‘Goats that stare at men’: dwarf goats alter their behaviour in response to human head orientation, but do not spontaneously use head direction as a cue in a food-related context

Abstract

Recently, comparative research on the mechanisms and species-specific adaptive values of attributing attentive states and using communicative cues has gained increased interest, particularly in non-human primates, birds, and dogs. Here, we investigate these phenomena in a farm animal species, the dwarf goat (Capra aegagrus hircus). In the first experiment, we investigated the effects of different human head and body orientations, as well as human experimenter presence/absence, on the behaviour of goats in a food-anticipating paradigm. Over a 30-s interval, the experimenter engaged in one of four different postures or behaviours (head and body towards the subject—'Control', head to the side, head and body away from the subject, or leaving the room) before delivering a reward. We found that the level of subjects’ active anticipatory behaviour was highest in the control condition and decreased with a decreasing level of attention paid to the subject by the experimenter. Additionally, goats ‘stared’ (i.e. stood alert) at the experimental set-up for significantly more time when the experimenter was present but paid less attention to the subject (‘Head’ and ‘Back’ condition) than in the ‘Control’ and ‘Out’ conditions. In a second experiment, the experimenter provided different human-given cues that indicated the location of a hidden food reward in a two-way object choice task. Goats were able to use both ‘Touch’ and ‘Point’ cues to infer the correct location of the reward but did not perform above the level expected by chance in the ‘Head only’ condition. We conclude that goats are able to differentiate among different body postures of a human, including head orientation; however, despite their success at using multiple physical human cues, they fail to spontaneously use human head direction as a cue in a food-related context.

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

Fig. 1
Fig. 2
Fig. 3

References

  1. Baciadonna L, McElligott AG, Briefer EF (2013) Goats favour personal over social information in an experimental foraging task. PeerJ 1:e172. doi:10.7717/peerj.172

    PubMed Central  PubMed  Article  Google Scholar 

  2. Bania AE, Stromberg EE (2013) The effect of body orientation on judgments of human visual attention in western lowland gorillas (Gorilla gorilla gorilla). J Comp Psychol 127:82–90. doi:10.1037/a0027261

    PubMed  Article  Google Scholar 

  3. Bolles RC (1968) Anticipatory general activity in thirsty rats. J Comp Physiol Psychol 65:511–513

    CAS  PubMed  Article  Google Scholar 

  4. Botting JL, Wiper ML, Anderson JR (2011) Brown (Eulemur fulvus) and ring-tailed lemurs (Lemur catta) use human head orientation as a cue to gaze direction in a food choice task. Folia Primatol 82:165–176. doi:10.1159/000333142

    PubMed  Article  Google Scholar 

  5. Bourjade M, Meguerditchian A, Maille A et al (2014) Olive baboons, Papio anubis, adjust their visual and auditory intentional gestures to the visual attention of others. Anim Behav 87:121–128. doi:10.1016/j.anbehav.2013.10.019

    Article  Google Scholar 

  6. Bräuer J, Call J, Tomasello M (2005) All great ape species follow gaze to distant locations and around barriers. J Comp Psychol 119:145–154. doi:10.1037/0735-7036.119.2.145

    PubMed  Article  Google Scholar 

  7. Briefer EF, Haque S, Baciadonna L, McElligott AG (2014) Goats excel at learning and remembering a highly novel cognitive task. Front Zool 11:20. doi:10.1186/1742-9994-11-20

    PubMed Central  PubMed  Article  Google Scholar 

  8. Bugnyar T, Stöwe M, Heinrich B (2004) Ravens, Corvus corax, follow gaze direction of humans around obstacles. Proc Biol Sci 271:1331–1336. doi:10.1098/rspb.2004.2738

    PubMed Central  PubMed  Article  Google Scholar 

  9. Bulloch MJ, Boysen ST, Furlong EE (2008) Visual attention and its relation to knowledge states in chimpanzees, Pan troglodytes. Anim Behav 76:1147–1155. doi:10.1016/j.anbehav.2008.01.033

