Abstract
We surveyed the distribution of small terrestrial mammals along the Da (Black) River in the Bac Yen district, Son La province, Vietnam. We recorded 21 species in the area. Species identifications were carried out using morphological and genetic methods in accordance with up-to-date taxonomy. The Da River is traditionally considered a zoogeographic boundary dividing different biogeographic regions in northern Vietnam. Our study was aimed at testing whether it can really be considered as such. Based on the observed distributions, we conclude that the water course is not the distribution boundary for 14 species out of 21 found in the area. Out of the seven remaining species, only those which are associated with the Chinese mountain-forest faunal complex demonstrate their southern boundary along the Da River. Thus, it is unjustified to consider this river as a biogeographic boundary for mammals.
Introduction
Vietnam belongs to the Indochinese subregion of the Indo-Malayan (Oriental) zoogeographic region (Takhtadzhyan 1978, Wikramanayake et al. 2002, Holt et al. 2013). The Indochinese subregion also includes Myanmar, Laos, Thailand, Cambodia, and the southern provinces of China. It is evident that the boundary between two natural zones passes through the territory of Vietnam—the northern subtropical zone, including elements of the Palearctic biota, and the southern zone, with elements of tropical Malayan ecosystems (Takhtadzhyan 1978, Krivolutskiy et al. 1995). Nevertheless, there are still few studies devoted to the biogeographical regions of Vietnam and of eastern Indochina as a whole.
The division of the territory of Vietnam into regions and subregions is generally based on the physical geography of the country proposed by Vu (1980) and does not always coincide with the distributions among different taxonomic groups of organisms. There are disputes regarding the location of the border between the northern Indochinese and southern Indochinese faunas. According to some authors, the boundary between these zones passes through central Vietnam (Dao 1978b, Cao 1989, 1998, Fooden 1996, Kuznetsov 2006); according to another scheme, it is shifted to the north and follows the Ma River in Thanh Hoa Province (Bobrov 1993); according to the botanical scheme, only the highland regions of northwestern and northern Vietnam are included in the northern Oriental zone (Averyanov et al. 2003, Krivolutskiy et al. 1995, Monastyrskiy 2007, 2010).
Northern Vietnam is divided into two biogeographic regions—northwestern and northeastern. The boundary between these divisions is traditionally taken to be the Da “Black” River and the Hoang Lien Ridge (Dao 1978a, 1978b, Cao 1989). However, this point of view is disputed by Abramov (2013, 2017), who, based on data on the geographical distribution of insectivorous mammals, comes to the conclusion that such a boundary may not be directly straight along the Da River and the Hoang Lien Ridge, as assumed by early Vietnamese researchers, but may run along the valley of the Hong “Red” River. This interpretation is supported by the distribution of white-toothed shrews (Crocidura attenuata, C. wuchihensis, and C. sapaensis), some species of moles (Euroscaptor orlovi and E. kuznetsovi), and a number of other species of mammals, primarily a number of species of squirrels of the genera Dremomys and Tamiops, some species of Niviventer, Eothenomys, Micromys, and Typhlomys of Oriental origin (Abramov 2017).
The distribution of a number of small terrestrial mammal species is limited to northeastern Vietnam. Several rodents and insectivorous species characteristic for this region (Crocidura attenuata, C. wuchihensis, Chodsigoa caovansunga, Leopoldamys edwardsi, Niviventer lotipes, N. langbianis, Petaurista alboniger, etc.) are also present in south-southeastern China. Endemic to northeastern Vietnam, but not found in China are species such as Euroscaptor kuznetsovi, Crocidura guy, as well as members of the endemic genus of tonkin rock rats, Tonkinomys (Musser et al., 2006, Balakirev et al., 2012, 2023), which are ecologically associated with karst regions. While other species are found throughout northern Vietnam: Chodsigoa parca, Crocidura dracula, Blarinella quadraticauda, Mogera latouchei, and Euroscaptor subanura.
In fact, there has been a long-standing debate over which of the two rivers, the Da or the Hong, is the biogeographic boundary in northern Vietnam. However, no mammal studies have yet directly tested these hypotheses. The main aim of this study was to analyze the contact boundary of zoogeographic regions along the East Indochina and South China biogeographical regions on both banks of the Da River, which crosses the Bac Yen District in Son La Province. The river, especially in its lower reaches, cannot be considered a serious barrier. Even taking into account the constructed hydroelectric structures (like Hoa Binh Dam and Son La Dam), the width of its natural channel does not exceed 200 m and the flow rate is never higher than 1 m s−1. The area is characterized by a tropical monsoon climate, with summer-autumn floods, which are not particularly destructive. This region contains a number of nature reserves and intact natural areas in which the natural fauna of small terrestrial mammals is preserved. There is still no exhaustive taxonomic list of small mammals for the territory, based on accurate species diagnostics and modern taxonomy. A clear understanding of species distributions and of the boundaries of biogeographic regions, as well as the causes of their formation is an important basis for the protection of biological diversity.
Material and methods
The small terrestrial mammals were trapped by snap traps during one of the recent theriological expeditions organized by the Russian-Vietnamese Tropical Research and Technological Center in Son La Province, Bac Yen District, within Xin Vang, Hang Dong, Ta Xua, Bac Yen, Song Pe, Hong Ngai, Ta Khoa, and Hua Nhan communes, within and in the vicinity of Ta Xua Nature Reserve. The field surveys were carried out during the period 21–30 November 2023. Our research goal was the analysis of the diversity of small mammals in the area of the zoogeographic boundary of the eastern Indochina and south China biogeographical regions, which follows the Ba River, crossing the study area. The nine points of capture of animals are shown on the map in Fig. 1.
Study area with animal sampling sites
Citation: Animal Taxonomy and Ecology 71, 1; 10.1556/1777.2025.00056
Species identification for most species was carried out in the field based on morphological characteristics (Francis 2008). External measurement was performed directly in the field. The standard external body measurements (head and body length, tail length, hind-foot length, ear length) were taken. Weight was taken in grams with a compact digital balance. Voucher specimens of each species were taken for confirmation of the record and further comparison with museum collections for clear taxonomical attribution by in-depth morphological and genetic analyses.
For species that's precise identification based on external morphological characteristics was not feasible, as well as in questionable cases, species diagnostics were carried out later based on genetic data. All morphological samples were preserved in technical grade 70% ethanol. Voucher specimens were cataloged and studied at the Zoological Museum of Moscow State University (ZMMU, Moscow, Russia).
For genetic analyses, small pieces of liver were stored in 96% molecular grade ethanol and used for the DNA extraction. The total genomic DNA was extracted using a routine phenol/chloroform/proteinase K protocol (Kocher et al. 1989, Sambrook et al. 1989). Each individual was genotyped by partial Cyt b (398-1140 bp positions) and COI genes (680 bp) and compared with all homologous sequences available in Gene Bank by DNA BLAST procedure. Universal routine PCR protocols were used to amplify mtDNA fragments as follows: initial denaturation for 1 min 30 s at 95°C, denaturation for 30 s at 95°C, annealing for 1 min at 52°C, and elongation for 45 s at 72°C, followed by terminal elongation for 3 min at 72°C. The PCR reaction was performed in a 25 µl volume that contained 2.5–3 mL of 10× standard PCR buffer, 50 mM of each dNTP, 2 mM MgCl, 10 pmol of each primer, 1 unit of Taq DNA polymerase, and 20–50 ng of total DNA template per tube. The Cyt b gene was amplified directly using primer pair L14724 (5′-CGAAGCTTGATATGAAAAACCTCGTTG-3'; Irwin et al. 1991) and H15915 (5′-GGAATTCATCTCTCCGGTTTACAAGAC-3'; Kocher et al. 1989).
For the COI gene, we sequenced the one-time routine BOLD primers LCO1490 and HCO2198 (5′-GGTCAACAAATCATAAAGATATTGG-3′ and 5′-TAAACTTCAGGGTGACCAAAAAATCA-3′), and followed the protocols explained in Hebert et al. (2003). The genetic sequences obtained were deposited in Genbank and are available under accession numbers PQ328088-PQ328118. The DNA sequences of reference species previously used in taxonomic works, the species affiliation of which was determined and reliably confirmed by various methods, were used as genetic vouchers.
