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.

Contrasting Rates of LINE-1 Amplification among New World Primates of the Atelidae Family.

LINE-1 (L1) retrotransposons constitute the dominant category of transposons in mammalian genomes. L1 elements are active in the vast majority of mammals, and only a few cases of L1 extinction have been documented. The only possible case of extinction in primates was suggested for South American spider monkeys. However, these previous studies were based on a single species. We revisited this question with a larger phylogenetic sample, covering all 4 genera of Atelidae and 3 species of spider monkeys. We used an enrichment method to clone recently inserted L1 elements and performed an evolutionary analysis of the sequences. We were able to identify young L1 elements in all taxa, suggesting that L1 is probably still active in all Atelidae examined. However, we also detected considerable variations in the proportion of recent elements indicating that the rate of L1 amplification varies among Atelidae by a 3-fold factor. The extent of L1 amplification in Atelidae remains overall lower than in other New World monkeys. Multiple factors can affect the amplification of L1, such as the demography of the host and the control of transposition. These factors are discussed in the context of host life history.

High consumption of primates by pumas and ocelots in a remnant of the Brazilian Atlantic Forest / Alto consumo de primatas por onças-pardas e jaguatiricas em um fragmento na Mata Atlântica no Brasil

We studied the diet of the ocelot and puma during the years 2007 and 2008 at the Feliciano Miguel Abdala Reserve, in Minas Gerais, south-eastern Brazil. We collected 49 faecal samples (scats) from cats, and identified the species of cat from 23 of them by the analysis of the microstructure patterns of hairs found in their faeces: 17 scats of the puma (Puma concolor) and six of the ocelot (Leopardus pardalis). In the puma scats, we identified three species of primates (Brachyteles hypoxanthus, Alouatta guariba and Sapajus nigritus), the remains of which were found in eight of 17 collected (47.1%), representing 26.7% of items consumed. For the ocelot, we detected capuchin monkey (S. nigritus) remains in three of the six scats (50%), accounting for 18.7% of items consumed by ocelot. We were unable to identify the cat species in the remaining 26 faecal samples, but we were able to analyse the food items present. Primates were found in five of these 26 faeces (19.2%) and represented 10.2% of the items found. Although the sample size is limited, our results indicate a relatively high consumption of primates by felines. We believe that this high predation may be the result of the high local density of primates as well as the greater exposure to the risks of predation in fragmented landscapes, which tends to increase the incidence of the primates using the ground.

Nós estudamos a dieta de jaguatiricas e onças-pardas entre os anos de 2007 e 2008 na Reserva Feliciano Miguel Abdala, em Minas Gerais, sudeste do Brasil. Nós coletamos 49 amostras fecais de felinos, em 23 das quais foi possível a identificação do predador através da análise do padrão microestrutural dos seus pelos encontrados nas fezes, sendo 17 fezes de onça-parda (Puma concolor) e seis de jaguatirica (Leopardus pardalis). Nas amostras de onça-parda nós identificamos três espécies de primatas (Brachyteles hypoxanthus, Alouatta guariba e Sapajus nigritus), cujas partes não digeridas foram encontradas em oito das 17 fezes coletadas, representando 26,7% dos itens consumidos por onças-pardas. Para jaguatirica, nós detectamos macacos-prego (S. nigritus) em três de seis fezes, o que correspondeu a 18,7% dos itens consumidos. Para as 26 amostras fecais restantes, cuja identificação do predador não foi possível, nós analisamos os itens alimentares presentes. Restos de primatas foram identificados em cinco dessas fezes (19,3%), representando 10,2% dos itens encontrados. Apesar do tamanho da amostra ser limitado, nossos resultados indicam uma taxa relativamente alta de consumo de primatas por felinos. Nós acreditamos que essa alta taxa de predação pode ser resultado da grande densidade local de primatas, bem como do aumento do risco de predação em paisagens fragmentadas, o que tende a aumentar a incidência do uso do chão por parte dos primatas.

Males follow females during fissioning of a group of northern muriquis.

Although well documented in matrilocal primate species, group fission is still a poorly known phenomenon among patrilocal primates. In this paper we describe in detail a group fission event in the population of northern muriquis at the Reserva Particular do Patrimônio Natural-Feliciano Miguel Abdala in Caratinga, Minas Gerais, Brazil, using Social Network Analyses (SNA). Data on association patterns were collected during systematic observations from May 2002 to September 2005, and analyzed for dry (from May to October) and rainy seasons (from November to April). The fission process started with subgroup formation in the rainy season 2002-2003, and was completed by the dry season of 2003. By the dry season 2003, the parent group (Jaó) had fissioned to form a second mixed-sex group (Nadir) while a subgroup of males (MU) moved between the parent group and the newly established group. Before the Jaó group fission started (dry season 2002) and during its initial phases (rainy season 2002-2003), females that ultimately composed the daughter group (Nadir) were the most peripheral in the association network. In the rainy season 2002-2003, the median monthly (N=6) operational sex ratio (OSR) of Jaó group was 2.81. However, once Jaó females initiated the fissioning process to establish the Nadir group, the OSR was more favorable to males in the Nadir group than in the Jaó group. Our results suggest that males followed the females to escape an unfavorable OSR in their natal group.

Mamíferos do Parque Estadual do Desengano, Rio de Janeiro, Brasil / Mammals of Desengano State Park, Rio de Janeiro, Brazil

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 por cento das espécies de mamíferos com ocorrência conhecida para o Estado, destacando a importância da área para a conservação da fauna do Rio de Janeiro.

Even after the devastation of large part of its forests, Rio de Janeiro State still harbors a rich terrestrial mammal fauna. However, information on the distribution and abundance of mammal species in the State is still scarce. This study aims to survey the mammals of the Desengano State Park, located on the northern part of Rio de Janeiro, one of the least studied and most altered regions of the State. The inventory was conducted using Sherman, Tomahawk, and pitfall traps for non-volant small mammals, mist nets for bats, camera traps, sightings and reports of residents and officials of the Park for large mammals. We recorded 56 species of mammals, of which 15 are on the list of threatened fauna of Rio de Janeiro State and 10 on the list of Brazilian threatened fauna, including Brachyteles arachnoides. The most abundant species were the bat Sturnira lilium and the rodent Akodon serrensis. Moreover, Thaptomys nigrita, a rodent not commonly captured in the State, was relatively abundant in the Desengano State Park. Results indicate that the park harbors 33.7 percent of the species of mammals known to occur in the State, highlighting the importance of the area for the conservation of Rio de Janeiro fauna.

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.

Capture techniques and morphometrics for the woolly spider monkey, or muriqui (Brachyteles arachnoides, E. Geoffroy 1806).

A total of 12 free-ranging muriquis (Brachyteles arachnoides) were captured with Telazol® at Fazenda Esmeralda, Minas Gerais, Brazil, and at Fazenda Barreiro Rico, São Paulo, Brazil. All animals were measured, marked, weighed, and released. Previously reported data suggested that Brachyteles is a sexually dimorphic species with female-male body weights of 12-15 kg, respectively. We found no statistically significant difference in body weight between females (mean = 8.4 kg, range = 6.9-9.3 kg, n = 4), and males (mean =9.6 kg, range = 9.3-10.2 kg, n = 4). Our results are at variance with previously published body weights in the literature. Larger sample size may reveal a significant sexual difference, particularly in body weight. © 1993 Wiley-Liss, Inc.