Mammal Study 43 (2018) DOI: 10.3106/ms2017-0033
© The Mammal Society of Japan Short communication
Interspecic 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. Human
Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506, Japan
Abstract. One aspect of interspecic 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 eciency.
Interspecic feeding associations (IFAs) range from
closely related species to species from dierent 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 eciency (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 dierent 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 benets 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: email@example.com
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 Human, 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
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
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
The nature of langur-bear gleaning interactions
e langur-bear feeding association described here
appears to be benecial 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 benets and detriments of this association for
langurs, we think that the nutritional benets 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
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
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 eciency: 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 Human, 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 eectively store energy needed to prepare
themselves, and their cubs, for the upcoming harsh winter.
2. Ospring 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,
Ruord 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.
Agoramoorthy, G. 1997. Apparent feeding association between
Alouatta seniculus and Odocoileus virginianus in Venezuela.
Mammalia 61: 271–273.
Altmann, J. 1974. Observational study of behaviour: sampling methods.
Behaviour 49: 227–267.
Bellemain, E., Zedrosser, A., Manel, S., Waits, L. P. and Taberlet, P.
2006. The dilemma of female mate selection in the brown bear, a
species with sexually selected infanticide. Proceedings of the
Royal Society B 273: 283–291.
Billings, W. D. 1973. Arctic and alpine vegetation: Similarities, dier-
ences and susceptability to disturbance. Bioscience 23: 697–704.
Bishop, N. 1975. Social Behavior of Langur Monkeys (Presbytis entellus)
in a High Altitude Environment. Doctoral Dissertation. University
of California, Berkeley, California, 213 pp.
Bisht, V. K., Kuniyal, C. P., Bhandari, A. K., Bhagwati, P., Nautiyal, B.
P. and Prasad, P. 2014. Phenology of plants in relation to ambient
environment in a subalpine forest of Uttarakhand, western
Himalaya. Physiology & Molecular Biology of Plants 20: 399–
Champion, H. G. and Seth, S. K. 1968. A Revised Survey of the
Forest Types of India. Government of India Publications, New
Delhi, 516 pp.
Cody, M. L. 1971. Finch ocks in the Mohave Desert. Theoretical
Population Biology 2: 142–158.
Davis, H., Weir, R. D., Hamilton, A. N. and Deal, J. A. 2006. Inuence
of phenology on site selection by female black bears in coastal
British Columbia. Ursus 17: 41–51.
Dickman, C. R. 1992. Commensal and mutualistic interactions among
terrestrial vertebrates. Trends in Ecology & Evolution 7: 194–197.
Elder, W. H. and Elder, N. L. 1970. Social groupings and primate
associations of the bushbuck (Tragelaphus scriptus). Mammalia
FitzGibbon, C. D. 1990. Mixed-species grouping in Thomson’s and
Grant’s gazelles: the anti-predator benets. Animal Behaviour 39:
Gairola, S., Sharma, S. K., Rana, C. S., Ghildiyal, S. K. and Suyal, S.
2010. Phytodiversity (Angiosperms and Gymnosperms) in
Mandal-Chopta Forest of Garhwal Himalaya, Uttarakhand,
India. Nature and Science 8: 1–17.
Garshelis, D. L. and Steinmetz, R. (IUCN SSC Bear Specialist Group)
2008. Ursus thibetanus. The IUCN Red List of Threatened Spe-
cies. DOI: e. T22824A9391633.
Glander, K. E. 1979. Feeding associations between howling monkeys
and basilisk lizards. Biotropica 11: 235–236.
González Kirchner, J. P. 1996. Asociaciones poliespecícas entre
aves y primates en Guinea Ecuatorial. Tomo Extraordinario, 125.
Aniversario de la Real Sociedad Española de Historia Natural
Heymann, E. W. and Hsia, S. S. 2014. Unlike fellows—a review of
primate-non-primate associations. Biological Review 90: 142–156.
Hill, G. 1974. Observations on a relationship between crested Guinea-
fowl and vervet monkeys. Bulletin of the British Ornithologists
Club 94: 68–69.
6 Mammal Study 43 (2018)
Koike, S. 2009. Fruiting phenology and its eect on fruit feeding
behavior of Asiatic black bears. Mammal Study 34: 47–52.
