Saguinus Imperator Research Articles

Taxonomic status of Tamarinus imperator subgrisescens (Lönnberg, 1940) (Cebidae, Callitrichinae)

The emperor tamarin, Tamarinus imperator, is composed of two subspecies, the nominal type, T. i. imperator, distributed between the Acre and Purus Rivers, whose range is limited between the Brazilian state of Acre and Peru are unbounded, and T. i. subgrisescens, occurring in Peru, Bolivia, and Brazil, in the Brazilian states of Acre and Amazonas. Morphologically, both taxa are easily identifiable by the pelage pattern (chromogenetic fields), and even being easily distinguishable, both lineages are considered subspecies according to the criterion based on the Biological Concept of Species from the 1970s, even without presenting some necessary criteria, such as the intergradation zone. Here we analyzed pelage traits, cranial morphometry, Cytochrome-b divergence, and distributional pattern data applying the premises of integrative taxonomy to elucidate the taxonomic status of both lineages. We hypothesize that both lineages are considered full species through a series of criteria for species recognition, such as distinguishability, level of phenotypical divergences of several morphological complexes with congruence among them, and some genetic divergence. The hybridization is unknown and the low or the lack of sampling in target areas does not allow us to determine whether a hybridization or even contact zone between the two lineages exists indeed. All character sets analyzed were congruent with each other and reinforced the high level of divergences between the two subspecies including several pelage differences, morphometry (descriptive statistics, PCA, and MANOVA), and mitochondrial DNA Cytochrome-b divergence. Most of the distribution in both lineages are allopatric, and the levels of intra-lineage phenotypical variation are much lower than between the lineages.

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.

Color preference and manual laterality in the emperor tamarin (Saguinus imperator).

The current research focuses on color preference between red and green stimuli and manual laterality in the emperor tamarin (Saguinus imperator). Trichromacy in primates has been related to a foraging advantage allowing frugivore primates to distinguish ripe from unripe fruits as well to socio-sexual communication, as trichromats would be advantaged in recognizing social and sexual signals. As warm colors can affect the emotive state of the subjects, leading to the activation of one hemisphere over the other (e.g., right hemisphere), this could lead to behavioral lateralization. Thus, studying of hand preference may be relevant when testing color preference. Nine adult zoo emperor tamarins were involved and the study aimed to investigate the preference between red, green, and white cones as well as manual laterality. Tamarins were provided with pairs of red-green, red-white, and green-white combinations of cones. Ten 30-minsessions per combination were carried out and data on the interaction with one of the two cones of each apparatus were collected to assess subjects' color preference. We also recorded the hand used by each subject during the interaction with cones of different colors and the position of the apparatus in respect to the tamarin. We found no preferences for colored versus white cones. Similarly, we reported no group-level preferences within different color combinations, whereas individual-level preferences were found when considering all choices. Finally, we found that red cones elicited a left-hand preference, suggesting a right-hemisphere involvement in the presence of red cones. Although we do not have genetic data on trichromat and dichromat females, the tendency to use the left hand when interacting with red stimuli provides further evidence that warm colors can influence the emotive state of the perceiver, affecting their manual lateralization.

The mitochondrial genome and Epigenome of the Golden lion Tamarin from fecal DNA using Nanopore adaptive sequencing

