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.     

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.     

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.     

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.     

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.     

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.     

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.     

Social Behavior,Reproductive Strategies,and Population Genetic Structure of <Emphasis Type="Italic">Lagothrix poeppigii</Emphasis>

For species of primates in which females emigrate, we would expect males within groups to be related to one another. Kin selection theory suggests that these males should associate preferentially with one another, be more affiliative and cooperative with one another than females are, and compete less overtly with one another over reproductive opportunities than males in female philopatric taxa do. Precisely these patterns of social behavior characterize well-studied populations of 2 of the 3 atelin primate genera: spider monkeys (Ateles) and muriquis (Brachyteles). For the third atelin genus, Lagothrix, patterns of intragroup social behavior have been less well-documented. We studied the social and reproductive behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Ecuador during a one-year observational study and subsequently used molecular techniques to investigate population genetic structure and dispersal patterns for this taxon. Among adult male woolly monkeys, both affiliative and agonistic interactions were rare, and males were seldom in close proximity to one another. Relationships among male woolly monkeys are best characterized as tolerant, especially in the context of mating wherein direct competition among males was minimal despite the fact that females mated with multiple males. Relationships among females were likewise generally tolerant but nonaffiliative, though females often directed harassment towards copulating pairs. Affiliative interactions that did occur among woolly monkeys tended to be directed either between the sexes—primarily from female to male—or from younger towards older males, and the proximity partners of females tended to be members of the opposite sex. These results suggest that bonds between the sexes may be more important than same-sex social relationships and that direct female-female competition is an important feature of woolly monkey reproductive biology. Our genetic results indicate that, as in other atelins, dispersal by females is common, but some male dispersal likely occurs as well. In some but not all groups we studied, nonjuvenile males within social groups were more closely related to one another on average than females were, which is consistent with greater male than female philopatry. However, differences in these patterns among our study groups may reflect local variation in dispersal behavior.     

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 .     

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.     

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).     

Diet of a group ofLagothrix Lagothricha Lagothricha in southeastern Colombia

We report the diet of a wild troop of woolly monkeys (Lagothricha lagothricha lagothricha)in undisturbed rain forest in the lower Apaporis River region of southeastern Colombia during 2400 hr of observation from January 1985 through September 1987. The woolly monkey diet consisted of 78.9% fleshy fruits, 4.3% seeds, 11.4% leaves, 4.9% invertebrates, 0.1% flowers, 0.1% tendrils, and 0.3% bark. Fleshy, endozoochorus fruits were by far the most important type of food for the subjects. Intensive sampling of food plants used by L. 1. lagothrichashows floristically diverse diet including 185 species in 41 families, the most frequently used and species-rich of which are the Sapotaceae,the Moraceae, and the Mimosaceae. We compare our findings with other recent data on the three other subspecies of Lagothrixand discuss some of the ecological influences that might account for the macrogeographic similarities and differences observed in woolly monkey diets. Together, these studies provide the empirical basis for an unambiguous conclusion: Lagothrix lagothricha,classified by the IUCN as vulnerable, is a significant seed disperser throughout its extensive range. Accordingly, extinction of a population of Lagothrix isa major perturbation in its ecosystem.     

Abundance and natural control of the woolly aphid <Emphasis Type="Italic">Eriosoma lanigerum</Emphasis> in an Australian apple orchard IPM program

Woolly aphid (Eriosoma lanigerum Hausmann) (Hemiptera: Aphididae), was monitored over three growing seasons (1995--1998) to assess its abundance and management under apple IPM programs at Bathurst on the Central Tablelands of NSW, Australia. Woolly aphid infestations were found to be extremely low in IPM programs utilising mating disruption and fenoxycarb for codling moth Cydia pomonella L. (Lepidoptera: Tortricidae) control. This was the direct result of increased numbers of natural enemies. No insecticides were applied for woolly aphid control. Under the IPM strategies tested the principal control agent was identified as European earwig (Forficula auricularia L.) (Dermaptera: Forficulidae). Earwigs in combination with Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) reduced woolly aphid infestations below the action threshold set by commercial growers. However, A. mali together with other flying natural enemies, e.g., ladybirds, lacewings and hoverflies, did not provide commercially acceptable control of woolly aphid in the absence of earwigs. Under the conventional spray program, using the broad-spectrum insecticide azinphos-methyl for codling moth control, the level of woolly aphid infestation increased with each successive season and biological control was not established. When azinphos-methyl was withdrawn, natural enemies migrated in and provided control of woolly aphid within one season. This is the first study to show that the biological control of woolly aphid can be achieved in a commercially viable IPM program.     

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.     

