Locomotion and feeding postures of spider and howling monkeys: field study and evolutionary interpretation

Field observations demonstrate clear differences in locomotion and feeding postures between spider monkeys (Ateles) and howling monkeys (Alouatta). When feeding, Ateles employs sitting postures approximately half the time, and a variety of suspensory postures using the tail the other half. Ateles moves quadrupedally during 52% of locomotion, by tail-arm suspension 25%, and various mixed support-suspensory modes the remainder. Tail-arm suspension is practiced more rapidly on thinner supports, and on more negatively inclined supports than is quadrupedal movement. Howlers do not locomote by tail-arm suspension: movement is almost entirely quadrupedal and is slower than that of spider monkeys. The positional behavior of spider monkeys fits closely recent views of major adaptive changes in hominoid evolution emphasizing brachiation and speed during travel. Howler locomotion and also tissue composition appear related to diet and digestive mechanisms.     

Positional behavior ofCebuella pygmaea in Yasuni National Park, Ecuador

In terms of positional behavior, the small-bodied callitrichids are distinguished from other anthropoids by their ability to leap between and to cling to large vertical supports, feeding occasionally or frequently on sap and bark insects. In this paper, I studied the positional behavior of a group of pygmy marmosets in a hilly wet tropical forest in Yasuni National Park, Ecuador. During traveling, the animals used quadrupedal walk/bound and leaping mostly on small horizontal supports. During foraging, quadrupedal walk/bound and clambering dominated. The main foraging postures were stand and cantilever, occurring mainly on small horizontal lianas. During feeding, scansorial locomotion was used very frequently. Claw clinging was the dominant feeding posture. Furthermore, large vertical lianas and tree boles were the most frequent feeding supports. These observations would suggest that scansorial locomotion, vertical clinging, and vertical leaping are most likelynot part of the same form function complex. Vertical leaps appear to be associated with moving in the lower parts of the forest. On the other hand, scansorial locomotion and vertical clinging appear to be related to feeding on the sap of tree boles and large lianas in the lower parts of the forest.     

Positional Behavior of Black Spider Monkeys (Ateles paniscus) in French Guiana

Spider monkeys (Ateles) frequently use suspensory locomotion and postures, and their postcranial morphology suggests convergence with extant hominoids in canopy and food utilization. Previous studies of positional behavior in Ateles, have produced variable rates in the use of different positional activities. I investigated the positional behavior of black spider monkeys (Ateles paniscus) in a wet rain forest in French Guiana, and assessed differences in the rates of use of positional modes across studies. I also discuss the significance of suspensory activities in forest utilization. In French Guiana, Ateles confined travel and feeding locomotion on small and medium-sized moderately inclined supports in the main canopy. Tail-arm brachiation and clamber were their main traveling modes, while clamber was the dominant feeding locomotor mode. Small horizontal supports were predominant during their feeding. Suspensory postures accounted for more than half of feeding bouts, with tail-hang and tail-hind limb(s) hang being the dominant postures. Feeding occurred largely in tree crown peripheries with the prehensile tail anchored frequently above the monkey. They usually collected food items below or at the same level as the body. There is no difference among the postures they used to acquire and eat young leaves and fruit. My results agree with reports on the positional behavior of different species of spider monkeys at other sites. Despite the use of different methods, the same species exhibited more or less similar profiles in similar forests. Interspecific differences could be associated with morphological differences. Moreover, intraspecific differences could be attributed to forest structure. The findings suggest that the major part of biological information is independent of methods used in the several studies. Suspensory behavior facilitates the exploitation of the forest canopy by shortening traveling pathways between and within trees, by enabling faster travel for the better exploitation of patchy food sources and by providing access to food in the flexible terminal twigs.     

Drinking from arboreal water sources by mantled howling monkeys (Alouatta palliata Gray).

Despite occasional trips to the ground and feeding in trees whose canopies touched the river, mantled howling monkeys were never seen to drink from any ground water. Drinking from arboreal cisterns was observed, but only during the wet season (meteorologically the less stressful season but phenologically the more stressful season). The lack of sufficient new leaves during the wet season forced the howlers to ingest more mature leaves which contained significantly less water. To compensate for the lowered amount of water in their food, the monkeys utilized arboreal water cisterns. The cisterns dried up during the dry season, but the howlers maintained their water balance by altering their time of actiivity and selecting a diet comprised largely of succulent new leaves. The effect of plant-produced secondary compounds on drinking also was discussed.     

