An observation of several Common Palm hermaphroditus at a fruiting tree of Endospermum diadenum in Tabin Wildlife Reserve, Sabah, Malaysia: comparing feeding patterns of frugivorous carnivorans

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Abstract M. NAKABAYASHI , H. BERNARD and Y. NAKASHIMA

Common Palm Civets Paradoxurus hermaphroditus as mother–young and as mating associations. Among three individuals observed feeding at a fruiting Endospermum diadenum tree, no aggression was noted between either of the live two solitarily adult males and reportedlyand one female, interact but intra-specifically agonistic behaviour only occurred rarely, other between than Arctogalidia trivirgata the males. Co-feeding seems to be rare in of subfamily , except in Small-toothed Palm are probably. By basedcontrast, on co-feedingdiffering patterns is more of frequently fruit production observed between in other these frugivorous places. carnivorans, distributed in Central and , and in Central Africa. Within Asia, there are perhaps regional differences in incidence of co-feeding. These differences Keywords: agonistic behaviour, gregarious feeding, social interaction

Satu pemerhatian beberapa Musang Pandan Paradoxurus hermaphroditus pada pokok sendok sendok mata udang Endospermum diadenum berbuah di Simpanan Hidupan Liar Tabin, Sabah, Malaysia: perbandingan corak makan karnivora yang memakan buah-buahan Abstrak

Musang Pandan Paradoxurus hermaphroditus perhubungan di antara ibu dengan anak dan di antara pasangan mengawan. Pemerhatian terhadap tiga individu Musang Pandan hidup secara bersendirian dan interaksi intra-spesies jarang dilaporkan, kecuali yang sedang makan di pokok Endospermum diadenum yang berbuah, menunjukkan bahawa tiada kelakuan agonistik di antara Musangdua individu Akar jantanArctogalidia dewasa trivirgata dengan seekor betina. Tetapi, kelakuan agonistik telah diperhatikan berlaku di antara individu jantan. Kelakuan makan-secara-bersama jarang sekali dilaporkan terhadap spesies di bawah subfamily Paradoxurinae, kecuali . Sebaliknya, kelakuan makan-secara-bersama adalah lebih kerap diperhatikan terhadap spesies furgivora-karnivora yang terdapat di bahagian Amerika tengah dan selatan, dan juga Afrika tengah. Di Asia pula, mung- kin terdapat perbezaan insiden kelakuan makan-secara-bersama iaitu bergantung kepada wilayah. Perbezaan ini mungkin disebabkan oleh perbezaan dalam pola penghasilan buah di wilayah-wilayah yang berlainan. Introduction of Sabah, on the island of . Tabin was heavily logged

Common Palm Civet Paradoxurus hermaphroditus is a car dipterocarp tropical dominated by pioneer species suchin the as 1970s Neolamarckia and 1980s, cadamba leaving and mainly Macaranga regenerating bancana mixed et al. 2010). It lives in a broad- et al. 2007). Common Palm Civets inhabiting Tabin nivoran weighing 2–5 kg as an adult. It is widespread in tropi- eat mostly fruits of pioneer plants such as Leea aculeata ,(Ra En- cal and subtropical Asia (Patou et al dospermumjaratnam diadenum array of natural habitats and survives well in human-modifiedet al. 2010a) kashima et al. 2010a). andareas thus (Corlett has been1998). regarded It is highly as frugivorousan important (Joshi . 1995, On the cloudy evening and some of 20 species August of 2011, fig trees the crown (Na of a- Grassman 1998, Su Su & Sale 2007, Nakashima relatively large fruiting Endospermum diadenum ma et al. 2010a, 2010b). Due to its nocturnal habit, little is diameter at breast height [DBH], about 30 m tall) was watched knownagent (Rabinowitz about its social 1991, relationships Nakashima in & the Sukor wild. 2010, Nakashi- from about 20 m from the tree, from a concealed (about position 50 cmon the ground to prevent detecting the observer. The tree Huai Kha Khaeng Wildlife Sanctuary in Thailand detected high Telemetry in the Royal Chitwan National Park in Nepal and ture oil palm plantation 20 or more years old, and its canopy et al was along the western boundary of Tabin, adjacent to a ma- onmale–male social interactions and male–female between home-range males, and overlap between (Rabinowitz males and females.1991, Joshi This paper. 1995). reports So far, male–male no studies and have male–female been conducted social was connected to an adjacent (non-fruiting) tree (species not interactions in one observation at a fruiting Endospermum dia- known; about 20 cm DBH) approximately 25 m tall. All obser- denum vations were aided by 8×36 binoculars and a 120-lumen head- takenlamp with not tored shine filter. lights The heightcontinuously of the tree or directly and the ontolocations the fo of tree in Tabin Wildlife Reserve (hereafter, Tabin). focal animals were measured by a laser rangefinder. Care was Tabin (5°05'–5°22'N, 118°30'–118°55'E) lies about 50 km - north-east of the town of Lahad Datu, in east Malaysian state cal . Sex was determined by visual check of the sexual Small Carnivore Conservation, 42

