All female primates incur energetic costs associated with producing and caring for offspring, but females belonging to the New World primate family Callitrichidae, the marmosets and tamarins, appear to face even further demands. In fact, the energetic demands of rearing callitrichid infants are thought to have led to the evolution of cooperative infant care in these species. If this explanation is true, then one might expect that natural selection should also have shaped patterns of maternal behavior to be sensitive to the costs of reproduction and equipped females to reduce their investment in offspring under certain conditions. Therefore, we examined the maternal effort and postpartum endocrine profiles of individual female marmosets (Callithrix kuhlii) across conditions that represented two hallmarks of callitrichid reproduction—conception during the early postpartum period and alloparental assistance. When females conceived during the early postpartum period and faced the upcoming demands of caring for their newly conceived litters (Study 1), they significantly reduced their caregiving effort and had significantly higher postpartum levels of estradiol relative to breeding attempts in which conception occurred later in the postpartum period. Postpartum estradiol was negatively correlated with maternal carrying effort. When experienced alloparents were present (Study 2), females again reduced their caregiving effort relative to breeding attempts in which experienced alloparents were not present. Postpartum cortisol, however, did not vary as a function of experienced alloparental assistance. The results of these studies suggest that female marmosets have been subjected to similar selection pressures as females of other primate taxa—to maximize their reproductive success by reducing their investment in offspring under the worst and best of conditions—and suggest that hormones may mediate within-female variation in maternal care. These studies also provide support for the notion that mothers are “flexible opportunists” when it comes to providing care to their young.
Wied’s black tufted-ear marmoset; Callitrichidae; Maternal care; Postpartum conception; Lactation; Alloparental care
The recent finding of a novel Epstein-Barr virus-related lymphocryptovirus (CalHV-3) in a captive colony of common marmoset (Callithrix jacchus) in the United States modifies the view that the host range of lymphocryptovirus is restricted to humans and Old World primates. We investigated the presence of Epstein-Barr virus-related viruses in 79 samples of New World monkeys caught in the wild, including six species of the Cebidae family and one of the Callitrichidae, living in the rain forest of French Guiana. Using a degenerate consensus PCR method for the herpesvirus DNA polymerase gene, we identified three novel lymphocryptoviruses from golden-handed tamarin (Saguinus midas) of the Callitrichidae family and squirrel monkey (Saimiri sciureus) and white-faced saki (Pithecia pithecia) of the Cebidae family. With the CalHV-3 strain, these three novel viruses constitute a well-supported phylogenetic clade in the Lymphocryptovirus genus, which is clearly distinct from the lineage of Old World lymphocryptovirus, hosted by catarrhine monkeys and humans. In tamarins, the prevalence of the novel lymphocryptovirus was more than 50%, indicating that it circulates well in the wild population, perhaps due to specific ecoethological patterns such as confrontations and intergroup migration. The detection and partial molecular characterization of the polymerase gene of three novel Gamma-1-Herpesvirinae from New World monkeys caught in the wild clearly indicate that free-ranging populations of platyrrhine are natural hosts of lymphocryptoviruses. Further characterization of these novel viruses will provide new insight not only into the origin and evolution of Gammaherpesvirinae but also into their pathogenicity.
Callitrichids, South American primates including marmosets and tamarins, have evolved a unique physiology. Twins share a placenta during gestation and exchange stem cells, resulting in naturally occurring chimeric adults. Our study used a quantitative PCR-based assay to address whether this chimerism was restricted to blood and other cells of the hematopoietic lineage or whether it extended to other somatic tissues. These studies help to characterize species that have adapted evolutionarily to pervasive chimerism, with every individual healthy and unperturbed. This experiment of evolution offers insight into transplantation and histocompatibility, reproductive biology and behavior, and innate and adaptive immunity.
