Juggling options: Manipulation ease determines primate optimal fruit-size choice

Optimal foraging theory predicts that animals will seek simultaneously to minimize food processing time and maximize energetic gain. To test this hypothesis, we evaluated whether a specialist seed-predator primate forages optimally when choosing among variable-sized thick-husked fruits. Our objects of study were the golden-backed uacari (Cacajao ouakary, Pitheciidae) and single-seeded pods of the macucu tree (Aldina latifolia, Fabaceae). We predict that golden-backed uacari will consume fruits of the size class that requires the least time to obtain, handle, and ingest. We used scan sampling, ad libitum to record feeding observations, and measured fruits, their penetrability, and the size of taxidermized C. ouakary hands. To test whether uacaris selected for optimal characteristics, we compared 8 metrics from 75 eaten and 105 uneaten seeds/fruits collected. Uacaris selected fruits of medium size and weight disproportionately to their abundance. Processing large fruits took six times longer than did medium-sized fruits, but seeds were only four times as large, that is, for energetic yield per unit time, thus choosing medium-sized pods was optimal. Disproportionate selection by C. ouakary of fruits of medium size and mass in relation to their abundance suggests active sub-sampling of the available weight–size continuum. This selectivity probably maximizes trade-offs between the energy derived from a seed, and time and energy expended in processing fruit to access this, so following optimal foraging theory predictions. The greater time spent processing large pods is attributed to difficulties manipulating objects five to seven times the size of the animal's palm and one-sixth its own body weight.     

Diet,Habitat Selection and Natural History of <Emphasis Type="Italic">Cacajao melanocephalus ouakary</Emphasis> in Jaú National Park,Brazil<Superscript>1</Superscript>

We studied golden-backed uacaris, (Cacajao melanocephalus ouakary) in the late-wet season of 1999 and in the mid-dry season of 2000 in Jaú National Park (JNP), Brazil. Additional observations were taken by other scientists working in JNP. Group counts range from 2 to 30 in the wet season and from 1 to > 100 in the dry. In the wet season, we recorded uacaris only in flooded forests (igapó). During the dry season they were in igapó, campinarana, and terra firme forests. We supplemented observations via interviews with local informants on seasonal use of the forest types and of particular small patches of different habitat types that exhibit high temporal patchiness in fruit availability. We recorded a total of 13 food plant species (dry season, 4; flooded season, 9), and a further 55 were provided by interviews. We noted the physical dimensions and hardness of 26 fruit species. Despite accepted specializations of the uakaris on hard unripe fruit, we recorded incidents of insectivory and folivory. Patterns of food availability, and therefore the seasonal habitat-use patterns by golden-backed uacaris, appear to be more complex than previously realized.The authors dedicate this paper to the memory of J. Marcio Ayres, the founding father of uacari field biology.     

Sleeping site selection by golden-backed uacaris, Cacajao melanocephalus ouakary (Pitheciidae), in Amazonian flooded forests

In Amazonian seasonally flooded forest (igapó), golden-backed uacaris, Cacajao melanocephalus ouakary, show high selectivity for sleeping trees. Of 89 tree species in igapó, only 16 were used for sleeping (18%). Hydrochorea marginata (Fabaceae) and Ormosia paraensis (Fabaceae) were used most frequently (41% of records) despite being uncommon (Ivlev electivity ratios were 0.76, and 0.84, respectively), though the third most commonly used species (11%), Amanoa oblongifolia (Euphorbiaceae), was selected at near parity. All three species have broad, open canopies with large horizontal limbs and uncluttered interiors. Compared with random trees, sleeping trees had above average diameter at breast height (DBH) and height, lacked lianas and wasp nests, and were more frequently within 5 m of open water. Uacaris generally slept one adult per tree or widely separated in the same canopy and on the outer third of the branch. These behaviours are interpreted as maximising detection of both aerial and arboreal predators.     