Vol. 47: 42–45, December 2012 Behavioural observations of Common Palm Civet

toothed Palm Civet and a . Both cases were Civet feeding in the focal tree, so we decided to observe this et al organ. On 19 August we had happened to find a Common Palm Brownaccompanied Palm Civets by loud Paradoxurus screaming jerdoni calls. ,Rajamani involving two .animals (2002) Observationstree the next night. Observation ran from 18h00 until 02h00. also reported an arboreal intra-specific interaction between Paradoxurus makingmay tend loud to vocaliseprolonged when spitting/brawling two animals encounter noises. In each these other. cases the animals’ sexes were not specified. Species of toAt 19h55,the tree a maleand started Common foraging Palm Civet until (hereafter 21h16 when male it1) climbedcame to feeding in the fruiting tree may vary by region or season. In downthe tree the and tree. started The male foraging and (28female m up). civets At 20h08,always stayeda female at came least Tabin,In we Common conducted Palm nocturnal Civets, the surveys degree for of nine intraspecific months andco- observed a mother and baby feeding in the same tree once, and two male Common Palm Civets growling at each other in 5 m apart. No aggression was seen. After the female’s depar- a fruiting tree of Ficus racemosa. In Kulen–Promtep Wildlife ture, male 1 continued to forage in the tree. At 22h35, another downmale, smallerthe tree quickly,than male and 1 growling (hereafter was male heard 2) forcame nine to minutes.the tree and started foraging. Ten minutes later (22h45) male 2 climbed 2012),Sanctuary, but Cambodia,it is unclear Common if the group Palm members Civets visiting were afamily salt-lick or time male 1 could be seen clearly, and was not growling. Male 1 were photographedin litt in. 2012). groups Also of in 1–5 Cambodia, individuals Iseborn (Edwards et al. The exact location of this growling was not clear, but during this male 2 climbed up the tree again, and male 1 immediately made notand (S.never Edwards observed Common Palm Civets feeding in a group ancontinued aggressive to forage move andtowards did not male climb 2. Male down 2 the reacted tree. Atby 23h29,climb (2012) surveyedin litt. 2012). in Veun Meanwhile, Sai–Siem Pangat Guning Conservation Halimun, Area,Java, ing down the tree. Ten minutes later, male 2 climbed up the tree again and started feeding. Male 1 came close to male 2, but- (T. Iseborn was not aggressive. At 23h43, male 2 stopped feeding and went Indonesia, although sex was not checked, four Common Palm tonCivets et aland five Small-toothedin litt. Palm2012). Civets were observed feed- ing in the same tree together at once without interaction (Ea- 1down, suddenly crossing ran towardsbranches male into 2 the and adjacent both climbed tree. Theydown showed the ad . 2010, J. Eaton no particular behaviour to each other, until 23h48 when male CivetsThe Arctogalidia other species trivirgata belonging are oftento subfamiliy seen foraging Paradoxurinae compan - are widely distributed across Asia. Only Small-toothed Palm fruitingjacent tree. Endospermum At this time,. Male growling 1 was was not heard. observed Then, thereafter. male 2 was At Borissenko et al et al - 00h14detected male growling 2 climbed on a intoliana the straddling fruiting treethe tree and adjacentcontinued to forthe obs.).ionably In inDanum duos Valleyor even Conservation larger groups Area, (e.g.: Sabah, Duckworth Malaysia, 1997, we observed four individuals. 2004, Eaton of this .species 2010, Moore feeding 2011, on Ficus MN pers. bin- - nendijkii aging,Discussion for 1½ hours (Fig. 1). Palm Civets are usually solo but observations of two together in June 2012, but could not specify theirin litt sex.. 2012). Brown By et al contrast, but similar to Common Palm Civet, Arctic- but in addition to the obvious needs of mother–young and mat tisare binturong not unusual and (Mudappa Masked Palm 2001, Civet N. Prakash Paguma larvata seem in ingCommon associations, Palm Civets may interactlive mainly directly solitarily with (Joshieach other, . at1995), least - seems to be presently too little information on Golden Palm close to each other in a fruiting tree in Laos. Moreover, he re Civetgeneral Paradoxurus to feed solitarily zeylonensis (MN to pers. determine obs.). Unfortunately, its feeding sociality. there occasionally. Duckworth (1997) also observed two individuals Other tropical continents hold several frugivorous car - Potos flavus and the olingos Bas- ported interspecific encounters of this species once each with saricyon in Central and South America, and - two other species of subfamily Paradoxurinae, namely a Small- Nandinianivorans, binotatanamely