Saguinus oedipus; Callithrix jacchus; hematopoiesis; quantitative pcr; animal models; transplantation; MHC
Free oligosaccharides are abundant components of mammalian milk and have primary roles as prebiotic compounds, in immune defense, and in brain development. Mass spectrometry-based technique is applied to profile milk oligosaccharides from apes (chimpanzee, gorilla, and siamang), new world monkeys (golden lion tamarin and common marmoset), and an old world monkey (rhesus). The purpose of this study was to evaluate the patterns of primate milk oligosaccharide composition from a phylogenetic perspective in order to assess the extent to which the compositions of hMOs derives from ancestral, primate patterns as opposed to more recent evolutionary events. Milk oligosaccharides were quantitated by nanoflow liquid chromatography on chip-based devices. The relative abundances of fucosylated and sialylated milk oligosaccharides in primates were also determined. For a systematic and comprehensive study of evolutionary patterns of milk oligosaccharides, cluster analysis of primate milk was performed using the chromatographic profile. In general, the oligosaccharides in primate milk, including humans, are more complex and exhibit greater diversity compared to the ones in non-primate milk. A detailed comparison of the oligosaccharides across evolution revealed non-sequential developmental pattern, i.e. that primate milk oligosaccharides do not necessarily cluster according to the primate phylogeny. This report represents the first comprehensive and quantitative effort to profile and elucidate the structures of free milk oligosaccharides so that they can be related to glycan function in different primates.
Primates; milk oligosaccharides; evolution; mass spectrometry; glycomics
Behavioral and endocrine suppression of reproduction in subordinate females produces the high reproductive skew that characterizes callitrichid primate mating systems. Snowdon et al. reported that the eldest daughters in tamarin families exhibit further endocrinological suppression immediately following the birth of siblings, and suggested that dominant females exert greater control over subordinate endocrinology during this energetically challenging phase of reproduction. We monitored the endocrine status of five Wied’s black tufted-ear marmoset daughters before and after their mother delivered infants by measuring concentrations of urinary estradiol (E2), pregnanediol glucuronide (PdG), testosterone (T), and cortisol (CORT). Samples were collected from marmoset daughters 4 weeks prior to and 9 weeks following three consecutive sibling-litter births when the daughters were prepubertal (M=6.1 months of age), peripubertal (M=11.9 months), and postpubertal (M=17.6 months). The birth of infants was associated with reduced ovarian steroid excretion only in the prepubertal daughters. In contrast, ovarian steroid levels tended to increase in the postpubertal daughters. Urinary E2 and T levels in the postpubertal daughters were 73.8% and 37.6% higher, respectively, in the 3 weeks following the birth of infants, relative to prepartum levels. In addition, peak urinary PdG concentrations in peri- and postpubertal daughters were equivalent to luteal phase concentrations in nonpregnant, breeding adult females, and all of the peri- and postpubertal daughters showed clear ovulatory cycles. Cortisol excretion did not change in response to the reproductive status of the mother, nor did the concentrations change across age. Our data suggest that marmoset daughters of potential breeding age are not hormonally suppressed during the mother’s peripartum period or her return to fertility. These findings provide an additional example of species diversity in the social regulation of reproduction in callitrichid primates.
callitrichid; cooperative breeding; marmoset; reproductive suppression; urinary steroids
Marmosets and tamarins are increasingly used in research, but their pathology remains poorly defined compared to old world primates.
Necropsy records of 129 marmosets and 52 tamarins were reviewed; none were used experimentally.
The most common marmoset lesions were dehydration, emaciation, nephritis, colitis and inanition. The most common tamarin lesions were dehydration, ascites, emaciation and congestive heart failure. Colitis and heart disease were the most common cause of death in marmosets and tamarins, respectively. Immature marmoset and tamarin deaths often occurred within the first month of life. Immature marmosets usually died from inanition, stillbirth and colitis; immature tamarins from atelectasis, stillbirth, heart failure and colitis. Lymphoma was the most common neoplasm for both marmosets and tamarins.
