Climate change; Last Glacial Maximum; Last Interglacia; Leopoldamys; Murinae; Pleistocene; rodents; Southeast Asia; species distribution modelling
Abstract :
[en] Aim: We tested the influence of Pleistocene climatic fluctuations and the
potential effect of future climate change on Southeast Asian small mammal distributions
using two forest-dwelling (Leopoldamys herberti and Leopoldamys
sabanus) and one karst (Leopoldamys neilli) endemic rodent species as models.
Location: Southeast Asia.
Methods: We used presence–absence data of genetically identified individuals,
bioclimatic variables and species distribution modelling techniques to predict
potential distributions of the three studied species under current, past [Last
Interglacial (LIG) and Last Glacial Maximum (LGM)] and future conditions.
We applied a variety of modelling techniques and then used consensus techniques
to draw up robust maps of potential distribution ranges at all stages.
Results: According to our models, these three Leopoldamys species did not
experience significant range contraction during the LGM. Our models revealed
substantial range contraction during the LIG for L. herberti in northern Indochina,
while its distribution expanded in southern Indochina. Evidence of a
southward range expansion during that period was also obtained for L. neilli,
whereas L. sabanus remained widely distributed in insular Southeast Asia but
experienced a range contraction on the Thai-Malay Peninsula. The two future
climate change scenarios used predicted that large climatically suitable areas
would still be available in the future for the three species.
Main conclusions: Our model predictions contradict the well-established
hypothesis that Southeast Asian forest-dwelling species were confined to small
refugia during the LGM. Moreover, our results suggest that some Southeast
Asian taxa may have been distributed in their refugial state during the LIG
rather than the LGM. This could be because of vegetation changes that may
have occurred at that time as a result of the increased seasonality observed during
the LIG. These Pleistocene refugia may have been localized in northern
Indochina but our study also revealed that southern Indochina could provide
major potential refugia.
Disciplines :
Zoology
Author, co-author :
Latinne, Alice ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Meynard, Christine
Herbreteau, Vincent
Waengsothorn, Surachit
Morand, Serge
Michaux, Johan ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Language :
English
Title :
Influence of past and future climate changes on the distribution of three Southeast Asian murine rodents
Achard, F., Eva, H.D., Stibig, H.J., Mayaux, P., Gallego, J., Richards, T. & Malingreau, J.P. (2002) Determination of deforestation rates of the world's humid tropical forests. Science, 297, 999-1002.
Araújo, M.B. & New, M. (2007) Ensemble forecasting of species distributions. Trends in Ecology and Evolution, 22, 42-47.
Bacon, A.M., Demeter, F., Rousse, S., Long, V.T., Duringer, P., Antoine, P.O., Thuy, N.K., Mai, B.T., Huong, N.T.M., Dodo, Y., Matsumura, H., Schuster, M. & Anezaki, T. (2006) New palaeontological assemblage, sedimentological and chronological data from the Pleistocene Ma U'Oi cave (northern Vietnam). Palaeogeography, Palaeoclimatology, Palaeoecology, 230, 280-298.
Balakirev, A.E., Abramov, A.V. & Rozhnov, V.V. (2013) Revision of the genus Leopoldamys (Rodentia, Muridae) as inferred from morphological and molecular data, with a special emphasis on the species composition in continental Indochina. Zootaxa, 3640, 521-549.
Bertelsmeier, C., Guénard, B. & Courchamp, F. (2013) Climate change may boost the invasion of the Asian needle ant. PLoS ONE, 8, e75438.
Bird, M.I., Taylor, D. & Hunt, C. (2005) Palaeoenvironments of insular Southeast Asia during the Last Glacial Period: a savanna corridor in Sundaland? Quaternary Science Reviews, 24, 2228-2242.
Brandon-Jones, D. (1996) The Asian Colobinae (Mammalia: Cercopithecidae) as indicators of Quaternary climatic change. Biological Journal of the Linnean Society, 59, 327-350.
Butler, C.J., Wheeler, E.A. & Stabler, L.B. (2012) Distribution of the threatened lace hedgehog cactus (Echinocereus reichenbachii) under various climate change scenarios. The Journal of the Torrey Botanical Society, 139, 46-55.
Cannon, C.H., Morley, R.J. & Bush, A.B.G. (2009) The current refugial rainforests of Sundaland are unrepresentative of their biogeographic past and highly vulnerable to disturbance. Proceedings of the National Academy of Sciences USA, 106, 11188-11193.
Chaimanee, Y. (1998) Plio-Pleistocene rodents of Thailand. Thai Studies in Biodiversity, 3, 1-303.
Chang, G. & Zhang, Z. (2011) Differences in hoarding behaviors among six sympatric rodent species on seeds of oil tea (Camellia oleifera) in Southwest China. Acta Oecologica, 37, 165-169.
