Parasites of Wild Howlers (Alouatta spp.)

A literature review of howler parasites provides the basis for an overview of the ecological significance of parasite surveys in primates. Within this framework, we have added insights into the interactions between primate hosts and their parasites from a long-term study in Costa Rica. We collected fecal samples from mantled howlers (Alouatta palliata) over a 9-year period (1986–1994 inclusive) and analyzed them for parasite eggs, larvae, cysts, and oocysts. We found many misperceptions inherent in the typical methodology of primate parasite surveys and in the reporting of the findings. Our work in Costa Rica suggests that a snapshot effect occurs with most surveys. A static view does not reflect the dynamic and changing ecological interaction between host and parasite. We describe some problems with parasite data analyses that emphasize the need for long-term longitudinal surveys in wild primate groups.     

Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes

The gastrointestinal (GI) microbiome contributes significantly to host nutrition and health. However, relationships involving GI microbes, their hosts and host macrohabitats remain to be established. Here, we define clear patterns of variation in the GI microbiomes of six groups of Mexican black howler monkeys (Alouatta pigra) occupying a gradation of habitats including a continuous evergreen rainforest, an evergreen rainforest fragment, a continuous semi-deciduous forest and captivity. High throughput microbial 16S ribosomal RNA gene sequencing indicated that diversity, richness and composition of howler GI microbiomes varied with host habitat in relation to diet. Howlers occupying suboptimal habitats consumed less diverse diets and correspondingly had less diverse gut microbiomes. Quantitative real-time PCR also revealed a reduction in the number of genes related to butyrate production and hydrogen metabolism in the microbiomes of howlers occupying suboptimal habitats, which may impact host health.     

Resource use by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas,Veracruz, Mexico

The feeding preferences of howler monkeys at their northernmost distribution in the Neotropics are reported for an annual cycle. A remarkable selectivity for 27 species representing 15 families was observed. The Moraceae and Lauraceae plant families were the most important in the diet. The howlers spent an almost equal proportion of their feeding time eating leaves and fruit, and displayed a marked preference for young leaves and mature fruit. The consumption of different plant parts was markedly seasonal and the howlers’ ranging behavior was closely associated with the availability of young leaves and mature fruit. Their home range was unusually large (ca. 60 ha) for howlers and the food species exploited occur at very low densities (93%, ≤ 4 ind/ha). They chose food items richer in protein and energy. Alkaloid compounds, present in some of the leaves, play a secondary role in their dietary selectivity.     

A mandible ofBranisella boliviana (Platyrrhini,Primates) from the oligocene of South America

A mandibular specimen from the Bolivian Early Oligocene is provisionally assigned toBranisella boliviana. The crown anatomy of the single preserved tooth, an M₂, indicates platyrrhine affinities and several details of the broken jaw are suggestive of symphyseal fusion. Like the African Oligocene parapithecids,Branisella contrasts with extant anthropoids in the relative shallowness of its mandible.Branisella is the most ancient, and seemingly the most primitive, fossil platyrrhine monkey, lacking any of the derived features of the two major clades of modern ceboids. Taxonomically, it is best regarded as family incertae sedis.     

Ovarian and Uterine Ultrasonography in <Emphasis Type="Italic">Aotus azarai infulatus</Emphasis>

We evaluated the uterus and ovaries of owl monkeys (Aotus azarai infulatus) via gynecological ultrasound examination. We evaluated the subjects in 2 different time periods. The first period (P1) was characterized by the absence of mating, with daily examinations, during 4 mo (n = 10). At the end of P1, we paired the subjects for 30 d, but without ultrasonographic evaluation. The second period (P2) was characterized by the presence of mating, with examinations once a week, during 7 consecutive months (n = 9). We evaluated the uterus and ovaries in sagittal and transverse scans, using a 5–12 MHz linear array probe. The uterine volume (UV) was directly proportional to the number of previous parturitions. The right ovary volume (RtOV) is greater than the left (LtOV) in P1 and P2. There is a positive correlation (p < 0.05) between the females’ mass, RtOV (r = 0.28) and LtOV (r = 0.16).     

