Analyze Diet
Animals : an open access journal from MDPI2019; 9(5); doi: 10.3390/ani9050265

Horses’ (Equus Caballus) Laterality, Stress Hormones, and Task Related Behavior in Innovative Problem-Solving.

Abstract: Domesticated horses are constantly confronted with novel tasks. A recent study on anecdotal data indicates that some are innovative in dealing with such tasks. However, innovative behavior in horses has not previously been investigated under experimental conditions. In this study, we investigated whether 16 horses found an innovative solution when confronted with a novel feeder. Moreover, we investigated whether innovative behavior in horses may be affected by individual aspects such as: age, sex, size, motor and sensory laterality, fecal stress hormone concentrations (GCMs), and task-related behavior. Our study revealed evidence for 25% of the horses being capable of innovative problem solving for operating a novel feeder. Innovative horses of the present study were active, tenacious, and may be considered to have a higher inhibitory control, which was revealed by their task related behavior. Furthermore, they appeared to be emotional, reflected by high baseline GCM concentrations and a left sensory and motor laterality. These findings may contribute to the understanding of horses' cognitive capacities to deal with their environment and calls for enriched environments in sports and leisure horse management.
Publication Date: 2019-05-22 PubMed ID: 31121937PubMed Central: PMC6562608DOI: 10.3390/ani9050265Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research examines the innovative problem-solving abilities of horses, focusing on individual factors such as age, sex, size, sensory and motor laterality, stress hormone levels, and task-related behavior. The study concluded that a quarter of the test horses demonstrated innovative behavior, showing traits such as activity, tenacity, high inhibitory control, emotional response, and left-sided sensory and motor laterality.

Investigating Innovative Behavior in Horses

The researchers observed 16 horses as they attempted to operate a novel feeder. This study aimed to determine whether horses could display innovative behavior – something that anecdotal evidence had suggested but had not been empirically tested before. The researchers operationalized “innovative behavior” as the ability of the horses to solve a new problem independently, namely, figuring out how to use the new feeder.

  • 25% of the horses in the study were found to be capable of solving the problem, demonstrating that some horses could indeed display innovative behavior.

Examining Factors Associated with Innovative Behavior

The researchers also examined various factors to see if they had an impact on this innovative behavior.

  • They considered individual aspects including the horse’s age, sex, and size, but the findings did not imply any of these affected the horses’ problem-solving ability.
  • Motor and sensory laterality were found to be significant, with those horses demonstrating innovative behavior showing a left-sided bias. This suggests a potential link between brain hemisphere specialization and innovative behavior in horses.
  • High levels of stress hormones (GCM concentrations) were also found in the innovative horses, indicating they might experience elevated emotionality.
  • The study also discovered that task-related behavior, including the horses’ activity level, tenaciousness, and inhibitory control, also played a significant role in their ability to solve the problem.

Implications of the Findings

These findings have important implications for understanding horses’ cognitive capacities and their ability to engage with and adapt to their environment. Recognizing this cognitive ability calls for more extended environments for horses in sports and leisure management, which could potentially stimulate their problem-solving abilities and improve their welfare. These findings also contribute to a growing body of evidence indicating the cognitive abilities of horses and their capacity for innovative problem-solving.

Cite This Article

APA
Esch L, Wöhr C, Erhard M, Krüger K. (2019). Horses’ (Equus Caballus) Laterality, Stress Hormones, and Task Related Behavior in Innovative Problem-Solving. Animals (Basel), 9(5). https://doi.org/10.3390/ani9050265