The findings were similar to prior reports with differences in frequency and severity. We report the first case of endometriosis in a marmoset.
nonhuman primate; Callitrichidae; disease; epidemiology; cancer
Bergmüller et al. (2007) make an important contribution to studies of cooperative breeding and provide a theoretical basis for linking the evolution of cooperative breeding with cooperative behavior. We have long been involved in empirical research on the only family of nonhuman primates to exhibit cooperative breeding, the Callitrichidae, which includes marmosets and tamarins, with studies in both field and captive contexts. In this paper we expand on three themes from Bergmüller et al. (2007) with empirical data. First we provide data in support of the importance of helpers and the specific benefits that helpers can gain in terms of fitness. Second, we suggest that mechanisms of rewarding helpers are more common and more effective in maintaining cooperative breeding than punishments. Third, we present a summary of our own research on cooperative behavior in cotton-top tamarins (Saguinus oedipus) where we find greater success in cooperative problem solving than has been reported for non-cooperatively breeding species.
Callitrichine primates (marmosets and tamarins) often remain in their natal groups beyond the time of sexual maturity. Although studies have characterized the development of female reproductive function in callitrichine offspring, less is known about the male reproductive development. To document reproductive development in male marmosets, we monitored urinary androgen (uA) excretion in males housed in a captive colony of white-faced marmosets (Callithrix geoffroyi). Young male marmosets showed relatively low and stable rates of uA excretion early in life, with elevated production at the end of the juvenile period (9–10 months) and again at the onset of adulthood (16 months). uA levels of adult breeding males were also measured to compare to adult-aged sons. Although breeding males did have higher uA levels than their adult-aged sons, these differences did not reach conventional levels of significance. Evidence from some other reports has suggested that androgen levels of males in other species are influenced by social factors, such as the presence of a sexually receptive female or of dependent offspring. In this study, however, uA levels did not vary, based on their mothers’ pregnancy status or the presence of younger siblings in the natal group. Patterns of androgen excretion in the white-faced marmoset roughly reflect those of other callitrichine species. Furthermore, unlike callitrichine daughters, gonadal activity in sons does not seem to be sensitive to within-group social cues.
testosterone; male sexual development; pregnancy status; social status; younger siblings presence
Marmosets are playing an increasingly large and important role in biomedical research. They share genetic, anatomical, and physiological similarities with humans and other primate model species, but their smaller sizes, reproductive efficiency, and amenability to genetic manipulation offer an added practicality. While their unique biology can be exploited to provide insights into disease and function, it is also important that researchers are aware of the differences that exist between marmosets and other species. The New World monkey family Callitrichidae, containing both marmoset and tamarin species, typically produces dizygotic twins that show chimerism in the blood and other cells from the hematopoietic lineage. Recently, a study extended these findings to identify chimerism in many tissues, including somatic tissues from other lineages and germ cells. This has raised the intriguing possibility that chimerism may play an increasingly pervasive role in marmoset biology, ranging from natural behavioral implications to increased variability and complexity in biomedical studies.
Using a quantitative PCR based methodology, Y-chromosomes can be reliably detected in the females with male fraternal twins allowing for a relative quantification of chimerism levels between individuals and tissues. With this approach in common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus), chimerism was detected across a broad array of tissues. Chimerism levels were significantly higher in tissues primarily derived from the hematopoietic lineage, while they were lower, though still detectable, in tissues with other origins. Interestingly, animals with a characteristic marmoset wasting disease show higher levels of chimerism in those tissues affected. Fibroblast cell lines from chimeric individuals, however, are not found to be chimeric themselves.
Taken together, the levels of chimerism in tissues of different origins coupled with other lines of evidence suggest that indeed only hematopoietic cell lineages are chimeric in callitrichids. The chimerism detected in other tissues is likely the result of blood or lymphocytic infiltration. Using molecular methods to detect chimerism in a tissue sample seems to have allowed a substantial increase in the ability to detect these minor cell populations.
Following a series of experiments in which six orangutans and one gorilla discriminated photographs of different animal species in a two-choice touch screen procedure, Vonk & MacDonald (2002) and Vonk & MacDonald (2004) concluded that orangutans, but not the gorilla, seemed to learn intermediate level category discriminations, such as primates versus non-primates, more rapidly than they learned concrete level discriminations, such as orangutans versus humans. In the current experiments, four of the same orangutans and the gorilla were presented with delayed matching-to-sample tasks in which they were rewarded for matching photos of different members of the same primate species; golden lion tamarins, Japanese macaques, and proboscis monkeys, or family; gibbons, lemurs (Experiment 1), and subsequently for matching photos of different species within the following classes: birds, reptiles, insects, mammals, and fish (Experiment 2). Members of both Great Ape species were rapidly able to match the photos at levels above chance. Orangutans matched images from both category levels spontaneously whereas the gorilla showed effects of learning to match intermediate level categories. The results show that biological knowledge is not necessary to form natural categories at both concrete and intermediate levels.
