- Email: [email protected]
Asymmetry of behavioral responses to a human approach in young naive vs. trained horses
Physiology & Behavior 104 (2011) 464–468
Contents lists available at ScienceDirect
Physiology & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p h b
Asymmetry of behavioral responses to a human approach in young naive vs. trained horses Carol Sankey a,⁎, Séverine Henry a, Caroline Clouard a, Marie-Annick Richard-Yris b, Martine Hausberger a, b a b
Laboratoire d'éthologie animale et humaine-UMR 6552 CNRS/ Université de Rennes 1, Station Biologique, 35380 Paimpont, France Laboratoire d'éthologie animale et humaine - UMR 6552 CNRS/Université de Rennes 1, Avenue du Général Leclerc, Campus de Beaulieu, F-35042 Rennes Cedex, France
a r t i c l e
i n f o
Article history: Received 17 September 2010 Received in revised form 12 April 2011 Accepted 6 May 2011 Keywords: Laterality Emotionality Human approach Horse
a b s t r a c t The aim of this study was to investigate the impact of training experience on young horses (Equus caballus)’ lateralized responses to an approaching human. The results show that the one year old untrained horses display asymmetrical responses to an approaching human, with more negative reactions (escapes, threats) when approached from the left side, while approaches towards the right shoulder elicited more positive behaviors. On the contrary, two years old trained horses reacted equally positively to approaches and contact on both sides. Our findings support those of previous studies investigating a link between emotionality and laterality and confirm the role of the left hemisphere in the processing of novel or negative stimuli. Moreover, the data underline the impact work and training can have on this laterality in horses. © 2011 Elsevier Inc. All rights reserved.
1. Introduction Long believed to be a human specificity, brain lateralization (i.e. asymmetry of brain function and behavior) is now accepted as a widespread characteristic of vertebrates [1,2] and recent evidence suggests it is also present in some invertebrate species (e.g. [3]). Throughout vertebrates, the general pattern of lateralization observed is that the right hemisphere is involved in the expression of intense emotions and controlling rapid responses, whereas the left hemisphere is concerned with responses that require inhibition of responding until a decision is made [4]. Behavioral laterality has been investigated in both intra- and interspecific encounter situations. For instance, a lateralized approach pattern has recently been demonstrated in mangabeys showing that when individuals approach another group member, they position themselves as so to have the approached individual in their right visual field [5]. In humans, a head turning bias towards the right side has been shown in human adult kissing behavior [6]. Most studies investigating interspecific interactions looked at the specific case of predator–prey encounters (e.g. in toads: [7], dunnarts [8]) or agonistic interactions (e.g. in gelada baboons [9]). Thus, these studies have focused on eye preference or lateralized escape responses as the outcome of a negative encounter. In domestic animals, the case of human animal interactions and more specifically the way to approach an unknown animal has not received particular attention. A single study, conducted by Austin and Rogers [10] investigated the asymmetry of flight turning response to a
⁎ Corresponding author. Tel.: + 33 2 99618155. E-mail address: [email protected] (C. Sankey). 0031-9384/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2011.05.009
human approaching with a frightening object (umbrella) in domestic horses. However, it was more the novel and frightening aspect of the object, rather than the human, that was being tested. Other studies have involved novel objects, including in marmosets [11], chicken [12] or even fish [13]. Here, our study aimed to investigate the behavioral responses of young domestic horses to a human approaching them from the left or right side, as well as to use visual laterality to evaluate the possible impact of horses' training experience on the way they perceive this approaching human (positive, neutral or negative). Horses are traditionally approached and handled on the left side. Yet, understanding lateralization in horses has many practical implications in order to understand current training methods, develop new training paradigms but also help for the selection of horses for the various disciplines and work practices [10]. So far, horses have been shown to display both motor [14] and sensory (e.g. auditory [15]) lateralization patterns. When it comes to visual laterality, horses prove to be a particularly interesting model, for they have laterally placed eyes and an almost complete decussation of the optic fibres [16,17], meaning that what is seen in the right monocular visual field is processed by the left hemisphere and what is seen in the left monocular visual field is processed by the right hemisphere. Interestingly, recent research has shown a link between emotionality and visual laterality in horse: adult horses show greater reactivity when approached by a human holding a novel object in their left monocular visual field [10] and horses that have the highest emotionality index tend to fixate a novel object with their left eye [18]. Up until today, the way this lateralization pattern develops remains unclear, but factors such as age and training experience (Larose et al. [18], Farmer et al. [26]) have been suggested to impact on horses’ emotional laterality.
C. Sankey et al. / Physiology & Behavior 104 (2011) 464–468
465
In this study, we investigated 1) whether one year old, naive horses show a lateralization in their response to a human approaching them from the left or from the right and 2) whether the potential lateralized response pattern differed in two years old horses that had undergone initial training at an earlier age (traditionally performed from the left side). 2. Material and methods 2.1. Study subjects This study was conducted at the “station expérimentale de Chamberet” in France with 39 Angloarabian (N = 33) and French saddlebred (N = 6) young horses, living in groups at pasture. A first group was composed of 16 one year old horses (10 females and 6 castrated males). The particularity of the group was that their experience with humans was limited to minimum veterinary care and feed distribution in the winter period. This group was considered as the “naïve” horses group. A second group was composed of 23 two years old horses (15 females and 8 castrated males). In addition to the veterinary care and winter feeding, these horses had received a two months initial training at the age of one year (cf. [19]), during which they had been trained to remain immobile on a vocal command given from their left side and then to accept usual handling procedures (such as being fitted with a halter and a surcingle, giving their feet, etc.). This group was here considered as the “trained” group. Otherwise, both groups were raised in similar conditions during their first year: from birth until weaning at the age of 6 months, they were brought up as a group with their dams in a pasture. Weanlings then spent their first winter in groups of 5 to 6 individuals in a stall where they stayed until the next Spring. Group 2 horses spent their second summer all together in a pasture, and were pushed in a large indoor stall for a few hours every day in order to carry out their initial training (~4 months). They spent their second winter in individual indoor stalls, where they could see and hear each other and also physically interact with their neighbors through the stall bars. In the Spring 2008, both groups were released in 2 different (but equivalent in size) pastures, sufficiently distant from one another so that they could not see or hear each other.
animals were approached was determined by the animals' availability in the pasture but the order in which the zones were approached for each horse was randomized. Overall, the experimenter approached each horse 7 times, once towards every predefined zone.
