Taxonomic diversity of Cebuella in the western Amazon: Molecular, morphological and pelage diversity of museum and free-ranging specimens.

OBJECTIVES: We investigated the diversity of the pygmy marmoset, Cebuella pygmaea, by comparing genetic, morphological and pelage traits of animals from Peru and Ecuador. MATERIALS AND METHODS: We extracted DNA from museum specimen osteocrusts and from fecal samples collected from free-ranging individuals. We sequenced the mtDNA cytochrome b gene and the control region from samples collected at 13 different sites and used Bayesian inference and Maximum Likelihood to identify distinct clades. We took measurements of the crania of a subset of these specimens (n = 26) and ran a logistic regression to determine if any of the cranial measurements (n = 22) could predict a specimen's clade. In addition, we examined the pelage patterns of the museum specimens and photographs taken of free-ranging individuals and divided them into pelage types based on coloration of the underbelly. RESULTS: We identified two divergent clades, and two distinct groups with clear geographic boundaries within one of those clades. Two measurements of the zygomatic bone perfectly predicted a given individual's mtDNA clade. We found four distinct pelage patterns in our samples, but these patterns are variable within clades and among individuals within the same population. CONCLUSION: These analyses indicate that the two recognized subspecies of pygmy marmoset should be elevated to the species level (C. pygmaea and C. niveiventris) based on molecular and cranial differences but not on pelage patterns. We provide evidence on the geographic limits of the two clades and identify regions where additional sampling is required to better define the geographic distribution of the two clades.

Variable infant care contributions in cooperatively breeding groups of wild saddleback tamarins.

Among non-human primates, alloparental infant care is most extensive in callitrichines, and is thought to be particularly costly for tamarins whose helpers may suffer increased energy expenditure, weight loss, and reduced feeding time and mobility. The costs and benefits of infant care likely vary among group members yet very few wild studies have investigated variable infant care contributions. We studied infant care over an 8-month period in four wild groups of saddleback tamarins in Bolivia to evaluate: (a) what forms of infant care are provided, by whom, and when, (b) how individuals adjust their behavior (activity, vigilance, height) while caring for infants, and (c) whether individuals differ in their infant care contributions. We found that infant carrying, food sharing, and grooming varied among groups, and immigrant males-those who joined the group after infants were conceived-participated less in infant care compared to resident males. Adult tamarins fed less, rested more, and increased vigilance while carrying infants. Although we did not detect changes in overall activity budgets between prepartum and postpartum periods, tamarins spent more time scanning their environments postpartum, potentially reflecting increased predation risk to both carriers and infants during this period. Our study provides the first quantitative data on the timing and amount of infant carrying, grooming, and food transfer contributed by all individuals within and among multiple wild groups, filling a critical knowledge gap about the factors affecting infant care, and highlighting evolutionary hypotheses for cooperative breeding in tamarins.

The gut microbiome and metabolome of saddleback tamarins (Leontocebus weddelli): Insights into the foraging ecology of a small-bodied primate.

Body mass is a strong predictor of diet and nutritional requirements across a wide range of mammalian taxa. In the case of small-bodied primates, because of their limited gut volume, rapid food passage rate, and high metabolic rate, they are hypothesized to maintain high digestive efficiency by exploiting foods rich in protein, fats, and readily available energy. However, our understanding of the dietary requirements of wild primates is limited because little is known concerning the contributions of their gut microbiome to the breakdown and assimilation of macronutrients and energy. To study how the gut microbiome contributes to the feeding ecology of a small-bodied primate, we analyzed the fecal microbiome composition and metabolome of 22 wild saddleback tamarins (adult body mass 360-390 g) in Northern Bolivia. Samples were analyzed using high-throughput Illumina sequencing of the 16 S rRNA gene V3-V5 regions, coupled with GC-MS metabolomic profiling. Our analysis revealed that the distal microbiome of Leontocebus weddelli is largely dominated by two main bacterial genera: Xylanibacter and Hallella (34.7 ± 14.7 and 22.6 ± 12.4%, respectively). A predictive analysis of functions likely carried out by bacteria in the tamarin gut demonstrated the dominance of membrane transport systems and carbohydrate metabolism as the predominant metabolic pathways. Moreover, given a fecal metabolome composed mainly of glucose, fructose, and lactic acid (21.7 ± 15.9%, 16.5 ± 10.7%, and 6.8 ± 5.5%, respectively), the processing of highly fermentable carbohydrates appears to play a central role in the nutritional ecology of these small-bodied primates. Finally, the results also show a potential influence of environmentally-derived bacteria in colonizing the tamarin gut. These results indicate high energetic turnover in the distal gut of Weddell's saddleback tamarin, likely influenced by dominant bacterial taxa that facilitate dietary dependence on highly digestible carbohydrates present in nectar, plant exudates, and ripe fruits.

