Health evaluation of translocated free-ranging primates in French Guiana

Among over 40 mammal species threatened by the filling of a hydroelectric dam reservoir in French Guiana, three species of primates have been translocated, comprising 124 red howler monkeys, six white-faced sakis, and 95 golden-handed tamarins. Health status of the animals was evaluated by direct physical examination and by hematological, biochemical, virological, and parasitological surveys of collected blood. The physical condition of the howlers was slightly worse toward the end of the capture period, but that of sakis and tamarins remained satisfactory. Several ectoparasites (ticks, larvae of dipterous insects, fleas, and lice) were collected, and various wounds, apparently nondebilitating, were recorded in howlers. Hematological and biochemical profiles determined for the three species revealed a slight anemia in howlers. Entamoeba, Strongyloides, and Trypanoxyurus were common in fecal samples of howlers. A survey of blood smears from the three species revealed infection by several types of microfilaria, Trypanosoma rangeli-like and Plasmodium brasilianum in all three, and Trypanosoma cruzi-like in howlers. These infections had no significant impact on the health status or the hematological profiles. Serologic investigations revealed occasional reactions against Toxoplasma gondii, a strong anti-Plasmodium response in the two Cebidae species, and a weaker one in tamarins. Attempts to isolate arbovirus failed, but antibody responses to Mayaro and yellow fever viruses were strong, especially in the howlers. A strong correlation between age and serological status led to a better understanding of the epidemic cycles. Our survey indicates French Guianan primates are reservoirs for several anthropozoonoses, including malaria, Chagas disease, and arboviruses.     

Habitat Selection and Use of Space by Bald-Faced Sakis (Pithecia irrorata) in Southwestern Amazonia: Lessons from a Multiyear, Multigroup Study

Population density and distribution in tropical forest vertebrates are directly linked to patterns of use of space relative to habitat structure and composition. To examine how forest type may explain the ranging behavior and high variance in group density observed within the geographic range of bald-faced saki monkeys (Pithecia irrorata), we monitored habitat use of 5 neighboring focal groups of this species in southwestern Amazonia over 3 yr. To test whether sakis are unflooded (terra firme) forest specialists, we compared home range (HR) use to the corresponding availability of 4 main forest types and quantified HR size and activity budgets as a function of forest type. HR size varied from 16 to 60 ha, and saki population density at this scale (12.5 ± 6.4 SD individuals/km²) was more closely related to forest type than to group size. Although sakis were not obligate habitat specialists, groups clearly avoided bamboo forest and preferred terra firme forest. Terra firme forests were associated with small HRs, intensive use, high HR overlap, and territorial defense, all of which suggest that saki densities will be higher in areas dominated by terra firme forest where large patches of bamboo (Guadua spp.) are absent. The increased desiccation and subsequent forest fires expected in this region from the combined impacts of climate change and human land use potentially threaten the long-term viability of old-growth terra firme forest specialists such as sakis. Regional-scale conservation efforts should ensure that extensive blocks of terra firme forest are protected in areas that remain relatively free of bamboo.     

The development of an operant conditioning training program for new world primates at the Bronx Zoo

This article describes the development of an operant conditioning training program for 17 species of New World primates at the Bronx Zoo. To apply less invasive techniques to husbandry protocols, the study introduced behaviors-hand feeding, syringe feeding, targeting, scale and crate training, and transponder reading-for formal training to 86 callitrichids and small-bodied cebids housed in 26 social groups. Individual responses to training varied greatly, but general patterns were noted among species. With the exception of lion tamarins, tamarins responded more rapidly than marmosets, Bolivian gray titi monkeys, and pale-headed saki monkeys in approaching trainers and learning behaviors. Marmosets, in comparison to most tamarins, had longer attention spans. This meant that fewer, lengthier sessions were productive whereas shorter, more frequent sessions were most successful for tamarins. Among the cebids, pale-headed saki monkeys needed relatively few sessions to perform basic and advanced behaviors whereas Bolivian gray titi monkeys were less responsive and progressed at a deliberate pace. Marked changes in the animals' behavior during daily husbandry procedures, their voluntary participation in training activities, and the disappearance of aggressive threats toward care staff indicated that training reduced stress and improved the welfare of the animals. During daily training displays, zoo visitors experienced interactive animals while learning the importance of low-stress animal husbandry.     

