Color vision and niche partitioning in a diverse neotropical primate community in lowland Amazonian Ecuador

A recent focus in community ecology has been on how within‐species variability shapes interspecific niche partitioning. Primate color vision offers a rich system in which to explore this issue. Most neotropical primates exhibit intraspecific variation in color vision due to allelic variation at the middle‐to‐long‐wavelength opsin gene on the X chromosome. Studies of opsin polymorphisms have typically sampled primates from different sites, limiting the ability to relate this genetic diversity to niche partitioning. We surveyed genetic variation in color vision of five primate species, belonging to all three families of the primate infraorder Platyrrhini, found in the Yasuní Biosphere Reserve in Ecuador. The frugivorous spider monkeys and woolly monkeys (Ateles belzebuth and Lagothrix lagotricha poeppigii, family Atelidae) each had two opsin alleles, and more than 75% of individuals carried the longest‐wavelength (553–556 nm) allele. Among the other species, Saimiri sciureus macrodon (family Cebidae) and Pithecia aequatorialis (family Pitheciidae) had three alleles, while Plecturocebus discolor (family Pitheciidae) had four alleles—the largest number yet identified in a wild population of titi monkeys. For all three non‐atelid species, the middle‐wavelength (545 nm) allele was the most common. Overall, we identified genetic evidence of fourteen different visual phenotypes—seven types of dichromats and seven trichromats—among the five sympatric taxa. The differences we found suggest that interspecific competition among primates may influence intraspecific frequencies of opsin alleles. The diversity we describe invites detailed study of foraging behavior of different vision phenotypes to learn how they may contribute to niche partitioning.     

Distribution,population density and conservation of the critically endangered brown spider monkey (<Emphasis Type="Italic">Ateles hybridus</Emphasis>) and other primates of the inter-Andean forests of Colombia

The inter-Andean tropical rainforests and dry forests of the Magdalena river basin (Tumbes-Choco-Magdalena biodiversity hotspot) in northern Colombia have undergone significant forest loss and degradation in recent decades. Six primate species inhabit this region, five of which are currently threatened with extinction and one of which—the brown spider monkey, Ateles hybridus—is considered critically endangered. Accurate and recent information on the distribution and conservation status of these threatened primate populations is scarce or nonexistent, even though such data are needed to implement successful conservation actions and management plans. Between 2006 and 2016, we evaluated the status and distribution of primates across inter-Andean lowland forests in northern Colombia. We visited 30 sites to evaluate the presence/absence of brown spider monkeys and other primate taxa in the region. We also carried out surveys at 10 of these sites to obtain estimates of primate population densities and demographic information from forests with different levels of anthropogenic disturbance. Novel data on primate presence/absence were obtained for 27 sites, and 136 records were collected in total. Only 33% of the sites visited were large forest fragments (>?500 Ha). This study confirms that at least six primate species are still present in the Rio Magdalena region, which represents the highest platyrrhine diversity west of the Andes. This study also confirms the persistence of a wild population of Colombian woolly monkeys (Lagothrix lagotricha lugens) in the Serranía de San Lucas. Assigning formal protected status to this region is an urgent priority for the conservation of primates in the Rio Magdalena region.     

Use of Mineral Licks by White-Bellied Spider Monkeys (<Emphasis Type="BoldItalic">Ateles belzebuth</Emphasis>) and Red Howler Monkeys (<Emphasis Type="BoldItalic">Alouatta seniculus</Emphasis>) in Eastern Ecuador

