The gut microbiome of exudivorous marmosets in the wild and captivity.

Mammalian captive dietary specialists like folivores are prone to gastrointestinal distress and primate dietary specialists suffer the greatest gut microbiome diversity losses in captivity compared to the wild. Marmosets represent another group of dietary specialists, exudivores that eat plant exudates, but whose microbiome remains relatively less studied. The common occurrence of gastrointestinal distress in captive marmosets prompted us to study the Callithrix gut microbiome composition and predictive function through bacterial 16S ribosomal RNA V4 region sequencing. We sampled 59 wild and captive Callithrix across four species and their hybrids. Host environment had a stronger effect on the gut microbiome than host taxon. Wild Callithrix gut microbiomes were enriched for Bifidobacterium, which process host-indigestible carbohydrates. Captive marmoset guts were enriched for Enterobacteriaceae, a family containing pathogenic bacteria. While gut microbiome function was similar across marmosets, Enterobacteriaceae seem to carry out most functional activities in captive host guts. More diverse bacterial taxa seem to perform gut functions in wild marmosets, with Bifidobacterium being important for carbohydrate metabolism. Captive marmosets showed gut microbiome composition aspects seen in human gastrointestinal diseases. Thus, captivity may perturb the exudivore gut microbiome, which raises implications for captive exudivore welfare and calls for husbandry modifications.

Dental Signatures for Exudativory in Living Primates, with Comparisons to Other Gouging Mammals.

Exudativory, the consumption of gums, is an obligate or a facultative dietary niche for some primates and marsupials. Exudativory has been cited as a dietary niche that may have been present in early primates, so finding a dental signature for exudativory is highly desirable. The present study combines exudativorous lorisoids (galagos and lorises) into one sample to compare to closely related, non-exudativorous lorisoids to search for a consistent dental signature of exudativory. Linear measurements were taken from the toothcomb, P2 , M3 , upper canine, and P2 from skulls of 295 adult galagids and lorisids. Also, differential distribution of enamel on the anterior teeth was qualitatively investigated as a dental signature for gouging (a behavior that facilitates some exudativory) by micro-CT scanning one specimen each from two gougers, Nycticebus coucang and Callithrix jacchus, and two non-gougers, Perodicticus potto, and Saguinus fuscicollis. Non-primate gouging mammals, the vampire bat Desmodus rotundus and the sugar glider Petaurus breviceps, were compared to non-gouging relatives. Statistical analysis revealed that exudativorous galagos and lorises had significantly (P < 0.05) reduced M3 relative to non-exudativorous galagos and lorises. While the sample sizes for assessing enamel thickness were small, preliminary results show that gouging primates and non-primate mammals have reduced lingual enamel thickness on the anterior dentition compared to non-gouging relatives. We suggest that reduction of mastication, and, therefore, M3 dimensions are a likely dental signature for exudativory in Primates. While broader samples are needed to statistically confirm, differential distribution of enamel in the anterior dentition may also be a signature of exudativory. Anat Rec, 2019. © 2018 Wiley Periodicals, Inc. Anat Rec, 303:265-281, 2020. © 2018 American Association for Anatomy.

A Novel Method for Assessing Enamel Thickness Distribution in the Anterior Dentition as a Signal for Gouging and Other Extractive Foraging Behaviors in Gummivorous Mammals.

Gummivory poses unique challenges to the dentition as gum acquisition may often require that the anterior teeth be adapted to retain a sharp edge and to resist loading because they sometimes must penetrate a highly obdurate substrate during gum extraction by means of gouging or scraping. It has been observed previously that the enamel on the labial surface of the teeth used for extraction is thicker relative to that on the lingual surface in taxa that extract gums, while enamel is more evenly distributed in the anterior teeth of taxa that do not regularly engage in extractive behaviors. This study presents a quantitative methodology for measuring the distribution of labial versus lingual enamel thickness among primate and marsupial taxa in the context of gummivory. Computed microtomography scans of 15 specimens representing 14 taxa were analyzed. Ten measurements were taken at 20% intervals starting from the base of the crown of the extractive tooth to the tip of the cutting edge across the lingual and labial enamel. A method for including worn or broken teeth is also presented. Mann-Whitney U tests, canonical variates analysis, and between-group principal components analysis were used to examine variation in enamel thickness across taxa. Our results suggest that the differential distribution of enamel thickness in the anterior dentition can serve as a signal for gouging behavior; this methodology distinguishes between gougers, scrapers, and nonextractive gummivores. Gouging taxa are characterized by significantly thicker labial enamel relative to the lingual enamel, particularly towards the crown tip. Examination of enamel thickness patterning in these taxa permits a better understanding of the adaptations for the extraction of gums in extant taxa and offers the potential to test hypotheses concerning the dietary adaptations of fossil taxa.

