Defining fallback foods and assessing their importance in primate ecology and evolution

Physical anthropologists use the term “fallback foods” to denote resources of relatively poor nutritional quality that become particularly important dietary components during periods when preferred foods are scarce. Fallback foods are becoming increasingly invoked as key selective forces that determine masticatory and digestive anatomy, influence grouping and ranging behavior, and underlie fundamental evolutionary processes such as speciation, extinction, and adaptation. In this article, we provide an overview of the concept of fallback foods by discussing definitions of the term and categorizations of types of fallback foods, and by examining the importance of fallback foods for primate ecology and evolution. We begin by comparing two recently published conceptual frameworks for considering the evolutionary significance of fallback foods and propose a way in which these approaches might be integrated. We then consider a series of questions about the importance of fallback foods for primates, including the extent to which fallback foods should be considered a distinct class of food resources, separate from preferred or commonly eaten foods; the link between life history strategy and fallback foods; if fallback foods always limit primate carrying capacity; and whether particular plant growth forms might play especially important roles as fallback resources for primates. We conclude with a brief consideration of links between fallback foods and primate conservation. Am J Phys Anthropol 140:603–614, 2009. © 2009 Wiley-Liss, Inc.     

Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, 2. Temporal variation and fallback foods

Highly frugivorous primates like chimpanzees (Pan trogolodytes) must contend with temporal variation in food abundance and quality by tracking fruit crops and relying more on alternative foods, some of them fallbacks, when fruit is scarce. We used behavioral data from 122 months between 1995 and 2009 plus 12 years of phenology records to investigate temporal dietary variation and use of fallback foods by chimpanzees at Ngogo, Kibale National Park, Uganda. Fruit, including figs, comprised most of the diet. Fruit and fig availability varied seasonally, but the exact timing of fruit production and the amount of fruit produced varied extensively from year to year, both overall and within and among species. Feeding time devoted to all major fruit and fig species was positively associated with availability, reinforcing the argument that chimpanzees are ripe fruit specialists. Feeding time devoted to figs-particularly Ficus mucuso (the top food)--varied inversely with the abundance of nonfig fruits and with foraging effort devoted to such fruit. However, figs contributed much of the diet for most of the year and are best seen as staples available most of the time and eaten in proportion to availability. Leaves also contributed much of the diet and served as fallbacks when nonfig fruits were scarce. In contrast to the nearby Kanywara study site in Kibale, pith and stems contributed little of the diet and were not fallbacks. Fruit seasons (periods of at least 2 months when nonfig fruits account for at least 40% of feeding time; Gilby & Wrangham., Behavioral Ecology and Sociobiology 61:1771-1779, 2007) were more common at Ngogo than Kanyawara, consistent with an earlier report that fruit availability varies less at Ngogo [Chapman et al., African Journal of Ecology 35:287-302, 1997]. F. mucuso is absent at Kanyawara; its high density at Ngogo, combined with lower variation in fruit availability, probably helps to explain why chimpanzee population density is much higher at Ngogo.     

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. AmJ Phys Anthropol 140:599–602, 2009. © 2009 Wiley-Liss, Inc.     

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. Am J Phys Anthropol 140:687–699, 2009. © 2009 Wiley-Liss, Inc.     

Nutritional correlates of the “lean season”: Effects of seasonality and frugivory on the nutritional ecology of diademed sifakas

Primate field studies often identify “lean seasons,” when preferred foods are scarce, and lower‐quality, abundant foods (fallback foods) are consumed. Here, we quantify the nutritional implications of these terms for two diademed sifaka groups (Propithecus diadema) in Madagascar, using detailed feeding observations and chemical analyses of foods. In particular, we sought to understand 1) how macronutrient and energy intakes vary seasonally, including whether these intakes respond in similar or divergent ways; 2) how the amount of food ingested varies seasonally (including whether changes in amount eaten may compensate for altered food quality); and 3) correlations between these variables and the degree of frugivory. In the lean season, sifakas shifted to non‐fruit foods (leaves and flowers), which tended to be high in protein while low in other macronutrients and energy, but the average composition of the most used foods in each season was similar. They also showed dramatic decreases in feeding time, food ingested, and consequently, daily intake of macronutrients and energy. The degree of frugivory in the daily diet was a strong positive predictor of feeding time, amount ingested and all macronutrient and energy intakes, though season had an independent effect. These results suggest that factors restricting how much food can be eaten (e.g., handling time, availability, or intrinsic characteristics like fiber and plant secondary metabolites) can be more important than the nutritional composition of foods themselves in determining nutritional outcomes—a finding with relevance for understanding seasonal changes in behavior, life history strategies, competitive regimes, and conservation planning. Am J Phys Anthropol 153:78–91, 2014. © 2013 Wiley Periodicals, Inc.     