广西西南部石山森林中熊猴的姿势行为

灵长类动物姿势行为研究对了解其环境适应机制具有重要意义.2012年9月至2013年8月,采用瞬时扫描取样法对广西弄岗国家级自然保护区内一群熊猴(Macaca assamensis)的姿势行为进行观察,比较熊猴姿势行为的季节和日时段变化.结果 表明,熊猴移动模式的频率存在显著差异,从高到低为四足行走(45.3％±7.6％...     

Resource use by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas,Veracruz, Mexico

The feeding preferences of howler monkeys at their northernmost distribution in the Neotropics are reported for an annual cycle. A remarkable selectivity for 27 species representing 15 families was observed. The Moraceae and Lauraceae plant families were the most important in the diet. The howlers spent an almost equal proportion of their feeding time eating leaves and fruit, and displayed a marked preference for young leaves and mature fruit. The consumption of different plant parts was markedly seasonal and the howlers’ ranging behavior was closely associated with the availability of young leaves and mature fruit. Their home range was unusually large (ca. 60 ha) for howlers and the food species exploited occur at very low densities (93%, ≤ 4 ind/ha). They chose food items richer in protein and energy. Alkaloid compounds, present in some of the leaves, play a secondary role in their dietary selectivity.     

Activity pattern of the brown howler monkeyAlouatta fusca,Geoffroy 1812, in a forest fragment of southeastern Brazil

A group of six brown howlers was studied during a year in the Santa Genebra Reserve, a 250ha-forest fragment near the city of Campinas, State of São Paulo, southeastern Brasil. On average, the group rested for 64% of the daylight hours and feeding and moving occupied 18% and 13% of this period, respectively. A greater proportion of time was spent feeding during dry season (24%) than the wet season (15%), and the reverse observed for time spent resting (59% and 69% of the group's daylight hours during dry and wet seasons, respectively). The increase of resting and decrease of feeding during wet season were related to the percentage of leaves in the group's diet, high even during the fruiting season (wet season). However, additional data of other groups are necessary to draw conclusions about the effects of habitat disturbance on this population.     

The diet of the capped langur (Presbytis pileata) in a moist deciduous forest in Bangladesh

Capped langurs (Presbytis pileata) in Madhupur National Park in north-central Bangladesh have an annual diet that is comprised largely of mature leaves (42% of 20,460 total feeding records). Among colobine monkeys, only some populations of red colobus (Procolobus badius) have a diet richer in mature leaves. New leaves (11%) and fruit (24%) are the other annually important dietary items. Seasonal breakdown of this diet, however, revealed that during the monsoon months of May through September theP. pileata diet is approximately 50% fruit, including pulpy ripe fruit. This is also the period of maximum fruit availability. Data on diet and food availability indicate that while capped langurs subsist on mature leaves during the dry season (80% of diet from November to March), they select fruit and new leaves and switch to these foods whenever they are available. These data support the hypothesis that the colobine feeding strategy is adapted to cope with seasonal food scarcity.     

Diets of some French guianan primates: Food composition and food choices

We studied food choices of black spider monkeys (Ateles paniscus) and red howlers (Alouatta seniculus) in an undisturbed tropical forest of French Guiana for 6 months in the rainy season. We made additional observations on tufted capuchins (Cebus apella) and examined the differences and similarities in feeding behavior with respect to the plant specific composition of the habitat and the biochemical characteristics of their food. Capuchins and spider monkeys mainly fed on ripe fruit pulp, to which they added invertebrates (capuchins) or young leaves (spider monkeys); their plant diet was more varied than that of howlers, which contained approximately equal proportions of ripe fruits and young leaves of many species, with large monthly variations in these food categories. BothAteles andAlouatta tended to feed preferentially on abundant plant species, with a large overlap in their fruit choices. The former species included a high proportion of soluble sugars and a low proportion of protein in its diet compared, to howlers. Leaves of several species selected byAlouatta reacted positively when screened for alkaloids and phenolic compounds. Besides specific metabolic requirements and adaptations to deriving nutrients from distinct food types, we hypothesize that the ability to taste sugars, which varies among primates, affects the range of foods appearing to be palatable and, consequently, contributes to the differentiation of feeding niches.     

The short-term effects of a hurricane on the diet and activity of black howlers (Alouatta pigra) in Monkey River, Belize

The diet and activity of a population of Alouatta pigra were compared before and immediately after a major hurricane to begin to explore how the monkeys cope with severe habitat destruction. Focal animal data were collected from January to April (dry season) for two seasons before (368 h) and one season after the storm (149 h) on a population of black howlers in Monkey River, Belize. During the first dry season after the storm, the monkeys changed their diet in direct accordance with the availability of food. The absence of fruit and flower production and the increase in new leaf availability forced the monkeys to adopt a completely folivorous diet. The activity budget of the monkeys also changed, and they spent more time inactive, which may be linked to the change in the distribution and type of food available. They also spent less time in social interactions, which may be due to the lower number of juveniles in the population or to the formation of new groups between unfamiliar individuals following the hurricane. The ability to live for long periods of time on leaves alone has allowed the remaining population to survive in the short term.     

