Neuroscience: unveiling the brain of Saimiri collinsi (Squirrel Monkey).

Behavioral intelligence among non-human primates is a somewhat puzzling area to study, since it is closely linked to the morphology of the central nervous system. However, this morphology is still unknown to science in the case of Saimiri collinsi. As a means of assisting future studies on the social behavior of this species, we analyzed the brains of six adult females from the National Primate Center / Pará, which were sent to the Animal Morphological Research Laboratory at the Federal Rural University of Amazônia after death by natural causes. The animals were fixed in formaldehyde solution (10%) and dissected. The brains were covered externally by the dura mater, with long cerebral hemispheres, although there was a complete absence of gyri. The internal structures which form a part of the telencephalon, diencephalon, midbrain, hindbrain and myelencephalon were identified, with the exception of the mammillary bodies. This condition, when linked to the lissencephaly found in these individuals raises questions about the real learning abilities of this species.

Pelvimetry in Squirrel Monkeys (Saimiri scireus Linnaeus, 1758) / Pelvimetria em macacos-de-cheiro (Saimiri scireus Linnaeus, 1758)

Saimiri sciureus is a neotropical primate widely used in research. However, there are still difficulties regarding their reproduction in vivaria due to the high incidence of dystocia. Dystocia in primates can be caused by cephalopelvic disproportion and in Squirrel Monkeys, pregnancy of large fetuses were reported. This paper describes pelvimetry data of adult females and subadults in specimens of Squirrel Monkeys, from a research colony of Para, Brazil. Pelvic radiographs were obtained in ventrodorsal projections and the following measurements were taken: superior bi-iliac diameter (SBID); inferior bi-iliac diameter (IBID); bi-iliac average diameter (BIAD); right diagonal diameter (RDD); left diagonal diameter (LDD); sacro-pubic diameter (SPD); Based on the obtained diameters, the entrance area of the pelvis (EAP) was also calculated. The average values of the pelvic diameters and EAP in adult females were SBID 1.714cm, BIAD 1.957cm, IBID 1.686cm, RDD 2.771cm, LDD 2.764cm, SPD 2.543cm and EAP 3.9056cm2; and subadult females: 1.588cm SBID, 1.850cm BIAD, 1.625cm IBID, 2.50cm RDD, LDD 2.474cm, 1.95cm SPD and 2.8293 cm2 EAP. Saimiri sciureus pelvis is characterized as dolichopelvic. There was statistical significance between the values for adult females and subadults to SBID, BIAD, RDD, LDD, SPD and EAP. The values of SBID and IBID were lower when compared to the published data for the same species. The result found on this paper will serve as a basis for future studies using pelvic measurements and dystocia prediction of neotropical primates and comparison between different vivaria.(AU)

Saimiri sciureus é uma espécie de primata neotropical muito utilizada como animal de pesquisa. No entanto ainda há dificuldades em biotérios quanto a sua reprodução devido à alta ocorrência de distocia. A distocia em primatas pode ter origem devido à desproporção cefalopélvica, sendo que em macacos-de-cheiro é relatada a gestação de fetos grandes. O presente trabalho descreve dados de pelvimetria em espécimes de macaco-de-cheiro, fêmeas adultas e subadultas provenientes de uma colônia de pesquisa do Pará, Brasil. Foram realizadas radiografias da pelve em projeção ventrodorsal e por meio destas mensurados os diâmetros biilíaco superior (DBIS); diâmetro biíliaco inferior (DBII); diâmetro biilíaco médio (DBIM); diâmetro diagonal direito (DDD); diâmetro diagonal esquerdo (DDE); diâmetro sacro-púbico (DSP); com base nos diâmetros obtidos também foi calculada a área de entrada da pelve (AEP). Os valores médios dos diâmetros pélvicos e da AEP em fêmeas adultas foram: DBIS 1,714cm, DBIM 1,957cm, DBII 1,686cm, DDD 2,771cm, DDE 2,764cm, DSP 2,543cm e AEP 3,9056cm2; e para fêmeas subadultas: 1,588cm DBIS, 1,850cm DBIM, 1,625cm DBII, 2,50cm DDD, 2,474cm DDE, 1,95cm DSP e 2,8293 cm2 AEP. Observou-se que a pelve de Saimiri sciureus é dolicopélvica. Houve diferença estatística significativa entre os valores para fêmeas adultas e subadultas para DBIS, DBIM, DDD, DDE, DSP e AEP. Em comparação com dados da literatura de pelvimetria para S. sciureus observaram-se menores valores de DBIS e DBII. O resultado deste trabalho servirá como base para futuros estudos utilizando-se mensurações pélvicas e predição de distocia em primatas neotropicais e referência para comparação entre S. sciureus de diferentes biotérios.(AU)

Morphologic analysis of sperm from two neotropical primate species: comparisons between the squirrel monkeys Saimiri collinsi and Saimiri vanzolinii.

