Jean P. Boubli

Feeding Ecology of Black-headed Uacaris (Cacajao melanocephalus melanocephalus) in Pico da Neblina National Park, Brazil

From June 1994 to October 1995, I conducted a study of the feeding ecology of one group of black-headed uacaris (Cacajao melanocephalus melanocephalus) in Pico da Neblina National Park, Brazil, near the Venezuelan border (01°10′N to 00°26′S, 65°03′W to 66°52′W). Of a total of 429 feeding records, 89% corresponded to fruits from which black-headed uacaris ate ripe and unripe seeds, mesocarps and arils. Seeds were the single most important food item year-around, corresponding to 81% of the feeding records for fruits. Black-headed uacaris used 120 different plant species in 32 families as food. The 3 most important plant species in their diet, Micrandra spruceana, Eperua leucantha, and Hevea braziliensis (all trees), accounted for 38% of the feeding records for fruits. These species produced fruits that were protected by very hard green husks, were barochorous, did not have fleshy mesocarps, and were slow to mature, thus being available as unripe fruits for long periods. The second and third most important species in the diet of black uacaris, Eperua leucantha and Hevea braziliensis, were dominant in the forest: approximately 30% of trees ≥10 cm dbh sampled in a 2-ha botanical transect at the study site. I discuss the formation of large social groups of black-headed uacaris in Pico da Neblina National Park in light of the peculiar floristic composition of the study site.

Modeling the Geographical Distribution and Fundamental Niches of Cacajao spp. and Chiropotes israelita in Northwestern Amazonia via a Maximum Entropy Algorithm

We modeled the geographical distribution of 4 pithecine primate species: brown-backed bearded sakis (Chiropotes israelita) and 3 black uakaris (Cacajao melanocephalus, C. hosomi, and C. ayresi) that inhabit remote regions of western Amazonas, Brazil. We applied a maximum entropy algorithm modeling program (MAXENT) to field data Boubli collected from 1991 to 2007. We used 23 environmental coverage variables to model the distribution of the primates. The layers were related to precipitation, temperature, topography, and ecological bioregions or Ecoregions. The predicted distribution for Cacajao hosomi was strongly associated with the Negro-Branco Moist Forest and Guianan Highlands Moist Forests Ecoregions, and the Worldclim variables Bio3 (isothermality), Bio4 (temperature seasonality) and Bio17 (precipitation of the driest quarter). Cacajao melanocephalus was strongly associated with Japurá/ Solimões-Negro Moist Forests, Caquetá Moist Forests, Purús Várzea Flooded Forests, Rio Negro Campinaranas, and Cordillera Oriental Montane Forests, Ecoregions. Cacajao ayresi was strongly associated with Negro-Branco Moist Forest and Rio Negro Campinarana Ecoregions as well as Worldclim Bio3 (isothermality). Chiropotes israelita was also strongly associated with Worldclim Bio3 (isothermality) followed by the Negro Branco Moist Forests and Guianan Piedmont and Lowland Moist Forests Ecoregion, and to the Guianan Highland moist forests. These results show a great overlap between the bearded saki and 2 black uakaris, Cacajao hosomi and C. ayresi. Given that one cannot attribute the separation between the species in the Rio Negro-Rio Branco interfluvium to the existence of geographical barriers such as rivers, we suggest that the present geographical boundaries and thus coexistence of the 3 pithecines north of the Rio Negro is maintained by competitive exclusion or stochastic events. Until more surveys are conducted, the present geographical distributions of the pithecines and the mechanism maintaining their boundaries in the Rio Negro-Rio Branco interfluvium will remain uncertain. One important contribution of our model is to identify areas of higher probability of occurrence that might be helpful in guiding future survey expeditions and choices of areas for future conservation of pithecines.

Cebus Phylogenetic Relationships: A Preliminary Reassessment of the Diversity of the Untufted Capuchin Monkeys

