Fallback Foods Research Articles

Fallback foods of temperate‐living primates: A case study on snub‐nosed monkeys

Only a few primate species thrive in temperate regions characterized by relatively low temperature, low rainfall, low species diversity, high elevation, and especially an extended season of food scarcity during which they suffer from dietary stress. We present data of a case study of dietary strategies and fallback foods in snub-nosed monkeys (Rhinopithecus bieti) in the Samage Forest, Northwest Yunnan, PRC. The snub-nosed monkeys adjusted intake of plant food items corresponding with changes in the phenology of deciduous trees in the forest and specifically showed a strong preference for young leaves in spring. A non-plant food, lichens (Parmeliaceae), featured prominently in the diet throughout the year (annual representation in the diet was about 67%) and became the dominant food item in winter when palatable plant resources were scarce. Additional highly sought winter foods were frost-resistant fruits and winter buds of deciduous hardwoods. The snub-nosed monkeys' choice of lichens as a staple fallback food is likely because of their spatiotemporal consistency in occurrence, nutritional and energetic properties, and the ease with which they can be harvested. Using lichens is a way to mediate effects of seasonal dearth in palatable plant foods and ultimately a key survival strategy. The snub-nosed monkeys' fallback strategy affects various aspects of their biology, e.g., two- and three-dimensional range use and social organization. The higher abundance of lichens at higher altitudes explains the monkeys' tendency to occupy relatively high altitudes in winter despite the prevailing cold. As to social organization, the wide temporal and spatial availability of lichens strongly reduces the ecological costs of grouping, thus allowing for the formation of "super-groups." Usnea lichens, the snub-nosed monkeys' primary dietary component, are known to be highly susceptible to human-induced environmental changes such as air pollution, and a decline of this critical resource base could have devastating effects on the last remaining populations. Within the order Primates, lichenivory is a rare strategy and only found in a few species or populations inhabiting montane areas, i.e., Macaca sylvanus, Colobus angolensis, and Rhinopithecus roxellana. Other temperate-dwelling primates rely mainly on buds and bark as winter fallback foods.

Shallow‐water habitats as sources of fallback foods for hominins

Underground storage organs (USOs) have been proposed as critical fallback foods for early hominins in savanna, but there has been little discussion as to which habitats would have been important sources of USOs. USOs consumed by hominins could have included both underwater and underground storage organs, i.e., from both aquatic and terrestrial habitats. Shallow aquatic habitats tend to offer high plant growth rates, high USO densities, and relatively continuous USO availability throughout the year. Baboons in the Okavango delta use aquatic USOs as a fallback food, and aquatic or semiaquatic USOs support high-density human populations in various parts of the world. As expected given fossilization requisites, the African early- to mid-Pleistocene shows an association of Homo and Paranthropus fossils with shallow-water and flooded habitats where high densities of plant-bearing USOs are likely to have occurred. Given that early hominins in the tropics lived in relatively dry habitats, while others occupied temperate latitudes, ripe, fleshy fruits of the type preferred by African apes would not normally have been available year round. We therefore suggest that water-associated USOs were likely to have been key fallback foods, and that dry-season access to aquatic habitats would have been an important predictor of hominin home range quality. This study differs from traditional savanna chimpanzee models of hominin origins by proposing that access to aquatic habitats was a necessary condition for adaptation to savanna habitats. It also raises the possibility that harvesting efficiency in shallow water promoted adaptations for habitual bipedality in early hominins.

