Gelatin as a vehicle for food and vitamin administration to marmosets

For a period of three years, gelatin was used as a vehicle for administration of food, vitamin complex and drugs to laboratory maintained Callithrix penicillata and Callithrix jacchus marmosets and a breeding colony of C. penicillata. In both circumstances, results were satisfactory. The animals survived for long periods of time, with adult, young and juvenile primates in the breeding colony showing good physical condition.     

Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour

It has been suggested that the major advantage of trichromatic over dichromatic colour vision in primates is enhanced detection of red/yellow food items such as fruit against the dappled foliage of the forest. This hypothesis was tested by comparing the foraging ability of dichromatic and trichromatic Geoffroy's marmosets (Callithrix geoffroyi) for orange- and green-coloured cereal balls (Kix) in a naturalized captive setting. Trichromatic marmosets found a significantly greater number of orange, but not green, Kix than dichromatic marmosets when the food items were scattered on the floor of the cage (at a potential detection distance of up to 6 m from the animals). Under these conditions, trichromats but not dichromats found significantly more orange than green Kix, an effect that was also evident when separately examining the data from the end of the trials, when the least conspicuous Kix were left. In contrast, no significant differences among trichromats and dichromats were seen when the Kix were placed in trays among green wood shavings (detection distance < 0.5 m). These results support an advantage for trichromats in detecting orange-coloured food items against foliage, and also suggest that this advantage may be less important at shorter distances. If such a foraging advantage for trichromats is present in the wild it might be sufficient to maintain the colour vision polymorphism seen in the majority of New World monkeys.     

Experimental infections of simians with human malaria: attempts to infect Callithrix penicillata with Plasmodium falciparum

After reviewing the use of non-human primates of the Old and New Worlds for human malaria research, we concluded that another experimental animal which is easily available to use and possible to rear indoors is needed. Thus, we studied the susceptibility of the marmoset Callithrix penicillata to Plasmodium falciparum erythrocytic infections. The marmosets received various P. falciparum human isolates, directly from a patient and from continuous cultures. The Palo Alto strain, which has been adapted to the night monkey Aotus trivirgatus and further maintained in the squirrel monkey Saimiri sciureus was also used. In a total of 20 marmosets we performed 31 inoculations, with 10(5) to 10(9) parasites, intraperitoneally, intracardiacly or intravenously. Blood samples from each animal were examined daily up to day 90 post-inoculation. None of the intact marmosets developed patent infections. Four out of 19 C. penicillata, previously splenectomized, showed circulating parasites for up to five days after intravenous inoculation with the Palo Alto strain, becoming negative thereafter. Neither the addition to the simian diet of p-aminobenzoic acid, essential for the parasite metabolism, nor drug-immunosuppression, improved the marmoset susceptibility to P. falciparum.     

Histochemical studies on the adrenal glands of the marmosets (Callithrix jacchus and Callithrix penicillata).

The histrochemistry of the adrenal glands was studied in four adult male marmosets (two Callithrix jacchus and two Callithrix penicillata). It was impossible to demonstrate any reactivity to UDPG-GT, ADH, alanyl aminopeptidase, leucine aminopeptidase, xilitol (NAD-dependent) dehydrogenase, beta-glucuronidase and aryl-sulfatase in these glands. Total phosphorylase was found in scattered cells of the glomerulosa and adjacent outer fasciculata of one C. penicillata. The dehydrogenases (LDH, G-6-PDH,6-PGDH, NADPH2-TR,ICDH,SDH,NADH2-TR, alpha-GPDH, beta-OHBDH) as well as the hydrolases (except alkaline phosphatase, ATPase, and acetylcholinesterase) showed a stonger reactivity in the cortical part. Some hydrolases (naphthol acetate esterase, acid phosphatase) and cytochrome oxidase were less reactive in the zona glomerulosa, where the dehydrogenases were more abundant. The outer fasciculata and the reticularis also showed a strong dehydrogenase reactivity.     

