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.     

Inter-population differences in the tolerance of a marsupial folivore to plant secondary metabolites

Plant secondary metabolites (PSMs) strongly influence diet selection by mammalian herbivores. Concentrations of PSMs vary within and among plant species, and across landscapes. Therefore, local adaptations may cause different populations of herbivores to differ in their ability to tolerate PSMs. Here, we tested the food intake responses of three populations of a marsupial folivore, the common brushtail possum (Trichosurus vulpecula Kerr), from different latitudes and habitat types, to four types of PSMs. We found clear variation in the responses of northern and southern Australian possums to PSMs. Brushtail possums from southern Australia showed marked decreases in food intake in response to all four PSMs, while the two populations from northern Australia were not as sensitive and their responses did not differ from one another. These results were unexpected, based on our understanding of the experiences of these populations with PSMs in the wild. Our results suggest that geographically separated populations of possums may have evolved differing abilities to cope with PSMs, as a result of local adaptation to their natural environments. Our results provide the basis for future studies to investigate the mechanisms by which populations of mammalian species differ in their ability to tolerate PSMs.     

Playing it safe? Solitary vervet monkeys (Chlorocebus pygerythrus) choose high‐quality foods more than those in competition

An important goal in foraging ecology is to determine how biotic and abiotic variables impact the foraging decisions of wild animals and how they move throughout their multidimensional landscape. However, the interaction of food quality and feeding competition on foraging decisions is largely unknown. Here we examine the importance of food quality in a patch on the foraging decisions of wild vervet monkeys (Chlorocebus pygerythrus) at Lake Nabugabo, Uganda using a multidestination platform array. The overall nutritional composition of the vervet diet was assessed and found to be low in sodium and lipids, thus we conducted a series of experimental manipulations in which the array was varied in salt and oil content. Although vervets prioritized platforms containing key nutrients (i.e., sodium and lipids) overall, we found that solitary vervets prioritized nutrient‐dense platforms more strongly than competing vervets. This finding was opposite to those in a similar experiment that manipulated food site quantity, suggesting that large, salient rewards may be worth competing over but slight differences in nutritional density may be only chosen when there are no potentially negative social consequences (i.e., aggression received). We also found that vervets chose platforms baited with oil‐only, and oil combined with salt, but not salt‐only, suggesting that energy was an important factor in food choice. Our findings demonstrate that when wild vervets detect differences in feeding patches that reflect nutritional composition, they factor these differences into their navigational and foraging decisions. In addition, our findings suggest that these nutritional differences may be considered alongside social variables, ultimately leading to the complex strategies we observed in this study.     

Nutritional Correlates of Koala Persistence in a Low-Density Population

It is widely postulated that nutritional factors drive bottom-up, resource-based patterns in herbivore ecology and distribution. There is, however, much controversy over the roles of different plant constituents and how these influence individual herbivores and herbivore populations. The density of koala (Phascolarctos cinereus) populations varies widely and many attribute population trends to variation in the nutritional quality of the eucalypt leaves of their diet, but there is little evidence to support this hypothesis. We used a nested design that involved sampling of trees at two spatial scales to investigate how leaf chemistry influences free-living koalas from a low-density population in south east New South Wales, Australia. Using koala faecal pellets as a proxy for koala visitation to trees, we found an interaction between toxins and nutrients in leaves at a small spatial scale, whereby koalas preferred trees with leaves of higher concentrations of available nitrogen but lower concentrations of sideroxylonals (secondary metabolites found exclusively in eucalypts) compared to neighbouring trees of the same species. We argue that taxonomic and phenotypic diversity is likely to be important when foraging in habitats of low nutritional quality in providing diet choice to tradeoff nutrients and toxins and minimise movement costs. Our findings suggest that immediate nutritional concerns are an important priority of folivores in low-quality habitats and imply that nutritional limitations play an important role in constraining folivore populations. We show that, with a careful experimental design, it is possible to make inferences about populations of herbivores that exist at extremely low densities and thus achieve a better understanding about how plant composition influences herbivore ecology and persistence.     

