Dialects in pygmy marmosets? Population variation in call structure

Population variation in primate vocal structure has been rarely observed. Here, we report significant population differences in the structure of two vocalizations in wild pygmy marmosets (Trills and J calls). We studied 14 groups of pygmy marmosets Callithrix (Cebuella) pygmaea pygmaea from five populations in northeastern Ecuador. We analyzed the acoustic structure of Trills and J calls recorded from two adult animals in each group through focal samples. Although individuals and groups within a population differed in call structure, we found consistent structural differences at a population level for Trills and J calls. Pair‐wise comparisons for the two call types point to San Pablo and Amazoonico as the populations that differed the most, whereas Hormiga and Zancudococha showed the least differences. Discriminant function analysis indicates that calls from each population could be classified accurately at rates significantly above chance. Habitat acoustics, social factors and genetic drift may explain interpopulation vocal differences. This is the first evidence of within‐subspecies vocal differences, or dialects, in wild populations of a neotropical primate species. Am. J. Primatol. 71:333–342, 2009. © 2009 Wiley‐Liss, Inc.     

Home-Range Size of the Bare-ear Marmoset (Callithrix argentata) at Alter do Chão,Central Amazonia,Brazil

We studied factors affecting variation in home-range size of four groups of bare-ear marmosets (Callithrix argentata) in patches of forest within a central Amazonian savanna. We determined relative use of different parts of the home range by radiotelemetry. We estimated fruit availability monthly in transects through each home range and mapped the habitats within the home range of each group. We determined the densities of gum- and fruit-producing trees in 18 50 × 50-m quadrats and related these data to the frequency of use by marmosets. Home-range size varied by a factor of 6 between groups, even though the study area covered <15 km ² and included only one major biome. Marmoset activity was concentrated in areas with many gum-producing trees. Monthly range size is positively correlated with fruit availability only for the group with the largest home range; the other groups appeared to be responding to other factors. Home-range sizes appeared to be limited by the size of the main patch of contiguous forest available to each group. Our findings suggest that conservation planning that does not consider the possibility of large differences among primate home-range sizes may be unsatisfactory.     

The positional behavior of pygmy marmosets (<Emphasis Type="Italic">Cebuella pygmaea</Emphasis>) in northwestern Bolivia

Pygmy marmosets are distinctive given their diminutive body size, their year-round reliance upon exudates, and their use of morphologically adapted tegulae to engage in a high degree of claw-clinging behaviors associated with exudate exploitation. This project examined the positional behavior and habitat preferences of one group of pygmy marmosets in a secondary forest within the Department of Pando, northwestern Bolivia. Results from this study indicate that pygmy marmosets primarily use claw-clinging during feeding (89.6%) with preferential use of large vertical trunks. Claw-clinging was also the dominant postural mode during exudate foraging (43.1%) with preferential use of large vertical trunks. Quadrupedalism was the dominant locomotor mode during travel (55.7%) with preferential use of bamboo and medium-sized substrates. These results support previous notions that claw-climbing is a solution to overcome the constraints of small body size while suggesting that quadrupedalism is a habitat-dependent locomotor mode.     

Little Evidence to Support the Risk–Disturbance Hypothesis as an Explanation for Responses to Anthropogenic Noise by Pygmy Marmosets (Cebuella niveiventris) at a Tourism site in the Peruvian Amazon

The risk–disturbance hypothesis states that animals react to human stressors in the same way as they do to natural predators. Given increasing human–wildlife contact, understanding whether animals perceive anthropogenic sounds as a threat is important for assessing the long-term sustainability of wildlife tourism and proposing appropriate mitigation strategies. A study of pygmy marmoset (Cebuella niveiventris) responses to human speech found marmosets fled, decreased feeding and resting, and increased alert behaviors in response to human speech. Following this study, we investigated pygmy marmoset reactions to playbacks of different acoustic stimuli: controls (no playback, white noise and cicadas), anthropogenic noise (human speech and motorboats), and avian predators. For each playback condition, we recorded the behavior of a marmoset and looked at how the behaviors changed during and after the playback relative to behaviors before. We repeated this on ten different marmoset groups, playing each condition once to each group. The results did not replicate a previous study on the same species, at the same site, demonstrating the importance of replication in primate research, particularly when results are used to inform conservation policy. The results showed increased scanning during playbacks of the cicadas and predators compared with before the playback, and an increase in resting after playbacks of avian predators, but no evidence of behavior change in response to playbacks of human speech. There was no effect of ambient sound levels or distance between the playback source and focal animals on their behavior for all playback conditions. Although we find that noise can change the behavior of pygmy marmosets, we did not find evidence to support the risk–disturbance hypothesis.