Results
We obtained 126 specimens of animals and confirmed the occurrence of at least 21 species of small mammals inhabiting the Bac Yen region and Ta Xua Nature Reserve, both scansorial and arboreal. Two species were recorded in the region for the first time. An annotated list of mammals is provided in Table 1. Short taxonomic notes and references are provided in Discussion below for every species.
List of the mammal species recorded in the study area
| Species | South-Western bank | North-Eastern bank | N captured [ ] and Location of capture | Comments |
| Tupaia sinensis | + | [1], 1 | Common species; listed as Tupaia glis by Dang et al. (1994, 2008) | |
| Neotetracus sinensis | + | [4], 1–2 | Rare species; often confused with Hylomys suillis in the region. | |
| Hylomys suillus | + | [2], 9 | Common species; may be confused with Neotetracus sinensis in the region | |
| Rattus andamanensis | + | + | [18], 4–9 | Common species; may be confused with any others Rattus species in the region |
| Rattus tanezumi | + | (+) | [20], 6 | Common species; listed as R. rattus germaini by Kuznetsov (2006) and Dang et al. (1994, 2008) |
| Mus cookie | (+) | + | [6], 4–5 | Few specimens collected in rural habitats |
| Mus pahari | + | [1], 8 | Only found in forests | |
| Niviventer lotipes | + | [13], 1 | Common species; listed as N. niviventer by Dang et al. (1994, 2008) | |
| Niviventer fulvescens | + | [27], 1–3 | Common species in mountain regions | |
| Niviventer mekongis | + | [4], 7–8 | Rare species, uncorrectly listed as Rattus fulvescens or Niviventer bukit by more recent literature | |
| Chiromyscus thomasi | + | (+) | [3], 9 | Rare species; listed as Chiromyscus chiropus by Dang et al. (1994, 2008) and former sources |
| Leopoldamys edwardsi | + | + | [5], 1, 5–6 | Common species |
| Leopoldamys herberty | + | (+) | [1], 2 | Common species |
| Berylmys bowersi | (+) | + | [4], 1–2, 5 | Common species; erroneously described as a new species and genus under the name Pseudoberylmys muongbangensis by Tran et al. (2009) |
| Typhlomys taxuansis sp. nov | + | [1], 1 | New species of Typhlomys, for a description see Balakirev et al. (2024) | |
| Eothenomys miletus | + | [6], 1 | Few specimens collected at higher elevations; listed as E. melanogaster by Dang et al. (1994, 2008) | |
| Tamiops swinhoei | + | [1], 2 | Rare species; may be confused with congeneric species in the region | |
| Tamiops maritimus | + | [2], 9 | Common species | |
| Dremomys ornatus | (+) | + | [1], 2 | Common species; listed as D. rufigenis by Dang et al. (1994, 2008) |
| Dremomys gularis | + | [2], 1 | Rare species, distributed only at higher elevations. | |
| Callosciurus erythraeus | + | (+) | [1], 6 | Common species |
Footnote: (+) indicates that although this species was not captured during our surveys, it was reliably recorded in the region earlier. Location points numeration as in Figure 1.
The cladogram of species relationships according to the genetic data from the cytochrome b gene is shown in Fig. 2.
Cladogram of species relationships according to the cytochrome b gene data. For the Minimum Evolution (ME) tree, bootstrap values are shown at the tree nodes. Sample vouchers and gene bank accession numbers are indicated in the sample names
Citation: Animal Taxonomy and Ecology 71, 1; 10.1556/1777.2025.00056
Discussion
ORDER: SCANDENTIA
Family: TUPAIIDAE Gray, 1825
Genus: Tupaia Raffles, 1821
Tupaia chinensis (Anderson, 1879)
ORDER: ERINACEOMORPHA Gregory, 1910
Family: ERINACEIDAE G. Fischer, 1814
Subfamily: Galericinae Pomel, 1848
Genus: Hylomys Müller, 1840
Hylomys suillus peguensis (Blyth, 1859)
Genus: Neotetracus Trouessart, 1909
Neotetracus sinensis Trouessart, 1909
ORDER: RODENTIA
Family: MURIDAE Illiger, 1811
Genus: Rattus (Fischer, 1803)
Rattus andamanensis Blyth, 1860
The taxonomy of the genus Rattus remains controversial. Rattus andamanensis is the only non-synanthropic Rattus species in southeast Asia. It is widely distributed in southern China (Yunnan, Guangxi, Fujian, Hong Kong, and Hainan Island), Vietnam (including coastal islands; Kuznetsov & Pham 1992, where it was recorded as koratensis), Laos, Cambodia, Thailand, Central and northern Burma, northeastern India (Sikkim, northwestern Bengal, Arunachal Pradesh, Nagaland, and Meghalaya), Bhutan, and Nepal but was not recorded from the mainland of peninsular Thailand south of the Isthmus of Kra. It is discussed under R. remotus by Corbet & Hill (1992), who noted that remotus is an older name than sikkimensis. South Vietnamese samples have also been treated as R. sladeni (Van Peenen et al., 1969), Northern Vietnamese samples as R. koratensis (Dao, 1978a), and Thai samples under R. koratensis and R. remotus (Marshall, Jr., 1977). According to our long-term research, in most areas of Vietnam it is one of the persistent species of the forest fauna (Balakirev & Rozhnov 2012), often hybridizing with co-occurring synanthropic species (Ge et al. 2018). Eighteen individuals of this species were caught in a number of localities, mainly near settlements on both banks of the Da River.
Rattus tanezumi Temminck, 1844
Genus: Mus Linnaeus, 1758.
Mus cookie Ryley, 1914
This synanthropic species is widely distributed in south and southeast Asia from India to Vietnam. It occurs in many regions of Vietnam and inhabits fields, shrubs, grasslands, and agricultural areas (Lunde & Nguyen 2001, Dang et al. 2008, Aplin et al. 2008). Six specimens were caught from two location in the northeast bank of the Da River, but there is every reason to believe that they occur on the southwest bank, as follows from our own unpublished data and from Kuznetzov (2006) based on ZMMU museum collection.
Mus (Coelomys) pahari Thomas, 1916
Genus: Niviventer (Marshall, Jr., 1976)
Niviventer mekongis (Robinson & Kloss, 1922)
For a long time, the species was considered part of Niviventer fulvescens, understood in broad and not always strictly defined limits (Pavlinov 1995, 2003, Lunde & Nguyen 2001, Musser & Carleton 2005, Dang et al. 2008). The recent taxonomic review based on morphological and molecular analyses (Balakirev et al. 2012) revealed in Vietnam two morphologically similar but genetically distinct species attributed to N. huang and N. fulvescens proper. The authors stated that N. huang is widely distributed throughout Indochina, whereas N. fulvescens occurs in the northern part of Vietnam and southern China only. Later, as a result of extensive genetic studies by Chinese authors, it was established that the nomen huang should be applied only to populations inhabiting the southeastern coastal provinces of China, while the Indochinese populations were identified as a separate species, N. mekongis (Ge et al. 2020).
A number of specimens of mekong white-bellied rats were collected from the forest sites located at the southeast bank of the river but not on the northern side. Today, the location with coordinates 21.174084N, 104.352508E (Ta Khoa commune, O Bo village) can be considered the northernmost genetically confirmed distribution point for this species. On the opposite bank of the Da River, this species was not found among many dozens of Niviventer specimens.