Indentation as a technique to assess the mechanical properties of fallback foods

A number of living primates feed part-year on seemingly hard food objects as a fallback. We ask here how hardness can be quantified and how this can help understand primate feeding ecology. We report a simple indentation methodology for quantifying hardness, elastic modulus, and toughness in the sense that materials scientists would define them. Suggested categories of fallback foods-nuts, seeds, and root vegetables-were tested, with accuracy checked on standard materials with known properties by the same means. Results were generally consistent, but the moduli of root vegetables were overestimated here. All these properties are important components of what fieldworkers mean by hardness and help understand how food properties influence primate behavior. Hardness sensu stricto determines whether foods leave permanent marks on tooth tissues when they are bitten on. The force at which a food plastically deforms can be estimated from hardness and modulus. When fallback foods are bilayered, consisting of a nutritious core protected by a hard outer coat, it is possible to predict their failure force from the toughness and modulus of the outer coat, and the modulus of the enclosed core. These forces can be high and bite forces may be maximized in fallback food consumption. Expanding the context, the same equation for the failure force for a bilayered solid can be applied to teeth. This analysis predicts that blunt cusps and thick enamel will indeed help to sustain the integrity of teeth against contacts with these foods up to high loads.

Fallback foraging as a way of life: Using dietary toughness to compare the fallback signal among capuchins and implications for interpreting morphological variation

The genus Cebus is one of the best extant models for examining the role of fallback foods in primate evolution. Cebus includes the tufted capuchins, which exhibit skeletal features for the exploitation of hard and tough foods. Paradoxically, these seemingly "specialized" taxa belong to the most ubiquitous group of closely related primates in South America, thriving in a range of different habitats. This appears to be a consequence of their ability to exploit obdurate fallback foods. Here we compare the toughness of foods exploited by two tufted capuchin species at two ecologically distinct sites; C. apella in a tropical rainforest, and C. libidinosus in a cerrado forest. We include dietary data for one untufted species (C. olivaceus) to assess the degree of difference between the tufted species. These data, along with information on skeletal morphology, are used to address whether or not a fallback foraging species exhibits a given suite of morphological and behavioral attributes, regardless of habitat. Both tufted species ingest and masticate a number of exceedingly tough plant tissues that appear to be used as fallback resources, however, C. libidinosus has the toughest diet both in terms of median and maximal values. Morphologically, C. libidinosus is intermediate in absolute symphyseal and mandibular measurements, and in measures of postcranial robusticity, but exhibits a higher intermembral index than C. apella. We propose that this incongruence between dietary toughness and skeletal morphology is the consequence of C. libidinosus' use of tools while on the ground for the exploitation of fallback foods.

The importance of fallback foods in primate ecology and evolution

The role of fallback foods in shaping primate ranging, socioecology, and morphology has recently become a topic of particular interest to biological anthropologists. Although the use of fallback resources has been noted in the ecological and primatological literature for a number of decades, few attempts have been made to define fallback foods or to explore the utility of this concept for primate evolutionary biologists and ecologists. As a preface to this special issue of the American Journal of Physical Anthropology devoted to the topic of fallback foods in primate ecology and evolution, we discuss the development and use of the fallback concept and highlight its importance in primatology and paleoanthropology.

Foraging and ranging behavior during a fallback episode: Hylobates albibarbis and Pongo pygmaeus wurmbii compared

Periodic episodes of food scarcity may highlight the adaptive value of certain anatomical traits, particularly those that facilitate the acquisition and digestion of exigent fallback foods. To better understand the selective pressures that favored the distinctive dental and locomotor morphologies of gibbons and orangutans, we examined the foraging and ranging behavior of sympatric Hylobates albibarbis and Pongo pygmaeus wurmbii during an episode of low fruit availability at Tuanan, Kalimantan Tengah, Indonesia. We found that Hylobates ranged 0.5 km day(-1) or 33% farther than did Pongo, but the overall daily ranging of both species did not vary as fruit availability decreased by as much as 50%. Among gibbons, we observed dietary switching to fallback foods; in particular, there was a progressively greater reliance on figs, liana products, and unripe fruit. Orangutans relied heavily on unripe fruit and fracture-resistant bark and pith tissues. Despite these divergent fallback patterns, the stiffness of fruit mesocarp consumed by Hylobates and Pongo did not differ. We discuss canine and molar functional morphology with respect to dietary mechanics. Next, to contextualize these results, we discuss our findings with respect to forest structure. The rain forests of Southeast Asia have been described as having open, discontinuous canopies. Such a structure may inform our understanding of the ranging behavior and distinctive locomotion of apes in the region, namely richochetal brachiation and quadrumanous clambering. Our approach of integrating behavioral ecology with physical measures of food may be a powerful tool for understanding the functional adaptations of primates.

