Small carnivore records from a threatened habitat linkage in Terengganu, Peninsular Malaysia
L. HEDGES1,2* , S. A. AZIZ1, W. YAP1 3, M. GOOSEM3 3 1,3,4 Abstract , G. R. CLEMENTS , S. LAURANCE and W. F. LAURANCE Habitat loss and fragmentation are a key threat to the survival of several small carnivore species in Southeast Asia. Enhancing habitat connectivity is therefore an important conservation strategy. In Peninsular Malaysia, the government plans to connect carnivore species composition in these linkages remains poorly documented. Of the 12 species detected in and around Linkage its fragmented forests via 17 habitat linkages to form a large contiguousThe forestIUCN Red complex List of known Threatened as the Species Central: BinturongForest Spine. Arctictis Small binturong Hemigalus derbyanus, Oriental Small-clawed Otter Aonyx cinereus and Smooth-coated Otter Lutrogale perspicillata7, in the state of Terengganu, four are categorised as VulnerableHerpestes urva by - ganu, extending, Banded eastwards Civet its known distribution in Peninsular Malaysia. Forests in and around this linkage are threatened by disturbance .associated A photograph with of an Crab-eating existing road, Mongoose and the construction ofwith a nearby young dam. is the The first study record area’s of this relatively species high from recorded Tereng small carnivore species richness, and its complement of globally threatened small carnivore species, supports its inclusion into - rants publication, especially from camera-trap surveys that consciously account for microhabitat use and behavioural variation betweena proposed different protected species. area This (known would as allow the Kenyir a clearer Wildlife understanding Corridor). of Information small carnivore on small communities carnivores in Peninsularin other linkages Malaysia. war
Keywords
: Central Forest Spine, conservation, habitat linkage, Kenyir, road, selective logging Introduction Suitable habitats for forest-dependant small carnivores are disappearing faster in Southeast Asia than anywhere else in the world (Schipper et al - gional populations of mammal species may be extinct by 2100, according to one alarming. 2008). study (BrookIn fact, aboutet al. 2003). 21–48% One of key re mammal conservation strategy for the region has been the establishment of corridors or linkages to restore ecological connectivity between fragmented habitats (e.g. Kawanishi et al et al. 2012b). Unfortunately, there is a paucity of research on the functional role of such corridors. 2003, DWNPin this 2008,region Clements (Sodhi et al. 2010), with almost noth- ing known about their small carnivore communities. In Peninsular Malaysia, the Federal government’s pro- visional plan to restore ecological connectivity between four - - fragmented forest complexes via a network of 17 habitat link DOFages (hereafter2012). These known linkages as linkages; are threatened Fig. 1) is knownby anthropogenic as the Cen tral Forest Spine Master Plan for Ecological Linkages (DTCP & ondisturbance. some mammal, For example, bird and all amphibian but two of thespecies 17 are in bisectedthe tropics by (Lauranceroads (Fig. et1; alDTCP & DOF 2012), which have negative impacts - prise production. 2009). forest reserves designated for selective Many linkages within the Central Forest Spine also com otherwise disturbed forests can have high conservation value fortimber mammals extraction (Wells (DTCP et al & DOF 2012).et Selectively al. 2010, Foster logged et and al. 2011, Giam et al. 2011, Gibson et al 2011, Schwitzer et al. 2011, Putz et al. 2012), particularly. 2007, for largerBerry mammals in Peninsular et al. 2012a, Ray- an et al Malaysia (Rayan & Mohamad 2009, Clements . 2012), but the species-specific effects of commercial Fig. 1. Locations of 17 linkages (‘×’) identified by the Malaysian Federal recordedlogging on a declinemost small in some carnivores species ofare small uncertain carnivores (Colón (Heydon 2002, government in the country’s Central Forest Spine, including Linkage 7 Meijaard & Sheil 2008). Several studies in logged forests have (circled), subject of this study.
