Enclosure environment affects the activity budgets of captive Japanese macaques (Macaca fuscata)

Individuals adapt to changes in their environment, such as food availability and temperature, by adjusting the amount of time spent in different behavioral activities. These adjustments in behavior should vary across age-sex class according to specific physiological and social needs. We studied the activity budgets of three social Japanese macaque groups inhabiting either vegetated or nonvegetated enclosures in order to compare the effects of access with vegetation, as both food and substrate on resting, feeding, grooming and moving activities over a 12-month period. Daily access to natural foods for monkeys in the vegetated enclosure seems to be largely responsible for the differences in daily time budgets of these three groups. Resting time in all three groups was longer than the time devoted to other activities. Resting and moving time in the two nonvegetated enclosures was significantly longer than in the vegetated enclosure. In contrast, feeding and grooming time was significantly longer in the vegetated enclosure. Seasonal variation in time spent feeding, resting and grooming was significantly effected by enclosure type. In all three enclosures, immatures, particularly females, spent more time feeding and moving, whereas adults spent more time resting. Significant monthly variation in time spent by age-sex class was noted only for feeding and resting. Interestingly, in the vegetated enclosure, time spent feeding on natural vegetation was equal to the amount of time spent feeding on provisioned food. This suggests that factors other than energetic and nutritional needs may be important determinants of the activity budget of the species. These results have important implications for the enrichment of captive primates and our understanding of the maintenance of activity patterns by primates in the wild.     

The foraging behavior of Japanese macaques Macaca fuscata in a forested enclosure:Effects of nutrient composition,energy and its seasonal variation on the consumption of natural plant foods

In the wild, primate foraging behaviors are related to the diversity and nutritional properties of food, which are affected by seasonal variation. The goal of environmental enrichment is to stimulate captive animals to exhibit similar foraging behavior of their wild counterparts, e.g. To extend foraging time. We conducted a 12-month study on the foraging behavior of Japanese macaques in a semi-naturally forested enclosure to understand how they use both provisioned foods and naturally available plant foods and what are the nutritional criteria of their consumption of natural plants. We recorded time spent feeding on provisioned and natural plant foods and collected the plant parts ingested of their major plant food species monthly, when available.We conducted nutritional analysis (crude protein, crude lipid, neutral detergent fiber-'NDF', ash) and calculated total non-slructural carbohydrate - 'TNC' and total energy of those food items. Monkeys spent 47% of their feeding time foraging on natural plant species. The consumption of plant parts varied significantly across seasons. We found that leaf items were consumed in months when crude protein, crude protein-to-NDF ratio, TNC and total energy were significantly higher and NDF was significantly lower, fruit/nut items in months when crude protein and TNC were significantly higher and crude lipid content was significantly lower, and bark items in months when TNC and total energy were higher and crude lipid content was lower. This preliminary investigation showed that the forested enclosure allowed troop members to more fully express their species typical flexible behavior by challenging them to adjust their foraging behavior to seasonal changes of plant item diversity and nutritional content, also providing the possibility for individuals to nutritionally enhance their diet.     

The effect of urban and rural habitats and resource type on activity budgets of commensal rhesus macaques (Macaca mulatta) in Bangladesh

Macaques are characterized by their wide distribution and ability to adapt to a variety of habitats. Activity budgets are affected by habitat type, season, and food availability in relation to differing age–sex class and individual requirements. We conducted a comparative study on two commensal rhesus groups, one living in a rural village and the other in the center of urban Dhaka, Bangladesh. The study was conducted in three different seasons between 2007 and 2009 in order to evaluate how habitat type and season affects their behavioral activities. Differences in food type and its availability between these two habitats were mainly responsible for the variations in activity budgets between groups. Feeding time in the rural group was significantly longer than that in the urban group. In contrast, grooming and object manipulation/play were significantly greater in the urban than the rural group. Seasonal variations in all major behaviors were significantly affected by group, with more time spent feeding in summer than in winter/dry season, and more time spent grooming and moving in winter/dry season than summer in the rural group. In contrast, time spent resting was greater in the monsoon and summer seasons than the winter/dry season in the urban group. Grooming time was greater in the winter/dry season than the monsoon and summer seasons. In both groups, immature of both sexes spent significantly more time on feeding and object manipulation/playing and less time resting than adults. Adult females spent more time grooming than males and immatures, of both sexes, in both groups. Moreover, the rural group spent most of their time feeding on garden/crop produce and wild plant food resources, while the urban group spent more time feeding on provisioned foods. These results showed that differences in the activity budgets of rural and urban dwelling macaques were due largely to the differences in available food resources. Commensal rhesus macaques show a high degree of behavioral flexibility in response to habitat and resource variability, and knowledge of these differences is important for the conservation and management of highly commensal primates.     

