Brachyteles Arachnoides Research Articles

A Survey of mid and large bodied mammals in Núcleo Caraguatatuba, Serra do Mar State Park, Brazil

We applied complementary survey techniques to obtain a baseline species list of mid and large bodied mammals in Núcleo Caraguatatuba, Serra do Mar State park, Brazil. Between May and September 2011 we surveyed the community of mid and large bodied mammals using diurnal line transect census (212.4 km), camera-traps (223.2 camera-trap days) and track-stations (478 track-station days). A total of 18 species were recorded from 14 families in eight orders. We recorded the presence of seven species considered threatened in the State of São Paulo, including Primates (Brachyteles arachnoides), Artiodactyla (Mazama cf. americana and Tayassu pecari), Carnivora (Leopardus pardalis, Leopardus tigrinus and Puma concolor) and Perissodactyla (Tapirus terrestris). Based on extrapolated (First order jackknife) species richness estimates we predict that there are between 19 and 32 species of mid and large bodied mammals in the Núcleo. Our revised Mammal Priority Index ranked Núcleo Caraguatatuba as being of medium overall importance for the conservation of mid and large bodied mammals in the Atlantic Forest. Combined with the number and diversity of species recorded, our results demonstrate that this Núcleo is an important area for mammal conservation.

Introduced Primate Species of an Atlantic Forest Region in Brazil: Present and Future Implications for the Native Fauna

The Atlantic Forest of the state of Rio de Janeiro was the habitat of six native primate species: Callithrix aurita, Leontopithecus rosalia, Alouatta guariba clamitans, Brachyteles arachnoides, Callicebus nigrifrons and Cebus nigritus; a seventh species, Brachteles hypoxanthus, possibly occurs in the state. In the literature, the number of non-native primate species for the state was less (three) than the native species (six or seven). Our study reviews the list of primate species, both native and non-native, within the state of Rio de Janeiro and discusses the possible impacts of the introduced primates on the native fauna. Using data from the literature, personal communication with experts, data from Brazilian Federal datasets (Linha Verde and CETAS), and specimens deposited in scientific collections of museums, we recorded 17 primate species with at least one record within the state of Rio de Janeiro. At least eight taxa can be considered non-native to the state. Conservation implications for native fauna may include food resource depletion and competition, hybridization, and disease transmission. Some of these effects were already recorded on the native fauna. We believe the removal of non-native primate species from the state is necessary in order to preserve native fauna regardless of political and ethical issues.

Fission–Fusion Dynamics in Southern Muriquis (Brachyteles arachnoides) in Continuous Brazilian Atlantic Forest

Fission–fusion social dynamics, the spatiotemporal variance in subunit size, composition, and cohesion, are the subject of considerable interest owing to their complex nature and widespread appearance in the primate order. We here aim to describe the nature of fission–fusion dynamics in a population of egalitarian southern muriquis inhabiting a relatively undisturbed extension of mildly seasonal Brazilian Atlantic forest to provide insights into the functions of fission–fusion dynamics and to examine the constraints on and opportunities for associations among individuals. We collected instantaneous scan samples and ad libitum data over a total of 13 mo in 2 yr (1599 observation hours) on subunit size at 2 spatiotemporal scales (party and nomadic party), party composition, spatial cohesion, and the behavioral context of fission–fusion events. These southern muriquis exhibited high levels of fission–fusion with significant variation in party size, cohesion, and composition. The group was weakly cohesive with a small mean party size (3.74 adults, 5.32 all individuals) and nomadic party size (13.73 adults, 19.38 all individuals). Mixed parties were the most frequently observed party type, although the high frequency of all-male parties suggests strong relationships based on philopatry and a mating strategy under scramble competition. We compare fission–fusion dynamics across populations of Brachyteles and highlight the striking continuum of these dynamics in the genus. We make interspecific comparisons with Ateles and Pan, with well documented high levels of fission–fusion, and demonstrate interspecific variation and convergence in grouping patterns.