Feeding Ecology of Black-headed Uacaris (Cacajao melanocephalus melanocephalus) in Pico da Neblina National Park,Brazil

From June 1994 to October 1995, I conducted a study of the feeding ecology of one group of black-headed uacaris (Cacajao melanocephalus melanocephalus) in Pico da Neblina National Park, Brazil, near the Venezuelan border (01°10N to 00°26S, 65°03W to 66°52W). Of a total of 429 feeding records, 89% corresponded to fruits from which black-headed uacaris ate ripe and unripe seeds, mesocarps and arils. Seeds were the single most important food item year-around, corresponding to 81% of the feeding records for fruits. Black-headed uacaris used 120 different plant species in 32 families as food. The 3 most important plant species in their diet, Micrandra spruceana, Eperua leucantha, and Hevea braziliensis (all trees), accounted for 38% of the feeding records for fruits. These species produced fruits that were protected by very hard green husks, were barochorous, did not have fleshy mesocarps, and were slow to mature, thus being available as unripe fruits for long periods. The second and third most important species in the diet of black uacaris, Eperua leucantha and Hevea braziliensis, were dominant in the forest: approximately 30% of trees 10 cm dbh sampled in a 2-ha botanical transect at the study site. I discuss the formation of large social groups of black-headed uacaris in Pico da Neblina National Park in light of the peculiar floristic composition of the study site.     

Preliminary survey ofCacajao melanocephalus melanocephalus in Southern Venezuela

We conducted a survey of Cacajao melanocephalus melanocephalusin southern Amazonas, Venezuela, to update information on their distribution and to select a site for a longitudinal study. We surveyed along the Rio Negro, Brazo Casiquiare, Rio Pasimoni, and Rio Baria and interviewed local people. We observed C. m. melanocephalusfour times along the Rio Pasimoni (N =2)and the Rio Baria (N =2).Group size ranged from 3 to 20 individuals. They ate immature seeds from heavily armored fruit of the chicletree (Manilkara bidentataor Manilkara zapota)and Mauritia flexuosa.Local people reported hunting primates, particularly C. m. melanocephalus,once per week. Mercury residue from illegal gold mining may be poisoning local ecosystems. Hunting pressures may have eliminated C. m. melanocephalusfrom much of its range in southern Amazonas. Urgent steps must be taken toward the conservation of C. m. melanocephalus irathis region.     

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

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

Evolutionary Consequences of Fallback Foods

Primatologists use the term fallback foods to denote resources of relatively low preference that are used seasonally when preferred foods are unavailable. We examine the assumption that fallback foods play an important role in shaping morphological adaptations, behavior, and socioecology in primates. We discuss operational definitions of preferred and fallback foods and suggest that the evolutionary importance of fallback foods applies more to adaptations for processing than for harvesting foods. Equally, we propose that preferred resources tend to drive adaptations for harvesting foods. We distinguish 2 classes of fallback foods according to their roles in the diet and their evolutionary effects. Staple fallback foods are available year-round, tend to be eaten throughout the year, and seasonally can constitute up to 100% of the diet. Filler fallback foods never constitute 100% of the diet, and may be completely avoided for weeks at a time. We suggest that the availability of the 2 classes of fallback foods have different effects on the socioecology of primate species.     

Dietary reconstruction of the Amphipithecidae (Primates, Anthropoidea) from the Paleogene of South Asia and paleoecological implications

The primate family, Amphipithecidae, lived during the early Cenozoic in South Asia. In this study, the diet of late middle Eocene amphipithecids from the Pondaung Formation (Central Myanmar) is characterized using three different approaches: body mass estimation, shearing quotient quantification and dental microwear analysis. Our results are compared with other Paleogene amphipithecids from Thailand and Pakistan, and to the other members of the primate community from the Pondaung Formation. Our results indicate a majority of frugivores within this primate community. Pondaungia and “Amphipithecus” included hard objects, such as seeds and nuts, in their diet. Folivory is secondary for these taxa. Myanmarpithecus probably had a mixed diet based on fruit and leaves. Contrasting results and a unique dental morphology distinguish Ganlea from other amphipithecids. These render interpretation difficult but nevertheless indicate a diet tending towards leaves and fruit. However, the anterior dentition of Ganlea suggests that this taxon engaged in seed predation, using its protruding canine as a tool to husk hard fruits and obtain the soft seeds inside. Bahinia and Paukkaungia, two other Pondaung primates, are small (<500 g) and therefore would have depended on insects as their source of protein. As such, they occupied a very different ecological niche from Pondaung amphipithecids. This primate community is then compared with the Eocene-Oligocene primate communities of the Fayum from North Africa. Similarities between the late middle Eocene Pondaung primate community and extant equatorial and tropical South American primate communities are noted.     

