Katharine Milton

Food Choice and Digestive Strategies of Two Sympatric Primate Species

Critical determinants of dietary choice in animals may be internal rather than external and hence not readily detected by field observation. Digestive strategies of two sympatric primate species, howler monkeys (Aloutta palliata) and spider monkeys (Ateles geoffroyi), both primary consumers, were investigated by carrying out feeding trials to determine food passage rates and by examining selected aspects of gut morphology. On the average, a given marker took 20.4 + 3.5 h to first appear in the feces of howler monkeys as contrasted with a mean of 4.4 + 1.5 h for spider monkeys. Gut morphology showed that howlers had colons approximately double the size of those of spider monkeys. Howler monkeys are highly folivorous while spider monkeys are primarily frugivorous. Yet leaves are generally low in nonstructural carbohydrates while fruits are low in protein. Howlers, with their capacious hindguts and slow food passage rates, are able to ferment refractory plant parts more efficiently than spider monkeys and in this way can maximize energy returns from leaves. Conversely, spider monkeys, with smaller hindguts than howlers, are able to process greater quantities of food per unit time. In this way they can specialize on fruits, which are generally too low in protein to support howlers. Once a particular digestive strategy has evolved, with its attendant morphological, physiological, and behavioral adaptations, diet switching, at least over the short run, does not appear possible.

Nutritional Characteristics of Wild Primate Foods: Do the Diets of Our Closest Living Relatives Have Lessons for Us?

The widespread prevalence of diet-related health problems, particularly in highly industrialized nations, suggests that many humans are not eating in a manner compatible with their biology. Anthropoids, including all great apes, take most of their diet from plants, and there is general consensus that humans come from a strongly herbivorous ancestry. Though gut proportions differ, overall gut anatomy and the pattern of digestive kinetics of extant apes and humans are very similar. Analysis of tropical forest leaves and fruits routinely consumed by wild primates shows that many of these foods are good sources of hexoses, cellulose, hemicellulose, pectic substances, vitamin C, minerals, essential fatty acids, and protein. In general, relative to body weight, the average wild monkey or ape appears to take in far higher levels of many essential nutrients each day than the average American and such nutrients (as well as other substances) are being consumed together in their natural chemical matrix. The recommendation that Americans consume more fresh fruits and vegetables in greater variety appears well supported by data on the diets of free-ranging monkeys and apes. Such data also suggest that greater attention to features of the diet and digestive physiology of non-human primates could direct attention to important areas for future research on features of human diet and health.

Habitat, diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroy 1806)

Results of a 10-month study of the ecology and behavior of free- ranging woolly spider monkeys (Brachyteles arachnoides)in Brazil show that these animals are strongly folivorous. Leaf-eating accounted for more than 50% of the total feeding time in all samples but one and accounted for more than 80% of the total feeding time in three samples. Mature foliage was routinely eaten. Woolly spider monkeys consistently spend more than 50% of each day quietly resting and sleeping. Animals travel little except when actively feeding and show low levels of social interaction. Such an activity profile suggests that woolly spider monkeys may often be living near the limits of their energetic resources. The social organization of the species is unusual for a folivorous primate in that small groups of females and associated immature animals confine their activities to discrete home-range areas, whereas males are itinerant, traveling over the home ranges of various female groups. Animals sharing a common home-range area show no permanent daily pattern of association other than that of mother-dependent offspring. Foraging alone or with few conspecifics should maximize each individual’s returns from foraging by minimizing the day range that must be traveled each day to locate foods while simultaneously lowering interference competition for higher-quality dietary resources.

Physiological Ecology of Howlers (Alouatta): Energetic and Digestive Considerations and Comparison with the Colobinae

Remarkably little attention has been focused on the physiological ecology of free-ranging primates. Yet without such information, it may prove difficult to advance our understanding of factors influencing the dietary behavior of wild primates much beyond its present state. Mantled howlers (Alouatta palliata) have been studied in terms of some features of physiological ecology. Results of this work have helped to clarify some factors influencing howler and other primate food choices in the natural environment and have called into question various assumptions about leaf-eating primates. For example, though howlers eat considerable foliage, they do not exhibit a lower than predicted basal metabolic rate, nor do available data suggest that secondary compounds strongly influence howler food selection. Comparison of howlers with members of the Colobinae reveals some differences in features of their respective energetic and digestive physiology and raises timely issues for future research.

The Critical Role Played by Animal Source Foods in Human (Homo) Evolution

Wild primates take most of the daily diet from plant sources, eating moderate to small amounts of animal source foods (ASF). Plant materials make up from 87% to >99% of the annual diet of great apes, the closest living relatives of modern humans (Homo sapiens sapiens). Reflecting their close genetic relationship, gut form and nutrient requirements of apes and humans (Hominoidea) are very similar, as is their pattern of digestive kinetics-one predicated on a relatively slow turnover of ingesta. In plant-eating mammals, in contrast to carnivorous mammals, greater body size is associated with lower dietary quality. Turning to ASF as a routine rather than occasional dietary component would have permitted the evolving human lineage to evade the nutritional constraints placed on body size increases in apes. Without routine access to ASF, it is highly unlikely that evolving humans could have achieved their unusually large and complex brain while simultaneously continuing their evolutionary trajectory as large, active and highly social primates. As human evolution progressed, young children in particular, with their rapidly expanding large brain and high metabolic and nutritional demands relative to adults would have benefited from volumetrically concentrated, high quality foods such as meat. Today, many humans, particularly those in high income nations, have a variety of high quality, non-ASF dietary alternatives, but such foods were not generally available to paleolithic human ancestors nor to many people today in low income nations.

