Age of epiphyseal closure in tamarins and marmosets

Estimates of the chronological age for animals of unknown age provide useful information for medical, demographic, and evolutionary studies. Skeletal development, as indicated by epiphyseal closure, can be used to estimate an animal's chronological age or specify its stage of development. Many studies of Primate skeletal development have used animals of unknown age, with the order of epiphyseal closure providing a relative age for each animal. This study examines the age of epiphyseal closure at 22 epiphyseal sites using animals of known age at death in three calitrichid species (Saguinus fuscicollis, Saguinus oedipus, and Callithrix jacchus). The observed average age of epiphyseal closure is similar in these tamarins and marmosets. There is a significant difference in rate of development between the species. Regression equations can predict the age of unknown animals to within 4.8 months for S. fuscicollis, 8.6 months for S. oedipus, and 7.6 months for C. jacchus (twice the standard error of the estimate). These age estimates allow us to determine if an animal is relatively mature or immature, but are largely unacceptable for studies in which precise age estimates are necessary. The order of epiphyseal closure is similar across 11 monkey species (using additional data from published literature) and supports the suggestion of a general pattern in Primate skeletal development. Am. J. Primatol. 41:129–139, 1997. © 1997 Wiley-Liss, Inc.     

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.     

The regulation of maternal behaviour in marmosets and tamarins

This article reviews a long-term investigation into the roles of (1) experience obtained with infants during development and postnatally, and (2) levels of reproductive-steroid hormones during late pregnancy, in the regulation of maternal caregiving motivation and behaviour in the red-bellied tamarin (Saguinus labiatus) and the common marmoset (Callithrix jacchus) (family Callitrichidae, Order Primates). Both observational studies, e.g. post hoc analysis of the relationship between developmental caregiving experience and infant-rearing success, and manipulative studies, e.g. direct analysis of the effects of sex-steroid administration on maternal motivation, were performed. In red-bellied tamarins, a breeding female's infant-rearing success was related to its caregiving experience obtained during development and postpartum/postnatally. In multiparous females lacking developmental caregiving experience, postpartum maternal caregiving behaviour and infant-rearing success were related to prepartum urinary oestradiol levels. In nulliparous common marmosets, caregiving of infant-siblings increased as a consequence of physical interaction with parent-infant dyads, late pregnancy, and exposure to late pregnancy-like levels of progesterone and oestradiol. The evidence for a dual mechanism of endocrine and experiential regulation of caregiving in these monkeys is discussed in terms its evolution and function.     

Gum feeder as environmental enrichment for zoo marmosets and tamarins

Tamarins and marmosets are small-bodied social callitrichines. Wild callitrichines feed on exudates, such as sap and gum; particularly, marmosets are mainly gummivores, while tamarins consume gums only occasionally and opportunistically. Zoo marmosets and tamarins are usually provided with gum arabic as an alternative to the exudates normally found in the wild. The aim of this study was to evaluate the effects of a gum feeder on the behavior and well-being of four zoo-managed callitrichines. We studied four cotton-top tamarins (Saguinus oedipus), four red-handed tamarins (S. midas), two pygmy marmosets (Cebuella pygmaea), and three Geoffroy's marmosets (Callithrix geoffroyi) housed at Parco Natura Viva (Italy). We conducted the study over two different periods, a baseline (control, without the gum feeder) and then a gum feeder (when the gum feeder was provided) period. We used continuous focal animal sampling to collect behavioral data, including durations of social and individual behaviors. We collected 240 min of observations per period per study subject, with a total of 3,120 min for all the subjects in the same period and of 6,240 min in both periods. We analyzed data by using nonparametric statistical tests. First, we found that the gum feeder promoted species-specific behaviors, such as exploration, and diminished self-directed behaviors, suggesting an enriching effect on tamarin and marmoset behavior. Moreover, in red-handed tamarins, the provision of the gum feeder reduced the performance of self-directed and abnormal behavior, specifically coprophagy. These results confirm that gum feeders are effective foraging enrichment tools for zoo marmosets and tamarins.     