    Article  Google Scholar 

  10. Butz MV, Sigaud O, Gérard P (2003) Anticipatory behavior: exploiting knowledge about the future to improve current behavior. Anticip Behav Adapt Learn Syst Found Theor Syst Springer, pp 1–10

  11. Craig W (1918) Appetites and aversions as constituents of instincts. Biol Bull 34:91–107

    Article  Google Scholar 

  12. Davidson GL, Butler S, Fernández-Juricic E et al (2014) Gaze sensitivity: function and mechanisms from sensory and cognitive perspectives. Anim Behav 87:3–15. doi:10.1016/j.anbehav.2013.10.024

    Article  Google Scholar 

  13. Flombaum JI, Santos LR (2005) Rhesus monkeys attribute perceptions to others. Curr Biol 15:447–452. doi:10.1016/j.cub.2004.12.076

    CAS  PubMed  Article  Google Scholar 

  14. Gácsi M, Miklosi A, Varga O et al (2004) Are readers of our face readers of our minds? Dogs (Canis familiaris) show situation-dependent recognition of human’s attention. Anim Cogn 7:144–153. doi:10.1007/s10071-003-0205-8

    PubMed  Article  Google Scholar 

  15. Gaunet F, Deputte BL (2011) Functionally referential and intentional communication in the domestic dog: effects of spatial and social contexts. Anim Cogn 14:849–860. doi:10.1007/s10071-011-0418-1

    PubMed  Article  Google Scholar 

  16. Giret N, Miklósi Á, Kreutzer M, Bovet D (2009) Use of experimenter-given cues by African gray parrots (Psittacus erithacus). Anim Cogn 12:1–10. doi:10.1007/s10071-008-0163-2

    PubMed  Article  Google Scholar 

  17. Gómez J-C (2005a) Species comparative studies and cognitive development. Trends Cogn Sci 9:118–125. doi:10.1016/j.tics.2005.01.004

    PubMed  Article  Google Scholar 

  18. Gómez J-C (2005b) Requesting gestures in captive monkeys and apes: conditioned responses or referential behaviours? Gesture 5:91–105. doi:10.1075/gest.5.1.08gom

    Article  Google Scholar 

  19. Hansen SW, Jeppesen LL (2006) Temperament, stereotypies and anticipatory behaviour as measures of welfare in mink. Appl Anim Behav Sci 99:172–182. doi:10.1016/j.applanim.2005.10.005

    Article  Google Scholar 

  20. Hare B, Tomasello M (2005) The emotional reactivity hypothesis and cognitive evolution. Trends Cogn Sci 9:464–465. doi:10.1016/j.tics.2005.08.010

    Article  Google Scholar 

  21. Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636. doi:10.1126/science.1072702

    CAS  PubMed  Article  Google Scholar 

  22. Hattori Y, Kuroshima H, Fujita K (2007) I know you are not looking at me: capuchin monkeys´ (Cebus apella) sensitivity to human attentional states. Anim Cogn 10:141–148. doi:10.1007/s10071-006-0049-0

    PubMed  Article  Google Scholar 

  23. Hooks MS, Jones GH, Juncos JL et al (1994) Individual differences in schedule-induced and conditioned behaviours. Behav Brain Res 60:199–209

    CAS  PubMed  Article  Google Scholar 

  24. Imfeld-Mueller S, Hillmann E (2012) Anticipation of a food ball increases short-term activity levels in growing pigs. Appl Anim Behav Sci 137:23–29. doi:10.1016/j.applanim.2012.01.012

    Article  Google Scholar 

  25. Kaminski J, Call J, Tomasello M (2004) Body orientation and face orientation: two factors controlling apes’ behavior from humans. Anim Cogn 7:216–223. doi:10.1007/s10071-004-0214-2

    PubMed  Article  Google Scholar 

  26. Kaminski J, Riedel J, Call J, Tomasello M (2005) Domestic goats, Capra hircus, follow gaze direction and use social cues in an object choice task. Anim Behav 69:11–18. doi:10.1016/j.anbehav.2004.05.008