Primatology in southern Brazil: a transdisciplinary approach to the conservation of the brown-howler-monkey Alouatta guariba clamitans (Primates, Atelidae)

Human interventions in natural environments are the main cause of biodiversity loss worldwide. The situation is not different in southern Brazil, home of five primate species. Although some earlier studies exist, studies on the primates of this region began to be consistently carried out in the 1980s and have continued since then. In addition to important initiatives to study and protect the highly endangered Leontopithecus caissara Lorrini & Persson, 1990 and Brachyteles arachnoides E. Geoffroy, 1806, other species, including locally threatened ones, have been the focus of research, management, and protection initiatives. Since 1993, the urban monkeys program (PMU, Programa Macacos Urbanos) has surveyed the distribution and assessed threats to populations of Alouatta guariba clamitans (Cabrera, 1940) in Porto Alegre and vicinity. PMU has developed conservation strategies on four fronts: (1) scientific research on biology and ecology, providing basic knowledge to support all other activities of the group; (2) conservation education, which emphasizes educational presentations and long-term projects in schools near howler populations, based on the flagship species approach; (3) management, analyzing conflicts involving howlers and human communities, focusing on mitigating these problems and on appropriate relocation of injured or at-risk individuals; and finally, (4) Public Policies aimed at reducing and/or preventing the impact of urban expansion, contributing to create protected areas and to strengthen environmental laws. These different approaches have contributed to protect howler monkey populations over the short term, indicating that working collectively and acting on diversified and interrelated fronts are essential to achieve conservation goals. The synergistic results of these approaches and their relationship to the prospects for primatology in southern Brazil are presented in this review.

Activity Patterns of Brachyteles arachnoides in the Largest Remaining Fragment of Brazilian Atlantic Forest

Time is an important currency for primate energetics, reproduction, and survival. Here, we describe the activity budgets of a group of southern muriquis (Brachyteles arachnoides) inhabiting the largest continuous fragment of Brazilian Atlantic Forest (210,000 ha) in Parque Estadual Carlos Botelho (24°44´–15´S, 47´46–10 W), in the southern region of Sao Paulo State. We collected instantaneous scan sampling data to assess monthly, seasonal, and between-year differences in time allocation for the different activities for 2 complete, nonconsecutive years—1995 and 2002—and compare these with measures of food availability. Over the 2 yr, the group rested on average for 48%, fed for 28%, traveled for 22.5%, and socialized for 1.5% of daylight hours. On a monthly basis, resting correlated negatively with traveling in 1995, and strongly negatively correlated with feeding for both years. Feeding correlated negatively with traveling in 2002, with significantly more time spent traveling during periods of higher young leaf availability. Season was a major influence on activity: the group rested more during the hotter, rainy austral summer season, whereas feeding occurred more frequently in the cooler, drier winter season. We found no consistent associations between food availability and the time that southern muriquis spent in most activities. We suggest that these southern muriquis, like many other large-bodied and atelin primates, minimize energy expenditure while maximizing energy intake, which may be associated with their ability to be folivorous when their preferred fruit foods are less available. They thus adopt a flexible energetic strategy for coping with variable climatic conditions rather than being constrained by food availability.

Intra‐community coalitionary lethal attack of an adult male southern muriqui (Brachyteles arachnoides)

We report on the first evidence of intra-community coalitionary lethal aggression in muriquis (Brachyteles). The event occurred in southern muriquis (Brachyteles arachnoides) during a long-term study (>15 years) of two social groups inhabiting mostly pristine Atlantic forest habitat in the Parque Estadual Carlos Botelho, southern São Paulo State, Brazil. The attack took place deep in the core area of the Group Caetê home range. Tense agonistic behaviors and vocalizations preceded the lethal coalitionary attack, and the tension increased over a 36-48 hr period. One adult female and two unidentified individuals also took part in a coalition led by six adult males. The members of the coalition collectively approached, embraced, immobilized and repeatedly bit the entire body of an adult male, resulting in severe bleeding injuries and the victim's death in less than 1 hr after the attack commenced. Combined ecological, behavioral and spatial data related to the event indicate that this was an intra-community attack and suggest social tensions related to mating competition as the proximate trigger of the coalitionary killing. The attack resembled those reported for chimpanzees, with clear numeric superiority and a low risk of injury to aggressors, resulting in the death of a lone conspecific victim. This observation (n=1) is suggestive of a capacity for escalated aggression in muriquis and reinforces arguments for the potential adaptive significance of intra-community aggression in male philopatric societies, as reported for spider monkeys and chimpanzees. These characteristics challenge the view of the muriquis as a peaceful primate and support the general hypothesis that imbalances of power contribute to intra-specific killing in primates, such as chimpanzees and humans.