Adult male replacement in socially monogamous equatorial Saki monkeys (Pithecia aequatorialis)

Sakis (genus Pithecia) commonly live in socially monogamous groups, but data from wild populations on group dynamics and on the turnover of reproductive-age animals are rare. Here we describe the replacement of the adult male in one group of sakis in the Ecuadorian Amazon following the death of the initial resident. We use 354 h of focal behavioral data to describe differences in the spatial relationships among group members before and after the replacement and to examine changes in the rate of male-to-female grooming, aggression, scent marking and vocalization. Interactions with extra group individuals within the group's home range were more frequent during and after the replacement than before. The presence of such additional animals during periods of reproductive turnover may explain at least some reported observations of saki groups with more than 1 reproductive-age male or female.     

Abundance, diversity, and patterns of distribution of primates on the Tapiche River in Amazonian Peru

This work presents data on the relative diversity, abundance, and distribution patterns of primates in a 20 km2 area of the Tapiche River in the Peruvian Amazon. Population data were collected while the study area was both inundated and dry (March to September 1997) using conventional line-transect census techniques. Survey results reflected the presence of 11 primate species, but population parameters on only eight of the species will be presented, including saddleback tamarins (Saguinus fuscicollis), Bolivian squirrel monkeys (Saimiri boliviensis), brown capuchins (Cebus apella), white-fronted capuchins (Cebus albifrons), monk sakis (Pithecia monachus), red titi monkeys (Callicebus cupreus), red uakaris (Cacajao calvus), and red howler monkeys (Alouatta seniculus). Woolly monkeys (Lagothrix lagotricha), night monkeys (Aotus nancymaae), and pygmy marmosets (Callithrix pygmaea) were also seen in the area. The data for the smaller-bodied primates is similar to that reported almost 18 years earlier, but the data for the larger-bodied primates reflect a loss in the number of animals present in the area. Pressure from hunters and the timber industry may account for declining numbers of large-bodied primates, while it appears that natural features peculiar to the conservation area contribute to the patchy pattern of distribution.     

Establishment of a Captive All‐male Group of Proboscis Monkey (Nasalis larvatus) at the Singapore Zoo

Surplus male proboscis monkeys at the Singapore Zoo pose a considerable problem for maintenance and maximizing of exhibition potential. In 2008, a new exhibit was constructed to house and display a group of six proboscis monkey males born in Singapore Zoo. To document and monitor the all‐male group establishment in the new exhibit, we conducted observations on intragroup interactions between the monkeys, spatial use of their new exhibit, and visitor effects on their behavior. We found contact aggressive interactions between the monkeys to be consistently lower than noncontact aggressive interactions and by week six of introduction to the new exhibit, contact aggression was almost nonevident. Affiliative interactions also developed between individuals in the group, with an interface of aggressive and socioreconcilatory behavior influenced by food competition and a dominance hierarchy. This was evident from significantly higher overall aggression and affiliation during feeding times compared to nonfeeding times, and this was reduced when food competition was mitigated by modifying the feeding regime. We measured the groups’ spatial use of the exhibit and the relation to behavior, crowd size, and density. Our results showed that the proboscis monkeys utilized the available exhibit space, were largely unaffected by visitor crowd size and density, and were able to exhibit a variety of natural behaviors, including swimming. Our accomplishment in maintaining and displaying an all‐male group of proboscis monkeys in captivity provides viable options for more comprehensive captive management and breeding programs for this endangered species. Zoo Biol. 32:281‐290, 2013. © 2012 Wiley Periodicals, Inc.     