The diet of the olive colobus monkey,Procolobus verus,in Sierra Leone

Observations of the feeding behavior of wild olive colobus monkeys (Procolobus verus)were made in southern Sierra Leone, West Africa. Most data came from systematically sampling one habituated social group, which inhabited old secondary rain forest on Tiwai Island. Olive colobus at Tiwai were highly selective feeders, obtaining most of their food from a small number of uncommon middle-canopy trees, from the forest understory, and from climbers. Mature leaf blades were largely ignored; young foliage (particularly of climbers) was a year-round dietary staple, while seeds, flowers, and mature leaf petioles were seasonally important. It is argued that this diet results largely from selection for two different attributes of food: high digestibility and physical location. Preferred foods had low fiber and tannin contents, while preferred feeding sites were in thick low growth and climber tangles. P. verusis the smallest extant primate species using a foregut fermentation system. Observations of its diet accord with inferences drawn from dental anatomy, digestive physiology, and considerations of body size.     

Ants in their plants: Pseudomyrmex ants reduce primate,parrot and squirrel predation on Macrolobium acaciifolium (Fabaceae) seeds in Amazonian Brazil

Although plant‐inhabiting ants are known to act as effective deterrents to a variety of vertebrate and invertebrate herbivores, this has been reported only once before for primates, a group better known for their predation of ants. In the present study, we investigated the effects that colonies of Pseudomyrmex viduus ants living in individual Macrolobium acaciifolium (Fabaceae) trees have on the rates of visitation and fruit removal by four taxa of seed‐predating vertebrates: the primate Cacajao melanocephalus ouakary; macaws (Ara spp.); large parrots (Amazona spp.); and the Northern Amazonian red squirrel (Sciurus igniventris). We found that ant presence significantly reduced both rates of visitation and of fruit removal by C. m. ouakary. The same pattern of reduced fruit removal was also observed for other seed predators (parrots, macaws, and squirrels) but not for visitation rates (although this may be a result of the small sample size). This appears to be only the second‐known demonstration of the repellent effect of ants on primates and, indeed, the first for squirrels and psittacine birds. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 260–273.     

Southern expansion of the geographical distribution ofCacajao melanocephalus melanocephalus

Cacajao melanocephalus melanocephalus, a subspecies of black uakari, was thought to be restricted to southern Venezuela. Observations of two groups of them in Pico da Neblina National Park, Brazil, suggest that its distribution should be extended to the Brazilian territory.     

Diet of the northern bearded saki (Chiropotes satanas chiropotes): A neotropical seed predator

Data on the diet of Chiropotes satanas chiropotes, the northern bearded saki, has been collected during several years of primate field observations in the Raleighvallen-Voltzberg Reserve in Suriname. This species feeds predominantly on immature seeds and ripe fruit, mainly the former. Chiropotes is especially fond of the members of the Brazil nut family, Lecythidaceae, and other species with exceptionally hard or tough seed pods. Concomitantly, Chiropotes shows striking dental and gnathic adaptations that facilitate opening and ingesting these well-protected food items. Seed predation in the Old World colobine, Colobus satanas, has been discussed primarily as a strategy for survival in forests characterized by leaves with low nutrient content and high toxicity; however, it now appears that arboreal seed predation is a relatively widespread primate dietary strategy found among higher primate species in a variety of forest types on three continents. It is yet another way of “making a living” in a tropical rain forest.     

Enamel thickness and microstructure in pitheciin primates, with comments on dietary adaptations of the middle Miocene hominoid Kenyapithecus

Many living primates that feed on hard food have been observed to have thick-enameled molars. Among platyrrhine primates, members of the tribe Pitheciini (Cacajao, Chiropotes, and Pithecia) are the most specialized seed and nut predators, and Cebus apella also includes exceptionally hard foods in its diet. To examine the hypothesized relationship between thick enamel and hard-object feeding, we sectioned small samples of molars from the platyrrhine primates Aotus trivergatus, Ateles paniscus, Callicebus moloch, Cebus apella, Cacajao calvus, Chiropotes satanas, Pithecia monachus, and Pithecia pithecia. We measured relative enamel thickness and examined enamel microstructure, paying special attention to the development of prism decussation and its optical manifestation, Hunter-Schreger Bands (HSB). Cebus apella has thick enamel with well-defined but sinuous HSB overlain by a substantial layer of radial prisms. Aotus and Callicebus have thin enamel consisting primarily of radial enamel with no HSB, Ateles has thin enamel with moderately developed HSB and an outer layer of radial prisms, and the thin enamel of the pitheciins (Cacajao, Chiropotes, and Pithecia) has extremely well-defined HSB. Among platyrrhines, two groups that feed on hard objects process these hard foods in different ways. Cebus apella masticates hard and brittle seeds with its thick-enameled cheek teeth. Pitheciin sclerocarpic foragers open hard husks with their canines but chew relatively soft and pliable seeds with their molars. These results reveal that thick enamel per se is not a prerequisite for hard object feeding. The Miocene hominoid Kenyapithecus may have included hard objects in its diet, but its thick-enameled molars indicate that its feeding adaptations differed from those of the pitheciins. The morphology of both the anterior and posterior dentition, including enamel thickness and microstructure, should be taken into consideration when inferring the dietary regime of fossil species.     

