Saguinus Fuscicollis Research Articles

The ontogeny of the postcranial skeleton in saddle-back tamarins, Leontocebus fuscicollis and callimicos, Callimico goeldii (Callitrichidae, Primates)

Ontogenetic studies of callitrichid anatomy are limited to research focused mainly on postcranial skeleton of adults. The goal of this study is to compare the ontogeny of postcranial skeletal development in Goeldi’s monkeys (i.e., callimico; Callimico goeldii) with the corresponding data on saddle-back tamarins (Leontocebus fuscicollis). The intermembral, humerofemoral, brachial, crural, and ulna-radius indices of callimicos and saddle-back tamarins were calculated and compared among different age classes in order to assess the implications for their ecology and behavior. Ontogenetic trajectories, including age at growth cessation, were also calculated. It is shown that for a given hindlimb length, L. fuscicollis has longer forelimbs compared to C. goeldii, maintaining this proportion across all age classes. A relatively elongated forelimb observed in L. fuscicollis may have a mechanical role in reducing the force of impact when landing on large vertical substrates. In contrast, hindlimb length and pattern of hindlimb development (such as derived features of the ankle that enhance stability) in callimicos appear to play a critical role in propulsion during trunk-to-trunk leaping. These differences may affect niche partitioning, foraging strategies, and substrate use.

Evaluating genital skin color as a putative sexual signal in wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins.

Coevolution between signalers and receivers has played a significant role in the diversity of animal signals and sensory systems. Platyrrhines (monkeys in the Americas) exhibit a remarkable color vision polymorphism that may have been selected by both natural and sexual selection, but sociosexual color signaling among platyrrhines has received almost no attention. Here, we study the color of reproductive skin among different reproductive classes in free-ranging female saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins, modeling color spaces, and contrasts for the different visual systems. We find that the chromatic saturation and luminance of genital color vary between reproductive classes in saddleback tamarins. Chromatic contrast between the vulva and belly is lower in the parous females (PFs) relative to adult but not currently breeding females, while achromatic contrast is higher in PFs in saddleback tamarins relative to nonparous females. However, in emperor tamarins, genital color (saturation, hue, and luminance) does not vary between reproductive classes. Overall, genital skin color variation is present in tamarins and may play a role in sexual signaling. Nevertheless, the patterns are inconsistent between species, suggesting interspecific variation. Future studies should integrate the perceiver's behavioral responses and the physical and social signaling environments into comprehensive studies of communication as well as consider the role and interaction between multiple sensory modalities.

Saguinus mystax(Primates: Callitrichidae)

AbstractSaguinus mystax (Spix, 1823), a callitrichid (tamarin and marmoset family) commonly called the mustached tamarin, is 1 of 12 species in the genus Saguinus. In this large callitrichid (450–650 g), females are slightly heavier than males. It occurs in Brazil and Peru, south of Rio Amazonas from Río Ucayali in the west to Rio Purus in the east, in primary and secondary tierra firma rainforests. The diet consists of fruit pulp, insects, gums, nectar, and small vertebrates. It lives in groups of 3–10 individuals with a male-biased adult sex ratio and has a cooperative breeding system. In areas of sympatry, S. mystax forms mixed-species groups with saddle-back tamarins, Leontocebus. Although captured for the pet trade and sporadically hunted, it is considered “Least Concern” (LC) by the International Union for Conservation of Nature.

On the identity of the tamarin AMNH 98303 ("Saguinus fuscicollis tripartitus"; Primates: Haplorrhini: Simiiformes: Platyrrhini: Callitrichidae).

The American Museum of Natural History houses the skin of a tamarin (AMNH 98303) labelled as Saguinus fuscicollis tripartitus. However, the specimen does not match the phenotype of this taxon, now named Leontocebus tripartitus, nor that of any other known species or subspecies of Leontocebus. In this note, we review past taxonomic revisions of the genus Saguinus – revisions that were largely driven by the contentious species or subspecies status of the golden-mantled saddleback tamarin S. fuscicollis tripartitus – and compare the phenotype of AMNH 98303 with those of other tamarins in the same genus to discuss the possible status of this specimen.

Hematological and biochemical parameters of Spix's Saddleback Tamarin (Leontocebus fuscicollis) raised in captivity.

