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.     

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.     

Nutritional and Health Status of Woolly Monkeys

Woolly monkeys (Lagothrix lagotricha and L. flavicauda) are threatened species in the wild and in captivity. Numerous zoological institutions have historically kept Lagothrix lagotricha spp., but only a few of them have succeeded in breeding populations. Therefore the majority of institutions that formerly kept Lagothrix lagotricha are no longer able or willing to do so. Captive populations of the species have frequent health problems, most significantly hypertension and related disorders. Researchers have conducted free-ranging dietary and behavior studies with respect to woolly monkeys, but have established no concrete link between diet or nutrients and captive health problems. The available literature we discuss indicates that researchers need to examine the link further. In addition, it is critical to the survival of the primates to be able to keep breeding populations in captivity owing to increasing natural pressures such as deforestation and hunting. Therefore, better understanding of the captive and free-ranging behavior and health parameters of the species is vital to ensure their survival and to maintain forest health and diversity. Researchers need to conduct large-scale research studies comparing the health and complete diet of individuals in the wild and captivity to resolve health problems facing the species in captivity.     

Habitat,diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroy 1806)

Results of a 10-month study of the ecology and behavior of free- ranging woolly spider monkeys (Brachyteles arachnoides)in Brazil show that these animals are strongly folivorous. Leaf-eating accounted for more than 50% of the total feeding time in all samples but one and accounted for more than 80% of the total feeding time in three samples. Mature foliage was routinely eaten. Woolly spider monkeys consistently spend more than 50% of each day quietly resting and sleeping. Animals travel little except when actively feeding and show low levels of social interaction. Such an activity profile suggests that woolly spider monkeys may often be living near the limits of their energetic resources. The social organization of the species is unusual for a folivorous primate in that small groups of females and associated immature animals confine their activities to discrete home-range areas, whereas males are itinerant, traveling over the home ranges of various female groups. Animals sharing a common home-range area show no permanent daily pattern of association other than that of mother-dependent offspring. Foraging alone or with few conspecifics should maximize each individual’s returns from foraging by minimizing the day range that must be traveled each day to locate foods while simultaneously lowering interference competition for higher-quality dietary resources.     

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 .     

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.     

Diet does not affect intercolonial fighting in Leptothoracine ants

Summary An experiment examined the effects of diet on brood rearing in colonies ofLeptothorax ambiguus andL. longispinosus and on fighting between colonies of the two species. Colonies fedDrosophila and honey reared more pupae than colonies fed the Bhatkar and Whitcomb (1970) diet. However, diet had no effect on intercolonial fighting.     

Diet of the Brown Mouse Lemur (Microcebus rufus) in Ranomafana National Park, Madagascar

The conventional notion is that small-bodied primates should be highly insectivorous in order to obtain protein and other nutrients from a food source that is more easily digestible than plant matter. I studied feeding behavior of Microcebus rufus for 16 months in the east coast rainforest of Ranomafana National Park. I determined the diet primarily through analysis of 334 fecal samples from live-trapped individuals. They consumed a mixed diet basically of fruit and insects year-round. I identified 24 fruits, while 40–52 remain unidentified. Bakerella, a high-lipid epiphytic semiparasitic plant, was in 58% of fecal samples that contained fruit seeds, and was consumed year-round irrespective of general resource availability. It served both as a staple and keystone resource. Fruit was less frequently totally absent from fecal samples of individual mouse lemurs than insect matter was. For Microcebus rufus, fruit may be a primary source of energy, not just complementary to insects. Fruit consumption increased in quantity and diversity during the latter part of the rainy season and the very early part of the dry season, when fruit production was relatively high. This pattern in fruit feeding is similar to that for mouse lemurs in the west coast dry forests and is related to specific nutritional needs dictated by the highly seasonal character of the life cycle. Coleoptera were present in 67% of samples examined and were consumed year-round by the subjects, but insect consumption did not increase during the rainy season when insect abundance was highest.     

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.     

Ectomycorrhizal fungal community structure across a bog-forest ecotone in southeastern Alaska