Niviventer fulvescens (Gray, 1847)
In reviews of the fauna of Vietnam, Indochina, and southeast Asia, this name was used for a whole group of what are now separate species of the genus (Corbet & Hill 1992, Musser and Carleton 1993, 2005, Dang et al. 2008, Francis 2008, Smith and Xie 2008). At present, the species is limited in its distribution to populations inhabiting mountainous regions and foothills of the Himalayas, Tibet, Qinghai, and Yunnan, and the northwestern provinces of Vietnam, where it inhabits almost exclusively mountain forest ecosystems. In Vietnam, we have previously recorded this species in the Sapa region, Lao Cai province (Balakirev et al. 2012), as well as in the provinces of Dien Bien and Son La and in the Xuan Son National Park (Balakirev 2022). In the study area, more than a dozen individuals were obtained from localities situated on the northeastern bank of the Da River. Thus, the study area can be considered one of the extreme southern points where this species has been reliably documented. Based on our data, N. fulvescens does not cross the Da River, but is replaced south of the river by the vicarious species N. mekongis.
Niviventer lotipes (G. M. Allen, 1926)
Genus: Chiromyscus Thomas, 1925
Chiromyscus thomasi Balakirev, Abramov, & Rozhnov, 2014
Genus: Leopoldamys Ellerman, 1947–1948
Leopoldamys edwardsi (Thomas, 1882)
Rats of the genus Leopoldamys are widely distributed in Vietnam; they are common terrestrial rats that inhabit lowland and montane forests (Dang et al. 1994, Lunde & Nguyen 2001, Dang et al. 2008, Smith & Xie 2008). This taxon requires taxonomic revision (Lunde & Nguyen 2001, Musser & Carleton 2005). Recent studies have established that L. edwardsi, in fact, does not represent a monotypic taxon but a species complex, with at least three genetic species (Li et al. 2019). The limits of the genetic species have not yet been established, and the species themselves have not received a formal description; therefore, here we use a common name, which should be understood as L. edwardsi sensu lato. This rat is common in the study area and in northern Vietnam in general (Balakirev et al. 2013), where it may coexist with its congeners, L. neilli and L. herberti. We collected five specimens in three sites from both banks of the Da River.
Leopoldamys herberti (Kloss, 1916)
Genus: Berylmys (Ellerman, 1947)
Berylmys bowersi (Anderson, 1879)
Family: Cricetidae Fischer, 1817.
Subfamily: Arvicolinae Gray, 1821.
Genus: Eothenomys Miller, 1896.
Eothenomys miletus Thomas, 1914
The Yunnan red-backed vole is a member of the melanogaster species group, and is its largest-bodied species (Kaneko et al. 1996). The species was initially described as a subspecies of E. melanogaster, a placement commonly recognized throughout the 1900s but later regarded as a distinct species (G. M. Allen 1940, Corbet & Hill 1992, Zhang et al. 1997, Ye et al. 2002). Eothenomys miletus in Yunnan may occur in the same regions as E. melanogaster but is usually larger in body size and cranial dimensions with a strikingly higher cranium; a tawny brown to reddish brown dorsal coat that is soft, thick, and long (shorter coat, velvety in texture, dark brown to melanistic in most melanogaster); and gray underparts either frosted or washed with brown to ochraceous hues (stark slate gray in melanogaster, infrequently washed with brown or buff). Specimens of E. melanogaster are generally small-bodied with small skulls, have dark brown to blackish upperparts, slate gray underparts (washed with buff or brown in some specimens), and possess a short to medium tail (21–42 mm) relative to body length. Cranial size varies geographically, with specimens from Sichuan and Yunnan being smaller on average than those from eastern China, Burma, northern Thailand, and northwestern Vietnam. Three lingual salient angles on each M3 were considered to be typical for E. melanogaster (G. M. Allen, 1940, Corbet & Hill, 1992, Musser and Carleton, 2005), but the number of lingual angles varies within the species (Kaneko 2002). Many E. miletus possess four lingual angles; of 71 specimens from Yunnan and Sichuan (AMNH, FMNH), 64 have four angles, but seven exhibit only three (Musser & Carleton 2005). It should be noted that all specimens lately investigated from northern Thailand and northwestern Vietnam had four lingual angles as specially noticed for exactly E. miletus (Allen, 1940, Musser & Carleton, 2005, Ye et al., 2002). Taxonomic significance of the variation in M3 lingual angles, tail length, and cranial size, as outlined here and discussed by Kaneko (2002), should be assessed by morphometric and molecular analyses.
Based on recent genetic data, the species status of E. miletus is beyond doubt, with debates only regarding its boundaries. Throughout the history of research in Vietnam, only one species of the genus Eothenomys has been recorded, namely E. melanogaster. It appears in all faunal reports (Cao 1998, Dang et al. 1994, 2008, Kuznetsov 2006, Lunde & Nguyen 2001), with Sapa, Lao Cai Province, as the only location with museum specimens from Vietnam to date (Osgood 1932). Only nine specimens are stored at the American Museum of Natural History (AMNH) and at the Fields Museum of Natural History (FMNH); other specimens from the same locality are available at the Institute of Zoology Museum, Saint-Petersburg (ZIN) (A.V. Abramov, pers comm), all attributed to E. melanogaster. We received another six individuals (three males and three females) from Ta Xua Nature Reserve, Xim Vang commune, Suong Chong village (21.319964N, 104.408068E), at about 2000 m. a.s.l. (Fig. 1). Thus, our data represent the second documented point of discovery of Eothenomys in Vietnam and the southernmost for the genus.
As shown by the analysis of mitochondrial genes, our samples belong to a species not previously recorded in Vietnam, namely Eothenomys miletus. Genetic distances for the cytochrome b gene between our samples and samples of the same species from Yunnan are 0.0219 (K2P), while the distance from E. melanogaster reaches 0.0788 (K2P). Morphometric features of the individuals are also consistent with such a species attribution. The external dimensions of the five individuals are HB 99–110 mm; TL 40–45 mm; FL 17–18 mm; EL 10–13 mm; W 20.7–27.9 g. These dimensions are within the limits characteristic for the species; of particular note is the relatively short tail (HL 46–59 mm, ratio 0.44–0.55 for E. melanogaster) and four lingual angles on M3. Also noteworthy are the relatively large (5.64–6.37 mm in length) auditory bullae and cranium height (height of brain case is 8.17–8.41 mm). Both features are also characteristic for E. miletus (Kaneko, 2002).
Family: Platacanthomyidae Alston, 1876
Genus: Typhlomys Milne-Edwards, 1877
Eothenomys miletus, museum voucher ZMMU S-210253 (Zoological Museum of Moscow State University), field number BY-69, adult, female. Origin: Ta Xua Nature Reserve, Bac Yen district, Son La Province, Vietnam. A: Dorsal view, B: Ventral view, C: Lateral view, D: Lower jaw, dorsal view, E: Lower jaw, lateral view, F: Right upper molar row, G: Right lower molar row
Citation: Animal Taxonomy and Ecology 71, 1; 10.1556/1777.2025.00056
Typhlomys taxuansis Balakirev et al. 2024
The type species of the genus, Typhlomys cinereus, was described from Fujian, China, and is known to occur over a fairly large range in central China (Hong et al. 1982, Wang et al. 1996, Smith 2008, Cheng et al. 2017). The Vietnamese population was initially described by Osgood (1932) as a separate species, T. chapensis, which had long been considered a subspecies of T. cinereus (Corbet and Hill, 1992, Wang et al., 1996, Musser & Carleton, 2005) until we restored its taxonomic status (Abramov et al. 2014). A recent study (Cheng et al. 2017) carried out the first successful revision of the genus based on a combination of morphological and molecular data. It was demonstrated that T. chapensis and T. c. jingdongensis are actually the same species. In a subsequent series of surveys (Hu et al. 2021, Pu et al. 2022), another species was described, along with two more genetic lineages of species rank that do not yet have a formal description. The only species of Typhlomys recorded from Vietnam was T. chapensis from Sapa, Lao Cai province.
Family: SCIURIDAE Fischer de Waldheim, 1817
Subfamily: Callosciurinae Pocock, 1923
Genus Tamiops Allen, 1906
Tamiops maritimus (Bonhote, 1900)
The Eastern striped squirrel is one of the common squirrel species found widely in Vietnam and southeastern China. It occurs in southern and eastern China (including Hainan) and Taiwan, in Laos and in Vietnam east of the Mekong River (Thorington & Hoffman 2005, Thorington et al. 2012, Duckworth 2017). This species is listed for many provinces of northern Vietnam (Dang et al. 2008). We obtained two individuals from commune Ta Khoe, three km west from Suoi He on the southwestern bank of the Da River.
