Lagothrix Research Articles

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.

Social Behavior, Reproductive Strategies, and Population Genetic Structure of Lagothrix poeppigii

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.

Contemporary Issues in Ecology, Behavior and Evolution of the Atelin Primates

In the early 1990s, when we were graduate students beginning our respective dissertation projects on atelin primates, the number of studies available to us for background information was limited. Long-term field research on the genera discussed in this issue was restricted to a few sites scattered around Central and South America and it was being carried out by an equally limited number of scientists. If one were interested in spider monkeys (Ateles spp.), Cant, Chapman, Klein, Symington, and van Roosmalen were among the few researchers who had each authored multiple publications on the ecology and behavior of the genus. Even fewer had contributed to the literature on woolly monkeys (Lagothrix spp.)— most notably Defler, Nishimura, Peres, and Soini—while Milton and Strier were the only scientists associated with multiple publications on muriquis (Brachyteles spp.). We are very pleased that in the intervening decade, the number of long-term studies conducted on atelin primates has grown dramatically as a diverse international group of new researchers and established veterans have made substantial contributions to our understanding of

Influence of seed size on dispersal patterns of woolly monkeys (Lagothrix lagothricha) at Tinigua Park, Colombia

Seed size in tropical forests is expected to vary in relation to dispersal mode, recruitment requirements and the nature of seed enemies in each community. Some studies have emphasized an advantage of large‐seeded species in environments subject to low rates of disturbance, but at the same time the number of dispersers tends to decrease as seed size increases. In this paper we describe how seed size affects the probabilities of seed dispersal by woolly monkeys at Tinigua National Park and we compare dispersal patterns among age/sex classes. The results are based on 1236 fecal samples recovered from focal individuals during two years. Woolly monkeys are able to swallow wide seeds; however, there seems to be a limit imposed by anatomical constraints that does not allow them to swallow seeds wider than 18 mm. Most of the seed mass dispersed by the monkeys falls in the categories between 6 and 12 mm wide. Seed selection in terms of mass was not observed for small‐seeded species, but it was observed for some of the medium sized species (without any clear size preference) and there was a clear tendency to swallow relatively small seeds from the large‐seeded species. Although we did not observe a difference in the number of seeds dispersed by deposition among age/sex classes, juveniles disperse a lower seed mass than adult animals. These differences highlight that different age/sex categories play distinct ecological roles in terms of seed dispersal processes. Seed selection by primates might impose selection pressures in seed size traits, but more studies are necessary to ascertain their potential evolutionary role.

Primate Population Densities in Three Nutrient-Poor Amazonian Terra Firme Forests of South-Eastern Colombia

We censused primate populations at three non-hunted ‘terra firme’ forests of south-eastern Colombian Amazonia. The aggregate biomass densities of diurnal primates at all sites were amongst the lowest recorded for any non-hunted forest in western Amazonia and elsewhere in the Neotropics. Densities of red howler monkeys were low, as is typical in Amazonian terra firme forests far removed from white-water rivers, and densities of woolly monkeys were 1.5–3.5 times lower than those estimated for this species in central-western Brazilian Amazonia. Densities of small to mid-sized primates except for brown capuchins (Cebus apella) and white-faced capuchins (Cebus albifrons) were similar to those of other oligotrophic Amazonian forest sites. Our results are in agreement with other studies showing that terra firme forests of lowland Amazonia typically sustain a low biomass density of primates and other mid-sized to large vertebrates. Large reserves are therefore required to assure the viability of primate populations in oligotrophic systems. Given the escalating negative impacts of human habitat disturbance and hunting in Colombian Amazonia, we urge that a baseline sampling protocol to quantify the abundance and distribution of the harvest-sensitive vertebrate fauna be established within protected areas and the large indigenous reserves so that conservation efforts can be defined and implemented.

