Molecular phylogeny of the genus Saguinus (Platyrrhini, Primates) based on the ND1 mitochondrial gene and implications for conservation

The systematics of the subfamily Callitrichinae (Platyrrhini, Primates), a group of small monkeys from South America and Panama, remains an area of considerable discussion despite many investigations, there being continuing controversy over subgeneric taxonomic classifications based on morphological characters. The purpose of our research was to help elucidate the phylogenetic relationships within the monkey genus Saguinus (Callitrichinae) using a molecular approach to discover whether or not the two different sections containing hairy-faced and bare-faced species are monophyletic, whether Saguinus midas midas and Saguinus bicolor are more closely related than are S. midas midas and Saguinus midas niger, and if Saguinus fuscicollis melanoleucus and Saguinus fuscicollis weddelli really are different species. We sequenced the 957 bp ND1 mitochondrial gene of 21 Saguinus monkeys (belonging to six species and nine morphotypes) and one Cebus monkey (the outgroup) and constructed phylogenetic trees using maximum parsimony, neighbor joining, and maximum likelihood methods. The phylogenetic trees obtained divided the genus Saguinus into two groups, one containing the small-bodied species S. fuscicollis and the other, the large-bodied species S. mystax, S. leucopus, S. oedipus, S. midas, S. bicolor. The most derived taxa, S. midas and S. bicolor, grouped together, while S. fuscicollis melanoleucus and S. f. weddelli showed divergence values that did not support the division of these morphotypes into subspecies. On the other hand, S. midas individuals showed divergence compatible with the existence of three subspecies, two of them with the same morphotype as the subspecies S. midas niger. The results of our study suggest that there is at least one Saguinus subspecies that has not yet been described and that the conservation status of Saguinus species and subspecies should be carefully revised using modern molecular approaches.

The current status of the new world monkey phylogeny

Four DNA datasets were combined in tandem (6700 bp) and Maximum parsimony and Neighbor-Joining analyses were performed. The results suggest three groups emerging almost at the same time: Atelidae, Pitheciidae and Cebidae. The total analysis strongly supports the monophyly of the Cebidae family, grouping Aotus, Cebus and Saimiri with the small callitrichines. In the callitrichines, the data link Cebuela to Callithrix, place Callimico as a sister group of Callithrix/Cebuella, and show Saguinus to be the earliest offshoot of the callitrichines. In the family Pithecidae, Callicebus is the basal genus. Finally, combined molecular data showed congruent branching in the atelid clade, setting up Alouatta as the basal lineage and Brachyteles-Lagothrix as a sister group and the most derived branch. Two major points remain to be clarified in the platyrrhine phylogeny: (i) what is the exact branching pattern of Aotus, Cebus, Saimiri and the small callitrichines, and (ii), which two of these three lineages, pitheciines, atelines or cebids, are more closely related?

Divergent evolution and purifying selection of the H (FUT1) gene in New World monkeys (Primates, Platyrrhini)

In the present study, the coding region of the H gene was sequenced and analyzed in fourteen genera of New World primates (Alouatta, Aotus, Ateles, Brachyteles, Cacajao, Callicebus, Callithrix, Cebus, Chiropotes, Lagothrix, Leontopithecus, Pithecia, Saguinus, and Saimiri), in order to investigate the evolution of the gene. The analyses revealed that this coding region contains 1,101 nucleotides, with the exception of Brachyteles, the callitrichines (Callithrix, Leontopithecus, and Saguinus) and one species of Callicebus (moloch), in which one codon was deleted. In the primates studied, the high GC content (63%), the nonrandom distribution of codons and the low evolution rate of the gene (0.513 substitutions/site/MA in the order Primates) suggest the action of a purifying type of selective pressure, confirmed by the Z-test. Our analyses did not identify mutations equivalent to those responsible for the H-deficient phenotypes found in humans, nor any other alteration that might explain the lack of expression of the gene in the erythrocytes of Neotropical monkeys. The phylogenetic trees obtained for the H gene and the distance matrix data suggest the occurrence of divergent evolution in the primates.

