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Living in small spaces: Forest fragment characterization and its use by Philippine tarsiers (Tarsius syrichta Linnaeus, 1758) in Mindanao Island, Philippines

Abstract

The Philippine tarsier (Tarsius syrichta) is a charismatic species that is threatened by illegal hunting and deforestation. Although they occur in forest and disturbed habitats, ecological information about them is still considerably lacking, which consequently hampers our ability to effectively protect tarsiers from further endangerment. Here, we characterized a 36-ha forest fragment in Mindanao Island where a population of tarsiers persist, and assessed the factors that could have influenced their distribution within the area. We sampled trees (> 1 cm DBH) within 10 × 10-m sampling plots (N = 54), which were established within 1-ha grids (N = 32) and locations where tarsiers were captured (N = 22). The habitat was characterized as a regenerating forest over limestone, with a generally homogeneous structure in terms of tree species richness, abundance, mean DBH, and height. In both sampling plots, we found an abundance of trees below 5 cm in DBH (> 50%) and between 2.6 and 5 m in height (> 40%), which, accordingly, the tarsiers appeared to prefer to use when foraging or sleeping. Lianas were among the most important features of the forest, possibly being a keystone structure in such habitats. Community assemblage, species richness, and mean height of trees, as well as distance to the forest edge, were found to be significant factors that influenced tarsier distribution in the fragment. Our study provides basic yet critical information on the habitat and ecology of Philippine tarsiers in Mindanao, and highlights the importance of forest fragments with rich flora diversity to the survival of the species.

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Fig. 1

Map source: Google Earth Satellite)

Fig. 2

(Map source: Google Earth Satellite). White squares represent 1-ha plot centers, and circles, in general, represent capture plots. Among capture plots, blue circles represent sleeping sites, and yellow circles represent foraging sites

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(Photographs by: Simeon Gabriel F. Bejar)

References

  • Anderson MJ (2014) Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: Statistics Reference Online. https://doi.org/10.1002/9781118445112.stat07841  

  • Arroyo-Rodriguez V, Asensio N, Dunn JC, Cristobal-Azkarate J, Gonzalez-Zamora A (2015) Use of lianas by primates: More than a food source. In: Schnitzer SA, Bongers F, Burnham RJ, Putz FE (eds) Ecology of Lianas. John Wiley and Sons, Ltd, Chichester, pp 407–426

  • Aure B, Escabi-Ruiz CM (2005) Tarsier talk: tarsiers, hunters, and ecotourism in Corella, Bohol. Philippine Q Cult Soc 33:76–99

    Google Scholar 

  • Brown RM, Weghorst JA, Olson KV, Duya MRM, Barley AJ, Duya MV et al (2014) Conservation genetics of the Philippine tarsier: Cryptic genetic variation restructures conservation priorities for an island archipelago primate. PLoS ONE 9:e104340

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Bueno AS, Bruno RS, Pimentel TP, Sanaiotti TM, Magnusson WE (2012) The width of riparian habitats for understory birds in an Amazonian forest. Ecol Appl 22:722–734

    PubMed  Article  Google Scholar 

  • Carandang A, Bugayong LA, Dolom PC, Garcia LN, Villanueva MMB et al (2013) Analysis of key drivers of deforestation and forest degradation in the Philippines. Deutsche Gesellschaft für Internationale Zusammenarbeit (GIZ) GmbH, Manila

  • Corporal-Lodangco IL, Leslie LM (2017) Defining Philippine climate zones using surface and high-resolution satellite data. Procedia Comput Sci 114:324–332

    Article  Google Scholar 

  • Crompton RH, Andau PM (1986) Locomotion and habitat utilization in free-ranging Tarsius bancanus: a preliminary report. Primates 27:337–355

    Article  Google Scholar 

  • Dagosto M, Gebo DL (1997) A preliminary study of the Philippine tarsier in Leyte. Asian Primates 6:4–8

    Google Scholar 

  • Dagosto M, Gebo DL, Dolino C (2001) Positional behavior and social organization of the Philippine tarsier (Tarsius syrichta). Primates 42:233–243

    Article  Google Scholar 

  • Department of Environment and Natural Resources (DENR) (2019) DENR Administrative Order No. 2019–09: Updated National List of Threatened Philippine Fauna and Their Categories. https://www.bmb.gov.ph/index.php/e-library/laws-and-policies/denr-administrative-orders/dao-2017-2019. Accessed 20 Nov 2019

