RESUMO

The yellow-tailed woolly monkey, Lagothrix flavicauda (Humboldt, 1812), is a large atelid endemic to the cloud forests of Peru. The identity of this species was uncertain for at least 150 years, since its original description in 1812 without a voucher specimen. Additionally, the absence of expeditions to the remote Peruvian cloud forests made it impossible to collect material that would help to confirm the true identity of L. flavicauda during the 19th and first half of the 20th century. Until now, the specimens of L. flavicauda collected by H. Watkins, in 1925, in La Lejía (Amazonas, Peru) were thought to be the oldest ones deposited in any scientific collection. Nevertheless, after reviewing the databases of the several international museums and literature, we found one specimen of L. flavicauda deposited at the Muséum National dhistoire Naturelle (Paris, France) collected in 1900 by G.A. Baër, in the most eastern part of San Martín (Peru), where the presence of this species was not confirmed until 2011. Thus, Baërs specimen represents the oldest known specimen of the yellow-tailed woolly monkey and the only one coming from the eastern part of the species distribution. Finally, we highlight the importance of online scientific databases for easily diagnosable species. However, caution needs to be taken when using them. We also discuss the value of scientific collections as sources of new discoveries.(AU)

Assuntos

RESUMO

The yellow-tailed woolly monkey, Lagothrix flavicauda (Humboldt, 1812), is a large atelid endemic to the cloud forests of Peru. The identity of this species was uncertain for at least 150 years, since its original description in 1812 without a voucher specimen. Additionally, the absence of expeditions to the remote Peruvian cloud forests made it impossible to collect material that would help to confirm the true identity of L. flavicauda during the 19th and first half of the 20th century. Until now, the specimens of L. flavicauda collected by H. Watkins, in 1925, in La Lejía (Amazonas, Peru) were thought to be the oldest ones deposited in any scientific collection. Nevertheless, after reviewing the databases of the several international museums and literature, we found one specimen of L. flavicauda deposited at the Muséum National dhistoire Naturelle (Paris, France) collected in 1900 by G.A. Baër, in the most eastern part of San Martín (Peru), where the presence of this species was not confirmed until 2011. Thus, Baërs specimen represents the oldest known specimen of the yellow-tailed woolly monkey and the only one coming from the eastern part of the species distribution. Finally, we highlight the importance of online scientific databases for easily diagnosable species. However, caution needs to be taken when using them. We also discuss the value of scientific collections as sources of new discoveries.

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RESUMO

RESUMEN La disminución de las poblaciones del mono choro común (Lagothrix lagotricha) ha llevado a categorizar la especie como amenazada, además, muchos ejemplares se mantienen en cautiverio debido al tráfico ilegal. La hematología es una herramienta muy útil para evaluar el bienestar y diagnóstico de condiciones patológicas, siendo necesario contar con parámetros referenciales para todas las especies de primates mantenidas en cautiverio. El objetivo del presente estudio fue determinar los valores hematológicos de ejemplares de mono choro común (L. lagotricha) bajo cautiverio en los zoológicos de la ciudad de Lima, (Perú). Para ello, el estudio contó con una población total de 28 individuos distribuidos en siete zoológicos, 16 hembras y 12 machos de cuatro grupos etarios diferentes. Se realizó la captura y contención físico-química de los primates utilizando mallas y un protocolo anestésico combinando clorhidrato de ketamina y xilazina. Las muestras de sangre se obtuvieron por punción de la vena femoral, se colectaron en tubos estériles con anticoagulante EDTA y se mantuvieron en refrigeración hasta su análisis. Se obtuvieron los siguientes resultados: eritrocitos 8,76 x 106/μl (± 2,91); hematocrito 36,46% (± 3,38); hemoglobina 12,32 g/dl (± 1,89); VCM 60,61 fl (± 7,85); HCM 20,37 pg (± 3.07); CMCH 33,85 g/dl (± 4,61); leucocitos 6,12 x 103/μl (± 1,05); abastonados 0,05 x 103/μl (± 0,11); segmentados 5,54 x 103/μl (± 2,23); linfocitos 2,62 x 103/ul (± 1,60); monocitos 0,07 x 103/μl (± 0,02); eosinófilos 0,42 x 103/μl (± 0,23); basófilos 0,13 x 103/μl (± 0,14) y plaquetas 314,39 x 103/μl (± 78,09). Se encontró diferencia estadística significativa para el valor de monocitos en relación al sexo.

