Digesta Passage Time,Digestibility, and Total Gut Fill in Captive Japanese Macaques (<Emphasis Type="BoldItalic">Macaca fuscata</Emphasis>): Effects Food Type and Food Intake Level

Digestion is an important process in understanding the feeding ecology of animals. We examined digesta passage time, digestibility, and total gut fill in Japanese macaques (Macaca fuscata; n = 4) under 4 dietary conditions representing the seasonal and regional variations in the diets of wild populations to determine the effects of food type and food intake on these digestive features. Food type is associated with mean retention time (MRT), digestibility, and total gut fill. Dry matter intake (DMI) of food correlates positively with total gut fill but not with MRT or digestibility. Conversely, indigestible DMI affected MRT negatively. Thus, when Japanese macaques consume high-fiber foods, MRT becomes shorter and digestibility is lower than when eating low-fiber foods. Moreover, macaques experience increases in total gut fill when they consume high-fiber diets or a large amount of food. Japanese macaques may excrete difficult-to-digest food components quickly; they nevertheless buffer an increase in food intake by an increase in gut fill. Our study offers new insights into the relationship between feeding ecology and nutritional physiology in primates by simultaneously examining the effects of food type and intake level on MRT and digestibility.     

Sex differences in the stone tool-use behavior of a wild population of burmese long-tailed macaques (Macaca fascicularis aurea)

We investigated sex differences in how Burmese long-tailed macaques (Macaca fascicularis aurea) used stone tools to open shelled food items along the shores of two islands in Laemson National Park, Thailand. Over a 2-week period in December 2009, we collected scan and focal samples on macaques when they were visible along the shores and mangroves. We found females used stones more often while feeding and used smaller tools than males. Females also processed sessile oysters more than males, whereas males processed unattached foods more than females. It was unclear which sex was overall more proficient at stone tool use, but males did perform significantly better at opening unattached food items with large pounding stones. Females also struck food items more times during tool-use bouts and at a faster rate, but no significant difference was found in average tool-use bout duration. Males processed foods slightly faster within a tool-use bout, but we were unable to detect a significant difference in the rate of food processing while foraging with tools. In summary females chipped open sessile oysters with an axing technique more than males, while males used larger stones to pound open unattached shelled food more often than females. Despite using pounding more than females, males also regularly utilized the axing technique on sessile oysters. Our results are the first assessment of sex differences in macaque stone tool use, providing a basis for comparison with tool use in other primates, and to nonfunctional forms of stone use in other macaques.     

Dietary generalists and nutritional specialists: Feeding strategies of adult female blue monkeys (Cercopithecus mitis) in the Kakamega Forest,Kenya

Generalist primates eat many food types and shift their diet with changes in food availability. Variation in foods eaten may not, however, match variation in nutrient intake. We examined dietary variation in a generalist‐feeder, the blue monkey (Cercopithecus mitis), to see how dietary food intake related to variation in available food and nutrient intake. We used 371 all‐day focal follows from 24 adult females (three groups) in a wild rainforest population to quantify daily diet over 9 months. We measured food availability using vegetation surveys and phenology monitoring. We analyzed >700 food and fecal samples for macronutrient content. Subjects included 445 food items (species‐specific plant parts and insect morphotypes) in their diet. Variation in fruit consumption (percentage of diet and total kcal) tracked variation in availability, suggesting fruit was a preferred food type. Fruits also constituted the majority of the diet (by calories) and some fruit species were eaten more than expected based on relative availability. In contrast, few species of young leaves were eaten more than expected. Also, subjects ate fewer young leaves (based on calories consumed) when fruit or young leaves were more available, suggesting that young leaves served as fallback foods. Despite the broad range of foods in the diet, group differences in fiber digestibility, and variation that reflected food availability, subjects and groups converged on similar nutrient intakes (grand mean ± SD: 637.1 ± 104.7 kcal overall energy intake, 293.3 ± 46.9 kcal nonstructural carbohydrate, 147.8 ± 72.4 kcal lipid, 107.8 ± 12.9 kcal available protein, and 88.1 ± 17.5 kcal structural carbohydrate; N = 24 subjects). Thus, blue monkeys appear to be food composition generalists and nutrient intake specialists, using flexible feeding strategies to regulate nutrient intake. Findings highlight the importance of simultaneously examining dietary composition at both levels of foods and nutrients to understand primate feeding ecology.     

