Timing of the luteal-placental shift is delayed with additional fetuses in litter-bearing callitrichid monkeys, Saguinus oedipus and Callithrix jacchus.

The luteal-placental shift is an important milestone of mammalian pregnancy signifying when endocrine control of pregnancy shifts from the corpus luteum of the ovary to the placenta. The corpus luteum is maintained by chorionic gonadotropin (CG). Upon sufficient placental maturation, CG production wanes, the corpus luteum involutes, and control is shifted to the placenta, one consequence of which is a midgestational rise in glucocorticoid production, especially cortisol and cortisone, by both mother and fetus. Glucocorticoids are involved in initiating parturition, prenatal programming of offspring phenotype, and maturing fetal organs. Limited evidence from human pregnancy suggests that the timing of this shift is delayed in twin pregnancies, but little is known about the timing of the luteal-placental shift in litter-bearing monkeys from the primate family Callitrichidae. Here we provide evidence from cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus) of longer duration of elevated CG associated with multiple infant births compared to single births. Urinary profiles from cotton-top tamarins demonstrate that the decline of the extended elevation of CG precedes the onset of the midpregnancy sustained rise in glucocorticoids; this shift occurs later with an increase from one to two fetuses carried to term. In the common marmoset, the onset of the sustained rise of glucocorticoids in maternal urine is also delayed with an increase in infant number. Total urinary glucocorticoid levels during the last half of gestation increase monthly but do not differ by infant number. The significant delay in the luteal-placental shift suggests a longer period of placental maturation is needed to support a greater number of fetuses.

Nonhuman Primate Paternal Care: Species and Individual Differences in Behavior and Mechanisms.

Direct care of offspring by the father (sire) is relatively rare in primates. Besides humans, there are a number of species where the male is essential for the survival of offspring: marmosets, tamarins, titis and owl monkeys, some lemurs, and siamangs. All these species show reduced sexual dimorphism, territoriality, and biparental care. However, timing and levels of direct care may vary among these species. Here, relying on both lab and field data, we address the variability found in father's involvement with his infants, the behavioral, neuroendocrine and sensory systems that are a cause and consequence of paternal care, and social bonds between the breeding pair. We integrate studies of laboratory animals (where detailed observations and experimentation are possible) with field studies (which illuminate the ecological and evolutionary functions of paternal care) and discuss the future directions for examining the proximate and ultimate mechanisms of paternal care in nonhuman primates.

Vascular, cardiac, and renal lesions attributed to primary systemic hypertension in western pygmy marmosets (Cebuella pygmaea).

In a retrospective study of a western pygmy marmoset (Cebuella pygmaea) colony, postmortem examination of 1/8 juvenile and 29/47 adult animals identified vascular, cardiac, and renal lesions consistent with systemic hypertension. This included frequent renal arteriolar hypertrophy, hyaline and proliferative arteriolosclerosis, fibrinoid necrosis of arterioles, glomerulosclerosis, and nephrosclerosis. Affected animals ranged from 0.6 to 12 years of age (mean 6 years) and had an observed male predominance. Genealogical relatedness was evident in several breeding pairs and spanned multiple generations. Concurrent cardiac and renal disease was commonly identified, although frequently subclinical, and both were important causes of morbidity and mortality in affected animals. Cardiomegaly and hypertrophy were typical features and were accompanied by left atrial thrombosis in 10 animals. Signs of heart failure included chronic pulmonary edema in 20 cases and body cavity effusions in 17. In the kidneys, 19 cases had glomerular disease and hypertensive vasculopathy, and 26 cases had nephrosclerosis or glomerulosclerosis. Common extrarenal secondary causes of hypertension were excluded by necropsy examination. The pathogenesis is suggested to involve primary hypertension leading to renal and cardiac disease. Elevated sympathetic activity might be an underlying factor in the frequent development of primary systemic hypertension in the pygmy marmoset, as for the owl monkey.

Animal Signals, Music and Emotional Well-Being.

Playing music or natural sounds to animals in human care is thought to have beneficial effects. An analysis of published papers on the use of human-based music with animals demonstrates a variety of different results even within the same species. These mixed results suggest the value of tailoring music to the sensory systems of the species involved and in selecting musical structures that are likely to produce the desired effects. I provide a conceptual framework based on the combined knowledge of the natural communication system of a species coupled with musical structures known to differentially influence emotional states, e.g., calming an agitated animal versus stimulating a lethargic animal. This new concept of animal-based music, which is based on understanding animal communication, will lead to more consistent and specific effects of music. Knowledge and appropriate use of animal-based music are important in future research and applications if we are to improve the well-being of animals that are dependent upon human care for their survival.