Ecological niche differences betweenAlouatta palliata andCebus capucinus comparing feeding modes,branch use,and diet

During the wet season, two sympatric species of primates,Alouatta palliata (mantled howlers) andCebus capucinus (white-faced capuchins), were assayed for feeding niche differences through behavioral and habitat use patterns at Refugio de Fauna Silvestre Curu in Costa Rica. Differences in the use of relative diameter and thickness of branches and five different modes of feeding were compared between the species. White-faced capuchins used more manipulative modes of obtaining food, a wider range of arboreal habitat, and had a more diverse diet than mantled howlers. Mantled howlers may be more restricted than white-faced capuchins in arboreal microhabitat use due to their possible need for large support branches during feeding bouts and resting periods. We report that differences in feeding behaviors, diet, and arboreal habitat use seem to play a large role in separating these species niches.     

Positional behavior of the white uakari (Cacajao calvus calvus)

The positional behavior and habitat use of a group of white uakaries (Cacajao calvus calvus) was observed for 6 weeks in the dry season at Lake Teiú, Brazil. Data are presented for feeding, traveling, and resting activities. The most common feeding posture is sit, followed by stand. Cacajao frequently exhibits locomotor behaviors while in feeding trees, using pronograde clamber and quadrupedal walk. The most frequently used locomotor behaviors in travel are quadrupedal walk, leap, and pronograde clamber. Quadrupedal run and drop also figure importantly in the behavioral repertoire. The most frequent resting posture was sit, followed by ventral lie. Compared to representative members of the other pitheciin genera, Pithecia and Chiropotes, Cacajao engages in more locomotion while feeding, and uses more pedal suspension. While traveling, pronograde clamber and drop are more frequently used by Cacajao. Multiple, deformable supports are used more by Cacajao than by the other pitheciins throughout all activities. Overall, the positional behavior of Cacajao is more similar to that of Chiropotes than of Pithecia. Cacajao's behavioral solutions to the problems of balance imposed by its greatly reduced tail are discussed. © 1996 Wiley-Liss, Inc.     

The ecological role of the prehensile tail in white-faced capuchins (Cebus capucinus).

Prehensile tails appear to have evolved at least twice in platyrrhine evolution. In the atelines, the tail is relatively long and possesses a bare area on the distal part of its ventral surface that is covered with der-matoglyphs and richly innervated with Meissner's corpuscles. In contrast, the prehensile tail of Cebus is relatively short, fully haired, and lacks specialized tactile receptors. Little is currently known regarding tail function in capuchins, and whether their prehensile tail serves a greater role in feeding or traveling. In this paper we examine patterns of positional behavior, substrate preference, and tail use in wild white-faced capuchins (Cebus capucinus) inhabiting a wet tropical forest in northeastern Costa Rica. Observational data were collected over the course of 3 months on adult capuchins using an instantaneous focal animal time sampling technique. Differences in the frequency and context of tail use, and the estimated amount of weight support provided by the tail relative to other appendages during feeding/foraging and traveling were used as measures of the ecological role of this specialized organ in capuchin positional behavior. During travel, quadrupedal walking, leaping, and climbing dominated the capuchin positional repertoire. The capuchin tail provided support in only 13.3% of travel and was principally employed during below branch locomotor activities. In contrast, tail-assisted postures accounted for 40.6% of all feeding and foraging records and occurred primarily in two contexts. The tail was used to suspend the individual below a branch while feeding, as well as to provide leverage and weight support in above-branch postures associated with the extraction of prey from difficult to search substrates. A comparison of tail use in Cebus, with published data on the atelines indicates that both taxa possess a grasping tail that is capable of supporting the animal's full body weight. In capuchins and howling monkeys, the tail appears to be used more frequently and serves a greater weight-bearing role during feeding than during traveling. In Ateles, and possibly Brachyteles, and Lagothrix, however, the prehensile tail serves a dual role in both feeding and forelimb suspensory locomotion. Additional relationships between white-faced capuchin feeding, positional behavior, extractive foraging techniques, and prehensile tail use are discussed.     