Sperm morphometry can be applied to identify different animal groups and species and to evaluate sperm quality. Furthermore, knowledge on species-specific differences will help to enhance biological information, as well as to develop efficient reproductive technologies. The aims in the present study were to describe sperm morphometry from the recently characterized species S. collinsi and S. vanzolinii, to verify if the morphometric sperm patterns are similar or different between both species, and to determine if the sperm morphometry is affected by the levels of sperm defects using the S. collinsi as a model. Semen was collected from S. collinsi (n = 10) and S. vanzolinii (n = 2) monkeys, and sperm was submitted to morphological analysis. From the 10 samples from S. collinsi, five presented sperm of poor quality and two subgroups were formed for this species, i.e. high and poor quality sperm. Data on sperm motility and vigour were analysed, as well morphometric parameters on sperm head and tail. It was observed the normal morphometry was correlated with high quality sperm. Poor quality sperm presented smaller and 7% more ellipticity in their head, when compared with high quality sperm. Sperm from S. vanzolinii presented larger head than those from S. collinsi, but tail lengths were similar. Sperm morphometry can be used as a complementary tool to predict sperm motility and vigour for the S. collinsi species, and S. collinsi appear as a suitable model for S. vanzolinii.

Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate.

The squirrel monkey, Saimiri, is a pan-Amazonian Pleistocene radiation. We use statistical phylogeographic methods to create a mitochondrial DNA-based timetree for 118 squirrel monkey samples across 68 localities spanning all Amazonian centers of endemism, with the aim of better understanding (1) the effects of rivers as barriers to dispersal and distribution; (2) the area of origin for modern Saimiri; (3) whether ancestral Saimiri was a lowland lake-affiliated or an upland forest taxa; and (4) the effects of Pleistocene climate fluctuation on speciation. We also use our topology to help resolve current controversies in Saimiri taxonomy and species relationships. The Rondônia and Inambari centers in the southern Amazon were recovered as the most likely areas of origin for Saimiri. The Amazon River proved a strong barrier to dispersal, and squirrel monkey expansion and diversification was rapid, with all speciation events estimated to occur between 1.4 and 0.6Ma, predating the last three glacial maxima and eliminating climate extremes as the main driver of squirrel monkey speciation. Saimiri expansion was concentrated first in central and western Amazonia, which according to the "Young Amazon" hypothesis was just becoming available as floodplain habitat with the draining of the Amazon Lake. Squirrel monkeys also expanded and diversified east, both north and south of the Amazon, coincident with the formation of new rivers. This evolutionary history is most consistent with a Young Amazon Flooded Forest Taxa model, suggesting Saimiri has always maintained a lowland wetlands niche and was able to greatly expand its range with the transition from a lacustrine to a riverine system in Amazonia. Saimiri vanzolinii was recovered as the sister group to one clade of Saimiri ustus, discordant with the traditional Gothic vs. Roman morphological division of squirrel monkeys. We also found paraphyly within each of the currently recognized species: S. sciureus, S. ustus, and S. macrodon. We discuss evidence for taxonomic revision within the genus Saimiri, and the need for future work using nuclear markers.

Morphology and mitochondrial phylogenetics reveal that the Amazon River separates two eastern squirrel monkey species: Saimiri sciureus and S. collinsi.

