Morphological analysis ofAlouatta seniculus species group (Primates,Cebidae). A comparison with biochemical and karyological data

Fifteen cranial measurements were taken from wild caught specimens ofAlouatta seniculus seniculus, A. s. stramineus andA. s. macconnelli. A morphological analysis showed sex dimorphism in these three groups. A multivariate analysis discriminated among these taxa; males being more clearly discriminated than females. Our data showed that these taxa can be separated on the basis of quantitative cranial traits, biogeographic distribution, karyological differences, and biochemical characters. We therefore propose a new taxonomic arrangement, changing their taxonomic status to the species level (Alouatta seniculus, A. macconnelli, andA. stramineus).     

Relation of Intergroup Variation in Allogrooming to Group Social Structure and Ectoparasite Loads in Red Howlers (Alouatta seniculus)

We compare the allogrooming behavior of 5 troops (average size = 8.2) of red howlers (Alouatta seniculus) from the Venezuelan Llanos with that of other A. seniculus and Alouatta spp. of the genus. In 126.9 observation hr, we recorded 118 allogrooming events, with an average bout length of 109 sec. Females groomed more frequently than males did, but as groomees there is no significant differences between sexes. Adult males groomed adult females mostly in a sexual context (before copulation). Allogrooming rates differ significantly among groups. There are also significant differences among members of the same troop both as groomers and groomees, which we explain in the context of the social behavior and history of each troop. There is no significant correlation between weight of the groomee and duration of the grooming bout. However, the examination of grooming rates and ectoparasite load suggests that allogrooming may have hygienic consequences. Differences in allogrooming rates among species of Alouatta are related to differences in group kin structure and patterns of female competition, in particular, coalition formation. We conclude that the social structure and the degree of relatedness among individuals within a group (or among individuals in a population in interpopulation comparisons) is a more important determinant of allogrooming rate than body size or group size. Our results emphasize the importance of considering intergroup and interpopulational variation in behavior.     

In situ hybridization (FISH) maps chromosomal homologies between Alouatta belzebul (Platyrrhini,Cebidae) and other primates and reveals extensive interchromosomal rearrangements between howler monkey genomes

We hybridized whole human chromosome specific probes to metaphases of the black-and-red howler monkey Alouatta belzebul in order to establish chromosomal homology between humans and black-and-red howlers. The results show that the black-and-red howler monkey has a highly rearranged genome and that the human chromosome homologs are often fragmented and translocated. The number of hybridization signals we obtained per haploid set was 40. Nine human chromosome probes gave multiple signals on different howler chromosomes, showing that their synteny is disturbed in A. Belzebul. Fourteen black-and-red howler autosomes were completely hybridized by one human autosomal paint, six had two signals, three had three signals, and one chromosome had four signals. Howler chromosomes with multiple signals have produced 12 chromosomal syntenies or hybridization associations which differ from those found in humans: 1/2, 2/20, 3/21, 4/15, 4/16, 5/7, 5/11, 8/18, 9/12, 10/16, 14/15, and 15/22. The hybridization pattern was then compared with those found in two red howler taxa and other mammals. The comparison shows that even within the genus Alouatta numerous interchromosomal rearrangements differentiate each taxa: A. belzebul has six unique apomorphic associations, A. seniculus sara and A. seniculus arctoidea share seven derived associations, and additionally A. seniculus sara has four apomorphic associations and A. seniculus arctoideaseven apomorphic associations. A. belzebul appears to have a more conserved karyotype than the red howlers. Both red and black-and-red howlers are characterized by Y-autosome translocations; the peculiar chromosomal sex system found in the red howler taxa could be considered a further transformation of the A. belzebul sex system. The finding that apparently morphologically similar or even identical taxa have such extreme genomic differences has important implications for speciation theory and neotropical primate conservation. Am. J. Primatol. 46:119–133, 1998. © 1998 Wiley-Liss, Inc.     

