlap), if the

152 activity densities of two species are identical [48]. The chosen estimator for overlapping was

153 Δ1 or Δ4, depending upon the sample size. Δ4 estimator for the coefficient of overlap was used

154 if both samples are larger than 50, whereas Δ1 was used for small sample size [47]. Data were

155 bootstrapped (99 samples) to extract 95% confidence intervals (CI) from the overlap

156 coefficients [26,49].

157 4. Moon phase

158 Moonphase SH software, version 3.3 was used to assess the effect of the moon phase on the

159 activity of mammals. The software classifies moon phase of records, according to the

160 percentage of visible moon surface, as follows: 0-25% [New Moon (New)], 25-75% [first


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161 quarter - Waxing Moon (Wx) & last quarter - Waning Moon (Wn)] and 75-100% [Full Moon

162 (Full)]. Then, the records from each moon phase were selected to assess the effect of the

163 moonlight and positioning on the time schedules of large – small carnivores and their potential

164 prey, during lunar cycle. One-way analysis of variance (ANOVA), Tukey HSD (honestly

165 significance difference) for Post-Hoc, and partial correlation tests were conducted to measure

166 the degree of association and pairwise comparisons among records of predator-prey in each

167 moon phase.

168 Results

169 1. Relative abundance indices & species assemblage

170 A total of 35 species were recorded with 16,214 independent records over the whole sampling

171 period of 7337 trap nights. The independent records (n) and relative abundance index (RAI)

172 for the photo-captured species varied from species-wise ranging from Neofelis nebulosa (n=7,

173 RAI=0.0011) to Panthera pardus (n=298, RAI=0.0417) for large – medium carnivores, from

174 Melogale moschata (n=1, RAI=0.0001) to Prionailurus bengalensis (n=221, RAI=0.0366) for

175 small carnivore, from Axis axis (n=1, RAI=0.0003) to Elephas maximus (n=4675,

176 RAI=0.5696) for large herbivores, and from Caprolagus hispidus (n=1, RAI=0.0002) to Gallus

177 gallus (n=574, RAI=0.0853) for small herbivores. The summarised photo captures with RAI

178 of all the species are given in table 1.

179

180

181

182

183


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184 Table 1. Activity periods of photo-captured species through camera-trapping in Manas

185 National Park, Assam, India.

SR No Species RAI N Photographic events (%) ClassificationDiurnal Nocturnal Crepuscular

Large Carnivores1 Panthera tigris 0.0367 269 39 50 12 Cathemeral2 Panthera pardus 0.0417 298 58 35 7 Cathemeral3 Cuon alpinus 0.0099 56 66 9 25 Diurnal4 Ursus thibetanus 0.0029 27 44 41 15 Cathemeral

Medium Carnivore5 Neofelis nebulosa 0.0011 7 14 86 0 Mostly Nocturnal

Small Carnivores6 Felis chaus 0.0004 3 0 100 0 Nocturnal7 Prionailurus bengalensis 0.0366 221 10 78 12 Mostly Nocturnal8 Viverra zibetha 0.0303 209 5 88 7 Mostly Nocturnal9 Viverricula indica 0.0212 114 7 82 11 Mostly Nocturnal10 Paradoxurus hermaphroditus 0.0164 104 14 69 16 Cathemeral11 Herpestes auropunctatus 0.0022 13 92 0 8 Diurnal12 Herpestes edwardsii 0.0017 10 100 0 0 Diurnal13 Herpestes urva 0.0088 62 89 3 8 Diurnal14 Lutrogale perspicillata 0.0018 10 70 30 0 Mostly Diurnal15 Martes flavigula 0.0023 16 75 0 25 Diurnal16 Melogale moschata 0.0001 1 0 100 0 Nocturnal17 Manis pentadactyla 0.0002 1 0 100 0 Nocturnal