Mother's little helpers: What we know (and don't know) about cooperative infant care in callitrichines.

Since Darwin (), scientists have been puzzled by how behaviors that impose fitness costs on helpers while benefiting their competitors could evolve through natural selection. Hamilton's () theory of inclusive fitness provided an explanation by showing how cooperative behaviors could be adaptive if directed at closely related kin. Recent studies, however, have begun to question whether kin selection is sufficient to explain cooperative behavior in some species (Bergmüller, Johnstone, Russell, & Bshary, ). Many researchers have instead emphasized the importance of direct fitness benefits for helpers in the evolution of cooperative breeding systems. Furthermore, individuals can vary in who, when, and how much they help, and the factors that affect this variation are poorly understood (Cockburn, ; Heinsohn, ). Cooperative breeders thus provide excellent models for the study of evolutionary theories of cooperation and conflict (Cant, ).

Navigating in small-scale space: the role of landmarks and resource monitoring in understanding saddleback tamarin travel.

Recent studies of spatial memory in wild nonhuman primates indicate that foragers may rely on a combination of navigational strategies to locate nearby and distant feeding sites. When traveling in large-scale space, tamarins are reported to encode spatial information in the form of a route-based map. However, little is known concerning how wild tamarins navigate in small-scale space (between feeding sites located at a distance of ≤60 m). Therefore, we collected data on range use, diet, and the angle and distance traveled to visit sequential feeding sites in the same group of habituated Bolivian saddleback tamarins (Saguinus fuscicollis weddelli) in 2009 and 2011. For 7-8 hr a day for 54 observation days, we recorded the location of the study group at 10 min intervals using a GPS unit. We then used GIS software to map and analyze the monkeys' movements and travel paths taken between feeding sites. Our results indicate that in small-scale space the tamarins relied on multiple spatial strategies. In 31% of cases travel was route-based. In the remaining 69% of cases, however, the tamarins appeared to attend to the spatial positions of one or more near-to-site landmarks to relocate feeding sites. In doing so they approached the same feeding site from a mean of 4.5 different directions, frequently utilized different arboreal pathways, and traveled approximately 30% longer than then the straight-line distance. In addition, the monkeys' use of non-direct travel paths allowed them to monitor insect and fruit availability in areas within close proximity of currently used food patches. We conclude that the use of an integrated spatial strategy (route-based travel and attention to near-to-goal landmarks) provides tamarins with the opportunity to relocate productive feeding sites as well as monitor the availability of nearby resources in small-scale space.

Ancient DNA of the pygmy marmoset type specimen Cebuella pygmaea (Spix, 1823) resolves a taxonomic conundrum.