(not closely related to Asian palm civets, despite its English name; Nyakatura & Bininda-Emonds 2012) in Central Africa. Ecological information on these carnivorans is patchy, but at least Kinkajou and African Palm Civet have sistentbeen reported social grouping to feed gregariously. in large fruiting Kays trees & Gittleman in the lowland (2001) reported that occasionally fed together with con-

mostforest frequentlyof Parque National observed. Soberania Interestingly, in the Republicmale–male of . combi nationsMale–female were combinationsalso observed followed several times.by female–juvenile Regarding African were Fig. 1. Times of presence of three Common Palm Civets Paradoxurus - hermaphroditus in a fruiting Endospermum diadenum tree, Tabin Wildlife Reserve, Sabah, Malaysia, on 20 August 2011. (Dashed lines trees.Palm Civet,Meanwhile, Charles-Dominique males of both (1978)animals reported have been that reported male– indicate that the individual was not under observation and was, almost male and female–juvenile co-feeding combinations in fruit- certainly, outside the fruiting tree. Vertical lines indicate that it was ship. There is particularly little information on olingos, but at entering or leaving, respectively, the fruiting tree. Solid horizontal lines leastto fight Beddard’s each other, Olingo perhaps B. beddardi reflecting a dominance relationB.- indicate its presence in the fruiting tree.) gabbii have been observed in groups occasionally, and these and Bushy-tailed Olingo