Feeding rates of a mammalian browser confirm the predictions of a ‘foodscape’ model of its habitat

Adequate nutrition is a fundamental requirement for the maintenance and growth of populations, but complex interactions between nutrients and plant toxins make it difficult to link variation in plant quality to the ecology of wild herbivores. We asked whether a ‘foodscape’ model of habitat that uses near-infrared spectroscopy to describe the palatability of individual trees in the landscape, predicted the foraging decisions of a mammalian browser, the koala (Phascolarctos cinereus). Specifically, we considered four behavioural decision points at which nutritional quality may influence an animal’s decision. These were: which tree to enter, whether to feed from that tree, when to stop eating, and how long to remain in that tree. There were trends for koalas to feed in eucalypt trees that were more palatable than unvisited neighbouring conspecific trees, and than trees that they visited but did not eat. Koalas ate longer meals in more palatable trees, and stayed longer and spent more time feeding per visit to these trees. Using more traditional chemical analyses, we identified that an interaction between the concentrations of formylated phloroglucinol compounds (a group of plant secondary metabolites) and available N (an integrated measure of tannins, digestibility and N) influenced feeding. The study shows that foodscape models that combine spatial information with integrated measures of food quality are a powerful tool to predict the feeding behaviour of herbivores in a landscape.     

Motive for Killing: What Drives Prey Choice in Wild Predators?

Carnivorous animals are assumed to consume prey to optimise energy intake. Recently, however, studies using Nutritional Geometry (NG) have demonstrated that specific blends of macronutrients (e.g. protein, fat and in some cases carbohydrates), rather than energy per se, drive the food selection and intake of some vertebrate and invertebrate predators in the laboratory. A vital next step is to examine the role of nutrients in the foraging decisions of predators in the wild, but extending NG studies of carnivores from the laboratory to the field presents several challenges. Biologging technology offers a solution for collecting relevant data which when combined with NG will yield new insights into wild predator nutritional ecology.     

Food preferences of wild mountain gorillas

Determining the nutritional and phenolic basis of food preference is important for understanding the nutritional requirements of animals. Preference is a measure of which foods would be consumed by an animal if there was no variation in availability among food items. From September 2004 to August 2005, we measured the food preferences of four wild mountain gorilla groups that consume foliage and fruit in Bwindi Impenetrable National Park, Uganda, to determine what nutrients and phenols are preferred and/or avoided. To do so, we asked the following questions: (1) Which plant species do the gorillas prefer? (2) Considering the different plant parts consumed of these preferred species, what nutrients and/or phenols characterize them? (3) Do the nutritional and phenolic characteristics of preferred foods differ among gorilla groups? We found that although some species were preferred and others were not, of those species found in common among the different group home ranges, the same ones were generally preferred by all groups. Second, all groups preferred leaves with relatively high protein content and relatively low fiber content. Third, three out of four groups preferred leaves with relatively high sugar amounts. Fourth, all groups preferred pith with relatively high sugar content. Finally, of the two groups tested, we found that the preferred fruits of one group had relatively high condensed tannin and fiber/sugar contents, whereas the other group's preferred fruits were not characterized by any particular nutrient/phenol. Overall, there were no differences among gorilla groups in nutritional and phenolic preferences. Our results indicate that protein and sugar are important in the diets of gorillas, and that the gorillas fulfil these nutritional requirements through a combination of different plant parts, shedding new light on how gorillas balance their diets in a variable environment. Am. J. Primatol. 70:927–938, 2008. © 2008 Wiley‐Liss, Inc.     

