The gut microbiome and metabolome of saddleback tamarins (Leontocebus weddelli): Insights into the foraging ecology of a small‐bodied primate

Body mass is a strong predictor of diet and nutritional requirements across a wide range of mammalian taxa. In the case of small‐bodied primates, because of their limited gut volume, rapid food passage rate, and high metabolic rate, they are hypothesized to maintain high digestive efficiency by exploiting foods rich in protein, fats, and readily available energy. However, our understanding of the dietary requirements of wild primates is limited because little is known concerning the contributions of their gut microbiome to the breakdown and assimilation of macronutrients and energy. To study how the gut microbiome contributes to the feeding ecology of a small‐bodied primate, we analyzed the fecal microbiome composition and metabolome of 22 wild saddleback tamarins (adult body mass 360–390 g) in Northern Bolivia. Samples were analyzed using high‐throughput Illumina sequencing of the 16 S rRNA gene V3‐V5 regions, coupled with GC‐MS metabolomic profiling. Our analysis revealed that the distal microbiome of Leontocebus weddelli is largely dominated by two main bacterial genera: Xylanibacter and Hallella (34.7 ± 14.7 and 22.6 ± 12.4%, respectively). A predictive analysis of functions likely carried out by bacteria in the tamarin gut demonstrated the dominance of membrane transport systems and carbohydrate metabolism as the predominant metabolic pathways. Moreover, given a fecal metabolome composed mainly of glucose, fructose, and lactic acid (21.7 ± 15.9%, 16.5 ± 10.7%, and 6.8 ± 5.5%, respectively), the processing of highly fermentable carbohydrates appears to play a central role in the nutritional ecology of these small‐bodied primates. Finally, the results also show a potential influence of environmentally‐derived bacteria in colonizing the tamarin gut. These results indicate high energetic turnover in the distal gut of Weddell's saddleback tamarin, likely influenced by dominant bacterial taxa that facilitate dietary dependence on highly digestible carbohydrates present in nectar, plant exudates, and ripe fruits.     

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.     

Predation on Orthoptera and other orders in insects by tamarin monkeys, Saguinus mystax mystax and Saguinus fuscicollis nigrifrons (Primates: Callitrichidae), in north-eastern Peru

Kaytydids and related insects are an important component in the diets of moustached ( Saguinus mystax mystax ) and saddle-back tamarins ( Saguinus fuscicollis nigrifrons ). Based on preliminary data of captured prey, trends suggest that partitioning occurs regarding orthopterans as a limited food resource. Of species caputre as prey, only three were shared by both tamarin species. Saddle-back tamarins appeared to specialize more on understorey species (0-4 m), concentrating on pseudophylline katydids. Moustached tamarins incorporated a greater percentage of phaneropterine katydids from the lower to middle canopy into their diet of insects. Although most prey species were exposed to view during the diurnal feeding period of the tamarins, only the saddle-back tamarin fed on katydids that spend the day concealed from view within dead curled leaves. Differentiation of the prey spectrum may represent a critical pattern of niche differentiation in these two sympatric tamarin species, which show a high overlap in their plant food resources.     

Feeding ecology of Saguinus bicolor bicolor (Callitrichidae: Primates) in a relict forest in Manaus, Brazilian Amazonia.

