Mammalian Biology

, Volume 93, Issue 1, pp 198–206 | Cite as

Mating calls are a sensitive indicator of phylogenetic relationships in tropical tree squirrels (Callosciurus spp.)

  • Noriko TamuraEmail author
  • Phadet Boonkhaw
  • Umphornpimon Prayoon
  • Budsabong Kanchanasaka
  • Fumio Hayashi
Original investigation


Vocal communication plays an important role in the mating behaviour of arboreal squirrels. Callosciurus is a genus of tree squirrels that includes 15 species distributed in Southeast Asia, and congeneric species often inhabit the same forest. As closely related species of Callosciurus have the potential to interbreed, species recognition from mating calls may be a fundamental reproductive barrier. We compared seven acoustic characteristics of male mating calls in six Callosciurus species and estimated whether the species differences were clear enough to function as a cue. Discriminant function analyses (DFA) classified 87.4% of mating calls to the correct species. All of the calls by C notatus, C. nigrovittatus and C. caniceps, and 88% of the calls by C. prevostii, were assigned to the correct species, while the percentage of correct classifications was lower in C. finlaysonii (71%) and C. erythraeus (63%). We compared these results with the genetic relationships to determine whether interspecific acoustic differences are caused by adaptive selection (habitat selection and body size) or by a stochastic process (drift). The genetic relationships among the six species were coincident with the differences in mating calls, which supports the stochastic divergence. Species-specific mating calls may be a useful cue for species recognition in Callosciurus, and thus these calls could be an effective trait for phylogenetic analysis in Callosciurus.


Acoustic properties Callosciurus Mating calls Arboreal squirrels Sympatric species 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abdullah, S.A., Yusoff-Rashid, N., Idris, A.H., 2001. Niche segregation among three sympatric species of squirrels inhabiting a lowland dipterocarp forest, Peninsular Malaysia. Mamm. Study 26, 133–144.CrossRefGoogle Scholar
  2. Ancillotto, L., Mori, E., 2017. Adaptive significance of coat colouration and patterns of Sciuromorpha(Rodentia). Ethol. Ecol. Evol. 29, 241–254.CrossRefGoogle Scholar
  3. Ancillotto, L., Russo, D., 2016. Individual vs. non-individual acoustic signaling in African woodland dormice (Graphiurus murinus). Mamm. Biol. 81, 410–414.CrossRefGoogle Scholar
  4. Balph, D.M., Balph, D.F., 1966. Sound communication of Uinta ground squirrels. J. Mammal. 47, 440–450.CrossRefGoogle Scholar
  5. Bergman, T.J., Cortés-Ortiz, L., Dias, P.A.D., Ho, L., Adams, D., Canales-Espinosa, D., Kitchen, D.M., 2016. Striking differences in the loud calls of howler monkey sister species (Alouatta pigra and A. palliate). Am. J. Primat. 78, 755–766.CrossRefGoogle Scholar
  6. Blankenship, D.J., Brand, L.R., 1987. Geographic variation in vocalizations of California chipmunks Tamias obscurus and T. merriami. Bull. South. Calif. Acad. Sci. 86, 126–135.Google Scholar
  7. Blumstein, D.T., Armitage, K.B., 1997. Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls. Am. Nat. 150, 179–200.PubMedCrossRefGoogle Scholar
  8. Boonkhaw, P., Prayoon, U., Kanchanasaka, B., Hayashi, F., Tamura, N., 2017. Colour polymorphism and genetic relationships among twelve subspecies of Callosciurus finlaysonii in Thailand. Mamm. Biol. 85, 6–13.CrossRefGoogle Scholar
  9. Boonkhaw, P., Kanchanasaka, B., Prayoon, U., 2014. Abundance and population of Callosciurus finlaysonii in some wildlife sanctuaries in the central and East Thailand. 2014 14, 27–140, 2012 (Thailand).Google Scholar
  10. Bradbury, J.W., 1977. Lek mating behavior in the hammer-headed bat. Z. Tierpsychol. 45, 225–255.CrossRefGoogle Scholar