Large Prey18 Elephas maximus 0.5696 4675 61 28 11 Mostly Diurnal19 Rhinoceros unicornis 0.0029 21 14 86 0 Mostly Nocturnal20 Bos gaurus 0.3457 2949 48 39 13 Cathemeral21 Bubalus arnee 0.0236 160 26 63 12 Cathemeral22 Axis axis 0.0003 1 0 0 100 Crepuscular23 Muntiacus muntjak 0.1492 1068 58 31 11 Cathemeral24 Hyelaphus porcinus 0.0050 35 40 37 23 Cathemeral25 Rusa unicolor 0.3395 2414 22 67 11 Cathemeral26 Sus scrofa 0.2517 1685 80 11 9 Mostly Diurnal27 Hystrix brachyura 0.0564 319 4 83 13 Mostly Nocturnal28 Pavo cristatus 0.0447 342 92 3 5 Diurnal

Small Prey29 Lepus nigricolis 0.0082 52 12 81 8 Mostly Nocturnal30 Caprolagus hispidus 0.0002 1 0 100 0 Nocturnal31 Macaca mulatta 0.0451 317 87 1 12 Diurnal32 Macaca assamensis 0.0010 8 100 0 0 Diurnal33 Trachypithecus pileatus 0.0014 10 100 0 0 Diurnal34 Gallus gallus 0.0853 574 75 10 15 Mostly Diurnal35 Lophura leucomelanos 0.0232 164 54 18 28 Mostly Diurnal

Total (N) 16214 52 37 11


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186 2. Activity periods of photo-captured species

187 Activity periods for 35 species depicts that the boundaries between the categories (diurnal,

188 nocturnal, cathemeral or crepuscular) of activity periods are not sharp (Table 1). However,

189 some animals restrict their routine activities to either the light or the dark phase, and rare

190 observations in the other period may represent activity elicited by unusual circumstances.

191 (i). Carnivores: Small carnivores were either mainly nocturnal such as Prionailurus

192 bengalensis, Viverra zibetha, and Viverricula indica, or diurnal such as Martes flavigula,

193 Lutrogale perspicillata, Herpestes urva, Herpestes auropunctatus and Herpestes edwardsii;

194 whereas Paradoxurus hermaphroditus with 69% photographs in the dark phase fell under the

195 cathemeral category (Table 1). Out of the five large – medium carnivore species; three large

196 body-sized mammals (Panthera tigris, Panthera pardus, and Ursus thibetanus) were

197 cathemeral, Cuon alpinus was diurnal, and Neofelis nebulosa was found with nocturnal nature

198 (Table 1).

199 (ii). Herbivores: Large herbivores were either mainly cathemeral such as Bos gaurus,

200 Bubalus arnee, Muntiacus muntjak, Hyelaphus porcinus, and Rusa unicolor, or diurnal such as

201 Elephas maximus, and Sus scrofa (Table 1). The only large herbivore tending toward

202 nocturnality was the Rhinoceros unicornis (Table 1). Terrestrial birds (Gallus gallus, Lophura

203 leucomelanos, Pavo cristatus) and primates (Macaca mulatta, Macaca assamensis,

204 Trachypithecus pileatus) were diurnal; whereas the routine activity of hares (Lepus nirgicolis,

205 Caprolagus hispidus) and Himalayan crestless porcupine (Hystrix brachyura) suggested

206 nocturnal nature of the species (Table 1).

207 3. Activity pattern and temporal overlap between sympatric

208 species


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209 (i). Small carnivores: Eight small carnivores were sufficiently common to evaluate their

210 diel activity pattern (Fig 2). Civets and leopard cats were active during night hours; whereas

211 mongooses and yellow-throated martens were active during the daytime (Fig 2). All four

212 nocturnal small carnivores had shown high temporal overlap between them, with the highest

213 overlap was found between leopard cat and small Indian civet with an overlap coefficient,

214 Δ4=0.93 (±0.15), followed by leopard cat and large Indian civet (Δ4=0.90); whereas least

215 overlap (Δ4=0.74) was found between large Indian civet and palm civet (Fig 2). Leopard cat

216 had a strong bimodal pattern, with a stronger peak at around 23:00 hr and a less pronounced

217 peak from about 01:00 to 04:00 hr. Large Indian civet also showed the bimodal pattern as it

218 increases post-sunset and reaches its peak at around 22:00 hr and then starts to decline; again,

219 it starts rising post-midnight and reaches its peak at about 01:00 hr and then begins to fall (Fig

220 2). Other two civets (small Indian civet and Asian palm civet) had also shown a bimodal

221 pattern, but with differences in peaks; less pronounced peaks for both the species were between

