Kasetsart J. (Nat. Sci.) 43 : 83 - 93 (2009)

Review Article “Rodent Biodiversity Human Health and Pest Control in a Changing Environments”

Rodent Biodiversity in Changing Environments

Jean-Christophe Auffray1*, Sabrina Renaud2 and Julien Claude1

ABSTRACT

Organisms adapt and evolve in response to environmental changes. Current changes in the environment occur at a rate and scale that are closer to those of mass extinction rather than of normal, background extinction. The response of species to global changes will depend on their ability to disperse and to acclimatize, as well as on their evolvability. The current view is that the high rate of current environmental changes impedes the evolutionary processes of adaptation to new conditions. Rodents, however, show a high potential to successfully adapt to changing environments over various time scales, including very rapid responses thanks to various characteristics of their life history, traits and plasticity. This paper briefly reviews the processes that allow rodents to respond to the challenges of changing environments, from the instantaneous plastic response to the paleontological perspective of long term evolution. Rodents indeed include very opportunistic and highly evolvable species, which may successfully overcome the ongoing changes, although some specialist species will inevitably be the victim of the adjustment of the communities to the human-driven modification of their environments. Key words: rodents, community, changing environment, adaptation, evolution

INTRODUCTION are often a source of diversification and can thus benefit the building and maintenance of The biosphere faces ongoing global biodiversity. What determines the ability of a change by variations that are drastic both by their species, group of organisms, or even individuals, amplitude and rapidity. It raises scientific, societal to successfully face a changing environment? The and political concerns about the ability of the processes involved vary depending on the spatial biosphere to respond to this complex cascade of and temporal scale of the changes. This paper processes, triggered by human activity, modifying provides a brief review of such processes, with a landscapes and climate. Organisms, however, have focus on rodents and the background question: faced changing environments throughout their how will the current rodent biodiversity face evolutionary history. If sometimes catastrophic in ongoing environmental changes? the case of mass extinction, environmental changes

1 Université Montpellier 2, Institut des Sciences de l’Evolution (CNRS), CC 065, 34095 Montpellier cedex 05, France. 2 Université Lyon 1, Paléoenvironnements et Paléobiosphère (CNRS), Bat. Géode, 2 rue Raphael Dubois, 69622 Villeurbanne, France. * Corresponding author, e-mail: [email protected] Received date : 30/10/08 Accepted date : 16/12/08 84 Kasetsart J. (Nat. Sci.) 43(1)

Rodents constitute a group of high relies on behavioural adjustments. In temperate interest in this context: they represent the most regions, the wood mouse Apodemus sylvaticus diverse order of mammals, with approximately forages in the open landscape during summer time 2000 species including nearly half of the to exploit the crops, being then territorial, but mammalian species. The specific richness of this retracts into forest during winter, sharing common order results from a succession of radiations and shelters (Butet, 1994). Such short-term tracking shows the potential of adaptation and of food availability by a change in the home range diversification in this group. In the context of has been also observed in the African striped human-driven environmental changes, rodents are mouse Rhabdomys pumilio (Schradin and Pillay, notable for the number of species that have 2006). successfully adapted to anthropic habitats. For These adjustments include a seasonal example, the house mouse (Mus musculus) and regulation of reproduction, with food availability the black and water rats (Rattus rattus and Rattus and/or quality being one trigger for starting norvegicus), have gained a world-wide distribution reproduction (Adler and Beatty, 1997; Leirs et al., because of their association with humans. 