Lactational Programming? Mother's milk energy predicts infant behavior and temperament in rhesus macaques (Macaca mulatta)
Authors: Katie Hinde & John P. Capitanio
There are many aspects of ''mothering'' that may provide information to the mammalian infant about environmental conditions during critical periods of development. One essential element of mothering involves the quantity and quality of milk that mothers produce for their infants, which reflect maternal condition, but little is known about the consequences for infant behavioral development. Here we present the first evidence for any mammal that natural variation in available milk energy (AME) from the mother is associated with later variation in infant behavior and temperament in rhesus macaques. Infants whose mothers produced greater AME early in infancy coped more effectively (e.g., locomoted more, explored the environment more, ate, drank) and showed greater 'Confidence' (were more playful, exploratory, curious, active, and confident) in a stressful, novel situation months later, independent of the milk their mothers produced at the time of assessment. These results suggest that early nutrition has an organizational effect on infant behavioral phenotype and may be a nutritional cue that calibrates the infant's behavior to environmental or maternal conditions. For infants whose mothers produce ample available milk energy when infants begin to explore their physical and social environment, active and confident behavioral dispositions (which presumably require more energy) are not risky. In contrast, infants whose mothers produce less milk energy potentially face tradeoffs between growth, maintenance, and behavioral activity and may adjust behavioral patterns to minimize energy expenditure. These data provide new insight into potential mechanisms for behavioral development and illuminate directions for investigating maternal effects, nutritional programming, and developmental plasticity.
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Ethical Issues Faced by Field Primatologists: Asking the Relevant Questions
Authors: Linda Marie Fedigan
Field primatologists face unusual ethical issues. We study wild, free-ranging animals and receive research approval from animal care committees. However, animal care evaluation forms developed from concerns about laboratory research and are based on the "Three R's" for humane treatment of captive experimental subjects (replacement, reduction, refinement), which are only debatably relevant to field research. This paper reviews ethical issues many field primatologists say they face and how these might be better addressed by animal care forms. These issues are divided into three categories: "Presence, Protocols and People." A commonly mentioned concern arising from our presence in the field is the possibility of disease transmission. Furthermore, although most primate field studies employ only observational protocols, the practice of habituating our study animals to close human presence is an ethical concern since it can lessen the animals' fear of humans, thereby facilitating undesirable behaviors (e.g., crop-raiding) and rendering them vulnerable to harm. Field primatologists who work in host countries must observe local laws and traditions. As conservationists, primatologists must often negotiate between the resource needs and cultural practices of local people and the interests of the nonhuman primates. Many say they face more ethical dilemmas arising from human interactions than from research on the animals per se. This review concludes with suggestions for relevant questions to ask on animal care forms and actions that field primatologists can take to better inform animal care committees about the common ethical issues we experience as well as how to develop guidelines for addressing them.
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Prey capture efficiency in brown capuchin monkeys (Cebus apella) is influenced by sex and corpus callosum morphology
Authors: Kaitlyn Hellner-Burris, Courtney A. Sobieski, Valerie R. Gilbert & Kimberley A. Phillips
Capuchin monkeys are New World Primates whose diet largely consists of fruits. However, these monkeys regularly prey upon vertebrates such as lizards, birds, and fish. Capturing small fast-moving prey requires the ability to process complex visuospatial information such as motion detection, shape, and pursuit. Here we report the results of an experimental investigation into whether capuchins display sex differences in prey capture efficiency, and whether these differences are associated with the morphology of a region of the brain involved in visuospatial ability, the corpus callosum.
We examined prey capture behavior in our laboratory by providing these monkeys opportunities to fish. We acquired structural magnetic resonance images from these same monkeys to relate behavioral performance to morphology of the corpus callosum. Our results indicate that males were faster and more successful than females at capturing prey. Furthermore, morphology of the corpus callosum significantly differed between males and females and was associated with prey capture. Taken together, our results suggest a relationship between prey capture efficiency, sex, and brain morphology.
