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.     

The Influence of Feeding Patch Size and Relative Fruit Density on the Foraging Behavior of the Black Spider Monkey Ateles chamek

Black spider monkey Ateles chamek foraging data from eastern Bolivia are examined in relation to the size of fruit patches and the relative fruit density within the patch. In general, spider monkeys exhibited a preference for larger fruit patches and foraged for longer and in larger subgroups as patch size and relative fruit density increased. Nevertheless, results for specific resources revealed considerable variation in the primary variables influencing foraging behavior and subgroup size with certain specific resources more influenced by patch size, and others more influenced by relative fruit density. The results are discussed in relation to the foraging ecology of fission–fusion primate social systems and previous studies on the influence of patch size on primate foraging decisions.     

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.     

Predicted and verified distributions of <Emphasis Type="Italic">Ateles geoffroyi</Emphasis> and <Emphasis Type="Italic">Alouatta palliata</Emphasis> in Oaxaca,Mexico

Primate conservation requires a better knowledge of the distributions and statuses of populations in both large areas of habitat and in areas for which we currently have no information. We focused on spider monkeys (Ateles geoffroyi) and howler monkeys (Alouatta palliata) in the state of Oaxaca, Mexico. This Mexican state has protected large tracts of forest, and has historical records for both primates, although very little is known about them. To update our knowledge of the distributions of these primates and identify potential areas in which they are present, we modeled their geographic distributions by characterizing their ecological niches using the genetic algorithm for rule-set production (GARP), performed interviews and carried out field surveys. The predicted distributions, surveys and interviews indicate that the distributions of these primates are restricted to northeastern Oaxaca. The results suggest that spider monkeys occupy a wider area and elevational range than howler monkeys. Throughout that range there is a wide variety of suitable habitats for these primates. Most of the sites where monkeys were recorded in the field are not officially protected and there was evidence of hunting and habitat destruction. It is important to improve protection, economic alternatives and environmental education as we move towards an integral solution for the conservation of these species. Validation of the GARP model was done for A. geoffroyi, since we had obtained enough field data for this species; this validation indicated that the predicted distribution of the species was statistically better than expected by chance. Hence, ecological niche modeling is a useful approach when performing an initial assessment to identify distribution patterns, detecting suitable areas for future exploration, and for conservation planning. Our findings provide an improved basis for primate conservation and productive fieldwork in Oaxaca.     

Social organization and food resources availability in primates: a socio-bioenergetic analysis of diet and disease hypotheses.

Data obtained during a field study of two species of nonhuman primates (Alouatta villosa and Ateles geoffroyi) living in the Tikal National Park in Guatemala are used to suggest an answer to the question: To what extent is the existence of a particular form of social organization (group size, structure, and composition) an indication of the amount of energy in the form of food resources available to animals in a particular habitat? Seven researchers working in teams spent 2,318 hours in the field, 1,145 hours of which were in contact with the monkeys. Comparisons of dietary data, estimated energy expenditures, and habitat productivity provide indications of the degree to which a habitat is capable of supporting the energy and other nutritional requirements of howler and spider monkeys living within the study area. These data suggest that much larger populations and different forms of social organizations can be supported by resources available within the habitat.     

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.     

Spider Monkeys (Ateles geoffroyi yucatenensis) Cope with the Negative Consequences of Hurricanes Through Changes in Diet, Activity Budget, and Fission–Fusion Dynamics

Hurricanes can bring about dramatic changes to ecosystems and adversely affect animals that live in them. We monitored behavioral responses in wild spider monkeys (Ateles geoffroyi yucatanensis) in the aftermath of two hurricanes (Emily and Wilma) that moved through the Yucatan peninsula in 2005. We predicted that the monkeys would shift their diets depending on relative food availability and experience a change in the distribution of activity patterns. Because spider monkeys’ social organization is characterized by a high degree of fission–fusion dynamics, we predicted they would form smaller subgroups subsequent to the hurricanes to mitigate competition over limited food resources. We compared their responses in the immediate aftermath of Hurricane Emily and across the dry seasons before and after both hurricanes, to control for seasonal changes, by examining their activity budgets, foods consumed, and subgrouping dynamics. In the immediate aftermath of Hurricane Emily spider monkeys spent less time moving and more time feeding on leaves than before the hurricane and they were in smaller subgroups. In the dry season after both hurricanes the monkeys spent more time resting and less time moving than before the hurricanes, and leaves replaced fruit as their primary food resource. They fused into larger subgroups less often and had smaller subgroup sizes in the dry season after than before the hurricanes. Thus, the high degree of fission–fusion dynamics of spider monkeys was instrumental in affording the behavioral flexibility critical to cope with the negative post-hurricane consequences.     

