Anim Cogn (2014) 17:1007–1011 DOI 10.1007/s10071-013-0717-9
SHORT COMMUNICATION
Horses (Equus caballus) discriminate body odour cues from conspecifics F. Pe´ron • R. Ward • O. Burman
Received: 25 June 2013 / Revised: 25 November 2013 / Accepted: 26 November 2013 / Published online: 5 December 2013 Ó Springer-Verlag Berlin Heidelberg 2013
Abstract Knowledge about social recognition and memory in animals can help us to determine appropriate management and husbandry techniques. In this study, we used a habituation–discrimination procedure to investigate the ability of horses (Equus caballus) to distinguish between the body odour samples of unfamiliar conspecifics. To pick up body odour, we rubbed material on the coat of horses and presented these unknown body odours to 16 different conspecifics of the same sex and similar age. The test consisted of two successive two-min presentations of a sample from one individual (e.g. individual ‘A’) and a simultaneous presentation of samples from individual ‘A’ and a novel individual (e.g. individual ‘B’) during a final third presentation. The results showed that horses, regardless of sex, decreased the time they spent investigating conspecific body odour across the initial two presentations—demonstrating habituation. In the final presentation, the results demonstrated successful discrimination of the previously experienced odour because horses investigated the novel olfactory sample (‘B’) significantly more than the pre-exposed sample (‘A’). Taken together, these findings suggest, for the first time, that horses are able to discriminate two stimuli derived from body odours of unfamiliar conspecifics over short period of time. Keywords Body odour Discrimination Equus caballus Habituation Social memory
F. Pe´ron R. Ward O. Burman (&) School of Life Sciences, Riseholme Campus, University of Lincoln, Lincoln LN2 2LG, UK e-mail: [email protected]
Introduction Individuals living within a social group should be able to discriminate between-group and non-group mates, kin from non-kin, and know about individual characteristics (sex, age, social status, etc.) in order to modify their behaviour appropriately (Heitor and Vicente 2007). Horse behaviour can change depending upon whether a conspecific is known or unknown, raising the likely conclusion that they are able to distinguish between familiar group members and strangers (Kiley-Worthington 1987, pp 46–54; Rubenstein and Hack 1992) as has been demonstrated in other species (see a review in mammals, Brennan and Kendrick 2006). Social memory processes can be based on several different sensory modalities, combined or not. Horses are capable of indirect inference of dominance relationships through observation (Krueger and Heinze 2008) and recognition ability on the basis of auditory cues has been shown (Lemasson et al. 2009), revealing that whinny calls appear to carry social information about the caller’s sex, body size, and identity, therefore also implying the use of social memory. Auditory recognition in conjunction with visual cues has been used to demonstrate cross-modal individual recognition in horses (Proops et al. 2008), and the olfactory abilities of equines have also been investigated. For example, Krueger and Flauger (2011) suggested that horses of both sex could distinguish individual competitors from the smell of their faeces. Hothersall et al. (2010) not only investigated faeces, but also tested urine and body odour in pregnant mares. Their results showed that horses demonstrated habituation across repeated presentations of all sample types, suggesting that they remembered the smell from the previous time it was presented to them. However, they found that the horses
123
1008
were apparently unable to discriminate between familiar and unfamiliar body odour when presented simultaneously after a short retention interval. In their study, Hothersall et al. (2010) observed that pregnant mares responded to a donor’s body odour (stimuli of a variety of ages and sexes) in a variety of ways, ranging from no response to a persistent sniffing. This lack of certainty about whether the samples contained olfactory information that permitted social discrimination (i.e. discrimination based on socially derived cues) meant that further investigation was necessary. The aim of this study was therefore to determine whether or not horses (of both sexes) were able to discriminate between conspecifics on the basis of body odour. We tested male and (non-pregnant) female horses with odours from donors of the same sex (as the subject) and of a similar age.
