Journal of Comparative Psychology 2015, Vol. 129, No. 3, 311–315
© 2015 American Psychological Association 0735-7036/15/$12.00 http://dx.doi.org/10.1037/a0039032
BRIEF REPORT
This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Tenseness Relaxed by Vocalizing, Illustrated by Horses (Equus caballus) Whinnying Alban Lemasson
Kevin Remeuf
Université de Rennes 1 and Institut Universitaire de France
Université de Rennes 1
Martine Hausberger Centre National de la Recherche Scientifique Animal calls are commonly considered indicators of a sudden change in their arousal state. However, reports evidencing associated internal physiological changes are rare. By homology with human “emotional” vocal productions (e.g., laughter and crying), we predicted that animal vocal productions may result in relaxing tenseness or excitement. In this study, 15 stallions equipped with a heart rate monitor were presented a mare at some distance so as to prevent contact, thereby increasing the males’ arousal. Stallions’ heart rates increased just before whinnying but returned to baseline rates while vocalizing. We found that sudden changes of a caller’s arousal state could be associated with vocalizing, and this opens new lines for noninvasive research concerning the self-regulation of emotional via vocal production in humans and animals. Keywords: heartbeat, vocal production, arousal, mammals
texts are similarly associated with increases in both call and heart rates or stress hormone concentrations—for example, aggressive encounters in bats (Gadziola, Grimsley, Faure, & Wenstrup, 2012), human approach in pigs (Marchant, Whittaker, & Broom, 2001), and social separation in domestic animals (Boissy & Le Neindre, 1997; Schrader & Todt, 1998). According to Owren et al. (2010), human laughter or crying appears when arousal is high, and vocalizations then relax tenseness (Miller & Fry, 2009). In fact, humans’ verbal productions follow a similar pattern. Before or when starting to speak in public, heart rate and the levels of some other physiological parameters increase, reach a peak, and decrease progressively during the talk (Behnke & Sawyer, 2001; Gatchel & Proctor, 1976; Steiner, Ryst, Berkowitz, Gschwendt, & Koopman, 2002). We hypothesized, by referring to a modern adaptation of Lorenz’s “psychohydraulic model of motivation” (Lorenz, 1950), that producing sounds would be a way for animals to relax tenseness in overexciting or stressful contexts. This model is comparable to a hydraulic flow system such as a flush toilet. The fluid in the tank is analogous to action-specific energy that accumulates over time, increasing the animal’s drive to perform a particular behavior. Authors proposed that this effect could also explain the association between play and chronic stress in horses (Hausberger, Fureix, Bourjade, Wessel-Robert, & Richard-Yris, 2012). Horses are appropriate models in this perspective. First, horses produce whinny calls during social separation and when seeking contact, indicating their role when dealing with social arousal (Durier, Henry, Sankey, Sizun, & Hausberger, 2012; Wolff, Hausberger, & Le Scolan, 1997). Second, whinnies are long vocalizations with a complex acoustic pattern (Lemasson, Boutin, Boivin, Blois-
Animal vocalizations are often considered external representations of a change in the caller’s internal state (Morton, 1977). Owren, Rendall, and Ryan (2010) compared the role of animal vocalizations to that of human laughter and crying, arguing that mammals’ vocal productions are associated with activation of emotional-related brain structures. However, a link between callers’ vocalizing and internal changes has been demonstrated mainly indirectly in most studies—for example, changes in call rates (Colonnello, Iacobucci, & Newberry, 2010; Marx, Leppelt, & Ellendorff, 2001) and structures (Lemasson, Remeuf, Rossard, & Zimmerman, 2012; Schehka & Zimmermann, 2009) following social disturbances. One difficulty to evidence a direct link is that it requires simultaneous recordings of the caller’s physiological changes. Experimental studies with mammals have evidenced that stressing con-
This article was published Online First April 27, 2015. Alban Lemasson, Ethologie animale et Humaine, Université de Rennes 1 and Institut Universitaire de France; Kevin Remeuf, Ethologie animale et Humaine, Université de Rennes 1; Martine Hausberger, Centre National de la Recherche Scientifique. This study was funded by the Institut français du cheval et de l’équitation, the French Ministry of Research, and the Centre National de la Recherche Scientifique (CNRS). We thank the stud farms for their logistical support and Ann Cloarec for correcting our English. Correspondence concerning this article should be addressed to Alban Lemasson, Université de Rennes 1, Ethologie animale et humaine, UMR 6552 - CNRS, Station Biologique, 35380, Paimpont, France. E-mail: [email protected] 311
LEMASSON, REMEUF, AND HAUSBERGER
This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
312
Heulin, & Hausberger, 2009). Third, heart rate is known to encode this species’ internal states (e.g., degree of calmness or fear) reliably (Christensen, Malmkvist, Nielsen, & Keeling, 2008; Sankey et al., 2010). Here, we created a context of sexual arousal and motivational conflict by presenting a mare to stallions at a distance. These stallions usually see mares only for mating and, when free to move, typically approach mares so as to make contact with them (McDonnell, 2005). Here, however, stallions were held by a human observer so that they remained out of reach of the mare. This context was used to ensure a high arousal level because it is known to trigger the “frenzied stallion syndrome” due to a conflict of motivation (restrained while wanting to approach) (McDonnell, 2005). Whinnies are considered a good measure of the emotional state in such situations (Durier et al., 2012; Wolff et al., 1997). For humans, laughing, crying, and giving a speech to an audience are contexts very different from the sexual encounter simulated with our horses, but regardless of the emotional valence of the context, we predicted that, as for human emotional expressions, arousal would peak just prior to vocal production, whereas whinnying would be associated with relaxing tenseness and hence a decrease in heart rate.
Method Study Horses In February 2012, we tested 15 stallions (S1–S15, Equus caballus) of various breeds and ages, housed at three French stud farms (see Table 1). Stallions were housed singly in 3-m ⫻ 3-m stalls and had access to paddocks for 1 or 2 h each day. Horses were fed hay and pellets twice a day. Water was provided ad libitum. These stallions were used only for breeding, and all had had the opportunity to cover mares (i.e., mate). Experiments complied with the American Psychological Association’s ethical standards and with the current French regulations governing the care and use of research animals and have been approved by the “Institut français du cheval et de l’équitation.” Experiments were performed in accordance with the European Communities Council Directive of
November 24, 1986 (86/609/CEE). Only noninvasive behavioral observations on nonlaboratory animals were conducted, which does not require ethics approval.
