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.     

Habitat selection and seasonal patterns of activity and foraging of mantled howling monkeys(Alouatta Palliata) in Northeastern Costa Rica

I conducted a 15- month ecological study of habitat preferences and activity and foraging patterns of two troops of mantled howling monkeys, Alouatta palliata,in a lowland rain forest at La Selva Biological Reserve in northeastern Costa Rica. The two troops specialized on different habitats in spite of the fact that both of them had all habitats available and were not constrained by neighboring troops since the population density of howlers is low (7- 15 howlers/km ² ).Troop 1 spent the majority of time in primary forest (80%) followed by secondary forest (10%), while troop 2 spent the majority of time in undisturbed riparian habitat (60%) followed by primary forest (30%). Habitat sampling indicates that neither the total number of stems, species, or families nor the diversity (Shannon index) or evenness is a good indicator for howler habitat selection. Instead the density of trees from the 12 species most commonly consumed by each troop is the most important factor. Activity and foraging patterns were not dependent upon the season as has been described for howling monkeys in forests with a more pronounced dry season at Barro Colorado Island, Panama, and La Pacifica in northwestern Costa Rica. This is likely a result of the more constant food supply at La Selva, combined with less intraspecific competition due to the low howler density. The intraspecific variability of foraging patterns and troop- specific habitat specialization observed in Alouatta palliatashould be considered in the conservation biology of primates. Primate relocation programs should include not only an ecological assessment of the release site but also a comparison of the release site with the habitat that the groups currently occupy.     

Population Characteristics of Howlers: Ecological Conditions or Group History

We examined the relative importance of ecological parameters—habitat productivity and seasonality—and group history—episodic predation, disease, and sudden habitat deterioration—to explain variation in the density and group structure of howlers (Alouatta spp.). We use data from a census of Guanacaste National Park, Costa Rica, and a literature review characterizing 80 howler populations. In Guanacaste National Park both habitat type and degree of protection affect howler density and group structure. Howlers were found at the highest density and in the largest groups in areas of semievergreen forest, which ecological sampling indicates have the most consistent level of food production. Differences in density between the sector of the park that first received protected status and more recently protected areas may be due partially to the degree of protection the areas received. We test the prediction that howler density and group structure would be influenced by habitat productivity as indexed by rainfall. Average group size and sex ratios differ among species, but female-to-immature ratios do not. Considering all censuses at one site to be independent, there are significant interspecific differences in density, with Alouatta pigra occurring at lower densities than the other species. In spite of such variability, there is no relationship between annual rainfall and howler density, and rainfall had a variable effect on group size depending on the level of independence that was considered. While such ecological comparisons are unrefined, e.g., rainfall must be used as a surrogate for habitat production, the fact that so few relationships were documented suggests that factors other than the ecological factors considered here are responsible for the observed differences in population characteristics. We suggest that much of the variability in howler population characteristics is related to events occurring in the recent history of the groups, such as habitat alteration, hunting, food tree crop failure, and disease.     

Diet and activity in black howler monkeys (<Emphasis Type="Italic">Alouatta pigra</Emphasis>) in southern Belize: does degree of frugivory influence activity level?

This study reports on the diet and activity budgets of Central American black howling monkeys (Alouatta pigra) at Monkey River, Belize. This is a previously unstudied population, close to the southern boundary of the species range, and it provides comparative data on A. pigra from a new study site. Both diet and activity are within the ranges reported for other A.pigra sites and for mantled howlers (A. palliata). No age-sex differences could be discerned in either diet or activity, though monthly variation was apparent. The monkeys switch from consuming leaves 86% of the time in January to March to consuming 67% fruit in April to July. This difference was statistically significant, and provided the opportunity to compare activity levels of the monkeys over two dietary periods, one characterized primarily by folivory, the other by frugivory. Howlers are often seen as a relatively inactive species, something that is associated with a low quality, folivorous diet. However, A. pigra have been described as being as frugivorous as possible and as folivorous as necessary. Yet, despite the opportunistic consumption of large quantities of high-energy foods, A. pigra has been observed as conforming to the howler lifestyle, resting as much as 80% of the day. The data in this paper support both of these reports. Black howlers at Monkey River Belize are typically inactive, maintaining high levels of inactivity even during months characterized by frugivory, suggesting that diet is more flexible and varied than is behavior and calling into question the assumption that howler inactivity is due to the digestion of large quantities of leaves.     

