Tamarin Species Research Articles

Discerning evolutionary processes in patterns of tamarin (genus Saguinus) craniofacial variation.

Quantitative genetic theory specifies evolutionary expectations for morphological diversification by genetic drift in a monophyletic clade. If genetic drift is responsible for the evolutionary morphological diversification of a clade, patterns of within- and between-taxon morphological variance/covariance should be proportional. We tested for proportionality of within- and between-species craniofacial morphological variation in 12 species of tamarins (genus Saguinus). We found that within- and between-taxon morphological variations across the entire genus were not proportional, and hence not likely to be due to genetic drift alone. The primary deviation from proportionality is that size and size-related shape in the cranium is more variable relative to other aspects of cranial morphology than expected under genetic drift, suggesting differential size selection between the two major clades, the small-bodied and large-bodied tamarins. Within each of these major clades, most of the interspecific variation is consistent with the pattern expected under genetic drift, although specific contrasts may indicate the involvement of differential selection. Morphological distances among taxa do not correspond very closely to the phylogeny derived from mtDNA. In particular, S. oedipus and S. geoffroyi are very distinct morphologically from the rest of the tamarins, although they are phylogenetically the sister clade to a clade containing S. midas and S. bicolor. Morphological similarity is not a good guide to phylogenetic affinity in the tamarins, especially with regard to deeper nodes in the phylogenetic tree.

Single-copy nuclear DNA sequences obtained from noninvasively collected primate feces.

Noninvasively collected primate feces have been shown to provide a useful source of mitochondrial DNA for sequencing and nuclear microsatellite DNA for size analysis. In this study, single-copy nuclear DNA sequences were obtained from noninvasively collected fecal samples of two species of wild tamarins, Saguinus fuscicollis and S. mystax, in the context of a project on the functional utility of color vision. Noninvasive genotyping of the X-linked opsin gene is important for future studies of selection and adaptation at this locus in a number of primate species. The wide range of techniques that can now be applied successfully to DNA extracted from feces introduces a broad spectrum of potential genetic studies that can be undertaken on primates, without the need for intrusive or invasive methods.

Interspecific communication in mixed-species groups of tamarins: evidence from playback experiments

Long-call vocalizations have been hypothesized to serve as communicative signals both within and between tamarin species. Prior evidence for the use of long calls as interspecific signals, however, is based solely on observations of apparent countercalling between species. I conducted playback experiments with groups of wild saddle-back tamarins, Saguinus fuscicollis, and emperor tamarins, S. imperator, to test the hypothesis that long calls function as interspecific signals between tamarin species forming polyspecific associations. Results show that in the absence of any other external cues, lone groups of saddle-back tamarins and emperor tamarins respond to the playback of long calls from both conspecific group members and heterospecific tamarins with which they associate. Playback of long calls from heterospecific tamarins elicited long calls and approaches towards the speaker. These findings are consistent with the hypothesis that long calls serve as interspecific signals between associating tamarin species.

Animal Models of Hepatitis A and E

Several useful animal models for both hepatitis A and E have been identified, characterized, and refined. At present, all of the best models utilize nonhuman primates: chimpanzees, tamarin species, and owl monkeys for hepatitis A; and macaque species, chimpanzees, and owl monkeys for hepatitis E. Pigs may prove useful for some studies of hepatitis E, and it is hoped that serological evidence of widespread infection of rats with an HEV-like agent may lead to the development of an animal model based on laboratory rats. As has been the case for each of the hepatitis viruses as they have been discovered, the development of useful and reproducible animal model systems has been critical for moving the field forward as expeditiously as possible.

Vertebrate predation by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis.

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

Phenotypic covariance structure in tamarins (genus Saguinus): a comparison of variation patterns using matrix correlation and common principal component analysis.

