Tractography of the Spider Monkey (Ateles geoffroyi) Corpus Callosum Using Diffusion Tensor Magnetic Resonance Imaging

The objective of this research was to describe the organization, connectivity and microstructure of the corpus callosum of the spider monkey (Ateles geoffroyi). Non-invasive magnetic resonance imaging and diffusion-tensor imaging were obtained from three subjects using a 3T Philips scanner. We hypothesized that the arrangement of fibers in spider monkeys would be similar to that observed in other non-human primates. A repeated measure (n = 3) of fractional anisotropy values was obtained of each subject and for each callosal subdivision. Measurements of the diffusion properties of corpus callosum fibers exhibited a similar pattern to those reported in the literature for humans and chimpanzees. No statistical difference was reached when comparing this parameter between the different CC regions (p = 0.066). The highest fractional anisotropy values corresponded to regions projecting from the corpus callosum to the posterior cortical association areas, premotor and supplementary motor cortices. The lowest fractional anisotropy corresponded to projections to motor and sensory cortical areas. Analyses indicated that approximately 57% of the fibers projects to the frontal cortex and 43% to the post-central cortex. While this study had a small sample size, the results provided important information concerning the organization of the corpus callosum in spider monkeys.     

Food Preferences and Nutrient Composition in Captive Spider Monkeys,Ateles geoffroyi

We assessed the occurrence of food preferences in captive spider monkeys and analyzed whether their preferences correlate with nutrient composition. Using a two-alternative choice test, we repeatedly presented 7 Ateles geoffroyi with all possible binary combinations of 12 types of food that are part of their diet in captivity. They exhibited the following rank order of preference: avocado > sapodilla > pineapple > mango > papaya > melon > banana > apple > tomato > orange > carrot > cucumber. Correlational analyses revealed that this preference ranking is significantly positively correlated with total energy content, irrespective of the source of energy as neither total carbohydrate content nor protein or lipid content is significantly correlated with food preference. Further, food preferences are significantly negatively correlated with water content and positively correlated with the content of magnesium, copper and manganese. These results suggest that despite their high degree of frugivory and high taste sensitivity for soluble carbohydrates, spider monkeys are opportunistic feeders with regard to maximizing net gain of energy.     

Massive Destruction of Symphonia globulifera (Clusiaceae) Flowers by Central American Spider Monkeys (Ateles geoffroyi)1

Although more than 39 primate species have been described as nectar feeders, no studies have documented the negative affect this behavior may have on the reproductive success of the plants they consume. Here we report, for the first time, massive flower destruction of the tropical tree Symphonia globulifera by the frugivorous spider monkey, Ateles geoffroyi, and document the detrimental effect this behavior has on fruit set. Foraging behavior was collected from one troop of A. geoffroyi during 460 contact hours from June 1999 to May 2000 in the tropical humid forest at the Refugio de Vida Silvestre Punta Rio Claro (8°39′N, 83°44′E) in the Osa Peninsula in Southwestern Costa Rica. Detailed phenological data were collected from ten S. globulifera trees that the monkeys fed upon and ten trees that were outside of their home range, but in the Refugio. From July to September 1999 S. globulifera was the most important species consumed, representing from 86 to 100 percent of the total feeding time each month. Monkey foraging on S. globulifera flowers was destructive, detaching the flowers completely from the branches in 80 percent of the foraging bouts, and leaving flowers without petals and with damaged reproductive parts in 20 percent of the bouts. None of the ten trees where the monkeys were foraging set fruit, but seven of ten trees outside of their home range set fruit in November and December 1999. These results suggest that some primates may play an important role in floral herbivory in tropical forests and the subsequent reduction in reproductive success. Future studies should focus on evaluating the long‐term effect this foraging behavior may have on the population structure of this species and evaluate the effect of primate floral herbivory on the reproductive success of other plant species.     

Copulation in free-ranging black-handed spider monkeys (Ateles geoffroyi)

I report ad libitum data on 18 copulations involving free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama. All copulations were performed in a dorsoventral position, as is typically reported for this genus. Intromission often appeared difficult to achieve, possibly as a result of the large size of the glans penis in these animals. The average length from intromission to termination of thrusting exceeded 17 min, followed by an average period of almost 2 min before separation occurred, which suggests the possibility of a copulatory lock. Offspring of the female participant were almost always in close proximity to or in contact with the pair, and harassment by the offspring was observed only during the final stages of the copulation. All but one copulatory event occurred in complete seclusion from other adult males, and sexual behavior was not limited to any one adult male in the group.     