Landeau, L. and Terborgh, J. 1986. Oddity and the ‘confusion’ eect in
predation. Animal Behaviour 34: 1372–1380.
LeCount, A. L. 1987. Causes of black bear cub mortality. International
Conference for for Bear Research and Management 7: 75–82.
Libal, N. S., Belant, J. L., Leopold, B. D., Wang, G. and Owen, P. A.
2011. Despotism and risk of infanticide inuence grizzly bear
den-site selection. PLOS ONE 6(9): e24133. DOI: 10.1371/
Makenbach, S. A., Waterman, J. M. and Roth, J. D. 2013. Predator
detection and dilution as benets of associations between yellow
mongooses and Cape ground squirrels. Behavioral Ecology and
Sociobiology 67: 1187–1194.
McDonald, J. J. E. and Fuller, T. K. 2005. Eects of spring acorn
availability on black bear diet, milk composition, and cub sur-
vival. Journal of Mammalogy 86: 1022–1028.
Morgan-Davies, A. M. 1960. The association between impala and
olive baboon. Journal of the East African Natural History Society
Newton, P. N. 1985. A note on golden jackals (Canis aureus) and their
relationship with hanuman langurs (Presbytis entellus). Journal of
the Bombay Natural History Society 82: 633–636.
Newton, P. N. 1989. Associations between langur monkeys (Presbytis
entellus) and chital deer (Axis axis): chance encounters or
mutualism? Ethology 83: 89–120.
Oommen, M. A. and Shanker, K. 2010. Shrewd alliances: mixed
foraging associations between treeshrews, greater racket-tailed
drongos and sparrow hawks on Great Nicobar Island, India.
Biology Letters 6: 304–307.
Ramesh, T., Kalle, R., Sankar, K. and Qureshi, Q. 2012. Langur—chital
association in Mudumalai Tiger Reserve, Western Ghats. Zoo’s
Print 27: 15–17.
Rasa, O. A. E. 1983. Dwarf mongoose and hornbill mutualism in the
Taru desert, Kenya. Behavioral Ecology and Sociobiology 12:
Sabino, J. and Sazima, I. 1999. Association between fruit-eating sh
and foraging monkeys in western Brazil. Ichtyological Explora-
tion of Freshwaters 10: 309–312.
Sangay, T. and Vernes, K. 2008. Human-wildlife conict in the
Kingdom of Bhutan: Patterns of livestock predation by large
mammalian carnivores. Biological Conservation 141: 1272.
Shrestha, T. K. 2003. Wildlife of Nepal. B. Shrestha Publisher,
Singh, J. S. and Singh, S. P. 1992. Forests of Himalaya: Structure,
Functioning and Impact of Man. Gyanodaya Prakashan, Nainital,
Stensland, E., Angerbjörn, A. and Berggren, P. 2003. Mixed species
groups in mammals. Mammal Review 33: 205–223.
Steyaert, S. M. J. G., Reusch, C., Brunberg, S., Swenson, J. E.,
Hackländer, K. and Zedrosser, A. 2013. Infanticide as a male
reproductive strategy has a nutritive risk eect in brown bears.
Biology Letters 9: 20130624. DOI: 10.1098/rsbl.2013.0624.
Székely, T., Szép, T. and Juhász, T. 1989. Mixed species ocking of
tits (Parus spp.) a eld experiment. Oecologia 78: 490–495.
Tsuji, Y., Shimoda-Ishiguro, M., Ohnishi, N. and Takatsuki, S. 2007. A
friend in need is a friend indeed: feeding associations between
Japanese macaques and sika deer. Acta Theriologica 52: 427–434.
Tsuji, Y., Widayati, K. A., Nila, S., Hadi, I., Suryobroto, B. and
Watanabe, K. 2015. “Deer” friends: feeding associations between
colobine monkeys and deer. Journal of Mammalogy 96: 1152–
1161. DOI: 10.1093/jmammal/gyv123.
Whitten, A. J., Mustafa, M. and Henderson, G. S. 1988. The Ecology
of Sulawesi. Gadjah Mada University Press, Yogyakarta, 779 pp.
Received 16 April 2017. Accepted 15 December 2017.
Editor was Naofumi Nakagawa.