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Impact of yellow fever outbreaks on two howler monkey species (Alouatta guariba clamitans and A. caraya) in Misiones, Argentina
Authors: Ingrid Holzmann, Ilaria Agostini, Juan Ignacio Areta, Hebe Ferreyra, Pablo Beldomenico, Mario Di Bitetti
The yellow fever is caused by a virus and transmited by mosquitoes. This virus came from Africa to America, causing serious damage in wild primate populations. All Neotropical primates are susceptible to this disease. Yellow fever outbreaks (YFOs), causing massive mortalities, have been observed especially in howler monkeys (Alouatta spp.). Howler monkeys are considered "sentinel species": they play an important role in the prevention of yellow fever in humans, by warning humans of the presence of the virus in the area, with their lives. They are to human populations as the canary was to the miners: the delicate canary informed, with its death, that gases were reaching a toxic level for the miners. The howler early-warning system allows the possibility of vaccination in humans. Between November 2007 and October 2008 two YFOs ocurred in Northeastern Argentina, with serious impact on two howler monkey species, the brown howler (Alouatta guariba clamitans) and the black howler (A. caraya). The first outbreak started in November 2007 in the North of the Misiones province, and continued during January 2008 in the central area of Misiones, in El Piñalito, where our four study groups of howlers were decimated. The second outbreak began in October 2008 in southern Misiones. Overall, 59 howlers were found dead in Misiones from November 2007 to December 2008, and 83 are estimated to have periled. The sentinel howler's deaths in El Piñalito, allowed a prompt human vaccination campaign, saving many lives. In Misiones, both howler species are in a delicate situation, especially the brown howler, an already endangered species in Argentina and present only in Misiones. If we add the recurrence of YFOs to the reduction of suitable habitat to small fragments, it could be only a matter of time until howler populations disappear from the Upper Paraná Atlantic Forest in Misiones.
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The use of artificial neural networks to classify primate vocalizations: a pilot study on black lemurs
Authors: Luca Pozzi, Marco Gamba & Cristina Giacoma
Vocal communication in non-human primate has received a lot of attention over the past few years, in particular in relation to the study of how human language evolved. The first step for understanding communication in our closest relatives is to describe the complexity of their vocal repertoire, including the number of calls emitted by a particular species. This is a crucial and preliminary step for all studies that want to investigate function and complexity of primate communication. In a new study recently published on the American Journal of Primatology , the authors employ for the first time a new computational tool to describe the repertoire of a lemur species: the Artificial Neural Networks (ANNs). ANNs are computer simulations of biological nervous systems and attempt to mimic the learning capacity of biological neural systems by modeling the low level structure of the brain. Although this technique cannot reach the complexity of most biological nervous systems, it has been suggested to provide a powerful tool of call classification thanks to its ability of learning from previous experience and dealing with incomplete information or noisy data. The results show that ANNs are able to successfully categorize lemur vocalizations and outperform some statistical techniques commonly used to address the same tasks. This study suggests that ANNs may provide a new powerful and more flexible tool for primatologists that need to classify vocalizations in discrete categories.
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Phylogeny and Phylogeography of Squirrel Monkeys (Genus Saimiri) Based on Cytochrome b Genetic Analysis
Authors: Anne Lavergne, Manuel Ruiz-García, François Catzeflis, Sandra Lacote, Hugues Contamin, Odile Mercereau-Puijalon, Vincent Lacoste, Benoît de Thoisy
The Squirrel monkeys (genus Saimiri) are widely distributed in Central and South America. The genus includes a complex of species and subspecies displaying a considerable morphological variation. Previous studies have identified one to seven species and up to 16 subspecies. Nevertheless, the genetic relationships between these taxa are not well known. In this work, we used cytochrome b sequences to investigate the phylogenetic relationships of squirrel monkeys and their patterns of diversification across South America. This genetic marker having already provided a consistent framework of the squirrel monkeys in Central and South America, here we focused on the Amazon basin. Thirty-two monkeys from well-defined geographic origins, belonging to four species, were studied: Saimiri oerstedii, S. sciureus, S. boliviensis and S. ustus. We recorded a high level of gene diversity consistent with the high level of behavioral and morphological variation observed across the geographic range of the genus. The maximum genetic divergence was observed between S. b. boliviensis and S. ustus, respectively found in Bolivia and on the Southern bank of the Amazon. Moreover, we confirm the existence of several subspecies already advocated on the basis of their geographic distribution: Saimiri sciureus macrodon, Saimiri sciureus albigena, Saimiri sciureus cassiquiarensis and Saimiri sciureus collinsi. We also show that the Eastern region of South America, in the Andean slopes, has been the point of dispersal of the squirrel monkeys, two to three million years ago. They since dispersed across Amazonia and the different species have emerged, shaped by large rivers and forest refuges.