Optimal foraging theory predicts effects of environmental enrichment in a group of adult golden lion tamarins

The success of environmental enrichment programs in effecting specific changes in the behavior of captive animals has not always been uniform. Separate studies demonstrated both an increase in food competition and a decrease in food competition among captive group-living primates upon introduction of foraging devices. The objectives of this study were to measure the effects of variation in resource distribution and availability on food competition in a group of captive adult golden lion tamarins (Leontopithecus rosalia). The resource variables chosen were suggested from optimal foraging theory. The energy invested to obtain an item influenced food transfer and aggressive behaviors while food abundance did not. All individuals obtained an equivalent number of items over the course of the experiment from the foraging device, even though some tamarins obtained most of their food rewards directly from the device while others received their food rewards primarily through food transfer from other group members. Because the monkeys appeared highly motivated to obtain food from the test apparatus and did not habituate to it, the foraging device used in this experiment could be used as regular environmental enrichment for golden lion tamarins. One way to circumvent potentially unacceptable rates of aggression, with this or any feeding protocol that increases foraging task complexity and search time, may be to provide more than one foraging device per group. Zoo Biol 17:231–244, 1998. © 1998 Wiley-Liss, Inc.     

The Hand That Feeds the Monkey: Mutual Influence of Humans and Rhesus Macaques (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) in the Context of Provisioning

Historically, humans and other primates (primates henceforth) have coexisted across cultures and contexts, and many primate populations use anthropogenic food sources as their main or supplementary food. While primates may actively forage for such food, they are also directly provisioned by humans in many regions. Ethnoprimatology views humans and primates as cohabitants of integrated socioecological spaces who mutually influence each other’s ecologies and social lives. We contextualized provisioning of primates by humans within an ethnoprimatological framework and examined if the availability of anthropogenic food affected primate diets or the amount of time primates spent in anthropogenic habitats and whether primates influenced the human act of provisioning. To this end, we used scan sampling on a group of rhesus macaques across a year, and conducted interviews with 86 people who paused at a nearby tea shop for refreshments. We found that the macaques’ consumption of natural resources and dietary diversity decreased, and they spent more time in human-modified habitats when provisioned food was available. We also found that particular behaviors of the provisioned macaques stimulated provisioning by humans. Our findings show that provisioning influences macaque feeding ecology and habitat use, and that the behavior of the macaques themselves drives people to provide them with food subsidies, illustrating a complex web of interactions between the sympatric species.     

Environmental enrichment to address behavioral differences between wild and captive black-and-white ruffed lemurs (Varecia variegata)

I compared the behaviors of wild Varecia variegata living in a Malagasy rain forest with those of caged groups living in zoos in the United Kingdom in order to design environmental enrichment to encourage more natural behaviors. Comparisons were made between wild and captive animals in terms of activity budgets (instantaneously sampled at 1-min intervals) and social and solitary behaviors, which were continuously recorded for focal individuals. I followed the same sampling protocol during behavioral enrichment experiments, with additional monitoring of the amount and type of food consumed, and with more detailed observations of feeding behavior. No significant differences were found in resting or moving between wild and captive V. variegata. However, captive V. variegata spent more time on self-grooming and social behaviors, and less time feeding than wild V. variegata. There was also a lack of manual manipulation of food items. Behavioral enrichment experiments were carried out in which whole rather than chopped fruit was provided and presented in a more naturalistic manner. With this method of dietary presentation, manual manipulation of dietary items increased. Time spent feeding also increased significantly. Captive conservation breeding programs should not be wholly concerned with maintaining a diverse gene pool-they should also be concerned with conserving species-typical behaviors, especially if they are to produce behaviorally intact captive animals that can be reintroduced to the wild with minimal training, financial resources, and loss of individuals.     

