Socio-sexual behavior of female northern muriquis (Brachyteles hypoxanthus)

Female northern muriquis (Brachyteles hypoxanthus) are known to engage in frequent copulations with multiple partners, a pattern that in other primates has been attributed to various functions such as confusing paternity, reducing male aggression, or ensuring fertilization. However, in some female primates, promiscuity is restricted to times when conceptions are unlikely. We investigated whether female northern muriquis might exhibit a similarly mixed strategy by examining their mating, social, and activity patterns during their conception cycles versus other times. Systematic behavioral data were collected during an 18-month period between August 2001 and February 2003 on 13 adult females in a well-studied group at the RPPN-Feliciano Miguel Abdala, Minas Gerais, Brazil. Females mated on an average of 12.5+/-7.9 days during the study period, and spent significantly less time resting and engaging in non-sexual social behaviors, and significantly more time in sexual behaviors on days that they copulated than on days they did not. Three of the eight females for which sufficient data were available copulated significantly more often with their spatially closest non-kin associates, and four of five females that could be analyzed copulated significantly more often with their most frequent non-kin embrace partners. Comparisons between conception and non-conception periods revealed no differences in female activity budgets or in either the number of copulations or the number of different mating partners per female. Our results suggest that some females mate preferentially with close associates and social partners, but there is no indication that females alter their behavior during the cycles in which they conceive.     

Mother-offspring associations in northern muriquis, Brachyteles hypoxanthus

Maternal care of offspring is ubiquitous among primates, but its duration varies across species due to factors such as dispersal patterns and social dynamics, which influence opportunities for and potential benefits of maternal investment in older offspring, respectively. We examined mother-offspring associations in wild northern muriquis (Brachyteles hypoxanthus), in which males are philopatric, females typically disperse before puberty, and social relationships among and between males and females are egalitarian. Associations were systematically recorded between ten mothers, each with two-six offspring in the study group, and all group members from August 2003-May 2004 at the RPPN-Feliciano Miguel Abdala in Minas Gerais, Brazil. Infants of both sexes received similarly high percentages of their mothers' association time. Mothers without infants also maintained strong associations with their youngest juvenile sons. Mothers did not spend consistently more time associating with either juvenile or adult sons than daughters. Our finding of non-preferential associations between muriqui mothers and their older male offspring suggests that extended maternal investment in offspring may be of minimal value in their egalitarian society compared with its value for species living in hierarchical societies.     

Social cliques in male northern muriquis Brachyteles hypoxanthus

Analyses of spatial relationships and social interactions provide insights into the social structure of animal societies and the ways in which social preferences among and between dyads affect higher order social relationships.In this paper we describe the patterns of spatial associations and social interactions among adult male northern muriquis in order to evaluate the dynamics of their social networks above the dyadic levels.Systematic observations were made on the 17 adult males present in a multi-male/multi-female group from April 2004 through February 2005,and in July 2005.Analyses of their spatial relationships identified two distinct male cliques; some adult males (called N males) were more connected to the females and immatures than other adult males (MU males),which were more connected to one another.Affiliative interactions were significantly higher among dyads belonging to the same clique than to different cliques.Although frequencies of dyadic agonistic interactions were similarly low among individuals within and between cliques,MU males appeared to be subordinate to N males.Nonetheless,there were no significant differences in the copulation rates estimated for MU males and N males.Mutual benefits of cooperation between MU and N cliques in intergroup encounters might explain their ongoing associations in the same mixed-sex group [Current Zoology 58 (2):342-352,2012].     

Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus).

