Diversity of Amphibians and Reptiles in Various Anthropogenic Disturbance Habitats in Nantu Forest, Sulawesi, Indonesia

Mirza Dikari Kusrini, Luna Raftika Khairunnisa, Aria Nusantara, Agus Priyono Kartono, Lilik Budi Prasetyo, Novi Tri Ayuningrum, Fata Habiburrahman Faz

Abstract

The Nantu Forest in Gorontalo Province, Sulawesi, Indonesia holds one of the few remaining pristine habitats in the island. The reserve is surrounded by human habituation which provide opportunity to study the impact of forest lost on biodversity. In addition, data on Nantu mostly focused on big mammals, as there is no previous herpetofauna survey at the area. Sampling of amphibian and reptile was conducted in June 2013 and in May–June 2014 using Visual Encounter Survey method, glue traps and transect sampling in seven different sites at the eastern part of Nantu. We categorized four habitat types based on human disturbances: high disturbed habitat (HDH), moderate disturbed habitat (MDH), low disturbed habitat (LDH) and pristine habitat (PH). A total of 680 individual amphibians (4 families; 17 species) and 119 individual reptiles (9 families; 29 species) were recorded. Species richness and species composition for amphibians and reptiles differs according to the level of human disturbances. Low level disturbances habitat demonstrated the highest diversity of amphibians and reptiles, whereas as expected, high distubed habitat showed the lowest diversity. Anthropogenic pressures in forest will decrease species richness of amphibian and reptiles. Although most amphibian and reptiles will be able to persist in low disturbances habitat, forest-dependent species will be lost when pristine forests are disturbed.

