Skip to main content

Advertisement

SpringerLink
Log in

The gradual vocal responses to human-provoked discomfort in farmed silver foxes

  • Original Paper
  • Published:
acta ethologica Aims and scope Submit manuscript

Abstract

Vocal indicators of welfare have proven their use for many farmed and zoo animals and may be applied to farmed silver foxes as these animals display high vocal activity toward humans. Farmed silver foxes were selected mainly for fur, size, and litter sizes, but not for attitudes to people, so they are fearful of humans and have short-term welfare problems in their proximity. With a human approach test, we designed here the steady increase and decrease of fox–human distance and registered vocal responses of 25 farmed silver foxes. We analyzed the features of vocalizations produced by the foxes at different fox–human distances, assuming that changes in vocal responses reflect the degrees of human-related discomfort. For revealing the discomfort-related vocal traits in farmed silver foxes, we proposed and tested the algorithm of “joint calls,” equally applicable for analysis of all calls independently on their structure, either tonal or noisy. We discuss that the increase in proportion of time spent vocalizing and the shift of call energy toward higher frequencies may be integral vocal characteristics of short-term welfare problems in farmed silver foxes and probably in other captive mammals.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ahola L, Mononen J (2002) Family break-up in farmed silver foxes (Vulpes vulpes) housed in enlarged cage systems as families. Acta Ethologica 4:125–127. doi:10.1007/s10211-001-0057-7

    Article  Google Scholar 

  • Bachorowski J-A, Smoski MJ, Owren MJ (2001) The acoustic features of human laughter. J Acoust Soc Am 110(3):1581–1597. doi:10.1121/1.1391244

    Article  CAS  PubMed  Google Scholar 

  • Bakken M (1998) The effect of an improved man–animal relationship on sex-ratio in litters and on growth and behaviour in cubs among farmed silver foxes (Vulpes vulpes). Appl Anim Behav Sci 56:309–317. doi:10.1016/S0168-1591(97)00088-9

    Article  Google Scholar 

  • Bakken M, Moe RO, Smith AJ, Selle G-ME (1999) Effects of environmental stressors on deep body temperature and activity levels in silver fox vixens (Vulpes vulpes). Appl Anim Behav Sci 64:141–151. doi:10.1016/S0168-1591(99)00022-2

    Article  Google Scholar 

  • Blumstein DT, Armitage KB (1997) Alarm calling in yellow-bellied marmots: I. The meaning of situationally specific calls. Anim Behav 53:143–171. doi:10.1006/anbe.1996.0285

    Article  Google Scholar 

  • Blumstein DT, Patton ML, Saltzman W (2006) Faecal glucocorticoid metabolites and alarm calling in free-living yellow-bellied marmots. Biol Lett 2:29–32. doi:10.1098/rsbl.2005.0405

    Article  CAS  PubMed  Google Scholar 

  • Braastad BO (1987) Abnormal behaviour in farmed silver fox vixens (Vulpes vulpes L.): tail-biting and infanticide. Appl Anim Behav Sci 17:376–377. doi:10.1016/0168-1591(87)90171-7

    Article  Google Scholar 

  • Braastad BO (1996) Behaviour of silver foxes in traditional breeding boxes and in boxes with an entrance tunnel. Anim Welf 5:155–166

    Google Scholar 

  • Broom DM, Johnson KG (1993) Stress and animal welfare. Chapman & Hall, London

    Google Scholar 

  • Coss RG, McCowan B, Ramakrishnan U (2007) Threat-related acoustical differences in alarm calls by wild bonnet macaques (Macaca radiata) elicited by python and leopard models. Ethology 113:352–367. doi:10.1111/j.1439-0310.2007.01336.x

    Article  Google Scholar 

  • Fichtel C, Hammerschmidt K, Jürgens U (2001) On the vocal expression of emotion, a multi-parametric analysis of different states of aversion in the squirell monkey. Behaviour 97:97–116. doi:10.1163/15685390151067094

    Article  Google Scholar 

  • Fischer J, Hammerschmidt K, Todt D (1995) Factors affecting acoustic variation in Barbary macaque (Macaca sylvanus) disturbance calls. Ethology 101:51–66

