Christy L. Hoffman

Mother–infant interactions in free-ranging rhesus macaques: Relationships between physiological and behavioral variables

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 offsprings 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 offsprings HPA axis and brain serotonergic system.

Sex differences in survival costs of reproduction in a promiscuous primate

In sexually promiscuous mammals, female reproductive effort is mainly expressed through gestation, lactation, and maternal care, whereas male reproductive effort is mainly manifested as mating effort. In this study, we investigated whether reproduction has significant survival costs for a seasonally breeding, sexually promiscuous species, the rhesus macaque, and whether these costs occur at different times of the year for females and males, namely in the birth and the mating season, respectively. The study was conducted with the rhesus macaque population on Cayo Santiago, Puerto Rico. Data on 7,402 births and 922 deaths over a 45-year period were analyzed. Births were concentrated between November and April, while conceptions occurred between May and October. As predicted, female mortality probability peaked in the birth season whereas male mortality probability peaked in the mating season. Furthermore, as the onset of the birth season gradually shifted over the years in relation to climatic changes, there was a concomitant shift in the seasonal peaks of male and female mortality. Taken together, our findings provide the first evidence of sex differences in the survival costs of reproduction in nonhuman primates and suggest that reproduction has significant fitness costs even in environments with abundant food and absence of predation.

Mu-opioid Receptor (OPRM1) Variation, Oxytocin Levels and Maternal Attachment in Free-Ranging Rhesus Macaques Macaca mulatta

Understanding the genetic and neuroendocrine basis of the mother-infant bond is critical to understanding mammalian affiliation and attachment. Functionally similar nonsynonymous mu-opioid receptor (OPRM1) SNPs have arisen and been maintained in humans (A118G) and rhesus macaques Macaca mulatta (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 cerebrospinal fluid 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.

Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques

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.

Immune function and HPA axis activity in free-ranging rhesus macaques

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.

Digit ratio (2D:4D) and dominance rank in female rhesus macaques ( Macaca mulatta )

Female rhesus macaques exhibit matrilineal dominance structures, and high dominance rank confers fitness benefits across a lifetime and across generations. Rank effects are “inherited” through social processes that are well understood; however, biological mechanisms that might impact these processes are not well known. Recently, it has been shown that prenatal androgens appear to be implicated in supporting dominance rank hierarchies in some mammals. In humans, interindividual differences in the second (index) to fourth (ring) digit ratio (2D:4D) have been linked indirectly to variation in prenatal androgens, with low 2D:4D in both sexes associated with higher inferred prenatal androgen effects. 2D:4D has also been related to dominant social behavior and has been shown to co-vary with social systems across nonhuman primate species. Here, we investigate how 2D:4D co-varies with socially inherited dominance rank in female rhesus macaques. Low 2D:4D was associated with higher-ranking females, while higher 2D:4D was associated with lower-ranking females. Similar relationships were also shown between ranked families within matrilines. This is the first study to show such a relationship between 2D:4D and dominance rank in a nonhuman primate and suggests that prenatal androgen effects could be involved in the maintenance of dominance rank in female cercopithecine primates.

Behavior and Social Dynamics of Rhesus Macaques on Cayo Santiago

Rhesus macaques are Asian primates with a current geographic distribution that encompasses many countries such as Afghanistan, India, Thailand, China, Pakistan, Bhutan, Burma, Nepal, Bangladesh, Laos, and Vietnam. They thrive in almost any type of habitat, including tropical forests, dry and semidesert regions, swamps, and mountains up to 4,000 m high. In some countries such as India, free-ranging rhesus macaques also live in highly populated urban areas including villages, towns, temples, and railway stations. Although rhesus macaques can be found in large numbers and, in many cases, are easily accessible for observations, studies of free-ranging rhesus macaques in Asia have mainly focused on population biology, demography, and geographic distribution and much less on behavior and ecology (e.g., Southwick and Siddiqi 1994).

One-Male Harems and Female Social Dynamics in Guinea Baboons

Little is known about the mating system and social organization of Guinea baboons. This study investigated whether Guinea baboons have a harem-based mating system similar to that of hamadryas and gelada baboons and whether one-male mating units also correspond to social units. Ten adult females in a captive multi-male multi-female group of Guinea baboons were focally observed 2 h per week for 12 weeks, and all observed copulations within the group were recorded. Some males copulated with a single female while others had harems of 2–4 females. All females copulated with a single male except 1 female that switched harems early in the study. The focal females had higher rates of social interaction with their harem members, especially their harem male, than with individuals outside the harem. Females appeared to be subordinate to the harem male but little or no physical aggression or herding behavior from the male was observed. Variation in female social interactions within the harem was not accounted for by their sexual interactions with the male or their genetic relatedness with the females. Females, however, appeared to maintain social relationships with their female relatives in other harems. Taken together, the results of this study show that both mating and affiliative interactions in Guinea baboons are concentrated within one-male units and that the social dynamics within and between these units share some similarities as well as differences with those of hamadryas and gelada baboons.

Costs of Reproduction Among Rhesus Macaque Females on Cayo Santiago

Reproduction is energetically costly for mammalian females during the periods of gestation and lactation and, consequently, is likely to be associated with reduced survival (Stearns 1989, 1992 ; Roff 2002), particularly when maternal condition is poor. Higher mortality may be associated with birth-related complications, but it also may be the consequence of elevated circulating levels of cortisol suppressing immune function (see McEwen et al. 1997, for a review). If the hypothalamic–pituitary–adrenal (HPA) axis is hyperactivated in post-partum females during prolonged periods as a result of either the energetic demands of lactation or the associated psychosocial stressors, immune function may become impaired, potentially making females more vulnerable to diseases and to increased risk of mortality.

Dogs on the Move: Factors Impacting Animal Shelter and Rescue Organizations’ Decisions to Accept Dogs from Distant Locations

Long-distance dog transfer programs are a topic of burgeoning interest in the animal welfare community, but little research has focused on such programs. This exploratory study, which surveyed 193 individuals associated with animal shelter and rescue organizations in the United States, evaluated factors that impacted organizations’ decisions to transfer in dogs over long distances (>100 miles) and assessed what criteria were commonly valued by destination organizations. Specifically, we examined the following aspects of long-distance transfer programs: (1) logistics of long-distance dog transfers; (2) factors impacting dog selection; (3) medical requirements; (4) partnerships formed between source and destination organizations; and (5) perceptions of long-distance dog transfer programs by individuals affiliated with the destination organizations. This study revealed that many logistical considerations factor into transfer decisions and the formation of healthy partnerships between source and destination organizations. Participants indicated their organization’s willingness to receive dogs of various sizes, coat colors and ages, but organizations often had restrictions regarding the breeds they would accept. Study findings indicate some organizations have strict quarantine policies and pre-transfer medical requirements, while others have no such requirements.