Geophagy occurs in all primate groups and is particularly common in species that consume greater quantities of plant material, i.e., leaves, fruit. The function of geophagy is not fully understood and likely varies over space and time, perhaps in connection with changes in diet. Central to a better understanding of geophagy in primate ecology is knowledge of the occurrence of such behavior among different species and seasons. We used camera traps triggered by heat and motion to document the use of mineral licks by primates over a 3-yr period at a lowland forest site in eastern Ecuador (Tiputini Biodiversity Station). Such mineral licks can be important sources of minerals, nutrients, and other compounds for a wide range of species in Amazonian forests. Although 10 species of primates are known from the study site, we obtained photographs of only 2 species, Ateles belzebuth (white-bellied spider monkey) and Alouatta seniculus (red howler) at 2 of 4 saladeros surveyed. From late December 2004 through early January 2008, we recorded 192 photographs with a total of 318 Ateles belzebuth representing ≥66 separate visits. Comparable numbers for Alouatta seniculus were 80, 121, and 37. We recorded both species visiting a mineral lick at the same time on ≥7 occasions. Use of mineral licks varied across months; we recorded more visits from November through February, the drier period at Tiputini. Visits also varied by hour, with no visits before 0830 or after 1630; Ateles belzebuth showed a stronger mid-day peak in visits. Average visit length (calculated as the time between the first and last photographs of a given visit) was similar between the 2 species but median visit length was more than twice as long for Ateles belzebuth (15 min) as for Alouatta seniculus (6 min). Results indicate that mineral licks are important in the ecology of these species, but further studies are needed to determine the precise benefit(s) obtained and how benefits may vary with diet and other factors.     

Reproductive seasonality in two sympatric primates (Ateles belzebuth and Lagothrix lagotricha poeppigii) from Amazonian Ecuador

With their large body size and “slow” life histories, atelin primates are thought to follow a risk‐averse breeding strategy, similar to capital breeders, in which they accumulate energy reserves in anticipation of future reproductive events such as gestation and lactation. However, given the paucity of longitudinal data from wild populations, few studies to date have been able to compare the timing of reproductive events (e.g., copulations, conceptions, and births) in relation to shifting resource availability over multiple years. We examined the reproductive patterns of two atelin species—white‐bellied spider monkeys (Ateles belzebuth) and lowland woolly monkeys (Lagothrix lagotricha poeppigii)—in relation to habitat‐wide estimates of fruit availability at the Tiputini Biodiversity Station (TBS) in Amazonian Ecuador. Our sample included 4 years of data on births (N = 36) and copulations (N = 170) for Lagothrix, 10 years of data on births (N = 35) and copulations (N = 74) for Ateles, and 7 years of data on ripe fruit availability. Reproductive events were distinctly seasonal. For both species, births were concentrated between May and September, a time period in which ripe fruit was relatively scarce, while inferred conceptions occurred between September and January, when ripe fruit availability was increasing and maintained at high‐levels throughout the forest. Interannual variation in births was relatively stable, except for in 2016 when twice as many infants were born following a strong El Niño event that may have led to unusually high levels of fruit productivity during the 2015 breeding season. Although copulations were observed year‐round, an overwhelming majority (>90% for Lagothrix and >80% for Ateles) took place between August and February when females were most likely to conceive. Collectively, these data follow the reproductive patterns observed in other atelin primates, and, as proposed by others, suggest that atelins may follow a risk‐averse breeding strategy.     

Evolutionary renovation of L/M opsin polymorphism confers a fruit discrimination advantage to ateline New World monkeys

New World monkeys exhibit prominent colour vision variation due to allelic polymorphism of the long‐to‐middle wavelength (L/M) opsin gene. The known spectral variation of L/M opsins in primates is broadly determined by amino acid composition at three sites: 180, 277 and 285 (the ‘three‐sites’ rule). However, two L/M opsin alleles found in the black‐handed spider monkeys (Ateles geoffroyi) are known exceptions, presumably due to novel mutations. The spectral separation of the two L/M photopigments is 1.5 times greater than expected based on the ‘three‐sites’ rule. Yet the consequence of this for the visual ecology of the species is unknown, as is the evolutionary mechanism by which spectral shift was achieved. In this study, we first examine L/M opsins of two other Atelinae species, the long‐haired spider monkeys (A. belzebuth) and the common woolly monkeys (Lagothrix lagotricha). By a series of site‐directed mutagenesis, we show that a mutation Y213D (tyrosine to aspartic acid at site 213) in the ancestral opsin of the two alleles enabled N294K, which occurred in one allele of the ateline ancestor and increased the spectral separation between the two alleles. Second, by modelling the chromaticity of dietary fruits and background leaves in a natural habitat of spider monkeys, we demonstrate that chromatic discrimination of fruit from leaves is significantly enhanced by these mutations. This evolutionary renovation of L/M opsin polymorphism in atelines illustrates a previously unappreciated dynamism of opsin genes in shaping primate colour vision.     