1994). Hence, behavioural plasticity in However, there are also species with a more reproductive traits allows rodent species to adjust restricted range, such as: the wood mouse quickly to changing environments (Vessey and Apodemus sylvaticus in Europe; the Vessey, 2007). In species displaying pluriannual multimammate rats Mastomys in Africa; the dynamics, such as arvicoline rodents, seasonality bandicoot rats Bandicota in southeast Asia; and of breeding has even been invoked as an important the rat Niviventer in China). Due to their successful factor conditioning population explosions and acclimatization to being in the vicinity of humans subsequent crashes (Tkadlec and Zejda, 1998; and their efficient reproduction, many of these Stenseth et al., 2003). species are a pest for the human populations they Adjustment to instantaneous conditions influence, either due to deterioration of crops, may also occur in response to predation, as shown spoiling of food stocks, or as vectors of various in bank voles suppressing breeding when exposed diseases. All these species pinpoint the high to cues of predator presence in their environment adaptive potential of some rodents and their ability (Ylönen and Ronkainen, 1994). to face changing environments even when These cases exemplify the potential for triggered by human activity. an adjustment of life-history traits and behaviour allowing rodents to face changing environments. Rodent populations in changing environments: Yet, seasonality and predation are somehow for mechanisms of short-term response rodents a predictable component, since they have Adjustment to short-term fluctuation been exposed to these factors throughout their Rodents are usually small-bodied evolutionary history. The mechanisms of response animals with a short life span. This is often to unpredictable changes may be different and their associated with a relatively “fast” life history. ability to adjust to new environments not as These characteristics enable a rapid population efficient. response to short term variation, including seasonal Acclimatization to new environments fluctuations in, among others, temperature, Murine rodents include Old World mice humidity conditions and food availability (Vessey and rats. Their diversity is maximal in the tropical and Vessey, 2007). areas of Africa and especially Asia (Misonne, Response to this pace of variation mostly 1969). This pattern exemplifies their preference Kasetsart J. (Nat. Sci.) 43(1) 85 for warm environments in contrast to arvicoline Unfavourable conditions are often rodents. Yet the house mouse managed a successful detected by an examination of life history traits, adaptation in developing permanent feral e.g. home range, size of the offspring and survival. populations on at least eight sub-Antarctic Islands Comparing such traits, one environment can (Berry et al., 1978). Experiments on artificial appear to be less adequate for a rodent species than selection for cold tolerance confirmed that another, e.g. sand dunes compared with woodlands adaptation to such conditions close to their for the wood mouse Apodemus sylvaticus physiological limits might achieve measurable (Attuquayefio et al., 1986). results in about 10 generations, with heavier and Such an approach, however, does not fatter mice and more concentrated milk (Barnett reveal whether any adjustment to the environment and Dickson, 1989). concerned was efficient or not. Phenotypic traits Arid environments are equally can then be relevant indicators of poor living demanding in terms of metabolic requirements, conditions. Developmental errors are likely to and water-availability can vary dramatically within occur in stressful conditions, being either of the distribution area of a species. This can lead to genetic or environmental origin and a adaptive differences in the energetic strategy, as quantification of the level of perturbation would exemplified by house mice on Porto Santo Island provide a measure of stress. Both sides of a (Mathias et al., 2004). In order to understand the symmetrically bilateral organism are supposed to process underlying the adjustment to changes in be coded by the same genotype. Accordingly, a the desiccating potential of the environment, a standard phenotype should express the perfect common desert rodent Dipodomys was cross-bred symmetry. Unless they are genetically determined, under either desiccating or water-abundant e.g. internal organs, any difference arising between conditions (Tracy and Walsberg, 2001). The the right and left sides of these organisms might experience showed that developmental plasticity be interpreted as a developmental perturbation and acclimatization completely accounted for the inappropriately corrected. This kind of asymmetry, existing intraspecific variability in desiccation the so-called fluctuating asymmetry (FA), thus resistance. indicates a developmental instability (DI). Though Such processes of phenotypic plasticity the underlying mechanisms have been poorly can operate quickly and therefore attenuate the identified, studies using FA have developed action of an apparently drastic natural selection considerably over the past two decades. and contribute