The untufted, or gracile, capuchin monkeys are currently classified in four species, Cebus albifrons, C. capucinus, C. olivaceus, and C. kaapori, with all but C. kaapori having numerous described subspecies. The taxonomy is controversial and their geographic distributions are poorly known. Cebus albifrons is unusual in its disjunct distribution, with a western and central Amazonian range, a separate range in the northern Andes in Colombia, and isolated populations in Trinidad and west of the Andes in Ecuador and northern Peru. Here we examine previous morphological and molecular hypotheses of the taxonomy and phylogeny of Cebus. We construct a time‐calibrated phylogeny based upon mitochondrial DNA sequences from 50 Cebus samples from across their range. Our data indicate that untufted capuchins underwent a radiation at about 2 Ma, and quickly diversified in both the Andes and the Amazon. We provide a provisional reassessment for the taxonomy of untufted capuchins in the Amazon, the Llanos, the Andes, Trinidad, and Central America, splitting currently paraphyletic taxa into several species, including: at least two Amazonian species (C. yuracus and C. unicolor); a species from the Guiana Shield (most likely the same as Humboldts C. albifrons); two northern Andean species, C. versicolor, C. cesarae; C. brunneus (with trinitatis a junior synonym) on the Venezuelan coast, and C. adustus in the region of Lake Maracaibo; C. capucinus in northwestern Ecuador and Colombia, and Panama; C. imitator in Central America; C. olivaceus and C. castaneus occupying a large part of the Guiana Shield; and C. kaapori in the eastern Amazon, south of the Rio Amazonas. More intensive and extensive geographic sampling is needed, including that for some subspecies not represented here. Taxa from the southwestern Amazon (yuracus, cuscinus, and unicolor) and the phylogenetic position of Humboldts Simia albifrons from the Orinoco remain particularly poorly defined. Am. J. Primatol. 74:381–393, 2012.

A Taxonomic Reassessment of Cacajao melanocephalus Humboldt (1811), with the Description of Two New Species

The author of the last published systematic review of Cacajao recognized 2 subspecies of black-headed uakaris (black uakaris): Cacajao melanocephalus melanocephalus and C. m. ouakary. As a result of a series of black uakari surveys and collecting expeditions to several tributaries of the Rio Negro and of morphological and molecular analyses of museum specimens and specimens we collected during field expeditions, we reassess their taxonomy. We describe a newly discovered species of black uakari from the Rio Aracá, a left bank tributary of the Rio Negro, Amazonas, Brazil. We also show that ouakary is a junior synonym of melanocephalus and provide a new name and a new description for Cacajao melanocephalus melanocephalus in the Pico da Neblina region of Brazil and Venezuela. Based on genetic, morphological, and ecological evidence, we propose that there are 3 species of black uakaris. We named the Rio Aracá species Cacajao ayresi sp. nov. (Ayres uakari) in honor of the late José Márcio Ayres, a pioneer in uakari research and conservation. We named the Neblina black uakari Cacajao hosomi, after the Yanomami word for uakaris. The new taxonomic arrangement provided here implies that the conservation status of black uakaris needs to be reassessed.

Spatial and temporal patterns of diversification on the Amazon: A test of the riverine hypothesis for all diurnal primates of Rio Negro and Rio Branco in Brazil.

The role of Amazonian rivers as drivers of speciation through vicariance remains controversial. Here we explore the riverine hypothesis by comparing spatial and temporal concordances in pattern of diversification for all diurnal primates of Rio Negro and its largest tributary, Rio Branco. We built a comprehensive comparative phylogenetic timetree to identify sister lineages of primates based on mitochondrial cytochrome b DNA sequences from 94 samples, including 19 of the 20 species of diurnal primates from our study region and 17 related taxa from elsewhere. Of the ten primate genera found in this region, three had populations on opposite banks of Rio Negro that formed reciprocally monophyletic clades, with roughly similar divergence times (Cebus: 1.85 Ma, HPD 95% 1.19-2.62; Callicebus: 0.83 Ma HPD 95% 0.36-1.32, Cacajao: 1.09 Ma, 95% HPD 0.58-1.77). This also coincided with time of divergence of several allopatric species of Amazonian birds separated by this river as reported by other authors. Our data offer support for the riverine hypothesis and for a Plio-Pleistocene time of origin for Amazonian drainage system. We showed that Rio Branco was an important geographical barrier, limiting the distribution of six primate genera: Cacajao, Callicebus, Cebus to the west and Pithecia, Saguinus, Sapajus to the east. The role of this river as a vicariant agent however, was less clear. For example, Chiropotes sagulata on the left bank of the Rio Branco formed a clade with C. chiropotes from the Amazonas Department of Venezuela, north of Rio Branco headwaters, with C. israelita on the right bank of the Rio Branco as the sister taxon to C. chiropotes+C. sagulata. Although we showed that the formation of the Rio Negro was important in driving diversification in some of our studied taxa, future studies including more extensive sampling of markers across the genome would help determine what processes contributed to the evolutionary history of the remaining primate genera.

