Taxonomic revision of Niviventer (Rodentia, Muridae) from Vietnam: a morphological and molecular approach

Balakirev A.E., Abramov A.V., Rozhnov V.V.

P. 1-26

Based on a comparative investigation of morphological and genetic data, a taxonomic revision of the genus Niviventer in Vietnam and the adjacent regions of East Indochina was carried out. The phylogenetic relationships within 13 species (N. andersoni, N. excelsior, N. eha, N. brahma, N. culturatus, N. coninga, N. rapit, N. niviventer, N. confucianus, N. tenaster, N. fulvescens, N. langbianis and N. cremoriventer) were investigated based on a full set of cytochrome b sequences and the cytochrome coxidase subunit I genes that are currently available. The full species rank for N. huang and N. bukit, which previously were regarded as forms of N. fulvescens, was approved. The occurrence of the members of the Malayan complex of species (N. tenaster, N. bukit and N. cremoriventer) among the mammal fauna of Southern Vietnam was established. The geographical distribution of the genetic lineages/species in Indochina is specified. It was shown that eight Niviventer species, namely N. niviventer, N. confucianus, N. bukit, N. tenaster, N. fulvescens, N. huang, N. langbianis and N. cremoriventer, occur in Vietnam. Some species (N. bukit, N. huang and N. langbianis) were demonstrated to be sympatrically distributed, whereas the others (N. fulvescens – N. huang and, apparently, N. cremoriventer – N. langbianis) formed vicariate pairs. Four species (N. niviventer, N. confucianus, N. fulvescens, and N. langbianis), were found to inhabit Northern Vietnam and the adjacent provinces of China (Yunnan, Guizhou); four species (N. tenaster, N. bukit, N. huang and N. langbianis) were recorded in the mountain regions of Central Vietnam and Laos; and three others (N. bukit, N. cremoriventer and N. huang) were found to inhabit most of the plains in Indochina, including Southern Vietnam, Cambodia, and a part of Thailand. It should be stressed that N. huang (but not N. fulvescens as it is usually considered) is the most common Niviventer species in Indochina, and its distribution range stretches over the plains of Thailand, Cambodia and Vietnam up to the south-eastern provinces of China.
Craniometrical characters and indexes were studied by applying discriminant analysis; the species-specific pattern of skull proportions and its applicability for species identification were demonstrated for some of the characters and indexes. By morphological analysis of genetically verified specimens, morphologically detailed descriptions of the external appearance and structural traits of the skull were presented for all eight Vietnamese Niviventer species. Practical recommendations and guidelines for visual species identification are also given. The size of the body and skull, the comparative length and the specific pattern of coloration of the tail and tail tip as well as the dorsal side of the feet, the size and shape of the auditory bullae, the comparative length of the incisive foramina and the bony palatal bridge and the extent of development of supraorbital ridges were demonstrated to be the most informative features for species identification. DOI: 10.15298/rusjtheriol.10.1.01

• Abe H. 1983. Variation and taxonomy of Niviventer group of rats in Thailand // Journal of Mammalogical Society of Japan. Vol.9. P.151-161.
• Allen G.M. 1926. Rats (genus Rattus) from the Asiatic Expeditions // American Museum Novitates. No.217. P.1-16.
• Allen G.M. 1940. The Mammals of China and Mongolia. Part 2. New York: American Museum of Natural History. P.621-1350.
• Balakirev A.E. & Rozhnov V.V. 2010. Phylogenic relationships and species composition in the genus Niviventer (Rodentia: Muridae) based on studies of the cytochrome b gene of mtDNA // Moscow University Biological Sciences Bulletin. Vol.65. No.4. P.171-174.
• Bekasova T.S. 1984. [Evolution of karyotypes in the subgenus Rattus (Rodentia, Muridae)] // Sokolov V.E. (ed.). [Evolutionary Studies. Macroevolution]. Moskva: Nauka. P.140-158 [in Russian].
• Bonhote J.L. 1903. On new species of Mus from Borneo and the Malay Peninsula // The Annals and Magazine of Natural History, Including Zoology, Botany, and Geology. Vol.11. Ser.7. P.123-125.