& Bulloh 1996, Colón 1999), whereas others suggest that many Small Carnivore Conservation
9 , Vol. 49: 9–14, December 2013 Hedges et al.
- Records were derived from a camera-trapping survey to rah et al et al. 2012). speciesTwenty persist species without of significant small carnivores population from declines four (Syaki fami- lies (Viverridae,. 2000, Meijaard Prionodontidae, & Sheil 2008, Mustelidae Samejima and Herpestidae) investigate habitat use by mammals in and around Linkage 7- inhabit Peninsular Malaysia (Francis 2008). In Malaysia, recent (Clements & Laurance 2012). Camera-trapping was conducted- records of small carnivores come mainly from production for- between April 2011 and March 2012, across dry (April–Sep× 2 km), et al. 2010, Wilt- tember)respectively. and wetWithin seasons each (October–March).cell, a camera-trap The was lower deployed and up in ing et al perthe upper-leftforest blocks sub-cell were stratified(1 × into 21 and 22 cells (2 - est reserves (e.g. Rayan & Shariff 2008, Mathai et al. 2011). Be- pling occasion, before being moved in a ‘Z’ - shaped manner cause the. 2010) designation and protected of linkages areas is (e.g. relatively Kawanishi recent & Sunquist at a na- until every sub-cell was surveyed. 1 km) duringThe lower the firstand upper60-day forest sam 2004, Brodie & Giordano 2011, Matsubayashi block respectively thereby had an array of 21 and 22 operation- is available on the small carnivores within them. al camera-traps during each of four sampling occasions. Within tionalThis policy paper level reports (DTCP the & DOFspecies 2012), composition very little and information detection each sub-cell, camera-traps were placed close to the centre of rates of small carnivores in and around one of Peninsular Malay- known to have high detection probabilities for some large the sub-cell, to minimise clumping, and/or on linear features linkagesia’s 17 inhabitat this country. linkages – Linkage 7, in the state of Terengganu. These are the first published data on small carnivores from a mammals (e.g. animal trail, ridge or old logging road). Camera- Location, materials and methods resultedtraps were in attachedlow detection to tree rates trunks of any~50 small cm above carnivore ground species level thatand 2–5avoid m these from typesthe trail’s of trails. centre. This survey design will have - Theft, malfunction, damage from Asian Elephants Ele- phas maximus, and blockage from vegetation all prevented use Located in the State of Terengganu, Linkage 7 is one of 17 hab- - turesitat linkages for vehicles) identified cuts withinthrough the this Central linkage Forest (Fig. Spine 2). The (Fig. study 1). A 60-km road with 10 underpasses (i.e. elevated road struc of some camera-traps’ data. The 158 sub-cells providing usa digitalble data elevation lay within model an elevational from the range Shuttle of 167–732Radar Topography m (Datum 2012).area consists Both forest of two blocks forest span blocks four totalling production 158 forest km², reserveswith the MissionWGS 84, elevation indicative database elevation and derived thus highly from 1approximate, km²-resolution es- (Tembat,lower forest Petuang, block encompassingHulu Telemong Linkage and Hulu 7 (see Nerus), DTCP &which DOF pecially in rugged terrain). ‘Day’ detections occurred between contain both lowland and hill dipterocarp forests. They were in either block during the present study, but forests were be- nearby07h00 andarea 18h59, with similar and ‘night’ sun-set detections and -rise between times. No19h00 attract and- ingfirst clear-felled selectively loggedfor construction in the 1970s. of aNo hydro-electric logging was conducted dam out- 06h59, following Kawanishi & Sunquist’s (2008) study in a- human settlements exist in the forest blocks. ants were employed around the cameras. Camera-trap pho side the study area (over 6 km away; Fig. 2). No permanent tos were catalogued using software Camera Base version 1.4 (http://www.atrium-biodiversity.org/tools/camerabase). To
Fig. 2. Locations of 158 camera-trap stations within two forest blocks that were stratified into 1× 1 km sub-cells in and around Linkage 7, Terengganu, Peninsular Malaysia.