     

Human speech reduces pygmy marmoset (Cebuella pygmaea) feeding and resting at a Peruvian tourist site,with louder volumes decreasing visibility

Although potentially beneficial in terms of raising awareness and conservation funding, tourist visitation of wild primates can have negative impacts on visited groups. Tourism‐generated noise is a relatively understudied facet of ecotourism research, and the effects of tourist‐generated speech on free‐ranging, wild primates has never been explored previously. This study investigates the behavioral responses of 10 groups of pygmy marmosets (Cebuella pygmaea) to human speech. Through the use of an experimental playback study using recorded human speech, we show that pygmy marmosets within the Tamshiyacu‐Tahuayo Reserve, Peru, are significantly less visible, and often move completely out of sight after louder playbacks. Although no consistent differences were found in other behaviors with playback duration and volume, playbacks of human speech tended to increase the amount of time individuals were alert and decrease feeding and resting behaviors. Our results demonstrate that human speech can alter the behavior of visited primates, and identifies a decrease in primate visibility within the increasing volume. As all trials in this study took place near a marmoset group's feeding tree, moving out of sight from the visible study area is a particularly energetically costly behavior, and also has a negative effect on visitor enjoyment as it limits the time that they are able to view the target species. This response was not observed (nor was any other consistent behavior change) in control trials where the marmosets were exposed to human presence but not to speech, suggesting that negative tourist impacts can be reduced by encouraging tourists to refrain from speaking in the presence of visited primate groups.     

Environmental correlates of vocal communication of wild pygmy marmosets, Cebuella pygmaea

We quantified the acoustic characteristics of the habitats of two wild populations of pygmy marmosets, in Amazonian Ecuador to evaluate their effects on vocal signal structure. We obtained measures of ambient noise, sound attenuation and reverberation through recordings and broadcasts of exemplars of two short-range vocalizations and one long-range vocalization of the marmosets. Ambient noise levels differed among habitats. The calls of pygmy marmosets had frequencies that coincided with relatively quiet regions of the ambient noise spectra of the habitats. The three vocalization types were degraded similarly in all habitats. The two short-range signals, with a pulsatile structure, were more affected by reverberation than was the long-range, less pulsatile vocalization. This degradation could be used by the marmosets to estimate the distance of the caller animals. We obtained data on context of vocalizations from six groups of pygmy marmosets, three from each population, in both the dry and rainy seasons. The use of Trills, J calls and Long calls was related to the distance between the calling animal and the potential receivers suggesting that marmosets are using the calls in a way appropriate to the effects of habitat acoustics. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Spatial Distribution and Exploitation of Trees Gouged by Common Marmosets (Callithrix jacchus)

Resource distribution shapes many aspects of primate behavioral ecology. Though the spatial patterning of fruits, leaves, and insects has been explored among primate foods, comparatively less is known about exudate distributions. Tree exudates are a renewable resource, provide long-term evidence of exploitation, and may be selectively exploited to manipulate spatial distribution. We assessed the spatial patterning of trees gouged by common marmosets (Callithrix jacchus) to determine if they exhibit a uniform, random, or clumped distribution. We also asked whether marmosets selectively gouge trees in home range centers, which may afford them exclusive access to exudates. We explored whether spatial or physical characteristics of trees predict how intensely gouged trees were exploited. The mean nearest neighbor distance of gouged trees was significantly closer than expected for a random distribution and Ripley’s K-function showed that gouged trees were clumped across all spatial scales in our study area. Clumping may enable marmosets to reduce day and home ranges and facilitate repeated gouging of trees. Gouged trees were not closer to marmosets’ home range centers than peripheries, nor were centrally located trees more intensely gouged. Increased gouging intensity was associated with larger tree circumferences, although this effect was primarily driven by interspecific differences in circumference. Although marmosets may benefit from exploiting clumped exudates, they do not concentrate gouging in areas where they are more likely to gain exclusive access. Species-specific tree characteristics such as exudate quality and/or bark properties may play a larger role in determining gouging patterns than intergroup feeding competition.     