A History of Long-term Research and Conservation of Northern Muriquis (Brachyteles hypoxanthus) at the Estação Biológica de Caratinga/RPPN-FMA

Abstract Northern muriquis (Brachyteles hypoxanthus) are endemic to the Brazilian Atlantic forest, and rank among the most critically endangered primates in the world. The 957-ha forest at the Biological Station of Caratinga/Reserva Particular do Patrimônio Natural – Feliciano Miguel Abdalla (EBC/RPPN-FMA), in Minas Gerais, supports a population of more than 230 individuals, one of the highest population densities known. Long-term research and conservation efforts have been underway there since 1982, during which time the behavioral ecology, reproductive biology, and life histories of members of one of the two original groups (Matão) have been systematically monitored. These data, together with a census conducted in 1999, signaled the importance of expanding the project to include the entire population at this site. Since 2002, all four of the muriqui groups that now inhabit this forest have been monitored. While continuing to provide training and research opportunities for Brazilian students, our new research initiatives are focusing on understanding the demography and ecology of this population. Analyses of vegetation structure and composition indicate that the forest at EBC is relatively species-rich compared with other tropical rainforests worldwide. Tree mortality and recruitment are relatively high and overall primary productivity, as measured by litter fall, is average for tropical forests. Given that the forest at EBC has suffered the impact of selective logging, fire, and agriculture, we believe that its high rate of turnover may be a response to past disturbance regimes, and one of the reasons muriquis are doing so well here. It has been proposed that primates that include substantial amounts of leaves in their diet may be favored by habitat disturbance if that means an increase in the availability of more palatable and more nutritious leaves. In addition, in terms of fruits, muriquis are very opportunistic feeders, not appearing to select fruits of any particular, size, shape, or dispersion syndrome. This paper reviews the history of research and conservation activities on behalf of this critically endangered species at a critically important field site.

Deslocamento Terrestre e o Comportamento de Beber em Um Grupo de Barbados (Alouatta guariba clamitans Cabrera, 1940) em Minas Gerais, Brasil

Dentre os diversos estudos envolvendo o gênero Alouatta, o comportamento locomotor tem sido bastante discutido (Mendel, 1976; Youlatos, 1993; Cant, 1986; Prates et al., 1990; Gebo, 1992; Bicca-Marques e Calegaro-Marques, 1995), embora sejam poucos os registros sobre o deslocamento terrestre. Um outro comportamento pouco documentado é o de beber água, considerado não muito comum para o gênero, já que os barbados obtêm água dos alimentos consumidos; principalmente folhas novas e de frutos (Glander, 1978; Bicca-Marques, 1992). O presente estudo relata a ocorrência de eventos de uso do solo para locomoção e obtenção de água em um grupo de Alouatta guariba clamitans e discute as possíveis causas para estes comportamentos nos barbados da Reserva Particular do Patrimônio Natural (RPPN) Feliciano Miguel Abdala / Estação Biológica de Caratinga (EBC).

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.

Is the Atlantic Forest protected area network efficient in maintaining viable populations of Brachyteles hypoxanthus

Habitat loss and fragmentation are serious threats to biodiversity conservation in the Atlantic Forest. A network of protected areas is essential to the protection of native biodiversity. However, internal and external factors may threaten the preservation of biota, thus population viability analyses (PVA) are important tools in protected area design and management planning. A PVA was carried out, using the computer package VORTEX, to assess the effectiveness of the protected area network within the Atlantic Forest in Brazil in retaining viable populations of the endemic primate Brachyteles hypoxanthus. The Brazilian Atlantic Forest has 42 protected areas within B. hypoxanthus geographic distribution area, and only five of those were considered to retain viable populations for 50 generations, whereas 28 were predicted to suffer from genetic decay, seven from both genetic decay and demographic stochasticity, and two of them are probably extinct populations. The model indicates that although the protected area network of the Atlantic Forest will likely keep B. hypoxanthus populations for the next 50 generations, most of them (35 out of 42, or 83%) will be facing some kind of demographic and/or genetic problem and will probably need management actions to be implemented in order to ensure their persistence.

Evolutionary Biology and Conservation of Titis, Sakis and Uacaris: Why we know so little: the challenges of fieldwork on the Pitheciids

Introduction Possessing a suite of unusual and interesting features, Pitheciids are at the extremes of many of primatology’s ecological and sociological continua (see Norconk 2011). Pitheciids should provide acute tests of many primatological models; however, this is frequently thwarted by the lack of even the most basic quantitative information concerning ecology, behavior and social organization. Such gaps are due not only to the small number of studies, but also to difficulties in obtaining data. This chapter considers why, given that these primates possess such aesthetic and intellectual appeal and high conservation value, they have been so little studied. The peculiarities of pitheciids, combined with their native habitats’ inherent challenges, have often undermined potentially successful fieldwork. Some researchers who began working with species of Callicebus or Chiropotes, for example, simply gave up because of problems habituating the animals or because the study was so difficult that the quality and quantity of gained data would not be worth the effort. Several researchers who persisted were either unable to obtain the expected volume of data or were incapable of answering many of their initial research questions, sometimes both. Using field experiences from a variety of research projects across a range of habitat types and pitheciid taxa, this chapter reports on the problems that arose during these studies and presents suggestions to minimize similar difficulties in the future.