Charles T Snowdon

Charles T Snowdon
University of Wisconsin–Madison | UW · Department of Psychology

Ph.D.

About

271
Publications
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11,363
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Publications

Publications (271)
Article
To examine how precipitation patterns and climate change impact feeding choices made by a population of critically endangered cotton-top tamarins (Saguinus oedipus), we examined 22 years of feeding data (1999-2020) from 21 groups collected at Parque Natural Regional Bosque Seco El Ceibal Mono Tití in Santa Catalina, Colombia. We describe the diet a...
Article
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 o...
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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...
Article
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 s...
Article
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 st...
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I review the historical context in which the vervet alarm call papers first appeared, showing that animal behavior researchers at the time were studying a wide array of cognitive abilities in primate communication. I then review how the initial study on vervet alarms has led to research on referential alarm calls in other primates as well as in non...
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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 developmen...
Chapter
Family-living and pair-bonded primates, such as gibbons, night monkeys, titi monkeys, marmosets, and tamarins, have some different social and ecological challenges than other primates and thus display some differences in vocal communication. Shared parental care, territory defense, pair-bond maintenance, and frequent exchange of roles throughout th...
Chapter
Karen Strier is the leading primatologist in the Neotropics. She has made major contributions to socioecological theory, to conservation, and to education. Her long-term research on muriquis has led to many novel results and insights and challenged traditional theories. She has spear-headed conservation efforts that have led to significant protecti...
Article
A fundamental problem for understanding the evolution of human language has been the lack of significant parallels among nonhuman primates. Most researchers have focused on vocal plasticity—that is, the ability to learn novel sounds or modify call structure in response to social or environmental variables. Although songbirds, whales, dolphins, and...
Article
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 a...
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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 masculi...
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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 (Leo...
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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...
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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 emotion...
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Many studies have attempted to use music to influence the behavior of nonhuman animals; however, these studies have often led to conflicting outcomes. We have developed a theoretical framework that hypothesizes that in order for music to be effective with other species, it must be in the frequency range and with similar tempos to those used in natu...
Article
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 t...
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Reviews the book, Evolution and Human Sexual Behavior, by Peter B. Gray and Justin R. Garcia (see record 2013-22563-000 ). This book is a collaboration between a biological anthropologist and an evolutionary biologist, both of whom have worked extensively on human sexual behavior. The book provides a novel approach to human sexuality for many psych...
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Rhesus monkeys were offered sodium chloride (NaCl) in various concentrations before and during the imposition of a dietary sodium deficiency. No evidence of a preference-aversion curve for NaCl appeared, providing support for the “dilute-water” hypothesis explaining sodium preference-aversion curves in rats. (Rhesus monkeys have separate sensory ch...
Article
New World monkeys are less well known and less frequently studied than Old World monkeys and apes, yet they have value as models for speech and language. All New World primates are arboreal living in dense forests. This has led to a reliance on vocal communication rather than the visual signaling most common in Old World primates and apes. As a res...
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Reviews the book, Homo Mysterious: Evolutionary Puzzles of Human Nature by David P. Barash (see record 2012-16541-000 ). The book discusses a large number of unique traits of human nature such as female orgasm, homosexuality, and art, music, and literature. Barash addresses the evolutionary or adaptive hypotheses that have been proposed for each tr...
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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...
Chapter
Affiliations take many forms in the social relationships of both human and nonhuman primates. Which relationships are most important will vary as a function of the social structure and breeding system that is typical of a species and will also vary with life history stages within a species. For example, in species where males disperse and females r...
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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...
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To investigate the social roles of countermarking in dogs, we measured tail base position (TBP, a measure of social status), adjacent-marking and overmarking responses of male, nonoestrous female, gonadectomized male and gonadectomized female dogs to controlled presentations of urine from unfamiliar dogs and social groupmates. We also recorded dog...