Materials and methods Subjects The study was conducted during November and December 2011 with six mares (7–17 years old; mean 12.6 years) and ten geldings (9–16 years old; mean 13.3 years) of mixed ‘‘sport horse’’ breeds housed in the same barn, in separate stables (4 m length 9 4 m width) containing either wood pellets or straw bedding. Their typical husbandry regime included a maximum of 3 h of exercise per day, a constant supply of water, and a diet consisting mainly of sugar beet, fibre nuts, silage, and hay. Testing sessions took place between 12 noon and 2 pm when there was minimal activity on the yard. Odour sample collection Horses used as ‘odour’ donors were matched to the test subjects for sex and age as far as possible. Subjects were presented with samples from donors of the same sex as themselves and there was an average difference of 1 year (males) and 3 years (females) between the ages of the subject and the donor. None of the odour donors were from the same yard as the subjects to ensure that the cue was completely novel to the horses being tested. Following the collection method used by Hothersall et al. (2010), a fleece fabric was rubbed along the horse’s neck, between the forelegs, and down their face from the eye (over glands and where the horse sweats) for approximately 30 s (5 s for each section on either side) in an attempt to collect a generalised body odour sample. This method was conducted by the owners themselves following clear instruction (precise order of collection). Following collection (between 8 and 9 am on the day of testing), each odour sample was put straight into an airtight sealed bag that was
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Anim Cogn (2014) 17:1007–1011
only opened again immediately prior to testing. Each bag was marked for identification, transferred to the test stable, and used in a test between 12 am and 2 pm. Rubber gloves were worn at all times when collecting and presenting samples and were changed between samples. Habituation–discrimination procedure Each piece of fabric containing a body odour was cut into four equal sections, so that three could be used as the familiar sample with one horse (i.e. three separate presentations) and one could be used as the novel sample for another (i.e. one presentation). Samples were placed over the end of an odour presentation apparatus (6.4 cm in diameter, 18.5 cm in length, and with a handle 11.5 cm long) and attached securely with an elastic band meaning that subjects were able to make physical contact with the sample but without being able to remove or destroy it (see Fig. 1). Each one was presented using a 3-step habituation– discrimination procedure like that of Hothersall et al. (2010), in which three consecutive exposures of body odour from the same individual (e.g. individual ‘A’) were presented to each subject horse but with a novel sample (e.g. individual ‘B’) being simultaneously presented on the final (third) exposure. Each sample was presented centrally to the horse over the stable door for a 2-min period separated by a 15-min inter-exposure interval. However, in the final (discrimination) presentation, body odour from the previously experienced and a novel individual was simultaneously presented 50 cm apart (see Fig. 1). The location (left/right) of these stimuli was balanced among subjects. A fresh body odour sample (i.e. a new section of fabric) was given on each exposure in order to avoid the horses using odour deposition as a cue, and the odour presentation apparatus was cleaned before each presentation. At the beginning of each exposure, a ‘start’ signal was given to get the attention of the subject. The 2-min period began once the horse approached and first investigated the sample. A subject was considered to be investigating when its nose was within 10 cm of the fabric and the horse could be seen to be sniffing, flaring its nostrils, showing a flehmen response, or attempting to make contact with the sample. One experimenter was in charge of positioning the horse at the starting point and another one was holding the odour samples and giving the start signal saying the horse name. Both were blind to the conditions. Behaviour was recorded live by a third person who was aware of the conditions. Ethical note The protocol was approved by the Faculty Research Ethics Committee of the University of Lincoln and complied with the relevant UK legislation.
Anim Cogn (2014) 17:1007–1011
1009
Fig. 1 Sample(s) presented either in the middle (exposure 1 and 2) or on the side (exposure 3) of the stable door. Horse exploring the sample (fleece fabric presented on a stick)
Data collection and Statistical analyses The total amount of time (seconds) spent investigating each of the samples was recorded to examine the habituation and discrimination of the horse’s investigative responses. The results were used to determine (1) whether the subjects showed a significant habituation to the presentation of the same sample in the first two presentations, (2) if the subjects investigated the novel sample more than the previously experienced sample in the final, third, presentation, and if this varied between sexes. Based on the results of a normality test (Kolmogorov– Smirnov), we used either t tests or Mann–Whitney tests in order to assess any difference between male and female responses during each presentation, and then a Wilcoxon signed ranks test to compare investigation times between the first and second presentations. Finally, we used a Wilcoxon signed ranks test to compare between the investigation times of previously experienced and new odour stimuli during the final presentation (SPSS Statistics 19 software).