This study is part of a long-term ecological study of habitat and dietary requirements of the pied bare-face tamarin (Saguinus bicolor bicolor). One group was studied for 11 months in an area of secondary forest in a suburb of Manaus, Amazonas, Brazil. Three main vegetation types occurred inside the group's home range (12 ha): capoeira, older secondary forest and campinarana (white sand forest). The tamarins ate fruits (21 species), flowers (1 species), exudates (4 species), and arthropods (insects and spiders). They spent 14.3% of total activity time seeking and eating animal prey, and 9.9% feeding on plant material, mostly fruits. In general, fruits consumed were ripe, small and succulent. Trees used for feeding were low and had small crown diameters. Three plant species (Protium aracouchinni, Myrcia cf. fallax, and Couma utilis) were used intensively during the three seasons covered by the study period. The concentrated use of 3 fruit species, each for an extended period (one fruiting species per season), provided the tamarins with a regular food supply. Tamarins consumed exudates from holes in the bark of trees of the families Anacardiaceae and Vochysiaceae, as well as gum exuded from seed pods of Mimosaceae. Exudates were exploited during the dry season and at the beginning of the wet season. Group travel was primarily based on routes connecting the fruiting trees exploited, with foraging for animal prey occurring during travel. Tamarins searched for arthropods on trunks, branches and leaves and in trunk holes. The foraging and feeding tactics displayed by S. b. bicolor are closely linked to morphological characteristics (small size and weight, claw-like nails) that allowed access to energy-rich resources (arthropods and plant exudates) in different strata of the vegetation.     

Hand specialization, sympatry, and mixed-species associations in callitrichines

Hand morphology in callitrichines (i.e., tamarins, marmosets, and Goeldi's monkey) is correlated with positional and foraging behaviors. This study examines hand shape in callitrichines using an allometric approach. It addresses a series of questions relating hand anatomy, insect foraging behavior, and resource partitioning in callitrichines. The main questions are: 1. Do the hands of Leontopithecus differ in shape from all other callitrichine taxa allowing it to perform highly manipulative prey foraging behaviors? 2. Are the hands of Saguinus fuscicollis adapted to manipulative foraging, and are they functionally similar to Leontopithecus' hands? 3. Is hand morphology in S. fuscicollis more similar to the hand morphology of sympatric tamarin species with whom it does not form mixed species troops (S. nigricollis and S. tripartitus) than to those sympatric tamarin species with whom it does form mixed troops (S. mystax, S. labiatus, and S. imperator)? Measurements of hand length (HL), width (HW), and thickness (HT) were taken from 1350 museum specimens of callitrichines (Callithrix, Cebuella, Leontopithecus, Saguinus, and Callimico), squirrel monkeys (Saimiri), and owl monkeys (Aotus). The analysis indicates that hand shape covaries with foraging strategy. Specifically, the hands of Leontopithecus are adapted for manipulative foraging and are relatively longer and more slender than the hands of other callitrichines. A similar pattern is observed in the hands of S. fuscicollis, S. tripartitus and S. nigricollis. These latter species, however, differ significantly in shape from all other tamarin species. Large differences in hand morphology are observed among tamarin species that form mixed-species troops. These anatomical differences may permit resource partitioning and coexistence among these closely related taxa. Hand shape, expressed as log HLGM (logged hand length divided by the geometric mean of all measurements), is a good predictor of manipulative and non-manipulative prey foraging techniques employed by callitrichines.     

Hemiparasites drive heterogeneity in litter arthropods: Implications for woodland insectivorous birds

Providing fruit, nectar, leaves and litter, mistletoes represent important resources for many organisms, linking above‐ground patterns with below‐ground processes. Here, we explore how mistletoe litter affects arthropod availability, especially those taxa preferentially consumed by ground‐feeding insectivorous birds, a group that has undergone widespread declines. We estimated the influence of mistletoe on arthropod occurrence by sampling arthropod communities beneath infected and uninfected trees with pit‐fall traps. Then, we experimentally isolated direct effects of mistletoe litter on arthropods with a litterbag study. Soil arthropod communities beneath infected trees had consistently greater abundance and biomass – total arthropods and the subset of arthropods preferentially consumed by ground‐foraging insectivores – compared to otherwise comparable uninfected trees. Arthropods showed a weak response to litter addition, with maximum abundances recorded from bags with low mistletoe litter, significantly lower abundances associated with higher mistletoe fractions and pure tree litter (after 5 months). Our findings confirm that mistletoe occurrence has a significant positive impact on arthropod availability, especially on those preferred by ground‐foraging bird insectivores. However, only a minor part of this impact is due to the direct, short‐term effects of mistletoe litter, which suggests that additional mistletoe‐mediated effects (e.g. local changes in structural or microclimatic factors, cumulative effects over multiple years) play significant roles. By altering arthropod assemblages within leaf litter and increasing the heterogeneity of resource availability on forest floors, mistletoe plays an important role in improving habitat quality for declining insectivores.     