BackgroundThe golden lion tamarin (Leontopithecus rosalia) is an endangered Platyrrhine primate endemic to the Atlantic coastal forests of Brazil. Despite ongoing conservation efforts, genetic data on this species remains scarce. Complicating factors include limitations on sample collection and a lack of high-quality reference sequences. Here, we used nanopore adaptive sampling to resequence the L. rosalia mitogenome from feces, a sample which can be collected non-invasively.ResultsAdaptive sampling doubled the fraction of both host-derived and mitochondrial sequences compared to sequencing without enrichment. 258x coverage of the L. rosalia mitogenome was achieved in a single flow cell by targeting the unfinished genome of the distantly related emperor tamarin (Saguinus imperator) and the mitogenome of the closely related black lion tamarin (Leontopithecus chrysopygus). The L. rosalia mitogenome has a length of 16,597 bp, sharing 99.68% sequence identity with the L. chrysopygus mitogenome. A total of 38 SNPs between them were identified, with the majority being found in the non-coding D-loop region. DNA methylation and hydroxymethylation were directly detected using a neural network model applied to the raw signal from the MinION sequencer. In contrast to prior reports, DNA methylation was negligible in mitochondria in both CpG and non-CpG contexts. Surprisingly, a quarter of the 642 CpG sites exhibited DNA hydroxymethylation greater than 1% and 44 sites were above 5%, with concentration in the 3′ side of several coding regions.ConclusionsOverall, we report a robust new mitogenome assembly for L. rosalia and direct detection of cytosine base modifications in all contexts.

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.

Scent Marks Signal Species, Sex, and Reproductive Status in Tamarins (Saguinus spp., Neotropical Primates).

Olfactory communication is an important mediator of social interactions in mammals, thought to provide information about an individual’s identity and current social, reproductive, and health status. In comparison with other taxa such as carnivores and rodents, few studies have examined primate olfactory communication. Tamarins (Callitrichidae) conspicuously deposit odorous secretions, produced by specialized scent glands, in their environment. In this study, we combined behavioral and chemical data on captive cotton-top tamarins, Saguinus oedipus, and bearded emperor tamarins, S. imperator subgrisescens, to examine the role of olfactory communication in the advertisement of species, sex, and reproductive status. We observed no difference in scent-marking behavior between species; however, females marked more frequently than males, and reproductive individuals more than non-reproductive ones. In addition, tamarins predominantly used their anogenital gland when scent-marking, followed by the suprapubic gland. We collected swabs of naturally deposited tamarin anogenital scent marks, and analyzed these samples using headspace gas chromatography-mass spectrometry. Despite a limited sample size, we established differences in tamarin anogenital mark chemical composition between species, sex and reproductive status, and identified 41 compounds. The compounds identified, many of which have been reported in previous work on mammalian semiochemistry, form targets for future bioassay studies to identify semiochemicals. Our non-invasive method for collecting deposited scent marks makes it a promising method for the study of olfactory communication in scent-marking animal species, applicable to field settings and for the study of elusive animals.

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.

Bifidobacterium primatium sp. nov., Bifidobacterium scaligerum sp. nov., Bifidobacterium felsineum sp. nov. and Bifidobacterium simiarum sp. nov.: Four novel taxa isolated from the faeces of the cotton top tamarin (Saguinus oedipus) and the emperor tamarin (Saguinus imperator)

Four novel Gram-stain-positive, non spore forming and fructose-6-phosphate phosphoketolase-positive strains were isolated from the faeces of a cotton top tamarin (Saguinus oedipus) and an emperor tamarin (Saguinus imperator). Phylogenetic analyses based on 16S rRNA revealed that bifidobacterial strains TRE 1T exhibit close phylogenetic relatedness to Bifidobacterium catulorum DSM 103154 (96.0%) and Bifidobacterium tissieri DSM 100201 (96.0%); TRE DT and TRE HT were closely related to Bifidobacterium longum subsp. longum ATCC 15708T with similarity values of 97.4% and 97.5%, respectively; TRI 7T was closely related to Bifidobacterium tissieri DSM 100201 (96.0%). The Average Nucleotide Identity (ANI) and in silico DDH (isDDH) analysis with closest neighbour supported an independent phylogenetic position of all strains with values ranged from 74 to 85% for ANI and from 24 to 28% for isDDH. DNA base composition of the four strains was in the range of 58.3–63.5mol% G+C. Based on the phylogenetic, genotypic and phenotypic data, the strains TRE 1T, TRE DT, TRE HT and TRI 7T clearly represent four novel taxa within the genus Bifidobacterium for which the names Bifidobacterium primatium sp. nov. (type strain TRE 1T=DSM 100687T=JCM 30945T), Bifidobacterium scaligerum sp. nov. (type strain TRE DT=DSM 103140T=JCM 31792T), Bifidobacterium felsineum sp. nov. (type strain TRE HT=DSM 103139T=JCM 31789T) and Bifidobacterium simiarum sp. nov. (type strain TRI 7T=DSM 103153T=JCM 31793) are proposed.