Comportamento e dieta de Chiropotes albinasus (I. Geoffroy & Deville, 1848) - cuxiú-de-nariz-vermelho

Os cuxiús-de-nariz-vermelho são primatas neotropicais pouco conhecidos e encontramse na Lista de Espécies Ameaçadas da IUCN na categoria “Ameaçada de Extinção”. Este estudo foi desenvolvido com um grupo desta espécie de primatas na RPPN Cristalino, MT. Foi estudado o orçamento de atividades, uso de espaço e a ecologia alimentar do grupo, através do método de “Varredura Instantânea”. O grupo foi acompanhado durante 6 meses, incluindo 2 meses na estação chuvosa e 4 meses na estação seca. As categorias comportamentais Deslocamento, Alimentação e Parado foram responsáveis por 81,17% dos registros gerais de atividades. Os animais utilizaram com maior intensidade o estrato intermediário da floresta (entre 16 e 20 metros). A dieta do grupo foi preferencialmente frugívora (82,52%), mas também se alimentaram de invertebrados. Cerca de 18 famílias botânicas foram consumidas. Sendo os taxons Arrabidaea sp. e Brosimum latescens os mais comuns. Nos meses de seca houve um maior acréscimo de outros itens alimentares, como flores e invertebrados na dieta dos cuxiús. O tamanho do grupo variou entre 1 e 19 indivíduos ao longo do estudo, assim como a estrutura sexual que também variou bastante. Foi observado o cuidado parental por parte dos machos, além de interações agonísticas interespecíficas entre Ateles marginatus e Sapajus apella.

Efeitos do tipo de floresta e da estrutura de habitat em assembléias de primatas no sudoeste da Amazônia

A heterogeneidade ambiental expressa diferenças naturais entre áreas e é um fator determinante para a riqueza e abundância local de primatas. Neste estudo nós investigamos a composição e estrutura de assembléias de primatas em quatro tipos de floresta: floresta de terra firme, florestas de igapó sazonalmente inundáveis por rios de águas claras (aberta e densa) e cerradão na Reserva Biológica do Guaporé, sudoeste da Amazônia Brasileira. Além disso, avaliamos a associação entre a ocorrência e abundância dos primatas com diferenças estruturais das florestas. Realizamos 617,8 km de censos pelo método de transecção linear (~154 km por tipo de floresta) e avaliamos a estrutura da vegetação em 108 parcelas de 200 m² (0,54 ha por tipo de floresta). Dez espécies de primatas foram registradas durante os 11 meses deste estudo. A floresta de terra firme apresentou o maior número de espécies e a maior densidade de primatas, principalmente devido à presença exclusiva de Callicebus moloch e a maior abundância de Sapajus apella. A elevada densidade de Ateles chamek na floresta aberta inundável foi preponderante para a maior biomassa de primatas neste tipo de floresta. Nas florestas inundáveis e na terra firme, Ateles chamek e Sapajus apella responderam juntas por mais de 70% da biomassa de primatas, e no cerradão apenas Sapajus apella foi responsável por 68% da biomassa. Diferenças entre tipos de floresta na composição específica e abundância relativa de primatas foram associadas com o regime de inundação e com algumas variáveis de estrutura de habitat (densidade de árvores no sub-bosque e no dossel, abertura do dossel, altura total do dossel e densidade de palmeiras e lianas). Nossos resultados reforçam a importância de paisagens heterogêneas na Amazônia, pois estas áreas tendem a contribuir para uma maior diversidade de espécies em uma escala de paisagem.

