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Interspecific Feeding Association between Central Himalayan Langurs ( Semnopithecus schistaceus ) and Himalayan Black Bears ( Ursus thibetanus ), in a Temperate Forest of the Western Indian Himalayas

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One aspect of interspecific feeding associations is gleaning, or the acquisition of food resources by one species eating items that incidentally drop to the ground by another species while feeding. Gleaning is a widespread phenomenon between primates and ungulates, but primate-carnivore gleaning associations are extremely rare in the literature. While studying the behavior and ecology of the Central Himalayan langur (Semnopithecus schistaceus) in the alpine zone (3300 m–3500 m a.s.l.) of Rudranath, Kedarnath Wildlife Sanctuary, Uttarakhand State, India, we observed three direct instances and gathered indirect putative evidence of gleaning by Himalayan black bear (Ursus thibetanus) beneath large Quercus semecarpifolia trees with langurs feeding on acorns during the peak fruiting season. This is the first report of such a feeding association between langurs and bears, and the second for primates and carnivores.
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Mammal Study 43 (2018) DOI: 10.3106/ms2017-0033
© The Mammal Society of Japan Short communication
Interspecic feeding association between Central Himalayan langurs
(Semnopithecus schistaceus) and Himalayan black bears (Ursus
thibetanus), in a temperate forest of the Western Indian Himalayas
Himani Nautiyal* and Michael A. Human
Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506, Japan
Abstract. One aspect of interspecic feeding associations is gleaning, or the acquisition of food
resources by one species eating items that incidentally drop to the ground by another species while
feeding. Gleaning is a widespread phenomenon between primates and ungulates, but such primate–
carnivore gleaning associations are extremely rare in the literature. While studying the behavior and
ecology of the Central Himalayan langur (Semnopithecus schistaceus) in the alpine zone (3300 m–3500
m a.s.l.) of Rudranath, Kedarnath Wildlife Sanctuary, Uttarakhand State, India, we observed three
direct instances and gathered indirect putative evidence of gleaning by Himalayan black bear (Ursus
thibetanus) beneath large Quercus semecarpifolia trees with langurs feeding on acorns during the peak
fruiting season. This is the rst report of such a feeding association between langurs and bears, and the
second for primates and carnivores.
Key words: acorn consumption, commensalism, gleaning, high altitude, increased foraging eciency.
Interspecic feeding associations (IFAs) range from
closely related species to species from dierent orders,
and occur across a wide range of taxa (Stensland et al.
2003). Most of the documented relationships are mutual-
istic by nature, e.g., facilitating predator avoidance (Rasa
1983; Landeau and Terborgh 1986; FitzGibbon 1990;
Dickman 1992; Makenbach et al. 2013) or promoting
higher foraging eciency (Cody 1971; Székely et al.
1989; Oommen and Shanker 2010).
One type of IFA is gleaning, the acquisition of food
resources by one species picking up and eating items that
incidentally drop to the ground by another species while
feeding (Newton 1989). Gleaning associations involving
primates are abundant in the literature. To date, at least
174 dierent examples involving 64 primate species
(20 genera, seven families) and 95 non-primate species
(73 genera, 35 families) have been documented (see
Heymann and Hsia 2014). Primate–ungulate gleaning
associations, including bovids and cervids, are most com-
mon across both Africa and Asia (e.g., Morgan-Davies
1960; Elder and Elder 1970; Hill 1974; Whitten et al.
1988; Newton 1989; Tsuji et al. 2007, 2015; Ramesh et
al. 2012), with only one report from the Neotropics
( Agoramoorthy 1997). Apart from this, there are reports
of birds, reptiles, and sh (e.g., Glander 1979; González
Kirchner 1996; Sabino and Sazima 1999) gleaning foods
dropped by primates.
Gleaning shows a strong asymmetry in the type and
distribution of benets with the main benefactors usually
being the animals that gain access to food incidentally
dropped by foraging primates. ere is only one case of
gleaning reported between a carnivore, the golden jackal
(Canis aureus) and a primate, the Hanuman langur (S.
entellus), in the lower altitudes of central India (Newton
1985). e fruits of Ficus infectoria, Syzygium cumini
and Buchanania lanzan were incidentally dropped by
langurs and gleaned by golden jackals from the ground.
Although jackals may prey on young langurs, they are not
a threat to langurs in the trees.
Here, we describe three instances of gleaning
between high altitude living Central Himalayan langur
(Semnopithecus schistaceus) and Himalayan black bear
(U. thibetanus, Carnivora). Himalayan black bears are
known to eat langurs and even livestock when their pre-
ferred vegetable matter foods are scarce (Bishop 1975;
Sangay and Vernes 2008), making this a particularly
unique association. To the best of our knowledge, this is
the rst report of gleaning between primates and bears.