References

Arini, D. I. D., Shabri, S., Kafiar, Y., Tabba, S., & Kama H. (2011). Keanekaragaman avifauna beberapa kawasan konservasi Propinsi Sulawesi Utara dan Gorontalo. Manado: Balai Penelitian Kehutanan Manado, Badan Penelitian dan Pengembangan Kehutanan, Kementrian Kehutanan
Austin, K. G., Schwantes, A., Gu, Y., & Kasibhatla, P. S. (2019). What causes deforestation in Indonesia? Environmental Research Letters, 14(2), 024007. https://doi.org/10.1088/1748-9326/aaf6db
Bain, R. H., Lathrop, A., Murphy, R. W., Orlov, N. L., & Ho, C. T. (2003). Cryptic species of a cascade frog from Southeast Asia: Taxonomic revisions and descriptions of six new species. American Museum Novitate, 3417, 1–60. https://doi.org/10.1206/0003-0082(2003)417<0001:CSOACF>2.0.CO;2
Bateman, H. L., & Merritt, D. M. (2020). Complex riparian habitats predict reptile and amphibian diversity. Global Ecology and Conservation, 22, e00957. https://doi.org/10.1016/j.gecco.2020.e00957
Bloom, S. (1981). Similarity indices in community studies: Potential pitfalls. Marine Ecology-Progress Series 5, 125–128. https://doi.org/10.3354/meps005125
Bouvet, A., Paillet, Y., Archaux, F., Tillon, L., Denis, P., Gilg, O., & Gosselin, F. (2016). Effects of forest structure, management and landscape on bird and bat communities. Environmental Conservation, 43, 148–160. https://doi.org/10.1017/S0376892915000363
Böhm, M., Collen, B., Baillie, J. E. M., Bowles, P., Chanson, J., Cox, N., …, & Zug, G. (2013). The conservation status of the world’s reptiles. Biological Conservation, 157, 372–385. https://doi.org/10.1016/j.biocon.2012.07.015
Brown, R. M., & Iskandar, D. T. (2000). Nest site selection, larval hatching, and advertisement calls, of Rana arathooni from Southwestern Sulawesi (Celebes) island, Indonesia. Journal of Herpetology, 34, 404–413. https://doi.org/10.2307/1565364
Brown, R. M., Supriatna, J., & Ota, H. (2000): Discovery of a new species of Luperosaurus (Squamata; Gekkonidae) from Sulawesi, with a phylogenetic analysis of the genus, and comments on the status of Luperosaurus serraticaudus. Copeia, 2000(1), 191–209. https://doi.org/10.1643/0045-8511(2000)2000[0191:DOANSO]2.0.CO;2
Chao, A., Colwell, R. K., Lin, C. W., & Gotelli, N. J. (2009). Sufficient sampling for asymptotic minimum species richness estimators. Ecology, 90(4), 1125–1133. https://doi.org/10.1890/07-2147.1
Chape, S., Harrison, J., Spalding, M., & Lysenko, I. (2005). Measuring the extent and effectiveness of protected areas as an indicator for meeting global biodiversity targets. Philosophical Transactions of the Royal Society B, 360(1454), 443–455. https://doi.org/10.1098/rstb.2004.1592
Che, J., Hu, J. S., Zhou, W., Murphy, R. W., Papenfuss, T. J., Chen, M., ..., & Zhang, Y. (2009). Phylogeny of the Asian spiny frog tribe Paini (Family Dicroglossidae) sensu Dubois. Molecular Phylogenetics and Evolution, 50, 59–73. https://doi.org/10.1016/j.ympev.2008.10.007
Church, G. (1960). The invasion of Bali by Bufo melanostictus. Herpetologica, 16, 15–21. https://doi.org/10.1016/j.ympev.2006.11.032
Clayton, L. M. (1996). Conservation biology of the babirusa in North Sulawesi, Indonesia [dissertation]. Oxford: University of Oxford.
Clayton, L., Keeling, M., & Milner-Gulland, E. J. (1997). Bringing home the bacon: A spatial model of wild pig hunting in Sulawesi, Indonesia. Ecological Applications, 7(2), 642–652. https://doi.org/10.2307/2269527
Clayton, L. M., & Macdonald, D. W. (1999). Social organization of the babirusa (Babyrousa babyrussa) and their use of salt licks in Sulawesi, Indonesia. Journal of Mammalogy, 80, 1147–1157. https://doi.org/10.2307/1383165
Clayton, L. M., & Milner-Gulland, E. J. (1999). The trade in wildlife in North Sulawesi Indonesia. Pages 473–496 In J. G. Robinson, & E. L. Bennett (Eds.), Hunting for Sustainability in Tropical Forests. New York: Columbia University Press.
Clayton, L. M., Milner-Gulland, E. J., Sinaga, D. W., & Mustari, A. H. (2000). Effects of a proposed ex situ conservation program on in situ conservation of the babirusa, an endangered suid. Conservation Biology, 14(2), 382–385. https://doi.org/10.1046/j.1523-1739.2000.99123.x
Cortes, A. M., Ruiz-Agudelo, C. A., Valencia-Aguilar, A., & Ladle, R. J. (2014). Ecological functions of Neotropical amphibians and reptiles: A review. Universitas Scientiarum, 20(2), 229. https://doi.org/10.11144/Javeriana.SC20-2.efna
Curran, L. M., Trigg, S. N., McDonald, A. K., Astiani, D., Hardiono, Y. M., Siregar, P., …., & Kasischke, E. (2004). Lowland forest loss in protected areas of Indonesian Borneo. Science, 303(5660), 1000–1003. https://doi.org/10.1126/science.1091714
de Lang, R., & Vogel, G. (2006). The snakes of Sulawesi. In J. K. M. Vences, T. Ziegler, & W. Böhme (Eds.), Herpetologia Bonnensis II. Proceedings of the 13th Congress of the Societas Europaea Herpetologica. Bonn: Societas Europaea Herpetologica.
de Miranda, E. B. P. (2017). The plight of reptiles as ecological actors in the tropics. Frontiers in Ecology and Evolution, 5(159). https://doi.org/10.3389/fevo.2017.00159
DeWalt, S. J., Maliakal, S. K., & Denslow, J. S. (2003): Changes in vegetation structure and composition along a tropical forest chronosequence: implications for wildlife. Forest Ecology and Management, 182, 139–151. https://doi.org/10.1016/S0378-1127(03)00029-X
Frost, D. R. (2018). Amphibian species of the world: An online reference version 6.0. Retrieved from http://research.amnh.org/herpetology/amphibia/index.html.
