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.     

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.     

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.     

Ecological strategies of woolly monkeys (Lagothrix lagotricha) at Tinigua National Park,Colombia

Information on the use of space, activity patterns, diet, and social interactions were recorded for a group of woolly monkeys (Lagothrix lagotricha) during 13 months at Tinigua National Park, Macarena, Colombia. In this region, fruit abundance changes throughout the year with a peak during March–April (beginning of the rainy season) and less fruit during September-November (end of rainy season). Woolly monkeys spent most of their time in mature forest where fruit abundance is higher than in opendegraded or flooded forests. Changes in habitat used by monkeys were coupled with changes in fruit supply across vegetation types. On an annual basis, woolly monkeys spent 24% of point samples locomoting, 36% resting, 36% feeding, and 4% on other activities. However, these proportions varied across the year depending on fruit availability. Based on instantaneous samples, the diet consisted mostly of fruits (60%), arthropods (23%), vegetative parts and flowers (17%), and other items (1%). Non-lactating females and juveniles spent more time eating insects than adult males and lactating females; however, significant differences between classes were detected only during the period of fruit scarcity. These differences are probably due to the high extent to which non-lactating females and juveniles were excluded from fruiting trees by males. The high proportion of arthropods in their diet is unusual for primates with large body size and is a possible factor influencing group cohesiveness in woolly monkeys. © 1994 Wiley-Liss, Inc.     

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.     

Estimation of the retention times and distances of seed dispersed by two monkey species, Alouatta seniculus and Lagothrix lagotricha, in a Colombian forest

Isolated-bout method to estimate the retention times and dispersal distances was applied to the seed dispersal by red howler monkeys (Alouatta seniculus) and Humboldts woolly monkeys (Lagothrix lagotricha) in a lowland tropical forest at La Macarena, on the border of the Macarena and Tinigua National Parks, the Department of Meta, Colombia. Continuous observations were made on the feeding and ranging behavior of well-habituated troops of howler monkeys and woolly monkeys as well as continuous collection of monkeys feces. We selected out the isolated-bout as a feeding bout on the specific species that was only once recorded within 48 h before the seeds of that species appeared in the feces of monkeys. In that case, the seeds were strongly suggested to come from that isolated bout. Then retention times, route seed dispersal distances and direct seed dispersal distances were estimated. Howler monkeys, which are regarded as generalist herbivores, showed longer retention times and dispersal distances along monkeys route than did woolly monkeys, which are specialist frugivores. However, the direct distances that seeds were carried from the mother tree were not significantly greater for howler monkeys than for woolly monkeys. This shows that both retention time and movement patterns by the monkeys, especially the total ranging area, influence the direct distance that seeds are carried from the mother tree.     

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.     

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.     

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 .     

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.     

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.     

Activity and ranging patterns of Colombian woolly monkeys in north-western Amazonia

In this study, I revise three aspects of the socioecology of woolly monkeys (genus Lagothrix) that might give us a better understanding of the patterns found in this species: (1) the association between temporal variation in fruit abundance and diet, activity, and ranging patterns; (2) the individual trade-offs associated with living in small or large groups, and (3) the relationship between social dominance and foraging success. Using behavioral and ecological data collected during 3 years in Tinigua Park, Colombia, I found that woolly monkeys tend to avoid open-degraded forests, where fruit production is generally lower than it is in mature forests. Diet and activity budgets were highly associated with temporal patterns of fruit production. Daily path length was positively correlated with group size and monthly fruit abundance, and negatively correlated with habitat quality. I found differences in activity budgets and the diet preferences of different age/sex classes. For example, adult males rest more and juveniles play more than other classes. Juveniles and adult females without infants look for arthropods more often than adult males and females with young infants, who showed the highest frequencies of fruit feeding. Dominant adult males were not consistently the most efficient foragers on fruits according to two different indexes. Most of these results are consistent with the expectations from strong intra-group competition for resources. However, females with infants received benefits during feeding similar to those of dominant adult males, which may be mediated by differential aggression from males to other group members (juveniles and females without infants).     

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. Am. J. Primatol. 56:57–64, 2002. © 2002 Wiley‐Liss, Inc.     

Ovarian functionality in Poeppig's woolly monkey (Lagothrix poeppigii)

This study examined ovarian features of 60 Poeppig's woolly monkey females in different reproductive stages, collected from wild animals hunted by rural communities in the North-eastern Peruvian Amazon, to provide knowledge on the reproductive physiology of this species. The observed mean ovulation rate was 1.73 follicles, reaching a maximum diameter of 1.0 cm. After ovulation, the matured follicle luteinizes resulting in functional corpora lutea (CL). In case of oocyte fertilization, the “pregnancy” CL grow to a maximum of 2 cm in diameter, and luteal volume decreases related to the advance of pregnancy. Pregnant females have waves of follicular activity until late pregnancy, but dominant follicles do not attain the maximum diameter of pre-ovulatory follicles. Some non-ovulated follicles of 1 mm maximum diameter do not undergo atretic processes and transform to accessory CL by luteinization of the membrane granulosa, resulting in a contribution of up to 7% of the total luteal volume. All pregnant females delivered at term only 1.00 foetus, resulting in a rate of reproductive wastage of 33.3% of embryos.     

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.     

Response to novel housing in two groups of captive tufted capuchin monkeys (Cebus apella)

The influence of age, maternal status, and the presence of a group male on use of space was assessed in two groups of captive tufted capuchin monkeys that underwent a move from indoor housing to a larger outdoor facility. Both groups originally contained two adult males, but only one group retained a male after the move. Following the move, mothers spent less time on the ground when carrying their infants than they did when not carrying their infants. In the group with no male (1) individuals decreased time spent on the ground relative to pre-move levels, whereas no such difference was noted in the group with the male; (2) females spent more time carrying their infants than did females in the group with a male. In the group with the adult male, juveniles spent less time on the ground than did non-mother adult females, whereas no difference had existed prior to the move. Grooming rates dropped from pre-move to post-move, but the mean number of partners with which each animal was in contact increased. Measures of social behavior varied across post-move observation periods inversely to time spent on the ground. These results are consistent with the view that an individual's relative vulnerability influences behavioral conservatism in novel environments, and suggests a relatively profound role for males in promoting exploration of new space in this species.     

Conflict and postconflict behaviour in captive black-and-white snub-nosed monkeys (<Emphasis Type="Italic">Rhinopithecus bieti</Emphasis>)

Black-and-white snub-nosed monkeys (Rhinopithecus bieti) have almost never been the subject of any behavioural observations in captivity. This study was aimed at providing preliminary information about agonistic and reconciliation behaviour in a group kept at the Kunming Institute of Zoology in China. Established procedures were used for this investigation (i.e., the postconflict/matched-control method and the time-rule method). Intra-group aggression rates were quite low. Postconflict affiliation as well as selective attraction of former opponents to each other following conflicts was demonstrated. Former opponents contacted each other earlier in postconflict periods than in matched-control periods. The average conciliatory tendency of all focal individuals combined was 54.5%. After an agonistic interaction, the first affiliative contact between former aggressors usually took place within the first minute. The behaviours most often shown as first affiliations after a conflict were body contact, mount, touch, and hold-lumbar, of which the latter is an explicit reconciliatory gesture. Furthermore, the adult male intervened non-aggressively in 84% of all conflicts (n=25) among the adult females. Overall, the patterns of aggression and reconciliation observed in R. bieti bear many of the traits that characterise tolerant primate species.