Synteny of human chromosomes 14 and 15 in the platyrrhines (Primates, Platyrrhini)

In order to study the intra- and interspecific variability of the 14/15 association in Platyrrhini, we analyzed 15 species from 13 genera, including species that had not been described yet. The DNA libraries of human chromosomes 14 and 15 were hybridized to metaphases of Alouatta guariba clamitans, A. caraya, A. sara, Ateles paniscus chamek, Lagothrix lagothricha, Brachyteles arachnoides, Saguinus midas midas, Leontopithecus chrysomelas, Callimico goeldii, Callithrix sp., Cebus apella, Aotus nigriceps, Cacajao melanocephalus,Chiropotes satanas and Callicebus caligatus. The 14/15 hybridization pattern was present in 13 species, but not in Alouatta sara that showed a 14/15/14 pattern and Aotus nigriceps that showed a 15/14/15/14 pattern. In the majority of the species, the HSA 14 homologue retained synteny for the entire chromosome, whereas the HSA 15 homologue displayed fragmented segments. Within primates, the New World monkeys represent the taxon with the highest variability in chromosome number (2n = 16 to 62). The presence of the HSA 14/15 association in all species and subspecies studied herein confirms that this association is the ancestral condition for platyrrhines and that this association has been retained in most platyrrhines, despite the occurrence of extensive inter- and intrachromosomal rearrangements in this infraorder of Primates.     

Environmental Determinants of Birth Seasonality in Night Monkeys (Aotus azarai) of the Argentinean Chaco

The night monkeys (Aotus azarai) of Formosa, Argentina provide an opportunity to investigate the influences of ambient temperature and photoperiod on reproduction in a highly seasonal environment: the Chaco. Between 1997 and 2000, we collected data to evaluate the relationship between rainfall, ambient temperature, photoperiod and food availability and the annual distribution of mating behavior and births in 15 groups of monkeys in the forests of the Eastern Argentinean Chaco. Our data show that the area is highly seasonal, characterized by significant fluctuations in rainfall, temperature, photoperiod and food availability. There are two rain peaks in April and November and a dry season lasting from June to August. Monthly mean temperatures were on average 11°C lower during winter months than they were during summer months. Temperatures <10°C and >33°C were also frequent through the year. Days are 3 h longer during the summer than during the winter months. Insect abundance and the percentage of tree species producing fruits, flowers or new leaves reached a low in the coldest winter months. Mating was infrequent, and we only observed it between May and September. Half the births (n = 13) occurred during a 2-week period in October. Infant survival during the first 6 mo of life was high (96%). Our findings suggest an environmental control of reproduction. Changes in photoperiod and temperature may promote reproductive activity in females that might conceive and begin pregnancy at a time void of high temperatures that could be metabolically challenging.     

Conservation Biology of the Genus Alouatta

As assessed by the IUCN Mace–Lande system, seven (35%) of the 20 Alouatta species and subspecies with adequate data are classified as threatened, i.e., critically endangered, endangered, or vulnerable (Rylands et al., 1995). This percentage is much lower than the 75 to 100% threatened taxa for the other large-bodied genera: Ateles, Lagothrix, and Brachyteles. Only 5 of the 16 Neotropical genera have lower percentages of threatened taxa than that of Alouatta: Cebuella, Pithecia, Saguinus, Saimiri, and Cebus. The threatened howler taxa occupy small distributions in areas of forest fragmentation. In general, populations are most affected by major habitat disturbance, such as total deforestation and flooding from dam construction, and by human hunters. Facilitated by their ability to exploit folivorous diets in small home ranges, howlers can tolerate considerable habitat fragmentation but not the increased exposure to hunting that may accompany it. Howlers seem particularly vulnerable to yellow fever and bot fly parasitism. Although the former threat may decrease by increasing fragmentation of the habitat, other sorts of parasitism may increase in disturbed habitats. The low genetic variability of the Central American howlers suggests a resistance to inbreeding depression potentially experienced during population bottlenecks. Greater between-population variability may still exist. Although howlers are not readily bred in captivity, they respond well to translocation. Translocation has been successfully achieved for 4 howler species and is a viable option for introducing new genetic variability into population fragments and repopulating areas from which howlers are extinct. Their pattern of bisexual dispersal facilitates colonization of regenerating habitats, and in suitable, protected habitats they have shown the capacity for strong population recovery.     

Erythrocyte glyoxalase I polymorphism in the owl monkey,Aotus

Three erythrocyte glyoxalase I phenotypes were observed in a sample of 235 karyotypically defined New World owl monkeys, Aotus. The selective distribution of glyoxalase I allele (GLO¹, GLO²) is related to the karyotype of each animal. Owl monkeys with a karyotype VI had an equal distribution of GLO¹ and GLO² genes in the population. Aotus with karyotype II, III, IV, or V had, exclusively, the GLO² allele (expressed as the fast electrophoretic phenotype), in contrast with monkeys with karyotype I or VII, which had only the GLO¹ allele (expressed as the slow electrophoretic phenotype).     

