Brachyteles Hypoxanthus Research Articles

Muriqui House: conservation management to support the recovery of the northern muriqui Brachyteles hypoxanthus in Ibitipoca, Minas Gerais, Brazil

Abstract Ensuring the demographic and genetic viability of small populations of threatened primates requires a range of management approaches. Here we describe a novel mixed in situ and ex situ management project that was developed to restore a population of the Critically Endangered northern muriqui Brachyteles hypoxanthus. This isolated population, located in Ibitipoca, Lima Duarte, Minas Gerais, Brazil, had declined to two adult males and would have gone extinct without intervention. A first attempt at in situ management in 2017 involved the translocation of a solitary female from another region, but this female did not associate or interact with the males and disappeared after 9 months. We thus initiated a second and ongoing ex situ management project that involved constructing a complex consisting of a large, open-air enclosure abutting a small patch of forest surrounded by an open area in the process of restoration, all of which is protected by electric fencing. The entire area within the fencing is called Muriqui House. The two Ibitipoca males and two solitary, wild females from another location were captured and released into the enclosed part of Muriqui House between March 2019 and January 2020 and into the forested part of Muriqui House in February 2020. The birth of an infant in this group in November 2020 and the acceptance by the group of a third female translocated from another area in January 2021 demonstrate the potential of this approach for the recovery of this isolated population, with positive implications for the conservation of the species.

First record of Cebidicola armatus (Phthiraptera: Trichodectidae) on the Brachyteles hypoxanthus (Primate: Atelidae) in Brazil.

This study reports for the first time the infestation of Cebidicola armatus in Brachyteles hypoxanthus. In total, 14 lice were recovered of an individual in Minas Gerais, Brazil. These were subjected to a microscopic analysis and the identification of C. armatus was carried out through its very characteristic morphology.

Observations on the anatomy of the funiculus spermaticus and the testis in Brachyteles sp. (SPIX, 1823) primates - Atelidae.

Analysing the literature about the reproductive anatomy on New World Primates, one can see the need of standardisation on the description methods and, more importantly, the lack of detailed information. The problem is aggravated by the difficult access to specimens of the endangered species such as Brachyteles sp. This paper's objective was to extend knowledge on the male reproductive anatomy of these primates. The testis and funiculus spermaticus of Brachyteles are described in detail. We utilised one individual of Brachyteles arachnoides, two hybrids (B. arachnoides × Brachyteles hypoxanthus) and photographs of the testis of a third fresh specimen of a hybrid individual. The septum formed by tunica dartos adheres to the testis and separates the scrotum in two testicular cavities. Passed the spermatic cord, the external spermatic fascia continues with the tunica dartos, covering the cranial half of the testis. The fascia cremasterica divides itself in bundles of fibres and forms loops around the testicles creating a sac like structure that seems to be unique among Neotropical Primates. The appendix testis is described for the first time in platyrrhini. It is presented as a sessile structure in the extremitas capitata of the testis. Previous literature on the reproductive anatomy of platyrrhini is limited. Despite that, it can be said that the large size and volume of the testis, and complex structure of the cremaster, could consist of a heat loss reduction strategy in cold and humid forest environments. Except for the larger size of the testicles in hybrid individuals, no other significant morphological differences were found between B. arachnoides and hybrids (B. arachnoides × B. hypoxanthus).

Assessing the gut microbiome and the influence of host genetics on a critically endangered primate, the northern muriqui (Brachyteles hypoxanthus)

AbstractThe Northern muriqui (Brachyteles hypoxanthus) is one of the world's most critically endangered primates, with only ~1000 mature individuals remaining in the wild. Habitat loss and hunting have led to its sharp decline, making conservation efforts crucial. Analyses of gut microbiomes in wild populations can provide valuable information on host health and vulnerability, and ultimately, contribute to baseline knowledge toward improving conservation programs and reintroduction efforts. In this study, we analyzed the microbiome (16S rRNA metabarcoding) of fecal samples belonging to 53 uniquely genotyped individuals from three social groups from the Caparaó National Park, aiming to provide the first assessment of the microbiome diversity and composition for this species. Our results showed the muriqui gut microbiome was predominantly composed of the phyla Bacteroidetes and Firmicutes, with the dominant classes represented by Bacteroidia and Clostridia. High similarity in bacterial diversity and composition was found for individuals from distinct groups, suggesting a negligible geographical effect at the fine spatial scale analyzed. No significant effect of host genotype heterozygosity levels on microbiota diversity was recovered, but a significant influence of genetic distance on microbiota community structure and composition was demonstrated. Our findings stress the importance of considering associations between host genetics and the microbiome and suggest that the analyzed populations host a similar microbiome composition. This detailed microbiome assessment can aid conservation actions, including future anthropogenic impact assessments and animal reintroductions.

