Personality research with non-human primates: theoretical formulation and methods

Since the earliest periods of primatology study, researchers have been aware of animals’ consistent individual differences in behavior or personality. Many papers have been published on this subject, but they lacked a common theoretical and methodological background. The present work is an attempt to provide such theoretical and methodological foundations to this field of biological science. In the theoretical formulation section, “biological study of personality” is first derived as an extension of the ethology paradigm, and non-human primate personality research is subsequently characterized as its strategic component. In the methodology section, brief reviews and discussions are presented on subjective and objective personality assessment methods with non-human primates with a reference to the reliability and validity concepts in human psychometrics. The work provides a theoretical framework and methodological suggestions for non-human primate personality research.     

Early behavioral development and temperamental traits in mother- vs peer-reared rhesus monkeys

Behavioral characteristics (“traits”) of 24 mother-reared and 24 nursery/peer-reared rhesus monkey infants were assessed via rating scales from the third through the seventh month of life while housed with their rearing partners, and from months 8–10 after all animals had been placed in novel peer groups. The animals were also tested at 8 months of age on the Bayley Scales of Infant Development adapted for nonhuman primates. During the early period effects noted were primarily developmental. Peer-reared animals were rated as increasingly less cautious and more attentive to the outside environment over time, while mother-reared infants declined in ratings of dependence on their mothers. All animals were rated as increasingly active and excitable, and less fearful, over time. For the period of months 8–10, peer-reared animals showed higher confidence ratings in month 10, and all animals showed a decline in attachment to cagemates. Mother-reared animals showed more hostility to the examiner during Bayley testing, whereas peer-reared animals showed more fear. Sex effects included greater ratings for independence from mothers, greater activity over both the early and later periods, greater excitability, greater attentiveness to the extra-cage environment, less cautiousness, and better performance on one Bayley problem for females.     

Infant temperament predicts life span in female rats that develop spontaneous tumors

In a recent study, we found that male rats that minimally explored a novel environment as infants died significantly faster than their more exploratory brothers. At death, these males had various complex pathologies, precluding identification of specific hormonal mechanisms underlying adult disease progression and mortality. To minimize the variance of disease processes at the end of life, we conducted a longitudinal study with female Sprague-Dawley rats prone to high rates of spontaneous mammary and pituitary tumors. For females that developed either mammary or pituitary tumors, those that had been neophobic (least exploratory) as infants died approximately 6 months earlier than their neophilic (most exploratory) sisters. In the case of mammary tumors, both benign and malignant, neophobic females developed palpable tumors earlier than neophilic females, whereas the interval between first palpation and death was the same for all females, indicating psychosocial regulation of early rather than later stages of the disease. Neophobic females' ovarian function aged more rapidly than their neophilic sisters. Concomitantly, they had lower corticosterone responses to restraint in late adulthood, ruling out high estrogen or corticosterone levels during senescence as causal factors in their accelerated mortality. During puberty, when mammary tissue is proliferating and differentiating, neophobic females experienced more irregular cycles with prolonged "luteal" phases, suggesting a role for prolactin, prolonged progesterone and fewer estrogen surges during this sensitive period for mammary tumor risk. Thus, we identified prolactin, estrogen, progesterone and possibly corticosterone dynamics as candidates for neuroendocrine mechanisms linking infant temperament with onset of adult neoplastic disease.     

The effect of early human contact and the separation method from the dam on responses of beef calves to humans

The objectives of this experiment were to evaluate the effect of early human contact and of the separation method from the dam on the future relationships of calves with humans, and to investigate the relationship between dam responses and calf responses. Thirty-three Salers calves aged 2–4 days old and reared outdoors were split into 3-week treatments balanced according to sex and birth dates. Group 1 (long separation from the dam and human contact: LS + H; n = 11) underwent 8 h of separation from the dam per day and 5 min of individual stroking; group 2 (short separation from the dam and human contact: SS + H; n = 11) underwent 1 h of separation and the same amount of human contact as LS + H calves. Group 3 (short separation from the dam and no human contact: SS − H; n = 11) was a control group undergoing the same duration of separation as SS + H but without stroking. At 3, 15 and 45 weeks of age, the calves were tested in a standard arena test (AT) where they were successively left alone (2 min), left with a stationary human (5 min), and left with a human approaching and touching them (2 min). At 15 and 45 weeks, the calves were also tested with the standard docility test (DT: test of restraint). The dams were also tested with DT 2 months before calving. Data analysis via Mann–Whitney tests and Spearman's correlations showed no significant effect of the duration calves were separated from their dams. Just after treatment at 3-week of age, calves given stroking (LS + H and SS + H) were more motionless and more willing to accept human contact (AT: touching) than control calves (SS − H, P < 0.01). At 45 weeks of age, calves given stroking spent also significantly more time (P < 0.05) motionless with the approaching human compared to non-stroked calves (SS − H), suggesting a persistent effect. However, this effect was not reproduced on the other behavioural criteria recorded (e.g., duration of human contact or docility score). In the different tests and at the different ages, the docility scores of the dams were significantly correlated (up to 0.7, P < 0.01) with behaviour towards humans shown by stroked calves but not non-stroked calves (SS − H). Our results suggest that additional human contact at early age, but not duration of the separation from the dam, could be beneficial for the human–animal relationship, but only for calves born to docile dams.     

