Nasal temperature drop in response to a playback of conspecific fights in chimpanzees: A thermo-imaging study
Graphical abstract
Chimpanzees dropped their nasal-tip temperature in response to the stimulus playback.
Introduction
Many researchers agree that emotion is, and will be, one of the central interests in the study of animal behavior [1], [2]. Yet, one barrier to the emotion studies in nonhuman animals is the scarcity of reliable, handy, and noninvasive tools to measure their physiological states [3]. In nonhuman primates, most of the previous studies used the directly-observable responses to infer the internal state of animals, such as facial expressions, bodily postures, vocalization, self-directed scratching, piloerection, and urination/defecation [as described in “ethograms” e.g. [4], [5]]. Endocrine responses, especially cortisol secretion through hypothalamus–pituitary–adrenal (HPA) axis, are also commonly used to measure stress levels in primates. Cortisol or cortisol metabolites can be measured in urine, feces, and saliva [6], [7], [8], [9], [10], [11], [12], [13]. These methods are noninvasive, and the sampling does not interfere with natural behaviors of animals; thus they are widely adopted in both laboratory and field studies. Currently lacking is a handy tool for measuring the activities of autonomic nervous system in nonhuman primates.
In humans, the autonomic-nervous-system (ANS) measures are commonly used to study emotion because these measures are well established and easily applicable, and are distinguishably related to a unique feeling, such as anger, fear, happiness, sadness [14], [15]. ANS is involved with the changes in heart-rate or heart-rate variability, pulse rate, blood pressure, pupil size, galvanic skin-conductance, respiratory rate, and skin temperature. ANS has two branches: the sympathetic nervous system (SNS) and the parasympathetic nervous system (PSNS), and these two systems typically act as antagonists. SNS is dominant when a body is preparing for impending risks/dangers while PSNS is dominant when a body is at rest [16], [17]. In nonhuman primates, several attempts were made to measure SNS activities to estimate their internal psychological states. Boysen and Berntson [18] used electrocardiogram to measure heart-rate of a young chimpanzee and found that they accelerated their heart-rate in response to the pictures of an aggressive conspecific. Berntson et al. [19] used the same method and found that chimpanzees decelerated their heart-rate in response to the pictures of familiar caretakers and the sounds of conspecific screams, presumably due to their increased attention to the stimuli. Aureli et al. [20] used the same technique (but wirelessly transmitted the signals to the recorder) to measure heart-rate of freely-moving macaques and found that the monkeys increased their heart-rate in response to the approaches by dominants. The monkeys decelerated their heart-rate faster during the receipt of grooming than matched control periods. Parr [21] used temperature transducer attached to a finger to measure the finger skin temperature of chimpanzees, and found that the finger temperatures dropped in response to a potentially threatening stimulus (a needle and a conspecific being injected with a needle). Although these studies were insightful, an unavoidable limit of their methods is that the subjects need to accept electrodes on their bodies. This typically results in a small number of testable (tolerant) subjects and a restricted movement of subject due to the attached electrodes (and cables).
Recent advance in thermo-imaging techniques offer a contact-free method of autonomic-nervous-system measures in humans and nonhuman primates and thus have potentials to handle with the above-mentioned issue. In humans, depending on the elicited emotion and the task nature, skin temperature changes in specific regions of face/body in a specific way [for a review, see Ioannou et al. [22]]. In general, negative emotion such as fear and stress decreases the nasal skin temperature primarily due to the reduced blood flow resulting from vasoconstriction of subcutaneous vessels in nasal skins [22]. Pain [23], startle [24], social pressure [e.g. public speech [25], accidental breaking of somebody's toy [26]], play [26], [27], empathy [e.g. seeing the person in a stress [28]], and the stress associated with task execution [e.g. driving [29], numeric task [30]] decreased the nasal (and perinasal) temperature. Sexual arousal, induced by intimate touch [31], interpersonal proximity and eye contact [32], and viewing erotic movies [23], caused the opposite effect; the increase in nasal (and perioral) temperature due to the increased blood flow. In monkeys, presentation of potentially fearful or stressful stimuli, such as a threatening experimenter, videos of screaming and threatening monkeys, caused the decrease in nasal temperature [3], [33]. In the same studies, behavioral responses and simultaneously-recorded galvanic responses of monkeys were correlated with the decrease in nasal temperature. Although the monkeys were restrained in chairs in these studies, a recent study [34] showed a possibility in using thermo-imaging with freely-moving monkeys. In great apes, there is no study that used thermo-imaging to examine their internal psychological states.