Locomotion and posture in Lagothrix lagotricha

This long-term study of woolly monkey (Lagothrix) locomotor and postural behaviour employs methods identical to those used during a previous study of the locomotion and posture of two species of Ateles, allowing a detailed comparison between the two genera, which are strong competitors in extensive parts of the Amazon basin and northern Andes. As in Ateles, Lagothrix locomotion can be divided into five patterns, based on limb usage: quadrupedal walking and running, suspensory locomotion, climbing, bipedalism (very rare in wild woolly monkeys) and leaping. Lagothrix differs from Ateles primarily in its greater reliance on quadrupedal locomotion during both travel and feeding and on its de-emphasis of the use of suspensory locomotion as compared to Ateles, while the use of climbing and leaping is roughly equal in the two genera. Lagothrix exhibits more generalised (primitive) locomotive behaviour in accordance with its morphology, in comparison to the more specialised Ateles. The generic differences reflect differences in habitat use and particularly foraging ecology.     

Effects of Seed Dispersal by Three Ateline Monkey Species on Seed Germination at Tinigua National Park, Colombia

We examined the effect of seed ingestion by three ateline primates: woolly monkeys, Lagothrix lagothricha; spider monkeys, Ateles belzebuth; and, red howler, Alouatta seniculus on germination rates and latency periods of seeds of several plant species in Tinigua National Park, Colombia. We collected dispersed seeds from feces and control seeds from the parental trees and washed them for germination trials. For the majority of plants, dispersed seeds germinated as well or better than control seeds did. Although spider monkeys depend more heavily on fruits than the other monkey species do, they were not more efficient than howlers or woolly monkeys at improving germination rates. A considerable proportion of the seeds dispersed by howlers and woolly monkeys showed reduced latency periods to germination, but spider monkeys showed less effect on reducing germination time. This result may be related to longer gut retention times, but such a trend has not been observed in other primate species. We conclude that, like many other primates, ateline monkeys are effective seed dispersers in terms of their effects on the seeds they swallow because they rarely decrease their germination rates. We discuss problems that make interspecific comparisons difficult, such as inappropriate control seeds and differences associated with germination substrates, and we stress the importance of studying other components of seed dispersal effectiveness.     

Bimodal evolution of the killer cell Ig-like receptor (KIR) family in New World primates

The immunoglobulin-like receptor (KIR) gene family in New World primates (Platyrrhini) has been characterized only in the owl monkey (Aotus sp.). To gain a better understanding of the KIR system in Platyrrhini, we analyzed a KIR haplotype in Ateles geoffroyi, and sequenced KIR complementary DNAs (cDNAs) from other three Atelidae species, Ateles hybridus, Ateles belzebuth, and Lagothrix lagotricha. Atelidae expressed a variable set of activating and inhibitory KIRs that diversified independently from their Catarrhini counterparts. They had a unique mechanism to generate activating receptors from inhibitory ones, involving a single nucleotide deletion in exon 7 and a change in the donor splice site of intron 7. The A. geoffroyi haplotype contained at least six gene models including a pseudogene, two coding inhibitory receptors, and three coding activating receptors. The centromeric region was in a tail-to-tail orientation with respect to the telomeric region. The owl monkey KIR haplotype shared this organization, and in phylogenetic trees, the centromeric genes clustered together with those of A. geoffroyi, whereas their telomeric genes clustered independently. KIR cDNAs from the other Atelidae species conformed to this pattern. Signatures of positive selection were found in residues predicted to interact with the major histocompatibility complex. Such signatures, however, primarily explained variability between paralogous genes but not between alleles in a locus. Atelidae, therefore, has expanded the KIR family in a bimodal fashion, where an inverted centromeric region has remained relatively conserved and the telomeric region has diversified by a rapid process of gene duplication and divergence, likely favored by positive selection for ligand binding.     

