Skip to main content
Log in

Species-specific and shared features in vocal repertoires of three Eurasian ground squirrels (genus Spermophilus)

  • Original Paper
  • Published:
Acta Theriologica Aims and scope Submit manuscript

Abstract

Along to alarm calls, Eurasian ground squirrels of the genus Spermophilus also produce other call types toward potential predators and rival conspecifics. Individually identified 50 speckled (Spermophilus suslicus), 18 European (S. citellus) and 59 yellow (S. fulvus) ground squirrels were examined for interspecies differences in their vocal repertoires. A separate sample of 116 (90 adult and 26 juvenile) S. suslicus was examined for presence of ultrasound in their alarm calls. In addition, all tonal calls in all the three species were checked for presence of nonlinear phenomena. Calls were elicited by approaching animals in live-traps or near burrows; some types of vocalizations were also recorded during handling. Eight call types, three tonal and five wideband ones, were described. Vocal repertoires were remarkably similar between species, excluding the alarm calls, which were species-specific. Alarm calls with ultrasonic components were found in two individuals of S. suslicus. Concerning nonlinear phenomena, biphonation in alarm calls of S. suslicus, frequency jumps and sidebands in screams of S. citellus, frequency jumps and subharmonics in screams of S. fulvus were found. Results are discussed with literature evidence on audible and ultrasonic vocalizations in ground squirrels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Balph DM, Balph DF (1966) Sound communication of Uinta ground squirrels. J Mammal 47:440–450

    Article  Google Scholar 

  • Betts BJ (1976) Behaviour in a population of Columbian ground squirrels, Spermophilus columbianus columbianus. Anim Behav 24:652–680

    Article  Google Scholar 

  • Blumstein DT (2007) The evolution of alarm communication in rodents: structure, function, and the puzzle of apparently altruistic calling in rodents. In: Wolff JO, Sherman PW (eds) Rodent societies. Univ. Chicago Press, Chicago, pp 317–327

    Google Scholar 

  • Blumstein DT, Récapet C (2009) The sound of arousal: the addition of novel non-linearities increases responsiveness in marmot alarm calls. Ethology 115:1074–1081

    Article  Google Scholar 

  • Blumstein DT, Richardson DT, Cooley L, Winternitz J, Daniel JC (2008) The structure, meaning and function of yellow-bellied marmot pup screams. Anim Behav 76:1055–1064

    Article  Google Scholar 

  • Davis LS (1984) Alarm calling in Richardson’s ground squirrels (Spermophilus richardsonii). Z Tierpsychol 66:152–164

    Article  Google Scholar 

  • Digweed SM, Rendall D (2009a) Predator-associated vocalizations in North American red squirrels, Tamiasciurus hudsonicus: are alarm calls predator specific? Anim Behav 78:1135–1144

    Article  Google Scholar 

  • Digweed SM, Rendall D (2009b) Predator-associated vocalizations in North American red squirrels (Tamiasciurus hudsonicus): To whom are alarm calls addressed and how do they function? Ethology 115:1190–1199

    Article  Google Scholar 

  • Eiler KC, Banack SA (2004) Variability in the alarm call of golden-mantled ground squirrels (Spermophilus lateralis and S. saturatus). J Mammal 85:43–50

    Article  Google Scholar 

  • Ermakov OA, Surin VL, Titov SV, Tagiev AF, Luk’yanenko AV, Formozov NA (2002) A molecular genetic study of hybridization in four species of ground squirrels (Spermophilus: Rodentia, Sciuridae). Russ J Genet 38(7):796–809

    Article  CAS  Google Scholar 

  • Fichtel C, Kappeler PM (2002) Anti-predator behavior of group-living Malagasy primates: mixed evidence for a referential alarm call system. Behav Ecol Sociobiol 51:262–275

    Article  Google Scholar 

  • Fitch WT, Neubauer J, Herzel H (2002) Calls out of chaos: the adaptive significance of nonlinear phenomena in mammalian vocal production. Anim Behav 63:407–418

