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Abundance, use of space, and activity patterns of white-faced sakis (Pithecia pithecia) in French Guiana.

White-faced sakis (Pithecia pithecia) are among the least studied neotropical primates. The combination of shy and quiet behavior, their ability to move silently, and the extreme difficulty of capturing them may explain why very few field studies have been undertaken in undisturbed habitats. During the course of a wildlife rescue in French Guiana, six individuals were captured and translocated to a safe area of primary rainforest. In this area, based on the observation of 35 groups, the average group size was 2.3 animals (SD = 1.2) and a density of 0.28 group/km(2) (0.64 individuals/km(2)) was estimated from transect censuses. Our study focused successively on three radio-collared animals (two males and one female) over a 287-day period, starting from release to the loss of the animal. From the study start, the triangulation method was used prior to habitutation to human presence, followed thereafter by 1,327 hr of visual monitoring. The translocated animals settled down, and two of them had a stable and compact home range. Two of them merged in association with members of the resident population. A resident group had a much larger home range than previously reported: 148 and 287 ha, using grid cells and 100% minimum convex polygon techniques, respectively. A group composed of two translocated individuals (one male and one female) had a home range of 68 and 135 ha using the same techniques. Additionally, two solitary animals used 152 and 162 1-ha quadrats. We observed animals (translocated and residents) moving quickly in one direction up to 11.5 km. The mean daily path length of resident animals was 1,880 m. Sakis used the lower strata of the forest more when in group, and the intermediate strata more when solitary. Allogrooming is fairly common in social groups. On average, the activity period ranged from 7:17 to 15:59 hr.

Animals↗

Geographic distribution and abundance of woolly (Lagothrix cana) and spider (Ateles chamek) monkeys in southwestern Brazilian Amazonia.

Two species of frugivorous atelids, Ateles chamek and Lagothrix cana, occur in southwestern Brazilian Amazonia. Populations were surveyed at 36 sites in the state of Rondônia. Ateles chamek is widespread, but the distribution of L. cana is limited by a combination of riverine barriers and ecological factors, possibly including competition with A. chamek. Groups of L. cana were generally larger and more abundant than those of A. chamek, even in syntopy. The transitional forest that predominates in the extreme south of Rondônia (Hylea-cerrado) is not a barrier to either species, with both species being tolerant of habitat disturbance when hunting pressure is low.

Animals↗

Sperm quality differences between the rainy and dry seasons in captive black-handed spider monkeys (Ateles geoffroyi).

The present work provides an assessment of sperm measures (concentration, motility, viability, etc.) of three black-handed spider monkeys (Ateles geoffroyi) during the rainy and dry seasons in Mexico City, as well as an evaluation of the between-subjects variability of sperm quality. Twenty samples obtained by rectal electroejaculation and digested with trypsin were evaluated. The results showed that during the dry season (n = 9) the semen samples were of better quality than those obtained during the rainy season (n = 11). The individual animals showed differences in sperm concentration, although there were no differences in sperm quality.

Animals↗

Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: A field experiment comparing Aotus, Callicebus, and Saguinus.

Early in their evolution, the ancestors of anthropoid primates radiated from a nocturnal to a diurnal niche. Foraging during the night differs from foraging during the day in terms of the availability of light and color cues, and in the movement of odor molecules through the canopy. In this study, we compared the ability of nocturnal and diurnal New World monkeys to use perceptual cues (i.e., the sight or smell of food) and spatial information (place predictability) in within-patch foraging decisions. An experimental field study was conducted on wild groups of night monkeys (Aotus nigriceps), tamarins (Saguinus imperator imperator and S. fuscicollis weddelli), and titi monkeys (Callicebus cupreus) at the Zoobotanical Park/UFAC, Rio Branco, Brazil. Our research design included the construction of feeding stations located in the home range of the study groups. Each feeding station consisted of eight visually identical feeding platforms located in a circular arrangement. In all test settings, two platforms at each feeding station contained a food reward (banana), and the remaining six platforms contained a sham reward (yellow plastic or inaccessible banana). In the night-monkey experiments, each feeding platform was illuminated by a 40-W red bulb to aid the researcher in observing their behavior. When the location of reward sites was predictable over time, individuals in all four species successfully relocated food rewards based solely on spatial information. Each species was also successful in using visual information to distinguish real from sham food rewards. However, only night monkeys and one group of emperor tamarins used olfactory information alone to locate food rewards. Overall, the species' performances did not clearly differentiate Aotus from diurnal New World primates in these experiments.