Male and female western gorilla diet: Preferred foods, use of fallback resources, and implications for ape versus old world monkey foraging strategies

Most of what is currently known about western gorilla (Gorilla gorilla) diet is based on indirect studies using fecal samples and trail signs rather than measures based on direct observations. Here we report results on adult male and female western gorilla foraging behavior, based on systematic focal observations and nutritional analyses of foods. We found that western gorillas, like other apes, are highly selective ripe fruit specialists, seeking fruit high in energy, low in antifeedants, and rare in the environment. During seasonal fruiting peaks, fruit accounted for up to 70% of feeding time. When ripe fruit was scarce, gorillas increased time spent feeding on leaves and nonpreferred fruits and herbs. Leaves were the major fallback food, accounting for up to 70% of feeding time in males and 50% in females during periods of fruit scarcity. In spite of large differences in body size, the sexes were remarkably similar in their overall diet, not differing in time spent feeding on fruit or preferred herbs. However, the male consistently fed more often and on a greater variety of leaves than did females, whereas females fed more often on fallback herbs and termites. Our findings, when considered in light of previous findings on sympatric mangabeys, indicate that the foraging strategy of western gorillas is broadly similar to that of chimpanzees and orangutans, and distinct from that of old world monkeys.

Summary to the symposium issue: Primate fallback strategies as adaptive phenotypic plasticity—Scale, pattern, and process

In this discussion, I evaluate our understanding of fallback foods in primate and hominin ecology and evolution with reference to the challenges of nomenclature, scale, and of linking individual responses to food availability and properties (process) to species traits (pattern). I use these challenges to form the framework of my discussion and ultimately conclude that we situate the discussion of primate fallback strategy into a broader, "synthetic" framework of animal form and the evolutionary significance of phenotypic plasticity.

The influence of fallback foods on great ape tooth enamel

Lucas and colleagues recently proposed a model based on fracture and deformation concepts to describe how mammalian tooth enamel may be adapted to the mechanical demands of diet (Lucas et al.: Bioessays 30 2008 374-385). Here we review the applicability of that model by examining existing data on the food mechanical properties and enamel morphology of great apes (Pan, Pongo, and Gorilla). Particular attention is paid to whether the consumption of fallback foods is likely to play a key role in influencing great ape enamel morphology. Our results suggest that this is indeed the case. We also consider the implications of this conclusion on the evolution of the dentition of extinct hominins.

Proceedings of the Seventy‐Eighth Meeting of the American Association of Physical Anthropologists, The Sheraton Chicago Hotel, Chicago, Illinois, April 1–4, 2009

American Journal of Physical AnthropologyVolume 140, Issue 4 p. 771-787 Proceedings Proceedings of the Seventy-Eighth Meeting of the American Association of Physical Anthropologists, The Sheraton Chicago Hotel, Chicago, Illinois, April 1–4, 2009 First published: 03 November 2009 https://doi.org/10.1002/ajpa.21219Citations: 1AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Citing Literature Volume140, Issue4Special Issue: The Importance of Fallback Foods in Primate Ecology and EvolutionDecember 2009Pages 771-787 RelatedInformation

Using carbon isotopes to track dietary change in modern, historical, and ancient primates