Phylogenetic classification of six novel species belonging to the genus Bifidobacterium comprising Bifidobacterium anseris sp. nov., Bifidobacterium criceti sp. nov., Bifidobacterium imperatoris sp. nov., Bifidobacterium italicum sp. nov., Bifidobacterium margollesii sp. nov. and Bifidobacterium parmae sp. nov.

Six Bifidobacterium strains, i.e., Goo31D, Ham19E, Rab10A, Tam1G, Uis4E and Uis1B, were isolated from domestic goose (Anser domesticus), European hamster (Cricetus cricetus), European rabbit (Oryctolagus cuniculus), emperor tamarin (Saguinus imperator) and pygmy marmoset (Callithrix pygmaea). Cells are Gram-positive, non-motile, non-sporulating, facultative anaerobic and fructose 6-phosphate phosphoketolase-positive. Phylogenetic analyses based on 16S rRNA, ITS-, multilocus- sequences and the core genome revealed that bifidobacterial strains Goo31D, Ham19E, Rab10A, Tam1G, Uis4E and Uis1B exhibit close phylogenetic relatedness with Bifidobacterium choerinum LMG 10510, Bifidobacterium hapali DSM 100202, Bifidobacterium saguini DSM 23967 and Bifidobacterium stellenboschense DSM 23968. Genotyping based on the genome sequence of the isolated strains combined with phenotypic analyses, clearly show that these strains are distinct from each of the type strains of the so far recognized Bifidobacterium species. Thus, Bifidobacterium anseris sp. nov. (Goo31D=LMG 30189T=CCUG 70960T), Bifidobacterium criceti sp. nov. (Ham19E=LMG 30188T=CCUG 70962T), Bifidobacterium imperatoris sp. nov. (Tam1G=LMG 30297T=CCUG 70961T), Bifidobacterium italicum sp. nov. (Rab10A=LMG 30187T=CCUG 70963T), Bifidobacterium margollesii sp. nov. (Uis1B=LMG 30296T=CCUG 70959T) and Bifidobacterium parmae sp. nov. (Uis4E=LMG 30295T=CCUG 70964T) are proposed as novel Bifidobacterium species.

Bifidobacterium callitrichidarum sp. nov. from the faeces of the emperor tamarin (Saguinus imperator).

Three Gram-stain-positive, non-spore-forming, microaerophilic and fructose-6-phosphate phosphoketolase positive strains were isolated from a faecal sample of an adult subject of the emperor tamarin (Saguinus imperator). Given that the isolates revealed identical BOX PCR profiles, strain TRI 5T was selected as a representative and characterized further. Comparative analysis of 16S rRNA gene sequence similarity revealed that strain TRI 5T was closely related to Bifidobacterium saguini DSM 23967T (96.4 %) and to Bifidobacterium longum subsp. longum ATCC 15708 (96.2 %). Multilocus sequence analyses of five housekeeping genes showed the close phylogenetic relatedness of this strain to Bifidobacterium breve DSM 20213T (hsp60 94.1 %), Bifidobacterium saguini DSM 23967T (clpC 91 %), Bifidobacterium avesanii DSM 100685T (dnaG 80.3 %), Bifidobacterium longumsubsp. infantis ATCC 15697T (dnaJ 85.3 %) and Bifidobacterium longumsubsp. longum ATCC 15708 (rpoB 93 %), respectively. The peptidoglycan type was A3β, with an interpeptide bridge comprising l-Orn (Lys) - l-Ser - l-Ala - l-Thr - l-Ala. The DNA G+C content of strain TRI 5T was 60.9 mol%. Based on the data provided, strain TRI 5T represents a novel species of the genus Bifidobacterium for which the name Bifidobacteriumcallitrichidarum sp. nov. is proposed. The type strain is TRI 5T (=DSM 103152T=JCM 31790T).

