Journal of Biogeography (J. Biogeogr.) (2015) ORIGINAL Influence of past and future climate ARTICLE changes on the distribution of three Southeast Asian murine rodents Alice Latinne1,2,3*, Christine N. Meynard4,5, Vincent Herbreteau6, Surachit Waengsothorn7, Serge Morand2,8,9 and Johan R. Michaux1,10 1Conservation Genetics Unit, Institut de ABSTRACT Botanique, University of Liege, Liege, Aim We tested the influence of Pleistocene climatic fluctuations and the Belgium, 2Institut des Sciences de l’Evolution, potential effect of future climate change on Southeast Asian small mammal dis- CNRS-IRD-UM2, Universite de Montpellier 2, Montpellier, France, 3Department of tributions using two forest-dwelling (Leopoldamys herberti and Leopoldamys Parasitology, Faculty of Veterinary Medicine, sabanus) and one karst (Leopoldamys neilli) endemic rodent species as models. Kasetsart University, Bangkok, Thailand, Location Southeast Asia. 4INRA, UMR CBGP (INRA/IRD/CIRAD/ Montpellier SupAgro), Campus international Methods We used presence–absence data of genetically identified individuals, de Baillarguet, CS 30016 Montferrier-sur-Lez bioclimatic variables and species distribution modelling techniques to predict cedex, France, 5Virginia Institute of Marine potential distributions of the three studied species under current, past [Last Science, College of William & Mary, Interglacial (LIG) and Last Glacial Maximum (LGM)] and future conditions. Gloucester Point, VA, USA, 6IRD, UMR We applied a variety of modelling techniques and then used consensus tech- ESPACE-DEV (IRD, UM2, UAG, UR), niques to draw up robust maps of potential distribution ranges at all stages. Station SEAS-OI, Saint-Pierre, France, 7Environment and Resources Technology Results According to our models, these three Leopoldamys species did not Department, Thailand Institute of Scientific experience significant range contraction during the LGM. Our models revealed and Technological Research, Pathum Thani, substantial range contraction during the LIG for L. herberti in northern Indo- Thailand, 8Walai Rukhavej Botanical china, while its distribution expanded in southern Indochina. Evidence of a Research Institute, Mahasarakham University, southward range expansion during that period was also obtained for L. neilli, Maha Sarakham, Thailand, 9CNRS-CIRAD, whereas L. sabanus remained widely distributed in insular Southeast Asia but Centre Infectiologie Christophe Merieux du experienced a range contraction on the Thai-Malay Peninsula. The two future Laos, Vientiane, Laos PDR, 10CIRAD, UR climate change scenarios used predicted that large climatically suitable areas AGIRs, Campus International de Baillarguet, would still be available in the future for the three species. Montpellier, France 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 dur- ing the LIG. These Pleistocene refugia may have been localized in northern Indochina but our study also revealed that southern Indochina could provide *Correspondence: Alice Latinne, Conservation major potential refugia. Genetics Unit, Institut de Botanique (B22), Keywords University of Liege, Boulevard du Rectorat, 27, 4000 Liege, Belgium. Climate change, Last Glacial Maximum, Last Interglacial, Leopoldamys, E-mail: [email protected] Murinae, Pleistocene, rodents, Southeast Asia, species distribution modelling. periods, followed by northward recolonizations from south- INTRODUCTION ern refugia during interglacial periods, has been frequently The distributional response of plant and animal species to documented (Hewitt, 2004; Michaux et al., 2005; and refer- Pleistocene climate changes has been studied widely in Eur- ences therein). However, recent studies have demonstrated ope and North America. In these temperate regions, the con- that this pattern does not always apply. For example, north- traction of the northern range of many species during glacial ern regions of central and eastern Europe have also acted as ª 2015 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12528 Past and future distributions of three Leopoldamys species refugia for some temperate plant and animal species (Kotlık changes on mammal distributions in Southeast Asia are not et al., 2006; Stewart et al., 2010). In the tropics, the effects of yet clearly understood. the Pleistocene cyclic glaciations were less intense than in In this study, we selected three long-tailed giant rat species temperate regions but it has been suggested that the cooler belonging to the genus Leopoldamys (Rodentia, Muridae) to arid climate during glacial periods led to the formation