Seasonal variations in the activity budget of Japanese macaques in the coniferous forest of Yakushima: effects of food and temperature

Seasonal variations in the activity budget of Japanese macaques in the coniferous forest of Yakushima were studied over the course of 1 year. On an annual basis, they spent 38% of the daytime feeding, 16% traveling, 14% in social interactions, and 32% engaged in resting. The effects of temperature and food-related factors (i.e., food distribution, feeding speed, and food abundance) on the seasonal variations of activity budget were examined by stepwise multiple regression analysis. When the temperature was low, the macaques decreased traveling and feeding time, in accordance with the prediction that endothermal animals save energy under severe thermoregulatory cost. When the feeding speed of available foods was slow, they spent more time feeding. When high-quality foods were abundant, they decreased feeding time. These macaques did not respond to fluctuations in food distribution. The present results indicate the importance of temperature, in addition to food-related factors, as a determinant of activity budgets.     

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.     

Effects of Food Type and Number of Feeding Sites in a Tree on Aggression During Feeding in Wild <Emphasis Type="Italic">Macaca fuscata</Emphasis>

It is important to understand the effects of ecological factors on aggression during feeding in order to link habitat characteristics to competitive regime and social relationships. Multiple habitat characteristics are likely to affect aggression, but few researchers have examined the effect of multiple factors on intragroup competition simultaneously. I examined the effect of 8 factors on aggression during feeding in wild Japanese macaques living in a coniferous forest in Yakushima: density of the tree species, feeding time, number of feeding sites within a feeding tree, number of cofeeding animals, intratree macaque density, food type, and rank and age of the focal individual. When macaques cofed with other individuals, food type, the number of feeding sites, and their interactions significantly influenced aggression. Aggression increased when macaques ate fruits/seeds versus other foods and as the number of feeding sites decreased. Primate socioecological models highlight the importance of clumped distribution of food patches as a correlate of intragroup contest. However, my study indicates that primatologists need to pay attention to the factors related to the current feeding tree—food type and feeding tree size with respect to monopolizability—in addition to the distribution of food in the entire home range.     

You Are What You Eat: Food Limitation Affects Reproductive Fitness in a Sexually Cannibalistic Praying Mantid

Resource limitation during the juvenile stages frequently results in developmental delays and reduced size at maturity, and dietary restriction during adulthood can affect longevity and reproductive output. Variation in food intake can also result in alteration to the normal pattern of resource allocation among body parts or life-history stages. My primary aim in this study was to determine how varying juvenile and/or adult feeding regimes affect particular female and male traits in the sexually cannibalistic praying mantid Pseudomantis albofimbriata. Praying mantids are sit-and-wait predators whose resource intake can vary dramatically depending on environmental conditions within and across seasons, making them useful for studying the effects of feeding regime on various facets of reproductive fitness. In this study, there was a significant trend/difference in development and morphology for males and females as a result of juvenile feeding treatment, however, its effect on the fitness components measured for males was much greater than on those measured for females. Food-limited males were less likely to find a female during field enclosure experiments and smaller males were slower at finding a female in field-based experiments, providing some of the first empirical evidence of a large male size advantage for scrambling males. Only adult food limitation affected female fecundity, and the ability of a female to chemically attract males was also most notably affected by adult feeding regime (although juvenile food limitation did play a role). Furthermore, the significant difference/trend in all male traits and the lack of difference in male trait ratios between treatments suggests a proportional distribution of resources and, therefore, no trait conservation by food-limited males. This study provides evidence that males and females are under different selective pressures with respect to resource acquisition and is also one of very few to show an effect of juvenile food quantity on adult reproductive fitness in a hemimetabolous insect.     

The nature of a primary feeding habit in different age-sex classes of yellow baboons (Papio cynocephalus).

Two feeding habits of 30 baboons selected equally from five age-sex classes were studied at Mikumi National Park, Tanzania. The finding, gathering, and preparing of sedge corms and of seeds of tamarind fruit were described in detail. Adults obtained these foods faster than younger animals, although even small juveniles and weaned infants were efficient in gathering and preparing them. While gathering sedges or tamarinds, adult males sat in one place longer than others and obtained more food per sitting. Adults ate more pieces of food per minute than juveniles, but adult rates of eating did not differ by sex. The adult rate of food intake was inconsistent with the assumption of different food requirements for males and females of a species with pronounced sexual dimorphism.     

Disproportionate participation by age/sex classes in aggressive interactions between long-tailed macaques (Macaca fascicularis) and human tourists at Padangtegal monkey forest, Bali, Indonesia

We observed 420 aggressive interactions between tourists and Macaca fascicularis at the Padangtegal Wanara Wana Temple forest site in Bali, Indonesia, during the months of June and July 2001. The data collected included patterns of aggression, presence or absence of food, and demographic information on resident macaques and human visitors. Analyses of the interactions suggest that macaques respond differentially to humans according to the age/sex classes involved. Additionally, adult and subadult male macaques participated in more aggressive behaviors than expected, while adult female macaques and immatures participated in such behaviors less than expected. These variations in interaction patterns between macaques and tourists may have substantial implications for management issues and the potential for pathogen transmission.     