Differences in aerial and terrestrial visual scanning in captive black tufted-ear marmosets (Callithrix penicillata) exposed to a novel environment

Aerial and terrestrial visual scanning were investigated in captive black tufted-ear marmosets, Callithrix penicillata, exposed to a novel environment. Naive adult subjects (n=24) were individually exposed to a figure-eight maze during seven 30-min trials, 48 h apart. Habituation to the maze was observed, as indicated by the significant decrease in locomotion. The frequency of aerial scanning, however, remained elevated throughout the 7 trials, while its duration rapidly increased to high levels. Frequency and duration of terrestrial scanning persisted at constant low rates, differing significantly from aerial scanning. Males and females did not differ significantly. The different impact of aerial versus terrestrial predators could have a significant influence on vigilant behaviour in this species. Thus, visual scanning is an important and highly organized antipredation strategy in marmosets.     

Advantage of dichromats over trichromats in discrimination of color-camouflaged stimuli in nonhuman primates

Due to a middle- to long-wavelength-sensitive (M/LWS) cone opsin polymorphism, there is considerable phenotypic variation in the color vision of New World monkeys. Many females have trichromatic vision, whereas some females and all males have dichromatic vision. The selective pressures that maintain this polymorphism are unclear. In the present study we compared the performance of dichromats and trichromats in a discrimination task. We examined tri- and dichromatic individuals of two species: brown capuchin monkeys (Cebus apella) and long-tailed macaques (Macaca fascicularis). We also examined one protanomalous chimpanzee (Pan troglodytes). The subjects' task was to discriminate a circular pattern from other patterns in which textural elements differed in orientation and thickness from the background. After they were trained with stimuli of a single color, the subjects were presented with color-camouflaged stimuli with a green/red mosaic overlaid onto the pattern. The dichromatic monkeys and the protanomalous chimpanzee selected the correct stimulus under camouflaged conditions at rates significantly above chance levels, while the trichromats did not. These findings demonstrate that dichromatic nonhuman primates possess a superior visual ability to discriminate color-camouflaged stimuli, and that such an ability may confer selective advantages with respect to the detection of cryptic foods and/or predators.     

Histochemical studies on the submandibular ganglia of marmosets (Callithrix jacchus and Callithrix penecillata).

The histochemistry of the neural cells was studied in the submandibular ganglia of 5 Callithrix jacchus (3 males and 2 females) and 4 Callithrix penicillata (2 males and 2 females). These cells contain neutral mucopolysaccharides, nucleoproteins and lipidic materia, but are apparently devoid of glycogen. It is impossible to demonstrate in them any reactivity for UDPG-GT, phosphorylases, ATPase at pH 6.3, leucine aminopeptidase and alanyl aminopeptidas. The reaction for the other searched enzymes was as follows: weak (F-1,6-P Ald and cytochrome oxidase), weak to moderate (ADH, 6-P-GDH, ICDH, SDH, MDH, alpha-GPDH and beta-OHBDH), moderate (G-6-PDH, F-1,6-PA, LDH and GDH), moderate to strong (ATPase at pH 7.4, nonspecific esterase and acid phosphatase) and strong (G-6-PA, NADH2,-TR, NADPH2-TR, ATPase at pH 8.5 and 9.4 and alkaline phosphatase).     

Detection of insect prey by wild common marmosets: The effect of color vision

Most species of New World primates have an unusual color vision pattern that can affect an individual's ability to detect food. Whereas males can only be dichromatic, females can be either dichromatic or trichromatic. Trichromats are expected to have an advantage in detecting conspicuous food whereas dichromats should be better at locating cryptic resources. Here we aimed to understand how color vision phenotype influences insect foraging by five groups of common marmosets living in a semiarid environment. We recorded insect predation events, noting morphotype and color of the captured insect, and the substrate from which it was captured. Color modeling suggested that, for all values of chromatic contrast resulting from comparing the measured insect–substrate pairs, trichromats outperformed dichromats. Females showed an overall higher insect capture rate than males. Females also showed a higher capture rate of conspicuous insects but there was no sex difference for the capture of cryptic insects. When we compared only dichromatic individuals there was no difference between sexes. These findings suggest that differences found in capture rate related not only to sex but also to visual polymorphism and that the latter is a crucial factor determining insect capture rate in common marmosets. Nevertheless, these results should be interpreted with caution because of the small number (three) of dichromat females and the unknown phenotype of the remaining females. Our results support the balancing selection hypothesis, suggesting that the advantage of one phenotype over the other may depend on environmental circumstances. This hypothesis has recently been considered as the most plausible for the maintenance of visual polymorphism in New World primates.     

