A Comparative Zoogeographic View on the Animal Biodiversity of Indonesia and Japan

  • Hitoshi Suzuki
  • Anang Setiawan Achmadi


The Indonesian Archipelago harbors unique fauna with a high level of species diversity and endemism. In this report, we provide basic information on the spatial and temporal aspects of the animal ecosystem in the Indonesian Islands. We discuss four zoogeographic topics, including (1) lineage dispersal events from the continents to the Islands, (2) speciation processes in the insular area, (3) accelerated phenotypic evolution and (4) human impact on commensal animals compared to previous cases in the Japanese Archipelago, in which the same eustatic geological events and global climatic changes have occurred.


Biogeography Indonesia Japan Molecular phylogeny Mammals Evolution 



We would like to thank all members of the Museum Zoologicum Bogoriense, Research Center for Biology – LIPI, especially Dwi Aswti, Ibnu Maryanto, Martua H. Sinaga and Agustinus Suyanto for their hospitality in the field investigation and valuable suggestions. We would also like to thank Alejandro A. Chinen, Seigo Higashi, Tomofumi Shimada and Hidenori Takahashi for their valuable comments. This study was supported in part by a Grant-in-Aid for Scientific Research (B) from Japan Society for the Promotion of Science (JSPS) to H. S. (2440513).


  1. Achmadi AS, Esselstyn JA, Rowe KC, Maryanto I, Abdullah MT (2013) Phylogeny, diversity, and biogeography of the Southeast Asian endemic spiny rats. J Mammal 94:1412–1423. doi: Accessed 21 Feb 2014CrossRefGoogle Scholar
  2. Aplin KP, Suzuki H, Chinen AA, Chesser RT, ten Have J, Donnellan SC et al (2011) Multiple geographic origins of commensalism and complex dispersal history of black rats. PLoS One 6, e26357. doi: 10.1371/journal.pone.0026357 CrossRefGoogle Scholar
  3. Astuti D, Azuma N, Suzuki H, Higashi S (2006) Phylogenetic relationships within parrots (Psittacidae) inferred from mitochondrial cytochrome-b gene sequences. Zool Sci 23:191–198. doi: Accessed May 5 2013CrossRefGoogle Scholar
  4. Berggren WA, Kent DV, Swisher ICC, Aubry MP (1995) A revised geochronology and chronostratigraphy. In: Berggren WA, Kent DV, Aubry MP, Hardenbol J (eds) Geochronology, time scales and global stratigraphic correlation. Society of Economic Paleontologists and Mineralogists Special Publication, Tulsa, Oklahoma, USA, vol 54, pp 129–212. doi: 10.2110/pec.95.04.0129
  5. Bonhomme F, Searle JB (2012) House mouse phylogeography. In: Macholán M, Baird SJE, Munclinger P, Piálek J (eds) Evolution of the house mouse, Cambridge series in morphology and molecules. Cambridge University Press, Cambridge, pp 278–296CrossRefGoogle Scholar
  6. Byrne M, Steane DA, Joseph L, Yeates DK, Jordan GJ, Crayn D, Aplin K, Cantrill DJ, Cook LG, Crisp MD et al (2011) Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. J Biogeogr 38:1636–1656. doi: 10.1111/j.1365-2699.2011.02535.x CrossRefGoogle Scholar
  7. Carleton MD, Musser GG (2005) Order Rodentia. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, vol 2, 3rd edn. Johns Hopkins University Press, Baltimore, pp 745–752Google Scholar
  8. Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158. doi: 10.1038/38229 CrossRefGoogle Scholar
  9. Einarsson T, Albertsson KJ (1988) The glacial history of Iceland during the past three million years. Philos Trans R Soc Lond 318:637–644. doi: 10.1098/rstb.1988.0027 CrossRefGoogle Scholar
  10. Esselstyn JA, Timm RM, Brown RM (2009) Do geological or climatic processes drive speciation in dynamic archipelagos? The tempo and mode of diversification in Southeast Asian shrews. Evolution 63:2595–2610. doi: 10.1111/j.1558-5646.2009.00743.x CrossRefGoogle Scholar
  11. Esselstyn JA, Achmadi AS, Rowe KC (2012) Evolutionary novelty in a rat with no molars. Biol Lett 8:990–993. doi: 10.1098/rsbl.2012.0574 CrossRefGoogle Scholar
  12. Esselstyn JA, Maharadatunkamsi AAS, Siler CD, Evans BJ (2013) Carving out turf in a biodiversity hotspot: multiple, previously unrecognized shrew species co-occur on Java Island, Indonesia. Mol Ecol 22:4972–4987. doi: 10.1111/mec.12450 CrossRefGoogle Scholar