Alliance formation in a free-ranging troop of Japanese macaques

Alliance formations in a troop of free-ranging Japanese macaques, which had been provisioned 16 months before the present study was begun, were observed at the feeding ground for about 300 hr from April 1973 to March 1974. The patterns of alliance formations and their roles were described. The leader male had a quite unique role in his alliance formations; he allied much frequently with the aggressees and attacked the aggressors. Besides, the leader male allied more frequently with babies, yearlings, 2-year-old animals, and adult females, while he frequently attacked the 3- and 4-year-old animals and adult males. The animals who belonged to the same matrilineal group always allied with one another. Except the leader male, the troop members rather preferred to ally, except in those cases where the former diads involved their matrilineal group members, with the first aggressors. Networks of such alliance formations in relation with the social organization of Japanese macaques are discussed.     

Nutritional quality of gorilla diets: consequences of age,sex, and season

We tested the effects of age, sex, and season on the nutritional strategies of a group of mountain gorillas (Gorilla beringei) in the Bwindi Impenetrable National Park, Uganda. Through observations of food intake of individual gorillas and nutritional analyses of dietary components over different seasons and environments, we estimated nutrient intake and evaluated diet adequacy. Our results suggest that the nutritional costs of reproduction and growth affect nutrient intake; growing juveniles and adult females ate more food and more protein per kilogram of metabolic body mass than did silverbacks. The diets of silverback males, adult females, and juveniles contained similar concentrations of protein, fiber, and sugar, indicating that adult females and juveniles did not select higher protein foods than silverbacks but rather consumed more dry matter to ingest more protein. Juveniles consumed more minerals (Ca, P, Mg, K, Fe, Zn, Mn, Mo) per kilogram of body mass than adult females and silverback males, and juveniles consumed diets with higher concentrations of phosphorous, iron, and zinc, indicating that the foods they ate contained higher concentrations of these minerals. Seasonally, the amount of food consumed on a dry weight basis did not vary, but with increased frugivory, dietary concentrations of protein and fiber decreased and those of water-soluble carbohydrates increased. Energy intake did not change over the year. With the exception of sodium, gorillas ate diets that exceeded human nutrient requirements. A better understanding of the relative importance of food quantity and quality for different age–sex classes provides insights into the ways in which gorillas may be limited by food resources when faced with environmental heterogeneity.     

Life history of male Japanese macaques living on Koshima Islet

In the study of Japanese macaques, two types of male transfer between groups, defined by the age of transfer and known as bottom- or top-rank transfer, have received much attention, whereas the meaning of the period of solitary life has received very little. Male solitary life has been regarded simply as a transient state between group transfer. We found that male solitary life is restricted to a specific period in the life history of Japanese macaques living on Koshima Islet. This period started when the body weights of males and females began to diverge and ended when the body weight increase of males had stopped. Solitary lifestyle is related to the growth of adolescent and post-adolescent males. We hypothesize that a solitary lifestyle is a necessary step for adolescent and post-adolescent males to achieve their full adult growth by avoiding feeding competition with others, especially with adult females. Increments of body weight increase between 3 and 15 years were larger for the sons of lower- and middle-rank females than for those of higher-ranking females. Although the sons of lower- plus middle-ranking females grew later, they achieved a full adult body weight similar to that of sons of higher-ranking females by the age of 15. We believe that this body weight increase was achieved because of the solitary lifestyle of adolescent and post-adolescent males. Correlation between male body weight and life-span was found for body weights at 12 years, but no correlation was evident at 6 years. Electronic Publication     

Diet of a Japanese Macaque Troop in the Coniferous Forest of Yakushima

I studied the diet of a troop of Japanese macaques in the coniferous forest of Yakushima over one year via focal animal sampling. Fiber-rich foods constituted 45% of annual feeding time, and mature leaves constituted 38% of total feeding time. Feeding time on fruits and seeds was only 13% and 4%, respectively. Flowers and fungi contributed a considerable amount of annual feeding time: 15% and 14%, respectively. Their diet changed seasonally. They fed on more fruits and seeds in response to increased availability, and when these foods were not available, they ate mature leaves. When the temperature was low, they ate more herbs, possibly to save energy by not climbing trees and staying in sunny places. The results imply two dietary characteristics of the species that might relate to adaptations in temperate regions, where fruit is available during a limited season and fiber-rich foods are the only candidate of fallback food. They are capable of digesting a large amount of fiber-rich food, but at the same time they preferentially select high-quality fruits or seeds when they are available.     

