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

• Autorzy: Matrosova V. A. , Schneiderova I. , Volodin I. A. , Volodina E. V.
• Języki publikacji: EN

Abstrakty

EN

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.

Słowa kluczowe

EN

animal species; specificity; vocal repertoire; Eurasian ground squirrel; squirrel; Spermophilus; nonlinear phenomenon; Spermophilus citellus; Spermophilus fulvus; Spermophilus suslicus; vocal diversity; ultrasound

• Wydawca: -
• Czasopismo: Acta Theriologica
• Rocznik: 2012
• Tom: 57
• Numer: 1
• Opis fizyczny: p.65-78,fig.,ref.

Twórcy

autor

Matrosova V. A.

• Department of Vertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, Vorobievy Gory, 12/1, Moscow, 119991, Russia
• Engelhardt Institute of Molecular Biology RAS, Vavilov Str., 32, Moscow, 119991, Russia

autor

Schneiderova I.

• Department of Zoology, Faculty of Sciences, Charles University, Viničná, 7, Prague 2, 128 44, Czech Republic

autor

Volodin I. A.

• Department of Vertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, Vorobievy Gory, 12/1, Moscow, 119991, Russia

autor

Volodina E. V.

• Scientific Research Department, Moscow Zoo, B. Gruzinskaya, 1, Moscow, 123242, Russia

Bibliografia

• Balph DM, Balph DF (1966) Sound communication of Uinta ground squirrels. J Mammal 47:440–450
• Betts BJ (1976) Behaviour in a population of Columbian ground squirrels, Spermophilus columbianus columbianus. Anim Behav 24:652–680
• 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
• 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
• 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
• Davis LS (1984) Alarm calling in Richardson’s ground squirrels (Spermophilus richardsonii). Z Tierpsychol 66:152–164
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Helgen KM, Cole FR, Helgen LE, Wilson DE (2009) Generic revision in the holarctic ground squirrel genus Spermophilus. J Mammal 90:270–305
• Kashkarov D, Lein L (1927) The yellow ground squirrel of Turkestan, Cynomys fulvus oxianus Thomas. Ecology 8:63–72
• Koeppl JW, Hoffman RS, Nadler CF (1978) Pattern analysis of acoustical behavior in four species of ground squirrels. J Mammal 59:677–696
• 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
• 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
• Leger DW, Berney-Key SD, Sherman PW (1984) Vocalizations of Belding’s ground squirrels (Spermophilus beldingi). Anim Behav 32:753–764
• Macedonia JME, Evans CS (1993) Variation among mammalian alarm call systems and the problem of meaning in animal signals. Ethology 93:177–197
• 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
• 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]
• 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
• 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
• Matrosova VA, Volodin IA, Volodina EV (2009) Short-term and long-term individuality in speckled ground squirrel alarm calls. J Mammal 90:158–166
• 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
• 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
• 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
• 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
• Melchior HR (1971) Characteristics of arctic ground squirrel alarm calls. Oecologia 7:184–190
• Nikoĺskii AA (1979) Species specifity of alarm call in sousliks (Citellus, Sciuridae) of Eurasia. Zool Zh 58:1183–1194 [In Russian]
• 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]
• 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]
• Nowak RM (1999) Walker’s mammals of the world, 6th edn. John Hopkins Univ. Press, Baltimore
• Owings DH, Leger DW (1980) Chatter vocalizations of California ground squirrels: predator- and social-role specifity. Z Tierpsychol 54:163–184
• Owings DH, Virginia RA (1978) Alarm calls of California ground squirrels (Spermophilus beecheyi). Z Tierpsychol 46:58–70
• 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
• Pollard KA, Blumstein DT (2011) Social group size predicts the evolution of individuality. Curr Biol 21:413–417
• Robinson SR (1981) Alarm communication in Belding’s ground squirrels. Z Tierpsychol 56:150–168
• 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
• 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
• Shekarova ON, Neronov VV, Savinetskaya LE (2008) Speckled ground squirrel (Spermophilus suslicus): current distribution, population dynamics and conservation. Lynx (Praha) ns 39:317–322
• Sherman PW (1977) Nepotism and the evolution of alarm calls. Science 197:1246–1253
• Sherman PW (1985) Alarm calls of Belding’s ground squirrels to aerial predators: nepotism or self-preservation? Behav Ecol Sociobiol 17:313–323
• 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
• 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
• 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]
• 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]
• 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
• 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]
• Volodin IA (2005) Individuality of alarm calls in the spotted suslik (Spermophilus suslicus, Rodentia, Sciuridae). Zool Zh 84:228–235 [In Russian]
• 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
• 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
• Wilden I, Herzel H, Peters G, Tembrock G (1998) Subharmonics, biphonation, and deterministic chaos in mammal vocalization. Bioacoustics 9:171–196
• Wilson DR, Hare JF (2004) Ground squirrel uses ultrasonic alarms. Nature 430:523
• 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