Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 August 2021 | 13(9): 19246–19253
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
https://doi.org/10.11609/jott.7510.13.9.19246-19253
#7510 | Received 09 June 2021 | Final
received 28 July 2021 | Finally accepted 09 July 2021
First record of interspecies
grooming between Raffles’ Banded Langur and Long-tailed Macaque
Zan Hui Lee 1, Andie Ang
2 & Nadine Ruppert 3
1,2,3 School of Biological Sciences, Universiti Sains Malaysia, 11800
USM, Penang, Malaysia.
1,2,3 Malaysian Primatological
Society, No 14, Lorong Nuri 3/1, Taman Nuri, 09000, Kulim, Kedah, Malaysia.
2 Raffles’ Banded Langur Working
Group, Mandai Nature
2 IUCN SSC Primate Specialist Group
(Asia)
3 IUCN SSC Primate Specialist Group
(Section Small Apes)
1 zanhui96@gmail.com, 2 andie.ang@colorado.edu,
3 n.ruppert@usm.my (corresponding author)
Abstract: In primates, observations of
interspecies grooming are not uncommon, especially between species of the same
genus. However, little is reported about grooming between different genera and
less is discussed about its ecological significance. Here, we report the first
sighting of Long-tailed Macaques grooming the Critically Endangered and rare
Raffles’ Banded Langur during two independent events at Gunung
Lambak Recreational Forest in Kluang,
Malaysia.
Keywords: Interspecies interactions, Macaca fascicularis,
Malaysia, Presbytis femoralis,
primate, Singapore.
Editor: Mewa Singh, University of Mysore,
Mysuru, India. Date of publication: 26 August
2021 (online & print)
Citation: Lee, Z.H., A. Ang & N. Ruppert (2021). First record
of interspecies grooming between Raffles’ Banded Langur and Long-tailed
Macaque. Journal of
Threatened Taxa 13(9): 19246–19253. https://doi.org/10.11609/jott.7510.13.9.19246-19253
Copyright: © Lee et al. 2021. Creative Commons Attribution
4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: World Wide Fund for
Nature (Singapore and Malaysia) disbursed
through the Malaysian Primatological Society,
Universiti Sains Malaysia Gra-ASSIST scheme, and Mandai Nature.
Competing interests: The authors
declare no competing interests.
Author details: Lee Zan
Hui is a postgraduate
student in Zoology at Universiti
Sains Malaysia who focuses on primate ecology and behaviour.
He is a trained environmental
scientist with interest in spatial ecology and conservation of wildlife and their
habitats. Andie Ang is a primatologist studying Asian colobines and chairing the
Raffles’ Banded Langurs Working Group, Singapore.
She is a research scientist
with Mandai Nature and a visiting researcher to School of Biological Sciences,
Universiti Sains Malaysia and member of the IUCN SSC Primate Specialist Group (Asia). Nadine Ruppert
is a zoologist focusing on primates, human-wildlife interactions, plant-animal interactions, and conservation issues related to Malaysia. She is a senior lecturer at Universiti Sains Malaysia, vice president of
the Malaysian Primatological Society and member
of the IUCN SSC Primate
Specialist Group Section on Small Apes.
Author contributions:
conceptualisation—NR; field work
and data analysis—ZHL; first manuscript draft—ZHL;
manuscript corrections—NR, AA; advisory
role—AA.
Acknowledgements: We are grateful to the Department
of Wildlife and National Parks Peninsular Malaysia for granting the research
permit (P-00183-15-19 issued to NR) to study the behaviour of Raffles’ Banded
Langurs at Gunung Lambak
and to the funders of this study: World Wide Fund (Singapore and Malaysia)
disbursed through the Malaysian Primatological
Society, Universiti Sains
Malaysia Gra-ASSIST scheme, and Mandai
Nature.
introduction
Most primate species are highly
social, and behaviour like allogrooming, alloparenting, and playing between members of the same
species are regularly observed in langurs and macaques (Lehman et al. 2007;
Matsuda et al. 2015). Social grooming is a key behaviour in primates to
facilitate kinship reciprocity (Schino & Aureli 2010), affiliation (Dunbar 1991; Lehman et al.
