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Cross-fostering effects on ultrasonic calls in two gerbil species
Volodin I.A., Kozhevnikova J.D., Ilchenko O.G., Sapozhnikova S.R., Volodina E.V.
P. 16-23
Mammals not experiencing vocal learning may slightly modify their voice calls (produced by vibration of the vocal folds) towards a higher similarity with conspecific groupmates. This pilot study is the first focused on interspecies social effects on whistle vocalizations (ultrasounds produced by turbulence at the vocal tract). Pup cross-fostering was applied between two related gerbil species Meriones unguiculatus and M. vinogradovi, producing acoustically different ultrasonic contact calls when adult (higher-frequency in M. vinogradovi). Calls of 3 survived foster individuals (2 M. unguiculatus and 1 M. vinogradovi) and of 22 control non-foster individuals raised by their own species (10 M. unguiculatus and 12 M. vinogradovi) were analysed bioacoustically. Call duration of non-fosters did not differ between species, whereas the fundamental and peak frequencies were lower in non-foster M. unguiculatus. Foster M. unguiculatus produced calls shorter and higher in the fundamental and peak frequencies than non-foster M. unguiculatus. Foster M. vinogradovi produced calls shorter and higher in the beginning and minimum fundamental frequencies than non-foster M. vinogradovi. We discuss that the observed trend, towards higher-frequency calls, was only expectable for foster M. unguiculatus, whereas the same trend observed in foster M. vinogradovi was opposed to the expected. These findings provide the possibility that the acoustic properties in foster M. unguiculatus are changed by social effect which apparently lacked on the calls of the foster individual M. vinogradovi. We discuss that these limited data on gerbils are consistent with published contradictory data on laboratory mice strains.

DOI: 10.15298/rusjtheriol.22.1.02

References

  • Arriaga G. & Jarvis E.D. 2013. Mouse vocal communication system: Are ultrasounds learned or innate? // Brain & Language. Vol.124. P.96–116.

  • Arriaga G., Zhou E.P. & Jarvis E.D. 2012. Of mice, birds, and men: the mouse ultrasonic song system has some features similar to humans and song-learning birds // PLoS ONE. Vol.7. P.e46610.

  • Azola A., Palmer J., Mulheren R., Hofer R., Fischmeister F. & Fitch W.T. 2018. The physiology of oral whistling: a combined radiographic and MRI analysis // Journal of Applied Physiology. Vol.124. P.34–39.

  • Barker A.J., Veviurko G., Bennett N.C., Hart D.W., Mograby L. & Lewin G.R. 2021. Cultural transmission of vocal dialect in the naked mole-rat // Science. Vol.371. P.503–507.

  • Bowling D.L., Garcia M., Dunn J.C., Ruprecht R., Stewart A., Frommolt K.-H. & Fitch W.T. 2017. Body size and vocalization in primates and carnivores // Scientific Reports. Vol.7. P.e41070.

  • Briefer E.F. & McElligott A.G. 2012. Social effects on vocal ontogeny in an ungulate, the goat, Capra hircus // Animal Behaviour. Vol.83. P.991–1000.

  • Chabout J., Serreau P., Ey E., Bellier L., Aubin T., Bourgeron T. & Granon S. 2012. Adult male mice emit context-specific ultrasonic vocalizations that are modulated by prior isolation or group rearing environment // PLoS ONE. Vol.7. P.e29401.

  • Charlton B.D. & Reby D. 2016. The evolution of acoustic size exaggeration in terrestrial mammals // Nature Communication. Vol.7. P.e12739.

  • Crockford C., Herbinger I., Vigiland L. & Boesch C. 2004. Wild chimpanzees produce group-specific calls: a case for vocal learning? // Ethology. Vol.110. P.221–243.

  • Dymskaya M.M., Volodin I.A., Smorkatcheva A.V., Vasilieva N.A. & Volodina E.V. 2022. Audible, but not ultrasonic, calls reflect surface-dwelling or subterranean specialization in pup and adult Brandt’s and mandarin voles // Behavioral Ecology and Sociobiology. Vol.76. P.e106.

  • Finck C. & Lejeune L. 2010. Structure and oscillatory function of the vocal folds // Brudzynski S.M. (ed.). Handbook of Mammalian Vocalization. Amsterdam: Elsevier. P.427–438.