Foraging Behavior and Activity Patterns of Alouatta caraya in the Northeastern Argentinean Flooded Forest

Howling monkeys (Alouatta spp.) are colonizer species, showing a plasticity in behavior that allows them to inhabit different sorts of forests. There is a series of hypotheses relating demography to behavioral and ecological characteristics of howlers: (1) as howler density increases, home range size will decrease; (2) howler groups occupying small home ranges will have a high proportion of leaves in their diet; and, (3) the proportion of mature leaves in the diet is negatively correlated with group daily travel distance. To test hypotheses about howler diet and ranging pattern in relation to food resources, we studied the foraging ecology and general activity patterns of 2 groups of black howlers (Alouatta caraya) inhabiting in flooded forest of Paraná River (Argentina), the habitat with the highest density recorded for Alouatta. We found, in addition to the highest densities, also the smallest home ranges for Alouatta (Group I: 1.7 ha and Group II: 2.2 ha). However, diet was not dominated by leaves, and high quality items—flowers, fruits, new leaves—were a high proportion of the diet all year. Also, daily travel distance is not correlated with the proportion of mature leaves in the diet, but is positively correlated with the number of group confrontations. Finally, we propose a model integrating and interpreting our results as a function of the spatial and temporal distribution of high quality food resources in the Argentinean flooded forest.     

Impact of yellow fever outbreaks on two howler monkey species (Alouatta guariba clamitans and A. caraya) in Misiones,Argentina

Two yellow fever outbreaks (YFOs) ocurred in northeastern Argentina between November 2007 and October 2008, seriously affecting populations of two howler monkey species: the brown howler Alouatta guariba clamitans and the black howler Alouatta caraya. Both howlers live syntopically in El Piñalito Provincial Park, Misiones, where four groups (36 individuals) were studied since January 2005. The first dead howlers were found on January 20, 2008, in El Piñalito. Systematic searches found 14 dead howlers within the area (12 from the study groups and two from neighboring groups), with only two young seen on January 25, 2008, and none found since up to December 2008. In October 2008, another YFO hit howler monkey populations from El Soberbio, Misiones. Overall, 59 howlers were found dead in Misiones from November 2007 to December 2008. Thanks to the alert of the howler's death in El Piñalito, a prompt human vaccination campaign started in the area. Wild howler monkey populations from both species are in a delicate situation in Misiones, especially the brown howler, an already endangered species in Argentina and endemic to the Atlantic Forest. If we add the recurrence of YFOs to the reduction of suitable habitat to small fragments, it could be only a matter of time until howler populations disappear from the Upper Paraná Atlantic Forest in Misiones. Am. J. Primatol. 72:475–480, 2010. © 2010 Wiley‐Liss, Inc.     

Effects of habitat fragmentation and disturbance on howler monkeys: a review

We examined the literature on the effects of habitat fragmentation and disturbance on howler monkeys (genus Alouatta) to (1) identify different threats that may affect howlers in fragmented landscapes; (2) review specific predictions developed in fragmentation theory and (3) identify the empirical evidence supporting these predictions. Although howlers are known for their ability to persist in both conserved and disturbed conditions, we found evidence that they are negatively affected by high levels of habitat loss, fragmentation and degradation. Patch size appears to be the main factor constraining populations in fragmented habitats, probably because patch size is positively related to food availability, and negatively related to anthropogenic pressures, physiological stress and parasite loads. Patch isolation is not a strong predictor of either patch occupancy or population size in howlers, a result that may be related to the ability of howlers to move among forest patches. Thus, we propose that it is probable that habitat loss has larger consistent negative effects on howler populations than habitat fragmentation per se. In general, food availability decreases with patch size, not only due to habitat loss, but also because the density of big trees, plant species richness and howlers' home range size are lower in smaller patches, where howlers' population densities are commonly higher. However, it is unclear which vegetation attributes have the biggest influence on howler populations. Similarly, our knowledge is still limited concerning the effects of postfragmentation threats (e.g. hunting and logging) on howlers living in forest patches, and how several endogenous threats (e.g. genetic diversity, physiological stress, and parasitism) affect the distribution, population structure and persistence of howlers. More long‐term studies with comparable methods are necessary to quantify some of the patterns discussed in this review, and determine through meta‐analyses whether there are significant inter‐specific differences in species' responses to habitat loss and fragmentation. Am. J. Primatol. 72:1–16, 2010. © 2009 Wiley‐Liss, Inc.     

