Brachyteles Hypoxanthus Research Articles

Energetic costs of reproduction in female northern muriquis, Brachyteles hypoxanthus (Primates: Platyrrinhi: Atelidae)

Infant care is known to impose high energetic costs on female primates because in addition to lactation, most primate mothers also provide transport for their offspring. Many studies have documented the high energetic costs of lactation, but less is known about energetic costs of infant carrying and their effects on the recovery of maternal physical condition. We compared the activities of female northern muriquis (Brachyteles hypoxanthus Kuhl, 1820) over a 12-month period at the RPPN Feliciano Miguel Abdala, Minas Gerais, Brazil to investigate whether mothers during their weaning year behaved differently than mothers in their post-weaning year, when they resumed reproductive cycling and copulating, and conceived again. We found no significant differences in the behavioral activity budgets of mothers in their weaning year (n = 4) versus post-weaning year (n = 5), despite the significantly higher proportion of time that mothers in their weaning year spent in close proximity with their infants and carrying their infants compared to mothers in their post-weaning year. We suggest that the energy budgets of weaning are similar to those of post-weaning in female northern muriquis.

Reserve selection and persistence: complementing the existing Atlantic Forest reserve system

This study is an exercise to check the efficiency of the existing reserve system, and to show how systematic conservation planning—using information available and the com- plementarity concept—can improve the basis for decisions and minimize costs. We verified the performance, in number of cells and primate species representation, of the existing Atlantic Forest (Brazil) reserve network with a quarter-degree resolution grid, with 1,884 cells. We used occurrence data of 20 endemic primate species, and the maps of 237 existing reserves. Reserve networks were selected to represent primate species first considering no pre-existing reserves in Atlantic Forest, and then, considering the existing reserve system, taking into account the minimum area for viable population of the larger species (Northern muriqui Brachyteles hypoxanthus). Reserve selection was carried out using the complementarity concept implemented by a simulated annealing algorithm. Primate species representation (at least one occurrence in the network) could be achieved with 8% of the existing reserve system (nine cells in relation to the 120 in the existing reserve system). We found that today's reserve system represents 89% of endemic primate species, excluding the species Coimbra Filho's titi monkey (Callicebus coimbrai) and Marcgraf's capuchin (Cebus flavius). The networks selected without considering existing reserves contained nine cells. The networks selected considering existing reserves (120 cells), had two new cells necessary to represent all the primates. This does not mean that a viable alternative is to start from zero (i.e., nonexistent reserves). Identifying critical supplementary areas using biodiversity information to fill the gaps and then starting ''conservation in practice'' in these areas should be priorities.

Seed predation of <i>Mabea fistulifera</i> (Euphorbiaceae) by northern muriquis (<i>Brachyteles hypoxanthus</i>)

Seeds are staple foods in the diets of primates with morphological and behavioral specializations for seed predation, but are considered a less important resource for most other primates. Here we report the first observation of seed predation by northern muriquis (Brachyteles hypoxanthus). Twenty-four Mabea fistulifera (Euphorbiaceae) seed eating events were observed during a systematic study of two groups of northern muriquis in an Atlantic forest fragment in southeastern Brazil in July 2003, accounting for 2.9% of 836 feeding records during this month. Only unripe seeds were consumed in all records. The absence of Mabea fistulifera seeds in any of the 102 fecal samples examined suggests that the seeds were predated. Analyses of 47 fruits of Mabea fistulifera collected in different stages of ripeness in June 2004 indicated that fruits at earlier stages of ripeness were significantly softer than ones of later stages, implying that fruit hardness made their seeds unprofitable to these non-specialized seed predator monkeys.

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.

Genetic structure in two northern muriqui populations (Brachyteles hypoxanthus, Primates, Atelidae) as inferred from fecal DNA

We assessed the genetic diversity of two northern muriqui (Brachyteles hypoxanthus Primata, Atelidae) populations, the Feliciano Miguel Abdala population (FMA, n = 108) in the Brazilian state of Minas Gerais (19°44' S, 41°49' W) and the Santa Maria de Jetibá population (SMJ, n = 18) in the Brazilian state of Espírito Santo (20°01' S, 40°44' W). Fecal DNA was isolated and PCR-RFLP analysis used to analyze 2160 bp of mitochondrial DNA, made up of an 820 bp segment of the gene cytochrome c oxidase subunit 2 (cox2, EC 1.9.3.1), an 880 bp segment of the gene cytochrome b (cytb, EC 1.10.2.2) and 460 bp of the hypervariable segment of the mtDNA control region (HVRI). The cox2 and cytb sequences were monomorphic within and between populations whereas the HVRI revealed three different population exclusive haplotypes, one unique to the SMJ population and two, present at similar frequencies, in the FMA population. Overall haplotype diversity (h = 0.609) and nucleotide diversity (pi = 0.181) were high but reduced within populations. The populations were genetically structured with a high fixation index (F ST = 0.725), possibly due to historical subdivision. These findings have conservation implications because they seem to indicate that the populations are distinct management units.