*To whom correspondence should be addressed. E-mail: himani.nautiyal.23w@st.kyoto-u.ac.jp
2 Mammal Study 43 (2018)
Materials and methods
is research was conducted in Rudranath (30.5°N,
79.3°E; 3400 m–3800 m a.s.l.) located in the Kedarnath
Wildlife Sanctuary (KWS), one of the largest designated
Protected Areas in the Chamoli-Rudraprayag district of
Uttarakhand, India. KWS covers an area of 975 km2
(Fig. 1). e study area was a high altitude alpine area,
consisting of two forest types: sub-alpine scattered tree
and scrub (2800 m–3400 m a.s.l.) and alpine meadows
and rocks (> 3400 m a.s.l.; Champion and Seth 1968). e
dominant tree species is oak, Q. semecarpifolia found in
the sub-alpine area.
e year in the study area is divided into three main
seasons; a cool and relatively dry winter (November to
March); a warm and dry summer (April to June); and a
warm and rainy monsoon period (July to September) with
transitional periods of February to March (Spring) con-
necting winter and summer, and October to November
(Autumn) connecting the rainy and winter seasons
( Gairola et al. 2010). e mean maximum temperature
between April and November in Rudranath is 15.1°C,
with a minimum temperature of 1.0°C. Mean relative
humidity ranges from 43% to 98% (Bisht et al. 2014). e
snow melts during April–May, producing an abundance
of soil moisture. e climate is harsh with low tempera-
tures, uctuating atmospheric pressure, blizzards and
hailstorms prevailing most months of the year. Even in
May, well before the beginning of the monsoon, cloud
and fog formation is common. In winter, snowfall is
heavy covering most of the study area (Billings 1973).
Our observations were made between June and Sep-
tember 2016. e campsite was 7 km from the survey
area, and we walked to the area daily along a xed trail.
e observations were carried out by four people on
any given day, searching for, following, and habituating
one troop of langurs, from morning (6 a.m.) to evening
(6 p.m.), independent of weather conditions. As part of
this daily routine, we systematically collected any in-
direct evidences of bears and their activity, i.e., scat,
feeding traces, scratch marks on trees, sleeping dens,
and footprints. Behavioural observations were carried
out by naked eye or through binoculars (Olympus 8 × 40)
for general activity (feed, travel, rest, play, social inter-
actions, and others) by 15-minute scan sampling at ve-
minute intervals (Altmann 1974). Activity for each visible
individual was recorded at the moment it was rst
observed. For individuals that were feeding during the
scan, we recorded food species and plant part eaten.
e langur study group contained ve adult males,
seven adult females, eight sub-adults, and six juveniles.
We spent a total of 468 hours (h) looking for and follow-
ing langurs and looking for signs of bear activity, and an
approximately equal number of hours were spent each
Fig. 1. The Kedarnath Wildlife Sanctuary in Chamoli-Rudraprayag district, Uttarakhand, India. The study area is indicated with a building icon
in the map which represents a Hindu temple.
Nautiyal and Human, Feeding association between Himalayan langurs and bears 3
month; June (109 h), July (118 h), August (127 h) and
September (113 h). All direct sightings of both species
were recorded.
Results
Langur feeding behavior
Langurs were observed to spend the majority of their
time feeding on Q. semecarpifolia, until the acorns were
almost totally nished at the end of September. Langurs
spent the rest of the time feeding on young leaves of
Betula utilis and Sorbus microphylla. Time spent feeding
on acorns was highest in July (61%) and lowest in Sep-
tember (6%, Table 1). In September, the langurs split up
into two groups. Only one of these sub-groups could be
found in the area, and they continued feeding on the
remaining acorns.
Fig. 2. Photographs suggesting the possible langur-bear association. a: bear den, dug out of a hollow standing tree; b: bear scat; c: bear footprints;
d: a juvenile of the Central Himalayan langur feeding on Quercus semecarpifolia acorns; e: ground nest made by bear, f: an adult female with her
cubs of the Himalayan black bear.