  11. Brand, L.R., 1976. The vocal repertoire of chipmunks (genus Eitamias) in California. Anim. Behav. 24, 319–335.CrossRefGoogle Scholar
  12. Brockelman, W.Y., Ali, R., 1987. Methods of surveying and sampling forest primate populations. In: Marsh, C.W., Mittermeier, R.A. (Eds.), Primate Conservation in the Tropical Rain Forest. Alan R Liss, New York, pp. 23–62.Google Scholar
  13. Campbell, P., Pasch, B., Pino, J.L., Crino, O.L., Phillips, M., Phelps, S.M., 2010. Geographic variation in the songs of neotropical singing mice: testing the relative importance of drift and local adaptation. Evolution 64, 1955–1972.PubMedPubMedCentralGoogle Scholar
  14. Clutton-Brock, T.H., Guiness, F.E., Albon, S.D., 1982. Red Deer, Behavior and Ecology of Two Sexes. The University Chicago Press, Chicago, 378pp.Google Scholar
  15. Corbet, G.B., Hill, J.E., 1992. The Mammals of the Indomalayan Region. Nat. Hist. Mus. Pub. Oxford Univ. Press, Oxford.Google Scholar
  16. Cox, C.R., LeBoeuf, B.J., 1977. Female incitation of male competition: a mechanism in sexual selection. Am. Nat. 111, 317–335.CrossRefGoogle Scholar
  17. de la Torre, S., Snowdon, C.T., 2002. Environmental correlates of vocal communication of wild pygmy marmosets, Cebuella pygmaea. Anim. Behav. 63, 847–856.CrossRefGoogle Scholar
  18. Digweed, S.M., Rendall, D., Imbeau, T., 2012. Who’s your neighbor? Acoustic cues to individual identity in red squirrel Tamiasciurus hudsonicus rattle calls. Curr. Zool. 58, 758–764.CrossRefGoogle Scholar
  19. Eiler, K.C., Banack, S.A., 2004. Variability in the alarm call of golden-mantled ground squirrels (Spermophilus lateralis and S. saturates). J. Mammal. 85, 43–50.CrossRefGoogle Scholar
  20. Eisinger, J.W., Scheibe, J.S., Flaherty, E.A., 2016. Novel Glaucomys volans vocalizations in Indiana and evidence of geographic variation in high frequency communication. J. Mammal. 97, 1219–1227.CrossRefGoogle Scholar
  21. Emmons, L.H., 1978. Sound communication among African rainforest squirrels. Z. Tierpsychol. 47, 1–49.CrossRefGoogle Scholar
  22. Ey, E., Pfefferle, D., Fischer, J., 2007. Do age- and sex-related variations reliably reflect body size in non-human primate vocalizations? A review. Primates 48, 253–267.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Fagerstone, K.A., 1987. Comparison of vocalizations between and within Spermophilus elegans elegans and S. richardsonii. J. Mammal. 68, 853–587.CrossRefGoogle Scholar
  24. Farentinos, R.C., 1972. Social dominance and mating activity in the tassel-eared squirrel, (Sciurus aberti ferreus). Anim. Behav. 20, 316–326.PubMedCrossRefPubMedCentralGoogle Scholar
  25. Farentinos, R.C., 1974. Social communication of the tassel-eared squirrel (Sciurus aberti): a descriptive analysis. Z. Tierpsychol. 34, 441–458.CrossRefGoogle Scholar
  26. Fitch, W.T., Hauser, M.D., 1995. Vocal production in nonhuman primates: acoustics, physiology, and functional constraints on ‘honest’ advertisement. Amer. J. Primatol. 37, 191–219.CrossRefGoogle Scholar
  27. Gabrielli, M., Cardoso, Y.P., Benitez, V., Gozzi, A.C., Guichón, M.L., Lizarralde, M.S., 2014. Genetic characterization of Callosciurus (Rodentia: Sciuridae) Asiatic squirrels introduced in Argentina. Ital.J. Zool. 2014, 1–16.Google Scholar
  28. García-Navas, V., Blumstein, D.T., 2016. The effect of body size and habitat on the evolution of alarm vocalizations in rodents. Biol. J. Linn. Soc. 118, 745–751.CrossRefGoogle Scholar
  29. Gautier, J.P., 1989. A redrawn phylogeny of guenons based upon their calls: biogeographical implications. Int. J. Anim. Sound Rec. 2, 11–21.Google Scholar
  30. Grady, R.M., Hoogland, J.L., 1986. Why do male black-tailed prairie dogs (Cynomys ludovicianus) give a mating call? Anim. Behav. 34, 108–112.CrossRefGoogle Scholar
  31. Hafner, G.W., Hamilton, C.L., Steiner, W.W., Thompson, T.J., Winn, H.E., 1979. Signature information in the song of the humpback whale. J. Acoust. Soc. Am. 66, 1–6.CrossRefGoogle Scholar