Spatio-Temporal Factors Shaping Diurnal Space Use by Pygmy Rabbits

Abstract: Factors influencing patterns of space use by pygmy rabbits (Brachylagus idahoensis) are poorly understood. We studied diurnal space use by adult pygmy rabbits during multiple breeding and nonbreeding seasons at 3 sites in the Lemhi Valley, Idaho, USA, during 2004–2005. Pygmy rabbits used larger areas than predicted by allometric models and documented by some previous investigations. Sex and season strongly influenced space use by rabbits. Males used larger home ranges and core areas, more burrow systems, and more widely dispersed burrow systems than did female rabbits. We also documented significant differences among study sites in many movement parameters, which suggested that local resource distribution also might influence how pygmy rabbits use space. Our results indicated that pygmy rabbits use large areas and exhibit seasonal, sex, and site-specific variation in patterns of movement and space use. Therefore, larger areas of habitat may be needed to conserve pygmy rabbits to accommodate seasonal, regional, and potentially annual variation in resource availability and to maintain linkages among populations.     

Individual recognition of contact calls by pygmy marmosets

Individual recognition by voice has been frequently assumed to be an important phenomenon in the social species. The present study on pygmy marmosets (Cebuella pygmaea) demonstrated that there are distinctive acoustic features in each of two contact calls by which individuals could be distinguished from each other. Individual pygmy marmosets responded differently depending on which type of contact call was given and on the identity of the vocalizing animal. Playbacks of individual calls through hidden speakers produced some evidence for differential individual responses, but only when they originated from familiar locations. These results indicate that pygmy marmosets recognize each other on the basis of their contact calls.     

Differences among captive callitrichids in the digestive responses to dietary gum

Although many members of the Callitrichidae, a monophyletic family of small, New World monkeys, have been observed to feed on plant exudates, available field data support the generalization that pygmy and common marmosets (Cebuella pygmaea and Callithrix jacchus) feed on gums to a greater extent than most other callitrichids. Because microbial fermentation is required for vertebrates to digest gums, gum-feeding primates may react differently to dietary gum from their relatives that eat little gum. To test this hypothesis, digestion trials were conducted on animals from the two marmoset species, two tamarin species (Saguinus fuscicollis and S. oedipus), and a species of lion tamarin (Leontopithecus rosalia). These species span the range of body sizes within the Callitrichidae. All animals were fed two variations of a homogeneous diet, which differed only in that gum arabic was added to one. Transit time of digesta (TFA) and digestive efficiency (as measured by the coefficients of apparent digestibility of dry matter and energy [ADDM and ADE, respectively]) were compared between diets for each individual. As predicted, the digestive responses of marmosets differed from the responses of the other study species. In marmosets, TFA tended to be longer when gum was added to the diet, while TFA did not change in the other three species. Digestive efficiency decreased in tamarins and lion tamarins with the addition of gum to the diet; marmoset digestive efficiency was unaffected by diet. The results of this research are consistent with the hypothesis that marmosets have digestive adaptations that aid in the digestion of gum that other callitrichids lack. © 1996 Wiley-Liss, Inc.     