Tamiops swinhoei (Milne-Edwards, 1874)
Genus: Dremomys Heude, 1898.
Dremomys ornatus Thomas, 1914
The Northern Indochinese red-cheeked squirrel is a taxon that has recently regained the species rank (Balakirev et al. 2022). For over a century, it was considered a subspecies of D. rufigenis and appears under this rank in all taxonomic reviews (Corbet & Hill 1992, Kuznetsov 2006, Lunde & Nguyen 2001, Dang et al. 2008, Thorington & Hoffmann 2005, Thorington et al. 2012). It is widely distributed throughout northern Indochina, including Vietnam, Laos, and the southern provinces of China. It is a species that is quite abundant over most of its range. During our work, one individual was captured in the Ta Xua Nature Reserve, four kilometers east of Y Xoa Homestay on the northeastern bank of the Da River. According to our data (BAE, unpublished), there is no reason to assume its absence in areas further south. This species has been repeatedly recorded by us in the provinces of Thanh Hoa, Nghe An, Quang Binh, and other more southern areas.
Dremomys gularis Osgood, 1932
Genus: Callosciurus Gray, 1867.
Callosciurus erythraeus (Pallas, 1779)
The Pallas squirrel is widely distributed in China (Smith and Xie 2008) and Vietnam (Dang et al. 1994, 2008). According to our more recent data based on genetic studies, this species is distributed in Vietnam south to Thanh Hoa Province (Balakirev & Rozhnov 2019). Generally, this is one of the most common squirrel species in northern Vietnam. We obtained one specimen from a mixed forest in Xa Hua Nhan, village Suoi Chai. These squirrels have an olivaceous-gray dorsum and deep reddish-brown ventrum; their tails are grizzled olivaceous-brown with silver guard hairs toward the tip. This pattern is consistent with subspecies or color form C. e. hendeei Osgood, 1932. Although no specimens of this species were obtained from the southwestern bank of the Da River during the recent survey, it is clear that this species crosses the river and spreads far to the south.
Many patterns in the geographic distribution of small mammals can be explained based on the refugial model of species evolution. The refugia hypothesis states that animal populations at low elevations are reduced when available habitats decreased during cold episodes in the Pleistocene (Haffer 1969, Heaney 1986, Cracraft & Prum 1988, Cox & Moore 2005) and repeatedly increased with considerable expansion during warm interglacials. In Indochina, reduction and expansion of forests, especially mountain forests, could have affected phylogeographic patterns in many species of mammals (Heuertz et al. 2010, Latinne et al. 2015, Stefenon et al. 2019). The possibilities of range expansion, in turn, are determined primarily by the location of barriers. The largest and most obvious of these barriers may be the large and ever-flowing rivers, which determine some of the phylogeographic patterns of mammals in tropical regions (Salo et al. 1986, MacKinnon et al. 1996, Patton et al. 1996, Endo et al. 2000, Meijaard 2003, Meijaard & Groves 2006, Woodruff & Turnner 2009). However, this model is not confirmed in relation to the Da River. In many ways, the fauna of the areas between Ca and Da Rivers should be considered as mixed communities Abramov (2017).
With regard to the role of lowland rivers as biogeographic boundaries, it should be recognized that it is not so much the river itself that is important as a geographic barrier. This is so because lowland rivers change their course over a fairly large range by meandering and avulsing (sudden change of channel location) over geological time scales, ensuring regular contact between populations along their banks. It is the ecosystems and communities that the rivers can delimit, which shape species distributions. In particular, the species diversity of the forest ecosystems of the Yunnan mountains is considerably greater than that of the lowland and plain ecosystems in the same region (Wang 1939, Cao and Zhang 1997, Zheng et al. 2006a, 2006b, Zhu et al. 2006). This circumstance should also be reflected in the structure of animal communities living in these ecosystems and subsisting on their resources (Wang and Jin 1987). The isolating effect of ecological mechanisms within an established community of species in its resistance to attempts of invasive species from outside is much stronger and more long-term than that of geographic barriers, such as rivers. That is why strong biogeographic boundaries are maintained not only by geographic barriers but by the stability of ecosystems and communities. The importance of this factor, unfortunately, is often underestimated by researchers, who often mechanically apply certain climatic models (for example, MaxEnt) to explain the distribution of species without taking into account changes in the structure of communities.
Several studies have shown that barriers created by rivers, can explain some species divergences, such as between bonobos (Pan paniscus) and chimpanzees (P. troglodytes) (Gonder et al., 2011), tamarins (Saguinus fuscicollis) (Peres et al., 1996) or some groups of rodents (e.g. Praomys; Kennis et al., 2011). However, the estimated timing of speciation events may well be inconsistent within and between clades (Jongsma et al. 2018), which may be related to the highly dynamic nature of river basins and the significant changes in their flows in some regions of the Earth during the Cenozoic (Goudie 2005).
To test whether rivers act as an effective barrier to gene flow in animals, several intraspecific studies of genetic variation have also been conducted within taxa occurring on both sides of large rivers (Patton et al. 1994, 1996, Anthony et al. 2007, Nicolas et al. 2011, Olayemi et al. 2012, Jacquet et al. 2014, Bell et al. 2017, Huntley et al. 2019). The results obtained are contradictory. For example, rivers were not found to be important barriers for a number of frog species (Epipedobates, Lougheed et al. 1999, Hyperolius, Bell et al., 2017); Chiromantis rufescens (Leache et al., 2019) some mammals (Patton et al. 1994) or the common pangolin Manis tricuspis (Gaubert et al., 2018). In contrast, rivers evidently formed intraspecific barriers in several other animal groups, including mammals (Nicolas et al. 2011, Guschanski et al. 2013, Jacquet et al. 2014, Huntley et al. 2019, Mizerovska et al. 2019), reptiles (Leache & Fujita 2010) and some bird groups (Huntley et al. 2018, 2019).
In general, in vertebrates, river systems can apparently be important barriers limiting the distribution of some modern species, but not from the point of view of biogeographical zoning (Colyn et al. 1991, Louette 1992, Katuala et al. 2008, Nicolas et al. 2011, Kennis et al. 2011). This is apparently due to the difference in the rates of speciation characteristics of lowland and mountain ecosystems (Patton et al. 1994, Gascon et al. 2000, Patton et al. 2000) or in cooperative influence of ecological and geographical factors (da Silva and Patton 1998). This is exactly the case also in northern Indochina, where rivers do not separate wide lowland areas, but mountain systems and ridges. To describe evolutionary processes in these conditions, a special mountain-geobiodiversity hypothesis was developed (Mosbrugger et al. 2018, Muellner-Riehl 2019). The hypothesis states that (1) steep environmental gradients along altitudinal zones allow adaptation and ecological speciation of species to new environments or immigration of preadapted taxa; (2) climatic variations leading to cycles of population separation and reunification may stimulate allopatric speciation through vicariance; and (3) there is a lower risk of local extinction under climate change (compared to lowland species) because changes in temperature and precipitation regimes can be compensated for by altitudinal shifts requiring limited horizontal displacement (Fjeldsa et al. 2012, Mosbrugger et al. 2018). All three processes significantly accelerate allopatric speciation processes compared to the riverine model and result in the formation of a series of montane endemics. This is exactly the situation we find in our study area.