  • Fitch W.T. & Hauser M.D. 2002. Unpacking “Honesty”: Vertebrate vocal production and the evolution of acoustic signals // Simmons A., Fay R.R. & Popper A.N. (eds.). Acoustic Communication (Springer Handbook of Auditory Research). New York: Springer. P.65–137.

  • Garcia M., Herbst C.T., Bowling D.L., Dunn J.C. & Fitch W.T. 2017. Acoustic allometry revisited: morphological determinants of fundamental frequency in primate vocal production // Scientific Reports. Vol.7. P.e10450.

  • Håkansson J., Jiang W., Xue Q., Zheng X., Ding M., Agarwal A.A. & Elemans C.P.H. 2022. Aerodynamics and motor control of ultrasonic vocalizations for social communication in mice and rats // BMC Biology. Vol.20. P.e3.

  • Hammerschmidt K., Reisinger E., Westekemper K., Ehrenreich L., Srenzke N. & Fischer J. 2012. Mice do not require auditory input for the normal development of their ultrasonic vocalizations // BMC Neuroscience. Vol.13. P.e40.

  • Holy T.E. & Guo Z. 2005. Ultrasonic songs of male mice // PLoS Biology. Vol.3. P.e386.

  • Janik V.M. & Knörnschild M. 2021. Vocal production learning in mammals revisited // Philosophical Transactions of the Royal Society B. Vol.376. P.e20200244.

  • Janik V.M. & Slater P.J.B. 2000. The different roles of social learning in vocal communication // Animal Behaviour. Vol.60. P.1–11.

  • Johnson S.A., Painter M.S., Javurek A.B., Murphy C.R., Howald E.C., Khan Z.Z., Conard C.M., Gant K.L., Ellersieck M.R., Hoffmann F., Schenk A.K. & Rosenfeld C.S. 2017. Characterization of vocalizations emitted in isolation by California mouse (Peromyscus californicus) pups throughout the postnatal period // Journal of Comparative Psychology. Vol.131. P.30–39.

  • Kikusui T., Nakanishi K., Nakagawa R., Nagasawa M., Mogi K. & Okanoya K. 2011. Cross fostering experiments suggest that mice songs are innate // PLoS ONE. Vol.6. P.e17721.

  • Klenova A.V., Volodin I.A., Ilchenko O.G. & Volodina E.V. 2021. Discomfort-related changes of call rate and acoustic variables of ultrasonic vocalizations in adult yellow steppe lemmings Eolagurus luteus // Scientific Reports. Vol.11. P.e14969.

  • Kobayasi K.I. & Riquimaroux H. 2012. Classification of vocalizations in the Mongolian gerbil, Meriones unguiculatus // Journal of the Acoustical Society of America. Vol.131. P.1622–1631.

  • Kozhevnikova J.D., Volodin I.A., Zaytseva A.S., Ilchenko O.G. & Volodina E.V. 2021. Pup ultrasonic isolation calls of six gerbil species and the relationship between acoustic traits and body size // Royal Society Open Science. Vol.8. P.e201558.

  • Lattenkamp E.Z., Hörpel S.G., Mengede J. & Firzlaff U. 2021. A researcher’s guide to the comparative assessment of vocal production learning // Philosophical Transactions of the Royal Society B. Vol.376. P.e20200237.

  • Lemasson A., Gautier J.-P. & Hausberger M. 2003. Vocal similarities and social bonds in Campbell’s monkey (Cercopithecus campbelli) // Comptes Rendus Biologies. Vol.326. P.1185–1193.

  • Lemasson A., Ouattara K., Petit E.J. & Zuberbühler K. 2011. Social learning of vocal structure in a nonhuman primate? // BMC Evolutionary Biology. Vol.11. P.e362.

  • Lopez-Salesansky N., Wells D.J., Chancellor N., Whitfield L. & Burn C.C. 2021. Handling mice using gloves sprayed with alcohol-based hand sanitiser: acute effects on mouse behaviour // Animal Technology and Welfare. Vol.20. No.1. P.11–20.

  • Mahrt E., Agarwal A., Perkel D., Portfors C. & Elemans C.P.H. 2016. Mice produce ultrasonic vocalizations by intra-laryngeal planar impinging jets // Current Biology. Vol.26. P.R865–R881.

  • Mahrt E.J., Perkel D.J., Tong L., Rubel E.W. & Portfors C.V. 2013. Engineered deafness reveals that mouse courtship vocalizations do not require auditory experience. Journal of Neuroscience. Vol.33. P.5573–5583.

