Catch me if you can: Species interactions and moon - bioRxiv

Catch me if you can: Species interactions and moon - bioRxiv
bioRxiv preprint first posted online Oct. 22, 2018; doi: http://dx.doi.org/10.1101/449918. The copyright holder for this preprint
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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 – salvador@wii.gov.in


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


                                                                                                                                     1
Catch me if you can: Species interactions and moon - bioRxiv
bioRxiv preprint first posted online Oct. 22, 2018; doi: http://dx.doi.org/10.1101/449918. The copyright holder for this preprint
 (which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
                                   It is made available under a CC-BY 4.0 International license.




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
Catch me if you can: Species interactions and moon - bioRxiv
bioRxiv preprint first posted online Oct. 22, 2018; doi: http://dx.doi.org/10.1101/449918. The copyright holder for this preprint
 (which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
                                   It is made available under a CC-BY 4.0 International license.




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.




                                                                                                                                     3
Catch me if you can: Species interactions and moon - bioRxiv
bioRxiv preprint first posted online Oct. 22, 2018; doi: http://dx.doi.org/10.1101/449918. The copyright holder for this preprint
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                                   It is made available under a CC-BY 4.0 International license.




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




                                                                                                                                     4
Catch me if you can: Species interactions and moon - bioRxiv
bioRxiv preprint first posted online Oct. 22, 2018; doi: http://dx.doi.org/10.1101/449918. The copyright holder for this preprint
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                                    It is made available under a CC-BY 4.0 International license.




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-



                                                                                                                                      5
bioRxiv preprint first posted online Oct. 22, 2018; doi: http://dx.doi.org/10.1101/449918. The copyright holder for this preprint
  (which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
                                    It is made available under a CC-BY 4.0 International license.




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,

                                                                                                                                      6
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138    Kalmar, Sweden). Species were classified as diurnal (
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                                    It is made available under a CC-BY 4.0 International license.




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 (%)                         Classification
                                                                            Diurnal Nocturnal Crepuscular
             Large Carnivores
      1      Panthera tigris                         0.0367        269          39            50                12               Cathemeral
      2      Panthera pardus                         0.0417        298          58            35                 7               Cathemeral
      3      Cuon alpinus                            0.0099         56          66             9                25                Diurnal
      4      Ursus thibetanus                        0.0029         27          44            41                15               Cathemeral
             Medium Carnivore
      5      Neofelis nebulosa                       0.0011         7           14            86                 0           Mostly Nocturnal
             Small Carnivores
       6     Felis chaus                             0.0004          3           0           100                 0             Nocturnal
       7     Prionailurus bengalensis                0.0366        221          10            78                12           Mostly Nocturnal
       8     Viverra zibetha                         0.0303        209           5            88                 7           Mostly Nocturnal
       9     Viverricula indica                      0.0212        114           7            82                11           Mostly Nocturnal
      10     Paradoxurus hermaphroditus              0.0164        104          14            69                16             Cathemeral
      11     Herpestes auropunctatus                 0.0022         13          92             0                 8               Diurnal
      12     Herpestes edwardsii                     0.0017         10         100             0                 0               Diurnal
      13     Herpestes urva                          0.0088         62          89             3                 8               Diurnal
      14     Lutrogale perspicillata                 0.0018         10          70            30                 0            Mostly Diurnal
      15     Martes flavigula                        0.0023         16          75             0                25               Diurnal
      16     Melogale moschata                       0.0001          1           0           100                 0             Nocturnal
      17     Manis pentadactyla                      0.0002          1           0           100                 0             Nocturnal
             Large Prey
      18     Elephas maximus                         0.5696       4675          61            28                11            Mostly Diurnal
      19     Rhinoceros unicornis                    0.0029         21          14            86                 0           Mostly Nocturnal
      20     Bos gaurus                              0.3457       2949          48            39                13             Cathemeral
      21     Bubalus arnee                           0.0236        160          26            63                12             Cathemeral
      22     Axis axis                               0.0003          1           0             0               100             Crepuscular
      23     Muntiacus muntjak                       0.1492       1068          58            31                11             Cathemeral
      24     Hyelaphus porcinus                      0.0050         35          40            37                23             Cathemeral
      25     Rusa unicolor                           0.3395       2414          22            67                11             Cathemeral
      26     Sus scrofa                              0.2517       1685          80            11                 9            Mostly Diurnal
      27     Hystrix brachyura                       0.0564        319           4            83                13           Mostly Nocturnal
      28     Pavo cristatus                          0.0447        342          92             3                 5               Diurnal
             Small Prey
      29     Lepus nigricolis                        0.0082        52           12            81                 8           Mostly Nocturnal
      30     Caprolagus hispidus                     0.0002         1            0           100                 0             Nocturnal
      31     Macaca mulatta                          0.0451       317           87             1                12               Diurnal
      32     Macaca assamensis                       0.0010         8          100             0                 0               Diurnal
      33     Trachypithecus pileatus                 0.0014        10          100             0                 0               Diurnal
      34     Gallus gallus                           0.0853       574           75            10                15            Mostly Diurnal
      35     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

                                                                                                                                      10
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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




                                                                                                                                      11
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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).




                                                                                                                                      12
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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

                                                                                                                                      13
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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
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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
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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) 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


                                                                                                                                      17
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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,



                                                                                                                                      18
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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

                                                                                                                                      19
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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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