The Spix's Saddleback Tamarin, Leontocebus fuscicollis is widely distributed across the Amazon region, but is endangered. This species is serving an important role in biomedical research in captivity. However, reference values for hematological and biochemical parameters are required for the proper characterization of the species. It was therefore the objective of our research to establish these parameters taking into consideration sex and body mass differences in healthy adult Spix's saddleback tamarins. Collecting 2 mL of blood from each individual, 20 animals were examined (7 males, 13 females), and hematological and biochemical parameters were determined using commercial kits. Of the sixteen variables measured, only red blood cell (RBC), hemoglobin (Hb) and hematocrit (Ht) values were significantly higher in males (7.12 ± 0.98 106/mm, 14.98 ± 1.25 g/dL and 48.71 ± 4.91%, respectively), while red cell distribution width (RDW) was higher in females (14.58 ± 1.89%). Of the biochemical parameters measured, only gamma-glutamyl transferase (GGT) enzyme showed higher activity in females (8.08 ± 4.87 U/L), and a high glucose concentration range was observed (102.0 to 521.0 mg/dL) for both sexes. These parameters established with reference ranges for healthy adults provide a reliable reference source for the interpretation of laboratory housed saddleback tamarin.

On the trail of primate scent signals: A field analysis of callitrichid scent-gland secretions by portable gas chromatography-mass spectrometry.

Chemosignals are mediators of social interactions in mammals, providing con- and hetero-specifics with information on fixed (e.g., species, sex, group, and individual identity) and variable (e.g., social, reproductive, and health status) features of the signaler. Yet, methodological difficulties of recording and quantifying odor signals, especially in field conditions, have hampered studies of natural systems. We present the first use of the Torion® portable gas chromatography-mass spectrometry (GC-MS) instrument for in situ chemical analysis of primate scents. We collected and analyzed swab samples from the scent glands and skin from 13 groups (57 individuals) of two sympatric species of wild emperor tamarins, Saguinus imperator, and Weddell's saddleback tamarins, Leontocebus weddelli (Callitrichidae). In total, 11 compounds of interest (i.e., probably derived from the animals) could be detected in the samples, with 31 of 215 samples containing at least one compound of interest. The composition of these 31 samples varied systematically with species, group, sex, and breeding status. Moreover, we tentatively identified seven of the compounds of interest as methyl hexanoate, benzaldehyde, ethyl hexanoate, acetophenone, a branched C15 alkane, 4-methoxybenzaldehyde, and hexadecan-1-ol. As the field of primate semiochemistry continues to grow, we believe that portable GC-MS instruments have the potential to help make progress in the study of primate chemosignaling in field conditions, despite limitations that we encountered. We further provide recommendations for future use of the Torion® portable GC-MS for in situ analyses.

Variable infant care contributions in cooperatively breeding groups of wild saddleback tamarins.

Among non-human primates, alloparental infant care is most extensive in callitrichines, and is thought to be particularly costly for tamarins whose helpers may suffer increased energy expenditure, weight loss, and reduced feeding time and mobility. The costs and benefits of infant care likely vary among group members yet very few wild studies have investigated variable infant care contributions. We studied infant care over an 8-month period in four wild groups of saddleback tamarins in Bolivia to evaluate: (a) what forms of infant care are provided, by whom, and when, (b) how individuals adjust their behavior (activity, vigilance, height) while caring for infants, and (c) whether individuals differ in their infant care contributions. We found that infant carrying, food sharing, and grooming varied among groups, and immigrant males-those who joined the group after infants were conceived-participated less in infant care compared to resident males. Adult tamarins fed less, rested more, and increased vigilance while carrying infants. Although we did not detect changes in overall activity budgets between prepartum and postpartum periods, tamarins spent more time scanning their environments postpartum, potentially reflecting increased predation risk to both carriers and infants during this period. Our study provides the first quantitative data on the timing and amount of infant carrying, grooming, and food transfer contributed by all individuals within and among multiple wild groups, filling a critical knowledge gap about the factors affecting infant care, and highlighting evolutionary hypotheses for cooperative breeding in tamarins.

A multiyear survey of helminths from wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins.

