[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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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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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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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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Non-metric features in the ulna of Aegyptopithecus, Alouatta, Ateles, and Lagothrix.
A comparison of the non-metric features of the ulnar fragment (YPM 23940) referred to Aegyptopithecus zeuxis with those in the same bone of Alouatta, Ateles, and Lagothrix -- the three living taxa whose ulnae most closely resemble that of the fossil -- reveals that the closest similarities of the fragment are with the ulna of Alouatta.
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Genetic diversity in black howler monkeys (Alouatta pigra) from Belize.
To assess the level of genetic variation in a threatened black howler monkey (Alouatta pigra) population, we examined 36 allozyme loci and restriction fragment profiles of mitochondrial DNA (mtDNA). Mean heterozygosity at allozyme loci was only 0.021 and 5.6 percent of the loci were polymorphic. Analyses of mtDNA also revealed low genetic diversity compared with other primates. F-statistics revealed no significant genetic heterogeneity among troops within the Bermudian Landing preserve, but did indicate a deficiency of heterozygotes at one of the two loci. We explore several explanations for this result, which is unexpected in a socially structured primate. Low genetic diversity in this population may reflect its history of demographic bottlenecks.
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Behavioral thermoregulation in a sexually and developmentally dichromatic neotropical primate, the black-and-gold howling monkey (Alouatta caraya).
Behavioral thermoregulation in primates may provide a means for the conservation of heat during periods of low ambient temperature and/or food shortage as well as a way to dissipate heat under hot conditions. This article focuses on behavioral thermoregulation in a sexually dichromatic primate, the black-and-gold howling monkey (Alouatta caraya). Two models have been proposed to explain the evolution of sexual dichromatism in this species: thermoregulation and sexual selection. Five hypotheses associated with thermoregulatory behaviors are tested. These are as follows: (1) energy-conserving postures are used mainly under low ambient temperatures; (2) sunny resting places are selected during periods of low temperature; (3) exposure of the less-insulated ventral region to sunlight decreases with increasing temperature; (4) black-colored adult males use energy-conserving postures, sunny places, and exposure of the ventral region to sunlight less frequently than do blonde-colored adult females; and (5) smaller individuals use energy-conserving postures, sunny places, and exposure of the ventral region to sunlight in significantly greater frequency than do larger individuals. Over a 12-month period, behavioral data were collected on a free-ranging habituated group of 15-17 howlers of all age-sex classes. Ambient temperature was measured each hour. The results indicate that during resting, howlers showed a consistent use of heat-conserving postures, showed a preference for sunny places, and exposed their ventral region to sunlight under low ambient temperatures. A preference for shady places, heat-dissipating postures, and exposure of the back were observed under high ambient temperatures. Despite sex differences in adult color patterns and differences in size between age classes, no significant age or sex differences in thermoregulatory behaviors were detected. Failure to confirm a thermoregulation model implies that sexual selection may be responsible for sexual dichromatism in this species.
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Anesthesia of wild red howler monkeys (Alouatta seniculus) with medetomidine/ketamine and reversal by atipamezole.
Wild red howler monkeys (Alouatta seniculus) were translocated during the flooding of the forest at a hydroelectric dam site in French Guiana. For a variety of minor clinical procedures, 96 monkeys were anesthetized with various intramuscular injections of combinations of medetomidine and ketamine. The howler population was composed of healthy animals (42 males and 54 females) of various ages. Medetomidine (150 micrograms/kg) associated with ketamine (4 mg/kg) gave the best results and was used on 63 animals. The injection rapidly resulted in complete immobilization with good to excellent myorelaxation. The induction stage was quiet, with absence of both corneal and pedal withdrawal reflexes in 57 animals after 2.9 +/- 1.4 min. Six animals required an additional injection. Rectal temperature and respiratory and heart rates decreased during anesthesia, whereas relative oxyhemoglobin saturation increased. One death occurred during anesthesia. One abortion and one death also occurred the day following anesthesia but were more probably a result of capture stress. Atipamezole given i.m. at a dose of five times the medetomidine dose 38.4 +/- 8.0 min after the anesthetic injection led to standing recovery in 7.1 +/- 4.5 min. Spontaneous recovery occurred in 17 animals before the atipamezole injection after an average of 30.6 +/- 9.6 min. Total recovery time was shorter in young animals. Medetomidine/ketamine induced good myorelaxation and provided considerably shortened immobilization duration, which are two notable advantages for field studies. We recommend this association for short procedures including minor surgery in red howler monkeys.
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Effects of black howler monkey (Alouatta caraya) seed ingestion on insect larvae.
Fig (Ficus monckii) and laurel (Ocotea puberula) seeds were obtained from Alouatta caraya feces (ingested seeds) and from trees (noningested) in northeastern Argentina. Seeds were examined to detect the presence (infested) or absence (noninfested) of larvae. Sixty percent (N = 315) of noningested fig seeds were galls with insect larvae inside, while 23% (N = 331) were encountered in the ingested group. Eighty-two percent (N = 28) of noningested laurel seeds were infested, and only 19% (N = 63) of ingested seeds were infested. According to the present data, the insects' larvae are digested by howlers intaking animal protein, but the laurel seeds were not destroyed.
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