2007), and hygiene (Goosen 1981), involving at least
two actors (groomer and recipient) physically touching each other. As an
affiliative interaction, grooming plays a significant role in primate societies
to reinforce social bonds and networks (Dunbar 2011). Grooming also facilitates communication,
contributing to the development of social cohesion (Dunbar 2011; Dunbar &
Lehman 2013; Grueter et al. 2013). Within social
groups of macaques, post-conflict reconciliation and consolation often involve
grooming (Long-tailed Macaques Macaca fascicularis: Cords 1992; Stump-tailed Macaques M. arctoides: Call et al. 2002; Barbary Macaques M. sylvanus: McFarland & Majolo
2011). Social grooming has a direct effect on the physiological health of
individuals, and other positive effects are associated with release of pleasure
hormone (i.e., oxytocin and endorphin; Dunbar 2010) or suppression of stress
hormones (i.e., cortisol: Wooddell et al. 2016).
Seyfarth (1977) proposed that social
grooming in female Cercopithecidae is principally
directed toward high-ranking individuals (reviewed in Schino
2001). This rank-related reciprocity in allogrooming
has been demonstrated for 16 species and nine genera (Alouatta,
Cercopithecus, Cebus, Erythrocebus,
Lemur, Macaca, Miopithecus,
Sapajus and Semnopithecus)
(Schino & Aureli 2008a;
Tiddi et al. 2012). Evidence of trading allogrooming for alloparenting is
also found in female Long-tailed Macaques (Gumert
2007).
Asymmetries in allogrooming resemble the context of ecological economy as
a trade for other commodities including food (reviewed in Barrett & Henzi 2001; see Russell & Phelps 2013) and services
(Lazaro-Perea et al. 2004). Several studies have
identified asymmetrical cost and benefits between groomer and recipient,
considering that altruistic behaviour benefits the recipient but imposes some
cost to the donor (Schino & Aureli
2008b; Russell & Phelps 2013). Grooming time is considered as cost to the
groomer in their daily activity budgets as metabolic cost and loss of foraging
opportunities (Russell & Phelps 2013). Cost and benefits can also be
categorised into immediate and delayed effects. For example, ectoparasite
removal is an immediate hygiene benefit to the recipient and constitutes a food
source for the groomer but has a delayed risk of disease transmission from the
close contact and ectoparasite consumption (reviewed in Veá
et al. 1999; Russell & Phelps 2013). Furthermore, there is an immediate
cost of time spent on grooming in return of immediate tension reduction with
delayed agonistic support through social bonding (reviewed in Veá et al. 1999; Russell & Phelps 2013).
Grooming is not restricted to
members of the same species but has been documented in members of different
species in the wild such as between Rhesus Macaque M. mulatta
and Sambar Deer Rusa unicolor (Vasava & Mahato 2013), Rhesus
Macaque and Hanuman Langur Semnopithecus
entellus (Nerlekar 2012), and Red-tailed Monkey Cercopithecus
ascanius and Blue Monkey C. mitis (Gathua 2000). Interspecies allogrooming
has also been seen in captivity between Long-tailed Macaque and Patas Monkey Erythrocebus
patas (Baker & Preston 1973), capuchin
monkeys Cebus albifrons
& Sapajus apella
and spider monkeys Ateles geoffroyi and A. paniscus
(Maple & Westlund 1975). However, most available
studies were only reviewed within the context of intraspecies allogrooming. Anecdotal records of interspecies allogrooming have been reported from the field, usually for
species of the same genus and/or within mixed species groups with
hybrids (e.g., M. nemestrina x M. fascicularis at Sepilok,
Sabah; Gilhooly & Colquhoun 2018) but, to the authors’ knowledge, published
observations of intergeneric grooming in wild sympatric primates are not
available. Interspecies grooming between primates of different genera is rarely
reported from the wild, and has, to our knowledge, not been documented for the
Critically Endangered (Ang et al. 2020; status currently being revised, A. Ang,
pers. comm. 01.vi.2021) and rare Raffles’ Banded Langur Presbytis
femoralis.