Exudativory in the Asian loris, Nycticebus: Evolutionary divergence in the toothcomb and M3.

OBJECTIVES: Slow lorises (Nycticebus spp.) are obligate exudativores that gouge tree bark. Dental adaptations for gouging within marmosets, the only other known primate obligate exudativore, are well-known but dental adaptations in Nycticebus are largely unidentified. In an effort to more completely understand potential dental adaptions within Nycticebus and the evolution of this dietary niche within Primates as an order, the present study examined dental morphometrics in the Asian lorises (Nycticebus and Loris). MATERIALS AND METHODS: We compared dental morphometrics between Nycticebus and the insectivorous slender lorises (Loris). Measurements from the toothcomb and select other teeth were taken from 92 specimens. Each variable was scaled by the geometric mean and resulting mean ratios were statistically compared between groups. A biomechanical shape variable was also calculated to estimate the ability of the toothcomb to resist bending that may be experienced during gouging. RESULTS: Toothcombs in Nycticebus were significantly (P < 0.05) more narrow, shorter, and thicker than those in Loris and had a higher calculated ability to withstand bending forces. Nycticebus also had reduced size in the last lower molar relative to Loris. CONCLUSIONS: The more robust, "squared off" toothcomb in Nycticebus matches behavioral observations that these primates gouge to access exudates. Results of the present study indicate that the toothcomb is the likely candidate for the dental tool used in gouging. The size reduction of the lower last molar in Nycticebus, a trait also found in a previous study in exudativorous galagos, may indicate that there is reduced selective pressure in a diet where little mastication would be needed to mechanically process exudates. These results may indicate that reduction in molar size could be a potential dental signature for exudativory, but further studies on a wider phylogenetic range of exudativorous primates would be necessary.

Modeling the origins of mammalian sociality: moderate evidence for matrilineal signatures in mouse lemur vocalizations.

INTRODUCTION: Maternal kin selection is a driving force in the evolution of mammalian social complexity and it requires that kin are distinctive from nonkin. The transition from the ancestral state of asociality to the derived state of complex social groups is thought to have occurred via solitary foraging, in which individuals forage alone, but, unlike the asocial ancestors, maintain dispersed social networks via scent-marks and vocalizations. We hypothesize that matrilineal signatures in vocalizations were an important part of these networks. We used the solitary foraging gray mouse lemur (Microcebus murinus) as a model for ancestral solitary foragers and tested for matrilineal signatures in their calls, thus investigating whether such signatures are already present in solitary foragers and could have facilitated the kin selection thought to have driven the evolution of increased social complexity in mammals. Because agonism can be very costly, selection for matrilineal signatures in agonistic calls should help reduce agonism between unfamiliar matrilineal kin. We conducted this study on a well-studied population of wild mouse lemurs at Ankarafantsika National Park, Madagascar. We determined pairwise relatedness using seven microsatellite loci, matrilineal relatedness by sequencing the mitrochondrial D-loop, and sleeping group associations using radio-telemetry. We recorded agonistic calls during controlled social encounters and conducted a multi-parametric acoustic analysis to determine the spectral and temporal structure of the agonistic calls. We measured 10 calls for each of 16 females from six different matrilineal kin groups. RESULTS: Calls were assigned to their matriline at a rate significantly higher than chance (pDFA: correct = 47.1%, chance = 26.7%, p = 0.03). There was a statistical trend for a negative correlation between acoustic distance and relatedness (Mantel Test: g = -1.61, Z = 4.61, r = -0.13, p = 0.058). CONCLUSIONS: Mouse lemur agonistic calls are moderately distinctive by matriline. Because sleeping groups consisted of close maternal kin, both genetics and social learning may have generated these acoustic signatures. As mouse lemurs are models for solitary foragers, we recommend further studies testing whether the lemurs use these calls to recognize kin. This would enable further modeling of how kin recognition in ancestral species could have shaped the evolution of complex sociality.