Constancy of variation/covariation structure among populations is frequently assumed in order to measure the differential selective forces which have caused population differentiation through evolutionary time. Following Steppan ([1997] Evolution 51:571-594), this assumption is examined among closely related tamarin species (genus Saguinus), using two distinct approaches applied to the task of evaluating similarity in patterns of morphological variation: common principal component analysis and matrix correlations. While the results of these analyses may appear contradictory, closer examination reveals them as complementary, highlighting the wisdom of combined methodologies. Overall, the results reveal a close relationship among the morphologically based variance structures of the tamarin species a relationship whose pattern is consistent with the pattern of phylogenetic relatedness as found via a molecular genetic study. More specifically, both methodological approaches provide some support for divergence of S. geoffroyi and S. oedipus (with regards to their patterns of morphological variation) from other tamarin species. This suggests that variance/covariance structure may have diverged through evolutionary time in the tamarin lineage, placing assumptions of constancy in doubt.

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 ofLeontopithecusdiffer in shape from all other callitrichine taxa allowing it to perform highly manipulative prey foraging behaviors? 2. Are the hands ofSaguinus fuscicollisadapted to manipulative foraging, and are they functionally similar toLeontopithecus’ hands? 3. Is hand morphology inS. fuscicollismore similar to the hand morphology of sympatric tamarin species with whom it does not form mixed species troops (S. nigricollisandS. tripartitus) than to those sympatric tamarin species with whom it does form mixed troops (S. mystax, S. labiatus, andS. imperator)? Measurements of hand length (HL), width (HW), and thickness (HT) were taken from 1350 museum specimens of callitrichines (Callithrix, Cebuella, Leontopithecus, Saguinus, andCallimico), squirrel monkeys (Saimiri), and owl monkeys (Aotus). The analysis indicates that hand shape covaries with foraging strategy. Specifically, the hands ofLeontopithecusare 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 ofS. fuscicollis, S. tripartitusandS. 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.

Intra-and Inter-Specific Social Learning of a Novel Food Task in Two Species of Tamarin

Intra- and inter-specific social learning was investigated in two species ofNew World monkey, the saddle-backed tamarin {Saguinus fuscicoUis) and the redbelliedtamarin {S. labiatus), which form stable and permanent mixed-species troops inthe wild. We explored whether improved food acquisition, through social learning, is apotential advantage of mixed-species troop formation by allowing a pair of naiveobservers to watch a pair of trained demonstrators complete a novel foraging task. Theaims of the study were (a) to determine if individuals succeeded at the task morequickly after having observed demonstrators, (b) to investigate whether speed ofacquisition differed after observation of conspecific demonstrators as opposed tocongeneric demonstrators, and (c) to compare performance between species. Thenumber of trials taken by observers to succeed on the task was compared with that takenby naive demonstrators to succeed on the task initially. Individuals succeeded on thetask more quickly if they had had the opportunity to watch demonstrators perform thetask, regardless of whether the demonstrator was a conspecific or congeneric. There wasno difference in performance between species. It is concluded that, for both species, thelearning of a new foraging technique is facilitated by the presence of both conspecificsand congenerics and that the likely mechanism for this facilitation is a combination ofstimulus enhancement and response facilitation. Social learning of this kind is discussedwith respect its adaptive value in wild mixed-species tamarin troops.

Foraging behavior and microhabitats used by black lion tamarins, Leontopithecus chrysopygus (Mikan) (Primates, Callitrichidae)

Foraging in the Black Lion Tamarin (L. chrysopygus Mikan, 1823) was observed in the Caetetus Ecological Station, São Paulo, southeastern Brazil, during 83 days between November 1988 to October 1990. These tamarins use manipulative, specific-site foraging behavior. When searching for animal prey items, they examine a variety of microhabitats (dry palm leaves, twigs, under loose bark, in tree cavities). These microhabitats were spatially dispersed among different forest macrohabitats such as swamp forests and dry forested areas. These data indicated that the prey foraging behavior of L. chrysopygus was quite variable, and they used a wide variety of microhabitats, different of the other lion tamarin species.

Foraging strategies among male and female marmosets and tamarins (Callitrichidae): new perspectives in an underexplored area.