Foraging and Spatial Memory in Wild Weddell’s Saddleback Tamarins (Saguinus fuscicollis weddelli) When Moving Between Distant and Out-of-Sight Goals

Two main types of cognitive maps, route-based and coordinate-based, have been proposed to explain how animals navigate through their environments. We examined patterns of feeding and ranging in Weddell’s saddleback tamarins (Saguinus fuscicollis weddelli) in northern Bolivia to assess which type of cognitive map best explains the tamarins’ movement patterns in large-scale space, e.g., when moving between distant and out-of-sight goals. We observed the tamarins for 236 h over the course of 32 d and used a GPS unit to record the location of nighttime sleeping sites and feeding trees and the locations of individuals at 10-min intervals. Based on an evaluation of 109 travel segments of >20 m in which the monkeys traveled from the tree of one major feeding species to another without stopping to rest, forage for insects, or interact with neighbors, we calculated a circuity index (actual distance traveled divided by the straight-line distance) of 1.43. We also plotted the monkeys’ daily movement patterns using GIS software. These analyses showed that tamarin travel was not random, that a limited set of route segments (N?=?29) was reused on multiple occasions, and that certain areas of the forest appeared to serve as switch points (N?=?9) where the monkeys reoriented travel. These results support the contention that the tamarins encoded the spatial relationships among many feeding and sleeping sites in their home range, and navigated in large-scale space using a route-based spatial representation. These results are consistent with those reported for a variety of primate taxa, suggesting that many primate species reuse a familiar set of travel routes and switch points to orient in large-scale space.     

Modeling monkeys: A comparison of computer-generated and naturally occurring foraging patterns in two species of neotropical primates

We present a series of computer-generated foraging models (random movement, olfactory navigation, and spatial memory) designed to examine the manner in which sensory cues and cognitive skills might be used by rainforest monkeys to locate patchily distributed feeding sites. These simulations are compared with data collected in the Amazon Basin of northeastern Peru on the foraging patterns of two species of neotropical primates, the moustached tamarin monkey (Saguinus mystax) and the saddle-back tamarin monkey (Saguinus fuscicollis). The results indicate that, although tamarins may rely on olfactory cues to locate nearby feeding sites, their foraging patterns are better explained by an ability to maintain a detailed spatial map of the location and distribution of hundreds of feeding trees in their home range. There is evidence that such informationis retained for a period of at least several weeks and is used to minimize the distance traveled between widely scattered feeding sites. The use of computer simulations provides a powerful research tool for generating predictive models regarding the role of memory and sensory cues in animal foraging patterns.     

Relative efficiency of fecal versus regurgitated samples for assessing diet and the deleterious effects of a tartar emetic on migratory birds

ABSTRACT We describe the deleterious effects of using an antimony potassium tartrate emetic to obtain diet samples from birds, and compare information obtained from regurgitated samples versus fecal samples in describing diets of autumn migrants. We also examined dose effectiveness in captive Dark‐eyed Juncos (Junco hyemalis) subjected to the same emetic technique used in the field. Over 70% of migrants given an emetic at a study site in Idaho regurgitated useful samples. For 5 of 7 species analyzed, regurgitated samples produced significantly more arthropods per sample than fecal samples, and one species, Warbling Vireo, showed higher numbers of distinct arthropod taxa per sample. In most species, regurgitated samples accumulated arthropod taxa more quickly than fecal samples. However, increasing the number of fecal samples by 5–17 produced a similar number of taxa. Diet composition based on fecal versus regurgitated samples was generally similar, but there were significant differences. Two of 130 treated migrants died soon after treatment. Recapture frequency for treated birds was less than half that for untreated birds, but it is not clear whether this difference was due to treatment‐related mortality or emigration. Each treated bird that we recaptured had lost mass and this suggests a deleterious effect because untreated migrants tended to gain mass. In captivity, 18 Dark‐eyed Juncos were treated with emetic: 6 with the full mass‐specific recommended dose, 6 with half the recommended dose, and the final 6 with one quarter the recommended dose. All were alive 15–20 min posttreatment (recommended release time), but 17 of 18 died within 30 min after receiving the emetic. Together, our data suggest that although the emetic technique may be slightly more information‐rich in assessing diet, it is more harmful than previously reported especially in certain species and should be used only after adequate consideration of the immediate mortality and short‐term physiological effects on birds to be studied.     