    Article  Google Scholar 

  • Gogoleva SS, Volodin IA, Volodina EV, Kharlamova AV, Trut LN (2009) Kind granddaughters of angry grandmothers: the effect of domestication on vocalization in cross-bred silver foxes. Behav Processes 81:369–375. doi:10.1016/j.beproc.2009.03.012

    Article  PubMed  Google Scholar 

  • Gogoleva SS, Volodin IA, Volodina EV, Trut LN (2008) To bark or not to bark: Vocalization in red foxes selected for tameness or aggressiveness toward humans. Bioacoustics 18:99–132

    Google Scholar 

  • Grandin T (1998) The feasibility of using vocalization scoring as an indicator of poor welfare during cattle slaughter. Appl Anim Behav Sci 56:121–128. doi:10.1016/S0168-1591(97)00102-0

    Article  Google Scholar 

  • Jahns G (2008) Call recognition to identify cow conditions—a call-recogniser translating calls to text. Comput Electron Agric 62:54–58. doi:10.1016/j.compag.2007.09.005

    Google Scholar 

  • Jürgens U (1976a) Reinforcing concomitants of electrically elicited vocalizations. Exp Brain Res 26:203–214. doi:10.1007/BF00238284

    Article  PubMed  Google Scholar 

  • Jürgens U (1976b) Positive and negative reinforcing properties of electrically elicitable vocalizations in the squirrel monkey. In: Wauquier A, Rolls ET (eds) Brain stimulation reward. Elsevier, Amsterdam, pp 397–402

    Google Scholar 

  • Jürgens U (1979) Vocalization as an emotional indicator: a neuroethological study in the squirrel monkey. Behaviour 69:88–117. doi:10.1163/156853979X00412

    Article  PubMed  Google Scholar 

  • Jürgens U (2009) The neural control of vocalization in mammals: a review. J Voice 23:1–10. doi:10.1016/j.jvoice.2007.07.005

    Article  PubMed  Google Scholar 

  • Jürgens U, Ploog D (1970) Cerebral representations of vocalization in squirrel monkey. Exp Brain Res 10:532–554. doi:10.1007/BF00234269

    Article  PubMed  Google Scholar 

  • Jürgens U, Ploog D (1981) On the neural control of mammalian vocalization. Trends Neurosci 4:135–137. doi:10.1016/0166-2236(81)90045-X

    Article  Google Scholar 

  • Kirchhof J, Hammerschmidt K, Fuchs E (2001) Aggression and dominance in tree shrews (Tupaia belangeri). Agonistic behaviour is reflected in vocal patterns. In: Martinez M (ed) Prevention and control of aggression and the impact on its victims. Kluwer, New York, pp 409–414

    Google Scholar 

  • Kukekova AV, Trut LN, Chase K, Shepeleva DV, Vladimirova AV, Kharlamova AV, Oskina IN, Stepika A, Klebanov S, Erb HN, Acland GM (2008) Measurement of segregating behaviors in experimental silver fox pedigrees. Behav Genet 38:185–194. doi:10.1007/s10519-007-9180-1

    Article  PubMed  Google Scholar 

  • Lay DC, Friend ТН, Bowers CL, Grissom KK, Jenkins OC (1992a) A comparative physiological and behavioral study of freeze and hot-iron branding using dairy cows. J Anim Sci 70:1121–1125

    PubMed  Google Scholar 

  • Lay DC, Friend ТН, Randell RD, Bowers CL, Grissom KK, Jenkins OC (1992b) Behavioral and physiological effects of freeze or hot-iron branding on crossbred cattle. J Anim Sci 70:330–336

    PubMed  Google Scholar 

  • Manser MB (2001) The acoustic structure of suricates’ alarm calls varies with predator type and the level of response urgency. Proc R Soc B 268:2315–2324. doi:10.1098/rspb.2001.1773

    Article  CAS  PubMed  Google Scholar 

  • Manteuffel G, Puppe B, Schön PC (2004) Vocalization of farm animals as a measure of welfare. Appl Anim Behav Sci 88:163–182. doi:10.1016/j.applanim.2004.02.012

