Spatial and Diurnal Distribution of Loud Calling in Black Howlers (Alouatta pigra)

Loud calling, i.e., howling, is the single most distinctive behavioral attribute of the social system of howler monkeys (Alouatta spp.), yet no general consensus has been established regarding its function. During a 16-mo study, we investigated the degree to which howling bouts varied in duration and spatial and temporal patterns across different social contexts in three groups of black howlers (Alouatta pigra) at Palenque National Park, Mexico, to assess how howling functions in intergroup spacing. We recorded 359 howling bouts, of which 42% were spontaneous with no apparent cause, 28% followed nearby howling without visual contact with the caller(s), 25% were during intergroup encounters, and 5% were during encounters with solitary individuals. The mean duration of howling bouts was 14.8 ± SE 0.6 min. During encounters with neighboring groups or solitary individuals howling bouts lasted significantly longer than spontaneous and reply calls. Spontaneous and reply howling showed a bimodal pattern with a marked concentration around dawn and a second increase of howling in the afternoon. In contrast, howling during encounters with neighboring groups or solitary individuals occurred randomly throughout the day. In addition, howling, irrespective of the context in which it was given, occurred throughout the groups’ home ranges without concentrations in the heavily used core areas or borders of the home ranges. Our findings suggest that loud calling in black howlers functions principally in regularly announcing the occupancy of an area, and is concentrated in the morning when sound propagation is optimal.     

Maternal Watchfulness in Black Howler Monkeys (Alouatta pigra)

In many vertebrates, parents protect their young by detecting predators and aggressive conspecifics before they attack. But parental investment in protection is a limited resource, whose allocation to offspring should reflect optimization strategies. Thus, we tested if maternal investment in vigilance varied with the risk faced by young black howler monkeys (Alouatta pigra). Twelve females in six groups were compared, including those with and without young and those with immatures of differing ages. The greatest increase in vigilance was seen when immatures were conspicuous, and to a lesser extent, among mothers of dependent young (neonates and infants). These findings support the idea that parents adjust their behavior to both chronic and episodic risk faced by young. We explore the possible role of predation and infanticide in shaping the vigilance of mothers.     

The Effect of Hurricane Iris on the Food Supply of Black Howlers (Alouatta pigra) in Southern Belize1

Hurricanes frequently affect the forests of South and Central America; however, few studies have quantified their effects to forest structure, especially when concentrating on the food supply of an animal population. Hurricane Iris made landfall in Southern Belize on 8 October 2001, severely damaging a 52 hectare site where the behavioral ecology of a population of Central American Black Howlers (Alouatta pigra) had been under study for 2.5 yr. The hurricane resulted in a mortality rate of 35 percent for major food trees, which was primarily attributed to uprooting, snapping, and major delimbing. This damage accounted for 97 percent of the food tree loss between the two sample periods. Tree species differences were found in both the percentage loss and category of damage to food trees. Trees of different heights also experienced different percentage loss and levels of damage; subcanopy and emergent trees experienced higher loss than canopy trees, and subcanopy trees were frequently uprooted. This was partially attributed to a lack of buttressing on these subcanopy trees. Buttressing was found to decrease the frequency of uprooting. Tree size was the only factor that did not influence either damage or death. Trees from which fruit were eaten by black howlers died more than twice as often as did trees eaten for leaves.     

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.     

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.     

Responses to Deforestation in a Group of Mantled Howlers (Alouatta palliata) in Costa Rica

To evaluate the effects of partial deforestation of the home range of a group of free-ranging howlers on Hacienda La Pacifica, Costa Rica, we compared activity patterns, social interactions, daily travel lengths, group sizes and migration patterns before, during, and after habitat destruction. Immediate responses were a decrease in social interactions and increase in start to travel. Long-term responses included an increase in feeding time and longer daily path length. The long-term responses were associated with the adjustment to a new home range which was longer and narrower, with the patchiest resources at the furthest end points. Group size decreased due to a significant decrease in adult males and females and a significant increase in infant deaths between the predeforestation period and the deforestation/postdeforestation periods. Significant increase in adult female deaths/emigration continues, though emigration of immatures remains unchanged. Reduced group size could be due to reduced resources or disturbed migration routes throughout the farm due to the construction of a major canal system.     

