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Fine structure and meiotic behaviour of the male multiple sex chromosomes in the genus Alouatta.

The meiotic cytology and fine structure of the sex multiples in males from two species of the genus Alouatta are presented and compared with descriptions from other species of this genus. As shown in pachytene by synaptonemal complex analysis and in metaphase I by spreading, there is a quadrivalent in male meiosis in A. caraya, which is formed by an X(1)X(2)Y(1)Y(2) complex, while in A. palliata there is a trivalent formed by an X(1)X(2)Y(1) complex. Chromosome painting with human probes shows that A. caraya sex multiples share the same components as those of A. seniculus sara and A. seniculus arctoidea. However, as shown here for A. palliata and by others in A. fusca, there are differences among the multiples of some species. It is shown that in this genus there are several varieties of sex multiples that share some features, and that the origin of these multiples is most probably a primitive development in the genus Alouatta.

Alouatta↗

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.

Alouatta↗

Retrospective evaluation of renal disease in captive black howler monkeys (Alouatta caraya).

Six of 15 (40%) inactive medical records of adult black howler monkeys (Alouatta caraya) at one zoological institution included either a pre- or postmortem diagnosis of renal disease. In these six cases, significantly abnormal hematologic and serum chemistry values were reported at onset of azotemia, onset of clinical signs, and at euthanasia. Average age of onset of azotemia was 14.8 +/- 2.9 yr, with clinical signs of disease noted at 17 +/- 4.7 yr. In four of the cases (66.6%), azotemia was documented earlier than the onset of clinical signs of renal disease. Average duration of clinical disease was 2.83 +/- 1.6 yr, with an average age at euthanasia of 18 +/- 4.7 yr. Chronic tubulointerstitial nephritis with secondary glomerular sclerosis was present in all cases. Thirteen of an additional 20 institutions in the United States that have held Alouatta caraya responded to a survey for prevalence of renal disease. These institutions showed a lower prevalence (15.1%) of renal disease in complete, inactive records, a higher prevalence of glomerulonephritis, and similar significant clinicopathologic values.

Age of Onset↗

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.

Alleles↗

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.

Alouatta↗

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.

Alouatta↗

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.

Alouatta↗

Craniometric variation in a population of mantled howler monkeys (Alouatta palliata): evidence of size selection in females and growth in dentally mature males.

A large body of work on monkey cranial metrics (involving conclusions about interspecific variation, sexual dimorphism, and ontogeny) depends on the assumptions that growth effectively ceases with dental maturity and that intraspecific variation is negligible. We test these assumptions by examining variation in 39 measurements of 166 dentally mature Alouatta palliata skulls from animals found dead on Barro Colorado Island (BCI), Panama. We also investigate whether this population is under size-based selection, since our found-dead sample reflects the natural mortality in this population. The sample was divided into three age stages by occlusal wear (A-C, least to most wear). Female stage A means are significantly smaller than female stage B means for three cranial measures. Female stage B means are significantly smaller than female stage C means for five cranial measures. Male stage A means are significantly smaller than male stage B means for 21 cranial measures. Multivariate analyses confirm this trend of expansion between adult age stages. The dental metric and suture closure data suggest that the cranial expansion in females is due to size-based selection, while the cranial expansion in males is due to significant growth after dental maturity. Sexual dimorphism ratios are highly variable across different samples of A. palliata, indicating that dimorphism varies between populations of this species. These results provide insight into the selective forces operating on the BCI howlers and challenge the validity of the many studies which pool subspecies and assume growth ceases with maturity.

Aging↗

Urinary progesterone in free-ranging red howler monkeys (Alouatta seniculus): preliminary observations of the estrous cycle and gestation.

The goals of this study were to develop and validate a radioimmunoassay (RIA) for measurement of unconjugated progesterone (P) concentrations in the urine of red howler monkeys (Alouatta seniculus) and to use urinary P profiles to characterize the reproductive cycle of this species. Analysis of P profiles from two females provided a preliminary estimate of the length of the estrous cycle (mean days +/- S.E.M. = 29.5 +/- 1.5; n = 2), and indicated that one female red howler copulated throughout two apparent estrous cycles. Urinary P concentrations during two confirmed pregnancies (211.8 +/- 29.7 ng P/ml) were higher (P < 0.05) than during the luteal phase (77.4 +/- 10.6 ng P/ml; n = 4) of the cycle.

Alouatta↗

Population of the black howler monkey (Alouatta pigra) in a fragmented landscape in Palenque, Chiapas, Mexico.