Quantitative molecular assessment of chimerism across tissues in marmosets and tamarins

Background

Periodic spacing of A-tracts (short runs of A or T) with the DNA helical period of ~10?C11?bp is characteristic of intrinsically bent DNA. In eukaryotes, the DNA bending is related to chromatin structure and nucleosome positioning. However, the physiological role of strong sequence periodicity detected in many prokaryotic genomes is not clear.

Results

We developed measures of intensity and persistency of DNA curvature-related sequence periodicity and applied them to prokaryotic chromosomes and phages. The results indicate that strong periodic signals present in chromosomes are generally absent in phage genomes. Moreover, chromosomes containing prophages are less likely to possess a persistent periodic signal than chromosomes with no prophages.

Conclusions

Absence of DNA curvature-related sequence periodicity in phages could arise from constraints associated with DNA packaging in the viral capsid. Lack of prophages in chromosomes with persistent periodic signal suggests that the sequence periodicity and concomitant DNA curvature could play a role in protecting the chromosomes from integration of phage DNA.     

Visualization and biopsy of the colon in tamarins and marmosets by endoscopy

Endoscopic visualization and biopsy have been performed under anesthesia in more than 65 tamarins and marmosets to study the pathogenesis of colitis and cancer of the colon. This procedure allows examination of the large bowel from the anus to the cecum and has been repeated at 2-6 month intervals with few complications. However, care must be exercised not to perforate the colon. Successful use of this technique will permit study of the pathogenesis of colonic diseases throughout the life of the animal and should provide cause-effect information about colitis and colon cancer in tamarins that may apply to the human diseases.     

Evaluation of a pelleted diet in a colony of marmosets and tamarins

By offering various pelleted diet modifications to five species of Callitrichidae, a palatable 24% protein diet was developed. The animals received limited fruit supplement, and families received an additional meal of commercial baby food. The pellets supplied approximately 75% of dietary energy and 95% of total protein. In 15 months on this regimen, mortality dropped drastically and fertility improved. No signs of a nutritional deficiency were observed. It was concluded that the nutrient levels of this diet were adequate or above actual requirements.     

Prevalence of ocular disease in a colony of tamarins and marmosets.

In a large tamarin and marmoset experimental colony, 526 animals were examined by biomicroscopy and ophthalmoscopy for the presence of ocular disease. In 109 animals, there were 147 abnormalities involving the eyelids, cornea, iris, lens, retina or optic nerve. Most abnormalities were unimportant in terms of ocular function, but a few did cause loss of vision and included diffuse, progressive retinal atrophy and a severely traumatized globe. The survey indicated that while usually minor, ocular disease in the tamarin and marmoset was widespread.     

Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates

Among primates, catarrhines (Old World monkeys and apes) andcertain platyrrhines (New World monkeys) possess trichromaticcolor vision, which might confer important evolutionary advantages,particularly during foraging. Recently, a polymorphism has beenshown to shift the spectral sensitivity of the X-linked opsinprotein in certain strepsirrhines (e.g., Malagasy lemurs); however,its behavioral significance remains unknown. We assign genotypesat the X-linked variant to 45 lemurs, representing 4 species,and test if the genetic capacity for trichromacy impacts foragingperformance, particularly under green camouflage conditionsin which red detection can be advantageous. We confirm polymorphismat the critical site in sifakas and ruffed lemurs and fail tofind this polymorphism in collared lemurs and ring-tailed lemurs.We show that this polymorphism may be linked to "behavioraltrichromacy" in heterozygous ruffed lemurs but find no comparableevidence in a single heterozygous sifaka. Despite their putativedichromatic vision, female collared lemurs were surprisinglyefficient at retrieving both red and green food items undercamouflage conditions. Thus, species-specific feeding ecologiesmay be as important as trichromacy in influencing foraging behavior.Although the lemur opsin polymorphism produced measurable behavioraleffects in at least one species, the ruffed lemur, these effectswere modest, consistent with the modest shift in spectral sensitivity.Additionally, the magnitude of these effects varied across individualsof the same genotype, emphasizing the need for combined geneticand behavioral studies of trichromatic vision. We conclude thattrichromacy may be only one of several routes toward increasedforaging efficiency in visually complex environments.     