2.2. Experimental procedure
2.4. Statistical analysis
In both groups, approach tests were carried out in 1 to 2 daily sessions, lasting 1 to 2 h and took place at different times every day, between 8.30 am and 7.30 pm. In the two groups, all approaches were carried out by the same experimenter (CC, woman who always wore the same dark green coat). She was blind to the horses' earlier experience with humans. During a single session, the experimenter never approached the same horse more than twice. In order to assess the young horses' responses to an approaching human, we defined 7 zones: shoulder, flank and croup on both left and right sides and front (Fig. 1). Each approach followed the same pattern: after choosing an immobile but awake (i.e. eyes open) animal, the experimenter placed herself at a distance of 8 m from the horse and started approaching it following an imaginary line, walking at a constant average speed of one step per second. She walked in a neutral position with her arms beside her body. During the whole approach, she looked at the horse, in the direction of the target zone. When she was close enough (distance b0.2 m), she extended her left arm to gently touch the target zone, while her other arm stayed beside her body. An approach ended when she established contact and touched the target zone or at whatever distance if the animal attempted to avoid, escape or threaten her by any means. Lastly, if another horse interrupted the approach by placing itself in the experimenter's trajectory, the approach was canceled and repeated later. The order in which the
Binomial tests allowed us to compare the frequency of successful approaches (i.e. leading to contact) as well as the frequency of approaches eliciting positive or negative reactions to frequencies expected by chance. Fisher's exact test was used to compare rates of positive/negative reactions between groups. The non-parametric Mann–Whitney U-test was also used to compare the two groups. Alpha was set at 5% for each analysis.
Fig. 1. Diagram of the paths taken by the experimenter to approach the pre-defined zones, commencing 8 m away.
2.3. Data collection The data were recorded by the experimenter herself using a digital voice recorder for later transcription. From the beginning of her approach, she recorded the horse's behavior continuously. She also noted whether the approach led to a contact on the target zone and the animal's positive or negative response to the contact. Standing still, looking at the experimenter and sniffing her were considered positive reactions, while avoidance, escape and threats, threats of biting and of kicking were considered negative reactions [20,21]. Thus, no neutral reactions were recorded.
3. Results 3.1. “Naïve” 1-year-old horses Most yearlings accepted to be touched at least once by the experimenter (N = 15/16). The mean number of zones where they accepted contact was 2.57 ± 0.39 out of the 7 predefined zones. Overall, 35.4% of the approaches from the right led to contact vs. 29.2% of the approaches from the left. Clear differences appeared regarding horses' preference or rather their dislike for certain zones. Left and right shoulders, as well as left flank were more difficult to touch than expected by chance: only 4 out of the 16 horses (20%, but not always the same 4 subjects) accepted to be touched on each of these zones (binomial test, P = 0.04; cf. Table 1), while the others withdrew during the approaches. For the
466
C. Sankey et al. / Physiology & Behavior 104 (2011) 464–468
Table 1 Number and percentage of one and two-year-old horses accepting to be touched on the different zones and their positive or negative response to contact and statistics (binomial tests). 1 year-old (« naïve »)
2 year-old (« trained »)
Approached zone
Success rate
P
Positive reactions
Negative reactions
P
Success rate
P
Positive reactions
Negative reactions
P
Left shoulder Left flank Left croup Front Right shoulder Right flank Right croup
4/16 4/16 6/16 10/16 4/16 8/16 5/16
0.04 0.04 0.2 0.2 0.04 0.6 0.1
0 2 1 6 3 3 3
4 2 5 4 1 5 2
NA NA 0.1 0.4 NA 0.4 0.5
18/23 (78%) 12/23 (52%) 10/23 (43%) 19/23(83%) 18/23 (78%) 14/23 (61%) 18/23 (78%)
0.005 0.5 0.3 0.001 0.005 0.2 0.005
18 10 8 17 18 11 12
0 2 2 2 0 3 6
b0.001 0.02 0.05 b0.001 b0.001 0.03 0.1
(25%) (25%) (38%) (63%) (25%) (50%) (31%)
other predefined zones, the proportion of approaches leading to contact did not significantly differ from chance level (P N 0.05). Concerning a potential lateralization bias in the horses' positive or negative responses to contact by zone (see Table 1 for details), it is interesting to note that amongst the yearlings that let the experimenter approach and touch their shoulders (most commonly approached zone in order to fit horses with their equipment), all of them (4/4) displayed negative reactions (i.e. threats or escape) at contact on the left side, contrary to the right side where most of them (3/4) displayed positive reactions (i.e. immobility or sniffing the experimenter). Though striking, this difference was not statistically tested due to the low number of animals that were touched. No such tendencies were found for the other contact zone (flank, croup). 3.2. Trained horses Here again, most horses accepted to be touched at least once by the experimenter in the pasture (N = 22/23), and the mean number of zones where they accepted contact was 4.74 ± 0.42 out of the 7 predefined zones. Overall, 72.5% of the approaches from the right led to contact vs. 57.9% of the approaches from the left. Clear differences appeared, this time regarding horses' preference for certain zones: left and right shoulders, as well as the front, appeared as privileged contact zones, for the experimenter was able to touch them without the horses fleeing or threatening during the approach (i.e. before contact) (for both shoulders: N = 18/23, binomial tests, P = 0.005; for the front: N = 19/23, binomial test, P = 0.001; cf. Table 1). Most horses also let the experimenter approach their right croup (N = 18/23, binomial test, P = 0.005). For the other predefined zones, the proportion of approaches leading to contact did not significantly differ from chance level (P N 0.05). Moreover, most horses displayed positive rather than negative reactions at contact, whatever the zone touched (binomial tests, P ≤ 0.05), exception made for the right croup for which this difference was not statistically significant (cf. Table 1). For instance, horses that let the experimenter touch their shoulder all displayed positive behaviors (i.e. remaining immobile or turning their head to sniff the experimenter) to the contact, whatever the side (N = 18/18).