Conservation Biology of the Genus Alouatta

As assessed by the IUCN Mace–Lande system, seven (35%) of the 20 Alouatta species and subspecies with adequate data are classified as threatened, i.e., critically endangered, endangered, or vulnerable (Rylands et al., 1995). This percentage is much lower than the 75 to 100% threatened taxa for the other large-bodied genera: Ateles, Lagothrix, and Brachyteles. Only 5 of the 16 Neotropical genera have lower percentages of threatened taxa than that of Alouatta: Cebuella, Pithecia, Saguinus, Saimiri, and Cebus. The threatened howler taxa occupy small distributions in areas of forest fragmentation. In general, populations are most affected by major habitat disturbance, such as total deforestation and flooding from dam construction, and by human hunters. Facilitated by their ability to exploit folivorous diets in small home ranges, howlers can tolerate considerable habitat fragmentation but not the increased exposure to hunting that may accompany it. Howlers seem particularly vulnerable to yellow fever and bot fly parasitism. Although the former threat may decrease by increasing fragmentation of the habitat, other sorts of parasitism may increase in disturbed habitats. The low genetic variability of the Central American howlers suggests a resistance to inbreeding depression potentially experienced during population bottlenecks. Greater between-population variability may still exist. Although howlers are not readily bred in captivity, they respond well to translocation. Translocation has been successfully achieved for 4 howler species and is a viable option for introducing new genetic variability into population fragments and repopulating areas from which howlers are extinct. Their pattern of bisexual dispersal facilitates colonization of regenerating habitats, and in suitable, protected habitats they have shown the capacity for strong population recovery.     

Feeding ecology of the black howler monkey (Alouatta pigra) in Northern Belize

We studied the feeding ecology of the black howler monkey (Alouatta pigra) from March 1994 to April 1995 in the Community Baboon Sanctuary in northern Belize, Central America. Activity and diet composition were recorded using continuous focal animal sampling. Diet composition was compared with the relative abundance of plant parts eaten by the howlers within the study site. The study animals spent an average of 24.4% of their time feeding, 61.9% resting, and approximately 9.8% traveling. In contrast to previously published reports on A. pigra, we found the diet composition to be similar to that of other Alouatta species (conforming to the folivore/frugivore profile), with 41% of feeding time spent eating fruit, 45% foliage, and 11% flowers. This contrast may indicate a wide degree of dietary flexibility that allows A. pigra to inhabit a variety of habitat types. We suggest that a high level of resource abundance throughout the year makes the Community Baboon Sanctuary excellent habitat for Alouatta pigra. Am. J. Primatol. 45:263–279, 1998. © 1998 Wiley-Liss, Inc.     

Seed Dispersal and Ingestion of Insect-Infested Seeds by Black Howler Monkeys in Flooded Forests of the Parana River, Argentina

All howler monkey species ( Alouatta spp.) have a folivorous–frugivorous diet. Howler monkeys are reported to be seed dispersers in several areas, including black howlers ( Alouatta caraya ), which are important seed dispersers in northern Argentinean forests. The goal of this work was to study the three-way interaction between insects, seeds, and black howlers, and assess the functional significance of this tri-trophic interaction for seed dispersal. I determined through direct observation that fruits of species with a high proportion of insect infestation were important components of howler monkey diet. Ocotea diospyrifolia seeds from fresh faeces of black howlers contained dead larvae, but seeds were still able to germinate. Seeds in which larvae had reached an advanced stage of development did not germinate. Larvae of infested Eugenia punicifolia fruits were killed by digestion when they occurred in the pulp early in the fruiting season, but were dispersed alive with seeds later in the season. Banara arguta fruits contained both healthy and infested seeds; infested seeds were destroyed during digestion, while healthy seeds were dispersed. Black howlers' ingestion of infested fruits could result in the: (1) killing of larvae and dispersion of healthy seeds; (2) spread of larvae; or (3) destruction of infested seeds. This will depend on the relationship between the time at which fruit is consumed by black howlers, the time at which insect infestation occurs, and also probably on the hardness of the seed coat and the seed–insect size ratio.     

