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.

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.

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.

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.

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.

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.

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.

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.

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).

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.

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.

Affective responses in tamarins elicited by species-specific music.

Theories of music evolution agree that human music has an affective influence on listeners. Tests of non-humans provided little evidence of preferences for human music. However, prosodic features of speech ('motherese') influence affective behaviour of non-verbal infants as well as domestic animals, suggesting that features of music can influence the behaviour of non-human species. We incorporated acoustical characteristics of tamarin affiliation vocalizations and tamarin threat vocalizations into corresponding pieces of music. We compared music composed for tamarins with that composed for humans. Tamarins were generally indifferent to playbacks of human music, but responded with increased arousal to tamarin threat vocalization based music, and with decreased activity and increased calm behaviour to tamarin affective vocalization based music. Affective components in human music may have evolutionary origins in the structure of calls of non-human animals. In addition, animal signals may have evolved to manage the behaviour of listeners by influencing their affective state.

Socially biased learning among adult cottontop tamarins (Saguinus oedipus).

We presented adult cottontop tamarins (Saguinus oedipus) with a novel foraging task that had been used previously to examine socially biased learning of juvenile observers [Humle & Snowdon, Animal Behaviour 75:267-277, 2008]. The task could be solved in one of two ways, and thus allowed for an analysis of behavioral matching between an observer and a skilled demonstrator (trained to use one of the two methods exclusively). Because the demonstrator was an adult in both this study and the juvenile study, the influence of the observer's age could be isolated and examined, as well as the behavior of demonstrators toward observers of different ages. Our main goals were to (1) compare adults and juveniles acquiring the same task to identify how the age of the observer affects socially biased learning and (2) examine the relationship between socially biased learning and behavioral matching in adults. Although adults spent less time observing the trained demonstrators than did juveniles, the adults were more proficient at solving the task. Furthermore, even though observers did not overtly match the behavior of the demonstrator, observation remained an important factor in the success of these individuals. The findings suggested that adult observers could extract information needed to solve a novel foraging task without explicitly matching the behavior of the demonstrator. Adult observers begged much less than juveniles and demonstrators did not respond to begging from adult. Skill acquisition and the process of socially biased learning are, therefore, age-dependent and are influenced by the behavioral interactions between observer and demonstrator. To what extent this holds true for other primates or animal species still needs to be more fully investigated and considered when designing experiments and interpreting results.

Social dynamics and individual plasticity of infant care behavior in cooperatively breeding cotton-top tamarins.

Individual variation in infant caretaking behavior is prevalent among marmoset and tamarin monkeys. Although most group members participate in infant care, the timing and amount provided differs greatly. In this study, we quantified general trends in infant carrying behavior by using a longitudinal database that included 11 years of instantaneous scan observations following 80 births of cotton-top tamarins. Using detailed focal observations on a subset of the same families (10 births) we identified influences that affected expression of infant care at the group and individual levels. Fathers were the primary carriers and paternal carry time gradually decreased with increasing infant age. Paternal carry time also decreased significantly with an increasing number of older sibling helpers. Most fathers began to carry on the first day postpartum. However, we report circumstances in which fathers delayed carrying until almost a month postpartum. Fathers retrieved infants the most, although adult brothers' rates of retrievals peaked and surpassed fathers' rates during week 4 postpartum. Fathers delayed rejection of infants until week 4, whereas mothers rejected infants immediately and throughout the eight weeks. Nonetheless, infants climbed onto their mothers more than onto any other family member. Mothers showed a high initial investment in carrying during the first two weeks, decreasing quickly thereafter. Maternal contributions to infant carrying remained low and relatively consistent regardless of group size. However, mothers dramatically increased their infant carrying behavior in families in which fathers were absent. Older siblings cared for infants more than did younger siblings, and brothers retrieved and carried infants more than did sisters. Individual expression of infant care changed to accommodate infant needs and changed according to varying social dynamics and circumstances across litters.

Social influences on ant-dipping acquisition in the wild chimpanzees (Pan troglodytes verus) of Bossou, Guinea, West Africa.

We currently have little understanding of the influence of learning opportunity, whether social or environmental, and maternal role on tool-use acquisition in young wild chimpanzees. This study aims to fill this gap by focusing on the acquisition of ant-dipping among chimpanzees of Bossou, Guinea. Ant-dipping is a hazardous tool-use behaviour aimed at army ants (Dorylus spp.). Bossou chimpanzees target these ants both at nests (high risk) and trails (low risk) and employ two techniques to consume them: direct mouthing and pull-through. We present data for 13 mother-offspring pairs (1-10 years old). Mothers with young < or =5 years old dipped significantly more often at trails than at nests, thus minimizing the risk posed to themselves and their young. Infants thus benefited from better conditions to observe and practice ant-dipping. Mothers also varied greatly in their percent time spent ant-dipping and offspring differed in their learning opportunity. Our results suggest that high opportunity young started to observe and perform ant-dipping sooner and were better at ant-dipping than low opportunity young. Although mothers and weaned offspring correlated positively in their percent time spent dipping and proficiency, they did not match in technique used or tool length. Finally, we propose that the learning trajectory of young may predict individual and sex differences in adulthood. This study demonstrates the important role of mothers and learning opportunity in the acquisition of a hazardous tool-use behaviour and suggests that chimpanzee material culture is a product of a complex interaction between social processes and ecological factors.

Cooperatively breeding cottontop tamarins (Saguinus oedipus) do not donate rewards to their long-term mates.