222 19:00 to 23:00 hr and 03:00 hr, whereas stronger peaks were about at 04:00 hr and 17:00 to

223 22:00 hr respectively (Fig 2). High temporal overlap was found between all the four diurnal

224 small carnivores, with the highest coefficient value of Δ1=0.84 (±0.09) between crab-eating

225 mongoose and yellow-throated marten, followed by crab-eating mongoose and grey mongoose

226 (Δ1=0.77); whereas least coefficient value (Δ1=0.54) was found between small Indian

227 mongoose and yellow-throated marten (Fig 2). Small Indian mongoose showed a unimodal

228 pattern, and it increases post 05:00 hr and reaches its peak at around 11:00 hr and then starts to

229 decline gradually until 18:00 hr (Fig 2). Grey mongoose, crab-eating mongoose, and yellow-

230 throated marten were active throughout the light phase, had a bimodal activity pattern, with a

231 stronger peak at 06:00, 15:00 and 16:00 hr, whereas less pronounce peak at 15:00, 08:00 and

232 06:00 hr respectively (Fig 2). Melogale moschata (n=1), Felis chaus (n=3), and Lutrogale


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233 perspicillata (n=10) had the fewest detections and therefore, were not considered for activity

234 analysis (Table 1).

235 Fig 2. Temporal overlap among small carnivores in Manas National Park, Assam, India.

236 Individual photograph times are indicated by the short vertical lines above the x-axis. The

237 overlap coefficient (Δ1 / Δ4) is the area under the minimum of the two density estimates, as

238 indicated by the shaded area in each plot. The abbreviations of species’ names are CEM-Crab-

239 eating Mongoose, SIM-Small Indian Mongoose, GM-Grey Mongoose, YTM-Yellow Throated

240 Marten, LC-Leopard Cat, LIC-Large Indian Civet, SIC-Small Indian Civet, and PC- Palm

241 Civet.

242 (ii). Large carnivores: Among the activity patterns of large carnivores, tigers and leopards

243 showed the highest daily activity overlap Δ4 = 0.82 (± 0.03) for any 2 species of top carnivores

244 in the study area, followed by leopards and Asiatic black bears (Δ1 = 0.82); whereas lowest

245 overlap Δ1 = 0.10 (± 0.07) was found between clouded leopards and dholes (Fig 3). Leopard

246 was active throughout the day and night but was more active during daylight, with peaks in the

247 early morning and late afternoon; tiger had also shown cathemeral activity pattern but was least

248 active from about 10:00 to 15:00 hr (Fig 3). Two activity peaks (between 21:00 and 23:00 hr

249 and between 2:00 and 4:00 hr) were observed for clouded leopards, suggesting a bimodal

250 activity pattern of the species (Fig 3). Dholes, showed a unimodal pattern of activity, with

251 peaks between 06:00 to 09:00 hr (Fig 3). However, Asiatic black bears were relatively

252 cathemeral, with 44% of their photo-captures obtained during daytime and 41% records

253 obtained during night-time; whereas least activity was observed between 20:00 to 02:00 hr

254 (Table 1, Fig 3). A synchronized least-active pattern was noted between midnight and 03:00 hr

255 for all the detected large carnivores (Fig 3).


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256 Fig 3. Temporal overlap among large carnivores in Manas National Park, Assam, India.

257 Individual photograph times are indicated by the short vertical lines above the x-axis. The

258 overlap coefficient (Δ1 / Δ4) is the area under the minimum of the two density estimates, as

259 indicated by the shaded area in each plot. The abbreviations of species’ names are T-Tiger, L-

260 Leopard, CL-Clouded Leopard, WD-Wild Dog, and ABB-Asiatic Black Bear.

261 (iii). Carnivores and their prey: High temporal overlap was found among nocturnal

262 prey species such as Indian hare with leopard cats and civets whereas red junglefowl, and kalij

263 pheasant was active during the daytime, hence had shown large overlaps with mongooses and

264 yellow-throated marten (Fig 4a). Activity patterns of large carnivores and its prey showed

265 variable temporal overlap with the highest overlap between tiger and wild buffalo (84%)

266 followed by sambar (84%), hog deer (84%), and gaur (79%) (Fig 4b). In case of leopard highest

267 overlap was found with hog deer (76%) followed by gaur (74%), barking deer (72%) and wild

268 buffalo (72%) (Fig 4b). Clouded leopard had shown highest overlap with Himalayan crestless

269 porcupine (66%), followed by sambar (65%) whereas dhole had maximum overlap with wild

270 boar (52%) and barking deer (50%) (Fig 4b). Chital (n=1) and hispid hare (n=1) had only one

271 detection and therefore, were not considered for the analysis (Table 1).