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, Vol. 49, December 2013 Small carnivores in a Malaysian habitat linkage facilitate comparisons with other studies, a notionally inde- Paradoxurus hermaphroditus were by night, consistent with previously documented activity patterns of these four species speciespendent at photograph the same camera-trap was defined station. as a photograph of a species Arctictis bintu- taken at least 0.5 hr after the previous photograph of the same rong(e.g. Van photos Schaik were 1996, taken Duckworth during the 1997, day, Grassmansupporting 1998, the notion Azlan Results and discussion 2006, Francis 2008). A third of the Binturong -
Twelve species of small carnivores were detected in and around speciesthat they were are detectednot solely singly nocturnal except (e.g. for Nettelbeck Yellow-throated 1997, MarBro- - tendie &Martes Giordano flavigula 2011)., which All adult was individualsdetected in ofduos small in carnivorethree out of seven photographs; others have also found them in duos or camera-trap-nights,Linkage 7, all of which one are was typical camera-trapped of lowland and subsequently, hill diptero et al onecarp wasforests. found Nine as ofa roadkillthem were and camera-trapped another was photographed over 10,502 in situ smallEight groups species (Duckworth of small 1997, carnivore Grassman known to occur2005, inParr Pen &- the adjacent Taman Negara National Park, with its boundary insularDuckworth Malaysia 2007). were not detected. Of four possible explana- (Table 1, Appendix 1). Kawanishi & Sunquist (2004), in the study area’s dense rainforest is unlikely to support Small ~4 km from our nearest camera-trap, detected nine species of Asiantions forMongoose this, the Herpestesfirst is inappropriate javanicus habitat. For example, trappedsmall carnivores small carnivore from 14,054 was Banded camera-trap-nights. Linsang Prionodon linsang Viverricula indica, which may occur mainly in open scrub-like (TableIn 1). and This around is surprising Linkage given 7, the its mosttypical frequently relative paucity camera- of and Small Indian Civet records during camera-trapping (e.g. Mathai et al. 2010, Wilting et al
. 2010, Brodie & Giordano 2011), including in Peninsular Malaysia (Taman Negara, Kawanishi & SunquistHerpestes 2004; Gunong urva, whichBasor Foresthas been Reserve, considered Rayan in2007). Malaysia to be rare and patch- The presence of Crab-eating Mongoose state of Terengganu, extending its known range south-east- wardsily distributed by over 100(Lim km 1991), from represents the previous the eastern-most first record forrecord the ′ ″N, ′30″ inwith Peninsular three juveniles, Malaysia three (Gunung weeks Basor,after a Kelantan,photograph 3°49 of a53 lone individual103°35 atE; the Rayan same & station Shariff (Fig.2008). 3). OneThe imageapproximate had an eleva adult- tions of the species’s records, within 600–700 m (Appendix 1), fall within the known range used in Malaysia (10–1,400 m;- Fig. 3. Camera-trapped adult Crab-eating Mongoose Herpestes urva Rayan & Shariff 2008). Viverra zibetha, with three juveniles, Linkage 7, Terengganu, Peninsular Malaysia, 27 All five detectionsPaguma of Crab-eating larvata Mongoose were dur December 2011. ing the day, but all those of Large Indian Civet Masked Palm Civet and Common Palm Civet Table 1. The 12 small carnivore species detected in and around Linkage 7. Terengganu, Peninsular Malaysia, 2011–2012. Species N PCRI Stations Red List Day Night Yellow-throated Marten Martes flavigula 7 0.07 6 LC 6 1 Oriental Small-clawed Otter Aonyx cinereus ** - - 1 VU - - Smooth-coated Otter Lutrogale perspicillata *** - - 1 VU - - Banded Linsang Prionodon linsang 9 0.09 9 LC 0 9 Malay Civet Viverra tangalunga 2 0.02 2 LC 0 2 Large Indian Civet Viverra zibetha 4 0.04 4 NT 0 4 Banded Civet Hemigalus derbyanus 2 0.02 2 VU 0 2 Masked Palm Civet Paguma larvata 5 0.05 4 LC 0 5 Common Palm Civet Paradoxurus hermaphroditus 2 0.02 2 LC 0 2 Binturong Arctictis binturong 3 0.03 3 VU 1 2 Small-toothed Palm Civet Arctogalidia trivirgata * - - - LC - - Crab-eating Mongoose Herpestes urva 5 0.05 2 LC 5 0 N = notionally independent detections (0.5 hr intervals); PCRI = Photographic Capture Rate Index (N/100 camera-trap- nights; based on O’Brien et al. 2003) over 10,502 camera-trap-nights; Stations = number of camera-traps (out of 158) that detected the species; Red List = IUCN Red List of Threatened Species category; Day = number of day detections; Night = number of night detections. *identified from a roadkill within the study area. **daytime detection during ongoing camera-trapping survey in the study area. ***species photographed by day in situ.
