Opportunistic Pneumocystis carinii infection in red-bellied tamarins (Saguinus labiatus).

P. carinii infection in red-bellied tamarins (Saguinus labiatus), born and maintained in a laboratory breeding colony, was examined by histopathologic examination postmortem. P. carinii cysts were detected in 6 of 10 red-bellied tamarins examined, by using Grocott's, toluidine blue O and immunostaining with avidin-biotin complex using antisera for rat-, simian-, and human-P. carinii. The results obtained from the present studies imply that P. carinii may be an important pathogen in this species.     

Karyotype of Saguinus labiatus labiatus (red-bellied marmosets)

The karyotype of Saguinus labiatus labiatus was determined by the Giemsa-banding technique on leukocytes cultured from 10 marmosets. The diploid chromosome number (2n = 46) was the same and the chromosome complement similar to other marmosets of genus Saguinus. Small karyotypic differences were found between S. l. labiatus and white-lipped marmosets (Saguinus fuscicollis) in the size of the X chromosome and in the banding pattern of one pair of metacentric chromosomes. A karyotypic variant was detected in 1 S. l. labiatus, characterized by a diploid chromosome number of 45 with balanced autosomal translocation involving two pairs of acrocentric chromosomes (T 16/19).     

Vigilance,vocalizations, and cryptic behavior at retirement in captive groups of red-bellied tamarins (Saguinus labiatus)

Frequent references are made to presumed antipredator adaptations exhibited by callitrichids, but there are very few systematic investigations of these behaviors. One set of untested presumptions stems from observations that callitrichids become especially vigilant and cryptic prior to retirement each evening. This hypothesis was tested in the current study by quantifying the rates of vocalizations and extragroup behavior at various times of the day. Using two groups of captive red-bellied tamarins, it was demonstrated that these primates do become relatively more quiet and more attentive to the nonsocial environment prior to retirement each evening, culminating in virtual silence once the nest box has been entered. While the adaptive significance of these phenomena has not yet been tested, it is likely that the behaviors reduce vulnerability to predation.     

Haematological, coagulation and blood chemistry data in red-bellied tamarins Saguinus labiatus

Haematology, coagulation and clinical chemistry data are reported for a group of male and female red-bellied tamarins (Saguinus labiatus). The tamarins were juvenile and young adults and were bred in captivity. High mean values for activities of alkaline phosphatase, alanine amino-transferase, aspartate aminotransferase and creatine kinase were noted. The findings are compared with data obtained from other members of the family Callitrichidae.     

A case study employing operant conditioning to reduce stress of capture for red-bellied tamarins (Saguinus labiatus)

Traditional techniques used to capture New World monkeys, such as net capture, can induce high levels of acute stress detrimental to welfare. Alternatively, training nonhuman animals via operant conditioning to voluntarily participate in husbandry and/or veterinary practices is accepted as a humane process that can reduce stress and improve welfare. This study details the use of operant conditioning using positive reinforcement training (PRT) and target training to train a family of 5 captive red-bellied tamarins (Saguinus labiatus) in a wildlife park to voluntarily enter a transportation box and remain calm for 1 min after 54 training sessions. Observations of 2 unrelated net-capture processes provided measures of locomotion and vocalizations as indicators of stress behavior that were compared with those of the trained tamarins. Net-captured monkeys exhibited rapid erratic locomotion and emitted long, high-frequency vocalizations during capture whereas the trained tamarins exhibited minimal locomotion and emitted only 4 brief vocalizations (root mean square 35 dB) during capture. This indicates that the use of PRT considerably reduced potential for stress and improved welfare during the capture and containment of the tamarins.     

An outbreak of Yersinia pseudotuberculosis infection in a small indoor breeding colony of red-bellied (Saguinus labiatus) tamarins

A spontaneous outbreak of yersiniosis caused by Yersinia pseudotuberculosis serotype IIB occurred in a small indoor breeding colony of red-bellied tamarins (Saguinus labiatus) during the winter of 1981. Of 35 monkeys at risk 6 died of an acute or subacute infection over a period of 23 days. Clinical signs were anorexia, weakness, listlessness and depression. The disease was characterized by focal necrosis of the liver, spleen, mesenteric lymph nodes, ulcerative enteritis, and the presence of colonies of Gram-negative bacilli in the lesions. Y. pseudotuberculosis was isolated from the liver, spleen, mesenteric lymph nodes and kidney but not from the blood, lung or intestine. Contaminated food was believed to be the source of infection.     

