Proximal Spacing Between Individuals in a Group of Woolly Monkeys (Lagothrix lagotricha) in Tinigua National Park, Colombia

I studied proximal spacing within a group of woolly monkeys (Lagothrix lagotricha) during 7 months at Parque Nacional Tinigua, Colombia. I collected a total of 1188 instantaneous samples on focal individuals, recording the number and age/sex class of individuals that were in contact with, <2 m from, <5 m from the focal animal. The results indicate that proximate spacing reflects social affinities and is related to mother–infant relationship and social grooming. Subadult females and adult males are the sex/age classes with the lowest number of individuals in proximity. There are low proximity between adult females and between adult males and high frequencies of nearness between mother and offspring. Associations between males and females were usually low, but in some cases males showed preferences for a given female. There was a relatively gradual increase in spacing between mothers and their offspring as they became older. Old juvenile males were associated chiefly with other males—mostly subadults—whereas juvenile females maintained some proximity only to their mothers. There are also differences in spacing behavior according to different activity types.     

Chest-rubbing in captive woolly monkeys (Lagothrix lagotricha)

The correlates of chest-rubbing were studied in a captive group of woolly monkeys (Lagothrix lagotricha) to assess possible functions of territorial marking, spacing among competing groups or competing males, reproductive communication, marking to identify familiar environments, selfanointing, and displacement activity. Chest-rubbing was observed only in sexually mature monkeys and was a predominantly male activity. Females increased chest-rubbing when the original adult male died. Chest-rubbing by the first adult male was more common during the two months that he was mating with two females and at times when keepers were likely to be at the exhibit. The results suggest a reproductive function for chest-rubbing in both males and females. There is also support for chest-rubbing as a spacing activity.     

Diet and feeding ecology of gray woolly monkeys (lagothrix lagotricha cana) in Central Amazonia: Comparisons with other Atelines

I studied gray woolly monkeys (Lagothrix lagotricha cana)in an undisturbed central Amazonian terra firme forest, near the headwaters of the Urucu river, Tefé, Amazonas, Brazil (5°50’S, 65°16’W). I report the diet and feeding ecology of a group of 39–41 individuals, based on systematic feeding observations obtained during 11 months. Woolly monkeys are primarily frugivorous; mature fruits and young seeds account for 83 and 7% of 3298 feeding records, respectively. On a seasonal basis, however, they relied heavily on young foliage (16%), seed-pod exudates (6%), and flowers (3%), particularly during the greatest annual period of ripe fruit scarcity, as determined by a phenological survey. Animals represent only 0.1% of their year-round diet, and they spent little time capturing arthropods and other prey items. Although at least 225 plant species, belonging to 116 genera and 48 families, are in their diet, the three top-ranking families (Moraceae, Sapotaceae, and Leguminosae) account for 43% of their food species and 63% of the time they spent feeding on a year-round basis. I compare the feeding ecology and diet of L. 1. canain the Urucu and other taxa of Lagothrixin upper Amazonia — the last large-bodied Neotropical primates to be studied — to those of other ateline genera: Atelesand Brachyteles. An erratum to this article is available at .     

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

Seven 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.     

Bird predation by captive woolly monkeys (Lagothrix lagotricha)

Vertebrate predation has not been reported for woolly monkeys (Lagothrix lagotricha) in their natural habitat. However, bird predation has been observed in captivity. The present report is based on 15 incidents of bird predation that occurred during a 1-year observational study of the nine woolly monkeys at the Louisville Zoo. All identified captures were by females. The captor and her prey were frequently pursued by the other monkeys. Social rank was related to attempts to steal the prey. Consumption was characterized by much chewing and frequent alternation between the prey and highly fiberous substances. Predation was not characterized by stereotypical behaviors for pursuit or killing of prey, but instead suggested opportunistic capture by a generalized organism. The low frequency of bird predation by captive woolly monkeys may indicate that a similar level of predation has gone undetected in the study ofLagothrix in the wild.     

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.     

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.     

Seed dispersal by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia: dispersal distance, germination rates, and dispersal quantity

The purpose of this study was to describe seed dispersal patterns of woolly monkeys (Lagothrix lagothricha) in terms of dispersal quantity and two factors related to dispersal quality: germination rates of dispersed seeds and the distance of dispersal to parental trees. The possible influence of retention time, travel distance, seed size, activity patterns, and fruit abundance on dispersal distance was also analyzed. Observations on activity, diet, daily movements, and seed dispersal were made on focal individuals of a group of woolly monkeys at a tropical rain forest in Tinigua National Park (Colombia). Sixty hours of focal samples per month were completed during 1 year. A total of 753 depositions were collected during the study. Each dropping contained seeds from an average of 2.68 different species (range 0 to 9). Collected depositions contained an underestimated total of 50,168 seeds (>1 mm). Given a population density of 30 individuals/km2, the woolly monkeys in the study area disperse more than 25,000 seeds/km2/day. These seeds belong to 112 different plant species. Germination rates of dispersed seeds are usually similar or higher than those of non-swallowed seeds. It was possible to determine dispersal distance in 264 cases when the focal animal was continuously followed from ingestion at the parental tree to deposition. Only 1% of these depositions landed in close proximity (<15 m) of the parental tree. It was very common that the droppings were deposited between 100 and 500 m from the parent tree, and up to 1.5 km. Higher retention times and longer travel distances were not correlated with increased dispersal distance. Two main reasons for this result were the prolonged and variable passage rates (avg=11.2 hr+/-6.5 SD.) and the circuitous routes of monkeys in this forest.     

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 (<15%). No multiple regression model explained >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.     

