Growth of Mantled Howler Groups in a Regenerating Costa Rican Dry Forest

We examined population dynamics in mantled howlers (Alouatta palliata palliata) in a regenerating tropical dry forest in Santa Rosa National Park (SRNP), Costa Rica. The population has grown at a rate of about 7% per annum during the past decade. The growth in numbers from 342 in 1984 to 554 in 1992 reflects an increase in the number of groups (from 25 to 34) and a slight increase in their average size (from 13.6 to 16.3). Population density has increased from 4.9 to 7.9 individuals per km ². Santa Rosa's population density and group compositions are similar to those at several other mantled howler sites, but densities of mantled howlers are much higher at two other well-studied sites: La Pacifica and Barro Colorado Island (BCI). We relate the low density of howlers at Santa Rosa to local historical and ecological factors. Howler populations at high and low densities differ in average group size and sex ratio. At high population densities, groups are larger and include more adult females. The number of male howlers per group appears to be more strictly limited and less variable than the number of females is. However, there is greater variation in male group membership at Santa Rosa than at La Pacifica or BCI, and at Santa Rosa there are more generating forests available into which males and females can disperse and form new groups. We present case studies describing two ways in which new howler groups are formed, and we suggest that, compared to females and compared to males at high density sites, males are relatively advantaged in the uncrowded habitats at Santa Rosa and other low density sites.     

Effective Solutions for Howler Conservation

All species of howlers are at risk due to habitat destruction. I review the three most serious threats to howler survival—agricultural disturbance, logging disturbance, and hunting—both in a general context and in species accounts. Withal, the adaptability of howlers has allowed them to be a widespread genus throughout Central and South America. Alouatta is especially adaptable due to its generalized folivorous diet. I discuss how this adaptability relates to survival in situations of habitat destruction. In addition, I examine howler preference for riverine habitats and their ability to capitalize on secondary forests and secondary growth. I take a practical approach, suggesting some solutions for species survival, which include habitat management and reintroductions. Successful conservation models highlighted are the Community Baboon Sanctuary in Belize, in which villagers manage their lands for the benefit of the black howler and for their own economic benefit from ecotourism, and a village-sustainable logging system in Quintana Roo, Mexico, which has reduced levels of deforestation while benefiting both villagers and howlers, as well as other wildlife. A successful translocation of black howlers in Belize in order to reestablish a viable population is also described. The paper concludes with further suggestions to encourage howler conservation.     

Socioecological Factors Affecting Range Defensibility Among Howler Monkeys

Range defensibility is defined as the ability of animals to efficiently move over an area to monitor and defend it. Therefore, range defensibility can help us understand the spatial structure of animal territoriality. We used howler monkeys (Alouatta spp.), a genus for which no agreement on the extent of their territoriality exists, to investigate the factors mediating range defensibility. We compared the defensibility index (D) across 63 groups of howler monkeys, representing 8 different species, based on a literature review. All species, except Alouatta palliata, were classified as potentially territorial according to D, although there was high variability within and among species. Group size had a positive effect on D, probably owing to the greater ability of groups to defend a territory as they become larger. Study area had a negative effect on D, perhaps suggesting that unlike small areas, large areas allow groups to have territories that do not require significant defense from neighbors. However, population density was the factor with the strongest effect on D, with greater monitoring of home ranges under high levels of competition. Our results suggest that howler monkeys are theoretically capable of maintaining a territory and suggest that animals can show a gradient in territoriality, which can be mediated by the competitive context in which it occurs.     

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.     

Growth layers in dental cementum ofSaguinus monkeys in South America

Dark stained layers were observed in the cementum of the teeth ofSaguinus monkeys living in South America. Since the number of layers correlated with the degree of attrition in the incisor, the dark layers probably showed the growth lines. The teeth of the monkeys captured at the beginning of the wet season showed the incremental dark line around most of the exterior of the cementum.     

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.     

Demographic Changes over Thirty Years in a Red Howler Population in Venezuela

During a 30-year span (1969–1999) the annual growth rate of a Venezuelan red howler (Alouatta seniculus) population fluctuated irregularly, but its size increased, remained stable for a short while, and finally declined sharply. The increase took place in three stages, and began as an increase in the size of established groups. The next two stages of population increase were due to the formation of new groups and their subsequent increases in size. These two stages likely occurred because of habitat regeneration, which increased the areas where newly formed groups could establish home ranges. The population decline of 74% was most likely due to disease. However, new groups died out more rapidly than established groups, indicating that food shortages, especially in recently regenerated areas, may also have contributed to the population crash. The food shortages could have been caused by unpredictable periods of drought, which may explain the irregular size fluctuations of the study population. Since many howler species show irregular size fluctuations and sharp declines, their demographic features may reflect adaptations to unpredictable events like droughts and disease epidemics. On this premise we explain the preponderance of unimale groups and female-biased birth sex ratios at low densities and the dispersal of both sexes as adaptations for increasing a population rapidly after a decline. Within the population, mortality of small juvenile females was higher in multimale than in unimale groups, though medium juvenile and older immature females were better represented in multimale than in unimale groups. These results may be explained in terms of group composition and the mating systems in red howlers.     

