Skip to main content
SpringerLink
Log in

Threat-level-dependent manipulation of signaled body size: dog growls’ indexical cues depend on the different levels of potential danger

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Body size is an important feature that affects fighting ability; however, size-related parameters of agonistic vocalizations are difficult to manipulate because of anatomical constraints within the vocal production system. Rare examples of acoustic size modulation are due to specific features that enable the sender to steadily communicate exaggerated body size. However, one could argue that it would be more adaptive if senders could adjust their signaling behavior to the fighting potential of their actual opponent. So far there has been no experimental evidence for this possibility. We tested this hypothesis by exposing family dogs (Canis familiaris) to humans with potentially different fighting ability. In a within-subject experiment, 64 dogs of various breeds consecutively faced two threateningly approaching humans, either two men or two women of different stature, or a man and a woman of similar or different stature. We found that the dogs’ vocal responses were affected by the gender of the threatening stranger and the dog owner’s gender. Dogs with a female owner, or those dogs which came from a household where both genders were present, reacted with growls of lower values of the Pitch–Formant component (including deeper fundamental frequency and lower formant dispersion) to threatening men. Our results are the first to show that non-human animals react with dynamic alteration of acoustic parameters related to their individual indexical features (body size), depending on the level of threat in an agonistic encounter.

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

Similar content being viewed by others

References

  • Altenmüller E, Schmidt S, Zimmermann E (2013) A cross-taxa concept of emotion in acoustic communication: an ethological perspective. In: Altenmüller E, Schmidt S, Zimmermann E (eds) Evolution of emotional communication: from sounds in nonhuman mammals to speech and music in man, Oxford University Press, Oxford, UK

    Chapter  Google Scholar 

  • Bálint A, Faragó T, Dóka A et al (2013) “Beware, I am big and non-dangerous!”—playfully growling dogs are perceived larger than their actual size by their canine audience. Appl Anim Behav Sci 148:128–137. doi:10.1016/j.applanim.2013.07.013

    Article  Google Scholar 

  • Bee MA, Perrill SA, Owen PC (2000) Male green frogs lower the pitch of acoustic signals in defense of territories: a possible dishonest signal of size? Behav Ecol 11:169–177. doi:10.1093/beheco/11.2.169

    Article  Google Scholar 

  • Besser R (2007) Personal views: dog attacks: it's time for doctors to bite back. BMJ: Br Med J 334(7590):425

  • Blackshaw JK (1991) An overview of types of aggressive behaviour in dogs and methods of treatment. Appl Anim Behav Sci 30:351–361. doi:10.1016/0168-1591(91)90140-S

    Article  Google Scholar 

  • Boersma P, Weenink D (2001) Praat, a system for doing phonetics by computer. Glot Int 5:341–345

    Google Scholar 

  • Briefer EF (2012) Vocal expression of emotions in mammals: mechanisms of production and evidence. J Zool 288:1–20. doi:10.1111/j.1469-7998.2012.00920.x

    Article  Google Scholar 

  • Briefer EF, McElligott AG (2011) Mutual mother-offspring vocal recognition in an ungulate hider species (Capra hircus). Anim Cogn. doi:10.1007/s10071-011-0396-3

    PubMed  Google Scholar 

  • Carlson CR, Collins FL, Stewart JF et al (1989) The assessment of emotional reactivity: a scale development and validation study. J Psychopathol Behav Assess 11:313–325. doi:10.1007/BF00961530

    Article  Google Scholar 

  • Cattel RB (1966) The scientific analysis of personality. Penguin Books, Harrnondsworth

    Google Scholar 

  • Charlton BD, Ellis WAH, McKinnon AJ et al (2011) Cues to body size in the formant spacing of male koala (Phascolarctos cinereus) bellows: honesty in an exaggerated trait. J Exp Biol 214:3414–3422. doi:10.1242/jeb.061358

    Article  PubMed  Google Scholar 

  • DeVellis RF (1991) Scale development. Theory and aplications. SAGE Publications, Newbury Park

