Feeding Competition and Group Size in Alouatta pigra

Researchers consider group size in primates to be determined by complex relationships among numerous ecological forces. Antipredator benefits and better resource defense are the primary pressures for large groups. Conversely, intragroup limited food availability, can result in greater intragroup feeding competition and individual energy expenditure in larger groups, creating energetic advantages for individuals in small groups and placing an upper limit group size. However, the extent to which food availability constrains group size remains unclear for many species, including black howlers (Alouatta pigra), which ubiquitously live in small social groups (≤10 individuals). We studied the relationship between group size and 2 key indices of feeding competition—day journey length and activity budgets—in 3 groups of wild Alouatta pigra at a hurricane-damaged site in Belize, Central America. We controlled for differences in food availability between home ranges (food tree density) and compared both indicators of feeding competition directly with temporal variation in food availability for each group. Our results show no consistent association between resource availability, group size, and either index of competition, indicating that feeding competition does not limit group size at the site—i.e., that larger groups can form without increased costs of feeding competition. The results support the search for other explanations, possibly social ones, for small group size in the primates, and we conclude with suggestions and evidence for such alternative explanations.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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

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

Geographic Distribution of Red Howlers (Alouatta seniculus) in Southwestern Brazilian Amazonia, with Notes on Alouatta caraya

We surveyed howler (Alouatta) populations at 36 sites throughout the Brazilian state of Rondônia, in southwestern Amazonia, using quantitative (line transect surveys) and qualitative (interviews) methods. We recorded the red howler (Alouatta seniculus) at only one- third of the sites, and the species was relatively rare at most of them, especially in comparison with sympatric atelids (Ateles chamek and Lagothrix cana). In addition to local discontinuities, Alouatta was absent from a wide area (possibly as much as 100,000 km²) of northern Rondônia, south of the upper Madeira river. This lacuna apparently contradicts the typical association of the species with flooded forest ecosystems, but the ecological factors that may underlie it remain unclear. Competition with sympatric atelids does not appear to be a significant factor anywhere within the study area. Also, there is no evidence to suggest that the distribution patterns are related to recent human colonization of the state. We collected indirect evidence of the presence of a second howler species – Alouatta caraya – at two sites in southern Rondônia, where they are associated with highland savanna habitats and gallery forests in the Guaporé grasslands.     

Behavioural development of howling monkey twins (Alouatta palliata) in Santa Rosa National Park,Costa Rica

Twins born to a young female howling monkey in Santa Rosa National Park, Costa Rica were observed during the first 96 days of their life. The comparison of their development to that of single infants and the comparison of the behaviour of the mother of the twins to that of mothers of single infants revealed few differences. However, qualitative observations suggests that high costs are associated with maternal care of infant twins. The mother had difficulty carrying both infants and was the only female observed to become sick during the study. Increased costs of lactation were not compensated for by an increase in foraging time. It would seem that howling monkey mothers possess a maternal care system which is capable of providing suitable care to twins. However, the costs on the mother of raising twins is suggested as a factor selecting for a litter size of one.     

Diet of the red howler monkey (Alouatta seniculus) in French Guiana

We report the feeding behavior and food preferences of a troop of red howler monkeys (Alouatta seniculus) over two annual cycles in primary tropical rain forest in French Guiana. The monkeys used 195 plant species from 47 families as food. Major food categories were young leaves (54%), mature fruits (21.5%), and flowers (12.6%). Other food categories included old leaves, immature fruits, termitarium soil, bark, and moss. The monkeys were less selective than other howler groups, since 19 plant species contributed 1% to their diet and accounted for only 35.7% of their total diet. The Sapotaceae was the most frequently eaten plant family and represented >10% of the total diet.     

Recruitment of Black Howler Fruit Trees in Fragmented Forests of Northern Belize

We examined recruitment of trees whose seeds are dispersed by black howler monkeys (Alouatta pigra) in forest fragments within the Community Baboon Sanctuary in north-central Belize. In the fragments, most other large frugivores are absent and howlers dominate the large frugivore community. Consequently, we expected to observe an increased representation of howler fruit trees among the sapling community. To test this prediction preliminarily we observed howler feeding behavior for one year and conducted adult tree and sapling transects in 6 locations where howlers were present. We sampled a seventh site where howlers were absent for vegetation only. We found that in 4 of 6 sites there were proportionately fewer howler fruit saplings when compared to adult tree samples. However, when recruitment of howler fruit trees in the 6 sites was compared to a site where howlers were absent, 11 of 12 species had relatively higher recruitment. The lack of recruitment among howler fruit trees in general likely reflects differences in responses of individual species, as well as disruptions from human activities to natural processes within the forests. The observed lower recruitment patterns of howler trees suggest that over time, the abundance of the trees will likely decline and thus affect the foraging behavior and possibly survival of howlers in the fragmented forests.     

Seasonal Changes in Male Associative Behavior and Subgrouping of Alouatta palliata on an Island

Howler groups are usually spatially cohesive and stable in composition; however, more flexible grouping patterns occur in some social groups. We analyzed the associative and subgrouping patterns of males living in a group with fission-fusion social organization. Based on information from previous studies on Alouatta palliata and other primates and in the current socioecological models, we established initial predictions on the variations in male behavior according to several socioecological factors. We studied associative behavior via scan sampling at 15-min intervals to register the identity of males in the subgroups and the presence and number of receptive females. We calculated an association index that was then transformed into a measure of association strength. We found individual association trends, as well as important seasonal differences in the subgrouping patterns of males. During the dry season the presence of many receptive females resulted in reduced levels of association, and therefore fewer males per subgroup. The scenario changed during the wet season, when males grouped together significantly more and kinship relationships were a major determinant for individual association preferences.     

Seismic activity response as observed in mantled howlers (Alouatta palliata), Cuero y Salado Wildlife Refuge, Honduras

This report documents the response of wild mantled howlers (Alouatta palliata) to coseismic activity (seismic activity at the time of an earthquake). During field work on the north coast of Honduras, data were collected on a habituated troop of mantled howlers as they responded to coseismic activity. The seismic event occurred on 13 February 2001 at 0822 hours local time with a magnitude of Richter scale 6.6, focus depth of approximately 15 km at a distance of 341 km from the epicentre to the field site, Cuero y Salado. At the field site, based upon Jeffreys and Bullen (1988), body waves, noted as P and S waves, arrived at 60 and 87 s, respectively, with surface waves arriving approximately 103 s post-origin time of the seismic event. While there are three reports on non-human primate response to coseismic activity in the literature, they report on captive non-human primates. This is the first documented response on a non-captive troop. In addition, this report compares the intensity measure encountered by a wild troop of howlers and one captive group of orangutans as set out by the Modified Mercalli Intensity scale. The Modified Mercalli measure of intensity is one of two standard measures of seismic activity and rates what a person sees and feels at their location (Wood and Neumann 1931; Richter 1958). Thus, arboreal nonhuman primates are found to respond to coseismic activity ranging from Level IV to Level VI as based upon the modified Mercalli intensity scale.