Conclusions
Summarizing the data on the distribution of individual species of small mammals presented above, it should be noted that of the 21 species directly recorded in the study area, the role of the Da River as a biogeographic barrier is supported for only seven species, based on the available data on the actual distribution of the species. Of these seven, the majority are characteristic endemics of the mountains of southern China, having the southern border of their distribution here. For squirrels of the genera Dremomys and Callosciurus, the southern boundary runs significantly further south (Balakirev & Rozhnov 2019, Balakirev et al. 2021); for rats of the genera Niviventer, Leopoldamys, and Chiromyscus, there are extensive areas of sympatry both south and east of the Da River basin (Balakirev et al. 2013, 2014, 2021); most species of the genera Rattus, Berylmys, and Bandicota are either synanthropic or have a significantly wider distribution, extending far beyond the region. Other large genera, such as Mus, Chiromyscus, Tamiops, Hylopetes, Petaurista, show an even more complex pattern of distribution. Thus, it should be inferred that the limits of their distribution are not the river as such, but the mountain ecosystems and forest communities of the upper altitudinal belt, that is, the spurs of the Hoang Lien Son Ridge, not the Da River. This is clearly visible on the height map, Fig. 1A. This can explain the fact that the strong correspondence of geographic distribution ranges with the river system is most often demonstrated by mountain endemics of Yunnan. Based on the results obtained, it can be confidently stated that the river model and the biogeographic boundaries drawn on its basis are generally not relevant for the northern part of Indochina.
Acknowledgements
This study was realized with the support of the Joint Vietnam-Russia Tropical Science and Technology Research Centre, Hanoi, Vietnam. We thank the local authorities of the Bac Yen District of Son La Province, Vietnam, for accompanying us in our surveys, and Dr. Sergei V. Kruskop and Ms. Yulia A. Ermilina (from the Zoological Museum of Moscow State University, Moscow, Russia) for giving access to the collections under their care. We also thank Dr. Dinh The Dung and Dr. Tran Huu Coi (both from the Joint Vietnam-Russia Tropical Science and Technology Research Centre, Hanoi, Vietnam), who put considerable effort into the expedition preparations. The maps were composed with a help of Pham Mai Phuong MD from the same organisation. We are also very grateful to Dr. Attila Hettyey and two reviewers for their helpful and constructive comments on an earlier version of the manuscript.
References
Aplin K, Lunde D, Molur S (2008) Mus cookii. The IUCN Red List of Threatened Species 2008:e.T13958A4371393. Available at: https://doi.org/10.2305/IUCN.UK.2008.RLTS.T13958A4371393.en [Accessed 13 Jan 2025].
Abramov AV (2017) Insectivorous mammals of Vietnam (Systematics, fauna, zoogeography). Theses of Doctor of biological Sciences. Sankt-Petersburg. 368 p. (in Russian).
Abramov AV, Balakirev AE, Rozhnov VV (2014) An enigmatic pygmy dormouse: Molecular and morphological evidence for the species taxonomic status of Typhlomys chapensis (Rodentia: Platacanthomyidae). Zoological Studies 53: 34. https://doi.org/10.1186/s40555-014-0034-2
Abramov AV, Dang NC, Bui TH, Nguyen TS (2013) An annotated checklist of the insectivores (Mammalia, Lipotyphla) of Vietnam. Russian Journal of Theriology 12(2): 57–70. https://doi.org/10.15298/rusjtheriol.12.2.01
Abramov AV, Jenkins PD, Rozhnov VV, Kalinin AA (2008) Description of a new species of Crocidura (Soricomorpha: Soricidae) from the island of Phu Quoc, Vietnam. Mammalia 72(4): 269–272. https://doi.org/10.1515/MAMM.2008.033
Agrawal VC (2000) Taxonomic studies on Indian Muridae and Hystricidae (Mammalia: Rodentia). Records of the Zoological Survey of India 180: 1–177.
Allen GM (1938–1940) The mammals of China and Mongolia [Natural history of Central Asia (W. Granger, ed.)]. Central Asiatic Expeditions of the American Museum of Natural History, New York, 11: pt. 1: 1–620[1938]; pt. 2:621–1350[1940].
Anthony NM, Johnson-Bawe M, Jeffery K, Clifford SL, Abernethy KA, Tutin CE, et al. (2007). The role of Pleistocene refugia and rivers in shaping gorilla genetic diversity in Central Africa. Proceedings of the National Academy of Sciences of the United States of America 104: 20432–20436.
Averyanov LV, Phan KL, Nguyen TH, Harder DK (2003) Phytogeographic review of Vietnam and adjacent areas of Eastern Indochina. Komarovia 3: 1–83.
Balakirev AE (2022) New occurrence records on the rodent’s species inhabits Vietnam based on Joint Russian-Vietnamese Tropical Research and Test Center genetic samples collection. Biodiversity Data Journal 10: e96062. https://doi.org/10.3897/BDJ.10.e96062
Balakirev AE, Abramov AV, Phuong BX, Rozhnov VV (2022) Natural diversity and phylogeny of Asian red-cheeked squirrels (Rodentia, Sciuridae, Dremomys) in Eastern Indochina. Biology Bulletin 49(1): 81–94. https://doi.org/10.1134/S1062359022010046
Balakirev AE, Abramov AV, Rozhnov VV (2012) Taxonomic revision of Niviventer (Rodentia, Muridae) from Vietnam: A morphological and molecular approach. Russian Journal of Theriology 10(1): 1–26. http://zmmu.msu.ru/rjt/articles/ther10_1_01_26_Balakirev.pdf
Balakirev AE, Abramov AV, Rozhnov VV. (2014) Phylogenetic relationships in the Niviventer-Chiromyscus complex (Rodentia, Muridae) inferred from molecular data, with description of a new species. ZooKeys 451: 109–136. https://doi.org/10.3897/zookeys.451.7210
Balakirev AE, Abramov AV, Rozhnov VV (2021) Distribution pattern and phylogeography of tree rats Chiromyscus (Rodentia, Muridae) in eastern Indochina. Zoosystematics and Evolution 97(1): 83–95. https://doi.org/10.3897/zse.97.57490
Balakirev AE, Aniskin VV, Tran QT, Rozhnov VV (2013) The taxonomic position of Tonkinomys daovantieni (Rodentia: Muridae) based on karyological and molecular data. Zootaxa 3734(5): 536–544. https://doi.org/10.11646/zootaxa.3734.5.3
Balakirev AE, Bui XP, Pham MP, Rozhnov VV (2011) On taxonomic status of Pseudoberylmys muongbangensis new species and genus described from Son La Province, Vietnam; Does it new or pseudo-new species? 2011. In: Proceedings of 4th national scientific conference on ecology and biological resources (pp. 11–19). Hanoi, 22 October 2011.
Balakirev AE, Bui XP, Rozhnov VV (2023) New data on the distribution and diversity of the little-studied rodent of the Tonkin limestone rat (Tonkinomys daovantieni, Rodentia, Muridae). Biodiversity Data Journal 11: e110350. https://doi.org/10.3897/BDJ.11.e110335
Balakirev AE, Bui XP, Rozhnov V (2024) Typhlomys taxuansis (Rodentia, Platacanthomyidae): New species of the genus from northern Vietnam with notes on conservation status and distribution. Biodiversity Data Journal 12: e133363. https://doi.org/10.3897/BDJ.12.e133363
Balakirev AE, Rozhnov VV (2012) Contribution to the species composition and taxonomic status of some Rattus inhabiting Southern Vietnam and Sundaland. Russian Journal of Theriology 11(1): 33–45.
Balakirev AE, Rozhnov VV (2019) Taxonomic revision of beautiful squirrels (Callosciurus, Rodentia: Sciuridae) from the Callosciurus erythraeus/finlaysonii complex and their distribution in eastern Indochina. Raffles Bulletin of Zoology 67: 459–489. https://doi.org/10.26107/RBZ-2019-0037
Bannikova AA, Lebedev VS, Abramov AV, Rozhnov VV (2014) Contrasting evolutionary history of hedgehogs and gymnures (Mammalia: Erinaceomorpha) as inferred from a multigene study. Biological Journal of the Linnean Society 112(3): 499–519. https://doi.org/10.1111/bij.12299
Bell RC, Parra JL, Badjedjea G, Barej MF, Blackburn DC, Burger M, et al. (2017). Idiosyncratic responses to climate-driven forest fragmentation and marine incursions in reed frogs from Central Africa and the Gulf of Guinea Islands. Molecular Ecology 26: 5223–5244.
Bobrov VV (1993) Zoogeographical analyses of lizard’s fauna (Reptilia, Sauria) of Vietnam. Zoologicheskiy Zhurnal 72(8): 70–79 (in Russian).
