The Ranging Costs of a Fallback Food: Liana Consumption Supplements Diet but Increases Foraging Effort in Howler Monkeys

Lianas are important components in the dynamics of tropical forests and represent fallback foods for some primates, yet little is known about their impact on primate ecology, behavior or fitness. Using 2 yr of field data, we investigated liana consumption and foraging effort in four groups of howler monkeys (two in bigger, more conserved forest fragments and two in smaller, less conserved fragments) to assess whether howler monkeys use lianas when and where food availability is scarce, and how liana consumption is related to foraging effort. Howler monkeys in smaller fragments spent more time consuming lianas and liana consumption was negatively related to the consumption of preferred food resources (fruit and Ficus spp.). Further, travel time was positively related to liana feeding time, but not to tree feeding time, and howler monkeys visited a greater number of food patches when feeding from liana leaves than when feeding from tree leaves. Our results suggest that these increases in foraging effort were related to the fact that lianas are mainly a source of leaves, and that liana patch size was probably smaller than tree patch size. While these results were clear when analyzing all four groups combined, however, they were not always significant in each of the groups individually. We suggest that this may be related to the differences in group size, patch size and the availability of resources among groups. Further studies are necessary to assess whether these dietary and behavioral adjustments negatively impact on the fitness and conservation of primates in fragments.     

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.     

Influence of the landscape matrix on the abundance of arboreal primates in fragmented landscapes

Composition of the landscape matrix of surrounding forest fragments is thought to be critically important to the survival of arboreal primates because it offers structures that help the animals move between fragments and other foraging sites. However, little is known about the composition of the matrix used by these animals. The aim of this study was to quantitatively assess the importance of the landscape matrix and its effects on primate abundance, using black howler monkeys (Alouatta pigra) living in a landscape fragmented by the expansion of agriculture and pastures for livestock in southeastern Mexico. In 2008, a complete census of the monkeys was carried out across the 2000-ha landscape matrix, and for every site where we observed monkeys, we recorded canopy height, tree basal area, food-source abundance, and distance to the nearest fragment. A total of 244 howler monkeys, distributed among 48 groups (including six solitary males) were counted in the matrix. Mean troop size was 5.6 ± 2.8 individuals, and the mode was three individuals. The highest number of troops and greatest howler monkey abundance were recorded in the isolated trees, the eucalyptus plantation, and orchards. A generalized linear model revealed that monkey abundance tended to be higher in matrix elements with higher canopy height, greater food availability, and closest to rainforest fragments. These results suggest that it is necessary to take into account the many elements of the landscape when drawing up conservation and habitat management plans, particularly in order to establish connectivity among the fragments and elements of the matrix with native trees.     

Densities of Two Frugivorous Primates with Respect to Forest and Fragment Tree Species Composition and Fruit Availability

Conservation of wildlife populations requires extensive knowledge of their habitat requirements, efficient methods to evaluate habitat quality, and an understanding of the value of fragments and edges. Kibale National Park, Uganda has areas that differ in the densities of 2 species of frugivorous monkeys—Cercopithecus mitis and Lophocebus albigena—including one on an edge and forest fragments outside the park that lack both species. We compared the basal area densities of important food trees with primate densities. The density of Cercopithecus mitis correlates most strongly with the basal area density of all types of food trees combined. The density of Lophocebus albigena does not correlate with the basal area densities of any category of food trees or with fruit availability. An index of their density—number of groups seen per km walked—correlates to fruit availability but with marginal significance. Lack of a relationship between the basal area densities of food trees and density of Lophocebus albigena may be the result of a mismatch in scale between the forest area measured and their large home ranges. We compared the unused area of forest to the other areas of the forest and the fragments and found it had higher basal area densities in all food tree categories for both species than the fragments and lower basal area densities of most categories than the other parts of the forest, indicating that the fragments are poor quality and would probably be unused even if dispersal were likely.     

