Sains Malaysiana 51(6)(2022): 1635-1651

http://doi.org/10.17576/jsm-2022-5106-03

Microhabitat and Microclimate Preferences of Anuran Species Inhabiting Restoration and Adjacent Forest of Cameron Highlands, Pahang Darul Makmur, Malaysia

(Keutamaan Mikrohabitat dan Mikroklimat Spesies Anuran yang Mendiami Pemulihan dan Hutan Bersebelahan Tanah Tinggi Cameron, Pahang Darul Makmur, Malaysia)

NADIA SIMON¹, MARINA MOHD. TOP^{1,2, *}, MOHD. ZAKI HAMZAH³, NOR AZWADY ABDUL AZIZ¹, MOHAMAD AZANI ALIAS³, MOHD. RIDZA AWANG⁴, ZAHARI IBRAHIM⁴, AHMAD FADZIL ABD. MAJID⁴, MOHD. SYAHRIR AZRIN SALLEH⁴ & AZHAR ANUAR⁴

¹Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia

²Centre of Foundation Studies for Agricultural Sciences, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia

³Department of Forestry Science and Biodiversity, Faculty of Forestry and Environment, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia

⁴Forestry Department of Peninsular Malaysia, Jalan Sultan Salahuddin, 50660 Kuala Lumpur, Federal Territory, Malaysia

Received: 14 February 2021/Accepted: 2 November 2021

Abstract

The conversion of forests to agricultural farmland modifies lands into small patches, making amphibians more susceptible to external environmental changes. It is important to restore the forest ecosystem so that fauna species, especially anurans, could gradually recover and help create a balanced ecosystem in the restoration process. The aims of this study are to determine diversity, richness, and evenness of the anuran species, and to investigate the relationship of the anuran species with environmental variables of restoration areas and adjacent forests of Terla Forest Reserve (FR), Cameron Highlands, Pahang. The study recorded 14 species belonging to six families with higher species diversity, whereby the Shannon Wiener (H’) value in the adjacent forest (H’ = 1.71) was higher as compared to the restoration area (H’ = 0.77). The anuran species in the restoration area showed an adaptation to bare soil, herbs, and shrubs. Meanwhile, in the forest, forest litter was favoured by the anuran species. Species abundance demonstrated correlation towards microclimate. The adaption of two species to the restoration area showed that temperature had a significant and negative correlation with Duttaphrynus melanostictus; relative humidity was significant and positively correlated with Polypedates leucomystax; while relative humidity had a significant and negative correlation with Microhyla annectens, a forest specialist. A deeper understanding of environmental factors that affect the presence of anurans, especially in restoration areas, can facilitate forest management in evaluating the effectiveness of forest restoration in this region.

Keywords: Agriculture; amphibian; biodiversity; highland; species richness

Abstrak

Penukaran hutan menjadi ladang pertanian mengubah tanah kepada kawasan kecil mengakibatkan amfibia lebih bergantung pada perubahan persekitaran luaran. Pemulihan ekosistem hutan adalah penting supaya spesies fauna, terutamanya spesies anura, akan pulih secara beransur-ansur, menggalakkan kawasan restorasi dan membantu mewujudkan ekosistem yang seimbang dalam proses pemulihan. Tujuan kajian ini adalah untuk menentukan kepelbagaian, kekayaan dan keserataan spesies serta menyelidiki hubungan spesies anura dengan pemboleh ubah persekitaran di kawasan restorasi dan hutan berhampiran iaitu di Hutan Simpan Terla, Tanah Tinggi Cameron, Pahang. Kajian merekodkan 14 spesies anura yang terdiri daripada enam famili dengan kepelbagaian spesies, Shannon-Wiener (H’) yang lebih tinggi di kawasan hutan berdekatan (H’ = 1.71) berbanding kawasan restorasi (H’ = 0.77). Spesies anura di kawasan restorasi menunjukkan adaptasi terhadap kawasan tanah kosong dan tumbuhan semak sementara di hutan, sesampah hutan disukai oleh spesies anura. Kelimpahan spesies menunjukkan korelasi terhadap mikroiklim. Dua spesies yang beradaptasi terhadap kawasan restorasi menunjukkan suhu berkorelasi negatif dan signifikan terhadap Duttaphrynus melanostictus; kelembapan relatif berkolerasi positif dan signifikan terhadap Polypedates leucomystax; sementara kelembapan relatif berkolerasi negatif yang signifikan terhadap spesies hutan, Microhyla annectens. Pemahaman yang lebih mendalam mengenai faktor persekitaran yang mempengaruhi kehadiran spesies anura, terutama di kawasan restorasi akan memudahkan pengurusan hutan dalam menilai keberkesanan pemulihan hutan di wilayah ini.