272 Fig 4. Pairwise temporal overlap (Δ1 / Δ4) between (a) small carnivore vs. prey and (b)

273 large carnivore vs. prey in Manas National Park, Assam, India. The bars indicate

274 percentage temporal overlap among carnivore species with potential prey and the whiskers

275 above the bars indicate standard errors.

276 4. Moon phase effect on prey-predator relationship

277 Photographs of large carnivores, small carnivores, and potential prey species were analysed

278 during four moon cycles (New, Wx, Full, and Wn) (Fig 5). Differences were observed in

279 carnivore community with respect to the moon cycle, with highest records of large carnivores


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280 in full moons except for dhole while small carnivores had more photographs at new moon

281 phase, except for Asian palm civet (Fig 5). Dhole activity was found mainly diurnal with only

282 9% photographs in nocturnal periods, out of which around 58% records were recorded in darker

283 nights (Fig 5). On the other hand, Asian palm civet had more photographs in full moon (33%);

284 and 21% photographs were recorded in new moon phase (Fig 5). All three photo-captured small

285 prey such as red junglefowl, kalij pheasant, and Indian hare had more photographs in the new

286 moon phase (Fig 5). Larger prey showed almost uniform activity in all moon phases, with

287 highest records in new moon (wild buffalo, hog deer, wild boar, Himalayan crestless porcupine

288 and Indian peafowl); whereas the remaining three species (gaur, barking deer and sambar) had

289 more photographs in a full moon (Fig 5).

290 Fig. 5. The proportion of nocturnal records of (a) small carnivore vs. prey, (b) large

291 carnivore vs. prey, and (c) large carnivore vs. small carnivore in different moon phases

292 in Manas National Park, Assam, India. The bars indicate species records in different moon

293 phases. The dashed line is to separate small carnivore and their prey, large carnivore and their

294 prey, large carnivore and small carnivore respectively.

295 One-way ANOVA result pointed significant difference only for small carnivore (F= 5.007,

296 p<0.005) and for small prey (F= 3.697, p<0.05). In case of small carnivores, the Tukey’s HSD

297 for post-hoc result showed significant more records in new moon (mean differences= 1.52,

298 p<0.005) and waning moon (mean differences= 1.38, p<0.05) than in full moon. For small

299 prey, more photo-captures were recorded in waxing moon (mean differences= 1.21, 1.49;

300 p<0.05) than in new moon and waning moon respectively.

301 The results of the partial correlation depicted a negative relation between small carnivore and

302 moon visible surface while controlling for small prey (r= -0.221, p<0.001) and large carnivore

303 (r= -0.213, p<0.01) (Table 2). However, Pearson's product-moment correlation also known as


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304 the zero-order correlation showed statistically significant, negative correlation between small

305 carnivore and moon visible surface (r= -0.205, p<0.01), without controlling for small prey or

306 large carnivore. This suggests that small prey or large carnivore had very little influence in

307 controlling the relationship between small carnivore and moon visible surface.

308 Table 2. Partial correlation test (r) for degree of association between prey-predator and

309 moon visible surface using different control variables in Manas National Park, Assam,

310 India.

311 ***. Partial correlation is significant at the 0.001 level (2-tailed).

312 **. Partial correlation is significant at the 0.01 level (2-tailed).

313 *. Partial correlation is significant at the 0.05 level (2-tailed).

314

Control VariablesMoon Visible Surface

Small Carnivore

Large Prey

Small Prey

Correlation -0.221*** 1.000 - -

Significance (2-tailed) 0.001 - - -

Small Prey

Small Carnivore

df 210 0 - -

Correlation - 0.227*** 0.462*** -

Significance (2-tailed) - 0.001 0.000 -

Large Carnivore

df - 210 210 -

Correlation - 1.000 - 0.232***

Significance (2-tailed) - - - 0.001

Moon Visible Surface

Small Carnivore

df - 0 - 210

Correlation 1.000 -0.213** - -

Significance (2-tailed) - 0.002 - -

Large Carnivore

Moon Visible Surface

df 0 210 - -


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315 Discussion

316 The current study provides baseline information on activity patterns and temporal overlaps of

317 mammals of Manas National Park as well as it is also the first of its kind of research on moon

318 illumination and effect of moon phases on prey-predator interactions in tropical forests of India.

