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1.  Do Dog Behavioral Characteristics Predict the Quality of the Relationship between Dogs and Their Owners? 
This paper explores whether dog behavioral characteristics predict the quality of the relationship between dogs and their owners (i.e., owner attachment to dog), and whether relations between dog behavior and owner attachment are moderated by demographic characteristics. In this study, N = 92 children and N = 60 adults from 60 dog-owning families completed questionnaires about their attachment to their pet dog, their level of responsibility for that dog, and their general attitudes toward pets. They also rated their dogs on observable behavioral characteristics. Individuals who held positive attitudes about pets and who provided much of their dog’s care reported stronger attachments to their dogs. The strength of owners’ attachments to their dogs was associated with dog trainability and separation problems. Relationships between owner attachment and both dog excitability and attention-seeking behavior were further moderated by demographic characteristics: for Caucasians but not for non-Caucasians, dog excitability was negatively associated with owner attachment to dog; and for adults, dog attention-seeking behavior was positively associated with owner attachment, but children tended to be highly attached to their dogs, regardless of their dogs’ attention-seeking behaviors. This study demonstrates that certain dog behavioral traits are indeed associated with the strength of owners’ attachments to their dogs.
PMCID: PMC4326091
attachment; attitudes; behavior; C-BARQ; dog
2.  Genetic and Environmental Influences on Individual Differences in Frequency of Play with Pets among Middle-Aged Men: A Behavioral Genetic Analysis 
Anthrozoos  2012;25(4):441-456.
There is growing evidence that pet ownership and human–animal interaction (HAI) have benefits for human physical and psychological well-being. However, there may be pre-existing characteristics related to patterns of pet ownership and interactions with pets that could potentially bias results of research on HAI. The present study uses a behavioral genetic design to estimate the degree to which genetic and environmental factors contribute to individual differences in frequency of play with pets among adult men. Participants were from the ongoing longitudinal Vietnam Era Twin Study of Aging (VETSA), a population-based sample of 1,237 monozygotic (MZ) and dizygotic (DZ) twins aged 51–60 years. Results demonstrate that MZ twins have higher correlations than DZ twins on frequency of pet play, suggesting that genetic factors play a role in individual differences in interactions with pets. Structural equation modeling revealed that, according to the best model, genetic factors accounted for as much as 37% of the variance in pet play, although the majority of variance (63–71%) was due to environmental factors that are unique to each twin. Shared environmental factors, which would include childhood exposure to pets, overall accounted for <10% of the variance in adult frequency of pet play, and were not statistically significant. These results suggest that the effects of childhood exposure to pets on pet ownership and interaction patterns in adulthood may be mediated primarily by genetically-influenced characteristics.
PMCID: PMC4286882  PMID: 25580056
genetics; pets; twins
3.  Is That Dog a Pit Bull? A Cross-Country Comparison of Perceptions of Shelter Workers Regarding Breed Identification 
Bull breeds are commonly kept as companion animals, but the pit bull terrier is restricted by breed-specific legislation (BSL) in parts of the United States and throughout the United Kingdom. Shelter workers must decide which breed(s) a dog is. This decision may influence the dog's fate, particularly in places with BSL. In this study, shelter workers in the United States and United Kingdom were shown pictures of 20 dogs and were asked what breed each dog was, how they determined each dog's breed, whether each dog was a pit bull, and what they expected the fate of each dog to be. There was much variation in responses both between and within the United States and United Kingdom. UK participants frequently labeled dogs commonly considered by U.S. participants to be pit bulls as Staffordshire bull terriers. UK participants were more likely to say their shelters would euthanize dogs deemed to be pit bulls. Most participants noted using dogs' physical features to determine breed, and 41% affected by BSL indicated they would knowingly mislabel a dog of a restricted breed, presumably to increase the dog's adoption chances.
PMCID: PMC4160292  PMID: 24673506
pit bull; breed identification; animal shelter
4.  Mu-opioid receptor (OPRM1) variation, oxytocin levels and maternal attachment in free-ranging rhesus macaques 
Behavioral neuroscience  2011;125(2):131-136.