Short-Term Dispersal Response of an Endangered Australian Lizard Varies with Time of Year

Dispersal is an important component in the demography of animal populations. Many animals show seasonal changes in their tendency to disperse, reflecting changes in resource availability, mating opportunities, or in population age structure at the time when new offspring enter the population. Understanding when and why dispersal occurs can be important for the management of endangered species. The pygmy bluetongue lizard is an endangered Australian species that occupies and defends single burrow refuges for extended periods of time, rarely moving far from the burrow entrance. However, previous pitfall trapping data have suggested movement of adult males in spring and of juveniles in autumn of each year. In the current study we compared behaviours of adult lizards each month, over the spring-summer activity period over two consecutive field seasons, to provide deeper understanding of the seasonal dispersal pattern. We released adult pygmy bluetongue lizards into a central area, provided with artificial burrows, within large enclosures, and monitored the behaviour and movements of the released lizards over a four day period. There was a consistent decline in time spent basking, amount of movement around burrow entrances, and rates of dispersal from the central release area from early spring to late summer. Results could be relevant to understanding and managing natural populations and for any translocation attempts of this endangered lizard species.     

Environmental Enrichment for New World Primates: Introducing Food-Irrelevant Objects and Direct and Secondary Effects

This study examined methods of environmental enrichment for zoo animals for 4 New World primate species: pygmy and Geoffrey's marmosets (Cebuella pygmaea and Callithrix geoffroyi), red-bellied tamarins (Saguinus labiatus), and golden- headed lion tamarins (Leontopithecus chrysomelus). Subjects were housed in groups at the Philadelphia Zoo. Baseline behavioral time budget data were collected, and stimulus objects were then introduced in succession to each enclosure. Each object included multiple manipulable subcomponents. Time budget data were collected while objects were in the enclosures, and subjects' contacts with objects were videotaped. Overall time budgets were significantly altered in only the red-bellied tamarins, the least active of the species, solely due to a shift from social grooming to passive social contact; when categories were collapsed into broader categories, this effect disappeared. Object contact occurred within the 1st hr for all species and ranged over nearly 2 orders of magnitude, from approximately 10 sec per subject (red-bellied tamarins) to approximately 700 sec per subject (Geoffrey's marmosets). Habituation was not evident within any 1st hr of observation but was shown when 1st hr observations were compared with those from subsequent days. This article discusses implications for environmental enrichment in zoos.     

Environmental Enrichment for New World Primates: Introducing Food-Irrelevant Objects and Direct and Secondary Effects

This study examined methods of environmental enrichment for zoo animals for 4 New World primate species: pygmy and Geoffrey's marmosets (Cebuella pygmaea and Callithrix geoffroyi), red-bellied tamarins (Saguinus labiatus), and golden- headed lion tamarins (Leontopithecus chrysomelus). Subjects were housed in groups at the Philadelphia Zoo. Baseline behavioral time budget data were collected, and stimulus objects were then introduced in succession to each enclosure. Each object included multiple manipulable subcomponents. Time budget data were collected while objects were in the enclosures, and subjects' contacts with objects were videotaped. Overall time budgets were significantly altered in only the red-bellied tamarins, the least active of the species, solely due to a shift from social grooming to passive social contact; when categories were collapsed into broader categories, this effect disappeared. Object contact occurred within the 1st hr for all species and ranged over nearly 2 orders of magnitude, from approximately 10 sec per subject (red-bellied tamarins) to approximately 700 sec per subject (Geoffrey's marmosets). Habituation was not evident within any 1st hr of observation but was shown when 1st hr observations were compared with those from subsequent days. This article discusses implications for environmental enrichment in zoos.     