319 Results from the present study are mainly concordant with basic accounts of natural history

320 (i.e., whether a species is most active during the day or night) [50]. We also compared our

321 results with those of previous studies on species body size, activity pattern and temporal

322 overlaps of mammalian fauna. The lunar cycle results largely showed that the moonlight has a

323 stronger effect on the activity of the prey than on the behavior of the predator.

324 Evaluation of the camera trapping data revealed that the study area had a healthy habitat for

325 the mammalian fauna. All the major fauna from MNP was photo-captured during the survey

326 confirming 35 species. Out of the 35 recorded species, 1 (Chinese pangolin) is classified as

327 Critically Endangered, 6 (tiger, dhole, Asiatic elephant, wild water buffalo, hog deer and hispid

328 hare) are classified as Endangered, 8 (leopard, clouded leopard, Himalayan black bear, one-

329 horned rhinoceros, gaur, sambar and capped langur) are classified as Vulnerable, 1 (Assamese

330 macaque) is classified as Near Threatened while the remaining 19 species are classified as least

331 concern [51]. The previous camera-trapping studies in Manas National Park provides

332 information on relative abundances of tigers and their prey [52], carnivore diversity [53], and

333 density estimation of carnivores and herbivores [40]. Recently, Borah et al. [54] provide info

334 on density estimation of common leopard and clouded leopard; whereas Lahkar et al. [55]

335 explained about diversity, distribution and photo-capture rate of mammals of MNP. In the

336 present study, we examine activity rhythms and the lunar cycle effect on the mammalian fauna

337 in the semi-evergreen forest of Manas National Park.


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338 1. Diel activity patterns and temporal overlap

339 Van Schaik and Griffiths [29] explained variation in activity periods for Indonesian rainforest

340 mammals using species body size as the primary factor influencing activity patterns. The theory

341 suggests that smaller mammals (<10 kg) tend to be specifically nocturnal or diurnal as an anti-

342 predation strategy, whereas larger mammals (>10 kg) are more cathemeral because of energy

343 requirements and associated feeding commitments. The intensive camera-trap survey provided

344 one of the most detailed studies of activity periods in mammals of MNP under natural

345 conditions and classified activity patterns into four categories [29]. In the present study, all the

346 photo-captured small mammals are found to be mainly nocturnal (jungle cats, leopard cats, and

347 civets) or diurnal (smooth-coated otter, yellow-throated marten, and mongooses), as predicted

348 by the van Schaik and Griffiths model. The results showed that the medium-sized mammals

349 are cathemeral (barking deer, hog deer, and wild boar) and diurnal (wild dog), and the larger-

350 sized mammals such as tiger, leopard, Asiatic black bear, gaur, wild buffalo, and sambar are

351 active during both day and night hours which is also in accordance with the Schaik and Griffiths

352 model.

353 We found differences in the activity peaks of tiger and leopard, but there was no active temporal

354 separation between predators probably owing to their similar morphology and hunting

355 strategies [2]; however, significant time overlap between them was evident. Tigers are

356 opportunistic predators [56] and had considerably higher activity overlap (>75%) with gaur,

357 wild buffalo, sambar and hog deer [57,58]. However, their diet includes birds, fish, rodents,

358 insects, amphibians, reptiles in addition to other mammals such as primates and porcupines

359 [56]. The present study also found higher overlap (>65%) with Himalayan crestless porcupine

360 as compared to leopard’s overlap. Leopard’s activity overlapped (>70%) with all the prey

361 species ranging from medium to large sized prey [59,60]. Leopard showed higher temporal


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362 overlaps with medium-sized prey [60] such as barking deer in comparison with tiger’s overlap.