Miocene marmosets: First fossil evidence

The first fossil remains of marmosets, an isolated incisor, premolar, and molar, all similar in size toCallithrix species, have been discovered in the middle Miocene La Venta fauna of Colombia. The M¹ is referred to a new genus and species,Micodon kiotensis, characterized by a fully developed hypocone and low occlusal relief. The P₄ and I¹ resemble those ofCallithrix, suggesting a close affinity with callitrichin marmosets. In combining small size with a four-cusped morphology,Micodon demonstrates the shortcomings of typological definitions of platyrrhine families and suggests that small body size may have preceded the tricuspid molar pattern in marmoset evolution. The 14- to 15-Ma date for the La Venta suggests that marmosets are an at least moderately ancient radiation, contrary to estimates based upon the molecular clock.     

Monitoring ovarian function in marmosets and tamarins by the measurement of urinary estrogen metabolites

Practical aspects of urinary estrogen analysis were considered with regard to establishing simple and reliable methods for monitoring ovarian function in marmosets and tamarins. Changes in the hormone:creatinine ratio in small volumes of urine from the common marmoset were significantly correlated with changes in 24-h excretion. Comparison of the metabolism and excretion of estrogens during the ovarian cycle in the common marmoset and cottontop tamarin revealed interesting species differences. High concentrations of conjugated estrone were measured in marmoset plasma, but estradiol 17β was the predominant estrogen in urine. In contrast, estrone was the most abundant estrogen measured in tamarin urine. Both species excreted very little estriol. Sulfates and glucuronides were present in urine in similar proportions before ovulation in the marmoset, although after ovulation sulfates were the more abundant. Conversely, most of the estrogens in tamarin urine appeared to be conjugated as glucuronides. Direct assay for estrone sulfate was applied to the measurement of urinary estrogen excretion during the ovarian cycle in a marmoset. The results compared well with those for total estradiol 17β after hydrolysis and ether extraction. The use of direct assays for conjugated estrogens in small volumes of urine is suggested as a practical method for monitoring ovarian function in marmosets and tamarins.     

Color vision: retinal blues

Two complementary studies have resolved the circuitry underlying green-blue color discrimination in the retina. A blue-sensitive interneuron provides the inhibitory signal required for computing green-blue color opponency.     

Comment on the evolution of claw-like nails in callitrichids (marmosets/tamarins)

A recently proposed scenario for the evolution of a unified complex of exudativory, vertical clinging, and claw-like nails in callitrichids is examined. Consideration of behaviors and morphologies exhibited by Callimico goeldii leads to a decoupling of this "complex," with the early occurrence of claws and vertical clinging in the callitrichid lineage and only later, in some descendents, the development of exudativory and possible related behaviors.     

Color vision: putting it together

Color vision depends on the visual system comparing signals that originate in different classes of cone photoreceptors. New work shows that the different classes of cones are not only distributed irregularly, but in different individuals they are present in very variable proportions. Surprisingly, this does not affect color vision.     

Color vision: mice see hue too

A transgenic mouse has been generated with three cone types, instead of the normal murine two. Remarkably, some of these mice use the extra cone to make trichromatic color discriminations similar to those that are the basis of human color vision.     

Color and polarization vision in foraging Papilio

This paper gives an overview of behavioral studies on the color and polarization vision of the Japanese yellow swallowtail butterfly, Papilio xuthus. We focus on indoor experiments on foraging individuals. Butterflies trained to visit a disk of certain color correctly select that color among various other colors and/or shades of gray. Correct selection persists under colored illumination, but is systematically shifted by background colors, indicating color constancy and simultaneous color contrast. While their eyes contain six classes of spectral receptors, their wavelength discrimination performance indicates that their color vision is tetrachromatic. P. xuthus innately prefers brighter targets, but can be trained to select dimmer ones under certain conditions. Butterflies trained to a dark red stimulus select an orange disk presented on a bright gray background over one on dark gray. The former probably appears darker to them, indicating brightness contrast. P. xuthus has a strong innate preference for vertically polarized light, but the selection of polarized light changes depending on the intensity of simultaneously presented unpolarized light. Discrimination of polarization also depends on background intensity. Similarities between brightness and polarization vision suggest that P. xuthus perceive polarization angle as brightness, such that vertical polarization appears brighter than horizontal polarization.