to the success of rodents in Practically, appraising FA on a single changing environments. metric trait consists of estimating the variance of the left-minus-right distribution in a population. Stress and its estimation in wild populations Considering rodents, skull and teeth traits are often Despite this potential for acclimatization, used to evaluate DI. While several methods exist some environmental conditions are less favourable to compile a global index of FA for several metric than others to rodents, despite the fact that they or meristic characters, the advent of geometric may manage to survive. Partly because of societal morphometrics allows an appraisal of the global anxiety and political concern, human-driven asymmetry in a complex structure such as the skull changes are often interpreted as potentially or mandible (Auffray et al., 1996; 1999a; detrimental to wild species. Is this really the case? Klingenberg et al., 1998). The problem is then to identify which conditions Several examples of developmental are really harmful. instability in natural populations of rodents due to 86 Kasetsart J. (Nat. Sci.) 43(1) environmental changes are found in the literature. Mid-term response to changing environments: Using a synthetic index of FA, the populations of adaptation and adjustment of the communities voles (Apodemus sylvaticus) have been shown to Building of gradients present higher levels of FA when they were closely Many of the previous cases have shown located to Chernobyl (Ukraine). Obviously, in this the potential for short-term acclimatization of case, radiation subsequent to the reactor accident rodents. This has allowed them to have a rapid at the nuclear power plant was supposed to have response to changing environments; yet the had a direct effect on the development of the amplitude of the response is limited by the animals (Oletsky et al., 2004). Populations of bank potential of developmental plasticity and voles (Clethrionomys glareolus) presented higher acclimatization. In the long run, natural selection levels of FA in a disturbed environment (extensive should act to fix some traits involved in adaptation agriculture) when compared to traditional to the new conditions. Fine-tuning of adaptation agricultural fields in northern France (Marchand is partly counteracted by gene-flow from et al., 2003). In that case, the fragmentation of surroundings environments (Lenormand, 2002). habitat may have had several indirect Despite this buffering effect, adaptation to local consequences on rodent populations by restraining conditions can build if selection is strong enough. available resources, reducing the effective Such a clinal variation in metabolic characteristics population size and favouring inbreeding. In is exemplified by cold adaptation in the house Portugal, Mediterranean mice (Mus spretus) mouse Mus musculus domesticus (Lynch, 1992). exhibited a higher level of FA in a polluted area Yet, at this scale, adaptation can concern (heavy metal soils around copper mines) than in phenotypic characteristics other than those varying control locations (Nunes et al., 2001). Rats and with plasticity and acclimatization. Clinal mice, as laboratory animals, were often used for environmental variations often include a series of testing potential environmental stressors in physical factors that in turn cause variations in controlled conditions (for a review, see Hoffman vegetation and hence, of the food available. This and Parsons, 1991). will select traits associated with nutrition, If FA may provide an interesting signal including skeletal and dental characters such as on the suitability of habitat, it may also fail to mandible and teeth. Phenotypic expression of provide a reliable indication on the origin of patterns of clinal selection has thus been observed disturbance. A study on mole rats (Spalax in various rodents (Fadda and Corti, 2001; Duarte ehrenbergi) in Israel has considered several et al., 2000). The establishment of such gradients populations and numerous features related to these can be quite rapid on an evolutionary time scale. natural populations or their habitat: geographic and An example of this is the latitudinal gradient in climatic variables, soil type, genetic features the mandible and molar shape observed through (karyotypes, heterozygosity, genetic diversity) and western Europe in the wood mouse Apodemus parasitic load. A general trend of increasing FA sylvaticus, built up since the end of the last glacial together with altitude and indurate soil was maximum, when the species migrated northward observed. However, the fact that environmental from refugia to re-colonize deglaciated areas and genetic variables are highly