Coprological Surveys of Alouatta pigra at Two Sites in Belize

Fecal samples were collected from black howler monkeys (Alouatta pigra) in north central Belize and analyzed for evidence of endoparasite life stages. At least six types of endoparasites were found in Alouatta pigra fecal samples collected in the Lamanai Archaeological Reserve and the Community Baboon Sanctuary in 1999. These include a digenean trematode, an oxyurid nematode, a strongyle-type nematode, an ascarid presumed to be Ascaris sp., Entamoeba coli and Iodamoeba bütschlii. Higher trematode prevalence was found in adult Alouatta pigra compared to juveniles and higher prevalence of nematode larvae in all animals was found in the wet season compared to the dry season.     

Shifts in Social Structure of Black Howler (Alouatta pigra) Groups Associated with Natural and Experimental Variation in Population Density

We examined variation in the group structure of black howlers (Alouatta pigra) using the adult composition of 48 social groups. We compared the structure of groups at 5 sites with different population densities and variation in group structure over time with rising population density. In addition, we examined changes in the group structure of monkeys that were translocated from an area of high population density to an area with a much lower population density. We found at low population densities, groups comprised either heterosexual pairs or a single male with two females. At high population densities groups tended to be multimale and often contained >2 adult females. We suggest the relative costs and benefits of dispersal by maturing adults varies with population density, and in Alouatta pigra results in a shift from single to multimale groups of larger size with increasing population density.     

Population Size and Characteristics of <Emphasis Type=Italic>Alouatta pigra</Emphasis> Before and After a Major Hurricane

Although some environmental risks and resources are known to affect the evolution of primate social groups, we know little about the effect of major natural disturbances on primate populations. Hurricane Iris hit the Monkey River watershed in southern Belize in October 2001, presenting a unique opportunity to document the effects of a natural disaster under circumstances wherein some pre-hurricane data were available. We measured the characteristics of the population of black howlers in the affected forest 3.5 years after the storm and compared the population data with pre-hurricane data from a 52-ha study area, that may represent the larger continuous riverine forest and from which all monkeys were known. From February to May 2004, we sampled 28.77 km² of the 96-km² forest fragment via five transects walked 12 times each. From these data we estimate that the population in the watershed has dropped from 9784 to 1181 monkeys, a reduction of 88%, reflected by both a 79% drop in the number of social groups and a 38% reduction in group size. Before the storm, 75% of the social groups were multimale; after the storm, 74% of the groups were unimale. While the ratio of adult females to males improved slightly, the ratio of adults to immatures, and adult females to immatures more than doubled, indicating a much lower potential for growth. These data provide a quantitative assessment of how a major natural disturbance can affect a primate population.     

Social modulation of testosterone levels in male black howlers (Alouatta pigra)

The influence of social factors on the modulation of male testosterone levels has been demonstrated among several vertebrate species. In addition to sexual activity, parental care and reproductive competition affect testosterone secretion. We examined variations in testosterone levels among male black howlers (Alouatta pigra) in various social contexts. Fecal samples were collected from nine males living in five different groups in the Mexican state of Campeche. The potential for intragroup and extragroup competition varied among the groups. The number of resident males living in the groups was the only variable that significantly explained variations in testosterone levels. Males living in unimale groups had higher testosterone levels; the highest testosterone levels were recorded for males that had experienced a shift from multimale to unimale group compositions. In this species, the probability of being challenged by extragroup males and evicted from the group during immigration events increases when males live in unimale groups. Therefore, our results suggest that male black howlers respond to competition for group membership by increasing their testosterone levels. In this context, testosterone secretion represents an anticipatory response to reproductive conflicts. Therefore, although males living in unimale groups have exclusive access to females, they face higher physiological costs associated with sustaining high testosterone levels for extended time periods.     

Intersexual Conflict and Group Size in <Emphasis Type="Italic">Alouatta palliata</Emphasis>: A 23-year Evaluation

Models of optimal primate group size suggest that group formation and growth arise to benefit individual fitness, but that size is limited by costs. The ecological constraints hypothesis posits that group formation and growth is driven by protection from predation or the advantages of group foraging, while an upper limit on group size is constrained by travel costs and intragroup competition for food or other critical resources. Socioecological models also predict that individual reproductive success, hypothesized to decrease with increasing group size, also places an upper limit on the number of individuals in a group. Our analysis of 23 yr of group composition data on mantled howlers (Alouatta palliata) from a single Panamanian study site on Barro Colorado Island not only corroborates the socioecological model but also shows that female reproductive success increased, whereas that of males decreased, with the less female-biased sex ratios in larger groups. We suggest that the conflict of interest between the sexes over adult sex ratio, particularly the male proportion in a group, in combination with ecological factors, is an important determinant of group size and composition.     