    Article  Google Scholar 

  27. Loretto M-C, Schloegl C, Bugnyar T (2010) Northern bald ibises follow others’ gaze into distant space but not behind barriers. Biol Lett 6:14–17. doi:10.1098/rsbl.2009.0510

    PubMed Central  PubMed  Article  Google Scholar 

  28. Maille A, Engelhart L, Bourjade M, Blois-Heulin C (2012) To beg, or not to beg? That is the question: mangabeys modify their production of requesting gestures in response to human’s attentional states. PLoS ONE 7:e41197. doi:10.1371/journal.pone.0041197

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  29. Maros K, Gácsi M, Miklósi Á (2008) Comprehension of human pointing gestures in horses (Equus caballus). Anim Cogn 11:457–466. doi:10.1007/s10071-008-0136-5

    PubMed  Article  Google Scholar 

  30. McKinley J, Sambrook TD (2000) Use of human-given cues by domestic dogs (Canis familiaris) and horses (Equus caballus). Anim Cogn 3:13–22. doi:10.1007/s100710050046

    Article  Google Scholar 

  31. Miklósi A, Soproni K (2006) A comparative analysis of animals’ understanding of the human pointing gesture. Anim Cogn 9:81–93. doi:10.1007/s10071-005-0008-1

    PubMed  Article  Google Scholar 

  32. Moe RO, Stubsjøen SM, Bohlin J et al (2012) Peripheral temperature drop in response to anticipation and consumption of a signaled palatable reward in laying hens (Gallus domesticus). Physiol Behav 106:527–533. doi:10.1016/j.physbeh.2012.03.032

    CAS  PubMed  Article  Google Scholar 

  33. Mulcahy NJ, Hedge V (2012) Are great apes tested with an abject object-choice task? Anim Behav 83:313–321. doi:10.1016/j.anbehav.2011.11.019

    Article  Google Scholar 

  34. Müller C, Mayer C, Dörrenberg S et al (2011) Female but not male dogs respond to a size constancy violation. Biol Lett 7:689–691. doi:10.1098/rsbl.2011.0287

    PubMed Central  PubMed  Article  Google Scholar 

  35. Nawroth C, Ebersbach M, von Borell E (2013) Are juvenile domestic pigs (Sus scrofa domestica) sensitive to the attentive states of humans?—The impact of impulsivity on choice behaviour. Behav Process 96:53–58. doi:10.1016/j.beproc.2013.03.002

    Article  Google Scholar 

  36. Nawroth C, von Borell E, Langbein J (2014a) Exclusion performance in dwarf goats (Capra aegagrus hircus) and sheep (Ovis orientalis aries). PLoS ONE 9:e93534. doi:10.1371/journal.pone.0093534

    PubMed Central  PubMed  Article  Google Scholar 

  37. Nawroth C, Ebersbach M, von Borell E (2014b) Juvenile domestic pigs (Sus scrofa domestica) use human-given cues in an object choice task. Anim Cogn 17:701–713. doi:10.1007/s10071-013-0702-3

    PubMed  Article  Google Scholar 

  38. Povinelli DJ, Eddy TJ (1996) What young chimpanzees know about seeing. Monogr Soc Res Child Dev 61:1–191

    Google Scholar 

  39. Proops L, McComb K (2010) Attributing attention: the use of human-given cues by domestic horses (Equus caballus). Anim Cogn 13:197–205. doi:10.1007/s10071-009-0257-5

    PubMed  Article  Google Scholar 

  40. Proops L, McComb K (2012) Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans. Proc R Soc B Biol Sci 279:3131–3138. doi:10.1098/rspb.2012.0626

    Article  Google Scholar 

  41. Proops L, Walton M, McComb K (2010) The use of human-given cues by domestic horses, Equus caballus, during an object choice task. Anim Behav 79:1205–1209. doi:10.1016/j.anbehav.2010.02.015