Stable isotope analysis can be used to document dietary changes within the lifetimes of individuals and may prove useful for investigating fallback food consumption in modern, historical, and ancient primates. Feces, hair, and enamel are all suitable materials for such analysis, and each has its own benefits and limitations. Feces provide highly resolved temporal dietary data, but are generally limited to providing dietary information about modern individuals and require labor-intensive sample collection and analysis. Hair provides less well-resolved data, but has the advantage that one or a few hair strands can provide evidence of dietary change over months or years. Hair is also available in museum collections, making it possible to investigate the diets of historical specimens. Enamel provides the poorest temporal resolution of these materials, but is often preserved for millions of years, allowing examination of dietary change in deep time. We briefly discuss the use of carbon isotope data as it pertains to recent thinking about fallback food consumption in ancient hominins and suggest that we may need to rethink the functional significance of the australopith masticatory package.

Orangutans

Orangutans

The effects of extreme seasonality of climate and day length on the activity budget and diet of semi‐commensal chacma baboons (Papio ursinus) in the Cape Peninsula of South Africa

We examined the effects of extreme seasonality on the activity budget and diet of wild chacma baboons with access to a high-quality, human-derived food source. The Cape Peninsula of South Africa is unusual among nonhuman primate habitats due to its seasonal extremes in day length and climate. Winter days are markedly shorter and colder than summer days but have higher rainfall and higher primary production of annually flowering plants. This combination of fewer daylight hours but higher rainfall is substantially different from the ecological constraints faced by both equatorial baboon populations and those living in temperate climates with summer rainfall. We sought to understand how these seasonal differences affect time budgets of food-enhanced troops in comparison to both other food-enhanced troops and wild foraging troops at similar latitudes. Our results revealed significant seasonal differences in activity budget and diet, a finding that contrasts with other baboon populations with access to high-return anthropogenic foods. Similar to nonprovisioned troops at similar latitudes, troop members spent more time feeding, socializing, and traveling during the long summer days compared to the short winter days, and proportionately more time feeding and less time resting in summer compared to winter. Summer diets consisted mainly of fynbos and nonindigenous foods, whereas winter diets were dominated by annually flowering plants (mainly grasses) and ostrich pellets raided from a nearby ostrich farm. In this case, food enhancement may have effectively exaggerated seasonal differences in activity budgets by providing access to a high-return food (ostrich pellets) that was spatially and temporally coincident with abundant winter fallback foods (grasses). The frequent use of both alien vegetation and high-return, human-derived foods highlights the dietary flexibility of baboons as a key element of their overall success in rapidly transforming environments such as the South African Cape Peninsula.

Feeding outside the Forest: The Importance of Crop Raiding and an Invasive Weed in the Diet of Gallery Forest Ring-Tailed Lemurs (Lemur catta) following a Cyclone at the Beza Mahafaly Special Reserve, Madagascar

In January 2005, a cyclone hit southern Madagascar, including the Beza Mahafaly Special Reserve, disrupting the flowering/fruiting cycle of Tamarindus indica, leaving Lemur catta without its major food resource during reproductive periods. We studied two adjacent groups of L. catta during the late gestation period, and both groups ventured outside the reserve to feed. The Red group (RG) fed daily on cultivated sweet potato (Ipomoea batatas) leaves in a nearby field, and both groups consumed leaves and stems of the invasive terrestrial flowering herb Mexican prickly poppy (Argemone mexicana), growing outside the reserve. The Green group (GG) spent significantly more time feeding than did RG, and more time feeding inside the forest compared to outside. The members of RG spent half of their time feeding in the crops, and nearly half of their diet consisted of easy-to-process sweet potato leaves. Additionally, RG defended and restricted GG’s access to the crop territory. Of the two non-forest foods, A. mexicana leaves were higher in protein and most minerals (P, Mg, K and Na, but not Ca) and lower in fiber than sweet potato leaves, but sweet potato leaves were preferred by RG. L. catta is a markedly flexible primate with respect to diet, and switches to fallback foods from outside the forest during periods of low food availability. In the highly seasonal and unpredictable climate of southern Madagascar, such behavioral adaptations are important to the survival of this species.