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.

Bifidobacterium vansinderenii sp. nov., isolated from faeces of emperor tamarin (Saguinus imperator).

A novel Bifidobacterium strain, Tam10BT, i.e. LMG 30126T, was isolated from emperor tamarin (Saguinus imperator). Cells were Gram-positive, non-motile, non-sporulating, non-haemolytic, facultative anaerobic and fructose 6-phosphate phosphoketolase-positive. Phylogenetic analyses based on 16S rRNA genes as well as multilocus sequences (representing hsp60, rpoB, dnaJ, dnaG and clpC genes) and the core genome revealed that Bifidobacterium Tam10BT exhibited close phylogenetic relatedness to Bifidobacterium tissieri DSM 100201T. Comparative analysis of 16S rRNA gene sequences confirmed the phylogenetic results showing the highest gene sequence identity with strain B. tissieri DSM 100201T (96.5 %). Furthermore, genotyping based on the genome sequence of Tam 10B, in combination with phenotypic analyses, clearly showed that strain Tam10BT is distinct from each of the type strains of the so far recognized Bifidobacterium species. The type strain Tam10BT (=LMG 30126T=CCUG 70655T) represents a novel species, for which the name Bifidobacteriumvansinderenii sp. nov is proposed.

Temporal and demographic blood parasite dynamics in two free-ranging neotropical primates.

Parasite-host relationships are influenced by several factors intrinsic to hosts, such as social standing, group membership, sex, and age. However, in wild populations, temporal variation in parasite distributions and concomitant infections can alter these patterns. We used microscropy and molecular methods to screen for naturally occurring haemoparasitic infections in two Neotropical primate host populations, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, in the lowland tropical rainforests of southeastern Peru. Repeat sampling was conducted from known individuals over a three-year period to test for parasite-host and parasite-parasite associations. Three parasites were detected in L. weddelli including Trypanosoma minasense, Mansonella mariae, and Dipetalonema spp., while S. imperator only hosted the latter two. Temporal variation in prevalence was observed in T. minasense and Dipetalonema spp., confirming the necessity of a multi-year study to evaluate parasite-host relationships in this system. Although callitrichids display a distinct reproductive dominance hierarchy, characterized by single breeding females that typically mate polyandrously and can suppress the reproduction of subdominant females, logistic models did not identify sex or breeding status as determining factors in the presence of these parasites. However, age class had a positive effect on infection with M. mariae and T. minasense, and adults demonstrated higher parasite species richness than juveniles or sub-adults across both species. Body weight had a positive effect on the presence of Dipetalonema spp. The inclusion of co-infection variables in statistical models of parasite presence/absence data improved model fit for two of three parasites. This study verifies the importance and need for broad spectrum and long-term screening of parasite assemblages of natural host populations.

Biased hand use in captive emperor tamarins (Saguinus imperator).

