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 .     

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.     

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.     

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.     

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.     

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.     

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.     

Seasonal patterns of diet and ranging in two species of tamarin monkeys: Stability versus variability

From June through December, data were collected on the diet and ranging patterns of moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarin monkeys in the Amazon Basin of northeastern Peru. During this 7-month period, insects and nonleguminous fruits accounted for 83% of tamarin feeding and foraging time. Despite marked seasonal variation in rainfall and forest productivity, patterns of habitat utilization, day range, dietary diversity, resource exploitation, and activity budget remained relatively stable throughout the year. Moustached and saddle-back tamarins appear to solve problems of food acquisition and exploit patchily distributed feeding sites using a relatively limited set of foraging patterns. In general, these primates concentrate their daily feeding efforts on several trees from a small number of target plant species. These feeding sites are uncommon, produce only a small amount of ripe fruit each day, and are characterized by a high degree of intraspecific fruiting and flowering synchrony. Trees of the same species are frequently visited in succession, and individual feeding sites are revisited several times over the course of 1–2 weeks. This type of foraging pattern occurred during both dry and wet seasons and when exploiting fruit, nectar, legume, and exudate resources. Seasonal variation in the percentage of feeding and foraging time devoted to insectivory was also limited. In this investigation, there was no consistent evidence that temporal changes in overall forest fruit production had a major impact on the feeding, foraging, or ranging behavior of either tamarin species.     

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.     

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.     

Activity budget and diet of patas monkeys in Kala Maloue National Park,Cameroon: A preliminary report

A preliminary study was carried out on the feeding ecology of patas monkeys in the rainy season in Cameroon. Their daily activity rhythm revealed two active peaks. The proportion of time spent on feeding with respect to waking time was 30%. Patas monkeys largely depended on the flowers and buds of herbaceous plants and the larvae of insects for their diet as they ranged widely. Patas monkeys spent more time in feeding and travelled for a longer distance per day than the sympatric primate species, the tantalus monkey. It is considered that these findings reflected the large amount of food requirement due to the large body size, as well as the low density and high degree of dispersal of their food.     

Activity and ranging patterns in relation to fruit utilization by Brown Capuchins (Cebus apella) in French Guiana

I studied brown capuchins (Cebus apella)in primary forest in French Guiana. They displayed different feeding and ranging patterns in response to changes in fruit availability and distribution. When fruit was scarce and patchily distributed, foliage/stem feeding and invertebrate foraging was high, and capuchins limited their daily movement to <2 km, focusing on large fruit patches. When fruit was in average supply and scattered throughout the forest, the proportions of foliage/stems and invertebrates in the diet decreased, and the day range length increased to 2.8 km. When fruit was abundant and widespread, foliage/stems were rarely eaten, while invertebrate foraging increased, and. the daily locomotor distance was reduced to 2 km.     

An experimental study of bamboo ants in western Amazonia

Numerous ant taxa naturally inhabit stems of live and dead Guadua bamboo (Bambusoidea, Poaceae) in western Amazonia. In an experiment at the onset of the wet season in Peru’s Manu National Park, we augmented potential nest sites in stems of live bamboo, dead bamboo and dead ca?a brava (Gynerium sagittatum, another woody grass) at five stations within each of ten bamboo patches and ten control areas outside those patches. Each experimental stem possessed three vacant and available internodes, pre-drilled with, respectively, large, small and linear holes, mimicking the range of forms of surveyed natural entrances. After 24 days, approximately 13% of 798 available internodes had been colonized, the majority by fragments of existing colonies. Ignoring entrance type, which did not affect colonization for any species or species group, and censoring non-independent internodes of the same stem, we used individual stems as independent sample units in other tests. One specialist in live bamboo (Camponotus longipilis), and a likely specialist in dead bamboo (Camponotus depressus), were identified based on overrepresentation in bamboo habitat and disproportionate occurrence in live or dead bamboo stems. A third species, Camponotus (Pseudocolobopsis sp.) was more abundant in bamboo areas but colonized both dead bamboo and dead ca?a. Relatively high abundance of standing dead stems in Guadua forests may account for the presence of a dead stem specialist. The experiment missed detecting specialization in one live culm specialist (Camponotus mirabilis), likely due to its failure to simulate conditions required for the species’ unique modes of colony establishment and spread into new culms. Most opportunistic stem nesters colonized dead bamboo at significantly greater rates than dead ca?a, but were either equally well represented in bamboo and control areas, or underrepresented in bamboo habitat. Given low colonization rates overall, underrepresentation in bamboo cannot be attributed to competition from bamboo specialists for nesting space. Rather, it may be due to combined effects of seasonal flooding of bamboo habitat, and greater importance of food limitation, relative to nest site limitation, in that habitat. Received 9 May 2005; revised 25 August 2005; accepted 29 August 2005.     