Kata kunci: Amfibia; kekayaan spesies; kepelbagaian biologi; pertanian; tanah tinggi

REFERENCES

Alvarez, D. & Nicieza, A.G. 2002. Effects of temperature and food quality on anuran larval growth and metamorphosis. Functional Ecology 16(5): 640-648.

Ash, A.N. 1997. Disappearance and return of plethodontid salamanders to clearcut plots in the Southern Blue Ridge Mountains. Conservation Biology 11(4): 983-989.

Barrow, C.J., Clifton, J., Chan, N.W. & Tan, Y.L. 2005. Sustainable development in the Cameron Highlands, Malaysia. Malaysian Journal of Environmental Management 6: 41-57.

Berry, P.Y. 1975. The Amphibian Fauna of Peninsular Malaysia. Kuala Lumpur: Tropical Press. p. 29.

Blaustein, A.R., Wake, D.B. & Sousa, W.P. 1994. Amphibian declines: Judging stability, persistence, and susceptibility of populations to local and global extinctions. Conservation Biology 8(1): 60-71.

Browne, R.K. & Edwards, D.L. 2003. The effect of temperature on the growth and development of the endangered green and golden bell frog (Litoria aurea). Journal of Thermal Biology 28(4): 295-299.

Chan, N.W., Suriati, G. & Norizan, M.N. 2006. Chapter 4: Climate change and heat island effects in Cameron Highlands, Malaysia. In Cameron Highlands-Issues & Challenges in Sustainable Development. School of Humanities, Universiti Sains Malaysia. pp. 35-55.

Chan, K.O. & Grismer, L.L. 2021. Integrating spatial, phylogenetic, and threat assessment data from frogs and lizards to identify areas for conservation priorities in Peninsular Malaysia. Global Ecology and Conservation 28: e01650.

Chan, K.O., Muin, M.A., Anuar, S., Andam, J., Razak, N. & Aziz, M.A. 2019. First checklist on the amphibians and reptiles of Mount Korbu, the second highest peak in Peninsular Malaysia. Check List 15(6): 1055-1069.

Chan, K.O., Wood, P.L.J., Anuar, S., Muin, M.A., Quah, E.S., Sumarli, A.X. & Grismer, L.L. 2014. A new species of upland stream toad of the genus Ansonia Stoliczka, 1870 (Anura: Bufonidae) from northeastern Peninsular Malaysia. Zootaxa 3764(4): 427-440.

Chan, K.O., Grismer, L.L., Ahmad, N. & Belabut, D.M. 2009. A new species of Gastrophrynoides (Anura: Microhylidae): An addition to a previously monotypic genus and a new genus. Zootaxa 2124: 63-68.

Colwell, R.K., Chao, A., Gotelli, N.J., Lin, S.Y., Mao, C.X., Chazdon, R.L. & Longino, J.T. 2012. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology 5(1): 3-21.

Coulloudon, B., Podborny, P., Eshelman, K., Rasmussen, A., Gianola, J., Robles, B., Habich, N., Shaver, P., Hughes, L., Spehar, J., Johnson, C., Willoughby, J. & Pellant, M. 1999. Sampling vegetation attributes. BLM, Technical Reference 1999: 1734.