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 9
Issue: 5

Researcher Affiliations

Esch, Laureen
  • Department of Veterinary Sciences, Faculty of Veterinary Medicine, Animal Hygiene and Animal Husbandry, Chair of Animal Welfare, Ethology, Ludwig Maximilian University Munich, Veterinaerstr 13/R, 80539 Munich, Germany. laureen.esch@gmx.de.
  • Department Equine Economics, Economics and Management, Faculty Agriculture, Nuertingen-Geislingen University, Neckarsteige 6-10, 72622 Nuertingen, Germany. laureen.esch@gmx.de.
Wöhr, Caroline
  • Department of Veterinary Sciences, Faculty of Veterinary Medicine, Animal Hygiene and Animal Husbandry, Chair of Animal Welfare, Ethology, Ludwig Maximilian University Munich, Veterinaerstr 13/R, 80539 Munich, Germany. caroline.woehr@tierhyg.vetmed.uni-muenchen.de.
Erhard, Michael
  • Department of Veterinary Sciences, Faculty of Veterinary Medicine, Animal Hygiene and Animal Husbandry, Chair of Animal Welfare, Ethology, Ludwig Maximilian University Munich, Veterinaerstr 13/R, 80539 Munich, Germany. m.erhard@tierhyg.vetmed.uni-muenchen.de.
Krüger, Konstanze
  • Department Equine Economics, Economics and Management, Faculty Agriculture, Nuertingen-Geislingen University, Neckarsteige 6-10, 72622 Nuertingen, Germany. konstanze.Krueger@hfwu.de.
  • Zoology/Evolutionary Biology, University of Regensburg, Universitaetsstraße 31, 93053 Regensburg, Germany. konstanze.Krueger@hfwu.de.