    Article  Google Scholar 

  • Georgiev A, Keppler S, Haas H (2004) A preliminary investigation into the alarm-calling behaviour of European sousliks (Spermophilus citellus). In: Behavioural Ecology excursion to Bulgaria. Project report on the European Souslik Working Group. http://www.geocities.com/thesousliks

  • Gould E (1983) Mechanisms of mammalian auditory communication. In: Eisenberg JF, Kleiman DG (eds) Advances in the study of mammalian behaviour. Special Publication. American Society of Mammalogists, Shippensburg, pp 265–342

    Google Scholar 

  • Helgen KM, Cole FR, Helgen LE, Wilson DE (2009) Generic revision in the holarctic ground squirrel genus Spermophilus. J Mammal 90:270–305

    Article  Google Scholar 

  • Kashkarov D, Lein L (1927) The yellow ground squirrel of Turkestan, Cynomys fulvus oxianus Thomas. Ecology 8:63–72

    Article  Google Scholar 

  • Koeppl JW, Hoffman RS, Nadler CF (1978) Pattern analysis of acoustical behavior in four species of ground squirrels. J Mammal 59:677–696

    Article  Google Scholar 

  • Koshev Y, Pandourski I (2008) Structure and variability of alarm calls of European ground squirrel (Rodentia: Spermophilus citellus L. 1766) from Western Bulgaria. Acta Zool Bulg 60:99–105

    Google Scholar 

  • Krenz MC (1977) Vocalization of the rock squirrel Spermophilus variegatus. Dissertation, Texas Tech University, Lubbock, TX

  • Kryštufek B, Vohralík V (2005) Mammals of Turkey and Cyprus. Rodentia: I. Sciuridae, Dipodidae, Gliridae, Arvicolinae. University of Primorska, Koper

    Google Scholar 

  • Leger DW, Berney-Key SD, Sherman PW (1984) Vocalizations of Belding’s ground squirrels (Spermophilus beldingi). Anim Behav 32:753–764

    Article  Google Scholar 

  • Macedonia JME, Evans CS (1993) Variation among mammalian alarm call systems and the problem of meaning in animal signals. Ethology 93:177–197

    Article  Google Scholar 

  • Manno TG, Nesterova AP, Debarbieri LM, Kennedy SE, Wright KS, Dobson FS (2007) Why do male Columbian ground squirrels give a mating call? Anim Behav 74:1319–1327

    Article  Google Scholar 

  • Matrosova VA, Volodin IA, Volodina EV (2006) The diversity of calls produced by live-trapped speckled ground squirrels Spermophilus suslicus (Rodentia, Sciuridae). Bull Moscow Soc Naturalists 111:84–87 [In Russian]

    Google Scholar 

  • Matrosova VA, Volodin IA, Volodina EV, Babitsky AF (2007) Pups crying bass: vocal adaptation for avoidance of age-dependent predation risk in ground squirrels? Behav Ecol Sociobiol 62:181–191

    Article  Google Scholar 

  • Matrosova VA, Volodin IA, Volodina EV (2008) Does kinship affect the alarm call structure in the yellow ground squirrel Spermophilus fulvus? Lynx (Praha) ns 39:295–303

    Google Scholar 

  • Matrosova VA, Volodin IA, Volodina EV (2009) Short-term and long-term individuality in speckled ground squirrel alarm calls. J Mammal 90:158–166

    Article  Google Scholar 

  • Matrosova VA, Volodin IA, Volodina EV, Vasilieva NA (2010a) Stability of acoustic individuality in the alarm calls of wild yellow ground squirrels Spermophilus fulvus and contrasting calls from trapped and free-ranging callers. Naturwissenschaften 97:707–715

    Article  PubMed  CAS  Google Scholar 

  • Matrosova VA, Volodin IA, Volodina EV, Vasilieva NA, Kochetkova AA (2010b) Between-year stability of individual alarm calls in the yellow ground squirrel Spermophilus fulvus. J Mammal 91:620–627