The Influence of Large Tree Density on Howler Monkey (Alouatta palliata mexicana) Presence in Very Small Rain Forest Fragments

The populations of the Mexican mantled howler monkey ( Alouatta palliata mexicana ) in the Los Tuxtlas region, Mexico, have declined drastically due to habitat loss and fragmentation. Nevertheless, several troops still inhabit very small and isolated rain forest fragments. We identified the main vegetation attributes that can favor the presence of howlers within 18 small (< 10-ha) fragments that did not differ significantly in size, shape, and isolation (nine occupied and nine unoccupied by howlers). We found that habitat quality ( i.e. , food resources and vegetation structure) affected howler incidence in small fragments. Particularly, the occupied fragments showed greater density of big trees (dbh > 60 cm), greater total basal area, greater basal area of persistent tree species, and greater basal area of top food species than the unoccupied fragments; suggesting that even for small fragments the loss of big trees and particularly the decrease in size class of the top food species can negatively affect howler distribution in highly fragmented landscapes. These findings could be used to establish foreground conservation areas for this critically endangered subspecies in fragmented landscapes of Los Tuxtlas.     

Population Survey and Demographic Features of a Coastal Island Population of <Emphasis Type="Italic">Alouatta clamitans</Emphasis> in Atlantic Forest,Southeastern Brazil

Brown howlers (Alouatta clamitans) are endemic to the Atlantic Forest. Because only 7.5% of this fragmented forest remains in Brazil, there is an urgent need for studies of its ecology. Understanding island populations, still poorly researched in the relatively well-studied Alouatta, can provide important information for understanding habitat fragmentation and conservation. We studied brown howlers on the northern portion of the coastal and protected island, Ilha do Cardoso State Park. We used distance sampling methods on 5 transects to estimate population density of the howlers. Estimated howler density on the island is 10.6 individuals/km², with a total of 36 (21–62) individuals in a 3.4 km² area. The density is low, but similar to that of other large and preserved areas. By triangulating on vocalization and following groups, we estimate that there are 10 groups with an average of 4.5 individuals per group. Groups comprise 42% adult females, 27% adult males, 20% juveniles, 7% infants, and the remaining 4% subadult males. Howlers apparently use all appropriate habitats, including Atlantic Forest of plains and slopes. We believe that the howler population is maintaining a typical replacement on the island, with low birth rates and high survival rates, but long-term studies are required to test this. Small group size and associated social structure may be due to the particular environmental conditions on Ilha do Cardoso State Park.     

Seed predation ofCariniana estrellensis (Lecythidaceae) by black howler monkeys,Alouatta caraya

Seed predation by howler monkeys is poorly documented. Here we report the seed predation onCariniana estrellensis (Lecythidaceae) fruits by the black howler monkeyAlouatta caraya in south-east Brazil during an intense dry season. This observation suggests that even non-specialized seed predators such as howlers can use seeds in critical periods of dry season.     

Ranging Patterns of Two Syntopic Howler Monkey Species (Alouatta guariba and A. caraya) in Northeastern Argentina