First record of the southern muriqui (Brachyteles arachnoides) in the state of Minas Gerais, Brazil.

The Critically Endangered southern muriqui (Brachyteles arachnoides) and its sister taxon the northern muriqui (Brachyteles hypoxanthus) are endemic to the Atlantic Forest in Brazil. To date, our understanding of the distribution of the southern muriqui has restricted it to the states of Paraná, São Paulo, and Rio de Janeiro. The northern muriqui occurs in the states of Minas Gerais, Rio de Janeiro, Espírito Santo, and Bahia. Here, we describe the first record of the southern muriqui in Minas Gerais. A group of seven individuals, including one infant, was detected and photographed on aprivate property in the district of Monte Verde, municipality of Camanducaia, on the northwestern slope of the Serra da Mantiqueira. This location is 5.3km from a population of southern muriquis (known since 1994) on the southeastern slope of the serra in São Paulo. This discovery highlights the importance of further surveys in the Serra da Mantiqueira in order to detect any new populations, provide data for a more accurate assessment of the conservation status of the two species-the delimitation of their distributions, the size and extent of isolation of their populations, and the threats they face.

Do século XVI ao XXI: registros antigos e recentes de Brachyteles arachnoides (Primates, Atelidae) no Estado do Rio de Janeiro

ABSTRACT. Two muriqui species are currently described in the literature: the southern muriqui, Brachyteles arachnoides (E. Geofroy, 1806) and the northern muriqui, Brachyteles hypoxanthus (Kuhl, 1820). Nowadays, the distribution of the southern muriqui is restricted to forest patches of the states of Rio de Janeiro, São Paulo and Paraná, while the northern muriqui occurs in Espírito Santo, Bahia and Minas Gerais. Both are threatened species, but there are still many gaps in our knowledge of their occurrence, especially for southern muriquis in the state of RJ. The purpose of this work is precisely to identify the primary areas of occurrence of the muriqui in Rio de Janeiro through historical reports by naturalists, adventurers and others since the 16th century. Thus, allowing to assist in the establishment and conservation strategies of the species.

Snapshot of the Atlantic Forest canopy: surveying arboreal mammals in a biodiversity hotspot

AbstractThe Atlantic Forest of South America supports a rich terrestrial biodiversity but has been reduced to only a small extent of its original forest cover. It hosts a large number of endemic mammalian species but our knowledge of arboreal mammal ecology and conservation has been limited because of the challenges of observing arboreal species from ground level. Camera trapping has proven to be an effective tool in terrestrial mammal monitoring but the technique has rarely been used for arboreal species. For the first time in the Atlantic Forest, we obtained data on the arboreal mammal community using arboreal camera trapping, focusing on Caparaó National Park, Brazil. We placed 24 infrared camera traps in the forest canopy in seven areas within the Park, operating them continuously during January 2017–June 2019. During this period the camera traps accumulated 4,736 camera-days of footage and generated a total of 2,256 photographs and 30-s videos of vertebrates. The arboreal camera traps were able to detect arboreal mammals of a range of body sizes. The mammal assemblage comprised 15 identifiable species, including the Critically Endangered northern muriqui Brachyteles hypoxanthus and buffy-headed marmoset Callithrix flaviceps as well as other rare, nocturnal and inconspicuous species. We confirmed for the first time the occurrence of the thin-spined porcupine Chaetomys subspinosus in the Park. Species richness varied across survey areas and forest types. Our findings demonstrate the potential of arboreal camera trapping to inform conservation strategies.

Thanatology in the northern muriqui (Brachyteles hypoxanthus).

Primate thanatology, or the study of primate responses to dying and death, has become increasingly relevant in recent years. However, the number of reports remains small and the quality of published records is highly variable. Here, we extend the literature on comparative thanatology with observations on a population of the northern muriqui (Brachyteles hypoxanthus). We compiled all seven cases of muriqui responses to dead, dying, or abandoned infants observed by trained researchers of the Muriqui Project of Caratinga between 1998 and 2020. Four different adult females were observed carrying their dead offspring (n = 4) and one of these females was also observed carrying her dead grand-offspring (n = 1). Five of the seven cases involved dead newborns, one involved a newborn abandoned by its mother on the forest floor, and one involved a 1.6-year-old infant that was visibly ill and died after its mother left it on the ground. Dead newborns were carried for 1-3days, and all cases occurred during the dry season months. No other age-sex classes were observed to interact with the dead or dying immatures. Our observations are consistent with hypotheses concerning the predominance of dead-infant carrying in other primates, and with the effects of climate on rates of corpse disintegration. They also show the value of long-term studies for obtaining and understanding anecdotal records of rare behavior.