Crump, M.L. & Scott Jr., N.J. 1994. Visual encounter surveys. In ‘Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians’, edited by Heyer, W.R., Donnelly, M.A., McDiarmid, R.W., Hayek, L.C. & Foster, M.S. Washington: Smithsonian Institution. pp. 84-92.

Cubides, P.I. & Cardona, J.U. 2011. Anthropogenic disturbance and edge effects on anuran assemblages inhabiting cloud forest fragments in Colombia. Natureza and Conservacao 9: 39-46.

da Silva, F.R., Almeida‐Neto, M., do Prado, V.H.M., Haddad, C.F.B. & de Cerqueira Rossa‐Feres, D. 2012. Humidity levels drive reproductive modes and phylogenetic diversity of amphibians in the Brazilian Atlantic Forest. Journal of Biogeography 39(9): 1720-1732.

Eekhout, X. 2010. Sampling amphibians and reptiles. Manual on field recording techniques and protocols for all taxa biodiversity inventories. Belgium: Belgian National Focal Point to The Global Taxonomy Initiative 8: 530-557.

Ehwan, N. 2017. Species composition and richness of amphibians and reptiles along an elevational gradient of Gunung Raya, Langkawi, Kedah, Malaysia. PhD Thesis. Universiti Kebangsaan Malaysia (Unpublished).

Ehwan, N. 2011. Assessment of riparian ecosystem on amphibians along a green corridor in oil palm plantation, Pasoh, Negeri Sembilan, Peninsular Malaysia. MSc Thesis, Universiti Kebangsaan Malaysia (Unpublished).

Faruk, A., Belabut, D., Ahmad, N., Knell, R.J. & Garner, T.W. 2013. Effects of oil‐palm plantations on diversity of tropical anurans. Conservation Biology 27(3): 615-624.

Gillespie, G.R., Howard, S., Stroud, J.T., Ul-Hassanah, A., Campling, M., Lardner, B., Scroggie, M.P. & Kusrini, M. 2015. Responses of tropical forest herpetofauna to moderate anthropogenic disturbance and effects of natural habitat variation in Sulawesi, Indonesia. Biological Conservation 192: 161-173.

Gotelli, N.J. & Colwell, R.K. 2001. Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4(4): 379-391.

Grismer, L.L., Chan, K.O., Grismer, J.L., Wood Jr., P.L. & Norhayati, A. 2010. A checklist of the herpetofauna of the Banjaran Bintang, Peninsular Malaysia. Russian Journal of Herpetology 17(2): 147-160.

Grismer, L.L., Grismer, J.L. & Youmans, T.M. 2004. A new species of Leptolalax (Anura: Megophryidae) from Pulau Tioman, West Malaysia. Asiatic Herpetological Research 10: 8-11.

Hanafiah, A.T. 2011. Potensi Cameron Highlands sebagai destinasi ekopelancongan. hutan pergunungan Cameron Highlands: Pengurusan hutan, persekitaran fizikal, dan kepelbagaian biologi. Jabatan Perhutanan Semenanjung Malaysia 14: 17-22.

Haziq Syahmi, R. 2018. Vegetation association at montane forests in Cameron Highlands, Pahang, Malaysia. Bsc. Thesis. Universiti Putra Malaysia (Unpublished).

Hayes, T.B., Collins, A., Lee, M., Mendoza, M., Noriega, N., Stuart, A.A. & Vonk, A. 2002. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proceedings of the National Academy of Sciences 99(8): 5476-5480.

Hamer, A.J. & McDonnell, M.J. 2008. Amphibian ecology and conservation in the urbanising world: A review. Biological Conservation 141(10): 2432-2449.

Hammer, O., Harper, D.A.T. & Ryan, P.D. 2001. PAST: Paleontological statistics software package for education and data analysis. Paleotologica Electronica 4(1): 9.

Hawkeswood, T.J. & Sommung, B. 2017. A record of Duttaphrynus melanostictus(Schneider, 1799) (Anura: Bufonidae) from Lat Krabang Park, Bangkok, Thailand. Calodema 455: 1-3.