The role of non-natural foods in the nutritional strategies of monkeys in a human-modified mosaic landscape

Many tropical animals inhabit mosaic landscapes including human-modified habitat. In such landscapes, animals commonly adjust feeding behavior, and may incorporate non-natural foods. These behavioral shifts can influence consumers' nutritional states, with implications for population persistence. However, few studies have addressed the nutritional role of non-natural food. We examined nutritional ecology of wild blue monkeys to understand how dietary habits related to non-natural foods might support population persistence in a mosaic landscape. We documented prevalence and nutritional composition of non-natural foods in monkey diets to assess how habitat use influenced their consumption, and their contribution to nutritional strategies. While most energy and macronutrients came from natural foods, subjects focused non-natural feeding activity on five exotic plants, and averaged about a third of daily calories from non-natural foods. Most non-natural food calories came from non-structural carbohydrates and least from protein. Consumption of non-natural foods related to time in human-modified habitats, which two groups used non-randomly. Non-natural and natural foods were similar in nutrients, and the amount of non-natural food consumed drove variation in nutritional strategy. When more daily calories came from non-natural foods, females consumed a higher ratio of non-protein energy to protein (NPE:P). Females also prioritized protein while allowing NPE:P to vary, increasing NPE while capitalizing on non-natural foods. Overall, these tropical mammals achieved a similar nutrient balance regardless of their intake of non-natural foods. Forest and forest-adjacent areas with non-natural vegetation may provide adequate nutrient access for consumers, and thus contribute to wildlife conservation in mosaic tropical landscapes.     

Geographic and seasonal variability in feeding behaviour of a small herbivorous rodent

Foraging strategies have traditionally been modelled as a result of food selection in response to one factor, as for instance resource availability, deterrent compounds or nutrients. Thus, a trade-off is assumed between plasticity (generalist strategy) and efficiency (specialist strategy). Nevertheless, several studies have demonstrated that animals cope behaviourally with food supply variation. For instance, desert-dwelling rodents partially compensate for nutritional bottlenecks through diet selection. The aim of our study was to test how foraging behaviour matches spatial and temporal variations in the trophic environment and how modelling hypotheses help us to understand the resultant foraging strategy. Our animal study model was the small cavy Microcavia australis, a widely distributed herbivorous rodent. Fieldwork was carried out in four places, in wet and dry seasons. We found significant differences in plant cover, plant diversity and niche breadth, and diet selection revealed a complex foraging strategy. M. australis shows a behavioural repertoire that exceeds single-criterion categories; therefore, we appeal to theoretical models that consider ecological and physiological perspectives. We classified the small cavy as a facultative specialist displaying a thoroughly opportunistic strategy based on the plasticity of the behavioural phenotype. We finally discuss the evolutionary relevance of our results and propose further investigation avenues.     

High Energy or Protein Concentrations in Food as Possible Offsets for Cyanide Consumption by Specialized Bamboo Lemurs in Madagascar

Plants producing toxic plant secondary metabolites (PSMs) deter folivores from feeding on them. Animals that can cope with noxious PSMs have a niche with a competitive advantage over other species. However, the ability to cope with toxic PSMs incurs the costs of detoxification. To assess possible compensations for the ingestion of toxic PSMs, we compare the chemical quality of plants consumed by bamboo lemurs (genera Hapalemur and Prolemur; strepsirrhine primates of Madagascar) in areas with and without bamboo. Some bamboo lemurs consume bamboo containing concentrations of cyanogenic substances 10–50 times above the average lethal dosage for mammals, and we postulate that animals consuming cyanogenic substances need supplementary protein or readily available energy for detoxification. We compared the chemical composition of food consumed by three species of bamboo lemurs that feed mainly (>80% of their time) on bamboo in the evergreen rainforest of Ranomafana (Madagascar) with published data of the diets of bamboo lemurs at two sites without highly cyanogenic plants (reed beds of Lac Alaotra and the evergreen littoral forest of Mandena) and with food of sympatric folivorous lemur species that do not feed on bamboo. Lemurs feeding on bamboo consumed up to twice as much protein as bamboo lemurs in areas without bamboo and sympatric lemur species that feed on leaves of trees. Concentrations of nonstructural carbohydrates (a source of energy) showed the opposite trend. This result supports the hypothesis that feeding on cyanogenic plants is linked to high protein intake, either as a source of protein or for sulfur-containing amino acids that can be used for detoxification. Owing to the high protein concentrations in bamboo, however, we cannot distinguish between the hypothesis that lemurs that eat bamboo target additional food items with higher protein from the hypothesis that lemurs feeding on bamboo unavoidably obtain higher concentrations of protein than animals feeding on leaves of trees, without an added nutritional benefit.     