Chronic infection with hepatitis B viruses and antiviral drug evaluation in uPA mice after liver repopulation with tupaia hepatocytes

Transplantation of primary human hepatocytes and establishment of hepatitis B virus (HBV) infection in immunodeficient urokinase plasminogen activator (uPA) transgenic mice was shown. However, the availability of usable primary human hepatocytes is very limited. Therefore, alternative and more accessible sources of hepatocytes permissive for HBV infection are highly desirable. Here we investigated the potential of primary hepatocytes from the tree shrew Tupaia belangeri that were shown to be susceptible to HBV infection. Freshly isolated or cryopreserved primary tupaia hepatocytes were transplantated via intrasplenic injection into immunodeficient uPA/RAG-2 mice. Engrafted mice were then infected with HBV and woolly monkey (WM)-HBV positive sera. Extensive proliferation of xenografted cells was demonstrated by the stable production of tupaia alpha1-antitrypsin in serum and liver of transplanted mice. Quantitative PCR assays demonstrated the presence of circulating viral particles as well as intracellular viral DNA, including covalently closed circular (ccc) DNA, in transplanted mice. Viral infection could be serially passaged in mice. Furthermore, viral replication was strongly inhibited by treating mice with adefovir dipivoxil. uPA mice repopulated with tupaia hepatocytes represent a useful and more accessible model for HBV infection studies, including the evaluation of antiviral therapy and cccDNA.

Diet and Feeding Ecology of Woolly Monkeys in a Western Amazonian Rain Forest

I investigated the diet and feeding ecology of two social groups of woolly monkeys (Lagothrix lagotricha poeppigii) in Yasuni National Park, Ecuador between April 1995 and March 1996. Woolly monkeys in Yasuni were predominantly frugivorous, with fruits comprising ca. 77% of the yearly diet; the next most common food type in the diet was insect and other animal prey. The fruit diet of woolly monkeys in Yasuni is the most diverse yet recorded for any ateline primate, including spider monkeys (Ateles), which are often regarded as ripe fruit specialists: ≥208 distinct morphospecies of fruits were consumed by woolly monkeys either during the study or during several preceding months of pilot work. Nonetheless, close to one-third of the yearly diet came from just 3 plant genera—Inga,Ficus, and Spondias—and only 20 genera each contributed to ≥1% of the diet. For one study group, the proportion of ripe fruit in the diet each month was correlated with the habitat-wide availability of this resource, a pattern evidenced by several other ateline species. However, the relationship was not apparent in the second study group. The modal party size for feeding bouts on all food types was a single monkey, and, contrary to reports for other atelines, neither feeding party size nor the total number of feeding minutes that groups spent in food patches was well predicted by patch size. Both results highlight the independent nature of woolly monkey foraging. Given that woolly monkeys and closely-related spider monkeys focus so heavily on ripe fruits, their very different patterns of social organization are intriguing and raise the question of just how their ecological strategies differ. Two important differences appear to be in the use of animal prey and in the phytochemical composition of the ripe fruits that they consume: spider monkeys rarely forage for animal prey, and woolly monkeys seldom consume the lipid-rich fruits that are an important part of spider monkey diets.

Microsatellite markers for woolly monkeys (Lagothrix lagotricha) and their amplification in other New World primates (Primates: Platyrrhini)

AbstractSeven polymorphic microsatellite loci were identified for woolly monkeys (Lagothrix lagotricha) from an ‘enriched’ genomic library. For a wild population of 66 animals, these markers averaged over 10 alleles per locus and provided a combined probability for excluding a random individual from parentage of over 98%. These loci were screened in up to 13 other genera of New World monkeys, and many were variable in multiple taxa. Few other platyrrhine‐specific microsatellite markers have been identified; thus, these loci should prove valuable for studying the population genetic structure and mating system not just of Lagothrix but also of other neotropical primates.

Fruit Choice by Woolly Monkeys in Tinigua National Park, Colombia

I combined morphological fruit data, phenological, and demographic information for 128 plant species, with nutritional information for 78 species, to assess feeding preferences of woolly monkeys (Lagothrix lagothricha lugens) in Tinigua National Park, Colombia. I used multiple and simple regression analyses to predict fruit feeding time and one index of fruit preference from 20 independent variables presumed to affect fruit choice. The results of the independent regressions indicated a trend to spend more time consuming good tasting fruits from abundant plants that produce large quantities of fruits and produce large crops. Among these variables, abundant fruit production and the astringency index are the most important variables explaining feeding times when other variables are statistically controlled in a multiple regression analysis. Furthermore, the preference index showed that woolly monkeys prefer fruits from large trees that produce in periods of fruit scarcity, with high pulp/seed ratios, low lipid contents, and clumped spatial distributions. The results suggest that woolly monkeys are primarily generalized, opportunistic frugivores that avoid some fruits with secondary compounds. Their feeding behavior is determined by many factors, but the predictive power of each one is always low ( 69% of the variation in feeding time. I suggest that a detailed quantification of secondary compounds might increase the predictive power of the models to explain fruit choice by frugivorous primates.