Grant Funding

  • MWK / Ministerium für Wissenschaft, Forschung und Kunst Baden-Württemberg

Conflict of Interest Statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

This article includes 90 references
  1. McGreevy P, Winther Christensen J, von Borstel UK, McLean A. Equitation Science. 2nd ed. John Wiley & Sons Incorporated; Newark, NJ, USA: 2018.
  2. Hockenhull J, Whay HR. A review of approaches to assessing equine welfare. Equine Vet. Educ. 2014;26:159–166.
    doi: 10.1111/eve.12129google scholar: lookup
  3. Brubaker L, Udell MA. Cognition and learning in horses (Equus caballus): What we know and why we should ask more.. Behav Processes 2016 May;126:121-31.
    doi: 10.1016/j.beproc.2016.03.017pubmed: 27018202google scholar: lookup
  4. Reader SM, Laland KN. Social intelligence, innovation, and enhanced brain size in primates.. Proc Natl Acad Sci U S A 2002 Apr 2;99(7):4436-41.
    doi: 10.1073/pnas.062041299pmc: PMC123666pubmed: 11891325google scholar: lookup
  5. Lefebvre L, Whittle P, Lascaris E, Finkelstein A. Feeding innovations and forebrain size in birds. Anim. Behav. 1997;53:549–560.
    doi: 10.1006/anbe.1996.0330google scholar: lookup
  6. Güntürkün O. The convergent evolution of neural substrates for cognition.. Psychol Res 2012 Mar;76(2):212-9.
    doi: 10.1007/s00426-011-0377-9pubmed: 21881941google scholar: lookup
  7. Ramsey G, Bastian ML, van Schaik C. Animal innovation defined and operationalized.. Behav Brain Sci 2007 Aug;30(4):393-407; discussion 407-32.
    doi: 10.1017/S0140525X07002373pubmed: 18081967google scholar: lookup
  8. Griffin AS, Guez D. Innovation and problem solving: a review of common mechanisms.. Behav Processes 2014 Nov;109 Pt B:121-34.
    doi: 10.1016/j.beproc.2014.08.027pubmed: 25245306google scholar: lookup
  9. Griffin AS. Innovativeness as an emergent property: a new alignment of comparative and experimental research on animal innovation.. Philos Trans R Soc Lond B Biol Sci 2016 Mar 19;371(1690).
    doi: 10.1098/rstb.2015.0544pmc: PMC4780539pubmed: 26926287google scholar: lookup
  10. Meehan CL, Mench JA. The challenge of challenge: Can problem solving opportunities enhance animal welfare?. Appl. Anim. Behav. Sci. 2007;102:246–261.
  11. Thornton A, Samson J. Innovative problem solving in wild meerkats. Anim. Behav. 2012;83:1459–1468.
  12. Kummer H, Goodall J. Conditions of innovative behaviour in primates. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1985;308:203–214.
    doi: 10.1098/rstb.1985.0020google scholar: lookup
  13. Boogert NJ, Reader SM, Hoppitt W, Laland KN. The origin and spread of innovations in starlings. Anim. Behav. 2008;75:1509–1518.
  14. Cole EF, Quinn JL. Personality and problem-solving performance explain competitive ability in the wild.. Proc Biol Sci 2012 Mar 22;279(1731):1168-75.
    doi: 10.1098/rspb.2011.1539pmc: PMC3267141pubmed: 21937498google scholar: lookup
  15. Griffin AS, Diquelou M, Perea M. Innovative problem solving in birds: A key role of motor diversity. Anim. Behav. 2014;92:221–227.
  16. Manrique HM, Völter CJ, Call J. Repeated innovation in great apes. Anim. Behav. 2013;85:195–202.
  17. Morand-Ferron J, Quinn JL. Larger groups of passerines are more efficient problem solvers in the wild.. Proc Natl Acad Sci U S A 2011 Sep 20;108(38):15898-903.
    doi: 10.1073/pnas.1111560108pmc: PMC3179046pubmed: 21930936google scholar: lookup
  18. Sol D, Griffin AS, Bartomeus I. Consumer and motor innovation in the common myna: The role of motivation and emotional responses. Anim. Behav. 2012;83:179–188.
  19. Webster SJ, Lefebvre L. Problem solving and neophobia in a columbiform–passeriform assemblage in Barbados. Anim. Behav. 2001;62:23–32.