Animals↗

Quantitative data on training new world primates to urinate.

This study assessed the effectiveness of operant conditioning in training three species of captive callitrichid primates (Leontopithecus rosalia, Callithrix geoffroyi, and Saguinus imperator) to urinate on demand. There were three goals to the study: 1) to develop a system for quantitatively assessing positive reinforcement training; 2) to ascertain whether or not positive reinforcement techniques can be used to train callitrichid monkeys to urinate on demand, and if so, how many training sessions are required; and 3) to determine the effect on urination behavior of the trainer entering the cage to collect a urine sample. Positive reinforcement with a continuous reinforcement schedule was used to capture a natural behavior: urination. Training sessions (30 min each) were conducted at dawn thrice weekly during five consecutive phases: habituation, control, training (animals were rewarded for urinating), maintenance (animals had reached a defined training criteria and continued to be rewarded for urinating), and collection (animals were rewarded for urinating, and the trainer entered the cage to collect the sample). The numbers of 30-min training sessions required to train the three monkey species (L. rosalia, C. geoffroyi, and S. imperator) were five, six, and eight, respectively. For the three species, the mean number of urinations per animal was significantly greater during the training, maintenance, and collection phases compared to the control phase. However, the three species differed significantly in the manner in which the rates of urination changed across the five phases. A higher proportion of subjects urinated during the training, maintenance, and collection phases compared to the control phase. Latency to first urination varied significantly across the five phases, with significantly reduced latencies to urinate during the training, maintenance, and collection phases compared to the control phase. The entry of the trainer into the cage to collect the urine sample did not appear to alter urination behavior. We demonstrate that operant conditioning techniques, which typically incur minimal cost, time investment, and disturbance, can be used to increase the quantity of urine samples collected for physiological analysis, the proportion of animals that urinate, and the speed of sample collection.

Animals↗

Leaping behavior of Pithecia pithecia and Chiropotes satanas in eastern Venezuela.

I observed leaping behavior in the white-faced saki (Pithecia pithecia) and the black-bearded saki (Chiropotes satanas satanas) for 15 and 10 months, respectively, as part of a larger study of positional behavior in the tribe Pitheciini. I used focal animal instantaneous sampling to observe the two species on separate islands in their natural habitat at Guri Lake, Venezuela. Leaping behavior correlates with patterns of forest use and body size, and differences between the species relate more to habitat preferences than to habitat differences per se. Pithecia usually chose vertical or highly angled supports of lower tree portions for take-off and landing, and took off from a stationary posture. Chiropotes took off from the main crown or terminal branches, gaining momentum from locomotor movement before performing a leaping take-off. Pithecia's vertical body orientation and longer leap distance allowed it to assume a mid-flight tuck to prepare for a hindlimb-first landing onto a solid support, and to absorb landing forces with its relatively longer hindlimbs. Chiropotes remained more pronograde throughout its leaps, and minimized landing forces by landing on all four limbs onto numerous flexible supports in the terminal branches. The smaller-bodied P. pithecia is specialized for vertical clinging and leaping, and exhibits behavioral and morphological parallels with other vertical clingers and leapers. The larger C. satanas is a generalized leaper that lacks morphological specializations for leaping. Pithecia's use of solid supports in the lower tree portions allows it to move quietly through the forest-one of a suite of behaviors related to predator avoidance. This example of variation within one behavioral category has implications for devising locomotor classifications and interpreting fossil remains.

Animals↗

Variation in the resumption of cycling and conception by fecal androgen and estradiol levels in female Northern Muriquis (Brachyteles hypoxanthus).

We measured fecal androgen (T+DHT) and estradiol (E2) levels in female northern muriquis (Brachyteles hypoxanthus) at the Estação Biológica de Caratinga/RPPN Feliciano Miguel Abdala, Minas Gerais, Brazil, to evaluate the hormonal bases underlying individual variation in the resumption of cycling and conception. We found that androgen levels were significantly lower in females than in males, and that there were no consistent patterns in female androgen levels across precycling or cycling conditions. Females that resumed cycling earlier in the study (weeks 4-8) had higher precycling E2 levels and correspondingly lower precycling androgen/E2 ratios than females that resumed cycling later (weeks 12-16). There were no differences in female precycling androgen levels, but cycling females that conceived during or immediately after the study period had lower androgen levels and threefold higher E2 peaks than the one cycling female that failed to conceive. These results suggest that minimum E2 thresholds are necessary for both the resumption of ovarian cycling and conception. Individual variation in these components of fertility may be regulated by differences in E2 levels, which affect androgen/E2 ratios, rather than by androgen levels per se. Further research into the relative concentrations of T vs. DHT will be necessary to fully evaluate whether androgens affect cycling and conception in this species.