Variation in aggressive behaviour in the poeciliid fish Brachyrhaphis episcopi: Population and sex differences

Aggression is often positively correlated with other behavioural traits such as boldness and activity levels. Comparisons across populations can help to determine factors that promote the evolution of such traits. We quantified these behaviours by testing the responses of wild-caught poeciliid fish, Brachyrhaphis episcopi, to mirror image stimuli. This species occurs in populations that experience either high or low levels of predation pressure. Previous studies have shown that B. episcopi from low predation environments are less bold than those that occur with many predators. We therefore predicted that fish from high predation populations would be more aggressive and more active than fish from low predation populations. However, we found the opposite - low predation fish approached a mirror and a novel object more frequently than high predation fish suggesting that ‘boldness’ and aggression were higher in low predation populations, and that population-level boldness measures may vary depending on context. When tested individually, low predation fish inspected their mirror image more frequently. Females, but not males, from low predation sites were also more aggressive towards their mirror image. Variation in female aggression may be driven by a trade-off between food availability and predation risk. This suggests that the relationship between aggression and boldness has been shaped by adaptation to environmental conditions, and not genetic constraints.     

Variability in vocal and behavioural responses to visual isolation between full-sibling families of beef calves

In order to assess the value of vocal response as an indicator of welfare in cattle, it is necessary to investigate factors which influence vocal behaviour of individuals, that are independent of the specific environmental conditions to which they are exposed. The effect of parental differences, sex, age and weight on vocal responses of calves to visual isolation were examined. The relationship between vocal response and the amount of body movement during isolation were also evaluated.

Seventeen full-sibling families of beef calves (N=130) were created by breeding five sires with 13 superovulated dams. Embryos were transferred into unrelated cows, which reared the calves to weaning age. Vocal response of calves and body movement were measured on four occasions, while they were visually isolated for 1 min on a single animal scale platform. The first two observations were made on the day of weaning (mean age 166 days) and the following day. At the third and fourth observations their average ages were 278 and 350 days, respectively. On the four occasions 33.3, 34.8, 27.8 and 38.6% of calves, respectively, vocalized. Both sire and family had a significant influence on the number of vocalizations and acoustic properties of the sounds. Electronically-measured movement while on the scale was also influenced by sire and family, but there was no relationship between vocal responses and body movement. There was a tendency (P=0.08) for older and therefore heavier calves to produce longer vocalizations. In the final observing session, age and weight were positively correlated with fundamental frequency and the sound pressure level at the frequency of greatest intensity, and negatively correlated with the loudest harmonic. At the last two observations, significantly more heifer calves than bull calves vocalized. There was little difference between the acoustic properties of heifers’ and bulls’ vocalizations.

The considerable individual variability in vocal response within a group of identically-treated calves is partly due to parental genetic influences that are independent of rearing and early experience. Other endogenous characteristics such as sex, age and weight also influence vocal response. But there is no clear relationship between individual temperament (as assessed by the amount of body movement during isolation) and characteristics of vocal response.     

Animal temperament and human disturbance: implications for the response of wildlife to tourism

Studies on the response of wildlife to human disturbance generally focus on demographic changes or on physiological and behavioural modifications directly related to stress response. Yet fewer studies have explored whether the distribution of individual animals in response to human disturbance is influenced by temperament. Temperament represents the consistency of responses of individuals in reaction to novel or challenging situations. Individuals are thus assumed to express highly consistent behaviour-hormonal response under specific stress conditions. In this study, we investigate the relations between exploration, grooming-scanning continuum, emotionality, and docility of individual Eastern chipmunks (Tamias striatus) and location of their burrow respective to frequentation by humans. We then assess the relationship between cortisol accumulated in the hair and both temperament and frequentation by humans. Explorative or docile chipmunks were more common in frequented areas. Hair cortisol increased with docility, but was not related to human frequentation. These results indicate that temperament may cause animals to distribute themselves in a non-random way in response to human disturbance. Integrating temperament into studies of the stress response of wildlife to humans could therefore help us understand the impact of tourism on wildlife.     