  32. Hamilton, W.J., Arrowood, P.C., 1978. Copulatory vocalizations of chacma baboons (Papio ursinus), gibbons (Hylobates hoolock), and humans. Science 200, 1405–1409.PubMedCrossRefGoogle Scholar
  33. Hennelly, L., Habib, B., Root-Gutteridge, Palacios, V., Passilongo, D., 2017. Howl variation across Himalayan, North African, Indian, and Holarctic wolf clades: tracing divergence in the world’s oldest wolf lineages using acoustics. Curr. Zool. 63, 341–348.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Irwin, D.E., Thimgan, M.P., Irwin, J.H., 2008. Call divergence is correlated with geographic and genetic distance in greenish warblers (Phylloscopus trochiloides): a strong role forstochasticity in signal evolution? J. Evol. Biol. 21, 435–448.CrossRefGoogle Scholar
  35. Jahelková, H., Horáček, I., Bartonička, T., 2008. The advertisement song of Pipistrellus nathusii (Chiroptera, Vespertilionidae): a complex message containing acoustic signatures of individuals. Acta Chiropterol. 10, 103–126.CrossRefGoogle Scholar
  36. Kanchanasaka, B., Boonkhaw, P., Hirankrilas, K., Prayoon, Y., Tamura, N., 2014. Color variation of Finlayson’s squirrel among populations and individuals in central Thailand. Mamm. Study 39, 237–244.CrossRefGoogle Scholar
  37. Klump, G.K., Shalter, M.D., 1984. Acoustic behaviour of birds and mammals inthe predator context; I. Factors affecting the structure of alarm signals. II. The functional significance and evolution of alarm signals. Ethology 66, 189–226.Google Scholar
  38. Lair, H., 1990. The calls of the red squirrel: a contextual analysis of function. Behaviour 115, 254–282.CrossRefGoogle Scholar
  39. Lekagul, B., McNeely, J., 1977. Mammals of Thailand. Association forthe Conservation of Wildlife, Thailand, 758pp.Google Scholar
  40. Lishak, R.S., 1982. Gray squirrel mating calls: a spectrographic and ontogenic analysis. J. Mammal. 63, 661–663.CrossRefGoogle Scholar
  41. Macedonia, J.M., Stanger, K.F., 1994. Phylogeny of the Lemuridae revisited: evidence from communication signals. Folia Primatol. 63, 1–43.PubMedCrossRefGoogle Scholar
  42. MacKinnon, K.S., 1978. Stratification and feeding differences among Malayan squirrels. Malay. Nat. J. 30, 593–608.Google Scholar
  43. Marler, P., 1955. Characteristics of some animal calls. Nature 176, 6–8.CrossRefGoogle Scholar
  44. Marten, K., Marler, P., 1977. Sound transmission and its significance for animal vocalization. 1. Temperate habitats. Behav. Ecol. Sociobiol. 2, 271–290.CrossRefGoogle Scholar
  45. Marten, K., Quine, D., Marler, P., 1977. Sound transmission and its significance for animal vocalization. 2. Tropical forest habitats. Behav. Ecol. Sociobiol. 2, 291–302.CrossRefGoogle Scholar
  46. Martin, K., Tucker, M.A., Rogers, T.L., 2017. Does size matter? Examining the drivers of mammalian vocalizations. Evolution 71, 249–260.PubMedCrossRefGoogle Scholar
  47. May-Collado, L.J., Agnarsson, I., Wartzok, D., 2007. Phylogenetic review of tonal sound production in whales in relation to sociality. BMC Evol. Biol. 7, 136.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Mazzamuto, M.V., Galimberti, A., Cremonesi, G., Pisanu, B., Chapuis, J.L., Stuyck, J., Amori, G., Su, H., Aloise, G., Preatoni, D.G., Wauters, L.A., Casiraghi, M., Martinoli, A., 2016. Preventing species invasion: a role for integrative taxonomy? Integr. Zool. 11, 214–228.Google Scholar
  49. Mobley, J.R., Herman, L.M., Frankel, A.S., 1988. Responses of wintering humpback whales (Megaptera novaeangliae) to playback of recordings of winter and summer vocalizations and of synthetic sound. Behav. Ecol. Sociobiol. 23, 211–223.CrossRefGoogle Scholar
  50. Morton, E.S., 1975. Ecological sources of selection on avian sounds. Am. Nat. 109, 17–34.CrossRefGoogle Scholar