An improved method for utilizing high‐throughput amplicon sequencing to determine the diets of insectivorous animals

DNA analysis of predator faeces using high‐throughput amplicon sequencing (HTS) enhances our understanding of predator–prey interactions. However, conclusions drawn from this technique are constrained by biases that occur in multiple steps of the HTS workflow. To better characterize insectivorous animal diets, we used DNA from a diverse set of arthropods to assess PCR biases of commonly used and novel primer pairs for the mitochondrial gene, cytochrome oxidase C subunit 1 (COI). We compared diversity recovered from HTS of bat guano samples using a commonly used primer pair “ZBJ” to results using the novel primer pair “ANML.” To parameterize our bioinformatics pipeline, we created an arthropod mock community consisting of single‐copy (cloned) COI sequences. To examine biases associated with both PCR and HTS, mock community members were combined in equimolar amounts both pre‐ and post‐PCR. We validated our system using guano from bats fed known diets and using composite samples of morphologically identified insects collected in pitfall traps. In PCR tests, the ANML primer pair amplified 58 of 59 arthropod taxa (98%), whereas ZBJ amplified 24–40 of 59 taxa (41%–68%). Furthermore, in an HTS comparison of field‐collected samples, the ANML primers detected nearly fourfold more arthropod taxa than the ZBJ primers. The additional arthropods detected include medically and economically relevant insect groups such as mosquitoes. Results revealed biases at both the PCR and sequencing levels, demonstrating the pitfalls associated with using HTS read numbers as proxies for abundance. The use of an arthropod mock community allowed for improved bioinformatics pipeline parameterization.     

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.     

Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae.

Primates of the subfamily Callitrichinae (Callimico, Callithrix, Leontopithecus, and Saguinus) are small-bodied New World monkeys (105-700 g) possessing clawlike nails on all manual and pedal digits excluding the hallux. Specialized nails in these genera serve a critical function in feeding by enabling tamarins and marmosets to cling to trunks and other large vertical supports while exploiting food resources. Within the subfamily, there is evidence of at least four distinct large-branch feeding patterns. These include (1) seasonal exudate feeding and occasional trunk foraging (many Saguinus spp.); (2) exploitation of bark surface insects and the use of trunks as a platform to locate terrestrial prey (Saguinus fuscicollis, S. nigricollis, and Callimico); (3) manipulative foraging and bark stripping to locate concealed insects and small vertebrates (Leontopithecus); and (4) tree gouging and year-round exudate feeding (many Callithrix). Large-branch feeding and the use of vertical clinging postures appear to be a primary adaptation among virtually all callitrichines, distinguishing them ecologically from other platyrrhine taxa. Given the anatomy and behavior of extant callitrichines, Saguinus appears to be the most ecologically generalized member of this subfamily, and species of this genus may provide useful models for reconstructing the feeding and foraging adaptations of early callitrichines.     

Ecological distinctions between sympatric species of Saguinus and Sciurus

Tamarins are small New World monkeys that have been described as "squirrellike." Squirrels, along with bats and birds, are the taxa most likely to utilize resources similar to those used by primates in the tropical forest canopy. In this paper we compare differences in ecology, diet, locomotion, and habitat utilization between sympatric populations of tamarins (Saguinus oedipus) and tree squirrels (Sciurus granatensis) in Panama. Data presented indicate that although there is some degree of resource overlap, patterns of habitat utilization differ significantly. Rather than being "squirrellike," the Panamanian tamarin exhibits a pattern of locomotor and feeding behavior consistent with that found in other arboreal primates.     