• Bonhote J.L. 1906. The mammalian fauna of China. Part I. Murinae // Proceedings of Zoological Society of London. Vol.2. P.384-397.
• Corbet G.B. & Hill J.E. 1992. The Mammals of the Indo-Malayan Region: A Systematic Review. Oxford: Oxford University Press. 488 p.
• Dang Huy Huynh, Dao Van Tien, Cao Van Sung, Pham Trong Anh & Hoang Minh Khien. 1994. [Checklist of Mammals in Vietnam]. Hanoi: Publishing House Science and Technics. 167 p. [in Vietnamese].
• Dang Ngoc Can, Endo H., Nguyen Truong Son, Oshida T., Le Xuan Canh, Dang Huy Phuong, Lunde D.P., Kawada S.-I., Hayashida A. & Sasaki M. 2008. [Checklist of Wild Mammal Species of Vietnam]. Hanoi: Institute of Ecology and Biological Resources. 400 p. [in Vietnamese].
• Duncan J.F., Van Peenen P.F.D. & Ryan P.F. 1970. Somatic chromosomes of eight mammals from Con Son Island, Southern Vietnam // Caryologia. Vol.23. P.173-181.
• Duncan J.F. & Van Peenen P.F.D. 1971. Karyotypes of ten rats (Rodentia: Muridae) from Southeast Asia // Caryologia. Vol.24. P.331-346.
• Ellerman J.R. 1941. The Families and Genera of Living Rodents. Vol.2. Family Muridae. London: British Museum (Natural History). 690 p.
• Ellerman J.R. 1947. A key to the Rodentia inhabiting India, Ceylon, and Burma, based on collections in the British Museum // Journal of Mammalogy. Vol.28. P.249-278.
• Ellerman J.R. 1948. Key to the rodents of south-west Asia in the British Museum collection // Proceedings of the Zoological Society of London. Vol.118. Pt.3. P.765-816.
• Ellerman J.R. 1949. The Families and Genera of Living Rodents. Vol.3. Pt.1. London: British Museum (Natural History). 210 p.
• Ellerman J.R. 1961. The Fauna of India, Including Pakistan, Burma and Ceylon: Mammalia. Second edition. Vol.3. Rodentia. Part 1-2. Calcutta: Zoological Survey of India. 884 p.
• Ellerman J.R. & Morrison-Scott T.C.S. 1951. Checklist of Palaearctic and Indian Mammals, 1758 to 1946. London: British Museum of Natural History. 810 p.
• Ellerman J.R. & Morrison-Scott T.C.S. 1966. Checklist of Palaearctic and Indian Mammals, 1758 to 1946. Second edition. London: British Museum of Natural History. 810 p.
• Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach // Journal of Molecular Evolution. Vol.17. No.6. P.368-376.
• Francis C.M. 2008. A Guide to the Mammals of Southeast Asia. Princeton and Oxford: Princeton University Press. 392 p.
• Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT // Nuclear Acids Symposium. Ser.41. P.95-98.
• Hebert P.D.N., Cywinska A., Ball S.L. & deWaard J.R. 2003. Biological identifications through DNA barcodes // Proceedings of the Royal Society of London, Series B. Vol.270. P.313-321.
• Irwin D., Kocher T.D. & Wilson A.S. 1991. Evolution of the cytochrome b gene of mammals // Journal of Molecular Evolution. Vol.32. P.128-144.
• Jansa S.A., Barker F.K. & Heaney L.R. 2006. The pattern and timing of diversification of Philippine endemic rodents: evidence from mitochondrial and nuclear gene sequences // Systematic Biology. Vol.55. No.1. P.73-88.
• Jing M., Yu H.-T., Wu S.-H., Wang W. & Zheng X. 2007. Phylogenetic relationships in genus Niviventer (Rodentia: Muridae) in China inferred from complete mitochondrial cytochrome b gene // Molecular Phylogenetic and Evolution. Vol.44. P.521-529.
• Jiang Q. 1995. Study on chromosomal classification of Rattus confucianus and R. fulvescens // Journal of Sun Yatsen University. Vol.1. P.98-103.