Provisioning of Young in Golden Lion Tamarins (Callitrichidae, Leontopithecus rosalia): A Test of the Information Hypothesis

Provisioning of young after weaning or fledging is a highly variable phenomenon. Among cooperative breeders, such as marmosets and tamarins, both parents and natal adults may provision immatures. Experiments designed to measure the effects of food familiarity on food-transfer interactions were conducted on zoo-living golden lion tamarin, Leontopithecus rosalia , families to test one proposed benefit of provisioning to recipient young — that immature callitrichids learn food preferences through exposure to food items obtained from older group members. Adults transferred to immatures foods that were known to adults, but novel to immatures, and foods that were novel to all more frequently than foods that were familiar to both adults and immatures. Results suggest that adults alter their behavior such that learning by immatures is fostered. Immatures also were less likely to reject new foods acquired from other group members, compared with those obtained independently, suggesting the possibility that immatures attend to food transfer to facilitate incorporation of new foods into the diet. In contrast, anecdotal accounts of wild marmoset and tamarin food transfer have indicated that infants receive from adults foods that primarily are high in lipids and/or protein, as expected if provisioning acts to supplement nutrition. These apparently contradictory findings may reflect the differing effects of the captive and wild environment on food-transfer behavior or may point to a dual function of provisioning dependent on age of the recipient.     

The puzzle-feeder as feeding enrichment for common marmosets (Callithrix jacchus): a pilot study

The use of a puzzle-feeder, as feeding enrichment, was investigated in three families of captive common marmosets (Callithrix jacchus). The study was carried out as a simultaneous choice test between two cages: one contained the puzzle-feeder, the other contained the usual food dishes, but otherwise both were arranged similarly. The monkeys were allowed to choose whether to feed from the usual dishes, or from the puzzle-feeder which required more effort. They were observed for two sessions in which they were differently motivated to feed. The enriched cage was always visited first, the marmosets managed to extract food from the puzzle-feeder, and spent more time eating from the puzzle-feeder when less hungry. These data contribute to a wider understanding on the use, and the effects, of feeding enrichments with different captive non-human primates.     

Contrafreeloading in grizzly bears: implications for captive foraging enrichment

Although traditional feeding regimens for captive animals were focused on meeting physiological needs to assure good health, more recently emphasis has also been placed on non‐nutritive aspects of feeding. The provision of foraging materials to diversify feeding behavior is a common practice in zoos but selective consumption of foraging enrichment items over more balanced “chow” diets could lead to nutrient imbalance. One alternative is to provide balanced diets in a contrafreeloading paradigm. Contrafreeloading occurs when animals choose resources that require effort to exploit when identical resources are freely available. To investigate contrafreeloading and its potential as a theoretical foundation for foraging enrichment, we conducted two experiments with captive grizzly bears (Ursus arctos horribilis). In Experiment 1, bears were presented with five foraging choices simultaneously: apples, apples in ice, salmon, salmon in ice, and plain ice under two levels of food restriction. Two measures of contrafreeloading were considered: weight of earned food consumed and time spent working for earned food. More free than earned food was eaten, with only two bears consuming food extracted from ice, but all bears spent more time manipulating ice containing salmon or apples than plain ice regardless of level of food restriction. In Experiment 2, food‐restricted bears were presented with three foraging choices simultaneously: apples, apples inside a box, and an empty box. Although they ate more free than earned food, five bears consumed food from boxes and all spent more time manipulating boxes containing apples than empty boxes. Our findings support the provision of contrafreeloading opportunities as a foraging enrichment strategy for captive wildlife. Zoo Biol 29:484–502, 2010. © 2009 Wiley‐Liss, Inc.     