43 Small Carnivore Conservation, Vol. 47, December 2012 Nakabayashi et al.

of other civet species at Phnom Samkos Wildlife Sanctuary and et al Veun Sai–Siem Pang Conservation Area, Cambodia. Small Carni- groupsThis have information also been reportedsuggests feeding that gregarious on individual feeding fig trees of vore Conservation frugivorous(Mendes-Pontes carnivorans . 2002, is less Gonzales-Maya common in Asia & Belant than 2010).in South America and Africa. Within Asia, there may also be regional tribution and predation 46: 26–29. pressure on spacing behavior in palm differences. Considering that fruit production differs between Joshi,civets. A. R., JournalSmith, J. of L. Mammalogy D. & Cuthbert, F. J. 1995. Influence of food dis- et al et al. 2011), these differences are Potos flavus 76: 1205–1212.Journal of Zoology, London continentsprobably based (van Schaikon variation . 1993) in patterns and between of fruit regions production (Wich Kays, R. W. & Gittleman, J. L. 2001. The social organization of the & van Schaik 2000, Wich Kinkajou (). ingos,253: 491–504. beddardi rousbetween carnivorans. these places. More field research is needed to allow Mendes-Pontes,nia: status and A. R., recommendations. Rosas Ribeiro, P. F. Small & Mendonça, Carnivore T. Conservation M. 2002. Ol- confident generalisation of patterns of co-feeding in frugivo- Pocock, 1921, in Brazilian Amazo- Acknowledgements Arcto- galidia26: 7–8. trivirgata trilineata on Gunung Salak, West Java, Indone Wildlife Department; the Danum Valley Management Committee; and Moore,sia. R. Small S. 2011. Carnivore Sightings Conservation of Javan Small-toothed Palm Civets theWe Sabah thank Biodiversity the Economic Council, Planning for granting Unit Sabah, us permission Malaysia; to the conduct Sabah Mudappa, D. 2001. Ecology of the - research in Sabah, Malaysia. We thank G. Reynolds and all the re ni in the tropical of the Western 44: 38–39. Ghats, India. Bharathiar Paradoxurus jerdo- - search assistants from Danum Valley Field Centre. We are grateful to UniversityParadoxurus (Ph.D. hermaphroditus thesis), Coimbatore, India. S. Kohshima, G. Hanya, H. Matsubayashi, H. Samejima, N. Kuze, I. Mat- Nakashima, Y. & Sukor, J. A. 2010. Importance ofTropics Common Palm Civets suda, T. Kanamori, T. Tajima, A. Matsukawa and S. Kobayashi for their ( ) as a long-distance disperser for helpfulencouragement comments and that suggestions. greatly improved We deeply previous appreciate versions James Eaton,of the large-seeded plants in degraded forests. 18: 221–229. Nisarg Prakash and an anonymous reviewer for critical readings and Nakashima,Palm Civet Y., Inoue, Paradoxurus E., Inoue-Murayama, hermaphroditus M. & Sukor, J. A. 2010a. High potential of a disturbance-tolerantMammal frugivore, Study the Common manuscript,draft. We are and grateful Sarah to Edwards C. J. Jaikal and for Tatiana preparing Iseborn the Malay for their language infor- (), as a seed mation. We sincerely thank W. Wong for revising the English of the uniquenessdisperser for of large-seeded a small carnivore plants. as seed dispersal 35: agents: 209–215. a case Grant from the Japan Science Society and International Training Pro Nakashima,study of Y., the Inoue, Common E. & Palm Inoue-Murayama, Civets in the Tabin M. 2010b. Wildlife Functional Reserve, text. This work was supported by the Sasagawa Scientific Research Sabah, Malaysia. Oecologia 164: 721–730. - Referencesgram of HOPE from The Japan Society for the Promotion of Science. Nyakatura,supertree K. & complete Bininda-Emonds, with divergence O. R. P. 2012.time estimates. Updating theBMC evolu Biol- Arctogalidia trivirgata from Viet ogytionary history of (Mammalia): a new species-level Borissenko,nam. Small A. V., Carnivore Ivanova, N.Conservation V. & Polet, G. 2004. First recent record of the Small-toothed Palm Civet Nandinia bino- 10(12): 1–31. tata 30: 5–6. Patou,Paradoxurus M. L., Wilting, palm A., civets Gaubert, – a new P., Esselstyn, model for J.Asian A., Cruaud, biogeography. C., Jen- Charles-Dominique,sympatriques du P. .1978. Ecologie Terre et Vieet vie (Revue sociale d’Ecologie) de 32: 477– Journalnings, A. of P., Biogeography Fickel, J. & Veron, G. 2010. Evolutionary history of the (carnivores, viverridés): comparison avec les prosimiens species in Huai Kha Khaeng 30: Wildlife2077–2097. Sanctuary, Thailand. Journal 528. Biological Reviews Rabinowitz,of Zoology, A. R. London 1991. Behaviour and movements of sympatric civet Corlett, R. T. 1998. Frugivory and seed dispersal by vertebrates in the notesOriental on (Indomalayan) ecology, behaviour region. and conservation. Small 73: 413–448.Carnivore status of the Brown 223: Palm 281–298. Civet in , South India. Duckworth,Conservation J. W. 1997. 16: 1–21. Small carnivores in Laos: a status review with Rajamani,Small N.,Carnivore Mudappa, Conservation D. & Van Rompaey, 27: 6–11. H. 2002. Distribution and