Phylogenetic Relationships of Spider Monkeys (Ateles) Based on Mitochondrial DNA Variation

Our goal was to determine phylogenetic relationships among geographically and taxonomically distinct haplotypes of spider monkeys (Ateles) based on DNA sequence variation for the mitochondrial DNA control region and cytochrome c oxidase subunit II gene. We obtained samples from most previously recognized subspecies of Ateles, ranging from Central America throughout the Amazon Basin, to determine phylogenetic relationships among racially recognized groups. Comparison of DNA sequences using both parsimony analysis and genetic distance analysis produced phylogenetic relationships that were very similar for each genetic region. We analyzed the phylograms produced, along with associated bootstrap support, confidence probabilities, and genetic distances between taxonomic groups, to identify four monophyletic species of Ateles: Ateles paniscus, composed of haplotypes from the northeastern Amazon Basin; A. belzebuth in the southern Amazon Basin; A. hybridus, located primarily along the Magdalena River valley of Colombia; and A. geoffroyi, which includes two former species: A. geoffroyi and A. fusciceps. This arrangement is contradictory to long-held taxonomies of Ateles based on pelage variation and is similar to a recent analysis based on craniodental variation. Results of this investigation suggest patterns of gene flow, evolutionary relationships, and speciation patterns that are more plausible than previous pelage-based taxonomies, which required seemingly impossible patterns of gene flow. Conservation efforts aimed at protecting Ateles, one of the Neotropics most endangered genera, will also benefit from the findings presented in this paper.     

Abundance, diversity, and patterns of distribution of primates on the Tapiche River in Amazonian Peru

This work presents data on the relative diversity, abundance, and distribution patterns of primates in a 20 km2 area of the Tapiche River in the Peruvian Amazon. Population data were collected while the study area was both inundated and dry (March to September 1997) using conventional line-transect census techniques. Survey results reflected the presence of 11 primate species, but population parameters on only eight of the species will be presented, including saddleback tamarins (Saguinus fuscicollis), Bolivian squirrel monkeys (Saimiri boliviensis), brown capuchins (Cebus apella), white-fronted capuchins (Cebus albifrons), monk sakis (Pithecia monachus), red titi monkeys (Callicebus cupreus), red uakaris (Cacajao calvus), and red howler monkeys (Alouatta seniculus). Woolly monkeys (Lagothrix lagotricha), night monkeys (Aotus nancymaae), and pygmy marmosets (Callithrix pygmaea) were also seen in the area. The data for the smaller-bodied primates is similar to that reported almost 18 years earlier, but the data for the larger-bodied primates reflect a loss in the number of animals present in the area. Pressure from hunters and the timber industry may account for declining numbers of large-bodied primates, while it appears that natural features peculiar to the conservation area contribute to the patchy pattern of distribution.     

Footfall patterns, stride length and speed of vertical climbing in spider monkeys (Ateles fusciceps robustus) and woolly monkeys (Lagothrix lagotricha)

Vertical climbing is central to theories surrounding the locomotor specialisations of large primates. In this paper, we present spatiotemporal gait parameters obtained from video recordings of captive spider monkeys (Ateles fusciceps robustus) and woolly monkeys (Lagothrix lagotricha) in semi-natural enclosures, with the aim of discovering the influence of body weight and differences in general locomotor behaviour on vertical climbing kinematics on various substrates. Results show that there are only few differences between gait parameters of climbing on thin trees, vertical and oblique ropes, while climbing on large-diameter trees differs considerably, reflecting the higher costs of locomotion on the latter. At the same speed, Ateles takes longer strides and the support phase takes a smaller percentage of cycle duration than in Lagothrix. Footfall patterns are more diverse in Ateles and include a higher proportion of ipsilateral limb coupling. Compared to other primates, the gait characteristics of vertical climbing of atelines most closely resemble those of African apes.     