Cao VS (1989) On the problem of zoogeographical division of the rodent fauna of Vietnam (Mammalia, Rodentia). Vertebrata Hungarica 23: 57–66.
Cao VS (ed.) (1998) Environment and bioresources of Vietnam present situation and solutions. The Gioi Publishers, Hanoi, 235 pp.
Cao M, Zhang JH (1997) Tree species diversity of tropical forest vegetation in Xishuangbanna, SW China. Biodivers. Conserv 6: 995–1006.
Cheng F, He K, Chen Z-Z, Zhang B, Wan T, Li J-T, et al. (2017) Phylogeny and systematic revision of the genus Typhlomys (Rodentia, Platacanthomyidae), with description of a new species. Journal of Mammalogy 98(3): 731–743. https://doi.org/10.1093/jmammal/gyx016
Colyn M, Gautier-Hion A, Verheyen W (1991). A re-appraisal of palaeoenvironmental history in Central Africa: Evidence for a major fluvial refuge in the Zaire Basin. Journal of Biogeography 18, 403–407.
Corbet GB, Hill JE (1992) The mammals of the Indomalayan region: A systematic review. Oxford University Press, Oxford, 488 pp.
Cox CB, Moore PD (2005) Biogeography: An ecological and evolutionary approach. 7th edition. Blackwell Publishing Ltd, Oxford, 488 pp.
Cracraft J, Prum RO (1988) Patterns and processes of diversification: Speciation and historical congruence in some neotropical birds. Evolution 42: 603–620. https://doi.org/10.1111/j.1558-5646.1988.tb04164.x
Dang HH, Dao VT, Cao VS, Pham TA, Hoang MK (1994) Checklist of mammals in Vietnam. Publishing House “Science & Technics”, Hanoi, 168 pp. (in Vietnamese).
Dang NC, Endo H, Nguyen TS, Oshida T, Le XC, Dang HP, et al. (2008) Checklist of wild mammal species of Vietnam. Institute of Ecology and Biological Resources, Hanoi, 400 pp. (in Vietnamese).
Dao VT (1978a) Sur une collection de mammiferes du plateau de Мос Chau, Nord Vietnam. Mitteilungen aus dem Zoologischen Museum in Berlin 54(2): 377–391. (In French).
Dao VT (1978b) Experience of zoogeographical zoning of Vietnam. Zoologicheskiy Zhurnal 57(4): 582–586 (in Russian).
Duckworth JW (2017) “Tamiops maritimus”. IUCN Red List of Threatened Species. 2017: e.T21380A22252211. https://doi.org/10.2305/IUCN.UK.2017-2.RLTS.T21380A22252211.en
Endo H, Nishiumi I, Hayashi Y, Rashdi ABM, Nadee N, Nabhitabhata J, et al. (2000) Multivariate analysis in skull osteometry of the common tree shrew from both sides of the Isthmus of Kra in southeastern Thailand. Journal of Veterinary Medical Science 62: 375–378. https://doi.org/10.1292/jvms.62.375
Feiler A, Nadler T, Stefen C (2008) Bemerkungen zu Kleinsäugern der vietnamesischen Nationalparke Cuc Phuong und Phong Nha-Ke Bang und des Naturschutzgebietes Ke Go. Vertebrate Zoology 58(1): 113–125 (In German).
Fjeldsa J, Bowie RCK, Rahbek C (2012). The role of mountain ranges in the diversification of birds. Annual Review of Ecology, Evolution, and Systematics 43: 249–265.
Fooden J (1996) Zoogeography of Vietnamese primates. International Journal of Primatology 17(5): 845–899.
Francis CM (2008) A guide to the mammals of Southeast Asia. Princeton University Press, Princeton and Oxford, 392 pp.
Gascon C, Malcolm JR, Patton JL, da Silva MN, Bogart JP, Lougheed SC, et al. (2000) Riverine barriers and the geographic distribution of Amazonian species. Proc Natl Acad Sci U S A 97(25): 13672–13677. https://doi.org/10.1073/pnas.230136397
Ge D, Lu L, Abramov AV, Wen Z, Cheng J, Xia L, et al. (2019) Coalescence models reveal the rise of the white-bellied rat (Niviventer confucianus) following the Loss of Asian Megafauna. Journal of Mammalian Evolution 26: 423–434. https://doi.org/10.1007/s10914-018-9428-y
Ge D, Lu L, Xia L, Du Y, Wen Z, Cheng J, et al. (2018) Molecular phylogeny, morphological diversity, and systematic revision of a species complex of common wild rat species in China (Rodentia, Murinae). Journal of Mammalogy 99(6): 1350–1374. https://doi.org/10.1093/jmammal/gyy117
Ge DY, Feijo A, Abramov A, Wen ZX, Liu ZJ, Cheng JL, et al. (2020) Molecular phylogeny and morphological diversity of the Niviventer fulvescens species complex with emphasis on species from China. Zoological Journal of the Linnean Society 191(2): 528–547. https://doi.org/10.1093/zoolinnean/zlaa040
Gaubert P, Antunes A, Meng H, Miao L, Peigne S, Justy F, et al. (2018) The complete phylogeny of pangolins: Scaling up resources for the molecular tracing of the most trafficked mammals on earth. Journal of Heredity 109: 347–359.
Gonder MK, Locatelli S, Ghobrial L, Mitchell MW, Kujawski JT, Lankester FJ, et al. (2011) Evidence from Cameroon reveals differences in the genetic structure and histories of chimpanzee populations. Proceedings of the National Academy of Sciences of the United States of America 108: 4766–4771.
Goudie AS (2005) The drainage of Africa since the cretaceous. Geomorphology 67: 437–456.
Guschanski K, Krause J, Sawyer S, Valente LM, Bailey S, Finstermeier K, et al. (2013) Next-generation museomics disentangles one of the largest primate radiations. Systematic Biology 62: 539–554.
Haffer J (1969) Speciation in Amazonian forest birds. Science 165: 131–137. https://doi.org/10.1126/science.165.3889.131
Heaney LR (1986) Biogeography of mammals in SE Asia: Estimates of rates of colonization, extinction and speciation. Biological Journal of the Linnean Society 28: 127–165.
Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B 270: 313–321. https://doi.org/10.1098/rspb.2002.2218
Heuertz M, Teufel J, González-Martínez SC, Soto A, Fady B, Alía R, et al. (2010) Geography determines genetic relationships between species of mountain pine (Pinus mugo complex) in western Europe. Journal of Biogeography 37: 541–556. https://doi.org/10.1111/j.1365-2699.2009.02223.x
Holt BG, Lessard JP, Borregaard MK, Fritz SA, Araújo MB, Dimitrov D, et al. (2013) An update of Wallace’s zoogeographic regions of the world. Science 339: 74–78. https://doi.org/10.1126/science.1228282
Hong ZF (1982) Redescription of Typhlomys cinereus Milne-Edward, with a note on its ecology (muscardinidae). Wuyi Science Journal 2(1): 103–107 (in Chinese).
Hu TL, Cheng F, Xu Z, Chen ZZ, Yu L, Ban Q, et al (2021) Molecular and morphological evidence for a new species of the genus Typhlomys (Rodentia: Platacanthomyidae). Zoological Research 42(1): 100–107. https://doi.org/10.24272/j.issn.2095-8137.2020.132
Huntley JW, Harvey J, Pavia M, Boano G, Voelker G (2018) The systematics and biogeography of the bearded Greenbuls (Aves: Criniger) reveals the impact of Plio-Pleistocene forest fragmentation on afro-tropical avian diversity. Zoological Journal of the Linnean Society 183: 672–686.
Huntley JW, Keith KD, Castellanos AA, Musher LJ, Voelker G (2019) Underestimated and cryptic diversification patterns across afro-tropical lowland forests. Journal of Biogeography 46: 381–391.
Hutterer R (2005) Order erinaceomorpha. pp. 212–219. In: Wilson D, Reeder DM (eds): Mammal species of the world. Vol. 1. 3rd edition. Johns Hopkins University Press, Baltimore.
