Range extension of the vulnerable dwarf marmoset, Callibella humilis (Roosmalen et al. 1998), and first analysis of its long call structure

We present two new records for the vulnerable dwarf marmoset, Callibella humilis. The first record, based on observed and photographed individuals, is from a campinarana area on the left (west) bank of the Rio Madeirinha, a left (west)-bank tributary of the Rio Roosevelt in the state of Amazonas, municipality of Novo Aripuanã and extends the distribution of the species ~270 km southwards, to the left (west) bank of the rio Roosevelt. The second record is based on an individual collected from the mouth of the Rio Roosevelt, at less than 10 km from the type locality of Mico marcai. This indicates that the species occurs sympatrically with M. marcai and probably Mico melanurus. We also present the first sonogram analysis of its long call structure, which shows some similarities, in the note duration and frequency, with Cebuella pygmaea and Mico argentatus.     

Rondon’s Marmoset, <Emphasis Type="Italic">Mico rondoni</Emphasis> sp. n., from Southwestern Brazilian Amazonia

We describe Rondon’s marmoset (Mico rondoni sp. n.) from the Rio Jamari in the Brazilian state of Rondônia and differentiate the species from other Amazonian marmosets on the basis of morphological, genetic, and zoogeographic characteristics. Mico rondoni sp. n. is a typical bare-eared marmoset of predominantly grayish coloration and unpigmented face and cheiridia, which contrasts clearly with its more brownish and pigmented parapatric congeners Mico melanurus and M. nigriceps. Genetically, the new species is unquestionably distinct from Mico emiliae, with which it had been synonimized previously. The geographic range of the new species is defined as the area delimited by the Mamoré, Madeira, and Jiparaná rivers to the west, north, and east, respectively, and the Serra dos Pacaás Novos, to the south, where it is substituted by Mico melanurus. Depending on its exact limits, this range may cover an area of little more than 100,000 km². A characteristic of the ecology of Mico rondoni sp. n. is its range-wide sympatry with the similarly sized tamarin Saguinus fuscicollis weddelli, which may be a key factor determining the rarity or absence of the new species from many areas within its geographic range. Its apparent scarcity may make the new species exceptionally vulnerable to the effects of the intense human colonization occurring throughout much of its known range, and provoke cause for concern for its long-term survival.     

The myoglobin of primates: the Night Monkey, Aotes trivirgatus (Cebidae,Platyrrhini, Anthropoidea)

The amino acid sequence of the myoglobin of the South American Night Monkey, Aotes trivirgatus, is identical to that of the marmoset (Callithrix jacchus [1]) except for residue 21 which is isoleucine in the marmoset, like in all other anthropoids, but valine in Aotes. Analysis of a possible pathway of the evolution of Aotes myoglobin using 18 known primate myoglobin sequences [2–5] supports the classification of the Night Monkey within Anthropoidea and Platyrrhini but it indicates that this species might be more closely related to the marmoset (family Callitrichidae) than to the family Cebidae as a member of which it is commonly classified.     

Mitochondrial COII gene sequences provide new insights into the phylogeny of marmoset species groups (Callitrichidae,Primates)

Mitochondrial cytochrome oxidase II (COII) gene sequences (549 base pairs) were used to investigate the taxonomic relationships among 12 marmoset (Callithrix, Cebuella and Mico) taxa. A large number of substitutions were found in the third base codon positions, providing a strong phylogenetic signal in a gene coding a conserved protein. Despite the significant affinity between the 2 Amazonian genera Cebuella and Mico, found in recent molecular studies, the analysis presented here did not resolve convincingly the phylogenetic relationships between the 3 genera. Mico nevertheless formed 3 distinct clades, reflecting a basic division of species groups based on geographic distribution (east or west of the Rio Tapajós) rather than morphology (presence or absence of auricular hair). This supports the taxonomic distinction of the allopatric emiliae forms. In Callithrix, Callithrix aurita forms a distinct clade, but the remaining morphotypes form a somewhat contradictory cluster, possibly resulting from an extremely rapid radiation.     