Call Elicitation Stallions were led out of their box in a random order by a familiar caretaker twice for 10 min on different days. During each 10-min session, the male stood 50 m from his stall while another caretaker led a mare (the same for all males from a given stud farm) to 10 –20 m from the stallion. From their stalls, males had frequent opportunities to hear (but not to see) the mare. A total of 178 whinnies (12 ⫾ 6 per stallion, minimum of 10 to maximum of 18) were uttered during these sessions. The first whinny of each session was uttered 174 ⫾ 22 s (mean ⫾ SE) after the mare arrival, and the interwhinny delay was 71 ⫾ 6 s. A whinny lasts for 1,751 ms on average and is typically composed of a short, flat tonal introduction, followed by a long atonal rhythmical climax (Lemasson et al., 2009) (see Figure 1 for an example).
Heartbeat Recordings Before being taken outdoors, subjects were equipped with a heart rate monitor for horses (Polar Horse Trainer S810i, Polar Electro, Finland) fixed around their chest, recording heartbeats per period of 5 s. Numbers of heartbeats were averaged for each stallion within four time windows: the 5 s when being led out from their stalls (control measure in the absence of the mare: HBc), the 5 s during which a whinny was emitted in the presence of a mare (HB5s), the 5 preceding seconds (HB-5s), and the 10-min session (HB10m ⫽ average of all 5-s measures of mare presentation, excluding HB5s and HB-5s values). We used a nonparametric two-tailed Friedman test and Wilcoxon matched-pairs signed-rank test to assess changes in heart rate measures, applying Bonferroni corrections for multiple comparisons. Spearman tests were also used to investigate the potential correlation between heart rates and latency to first call and number of calls.
Results Table 1 Stallion Characteristics Stallion No.
Age (y)
Breed
Stud farm (Haras National)
S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12 S13 S14 S15
15 17 27 17 23 13 13 12 10 10 10 9 9 14 4
Holsteiner Thoroughbred Dutch warmblood French trotter Arab purebred French saddlebred French saddlebred French trotter French trotter French saddlebred French trotter French saddlebred Arab purebred Saddlebred Connemara
Saint-Lô Le Pin Lamballe Le Pin Lamballe Saint-Lô Le Pin Le Pin Le Pin Saint-Lô Lamballe Saint-Lô Le Pin Le Pin Saint-Lô
First, stallions’ heart rates were significantly higher (almost twice) in the presence (HB10m: mean ⫾ CI ⫽ 93.87 ⫾ 7.4 beats per minute [bpm]) than in the absence of a mare (HBc: 49.4 ⫾ 8.2 bpm) (Wilcoxon test, N ⫽ 15, z ⫽ 3.41, p ⫽ .0007), confirming the effect of the experimental procedure on the stallion’s arousal. Second, we found no long-term relationship between vocalizing and change in heart rate. Stallions’ heart rates did not differ between the first and second halves of the 10-min mare presentation (Wilcoxon test, N ⫽ 15, z ⫽ 1.19, p ⫽ .23), suggesting no habituation. Also, the latency duration to produce the first call after spotting the female (178 ⫾ 52 s) was not correlated to the average heart rate of the stallion in that time window (Spearman test, N ⫽ 15, R ⫽ ⫺0.09, p ⫽ .76). Last, the difference between the overall heartbeat rate measured during the 10-min encounter (HB10m) and the baseline heartbeat measured just before meeting with the mare (HBc), reflecting the overall increase of arousal, did not predict the number of vocalizations emitted (N ⫽ 15, R ⫽ ⫺0.12, p ⫽ .65).
This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
TENSENESS RELAXED BY WHINNYING
Figure 1.
313
Sonogram of a typical stallion’s whinny.
Third, we found a short-term relationship between vocalizing and change in heart rate. Heart rates were subject to significant variations according to the timing of call utterances (Friedman test: HB10m/HB5s/HB-5s, N ⫽ 15, 2 ⫽ 14.93, p ⫽ .0006). Stallions’ heart rates were higher during the 5 s preceding whinnying (HB5s: 102.38 ⫾ 8.2 bpm) than during the 5 s a whinny was emitted (HB5s: 96.02 ⫾ 8.2 bpm) (Wilcoxon test, N ⫽ 15, z ⫽ 3.41, p ⫽ .0007) and also higher than the overall heartbeat rate measured during the 10-min encounter with the mare (HB10m, N ⫽ 15, z ⫽ 2.39, p ⫽ .017) (see Figure 2). Heart rates after starting calling (HB5s) did not differ significantly from this overall heartbeat rates (HB10m) (N ⫽ 15, z ⫽ 0.57, p ⫽ .57).
Discussion During an encounter with a mare that is out of reach, a stallion’s heart rate varied significantly in relation to his vocal activity. Just before calling, his heart rate accelerated but returned to baseline level while whinnying. Hence, calling can be seen as an emotional discharge following a sudden change in the stallion’s internal state, a reaction that may be mechanistically homologous to human crying and laughter. However, this emotional discharge is a shortterm (i.e., a few seconds) mechanism because no long-term (i.e., several minutes) effect of vocalizing was found here. An encounter between two conspecifics, especially if it is occasional and involves both sexes, is a source of arousal. Increase of heartbeat rates in socially exciting contexts is a well-known trait in humans and animals (Appelhans & Luecken, 2006; Christensen et al., 2008). Horses’ heartbeat rates recorded during our encounters were almost twice as high as their heart rates preceding mare presentation. This latter control measure was about the top of the range of typical rates found in horses at rest (26 – 42 bpm; Pilliner & Davies, 2004). Interestingly, the fact that our subjects’ heartbeat rates were higher during the 5 s preceding whinnying recalls the reactions of humans about to give a talk (Behnke & Sawyer, 2001). The relationship between humans’ sudden arousal changes and oral expression has been described. Arousal changes, notably in a frustrating or exciting context, also trigger unconscious oral expression such as swearing, laughing, or crying (Hirsch, 1985). Some arousal states, such as happiness and anger, are considered typically “talkative” emotions, in contrast to fear and sadness (Cosnier, 1994). Vocal expressions can be considered a human as well as an animal “reflex” for searching for social contact, because social encounters usually
trigger sudden increases of call rates (De Marco, Cozzolino, DessiFulgheri, & Thierry, 2011). Our stallions may have been frustrated during the distant (preventing physical contact) encounters with a mare or just sexually excited, inducing a sudden increase of heartbeat rate, followed by a vocalization enabling emotional regulation. The acoustic structures of whinnies support the pattern expected after comparison with human and nonhuman primate vocalizations following experiencing an intense arousal change, that is, long calls with a noisy frequency spectrum and marked energy pulses (Davila Ross, Owren, & Zimmermann, 2009; Lemasson et al., 2009). There is an open debate about the potential neurophysiological mechanisms underlying homeostasis and self-regulation of emotion. As mentioned earlier, it is possible that vocalizing enables an emotional discharge, fitting with Lorenz’s psychohydraulic model of motivation (Lorenz, 1950). In line with that idea, Takahashi, Narayanan, and Ghazanfar (2012) constructed a computational model of marmoset monkey vocal production, based on the interactions among three neural components: auditory, motor, and drive. On the basis of physiological and anatomical data, they envisioned these components as roughly representing the auditory cortex, motor cortex, and limbic system, respectively. Four steps are involved: (a) the neural activity in the drive component spontaneously increases until it reaches a threshold; (b) it activates the motor component, which will produce a call; and (c) the sound of this call increases activity in the auditory component, (d) which will then inhibit the drive component. How-
Figure 2. Stallions’ heartbeat rates preceding calling (HB-5s), during calling (HB5s), and overall (HB10m) (mean numbers per minute ⫾ SE) (Wilcoxon tests with Bonferroni correction: ⴱ p ⱕ .017, ⴱⴱ p ⱕ .003).