Cytogenetic analysis shows extensive genomic rearrangements between red howler (Alouatta seniculus,Linnaeus) subspecies

A comparison of the G-banded karyotypes of two red howler subspecies, Alouatta seniculus arctoidea and A. s. sara, showed that they differed by at least 14 chromosomal rearrangements. Genomic reshuffling is so great that homologs between subspecies could not be found for some chromosome, while the assignment of homology for other chromosomes remains uncertain. The two red howlers, however, share an unusual X₁X₂Y₁Y₂/ X₁X₁X₂X₂ sex-chromosome system that resulted from a Y-autosome translocation, probably in a common ancestor. The great chromosomal variability resulting from rapid chromosomal evolution in howlers indicates that cytogenetic data could make an important contribution to resolving phylogenetic and conservation problems in this group of highly conspicuous New World Monkeys. © 1995 Wiley-Liss, Inc.     

A field observation on color selection by New World sympatric primates,Pithecia pithecia and Alouatta seniculus

This work characterizes differences in selection ofTalisia retusa fruits by two sympatric Neotropical primates,Pithecia pithecia (white-faced sakis) andAlouatta seniculus (red howlers). Color appears to be the criterion by which fruits were selected. Greenish fruits were mainly eaten byPithecia, while yellowish fruits byAlouatta. The characteristics of these primates in relation to seed predation and seed dispersal are discussed in the context of theTalisia retusa fruit color spectrum. Furthermore, a possible differential acquisition of chemical components, like tannins, is hypothetically treated considering the variation in fruit color.     

Serum Nutritional Profiles of Free-Ranging <Emphasis Type="Italic">Alouatta Caraya</Emphasis> in Northern Argentina: Lipoproteins; Amino Acids; Vitamins A,D, and E; Carotenoids; and Minerals

Quantifying circulating nutrient concentrations in sera of free-ranging subjects will help to establish a basis from which we can evaluate the nutritional status and needs of the captive population. We collected serum samples from 26 free-ranging black-and-gold howlers (Alouatta caraya) in San Cayetano forest in northern Argentina. We analyzed them for concentrations of lipoproteins; amino acids; vitamins A, D, and E; carotenoids; and minerals. There are a few significant differences between sexes in concentrations of high-density lipoprotein cholesterol, certain amino acids, vitamin E, lutein + zeaxanthin, and copper. Most nutritional parameters are similar to the ones measured in free-ranging Mexican mantled howlers (Alouatta palliata mexicana) and in captive New World primates (NWPs). Carotenoid, vitamin D, and phosphorus concentrations are the exceptions. Carotenoid concentrations are higher in free-ranging Alouatta caraya than reported for other free-ranging and captive species. Vitamin D concentrations are 14 times greater in the free-ranging black-and-gold howlers than in captive NWPs. Phosphorus concentrations are also higher than expected and higher than typically occur in captive primates, leading to a 1:1.6 calcium:phosphorus ratio. Because we based our study on a small number of free-ranging howlers, additional samples from different regions and throughout the year would better define desirable nutritional parameters for captive howlers.     

Genetic variability in four Alouatta species measured by means of nine DNA microsatellite markers: genetic structure and recent bottlenecks

We used microsatellite DNA to study the population genetics of 4 Alouatta species from Central and South America. Our main findings include the following: (1) A. seniculus had the highest level of microsatellite variability while A. caraya and A. palliata had the lowest mean number of alleles per locus and the lowest expected heterozygosity, respectively; (2) the samples of A. seniculus and A. palliata came from different regions and were not in Hardy-Weinberg equilibrium (HWE) which may indicate a Wahlund effect and differentiated gene pools -- in contrast, A. macconnelli and A. caraya were in HWE; (3) the microsatellite genetic heterogeneity of the 4 Alouatta species was similar to the karyotype divergence found among these Alouatta species; the species pair with the lowest level of heterogeneity (genetic differentiation) was A. seniculus/A. caraya, while the Central American species, A. palliata, was highly differentiated from the other 3 South American species; (4) we recommend the establishment of a conservation plan to help protect A. caraya because the Cornuet and Luikart procedure demonstrated a recent bottleneck for this species.     