Gaveau, D. L. A., Curran, L. M., Paoli, G. D., Carlson, K. M., Wells, P., Besse-Rimba, A., …, & Leader-Williams, N. (2012). Examining protected area effectiveness in Sumatra: Importance of regulations governing unprotected lands: Evaluating protected area effectiveness. Conservation Letters 5(2), 142–148. https://doi.org/10.1111/j.1755-263X.2011.00220.x
Gaveau, D. L. A., Wandono, H., & Setiabudi, F. (2007). Three decades of deforestation in southwest Sumatra: Have protected areas halted forest loss and logging, and promoted re-growth? Biological Conservation, 134(4), 495–504.
Gillespie, G. R., Howard, S., Stroud, J. T., Ul-Hassanah, A., Campling, M., Lardner, B., ..., & 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. https://doi.org/10.1016/j.biocon.2006.08.035
Gillespie, G., Howard, S., Lockie, D., Scroggie, M., & Boeadi. (2005). Herpetofaunal richness and community structure of offshore islands of Sulawesi, Indonesia. Biotropica, 37(2), 279–290. https://doi.org/10.1111/j.1744-7429.2005.00038.x.
Gulson-Castillo, E. R., Pegan, T. M., & Winarni, N. L. (2018). Sulawesi endemic in the spotlight: First images and sound recordings of the Snoring Rail. BirdingASIA, 30, 60–64.
Hammer, Ø. (2018). PAST PAleontological STatistics version 3.21. Reference manual. Oslo: Natural History Museum University of Oslo.
Hayden, C. J., Brown, R. M., Gillespie, G., Setiadi, M. I, Linkem, C. W., Iskandar, D. T., ..., & McGuire, J. A. (2008). A new species of bent-toed gecko Cyrtodactylus gray, 1827, (Squamata: Gekkonidae) from the island of Sulawesi, Indonesia. Herpetologica, 64(1), 109–120. https://doi.org/10.1655/07-026.1
Heyer, W. R., Donnely, M. A., McDiarmid, R. W., Hayek, L. C., & Foster, M. S. (1994). Measuring and monitoring biological diversity: Standard methods for amphibians (M. S. Foster, Ed.). Washington: Smithsonian Institution Press.
Hocking, D. J., & Babbitt, K. J. (2014). Amphibian contributions to ecosystem services. Herpetological Conservation and Biology, 9(1), 1–17.
Howard, S. D., & Gillespie, G. R. (2007). Two new Calamaria (Serpentes) species from Sulawesi, Indonesia. Journal of Herpetology, 41(2), 237–242. https://doi.org/10.1670/0022-1511(2007)41[237:TNCSSF]2.0.CO;2
Howard, S. D., Gillespie, G. R., Riyanto, A., & Iskandar, D. T. (2007). A new species of Large eutropis (Scincidae) from Sulawesi, Indonesia. Journal of Herpetology, 41(4), 604–610. https://doi.org/10.1670/233-05.1
Huston, M. (1979). A general hypothesis of species diversity. American Naturalist, 113, 81–101. https://doi.org/10.1086/283366
Huston, M. A. (1994). Biological diversity: The coexistence of species on changing landscapes. Cambridge: Cambridge University Press.
Iskandar, D. T. (1998). Amfibi Jawa dan Bali. Bogor: Puslitbang Biologi-LIPI.
Iskandar, D. T., Arifin, U., & Rachmansah, A. (2011a). A new frog (Anura, Dicroglossidae), related to Occidozyga semipalmata Smith, 1927 from the eastern peninsula of Sulawesi, Indonesia. Raffles Bulletin of Zoology, 59(2), 219–228.
Iskandar, D. T., Rachmansah, A., & Umilaela. (2011b). A new bent-toed gecko of the genus Cyrtodactylus Gray, 1827 (Reptilia, Gekkonidae) from Mount Tompotika, eastern peninsula of Sulawesi, Indonesia. Zootaxa, 2838, 65–78. https://doi.org/10.11646/zootaxa.2838.1.4
Iskandar, D. T., & Erdelen, W. R. (2006). Conservation of amphibians and reptiles in Indonesia: Issues and problems. Amphibian and Reptile Conservation, 4(1), 60–93. https://doi.org/10.1514/journal.arc.0040016
Iskandar, D. T., Evans, B. J., & McGuire, J. A. (2014). A novel reproductive mode in frogs: A new species of fanged frog with internal fertilization and birth of tadpoles. PLoS One, 9(12), e115884. https://doi.org/10.1371/journal.pone.0115884
Iskandar, D. T., &Tjan, K. N. (1996). The amphibians and reptiles of Sulawesi, with notes on the distribution and chromosomal number of frogs. In D. J. Kitchener, & A. Suyanto (Eds.), Proceedings of the First International Conference on Eastern Indonesian-Australian Vertebrate Fauna. (pp. 39–46). Manado, Indonesia.
[IUCN] International Union for Conservation of Nature. (2020). IUCN red list of threatened species. Version 2020-1. Retrieved from http://www.iucnredlist.org.
Koch, A. (2008). Discovery of new specimens of Sarasin’s Keelback, Amphiesma sarasinorum (Boulenger, 1896), endemic to SW Sulawesi, Indonesia. Herpetozoa, 20(3/4), 178–182.
Koch, A. (2011). The amphibians and reptiles of Sulawesi: Underestimated diversity in a dynamic environment. In F. E. Zachos, & J. H. Habel (Eds.), Biodiversity Hotspots (pp. 383–404). Springer.
Kuch, U., Gumprecht, A., & Melaun, C. (2007). A new species of Temple pitviper (Tropidolaemus Wagler, 1830) from Sulawesi, Indonesia (Squamata: Viperidae: Crotalinae). Zootaxa, 1446, 1–20. https://doi.org/10.5281/zenodo.176141
Kusrini, M. D., Rowley, J. J. L., Khairunnisa, L. R., Shea, G. M., & Altig, R. (2015). The reproductive biology and larvae of the first tadpole-bearing frog, Limnonectes larvaepartus. PLoS ONE, 10(1), e116154. https://doi.org/10.1371/journal.pone.0116154
Lassau, S. A., Hochuli, D. F., Cassis, G., & Reid, C. A. M. (2005). Effects of habitat complexity on forest beetle diversity: Do functional groups respond consistently? Habitat complexity and beetle diversity. Diversity and Distributions, 11(1), 73–82. https://doi.org/10.1111/j.1366-9516.2005.00124.x
Linkem, C. W., Mcguire, J. A., Hayden, C. J., Setiadi, M. I., Bickford, D. P., & Brown, R. M. (2008). A new species of bent-toe gecko (gekkonidae:cyrtodactylus) from Sulawesi island, eastern Indonesia. Herpetologica, 64, 224–234. https://doi.org/10.1655/07-040.1