    Article  Google Scholar 

  • Marchant JN, Whittaker X, Broom DM (2001) Vocalisations of the adult female domestic pig during a standard human approach test and their relationships with behavioural and heart rate measures. Appl Anim Behav Sci 72:23–39. doi:10.1016/S0168-1591(00)00190-8

    Article  PubMed  Google Scholar 

  • Moe RO, Bakken M (1997) Effects of handling and physical restraint on rectal temperature, cortisol, glucose and leucocyte counts in the silver fox (Vulpes vulpes). Acta Vet Scand 38:29–39

    CAS  PubMed  Google Scholar 

  • Moe RO, Bakken M (1998) Anxiolytic drugs inhibit hyperthermia induced by handling in farmed silver foxes (Vulpes vulpes). Anim Welf 7:97–100

    Google Scholar 

  • Moe RO, Bakken M, Kittilsen S, Kingsley-Smith H, Spruijt BM (2006) A note on reward-related behaviour and emotional expressions in farmed silver foxes (Vulpes vulpes)—basis for a novel tool to study animal welfare. Appl Anim Behav Sci 101:362–368. doi:10.1016/j.applanim.2006.02.004

    Article  Google Scholar 

  • Monticelli PF, Tokumaru RS, Ades C (2004) Isolation induced changes in guinea pig Cavia porcellus pup distress whistles. An Brazil Acad Sci 76:368–372

    Google Scholar 

  • Morton ES (1977) On the occurrence and significance of motivation–structural rules in some bird and mammal sounds. Am Nat 111(981):855–869. doi:10.1086/283219

    Article  Google Scholar 

  • Moura DJ, Silva WT, Naas IA, Tolón YA, Lima KAO, Vale MM (2008) Real time computer stress monitoring of piglets using vocalization analysis. Comput Electron Agr 64:11–18. doi:10.1016/j.compag.2008.05.008

    Article  Google Scholar 

  • Nakagawa T (1987) Conversion of vortex energy into acoustic energy. Naturwissenschaften 74:338–339. doi:10.1007/BF00367929

    Article  Google Scholar 

  • Newman JD, Goedeking P (1992) Noncategorical vocal communication in primates: the example of common marmoset phee calls. In: Papousek H, Jürgens U, Papousek M (eds) Nonverbal vocal communication. Cambridge University Press, Cambridge, pp 87–101

    Google Scholar 

  • Nimon AJ, Broom DM (2001) The welfare of farmed foxes Vulpes vulpes and Alopex lagopus in relation to housing and management: a review. Anim Welf 10:223–248

    Google Scholar 

  • Oskina IN, Herbeck YE, Shikhevich SG, Plyusnina IZ, Gulevich RG (2008) Alterations in the hypothalamus–pituitary–adrenal and immune systems during selection of animals for tame behavior. VOGiS Herald 12:39–49

    Google Scholar 

  • Pedersen V (1991) Early experience with the farm environment and later effects on behaviour in silver (Vulpes vulpes) and blue (Alopex lagopus) foxes. Behav Processes 25:163–169. doi:10.1016/0376-6357(91)90018-U

    Article  Google Scholar 

  • Pedersen V (1993) Effects of different post-weaning handling procedures on the later behaviour of silver foxes. Appl Anim Behav Sci 37:239–250. doi:10.1016/0168-1591(93)90114-5

    Article  Google Scholar 

  • Pedersen V (1994) Long-term effects of different handling procedures on behavioural, physiological, and production-related parameters in silver foxes. Appl Anim Behav Sci 40:285–296. doi:10.1016/0168-1591(94)90069-8

    Article  Google Scholar 

  • Pedersen V, Jeppesen LL (1990) Effect of early handling on later behaviour and stress responses in the silver fox (Vulpes vulpes). Appl Anim Behav Sci 26:383–393. doi:10.1016/0168-1591(90)90037-E

    Article  Google Scholar 

  • Pongrácz P, Miklosi A, Molnar C, Csanyi V (2005) Human listeners are able to classify dog (Canis familiaris) barks recorded in different situations. J Comp Psychol 119:136–144. doi:10.1037/0735-7036.119.2.136