The establishment of baseline data on parasites from wild primates is essential to understand how changes in habitat or climatic disturbances will impact parasite-host relationships. In nature, multiparasitic infections of primates usually fluctuate temporally and seasonally, implying that the acquisition of reliable data must occur over time. Individual parasite infection data from two wild populations of New World primates, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, were collected over 3 years to establish baseline levels of helminth prevalence and parasite species richness (PSR). Secondarily, we explored variation in parasite prevalence across age and sex classes, test nonrandom associations of parasite co-occurrence, and assess the relationship between group size and PSR. From 288 fecal samples across 105 individuals (71 saddleback and 34 emperor tamarins), 10 parasite taxa were identified by light microscopy following centrifugation and ethyl-acetate sedimentation. Of these taxa, none were host-specific, Dicrocoeliidae and Cestoda prevalences differed between host species, Prosthenorchis and Strongylida were the most prevalent. Host age was positively associated with Prosthenorchis ova and filariform larva, but negatively with cestode and the Rhabditoidea ova. We detected no differences between expected and observed levels of co-infection, nor between group size and parasite species richness over 30 group-years. Logistic models of individual infection status did not identify a sex bias; however, age and species predicted the presence of four and three parasite taxa, respectively, with saddleback tamarins exhibiting higher PSR. Now that we have reliable baseline data for future monitoring of these populations, next steps involve the molecular characterization of these parasites, and exploration of linkages with health parameters.

Effect of gluten diet on blood innate immune gene expressions and stool consistency in Spix’s Saddleback Tamarin (Leontocebus fuscicollis) raised in captivity

The callitrichids are non-human primates that feed on insects and plant matter in nature, but in captivity, they are fed mostly an artificial diet containing amounts of gluten, in their toxic forms in items such as wheat, barley and rye. The aim of this research was to estimate the blood β-defensin and Toll like receptor 5 (TLR5) gene expressions and to analyze the stool consistency (firm, soft, diarrheic) in Leontocebus fuscicollis raised in captivity. Blood samples of animals under gluten-free and gluten diets were collected and their fecal output quality was periodically monitored and classified during the course of the study. Gene expression was evaluated using real-time PCR. The stool consistencies of individuals fed a gluten diet were most frequently soft or diarrheic, while it was mostly normal in individuals fed a gluten-free diet. β-Defensin expression increased in individuals fed a gluten diet, but decreased after 15days. Expression normalized between 30 and 45days on a gluten-free diet. However, expression of the TLR5 gene did not change under a gluten diet. A gluten diet affects stool quality, and brings about an immediate increase in blood β-defensin expression in the beginning but decreases after 15days.

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.

Classification of producer characteristics in primate long calls using neural networks

Primate long calls are high-amplitude vocalizations that can be critical in maintaining intragroup contact and intergroup spacing, and can encode abundant information about a call's producer, such as age, sex, and individual identity. Long calls of the wild emperor (Saguinus imperator) and saddleback (Leontocebus weddelli) tamarins were tested for these identity signals using artificial neural networks, machine-learning models that reduce subjectivity in vocalization classification. To assess whether modelling could be streamlined by using only factors which were responsible for the majority of variation within networks, each series of networks was re-trained after implementing two methods of feature selection. First, networks were trained and run using only the subset of variables whose weights accounted for ≥50% of each original network's variation, as identified by the networks themselves. In the second, only variables implemented by decision trees in predicting outcomes were used. Networks predicted dependent variables above chance (≥58.7% for sex, ≥69.2 for age class, and ≥38.8% for seven to eight individuals), but classification accuracy was not markedly improved by feature selection. Findings are discussed with regard to implications for future studies on identity signaling in vocalizations and streamlining of data analysis.