We monitored the birth patterns of sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus) during a 4‐yr period from October 1996 to August 2000 at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Brown howler monkey births (n = 34) occurred throughout the year, and birth frequencies did not differ between rainy and dry season months. The aseasonal birth patterns of the howler monkeys differed significantly from the dry season concentration and dry month peak in muriqui births (n = 23). We found no effects of infant sex or the number of females on interbirth intervals (IBIs) in our 10 howler monkey study troops. IBIs of brown howler monkeys averaged 21.2 ± 2.5 mo (n = 8, median = 21.0 mo), and were significantly shorter following dry season births than rainy season births. Their IBIs and yearling survivorship (74%) were similar to those reported for other species of howler monkeys, but yearling survivorship was much lower than that of muriquis (94%), whose IBIs were more than 12 mo longer than those of the howler monkeys. Our study extends comparative knowledge of birth patterns in Alouatta to a poorly known species, and provides insights into the different ways in which diet and life history may affect the timing of births in large‐bodied platyrrhines under the same seasonal ecological conditions. Am. J. Primatol. 55:87–100, 2001. © 2001 Wiley‐Liss, Inc.     

Hormonal changes during the mating and conception seasons of wild northern muriquis (Brachyteles arachnoides hypoxanthus)

We investigated hormonal and behavioral changes in wild male and female northern muriquis (Brachyteles arachnoides hypoxanthus) at the Estação Biológica de Caratinga, Minas Gerais, Brazil, during a 6‐mo period that encompassed the onset of the 1998–1999 mating and conception seasons. Individual females resumed mating with the resumption of ovarian cycling, which was not synchronized among them or related to their cortisol levels. Females experienced two to seven cycles prior to conceiving, and the first conception occurred 2 mo after the onset of the group's mating season. There were no differences in female cortisol levels across their premating, mating, and conception conditions. Cortisol levels were significantly higher in females than in males prior to the conception season, consistent with the prediction that energy reserves may be associated with breeding readiness in females, but not males, in this species. The sustained elevation in male cortisol occurred after the peak in their sexual activity, which resulted in the first conception of the year. Male cortisol levels were positively correlated between years that were similar in rainfall, but differed in the timing of sexual and reproductive events. The timing of cortisol elevations in males appears to be generally regulated by environmental cues, but is responsive to fine‐tuning by social and behavioral cues related to the unpredictable timing of reproductive opportunities within their extended mating season. Am. J. Primatol. 61:85–99, 2003. © 2003 Wiley‐Liss, Inc.     

A case of infant swapping by wild northern muriquis (<Emphasis Type="Italic">Brachyteles hypoxanthus</Emphasis>)

Allo-parenting has been observed in a variety of female primates, and typically infants are reunited with their biological mothers assuming that their mothers are alive. We observed an exception to this pattern when two wild northern muriquis (Brachyteles hypoxanthus) exchanged infants of different sexes and then reared their adopted infants through weaning. The process of this exchange began when the infants were 4 and 8 days old, respectively. The mother of a 4-day old female carried and nursed her own daughter and the 8-day old son of a second female. The exchange ended when the second mother was first observed carrying the wrong infant 1.5 days later. This observation raises questions about the age and mechanisms of mother–infant recognition in this species, and about assumptions of mother–infant relatedness based on behavioral observations alone.     

Adult male-infant interactions in wild muriquis (Brachyteles arachnoides hypoxanthus)

We examined adult male-infant interactions in wild muriquis (Brachyteles arachnoides hypoxanthus), a species in which close relatedness among philopatric males and high paternity uncertainty should minimize both aggressive and affiliative behavior by males toward infants. As expected, male-infant interactions were extremely rare during this 10-month field study. None were observed in over 236 hr of observation on a cohort of six infants (0 – 13 months old). The 29 interactions observed ad lib involved 5 of the 6 infants and 9 of the 16 adult males in the group. All of the male-infant interactions were affiliative, but extremely brief. The median duration of interactions was only 0.33 min, and none lasted longer than 1.52 min. Infants always initiated, and nearly always terminated, their interactions with adult males. The indifference that appears to characterize muriqui male-infant interactions differs from the ways in which other male primates interact with infants when protection of genetic interests or investment in mating effort are involved.     