Saimiri has a complicated taxonomic history, and there is continuing disagreement about the number of valid taxa. Despite these controversies, one point of consensus among morphologists has been that the eastern Amazonian populations of squirrel monkeys form a single terminal taxon, Saimiri sciureus sciureus (Linnaeus, 1758). This group is distributed to both the north and south of the middle to lower Amazon River and in the Marajó Archipelago. However, a recent molecular study by Lavergne and colleagues suggested that the Saimiri sciureus complex (comprised of S. s. sciureus sensu lato, S. s. albigena, S. s. macrodon, and S. s. cassiquiarensis) was paraphyletic. The discordance between morphological and molecular studies prompted us to conduct a new multidisciplinary analysis, employing a combination of morphological, morphometric, and molecular markers. Our results suggest the currently recognized taxon S. s. sciureus contains two distinct species, recognized by the Phylogenetic Species Concept: Saimiri sciureus (Linnaeus, 1758) and Saimiri collinsi Osgood, 1916. East Amazonian squirrel monkeys north of the Amazon have a gray crown (S. sciureus), and south of the Amazon, the crown is yellow (S. collinsi). Morphometric measurements also clearly distinguish between the two species, with the most important contributing factors including width across upper canines for both sexes. For males, the mean zygomatic breadth was significantly wider in S. sciureus compared to S. collinsi, and for females, the width across the upper molars was wider in S. sciureus compared to S. collinsi. Mitochondrial phylogenetic analyses support this separation of the eastern Amazonian squirrel monkeys into two distinct taxa, recovering one clade (S. sciureus) distributed to the north of the Amazon River, from the Negro River and Branco River to the Guiana coast and the Brazilian state of Amapá, and another clade (S. collinsi) south of the Amazon River, from the region of the Tapajós River to the state of Maranhão, as well as within the Marajó Archipelago. The revalidation of the species S. collinsi was corroborated by all of the methods in the study, as the clades recovered in our molecular study are congruent with the pattern of morphological variation. We confirm both the paraphyly of the Saimiri sciureus complex and the paraphyly of the subspecies S. s. sciureus as defined in the current literature.

Pleistocene diversification of living squirrel monkeys (Saimiri spp.) inferred from complete mitochondrial genome sequences.

In order to enhance our understanding of the evolutionary history of squirrel monkeys (Saimiri spp.), we newly sequenced and analyzed data from seven complete mitochondrial genomes representing six squirrel monkey taxa. While previous studies have lent insights into the taxonomy and phylogeny of the genus, phylogenetic relationships and divergence date estimates among major squirrel monkey clades remain unclear. Using maximum likelihood and Bayesian procedures, we inferred a highly resolved phylogenetic tree with strong support for a sister relationship between Saimiri boliviensis and all other Saimiri, for monophyly of Saimiri oerstedii and Saimiri sciureus sciureus, and for Saimiri sciureus macrodon as the sister lineage to the S. oerstedii/S. s. sciureus clade. We inferred that crown lineages for extant squirrel monkeys diverged around 1.5 million years ago (MYA) in the Pleistocene Epoch, with other major clades diverging between 0.9 and 1.1 MYA. Our results suggest a relatively recent timeline of squirrel monkey evolution and challenge previous conceptions about the diversification of the genus and its expansion into Central America.

Genetic analysis of the Saimiri breeding colony of the Pasteur Institute (French Guiana): development of a molecular typing method using a combination of nuclear and mitochondrial DNA markers.

Saimiri (Cebidae) groups a complex of species and subspecies, which present a large morphological plasticity. Genetic analysis is complicated by the absence of consensus on classification criteria and the paucity of molecular tools available for the genus. As the squirrel monkey is widely used in biomedical research, breeding centers have been established, but the genetic make up and diversity of many of the existing colonies is unknown precluding a rationale breeding policy. To develop a genetic typing strategy for the Saimiri breeding colony of Pasteur Institute of French Guiana, we have used Cytochrome b, a mitochondrial marker, and nuclear microsatellites. Cytochrome b sequences from wild-caught Saimiri boliviensis, Saimiri sciureus sciureus and S. s. collinsi reference specimens and captive animals identified 11 haplotypes, grouped into three distinct clades. An estimate of genetic variability within each captive morphotype, and of the extent of molecular divergence between the Bolivian, Guyanese and Brazilian breeds was obtained from the analysis of three nuclear microsatellites. Taxon-specific microsatellites enabled typing of F0-F3 animals, but did not differentiate Brazilian from Guyanese animals. Three locus microsatellite analysis of a representative sample from each generation showed no trend for loss of heterozygosity, and identified hybrid animals between Bolivian and the two others sub-species. These data provide novel evidence for taxonomic classification and a rationale strategy to further type the whole colony.

Telomere biology and cellular aging in nonhuman primate cells.