Magurran, A. E. (2010). Measuring biological diversity. Malden: Blackwell Pub.
Margono, B. A., Potapov, P. V., Turubanova, S., Stolle, F., & Hansen, M. C. (2014). Primary forest cover loss in Indonesia over 2000–2012. Nature Climate Change, 4(8), 730–735. https://doi.org/10.1038/nclimate2277
McDiarmid, R. W., Foster, M. S., Guyer, C., Gibbons, J. W., & Chernoff, N. (Eds.). (2012). Reptile biodiversity: Standard methods for inventory and monitoring. California: University of California Press.
Moy, M. S., Mardiastuti, A., & Kahono, S. (2016). Response of Dung Beetle communities (Coleoptera: Scarabaeidae) across gradient of disturbance in the tropical low-land forest of Buton, Sulawesi. Zoo Indonesia, 25(1), 58–70.
Muñoz, J. (2007). Biodiversity conservation including uncharismatic species. Biodiversity Conservation, 16, 2233–2235. https//doi.org/10.1007/s10531-006-9147-1
Prabowo, W. E., Darras, K., Clough, Y., Toledo-Hernandez, M., Arlettaz, R., Mulyani, Y. A., & Tscharntke, T. (2016). Bird responses to lowland rainforest conversion in Sumatran smallholder landscapes, Indonesia. PLOS ONE, 11, e0154876. https://doi.org/10.1371/journal.pone.0154876
Robertson, J. M. Y., & Schaik, C. P. van. (2001). Causal factors underlying the dramatic decline of the Sumatran orang-utan. Oryx, 35(1), 26–38. https://doi.org/10.1046/j.1365-3008.2001.00149.x
Riyanto, A., Kurniati, H., & Engilis, Jr. A. (2016). A new bent-toed gecko (Squamata: Gekkonidae) from the Mekongga Mountains, South East Sulawesi, Indonesia. Zootaxa, 4109(1), 59. https://doi.org/10.11646/zootaxa.4109.1.5
Rowley, J., Brown, R., Bain, R., Kusrini, M., Inger, R., Stuart, B., ..., & Phimmachak, S. (2009). Impending conservation crisis for Southeast Asian amphibians. Biological Letters, 6(3), 336–338. https://doi.org/10.1098/rsbl.2009.0793
Semiadi, G., & Meijaard, E. (2006). Declining populations of the javan warty pig (Sus verrucosus). Oryx, 40(1), 1–7. https://doi.org/10.1017/S003060530600007X
Setiadi, M. I., McGuire, J. A., Brown, R. M., Zubairi, M., Iskandar, D. T., Andayani, N., ..., & Evans, B. J. (2011). Adaptive radiation and ecological opportunity in Sulawesi and Philippine fanged frog (Limnonectes) communities. The American Naturalist, 178(2), 221–240. https://doi.org/10.1086/660830
Shah, P., & Baylis, K. (2015). Evaluating heterogeneous conservation effects of forest protection in Indonesia. PLoS ONE, 10(6), e0124872. https://doi.org/10.1371/journal.pone.0124872
Smith, O., Wang, J., & Carbone, C. (2018). Evaluating the effect of forest loss and agricultural expansion on sumatran tigers from scat surveys. Biological Conservation, 221, 270–278. https://doi.org/10.1016/j.biocon.2018.03.014
Sodhi, N. S., Posa, M. R. C., Lee, T. M., Bickford, D., Koh, L. P., & Brook, B. W. (2010). The state and conservation of Southeast Asian biodiversity. Biodiversity Conservation, 19, 317–328. https://doi.org/10.1016/j.tree.2005.05.013
Stuart, B. L., Inger, R. F., & Voris, H. K. (2006). High level of cryptic species diversity revealed by sympatric lineages of Southeast Asian forest frogs. Biology Letters, 2, 470–474. https://doi.org/10.1098/rsbl.2006.0505.
Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S. L., Fischman, D. L., & Waller, R. W. (2005). Status and trends of amphibian declines and extinctions worldwide. Science, 306, 1783–1786. https://doi.org/10.1126/science.1103538
Supriatna, J., Shekelle, M., Fuad, H. A. H., Winarni, N. L., Dwiyahreni, A. A., Farid, M., ...., & Zakaria, Z. (2020). Deforestation on the Indonesian island of Sulawesi and the loss of primate habitat. Global Ecology and Conservation, 24, e01205. https://doi.org/10.1016/j.gecco.2020.e01205
Susanto, E., Lestari, N., & Hapsari, M. (2018). Driving factors of deforestation in Indonesia: A case of Central Kalimantan. Jurnal Studi Pemerintahan, 9(4), 23. https://doi.org/10.18196/jgp.2018.9390
Uetz, P., & Hosek, J. (Eds.). (2014). The reptile database. Retrived from http://www.reptile-database.org.
Valencia-Aguilar, A., Cortés-Gómez, A. M., & Ruiz-Agudelo, C. A. (2013). Ecosystem services provided by amphibians and reptiles in Neotropical ecosystems. International Journal of Biodiversity Science, Ecosystem Services & Management, 9(3), 257–272. https://doi.org/10.1080/21513732.2013.821168
Waltert, M., Mardiastuti, A., & Mühlenberg, M. (2005). Effects of deforestation and forest modification on understorey birds in Central Sulawesi, Indonesia. Bird Conservation International, 15(3), 257–273. https://doi.org/10.1017/S0959270905000432
Wanger, T. C., Iskandar, D. T., Motzke, I., Brook, B. W., Sodhi, N. S., Clough, Y., & Tscharntke, T. (2010). Effects of land-use change on community composition of tropical amphibians and reptiles in Sulawesi, Indonesia. Conservation Biology, 24(3), 795–802. https://doi.org/10.1111/j.1523-1739.2009.01434.x
Wanger, T. C., Motzke, I., Saleh, S., & Iskandar, D. T. (2011). The amphibians and reptiles of the Lore Lindu National Park area, Central Sulawesi, Indonesia. Salamandra, 47(1), 17–29.
Whitten, A. J., Mustafa, M., & Henderson, G. S. (1987). The ecology of Sulawesi. Yogyakarta: Gadjah Mada University Press.
Williams, S. E., Marsh, H., & Winter, J. (2002). Spatial scale, species diversity, and habitat structure: small mammals in Australian tropical rain forest. Ecology, 83, 1317–1329. https://doi.org/10.2307/3071946

