Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (S. mystax) tamarins in an Amazonian terra firme forest

The feeding ecology of two small-bodied primate species—saddle-back ( Saguinus fuscicollis auilapiresi ) and moustached tamarins ( S. mystax pileatus )—occurring in stable, mixed-species groups was studied in a terra firme forest site in the upper Urucu River, Amazonas, Brazil. Ecological data are based primarily on one mixed-species group of 5–8 saddle-back and 8–10 moustached tamarins. The overall vegetative and animal-prey components of each tamarin species' diet, their selection of food species, and the seasonal variation in their use of plant resources are described, and compared to those of callitrichids elsewhere. The extremely diverse diet of tamarins included at least 136 tree, 33 vine and liana, 12 epiphyte and nine shrub species, as well as a wide range of prey items. They fed primarily on ripe fruit pulp of most of these species for most of the year, but shifted to floral nectar and plant exudates of a few key plant species during the dry season. Taxonomic overlap in plant diet was nearly complete between the two tamarin species, but they diverged considerably in their prey capture techniques. Saddle-backs used the low forest understorey, and manipulatively searched for sedentary prey concealed within discrete, usually rigid, microhabitats, whereas moustached tamarins used the midstorey where they visually searched for mobile prey well exposed on foliage. These and other feeding and foraging patterns are discussed in the light of other callitrichid species studied to date.     

Responses of squirrel monkeys to seasonal changes in food availability in an eastern Amazonian forest

Tropical forests are characterized by marked temporal and spatial variation in productivity, and many primates face foraging problems associated with seasonal shifts in fruit availability. In this study, I examined seasonal changes in diet and foraging behaviors of two groups of squirrel monkeys (Saimiri sciureus), studied for 12 months in Eastern Brazilian Amazonia, an area characterized by seasonal rainfall. Squirrel monkeys were primarily insectivorous (79% of feeding and foraging time), with fruit consumption highest during the rainy season. Although monkeys fed from 68 plant species, fruit of Attalea maripa palms accounted for 28% of annual fruit-feeding records. Dietary shifts in the dry season were correlated with a decline in ripe A. maripa fruits. Despite pronounced seasonal variation in rainfall and fruit abundance, foraging efficiency, travel time, and distance traveled remained stable between seasons. Instead, squirrel monkeys at this Eastern Amazonian site primarily dealt with the seasonal decline in fruit by showing dietary flexibility. Consumption of insects, flowers, and exudates increased during the dry season. In particular, their foraging behavior at this time strongly resembled that of tamarins (Saguinus sp.) and consisted of heavy use of seed-pod exudates and specialized foraging on large-bodied orthopterans near the forest floor. Comparisons with squirrel monkeys at other locations indicate that, across their geographic range, Saimiri use a variety of behavioral tactics during reduced periods of fruit availability.     

Diet of a free-ranging group of squirrel monkeys (Saimiri sciureus) in eastern Brazilian Amazonia

The feeding behaviour of free-ranging Saimiri sciureus was monitored over a 6-month period in eastern Brazilian Amazonia. Behavioural data were collected in scan samples (7-9 days per month), and fruit and arthropod availability were recorded monthly. A total of 3,546 feeding records were collected, divided between reproductive plant parts (55.1%) and arthropods (44.9%). The majority of identified prey were orthopterans and lepidopterans, and 10 of the 23 plant species exploited were Leguminosae and Sapotaceae. The diet varied progressively between August (20.0% plant, 80.0% animal) and January (79.7% plant, 20.3% animal). This shift accompanied an increase in the number of fruiting trees and evidence of declining arthropod availability. This included a marked reduction in foraging success and increasing consumption of immature prey. Overall, the data indicate that Amazonian squirrel monkeys may be relatively frugivorous during periods when prey is scarce.     