Factors influencing the survival of wild cotton-top tamarin (Saguinus oedipus) infants.

Studies of cooperative breeding species have suggested that helpers are needed for infant survival and that helpers gain skills to successfully raise their own offspring. Studies of callitrichids in managed care and early field studies suggested that group size correlated with infant survival and that helpers needed to learn parental skills to be successful breeders. We present infant survival data from a 20-year field study of cotton-top tamarins (Saguinus oedipus) in Colombia involving 126 litters born to 41 females. There was no difference in the survival of male and female offspring to 6 months of age. However, litter size impacted survival, with triplet litters having lower survival and male triplets having lower survival than females. Loss of infants was highest in the first week of life and, of the animals remaining in the group at 6 months of age, 90% of them survived to 1 year. The mean length of time in the natal group was 2.3 years but some young migrated to other groups after 4 months of age. Group size and number of male helpers (>1 year) was not related to infant survival. However, groups with only one male had fewer surviving infants. Primiparous females had lower infant survival, but previous infant care experience by mothers as helpers had no effect on survival. A major cause of infant loss was group disruption due to deaths/evictions/loss of the reproductively active animals, or immigration of pregnant females. Thus, factors that cause a change in the stability of the reproductively active animals can disrupt group cohesion. Capture of individuals for the illegal pet trade, as well as habitat fragmentation, may increase competition between groups for access to territories and breeding opportunities. This may have long-term impacts to infant survival in this critically endangered species.

A century of the Journal of Comparative Psychology.

The Journal of Comparative Psychology, the oldest continuously published journal on animal behavior, has reached its centennial year. I examined each article published in the Journal over the past 100 years to document the changing roles of women and of international authors over the past century. The analysis also documented changes in the range of species and topics studied over the Journal's history. The Journal published the greatest number of articles in 1969, but as new journals appeared that focused on animal learning and behavioral neuroscience, the number of articles published decreased. In the past 35 years, since these other journals appeared, there has been a steady increase in the proportion of female authors and of authors working from outside North America. At the same time, the diversity of species and topics studied has increased. As a result, the Journal today is very different than it was 100 years ago. Comparative psychology appears to be thriving better in Europe and Asia than in North America, so maintaining a diversity of taxa studied and an international authorship and readership will be critical for the Journal's continued vitality. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Contextual complexity of chemical signals in callitrichids.

In nearly four decades our research and that of others on chemical signaling in callitrichid primates suggest a high degree of contextual complexity in both the use of signals and the response to these signals. We describe our research including observational field studies, behavioral bioassays ("playbacks"), functional imaging, and conditioning studies. Scent marking in both captivity and the wild is used for more than just territorial marking. Social contextual effects are seen in responses by subordinate females responding with ovulatory inhibition only to chemical signals from familiar dominant reproductive females. Males detect ovulation through changes in scent marks. Males responded behaviorally and hormonally to chemical signals of novel ovulating females as a function of their reproductive status (fathers, males paired with a female but not fathers, and single males). Multiple brain areas are activated in males by female chemical signals of ovulation including areas relating to memory, evaluation, and motivation. Furthermore, males can be conditioned to respond sexually to a nonsexual odor demonstrating that learning plays an important role in response to chemical signals. Male androgen and estrone levels changed significantly in response to infant chemical signals as a function of whether the males were fathers or not, whether the odors were from their own versus other infants, as well as the infant's stage of development. Chemical signals in callitrichids are providing a rich source of understanding the context and function of the chemical sensory system and its stimulation of neural, behavioral, and hormonal actions in the recipients.

Cognitive Components of Vocal Communication: A Case Study.

Communication among nonhuman animals is often presented as rigid and inflexible, reflecting emotional states rather than having any cognitive basis. Using the world's smallest monkey, the pygmy marmoset (Cebuella pygmaea), with the smallest absolute brain size amongst simian primates as a case study, I review the role of cognition in the development and usage of vocalizations in pygmy marmosets and present new data on the instrumental use of babbling and of food associated vocalizations. Pygmy marmosets have several contact calls that differ in the psychoacoustic properties for sound localization as well as the distance at which they carry through the rainforest. Marmosets use these calls strategically based on distance from neighbors. Marmosets alter spectral and temporal aspects of call structure when exposed to new groups and when newly mated. They display population specific vocal dialects. Young pygmy marmosets engage in extensive babbling behavior rewarded by parents that helps the young develop adult vocal structures, but older monkeys also use babbling instrumentally in conflict situations. Specific food referential calls generally relate to food preferences, but food calls are suppressed in the presence of animate prey. Unmated animals systematically combine a long distance call with food calls as though advertising for mates. Taken together, these examples show that even small brained primates use their vocal signals flexibly and strategically in response to a variety of environmental and social conditions.