Effects of Group Size on Ranging Patterns in Brachyteles arachnoides hypoxanthus

We collected systematic data on the home range and day ranges of one group of 57–63 muriquis (Brachyteles arachnoides hypoxanthus) at the Estação Biológica de Caratinga, Minas Gerais, Brazil from September 1998–July 1999, and compared them with similar data collected 15 years ago when the 23–27 individuals in the group traveled together as a cohesive unit. Home range size increased from 168 ha to 309 ha, reflecting an expansion into areas of the forest that were previously unutilized and consistent with the positive relationship predicted between group size and home range size. By contrast, muriquis exhibited remarkable seasonal and interannual stability in their day ranges. Day ranges, which were calculated from 144 days with 8 h of observation, averaged 1,313 ± 573 m (median = 1,206 m). Day ranges did not vary with the size of subgroups, defined as independent individuals that traveled with one another out of contact with other group members. Subgroups were significantly larger during the rainy season (mean = 41.8 ± 12.7, median = 46.0 individuals, n = 72) than the dry season (mean = 36.6 ± 13.25, median = 39.5 individuals, n = 72). Subgroups were also larger than the size of the entire group during the previous study, yet their day ranges are indistinguishable. The stability in muriqui day ranges is consistent with predictions for folivorous primates in which other indicators of intragroup feeding competition, such as female dominance relationships, are also absent. We attribute the transition from cohesive to fluid grouping patterns to limits on the number of individuals that can coordinate their movements when they spread out while foraging and suggest that seasonal differences in subgroup sizes without corresponding adjustments in day ranges reflect seasonal differences in the distribution of preferred foods coupled with the effects of reproductive seasonality on muriqui grouping patterns.     

Liver iron overloading in captive muriquis (Brachyteles spp.)

Background Iron accumulation was investigated qualitatively and quantitatively in the liver of 15 captive Brachyteles spp. Methods Hepatic hemosiderosis index (HHI) was determined as the area percentage of the liver parenchyma occupied by hemosiderin and ferritin deposits, through computerized histomorphometric analysis of Prussian blue–stained histologic sections. Results All studied animals presented liver hemosiderosis, and HHI ranged from 0.2% to 41.7%. There were no significant differences in HHI between muriqui species or genders, and no correlations were detected among HHI and age, time in captivity or body mass. Iron deposits were accompanied by other hepatic disorders. Conclusions This is the first study addressing the occurrence and consequences of iron overloading in the liver of muriquis. We propose that hemosiderosis may act as a contribute factor for the development of hepatic injuries. Further studies are advised to clarify the role of diet in the pathogenesis of hemosiderosis in these atelids.     

Thanatology in the northern muriqui (Brachyteles hypoxanthus)

Primates - Primate thanatology, or the study of primate responses to dying and death, has become increasingly relevant in recent years. However, the number of reports remains small and the quality...     

Sex differences in vocal patterns in the northern muriqui (Brachyteles hypoxanthus)

We investigated whether sex differences in spatial dynamics correlate with rates of staccato and neigh vocalizations in northern muriquis (Brachyteles hypoxanthus) at the Reserva Particular do Patrimônio Natural–Feliciano Miguel Abdala, Minas Gerais, Brazil. A total of 2,727 10 min focal subject samples were collected on 32 adult females and 31 adult males between April 2007 and March 2008. Compared with males, females spent a significantly lower proportion of their time in proximity to other group members and gave staccatos at significantly higher rates while feeding, resting, and traveling. Conversely, males emitted neigh vocalizations at significantly higher rates than females when feeding and resting only. Both sexes gave significantly more staccatos when feeding than when they were engaged in other activities, but their respective rates of neighs did not vary across activities. Both females and males emitted staccato vocalizations at significantly higher rates during times of the year when preferred foods were scarce, but no seasonal differences in the rates of neigh vocalizations were observed in either sex. Females and males showed a reduction in the number of neighbors following staccato vocalizations and an increase in the number of neighbors following neigh vocalizations. Our findings of sex differences in the rates of staccato and neigh vocalizations and the effects of these vocalizations on interindividual spacing are consistent with sex differences in spatial dynamics, and confirm the role of vocal communication in mediating spatial associations in this species. Am. J. Primatol. 72:122–128, 2010. © 2009 Wiley‐Liss, Inc.     