Heyer, W.R., McDiarmid, R.W., Hayek, L.C. & Foster, M.S. 1994. Measuring and Monitoring Biological Diversity-Standard Methods for Amphibians. Washington: Smithsonian Institution Press. p. 384.

Hsieh, H.L. & Li, L.A. 1998. Rarefaction diversity: A case study of Polychaete communities using an amended FORTRAN program. Zoological Studies 37(1): 13-21.

Iangrai, A.J. 2008. Studies on ecology, breeding behaviour, and metamorphosis of tree frogs polypedates leucomystaxand rhacophrous bipunctatus(Anura: Rhacophoridae) in Meghalaya (North-East India). PhD Thesis. Northeastern Hill University (Unpublished).

Ibrahim, J., Nur, H., Nurul, D., Choimmber, T. & Muin, M.A. 2012. Amphibian biodiversity of Gunung Inas Forest Reserve, Kedah, Malaysia. Pertanika Journal of Tropical Agricultural Science 35(2): 249-256.

Inger, R.F., Tan, F.L., Voris, H.K., Vermeulen, J.J., Sheldon, F.H., Diong, C.H. & Stewart, C.M. 2000. Protocols for Conservation Program in Planted Forest Zone (PFZ). Conservation Department, Grand Perfect Sdn. Bhd. Bintulu, Sarawak.

Inger, R.F. & Stuebing, R.S. 2005. A Field Guide to the Frogs of Borneo. 2nd ed. Kota Kinabalu: Natural History Publications (Borneo) Sdn. Bhd. pp. viii + 201.

IUCN. 2019. Microhyla annectens. The IUCN Red List of Threatened Species 2019: e.T57875A91879626. https://www.iucnredlist.org/species/57875/91879626.

Izam, N.A.M., Ahmad, A., Grismer, L.L., Saidin, A.N., Nor, S.M. & Ahmad, N. 2016. Species composition and richness of amphibians in logged forests at Hulu Terengganu, Peninsular Malaysia. AIP Conference Proceedings 1784(1): 060034.

James, F.C. & Rathbun, S. 1981. Rarefaction, relative abundance, and diversity of avian communities. The Auk 98(4): 785-800.

Kumaran, S. & Ainuddin, A.S. 2006. Chapter 1: Forests, water, and climate of Cameron Highlands, Malaysia. In Cameron Highlands-Issues & Challenges in Sustainable Development. Penang: Universiti Sains Malaysia. pp. 1-11.

Lim, K.K.P., Leong, T.M. & Lim, B.L. 2002. Herpetofaunal records from Cameron Highlands, Peninsular Malaysia. Journal of Wildlife and Parks 20(2002): 49-57.

Leong, T.M. & Lim, B.L. 2003. A new species of rana (amphibia: Anura: Ranidae) from the highlands of the Malay Peninsular, with diagnostic larval descriptions. The Raffles Bulletin of Zoology 51(1): 115-122.

Leong, C.P. 2006. Chapter 3: Global warming: Has there been a change in the Climate of Cameron Highlands, Malaysia. In Cameron Highlands-Issues & Challenges in Sustainable Development. Penang: Universiti Sains Malaysia. pp. 26-34.

Loehle, C., Wigley, T.B., Shipman, P.A., Fox, S.F., Rutzmoser, S., Thill, R.E. & Melchiors, M.A. 2005. Herpetofaunal species richness responses to forest landscape structure in Arkansas. Forest Ecology and Management 209(3): 293-308.

Lima, N.G., Oliveira, U., Souza, R.C. & Eterovick, P.C. 2019. Dynamic and diverse amphibian assemblages: Can we differentiate natural processes from human induced changes? PLoS ONE 14(3): 214-316.

Lofts, B., Wellen, J.J. & Benraad, T.S. 1972. Seasonal changes in endocrine organs of the male common frog, Rana temporaria III. The gonads and cholesterol cycle. General and Comparative Endocrinology 18: 344-363.

