Modelling Niche Differentiation of Co-Existing, Elusive and Morphologically Similar Species: A Case Study of Four Macaque Species in Nakai-Nam Theun National Protected Area, Laos
Species misidentification often occurs when dealing with co-existing and morphologically similar species such as macaques, making the study of their ecology challenging. To overcome this issue, we use reliable occurrence data from camera-trap images and transect survey data to model their respective ecological niche and potential distribution locally in Nakai-Nam Theun National Protected Area (NNT NPA), central-Eastern Laos. We investigate niche differentiation of morphologically similar species using four sympatric macaque species in NNT NPA, as our model species: rhesus Macaca mulatta (Taxonomic Serial Number, TSN 180099), Northern pig-tailed M. leonina (TSN not listed); Assamese M. assamensis (TSN 573018) and stump-tailed M. arctoides (TSN 573017). We examine the implications for their conservation. We obtained occurrence data of macaque species from systematic 2006–2011 camera-trapping surveys and 2011–2012 transect surveys and model their niche and potential distribution with MaxEnt software using 25 environmental and topographic variables. The respective suitable habitat predicted for each species reveals niche segregation between the four species with a gradual geographical distribution following an environmental gradient within the study area. Camera-trapping positioned at many locations can increase elusive-species records with a relatively reduced and more systematic sampling effort and provide reliable species occurrence data. These can be used for environmental niche modelling to study niche segregation of morphologically similar species in areas where their distribution remains uncertain. Examining unresolved species' niches and potential distributions can have crucial implications for future research and species' management and conservation even in the most remote regions and for the least-known species.
References
[1]
Bojórquez-Tapia, L.A.; Azuara, I.; Ezcurra, E.; Flores-Villela, O. Identifying conservation priorities in Mexico through geographic information systems and modeling. Ecol. Appl. 1995, 5, 215–231, doi:10.2307/1942065.
[2]
Raxworthy, C.J.; Ingram, C.M.; Rabibisoa, N.; Pearson, R.G. Applications of ecological niche modeling for species delimitation: A review and empirical evaluation using day geckos (Phelsuma) from Madagascar. Syst. Biol. 2007, 56, 907–923, doi:10.1080/10635150701775111.
[3]
Buermann, W.; Saatchi, S.; Smith, T.B.; Zutta, B.R.; Chaves, J.A.; Milá, B.; Graham, C.H. Predicting species distributions across the Amazonian and Andean regions using remote sensing data. J. Biogeogr. 2008, 35, 1160–1176, doi:10.1111/j.1365-2699.2007.01858.x.
[4]
Parolo, G.; Rossi, G.; Ferrarini, A. Toward improved species niche modelling: Arnica montana in the Alps as a case study. J. Appl. Ecol. 2008, 45, 1410–1418, doi:10.1111/j.1365-2664.2008.01516.x.
[5]
Martínez-Freiría, F.; Sillero, N.; Lizana, M.; Brito, J.C. GIS-based niche models identify environmental correlates sustaining a contact zone between three species of European vipers. Divers. Distrib. 2008, 14, 452–461, doi:10.1111/j.1472-4642.2007.00446.x.
[6]
Pineda, E.; Lobo, J.M. Assessing the accuracy of species distribution models to predict amphibian species richness patterns. J. Appl. Ecol. 2009, 78, 182–190, doi:10.1111/j.1365-2656.2008.01471.x.
[7]
Timmins, R.J.; Evans, T.D.; Khounboline, K.; Sisomphone, C. Status and conservation of the giant muntjac Megamuntiacus vuquangensis, and notes on other muntjac species in Laos. Oryx 1998, 32, 59–67.
[8]
Duckworth, J.W.; Stones, T.; Tizard, R.; Watson, S.; Wolstencroft, J. Does the fishing cat inhabit Laos? Cat News 2010, 52, 4–7.
[9]
Timmins, R.J.; Duckworth, J.W. Distribution and habitat of Assamese Macaque Macaca assamensis in Lao PDR, including its use of low altitude karsts. Primate Conserv. 2011, 26, 1–12.
[10]
Duckworth, J.W.; Poole, C.M.; Tizard, R.J.; Walston, J.L.; Timmins, R.J. The jungle cat Felis chaus in Indochina: A threatened population of a widespread and adaptable species. Biodivers. Conserv. 2005, 14, 1263–1280, doi:10.1007/s10531-004-1653-4.