  • Engels B (2015) XNomial: Exact goodness-of-fit for multinomial data with fixed probabilities. R package version 1.0.4

  • Erenso F, Maryo M, Abebe W (2014) Floristic composition, diversity and vegetation structure of woody plant communities in Boda dry evergreen montane forest, West Showa, Ethiopia. Int J Biodivers Conserv 6:382–391

    Article  Google Scholar 

  • Fernando ES, Suh MH, Lee J, Lee DK (2008) Forest Formations of the Philippines. ASEAN-Korea Environmental Cooperation Unit, Seoul

    Google Scholar 

  • Galindon JM, Pasion BO, Tongco MD, Fidelino JM, Duya MR, Ong PS (2018) Plant diversity patterns in remnant forests and exotic tree species-based reforestation in active limestones quarries in the Luzon and Mindanao biogeographic sub-regions in the Philippines. Ecol Res 33:63–72

    CAS  Article  Google Scholar 

  • Gonzalez JCT, Layusa CAA, Afuang LE, Duya MRM, Heaney LR, Balete DS et al (2018) Review and update of the 2004 National List of Threatened Terrestrial Fauna of the Philippines. Sylvatrop 281:73–144

    Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–1

    Article  Google Scholar 

  • Graham MH (2003) Confronting multicollinearity in ecological multiple regression. Ecology 84:2809–2815

    Article  Google Scholar 

  • Grow N, Gursky S, Duma Y (2013) Altitude and forest edges influence the density and distribution of pygmy tarsiers (Tarsius pumilus). Am J Primatol 75:464–477

    PubMed  Article  Google Scholar 

  • Gursky S, Salibay CC, Cuevas CZ (2011) Population survey of the Philippine tarsier (Tarsius syrichta) in Corella, Bohol. Folia Primatol 82:189–196

    PubMed  Article  Google Scholar 

  • Heaney LR (1985) Zoogeographic evidence for Middle and Late Pleistocene land bridges to the Philippine Islands. Mod Quat Res Southeast Asia 9:127–143

    Google Scholar 

  • Heaney LR, Balete DS, Duya MRM, Duya MV, Jansa SA, Steppan SJ, Rickart EA (2016) Doubling diversity: a cautionary tale of previously unsuspected mammalian diversity on a tropical oceanic island. Front Biogeogr 8:e29667

    Article  Google Scholar 

  • Heaney LR, Dolar ML, Balete DS, Esselstyn JA, Rickart EA, Sedlock JL (2010) Synopsis of Philippine mammals. Field Museum of Natural History, Chicago. https://www.fieldmuseum.org/philippine_mammals/. Accessed 20 November 2019

  • Legendre P, Legendre LF (2012) Numerical Ecology, vol 24. Elsevier, Amsterdam

  • Lehman SM, Rajaonson A, Day S (2006) Edge effects and their influence on lemur density and distribution in southeast Madagascar. Am J Phys Anthropol 129:232–241

    PubMed  Article  Google Scholar 

  • Leles B, Xiao X, Pasion BO, Nakamura A, Tomlinson KW (2017) Does plant diversity increase top-down control of herbivorous insects in tropical forest? Oikos. https://doi.org/10.1111/oik.03562

    Article  Google Scholar 

  • Mac Nally R (2000) Regression and model-building in conservation biology, biogeography and ecology: The distinction between – and reconciliation of – ‘predictive’ and ‘explanatory’ models. Biodivers Conserv 9:655–671

    Article  Google Scholar 

  • MacKinnon J, MacKinnon K (1980) The behaviour of wild Spectral tarsiers. Int J Primatol 1:361–379

    Article  Google Scholar 

  • McDonald JH (2009) Handbook of biological statistics, vol 2. Sparky House Publishing, Baltimore

    Google Scholar 

  • Merker S (2010) The population ecology of Dian’s Tarsier. In: Gursky-Doyen S, Supriatna J (eds) Indonesian primates. Springer, New York, pp 371–382

    Chapter  Google Scholar 

  • Merker S, Driller C, Dahruddin H, Wirdateti SW, Perwitasari-Farajallah D, Shekelle M (2010) Tarsius wallacei: A new tarsier species from Central Sulawesi occupies a discontinuous range. Int J Primatol 31:1107–1122

    Article  Google Scholar 

  • Merker S, Yustian I, Mühlenberg M (2005) Responding to forest degradation: Altered habitat use by Dian’s tarsier Tarsius dianae in Sulawesi, Indonesia. Oryx 39:189–195