Color vision pigment frequencies in wild tamarins (Saguinus spp.)

The adaptive importance of polymorphic color vision found in many New World and some prosimian primates has been discussed for many years. Polymorphism is probably maintained in part through a heterozygote advantage for trichromatic females, as such individuals are observed to have greater foraging success when selecting ripe fruits against a background of forest leaves. However, recent work also suggests there are some situations in which dichromatic individuals may have an advantage, and that variation in color vision among individuals possessing different alleles may also be significant. Alleles that confer a selective advantage to individuals are expected to occur at a higher frequency in populations than those that do not. Therefore, analyzing the frequencies of color vision alleles in wild populations can add to our understanding of the selective advantages of some color vision phenotypes over others. With this aim, we used molecular techniques to determine the frequencies of color vision alleles in 12 wild tamarin groups representing three species of the genus Saguinus. Our results show that allele frequencies are not equal, possibly reflecting different selective regimes operating on different color vision phenotypes.     

Trans-specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates

Many New World (NW) primates possess a remarkable polymorphism in an X-linked locus, which encodes for the visual pigments (opsins) used for colour vision. Females that are heterozygous for opsin alleles of different spectral sensitivity at this locus have trichromatic colour vision, whereas homozygous females and males are dichromatic, with poor colour discrimination in the red-green range. Here we describe an extensive survey of allelic variation in both exons and introns at this locus within and among species of the Callitrichines (marmosets and tamarins). All five genera of Callitrichines have the X-linked polymorphism, and only the three functional allelic classes described previously (with maximum wavelength sensitivities at about 543 nm, 556 nm and 563 nm) were found among the 16 species and 233 or more X-chromosomes sampled. In spite of the homogenizing effects of gene conversion, phylogenetic analyses provide direct evidence for trans-specific evolution of alleles over time periods of at least 5-6 million years, and up to 14 million years (estimated from independent phylogenies). These conclusions are supported by the distribution of insertions and deletions in introns. The maintenance of polymorphism over these time periods requires an adaptive explanation, which must involve a heterozygote advantage for trichromats. The lack of detection of alleles that are recombinant for spectral sensitivity suggests that such alleles are suboptimal. The two main hypotheses for the selective advantage of trichromacy in primates are frugivory for ripe fruits and folivory for young leaves. The latter can be discounted in Callitrichines, as they are not folivorous.     

Visual monitoring of threatening objects by captive tamarins (Saguinus labiatus)

Captive social groups of red-bellied tamarins (Saguinus labiatus) were observed in the presence of threatening, inanimate objects. The tamarins monitored the stimuli over the course of the 20-minute trials by conducting brief, periodic visual checks of the objects. The average number of checks per subject per trial was stable both across trials and between groups, and individual differences in rates varied relatively little around the group means. These data generate the hypothesis that there is a species-typical execution of vigilance in the presence of mildly threatening objects. This execution takes the form of brief visual inspections of the stimulus, usually by one tamarin at a time, at a fairly consistent rate. The discussion of the data takes place in the context of the behavioral ecology of callitrichid species.     

Red-bellied tamarins (Saguinus labiatus): Hematologic reference values and hemopathologic responses

Hematologic reference values have been established for captive adult red-bellied tamarins (Saguinus labiatus) by carrying out full blood counts and fibrinogen estimations on 25 clinically normal animals. The only significant sex difference detected was in the reticulocyte count which was higher in females than in males. The reference values were used to identify abnormal changes in the blood of nine clinical cases. Hypochromic anemia, neutrophilia, and raised fibrinogen levels were found in animals with self-inflicted injuries, dermatitis, and ileocecal intussusception. Target cells and jaundiced plasma were noted in a case of yersiniosis. Two animals in which generalized muscle wasting was the main abnormal clinical sign were severely anemic, and in one of these cases a significant number of Heinz bodies was present. The findings in these two animals were compared with those in common marmosets (Callithrix jacchus) with possible wasting marmoset syndrome.     

Hepatic multiple myelolipoma with severe coelomic edema in a red-bellied tamarin (Saguinus labiatus)

This report describes hepatic multiple myelolipoma with severe coelomic edema in a 14-year-old, male red-bellied tamarin (Saguinus labiatus). Multiple small and large nodules were formed in all lobes of the liver. Histopathologically, the nodules comprised mature and normal adipocytes and hematopoietic elements at various ratios that were composed of granulocytic, erythrocytic, and megakaryocytic series in various phases of maturation. All nodules were encapsulated and demarcated hepatocytes around masses. Myelolipoma in the liver is rare, and there are no reports of any cases to date. To our knowledge, this is the first report of hepatic multiple myelolipoma in a red-bellied tamarin.     