Exudates as a fallback food for Callimico goeldii

Fallback foods have been defined as resources for which a species has evolved specific masticatory and digestive adaptations, and are consumed principally when preferred foods are scarce. In the present field investigation, we examine fungi, fruit, and exudate consumption in one group of Callimico goeldii in order to determine the importance of exudates as a fallback food for this species. Based on a total of 1,198 hr of quantitative behavioral data collected between mid-November 2002-August 2003, we found that pod exudates of Parkia velutina accounted for 19% of callimico feeding time in the dry season. This resource was not consumed in the wet season when fruits and fungi were the most common items in the diet. In the dry season of 2005 (July), the same callimico study group did not consume Parkia pod exudates. Instead, the group ate exudates obtained from holes gouged in tree trunks by pygmy marmosets and exudates resulting from natural weathering and insect damage on trunks, roots, and lianas. Pod exudates are reported to contain greater amounts of readily available energy than do trunk and root exudates, and were consumed throughout all periods of the day, particularly in the late afternoon. Trunk and root exudates were consumed principally in the morning. We propose that digestive adaptations of the hindgut, which enable callimicos to exploit fungi (a resource high in structural carbohydrates) year-round, predispose them to efficiently exploit and process exudates as fallback foods when other resources, such as ripe fruits, are scarce.     

Floral resources and hummingbirds on an island of flooded forest in Central Brazil

Nectar availability for hummingbirds was studied for two and a half years in an island of flooded forest in Uberlândia, MG, in the Cerrado region, the Neotropical savanna areas in Central Brazil. Flowering individuals of ten plant species from eight families that offered resources potentially used by hummingbirds were recorded along transects crisscrossing the area, which were surveyed every other week. The number of flowers was estimated for each plant. The volume and concentration of nectar were measured for a sample of flowers of each species, and the data were used to estimate the caloric content available per flower and the general resource availability in the area throughout the study period. Focal observations of hummingbird visits were carried out on blooming individuals of all plant species. Hummingbird flowers occurred throughout the study period between January 2001 and June 2003. Only three of the studied plants did not present clear ornithophilous features. Six hummingbird species were recorded in the area, but total nectar availability in the area was seldom sufficient for the daily energy requirements of a single bird. Therefore, it can be inferred from the study that these hummingbirds need to move among the mosaic of different plant physiognomies in the region in order to obtain enough energy for their survival. These movements may also contribute to increasing gene flow and regeneration of plant populations isolated in forest patches as the one studied here.     

Birth and perinatal behaviour in family groups of the common marmoset (Callithrix jacchus jacchus), compared to other primates

Birth and perinatal behaviour in five family groups of the common marmoset are described. Information is given on 16 births, seven of which are described in detail.The birth process was divided into five stages; data are presented on the durations of the stages and the behaviours exhibited by the female in each stage.Infant marmosets cling unaided to the pelage of the female from birth, and the behaviour of neonates and the reactions of the female to infants are discussed.The interactions of other group members to the mother and neonates were analysed. The adult male's first interactions with the neonates appeared to occur much earlier (less than one hour after birth) than in other non-human primate species.Perinatal behaviour in marmosets is compared to that recorded in other non-human primate species and discussed in relation to the social organisation of C. j. jacchus.     

Densities of Two Frugivorous Primates with Respect to Forest and Fragment Tree Species Composition and Fruit Availability

Conservation of wildlife populations requires extensive knowledge of their habitat requirements, efficient methods to evaluate habitat quality, and an understanding of the value of fragments and edges. Kibale National Park, Uganda has areas that differ in the densities of 2 species of frugivorous monkeys—Cercopithecus mitis and Lophocebus albigena—including one on an edge and forest fragments outside the park that lack both species. We compared the basal area densities of important food trees with primate densities. The density of Cercopithecus mitis correlates most strongly with the basal area density of all types of food trees combined. The density of Lophocebus albigena does not correlate with the basal area densities of any category of food trees or with fruit availability. An index of their density—number of groups seen per km walked—correlates to fruit availability but with marginal significance. Lack of a relationship between the basal area densities of food trees and density of Lophocebus albigena may be the result of a mismatch in scale between the forest area measured and their large home ranges. We compared the unused area of forest to the other areas of the forest and the fragments and found it had higher basal area densities in all food tree categories for both species than the fragments and lower basal area densities of most categories than the other parts of the forest, indicating that the fragments are poor quality and would probably be unused even if dispersal were likely.     