covariant renders (Renaud and Michaux, 2007). it difficult to disentangle the origins of Changing climate triggering developmental instability (Auffray et al., 1999b). diversification: vicariance and refugia Species do not always have to adapt in order to respond to changing environment. The Kasetsart J. (Nat. Sci.) 43(1) 87 simplest way to cope with environmental changes speciation in allopatry in several rodent species, is often to track the same habitat by shifting their e.g. Oenomys (Renaud, 1999), the African wood area of distribution. In this case, no special mouse, Hylomyscus (Nicolas et al., 2006), and the metabolic or phenotypic adaptation will occur, but multimammate rat Mastomys (Robbins and Van one species can be split into several separate der Straeten, 1989). Environmental changes may isolates that will diverge progressively in the alternatively strengthen or weaken such barriers, prolonged absence of gene flow. favouring speciation or contact between the The glacial cycles that have characterized populations. the Earth’s history since the Pleistocene, caused many such fragmentations within species and may Rodents within community: ecological hence be viewed as a stimulating factor of processes, phenotypic expression? diversification. Widespread glaciers durably Previous sections provided a brief review hindered exchanges among wood mice of the possible responses of a single species to populations from both sides of the Alps, leading environmental changes. Yet, any species is part of to the significant differentiation of northwestern a small-mammal community that will influence and Italo-balkanic clades within Apodemus its habits and ability to cope with changes. The sylvaticus (Michaux et al., 2003). In the same way, coexistence of several rodent species within a the bank vole Clethrionomys glareolus community relies on resource partitioning. This (Deffontaine et al., 2005; Kotlik et al., 2006) or is achieved by exploiting various microhabitats the east Mediterranean mouse Mus macedonicus within a mosaic landscape (Price, 1978; Decher (Orth et al., 2002) repeatedly retracted into various and Bahian, 1999) and by the differential refugia during glacial cycles, leading to the exploitation of the resources, for example larger differentiation of geographic lineages. rodents consuming larger seeds (Brown and Such processes are not exclusive to Lieberman, 1973). Further aspects of habitat use temperate regions. Sub-tropical environments can contribute to segregation among species, such were also affected by the glacial cycles, that were as vertical segregation (Sekijima and Soné, 1994) expressed there as alternatively arid and more or temporal heterogeneity (Ben-Natan et al., humid phases. Hence, forest and open-field species 2004). were alternatively expanding and retracting. Such Hence, behavioural aspects strongly a process was likely the cause of a morphological contribute to this fine-scale resource partitioning. differentiation in tooth morphology between Yet, exploitation of food of a different size or central versus eastern Africa in the forest rusty- composition can be related to characteristics of nosed rat Oenomys hypoxanthus (Renaud, 1999). the feeding apparatus. Accordingly, rodent species Persistent biogeographic barriers can act over an within communities are structured according to the even-longer time scale, causing differentiation of size or shape of teeth (Millien-Parra and Loreau, many species across these boundaries. This was 2000; Dayan and Simberloff, 1994), showing that the case with the Dahomey gap in Africa that resource partitioning has a phenotypic expression. separates west Africa from the central African Changing environments affect the forest block. This “gap” corresponds to a zone of distribution of microhabitats and hence, the lower rainfall between the Volta and the Niger composition of the rodent community. The effect rivers, the rivers themselves acting as a barrier to of changing productivity is obvious - less dispersion for small mammals. The disjunction of productive habitats cannot support as many species forest habitat caused by this gap has led to a as richer ones (Brown and Lieberman, 1973). Yet, 88 Kasetsart J. (Nat. Sci.) 43(1) changing environments may also act on rodent the ecology, including diet (in most cases communities by modifying the structure of omnivorous but also herbivorous, insectivorous, landscapes. The equilibrium model of island worm eaters and seedeaters) and life habits biogeography (MacArthur and Wilson, 1963) (cursorial, arboreal, burrowing, amphibious, predicted a relationship between the number of richochetal). This diversity in diet and life habits species and the area of an