Comparative studies on vertical separation,foraging behavior and traveling mode of saddle-backed tamarins (Saguinus fuscicollis) and red-chested moustached tamarins (Saguinus labiatus) in Northern Bolivia

The author made comparative studies on the ecology of saddle-backed tamarins (Saguinus fuscicollis) and red-chested moustached tamarins (S. labiatus) on the upper Amazon in northern Bolivia. The unit group of both species of monkeys was a family group composed of two to seven individuals, but they often formed polyspecific associations comprising one such family group each. However, both species preferred different layers of forest for foraging insects and traveling.S. fuscicollis mainly utilized the lower layer of the forest and foraged large-sized insects lurking in tree hollows, whereasS. labiatus mainly utilized the middle layer of the forest and foraged small-sized animals on branches. These differences were more clearly noticeable in secondary forest than in primary forest.     

Reproductive events of wild cotton-top tamarins (Saguinus oedipus) in Colombia

Reproductive patterns of wild cotton-top tamarin (Saguinus oedipus) females located in La Reserva Forestal Protectora Serranía de Coraza-Montes de María in Colosó, Colombia, were examined using long-term behavioral observations and fecal steroid analysis. Using an enzyme immunoassay, we analyzed fecal samples for E₁C and PdG. Comparisons of reproductive cycles of a reproductively active female and her daughters were made. An inhibition of ovarian cycles has been observed in daughters living in their families. However, daughters also exhibited normal ovarian cycling that subsequently resulted in pregnancy. Factors influencing the fertility are discussed as they relate to the reproductive strategies of wild cotton-top tamarin females. Am. J. Primatol. 43:329–337, 1997. © 1997 Wiley-Liss, Inc.     

Social interaction with non-averse group-mates modifies a learned food aversion in single- and mixed-species groups of tamarins (Saguinus fuscicollis and S. labiatus)

For social species, being a member of a cohesive group and performing activities as a coordinated unit appear to provide a mechanism for the efficient transmission of information about food. Social learning about food palatability was investigated in two captive primates, Saguinus fuscicollis and S. labiatus, which form stable and cohesive mixed-species groups in the wild. We explored whether an induced food aversion toward a preferred food is modified during and after social interaction with non-averse conspecifics or congeners. Sets of intra- and interspecific pairs were presented with two foods, one of which was considered distasteful by one of the pairs (the other was palatable), and their behavior was compared pre-interaction, during interaction, and post-interaction. For the aversely-conditioned individuals of both species, the change in social context corresponded to a change in their preference for the food that they considered unpalatable, regardless of whether they had interacted with a conspecific or congeneric pair, and the change in food preference was maintained post-interaction. In a control condition, in which averse individuals did not have the opportunity to interact with non-averse animals, S. fuscicollis sampled the preferred food, but not as quickly as when given the opportunity to interact. We conclude that the social learning demonstrated here may allow individual tamarins to track environmental change, such as fruit ripening, more efficiently than asocial learning alone, because social learners can more quickly and safely focus on appropriate behavior by sharing up-to-date foraging information. Furthermore, since the behavior of congeners, as well as conspecifics, acts to influence food choice in a more adaptive direction, social learning about food palatability may be an advantage of mixed-species group formation to tamarins of both species.     

Litter size and infant survivorship in wild groups of cotton‐top tamarins (Saguinus oedipus) in Colombia

Cotton‐top tamains (Saguinus oedipus) are a critically endangered primate found only in Colombia. Efforts to conserve this species are centered on developing effective management plans that integrate biological information regarding population dynamics and factors that influence their survival. This study documented infants born to wild cotton‐top tamarin females from 1994–2008 at two distinct field sites in northern Colombia. Our studies have shown that wild cotton‐top tamarins typically give birth to one litter each year and infant survival to 6 months of age was greater in the wild than has been reported in captive colonies. However, similar to reports from captive colonies, litter size of wild cotton‐top tamarins ranges from 1–3 infants, with twin litters most common. Here we report the first occurrence of triplet litters in nearly 20 years of observing wild cotton‐top tamarin groups. Over the first 3 months of life, wild‐born infants exhibited highest mortality during the first week of life, similar to reports from captive colonies. Infant survival in the wild also increases with successive litters as it does in captivity. However, inter‐birth interval, group size, and the number of adult males in the group did not appear to influence infant survival in the wild. The value of such long‐term data from field studies aids in the information that can be used to model future population trends and develop effective conservation plans for this critically endangered primate. Am. J. Primatol. 71:707–711, 2009. © 2009 Wiley‐Liss, Inc.     