    Google Scholar 

  • Fant G (1960) Acoustic theory of speech production. Mouton & Co., The Hague

    Google Scholar 

  • Faragó T, Pongrácz P, Miklósi Á et al (2010a) Dogs’ expectation about signalers’ body size by virtue of their growls. PLoS ONE 5:e15175. doi:10.1371/journal.pone.0015175

    Article  PubMed  PubMed Central  Google Scholar 

  • Faragó T, Pongrácz P, Range F et al (2010b) “The bone is mine”: affective and referential aspects of dog growls. Anim Behav 79:917–925. doi:10.1016/j.anbehav.2010.01.005

    Article  Google Scholar 

  • Faragó T, Andics A, Devecseri V et al (2014) Humans rely on the same rules to assess emotional valence and intensity in conspecific and dog vocalizations. Biol Lett 10:20130926. doi:10.1098/rsbl.2013.0926

    Article  PubMed  PubMed Central  Google Scholar 

  • Feddersen-Petersen DU (2000) Vocalization of European wolves (Canis lupus lupus L.) and various dog breeds (Canis lupus f. familiaris). Arch Tierzucht Dummerstorf 43:387–397

    Google Scholar 

  • Fitch WT (1997) Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. J Acoust Soc Am 102:1213–1222. doi:10.1121/1.421048

    Article  CAS  PubMed  Google Scholar 

  • Fitch WT (1999) Acoustic exaggeration of size in birds via tracheal elongation: comparative and theoretical analyses. J Zool 248:31–48. doi:10.1111/j.1469-7998.1999.tb01020.x

    Article  Google Scholar 

  • Fitch WT, Fritz JB (2006) Rhesus macaques spontaneously perceive formants in conspecific vocalizations. J Acoust Soc Am 120:2132. doi:10.1121/1.2258499

    Article  PubMed  Google Scholar 

  • Fitch WT, Hauser MD (2003) Unpacking “honesty”: vertebrate vocal production and the evolution of acoustic signals. In: Simmons AM, Popper AN, Fay RR (eds) Acoustic communication. Springer-Verlag, New York, pp 65–137

    Chapter  Google Scholar 

  • Fitch WT, Reby D (2001) The descended larynx is not uniquely human. Proc R Soc B Biol Sci 268:1669–1675. doi:10.1098/rspb.2001.1704

    Article  CAS  Google Scholar 

  • Fredrickson BL, Levenson RW (1998) Positive emotions speed recovery from the cardiovascular sequelae of negative emotions. Cogn Emot 12:191–220. doi:10.1080/026999398379718

    Article  PubMed  PubMed Central  Google Scholar 

  • Frey R, Gebler A, Olson KA et al (2008) Mobile larynx in Mongolian gazelle: retraction of the larynx during rutting barks in male Mongolian gazelle (Procapra gutturosa Pallas, 1777). J Morphol 269:1223–1237. doi:10.1002/jmor.10656

    Article  PubMed  Google Scholar 

  • Gácsi M, Maros K, Sernkvist S et al (2013) Human analogue safe haven effect of the owner: behavioural and heart rate response to stressful social stimuli in dogs. PLoS ONE 8:e58475. doi:10.1371/journal.pone.0058475

    Article  PubMed  PubMed Central  Google Scholar 

  • Gogoleva SS, Volodin IA, Volodina EV et al (2010a) Sign and strength of emotional arousal: vocal correlates of positive and negative attitudes to humans in silver foxes (Vulpes vulpes). Behaviour 147:1713–1736. doi:10.1163/000579510X528242

    Article  Google Scholar 

  • Gogoleva SS, Volodin IA, Volodina EV et al (2010b) Vocalization toward conspecifics in silver foxes (Vulpes vulpes) selected for tame or aggressive behavior toward humans. Behav Process 84:547–554. doi:10.1016/j.beproc.2010.01.021

    Article  CAS  Google Scholar 

  • Guy NC, Luescher UA, Dohoo SE et al (2001) Demographic and aggressive characteristics of dogs in a general veterinary caseload. Appl Anim Behav Sci 74:15–28. doi:10.1016/S0168-1591(01)00153-8

