Helder L. Queiroz

Diversity, Geographic Distribution and Conservation of Squirrel Monkeys, Saimiri (Primates, Cebidae), in the Floodplain Forests of Central Amazon

Eleven taxa of primates are found in the floodplains of the western portion of the central Brazilian Amazon, protected in part by the Mamirauá Sustainable Development Reserve. The taxonomy of the squirrel monkeys, the number of taxa, and their geographic distributions are still poorly understood. Here we investigate differentiation among the taxa of this genus in Mamirauá, examining their morphology and geographic distribution. We registered 333 points of occurrence of squirrel monkeys and examined 117 specimens deposited in scientific collections. The results of the morphological analyses were generally in good agreement with field observations. Together they indicate the existence of three taxa: Saimiri vanzolinii, Saimiri sciureus macrodon, and S. s. cassiquiarensis. The restricted range of Saimiri vanzolinii in the southeastern portion of the reserve covers an area of 870 km2, and it is among the smallest of the distribution areas for any Neotropical primate species. Saimiri sciureus cassiquiarensis has a disjunct distribution, crossing the Japurá River to the right bank into the reserve in two places, and S. s. macrodon is the squirrel monkey ranging widely in the northwest of Mamirauá. There are three areas of parapatry: one between Saimiri vanzolinii and Saimiri sciureus macrodon and two between S. vanzolinii and S. s. cassiquiarensis. We recommend that anthropogenic changes in the region be monitored, and conservation measures be taken to protect these primates, especially considering the endemism and very restricted range of Saimiri vanzolinii and its consequent vulnerability to extinction.

New records and range expansion of the white bald uakari (Cacajao calvus calvus, I. Geoffroy, 1847) in Central Brazilian Amazonia

The white bald uakari (Cacajao calvus calvus) is among the least studied of the Amazonian primates and is found exclusively in remote areas of the central Amazon. The geographic distribution of this subspecies is still uncertain, and information on current threats and its conservation status is sparse. In this paper, we identify new locations of occurrence and propose range expansion of the Cacajao calvus calvus. Between 2008 and 2010, six field expeditions were undertaken in the middle Solimões region to search for the subspecies and to conduct interviews with local residents regarding its presence. The presence of the white bald uakari was confirmed in the lower courses of the Juruá and lower Jutaí rivers, in addition to areas inside the Mamirauá Reserve, where its presence was expected. Results indicate an expansion and new limits on the geographic range of the subspecies, including its detection in areas in which it had not previously been reported and its exclusion from areas where white bald uakaris were assumed to occur. The new information provided by this study and the remaining shortcomings regarding the distribution of the calvus group point to the urgent need for further research on the geographic distribution and habitat use of this group, especially along the lower courses of the Juruá and Jutaí rivers, which remain little explored.

Does Resource Availability Affect the Diet and Behavior of the Vulnerable Squirrel Monkey, Saimiri vanzolinii?

Seasonal changes in food availability influence the behavior and diet of primates, and an understanding of dietary changes is important for the development of informed conservation plans. Saimiri vanzolinii is a small-bodied, omnivorous squirrel monkey endemic to the floodplain forests in Central Amazonia. It has a restricted distribution of only ca. 870 km2 and is classified as Vulnerable. We examined seasonal variation in this species’ diet. We collected phenological (presence and absence of ripe fruits from 205 tree species) and dietary and behavioral data for unhabituated groups of S. vanzolinii on nine 2-km transects in the floodplain forests of Central Amazonia for 2 years, encompassing the high-water and low-water periods. Fruit availability was higher, and the monkeys traveled less and fed more during the high-water than the low-water period. There were no seasonal differences between the high-water and low-water periods in the time spent feeding on fruits, flowers, or arthropods. S. vanzolinii spent more time consuming fruit than arthropods in the high-water period, but this was not the case in the low-water period. These findings suggest that food selection changed between seasons, and S. vanzolinii focused more on fruit in the low-water period, when fruit was less available, than in the high-water period, when fruit was more available. These results support the predictions of the ecological constraints model.

Seminal coagulation and sperm quality in different social contexts in captive tufted capuchin monkeys (Sapajus apella)

In the present study, we aimed to assess the influence of different social contexts on the seminal coagulation and sperm quality in captive tufted capuchin monkeys. For this, males were housed either individually, in mixed‐sex groups (with females), or in male‐only groups. Monkeys were housed in cages and each cage type (i.e., individual or group cage) was placed in a different room. Forty‐one males were subjected to semen collection by rectal electroejaculation. The degree of seminal coagulation was determined on a scale of I–IV. Seminal volume, sperm concentration, sperm motility, vigor, and plasma membrane integrity were evaluated for all ejaculate samples. All ejaculates collected showed degrees of coagulation between II and IV, where the majority presented coagulation degree IV, when collected from animals housed in groups. No statistical differences among percentages of coagula degree when samples were collected from males housed individually. Animals housed in group cages (male‐only groups and mixed‐sex groups) showed a significantly higher percentage of ejaculates at degree IV than males housed individually. Seminal volume was not affected by the coagula degree but by the housing system, where animals housed individually showed the highest volume (543 μl) when compared with those animals from male (273 μl) and mixed‐sex (318 μl) groups. No differences were observed in semen volume when comparing male‐only groups with mixed‐sex groups. Sperm motility was affected by both housing system and coagula degree. Samples with coagula degree IV from animals housed individually showed the highest (72%) sperm motility percentages. Sperm plasma membrane integrity was lower when samples were presenting coagula degree II + III and collected from male‐ (17%) or mixed‐sex (23%) groups. However, this housing system effect was not observed when sperm was obtained from coagula degree IV semen. Sperm vigor was neither affect by housing system or coagula degree.