This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
314
LEMASSON, REMEUF, AND HAUSBERGER
ever, confirming the precalling accumulation of arousal up to a certain threshold would require measurements at a more precise temporal level (i.e., less than a second). The question would then be as follows: what happens when the threshold is reached and the animal cannot call? We believe that alternative behavioral expressions (e.g., body movement) would compensate and enable the emotional regulation. We also acknowledge that body movements, as well as their potential direct impact on heart rates, have not been scored here. However, the fact that those stallions were held by a caretaker limited locomotion anyway, especially because they were trained to remain immobile when on a halt. Several other self-regulation mechanisms have been discussed. First, calling, especially when emitting long vocalizations such as whinnies, is associated with a ventilation process, and it has been shown that cardiac and respiration rates are linked (Samet, Lambert, James, Mermier, & Chick, 1993). Second, physiological, including hormonal, measures (heart rate and prolactin, oxytocin, and cortisol concentrations) showed that singing has a clear effect on human well-being (i.e., release of emotional tension) (Grape, Sandgren, Hansson, Ericson, & Theorell, 2002). Also, data on surgically “devocalized” and sham-operated budgerigars indicated that the gonadal activity of males may be stimulated as a result of their own performance of vocal display rather than as a result of hearing such behavior by others (Brockway, 1967). Third, Riters (2011) reviewed the literature about the neural regulation of the motivation to sing in birds and highlighted different mechanisms in social-directed and undirected (self-directed?) sounds. Dopamine and opioid neuropeptides play a primary role in reward seeking and sensory pleasure in general but also in songbirds. Distinct patterns of dopamine activity influence the motivation to produce undirected and social-directed song. Undirected communication is intrinsically reinforced by immediate release of opioids induced by the act of singing. Directed communication is socially reinforced by opioids released as part of social interactions. Fourth, it was reported that in primates, a somatosensory feedback occurs during vocal production due to face and tongue movements (Ghazanfar, 2011). Hence, calling or being about to call is directly associated with changes similarly in a human and animal’s arousal state. This finding is in line with previous work that suggested that whinnying was a response to stress in a context of locomotor inhibition (Durier et al., 2012), as also used here. Perspectives for future work may deal with the relation between the type of emotion experienced and heart rate variability, as well as between the heart rate values and subsequent acoustic structures. For instance, it is unclear how vocalizations affect heart rate after experiencing a positive or a negative emotional change. Also, whinnies are basically composed of a long tonal introduction and a long atonal climax with repeated units. A more detailed investigation is needed to understand the relative influence of both acoustic structures on emotional regulation. Moreover, more comparative work is necessary to assess the evolutionary distribution of this mechanism in mammals. Finally, this finding opens new lines of theoretical research about the definition of the functions of vocal communication. Although the traditional definition stipulates that vocal signals are targeting one or several external receivers, one may also consider that vocalizing has a self-regulatory function (see also Owren et al., 2010). More generally, the impact of the communicative act on the performer has been largely understudied so far.
References Appelhans, B. M., & Luecken, L. J. (2006). Heart rate variability as an index of regulated emotional responding. Review of General Psychology, 10, 229 –240. http://dx.doi.org/10.1037/1089-2680.10.3.229 Behnke, R. R., & Sawyer, C. R. (2001). Patterns of psychological state anxiety in public speaking as a function of anxiety sensitivity. Communication Quarterly, 49, 84 –94. http://dx.doi.org/10.1080/ 01463370109385616 Boissy, A., & Le Neindre, P. (1997). Behavioral, cardiac and cortisol responses to brief peer separation and reunion in cattle. Physiology & Behavior, 61, 693– 699. http://dx.doi.org/10.1016/S0031-9384(96) 00521-5 Brockway, B. F. (1967). The influence of vocal behavior on the performer’s testicular activity in budgerigars (Melopsittacus undulatus). The Wilson Bulletin, 79, 328 –334. Christensen, J. W., Malmkvist, J., Nielsen, B. L., & Keeling, L. J. (2008). Effects of a calm companion on fear reactions in naive test horses. Equine Veterinary Journal, 40, 46 –50. http://dx.doi.org/10.2746/ 042516408X245171 Colonnello, V., Iacobucci, P., & Newberry, R. C. (2010). Vocal and locomotor responses of piglets to social isolation and reunion. Developmental Psychobiology, 52, 1–12. http://dx.doi.org/10.1002/dev.20406 Cosnier, J. (1994). La Psychologie des emotions et des sentiments. [The psychology of emotions and feelings]. Paris, France: Retz. Davila Ross, M., Owren, M. J., & Zimmermann, E. (2009). Reconstructing the evolution of laughter in great apes and humans. Current Biology, 19, 1106 –1111. http://dx.doi.org/10.1016/j.cub.2009.05.028 De Marco, A., Cozzolino, R., Dessì-Fulgheri, F., & Thierry, B. (2011). Collective arousal when reuniting after temporary separation in Tonkean macaques. American Journal of Physical Anthropology, 146, 457– 464. http://dx.doi.org/10.1002/ajpa.21606 Durier, V., Henry, S., Sankey, C., Sizun, J., & Hausberger, M. (2012). Locomotor inhibition in adult horses faced to stressors: A single postpartum experience may be enough! Frontiers in Psychology, 3, 442. http://dx.doi.org/10.3389/fpsyg.2012.00442 Gadziola, M. A., Grimsley, J. M. S., Faure, P. A., & Wenstrup, J. J. (2012). Social vocalizations of big brown bats vary with behavioral context. PLoS One, 7, e44550. http://dx.doi.org/10.1371/journal.pone.0044550 Gatchel, R. J., & Proctor, J. D. (1976). Effectiveness of voluntary heart rate control in reducing speech anxiety. Journal of Consulting and Clinical Psychology, 44, 381–389. http://dx.doi.org/10.1037/0022-006X.44.3 .381 Ghazanfar, A. A. (2011). The unity of the senses in primate vocal communication. In M. J. Murray & M. Wallace (Eds.), The neural bases of multisensory processes (pp. 653– 666). Boca Raton, FL: CRC Press. http://dx.doi.org/10.1201/9781439812174-41 Grape, C., Sandgren, M., Hansson, L. O., Ericson, M., & Theorell, T. (2002). Does singing promote well-being? An empirical study of professional and amateur singers during a singing lesson. Integrative Physiological & Behavioral Science, 38, 65–74. http://dx.doi.org/10.1007/ BF02734261 Hausberger, M., Fureix, C., Bourjade, M., Wessel-Robert, S., & RichardYris, M.