Phylogenetic Relationships of Spider Monkeys (Ateles) Based on Mitochondrial DNA Variation

Our goal was to determine phylogenetic relationships among geographically and taxonomically distinct haplotypes of spider monkeys (Ateles) based on DNA sequence variation for the mitochondrial DNA control region and cytochrome c oxidase subunit II gene. We obtained samples from most previously recognized subspecies of Ateles, ranging from Central America throughout the Amazon Basin, to determine phylogenetic relationships among racially recognized groups. Comparison of DNA sequences using both parsimony analysis and genetic distance analysis produced phylogenetic relationships that were very similar for each genetic region. We analyzed the phylograms produced, along with associated bootstrap support, confidence probabilities, and genetic distances between taxonomic groups, to identify four monophyletic species of Ateles: Ateles paniscus, composed of haplotypes from the northeastern Amazon Basin; A. belzebuth in the southern Amazon Basin; A. hybridus, located primarily along the Magdalena River valley of Colombia; and A. geoffroyi, which includes two former species: A. geoffroyi and A. fusciceps. This arrangement is contradictory to long-held taxonomies of Ateles based on pelage variation and is similar to a recent analysis based on craniodental variation. Results of this investigation suggest patterns of gene flow, evolutionary relationships, and speciation patterns that are more plausible than previous pelage-based taxonomies, which required seemingly impossible patterns of gene flow. Conservation efforts aimed at protecting Ateles, one of the Neotropics most endangered genera, will also benefit from the findings presented in this paper.     

Housing with Females Increases Testosterone and Cortisol Levels in Captive Groups of Black-Handed Spider Monkeys (Ateles geoffroyi)

The black‐handed spider monkey (Ateles geoffroyi) is a seasonal reproducer that requires a seclusiveness to copulate and has a fusion–fission social system. These features impose important restrictions to achieve reproduction of captive animals. We investigated if group composition in captive spider monkeys has any endocrine effects. We compared testosterone and cortisol concentrations during the mating season in all‐male and multifemale–multimale groups to study if the former condition impairs reproductive potential and increases stress. Concentrations of testosterone and cortisol of males living with females were higher than those of all‐male groups. In the multifemale–multimale condition, dominant males had the highest levels of testosterone, while the youngest males showed the highest concentrations of cortisol. Results show that males adjust well to isosexual grouping, this being an appropriate condition to keep animals when controlled reproduction is sought. Zoo Biol 31:490;–497, 2012. © 2012 Wiley Periodicals, Inc.     

Artificial insemination in black-handed spider monkey (Ateles geoffroyi)

Artificial insemination (AI) was performed in spider monkeys; these primates are vulnerable to extinction and usually do not reproduce spontaneously in captivity. Uterine cycles were followed by daily assessment of vaginal cytology, and corroborated a posteriori by concentrations of 17-beta estradiol and progesterone, measured by radioimmunoassay (RIA), in fecal samples collected once daily. Five females between 13 to 27 years old were inseminated intravaginally (with fresh semen) twice each during the periovulatory phase (Days 9-12 of the menstrual cycle; Day 0, first day of menstrual bleeding), from September to the first 3 weeks of November (most fertile months). Transcervical AI was not useful in this primate because the liquid portion of the semen completely solidified instead of liquefying as in other primates. Pregnancies were apparently achieved in 5 of 14 attempts. One female became pregnant after the first round of inseminations, delivered a healthy infant, was inseminated and got pregnant again (subsequently aborted). One female aborted, apparently due to an intramural uterine leiomyoma. Another two females stopped menstruating for a few months, then restarted menstruating (these females may have been pregnant and aborted). In conclusion, in spider monkeys: (1) captivity-induced stress did not inhibit reproduction; (2) fecal steroid hormones were useful to assess cyclicity; (3) the semen coagulum, which apparently is a tightly packed and large reservoir of spermatozoa, must not be discarded but used in AI; (4) old female spider monkeys did not have cessation of reproductive function.     

Assessing the Occurrence of Sexual Segregation in Spider Monkeys (Ateles geoffroyi yucatanensis), Its Mechanisms and Function

Sexual segregation is a recognized dimension of the socioecology of many vertebrates, but it has not been systematically examined in primates. We investigated temporal patterns of sexual segregation in spider monkeys (Ateles geoffroyi yucatanensis) using a test that distinguishes sexual segregation from aggregation and random association between the sexes. We further investigated how sexual segregation varies over time as a function of food availability, and then tested other possible factors that might be causally linked to sexual segregation in spider monkeys. We predicted that male philopatry and cooperative territorial defence leads to sexual dimorphism in behavior, which in turn creates different optimal energetic requirements for males and females as reflected in differing activity budgets and diet. We investigated sexual segregation in a group of 33–35 spider monkeys at Runaway Creek Nature Reserve in Belize over 23 mo in 2008–2009. We used the sex compositions of subgroups recorded in scan samples to test the occurrence of sexual segregation at monthly and biweekly time scales.We found that males and females were significantly segregated in 15 out of the 23 mo of the study, and that periods of nonsegregation coincided with months of low food availability. The sexes differed significantly in activity and diet; males spent more time traveling, and less time resting and feeding than females, and they had a higher proportion of ripe fruits in their diets than did females. We propose that sexual segregation in spider monkeys is primarily a form of social segregation that results from males and females pursuing optimal dietary and behavioral strategies to satisfy sex-specific energetic demands. We further suggest that sexual segregation represents an important constraint on fission–fusion dynamics that should be considered when assessing the potential for variability in subgroup composition.     