Gorilla; Matching; Orangutans; Biological categories; Concepts
Decision making often involves choosing between small, short-term rewards and large, long-term rewards. All animals, humans included, discount future rewards—the present value of delayed rewards is viewed as less than the value of immediate rewards. Despite its ubiquity, there exists considerable but unexplained variation between species in their capacity to wait for rewards—that is, to exert patience or self-control. Using two closely related primates—common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus)—we uncover a variable that may explain differences in how species discount future rewards. Both species faced a self-control paradigm in which individuals chose between taking an immediate small reward and waiting a variable amount of time for a large reward. Under these conditions, marmosets waited significantly longer for food than tamarins. This difference cannot be explained by life history, social behaviour or brain size. It can, however, be explained by feeding ecology: marmosets rely on gum, a food product acquired by waiting for exudate to flow from trees, whereas tamarins feed on insects, a food product requiring impulsive action. Foraging ecology, therefore, may provide a selective pressure for the evolution of self-control.
temporal discounting; impulsivity; rate maximization; tamarins; marmosets
Callitrichid hepatitis (CH) is an acute, often fatal viral infection of New World primates from the family Callitrichidae. The etiologic agent of CH is unknown. We report here the isolation of an arenavirus from a common marmoset (Callithrix jacchus) with CH by using in vitro cultures of marmoset hepatocytes and Vero-E6 cells. Enveloped virions 67 to 133 nm in diameter with ribosomelike internal structures were seen in infected cultures. Immunofluorescence and Western immunoblot analysis using CH-specific antisera (principally from animals exposed to CH during zoo outbreaks) revealed three antigens in cells infected with this CH-associated virus (CHV). These antigens had the same electrophoretic mobilities on sodium dodecyl sulfate-polyacrylamide gels as did the nucleocapsid, GP2, and GPC proteins of lymphocytic choriomeningitis virus (LCMV). Monoclonal antibodies specific for these arenavirus proteins also reacted with the three CHV antigens. Conversely, the CH-specific antisera reacted with the nucleocapsid, GP2, and GPC proteins of LCMV. CHV thus appears to be a close antigenic relative of LCMV. The serologic association of CHV with several CH outbreaks implicate it as the etiologic agent of this disease.
The Rosalia longicorn or Alpine longhorn (Coleoptera: Cerambycidae) is an endangered and strictly protected icon of European saproxylic biodiversity. Despite its popularity, lack of information on its demography and mobility may compromise adoption of suitable conservation strategies. The beetle experienced marked retreat from NW part of its range; its single population survives N of the Alps and W of the Carpathians. The population inhabits several small patches of old beech forest on hill-tops of the Ralska Upland, Czech Republic. We performed mark-recapture study of the population and assessed its distribution pattern. Our results demonstrate the high mobility of the beetle, including dispersal between hills (up to 1.6 km). The system is thus interconnected; it contained ∼2000 adult beetles in 2008. Estimated population densities were high, ranging between 42 and 84 adult beetles/hectare a year. The population survives at a former military-training ground despite long-term isolation and low cover of mature beech forest (∼1%). Its survival could be attributed to lack of forestry activities between the 1950s and 1990s, slow succession preventing canopy closure and undergrowth expansion, and probably also to the distribution of habitat patches on conspicuous hill-tops. In order to increase chances of the population for long term survival, we propose to stop clear-cuts of old beech forests, increase semi-open beech woodlands in areas currently covered by conifer plantations and active habitat management at inhabited sites and their wider environs.
