[Natural infection of the monkey Alouatta seniculus straminea, and Alouatta seniculus artroidea by Trypanosoma mycetae in Venezuela].
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Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta.
We take advantage of the broad distribution of howler monkeys from Mexico to Argentina to provide a historical biogeographical analysis on a regional scale that encompasses the entire Neotropics. The phylogenetic relationships among 9 of the 10 recognized Alouatta species were inferred using three mitochondrial and two nuclear genes. The nuclear gene regions provided no phylogenetic resolution among howler monkey species, and were characterized by very low levels of sequence divergence between Alouatta and the Ateles outgroup. The mtDNA genes, on the other hand, produced a well-resolved phylogeny, which indicated that the earliest split among howler monkeys separated cis- and trans-Andean clades. Eight monophyletic mtDNA haplotype clades were identified, representing six named species in South America, including Alouatta seniculus, Alouatta sara, Alouatta macconelli, Alouatta caraya, Alouatta belzebul, and Alouatta guariba, and two in Mesoamerica, Alouatta pigra and Alouatta palliata. Molecular clock-based estimates of branching times indicated that contemporary howler monkey species originated in the late Miocene and Pliocene, not the Pleistocene. The causes of Alouatta diversification were more difficult to pin down, although we posit that the initial cis-, trans-Andean split in the genus was caused by the late Miocene completion of the northern Andes. Riverine barriers to dispersal and putative forest refuges can neither be discounted nor distinguished as causes of speciation in many cases, and one, the other or both have likely played a role in the diversification of South American howler monkeys. Finally, we estimated the separation of Mesoamerican A. pigra and A. palliata at 3Ma, which corresponds to the completion date of the Panama Isthmus promoting a role for this earth history event in the speciation of Central American howler monkeys.
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Extensive enlargement of the maxillary sinus in Alouatta caraya (mammalia, primates, cebidae): an allometric approach to skull pneumatization in Atelinae.
In contrast to the paranasal sinuses of Old World monkeys and hominoids, little information is available about the paranasal sinuses of New World monkeys. Because this information is crucial in order to draw further conclusions about the evolution and biological role of skull pneumatization, this study investigates the morphology of the paranasal sinuses in adult black-and-gold howler monkeys (Alouatta caraya). Volumes of the paranasal sinuses were calculated using computer software (SURFdriver or Allegro) from serial coronal CT scans of 20 skulls of both sexes. Skull pneumatization in A. caraya is more complex than in other higher primates. In both sexes, the maxillary sinus (MS) is the only pneumatic cavity and enlarges regularly into neighboring bones such as the frontal bone and the basisphenoid. The resulting pansinus is often partitioned by several vertical septa. As in most external cranial dimensions, mean MS volume of A. caraya (male 4.08 cm(3); female 2.00 cm(3)) shows significant sexual dimorphism. Reduced major axis regression analysis between MS volume and different cranial dimensions for A. caraya (and for available data from other platyrrhines) suggests a distinct association for this group, with Alouatta having one of the largest pneumatic cavities. The combination of this unusual expansion of the MS of Alouatta and the occurrence of distinct septa within the sinus may be a consequence of the distinct skull architecture of Alouatta.
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Feeding ecology of the black howler monkey (Alouatta pigra) in northern Belize.
We studied the feeding ecology of the black howler monkey (Alouatta pigra) from March 1994 to April 1995 in the Community Baboon Sanctuary in northern Belize, Central America. Activity and diet composition were recorded using continuous focal animal sampling. Diet composition was compared with the relative abundance of plant parts eaten by the howlers within the study site. The study animals spent an average of 24.4% of their time feeding, 61.9% resting, and approximately 9.8% traveling. In contrast to previously published reports on A. pigra, we found the diet composition to be similar to that of other Alouatta species (conforming to the folivore/frugivore profile), with 41% of feeding time spent eating fruit, 45% foliage, and 11% flowers. This contrast may indicate a wide degree of dietary flexibility that allows A. pigra to inhabit a variety of habitat types. We suggest that a high level of resource abundance throughout the year makes the Community Baboon Sanctuary excellent habitat for Alouatta pigra.
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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.