-A. (2012). On the significance of adult play: What does social play tell us about adult horse welfare? Naturwissenschaften, 99, 291– 302. http://dx.doi.org/10.1007/s00114-012-0902-8 Hirsch, R. (1985). Swearing and the expression of emotions. In L. G. Andersson & R. Hirsch (Eds.), Perspectives on swearing (pp. 61– 82). Goteborg, Sweden: University of Goteborg. Lemasson, A., Boutin, A., Boivin, S., Blois-Heulin, C., & Hausberger, M. (2009). Horse (Equus caballus) whinnies: A source of social information. Animal Cognition, 12, 693–704. http://dx.doi.org/10.1007/s10071009-0229-9 Lemasson, A., Remeuf, K., Rossard, A., & Zimmermann, E. (2012). Cross-taxa similarities in affect-induced changes of vocal behavior and
This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
TENSENESS RELAXED BY WHINNYING voice in arboreal monkeys. PLoS One, 7, e45106. http://dx.doi.org/ 10.1371/journal.pone.0045106 Lorenz, K. Z. (1950). The comparative method in studying innate behavior patterns. In Society for Experimental Biology Symposium IV (Ed.), Physiological mechanisms in animal behavior (pp. 221–268). Oxford, UK: Academic Press. Marchant, J. N., Whittaker, X., & Broom, D. M. (2001). Vocalisations of the adult female domestic pig during a standard human approach test and their relationships with behavioural and heart rate measures. Applied Animal Behaviour Science, 72, 23–39. http://dx.doi.org/10.1016/S01681591(00)00190-8 Marx, G., Leppelt, J., & Ellendorff, F. (2001). Vocalisation in chicks (Gallus gallus dom.) during stepwise social isolation. Applied Animal Behaviour Science, 75, 61–74. http://dx.doi.org/10.1016/S0168-1591 (01)00180-0 McDonnell, S. M. (2005). Sexual behavior. In D. S. Mills & S. M. McDonnell (Eds.), The domestic horse: The origins, development, and management of its behavior (pp. 110 –125). London, UK: Cambridge University Press. Miller, M., & Fry, W. F. (2009). The effect of mirthful laughter on the human cardiovascular system. Medical Hypotheses, 73, 636 – 639. http:// dx.doi.org/10.1016/j.mehy.2009.02.044 Morton, E. S. (1977). On the occurrence and significance of motivationstructural rules in some bird and mammal sounds. American Naturalist, 111, 855– 869. http://dx.doi.org/10.1086/283219 Owren, M., Rendall, D., & Ryan, M. (2010). Redefining animal signaling: Influence versus information in communication. Biology and Philosophy, 25, 755–780. http://dx.doi.org/10.1007/s10539-010-9224-4 Pilliner, S., & Davies, Z. (2004). Equine science (2nd ed.). Oxford, UK: Blackwell. Riters, L. V. (2011). Pleasure seeking and birdsong. Neuroscience and Biobehavioral Reviews, 35, 1837–1845. http://dx.doi.org/10.1016/j .neubiorev.2010.12.017
315
Samet, J. M., Lambert, W. E., James, D. S., Mermier, C. M., & Chick, T. W. (1993). Assessment of heart rate as a predictor of ventilation. Research Report (Health Effects Institute), 59, 19 –55. Sankey, C., Richard-Yris, M.-A., Henry, S., Fureix, C., Nassur, F., & Hausberger, M. (2010). Reinforcement as a mediator of the perception of humans by horses (Equus caballus). Animal Cognition, 13, 753–764. http://dx.doi.org/10.1007/s10071-010-0326-9 Schehka, S., & Zimmermann, E. (2009). Acoustic features to arousal and identity in disturbance calls of tree shrews (Tupaia belangeri). Behavioural Brain Research, 203, 223–231. http://dx.doi.org/10.1016/j.bbr .2009.05.007 Schrader, L., & Todt, D. (1998). Vocal quality is correlated with levels of stress hormones in. domestic pigs (Sus scrofa domestica). Ethology, 104, 859 – 876. http://dx.doi.org/10.1111/j.1439-0310.1998.tb00036.x Steiner, H., Ryst, E., Berkowitz, J., Gschwendt, M. A., & Koopman, C. (2002). Boys’ and girls’ responses to stress: Affect and heart rate during a speech task. Journal of Adolescent Health, 30(Suppl.), 14 –21. http:// dx.doi.org/10.1016/S1054-139X(01)00387-1 Takahashi, D. Y., Narayanan, D., & Ghazanfar, A. A. (2012). A computational model for vocal exchange dynamics and their development in marmoset monkeys. IEEE International Conference on Development and Learning and Epigenetic Robotics, 2012, 1–2. Wolff, A., Hausberger, M., & Le Scolan, N. (1997). Experimental tests to assess emotionality in horses. Behavioural Processes, 40, 209 –221. http://dx.doi.org/10.1016/S0376-6357(97)00784-5
Received November 28, 2014 Revision received February 4, 2015 Accepted February 5, 2015 䡲
© 2015 American Psychological Association 0735-7036/15/$12.00 http://dx.doi.org/10.1037/a0039032
BRIEF REPORT
This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Tenseness Relaxed by Vocalizing, Illustrated by Horses (Equus caballus) Whinnying Alban Lemasson
Kevin Remeuf
Université de Rennes 1 and Institut Universitaire de France
Université de Rennes 1
Martine Hausberger Centre National de la Recherche Scientifique Animal calls are commonly considered indicators of a sudden change in their arousal state. However, reports evidencing associated internal physiological changes are rare. By homology with human “emotional” vocal productions (e.g., laughter and crying), we predicted that animal vocal productions may result in relaxing tenseness or excitement. In this study, 15 stallions equipped with a heart rate monitor were presented a mare at some distance so as to prevent contact, thereby increasing the males’ arousal. Stallions’ heart rates increased just before whinnying but returned to baseline rates while vocalizing. We found that sudden changes of a caller’s arousal state could be associated with vocalizing, and this opens new lines for noninvasive research concerning the self-regulation of emotional via vocal production in humans and animals. Keywords: heartbeat, vocal production, arousal, mammals