植物次生代谢物对植食性哺乳动物营养和生理生态特征的影响

植物次生代谢物对植食性哺乳动物的营养和生理生态效应是动植物相互关系研究中的一个重要方面。本文简要介绍了植食性哺乳动物处理植物次生代谢物的一般途径,着重阐述了植物次生代谢物对植食性哺乳动物的营养和生理特征的限制方式,并对决定植食性哺乳动物处理植物次生代谢物能力差异性的相关因素进行了探讨。最后,结合国际上的研究趋势,论述了国内开展此类研究的方向和重点。     

Genotyping faeces links individuals to their diet

The detection of individual variation in foraging behaviour within wild mammal populations requires large sample sizes and relies on the multifold re-sampling of individuals. However, limits for observational studies are posed by the rarity and nocturnal or otherwise elusive habits of many mammals. We propose that the detection of foraging variation within populations of mammals may be facilitated if conventional diet analysis from faeces is combined with DNA-based individual identification methods using "genetic fingerprinting" from faeces. We applied our approach to a coyote ( Canis latrans ) population, and showed how individuals may vary from one another in their diet profiles. Two main groups of coyotes were distinguished on the basis of their relative use of small mammals and "other vertebrates" as primary food sources, and these two groups were further subdivided on the basis of their relative use of "other vertebrates" and fruit as secondary food sources. We show that, unless a faecal sampling scheme is used that maximizes the number of different individuals included in a survey, individual foraging variation that is left unaccounted for may result in downwardly biased faecal diet diversity estimates. Our approach allows the re-sampling of individuals over time and space, and thus may be generally useful for the testing of optimal foraging theory hypotheses in mammals and also has conservation applications.     

Prey use and nutritional differences between reproductive states and age classes in Atlantic spotted dolphins (Stenella frontalis) in the Bahamas

Nutritional quality of prey is a significant driver of predator foraging patterns. In mammals, nutritional needs are known to change across ontogeny and reproductive state; however, little is known about nutrition in marine mammals. For this study, we used observational data of diurnal foraging events, collected annually from 1992 to 2009, to investigate nutrition and prey use in Atlantic spotted dolphins (Stenella frontalis) on Little Bahama Bank, Bahamas, between reproductive states (lactating, pregnant, nonreproductively active [NRA]. We also investigated the impact of age class association (various calf age groups [ages 1–6], older “noncalf” juveniles, and adults) on foraging group nutrition and prey use. To obtain representative nutrient values, we measured calories, lipids, proteins, and moisture in common prey. Using nutritional values and observational data, we investigated the influence of nutritional value on prey use. Results indicated that specific nutrients were targeted by different reproductive states and age class groups. Nutritional intake of all nutrients was higher for lactating females than pregnant females, but lower than NRA females. Investigation of age group associations revealed that nutritional intake of all four nutrients was higher for noncalf than calf‐associated groups. This study represents one of the first investigations of intraspecific prey use and nutritional differences in cetaceans.     

A hot lunch for herbivores: physiological effects of elevated temperatures on mammalian feeding ecology

Mammals maintain specific body temperatures (T_b) across a broad range of ambient temperatures. The energy required for thermoregulation ultimately comes from the diet, and so what animals eat is inextricably linked to thermoregulation. Endothermic herbivores must balance energy requirements and expenditure with complicated thermoregulatory challenges from changing thermal, nutritional and toxicological environments. In this review we provide evidence that plant‐based diets can influence thermoregulation beyond the control of herbivores, and that this can render them susceptible to heat stress. Notably, herbivorous diets often require specialised digestive systems, are imbalanced, and contain plant secondary metabolites (PSMs). PSMs in particular are able to interfere with the physiological processes responsible for thermoregulation, for example by uncoupling mitochondrial oxidative phosphorylation, binding to thermoreceptors, or because the pathways required to detoxify PSMs are thermogenic. It is likely, therefore, that increased ambient temperatures due to climate change may have greater and more‐specific impacts on herbivores than on other mammals, and that managing internal and external heat loads under these conditions could drive changes in feeding ecology.     