363 Asiatic black bear tends to be diurnally active [61] or crepuscular [62]. The current study found

364 cathemeral nature of the species as it has to spend most of its time in search of food for energy

365 requirements under a very high competition with conspecifics (for vegetal food/and animal

366 matter) as well as other carnivores (for the animal matter) [63].

367 The study showed that clouded leopard activity was predominantly nocturnal, similar to the

368 studies of Gumal et al. [64], and Azlan & Sharma [65] from Peninsular Malaysia, and also

369 Kanchanasaka [66], and Grassman et al. [67] from Southern Thailand. Austin et al. [68]

370 recorded activity peaks at crepuscular hours in two radio-collared clouded leopards. However,

371 the overall activity pattern from radio-telemetry studies (n=4) indicated two peaks at 18:00-

372 02:00 hr and 08:00-12:00 hr [69]. The present study also found a bimodal pattern but with

373 different peaks at 21:00-23:00 hr and 2:00-4:00 hr. In case of its prey, the study found the high

374 temporal overlap with sambar and Himalayan crestless porcupine [57] as compared to the other

375 prey species. It is possible that clouded leopard terrestrial activity is higher at night-time due

376 to the avoidance of leopards in the study area being more active on trees during daytime (A.

377 Wilting, pers. comm). However, studies suggest clouded leopards be more terrestrial [70,71,72]

378 with the use of trees primarily for resting [70,73]. The low capture rate of 7 photos in 7337 trap

379 nights in our study, does not necessarily reflect low numbers of the felid, but rather a decreased

380 probability to capture it along wildlife trails and roads that are frequented by high numbers of

381 leopards and tigers, the top predator of the area. The species is known to use a dimension that

382 was not covered in our sampling, namely trees higher up than 60 cm above ground [74].

383 The only canid species recorded during the study was wild dog (dhole). Dholes showed less

384 temporal overlap with their dominant competitors (tiger, leopard and clouded leopard) because

385 they were more active during the daytime and crepuscular hours and less active in full darkness,


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386 similar to most other studies of India and Southeast Asia (67,75,76,77]. Dholes’ diet includes

387 a wide variety of prey species, ranging from small rodents and hares to gaur [2,78,76,79]. In

388 tropical semi-evergreen forests of Southeast Asia, the species appear to persist in smaller packs

389 and consume medium-sized prey [75], as smaller packs are more energetically advantageous

390 in the rainforest where large prey species are scarce, thick vegetation favors stalk and ambush

391 hunting techniques over cursorial hunting, and competition with tiger and leopards [80]. The

392 present study also found the high temporal overlap of dhole with medium-sized prey such as

393 barking deer and wild boar as compared to other large-sized prey.

394 The present study recorded the two small cats (leopard cat and jungle cat) to be strictly

395 nocturnal which is consistent with other reported studies only in case of leopard cat [81,82],

396 yet there are studies contradicting nocturnality of leopard cats (83,65,84]. According to Prater

397 [81], jungle cat is diurnal as well as crepuscular and can even kill porcupine species which are

398 nocturnal. In this study, jungle cat is found to be strictly nocturnal as reported by Majumder et

399 al. [85], though our result is insignificant because of only three captures of a jungle cat. The

400 small Indian civets and large Indian civets are found active in nocturnal hours which is

401 consistent with other reported studies [86,87]; whereas with 69% photographs in darker hours

402 of Asian palm civet also supports other study of Duckworth [88] and Azlan [89] which suggests

403 crepuscular or nocturnal nature of the species. Mongooses are predominantly diurnal or

404 cathemeral [90] and the present study found a strictly diurnal pattern for all the three photo-

405 captured mongooses. The yellow-throated marten was completely a diurnal species in the study

406 area [91] but can hunt both by day and night and also known to attack young deer species [81].

407 On the other hand, results of the current study showed a Himalayan crestless porcupine as a

408 nocturnal species which is consistent with the previous studies by Menon [92]. Indian hare

409 which is mainly active during crepuscular and nocturnal hours [93] are found to be active only

410 in nocturnal phase in this study. According to several studies [13,94], the diel activity of many


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411 felids is associated with the activity pattern of their prey. The main reason of these small cats

412 being nocturnal in the study area could be that rodents (Himalayan crestless porcupine) and

413 hares (Indian hare and hispid hare), their primary preys, are generally nocturnal [81,94]

414 although we could not quantify this point through camera trapping for small-sized prey.