Dam failure and mammals

Brazil experienced the largest socioenvironmental catastrophe of its history, caused by a tailings dam failure, known as “Mariana disaster”. The wave of iron-mining waste buried villages, contaminated the Doce River, and left an immense ocean plume. The Doce River watershed is the largest in southeast Brazil, and located in the Atlantic Forest domain, presenting an outstanding economic, social, and biological relevance. Although the effects of such tragic events are usually assessed through fish assemblage changes, mammals have important effects on environment structure and regeneration. Inventories are of prime importance for adequate conservation efforts as well as for evaluating impacts of any disaster. Therefore, the aim of this paper was to present an updated assessment of mammalian list collected in the affected portion of Doce River before the dam failure therefore contributing to future conservation efforts. Data collection comprised specimens deposited in Museu Nacional/UFRJ, the oldest mammal collection of Brazil, and literature review. The two surveys together retrieved 157 species from 31 families and 11 orders, representing around 60% of the known mammalian diversity in the Atlantic Forest, including some in critical conservation condition, such as the Franciscana dolphin, the northern muriqui and the giant otter. Mining is a byproduct of present society, with dam breaches as a recurring problem. Facing the importance of Doce River to both Brazilian biodiversity and society, the chain of events must be taken into account in environmental rehabilitation strategies, and taxa less commonly assessed, like mammals, should be included.

Science, Policy, and Conservation Management for a Critically Endangered Primate in the Atlantic Forest of Brazil

Long-standing concerns about the status of the world's endangered primates have stimulated significant international efforts, such as the primate action plans published by the Primate Specialist Group of the International Union for Conservation of Nature's Species Survival Commission. However, national-level action plans that bring together diverse scientific experts, non-governmental organizations, and governmental agencies to focus on improving the status of endangered species are generally rare. Here, we highlight one such plan published a decade ago, the Brazilian National Action Plan for the Conservation of Muriquis, which promoted the integration of scientific findings about the behavioral ecology, demography, and genetics of northern muriquis with conservation measures supported by the Brazilian government. This plan provided a holistic framework for the development of an effective national strategy that has contributed to significant advances in research and management applied to the conservation of this Critically Endangered species. We hope that this model for muriquis will stimulate conservationists around the world to pursue integrative national-level sponsorship of action plans on behalf of other endangered species.

Pre-capture monitoring for a planned translocation of a northern muriqui (<i>Brachyteles hypoxanthus</i>) female from a forest fragment surrounding Caparaó National Park, Brazil


 
 
 Conservation translocation may play an important and necessary role in primate conservation as several species are facing an impending extinction risk and population decline. However, translocations are a high-cost endeavor. Therefore, pre-capturing monitoring can be an essential component in the success of primate translocation. In this study, we report the first confirmed sighting of a female Northern Muriqui (Brachyteles hypoxanthus) stranded alone in a small fragment of Brazilian Atlantic Forest, and her pre-capture monitoring for a future planned translocation. Monitoring was realized from June 2018 to July 2019, and included data collection through direct observational and arboreal camera trap methods, and non-invasive collection of faecal samples for additional genetic studies. Our results showed that the female used the total area of the 1-ha forest fragment with an average daily displacement of 59.6 m ± 76.2. The female spent most of the time ‘Resting’, followed by ‘Travelling’ and ‘Feeding’, which did not vary significantly between seasons. Intraspecific activity pattern variations may be related to the amount and quality of the feeding resources available in the forest fragments. No stereotyped behavior or advertising signals were reported during the monitoring. Our study provides insights on solitary primates living in marginal habitats and highlight the importance of pre-capture monitoring to provide important information on the general behavior of the target individuals, on the regular movements and overall home ranges, and to help to guide future translocations.
 
 

Phylogeographic evidence for two species of muriqui (genus Brachyteles).

