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 Yasuní National Park, Ecuador between April 1995 and March 1996. Woolly monkeys in Yasuní 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 Yasuní 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.     

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.     

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 .     

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.     

Foraging,Food Choice,and Food Processing by Sympatric Ripe-Fruit Specialists: <Emphasis Type="Italic">Lagothrix lagotricha poeppigii</Emphasis> and <Emphasis Type="Italic">Ateles belzebuth belzebuth</Emphasis>

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.     

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.     

Associative behavior ofCacajao calvus ucayalii with other primate species in amazonia Peru

Red uakari (Cacajao calvus ucayalii) living near the Communal Reserve Tamshiyacu-Tahuayo in northeastern Peru frequently associate with other species of primate, especially the woolly monkey (Lagothrix lagotricha). In 42 observation follows over 14 months (April 1993 – December 1994), the uakari were in association with other species for all or some portion of time during 62% of the follows. Woolly monkeys were present during 65% of the polyspecific groupings. During 151.5 hr of timed observations, the uakari spent 29.21% of their time with other species, and 76% of their associative time with woolly monkeys. The participants of the associations may benefit from increased predator protection and more efficient use of resource. These data represent the first published notes from a long-term behavioral ecology study of red uakari.     

Estimation of Seed Shadows Generated by Andean Woolly Monkeys (Lagothrix lagothricha lugens)

Seed dispersal is known to play an important role in the ecology and evolution of plant communities, and there is ample evidence that seed dispersal by primates influences plant population dynamics in tropical forests directly. We used nonparametric statistical methods to estimate the dispersal kernels, i.e., the probability that a seed is moved a particular distance, generated by woolly monkeys (Lagothrix lagothricha lugens) at a sub-Andean forest in Colombia and test the hypothesis that the time of feeding influences dispersal distances. We collected data on monkey ranging patterns with the aid of global positioning system (GPS) units and obtained information on gut retention times from behavioral follows to build a model based on the kernel density estimator. Woolly monkeys drop most seeds hundreds of meters from parent trees and only a small proportion of seeds within close proximity. The time of seed ingestion had a significant effect on dispersal kernels, with seeds from fruits consumed early in the day having a greater chance of landing farther away from the tree than seeds swallowed in the late afternoon. The results of this study build on previous findings suggesting that woolly monkeys have a positive effect on the fitness of plants, which may be exacerbated in mountain forests where the diversity of large frugivores is low.     

Nutrient transport within and between habitats through seed dispersal processes by woolly monkeys in north‐western Amazonia

The contribution of vertebrate animals to nutrient cycling has proven to be important in various ecosystems. However, the role of large bodied primates in nutrient transport in neotropical forests is not well documented. Here, we assess the role of a population of woolly monkeys (Lagothrix lagothricha lugens) as vectors of nutrient movement through seed dispersal. We estimated total seed biomass transported by the population within and between two habitats (terra firme and flooded forests) at Tinigua Park, Colombia, and quantified potassium (K), phosphorus (P) and nitrogen (N) content in seeds of 20 plant species from both forests. Overall, the population transported an estimated minimum of 11.5 (±1.2 SD) g of potassium, 13.2 (±0.7) g of phosphorus and 34.3 (±0.1) g nitrogen, within 22.4 (±2.0) kg of seeds ha^?1 y^?1. Approximately 84% of all nutrients were deposited in the terra firme forest mostly through recycling processes, and also through translocation from the flooded forest. This type of translocation represents an important and high‐quality route of transport since abiotic mechanisms do not usually move nutrients upwards, and since chemical tests show that seeds from flooded forests have comparatively higher nutrient contents. The overall contribution to nutrient movement by the population of woolly monkeys is significant because of the large amount of biomass transported, and the high phosphorus content of seeds. As a result, the phosphorus input generated by these monkeys is of the same order of magnitude as other abiotic mechanisms of nutrient transport such as atmospheric deposition and some weathering processes. Our results suggest that via seed dispersal processes, woolly monkey populations can contribute to nutrient movement in tropical forests, and may act as important nutrient input vectors in terra firme forests. Am. J. Primatol. 72:992–1003, 2010. © 2010 Wiley‐Liss, Inc.     

Habitat preference in the critically endangered yellow‐tailed woolly monkey (Lagothrix flavicauda) at La Esperanza,Peru

Habitat loss is one of the main threats to wildlife. Therefore, knowledge of habitat use and preference is essential for the design of conservation strategies and identification of priority sites for the protection of endangered species. The yellow‐tailed woolly monkey (Lagothrix flavicauda Humboldt, 1812), categorized as Critically Endangered on the IUCN Red List, is endemic to montane forests in northern Peru where its habitat is greatly threatened. We assessed how habitat use and preference in L. flavicauda are linked to forest structure and composition. The study took place near La Esperanza, in the Amazonas region, Peru. Our objective was to identify characteristics of habitat most utilized by L. flavicauda to provide information that will be useful for the selection of priority sites for conservation measures. Using presence records collected from May 2013 to February 2014 for one group of L. flavicauda, we classified the study site into three different use zones: low‐use, medium‐use, and high‐use. We assessed forest structure and composition for all use zones using 0.1 ha Gentry vegetation transects. Results show high levels of variation in plant species composition across the three use zones. Plants used as food resources had considerably greater density, dominance, and ecological importance in high‐use zones. High‐use zones presented similar structure to medium‐ and low‐use zones; thus it remains difficult to assess the influence of forest structure on habitat preference. We recommend focusing conservation efforts on areas with a similar floristic composition to the high‐use zones recorded in this study and suggest utilizing key alimentation species for reforestation efforts.     