Chiu, C.-A., Lin, P.-H., Hsu, C.-K. & Shen, Z.-H. (2012) A novel thermal index improves prediction of vegetation zones: associating temperature sum with thermal seasonality. Ecological Indicators, 23, 668-674.
Clements, R., Sodhi, N.S., Schilthuizen, M. & Ng, P.K.L. (2006) Limestone karsts of southeast Asia: imperiled arks of biodiversity. BioScience, 56, 733-742.
Dai, C., Zhao, N., Wang, W., Lin, C., Gao, B., Yang, X., Zhang, Z. & Lei, F. (2011) Profound climatic effects on two East Asian black-throated tits (Ave: Aegithalidae), revealed by ecological niche models and phylogeographic analysis. PLoS ONE, 6, e29329.
Esposito, M., Reyss, J.-L., Chaimanee, Y. & Jaeger, J.-J. (2002) U-series dating of fossil teeth and carbonates from Snake Cave, Thailand. Journal of Archaeological Science, 29, 341-349.
Fang, J.-Y., Ohsawa, M. & Kira, T. (1996) Vertical vegetation zones along 30° N latitude in humid East Asia. Vegetatio, 126, 135-149.
Fielding, A.H. & Bell, J.F. (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation, 24, 38-49.
Fuchs, J., Ericson, P.G.P. & Pasquet, E. (2008) Mitochondrial phylogeographic structure of the white-browed piculet (Sasia ochracea): cryptic genetic differentiation and endemism in Indochina. Journal of Biogeography, 35, 565-575.
Gorog, A.J., Sinaga, M.H. & Engstrom, M.D. (2004) Vicariance or dispersal? Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer, Leopoldamys sabanus and Maxomys whiteheadi). Biological Journal of the Linnean Society, 81, 91-109.
Haffer, J. (1997) Alternative models of vertebrate speciation in Amazonia: an overview. Biodiversity and Conservation, 6, 451-476.
Heaney, L.R. (1986) Biogeography of mammals in SE Asia: estimates of rates of colonization, extinction and speciation. Biological Journal of the Linnean Society, 28, 127-165.
Heaney, L.R. (1991) A synopsis of climatic and vegetational change in Southeast Asia. Climatic Change, 19, 53-61.
Hewitt, G.M. (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 183-195.
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978.
Hope, G., Kershaw, A.P., van der Kaars, S., Xiangjun, S., Liew, P.M., Heusser, L.E., Takahara, H., McGlone, M., Miyoshi, N. & Moss, P.T. (2004) History of vegetation and habitat change in the Austral-Asian region. Quaternary International, 118, 103-126.
IPCC (2007) Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK.
Jimenez-Valverde, A. & Lobo, J.M. (2007) Threshold criteria for conversion of probability of species presence to either-or presence-absence. Acta Oecologica, 31, 361-369.
Kotlík, P., Deffontaine, V., Mascheretti, S., Zima, J., Michaux, J.R. & Searle, J.B. (2006) A northern glacial refugium for bank voles (Clethrionomys glareolus). Proceedings of the National Academy of Sciences USA, 103, 14860-14864.
Kriticos, D.J., Webber, B.L., Leriche, A., Ota, N., Macadam, I., Bathols, J. & Scott, J.K. (2012) CliMond: global high-resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods in Ecology and Evolution, 3, 53-64.
Latinne, A., Waengsothorn, S., Herbreteau, V. & Michaux, J.R. (2011) Evidence of complex phylogeographic structure for the threatened rodent Leopoldamys neilli, in Southeast Asia. Conservation Genetics, 12, 1495-1511.
Latinne, A., Waengsothorn, S., Rojanadilok, P., Eiamampai, K., Sribuarod, K. & Michaux, J.R. (2012) Combined mitochondrial and nuclear markers revealed a deep vicariant history for Leopoldamys neilli, a cave-dwelling rodent of Thailand. PLoS ONE, 7, e47670.
Latinne, A., Chaval, Y., Waengsothorn, S., Rojanadilok, P., Eiamampai, K., Sribuarod, K., Herbreteau, V., Morand, S. & Michaux, J.R. (2013a) Is Leopoldamys neilli (Rodentia, Muridae) a synonym of Leopoldamys herberti? A reply to Balakirev et al. (2013). Zootaxa, 3731, 589-598.
Latinne, A., Waengsothorn, S., Rojanadilok, P., Eiamampai, K., Sribuarod, K. & Michaux, J.R. (2013b) Diversity and endemism of Murinae rodents in Thai limestone karsts. Systematics and Biodiversity, 11, 323-344.
Lim, H.C. & Sheldon, F.H. (2011) Multilocus analysis of the evolutionary dynamics of rainforest bird populations in Southeast Asia. Molecular Ecology, 20, 3414-3438.
