Age class differences in the feeding behavior of captive Japanese macaques (Macaca fuscataia) in the forested and nonvegetated enclosure groups

Age class differences in feeding behavior of primates are affected by many factors, including feeding competition, foraging skills, habitat type, food abundance and distribution, body mass, and food types. Two captive groups of Japanese macaques (Macaca fuscata), one housed in a forested enclosure and the other in a nonvegetated enclosure, were studied to examine the effect of environmental enrichment on age class differences in feeding behavior. Although there was no significant age class difference in time spent feeding on provisioned foods in either enclosure, the feeding rate (intake of unit food/minute) of adults consuming provisioned monkey chow was significantly higher than that of immatures in both enclosures, and was faster for both age groups in the nonvegetated than in the forested enclosure. Overall, feeding time was greatly extended for individuals of both age classes in the forested enclosure compared with their counterparts in the nonvegetated enclosure. Immatures in the forested enclosure utilized a significantly greater number of plant species and food items, exploiting many food items available among the terminal branches, and spent significantly more time feeding than adults. Perhaps constrained by larger body size, adults fed more often on the ground or middle height of the trees, likely reducing competition over plant food resources between adults and immatures. The natural vegetation played an important role in extending feeding time and segregating substrate use during feeding by adults and immatures. This study revealed the benefits concerning environmental enrichment of a naturally forested enclosure, which provides captive primates the opportunity to exhibit age class and species-typical feeding behaviors of importance for their dietary maintenance and general health.     

Encouraging natural feeding behavior in captive-bred black and white ruffed lemurs (Varecia variegata variegata)

Captive breeding of endangered species is commonly proposed as a means of conserving biodiversity. The suggestion is that captive populations can be built up to provide individuals to reinforce or re-establish wild populations. However, there is evidence to suggest that captive-bred animals lack the skills necessary for survival in their natural habitat. This research was designed to assess whether a group of captive-bred Varecia variegata variegata exhibit such behavioral deficiencies in relation to feeding behavior compared to two wild groups. A further aim was to determine which of four methods of food presentation and two captive environments were most effective in encouraging the exhibition of natural feeding behavior. An identical focal animal, instantaneous time-sampling technique was used to collect data from the wild groups in the Betampona Reserve, Madagascar, and the captive group at Chester, UK. Results from Betampona confirm the highly frugivorous and arboreal nature of V. v. variegata. Under all captive conditions, except the rooftop feed in the cage environment, the captive V. v. variegata spent significantly less time feeding than their wild conspecifics. Suspensory feeding postures are an important adaptation enabling wild V. v. variegata to harvest fruit in the small-branch setting. Similar frequencies of use of such postures to those observed at Betampona were most effectively encouraged among captive V. v. variegata in the cage environment by the rooftop food presentation method and on a naturalistic island exhibit by the suspended method of food presentation. Differences in feeding behavior between the wild and captive V. v.variegata can be explained in terms of structural differences between their environments. As naturalistic captive environments allow lemurs to experience the challenges associated with feeding in the wild, it is strongly recommended that zoos endeavor to provide them with such conditions. Zoo Biol 17:379–392, 1998. © 1998 Wiley-Liss, Inc.     

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.     

Environmental Enrichments for a Group of Captive Macaws: Low Interaction Does Not Mean Low Behavioral Changes

Environmental enrichment has been widely used to improve conditions for nonhuman animals in captivity. However, there is no consensus about the best way to evaluate the success of enrichments. This study evaluated whether the proportion of time spent interacting with enrichments indicated the proportion of overall behavioral changes. Six environmental enrichments were introduced in succession to 16 captive macaws, and interaction of the animals with them as well as the behaviors of the group were recorded before and during the enrichments. All of the enrichments affected the proportions of time spent in different behaviors. Macaws interacted more with certain items (hibiscus and food tree) than with others (a toy or swings and stairs), but introduction of the enrichments that invoked the least interaction caused as many behavioral changes as those that invoked the most. Moreover, feeding behavior was only affected by the enrichment that invoked the least interaction, a change not detected by a general analysis of enrichment effects. In conclusion, little interaction with enrichment does not mean little change in behavior, and the effects of enrichments are more complex than previously considered.     

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.     