A Comparative Assessment of Hand Preference in Captive Red Howler Monkeys,Alouatta seniculus and Yellow-Breasted Capuchin Monkeys,Sapajus xanthosternos

There are two major theories that attempt to explain hand preference in non-human primates–the ‘task complexity’ theory and the ‘postural origins’ theory. In the present study, we proposed a third hypothesis to explain the evolutionary origin of hand preference in non-human primates, stating that it could have evolved owing to structural and functional adaptations to feeding, which we refer to as the ‘niche structure’ hypothesis. We attempted to explore this hypothesis by comparing hand preference across species that differ in the feeding ecology and niche structure: red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos. The red howler monkeys used the mouth to obtain food more frequently than the yellow-breasted capuchin monkeys. The red howler monkeys almost never reached for food presented on the opposite side of a wire mesh or inside a portable container, whereas the yellow-breasted capuchin monkeys reached for food presented in all four spatial arrangements (scattered, on the opposite side of a wire mesh, inside a suspended container, and inside a portable container). In contrast to the red howler monkeys that almost never acquired bipedal and clinging posture, the yellow-breasted capuchin monkeys acquired all five body postures (sitting, bipedal, tripedal, clinging, and hanging). Although there was no difference between the proportion of the red howler monkeys and the yellow-breasted capuchin monkeys that preferentially used one hand, the yellow-breasted capuchin monkeys exhibited an overall weaker hand preference than the red howler monkeys. Differences in hand preference diminished with the increasing complexity of the reaching-for-food tasks, i.e., the relatively more complex tasks were perceived as equally complex by both the red howler monkeys and the yellow-breasted capuchin monkeys. These findings suggest that species-specific differences in feeding ecology and niche structure can influence the perception of the complexity of the task and, consequently, hand preference.     

Foraging,Food Choice,and Food Processing by Sympatric Ripe-Fruit Specialists: <Emphasis Type="Italic">Lagothrix lagotricha poeppigii</Emphasis> and <Emphasis Type="Italic">Ateles belzebuth belzebuth</Emphasis>

Studies of interspecific competition and niche separation have formed some of the seminal works of ecology. I conducted an 18-mo study comparing the feeding ecologies of 2 sympatric, closely-related ripe-fruit specialists, Humboldt's woolly monkeys (Lagothrix lagotricha poeppigii), and the white-bellied spider monkeys (Ateles belzebuth belzebuth) in Amazonian Ecuador. Woolly monkeys in the terra firme forest live at roughly triple the density of spider monkeys (31 versus 11.5 animals/km²). Woolly monkeys spend 17% of their time foraging, while spider monkeys spend only 1% of their time foraging. Spider monkeys alone fed on soil and termitaria, which are rich in phosphorus. Woolly monkeys are not hard-fruit specialists. Their fruit diet is significantly more diverse than that of spider monkeys. Dietary overlap between the 2 species is high, yet each specializes to some degree on a different set of fruit resources. Woolly monkeys visit more food sources per unit of time, feed lower in the canopy, visit more small food patches, and prey on more seeds. Spider monkeys feed on fewer, richer food sources and are more than twice as likely to return to a particular fruit source than woolly monkeys are. Spider monkeys maximize fruit pulp intake, carrying more intact seeds in their guts, while woolly monkeys minimize seed bulk swallowed through more careful food processing. Surprisingly, several preferred spider monkey foods with high fat content and large seeds are avoided by woolly monkeys. I outline the different ecological dimensions involved in niche separation between the 2 species and discuss the possible impetus for their evolutionary divergence.     