Feeding and Resting Postures of Wild Northern Muriquis (Brachyteles hypoxanthus)

Increased body size in Brachyteles has been regarded as an important evolutionary adaptation that allowed a greater reliance on leaves compared to other more frugivorous Atelidae, but its association with muriqui positional behavior and substrate use is still unknown. Here, we present original data on the feeding and resting postures of the northern muriqui (Brachyteles hypoxanthus) and evaluate predictions about the relationships between body size, postural behavior, and substrate use derived from previously published data for other atelids (e.g. Alouatta, Ateles, and Lagothrix). The study was undertaken from August 2002 to July 2003 on a large group of well‐habituated muriquis inhabiting the Reserva Particular do Patrimônio Natural – Felíciano Miguel Abdala in Minas Gerais, Brazil. Consistent with our predictions, we found that B. hypoxanthus was highly suspensory during postural feeding (60.9%) and commonly used tail–hind limb suspension/horizontal tripod (38.0%) or tail–forelimb/hind limb suspension (21.4%). However, although tail‐suspensory postures permitted the muriquis to use the terminal canopy and small‐sized substrates, these areas were also accessed via tail‐assisted above‐branch postural behaviors involving multiple substrates. Unexpectedly, tail‐suspensory postures were found to be frequently associated with large substrates, tree trunks, and the understory. We suggest that Brachyteles’ ability to access food resources from all areas of a feeding tree and from tree crowns at different canopy levels may account for their ability to efficiently exploit food resources in seasonal disturbed forest fragments of the Brazilian Atlantic Forest today. Am. J. Primatol. 75:74‐87, 2013. © 2012 Wiley Periodicals, Inc.     

Age at first reproduction in philopatric female muriquis (<Emphasis Type="Italic">Brachyteles arachnoides hypoxanthus</Emphasis>)

Female northern muriquis (Brachyteles arachnoides hypoxanthus or B. hypoxanthus) at the Estação Biológica de Caratinga/RPPN-FMA, Minas Gerais, Brazil typically disperse from their natal groups at an average age of 6.1±0.6 years (median =6.0 years, range =5.3–7.8 years, n =22), prior to the onset of puberty and sexual activity. Immigrants do not conceive until at least their second mating season, and the minimum interval from immigration to first reproduction has been 2.0 years. Age at first reproduction in dispersing females, previously estimated at 8.9 years, has now been documented at 9.0 and 9.25 years for two females whose birth dates are known. This is older than the 7.5 years at which the only female previously known to have reproduced in her natal group gave birth. Here, we present new data from a second female that reproduced in her natal group. This female (BA) was first observed to copulate at 5.5 years, and gave birth to her first infant at 7.25 years of age. Her 1.75-year cycling-to-first conception delay was only slightly shorter than the minimum recorded for immigrant females, and thus was not responsible for her young age at first reproduction compared to dispersing females. Although our sample size is small, our findings suggest that early puberty may permit females to reproduce in their natal group, implying a possible link between life history trade-offs and dispersal patterns. Because the only two females that have reproduced in their natal group were maternal sisters, it is also possible that maternal effects on age at puberty can impact dispersal patterns, particularly in small populations of primates.     