The mitochondrial control region of the black howler monkey,Alouatta caraya (Primates,Platyrrhini), and the development of new primers

The analysis of polymorphic genetic markers is necessary to assess the genetic variability of natural populations in order to develop effective conservation strategies. However, the molecular genetic variability of most neotropical primates is not well known. Therefore, we describe 13 primers for the amplification and sequencing of the mitochondrial control region that were developed for Alouatta caraya. Six of these primers gave unique bands on four other platyrrhine species (Alouatta palliata, Ateles paniscus, Ateles belzebuth and Saimiri boliviensis) showing their utility for control region amplification and sequencing in these platyrrhine species.     

The natural place to begin: The ethnoprimatology of the Waorani

Ethnoprimatology is an important and growing discipline, studying the diverse relationships between humans and primates. However there is a danger that too great a focus on primates as important to humans may obscure the importance of other animal groups to local people. The Waorani of Amazonian Ecuador were described by Sponsel [Sponsel (1997) New World Primates: Ecology, evolution and behavior. New York: Aldine de Gruyter. p 143–165] as the “natural place” for ethnoprimatology, because of their close relationship to primates, including primates forming a substantial part of their diet. Therefore they are an ideal group in which to examine contemporary perceptions of primates in comparison to other types of animal. We examine how Waorani living in Yasuní National Park name and categorize primates and other common mammals. Although there is some evidence that the Waorani consider primates a unique group, the non‐primate kinkajou and olingo are also included as part of the group “monkeys,” and no evidence was found that primates were more important than other mammals to Waorani culture. Instead, a small number of key species, in particular the woolly monkey (Lagothrix poeppigii) and white‐lipped peccary (Tayassu pecari), were found to be both important in the diet and highly culturally salient. These results have implications for both ethnoprimatologists and those working with local communities towards broader conservation goals. Firstly, researchers should ensure that they and local communities are referring to the same animals when they use broad terms such as “monkey,” and secondly the results caution ethnoprimatologists against imposing western taxonomic groups on indigenous peoples, rather than allowing them to define themselves which species are important. Am. J. Primatol. 75:1117–1128, 2013. © 2013 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.     

Locomotor behavior of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park, Ecuador: general patterns and nonsuspensory modes.

Field study of the locomotor behavior of sympatric woolly monkeys (Lagothrix lagothricha) and spider monkeys (Ateles belzebuth) in undisturbed rainforest of northern Ecuador revealed similar patterns in use of plant forms (categorized tree and liana structure), and substantial differences in the frequencies of use of different grouped modes (aggregates of kinematically similar specific modes). Lagothrix progressed more than Ateles by leaping/dropping and quadrupedal walking/running, whereas Ateles exhibited more suspensory locomotion. Grouped modes are associated with different plant forms in similar ways in the two species. In contrast, the species differed in use of tree zone (trunk/bole, major branches, intermediate branches, and terminal branches), with Lagothrix using intermediate branches and Ateles terminal branches more. Correlated with this difference was greater use by Lagothrix of quadrupedal movement, especially on intermediate branches, and greater use of suspensory modes by Ateles, especially in the terminal zone. Further research is needed to determine how these patterns are facilitated and constrained by morphological mechanisms. Analysis of specific locomotor modes within groups shows several interspecific differences in relative frequencies.     

