Advertisement

Behavioral Ecology and Sociobiology

, Volume 62, Issue 2, pp 181–191 | Cite as

Pups crying bass: vocal adaptation for avoidance of age-dependent predation risk in ground squirrels?

  • Vera A. Matrosova
  • Ilya A. Volodin
  • Elena V. Volodina
  • Andrey F. Babitsky
Original Paper

Abstract

In most mammals, larger adult body size correlates with lower fundamental frequency and more closely spaced formants in vocalizations relative to juveniles. In alarm whistles of two free-living rodents, the speckled ground squirrel Spermophilus suslicus and yellow ground squirrel S. fulvus, these cues to body size were absent despite prominent differences in body weight and skull and larynx sizes between juveniles and adults. No significant correlations were found between the individual maximum fundamental frequency and body weight, both within age classes and for pooled samples of all animals within species. Furthermore, the mean alarm whistle maximum fundamental frequencies did not differ significantly between age classes (juvenile versus adult) in the speckled squirrel and were even significantly lower in juvenile yellow squirrels. We discuss the hypothesis that the obfuscation of vocal differences between juvenile and adult squirrels may represent a special adaptation of pup vocal behaviour—a form of “vocal mimicry,” resulting in imitation of adult vocal pattern to avoid infanticide and age-dependent predation risk.

Keywords

Spermophilus suslicus Spermophilus fulvus Alarm call Vocal mimicry Infanticide Antipredator behaviour 

Notes

Acknowledgments

We thank S.A. Schilova, A.V. Tchabovsky, L.E. Savinetskaya, N.A. Stukolova, and V.S. Popov for collaboration in the field, and M.M. Nagaylik, D.I. Volodina and A.I. Volodin for help with data collection. We sincerely appreciate the assistance of F.J. Dzerjinsky, V.S. Lebedev, and O.G. Iltchenko with the morphological part of our study. We thank A.A. Nikol’skii, O.A. Filatova, T. Riede, and R. Frey for valuable comments and are sincerely grateful to J.F. Hare, D. Blumstein, and an anonymous referee, whose comments were useful and inspiring. This study was supported by the Russian Foundation for Basic Research (grant 06-04-48400). During our work, we adhered to the Guidelines for the Use of Animals in Research (Animal Behaviour, 2006, 71: 245–253) and to the laws of Russian Federation, the country where the research was conducted.