This study tested the hypothesis that cooperative breeding facilitates the emergence of prosocial behavior by presenting cottontop tamarins (Saguinus oedipus) with the option to provide food rewards to pair-bonded mates. In Experiment 1, tamarins could provide rewards to mates at no additional cost while obtaining rewards for themselves. Contrary to the hypothesis, tamarins did not demonstrate a preference to donate rewards, behaving similar to chimpanzees in previous studies. In Experiment 2, the authors eliminated rewards for the donor for a stricter test of prosocial behavior, while reducing separation distress and food preoccupation. Again, the authors found no evidence for a donation preference. Furthermore, tamarins were significantly less likely to deliver rewards to mates when the mate displayed interest in the reward. The results of this study contrast with those recently reported for cooperatively breeding common marmosets, and indicate that prosocial preferences in a food donation task do not emerge in all cooperative breeders. In previous studies, cottontop tamarins have cooperated and reciprocated to obtain food rewards; the current findings sharpen understanding of the boundaries of cottontop tamarins' food-provisioning behavior.

Dialects in pygmy marmosets? Population variation in call structure.

Population variation in primate vocal structure has been rarely observed. Here, we report significant population differences in the structure of two vocalizations in wild pygmy marmosets (Trills and J calls). We studied 14 groups of pygmy marmosets Callithrix (Cebuella) pygmaea pygmaea from five populations in northeastern Ecuador. We analyzed the acoustic structure of Trills and J calls recorded from two adult animals in each group through focal samples. Although individuals and groups within a population differed in call structure, we found consistent structural differences at a population level for Trills and J calls. Pair-wise comparisons for the two call types point to San Pablo and Amazoonico as the populations that differed the most, whereas Hormiga and Zancudococha showed the least differences. Discriminant function analysis indicates that calls from each population could be classified accurately at rates significantly above chance. Habitat acoustics, social factors and genetic drift may explain interpopulation vocal differences. This is the first evidence of within-subspecies vocal differences, or dialects, in wild populations of a neotropical primate species.

Spatial cues more salient than color cues in cotton-top tamarins (Saguinus oedipus) reversal learning.

Animals living in stable home ranges have many potential cues to locate food. Spatial and color cues are important for wild Callitrichids (marmosets and tamarins). Field studies have assigned the highest priority to distal spatial cues for determining the location of food resources with color cues serving as a secondary cue to assess relative ripeness, once a food source is located. We tested two hypotheses with captive cotton-top tamarins: (a) Tamarins will demonstrate higher rates of initial learning when rewarded for attending to spatial cues versus color cues. (b) Tamarins will show higher rates of correct responses when transferred from color cues to spatial cues than from spatial cues to color cues. The results supported both hypotheses. Tamarins rewarded based on spatial location made significantly more correct choices and fewer errors than tamarins rewarded based on color cues during initial learning. Furthermore, tamarins trained on color cues showed significantly increased correct responses and decreased errors when cues were reversed to reward spatial cues. Subsequent reversal to color cues induced a regression in performance. For tamarins spatial cues appear more salient than color cues in a foraging task.

Captive-born cotton-top tamarins (Saguinus oedipus) respond similarly to vocalizations of predators and sympatric nonpredators.

What types of cues do callitrichid primates use to detect and respond to predators? Do they respond to predator-specific cues or to more general cues? The evidence for these questions remains conflicting. We presented captive-born and reared cotton-top tamarins with no previous exposure to predators (or predator cues) with vocalizations from three potential predators of cotton-top tamarin in the wild (white hawk, jaguar, and tayra) and with vocalizations from sympatric nonpredators (black-faced antthrush and red howler monkey). Vocalizations from predators and from nonpredator mammals elicited equivalent arousal, fear, and vocal responses. Howler monkey roars produced the strongest responses. The results suggest that predator-naïve cotton-top tamarins do not recognize specific predator vocalizations, but may respond to vocal qualities (low-frequency, noisy sounds) that indicate large body size, threat, or aggression. On the other hand, tamarins responded much more strongly to the higher frequency calls from the hawk than the antthrush, suggesting another mechanism must also be involved. The failure of captive-reared tamarins to distinguish between vocalizations of predators and nonpredator mammals has important implications for reintroduction studies.

Changes in prolactin and glucocorticoid levels in cotton-top tamarin fathers during their mate's pregnancy: the effect of infants and paternal experience.

We have previously shown that paternally experienced cotton-top tamarin fathers (Saguinus oedipus) had significant increases in prolactin and glucocorticoids at the midpoint of their mate's pregnancy, whereas less experienced fathers showed prolactin increases only the month before offspring birth [Ziegler & Snowdon, Hormones & Behavior 38:159-167, 2000; Ziegler et al., Hormones & Behavior 45:84-92, 2004]. These results could be owing to differing paternal experience or from paternal care given to previous offspring. To test the relative role of infant cues and paternal experience in these hormonal changes, we paired four paternally experienced tamarin fathers with a novel, primiparous female and monitored hormone levels during their first pregnancy together. No fathers showed the significant mid-pregnancy increase in prolactin seen previously. However, all fathers showed increases in cortisol and significant peaks of corticosterone in mid-pregnancy. The increase in corticosterone was consistent with previous data occurring in each male during the same week or the week following the urinary cortisol increase shown by his mate. These data may suggest that the elevated mid-gestation prolactin seen previously in experienced males may be owing to the presence of offspring from the previous set of infants. In contrast, increased cortisol and corticosterone occurred independently of infant cues and may be related to previous paternal experience. We therefore conclude that both offspring presence and paternal experience contribute to the hormonal changes seen in experienced cotton-top tamarin fathers during their mate's pregnancy.