Irwin D, Kocher TD, Wilson AS (1991) Evolution of the cytochrome b gene of mammals. Journal of Molecular Evolution 32: 128–144.
Jacquet F, Nicolas V, Colyn M, Kadjo B, Hutterer R, Decher J, et al. (2014) Forest refugia and riverine barriers promote diversification in the west African pygmy shrew (Crocidura obscurior complex, Soricomorpha). Zoologica Scripta 43: 131–148.
Jongsma GFM, Barej MF, Barratt CD, Burger M, Conradie W, Ernst R, et al. (2018) Diversity and biogeography of frogs in the genus Amnirana (Anura: Ranidae) across sub-Saharan Africa. Molecular Phylogenetics and Evolution 120: 274–285.
Kaneko Y (1996) Morphological variation, and latitudinal and altitudinal distribution of Eothenomys chinensis, E. wardi, E. custos, E. proditor, and E. olitor (Rodentia, Arvicolidae) in China. Mammal Study 21(2): 89–114.
Kaneko Y (2002) Morphological variation and geographical and altitudinal distribution in Eothenomys melanogaster and E. mucronatus (Rodentia, Arvicollinae) in China, Taiwan, Burma, India, Thailand, and Vietnam. Mammal Study 27: 31–63.
Katuala PGB, Kennis J, Nicolas V, Wendelen W, Hulselmans J, Verheyen E, et al. (2008) The presence of Praomys, Lophuromys, and Deomys species (Muridae, Mammalia) in the forest blocks separated by The Congo River and its tributaries (Kisangani region, Democratic Republic of Congo). Mammalia 72: 223–228.
Kennis J, Nicolas V, Hulselmans J, Katuala PGB, Wendelen W, Verheyen E, et al. (2011). The impact of The Congo River and its tributaries on the rodent genus Praomys: Speciation origin or range expansion limit? Zoological Journal of the Linnean Society 163: 983–1002.
Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablanca F, et al. (1989) Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proceedings of National Academy of Sciences (USA) 86: 6196–6200. https://doi.org/10.1073/pnas.86.16.6196
Krivolutskiy DA, Ogureeva GN, Huynh KH (1995) Palearctic elements in the mountain forest ecosystems of Northern Vietnam. Bulletin of Moscow State University, Geography 5(6): 53–59 (in Russian).
Kuznetsov GV (2006) Mammals of Vietnam. KMK Scientific Press, Moskva, 428 pp. (in Russian).
Kuznetsov GV, Pham TA (1992) Mammals of the Coastal Islands of Vietnam (Biogeographical and ecological aspects). pp. 182–197. In: Sokolov (ed.): Zoological Studies in Vietnam. Nauka Publ., Moscow (in Russian).
Kuznetsov GV, Rozhnov VV (1998) Mammals of Shapa and the Phan Xi Pang Mountain range: Species diversity and problems of its conservation. pp. 129–158. In: Korzun LP, Kalyakin M (eds): Materials of zoological and botanical studies in the Phan Xi Pang Mountain range (Northern Vietnam). Tropcentr., Moscow, Hanoi (in Russian).
Latinne A, Chaval Y, Waengsothorn S, Rojanadilok P, Eiamampai K, Sribuarod K, et al. (2013). Is Leopoldamys neilli (Rodentia, Muridae) a synonym of Leopoldamys herberti? A reply to Balakirev et al. (2013). Zootaxa 3731: 589–598. https://doi.org/10.11646/zootaxa.3731.4.10
Latinne A, Meynard CN, Herbreteau V, Waengsothorn S, Morand S, Michaux JR (2015) Influence of past and future climate changes on the distribution of three Southeast Asian murine rodents. Journal of Biogeography 42: 1714–1726. https://doi.org/10.1111/jbi.12528
Leache AD, Fujita MK (2010) Bayesian species delimitation in west African forest geckos (Hemidactylus fasciatus). Proceedings of the Royal Society B: Biological Sciences 277: 3071–3077.
Leache AD, Portik DM, Rivera D, Rodel M-O, Penner J, Gvozdik V, et al. (2019) Exploring rain forest diversification using demographic model testing in the African foam-nest treefrog Chiromantis rufescens. Journal of Biogeography 46: 2706–2721.
Li H, Kong L, Wang K, Zhang S, Motokawa M, Wu Y, et al. (2019) Molecular phylogeographic analyses and species delimitations reveal that Leopoldamys edwardsi (Rodentia: Muridae) is a species complex. Integrative Zoology 5: 494–505. https://doi.org/10.1111/1749-4877.12378
Li Y, Wu Y, Harada M, Lin LK, Motokawa M (2008) Karyotypes of three rat species (Mammalia: Rodentia: Muridae) from Hainan Island, China, and the valid specific status of Niviventer lotipes. Zoological Science 25: 686–692. https://doi.org/10.2108/zsj.25.686
Liu, C, Li C, Wu W, Meng J (1985) The faunal distribution and geographical divisions of rodents in Anhui Province. Acta Theriologica Sinica 5: 111–118.
Louette M (1992) Barriers, contact zones and subspeciation in central equatorial Africa. Bulletin of the British Ornithologists’ Club 122A: 209–216.
Lougheed SC, Gascon C, Jones DA, Bogart JP, Boag PT (1999) Ridges and rivers: A test of competing hypotheses of Amazonian diversification using a dart-poison frog (Epipedobates femoralis). Proceedings of the Royal Society of London. Series B: Biological Sciences 266(1431): 1829–1835.
Lunde D, Nguyen TS (2001) An identification guide to the rodents of Vietnam. Center for biodiversity and conservation, American Museum of Natural History, New York, 80 pp.
MacKinnon K, Hatta G, Halim H, Mangalic A (1996) The ecology of Kalimantan: Indonesian Borneo. Periplus Editions Ltd, Singapore, 802 pp.
Marshall JT Jr (1977) Family Muridae (rats and mice). Reprinted. pp. 396–487. In: Lekagul B, McNeely G (eds): Mammals of Thailand. Government Printing Office, Kurusapha Ladprao, Bangkok.
Meijaard E (2003) Mammals of south-east Asian islands and their Late Pleistocene environments. Journal of Biogeography 30: 1245–1257. https://doi.org/10.1046/j.1365-2699.2003.00890.x
Meijaard E, Groves CP (2006) The geography of mammals and rivers in mainland Southeast Asia. pp. 305–329. In: Lehman SM, Fleagle JG (eds): Primate biogeography. Springer Science + Business Media, LLC, New York.
Mizerovska D, Nicolas V, Demos TC, Akaibe D, Colyn M, Denys C, et al. (2019) Genetic variation of the most abundant forest-dwelling rodents in Central Africa (Praomys jacksoni complex): Evidence for Pleistocene refugia in both montane and lowland forests. Journal of Biogeography 46: 1466–1478.
Monastyrsky AL (2007) Ecological and biogeographical features of the fauna of Lepidoptera (Rhopalocera) in Vietnam. Enthomology Review 86(1): 43–72.
Monastyrsky AL (2010) Fauna of Lepidoptera (Papilionoidea) of Vietnam: Origin and modern diversity. Abstract of diss. Doc. of Biological Sciences. Мoscow, Severtsov’s Institute of Ecology and Evolution of RAS, 46 pp (in Russian).
Moore JC, Tate GHH (1965) A study of the Diurnal Squirrels, Sciurinae, of the Indian and Indochinese Subregions. Fieldiana, Zoology, Vol. 48. Chicago Natural History Museum Press, Chicago, 351 pp.
Mosbrugger V, Favre A, Muellner-Riehl AN, Packert M, Mulch A (2018) Cenozoic evolution of geo–biodiversity in the Tibeto–Himalayan region. pp. 429–448. In: Hoorn C Antonelli A, Perrigo A (eds): Mountains, climate, and biodiversity. Wiley-Blackwell, Hoboken.