Paternal kin recognition in the high frequency / ultrasonic range in a solitary foraging mammal.

BACKGROUND: Kin selection is a driving force in the evolution of mammalian social complexity. Recognition of paternal kin using vocalizations occurs in taxa with cohesive, complex social groups. This is the first investigation of paternal kin recognition via vocalizations in a small-brained, solitary foraging mammal, the grey mouse lemur (Microcebus murinus), a frequent model for ancestral primates. We analyzed the high frequency/ultrasonic male advertisement (courtship) call and alarm call. RESULTS: Multi-parametric analyses of the calls' acoustic parameters and discriminant function analyses showed that advertisement calls, but not alarm calls, contain patrilineal signatures. Playback experiments controlling for familiarity showed that females paid more attention to advertisement calls from unrelated males than from their fathers. Reactions to alarm calls from unrelated males and fathers did not differ. CONCLUSIONS: 1) Findings provide the first evidence of paternal kin recognition via vocalizations in a small-brained, solitarily foraging mammal. 2) High predation, small body size, and dispersed social systems may select for acoustic paternal kin recognition in the high frequency/ultrasonic ranges, thus limiting risks of inbreeding and eavesdropping by predators or conspecific competitors. 3) Paternal kin recognition via vocalizations in mammals is not dependent upon a large brain and high social complexity, but may already have been an integral part of the dispersed social networks from which more complex, kin-based sociality emerged.

Factors affecting wounding aggression in a colony of captive chimpanzees (Pan troglodytes).

Previous research has suggested that chimpanzees (Pan troglodytes) display higher levels of aggression in captivity than in the wild. One of the challenges of captive management, therefore, is to balance the chimpanzees' need for social interaction with managements' desire to minimize wounding and aggression. Various captive studies have examined the effects of individual and social variables on the frequency of wounding aggression, but none have examined these variables simultaneously. We collected retrospective wounding data for severe wounds from 83 captive chimpanzees (36 males, 47 females) from January 1993 to December 2003. The context of the wounding event, including individual age and sex, group age and sex composition, group duration, and portion of the week (weekday vs. weekend) were collected. Logistic regression analysis was performed to determine which variables had a significant effect on the probability of a severe wounding event. The sex and age composition of the group, group duration, and portion of the week had a statistically significant association with wounding. All-male groups (Odds Ratio (OR)=6.738) had the highest risk of wounding aggression, with uni-male groups (OR=3.311) having the next largest. Compared to individuals in all sub-adult groups, individuals in either all-adult (OR=4.516) or mixed-age (OR=3.587) groups had a higher risk of wounding. There was an inverse association between group duration and wounding (OR=0.821). Finally, there was an increased risk of wounding during the work week (OR=1.653). These results suggest that captive management should pay close attention to group composition, as well as levels of human activity, when devising strategies to reduce captive chimpanzee aggression.

Limb growth in captive Galago senegalensis: getting in shape to be an adult.