    doi: 10.1006/anbe.2000.1725google scholar: lookup
  20. Lonsdorf EV, Ross SR, Linick SA, Milstein MS, Melber TN. An experimental, comparative investigation of tool use in chimpanzees and gorillas. Anim. Behav. 2009;77:1119–1126.
  21. Benson-Amram S, Holekamp KE. Innovative problem solving by wild spotted hyenas.. Proc Biol Sci 2012 Oct 7;279(1744):4087-95.
    doi: 10.1098/rspb.2012.1450pmc: PMC3427591pubmed: 22874748google scholar: lookup
  22. Greenberg R. The role of neophobia and neophilia in the development of innovative behaviour of birds. In: Reader SM, Laland KN, editors. Animal Innovation. Oxford University Press; Oxford, UK: 2003. pp. 175–196.
  23. Reader SM, Laland KN. Primate innovation: Sex, age and social rank differences. Int. J. Primatol. 2000;22:787–805.
    doi: 10.1023/A:1012069500899google scholar: lookup
  24. Cole EF, Cram DL, Quinn JL. Individual variation in spontaneous problem-solving performance among wild great tits. Anim. Behav. 2011;81:491–498.
  25. Hunt GR, Corballis MC, Gray RD. Animal behaviour: Laterality in tool manufacture by crows.. Nature 2001 Dec 13;414(6865):707.
    doi: 10.1038/414707apubmed: 11742382google scholar: lookup
  26. Magat M, Brown C. Laterality enhances cognition in Australian parrots.. Proc Biol Sci 2009 Dec 7;276(1676):4155-62.
    doi: 10.1098/rspb.2009.1397pmc: PMC2821354pubmed: 19726480google scholar: lookup
  27. Austin NP, Rogers LJ. Lateralization of agonistic and vigilance responses in Przewalski horses (Equus przewalskii). Appl. Anim. Behav. Sci. 2014;151:43–50.
  28. Brooks DE, Komàromy AM, Källberg ME. Comparative retinal ganglion cell and optic nerve morphology.. Vet Ophthalmol 1999;2(1):3-11.
  29. Farmer K, Krüger K, Byrne RW, Marr I. Sensory laterality in affiliative interactions in domestic horses and ponies (Equus caballus).. Anim Cogn 2018 Sep;21(5):631-637.
    doi: 10.1007/s10071-018-1196-9pmc: PMC6097077pubmed: 29948296google scholar: lookup
  30. Austin NP, Rogers LJ. Limb preferences and lateralization of aggression, reactivity and vigilance in feral horses, Equus caballus. Anim. Behav. 2012;83:239–247.
  31. Siniscalchi M, Padalino B, Lusito R, Quaranta A. Is the left forelimb preference indicative of a stressful situation in horses?. Behav Processes 2014 Sep;107:61-7.
    doi: 10.1016/j.beproc.2014.07.018pubmed: 25108052google scholar: lookup
  32. Schultheiss OC, Riebel K, Jones NM. Activity inhibition: a predictor of lateralized brain function during stress?. Neuropsychology 2009 May;23(3):392-404.
    doi: 10.1037/a0014591pubmed: 19413452google scholar: lookup
  33. Vallortigara G, Rogers LJ. Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization.. Behav Brain Sci 2005 Aug;28(4):575-89; discussion 589-633.
    doi: 10.1017/S0140525X05000105pubmed: 16209828google scholar: lookup
  34. Rogers LJ. Hand and paw preferences in relation to the lateralized brain.. Philos Trans R Soc Lond B Biol Sci 2009 Apr 12;364(1519):943-54.
    doi: 10.1098/rstb.2008.0225pmc: PMC2666076pubmed: 19064357google scholar: lookup
  35. McGreevy PD, Rogers LJ. Motor and sensory laterality in thoroughbred horses. Appl. Anim. Behav. Sci. 2005;92:337–352.
  36. MacNeilage PF, Rogers LJ, Vallortigara G. Origins of the left & right brain.. Sci Am 2009 Jul;301(1):60-7.
  37. Wells AE, Blache D. Horses do not exhibit motor bias when their balance is challenged.. Animal 2008 Nov;2(11):1645-50.
    doi: 10.1017/S1751731108002772pubmed: 22444016google scholar: lookup
  38. Marr I, Farmer K, Krüger K. Evidence for Right-Sided Horses Being More Optimistic than Left-Sided Horses.. Animals (Basel) 2018 Nov 22;8(12).
