Home A new subspecies of Finlayson’s squirrel from an isolated island offshore of the Indochina Peninsula in southern Vietnam
Article
Licensed
Unlicensed Requires Authentication

A new subspecies of Finlayson’s squirrel from an isolated island offshore of the Indochina Peninsula in southern Vietnam

  • Duong Thuy Vu , Son Truong Nguyen EMAIL logo , Masaharu Motokawa , Tu Ngoc Ly , Phuong Huy Dang , Hai Tuan Bui , Minh Duc Le , Hideki Endo and Tatsuo Oshida EMAIL logo
Published/Copyright: August 16, 2021

Abstract

We describe a new subspecies of Finlayson’s squirrel (Callosciurus finlaysonii) from Hon Nghe Island in the Gulf of Thailand. This island is located off the coast of southern Vietnam. In addition, we discussed the phylogenetic relationships among C. finlaysonii subspecies distributed on the isolated islands in the Gulf of Thailand. The new subspecies (C. finlaysonii honnghensis), which is endemic to Hon Nghe Island, differs from other C. finlaysonii subspecies in pelage colouration. The mitochondrial cytochrome b sequences showed that this squirrel is closely related to C. finlaysonii albivexilli and C. finlaysonii frandseni, which are endemic to the Koh Kut and Koh Chang islands, respectively, suggesting that the three subspecies diverged approximately 30,000 years ago. After the last glacial maximum, many small islands were formed by the sea level rise in the Gulf of Thailand, which was a consequence of global warming. Following the continuous fragmentation of the Sunda Continent, each C. finlaysonii subspecies could have evolved in each geographically isolated island in this gulf. Thus, studying C. finlaysonii subspecies may be used to track the recent geological history of the Gulf of Thailand.


Corresponding authors: Son Truong Nguyen, Department of Vertebrate Zoology, Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam; and Graduate University of Science and Technology, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam, E-mail: ; and Tatsuo Oshida, Laboratory of Wildlife Biology, Obihiro University of Agriculture and Veterinary Medichine, Obihiro 080-8555, Hokkaido, Japan, E-mail:

Funding source: Grants-in-Aid for Scientific Research, Ministry of Education, Science, Sports, and Culture, Japan

Award Identifier / Grant number: 18H03602

Award Identifier / Grant number: 19H00534

Award Identifier / Grant number: 20H01979

Funding source: The Program of Developing Basic Sciences in Chemistry, Life Sciences, Earth Sciences and Marine Sciences, Vietnam

Award Identifier / Grant number: KHCBSS.02/20–22

Funding source: University of Science, Vietnam National University, Hanoi

Funding source: Cooperation Research Program of the Wildlife Research Centre, Kyoto University

Funding source: Idea Wild Grant

Acknowledgements

We are grateful to Lam Quang Ngon at Can Tho University and Cao Truong Sang at Hon Nghe Junior High School for providing the information on Hon Nghe squirrel and Tran Anh Tuan for designing the map. We thank Nguyen Van Sinh (the director of Institute of Ecology and Biological Resources – IEBR) for supporting the expedition and Nguyen The Cuong for providing the information on the flora of Hon Nghe Island. We thank Vu Dinh Thong at IEBR and Nguyen Thanh Nam and Hoang Trung Thanh at VNU University of Science for their support with museum reference specimens. We thank Mitsuhiro Iwasa for his thoughtful comments for our study. We greatly thank two anonymous reviewers and John Koprowski (Dean, University of Wyoming) for thoughtful comments on our manuscript.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This research was funded by The Program of Developing Basic Sciences in Chemistry, Life Sciences, Earth Sciences and Marine Sciences, Vietnam Academy of Science and Technology (KHCBSS.02/20–22), as well as partially supported by Grants-in-Aid for Scientific Research nos. 18H03602, 19H00534 and 20H01979 from the Ministry of Education, Science, Sports, and Culture, Japan and Idea Wild Grant. This study was partly funded by the Cooperation Research Program of the Wildlife Research Centre, Kyoto University.