Malkmus, R., Manthey, U., Vogel, G., Hoffmann, P. & Kosuch, J. 2002. Amphibians & Reptiles of Mount Kinabalu (North Borneo). https://www.researchgate.net/profile/Ulrich_Manthey/publication/256088510_Amphibians_and_Reptiles_of_Mount_Kinabalu_North_Borneo/links/570a2fd308ae8883a1fbba9b/Amphibians-and-Reptiles-of-Mount-Kinabalu-North-Borneo.pdf.

Marsh, D.M. & Pearman, P.B. 1997. Effects of habitat fragmentation on the abundance of two species of Leptodactylid frogs in an Andean montane forest. Conservation Biology 11(6): 1323-1328.

Matsui, M., Belabut, D.M., Ahmad, N. & Yong, H.S. 2009. A new species of Leptolalax (Amphibia, Anura, Megophryidae) from peninsular Malaysia. Zoological Science 26(3): 243-247.

McCann, S., Greenlees, M.J., Newell, D. & Shine, R. 2014. Rapid acclimation to cold allows the cane toad to invade montane areas within its Australian range. Functional Ecology 28(5): 1166-1174.

Muhammad Faris, A.A., Mohammad Nur Firdaus, M., Shamarina, S. & Marina, M.T. 2016. Frog biodiversity in Ayer Hitam Forest Reserve, Puchong, Selangor, Malaysia. Acta Biologica Malaysiana 5(2&3): 53-60.

Nietfeld, M.T., Barrett, M.W. & Silvy, N. 1994. Wildlife marking techniques. In Research and Management Techniques for Wildlife and Habitat, edited by Bookhout, T.A. Bethesda, Maryland: Wildlife Society. pp. 140-168.

Noor Bahiah, S., Marina, M.T., Hani Nabilia, M.S. & Mohd Zafri, H. 2019. Microhabitat preference of frogs at Similajau National Park, Sarawak, Malaysia. International of Scientific and Research Publications 9(4): 2250-3153.

Norhayati, A., Farah, A.D., Chan, K.O., Daicus, B. & Muin, M.A. 2011. An update of herpetofaunal records from Bukit Fraser, Pahang, Peninsular Malaysia. Malaysian Applied Biology 40(2): 9-17.

Norhayati, A., Mohd Amir Syafiq, M.Z., Juliana, S., Daicus, B. & Chan, K.O. 2011. Herpetofaunal records from Cameron Highlands. In Hutan Pergunungan Cameron Highlands: Pengurusan Hutan, Persekitaran Fizikal dan Kepelbagaian Biologi. Jabatan Perhutanan Semenanjung Malaysia. pp. 262-273.

Norhayati, A. 2017. Frogs and Toads of Malaysia: Malaysia Biodiversity Information System (MyBIS). Bangi: Penerbit UKM. p. 101.

Nur Johana, J., Muzzneena, A.M., Grismer, L.L. & Norhayati, A. 2016. Species composition, diversity and relative abundance of amphibians in forests and non-forest habitats on Langkawi Island, Peninsular Malaysia. In AIP Conference Proceedings 1784(1):  060035.

Peh, K.S.H., Soh, M.C., Sodhi, N.S., Laurance, W.F., Ong, D.J. & Clements, R. 2011. Up in the clouds: Is sustainable use of tropical montane cloud forests possible in Malaysia? Bioscience 61(1): 27-38.

Razali, A., Ismail, S.N.S., Awang, S., Praveena, S.M. & Abidin, E.Z. 2018. Land use change in highland area and its impact on river water quality: A review of case studies in Malaysia. Ecological Processes 7(1): 1-17.

Rios-López, N. & Mitchell Aide, T. 2007. Herpetofaunal dynamics during secondary succession. Herpetologica 63(1): 35-50.

Rittenhouse, T.A., Harper, E.B., Rehard, L.R. & Semlitsch, R.D. 2008. The role of microhabitats in the desiccation and survival of anurans in recently harvested oak-hickory forest. Copeia 2008(4): 807-814.

Rosenzweig, M.L. 1995. Species Diversity in Space and Time. Cambridge: Cambridge University Press.