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Multiple Measures of Laterality in Garnett's Bushbaby (Otolemur garnettii)
Authors: David B. Hanbury, Kyle D. Edens, David A. Bunch, Claire E. Legg, & Sheree L. Watson
A recent review of prosimian laterality [Watson & Hanbury, 2007] points out the lack of a systematic study in a prosimian species that examines the interrelationships between multiple measures of lateralized behavior in a single species. Thus, we examined seven measures of laterality in 17 bushbabies (Otolemur garnettii) including simple reaching, hand use in prey capture, turning, side-of-mouth use, tail wrapping, leading foot in locomotion, and foot-rubbing. We tested bushbabies simple reaching and turning from either a quadrupedal or bipedal posture, and while clinging to the side of the cage. Each bushbaby was significantly and strongly lateralized in simple reaching and maintained the same bias from each posture. Biases in simple reaching correlated positively with hand use in prey capture. Turning biases were inconsistent across postural conditions. Negative correlations emerged between tail wrapping and leading foot measures, bipedal turning and tail wrapping, as well as between quadrupedal reaching and bipedal turning. Overall, measures requiring the use of the hands were significantly more strongly lateralized than those that did not. Individual bushbabies showed unique patterns of lateral biases. We suggest that bushbabies may possess multiple lateralized motoric systems that are differentially implicated in a variety of behaviors. The data from this study suggest that the use of handedness as a behavioral surrogate for hemispheric specialization of the brain is not adequate. Further research on prosimian laterality in bushbabies and other species is necessary to better elucidate these relationships.
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Male and female range use in a group of white-bellied spider monkeys (Ateles belzebuth) in Yasuní National Park, Ecuador
Authors: Stephanie N. Spehar, Andres Link, and Anthony Di Fiore
Spider monkeys exhibit fission-fusion social systems in which group members range in ever-changing subgroups rather than as a cohesive group. Most studies indicate that male and females in these groups differ considerably in their ranging patterns: males use large ranges that overlap the ranges of other group members, and use boundary areas more often than females. Females, on the other hand, use nonoverlapping "core areas" that only cover a small portion of the group range. These patterns may be due to resource competition and relatedness: females may range alone to avoid competition for food, and may avoid potentially dangerous boundary areas. Males, who usually remain in the group they were born in and are thus more closely related, may be cooperating to defend the group range. We evaluated whether the one group of spider monkeys in Yasuní National Park, Ecuador conformed to these "male-bonded" ranging patterns. Surprisingly, we found that females in our group did not use "core areas," and the ranges of females overlapped considerably. The size of male and female home ranges was nearly identical, and males and females used boundary areas equally. Similar "bisexually bonded" ranging patterns are seen in some groups of West African chimpanzees. We suggest that the less sex-segregated ranging patterns of this spider monkey group may be due to low relatedness between males, perhaps as a result of human disturbance, or to the distribution of key resources. This highlights the potential for behavioral flexibility in spider monkeys and other fission-fusion primates in response to varying local conditions.