Spatial and temporal patterns of morel fruiting

The biotic and abiotic factors conditioning morel fruit body production are incompletely known. We examined spatial and temporal patterns of Morchella esculenta fruiting over five years in a wooded site in Missouri, USA. Fruiting onset was inversely correlated with spring air and soil temperatures, whereas abundance was positively correlated with rain events (>10 mm) during the 30 d preceding fruiting. The two years with the greatest fruiting had the shortest fruiting seasons (6–7 d). Fruiting season length was positively correlated with soil warming, suggesting that a narrow range of optimum soil temperatures favour the explosive production of fruit bodies. All woody stems of at least 1 cm diam were mapped and stem diameter and crown condition were noted. Morel fruit bodies were significantly closer to stems of Carya spp., Tilia americana and Ulmus americana than predicted by the frequencies of these woody species or their contribution to the total basal area on the site. Although intra-annual clustering of fruit bodies was often observed, inter-annual clustering was not. The spatial pattern of M. esculenta fruiting appears to be associated with vegetation pattern, whereas the onset and abundance of fruiting are determined by the interaction of spring temperatures with availability of supporting precipitation.     

Sexual dimorphism in canine length of woolly spider monkeys (Brachyteles arachnoides,E. Geoffroy 1806)

We measured canine teeth from 28 woolly spider monkeys (Brachyteles arachnoides) to assess sexual dimorphism and population differences. The specimens are from the Brazilian states of Bahia, Minas Gerais, Espírito Santo, Rio de Janeiro, and São Paulo. We found strong sexual dimorphism in canine length for individuals belonging to populations south of 22°00 latitude but no sexual dimorphism in canine length from individuals of populations north of 21°00 latitude. Canine length did not vary among females of northern and southern populations. However, southern males had significantly longer canines than northern males. This geographical difference in canine morphology, together with the presence or absence of thumbs and published accounts of differences in genetics and social structure between northern and southern populations, suggests thatBrachyteles arachnoides may be composed of at least two subspecies, which appear to be separated by the rivers Grande and Paraiba do Sul and the Serra da Mantiqueira.     

Geographical patterns of deep mitochondrial differentiation in widespread Malagasy reptiles

Using sequences of the mitochondrial 16S rRNA gene, we reconstructed the phylogeography of six widely distributed Malagasy reptiles: two gekkonid lizard species, Phelsuma lineata and Hemidactylus mercatorius; two chameleons, the Calumma brevicorne complex, and Furcifer lateralis; and two skinks, Trachylepis gravenhorstii and Trachylepis elegans. Genetic differentiation among major haplotype lineages was high and in some cases indicates or confirms species status of the divergent populations. Maximum uncorrected sequence divergences were between 2.2% and 8.3% within the various species or species complexes. Haplotype lineages were exclusive to geographic regions, except in the commensal H. mercatorius where in three anthropogenic habitats coexistence of haplotype lineages was observed, possibly due to human translocation. The eastward flowing rivers Mangoro and Mananara may represent barriers to gene flow in the case of three species each. Some species sampled from humid eastern and arid western Madagascar showed no differentiation between populations from these two regions; instead the pattern observed was in several cases more concordant with a differentiation along a north-south axis.     

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.     

Development of co-feeding relationships in immature free-ranging Japanese monkeys (Macaca fuscata fuscata)

The co-feeding relationships of immature Japanese monkeys in the provisioned situation were studied. The most frequent co-feeders for immature females were diversified as compared to those for immature males. The number of immature females who showed strong co-feeding relationships with their mothers gradually decreased with age in both high- and middle/low-ranking matrilines, but the percent decrease was greater for middle/low-ranking immatures. Almost all immature females who displayed strong co-feeding relationships with adult males were from middle/low-ranking matrilines. Strong co-feeding relationships with mothers among immature males from high-ranking matrilines remained until 4 years of age. In contrast, strong co-feeding relationships with mothers among middle/low-ranking immature males decreased rapidly in the first year of life, and most 1- to 4-year-olds showed no strong co-feeding relationships with other group members. It is considered that middle/low-ranking mothers may not provide their immatures with a secure base for obtaining food in the provisioned situation.     

Diurnal and spatial patterns of Phytoseiidae in the citrus canopy

Phytoseiid mites were sampled in a grapefruit orchard at various times of the day to study their diurnal and seasonal distributions in the tree canopy. Samples were collected on 14, 20 and 28 October 1999 at 2 h intervals from 0600 to 2200 h. Similar samples were collected in a grapefruit orchard at 3 h intervals from 0600 to 2100 h on 9 and 16 March and on 17 and 24 August 2000 for phytoseiid mites. No differences in numbers of phytoseiid motiles were observed among the hours sampled in any of the three months. However, significant differences were observed in the number of phytoseiids per leaf based on location within the tree (eastern, western sides of the canopy or interior). Interior leaves collected in March and August 2000 had higher numbers of phytoseiids than exterior leaves taken from either the eastern or western sides of the tree canopy. Phytoseiids were more abundant in the March 2000 samples (mean = 1.10 phytoseiids/leaf) than in either October 1999 or August 2000 samples (mean = 0.16 and 0.19 phytoseiids/leaf, respectively). Prevalent phytoseiid species were Typhlodromalus peregrinus (Muma) (42.1%) and Iphiseiodes quadripilis (Banks) (50.4%) in October 1999, Typhlodromalus peregrinus (Muma) (76.2%) in March 2000, and Euseius mesembrinus (Dean) (54%) in August 2000.