References

  1. Babitsky AF, Tchabovsky AV, Savinetskaya LE (2006) Reproductive costs in female speckled ground squirrels. Bulletin MOIP Ser Biol 111(5):80–83 (in Russian)Google Scholar
  2. 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. U. Chicago Press, Chicago, pp 317–327Google Scholar
  3. Blumstein DT, Arnold W (1995) Situational specificity in alpine-marmot alarm communication. Ethology 100:1–13CrossRefGoogle Scholar
  4. Blumstein DT, Daniel JC (2004) Yellow-bellied marmots discriminate between the alarm calls of individuals and are more responsive to calls from juveniles. Anim Behav 68:1257–1265CrossRefGoogle Scholar
  5. Blumstein DT, Munos O (2005) Individual, age and sex-specific information is contained in yellow-bellied marmot alarm calls. Anim Behav 69:353–361CrossRefGoogle Scholar
  6. Collins SA (2000) Men’s voices and women’s choices. Anim Behav 60:773–780PubMedCrossRefGoogle Scholar
  7. Ebensperger LA (1998) Strategies and counterstrategies to infanticide in mammals. Biol Rev 73:321–346CrossRefGoogle Scholar
  8. Ebensperger LA, Blumstein DT (2007) Functions of non-parental infanticide in rodents. In: Wolff JO, Sherman PW (eds) Rodent societies. U. Chicago Press, Chicago, pp 267–279Google Scholar
  9. Elowson AM, Snowdon CT, Sweet CJ (1992) Ontogeny of trill and j-call vocalizations in the pygmy marmoset Cebuella pygmaea. Anim Behav 43:703–715CrossRefGoogle Scholar
  10. Fant G (1960) Acoustic theory of speech production. The Hague, MoutonGoogle Scholar
  11. Fitch WT (1997) Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. J Acoust Soc Am 102:1213–1222PubMedCrossRefGoogle Scholar
  12. Fitch WT (1999) Acoustic exaggeration of size in birds via tracheal elongation: comparative and theoretical analyses. J Zool Lond 248:31–48CrossRefGoogle Scholar
  13. Fitch WT (2000) Skull dimensions in relation to body size in nonhumans mammals: the causal bases for acoustic allometry. Zoology Anal Complex Syst 103:40–58Google Scholar
  14. Fitch WT, Giedd J (1999) Morphology and development of the human vocal tract: a study using magnetic resonance imaging. J Acoust Soc Am 106:1511–1522PubMedCrossRefGoogle Scholar
  15. Fitch WT, Hauser MD (1995) Vocal production in nonhuman primates: acoustic, physiology, and functional constraints on “honest” advertisement. Am J Primatol 37:191–219CrossRefGoogle Scholar
  16. Fitch WT, Hauser MD (2002) Unpacking “honesty”: vertebrate vocal production and the evolution of acoustic signals. In: Simmons A, Fay RR, Popper AN (eds) Acoustic communication, springer handbook of auditory research. Springer, Berlin, pp 65–137Google Scholar
  17. Gebauer A, Kaiser M (1998) Anmerkungen zur Lautenwicklung und zum Stimmbruch beim Grauen Kranich (Grus grus). Brandenburgische Umwelt Berichte 3:25–33Google Scholar
  18. Hanson MT, Coss RG (2001) Age differences in the response of California ground squirrels (Spermophilus beecheyi) to conspecific alarm calls. Ethology 107:259–275CrossRefGoogle Scholar
  19. Hare JF (1991) Intraspecific killing of pre-weaned young in the Columbian ground squirrel, Spermophilus columbianus. Can J Zool 69:797–800CrossRefGoogle Scholar
  20. Hare JF (1998) Juvenile Richardson's ground squirrels, Spermophilus richardsonii, discriminate among individual alarm callers. Anim Behav 55:451–460PubMedCrossRefGoogle Scholar
  21. Hartwig S (2005) Individual acoustic identification as a non-invasive conservation tool: an approach to the conservation of the African wild dog Lycaon pictus (Temminck, 1820). Bioacoustics 15:35–50Google Scholar
  22. Hoogland JL (1995) The black-tailed prairie dog: social life of a burrowing mammal. University of Chicago Press, ChicagoGoogle Scholar
  23. Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethology and Sociobiol 1:13–40CrossRefGoogle Scholar
  24. Inoue M (1988) Age gradation in vocalization and body weight in Japanese monkeys (Macaca fuscata). Folia Primatol 51:76–86PubMedCrossRefGoogle Scholar
  25. Ismagilov MI (1952) A description of a population of the yellow ground squirrel at Barsa-Kelmes Island. Zoologichesky Zhurnal 31:932–939 (in Russian)Google Scholar
  26. Ismagilov MI (1969) Yellow ground squirrel–Citellus fulvus. In: Sludskiy AA (ed) Mammals of Kazakhstan, v. 1, Rodents (Marmots and ground squirrels). Science, Alma-Ata, pp 120–159 [in Russian]Google Scholar
  27. Lass NJ, Brown WS (1978) Correlational study of speakers heights, weights, body surface areas and speaking fundamental frequencies. J Acoust Soc Am 63:1218–1220PubMedCrossRefGoogle Scholar
  28. Leger DW, Owings DH, Boal LM (1979) Contextual information and differential responses to alarm whistles in California ground squirrels. Z Tierpsychol 49:142–155Google Scholar
  29. Lobkov VA (1999) The speckled ground squirrel of north-western shores of the Black sea: biology and population dynamics. Astroprint, Odessa (in Russian)Google Scholar
  30. Loughry WJ, McDonough CM (1989) Calling and vigilance in California ground squirrels: age, sex and seasonal differences in responses to calls. Am Midl Nat 121:312–321CrossRefGoogle Scholar
  31. McComb KE (1991) Female choice for high roaring rates in red deer, Cervus elaphus. Anim Behav 41:79–88CrossRefGoogle Scholar
  32. McCowan B, Hooper SL (2002) Individual acoustic variation in Belding’s ground squirrel alarm chirps in the High Sierra Nevada. J Acoust Soc Am 111:1157–1160PubMedCrossRefGoogle Scholar