Physiological Ecology of Howlers (Alouatta): Energetic and Digestive Considerations and Comparison with the Colobinae

Remarkably little attention has been focused on the physiological ecology of free-ranging primates. Yet without such information, it may prove difficult to advance our understanding of factors influencing the dietary behavior of wild primates much beyond its present state. Mantled howlers (Alouatta palliata) have been studied in terms of some features of physiological ecology. Results of this work have helped to clarify some factors influencing howler and other primate food choices in the natural environment and have called into question various assumptions about leaf-eating primates. For example, though howlers eat considerable foliage, they do not exhibit a lower than predicted basal metabolic rate, nor do available data suggest that secondary compounds strongly influence howler food selection. Comparison of howlers with members of the Colobinae reveals some differences in features of their respective energetic and digestive physiology and raises timely issues for future research.     

Chromosome comparison among five species of platyrrhini (Alouatta caraya,Aotus azarae,Callithrix jacchus,Cebus apella,andSaimiri sciureus)

Karyotypes of 82 individuals from five Platyrrhini species (Alouatta caraya, Aotus azarae, Callithrix jacchus, Cebus apella, andSaimiri sciureus) were studied and compared using a G-banding technique. Cytogenetic analysis showed full chromosome or full arm homologies among these geographically neighbouring species. A small number of chromosomal rearrangements (inversions, deletions, and translocations) could be detected among these taxa. These five species are closely related in chromosomal evolution. An interesting correspondance was found betweenCebus apella chromosomes and those of the other four species.Alouatta caraya andCebus apella are the closest species.Callithrix jacchus andAotus azarae would have the most separated karyotypes.     

Owl monkeys (Aotus) are highly divergent in mitochondrial Cytochromec Oxidase (COII) sequences

The evolutionary history and differentiation of the owl or night monkeys (Aotus),remain poorly resolved. Variation in pelage and skeletal morphology is relatively minor across their broad range, but cytogenetic studies have revealed that at least 12 karyotypically distinct forms exist, with 2Nchromosome numbers ranging from 46 to 58. We obtained DNA samples from three putative species- A. lemurinus, A. nancymae,and A. azarae-and five karyotypes (I, II, III, IV and VI), amplified the mitochondrial cytochrome coxidase subunit II gene (COII) via PCR and sequenced it. Comparisons of the sequences indicate relatively high levels of sequence divergence among the putative species (4.3 to 6.3%), and suggest that the taxa are genetically quite distinct and have likely experienced extended periods of isolated evolution. The levels of COII divergence represent approximately one- third of the levels found between divergent platyrrhine genera, such as Aotus, Saimiriand Callimico.Using estimates of substitution rates of COII evolution in hominoid primates,the estimated date of divergence for the AotusCOII sequences is 3.6 million years. The AotusCOII data support the existence of multiple species of Aotus,with origins predating late Pleistocene climatic events. Although A. nancymaeand A. azaraeboth live south of the Amazon River and have been considered members of the same species group, phylogenetic analysis of the COII sequences does not support a close relationship between them.     

Electron microscopic study of the origin and formation of Reissner's fiber in the subcommissural organ of Cebus apella (Primates,Platyrrhini)

Summary Two kinds of secretion are formed in cells of the subcommissural organ (SCO) of Cebus apella. The light secretion is found in saccules originating from the endoplasmic reticulum. This secretion is stored in the peripheral portion of the cells and is not involved in formation of Reissner's fiber (RF). In close association with the Golgi complex, electron-dense granules are developed, containing a finely granular substance. These granules accumulate beneath the apical plasmalemma of the cell. Their content is discharged into the third ventricle, where it occurs in the form of a thin layer of secretion. This material appears to constitute the RF at the level of the entrance to the mesencephalic aqueduct.     

Taxonomy of theAlouatta seniculus group: Biochemical and chromosome data

Wild populations ofAlouatta belzebul andA. seniculus from Brazil were surveyed in relation to 20 protein loci. Estimates of genetic variability demonstrated thatA. seniculus presents the highest level of heterozygosity among several New World monkey species studied for the same loci. Additional information from DNA and chromosomes suggest thatA. seniculus andA. belzebul are not the closest species in theHershkovitz’sAlouatta seniculus group.     