Caracterização e dinâmica espacial da caça de primatas em comunidades ribeirinhas da Amazônia Central

Os primatas são importante item alimentar para as populações que vivem em locais isolados, e estão entre as espécies mais caçadas por populações tradicionais e indígenas, principalmente nas regiões neotropicais. No entanto, pouco se conhece sobre as características e os padrões espaciais da atividade de caça, e sua abrangência no espaço e no tempo, impedindo uma real avaliação do impacto desta atividade. O objetivo deste trabalho foi descrever, quantificar e analisar a dinâmica espacial da caça de primatas na Amazônia Central, em ambientes de várzea e de terra firme, através de dados de monitoramento de pequenas comunidades ribeirinhas acumulados ao longo de 11 anos. Neste período, o sistema de monitoramento registrou 402 caçadas de primatas, totalizando 541 animais abatidos de nove espécies: Alouatta juara, Aotus cf. vociferans, Ateles chamek, Cacajao ouakary, Callicebus torquatus, Cebus albifrons, Saguinus inustus, Saimiri cassiquiarensis e Sapajus macrocephalus. Destas caçadas, 240 ocorreram em Amanã e 162 em Mamirauá. As distâncias percorridas pelos caçadores a partir das suas comunidades foram significativamente diferentes nos dois ambientes (T= -2,451; gl = 41; p <0,05), os caçadores de terra firme caçam em locais mais distantes que os caçadores de várzea. Quando analisamos o tamanho das áreas utilizadas pelos caçadores, as de terra firme também foram significativamente maiores do que a várzea (F(2,56)=21,471; P<0,01). Embora a contribuição da biomassa de primatas seja pequena, quando comparada a outras espécies, como queixada e paca, o guariba ainda é uma das espécies mais caçadas na Amazônica Central. Para conhecermos o real impacto da atividade de caça entre os primatas, o estudo comprova a necessidade de um monitoramento contínuo das áreas de caça, bem como a análise da sua variação espacial ao longo dos anos.

Goniometric evaluation of both forelimbs and hind limbs in two species of Neotropical monkeys

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Levantamento e censo de primatas em fragmentos florestais de mata atlântica na região de Sousas e Joaquim Egídio, Campinas, SP

A Mata Atlântica, um dos biomas mais ameaçados do mundo, possui alta biodiversidade e endemismos, restando apenas 7% de sua área original, e por isso considerada um hotspot. O município de Campinas está incluído no domínio vegetal de Mata Atlântica com transição para Cerrado, onde restam menos de 3% de floresta estacional semidecidual. A fragmentação de áreas naturais, a caça ilegal e a introdução de espécies exóticas são as principais causas de extinção de espécies. Neste estudo buscou-se identificar a riqueza e a densidade populacional de primatas em dez fragmentos de mata na região da Área de Proteção Ambiental de Sousas e Joaquim Egídio, área de ocorrência do sagüi-do-tufo-preto (Callithrix penicilatta), do macaco-prego (Cebus nigritus) e dos ameaçados, segundo a IUCN (2007), sagüi-da-serra-escuro (Callithrix aurita), sauá (Callicebus nigrifrons) e bugio-ruivo (Alouatta guariba clamitans). Os fragmentos variam entre dois e 24ha com formatos variados e de diferentes composições de capoeiras e matas secundárias, numa matriz agrícola, composta de pastagens, silvicultura e culturas perenes e anuais. O levantamento foi feito entre maio de 2007 e outubro de 2008 através de contagens absolutas dos grupos, diferenciados pelo local dos reavistamentos, composição sexual e etária. Cada avistamento foi georreferenciado com um GPS Garmin Camo Etrex®. Por serem territoriais, sauás foram atraídos através do uso de playbacks. A comunidade de primatas da Mata Ribeirão Cachoeira (245ha), maior remanescente local, é composta por cinco espécies. Sagüi-detufo- preto e bugio foram avistados em seis fragmentos e sauás em dois. Em cinco, foram observados grupos de Callithrix jacchus (sagüi-comum), exóticos na região. Em três fragmentos foram encontrados grupos mistos ou híbridos de Callithrix jacchus e C. penicillata. A área total...(Resumo completo, clicar acesso eletrônico abaixo)

Pesquisa de genomas virais em primatas não humanos do novo mundo por metagenômica

Pós-graduação em Medicina Veterinária - FMVZ

The primate seahorse rhythm

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Bearded capuchin monkeys` and a human`s efficiency at cracking palm nuts with stone tools: field experiments