Body weights of ruffed lemurs (Varecia variegata) in European zoos with reference to the problem of obesity

Qualitative observations in several European zoos revealed a high proportion of obese individuals in different species of lemurs. This phenomenon was examined in both subspecies of the ruffed lemur (Varecia variegata variegata and Varecia variegata rubra). Data on body weight were obtained from 43 animals in 13 European zoos and were compared with body weights of wild ruffed lemurs. The captive individuals’ mean weight was significantly higher than either of two different samples of wild V. variegata variegata. Using a weight‐based definition of obesity, 46.5% of the individuals in our sample were obese. Neither significant differences in body weight between the two subspecies nor between sexes could be found. Body weight did not correlate with age. The findings are discussed with reference to the feeding ecology of ruffed lemurs and their nutrition in captivity and to implications for captive breeding programs for this species. Zoo Biol 20:261–269, 2001. © 2001 Wiley‐Liss, Inc.     

Effects of Selected Behavioral Enrichment Devices on Behavior of Western Lowland Gorillas (Gorilla gorilla gorilla)

Environmental complexity plays an integral role in the activity and psychological well-being of primates. The experiment described in this article evaluates the effects of nonintrusive, inexpensive, and easily managed behavioral enrichment devices on the behavior of a group of captive Western lowland gorillas. Devices used included cardboard boxes containing food items, paper bags containing food items, burlap rags, and willow and maple browse. The enrichment devices increased foraging, social play, and solitary play behaviors. Sedentary behaviors decreased. Rags, bags, browse, and boxes did not statistically decrease the incidence of regurgitation/reingestation or coprophagy. Depending on the type of enrichment item used, the effects on agonism and manipulation of enrichment item were variable. To make informed management decisions about the psychological well-being of captive animals, it is important to objectively quantify and examine the influences on their behavior.     

Effects of selected behavioral enrichment devices on behavior of Western Lowland Gorillas (Gorilla gorilla gorilla)

Environmental complexity plays an integral role in the activity and psychological well-being of primates. The experiment described in this article evaluates the effects of nonintrusive, inexpensive, and easily managed behavioral enrichment devices on the behavior of a group of captive Western lowland gorillas. Devices used included cardboard boxes containing food items, paper bags containing food items, burlap rags, and willow and maple browse. The enrichment devices increased foraging, social play, and solitary play behaviors. Sedentary behaviors decreased. Rags, bags, browse, and boxes did not statistically decrease the incidence of regurgitation/reingestation or coprophagy. Depending on the type of enrichment item used, the effects on agonism and manipulation of enrichment item were variable. To make informed management decisions about the psychological well-being of captive animals, it is important to objectively quantify and examine the influences on their behavior.     

The influence of experimental manipulations on chewing speed during in vivo laboratory research in tufted capuchins (Cebus apella)

Even though in vivo studies of mastication in living primates are often used to test functional and adaptive hypotheses explaining primate masticatory behavior, we currently have little data addressing how experimental procedures performed in the laboratory influence mastication. The obvious logistical issue in assessing how animal manipulation impacts feeding physiology reflects the difficulty in quantifying mechanical parameters without handling the animal. In this study, we measured chewing cycle duration as a mechanical variable that can be collected remotely to: 1) assess how experimental manipulations affect chewing speed in Cebus apella, 2) compare captive chewing cycle durations to that of wild conspecifics, and 3) document sources of variation (beyond experimental manipulation) impacting captive chewing cycle durations. We find that experimental manipulations do increase chewing cycle durations in C. apella by as much as 152 milliseconds (ms) on average. These slower chewing speeds are mainly an effect of anesthesia (and/or restraint), rather than electrode implantation or more invasive surgical procedures. Comparison of captive and wild C. apella suggest there is no novel effect of captivity on chewing speed, although this cannot unequivocally demonstrate that masticatory mechanics are similar in captive and wild individuals. Furthermore, we document significant differences in cycle durations due to inter-individual variation and food type, although duration did not always significantly correlate with mechanical properties of foods. We advocate that the significant reduction in chewing speed be considered as an appropriate qualification when applying the results of laboratory-based feeding studies to adaptive explanations of primate feeding behaviors.     

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.     