• Kocher T.D., Thomas W.K., Meyer A., Edwards S.V., Pддbo S., Villablanca F. & Wilson A. 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers // Proceedings of National Academy of Sciences of USA. Vol.86. P.6196-6200.
• Kuznetsov G.V. 2006. [Mammals of Vietnam]. Moskva: KMK Scientific Press Ltd. 420 p. [in Russian].
• Lecompte E., Aplin K., Denys Ch., Catzeflis F., Chades M. & Chevret P. 2008. Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily // BMC Evolutionary Biology. Vol.8. P.199.
• Li Y., Wu Y., Harada M., Lin L-K. & 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. Vol.25. P.686-692.
• Lunde D.P. & Nguyen Truong Son. 2001. An Identification Guide to the Rodents of Vietnam. New York: Center for Biodiversity and Conservation, American Museum of Natural History. 80 p.
• Lunde D.P., Nguyen Truong Son & Musser G.G. 2007. A survey of small mammals from Huu Lien Natural Reserve, Lang Son Province, Vietnam // Mammal Study. Vol.32. P.155-168.
• Markvong A., Marshall J.T. & Gropp A. 1973. Chromosomes of rats and mice of Thailand // Natural History Bulletin of Siam Society (Biological Sciences). Vol.25. P.233-240.
• Marshall J.T. 1977. Family Muridae (rats and mice) // Lekagul B. & McNeely G. Mammals of Thailand. Bangkok: Kurusapha Ladprao. P.397-487.
• Mayr E. 1963. Animal Species and Evolution. Cambridge: Harvard University Press. 597 p.
• Miller G.S. 1900. Seven new rats collected by Dr. W.L. Abbott in Siam // Proceedings of Biological Society Washington. Vol.13. P.137-150.
• Misonne X. 1969. African and Indo-Australian Muridae; evolutionary trends // Annales of Museum of Royal African Centre of Tervuren, Zoology. Vol.172. P.1-219.
• Molur S., Srinivasulu C., Srinivasulu B., Walker S., Nameer P.O. & Ravikumar L. 2005. Status of Non-volant Small Mammals: Conservation Assessment and Management Plan Workshop Report. Comibatore: Zoo Outreach Organization / CBSG-South Asia. 618 p.
• Musser G.G. 1973. Species-limits of Rattus cremoriventer and Rattus langbianis, murid rodents of southeastern Asia and the Greater Sunda Islands // American Museum Novitates. No.2525. P.1-65.
• Musser G.G. 1981. Results of the Archbold expeditions. No.105. Notes on systematics of Indo-Malayan murid rodents and descriptions of new genera and species from Ceylon, Sulawesi and the Philippines // Bulletin of American Museum (Natural History). Vol.168. No.3. P.236-256.
• Musser G.G. & Carleton M.D. 1993. Family Muridae // Wilson D.E. & Reeder D.M. (eds.). Mammal Species of the World. A Taxonomic and Geographic Reference. Second edition. Washington: Smithsonian Institution Press. P.501-755.
• Musser G.G. & Carleton M.D. 2005. Superfamily Muroidea // Wilson D.E. & Reeder D.M. (eds.). Mammals Species of the World. A Taxonomic and Geographic Reference. Third edition. Vol.2. Baltimore: Johns Hopkins University Press. P.894-1531.
• Musser G.G. & Heaney L.R. 1992. Philippine rodents: definitions of Tarsomys and Limnomys plus a preliminary assessment of phylogenetic patterns among native Philippine murines (Murinae, Muridae) // Bulletin of the American Museum of Natural History. Vol.211. P.1-138.
• Musser G.G. & Newcomb C. 1983. Malaysian murids and the giant rat of Sumatra // Bulletin of the American Museum of Natural History. Vol.174. P.327-598.
• Musser G.G., Lunde D.P. & Nguyen Truong Son. 2006. Description of a new genus and species of rodent (Murinae, Muridae, Rodentia) from the Tower Karst Region of Northeastern Vietnam // American Museum Novitates. No.3517. P.1-41.