    Article  Google Scholar 

  42. Proops L, Rayner J, Taylor AM, McComb K (2013) The responses of young domestic horses to human-given cues. PLoS ONE 8:e67000. doi:10.1371/journal.pone.0067000

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  43. Range F, Virányi Z (2011) Development of gaze following abilities in wolves (Canis lupus). PLoS ONE 6:e16888

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  44. Rosati AG, Hare B (2009) Looking past the model species: diversity in gaze-following skills across primates. Curr Opin Neurobiol 19:45–51. doi:10.1016/j.conb.2009.03.002

    CAS  PubMed  Article  Google Scholar 

  45. Sandel AA, MacLean EL, Hare B (2011) Evidence from four lemur species that ringtailed lemur social cognition converges with that of haplorhine primates. Anim Behav 81:925–931. doi:10.1016/j.anbehav.2011.01.020

    Article  Google Scholar 

  46. Scheumann M, Call J (2004) The use of experimenter-given cues by South African fur seals (Arctocephalus pusillus). Anim Cogn 7:224–230. doi:10.1007/s10071-004-0216-0

    PubMed  Article  Google Scholar 

  47. Schmidt J, Scheid C, Kotrschal K et al (2011) Gaze direction: a cue for hidden food in rooks (Corvus frugilegus)? Behav Processes 88:88–93. doi:10.1016/j.beproc.2011.08.002

    PubMed Central  PubMed  Article  Google Scholar 

  48. Soproni K, Miklósi Á, Topál J, Csányi V (2001) Comprehension of human communicative signs in pet dogs (Canis familiaris). J Comp Psychol 115:122–126

    CAS  PubMed  Article  Google Scholar 

  49. Spruijt BM, Van den Bos R, Pijlman FTA (2001) A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems. Appl Anim Behav Sci 72:145–171

    PubMed  Article  Google Scholar 

  50. Tempelmann S, Kaminski J, Liebal K (2011) Focus on the essential: all great apes know when others are being attentive. Anim Cogn 14:433–439. doi:10.1007/s10071-011-0378-5

    PubMed  Article  Google Scholar 

  51. Tomasello M, Call J, Hare B (1998) Five primate species follow the visual gaze of conspecifics. Anim Behav 55:1063–1069

    PubMed  Article  Google Scholar 

  52. Udell MaR, Dorey NR, Wynne CDL (2008) Wolves outperform dogs in following human social cues. Anim Behav 76:1767–1773. doi:10.1016/j.anbehav.2008.07.028

    Article  Google Scholar 

  53. Von Bayern AMP, Emery NJ (2009) Jackdaws respond to human attentional states and communicative cues in different contexts. Curr Biol 19:602–606. doi:10.1016/j.cub.2009.02.062

    Article  Google Scholar 

  54. Wilkinson A, Mandl I, Bugnyar T, Huber L (2010) Gaze following in the red-footed tortoise (Geochelone carbonaria). Anim Cogn 13:765–769. doi:10.1007/s10071-010-0320-2

    PubMed  Article  Google Scholar 

  55. Zimmerman PH, Buijs SaF, Bolhuis JE, Keeling LJ (2011) Behaviour of domestic fowl in anticipation of positive and negative stimuli. Anim Behav 81:569–577. doi:10.1016/j.anbehav.2010.11.028

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Katrin Siebert for data coding, Gerd Nürnberg for statistical advice, and Dieter Sehland and Heinz Deike for excellent technical assistance.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jan Langbein.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (MP4 13,142 kb)

Supplementary material 2 (MP4 10,226 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nawroth, C., von Borell, E. & Langbein, J. ‘Goats that stare at men’: dwarf goats alter their behaviour in response to human head orientation, but do not spontaneously use head direction as a cue in a food-related context. Anim Cogn 18, 65–73 (2015). https://doi.org/10.1007/s10071-014-0777-5

Download citation

Keywords

  • Dwarf goats
  • Social cognition
  • Food-anticipation paradigm
  • Attentive states
  • Human-given cues