Group densities of endangered small apes (Hylobatidae) in two adjacent forest reserves in Merapoh, Pahang, Malaysia

Main Article Content

Adilah Suhailin Kamaruzaman
Nurul Iza Adrina Mohd Rameli
Susan Lappan
https://orcid.org/0000-0002-0139-8837
Thad Quincy Bartlett
https://orcid.org/0000-0001-5994-9454
Nik Rosely Nik Fadzly
Mohd Sah Shahrul Anuar
Nadine Ruppert
https://orcid.org/0000-0002-9760-0058

Abstract

Small ape habitat is rapidly declining due to anthropogenic activities but the current population status of this endangered primate family in Malaysia remains unknown. Group densities of Hylobates lar and Symphalangus syndactylus in two adjacent forest reserves across the Sungai Yu Ecological Corridor (SYEC) in Merapoh, a critical connectivity area of the Central Forest Spine, were assessed. Vegetation assessment and satellite imagery were used to identify habitat characteristics and fixed-point active acoustic triangulation at six listening areas was conducted to estimate small ape group densities. Small ape habitat quality was high in the forested areas of the SYEC. The mean group density of H. lar across these six areas was 3.55 ± 0.9 groups km-² while the mean group density of S. syndactylus was 2.75 ± 1.0 groups km-². The mean group densities of small apes at SYEC were moderately high, compared with densities at other sites in the region, which suggests that the forests here constitute good habitat for both species, despite some observed anthropogenic disturbances. Both species occurred in all listening areas. A nationwide population census for small apes and regular monitoring to inform conservation planning are recommended. Further improvement to connectivity across the SYEC by installing artificial canopy bridges for arboreal animals is important to support the movement of small apes across habitat fragments in Merapoh.

Article Details

Section
Articles

Funding data

References

Asensio, N., J. Kachanan, C. Saralamba & J.M. José-Domínguez (2021). The impact of roads on the movement of arboreal fauna in protected areas: the case of lar and pileated gibbons in Khao Yai National Park, Thailand. Journal of Tropical Ecology 37(6): 276–285. https://doi.org/10.1017/S0266467421000390

Balbuena, D., A. Alonso, M. Panta, A. Garcia & T. Gregory (2019). Mitigating tropical forest fragmentation with natural and semi-artificial canopy bridges. Diversity 11(4): 66. https://doi.org/10.3390/d11040066https://doi.org/10.3390/d11040066

Bartlett, T.Q. (2010). The Hylobatidae: Small apes of Asia, pp. 274–289. In: Campbell, C., A. Fuentes, K. MacKinnon, S. Bearder & R. Stumpf (eds.). Primates in Perspective, 2nd Edition. Oxford University Press, UK, 864 pp.

Brockelman, W.Y. & R. Ali (1987). Methods of surveying and sampling forest primate populations, pp. 23–63. In: Marsh, C.W. & R.A. Mittermeier (eds). Primate Conservation in Tropical Rainforests. Alan R. Liss, USA, 365 pp.

Brockelman, W.Y. & S. Srikosamatara (1993). Estimation of density of gibbon groups by use of loud songs. American Journal of Primatology 29(2): 93–108. https://doi.org/10.1002/ajp.1350290203

Brockelman, W.Y. & T. Geissmann (2020). Hylobates lar. The IUCN Red List of Threatened Species 2020: e.T10548A17967253. Downloaded on 23 May 2023. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T10548A17967253.en

Caldecott, J.O. (1980). Habitat quality and populations of two sympatric gibbons (Hylobatidae) on a mountain in Malaya. Folia Primatologica 33(4): 291–309. https://doi.org/10.1159/000155943

Cannon, C., & M. Leighton (1994). Comparative locomotor ecology of gibbons and macaques: Selection of canopy elements for crossing gaps. American Journal of Physical Anthropology 93(4): 505–524. https://doi.org/10.1002/ajpa.1330930409