Growth of the masseter muscle in rhesus monkeys (Macaca mulatta)

The growth of the masseter muscle in eight infant, juvenile, and adolescent female rhesus monkeys (M. mulatta) was examined over a 2.5 year period using serial radiographic cephalometric techniques with the aid of radiopaque muscle markers. The radiopaque markers, which are composed of small pieces of root canal broach inserted into the muscle belly, make it possible to determine longitudinal masseter muscle growth as well as migration of the masseter muscle relative to the mandible. It was found that the masseter muscle increased in length by 64% during the total growth period, most of which occurred between 6 and 18 months of age. Relative to the cranium, the masseter muscle grew markedly inferiorly and only slightly posteriorly. Relative to the mandible, the masseter migrated in a posterior and slightly superior direction, keeping pace with the ramus and condyle as they grew posteriorly and posterosuperiorly throughout the study period. It was concluded that: 1) radiopaque muscle markers are a valuable tool for analysis of muscle growth and alteration of muscle location; 2) the masseter muscle in the rhesus monkey undergoes elongation, probably due to addition of sarcomeres at the fiber-tendon junctions; and 3) posterior migration of the masseter muscle relative to the corpus of the mandible, probably due to the nature of its periosteal attachment, results in a stability of the anteroposterior position of the masseter muscle despite the anterior displacement of the mandible.     

Feeding Strategies of Brown Howler Monkeys in Response to Variations in Food Availability

Primates display varying degrees of behavioral flexibility that allow them to adjust their diet to temporal changes in food availability. This trait might be critical for the survival of folivorous-frugivorous species inhabiting small forest fragments, where the availability of food resources tends to be lower than in large fragments and continuous forests. However, the scarcity of studies addressing this issue hampers our understanding of the adaptive behaviors that favor the survival of these primates in low-quality habitats. We conducted a 36-mo study testing the hypothesis that brown howler monkeys (Alouatta guariba clamitans) are able to adjust their diet in response to local and seasonal changes in resource availability. We compared the diet of six free-ranging groups inhabiting three small (<10 ha) and three large (>90 ha) Atlantic forest fragments in southern Brazil and estimated the temporal availability of their top food species (i.e., those species that together contribute ≥80% of total feeding records). We found that brown howlers exploited similarly rich diets in small (45, 54, and 57 plant species) and large (48, 51, and 56 species) fragments. However, intermonth diet similarity was higher for groups in small fragments, where howlers also fed on plant items from nine alien species. Fruits and leaves were the most consumed plant items in both small (42% and 49% of feeding records, respectively) and large (51% and 41%, respectively) fragments. The consumption of young leaves was higher in small than in large fragments, whereas the consumption of other plant items did not show a pattern related to fragment size. Regarding the contribution of growth forms as food sources, only the exploitation of palms showed a pattern related to fragment size. Palms contributed more to the diet of groups inhabiting large fragments. The availability of seasonal food items–ripe fruits and young leaves–influenced their consumption in both habitat types. Therefore, brown howlers cope with local and seasonal fluctuations in food availability by opportunistically exploiting resources. We believe that this feeding flexibility is a key component of the phenotypic plasticity that enables howlers to thrive in disturbed habitat patches, where periods of scarcity of preferred foods shall be more common.     

In and Out the Amazonia: Evolutionary Ecomorphology in Howler and Capuchin Monkeys

The impact of environmental variation on phenotypic diversification is one major issue in evolutionary studies. Environmental variation is thought to be a primary factor in evolution, especially at high latitudes. In contrast, tropical areas are traditionally viewed as the cradle where the long-term effects of biological interactions on phenotypic change reside. We analyse patterns of skull shape variation in two New World monkey groups: capuchins and howlers. These two monophyletic clades are exceptionally similar in terms of the geographic distribution of their species. Yet, their body size and diet are different: howler monkeys are large and almost exclusively folivorous, whereas capuchins are small omnivorous. We found that the size, and direction of vectors of phenotypic changes across South American biomes in those clades are not statistically different. This similarity persists after removing the strong impact of allometry in our data. Additionally, partial least squares and comparative analyses confirm that “allometry free” skull shape is influenced to the same set of environmental variables in both clades. This study remarks the paramount importance of both body size and environmental variation on phenotypic evolution.     

Male Relationships and Infant Deaths in Red Howler Monkeys (Alouatta seniculus)

For decades howler monkeys were considered to be among the most peaceful animals. Recent investigators, however, have noted that, although male aggression is rare, it may be extremely severe; the criteria used to quantify howler relationships should therefore be different from those used for other primates. This paper describes the pattern of male relationships in the red howler monkey Alouatta seniculus, and examines its effect on reproductive success within the troop and the ability of troop males to resist intrusion by competing males. 4 of the 8 infants born during the study period were killed or disappeared when change occurred in relative status between two adult males.     