Behavioral and adrenocortical responses of male cynomolgus and lion-tailed macaques to social stimulation and group formation

Several recent studies indicate that primate species may differ in behavioral, and in some instances physiological, responses to social manipulations. These differences in response dispositions have been interpreted as being based on temperamental differences among species. This report extends previous comparative studies of macaques by describing behavioral contrasts observed between males of two macaque species, lion-tailed and cynomolgus macaques, in response to social manipulations. Males were exposed to a mirror, then visually exposed to conspecific neighbors in all pairwise combinations, and then formed into conspecific social groups. Urine samples were collected in the pairing and group formation conditions for cortisol assay. The cynomolgus demonstrated more affiliative behavior than the lion-tails in all conditions, while the lion-tails tended to exhibit more aggressive behavior. Following group formation cortisol values showed a decreasing trend in the cynomolgus, but not in the lion-tails. The cynomolgus rapidly adapted to group living and relations between them were primarily affiliative. In contrast, no affiliative behavior was ever observed in the lion-tail group, which appeared to be highly stressed by group living and was eventually disbanded.     

Quality of handling and holding yard environment, and beef cattle temperament: 2. Consequences for stress and productivity

This experiment assessed the effects of different quality and quantity of handling and quality of the holding yard environment on the productivity and physiological parameters indicative of stress in beef cattle. One-hundred-and-forty-four steers were given one of three human handling and yarding experiences on six occasions during a 12-month grazing period post-weaning (backgrounding): Good handling/yarding, Poor handling/yarding and Minimal handling/yarding. At the end of this phase the cattle were lot-fed for 78 days, with no handling/yarding treatments imposed, before being transported for commercial slaughter. Temperament was assessed by flight speed (FS) and a fear of humans (FOH) test, which measured the proximity to a stimulus person (ZA), the closest approach to the person (CA) and the amount the cattle moved around the test arena (TT). Mid-way through backgrounding, the Minimal treatment group was heavier than the Good, which was heavier than the Poor (mean weights 207, 201 and 194 kg, respectively; P = 0.05; LSD = 5.4), but by the end of backgrounding there was no difference between treatments and treatment did not affect liveweight during lot-feeding. At the end of backgrounding, plasma cortisol levels were significantly lower (P < 0.001) in the Good treatment group compared to the Poor and Minimal groups but at the end of lot-feeding there was no significant difference between the groups. Treatment affected plasma non-esterified fatty acid levels in backgrounding (P = 0.060) and lot-feeding (P = 0.046) with levels being higher in the Minimal than the Good and Poor groups (backgrounding: 0.52, 0.44 and 0.47 nmol/L, respectively; SE 0.02; lot-feeding: 0.46, 0.41 and 0.41 mmol/L, respectively; LSD = 0.05). Significant weak to moderate (r-value <0.50) negative correlations were found between FS and average daily gain, but there were no consistent correlations between measures from the FOH test and productivity. FS and TT were weakly positively correlated with plasma l-lactate, glucose and cortisol levels, and CA was weakly to moderately negatively correlated with l-lactate and glucose levels. The results indicate that, whilst being imposed, the Good treatment reduced stress and the Poor treatment negatively impacted on liveweight gain. Minimal handling/yarding appeared to cause the cattle to experience stress, perhaps because of the relative novelty of being handled and confined. This work also confirms previous findings that cattle with high FS have poorer liveweight gains under both pasture and feedlot conditions and FS has some value as a predictor of productivity. Correlations also indicated that agitated cattle show a heightened arousal and stress responses when being handled. Fear of humans, as assessed by ZA, CA and TT, did not adversely affect productivity.     

CIRCADIAN TYPOLOGY AND TEMPERAMENT AND CHARACTER PERSONALITY DIMENSIONS

The purpose of the present study is to explore the relationships between circadian typology and Cloninger’s model of the seven dimensions of personality, taking into account the possible sex interactions. This model considers four temperament dimensions (viz., HA, harm avoidance; NS, novelty seeking; RD, reward dependence; and PS, persistence) and three character dimensions (viz., SD, self-directedness; C, cooperativeness; and ST, self-transcendence). A sample of 862 university students (500 women), between 18 and 30 (21.94?±?2.64) yrs of age completed the short versions of the Temperament and Character Inventory (TCI-56) and the reduced Morningness-Eveningness Questionnaire (rMEQ). Women showed higher values for HA, RD, and C, while men showed higher values for NS. Evening-type subjects had higher NS but lower HA, PS, and SD scores. Moreover, circadian typology modulated the sex differences in HA and NS, and only evening-type men showed a lower HA score and higher NS score. Circadian typology is related to Cloninger’s model of Temperament and Character personality dimensions. Future studies should further examine possible implications, regarding both the vulnerability of developing psychopathological disorders and the prognosis of response to different treatments. (Author correspondence: aadan@ub.edu)