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The phylogeny of howler monkeys (Alouatta, Platyrrhini): reconstruction by multicolor cross-species chromosome painting.
We performed multidirectional chromosome painting in a comparative cytogenetic study of the three howler monkey species Alouatta fusca, A. caraya and A. seniculus macconnelli (Atelinae, Platyrrhini) in order to reconstruct phylogenetic relationships within this genus. Comparative genome maps between these species were established by multicolor fluorescence in-situ hybridization (FISH) employing human, Saguinus oedipus and Lagothrix lagothricha chromosome-specific probes. The three species included in this study and previously analyzed howler monkey species were subjected to a phylogenetic analysis on the basis of a data matrix comprised of 98 discrete molecular cytogenetic characters. The results revealed that howler monkeys represent the genus with the most extensive karyotype diversity within Platyrrhini so far analyzed with high levels of intraspecific chromosomal variability. Two different multiple sex chromosome systems were identified. The phylogenetic analysis indicated that Alouatta is a monophyletic clade which can be derived from a proposed ancestral Atelinae karyotype of 2n = 62 chromosomes by a chromosome fusion, a fission, a Y-autosomal translocation and a pericentric inversion. Following these suggestions, the genus Alouatta can be divided into two distinct species groups: the first includes A. caraya and A. belzebul, the second A. s. macconnelli, A. sara, A. s. arctoidea and A. fusca.
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Cytochrome b polymorphisms and population structure of two species of Alouatta (Primates).
We carried out a phylogenetic and population study in Alouatta caraya and Alouatta belzebul based on cytochrome b DNA sequence data. Maximum Parsimony and Median-Joining analyses grouped A. caraya from different localities showing a population structure in accordance with geographic distribution. The relation between A. caraya haplotypes could be explained with respect to the species range in the Cerrado, one of the most ancient morphoclimatic domains of South America, and the Chaco. Conversely, A. belzebul from the Amazonas and Atlantic forests grouped in a paraphyletic arrangement without an evident geographic pattern. Recent geologic events resulting in the separation of A. belzebul might explain why these geographically distant groups shared similar haplotypes and why ancestral polymorphisms might have been maintained in this species. Time of divergence estimates indicated that the splitting of the Alouatta lineage leading to A. caraya occurred some 4.58 MYA while the lineage leading to A. belzebul emerged 4.14 MYA.
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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 arctoidea seven 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.
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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.
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Parasites of free-ranging black howler monkeys (Alouatta pigra) from Belize and Mexico.
Parasites are important members of the ecological web within which an animal lives, and can be used as indicators of ecosystem health. However, few baseline parasitological data are available for free-ranging animals, particularly for the black howler monkey (Alouatta pigra). In this study a total of 283 fecal samples were collected from 50 individually identified A. pigra during 2003 and 2004 and examined for parasites. The samples were processed using standard quantitative centrifugation concentration techniques, with sugar and zinc sulfate used as flotation media. The slides were examined using bright-field and phase microscopy. Antigen capture enzyme-linked immunosorbent assays (ELISAs) were used to detect protozoa. Four parasites were detected: 1) Controrchis biliophilus (Dicrocoeliidae), 2) Trypanoxyuris minutus (Oxyuridae), 3) Giardia sp. (Hexamitidae), and 4) Entamoeba sp. (Endamoebidae). Controrchis biliophilus was detected in 80% (wet season) and 81% (dry season) of the A. pigra samples; Trypanoxyuris minutus was detected in 8% (wet season) and 27% (dry season) of samples; and Giardia sp. was detected in 40% (wet season) and 27% (dry season) of samples. For the first time, DNA from Giardia sp.-positive fecal samples was extracted from A. pigra. Alouatta pigra individuals that lived near human settlements in Belize were infected with Giardia duodenalis (syn. G. lamblia, G. intestinalis) Assemblages A and B. These results suggest that G. duodenalis is transmitted from people and/or domestic animals to A. pigra.
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Use of traps to capture black and gold howlers (Alouatta caraya) on the Islands of the upper Paraná River, Southern Brazil.