Therefore, in this study, we aimed to establish the procedures optimized to measure the facial temperature (with a particular focus on nasal areas) of great apes using thermo-imaging and then to estimate their psychological responses to social stimuli. We focused on chimpanzees, one of the most common species in the studies of cognition and emotion. We aimed to replicate and extend the results from Kuraoka and Nakamura [3] and Nakayama et al. [33], in which the tested monkeys showed the decrease in nasal temperature to potentially threatening stimuli. Specifically, (1) we aimed to establish the optimized procedures in two of the research facilities which noninvasively study apes, (2) to measure the change in nasal temperature when chimpanzees were hearing/watching various auditory and visual stimuli which differs in the degree of potential psychological impacts (e.g. conspecific fighting, conspecific resting, vs. no event) (3) to find the response and recovery speed of change in nasal temperature, (4) to find behavioral, hormonal, and heart-rate (HR)/heart-rate variability (HRV) correlates, and (5) to find the potential confounding factors that may have influenced the nasal temperature independently of the stimuli. We expected that, according to the results by Kuraoka and Nakamura [3], chimpanzees would show the decrease in nasal temperature in response to potentially threatening stimuli. The response and recovery speed should be moderate (e.g. detectable changes within 30 s after the stimulus onset/offset). The degree of temperature drop should depend on the potential psychological impacts of stimuli. During the presentation of potentially threatening stimuli, chimpanzees should exhibit the increase in excitement behavior, and the decrease in HRV as well as the decrease in nasal temperature. These changes (related to sympathetic nervous activation) may even lead to an activation of the HPA axis and an increase in salivary cortisol levels. The potential confounding factors should be any physical activities that trigger the sympathetic nervous activation [e.g. walking [35], food consumption [34], [36]] as well as the environmental temperature when/where the test would be conducted.
Section snippets
Experiment 1
Using playback stimuli, Experiment 1 examined the change in nasal temperature with nine chimpanzees in Germany. Chimpanzees were tested in three conditions, in which they heard 1) fighting vocalizations by groupmate individuals (screams and barks), 2) display calls by an allospecific individual, or 3) no sound in the testing room. As six of the tested chimpanzees were already trained to chew the oral swabs and return them to the experimenter on request, we additionally collected the saliva
Experiment 2
To answer the remaining questions raised above, we conducted an additional experiment in another research facility, Kumamoto Sanctuary, Japan. In this facility, a familiar experimenter can be in the same experimental booth with the chimpanzees, and therefore can control the chimpanzees to some extent on verbal commands and rewards (without physically restraining their bodies). With this unique set-up, Experiment 2 aimed to replicate and extend the results from Experiment 1. In each condition,
General discussion
We established thermo-imaging with chimpanzees at two of the research facilities differing in their experimental set-ups. We then characterized the psychological, physical, and environmental factors that affected their nasal temperature. In the WKPRC facility, the chimpanzees freely moved during the stimulus presentation. We thus conducted thermal measurements by attracting them to the mesh with pieces of food before and after the stimulus presentation. Chimpanzees showed the decrease in nasal
Acknowledgments
This study was conducted in part under the first author's postdoc program; the Japan Society for Promotion of Science (JSPS) for study abroad. FK and SH respectively received JSPS KAKENHI Grant Number 26885040 and 26245069. This study was also in part funded by JSPS MEXT KAKENHI Grant Number 24000001, JSPS-LGP-U04, JSPS core-to-core type A CCSN, and MEXT-PRI-Human Evolution. We thank Dr. Morimura and the keepers of Kumamoto Sanctuary, Kyoto University, Japan, and the keepers and interns of
References (70)
- et al.
The use of nasal skin temperature measurements in studying emotion in macaque monkeys
Physiol. Behav.
(2011) - et al.
Stress affects salivary alpha-amylase activity in bonobos
Physiol. Behav.
(2012) - et al.
Dynamics of social and energetic stress in wild female chimpanzees
Horm. Behav.
(2010) - et al.
Facial skin temperature decreases in infants with joyful expression
Infant Behav. Dev.
(2008) - et al.
Mother and child in synchrony: thermal facial imprints of autonomic contagion
Biol. Psychol.
(2012) - et al.
Decrease in nasal temperature of rhesus monkeys (Macaca mulatta) in negative emotional state
Physiol. Behav.
(2005) Meal-induced activation of the sympathetic nervous system and its cardiovascular and thermogenic effects in man
Physiol. Behav.
(2008)- et al.
Salivary cortisol in psychoneuroendocrine research: recent developments and applications
Psychoneuroendocrinology
(1994) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies
Anim. Behav.
(2005)- et al.
A simple method for distinguishing within-versus between-subject effects using mixed models
Anim. Behav.
(2009)