Dietary Flexibility of the Brown Howler Monkey Throughout Its Geographic Distribution

Habitat loss and fragmentation constrain the survival of most forest‐living mammals, particularly strictly arboreal primates. Because fragment size directly affects food availability, primate survival in small fragments may depend on dietary flexibility. Here, we review the literature on the diet of 29 wild groups of Alouatta guariba clamitans inhabiting forest fragments in Brazil and Argentina. We identify general feeding patterns and analyze the influence of fragment size and latitude on diet composition. Brown howlers presented a diet composed of 402 plant species belonging to 227 genera and 80 families. Rarefaction curves suggest that the richness of top food species is similar among groups living in larger (>100 ha), medium (11–100 ha) or small (1–10 ha) fragments. On average, only 12% of the plant species used as food sources by a given group was also consumed by groups from other sites. The shorter the distance between sites, the higher the diet similarity among groups. Despite their diet flexibility, brown howlers spent >80% of the total feeding records on 6–24 species belonging to genera such as Ficus, Zanthoxylum, and Eugenia. Leaves and fruits were the plant items most consumed (65% and 22% of the total feeding records, respectively). Leaf consumption was not affected by fragment size, but it was inversely related to latitude, which may be linked to an increase in the concentration of secondary metabolites in leaves at higher latitudes. We suggest that the ability of brown howlers to exploit a large number of plant food species, including native and exotic trees, shrubs, vines, and lianas, is an important trait that contributes to their survival in highly fragmented habitats along the Atlantic forest. Similar meta‐analyses of data from other howler species are necessary to test whether such dietary flexibility is a genus‐wide pattern. Am. J. Primatol. 75:16‐29, 2013. © 2012 Wiley Periodicals, Inc.     

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.     

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...     

Nerve Growth Factor and glucocorticoids regulate phenotypic expression in cultured chromaffin cells from adult rhesus monkeys

Adrenal chromaffin cells and sympathetic neurons are both derivatives of the neural crest. Despite their morphological and functional differences, chromaffin cells retain some developmental plasticity and if treated with Nerve Growth Factor (NGF), can express certain characteristics of sympathetic neurons. However, there is some age and species variability in the response of chromaffin cells to NGF: in general chromaffin cells from adult animals are not considered to be dependent on NGF for survival, and chromaffin cells from adults of several species fail to respond to NGF in vitro by growing neurites. This is in contrast to the dramatic effects of NGF on chromaffin cells from perinatal rats. We have examined the requirements of chromaffin cells from adult rhesus monkeys to survive, to proliferate, and to express a neuronal morphology in vitro. NGF greatly enhances the proportion of rhesus chromaffin cells that form neurites and the length of the neurites that are formed, but the conversion to a neuronal phenotype is more limited than in chromaffin cells cultured from young rats. NGF also enhances rhesus chromaffin cell survival, but fails to stimulate their proliferation, in contrast to its effect on perinatal rat cells [18]. Glucocorticoid hormones (GCs) specifically antagonize the effects of NGF on neuritic outgrowth while promoting chromaffin cell survival. Thus adrenal chromaffin cells from rhesus monkeys retain a degree of developmental plasticity even in the adult animal.     

Neotropical Primates in a Regenerating Costa Rican Dry Forest: A Comparison of Howler and Capuchin Population Patterns

Few data exist on how primate populations return to regenerating tropical forests. We compare the ways that two populations of neotropical monkeys, Alouatta palliata and Cebus capucinus, expanded over a 28-year period after the establishment of Santa Rosa National Park on reclaimed ranchlands in Costa Rica. We found that both howler and capuchin populations increased substantially in size subsequent to protection, but the howler population grew faster. This is likely due to their faster-paced life-history pattern than that of capuchins. The howler population increased mainly via the establishment of many new groups, whereas the capuchins expanded mainly by increasing the size of existing groups. We related this finding to the fact that capuchins are limited largely by their need to drink from water holes during the dry seasons whereas howlers are limited principally by their preference for larger-sized trees that occur in older forests. Proportions of adult male capuchins increased significantly during our study, likely due to skewed sex ratio at birth or male-biased immigration into the protected park or both factors. Our main finding is that, in as short a time period as 28 years, we can substantially enhance the size of monkey populations by allowing the regeneration of tropical forest. Furthermore, we provide a preliminary interpretation of how extrinsic factors—deforestation, hunting, crop-spraying, destruction of the watershed—and intrinsic variables, e.g., pace of reproduction; diet, differentially affect not only each species' vulnerability to extinction but also its capacity to recover when human disturbances are minimized.     

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.