Table 1. Feeding activity of Central Himalayan langur and Himalayan black bear activity between 3300 m–3500 m a.s.l. at Rudranath
Month June July August September
% individuals feeding on acorns by langurs (total number of feeding
records in scan samples / month)
10.3 (58) 61 (359) 39.3 (351) 6 (200)
Direct bear sightings 0 23 0
Direct sightings of bear gleaning oak fruits under the langur feeding tree 0 2 1 0
Fresh bear scats encountered 125 32 6
Fresh tree scratch marks encountered 0 862
Fresh pugmark encountered 110 12 3
4 Mammal Study 43 (2018)
Direct evidences of bear gleaning
We encountered one adult female bear twice and sub-
adults three times (Fig. 2) in the month of July and August.
Gleaning by bears was observed only in July and August
(Table 1), the peak period for langur acorn consumption.
ree times we directly encountered bears gleaning
acorns of Q. semecarpifolia on the ground that were inci-
dentally dropped by langurs feeding above in the tree.
Coinciding with peaks in langur feeding on acorns, our
indirect evidence of Himalayan black bears in the study
area also increased in July and August (Table 1).
Indirect evidence of langur-bear association
We frequently found bear scat (Fig. 2) under acorn
trees where langurs had recently been observed feeding.
e scat consisted mostly of digested acorn matter, as
indicated by the pale, soft fecal matrix (Fig. 2).
Bear scat deposition and ground vegetation destruc-
tion, apparently, the result of searching for food, were
frequently found in the langurs’ home range area (Fig. 2).
Additionally, indirect evidence of bear activity in the
langur home range were four daily sleeping dens, dug out
of hollow standing trees and one ground nest with fresh
feces deposited nearby (Fig. 2). Partly attached broken
branches up in a tree, a sign of bear feeding, were never
observed, unlike what we commonly found at lower
elevations, 1500 m to 2500 m a.s.l. (Nautiyal, personal
observation).
Discussion
The nature of langur-bear gleaning interactions
e langur-bear feeding association described here
appears to be benecial for the bear to gain access to
fallen Q. semecarpifolia acorns. What makes this asso-
ciation perhaps unique from other reports involving pri-
mates however is the fact that Himalayan black bears are
potential predators of langurs, and have been reported to
kill langurs in neighboring Nepal (Bishop 1975). While
more observations are needed to make rm conclusions
about the benets and detriments of this association for
langurs, we think that the nutritional benets of gleaning
highly nutritious acorns by bears outweighs the risk and
energy expenditure of hunting, especially for females
with their cubs (see below), at this critical time of year in
Rudranath.
e black bear is normally omnivorous, but when food
is scarce they are known to sometimes hunt. In the situa-
tion we report here however, the relationship was about
getting seasonally available acorns fallen to the ground, a
favored high energy content food item (McDonald and
Fuller 2005). Quercus semecarpifolia is the dominant tree
of the sub-alpine and alpine forest between 2100 m and
3800 m a.s.l. (Singh and Singh 1992) and owering time
is typically in June and July, with August being the peak
fruiting period (Shrestha 2003). Bears select or shift habi-
tats based not only on the distribution of food-producing
plants, but also on the phenological development of these
food plants (Davis et al. 2006; Koike 2009). During our
study, langurs and bears were found together during the
short Q. semecarpifolia fruiting season (July and August).
As mentioned, the IFA described here involving females
and their cubs occurred in the month of July and August,
which is right before winter. For such bears acorns may
be an important nutritional source for accumulating fat in
preparation for the harsh winter ahead (Garshelis and
Steinmetz 2008).
In this situation, it seems necessary for bears to mini-
mize their expenditure of energy for foraging or hunting
to maximize energy and fat stores. If so, then we would
expect them to prefer the most easily available rich
resources for themselves and their cubs. Hunting agile
prey like langurs up in the canopy is not itself an easy task
which involves climbing up in these tree, balancing on
the thin branches to capture a langur. us, considering
energy management, bears should prefer to glean the
acorns rather than attempting to go after langurs high up
in the oak canopy at Rudranath.
Why glean instead of forage in the trees?
Why did not we see bears climb up into the trees to
forage on acorns themselves instead of gleaning them
from the ground under langur feeding trees? Based on the
observations reported here, we present three possible
non-exclusive hypotheses to help explain this.
1. Increased foraging eciency: In the alpine meadows
of Rudranath, food resources are scarce throughout the
year and negligible in the winter. Quercus semecarpifolia
is the dominant tree in the study area. During our study,
langurs and bears were found together during the short
Q. semecarpifolia fruiting season (July and August).
We noticed that the common feeding patches used by
langurs and bears had higher concentration of fruiting
Q. semecarpifolia trees as compared to other patches in the
study area. In principle, bears can climb up trees to get
acorns but the energetic cost involved in nding fruiting
trees, climbing up into them and taking acorns from the
terminal branches where they are found seems much
Nautiyal and Human, Feeding association between Himalayan langurs and bears 5
greater, compared to simply gleaning them from forest
oor. Following a langur troop and gleaning acorns on
the ground, may help bears, especially females with
young cubs (see below), to easily locate fruiting trees in
the forest, increase foraging success, and reduce energy
expenditure. is strategy adopted by bears could help
them to more eectively store energy needed to prepare
themselves, and their cubs, for the upcoming harsh winter.