Influence of Human Food Consumption on the Time Budget of Vervets

In nonhuman primate groups that utilize crop and food-raiding strategies, the inclusion of human food in the diet can have a pervasive impact on the activity budget. Human food is usually of higher quality and energy per unit than wild food. Thus, metabolic demands may be reached sooner on a human food diet, which in turn leads to improved foraging efficiency. In particular, a reduction in time spent feeding is associated with an increase in time spent resting. We investigated changes in time budget in a group of vervets (Chlorocebus aethiops pygerthrus) living in a tourist and cultivated area of Entebbe, Uganda (Zoo group). Saj collected 123 hr of focal observations on 17 individuals. Human food constituted half of the diet of Zoo group. Access to human food resulted in a high proportion of time resting and a low proportion of time feeding. The group had a small average daily range and a small home range in relation to other reports on unprovisioned groups. The time budget differences suggest that the juveniles spent more time moving and feeding and less time resting than adults did, and that adult females were more social than adult males were. These patterns have been observed in both provisioned and unprovisioned vervet groups. In contrast to a report from an unprovisioned group (Harrison, 1983), lactating females in this provisioned situation were able to maintain feeding and activity levels similar to those of other adults. However, adult females spent significantly less time consuming human food than juveniles did. We suggest that the risk associated with human food consumption may explain the low consumption of human food by females with dependent offspring. The differences may also reflect the different nutritional requirements of lactating females or the tendency for juveniles to be more exploratory than other group members.     

Effect of food preparation on feeding behavior of lion-tailed macaques

Ten group-living lion-tailed macaques (Macaca silenus), accustomed to receiving fruits and vegetable items of the diet in chopped form, were given these same foods in whole form to compare reactions to the non-nutritional properties of food. Contrary to common belief, the access of individuals to the different food items was not equalized through chopping into bite-sized morsels. Mean dietary diversity actually increased with presentation of whole foods, as did time spent feeding and total amount of food consumed. The widespread practice of chopping of food for captive primates has little to commend it in light of these findings.     

灵长类动物的食物分享行为

食物分享是灵长类动物的一种重要社会交往行为,主要发生在成体-幼体间和成体-成体之间。本文从这两个方面对灵长类动物食物分享的行为表现、特点以及功能进行总结,着重比较了无亲缘关系的成年个体间食物分享的互惠解释和骚扰解释。通过对以上内容的综合分析,进一步提出了食物分享行为的未来研究方向以及对人类合作行为演化的启示。     

Seasonal Variation in the Activity Patterns and Time Budgets of <Emphasis Type="Italic">Trachypithecus francoisi</Emphasis> in the Nonggang Nature Reserve,China

Activity patterns and time budgets are 2 important aspects of animal behavior that researchers use to investigate ecological influences on individual behavior. We collected data on activity patterns and time budgets in 1 group of François’ langurs (Trachypithecus francoisi) from August 2003 to July 2004 in the Nonggang Nature Reserve, Guangxi Province, China, via instantaneous scan sampling method with 15-min intervals. The diurnal activity pattern of François’ langurs showed morning and afternoon feeding peaks, with a midday resting peak. Seasonal change was apparent in the activity pattern: 2 significant feeding peaks occurred in the dry season and only 1 significant feeding peak in the rainy season. The group spent an average of 51.5% of the daytime resting. Feeding and moving accounted on average for 23.1% and 17.3% of the activity budget, respectively. Subjects spent little time on social activities, averaging 2% for grooming and 5.5% for playing. Their time budgets showed significant seasonal variation: they spent a greater proportion of time on feeding and less time on resting and grooming in the dry season than in the rainy season. They also differed among different sex-age classes: immatures spent more time playing, whereas adults devoted more time to resting, feeding, and grooming. Correlations between time budgets and food items or food availability clearly indicated that François’ langurs might adopt an energy-maximizing strategy when preferred foods were scarce in the dry season.     