Chan, B.P.L., Y.F.P. Lo, X.J. Hong, C.F. Mak & Z. Ma (2020). First use of artificial canopy bridge by the world’s most critically endangered primate the Hainan gibbon Nomascus hainanus. Scientific Reports 10(1): 15176. https://doi.org/10.1038/s41598-020-72641-z

Cheyne, S.M., C.J. Thompson, A.C. Phillips, R.M. Hill & S.H. Limin (2008). Density and population estimate of gibbons (Hylobates albibarbis) in the Sabangau catchment, Central Kalimantan, Indonesia. Primates 49: 50–56. https://doi.org/10.1007/s10329-007-0063-0

Cheyne, S., C. Thompson & D.J. Chivers (2013). Travel adaptations of Bornean Agile Gibbons Hylobates albibarbis (Primates: Hylobatidae) in a degraded secondary forest, Indonesia. Journal of Threatened Taxa 5(5): 3963–3968. https://doi.org/10.11609/JoTT.o3361.3963-8

Cheyne, S.M., L.J. Gilhooly, M.C. Hamard, A. Höing & P.R. Houlihan (2016). Population mapping of gibbons in Kalimantan, Indonesia: correlates of gibbon density and vegetation across the species’ range. Endangered Species Research 30: 133–143.

Cheyne, S., B. Capilla, K. Abdulaziz, Supiansyah, Adul, E. Cahyaningrum & D. Smith (2019). Home range variation and site fidelity of Bornean southern gibbons (Hylobates albibarbis) from 2010–2018. PLoS ONE 14(7): 1–13.

Cheyne, S.M. & V. Nijman (2020). Hylobates abbotti. The IUCN Red List of Threatened Species 2020: e.T39889A17990882. Downloaded on 23 May 2023. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T39889A17990882.en

Chapman, C.A., M.J. Lawes & H.A. Eeley (2006). What hope for African primate diversity? African Journal of Ecology 44(2): 116–133. https://doi.org/10.1111/j.1365-2028.2006.00636.x

Chivers, D.J. (1977). Socio-ecology and Conservation of Malayan Forest Primates. Environmental Conservation 4(2): 102.

Chivers, D.J. (1984). Feeding and ranging in gibbons: a summary, pp. 267–281. In: Preuschoft, H., D.J. Chivers, W.Y. Brockelman & N. Creel (eds.). The Lesser Apes: Evolutionary and Behavioural Biology. Edinburgh University Press, U.K., 709 pp.

Elder, A.A. (2009). Hylobatid diets revisited: the importance of body mass, fruit availability, and interspecific competition, pp. 133–159. In: Lappan, S. & D.J. Whittaker (eds.). The Gibbons: New Perspectives on Small Ape Socioecology and Population Biology. Springer, USA, 526 pp. https://doi.org/10.1007/978-0-387-88604-6_8

Elder, A.A. (2013). Competition among three primate species at Way Canguk, Sumatra, Indonesia. PhD Thesis. Department of Anthropology, State University of New York at Stony Brook, xxii+272 pp. https://www.proquest.com/openview/988854f8758f8d5d54ec2942e7e1614c/1?pq-origsite=gscholar&cbl=18750

Estrada, A., P.A. Garber, A.B. Rylands, C. Roos, E. Fernandez-Duque & A. Di Fiore (2017). Impending extinction crisis of the world’s primates: Why primates matter. Science Advances 3(1): e1600946. https://doi.org/10.1126/sciadv.1600946

Estrada, A., P.A. Garber & A. Chaudhary (2019). Expanding global commodities trade and consumption place the world’s primates at risk of extinction. PeerJ 7: e7068. https://doi.org/10.7717/peerj.7068

Geissmann, T., V. Nijman, R. Boonratana, W.Y. Brockelman, C. Roos & M.G. Nowak (2020). Hylobates agilis. The IUCN Red List of Threatened Species 2020: e.T10543A17967655. Downloaded on 23 May 2023. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T10543A17967655.en

Geissmann, T. (2007). Status reassessment of the gibbons: results of the Asian primate red list workshop 2006. Gibbon Journal 7(3): 5–15.