Time Allocation Patterns of Lowland Woolly Monkeys (Lagothrix lagotricha poeppigii) in a Neotropical Terra Firma Forest

We investigated the time allocation decisions of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a terra firma forest in eastern Ecuador where they occur sympatrically with 9 other primate species. Woolly monkeys spent considerable amounts of time searching for and attempting to procure animal prey—roughly as much time as they spent consuming plant material: ripe fruits, leaves, and flowers. The amount of time spent foraging for animal prey is positively related to the habitat-wide availability of ripe fruits (the predominant component of the woolly monkey diet), and negatively related to both ambient temperature and the abundance of potential prey items in the habitat. Time spent resting showed exactly the opposite pattern with respect to these ecological variables. These results suggest that woolly monkeys follow an energy-maximizing strategy of food acquisition during times of fruit abundance—focusing on animal foods and perhaps laying down fat reserves to utilize when ecological conditions worsen—and follow an energy-minimizing strategy when fruit resources are scarce. Such a strong and seasonal commitment to animal prey foraging is unique among the ateline primates and is not ubiquitous even among lowland woolly monkeys. We suggest that this foraging strategy, and the greater intragroup cohesion that characterizes some populations of Lagothrix, are both opportunistic responses to regional differences in habitat quality. Identifying and accounting for such intraspecific variation should be a goal of any analysis of comparative socioecology.     

Development and annotation of shotgun sequence libraries from New World monkeys

The draft genome sequences of several primates are available, providing insights into evolutionary and anthropological research. However, genomic resources from New World monkeys are conspicuously lacking. To date, the genomes of only two platyrrhine species, the common marmoset and the Bolivian squirrel monkey, have been fully sequenced. This is especially limiting for comparative genomics research, considering that New World monkeys are the most speciose primate group, and platyrrhine genetic diversity is comparable to that of the catarrhines (i.e. apes and Old World monkeys). Here, we present the generation and annotation of numerous sequence reads from the genomes of Spider monkey (Ateles belzebuth), Owl monkey (Aotus lemurinus) and Uakari (Cacajao calvus), representing the three platyrrhine families, Atelidae, Cebidae and Pitheciidae, respectively. These sequencing reads were developed from gDNA shotgun libraries containing over 3000 individual sequences with an average length of 726 bps. Of these sequences, 1220 contain <20% repeats, and thus are potentially highly useful phylogenetic markers for other platyrrhine species. Among them, a large number of sequencing reads were found to match unique regions within the human (2462 sequences) and the marmoset (2829 sequences) genomes. In particular, the majority of these sequencing reads are from putatively neutrally evolving intergenic regions. Thus, they are likely to be highly informative for inferring neutral evolutionary patterns and genomic evolution for other New World monkeys.     

Comparative and functional myology of the prehensile tail in new world monkeys

The caudal myology of prehensile-tailed monkeys (Cebus apella, Alouatta palliata, Alouatta seniculus, Lagothrix lagotricha, and Ateles paniscus) and nonprehensile-tailed primates (Eulemur fulvus, Aotus trivirgatus, Callithrix jacchus, Pithecia pithecia, Saimiri sciureus, Macaca fascicularis, and Cercopithecus aethiops) was examined and compared in order to identify muscular differences that correlate with osteological features diagnostic of tail prehensility. In addition, electrophysiological stimulation was carried out on different segments of the intertransversarii caudae muscle of an adult spider monkey (Ateles geoffroyi) to assess their action on the prehensile tail. Several important muscular differences characterize the prehensile tail of New World monkeys compared to the nonprehensile tail of other primates. In atelines and Cebus, the mass of extensor caudae lateralis and flexor caudae longus muscles is more uniform along the tail, and their long tendons cross a small number of vertebrae before insertion. Also, prehensile-tailed monkeys, especially atelines, are characterized by well-developed flexor and intertransversarii caudae muscles compared to nonprehensile-tailed primates. Finally, Ateles possesses a bulkier abductor caudae medialis and a more cranial origin for the first segment of intertransversarii caudae than do other prehensile-tailed platyrrhines. These myological differences between nonprehensile-tailed and prehensile-tailed primates, and among prehensile-tailed monkeys, agree with published osteological and behavioral data. Caudal myological similarities and differences found in Cebus and atelines, combined with tail-use data from the literature, support the hypothesis that prehensile tails evolved in parallel in Cebus and atelines. © 1995 Wiley-Liss, Inc.     

Immunodiffusion systematics of the primates. Part V. The Platyrrhini.