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.

An infectious clone of woolly monkey hepatitis B virus.

Members of the Hepadnaviridae family have been isolated from birds, rodents, and primates. A new hepadnavirus isolated from the woolly monkey, a New World primate, is phylogenetically distinct from other primate isolates. An animal model has been established for woolly monkey hepatitis B virus (WMHBV) by using spider monkeys, since woolly monkeys are endangered. In this study, a greater-than-genome length construct was prepared without amplification by using covalently closed circular DNA extracted from the liver of an infected woolly monkey. Transfection of the human liver cell line Huh7 with WMHBV DNA resulted in the production of viral transcripts, DNA replicative intermediates, and secreted virions at levels similar to those obtained with an infectious human HBV clone, demonstrating that the host range restriction of WMHBV is not at the level of genome replication. WMHBV particles from the medium of transfected cultures initiated an infection in a spider monkey similar to that obtained with virions derived from woolly monkey serum. In an attempt to adapt the virus for higher levels of replication in spider monkeys, immunosuppressed and newborn animals were inoculated. Neither procedure produced persistent infections, and the level of viral replication remained several logs lower than that observed in persistently infected woolly monkeys. These data demonstrate the production of an infectious clone for WMHBV and extend the characterization of the spider monkey animal model.

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.

Transcomplementation of core and polymerase functions of the woolly monkey and human hepatitis B viruses

Woolly monkey hepatitis B virus (WMHBV) is a new member of Hepadnaviridae that was isolated from a New World monkey and is phylogenetically distinct from the HBV family. In this study, we explored the functional significance of sequence divergence in the HBV and WMHBV genomes. Independently expressed TP and RT domains of the WMHBV reverse transcriptase (Pol) formed a complex functional for in vitro nucleotide priming, consistent with previous results from priming reactions conducted with HBV. Transcomplementation assays between HBV and WMHBV TP and RT components for in vitro priming demonstrated functional compatibility, although priming with the combination of WMHBV RT and HBV TP was reduced. Examination of cross-species protein-protein interactions revealed that WMHBV core coprecipitated with HBV TP and RT, as well as with WMHBV TP and RT. Analysis in Huh7 cells revealed that WMHBV core and Pol complemented core-negative and Pol-negative HBV mutant genomes for replication. These results highlight the conservation of function despite significant sequence divergence in these viruses.

Ranging behavior and foraging ecology of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Yasuní National Park, Ecuador.

In a year-long study, I investigated the ranging behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a terra firma rainforest in Yasuní National Park, Ecuador, and examined the relationship between ranging, diet, food availability, and food patch use for this population. In Yasuní the total home range sizes for two social groups were 124 and 108 ha, which are much smaller than has been reported previously for Lagothrix elsewhere in its geographic distribution. The mean yearly day range estimates for these same groups were 1,792 m and 1,878 m, which are well within the range of variation previously reported. Ranging behavior was not correlated with the current habitat-wide abundance of ripe fruit, which comprises 76.3% of the yearly diet for this population, but was associated with one measure of likely insect prey abundance and with the availability of immature fruits, a minimal part of the diet. Specifically, one study group moved significantly greater distances during months of high likely insect prey abundance and when immature fruits were abundant. The second study group also traveled farther when likely insect prey abundance was high and when immature fruits were abundant, although the latter relationship only approached significance. This group also devoted significantly more of its daily activity budget to travel during these times. These results indicate that variation in ripe fruit abundance makes no meaningful contribution to explaining variation in ranging behavior for this population of woolly monkeys. Instead, the results raise the possibility that some aspects of the ranging behavior of frugivorous primates may be related to the availability of alternative food sources, such as animal prey, or to monitoring the phenological status of important fruit trees, rather than simply reflecting the degree of intragroup feeding competition.