[11]
Tobler, M.W.; Carrillo-Percastegui, S.E.; Leite Pitman, R.; Mares, R.; Powell, G. An evaluation of camera traps for inventorying large- and medium-sized terrestrial rainforest mammals. Anim. Conserv. 2008, 11, 169–178, doi:10.1111/j.1469-1795.2008.00169.x.
Di Bitetti, M.S.; De Angelo, C.D.; Di Blanco, Y.E.; Paviolo, A. Niche partitioning and species coexistence in a Neotropical felid assemblage. Acta Oecol. 2010, 36, 403–412, doi:10.1016/j.actao.2010.04.001.
[14]
Pereira, P.; da Silva, A.A.; Alves, J.; Matos, M.; Fonseca, C. Coexistence of carnivores in a heterogeneous landscape: Habitat selection and ecological niches. Ecol. Res. 2012, 27, 745–753, doi:10.1007/s11284-012-0949-1.
[15]
Jenks, K.E.; Kitamura, S.; Lynam, A.J.; Ngoprasert, D.; Chutipong, W.; Steinmetz, R.; Sukmasuang, R.; Grassman, L.I.; Cutter, P.; Tantipisanuh, N.; Bhumpakphan, N.; Gale, G.A.; Reed, D.H.; Leimgruber, P.; Songsasen, N. Mapping the distribution of dholes, Cuon alpinus (Canidae, Carnivora), in Thailand. Mammalia 2012, 76, 1–10, doi:10.1515/mammalia-2011-0108.
[16]
Timmins, R.J.; Evans, T.D. Wildlife and Habitat Survey of the Nakai-Nam Theun National Biodiversity Conservation Area; Wildlife Conservation Society: Vientiane, Lao PDR, 1996.
[17]
Fooden, J. Ecogeographic segregation of macaque species. Primates 1982, 23, 574–579, doi:10.1007/BF02373969.
[18]
Robichaud, W.; Sinclair, A.; Odarkor-Lanquaye, N.; Klinkenberg, B. Stable forest cover under increasing populations of swidden cultivators in central Laos: The roles of intrinsic culture and extrinsic wildlife trade. Ecol. Soc. 2009, 14, 33–60.
[19]
Hijmans, R.J.; Cameron, S.E.; Parra, J.L.; Jones, P.G.; Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 2005, 25, 1965–1978, doi:10.1002/joc.1276.
[20]
Johnson, A.; Johnston, J. Biodiversity Monitoring and enforcement project in the Nam Theun 2 watershed (including the Nakai-Nam Theun NPA and corridors linking to the Phou Hin Poun and Hin Nam Nor PA); Wildlife Conservation Society: Vientiane, Lao PDR, 2007.
Coudrat, C.N.Z. Wildlife Surveys in Nakai-Nam Theun National Protected Area 2011-2012 (Final Report). NT2-WMPA, Ban Oudomsouk: Nakai District, Lao PDR, 2012. Unpublished work.
[23]
Thierry, B. The macaques. In Primates in Perspective, 2nd; Campbell, C., Fuentes, A., MacKinnon, K., Bearder, S., Stumpf, R., Eds.; Oxford University Press: New York, NY, USA, 2010; pp. 229–241.
[24]
Phillips, S.J.; Dudík, M.; Schapire, R.E. A maximum entropy approach to species distribution modeling. In Proceedings of the Twenty-First International Conference on Machine Learning, Banff, AB, Canada, 4–8 July 2004; pp. 655–662.
[25]
Phillips, S.J.; Anderson, R.P.; Schapire, R.E. Maximum entropy modeling of species geographic distributions. Ecol. Model. 2006, 190, 231–259, doi:10.1016/j.ecolmodel.2005.03.026.
Kohavi, R. A study of cross-validation and bootstrap for accuracy estimation and model selection. In Proceedings of the Fourteenth International Joint Conference on Artificial Intelligence, Montréal, QC, Canada, 20–25 August 1995; pp. 1137–1143.
[28]
Phillips, S.J.; Dudik, M. Modeling of species distributions with Maxent: New extensions and a comprehensive evaluation. Ecogeography 2008, 31, 161–175, doi:10.1111/j.0906-7590.2008.5203.x.
[29]
Raes, N.; Steege, H. A null-model for significance testing of presence-only species distribution models. Ecography 2007, 30, 727–736, doi:10.1111/j.2007.0906-7590.05041.x.