Brief communication: Puncture and crushing resistance scores of Tana river mangabey (Cercocebus galeritus) diet items

Cercocebus mangabeys are characterized by dental traits that have been interpreted as adaptations to eat hard diet items. Although there are data that mangabeys include a large proportion of fruit and especially seeds in their diets, no hardness measurements have been done on mangabeys' food items. This study measured puncture and crushing resistance of food items in the diet of the Tana River mangabey (C. galeritus). Feeding data were collected by the use of scan samples from one mangabey group from August 2000 to July 2001 and from July 2005 to June 2006. Food items were collected during the latter period only, and from the same tree in or under which mangabeys had been observed eating. A portable agricultural fruit tester was used to measure the puncture resistance of fruit and a valve spring tester was used to measure the crushing resistance of seeds. The average puncture resistance of fruit was 1.7 kg/mm(2), and the average crushing resistance of seeds was 12.8 kg. There were no correlations between puncture resistance, crushing resistance, or all resistance scores and frequency contribution to the diet. Resistance scores measured in this study were within the range of hardness scores of fruit and exceeded hardness scores of seeds eaten by other hard object feeders. Although this study supports the interpretation that Cercocebus dental traits are adaptations to hard object feeding, future research should investigate other material properties of food, as well as the role hard diet items play in niche separation and as fallback foods.

Factors Influencing Interannual and Intersite Variability in the Diet of Trachypithecus francoisi

Comparative studies of the diet of the same species in different habitats, and over the long term, are essential to understanding a species’ behavioral and ecological plasticity. Moreover, such studies can help researchers and managers evaluate a species’ capacity to cope with changes in habitat quality resulting from natural processes or human disturbance, which is important for developing conservation strategies. We compared dietary data for Francois’ langur (Trachypithecus francoisi) collected at Nonggang and Fusui Nature Reserves, Guangxi Province, China, over 2 separate study periods to evaluate interannual and intersite variation in diet. Young leaves were the preferred staple foods for langurs, whereas mature leaves and seeds served as fallback foods in response to seasonal shortage in the abundance of young leaves. Species composition of the diets and the percentage of feeding records for plant species varied between the 2 study periods. The langurs at both study sites fed selectively, and they did not base their diet simply on the abundance of plant species in the habitat. However, the plant species eaten by langur groups inhabiting the 2 different reserves were markedly different, and the top 10 food species eaten by the Fusui group showed no overlap with those eaten by the Nonggang group. The variation may be related to differences in forest composition resulting from different level of human disturbance. In summary, our results indicate that Francois’ langurs exhibit a comparable dietary pattern both temporally and geographically, but there is marked interannual and intersite difference in species composition of the langur diet.

Chimpanzee seed dispersal quantity in a tropical montane forest of Rwanda

We describe chimpanzee seed dispersal in the tropical montane forest of Nyungwe National Park (NNP), Rwanda, for a total of three years from January 1998 through May 2000 and May 2006 through March 2007. Relatively few studies have examined chimpanzee seed dispersal in montane communities where there are generally fewer fruiting tree species than in lowland forests. Such studies may reveal new insights into chimpanzee seed dispersal behaviors and the role that they play in forest regeneration processes. Chimpanzees are large-bodied, highly frugivorous, and tend to deposit the seeds of both large- and small-seeded fruits they consume in a viable state. We found that chimpanzees dispersed a total of 37 fruiting species (20 families) in their feces, 35% of which were large-seeded trees (> or =0.5 cm). A single large-seeded tree, Syzygium guineense, was the only species to be dispersed in both wadges and feces. Based on phenological patterns of the top five large-seeded tree species found in chimpanzee feces, our results indicate that chimpanzees do not choose fruits based on their availability. There was, however, a positive relationship between the presence of Ekebergia capensis seeds in chimpanzee feces and S. guineense seeds in chimpanzee wadges and their respective fruit availabilities. Our data reveal that proportionately fewer chimpanzee fecal samples at NNP contained seeds than that reported in two other communities in the Albertine Rift including one at mid-elevation and one in montane forest. As in other chimpanzee communities, seeds of Ficus spp. were the most common genus in NNP chimpanzee feces. Our data do not support previous studies that describe Ficus spp. as a fallback food for chimpanzees and highlights an intriguing relationship between chimpanzees and the large-seeded tree species, S. guineense.