Here, we report the first
sighting of Long-tailed Macaques grooming Raffles’ Banded Langurs in Gunung Lambak Recreational Forest
in Johor, Malaysia, and discuss the potential meaning of this interspecies
interaction.
Methods
The state of Johor in Peninsular
Malaysia is home to six species of non-human primates, namely: Sunda Slow Loris Nycticebus
coucang, Long-tailed Macaque Macaca
f. fascicularis, Southern Pig-tailed Macaque M.
nemestrina, Reid’s Dusky Langur Trachypithecus o. obscurus, Raffles’ Banded
Langur Presbytis femoralis,
and Malaysian White-handed Gibbon Hybolates
l. lar. Specifically, the Raffles’ Banded Langur is Critically Endangered
(Ang et al. 2020) due to its small population size and restricted distribution
in fragmented habitats. This species is only found in southern Peninsular
Malaysia (states of Johor and Pahang) and the Republic of Singapore with an
estimated global population size of fewer than 400 individuals (Ang et al.
2020).
Gunung Lambak
is a twin-peak hill (highest at 510 m) located in Kluang,
Johor (2.0275° N, 103.3575° E). Also known as Gunung Lambak Recreational Forest, it has an area of 744 ha (i.e.,
Renggam Forest Reserve) (Image 1). The vegetation consists
mainly of secondary forest with patches of old growth trees. Pioneer tree
species, such as Campnosperma auriculatum, Macaranga spp. and non-native Acacia
spp. are common at the foot of the recreation forest and along the trails (Lee Zan Hui pers. obs. 14.iv.2021). Despite being an isolated
secondary forest, trees of the Fagaceae family, Lithocarpus cantelyanus,
L. sundaicus, Castanopsis
acuminatissima, C. scortechinii,
and C. inermis have been observed fruiting at
different times throughout the year providing a food source to the primate
community at the site (Lee Zan Hui pers. obs.
14.iv.2021). All six species of primates in Johor can be found in Gunung Lambak. Renggam Forest Reserve also holds a high in situ
conservation value for endangered Dipterocarpaceae
species, with Hopea glaucescens
and H. johorensis being listed as Critically
Endangered, Dipterocarpus sublamellatus as Endangered, and Shorea exelliptica,
S. gibbose, S. gratissima,
H. nutans, and Anisoptera
megistocarpa as Vulnerable (Chua et al. 2010).
Non-invasive opportunistic
observations were made on a group of Raffles’ Banded langurs (hereafter RBL)
during the assessment of phenology transects for the study of the feeding
ecology of this species. Footage of behaviour was recorded with a DSLR camera
(Nikon D5600) with a telephoto lens (Nikkor 200–500
mm). The study group consists of 11 individuals (one adult male, five adult
females with three dependent infants, and two juvenile females). Long-tailed
Macaques (LTMs), which are observed in groups of up to 20 individuals in the
area, range sympatrically with RBLs and can often be
observed in close proximity to RBLs.
Results
The first interspecies grooming
event was observed in the late afternoon of 02 October 2020 at the foot of Gunung Lambak during light
drizzling rain. At 1715h, a group of ca. 20 LTMs were attracted to food
provided by people with the intention to feed macaques at the roadside.