Ecology of <Emphasis Type="Italic">Callithrix kuhlii</Emphasis> and a Review of Eastern Brazilian Marmosets

We provide data on wild Callithrix kuhlii, a little studied species. We describe their ecology, focusing on demography, diet, and ranging patterns in 8 groups studied from 1995 to 1999. The groups averaged 4.3 individuals, with 1 breeding female and 1–2 adult males, and reproduction was seasonal. Evidence from nonstudy groups indicated the possibility of polygynous group structure. We observed group formation and the transfer of adults between groups. The marmosets ate 20 species of fruit and nectar and 5 exudate species. Home ranges were 34–39 ha, and daily path lengths averaged 1498 m. We include our data in a comprehensive review of eastern Brazilian marmosets to characterize their ecology. Callithrix kuhlii ate more fruit species and less gum species, and had larger home ranges and daily path lengths versus those of most congeners. There was also a tradeoff between travel time and other behaviors. Species with smaller home ranges spent more time foraging and resting and less time traveling than the ones with larger ranges. Attributes consistent with all species included their reliance on gum during fruit scarcity and preference for disturbed habitat. We explored factors relating to the variation in diet and ranging patterns within the eastern Brazilian marmosets, in particular by considering the species in relation to elevation and the extent and proximity of their distribution to the sea. However, large intraspecific variation resulting in part from variable levels of anthropogenic disturbance across sites confounded our ability to verify trends corresponding to the geographic characteristics.     

The effects of infant births on the sociosexual behavior and hormonal patterns of a cooperatively breeding primate (Cebuella pygmaea)

This study examined changes in the behavioral and hormonal patterns of cooperatively breeding pairs in a primate species with the passing of time and with specific reproductive events. We (1) compared patterns of sexual, agonistic, and affiliative behavior of newly paired pygmy marmosets with the same behavioral patterns immediately after the birth of their first set of infants; (2) determined if postpartum behavioral differences existed between pairs whose infants lived and those whose infants died; and (3) examined whether behavioral patterns changed over the course of ovarian cycles in parous pygmy marmosets as had been documented in nulliparous pairs. The behavior of pairs was recorded during daily half-hour focal samples for 60 days after pairing, and 30 or 60 days after the birth of infants for pairs whose litters died or lived, respectively. Daily urine samples from females during the study were analyzed for luteinizing hormone and pregnanediol glucuronide concentrations to determine dates of ovulation. The results indicated that males consistently altered their sexual behavior and olfactory monitoring of mates during periovulatory periods in the females' cycles both postpairing and postpartum, while similar rates of social and sexual behavior were maintained between the conditions. Sexual behavior occurred throughout the females' ovarian cycles. Peaks in sexual behavior during the periovulatory period in nulliparous pairs disappeared after the birth of infants. Pairs whose infants died showed higher rates of sexual behavior than pairs with surviving infants. Social and sexual behavior may function to maintain the relationship both during and outside of ovulation, especially with the loss of infants. © 1996 Wiley-Liss, Inc.     

Survival of Juvenile Pygmy Rabbits

ABSTRACT Until recently, natal behavior of pygmy rabbits (Brachylagus idahoensis) was largely unknown, and no information on survival of free-ranging juveniles was available. We evaluated survival of radiotagged juvenile pygmy rabbits at 2 sites in east-central Idaho, USA, during 2004 and 2005. We captured juveniles (n 58) shortly after they emerged from natal burrows. Mortality rates were high and variable, ranging from 27% for females during 2004 to 63% for males during 2005. Approximately 69% of mortalities were attributed to predation. We evaluated variables influencing juvenile survival through 18 weeks old using known-fate models in Program MARK. We expected survival to decline around the age of natal dispersal and to be lower for young born later in the season. We evaluated 14 candidate models that included sex, year, study area, and relative date of birth within each year. Model selection results did not indicate strong support for any single combination of variables, and 8 competing models all included effects of relative date of birth, year, and study area. These results revealed substantial variability in survival of juveniles across multiple factors, and we documented similar patterns for adult pygmy rabbits. Such high variability in survival over relatively small spatial and temporal scales might contribute to marked fluctuations in populations of pygmy rabbits and, hence, managers interested in monitoring this species might consider monitoring multiple populations across broader geographic areas to assess regional trends in numbers.