The Perception of Sex-specificity in Long Calls of the Tamarin (Saguinus labiatus labiatus)

Long calls given by red-chested moustached tamarins (Saguinus l. labiatus), typically 1–2 s in duration and made up of individual syllables, reveal distinctive sex-specificity as well as population and individual differences in their acoustic structure. Distributions of male calls and female vocalizations are discrete with regard to two acoustic parameters, i.e. number of syllables and mean inter-syllable intervals. Mean number of syllables produced in a given time is much greater in male than in female calls. I played back synthetic versions of the long calls varying in mean inter-syllable intervals to captive tamarins and found that the sex differences were encoded in a relatively simple acoustic form. The tamarin is able to identify the sex of unfamiliar calling conspecifics by voice alone.     

Behavioural observations on captive pairs of wild caught tamarins (Saguinus mystax)

Quantitative data are given on 12 categories of behaviour, including scent marking, allogrooming, huddling, and proximity for individual tamarins within 14 male, female pairs and the mated pair of one family group of four animlals. Time sample data were recorded at 30 sec intervals to a total of 260 hr. In addition, some data were collected from within time sample intervals. Individual and intergroup variation in behaviour was a main finding of the study. It was found, however, that females scent marked significantly more than males, at least on the basis of their total marking frequencies, that females tended to groom males more than vice versa, and that although the general proportions of activities were similar in two conditions of housing, their spatial distribution was different under the two conditions. There was very little overt aggression among the pairs.     

Forest use and activity patterns of Callimico goeldii in comparison to two sympatric tamarins, Saguinus fuscicollis and Saguinus labiatus

Callimico goeldii, Saguinus fuscicollis, and S. labiatus are sympatric in northern Bolivia and differ from each other in patterns of spatial and structural use of their environment. C. goeldii has a home range five times larger than that of mixed-species troops of S. fuscicollis and S. labiatus. The larger overlapping home range of C. goeldii allows it to move among Saguinus troops, giving it access to a wide range of different microhabitats. All three species use the most common microhabitat in the area, primary forest with dense understory, more than any other microhabitat type. C. goeldii habitat use varies by season, with bamboo and Heliconia microhabitats used more during the dry season. Each species shows preferences for different height classes: C. goeldii is found almost exclusively in the understory, S. fuscicollis uses the understory and middle canopy, and S. labiatus is found mostly in the middle canopy. These height class preferences are reflected in each species' locomotor styles, with C. goeldii showing the highest rates of vertical clinging and leaping, and S. labiatus showing the highest rates of branch-to-branch leaping and quadrupedal movement. The results suggest that C. goeldii may be restricted to forests with dense understory and a mosaic of other microhabitats. Furthermore, C. goeldii does not appear to use its tegulae for large branch foraging, but rather for vertical clinging and leaping between small vertical supports.     

Genetic markers in the blood of three species of tamarins (Saguinus mystax, S. labiatus and S. oedipus)

Alkaline phosphatase (Alp), esterase-I (Es-I), esterase-II (Es-II), carbonic anhydrase (CA), cell esterase (cEs), esterase-D (Es-D), isocitrate dehydrogenase (ICD), malate dehydrogenase (MDH), 6-phosphogluconate dehydrogenase (PGD), tetrazolium oxidase (To), ceruloplasmin (Cp), Haptoglobin (Hp) and hemoglobin (Hb) in 58-75 samples of three species of tamarins (Saguinus mystax, S. labiatus and S. oedipus) were detected by means of horizontal starch gel electrophoresis. Two types (Es-I 1 and Es-I 2) for Es-I, four types (Es-II 1, Es-II 2, Es-II 3 and Es-II 2-3) for Es-II, three types (cEs 1, cEs 2 and cEs 1-2) for cEs, three types (PGD 1, PGD 2 and PGD 1-2) for PGD, two types (To 1 and To 2) for To, and three types (Hp 3, Hp 1-3 and Hp 2-3) for Hp were observed. However, Alp, CA, Es-D, ICD, MDH, Cp and Hb were monomorphic. In the S. mystax, no Es-II or PGD variants were observed. No Es-II variant was seen in the S. oedipus. Gene frequencies of cEs, PGD and Hb were biased in the three species. It is concluded that six polymorphic loci are useful as genetic markers for a species or individual.