Ateles Belzebuth Research Articles

Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity

Seed dispersal by frugivores is thought to play an important role in the maintenance of tropical forest diversity. Spider monkeys (Ateles spp.) are amongst the most frugivorous primates known, and they incorporate a diverse array of fruit species in their diets. In a 1-y study in lowland Ecuador, 670 h of focal observations and data on 916 faecal depositions were collected, and these data are used to describe the seed dispersal patterns of one group of wild spider monkeys (Ateles belzebuth) in terms of both the quantity of seeds dispersed and the primary seed shadows generated. Spider monkeys fed on the fruits of at least 152 plant species and swallowed seeds from more than 98% of these. Collected faecal samples contained seeds from at least 133 different plant species, with an average of 1.9 species (range: 0–7) per defecation. Individual spider monkeys dispersed a minimum of ∼195 000 seeds >1 mm in diameter per year, ∼35 000 of which were >3 mm in diameter. Mean retention time for seeds was 4.5 h. Seed dispersal distances averaged 443 m, but some seeds were moved >1250 m away from parental sources. These results suggest that declines in populations of spider monkeys might have a direct effect on forest dynamics, especially if other disperser species cannot compensate for their lost ecological services.

Evaluating the sustainability of hunting: a comparison of harvest profiles across three Huaorani communities

Yasuni National Park and Biosphere Reserve in Ecuador's Amazon basin is home to the Huaorani and an area of high conservation value. As a result of oil development in the early 1990s, a road was constructed in the northern region of the Park. Three Huaorani communities have since been established in proximity to the road, two of them when the road was built, ten years prior to this study, and the third in a previously uninhabited area. This allowed for a natural experiment comparing harvest compositions across communities of different ages at one point in time. Harvest profiles suggest that the spider monkey Ateles belzebuth is facing local depletion near the two old communities and the howler monkey Alouatta seniculus may also be depleted near one of the old communities. That the two oldest communities still harvested a relatively high number of other vulnerable species is attributed to their use of the road to increase forest access. The spider monkey appears to be the first species to become depleted in persistently hunted areas.

Costs of twins in free-ranging white-bellied spider monkeys (Ateles belzebuth belzebuth) at Tinigua National Park, Colombia

A female spider monkey (Ateles belzebuth belzebuth) that gave birth to twins was studied during 13 months, and her activity budget and diet were compared to those of females with single offspring and females with no offspring to assess selective pressures that could influence litter size. We recorded qualitative information on the development and social interactions of the twins and three other single infants. Emi, the female that had the twins, had the highest proportion of resting time and the lowest proportion of feeding and moving time compared to other adult females and males. Emi also had the lowest average daily travel distance and relied more heavily on flowers and leaves than other group members who included a higher proportion of fruits in their diets. These results suggest that twins are energetically costly to spider monkeys because of the direct energy allocated into raising and carrying the twins and, also, because these costs have direct effects in the ability of a mother to obtain high-quality resources (e.g., fruits). The twins had a slower rate of physical and social development as well as a smaller body size compared to same-aged singletons by the end of the study. Thus, the extended periods of maternal care and the costs associated with rearing and carrying offspring are some of the factors that influence the evolution and maintenance of a litter size of one in most anthropoid primates.

Foraging, Food Choice, and Food Processing by Sympatric Ripe-Fruit Specialists: Lagothrix lagotricha poeppigii and Ateles belzebuth belzebuth