Muellner-Riehl AN, Schnitzler J, Kissling WD, Mosbrugger V, Rijdijk KF, Seijmonsbergen AC, et al. (2019) Origins of global mountain plant biodiversity: Testing the ‘mountain-geobiodiversity hypothesis’. Journal of Biogeography 46: 2826–2838.
Musser GG, Carleton MD (1993) Family Muridae. pp. 501–755. In: Wilson DE, Reeder DM (eds): Mammal species of the world. A taxonomic and geographic reference. 2nd edition. Smithsonian Institution Press, Washington.
Musser GG, Carleton MD (2005) Superfamily Muroidea. pp. 894–1531. In: Wilson DE, Reeder DM (eds): Mammal species of the world. A taxonomic and geographic reference, Vol. 2. 3rd edition. Johns Hopkins University Press, Baltimore.
Musser GG, Lunde DP, Nguyen TS (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.
Nguyen XD, Nguyen XN, Nguyen TS, Tran HH (2012) Study of mammal diversity in Xuan Nha and Muong Do Nature Reserves, Son La Province, northwestern Vietnam. Mammal Study 37(1): 55–62.
Nicolas V, Missoup AD, Denys C, Peterhans JK, Katuala P, Couloux A, et al. (2011) The roles of rivers and Pleistocene refugia in shaping genetic diversity in Praomys misonnei in tropical Africa. Journal of Biogeography 38: 191–207.
Olayemi A, Nicolas V, Hulselmans J, Missoup AD, Fichet-Calvet E, Amundala D, et al. (2012) Taxonomy of the African giant pouched rats (Nesomyidae: Cricetomys): Molecular and craniometric evidence support an unexpected high species diversity. Zoological Journal of the Linnean Society 165: 700–719.
Osgood WH (1932) Mammals of the Kelley-Roosevelts and Delacour Asiatic expeditions. Field Museum of Natural History. Publication №132. Zoology Series 18(10): 193–339.
Patton JL, Da Silva MNF, Malcolm JR (1994) Gene genealogy and differentiation among arboreal spiny rats (Rodentia: Echimyidae) of the Amazon basin: A test of the riverine barrier hypothesis. Evolution 48(4): 1314–1323.
Patton JL, Silva MD, Malcolm J R (1996) Hierarchical genetic structure and gene flow in three sympatric species of Amazonian rodents. Molecular Ecology 5(2): 229–238.
Patton JL, Da Silva MNF, Malcolm JR (2000) Mammals of the Rio Jurua and the evolutionary and ecological diversification of Amazonia. Bulletin of the American Museum of Natural History 2000(244): 1–306.
Pavlinov IY (2003) Taxonomy of recent mammals. Archives of Zoological Museum of Moscow State University 46: 3–297 (in Russian).
Pavlinov IY, Yakhontov EL, Agadjanyan AK (1995) Mammals of Eurasia. I. Rodentia: Systematic-geographic reference book. Archives of Zoological Museum of Moscow State University 32: 3–240 (in Russian).
Peres CA, Patton JL, Nazareth F, da Silva M (1996) Riverine barriers and gene flow in Amazonian saddle-back tamarins. Folia Primatologica 67(3): 113–124.
Pu YT, Wan T, Fan RH, Fu CK, Tang KY, Jiang XL, et al. (2022) A new species of the genus Typhlomys Milne-Edwards, 1877 (Rodentia: Platacanthomyidae) from Chongqing, China. Zoological Research 43(3): 413–417. https://doi.org/10.24272/j.issn.2095-8137.2021.338
Salo J, Kalliola R, Häkkinen I, Mäkinen Y, Niemelä P, Puhakka M, et al. (1986): River dynamics and the diversity of Amazon lowland forest. Nature 322: 254–258. https://doi.org/10.1038/322254a0
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratories, Cold Spring Harbor.
Smith AT (2008) Family platacanthomyidae. pp. 208–209. In: Smith AT, Xie Y (eds): A guide to the mammals of China. Princeton University Press, Princeton, New Jersey.
Smith AT, Xie Y (2008) A guide to the mammals of China. Princeton University Press, Princeton and Oxford, 544 pp.
Stefenon VM, Klabunde G, Lemos RPM, Rogalski M, Nodari RO (2019) Phylogeography of plastid DNA sequences suggests post-glacial southward demographic expansion and the existence of several glacial refugia for Araucaria angustifolia. Scientific Reports 9: 27–52. http://doi.org/10.1038/s41598-019-39308-w
da Silva MNF, Patton JL (1998) Molecular phylogeography and the evolution and conservation of Amazonian mammals. Molecular Ecology 7(4): 475–486.
Takhtadzhyan AL (1978) Floristic regions of the Earth. Nauka, Leningrad, 247 pp. (in Russian).
Thorington RW, Hoffmann RS (2005) Family sciuridae pp. 754–818. In: Wilson DE, Reeder DM (eds): Mammal species of the world: A taxonomic and geographic reference, Vol. 2. 3rd edition. Johns Hopkins University Press, Baltimore.
Thorington RW, Koprowski JL, Steele MA, Whatton JF (2012) Squirrels of the world. Johns Hopkins University Press, Baltimore, 459 pp.
Trần HH, Trần HV, Lê XC, Nguyễn XD 2009. Phát hiện giống và loài chuột mới- Chuột bụng vạch (Pseudoberylmys muongbangensis), Tạp chí sinh học, 3(2): 33–39. (in Vietnamese with English summary).
van Peenen PFD, Ryan PF, Light RH (1969) Preliminary identification manual for mammals of South Vietnam. Smithsonian Institute, Washington, 310 pp.
Vu TL (1980) Vietnam. Geographical references. Publishing House of foreign languages literature, Hanoi, 280 pp. (in Russian).
Wang CW (1939) A preliminary study of the vegetation of Yunnan. Bulletin of the Fan Memorial Institute of Biology; Botany 9: 65–125 (in Chinese).
Wang Y, Li C, Chen Z (1996) Taxonomy, distribution and differentiation on Typhlomys cinereus (Platacanthomyidae, Mammalia). Acta Theriologica Sinica 16: 54–66.
Wang YX, Jin B (1987). Mammals in Xishuangbanna area and a brief survey of its fauna. pp. 289–304. In: Xu YC, Jiang HQ, Quan F (eds): Proceedings of synthetical investigation of Xishuangbanna nature reserves. Yunnan Science and Technology Press, Kunming (in Chinese).
Wikramanayake E, Dinerstein E, Louks CJ, Olson DM, Morrison J, Lamoreux J, et al. (2002) Terrestrial ecoregions of the Indo-Pacific. A conservation assessment. Island Press, Washington, 643 pp.
Wilson DE, Reeder DM. (eds) (2005) Mammal species of the world: A taxonomic and geographic reference, Vols. 1–2. Third edition. Johns Hopkins University Press, Baltimore, 2142 pp.
Woodruff DS, Turner LM (2009): The Indochinese–Sundaic zoogeographic transition: A description and analysis of terrestrial mammal species distributions. Journal of Biogeography 39: 803–821. https://doi.org/10.1111/j.1365-2699.2008.02071.x
Ye X-D, Ma Y, Zhang J-S, Wang Z-L, Wang Z-K (2002) A summary of Eothenomys (Rodentia: Cricetidae: Microtinae). Acta Zootaxonomica Sinica 27(1): 173–182 (in Chinese with English summary).
Zhang Y, Jin S. Quan G, Li S, Ye Z, Wang F, et al. (1997) Distribution of mammalian species in China. China Forestry Publishing House, Beijing, 280 pp.
Zheng Z, Feng ZL, Cao M, Li ZF, Zhang JH (2006a) Forest structure and biomass of a tropical seasonal rainforest in Xishuangbanna, Southwest China. Biotropica 38: 318–327.
Zheng Z, Shanmughavel P, Sha LQ, Cao M, Warren M (2006b) Litter decomposition and nutrient release in a tropical seasonal rainforest of Xishuangbanna, Southwest China. Biotropica 38: 342–347.
Zhu H, Cao M, Hu BH (2006) Geological history, flora and vegetation of Xishuangbanna, southern Yunnan, China. Biotropica 38: 310–317.