texts are similarly associated with increases in both call and heart rates or stress hormone concentrations—for example, aggressive encounters in bats (Gadziola, Grimsley, Faure, & Wenstrup, 2012), human approach in pigs (Marchant, Whittaker, & Broom, 2001), and social separation in domestic animals (Boissy & Le Neindre, 1997; Schrader & Todt, 1998). According to Owren et al. (2010), human laughter or crying appears when arousal is high, and vocalizations then relax tenseness (Miller & Fry, 2009). In fact, humans’ verbal productions follow a similar pattern. Before or when starting to speak in public, heart rate and the levels of some other physiological parameters increase, reach a peak, and decrease progressively during the talk (Behnke & Sawyer, 2001; Gatchel & Proctor, 1976; Steiner, Ryst, Berkowitz, Gschwendt, & Koopman, 2002). We hypothesized, by referring to a modern adaptation of Lorenz’s “psychohydraulic model of motivation” (Lorenz, 1950), that producing sounds would be a way for animals to relax tenseness in overexciting or stressful contexts. This model is comparable to a hydraulic flow system such as a flush toilet. The fluid in the tank is analogous to action-specific energy that accumulates over time, increasing the animal’s drive to perform a particular behavior. Authors proposed that this effect could also explain the association between play and chronic stress in horses (Hausberger, Fureix, Bourjade, Wessel-Robert, & Richard-Yris, 2012). Horses are appropriate models in this perspective. First, horses produce whinny calls during social separation and when seeking contact, indicating their role when dealing with social arousal (Durier, Henry, Sankey, Sizun, & Hausberger, 2012; Wolff, Hausberger, & Le Scolan, 1997). Second, whinnies are long vocalizations with a complex acoustic pattern (Lemasson, Boutin, Boivin, Blois-
Animal vocalizations are often considered external representations of a change in the caller’s internal state (Morton, 1977). Owren, Rendall, and Ryan (2010) compared the role of animal vocalizations to that of human laughter and crying, arguing that mammals’ vocal productions are associated with activation of emotional-related brain structures. However, a link between callers’ vocalizing and internal changes has been demonstrated mainly indirectly in most studies—for example, changes in call rates (Colonnello, Iacobucci, & Newberry, 2010; Marx, Leppelt, & Ellendorff, 2001) and structures (Lemasson, Remeuf, Rossard, & Zimmerman, 2012; Schehka & Zimmermann, 2009) following social disturbances. One difficulty to evidence a direct link is that it requires simultaneous recordings of the caller’s physiological changes. Experimental studies with mammals have evidenced that stressing con-
This article was published Online First April 27, 2015. Alban Lemasson, Ethologie animale et Humaine, Université de Rennes 1 and Institut Universitaire de France; Kevin Remeuf, Ethologie animale et Humaine, Université de Rennes 1; Martine Hausberger, Centre National de la Recherche Scientifique. This study was funded by the Institut français du cheval et de l’équitation, the French Ministry of Research, and the Centre National de la Recherche Scientifique (CNRS). We thank the stud farms for their logistical support and Ann Cloarec for correcting our English. Correspondence concerning this article should be addressed to Alban Lemasson, Université de Rennes 1, Ethologie animale et humaine, UMR 6552 - CNRS, Station Biologique, 35380, Paimpont, France. E-mail: [email protected] 311
LEMASSON, REMEUF, AND HAUSBERGER
This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
312
Heulin, & Hausberger, 2009). Third, heart rate is known to encode this species’ internal states (e.g., degree of calmness or fear) reliably (Christensen, Malmkvist, Nielsen, & Keeling, 2008; Sankey et al., 2010). Here, we created a context of sexual arousal and motivational conflict by presenting a mare to stallions at a distance. These stallions usually see mares only for mating and, when free to move, typically approach mares so as to make contact with them (McDonnell, 2005). Here, however, stallions were held by a human observer so that they remained out of reach of the mare. This context was used to ensure a high arousal level because it is known to trigger the “frenzied stallion syndrome” due to a conflict of motivation (restrained while wanting to approach) (McDonnell, 2005). Whinnies are considered a good measure of the emotional state in such situations (Durier et al., 2012; Wolff et al., 1997). For humans, laughing, crying, and giving a speech to an audience are contexts very different from the sexual encounter simulated with our horses, but regardless of the emotional valence of the context, we predicted that, as for human emotional expressions, arousal would peak just prior to vocal production, whereas whinnying would be associated with relaxing tenseness and hence a decrease in heart rate.
Method Study Horses In February 2012, we tested 15 stallions (S1–S15, Equus caballus) of various breeds and ages, housed at three French stud farms (see Table 1). Stallions were housed singly in 3-m ⫻ 3-m stalls and had access to paddocks for 1 or 2 h each day. Horses were fed hay and pellets twice a day. Water was provided ad libitum. These stallions were used only for breeding, and all had had the opportunity to cover mares (i.e., mate). Experiments complied with the American Psychological Association’s ethical standards and with the current French regulations governing the care and use of research animals and have been approved by the “Institut français du cheval et de l’équitation.” Experiments were performed in accordance with the European Communities Council Directive of
November 24, 1986 (86/609/CEE). Only noninvasive behavioral observations on nonlaboratory animals were conducted, which does not require ethics approval.