Studies of interspecific competition and niche separation have formed some of the seminal works of ecology. I conducted an 18-mo study comparing the feeding ecologies of 2 sympatric, closely-related ripe-fruit specialists, Humboldt's woolly monkeys (Lagothrix lagotricha poeppigii), and the white-bellied spider monkeys (Ateles belzebuth belzebuth) in Amazonian Ecuador. Woolly monkeys in the terra firme forest live at roughly triple the density of spider monkeys (31 versus 11.5 animals/km2). Woolly monkeys spend 17% of their time foraging, while spider monkeys spend only 1% of their time foraging. Spider monkeys alone fed on soil and termitaria, which are rich in phosphorus. Woolly monkeys are not hard-fruit specialists. Their fruit diet is significantly more diverse than that of spider monkeys. Dietary overlap between the 2 species is high, yet each specializes to some degree on a different set of fruit resources. Woolly monkeys visit more food sources per unit of time, feed lower in the canopy, visit more small food patches, and prey on more seeds. Spider monkeys feed on fewer, richer food sources and are more than twice as likely to return to a particular fruit source than woolly monkeys are. Spider monkeys maximize fruit pulp intake, carrying more intact seeds in their guts, while woolly monkeys minimize seed bulk swallowed through more careful food processing. Surprisingly, several preferred spider monkey foods with high fat content and large seeds are avoided by woolly monkeys. I outline the different ecological dimensions involved in niche separation between the 2 species and discuss the possible impetus for their evolutionary divergence.

コロンビア国マカレナ地域に生息するクモザル（Ateles belzebuth）の一群で短期間に生じた採食とグルーピングの変化

コロンビア国マカレナ地域に生息するクモザル（Ateles belzebuth）の一群で短期間に生じた採食とグルーピングの変化

Phylogenetic inferences of Atelinae (Platyrrhini) based on multi-directional chromosome painting in Brachyteles arachnoides, Ateles paniscus paniscus and Ateles b. marginatus

We performed multi-directional chromosome painting in a comparative cytogenetic study of the three Atelinae species Brachyteles arachnoides, Ateles paniscus paniscus and Ateles belzebuth marginatus, in order to reconstruct phylogenetic relationships within this Platyrrhini subfamily. Comparative chromosome maps between these species were established by multi-color fluorescence in situ hybridization (FISH) employing human, Saguinus oedipus and Lagothrix lagothricha chromosome-specific probes. The three species included in this study and four previously analyzed species from all four Atelinae genera were subjected to a phylogenetic analysis on the basis of a data matrix comprised of 82 discrete chromosome characters. The results confirmed that Atelinae represent a monophyletic clade with a putative ancestral karyotype of 2n = 62 chromosomes. Phylogenetic analysis revealed an evolutionary branching sequence {Alouatta {Brachyteles {Lagothrix and Ateles}}} in Atelinae and {Ateles belzebuth marginatus {Ateles paniscus paniscus {Ateles belzebuth hybridus and Ateles geoffroyi}}} in genus Ateles. The chromosomal data support a re-evaluation of the taxonomic status of Ateles b. hybridus.

Evaluación del estado de conservación de los mamíferos de caza: un modelo comparativo en comunidades de la Reserva Nacional Pacaya Samiria (Loreto, Peru)

El presente trabajo contiene información relacionada a la caza, la abundancia y el impacto de la caza de los mamíferos que habitan los bosques inundables aledaños a dos comunidades asentadas en el interior de la Reserva Nacional Pacaya Samiria. Está basado en registros de caza y censos por transectos. Los registros de caza muestran un promedio de cosecha anual de 190,3 mamíferos del área de San Miguel, equivalente a 2275,9 kg de carne de monte, y 104,5 mamíferos del área de Parinari, equivalente a 985,9 kg de carne de monte. Los primates fueron los más abundantes en ambas áreas de estudio; sin embargo, las densidades estimadas fueron mayores para el área de Parinari. Ninguna especie de ungulados fue observada en el área de San Miguel, mientras que para el área de Parinari la densidad del tapir (Tapirus terrestris Linnaeus) fue estimada en 0,2 individuos/ km2 y para el pecarí labiado (Tayassu pecari Link) en 6,6 individuos/ km2 . Finalmente, el modelo de cosecha sugiere sobrecaza para el tapir, maquisapa cenizo (Ateles belzebuth E. Geoffroy), choro (Lagothrix lagotricha Humboldt) y mono aullador (Alouatta seniculus Linnaeus), cuyas cosechas en algunos casos alcanzaron el 100% de la producción. Se discuten los factores que podrían influir para la escasez y/o ausencia de algunas especies, particularmente ungulados y primates.