Spider Monkeys (Ateles geoffroyi) Habituate to Anthropogenic Pressure in a Low-Impact Tourism Area: Insights from a Multi-Method Approach

International Journal of Primatology - Shared habitats between humans and other animals are increasing in the twenty-first century, which may require behavioral flexibility from animal species to...     

The menstrual cycle of the spider monkey (Ateles geoffroyi)

The ovarian cycles of four adult female spider monkeys (Ateles geoffroyi) were followed daily throughout 30 days by means of vaginal swabs and blood samplings. Cytological analyses of the vaginal swabs and radioimmunoassay determination of the daily levels of estradiol-17β (E₂) and progesterone (P₄) were done in order to classify the kind of ovarian cycle of this species. Our results show that Ateles geoffroyi females display menstrual cycles of about 24 days on average. By comparison with the well-known menstrual cycles of women, apes, and Old World monkeys, the four distinctive cytological phases (bleeding, follicular, periovulatory, and luteal) could be recognized; mid-cycle E₂ peaks followed by mid-luteal increases of the same hormone were present in all four females. P₄ levels were higher after the E₂ peak, although both hormones were present throughout the cycles. Also, age-dependent features, hormone profiles, and changes in menstrual phases lengths were detected. Am. J. Primatol. 44:183–195, 1998. © 1998 Wiley-Liss, Inc.     

Genetic Variation in Remnant Populations of the Woolly Spider Monkey (Brachyteles arachnoides)

The muriqui or woolly spider monkey (Brachyteles arachnoids) is an endangered primate endemic to the Atlantic Forest of Brazil, <5% of which remains. The known muriqui population consists of <700 individuals separated into approximately 15 geographically isolated forest fragments. I present data on the distribution of genetic variation within and between two such remnant populations (FE and FBR) and summarize the implications of these results for long-range management of species genetic diversity. Eleven of 32 allozyme loci were polymorphic, representing an overall level of polymorphism of 34.4% and a mean heterozygosity per locus of 11%. Both values are among the highest reported for New World monkeys. Genetic differentiation between the two localities is highly significant (F_ST = 0.413, p < 0.001). Genetic distance between them is an order of magnitude greater than that between other populations of platyrrhine subspecies, but this could be an artifact of the small sample size from FBR. High levels of genetic diversity apparently characteristic of this species persist because (1) fragmentation and size reduction of muriqui populations has occurred very rapidly relative to the muriqui life span—although both polymorphism and heterozygosity were lost between generations in the largest population, the high genetic diversity present in the parent population was still in evidence; and (2) genetic diversity before population fragmentation by human activity was not distributed uniformly throughout the species' historic distribution. Thus, remnant muriqui populations are important genetic reservoirs of alleles that are unique or rare in the species gene pool as a whole. These results emphasize the need for the integration of conservation management efforts throughout the species range.     

Chromosome polymorphism in Ateles geoffroyi (Cebidae; Primates; Mammalia)

Summary The karyotype of Ateles geoffroyi (Cebidae; Primates; Mammalia) was studied using G- and C-banding techniques, and standardized idiograms are proposed. A polymorphism of chromosome 3 due to a pericentric inversion has been identified for the first time. Genetic analysis of this polymorphism showed Mendelian inheritance.     

Aging-related reproductive decline in the male spider monkey (Ateles geoffroyi)

Background It is unknown whether male black‐handed spider monkeys (Ateles geoffroyi) undergo a reproductive decline as they age. The purpose of this work was investigating whether serum testosterone and semen quality decrease with age in these primates as occur in other species. Methods In this study, we assessed age variations in the concentration of serum testosterone, sperm counts, and motility in nine males. We took serum blood samples and semen samples by electroejaculation of anesthetized males throughout the fertile season. Results We found that testosterone levels and total sperm concentration, motile, progressive, fast linearly moving, medium linearly moving, slow linearly moving and immotile sperm significantly decreased with age. Conclusions Our results show that a reproductive decline occurs in male spider monkeys because of a decrease in sperm counts. These results are similar to those of rhesus monkeys and men, despite the phylogenetic distance between New and Old World primates.