Brachyteles Arachnoides Research Articles

Diet of Southern Muriquis in Continuous Brazilian Atlantic Forest

We systematically collected data on feeding behavior for one group of 33–39 southern muriquis (Brachyteles arachnoides) in Parque Estadual Carlos Botelho (PECB), Sao Paulo State, Brazil (37,432.45 ha of continuous Atlantic Forest), between January and December 1995. We determined food item consumption from instantaneous scans of behavior. Fruits were the most eaten food items in all 12 mo (40–80% of scan in every mo, average = 71.3%). Muriquis ate young leaves more than mature leaves or flowers. Our results are consistent with previous findings at the same and neighboring forest sites that southern muriquis have a consistently frugivorous diet when inhabiting less disturbed habitats, but contrast with previous observations on oppportunistic frugivory in muriqui populations inhabiting fragmented forests. Sustained high levels of frugivory probably result from year-round availability of fruit within large continuous forests.

Density of Primates in Four Semi-deciduous Forest Fragments of São Paulo, Brazil

Populational parameters of primates in the remaining southeastern Brazilian Atlantic Forest have been estimated, but investigations are biased to coastal evergreen sites. In this study density of three primate species was assessed through line-transect surveys in four semi-deciduous forest fragments (240 to 1450 ha) in Fazenda Barreiro Rico, eastern range of central Plateau of Sao Paulo state, Brazil. A total of 274 km was surveyed from January to October 2000. I estimated densities via DISTANCE software. Two of the largest fragments contained five primate species while two of the smallest ones harboured, respectively, four and two species. Densities of Cebus apella (15.34–47.92 ind./km2), Alouatta guariba (8.32–34.61), and Brachyteles arachnoides (19.92–35.11) were considerable. Differently from C. apella and A. guariba, B. arachnoides presented a density higher than previously estimated for the largest patch. The hypothetical minimum total population of B. arachnoides (601) may be the largest in semi-deciduous sites. This reinforces the value of the area in terms of its relative contribution for conservation of this endangered species. The narrow spatial scale distribution of forest fragments at Barreiro Rico and its proximity to academic institutions make the site suitable for programs of forest connectivity, studies on conservation biology, and wildlife management endeavours.

Phylogenetic inferences of Atelinae (Platyrrhini) based on multi-directional chromosome painting in Brachyteles arachnoides, Ateles paniscus paniscus and Ateles b. marginatus

We performed multi-directional chromosome painting in a comparative cytogenetic study of the three Atelinae species Brachyteles arachnoides, Ateles paniscus paniscus and Ateles belzebuth marginatus, in order to reconstruct phylogenetic relationships within this Platyrrhini subfamily. Comparative chromosome maps between these species were established by multi-color fluorescence in situ hybridization (FISH) employing human, Saguinus oedipus and Lagothrix lagothricha chromosome-specific probes. The three species included in this study and four previously analyzed species from all four Atelinae genera were subjected to a phylogenetic analysis on the basis of a data matrix comprised of 82 discrete chromosome characters. The results confirmed that Atelinae represent a monophyletic clade with a putative ancestral karyotype of 2n = 62 chromosomes. Phylogenetic analysis revealed an evolutionary branching sequence {Alouatta {Brachyteles {Lagothrix and Ateles}}} in Atelinae and {Ateles belzebuth marginatus {Ateles paniscus paniscus {Ateles belzebuth hybridus and Ateles geoffroyi}}} in genus Ateles. The chromosomal data support a re-evaluation of the taxonomic status of Ateles b. hybridus.

Vocal sequential exchanges and intragroup spacing in the Northern Muriqui Brachyteles arachnoides hypoxanthus.

Sequential exchanges of vocalizations (staccatos and neighs) emitted by Northern Muriquis Brachyteles arachnoides hypoxanthus were recorded at the Biological Station of Caratinga, Minas Gerais State, Brazil. Staccatos and neighs containing larger proportion of short elements were preferentially produced during short-range exchanges; neighs, produced by a larger number of participants, were typical of long-range exchanges. Staccatos emitted by animals feeding in a dispersed manner contained a larger proportion of tonal elements than those emitted by muriquis feeding in a cohesive manner. Sequential exchanges seem thus to be constituted by two inter-related subsystems of calls that aid muriquis to coordinate intragroup spacing, despite the poor visibility of the habitat.

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.

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 Estacao Biologica 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.