ABSTRACT The decrease in the populations of common woolly monkey (Lagothrix lagotricha) has generated its categorization as an endangered species, and many specimens are kept in captivity due to illegal trafficking. Hematology is a very useful tool to assess the well-being and diagnosis of pathological conditions, it is necessary to have reference parameters for all primate species kept in captivity. The aim of this study was to determine the hematological values of the common woolly monkey (L. lagotricha) kept in captivity in zoos in Lima-Peru. The study was counted with 28 individuals in seven zoos, 16 females and 12 males from four different age groups. Primates were captured and the physical-chemical containment was done using screens and an anesthetic protocol based on a combination of ketamine hydrochloride and xylazine. Blood samples were obtained by puncture of the femoral vein and placed into sterile tubes with EDTA anticoagulant and refrigerated until analysis. The following results were obtained: erythrocytes 8,76 x 10<7ul (± 2,91), hematocrit 36,46% (± 3,38), hemoglobin 12,32 g/dl (± 1,89), MCV 60,61 fl (± 7,85), HCM 20,37 pg (± 3,07), CMHC 33,85 g/dl (± 4,61), leucocytes 6,12 x 103/μl (± 1,05), abastonados 0,05 x 103/μl (± 0,11), segmented 5,54 x 103/μl (± 2,23), lymphocytes 2,62 x 103/μl (± 1,60), monocytes 0,07 x 103/μl (± 0,02), eosinophils 0,42 x 103/μl (± 0,23), basophils 0,13 x 103/μl (± 0,14) and platelets 314,39 x 103/μl (± 78,09). A significant statistical difference to the value of monocytes in relation to sex was found.

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Dipetalonema gracile (Rudolphi, 1809) (Filarioidea: Onchocercidae) is one of six species of cavities filarial parasites of Neotropical non-human primates. The present study recorded the occurrence of D. gracile, provides morphological and morphometric data and extends the geographical distribution. Adult filariae were obtained from the thoracic and abdominal cavities of 38 specimens of woolly monkey, which were used for local human consumption, in the northeastern Peruvian Amazon. Male and female filarids were processed and analysed using light and scanning electron microscopy. Details of the cephalic papillae, post-cloacal bands and papillae, vulva, phasmid position and lateral appendages are showed by scanning electron microscopy and is recorded the occurrencce of Lagothrix poeppigii monkey as a new host of this filaria in the Yavari-Mirin river basin, Peruvian Amazon.(AU)

Dipetalonema gracile (Rudolphi, 1809) (Filarioidea: Onchocercidae), é uma das seis espécies de filarias parasitas de primatas não humanos neotropicais. O presente trabalho registra a ocorrência de D. gracile , proporciona dados morfológicos e morfométricos e amplia sua distribuição geográfica. Filárias adultas foram obtidas da cavidade torácica e abdominal de 38 espécimes de macaco barrigudo, que foram utilizados para consumo humano local. Essa espécie de primatas não humanos neotropicais tem distribuição ao nordeste da Amazônia peruana. Filarídeos machos e fêmeas foram processados e analisados pela microscopia de luz e microscopia eletrônica de varredura. Detalhes das papilas cefálicas, bandas e papilas pós-cloacais, vulva, posição dos fasmídeos e apêndices laterais são mostradas pela microscopia eletrônica de varredura e registra-se a ocorrência do macaco Lagothrix poeppigii como novo hospedeiro desta filaria na bacia do rio Yavari-Mirin na Amazônia peruana.(AU)

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RESUMO

Abstract Dipetalonema gracile (Rudolphi, 1809) (Filarioidea: Onchocercidae) is one of six species of cavities filarial parasites of Neotropical non-human primates. The present study recorded the occurrence of D. gracile, provides morphological and morphometric data and extends the geographical distribution. Adult filariae were obtained from the thoracic and abdominal cavities of 38 specimens of woolly monkey, which were used for local human consumption, in the northeastern Peruvian Amazon. Male and female filarids were processed and analysed using light and scanning electron microscopy. Details of the cephalic papillae, post-cloacal bands and papillae, vulva, phasmid position and lateral appendages are showed by scanning electron microscopy and is recorded the occurrencce of Lagothrix poeppigii monkey as a new host of this filaria in the Yavari-Mirin river basin, Peruvian Amazon.