Positional behavior of Siberian chipmunks (Tamias sibiricus) in captivity

Arboreal and semi-arboreal mammals have remarkably diverse positional behavior and associated morpho-functional adaptations related to the three-dimensional nature of their arboreal habitat. In this context, we investigated the positional behavior of captive Siberian chipmunks (Tamias sibiricus), small bodied semi-arboreal sciurids, in an aviary-type wire-mesh cage containing both terrestrial and arboreal supports. We sampled four adult individuals during a five-month period using focal animal sampling every 30 s. Results showed that animals preferred 8–10 cm horizontal supports and always avoided vertical supports. Locomotion occurred on both terrestrial and 8–10 cm arboreal supports whereas postural behavior occurred primarily on 8–10 cm arboreal supports. Quadrupedal walk dominated during locomotion, and occurred primarily on terrestrial horizontal supports, as is observed for other squirrels. The predominance of quadrupedal locomotion is consistent with the postcranial morphology of chipmunks. In contrast, clawed locomotion occurred on wire mesh and on >13 cm arboreal vertical supports. Finally, pronograde and orthograde sitting, both on 8–10 cm arboreal supports and on terrestrial supports, were the predominant postures, implying general predisposition to selection of stable postures on stable supports for food item manipulation and ingestion.     

Foraging ecology of howler monkeys in a cacao (Theobroma cacao) plantation in Comalcalco, Mexico

Recent evidence indicates that primate populations may persist in neotropical fragmented landscapes by using arboreal agroecosystems, which may provide temporary habitats, increased areas of vegetation, and connectivity, among other benefits. However, limited data are available on how primates are able to sustain themselves in such manmade habitats. We report the results of a 9-month-long investigation of the feeding ecology of a troop of howler monkeys (n = 24) that have lived for the past 25 years in a 12-ha cacao plantation in the lowlands of Tabasco, Mexico. A vegetation census indicated the presence of 630 trees (> or =20 cm diameter at breast height (DBH)) of 32 shade species in the plantation. The howlers used 16 plant species (13 of which were trees) as sources of leaves, fruits, and flowers. Five shade tree species (Ficus cotinifolia, Pithecellobium saman, Gliricidia sepium, F. obtusifolia, and Ficus sp.) accounted for slightly over 80% of the total feeding time and 78% of the total number trees (n = 139) used by the howlers, and were consistently used by the howlers from month to month. The howlers spent an average of 51% of their monthly feeding time exploiting young leaves, 29% exploiting mature fruit, and 20% exploiting flowers and other plant items. Monthly consumption of young leaves varied from 23% to 67%, and monthly consumption of ripe fruit varied from 12% to 64%. Differences in the protein-to-fiber ratio of young vs. mature leaves influenced diet selection by the monkeys. The howlers used 8.3 ha of the plantation area, and on average traveled 388 m per day in each month. The howlers preferred tree species whose contribution to the total tree biomass and density was above average for the shade-tree population in the plantation. Given the right conditions of management and protection, shaded arboreal plantations in fragmented landscapes can sustain segments of howler monkey populations for many decades.     

Responses of squirrel monkeys to seasonal changes in food availability in an eastern Amazonian forest

Tropical forests are characterized by marked temporal and spatial variation in productivity, and many primates face foraging problems associated with seasonal shifts in fruit availability. In this study, I examined seasonal changes in diet and foraging behaviors of two groups of squirrel monkeys (Saimiri sciureus), studied for 12 months in Eastern Brazilian Amazonia, an area characterized by seasonal rainfall. Squirrel monkeys were primarily insectivorous (79% of feeding and foraging time), with fruit consumption highest during the rainy season. Although monkeys fed from 68 plant species, fruit of Attalea maripa palms accounted for 28% of annual fruit-feeding records. Dietary shifts in the dry season were correlated with a decline in ripe A. maripa fruits. Despite pronounced seasonal variation in rainfall and fruit abundance, foraging efficiency, travel time, and distance traveled remained stable between seasons. Instead, squirrel monkeys at this Eastern Amazonian site primarily dealt with the seasonal decline in fruit by showing dietary flexibility. Consumption of insects, flowers, and exudates increased during the dry season. In particular, their foraging behavior at this time strongly resembled that of tamarins (Saguinus sp.) and consisted of heavy use of seed-pod exudates and specialized foraging on large-bodied orthopterans near the forest floor. Comparisons with squirrel monkeys at other locations indicate that, across their geographic range, Saimiri use a variety of behavioral tactics during reduced periods of fruit availability.     