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 individual experience in the acquisition of a novel foraging task in captive cottontop tamarins. The task involved learning how to locate and access two hidden food rewards from among 10 differently cued forage sites. Tamarins were tested in three different conditions: (1) individually, (2) while interacting with a naïve mate, and (3) while interacting with a mate trained as a knowledgeable demonstrator. For tamarins tested with mates present, we interspersed social input test days with exposure to the task while alone. Tamarins were tested again 17 months after their last exposure to the task, to assess long-term memory. All tamarins tested with knowledgeable demonstrators solved the task. In contrast, tamarins tested alone or with naïve mates had similarly high levels of neophobia and low levels of task acquisition. We conclude that joint interaction occurs in mated pairs of cottontop tamarins and facilitates the spread of novel behaviour. Interspersing test days with a knowledgeable demonstrator present and test days alone with the task helped tamarins to achieve the ultimate goal of the task: obtaining food rewards. Tamarins performed similarly when tested 17 months later, regardless of their initial learning environment. Tamarins had memory deficits for the location of hidden food rewards, but retained memory of the necessary motor actions and solved the task.
The potentiality to find precursors of human language in nonhuman primates is questioned because of differences related to the genetic determinism of human and nonhuman primate acoustic structures. Limiting the debate to production and acoustic plasticity might have led to underestimating parallels between human and nonhuman primates. Adult-young differences concerning vocal usage have been reported in various primate species. A key feature of language is the ability to converse, respecting turn-taking rules. Turn-taking structures some nonhuman primates' adult vocal exchanges, but the development and the cognitive relevancy of this rule have never been investigated in monkeys. Our observations of Campbell's monkeys' spontaneous vocal utterances revealed that juveniles broke the turn-taking rule more often than did experienced adults. Only adults displayed different levels of interest when hearing playbacks of vocal exchanges respecting or not the turn-taking rule. This study strengthens parallels between human conversations and nonhuman primate vocal exchanges.
Our recent paper Lledo-Ferrer et al. (International Journal of Primatology 32: 974–991, 2011) questioned the classic view of territoriality and chemical communication in wild callitrichids, saddleback tamarins (Saguinus fuscicollis). We suggested that rather than defending a territory or resources, chemical communication was more likely to be a way of exchanging reproductive information between groups. Roberts (International Journal of Primatology 33, 2012). challenged this interpretation, considering that the results could more parsimoniously be interpreted as fulfilling a resource defense strategy. This response is intended to clarify some aspects of the debate and to suggest how further research could shed new light on the present polemics.
Communication; Costs and benefits; Scent-marking; Tamarins
Altruistic food giving among genetically unrelated individuals is rare in nature. The few examples that exist suggest that when animals give food to unrelated others, they may do so on the basis of mutualistic or reciprocally altruistic relationships. We present the results of four experiments designed to tease apart the factors mediating food giving among genetically unrelated cotton-top tamarins (Saguinus oedipus), a cooperatively breeding New World primate. In experiment 1 we show that individuals give significantly more food to a trained conspecific who unilaterally gives food than to a conspecific who unilaterally never gives food. The apparent contingency of the tamarins' food-giving behaviour motivated the design of experiments 2-4. Results from all three experiments show that altruistic food giving is mediated by prior acts of altruistic food giving by a conspecific. Specifically, tamarins do not give food to unrelated others when the food received in the past represents the by-product of another's selfish actions (experiments 2 and 3) or when a human experimenter gives them food (experiment 4) as did the unilateral altruist in experiment 1. By contrast, if one tamarin gives another food without obtaining any immediate benefit, then the recipient is more likely to give food in return. Overall, results show that tamarins altruistically give food to genetically unrelated conspecifics, discriminate between altruistic and selfish actions, and give more food to those who give food back. Tamarins therefore have the psychological capacity for reciprocally mediated altruism.