To determine how cellular aging is conserved among primates, we analyzed the replicative potential and telomere shortening in skin fibroblasts of anthropoids and prosimians. The average telomere length of the New World primates Ateles geoffroyi (spider monkey) and Saimiri sciureus (squirrel monkey) and the Old World primates Macaca mulatta (rhesus monkey), Pongo pygmaeus (orangutan), and Pan paniscus (pigmy chimpanzee) ranged from 4 to 16 kb. We found that telomere shortening limits the replicative capacity of anthropoid fibroblasts and that the expression of human telomerase produced telomere elongation and the extension of their in vitro life span. In contrast the prosimian Lemur catta (ring-tailed lemur) had both long and short telomeres and telomere shortening did not provide an absolute barrier to immortalization. Following a transient growth arrest a subset of cells showing a reduced number of chromosomes overgrew the cultures without activation of telomerase. Here we show that the presence of continuous TTAGGG repeats at telomeres and rigorous control of replicative aging by telomere shortening appear to be conserved among anthropoid primates but is less effective in prosimian lemurs.

The origin of four squirrel monkey cell lines established by karyotype analysis.

The squirrel monkey is a neotropical primate genus which is widely used in biomedical research but includes individual species and subspecies that respond differently to experimental perturbations. GTG-banding patterns of chromosomes 15 and 16, which are distinct among different squirrel monkey species and subspecies, were used to determine the origin of three lung fibroblast cell lines from squirrel monkeys of unknown genetic background (DPSO 114/74, SqMkLu/68, and 7603830) and to confirm the origin of a lymphoblast cell line (GSML) recently established from Guyanese squirrel monkey. DPSO 114/74 cells are from Peruvian squirrel monkey, SqMkLu/68 cells are Bolivian squirrel monkey, and 7603830 cells are from a Peruvian/Bolivian hybrid. Chromosome analysis of GSML cells confirmed that they are from Guyanese squirrel monkey.

The Central American squirrel monkey (Saimiri oerstedii): introduced hybrid or endemic species?

Although squirrel monkeys (Saimiri spp., Primates: Cebidae) are abundant and widespread in South America, the disjunct Central American species, Saimiri oerstedii, has been restricted to the Pacific wet lowlands of Costa Rica and Panama since the earliest historical records. This taxon is now endangered in Costa Rica and nearly extinct in Panama because of habitat loss, development, and the pet trade. Conservation efforts have been hampered because of the influential, but untested, speculation that S. oerstedii represents a hybrid species introduced by prehispanic Amerind traders from multiple localities in South America. Using nuclear and mitochondrial DNA sequence data to reconstruct the phylogenetic relationships among Saimiri from Central and South America, we reexamine the taxonomic status of squirrel monkeys from different geographic regions. The sequence data support P. Hershkovitz's (1984, Am. J. Primatol. 6: 257-281) taxonomy advocating four distinct species. Combining this information with evidence from the fossil record to date the divergence times among sister taxa, we test and reject the hypothesis that Central American squirrel monkeys are the result of human introduction.

Phylogeny of neotropical monkeys: the interplay of morphological, molecular, and parasitological data.

Separate independent hypotheses of the phylogenetic relationships among the Platyrrhini monkeys have been produced in a recent past, either based upon morphological or molecular data, but the results are generally conflicting and the phylogeny of the group still is debated. The high host specificity observed among primates and their oxyurid parasites allows to consider the result of a morphologically based cladistic analysis of the pinworms of the Platyrrhini as an estimate of the phylogeny of these monkeys. Using the matrix representation method this "parasite-tree" is combined, using parsimony analysis, with several conflicting molecular or morphological hypothesis of the phylogeny of the host group. The results are discussed with respect to previously published classification, or composite computations of the phylogeny, of the Neotropical monkeys. Comparison of different hypothesis makes apparent several stable groups: (i) the Callithrichidae + Saimiri, (ii) the Atelidae/Alouattidae, (iii) the Pitheciidae, and (iv) the Alouattidae/Atelidae + Pitheciidae. In addition, the parasite and the molecular trees support close relationships between Callimico and Callithrix/Cebuella. The study also makes apparent that the parasite tree generally portrays the results of other studies, both when they are congruous and when they are conflicting. This is interpreted to be additional evidence for close coevolution between the Platyrrhini and their specific pinworms. Because, whatever the combination of data being considered no consensus can be found on the exact position of Aotus and Callicebus, and because it is likely that the earliest radiation of the Platyrrhini could be comparable to an evolutionary burst, which renders identification of homologous characters difficult, it is suggested that, possibly, not enough discriminating tracks of the evolutionary paths have been conserved to allow to resolve this uncertainty in the future.

The anterior dentition of adapids and anthropoid origins.