Comparing forelimb use across primates can improve the understanding of the mechanisms and functions of brain asymmetry. We broadened the comparative framework by investigating hand use biases across spontaneous behaviors in 11 captive emperor tamarins of 2 family groups. We found a right preference across 58% of pooled unimanual bouts and 60% of all tasks. The maximum biases for a single task were 88% right-hand use and 78% left-hand use. On an individual basis, for most tasks, 6 tamarins preferred their right hand, 2 tamarins the left, and 2 animals were ambidextrous. Only a single tamarin did not switch between left and right hand bias according to task, but displayed a consistent right-hand bias. Our accompanying review of the 2 dozen previous callitrichid hand use studies confirms this picture. Across the board, these report hand preferences for single tasks. Task specialization is found in less than half of the studies, hand specialization in less than a third, whereas population level handedness is almost never reported. Importantly, right-hand use is preponderant, but very rarely consistent across tasks or subjects. This might be attributable to the fact that often-employed simple (food-reaching) tasks may not be coupled to a specialized hemisphere and therefore not constrain forelimb use. A better understanding of what causes directional forelimb use in callitrichids and other animals is currently hampered by a lack of standardized methods including measurement criteria, task difficulty, and social setting as well as a dearth of taxonomic diversity and field studies.

Naturally acquired visceral leishmaniasis in non-human primates in Brazil

Visceral leishmaniasis (VL) is a chronic and often fatal protozoal disease that is endemic in Belo Horizonte (State of Minas Gerais, Brazil). Leishmania sp. is an intracellular obligatory parasite of macrophages that can naturally infect several mammalian species. Non-human primates (NHP) have been used as experimental models for infection with Leishmania of the donovani complex. The present report describes a case of visceral leishmaniasis in a black-fronted titi. Among 41 primates kept in captivity in a zoo in Belo Horizonte (State of Minas Gerais, Brazil), one animal, a black-fronted titi ( Callicebus nigrifrons), was positive for Leishmania chagasi infection by PCR and immunohistochemistry, and developed a fatal disease with clinical signs and lesions compatible with VL. Other 17 NHP, including six black-fronted titis ( C. nigrifrons), one howler monkey ( Alouatta guariba), three golden-bellied capuchins ( Cebus xanthosternos), one golden-headed lion tamarin ( Leontopithecus crysomelas), one black-headed owl monkey ( Aotus nigriceps), two Rio Tapajós sakis ( Pithecia irrorata) and three emperor tamarins ( Saguinus imperator) had blood samples that tested positive for amplification of Leishmania kDNA by PCR, although these NPH had no clinical signs of the disease.

Disseminated Encephalitozoonosis in Captive, Juvenile, Cotton-top (Saguinus oedipus) and Neonatal Emperor (Saguinus imperator) Tamarins in North America

Disseminated encephalitozoonosis was diagnosed in 2 sibling, juvenile, cotton-top tamarins (Saguinus oedipus) and 3 sibling, neonatal, emperor tamarins (S. imperator) by use of histologic examination, histochemical analysis, electron microscopy, and polymerase chain reaction (PCR) analysis with nucleotide sequencing. All tamarins were captive born at zoos in North America and died with no premonitory signs of disease. The main pathologic findings were myocarditis (4/5), hepatitis (3/5), interstitial pneumonia (3/5), skeletal myositis (3/5), meningoencephalitis (2/5), adrenalitis (2/5), tubulointerstitial nephritis (1/5), myelitis (1/5), sympathetic ganglioneuritis (1/5), and retinitis (1/5). Central nervous system lesions were the most prominent findings in cotton-top tamarins. The inflammation was predominantly lymphocytic and suppurative in cotton-top tamarins, whereas emperor tamarins had granulomatous or lymphoplasmacytic lesions. Intralesional periodic acid-Schiff-, gram-, or acid-fast (or all 3)-positive, oval-to-elliptical shaped organisms were found in 1 cotton-top and the 3 emperor tamarins. By electron microscopy, these organisms were consistent with microsporidia of the genus Encephalitozoon. E. cuniculi genotype III was detected by PCR analysis and sequencing in paraffin-embedded brain, lung, and bone marrow specimens from the cotton-top tamarins. Although PCR results were negative for one of the emperor tamarins, their dam was seropositive for E. cuniculi by ELISA and Western blot immunodetection. These findings and recent reports of encephalitozoonosis in tamarins in Europe suggest that E. cuniculi infection may be an emerging disease in callitrichids, causing high neonatal and juvenile mortality in some colonies. The death of 2 less than 1-day-old emperor tamarins from a seropositive dam supports the likelihood of vertical transmission in some of the cases reported here.