Feeding ecology and morphology of the upper canines in bears (carnivora: Ursidae)

The morphology and mechanical strength of the upper canines in all eight extant species of ursids is analyzed, and the findings are discussed in relation to feeding ecology. Ursids have proportionally smaller canines than other large carnivores with a specialized feeding ecology, such as large felids, and the upper canine morphology is both canid‐like and felid‐like. The giant panda is the most divergent species, and its short, blunt, and cone‐like canines appear well adapted for tearing into bamboo. The almost equally herbivorous spectacled bear has a less derived canine morphology. The large canines of the sun bear are divergent from other ursine ursids, and may be an adaptation for tearing open tree trunks in search of insects. Discriminant Analysis is successful in separating ursid species on the basis of canine morphology, but the canines of ursine ursids, and also of the spectacled bear, show greater resemblance among the species than the marked differences in feeding ecology would suggest. This could be in part due to a short evolutionary history, and in part due to canines not having been subjected to much evolutionary selection as has been the case among other large carnivores, such as large felids. Ursids are probably evolutionarily and ecologically successful due to physical size and strength rather than a derived craniodental anatomy. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Feeding ecology and foraging behaviour of impala Aepyceros melampus in Lake Mburo National Park, Uganda

Intersexual and seasonal variation in foraging behaviour of impala (Aepyceros melampus), was studied in the Lake Mburo National Park, Uganda. There was a moderate seasonal difference in foraging efficiency (as measured by ‘acceptable food abundance’), with a minimum in dry season and a maximum in Rainy season. The variation between sexes was more distinct with a pronounced minimum in time spent browsing of males in early wet season. By distinguishing between feeding time spent grazing and feeding time spent browsing the seasonal variation was confirmed. The proportion of foraging time spent feeding (expressed as ‘food ingestion rate’) showed an inverse pattern with a maximum in the late dry season (75.5%), decreasing values throughout the Rainy season and a minimum in early dry season (57.8%). Differences between sexes were explained in terms of reproductive demands and seasonal balance in terms of moderate climate throughout the year. Impala foraging patterns in the bimodal tropics (two Rainy seasons) is discussed and compared with unimodal tropics. The findings are matched against current ideas on optimal foraging.     

Feeding Ecology of Two Plecopterans in Low Order Andean‐Patagonian Streams

Feeding plasticity of the Andean plecopteran Klapopteryx kuscheli and Notoperla archiplatae larvae was assessed through a field experiment using enclosures. K. kuscheli has previously been described as a shredder and N. archiplatae as a scraper. Further information on gut contents from different populations supported those results. In the experiment, larvae of both species were exposed to contrasting food items: leaf litter and periphyton. Consumption, growth and the efficiency of food conversion were measured. K. kuscheli was able to feed on periphyton, though it did not grow. N. archiplatae failed to feed on leaf litter. While K. kuscheli might be considered a facultative shredder, N. archiplatae functions as a specialist scraper. The natural distribution and seasonal abundance in two small streams showed contrasting habitat use of both species. N. archiplatae inhabited high velocity runs and riffles underneath large substrates while K. kuscheli presented a higher habitat plasticity. Implications of those results for ecosystem function are discussed. (© 2006 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Diet of four rock‐dwelling macropods in the Australian monsoon tropics