Evolutionary relationships between New World monkeys and marmoset genera and the place of the Ceboidea within the primates are considered in terms of the immunological specificity of ceboid proteins. Antigenic distances between the New World primates are measured using antisera produced in rabbits to nine ceboid genera: Alouatta, Aotes, Ateles, Callicebus, Cebus, Chiropotes, Lagothrix, Saimiri and Saguinus. A cladogram constructed on the basis of increasing degrees of antigenic distance between branches depicts Ceboidea as a monophyletic assemblage within which Alouatta is grouped with the Atelinae genera, Lagothrix and Ateles, Chiropotes joins Cacajao and Cebus joins Saimiri. The joining of the cebid genera Aotes and Callicebus with callithricid genera Callimico and Saguinus into a single complex lineage suggests that Cebidae is a paraphyletic or polyphyletic taxon. A phylogenetic taxonomy for Platyrrhini is proposed.     

Social Behavior,Reproductive Strategies,and Population Genetic Structure of <Emphasis Type="Italic">Lagothrix poeppigii</Emphasis>

For species of primates in which females emigrate, we would expect males within groups to be related to one another. Kin selection theory suggests that these males should associate preferentially with one another, be more affiliative and cooperative with one another than females are, and compete less overtly with one another over reproductive opportunities than males in female philopatric taxa do. Precisely these patterns of social behavior characterize well-studied populations of 2 of the 3 atelin primate genera: spider monkeys (Ateles) and muriquis (Brachyteles). For the third atelin genus, Lagothrix, patterns of intragroup social behavior have been less well-documented. We studied the social and reproductive behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Ecuador during a one-year observational study and subsequently used molecular techniques to investigate population genetic structure and dispersal patterns for this taxon. Among adult male woolly monkeys, both affiliative and agonistic interactions were rare, and males were seldom in close proximity to one another. Relationships among male woolly monkeys are best characterized as tolerant, especially in the context of mating wherein direct competition among males was minimal despite the fact that females mated with multiple males. Relationships among females were likewise generally tolerant but nonaffiliative, though females often directed harassment towards copulating pairs. Affiliative interactions that did occur among woolly monkeys tended to be directed either between the sexes—primarily from female to male—or from younger towards older males, and the proximity partners of females tended to be members of the opposite sex. These results suggest that bonds between the sexes may be more important than same-sex social relationships and that direct female-female competition is an important feature of woolly monkey reproductive biology. Our genetic results indicate that, as in other atelins, dispersal by females is common, but some male dispersal likely occurs as well. In some but not all groups we studied, nonjuvenile males within social groups were more closely related to one another on average than females were, which is consistent with greater male than female philopatry. However, differences in these patterns among our study groups may reflect local variation in dispersal behavior.     

Suspensory locomotion of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park,Ecuador

A comparative field study of the locomotion of woolly monkeys (Lagothrix lagothricha) and spider monkeys (Ateles belzebuth) in undisturbed rainforest of northeastern Ecuador reveals substantial differences in their use of suspensory modes. Ateles performed both more brachiation (by forelimbs and tail, with trunk rotation), and forelimb swing (similar to brachiation, but without trunk rotation) than Lagothrix. In contrast, in Lagothrix 20% of suspensory movement was by pronograde forelimb swing, which resembles forelimb swing except that the body is held in a pronograde orientation due to the tail and/or feet intermittently grasping behind the trailing forelimb. Ateles never exhibited this mode. Both brachiation and forelimb swing by Ateles were more dynamic than in Lagothrix, consisting of higher proportions of full-stride bouts (versus single-step). Both species used smaller supports for suspensory than for quadrupedal locomotion, and Ateles used both smaller and larger supports for suspension than did Lagothrix. Analysis of support inclination shows that both species tended to perform more above-support movement on horizontal supports and more below-support (suspensory) movement from oblique supports. Our attempt to elucidate the aspects of canopy structure that favor suspension suggests the need for additional kinds of observational data, focusing on the "immediate structural context" of positional events.