Distribution, population size and conservation of the endemic muriquis (Brachyteles spp.) of the Brazilian Atlantic Forest

Muriquis are endemic primates of the Brazilian Atlantic Forest, with two recognized species: Brachyteles hypoxanthus and Brachyteles arachnoides. Although the state of Rio de Janeiro is the type locality for B. arachnoides the muriqui population of this region was, until recently, poorly known. We report our surveys for muriquis in seven localities in the state. Our objectives were to estimate the number of muriquis remaining and to identify local threats. We recorded muriquis in Parque Nacional da Serra dos Orgaos, Parque Nacional do Itatiaia and Guapiacu Private Reserve. Based on our sightings and information from local people we estimate that the remaining muriquis in Rio de Janeiro total c. 160, with 110 B. arachnoides and 50 B. hypoxanthus. The most severe threat to muriquis in these areas is hunting, followed by small population sizes, habitat fragmentation, forest disturbance and ecotourism. Central Rio de Janeiro state still harbours large tracts of intact forests potentially available to muriquis. Thus, if conservation actions could be targeted to mitigate the main threat of hunting there is potential for the recovery of muriquis in the state of Rio de Janeiro, at least in the short-term.

Synteny of human chromosomes 14 and 15 in the platyrrhines (Primates, Platyrrhini).

In order to study the intra- and interspecific variability of the 14/15 association in Platyrrhini, we analyzed 15 species from 13 genera, including species that had not been described yet. The DNA libraries of human chromosomes 14 and 15 were hybridized to metaphases of Alouatta guariba clamitans, A. caraya, A. sara, Ateles paniscus chamek, Lagothrix lagothricha, Brachyteles arachnoides, Saguinus midas midas, Leontopithecus chrysomelas, Callimico goeldii, Callithrix sp., Cebus apella, Aotus nigriceps, Cacajao melanocephalus,Chiropotes satanas and Callicebus caligatus. The 14/15 hybridization pattern was present in 13 species, but not in Alouatta sara that showed a 14/15/14 pattern and Aotus nigriceps that showed a 15/14/15/14 pattern. In the majority of the species, the HSA 14 homologue retained synteny for the entire chromosome, whereas the HSA 15 homologue displayed fragmented segments. Within primates, the New World monkeys represent the taxon with the highest variability in chromosome number (2n = 16 to 62). The presence of the HSA 14/15 association in all species and subspecies studied herein confirms that this association is the ancestral condition for platyrrhines and that this association has been retained in most platyrrhines, despite the occurrence of extensive inter- and intrachromosomal rearrangements in this infraorder of Primates.

Lianas as a food resource for brown howlers (Alouatta guariba) and southern muriquis (Brachyteles arachnoides) in a forest fragment

Lianas, woody vines, are abundant and diverse in tropical forests, but their relative contribution as a source of food for herbivores has been neglected. I compared feeding rates on lianas and trees of two sympatric primates, A. guariba and B. arachnoides, in Southeastern Brazil. Availability of liana foods was gathered in parallel with primate behavioral data collection. Liana represented 33.9% and 27.3% of food sources for A. guariba and B. arachnoides, respectively. Foods coming from trees, rather than from lianas, were significantly more consumed by B. arachnoides. However, both species took advantage of the continuously renewable and ephemeral food resources provided by liana. Availability of liana flowers correlated positively with A. guariba feeding proportions. The nutritional supply provided by lianas is apparently beneficial, or at least unharmful, but experiments comparing primate choices in forests with different liana abundances will help to shed light on their possible negative effect on communities