11 Small Carnivore Conservation
, Vol. 49, December 2013 Hedges et al. areas (e.g. Francis 2008). In Peninsular Malaysia, Short-tailed - Mongoose Herpestes brachyurus seems to have been detected ity ‘targets’ for future small carnivore studies in the linkages. Otter Civet and, further north, Large-spotted Civet), are prior Borneo (e.g. Mathai et al. 2010, Matsubayashi et al. 2011) and Acknowledgements thusonly mightbelow yet100 be m found (Wells at 1989),much higher although elevations it ranges on higherPeninsu in- - lar Malaysia. The second possible explanation is camera-trap placement. Non-detection of Hairy-nosed Otter Lutra sumatra- We are especially grateful to Dato’ Toh Chin Yaw, Chairman of the In na Cynogale bennettii dustry, Trade and Environment Committee for the Terengganu State of most camera-traps away from water bodies. The non-detec- Government, who took heed of our findings and assisted in halting the tion and of Malay Otter WeaselCivet Mustela nudipes could reflect placement Primedevelopment Minister’s along Department the highway and bisecting the Department Linkage of 7. Wildlife GRC would and likeNa- placement inimical to detecting this species, typically camera- tionalto thank Parks the Economic(HQ and Terengganu) Planning Unit for (Permit granting number permission 3072) to from under the- trapped only rarely (Duckworth et al could reflect camera-trapet al. 2013). take this project, as well as the Department of Forestry (Terengganu) A third possible explanation is extinction: the introduced In- for granting permission to enter the forest reserves in Kenyir. We are dian Grey Mongoose Herpestes edwardsii 2006, is now Ross likely to be ex-
2010). The fourth explanation is that the species may have indebted to financial support from the U.S. Fish and Wildlife Service nevertinct in naturally Peninsular occurred Malaysia in this (Wells geographical 1989, Francis area. 2008, Earlier, DWNP gen- Rhino and Tiger Conservation Fund (GRC), Rufford Small Grant for eralised, claims of an extensive distribution of Large-spotted Nature Conservation (GRC), Cleveland Metroparks Zoo and Cleveland Viverra megaspila Zoological Society Asian Seed Grant (GRC), IDEA WILD (GRC), James Cook University Graduate Research Scheme (GRC), Universiti Malaya Civetdetailed collation and evaluation in Peninsular of records Malaysia from (Corbett the country, & Hill Research Grant (GRC), James Cook University Postgraduate Research which1992, Papeşsuggests & Gaubert strongly 2007, that it Francis inhabits 2008), only theare northwestcontested byof Scholarship (GRC), Mohamed bin Zayed Species Conservation Fund- (LH, GRC), Kay Arnold and Ian Mellsop (LH, GRC) and the Australian Research Council (WFL). This project would also not be possible with