Stick-weaving: Innovative behavior in tamarins (Saguinus oedipus).

Some captive cotton-top tamarins spontaneously weave sticks in the mesh of their enclosures so that the stick is lodged between two mesh openings. Sticks are broken from natural branches placed in the enclosures and often modified by biting them in the center before weaving through the mesh. To investigate this further, we systematically surveyed all animals in our colony and found that all successful stick-weaving tamarins were descendants from only 2 of the 16 breeding groups contributing to the colony membership at the time of surveying or were the mates of these descendants, suggesting stick-weaving is a socially learned behavior. Successful stick-weavers were presented with pipe cleaners, soda straws, and wooden dowels to see if they would generalize stick-weaving to novel objects. Seven of 10 animals successfully wove with straws or pipe cleaners, showing that they could generalize the behavior to objects that were physically different but had the same affordances as the sticks. Data from a father-daughter pair suggest a form of coaching. Innovative behavior is needed for the emergence of culture with subsequent social transmission. Although innovative behavior in primates is mainly associated with foraging and is more likely to occur among males, stick-weaving has no obvious reward and appeared equally in both sexes. Stick-weaving behavior and its probable social transmission across generations suggest the possibility of cultural traditions emerging in this species. (PsycINFO Database Record

Non-human primates avoid the detrimental effects of prenatal androgen exposure in mixed-sex litters: combined demographic, behavioral, and genetic analyses.

Producing single versus multiple births has important life history trade-offs, including the potential benefits and risks of sharing a common in utero environment. Sex hormones can diffuse through amniotic fluid and fetal membranes, and females with male littermates risk exposure to high levels of fetal testosterone, which are shown to have masculinizing effects and negative fitness consequences in many mammals. Whereas most primates give birth to single offspring, several New World monkey and strepsirrhine species regularly give birth to small litters. We examined whether neonatal testosterone exposure might be detrimental to females in mixed-sex litters by compiling data from long-term breeding records for seven primate species (Saguinus oedipus; Varecia variegata, Varecia rubra, Microcebus murinis, Mirza coquereli, Cheirogaleus medius, Galago moholi). Litter sex ratios did not differ from the expected 1:2:1 (MM:MF:FF for twins) and 1:2:2:1 (MMM:MMF:MFF:FFF for triplets). Measures of reproductive success, including female survivorship, offspring-survivorship, and inter-birth interval, did not differ between females born in mixed-sex versus all-female litters, indicating that litter-producing non-human primates, unlike humans and rodents, show no signs of detrimental effects from androgen exposure in mixed sex litters. Although we found no evidence for CYP19A1 gene duplications-a hypothesized mechanism for coping with androgen exposure-aromatase protein evolution shows patterns of convergence among litter-producing taxa. That some primates have effectively found a way to circumvent a major cost of multiple births has implications for understanding variation in litter size and life history strategies across mammals.

Fecal glucocorticoid metabolite responses to management stressors and social change in four species of callitrichine monkeys.

The use of enzyme immunoassays (EIA) for the non-invasive measurement of glucocorticoids provides a valuable tool for monitoring health and welfare in sensitive species. We validated methods for measuring fecal glucocorticoid metabolites (FGM) using the response to veterinary exams for four species of callitrichine monkeys: golden lion tamarin (Leontopithecus rosalia, n = 7), callimico (Callimico goeldii, n = 2), pied tamarin (Saguinus bicolor, n = 2), and white-fronted marmoset (Callithrix geoffroyi, n = 2). Routine veterinary exams were performed for the golden lion tamarins and callimicos, but exams for the pied tamarins and white-fronted marmosets were prompted by the death of a social partner. Prior to veterinary exams, fecal markers were evaluated to allow collection of individual samples and estimate approximate gut transit times. Based on this assessment, individual markers were fed in the afternoon, and fresh morning fecal samples were collected throughout this study. Following a veterinary exam, FGM increased roughly 3- to 28-fold above baseline in all species. Although FGM for most species returned to baseline concentrations within 24-48 h, the marmosets exhibited a progressive increase in FGM after an exam in response to the death of a breeding female and subsequent hand-rearing of a neonate. Individual differences were noted in the callimicos and tamarins, with higher baseline FGM levels in females vs. males, although small sample size precluded a clear determination of sex differences. To our knowledge, this is the first study to measure FGM in callimicos and white-fronted marmosets and the first to compare FGM across callitrichine species. These findings highlight the broad applicability of this EIA to measure the stress response of callitrichine monkeys. The progressive increase in FGM in the marmosets during hand-rearing of a neonate suggests that care should be taken to minimize this disturbance as much as possible.