Since primate infants are not simply miniature adults, adult shape results from differential growth patterns of individual body segments. Initially an infant relies on its mother for transportation, and later begins independent locomotion. Skeletal growth patterns must meet the functional demands of independent locomotion. In this study we sought to determine whether Galago senegalensis braccatus follow the general primate pattern of decreasing intermembral index (IMI) throughout ontogeny. We also asked whether ontogenetic attainment of adult limb proportions coincides with attainment of independent locomotion, i.e., do infants reach adult limb proportions near the time they begin independent locomotion (approximately 7 weeks of age)? Mixed-longitudinal data were taken from a sample of 10 captive-born Galago senegalensis. Linear lengths of the trunk, arm, forearm, thigh, and leg were measured in the animals from birth until they were approximately 500 days old. The IMI and the ratio of each limb segment to both trunk length and the cube root of body mass were calculated. The results of a Mann-Whitney Wilcoxon rank-sum test for unmatched samples indicate that G. senegalensis do exhibit the primate pattern of decreasing IMI throughout ontogeny, and that the IMIs of infants at the time of initial locomotor independence are significantly higher than those of adult IMIs. Some (but not all) measures of relative limb lengths differed between neonates or 7-week-old infants and adults. Therefore, the hypothesis that infants acquire adult limb proportions by the time they begin independent locomotion is not supported by this study. The current results indicate that ontogenetic shape changes in galagos are a complex process and apparently cannot be explained by simple initial locomotor competency.

Sex differences in the behavior and the social interactions of immature Galago senegalensis braccatus.

There is little detailed documentation of immature behavior, especially mother-offspring interactions, for nocturnal prosimians, and few studies have examined sex differences in mother-offspring interactions. This study compares the behavior of captive-born Galago senegalensis braccatus, the Senegal galago, from 1 to 20 weeks of age for 3-5 females and 4-6 males. The subjects lived in social groups, on a reversed light cycle. Three 10-min focal samples were taken each week, for each subject, during each of the 6 most active hours of the waking cycle (night). Locally weighted regression scatterplot smoothing analysis was used to test for sex differences in behavior. There were no sex differences in most forms of mother-offspring contact, including nursing, control of proximity with the mother or grooming. Females were more active than males in the rate of solitary acrobatic play and, only after the age of weaning, in locomotion. Altogether, these observations suggest that the sexes might not present more energetic 'costs' to mothers. There were tendencies for female immatures to play with the mother more than male immatures did, and a tendency for the males to investigate the cage more than the females. Male and female immatures groomed non-mother group mates in equivalent amounts. Since males are likely the dispersing sex in galagos, these differences might be reflective of later dispersal patterns. However, comparisons are needed with a female dispersal species (e.g. chimpanzees) to test this hypothesis. Alternative hypotheses concerning the 'cost' and/or 'value' of sons versus daughters need to be explored.

Ecological attributes recorded in stable isotope ratios of arboreal prosimian hair.

Carbon and nitrogen stable isotope ratios were measured in hair samples from two species of Galago from Gedi Ruins National Monument in eastern Kenya and from Lepilemur leucopus from Beza Mahafaly Special Reserve in southern Madagascar. Forest structure was generally similar in the two areas but average rainfall was lower in Madagascar. Species average 13C values varied with feeding height in the forest canopy and with average rainfall level as expected from reported variation in plant 13C values. G. garnettii, which feeds higher in the forest canopy, had less negative 13C values than G. zanzibaricus, which spends more time below 5 m. L. leucopus, from a drought-afflicted forest, had less negative hair 13C values than the two galago species. The values within the Lepilemur sample showed a positive linear relation with percent dependence on a CAM tree species and with xeric conditions within the species reserve. Nitrogen stable isotope ratios varied with trophic level of feeding and with time spent feeding on leguminous plants. The insectivorous galagos had significantly more positive 15N values than the folivorous L. leucopus. Within the Lepilemur sample, 15N values varied inversely with the percent of feeding time spent on leguminous plants. The range of 15N and 13C values in each of the prosimian species is larger than reported for animals fed monotonous diets and for New World monkey species. The monkey species feed as groups of individuals whereas the prosimians have solitary feeding habits. The ranges in the prosimian species apparently reflect the greater variation in diet among individual prosimians compared to individual monkeys. The isotope data reported here are equivalent, on average, to those reported for other arboreal species from similar forest habitats and with similar dietary habits. This supports the use of such data for paleoecological reconstruction of forest and woodland systems and diet reconstruction of extinct primate populations and species.

Excrement distribution and habitat use in Rhinopithecus bieti in winter.