    doi: 10.3390/ani8120219pmc: PMC6315450pubmed: 30469484google scholar: lookup
  39. Rogers LJ. A Matter of degree: Strength of brain asymmetry and behaviour. Symmetry 2017;9:57.
    doi: 10.3390/sym9040057google scholar: lookup
  40. Marshall-Pescini S, Barnard S, Branson NJ, Valsecchi P. The effect of preferential paw usage on dogs' (Canis familiaris) performance in a manipulative problem-solving task.. Behav Processes 2013 Nov;100:40-3.
    doi: 10.1016/j.beproc.2013.07.017pubmed: 23933377google scholar: lookup
  41. Mendl M. Performing under pressure: Stress and cognitive function. Appl. Anim. Behav. Sci. 1999;65:221–244.
  42. McEwen BS, Sapolsky RM. Stress and cognitive function.. Curr Opin Neurobiol 1995 Apr;5(2):205-16.
    doi: 10.1016/0959-4388(95)80028-Xpubmed: 7620309google scholar: lookup
  43. Grace L, Hescham S, Kellaway LA, Bugarith K, Russell VA. Effect of exercise on learning and memory in a rat model of developmental stress.. Metab Brain Dis 2009 Dec;24(4):643-57.
    doi: 10.1007/s11011-009-9162-5pmc: PMC2857751pubmed: 19821018google scholar: lookup
  44. Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E. Stress revisited: a critical evaluation of the stress concept.. Neurosci Biobehav Rev 2011 Apr;35(5):1291-301.
  45. Laland KN, Reader SM. Foraging innovation is inversely related to competitive ability in male but not in female guppies. Behav. Ecol. 1999;10:270–274.
    doi: 10.1093/beheco/10.3.270google scholar: lookup
  46. Hopper LM, Price SA, Freeman HD, Lambeth SP, Schapiro SJ, Kendal RL. Influence of personality, age, sex, and estrous state on chimpanzee problem-solving success.. Anim Cogn 2014 Jul;17(4):835-47.
    doi: 10.1007/s10071-013-0715-ypmc: PMC4681294pubmed: 24322874google scholar: lookup
  47. Tebbich S, Sterelny K, Teschke I. The tale of the finch: adaptive radiation and behavioural flexibility.. Philos Trans R Soc Lond B Biol Sci 2010 Apr 12;365(1543):1099-109.
    doi: 10.1098/rstb.2009.0291pmc: PMC2830236pubmed: 20194172google scholar: lookup
  48. Olczak K, Winther Christensen J, Klocek C. Food motivation in horses appears stable across different test situations. Appl. Anim. Behav. Sci. 2018;204:60–65.
  49. Krueger K, Esch L, Byrne RW. Animal behaviour in a human world: A crowd sourcing study on horses that open door and gate mechanisms. PLoS ONE 2018 under Review.
  50. Mader DR, Price EO. Discrimination learning in horses: effects of breed, age and social dominance.. J Anim Sci 1980 May;50(5):962-5.
    doi: 10.2527/jas1980.505962xpubmed: 7390949google scholar: lookup
  51. Krueger K, Heinze J. Horse sense: social status of horses (Equus caballus) affects their likelihood of copying other horses' behavior.. Anim Cogn 2008 Jul;11(3):431-9.
    doi: 10.1007/s10071-007-0133-0pubmed: 18183432google scholar: lookup
  52. Krueger K, Farmer K, Heinze J. The effects of age, rank and neophobia on social learning in horses.. Anim Cogn 2014 May;17(3):645-55.
    doi: 10.1007/s10071-013-0696-xpubmed: 24170136google scholar: lookup
  53. Wolff A, Hausberger M. Learning and memorisation of two different tasks in horses: The effects of age, sex and sire. Appl. Anim. Behav. Sci. 1996;46:137–143.
  54. Winther Christensen J, Ahrendt LP, Lintrup R, Gaillard C, Palme R, Malmkvist J. Does learning performance in horses relate to fearfulness, baseline stress hormone, and social rank?. Appl. Anim. Behav. Sci. 2012;140:44–52.
  55. Lansade L, Simon F. Horses’ learning performances are under the influence of several temperamental dimensions. Appl. Anim. Behav. Sci. 2010;125:30–37.