  3. Conflict of interest statement: The authors declare no conflict of interest regarding this article.

  4. Research ethics: In handling of squirrels, we followed the methods approved in the Animal Care and Use Guidelines of the American Society of Mammalogists (Sikes et al. 2016). In the open air, we euthanized squirrels using ether. We obtained permission to land on Hon Nghe Island and collect animals from the Vietnam Academy of Science and Technology (VAST), Hanoi, Vietnam (permission number: QTJP01.02/18-20; KC09.11/16-20; No 2027/QD-VHL/2019/-KHCBSS.02/20-22; No731/QD-STTNSV/2019; No730/STTNSV/2020).

References

Balakirev, A.E. and Rozhnov, V.V. (2019). Taxonomic revision of beautiful squirrels (Callosciurus, Rodentia: Sciuridae) from the Callosciurus erythraeus/finlaysonii complex and their distribution in eastern Indochina. Raffles Bull. Zool. 67: 459–489.Search in Google Scholar

Boonkhaw, P., Prayoon, U., Kanchanasaka, B., Hayashi, F., and Tamura, N. (2017). Colour polymorphism and genetic relationships among twelve subspecies of Callosciurus finlaysonii in Thailand. Mamm. Biol. 85: 6–13, https://doi.org/10.1016/j.mambio.2017.02.001.Search in Google Scholar

Bridges, E.M. (1990). World geomorphology. Cambridge University Press, Cambridge.10.1017/CBO9781139170154Search in Google Scholar

Clark, P.U., Dyke, A.S., Shakun, J.D., Carlson, A.E., Clark, J., Wohlfarth, B., Mitrovica, J.X., Hostetler, S.W., and McCabe, A.M. (2009). The last glacial maximum. Science 325: 710–714, https://doi.org/10.1126/science.1172873.Search in Google Scholar PubMed

Clark, P.U., Shakun, J.D., Baker, P.A., Bartlein, P.J., Brewer, S., Brook, E., Carlson, A.E., Cheng, H., Kaufman, D.S., Liu, Z., et al.. (2012). Global climate evolution during the last deglaciation. Proc. Natl. Acad. Sci. U. S. A. 109: E1134–E1142, https://doi.org/10.1073/pnas.1116619109.Search in Google Scholar PubMed PubMed Central

Combe, F.J., Ellis, J.S., Lloyd, K.L., Cain, B., Wheater, C.P., and Harris, W.E. (2016). After the ice age: the impact of post-glacial dispersal on the phylogeography of a small mammal, Muscardinus avellanarius. Front. Ecol. Evol. 4: 72, https://doi.org/10.3389/fevo.2016.00072.Search in Google Scholar

Corbet, G.B. and Hill, J.E. (1992). The mammals of the Indomalayan region: a systematic review. Oxford University Press, New York.Search in Google Scholar

Cox, C.B. and Moore, P.D. (2005). Biogeography: an ecological and evolutionary approach, 7th ed. The Bath Press, Oxford.Search in Google Scholar

Endo, H., Hayashi, Y., Rerkamnuaychoke, W., Nadee, N., Nabhitabhata, J., Kawamoto, Y., Hirai, H., Kimura, J., Nishida, T., and Yamada, J. (2000). Sympatric distribution of the two morphological types of the common tree shrew in Hat–Yai Districts (south Thailand). J. Vet. Med. Sci. 62: 759–761, https://doi.org/10.1292/jvms.62.759.Search in Google Scholar PubMed

Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791, https://doi.org/10.2307/2408678.Search in Google Scholar

Hall, R. and Morley, C.K. (2004). Sundaland basins. In: Clift, P., Kuhnt, W., Wang, P., and Hayes, D. (Eds.), Continent-ocean interaction within the East Asian marginal seas. American geophysical union geophysical monograph series 149, USA, pp. 55–85.10.1029/149GM04Search in Google Scholar

Hanebuth, T., Stattegger, K., and Grootes, P.M. (2000). Rapid flooding of the Sunda Shelf: a late-glacial sea-level record. Science 288: 1033–1035, https://doi.org/10.1126/science.288.5468.1033.Search in Google Scholar PubMed

Hanebuth, T.J.J., Voris, H.K., Yokoyama, Y., Saito, Y., and Okuno, J. (2011). Formation and fate of sedimentary depocentres on Southeast Asia’s Sunda Shelf over the past sea-level cycle and biogeographic implications. Earth Sci. Rev. 104: 92–110, https://doi.org/10.1016/j.earscirev.2010.09.006.Search in Google Scholar