We examined the ectomycorrhizal (ECM) fungal community across a bog-forest ecotone in southeastern Alaska. The bog and edge were both characterized by poorly drained Histosols and a continuous layer of Sphagnum species, ericaceous shrubs, Carex species, and shore pine [Pinus contorta Dougl. ex Loud. var. contorta]. The forest had better-drained Inceptisols and Spodosols, a tree community comprised of western hemlock [Tsuga heterophylla (Raf.) Sarg.], yellow cedar (Thuja plicata Donn ex D. Don.), Sitka spruce [Picea sitchensis (Bong.) Carr.] and shore pine, and an understorey of ericaceous shrubs and herbs. ECM root tip density (tips cm^–3 soil) was significantly greater in the forest than the edge or bog and ECM colonization was significantly different in all three plant communities. The below ground ECM fungal taxa were analyzed using molecular techniques (PCR-RFLP and DNA sequencing). Three ECM fungal taxa, Suillus tomentosus (Kauffman) Singer, Cenococcum geophilum Fr.:Fr, and a Russula species, differed in relative frequency, yet were among the four most frequent in all three plant communities. Although differences in ECM fungal richness were observed across plant communities, unequal sampling of ECM roots due to root density and colonization differences confounded richness comparisons. Using resampling procedures for creating taxon-accumulation curves as a function of sampled ECM roots revealed similarities in cumulative ECM fungal taxa richness across the ecotone.     

Diet of Buffy Tufted-Eared Marmosets (Callithrix aurita) in a Forest Fragment in Southeastern Brazil

The feeding ecology of the Atlantic forest marmosets (Callithrix spp.) in southeastern Brazil is poorly known, and few studies have focused on buffy tufted-eared marmosets, Callithrix aurita. We determined the food items and investigated the seasonal variation in the diet of a group of four Callithrix aurita in a 17-ha semideciduous forest fragment in southern Minas Gerais State, Brazil. We recorded daily feeding activities between October 1994 and September 1995 using scan sampling at 5-min intervals. The marmosets devoted feeding time to gums (50.5%), fruits (11%), and animal prey (38.5%) in a total of 499 records. Plant resources comprised 27 species from 16 families. They used Acacia paniculata (Mimosoideae, Leguminosae), the main gum source (82%), year-round. Maclura tinctoria (Moraceae) was the fruit species that they consumed most (22%). The marmosets preyed on caterpillars (33%), katydids (5%), and homopterans (4%). Feeding on fruits varied seasonally and was inversely related to gum feeding. Consumption of animal prey remained constant over the year. The wide and year-round dependence on gum suggests that Acacia may play a critical role in marmoset persistence in forest fragments.     

Alloparental behavior in a captive group of spider monkeys (Ateles geoffroyi) at the Auckland zoo

I studied alloparental behavior in a captive group of spider monkeys at the Auckland Zoo using seven infants as focal subjects and assessed the effects of age, sex, and reproductive status of alloparents on patterns of infant-other interaction. Adult males initiated interactions with infants most often, followed by adult females. Immature individuals interacted with infants infrequently. Infants themselves initiated contact with adult males more often than with other members of the group. Alloparental behavior in spider monkeys differs from that in most other species in that the infant is an active rather than a passive participant in alloparental interactions. I discuss the patterns of infant-other interaction in relation to the social structure and dispersal patterns of Ateles.     

A case of adoption in a wild group of black-fronted titi monkeys (Callicebus nigrifrons)

We observed a case of infant adoption in an unprovisioned group of wild black-fronted titi monkeys (Callicebus nigrifrons). During our long-term field study we noticed that an infant had moved from one of our study groups (“Desbotado”) to another (“Rio”). Observations of the adoptive group confirm that it was being cared for by the adult male, and initially the group’s adult female was nursing the infant alongside her biological infant. Interestingly, the native and adoptive groups have frequent inter-group interactions, but at no point have we observed the native group trying to retrieve its infant. As of April 2007 the infant has been living in its adoptive group for 19 months. These data document the first case of adoption in this genus; they suggest that infant recognition is poorly developed in this species and that under certain circumstances wild groups of C. nigrifrons can successfully rear twins. In our study population reproductive females give birth to one infant every year; the only case when this has not happened is with the group that adopted the infant, suggesting that adoption may generate a reproductive cost.     

Primate Diet and Biomass in Relation to Vegetation Composition and Fruiting Phenology in a Rain Forest in Gabon

To test the hypothesis that primate populations are limited by food resources, we studied the feeding ecology of three cercopithecines and one colobine in a rain forest in central Gabon. Simultaneously, we monitored the fruiting phenology of trees and estimated the biomass of the monkey community. The Makandé Forest is dominated by Caesalpiniaceae and characterized by a lack of secondary vegetation and of trees species producing fleshy fruits. Fruit production was irregular intra- and interannually. Fruiting peaks of dry fruits (mainly Caesalpiniaceae) and of fleshy fruits occurred at the same period. However, interseasonal and interannual variability was greater in Caesalpiniaceae than in other families. As a result, the Makandé forest is subject to bottlenecks when food is scarce. On an annual basis, seeds (primarily Caesalpiniaceae) dominated the diet of all monkeys. On a seasonal basis, cercopithecines preferentially consumed fleshy fruits as long as they were available, whereas colobines increased consumption of young leaves when seed availability declined. The consumption of mature leaves was low. The monkey community biomass (ca. 204 kg/km²) is one of the lowest in Central Africa. We suggest that both cercopithecine and colobine populations are limited as a result of the combined effect of the dominance of Caesalpiniaceae, which provide dry fruits according to a mast-fruiting pattern and mature leaves of low quality, and the lack of seral successional stages, which provide fleshy fruit on a more regular pattern and leaves of better quality. During the period of food scarcity, cercopithecines should suffer from the low availability of fleshy fruit, which are their favorite food. At the same period, colobines should be limited by the low availability of edible leaves. Similar low primate biomasses are found in forests dominated by Caesalpiniaceae or Lecythidaceae in South America and in Dipterocarpaceae forests in South Asia, which suggests that their biological characteristics, in particular dry fruits and mast fruiting, are unfavorable to monkey populations. Our results confirm that habitat mosaics may support larger populations of primary consumers than homogeneous primary forests can.     