To avoid competition, ecologically similar and closely related species tend to differ in their patterns of habitat use when they live in sympatry. We compared ranging patterns of brown howler (Alouatta guariba) and black and gold howler (A. caraya) monkeys living syntopically, i.e., co-occurring and overlapping their ranges in the same habitat within the zone of sympatry, in the Atlantic Forest of northeastern Argentina with the objective of evaluating whether their use of space contributes to the avoidance of interspecific competition for food resources. During 12 mo we collected data on the ranging behavior of 2 groups of each howler species. We analyzed annual and seasonal daily path lengths and movement rates, home range size, use and overlap, habitat and vertical strata use, and intergroup encounters. Black and gold howlers traveled farther and faster during the time of relative food abundance (abundant season) than during the time of relative food shortage (lean season), and their movement rates were affected by group identity and increased with the proportion of fruits in the diet. Brown howlers’ traveling patterns were not affected by any of these factors. Home ranges for both species (95% fixed kernel; brown howlers: 31–70 ha, black-and-gold howlers: 17–112 ha) were among the largest recorded for Alouatta. For both species, core areas (50% fixed kernel) were larger for larger versus smaller groups, and decreased in the lean season compared to the abundant season. Both species showed similar patterns of habitat use, except for a slight vertical stratification. Groups of different species overlapped their ranging areas consistently more and responded to one another less aggressively during encounters than groups of the same species, suggesting that interspecific spatial niche separation for these two syntopic species is not occurring. The vertical stratification, as well as a day-to-day avoidance strategy, may be the only responses of species to one another that could reduce the potentially high levels of competition for food suggested by their elevated trophic niche overlap. A high degree of niche overlap may explain the parapatric distribution of howlers and other closely related and ecologically similar species of primates.     

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.     

The Role of Minerals in Food Selection in a Black Howler Monkey (Alouatta Pigra) Population in Belize Following a Major Hurricane

As plants may contain low levels of some minerals including sodium, copper, and phosphorous, herbivores may become deficient in these nutrients. In 2001, Hurricane Iris hit the Monkey River Forest in Belize causing substantial damage to the food supply of the black howler monkey population (Alouatta pigra) living there. This included an 18‐month absence in fruit production and a complete loss of figs that are high in calcium. In this article, we describe the post‐hurricane diet of this monkey population and compare the mineral content of food items to each other and to recommendations for non‐human primates [NRC 2003]. We also investigate food selection in relation to potentially limiting minerals. Behavioral data from four groups of howlers (2002–2006) and samples of all ingested food items were collected and a sample of 99 plant from 18 food species was analyzed for mineral content. Unexpectedly, the post‐hurricane diet contained more mature leaves than new leaves despite the availability of new leaves. Leaves contained higher amounts of minerals than reproductive parts and with the exception of Cecropia peltata stems, plant parts were low in sodium. Cecropia peltata is a pioneer species that grows following habitat disturbance thus the ingestion of these stems may be a potential mechanism to avoid sodium deficiency in this damaged forest. Calcium and zinc were found above recommended values in most food items; however, both positively predicted food selection, which may reflect a difference between their abundance and their bioavailability. However, as mature leaves contained more calcium than other plant parts, their high post‐hurricane consumption may also be a response to the absence of figs and the need to find an alternate calcium source. This study highlights how habitat disturbance may affect mineral abundance and the dietary choices of primates. Am. J. Primatol. 74:1054‐1063, 2012. © 2012 Wiley Periodicals, Inc.     

Experimental technique for the conservation of private lands

A community-based sanctuary for the black howler monkey (Alouatta pigra) has been established on 18 square miles of riverine forest along the Belize river, Belize. It is based on voluntary signed pledges by subsistence farmers to abide by management plans for their lands. Conservation-education programs which impact favorably on the villagers are being carried out.     

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.     

Resource use by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas,Veracruz, Mexico

The feeding preferences of howler monkeys at their northernmost distribution in the Neotropics are reported for an annual cycle. A remarkable selectivity for 27 species representing 15 families was observed. The Moraceae and Lauraceae plant families were the most important in the diet. The howlers spent an almost equal proportion of their feeding time eating leaves and fruit, and displayed a marked preference for young leaves and mature fruit. The consumption of different plant parts was markedly seasonal and the howlers’ ranging behavior was closely associated with the availability of young leaves and mature fruit. Their home range was unusually large (ca. 60 ha) for howlers and the food species exploited occur at very low densities (93%, ≤ 4 ind/ha). They chose food items richer in protein and energy. Alkaloid compounds, present in some of the leaves, play a secondary role in their dietary selectivity.     

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.