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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 produ...
Article
This study examines the behavioral ecology of a chimpanzee population on Rubondo Island in Lake Victoria, Tanzania, over 40 years after chimpanzees were first introduced to the island from captivity. Despite little pre-release habitat assessment, rehabilitation, or post-release monitoring, these chimpanzees are one of the only released populations...
Article
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 behavior...
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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 (Sagu...
Article
The cotton-top tamarin (Saguinus oedipus oedipus) has an extensive vocal repertoire which is derived from the variation of two basic elements and the sequential combination of those elements. A distinctive features analysis demonstrated at least 8 phonetic variants of a short, frequency modulated call (chirp) and five longer constant frequency call...
Article
Long call vocalizations were recorded in the field from four adjacent subspecies of the saddle-back tamarin, Saguinus fusckollis ssp. Quantitative measurements of several call parameters were analyzed and four variables were found to be significantly different across subspecies. Each of the four subspecies had a distinctive set of long call paramet...
Article
This chapter reviews recent work on communication in nonhuman primates that supports considerable plasticity in production, usage, and understanding of signals. Although there is little direct evidence of vocal learning, signal structure can be altered in response to social, environmental, or developmental influences. Nonhuman primates have a sophi...
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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 t...
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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...
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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 t...
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Since 1996 we have studied eight populations of pygmy marmosets Cebuella pygmaea in northeastern Ecuador. Our data suggest that the habitat and diet specializations of pygmy marmosets make them particularly vulnerable to local extinction because of human activities. In periodical surveys we conducted of these populations, we found that pygmy marmos...
Article
In the biparental, cooperatively breeding cottontop tamarin, Saguinus oedipus oedipus, adult sons provide an energetically and reproductively valuable service to their breeding parents by helping to carry infants. Other species may use aggressive coercion or punishment to enforce alloparenting. Yet, affiliation in primates is important in negotiati...
Article
Little is known about social roles of urine marking and mark investigation in interpack communication in canids beyond mate acquisition, or of the influence of gonadal hormones on interpack urinary communication. We studied the responses of male and female, intact (nonoestrous) and gonadectomized Labrador retrievers to urine from unfamiliar dogs of...
Article
Clavulanic acid is a member of the beta lactam family of antibiotics with little or no intrinsic antibacterial activity of its own; instead, it is used to enhance the activity of antibiotics by blocking bacterial beta-lactamases. Because clavulanic acid by itself is very safe, orally active and shows good brain penetrance, we sought to determine if...
Article
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...
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Captive reintroductions often suffer high mortality, with predation as one source. Many species learn about predators; thus training captive-born animals to recognize predators may increase survivorship. We adapted variants of methods developed for birds to attempt to condition monkeys to mob a predator. Captive-reared cotton-top tamarins (Saguinus...
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Kelp gulls (Larus dominicanus) feed on the skin and blubber of southern right whales (Eubalaena australis) at Península Valdés, Argentina, notably affecting the whales' behavior. We have monitored the frequency of gull attacks from 1995 to 2008, and studied behavioral aspects of these interactions during the 1999 - 2001 right whale calving seasons....
Article
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 s...
Article
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...
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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 ripen...
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Common marmoset (Callithrix jacchus) males are bi-parental non-human primates that show extensive paternal behaviour. Fathers are in direct sensory contact with their infants during the natal period. We found that fathers exposed to isolated scents of their infant displayed a significant drop in serum testosterone levels within 20min after exposure...
Article
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...
Article
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,...
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Cooperation among non-human animals has been the topic of much theoretical and empirical research, but few studies have examined systematically the effects of various reward payoffs on cooperative behaviour. Here, we presented heterosexual pairs of cooperatively breeding cottontop tamarins with a cooperative problem solving task. In a series of fou...
Article
Our longitudinal study explored the role of socially biased learning in the acquisition of a novel foraging task that could be solved in two ways in captive juvenile cottontop tamarins. We trained parents to adopt a single solution (pole or ceiling strategy). We tested 13 different juvenile offspring–parent pairs on the task over the course of 11 w...
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The Evolution of Communication. Marc D. Hauser. Cambridge, MA: MIT Press, 1996. 760 pp.