The pygmy marmoset, the smallest of the anthropoid primates, has a broad distribution in Western Amazonia. Recent studies using molecular and morphological data have identified two distinct species separated by the Napo and Solimões-Amazonas rivers. However, reconciling this new biological evidence with current taxonomy, i.e., two subspecies, Cebuella pygmaea pygmaea (Spix, 1823) and Cebuella pygmaea niveiventris (Lönnberg, 1940), was problematic given the uncertainty as to whether Spix's pygmy marmoset ( Cebuella pygmaea pygmaea) was collected north or south of the Napo and Solimões-Amazonas rivers, making it unclear to which of the two newly revealed species the name pygmaea would apply. Here, we present the first molecular data from Spix's type specimen of Cebuella pygmaea, as well as novel mitochondrial genomes from modern pygmy marmosets sampled near the type locality (Tabatinga) on both sides of the river. With these data, we can confirm the correct names of the two species identified, i.e., C. pygmaea for animals north of the Napo and Solimões-Amazonas rivers and C. niveiventris for animals south of these two rivers. Phylogenetic analyses of the novel genetic data placed into the context of cytochrome b gene sequences from across the range of pygmy marmosets further led us to re-evaluate the geographical distribution for the two Cebuella species. We dated the split of these two species to 2.54 million years ago. We discuss additional, more recent, subdivisions within each lineage, as well as potential contact zones between the two species in the headwaters of these rivers.

Mycophagy and its influence on habitat use and ranging patterns in Callimico goeldii.

Mycophagy has been documented in a number of species of marmosets and lion tamarins (Callitrichinae) but its effect on ranging behavior is not known. We present the results of 10 years of research on five groups of Goeldi's monkey (Callimico goeldii) at a field site in northwestern Bolivia. We studied the diet and ranging behavior of two of the groups. On average, groups contained 4.5 individuals (range 2.0-9.0), but they gradually decreased in size until only the breeding female remained in the home range. The annual diet was composed of fungi (31.1-34.9%), fruits (34.0-40.6%), prey (17.4-30.1%), and exudates (1.0-10.9%). They had large home ranges (114-150 ha) and over time individuals tended to shift their core areas of use. They used secondary and bamboo forest and forest with dense understories more than expected based on availability. We suggest that the large home ranges and shifting core areas used by C. goeldii are components of a foraging strategy to track patchy, low density, and ephemeral fungal fruiting bodies. Our results, along with data published on other callitrichines, indicate that groups of Leontopithecus, Callithrix, and Callimico that eat fungi have larger home ranges than those that do not. Mycophagy is one of the several factors that evidently affect home range size in callitrichines. Fungi are clearly an important food source for a number of populations, but additional studies are needed to determine why some eat fungi frequently while others do not.

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.

Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys.

Certain types of inanimate environmental enrichment have been shown to positively affect the behavior of laboratory primates, as has housing them in appropriate social conditions. While social housing is generally advocated as an important environmental enhancement, few studies have attempted to measure the influence of social conditions on the effects of inanimate enrichment or to compare the relative merits of social and inanimate enhancements. In the present study, inanimate enrichment (predominately physical and feeding enhancements) resulted in increased species-typical behavior for socially restricted subjects. However, social enrichment (living in groups) appeared to be more beneficial for young rhesus monkeys, leading to increased species-typical activities and decreased abnormal activities. The behavior of one cohort of yearling rhesus monkeys (Macaca mulatta) housed in small peer groups was compared with the behavior of four yearling cohorts housed in single cages. Half the animals in each cohort received a three-phase enrichment program and the rest served as controls. Group-housed yearlings spent significantly more time feeding and exploring and significantly less time behaving abnormally, self-grooming, and drinking than did singly housed yearlings. Enriched subjects spent significantly more time playing by themselves, and significantly less time self-grooming and exploring than did controls. Among group-housed subjects only, there were no differences between enriched and control monkeys. Captive primates should be housed socially, whenever appropriate, as the first and most important step in an enrichment program, with the provision of inanimate enhancements being considerably less important. Limited resources for inanimate enrichment programs instead should be focused on those individuals who can not be housed socially. © 1996 Wiley-Liss, Inc.

Maternal care and infant development in Callimico goeldii and Callithrix jacchus.