Call Elicitation Stallions were led out of their box in a random order by a familiar caretaker twice for 10 min on different days. During each 10-min session, the male stood 50 m from his stall while another caretaker led a mare (the same for all males from a given stud farm) to 10 –20 m from the stallion. From their stalls, males had frequent opportunities to hear (but not to see) the mare. A total of 178 whinnies (12 ⫾ 6 per stallion, minimum of 10 to maximum of 18) were uttered during these sessions. The first whinny of each session was uttered 174 ⫾ 22 s (mean ⫾ SE) after the mare arrival, and the interwhinny delay was 71 ⫾ 6 s. A whinny lasts for 1,751 ms on average and is typically composed of a short, flat tonal introduction, followed by a long atonal rhythmical climax (Lemasson et al., 2009) (see Figure 1 for an example).
Heartbeat Recordings Before being taken outdoors, subjects were equipped with a heart rate monitor for horses (Polar Horse Trainer S810i, Polar Electro, Finland) fixed around their chest, recording heartbeats per period of 5 s. Numbers of heartbeats were averaged for each stallion within four time windows: the 5 s when being led out from their stalls (control measure in the absence of the mare: HBc), the 5 s during which a whinny was emitted in the presence of a mare (HB5s), the 5 preceding seconds (HB-5s), and the 10-min session (HB10m ⫽ average of all 5-s measures of mare presentation, excluding HB5s and HB-5s values). We used a nonparametric two-tailed Friedman test and Wilcoxon matched-pairs signed-rank test to assess changes in heart rate measures, applying Bonferroni corrections for multiple comparisons. Spearman tests were also used to investigate the potential correlation between heart rates and latency to first call and number of calls.
Results Table 1 Stallion Characteristics Stallion No.
Age (y)
Breed
Stud farm (Haras National)
S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12 S13 S14 S15
15 17 27 17 23 13 13 12 10 10 10 9 9 14 4
Holsteiner Thoroughbred Dutch warmblood French trotter Arab purebred French saddlebred French saddlebred French trotter French trotter French saddlebred French trotter French saddlebred Arab purebred Saddlebred Connemara
Saint-Lô Le Pin Lamballe Le Pin Lamballe Saint-Lô Le Pin Le Pin Le Pin Saint-Lô Lamballe Saint-Lô Le Pin Le Pin Saint-Lô
First, stallions’ heart rates were significantly higher (almost twice) in the presence (HB10m: mean ⫾ CI ⫽ 93.87 ⫾ 7.4 beats per minute [bpm]) than in the absence of a mare (HBc: 49.4 ⫾ 8.2 bpm) (Wilcoxon test, N ⫽ 15, z ⫽ 3.41, p ⫽ .0007), confirming the effect of the experimental procedure on the stallion’s arousal. Second, we found no long-term relationship between vocalizing and change in heart rate. Stallions’ heart rates did not differ between the first and second halves of the 10-min mare presentation (Wilcoxon test, N ⫽ 15, z ⫽ 1.19, p ⫽ .23), suggesting no habituation. Also, the latency duration to produce the first call after spotting the female (178 ⫾ 52 s) was not correlated to the average heart rate of the stallion in that time window (Spearman test, N ⫽ 15, R ⫽ ⫺0.09, p ⫽ .76). Last, the difference between the overall heartbeat rate measured during the 10-min encounter (HB10m) and the baseline heartbeat measured just before meeting with the mare (HBc), reflecting the overall increase of arousal, did not predict the number of vocalizations emitted (N ⫽ 15, R ⫽ ⫺0.12, p ⫽ .65).
This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
TENSENESS RELAXED BY WHINNYING
Figure 1.
313
Sonogram of a typical stallion’s whinny.
Third, we found a short-term relationship between vocalizing and change in heart rate. Heart rates were subject to significant variations according to the timing of call utterances (Friedman test: HB10m/HB5s/HB-5s, N ⫽ 15, 2 ⫽ 14.93, p ⫽ .0006). Stallions’ heart rates were higher during the 5 s preceding whinnying (HB5s: 102.38 ⫾ 8.2 bpm) than during the 5 s a whinny was emitted (HB5s: 96.02 ⫾ 8.2 bpm) (Wilcoxon test, N ⫽ 15, z ⫽ 3.41, p ⫽ .0007) and also higher than the overall heartbeat rate measured during the 10-min encounter with the mare (HB10m, N ⫽ 15, z ⫽ 2.39, p ⫽ .017) (see Figure 2). Heart rates after starting calling (HB5s) did not differ significantly from this overall heartbeat rates (HB10m) (N ⫽ 15, z ⫽ 0.57, p ⫽ .57).
Discussion During an encounter with a mare that is out of reach, a stallion’s heart rate varied significantly in relation to his vocal activity. Just before calling, his heart rate accelerated but returned to baseline level while whinnying. Hence, calling can be seen as an emotional discharge following a sudden change in the stallion’s internal state, a reaction that may be mechanistically homologous to human crying and laughter. However, this emotional discharge is a shortterm (i.e., a few seconds) mechanism because no long-term (i.e., several minutes) effect of vocalizing was found here. An encounter between two conspecifics, especially if it is occasional and involves both sexes, is a source of arousal. Increase of heartbeat rates in socially exciting contexts is a well-known trait in humans and animals (Appelhans & Luecken, 2006; Christensen et al., 2008). Horses’ heartbeat rates recorded during our encounters were almost twice as high as their heart rates preceding mare presentation. This latter control measure was about the top of the range of typical rates found in horses at rest (26 – 42 bpm; Pilliner & Davies, 2004). Interestingly, the fact that our subjects’ heartbeat rates were higher during the 5 s preceding whinnying recalls the reactions of humans about to give a talk (Behnke & Sawyer, 2001). The relationship between humans’ sudden arousal changes and oral expression has been described. Arousal changes, notably in a frustrating or exciting context, also trigger unconscious oral expression such as swearing, laughing, or crying (Hirsch, 1985). Some arousal states, such as happiness and anger, are considered typically “talkative” emotions, in contrast to fear and sadness (Cosnier, 1994). Vocal expressions can be considered a human as well as an animal “reflex” for searching for social contact, because social encounters usually
trigger sudden increases of call rates (De Marco, Cozzolino, DessiFulgheri, & Thierry, 2011). Our stallions may have been frustrated during the distant (preventing physical contact) encounters with a mare or just sexually excited, inducing a sudden increase of heartbeat rate, followed by a vocalization enabling emotional regulation. The acoustic structures of whinnies support the pattern expected after comparison with human and nonhuman primate vocalizations following experiencing an intense arousal change, that is, long calls with a noisy frequency spectrum and marked energy pulses (Davila Ross, Owren, & Zimmermann, 2009; Lemasson et al., 2009). There is an open debate about the potential neurophysiological mechanisms underlying homeostasis and self-regulation of emotion. As mentioned earlier, it is possible that vocalizing enables an emotional discharge, fitting with Lorenz’s psychohydraulic model of motivation (Lorenz, 1950). In line with that idea, Takahashi, Narayanan, and Ghazanfar (2012) constructed a computational model of marmoset monkey vocal production, based on the interactions among three neural components: auditory, motor, and drive. On the basis of physiological and anatomical data, they envisioned these components as roughly representing the auditory cortex, motor cortex, and limbic system, respectively. Four steps are involved: (a) the neural activity in the drive component spontaneously increases until it reaches a threshold; (b) it activates the motor component, which will produce a call; and (c) the sound of this call increases activity in the auditory component, (d) which will then inhibit the drive component. How-
Figure 2. Stallions’ heartbeat rates preceding calling (HB-5s), during calling (HB5s), and overall (HB10m) (mean numbers per minute ⫾ SE) (Wilcoxon tests with Bonferroni correction: ⴱ p ⱕ .017, ⴱⴱ p ⱕ .003).