Isolation and characterization of microsatellite loci in Amazonian red‐handed howlers Alouatta belzebul (Primates,Plathyrrini)

Ten highly polymorphic microsatellite loci are described for Amazonian red‐handed howlers (Alouatta belzebul), an endemic Brazilian primate species subject to intense hunting pressure. The number of alleles observed in 30 individuals ranged from nine to 20, and observed heterozygosity varied from 0.35 to 0.93. No linkage associations were evident from pairwise comparisons of loci. These microsatellites offer a powerful tool for fine‐scale studies of genetic structure in both captive colonies and wild populations of red‐handed howlers.     

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.     

Ecological niche differences betweenAlouatta palliata andCebus capucinus comparing feeding modes,branch use,and diet

During the wet season, two sympatric species of primates,Alouatta palliata (mantled howlers) andCebus capucinus (white-faced capuchins), were assayed for feeding niche differences through behavioral and habitat use patterns at Refugio de Fauna Silvestre Curu in Costa Rica. Differences in the use of relative diameter and thickness of branches and five different modes of feeding were compared between the species. White-faced capuchins used more manipulative modes of obtaining food, a wider range of arboreal habitat, and had a more diverse diet than mantled howlers. Mantled howlers may be more restricted than white-faced capuchins in arboreal microhabitat use due to their possible need for large support branches during feeding bouts and resting periods. We report that differences in feeding behaviors, diet, and arboreal habitat use seem to play a large role in separating these species niches.     

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.     

Molecular phylogenetics of howler monkeys (Alouatta, Platyrrhini). A comparison with karyotypic data

Molecular phylogenetic analyses of seven Brazilian Alouatta species, based on cytochrome b DNA sequence data were carried out. Parsimony and neighbor joining topologies grouped Alouatta belzebul and A. fusca as sister groups in one clade while another, well-supported clade contained A. seniculus as the most basal offshoot, followed by A. nigerrima as a sister lineage of A. macconnelli/A. stramineus. Estimates of inter-specific sequence divergence were generally low, and estimates of the time of divergence indicated that the main Alouatta lineages emerged during a short evolutionary interval. A comparison with karyotypic data confirmed the molecular topology showing a closer relationship between A. macconnelli and A. stramineus in respect to A. nigerrima. It also showed that the XX/XY sex chromosome system was maintained in several lineages while the X1X2Y/X1X1X2X2 system appeared independently at least three times during the radiation of howler monkeys. Moreover, the X1X2Y1Y2/X1X1X2X2 system might have appeared once or, alternatively, twice and independently.     

Chromosome studies in the red howler monkey, Alouatta seniculus stramineus (Platyrrhini, Primates): description of an X1X2Y1Y2/X1X1X2X2 sex-chromosome system and karyological comparisons with other subspecies

In the red howler monkey, Alouatta seniculus stramineus (2n = 47, 48, or 49), variations in diploid chromosome number are due to different numbers of microchromosomes. Males exhibit a Y;autosome translocation involving the short arm of an individual biarmed autosome. Consequently, the sex-chromosome constitution in the male is X1X2Y1Y2, with X1 representing the original X chromosome, X2 the biarmed autosome (No. 7), Y1 the Y;7p translocation product, and Y2 the acrocentric homolog of 7q. In the first meiotic division, a quadrivalent with a chain configuration can be observed in spermatocytes. Females have an X1X1X2X2 sex-chromosome constitution. Chromosome heteromorphisms were observed in pair 13, due to a pericentric inversion, and pair 19, due to the presence of constitutive heterochromatin. Microchromosomes, which varied in number between individuals, were also heterochromatic. NOR-staining was observed at two separate sites on a single chromosome pair (No. 10). A comparison of A.s. stramineus with A.s. macconnelli shows that these two subspecies have identical diploid chromosome numbers (47, 48, or 49), again due to a varying number of microchromosomes, and that they share a similar sex-chromosome constitution. Their karyotypes, however, are not identical, but can be derived from each other by a reciprocal translocation. Further comparisons with other A. seniculus subspecies reported in the literature indicate that this taxon is not karyologically uniform and that substantial chromosome shuffling has occurred between populations that have been considered to be subspecies by taxonomic criteria based on their morphometric attributes.     