A New Subspecies of <Emphasis Type="Italic">Saguinus fuscicollis</Emphasis> (Primates,Callitrichidae)

Saddleback tamarins (Saguinus fuscicollis, S. melanoleucus, and S. tripartitus) occur in the upper Amazon, west of the rios Madeira and Mamoré–Guaporé to the Andes. They currently comprise 13 species and subspecies in Bolivia, Brazil, Colombia, Ecuador, and Peru. Here we report on a previously undescribed subspecies of Saguinus fuscicollis from the interfluvium of the lower rios Madeira and Purus in the central Amazon of Brazil. It is a distinct form with a very pronounced mottling on the back giving the appearance of a saddle, a characteristic shared by the 3 species, and the reason for their collective common name. The lack of a white superciliary chevron and its highly mottled ochraceous-dark brown to black saddle that extends from the scapular region to the base of the tail distinguish the new taxon from Saguinus fuscicollis weddelli. The latter characteristic also distinguishes it from another saddleback tamarin (Saguinus fuscicollis ssp.) that has been reported immediately to the south of its range in the same interfluvium. We compare pelage coloration, external characters and craniometric measurements with its geographically closest relatives, Saguinus fuscicollis weddelli and S. f. avilapiresi, and indicate its probable geographic distribution in a small area between the rios Madeira and Purus, just south of the Rio Amazonas.     

The skin of primates. XLI. The skin of the silver marmoset—Callithrix (= Mico) Argentata

The skin of the silver marmoset, Callithrix (= Mico) argentata Linnaeus, has many outstanding characteristics. The unusually thin epidermis and dermis are generally devoid of melanotic melanocytes. The surface of the interramal gular region is peppered with small, elevated papillae; that of the corpus penis is characterized by keratinized, proximally directed hollow spines in whose cavities are organized nerve end-organs and capillary loops. Cholinesterase-reactive papillary nerve end-organs and Meissner corpuscles populate all volar friction surfaces. A highly vascular dermis and subcutaneous fat pad partially contribute to the characteristic rubicund color of the face, external ears, and anogenital region. Many body surface hairs are accompanied by the classic Haarscheibe of Pinkus. Sinus hairs are plentiful; a circumscribed vibrissa-bearing eminence is located on the ventral ulnar aspect of each wrist. Alkaline phosphatase-positive, stellate-shaped cells are found on the outer root sheath and epithelial sac of active and quiescent hairs in all cephalic regions; such cells are not argyrophilic, aurophilic, or osmiophilic. Hairs grow in linear perfect sets of 3 to 5 follicles; they do not grow singly on the cheek. Large sebaceous glands contain alkaline phosphatase in their peripheral acini; extensive fields of gigantic multilobular sebaceous glands contribute to the distinct, opaque-white color of the scrotal skin. Numbers of apocrine sweat glands are diminished in cephalic regions but one gland occurs with each hair follicle in the axilla, scrotum, suprapubic region, and ulnar eminence. Relatively avascular eccrine sweat glands are confined to the volar friction surfaces. Their secretory coils contain sporadically distributed glycogen and phosphorylase and surrounding nerves are much more reactive for acetyl- than butyrylcholinesterase.     

The black-tailed marmoset (Callithrix argentata melanura) recorded from paraguay

The black-tailed marmoset (Callithrix argentata melanura) occurs in central-western Brazil and adjacent parts of Bolivia, and is the only member of the genus (Callithrix) to occur naturally outside Brazil. Data presented in this paper extend the range of this marmoset at least 200 km to the southwest into yet another country, Paraguay.     

Comparative chromosomal study of five taxa of genus Callithrix,group Jacchus (Platyrrhini,primates)

The karyotypes of four marmoset species of the Callithrix jacchus group (C. aurita, C. kuhlii, C. geoffroyi, and C. penicillata) were investigated. The patterns of G-, C-, and NOR-bands of these karyotypes were compared with those of C. jacchus, previously described, in order to clarify the taxonomic relationships of this species group. All species present 2n = 46, 14 uni- and 30 biarmed autosomes, a median size submetacentric X chromosome, and the same NOR-band patterns. No rearrangement or constitutive heterochromatic variation differentiate these species, which differ only in the morphology of the Y chromosome. The data obtained indicate that, from the chromosomal point stand, the marmoset species of C. jacchus group constitute a homogeneous clade. Am J Primatol 41:53–60, 1997. © 1997 Wiley-Liss, Inc.     

Looking to the past and the future: were the Madeira River rapids a geographical barrier to the boto (Cetacea: Iniidae)?