Gibbs, J.P. (2001). Demography versus habitat fragmentation as determinants of genetic variation in wild populations. Biological Conservation 100(1): 15–20. https://doi.org/10.1016/S0006-3207(00)00203-2

Gittins, S.P. (1980). Territorial behavior in the Agile Gibbon. International Journal of Primatology 1(4): 381–399. https://doi.org/10.1007/BF02692281

Gregory, T., F.C. Rueda, J. Deichmann, J. Kolowski, M.C. Faura, F. Dallmeier & A. Alonso (2013). Methods to establish canopy bridges to increase natural connectivity in linear infrastructure development. In: SPE Latin-American and Caribbean Health, Safety, Environment and Social Responsibility Conference, 26-27 June 2013; OnePetro, Peru. https://doi.org/10.2118/165598-MS

Haimoff, E.H. & S.P. Gittins (1985). Individuality in the songs of wild agile gibbons (Hylobates agilis) of Peninsular Malaysia. American Journal of Primatology 8(3): 239–247. https://doi.org/10.1002/ajp.1350080306

Hamard, M., S.M. Cheyne & V. Nijman (2010). Vegetation correlates of gibbon density in the peat-swamp forest of the Sabangau catchment, Central Kalimantan, Indonesia. American Journal of Primatology 72: 607–616. https://doi.org/10.1002/ajp.20815

Hansen, M.C., P.V. Potapov, R. Moore, M. Hancher, S.A. Turubanova, A. Tyukavina, D. Thau, S. Stehman, S. Goetz, T. Loveland, A. Kommareddy, A. Egorov, L. Chini, C. Justice & J.R. Townshend (2013). High‐resolution global maps of 21st century forest cover change. Science 342: 850–853. https://doi.org/10.1126/science.1244693

Hughes, A.C. (2017). Understanding the drivers of Southeast Asian biodiversity loss. Ecosphere 8(1): e01624. https://doi.org/10.1002/ecs2.1624

IC-CFS (2021). https://www.ic-centralforestspine.com.my/. Accessed on 23 May 2023.

Johns, A.D. (1986). Effects of selective logging on the behavioral ecology of West Malaysian primates. Ecology 67(3): 684–694. https://doi.org/10.2307/1937692

Laidlaw, R.K. (2000). Effects of habitat disturbance and protected areas on mammals of Peninsular Malaysia. Conservation Biology 14(6): 1639–1648. https://doi.org/10.1111/j.1523-1739.2000.99073.x

Leighton, D.R. (1987). Gibbons: Territoriality and Monogamy, pp. 135–145. In: Smuts, B.B., D.L. Cheney, R.M. Seyfarth, R.W. Wrangham & T.T. Struhsaker (eds.). Primate Societies. University of Chicago Press, USA, 585 pp. https://doi.org/10.7208/9780226220468-014

Link, A., & A. Di Fiore (2006). Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity. Journal of Tropical Ecology 22(3): 235. https://doi.org/10.1017/S0266467405003081

Lucas, P.W. & R.T. Corlett (1998). Seed dispersal by long‐tailed macaques. American Journal of Primatology 45(1): 29–44. https://doi.org/10.1002/(SICI)1098-2345(1998)45:1<29::AID-AJP4>3.0.CO;2-Y

MacKinnon, J. & K. MacKinnon (1980). The behavior of wild spectral tarsiers. International Journal of Primatology 1(4): 361–379. https://doi.org/10.1007/BF02692280

Marshall, A.J., C.M. Boyko, K.L. Feilen, R.H. Boyko & M. Leighton (2009). Defining fallback foods and assessing their importance in primate ecology and evolution. American Journal of Physical Anthropology 140(4): 603–614. http://doi.org/10.1002/ajpa.21082

Marshall, A.J. (2010). Effect of habitat quality on primate populations in Kalimantan: gibbons and leaf monkeys as case studies, pp. 157–177. In: J. Supriatna & S.L. Gursky (eds.). Indonesian Primates. Springer, USA. Xvi+410 pp.