Measuring social tolerance: An experimental approach in two lemurid primates

Social tolerance crucially affects the life of group‐living animals as it can influence, among other things, their competitive regimes, access to food, learning behavior, and recruitment. However, social tolerance tests were mainly conducted in semi‐free or captive populations, and we know little about the behavioral mechanisms and consequences of social tolerance under natural conditions. We therefore developed a co‐feeding experiment to measure social tolerance in groups of wild and captive animals across two primate species. Specifically, we recorded the social tolerance level of redfronted lemurs (Eulemur rufifrons, four wild, one captive group) and ringtailed lemurs (Lemur catta, three wild, three captive groups) by presenting a clumped food resource in an experimental arena, and recorded patterns of resource use during the experiment. Because redfronted lemurs exhibit lower levels of decided conflicts than ringtailed lemurs, we predicted that they would be socially more tolerant. The probability for an individual to feed in the arena was higher in redfronted lemurs than in ringtailed lemurs. In addition, in both species, the probability for an individual to feed in the arena was higher in the captive populations than in their wild counterparts, suggesting that proximate factors, such as a relaxation of feeding competition in captivity, may adapt species‐specific levels of social tolerance to local levels of food availability. Hence, the number of individuals co‐feeding on a valuable food resource appears to be a useful proxy of social tolerance that could be measured with this experimental setup in other wild and captive species as well.     

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.     

Effects of feeding enrichment on behavior of three species of captive bears

Bears are extremely popular among the zoo-going public, yet while many zoo exhibits have undergone dramatic design changes in recent years, most bears continue to be housed in moated grottos constructed largely of gunite. In these traditional exhibits they frequently demonstrate stereotypic locomotor patterns and are often encouraged by the public to beg. Thus, the manner in which most captive bears are exhibited does not facilitate conservation education. It is possible, however, to provide bears with opportunities to demonstrate species-typical feeding and foraging behaviors, even in standard exhibits. Subjects were four individuals of three bear species. Feeding enrichment was provided to one bear per week during three mornings during the summers of 1989 and 1990. Overall, animals were more active, less passive and less often engaged in abnormal behaviors during sessions with enrichment. Effects showed individual variation and were more profound during the second year of the study, when a greater variety of enrichment items was presented. These results suggest that simple and inexpensive methods of enrichment may have a significant, positive influence on the behavior of captive bears. © 1992 Wiley-Liss, Inc.     

Effects of three food enrichment items on the behavior of black lemurs (Eulemur macaco macaco) and Ringtail Lemurs (Lemur catta) at the Henson Robinson Zoo, Springfield, Illinois

This study tested 3 food enrichment items mentioned in a laboratory primate newsletter with 6 adult Eulemur macaco and 3 adult Lemur catta to examine whether the items would affect the behavior of the lemurs. The results suggest that Food Enrichment Item 3 (a wire box filled with whole grapes, apples, or both hidden in straw hung from a branch within the enclosure) caused a significant decrease in the incidence of resting and a significant increase in the incidences of playing and grooming, with no significant effect on the incidence of feeding or foraging. The lemurs' behavior appeared to be most affected by the food enrichment item that required the most manipulation, closely followed by an enrichment that required a moderate amount of manipulation. The order of the exposure to the food enrichment items and the day of the week appear to have an attenuation effect on these behaviors and did affect the incidence of 3 stereotypic behaviors exhibited by a male L. catta such that 3 behaviors declined in occurrence as the study progressed.     

A survey assessment of variables related to stereotypy in captive giraffe and okapi

Stereotypic behavior has been investigated in a wide variety of animals, but little published information is available on this problem in captive exotic ungulates. A survey was used to gather information on the prevalence of stereotypic behavior in giraffe and okapi and to identify variables associated with these behaviors. Of the 71 institutions that received a survey, 69.0% responded. Data were reported for 257 individuals, including 214 giraffe (representing five subspecies) and 29 okapi. Of the animals included in the survey, 79.7% performed at least one type of stereotypic behavior. Licking of non-food objects (72.4%) and pacing (29.2%) were the most prevalent stereotypic behaviors, though other stereotypies were reported in 3.2% of the animals. The results of a logistic regression performed on the data indicated that sub species, number of hours the individuals spent indoors, access at night to conspecifics, feeding frequency, method of feeding, and type of food provided were predictors of stereotypic licking. Sub species, birth history, size of the indoor enclosure, environmental change, and type of food provided were found to be significant predictors of stereotypic pacing. In general, feeding motivation appears to be related to an oral stereotypy, whereas other environmental factors appear to be associated with a locomotor stereotypy. The results of this study suggest changes in management strategies that may be empirically studied and applied to improve the well-being of captive populations of giraffe and okapi.     