Decreased food intake in reproducing lizards: A fecundity-dependent cost of reproduction?

Abstract Reproduction has been shown to be costly in viviparous skinks, both in terms of survival and in terms of growth and future reproductive output. One possible source of such costs could be a reduction in food intake, with an associated reduction in energy available for maintenance and future reproduction. Therefore, I compared food intake in male and female southern water skinks (Eulamprus tympanum), to determine whether food intake was reduced during reproduction in either sex. In addition, I measured the relationship between reduction in food intake and the total volume of offspring or testis. A reduction in food intake proportional to the volume of offspring suggests that costs associated with reduced energy intake may be fecundity dependent. Food intake was estimated using the total volume of stomach contents of individuals. Females ate significantly less (mean volume of stomach contents = 0.13mL) than males (mean = 0.36mL) just before parturition in January, when embryos were largest. After parturition, females ate significantly more than males. Otherwise, there were no significant differences between the food intake of males and females. Females reduced food intake by eating smaller food items. Females with relatively large numbers of ova or embryos ate relatively less, and therefore decreased food intake in females may be a fecundity-dependent cost of reproduction in these lizards. Males did not reduce food intake during periods when testes were enlarged and mating occurred. Decreased food intake during reproduction is probably an important source of reproductive costs to females of these viviparous lizards, but does not appear to be important in males.     

Home range structure and inter-group competition for land of Japanese macaques in evergreen and deciduous forests

The per capita home range area of Japanese macaques,Macaca fuscata, is significantly smaller in evergreen forest than in deciduous forest, though a corresponding difference in food resource utilization patterns has never been described. The present study compared the home range utilization pattern of Japanese macaques living in two habitats: the Yakushima population inhabits an evergreen forest, while the Kinkazan population inhabits a deciduous forest. We found that in the Yakushima population, (1) food density was higher; (2) inter-feeding bout sites distance was shorter; (3) daily travel distance was shorter; (4) home range size was smaller; and (5) the unit value of the main home range was higher, than in the Kinkazan population. Yakushima groups utilized a small home range area intensively, compared to Kinkazan groups. We also found that a Yakushima group shared 24% of its main home range with neighboring groups, though a Kinkazan group shared only 10% with other groups. It is supposed that food distribution affects daily ranging pattern, and ultimately the social relationships between groups in Japanese macaques.     

The GLP-1 agonist exendin-4 reduces food intake in nonhuman primates through changes in meal size

Exendin-4 (Ex4), a long-acting glucagon-like peptide-1 (GLP-1) receptor agonist, has been shown to reduce food intake and suppress gastric emptying in rodents and humans. In this study we investigated the effects of peripheral administration of Ex4 on food intake and meal patterns in adult male rhesus macaques. Rhesus macaques (n = 4) that had been trained to lever press for food pellets were injected intramuscularly 15 min before the start of their 6-h daily feeding period. Ex4 was given at doses of 0.10, 0.32, 0.56, 1.0, and 3.0 microg/kg. Ex4 suppressed food intake in a dose-dependent manner, with the 3.0 microg/kg dose completely preventing feeding during the 6-h period and the 0.10 microg/kg dose suppressing intake by 17%. Doses of 0.32, 0.56, 1.0, and 3.0 microg/kg caused significant reductions in cumulative intake at all six hourly time points. Ex4 inhibited food intake through a specific effect on meal size. Meal size was significantly reduced in a dose-dependent manner with significant reductions at the 0.32 and 1.0 microg/kg doses (P < 0.05). Day 2 and 3 intakes returned to baseline levels with no compensation for Ex4-induced feeding suppression. Administration of doses of 0.32 and 0.56 microg/kg Ex4 over 5 consecutive days led to sustained reductions in intake with no evidence of compensation. Again, these reductions were due to specific effects on meal size. These results demonstrate that activation of GLP-1 pathways has potent effects on the controls of meal size and overall food intake in a nonhuman primate model.     

Radio tracking of a male Japanese macaque emigrated from its group

A male Japanese macaque's ranging behavior before and after emigration from its group was investigated by using radiotelemetry techniques. The male's locations before leaving the troop were regarded as those of the troop, while those after leaving were regarded as those of a solitary male. Monthly home range sizes of the male with the troop were larger than those of the male moving alone, while the whole home range of the male with the troop for three months was much smaller than that of the male moving alone for five months. Overlaps between the male's home ranges with the troop between months were much greater than those between the ranges of the male moving alone. One neighboring troop's home range overlapped the male's range in August and September, and another neighboring troop's range overlapped the male's in October. The mean travel distance and speed of the male with the troop per day did not differ significantly from those of the male moving alone. The results suggest that emigrated males of Japanese macaques may visit home ranges of some troops and stay for a while without interacting troop monkeys before they decide to visit or join the troops.     