Genetic differentiation and diversity of natural populations of Cryptocarya spp. (Lauraceae) from the Brazilian Atlantic rain forest

The genetic variability and structure of ten populations of Cryptocarya spp. (Lauraceae) were investigated by means of isozymes. Leaf samples of adult individuals of C. aschersoniana, C. moschata, and Cryptocarya sp., from two regions of São Paulo state, Brazil, were collected. Seeds from 35 families of C. moschata and juveniles of three populations from diaspores dispersed by “muriquis”, Brachyteles arachnoides (Primates - Cebidae), were also collected. From twenty loci analysed, the expected average heterozygosity of progenies, juveniles, and adults of C. moschata was respectively 0.313, 0.227, and 0.351, whereas it was 0.258 and 0.393 for C. aschersoniana and Cryptocarya sp., respectively. Results indicated that a greater variability occurred within populations for all categories analysed. For adult populations of C. moschata, the divergence obtained through GST estimates suggests the existence of significant genetic drift and/or natural selection effects between regions. The level of gene differentiation (GST = 0.107) was relatively high, and comparable to what would be expected for groups of plants having a half-sib family structure in a single generation. For juvenile populations, the genetic differentiation was also high (GST = 0.084). This could be explained by differential feeding behaviour of “muriquis” within their home range, allied to the distance among sites of seed dispersion. Nei’s average genetic distance (D) between pairs of C. moschata adult populations was 0.07, indicating again a pronounced genetic differentiation. Present values obtained from isozymes support morphological and wood anatomy evidences that C. moschata and C. aschersoniana are closely related species.

Social dynamics of male muriquis (Brachyteles arachnoides hypoxanthus)

We investigated patterns of sociality among wild male northern muriquis (Brachyteles arachnoides hypoxanthus) to explore some of the possible ways in which within-group scramble competition might shape their social and mating strategies. The 13 adult males in our study group spent an average of 54.5′4.2% of their time in proximity to at least one other adult male. They were more likely to associate with one another, but not with adult females, when they were resting than when they were feeding. Embrace rates were positively related to the proportion of time males spent in proximity during resting. Males that associated closely with one another tended to interact more often, although individual differences in male social styles and rates of interactions were apparent. Young adult males had significantly higher social maintenance rates than the oldest males in our sample, but no other effects of age were detected in any of our other behavioral comparisons. In roughly 20% of all dyads, one male valued the association significantly more than the other. Males tended to value associates with higher mating success than themselves, and to share access to the same females on the same days with their closest associates. Neither of the two pairs of maternal brothers in our study group were important associates to their kin, but brothers shared copulations in the same polyadic copulation partnerships with one another. Although still preliminary, our findings suggest that muriqui males differentiate among their possible social partners in ways that may minimize the variance in their mating success under the unusual conditions imposed by scramble competition for reproductive opportunities.

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.

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.

Population density of primates in a large fragment of the Brazilian Atlantic rainforest

We performed a line transect survey (352.4 km) of primates in the Serra de Paranapiacaba, at one of the largest relatively undisturbed fragments of the Atlantic rainforest of Southeastern Brazil (ca. 1400 km2), in August 1998. The brown capuchin, Cebus apella nigritus, was the most common species found in the area (20 groups, density estimate: 5.31 ± 2.05 individuals per km2, mean ± SE). Nine groups of the brown howler monkey, Alouatta guariba clamitans, and eight of the woolly spider monkey, Brachyteles arachnoides arachnoides, were also recorded, with preliminary density estimates of 0.79 ± 0.40 and 2.33 ± 1.37 individuals per km2, respectively. Density estimates for these species in other fragments of Atlantic rainforest are reviewed, showing that densities in Paranapiacaba are among the lowest reported. It is suggested that the higher densities reported for isolated populations in small forest patches (<50 km2) is related to the absence of main primate predators, the density compensation phenomenon and the ecological plasticity of some primate species. In contrast, local extinction in many small patches is probably related to hunting pressure. Given the important primate populations found in the Paranapiacaba fragment, conservation strategies for the studied species should give priority to effective protection of the largest remnant fragments from illegal hunting and deforestation, rather than translocation of individuals or captive breeding programs to introduce monkeys in small forest fragments vulnerable to hunting and of uncertain future.

Lack of pubertal influences on female dispersal in muriqui monkeys, Brachyteles arachnoides

The hormonal mediation of dispersal in female mammals is poorly understood, in part because of the difficulties of detecting the onset of ovarian cycling and puberty in dispersing individuals. We used noninvasive methods of faecal steroid assays to determine the timing of dispersal relative to puberty and ovarian cycling in wild female muriqui monkeys, a species in which males are philopatric and nearly all females transfer from their natal groups. Natal females had a mean±SE age of 73.4±7.2 months (N=18) at the time of their transfers. Intergroup transfers occurred when one or more sexually active adult females were present, but did not show any seasonal patterns. Faecal progesterone and oestradiol profiles from nine natal females prior to transfer and four non-natal females that transferred into our study group demonstrate unequivocally that dispersal occurs prior to puberty in this species. All females showed baseline oestradiol levels and low progesterone levels compared with cycling adult females. Immigrants were first observed to copulate at 11.2±2.2 months of age (N=4), prior to the onset of normal ovarian cycles, and gave birth to their first offspring at 33.8±7.3 months (N=4) after transferring. Mean cortisol levels did not differ between natal emigrants or recent immigrants, and were within the range of those of adult males during the nonbreeding season in 10 of the 11 prepubertal females sampled. These results indicate that female dispersal is not triggered by activational hormones associated with puberty or escape from reproductive suppression in this species.