In the present study we tested if a series of 18 rapids on the upper Madeira River form an effective barrier to gene flow, and in particular if they delimit the distribution of the boto Inia boliviensis—which it is believed to occurs only in the Bolivian sub-basin, above the rapids—and I. geoffrensis, which occurs throughout the Amazon basin and below the upper Madeira River rapids. We analyzed 125 individuals from the Madeira River basin sampled from upstream and downstream of the rapids. As the two species are morphologically similar, we used diagnostic molecular characters from known reference specimens to assign individuals to species. We observed that all individuals of Inia from the Bolivian sub-basin up to almost the mouth of the Madeira River belong to the species I. boliviensis. Therefore we concluded that the rapids do not delimit the distribution of I. boliviensis upstream and I. geoffrensis downstream of the rapids as previously hypothesized. Since we registered I. boliviensis along almost the entire length of the Madeira River, we estimated gene flow, time of divergence and effective population sizes of the upstream (Bolivian) and downstream (Madeira River) groups of I. boliviensis using IMa2. We concluded that gene flow is uni-directional from the upstream to the downstream group. Divergence time between the two groups was estimated to have occurred ~122 thousand years ago. The coalescent effective population size for the upstream group was estimated at ~131 thousand individuals, while for the downstream group it was estimated at ~102 thousand individuals. Recently two dams have been constructed in the region of the rapids; neither has a mechanism that will maintain connectivity between the upstream and downstream regions, and together with anthropogenic alterations to the hydrodynamic regime and ecology of the river will likely pose serious long-term and short-term consequences for I. boliviensis and other aquatic taxa.     

Pasteurella canis infection in a non-human primate black-tailed marmoset (Mico melanurus)—A case report

This study reports the pathological and microbiological findings of pneumonia in a Mico melanurus caused by Pasteurella canis, confirmed for molecular analyses. It demonstrated the importance that wild species represent in the epidemiology of pasteurellosis in anthropic environments, when inserted into urban areas.     

Microcultures of marmoset lymphocytes: I. Response to mitogens

A microtechnique for marmoset lymphocyte cultures is described that allows a 10-fold reduction of cell numbers and the amount of culture medium and radioisotopes. Optimal culture conditions for the response of Saguinus fuscicollis, Saguinus oedipus, and Callithrix jacchus peripheral blood lymphocytes to a variety of mitogens were established. The usefulness of marmoset lymphocyte microcultures for the evaluation of alterations of immunocompetence associated with experimental viral disease and its possible application for immunogenetic studies are discussed.     

Differential infant carrying in captive and wild common marmosets (Callithrix jacchus)

Callitrichids are communal breeders that lack sexual dimorphism, and only a few studies have examined behavioral gender differences among them. The purpose of this study was to investigate gender differences in infant carrying in 16 captive and seven wild common marmoset groups. Our results showed that female–female twin pairs were carried significantly more often by fathers than were male–male and male–female pairs both in the wild and in captivity. We suggest these differences may be related to different reproductive potentials of male and female Callithrix jacchus and possibly to future breeding competition among females.     

Loaches of the genus <Emphasis Type="Italic">Barbatula</Emphasis> (Nemacheilinae) of the Zavkhan River basin (Western Mongolia)

Two sympatric species of Siberian loaches are recorded in the Zavkhan River basin (Great Lakes Depression, Western Mongolia) and described as new for science: Barbatula conilobus and B. dsapchynensis spp. n. The former species, most likely, is widely distributed over the entire river basin, and the latter species, apparently, occurs locally, but in sympatry with B. conilobus. Morphological differences of the new species from other representatives of the genus Barbatula and their relationships are analyzed. Ecological distinctions between the species of the genera Barbatula and Triplophysa in the Zavkhan River basin are described. Possible mechanisms of development of the present fauna of loaches in Mongolia and adjacent territories with an appearance of sympatric species pairs in a single water basin are discussed.     

An Overview of Models,Methods, and Reagents Developed for Translational Autoimmunity Research in the Common Marmoset (Callithrix jacchus)

The common marmoset (Callithrix jacchus) is a small-bodied Neotropical primate and a useful preclinical animal model for translational research into autoimmune-mediated inflammatory diseases (AIMID), such as rheumatoid arthritis (RA) and multiple sclerosis (MS). The animal model for MS established in marmosets has proven their value for exploratory research into (etio) pathogenic mechanisms and for the evaluation of new therapies that cannot be tested in lower species because of their specificity for humans. Effective usage of the marmoset in preclinical immunological research has been hampered by the limited availability of blood for immunological studies and of reagents for profiling of cellular and humoral immune reactions. In this paper, we give a concise overview of the procedures and reagents that were developed over the years in our laboratory in marmoset models of the above-mentioned diseases.     

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.     

