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First record of interspecies grooming between Raffles’ Banded Langur and Long-tailed Macaque
Zan Hui Lee, Andie Ang & Nadine Ruppert
26 August 2021 | Vol. 13 | No. 9 | Pages: 19246–19253 DOI: 10.11609/jot.7510.13.9.19246-19253
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Threatened Taxa Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2021 | 13(9): 19246–19253 ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print) OPEN ACCESS htps://doi.org/10.11609/jot.7510.13.9.19246-19253
#7510 | Received 09 June 2021 | Final received 28 July 2021 | Finally accepted 09 July 2021 COMMUNICATION
First record of interspecies grooming between Rafes’ Banded Langur and Long-tailed Macaque
Zan Hui Lee 1 , Andie Ang 2 & Nadine Ruppert 3
1,2,3 School of Biological Sciences, Universit 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 Rafes’ Banded Langur Working Group, Mandai Nature 2 IUCN SSC Primate Specialist Group (Asia) 3 IUCN SSC Primate Specialist Group (Secton Small Apes) 1 [email protected], 2 [email protected], 3 [email protected] (corresponding author)
Abstract: In primates, observatons of interspecies grooming are not uncommon, especially between species of the same genus. However, litle is reported about grooming between diferent genera and less is discussed about its ecological signifcance. Here, we report the frst sightng of Long-tailed Macaques grooming the Critcally Endangered and rare Rafes’ Banded Langur during two independent events at Gunung Lambak Recreatonal Forest in Kluang, Malaysia.
Keywords: Interspecies interactons, Macaca fascicularis, Malaysia, Presbyts femoralis, primate, Singapore.
Bahasa Malaysia: Pemerhatan terhadap proses hias diri (‘grooming’) antara spesies dalam kalangan primat bukanlah sesuatu yang jarang berlaku, terutama antara spesies yang memiliki genus yang sama. Walau bagaimanapun, sangat sedikit laporan ditemui berhubung proses hias diri antara genera yang berbeza dan kepentngan ekologi perilaku ini amatlah kurang dibincangkan. Di sini kami melaporkan pemerhatan awal Kera melakukan proses hias diri ke atas Lotong Cenekah yang merupakan spesies yang amat jarang ditemui dan terancam kepupusan dalam dua insiden berasingan di Hutan Rekreasi Gunung Lambak, Kluang, Malaysia.
Editor: Mewa Singh, University of Mysore, Mysuru, India. Date of publicaton: 26 August 2021 (online & print)
Citaton: Lee, Z.H., A. Ang & N. Ruppert (2021). First record of interspecies grooming between Rafes’ Banded Langur and Long-tailed Macaque. Journal of Threat- ened Taxa 13(9): 19246–19253. htps://doi.org/10.11609/jot.7510.13.9.19246-19253
Copyright: © Lee et al. 2021. Creatve Commons Atributon 4.0 Internatonal License. JoTT allows unrestricted use, reproducton, and distributon of this artcle in any medium by providing adequate credit to the author(s) and the source of publicaton.
Funding: World Wide Fund for Nature (Singapore and Malaysia) disbursed through the Malaysian Primatological Society, Universit Sains Malaysia Gra-ASSIST scheme, and Mandai Nature.
Competng interests: The authors declare no competng interests.
Author details: Lee Zan Hui is a postgraduate student in Zoology at Universit Sains Malaysia who focuses on primate ecology and behaviour. He is a trained environmental scientst with interest in spatal ecology and conservaton of wildlife and their habitats. Andie Ang is a primatologist studying Asian colobines and chairing the Rafes’ Banded Langurs Working Group, Singapore. She is a research scientst with Mandai Nature and a visitng researcher to School of Biological Sciences, Universit Sains Malaysia and member of the IUCN SSC Primate Specialist Group (Asia). Nadine Ruppert is a zoologist focusing on primates, human- wildlife interactons, plant-animal interactons, and conservaton issues related to Malaysia. She is a senior lecturer at Universit Sains Malaysia, vice president of the Malaysian Primatological Society and member of the IUCN SSC Primate Specialist Group Secton on Small Apes.
Author contributons: conceptualisaton—NR; feld work and data analysis—ZHL; frst manuscript draf—ZHL; manuscript correctons—NR, AA; advisory role—AA.
Acknowledgements: We are grateful to the Department of Wildlife and Natonal Parks Peninsular Malaysia for grantng the research permit (P-00183-15-19 issued to NR) to study the behaviour of Rafes’ Banded Langurs at Gunung Lambak and to the funders of this study: World Wide Fund (Singapore and Malaysia) disbursed through the Malaysian Primatological Society, Universit Sains Malaysia Gra-ASSIST scheme, and Mandai Nature.