Winter ranging patterns of Rhinopithecus bieti were determined using feces as the ranging trace. The appearance of the feces was unique in the study habitat. The sampled habitats were a well-forested area and a partly altered one. Analyses of excrement distribution showed: (1) monkeys tended to use the upper part of the forest belt, ranging between 3,900 and 4,100 m above sea level; (2) monkeys came to the ground and used the partly altered habitat, where only some forest remained; (3) the structure of resources had little influence on determining the ranging elevation; and (4) the animals spent more time in the local valley than on the local ridge, probably using the former as a sleeping site.

Social organization of Galagos in Kenyan coastal forests: II. Galago garnettii.

The social organization of Galago garnettii was studied for the first time and the study included data from two different sites in the coastal forests of Kenya. A combination of mark-recapture and radio-tracking techniques was used to investigate patterns of inter- and intrasexual home range overlap. Patterns of range use were established by radio tracking focal individuals. Adult females of different ages shared highly overlapping ranges, while like-aged females showed little range overlap. Females matured and had their first infants in their natal ranges. Adult males' ranges were larger than those of females and overlapped them extensively. Resident adult males showed little range overlap with each other, unless they were of different ages. Turnover of males was frequent in both populations. Males probably dispersed from their natal ranges. Adults rarely slept together. The social organization of G. garnettii is relatively similar to that of the closely related G. crassicaudatus of southern Africa but contrasts with that of its sympatric congener, G. zanzibaricus. The differences and similarities between these three species are discussed in relation to diet and body size.

Social organization of Galagos in Kenyan coastal forests: I. Galago zanzibaricus.

The social organization of Galago zanzibaricus was studied for the first time and the study included data from two different sites in the coastal forests of Kenya. A combination of mark-recapture and radio-tracking techniques was used to investigate patterns of inter- and intrasexual home range overlap. Associations in sleeping groups indicated social ties between individuals. Patterns of range use were established by radio-tracking focal individuals. Adult males generally had nonoverlapping ranges, shared with one or two females and their offspring with which the male regularly slept. Young females remained longer in their natal ranges than males and reproduced within their natal ranges. Range size and distance traveled per night were similar between the sexes; both sexes probably defended territories. None of the other galago (bushbaby) species studied to date show the degree of close male-female association found in G. zanzibaricus. This study thus extends the variety of social organization documented in nocturnal prosimians.

Space or novelty?: Effects of altered cage size on Galago behavior.

The influences of cage size and novelty on the behavior of Galago senegalensis braccatus were examined in two captive groups (five adults and one immature per group) having similarly furnished but unequally sized cages. One group experienced expansion, and the other experienced contraction of space. Each group experienced the novelty of a new cage and return to its old cage. Exploration, nonsocial activity, and social sniffing behaviors were most frequent in both groups during the novelty phase independent of cage size. These behaviors remained elevated after return to the original cage. This pattern indicated that novelty, not space, was responsible for these behavioral changes. The increase in social sniffing indicated that group members may use olfactory cues to recognize each other, expecially when the setting is novel. In both groups, frequencies of displacements and chases were highest in the smaller space. Group differences in behavior prior to cage change also influenced a group's response to change.

Reproductive patterns in galagos (Galago zanzibaricus and Galago garnettii) in relation to climatic variability.

The reproductive patterns (birth seasonality, litter size, litters per year) of two sympatric species of galago (Galago zanzibaricus and G. garnettii) were studied in a coastal forest in Kenya for a two-year period. Trap-retrap and radio tracking methods were employed. G. zanzibaricus has one infant twice per year; G. garnettii has one infant once per year. Both species are seasonal breeders. These East African galagos are intermediate in reproductive patterns when compared with galagos from South African woodland (G. senegalensis moholi and G. crassicaudatus umbrosis) and West African rainforest (G. alleni and G. demidovii). Climatic patterns (total annual rainfall, seasonal variability of rainfall, variability in total annual rainfall, and annual temperature variability) are also compared for the three regions. Climatically, East Africa is intermediate between West and South Africa in total annual rainfall and in seasonality of rainfall, but not in year-to-year variability in rainfall. East Africa shows the highest variability in annual rainfall. South Africa has the coldest dry seasons and highest variability in temperatures. The results of this study suggest that "r-selection" and "K-selection" do not provide adequate explanations of galago reproductive patterns.