Social Relationships Among Male <Emphasis Type="Italic">Alouatta pigra</Emphasis>

We investigated male social relationships in 2 groups of black howlers (Alouatta pigra) in Palenque National Park, Mexico, over a 14-mo study characterized by frequent changes in male group membership. Both single males and pairs of males entered our focal groups. Single males tended to join groups, whereas pairs of males entering groups together successfully evicted resident males. The 19 male dyads across the 11 periods defined by changes in group membership were rarely in close proximity or interacting with one another. Nevertheless, 1 male formed significantly closer associations with resident females in 6 periods and achieved higher mating success during 4 of the periods when ≥1 female was sexually active. In the other 5 periods, no particular male maintained significantly closer associations with resident females, which may be a result of the rapid sequence of changes in male membership and corresponding social instability. Resident males participated frequently and consistently in mutual howling, but the resident male with the strongest female associations and highest mating success initiated howling bouts more frequently in all but 1 of the 6 socially stable periods. Though still preliminary, our findings suggest that variation in social relationships among male black howlers may be more related to their ability to establish strong relationships with females than to their relationships with one another.     

The distributions of howling monkeys (<Emphasis Type="Italic">Alouatta pigra</Emphasis> and <Emphasis Type="Italic">A. palliata</Emphasis>) in southeastern Mexico and Central America

We compared the distributions of Alouatta palliata and A. pigra in southeastern Mexico and Central America with geographic and ecological features to infer current barriers and ecological preferences. Distribution data were obtained from museum specimen localities, study sites, historic records and field surveys and integrated into digital elevation and ecosystem maps using GIS. A. pigra evidently occurs at a number of sites above 2,000 m, where temperatures can even drop below zero on some days of the year, thus indicating a broader ecological tolerance than previously reported. Both species occupy a number of vegetation types and can be found in seasonal and nonseasonal forests. We identified the highland massif of northern Central America and its associated coniferous and subalpine vegetation as a geographic barrier that separates the species. In the past, distribution maps for these species have indicated adjacent contiguous ranges, but we propose that they are largely separated by these mountains. There are two contact zones: a broad area of sympatry north of the highland massif in Mexico and a narrow zone in eastern Guatemala where parapatry is maintained by a river barrier and where only A. pigra occurs in the high elevations and cooler habitats inland. We explore an alternative biogeographic scenario for the split of the two species that accounts for the current distribution and differences in elevation and cold tolerances. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

Determination of Fecal Glucocorticoid Metabolites to Evaluate Stress Response in <Emphasis Type="Italic">Alouatta pigra</Emphasis>

Measuring fecal glucocorticoid metabolites is now a common practice to assess the stress response in primates. Nevertheless, it is important to validate the utilized immunoassay for each primate species before the technique is applied to populations in the wild. We determined the stress response of black howlers (Alouatta pigra) via 2 different group-specific enzyme immunoassays (EIAs). 11-oxoetiocholanolone EIAs are suited to assess the stress response of black howlers via fecal glucocorticoid metabolites. Levels of fecal glucocorticoid metabolites increased after we applied a stressor, i.e. anesthesia, reaching peak concentrations 24–96 h poststressor. Both basal and stress-induced fecal glucocorticoid metabolite levels showed individual variations. The increase of fecal glucocorticoid metabolites after the stressor (paralleling increases in serum) indicates that one can effectively measure adrenocortical activity in Alouatta pigra via these 2 enzyme immunoassays. However, it is important to consider individual variations in the excretion of fecal glucocorticoid metabolites when planning field endocrinological research on Alouatta pigra. Fecal glucocorticoid metabolite excretion takes 1–3 d poststressor depending on the individual. Further, there is an important individual variability in the concentrations of glucocorticoid metabolites, which might reflect differences in stress reactivity or fecal glucocorticoid metabolite metabolism and excretion.     