    Article  Google Scholar 

  • Matrosova VA, Blumstein DT, Volodin IA, Volodina EV (2011) The potential to encode sex, age and individual identity in the alarm calls of three species of Marmotinae. Naturwissenschaften 98:181–192

    Article  PubMed  CAS  Google Scholar 

  • McCowan B, Hooper SL (2002) Individual acoustic variation in Belding’s ground squirrel alarm chirps in the High Sierra Nevada. J Acoust Soc Am 111:1157–1160

    Article  PubMed  Google Scholar 

  • Melchior HR (1971) Characteristics of arctic ground squirrel alarm calls. Oecologia 7:184–190

    Article  Google Scholar 

  • Nikoĺskii AA (1979) Species specifity of alarm call in sousliks (Citellus, Sciuridae) of Eurasia. Zool Zh 58:1183–1194 [In Russian]

    Google Scholar 

  • Nikoĺskii AA (1984) Zvukovye signaly mlekopitajushchih v evolucionnom processe [Sound signals of mammals in evolution]. Nauka, Moscow [in Russian]

  • Nikoĺskii AA, Rumyantsev VYu (2004) Variability of alarm call in ground squirrels of Major group (Rodentia, Sciuridae, Spermophilus) as a model of geographic species formation. Zool Zh 83:1008–1017 [In Russian]

    Google Scholar 

  • Nikoĺskii AA, Denisov VP, Stojko TG, Formozov NA (1984) The alarm call in F1 hybrids Citellus pygmaeus x C. suslica (Sciuridae, Rodentia). Zool Zh 63:1216–1225 [In Russian]

    Google Scholar 

  • Nowak RM (1999) Walker’s mammals of the world, 6th edn. John Hopkins Univ. Press, Baltimore

    Google Scholar 

  • Owings DH, Leger DW (1980) Chatter vocalizations of California ground squirrels: predator- and social-role specifity. Z Tierpsychol 54:163–184

    Article  Google Scholar 

  • Owings DH, Virginia RA (1978) Alarm calls of California ground squirrels (Spermophilus beecheyi). Z Tierpsychol 46:58–70

    Article  Google Scholar 

  • Owren MJ, Rendall D (1997) An affect-conditioning model of nonhuman primate vocal signals. In: Owings DH, Beecher MD, Thompson NS (eds) Perspectives in ethology, vol. 12. Plenum, New York, pp 299–346

    Google Scholar 

  • Pollard KA, Blumstein DT (2011) Social group size predicts the evolution of individuality. Curr Biol 21:413–417

    Article  PubMed  CAS  Google Scholar 

  • Robinson SR (1981) Alarm communication in Belding’s ground squirrels. Z Tierpsychol 56:150–168

    Article  Google Scholar 

  • Russo D, Teixeira S, Cistrone L, Jesus J, Teixeira D, Freitas T, Jones G (2009) Social calls are subject to stabilizing selection in insular bats. J Biogeogr 36:2212–2221

    Article  Google Scholar 

  • Schneiderová I, Policht R (2010) Alarm calls of the European ground squirrel Spermophilus citellus and the Taurus ground squirrel S. taurensis encode information about caller identity. Bioacoustics 20:29–43

    Google Scholar 

  • Shekarova ON, Neronov VV, Savinetskaya LE (2008) Speckled ground squirrel (Spermophilus suslicus): current distribution, population dynamics and conservation. Lynx (Praha) ns 39:317–322

    Google Scholar 

  • Sherman PW (1977) Nepotism and the evolution of alarm calls. Science 197:1246–1253

    Article  PubMed  CAS  Google Scholar 

  • Sherman PW (1985) Alarm calls of Belding’s ground squirrels to aerial predators: nepotism or self-preservation? Behav Ecol Sociobiol 17:313–323

    Article  Google Scholar 

  • Slobodchikoff CN, Kiriazis J, Fischer C, Creef E (1991) Semantic information distinguishing individual predators in the alarm calls of Gunnison’s prairie dogs. Anim Behav 42:713–719