A recent discussion of the anterior teeth of adapids led to the conclusion that similarities to anthropoids are convergent. It is shown here that alternative functional and phylogenetic interpretations can be supported. These alternative interpretations are based on a different perspective on the anterior dentitions of extant and fossil anthropoids, which cannot be characterized by a single pattern of morphology and occlusion. More importantly, when this interspecific variation is placed within a phylogenetic framework it reveals persistent evolutionary trends that can be extrapolated back to infer a modest range of probable conditions in an Eocene anthropoid ancestor. The morphology and occlusion of adapid anterior teeth fall within this extrapolated range. This is compatible with an adapid ancestry for anthropoids.

Morphological and behavioral adaptations for foraging in generalist primates: the case of the cebines.

In addition to being frugivorous, Cebus and Saimiri stand out among the New World primates of similar body size in being heavily dependent on animal matter for protein (faunivory). A detailed description of the morphology and behavior of the two genera is presented with the object of evaluating the interaction and respective contributions of morphological and behavioral adaptations to foraging patterns. Our conclusions include the following: First, body size is extremely important in explaining the observed variation in diet. Second, the emphasis on faunivory is facilitated more by behavioral than by morphological specialization. Third, whatever morphological specializations are present, particularly in Cebus, are probably favored by diet at the most food-depauperate time of year. Fourth, although morphology may well reveal what a primate may potentially eat, to map this potential onto actual diet requires a detailed knowledge of its natural ecosystem. Finally, we consider whether the behavioral data support the tenuous morphological evidence for grouping Cebus and Saimiri within the clade Cebinae.

Laventiana annectens, new genus and species: fossil evidence for the origins of callitrichine New World monkeys.

A previously unidentified middle Miocene primate from the La Venta deposits of Colombia is intermediate between squirrel monkeys (Saimiri) and callitrichines (marmosets and tamarins) in the morphology of the lower molars, mandible, and talus. Laventiana annectens is closely related to Saimiri and to Cebus (capuchin monkeys) yet resembles the probable callitrichine morphotype, demonstrating that archaic relatives of a Saimiri-like stock were suitable structural ancestors for the enigmatic callitrichines. Laventiana is also more primitive than Saimiri (= Neosaimiri) fieldsi from the same fauna, further increasing the likelihood that the latter is a lineal ancestor of modern squirrel monkeys.

Interrelationships among primate higher taxa.

One of the most controversial issues in primate palaeontology concerns the phylogenetic position of the extinct primate infraorder Adapiformes. During the Eocene, this group of primates of modern aspect possessed a holarctic distribution, and may have been present in the poorly known Palaeogene of Africa. Mainly on the basis of craniodental morphology, at least four hypotheses have been proposed concerning the phylogenetic interrelationships among adapiforms and other primate higher taxa: (1) that adapiforms are ancestral to both lemuriforms (including Lorisoidea) and anthropoids; (2) that adapiforms cannot be shown to possess a special phylogenetic relationship with either lemuriforms or anthropoids; (3) that adapiforms are the sister taxon of lemuriforms; and (4) that Adapiformes is not a natural, monophyletic group, but rather consists of nested clades within the radiation of lemuriforms. Here, we describe features of the ankle and wrist joints of several adapiform taxa that provide an independent test of the preceding hypotheses. These traits suggest that lemuriforms are monophyletic with respect to known adapiforms, but that adapiforms nevertheless are their stem lineage (sensu Ax).

Possible errors in identification of squirrel monkeys (Saimiri sciureus) from different South American points of export.

We conducted karyological studies on one colony consisting of 12 Colombian and 34 Bolivian squirrel monkeys and a second colony of 47 monkeys imported into the United States between 1968 and 1974 through six importers. All animals in the first colony showed six acrocentric pairs of chromosomes. Bolivian monkeys were phenotypically distinguishable by their large size and coloration. In the second colony, 19 Peruvian, seven Colombian, five Bolivian and six Guyanan monkeys were correctly identified phenotypically and had five, six, six, and seven acrocentric pairs of chromosomes, respectively. Among Peruvian monkeys, 34.5% of the phenotypic classifications were in error.

The management of a squirrel monkey (Saimiri sciureus) unit.

Biological, particularly reproductive data for the squirrel monkey were reviewed. Information was also given on the care, diet, maintenance, health status, and handling of the species. The value of squirrel monkey in research was discussed. It was concluded that a controlled monkey unit produces a more homogeneous population than one would find in a natural environment and does not deplete the natural populations.