  51. Mumm, C.A., Urrutia, M.C., Knörnschild, M., 2014. Vocal individuality in cohesion calls of giant otters, Pteronura brasiliensis. Anim. Behav. 88, 243–252.CrossRefGoogle Scholar
  52. Oshida, T., Yasuda, M., Endo, H., Hussein, N.A., Masuda, R., 2001. Molecular phylogeny of five squirrel species of the genus Callosciurus (Mammalia, Rodentia) inferred from cytochrome b gene sequences. Mammalia 65, 473–482.CrossRefGoogle Scholar
  53. Oshida, T., Dang, C.N., Nguyen, S.T., Nguyen, N.X., Endo, H., Kimura, J., Sasaki, M., Hayashida, A., Takano, A., Yasuda, M., Hayashi, Y., 2011. Phylogenetic relationship between Callosciurus caniceps and C inornatus (Rodentia, Sciuridae): implications for zoogeographical isolation by the Mekong river. Ital. J. Zool. 78, 328–335.CrossRefGoogle Scholar
  54. Oshida, T., Dang, C.N., Nguyen, S.T., Nguyen, N.X., Endo, H., Kimura, J., Sasaki, M., Hayashida, A., Takano, A., Koyabu, D., Hayashi, Y., 2013. Phylogenetic position of Callosciurus erythraeus griseimanus from Vietnam in the genus Callosciurus. Mamm. Study 38, 41–47.CrossRefGoogle Scholar
  55. Oshida, T., Ysuda, M., Sasaki, M., 2016. Preliminary study on phylogeography of Callosciurus prevostii in Southeast Asia: mitochondrial DNA evidence supports riverine barrier hypothesis. Mamm. Study 41, 149–154.CrossRefGoogle Scholar
  56. Owings, D.H., Leger, D.W., 1980. Chatter vocalizations of California ground squirrels: predator- and social-role specificity. Ethology 54, 163–184.Google Scholar
  57. Peters, G., Peters, M., 2010. Long-distance call evolution in the Felidae: effects of body weight, habitat, and phylogeny. Biol. J. Linn. Soc. 101, 487–500.CrossRefGoogle Scholar
  58. Poole, J.H., 1989. Mate guarding, reproductive success and female choice in African elephants. Anim. Behav. 37, 842–849.CrossRefGoogle Scholar
  59. Ross, M.D., Geissmann, T., 2007. Call diversity of wild male orangutans: a phylogenetic approach. Am. J. Primatol. 69, 305–324.PubMedCrossRefPubMedCentralGoogle Scholar
  60. Russo, D., Mucedda, M., Bello, M., Biscardi, S., Pidichedda, E., Jones, G., 2007. Divergent echolocation call frequencies in insular rhinolophids (Chiroptera): a case of character displacement? J. iBiogeogr. 34, 2129–2138.CrossRefGoogle Scholar
  61. Ryan, M.J., Brenowitz, E.A., 1985. The role of body size, phylogeny and ambient noise inthe evolution of bird song. Am. Nat. 126, 87–100.CrossRefGoogle Scholar
  62. Saiful, A.A., Idris, A.H., Yusoff-Rashid, N., Tamura, N., Hayashi, F., 2001. Home range size of sympatric squirrel species inhabiting a lowland dipterocarp forest in Malaysia. Biotropica 33, 346–351.CrossRefGoogle Scholar
  63. Schneiderova, I., Volodina, E.V., Matrosova, V., Volodin, I.A., 2017. One plus one: binary alarm calls retain individual signature for longer periods than single-note alarms in the European ground squirrel (Spermophilus citellus). Behav. Processes 138, 73–81.PubMedCrossRefPubMedCentralGoogle Scholar
  64. Seddon, N., 2005. Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds. Evolution 59, 200–215.PubMedCrossRefPubMedCentralGoogle Scholar
  65. Sherman, P., 1977. Nepotism and the evolution of alarm calls. Science 197, 1246–1253.PubMedCrossRefPubMedCentralGoogle Scholar
  66. Smith, C.C., 1968. The adaptive nature of social organization in the genus Tamiasciurus. Ecol. Monogr. 38, 31–63.CrossRefGoogle Scholar
  67. Smith, C.C., 1978. Structure and function of the vocalizations of tree squirrels (Tamiasciurus). J. Mammal. 59, 793–808.CrossRefGoogle Scholar
  68. Stachowicz, J.B., Vannoni, E., Pitcher, B.J., Briefer, E.F., Gaffen, E., 2014. Acoustic divergence in the rut vocalizations of Persian and European fallow deer. J. Zool. 292, 1–9.CrossRefGoogle Scholar
  69. Steele, M.A., Koprowski, J.L., 2001. North American Tree Squirrels. Smithsonian Institution Press, Washington and London, 201pp.Google Scholar