    Article  Google Scholar 

  • Hennessy MB, Williams MT, Miller DD et al (1998) Influence of male and female petters on plasma cortisol and behaviour: can human interaction reduce the stress of dogs in a public animal shelter? Appl Anim Behav Sci 61:63–77. doi:10.1016/S0168-1591(98)00179-8

    Article  Google Scholar 

  • Jennings DJ, Gammell MP, Carlin CM, Hayden TJ (2004) Effect of body weight, antler length, resource value and experience on fight duration and intensity in fallow deer. Anim Behav 68(1): 213–221

    Article  Google Scholar 

  • Klausz B, Kis A, Persa E, Miklósi A, Gácsi M (2014) A quick assessment tool for human-directed aggression in pet dogs. Aggress Behav 40(2):178–188

  • Lappin AK, Husak JF (2005) Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris). Am Nat 166(3):426–436

    Article  PubMed  Google Scholar 

  • Landsberg G, Hunthausen W, Ackerman L (2013) Behavior problems of the dog and cat, 3rd edn. Saunders Elsevier, Edinburgh

    Google Scholar 

  • Larrañaga A, Bielza C, Pongrácz P et al (2015) Comparing supervised learning methods for classifying sex, age, context and individual Mudi dogs from barking. Anim Cogn 18:405–421. doi:10.1007/s10071-014-0811-7

    Article  PubMed  Google Scholar 

  • Lore RK, Eisenberg FB (1986) Avoidance reactions of domestic dogs to unfamiliar male and female humans in a kennel setting. Appl Anim Behav Sci 15:261–266. doi:10.1016/0168-1591(86)90096-1

    Article  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 Biol Sci 268:2315–2324. doi:10.1098/rspb.2001.1773

    Article  CAS  Google Scholar 

  • McElligott AG, Birrer M, Vannoni E (2006) Retraction of the mobile descended larynx during groaning enables fallow bucks (Dama dama) to lower their formant frequencies. J Zool 270:340–345. doi:10.1111/j.1469-7998.2006.00144.x

    Article  Google Scholar 

  • Meints K, De Keuster T (2009) Brief report: don’t kiss a sleeping dog: the first assessment of “the blue dog” bite prevention program. J Pediatr Psychol 34(10):1084–1090

    Article  Google Scholar 

  • Miklósi Á, Topál J (2013) What does it take to become “best friends”? Evolutionary changes in canine social competence. Trends Cogn Sci 17:287–294. doi:10.1016/j.tics.2013.04.005

    Article  PubMed  Google Scholar 

  • Molnár C, Kaplan F, Roy P et al (2008) Classification of dog barks: a machine learning approach. Anim Cogn 11:389–400. doi:10.1007/s10071-007-0129-9

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Morton ES (1994) Sound symbolism and its role in non-human vertebrate communication. In: Hinton L, Nichols J, Ohala JJ (eds) Sound symbolism. Cambridge University Press, Cambridge, pp 348–365

    Google Scholar 

  • Nagasawa M, Murai K, Mogi K, Kikusui T (2011) Dogs can discriminate human smiling faces from blank expressions. Anim Cogn. doi:10.1007/s10071-011-0386-5

    PubMed  Google Scholar 

  • Nelson RJ, Trainor BC (2007) Neural mechanisms of aggression. Nat Rev Neurosci 8:536–546. doi:10.1038/nrn2174

    Article  CAS  PubMed  Google Scholar 

  • O’Connor BP (2000) SPSS and SAS programs for determining the number of components using parallel analysis and Velicer’s MAP test. Behav Res Methods Instrum Comput 32:396–402. doi:10.3758/BF03200807

    Article  PubMed  Google Scholar 

  • O’Sullivan EN, Jones BR, O’Sullivan K, Hanlon AJ (2008) Characteristics of 234 dog bite incidents in Ireland during 2004 and 2005. Vet Rec 163:37–42. doi:10.1136/vr.163.2.37