McConkey, K.R. (2009). The seed dispersal niche of gibbons in Bornean dipterocarp forests, pp. 189–207. In: Lappan, S. & D.J. Whittaker (Eds). The Gibbons: New Perspectives on Small Ape Socioecology and Population Biology. Springer, USA, 526 pp. https://doi.org/10.1007/978-0-387-88604-6_10

Meisery, A.A.H.A., L. Adam, A.N. Ghazali, M.H.H. Shah, M.F. Yazi, C.C. Tan, P.A. Patah, M. Azhari & S. Fairi (2020). Diversity of mammals in Sungai Yu Ecological Corridor, Pahang. Journal of Wildlife and Parks 35: 1–15. https://jwp.wildlife.gov.my/index.php/jwp/article/view/14

Mitani, J.C. (1987). Territoriality and monogamy among agile gibbons (Hylobates agilis). Behavioral Ecology and Sociobiology 20(4): 265–269. https://doi.org/10.1007/BF00292179

Nijman, V. (2001). Effects of behavioural changes due to habitat disturbance on density estimation of rain forest vertebrates, as illustrated by gibbons (Primates: Hylobatidae), pp. 33–42. In: Hillegers, P. & H. H. di Iongh (eds.). Forest and primates: conservation and ecology of the endemic primates of Java and Borneo. Tropenbos Foundation, Netherlands, 278 pp.

Nijman, V., T. Geissmann, C. Traeholt, C. Roos & M.G. Nowak (2020). Symphalangus syndactylus. The IUCN Red List of Threatened Species 2020: e.T39779A17967873. Downloaded on 23 May 2023. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T39779A17967873.en

Nijman, V., S. Cheyne & C. Traeholt (2020). Hylobates funereus. The IUCN Red List of Threatened Species 2020: e.T39890A17990856. Downloaded on 23 May 2023. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T39890A17990856.en

‘Brien, T.G., M.F. Kinnaird, A. Nurcahyo, M. Prasetyaningrum & M. Iqbal (2003). Fire, demography, and the persistence of siamang (Symphalangus syndactylus: Hylobatidae) in a Sumatran rainforest. Animal Conservation 6: 115–121. https://doi.org/10.1017/S1367943003003159

O’Brien, T.G., M.F. Kinnaird, A. Nurcahyo, M. Iqbal & A. Rusmanto (2004). Abundance and distribution of sympatric gibbons in a threatened Sumatran rain forest. International Journal of Primatology 25(2): 267–284. https://doi.org/10.1023/B:IJOP.0000019152.83883.1c

O’Grady, J.J., B.W. Brook, D.H. Reed, J.D. Ballou, D.W. Tonkyn & R. Frankham (2006). Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biological Conservation 133(1): 42–51. https://doi.org/10.1016/j.biocon.2006.05.016

Ong, L., K.R. McConkey & A. Campos‐Arceiz (2022). The ability to disperse large seeds, rather than body mass alone, defines the importance of animals in a hyper‐diverse seed dispersal network. Journal of Ecology 110(2): 313–326. https://doi.org/10.1111/1365-2745.13809

Palombit, R. (1993). Lethal territorial aggression in a White-Handed Gibbon. American Journal of Primatology 31: 311–318.