Rapid shifting of foraging pattern by Yakushima macaques ( Macaca fuscata yakui ) in response to heavy fruiting of Myrica rubra

We describe short-term changes in foraging behavior by wild Yakushima macaques (Macaca fuscata yakui),which inhabit a warm-temperate broad—leaved forest on Yakushima Island (30°N, 131°E), Japan. Rapid changes of dietary composition, activity budget, and range use by the monkeys occurred from May to June, apparently associated with changes in the availability of the fruit of Myrica rubraBefore the fruit ripened, monkeys spent less time moving and more time feeding on many species of leaves, which accounted for 40% of feeding time. However, when M. rubrabegan to ripen, they fed intensively on the fruit, which accounted for three-fourths of feeding time,though the activity budget remained unaffected As fiuit of M. rubradecreased,the monkeys fed more on the fruit of other species and on insects, and spent more time moving at higher speeds. There marked shifts in foraging pattern occurred within only two months. In terms of moving cost and dietary quality,Yakushima macaques shifted their foraging pattern according to the availability of M. rubrafrom a “low-cost, low-yield” strategy to a “low-cost, high-yield” strategy, and then to a more costly strategy. The ability to make such rapid shifts in foraging pattern may allow the macaques to effectively use the highly variable food supply within their small range.     

Composition and Nutritional Characteristics of Fungi Consumed by Callimico goeldii in Pando, Bolivia

Though ≥22 species of Primates consume fungi, most do so at low rates, comprising <5% of their feeding time. Goeldi's monkeys (Callimico goeldii), spend up to 29% of their feeding time year-round consuming fungal sporocarps, the fruiting bodies of fungi. We provide comprehensive data on the nutritional characteristics of 4 species of fungi consumed by Callimico goeldii (Ascopolyporus polyporoides, Ascopolyporus polychrous, Auricularia auricula, and Auricularia delicata). The composition of the fungi is similar to that of other fungi: predominantly fiber (66.2–83.0% dry matter) with small amounts of sugar (2.0–5.6% dry matter) and crude fat (0.9–1.6% dry matter). Though the crude protein content is substantial (5.5–13.4% dry matter), much of the nitrogen in the fungi is not likely to be available to Callimico goeldii because it is associated with indigestible food components or is in nonprotein form. The mineral content of the fungi are within the normal range for fungi generally and the calcium-to-phosphorus ratio is low (0.07–0.25). Fungi appear to be a low-quality food resource for Callimico goeldii and may contribute to their relatively large home ranges and low population density compared to other Callitrichinae. Research on the ability of Callimico goeldii to digest fungi is needed to understand fully the nutritional value of fungi to them. We discuss adaptations Callimico goeldii may have for improving their ability to obtain nutrients from fungi and potential ecological correlates of mycophagy.     

Vocal Repertoire of Golden-backed Uakaris (<Emphasis Type="Italic">Cacajao melanocephalus</Emphasis>): Call Structure and Context

The study of vocal behavior can reveal important aspects of how and why a species communicates in relation to ecological and social challenges. We here focus on vocal communication in golden-backed uakaris (Cacajao melanocephalus), diurnal, pitheciine monkeys that exhibit fission-fusion social organization and typically inhabit dense forests that limit the potential for visual communication. Moreover, the species spends little time engaged in tactile or olfactory communication, e.g., social grooming and scent marking, respectively. Hence, vocalizations may be very important for the coordination of social organization in these monkeys. We 1) categorized golden-backed uakari vocalizations, 2) ascertained their behavioral context, and 3) investigated whether golden-backed uakari calls can encode information about the signaler. We observed the monkeys during 2 wet seasons in the flooded igapó forest of Jaú National Park, Brazil. We showed that golden-backed uakaris have 9 call types in their vocal repertoire, all distinguishable by ear and from analysis of spectrograms. Some calls, e.g., play-specific calls, were used only in particular behavioral contexts, and by individuals of specific age, whereas others were emitted under a range of situations. The structure of the loud tchó call varied among individuals, and according to behavioral context, i.e., whether individuals were foraging/feeding, traveling, or performing agonistic interactions. This knowledge of the species’ vocal repertoire is valuable for surveying the monkeys acoustically in habitats where visual surveys are difficult.     

Diet and activity budget of <Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis> in the Qinling Mountains,China

We collected data on diet and daytime activity budget, and investigated the phenology of food trees and food abundance for a group of Rhinopithecus roxellana on the East Ridge of Yuhuangmiao in the Qinling Mountains from November 2001 to December 2003. We calculated the seasonal activity budget using data collected by scan sampling from 84 full-day observations (winter 16, spring 18, summer 28, autumn 22 days). During scan sampling we recorded behavioral states, and the food items and species consumed. The subjects consumed 84 plant species, including trees and shrubs of 29 families, and lichens. Food species varied seasonally. The overall diet of R. roxellana consisted of 29.4% fruit/seeds, 29.0% lichens, 24.0% leaves, 11.1% bark, 4.2% buds, 1.3% twigs and 1.0% unidentified items. Because the abundance of different food items varied seasonally, the monkeys had to shift their major food items seasonally. The annual activity budget of R. roxellana was 36.2% time spent resting, 35.8% feeding, 22.9% moving, and 5.1% other behavior. Seasonal changes in activity budget were observed. R. roxellana spent more time moving in autumn, when the quality of the food might be highest, and least time moving in winter when the food quality might be lowest. Thus, this type of monkey has a passive foraging strategy.