  56. Petersen JL, Mickelson JR, Rendahl AK, Valberg SJ, Andersson LS, Axelsson J, Bailey E, Bannasch D, Binns MM, Borges AS, Brama P, da Câmara Machado A, Capomaccio S, Cappelli K, Cothran EG, Distl O, Fox-Clipsham L, Graves KT, Guérin G, Haase B, Hasegawa T, Hemmann K, Hill EW, Leeb T, Lindgren G, Lohi H, Lopes MS, McGivney BA, Mikko S, Orr N, Penedo MC, Piercy RJ, Raekallio M, Rieder S, Røed KH, Swinburne J, Tozaki T, Vaudin M, Wade CM, McCue ME. Genome-wide analysis reveals selection for important traits in domestic horse breeds.. PLoS Genet 2013;9(1):e1003211.
  57. Pirault P, Danvy S, Verrier E, Leroy G. Genetic structure and gene flows within horses: a genealogical study at the french population scale.. PLoS One 2013;8(4):e61544.
  58. Henneke DR, Potter GD, Kreider JL, Yeates BF. Relationship between condition score, physical measurements and body fat percentage in mares.. Equine Vet J 1983 Oct;15(4):371-2.
  59. Bundesministerium für Ernährung Landwirtschaft und Verbraucherschutz. Leitlinien zur Beurteilung von Pferdehaltungen unter Tierschutzgesichtspunkten. Bundesministerium für Ernährung, Landwirtschaft und Verbraucherschutz; Bonn, Germany: 2009.
  60. Winther Christensen J, Zharkikh T, Chovaux E. Object recognition and generalisation during habituation in horses. Appl. Anim. Behav. Sci. 2011;129:83–91.
  61. Leiner L, Fendt M. Behavioural fear and heart rate responses of horses after exposure to novel objects: Effects of habituation. Appl. Anim. Behav. Sci. 2011;131:104–109.
  62. Roberts SM. Equine vision and optics.. Vet Clin North Am Equine Pract 1992 Dec;8(3):451-7.
    doi: 10.1016/S0749-0739(17)30435-2pubmed: 1458323google scholar: lookup
  63. Murphy J, Hall C, Arkins S. What horses and humans see: A comparative review. Int. J. Zool. 2009;2009:1–14.
    doi: 10.1155/2009/721798google scholar: lookup
  64. McLean AN. Short-term spatial memory in the domestic horse. Appl. Anim. Behav. Sci. 2004;85:93–105.
  65. Baragli P, Vitale V, Paoletti E, Mengoli M, Sighieri C. Encoding the object position for assessment of short term spatial memory in horses (Equus caballus). Int. J. Comp. Psychol. 2011;24:284–291.
  66. Larose C, Richard-Yris MA, Hausberger M, Rogers LJ. Laterality of horses associated with emotionality in novel situations.. Laterality 2006 Jul;11(4):355-67.
    doi: 10.1080/13576500600624221pubmed: 16754236google scholar: lookup
  67. Möstl E, Palme R. Hormones as indicators of stress.. Domest Anim Endocrinol 2002 Jul;23(1-2):67-74.
    doi: 10.1016/S0739-7240(02)00146-7pubmed: 12142227google scholar: lookup
  68. Palme R. Monitoring stress hormone metabolites as a useful, non-invasive tool for welfare assessment in farm animals. Anim. Welf. 2012;21:331–337.
    doi: 10.7120/09627286.21.3.331google scholar: lookup
  69. Pawluski J, Jego P, Henry S, Bruchet A, Palme R, Coste C, Hausberger M. Low plasma cortisol and fecal cortisol metabolite measures as indicators of compromised welfare in domestic horses (Equus caballus).. PLoS One 2017;12(9):e0182257.
  70. Krueger K, Marr I, Dobler A, Palme R. Preservation of fecal cortisol metabolites (GCM) and immunoglobulin A (IgA) through silica gel drying for field studies in horses: submitted. Conserv. Physiol. 2019.
  71. Flauger B, Krueger K, Gerhards H, Möstl E. Simplified method to measure glucocorticoid metabolites in faeces of horses.. Vet Res Commun 2010 Feb;34(2):185-95.
    doi: 10.1007/s11259-010-9344-ypubmed: 20182914google scholar: lookup
  72. van de Waal E, Borgeaud C, Whiten A. Potent social learning and conformity shape a wild primate's foraging decisions.. Science 2013 Apr 26;340(6131):483-5.
    doi: 10.1126/science.1232769pubmed: 23620053google scholar: lookup