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.     

Travel Time Predicts Fecal Glucocorticoid Levels in Free-Ranging Howlers (Alouatta palliata)

Environmental stressors impact physiology in many animal species. Accordingly, the monitoring of fecal glucocorticoid metabolites (fGCM) has been increasingly used to evaluate the physiological costs of habitat disturbance on wild animal populations, providing a powerful tool for conservation and management. Several studies have suggested that primates in forest fragments have higher fGCM levels than those in continuous forests, yet the proximate causes of fGCM variation remain to be identified. In previous studies of Mexican howlers (Alouatta palliata mexicana) in Los Tuxtlas, Mexico, we found that individuals living in a smaller and more disturbed forest fragment consumed significantly less fruit and had a significantly higher feeding effort than those living in a bigger, more conserved forest fragment. Here, we aimed to examine the effects of fruit consumption and travel time on fGCM levels in the same two groups of howlers, during three sampling sessions that differed markedly in fruit availability. We found that fGCM levels (N?=?202 fecal samples) were higher in the howler group living in the smaller forest fragment and varied seasonally in both focal groups, being lowest when fruit consumption was highest. However, our results suggest that travel time is the main factor predicting fGCM levels in howlers, and that although fruit consumption may be negatively related to fGCM levels, this relationship is probably mediated by the strong effect that fruit consumption has on travel time. Our results provide important insight into the proximate causes of fGCM variation in primates in fragments and highlight the potential conservation significance of studies showing that habitat loss and transformation can lead to increases in travel time in wild primates.     

The Influence of Loud Calls on Intergroup Spacing Mechanism in Black Howler Monkeys (Alouatta pigra)

International Journal of Primatology - Long-distance vocalizations form an integral part of intergroup spacing mechanisms. The decision to approach, retreat, or ignore loud calls of neighboring...     

Group size and composition influence male and female reproductive success in black howler monkeys (Alouatta pigra)

It has been argued that grouping patterns might influence the reproductive performance of individuals. Increasing group size results in greater travel costs and competition over depletable food resources, which could lead to reduced individual reproductive success. However, in groups with an increasing number of males, female reproductive success is predicted to augment because larger male groups might better protect immatures from infanticidal attacks. In contrast, male reproductive success is predicted to decrease with number of males in a group because fertilization cannot be shared between males. In this paper, we test these predictions on the Mesoamerican black howler monkey (Alouatta pigra) with data on group size and composition for 120 groups from eight populations of black howler monkeys existing in eight protected forests in Mexico and Guatemala. Male and female reproductive success were calculated as a deviation of the observed number of infants (or immatures) from the expected number of infants (or immatures), relative to the number of males and females in a group. Results indicate that both male and female reproductive success decreased with group size. Male reproductive success decreased with an increasing number of males in a group and with increasing proportion of males relative to females in a group. Decreased female reproductive success was associated with increasing number of females in a group, and female reproductive success had a tendency to increase with increasing number of males in a group. These results suggest that in black howler monkeys, living in larger groups might negatively affect the reproductive success of each member. Our findings are similar to those reported for a population of a sister species, Alouatta palliata, living in larger groups.     

Resource Use in a Landscape Matrix by an Arboreal Primate: Evidence of Supplementation in Black howlers (Alouatta pigra)

Across the tropics, landscapes of continuous rain forest are being replaced by forest fragments embedded in a matrix of pastures and farmlands. This conversion has endangered many species, including arboreal primates. Species vary, however, in how they are able to supplement their diets from the matrix, although this is rarely studied in primates. We studied two groups of black howlers (Alouatta pigra) for a total of 1156 h, one inhabiting a smaller fragment (0.4 ha) and the other a larger fragment (20 ha). monkeys inhabiting the smaller fragment spent more time in the matrix than in the habitat fragment, spending 50 % of their time (335 of 667 h) in an abandoned mango (Mangifera indica) plantation, 8.8 % in scattered trees, and 0.2 % in pastures. In contrast, monkeys in the larger fragment spent 75 % of their time (368 of 489 h) in the forest fragment and only 25 % of their time in the matrix. Feeding in the matrix accounted for 53 % and 12 % of the foraging time for groups in the smaller and larger fragments respectively. We suggest that Alouatta pigra can use resources in the matrix to supplement their diet by means of crop raiding or taking other resources in many fragmented landscapes and that this may be true also for many fragment-dwelling primates. It is important to include a consideration of the matrix in conservation planning, considering both the total resources available to primates and the consequences of crop raiding for farmers.     