415 2. Do species respond differently to moonlight?

416 Moonlight has usually been thought to increase predation risk by enhancing the ability of

417 predators to detect prey [14,95], therefore leading to decreased activity or shifts in prey

418 foraging efficiency in the presence of bright moonlight [16,96,97]. The results of the present

419 study demonstrate that the effects of moon illumination on activity across nocturnal mammal

420 species. The response of nocturnal mammals to the moonlight differs among taxa and may vary

421 according to several determinants, such as phylogeny, trophic level, sensory systems and

422 habitat type [13,97]. The current study suggests that the moon phases are also likely to

423 influence how prey distribute their activities through time to face different predation risk

424 periods.

425 Large-sized prey species activity were not significantly affected by moon phases as they

426 showed uniform activity with highest record of photographs in new moon (wild buffalo, hog

427 deer, wild boar, Himalayan crestless porcupine and Indian peafowl) and full moon (gaur,

428 barking deer and sambar) (Figs 5 and 6b). Large carnivore did not get influenced by moonlight

429 as they follow the feeding and starvation pattern of cyclic activity across a lunar cycle (Fig 6a).

430 We, therefore, suggest that large carnivores switch their type of prey, they hunt in different

431 moon phases, their hunting efficiency increases in the full moon and the greater foraging

432 benefits they take in brighter nights as they are more photo-captured during a full moon (Fig

433 5).


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434 Small-sized prey species were more active during brighter nights to avoid predation risk against

435 smaller carnivores (Fig 5). This anti-predator behavior is already well recognised for the

436 species such as marsupials and rodents [33]. However, statistics showed that moonlight did not

437 influence the activity of small prey (Fig 6d). Small carnivores displayed a higher level of

438 activity during the darker nights when reduced brightness hampers their visual detections by

439 large carnivores which were active more in brighter nights (Fig 5). Tukey and partial

440 correlation tests also highlighted that moonlight had negative influence on the small carnivore

441 activity; their activity decreases with an increasing moonlight intensity (Fig 6c, Table 2).

442 Fig. 6. Photo-captures of (a) large carnivore, (b) large prey, (c) small carnivore, and (d)

443 small prey in a lunar cycle in Manas National Park, Assam, India. The bars indicate

444 percentage moon visible surface in a complete lunar cycle. The lines indicate average records

445 in each day from all 7 lunar cycles, and the whiskers above and below the lines indicate

446 standard errors.

447 Conclusion & limitation

448 Our result suggests that despite historical ethnopolitical conflict and continued threats in some

449 areas, MNP supports a diversity of mammalian fauna of conservation concern, including

450 clouded leopards, dholes, tigers and other species. Adaptations are bidirectional and take place

451 over at least two dimensions: spatial and temporal [9,98] and our study focuses primarily on

452 the temporal component and provides some interesting insights into the diel activity patterns

453 and temporal overlap among mammals of MNP. The current study also highlights the

454 significance of incorporating moon illumination into movement and activity pattern of

455 mammals as well as interactions between prey-predator in tropical forests of India. The brighter

456 hours or full moon lights shows an inverse relation in the activity pattern of prey and predator.


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457 Camera trapping is effective in recording species interaction but with certain limitations such

458 as the inability to account for detection probability, which is bound to vary with species [76].

459 Placement of camera traps should be done depending on size, habitat and activity pattern of

460 species. Like in our study, some of the species are at least partially, or even predominantly,

461 arboreal such as clouded leopard, small prey and primate species. Hence, activity patterns of

462 such species would be better explained if camera-traps were deployed in species-specific

463 habitats. Moonlight effects were not only related to the trophic level and were better explained

464 by phylogenetic relatedness, visual acuity, and habitat cover.

465 Acknowledgements

466 We thank the director, dean & research co-ordinator, wildlife institute of India. We are thankful

467 to the Doyil Vengayil & Syed Asrafuzzaman, Department of Science and Technology,

468 Government of India to carry out the study on the clouded leopard (Neofelis nebulosa).

469 Paniram, Tapan, Anukul, Dipul, Dipen and Dilli are thanked for their assistance in the field.

470 We thank the Dept., Environment & Forests, Govt., of Assam, field staff of Manas National

471 Park, for permissions and field support.

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