Hasegawa, M., Kishino, H., and Yano, T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22: 160–174, https://doi.org/10.1007/bf02101694.Search in Google Scholar

Institute of Marine Environment and Resources (2020). Technical report of “The research on biodiversity of limestone island and archipelagos in the coastal zone of Vietnam, propose solution and models for use, conservation and sustainable development”, Vietnam, (in Vietnamese).Search in Google Scholar

Irwanto, D. (2019). Sundaland: tracing the cradle of civilizations. Indonesia Hydro™ Media, Bogor, Indonesia.Search in Google Scholar

Jenkins, P.D., Kilpatrick, C.W., Robinson, M.F., and Timmins, R.J. (2005). Morphological and molecular investigation of a new family, genus and species of rodent (Mammalia: Rodentia: Hystricognatha) from Lao PDR. Syst. Biodivers. 2: 419–454, https://doi.org/10.1017/s1477200004001549.Search in Google Scholar

Kanchanasaka, B., Boonkeow, P., Hirankrilas, K., Prayoon, U., and Tamura, N. (2014). Color variation of Finlayson’s squirrel among populations and individuals in central Thailand. Mamm. Stud. 39: 237–244, https://doi.org/10.3106/041.039.0401.Search in Google Scholar

Kloss, C.B. (1915). On two squirrels from the inner gulf of Siam. J. Nat. Hist. Soc. Siam 1: 157–162.Search in Google Scholar

Kloss, C.B. (1916a). On a collection of mammals from Siam. J. Nat. Hist. Soc. Siam 2: 1–32.Search in Google Scholar

Kloss, C.B. (1916b). On a collection of mammals from the coast and islands of Southeast Siam. Proc. Zool. Soc. Lond. 1: 27–75.10.1111/j.1096-3642.1916.tb02008.xSearch in Google Scholar

Kloss, C.B. (1916c). On diagnoses of four new squirrels from Siam. J. Nat. Hist. Soc. Siam 2: 178.Search in Google Scholar

Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Pääbo, S., Villablanca, F.X., and Wilson, A.C. (1989). Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. U. S. A. 86: 6196–6200, https://doi.org/10.1073/pnas.86.16.6196.Search in Google Scholar PubMed PubMed Central

Koprowski, J.L., Goldstein, E.A., Bennett, K.R., and Mendes, C.P. (2016). Family Sciuridae (tree, flying and ground squirrels, chipmunks, marmots and prairie dogs). In: Wilson, D.E., LacherJrT.E., and Mittermeier, R.A. (Eds.), Handbook of the mammals of the world 6: lagomorphs and rodents I. Lynx Edicions, Barcelona, pp. 648–837.Search in Google Scholar

Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870–1874, https://doi.org/10.1093/molbev/msw054.Search in Google Scholar PubMed PubMed Central

Lekagul, B. and McNeely, J.A. (1988). Mammal of Thailand, 2nd ed. Darnsutha Press, Bangkok.Search in Google Scholar

MacKinnon, K., Hatta, G., Halim, H., and Mangalik, A. (1996). The ecology of Kalimantan. Periplus Editions Ltd, Singapore.Search in Google Scholar

Meijaard, E. and Groves, C.P. (2006). The geography of mammals and rivers in mainland Southeast Asia. In: Lehman, S.M. and Fleagle, J.G. (Eds.), Primate biogeography. Springer Science + Business Media, LLC, New York, pp. 305–329.10.1007/0-387-31710-4_11Search in Google Scholar

Mercer, J.M. and Roth, V.L. (2003). The effects of Cenozoic global change on squirrel phylogeny. Science 299: 1568–1572, https://doi.org/10.1126/science.1079705.Search in Google Scholar PubMed

Milne-Edward, A. (1877). Sur quelques Mammifères et Crustacés nouveaux. Bull. Soc. Philomath. Paris 11: 8–10.Search in Google Scholar

Mittermeier, R.A., Turner, W.R., Larsen, F.W., Brooks, T.M., and Gascon, C. (2011). Global biodiversity conservation: the critical role of hotspots. In: Zachos, F.E. and Habel, J.C. (Eds.), Biodiversity hotspots: distribution and protection of conservation priority areas. Springer, Heidelberg, pp. 3–22.10.1007/978-3-642-20992-5_1Search in Google Scholar