  73. Sih A, Del Giudice M. Linking behavioural syndromes and cognition: a behavioural ecology perspective.. Philos Trans R Soc Lond B Biol Sci 2012 Oct 5;367(1603):2762-72.
    doi: 10.1098/rstb.2012.0216pmc: PMC3427552pubmed: 22927575google scholar: lookup
  74. Marchetti C, Drent PJ. Individual differences in the use of social information in foraging by captive great tits.. Anim Behav 2000 Jul;60(1):131-140.
    doi: 10.1006/anbe.2000.1443pubmed: 10924212google scholar: lookup
  75. Amici F, Aureli F, Call J. Fission-fusion dynamics, behavioral flexibility, and inhibitory control in primates.. Curr Biol 2008 Sep 23;18(18):1415-9.
    doi: 10.1016/j.cub.2008.08.020pubmed: 18804375google scholar: lookup
  76. Bray EE, MacLean EL, Hare BA. Context specificity of inhibitory control in dogs.. Anim Cogn 2014 Jan;17(1):15-31.
    doi: 10.1007/s10071-013-0633-zpmc: PMC4154138pubmed: 23584618google scholar: lookup
  77. Wimpenny JH, Weir AA, Clayton L, Rutz C, Kacelnik A. Cognitive processes associated with sequential tool use in New Caledonian crows.. PLoS One 2009 Aug 5;4(8):e6471.
  78. Griffin AS, Diquelou MC. Innovative problem solving in birds: A cross-species comparison of two highly successful passerines. Anim. Behav. 2015;100:84–94.
  79. Greenberg R, Mettke-Hofmann C. Ecological aspects of Neophobia and Neophilia in birds. Current Ornithology. Volume 319. Springer; Boston, MA, USA: 2001. pp. 119–178.
  80. Rogers LJ. Relevance of brain and behavioural lateralization to animal welfare. Appl. Anim. Behav. Sci. 2010;127:1–11.
  81. Rogers LJ, Zucca P, Vallortigara G. Advantages of having a lateralized brain.. Proc Biol Sci 2004 Dec 7;271 Suppl 6(Suppl 6):S420-2.
    doi: 10.1098/rsbl.2004.0200pmc: PMC1810119pubmed: 15801592google scholar: lookup
  82. Hausberger M, Fureix C, Bourjade M, Wessel-Robert S, Richard-Yris MA. On the significance of adult play: what does social play tell us about adult horse welfare?. Naturwissenschaften 2012 Apr;99(4):291-302.
    doi: 10.1007/s00114-012-0902-8pubmed: 22402927google scholar: lookup
  83. Duberstein KJ, Gilkeson JA. Determination of sex differences in personality and trainability of yearling horses utilizing a handler questionnaire. App. Anim. Behav. Sci. 2010;128:57–63.
  84. Miyata H, Gajdon GK, Huber L, Fujita K. How do keas (Nestor notabilis) solve artificial-fruit problems with multiple locks?. Anim Cogn 2011 Jan;14(1):45-58.
    doi: 10.1007/s10071-010-0342-9pubmed: 20640911google scholar: lookup
  85. HARLOW HF, HARLOW MK, MEYER DR. Learning motivated by a manipulation drive.. J Exp Psychol 1950 Apr;40(2):228-34.
    doi: 10.1037/h0056906pubmed: 15415520google scholar: lookup
  86. Hagen K, Broom DM. Emotional reactions to learning in cattle. App. Anim. Behav. Sci. 2004;85:203–213.
  87. von Bayern AM, Heathcote RJ, Rutz C, Kacelnik A. The role of experience in problem solving and innovative tool use in crows.. Curr Biol 2009 Dec 1;19(22):1965-8.
    doi: 10.1016/j.cub.2009.10.037pubmed: 19913421google scholar: lookup
  88. Deaner RO, Isler K, Burkart J, van Schaik C. Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates.. Brain Behav Evol 2007;70(2):115-24.
    doi: 10.1159/000102973pubmed: 17510549google scholar: lookup
  89. Murphy J, Arkins S. Equine learning behaviour.. Behav Processes 2007 Sep;76(1):1-13.
    doi: 10.1016/j.beproc.2006.06.009pubmed: 17400403google scholar: lookup
  90. Reader SM, Hager Y, Laland KN. The evolution of primate general and cultural intelligence.. Philos Trans R Soc Lond B Biol Sci 2011 Apr 12;366(1567):1017-27.
    doi: 10.1098/rstb.2010.0342pmc: PMC3049098pubmed: 21357224google scholar: lookup