Arboreal Quadrupedism and Forelimb Articular Anatomy of Red Howlers

I describe the patterns of forelimb movements that facilitate adult red howling monkeys (Alouatta seniculus) to advance quadrupedally on arboreal trails in directions ± 45° from the horizontal, the articular surface morphology at the scapulohumeral and elbow joints, and the structure of the trails. Results indicate (1) that red howlers splay their forelimbs when advancing on arboreal trails of mesh-like substrates, but they do not splay them to proceed on unilineal arboreal trails, and (2) that the articular surfaces are adapted to enable the scapulohumeroulnar bony alignments that result in both splayed and nonsplayed forelimb motions. These results have implications for the locomotor habits of several fossil catarrhines.     

Loud calls of adult male red howling monkeys (Alouatta seniculus)

Loud calls of adult male red howlers (Alouatta seniculus) inhabiting a deciduous and semideciduous open woodland site in Venezuela were recorded opportunistically and categorized by ear and sonographically as barks and roars. Five to six different bark syllables were identified as occurring singly or in sequences of doublets and triplets. In barks, spectral energy was concentrated in bands at 350-400 Hz, 900-1,100 Hz, 1,800-2,200 Hz and 3,000-3,500 Hz, but not all higher bands were present in each syllable. Roars appeared sonographically like prolonged barks composed of a pulsated preface, a long legato climax and a brief, fractionated and at times pulsated coda; each part varied internally to the ear and in acoustic structure. All loud calls were of the noisy type (nonharmonic energy over a broad frequency range). Acoustic characteristics of the calls are interpreted in terms of the subserving vocal tract anatomy. I compare loud calls of red howlers with those of mantled (A. palliata) and black (A. caraya) howlers.     

Antipredator Behavior of Brown Howlers Attacked by Black Hawk-eagle in Southern Brazil

In field studies between 2002 and 2004 in southern Brazil, we recorded antipredatory behaviors (N=9) of brown howlers (Alouatta guariba clamitans) under attack by the black hawk-eagle (Spizaetus tyrannus). We observed 2 types of behavioral responses: the descent to the understory followed by the dispersion of the group and immobility and silence. Brown howlers displayed behaviors specific to evading aerial predators, which are similar to the ones in other Neotropical primates.The article is contribution number 1578 of Departamento de Zoologia, Universidade Federal do Paraná     

Cougar Predation on Black-and-Gold Howlers on Mutum Island,Southern Brazil<Superscript>1</Superscript>

Researchers consider predation rates by terrestrial animals to be lower in the case of arboreal primates, particularly among large-bodied species. We recorded the consumption of black-and-gold howlers (Alouatta caraya) by cougars (Puma concolor) as evidence of predation on an island of the upper Paraná River. We collected and processed fecal samples of the felid in 2004 and 2005. We identified items in the laboratory by comparison with museum specimens. We considered each species in a fecal sample as a single occurrence. Based on analysis of the cuticle scale pattern, we identified the felid as cougar. Howlers occurred in 4 out of the 8 fecal samples (40% of the occurrences). In addition to howlers, we also recorded 5 occurrences of agouti (Dasyprocta azarae; 50%) and a small unidentified sigmodontine rodent (10%). The abundance of howlers and the low forest canopy in a successional vegetation might have facilitated the predation of the large primates by a primarily terrestrial predator. The versatility of cougars is corroborated by the consumption of prey species that were abundant in the region and that were available in different forest strata, such as howlers and agoutis.     