Genetic diversity and population history of a critically endangered primate, the northern muriqui (Brachyteles hypoxanthus)

Social, ecological, and historical processes affect the genetic structure of primate populations, and therefore have key implications for the conservation of endangered species. The northern muriqui (Brachyteles hypoxanthus) is a critically endangered New World monkey and a flagship species for the conservation of the Atlantic Forest hotspot. Yet, like other neotropical primates, little is known about its population history and the genetic structure of remnant populations. We analyzed the mitochondrial DNA control region of 152 northern muriquis, or 17.6% of the 864 northern muriquis from 8 of the 12 known extant populations and found no evidence of phylogeographic partitions or past population shrinkage/expansion. Bayesian and classic analyses show that this finding may be attributed to the joint contribution of female-biased dispersal, demographic stability, and a relatively large historic population size. Past population stability is consistent with a central Atlantic Forest Pleistocene refuge. In addition, the best scenario supported by an Approximate Bayesian Computation analysis, significant fixation indices (Φ_ST = 0.49, Φ_CT = 0.24), and population-specific haplotypes, coupled with the extirpation of intermediate populations, are indicative of a recent geographic structuring of genetic diversity during the Holocene. Genetic diversity is higher in populations living in larger areas (>2,000 hectares), but it is remarkably low in the species overall (θ = 0.018). Three populations occurring in protected reserves and one fragmented population inhabiting private lands harbor 22 out of 23 haplotypes, most of which are population-exclusive, and therefore represent patchy repositories of the species'' genetic diversity. We suggest that these populations be treated as discrete units for conservation management purposes.     

Demography and social structure of one group of muriquis (Brachyteles arachnoides)

We monitored one group of muriquis, or woolly spider monkeys (Brachyteles arachnoides), over a 9-year period at Fazenda Montes Claros, Minas Gerais, Brazil. The group grew from 22 to 42 individuals due to the births of 21 surviving infants. Eight immigrations involving immature females were offset by emigrations and disappearances. The home range of the group expanded as the group size increased. The group traveled as a cohesive unit during the first 6 years of the study, but recently it has begun to show greater tendencies to fission temporarily into smaller subgroups. Six adult males from the other muriqui group at this site have simultaneously increased their associations with the main study group. These observations indicate that the group is in a state of transition which may lead, ultimately, either to its division into two smaller units or to a more fluid social structure.     

Activity budgets of woolly spider monkeys,or muriquis (Brachyteles arachnoides)

One group of woolly spider monkeys, or muriquis (Brachyteles arachnoides), was observed from June 1983 through July 1984 at Fazenda Montes Claros, Minas Gerais, Brazil. The study subjects spent an average of 49% of their daylight time resting, 29% traveling, and 19% feeding. They shifted their diurnal schedule of activities in response to seasonal changes in temperature and rainfall. The activity budgets of adult males and females were similar. However, a comparison of three adult females in different reproductive conditions revealed that the lactating female spent a greater proportion of time feeding than did both the pregnant and nonreproductive females. Intraspecific differences in group size and diet appear to be important to understanding differences in the activity budgets of Brachyteles. Differences between locomotion patterns of woolly spider monkeys and sympatric howler monkeys may explain activity budget differences based on group size and diet.     

Diet in one group of woolly spider monkeys,or muriquis (Brachyteles arachnoides)

Data on feeding behavior in one group of muriquis (Brachyteles arachnoides) were collected during a 14 month study at Fazenda Montes Claros, Minas Gerais, Brazil. Muriquis devoted an average of 51% of their annual feeding time to leaves, 32% to fruits, and 11% to flowers. The high proportion of leaves in their diet is consistent with predictions from the energetics of body size. However, they devoted a greater proportion of their feeding time to patchy fruit and flower resources than was expected from comparisons with smaller, sympatric howler monkeys. Muriqui diet varied with the availability of preferred food types across sample months. Fruit and flower consumption corresponded to the availability and abundance of these food resources in the forest. Leaves contributed substantially to muriqui diet throughout the year but appeared to be eaten primarily to provide necessary protein and/or necessary bulk. Male and female diets differed only in the greater proportion of feeding time females devoted to flowers.