ConclusionPeninsula Malaysia (Jennings & Veron 2011). hisout comments,our indigenous Nicole field Duplaix assistants for her and assistance many friends in identifying and volunteers the spe- (http://myrimba.org/donors). We thank Ahimsa Campos-Arceiz for The species composition of small carnivores in Peninsular reviewer for improving the quality of this manuscript. Malaysia’s habitat linkages was hitherto little known. The cies of otters, and John Mathai, Kae Kawanishi and one anonymous - References est small carnivore species totals documented from a single study12 species in Peninsular detected Malaysia in Linkage to date. 7 represent Four of these one of species the high are secondary forest in Peninsular Malaysia. Biodiversity and Con- globally threatened (all categorised as Vulnerable) according Azlanservation J. B. A. G. A., M. 2006. 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Appendix 1. Geographical coordinates and indicative elevation of the 12 small carnivore species recorded in and around Linkage 7, Terengganu, Peninsular Malaysia, 2011–2012. Latitude N Longitude E Elevation (m) Latitude N Longitude E Elevation (m) Yellow-throated Marten Martes flavigula Banded Civet Hemigalus derbyanus 4°58′37.2″ 102°31′04.8″ 216 5°03′03.6″ 102°33′32.4″ 242 4°59′38.4″ 102°30′54.0″ 239 5°00′21.6″ 102°32′31.2″ 203 5°10′33.6″ 102°46′58.8″ 198 Masked Palm Civet Paguma larvata 5°00′21.6″ 102°32′31.2″ 203 5°03′07.2″ 102°30′46.8″ 620 5°03′25.2″ 102°31′22.8″ 562 5°03′07.2″ 102°31′15.6″ 662 5°12′46.8″ 102°43′48.0″ 446 5°02′24.0″ 102°30′39.6″ 600 Oriental Small-clawed Otter Aonyx cinereus 5°00′03.6″ 102°33′25.2″ 353 5°00′54.0″ 102°31′37.2″ 218 5°03′25.2″ 102°30′39.6″ 825 Smooth-coated Otter Lutrogale perspicillata Common Palm Civet Paradoxurus hermaphroditus 5°03′38.0″ 102°33′49.7″ 160 5°13′30.0″ 102°46′04.8″ 392 Banded Linsang Prionodon linsang 5°13′30.0″ 102°46′04.8″ 392 4°59′38.4″ 102°30′54.0″ 239 4°59′31.2″ 102°32′24.0″ 179 5°00′21.6″ 102°32′31.2″ 203 5°10′01.2″ 102°47′02.4″ 272 4°58′04.8″ 102°30′46.8″ 286 Binturong Arctictis binturong 5°12′46.8″ 102°42′10.8″ 472 4°58′37.2″ 102°31′22.8″ 233 5°11′42.0″ 102°47′31.2″ 384 5°11′49.2″ 102°41′45.6″ 269 5°01′26.4″ 102°34′30.0″ 412 5°10′40.8″ 102°43′30.0″ 444 5°09′25.2″ 102°43′40.8″ 310 Small-toothed Palm Civet Arctogalidia trivirgata 5°00′03.6″ 102°33′25.2″ 353 5°10′40.2″ 102°47′48.0″ 156 4°59′16.8″ 102°31′55.2″ 184 Crab-eating Mongoose Herpestes urva Malay Civet Viverra tangalunga 5°13′33.6″ 102°43′51.6″ 673 4°58′37.2″ 102°31′22.8″ 233 5°12′57.6″ 102°43′22.8″ 648 5°03′00.0″ 102°34′26.4″ 303 Large Indian Civet Viverra zibetha 4°59′09.6″ 102°30′03.6″ 486 5°12′50.4″ 102°44′16.8″ 357 5°00′18.0″ 102°31′19.2″ 215 5°12′46.8″ 102°43′48.0″ 446
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