Wild bearded capuchins, Cebus libidinosus, in Fazenda Boa Vista, Brazil crack tough palm nuts using hammer stones. We analysed the contribution of intrinsic factors (body weight, behaviour), size of the nuts and the anvil surface (flat or pit) to the efficiency of cracking. We provided capuchins with local palm nuts and a single hammer stone at an anvil. From video we scored the capuchins` position and actions with the nut prior to each strike, and outcomes of each strike. The most efficient capuchin opened 15 nuts per 100 strikes (6.6 strikes per nut). The least efficient capuchin that succeeded in opening a nut opened 1.32 nuts per 100 strikes (more than 75 strikes per nut). Body weight and diameter of the nut best predicted whether a capuchin would crack a nut on a given strike. All the capuchins consistently placed nuts into pits. To provide an independent analysis of the effect of placing the nut into a pit, we filmed an adult human cracking nuts on the same anvil using the same stone. The human displaced the nut on proportionally fewer strikes when he placed it into a pit rather than on a flat surface. Thus the capuchins placed the nut in a more effective location on the anvil to crack it. Nut cracking as practised by bearded capuchins is a striking example of a plastic behaviour where costs and benefits vary enormously across individuals, and where efficiency requires years to attain. (C) 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Characterization of Opsin Gene Alleles Affecting Color Vision in a Wild Population of Titi Monkeys (Callicebus brunneus)

The color vision of most platyrrhine primates is determined by alleles at the polymorphic X-linked locus coding for the opsin responsible for the middle- to long-wavelength (M/L) cone photopigment. Females who are heterozygous at the locus have trichromatic vision, whereas homozygous females and all males are dichromatic. This study characterized the opsin alleles in a wild population of the socially monogamous platyrrhine monkey Callicebus brunneus (the brown titi monkey), a primate that an earlier study suggests may possess an unusual number of alleles at this locus and thus may be a subject of special interest in the study of primate color vision. Direct sequencing of regions of the M/L opsin gene using feces-, blood-, and saliva-derived DNA obtained from 14 individuals yielded evidence for the presence of three functionally distinct alleles, corresponding to the most common M/L photopigment variants inferred from a physiological study of cone spectral sensitivity in captive Callicebus. Am. J. Primatol. 73:189-196, 2011. (C) 2010 Wiley-Liss, Inc.

The interface between morphology and action planning: a comparison of two species of New World monkeys

Recent research with several species of nonhuman primates suggests sophisticated motor-planning abilities observed in human adults may be ubiquitous among primates. However, there is considerable variability in the extent to which these abilities are expressed across primate species. In the present experiment, we explore whether the variability in the expression of anticipatory motor-planning abilities may be attributed to cognitive differences (such as tool use abilities) or whether they may be due to the consequences of morphological differences (such as being able to deploy a precision grasp). We compared two species of New World monkeys that differ in their tool use abilities and manual dexterity: squirrel monkeys, Saimiri sciureus (less dexterous with little evidence for tool use) and tufted capuchins, Sapajus apella (more dexterous and known tool users). The monkeys were presented with baited cups in an untrained food extraction task. Consistent with the morphological constraint hypothesis, squirrel monkeys frequently showed second-order motor planning by inverting their grasp when picking up an inverted cup, while capuchins frequently deployed canonical upright grasping postures. Findings suggest that the lack of ability for precision grasping may elicit more consistent second-order motor planning, as the squirrel monkeys (and other species that have shown a high rate of second-order planning) have fewer means of compensating for inefficient initial postures. Thus, the interface between morphology and motor planning likely represents an important factor for understanding both the ontogenetic and phylogenetic origins of sophisticated motor-planning abilities.