Little is known about the population characteristics of Alouatta pigra under conditions of forest fragmentation-information that is important to understanding its tolerance to habitat loss. In this work we present data on forest loss and on troop size, age, and sex composition for a population of black howler monkeys existing in the fragmented landscape surrounding the Mayan site of Palenque, Chiapas, Mexico. Two aerial photos (1:70,000) of the study area (261 km(2)) taken in 1984 and 2001 were examined to assess forest loss. Between June and December 2001 and January and March 2002 we surveyed 44 forest fragments for the presence of howler monkeys. Examination of aerial photos showed that 33% of the forest present in 1984 had disappeared by 2001, and detected an increment in the number of forest fragments present in the landscape. We discovered a total of 115 howler monkeys living in 22 of the 44 forest fragments studied, of which 107 were members of 18 troops. The rest were solitary males or small groups of males living in isolated forest fragments. Troop size ranged from two to 15 individuals (mean 5.9+3.0 ind). 31% and 15% of individuals in the troops were juveniles and infants, respectively, suggesting continued reproductive activity. Howler monkey troops in the forest fragments were on average smaller (5.9+/-3.0 ind) than troops in the nearby protected forest of the Mayan site (7.0+/-2.8 ind). The mean density of howlers in the forest fragments was 119+/-82.9 ind/km(2). The establishment of corridors is suggested as a possible conservation scenario for the fragmented howler population investigated, and as a conservation measure to connect this population with the howler population found in the protected forest of the Mayan site.

Age Distribution↗

Ranging pattern and use of space in a group of red howler monkeys (Alouatta seniculus) in a southeastern Colombian rainforest.

We studied a group of red howler monkeys (Alouatta seniculus) bordering a lake in an eastern Colombian Amazon rainforest for 10 months. The group used an area of 182 ha located mainly on Pleistocene terrace forest and had no overlap with other howler home ranges. Home range use varied through the year as a consequence of fruit and leaf abundance. For example, during the fruit scarcity season the group used an area of flooded forest nearly exclusively, indicating that at least for a portion of the year they are habitat specialists. Two areas intensively used by the group were identified, representing 17.6 % of the home range, and within which 56.9 % of the feeding trees were located. Overall density of feeding trees within the group's home range was very low (1.12 trees/ha). Home range size, as well as mean length of daily ranges (1,150 m), is the largest reported for this species to date, and it is likely a consequence of the diminished productivity of the plant communities on poor soil. Our results give an interesting example of the ranging behavior of this primate, which clearly differs from previous descriptions of red howlers.

Alouatta↗

Observed case of infanticide committed by a resident male central American black howler monkey (Alouatta pigra).

Although infanticide has been witnessed in other species of howler monkey, and has been inferred for Alouatta pigra, an observed case of infanticide has not previously been recorded for this species. Here we describe the killing of a 2-week-old infant by the resident male of a small social group in southern Belize. The infanticide was witnessed as part of an intensive observational study that began in January 2003. The male was known to have resided in the group for at least 4 months, but it is not known whether he was the father of the infant. The literature proposes three main explanations for infanticide: two adaptive hypotheses (sexual selection and resource competition), and one nonadaptive hypothesis (social pathology). Individual cases of infanticide such as this one are important for comparative purposes, but when examined on their own they are difficult to interpret in relation to established theoretical frameworks. The data presented here show some consistency with the sexual-selection and resource-competition hypotheses, but the lack of critical information (i.e., as to paternity) makes it impossible to draw firm conclusions.

Alouatta↗

Observation of parturition in the Mexican mantled howler monkeys (Alouatta palliata) on the Island of Agaltepec, Veracruz State, Mexico.

We observed a birth in a group of Mexican mantled howler monkeys (Alouatta palliata) living under semi-free-ranging conditions on Agaltepec Island, Catemaco, Veracruz, Mexico. Although we could not quantify contractions, we were able to record a complete description of the sequence of events that resulted in a successful birth. Nine minutes passed from the release of the amniotic fluid to the total emergence of the infant. Although all group members were resting relatively close to the female when the birth occurred, none approached her until the postpartum period. Only then did several individuals briefly inspect the newborn and then resume their foraging activities.

Alouatta↗

Biogeographical and floristic predictors of the presence and abundance of mantled howlers (Alouatta palliata mexicana) in rainforest fragments at Los Tuxtlas, Mexico.

This research focuses on identifying the principal habitat characteristics that influence the presence and abundance of mantled howlers in forest fragments. We provide information on the demography of several fragmented Alouatta palliata mexicana subpopulations at Los Tuxtlas, Mexico, and relate this to the biogeographical and floristic characteristics of the forest fragments inhabited. The most important habitat characteristics related to the presence and abundance of howlers in the fragments were fragment size and floristic diversity. On the other hand, some evidence suggests that given the conditions under which howlers in our study area live (i.e., small and degraded fragments with high densities), secondary vegetation may be beneficial for the survival of the howlers. Finally, we discuss the possibility that the very low immature-to-female ratio (IFR) in the groups, and the lack of juveniles found in many of the study groups may be due to high mortality rates in immatures. A reduction in food availability because of the high population densities of these groups may be responsible for this process.