Linking frugivore behavior to plant population dynamics

Despite the acknowledged importance of frugivores as seed dispersal agents we still lack a general understanding of the mechanisms by which these animals could shape plant populations and communities. We used a spatially explicit stochastic simulation to explore how frugivore movement decisions interact with landscape properties, thus affecting plant population dynamics through dispersal. The model simulated bird movement, foraging, seed deposition and plant recruitment. We assumed that plants lived only for one season and that recruitment was a function of local seed density. We also considered the effect of perches as non‐food landscape features. Our simulation experiments consisted in varying the parameters governing bird foraging decisions in relation to 1) how fruit abundance biased their movement, and 2) how the willingness to visit a plant or perch decreased with distance to current location. Simulated plant population dynamics was strongly influenced by bird behavior. The scale of foraging decisions had a much stronger effect on plant dynamics than biases due to fruit abundance. Birds tended to concentrate their activities in the center of the landscape where plants became more abundant, increasing local competition. The presence of perches reduced this tendency resulting in larger population sizes. The importance of perches highlights the fact that behaviors other than foraging can have a strong impact on the patterns of seed deposition and hence on plant population dynamics. Several recent studies have combined animal movement data with seed retention time in order to predict seed dispersal kernels. These studies usually emphasize the ecological implications of the scale and shape of such kernels. However, our simulation results reveal that movement directionality and the fact that birds moved mostly among plants and perches can have a major impact on plant population dynamics.     

Current perspectives in avian nutrition: domestic animal models and their role in conservation management

As biodiversity declines, wildlife conservation focuses on in situ and ex situ management strategies. Zoo-based breeding programmes are often designed to contribute to the conservation of species that are threatened in the wild. Diet contributes to the reproductive success, disease status and longevity of all animals. It is near-impossible to replicate a species' diet in captivity using only the species they consume in the wild, but the nutritional composition of a wild diet, if known, can be closely matched using commercially available foods for which the nutritional composition has been calculated. Ecological research has identified food items of importance in the diet of many species. However, the nutritional composition of these food items is rarely evaluated, even though the composition of wild food items is important in understanding the dietary adaptations and requirements of wildlife. In contrast, the nutritional requirements of domestic species are well researched and can be used to predict a range of plausible nutrient requirements of some wild species, especially those with similar life histories. Access to wild populations provides further opportunities for nutritional science to determine the requirements of individual species. Small-scale dietary experimentation undertaken at conservation institutions may show positive effects on health and welfare but is rarely published in the scientific literature. This review describes current standards in nutritional management of birds and recommends pathways for filling knowledge gaps. Research on mammals has dominated the nutrition literature, so there is a relative lack of nutritional management information for birds. We combine concepts of domestic animal nutrition with recent findings on the nutritional requirements of birds to provide a foundation for further studies of avian nutrition. We call for the broader zoological community to share data and collaborate on nutritional research to support conservation institutions in nutritional management of wild birds.     