Mamíferos do Parque Estadual do Desengano, Rio de Janeiro, Brasil

Mesmo após a devastação de grande parte das suas matas, o Estado do Rio de Janeiro ainda abriga uma grande riqueza de mamíferos terrestres. Contudo, informações sobre abundância e distribuição da mastofauna do Estado ainda são escassas. Este estudo tem como objetivo inventariar os mamíferos do Parque Estadual do Desengano, localizado na região norte do Estado do Rio de Janeiro, uma das regiões menos amostradas e mais alteradas do Estado. O inventário foi realizado utilizando armadilhas do tipo Sherman e Tomahawk, e armadilhas de queda para os pequenos mamíferos não-voadores, redes de neblina para os morcegos, armadilhas fotográficas, avistamentos e relatos de moradores e funcionários do Parque para os mamíferos de maior porte. Nós registramos 56 espécies de mamíferos, das quais 15 constam na lista da fauna ameaçada de extinção do Estado do Rio de Janeiro e 10 na lista da fauna brasileira ameaçada de extinção, incluindo Brachyteles arachnoides. As espécies mais abundantes foram o morcego Sturnira lilium e o roedor Akodon serrensis. Além disso, Thaptomys nigrita, roedor normalmente pouco capturado no Estado, foi relativamente abundante no Parque Estadual do Desengano. Nossos resultados indicam que o Parque abriga 33,7% das espécies de mamíferos com ocorrência conhecida para o Estado, destacando a importância da área para a conservação da fauna do Rio de Janeiro.

Fruit diet of Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil: comparison of fruit type, color, and seed size

Fruit is an important food resource for neotropical primates. In this study I compare the fruit diet of sympatric brown howlers (Alouatta guariba) and southern muriquis (Brachyteles arachnoides). Feeding behavior was studied over 12 months and fruit species consumed were identified and assigned to the categories fruit type, fruit color, and seed size. Observed-fruit feeding records were compared with expected records determined from local availability of the fruit of the tree species. I also determined dietary overlap. Fruit consumption occupied 8 and 12% of the feeding time of A. guariba and B. arachnoides, respectively. Fruit from eight tree species were consumed by the former and fruit from twenty-two species by the latter. Patterns of fruit selection of A. guariba and B. arachnoides varied widely. Although howlers and muriquis converge behaviorally by selecting fruit with common attributes (fleshy/unprotected, violet and brown/black-colored), unlike A. guariba, B. arachnoides fed on immature seeds of fleshy/protected and dry fruit. Large seeds were ingested, and defecated intact, by B. arachnoides only. There was little overlap of fruit diet even within categories that had been selected by both, suggesting that dietary divergence is occurring at the interspecific level. Different resource exploitation probably mediates the coexistence of A. guariba and B. arachnoides in low diversity, semideciduous forests, where the environment imposes narrow limits on primate food choices.

The southern muriqui, <i>Brachyteles arachnoides</i>, in the state of Paraná: current distribution, ecology, and the basis for a conservation strategy


 
 
 
 Primatologists have suspected the existence of remnant populations of the southern muriqui, Brachyteles arachnoides (É. Geoffroy, 1806), in the state of Paraná since the early 1970s. Only in 2002, however, was this confirmed, with the discovery of a group in the upper Rio Ribeira valley. Here we report on some observations of this group, which totals 23 individuals living in a tiny remnant of the primary dense broadleaf forest that formerly extended in a continuous belt into Paraná’s first planalto along the valleys of the rios Ribeira and Açungui. We also discuss possibilities for the occurrence of muriquis elsewhere, and our ongoing efforts for the conservation of this threatened species in the state of Paraná.
 
 
 

Management of muriquis (<i>Brachyteles</i>, Primates) in captivity


 
 
 
 Muriquis are the largest of the Neotropical primates. Two forms are recognized today — Brachyteles arachnoides (É. Geoffroy, 1806), the southern muriqui with a black face, and Brachyteles hypoxanthus (Kuhl, 1820), the northern muriqui with face and genitalia mottled pink and black. They occur in eastern Brazil from the south of the state of Bahia to northern Paraná. The destruction, degradation and fragmentation of the Atlantic forest, along with hunting, are the reasons for their severely threatened status today. In this article, I briefly describe the history of conservation efforts and research on muriquis. Captive breeding, although still incipient as an effective conservation measure, has been successful at the Rio de Janeiro Primate Center (CPRJ/FEEMA) and the Curitiba Zoological Park, Paraná. I discuss particularly aspects of breeding success, cage design, colony formation, feeding and nutrition, diseases and the prevention and treatment of illnesses.
 