Besides, it is noteworthy that whereas the 2 groups' horses behavior did not differ significantly in response to a contact on the right shoulder (number of horses displaying positive behavior: N1 year = 3/4, N2 years = 18/18, Fisher's exact test, P = 0.2; Fig. 2) and croup (N1 year = 3/5, N2 years = 12/18, Fisher's exact test, P = 0.4), they clearly differed in their behavioral response when these zones were touched on the left side (Number of horses displaying positive behavior: shoulder: N1 year = 0/4, N2 years = 18/18, Fisher's exact test, P b 0.001; Fig. 2; croup: N1 year = 1/6, N2 years = 8/10, Fisher's exact test, P = 0.002). 4. Discussion Overall, the one year old “naïve” horses showed a clear asymmetry in their response to an approaching human. They displayed more negative reactions when approached from the left side: two out of the three zones on the left side were amongst the most difficult ones to approach. Moreover, when they did let the experimenter touch their left shoulder, most horses escaped or threatened her. On the contrary, most horses displayed positive behaviors when touched on the right shoulder. However, it seems that the positive training received by the two years old horses alleviated this asymmetry, as these horses reacted equally positively to approaches and contact on both sides. In our study, one year old naïve horses appeared more reluctant to accept contact when approached by the human in their left monocular visual field and conversely better accepted the human approach in their right monocular visual field. This result support previous studies conducted in adult horses, that showed that the left monocular visual field (information processed by the right cerebral hemisphere) was associated with a higher reactivity [10,18] and fits in the theory of valence (right hemisphere mainly processing negative emotions and left hemisphere mostly processing neutral or positive emotions; [22,23]). However, the negative reactions observed in the naïve horses when they were approached on their left side were not displayed by the two years old trained horses. In fact, they did not display asymmetrical behavioral responses and accepted approach and contact equally well on both sides. Age may be a factor as Søndergaard
3.3. Effect of training or age: comparison of the 2 groups As previously mentioned, most yearlings and 2-year-olds accepted to be touched at least once by the experimenter. However, the tolerance of contact was higher in older horses that accepted to be touched on a larger number of predefined zones than yearlings (mean number of zones touched: X1 year = 2.57 ± 0.39; X2 years = 4.74 ± 0.42 out of 7, Mann–Whitney U-test, U = 74.5, P = 0.001). A greater proportion of 2-year-olds accepted contact on both shoulders (Fisher's exact test, N1 year = 4/16, N2 years = 18/23, P = 0.001), as well as on the right croup (Fisher's exact test, N1 year = 5/16, N2 years = 18/23, P = 0.004). There were no significant differences in the tolerance of contact between age groups for the other zones.
Fig. 2. Percentage of horses reacting either positively or negatively to the human touching their left/right shoulder.
C. Sankey et al. / Physiology & Behavior 104 (2011) 464–468
and Halekoh [24] suggest that the chance of a horse approaching a human and the chance of approaching a horse increased with age. Thus, horses' increasing acceptance of an approaching human with age could be attributed to a simple maturation effect, resulting from the normal physiological development horses undergo with age. Nevertheless, this same study revealed that handled horses approached humans more rapidly than unhandled ones [24], showing that older horses are also more familiar, by an effect of habituation to humans due to the daily feeding by humans [24]. In fact, the only direct evidence of age dependent shifts in bias during development is found in humans, chicks and rats [1]. In horses, McGreevy and Rogers reported a shift in motor laterality (foreleg preference) in horses over two years of age, compared to horses aged two years or less [14]. In addition, Larose et al. [18] found that 3 years old Saddlebred horses had a stronger visual lateralization than 2 years old ones. However, studies in other species have reported an effect of age over a much greater span of years than the one year difference observed in Larose et al.'study [18] or ours, in which all horses tested can be classified as young horses. As previously suggested, the training paradigms applied by humans may greatly influence the expression of lateralization in domestic horses [18]. The fact that this study's two years old horses had undergone initial training at the age of one year is probably a very relevant event. The absence of lateralized responses to the human approach could be inferred to the repeated interactions with the trainer, for handling was mostly performed on the left side of the horse (cf. [19]). Other studies previously suggested an effect of work on horses' motor [14] and visual [18] laterality. The question that arises here is one about the type of work that is performed and the emotional memory horses keep about it, for evidence suggests that different training methods can greatly impact the way horses perceive working sessions and more generally the human-horse relationship [25]. In the present study, the initial training of the two years old horses included repeated handling sessions using, or not, positive reinforcement. Such positive reinforcement based training has been shown to have long lasting positive effects on the human–horse relationship [19,25], which could explain the decrease of negative responses on the left side. In most studies, horses’ left eye is repeatedly associated with fear inducing situations; while the right one is associated with more positive events (Larose et al. [18], De Boyer Des Roches et al. [29]). In addition, horses spontaneously display less reactivity to a frightening object on the right side than on the left one (Austin and Rogers [10]). In our study, we observed less emotional reactions on the more “reactive” side (i.e. left) in the horses that had undergone training. In a recent study, Farmer et al. [26] found, on the contrary, that training in an interactive situation induced in horses a strong preference for looking at the trainer with the left eye. The authors argue that the trainers involved were well known to the horses and cared for them and fed them, as well as working with them, so there is no reason to suppose that there would be any negative emotion associated with them. However, in the light of the literature investigating a link between emotionality and laterality, one can question the way horses perceived that particular training situation, for it involved chasing the horse away before turning your back and waiting for it to return (“join up” technique and “hook on” method). Such techniques could indeed be a source of stress and negative emotions associated with the trainer, for a previous study involving the agitation of a stick in front of ponies' heads to make them back up showed that this type of negative reinforcement-based training (i.e. using an aversive stimulus) induced a rise in the ponies' heart rates and a negative perception of training [25]. The fact that in Farmer's study the trainer also fed and cared for the horses may not have been sufficient to compensate the possible negative memory acquired at work, as negative events seem to be stronger in memory than positive ones [27]. Evidence suggests that eye preference to fixate an object may give insight into how an object is perceived [28]. A Study by De Boyer Des