The skin of primates. XXXIV. The skin of the golden spider monkey (Ateles geoffroyi)

The skin of the golden spider monkey (Ateles geoffroyi) has many histological and histochemical similarities to that of the woolly monkey (Lagothrix lagotricha) and howler monkey (Alouatta caraya); however, this monkey possesses certain peculiar properties such as large sebaceous glands, a combined distributional pattern of eccrine and apocrine sweat glands, and abundant alkaline phosphatase in the sebaceous glands, apocrine and eccrine sweat glands. In brief, the anatomical and histochemical properties of the skin of this animal are more similar to those of the howler monkey than to the woolly monkey. In addition, the skin of these three Ceboids falls phylogenetically between that of the Cercopithecoidea and Pithecoidea.     

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.     

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.     

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.     

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.     

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.     

Diet of the brown howler monkeyAlouatta fusca in a semi-deciduous forest fragment of southeastern Brazil

The diet of a group of six brown howlers was studied weekly during 12 months in a reserve of 250 ha of secondary, mesophytic, semi-deciduous forest. The phenology of 186 trees of 72 species and 29 families was monitored simultaneously. Scan sampling was used to record the diet from dawn until dusk on a total of 60 days of observation, yielding 718 hr of animal-observer contact and 2,943 feeding scans. The diet was composed of leaves (73%), flowers (12%), and fruits (5%), from 68 identified plant species.Celtis iguanae, Cassia ferruginea, andInga spp. were the main food sources, accounting for approximately 50% of the diet. Young leaves (59%) were preferred to mature leaves (31%), trees contributing 56% and lianas 41% of the leaf diet. The ingestion of young leaves was correlated to the availability of these items, however, the correlations were not significant for flowers and fruits. The diet was poorer in fruits and richer in young leaves of lianas in comparison to other howler monkey species studies, probably as a consequence of the liana abundance in this forest fragment.     

Evidence for insectivory in two primate species (Callicebus torquatus lugens and Lagothrix lagothricha lagothricha) from northwestern Amazonia

Insects were recovered and identified from stomach contents of two Callicebus torquatus lugens and one Lagothrix lagothricha lagothricha collected in a remote area of northwestern Amazonia. Both C. torquatus lugens showed little insect matter in stomach contents. Conversely, a minimum of 133 individual insects were recovered from stomach contents of the L. lagothricha lagothricha. These included various larger, rapid forms (Cicadellidae) unlikely to have been inadvertently consumed while the animal was eating fruit.     

Behavioral ecology ofAlouatta seniculus in Andean cloud forest

The behavior and ecology ofAlouatta palliate àre well studied; we report here on the first long-term study of anotherAlouatta species, the red howler monkey,A. seniculus. AlthoughA. seniculus was studied at a high elevation in the Colombian Andes, it exhibits many behavioral and ecological similarities to lowlandA. palliata. Continuous focal sampling indicates thatA. seniculus spends 78.5% of its time resting, 5.6% moving, and 12.7% feeding. It has a day range of 1.09 km and a home range of 22 ha. Like its more northern relative,A. seniculus spends more than 50% of its feeding time on leaves–especially young leaves–but on a dry-weight basis, fruits comprise the majority of its diet. The small home and day ranges observed as well as the large amounts of time spent resting are all argued to be aspects of a relatively folivorous foraging strategy. Daily food intake is estimated to be 1.23 kg fresh weight (0.266 kg dry weight). Foraging efficiency (yield/time) varies by a factor of almost 6 across major food types, with item size and distribution being the key determinants. Food preferences change markedly over the activity period, with high-energy sources predominating early and high-protein sources late.     

Diet of the red howler monkey (Alouatta seniculus) in French Guiana

We report the feeding behavior and food preferences of a troop of red howler monkeys (Alouatta seniculus) over two annual cycles in primary tropical rain forest in French Guiana. The monkeys used 195 plant species from 47 families as food. Major food categories were young leaves (54%), mature fruits (21.5%), and flowers (12.6%). Other food categories included old leaves, immature fruits, termitarium soil, bark, and moss. The monkeys were less selective than other howler groups, since 19 plant species contributed 1% to their diet and accounted for only 35.7% of their total diet. The Sapotaceae was the most frequently eaten plant family and represented >10% of the total diet.