    Article  Google Scholar 

  • Swan DC, Hare JF (2008) Signaler and receiver ages do not affect responses to Richardson’s ground squirrel alarm calls. J Mammal 89:889–894

    Article  Google Scholar 

  • Tchabovsky AV (2005) Sociality of ground squirrels: effect of body size and habitat type. Bull Moscow Soc Nat Explorers, Dept of Biology 110(4):80–88 [In Russian]

    Google Scholar 

  • Titov SV, Ermakov OA, Surin VL, Formozov AN, Kasatkin MV, Shilova SA, Shmyrov AA (2005) Molecular genetic and bioacoustic diagnostics russet (Spermophilus major Pallas, 1778) and yellow (S. fulvus Lichtenstein, 1823) ground squirrels from mixed colony. Bull Moscow Soc Naturalists 110:72–77 [In Russian]

    Google Scholar 

  • Townsend SW, Manser MB (2010) The function of nonlinear phenomena in meerkat alarm calls. Biol Lett. doi:10.1098/rsbl.2010.0537

  • Turner LW (1973) Vocal and escape responses of Spermophilus beldingi to predators. J Mammal 54:990–993

    Article  Google Scholar 

  • Vasilieva NA, Savinetskaya LE, Tchabovsky AV (2009) Large body size and short period of activity do not impede fast growth in the long-teeth ground squirrel (Spermophilus fulvus). Zool Zh 88:339–343 [In Russian]

    Google Scholar 

  • Volodin IA (2005) Individuality of alarm calls in the spotted suslik (Spermophilus suslicus, Rodentia, Sciuridae). Zool Zh 84:228–235 [In Russian]

    Google Scholar 

  • Volodin IA, Volodina EV, Matrosova VA, Savinetskaya LE, Shekarova ON, Voytsik VA (2008) Population density does not affect the alarm call characteristics in the speckled ground squirrel (Spermophilus suslicus). Lynx (Praha), ns 39(2):333–342

    Google Scholar 

  • Volodina EV, Matrosova VA, Volodin IA (2010) An unusual effect of maturation on the alarm call fundamental frequency in two species of ground squirrels. Bioacoustics 20:87–98

    Google Scholar 

  • Wilden I, Herzel H, Peters G, Tembrock G (1998) Subharmonics, biphonation, and deterministic chaos in mammal vocalization. Bioacoustics 9:171–196

    Google Scholar 

  • Wilson DR, Hare JF (2004) Ground squirrel uses ultrasonic alarms. Nature 430:523

    Article  PubMed  CAS  Google Scholar 

  • Wilson DR, Hare JF (2006) The adaptive utility of Richardson’s ground squirrel (Spermophilus richardsonii) short-range ultrasonic alarm signals. Can J Zool 84:1322–1330

    Article  Google Scholar 

Download references

Acknowledgments

We thank S.A. Shilova, A.V. Tchabovsky, L.E. Savinetskaya, O.N. Shekarova, A.F. Babitsky, S.V. Pivanova, N.A. Vasilieva, J. Matějů and P. Schnitzerová for help with data collection and to V. Vohralík and R. Frey for help with literature. We are sincerely grateful to the two anonymous reviewers for very constructive comments. This study was supported by the Russian Foundation for Basic Research, grant 09-04-00416 (for VAM, IAV, EVV), and by the Ministry of Education, Youth and Sports of the Czech Republic (project No. 0021620828) and the Ministry of the Environment of the Czech Republic (project No. SP/2d4/61/08) (for IS).

Conflict of interest

The authors do not have any conflict of interest. All funding sources are declared in the Acknowledgements.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vera A. Matrosova.

Additional information

Communicated by: Jan M. Wójcik

Rights and permissions

Reprints and permissions

About this article

Cite this article

Matrosova, V.A., Schneiderová, I., Volodin, I.A. et al. Species-specific and shared features in vocal repertoires of three Eurasian ground squirrels (genus Spermophilus). Acta Theriol 57, 65–78 (2012). https://doi.org/10.1007/s13364-011-0046-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13364-011-0046-9

Keywords

Navigation