467
Roches [29] revealed that horses use more their left eye to look at an object with a negative emotional value (veterinary's white shirt) than to look at a neutral (plastic cone) or positive (feed bucket) one. Thus, we hypothesize that the type of work and how it is perceived by horses, rather than work itself, impacts differently on horses' perceptual laterality. Knowing that horses perceive the world differently on each side has practical applications. Young or highly reactive horses would certainly learn faster and be more relaxed if first approached on the right side. Beginning their training by handling them on their most reactive side (i.e. left) may in some cases exacerbate their emotional reactivity. Besides, knowing that interocular transfer occurs in horses [30], at least from the right eye to the left one (i.e. from left to right hemisphere; [10]), they could progressively learn to accept approach and handling on the left side. Once a positive relationship is established, this study suggests that the laterality bias may fade to allow horses to accept human contact equally on both sides. Acknowledgements The authors are grateful to the Director and staff of the “Station expérimentale des Haras”, Chamberet. We also wish to thank the COST of the “Haras Nationaux” and the “Region Bretagne” for their financial support. Thanks to Dr Nadav Shashar, Dr Catherine BloisHeulin, Audrey Maille and three anonymous referees for their useful comments on the manuscript. This study complies with the French laws concerning the use of animals in research. References [1] Rogers LJ, Andrew RJ. Comparative Vertebrate Lateralization. New York: Cambridge University Press; 2002. [2] Vallortigara G, Rogers LJ. Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 2005;28:575–89. [3] Rogers LJ, Vallortigara G. Lateral shift of olfactory memory recall by honeybees. PLoS One 2008;3(6):e2340. [4] Rogers LJ. Lateralisation in vertebrates: its early evolution, general pattern, and development. Adv Stud Behav 2002;31:108–61. [5] Baraud I, Buytet B, Bec P, Blois-Heulin C. Social laterality and “transversality” in two species of mangabeys: influence of rank and implication for hemispheric specialization. Behav Brain Res 2009;198:449–58. [6] Güntürkün O. Adult persistence of head turning asymmetry. Nature 2003;421:711. [7] Lippolis G, Bisazza A, Rogers LJ, Vallortigara G. Lateralization of predator avoidance responses in three species of toads. Laterality 2002;7:163–83. [8] Lippolis G, Westman W, McAllan BM, Rogers LJ. Lateralization of escape responses in the striped-faced dunnart, Sminthopsis macroura (Dasyuridae: Marsupalia). Laterality 2005;10:457–70. [9] Casperd JM, Dunbar RIM. Asymmetries in the visual processing of emotional cues during agonistic interactions by gelada baboons. Behav Process 1996;37:57–65. [10] Austin NP, Rogers LJ. Asymmetry of flight and escape turning responses in horses. Laterality 2007;12:464–74. [11] Hook-Costigan MA, Rogers LJ. Lateralized use of the mouth in production of vocalizations by marmosets. Neuropsychologia 1998;36:1265–73. [12] Vallortigara G, Regolin L, Pagni P. Detour behavior, imprinting and visual lateralization in the domestic chick. Cogn Brain Res 1999;7:307–20. [13] Facchin L, Bisazza A, Vallortigara G. What causes lateralisation of detour behavior in fish? Evidence for asymmetries in eye use. Behav Brain Res 1999;103:229–34. [14] McGreevy PD, Rogers LJ. Motor and sensory laterality in thoroughbred horses. Appl Anim Behav Sci 2005;92:337–52. [15] Basile M, Boivin S, Boutin A, Blois-Heulin C, Hausberger M. Socially dependent auditory laterality in domestic horses (Equus caballus). Anim Cogn 2009;12:611–9. [16] Brooks DE, Komaromy AM, Kallberg ME. Comparative retinal ganglion and optic nerve morphology. Vet Ophthalmol 1999;2:1463–5224. [17] Harman AM, Moore S, Hoskins R, Keller P. Horse vision and an explanation for the visual behavior originally explained by the “ramp retina”. Equine Vet J 1999;31: 384–90. [18] Larose C, Richard-Yris M-A, Hausberger M, Rogers L. Laterality of horses associated with emotionality in novel situations. Laterality 2006;11:335–67. [19] Sankey C, Richard-Yris M-A, Leroy H, Henry S, Hausberger M. Training experience induces lasting memories of humans in horses, Equus caballus. Anim Behav 2010;79:869–75. [20] McDonnell S, Haviland J. Agonistic ethogram of the equid bachelor band. Appl Anim Behav Sci 1995;43:147–88. [21] McDonnell S, Poulin A. Equid play ethogram. Appl Anim Behav Sci 2002;78: 263–90. [22] Davidson RJ. Anterior asymmetry and the nature of emotion. Brain Cogn 1992;20: 125–51.
468
C. Sankey et al. / Physiology & Behavior 104 (2011) 464–468
[23] Demaree HA, Everhart DE, Youngstrom EA, Harrison DW. Brain lateralization of emotional processing: historical roots and a future incorporating “dominance”. Behav Cogn Neurosci Rev 2005;4:3–20. [24] Søndergaard E, Halekoh U. Young horses’ reactions to humans in relation to handling and social environment. App Anim Behav Sci 2003;84:265–80. [25] Sankey C, Richard-Yris M-A, Henry S, Fureix C, Nassur F, Hausberger M. Reinforcement as a mediator of the perception of humans by horses (Equus caballus). Anim Cogn 2010;13:753–64. [26] Farmer K, Krueger K, Byrne RW. Visual laterality in the domestic horse (Equus caballus) interacting with humans. Anim Cogn 2010;13:229–38.
[27] Fureix C, Jego P, Sankey C, Hausberger M. How horses (Equus caballus) see the world: humans as significant “objects”. Anim Cogn 2009;12:643–54. [28] McKenzie R, Andrew RJ, Jones RB. Lateralisation in chicks and hens: new evidence for control of response by the right eye system. Neuropsychologia 1998;36:51–8. [29] De Boyer Des Roches A, Richard-Yris M-A, Henry S, Hausberger M. Laterality and emotions: visual laterality in the domestic horse (Equus caballus) differs with objects' emotional value. Physiol Behav 2008;94:487–90. [30] Hanggi EB. Interocular transfer in horses (Equus caballus). J Equine Vet Sci 1999;19 (8):518–24.