  • McComb K., Taylor A.M., Wilson C. & Charlton B.D. 2009. The cry embedded within the purr // Current Biology. Vol.19. P.R507–R508.

  • Nicastro N. 2004. Perceptual and acoustic evidence for species-level differences in meow vocalizations by domestic cats (Felis catus) and African wild cats (Felis silvestris lybica) // Journal of Comparative Psychology. Vol.118. P.287–296.

  • Owings D.H. & Morton E.S. 1998. Animal Vocal Communication: A New Approach. Cambridge: Cambrige Univ. Press. 284 p.

  • Pasch B., Abbasi M.Z., Wilson M., Zhao D., Searle J.B., Webster M.S. & Rice A.N. 2016. Cross-fostering alters advertisement vocalizations of grasshopper mice (Onychomys): Evidence for the developmental stress hypothesis // Physiology & Behavior. Vol.157. P.265–269.

  • Pasch B., Tokuda I.T. & Riede T. 2017. Grasshopper mice employ distinct vocal production mechanisms in different social contexts // Proceedings of the Royal Society B. Vol.284. P.e20171158.

  • Riede T. 2011. Subglottal pressure, tracheal airflow, and intrinsic laryngeal muscle activity during rat ultrasound vocalization // Journal of Neurophysiology. Vol.106. P.2580–2592.

  • Riede T. 2013. Stereotypic laryngeal and respiratory motor patterns generate different call types in rat ultrasound vocalization // Journal of Experimental Zoology, Part A. Vol.319. P.213–224.

  • Riede T., Borgard H.L. & Pasch B. 2017. Laryngeal airway reconstruction indicates that rodent ultrasonic vocalizations are produced by an edge-tone mechanism // Royal Society Open Science. Vol.4. P.e170976.

  • Riede T. & Pasch B. 2020. Pygmy mouse songs reveal anatomical innovations underlying acoustic signal elaboration in rodents // Journal of Experimental Biology. Vol.223. P.jeb.223925.

  • Riede T., York A., Furst S., Müller R. & Seelecke S. 2011. Elasticity and stress relaxation of a very small vocal fold // Journal of Biomechanics. Vol. 44. P.1936–1940.

  • Rukstalis M., Fite J.E. & French J.A. 2003. Social change affects vocal structure in a callitrichid primate (Callitrix kuhlii) // Ethology. Vol.109. P.327–340.

  • Snowdon C.T. & Elowson A.M. 1999. Pygmy marmosets modify call structure when paired // Ethology. Vol.105. P.893–908.

  • 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. Vol.112. P.7–21.

  • Ter-Mikaelian M., Yapa W.P. & Rübsamen R. 2012. Vocal behavior of the Mongolian gerbil in a seminatural enclosure // Behaviour. Vol.149. P.461–492.

  • Vernes S.C., Janik V.M., Fitch W.T. & Slater P.J.B. 2021. Vocal learning in animals and humans // Philosophical Transactions of the Royal Society B. Vol.376. P.e20200234.

  • Volodin I.A., Ilchenko O.G. & Popov S.V. 1996. [Gerbils: Captive Management and Population Demography of Different Species in Laboratory]. Moscow: Moscow Zoo Press. 233 p. [in Russian].

  • Volodin I.A., Volodina E.V., Lapshina E.N., Efremova K.O. & Soldatova N.V. 2014. Vocal group signatures in the goitred gazelle Gazella subgutturosa // Animal Cognition. Vol.17. No.2. P.349–357.

  • Volodin I.A., Yurlova D.D., Ilchenko O.G. & Volodina E.V. 2021. Ontogeny of audible squeaks in yellow steppe lemming Eolagurus luteus: trend towards shorter and low-frequency calls is reminiscent of those in ultrasonic vocalization // BMC Zoology. Vol.6. P.e27.

  • Yurlova D.D., Volodin I.A., Ilchenko O.G. & Volodina E.V. 2020. Rapid development of mature vocal patterns of ultrasonic calls in a fast-growing rodent, the yellow steppe lemming (Eolagurus luteus) // PLoS ONE. Vol.15. P.e0228892.

  • Zaytseva A.S., Volodin I.A., Ilchenko O.G. & Volodina E.V. 2019. Ultrasonic vocalization of pup and adult fat-tailed gerbils (Pachyuromys duprasi) // PLoS ONE. Vol.14. P.e0219749.

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