Group size in folivorous primates: ecological constraints and the possible influence of social factors

The ecological-constraints model assumes that food items occur in depletable patches and proposes that an increase in group size leads to increased day range due to more rapid patch depletion. Smaller groups become advantageous when an increase in travel costs is not repaid by an increase in energy gained or some other fitness advantage. On the other hand, we also know that group size can be influenced by social factors. Here we contrast the diet and group size of red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) in Kibale National Park, Uganda to consider how ecological and social factors are affecting their group sizes. Subsequently, we examine whether the insights gained from this detailed comparison can provide an understanding of why the social organization and group size of mantled howlers (Alouatta palliata) and black howlers (A. pigra) differ. Two groups of red colobus and two groups of black-and-white colobus were studied over 10 months. Red colobus groups were larger (48 and 24) than black-and-white colobus groups (9 and 6). The two groups of red colobus overlap home ranges with the two groups of black-and-white colobus; 75% and 95% of their home ranges were within red colobuss home range. There was a great deal of similarity in the plant parts eaten by the two species and both species fed primarily on young leaves (red colobus 70%, black-and-white colobus 76%). In terms of the actual species consumed, again there was a great deal of similarity between species. The average dietary overlap among months for the two neighboring groups of red colobus was 37.3%, while the dietary overlap between the red colobus and the black-and-white colobus group that had its home range almost entirely within the home range of the red colobus groups averaged 43.2% among months. If ecological conditions were responsible for the difference in group size between the two colobine species, one would expect the density of food trees to be lower in the home ranges of the black-and-white colobus monkeys, since they have the smaller group size. We found the opposite to be true. Both black-and-white colobus groups had more food trees and the cumulative size of those trees was greater than those in the red colobuss home ranges. We quantify how these differences parallel differences in mantled and black howlers. The average group size for mantled howlers was 12.9 individuals, and for black howlers it was 5.3 individuals. We explore possible social constraints, such as infanticide, that prevent black-and-white colobus and black howlers from living in large groups.This revised version was published online in April 2005 with corrections to the cover date of the issue.     

Effects of Seed Dispersal by Three Ateline Monkey Species on Seed Germination at Tinigua National Park, Colombia

We examined the effect of seed ingestion by three ateline primates: woolly monkeys, Lagothrix lagothricha; spider monkeys, Ateles belzebuth; and, red howler, Alouatta seniculus on germination rates and latency periods of seeds of several plant species in Tinigua National Park, Colombia. We collected dispersed seeds from feces and control seeds from the parental trees and washed them for germination trials. For the majority of plants, dispersed seeds germinated as well or better than control seeds did. Although spider monkeys depend more heavily on fruits than the other monkey species do, they were not more efficient than howlers or woolly monkeys at improving germination rates. A considerable proportion of the seeds dispersed by howlers and woolly monkeys showed reduced latency periods to germination, but spider monkeys showed less effect on reducing germination time. This result may be related to longer gut retention times, but such a trend has not been observed in other primate species. We conclude that, like many other primates, ateline monkeys are effective seed dispersers in terms of their effects on the seeds they swallow because they rarely decrease their germination rates. We discuss problems that make interspecific comparisons difficult, such as inappropriate control seeds and differences associated with germination substrates, and we stress the importance of studying other components of seed dispersal effectiveness.     

Skeletal Pathologies in a Population of Alouatta palliata: Behavioral, Ecological, and Evolutionary Implications

We examined the pathological conditions in a sample of 200 skulls of Alouatta palliata recovered from Barro Colorado Island (BCI), Panama, to investigate the prevalence of disease and injury in a free-ranging monkey population. Forty-five individuals (22.5%) have some type of nondental pathological condition, indicating that illness and injury are relatively common in this population. Ten individuals, all older adult males, exhibit clear signs of antemortem trauma in the form of healed fractures. We attribute the trauma primarily to fighting, and its frequency (16.4% of adult males) contradicts previous assertions that BCI howlers are nonaggressive. Nine of the 37 scorable immature individuals (24%) have signs of a larval infestation, supporting the suggestion that ectoparasites play an important role in BCI howler mortality. Other pathological conditions in the sample include shifted muscle attachments, periostitis, arthritis, neoplasm, periapical abscesses, and facial deformity, as well as various dental abnormalities.