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Callithrix jacchus infants are raised in complex family environments where most members participate in rearing the young. Many studies examining male parental behavior have focused on the carrying of infants with observations made within the family context. However, interference from family members can make it difficult to assess the father's motiv...
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Full-text available
Bergmüller et al. (2007) make an important contribution to studies of cooperative breeding andprovide a theoretical basis for linking the evolution of cooperative breeding with cooperativebehavior. We have long been involved in empirical research on the only family of nonhuman primatesto exhibit cooperative breeding, the Callitrichidae, which inclu...
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Mobbing is an important component of antipredator behavior for animals from many taxa. Callitrichids are small-bodied primates that mob multiple types of predators. Though there have been several observations of callitrichids mobbing predators in the wild, their anecdotal nature provides only rough descriptions of behavior and vocalizations. Resear...
Article
We investigated the development of food transfer and independent feeding in cotton-top tamarin (Saguinus oedipus) families. We studied the relationship between infant-directed vocalizations and food transfers on the development of independent feeding in infants. We experimentally tested ten infants (eight twins and two singletons) three times a wee...
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Full-text available
Mobbing is an important component of antipredator behavior for animals from many taxa. Callitrichids are small-bodied primates that mob multiple types of predators. Though there have been several observations of callitrichids mobbing predators in the wild, their anecdotal nature provides only rough descriptions of behavior and vocalizations. Resear...
Article
We examined seasonal patterns of fruit availability, dietary quality, and group size in the descendants of an introduced chimpanzee population on Rubondo Island, Tanzania. The site has supported a free-ranging population without provisioning for 40 years. Our goals were to determine whether Rubondo chimpanzees experience periods of fruit shortage,...
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Full-text available
Parenting patterns range widely among human and nonhuman primates. Rarely do single mothers parent without help. Many female-bonded species have female relatives (grandmothers and aunts) to help with infant care. In other species both parents assist in infant care, or there is cooperative care where several group members work together to rear a sin...
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We describe the role of social odours in sexual arousal and maintaining pairbonds in biparental and cooperatively breeding primates. Social odours are complex chemical mixtures produced by an organism that can simultaneously provide information about species, kinship, sex, individuality and reproductive state. They are long lasting and have advanta...
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Charles T Snowdon is Hilldale Professor of Psychology and Zoology at the University of Wisconsin-Madison, USA. His research has focused primarily on field and captive studies of cooperative breeding primates, the marmosets and tamarins, with emphasis on vocal and chemical communication and development, social learning, and behavioral and physiologi...
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Full-text available
Paternal behaviour is critical for the survival of offspring in many monogamous species. Common marmoset (Callithrix jacchus) and cotton-top tamarin (Saguinus oedipus) fathers spend as much or more time caring for infants than mothers. Expectant males of both species showed significant increases in weight across the pregnancy whereas control males...
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In socially tolerant settings, naïve individuals may have opportunities to interact jointly with knowledgeable demonstrators and novel tasks. This process is expected to facilitate social learning. Individual experience may also be important for reinforcing and honing socially acquired behaviours. We examined the role of joint interaction and indiv...
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Sex differences in behavior are quite common among nonhuman primates. In sexually monomorphic species, sex differences might be expected to be less evident than in polygynous and highly dimorphic species. Callitrichid primates (marmosets and tamarins) are cooperative breeders that exhibit little sexual size dimorphism. However, several sex differen...
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Local variations in fruit- and leaf-eating have been reported for some primate species; however, similar variations in exudate-feeding of pygmy marmosets, one of the most specialized neotropical primate species, have not been studied. In our 3-year study of four populations of pygmy marmosets in northeastern Ecuador, we characterized their exudate-...
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Full-text available
We investigated cooperative problem solving in unrelated pairs of the cooperatively breeding cottontop tamarin, Saguinus oedipus, to assess the cognitive basis of cooperative behaviour in this species and to compare abilities with other apes and monkeys. A transparent apparatus was used that required extension of two handles at opposite ends of the...
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Male mammals show rapid behavioral and hormonal responses to signals from sexually receptive females. However, rapid endocrine responses to female signals have not been observed in a nonhuman primate. Here, we tested the behavioral and hormonal response of male common marmosets (Callithrix jacchus) to isolated scent secretions from ovulatory female...