  70. Struhsaker, T.T., 1981. Vocalizations, phylogeny and palaeogeography of red colobus monkeys (Colobus badius). Afr. J. Ecol. 19, 265–283.CrossRefGoogle Scholar
  71. Tamura, N., 1993. Role of sound communication in mating of Malaysian Callosciurus (Sciuridae). J. Mammal. 74, 468–476.CrossRefGoogle Scholar
  72. Tamura, N., 1995. Postcopulatory mate guarding by vocalization inthe Formosan squirrel. Behav. Ecol. Sociobiol. 36, 377–386.CrossRefGoogle Scholar
  73. Tamura, N., Fujii, Y., Bookhaw, P., Prayoon, U., Kanchanasaka, B., 2017. Colour vision in Finlayson’s squirrel (Callosciurus finlaysonii): is conspicuous pelage colour useful for species recognition? Trop. Zool. 30, 110–124.CrossRefGoogle Scholar
  74. Tamura, N., Hayashi, F., Miyashita, F., 1988. Dominance hierarchy and mating behavior of the Formosan squirrel, Callosciurus erythraeus thaiwanensis. J. Mammal. 69, 320–331.CrossRefGoogle Scholar
  75. Tamura, N., Ohba, T., 1993. Nestling sounds of the plantain squirrel (Sciuridae: Callosciurus notatus). Nat. Hist. Res. 2, 167–173.Google Scholar
  76. Tamura, N., Yong, H.S., 1993. Vocalizations in response to predators in three species of Malaysian Callosciurus (Sciuridae). J. Mammal. 74, 703–714.CrossRefGoogle Scholar
  77. Thinh, V.N., Hallam, C., Roos, C., Hammerschmidt, K., 2011. Concordance between vocal and genetic diversity in crested gibbons. BMC Evol. Biol. 11, 36.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Thompson, D.C., 1977. Reproductive behavior of the grey squirrel. Can. J. Zool. 55, 1176–1184.CrossRefGoogle Scholar
  79. Viljoen, S., 1983. Communicatory behavior of southern African tree squirrels, Paraxerus palliates ornatus, p. p. tongensis, P. c. cepapi and Funisciurus conjicus. Mammalia 47, 441–461.CrossRefGoogle Scholar
  80. Waring, G.H., 1970. Sound communications of black-tailed, white-tailed, and Gunnison’s prairie dogs. Am. Midl. Nat. 83, 167–185.CrossRefGoogle Scholar
  81. West-Eberhard, M.J., 1983. Sexual selection, social competition, and speciation. Q. Rev. Biol. 58, 155–183.CrossRefGoogle Scholar
  82. Wiley, R.H., Richards, D.G., 1978. Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behav. Ecol. Sociobiol. 3, 69–94.CrossRefGoogle Scholar
  83. Wilkins, M.R., Seddon, N., Safran, R.J., 2013. Evolutionary divergence in acoustic signals: causes and consequences. Tree 28, 156–166.PubMedGoogle Scholar
  84. Wilson, D.E., Reeder, D.M., 2005. Mammal Species of the World: a Taxonomic and Geographic Reference, 3rd ed. The John Hopkins University Press, Baltimore, pp. 2142.Google Scholar
  85. Wilson, D.R., Goble, A.R., Boutin, S., Humphries, M.M., Coltman, D.W., Gorrell, J.C., Shonfield, J., McAdam, A.G., 2015. Red squirrels use territorial vocalizations for kin discrimination. Anim. Behav. 107, 79–85.CrossRefGoogle Scholar
  86. Yamamoto, O., Moore, B., Brand, L., 2001. Variation in the bark call of the red squirrel (Tamiasciurus hudsonicus. West. North Am. Nat. 61, 395–402.Google Scholar
  87. Yasuda, M., Ishii, N., Okuda, T., Hussein, N.A., 2003. Small mammal community: habitat preference and effects after selective logging. In: Okuda, T., Manokaran, N., Matsumoto, Y., Niiyama, K., Thomas, S.C., Ashton, P.S. (Eds.), Pasoh, Ecology of a Lowland Rain Forest in Southeast Asia. Springer, Tokyo, pp. 533–546.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde, e. V. DGS 2018

Authors and Affiliations

  • Noriko Tamura
    • 1
    Email author
  • Phadet Boonkhaw
    • 2
  • Umphornpimon Prayoon
    • 2
  • Budsabong Kanchanasaka
    • 2
  • Fumio Hayashi
    • 3
  1. 1.Tama Forest Science GardenForestry and Forest Products Research InstituteHachioji, TokyoJapan
  2. 2.Department of National Park Wildlife and Plant ConservationBangkokThailand
  3. 3.Department of BiologyTokyo Metropolitan UniversityHachioji, TokyoJapan

Personalised recommendations