Music evolution and neuroscience.

There have been many attempts to discuss the evolutionary origins of music. We review theories of music origins and take the perspective that music is originally derived from emotional signals. We show that music has adaptive value through emotional contagion, social cohesion, and improved well-being. We trace the roots of music through the emotional signals of other species suggesting that the emotional aspects of music have a long evolutionary history. We show how music and speech are closely interlinked with the musical aspects of speech conveying emotional information. We describe acoustic structures that communicate emotion in music and present evidence that these emotional features are widespread among humans and also function to induce emotions in animals. Similar acoustic structures are present in the emotional signals of nonhuman animals. We conclude with a discussion of music designed specifically to induce emotional states in animals.

Variation in prolactin is related to variation in sexual behavior and contact affiliation.

Prolactin is associated with both maternal and paternal care and appears important in developing a bond between parent and infant. In contrast with oxytocin, another hormone important in infant care, there is scant information on the role of prolactin in maintaining adult heterosexual relationships. We present here the first results demonstrating a relationship between prolactin levels and sexual and contact affiliation behavior in a pair-bonded species. We studied cotton-top tamarins, a socially-monogamous, cooperatively-breeding primate. We measured chronic urinary prolactin levels over a four week period to include the entire female ovulatory cycle and correlated prolactin levels in males and females with simultaneous measures of contact affiliation and sexual behavior. Current mothers who were no longer nursing displayed lower amounts of sexual behavior and proximity than non-breeding females and also had marginally lower levels of prolactin. The prolactin levels of males and females were similar within pairs, and variation in prolactin levels for both sexes was explained both by the amount of sexual behavior and contact affiliation. The results parallel a previous study that compared oxytocin levels with sociosexual behavior in the same species, and supports the hypothesis that both prolactin and oxytocin are involved in pair-bonding as well as in infant care.

Both parents respond equally to infant cues in the cooperatively breeding common marmoset, Callithrix jacchus.

Although there has been great interest in the evolutionary approach to cooperative breeding species, few studies actually directly compare fathers and mothers on their motivation to parent offspring. We tested the responsiveness of common marmoset mothers and fathers to vocal and olfactory cues from their own and other infants using a two-chamber test apparatus designed to evaluate responses in the absence of competition from other caregivers within the family. We tested parentally experienced mothers and fathers living with young infants and former parents with no current offspring to address the following questions: (1) do mothers and fathers respond equally to sensory cues of infants; (2) do parents discriminate cues of their own offspring when the infants are highly dependent and when the infants are more independent; and (3) are parents responsive to both auditory and olfactory cues? Mothers and fathers reacted similarly in all tests. Parents responded equally to isolation calls from their own and unfamiliar dependent infants and there was minimal response to olfactory cues. Responses to infant vocal cues were significantly stronger when infants were dependent upon direct parental care. There was no difference in response between parents whose infants were no longer dependent and former parents with no current offspring. The results show that both parents are highly responsive to infant vocal cues when their own infants are dependent on parental care, supporting an effect of hormonal priming. However, parents only showed behavioural discrimination between vocalizations from their own and unfamiliar infants when their infants were mostly independent.

Normal hematologic and serum biochemical values of cotton-top tamarins (Saguinus oedipus).

We obtained whole-blood hematologic and serum biochemical values from 38 captive-bred cotton-top tamarins (Saguinus oedipus). Data were analyzed to determine the effect of sex on blood parameters. Significant differences between either the means or medians of male and female tamarins were found for creatinine, hematocrit, hemoglobin, RBC count, and PCV. These results establish baseline hematologic and serum biochemical values and provide a useful resource not previously available in the peer-reviewed literature for the clinical care of cotton-top tamarins, a critically endangered New World primate, in a captive setting.

Long-term memory for calls of relatives in cotton-top tamarins (Saguinus oedipus).