Prionailurus bengalen- Eaton,toothed J. A., Wüst, Palm CivetR., Wirth, Arctogalidia R., Shepherd, trivirgata C. R.,) trilineata. Semiadi, SmallG., Hall, Car J.- Rajaratnam,sis borneoensis R., Sunquist,) in an agriculturalM., Rajaratnam, landscape L. & Ambu, in Sabah, L. 2007. Malaysian Diet &nivore Duckworth, Conservation J. W. 43: 2010. 16–22. Recent records of the Javan Small- Borneo.and habitat Journal selection of Tropical of the Ecology ( ( sector of Kulen–Promtep Wildlife Sanctuary, northern Cambo Civet Paradoxurus hermaphroditus and23: 209–217. Viver- Edwards,dia. Small S. 2012. Carnivore Small carnivore Conservation records from the Oddar Meanchay Su Suricula & Sale, indica J. 2007. in regenerating Niche differentiation degraded betweenforest, Myanmar. Common SmallPalm - Carnivore Conservation 36: 30–34. Bassaricyon 46: 22–25. gabbii in . Small Gonzales-Maya,Carnivore Conservation J. F. & Belant, J. L. 2010. Range extension and social- ity of Bushy-tailed Olingo van Schaik,mary consumers. C. P., Terborgh, Annual J. W. Review & Wright, of Ecology S. J. 1993. and The Systematics phenology 24: of 43: 37–39. tropical forests: adaptive significance and consequence for pri- Grassman,Small CarnivoreL. I., Jr. 1998. Conservation Movements and fruit selection of two Para- doxurinae species in a dry evergreen forest in southern Thailand. fruiting353–377. in Sumatra and elsewhere in Malesia. Journal of Tropical ings of Common Palm Civets 19: Paradoxurus 25–29. hermaphroditus and Wich,Ecology S. A. & van Schaik, C. P. 2000. The impact of El Niño on mast Iseborn, T., Rogers, L. D., Rawson, B. & Nekaris, K. A. I. 2012. Sight- 16: 563–577.

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Email: [email protected] 2Institute for Tropical Biology and Conservation, Wich, S. A., Vogel, E. R., Larsen, M. D., Fredriksson, G., Leighton, M., Universiti Malaysia Sabah, Jalan UMS, 88400, Kota PLoSYeager, ONE C. P., Brearley, F. Q., van Schaik, C. P. & Marshall, A. J. 2011. Kinabalu, Sabah, Malaysia. Forest fruit production is higher on Sumatra than on Borneo. 3Graduate School of Science, Kyoto University, Oiwake- 1Wildlife 6Research (6) e21278: Center 1–9. of Kyoto University, 2-24 cho, Kitashirakawa, Sakyo, Kyoto 606-8502, Japan. Tanaka-Sekiden-cho, Sakyo, Kyoto 606-8203, Japan. Email: [email protected]

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