Cranial evolution in sakis (Pithecia, Platyrrhini). II: Evolutionary processes and morphological integration

Patterns of interspecific differentiation in saki monkeys (Pithecia) are quantitatively described and possible evolutionary processes producing them are examined. The comparison of species correlation matrices to expected patterns of morphological integration reveal significant and similar patterns of development-based cranial integration among species. Aspects of the facial region are more heavily influenced by general size variation than features of the neural region. The comparison of pooled within- and between-groups V/CV matrices suggests that genetic drift might be a sufficient explanation for saki cranial evolution. Differential natural selection gradients are also reconstructed because selection may also have caused population differentiation through evolutionary time. These gradients illustrate the inherent multivariate nature of selection, being a consequence of the interaction between existing morphological integration (correlation) among traits and the action of natural selection. Yet, our attempt to interpret selection gradients in terms of their functional significance did not result in any clear association between selection and function. Perhaps this is also an indication that morphological evolution in sakis was mostly neutral.     

Alu insertion loci and platyrrhine primate phylogeny

Short INterspersed Elements (SINEs) make very useful phylogenetic markers because the integration of a particular element at a location in the genome is irreversible and of known polarity. These attributes make analysis of SINEs as phylogenetic characters an essentially homoplasy-free affair. Alu elements are primate-specific SINEs that make up a large portion of the human genome and are also widespread in other primates. Using a combination wet-bench and computational approach we recovered 190 Alu insertions, 183 of which are specific to the genomes of nine New World primates. We used these loci to investigate branching order and have produced a cladogram that supports a sister relationship between Atelidae (spider, woolly, and howler monkeys) and Cebidae (marmosets, tamarins, and owl monkeys) and then the joining of this two family clade to Pitheciidae (titi and saki monkeys). The data support these relationships with a homoplasy index of 0.00. In this study, we report one of the largest applications of SINE elements to phylogenetic analysis to date, and the results provide a robust molecular phylogeny for platyrrhine primates.     

Cranial evolution in sakis (Pithecia, Platyrrhini) I: interspecific differentiation and allometric patterns

Patterns of interspecific differentiation in saki monkey (Pithecia) skulls are quantitatively described. The taxonomic arrangement previously proposed by Hershkovitz ([1987] Am. J. Primatol. 12:387-468) is consistent with quantitative differences in saki morphology. Discriminant analyses on 39 skull traits show that Pithecia species and subspecies are well-differentiated. Morphological distances (D2) among sakis clearly show the morphological unity of the pithecia-chrysocephala (Pithecia) and irrorata-vanzolinii-monacha (Monacha) species groups. The Pithecia species group is distributed north of the Amazon and has a smaller cranium than the Monacha group, distributed south of that river. Despite the size difference, multivariate static allometric patterns among sakis are quite similar. After removing size and allometric changes in shape from the data, species and subspecies are still differentiated, although to a lesser extent. D2 distances obtained from these scale-corrected data are similar in magnitude and pattern to the original D2, but show a closer similarity of P. monacha with the Pithecia group. P. monacha is a scaled-up version of the smaller sakis.     

Model vs. playback experiments: The impact of sensory mode on predator-specific escape responses in saki monkeys

Although experimentally simulating predator presence helps improve sample sizes in studies of free-ranging animals, few studies have examined whether auditory playbacks and visual models produce similar results. Additionally, it is unclear if anti-predator strategies are specific to predator hunting styles in understudied Neotropical pitheciid primates, limiting what we can generalize about this phenomenon across this taxonomic order. We conducted predator simulation experiments to assess whether wild Rylands' bald-faced saki monkeys (Pithecia rylandsi) recognize predators based solely on acoustic cues, exhibit predator-specific responses to different predator types, and vary responses to presentations in different sensory modes. In our playback experiments, sakis had weak responses to non-predator control vocalizations compared to jaguar growls and harpy eagle shrieks. In most predator playbacks, subjects' first glance corresponded to the direction from which simulated predators would typically attack (above vs. below). However, although sakis exhibited appropriate movement responses to harpy playbacks (i.e., descending canopy), they exhibited no clear movement patterns when presented with jaguar playbacks. In contrast, jaguar model experiments consistently elicited fast approaches, mobbing-style responses, and long alarm calling bouts. Thus, if we had relied on playbacks alone, we might have concluded that sakis have only generalized responses to terrestrial ambush predators. In fact, in all variables measured (e.g., latency, number of calls, and response duration), models of both predator species elicited stronger reactions than playbacks. Results indicate that bald-faced sakis can identify predators based solely on vocalizations, but do not exhibit predator-specific escape responses to terrestrial predators based on acoustic cues alone. The differential response to playbacks and models calls into question the reliability of using acoustic-only stimuli to assess the specificity of anti-predator behavior to predator hunting styles in some primate species.     