island. Progressive has a phenotypic expression in the diversity of the impoverishment would not be random but would mandible shape, with convergent shape for result in assemblages of fewer species as a subset omnivorous versus herbivorous rodents (Michaux of the species present in richer communities, et al., 2007). Confronting molecular and according to their efficiency in sharing resources. morphological evolutionary rates provides further The island theory can be applied to many evidence that within omnivorous generalist continental contexts, habitat fragmentation leading rodents, differences in mandible shape to “island-like” patches of a given habitat. Indeed, accumulated slowly and progressively with time. the composition in desert rodent assemblages has In contrast, the occurrence of an ecological shown the predicted nested pattern in species specialization triggered an acceleration of composition (Patterson and Brown, 1991). morphological evolution and a departure from a A well-known case of such “island-like” phenotypic drift pattern (Renaud and Michaux, structure combined with an impact of climate 2007). Hence, both phylogenetic history and change is displayed by the rodent community of ecological strategy appear crucial in determining the Great Basin of western North-America, where the patterns of diversification. island-like mountain ranges are surrounded by The temporal dynamics of such a “seas” of desert shrublands. These habitat islands diversification can be observed in fossil lineages. are the remnants of a former contiguous network The interpretation of morphological changes in of mountain habitats fragmented by Holocene terms of phylogeny and ecology is then crucial, climate warming. This resulted in a progressive since only morphological remains can be found impoverishment of the fauna in the relict patches in paleontological deposits, and especially the (Brown, 1971). small but resistant teeth in the case of the rodents. Molar teeth are known as good phylogenetic Long-term evolution in changing environments markers (Misonne, 1969), but their shape is also Competition among species, resource related to diet in modern rodents, allowing partitioning and adjustment to the local inference of the ecology of past taxa based on their environment occur in a reduced time and space fossil remains (Renaud et al., 2005). scale. In contrast, radiation and evolutionary trends A survey of Mio-Pleistocene murine document long-term outputs. Can similar rodents in southwestern Europe pointed out first, processes be identified at different time scales as the importance of changing environment in determinants of biodiversity in rodents? opening new niches and allowing diversification. Within rodents, the subfamily Murinae During this period, a trend of decreasing exemplifies one episode of diversification temperature led to the opening of an initially- originating 12-14 Myrs ago and leading today to forested landscape. Starting from a generalist approximately 120 genera and 550 species in ancestor associated with forest habits, the increase Europe, southeast Asia, Australia and Africa of grassland allowed evolution towards grass- (Wilson and Reader, 2005). This radiation includes eating exhibited by Stephanomys, a rodent with a diversification according to numerous aspects of particular dental morphology interpreted as an Kasetsart J. (Nat. Sci.) 43(1) 89 adaptation to herbivory (Renaud et al., 2005). In related changes on wild fauna (Amori and Clout, the same deposits, however, the lineage leading 2003). Many of these endemic rodents disappeared to the modern wood mouse Apodemus displays a during archeological or modern times on islands. rather stable dental morphology, suggesting few Among others Microtus (Thyrrenicola) henseli and ecological changes throughout the 10 Myr record. Rhagomys orthodon on Sardinia and Corsica The discrepancies in the evolutionary trends as a became extinct during Roman times, presumably result of the same environmental change suggest due to the progressive introduction of alien species that one rodent colonized grass fields which that started at the beginning of the Neolithic period represented new habitats related to global cooling, (Vigne, 1992). Malpaisomys and Canariomys while the other tracked its original habitat that became extinct on the Canary Islands, probably remained present as forest patches in a mosaic due to several factors: alien predator species like landscape. dogs; competition with the introduced house In this case, changing environment is a mouse, Mus musculus; and possibly introduced key factor in triggering evolution, but the response parasites or diseases (Michaux et al., 1996). It is of the rodents