Montgomery, W.I., Provan, J., McCabe, A.M., and Yalden, D.W. (2014). Origin of British and Irish mammals: disparate post–glacial colonization and species introductions. Quat. Sci. Rev. 98: 144–165, https://doi.org/10.1016/j.quascirev.2014.05.026.Search in Google Scholar

Moore, J.C. and Tate, G.H.H. (1965). A study of the diurnal squirrels, Sciurinae, of the Indian and Indochinese subregions. Natural History Museum, Chicago.10.5962/bhl.title.2919Search in Google Scholar

Musser, G.G., Smith, A.L., Robinson, M.F., and Lunde, D.P. (2005). Description of a new genus and species of rodent (Murinae, Muridae, Rodentia) from the Khammouan limestone national biodiversity conservation area in Lao PDR. Am. Mus. Novit. 3497: 1–31, https://doi.org/10.1206/0003-0082(2005)497[0001:doanga]2.0.co;2.10.1206/0003-0082(2005)497[0001:DOANGA]2.0.CO;2Search in Google Scholar

Musser, G., Lunde, D., and Nguyen, T.S. (2006). Description of a new genus and species pf rodent (Murinae, Muridae, Rodentia) from the lower karst region of northeastern Vietnam. Am. Mus. Novit. 3571: 1–41, https://doi.org/10.1206/0003-0082(2006)3517[1:doanga]2.0.co;2.10.1206/0003-0082(2006)3517[1:DOANGA]2.0.CO;2Search in Google Scholar

Nguyen, T.S., Dinh, H.V., Chan, T.D., and Nguyen, C.H. (2010). Morpho-genetic features of Vietnam coast. Proceedings of the 5th National Scientific Conference on Geography, Vietnam. Publishing House of Natural Science and Technology.Search in Google Scholar

Nguyen, S.T., Oshida, T., Dang, P.H., Bui, H.T., and Motokawa, M. (2018). A new species of squirrel (Sciuridae: Callosciurus) from an isolated island off the Indochina Peninsula in southern Vietnam. J. Mammal. 99: 813–825, https://doi.org/10.1093/jmammal/gyy061.Search in Google Scholar

Oshida, T., Lin, L.-K., Masuda, R., and Yoshida, M.C. (2000). Phylogenetic relationships among Asian species of Petaurista inferred from mitochondrial cytochrome b gene sequences. Zool. Sci. 17: 123–128, https://doi.org/10.2108/zsj.17.123.Search in Google Scholar

Oshida, T., Dang, C.N., Nguyen, S.T., Nguyen, N.X., Endo, H., Kimura, J., Sasaki, M., Hayashida, A., Takano, A., Yasuda, M., et al.. (2011). Phylogenetic relationship between Callosciurus caniceps and C. inornatus (Rodentia, Sciuridae): implication for zoogeographical isolation by the Mekong River. Ital. J. Zool. 78: 328–335, https://doi.org/10.1080/11250003.2010.490566.Search in Google Scholar

Oshida, T., Than, W., Oo, T., Swe, K.Y.Y., Saito, H., Motokawa, M., Kimura, J., Nguyen, S.T., Bui, H.T., and Dang, P.H. (2021). Phylogenetic relationships among Callosciurus squirrels in the Indochina peninsula: phylogenetic position of C. pygerythrus from Myanmar. Acta Zool. Acad. Sci. Hung. 67: 87–98, https://doi.org/10.17109/azh.67.1.87.2021.Search in Google Scholar

Pagès, M., Latinne, A., and Johan, M. (2011). Inter- and intraspecific genetic biodiversity in South East Asian rodents: new insights for their conservation. In: Zachos, F.E. and Habel, J.C. (Eds.), Biodiversity hotspots: distribution and protection of conservation priority areas. Springer, Heidelberg, pp. 363–382.10.1007/978-3-642-20992-5_19Search in Google Scholar

Robinson, H.C. and Kloss, C.B. (1922). New mammals from French Indo-China and Siam. Ann. Mag. Nat. Hist. ser. 9: 87–99, https://doi.org/10.1080/00222932208632642.Search in Google Scholar