Increasing foraging opportunities for a group of captive capuchin monkeys (Cebus capucinus)

Capuchin monkeys often employ complex manipulative skills while recovering food items. Five captive Cebus capucinus were presented with two identical feeders that required the monkeys to lift up flaps, search through hay, and perform coordinated hand movements in order to obtain food items. The intent of this study was not to merely increase the amount of time the animals spent feeding, but to provide opportunities for greater expression of species-typical foraging behavior. In addition to their regular diet, figs and various types of unshelled nuts were placed inside the feeders. The monkeys avidly searched for and removed food from the feeders, displaying a wide variety of manipulative abilities. The amount of time the animals spent foraging significantly increased (p less than 0.05) whereas the amount of time the animals spent locomoting and resting significantly decreased (p less than 0.05) when the feeders were available. The feeders were portable, durable, easy to clean, and relatively inexpensive.     

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.     

Can Captive-Bred Varecia variegata variegata Adapt to a Natural Diet on Release to the Wild?

We compared the diets of 3 groups of released captive-bred Varecia variegata variegata (RG1, RG2, RG3) in the Betampona Reserve to that recorded for a resident wild group, between 1998 and 2001. We investigated whether the released captive-bred Varecia, from differing captive backgrounds, could cope with seasonal changes in climate and consequently food availability, finding sufficient food to meet their nutritional requirements, and dietary choices and selection. We collected data on diet, including plant part, family, genus and, if known, species. In addition, we collected data on seasonal variation in dietary composition. Dietary overlap is significant at the familial level between RG1/RG3 and the wild group. There is some dietary overlap between RG2 and the wild group, but it is not significant. In general, RG1 and RG3 more closely followed the dietary choices and seasonal changes in diet exhibited by the wild group. We conclude that Varecia raised in free-ranging environments are better adapted to meet their nutritional requirements in the wild than those raised in cages are. However, even they struggle to deal with seasonal climatic changes and consequent changes in food availability. We suggest that future re-introduction efforts for primates include attempts to integrate released individuals rapidly into wild groups so that they can learn to cope with a seasonal environment through direct observation of wild conspecifics.     

Social Dependence of Infant Slow Lorises to Learn Diet

Nocturnal lorises and pottos (Lorisinae) are among the least gregarious of primates. Mothers start to leave their infants alone during the night as early as the day of birth. However, captive studies also indicate that weaning young lorisines closely follow their mothers nearly all the time and obtain their first solid food via scrounging. Accordingly, it has been suggested that young lorisines depend on their mothers to obtain dietary information and to achieve dietary independence by watching their mothers feeding or interacting directly with their mothers over food. We tested for a social dependence on dietary learning by infants in a social network of wild slow lorises (Nycticebus coucang). The social network included one male infant, his mother, and two subadult females. The infant only took to mouth food items that were also part of the females' diet and showed concordance in the frequency of use of food patches with the females. These results contradict dietary learning by trial and error. They indicate that dietary learning by infants depends on information obtained from older conspecifics. However, the infant was never involved in direct interactions with conspecifics over food and fed mostly alone. He was not within a distance where he could see the females feeding more often than expected from the configuration and utilization of home ranges. The infant never looked at conspecifics feeding in his vicinity, which suggests that visual observation or direct interaction over food may not be the mechanisms by which information about food resources is passed from older individuals to young, but that other ways of obtaining such information are used.     

Use of space and activity budgets in relation to age and social status in a captive herd of American bison,Bison bison

A stable herd of 11 captive American bison (Bison bison) of known ages and social rank was studied between June 18 and August 6, 1979 at the Jardin zoologique du Québec, Charlesbourg, Quebec. During the 8-week study, the first author collected scan data of predefined behaviors and locations on all individuals of the herd. Space use analysis revealed extensive occupation of (and preference for) the barn and sand mound by higher-ranking animals and calves, and the tendency for lower-ranked individuals to use alternate, lower-quality sites. Overall, the herd spent an average of 40% of the daytime resting, 25% standing, 23% feeding, and 12% walking/running and group exploring. High-ranking individuals spent significantly more time standing and walking, and less time foraging than average. Most low-ranking individuals spent significantly less time lying, and more time feeding than average. Calves spent significantly more time lying than average. The extra feeding time of low-ranking individuals occurred mostly in early morning and mid-day, when the high-ranking individuals were mostly inactive. Our results suggest differential space and time use in relation to age and social status. The effects of resource limitations caused by captivity conditions, as compared with natural conditions, are discussed in regard to the activity and movement coordination of individuals in this particular captive herd. © 1993 Wiley-Liss, Inc.