Contents lists available at ScienceDirect
Physiology & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p h b
Asymmetry of behavioral responses to a human approach in young naive vs. trained horses Carol Sankey a,⁎, Séverine Henry a, Caroline Clouard a, Marie-Annick Richard-Yris b, Martine Hausberger a, b a b
Laboratoire d'éthologie animale et humaine-UMR 6552 CNRS/ Université de Rennes 1, Station Biologique, 35380 Paimpont, France Laboratoire d'éthologie animale et humaine - UMR 6552 CNRS/Université de Rennes 1, Avenue du Général Leclerc, Campus de Beaulieu, F-35042 Rennes Cedex, France
a r t i c l e
i n f o
Article history: Received 17 September 2010 Received in revised form 12 April 2011 Accepted 6 May 2011 Keywords: Laterality Emotionality Human approach Horse
a b s t r a c t The aim of this study was to investigate the impact of training experience on young horses (Equus caballus)’ lateralized responses to an approaching human. The results show that the one year old untrained horses display asymmetrical responses to an approaching human, with more negative reactions (escapes, threats) when approached from the left side, while approaches towards the right shoulder elicited more positive behaviors. On the contrary, two years old trained horses reacted equally positively to approaches and contact on both sides. Our findings support those of previous studies investigating a link between emotionality and laterality and confirm the role of the left hemisphere in the processing of novel or negative stimuli. Moreover, the data underline the impact work and training can have on this laterality in horses. © 2011 Elsevier Inc. All rights reserved.
1. Introduction Long believed to be a human specificity, brain lateralization (i.e. asymmetry of brain function and behavior) is now accepted as a widespread characteristic of vertebrates [1,2] and recent evidence suggests it is also present in some invertebrate species (e.g. [3]). Throughout vertebrates, the general pattern of lateralization observed is that the right hemisphere is involved in the expression of intense emotions and controlling rapid responses, whereas the left hemisphere is concerned with responses that require inhibition of responding until a decision is made [4]. Behavioral laterality has been investigated in both intra- and interspecific encounter situations. For instance, a lateralized approach pattern has recently been demonstrated in mangabeys showing that when individuals approach another group member, they position themselves as so to have the approached individual in their right visual field [5]. In humans, a head turning bias towards the right side has been shown in human adult kissing behavior [6]. Most studies investigating interspecific interactions looked at the specific case of predator–prey encounters (e.g. in toads: [7], dunnarts [8]) or agonistic interactions (e.g. in gelada baboons [9]). Thus, these studies have focused on eye preference or lateralized escape responses as the outcome of a negative encounter. In domestic animals, the case of human animal interactions and more specifically the way to approach an unknown animal has not received particular attention. A single study, conducted by Austin and Rogers [10] investigated the asymmetry of flight turning response to a
⁎ Corresponding author. Tel.: + 33 2 99618155. E-mail address: [email protected] (C. Sankey). 0031-9384/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2011.05.009
human approaching with a frightening object (umbrella) in domestic horses. However, it was more the novel and frightening aspect of the object, rather than the human, that was being tested. Other studies have involved novel objects, including in marmosets [11], chicken [12] or even fish [13]. Here, our study aimed to investigate the behavioral responses of young domestic horses to a human approaching them from the left or right side, as well as to use visual laterality to evaluate the possible impact of horses' training experience on the way they perceive this approaching human (positive, neutral or negative). Horses are traditionally approached and handled on the left side. Yet, understanding lateralization in horses has many practical implications in order to understand current training methods, develop new training paradigms but also help for the selection of horses for the various disciplines and work practices [10]. So far, horses have been shown to display both motor [14] and sensory (e.g. auditory [15]) lateralization patterns. When it comes to visual laterality, horses prove to be a particularly interesting model, for they have laterally placed eyes and an almost complete decussation of the optic fibres [16,17], meaning that what is seen in the right monocular visual field is processed by the left hemisphere and what is seen in the left monocular visual field is processed by the right hemisphere. Interestingly, recent research has shown a link between emotionality and visual laterality in horse: adult horses show greater reactivity when approached by a human holding a novel object in their left monocular visual field [10] and horses that have the highest emotionality index tend to fixate a novel object with their left eye [18]. Up until today, the way this lateralization pattern develops remains unclear, but factors such as age and training experience (Larose et al. [18], Farmer et al. [26]) have been suggested to impact on horses’ emotional laterality.
C. Sankey et al. / Physiology & Behavior 104 (2011) 464–468
465
In this study, we investigated 1) whether one year old, naive horses show a lateralization in their response to a human approaching them from the left or from the right and 2) whether the potential lateralized response pattern differed in two years old horses that had undergone initial training at an earlier age (traditionally performed from the left side). 2. Material and methods 2.1. Study subjects This study was conducted at the “station expérimentale de Chamberet” in France with 39 Angloarabian (N = 33) and French saddlebred (N = 6) young horses, living in groups at pasture. A first group was composed of 16 one year old horses (10 females and 6 castrated males). The particularity of the group was that their experience with humans was limited to minimum veterinary care and feed distribution in the winter period. This group was considered as the “naïve” horses group. A second group was composed of 23 two years old horses (15 females and 8 castrated males). In addition to the veterinary care and winter feeding, these horses had received a two months initial training at the age of one year (cf. [19]), during which they had been trained to remain immobile on a vocal command given from their left side and then to accept usual handling procedures (such as being fitted with a halter and a surcingle, giving their feet, etc.). This group was here considered as the “trained” group. Otherwise, both groups were raised in similar conditions during their first year: from birth until weaning at the age of 6 months, they were brought up as a group with their dams in a pasture. Weanlings then spent their first winter in groups of 5 to 6 individuals in a stall where they stayed until the next Spring. Group 2 horses spent their second summer all together in a pasture, and were pushed in a large indoor stall for a few hours every day in order to carry out their initial training (~4 months). They spent their second winter in individual indoor stalls, where they could see and hear each other and also physically interact with their neighbors through the stall bars. In the Spring 2008, both groups were released in 2 different (but equivalent in size) pastures, sufficiently distant from one another so that they could not see or hear each other.
animals were approached was determined by the animals' availability in the pasture but the order in which the zones were approached for each horse was randomized. Overall, the experimenter approached each horse 7 times, once towards every predefined zone.