Recognition of relatives is important for dispersing animals to avoid inbreeding and possibly for developing cooperative, reciprocal relationships between individuals after dispersal. We demonstrate under controlled captive conditions that cotton-top tamarins (Saguinus oedipus) have a long-term memory for long calls of relatives from which they had been separated for periods ranging from 4 to 55 months. Tamarins responded with lower levels of arousal behavior to playbacks of long calls from current mates and from separated relatives compared to calls of unfamiliar, unrelated tamarins. Four tamarins had been out of contact with relatives for more than 4 years and still showed recognition as evidenced by low levels of arousal. Results could not be explained in terms of proximity to former relatives. Long-term memory for vocal signatures of relatives is adaptive and may be much more common than has been demonstrated.

Conditioned sexual arousal in a nonhuman primate.

Conditioning of sexual arousal has been demonstrated in several species from fish to humans but has not been demonstrated in nonhuman primates. Controversy exists over whether nonhuman primates produce pheromones that arouse sexual behavior. Although common marmosets copulate throughout the ovarian cycle and during pregnancy, males exhibit behavioral signs of arousal, demonstrate increased neural activation of anterior hypothalamus and medial preoptic area, and have an increase in serum testosterone after exposure to odors of novel ovulating females suggestive of a sexually arousing pheromone. Males also have increased androgens prior to their mate's ovulation. However, males presented with odors of ovulating females demonstrate activation of many other brain areas associated with motivation, memory, and decision making. In this study, we demonstrate that male marmosets can be conditioned to a novel, arbitrary odor (lemon) with observation of erections, and increased exploration of the location where they previously experienced a receptive female, and increased scratching in post-conditioning test without a female present. This conditioned response was demonstrated up to a week after the end of conditioning trials, a much longer lasting effect of conditioning than reported in studies of other species. These results further suggest that odors of ovulating females are not pheromones, strictly speaking and that marmoset males may learn specific characteristics of odors of females providing a possible basis for mate identification.

Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins.

Oxytocin plays an important role in monogamous pairbonded female voles, but not in polygamous voles. Here we examined a socially monogamous cooperatively breeding primate where both sexes share in parental care and territory defense for within species variation in behavior and female and male oxytocin levels in 14 pairs of cotton-top tamarins (Saguinus oedipus). In order to obtain a stable chronic assessment of hormones and behavior, we observed behavior and collected urinary hormonal samples across the tamarins' 3-week ovulatory cycle. We found similar levels of urinary oxytocin in both sexes. However, basal urinary oxytocin levels varied 10-fold across pairs and pair-mates displayed similar oxytocin levels. Affiliative behavior (contact, grooming, sex) also varied greatly across the sample and explained more than half the variance in pair oxytocin levels. The variables accounting for variation in oxytocin levels differed by sex. Mutual contact and grooming explained most of the variance in female oxytocin levels, whereas sexual behavior explained most of the variance in male oxytocin levels. The initiation of contact by males and solicitation of sex by females were related to increased levels of oxytocin in both. This study demonstrates within-species variation in oxytocin that is directly related to levels of affiliative and sexual behavior. However, different behavioral mechanisms influence oxytocin levels in males and females and a strong pair relationship (as indexed by high levels of oxytocin) may require the activation of appropriate mechanisms for both sexes.

Prosocial behaviour emerges independent of reciprocity in cottontop tamarins.

The cooperative breeding hypothesis posits that cooperatively breeding species are motivated to act prosocially, that is, to behave in ways that provide benefits to others, and that cooperative breeding has played a central role in the evolution of human prosociality. However, investigations of prosocial behaviour in cooperative breeders have produced varying results and the mechanisms contributing to this variation are unknown. We investigated whether reciprocity would facilitate prosocial behaviour among cottontop tamarins, a cooperatively breeding primate species likely to engage in reciprocal altruism, by comparing the number of food rewards transferred to partners who had either immediately previously provided or denied rewards to the subject. Subjects were also tested in a non-social control condition. Overall, results indicated that reciprocity increased food transfers. However, temporal analyses revealed that when the tamarins' behaviour was evaluated in relation to the non-social control, results were best explained by (i) an initial depression in the transfer of rewards to partners who recently denied rewards, and (ii) a prosocial effect that emerged late in sessions independent of reciprocity. These results support the cooperative breeding hypothesis, but suggest a minimal role for positive reciprocity, and emphasize the importance of investigating proximate temporal mechanisms underlying prosocial behaviour.