Intragroup aggression among LTMs competing for the provisioned food was
observed and some LTMs climbed up the trees nearby where the focal RBL troop of
11 individuals was resting, likely trying to avoid direct confrontation with
dominant LTMs who guarded the food. At 1730h, RBLs moved from the forest toward
the roadside, preparing to cross the road to their sleeping sites. At 1733h,
two LTMs, who both appeared to be subadult males, approached an adult female
RBL and groomed her (Image 2, Video 1). The grooming event was
unidirectional and only LTMs engaged in grooming while the RBL female was
solely receiving. This RBL was a lactating mother who had a dependent infant
(which was out of sight during the grooming event). The rest of the RBLs who
were not engaged with the LTMs were resting and feeding on flower buds and
leaves of Garcinia mangostana, Acacia mangium, and other trees nearby. One of the two LTM
groomers stopped grooming and moved onto a higher branch after ca. half a
minute while the other LTM continued grooming for eight minutes. This LTM was
observed picking substances from the RBL’s fur and feeding on it. Without
leaving its location, the LTM also occasionally fed on flower buds of the tree
(species unidentified) that they sat on. No aggression was observed in this
interspecies interaction. The female RBL was observed being vigilant, actively
scanning the surrounding environment and responding to vehicles that passed by.
At 1753h, the grooming event was interrupted by the alpha RBL male as he
approached the female and displaced the LTM, before directing the RBL group to
cross the road. The LTM group, including the two groomers, followed the RBLs to
cross the road. Both species separated after the road crossing and headed to their
respective sleeping sites.
The second observation of
interspecies grooming was on 08 October 2020, around 1808h during clear, sunny
weather. A female subadult LTM was observed actively seeking RBLs to groom
while the RBL group was feeding on sprouting leaf buds of a tall Saga Tree Adenanthera pavonina at the same site (Image 3, Video 2). The RBL group was observed
foraging on leaf buds, which were limited and sparsely distributed across the
crown of the Saga Tree, then the LTM groomer approached for grooming. In
contrast to the first observation with a fairly long grooming bout (around
eight minutes) between the fixed groomer and recipient pair, RBLs actively
terminated this grooming event by leaving the position for foraging, hence
leaving the LTM groomer to seek another recipient. Having been rejected by some
RBLs, the LTM female seemed cautious about approaching RBLs, especially female
adults. She started by touching a RBL’s tail from a distance with an extended
hand, and only if the RBL stayed in position, she got closer to inspect
(possibly for ectoparasites), also presenting her body in front of the RBL
recipient. At least two RBL juvenile females and two adult females were
eventually groomed at different timings by the same LTM (Table 1). The LTM groomer
was also observed extracting substances from RBL’s fur by hand-picking and
feeding on it as well as directly biting the RBL fur with her mouth. Although
no direct confrontation or aggressive behaviour was observed, some RBLs
appeared impatient towards the groomer and prioritised feeding on the leaf
buds. While being groomed, the RBLs seemed to pay high attention on locating
the scarce food resources instead of being vigilant to the surroundings. It
could not be observed whether the other individuals nearby and/ or the alpha
male of the RBL group were engaged in the event or groomed by the LTM at any
time but the troop was directed by his call to leave the Saga Tree and headed
to the sleeping site by 1820h, eventually ending the grooming event as the LTM
groomer was left behind.
Discussion
Interspecies grooming between RBL
and other primate species has not been reported before. In Singapore, where the
two species are also found sympatrically, grooming
has been observed only once between the two species during more than four years
of continuous research (A. Ang pers. obs. 13.ii.2021). However, interspecies
grooming between Dusky Langurs T. obscurus and LTMs has frequently been
observed between different individuals in mainland Penang, Malaysia with a mixed-species
group reported from Cherok Tokun
(Nadine Ruppert pers. obs. 2019–2020), and Dusky
Langurs, LTMs and White-thighed Langurs Presbytis
siamensis form tolerant foraging associations
with juveniles being observed playing together near a residential area in
Ampang Jaya, Selangor, Malaysia (N. Ruppert pers.