Semple et al. (Semple et al. in press, Biol. Lett. (doi:10.1098/rsbl.2009.1062)) argued that the ‘law of brevity’ (an inverse relationship between word length and frequency of use) applies not only to human language but also to vocal signalling in non-human primates, because coding efficiency is paramount in both situations. We analysed the frequency of use of signals of different duration in the vocal repertoires of two Neotropical primate species studied in the wild—the common marmoset (Callithrix jacchus) and the golden-backed uakari (Cacajao melanocephalus). The key prediction of the law of brevity was not supported in either species: although the most frequently emitted calls were relatively brief, they were not the shortest signals in the repertoire. The costs and benefits associated with signals of different duration must be appreciated to understand properly their frequency of use. Although relatively brief vocal signals may be favoured by natural selection in order to minimize energetic costs, the very briefest signals may be ambiguous, contain reduced information or be difficult to detect or locate, and may therefore be selected against. Analogies between human language and vocal communication in animals can be misleading as a basis for understanding frequency of use, because coding efficiency is not the only factor of importance in animal communication, and the costs and benefits associated with different signal durations will vary in a species-specific manner.
law of brevity; Neotropical primates; vocal repertoire; signalling
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.
music evolution; vocal communication; affective responses; tamarins; species-specific music
Worldwide, approximately 170 million people are chronically infected with hepatitis C virus (HCV), and chronic infection frequently progresses to serious liver disease, including cirrhosis and hepatocellular carcinoma. GB virus B (GBV-B), the virus phylogenetically most closely related to HCV, causes hepatitis in tamarins. We have demonstrated the suitability of the tamarin as a host for GBV-B and as a surrogate nonhuman primate model for HCV infection, and we have initiated studies of GBV-B infection in a closely related species, the common marmoset (Callithrix jacchus). Here, we demonstrate that marmosets exhibit two phenotypes upon infection with GBV-B: the susceptible phenotype and the partially resistant phenotype. In addition, we identify changes that may correlate with adaptation of the virus to the partially resistant host. GBV-B was serially passaged five times through 14 marmosets as one lineage and two times through 6 marmosets as a second lineage. Virus adapted to the marmosets and eventually exhibited robust infections in two separate lineages, lineages 1 and 2. A third lineage was initiated with a molecular clone, and again, susceptible and partially resistant phenotypes were observed. Three isolates were fully sequenced (from lineage 1), and 21 nucleotide changes were observed, with six amino acid changes. We speculate that the marmoset partially resistant phenotype may be due to a polymorphism in the marmoset population that affects critical virus-host interactions and that wild-type GBV-B is capable of rapidly adapting to this altered host.
In many primate species a close attachment between mother and infant provides a secure base for the infant when the infant is frightened or under stress. In cooperatively breeding primates infant carrying is divided among several individuals in the group, with the mother often doing little more than nursing. In these species it is not clear which individual would best serve as a secure base for the infant. We studied eight infant cotton-top tamarins from birth through 20 weeks of age, noting who carried the infant during the first 100 days, who transferred food with the infants, and, as infants became independent, with whom they associated during social play and affiliative behavior. From week 9 to week 20, when infants were independent of carriers most of the time, we presented families with six trials (once every 2 weeks) with a threatening stimulus (a human dressed in a lab coat and wearing an animal mask). Infants played primarily with their twin or youngest sibling and had affiliative interactions with many family members. However, in fearful situations, infants ran to those who had carried them and transferred food with them the most–their father or oldest brother (never to the mother). Although adults increased rates of mobbing calls in response to the threat, infants significantly reduced their vocalization rate. For these cooperatively breeding monkeys, the attachment object for infants is the family member that invested the most effort in carrying the infant and transferring food with the infant. These results parallel and extend results from bi-parental infant care species in which the father serves as the primary attachment figure.
infant attachment; secure base; response to threats; cooperative breeding; cotton-top tamarins (Saguinus oedipus)
Many animals interrupt their moving with brief pauses, which appear to serve several different functions. We examined the function of such intermittent locomotion in wild living mustached tamarins (Saguinus mystax), small arboreal New World primates that form mixed-species groups with saddleback tamarins (Saguinus fuscicollis). We investigated how different environmental and social factors affect pausing during locomotion and used these data to infer the function of this behavior. As measures of intermittent locomotion, we used percentage of time spent pausing and pause rate. We considered 3 possible functions that are not mutually exclusive: increased endurance, route planning, and antipredator vigilance. Mustached tamarins spent on average (mean ± SE) 55.1 ± 1.0% of time pausing, which makes effective resource exploitation more time consuming and needs to be outweighed by correspondingly large benefits. Percentage of time spent pausing decreased in larger mixed-species groups vs. smaller mixed-species groups and decreased with height and in monkeys carrying infants. It was not affected by sex, age, spatial arrangement, or single-species group size. Pause rate increased in individuals traveling independently compared to those traveling in file, but was not affected by other factors. The group size effect in mixed-species groups lends support to the notion that pausing during locomotion is an antipredator tactic that can be reduced in the increased safety of larger groups, but other results suggest that additional functions, particularly route planning, are also of great importance. Benefits in terms of predator confusion and group movement coordination are also likely to play a role and remain a topic for further research.