This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
314
LEMASSON, REMEUF, AND HAUSBERGER
ever, confirming the precalling accumulation of arousal up to a certain threshold would require measurements at a more precise temporal level (i.e., less than a second). The question would then be as follows: what happens when the threshold is reached and the animal cannot call? We believe that alternative behavioral expressions (e.g., body movement) would compensate and enable the emotional regulation. We also acknowledge that body movements, as well as their potential direct impact on heart rates, have not been scored here. However, the fact that those stallions were held by a caretaker limited locomotion anyway, especially because they were trained to remain immobile when on a halt. Several other self-regulation mechanisms have been discussed. First, calling, especially when emitting long vocalizations such as whinnies, is associated with a ventilation process, and it has been shown that cardiac and respiration rates are linked (Samet, Lambert, James, Mermier, & Chick, 1993). Second, physiological, including hormonal, measures (heart rate and prolactin, oxytocin, and cortisol concentrations) showed that singing has a clear effect on human well-being (i.e., release of emotional tension) (Grape, Sandgren, Hansson, Ericson, & Theorell, 2002). Also, data on surgically “devocalized” and sham-operated budgerigars indicated that the gonadal activity of males may be stimulated as a result of their own performance of vocal display rather than as a result of hearing such behavior by others (Brockway, 1967). Third, Riters (2011) reviewed the literature about the neural regulation of the motivation to sing in birds and highlighted different mechanisms in social-directed and undirected (self-directed?) sounds. Dopamine and opioid neuropeptides play a primary role in reward seeking and sensory pleasure in general but also in songbirds. Distinct patterns of dopamine activity influence the motivation to produce undirected and social-directed song. Undirected communication is intrinsically reinforced by immediate release of opioids induced by the act of singing. Directed communication is socially reinforced by opioids released as part of social interactions. Fourth, it was reported that in primates, a somatosensory feedback occurs during vocal production due to face and tongue movements (Ghazanfar, 2011). Hence, calling or being about to call is directly associated with changes similarly in a human and animal’s arousal state. This finding is in line with previous work that suggested that whinnying was a response to stress in a context of locomotor inhibition (Durier et al., 2012), as also used here. Perspectives for future work may deal with the relation between the type of emotion experienced and heart rate variability, as well as between the heart rate values and subsequent acoustic structures. For instance, it is unclear how vocalizations affect heart rate after experiencing a positive or a negative emotional change. Also, whinnies are basically composed of a long tonal introduction and a long atonal climax with repeated units. A more detailed investigation is needed to understand the relative influence of both acoustic structures on emotional regulation. Moreover, more comparative work is necessary to assess the evolutionary distribution of this mechanism in mammals. Finally, this finding opens new lines of theoretical research about the definition of the functions of vocal communication. Although the traditional definition stipulates that vocal signals are targeting one or several external receivers, one may also consider that vocalizing has a self-regulatory function (see also Owren et al., 2010). More generally, the impact of the communicative act on the performer has been largely understudied so far.
References Appelhans, B. M., & Luecken, L. J. (2006). Heart rate variability as an index of regulated emotional responding. Review of General Psychology, 10, 229 –240. http://dx.doi.org/10.1037/1089-2680.10.3.229 Behnke, R. R., & Sawyer, C. R. (2001). Patterns of psychological state anxiety in public speaking as a function of anxiety sensitivity. Communication Quarterly, 49, 84 –94. http://dx.doi.org/10.1080/ 01463370109385616 Boissy, A., & Le Neindre, P. (1997). Behavioral, cardiac and cortisol responses to brief peer separation and reunion in cattle. Physiology & Behavior, 61, 693– 699. http://dx.doi.org/10.1016/S0031-9384(96) 00521-5 Brockway, B. F. (1967). The influence of vocal behavior on the performer’s testicular activity in budgerigars (Melopsittacus undulatus). The Wilson Bulletin, 79, 328 –334. Christensen, J. W., Malmkvist, J., Nielsen, B. L., & Keeling, L. J. (2008). Effects of a calm companion on fear reactions in naive test horses. Equine Veterinary Journal, 40, 46 –50. http://dx.doi.org/10.2746/ 042516408X245171 Colonnello, V., Iacobucci, P., & Newberry, R. C. (2010). Vocal and locomotor responses of piglets to social isolation and reunion. Developmental Psychobiology, 52, 1–12. http://dx.doi.org/10.1002/dev.20406 Cosnier, J. (1994). La Psychologie des emotions et des sentiments. [The psychology of emotions and feelings]. Paris, France: Retz. Davila Ross, M., Owren, M. J., & Zimmermann, E. (2009). Reconstructing the evolution of laughter in great apes and humans. Current Biology, 19, 1106 –1111. http://dx.doi.org/10.1016/j.cub.2009.05.028 De Marco, A., Cozzolino, R., Dessì-Fulgheri, F., & Thierry, B. (2011). Collective arousal when reuniting after temporary separation in Tonkean macaques. American Journal of Physical Anthropology, 146, 457– 