Callimico goeldii gives birth to single offspring, whereas other callitrichids, including Callithrix jacchus, twin. This study compares maternal effort and infant development in C. goeldii and C. jacchus; it is the first study to look at nursing frequency. Infants were observed from birth for 7 weeks in two captive groups each of C. goeldii and C. jacchus. C. goeldii mothers physiologically invested the same or less than C. jacchus mothers. C. goeldii mothers gained the same amount of weight during pregnancy in absolute terms as did the smaller C. jacchus. This results in a smaller gain in proportion to maternal weight but an equivalent proportional gain on a per fetus basis. C. goeldii mothers nursed their infants less based on duration of nursing bouts compared with C. jacchus mothers. C. goeldii mothers transported their infants exclusively through the first 2 weeks of life, which is longer than C. jacchus mothers, who exclusively transported infants only during the first week of life. As maternal infant carriage declined, other group members transported offspring in both species. C. goeldii infants engaged in independent locomotive sequences later in development and tasted solid foods less frequently than C. jacchus infants when compared at equivalent ages. A single, opportunistic milk sample obtained from a C. goeldii mother when her infant was 48 days old indicates that C. goeldii milk contains gross energy from crude protein within the range of variation observed in Callithrix milk. Despite the similarities in milk quality and prenatal effort in individual fetuses, C. goeldii infants gain weight faster from 0 to 18 months than do C. jacchus infants. A reduction in litter size allows C. goeldii mothers to spend more time carrying their infant and to delay weaning, thereby allowing accelerated infant and juvenile growth rates compared with C. jacchus.

Niche expansion of a cryptic primate, Callimico goeldii, while in mixed species troops.

We examined the effects of polyspecific associations on the behavior of one group of Callimico goeldii in northwestern Bolivia. Data were collected for 1 year using focal animal sampling at 5-min intervals, for a total of 1,375 observation hours. In total, C. goeldii formed mixed species troops with five groups of Saguinus fuscicollis and six groups of S. labiatus, and these were maintained during 81% of observations. C. goeldii rested more and traveled less while alone than while associated, but neither vigilance behavior in the understory nor habitat use were affected by association status. The composition of the group's diet was different while alone (higher in structural carbohydrates [fungi] and lower in simple sugars [ripe fruits] and protein [insects]) than while associated (fungi 65 vs. 37%; fruits 13 vs. 32%; insects 5 vs. 15%). We propose therefore, that C. goeldii has a lower quality and more narrowly based diet while alone as compared to while associated. The factors that allow for this dietary expansion while in mixed species troops require further investigation.

Distribution and density of Callimico goeldii in the Department of Pando, Bolivia.

A survey of the distribution and density of Callimico goeldii was conducted at five sites across northwestern Bolivia, in the Department of Pando. C. goeldii was found at two sites north of the Manuripi River, with high densities at one site located along the Acre River. Estimates of habitat availability at these sites suggest that C. goeldii reaches high densities in areas with low human density and well established and extensive bamboo forests. These results, when reviewed with those of prior studies, indicate that the patchy distribution of C. goeldii in Pando is a result of both riverine barriers and the availability of bamboo habitat.

Forest use and activity patterns of Callimico goeldii in comparison to two sympatric tamarins, Saguinus fuscicollis and Saguinus labiatus.

Callimico goeldii, Saguinus fuscicollis, and S. labiatus are sympatric in northern Bolivia and differ from each other in patterns of spatial and structural use of their environment. C. goeldii has a home range five times larger than that of mixed-species troops of S. fuscicollis and S. labiatus. The larger overlapping home range of C. goeldii allows it to move among Saguinus troops, giving it access to a wide range of different microhabitats. All three species use the most common microhabitat in the area, primary forest with dense understory, more than any other microhabitat type. C. goeldii habitat use varies by season, with bamboo and Heliconia microhabitats used more during the dry season. Each species shows preferences for different height classes: C. goeldii is found almost exclusively in the understory, S. fuscicollis uses the understory and middle canopy, and S. labiatus is found mostly in the middle canopy. These height class preferences are reflected in each species' locomotor styles, with C. goeldii showing the highest rates of vertical clinging and leaping, and S. labiatus showing the highest rates of branch-to-branch leaping and quadrupedal movement. The results suggest that C. goeldii may be restricted to forests with dense understory and a mosaic of other microhabitats. Furthermore, C. goeldii does not appear to use its tegulae for large branch foraging, but rather for vertical clinging and leaping between small vertical supports.