Qualitative analysis of constitutive heterochromatin and primate evolution

The results of qualitative heterochromatin analysis in 16 species of primates: Homo sapiens, Pan troglodytes and Gorilla gorilla (F. Hominidae), Hylobates syndactilus (F. Hylobatidae), Macaca fascicularis, M. tibetana, Mandrillus sphinx, M. leucophaeus, Cercopithecus aethiops, C. sabaeus and C. albogularis (F. Cercopithecidae), Cebus apella, Ateles belzebuth hybridus, Aotus azarae, Saimiri sciureus and Lagothrix lagothricha (F. Cebidae) are presented in this work. We characterized heterochromatin using: (a) in situ digestion with restriction enzymes AluI, HaeIII, RsaI and Sau3A, and (b) chromosome staining with DA/DAPI on unbanded chromosomes, on C-banded chromosomes and on sequentially G-C-banded chromosomes. The aim of this work was to relate the qualitative characteristics of constitutive heterochromatin observed with the cytogenetic evolutive processes in the primate group. Results obtained show that (1) in the family Cercopithecidae, Papionini species do not present chromosomal rearrangements when their karyotypes are compared and the heterochromatin characteristics are uniform, while Cercopithecini species show a high number of chromosomal reorganizations, but they have the same heterochromatic characteristics; (2) the Platyrrhini species analysed show variability in their karyological and heterochromatic characteristics; (3) the Hominoidea present two different situations: Pan, Gorilla and Homo with few chromosomal reorganizations among their karyotypes but with a high variability in their heterochromatin characteristics, and Hylobates with low heterochromatin variability and a highly derived karyotype. Speciation processes related to chromosome changes and heterochromatin variations in different groups of primates are discussed. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 107–124.

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.

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

AbstractThe 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.

Seasonal variation in association patterns of wild spider monkeys (Ateles belzebuth belzebuth) at La Macarena, Colombia.

Spider monkeys exhibit a fission-fusion type of social organization. I studied party size and party composition in wild long-haired spider monkeys (Ateles belzebuth belzebuth) in three study periods at La Macarena, Colombia and found that overall party size was larger in the fruit-abundant season. Mean party size in which males were observed was relatively stable across seasons. In contrast, the mean party size of females varied. Females were observed in larger parties in the fruit-abundant season than in the fruit-scarce season. Moreover, whereas males associated with each other at an almost equal frequency across seasons, females associated with each other more frequently in the fruit-abundant season. Females with infants or small juveniles were more often in association with other individuals than were cycling females. The intensity of individual relationships varied according to season, such that even mothers and sons were not always strongly associated. In a large party, females with infants may gain from predation avoidance but they are at a disadvantage in terms of scramble competition. The balance between these factors may change with fruit availability and may influence party size in different periods. For males, party formation may facilitate the defense of resources from neighboring groups more than provide predation avoidance.

Entamoeba histolytica infections in captive primates.

A group based survey on the presence of Entamoeba histolytica and Entamoeba dispar using real-time PCR among 20 species of captive non-human primates was performed after diagnosis of E. histolytica dysentery in a spider monkey ( Ateles belzebuth hybridus). E. histolytica DNA was detected in three species of New World primates and in three species of Old World primates. In five of six E. histolytica isolates, it was possible to amplify the SREHP gene. They all revealed the same pattern after AluI digestion, indicating a common source of infection. E. dispar DNA was detected in two species of New World monkeys and three species of Old World monkeys. The results demonstrate that E. histolytica is capable of causing symptomatic and non-symptomatic infections in Old World and New World non-human primates. To our knowledge, this is the first report of E. histolytica sensu stricto in non-human primates after the redescription separating it from E. dispar in 1993.

Chromosomal homologies between Cebus and Ateles (primates) based on ZOO-FISH and G-banding comparisons.