is still conditioned by the ecological noteworthy, that one of the few endemic rodents strategy adopted. This latter aspect was likely to have successfully faced human arrival with its related to interspecific interactions. In fossil cortege of changes is the Cyprus mouse, Mus deposit, segregation in size and/or shape of the cypriacus (Cucchi et al., 2006). Phenotypically tooth morphology between the different species close to continental mice, it likely displays similar (Renaud, 1999) provides evidence of resource adaptability and proved competitively superior in partitioning similar to what has been observed in its local environment on Cyprus to the invading modern communities (Dayan and Simberloff, house mouse. 1994; Ledevin, 2007). One might argue that insular rodents evolved into a context characterized by a release Rodents and the ongoing human-driven in interspecific competition and predation, making changes them especially sensitive to the arrival of human- Previous examples show evidence of a related fauna. Changes in the landscape due to high adaptive potential in some rodents to face agricultural practices are nevertheless recognised changing and new environments. The two lineages as having strongly affected rodent communities, of fossil rodents, however, exemplify that the directly changing the available resources, ecological strategy may condition the long-term fragmenting the suitable habitat, or affecting the success: while the generalist wood mouse is still distribution of the predators (e.g. Delattre et al., flourishing today, the specialist Stephanomys was 1999; Hansson, 1999). Traditional agricultural not able to cope with the highly variable practices may contribute to a high local diversity Pleistocene climate and became extinct around 1.8 by maintaining a variety of resources (Decher and Myrs ago (Renaud et al., 2005). In a similar way, Bahian, 1999), whereas more intensive human opportunist species like the house mouse and rats impact may favour invasive species. Investigation are evidently successful in disturbed or anthropic of a rodent community close to the city of Boulder, habitats, but other species might be less successful Colorado found that suburban landscapes had a in coping with the range of perturbation occurring negative effect on the abundance of native rodents, due to human activity. whereas the house mouse was not affected (Bock Endemic rodents on islands illustrate et al., 2002) such a negative impact of human activity and Predicting the evolutionary output of the 90 Kasetsart J. (Nat. Sci.) 43(1) ongoing global change on rodent communities radiation in Spalax ehrenberghi superspecies would require too much complex modelling in the Near East. Journal of Evolutionnary coupled to detailed field observations. Some Biology 12: 207-221. conclusions emerge, however: rodents are Attuquayefio, D. K., M. L. Gorman and R. J. probably on the whole highly adaptable and prone Wolton. 1986. Home range size in the Wood to adjust rapidly to new environments. For sure, mouse Apodemus sylvaticus: habitat, sex and some species will successfully cope with human- seasonal differences. Journal of Zoology, driven changes as they have up until now. This London 210: 45-53. process, however, may select for some Barnett, S.A. and R.G. Dickson. 1989 Wild mice opportunistic species showing adequate life- in the cold: some findings on adaptation. history traits to the detriment of more specialist Biological Reviews 64(4): 317-340. species. Ben-Natan, G. Z. Abramsky, B.P. Kotler and J.S. Brown. 2004. Seeds redistribution in sand LITERATURE CITED dunes: a basis for coexistence of two rodent species. Oikos 105: 325-335. Adler, G.H. and R.P. Beatty. 1997. Changing Berry, R.J., J. Peters and R.J. van Aarde. 1978. reproductive rates in a Neotropical forest Sub-Antarctic house mice: colonization, rodent, Proechimys semispinosus. Journal of survival and selection. Journal of Zoology Animal Ecology 66: 472-480. 184:127–141. Amori, G and M. Clout. 2003. Rodents on islands: Bock, C.E., K.T. Vierling, S.L. Haire, J.D. Boone a conservation challenge, pp. 63-88. In G.R. and W.W. Merkle. 2002. Patterns of rodent Singleton, L.A. Hinds, C.J. Krebs and D.M. abundance on open-space grasslands in Spratt (eds). Rats, mice and people: rodent relation to suburban edges. Conservation biology and management. Australian Centre Biology 16(6): 1653-1658. for International Agricultural Research. Brown, J.H. 1971. Mammals on mountaintops: Canberra. nonequilibrium insular biogeography. Auffray, J.-C., P. Alibert, S. Renaud, A. Orth and American Naturalist 105: 467-478. F. Bonhomme. 1996. Fluctuating asymmetry Brown, J. H. and G. A. Lieberman. 