  13. Evans BJ, Supriatna J, Andayani N, Melnick DJ (2003) Diversification of Sulawesi macaque monkeys: decoupled evolution of mitochondrial and autosomal DNA. Evolution 57:1931–1946. doi: 10.1111/j.0014-3820.2003.tb00350.x CrossRefGoogle Scholar
  14. Gorog AJ, Sinaga MH, Engstrom MD (2004) Vicariance or dispersal? Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer, Leopoldamys sabanus and Maxomys whiteheadi). Biol J Linn Soc Lond 81:91–109. doi: 10.1111/j.1095-8312.2004.00281.x CrossRefGoogle Scholar
  15. Hall R (2002) Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. J Asian Earth Sci 20:353–431. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  16. Hall R (2012) Late Jurassic–Cenozoic reconstructions of the Indonesian region and the Indian Ocean. Tectonophysics 570–571:1–41. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  17. Haq BU, Hardenbol J, Vail PR (1987) Chronology of fluctuating sea levels since the Triassic. Science 235:1156–1167. doi: 10.1126/science.235.4793.1156 CrossRefGoogle Scholar
  18. Hosoda T, Sato JJ, Shimada T, Campbell KL, Suzuki H (2005) Independent nonframeshift deletions in the MC1R gene are not associated with melanistic coat coloration in three mustelid lineages. J Hered 96:607–613. doi: 10.1093/jhered/esi096 CrossRefGoogle Scholar
  19. Hosoda T, Sato JJ, Lin L-K, Chen Y-J, Harada M, Suzuki H (2011) Phylogenetic history of mustelid fauna in Taiwan inferred from mitochondrial genetic loci. Can J Zool 89:559–569. doi: 10.1139/z11-029 CrossRefGoogle Scholar
  20. Jansa SA, Barker FK, Heaney LR (2006) The pattern and timing of diversification of Phillippine endemic rodents: evidence from mitochondrial and nuclear gene sequences. Syst Biol 55:73–88. doi: 10.1080/10635150500431254 CrossRefGoogle Scholar
  21. Kambe Y, Tanikawa T, Matsumoto Y, Tomozawa M, Aplin KP, Suzuki H (2011) Origin of agouti-melanistic polymorphism in wild Black Rats (Rattus rattus) inferred from Mc1r gene sequences. Zool Sci 28:560–567. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  22. Kambe Y, Nakata K, Yasuda SP, Suzuki H (2012) Genetic characterization of Okinawan black rats showing coat color polymorphisms of white spotting and melanism. Genes Genet Syst 87:29–38. doi: Accessed 30 June 2014CrossRefGoogle Scholar
  23. Kambe Y, Suzuki S, Yabe T, Nakata K, Maezono Y, Abe S, Ishida K, Tanikawa T, Hashimoto T, Takeda M, Tsuchiya K, Yoshimatsu K, Suzuki H (2013) Introgressive hybridization of two major lineages of invasive Black Rats, Rattus rattus and R. tanezumi on the Japanese Islands inferred from Mc1r sequences. Honyurui Kagaku Mamm Sci 53:289–299, (in Japanese with English summary). doi: Accessed 30 June 2014Google Scholar
  24. Khush GS (1997) Origin dispersal cultivation and variation of rice. Plant Mol Biol 35:25–34. doi: 10.1007/978-94-011-5794-0_3 CrossRefGoogle Scholar
  25. Kirihara T, Shinohara A, Tsuchiya K, Harada M, Kryukov AP, Suzuki H (2013) Spatial and temporal aspects of Mogera species occurrence in the Japanese Islands inferred from mitochondrial and nuclear gene sequences. Zool Sci 30:267–281. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  26. Kitamura A, Kimoto K (2006) History of the inflow of the warm Tsushima current into the sea of Japan between 35 and 08 Ma. Palaeogeogr Palaeoclimatol Palaeoecol 236:355–366. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  27. Lohman DJ, Ingram KK, Prawiradilaga DM, Winder K, Sheldon FH et al (2010) Cryptic genetic diversity in “widespread” Southeast Asian bird species suggests that Philippine avian endemism is gravely underestimated. Biol Conserv 143:1885–1890. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  28. Lohman DJ, de Bruyn M, Page T, von Rintelen K, Hall R, Ng PKL, Shih H-T, Carvalho GR, von Rintelen T (2011) Biogeography of the Indo-Australian archipelago. Annu Rev Ecol Evol Syst 42:205–226. doi: 10.1146/annurev- ecolsys-102710-145001 CrossRefGoogle Scholar