19246 Interspecies grooming between langur and macaque Lee et al. J TT INTRODUCTION consttutes a food source for the groomer but has a delayed risk of disease transmission from the close Most primate species are highly social, and behaviour contact and ectoparasite consumpton (reviewed in Veá like allogrooming, alloparentng, and playing between et al. 1999; Russell & Phelps 2013). Furthermore, there members of the same species are regularly observed in is an immediate cost of tme spent on grooming in return langurs and macaques (Lehman et al. 2007; Matsuda et of immediate tension reducton with delayed agonistc al. 2015). Social grooming is a key behaviour in primates support through social bonding (reviewed in Veá et al. to facilitate kinship reciprocity (Schino & Aureli 2010), 1999; Russell & Phelps 2013). afliaton (Dunbar 1991; Lehman et al. 2007), and Grooming is not restricted to members of the same hygiene (Goosen 1981), involving at least two actors species but has been documented in members of (groomer and recipient) physically touching each other. diferent species in the wild such as between Rhesus As an afliatve interacton, grooming plays a signifcant Macaque M. mulata and Sambar Deer Rusa unicolor role in primate societes to reinforce social bonds and (Vasava & Mahato 2013), Rhesus Macaque and Hanuman networks (Dunbar 2011). Grooming also facilitates Langur Semnopithecus entellus (Nerlekar 2012), and Red- communicaton, contributng to the development of tailed Monkey Cercopithecus ascanius and Blue Monkey social cohesion (Dunbar 2011; Dunbar & Lehman 2013; C. mits (Gathua 2000). Interspecies allogrooming Grueter et al. 2013). Within social groups of macaques, has also been seen in captvity between Long-tailed post-confict reconciliaton and consolaton ofen involve Macaque and Patas Monkey Erythrocebus patas (Baker grooming (Long-tailed Macaques Macaca fascicularis: & Preston 1973), capuchin monkeys Cebus albifrons & Cords 1992; Stump-tailed Macaques M. arctoides: Call Sapajus apella and spider monkeys Ateles geofroyi et al. 2002; Barbary Macaques M. sylvanus: McFarland and A. paniscus (Maple & Westlund 1975). However, & Majolo 2011). Social grooming has a direct efect most available studies were only reviewed within the on the physiological health of individuals, and other context of intraspecies allogrooming. Anecdotal records positve efects are associated with release of pleasure of interspecies allogrooming have been reported from hormone (i.e., oxytocin and endorphin; Dunbar 2010) or the feld, usually for species of the same genus and/ suppression of stress hormones (i.e., cortsol: Wooddell et or within mixed species groups with hybrids (e.g., M. al. 2016). Seyfarth (1977) proposed that social grooming nemestrina x M. fascicularis at Sepilok, Sabah; Gilhooly in female Cercopithecidae is principally directed toward & Colquhoun 2018) but, to the authors’ knowledge, high-ranking individuals (reviewed in Schino 2001). published observatons of intergeneric grooming in This rank-related reciprocity in allogrooming has been wild sympatric primates are not available. Interspecies demonstrated for 16 species and nine genera (Alouata, grooming between primates of diferent genera is rarely Cercopithecus, Cebus, Erythrocebus, Lemur, Macaca, reported from the wild, and has, to our knowledge, not Miopithecus, Sapajus and Semnopithecus) (Schino & been documented for the Critcally Endangered (Ang et Aureli 2008a; Tiddi et al. 2012). Evidence of trading al. 2020; status currently being revised, A. Ang, pers. allogrooming for alloparentng is also found in female comm. 01.vi.2021) and rare Rafes’ Banded Langur Long-tailed Macaques (Gumert 2007). Presbyts femoralis. Asymmetries in allogrooming resemble the context Here, we report the frst sightng of Long-tailed of ecological economy as a trade for other commodites Macaques grooming Rafes’ Banded Langurs in Gunung including food (reviewed in Barret & Henzi 2001; see Lambak Recreatonal Forest in Johor, Malaysia, and Russell & Phelps 2013) and services (Lazaro-Perea et discuss the potental meaning of this interspecies al. 2004). Several studies have identfed asymmetrical interacton. cost and benefts between groomer and recipient, considering that altruistc behaviour benefts the recipient but imposes some cost to the donor (Schino METHODS & Aureli 2008b; Russell & Phelps 2013). Grooming tme is considered as cost to the groomer in their The state of Johor in Peninsular Malaysia is home daily actvity budgets as metabolic cost and loss of to six species of non-human primates, namely: Sunda foraging opportunites (Russell & Phelps 2013). Cost Slow Loris Nyctcebus coucang, Long-tailed Macaque and benefts can also be categorised into immediate Macaca f. fascicularis, Southern Pig-tailed Macaque and delayed efects. For example, ectoparasite removal M. nemestrina, Reid’s Dusky Langur Trachypithecus o. is an immediate hygiene beneft to the recipient and obscurus, Rafes’ Banded Langur Presbyts femoralis,
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2021 | 13(9): 19246–19253 19247 J TT Interspecies grooming between langur and macaque Lee et al.
Image 1. Forest edge environment where interspecies grooming was observed at Gunung Lambak in Kluang district, Johor, Malaysia.
and Malaysian White-handed Gibbon Hybolates l. lar. a food source to the primate community at the site (Lee Specifcally, the Rafes’ Banded Langur is Critcally Zan Hui pers. obs. 14.iv.2021). All six species of primates Endangered (Ang et al. 2020) due to its small populaton in Johor can be found in Gunung Lambak. Renggam size and restricted distributon in fragmented habitats. Forest Reserve also holds a high in situ conservaton This species is only found in southern Peninsular value for endangered Dipterocarpaceae species, with Malaysia (states of Johor and Pahang) and the Republic Hopea glaucescens and H. johorensis being listed as of Singapore with an estmated global populaton size of Critcally Endangered, Dipterocarpus sublamellatus fewer than 400 individuals (Ang et al. 2020). as Endangered, and Shorea exelliptca, S. gibbose, S. Gunung Lambak is a twin-peak hill (highest at 510 m) gratssima, H. nutans, and Anisoptera megistocarpa as located in Kluang, Johor (2.0275° N, 103.3575° E). Also Vulnerable (Chua et al. 2010). known as Gunung Lambak Recreatonal Forest, it has an Non-invasive opportunistc observatons were made area of 744 ha (i.e., Renggam Forest Reserve) (Image 1). on a group of Rafes’ Banded langurs (hereafer RBL) The vegetaton consists mainly of secondary forest with during the assessment of phenology transects for the patches of old growth trees. Pioneer tree species, such study of the feeding ecology of this species. Footage as Campnosperma auriculatum, Macaranga spp. and of behaviour was recorded with a DSLR camera (Nikon non-natve Acacia spp. are common at the foot of the D5600) with a telephoto lens (Nikkor 200–500 mm). The recreaton forest and along the trails (Lee Zan Hui pers. study group consists of 11 individuals (one adult male, obs. 14.iv.2021). Despite being an isolated secondary fve adult females with three dependent infants, and forest, trees of the Fagaceae family, Lithocarpus two juvenile females). Long-tailed Macaques (LTMs), cantelyanus, L. sundaicus, Castanopsis acuminatssima, which are observed in groups of up to 20 individuals in C. scortechinii, and C. inermis have been observed the area, range sympatrically with RBLs and can ofen be fruitng at diferent tmes throughout the year providing observed in close proximity to RBLs.