Reproductive Parameters of Wild Female Lagothrix lagotricha

I describe the reproductive patterns of female woolly monkeys (Lagothrix lagotricha) based on a 12-year study of one group of them at Macarena Ecological Investigations Center, Meta, Colombia. As in other atelin species—muriquis and spider monkeys—characterized by male philopatry, female woolly monkeys leave their natal groups. The age of emigration is ca. 6 years. Females probably begin to copulate with adult males soon after emigration, while their mean age of first parturition is 9 years. They frequently changed groups until they birthed. The average interbirth interval is 36.7 mo (n = 13). All births occurred between July and December (late wet season to early dry season). Copulation occurred throughout the year. However, they copulated more frequently in the estimated conception period from December to May (early dry season to early wet season) than in the birth season. The females had a period of sexual inactivity averaging 7.2 mo until conception. The copulation period and copulation cycle or interval between copulation periods averaged 2.3 and 11.3 days calculated by a conventional method, or 3.1 and 14.7 days by a slightly modified method. The reproductive parameters of woolly monkeys are quite similar to those reported for other atelins in many respects, except the immigration process and age of first copulation.

Primate hepatitis B viruses – genetic diversity, geography and evolution

There are six well characterised genotypes (A-F) of human hepatitis B virus that have distinct geographic ranges which generally relate to chronic HBV infection. A seventh human genotype (G) has recently been described, but there is limited information on ethnic and geographic distribution. Despite the fact that early studies indicated that HBV antigens were present in other primates, the prevailing dogma that HBV was a human disease precluded alternative explanations. Within the past 5 years, hepatitis B viruses have been characterised from all the Old World great apes (orangutan, gibbons, gorillas and chimpanzees) and from a New World woolly monkey. Each group of non-human primates appears to have a distinct strain of hepatitis B virus that can be distinguished from human sequences based upon the nucleotide sequence and selected amino acid changes in the viral proteins. The woolly monkey HBV is most divergent from other primate and human sequences, while the great ape HBV sequences cluster together with separate branches for each group.

THE VOCAL REPERTOIRE OF THE WOOLLY MONKEY LAGOTHRIX LAGOTHRICHA

ABSTRACT A preliminary redefinition of woolly monkey Lagothrix lagothricha basic vocalisation repertoire was made from the analysis of the vocalisations from a captive colony of woolly monkeys. Modern bioacoustic methods were used on a woolly monkey group showing complex and species typical behaviour. Spectrograms, percentages of the occurrence of the basic vocalisation types, and analyses of eolk vocalisations were made. The results show that six basic vocalisation types can be found in this species, and that the eolk type is the most common.

Geographic distribution and abundance of woolly (Lagothrix cana) and spider (Ateles chamek) monkeys in southwestern Brazilian Amazonia.

Two species of frugivorous atelids, Ateles chamek and Lagothrix cana, occur in southwestern Brazilian Amazonia. Populations were surveyed at 36 sites in the state of Rondônia. Ateles chamek is widespread, but the distribution of L. cana is limited by a combination of riverine barriers and ecological factors, possibly including competition with A. chamek. Groups of L. cana were generally larger and more abundant than those of A. chamek, even in syntopy. The transitional forest that predominates in the extreme south of Rondônia (Hylea-cerrado) is not a barrier to either species, with both species being tolerant of habitat disturbance when hunting pressure is low.

A short N-proximal region in the large envelope protein harbors a determinant that contributes to the species specificity of human hepatitis B virus.

Infection by hepatitis B virus (HBV) is mainly restricted to humans. This species specificity is likely determined at the early phase of the viral life cycle. Since the envelope proteins are the first viral factors to interact with the cell, they represent attractive candidates for controlling the HBV host range. To investigate this assumption, we took advantage of the recent discovery of a second virus belonging to the primate Orthohepadnavirus genus, the woolly monkey HBV (WMHBV). A recombinant plasmid was constructed for the expression of all WMHBV envelope proteins. In additional constructs, N-terminal sequences of the WMHBV large envelope protein were substituted for their homologous HBV counterparts. All wild-type and chimeric WMHBV surface proteins were properly synthesized by transfected human hepatoma cells, and they were competent to replace the original HBV proteins for the production of complete viral particles. The resulting pseudotyped virions were evaluated for their infectious capacity on human hepatocytes in primary culture. Virions pseudotyped with wild-type WMHBV envelope proteins showed a significant loss of infectivity. By contrast, infectivity was completely restored when the first 30 residues of the large protein originated from HBV. Analysis of smaller substitutions within this domain limited the most important region to a stretch of only nine amino acids. Reciprocally, replacement of this motif by WMHBV residues in the context of the HBV L protein significantly reduced infectivity of HBV. Hence this short region of the L protein contributes to the host range of HBV.

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.