Fruiting Phenologies of Two Neotropical Ficus Species

Fruit production by 65 Ficus yoponensis and 39 F. insipida trees was scored at 2—wk intervals for 7 yr in the seasonal, semideciduous forest on Barro Colorado Island, Republic of Panama. Unlike most other tree species in this forest, which flower and fruit in synchrony at a particular time each year, some individuals of both fig species were producing fruit in all months of the study. Nevertheless, a greater amount of fruiting occurred at the beginning and near the end of the 8—mo wet season than would be expected if the two species were fruiting entirely randomly. In both species, the major fruiting peak occurred when mst other tree species were not producting ripe fruit. Large trees of both fig species tended to produce fruit crops at shorter intervals than small trees. The average interval between crops was slightly longer than a half year for F. yoponensis and slightly shorter than a full year for F. insipida. These results, combined with life history data, suggest that individuals of these two Ficus species are fruiting asynchronously at relatively short intervals, thereby increasing total lifetime fruit production and ultimately maximizing reproductive success. The flexibility shown by these two species in the timing of fruit crops appears to have coevolved with the intricate mutualism between these Ficus species and their obligately species—specific wasp pollinators.

ENERGY METABOLISM AND FOOD CONSUMPTION BY WILD HOWLER MONKEYS (ALOUATTA PALLIATA)

Rates of CO2 production in free-living and captive howler monkeys were measured using doubly labeled water, and assimilation of energy from natural foods was determined. Results permit construction of a field energy budget, and estimation of the feeding rate of these arboreal, plant-eating primates. Field metabolic rates averaged 355 kJ kg-1 day-1 (=2x basal metabolic rate). Assimilation of the energy in a fruit and leaf diet was =400o. Feeding rate in the field is estimated to be =54 g dry matter kg-1 day-1, or =90 kg dry matter ha-1 yr-1.

Hominid Dietary Selection Before Fire

Control of fire was apparently acquired rather late in the course of hominid evolution. It is therefore necessary, in the study of dietary selection by early hominids, to consider the range of plants that would have proven inedible without cooking. Some plants contain toxins or digestibility-reducing compounds, and some plant constituents are indigestible. Cooking mitigates the impact of toxins and renders complex carbohydrates more digestible. Plant foods high in cellulose and/or starch are not readily digestible uncooked, and these constituents reduce the digestibility of other nutrients. Since nutrient intake is limited by the amount of food that can be processed per unit time, non-fire-using hominids should have attempted to increase nutrient intake by minimizing intake of these carbohydrates. Unlike animal sources of protein, plant materials generally lack a full complement of amino acids, and a variety of such materials must be ingested to obtain a balance of essential amino acids. Leaves and legumes, both possible sources of essential amino acids, may be ruled out as major suppliers of them for non-fire-using hominids-leaves because of their cellulose content and legumes because of their high frequency of toxic compounds. The limitations on the availability of plant protein strengthen the inference that some animal protein was ingested by early hominids on a regular basis. A ranking of plant parts as potential foodstuffs for non-fire-using hominids is proposed. When considered in conjunction with ecological factors, such a ranking should be helpful in generating models of hominid dietary selection before fire.

Digestive Efficiencies of Wild Howler Monkeys

(1) Two sets of feeding trials were carried out on temporarily caged wild howler monkeys (Alouatta palliata) to determine digestive efficiencies with respect to cell-wall constituents and protein in natural items of diet. One trial diet consisted primarily (81%) of ripe fruit; the other consisted primarily (87%) of young leaves. (2) Samples of all foods used in the trials, as well as urine and feces, were collected and preserved. These were analyzed for total cell-wall content, cell-wall components (cellulose, hemicelluloses, lignin, cutin), and crude protein. In vitro digestibility of crude protein in trial foods was examined, using pepsin in a solution of HCl. (3) Adult howler monkeys averaged a digestive efficiency of 24% with respect to total cell-wall material on the fruit diet and 42% on the leaf diet. All animals were more efficient at degrading cellulose than hemicelluloses. In both trials fecal nitrogen content was high, and apparent digestibility of protein was low. True digestibility estimates, however, indicated that an average of 77% of dietary protein was removed in transit on the fruit diet and 89% on the leaf diet. The results of the in vitro digestibility trials indicated that tannins or their precursors are present in many natural foods of howlers. (4) It is concluded that considerable fermentation of plant structural carbohydrates takes place in the digestive tract of howler monkeys. Fermentation end products may be of particular importance to howlers at times of the year when foods rich in ready energy are in short supply.

Mating patterns of woolly spider monkeys, Brachyteles arachnoides: implications for female choice

SummaryWoolly spider monkeys show a promiscuous, polygynous mating system in which a receptive female mates with several males, often in rapid succession. Copulation is prolonged with an average duration of 4.1±1.5 (SD) min. Coitus consists of a stationary phase with the male in intromission, followed by stercotypic behaviours of the female which appear to cue and/or accompany male climax and ejaculation. Subadult and adult males show different association patterns with individual females. Subadult males form long-term consortships with particular females while adult males appear strongly attracted to a particular female only when the is receptive. These different behavior patterns of males are viewed as age-specific mating tactics. Males in a mating aggregation show little intermale aggression for sexual access to a receptive female. Large testis size in this species suggests that much intermale competition for reproductive success may be carried out at a postcopulatory level, perhaps by sperm competition. The copulatory pattern of woolly spider monkeys may function primarily as a mechanism of female choice, aiding a female in assessing the quality of males in hei mating aggregation while helping to ensure that maximal high quality spermatozoa will be available at the proper time for fertilization.