Group takeover by a natal male howling monkey (Alouatta palliata) and associated disappearance and injuries of immatures

As part of a long-term study on howling monkey behavior and social dynamics, a known natal male was observed taking over his group from his putative sire. Due to the accidental death of one of the adult males, this natal male had matured in a one-male group and had never observed juvenile male emigration nor adult male immigration and associated behaviors. Nevertheless, the behaviors associated with the takeover were indistinguishable from those of an immigrant male, including disappearance of immatures, one of whom was found with extensive injuries. While it cannot be said that the natal male inherited these behaviors from his presumed father, it can be said that he exhibited species-typical behaviors associated with male takeover in the absence of observational learning.     

Survey of Helminth Parasites in Populations of <Emphasis Type=Italic>Alouatta palliata mexicana</Emphasis> and <Emphasis Type=Italic>A. pigra</Emphasis> in Continuous and in Fragmented Habitat in Southern Mexico

The 2 howler species that occur in southern Mexico, Alouatta palliata mexicana and Alouatta pigra are endangered, mainly as a result of habitat loss and fragmentation from human activity. Little is known about the gastrointestinal parasite communities affecting their populations, and lack of baseline information for populations of howler species in continuous forest habitats, makes evaluations of gastrointestinal parasite prevalence in populations in fragmented landscapes difficult. We report the results of a one-time broad survey of gastrointestinal parasites in fecal samples of individuals from several demographically stable populations of Alouatta palliata mexicana and A. pigra existing in continuous and/or protected forests. We further report similar data for populations of both species in human-fragmented landscapes. We detected 6 parasites for each howler monkey species, but only 3 of them (Trematode I, Controrchis biliophilus, Trypanoxyuris sp.) were common to both species. While parasitic prevalence in populations of both howler species was, in general, higher in the fragmented habitat than in continuous and/or protected forests. The difference is only marginally significant in Alouatta pigra. Some parasites (Coccidia and Strongylid) only appeared in populations in fragmented landscapes. Preliminary data suggest that adult males tended to have higher parasite prevalence values than those of adult females in both howler species. Parasite prevalence is associated to average group size, but not to population density in Alouatta pigra.     

Risk factors connected to gastrointestinal parasites in mantled Alouatta palliata mexicana and black howler monkeys Alouatta pigra living in continuous and in fragmented rainforests in Mexico

In this study we document the prevalence of gastrointestinal parasites (helminths and protozoans) found in fecal samples of populations of Alouatta palliata mexicana and of A.pigra in Los Tuxtlas and in Palenque,southeast Mexico,and its relation to habitat condition,sex/age and season.Nineteen parasite morphotypes were detected in the fecal samples from populations of the two howler monkeys,of which 58％ were shared by both species.When considering all parasite species,populations of the two howler species were more likely to be parasitized in fragmented habitat compared to continuous habitat.Individuals of both howler monkey species that lived in fragmented habitat had a higher prevalence of Controrchis biliophilus.A.p.mexicana individuals had a higher prevalence of Trypanoxyuris minutus than A.pigra,probably the result of the larger group sizes found in the former species,and T.minutus was more likely to be found in A.palliata individuals that lived in fragmented habitat.Adult A.p.mexicana males had a higher risk of being parasitized compared to adult females,but these differences were not detected in A.pigra.Parasite species such as Entamoeba sp.,Nematoda sp.28.Nematoda sp.B and Parabronema sp.where only found during the wet season m both howler monkey species.Populations of both howler monkey species had a higher prevalence of Nematoda sp.A in the wet season and Ascaridae eggs were only detected during the wet season in A.pigra.Other parasites detected displayed no clear seasonal pattern.     

Constraints on Group Size in Red Colobus and Red-tailed Guenons: Examining the Generality of the Ecological Constraints Model