Conservation Implications of Hybridization in African Cercopithecine Monkeys

Numerous field reports of hybrid monkeys and documented cases of persistent hybrid zones suggest that natural hybridization is common among African cercopithecines. Both theoretical considerations and a review of cases lead us to conclude that parapatric hybridization among closely related allotaxa is a widespread, usually natural process whose incidence may be modified by human influence. Sympatric hybridization, between species ecologically distinct enough to have overlapping ranges, is rarer, and in monkeys tends to occur in settings where natural or anthropogenic habitat edges restrict migration and hence access to unrelated conspecific mates. Although sympatric hybridization occurs in the absence of human disturbance, and may even have been a creative force in cercopithecine evolution, anthropogenic habitat fragmentation may increase its incidence. Hybridization with a more abundant form may increase the level of threat faced by a species whose numbers and range have been severely restricted, either naturally or artificially.     

Behavioral Ecology of Sympatric Chimpanzees and Gorillas in Bwindi Impenetrable National Park,Uganda: Diet

Via a field study of chimpanzees (Pan troglodytes schweinfurthii) and gorillas (Gorilla gorilla beringei) in Bwindi Impenetrable National Park, Uganda, we found that their diets are seasonally similar, but diverge during lean seasons. Bwindi chimpanzees fed heavily on fruits of Ficus sp., which were largely ignored by the gorillas. Bwindi gorilla diet was overall more folivorous than chimpanzee diet, but was markedly more frugivorous than that of gorillas in the nearby Virunga Volcanoes. During 4 mo of the year Bwindi gorilla diet included more food species than that of the chimpanzees. Three factors in particular—seasonal consumption of fibrous foods by gorillas, interspecific differences in preferred fruit species, and meat consumption by chimpanzees—contributed to dietary divergence between the two species. When feeding on fruits, gorillas ate Myrianthus holstii more frequently than chimpanzees did, while chimpanzees included more figs in their annual diet. Chimpanzee diet included meat of duikers and monkeys; gorilla frequently consumed decaying wood.     

Diet of the black-headed heron Ardea melanocephala during the breeding season in South African grasslands

The diet of the black-headed heron was studied using analysis of pellets and prey remnants (225 prey items identified) collected from four sites in South African Highveld Grassland, transformed into cultivated fields. Small vertebrates comprised the staple food of chicks. Rodents were the most important vertebrate prey. Otomys irroratus comprised ca. 50% of the total biomass of vertebrate prey consumed. The diet was supplemented by small lizards, snakes, frogs and fishes. Grasshoppers, beetles, crabs and other arthropods were occasionally preyed upon.     

Rhinopithecus bieti at Tacheng,Yunnan: Diet and Daytime Activities

We collected data on diet and activity budget in a group of Rhinopithecus bieti at Tacheng (99°18E, 27° 36'N, between 2,700–3,700 m asl), Yunnan, from March 1999 to December 2000. We mainly recorded species-parts eaten with feeding scores from scanning state behaviors of one-male units in tree-crowns. We also conducted microscopic analysis of feces collected monthly. The subjects consumed 59 plant species, belonging to 42 genera in 28 families, of which 90 species-parts were distributed as follows: 21 in Winter, 38 in spring, 39 in Summer, 47 in autumn. Conversely, the group annually spent, on average, 35% of daytime feeding, 33% resting, 15% moving, and 13% in social activities. Seasonal changes are apparent in daytime budget and food item-related feeding time in tree-crowns, food remains in feces, and the number of species-parts eaten. Correlations within and between food items and time budget clearly indicate maximization of foraging effectiveness and minimization of energy expenditure. In consideration of reports from northern and southern groups, that which underlay the specific adaptation to the habitat appeared to be similar to those of other colobines. Thus, the ultimate factors for survival of the species are more hopeful than expected.     

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.