Results We did not find any statistically significant difference between the males and the females regarding the time that
they spent exploring each stimulus (first exposure: t(14) = -0.34, P = 0.74; second exposure: U = 29, Z = -0.11, n1 = 6, n2 = 10, P = 0.96; previously experienced odour: U = 19, Z = -1.25, n1 = 6, n2 = 10, P = 0.26; new odour: U = 19, Z = -1.21, n1 = 6, n2 = 10, P = 0.26). When comparing investigation time between the initial two ‘habituation’ presentations, we found a statistically significant difference (T = 14, Z = -2.8, N = 16, P = 0.005), with higher levels of investigation of the body odour in presentation 1 (range 3–44 s; mean 16.25 s) compared to presentation 2 (0–41 s; mean 8.25 s). For the third (discrimination) presentation, we found a statistically significant difference (T = 3, Z = -3.25, N = 15, P = 0.001), with higher levels of investigation of the new stimuli (0–10 s; mean 2.56 s) compared to the previously experienced stimuli (0–44 s; mean 7.81 s) (see Fig. 2).
Discussion We observed that horses habituated to a body odour sample obtained from a previously unfamiliar conspecific when it was presented on two separate occasions and when the same sample was presented for a third presentation at the same time as a novel sample, spent more time investigating the novel sample. These results suggest that horses (of both
123
1010
Anim Cogn (2014) 17:1007–1011
Fig. 2 Mean time spent sniffing the stimulus (± SE) in the initial two presentations of the same odour cue and in the final ‘discrimination’ test
sexes) were able to discriminate between two stimuli derived from the body odour of unfamiliar conspecifics, confirming the findings of Hothersall et al. (2010) that horses were able to remember body odours of individuals over a 15-min retention interval, but extending their findings to include successful discrimination. Our results suggest that we can now add body odour to the other sensory sources that horses can use to discriminate between conspecifics: visual and acoustic cues (Feh 2005; Proops et al. 2008; Lemasson et al. 2009), urine/vaginal secretions (Marinier et al. 1988; Hothersall et al. 2010), and faeces (Stahlbaum and Houpt 1989; Krueger and Flauger 2011). Compared to the results of Hothersall et al. (2010), we observed less variation in the investigatory responses of the horses. This is likely to have been due to our larger sample size as well as our matching of odour samples to test subjects in terms of sex and age. A better understanding of social memory and recognition processes may help us to refine husbandry/management techniques and consequently improve animal welfare (Mendl et al. 2001; Burman and Mendl 2003). Given that increased social contact between horses is likely to be beneficial in relation to animal welfare (see, for example, Christensen et al. 2002), there is a need to identify suitable and safe ways to integrate horses together (see Hartmann et al. 2012) and the use of olfactory cues could be one way to achieve this. Although our study demonstrates habituation and discrimination in horses on the basis of socially derived body odour cues, the stimuli were only presented for brief 2-min periods. Experimental data (Murphy and Arkins 2007; Proops et al. 2008; Hanggi and Ingersoll 2009) suggest that
123
horses are able to discriminate and recognise other horses over long periods of time. Future research is therefore required to investigate how the retention interval and the quality of the sample influence the process (e.g. Burman and Mendl 2006) and whether the familiarity of odour cues influences resilience of social memory, as studies in other species have revealed that the elements of common husbandry procedures, e.g. handling, can disrupt social recognition (Burman and Mendl 2000, 2004). The results of this study indicate that horses have a social memory that can be based on body odours (lasting for at least for 15 min), and this may well be a step towards developing an understanding of the cognitive processes that inform the practical issue of how, and when, to introduce horses into social groups. Acknowledgments We would like to thank the horse owners, Robin Snelson, and the equine yard staff at the Riseholme Park campus. We would also like to thank two anonymous reviewers and the editor for their constructive comments.
References Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Trans R Soc B 361:2061–2078 Burman O, Mendl M (2000) Short-term social memory in the laboratory rat: its susceptibility to disturbance. Appl Anim Behav Sci 67:241–254 Burman O, Mendl M (2003) The influence of pre-experimental experience on social discrimination in rats (Rattus norvegicus). J Comp Psychol 117:344–345
Anim Cogn (2014) 17:1007–1011 Burman O, Mendl M (2004) Disruptive effects of standard husbandry practice on laboratory rat social discrimination. Anim Welf 13:125–135 Burman O, Mendl M (2006) Long-term social memory in the laboratory rat (Rattus norvegicus). Anim Welf 15:379–382 Christensen J, Ladewig J, Sondergaard E, Malmkvist J (2002) Effects of individual versus group stabling on social behaviour in domestic stallions. Appl Anim Behav Sci 75:233–248 Feh C (2005) Relationships and communication in socially natural horse herds. In: Mills DS, McDonnell SM (eds) The domestic horse: the origins, development, and management of its behaviour. Cambridge University Press, Cambridge Hanggi E, Ingersoll J (2009) Long-term memory for categories and concepts in horses (Equus caballus). Anim Cogn 12:451–462 Hartmann E, Sondergaard E, Keeling L (2012) Keeping horses in groups: a review. Appl Anim Behav Sci 136:77–87 Heitor F, Vicente L (2007) Learning about horses: what is equine learning all about? Behav Process 76:34–36 Hothersall B, Harris P, So¨rtoft L, Nicol C (2010) Discrimination between conspecific odour samples in the horse (Equus caballus). Appl Anim Behav Sci 126:37–44 Kiley-Worthington M (1987) The behaviour of horses. J.A. Allen, London Krueger K, Flauger B (2011) Olfactory recognition of individual competitors by means of faeces in horse (Equus caballus). Anim Cogn 14:245–257
1011 Krueger K, Heinze J (2008) Horse sense: social status of horses (Equus caballus) affects their likelihood of copying other horses’ behaviour. Anim Cogn 11:431–439 Lemasson A, Boutin A, Boivin S, Blois-Heulin C, Hausberger M (2009) Horse (Equus caballus) whinnies: a source of social information. Anim Cogn 12:693–704 Marinier S, Alexander A, Waring G (1988) Flehmen behaviour in the domestic horse: discrimination of conspecific odours. Appl Anim Behav Sci 19:227–237 Mendl M, Burman O, Laughlin K, Paul E (2001) Animal memory and animal welfare. Anim Welf 10:141–159 Murphy J, Arkins S (2007) Equine learning behaviour. Behav Process 76:1–13 Proops L, McComb K, Reby D (2008) Cross-modal individual recognition in domestic horses (Equus caballus). PNAS 106:947–951 Rubenstein DI, Hack MA (1992) Horse signals: the sounds and scents of fury. Evol Ecol 6:254–260 Stahlbaum CC, Houpt KA (1989) The role of the Flehmen response in the behavioral repertoire of the stallion. Physiol Behav 45:1207–1214
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SHORT COMMUNICATION
Horses (Equus caballus) discriminate body odour cues from conspecifics F. Pe´ron • R. Ward • O. Burman
Received: 25 June 2013 / Revised: 25 November 2013 / Accepted: 26 November 2013 / Published online: 5 December 2013 Ó Springer-Verlag Berlin Heidelberg 2013
Abstract Knowledge about social recognition and memory in animals can help us to determine appropriate management and husbandry techniques. In this study, we used a habituation–discrimination procedure to investigate the ability of horses (Equus caballus) to distinguish between the body odour samples of unfamiliar conspecifics. To pick up body odour, we rubbed material on the coat of horses and presented these unknown body odours to 16 different conspecifics of the same sex and similar age. The test consisted of two successive two-min presentations of a sample from one individual (e.g. individual ‘A’) and a simultaneous presentation of samples from individual ‘A’ and a novel individual (e.g. individual ‘B’) during a final third presentation. The results showed that horses, regardless of sex, decreased the time they spent investigating conspecific body odour across the initial two presentations—demonstrating habituation. In the final presentation, the results demonstrated successful discrimination of the previously experienced odour because horses investigated the novel olfactory sample (‘B’) significantly more than the pre-exposed sample (‘A’). Taken together, these findings suggest, for the first time, that horses are able to discriminate two stimuli derived from body odours of unfamiliar conspecifics over short period of time. Keywords Body odour Discrimination Equus caballus Habituation Social memory
F. Pe´ron R. Ward O. Burman (&) School of Life Sciences, Riseholme Campus, University of Lincoln, Lincoln LN2 2LG, UK e-mail: [email protected]
Introduction Individuals living within a social group should be able to discriminate between-group and non-group mates, kin from non-kin, and know about individual characteristics (sex, age, social status, etc.) in order to modify their behaviour appropriately (Heitor and Vicente 2007). Horse behaviour can change depending upon whether a conspecific is known or unknown, raising the likely conclusion that they are able to distinguish between familiar group members and strangers (Kiley-Worthington 1987, pp 46–54; Rubenstein and Hack 1992) as has been demonstrated in other species (see a review in mammals, Brennan and Kendrick 2006). Social memory processes can be based on several different sensory modalities, combined or not. Horses are capable of indirect inference of dominance relationships through observation (Krueger and Heinze 2008) and recognition ability on the basis of auditory cues has been shown (Lemasson et al. 2009), revealing that whinny calls appear to carry social information about the caller’s sex, body size, and identity, therefore also implying the use of social memory. Auditory recognition in conjunction with visual cues has been used to demonstrate cross-modal individual recognition in horses (Proops et al. 2008), and the olfactory abilities of equines have also been investigated. For example, Krueger and Flauger (2011) suggested that horses of both sex could distinguish individual competitors from the smell of their faeces. Hothersall et al. (2010) not only investigated faeces, but also tested urine and body odour in pregnant mares. Their results showed that horses demonstrated habituation across repeated presentations of all sample types, suggesting that they remembered the smell from the previous time it was presented to them. However, they found that the horses