    Article  Google Scholar 

  • Moritz GL, Melin AD, Tuh Yit YuF, Bernard H, Ong PS, Dominy NJ (2014) Niche convergence suggests functionality of the nocturnal fovea. Front Integr Neurosci 8:1–12

    Article  Google Scholar 

  • Neri-Arboleda I, Stott P, Arboleda NO (2002) Home ranges, spatial movements and habitat associations of the Philippine tarsier (Tarsius syrichta) in Corella, Bohol. J Zool 257:387–402

    Article  Google Scholar 

  • Okuda T, Suzuki M, Adachi N, Quah ES, Hussein NA, Manokaran N (2003) Effect of selective logging on canopy and stand structure and tree species composition in a lowland dipterocarp forest in peninsular Malaysia. Forest Ecol Manag 175:297–320

    Article  Google Scholar 

  • Posa MRC, Diesmos AC, Sodhi NS, Brooks TM (2008) Hope for Threatened Tropical Biodiversity: Lessons from the Philippines. Bioscience 58:231–240

    Article  Google Scholar 

  • Proclamation No. 1030 (1997) Declaring the Philippine Tarsier (Tarsius syrichta) as a Specially Protected Faunal Species of the Philippines. https://www.officialgazette.gov.ph/1997/06/23/proclamation-no-1030-s-1997/. Accessed 20 Nov 2019

  • Purificacion DMP (2019) Home range of the Philippine tarsiers, Carlito (=Tarsius) syrichta (L.), in Initao-Libertad Protected Landscape and Seascape, Misamis Oriental, Philippines: Implications for conservation. Master’s Thesis, University of the Philippines Diliman

  • R Core Team (2006) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/

  • Reason RC (1978) Support use behavior in Mindanao tarsiers (Tarsius syrichta carbonarius). J Mammal 59:205–206

    Article  Google Scholar 

  • Řeháková-Petrů M, Peške L, Daněk T (2012) Predation on a wild Philippine tarsier (Tarsius syrichta). Acta Ethol 15:217–220

    Article  Google Scholar 

  • Ries L, Fletcher RJ Jr, Battin J, Sisk TD (2004) Ecological responses to habitat edges: Mechanisms, models, and variability explained. Annu Rev Ecol Evol Syst 35:491–522

    Article  Google Scholar 

  • Roberts M, Cunningham B (1986) Space and substrate use in captive Western tarsiers, Tarsius bancanus. Int J Primatol 7:113–130

    Article  Google Scholar 

  • Roberts M, Kohn F (1993) Habitat use, foraging behavior, and activity patterns, in reproducing Western tarsiers, Tarsius bancanus, in captivity: A management synthesis. Zoo Biol 12:217–232

    Article  Google Scholar 

  • Rosenberger AL (2010) The skull of Tarsius: Functional morphology, eyeballs, and the nonpursuit predatory lifestyle. Int J Primatol 31:1032–1054

    Article  Google Scholar 

  • Sahimi HNM, Chubo JK, Mohd M, Saripuddin NB, Ab Rahim SS (2018) The Distribution and Population Density of Bornean Tarsier, “Tarsius Bancanus Borneanus (Elliot)” in Secondary and Rehabilitated Forests of Universiti Putra Malaysia, Bintulu Sarawak Campus, Sarawak, Malaysia. Trop Life Sci Res 29:139–154

    PubMed  PubMed Central  Article  Google Scholar 

  • Schmitz J, Noll A, Raabe CA, Churakov G, Voss R, Kiefmann M et al (2016) Genome sequence of the basal haplorrhine primate Tarsius syrichta reveals unusual insertions. Nat Commun 7:12997

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Shekelle M (2008) Distribution and biogeography of tarsiers. In: Shekelle M, Maryanto I, Groves C, Schulze H, Fitch-Snyder H (eds) Primates of the Oriental Night. LIPI Press, Jakarta, pp 13–28

    Google Scholar 

  • Shekelle M, Arboleda I (2008) Tarsius syrichta. The IUCN Red List of Threatened Species 2008 e.T21492A9289252. https://doi.org/10.2305/IUCN.UK.2008.RLTS.T21492A9289252.en.