2. Ospring protection: Infanticide is a widespread
behaviour by adult male bears and coincides with the
breeding season of Asiatic black bears from mid-June to
mid-August (our study period) (e.g., LeCount 1987;
Bellemain et al. 2006; Libal et al. 2011; Steyaert et al.
2013) It is reported that during each breeding season, sev-
eral males compete for breeding privileges with females.
e langur-bear IFA described here coincided with this
period of high risk of infanticide. For females with cubs,
it is probably a safer option to follow langurs and glean
the acorns from the forest oor, instead of leaving their
cubs vulnerable to possible infanticide by males on the
ground. At this stage, the cubs are too big to cling to
mother but too small to climb up large girthed, tall trees.
3. Risk of falling: At our site, timberline Q.
semecarpifolia are conspicuously wider girthed and taller
(average 225 cm diameter, 15 m height, n = 60) than at
the lower elevation Q. leucotrichophora (1500 m–2500 m
a.s.l.) in our study areas (average 87 cm diameter, 10 m
height, n = 40). Bears are generally good climbers, but
adults become too heavy to climb out onto to the termi-
nal branches where acorns are found. e risk of falling
for a bear seems to be considerably higher in these taller
trees, especially on terminal branches while reaching out
for acorns. At the lower elevation site, bears frequently
foraged and even built daily tree sleeping nests up in the
shorter and smaller girthed Q. leucotrichophora trees, but
this was simply never seen at Rudranath during our study
(Nautiyal, personal observation).
We propose that this IFA is not a chance encounter, but
rather an adaptive bear survival strategy, perhaps for
females in particular, to combat lean times when access to
highly nutritious food resources are scarce in high alpine
meadows of the Himalayas.
Acknowledgments: We thank our funding agency,
Ruord Small grant and the Forest Department of
Uttarakhand for giving us the required permission to
work in KWLS. We would also like to thank Anjana Dey,
Takhe Bamin, and Vinod Kumar for their assistance in
the eld. Finally, we are wholeheartedly grateful to the
local people for providing the team with all kinds of
logistical support. Their help was important for our
safety and survival in the harsh conditions of the higher
Himalayan region. We thank our anonymous reviewers
for their helpful comments.
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... These include conservation of soil from erosion and landslides, regulation of water flow in watersheds and maintenance of water quality in streams and rivers, (Singh and Singh, 1986;. However, they also serve as a major component of the natural habitat and as a key food resource for the wildlife in the region (Singh, 1981;Nautiyal and Huffman, 2018). To what degree these changes in the oak dominated forest affect the ecology and behavior of the wildlife inhabiting this landscape, is an emerging research topic with important implications for the formulation of wildlife management and conservation strategies. ...
... One of the pioneering studies conducted in the Indian Himalaya by Sugiyama (1976), for example, showed that Quercus incana fruits were the most important food resource for langurs in all six months of the study. Furthermore, for langurs inhabiting alpine meadows, where food resources are scarce throughout the year and negligible in winter, their main food, before the onset of harsh winter, was Quercus semecarpifolia (Nautiyal and Huffman, 2018). Minhas et al. (2010) suggested that Quercus incana was one of the essential species used both as sleeping trees and as an important food resource in both summer and winter by langurs in the Hindu Kush Himalayan range. ...
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Crop-foraging by primates is a rapidly growing concern. Effective mitigation strategies are urgently required to resolve this issue. In the Garhwal Himalayas, local people's high dependency on forest resources is a major cause of habitat loss, which paves the way for human-primate interactions in this area. To investigate the socioeconomic factors that might explain langur crop-foraging, we conducted structured interviews among 215 households in the Garhwal Himalayas India. We also examined langur resource use by monitoring their feeding and sleeping site activity. Less agricultural land, less agricultural production, and possession of large numbers of livestock significantly predicted villagers reporting crop-foraging events, although economic status of the correspondents did not have any effect. Perception of the villagers about reduction in forest resource was significantly affected by the amount of livestock possessed by the villagers. Our observations suggested that Banj oak Quercus leucotrichophora was the dominant species (59.2%, N = 306) in the pool of sleeping trees used by the langurs. Langurs also showed a preference in their use of sleeping sites and feeding sites, which were different from that expected by chance. Sleeping sites with high density of oak were re-used most frequently. Similarly, dense oak patches were also the preferred feeding patches. Thus, we suggest replanting of oak trees and conservation of intact oak patches, environmental education outreach, and empowerment of women in the community as potential mitigating factors to lessen the interaction between humans and langurs.