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Semi-quantitative tests of cyanide in foods and excreta of Three Hapalemur species in Madagascar
Authors: Nayuta Yamashita, Chia L. Tan, Christopher J. Vinyard, Cathy Williams
Three sympatric Hapalemur species (H. g. griseus, H. aureus, and H. (Prolemur) simus) in Ranomafana National Park, Madagascar are known to eat bamboo food parts that contain cyanide. How these lemurs avoid cyanide poisoning remains unknown. In this study, we tested for the presence/absence of cyanide in bamboo lemur foods and excreta to (1) document patterns of cyanide consumption among species with respect to diet, (2) identify routes of elimination of cyanide from the gastrointestinal tract, and (3) determine whether cyanide is absorbed from the diet. We tested 102 food, urine, and fecal samples for hydrogen cyanide (HCN) during two pre-dry seasons (April 2006, May 2007) using commercially available Cyantesmo test strips. The test strips changed color in the presence of HCN, and we recorded color change on a scale of 0 (no change) to 5 (cobalt) at preset intervals with a final score taken at 24 hr. We detected cyanide in bamboo food parts and urine of all three Hapalemur species. Time to color change of the test strips ranged from almost instantaneous to >12 hr incubation. Of the foods tested, only bamboo contained cyanide, but results differed among bamboo species and plant parts of the same species. Specifically, branch shoot and culm pith of the giant bamboo produced strong, immediate reactions to the test paper, whereas parts of liana bamboos produced either weak or no color change. Cyanide was present in almost all urine samples but rarely in fecal samples. This suggests that dietary cyanide is absorbed in the gastrointestinal tract of the Hapalemur species and excreted, at least in part, by the kidneys. Samples from H. griseus exhibited lower, though still detectable, cyanide levels compared with H. simus and H. aureus. Differences among lemur species appear to be related to the specific bamboo parts consumed.
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High-fiber diet promotes weight loss and affects maternal behavior in vervet monkeys
Authors: Lynn A. Fairbanks, Karin Blau, Matthew J. Jorgensen
The dramatic increase in obesity in western societies has shifted the emphasis in nutrition research from the problems of undernutrition to the adverse consequences of being overweight. As with humans, Old World monkeys are at increased risk for type II diabetes and other chronic diseases when they gain excessive weight. To prevent overweight and obesity, promote animal health, and provide a more natural level of fiber in the diet, the standard commercial monkey chow diet at a vervet monkey breeding colony was changed to a higher fiber formulation in 2004. The new diet was also higher in protein and lower in carbohydrate and energy density than the standard diet. Because maternal behavior is known to be sensitive to differences in resource availability, data on weight and mother-infant interactions for 147 mothers with 279 infants born from 2000 through 2006 were assessed for effects of the diet change. The results showed that, even though food was provided ad libitum, the mean body weight of breeding females was 10% lower after the transition to the high-fiber diet. Behaviorally, mothers on the high-fiber diet were significantly more rejecting to their infants, and their infants had to play a greater role in maintaining ventral contact in the first few months of their lives. The effects of the diet change on maternal rejection were significantly related to the mother's body weight, with lower-weight mothers scoring higher in maternal rejection. These results demonstrate that maternal behavior is responsive to changes in maternal condition, and that beneficial changes in the diet may have unintended consequences on behavior.
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Chimpanzees Prey on Army Ants with Specialized Tool Set
Authors: Crickette M. Sanz, Caspar Schöning, and David B. Morgan
The chimpanzee culture debate has received a great deal of attention over the past ten years. New cultural variants have been proposed, while others have been challenged. Ant dipping is one of the most commonly cited examples of a behavior that differs between chimpanzee populations. It was claimed that chimpanzees in East Africa show a particular gathering technique, whereas apes in West Africa exhibit another variant of the behavior. More recently, detailed studies of these techniques across sites have shown that most of the variation in tool use to prey upon army ants could be explained by the characteristics of the targeted ant species. However, remote video cameras stationed in the Republic of Congo are revealing that chimpanzees in the Goualougo Triangle have developed a more sophisticated way to gather army ants. In the American Journal of Primatology, scientists report their observations of chimpanzees preying upon ants with a specialized tool set consisting of a wooden perforating tool to open the ant nest and another flexible tool to gather insects. Although these chimpanzees are targeting the same ants harvested in other regions, there are no other reports of such regular or widespread use of more than one type of tool to prey upon Dorylus ants. It has only recently been discovered that these particular chimpanzees use several different types of tool sets which could be their own cultural signature. There is an urgency to learn about these behaviors as the existence of the apes in the Congo Basin is threatened by logging, hunting, and disease.