Roznik, E.A., Johnson, S.A., Greenberg, C.H. & Tanner, G.W. 2009. Terrestrial movements and habitat use of gopher frogs in longleaf pine forests: A comparative study of juveniles and adults. Forest Ecology and Management 259(2): 187-194.

Saadati, N., Abdullah, M.P., Zakaria, Z., Rezayi, M. & Hosseinizare, N. 2012. Distribution and fate of HCH isomers and DDT metabolites in a tropical environment - Case study Cameron Highlands - Malaysia. Chemistry Central Journal 6(1): 1-15.

Scott-Manga, J. & Beeuwkes, J. 2005. Vegetation and height preference of juvenile frogs (Hyperolius) in the Amani Pond, Amani Nature Reserve, Tanzania. Herpetofauna 2005: 1-12.

Shahriza, S., Ibrahim, J. & Shahrul Anuar, M.S. 2011. The amphibian fauna of Lata Bukit Hijau, Kedah, Malaysia. Russian Journal of Herpetology 18(3): 221-227.

Simberloff, D. 1978. Use of rarefaction and related methods in ecology. In Biological Data in Water Pollution Assessment: Quantitative and Statistical Analyses. ASTM International.

Snyder, G.K. & Hammerson, G.A. 1993. Interrelationships between water economy and thermo-regulation in the Canyon tree-frog Hyla arenicolor. Journal of Arid Environments 25(3): 321-329.

Society for Ecological Restoration International Science and Policy Working Group. 2004. The SER International Primer on Ecological Restoration.

Sodhi, N.S. & Brook, B.W. 2006. Southeast Asian Biodiversity in Crisis. Cambridge: Cambridge University Press.

Sodhi, N.S., Koh, L.P., Brook, B.W. & Ng, P.K. 2004. Southeast Asian biodiversity: An impending disaster. Trends in Ecology and Evolution 19(12): 654-660.

Sumarli, A.X., Grismer, L.L., Anuar, S., Muin, M.A. & Quah, E.S. 2015. First report on the amphibians and reptiles of a remote mountain, Gunung Tebu in northeastern Peninsular Malaysia. CheckList 11(4): 1-32.

Thorpe, C.J., Lewis, T.R., Kulkarni, S., Watve, A., Gaitonde, N., Pryce, D., Davies, L., Bilton, D.T. & Knight, M.E. 2018. Micro-habitat distribution drives patch quality for sub-tropical rocky plateau amphibians in the northern Western Ghats, India. PLoS ONE 13(3): e0194810.

Tingley, R., Greenlees, M.J. & Shine, R. 2012. Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone. Oikos 121(12): 1959-1965.

Watters, J.L., Cummings, S.T., Flanagan, R.L. & Siler, C.D. 2016. Review of morphometric measurements used in anuran species descriptions and recommendations for a standardized approach. Zootaxa 4072(4): 477-495.

Wilson, R.S. 2001. Geographic variation in thermal sensitivity of jumping performance in the frog Limnodynastes peronii. Journal of Experimental Biology 204(24): 4227-4236.

Yap, C.H. 2015. Diet of five common anurans found in disturbed areas in Northern Peninsular Malaysia. MSc Thesis. Universiti Sains Malaysia (Unpublished).

Zainudin, R., Zain, B.M.M., Ahmad, N. & Nor, S.M. 2017. Microhabitat partitioning of closely related Sarawak (Malaysian Borneo) frog species previously assigned to the genus Hylarana (Amphibia: Anura). Turkish Journal of Zoology 41(5): 876-891.

Zimmerman, B.L. 1994. Audio strip transects. In Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians, edited by Heyer, W.R., Donnelly, M.A., McDiarmid, R.W., Hayek, L.C. & Foster, M.S. Washington, DC: Smithsonian Institution Press. pp. 92-97.

Zweifel, R.G. 1998. Encyclopedia of Reptiles and Amphibians. San Diego: Academic Press. pp. 76-105.

^*Corresponding author; email: marinamohd@upm.edu.my