Few studies have involved an examination of behavioural gender differences among callitrichid primates. The present paper presents consistent evidence from experimental projects, together with less formal observations, that adult females of both breeding and non-breeding status in species of marmosets (Callithrix) and tamarins (Saguinus) demonstrate priority of access to preferred and/or restricted sources of food. Differences in behavioural strategies between males and females in this regard are not only functionally plausible, but are consistent with differences in natural behaviour both in feeding ecology and social organization in species of the different genera. Behavioural propensities that relate to the behavioural strategies of males and females are also considered, together with a number of suggestions for future research that arise directly from the observations reported.

Geographic Distribution of the Golden-Headed Lion Tamarin, Leontopithecus chrysomelas: Implications for Its Management and Conservation

The geographic distribution and conservation status of the golden-headed lion tamarin, Leontopithecus chrysomelas, were studied during a survey carried out through an area of about 37,000 km2 in southern Bahia from March 1991 to March 1993. The survey involved interviews of local people and direct censusing in 33 forest patches using playback recordings of a male and female lion tamarin long-call. Populations were found to occur in 94 localities. An Appendix provides a full gazetteer of these localities and a further 28 localities recorded in previous studies. The distributional limits were found to agree closely with the ranges described by previous authors, except for its absence in the extreme north-east of its range, from the south of the Rio de Contas to the Rio Almada, where it might have become extinct. The total geographic range was estimated to cover approximately 19,462 km2, including two distinct regions in terms of land use and forest cover. The forests in both regions are severely reduced and fragmented. Unlike the other three species of lion tamarins, L. chrysomelas evidently still occurs throughout a large part of its historic range, but the fragmentation and rapid rate of forest destruction clearly indicate that the species is endangered. The Una Biological Reserve is the only protected area within its range, and is believed to be too small (7,059 ha) to maintain a genetically viable population. The conservation status of L. chrysomelas is discussed, particularly in terms of the socioeconomy of the region where it occurs, as well as the need for further ecological research.

The Relationship between Body Size and Mixed-Species Troops of Tamarins (Saguinusspp.)

While Saguinus fuscicollis forms mixed-species troops with sympatric tamarin species in parts of its geographic range, in other parts it does not. The question is addressed whether body size divergence is a critical factor for this difference. Analysis of body size (head-body length) data shows that body size divergence ranges between 8 and 17% for associated species and between 1 and 4% for non-associated species. In associated species, the degree of body size divergence seems to correlate with the stability of mixed-species troops (i.e., time spent in interspecific association). It is concluded that body size plays an important role for niche differentiation, sympatric coexistence and the formation of mixed-species troops in tamarins.

Vigilance in single- and mixed-species groups of tamarins (Saguinus labiatus and Saguinus fuscicollis)

By forming larger sizes of groups, individuals benefit from a decrease in vigilance, but the collective vigilance of the group as a whole is not compromised. We examined whether this group size effect is apparent in mixed-species groups of red-bellied tamarins (S. labiatus) and saddleback tamarins (S. fuscicollis) which form stable and permanent associations in the wild. We studied general vigilance and responses to hidden threatening stimuli in five captive groups of each species, while they were housed in single- and mixed-species groups. For vigilance, the individual rate was lower in the larger mixed-species groups than in the smaller single-species groups. In addition, the amount of time when at least one individual was vigilant was higher in mixed-species groups. This suggests that the tamarins alter their vigilance behavior in the presence of the other species. In response to hidden threats, both species performed brief vigilance checks and frequencies of checking did not differ in single- and mixed-species groups. However, both species had a significant reduction in the mean duration per check, and there was a reduced total amount of time spent vigilance checking in the mixed-species groups compared to the single-species groups, demonstrating the group size effect. Overall the mixed-species groups had a higher number and mean duration of checking than the smaller single-species groups. Given that the two species share a common set of predators, and respond to each other's alarm calls, these findings provide strong evidence that individuals of both tamarin species may be able to benefit from forming mixed-species groups via improved vigilance and monitoring of threats.