Modeling Developmental Class Provides Insights into Individual Contributions to Infant Survival in Callitrichids

Cooperative breeders live in social groups in which individuals in an age–sex class vary in reproductive development due to reproductive dominance by a few individuals in each group. Among callitrichids, adult males have been implicated in driving group reproductive output, but uneven sampling efforts, the underlying effects of group size, and pseudoreplication at the group and species levels are confounding variables in these analyses. We examined the drivers of group reproductive output in callitrichids by 1) conducting a meta-analysis of published studies of callitrichid group composition; 2) assigning developmental class based on reproductive morphology; and 3) using multivariate modeling to test whether the proportion of individuals of each developmental class predicts the presence and the number of surviving offspring among free-ranging Weddell’s saddleback tamarins (Leontocebus weddelli) and emperor tamarins (Saguinus imperator) in Peru. The meta-analysis revealed that the number of adult females and group size, but not the number of adult males, are significantly correlated with group reproductive output. Statistical models of the new dataset revealed that the proportion of primary breeding males, primary breeding females, and group size predicted whether groups had surviving infants, and that only the proportion of primary breeding females and group size predicted the number of surviving infants. Thus, primary breeding males appear to be necessary for groups to raise any infants, but a higher proportion of primary breeding females and a larger group size increase group reproductive output overall.

Chronic Plasmodium brasilianum infections in wild Peruvian tamarins.

There is an increased interest in potential zoonotic malarias. To date, Plasmodium malariae that infects humans remains indistinguishable from Plasmodium brasilianum, which is widespread among New World primates. Distributed throughout tropical Central and South America, the Callitrichidae are small arboreal primates in which detection of natural Plasmodium infection has been extremely rare. Most prior screening efforts have been limited to small samples, the use of low-probability detection methods, or both. Rarely have screening efforts implemented a longitudinal sampling design. Through an annual mark-recapture program of two sympatric callitrichids, the emperor (Saguinus imperator) and saddleback (Saguinus fuscicollis) tamarins, whole blood samples were screened for Plasmodium by microscopy and nested PCR of the cytochrome b gene across four consecutive years (2012–2015). Following the first field season, approximately 50% of the samples collected each subsequent year were from recaptured individuals. In particular, out of 245 samples from 129 individuals, 11 samples from 6 individuals were positive for Plasmodium, and all but one of these infections was found in S. imperator. Importantly, the cytochrome b sequences were 100% identical to former isolates of P. malariae from humans and P. brasilianum from Saimiri sp. Chronic infections were detected as evidenced by repeated infections (7) from two individuals across the 4-year study period. Furthermore, 4 of the 5 infected emperor tamarins were part of a single group spanning the entire study period. Overall, the low prevalence reported here is consistent with previous findings. This study identifies two new natural hosts for P. brasilianum and provides evidence in support of chronic infections in wildlife populations. Given that callitrichids are often found in mixed-species associations with other primates and can be resilient to human-disturbed environments, they could contribute to the maintenance of P. malariae populations if future work provides entomological and epidemiological evidence indicating human zoonotic infections.

Uso y competición por plantas alimenticias entre Pithecia aequatorialis (Primates: Pitheciidae) y otros animales en la Amazonía peruana

En este reporte proporcionamos información sobre plantas alimenticias del huapo negro (Pithecia aequatorialis) y sus competidores en bosque de altura de la microcuenca del río Itaya, Amazonía peruana. De mayo a noviembre del 2009 y de enero a abril del 2010 seguimos silenciosamente a dos grupos familiares con el propósito de registrar las plantas cuyos frutos forman parte de su dieta. Durante los contactos tuvimos 90 eventos alimenticios en 48 especies de plantas agrupadas en 24 familias. De ellas, 36 habitan en bosque de colina baja y el resto en bosque de terraza alta. La mayor diversidad de plantas alimenticias está agrupada en siete familias que en conjunto representaron el 60.4%, sobresaliendo entre ellas las familias Moraceae (8 especies), Fabaceae (6 especies) y Annonaceae (4 especies). Los frutos en su mayoría fueron consumidos en estado maduro, siendo el mesocarpio el más apreciado (40%). Entre los mamíferos, siete de los competidores fueron primates, siendo el principal el pichico pardo (Saguinus lagonotus) y entre las aves el tucán de cuello blanco (Ramphastos tucanus). Finalmente, los frutos de Pseudolmedia laevigata (Moraceae) fueron los más preferidos por los competidores (7 especies de mamíferos y 2 de aves).

Re-description and assessment of the taxonomic status of Saguinus fuscicollis cruzlimai Hershkovitz, 1966 (Primates, Callitrichinae).