  • Shekelle M, Salim A (2009) An acute conservation threat to two tarsier species in the Sangihe Island chain, North Sulawesi, Indonesia. Oryx 43:419–426

    Article  Google Scholar 

  • Shekelle M, Gursky S, Merker S, Ong P (2015) Philippine tarsier Carlito syrichta (Linnaeus, 1758). In: Schwitzer C, Mittermeier RA, Rylands AB, Chiozza F, Williamson EA, Macfie EJ, Wallis J, Cotton A (eds) Primates in Peril: The World’s 25 Most Endangered Primates 2014-2016. IUCN SSC Primate Specialist Group (PSG), International Primatological Society (IPS), Conservation International (CI), and Bristol Zoological Society, pp 43–44

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles of statistics in biological research. WH Freeman and Co, New York

    Google Scholar 

  • Straub CS, Simasek NP, Dohm R, Gapinski MR, Aikens EO, Nagy C (2014) Plant diversity increases herbivore movement and vulnerability to predation. Basic Appl Ecol 15:50–58

    Article  Google Scholar 

  • Tews J, Brose U, Grimm V, Tielbörger K, Wichmann MC, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31:79–92

    Article  Google Scholar 

  • Tjur T (2009) Coefficients of determination in logistic regression models – a new proposal: the coefficient of discrimination. Am Stat 63:366–372

    Article  Google Scholar 

  • Villanueva ELC, Buot IE Jr (2015) Threatened Plant Species of Mindoro, Philippines. IAMURE Int J Ecol Conserv 14:168–190

    Google Scholar 

  • Wickham H (2009) ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  • Whitford HN (1911) The Forests of the Philippines: Part 1 Forest types and products. Bureau of Printing, Manila

    Google Scholar 

  • Yustian I (2007) Ecology and conservation status of Tarsius bancanus saltator on Belitung Island, Indonesia. Dissertation, Georg-August-Universitat Göttingen

  • Yustian I, Merker S, Supriatna J, Andayani N (2008) Relative population density of Tarsius dianae in man-influenced habitats of Lore Lindu National Park, Central Sulawesi, Indonesia. Asian Primates J 1:10–16

    Google Scholar 

Download references

Acknowledgements

This paper was part of an undergraduate thesis of SGFB. Funding was provided by Forest Foundation Philippines (formerly Philippine Tropical Forest Conservation Foundation), Holcim Philippines, Inc. (HPI), and Holcim Mining and Development Corporation (HMDC) through the Biodiversity Research Laboratory, Institute of Biology, College of Science, University of the Philippines Diliman and the Diliman Science Research Foundation. Thanks are due to the Department of Environment and Natural Resources Region 10 (DENR R10), the Protected Area Management Board (PAMB), former Protected Area Superintendent (PaSU) Liza Requina, PaSU Eddie Macasusi, and the rest of the staff for the logistic assistance and issuance of permits, and for allowing the authors to conduct the research in the Initao-Libertad Protected Landscape and Seascape under Gratuitous Permit no. R10-2014-36. The authors are grateful to Jaime Mangalindan, Nonito Antoque, Rey Antoque, and Medeva Jay Busaing for their assistance in the field, and to the biologists and research associates of the Biodiversity Research Laboratory, and Dr. Olga M. Nuneza and the volunteer student-researchers from Mindanao State University-Iligan Institute of Technology for their contributions in the data collection.

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The research project and study methods were conceptualized and designed by Perry S. Ong. Funding and managing of the research process were secured by Perry S. Ong, Mariano Roy M. Duya, and Melizar V. Duya. Data collection and fieldworks were conducted by Simeon Gabriel F. Bejar with John Michael M. Galindon. Data analyses were performed by Simeon Gabriel F. Bejar and Bonifacio O. Pasion. All authors were involved in the drafting and finalization of the manuscript.

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Correspondence to Simeon Gabriel F. Bejar.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All animal procedures performed in this research were in accordance with the current laws of the Philippines as promulgated with the ethical standards under the Department of Environment and Natural Resources and the Protected Area Management Board, and approved under Gratuitous Permit no. R10-2014-36.

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Bejar, S.G.F., Duya, M.R.M., Duya, M.V. et al. Living in small spaces: Forest fragment characterization and its use by Philippine tarsiers (Tarsius syrichta Linnaeus, 1758) in Mindanao Island, Philippines. Primates 61, 529–542 (2020). https://doi.org/10.1007/s10329-020-00798-2

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Keywords

  • Forest over limestone
  • Edge effect
  • Habitat use
  • Plant diversity
  • Substrate use
  • Tarsier ecology