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Social learning of diet and foraging skills by wild immature Bornean orangutans: Implications for culture
Authors: Adrian V. Jaeggi, Lynda P. Dunkel, Maria A. Van Noordwijk, Serge A. Wich, Agnes A. L. Sura and Carel P. Van Schaik
Imagine you were in a rain forest and had to find your own food to survive, what would you do? If you are an immature orangutan you rely on your mother to show you what to eat. In this study immatures foraged together with their mothers and only rarely tried novel food, thus acquiring largely the same diet. However, they did not just eat everything available in the forest. Knowledge about edible items differed among adults, as shown by the example of an immigrant female who ate different items even when foraging in the same area as others. This indicates that a reliance on social learning may lead to diet differences for no ecological reason, i.e. food traditions. Such traditions can be expected for all animals where immatures spend a long time with parents or other role-models and are of course well known among humans.
But some items eaten by orangutans are not easily recognized as food and are difficult to process. Foraging for embedded items such as inner bark or hidden insect nests requires skills that have to be learned through repeated observation and practice. Immatures observed their mothers especially when processing such items and practiced this behavior afterwards by mimicking their mothers'. This suggests that immatures used observation to focus their learning. Observational forms of learning may have been necessary to evolve for species relying on extractive foraging and became an essential process in the development of human cultures as they allow the transmission of difficult skills.
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Social Behavior in Fission-Fusion Groups of Red Uakari Monkeys (Cacajao calvus ucayalii)
Authors: Mark Bowler and Richard Bodmer
Red uakaris (cacajao calvus ucayalii) are one of the least-known neotropical primates, and very little has been studied on their social behavior, particularly in the wild. This study reveals some very unusual social behavior for this very unusual looking primate, and presents some interesting possibilities for the evolution of social behavior in pitheciine primates. Uakaris live in very large groups that fission and fuse during foraging, and may be extremely flexible in their size and composition. Adult females travelled with their offspring and typically an older juvenile, and several of these units made up much larger groups. Units of male uakaris accompanied these groups, and males in these units were affiliative and acted together to display to other males during aggressive encounters. Several of these displays had never been observed before, and included swinging by their ankles like a pendulum while bristling their fur, and vigorous urine washing. These observations are compatible with the theory that a short breeding season has lead to intense competition for females. In this paper we speculate that affiliative male uakaris cooperate in groups to defend access to females during this breeding season, and may be tolerant of each other's mating activity. This raises interesting questions like; are these males related? And, which sexes disperse from uakari groups?
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Volumetric and Lateralized Differences in Selected Brain Regions of Chimpanzees (Pan troglodytes) and Bonobos (Pan paniscus)
Authors: William D. Hopkins, Heidi Lyn, and Claudio Cantalupo
Bonobo and chimpanzees, two species within the genus Pan, have reportedly only split from their common ancestor 2-3 million years ago, but have been described as having different social organization, cognitive and linguistic abilities and motor skills, despite their close biological relationship. Here, we examined whether bonobos and chimpanzee differ in selected brain regions that may map to these different social and cognitive abilities.
Eight chimpanzees and eight bonobos were matched on age, sex and rearing experiences. These sixteen apes were MRI scanned and measures were obtained for volumes of the whole brain, cerebellum, caudate, putamen, motor-hand area, hippocampus, inferior frontal gyrus and planum temporale. Chimpanzees had significantly larger cerebellum and borderline significantly larger hippocampus and putamen, after adjusting for brain size, compared to bonobos. Bonobos showed greater leftward asymmetries in the caudate, putamen, and motor-hand area compared to chimpanzees. The hippocampus is most often associated with spatial memory and the difference in size may relate to the chimpanzee's relatively larger home range size. The differences in the cerebellum, caudate, putamen, and motor-hand areas may reflect differences in inherent skill for motor actions.