Pearson, R.G.; Raxworthy, C.J.; Nakamura, M.; Townsend Peterson, A. Predicting species distributions from small numbers of occurrence records: A test case using cryptic geckos in Madagascar. J. Biogeogr. 2007, 34, 102–117.
[32]
Yost, A.C., Petersen; Miller, R. Predictive modeling and mapping sage grouse (Centrocercus urophasianus) nesting habitat using Maximum Entropy and a long-term dataset from Southern Oregon. Ecol. Inform. 2008, 3, 375–386.
[33]
Hirzel, A.H.; Le Lay, G.; Helfer, V.; Randin, C.; Guisan, A. Evaluating the ability of habitat suitability models to predict species presences. Ecol. Model. 2006, 199, 142–152, doi:10.1016/j.ecolmodel.2006.05.017.
[34]
Hernandez, P.A.; Graham, C.H.; Master, L.L.; Albert, D.L. The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecogeography 2006, 29, 773–785, doi:10.1111/j.0906-7590.2006.04700.x.
[35]
Schoener, T.W. Anolis lizards of Bimini: Resource partitioning in a complex fauna. Ecology 1968, 49, 704–726, doi:10.2307/1935534.
[36]
Warren, D.L.; Glor, R.E.; Turelli, M. Environmental niche equivalency versus conservatism: Quantitative approaches to niche evolution. Evolution 2008, 62, 2868–2883, doi:10.1111/j.1558-5646.2008.00482.x.
[37]
Duckworth, J.; Salter, R.E.; Khounboline, K. Wildlife in Lao PDR 1999 Status Report; IUCN–The World Conservation Union, Wildlife Conservation Society, Centre for Protected Areas and Watershed Management: Vientiane, Lao PDR, 1999.
[38]
Abegg, C.; Thierry, B. Macaque evolution and dispersal in insular south-east Asia. Biol. J. Linn. Soc. 2002, 75, 555–576, doi:10.1046/j.1095-8312.2002.00045.x.
[39]
Eudey, A.A. Pleistocene glacial phenomena and the evolution of Asian macaques. In The Macaques: Studies in Ecology, Behavior and Evolution; Lindburg, D.G., Ed.; Van Nostrand Reinhold: New York, NY, USA, 1980; pp. 52–83.
[40]
Eudey, A.A. Macaques habitat preference in west-central Thailand and quaternary glacial events. In Primatology Today; Ehara, A., Kimura, T., Takenaka, O., Iwamoto, M., Eds.; Elsevier Science Publishers: Amsterdam, The Netherlands, 1991; pp. 21–24.
[41]
Rodman, P.S. Structural Differentiation of microhabitats of sympatric Macaca fascicularis and M. nemestrina in East Kalimantan, Indonesia. Int. J. Primatol. 1991, 12, 357–375.
[42]
Borries, C.; Larney, K.; Kreetiyutanony, K.; Koenig, A. The diurnal primate community in a dry evergreen forest in Phu Khieo Wildlife Sanctuary, Northeast Thailand. Nat. Hist. Bull. Siam Soc. 2002, 50, 75–88.
[43]
IUCN Red List v.2011. Available online: http://www.iucnredlist.org (accessed on 16 August 2012).
[44]
Wintle, B.A.; Elith, J.; Potts, J.M. Fauna habitat modelling and mapping: A review and case study in the Lower Hunter Central Coast region of NSW. Austral. Ecol. 2005, 30, 719–738, doi:10.1111/j.1442-9993.2005.01514.x.
[45]
Phillips, S.J.; Dudík, M.; Elith, J.; Graham, C.H.; Lehmann, A.; Leathwick, J.; Ferrier, S. Sample selection bias and presence-only distribution models: Implications for background and pseudo-absence data. Ecol. Appl. 2009, 19, 181–197, doi:10.1890/07-2153.1.
[46]
Blanco, G.; Sergio, F.; Sanchéz-Zapata, J.A.; Pérez-García, J.M.; Botella, F.; Martínez, F.; Zuberogoitia, I.; Frías, O.; Roviralta, F.; Martínez, J.E.; Hiraldo, F. Safety in numbers? Supplanting data quality with fanciful models in wildlife monitoring and conservation. Biodivers. Conserv. 2012, 21, 3269–3276, doi:10.1007/s10531-012-0344-9.
[47]
Thorn, J.S.; Nijman, V.; Smith, D.; Nekaris, K.A.I. Ecological niche modelling as a technique for assessing threats and setting conservation priorities for Asian slow lorises (Primates: Nycticebus). Divers. Distrib. 2009, 15, 289–298, doi:10.1111/j.1472-4642.2008.00535.x.