Animals↗

Comparative use of color vision for frugivory by sympatric species of platyrrhines.

Ateles spp. and Alouatta spp. are often sympatric, and although they are mainly frugivorous and folivorous, respectively, they consume some of the same fruit species. However, they differ in terms of color vision, which is thought to be important for fruit detection. Alouatta spp. have routine trichromatic color vision, while Ateles spp. presents the classic polymorphism of platyrrhines: heterozygous females have trichromatic color vision, and males and homozygous females have dichromatic vision. Given these perceptual differences, one might expect Alouatta spp. to consume more reddish fruits than Ateles spp., since trichromats have an advantage for detecting fruits of that hue. Furthermore, since Ateles spp. have up to six different color vision phenotypes, as do most other platyrrhines, they might be expected to include fruits with a wider variety of hues in their diet than Alouatta spp. To test these hypotheses we studied the fruit foraging behavior of sympatric Alouatta palliata and Ateles geoffroyi in Costa Rica, and modeled the detectability of fruit via the various color vision phenotypes in these primates. We found little similarity in fruit diet between these two species (Morisita = 0.086). Furthermore, despite its polymorphism, A. geoffroyi consumed more reddish fruits than A. palliata, which consumed more greenish fruits. Our modeling results suggest that most fruit species included in the diet of A. geoffroyi can be discriminated by most color vision phenotypes present in the population. These findings show that the effect of polymorphism in platyrrhines on fruit detection may not be a disadvantage for frugivory. We suggest that routine trichromacy may be advantageous for other foraging tasks, such as feeding on young leaves.

Alouatta↗

Sugar concentration of fruits and their detection via color in the Central American spider monkey (Ateles geoffroyi).

Although most arguments explaining the predominance of polymorphic color vision in platyrrhine monkeys are linked to the advantage of trichromacy over dichromacy for foraging for ripe fruits, little information exists on the relationship between nutritional reward and performance in fruit detection with different types of color vision. The principal reward of most fruits is sugar, and thus it seems logical to investigate whether fruit coloration provides a long-distance sensory cue to primates that correlates with sugar content. Here we test the hypothesis that fruit detection performance via trichromatic color vision phenotypes provides better information regarding sugar concentration than dichromatic phenotypes (i.e., is a color vision phenotype with sufficient red-green (RG) differentiation necessary to "reveal" the concentration of major sugars in fruits?). Accordingly, we studied the fruit foraging behavior of Ateles geoffroyi by measuring both the reflectance spectra and the concentrations of major sugars in the consumed fruits. We modeled detection performance with different color phenotypes. Our results provide some support for the hypothesis. The yellow-blue (YB) color signal, which is the only one available to dichromats, was not significantly related to sugar concentration. The RG color vision signal, which is present only in trichromats, was significantly correlated with sugar content, but only when the latter was defined by glucose. There was in fact a consistent negative relationship between fruit detection performance and sucrose concentration, although this was not significant for the 430 nm and 550 nm phenotypes. The regular trichromatic phenotypes (430 nm, 533 nm, and 565 nm) showed higher correlations between fruit performance and glucose concentration than the other two trichromatic phenotypes. Our study documents a trichromatic foraging advantage in terms of fruit quality, and suggests that trichromatic color vision is advantageous over dichromatic color vision for detecting sugar-rich fruits.

Animals↗

Color-vision polymorphism in wild capuchins (Cebus capucinus) and spider monkeys (Ateles geoffroyi) in Costa Rica.