Conservation Value of Landscape Supplementation for Howler Monkeys Living in Forest Patches

Many animal populations are forced to inhabit very small forest patches, which may threaten their long-term survival. In some cases, animals in these forest remnants are able to supplement their diet by using resources outside of their home patch, a process named 'landscape supplementation'. Although this is probably a key process for population survival in fragmented landscapes, little is known about the ability of most animal species to move through the matrix and feed from different landscape elements. In this paper we report several cases of landscape supplementation by two groups of Mexican mantled howler monkeys Alouatta palliata mexicana inhabiting two different forest patches in Los Tuxtlas, Mexico. Our observations show that howler monkeys used several landscape elements, such as isolated trees, live fences and neighboring forest patches to supplement their diet. These observations underline the importance of these landscape elements for the survival of forest-dependent animals in highly fragmented landscapes, as they can provide important food resources and, hence, can be considered as potential extensions of their home range. However, the degree of protection the landowner provides to howler monkeys and proper management of these landscape elements are key aspects in determining the use of these elements by these animals.     

Seasonal Variations in the Diet and Feeding Effort of Two Groups of Howlers in Different Sized Forest Fragments

Little is known about how resource limitation affects the feeding ecology of primates in forest fragments. Here, we describe seasonal variation in the diet and feeding effort of 2 groups (RH and RC3) of howlers (Alouatta palliata mexicana) living in different sized forest fragments in Los Tuxtlas, Mexico. The RH group, which lived in a larger and more preserved forest fragment, with a higher availability of fruit and Ficus trees, had a higher and more constant consumption of fruit throughout the study year. Moreover, this group fed from larger food sources, i.e., trees, lianas, and shrubs, and spent more time feeding from each food source. The feeding effort, defined as the time spent feeding and traveling divided by time spent resting, of the RH group was also significantly lower and more stable than that of the RC3 group throughout the study year. As feeding effort has been positively related to stress in primates, such increases in feeding effort could have negative consequences for howlers in small or degraded forest fragments. Our study suggests that habitat characteristics interact with plant seasonality to determine the diet and feeding effort of howlers in forest fragments and that groups living in small and degraded forest fragments may be particularly vulnerable to years of low fruit production.     

Anthropogenic edges impact howler monkey (Alouatta palliata) feeding behaviour in a Costa Rican rainforest

Anthropogenic forest fragmentation impacts many aspects of animal behaviour, including feeding ecology. With forests increasingly fragmented in tropical regions due to human development, the proportion of forest edge (≤?100 m from clear-cut regions) is higher relative to forest interior. Forest edges differ in vegetation from interior, making it important to better understand how anthropogenic edges impact the feeding behaviour of primates such as mantled howler monkeys (Alouatta palliata). We predicted that howler monkeys would feed on higher-quality plant resources, from a larger number of tree families, and from larger trees in forest interior compared to anthropogenic forest edge. We surveyed howler monkey feeding behaviour across forest zones in a fragmented rainforest in Costa Rica, La Suerte Biological Research Station. We observed individual monkeys for 30-minute periods, collecting data on their feeding behaviour and tree use at 2-minute intervals. We measured feeding trees and recorded the plant parts and taxonomy of resources consumed. Monkeys consumed more leaves and fewer stems and fed from a smaller number of tree families in the forest interior, while they consumed fewer leaves and more stems and fed from a larger number of tree families in the forest edge. Monkeys also fed from larger, taller trees in the forest interior than the edge. The differences in howler monkey feeding behaviour between forest zones attest to the impact of human disturbance on howler monkey feeding ecology.

     

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.     

High flexibility in diet and ranging patterns in two golden monkey (Cercopithecus mitis kandti) populations in Rwanda