    Article  PubMed  Google Scholar 

  • Ohala JJ (1984) An ethological perspective on common cross-language utilization of F0 of voice. Phonetica 41:1–16

    Article  CAS  PubMed  Google Scholar 

  • Owings DH, Morton ES (1998) Animal vocal communication: A new approach. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Pageat P (2004) Evaluation of the aggressive dog: what is a really dangerous dog? In: Documento procedente de 29 th World Small Animal Veterinary Congress. WSAVA

  • Pongrácz P, Molnár C, Miklósi Á, Csányi 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, Molnár C, Miklósi Á (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 

  • Ratcliffe VF, McComb K, Reby D (2014) Cross-modal discrimination of human gender by domestic dogs. Anim Behav 91:126–134. doi:10.1016/j.anbehav.2014.03.009

    Article  Google Scholar 

  • Reby D, McComb K (2003) Vocal communication and reproduction in deer. In: Brockmann HJ, Roper TJ, Naguib M et al (eds) Advances in the Study of Behavior, vol 33. Academic Press, Burlington MA, pp 231–264

    Google Scholar 

  • Reby D, McComb K, Cargnelutti B et al (2005) Red deer stags use formants as assessment cues during intrasexual agonistic interactions. Proc Biol Sci 272:941–947. doi:10.1098/rspb.2004.2954

    Article  PubMed  PubMed Central  Google Scholar 

  • Reisner IR (2003) Differential diagnosis and management of human-directed aggression in dogs. Vet Clin North Am Small Anim Pract 33:303–320. doi:10.1016/S0195-5616(02)00132-8

    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. doi:10.1121/1.1568942

    Article  PubMed  Google Scholar 

  • Rendall D, Vokey JR, Nemeth C (2007) Lifting the curtain on the Wizard of Oz: biased voice-based impressions of speaker size. J Exp Psychol Hum Percept Perform 33:1208–1219. doi:10.1037/0096-1523.33.5.1208

    Article  PubMed  Google Scholar 

  • Riede T, Fitch WT (1999) Vocal tract length and acoustics of vocalization in the domestic dog (Canis familiaris). J Exp Biol 202:2859–2867

    CAS  PubMed  Google Scholar 

  • Robbins RL, McCreery EK (2003) African wild dog pup vocalizations with special reference to Morton’s model. Behaviour 140:333–351

    Article  Google Scholar 

  • Ruffman T, Yong MH (2015) Domestic dogs match human male voices to faces, but not for females. Behaviour 152:1585–1600. doi:10.1163/1568539X-00003294

    Article  Google Scholar 

  • Sanvito S, Galimberti F, Miller EH (2007) Vocal signalling of male southern elephant seals is honest but imprecise. Anim Behav 73:287–299. doi:10.1016/j.anbehav.2006.08.005

    Article  Google Scholar 

  • Schassburger RM (1993) Vocal communication in the timber wolf, Canis lupus, Linnaeus: structure, motivation, and ontogeny. In: Dehnhard M, Hofer H (eds) Advances in Ethology. Paul Parey Publishers, Berlin

    Google Scholar 

  • Scheumann M, Roser AE, Konerding W, Bleich E, Hedrich HJ, Zimmermann E (2012) Vocal correlates of sender-identity and arousal in the isolation calls of domestic kitten (Felis silvestris catus). Front zool 9(1):1

    Article  Google Scholar 

  • Sell A, Cosmides L, Tooby J, Sznycer D, Rueden CV, Gurven M (2009) Human adaptations for the visual assessment of strength and fighting ability from the body and face. Proc R Soc B Biol Sci 276:575–584

    Article  Google Scholar 

  • Spillmann B, Dunkel LP, Van Noordwijk MA, Amda RN, Lameira AR, Wich SA, Van Schaik CP (2010) Acoustic properties of long calls given by flanged male orang-utans (pongo pygmaeus wurmbii) reflect both individual identity and context. Ethol 116(5):385–395