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Vigilance in ursine black and white colobus monkeys (Colobus vellerosus): an examination of the effects of conspecific threat and predation
Authors: Andrew MacIntosh and Pascale Sicotte
"Knowledge comes by eyes always open...and there is no knowledge that is not power." (Ralph Waldo Emerson, American essayist, b.1803)
To look or not to look, that is the question concerning a new study in the American Journal of Primatology, which examines vigilance behaviour in black and white colobus monkeys (Colobus vellerosus) at the Boabeng-Fiema Monkey Sanctuary in Central Ghana. Vigilance refers to a state of watchfulness or alertness, and has most commonly been viewed as a response to the threat of predation. The phrase "eat or be eaten" illustrates an important problem facing animals in the wild, which need to balance behaviors such as feeding with scanning for potential predators. However, studies have also shown that for many social animals, predators aren't the only things pressing for their attention. This study emphasizes this fact, and examines the importance of directing vigilance toward other individuals of the same species (conspecifics), and even toward those living within the same social group. In ursine colobus monkeys, it is far from a civil affair when two neighboring social groups come into contact, and these events generally consist of a series of chases, distress vocalizations and chaos, and provide the context for rare events such as group takeovers, infanticide, female transfer, and for individuals to sneak in a few copulations with individuals outside of their social group. The authors found that, indeed, colobus were most vigilant during such encounters, but individuals were also more vigilant when even the potential to encounter other groups increased. Although the authors do not discount the importance of anti-predator vigilance, they highlight the possibility that the greatest threat may come from members of neighboring groups, particularly in locations at which predation pressures may be low.
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Kinship and Social Bonds in Female Chimpanzees (Pan troglodytes)
Authors: Kevin Langergraber, John Mitani, and Linda Vigilant
In humans as well as many other social mammals, individuals do not interact in the same way with all group members, but instead form close social bonds with a few individuals. In most primate species, females remain in the same group their entire lives, and preferentially form close social bonds with their close maternal kin (i.e., mothers, daughters, sisters, etc.). This bias in favor of relatives makes sense from an evolutionary point of view: if social bonds are beneficial to individuals, then it pays to form them with individuals who are likely to share the same genes. Humans have been thought to be unique among primates in the extent to which close social bonds form between unrelated females. We investigated whether chimpanzees, one of the few primate species in which, like humans, females routinely disperse from their natal group, also form strong social bonds in the absence of kinship. We compared our results on patterns of female association in temporary parties, spatial proximity, and grooming with those of males from the same group who have previously been shown to form strong social bonds. We found that it was certain pairs of females, not males, who had the highest association frequencies, and that patterns of association were also reflected in patterns of close spatial proximity and grooming, and persisted over several years. Using molecular genetic analyses, we also found that females very rarely have other female family members in their group, suggesting that females do not preferentially join groups that already contain their adult relatives.
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Grooming in mandrills and the time frame of reciprocal partner choice
Authors: Gabriele Schino and Barbara Pellegrini
A widely held view argues that reciprocal altruism is rare because its cognitive requirements would exceed those of most animals and that, when reciprocity does occur, it should be constrained to occurring over very short time frames because this is the only way to circumvent animal cognitive limitations.
In this study, we tested the cognitive constraint hypothesis by examining the time frame of reciprocal partner choice in the grooming interactions of mandrills (Mandrillus sphinx). In contrast to what is predicted by the cognitive constraint hypothesis, mandrills groomed preferentially those individuals that groomed them more even when cases of immediate reciprocation were excluded from the analysis. These results show that mandrills were not limited to reciprocating grooming over short time intervals.
We propose that the cognitive requirements of reciprocity have been vastly overestimated, and that a system of emotional bookkeeping may support the ability of primates to reciprocate over long time frames.
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