  33. McLean IG (1983) Paternal behaviour and killing of young in arctic ground squirrels. Anim Behav 31:32–44CrossRefGoogle Scholar
  34. McShane LJ, Estes JA, Riedman ML, Staedler MM (1995) Repertoire, structure, and individual variation of vocalizations in the sea otter. J Mammal 76:414–427CrossRefGoogle Scholar
  35. Morton ES (1977) On the occurrence and significance of motivation—structural rules in some bird and mammal sounds. Am Natur 111:855–869CrossRefGoogle Scholar
  36. Nesterova NL (1996) Age-dependent alarm behavior and response to alarm call in bobac marmots (Marmota bobac Mull.). In: Le Berre M, Ramousse R, Le Guelte L (eds) Biodiversity in marmots. International network on marmots, Moscow-Lyon, pp 181–186Google Scholar
  37. Niemeier MM (1979) Structural and functional aspects of vocal ontogeny in Grus canadensis (Gruidae: Aves). PhD thesis, Univ. of Nebraska, LincolnGoogle Scholar
  38. Nikol’skii AA (1979) Species specificity of alarm call in sousliks (Citellus, Sciuridae) of Eurasia. Zoologichesky Zhurnal 58:1183–1194 (in Russian)Google Scholar
  39. Nikol’skii AA (2007) A comparative analysis of the alarm call frequency in different age rodent groups. Zoologichesky Zhurnal 86:499–504 (in Russian)Google Scholar
  40. Nikol’skii AA, Vinogradov NS (2000) Burrows of mammals as acoustic devices: a study of the bobac burrow as an example. Doklady Biological Sciences 374:509–513 (Doklady Akademii Nauk 374:422–426 [in Russian])PubMedGoogle Scholar
  41. Nikol’skii AA, Denisov VP, Stoiko TG, Formosov NA (1984) The alarm call in F1 hybrids Citellus pygmaeus X C. suslicus (Sciuridae, Rodentia). Zoologichesky Zhurnal 63:1216–1225 (in Russian)Google Scholar
  42. Owings DH, Loughry WJ (1985) Variation in snake-elicited jump-yipping by black-tailed prairie dogs: ontogeny and snake specificity. Z Tierpsychol 70:177–200Google Scholar
  43. Owings DH, Morton ES (1998) Animal vocal communication: a new approach. Cambridge Univ. Press, CambridgeGoogle Scholar
  44. 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 Press, New York, pp 299–346Google Scholar
  45. Peters G (1978) Vergleichende Untersuchung zur Lautgebund einiger Feliden (Mammalia, Felidae). Zeit Zool Spixiana 1:1–283Google Scholar
  46. Riede T, Fitch WT (1999) Vocal tract length and acoustics of vocalization in the domestic dog (Canis familiaris). J Exp Biol 202:2859–2867PubMedGoogle Scholar
  47. Sherman PW (1981) Reproductive competition and infanticide in Belding’s ground squirrels and other animals. In: Alexander RD, Tinkle RW (eds) Natural selection and social behavior: recent research and new theory. Chiron Press, New York, pp 311–331Google Scholar
  48. Sloan JL, Wilson DR, Hare JF (2005) Functional morphology of Richardson's ground squirrel (Spermophilus richardsonii) alarm calls: the meaning of chirps, whistles and chucks. Anim Behav 70:937–944CrossRefGoogle Scholar
  49. Tanaka T, Sugiura H, Masataka N (2006) Cross-sectional and longitudinal studies of the development of group differences in acoustic features of coo calls in two groups of Japanese macaques. Ethology 112:7–21CrossRefGoogle Scholar
  50. Titov SV, Ermakov OA, Surin VL, Formozov NA, Kasatkin MV, Schilova SA, Schmyrov AA (2005) Molecular genetic and bioacoustic diagnostics russet (Spermophilus major Pallas, 1778) and yellow (S. fulvus Lichtenstein, 1823) ground squirrels from mixed colony. Bulletin MOIP Ser Biol 110:72–77 (in Russian)Google Scholar
  51. Titze IR (1994) Principles of voice production. Prentice Hall, Englewood CliffsGoogle Scholar
  52. Trulio LA (1996) The functional significance of infanticide in a population of California ground squirrels (Spermophilus beecheyi). Behav Ecol Sociobiol 38:97–103CrossRefGoogle Scholar
  53. Volodin IA (2005) Individuality in the alarm call of the speckled suslik Spermophilus suslicus (Rodentia, Sciuridae). Zoologichesky Zhurnal 84:228–235 (in Russian)Google Scholar
  54. Volodina EV (1998) Infantile call characteristics in the cheetah in captivity are clues to the recognition of an animal’s self-esteem as being strong or weak. Scientific Research in Zoological Parks 10:143–159 (in Russian)Google Scholar
  55. Volodina EV (2000) Vocal repertoire of cheetah Acinonyx jubatus (Carnivora, Felidae) in captivity: sound structure and search for means of assessing the state of adult animals. Entomological Review 80:S368–S378 (Zoologichesky Zhurnal 79:833–843 [in Russian])Google Scholar
  56. Waterman JM (1984) Infanticide in the Columbian ground squirrel, Spermophilus columbianus. J Mammal 65:137–138CrossRefGoogle Scholar
  57. Wilden I (1997) Phonetische Variabilität in der Lautgebung Afrikanischer Wildhunde (Lycaon pictus) und deren frühe Ontogenese. Shaker Verlag, AachenGoogle Scholar
  58. Wilson DR, Hare JF (2004) Ground squirrel uses ultrasonic alarms. Nature 430:523PubMedCrossRefGoogle Scholar
  59. Wilson DR, Hare JF (2006) The adaptive utility of Richardson’s ground squirrel (Spermophilus richardsonii) short-range ultrasonic alarm signals. Can J Zool 84:1322–1330CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Vera A. Matrosova
    • 1
  • Ilya A. Volodin
    • 1
    • 2
  • Elena V. Volodina
    • 2
  • Andrey F. Babitsky
    • 3
  1. 1.Department of Vertebrate Zoology, Faculty of BiologyLomonosov Moscow State UniversityMoscowRussia
  2. 2.Scientific Research DepartmentMoscow ZooMoscowRussia
  3. 3.Severtsov Institute of Ecology and EvolutionRussian Academy of SciencesMoscowRussia

Personalised recommendations