Serum chemistry concentrations of captive woolly monkeys (Lagothrix lagotricha)

Woolly monkeys (Lagothrix sp.) are threatened species and numerous zoos have failed to sustain successful populations. The most common causes of death in captive woolly monkeys are related to pregnancy and hypertension. The objective of this retrospective study was to evaluate serum concentrations of a large number of captive woolly monkeys to establish baseline means and compare these concentrations with their closest related species to determine potential abnormalities. Serum analyses from 30 woolly monkeys housed at two institutions (Apenheul, The Netherlands and The Louisville Zoo, KY, USA) over 12 yr were collected. The statistical model included gender, age group (young, 0–4 yr of age; middle, 5–9 yr; and old, 10+ yr), and zoological institution. All panel result means were similar to previously reported concentrations for howler (Alouatta sp.) and spider monkeys (Ateles sp.) with the possible exception of alanine aminotransferase and γ‐glutamyl‐transferase being higher, whereas creatinine and phosphorus were lower. The serum glucose mean of 6.7 mmol/L is above the baseline range for humans and spider monkeys. Alkaline phosphatase (ALP), alanine aminotransferase, and sodium (Na) were higher in females and magnesium (Mg) was higher in males (P<0.05). ALP, Mg, and phosphorus were highest (P<0.05) and calcium and sodium tended to be highest (P<0.10) in the oldest animals. Ferritin tended to be highest (P<0.10) in the oldest animals. Albumin, ALP, chloride, Na, and total bilirubin were higher for Zoo A, whereas γ‐glutamyl‐transferase, glucose, and lactate dehydrogenase were lower for Zoo A (P<0.05). Areas of potential woolly monkey health risk were noted and discussed. Future studies are needed to determine free‐ranging serum concentrations to elucidate parameters that contain aberrant concentrations and decrease health status. Zoo Biol 27:188–199, 2008. © 2008 Wiley‐Liss, Inc.     

The time budget of a group of wild woolly monkeys (Lagothrix lagotricha)

I studied a group of woolly monkeys (Lagothrix lagotricha)for 1800 hr from early 1985 until September 1987 near the lower Apaporis river of the Vaupés Department in the eastern Colombian Amazon. The group had an activity budget of 29.9% rest, 38.8% move, 25.8% forage, and 5.5% other activities during 720 hr of observations evenly spaced throughout this year. The only significant change in these activities during the study period was social activity, which increased as a function of increased food supply. Average diurnal activities of resting and moving are negatively correlated, and each activity show significant changes during the day, while foraging show no significant change. The activity budgets of the adult males and females are not significantly different, but the activities of the juveniles and infants showed much more social activity than the adults. High moving scores may be correlated with the comparative infertility of the soils of the Caparú forest, which require increased effort to maintain the energy levels necessary for maintenance and reproduction in Lagothrix.     

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.     

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.     

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 <23.4 mo after parturition, followed by a period of sexual activity >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.     

Spontaneous hypertension and its sequelae in woolly monkeys (Lagothrix lagotricha)

Arteriolar nephrosclerosis was observed at necropsy in 26 of 38 woolly monkeys (Lagothrix lagotricha). This lesion is the earliest histologic change associated with hypertension in humans. Seventeen of the monkeys had died of congestive heart failure, renal failure or acute cardiovascular accident, complications similar to those seen in human hypertension. All monkeys known to be over 4 years of age were affected. Direct blood pressure measurements in nine otherwise healthy woolly monkeys revealed systolic pressures of 194 +/- 20 mmHg. Our physiologic, clinical and pathologic studies suggest that woolly monkeys develop hypertension spontaneously and could be a useful model for the study of human hypertension.     

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, andAlouatta 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 (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. 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 bataud) during periods of fruit scarcity and abundance, while L. lagothricha completely ignored this fruit.     

The time budget of a group of wild woolly monkeys (Lagothrix lagotricha)

I studied a group of woolly monkeys (Lagothrix lagotricha)for 1800 hr from early 1985 until September 1987 near the lower Apaporis river of the Vaupés Department in the eastern Colombian Amazon. The group had an activity budget of 29.9% rest, 38.8% move, 25.8% forage, and 5.5% other activities during 720 hr of observations evenly spaced throughout this year. The only significant change in these activities during the study period was social activity, which increased as a function of increased food supply. Average diurnal activities of resting and moving are negatively correlated, and each activity show significant changes during the day, while foraging show no significant change. The activity budgets of the adult males and females are not significantly different, but the activities of the juveniles and infants showed much more social activity than the adults. High moving scores may be correlated with the comparative infertility of the soils of the Caparú forest, which require increased effort to maintain the energy levels necessary for maintenance and reproduction in Lagothrix.     

Scent marking in two western Amazonian populations of woolly monkeys (Lagothrix lagotricha)

We describe patterns of scent marking observed in two wild populations of lowland woolly monkeys that were the subjects of long-term studies in the westernmost portion of the Amazon basin. The woolly monkeys engaged primarily in two types of scent marking: chest rubbing and anogenital rubbing. In both study populations, males and females performed both types of scent marking, but males chest-rubbed more commonly than females, while females engaged in more anogenital rubbing. We evaluated two nonexclusive hypotheses for the function of scent marking by woolly monkeys: 1) that scent marking is used in sociosexual contexts, and 2) that scent marking is used to convey information about occupancy of or willingness to defend an area from conspecifics in other social groups. We found no association between the occurrence of scent-marking behavior and location within the home range, but did find that scent marking occurred more commonly than expected on days when copulations, mating solicitations, and intergroup encounters were observed. Additionally, mating activity and chest rubbing were highly correlated across the yearly cycle, even when the potentially confounding variable of ripe fruit availability was controlled for. In woolly monkeys, overt male-male competition is rare and female choice is an important part of the mating system. Our results are most consistent with the idea that scent marking plays a role in advertising male quality or competitive ability, and perhaps in coordinating mating activity.     

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.