Understanding the genetic and neuroendocrine basis of the mother-infant bond is critical to understanding mammalian affiliation and attachment. Functionally similar non-synonymous mu-opioid receptor (OPRM1) SNPs have arisen and been maintained in humans (A118G) and rhesus macaques (C77G). In rhesus macaques, variation in OPRM1 predicts individual differences in infant affiliation for mothers. Specifically, infants carrying the G allele show increased distress on separation from their mothers, and spend more time with them upon reunion, than individuals homozygous for the C allele. In humans, individuals possessing the G allele report higher perceptions of emotional pain on receiving rejection by social partners. We studied maternal behavior over the course of a year among free-ranging female rhesus macaques on Cayo Santiago, Puerto Rico. We then trapped females and collected blood samples, from which we assessed OPRM1 genotype; we also collected CSF samples from which we measured oxytocin (OT) levels. We show that females possessing the G allele restrain their infants more (i.e. prevent infants from separating from them by pulling them back) than females homozygous for the C allele. Females possessing the G allele also show higher OT levels when lactating, and lower OT levels when neither lactating nor pregnant, than females homozygous for the C allele. This is the first study to demonstrate an association between OPRM1 genotype and maternal attachment for infants, and is one of the first studies of any free-ranging primate population to link functional genetic variation to behavior via potentially related neuroendocrine mechanisms.
PMCID: PMC4018727  PMID: 21463018
mother-infant bond; opioids; oxytocin; functional genetics; attachment
5.  Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free-ranging female rhesus macaques 
American journal of primatology  2010;72(7):559-565.
The hypothalamic-pituitary-adrenal (HPA) axis modulates individuals’ physiological responses to social stress, which is an inevitable aspect of the daily lives of group-living animals. Previous nonhuman primate studies have reported that sex, age, rank and reproductive condition influence cortisol levels under stressful conditions. In this study we investigated cortisol responses to stress among 70 multiparous, free-ranging female rhesus macaques (Macaca mulatta) on the island of Cayo Santiago, PR. Plasma cortisol samples were collected in two consecutive years under similar conditions. Twenty-two females were sampled both years, and most of those females were lactating in only one of the years. Individual differences in cortisol levels were stable across years, even though reproductive condition changed for most individuals. No relationship was found between age or social rank and cortisol levels. Of the females that changed reproductive conditions, cortisol levels were higher when they were lactating than when they were cycling, and the amount of change in cortisol from cycling to lactating was greatest for low-ranking individuals. Heightened reactivity to stress during lactation may be the result of concerns about infant safety, and such concerns may be higher among low-ranking mothers than among higher ranking mothers. Psychosocial stress and hyperactivation of the HPA axis during lactation can suppress immune function and increase vulnerability to infectious diseases, thus explaining why adult females in the free-ranging rhesus macaque population on Cayo Santiago have a higher probability of mortality during the birth season than during the mating season.
PMCID: PMC4013499  PMID: 20039328
reproductive condition; cortisol; rank; rhesus macaques
6.  Mother–infant interactions in free-ranging rhesus macaques: Relationships between physiological and behavioral variables 
Physiology & behavior  2008;96(0):613-619.
Studies of mother–infant relationships in nonhuman primates have increasingly attempted to understand the neuroendocrine bases of interindividual variation in mothering styles and the mechanisms through which early exposure to variable mothering styles affects infant behavioral development. In this study of free-ranging rhesus macaques on Cayo Santiago, Puerto Rico, we aimed to: 1) compare lactating and nonlactating females to investigate whether lactation is associated with changes in plasma cortisol, prolactin and oxytocin, as well as changes in CSF levels of serotonin and dopamine metabolites (5-HIAA and HVA); 2) examine the extent to which interindividual variation in maternal physiology is associated with variation in maternal behavior; 3) examine the extent to which interindividual variation in infant physiology and behavior is accounted for by variation in maternal physiology and behavior. Lactating females had higher plasma concentrations of cortisol, prolactin, and oxytocin but lower CSF concentrations of HVA than nonlactating females. Variation in maternal rejection behavior was positively correlated with variation in maternal plasma cortisol levels and in CSF 5-HIAA levels while variation in the time spent nursing and grooming was associated with maternal plasma oxytocin levels. Infants who were protected more by their mothers had higher cortisol levels than those who were protected less, while infants who were rejected more had lower CSF 5-HIAA than infants who were rejected less. Since exposure to high levels of maternal protectiveness and rejection is known to affect the offspring’s behavior and responsiveness to the environment later in life, our results are consistent with the hypothesis that these effects are mediated by long-term changes in the activity of the offspring’s HPA axis and brain serotonergic system.