123
1008
were apparently unable to discriminate between familiar and unfamiliar body odour when presented simultaneously after a short retention interval. In their study, Hothersall et al. (2010) observed that pregnant mares responded to a donor’s body odour (stimuli of a variety of ages and sexes) in a variety of ways, ranging from no response to a persistent sniffing. This lack of certainty about whether the samples contained olfactory information that permitted social discrimination (i.e. discrimination based on socially derived cues) meant that further investigation was necessary. The aim of this study was therefore to determine whether or not horses (of both sexes) were able to discriminate between conspecifics on the basis of body odour. We tested male and (non-pregnant) female horses with odours from donors of the same sex (as the subject) and of a similar age.
Materials and methods Subjects The study was conducted during November and December 2011 with six mares (7–17 years old; mean 12.6 years) and ten geldings (9–16 years old; mean 13.3 years) of mixed ‘‘sport horse’’ breeds housed in the same barn, in separate stables (4 m length 9 4 m width) containing either wood pellets or straw bedding. Their typical husbandry regime included a maximum of 3 h of exercise per day, a constant supply of water, and a diet consisting mainly of sugar beet, fibre nuts, silage, and hay. Testing sessions took place between 12 noon and 2 pm when there was minimal activity on the yard. Odour sample collection Horses used as ‘odour’ donors were matched to the test subjects for sex and age as far as possible. Subjects were presented with samples from donors of the same sex as themselves and there was an average difference of 1 year (males) and 3 years (females) between the ages of the subject and the donor. None of the odour donors were from the same yard as the subjects to ensure that the cue was completely novel to the horses being tested. Following the collection method used by Hothersall et al. (2010), a fleece fabric was rubbed along the horse’s neck, between the forelegs, and down their face from the eye (over glands and where the horse sweats) for approximately 30 s (5 s for each section on either side) in an attempt to collect a generalised body odour sample. This method was conducted by the owners themselves following clear instruction (precise order of collection). Following collection (between 8 and 9 am on the day of testing), each odour sample was put straight into an airtight sealed bag that was
123
Anim Cogn (2014) 17:1007–1011
only opened again immediately prior to testing. Each bag was marked for identification, transferred to the test stable, and used in a test between 12 am and 2 pm. Rubber gloves were worn at all times when collecting and presenting samples and were changed between samples. Habituation–discrimination procedure Each piece of fabric containing a body odour was cut into four equal sections, so that three could be used as the familiar sample with one horse (i.e. three separate presentations) and one could be used as the novel sample for another (i.e. one presentation). Samples were placed over the end of an odour presentation apparatus (6.4 cm in diameter, 18.5 cm in length, and with a handle 11.5 cm long) and attached securely with an elastic band meaning that subjects were able to make physical contact with the sample but without being able to remove or destroy it (see Fig. 1). Each one was presented using a 3-step habituation– discrimination procedure like that of Hothersall et al. (2010), in which three consecutive exposures of body odour from the same individual (e.g. individual ‘A’) were presented to each subject horse but with a novel sample (e.g. individual ‘B’) being simultaneously presented on the final (third) exposure. Each sample was presented centrally to the horse over the stable door for a 2-min period separated by a 15-min inter-exposure interval. However, in the final (discrimination) presentation, body odour from the previously experienced and a novel individual was simultaneously presented 50 cm apart (see Fig. 1). The location (left/right) of these stimuli was balanced among subjects. A fresh body odour sample (i.e. a new section of fabric) was given on each exposure in order to avoid the horses using odour deposition as a cue, and the odour presentation apparatus was cleaned before each presentation. At the beginning of each exposure, a ‘start’ signal was given to get the attention of the subject. The 2-min period began once the horse approached and first investigated the sample. A subject was considered to be investigating when its nose was within 10 cm of the fabric and the horse could be seen to be sniffing, flaring its nostrils, showing a flehmen response, or attempting to make contact with the sample. One experimenter was in charge of positioning the horse at the starting point and another one was holding the odour samples and giving the start signal saying the horse name. Both were blind to the conditions. Behaviour was recorded live by a third person who was aware of the conditions. Ethical note The protocol was approved by the Faculty Research Ethics Committee of the University of Lincoln and complied with the relevant UK legislation.