Citations

This article has been cited 12 times.
  1. Krueger K, Trager L, Farmer K, Byrne R. Tool Use in Horses. Animals (Basel) 2022 Jul 22;12(15).
    doi: 10.3390/ani12151876pubmed: 35892526google scholar: lookup
  2. Krueger K, Schwarz S, Marr I, Farmer K. Laterality in Horse Training: Psychological and Physical Balance and Coordination and Strength Rather Than Straightness. Animals (Basel) 2022 Apr 16;12(8).
    doi: 10.3390/ani12081042pubmed: 35454288google scholar: lookup
  3. Rowell MK, Santymire RM, Rymer TL. Corticosterone Metabolite Concentration Is Not Related to Problem Solving in the Fawn-Footed Mosaic-Tailed Rat Melomys Cervinipes. Animals (Basel) 2021 Dec 30;12(1).
    doi: 10.3390/ani12010082pubmed: 35011188google scholar: lookup
  4. Krueger K, Esch L, Byrne R. Need or opportunity? A study of innovations in equids. PLoS One 2021;16(9):e0257730.
    doi: 10.1371/journal.pone.0257730pubmed: 34570831google scholar: lookup
  5. Baragli P, Scopa C, Felici M, Reddon AR. Horses show individual level lateralisation when inspecting an unfamiliar and unexpected stimulus. PLoS One 2021;16(8):e0255688.
    doi: 10.1371/journal.pone.0255688pubmed: 34351986google scholar: lookup
  6. Caicoya AL, Colell M, Ensenyat C, Amici F. Problem solving in European bison (Bison bonasus): two experimental approaches. R Soc Open Sci 2021 Apr 28;8(4):201901.
    doi: 10.1098/rsos.201901pubmed: 34007461google scholar: lookup
  7. Perry S, Carter A, Smolla M, Akçay E, Nöbel S, Foster JG, Healy SD. Not by transmission alone: the role of invention in cultural evolution. Philos Trans R Soc Lond B Biol Sci 2021 Jul 5;376(1828):20200049.
    doi: 10.1098/rstb.2020.0049pubmed: 33993757google scholar: lookup
  8. Krueger K, Esch L, Byrne R. Animal behaviour in a human world: A crowdsourcing study on horses that open door and gate mechanisms. PLoS One 2019;14(6):e0218954.
    doi: 10.1371/journal.pone.0218954pubmed: 31242266google scholar: lookup
  9. Ricci-Bonot C, Brosche K, Baragli P, Nicol C. A systematic review on the effect of individual characteristics and management practices on equine cognition. Anim Cogn 2025 Nov 26;28(1):96.
    doi: 10.1007/s10071-025-02016-2pubmed: 41296132google scholar: lookup
  10. Haussler KK, le Jeune SS, MacKechnie-Guire R, Latif SN, Clayton HM. The Challenge of Defining Laterality in Horses: Is It Laterality or Just Asymmetry?. Animals (Basel) 2025 Jan 21;15(3).
    doi: 10.3390/ani15030288pubmed: 39943060google scholar: lookup
  11. Poochipakorn C, Wonghanchao T, Sanigavatee K, Chanda M. Stress Responses in Horses Housed in Different Stable Designs during Summer in a Tropical Savanna Climate. Animals (Basel) 2024 Aug 4;14(15).
    doi: 10.3390/ani14152263pubmed: 39123789google scholar: lookup
  12. Goma AA, Uddin J, Kieson E. Lateralised Behavioural Responses in Livestock to Environmental Stressors: Implications for Using Infrared Thermography to Assess Welfare Conditions. Animals (Basel) 2023 Nov 27;13(23).
    doi: 10.3390/ani13233663pubmed: 38067014google scholar: lookup