of assess the influence of Pleistocene climatic fluctuations and isolated rain forest refugia in mountainous areas (Brandon- the potential effect of future climate change on small forest Jones, 1996; Haffer, 1997). However, little is currently known mammal distributions in Southeast Asia using SDMs. These regarding the distributional consequences of Pleistocene are interesting model species because their distinct distribu- climatic fluctuations for tropical species, especially in Southeast tions span a large portion of Southeast Asia and they have Asia. contrasting ecological and forest habitat requirements. Leo- Southeast Asia encompasses four biogeographical subre- poldamys sabanus (Thomas, 1887) (lineage L5 in Balakirev gions that host around 18% of all plant and animal species et al., 2013) is semi-arboreal and found in lowland Sundaic on Earth (Myers et al., 2000). A complex geological history forest habitats. Leopoldamys herberti (Kloss, 1916) (lineage and repeated climatic fluctuations over the last few million L1) occurs in primary and secondary evergreen lowland and years have influenced the biogeographical patterns of many montane forests of Indochina. Leopoldamys neilli (Marshall, species in the region and created a unique fauna character- 1977) (lineage L2) is endemic to limestone karsts of Indo- ized by high levels of endemism (Woodruff, 2010). In Asia, china. These giant rats may also play an important role in the glacial advance was less extensive than in Europe or forest regeneration as they are better seed dispersers than North America. Two main climate-related events may have many other rodent species in Southeast Asia and China contributed to diversification and population divergence dur- (Wells et al., 2009; Chang & Zhang, 2011). ing the Pleistocene in Southeast Asia. First, drastic changes The taxonomy of Leopoldamys species has been reviewed in the Southeast Asian landscape occurred throughout the recently and is now better understood. Six species were rec- Pleistocene as a result of sea-level variations. Parts of the ognized by Musser & Carleton (2005). Balakirev et al. (2013) Sunda shelf were repeatedly exposed and submerged during and Latinne et al. (2013a), however, suggested that an addi- this time period (Voris, 2000). Consequently, temporary land tional species existed in the Indochinese region, i.e. L. her- bridges were frequently created between the mainland and berti, a phylogenetic lineage that was previously thought to insular regions of Sundaland, possibly enabling biotic migra- belong to Leopoldamys edwardsi (Pages et al., 2010). Evi- tions from the mainland to the archipelago (Heaney, 1986). dence of L. herberti has been found in northern Thailand, Second, Pleistocene climatic fluctuations also contributed to Laos, Vietnam and Cambodia, but its occurrence in neigh- vegetation changes in Southeast Asia. However, the Quater- bouring countries has not been documented. Leopoldamys nary distribution of forest types in this region is still uncer- neilli has been described in Thailand but has also recently tain and highly debated (Hope et al., 2004; Bird et al., 2005; been discovered in northern Laos and Vietnam (Balakirev Cannon et al., 2009; Wurster et al., 2010). et al., 2013; Latinne et al., 2013a). The distribution of L. sab- Many Sundaic bird and mammal species did not seem to anus was previously thought to encompass both the Indochi- experience significant population fragmentation during the nese and Sundaic subregions, but Balakirev et al. (2013) and Last Glacial Maximum (LGM; 19–26.5 ka; Peltier & Fair- Latinne et al. (2013b) have shown that it is probably a Sun- banks, 2006) (Gorog et al., 2004; Lim et al., 2010; Lim & daic species with southern Thailand the northern limit of its Sheldon, 2011) but Indochinese forest-dwelling mammals range: it does not occur further north in Indochina. These (Brandon-Jones, 1996; Luo et al., 2004; Patou et al., 2010), molecular studies have therefore revealed important misclas- birds (Fuchs et al., 2008) and insects (Morgan et al., 2011) sification errors in previous studies, showing that current may have been restricted to allopatric rain forest refugia in knowledge of these species distributions is uncertain, as is some northern Southeast Asian mountain ranges during the conservation status of the three species. Leopoldamys neil- Pleistocene glacial periods before expanding southwards dur- li was previously classified as Endangered on the IUCN Red ing interglacial periods. However, recent studies combining List but is now considered