2.2. Experimental procedure
2.4. Statistical analysis
In both groups, approach tests were carried out in 1 to 2 daily sessions, lasting 1 to 2 h and took place at different times every day, between 8.30 am and 7.30 pm. In the two groups, all approaches were carried out by the same experimenter (CC, woman who always wore the same dark green coat). She was blind to the horses' earlier experience with humans. During a single session, the experimenter never approached the same horse more than twice. In order to assess the young horses' responses to an approaching human, we defined 7 zones: shoulder, flank and croup on both left and right sides and front (Fig. 1). Each approach followed the same pattern: after choosing an immobile but awake (i.e. eyes open) animal, the experimenter placed herself at a distance of 8 m from the horse and started approaching it following an imaginary line, walking at a constant average speed of one step per second. She walked in a neutral position with her arms beside her body. During the whole approach, she looked at the horse, in the direction of the target zone. When she was close enough (distance b0.2 m), she extended her left arm to gently touch the target zone, while her other arm stayed beside her body. An approach ended when she established contact and touched the target zone or at whatever distance if the animal attempted to avoid, escape or threaten her by any means. Lastly, if another horse interrupted the approach by placing itself in the experimenter's trajectory, the approach was canceled and repeated later. The order in which the
Binomial tests allowed us to compare the frequency of successful approaches (i.e. leading to contact) as well as the frequency of approaches eliciting positive or negative reactions to frequencies expected by chance. Fisher's exact test was used to compare rates of positive/negative reactions between groups. The non-parametric Mann–Whitney U-test was also used to compare the two groups. Alpha was set at 5% for each analysis.
Fig. 1. Diagram of the paths taken by the experimenter to approach the pre-defined zones, commencing 8 m away.
2.3. Data collection The data were recorded by the experimenter herself using a digital voice recorder for later transcription. From the beginning of her approach, she recorded the horse's behavior continuously. She also noted whether the approach led to a contact on the target zone and the animal's positive or negative response to the contact. Standing still, looking at the experimenter and sniffing her were considered positive reactions, while avoidance, escape and threats, threats of biting and of kicking were considered negative reactions [20,21]. Thus, no neutral reactions were recorded.
3. Results 3.1. “Naïve” 1-year-old horses Most yearlings accepted to be touched at least once by the experimenter (N = 15/16). The mean number of zones where they accepted contact was 2.57 ± 0.39 out of the 7 predefined zones. Overall, 35.4% of the approaches from the right led to contact vs. 29.2% of the approaches from the left. Clear differences appeared regarding horses' preference or rather their dislike for certain zones. Left and right shoulders, as well as left flank were more difficult to touch than expected by chance: only 4 out of the 16 horses (20%, but not always the same 4 subjects) accepted to be touched on each of these zones (binomial test, P = 0.04; cf. Table 1), while the others withdrew during the approaches. For the
466
C. Sankey et al. / Physiology & Behavior 104 (2011) 464–468
Table 1 Number and percentage of one and two-year-old horses accepting to be touched on the different zones and their positive or negative response to contact and statistics (binomial tests). 1 year-old (« naïve »)
2 year-old (« trained »)
Approached zone
Success rate
P
Positive reactions
Negative reactions
P
Success rate
P
Positive reactions
Negative reactions
P
Left shoulder Left flank Left croup Front Right shoulder Right flank Right croup
4/16 4/16 6/16 10/16 4/16 8/16 5/16
0.04 0.04 0.2 0.2 0.04 0.6 0.1
0 2 1 6 3 3 3
4 2 5 4 1 5 2
NA NA 0.1 0.4 NA 0.4 0.5
18/23 (78%) 12/23 (52%) 10/23 (43%) 19/23(83%) 18/23 (78%) 14/23 (61%) 18/23 (78%)
0.005 0.5 0.3 0.001 0.005 0.2 0.005
18 10 8 17 18 11 12
0 2 2 2 0 3 6
b0.001 0.02 0.05 b0.001 b0.001 0.03 0.1
(25%) (25%) (38%) (63%) (25%) (50%) (31%)
other predefined zones, the proportion of approaches leading to contact did not significantly differ from chance level (P N 0.05). Concerning a potential lateralization bias in the horses' positive or negative responses to contact by zone (see Table 1 for details), it is interesting to note that amongst the yearlings that let the experimenter approach and touch their shoulders (most commonly approached zone in order to fit horses with their equipment), all of them (4/4) displayed negative reactions (i.e. threats or escape) at contact on the left side, contrary to the right side where most of them (3/4) displayed positive reactions (i.e. immobility or sniffing the experimenter). Though striking, this difference was not statistically tested due to the low number of animals that were touched. No such tendencies were found for the other contact zone (flank, croup). 3.2. Trained horses Here again, most horses accepted to be touched at least once by the experimenter in the pasture (N = 22/23), and the mean number of zones where they accepted contact was 4.74 ± 0.42 out of the 7 predefined zones. Overall, 72.5% of the approaches from the right led to contact vs. 57.9% of the approaches from the left. Clear differences appeared, this time regarding horses' preference for certain zones: left and right shoulders, as well as the front, appeared as privileged contact zones, for the experimenter was able to touch them without the horses fleeing or threatening during the approach (i.e. before contact) (for both shoulders: N = 18/23, binomial tests, P = 0.005; for the front: N = 19/23, binomial test, P = 0.001; cf. Table 1). Most horses also let the experimenter approach their right croup (N = 18/23, binomial test, P = 0.005). For the other predefined zones, the proportion of approaches leading to contact did not significantly differ from chance level (P N 0.05). Moreover, most horses displayed positive rather than negative reactions at contact, whatever the zone touched (binomial tests, P ≤ 0.05), exception made for the right croup for which this difference was not statistically significant (cf. Table 1). For instance, horses that let the experimenter touch their shoulder all displayed positive behaviors (i.e. remaining immobile or turning their head to sniff the experimenter) to the contact, whatever the side (N = 18/18).