Howlers (genus Alouatta) are widely captured with the use of anesthetic projectiles; however, no capture protocol involving the use of traps has been described to date. In the present study we describe the first efficient capture program for black and gold howlers (Alouatta caraya) using traps, which was implemented on the islands of the upper Paraná River in southern Brazil. We constructed two trap models with either manual or automatic activation (trap A with two entrances and guillotine-type doors; trap B with one entrance and a guillotine-type door). The traps were suspended in the canopy by means of vertical climbing techniques, and were baited regularly and abundantly with bananas and mangoes. We captured 70 howlers (86% using manual activation and 14% using automatic activation) on four different islands. We restrained 41 of these animals and measured their body mass, which averaged 5.30 kg+/-1.79. Given our results, we suggest that the system described in the present study represents an alternative capture program for howlers in areas that have low food diversity and no other mammal species that will compete for the bait, as has been observed in riparian environments, islands, and forest fragments.
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Mechanical defenses in leaves eaten by Costa Rican howling monkeys (Alouatta palliata).
Primate species often eat foods of different physical properties. This may have implications for tooth structure and wear in those species. The purpose of this study was to examine the mechanical defenses of leaves eaten by Alouatta palliata from different social groups at Hacienda La Pacifica in Costa Rica. Leaves were sampled from the home-ranges of groups living in different microhabitats. Specimens were collected during the wet and dry seasons from the same tree, same plant part, and same degree of development as those eaten by the monkeys. The toughness of over 300 leaves was estimated using a scissors test on a Darvell mechanical tester. Toughness values were compared between social groups, seasons, and locations on the leaves using ANOVA. Representative samples of leaves were also sun-dried for subsequent scanning electron microscopy and energy dispersive x-ray (EDX) analyses in an attempt to locate silica on the leaves. Both forms of mechanical defense (toughness and silica) were found to be at work in the plants at La Pacifica. Fracture toughness varied significantly by location within single leaves, indicating that measures of fracture toughness must be standardized by location on food items. Monkeys made some food choices based on fracture toughness by avoiding the toughest parts of leaves and consuming the least tough portions. Intergroup and seasonal differences in the toughness of foods suggest that subtle differences in resource availability can have a significant impact on diet and feeding in Alouatta palliata. Intergroup differences in the incidence of silica on leaves raise the possibility of matching differences in the rates and patterns of tooth wear.
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Taste areas of the plica sublingualis of Alouatta and Aotus (Primates, Platyrrhini).
A conspicuous accumulation of taste buds occurs in the rostral part of the plica sublingualis ("frenal lamella") of Alouatta and Aotus forming taste areas (area gustatoria) superficially situated in the oral mucous membrane. They are found in close vicinity to the orifices of the sublingual salivary glands, but are lacking in the aboral part of the plica sublingualis. They do not occur in all primate species studied. A taste area does not projects above the surface of the surrounding tissue like a papilla. The taste buds open not in crypts of furrows of the oral mucosa, but directly into the spatium sublinguale of the oral cavity proper. In the anterior part of the cavum oris proprium different kinds and very differentiated qualities of sensoral information are perceived (touch, olfaction, temperature). It is conceivable that the taste areas play an important role in perceiving fresh saliva, together with the other sensorial structures in this part of the mouth. This problem can be solved experimentally and by behavioral studies, In addition to its topographical relation to the tongue, the organon sublinguale of Callicebus is structurally very similar to the plica sublingualis of Aotus and Alouatta. Since a sublingua does not occur in New World monkeys, it can be concluded that this organ represents a plica sublingualis which became adherent to the undersurface of the tongue.
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Meiotic behavior of the X1X2Y1Y2 quadrivalent of the primate Alouatta caraya.
A multiple sex chromosome system was found in three unrelated individuals of the primate Alouatta caraya. This mechanism is originated by a translocation between the Y chromosome and one of the autosomes (A7). Mitotic karyotypes show two small, acrocentric chromosomes (AY and YA), which are the translocation products. In metaphase I of male meiosis, there is a very long chain quadrivalent in which the order of the element is: X-YA-A7-AY. Segregation in the quadrivalent is alternate and gives balanced products. Synaptonemal complex karyotypes at pachytene show the structure of the quadrivalent made by the four axes. There is a slight difference in the relative length of AY and YA and the kinetochore of A7 aligns with that of AY. The synaptic pattern and changes in the quadrivalent during pachytene are described. Thin sections of the quadrivalent body show that the chromatin packing in the sex chromosome region is different from that of the autosomal region. This X1X2Y1Y2/X1X1XX2 sex chromosome system may be extended among other members of the genus Alouatta.