Sociality in Callithrix penicillata: II. Individual Strategies During Intergroup Encounters

In social animals, intergroup interactions, whether through agonistic and competitive behaviors or affiliative ones, can influence important parameters such as home range, territory sizes, and access to resources, which may directly affect both female and male fitness. We studied the intergroup interaction patterns of a wild group of black-tufted-ear marmosets (Callithrix penicillata) in central Brazil. Agonistic interactions occurred at low frequencies during intergroup encounters. The marmosets directed agonistic interactions without physical aggression primarily against same-sex individuals, suggesting that male and female aggression patterns are shaped by their sexual interests. However, females of the focal group also directed agonistic behavior toward extragroup males that attempted copulation. The marmosets appeared to use intergroup encounters to gather information about possible partners and extragroup reproductive opportunities. Intergroup sexual interactions occurred mainly in the form of copulations or attempted copulations by all adults, with the exception of the dominant female. Our results suggest that a possible reproductive strategy used by males is to attempt fertilization of extragroup females. Adult males copulated with the same extragroup female during several opportunities, which suggests sperm competition or the establishment of social bonds with neighboring females.     

Sexual differences in colour and size in the Great Spotted Cuckoo Clamator glandarius

The appearance of plumage in brood parasites represents an evolutionary conflict between sexual selection that favours colourful plumages, and parasite–host coevolution that favours crypsis. In this study we quantified the degree of sexual dimorphism from a sample of 179 Great Spotted Cuckoos and determined which features facilitate accurate sex discrimination. In addition, we collected spectrophotometric measures of two colour patches (the crown and the throat) and ran visual models to test for physical and bird‐perceivable sexual differences in coloration. We found that males are bigger and brighter than females in both colour patches. Using visual modelling techniques we demonstrate for the first time that adult Great Spotted Cuckoos are sexually dichromatic in an avian visual framework.     

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.     

Color Vision in <Emphasis Type="Italic">Leontopithecus chrysomelas</Emphasis>: A Behavioral Study

We assessed the color discriminations by golden-headed lion tamarins (Leontopithecus chrysomelas) via a series of tasks involving a behavioral paradigm that maximizes the naturalness of the stimuli. The stimuli were pairs of Munsell color chips used in earlier experiments with human dichromats. We tested 3 male and 3 female monkeys with stimuli of random brightness values in order to assure that discriminations were based on color rather than brightness cues. Results indicate that each male and one female presented random performances for stimuli resembling hue conditions under which tamarins forage: oranges vs. greens. Two females exhibited discriminations consistent with allelic trichromacy. Findings indicate the presence of an M/L cone opsin polymorphism, a condition of most platyrrhines that is characterized by dichromatic and/or trichromatic females and dichromatic males. Interspecific differences in allelic frequency among lion tamarins raises the possibility that habitat fragmentation is affecting heterozygous frequencies, a trend that could impact tamarin foraging efficiency.     

Cross-fostering between two species of marmosets (Callithrix jacchus) and Callithrix penicillata)

Cross-fostering technique can be defined as adoption of infants by adults of other species. This phenomenon is poorly investigated because very young animals have few opportunities to interact peacefully with non-conspecific adults, either in captivity or in natural conditions. This study describes the induction of cross-fostering in captivity between white tufted-ear (Callithrix jacchus) and black tufted-ear marmosets (Callithrix penicillata). We conclude that this technique can be very useful for preserving the life of rejected by parents or orphan infants, mainly in the case of species with low reproduction rate in captivity or those threatened by extinction, as well for investigating the environmental effects on the typical behavior of species (courtship, food preference, vocalization patterns, e.g.).     

Non-random association of opsin alleles in wild groups of red-bellied tamarins (Saguinus labiatus) and maintenance of the colour vision polymorphism

The remarkable X-linked colour vision polymorphism observed in many New World primates is thought to be maintained by balancing selection. Behavioural tests support a hypothesis of heterozygote advantage, as heterozygous females (with trichromatic vision) exhibit foraging benefits over homozygous females and males (with dichromatic vision) when detecting ripe fruit on a background of leaves. Whilst most studies to date have examined the functional relevance of polymorphic colour vision in the context of foraging behaviour, alternative hypotheses proposed to explain the polymorphism have remained unexplored. In this study we examine colour vision polymorphism, social group composition and breeding success in wild red-bellied tamarins Saguinus labiatus. We find that the association of males and females within tamarin social groups is non-random with respect to colour vision genotype, with identified mating partners having the greatest allelic diversity. The observed distribution of alleles may be driven by inbreeding avoidance and implies an important new mechanism for maintaining colour vision polymorphism. This study also provides the first preliminary evidence that wild trichromatic females may have increased fitness compared with dichromatic counterparts, as measured by breeding success and longevity.     