19248 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2021 | 13(9): 19246–19253 Interspecies grooming between langur and macaque Lee et al. J TT RESULTS interrupted by the alpha RBL male as he approached the female and displaced the LTM, before directng the RBL The frst interspecies grooming event was observed group to cross the road. The LTM group, including the in the late afernoon of 02 October 2020 at the foot of two groomers, followed the RBLs to cross the road. Both Gunung Lambak during light drizzling rain. At 1715h, a species separated afer the road crossing and headed to group of ca. 20 LTMs were atracted to food provided their respectve sleeping sites. by people with the intenton to feed macaques at the The second observaton of interspecies grooming roadside. Intragroup aggression among LTMs competng was on 08 October 2020, around 1808h during clear, for the provisioned food was observed and some LTMs sunny weather. A female subadult LTM was observed climbed up the trees nearby where the focal RBL troop actvely seeking RBLs to groom while the RBL group of 11 individuals was restng, likely trying to avoid direct was feeding on sproutng leaf buds of a tall Saga Tree confrontaton with dominant LTMs who guarded the Adenanthera pavonina at the same site (Image 3, Video food. At 1730h, RBLs moved from the forest toward the 2). The RBL group was observed foraging on leaf buds, roadside, preparing to cross the road to their sleeping which were limited and sparsely distributed across sites. At 1733h, two LTMs, who both appeared to be the crown of the Saga Tree, then the LTM groomer subadult males, approached an adult female RBL and approached for grooming. In contrast to the frst groomed her (Image 2, Video 1). The grooming event observaton with a fairly long grooming bout (around was unidirectonal and only LTMs engaged in grooming eight minutes) between the fxed groomer and recipient while the RBL female was solely receiving. This RBL was pair, RBLs actvely terminated this grooming event by a lactatng mother who had a dependent infant (which leaving the positon for foraging, hence leaving the was out of sight during the grooming event). The rest LTM groomer to seek another recipient. Having been of the RBLs who were not engaged with the LTMs were rejected by some RBLs, the LTM female seemed cautous restng and feeding on fower buds and leaves of Garcinia about approaching RBLs, especially female adults. She mangostana, Acacia mangium, and other trees nearby. started by touching a RBL’s tail from a distance with an One of the two LTM groomers stopped grooming and extended hand, and only if the RBL stayed in positon, moved onto a higher branch afer ca. half a minute while she got closer to inspect (possibly for ectoparasites), the other LTM contnued grooming for eight minutes. also presentng her body in front of the RBL recipient. This LTM was observed picking substances from the At least two RBL juvenile females and two adult females RBL’s fur and feeding on it. Without leaving its locaton, were eventually groomed at diferent tmings by the the LTM also occasionally fed on fower buds of the tree same LTM (Table 1). The LTM groomer was also observed (species unidentfed) that they sat on. No aggression extractng substances from RBL’s fur by hand-picking and was observed in this interspecies interacton. The female feeding on it as well as directly bitng the RBL fur with her RBL was observed being vigilant, actvely scanning the mouth. Although no direct confrontaton or aggressive surrounding environment and responding to vehicles behaviour was observed, some RBLs appeared impatent that passed by. At 1753h, the grooming event was towards the groomer and prioritsed feeding on the leaf
Table 1. Interspecies grooming observaton of Long-tailed Macaques (LTM) grooming Rafes’ Banded Langurs (RBL) and possible reason (SR— stress relieve with oxytocin hormone | Co—post confict consolaton | ER—ectoparasite removal | Fo—foraging for ectoparasite by actors | na—non-applicable).
Rafes’ Banded Langur Long-tailed Macaque Possible reason or beneft Date Grooming duraton recipients actors from grooming LTM: SR, Co, Fo 02.x.2020 Adult female 1 Subadult male 1 & 2 8 minutes RBL: ER LTM: Fo 08.x.2020 Juvenile female 1 Juvenile female 1 1 minutes 10 seconds RBL: ER LTM: Fo 08.x.2020 Juvenile female 2 Juvenile female 1 50 seconds RBL: ER Adult female LTM: Fo 08.x.2020 Juvenile female 1 1 second (Unidentfed) RBL: na Adult female LTM: Fo 08.x.2020 Juvenile female 1 28 seconds (Unidentfed) RBL: ER Adult female LTM: Fo 08.x.2020 Juvenile female 1 1 minutes 10 seconds (Unidentfed) RBL: ER
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2021 | 13(9): 19246–19253 19249 J TT Interspecies grooming between langur and macaque Lee et al.