Age-specific functions of stone handling, a solitary-object play behavior, in Japanese macaques (Macaca fuscata)

Stone handling (SH) in Japanese macaques, a form of solitary-object play, is newly acquired only by young individuals, and is the first example of a directly nonadaptive behavior that is maintained as a behavioral tradition within free-ranging provisioned social troops. We report here the first systematic investigation of this behavior in a stable captive social troop, the Takahama troop, which is housed in an outdoor enclosure of the Primate Research Institute (PRI), Kyoto University, Japan. This study was conducted to evaluate relevant competing hypotheses regarding the function of object play (e.g., misdirected foraging behavior and motor training) to explain the proximal causes and ultimate function(s) of SH. The "misdirected foraging behavior" hypothesis can be ruled out because of the lack of a clear temporal relationship between feeding and the occurrence of SH in any age class. Age-related differences in SH performance and behavioral patterns were observed, suggesting possible differences in the immediate cause and ultimate function between young and adults. Young individuals engaged in frequent bouts of short duration, involving locomotion and vigorous body actions throughout the day, which is typical for play by young in general. This pattern of behavior is consistent with the motor training hypothesis, which states that play occurs during the development of motor and perceptual skills and is thus potentially critical for neural and cognitive development. This practice is continued by those who acquire it at an early age, with adults engaging in significantly fewer but longer bouts that involve more stationary, complex manipulative patterns, almost exclusively in the late afternoon. We propose that for adults, at the proximate level SH is psychologically relaxing, but ultimately functions to maintain and regenerate neural pathways, and potentially helps to slow down the deterioration of cognitive function associated with advanced age in long-lived provisioned and captive macaques.     

黄山短尾猴食土行为

从行为生态学角度,依据黄山短尾猴食土行为在年龄、性别、社会等级序位、食土量、食土频率、食土持续时间中的分布和变化规律,结合土壤基本理化性质测定和分析,探讨了黄山短尾猴食土行为。黄山短尾猴对土壤的摄取是寻找和有目的的选择,有些场所是其"喜好"或"常去之处",食土场所通常是以多个体多次取食挖掘而形成的洞穴形式存在。取食土壤颜色黄色或黄棕色,酸性土壤,富含铁、钙、镁等矿物元素,粘土比例较高。社群各年龄段及性别个体均参与食土行为。平均食土行为持续时间在年龄和性别之间无显著差异;平均食土频率和食土量在成年雌性或雄性个体的社会等级序位之间无显著性差异;而成年雌性的平均食土频率和食土量,显著高于其它年龄或性别组,与雌性正值怀孕末期及产仔哺乳期,需要补充大量铁等矿物元素,以维持生理所需和体力消耗有关。典型的植食性动物黄山短尾猴有规律地取食粘土的行为,支持了食土行为具有"食物解毒作用"假说。人工投喂和食土行为的相关性表现为提高了食土频率,可能与粘土能够缓解高热量、低纤维人工食物造成的胃肠不适有关。     

Female feeding priority in bonobos, Pan paniscus, and the question of female dominance

The question of whether bonobos show feeding priority and female dominance has been proposed and examined, both in the wild and in captive studies, with differing results. The relationship between female dominance and female feeding priority has been best studied in prosimian primates. These studies use established criteria of females consistently evoking submissive behavior from males in dyadic encounters for determining female dominance. Although the relationship is complex, female dominance in prosimians is associated with preferential access to food. Data from studies of wild habituated bonobos in the Lomako Forest, Democratic Republic of the Congo, are examined for evidence of both female feeding priority and female social dominance using similar criteria as used for prosimians. Bonobos showed evidence of female feeding priority in small, but not in large, food patches. Male-male competition for mating opportunities at the start of the food bout was related to some, but not all, differences in time spent feeding between the sexes. Female dominance similar to that seen in prosimians was not observed in these bonobos. Males were consistently dominant in dyadic interactions. Female feeding priority with male dyadic social dominance implies that male deference during feeding cannot be excluded as one explanation of interpretations of female dominance in bonobos. Additionally, dominance of male bonobos by females appears to require the presence of female coalition partners. As in other primates with female feeding priority, bonobo females express this trait where food is economically defendable. Unlike prosimians, however, bonobo female feeding priority may result from male deference and the importance of female coalitions in nondyadic interactions.     