Flowers Are an important food for small apes in southern Sumatra

Flowers are included in the diets of many primates, but are not generally regarded as making an important contribution to primate energy budgets. However, observations of a number of lemur, platyrrhine, and cercopithecine populations suggest that some flower species may function as key primate fallback foods in periods of low abundance of preferred foods (generally ripe fruits), and that flowers may be preferred foods in some cases. I report heavy reliance on flowers during some study months for a siamang (Symphalangus syndactylus) population in southern Sumatra. Siamangs at Way Canguk spent 12% of feeding time eating flowers from October 2000 to August 2002, and in 1 month flower-feeding time exceeded 40% of total feeding time. The overall availabilities of fig and nonfig fruits, flowers, and new leaves in the study area were not significant predictors of the proportion of time that siamangs spent consuming any plant part. However, flower-feeding time was highest in months when nonfig fruit-feeding time was lowest, and a switch from heavy reliance on fruit to substantial flower consumption was associated with a shift in activity patterns toward reduced energy expenditure, which is consistent with the interpretation that flowers may function as a fallback food for Way Canguk siamangs. Hydnocarpus gracilis, a plant from which siamangs only consume flowers, was the third-most-commonly consumed plant at Way Canguk (after Ficus spp. and Dracontomelon dao), and flowers from this plant were available in most months. It is possible that relatively high local availability of these important siamang plant foods is one factor promoting high siamang density in the study area.

Use of wild and cultivated foods by chimpanzees at Bossou, Republic of Guinea: feeding dynamics in a human‐influenced environment

Increased human population growth and more conversions of natural habitat to agricultural land have resulted in greater proximity between humans and nonhuman primate species. Consequent increases in resource competition including crop-raiding are a by-product of both natural resources becoming less available and the nutritional benefits of cultivated foods becoming more known to the nonhuman primates. Chimpanzees at Bossou in the Republic of Guinea, West Africa, consume 17 different types of cultivated foods that are grown extensively throughout their small, fragmented home range. Direct observations of feeding behavior conducted over an 18-month period revealed that during specific months crops account for up to one quarter of chimpanzee feeding time, with higher overall crop-raiding levels throughout the periods of wild fruit scarcity. Some cultivated foods, especially sugar fruits, are mostly fallback foods, whereas others, such as rice pith (Oryza sp.) and maize (Zea mays), are consumed according to their availability even when wild foods are abundant. These findings highlight the importance of both crop choice by farmers and a thorough understanding of the ecology of resident primate species when establishing land management techniques for alleviating human-primate conflict.

Tubers as fallback foods and their impact on Hadza hunter‐gatherers

The Hadza are hunter-gatherers in Tanzania. Their diet can be conveniently categorized into five main categories: tubers, berries, meat, baobab, and honey. We showed the Hadza photos of these foods and asked them to rank them in order of preference. Honey was ranked the highest. Tubers, as expected from their low caloric value, were ranked lowest. Given that tubers are least preferred, we used kilograms of tubers arriving in camp across the year as a minimum estimate of their availability. Tubers fit the definition of fallback foods because they are the most continuously available but least preferred foods. Tubers are more often taken when berries are least available. We examined the impact of all foods by assessing variation in adult body mass index (BMI) and percent body fat (%BF) in relation to amount of foods arriving in camp. We found, controlling for region and season, women of reproductive age had a higher %BF in camps where more meat was acquired and a lower %BF where more tubers were taken. We discuss the implications of these results for the Hadza. We also discuss the importance of tubers in human evolution.