  29. Maryanto I, Yani M (2003) A new species of Rousettus (Chiroptera: Pteropodidae) from Lore Lindu, Central Sulawesi. Mamm Study 28:111–120. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  30. Mittermeier RA, Gil PR, Hoffmann M, Pilgrim J, Brooks T, Mittermeier CG, Lamoreux J, Da Fonseca GAB (2004) Hotspots revisited: Earth’s biologically richest and most endangered terrestrial ecoregions. CEMEX, Mexico CityGoogle Scholar
  31. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. doi: 10.1038/35002501 CrossRefGoogle Scholar
  32. Nakayama K, Shotake T, Takenaka O, Ishida T (2008) Variation of the melanocortin 1 receptor gene in the macaques. Am J Primatol 70:778–785. doi: 10.1002/ajp.20547 CrossRefGoogle Scholar
  33. Nunome M, Ishimori C, Aplin KP, Yonekawa H, Moriwaki K, Suzuki H (2010) Detection of recombinant haplotypes in wild mice (Mus musculus) provides new insights into the origin of Japanese mice. Mol Ecol 19:2474–2489. doi: 10.1111/j.1365-294X.2010.04651.x Google Scholar
  34. Pagès M, Chaval Y, Herbreteau V, Waengsothorn S, Cosson JF, Hugot JP, Morand S, Michaux J (2010) Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC Evol Biol 10:184. doi: 10.1186/1471-2148-10-184 CrossRefGoogle Scholar
  35. Randall JE (1998) Zoogeography of shore fishes of the Indo-Pacific region. Zool Stud 37:227–268Google Scholar
  36. Robins JH, Hingston M, Matisoo-Smith E, Ross HA (2007) Identifying Rattus species using mitochondrial DNA. Mol Ecol Notes 7:717–729. doi: 10.1111/j.1471-8286.2007.01752.x CrossRefGoogle Scholar
  37. Rowe KC, Reno ML, Richmond DM, Adkins RM, Steppan SJ (2008) Pliocene colonization and adaptive radiations in Australia and New Guinea (Sahul): multilocus systematics of the old endemic rodents (Muroidea: Murinae). Mol Phylogenet Evol 47:84–101. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  38. Rowe KC, Aplin KP, Baverstock PR, Moritz C (2011) Recent and rapid speciation with limited morphological disparity in the genus rattus. Syst Biol 60:188–203. doi: 10.1093/sysbio/syq092 CrossRefGoogle Scholar
  39. Rowe KC, Achmadi AS, Esselstyn JA (2014) Convergent evolution of semi-aquatic carnivory in a new genus and species (Rodentia: Muridae) from Wallacea. Zootaxa 3815:541–564. doi: Accessed 30 June 2014CrossRefGoogle Scholar
  40. Sato JJ, Wolsan M, Minami S, Hosoda T, Sinaga MH, Hiyama K, Yamaguchi Y, Suzuki H (2009) Deciphering and dating the red panda’s ancestry. Mol Phylogenet Evol 53:907–922. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  41. Serizawa K, Suzuki H, Tsuchiya K (2000) A phylogenetic view on species radiation in Apodemus inferred from variation of nuclear and mitochondrial genes. Biochem Genet 38:27–40. doi: 10.1023/A:1001828203201 CrossRefGoogle Scholar
  42. Shimada T, Aplin K, Jogahara T, Lin KL, Gonzalez JP, Herbreteau V, Suzuki H (2007) Complex phylogeographic structuring in a continental small mammal from East Asia, the rice field mouse, Mus caroli (Rodentia, Muridae). Mamm Study 32:49–62. doi:[49:CPSIAC]2.0.CO;2. Accessed 5 May 2013CrossRefGoogle Scholar
  43. Shimada T, Sato JJ, Aplin KP, Suzuki H (2009) Comparative analysis of evolutionary modes in Mc1r coat color gene in wild mice and mustelids. Genes Genet Syst 84:225–231. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  44. Shinohara A, Suzuki H, Tsuchiya K, Zhang YP, Luo J, Jiang XY, Wang YX, Campbell KL (2004) Evolution and biogeography of talpid moles from continental East Asia and the Japanese Islands inferred from mitochondrial and nuclear gene sequences. Zool Sci 21:1177–1185. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  45. Sodhi NS, Koh LP, Brook BW, Ng PKL (2004) Southeast Asian biodiversity: an impending disaster. Trends Ecol Evol 19:654–660. doi: Accessed 30 June 2014CrossRefGoogle Scholar
  46. Stelbrink B, Albrecht C, Hall R, von Rintelen T (2012) The biogeography of Sulawesi revisited: is there evidence for a vicariant origin of taxa on Wallace’s “anomalous island”? Evolution 66:2252–2271CrossRefGoogle Scholar