The ecological constraints model proposes that an increase in group size will increase intragroup feeding competition and thereby constrain group size. Although this model has received wide acceptance, tests of it are based only on a few studies of species that have similar ecological requirements and social organizations, and there are reasons to question the widespread acceptance of the assumptions underpinning it. Via a 2-year study, we explored determinants of group size in species that feed on markedly different types of foods: the folivorous red colobus (Procolobus pennantii) and the frugivorous/insectivorous red-tailed guenon (Cercopithecus ascanius). We established 4 study sites approximately 15 km apart in Kibale National Park, Uganda, to examine the relationship between average group size and food availability. In both species, we quantified interdemic variation in diet, density of food trees, rate of travel, and group size. Red colobus at all sites relied heavily on leaf resources (75.5%–86.9%), but fruit (6.4%–13.9%) and flowers (2.0%–13.9%) were important in some populations. In general, red-tailed guenons fed on fruit (35.7%–59.7%), insects (14.5%–17.6%), and young leaves (12.2%–32.8%), but the amount of time allocated to these foods varied among sites. Average monthly density of trees bearing food items ranged among sites from 45 to 79 trees/ha for red colobus and from 19.6 to 67.3 trees/ha for red-tailed guenons. For both species, rate of travel was similar among sites, with one exception for red colobus. Average red colobus group size varied among sites from 14 to 40 (28 groups counted). Red-tailed guenon group size varied among sites from 11 to 24 (16 groups counted). As predicted by the ecological constraints model, group size increased with food tree density across sites for both species.     

Group Size, Home Range Use, and Seasonal Variation in the Ecology of Eulemur mongoz

We collected data during a 10-month study carried out on the mongoose lemur, Eulemur mongoz, at Anjamena in northwestern Madagascar, which provide baseline information on seasonal variation in the ecology, home range use and some aspects of the behavior of two neighboring groups. We monitored group size of nine groups in the study area and assessed them for seasonal variation. We present additional information collected during short-term surveys in other areas before and during the study for comparison. The study groups were small family units, and changes in group size were limited to births and emigrations of sexually mature progeny. In spite of clear seasonal changes in climate and vegetation, there is no variation in grouping patterns, so it is not possible to correlate variation in group size with seasonal variation of ecological variables. Comparison with ecological data from other field studies on lemurids reveals differences in food resource distribution in western forests versus other types of Malagasy forest. This distribution of food resources may predict home range size in mixed frugivorous–folivorous lemurs. Small home ranges, mainly in the West, could be correlated with a uniform distribution of food resources. Finally, we suggest that the dry season in the West may not present frugivorous–folivorous lemurs with major problems in finding an adequate food supply. This is supported by the lack of seasonal differences in ranging behavior of mongoose lemurs.     

Birth Seasonality in Alouatta caraya in Northern Argentina

Given appropriate ecological and social conditions, natural selection should favor individuals that can concentrate their reproductive events to a particular time of the year that offers high opportunities for infant survivorship. Previous studies on births in Alouatta caraya in Northern Argentina revealed the existence of a peak during the dry season—a period with scarcity of food resources—in mainland gallery forest (G. E. Zunino, Extra 133: 1–10, 1996). The time of conception and the period of independence of the offspring are positively correlated with precipitation, temperature and availability of food. Offspring became independent from their mothers when the availability of resources was high, and conception coincided with the peak of fruit production. Our goal was to examine patterns of birth seasonality in Alouatta caraya in flooded forest on an island in Northern Argentina for comparison with the mainland population. Both sites are at similar latitudes, but differ in forest type. The results indicate that the availability of new and mature leaves is more consistent throughout the year in the flooded forest (p<0.05); however, there was no difference in the availability of fleshy fruits between sites (p>0.05). The pattern of births differed between the gallery forest and the flooded forest (2-way Anova, p<0.001). In the flooded forest births occurred throughout the year, which supports the contentions that howlers do not have a fixed birth season and that the observed variation in the timing of births appears to represent a facultative behavioral response to changes in food availability.     

Adoption in free-ranging red howler monkeys,Alouatta seniculus of Venezuela

This report describes three cases of infant adoption in red howler monkeys (Alouatta seniculus) of Venezuela. In one case, a lactating female adopted her infant granddaughter after the infant's mother disappeared and the infant survived for the next 25 months. In the second case, an adult female adopted her infant granddaughter for nine days while the infant's mother was still a group member. In the third case, a nulliparous female temporarily adopted an infant from a neighboring group. The details and the possible reasons for these adoption are described.     

Seasonal and age-related differential mortality by sex in the Mantled Howler monkey,Alouatta palliata

Age-specific, differential mortality occurs between male and female mantled howler monkeys, Alouatta palliata,on Barro Colorado Island, Panama. A peak in mortality between 5 and 7 years is seen in males but not infernales. Dates when howler cadavers have been found suggest a seasonal mortality, with peaks in July and perhaps also in December through January.     

Survey of the black howler monkey,<Emphasis Type="Italic">Alouatta pigra</Emphasis>, 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/km². 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 ≥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 ofAlouatta 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.