New World monkeys are unique in exhibiting a color-vision polymorphism due to an allelic variation of the red-green visual pigment gene. This makes these monkeys excellent subjects for studying the adaptive evolution of the visual system from both molecular and ecological viewpoints. However, the allele frequencies of the pigments within a natural population have not been well investigated. As a first step toward understanding the relationship between vision and behavior, we conducted color-vision typing by analyzing fecal DNA from two wild groups of white-faced capuchin monkeys (Cebus capucinus) and one group of black-handed spider monkeys (Ateles geoffroyi) inhabiting Santa Rosa National Park of Costa Rica. All color-typed monkeys were individually identified. In C. capucinus and A. geoffroyi we found three and two pigment types, respectively, and the spectral mechanism that created one of the two Ateles pigments was found to be novel. In one Cebus group and the Ateles group, all alleles were present, whereas in the other Cebus group only two alleles were found, with one allele predominating. This was likely due to the effect of close inbreeding, indicating that wild populations can exhibit a variety of allele compositions. This result also suggests that the color-vision polymorphism can be easily distorted by natural factors, such as inbreeding, skewing the population structure.

Animals↗

Predation of arthropods by southern bearded sakis (Chiropotes satanas) in Eastern Brazilian Amazonia.

Bearded sakis are seed predators, but are also known to consume arthropods. This is the first detailed report of arthropod predation in southern bearded sakis (Chiropotes satanas). Two groups were monitored-one in continuous forest, and one on a small island-between January 2003 and February 2004. The arthropod prey included spiders and six insect orders. Island group members spent more time foraging for arthropods (3.8% vs. 2.6% of activity time) but ingested less prey (3.7% vs. 4.6% of feeding time). Arthropods accounted for a small proportion of feeding records in most months, but there were occasional sharp peaks due to the exploitation of temporary agglomerations of insects. In November, arthropods accounted for 26.6% and 14.2% of the feeding records of the mainland and island groups, respectively. The results suggest that bearded sakis actively seek arthropods as a dietary supplement, but that they represent a minor resource during most of the year, even under conditions of intense habitat fragmentation (island group).

Animals↗

Seasonal variations in black-faced black spider monkey (Ateles chamek) habitat use and ranging behavior in a southern Amazonian tropical forest.

Data are presented regarding the habitat use and ranging behavior of a spider monkey (Ateles chamek) community at Lago Caiman in northeastern Bolivia. Habitat use was driven primarily by fruit availability and distribution across the community home range. Strong seasonal variations occurred in fruit availability within all five of the floristically and phenologically distinct habitat types identified within the study site, and the spider monkeys dramatically shifted their ranging according to which habitat was richest in fleshy fruits. This use of local habitat diversity resulted in an unusually elongated shape for the home range that was otherwise typical of previous Ateles studies in terms of size. Ranging behavior was clumped and community core areas shifted seasonally across the focal community home range. Individual core areas were not relevant to the study due to dramatic community-wide shifts in ranging patterns. Day journey lengths were highly variable (460-5,690 m) and the distribution and abundance of fleshy fruit resources explained 81% of the monthly variations in mean day journey length. Keystone habitats for forest frugivores are identified and results are discussed with reference to previous studies on this genus, and the importance of considering keystone habitats and local habitat diversity within the management of forestry concessions in the region. Results are also discussed with reference to the behavioral ecology of the genus Ateles.

Animal Migration↗

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.

Animals↗

Scent marking in two western Amazonian populations of woolly monkeys (Lagothrix lagotricha).

We describe patterns of scent marking observed in two wild populations of lowland woolly monkeys that were the subjects of long-term studies in the westernmost portion of the Amazon basin. The woolly monkeys engaged primarily in two types of scent marking: chest rubbing and anogenital rubbing. In both study populations, males and females performed both types of scent marking, but males chest-rubbed more commonly than females, while females engaged in more anogenital rubbing. We evaluated two nonexclusive hypotheses for the function of scent marking by woolly monkeys: 1) that scent marking is used in sociosexual contexts, and 2) that scent marking is used to convey information about occupancy of or willingness to defend an area from conspecifics in other social groups. We found no association between the occurrence of scent-marking behavior and location within the home range, but did find that scent marking occurred more commonly than expected on days when copulations, mating solicitations, and intergroup encounters were observed. Additionally, mating activity and chest rubbing were highly correlated across the yearly cycle, even when the potentially confounding variable of ripe fruit availability was controlled for. In woolly monkeys, overt male-male competition is rare and female choice is an important part of the mating system. Our results are most consistent with the idea that scent marking plays a role in advertising male quality or competitive ability, and perhaps in coordinating mating activity.

Animal Communication↗

Intragroup lethal aggression in wild spider monkeys.

We report the first evidence of intragroup coalitionary aggression leading to the death of a wild young adult male spider monkey. During a long-term study of a well-habituated community at the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico, a young adult male sustained severe injuries repeatedly between January and March 2002. On 1 April 2002 the same male was the victim of an intragroup attack by at least one adult male that resulted in his death. We highlight several causes of intragroup aggression that may account for the killing.