Alouatta↗

Dental topography and molar wear in Alouatta palliata from Costa Rica.

Paleoprimatologists depend on relationships between form and function of teeth to reconstruct the diets of fossil species. Most of this work has been limited to studies of unworn teeth. A new approach, dental topographic analysis, allows the characterization and comparison of worn primate teeth. Variably worn museum specimens have been used to construct species-specific wear sequences so that measurements can be compared by wear stage among taxa with known differences in diet. This assumes that individuals in a species tend to wear their molar teeth in similar ways, a supposition that has yet to be tested. Here we evaluate this assumption with a longitudinal study of changes in tooth form over time in primates. Fourteen individual mantled howling monkeys (Alouatta palliata) were captured and then recaptured after 2, 4, and 7 years when possible at Hacienda La Pacifica in Costa Rica between 1989-1999. Dental impressions were taken each time, and molar casts were produced and analyzed using dental topographic analysis. Results showed consistent decreases in crown slope and occlusal relief. In contrast, crown angularity, a measure of surface jaggedness, remained fairly constant except with extreme wear. There were no evident differences between specimens collected in different microhabitats. These results suggest that different individual mantled howling monkeys wear their teeth down in similar ways, evidently following a species-specific wear sequence. Dental topographic analysis may therefore be used to compare morphology among similarly worn individuals from different species.

Alouatta↗

Coat color and biochemical variation in Amazonian wild populations of Alouatta belzebul.

A comparative study of 13 blood genetic systems and pelage color variation was performed in four wild populations of Alouatta belzebul. The animals from the west bank of the Tocantins River showed less color variation than those from the east bank, as well as less than those from Tocantins Island. The blood genetic markers, however, revealed an opposite pattern of variation. A previously undescribed morphological variant (completely red) was observed in one specimen of the east bank, where pelage color of the local population varied from completely black to completely red. Levels of heterozygosity and inter- and intralocus variances for the blood systems are compared with those observed in five other species of New World primates.

Alleles↗

Dental microwear in live, wild-trapped Alouatta palliata from Costa Rica.

One problem with dental microwear analyses of museum material is that investigators can never be sure of the diets of the animals in question. An obvious solution to this problem is to work with live animals. Recent work with laboratory primates has shown that high resolution dental impressions can be obtained from live animals. The purpose of this study was to use similar methods to begin to document rates and patterns of dental microwear for primates in the wild. Thirty-three Alouatta palliata were captured during the wet season at Hacienda La Pacifica near Canas, Costa Rica. Dental impressions were taken and epoxy casts of the teeth were prepared using the methods of Teaford and Oyen (1989a). Scanning electron micrographs were taken of the left mandibular second molars at magnifications of 200x and 500x. Lower magnification images were used to calculate rates of wear, and higher magnification images were used to measure the size and shape of microwear features. Results indicate that, while basic patterns of dental microwear are similar in museum samples and samples of live, wild-trapped animals of the same species, ecological differences between collection locales may lead to significant intraspecific differences in dental microwear. More importantly, rates of microwear provide the first direct evidence of differences in molar use between monkeys and humans.

Alouatta↗

Experimental test of female black howler monkey (Alouatta Pigra) responses to loud calls from potentially infanticidal males: effects of numeric odds, vulnerable offspring, and companion behavior.

During group defense, the contribution of female black howler monkeys (Alouatta pigra) may help deter male intruders; however, their involvement during natural intergroup encounters is facultative. Experimental playback trials simulating potentially infanticidal males were used to examine whether a female's reproductive investment and/or her group's relative fighting ability would influence her participation in loud call displays. Female howlers never responded to recordings without alpha male accompaniment, but their response patterns did not simply mimic his. For example, unlike alpha males, females with small, vulnerable offspring were no more likely than females without infants to participate in howling displays during playback trials. Further, although females without any small infants in their group got closer to speakers than females living in groups with small infants, males did not respond in the same way. To artificially simulate different "numeric odds" scenarios, recordings of one or three howling males (simulated intruders) were broadcast to females living in groups with 1-3 resident males. Responses were consistent with the hypothesis that females assessed intergroup fighting ability. As in alpha males, the weakest female responses occurred when the numeric odds were against their group. However, whereas alpha males participated most when numeric odds were in their favor, females had the most intense approach responses when the number of defending and intruding males was equal. Females appeared to use a cost-effective strategy, reserving their assistance for when their participation could have the greatest impact.

Alouatta↗