    Article  PubMed  Google Scholar 

  • Pongrácz P, Molnar C, Miklosi A (2006) Acoustic parameters of dog barks carry emotional information for humans. Appl Anim Behav Sci 100:228–240. doi:10.1016/j.applanim.2005.12.004

    Article  Google Scholar 

  • Rekilä T, Harri M, Ahola L (1997) Validation of the feeding test as an index of fear in farmed blue (Alopex lagopus) and silver foxes (Vulpes vulpes). Physiol Behav 62:805–810. doi:10.1016/S0031-9384(97)00241-2

    Article  PubMed  Google Scholar 

  • Rendall D (2003) Acoustic correlates of caller identity and affect intensity in the vowel-like grunt vocalizations of baboons. J Acoust Soc Am 113:3390–3402. doi:10.1121/1.1568942

    Article  PubMed  Google Scholar 

  • Riede T, Herzel H, Hammerschmidt K, Brunnberg L, Tembrock G (2001) The harmonic-to-noise ratio applied to dog barks. J Acoust Soc Am 110:2191–2197. doi:10.1121/1.1398052

    Article  CAS  PubMed  Google Scholar 

  • Schehka S, Esser K-H, Zimmermann E (2007) Acoustical expression of arousal in conflict situations in tree shrews (Tupaia belangeri). J Comp Physiol A 93:845–852. doi:10.1007/s00359-007-0236-8

    Article  Google Scholar 

  • Schrader L, Todt D (1993) Contact call parameters covary with social context in common marmosets, Callithrix j. jacchus. Anim Behav 46:1026–1028. doi:10.1006/anbe.1993.1288

    Article  Google Scholar 

  • Schrader L, Todt D (1998) Vocal quality is correlated with levels of stress hormones in domestic pigs. Ethology 104:859–876

    Article  Google Scholar 

  • Schön PC, Puppe B, Manteuffel G (2001) Linear prediction coding analysis and self-organizing feature map as tools to classify stress calls of domestic pigs (Sus scrofa). J Acoust Soc Am 110:1425–1431. doi:10.1121/1.1388003

    Article  PubMed  Google Scholar 

  • Schön PC, Puppe B, Manteuffel G (2004) Automated recording of stress vocalisations as a tool to document impaired welfare in pigs. Anim Welf 13:105–110

    Google Scholar 

  • Sherwin CM, Christiansen SB, Duncan IJ, Erhard H, Lay D, Mench J, O’Connor C, Petherick C (2003) Guidelines for the ethical use of animals in applied ethology studies. Appl Anim Behav Sci 81:291–305. doi:10.1016/S0168-1591(02)00288-5

    Article  Google Scholar 

  • Specht R (2006) Software tools for automatically detecting, measuring and classifying animal sounds. Advances in Bioacoustics 2. Dissertationes Classis IV: Historia Naturalis, Academy of Sciences and Arts, Ljubljana, vol 37, pp 177–184

  • Taylor AA, Weary DM (2000) Vocal responses of piglets to castration: identifying procedural sources of pain. Appl Anim Behav Sci 70:17–26. doi:10.1016/S0168-1591(00)00143-X

    Article  PubMed  Google Scholar 

  • Taylor AA, Weary DM, Lessard M, Braithwaite L (2001) Behavioural responses of piglets to castration: the effect of piglet age. Appl Anim Behav Sci 73:35–43. doi:10.1016/S0168-1591(01)00123-X

    Article  PubMed  Google Scholar 

  • The Welfare of Animals Kept for Fur Production (2001) Report of the Scientific Committee on Animal Health and Animal Welfare. EC Health and Consumer Protection Directorate-General. http://ec.europa.eu/food/animal/welfare/international/out67_en.pdf

  • Titze IR (1994) Principles of voice production. Prentice Hall, Englewood Cliffs

    Google Scholar 

  • Trut LN (1999) Early canid domestication: farm-fox experiment. Amer Sci 87:160–169. doi:10.1511/1999.2.160