Preliminary survey of Cacajao melanocephalus melanocephalus in Southern Venezuela

We conducted a survey of Cacajao melanocephalus melanocephalusin southern Amazonas, Venezuela, to update information on their distribution and to select a site for a longitudinal study. We surveyed along the Rio Negro, Brazo Casiquiare, Rio Pasimoni, and Rio Baria and interviewed local people. We observed C. m. melanocephalusfour times along the Rio Pasimoni (N =2)and the Rio Baria (N =2).Group size ranged from 3 to 20 individuals. They ate immature seeds from heavily armored fruit of the chicletree (Manilkara bidentataor Manilkara zapota)and Mauritia flexuosa.Local people reported hunting primates, particularly C. m. melanocephalus,once per week. Mercury residue from illegal gold mining may be poisoning local ecosystems. Hunting pressures may have eliminated C. m. melanocephalusfrom much of its range in southern Amazonas. Urgent steps must be taken toward the conservation of C. m. melanocephalus irathis region.     

The primate community of the Lopé reserve,Gabon: Diets,responses to fruit scarcity,and effects on biomass

The diets of all diurnal primates (Gorilla g. gorilla, Pan t. troglodytes, Mandrillus sphinx, Colobus satanas, Cercocebus albigena, Cercopithecus nictitans, C. pogonias, C. cephus) in the Lopé Reserve, central Gabon, are described from qualitative and quantitative data collected over 10 years. A total of 397 foods were recorded, of which 91% were from plants. The diets of seven of the eight species were numerically dominated by fruit, the exception being Colobus satanas with a diet dominated by seeds. When proportion of feeding time was examined, fruit remained the dominant food class for six species, while Cercocebus albigena, like the black colobus, spent most time feeding on seeds. The number of foods recorded per species ranged from 46–220, but dietary breadth of the four species that have not been subjects of detailed study was certainly underestimated. Almost half of the foods (46%) were eaten by only one species, and only four (1%) were recorded for all eight species. At Lopé, fruit is scarce for 2–3 months during the annual dry season, and fruit crop failures can prolong this period of scarcity to as many as 8 months in some years. When fruit is scarce, the diets of all species changed to include more nonfruit foods, but chimpanzees and the three species of guenons maintained a fruit dominated diet. The total biomass of the Lopé primate community is 374 kg/km², which is low compared to other sites in tropical Africa. Within the Lopé community, biomass correlates negatively with degree of frugivory, suggesting that fruit availability may be critical, but this does not explain the low total biomass compared to other sites. Neither floristic diversity nor the composition of the primate community at Lopé can account for the low biomass. While historical events such as climate-induced changes in forest cover, disease, or impact of human activities cannot be ruled out, we conclude that the most likely explanation of low primate biomass is the occurrence of an ecological “catastrophe” in the fairly recent past from which populations have not yet recovered. We believe that the most likely scenario was climate-mediated disturbance of flowering of important fruit food species. Prolonged fruit scarcity would have caused mortalities and affected the most frugivorous species more severely. Am. J. Primatol. 42:1–24, 1997. © 1997 Wiley-Liss, Inc.     