邦亮东黑冠长臂猿日食性与活动节律的季节性变化

日食性变化和活动节律是动物行为的重要方面,通过对日食性变化与活动节律的研究,可以了解食物、温度和光照时间等环境因素的变化对动物行为的影响,以及动物在行为上的应对策略。2009 年1 -12 月,在广西靖西县邦亮东部黑冠长臂猿自治区级自然保护区内,采用瞬时扫描取样法对2 群东黑冠长臂猿觅食行为和活动节律进行了研究。结果显示,东黑冠长臂猿的活动和食性在旱季和雨季都具有明显的节律。鸣叫只发生在12:00之前,但旱季的鸣叫时间偏晚。在日节律上,东黑冠长臂猿在离开过夜树后和进入过夜树前各有一个取食高峰,07:00 喜欢取食果实和无花果,16:00 也选择更多的果实,但无花果较少,13:00 - 15:00 取食更多的叶和芽。在10:00 - 12:00,其用于休息和社会活动的时间增加。在雨季,东黑冠长臂猿以果实和无花果为主要食物,并且花大量时间觅食无脊椎动物;但在旱季,其食物以叶和芽为主。与之相适应,东黑冠长臂猿在旱季通过减少移动增加休息来节约能量开支和应对低温,同时它们增加取食的时间以获得等价的能量和营养。雨季时社会行为的比例明显高于旱季,而且其高峰出现在08:00 - 10:00,但旱季社会行为主要出现在11:00 - 14:00。在雨季东黑冠长臂猿没有出现休息高峰,相反在旱季10:00 左右出现一个明显的休息高峰。上述行为节律体现了东黑冠长臂猿对环境季节性变化的良好适应,使其能够在寒冷并且退化的喀斯特森林中生存繁衍。     

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.     

Seasonal variation in the feeding ecology of the grey-cheeked mangabey (Lophocebus albigena) in Cameroon

Seasonal fluctuations in resource abundance often cause primates to change their feeding behavior and ecology. The objective of this study was to examine the response of a largely frugivorous monkey, the grey-cheeked mangabey (Lophocebus albigena), to seasonal variations in fruit abundance. We used 15-min scan sampling to quantify feeding, activity, and habitat use by monkeys between February and December 1998 in the Dja Reserve, Cameroon. L. albigena were found to have omnivorous feeding habits, consuming the fruits, seeds, leaves, and flowers of 132 plant species. Although monkeys fed from many plant species, only five plant species accounted for 45% of all feeding records. The number of feeding observations on a plant species was significantly correlated with its fruit production. L. albigena responded to fruit-lean periods by shifting from a diet dominated by fruit to one dominated by seeds, flowers, and young leaves. This diet shift coincided with greater use of swamp habitat and higher dietary diversity. L. albigena spent the greatest percentage of scan samples feeding and traveling, but activities varied significantly over the day. Individuals spent a significantly higher percentage of scan samples feeding during the fruit-rich season than in the fruit-lean season. Comparing our results to those of studies in Gabon and Uganda, we found that L. albigena differ across regions in the number of plant species they consume and time spent feeding. These differences may be a result of variations in tree diversity or the strength of seasonal fluctuations in resource abundance among sites.     

Diet and feeding patterns in the kipunji (<Emphasis Type="Italic">Rungwecebus kipunji</Emphasis>) in Tanzania’s Southern Highlands: a first analysis

The diet and feeding behaviour of the kipunji (Rungwecebus kipunji) was studied over 45 months, the first dietary analysis for this species. During 9498 h of direct observation of 34 kipunji groups, a list of 122 identified foodplants was recorded. The list represents 60 families, including 64 trees, 30 herbs, 9 climbers, 7 shrubs, 6 lianas, 3 grasses and 3 ferns. Kipunji were observed eating bark, young and mature leaves, ripe and unripe fruits, flowers, pith, seed pods, rhizomes, tubers, shoots and stalks. Invertebrates, fungi, moss, lichen, and soil were also eaten. Macaranga capensis var. capensis, an early successional tree, was the most commonly consumed species, with leaves, leaf stalks, pith, flowers and bark all eaten. We demonstrate that the kipunji is an omnivorous dietary generalist, favouring mature and immature leaves, ripe and unripe fruits and bark in similar proportions, with an almost comparable fondness for leaf stalks and flowers. Kipunji appear to be adaptable foragers able to modify their diet seasonally, being more folivorous in the dry season and more frugivorous in the wet. Whereas more ripe fruit is eaten in the wet season, the proportion of unripe fruit remains similar across the year. The proportion of mature leaves and pith increases throughout the dry season at the expense of ripe fruits and bark, and this may compensate nutritionally for the lack of available dry-season ripe fruits. Relatively more pith is eaten in the dry season, more stalks at the end of the dry and beginning of the wet seasons, and bark consumption increases as the rainfall rises.