    Article  Google Scholar 

  • Taylor AM, Reby D (2010) The contribution of source-filter theory to mammal vocal communication research. J Zool 280:221–236. doi:10.1111/j.1469-7998.2009.00661.x

    Article  Google Scholar 

  • Taylor AM, Reby D, McComb K (2008) Human listeners attend to size information in domestic dog growls. J Acoust Soc Am 123:2903–2909. doi:10.1121/1.2896962

    Article  PubMed  Google Scholar 

  • Taylor AM, Reby D, McComb K (2010) Why do large dogs sound more aggressive to human listeners: acoustic bases of motivational misattributions. Ethology 116:1155–1162. doi:10.1111/j.1439-0310.2010.01829.x

    Article  Google Scholar 

  • Theis KR, Greene KM, Benson-Amram SR, Holekamp KE (2007) Sources of variation in the long-distance vocalizations of spotted hyenas. Behav 144(5):557–584

    Article  Google Scholar 

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

    Google Scholar 

  • Vas J, Topál J, Gácsi M et al (2005) A friend or an enemy? Dogs’ reaction to an unfamiliar person showing behavioural cues of threat and friendliness at different times. Appl Anim Behav Sci 94:99–115. doi:10.1016/j.applanim.2005.02.001

    Article  Google Scholar 

  • Volodin IA, Volodina EV, Efremova KO (2009) Antelope, calling through the nose: structure of sounds and effect of sexual selection on the vocal behavior of the saiga (Saiga tatarica). Zool Žurnal 88:113–124

    Google Scholar 

  • Wells DL, Hepper PG (1999) Male and female dogs respond differently to men and women. Appl Anim Behav Sci 61:341–349. doi:10.1016/S0168-1591(98)00202-0

    Article  Google Scholar 

  • Wyman MT, Mooring MS, McCowan B et al (2012) Acoustic cues to size and quality in the vocalizations of male North American bison, Bison bison. Anim Behav 84:1381–1391. doi:10.1016/j.anbehav.2012.08.037

    Article  Google Scholar 

  • Yin S, McCowan B (2004) Barking in domestic dogs: context specificity and individual identification. Anim Behav 68:343–355. doi:10.1016/j.anbehav.2003.07.016

    Article  Google Scholar 

Download references

Acknowledgments

This study was funded by the Hungarian Ministry of Education OTKA K82020 and by the Hungarian Academy of Sciences, MTA (01 031). During the time of manuscript preparation, TF was also supported by the Stanton Foundation, Next Generation Canine Research Grant. The authors are also thankful to Celeste R. Pongrácz for the English proofreading of the manuscript.

Author information

Author notes

    Authors and Affiliations

    1. Department of Ethology, Biological Institute, Eötvös Loránd University, Pázmány Péter s. 1/c, Budapest, 1117, Hungary

      Anna Bálint, Ádám Miklósi & Péter Pongrácz

    2. MTA-ELTE Comparative Ethology Research Group, Budapest, Hungary

      Tamás Faragó & Ádám Miklósi

    Authors
    1. Anna Bálint
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Tamás Faragó
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Ádám Miklósi
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Péter Pongrácz
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Péter Pongrácz.

    Ethics declarations

    Ethical approval

    Research was done in accordance with the Hungarian regulations on animal experimentation and the Guidelines for the use of animals in research described by the Association for the Study Animal Behaviour (ASAB). Ethical approval was obtained from the National Animal Experimentation Ethics Committee, and the Animal Welfare Committee of the Eötvös Loránd University reviewed and accepted the protocol of the experiment (Ref. No.: ELTE-AWC-014/2015).

    Additional information

    Anna Bálint and Tamás Faragó have contributed equally to this work.

    Electronic supplementary material

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Bálint, A., Faragó, T., Miklósi, Á. et al. Threat-level-dependent manipulation of signaled body size: dog growls’ indexical cues depend on the different levels of potential danger. Anim Cogn 19, 1115–1131 (2016). https://doi.org/10.1007/s10071-016-1019-9

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10071-016-1019-9

    Keywords

    Search

    Navigation