Palombit, R.A. (1997). Inter-and intraspecific variation in the diets of sympatric Siamang (Hylobates syndactylus) and Lar Gibbons (Hylobates lar). Folia Primatologica 68(6): 321–337. https://doi.org/10.1159/000157260

Pang, Y.H., S. Lappan, T.Q. Bartlett, S.A.M. Sah, N.F.N. Rosely & N. Ruppert (2022). Population densities of Hylobates agilis in forests with different disturbance histories in Ulu Muda Forest Reserve, Malaysia. American Journal of Primatology 84(7): e23388. https://doi.org/10.1002/ajp.23388

Phoonjampa, R. & W.Y. Brockelman (2008). Survey of pileated gibbon Hylobates pileatus in Thailand: populations threatened by hunting and habitat degradation. Oryx 42(4): 600–606. https://doi.org/10.1017/S0030605308000306

Phoonjampa, R., A. Koenig, W.Y. Brockelman, C. Borries, G.A. Gale, J.P. Carroll & T. Savini (2011). Pileated gibbon density in relation to habitat characteristics and post‐logging forest recovery. Biotropica 43(5): 619–627. https://doi.org/10.1111/j.1744-7429.2010.00743.x

Raemaekers, J. (1978). Changes through the day in food choice of wild gibbons. Folia Primatologica 30: 194–205.

Smith, R.J. & W.L. Jungers (1997). Body mass in comparative primatology. Journal of Human Evolution 32(6): 523–559. https://doi.org/10.1006/jhev.1996.0122

Srikosamatara, S. (1984). Ecology of pileated gibbons in southeast Thailand, pp. 242–257. In: H. Preuschoft, D.J. Chivers, W.Y. Brockelman & N. Creel (eds.). The Lesser Apes: Evolutionary and Behavioural Biology. Edinburgh University Press, UK, 709 pp.

Sutherland, W.J. (2000). Mammals, pp. 57–59. In: Sutherland, W.J. (ed.). The Conservation Handbook: Research, Management and Policy. Oxford: Blackwell Science Ltd, UK, 294 pp.

Teixeira, F.Z., R.C. Printes, J.C.G. Fagundes, A.C. Alonso & A. Kindel (2013). Canopy bridges as road overpasses for wildlife in urban fragmented landscapes. Biota Neotropica 13: 117–123. https://doi.org/10.1590/S1676-06032013000100013

Weston, N., M. Goosem, H. Marsh, M. Cohen & R. Wilson (2011). Using canopy bridges to link habitat for arboreal mammals: successful trials in the wet tropics of Queensland. Australian Mammalogy 33(1): 93–105. https://doi.org/10.1071/AM11003

Yap, J.L., N.F.N. Rosely, M. Mahadzir, M.L. Benedict, V. Muniandy & N. Ruppert (2022). “Ah Lai’s Crossing”–Malaysia’s first artificial road canopy bridge to facilitate safer arboreal wildlife crossings. Folia Primatologica 93(3–6): 255–269. https://doi.org/10.1163/14219980-20211105

Yanuar, A. (2001). The Population Distribution and Abundance of Primates in Kerinci-Seblat National Park, Sumatra, Unpublished MSc Thesis, University of Cambridge, Cambridge, UK.

Yokochi, K. & R. Bencini (2015). A remarkably quick habituation and high use of a rope bridge by an endangered marsupial, the western ringtail possum, pp. 79–94. In: Seiler, A. & J.-O. Helldin (eds.). Proceedings of IENE 2014 International Conference on Ecology and Transportation, Malmö, Sweden. Nature Conservation 11: 74–94. https://doi.org/10.3897/natureconservation.11.4385

Zhang, D., H. Fei, S. Yuan, W. Sun, Q. Ni, L. Cui & P. Fan (2014). Ranging behavior of Eastern Hoolock Gibbon (Hoolock leuconedys) in a northern montane forest in Gaoligongshan, Yunnan, China. Primates 55(2): 239–247.

Zihlman, A.L., A.R. Mootnick & C.E. Underwood (2011). Anatomical contributions to hylobatid taxonomy and adaptation. International Journal of Primatology 32(4): 865–877.