 
 

Muriqui populations reported in the literature over the last 40 years


 
 
 
 Aguirre (O mono Brachyteles arachnoides (E. Geoffroy). Situação Atual da Espécie no Brasil. Acad. Brasil. Ciênc., Rio de Janeiro, 1971) identified 61 localities for the occurrence of the muriqui (Brachyteles arachnoides) in the states of Bahia, Espírito Santo, Minas Gerais, Rio de Janeiro, São Paulo and Paraná. He estimated a total population of 2,791–3,226 muriquis, contrasting with a population of about 400,000 he reckoned would have existed in 1500. Accepting the position that there are two species, Aguirre’s (1971) data suggested a maximum of 996 individuals for the northern muriqui (Brachyteles hypoxanthus) and about 2,230 for the southern muriqui (B. arachnoides). Current population estimates for the northern muriqui have indicated at least 864 individuals in the wild. Data available for the southern muriqui, suggest a minimum population of about 1,300. These numbers combined approximate to the total population of 2,230 estimated by Aguirre (1971). Further population surveys for muriquis in the states São Paulo, Rio de Janeiro and Bahia are urgently needed, along with comparative studies on their basic ecology, diet and behavior in the different-sized forest fragments and the more extensive forests. Although stochastic effects could rapidly eliminate the very small isolated populations of the northern muriqui, in larger forests, persistent threats, such as hunting, could gradually but invidiously reduce those of the southern muriqui.
 
 
 

Survey and status of the muriquis (<i>Brachyteles arachnoides</i>) in the Serra dos Órgãos National Park, Rio de Janeiro


 
 
 
 The Serra dos Órgãos National Park protects 11,800 ha of Atlantic forest in the state of Rio de Janeiro (22°30'S, 43°06'W; 300 to 2,263 m above sea level). Vegetation types include montane dense evergreeen forest up to altitudes of 1,800 m; cloud forest from 1,800 to 2,000 m; and high altitude grassland above 2,000 m. This paper reports on surveys carried out in 10 localities in the park specifically to obtain a minimum estimate of the population of northern muriquis (Brachyteles arachnoides). Muriquis were sighted 26 times at altitudes ranging from 800 to 1,500 m. It is possible that they belonged to four groups in which case the minimum number of individuals recorded would be 56. If in fact the sightings were of just two groups, the minimum number of individuals would be 32. Black-horned capuchin (Cebus nigritus) and brown howler monkeys (Alouatta guariba) were also recorded for the park. The buffy-tufted-ear marmoset (Callithrix aurita) was not seen.
 
 
 

The southern muriqui, <i>Brachyteles arachnoides</i>: ecology of a population in a semideciduous forest fragment


 
 
 
 Southern muriquis (Brachyteles arachnoides) inhabit evergreen and semideciduous forest fragments in southeastern Brazil. Contrary to the broadleaf evergreen forests, the seasonal mesophytic forests experience a relatively severe dry season, which affects the muriquis’ diet. Through behavioral sampling of feeding activity, I determined the diet of a group of muriquis in a semideciduous forest fragment. Leaves represented 55.3% of feeding records, flowers 16.1%, fruits 12.1%, and seeds 16.5%. Muriquis included 47 plant species in their diet. Leaf consumption was significantly higher in the dry season, but there was no evident difference between seasons in their feeding on either flowers, fruits, or seeds. Muriquis in this study shared only 11 taxa with groups in evergreen forests. The study group made consistent use of immature seeds. Dietary flex- ibility and the consumption of alternative resources may likely be advantageous where there are repeated lean periods and anthropogenic interference.
 
 
 

Conservation research on the southern muriqui (<i>Brachyteles arachnoides</i>) in São Paulo state, Brazil


 
 
 
 In this paper we present an overview of the past and current conservation research on southern muriquis, Brachyteles arachnoides, in the state of São Paulo, most particularly in the forests of the Serra de Paranapiacaba, in four connected protected areas, which comprise the so-called Paranapiacaba Ecological Continuum: the state parks of Carlos Botelho, Intervales, and Alto Ribeira and the Xitué Ecological Station. These areas are the major stronghold for this species, and we discuss particularly the history of research on the muriquis of the Carlos Botelho State Park and the importance of statewide surveys and the establishment of further long term research sites to understand better its status and for the elaboration of management plans for its conservation.
 