Callithrix penicillata as a nonhuman primate model for strongyloidiasis

In order to better understand experimental strongyloidiasis in small New World primates, and to evaluate aspects of reinfection and immunosuppression induced by glucocorticoids, nine specimens of Callithrix penicillata (Primates: Cebidae) were administered (by subcutaneous injection, sc) 3000 infective larvae of a strain of Strongyloides venezuelensis (Rhabditida: Strongyloididae) that had been maintained in successive passages through AKR/J mice since 1987. The mean prepatent period was 5.6 ± 0.7 days post-infection (DPI). The mean patent period of infection among the untreated animals (marmosets 1-7) was 123.4 ± 61.4 DPI. Two animals (marmosets 8 and 9) received dexamethasone (2.5 mg/kg, sc) for five consecutive days starting on the 20th day after infection, but this treatment did not alter the course of the infection, and the patent period for these animals was 100.5 ± 58.7 DPI (59 and 142, respectively). Stool examination showed that the highest quantities of parasite eggs were expelled between the 8th and 19th days after inoculation of the larvae. Thereafter, there was a gradual reduction in the number of parasite eggs in feces of all marmosets. During the chronic phase of the infection, before completely negative parasitological findings were obtained, the parasitological examinations were intermittently positive. Reinfection of three of these animals did not result in new positive examinations. However, given the receptiveness of these animals to initial infection with S. venezuelensis and their similarities to human beings, it is proposed that C. penicillata could be used as a nonhuman primate model for experimental strongyloidiasis.     

Oxytocin and vasopressin enhance responsiveness to infant stimuli in adult marmosets

The neuropeptides oxytocin (OT) and arginine-vasopressin (AVP) have been implicated in modulating sex-specific responses to offspring in a variety of uniparental and biparental rodent species. Despite the large body of research in rodents, the effects of these hormones in biparental primates are less understood. Marmoset monkeys (Callithrix jacchus) belong to a clade of primates with a high incidence of biparental care and also synthesize a structurally distinct variant of OT (proline instead of leucine at the 8th amino acid position; Pro⁸-OT). We examined the roles of the OT and AVP systems in the control of responses to infant stimuli in marmoset monkeys. We administered neuropeptide receptor agonists and antagonists to male and female marmosets, and then exposed them to visual and auditory infant-related and control stimuli. Intranasal Pro⁸-OT decreased latencies to respond to infant stimuli in males, and intranasal AVP decreased latencies to respond to infant stimuli in females. Our study is the first to demonstrate that Pro⁸-OT and AVP alter responsiveness to infant stimuli in a biparental New World monkey. Across species, the effects of OT and AVP on parental behavior appear to vary by species-typical caregiving responsibilities in males and females.     

Neuroendocrine response to female ovulatory odors depends upon social condition in male common marmosets, Callithrix jacchus

Male mammals show rapid behavioral and hormonal responses to signals from sexually receptive females. However, rapid endocrine responses to female signals have not been observed in a nonhuman primate. Here, we tested the behavioral and hormonal response of male common marmosets (Callithrix jacchus) to isolated scent secretions from ovulatory females or to vehicle control scent. Fifteen males were tested in their home cage for behavioral and hormonal responses. These males showed increased investigative and arousal behaviors to the ovulatory scent compared to the vehicle scent. Time sniffing the scent substrate and the duration of erections were significantly elevated in relation to the vehicle scent. Thirty minutes after presentation of ovulatory scent, males showed a significant increase in testosterone compared to the vehicle, but there was no difference in cortisol values. To better control for scent presentation, 15 additional males were tested under a controlled scent exposure. Current social housing condition influenced the male's testosterone response to the ovulatory scent. Single and paired males showed significant increases in testosterone levels with the ovulatory scent but did not increase cortisol levels. Single males also showed the highest change in testosterone with the ovulatory scent, but fathers showed no changes. These results indicate that a rapid hormonal response to sexually arousing cues occurs in marmosets, and the data suggest that a male's social condition influences how he responds to sexually relevant cues.     