Anim Cogn (2014) 17:1007–1011
1009
Fig. 1 Sample(s) presented either in the middle (exposure 1 and 2) or on the side (exposure 3) of the stable door. Horse exploring the sample (fleece fabric presented on a stick)
Data collection and Statistical analyses The total amount of time (seconds) spent investigating each of the samples was recorded to examine the habituation and discrimination of the horse’s investigative responses. The results were used to determine (1) whether the subjects showed a significant habituation to the presentation of the same sample in the first two presentations, (2) if the subjects investigated the novel sample more than the previously experienced sample in the final, third, presentation, and if this varied between sexes. Based on the results of a normality test (Kolmogorov– Smirnov), we used either t tests or Mann–Whitney tests in order to assess any difference between male and female responses during each presentation, and then a Wilcoxon signed ranks test to compare investigation times between the first and second presentations. Finally, we used a Wilcoxon signed ranks test to compare between the investigation times of previously experienced and new odour stimuli during the final presentation (SPSS Statistics 19 software).
Results We did not find any statistically significant difference between the males and the females regarding the time that
they spent exploring each stimulus (first exposure: t(14) = -0.34, P = 0.74; second exposure: U = 29, Z = -0.11, n1 = 6, n2 = 10, P = 0.96; previously experienced odour: U = 19, Z = -1.25, n1 = 6, n2 = 10, P = 0.26; new odour: U = 19, Z = -1.21, n1 = 6, n2 = 10, P = 0.26). When comparing investigation time between the initial two ‘habituation’ presentations, we found a statistically significant difference (T = 14, Z = -2.8, N = 16, P = 0.005), with higher levels of investigation of the body odour in presentation 1 (range 3–44 s; mean 16.25 s) compared to presentation 2 (0–41 s; mean 8.25 s). For the third (discrimination) presentation, we found a statistically significant difference (T = 3, Z = -3.25, N = 15, P = 0.001), with higher levels of investigation of the new stimuli (0–10 s; mean 2.56 s) compared to the previously experienced stimuli (0–44 s; mean 7.81 s) (see Fig. 2).
Discussion We observed that horses habituated to a body odour sample obtained from a previously unfamiliar conspecific when it was presented on two separate occasions and when the same sample was presented for a third presentation at the same time as a novel sample, spent more time investigating the novel sample. These results suggest that horses (of both
123
1010
Anim Cogn (2014) 17:1007–1011
Fig. 2 Mean time spent sniffing the stimulus (± SE) in the initial two presentations of the same odour cue and in the final ‘discrimination’ test
sexes) were able to discriminate between two stimuli derived from the body odour of unfamiliar conspecifics, confirming the findings of Hothersall et al. (2010) that horses were able to remember body odours of individuals over a 15-min retention interval, but extending their findings to include successful discrimination. Our results suggest that we can now add body odour to the other sensory sources that horses can use to discriminate between conspecifics: visual and acoustic cues (Feh 2005; Proops et al. 2008; Lemasson et al. 2009), urine/vaginal secretions (Marinier et al. 1988; Hothersall et al. 2010), and faeces (Stahlbaum and Houpt 1989; Krueger and Flauger 2011). Compared to the results of Hothersall et al. (2010), we observed less variation in the investigatory responses of the horses. This is likely to have been due to our larger sample size as well as our matching of odour samples to test subjects in terms of sex and age. A better understanding of social memory and recognition processes may help us to refine husbandry/management techniques and consequently improve animal welfare (Mendl et al. 2001; Burman and Mendl 2003). Given that increased social contact between horses is likely to be beneficial in relation to animal welfare (see, for example, Christensen et al. 2002), there is a need to identify suitable and safe ways to integrate horses together (see Hartmann et al. 2012) and the use of olfactory cues could be one way to achieve this. Although our study demonstrates habituation and discrimination in horses on the basis of socially derived body odour cues, the stimuli were only presented for brief 2-min periods. Experimental data (Murphy and Arkins 2007; Proops et al. 2008; Hanggi and Ingersoll 2009) suggest that
123
horses are able to discriminate and recognise other horses over long periods of time. Future research is therefore required to investigate how the retention interval and the quality of the sample influence the process (e.g. Burman and Mendl 2006) and whether the familiarity of odour cues influences resilience of social memory, as studies in other species have revealed that the elements of common husbandry procedures, e.g. handling, can disrupt social recognition (Burman and Mendl 2000, 2004). The results of this study indicate that horses have a social memory that can be based on body odours (lasting for at least for 15 min), and this may well be a step towards developing an understanding of the cognitive processes that inform the practical issue of how, and when, to introduce horses into social groups. Acknowledgments We would like to thank the horse owners, Robin Snelson, and the equine yard staff at the Riseholme Park campus. We would also like to thank two anonymous reviewers and the editor for their constructive comments.
References Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Trans R Soc B 361:2061–2078 Burman O, Mendl M (2000) Short-term social memory in the laboratory rat: its susceptibility to disturbance. Appl Anim Behav Sci 67:241–254 Burman O, Mendl M (2003) The influence of pre-experimental experience on social discrimination in rats (Rattus norvegicus). J Comp Psychol 117:344–345
Anim Cogn (2014) 17:1007–1011 Burman O, Mendl M (2004) Disruptive effects of standard husbandry practice on laboratory rat social discrimination. Anim Welf 13:125–135 Burman O, Mendl M (2006) Long-term social memory in the laboratory rat (Rattus norvegicus). Anim Welf 15:379–382 Christensen J, Ladewig J, Sondergaard E, Malmkvist J (2002) Effects of individual versus group stabling on social behaviour in domestic stallions. Appl Anim Behav Sci 75:233–248 Feh C (2005) Relationships and communication in socially natural horse herds. In: Mills DS, McDonnell SM (eds) The domestic horse: the origins, development, and management of its behaviour. Cambridge University Press, Cambridge Hanggi E, Ingersoll J (2009) Long-term memory for categories and concepts in horses (Equus caballus). Anim Cogn 12:451–462 Hartmann E, Sondergaard E, Keeling L (2012) Keeping horses in groups: a review. Appl Anim Behav Sci 136:77–87 Heitor F, Vicente L (2007) Learning about horses: what is equine learning all about? Behav Process 76:34–36 Hothersall B, Harris P, So¨rtoft L, Nicol C (2010) Discrimination between conspecific odour samples in the horse (Equus caballus). Appl Anim Behav Sci 126:37–44 Kiley-Worthington M (1987) The behaviour of horses. J.A. Allen, London Krueger K, Flauger B (2011) Olfactory recognition of individual competitors by means of faeces in horse (Equus caballus). Anim Cogn 14:245–257
1011 Krueger K, Heinze J (2008) Horse sense: social status of horses (Equus caballus) affects their likelihood of copying other horses’ behaviour. Anim Cogn 11:431–439 Lemasson A, Boutin A, Boivin S, Blois-Heulin C, Hausberger M (2009) Horse (Equus caballus) whinnies: a source of social information. Anim Cogn 12:693–704 Marinier S, Alexander A, Waring G (1988) Flehmen behaviour in the domestic horse: discrimination of conspecific odours. Appl Anim Behav Sci 19:227–237 Mendl M, Burman O, Laughlin K, Paul E (2001) Animal memory and animal welfare. Anim Welf 10:141–159 Murphy J, Arkins S (2007) Equine learning behaviour. Behav Process 76:1–13 Proops L, McComb K, Reby D (2008) Cross-modal individual recognition in domestic horses (Equus caballus). PNAS 106:947–951 Rubenstein DI, Hack MA (1992) Horse signals: the sounds and scents of fury. Evol Ecol 6:254–260 Stahlbaum CC, Houpt KA (1989) The role of the Flehmen response in the behavioral repertoire of the stallion. Physiol Behav 45:1207–1214
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