1973. Resource in Mus musculus subspecific hybridization: utilization and coexistence of seed-eating Traditional and Procrustes comparative desert rodents in sand dune habitats. Ecology approach, pp. 275-283. In L. F. Marcus, M. 54(4): 788-797. Corti, A. Loy, D. Slice and G. Naylor (eds). Butet, A. 1994. Nutritional conditions and annual Advances in Morphometrics. Plenum. New fluctuations in Apodemus sylvaticus York. populations. Russian Journal of Ecology Auffray, J.-C., V. Debat and P. Alibert. 1999a. 25(2): 111-119. Shape Asymmetry and Developmental Cucchi, T., A. Orth, J.-C. Auffray, S. Renaud, L. Stability, pp. 309-324. In AJ Chaplain, GD Fabre, J. Catalan, E. Hadjisterkotis, F. Singh, JC MacLachlan (eds). On Growth and Bonhomme, J.D. Vigne. 2006. A new endemic Form - Spato-temporal Pattern Formation species of the subgenus Mus (Rodentia, in Biology. John Wiley and Son Ltd. Mammalia) on the Island of Cyprus. Zootaxa Chichester 1241: 1-36 Auffray, J.-C., S. Renaud, P. Alibert and E. Nevo. Dayan, T. and D. Simberloff. 1994. Morphological 1999b. Developmental stability and adaptive relationships among coexisting heteromyids: Kasetsart J. (Nat. Sci.) 43(1) 91

an incisive dental character. American Kotlík, P., V. Deffontaine, S. Mascheretti, J. Zima, Naturalist 143: 462-477. J.R. Michaux and J.B. Searle. 2006. A northern Decher, J. and L.K. Bahian. 1999. Diversity and glacial refugium for bank voles structure of terrestrial small mammal (Clethrionomys glareolus). Proceedings of communities in different vegetation types on the National Academy of Sciences, USA the Accra Plains of Ghana. Journal of 103(40): 14860-14864. Zoology 247: 395-408. Ledevin, R. 2007. Analyse de forme et de taille Deffontaine, V., R. Libois, P. Kotlík, R. Sommer, des mandibules et première molaire supérieure C. Nieberding, E. Paradis, J. B. Searle and J. du mulot Apodemus: influence de la R. Michaux. 2005. Beyond the Mediterranean phylogénie et de la géographie. In peninsulas: evidence of central European Paléontologie Sédimentologie glacial refugia for a temperate forest mammal Paléoenvironnements: 43. Lyon: Université species, the bank vole (Clethrionomys Lyon 1. glareolus). Molecular Ecology 14: 1727- Leirs, H. R. Verhagen and W. Verheyen. 1994. The 1739. basis of reproductive seasonality in Mastomys Delattre, P., B. De Sousa, E. Fichet-Calvet, J.-P. rats (Rodentia: Muridae) in Tanzania. Journal Quéré and P. Giraudoux. 1999. Vole outbreaks of Tropical Ecology 10(1): 55-66. in a landscape context : evidence from a six Lenormand, T. 2002. Gene flow and the limits to year study of Microtus arvalis. Landscape natural selection. Trends in Ecology and Ecology 14: 401-412. Evolution 17(4): 183-189. Duarte, L. C., L.R. Monteiro, F.J. Von Zuben and Lynch, C.B. 1992. Clinal variation in cold S.F. Dos Reis. 2000. Variation in mandible adaptation in Mus domesticus: verification of shape in Thrichomys apereoides (Mammalia: predictions from laboratory populations. Rodentia): Geometric analysis of a complex American Naturalist 139(6): 1219-1236. morphological structure. Systematic Biology MacArthur, R. H. and E.O. Wilson. 1963. An 49(3): 563-578. equilibrium theory of insular zoogeography. Fadda, C. and M. Corti. 2001. Three-dimensional Evolution 17(4): 373-387. geometric morphometrics of Arvicanthis: Marchand, H. L., G. Paillat, S. Montuire and A. implications for systematics and taxonomy. Butet. 2003. Fluctuating asymmetry in bank Journal of Zoological Systematics and vole populations (Rodentia, Arvicolinae) Evolutionary Research 39: 235-245. reflects stress caused by landscape Hansson, L. 1999. Intraspecific variation in fragmentation in the Mont-Saint-Michel Bay. dynamics: small rodents between food and Biological Journal of the Linnean Society predation in changing landscapes. Oikos 80(1): 37-44. 86(1): 159-169. Mathias, M. L., A.C. Nunes, C.C. Marques, I. Hoffmann, A. A. and P. A. Parson. 1991. Sousa, M.G. Ramalhinho, J.-C. Auffray, J. Evolutionary genetics and environmental Catalan and J. Britton-Davidian. 2004. stress. Oxford, Oxford University Press. Adaptive energetics in house mice, Mus Klingenberg, C. P. and G. S. McIntyre. 1998. musculus domesticus, from the island of Porto Geometric morphometrics of developmental Santo (Madeira archipelago, North Atlantic). instability: analyzing patterns of fluctuating Comparative Biochemistry and Physiology asymmetry with procrustes methods. Part A 137: 703-709. Evolution. 52(5): 1363-1375. Michaux, J., N. López-Martínez and J.-J. 92 Kasetsart J. (Nat. Sci.) 43(1)