  47. Steppan SJ, Adkins RM, Spinks PQ, Hale C (2005) Multigene phylogeny of the Old World mice, Murinae, reveals distinct geographic lineages and the declining utility of mitochondrial genes compared to nuclear genes. Mol Phylogenet Evol 37:370–388. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  48. Suyanto A, Yoneda M, Maryanto I, Maharadatunkamsi SJ (2002) Checklist of the mammals of Indonesia. Scientific name and distribution area table in Indonesia including CITES, IUCN and Indonesian category for conservation. LIPI-JICA-PHKA, BogorGoogle Scholar
  49. Suzuki H (2009) A molecular phylogenetic view of mammals in the “three-story museum” of Hokkaido, Honshu, and Ryukyu Islands, Japan. In: Ohdachi SD, Ishibashi Y, Iwasa MA, Saitoh T (eds) The wild mammals of Japan. Shoukadoh, Kyoto, pp 261–263Google Scholar
  50. Suzuki H (2013) Evolutionary and phylogeographic views on Mc1r and Asip variation in mammals. Genes Genet Syst 88:155–164. doi: Assessed 30 June 2014CrossRefGoogle Scholar
  51. Suzuki H, Aplin KP (2012) Phylogeny and biogeography of the genus Mus in Eurasia. In: Macholán M, Baird SJE, Munclinger P, Piálek J (eds) Evolution of the house mouse. Cambridge series in morphology and molecules. Cambridge University Press, Cambridge, pp 35–64CrossRefGoogle Scholar
  52. Suzuki H, Tsuchiya K, Takezaki N (2000) A molecular phylogenetic framework for the Ryukyu endemic rodents Tokudaia osimensis and Diplothrix legata. Mol Phylogenet Evol 15:15–24. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  53. Suzuki H, Sato JI, Tsuchiya K, Luo J, Zhang YP, Wang YX, Jiang XL (2003) Molecular phylogeny of wood mice (Apodemus, Muridae) in East Asia. Biol J Linn Soc 80:469–481. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  54. Suzuki H, Filippucci MG, Chelomina GN, Sato JJ, Serizawa K, Nevo E (2008) A biogeographic view of Apodemus in Asia and Europe inferred from nuclear and mitochondrial gene sequences. Biochem Genet 46:329–346. doi: 10.1007/s10528-008-9149-7 CrossRefGoogle Scholar
  55. Suzuki H, Nunome M, Kinoshita G, Aplin KP, Vogel P, Kryukov AP, Jin ML, Han SH, Maryanto I, Tsuchiya K, Ikeda H, Shiroishi T, Yonekawa H, Moriwaki K (2013) Evolutionary history of Eurasian house mice Mus musculus clarified by more extensive geographic sampling of mitochondrial DNA. Heredity 111:375–390. doi: 10.1038/hdy.2013.60 CrossRefGoogle Scholar
  56. Terashima M, Furusawa S, Hanzawa N, Tsuchiya K, Suyanto A, Moriwaki K, Yonekawa H, Suzuki H (2006) Phylogeographic origin of Hokkaido house mice (Mus musculus) as indicated by genetic markers with maternal, paternal and biparental inheritance. Heredity 96:128–138. doi: 10.1038/sj.hdy.6800761 CrossRefGoogle Scholar
  57. Tsuchiya K, Suzuki H, Shinohara A, Harada M, Wakana S, Sakaizumi M, Han SH, Lin LK, Kryukov AP (2000) Molecular phylogeny of east Asian moles inferred from the sequence variation of the mitochondrial cytochrome b gene. Genes Genet Syst 75:17–24. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  58. Woodruff DS (2003) Neogene marine transgressions, palaeogeography and biogeographic transitions on the Thai–Malay Peninsula. J Biogeogr 30:551–567. doi: 10.1046/j.1365-2699.2003.00846.x. Accessed 5 May 2013CrossRefGoogle Scholar
  59. Yamada F, Takaki M, Suzuki H (2002) Molecular phylogeny of Japanese Leporidae, the Amami rabbit Pentalagus furnessi, the Japanese hare Lepus brachyurus, and the mountain hare Lepus timidus, inferred from mitochondrial DNA sequences. Genes Genet Syst 77:107–116. doi: Accessed 5 May 2013CrossRefGoogle Scholar
  60. Yonekawa H, Moriwaki K, Gotoh O, Miyashita N, Matsushima N et al (1988) Hybrid origin of Japanese mice “Mus musculus molossinus”: evidence from restriction analysis of mitochondrial DNA. Mol Biol Evol 5:63–78Google Scholar
  61. Yosida TH (1980) Cytogenetics of the black rat: karyotype evolution and species differentiation. University of Tokyo Press, TokyoGoogle Scholar
  62. Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to Present. Science 292:686–693. doi: 10.1126/science.1059412 CrossRefGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  1. 1.Laboratory of Ecology and Genetics, Graduate School of Environmental Earth ScienceHokkaido UniversitySapporoJapan
  2. 2.Museum Zoologicum BogorienseResearch Center for Biology – LIPICibinongIndonesia

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