A faecal index of diet quality that predicts reproductive success in a marsupial folivore

Estimating the nutritional value of a herbivore’s diet is difficult because it requires knowing what the animal eats, the relative quality of each component and how these components interact in relation to animal physiology. Current methods are cumbersome and rely on many assumptions that are hard to evaluate. We describe a new method for estimating relative diet quality directly from faeces that avoids the problems inherent in other methods. We combine this method with near infrared reflectance spectroscopy (NIRS) to analyse many samples and thus provide a technique with immense value in ecological studies. The method stems from the correlation between the concentrations of dietary and faecal nitrogen in herbivores eating a tannin-free diet, but a weaker relationship in browsers that ingest substantial amounts of tannins, which form complexes with proteins. These complexes reduce the availability of nitrogen and may increase faecal nitrogen concentrations. Using the tannin-binding compound, polyethylene glycol, we showed that tannin-bound nitrogen is a significant and variable part of faecal nitrogen in wild common brushtail possums (Trichosurus vulpecula). We developed a technique to measure faecal available nitrogen and found that it predicted the reproductive success of female brushtail possums in northern Australia. Faecal available nitrogen combined with NIRS provides a powerful tool for estimating the relative nutritional value of the diets of browsing herbivores in many ecological systems. It is a better indicator of diet quality than other commonly used single-nutrient measures such as faecal nitrogen and foliage analysis paired with observed feeding behaviour.     

灵长类营养生态学的研究进展

营养生态学是现代生态学领域研究动物食物数量和质量、营养适应以及营养对种群特征作用规律的分支学科.目前从营养生态学研究灵长类食性需求主要分为五种假说,1)能量最大化假说;2)氮(蛋白质)最大化假说;3)植物次级代谢产物调节假说;4)膳食纤维调节假说;5)食物营养均衡假说.本文从研究方法和研究内容分别介绍了这些假说在灵长类...     

饥饿和食物单宁酸对东方田鼠(Microtus fortis)食物摄入量和觅食行为的影响

实验室条件下,测定饥饿和食物单宁酸对东方田鼠食物摄入量和觅食行为的影响。结果表明,饥饿使实验个体的食物总摄入量增加,食物摄入率及口量大小随饥饿强度的增大而增加,而觅食频次则无显著改变,实验个体每取食回合的觅食时间呈缓慢增加的趋势,与对照组比较,觅食时间差异不显著。东方田鼠优先选择0%单宁酸食物,次为3%单宁酸食物,而对6%单宁酸食物的摄入量最少。在饥饿条件下,东方田鼠食物摄入率的增加主要源于其口量大小,觅食频次和觅摄食时间对食物摄入量增加的贡献不显著。在饥饿条件下,植食性小哺乳动物并未通过延长觅食时间,降低用于防卫、繁殖活动时间来增加食物摄入量,而是通过增加口量大小,提高其食物摄入率来满足其营养需要。验证了饥饿与植物次生化合物共同作用引起田鼠类动物生理的改变,能影响其食物摄入量及觅食行为的假设。     

Simulating cheatgrass (<Emphasis Type="Italic">Bromus tectorum</Emphasis>) invasion decreases access to food resources for small mammals in sagebrush steppe

Invasions by nonnative plants can alter the abundance of native animals, yet we know little about the mechanisms driving these changes. Shifts in vegetation characteristics resulting from nonnative plants can alter availability of food resources, predation risk, and foraging efficiency (both the access to and ability to find food), each providing a potential mechanism for documented changes in animal communities and populations in invaded systems. Cheatgrass (Bromus tectorum) is a nonnative grass that invades sagebrush steppe, resulting in declines in some small mammal populations. We examined whether changes in structural characteristics associated with cheatgrass invasion could alter foraging by small mammals, providing a potential mechanism for documented population declines. We quantified differences in vegetation structure between native and cheatgrass-invaded sagebrush steppe, then experimentally added artificial structure in native areas to simulate these differences. We placed grain at foraging stations and measured the amount removed by small mammals nightly. Adding litter at depths approximating invasion by cheatgrass reduced the average amount of grain removed in 2 of 3 study areas, but increasing stem density did not. Based on this experiment, the deeper litter created by cheatgrass invasion may increase costs to small mammals by decreasing foraging efficiency and access to existing food resources, which may explain population-level declines in small mammals documented in other studies. By isolating and identifying which structural attributes of cheatgrass invasion are most problematic for small mammals, land managers may be able to design treatments to efficiently mitigate impacts and restore invaded ecosystems.