Sanamxay, D., Douangboubpha, B., Bumrungsri, S., Xavavong, S., Xayaphet, V., Satasook, C., and Bates, P.J.J. (2013). Rediscovery of Biswamoyopterus (Mammalia: Rodentia: Sciurudae: Pteromyni) in Asia, with the description of a new species from Lao PDR. Zootaxa 3686: 471–481, https://doi.org/10.11646/zootaxa.3686.4.5.Search in Google Scholar

Sikes, R.S. and Animal Care and Use Committee of the American Society of Mammalogists (2016). (2016) Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J. Mammal. 97: 663–688, https://doi.org/10.1093/jmammal/gyw078.Search in Google Scholar

Suchard, M.A., Lemey, P., Baele, G., Ayres, D.L., Drummond, A.J., and Rambaut, A. (2018). Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4: vey016, https://doi.org/10.1093/ve/vey016.Search in Google Scholar

Tammone, M.N., Hajduk, A., Arias, P., Teta, P., Lacey, E.A., and Pardiñas, U.F.J. (2014). Last Glacial Maximum environments in northwestern Patagonia revealed by fossil small mammals. Quat. Res. 82: 198–208, https://doi.org/10.1016/j.yqres.2014.04.015.Search in Google Scholar

Tamura, K., Battistuzzi, F.U., Billing-Ross, P., Murillo, O., Filipski, A., and Kumar, S. (2012). Estimating divergence times in large molecular phylogenies. Proc. Natl. Acad. Sci. U. S. A. 109: 19333–19338, https://doi.org/10.1073/pnas.1213199109.Search in Google Scholar PubMed PubMed Central

Tamura, N., Fujii, Y., Boonkhaw, P., Prayoon, U., and Kanchanasaka, B. (2017). Colour vision in Finlayson’s squirrel (Callosciurus finlaysonii): is conspicuous pelage colour useful for species recognition? Trop. Zool. 30: 110–124, https://doi.org/10.1080/03946975.2017.1345471.Search in Google Scholar

Thomas, O. (1915). The penis bone, or “baculum”, as a guide to the classification of certain squirrels. Annal. Mag. Nat. Hist. ser. 8: 383–387, https://doi.org/10.1080/00222931508693653.Search in Google Scholar

Thomas, O. (1929). The Delacour exploration of French Indo-China – mammals III. Proc. Zool. Soc. Lond.: 831–841.10.1111/j.1469-7998.1928.tb07170.xSearch in Google Scholar

ThoringtonJrR.W., Koprowski, J.L., Steels, M.A., and Whatton, J.F. (2012). Squirrels of the world. Johns Hopkins University Press, Baltimore.10.1353/book.17238Search in Google Scholar

Tran, D.T., Le, D.A., Nguyen, H.C., Tran, D.L., Nguyen, V.Q., and Ta, H.P. (2012). Vietnamese sea and island–position, resources, and typical geological and ecological wonders. Publishing House for Scientific and Technology, Hanoi, Vietnam, (in Vietnamese).Search in Google Scholar

Voris, H.K. (2000). Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J. Biogeogr. 27: 1153–1167, https://doi.org/10.1046/j.1365-2699.2000.00489.x.Search in Google Scholar

Wattayakorn, G. (2006). Environmental issues in the Gulf of Thailand. In: Wolanski, E. (Ed.), The environment in Asia Pacific harbours. Springer, The Netherland, pp. 249–259.10.1007/1-4020-3655-8_16Search in Google Scholar

Winston, J.E. (1999). Describing species: practical taxonomic procedure for biologists. Columbia University Press, New York.Search in Google Scholar

Wroughton, R.C. (1908). On the forms of squirrel hitherto classed under Sc. finlaysoni, Hors. Ann. Mag. Nat. Hist. ser. 8: 393–401, https://doi.org/10.1080/00222930808692502.Search in Google Scholar


Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/mammalia-2021-0015).


Received: 2021-02-19
Accepted: 2021-07-08
Published Online: 2021-08-16
Published in Print: 2022-01-27

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 25.7.2025 from https://www.degruyterbrill.com/document/doi/10.1515/mammalia-2021-0015/html
Scroll to top button