Many primates exhibit behavioral flexibility which allows them to adapt to environmental change and different habitat types. The golden monkey (Cercopithecus mitis kandti) is a little-studied endangered primate subspecies endemic to the Virunga massif and the Gishwati forest in central Africa. In the Virunga massif, golden monkeys are mainly found in the bamboo forest, while in the Gishwati forest they live in mixed tropical montane forest. Here we describe and compare the diet of golden monkeys in both fragments. Over 24 consecutive months from January 2017 we used scan sampling to record feeding and ranging behavior of two Virunga groups and one Gishwati group totaling ca. 240 individuals. We also examined the phenology of bamboo and fruit trees, key seasonal food plant species for the monkeys. Golden monkeys fed on more than 100 plant species. The Virunga groups were mostly folivorous (between 72.8% and 87.16% of the diet) and fed mostly on young bamboo leaves and bamboo shoots, while 48.69% of the diet of the Gishwati group consisted of fruit from 22 different tree and shrub species. Bamboo shoots and fruit are seasonally available foods and were consumed regularly throughout the period when they were available. Despite being the smallest of the three study groups, the Gishwati group had a larger home range area (150.07 ha) compared to both Virunga groups (25.24 and 91.3 ha), likely driven by the differences in availability and distribution of fruit and bamboo in the habitats. Like other blue monkey subspecies, golden monkeys appear to have a flexible dietary strategy enabling them to adjust diet and ranging behavior to local habitats and available food resources. Additional studies and continuing conservation efforts are needed to better understand how variation in feeding and ranging ecology affects reproduction, population growth, and carrying capacity.     

Differences in Diet Between Spider Monkey Groups Living in Forest Fragments and Continuous Forest in Mexico

Forest fragmentation can lead to reductions in food availability, especially for some large‐bodied tropical mammals such as spider monkeys. During a 15\xE2\x80\x90mo period, we assessed the diet of Geoffroyi's spider monkey (Ateles geoffroyi) in continuous forest and fragments in the Lacandona region, southern Mexico, and related differences in diet to differences in vegetation structure and composition. We found that both forest types presented top food species for monkeys (e.g., Spondias spp., Brosimum alicastrum), but the sum of the importance value index of these species and the density of large trees were lower in fragments than in continuous forest. We also found that, compared with continuous forest, monkeys in fragments diversified their overall diet, increased consumption of leaves, and reduced the time they spent feeding on trees in favor of more time feeding on hemiepiphytes (particularly Ficus spp.) and palms, both of which were common in fragments. We attribute these changes to the relative food scarcity of the most favored feeding plants in forest fragments. Overall, our findings suggest that monkeys are able to adjust their diet to food availability in fragments, and thus persist in small‐ and medium‐sized fragments. Although it is unlikely that the small size of two of the three study fragments (14 and 31 ha) can maintain viable populations of monkeys in the long term, they may function as stepping stones, facilitating inter‐fragment movements and ultimately enhancing seed dispersal in fragmented landscapes.     

Do Forest Composition and Fruit Availability Predict Demographic Differences Among Groups of Territorial Owl Monkeys (Aotus azarai)?

Small-scale ecological variables, such as forest structure and resource availability, may affect primate groups at the scale of group home ranges, thereby influencing group demography and life-history traits. We evaluated the complete territories of 4 groups of owl monkeys (Aotus azarai), measuring and identifying all trees and lianas with a diameter at breast height ≥10 cm (n = 7485). We aimed to determine all food sources available to each of those groups and to relate food availability to group demographics. For analyses, we considered the core areas of the home range separately from the 80% home range. Our results showed that groups occupy territories that differ in size, species evenness, stem density, and food species’ stem abundances. The territories differed in the availability of fruits, flowers, and leaves, and most fruit sources were unevenly distributed in space. Differences among territories were more pronounced for the whole range than they were for the core areas. Despite marked differences among territories in structure and food availability, the number of births and age at natal dispersal were quite similar, but 1 group had a consistently lower group size. Our results suggest that owl monkey groups occupy territories of different structure and composition and food availability, yet ones that contain similar quantities of, mostly, dry season fruit sources. We propose that groups inhabit these territories to overcome food shortages safely during limiting periods, specifically the dry season, in this markedly seasonal forest. The occupancy and defense of territories with strict boundaries may therefore be associated with food resources available during limiting seasons that may be the ones influencing life history patterns and demographics.     