Hernández-Pacheco. 1996. A 14C dating of most contaminated area in Chornobyl. Canariomys bravoi (Mammalia Rodentia), the Journal of Environmental Radioactivity 73: extinct giant rat from Tenerife (Canary islands, 1-20. Spain), and the recent history of the endemic Orth, A., J.-C. Auffray and F. Bonhomme. 2002. mammals in the archipelago. Vie et Milieu Two deeply divergent mitochondrial clades in 46(3/4): 261-266. the wild mouse Mus macedonicus reveal Michaux, J. R., E. Magnanou, E. Paradis , C. multiple glacial refuges south of Caucasus. Nieberding and R. Libois. 2003. Heredity 89: 353-357. Mitochondrial phylogeography of the Patterson, B.D. and J.H. Brown. 1991. Regionally Woodmouse (Apodemus sylvaticus) in the nested patterns of species composition in Western Palearctic region. Molecular granivorous rodent assemblages. Journal of Ecology 12: 685-697. Biogeography 18(4): 395-402. Michaux, J., P. Chevret and S. Renaud. 2007. Price, M. 1978. The role of microhabitat in Morphological diversity of Old World rats and structuring desert rodent communities. mice (Rodentia, Muridae) mandible in relation Ecology 59(5): 910-921. with phylogeny and adaptation. Journal of Renaud, S. 1999. Size and shape variability in Zoological Systematics and Evolutionary relation to species differences and climatic Research 45(3): 263-279. gradients in the African rodent Oenomys. Millien-Parra, V. and M. Loreau. 2000. Journal of Biogeography 26: 857-865. Community composition and size structure of Renaud, S., J. Michaux, P. Mein, J.-P Aguilar and murid rodents in relation to the biogeography J.-C. Auffray. 1999. Patterns of size and shape of the Japanese archipelago. Ecography 23: differentiation during the evolutionary 413-423. radiation of the European Miocene murine Misonne, X. 1969. African and Indo-Australian rodents. Lethaia 32: 61-71. Muridae. Evolutionary trends. Musée Royal Renaud, S. and J. R. Michaux. 2007. Mandibles de l’Afrique Centrale. Tervuren and molars of the wood mouse, Apodemus Nicolas, V., S. Quérouil, E. Verheyen, W. sylvaticus (L.): integrated latitudinal signal Verheyen, J.F. Mboumba, M. Dillen and M. and mosaic insular evolution. Journal of Colyn. 2006. Mitochondrial phylogeny of Biogeography 34(2): 339-355. African wood mice, genus Hylomyscus Renaud, S., J. Michaux, D.N. Schmidt, J.-P. (Rodentia, Muridae): implications for their Aguilar, P. Mein and J.-C. Auffray. 2005. taxonomy and biogeography. Molecular Morphological evolution, ecological Phylogenetics and Evolution 38(3): 779-793 diversification and climate change in rodents. Nunes, A. C., J.-C. Auffray and M. L. Mathias. Proceedings of the Royal Society of 2001. Developmental instability in a riparian London, Biological Sciences (serie B) 272: population of the Algerian mouse (Mus 609-617. spretus) associated with a heavy metal- Robbins, C. B. and E. Van der Straeten. 1989. polluted area in central Portugal. Archives of Comments on the systematics of Mastomys Environmental Contamination and Thomas 1915 with a description of a new West Toxicology 41(4): 515-521. African species (Mammalia: Rodentia: Oleksyk, T., J. Novak, P. JR, G. SP and S. MH. Muridae). Senckenbergiana Biologica 69:1– 2004. High levels of fluctuating asymmetry 14. in populations of Apodemus flavicollis from Schradin, C. and N. Pillay. 2006. Female striped Kasetsart J. (Nat. Sci.) 43(1) 93

mice (Rhabdomys pumilio) change their home to water loss in a desert rodent: investigating ranges in response to seasonal variation in the time course of adaptive changes. Journal food availability. Behavioral Ecology 17: of Comparative Physiology B 171(8): 669- 452-458. 679. Sekijima, T. and K. Soné. 1994. Role of Vessey, S.H. and K.B. Vessey. 2007. Linking interspecific competition in the coexistence behavior, life history and food supply with the of Apodemus argenteus and A. speciosus. population dynamics of white-footed mice Ecological Research 9: 237-244. (Peromyscus leucopus). Integrative Zoology Stenseth, N.C., H. Viljugrein, T. Saitoh, T.F. 2: 123-130. Hansen, M.O. Kittilsen, E. Bølviken and F. Vigne, J.-D. 1992. Zooarchaelogy and Glöckner. 2003. Seasonality, density biogeographical history of the mammals of dependence, and population cycles in Corsica and Sardinia since the last ice age. Hokkaido voles. Proceedings of the National Mammal Review 22: 87–96. Academy of Sciences, USA 100(20): 11478- Ylönen, H. and H. Ronkainen. 1994. Breeding 11483. suppression in the bank vole as antipredatory Tkadlec, E. and J. Zejda. 1998. Small rodent adaptation in a predictable environment. population fluctuations: The effects of age Evolutionary Ecology 8(6): 658-666. structure and seasonality. Evolutionary Wilson, D.E. and D.M. Reader. 2005. Mammals Ecology 12: 191-210. Species of the World: A Taxonomic and Tracy, R.L. and G.E. Walsberg. 2001. Geographic Reference. Smithsonian Developmental and acclamatory contributions Institution Press. Washington DC.