Besides, it is noteworthy that whereas the 2 groups' horses behavior did not differ significantly in response to a contact on the right shoulder (number of horses displaying positive behavior: N1 year = 3/4, N2 years = 18/18, Fisher's exact test, P = 0.2; Fig. 2) and croup (N1 year = 3/5, N2 years = 12/18, Fisher's exact test, P = 0.4), they clearly differed in their behavioral response when these zones were touched on the left side (Number of horses displaying positive behavior: shoulder: N1 year = 0/4, N2 years = 18/18, Fisher's exact test, P b 0.001; Fig. 2; croup: N1 year = 1/6, N2 years = 8/10, Fisher's exact test, P = 0.002). 4. Discussion Overall, the one year old “naïve” horses showed a clear asymmetry in their response to an approaching human. They displayed more negative reactions when approached from the left side: two out of the three zones on the left side were amongst the most difficult ones to approach. Moreover, when they did let the experimenter touch their left shoulder, most horses escaped or threatened her. On the contrary, most horses displayed positive behaviors when touched on the right shoulder. However, it seems that the positive training received by the two years old horses alleviated this asymmetry, as these horses reacted equally positively to approaches and contact on both sides. In our study, one year old naïve horses appeared more reluctant to accept contact when approached by the human in their left monocular visual field and conversely better accepted the human approach in their right monocular visual field. This result support previous studies conducted in adult horses, that showed that the left monocular visual field (information processed by the right cerebral hemisphere) was associated with a higher reactivity [10,18] and fits in the theory of valence (right hemisphere mainly processing negative emotions and left hemisphere mostly processing neutral or positive emotions; [22,23]). However, the negative reactions observed in the naïve horses when they were approached on their left side were not displayed by the two years old trained horses. In fact, they did not display asymmetrical behavioral responses and accepted approach and contact equally well on both sides. Age may be a factor as Søndergaard
3.3. Effect of training or age: comparison of the 2 groups As previously mentioned, most yearlings and 2-year-olds accepted to be touched at least once by the experimenter. However, the tolerance of contact was higher in older horses that accepted to be touched on a larger number of predefined zones than yearlings (mean number of zones touched: X1 year = 2.57 ± 0.39; X2 years = 4.74 ± 0.42 out of 7, Mann–Whitney U-test, U = 74.5, P = 0.001). A greater proportion of 2-year-olds accepted contact on both shoulders (Fisher's exact test, N1 year = 4/16, N2 years = 18/23, P = 0.001), as well as on the right croup (Fisher's exact test, N1 year = 5/16, N2 years = 18/23, P = 0.004). There were no significant differences in the tolerance of contact between age groups for the other zones.
Fig. 2. Percentage of horses reacting either positively or negatively to the human touching their left/right shoulder.
C. Sankey et al. / Physiology & Behavior 104 (2011) 464–468
and Halekoh [24] suggest that the chance of a horse approaching a human and the chance of approaching a horse increased with age. Thus, horses' increasing acceptance of an approaching human with age could be attributed to a simple maturation effect, resulting from the normal physiological development horses undergo with age. Nevertheless, this same study revealed that handled horses approached humans more rapidly than unhandled ones [24], showing that older horses are also more familiar, by an effect of habituation to humans due to the daily feeding by humans [24]. In fact, the only direct evidence of age dependent shifts in bias during development is found in humans, chicks and rats [1]. In horses, McGreevy and Rogers reported a shift in motor laterality (foreleg preference) in horses over two years of age, compared to horses aged two years or less [14]. In addition, Larose et al. [18] found that 3 years old Saddlebred horses had a stronger visual lateralization than 2 years old ones. However, studies in other species have reported an effect of age over a much greater span of years than the one year difference observed in Larose et al.'study [18] or ours, in which all horses tested can be classified as young horses. As previously suggested, the training paradigms applied by humans may greatly influence the expression of lateralization in domestic horses [18]. The fact that this study's two years old horses had undergone initial training at the age of one year is probably a very relevant event. The absence of lateralized responses to the human approach could be inferred to the repeated interactions with the trainer, for handling was mostly performed on the left side of the horse (cf. [19]). Other studies previously suggested an effect of work on horses' motor [14] and visual [18] laterality. The question that arises here is one about the type of work that is performed and the emotional memory horses keep about it, for evidence suggests that different training methods can greatly impact the way horses perceive working sessions and more generally the human-horse relationship [25]. In the present study, the initial training of the two years old horses included repeated handling sessions using, or not, positive reinforcement. Such positive reinforcement based training has been shown to have long lasting positive effects on the human–horse relationship [19,25], which could explain the decrease of negative responses on the left side. In most studies, horses’ left eye is repeatedly associated with fear inducing situations; while the right one is associated with more positive events (Larose et al. [18], De Boyer Des Roches et al. [29]). In addition, horses spontaneously display less reactivity to a frightening object on the right side than on the left one (Austin and Rogers [10]). In our study, we observed less emotional reactions on the more “reactive” side (i.e. left) in the horses that had undergone training. In a recent study, Farmer et al. [26] found, on the contrary, that training in an interactive situation induced in horses a strong preference for looking at the trainer with the left eye. The authors argue that the trainers involved were well known to the horses and cared for them and fed them, as well as working with them, so there is no reason to suppose that there would be any negative emotion associated with them. However, in the light of the literature investigating a link between emotionality and laterality, one can question the way horses perceived that particular training situation, for it involved chasing the horse away before turning your back and waiting for it to return (“join up” technique and “hook on” method). Such techniques could indeed be a source of stress and negative emotions associated with the trainer, for a previous study involving the agitation of a stick in front of ponies' heads to make them back up showed that this type of negative reinforcement-based training (i.e. using an aversive stimulus) induced a rise in the ponies' heart rates and a negative perception of training [25]. The fact that in Farmer's study the trainer also fed and cared for the horses may not have been sufficient to compensate the possible negative memory acquired at work, as negative events seem to be stronger in memory than positive ones [27]. Evidence suggests that eye preference to fixate an object may give insight into how an object is perceived [28]. A Study by De Boyer Des