Role of spatial memory in primate foraging patterns: Saguinus mystax and Saguinus fuscicollis

From field data collected in the Amazon Basin of northeastern Peru, I present evidence that moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarins maintain detailed knowledge of the distribution and location of many tree species in their home range. During the wet season months of October through December 1984, fruits and exudates from 20 tree species and over 150 individual trees accounted for 75% of plant feeding time. These trees exhibited a patchy distribution; mean nearest-neighbor distances between trees of the same species averaged 148 meters. Moustached and saddle-back tamarins visited an average of 13 trees per day, concentrating their feeding efforts on 4–11 individual trees from a small number of target species. In 70% of all cases the nearest tree of a given species was selected as the next feeding site. Movement between these sites was characterized by relatively straight-line travel. It is argued that S. mystax and S. fuscicollis offset the patchiness component of the fruit and exudate part of their diet through goal-directed foraging and an ability to compare accurately the distances and directions from their present location to a large number of potential feeding trees.     

Seasonal patterns of diet and ranging in two species of tamarin monkeys: Stability versus variability

From June through December, data were collected on the diet and ranging patterns of moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarin monkeys in the Amazon Basin of northeastern Peru. During this 7-month period, insects and nonleguminous fruits accounted for 83% of tamarin feeding and foraging time. Despite marked seasonal variation in rainfall and forest productivity, patterns of habitat utilization, day range, dietary diversity, resource exploitation, and activity budget remained relatively stable throughout the year. Moustached and saddle-back tamarins appear to solve problems of food acquisition and exploit patchily distributed feeding sites using a relatively limited set of foraging patterns. In general, these primates concentrate their daily feeding efforts on several trees from a small number of target plant species. These feeding sites are uncommon, produce only a small amount of ripe fruit each day, and are characterized by a high degree of intraspecific fruiting and flowering synchrony. Trees of the same species are frequently visited in succession, and individual feeding sites are revisited several times over the course of 1–2 weeks. This type of foraging pattern occurred during both dry and wet seasons and when exploiting fruit, nectar, legume, and exudate resources. Seasonal variation in the percentage of feeding and foraging time devoted to insectivory was also limited. In this investigation, there was no consistent evidence that temporal changes in overall forest fruit production had a major impact on the feeding, foraging, or ranging behavior of either tamarin species.     

Forest type affects prey foraging of saddleback tamarins,Saguinus nigrifrons

Callitrichids can persist in secondary forests where they may benefit from elevated prey abundance. However, how tamarins forage for prey in secondary forest compared to primary forest has not been examined. Using scan and focal sampling, we compared prey foraging and capture success of two groups of Saguinus nigrifrons in north-eastern Peru: one ranging in primary forest, the other with access to a 10-year-old anthropogenic secondary forest. There was a trend for more prey search in the secondary forest, but prey feeding, capture success and size were lower compared to the primary forest. Tamarins avoided the forest floor, used vertical supports less often and searched on a lower variety of substrates in the secondary forest. In the secondary forest, tamarins did not capture flushed prey, which make up a substantial part of the total prey captures biomass in primary forests. Reduced prey capture success is unlikely to reflect reduced prey availability, since more Orthoptera were found in secondary forest through ultrasonic surveys. Therefore, the prey search activity of S. nigrifrons in young secondary forests seemed rather opportunistic, presumably influenced by altered predation patterns, vegetation structure, as well as prey diversity.     

Feeding behavior of Geoffroy's marmoset (Callithrix geoffroyi) in an Atlantic forest fragment of South-eastern Brazil

We report on the diet and feeding behaviour of a group of Geoffroy's marmosets (Callithrix geoffroyi) in an Atlantic forest fragment in south-eastern Brazil, studied during the period February 1993 to Januaray 1994. Major food categories were gums (68.6%) fruits (15%), and small animal prey (invertebrates 14.6% and vertebrates 0.8%). Dietary changes were observed between the wet and dry seasons, although they were not statistically significant. Insects and gums were consumed throughout the year but fruits were more prevalent in the diet in the wet season. Plant species exploited for their gums includedInga stipularis, followed byAcacia paniculata, Paulinia carpopodia, andBauhinia angulosa. Chemical analysis of the gum of the four species most used all presented high values for carbohydrates and crude proteins. Fruits of an unidentified species of Myrtaceae (sp. 2) were consumed the most. Animal prey consisted mainly of insects, arachnids, snails, and in three cases, lizards and frogs, with orthopterans being the most prevalent insect prey. This study demonstrates thatC. geoffroyi efficiently exploits resources typically available in secondary and disturbed forest habitat. The main threat to the species is forest destruction, degradation, and fragmentation, but the management of small forest fragments may be an effective corservation strategy.     