Notes on the ecology of buffy saki monkeys (Pithecia albicans,Gray 1860): A canopy seed-predator

Data on the ecology and diet of buffy sakis (Pithecia albicans) were obtained during a 20-month study in an entirely undisturbed terra firme forest in the upper Urucu river, Amazonas, Brazil. Groups of 3–7 sakis found in a 900-ha study plot used large home ranges (147–204 ha), which overlapped extensively with those of neighboring groups. Similar to other pitheciines, buffy sakis were primarily seed predators, relying heavily on young seeds of certain key plant families, such as the Sapotaceae and Leguminosae. Ripe fruits, ripe seeds, young leaves, flowers, and nectar were eaten to a lesser extent. Whether or not feeding, sakis spent most of their time in the canopy and subcanopy, a pattern similar to that of other southwestern Amazonian saki species, but sharply different from that of Guianan sakis (Pithecia pithecia), which use considerably lower levels of the forest. Comparisons are made between different Pithecia species to show whether and how P. albicans diverges ecologically from its congeners. © 1993 Wiley-Liss, Inc.     

Gis analysis of patch use and group cohesiveness of bearded sakis (chiropotes sagulatus) in the upper essequibo conservation concession,guyana

This study examines how northern bearded sakis (Chiropotes sagulatus) in Guyana adjust group cohesiveness according to the distribution and quality of food patches. I introduce a GIS based method for quantifying food patch quality and how it relates to bearded saki group spread and group size. While the concept of food patch is central to most models of primate socioecology, defining what constitutes a patch has been notoriously problematic in primate studies. In addition, researchers have struggled to quantify group spread and group cohesiveness. Advances in spatial analysis software in the last decade now allow primate researchers to better quantify these variables. Group spread in bearded sakis was not significantly greater in lower quality patches and sakis were not more spread out during feeding than during other activities. However, the study group was significantly less spread out during social behavior. Bearded saki group size was significantly correlated with both monthly fruit abundance and patch quality. In fact, mean daily patch quality explained ～40% of the variation in foraging party size. These results suggest that bearded sakis may rely on a highly fluid social structure to mitigate the effects of intragroup feeding competition while living in large groups. Sakis do not adjust group spread on a patch‐by‐patch basis but rather fission into smaller foraging parties when resources become scarce seasonally and patch quality is low. This study shows that GIS is a powerful tool for modeling the relationship between group cohesiveness and resource quality and distribution. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Seed predation by monkeys and macaws in eastern Venezuela: Preliminary findings

Feeding data collected concurrently on bearded sakis (Chiropotes satanas) and red and green macaws (Ara chloroptera) on a large island in Guri, Venezuela provides preliminary evidence that these two seed predators have similar diets. Individuals of both species were equally capable of opening very hard, protected fruits. Of the seven fruit species used by macaws during the study period, four species were also ingested by sakis at the same stage of ripeness, two species were ingested at different stages of ripeness (macaws earlier than sakis), and one species was never observed to have been eaten by sakis. The second finding, that macaws ingest young seeds of the Anacardiaceae and Burseraceae families and the bearded sakis ingest only the ripe mesocarp of these species suggests that the most distinguishable difference in their diets might be a tolerance of toxins by the macaws that act as feeding deterrents for the monkeys. Although we did not document the location of local clay licks in eastern Venezuela, the use of clay licks by macaws in Peru (Munn, 1992) suggests that this activity (that is not practiced by the sakis) may be helpful in detoxifying or ameliorating the effects of ingesting chemically protected fruit. deceased.     

Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus).