... Some methods are useful to have information on feeding habit of bears like direct sighting and collection of indirect feeding signs like feeding platform, claw mark on the food tree, scat analysis and indigenous knowledge of forest dwelling people to record the feeding habit of bears [10,22,25] . Direct and indirect observation were recorded of gleaning in Kedarnath Wildlife Sanctuary, Uttarakhand, India by Himalayan black bear beneath large Quercus semecarpifolia trees with langurs feeding on acorns during the peak fruiting season [18] . Attractions of Asiatic black bear towards human habitation are due to shrinkage and degradation of its habitat and these attractions are leading to increase Asiatic black bear-human conflict [20] . ...
... Similarly, Ali et al. reported 21 different types of food items in scats, with maximum frequency of occurrence (22.64%) for maize in the Kaghan valley, Pakistan [1] . Direct and indirect feeding observations were recorded of Himalayan black bear gleaning beneath large Quercus semecarpifolia trees with langurs (Semnopithecus schistaceus) in Kedarnath Wildlife Sanctuary, Uttarakhand, India [18] . Overall composition of feeding habit of black bear maximum on fleshy fruits like berries (31.58%) than easily available food item from crops (15.79%), similar value calculated for nut and livestock (7.89%) which were rich in fat contents. ...
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The Asiatic black bear (Ursus thibetanus) is one of the largest species found in the Greater Himalayan region and very few studies has conducted for investigation its status and feeding habits in the Himalaya. We assessed its occurrence along with altitudes and feeding habits in the Nanda Devi Biosphere Reserve (NDBR), Uttarakhand, India. We collected and analysed scats (n = 38), and based on scat analysis we identified 38 different types of food items, with maximum frequency of occurrence for Zea mays (50%) followed by Ribes himalense, Malus pumila, Honey Bees and Honey with similar frequency of occurrence (47.37%) and Phaseolus vulgaris (44.74%). We observed that maximum intake of food items by black bear from the Rosaceae family (41%) followed by the Poaceae family (14%). According to vegetation life form overall percentage of tree, shrub, herb and climber was 28.95%, 23.68%, 18.42% and 5.26% respectively and animal life form percentage of vertebrate, invertebrate and other was 10.53%, 5.26% and 7.89% respectively. We recorded four key types of bear signs (n = 192) from the NDBR; feeding signs (46.35%), claw/bite marks (24.48%), scats (19.79%) and direct sightings (9.38%). Maximum signs were encountered between 2501-3000 m altitude (38.02%) followed by between 3001-3500 m altitude (23.96%). Crop and livestock depredation shows the attraction of Asiatic black bear towards high risk human related food and this attraction is the key factor for human-black bear conflict in the reserve.
... A reduction of fear would be of benefit to the bear when competing for mates. Competition is high and interactions between males and females at mating time can be violent, as males are known to kill young cubs to induce females to resume reproductive cycling [51][52][53]. ...
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Associations among organisms are thought to form because the benefits, such as increased foraging efficiency or decreased risk of predation, outweigh any costs, such as resource competition. Though many interspecific associations have been described for closely related mammals, few studies have examined the associations between mammals in different orders. The yellow mongoose (Cynictus pencillata), a carnivore, and the Cape ground squirrel (Xerus inauris), a rodent, co-occur in arid and semi-arid South Africa where they share sleeping burrows, predators, a similar body size, and the capability to emit alarm calls in response to predators. To investigate enhanced predator avoidance as a potential benefit explaining the persistence of this association, we assessed individual mongoose vigilance alone and with squirrels or other mongooses, and with varying interspecific group size, using field observations. We also tested for responses to conspecific and heterospecific alarm calls in both study species using playback experiments. The proportion of time mongoose individuals spent vigilant decreased in the presence of squirrels or other mongooses and was negatively correlated with interspecific group size; a similar pattern was previously shown for conspecific groups of Cape ground squirrels. These results are predicted by both the dilution and collective detection hypotheses. In addition, hetero- and conspecific alarm calls elicited vigilance responses in both species. These results suggest that both species can benefit from the collective detection and dilution arising from their interspecific association and that this interspecific association could be mutualistic.
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