Image 2. First observaton of the interspecies allogrooming between Image 3. Second observaton of the interspecies allogrooming Long-tailed Macaques and a Rafes’ Banded Langur on 02 October between a Long-tailed Macaque and diferent individuals of Rafes’ 2020. © Lee Zan Hui. Banded Langur on 08 October 2020. © Lee Zan Hui.
buds. While being groomed, the RBLs seemed to pay ofen from studies conducted in captvity, such as zoos high atenton on locatng the scarce food resources with mixed species displays, e.g., capuchin monkeys and instead of being vigilant to the surroundings. It could spider monkeys grooming each other (Maple & Westlund not be observed whether the other individuals nearby 1975), or laboratory setngs designed to test hypotheses and/ or the alpha male of the RBL group were engaged in interspecies interactons, e.g., interspecies infant in the event or groomed by the LTM at any tme but the interactons between LTMs and Patas Monkeys (Baker & troop was directed by his call to leave the Saga Tree and Preston 1973). There are only a handful of publicatons headed to the sleeping site by 1820h, eventually ending on interspecies grooming in the wild, such as the the grooming event as the LTM groomer was lef behind. unidirectonal grooming events by macaques toward non-primate species such as deers, mostly occurring during social coaliton when the ungulates followed a DISCUSSION primate troop and foraged on fallen food items (Tsuji et al. 2007; Vasava & Mahato 2013). Interspecies grooming between RBL and other The reported interspecies grooming here was primate species has not been reported before. In unidirectonal in both observatons, with young LTMs Singapore, where the two species are also found of both sexes being the groomers. As adult RBLs have sympatrically, grooming has been observed only once larger body sizes (weight around 6 kg, 59 cm in body between the two species during more than four years length and up to 84 cm with tail length), ca. two tmes of contnuous research (A. Ang pers. obs. 13.ii.2021). the size of young LTMs (Ang et al. 2016), the LTMs However, interspecies grooming between Dusky Langurs likely groomed for rank-related benefts (Schino & T. obscurus and LTMs has frequently been observed Aureli 2008b), especially in the frst observaton where between diferent individuals in mainland Penang, a macaque intragroup confict was observed just Malaysia with a mixed-species group reported from before the grooming event when the young macaques Cherok Tokun (Nadine Ruppert pers. obs. 2019–2020), were displaced from the food provisioning site. Post- and Dusky Langurs, LTMs and White-thighed Langurs confict consolaton is an afliatve interacton from Presbyts siamensis form tolerant foraging associatons the victm of aggression and individuals other than with juveniles being observed playing together near a the former aggressor (Aureli 1992). Bystanders, who residental area in Ampang Jaya, Selangor, Malaysia (N. are not directly involved in the aggression may ofer Ruppert pers. obs. 08.ii.2020). Published informaton afliatve interactons to relieve stress of the victm by on interspecies grooming, with clear explanatons, is putng themselves at risk of receiving aggression from
19250 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2021 | 13(9): 19246–19253 Interspecies grooming between langur and macaque Lee et al. J TT the aggressor (Fraser et al. 2009). RBLs, as a diferent the frst observaton, LTMs followed RBLs from the species, have no apparent relaton with the aggressor, developed area back to the forest by crossing a road, nor any long-term associaton with the macaque group. and aferwards the two groups separated to reach their It is uncertain if post-confict consolaton happens respectve sleeping trees without further interacton. In between diferent primate species, yet genera (Kazem & the second observaton, the female RBL was observed Aureli 2005), but this might explain our observaton. As feeding and actvely terminated the grooming session the LTM groomers made their way to the higher strata without aggression toward the groomer, ending the and away from LTMs that competed for the provisioned session as the RBLs headed to their sleeping trees. food on ground, the LTM groomers might have found Judging from the several short grooming bouts in the an opportunity to relieve stress by grooming the large second observaton, RBLs likely prioritzed feeding female RBL who might simultaneously have deterred shortly before reaching their sleeping sites rather than some other low-ranking macaques due to her body losing foraging opportunites from being groomed by size (Schino & Aureli 2008a). In additon, there was no the macaques. Being groomed can also be painful as it apparent competton between RBLs and LTMs over involves pinching and pulling substances of the skin’s the provisioned anthropogenic food in this context. surface (Dunbar 2010). It was not obvious if the RBLs However, the possibility of LTMs solely seeking food, i.e. were uncomfortable or experiencing pain, especially ectoparasite on langurs’ skin, from grooming, and RBLs’ when the groomer directly bit