Food patch structure and plant resource partitioning in interspecific associations of amazonian tamarins

ávila-Pires’ saddle-back tamarins (Saguinus fuscicollis avilapiresi) and red-cap moustached tamarins (S. mystax pileatus), coexisting in highly stable mixed-species groups, overlapped considerably in their use of plant food resources at an Amazonian terra firme forest site. Overlap between food types consumed by the two species was particularly high during periods of lowest fruit availability, when they resorted to a common food supply, primarily the pod exudates of two emergent species of legume trees (Parkia nitida andParkia pendula) and nectar ofSymphonia globulifera. Within-group interspecific competition did not covary with independent measures of resource availability, contrary to predictions based on resource partitioning models. A greater number of both saddle-back and moustached tamarins were able to feed for longer patch residence periods within larger and more productive food patches, whereas small and clumped patches could be monopolized by the socially and numerically dominant moustached tamarins to the physical exclusion of the smaller-bodied saddle-back tamarins. Overall rates of interspecific aggression were extremely low, however, partly because patches that could be monopolized contributed with a minor proportion of either species’ diet. Saddle-backs foraged at lower levels in the understory and encountered smaller food patches more often, whereas moustached tamarins foraged higher and encountered more larger patches in the middle canopy. Although the two species led one another to differently-sized patches, moustached tamarins initiated most feeding bouts and encountered significantly larger and more productive patches that tended to accommodate the entire mixed-species group. Disadvantages of exploitative and interference feeding competition over plant resources, and advantages of shared knowledge of food patches, are but one component of the overall cost-benefit relationship of interspecific associations in tamarins.     

High‐throughput sequencing of fecal DNA to identify insects consumed by wild Weddell's saddleback tamarins (Saguinus weddelli,Cebidae, Primates) in Bolivia

The genus Saguinus represents a successful radiation of over 20 species of small‐bodied New World monkeys. Studies of the tamarin diet indicate that insects and small vertebrates account for ～16–45% of total feeding and foraging time, and represent an important source of lipids, protein, and metabolizable energy. Although tamarins are reported to commonly consume large‐bodied insects such as grasshoppers and walking sticks (Orthoptera), little is known concerning the degree to which smaller or less easily identifiable arthropod prey comprises an important component of their diet. To better understand tamarin arthropod feeding behavior, fecal samples from 20 wild Bolivian saddleback tamarins (members of five groups) were collected over a 3 week period in June 2012, and analyzed for the presence of arthropod DNA. DNA was extracted using a Qiagen stool extraction kit, and universal insect primers were created and used to amplify a ～280 bp section of the COI mitochondrial gene. Amplicons were sequenced on the Roche 454 sequencing platform using high‐throughput sequencing techniques. An analysis of these samples indicated the presence of 43 taxa of arthropods including 10 orders, 15 families, and 12 identified genera. Many of these taxa had not been previously identified in the tamarin diet. These results highlight molecular analysis of fecal DNA as an important research tool for identifying anthropod feeding patterns in primates, and reveal broad diversity in the taxa, foraging microhabitats, and size of arthropods consumed by tamarin monkeys. Am J Phys Anthropol 156:474–481, 2015. © 2014 Wiley Periodicals, Inc.     

Vertebrate predation by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis

Vertebrate predation was examined in sympatric moustached tamarins (Saguinus mystax) and saddle-back tamarins (Saguinus fuscicollis) in the Amazon rainforest of northeastern Peru. Both species prey on frogs and lizards, and very rarely on nestling birds. As a result of divergent foraging strategies, S. mystax primarily exploited frogs at higher strata of the forest, while S. fuscicollis predominantly preyed on reptiles in the lower strata and on the ground. This difference may strengthen the niche differentiation between these two tamarin species that exists with regard to other prey.     