obs. 08.ii.2020). Published information on interspecies grooming, with clear
explanations, is often from studies conducted in captivity, such as zoos with
mixed species displays, e.g., capuchin monkeys and spider monkeys grooming each
other (Maple & Westlund 1975), or laboratory
settings designed to test hypotheses in interspecies interactions, e.g.,
interspecies infant interactions between LTMs and Patas
Monkeys (Baker & Preston 1973). There are only a handful of publications on
interspecies grooming in the wild, such as the unidirectional grooming events
by macaques toward non-primate species such as deers,
mostly occurring during social coalition when the ungulates followed a primate
troop and foraged on fallen food items (Tsuji et al. 2007; Vasava
& Mahato 2013).
The reported interspecies
grooming here was unidirectional in both observations, with young LTMs of both
sexes being the groomers. As adult RBLs have larger body sizes (weight around 6
kg, 59 cm in body length and up to 84 cm with tail length), ca. two times the
size of young LTMs (Ang et al. 2016), the LTMs likely groomed for rank-related
benefits (Schino & Aureli
2008b), especially in the first observation where a macaque intragroup conflict
was observed just before the grooming event when the young macaques were
displaced from the food provisioning site. Post-conflict consolation is an
affiliative interaction from the victim of aggression and individuals other
than the former aggressor (Aureli 1992). Bystanders,
who are not directly involved in the aggression may offer affiliative
interactions to relieve stress of the victim by putting themselves at risk of
receiving aggression from the aggressor (Fraser et al. 2009). RBLs, as a
different species, have no apparent relation with the aggressor, nor any
long-term association with the macaque group. It is uncertain if post-conflict
consolation happens between different primate species, yet genera (Kazem & Aureli 2005), but this might explain our observation. As
the LTM groomers made their way to the higher strata and away from LTMs that
competed for the provisioned food on ground, the LTM groomers might have found
an opportunity to relieve stress by grooming the large female RBL who might
simultaneously have deterred some other low-ranking macaques due to her body
size (Schino & Aureli
2008a). In addition, there was no apparent competition between RBLs and LTMs
over the provisioned anthropogenic food in this context. However, the
possibility of LTMs solely seeking food, i.e. ectoparasite on langurs’ skin,
from grooming, and RBLs’ desire for grooming for hygiene purposes, cannot be
ruled out (Johnson et al. 2010).
The different duration of these
interspecies grooming bouts during two independent observations was probably
due to different extrinsic factors from the environment, and the intrinsic
motivation of the primate individuals. The desire to be groomed usually follows
a cyclical pattern of motivation and demotivation (Russell & Phelps 2013).
Grooming is likely a crucial instigator of pleasure in primates, and the length
of grooming time is the most available and applicable variable to reflect the
quantity of the pleasurable effect (Russell & Phelps 2013). The female RBL
recipient from the first observation was initially in a resting state before
two young LTMs approached her and attempted to groom her. The relatively long
grooming bout and her relaxed behaviour during the bout implied that she was
not only tolerating but enjoying it. However, in the second observation, RBLs
were already engaged in feeding while the young female LTM sought grooming
opportunities, which were rejected or actively terminated by several
individuals. It is unclear why the adult female RBLs tolerated the grooming in
the first observation but not the second. A study on inter primates species
interactions near Sungai Bernam, Malaysia, which
included one of the closely related Presbytis
langurs (older synonymization P. melalophos in the text; updated to either P. robinsoni or P. s. siamensis
in the region) have concluded that intergenera
interactions are typically non-competitive, and the association occurs with
indication of selective preferences rather than by chance (Bernstein 1967).