ectoparasites of the desire for grooming for hygiene purposes, cannot be langurs’ skin. ruled out (Johnson et al. 2010). Indeed, tme spent on grooming is a signifcant The diferent duraton of these interspecies part of primates’ actvity budgets, but not much grooming bouts during two independent observatons informaton related to grooming is published for was probably due to diferent extrinsic factors from the Presbyts langurs. A study on Hanuman Langurs showed environment, and the intrinsic motvaton of the primate that recipients determine grooming spots on the individuals. The desire to be groomed usually follows a body during allogrooming, directng the groomer also cyclical patern of motvaton and demotvaton (Russell toward inaccessible body parts (Borries 1992). From & Phelps 2013). Grooming is likely a crucial instgator of our observaton, RBLs autogroom themselves mostly on pleasure in primates, and the length of grooming tme limb parts while restng, but no allogrooming between is the most available and applicable variable to refect adult female RBLs or between mother-infant pairs have the quantty of the pleasurable efect (Russell & Phelps been observed in this study so far. However, our study 2013). The female RBL recipient from the frst observaton period is stll considered short and the study troop is not was initally in a restng state before two young LTMs fully habituated. approached her and atempted to groom her. The LTMs that have been regularly provisioned by relatvely long grooming bout and her relaxed behaviour humans may alter their natural behaviour exhibitng during the bout implied that she was not only toleratng more fexibility and are likely more willing to engage but enjoying it. However, in the second observaton, in interspecies interactons (Sugiyama 2015). It is RBLs were already engaged in feeding while the young not uncommon to see interspecies interactons and female LTM sought grooming opportunites, which were grooming in captve environments, especially in zoos rejected or actvely terminated by several individuals. and sanctuaries (Silva 2017). In general, LTMs that It is unclear why the adult female RBLs tolerated the regularly receive provisioning reduce their foraging grooming in the frst observaton but not the second. distance, resultng in smaller home ranges, as A study on inter primates species interactons near concentrated food resources can be obtained nearby Sungai Bernam, Malaysia, which included one of the (Sha & Hanya 2013). This may increase the likelihood closely related Presbyts langurs (older synonymizaton of interactons with humans and domestc animals P. melalophos in the text; updated to either P. robinsoni in these anthropogenically modifed environments or P. s. siamensis in the region) have concluded that (Bicca-Marques 2017). However, it also raises concerns intergenera interactons are typically non-compettve, about interspecies disease transmission as a spillover and the associaton occurs with indicaton of selectve efect of the human-macaque interface (Gillespie et al. preferences rather than by chance (Bernstein 1967). 2008; Rushmore et al. 2017; Balasubramaniam et al. In our study, both interspecies grooming events 2020a,b). When macaques engage in interactons and happened around dusk tme, but there was a main close proximity with threatened primates, such as RBLs diference in the RBL actvites during both events. In who are Critcally Endangered, the risk of transmitng
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2021 | 13(9): 19246–19253 19251 J TT Interspecies grooming between langur and macaque Lee et al. zoonotc diseases adds to the factors that already htps://doi.org/10.1002/9781119179313.wbprim0153 threaten this rare species (Ang et al. 2012, 2020). Borries, C. (1992). Grooming site preferences in female Langurs (Presbyts entellus). Internatonal Journal of Primatology 13(1): 19– In future studies, the frequency and ecological 32. htps://doi.org/10.1007/BF02547725 signifcance of interspecies grooming should be Call, J., F. Aureli & F.B.M. de Waal (2002). Postconfict third-party afliaton in stump-tailed macaques. Animal Behaviour 63(2): 209– examined more thoroughly. The authors believe that this 216. htps://doi.org/10.1006/anbe.2001.1908 behaviour is more common in the wild than refected Chua, L.S.L., M. Suhaida, M. Hamidah & L.G. Saw (2010). Malaysia by almost non-existent reports in literature. The role Plant Red List: Peninsular Malaysian Dipterocarpaceae. Forest Research Insttute Malaysia, Kepong, Malaysia, 210 pp. of anthropogenic factors, such as food provisioning Cords, M. (1992). Post-confict reunions and reconciliaton in long- and potental edge efects from habitat degradaton tailed macaque. Animal Behaviour 44(1): 57–61. htps://doi. should be investgated for their impacts on behavioural org/10.1016/S0003-3472(05)80754-7 Dunbar, R.I.M. (1991). Functonal Signifcance of Social Grooming fexibility, which may facilitate interspecies interactons in Primates. Folia Primatologica 57: 121–131. htps://doi. in disturbed sites. Cross-species transmission of diseases org/10.1159/000156574 and parasites as a potental consequence