We monitored the birth patterns of sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus) during a 4‐yr period from October 1996 to August 2000 at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Brown howler monkey births (n = 34) occurred throughout the year, and birth frequencies did not differ between rainy and dry season months. The aseasonal birth patterns of the howler monkeys differed significantly from the dry season concentration and dry month peak in muriqui births (n = 23). We found no effects of infant sex or the number of females on interbirth intervals (IBIs) in our 10 howler monkey study troops. IBIs of brown howler monkeys averaged 21.2 ± 2.5 mo (n = 8, median = 21.0 mo), and were significantly shorter following dry season births than rainy season births. Their IBIs and yearling survivorship (74%) were similar to those reported for other species of howler monkeys, but yearling survivorship was much lower than that of muriquis (94%), whose IBIs were more than 12 mo longer than those of the howler monkeys. Our study extends comparative knowledge of birth patterns in Alouatta to a poorly known species, and provides insights into the different ways in which diet and life history may affect the timing of births in large‐bodied platyrrhines under the same seasonal ecological conditions. Am. J. Primatol. 55:87–100, 2001. © 2001 Wiley‐Liss, Inc.     

Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest

This paper presents and discusses aspects of fruit selectivity by red howler monkeys (Alouatta seniculus) in relation with morphological characteristics of fruits. These data are used to provide an answer to the following questions: which are the fruit characteristics that lead fruit choice of howler monkeys and to what extent fruit characteristics play a role in seed dispersal by monkeys? The frugivorous diet of a troop of red howler monkeys was determined during a 2-year field study in French Guiana. The selection of fruit by howler monkeys was analyzed in relation to the fruit availability. Results showed that, although consumption followed availability, fruit species could be classified in three categories according to their selection ratio (percentage of consumption/percentage of abundance) as “high ranking,” “middle ranking,” and “low ranking” species. Also, the 97 species of fruit eaten by the monkeys were grouped according to the morphological characteristics thought to influence the monkeys' choice. This showed that howler monkeys consumed essentially fruits with juicy pulp, bright color, and a small number of well-protected seeds. Most of high ranking species had medium-sized fruits with yellow color, and low ranking species often had small fruits. However, howler monkeys are associated with the dispersal of seeds from fruit with a hard and indehiscent pericarp and/or large seeds, like those of the Sapotaceae family. Consequently, they can be considered as “specialized” frugivores for this fruit syndrome. © l996 Wiley-Liss, Inc.     

Male Relationships and Infant Deaths in Red Howler Monkeys (Alouatta seniculus)

For decades howler monkeys were considered to be among the most peaceful animals. Recent investigators, however, have noted that, although male aggression is rare, it may be extremely severe; the criteria used to quantify howler relationships should therefore be different from those used for other primates. This paper describes the pattern of male relationships in the red howler monkey Alouatta seniculus, and examines its effect on reproductive success within the troop and the ability of troop males to resist intrusion by competing males. 4 of the 8 infants born during the study period were killed or disappeared when change occurred in relative status between two adult males.     

Captive-born cotton-top tamarins (Saguinus oedipus) respond similarly to vocalizations of predators and sympatric nonpredators

What types of cues do callitrichid primates use to detect and respond to predators? Do they respond to predator‐specific cues or to more general cues? The evidence for these questions remains conflicting. We presented captive‐born and reared cotton‐top tamarins with no previous exposure to predators (or predator cues) with vocalizations from three potential predators of cotton‐top tamarin in the wild (white hawk, jaguar, and tayra) and with vocalizations from sympatric nonpredators (black‐faced antthrush and red howler monkey). Vocalizations from predators and from nonpredator mammals elicited equivalent arousal, fear, and vocal responses. Howler monkey roars produced the strongest responses. The results suggest that predator‐naïve cotton‐top tamarins do not recognize specific predator vocalizations, but may respond to vocal qualities (low‐frequency, noisy sounds) that indicate large body size, threat, or aggression. On the other hand, tamarins responded much more strongly to the higher frequency calls from the hawk than the antthrush, suggesting another mechanism must also be involved. The failure of captive‐reared tamarins to distinguish between vocalizations of predators and nonpredator mammals has important implications for reintroduction studies. Am. J. Primatol. 70:707–710, 2008. © 2008 Wiley‐Liss, Inc.     