The taxonomy of muriquis, the largest extant primates in the New World, is controversial. While some specialists argue for a monotypic genus (Brachyteles arachnoides), others favor a two-species classification, splitting northern muriquis (Brachyteles hypoxanthus) from southern muriquis (B. arachnoides). This uncertainty affects how we study the differences between these highly endangered and charismatic primates, as well as the design of more effective conservation programs. To address this issue, between 2003 and 2017 we collected over 230 muriqui fecal samples across the genus' distribution in the Brazilian Atlantic Forest, extracted DNA from these samples, and sequenced 423 base pairs of the mitochondrial DNA (mtDNA) control region. Phylogenetic and species delimitation analyses of our sequence dataset robustly support two reciprocally monophyletic groups corresponding to northern and southern muriquis separated by an average 12.7% genetic distance. The phylogeographic break between these lineages seems to be associated with the Paraíba do Sul River and coincides with the transition between the north and south Atlantic Forest biogeographic zones. Published divergence estimates from whole mitochondrial genomes and nuclear loci date the split between northern and southern muriquis to the Early Pleistocene (ca. 2.0 mya), and our new mtDNA dataset places the coalescence time for each of these two clades near the last interglacial (ca. 120-80 kya). Our results, together with both phenotypic and ecological differences, support recognizing northern and southern muriquis as sister species that should be managed as distinct evolutionarily significant units. Given that only a few thousand muriquis remain in nature, it is imperative that conservation strategies are tailored to protect both species from extinction.

Habitat Use in a Population of the Northern Muriqui (Brachyteles hypoxanthus)

Habitat loss and fragmentation are known to restrict the movements of primates, including their ability to expand their home ranges. These effects are especially strong at high densities, where home range overlap can result in high rates of agonistic intergroup encounters over range defense. We investigated habitat use and range defense in a population of northern muriquis (Brachyteles hypoxanthus) at the Reserva Particular do Patrimonio Natural – Feliciano Miguel Abdala, in Minas Gerais, Brazil from August 2010 to July 2013. The four groups in this isolated population used 878 ha of forest, with home ranges exhibiting high interannual fidelity in location and low intergroup overlap. Core areas represented 13–29% of the respective home ranges and, except for one group, showed only moderate to low interannual fidelity in successive years. Of 130 intergroup encounters recorded in 2010–2011, significantly more occurred in core areas that overlapped with the range of another group than in areas of home range overlap or areas used exclusively by one group. Daily path lengths of the one group used in assessing range defensibility varied little (1075–1132 m) across years and relative to home range diameter did not meet the criteria for defensibility. However, the occurrence of independent subgroups, combined with a mean monthly detection distance of 242 m, provides strong evidence of range defensibility. These findings point to the importance of fission–fusion dynamics for intergroup range defense, particularly in primates living at high densities in fragmented habitats.

Status of the northern muriqui (Brachyteles hypoxanthus) in the time of yellow fever.

Understanding the impact of zoonotic diseases on wild primate populations is important for assessing local extinction risks and for evaluating potential mitigating factors. Comparative data on demographic changes in two isolated populations of the northern muriqui (Brachyteles hypoxanthus) during a severe yellow fever outbreak in southeastern Brazil provide unique insights into the potential effects of this disease in this Critically Endangered species. From October 2016 to April 2017, the muriqui population at the Reserva Particular do Patrimônio Natural-Feliciano Miguel Abdala (Caratinga) lost 31 of its 324 members, or nearly 10%, whereas the population at the Reserva Particular do Patrimônio Natural-Mata do Sossego (Sossego) declined from 34 to 25 individuals, or 26%. Greater per-capita risks to muriquis in the Sossego population could be related to ecological and anthropogenic differences, including a wetter climate and an absence of sympatric howler monkeys (Alouatta guariba), which may have directly or indirectly buffered the Caratinga muriquis. Although we lack definitive confirmation that the muriqui population declines were caused by yellow fever, the timing and magnitude of the losses strongly implicate the disease. We highlight the risks of catastrophic population declines in small populations and emphasize the value of long-term demographic monitoring studies.

From the field to the lab: Muriqui endocrinology from a collaborative perspective.

The northern muriqui (Brachyteles hypoxanthus) is a critically endangered species endemic to the Atlantic Forest of southeastern Brazil. Long-term observational studies of wild muriquis have provided many insights into the behavioral ecology and life history of this species. However, nearly everything that is currently known about the northern muriqui's behavioral endocrinology has come from combining our respective expertise in noninvasive field and laboratory research. Here, we reflect on the history of our collaboration, focusing on major challenges, key scientific findings, and factors that contributed to its success. Challenges included insuring the reliable collection of frequent fecal samples from a large enough number of known individuals over extended periods of time, preserving the steroids in the field and transporting them, developing and validating the fecal steroid assays, and interpreting the hormonal profiles within the behavioral and ecological contexts of the study subjects. Major findings included our thorough description of the fecal progesterone and estradiol profiles associated with muriqui ovarian cycling and gestation, the seasonal resumption of cycling, its onset during puberty of dispersing females, and the differences between fertile and infertile cycles. We also documented the relationship between fecal cortisol and testosterone in sexually active males across breeding and nonbreeding seasons, and sex differences in cortisol levels across the mating and conception seasons. We attribute the success of our collaboration to a number of factors including our mutual appreciation for one another's high standards for ethics, data quality, and data interpretation.