Lim, H.C., Zou, F., Taylor, S.S., Marks, B.D., Moyle, R.G., Voelker, G. & Sheldon, F.H. (2010) Phylogeny of magpie-robins and shamas (Aves: Turdidae: Copsychus and Trichixos): implications for island biogeography in Southeast Asia. Journal of Biogeography, 37, 1894-1906.
Liu, C.R., Berry, P.M., Dawson, T.P. & Pearson, R.G. (2005a) Selecting thresholds of occurrence in the prediction of species distributions. Ecography, 28, 385-393.
Liu, W., Huang, Y., An, Z., Clemens, S.C., Li, L., Prell, W.L. & Ning, Y. (2005b) Summer monsoon intensity controls C4/C3 plant abundance during the last 35 ka in the Chinese Loess Plateau: carbon isotope evidence from bulk organic matter and individual leaf waxes. Palaeogeography, Palaeoclimatology, Palaeoecology, 220, 243-254.
Lunde, D.P. & Aplin, K. (2008) Leopoldamys neilli. IUCN Red List of Threatened Species. Version 2014.2. Available at: http://www.iucnredlist.org.
Lunde, D.P., Aplin, K., Ruedas, L.A. & Molur, S. (2008) Leopoldamys sabanus. IUCN Red List of Threatened Species. Version 2014.2. Available at: http://www.iucnredlist.org.
Luo, S.-J., Kim, J.-H., Johnson, W.E. et al. (2004) Phylogeography and genetic ancestry of tigers Panthera tigris. PLoS Biology, 2, e442.
Marmion, M., Parviainen, M., Luoto, M., Heikkinen, R.K. & Thuiller, W. (2009) Evaluation of consensus methods in predictive species distribution modelling. Diversity and Distributions, 15, 59-69.
Medway, L. (1977) The Niah excavations and an assessment of the impact of early man on mammals in Borneo. Asian Perspectives, 20, 51-69.
Michaux, J.R., Libois, R. & Filippucci, M.G. (2005) So close and so different: comparative phylogeography of two small mammal species, the yellow-necked fieldmouse (Apodemus flavicollis) and the woodmouse (Apodemus sylvaticus) in the western Palearctic region. Heredity, 94, 52-63.
Morgan, K., O'Loughlin, S.M., Chen, B., Linton, Y.M., Thongwat, D., Somboon, P., Fong, M.Y., Butlin, R., Verity, R., Prakash, A., Htun, P.T., Hlaing, T., Nambanya, S., Socheat, D., Dinh, T.H. & Walton, C. (2011) Comparative phylogeography reveals a shared impact of Pleistocene environmental change in shaping genetic diversity within nine Anopheles mosquito species across the Indo-Burma biodiversity hotspot. Molecular Ecology, 20, 4533-4549.
Musser, G.G. & Carleton, M. (2005) Superfamily Muroidea. Mammal species of the world: a taxonomic and geographic reference (ed. by D.E. Wilson and D.M. Reeder), pp. 894-1531. Johns Hopkins University Press, Baltimore, MD.
Musser, G.G., Lunde, D.P. & Son, N.T. (2006) Description of a new genus and species of rodent (Murinae, Muridae, Rodentia) from the tower karst region of northeastern Vietnam. American Museum Novitates, 3517, 1-41.
Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853-858.
Nikolova, I., Yin, Q., Berger, A., Singh, U.K. & Karami, M.P. (2013) The last interglacial (Eemian) climate simulated by LOVECLIM and CCSM3. Climate of the Past, 9, 1789-1806.
Pagès, M., Chaval, Y., Herbreteau, V., Waengsothorn, S., Cosson, J.F., Hugot, J.P., Morand, S. & Michaux, J. (2010) Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC Evolutionary Biology, 10, 184.
Patou, M.L., Wilting, A., Gaubert, P., Esselstyn, J.A., Cruaud, C., Jennings, A.P., Fickel, J. & Veron, G. (2010) Evolutionary history of the Paradoxurus palm civets: a new model for Asian biogeography. Journal of Biogeography, 37, 2077-2097.
Peltier, W.R. & Fairbanks, R.G. (2006) Global glacial ice volume and Last Glacial Maximum duration from an extended Barbados sea level record. Quaternary Science Reviews, 25, 3322-3337.
Penny, D. (2001) A 40, 000 year palynological record from north-east Thailand; implications for biogeography and palaeo-environmental reconstruction. Palaeogeography, Palaeoclimatology, Palaeoecology, 171, 97-128.
Peterson, A.T. & Ammann, C.M. (2013) Global patterns of connectivity and isolation of populations of forest bird species in the late Pleistocene. Global Ecology and Biogeography, 22, 596-606.