of interspecies Dunbar, R.I.M. (2010). The social role of touch in humans and primates: behavioural functon and neurobiological mechanisms. grooming should also be studied to reveal vulnerability Neurosicence & Biobehavioral Reviews 34: 260–268. htps://doi. of diferent primate species to potental pathogens. org/10.1016/j.neubiorev.2008.07.001 Dunbar, R.I.M. (2011). Grooming, Gossip and the Evoluton of Language. Clays Ltd, St Ives Plc, England, 230 pp. Dunbar, R.I.M. & J. Lehman (2013). Grooming and social REFERENCES cohension in primates: a comment on Grueter et al. Evoluton and Human Behaviour 34: 453–455. htps://doi.org/10.1016/j. evolhumbehav.2013.08.003 Ang, A., A. Srivasthan, B.M. Md-Zain, M.R.B. Ismail & R. Meier (2012). Fraser, O.N., S.E. Koski, R.M. Witng & F. Aureli (2009). Why are Low genetc variability in the recovering urban banded leaf monkey bystanders friendly to recipients of aggression? Communicatve populaton of Singapore. Rafes Bulletn of Zoology 60(2): 589–594. & Integratve Biology 2(3): 285–291. htps://doi.org/10.4161/ Ang, A., V. D’Rozario, S.L. Jayasri, C.M. Lees, T.J. Li & S. Luz (2016). cib.2.3.8718 Species Acton Plan for the Conservaton of Rafes’ Banded Langur Gathua, M. (2000). Social interactons between two sympatric (Presbyts femoralis femoralis) in Malaysia and Singapore. IUCN SSC forest guenons, Cercopithecus ascanius and Cercopithecus Conservaton Breeding Specialist Group, Apple Valley, MN, USA. mits¸ in Kenya. Folia Primatologica 71: 353–355. htps://doi. Ang, A., D.I. Roesma, V. Nijman, R. Meier, A. Srivathsan & Rizaldi org/10.1159/000021760 (2020). Faecal DNA to the rescue: Shotgun sequencing of non- Gilhooly, L.J. & I.C. Colquhoun (2018). Variatons in aggressive invasive samples reveals two subspecies of Southeast Asian encounters between tourists and a hybrid macaque group (Macaca primates to be Critcally Endangered species. Scientfc Report 10: fascicularis x M. nemestrina) in Sabah, Malaysia. American Journal 9396. htps://doi.org/10.1038/s41598-020-66007-8 of Physical Anthropology 165: 98–99, Conference Abstract. Aureli, F. (1992). Post-confict behaviour among wild Long-tailed Gillespie, T.R., C.L. Nunn & F.H. Leendertz (2008). Integratve Macaques (Macaca fascicularis). Behavioral Ecology and approaches to the study of primate infectous disease: implicatons Sociobiology 31: 329–337. for biodiversity conservaton and global health. American Journal of Baker, R.P. & D.G. Preston (1973). The efects of interspecies infant Physical Anthropology 137(S47): 53–69. htps://doi.org/10.1002/ interacton upon social behavior of Macaca irus and Erythrocebus ajpa.20949 patas. Primates 14(4): 383–392. htps://doi.org/10.1007/ Goosen, C. (1981). On the functon of allogrooming in Old-World BF01731359 Monkey, pp. 110–120. In: Chiarelli, A.B. & R.S. Corruccini (eds.). Balasubramaniam, K.N., C. Sueur, M.A. Hufman & A.J.J. MacIntosh Primate Behavior and Sociobiology. Proceedings in Life Sciences. (2020a). Primate Infectous Disease Ecology: Insight and Future Springer, Berlin, Heidelberg, 140 pp. Directons at the Human-Macaque Interface, pp. 249–284. In: Li, Grueter, C.C., A. Bissonete., K. Isler. & C.P. van Schaik (2013). J.H., L. Sun. & P.P. Kappeler (eds.). The Behavioral Ecology of the Grooming and group cohesion in primates: implicatons for the Tibetan Macaque. Springer, Switzerland, 302pp. evoluton of language. Evoluton and Human Behaviour 34: 61–68. Balasubramaniam, K.N., P.R. Marty, S. Samartno, A. Sobrino, G. htps://doi.org/10.1016/j.evolhumbehav.2012.09.004 Taniya, M. Ismail, R. Saha, B.A. Beisner, S.S.K. Kaburu, E. Bliss- Gumert, M.D. (2007). Grooming and infant handling interchange in Moreau, M.E. Arlet, N. Ruppert, A. Ismail, S.A.M. Sah, L. Mohan, Macaca fascicularis; The relatonship between infant supply and S.K. Ratan, U. Kodandaramaiah & B. McCowan (2020b). Impact grooming payment. Internatonal Journal of Primatology 28: 1059– of individual demographic and social factors on human-wildlife 1074. htps://doi.org/10.1007/s10764-007-9202-0 interactons: a comparatve study of three macaque species. Johnson, P.T.J., A. Dobson., K.D. Laferty, D.J. Marcogliese, J. Scientfc Reports 10: 21991. htps://doi.org/10.1038/s41598-020- Memmot, S.A. Orlofske, R. Poulin. & D.W. Thieltges (2010). When 78881-3 parasites become prey: ecological and epidemiological signifcance Barret, L. & S.P. Henzi (2001). The utlity of grooming in baboon troops, of eatng parasites. Trends in Ecology and Evoluton 25(6): 362–371. pp. 119–145. In: Noë, R., J.A.R.A.M. van Hoof & P. Hammerstein htps://doi.org/10.1016/j.tree.2010.01.005 (eds.). Economics in nature: social dilemmas, mate choice and Kazem, A.J.N. & F. Aureli (2005). Redirecton of aggression: multparty biological markets. Cambridge University Press, Cambridge, 276 pp. signalling within a network, pp. 191–218. In: McGregor, P.J. (ed.). Bernstein, I.S. (1967). Intertaxa Interactons in a Malayan Animal Communicaton Networks. Cambridge University Press, 444 Primate Community. Folia Primatol. 7: 198–207. htps://doi. p. org/10.1159/000155119 Lazaro-Perea, C., M.D.F. Arruda & C.R. Snowdon (2004). Grooming Bicca-Marques, J.C. (2017). Urbanizaton (and primate conservaton). as a reward? Social functon of grooming between females in pp. 1–5. In: Fuentes, A., M. Bezanson, C.J. Campbell, A.F. Di cooperatvely breeding marmosets. Animal Behaviour 67: 627–636. Fiore, S. Elton., A. Estrada & J. Yamagiwa (eds.). The Internatonal htps://doi.org/10.1016/j.anbehav.2003.06.004 Encyclopedia of Primatology – 3 Volumes. Wiley-Blackwell, 1608 pp. Lehman, J., A.H. Korsthens & R.I.M. Dunbar (2007). Group size,