In our study, both interspecies
grooming events happened around dusk time, but there was a main difference in
the RBL activities during both events. In the first observation, LTMs followed
RBLs from the developed area back to the forest by crossing a road, and
afterwards the two groups separated to reach their respective sleeping trees
without further interaction. In the second observation, the female RBL was
observed feeding and actively terminated the grooming session without
aggression toward the groomer, ending the session as the RBLs headed to their
sleeping trees. Judging from the several short grooming bouts in the second
observation, RBLs likely prioritized feeding shortly before reaching their
sleeping sites rather than losing foraging opportunities from being groomed by
the macaques. Being groomed can also be painful as it involves pinching and
pulling substances off the skin’s surface (Dunbar 2010). It was not obvious if
the RBLs were uncomfortable or experiencing pain, especially when the groomer
directly bit ectoparasites off the langurs’ skin.
Indeed, time spent on grooming is
a significant part of primates’ activity budgets, but not much information
related to grooming is published for Presbytis
langurs. A study on Hanuman Langurs showed that recipients determine
grooming spots on the body during allogrooming,
directing the groomer also toward inaccessible body parts (Borries 1992). From
our observation, RBLs autogroom themselves mostly on
limb parts while resting, but no allogrooming between
adult female RBLs or between mother-infant pairs have been observed in this
study so far. However, our study period
is still considered short and the study troop is not fully habituated.
LTMs that have been regularly
provisioned by humans may alter their natural behaviour exhibiting more flexibility
and are likely more willing to engage in interspecies interactions (Sugiyama
2015). It is not uncommon to see interspecies interactions and grooming in
captive environments, especially in zoos and sanctuaries (Silva 2017). In
general, LTMs that regularly receive provisioning reduce their foraging
distance, resulting in smaller home ranges, as concentrated food resources can
be obtained nearby (Sha & Hanya 2013). This may
increase the likelihood of interactions with humans and domestic animals in
these anthropogenically modified environments (Bicca-Marques
2017). However, it also raises concerns about interspecies disease transmission
as a spillover effect of the human-macaque interface
(Gillespie et al. 2008; Rushmore et al. 2017; Balasubramaniam
et al. 2020a,b). When macaques engage in interactions and close proximity with
threatened primates, such as RBLs who are Critically Endangered, the risk of
transmitting zoonotic diseases adds to the factors that already threaten this
rare species (Ang et al. 2012, 2020).
In future studies, the frequency
and ecological significance of interspecies grooming should be examined more
thoroughly. The authors believe that this behaviour is more common in the wild
than reflected by almost non-existent reports in literature. The role of
anthropogenic factors, such as food provisioning and potential edge effects
from habitat degradation should be investigated for their impacts on
behavioural flexibility, which may facilitate interspecies interactions in
disturbed sites. Cross-species transmission of diseases and parasites as a
potential consequence of interspecies grooming should also be studied to reveal
vulnerability of different primate species to potential pathogens.
Table 1. Interspecies grooming
observation of Long-tailed Macaques (LTM) grooming Raffles’ Banded Langurs
(RBL) and possible reason (SR—stress relieve with oxytocin hormone | Co—post
conflict consolation | ER—ectoparasite removal | Fo—foraging
for ectoparasite by actors | na—non-applicable).
|
Date |
Raffles’ Banded Langur
recipients |
Long-tailed Macaque actors |
Grooming duration |
Possible reason or benefit from
grooming |
|
02.x.2020 |
Adult female 1 |
Subadult male 1 & 2 |
8 minutes |
LTM: SR, Co, Fo RBL: ER |
|
08.x.2020 |
Juvenile female 1 |
Juvenile female 1 |
1 minutes 10 seconds |
LTM: Fo RBL: ER |
|
08.x.2020 |
Juvenile female 2 |
Juvenile female 1 |
50 seconds |
LTM: Fo RBL: ER |
|
08.x.2020 |
Adult female (Unidentified) |
Juvenile female 1 |
1 second |
LTM: Fo RBL: na |
|
08.x.2020 |
Adult female (Unidentified) |
Juvenile female 1 |
28 seconds |
LTM: Fo RBL: ER |
|
08.x.2020 |
Adult female (Unidentified) |
Juvenile female 1 |
1 minutes 10 seconds |
LTM: Fo RBL: ER |
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