Resumo Dipetalonema gracile (Rudolphi, 1809) (Filarioidea: Onchocercidae), é uma das seis espécies de filarias parasitas de primatas não humanos neotropicais. O presente trabalho registra a ocorrência de D. gracile , proporciona dados morfológicos e morfométricos e amplia sua distribuição geográfica. Filárias adultas foram obtidas da cavidade torácica e abdominal de 38 espécimes de macaco barrigudo, que foram utilizados para consumo humano local. Essa espécie de primatas não humanos neotropicais tem distribuição ao nordeste da Amazônia peruana. Filarídeos machos e fêmeas foram processados e analisados pela microscopia de luz e microscopia eletrônica de varredura. Detalhes das papilas cefálicas, bandas e papilas pós-cloacais, vulva, posição dos fasmídeos e apêndices laterais são mostradas pela microscopia eletrônica de varredura e registra-se a ocorrência do macaco Lagothrix poeppigii como novo hospedeiro desta filaria na bacia do rio Yavari-Mirin na Amazônia peruana.

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The intrauterine development is an evolutionary strategy that prepares the neonate for extra-uterine life, thus providing important information on the life history of species. In this study, we described the external and internal morphology of 25 fetuses of Poeppig's woolly monkeys (Lagothrix poeppigii) by taking advantage of a 10-year participatory collection of biological samples originated from animals hunted for subsistence purposes in the Peruvian Amazon. Logistic regressions estimated the probability of occurrence of each external morphological characteristic in relation to the crown-rump length (CRL). The presence of nails, closed eyelids, differentiated genitalia and formed limbs with separation of the digits were observed in all analyzed fetuses (≥4.2 cm CRL). The other characteristics appeared in the following order: skin with epidermal pigmentation, oral and nasal mucosal pigmentation, tactile pelage and covering pelage. Although advanced fetuses (>15.8 cm CRL) showed most fetal external characteristics, they were not fully developed and no specimen showed tooth eruption or opened eyelids. The growth formula used to determine fetal age was ∛W = 0.042 (t - 45), with a high linear relationship between CRL and gestational age. All associations between the external biometry, absolute volume of internal organs and the CRL had a high coefficient of determination. Advanced fetuses and adults showed similar relative volume of thoracic and abdominal organs, except for thymus and the liver with a higher and lower relative volume, respectively. The relative volume of the tubular gastrointestinal tract and the thymus had a constant increase along fetal development, and the liver showed a significant decrease. This study describes important morphological events for understanding the gestational development in the Lagothrix genus. In addition, these results may be useful to improve imaging techniques, contributing to the in situ and ex situ reproductive management of this highly hunted species in the Amazon.

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Lagothrix flavicauda es endémica y vive en simpatría con otros primates en bosques montanos de Amazonas, San Martín, La Libertad y Huánuco. Información detallada sobre su abundancia y estado de conservación, así como de los sitios con poblaciones saludables son desconocidas, excepto para Amazonas donde fueron ejecutados la mayoría de los estudios. Para obtener la información sobre los aspectos mencionados fueron conducidos censos por transecto entre noviembre y diciembre del 2015, febrero a mayo del 2016 y entre junio y julio del 2016 en seis sitios de muestreo localizados entre las regiones de San Martín y Huánuco. Como resultado de los censos fueron avistados 49 grupos pertenecientes a 7 especies, siendo L. flavicauda la más observada con 14 grupos. Grupos más grandes se observaron en L. flavicauda (promedio 13.5±2.2 individuos) y Cebus yuracus (promedio 12.5±3.6 individuos) y más pequeños en Alouatta seniculus (promedio 3.0±2.4 individuos), ambos en Huánuco. La abundancia relativa fue más alta para L. flavicauda en San Martín (2.4 individuos/10 km) y más baja para A. seniculus en Huánuco (0.2 individuos/10 km). Con el registro de L. flavicauda en el lado oriental del río Huallaga su distribución en Huánuco se amplía hasta el río Pozuzo, pero en el lado occidental podemos considerarlo localmente extinta en gran parte de su distribución. En los sitios de muestreo, la deforestación y la caza son las principales amenazas para los primates y otros componentes de la fauna silvestre