Fruiting phenology of animal-dispersed plants in response to winter migration of frugivores in a warm temperate forest on Yakushima Island, Japan

The fruiting phenology of animal-dispersed plants was observed in a warm temperate, evergreen forest on Yakushima Island. The number of ripe fruits was counted for 22 trees, four lianas and one parasitic epiphyte species with sapfruit. These fruits were consumed by birds and Japanese macaques (Macaca fuscata yakui). Birds with small gapes (e.g. Japanese white-eye [Zosterops japonica]) consumed only small fruit less than 6 mm in diameter, while birds with large gapes (e.g. red-capped green pigeon [Sphenurus formosae]) and Japanese macaques consumed a wide range of fruits from 4 to 16 mm in diameter. The larger animals did not ignore the smaller fruits. Brown-eared bulbul (Hypsipetes amaurotis) and Japanese white-eye were the main consumers of sapfruit in terms of frequency in winter. Some of the observed consumers were year-round residents, but most of the consumers migrated to Yakushima Island from the main islands of Japan to overwinter (from November to March), and their abundance in winter was four times as high as during the rest of the year (from May to October). In 23 of the 27 plant species investigated, sapfruit production coincided with their immigration season, whereas tree species bear capsules and nuts during autumn from September to November. We suggest that sapfruit species set their ripe period to the season when frugivorous birds are most abundant.     

Habitat Exploitation by Free-ranging Saguinus niger in Eastern Amazonia

We monitored the foraging behavior of the members of a group of black-handed tamarins (Saguinus niger) at a site in eastern Amazonia. Their diet was frugivorous-insectivorous, but also included pod exudate of Parkia pendula. The focal group used all 3 types of forest—primary, logged, and secondary— in all months, but differentially between seasons. In the dry season, tamarins spent more than half of activity time in primary forest and less than a third in secondary forest whereas during the wet season, the proportions were reversed. Data on resource abundance indicated that the shift in habitat preference is related to a seasonal change in the distribution of fruit sources, with a larger number of species and individuals fruiting during the wet season. We recorded no such variation in the abundance of arthropods. While using a larger area, including more secondary forest, during the wet season, the group traveled significantly shorter distances each day, reflecting the availability of a larger number of fruit sources. Overall, the results reemphasize the ecological and behavioral flexibility of Saguinus niger and their ability to cope with habitat disturbance.     

Will travel for food: spatial discounting in two new world monkeys

Nonhuman animals steeply discount the future, showing a preference for small, immediate over large, delayed rewards. Currently unclear is whether discounting functions depend on context. Here, we examine the effects of spatial context on discounting in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus), species known to differ in temporal discounting. We presented subjects with a choice between small, nearby rewards and large, distant rewards. Tamarins traveled farther for the large reward than marmosets, attending to the ratio of reward differences rather than their absolute values. This species difference contrasts with performance on a temporal task in which marmosets waited longer than tamarins for the large reward. These comparative data indicate that context influences choice behavior, with the strongest effect seen in marmosets who discounted more steeply over space than over time. These findings parallel details of each species' feeding ecology. Tamarins range over large distances and feed primarily on insects, which requires using quick, impulsive action. Marmosets range over shorter distances than tamarins and feed primarily on tree exudates, a clumped resource that requires patience to wait for sap to exude. These results show that discounting functions are context specific, shaped by a history of ecological pressures.     