Effect of Group Size on Time Budgets of Sichuan Snub-Nosed Monkeys (Rhinopithecus roxellana) in Shennongjia National Nature Reserve, China

Group size influences intragroup scramble competition, which in turn influences time budgets in some primates, and may impact age–sex classes differently. There is a great deal of debate about whether folivorous primates, e.g., colobines, experience significant feeding competition. Unlike most colobines, Sichuan snub-nosed monkeys (Rhinopithecus roxellana) live in extraordinarily large groups and eat mainly lichens supplemented by seasonal plant food. We examined the effect of group size on time budgets in this species by studying two groups of different sizes in the same habitat in Shennongjia National Nature Reserve, China (study periods: August 2006–July 2008 for the larger group, November 2008–July 2009 for the smaller group). Results showed that the distribution of activities throughout the day did not differ between groups, but that time budgets did differ. Specifically, the monkeys spent more time moving and less time resting in the larger group than in the smaller group. Intergroup comparisons for each age–sex class indicated that adult females (but not adult males or juveniles) in the larger group spent more time moving and less time resting, and tended to spend more time feeding compared to those in the smaller group. The results suggested that increased scramble competition was occurring for adult females in the larger group. We provided preliminary evidence for the existence of intragroup scramble competition in Rhinopithecus roxellana.     

Response to novel objects and foraging tasks by common marmoset (Callithrix jacchus) female pairs

The authors analyze the effects of enrichment devices on the behavior of common marmoset female pairs, and determine which aspects of these devices are more likely to elicit explorative behaviors, and how their presence affects aggressive and stress-related behaviors. The results support the use of enrichment devices for captive primates and show that in marmosets, their effectiveness strongly depends on location within the enclosure and the presence of hidden food.     

The Effects of Automated Scatter Feeders on Captive Grizzly Bear Activity Budgets

Although captive bears are popular zoo attractions, they are known to exhibit high levels of repetitive behaviors (RBs). These behaviors have also made them particularly popular subjects for welfare research. To date, most research on ursid welfare has focused on various feeding methods that seek to increase time spent searching for, extracting, or consuming food. Prior research indicates an average of a 50% reduction in RBs when attempts are successful and, roughly, a 50% success rate across studies. This research focused on decreasing time spent in an RB while increasing the time spent active by increasing time spent searching for, extracting, and consuming food. The utility of timed, automated scatter feeders was examined for use with captive grizzly bears (Ursis arctos horribilis). Findings include a significant decrease in time spent in RB and a significant increase in time spent active while the feeders were in use. Further, the bears exhibited a wider range of behaviors and a greater use of their enclosure.     

The nutritional value of feeding on crops: Diets of vervet monkeys in a humanized landscape

Anthropogenic influences have dramatically altered the environments with which primates interact. In particular, the introduction of anthropogenic food sources to primate groups has implications for feeding behaviour, social behaviour, activity budgets, demography and life history. While the incorporation of anthropogenic foods can be beneficial to primates in a variety of nutritional ways including increased energetic return, they also carry risks associated with proximity to humans, such as risk of being hunted, disease risk and risk of conflict. Given such risks, we initiated a 3‐year study where we sought to understand the underlying nutritional motivations for anthropogenic food resource use by vervet monkeys (Cercopithecus aethiops) in the humanized matrix surrounding the Nabugabo Field Station in central Uganda. Feeding effort, defined as proportion of feeding scans spent on anthropogenic food, was not associated with ripe fruit availability nor with crop availability as determined by phenological monitoring. Likewise, there was no difference in the protein, fibre, or lipid composition of crop food items compared to wild food items. Individuals spent less time feeding overall in months over the 3 years with a higher proportion of time spent feeding on crop foods, suggesting a potential benefit in terms of accessibility (reduction in the proportion of activity budget devoted to feeding).