Aggression↗

Variability of metapodials in primates with rudimentary digits: Ateles geoffroyi, Colobus guereza, and Perodicticus potto.

A tenet of evolutionary theory is that, within a species, phenotypic variability is inversely related to the intensity of stabilizing selection. A corollary is that a rudimentary or vestigial structure should be highly variable. This relationship between rudimentation and variability, however, may simply be part of a continuum, as several studies have shown that variability and size of a structure are inversely related. This study tests whether the first metacarpal (MC1) in Ateles geoffroyi and Colobus guereza and the second metacarpal (MC2) in Perodicticus potto are highly variable in their lengths relative to their other metapodials. The former two species have rudimentary thumbs, and the latter species has a rudimentary index finger. Fourteen other species of primates are included in the comparison. The results show that MC1 in A. geoffroyi and C. guereza and MC2 in P. potto are the relatively shortest first and second metapodials, respectively, in this sample of primates. However, an intraspecific analysis shows that neither MC1 in A. geoffroyi and C. guereza nor MC2 in P. potto is significantly more variable than the other metapodials. Nevertheless, an interspecific analysis shows that MC1 in A. geoffroyi and C. guereza is relatively the most variable among the first metapodials (i.e., MC1 and first metatarsal) in this study. MC2 in P. potto, however, is of relatively low variability compared with the other primates. These contrasting results are interpreted in terms of the developmental and evolutionary biology of digits.

Adaptation, Physiological↗

Tooth-root form and function in platyrrhine seed-eaters.

Research into the functional and adaptive basis of tooth crown form has provided a useful framework for the inference of diet in extinct primates. However, our understanding of variation in tooth-root form is limited. Studies within the clinical literature emphasize the influence of tooth-root surface area on stress resistance, but it is not known if root form has diversified during primate evolution in relation to dietary specialization. This hypothesis was tested by quantifying maxillary canine and postcanine tooth-root surface areas in four platyrrhine species that differ in the material properties of their diet: Cebus apella, Cebus albifrons, Chiropotes satanas, and Pithecia pithecia. Pairwise comparisons between closely related taxa support predictions based on dietary differences. Taxa that regularly consume resistant seeds (Cebus apella and Chiropotes satanas) exhibit significantly larger relative surface area values for those teeth used in seed processing than closely related taxa that consume resistant foods less often (Cebus albifrons and Pithecia pithecia). Additionally, relative molar-root surface area appears to be greater in Pithecia than in Chiropotes, as predicted from the more folivorous diet of Pithecia. Tooth-root surface area was also found to vary along the tooth row and should therefore have a significant influence on antero-posterior bite-force gradients. The results of this study suggest a close relationship between tooth-root form and patterns of occlusal loading. Further elucidation of this relationship could improve our inferences of diet in extinct taxa, and augment research into the mechanics and evolution of feeding.

Animals↗

Multivariate analysis of organismal and habitat parameters in two neotropical primate communities.

This paper investigates the interrelations of some organismal and habitat parameters in two platyrrhine primate communities in French Guiana and Ecuadorian Amazonia. Fifteen habitat and organismal parameters and body weight were retained after a preliminary analysis, on the basis of frequent use and constraints reflected in anatomical specializations. The 16 parameters for 13 platyrrhine species were used for a series of principal components analyses (PCAs). All PCAs on separate or combined communities provided comparable results. The Atelinae, Ateles, Alouatta, and Lagothrix, were clustered together with Pithecia, associated with canopy, mature forest, frugivory, and (to a lesser degree) climb/suspensory locomotion. On the other hand, the three species of Cebus usually formed a loose cluster, located in the center of the cloud of species. Lastly, the Callitrichinae, involving two species of Saguinus and Cebuella, were relatively dispersed and frequently associated with liana forest, lianas, understory, and faunivory. However, Cebuella was consistently isolated and associated with liana forest, lianas, body weight, understory, and vertical supports. In this way, clusters appeared to conform to the major platyrrhine taxonomic groups, supporting the fact that basic ecological and behavioral adaptations have evolved in a phylogenetic context. In addition, the analyses revealed that body weight, forest type and layer, feeding behavior, and locomotion are the most important variables that have apparently shaped or driven the adaptive zones of extant platyrrhines.

Alouatta↗