Experimental field study of the relative costs and benefits to wild tamarins (Saguinus imperator and S. fuscicollis) of exploiting contestable food patches as single- and mixed-species troops

Several species of tamarins form stable mixed-species troops in which groups of each species feed, forage, rest, and travel together during much of the year. Although the precise set of factors that facilitate this ecological relationship remains unclear, predator detection and foraging benefits are presumed to play a critical role in maintaining troop stability. In this work we present data from an experimental field study designed to examine how factors such as social dominance and within-patch foraging decisions affect the costs and benefits to tamarins of visiting feeding sites as single- and mixed-species troops. Our data indicate that when they exploited contestable food patches (sets of eight feeding platforms, two of which contained a 100-g banana), each tamarin species experienced foraging costs when they arrived as part of a mixed-species troop. These costs were found to be less severe for emperor tamarins because they were socially dominant to saddle-back tamarins and could displace them at feeding sites. We conclude that the foraging benefits to tamarins residing in mixed-species troops are asymmetrical, and that at feeding sites in which the amount of food in a patch is insufficient to satiate all troop members, even minor differences in the timing of return to food patches and changes in troop cohesion have a measurable effect on the costs and benefits to participating tamarin species.     

Yellow‐chevroned Parakeet (Brotogeris chiriri) abundance and canopy foraging at a dry forest in western Brazil

I studied Brotogeris chiriri abundance and foraging activity at a dry forest of the Urucum mountains in western Mato Grosso do Sul, Brazil, to evaluate their relationships with food resource production. Brotogeris chiriri abundance sharply increased during the early wet season (mainly October 2001) when it mostly foraged for fleshy fruits. At that time Protium heptaphyllum, one of the most common tree species, bore a large crop of fruits, the arils of which were extensively consumed by B. chiriri. Conversely, only a few parakeets were recorded foraging from the late wet to the late dry season, when dry fruit production predominated. The monthly pattern of parakeet abundance paralleled both its monthly pattern of foraging activity and fleshy fruit availability. Moreover, the variations in foraging activity were highly correlated to fleshy fruit production. Thus, data presented here evidenced the effect of both fruiting pulses and a common tree species that produced a large and ephemeral fruit crop, on the dynamic of a small and mobile canopy forager at a primary dry forest.     

Diet, foraging, and use of space in wild golden-headed lion tamarins

Lion tamarins (Callitrichidae: Leontopithecus) are small frugi-faunivores that defend large home ranges. We describe results from the first long-term investigation of wild golden-headed lion tamarins (L. chrysomelas; GHLTs). We present data about activity budgets, daily activity cycles, diet, daily path length, home range size, home range overlap, and territorial encounters for three groups of GHLTs that were studied for 1.5-2.5 years in Una Biological Reserve, Bahia State, Brazil, an area characterized by aseasonal rainfall. We compare our results to those from other studies of lion tamarins to identify factors that may influence foraging and ranging patterns in this genus. Ripe fruit, nectar, insects, and small vertebrates were the primary components of the GHLT diet, and gums were rarely eaten. Fruit comprised the majority of plant feeding bouts, and the GHLTs ate at least 79 different species of plants from 32 families. The most common foraging sites for animal prey were epiphytic bromeliads. The GHLTs defended large home ranges averaging 123 ha, but showed strong affinities for core areas, spending 50% of their time in approximately 11% of their home range. Encounters with neighboring groups averaged two encounters every 9 days, and they were always aggressive. Data about time budgets and daily activity cycles reveal that the GHLTs spent most of their time foraging for resources or traveling between foraging sites distributed throughout their home ranges. The GHLTs spent much less time consuming exudates compared to lion tamarins in more seasonal environments. Additionally, the GHLTs had much larger home ranges than golden lion tamarins (L. rosalia), and did not engage in territorial encounters as frequently as L. rosalia. GHLT ranging patterns appear to be strongly influenced by resource acquisition and, to a lesser extent, by resource defense.     

Fruiting phenology in a tropical dry evergreen forest on the Coromandel coast of India in relation to plant life-forms,physiognomic groups,dispersal modes,and climatic constraints