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.

Ocelot (Leopardus pardalis) predation on primates in Caratinga Biological Station, Southeast Brazil

This study demonstrates that ocelots (Leopardus pardalis) extensively use primates as a food resource at the Caratinga Biological Station (CBS) in Southeast Brazil. Analysis of 60 fecal samples collected over 4 years revealed predation upon the brown howler monkey (Alouatta guariba), the muriqui (Brachyteles hypoxanthus), and the brown capuchin monkey (Cebus apella). The most frequent items found in the fecal samples analyzed were Calomys (n=16) and non-identified Aves (n=15), followed by A. guariba (n=12). Although Rodentia was the most common group consumed (n=52) Primates were found in 27% of total fecal samples and were the third most consumed group in relation to the total items. Particularly, predation of A. guariba by ocelots (20% of the total fecal samples) was not an isolated event; our results showed that this species was preyed on across several months. Predation on primates was far higher at CBS than at other sites where comparable studies have been carried out.

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.

Ground use by northern muriquis (Brachyteles hypoxanthus)

Many arboreal primates descend to the ground, a custom that may occur more frequently in disturbed habitats, and in the presence of researchers to whom the primates are habituated. In this paper, we describe opportunistic observations of ground use in two groups of northern muriquis (Brachyteles hypoxanthus) at the RPPN Feliciano Miguel Abdala, Minas Gerais, Brazil. Members of both groups were observed drinking, resting, feeding, playing, and traveling on the ground to different degrees, and variation in the levels of habituation of the two groups may be responsible for the differences in the distribution of their terrestrial activities. The potential increase in vulnerability to predation or disease owing to ground use has implications for the conservation of this critically endangered species.

A case of infant swapping by wild northern muriquis (Brachyteles hypoxanthus)

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.

Estimating Minimum Area of Suitable Habitat and Viable Population Size for the Northern Muriqui (Brachyteles hypoxanthus)

A population viability analysis (PVA) using the computer package VORTEX was conducted to assess the minimum viable population (MVP) of the Atlantic Forest endemic primate Brachyteles hypoxanthus. The objectives were: (1) to estimate demographic and genetic MVPs that could be used as quasi-extinction thresholds for future modeling, and (2) to estimate the minimum area of suitable habitat (MASH). The model predicted that populations of 40 and 700 individuals were necessary to achieve demographic and genetic stability, respectively. The model was more sensitive to changes in inbreeding depression, sex ratio and reproduction (percentage of breeding females). MASH estimated to contain genetically viable populations reached 11,570 ha. Muriquis have managed to persist despite severe habitat disturbance, but the results suggest that although most of the extant populations are not threatened by extinction, they are too small to be genetically viable in the long-run, and will loose most of their heterozygosity.

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

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.

Population demography of Northern muriquis (Brachyteles hypoxanthus) at the Estação Biológica de Caratinga/Reserva particular do Patrimônio Natural‐Felìciano Miguel Abdala, Minas Gerais, Brazil

The 957-ha forest at the Estação Biológica de Caratinga/Reserva Particular do Patrimônio Natural-Felìciano Miguel Abdala, in Minas Gerais, Brazil, supports one of the largest known populations of the critically endangered northern muriqui (Brachyteles hypoxanthus). We combine long-term data on one group that has been monitored since 1982 with new data obtained on the other three groups since 2002 and 2003 to describe the demographic structure of this population, evaluate its potential for future growth, and predict how dispersal and competitive regimes may change in response to current demographic conditions. As of January 2005, the 226 individuals in the population were divided into four mixed-sex groups with 37-77 members, and an all-male unit whose eight males maintained transient associations with two of the mixed-sex groups. Although 51.77% of the population was female, the sex ratio among adults and subadults was female-biased (0.75), while that among immatures was male-biased (1.47). Consistent with expectations from mean interbirth intervals, 64.18% of adult females gave birth in 2003 and 2004. However, by January 2005, only 52.31% of adult females were still carrying infants <24 months of age due to unusually high infant mortality. First-year survivorship among the 25 infants born in the population in 2003 was only 76%, considerably lower than previously documented in the longest-studied group. High female fecundity is indicative of a healthy population, but the current male bias in births will result in a decline in the population growth rate within two decades, and may increase levels of male reproductive competition and alter dispersal patterns.