ZOO-FISH (Fluorescent "in vitro" hybridization) was used to establish the chromosomal homology between humans (HSA) and Cebus nigrivitatus (CNI) and Ateles belzebuth hybridus (ABH). These two species belong to different New World monkey families (Cebidae and Atelidae, respectively) which differ greatly in chromosome number and in chromosome morphology. The molecular results were followed by a detailed banding analysis. The ancestral karyotype of Cebus was then determined by a comparison of in situ hybridization results, as well as chromosomal morphology and banding in other Platyrrhini species. The karyotypes of the four species belonging to the genus Cebus differ from each other by three inversions and one fusion as well as in the location and amounts of heterochromatin. Results obtained by ZOO-FISH in ABH are in general agreement with previous gene-mapping and in situ hybridization data in Ateles, which show that spider monkeys have highly derived genomes. The chromosomal rearrangements detected between HSA and ABH on a band-to-band basis were 27 fusions/fissions, 12 centromeric shifts, and six pericentric inversions. The ancestral karyotype of Cebus was then compared with that of Ateles. The rearrangements detected were 20 fusions/fissions, nine centromeric shifts, and five inversions. Atelidae species are linked by a fragmentation of chromosome 4 into three segments forming an association of 4/15, while Ateles species are linked by 13 derived associations. The results also helped clarify the content of the ancestral platyrrhine karyotype and the mode of chromosomal evolution in these primates. In particular, associations 2/16 and 5/7 should be included in the ancestral karyotype of New World monkeys.

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.

Locomotor behavior of Lagothrix lagothricha and Ateles belzebuth in Yasunı́ 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.

Influence of Fruit Availability on Ecological Overlap among Four Neotropical Primates at Tinigua National Park, Colombia1

ABSTRACTData on fruit abundance and ecological overlap amongAteles belzebuth, Lagothrix lagothricha, Cebus apella, andAlouatta seniculuswere gathered during 13 months at Tinigua National Park (Colombia), in an effort to test the following hypotheses concerning competition for fruits. Coexistence is possible because: (1) during periods when fruit availability is limited, the species utilize different resources; and (2) the species have different fruit preferences independent of fruit production in the forest. Differences were found in resource use (diet and habitat) for all four species. Despite these differences, all four devoted large proportions of time feeding on fruit. Fruit abundance influenced their activity patterns. Ninety percent of all interspecific aggressive interactions (TV = 69) were seen in fruiting trees. The first hypothesis was best supported, given that all species significantly increased their intake of the vegetative parts of plants during periods of fruit scarcity. Fruit partitioning during periods of scarcity was observed clearly only for one pair of species (C. apellaandL. lagothricha).In general, the second hypothesis was not supported as a mechanism for reducing competition because most fruit species were consumed by more than one primate species. Fruit preferences, however, may be particularly important in explaining differences in niche overlap between the most ecologically similar species:A. belzebuthrelied heavily on the fruits of one palm species (Oenocarpus bataud) during periods of fruit scarcity and abundance, whileL. lagothrichacompletely ignored this fruit.

Influence of Fruit Availability on Ecological Overlap among Four Neotropical Primates at Tinigua National Park, Colombia1

Data on fruit abundance and ecological overlap among Ateles belzebuth, Lagothrix lagothricha, Cebus apella, and Alouatta seniculus were gathered during 13 months at Tinigua National Park (Colombia), in an effort to test the following hypotheses concerning competition for fruits. Coexistence is possible because: (1) during periods when fruit availability is limited, the species utilize different resources; and (2) the species have different fruit preferences independent of fruit production in the forest. Differences were found in resource use (diet and habitat) for all four species. Despite these differences, all four devoted large proportions of time feeding on fruit. Fruit abundance influenced their activity patterns. Ninety percent of all interspecific aggressive interactions (N = 69) were seen in fruiting trees. The first hypothesis was best supported, given that all species significantly increased their intake of the vegetative parts of plants during periods of fruit scarcity. Fruit partitioning during periods of scarcity was observed clearly only for one pair of species (C. apella and L. lagothricha). In general, the second hypothesis was not supported as a mechanism for reducing competition because most fruit species were consumed by more than one primate species. Fruit preferences, however, may be particularly important in explaining differences in niche overlap between the most ecologically similar species: A. belzebuth relied heavily on the fruits of one palm species (Oenocarpus bataua) during periods of fruit scarcity and abundance, while L. lagothricha completely ignored this fruit.