Population Viabilities and Conservation Implications for Muriquis (Brachyteles arachnoides) in Brazil's Atlantic Forest1

Abstract Muriquis (Brachyteles arachnoides) are endemic to the Atlantic Forest of southeastern Brazil, where an estimated 1200 individuals are distributed unevenly among only 19 populations. Despite the fact that over two-thirds of all muriquis live at low densities in large and protected, undisturbed forests, virtually nothing is known about the demography of these populations. Consideration of the mechanisms underlying the low extinction probabilities simulated for muriquis inhabiting the small, disturbed forest at the Estacao Biologica de Caratinga (EBC), Minas Gerais, where long-term demographic and behavioral studies have been conducted, provides disturbing predictions about the viability of other populations living at lower densities. Local resource competition may be responsible for the female-biased infant sex ratio documented at the EBC under the female-biased dispersal regime exhibited by muriquis. At lower population densities, however, release from competition may lead to male-biased infant se...

Seasonal and Social Correlates of Fecal Testosterone and Cortisol Levels in Wild Male Muriquis (Brachyteles arachnoides)

Fecal testosterone and cortisol levels were analyzed from six wild male muriquis (Brachyteles arachnoides) over a 19-month period at the Estação Biológica de Caratinga in Minas Gerais, Brazil, to investigate the hormonal correlates of seasonal sexual behavior and environmental conditions. Group mean testosterone levels based on weekly samples from the six males did not differ between copulatory and noncopulatory periods or between rainy and dry seasons. Cortisol levels did change with copulatory periods, and were significantly higher during the second dry season, when mating continued following an exceptionally heavy rainy season, than during the first dry season, when mating ceased. Males exhibited individual variation in the timing of their hormone shifts relative to their sexual activity, but neither hormone levels nor sexual activity were related to male age. Despite individual differences in the timing of testosterone fluctuations around the onset and offset of the copulatory season, all males exhibited elevated cortisol concentrations following a slight increase in testosterone at the beginning of the copulatory season. Both the lack of significant changes in testosterone levels with the onset of the rainy and copulatory season and the lack of prebreeding increases in cortisol may be related to the low levels of overt aggression displayed by male muriquis over access to mates.

Interactions between aroids and arboreal mammals in the Brazilian Atlantic rainforest

The Brazilian Atlantic rainforest harbours at least 129 non-volant mammal species. There is also a diverse and numerous epiphytic flora associated with this Neotropical rainforest, including several species of Araceae. Nevertheless, knowledge of the ecology of this group of plants and its interaction with animals is poor. In this study we investigated the interactions between epiphytic aroids and arboreal mammals in the Atlantic forest. We carried out the field work between November 1995 and June 1997 in the Parque Estadual Intervales, southeastern Brazil, a still well preserved forest area of approximately 490 km2. We analysed faecal samples from primates (Cebus apella and Brachyteles arachnoides), collected during observations in the field, and marsupials (Didelphis aurita, Micoureus demerarae, Gracilinanus microtarsus), collected from animals captured monthly or bi-monthly in live-traps. We recorded 17 species of Araceae in the study area. The seeds of eight species occurred in the faecal samples: Anthurium harrissi, Monstera adansonii, Philodendron corcovadense, P. appendiculatum, P. exymium, P. crassinervium, P. obliquifolium, and Heteropsis oblongifolia. Aroids were present in faecal samples of the primates during most of the year, with a mean monthly percentage of occurrence of about 56.2%. For marsupials, aroids also were a seasonally important food source, as between November and June the mean monthly percentage of occurrence in faecal samples was about 26.5%. Our data indicate that aroids are an important food source for arboreal and semi-arboreal mammals and that these animals may play an important role as seed dispersers of this group. Aroids and arboreal mammals appear to interact more strongly in Atlantic forest than in other Neotropical forests.