Directives for the conservation of the northern muriqui, &lt;i&gt;Brachyteles hypoxanthus&lt;/i&gt; (Primates, Atelidae)

&#x0D; &#x0D; &#x0D; &#x0D; 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.&#x0D; &#x0D; &#x0D; &#x0D;

Muriqui populations reported in the literature over the last 40 years

&#x0D; &#x0D; &#x0D; &#x0D; 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.&#x0D; &#x0D; &#x0D; &#x0D;

Management of muriquis (&lt;i&gt;Brachyteles&lt;/i&gt;, Primates) in captivity

&#x0D; &#x0D; &#x0D; &#x0D; 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.&#x0D; &#x0D; &#x0D; &#x0D;

Reproductive biology and conservation of muriquis

&#x0D; &#x0D; &#x0D; &#x0D; This paper summarizes some of the major findings on the reproductive biology of one group of northern muriquis (Brachyteles hypoxanthus) at the RPPN Feliciano Miguel Abdala (previously known as the Estação Biológica de Caratinga). Long-term monitoring of individual members of the Matão group, combined with non-invasive fecal sampling to measure hormone levels, provide insights into ovarian function, reproductive seasonality, and factors that influence individual and population reproductive rates. All of these parameters have direct applications for assessing the long-term viability of this population, and for conservation of this critically endangered species. These findings were presented at the first meeting of the Committee for the Conservation and Management of the Muriqui (IBAMA), held in Teresópolis, Rio de Janeiro, in October 2002; more recent data have been added or are included in the references.&#x0D; &#x0D; &#x0D; &#x0D;

The International Committee for the Conservation and Management of Atlantic Forest Atelids

&#x0D; &#x0D; &#x0D; &#x0D; We briefly describe in this paper the objectives, structure and organization of the International Committee for the Conservation and Management of the Atlantic Forest Atelids. This is an advisory group established to assist the Brazilian Institute for the Environment (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis – IBAMA) in the definition of effective conservation measures for the two species of muriqui (Brachyteles hypoxanthus and B. arachnoides) along with the northern brown howling monkey (Alouatta guariba guariba), all of which are on the Brazilian Official List of Fauna Threatened of Extinction. We also describe the participation of IBAMA’s Center for the Protection of Brazilian Primates (Centro de Proteção de Primatas Brasileiros – CPB) and the Coordination for the Conservation of Threatened Fauna and Migratory Species (Coordenação de Conservação das Espécies da Fauna Ameaçada de Extinção e Migratória – COFAU). These are the sectors of IBAMA most involved with the planning and execution of conservation actions for threatened primates in Brazil.&#x0D; &#x0D; &#x0D; &#x0D;

Population density and vertical stratification of four primate species at the Estação Biológica de Caratinga/RPPN-FMA, Minas Gerais, Brazil

&#x0D; &#x0D; &#x0D; &#x0D; In 2003, we carried out a line-transect sampling for all the primates (Alouatta guariba clamitans, Brachyteles hypoxanthus, Cebus nigritus, and Callithrix flaviceps) at the Estação Biológica de Caratinga (EBC) to estimate the sizes of their populations. Our goal was to examine whether the trend in population growth observed in the northern muriqui population was accompanied by similar trends in the other three species, or if there was a decline which could indicate the possible effect of competition with northern muriquis. In addition, we studied stratification to verify if the different species use the forest strata in different ways to avoid direct competition. We registered a total of 78 sightings of primates: 33 for A. guariba clamitans, 23 for C. nigritus, 18 for B. hypoxanthus and four for C. flaviceps. Our results indicated that A. guariba clamitans continued to be the most abundant primate at the EBC. Cebus nigritus and B. hypoxanthus occur at almost the same abundances, being half of that of brown howlers. Callithrix flaviceps is the least common primate in this forest fragment. Compared to previous studies, our census shows a decline in the abundance of howlers. This study confirms the prediction that larger primates use higher strata of the forest while smaller species move in the lower strata.&#x0D; &#x0D; &#x0D; &#x0D;

The Caratinga Alliance: community-based conservation efforts to increase forest for the muriquis and water for the farmers

&#x0D; &#x0D; &#x0D; &#x0D; The northern muriqui is Critically Endangered. About 25% of the known population lives in the 1,200 ha of secondary for- ests of the Caratinga Biological Station (EBC) Feliciano Miguel Abdala Private Natural Heritage Reserve (RPPN-FMA) and neighboring farms. Long-term survival of the muriquis there depends on an increase in the availability of suitable habitat. Widespread deforestation has depleted soil fertility and dried up the streams in the region. Community-based conserva- tion actions were carried out: 1) to protect and restore degraded areas to increase the availability of forests for the muriquis, and 2) to implement reforestation to improve the water balance vital for the regional recovery of rural production. Rural extension courses were provided for the local communities, which introduced modern production techniques to increase efficiency while decreasing environmental impacts. A new plant nursery was built and a pilot project to test forest restoration techniques was initiated.&#x0D; &#x0D; &#x0D; &#x0D;