Variation in circulating and excreted estradiol associated with testicular activity in male marmosets.

Concentrations of estradiol (E2) are high in the urine of male marmosets, and links between E2 and paternal behavior have been proposed in black tufted-ear marmosets, Callithrix kuhlii. However, it is not clear whether urinary E2 in male marmosets: 1) represents production of E2 associated with testicular activity, 2) is associated with adrenal steroid production, or 3) merely reflects peripheral conversion of T to E2 prior to excretion. We tested the hypothesis that urinary E2 in male marmosets represents estrogen production-associated activity in the hypothalamus-pituitary-gonad (HPG) axis. We treated adult male marmosets with gonadotropin-releasing hormone (GnRH), and used saline-treated males as controls. We collected blood and urine samples from males before and after treatment, and assayed them for testosterone (T), estradiol (E2), and cortisol (CORT). Treatment with GnRH increased circulating T and E2, and prevented decreases in levels of urinary T and E2. Moreover, changes in plasma and urinary E2 after treatment were positively correlated with post-treatment changes in T. Thus, our data are consistent with both plasma and urinary E2 in male marmosets increasing as a result of testicular stimulation. However, treatment with GnRH did not affect plasma or urinary CORT concentrations of males, suggesting that the E2 excreted by males is not of adrenal origin. We also compared urinary T, E2, and CORT levels between intact and castrated male common marmosets (Callithrix jacchus). Urinary concentrations of T and E2, but not CORT, were significantly lower in castrated than in intact males, further suggesting that E2 in male marmosets varies with testicular activity.     

Experimental infection with Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis in the marmoset, Callithrix penicillata (Primates:Callithricidae)

Fourteen marmosets (Callithrix penicillata) were inoculated intradermally with promastigotes and/or amastigotes of Leishmania (Viannia) braziliensis (L. (V) b.) strains MHOM/BR/83/LTB-300 MHOM/BR/85/LTB-12 MHOM/BR/81/LTB-179 and MHOM/BR/82/LTB-250. The evolution of subsequent lesions was studied for 15 to 75 weeks post-inoculation (PI). All but 3 of the L. (V) b. injected marmosets developed a cutaneous lesion at the point of inoculation after 3 to 9 weeks, characterized by the appearance of subcutaneous nodules containing parasites. Parasites were isolated by culture (Difco Blood Agar) from all 11 positive animals. The maximum size of the lesions was variable and ranged between 37 mm2 to 107 mm2. Ulceration of primary nodules became evident after 3 to 12 weeks in all infected marmosets, but was faster and larger in 5 of the 11 animals. The active lesions persisted in 9 out of 11 Callithrix until the end of the observation period, which varied from 15-75 weeks. In 3 animals spontaneous healing of their lesions (13 to 25 weeks, PI) was observed but with cryptic parasitism. In another 2 infected animals there was regression followed by reactivation of the cutaneous lesions. The appearance of smaller satellite lesions adjacent to primary ones, as well as metastatic lesions to the ear lobes, were documented in 2 animals. Promastigotes of L. (Leishmania) amazonensis (L. (L) a.) MHOM/BR/77/LTB-16 were inoculated in 1 marmoset. This animal remained chronically infected for 6 months and the lesion developed in a similar manner to L. (V) b. infected marmosets. No significant differences in clinical and parasitological behaviour were observed between promastigote or amastigote derived infections of the 2 species.(ABSTRACT TRUNCATED AT 250 WORDS)     

A marmoset model for some New World dermatotropic leishmaniases

Callithrix penicillata is a good model for dermatotropic strains of some New World Leishmania species (L. mexicana mexicana, L. m. amazonensis, and L. braziliensis guyanensis). Both amastigotes and promastigotes readily infect these primates, with a relative short period of incubation. The developed lesions parallel those found in man, and despite the self healing presented by some marmosets, cell and serum immunological responses are presented. Skin alterations are confined to the site of inoculum, and visceralization is very rarely found. A good response to standard antimonial treatment makes the model useful for preclinical experiments with promising compounds.