Ranging behavior of woolly spider monkeys,or muriquis,Brachyteles arachnoides

During a 14-month study of one group of woolly spider monkeys, or muriquis (Brachyteles arachnoides),at Fazenda Montes Claros, M. G., Brazil, the group used a home range of 168 ha. Day-range lengths averaged 1283 m and were longer in the wet season than in the dry season. An analysis of travel rates indicated that the group traveled faster on those days when they traveled farther. The availability of large patches of preferred food sources appears to affect daily movement patterns. Intraspecific comparisons, in addition to an apparent expansion of the study group’s home range as their group size has increased, suggest the importance of group size to muriqui range size. Interspecific comparisons between muriquis and sympatric brown howler monkeys suggest that locomotor adaptations are important to understanding species differences in ranging behavior.     

Diet in one group of woolly spider monkeys,or muriquis (Brachyteles arachnoides)

Data on feeding behavior in one group of muriquis (Brachyteles arachnoides) were collected during a 14 month study at Fazenda Montes Claros, Minas Gerais, Brazil. Muriquis devoted an average of 51% of their annual feeding time to leaves, 32% to fruits, and 11% to flowers. The high proportion of leaves in their diet is consistent with predictions from the energetics of body size. However, they devoted a greater proportion of their feeding time to patchy fruit and flower resources than was expected from comparisons with smaller, sympatric howler monkeys. Muriqui diet varied with the availability of preferred food types across sample months. Fruit and flower consumption corresponded to the availability and abundance of these food resources in the forest. Leaves contributed substantially to muriqui diet throughout the year but appeared to be eaten primarily to provide necessary protein and/or necessary bulk. Male and female diets differed only in the greater proportion of feeding time females devoted to flowers.     

Howler monkey tolerance to habitat shrinking: Lifetime warranty or death sentence?

Habitat loss and fragmentation are major threats to the conservation of nonhuman primates. Given that species differ in their responses to fragmented landscapes, identifying the factors that enable them to cope with altered environments or that cause their extirpation is critical to design conservation management strategies. Howler monkeys (Alouatta spp.) are good models for studying the strategies of tolerant arboreal taxa and how they cope with spatial restriction, because they live in habitats ranging from vast pristine forests to small disturbed fragments and orchards. While some aspects of their ecology and behavior are conserved, others vary in predictable ways in response to habitat shrinking and decreasing resource availability. We argue that the ability of individual howler monkeys to inhabit low-quality environments does not guarantee the long-term persistence of the small populations that live under these conditions. Their local extirpation explains why few forest fragments below a given area threshold are frequently inhabited in landscapes where recolonization and gene flow are compromised by long isolation distances or less permeable matrices. In sum, howlers’ ability to cope with habitat restriction at the individual level in the short-term may mask the inevitable fate of isolated populations, thereby compromising the persistence of the species at a regional scale in the long-term if howlers’ need for protection in large forests is undervalued.     

Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications for conservation

Accelerated deforestation is causing the rapid loss and fragmentation of primary habitat for primates. Although the genus Alouatta is one of the most studied primate taxa under these circumstances, some results are contradictory and responses of howlers to habitat fragmentation are not yet clear. In this paper, we conduct a cross-study of the available researches on mantled howlers (Alouatta palliata) in forest fragments in Los Tuxtlas, Mexico, to (1) describe the diet and activity pattern of howlers; (2) analyze the similarity in the diet across studies; and (3) relate both fragment size and howler population density with different characteristics of their diet, home range size, and activity pattern. Howlers consumed 181 plant species belonging to 54 families. Ficus was the most important taxa in the howlers' diet, followed by primary species such as Pterocarpus rohrii, Nectandra ambigens, Poulsenia armata, and Brosimum alicastrum. Secondary and non-secondary light-demanding plant species, which are representatives of disturbed habitat, contributed with a high percentage of their feeding time. Only 23% of the species consumed were the same across all the studies, suggesting that howlers adapt their diet to the food availability of their respective habitats. Population density is the best predictor of howlers' ecological and behavioral changes in response to forest fragmentation, probably owing to its relationship with food availability. Howlers respond to the increase in population densities by increasing the (1) diversity of food species in the diet; (2) consumption of non-tree growth forms; and (3) consumption of new plant items. Home range size is also predicted by population density, but fragment size is a better predictor, probably owing to the fact that howler groups can overlap their home ranges. Our results emphasize the importance of conserving the larger fragments and increasing the size of small and medium-sized ones.     