Cruz Lima's saddle-back tamarin Saguinus fuscicollis cruzlimai Hershkovitz, 1966, was described from a painting by Eládio da Cruz Lima in his book Mammals of Amazonia, Vol. 1, Primates (1945). The painting was of four saddle-back tamarins from the upper Rio Purus, one of them distinct and the inspiration for Hershkovitz to describe it as a new subspecies. Its exact provenance was unknown, however, and the specimen was lost. Surveys in the Purus National Forest in 2011 resulted in sightings of this tamarin along the north bank of the Rio Inauini, a left-bank tributary of the middle Purus, and also on the left bank of the Purus, north and south of the Rio Inauini. It is possible that it extends north as far as the Rio Pauini, and that S. f. primitivus Hershkovitz, 1977, occurs north of the Pauini as far the Rio Tapauá, both also left-bank tributaries of the Purus. Morphometric and molecular genetic analyses and the coloration of the pelage indicate that this tamarin differs from its neighbors sufficiently to be considered a full species. In his doctoral dissertation [2010, Taxonomy, Phylogeny and Distribution of Tamarins (Genus Saguinus Hoffmannsegg, 1807) Georg-August Universität, Göttingen], C. Matauschek found that saddle-back and black-mantle tamarins diverged from the tamarin lineage around 9.2 million years ago; time enough to warrant their classification in a distinct genus. Leontocebus Wagner, 1840, is the first name available. In this article we re-describe Cruz Lima's saddle-back tamarin. We propose a neotype with a precise locality, and make it a full species in the genus Leontocebus.

Tamarins: Insights into monogamous and non-monogamous single female social and breeding systems.

Tamarins are reported to live in small multimale-multifemale groups characterized by a single breeding female. Here we present information on the composition and genetic relatedness of individuals in 12 wild-trapped groups of Weddell's saddleback tamarins (Saguinus weddelli) from northern Bolivia to determine if groups are best described as nuclear or extended families suggesting social monogamy or whether groups contain several unrelated same sex adults indicative of social polyandry/polygyny. Mean group size was 6.25 including an average of 2.16 adult males (range 1-4) and 2.08 adult females (1-3). No group contained only one adult male and one adult female and 25% of groups contained two parous females. We estimated the genetic relatedness among individuals using 13 polymorphic microsatellite markers. Across the population, mean relatedness was low and not significantly different among adult males versus among adult females, suggesting that both sexes disperse from their natal groups. Adults of both sexes also tended to have close same-sex adult relatives within their groups; relatedness among adult females of the same group averaged 0.31 and among adult males was 0.26. This suggests that tamarins of one or both sexes sometimes delay dispersal and remain as adults in their natal group or that emigration of same-sexed relatives into the same group may be common. Finally, parentage analyses indicated that, whereas the parents of juveniles generally were present in the group, this was not always the case. Based on these data, published reports of the presence of multiple breeding males and occasionally multiple breeding females in the same group, and the fact that less than 10% of groups in the wild contain a single adult male-adult female pair, we argue that social polyandry best characterizes the composition of tamarin groups and that monogamy is not a common mating pattern in Saguinus weddelli or other tamarin species.

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.

Navigating in small‐scale space: The role of landmarks and resource monitoring in understanding saddleback tamarin travel

Recent studies of spatial memory in wild nonhuman primates indicate that foragers may rely on a combination of navigational strategies to locate nearby and distant feeding sites. When traveling in large-scale space, tamarins are reported to encode spatial information in the form of a route-based map. However, little is known concerning how wild tamarins navigate in small-scale space (between feeding sites located at a distance of ≤60 m). Therefore, we collected data on range use, diet, and the angle and distance traveled to visit sequential feeding sites in the same group of habituated Bolivian saddleback tamarins (Saguinus fuscicollis weddelli) in 2009 and 2011. For 7-8 hr a day for 54 observation days, we recorded the location of the study group at 10 min intervals using a GPS unit. We then used GIS software to map and analyze the monkeys' movements and travel paths taken between feeding sites. Our results indicate that in small-scale space the tamarins relied on multiple spatial strategies. In 31% of cases travel was route-based. In the remaining 69% of cases, however, the tamarins appeared to attend to the spatial positions of one or more near-to-site landmarks to relocate feeding sites. In doing so they approached the same feeding site from a mean of 4.5 different directions, frequently utilized different arboreal pathways, and traveled approximately 30% longer than then the straight-line distance. In addition, the monkeys' use of non-direct travel paths allowed them to monitor insect and fruit availability in areas within close proximity of currently used food patches. We conclude that the use of an integrated spatial strategy (route-based travel and attention to near-to-goal landmarks) provides tamarins with the opportunity to relocate productive feeding sites as well as monitor the availability of nearby resources in small-scale space.