Distance influences the foraging decisions of emperor and saddleback tamarins

AbstractStudies on great apes, Old World monkeys, and New World monkeys suggest that anthropoid primates may retain a detailed spatial representation of the distribution of important food resources in their home range. This is evidenced by selecting the shortest travel routes between sets of feeding sites. In this research, I tested whether distance influences between‐patch foraging decisions of free‐ranging social groups of black‐chinned emperor tamarins Saguinus imperator imperator and Weddell's saddleback tamarins Saguinus fuscicollis weddelli living in a 100‐ha forest reserve (Zoobotanical Park of the Universidade Federal do Acre) located in Rio Branco, State of Acre, Brazil. Four artificial feeding sites (feeding stations) were established within the home ranges of one group of each species. They were distributed in a diamond configuration and located from 58 to 256 m from each other. Each feeding station was composed of eight feeding platforms (two of which baited with one banana). Data collection was conducted from 3 October to 28 November 1997 (54 days). To determine whether distance among feeding sites influences tamarin daily between‐patch foraging decisions, it was recorded whether a group visited the nearest, intermediate or farthest station after departing from a particular one. The emperor tamarin group visited the feeding stations 207 times (average=3.8 visits day−1) and the saddleback tamarin group visited the feeding stations 265 times (average=4.9 visits day−1). After arriving at a feeding station, both species tended to choose the nearest station to visit and to avoid the farthest one at a frequency greater than chance, supporting the contention that these tamarins know the distribution and spatial relationships of their main food resources.

Use of Social and Ecological Information in Tamarin Foraging Decisions

A major consequence of group living is that foragers may rely on social information in addition to ecological information to locate feeding sites. Although conspecifics can provide cues as to the spatial location of food patches, individual foraging decisions also must include some assessment of the likelihood of obtaining access to a resource other group members seek. This likelihood differs in the 2 models generally proposed to explain intragroup social foraging: the information-sharing model and the producer-scrounger model. We conducted an experimental field study on wild groups of emperor (Saguinus imperator) and saddleback (S. fuscicollis) tamarins to determine the foraging strategies adopted by individual group members and their relationship to social rank, food intake, and the ability to use ecological and social information in making intra-patch foraging decisions. Individual tamarins applied different behavioral strategies compatible with a finder-joiner paradigm to solve foraging problems. About half of the individuals in each study group initiated 74%–90% of all food searches and acted as finders. Most alpha individuals adopted a joiner strategy by monitoring the activities of others' to obtain a reward. The individual arriving first at a reward platform enjoyed a finder's advantage. Despite differences in search effort, both finders and joiners presented similar abilities in learning to associate ecological cues with the presence of food rewards at our experimental feeding stations. We conclude that within a group foraging context, tamarins integrate social and ecological information in decision-making.

The win-stay rule in foraging decisions by free-ranging titi monkeys (Callicebus cupreus cupreus) and tamarins (Saguinus imperator imperator and Saguinus fuscicollis weddelli).

Rainforest primates need to apply distinct foraging rules for efficiently using the spatial knowledge of the distribution of resources showing different temporal patterns of renewal. A win-stay rule is very important for exploiting abundant, long-lasting resources. Here, the author tests the use of this rule in wild groups of emperor tamarins (Saguinus imperator imperator), saddle-back tamarins (Saguinus fuscicollis weddelli), and titi monkeys (Callicebus cupreus cupreus) during a series of foraging tasks. Four feeding stations composed of 8 visually similar feeding platforms (2 containing a food reward and 6 containing a sham reward) were constructed. The location of food rewards was reliable during some experiments and unreliable during others. All 3 species consistently adopted a win-stay rule for returning to reward platforms when their location was predictable over time but stopped using it when their spatial distribution changed randomly across experimental trials.