Interannual Variation in Nut Abundance Is Related to Agonistic Interactions of Foraging Female Japanese Macaques (Macaca fuscata)

The importance of dominance status to foraging and ultimately survival or reproductive success in wild primates is known; however, few studies have addressed these variables simultaneously. We investigated foraging and social behavior among 17 adult female Japanese macaques (Macaca fuscata) on Kinkazan Island, northern Japan, from September to November in 2 consecutive years (2004 and 2005) to determine whether interannual variation in food availability was related to variation in agonistic interactions over food resources and the feeding behavior of individuals of different dominance rank. We compared energy obtained with daily energy requirements and also examined the effect of variation in feeding behavior on female survival and reproductive success. Fruiting conditions differed considerably between the 2 yr: of four nut-producing species, the nuts of only Torreya nucifera fruited in 2004, whereas all four species, particularly Fagus crenata, produced nuts in abundance in 2005. The abundance and average crown size of trees of Torreya nucifera were smaller than those of Fagus crenata, and there was a higher frequency of agonistic interactions during 2004, when dominant, but not subordinate, individuals were able to satisfy daily energy requirements from nut feeding alone through longer nut feeding bouts. In contrast, all macaques, regardless of their dominance rank, were able to satisfy their energy requirements by feeding on nuts in 2005. Subordinate macaques appeared to counter their disadvantage in 2004 by moving and searching for food more and maintaining larger interindividual distances. Several lower-ranking females died during the food-scarce season of 2004, and only one dominant female gave birth the following birth season. In contrast, none of the adult females died during the food-scarce season of 2005, and 12 females gave birth the following birth season. These findings suggest that an interaction between dominance rank and interannual variation in food availability are related to macaque behavior, survival, and reproduction.     

A pilot study on the ontogeny of digestive physiology in Japanese macaques (Macaca fuscata)

An assumption based on the Jarman–Bell principle suggests a positive relationship between body size and the digestive efficiency in animals, where smaller animals are less effective at digesting fibrous food due to shorter digesta passage. To examine the effect of body size within a species and explore a potential physiological background of ontogenetic diet shifts, we measured food intake, digestibility, digesta passage and gut fill in nine Japanese macaques, including three juveniles/subadult animals. Although these three showed a comparable digestive efficiency as the older animals on a low-fiber diet, they did not achieve the long retention times of adults in spite of similar levels of indigestible food intake and gut capacity. While the limited sample size would not allow generalized conclusions on ontogenetic digestive development in primates, this study suggests additional, yet unexplored effects other than food intake, digestion and gut capacity on digesta retention during ontogeny.     

Effect of ketamine anesthesia on daily food intake in Macaca mulatta and Cercopithecus aethiops

Ketamine hydrochloride is frequently administered to non-human primates as a means of chemical restraint. This procedure can be a frequent source of stress to monkeys at research facilities, impacting animal health, well-being and research quality. This study was designed to measure ketamine's effect on daily food intake, a parameter that reflects and influences animal well-being and directly impacts research studies. On five occasions, baseline daily food intake was compared to daily food intake occurring 24, 48, 72, 96, and 120 h after an intramuscular injection of 10 mg/kg ketamine in male African green monkeys (AGMs) (Cercopithecus aethiops) and male and female rhesus macaques (Macaca mulatta). AGMs and female rhesus macaques had significantly reduced daily food intake during the first 4 days after receiving ketamine. The AGMs continued to display significantly reduced daily food intake on the fifth day after ketamine. The male rhesus macagues showed a trend toward reduced daily food intake, greatest during the first 2 days and remaining less than baseline intake through the fifth day following ketamine. The degree of observed food intake reduction was most severe at the 24 h (mean percent intake reduction: AGMs: 57%; rhesus males: 48%; rhesus females: 40%) and 48 h time points (AGMs: 24%; rhesus males: 14%; rhesus females: 13%). A subset of the AGMs that did not receive ketamine, but observed other animals in the room receive ketamine, showed reduced food intake at 24 and 48 h after ketamine, though not to the degree associated with ketamine administration. These results indicate that ketamine anesthesia is associated with a prolonged reduction in daily food intake in AGMs and rhesus macaques. Frequent use of ketamine in non-human primates may have a significant impact on animal health and well-being, and alternatives to its use warrant consideration.