467
Roches [29] revealed that horses use more their left eye to look at an object with a negative emotional value (veterinary's white shirt) than to look at a neutral (plastic cone) or positive (feed bucket) one. Thus, we hypothesize that the type of work and how it is perceived by horses, rather than work itself, impacts differently on horses' perceptual laterality. Knowing that horses perceive the world differently on each side has practical applications. Young or highly reactive horses would certainly learn faster and be more relaxed if first approached on the right side. Beginning their training by handling them on their most reactive side (i.e. left) may in some cases exacerbate their emotional reactivity. Besides, knowing that interocular transfer occurs in horses [30], at least from the right eye to the left one (i.e. from left to right hemisphere; [10]), they could progressively learn to accept approach and handling on the left side. Once a positive relationship is established, this study suggests that the laterality bias may fade to allow horses to accept human contact equally on both sides. Acknowledgements The authors are grateful to the Director and staff of the “Station expérimentale des Haras”, Chamberet. We also wish to thank the COST of the “Haras Nationaux” and the “Region Bretagne” for their financial support. Thanks to Dr Nadav Shashar, Dr Catherine BloisHeulin, Audrey Maille and three anonymous referees for their useful comments on the manuscript. This study complies with the French laws concerning the use of animals in research. References [1] Rogers LJ, Andrew RJ. Comparative Vertebrate Lateralization. New York: Cambridge University Press; 2002. [2] Vallortigara G, Rogers LJ. Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 2005;28:575–89. [3] Rogers LJ, Vallortigara G. Lateral shift of olfactory memory recall by honeybees. PLoS One 2008;3(6):e2340. [4] Rogers LJ. Lateralisation in vertebrates: its early evolution, general pattern, and development. Adv Stud Behav 2002;31:108–61. [5] Baraud I, Buytet B, Bec P, Blois-Heulin C. Social laterality and “transversality” in two species of mangabeys: influence of rank and implication for hemispheric specialization. Behav Brain Res 2009;198:449–58. [6] Güntürkün O. Adult persistence of head turning asymmetry. Nature 2003;421:711. [7] Lippolis G, Bisazza A, Rogers LJ, Vallortigara G. Lateralization of predator avoidance responses in three species of toads. Laterality 2002;7:163–83. [8] Lippolis G, Westman W, McAllan BM, Rogers LJ. Lateralization of escape responses in the striped-faced dunnart, Sminthopsis macroura (Dasyuridae: Marsupalia). Laterality 2005;10:457–70. [9] Casperd JM, Dunbar RIM. Asymmetries in the visual processing of emotional cues during agonistic interactions by gelada baboons. Behav Process 1996;37:57–65. [10] Austin NP, Rogers LJ. Asymmetry of flight and escape turning responses in horses. Laterality 2007;12:464–74. [11] Hook-Costigan MA, Rogers LJ. Lateralized use of the mouth in production of vocalizations by marmosets. Neuropsychologia 1998;36:1265–73. [12] Vallortigara G, Regolin L, Pagni P. Detour behavior, imprinting and visual lateralization in the domestic chick. Cogn Brain Res 1999;7:307–20. [13] Facchin L, Bisazza A, Vallortigara G. What causes lateralisation of detour behavior in fish? Evidence for asymmetries in eye use. Behav Brain Res 1999;103:229–34. [14] McGreevy PD, Rogers LJ. Motor and sensory laterality in thoroughbred horses. Appl Anim Behav Sci 2005;92:337–52. [15] Basile M, Boivin S, Boutin A, Blois-Heulin C, Hausberger M. Socially dependent auditory laterality in domestic horses (Equus caballus). Anim Cogn 2009;12:611–9. [16] Brooks DE, Komaromy AM, Kallberg ME. Comparative retinal ganglion and optic nerve morphology. Vet Ophthalmol 1999;2:1463–5224. [17] Harman AM, Moore S, Hoskins R, Keller P. Horse vision and an explanation for the visual behavior originally explained by the “ramp retina”. Equine Vet J 1999;31: 384–90. [18] Larose C, Richard-Yris M-A, Hausberger M, Rogers L. Laterality of horses associated with emotionality in novel situations. Laterality 2006;11:335–67. [19] Sankey C, Richard-Yris M-A, Leroy H, Henry S, Hausberger M. Training experience induces lasting memories of humans in horses, Equus caballus. Anim Behav 2010;79:869–75. [20] McDonnell S, Haviland J. Agonistic ethogram of the equid bachelor band. Appl Anim Behav Sci 1995;43:147–88. [21] McDonnell S, Poulin A. Equid play ethogram. Appl Anim Behav Sci 2002;78: 263–90. [22] Davidson RJ. Anterior asymmetry and the nature of emotion. Brain Cogn 1992;20: 125–51.
468
C. Sankey et al. / Physiology & Behavior 104 (2011) 464–468
[23] Demaree HA, Everhart DE, Youngstrom EA, Harrison DW. Brain lateralization of emotional processing: historical roots and a future incorporating “dominance”. Behav Cogn Neurosci Rev 2005;4:3–20. [24] Søndergaard E, Halekoh U. Young horses’ reactions to humans in relation to handling and social environment. App Anim Behav Sci 2003;84:265–80. [25] Sankey C, Richard-Yris M-A, Henry S, Fureix C, Nassur F, Hausberger M. Reinforcement as a mediator of the perception of humans by horses (Equus caballus). Anim Cogn 2010;13:753–64. [26] Farmer K, Krueger K, Byrne RW. Visual laterality in the domestic horse (Equus caballus) interacting with humans. Anim Cogn 2010;13:229–38.
[27] Fureix C, Jego P, Sankey C, Hausberger M. How horses (Equus caballus) see the world: humans as significant “objects”. Anim Cogn 2009;12:643–54. [28] McKenzie R, Andrew RJ, Jones RB. Lateralisation in chicks and hens: new evidence for control of response by the right eye system. Neuropsychologia 1998;36:51–8. [29] De Boyer Des Roches A, Richard-Yris M-A, Henry S, Hausberger M. Laterality and emotions: visual laterality in the domestic horse (Equus caballus) differs with objects' emotional value. Physiol Behav 2008;94:487–90. [30] Hanggi EB. Interocular transfer in horses (Equus caballus). J Equine Vet Sci 1999;19 (8):518–24.