Effect of a red oak species gradient on genetic structure and diversity of Quercus castanea (Fagaceae) in Mexico

Incipient reproductive barriers are a common characteristic of oak species. Disruption of these barriers promotes changes in diversity and genetic structure of the species involved. Quercus castanea is a red oak with wide geographic distribution in Mexico, which presents atypically high morphological variability when it occurs in sympatry with other red oak species, suggesting that hybridization may explain the observed variation. We tested if the genetic structure and diversity levels of Q. castanea are related to the number of red oak species growing in sympatry. In total, 14 microsatellite (SSRs) primers (six nSSRs and eight cpSSRs) were used in 120 Q. castanea individuals (20/site) belonging to six populations, where the number of red oak species associated varied from zero to five. Results showed a positive and significant relationship between the genetic diversity of Q. castanea and the number of red oak species growing in sympatry, regardless of the marker type or the parameter of genetic diversity analyzed. Also, we found a higher genetic differentiation of Q. castanea populations using cpSSRs in comparison with nSSRs. Our results suggest that temperate forests with high red oaks species richness co-dominated by Q. castanea promote the increase in this species genetic diversity. From a conservation perspective, high genetic diversity levels of foundation species such as Q. castanea may have positive cascade effects extending to other species in the community.     

Playful interactions in family groups of the common marmoset (Callithrix jacchus jacchus)

Play behaviour in six family groups of common marmosets (Callithrix jacchus jacchus) is described. Playful behaviour patterns comprised a distinct repertoire of behaviour and the patterns formed ordered sequences. The differences in the play of adults and offspring are described and analysed. Adult play was infrequent and most took the form of adult-offspring interactions; it contained fewer bouts of chasing and was less active, and adults elicited fewer bouts. No differences attributable to sex could be determined in the play of offspring and the only pattern that decreased with age was bouncing gait. Possible partner preferences were analysed, and it was found that marmoset twins showed an overall preference for playing with the twin. The vocalizations heard during bouts of play were recorded and analysed and their relationship to non-playful vocalization discussed; during bouts of play younger animals were found to vocalize to older animals. Marmoset play wrestling differed in form from aggressive wrestling, and patterns occurred during aggressive interactions which were not observed in play. The play of marmosets is discussed with regard to the socioecology of the species and compared to the play of other mammalian species.     

Update on the Phylogenetic Systematics of New World Monkeys: Further DNA Evidence for Placing the Pygmy Marmoset (Cebuella) within the Genus Callithrix

We determined DNA sequences spanning the 1.8-kb long intron 1 of the interstitial retinol-binding protein nuclear gene (IRBP) for Callithrix geoffroyi, Callithrix humeralifer, and Callithrix argentata. With the 22 previously determined IRBP intron 1 sequences—21 from the 16 currently recognized genera of New World monkeys—the enlarged IRBP data represent for the marmoset genus Callithrix both its argentata and its jacchus species groups. Maximum-parsimony and neighbor-joining trees, constructed for the 25 aligned IRBP intron 1 sequences, support a provisional phylogenetic classification with three families: Atelidae, containing subfamily Atelinae; Pitheciidae, containing subfamily Pitheciinae; and Cebidae, containing subfamilies Cebinae, Aotinae, and Callitrichinae. In order to have taxa at the same hierarchical rank at equivalent age, this classification has all living callitrichines in a single tribe, Callitrichini, with four subtribes: Saguinina (Saguinus), Callimiconina (Callimico), Leontopithecina (Leontopithecus), and Callitrichina (Callithrix with the pygmy marmoset, Cebuella pygmaea, merged into it). The DNA evidence shows not only that Callithrix must include C. pygmaea to be monophyletic but also that the times of separation of pygmaea and the argentata and jacchus species groups from one another are to be expected (<5 Ma—million years ago) for species in a single genus. On relating the time course of the ceboid radiation to biogeographic information, it appears that in mid-Miocene times (10–11 Ma) a basal callitrichin stock branched into the ancestral population of Saguinus in one clade and the ancestral population of Leontopithecus and Callimico–Callithrix (or Leontopithecus–Callimico and Callithrix) in another clade. The proto-lion tamarins migrated south and eastward, where they were isolated in refugia, becoming the genus Leontopithecus. The stock remaining in Amazonia gave rise to present-day Callimico and Callithrix. The latter genus occupied a vast geographic area, giving rise to the argentata and pygmaea groups in Amazonia and to the jacchus group in central and eastern Brazil.