    Google Scholar 

  • Volodin IA, Goltsman ME, Borisova NG (1994) Situational changes in vocalization of great gerbils (Rhombomys opimus Licht) during defensive behavior. Dokl Biol Sci 334:65–68

    Google Scholar 

  • Waiblinger S, Boivin X, Pedersen V, Tosi M-V, Janczak AM, Visser EK, Jones RB (2006) Assessing the human–animal relationship in farmed species: a critical review. Appl Anim Behav Sci 101:185–242. doi:10.1016/j.applanim.2006.02.001

    Article  Google Scholar 

  • Watts JM, Stookey JM (1999) Effects of restraint and branding on rates and acoustic parameters of vocalization in beef cattle. Appl Anim Behav Sci 62:125–135. doi:10.1016/S0168-1591(98)00222-6

    Article  Google Scholar 

  • Watts JM, Stookey JM (2000) Vocal behaviour in cattle: the animal’s commentary on its biological processes and welfare. Appl Anim Behav Sci 67:15–33. doi:10.1016/S0168-1591(99)00108-2

    Article  PubMed  Google Scholar 

  • Weary DM, Frazer D (1995a) Signaling need: costly signals and animal welfare assessment. Appl Anim Behav Sci 44:159–169. doi:10.1016/0168-1591(95)00611-U

    Article  Google Scholar 

  • Weary DM, Frazer D (1995b) Calling by domestic piglets: reliable signals of need? Anim Behav 50:1047–1055. doi:10.1016/0003-3472(95)80105-7

    Article  Google Scholar 

  • Weary DM, Braithwaite LA, Fraser D (1998) Vocal response to pain in piglets. Appl Anim Behav Sci 56:161–172. doi:10.1016/S0168-1591(97)00092-0

    Article  Google Scholar 

  • Zahavi A (1977) Reliability in communication systems and the evolution of altruism. In: Stonehouse B, Perrins C (eds) Evolutionary ecology. MacMillan, London, pp 253–260

    Google Scholar 

  • Zahavi A (1982) The pattern of vocal signals and the information they convey. Behaviour 80:1–8. doi:10.1163/156853982X00409

    Article  Google Scholar 

Download references

Acknowledgments

We thank the staff of the experimental fur farm of the Institute of Cytology and Genetics RAS, Novosibirsk, Russia for help and support, Dr. Vladimir Lebedev, Nina Vasilieva, and Dr. Andrey Babitsky for consulting in statistics, and Dr. Irina Oskina for consulting in hormonal responses to handling in foxes. Also, we thank two anonymous referees for their constructive and inspiring comments. During our work, we adhered to the Ethical Treatment of Animals in Applied Animal Behaviour Research (Sherwin et al. 2003) and to the laws of Russian Federation, the country where the research was conducted. PHS Approved Animal Welfare Assurance Numbers for Lomonosov Moscow State University is A5751-01 and for Institute of Cytology and Genetics is A5761-01. This study was supported by the Russian Foundation for Basic Research grant 09-04-00416 (for S.S.G, I.A.V and E.V.V), by National Institutes of Health grants R03 TW008098-01 and R01 MH077811, and the Programs of Basic Research of the RAS Presidium “Biodiversity and gene pool dynamics” and “Molecular and Cell Biology” (for A.V.K and L.N.T).

Author information

Authors and Affiliations

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

    Svetlana S. Gogoleva & Ilya A. Volodin

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

    Elena V. Volodina & Ilya A. Volodin

  3. Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, Pr. Lavrentjeva, 10, Novosibirsk, 630090, Russia

    Anastasia V. Kharlamova & Lyudmila N. Trut

Authors
  1. Svetlana S. Gogoleva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elena V. Volodina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ilya A. Volodin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anastasia V. Kharlamova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lyudmila N. Trut
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ilya A. Volodin.

Additional information

Communicated by: Emanuel Gonçalves

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gogoleva, S.S., Volodina, E.V., Volodin, I.A. et al. The gradual vocal responses to human-provoked discomfort in farmed silver foxes. acta ethol 13, 75–85 (2010). https://doi.org/10.1007/s10211-010-0076-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10211-010-0076-3

Keywords

Search

Navigation