Intragroup Social Relationships of Male Alouatta palliata on Barro Colorado Island,Republic of Panama

We examined social and spatial relations of adult males in one group of mantled howling monkeys (Alouatta palliata) on Barro Colorado Island (BCI) in central Panama to document patterns of association. Beyond the existence of an alpha male, we could not distinguish any linear dominance hierarchy among the 6 study males. All males copulated with estrous females. Our findings contrast with reports of intragroup male behavior in Costa Rican howlers. Study males engaged in little or no affiliative or agonistic behavior with one another, but engaged in significantly more such interactions with females. The alpha male, the oldest male and a younger male were most frequently in association with females. Of group males, the oldest male associated significantly more with other males. Overall, male behavior in mantled howling monkeys on BCI generally followed the van Hooff and van Schaik (1994) model of male relationships. The low incidence of intragroup social interactions of any type in the focal males may reflect the energetic costs of social behavior. We suggest that intragroup social relationships among mantled howler males are structured by more subtle means than overt physical interactions, possibly including vocal communication, relationships with individual group females, and kinship.     

Aotus from the southwestern Amazon region is geographically and chromosomally intermediate betweenA. azarae boliviensis andA. infulatus

We described the karyotypes detected in 23Aotus specimens captured on Southwestern Amazon region (63°30'W, 9°00'S). This region should be occupied byA. nigriceps. However, the animals described here have a fur pattern and a karyotypes similar to those ofA. azarae boliviensis andA. infulatus. The females presented 50 chromosomes and the males 49 as a consequence of fusion between the chromosome Y and an autosome. This sample presented polymorphisms of G- and C-banding and NOR-staining. These animals are karyotypically intermediate betweenA. a. boliviensis andA. infulatus. The taxonomy and karyotypic evolution of these taxa are discussed.     

Mitochondrial pseudogenes and phyletic relationships ofCebuella andCallithrix (Platyrrhini, primates)

Two cytochromeb pseudogenes were isolated from PCR amplified products ofCebuella pygmaea DNA. These sequences showed insertions and deletions when compared to paralogous mitochondrial sequence regions of several primates. Phylogenetic analyses indicated that an ancestral pseudogene originated sometime before the divergence ofCebuella andCallithrix and that this sequence was later duplicated some 5.6 million years ago. Parsimony and distance analyses indicated thatCebuella pygmaea andCallithrix species of theargentata group were more closely related to one another than any of them was toCallithrix species of thejacchus group, in agreement with previous analyses based on nuclear genes and karyotypic data. These findings also indicated thatCallithrix is a paraphyletic genus, in agreement with previous propositions thatCebuella should be included within the genusCallithrix.     

Taste preference thresholds for food-associated sugars in the squirrel monkey (Saimiri sciureus)

The purpose of this study was to determine taste preference thresholds for four different food-associated sugars inSaimiri sciureus. Using a two-bottle test three male squirrel monkeys were found to significantly prefer 10 mM sucrose, 40 mM fructose, 90 mM glucose, and 100 mM lactose over tap water. Presentation of suprathreshold sugar solutions led to marked concentration-dependent and monotonically increasing polydipsia. The results showed the squirrel monkey to prefer lower sugar concentrations compared to other non-human primates and thus support the assumption that this species may use sweetness as a criterion for food selection.     

Zoogeography of Chiropotes albinasus (Platyrrhini,Atelidae) in Southwestern Amazonia

White-nosed bearded sakis (Chiropotes albinasus) are endemic to the Madeira–Xingú interfluvium in southern Amazonia, though recent fieldwork has produced conflicting data on the southwestern limits of the species's geographic range. We reevaluated the distribution of bearded sakis on the basis of surveys from 34 sites throughout the Brazilian state of Rondônia. Chiropotes albinasus occurred at seven sites in the eastern part of the state, including two west of the Jiparaná–Pimenta Bueno river system in the extreme south, but there is no record of their presence further north and west in the Jiparaná–Guaporé interfluvium and they were absent from the Jiparaná–Mamoré interfluvium. The data suggest that ecological, rather than geographic barriers restrict the distribution of Chiropotes albinasus in southern Rondônia, but are contradictory with regard to the possible determining factors. Chiropotes albinasus appears able to thrive in transitional, savanna-like ecosystems in southern Rondônia, but is unexpectedly absent from adjacent areas of terra firme forest. Syntopy with the only other pitheciine found in the state (Pithecia irrorata) appears to have a negative effect on the abundance of Chiropotes albinasus which implies that interspecific competition may reinforce a complex of limiting factors, such as the availability of key plant species. Despite showing that Chiropotes albinasus is widespread in southern Rondônia, we also confirm its absence from the western two thirds of the state, a significant reduction in the known range of the species.