Development of an enzyme‐immunoassay (EIA) for the measurement of follicle‐stimulating‐hormone (FSH) in callitrichid primates using a monoclonal antibody against the human‐FSH‐β‐subunit

Despite the importance of Callitrichid primates in both biomedical and conservation research, practical and reliable immunoassays for the measurement of follicle-stimulating hormone (FSH) have not yet been described. A panel of monoclonal antibodies against specific peptide fragments within either the alpha or beta subunit of human FSH was evaluated for their ability to recognize FSH from Callitrichid and other New World primates. One of these, monoclonal antibody 46.3h6.b7 raised against human FSH, was selected due to its ability to recognize marmoset monkey FSH and its low crossreactivity with other gonadotrophins. The antibody formed the basis of an enzymeimmunoassay using a highly purified human urinary FSH (Metrodin®, Serono) preparation coupled to biotin as label and unmodified as standard. After 24 h incubation, antibody bound label was visualized by addition of streptavidin-peroxidase followed by the appropriate substrate. Parallelism was obtained between the standard and dilutions of pituitary extracts, urine and plasma from the common marmoset (Callithrix jacchus) as well as from two tamarin species (Saguinus fuscicollis and S. oedipus) and one squirrel monkey (Saimiri sciureus). Profiles of plasma and urinary FSH during the follicular phase are shown for two individual marmosets. The ability to measure FSH in Callitrichidae provides new opportunities for studies of the reproductive biology of these New World primate species. Am. J. Primatol. 41:179–193, 1997. © 1997 Wiley-Liss, Inc.

Seed swallowing in Tamarins : Evidence of a curative function or enhanced foraging efficiency ?

Nonhuman primates represent a major component of the frugivore biomass in several rain-forest communities. Although there is considerable evidence that prosimians, monkeys, and apes serve as dispersal agents for many tropical trees, little attention has been paid to the more basic questions of why certain species of primates swallow and void seeds, and what, if any, are the advantages to an animal of having a large, hard, bolus pass through its digestive tract. We examine patterns of fruit-eating and seed-swallowing in two species of free-ranging tamarins: Saguinus mystax and Saguinus geoffroyi. Fruits commonly eaten by tamarins contain large seeds surrounded by a fibrous and adhesive pulp or arilate seed coat. They generally swallow seeds and pulp together. Intact seeds are voided over a 1- to 3-h period. Measurements of 132 seeds naturally voided by Panamanian tamarins average 11.2 mm in length and 0.3 g. The greatest number of large seeds contained in the digestive tract of a single animal at one time was 13. In the case of moustached tamarins, we collected 220 seeds. Average seed length is 11.9 mm and average seed weight is 0.3 g. At the time of capture, one animal had 26 seeds in its digestive tract. In both tamarin species, there is evidence of sex-based differences in feeding behavior. Adult female moustached and Panamanian tamarins swallowed and voided seeds of larger size than adult males did. Seed size is positively correlated with pulp weight (p <. 001), therefore females were selecting food items with higher nutritional rewards than adult males did. Given their small body size and relatively short digestive tract, why do tamarins swallow such large seeds? Although several explanations are possible, we propose that the large number and size of undigested seeds continuously passing through the tamarin gut serve a curative role in mechanically dislodging and expelling intestinal parasites—Ancanthocephala (spiny-headed worms)—from their digestive tracts.

Development of an enzyme-immunoassay (EIA) for the measurement of follicle-stimulating-hormone (FSH) in Callitrichid primates using a monoclonal antibody against the human-FSH-beta-subunit.

Despite the importance of Callitrichid primates in both biomedical and conservation research, practical and reliable immunoassays for the measurement of follicle-stimulating hormone (FSH) have not yet been described. A panel of monoclonal antibodies against specific peptide fragments within either the alpha or beta subunit of human FSH was evaluated for their ability to recognize FSH from Callitrichid and other New World primates. One of these, monoclonal antibody 46.3h6.b7 raised against human FSH, was selected due to its ability to recognize marmoset monkey FSH and its low crossreactivity with other gonadotrophins. The antibody formed the basis of an enzymeimmunoassay using a highly purified human urinary FSH (Metrodin, Serono) preparation coupled to biotin as label and unmodified as standard. After 24 h incubation, antibody bound label was visualized by addition of streptavidin-peroxidase followed by the appropriate substrate. Parallelism was obtained between the standard and dilutions of pituitary extracts, urine and plasma from the common marmoset (Callithrix jacchus) as well as from two tamarin species (Saguinus fuscicollis and S. oedipus) and one squirrel monkey (Saimiri sciureus). Profiles of plasma and urinary FSH during the follicular phase are shown for two individual marmosets. The ability to measure FSH in Callitrichidae provides new opportunities for studies of the reproductive biology of these New World primate species.