• Musser G., Lunde D., Aplin K. & Molur S. 2008. Niviventer fulvescens // IUCN 2011. IUCN Red List of Threatened Species. Version 2011.1. . Downloaded on 08 July 2011.
• Niethammer J. & Martens J. 1975. Die gattungen Rattus und Maxomys in Afghanistan und Nepal // Zeitschrift fьr Sдugetierkunde. Vol.40. P.325-355.
• Nowak R.M. 1999. Walker's Mammals of the World. Sixth edition. Baltimore and London: The Johns Hopkins University Press. Vol.2. P.837-1936.
• Osgood W.H. 1932. Mammals of the Kelley-Roosevelt and Delacour Asiatic expeditions // Fields Museum of Natural History Publications. Vol.18. P.193-339.
• Page R.D.M. 1996. Tree View: An application to display phylogenetic trees on personal computers // Computers and Applied Bioscience. Vol.12. No.4. P.357-358.
• Pagés M., Chaval Y., Herberteau V., Waengsothorn S., Cosson J-F., Hugot J.-P., Morand S. & Michaux J. 2010. Revisiting the taxonomy of the Rattini tribe: a phylogeny based delimitation of species boundaries // BMC Evolutionary Biology. Vol.10. P.184.
• Pavlinov I.Ya. 2005. [Systematic of Recent Mammals]. Second Edition. Moskva: Izdatel'stvo Moskovskogo Universiteta. 297 p. [In Russian].
• Robins J.H., Hingston M., Matisoo-Smith E. & Ross H.A. 2007. Identifying Rattus species using mitochondrial DNA // Molecular Ecology Notes. Vol.7. P.717-729.
• Robinson H.C. & Kloss C.B. 1922. New mammals from French Indo-China and Siam // Annals and Magazine of Natural History (Zoology, Botany and Geology). Vol.9. P.87-99.
• Sambrook J., Fritsch E.F. & Maniatis T. 1989. Molecular Cloning: A Laboratory Manual, Cold Spring Harbor: Cold Spring Harbor Lab. 256 p.
• Savolainen V., Cowan R.S., Vogler A.P., Roderick G.K. & Lane R. 2005. Towards writing the encyclopedia of life: an introduction to DNA barcoding // Philosophical Transactions of the Royal Society of London, Series B. Vol.60. P.1805-1811.
• Smith A.T. & Lunde D. 2008. Family Muridae // Smith A.T. & Yan Xie. A Guide to the Mammals of China. Princeton and Oxford: Princeton University Press. P.247-273.
• StatSoft, Inc. 2001. STATISTICA (data analysis software system), version 6. www.statsoft.com.
• Stephen C. & Rudolf M. 2007. Contribution to the taxonomic status of the Chinese rats Niviventer confucianus and N. fulvescens // Mammalian Biology. Vol.72. No.4. P.213-222.
• Tamura K., Dudley J., Nei M. & Kumar S. 2007. MEGA 4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0 // Molecular Biology and Evolution. Vol.24. P.1596-1599.
• Thomas O. 1916. A new rat from Tenasserim // Annals and Magazine of Natural History (Zoology, Botany and Geology). Vol.17. P.425.
• Van Peenen P.F.D. 1969. Preliminary Identification Manual for Mammals of South Vietnam. Washington: United States National Museum, Smithsonian Institution. 193 p.
• Wang Y.X. 2003. A Complete Checklist of Mammal Species and Subspecies in China: A Taxonomic and Geographic Reference. Beijing: China Forestry Publishing House. 394 p. [in Chinese with English foreword].
• Zhang Y., Jin S., Quan G., Li S., Ye Z., Wang F. & Zhang M. 1997. Distribution of Mammalian Species in China. Beijing: China Forestry Publishing House. 280 p.
• Yong H.S. 1969. Karyotypes of Malay rats (Rodentia: Muridae, genus Rattus Fischer) // Chromosoma. Vol.27. P.245-267.
• Yoshida T.H. 1973. Evolution of karyotypes and differentiation in 13 Rattus species // Chromosoma. Vol.40. P.285-297.