Ontogenetic plasticity of food habits in the Mexican spiny-tailed iguana, Ctenosaura pectinata

Ontogenetic shifts from insect consumption by juveniles to plant consumption by adults are rare in the herbivorous lizard family Iguanidae. My investigations on diet and digestive tract anatomy of the iguanid lizard Ctenosaura pectinata show that this species has an ontogenetic diet shift. Insects were rare in adult diets but constituted 86.5% (by volume) of the food eaten by the smallest juveniles. All age classes ate some plant parts from a range of plant types, but flowers and leaves of legumes were a primarily food source. Non-adult lizards had the widest food niche breadths. Arthropods in the diet of juveniles and immatures covaried seasonally with the decline of arthropod abundance. Several hypotheses could explain this ontogenetic plasticity in diet. I rejected hypotheses that gut structure constrained juveniles to an arthropod diet and that insect consumption was purely an artifact of plant consumption because (1) size-adjusted gut morphology and capacity was similar among age classes, and (2) no food plants sampled had an excessive density of arthropods. I supported an alternative hypothesis that juveniles can eat plants but do not because insects provide a more nutritious diet. This conclusion was based on the observation that the juvenile hindgut is similar to that of herbivorous adults, and the propensity for juveniles to consume primarily, but not exclusively, insects when they were most abundant. The hindgut represents the site of fermentative plant fiber breakdown in many herbivorous lizards. Insect foods can compensate for size-related nutritional needs (energy and protein) and digestive limitations in juveniles. Opportunistic feeding to maintain a broad diet might help juvenile and immature lizards through high-predation-risk growth periods by reducing searching costs, increasing nutritional and energetic gains due to associative effects, and increasing new food exposure. Received: 20 January 1999 / Accepted: 25 January 2000     

The time of divergence between the two species of uacari monkeys: Cacajao calvus and Cacajao melanocephalus

It has been suggested in the literature that primates of the genus Cacajao have been restricted to flooded-forest habitats of western Amazonia since their split from the Chiropotes line in the Tertiary. It has been proposed further that the differentiation of the two species of this genus, Cacajao melanocephalus and Cacajao calvus, occurred during the Pleistocene period as a result of the fragmentation of the Amazon forest and the isolation of populations in these forest fragments or refuges. However, recent evidence has shown that at least C. melanocephalus is not dependent on flooded-forest habitats, and molecular analysis of mitochondrial DNA shows that the two species had already differentiated during the Pliocene, thus Pleistocene glaciations do not explain the speciation in Cacajao. Considering that C. melanocephalus and its closest relative, Chiropotes, inhabit terra firme forests, it is suggested that preference for flooded-forest habitats may be an apomorphy in C. calvus.     

食物对棉铃虫生长发育及繁殖的影响

用棉花、花生、玉米及人工饲料作为食料,模拟幼虫田间取食习性,同时为雌蛾设立补充和无补充营养两个处理,研究了食物对棉铃虫 Helicoverpa armigera (Hübner) 生长发育及繁殖的影响。4种食料组幼虫历期之间有显著差异;雌、雄蛹重花生组显著小于其余三组。雌蛾腹部干重及其脂肪百分含量与雌蛹体重的排列顺序一样,雌蛾腹部干重人工饲料组显著大于棉花组和花生组。雌蛾寿命和繁殖受幼虫食料和成虫食物的双重影响。喂10%蜂蜜时,雌蛾寿命、交配率和产卵量在四个幼虫食料组之间没有显著差异。但喂以清水时,花生组雌蛾均未交配,寿命和产卵量显著小于其余三组。从同种幼虫食料来看,除人工饲料组外,其余3组雌蛾喂清水时的产卵量和寿命均比喂10%蜂蜜溶液时的显著下降。基于这些结果,作者认为棉花、玉米比花生更适合于棉铃虫的生长发育和繁殖。在田间自然栽培状态下,不同食料植物的糖分含量对棉铃虫生长发育和繁殖影响较大,含氮量的变化影响小。     

Food Items Consumed by White-headed Langurs in Fusui, China

We studied the socioecology of white-headed langurs (Trachypithecus leucocephalus) from September 1997 to September 1998 in Fusui Precious Animal Reserve, SW Guangxi, China. We collected data on climate, phenology of food plant species, and foods consumed by langurs living in habitats with different levels of human disturbance. Feeding records showed that the most food is from less common plant species. Young leaves were the staple food item in all langur groups, and consumption correlates with availability. Consumption of mature leaves is not significantly correlated with their availability, but the langurs fed on them, and other food items such as fruits and seeds, when the availability of young leaves was low. Langurs in different areas had broadly similar diets, but they varied most in the proportion of supplementary items such as fruit. Groups in more disturbed habitat did not increase the overall proportion of mature leaves in their diet, but instead maintained their intake of young leaves from a greater diversity of species, and incorporated more immature fruit. Conservationists should direct efforts toward protection of rare plant species providing preferred food items, particularly supplementary foods at times when, and in areas where, preferred food items are less available.