Effects of Fruit Patch Availability on Feeding Subgroup Size and Spacing Patterns in Four Primate Species at Tinigua National Park, Colombia

We examined the effects of fruit patch size, density, and distribution on feeding subgroup size and feeding bout duration in four Neotropical primates—Lagothrix lagotricha, Ateles belzebuth, Cebus apella, and Alouatta seniculus—based on 2494 hr of focal animal sampling in Tinigua National Park, Colombia. All four species show positive correlations between patch size (tree diameter at breast height; DBH) and subgroup size (maximum number of individuals from the focal group feeding at the same time), but the determination coefficients are very low and this relationship does not seem to influence strongly the actual size of the groups. Ateles showed the weakest correlation between patch size and feeding party size, and their fission–fusion sociality is best explained as a mechanism to reduce intragroup competition rather than to adjust the subgroup size to the availability of patches. Feeding associations as well as proximal spacing patterns, in general, are more alike in species with similar ecological requirements.

Foraging and ranging patterns in white-bellied spider monkeys.

Ranging and foraging patterns observed during a field study of the behavioral ecology of Ateles belzebuth belzebuth are analysed in the context of temporal and spatial variation in the distribution of plant resources at the study site. The study group exhibited two basic patterns of foraging behaviour and habitat exploitation, which appeared to correlate with the observed variation in resource availability. During the dry season, when the relative abundance of fruit decreased, the spider monkeys ranged over a smaller area, repeatedly visiting a few intensively used fruiting and sleeping trees. As fruit abundance increased during the course of the wet season, the study group expanded its range, and both the daily path length and the number of fruiting trees visited increased daily. These patterns are analysed and evaluated in relation to foraging strategies.

新世界ザルの森林利用

Although some primate species in Africa and Asia are terrestrial, most primates in the world are arboreal and important consumers in tropical forests. In various habitats, several to ten-odd primate species inhabit sympatrically. Comparative studies of forest utilization of a local primate community are important to focus on relationships of arboreal animal community and plants in tropical forests. Ten species of Neotropical primate are confirmed in a study area in northern Bolivia, and two Callitrichidae monkeys, Saguinus fuscicollis and S. labiatus, inhabit sympatrically in the area. The unit group of both sprecies was a family group consisting of two to seven individuals. Home ranges of the family groups of both species were overlapped and the two species frequently made polyspecific associations, but both species preferred. different layers of the forest for traveling and showed different foraging behaviors in the study area. S. fuscicollis tended to utilize the lower layer of the forest, jump from a trunk to a trunk for traveling and forage large-size invertebrates, whereas S. labiatus mainly utilized the middle layer of the forest, jumped from a branch to a branch and foraged small-size invertebrates. Seven species of Cebidae monkeys were distributed in a study area of the Macarena National Park in the upper River Duda Basin in Colombia. Callicebus moloch and Cebus apella usually moved in the lower layer of the forest and used small-size trees for traveling, whereas Alouatta seniculus and Ateles belzebuth tended to use the higher layer of the forest and used large trees for moving support and resting in the area. Differences of height preference in forest utilization, traveling mode and foraging behavior are usually recognized in sympatric monkeys, and small-size species tend to use the lower layer than large ones. Cebidae monkeys inhabit from Argentina to Mexico, but the distribution area of Callitrichidae monkeys is restricted to lower latitude area and the range of genera of the family is bordered by major rivers in the Neotropical area. The author considers that the distribution pattern of both primate families and the differences of forest utilization of a primate community are prescribed by recent species compositions and forest types that were determined by refuge distribution of the tropical humid forest in the last ice age in the Amazon area.