The Interface Between Morphology and Action Planning: a Comparison of Two Species of New World Monkeys

Recent research with several species of nonhuman primates suggests sophisticated motor-planning abilities observed in human adults may be ubiquitous among primates. However, there is considerable variability in the extent to which these abilities are expressed across primate species. In the present experiment, we explore whether the variability in the expression of anticipatory motor-planning abilities may be attributed to cognitive differences (such as tool use abilities) or whether they may be due to the consequences of morphological differences (such as being able to deploy a precision grasp). We compared two species of New World monkeys that differ in their tool use abilities and manual dexterity: squirrel monkeys, Saimiri sciureus (less dexterous with little evidence for tool use) and tufted capuchins, Sapajus apella (more dexterous and known tool users). The monkeys were presented with baited cups in an untrained food extraction task. Consistent with the morphological constraint hypothesis, squirrel monkeys frequently showed second-order motor planning by inverting their grasp when picking up an inverted cup, while capuchins frequently deployed canonical upright grasping postures. Findings suggest that the lack of ability for precision grasping may elicit more consistent second-order motor planning, as the squirrel monkeys (and other species that have shown a high rate of second-order planning) have fewer means of compensating for inefficient initial postures. Thus, the interface between morphology and motor planning likely represents an important factor for understanding both the ontogenetic and phylogenetic origins of sophisticated motor-planning abilities. (C) 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

A Mechanical Analysis of Suspensory Locomotion in Primates and Other Mammals

For primates, and other arboreal mammals, adopting suspensory locomotion represents one of the strategies an animal can use to prevent toppling off a thin support during arboreal movement and foraging. While numerous studies have reported the incidence of suspensory locomotion in a broad phylogenetic sample of mammals, little research has explored what mechanical transitions must occur in order for an animal to successfully adopt suspensory locomotion. Additionally, many primate species are capable of adopting a highly specialized form of suspensory locomotion referred to as arm-swinging, but few scenarios have been posited to explain how arm-swinging initially evolved. This study takes a comparative experimental approach to explore the mechanics of below branch quadrupedal locomotion in primates and other mammals to determine whether above and below branch quadrupedal locomotion represent neuromuscular mirrors of each other, and whether the patterns below branch quadrupedal locomotion are similar across taxa. Also, this study explores whether the nature of the flexible coupling between the forelimb and hindlimb observed in primates is a uniquely primate feature, and investigates the possibility that this mechanism could be responsible for the evolution of arm-swinging.

To address these research goals, kinetic, kinematic, and spatiotemporal gait variables were collected from five species of primate (Cebus capucinus, Daubentonia madagascariensis, Lemur catta, Propithecus coquereli, and Varecia variegata) walking quadrupedally above and below branches. Data from these primate species were compared to data collected from three species of non-primate mammals (Choloepus didactylus, Pteropus vampyrus, and Desmodus rotundus) and to three species of arm-swinging primate (Hylobates moloch, Ateles fusciceps, and Pygathrix nemaeus) to determine how varying forms of suspensory locomotion relate to each other and across taxa.

From the data collected in this study it is evident the specialized gait characteristics present during above branch quadrupedal locomotion in primates are not observed when walking below branches. Instead, gait mechanics closely replicate the characteristic walking patterns of non-primate mammals, with the exception that primates demonstrate an altered limb loading pattern during below branch quadrupedal locomotion, in which the forelimb becomes the primary propulsive and weight-bearing limb; a pattern similar to what is observed during arm-swinging. It is likely that below branch quadrupedal locomotion represents a “mechanical release” from the challenges of moving on top of thin arboreal supports. Additionally, it is possible, that arm-swinging could have evolved from an anatomically-generalized arboreal primate that began to forage and locomote below branches. During these suspensory bouts, weight would have been shifted away from the hindlimbs towards forelimbs, and as the frequency of these boats increased the reliance of the forelimb as the sole form of weight support would have also increased. This form of functional decoupling may have released the hindlimbs from their weight-bearing role during suspensory locomotion, and eventually arm-swinging would have replaced below branch quadrupedal locomotion as the primary mode of suspensory locomotion observed in some primate species. This study provides the first experimental evidence supporting the hypothetical link between below branch quadrupedal locomotion and arm-swinging in primates.