464. http://dx.doi.org/10.1002/ajpa.21606 Durier, V., Henry, S., Sankey, C., Sizun, J., & Hausberger, M. (2012). Locomotor inhibition in adult horses faced to stressors: A single postpartum experience may be enough! Frontiers in Psychology, 3, 442. http://dx.doi.org/10.3389/fpsyg.2012.00442 Gadziola, M. A., Grimsley, J. M. S., Faure, P. A., & Wenstrup, J. J. (2012). Social vocalizations of big brown bats vary with behavioral context. PLoS One, 7, e44550. http://dx.doi.org/10.1371/journal.pone.0044550 Gatchel, R. J., & Proctor, J. D. (1976). Effectiveness of voluntary heart rate control in reducing speech anxiety. Journal of Consulting and Clinical Psychology, 44, 381–389. http://dx.doi.org/10.1037/0022-006X.44.3 .381 Ghazanfar, A. A. (2011). The unity of the senses in primate vocal communication. In M. J. Murray & M. Wallace (Eds.), The neural bases of multisensory processes (pp. 653– 666). Boca Raton, FL: CRC Press. http://dx.doi.org/10.1201/9781439812174-41 Grape, C., Sandgren, M., Hansson, L. O., Ericson, M., & Theorell, T. (2002). Does singing promote well-being? An empirical study of professional and amateur singers during a singing lesson. Integrative Physiological & Behavioral Science, 38, 65–74. http://dx.doi.org/10.1007/ BF02734261 Hausberger, M., Fureix, C., Bourjade, M., Wessel-Robert, S., & RichardYris, M.-A. (2012). On the significance of adult play: What does social play tell us about adult horse welfare? Naturwissenschaften, 99, 291– 302. http://dx.doi.org/10.1007/s00114-012-0902-8 Hirsch, R. (1985). Swearing and the expression of emotions. In L. G. Andersson & R. Hirsch (Eds.), Perspectives on swearing (pp. 61– 82). Goteborg, Sweden: University of Goteborg. Lemasson, A., Boutin, A., Boivin, S., Blois-Heulin, C., & Hausberger, M. (2009). Horse (Equus caballus) whinnies: A source of social information. Animal Cognition, 12, 693–704. http://dx.doi.org/10.1007/s10071009-0229-9 Lemasson, A., Remeuf, K., Rossard, A., & Zimmermann, E. (2012). Cross-taxa similarities in affect-induced changes of vocal behavior and
This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
TENSENESS RELAXED BY WHINNYING voice in arboreal monkeys. PLoS One, 7, e45106. http://dx.doi.org/ 10.1371/journal.pone.0045106 Lorenz, K. Z. (1950). The comparative method in studying innate behavior patterns. In Society for Experimental Biology Symposium IV (Ed.), Physiological mechanisms in animal behavior (pp. 221–268). Oxford, UK: Academic Press. Marchant, J. N., Whittaker, X., & Broom, D. M. (2001). Vocalisations of the adult female domestic pig during a standard human approach test and their relationships with behavioural and heart rate measures. Applied Animal Behaviour Science, 72, 23–39. http://dx.doi.org/10.1016/S01681591(00)00190-8 Marx, G., Leppelt, J., & Ellendorff, F. (2001). Vocalisation in chicks (Gallus gallus dom.) during stepwise social isolation. Applied Animal Behaviour Science, 75, 61–74. http://dx.doi.org/10.1016/S0168-1591 (01)00180-0 McDonnell, S. M. (2005). Sexual behavior. In D. S. Mills & S. M. McDonnell (Eds.), The domestic horse: The origins, development, and management of its behavior (pp. 110 –125). London, UK: Cambridge University Press. Miller, M., & Fry, W. F. (2009). The effect of mirthful laughter on the human cardiovascular system. Medical Hypotheses, 73, 636 – 639. http:// dx.doi.org/10.1016/j.mehy.2009.02.044 Morton, E. S. (1977). On the occurrence and significance of motivationstructural rules in some bird and mammal sounds. American Naturalist, 111, 855– 869. http://dx.doi.org/10.1086/283219 Owren, M., Rendall, D., & Ryan, M. (2010). Redefining animal signaling: Influence versus information in communication. Biology and Philosophy, 25, 755–780. http://dx.doi.org/10.1007/s10539-010-9224-4 Pilliner, S., & Davies, Z. (2004). Equine science (2nd ed.). Oxford, UK: Blackwell. Riters, L. V. (2011). Pleasure seeking and birdsong. Neuroscience and Biobehavioral Reviews, 35, 1837–1845. http://dx.doi.org/10.1016/j .neubiorev.2010.12.017
315
Samet, J. M., Lambert, W. E., James, D. S., Mermier, C. M., & Chick, T. W. (1993). Assessment of heart rate as a predictor of ventilation. Research Report (Health Effects Institute), 59, 19 –55. Sankey, C., Richard-Yris, M.-A., Henry, S., Fureix, C., Nassur, F., & Hausberger, M. (2010). Reinforcement as a mediator of the perception of humans by horses (Equus caballus). Animal Cognition, 13, 753–764. http://dx.doi.org/10.1007/s10071-010-0326-9 Schehka, S., & Zimmermann, E. (2009). Acoustic features to arousal and identity in disturbance calls of tree shrews (Tupaia belangeri). Behavioural Brain Research, 203, 223–231. http://dx.doi.org/10.1016/j.bbr .2009.05.007 Schrader, L., & Todt, D. (1998). Vocal quality is correlated with levels of stress hormones in. domestic pigs (Sus scrofa domestica). Ethology, 104, 859 – 876. http://dx.doi.org/10.1111/j.1439-0310.1998.tb00036.x Steiner, H., Ryst, E., Berkowitz, J., Gschwendt, M. A., & Koopman, C. (2002). Boys’ and girls’ responses to stress: Affect and heart rate during a speech task. Journal of Adolescent Health, 30(Suppl.), 14 –21. http:// dx.doi.org/10.1016/S1054-139X(01)00387-1 Takahashi, D. Y., Narayanan, D., & Ghazanfar, A. A. (2012). A computational model for vocal exchange dynamics and their development in marmoset monkeys. IEEE International Conference on Development and Learning and Epigenetic Robotics, 2012, 1–2. Wolff, A., Hausberger, M., & Le Scolan, N. (1997). Experimental tests to assess emotionality in horses. Behavioural Processes, 40, 209 –221. http://dx.doi.org/10.1016/S0376-6357(97)00784-5
Received November 28, 2014 Revision received February 4, 2015 Accepted February 5, 2015 䡲