Feeding and general activity patterns of a howler monkey (Alouatta palliata) troop living in a forest fragment at Los Tuxtlas,Mexico

The feeding behavior and general activity patterns of a howler monkey troop living in a 3.6 ha forest fragment were studied at Los Tuxtlas, Mexico, for an annual cycle. Monthly samples of their feeding behavior indicated that they used 52 species of 24 plant families as sources of food. Of these, 67% were trees, which accounted for 96% of total feeding time recorded. Ten species of Moraceae, Cecropiaceae, Anacrdiaceae. and Sapotaceae contributed to 70% of the trees used and to almost 90% of feeding time. The number of plant species used per monthly record varied from 7 to 31 with an average of 19.9 species. Young leaves and ripe fruit were the principal items in the monthly diet of howlers and average percent of time spent consuming these plant parts was 46.7% and 34.8%, respectively. The use of tree species was found to be associated to their importance value and to their pattern of spatial dispersal in the study site. Availability of young leaves was fairly constant from month to month, but it presented a seasonal pattern, and there was a significantly lower number of tree species bearing ripe fruit through the year with brief pulses of production. The monthly activity pattern was found to be related to variations in the availability of young leaves and ripe fruit as well as to the values of the intermonthly overlap in plant species used. Resting and feeding presented a bimodal pattern of occurrence throughout the day that seemed to be related to variations in maximum ambient temperatures. Results are discussed in light of the small size and shape of the forest fragment inhabited by the howler troop. Am. J. Primatol. 48:167–183, 1999. © 1999 Wiley‐Liss, Inc.     

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.     

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.     

Use of space, activity patterns, and foraging behavior of red howler monkeys (Alouatta seniculus) in an Andean forest fragment in Colombia

Howler monkeys are among the most studied primates in the Neotropics, however, behavioral studies including estimation of food availability in Andean forests are scarce. During 12 months we studied habitat use, behavior, and feeding ecology of two groups of red howler monkeys (Alouatta seniculus) in an isolated fragment in the Colombian Andes. We used a combination of focal animal and instantaneous sampling. We estimated fruit production (FP) using phenology transects, and calculated young leaf abundance by observing marked trees. The home range area used by each group was 10.5 and 16.7 ha and daily distances traveled were 431 ± 228 and 458 ± 259 m, respectively. We found that both groups spent most of their time resting (62–64%). Resting time did not increase with leaf consumption as expected using a strategy of energy minimization. We did not find a relationship between daily distances traveled and leaf consumption. However, howlers consumed fruits according to their availability, and the production of young leaves did not predict feeding time on this resource. Overall, our results are similar to those found on other forest types. We found that despite limited FP in Andean forests, this did not lead to a higher intake of leaves, longer resting periods, or shorter traveling distances for red howlers. Am. J. Primatol. 73:1062–1071, 2011. © 2011 Wiley‐Liss, Inc.     

Aspects of dietary quality,nutrient assimilation and water balance in wild howler monkeys (Alouatta palliata)

Summary Wild howler monkeys were fed natural fruit and leaf diets in order to determine their ability to assimilate minerals (Ca, P, Mg, Si, Sr, Ba, Fe, Al, Mn, B, Cu, Li, V), and to assess their water and electrolyte budgets by the balance method. Results were extrapolated to the field situation so that the nutritional status of free-living monkeys could be examined in relation to their diet. The figs and young leaves of Ficus insipida and F. yoponensis trees (the most important foods in the dry season) provide adequate amounts of most required minerals, and an abundance of water. However, the copper requirement would not be met by this diet, which also provides only marginal amounts of sodium and phosphorus. These deficiencies may be corrected by consuming other available food items that are rich in Cu, Na or P. These results help explain the diversity that has been observed in the diet of wild howler monkeys, and suggest that these herbivores should feed selectively in order to obtain a nutritionally adequate diet.