[48]
Chunco, A.J.; Jobe, T.; Pfennig, K.S. Why do species co-occur? A test of alternative hypotheses describing abiotic differences in sympatry versus allopatry using spadefoot toads. PLoS ONE 2012, 7, e32748.
[49]
Wisz, M.S.; Hijmans, R.; Li, J.; Peterson, A.T.; Graham, C.H.; Guisan, A.; The Nceas Predicting Species Distributions Working Group. Effects of sample size on the performance of species distribution models. Divers. Distrib. 2008, 14, 763–773, doi:10.1111/j.1472-4642.2008.00482.x.
[50]
Graham, C.H.; Elith, J.; Hijmans, R.J.; Guisan, A.; Townsend-Peterson, A.; Loiselle, B.A.; The Nceas Predicting Species Distributions Working Group. The influence of spatial errors in species occurrence data used in distribution models. J. Appl. Ecol. 2008, 45, 239–247.
[51]
Warren, D.; Steifert, S. Ecological niche modeling in Maxent: The importance of model complexity and the performance of model selection criteria. Ecol. Appl. 2011, 21, 335–342, doi:10.1890/10-1171.1.
[52]
McPherson, J.M.; Jetz, W. Effects of species? Ecology on the accuracy of distribution models. Ecography 2007, 30, 135–151.
[53]
Hardcastle, J.; Cox, S.; Dao, N.T.; Johns, A.G. Rediscovering the Saola. In Proceedings of the Rediscovering the Saola—A Status Review and Conservation Planning Workshop, Hanoi, Vietnam, 27–28 February 2004.
McCarthy, J.L.; Fuller, T.K.; McCarthy, K.P.; Wibisono, H.T.; Livolsi, M.C. Using camera trap photos and direct sightings to identify possible refugia for the Vulnerable Sumatran striped rabbit Nesolagus netscheri. Oryx 2012, 46, 438–441, doi:10.1017/S0030605312000051.
[56]
Johnson, A.; Vongkhamheng, C.; Hedemark, M.; Saithongdam, T. Effects of human carnivore conflict on tiger (Panthera tigris) and prey populations in Lao PDR. Anim. Conserv. 2006, 9, 421–430, doi:10.1111/j.1469-1795.2006.00049.x.
[57]
Mohamed, A.; Samejima, H.; Wilting, A. Records of five Bornean cat species from Deramakot Forest Reserve in Sabah, Malaysia. Cat News 2009, 51, 3–6.
[58]
Wilting, A.; Mohamed, A.; Ambu, L.N.; Lagan, P.; Mannan, S.; Hofer, H.; Sollmann, R. Density of the Vulnerable Sunda clouded leopard Neofelis diardi in two commercial forest reserves in Sabah, Malaysian Borneo. Oryx 2012, 46, 423–426, doi:10.1017/S0030605311001694.
Duckworth, J.W.; Batters, G.; Belant, J.L.; Bennett, E.L.; Brunner, J.; Burton, J.; Challender, D.W.S.; Cowling, V.; Duplaix, N.; Harris, J.D.; Hedges, S.; Long, B.; Mahood, S.P.; McGowan, P.J.K.; McShea, W.J.; Oliver, W.L.R.; Perkin, S.; Rawson, B.M.; Shepherd, C.R.; Stuart, S.N.; Talukdar, B.K.; van Dijk, P.P.; Vié, J.-C.; Walston, J.L.; Whitten, T.; Wirth, R. Why South-East Asia should be the world’s priority for averting imminent species extinctions, and a call to join a developing cross-institutional programme to tackle this urgent issue. SAPIENS 2012, 5, 76–95.
[61]
Catullo, G.; Masi, M.; Falcucci, A.; Maiorano, L.; Rondinini, C.; Boitani, L. A gap analysis of Southeast Asian mammals based on habitat suitability models. Biodivers. Conserv. 2008, 141, 2730–2744.
[62]
Yen, P.; Ziegler, S.; Huettmann, F.; Onyeahialam, A.I. Change detection of forest and habitat resources from 1973 to 2001 in Bach Ma National Park, Vietnam, using remote sensing imagery. Int. For. Rev. 2005, 7, 1–8.
[63]
Kelly, M.J. Design, evaluate, refine: Camera trap studies for elusive species. Anim. Conserv. 2008, 11, 182–184, doi:10.1111/j.1469-1795.2008.00179.x.