Lagothrix flavicauda is endemic and lives sympatrically with other primates in the montane forests of Amazonas, San Martín, La Libertad and Huánuco. Detailed information on its density and conservation status, as well as sites with healthy populations is lacking, except for Amazonas where most of the studies were carried out. In order to obtain information on the mentioned aspects, transect censuses were conducted between November and December of 2015, February to May of 2016, and between June and July of 2016 in six survey sites located in the regions of San Martín and Huánuco. As a result of the census, 49 groups belonging to 7 species were sighted, being L. flavicauda the most observed with 14 groups. The largest groups were observed in L. flavicauda (average 13.5±2.2 individuals) and Cebus yuracus (average 12.5±3.6 individuals) and the smallest in Alouatta seniculus (average 3.0± 2.4 individuals), both in Huánuco. The relative abundance was the highest for L. flavicauda in San Martín (2.4 individuals /10 km) and the lowest for A. seniculus in Huánuco (0.2 individuals/ 10 km). Our observation of L. flavicauda on the eastern side of the Huallaga River extends its distribution in Huánuco to the Pozuzo River, but on the western side we can consider it locally extinct in much of its distributional range. At our survey sites, deforestation and hunting are the main threats to primates and other components of wildlife

RESUMO

The taxonomic history of the genus Lagothrix is complex, with molecular and morphological assessments giving conflicting results for the separation between its taxa. Phylogeographic studies of the most widely distributed species, Lagothrix lagotricha, have only been attempted recently and are limited to few individuals per collection site, many of which were captive making their geographical origin dubious. There is debate regarding the possibility of raising subspecies of Lagothrix lagotricha to the species level, therefore the geographical origin of samples is particularly relevant. In the present work we revisit the intraspecific phylogeography of L. lagotricha from northwestern South America, including the subspecies L. l. poeppiggi, L. l. lagotricha and L. l. lugens (sensu Fooden, 1963), using DNA sequence data from hypervariable region I of the mitochondrial control region (D-loop HVI). Our results suggest a complex picture in which there are well delimited evolutionary units that, nonetheless, do not correlate well with the morphological variation used to support the current delimitation of taxa. Additionally, we corroborate previous results showing a lack of reciprocal monophyly between the putative subspecies of Lagothrix lagotricha, and we propose that this may be due to ancestral polymorphism that has been maintained following the recent spread of woolly monkeys throughout the western Amazonian lowlands and into the inter-Andean region of Colombia.

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Using complete mitochondrial genome sequences, we provide the first molecular analysis of the phylogenetic position of the yellow-tailed woolly monkey, Lagothrix flavicauda (a.k.a. Oreonax flavicauda), a critically endangered neotropical primate endemic to northern Perú. The taxonomic status and phylogenetic position of yellow-tailed woolly monkeys have been debated for many years, but in this study both Bayesian and maximum likelihood phylogenetic reconstructions unequivocally support a monophyletic woolly monkey clade that includes L. flavicauda as the basal taxon within the radiation. Bayesian dating analyses using several alternative calibrations suggest that the divergence of yellow-tailed woolly monkeys from other Lagothrix occurred in the Pleistocene, ∼2.1Ma, roughly 6.5 my after the divergence of woolly monkeys from their sister genus, Brachyteles. Additionally, comparative analysis of the cytochrome oxidase subunit 2 (COX2) gene shows that genetic distances between yellow-tailed woolly monkeys and other Lagothrix from across the genus' geographic distribution fall well within the range of between-species divergences seen in a large number of other platyrrhine primate genera at the same locus and outside the range of between-genus divergences. Our results thus confirm a position within Lagothrix for the yellow-tailed woolly monkey and strongly suggest that the name Oreonax be formally considered a synonym for this genus. This revision in taxonomic status does not change the dire conservation threats facing the yellow-tailed woolly monkey in Perú, where the remaining wild population is estimated at only ∼10,000 individuals living in a highly fragmented landscape.

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