Craniometric sexual dimorphism inLeontopithecus Lesson, 1840 (Callitrichidae, Primates)

Lion tamarins are among the World's most critically endangered primates. Many studies have been produced under guidance of the International Management Committees for the preservation and management of these tamarins. Primates present morphological sexual differences in a wide range of characteristics, including cranial morphology. Studies of sexual dimorphism in the cranial morphology of theLeontopithecus are few in number and contradictory in their results. In order to check for the existence of sexual dimorphism in lion tamarins the present study analyzed 17 craniometric distances on 56 crania of three species of lion tamarins (Leontopithecus): 20L. rosalia (14 females and 6 males); 13L. chrysomelas (6 females and 7 males); and 23L. chrysopygus (8 females and 15 males). All crania are housed in the CPRJ-FEEMA collection (Primatological Center of Rio de Janeiro) and came from animals born in captivity.L. chrysopygus was more sexually dimorphic (10/17 measurements, 59%) thanL. chrysomelas (9/17 measurements, 53%) orL. rosalia (7/17 measurements, 41%). In all three species, male values are greater than the female ones, except for orbital breadth (m7) inL. rosalia. However, this distance is not sexually dimorphic in this species. This study reveals that some cranial distances, especially in the facial region, are sexually dimorphic in lion tamarins.

Exhibiting mixed-species groups of sympatric tamarins Saguinus spp at Belfast Zoo

In the wild sympatric tamarin species show a high degree of spatial co-ordination. Stable associations between Saddleback tamarins Saguinus fuscicollis and members of the Saguinus mystax group (Red-bellied tamarin Saguinus labiatus, Emperor tamarin Saguinus imperator and Moustached tamarin S. mystax) have been observed at all sites where the species co-occur and are related to the stratification of ecological niches within the forest. Since 1992 a study of mixed-species tamarin groups has been carried out at Belfast Zoo. Stable associations were established between groups of S. labiatus and S. fuscicollis, and few agonistic interactions were observed. Most aggression involved disputes over food and typically consisted of S. labiatus displacing S. fuscicollis, merely by approaching. Other interactions included some inter-specific grooming and huddling. This paper describes the introduction procedure and the social and reproductive behaviour of each species within the group, and suggests that mixed-species exhibits may be a beneficial way of exhibiting tamarins.

Predation on Orthoptera and other orders in insects by tamarin monkeys,Saguinus mystax mystaxandSaguinus 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.

Riverine barriers and gene flow in Amazonian saddle-back tamarins.

We describe patterns of genotypic and phenotypic variation in saddle-back tamarin (Saguinus fuscicollis) populations along the central and upper Rio Juruá, western Brazilian Amazonia. The genetic data are sequence haplotypes of the mitochondrial cytochrome b gene; phenotypic data are pelage colour variants that define sharply demarcated subspecies of this extremely variable tamarin species. We show that gene flow occurs between adjacent subspecies, but that this phenomenon is restricted to the headwater section of the river, which is consistent with expectations from the riverine barrier hypothesis. In this model, the major first-order tributaries of the Amazon form effective barriers to dispersal, with between-bank gene flow limited to the narrowed sections of headwater streams and parallel divergence increasing along both banks from the headwaters to the mouth of a given river. In meandering rivers such as the Rio Juruá, we suggest passive transfer through river channel dynamics as the main mechanism permitting genetic contact between populations on opposite banks of the river. Finally, we argue that in the case of plant and animal species that are largely restricted to unflooded (terra firme) forests, such as tamarins, seasonally flooded (várzea) forest can operate as a critical additional barrier to between-bank gene flow.