PMCID: PMC3955190  PMID: 19150451
Maternal behavior; Infant behavior; Cortisol; Monoamine neurotransmitters; Oxytocin; Prolactin; Rhesus monkeys
7.  Chronic stress, allostatic load, and aging in nonhuman primates 
Development and psychopathology  2011;23(4):1187-1195.
Allostatic load is the “wear and tear” of the body resulting from the repeated activation of compensatory physiological mechanisms in response to chronic stress. Allostatic load can significantly affect the aging process and result in reduced longevity, accelerated aging, and impaired health. Although low socioeconomic status is associated with high allostatic load during aging, the effects of status-related psychosocial stress on allostatic load are often confounded by lifestyle variables. Chronic psychosocial stress associated with low dominance rank in nonhuman primates represents an excellent animal model with which to investigate allostatic load and aging in humans. Research conducted with free-ranging rhesus monkeys suggests that female reproduction can also be a source of stress and allostatic load. Female reproduction is associated with increased risk of mortality and hyperactivation of the hypothalamic–pituitary–adrenal axis. Reproduction is especially stressful and costly for aging females of low rank. Although many indicators of body condition and neuroendocrine and immune function are influenced by aging, there are marked and stable individual differences among aging females in body condition, plasma cortisol responses to stress, and cytokine responses to stress. These differences are consistent with the hypothesis that there are strong differences in chronic stress among individuals, and that allostatic load resulting from chronic stress affects health during aging. Comparisons between captive and free-ranging rhesus monkey populations may allow us to understand how differences in environmental stress and allostatic load affect rates of aging, and how these in turn translate into differences in longevity and health.
PMCID: PMC3942660  PMID: 22018089
8.  Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques 
Hormones and behavior  2007;53(1):10.1016/j.yhbeh.2007.09.013.
Lactating female rats without their pups exhibit lower HPA responsiveness to stress than nonlactating females. However, responsiveness to stress is similar when lactating females are tested with their pups and the stressor involves a potential threat to the offspring. This study constitutes the first comparison of stress responsiveness in lactating and nonlactating female nonhuman primates. Subjects were 53 multiparous female free-ranging rhesus macaques. Approximately half of the females were lactating and half were nonpregnant/nonlactating. Blood samples were obtained after capture and after overnight housing in an individual cage. Lactating females were tested with their infants. Lactating females had significantly higher plasma cortisol levels than nonlactating females on both days. Having or not having an infant was also a better predictor of plasma cortisol levels among all females than their age, dominance rank, group of origin, time of day at which the sample was obtained, and time elapsed since beginning of the sampling procedure or since anesthesia. Plasma cortisol levels of lactating females were not significantly correlated with post-partum stage or with the cortisol levels of their infants. Capture, handling, and individual housing in a cage are powerful psychological stressors for free-ranging primates. We suggest that the higher plasma cortisol levels exhibited by lactating females reflect greater responsiveness to stress associated with perception of risks to infants. Hyporesponsiveness to stress may not be a general characteristic of lactation in all mammalian species, but a short-term effect of infant suckling that is most apparent with stressors unrelated to the offspring.
PMCID: PMC3859185  PMID: 17963759
Responsiveness to stress; Cortisol; Lactation; Infants; Humans; Nonhuman primates
9.  Effects of age on cerebrospinal fluid oxytocin levels in free-ranging adult female and infant rhesus macaques 
Behavioral neuroscience  2010;124(3):10.1037/a0019576.