Lake‐derived midges increase abundance of shoreline terrestrial arthropods via multiple trophic pathways

Aquatic insects link adjacent ecosystems by transporting nutrients, energy, and material as they move from bodies of water into terrestrial habitats. Insects emerging from streams and rivers are known to benefit arthropod predators such as spiders, but their influence may extend to other arthropod feeding groups as well. We conducted a terrestrial arthropod survey at a series of lakes spanning a strong gradient of midge (Chironomidae, Diptera) emergence. These small, short‐lived insects reach high densities in some areas such that their carcasses litter the ground, and serve as a potential resource for non‐predatory arthropods. Our study revealed that arthropod assemblages in areas of high midge density were significantly different from those with few midges, the result of an increase of all taxa rather than changes in taxonomic composition. Eight of nine terrestrial arthropod taxa sampled showed a strong positive response to the presence of midges including detritivores and herbivores in addition to predators. Taxa that could consume living or dead midges directly responded especially strongly to midge gradients. Our results strongly suggest that midges enter the terrestrial arthropod food web through multiple pathways, increasing numbers of a wide range of arthropods. Furthermore, they emphasize the importance of lakes as sources of aquatic insects that significantly alter processes in the neighboring terrestrial environment.     

Proposed nutritional importance of plant exudates in the diet of the Panamanian Tamarin,Saguinus oedipus geoffroyi

Data collected on the feeding behavior of Saguinus oedipus geoffroyi(Panamanian tamarin) in Panama show that plant exudates, as well as insects and fruits, are a major component of the diet. During the months of May, June, and July, tamarins were observed clinging to the trunks of Anacardium excelsum(Anacardiaceae) while feeding on exudates. These observations accounted for greater than 14% of the total feeding time of this primate. Nutritional analyses indicate that Anacardiumexudates provide these tamarins with a rich source of the mineral calcium as well as protein, carbohydrates, and water. The seasonal pattern of exudate feeding observed in S. oedipusappears to coincide with certain nutritionally sensitive periods of the reproductive cycle and may serve to offset a potential mineral imbalance incurred during the terminal phase of gestation and lactation.     

Body weights in mixed species troops of Saguinus mystax mystax and Saguinus fuscicollis nigrifrons in Amazonian Peru

An investigation of body weights of members of mixed species troops of Saguinus mystax mystax and Saguinus fuscicollis nigrifrons was conducted at the Rio Blanco Research Station in northeastern Peru. A total of 107 adult and subadult tamarin monkeys were trapped, measured, and released. Data collected indicate that mean body weights for adult male and female moustached tamarins are 564 gm and 626 gm, respectively, whereas for adult saddle-back tamarins these values are 412 gm and 411 gm. Subadults weighed 11-27% less than adults. Body weights recorded in this study are significantly greater than those previously reported for tamarins of the same species and age living in other areas of Amazonian Peru. We hypothesize that, in the case of moustached and saddle-back tamarins, advantages associated with feeding and foraging in mixed species troops facilitate greater efficiency in resource monitoring and result in the maintenance of larger body weights.     

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.     

Lipid content of terrestrial arthropods in relation to body size,phylogeny, ontogeny and sex

Energy storage in arthropods has important implications for survival and reproduction. The lipid content of 276 species of adult arthropods with wet mass in the range 0.2–6.13 g is determined to assess how lipid mass scales with body mass. The relative contribution of lipids to total body mass is investigated with respect to phylogeny, ontogeny and sex. The lipid content of adult insects, arachnids, and arthropods in general shows an isometric scaling relationship with respect to body mass (M) (M_{arthropod lipid} = ?1.09 ×M_dry^1.01 and M_{arthropod lipid} = ?1.00 ×M_lean^0.98). However, lipid allocation varies between arthropod taxa, as well as with sex and developmental stage within arthropod taxa. Female insects and arachnids generally have higher lipid contents than males, and larval holometabolous insects and juvenile arachnids have higher lipid contents than adults.     

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.