Authors

Mirza Dikari Kusrini
mirza_kusrini@yahoo.com (Primary Contact)
Luna Raftika Khairunnisa
Aria Nusantara
Agus Priyono Kartono
Lilik Budi Prasetyo
Novi Tri Ayuningrum
Fata Habiburrahman Faz
Author Biography

Mirza Dikari Kusrini, Faculty of Forestry, Bogor Agricultural University

Lecturer at Department of Forest Resourcesw Conservation & Ecotourism.
KusriniM. D., KhairunnisaL. R., NusantaraA., KartonoA. P., PrasetyoL. B., AyuningrumN. T., & FazF. H. (2020). Diversity of Amphibians and Reptiles in Various Anthropogenic Disturbance Habitats in Nantu Forest, Sulawesi, Indonesia. Jurnal Manajemen Hutan Tropika, 26(3), 291. https://doi.org/10.7226/jtfm.26.3.291

Article Details

Expedition and Characterization of the Corpse Flower (Amorphophallus titanum (Becc.)) in West Sumatra

Yusniwati, Ryan Budi Setiawan, Mellyyana Handayani, Alifma Rahimmi Nanda, Dian Sukma, Alfazlul...
Abstract View : 165
Download :134

Assessment of Natural Resources and Local Community Participationin Nature-Based Tourism of Wehea Forest, East Kalimantan

Muli Edwin, Iin Sumbada Sulistyorini, Jerlita Kadang Allo
Abstract View : 1620
Download :1070