Demographic monitoring of wild muriqui populations: Criteria for defining priority areas and monitoring intensity.

Demographic data are essential to assessments of the status of endangered species. However, establishing an integrated monitoring program to obtain useful data on contemporary and future population trends requires both the identification of priority areas and populations and realistic evaluations of the kinds of data that can be obtained under different monitoring regimes. We analyzed all known populations of a critically endangered primate, the muriqui (genus: Brachyteles) using population size, genetic uniqueness, geographic importance (including potential importance in corridor programs) and implementability scores to define monitoring priorities. Our analyses revealed nine priority populations for the northern muriqui (B. hypoxanthus) and nine for the southern muriqui (B. arachnoides). In addition, we employed knowledge of muriqui developmental and life history characteristics to define the minimum monitoring intensity needed to evaluate demographic trends along a continuum ranging from simple descriptive changes in population size to predictions of population changes derived from individual based life histories. Our study, stimulated by the Brazilian government’s National Action Plan for the Conservation of Muriquis, is fundamental to meeting the conservation goals for this genus, and also provides a model for defining priorities and methods for the implementation of integrated demographic monitoring programs for other endangered and critically endangered species of primates.

Unusual intergroup movement of young males in a male philopatric society


 
 
 Deviations from sex-biased dispersal patterns of primate species have often been attributed to local demography, particularly in cases of dispersal by males in what are typically male philopatric societies. Here, we evaluate the demographic conditions associated with novel observations of intergroup movements by two male northern muriquis, Brachyteles hypoxanthus, monitored since their births at the Reserva Particular do Patrimônio Natural - Feliciano Miguel Abdala, in Caratinga, Minas Gerais, Brazil. Specifically, we compare the size and operational sex ratios (OSR) of all four muriqui groups in the study population at the time the two males, aged 5.4 and 7.9 years, left their natal group to associate with members of a non-natal group, and again 3 months later, when the older male, ZS-J, returned to his natal group. We also use Association Indices to evaluate the males’ spatial relationships in their natal and non-natal groups to better understand the social conditions that may have also affected their unusual movements. The two males initially moved from their natal group (Jaó), which had the highest OSR in the population, into the smallest group with the most favorable OSR (M2). However, ZS-J subsequently returned to his natal group despite its much higher OSR. Both males had strong spatial associations in their natal group prior to their departures, but only the younger male achieved similar spatial associations in M2 group, where he remained. ZS-J’s extreme spatial peripheralization in M2 group may have contributed, at least in part, to his return to Jaó group, where his earlier strong spatial associations were restored. These findings suggest that social and demographic factors may be involved in individual deviations from a species or population’s normative dispersal patterns. They also demonstrate the value of long-term field studies of recognized individuals over the duration of their lives for documenting behavioral flexibility.
 
 

New northern muriqui group discovered in Brazil's Caparaó National Park

New northern muriqui group discovered in Brazil's Caparaó National Park

A Current Perspective on the Historical Geographic Distribution of the Endangered Muriquis (Brachyteles spp.): Implications for Conservation.

The muriqui (Brachyteles spp.), endemic to the Atlantic Forest of Brazil, is the largest primate in South America and is endangered, mainly due to habitat loss. Its distribution limits are still uncertain and need to be resolved in order to determine their true conservation status. Species distribution modeling (SDM) has been used to estimate potential species distributions, even when information is incomplete. Here, we developed an environmental suitability model for the two endangered species of muriqui (Brachyteles hypoxanthus and B. arachnoides) using Maxent software. Due to historical absence of muriquis, areas with predicted high habitat suitability yet historically never occupied, were excluded from the predicted historical distribution. Combining that information with the model, it is evident that rivers are potential dispersal barriers for the muriquis. Moreover, although the two species are environmentally separated in a large part of its distribution, there is a potential contact zone where the species apparently do not overlap. This separation might be due to either a physical (i.e., Serra da Mantiqueira mountains) or a biotic barrier (the species exclude one another). Therefore, in addition to environmental characteristics, physical and biotic barriers potentially shaped the limits of the muriqui historical range. Based on these considerations, we proposed the adjustment of their historical distributional limits. Currently only 7.6% of the predicted historical distribution of B. hypoxanthus and 12.9% of B. arachnoides remains forested and able to sustain viable muriqui populations. In addition to measurement of habitat loss we also identified areas for conservation concern where new muriqui populations might be found.

Twinning in titis (<i>Callicebus coimbrai</i>): stretching the limits of biparental infant caregiving?

No abstract