Predicting primate responses to “Stochastic” demographic events

Comparative approaches in contemporary primate behavioral ecology have tended to emphasize the deterministic properties of stochastic ecological variables. Yet, primate responses to ecological fluctuations may be mediated by the interactions among demographic processes at the levels of individuals, groups, and populations. In this paper I examine long-term data collected from June 1982-July 1998 on one expanding group of muriquis (Brachyteles arachnoides) at the Estação Biologica de Caratinga, Minas Gerais, Brazil to explore the demographic and life history correlates of reproductive seasonality and skewed infant sex ratios. Variation in the size of annual birth cohorts (≥2 infants) was positively related to variation in the annual distribution of births (r (s)=0.96,n=10,p<0.01), indicating the importance of considering the effects that the number of reproductive females may have on interpretations of reproductive seasonality. The female-biased infants sex ratio documented from 59 births was attributed exclusively to multiparous mothers. Primiparous mothers produced comparable numbers of sons (n=6) and daughters (n=7), and were increasingly likely to produce daughters with each subsequent reproductive event. Seven of the 11 females that have produced≥3 infants to date exhibited biases in favor of daughters whereas only 1 was biased in favor of sons. Variation in female sensitivity to local resource competition at different stages of their life histories may account for the female-biased infant sex ration in this population.

Behavioral Correlates of Dispersal in Female Muriquis (Brachyteles arachnoides)

We documented four adolescent female transfers—two emigrations, two immigrations—during a 12-month study from August 1994 to July 1995 on one group of muriquis (Brachyteles arachnoides) at Estacao Biologica de Caratinga in Minas Gerais, Brazil. Intergroup transfers occurred throughout the year independent of season. A total of 613 focal samples of 10-min duration conducted on six adolescent females (5–9 years of age) revealed significant differences in the behavior of migrant versus natal resident females. During the seasons encompassing their respective group transfers, both emigrants and immigrants devoted more of their time to resting than resident females belonging to the same age cohorts did. Time spent feeding on mature fruit was higher for one emigrant and lower for both immigrants compared to the two resident females. Emigrant females had fewer neighbors within a 1-m radius than resident females did, whereas immigrant females were within a 1-m radius of adult females and within a 5-m radius of adult males more often than resident adolescent females were. Adolescent females were displaced on 26 occasions. Displacements occurred mainly during the dry seasons (n = 21) and mainly at food sources (n = 21). Using the number of focal samples conducted on each female as an estimate of observation time, immigrant females were displaced at twice the rate of residents. However, like other behavioral differences detected between resident and migrant adolescent females, differences in individual displacement rates were evident only during the season in which each of the immigrants joined the group. Collectively, our findings imply that female intergroup transfer in this population involves relatively mild, short-term costs.

Population Variation in Patch and Party Size in Muriquis (Brachyteles arachnoides)

We examined the relationship between food patch size and feeding party size with comparative data from two populations of muriquis (Brachyteles arachnoides) in the 37,797-ha forest at the Parque Estadual de Carlos Botelho (PECB), Sao Paulo, and the 800-ha forest at the Estacao Biologica de Caratinga (EBC), Minas Gerais. Precipitation was more abundant and less seasonal at PECB than EBC, and the density of large trees (>25.0 cm) was higher at PECB (206 ha−1) than at EBC (132 ha−1). At both sites, the size of feeding parties is positively related to the size of food patches. As predicted, food patches at PECB are significantly larger than those at EBC for both fruit and leaf sources. Contrary to expectations, feeding parties were larger at EBC than PECB. The higher population density of muriquis and sympatric primates at EBC may make large associations more advantageous to these muriquis than to muriquis living at lower population densities in PECB.

Genetic variation in remnant populations of the woolly spider monkey (Brachyteles arachnoides)

The muriqui or woolly spider monkey (Brachyteles arachnoids) is an endangered primate endemic to the Atlantic Forest of Brazil, <5% of which remains. The known muriqui population consists of <700 individuals separated into approximately 15 geographically isolated forest fragments. I present data on the distribution of genetic variation within and between two such remnant populations (FE and FBR) and summarize the implications of these results for long-range management of species genetic diversity. Eleven of 32 allozyme loci were polymorphic, representing an overall level of polymorphism of 34.4% and a mean heterozygosity per locus of 11%. Both values are among the highest reported for New World monkeys. Genetic differentiation between the two localities is highly significant (FST = 0.413, p < 0.001). Genetic distance between them is an order of magnitude greater than that between other populations of platyrrhine subspecies, but this could be an artifact of the small sample size from FBR. High levels of genetic diversity apparently characteristic of this species persist because (1) fragmentation and size reduction of muriqui populations has occurred very rapidly relative to the muriqui life span—although both polymorphism and heterozygosity were lost between generations in the largest population, the high genetic diversity present in the parent population was still in evidence; and (2) genetic diversity before population fragmentation by human activity was not distributed uniformly throughout the species' historic distribution. Thus, remnant muriqui populations are important genetic reservoirs of alleles that are unique or rare in the species gene pool as a whole. These results emphasize the need for the integration of conservation management efforts throughout the species range.

A new locality for &lt;i&gt;Brachyteles arachnoides&lt;/i&gt; and the urgency or finding new directions for muriqui conservation

No abstract