19252 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2021 | 13(9): 19246–19253 Interspecies grooming between langur and macaque Lee et al. J TT grooming and social cohesion in primates. Animal Behaviour 74: Schino, G. & F. Aureli (2010). The relatve roles of kinship and 1617–629. htps://doi.org/10.1016/j.anbehav.2006.10.025 reciprocity in explaining primate altruism. Ecology Leters 13: 45– Maple, T. & B. Westlund (1975). The integraton of social interactons 50. htps://doi.org/10.1111/j.1461-0248.2009.01396.x between cebus and spider monkeys in captvity. Applied Seyfarth, R.M. (1977). A model of social grooming among adult female Animal Ethology 1(3): 305–308. htps://doi.org/10.1016/0304- monkeys. Journal of Theoretcal Biology 65: 671–698. 3762(75)90024-3 Sha, J.C.M. & G. Hanya (2013). Diet, actvity, habitat use, and ranging McFarland R. & B. Majolo (2011). Grooming coercion and the post- of two neighboring groups of food-enhanced long-tailed macaques confict trading of social services in Wild Barbary Macaques. PLOS (Macaca fascicularis). American Journal of Primatology 75: 581– ONE 6(10): e26893. htps://doi.org/10.1371/journal.pone.0026893 592. htps://doi.org/10.1002/ajp.22137 Matsuda, I., K. Fukaya, C. Pasquareta & C. Sueur (2015). Factors Silva, N. (2017). Interspecies animal “Friendships”. MSc Thesis, Infuencing Grooming Social Networks: Insights from Comparisons Department of Animal Environment and Health, Swedish University of Colobines with Diferent Dispersal Paterns, pp. 231–254. In: of Agricultural Sciences, 54pp. Furuichi, T., J. Yamagiwa & F. Aureli (eds.). Dispersing Primate Sugiyama, Y. (2015). Infuence of provisioning on primate behavior Females: Life History and Social Strategies in Male-Philopatric and primate studies. Mammalia 75(3): 255–265. htps://doi. Species. Springer Japan, 299pp. org/10.1002/ajp.22137 Nerlekar, A. (2012). An instance of inter species interacton between Tiddi, B., F. Aureli & G. Schino (2012). Grooming up the hierarchy: the Hanuman Langur (Semnopithecus entellus) and Rhesus Macaque exchange of grooming and rank-related benefts in a New World (Macaca mulata). Zoo’s Print XXII(8): 27–28. primate. PLoS ONE 7(5): e36641. htps://doi.org/10.1371/journal. Rushmore, J., D. Bisanzio & T.R. Gillespie (2017). Making new pone.0036641 connectons: insights from primate-parasite networks. Trends in Tsuji, Y., M. Shimoda-Ishiguro, N. Ohnishi & S. Takatsuki (2007). Parasitology 33(7): 547–560. A friend in need is a friend indeed: feeding associaton between Russell, Y.I. & S. Phelps (2013). How do you measure pleasure? Japanese Macaques and Sika Deer. Acta Theriologica 52(4): 427– A discussion about intrinsic costs and benefts in primate 434. htps://doi.org/10.1007/BF03194240 allogrooming. Biology & Philosophy 28: 1005–1020. htps://doi. Vasava, A.G. & S. Mahato (2013). Grooming of Sambar (Rusa unicolor) org/10.1007/s10539-013-9372-4 by Rhesus Macaque (Macaca mulata) in Sariska Tiger Reserve, Schino, G. (2001). Grooming, competton and social rank among Rajasthan, India. Current Science 104(3): 296–298. female primate: a meta-analysis. Animal Behaviour 62: 265–271. Veá, J.J., A.P. Pérez, M. Baldellou & V. Alea (1999). Cost-beneft htps://doi.org/10.1006/anbe.2001.1750 analysis of allogrooming behaviour in Cercocebus Torquatus Schino, G. & F. Aureli (2008a). Trade-ofs in primate grooming lunulatus. Behaviour 136(2): 243–256. htps://brill.com/view/ reciprocaton: testng behavioural fexibility and correlated journals/beh/136/2/artcle-p243_6.xml evoluton. Biological Journal of the Linnean Society 95: 439–446. Wooddell, L.J., S.S.K. Kaburu, K.L. Rosenberg, J.S. Meyer, S.J. Suomi, htps://doi.org/10.1111/j.1095-8312.2008.01067.x A.M. Detmer (2016). Matrilineal behavioral and physiological Schino, G. & F. Aureli (2008b). Grooming reciprocaton among female changes following the removal of a non-alpha matriarch in Rhesus primates: a meta-analysis. Biology Leters 4: 9–11. htps://doi. Macaques (Macaca mulata). PLoS ONE 11(11): e0167739. htps:// org/10.1098/rsbl.2007.0506 doi.org/10.1371/journal.pone.0167739
Threatened Taxa
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2021 | 13(9): 19246–19253 19253
The Journal of Threatened Taxa (JoTT) is dedicated to building evidence for conservaton globally by OPEN ACCESS publishing peer-reviewed artcles online every month at a reasonably rapid rate at www.threatenedtaxa.org. All artcles published in JoTT are registered under Creatve Commons Atributon 4.0 Internatonal License unless otherwise mentoned. JoTT allows allows unrestricted use, reproducton, and distributon of artcles in any medium by providing adequate credit to the author(s) and the source of publicaton.
ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)
August 2021 | Vol. 13 | No. 9 | Pages: 19191–19390 Date of Publicaton: 26 August 2021 (Online & Print) www.threatenedtaxa.org DOI: 10.11609/jot.2021.13.9.19191-19390
Artcles Review
On the impact of earthquake-induced landslides on Red Panda Ailurus fulgens Wild ungulates in Jordan: past, present, and forthcoming opportunites (Mammalia: Carnivora: Ailuridae) habitat in Langtang Natonal Park, Nepal – Ehab Eid & David Mallon, Pp. 19338–19351 – Yogesh Rana Magar, Man Kumar Dhamala, Ajay Mathema, Raju Chauhan & Sijar Bhata, Pp. 19191–19202 Viewpoint Rhesus Macaque Macaca mulata (Mammalia: Primates: Cercopithecidae) in a human-modifed landscape: populaton, actvity budget, and societal perceptons in The captve populaton of the Lion-tailed Macaque Macaca silenus (Linnaeus, 1758). Bangladesh The future of an endangered primate under human care – Sufa Akter Neha, Mohammad Ashraf Ul Hasan, Mohammad Abdul Baki & Subrina – Nilofer Begum, Werner Kaumanns, Alexander Sliwa & Mewa Singh, Pp. 19352–19357 Sehrin, Pp. 19203–19211
Factors afectng the species richness and compositon of bird species in a community Short Communicaton managed forest of Nepal – Bishow Poudel, Bijaya Neupane, Rajeev Joshi, Thakur Silwal, Nirjala Raut & Dol Raj Jaguar Panthera onca (Linnaeus, 1758) (Mammalia: Carnivora: Felidae) presumably Thanet, Pp. 19212–19222 feeding on Flathead Catish Pylodicts olivaris (Rafnesque, 1818) (Actnopterygii: Siluriformes: Ictaluridae) at Aros and Yaqui rivers, Sonora, Mexico – Juan Pablo Gallo-Reynoso, Pp. 19358–19362 Communicatons
A large mammal survey in Koyli Alpha Community Wildlife Reserve and its Notes surroundings in the Great Green Wall extension area in Senegal – Anna Niang & Papa Ibnou Ndiaye, Pp. 19223–19231 Life near a city: actvity patern of Golden Jackal Canis aureus Linnaeus, 1758 (Mammalia: Carnivora: Canidae) in a habitat adjoining Bhubaneswar, India Blackbuck Antlope cervicapra (Mammalia: Cetartodactyla: Bovidae) estmates in – Subrat Debata, Pp. 19363–19366 human-dominated landscape in Aligarh, Utar Pradesh, India – Mujahid Ahamad, Jamal A. Khan & Satsh Kumar, Pp. 19232–19238 Chemical immobilisaton of a Eurasian Lynx Lynx lynx (Linnaeus, 1758) (Mammalia: Carnivora: Felidae) with ketamine-dexmedetomidine mixture in Ladakh, India Diet of Leopards Panthera pardus fusca inhabitng protected areas and – Animesh Talukdar & Pankaj Raina, Pp. 19367–19369 human-dominated landscapes in Goa, India – Bipin S. Phal Desai, Avelyno D’Costa, M.K. Praveen Kumar & S.K. Shyama, Pp. 19239– White-bellied Heron Ardea insignis in Hkakabo Razi Landscape, northern Myanmar 19245 – Myint Kyaw, Paul J.J. Bates, Marcela Suarez-Rubio, Bran Shaung, Han Nyi Zaw, Thein Aung, Sai Sein Lin Oo & Swen C. Renner, Pp. 19370–19372 First record of interspecies grooming between Rafes’ Banded Langur and Long-tailed Macaque Range extension of the Common Slug Snake Pareas montcola (Cantor, 1839) – Zan Hui Lee , Andie Ang & Nadine Ruppert, Pp. 19246–19253 (Reptlia: Squamata: Pareidae): a new family record for Nepal – Dipa Rai, Manoj Pokharel & Tapil P. Rai, Pp. 19373–19375 Photographic evidence of Red Panda Ailurus fulgens Cuvier, 1825 from West Kameng and Shi-Yomi districts of Arunachal Pradesh, India First record of Mantspilla indica (Westwood, 1852) (Neuroptera: Mantspidae) – Moktan Megha, Sylvia Christ, Rajesh Gopal, Mohnish Kapoor & Ridhima Solanki, from the Western Ghats, India Pp. 19254–19262 – T.B. Suryanarayanan & C. Bijoy, Pp. 19376–19379
On the reproductve biology of the invasive Armoured Sailfn Catish Pterygoplicthys A new distributon record of the Western Ghats endemic damselfy pardalis (Castelnau, 1855) (Siluriformes: Loricariidae) from the natural drainages in Melanoneura bilineata Fraser, 1922 (Insecta: Odonata) from Maharashtra, India Thiruvananthapuram, India – Yogesh Koli & Akshay Dalvi, Pp. 19380–19382 – Smrithy Raj, Suvarna S. Devi, Amrutha Joy & A. Biju Kumar, Pp. 19263–19273 A new record of the Emerald Striped Spreadwing Lestes viridulus Rambur, 1842 On the high bird diversity in the non-protected regions of Trashiyangtse District in (Zygoptera: Lestdae) from Nepal Bhutan – Manoj Sharma, Pp. 19383–19385 – Lam Norbu, Phuntsho Thinley, Tandin Wangchuck, Ugyen Dechen, Lekey Dorji, Tshering Choephel & Pasang Dorji, Pp. 19274–19292 Rediscovery of the Bhutan Primrose Primula jigmediana W.W. Smith (Angiosperms: Primulaceae) afer 87 years in Bumdeling Wildlife Sanctuary, Bhutan Populaton status and distributon of the Critcally Endangered Bengal Florican – Tez B. Ghalley, Tshering Dendup, Karma Sangay & Namgay Shacha, Pp. 19386–19388 Houbaropsis bengalensis in the grassland of Koshi Tappu Wildlife Reserve, Nepal – Ritka Prasai, Hemanta Kafey, Suraj Upadhaya, Swosthi Thapa, Pratstha Shrestha, First report of Golovinomyces sp. causing powdery mildew infecton on Alex Dudley & Yajna Prasad Timilsina, Pp. 19293–19301 Dyschoriste nagchana in Western Ghats of India – Sachin Vasantrao Thite, Pp. 19389–19390 Is habitat heterogeneity efectve for conservaton of buterfies in urban landscapes of Delhi, India? – Monalisa Paul & Aisha Sultana, Pp. 19302–19309 Publisher & Host A preliminary checklist of moths (Lepidoptera: Heterocera) from Gangajalghat, Bankura, West Bengal, India – Ananya Nayak, Pp. 19310–19323
First report of three species of the genus Diaphanosoma (Crustacea: Cladocera: Sididae) from Jammu waters (J&K), India – Nidhi Sharma & Sarbjeet Kour, Pp. 19324–19337
Threatened Taxa