Atualização do conhecimento sobre o sauim-de-cara-suja, <i>Saguinus weddelli</i> (Primates, Callitrichinae), no estado de Rondônia

O presente estudo consiste em uma atualização do conhecimento sobre a distribuição geográfica e dados populacionais do sauim-de-cara-suja (Saguinus weddelli) na área situada a leste do rio Madeira, em Rondônia. Foi realizado um levantamento bibliográfico e uma série de expedições aos municípios de Cacoal, Machadinho D'Oeste, Nova Brasilândia D'Oeste, Chupinguaia, São Francisco do Guaporé e Costa Marques. Os resultados indicaram a existência de 39 pontos de registros empíricos de S. weddelli na área de estudo, 31 dos quais foram extraídos da literatura e oito resultaram dos trabalhos de campo. Um dos novos registros situa-se além da distribuição geográfica conhecida, representando uma extensão da mesma. Apesar deste táxon não ser considerado como ameaçado de extinção, sua situação na área de estudo requer cuidados, uma vez que têm sido registrados altos índices de desmatamento nesta região nos últimos 40 anos.

Can Seeds Help to Expel Parasites? A Comment on the Garber-Kitron (1997) Hypothesis

Like many other primates, moustached and saddle-back tamarins (Saguinus mystax and Saguinus nigrifrons; previously Saguinus fuscicollis nigrifrons: Matauschek et al. 2011) are seed dispersers for a large number plant species whose fruits they exploit for food (Culot 2009; Garber 1986; Knogge and Heymann 2003). Tamarins consistently swallow seeds (ca. 95 % of fecal samples contain seeds) that are often very large in relation to the tamarins’ body size (Garber and Kitron 1997; Knogge and Heymann 2003). Mean length and width of seeds (± SD) recovered from feces was 1.75 ± 0.59 cm (maximum: 2.35 cm) and 0.74 ± 0.32 cm (maximum: 1.31 cm) in Saguinus mystax, and 1.74 ± 0.56 cm (maximum: 2.33 cm) and 0.75 ± 0.31 cm (maximum: 1.35 cm) in S. nigrifrons (Knogge and Heymann 2003). Heymann (1992) speculated that large seeds may function physiologically as a kind of “roughage” and that the lack of continuous gut stimulation may be one cause of the high prevalence of gastrointestinal diseases in captive tamarins (Clapp et al. 1988; Gozalo and Montoya 1992), which contrasts to the low prevalence in wild tamarins (Wood et al. 1989). Seeds do not provide a nutritional benefit but rather are ballast that occupies much space in the gastrointestinal tract (Garber and Kitron 1997). Therefore, seeking an adaptive explanation of seed swallowing, Garber and Kitron (1997) proposed dislodging and expelling intestinal parasites, particularly the highly damaging acanthocephalan hookworm Prosthenorchis elegans, as the major function. Huffman (1997; see also Huffman and Caton 2001; Huffman et al. 1996) and Wrangham (1995) had provided evidence for the mechanical expulsion of parasites through swallowing of entire leaves in chimpanzees (Pan troglodytes). Garber and Kitron (1997) based their argument on the high prevalence (and lethality; Cosgrove et al. 1968) of Prosthenorchis elegans infections in captive tamarins and low prevalence in the wild. Under the Garber–Kitron hypothesis, the following predictions can be made: At the group level, the prevalence of infections with Prosthenorchis elegans should correlate negatively with the proportion of fecal samples per group that contain seeds. At the individual level, individuals infected with Prosthenorchis elegans should swallow seeds more often than noninfected individuals. Because rates of seed swallowing itself are difficult to determine, I use the number of fecal samples per individual containing seeds as a surrogate variable. I used data from field studies of a population of Saguinus mystax and S. nigrifrons at the Estacion Biologica Quebrada Blanco (EBQB), in northeastern Peruvian Amazonia since 1994 to test these predictions.