intermittent locomotion; mixed-species groups; Saguinus mystax; vigilance
For conservation purposes, accurate methods are
required to track cotton-top tamarins in their natural habitat. As existing census methods are
not appropriate for surveying these monkeys, a lure-transect method combined with playback
vocalization was used here to allow accurate counting of the animals.
The cotton-top tamarin (Saguinus oedipus) is a critically endangered primate,
endemic to the tropical forests of Colombia. Population monitoring is essential to evaluate
the success of conservation efforts, yet standard survey methods are ineffective because
animals flee silently before they are seen. We developed a novel technique that combines the
use of playbacks of territorial vocalizations with traditional transect surveys. We used
remote sensing to identify potential habitat within the species' historic range, and visited
the 27% that we could survey safely. Of this, only 99 km2 was extant forest,
containing an estimated 2,045 animals (95% confidence interval 1,587–2,634). Assuming
comparable densities in non-surveyed areas, approximately 7,394 wild cotton-top tamarins
remain in Colombia. With 20–30,000 animals exported to the United States in the late 1960s,
this must represent a precipitous decline. Habitat destruction and capture for the illegal
pet trade are ongoing. Urgent conservation measures are required to prevent extinction in
Approximately 3% of the world population is chronically infected with hepatitis C virus (HCV). GB virus B (GBV-B), a surrogate model for HCV, causes hepatitis in tamarins and is the virus phylogenetically most closely related to HCV. Previously we described a chimeric GBV-B containing an HCV insert from the 5′ noncoding region (NCR) that was adapted for efficient replication in tamarins (Saguinus species). We have also demonstrated that wild-type (WT) GBV-B rapidly adapts for efficient replication in a closely related species, the common marmoset (Callithrix jacchus). Here, we demonstrate that the chimeric virus failed to adapt during serial passage in marmosets. The chimeric virus was passaged four times through 24 marmosets. During passage, two marmoset phenotypes were observed: susceptible and partially resistant. Although appearing to adapt in a resistant animal during a prolonged and gradual increase in viremia, the chimeric GBV-B failed to replicate efficiently upon passage to a naïve marmoset. The resistance was specific to the chimeric virus, as the chimeric virus-resistant animals were susceptible to marmoset-adapted WT virus during rechallenge studies. Three isolates of the chimeric virus were sequenced, and 20 nucleotide changes were observed, including eight amino acid changes. Three unique changes were observed in the 5′ NCR chimeric insert, an area that is highly conserved in HCV. We speculate that the failure of the chimeric virus to adapt in marmosets might be due to a bottleneck that occurs at the time of infection of resistant animals, which may lead to a loss of fitness upon serial passage.
There is a surprising degree of overlapping structure evident across the languages of the world. One factor leading to cross-linguistic similarities may be constraints on human learning abilities. Linguistic structures that are easier for infants to learn should predominate in human languages. If correct, then (a) human infants should more readily acquire structures that are consistent with the form of natural language, whereas (b) non-human primates’ patterns of learning should be less tightly linked to the structure of human languages. Prior experiments have not directly compared laboratory-based learning of grammatical structures by human infants and non-human primates, especially under comparable testing conditions and with similar materials. Five experiments with 12-month-old human infants and adult cotton-top tamarin monkeys addressed these predictions, employing comparable methods (familiarization-discrimination) and materials. Infants rapidly acquired complex grammatical structures by using statistically predictive patterns, failing to learn structures that lacked such patterns. In contrast, the tamarins only exploited predictive patterns when learning relatively simple grammatical structures. Infant learning abilities may serve both to facilitate natural language acquisition and to impose constraints on the structure of human languages.