There is growing interest in studying oxytocin biology in the context of social functioning in human and non-human primates. Studies of human subjects are typically restricted to peripheral oxytocin assessments because opportunities to collect cerebrospinal fluid (CSF) are rare. A few studies have examined CSF oxytocin levels in captive adult primates, but none to our knowledge have been conducted under free-ranging conditions and inclusive of young infants. The main goal of the present study was to establish feasibility of quantifying CSF oxytocin levels in free-ranging adult female and infant rhesus monkeys living on the island of Cayo Santiago, Puerto Rico. CSF oxytocin levels were examined in relation to individuals’ demographic and reproductive characteristics, as well as in relation to plasma cortisol levels. CSF oxytocin concentrations ranged from 36.02 to 134.41 pg/ml in adult females (ages 7–26 years; N = 31) and 35.94 to 77.3 pg/ml in infants (ages 38–134 days; N = 17). CSF oxytocin levels were positively correlated with adult female age and negatively correlated with infant age. The former correlation was driven by reproductive status. CSF oxytocin levels were unrelated to dominance rank or plasma cortisol levels. In contrast to a previous study of plasma oxytocin concentrations in this population, CSF oxytocin levels did not differ significantly between lactating and non-lactating females. In summary, these findings: 1) provide feasibility data for examining CSF oxytocin biology in free-ranging nonhuman primates and 2) indicate that CSF oxytocin levels may be a biomarker of age-related central nervous system changes across lifespan development. Although our study did not report significant associations between CSF oxytocin levels and socially-relevant demographic variables, the relationships between CSF oxytocin levels and assessments of social functioning warrant future investigation.
PMCID: PMC3859199  PMID: 20528088
Age; CSF; infant; cortisol; free-ranging; oxytocin; rhesus monkey
10.  Immune Function and HPA Axis Activity in Free-Ranging Rhesus Macaques 
Physiology & behavior  2011;104(3):507-514.
In mammals, the hypothalamic-pituitary-adrenal (HPA) axis and immune system play an important role in the maintenance of homeostasis. Dysregulation of either system resulting, for example, from psychosocial or reproductive stress increases susceptibility to disease and mortality risk, especially in aging individuals. In a study of free-ranging rhesus macaques, we examined how female age, reproductive state, social rank, and body condition influence (i) aspects of cytokine biology (plasma concentrations of interleukin-1 receptor antagonist (IL-1ra), IL-6 and IL-8), and (ii) HPA axis activity (plasma and fecal glucocorticoid levels). We also assessed individual differences in cytokine and hormone concentrations over time to determine their consistency and to investigate relations between these two indicators of physiological regulation and demand. Female monkeys showed marked increases in HPA axis activity during pregnancy and lactation, and increased circulating levels of IL-1ra with advancing age. Inter-individual differences in IL-1ra and IL-8 were consistent over successive years, suggesting that both are stable, trait-like characteristics. Furthermore, the concentrations of fecal glucocorticoid hormones in non-pregnant, non-lactating females were correlated with their plasma cortisol and IL-8 concentrations. Some individuals showed permanently elevated cytokine levels or HPA axis activity, or a combination of the two, suggesting chronic stress or disease. Our results enhance our understanding of within- and between-individual variation in cytokine levels and their relationship with glucocorticoid hormones in free-ranging primates. These findings can provide the basis for future research on stress and allostatic load in primates.
PMCID: PMC3133459  PMID: 21635909
rhesus macaque; cytokines; cortisol; aging; reproduction; allostatic load
11.  Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago 
Behavioral Ecology  2010;21(5):972-978.
Long-lived iteroparous species often show aging-related changes in reproduction that may be explained by 2 non-mutually exclusive hypotheses. The terminal investment hypothesis predicts increased female reproductive effort toward the end of the life span, as individuals have little to gain by reserving effort for the future. The senescence hypothesis predicts decreased female reproductive output toward the end of the life span due to an age-related decline in body condition. Nonhuman primates are ideal organisms for testing these hypotheses, as they are long lived and produce altricial offspring heavily dependent on maternal investment. In this study, we integrated 50 years of continuous demographic records for the Cayo Santiago rhesus macaque (Macaca mulatta) population with new morphometric and behavioral data to test the senescence and terminal investment hypotheses. We examined relationships between maternal age and activity, mother and infant body condition, interbirth intervals, measures of behavioral investment in offspring, and offspring survival and fitness to test for age-associated declines in reproduction that would indicate senescence, and for age-associated increases in maternal effort that would indicate terminal investment. Compared with younger mothers, older mothers had lower body mass indices and were less active, had longer interbirth intervals, and spent more time in contact with infants, but had infants of lower masses and survival rates. Taken together, our results provide strong evidence for the occurrence of reproductive senescence in free-ranging female rhesus macaques but are also consistent with some of the predictions of the terminal investment hypothesis.
PMCID: PMC2920293  PMID: 22475990
aging; life history; maternal investment; offspring fitness; reproductive senescence; rhesus macaques

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