Tree community structure reflects niche segregation of three parapatric squirrel monkey species (Saimiri spp.)

Integration between ecology and biogeography provides insights into how niche specialization affects the geographical distribution of species. Given that rivers are not effective barriers to dispersal in three parapatric species of squirrel monkeys (Saimiri vanzolinii, S. cassiquiarensis and S. macrodon) inhabiting floodplain forests of Central Amazonia, we tested whether forest structure and tree diversity may explain species differences in niche specialization and spatial segregation. We sampled 6617 trees of 326 species in three habitats (high várzea, low várzea and chavascal) used by three Saimiri species, and estimated tree species richness in each of them. For each tree, we measured variables known to influence habitat use in primates, such as crown area and presence of lianas, epiphytes and hemi-epiphytes. We used ANOVA to compare these variables and performed multivariate analyses (NMDS, ANOSIM and SIMPER) to evaluate dissimilarities in forest structure among each habitat inhabited by the three Saimiri species. We identified differences in the tree species richness, crown area and presence of lianas, epiphytes and hemi-epiphytes between the three habitats for all Saimiri species. NMDS demonstrated that areas of high and low várzeas occupied by S. vanzolinii were clearly separated from the other species. We also found that different plant species contributed to dissimilarity among Saimiri ranges. Our findings support the hypothesis that tree community structure may promote niche specialization and spatial segregation among primates. We discuss how these patterns could have been favored by historical changes in forest flood patterns, the evolutionary history of Saimiri spp., and past competition.

The tree species pool of Amazonian wetland forests: Which species can assemble in periodically waterlogged habitats?

We determined the filtered tree species pool of Amazonian wetland forests, based on confirmed occurrence records, to better understand how tree diversity in wetland environments compares to tree diversity in the entire Amazon region. The tree species pool was determined using data from two main sources: 1) a compilation of published tree species lists plus one unpublished list of our own, derived from tree plot inventories and floristic surveys; 2) queries on botanical collections that include Amazonian flora, curated by herbaria and available through the SpeciesLink digital biodiversity database. We applied taxonomic name resolution and determined sample-based species accumulation curves for both datasets, to estimate sampling effort and predict the expected species richness using Chao’s analytical estimators. We report a total of 3 615 valid tree species occurring in Amazonian wetland forests. After surveying almost 70 years of research efforts to inventory the diversity of Amazonian wetland trees, we found that 74% these records were registered in published species lists (2 688 tree species). Tree species richness estimates predicted from either single dataset underestimated the total pooled species richness recorded as occurring in Amazonian wetlands, with only 41% of the species shared by both datasets. The filtered tree species pool of Amazonian wetland forests comprises 53% of the 6 727 tree species taxonomically confirmed for the Amazonian tree flora to date. This large proportion is likely to be the result of significant species interchange among forest habitats within the Amazon region, as well as in situ speciation processes due to strong ecological filtering. The provided tree species pool raises the number of tree species previously reported as occurring in Amazonian wetlands by a factor of 3.2.

Population estimate and morphometry of ovarian preantral follicles from three recently recognized squirrel monkey species: a comparative study

We describe morphological and morphometrical characteristics of preantral ovarian follicles from three recently recognized Saimiri species: S. macrodon, S. cassiquiarensis and S. vanzolinii; the last one a threatened species. Ovaries from four adult monkeys were evaluated: one pair from a pregnant S. macrodon, two ovarian pairs from S. cassiquiarensis females (one of them pregnant), and one left ovary from a senile S. vanzolinii, applying classical histology. Follicular preantral population was quantified and morphology and morphometry of primordial, primary and secondary follicles were evaluated. Follicular preantral population varied among species, being 347,153 in the ovaries of the S. macrodon, 270,342 and 278,376 in the ovaries of both adult non-pregnant and pregnant S. cassiquiarensis females, and 28,149 in the ovary from a senile S. vanzolinii. Most follicles were at primordial or transition stages, except for the senile S. vanzolinii female, which presented the lowest percentages of primordial and transition follicles when compared with primary and secondary ones. Most preantral follicles (>70%) were morphologically normal in the ovaries from all studied S. macrodon and S. cassiquiarensis females, but the ovary of the senile S. vanzolinii female presented a significant decrease in the percentage of normal follicles (primordial: 61%, transition: 52%, primary: 54%, and secondary: 48%). In general, follicular diameter increased significantly from primordial to transition, and subsequently from primary to secondary follicles.

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.

Unilateral ovarian absence in a Black‐headed Squirrel Monkey (Saimiri vanzolinii Ayres, 1985), a threatened neotropical primate species

Ovarian agenesis is an unusual anomaly with traumatic or congenital origin. In the present case report, we describe our findings in a senile S. vanzolinii female. As this neotropical primate species is listed as vulnerable, with limited geographic distribution in the Brazilian Amazonia, ovarian agenesis may be an important finding to be reported.