Abstract An unusually high diversity of macropods inhabit the rocky areas in the monsoon tropics of the Northern Territory, Australia, yet the mechanisms that allow their niche separation are not clear. Previous studies suggest that the nabarlek, Petrogale concinna, may have a more grazing diet than the short‐eared rock‐wallaby, Petrogale brachyotis, with whom it coexists. Thus, diet may be an important mechanism of niche separation between these species. We examined the diet of the four sympatric species (the black wallaroo Macropus bernardus, common wallaroo Macropus robustus, P. brachyotis and P. concinna) to determine whether there are differences in the dominant plant groups eaten by the species across the landscape and with season. Diets were determined with a macroscopic analysis of the seed and fruit content of scats and an analysis of the ¹²C to ¹³C isotope ratios of scats using mass spectrometry. In the dry season the rock‐wallaby species predominantly consumed browse and/or forbs, and the larger wallaroos predominantly consumed grass. However, there was large variation across the landscape in the dry season diets of P. brachyotis, M. bernardus and M. robustus; including high proportions of grass eaten at some sites and high proportions of browse at other sites. In the wet season, greater proportions of grass were eaten by P. brachyotis and M. bernardus than in the dry season. Generally, there was little evidence to support the previous suggestion that P. concinna is more of a grazer than P. brachyotis, but there was some evidence than M. bernardus consumes greater amounts of browse and/or forbs than M. robustus.     

Feeding dynamics,consumption rates and daily ration of wahoo Acanthocybium solandri in Indo‐Pacific waters

This study reports the diet composition of 363 wahoo Acanthocybium solandri captured from the Indo‐Pacific. The study also provides the first estimates of consumption and daily ration for the species worldwide, which are important parameters for ecosystem models and may improve ecosystem‐based fisheries management. Thirty‐four prey taxa were identified from A. solandri stomachs with Scombridae having the highest relative importance. Actinopterygii comprised 96% of the total prey wet mass, of which 29% were epipelagic fishes, with 22% alone from Scombridae. There was no significant relationship between fish size and the size of prey items consumed. Feeding intensity, as measured by stomach fullness, did not significantly differ either among seasons or reproductive activity. The mean daily consumption rate was estimated as 344 g day^?1, which corresponded to a mean daily ration of 2·44% body mass day^?1. The results from this study suggest A. solandri is an opportunistic predator similar to other pelagic piscivores, worldwide.     

Feeding ecology of larval and juvenile black seabream (Acanthopagrus schlegeli) and Japanese seaperch (Lateolabrax japonicus) in Tolo Harbour, Hong Kong

Black seabream, Acanthopagrus schlegeli, and Japanese seaperch, Lateolabrax japonicus, are important commercial species in the coastal waters of western Pacific Ocean, including Japan, Korea and China. In Hong Kong, larvae and juveniles of these two species occur in bays and estuaries during late winter and spring. This study reports on the ontogenetic changes in food habits in larvae and juveniles of these species in an artificial rocky shore area. Copepods and cladocerans were the most numerous food items for black seabream. There was a shift to larger and benthic prey as the fishes grew. Japanese seaperch <2.1cm fed predominantly on copepods and cladocerans, while larger prey were added as fish size increased. Japanese seaperch >6.0cm were piscivorous. Maximum prey width increased with fish standard length and mouth gape width in both species. Overall, black seabream showed greater diet breadth than did Japanese seaperch. In black seabream, diet breadth increased with fish size. In Japanese seaperch, diet breadth increased with size for fishes <4.0cm, then decreased as the fishes became piscivorous. Prey selectivity in black seabream was determined using information on prey availability in plankton samples. In general, preference was stronger for cypris larvae, Penilia avirostris and decapod larvae than for copepods and podonids. In recent years, overfishing and environmental degradation have led to the decline of fish populations in Tolo Harbour. Absence of fishes with empty gut indicates that inner Tolo Harbour is still an important nursery area for these two commercial species.     

Feeding ecology of a group of buffy‐headed marmosets (Callithrix flaviceps): fungi as a preferred resource