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. Am. J. Phys. Anthropol. 102:329–336, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Roaring rhythms in black howler monkeys (Alouatta pigra) of Belize

Roaring was recorded during 15-min intervals for 55 days from April 29 to July 14, 1981 in the area around Bermuda Landing, Belize. Roaring profiles were compiled to represent four three-week periods in which roaring was graphed against the time of day. Rates of roaring were also calculated for three troops. Results indicate a gradual change in the daily profile of roaring from dry to rainy season. The marked bimodality of roaring at dawn and dusk in the dry season changed to a more dampened bimodality with reduced dawn and dusk peaks and more roaring during the midday in the rainy season. This seems related to the decreased hours of sun and the amount of rain during the wet season. Additionally, literature on monkeys with long range vocalizations suggests that bimodal peaks in calling may be more prevalent in species which display territorial defense.     

Physiological Ecology of Howlers (Alouatta): Energetic and Digestive Considerations and Comparison with the Colobinae

Remarkably little attention has been focused on the physiological ecology of free-ranging primates. Yet without such information, it may prove difficult to advance our understanding of factors influencing the dietary behavior of wild primates much beyond its present state. Mantled howlers (Alouatta palliata) have been studied in terms of some features of physiological ecology. Results of this work have helped to clarify some factors influencing howler and other primate food choices in the natural environment and have called into question various assumptions about leaf-eating primates. For example, though howlers eat considerable foliage, they do not exhibit a lower than predicted basal metabolic rate, nor do available data suggest that secondary compounds strongly influence howler food selection. Comparison of howlers with members of the Colobinae reveals some differences in features of their respective energetic and digestive physiology and raises timely issues for future research.     

Geographical distribution of the black howler (Alouatta pigra) in Central America

The geographic range of the black howler,Alouatta pigra in Mexico, Guatemala, and Belize was investigated by travelling through and visiting 65 locations within or close to the expected range. The existence of the species was noted through first hand observations or was documented by talking with residents and knowledgeable people in the area. Observations were made on captive animals as well. All sites and probable sites ofA. pigra were noted to be under 1,300 ft in altitude and in areas with a mean annual temperature above 25°C and a mean annual rainfall over 1,000 mm per year. This area coincides with tropical rain forest areas, including both tropical evergreen and semievergreen rain forests.A. pigra was most plentiful in riverine areas which showed flooding for some part of the year. Two areas of possible sympatry withA. palliata were noted. In all cases, the troop sizes ofA. pigra were extremely small, under ten individuals, and infants could easily be sexed, in contrast toA. palliata which is known to occur in troops of 15–18 and is difficult to sex at an early age. Finally, a very gross method for population estimation from searching time emerged from the study.     

Breeding behaviors in the black howler monkey (Alouatta pigra) of belize

Adulterous breeding between a female howling monkey (Alouatta pigra) of one troop with a male of an adjacent troop occurred despite territorial defense between the two troops. The specific behaviors are described as well as a synopsis of daily events which occurred between the female and two males from adjacent troops. A discussion of how this interaction and the behavior patterns relate to what is known about breeding in howler monkeys and related species follows.     

Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes

The gastrointestinal (GI) microbiome contributes significantly to host nutrition and health. However, relationships involving GI microbes, their hosts and host macrohabitats remain to be established. Here, we define clear patterns of variation in the GI microbiomes of six groups of Mexican black howler monkeys (Alouatta pigra) occupying a gradation of habitats including a continuous evergreen rainforest, an evergreen rainforest fragment, a continuous semi-deciduous forest and captivity. High throughput microbial 16S ribosomal RNA gene sequencing indicated that diversity, richness and composition of howler GI microbiomes varied with host habitat in relation to diet. Howlers occupying suboptimal habitats consumed less diverse diets and correspondingly had less diverse gut microbiomes. Quantitative real-time PCR also revealed a reduction in the number of genes related to butyrate production and hydrogen metabolism in the microbiomes of howlers occupying suboptimal habitats, which may impact host health.