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Survey of the black howler monkey, alouatta pigra, population at the Mayan site of Palenque, Chiapas, Mexico.
A survey of the population of the black howler monkey (Alouatta pigra) present at the Mayan site of Palenque was conducted during 2000. A total of 911 man/hours, spread over 112 days were spent surveying the 600 ha area of pristine forest at the site for howler troops. We detected the presence of 136 individuals of which 131 were members of 20 troops, the rest were 3 solitary adult males and 2 adult males travelling as a pair. Ecological density was estimated at 23 individuals/km(2). Mean troop size was 7.0 individuals and it ranged from 2 - 12 individuals; 60% of the troops were multimale. All sighting of howler monkeys were in evergreen rain forest and 75% were in trees > or = 20 m in height. The reported densities and mean troop size are higher than those reported for the species in Guatemala and in central Quintana Roo, Mexico. The vegetation of the forest contains tree species reported to be used by species of Alouatta in the Moraceae, Sapotaceae, Leguminosae, and Lauraceae plant families. Protection of a large perimeter area (ca 1700 ha) around the archeological site by the Mexican government ensures the conservation of the forest and of the black howler monkey population present at the site.
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Interspecific interaction and predator avoidance behavior in response to tayra (Eira barbara) by mantled howler monkeys (Alouatta palliata).
This paper reports the response of one howler monkey group (Alouatta palliata) to a group of potential predators, the tayra (Eira barbara). The apparently successful predator avoidance behavior of the monkeys was recorded in detail. We observed a group of four adult tayras moving around the Alouatta group displaying a species-typical aggressive behavioral pattern. The two adult females of the howler group successfully chased the tayras away by repeatedly moving closer to the mustelids and even following them until the predators moved off.
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A field observation on color selection by New World sympatric primates, Pithecia pithecia and Alouatta seniculus.
This work characterizes differences in selection of Talisia retusa fruits by two sympatric Neotropical primates, Pithecia pithecia (white-faced sakis) and Alouatta seniculus (red howlers). Color appears to be the criterion by which fruits were selected. Greenish fruits were mainly eaten by Pithecia, while yellowish fruits by Alouatta. The characteristics of these primates in relation to seed predation and seed dispersal are discussed in the context of the Talisia retusa fruit color spectrum. Furthermore, a possible differential acquisition of chemical components, like tannins, is hypothetically treated considering the variation in fruit color.
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Geophagy as a correlate of folivory in red-handed howler monkeys (Alouatta belzebul) from eastern Brazilian Amazonia.
Howler monkeys, Alouatta spp., are the most folivorous of neotropical primates (Platyrrhini), although Amazonian red-handed howlers (Alouatta belzebul) are relatively frugivorous. The feeding ecology of a free-ranging group of A. belzebul was monitored at a site in eastern Brazilian Amazonia over a tenmonth period (November 1997 to August 1998). The first half of the study period encompassed the peak of the wet season, during which the study group's diet was predominantly frugivorous (scan sample records: 53.5% fruit, 40.8% leaves), and the second half, the transition from wet to dry season, characterized by a marked shift to folivory (18.9% fruit, 77.9% leaves). This shift was accompanied by a marked increase in mature, as opposed to flush leaves, which are relatively rich in secondary compounds. Ingestion of soil from termitaria was recorded on a total of 26 occasions, all of which occurred during the second half of the study period. Soil from termitaria was relatively rich in elements such as Ca and Na and in organic carbon, in comparison with that from the forest floor. The extent to which the monkeys ingested soil for their mineral supplements, or as an aid for the digestion of leaves, in particular the absorption of secondary compounds, remains unclear. The marked correlation with the observed patterns of folivory suggests that the latter function may have been the primary motive for geophagy in this species.
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