Mycophagy is a relatively rare behavior in primates and has only been recorded in five callitrichid species. Here, we present data on the feeding ecology of a free‐ranging group of Callithrix flaviceps, which was studied in the Augusto Ruschi Biological Reserve, Southeastern Brazil, in 2008. In contrast with other marmosets, which are typically gummivorous, the study group was predominantly mycophagous–insectivorous, with fungi corresponding to 64.8% of total feeding records, and gum (6.1%) and fruit (3.3%) together providing only a minor part of the diet. Prey corresponded to 25.8% of the group's diet. The fungi (Mycocitrus spp.) consumed by the marmosets were found attached to the stems of Merostachys bamboo. As the animal component of the group's diet was similar to that recorded in studies of other marmosets, we propose that fungi were exploited primarily as a substitute for plant material, in particular exudates. This highly mycophagous diet may be determined by two principal factors: (1) the abundance of fungi within the study area, and (2) the avoidance of bark gouging, for which C. flaviceps may be less specialized than most other marmosets. These conclusions are supported by comparisons with other marmoset groups, which indicate an ecological specialization for mycophagy in C. flaviceps, and that the species will resort to gummivory in habitats where fungi are scarce. Am. J. Primatol. 72:515–521, 2010. © 2010 Wiley‐Liss, Inc.     

Feeding ecology of Mediterranean common dolphins: The importance of mesopelagic fish in the diet of an endangered subpopulation

The Mediterranean subpopulation of common dolphin (Delphinus delphis) is classified as endangered by the IUCN. Still, information about their diet in the Mediterranean is scarce. Stomach contents of 37 common dolphins stranded in the Alboran Sea and Strait of Gibraltar were analyzed. A total of 13,634 individual prey of 28 different taxa were identified. For fish, Myctophidae was the most important family as indicated by the highest index of relative importance (IRI = 8,470), followed by the family Sparidae (IRI = 609). The most important Myctophidae species was Madeira lantern fish (Ceratoscopelus maderensis) and for Sparids, the bogue (Boops boops). Cephalopods, instead, were found in low quantities only with 31 prey from the Loliginidae, Ommastrephidae, and Sepiolidae families. Overall, our results indicate that common dolphins are mainly piscivorous (99.77%N, 94.59%O, 99.73%W), feeding mostly on mesopelagic prey. Although common dolphins inhabit mainly coastal waters in the study area, the narrow continental shelf seems to facilitate the availability of Myctophids and other members of the mesopelagic assemblage to dolphins when the assemblage migrates to the surface at night. Our results represent the first attempt at quantifying the diet of this predator in the Alboran Sea and Strait of Gibraltar.     

Role of breeding and natal movements in lifetime dispersal of a forest‐dwelling rodent

The lifetime movements of an individual determine the gene flow and invasion potential of the species. However, sex dependence of dispersal and selective pressures driving dispersal have gained much more attention than dispersal at different life and age stages. Natal dispersal is more common than dispersal between breeding attempts, but breeding dispersal may be promoted by resource availability and competition. Here, we utilize mark–recapture data on the nest‐box population of Siberian flying squirrels to analyze lifetime dispersal patterns. Natal dispersal means the distance between the natal nest and the nest used the following year, whereas breeding movements refer to the nest site changes between breeding attempts. The movement distances observed here were comparable to distances reported earlier from radio‐telemetry studies. Breeding movements did not contribute to lifetime dispersal distance and were not related to variation in food abundance or habitat patch size. Breeding movements of males were negatively, albeit not strongly, related to male population size. In females, breeding movement activity was low and was not related to previous breeding success or to competition between females for territories. Natal philopatry was linked to apparent death of a mother; that is, we did not find evidence for mothers bequeathing territories for offspring, like observed in some other rodent species. Our results give an example of a species in which breeding movements are not driven by environmental variability or nest site quality. Different evolutionary forces often operate in natal and breeding movements, and our study supports the view that juveniles are responsible for redistributing individuals within and between populations. This emphasizes the importance of knowledge on natal dispersal, if we want to understand consequences of movement ecology of the species at the population level.     

The importance of seasonal variation in hair coloration for thermoregulation of Ctenucha virginica larvae (Lepidoptera: Arctiidae)

ABSTRACT. . A marked seasonal variation in the hair colour of Ctenucha virginica (Esp.) larvae is observed under field conditions. During the autumn and spring larvae are black and yellow, while during the summer they are predominantly yellow. Under sunny conditions in the field, or when exposed to a radiation heat source in the laboratory, black and yellow larvae have significantly higher body temperatures than yellow ones. As larvae feed over a limited range of temperatures, it is proposed that seasonal changes in hair colour may help larvae to thermoregulate, thereby maintaining body temperatures within the range where feeding is possible.     

Seasonal variation in food availability and relative importance of dietary items in the Gambian epauletted fruit bat (Epomophorus gambianus)

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