Porretta, D., Mastrantonio, V., Bellini, R., Somboon, P. & Urbanelli, S. (2012) Glacial history of a modern invader: phylogeography and species distribution modelling of the Asian Tiger mosquito Aedes albopictus. PLoS ONE, 7, e44515.
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Sang, W. (2009) Plant diversity patterns and their relationships with soil and climatic factors along an altitudinal gradient in the middle Tianshan Mountain area, Xinjiang, China. Ecological Research, 24, 303-314.
Shackleton, N.J., Sánchez-Goñi, M.F., Pailler, D. & Lancelot, Y. (2003) Marine isotope substage 5e and the Eemian interglacial. Global and Planetary Change, 36, 151-155.
Slik, J.W.F., Aiba, S.I., Bastian, M. et al. (2011) Soils on exposed Sunda Shelf shaped biogeographic patterns in the equatorial forests of Southeast Asia. Proceedings of the National Academy of Sciences USA, 108, 12343-12347.
Stewart, J.R., Lister, A.M., Barnes, I. & Dalén, L. (2010) Refugia revisited: individualistic responses of species in space and time. Proceedings of the Royal Society B: Biological Sciences, 277, 661-671.
Storm, P., Aziz, F., de Vos, J., Kosasih, D., Baskoro, S., Ngaliman & van den Hoek Ostende, L.W. (2005) Late Pleistocene Homo sapiens in a tropical rainforest fauna in East Java. Journal of Human Evolution, 49, 536-545.
Voris, H.K. (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography, 27, 1153-1167.
Wang, Y., Cheng, H., Edwards, R.L., Kong, X., Shao, X., Chen, S., Wu, J., Jiang, X., Wang, X. & An, Z. (2008) Millennial- and orbital-scale changes in the East Asian monsoon over the past 224, 000 years. Nature, 451, 1090-1093.
Wang, X., Sun, X., Wang, P. & Stattegger, K. (2009) Vegetation on the Sunda Shelf, South China Sea, during the Last Glacial Maximum. Palaeogeography, Palaeoclimatology, Palaeoecology, 278, 88-97.
Wang, W., McKay, B.D., Dai, C., Zhao, N., Zhang, R., Qu, Y., Song, G., Li, S.-H., Liang, W., Yang, X., Pasquet, E. & Lei, F. (2013) Glacial expansion and diversification of an East Asian montane bird, the green-backed tit (Parus monticolus). Journal of Biogeography, 40, 1156-1169.
Wells, K., Kalko, E.K.V., Lakim, M.B. & Pfeiffer, M. (2007) Effects of rain forest logging on species richness and assemblage composition of small mammals in Southeast Asia. Journal of Biogeography, 34, 1087-1099.
Wells, K., Corlett, R.T., Lakim, M.B., Kalko, E.K.V. & Pfeiffer, M. (2009) Seed consumption by small mammals from Borneo. Journal of Tropical Ecology, 25, 555-558.
Westaway, K.E., Morwood, M.J., Roberts, R.G., Rokus, A.D., Zhao, J.X., Storm, P., Aziz, F., van den Bergh, G., Hadi, P., Jatmiko & de Vos, J. (2007) Age and biostratigraphic significance of the Punung Rainforest Fauna, East Java, Indonesia, and implications for Pongo and Homo. Journal of Human Evolution, 53, 709-717.
Woodruff, D.S. (2010) Biogeography and conservation in Southeast Asia: how 2.7 million years of repeated environmental fluctuations affect today's patterns and the future of the remaining refugial-phase biodiversity. Biodiversity and Conservation, 19, 919-941.
Wurster, C.M., Bird, M.I., Bull, I.D., Creed, F., Bryant, C., Dungait, J.A.J. & Paz, V. (2010) Forest contraction in north equatorial Southeast Asia during the Last Glacial Period. Proceedings of the National Academy of Sciences USA, 107, 15508-15511.
Yang, S., Ding, Z., Wang, X., Tang, Z. & Gu, Z. (2012) Negative δ18O-δ13C relationship of pedogenic carbonate from northern China indicates a strong response of C3/C4 biomass to the seasonality of Asian monsoon precipitation. Palaeogeography, Palaeoclimatology, Palaeoecology, 317-318, 32-40.
Zhao, N., Dai, C., Wang, W., Zhang, R., Qu, Y., Song, G., Chen, K., Yang, X., Zou, F. & Lei, F. (2012) Pleistocene climate changes shaped the divergence and demography of Asian populations of the great tit Parus major: evidence from phylogeographic analysis and ecological niche models. Journal of Avian Biology, 43, 297-310.
Zheng, S. (1993) Quaternary rodents of Sichuan-Guizhou area. Science Press, Beijing, China.