 
 

Directives for the conservation of the northern muriqui, <i>Brachyteles hypoxanthus</i> (Primates, Atelidae)


 
 
 
 There are two species of muriqui, Brachyteles — the northern muriqui (B. hypoxanthus) and the southern muriqui (B. arachnoides). The northern muriqui is the most endangered of the two. The species originally occurred through most of the Atlantic forest in the south of the state of Bahia, eastern Minas Gerais, and south central Espírito Santo. Hunting and widespread loss of its native forest means that today just a few small and isolated populations remain, with poor chances of survival in the long term. Currently the northern muriqui can be found in 12 places, six on private land, three in state protected, and three in federal protected areas. Combined, these areas total about 160,000 ha and a minimum known number of 855 individuals. The known population has increased significantly in the last five years, but the total is still very small and fragmented for long-term viability — no single population exceeds 500. In this article we report on the areas where they are known to occur, the main threats to them, and the conservation measures that have been proposed to avoid the premature extinction of the species.
 
 
 

Conservation genetics of the muriqui: past, present and future


 
 
 
 Our understanding of the genetics of the muriqui have increased in recent decades. In the mid 1980’s the first data was obtained from polymorphisms of allozymes of 10 individuals of B. hypoxanthus (northern muriqui) from Minas Gerais, and two individuals of B. arachnoides (southern muriqui) from São Paulo. All specimens were considered to be of a single species. The DNA was extracted from blood samples, which required capture and anesthesia of animals. We can now extract mitochondrial DNA from feces samples. Analyzing more than 120 individuals of the northern muriqui from two populations, we are now able make inferences about genetic variability, population distinctiveness as well as intra- and interpopulation gene flow. DNA sampling through feces is reliable, efficient, and economic, and does not risk the physical integrity of the animals, and furnishes enough DNA that is easily reproducible for PCR amplification. Using this method it is possible to sample a greater number of individuals in nature than would be possible if live capture were necessary. A muriqui feces and DNA bank has been set up, and currently has samples of 230 individuals from seven of the twelve known populations of northern muriqui. The samples resulted from field studies, but more coordinated and systematic efforts among fieldworkers at the different muriqui sites are needed to improve representation across populations and species. Future perspectives include the use of new genetic markers (nuclear and mitochondrial DNA) to identify parents, offspring, and closely related individuals in captive and wild populations; to define units for conservation and the gene flow between them; to quantify genetic variability in the populations; to assess the rate at which genetic variation has been lost over time; to estimate the degree of inbreeding in the population; and to understand better the genetic differentiation of the two species.
 
 
 

Comparative Seed Dispersal Effectiveness of Sympatric Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil1

ABSTRACTI compared the effectiveness of sympatric brown howlers (Alouatta guariba) and muriquis (Brachyteles arachnoides) as seed dispersers in terms of quantitative and qualitative attributes. I hypothesized that differences in feeding and behavioral patterns between these large‐bodied folivorous/frugivorous primates would lead to dissimilarities in their effectiveness as endozoochoric seed dispersal agents. The study was carried out in a semideciduous forest fragment of Fazenda Barreiro Rico, southeastern Brazil. Through behavioral sampling of frugivory and defecation events as well as analyses of fecal samples, I determined that A. guariba dispersed fewer species and produced a lower proportion of dung with intact seeds than B. arachnoides. There was no difference between the number of seeds in fecal samples of A. guariba and B. arachnoides. These primates affected to a similar degree both germination percentage and latency to germination of seeds they ingested or removed the pulp from. Howlers and muriquis were also similar in carrying seeds away from the parent trees. Contrary to muriquis, howlers defecated seeds under the canopy of conspecific lianas, where seeds are expected to suffer high mortality rates, and voided seeds predominantly in a clumped pattern. B. arachnoides was a more effective seed disperser when compared to A. guariba in some attributes evaluated, but not in others. Given the interspecific variation in recruitment patterns of tropical plants and the loss of frugivorous bird species at the study site, the differences between howlers and muriquis in their abilities as seed dispersers may crucially influence the composition and maintenance of seedling diversity.