The fruiting phenology of 22 woody plant species belonging to 19 families was studied with respect to life-forms, physiognomic groups and dispersal modes, for 1 year at monthly intervals, in a tropical dry evergreen forest at Oorani (12°11′N, 79°57′E) on the Coromandel coast of India. At the community level, bimodal fruiting pattern prevailed, with a major peak in the dry season and a minor one in the early rainy season. An annual fruiting pattern was observed in many species and among the studied species fruiting lasted for 2–9 months. There was no significant difference in the frequency of species at three fruiting stages across the life-form categories and many species of upper and lower canopy trees and lianas were in the ripe fruiting phase during the late dry season. Plant physiognomic groups displayed distinct seasonality in fruiting pattern. The fruit maturation period was much longer for the wet season fruiting brevi-deciduous species than evergreen and deciduous species that fruited during the dry season. The variation in timing of fruiting behaviour among zoochorous species demonstrated less seasonality and zoochorous fruits were available throughout the year. Fruiting in anemochorous species peaked during the driest months and dryness favoured the dissemination of seeds. The fruiting patterns observed in the studied tropical dry evergreen forest across various plant traits were comparable with patterns recorded in other tropical seasonal forests.     

Feeding ecology of mandrills (Mandrillus sphinx) in campo animal reserve,Cameroon

A field study on the ecology of mandrills (Mandrillus sphinx) was carried out for 28 months in Cameroon. Fresh food remnants and large quantities of fresh feces were collected by following the groups. Analyses of these products indicated that fruit (including seeds), monocotyledonous plant leaves and insects (especially ants and termites), were frequently eaten. Mandrills mostly ate the plant and animal foods in the lower forest stratum and on the ground. Fallen seeds and monocotyledonous plant leaves were eaten more frequently in the minor fruiting season than in the major fruiting season presumably to compensate for the shortage of fresh fruit during the former. Daily travel distances were shorter during the minor fruiting season than during the major fruiting season, because in the minor fruiting season mandrills forage for small food items, such as the new leaves and piths of monocotyledons and fallen seeds which are sparsely distributed on the ground, while in the major fruiting season they search for widely distributed food such as fruit. The daily pattern of group movement and a food intake experiment suggest that mandrills move and feed continuously throughout the day. Use of fallen seeds and monocotyledonous plant leaves appears to enable mandrills to maintain a terrestrial life in the tropical rain forest. The feeding and ranging characteristics of mandrills are basically similar to those of other baboon species in open land, though their environments differ extremely.     

Foraging ecology and use of space in wild golden lion tamarins (Leontopithecus rosalia)

In this paper we describe the use of space and feeding ecology of seven groups of golden lion tamarins observed for a total of 2,164 hr in Poço das Antas Reserve, Rio de Janeiro, Brazil. Relative to habitat availability in the home ranges of these groups, lion tamarins spent more time than expected in relatively undisturbed swamp forests and less time than expected in more degraded hillside and pasture habitats. Home range area was correlated with group biomass but not group size. Golden lion tamarins fed primarily on fruits and small animal prey, but relied heavily on floral nectar during seasonal periods of relatively low fruit availability. Compared to other New World monkeys, lion tamarins used larger home range areas and exhibited longer daily path lengths than would be predicted by group biomass alone. We suggest that this pattern of foraging and use of space may be explained by the relatively greater availability of cryptic prey and their microhabitats in forests that are flooded and/or have closed canopies than in forests that are in earlier stages of succession where prey may be more susceptible to desiccation during the dry season. Am. J. Primatol. 41:289–305, 1997. © 1997 Wiley-Liss, Inc.     

Resource partitioning among three woodpecker species Dendrocopos spp. during the breeding season

Food composition, prey size utilization and foraging behaviour of three sympatric woodpecker species ( Dendrocopos major, D. medius, D. minor ) were studied in an oak forest near Budapest during the breeding season in 1983 and 1984. Considering these three aspects of feeding, the great spotted woodpecker is a generalist species. Food composition of this species resembled the arthropod supply on the bark of trees more than those of the other two species. The bark of the trees seems to be a relatively unproductive microhabitat in the breeding season, so woodpecker species use, to different degrees, the food supply of the foliage as well. The food and the foraging behaviour of the middle spotted woodpecker show that this species feeds on prey living both on barks and in the foliage; it occupies-an intermediate position between the great and the lesser spotted woodpeckers. Prey size did not correlate with predator size suggesting that woodpeckers adapted not to the summer resources but rather the winter ones.