Selected aspects of female white-faced saki (Pithecia pithecia) reproductive biology in captivity

Little is known regarding the reproductive biology of the white-faced saki. Although sakis have been in zoos since the mid-1970s, little attention has been paid to the reproductive biology of this threatened species. This study describes the results of a 3-year study of the reproduction of the white-faced saki in captivity. Using noninvasive methods to determine levels of estrone conjugates (E₁C) and pregnanediol-3-glucuronide (PdG) in daily urine samples, we have characterized the female reproductive cycle of this species. Nonconceptive ovarian cycles were 16.95 ± 1.57 (SD) days, gestational length was 146.1 ± 5.2 (SD) days, and the length of lactationally induced infertility varied among females but averaged 163 ± 40.6 (SD) days. Attempts to accelerate puberty by pairing a young female with an adult male was without effect. Puberty occurred at 32 months of age in one female. This study provides information that enhances our understanding of the reproductive biology of this species. © 1995 Wiley-Liss, Inc.     

Within-group social bonds in white-faced saki monkeys (Pithecia pithecia) display male-female pair preference

White‐faced saki monkeys (Pithecia pithecia) lack most of the behavioral and physical traits typical of primate monogamy [Fuentes, 1999 ]. In order to determine if social bonds in this species reflect patterns displayed by pair‐bonded groups or larger multimale–multifemale groups, we draw on 17 months of data collected on wild white‐faced sakis at Brownsberg Nature Park, Suriname. We analyzed within‐group social bonds for three habituated groups (one two‐adult and two multiadult groups) by measuring grooming, proximity, and approach/leave patterns between adult and subadult group members. We found that both two‐adult and multiadult groups showed significantly stronger social bonds between a single male–female dyad within each group (deemed “primary dyads”). In all three groups, primary dyads were composed of the oldest adult male and a breeding female. These pairs had significantly higher levels of grooming than other within‐group dyads and were also in close proximity (<1 m) more often than nonprimary dyads. Grooming in primary dyads was nonreciprocal, and consistently biased toward female investment. Grooming patterns in nonprimary dyads varied, but were often more reciprocal. Grooming and proximity of the primary dyad also changed in relation to infant development. Our results suggest that while white‐faced sakis do not show behavioral and physical traits typical of monogamy or pair‐bonding, social bonds are strongest between a single male–female pair. Pitheciine social systems range from small group monogamy in Callicebus to large multimale–multifemale groups in Chiropotes and Cacajao. As the middle taxon in this platyrrhine radiation, behavioral strategies of white‐faced sakis provide a model for how social bonds and affiliation could be influenced by and affect the evolution of larger group size in primates. Am. J. Primatol. 73:1051–1061, 2011. © 2011 Wiley‐Liss, Inc.     

Comparative locomotion of six sympatric primates in Ecuador

Primates exhibit a great variety of arboreal locomotor modes associated with their size and postcranial morphology. The study of sympatric primates is interesting in that it may reveal how primates of different sizes and anatomies move and select for forest structure. This study reports on preliminary data on the locomotion of six non-ateline platyrrhines found in the Yasuni National Park, Napo Province, Ecuador. Pygmy marmosets are confined to the understory using scansorial locomotion and quadrupedalism, preferring large vertical supports. Golden-mantled tamarins, common squirrel monkeys and dusky titis also range in the understory, moving by quadrupedal walk and leap, mainly on small horizontal supports. Monk sakis are found in the main canopy and use quadrupedal walk and less leap on medium-sized horizontal supports. Whitefronted capuchins use the understory and the main canopy equally often, walking quadrupedally and leaping on small and medium-sized oblique supports. In general, smaller species occupy lower strata while larger species tend to spend more time in the upper strata. Small tegulae-bearing monkeys showed the highest proportions of large vertical support use. For all species, leaping was the main gap-crossing mode, though decreasing in proportion with a higher use of the upper forest layers.