Distribution Patterns of Tropical Plant Foods as an Evolutionary Stimulus to Primate Mental Development

Primates are noted for their mental abilities but the selective basis for such traits has remained obscure. It is hypothesized that the element of predictability associated with the spatial and temporal distribution patterns of plant foods in tropical forests has served to stimulate mental development in primates taking much of their food from the first trophic level. Primates able to remember the locations and phenological patterns of a wide variety of plant foods could move directly to such foods when and where available without wasting time and energy in random search. This would enhance overall foraging success by lowering procurement costs associated with a varied and patchily distributed plant diet. Membership in a cohesive social unit, that utilized the same supplying area over many consecutive generations, would also enhance foraging success by serving to transmit important information about diet to close kin. Data on the foraging behavior of howler and spider monkeys are presented to test certain implications of this hypothesis. Similar selective pressures, but applied to foods from the second trophic level, may have been of critical importance in the mental development of hominids . [primates, evolution, intelligence, plant foods, Aleles, Alouatta ]     

Down by the riverside: Riparian edge effects on three monkey species in a fragmented Costa Rican forest

Rivers represent natural edges in forests, serving as transition zones between landscapes. Natural edge effects are important to study to understand how intrinsic habitat variations affect wildlife as well as the impact of human-induced forest fragmentation. We examined the influence of riparian and anthropogenic edge on mantled howler, white-faced capuchin, Central American spider monkeys, and vegetation structure at La Suerte Biological Research Station (abbreviated as LSBRS), Costa Rica. We predicted lower monkey encounter rate, tree species richness, and median dbh at both edge types compared to interior and that monkeys would show species-specific responses to edge based on size and diet. We expected large, folivorous–frugivorous howler monkeys and small, generalist capuchins would be found at increased density in forest edge, while large, frugivorous spider monkeys would be found at decreased density in forest edge. We conducted population and vegetation surveys along interior, riparian, and anthropogenic edge transects at LSBRS and used GLMM to compare vegetation and monkey encounter rate. Tree species richness and median dbh were higher in forest interior than anthropogenic edge zones. Although spider monkey encounter rate did not vary between forest edges and interior, howler monkeys were encountered at highest density in riparian edge, while capuchins were encountered at highest density in anthropogenic edge. Our results indicate that diverse forest edges have varying effects on biota. Vegetation was negatively affected by forest edges, while monkey species showed species-specific edge preferences. Our findings suggest that riparian zones should be prioritized for conservation in Neotropical forests.     

Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis)

Competition for resources and the need for cooperation are reported to affect patterns of social interactions and thus the quality of social relationships in primates. Relationships may be described as high quality when both individuals behave in a way that benefits their partner. We investigated the distribution of a wide range of social behaviors across sex partner combinations of adult spider monkeys with specific reference to contested resources. Data were collected from two communities of wild spider monkeys (Ateles geoffroyi yucatanensis) in the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico. Affiliative behavior was exchanged most frequently between males, and as male-male aggression was rare, male-male social relationships were characterized as high quality. Female-female social relationships were best described as low quality as females showed no preference to be in proximity with other females and female-female affiliative behavior was rare. Relationships between the sexes generally were characterized by high rates of female-directed male aggression, although additional investigation into the effects of kinship and female reproductive state on male-female relationships is required before further conclusions can be drawn. Dyadic and coalitionary female-female aggression was significantly higher than expected in a feeding context, confirming that female spider monkeys primarily compete for access to food. Male-male aggression did not increase significantly when in the presence of females, but males embraced at higher rates when in mixed-sex subgroups. As embraces serve to reduce the likelihood of aggression during tense situations, high rates of male-male embraces in mixed-sex subgroups may mitigate male conflicts over access to females.     

Survey of black howler (<Emphasis Type="Italic">Alouatta pigra</Emphasis>) and spider (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>) monkeys in the Mayan sites of Calakmul and Yaxchilán,Mexico and Tikal,Guatemala

Surveys of populations of spider and howler monkeys were conducted at the Mayan sites of Calakmul and Yaxchilán, Mexico and Tikal, Guatemala. The forests in which these sites are found are part of the largest landmass of tropical rain forests present in Mesoamerica, encompassing about 4 million ha. Triangulation of monkey vocalization combined with ground surveys was used to determine the presence of howler and spider monkey groups. Howler monkey mean troop size at these sites varied from 6.6±2.1 individuals in Yaxchilán to 7.5±1.9 in Calakmul to 8.7±2.2 in Tikal. Density estimates varied from 12.8 individuals/km² in Yaxchilán to 15.2 individuals/km² in Calakmul to 17.8 individuals/km² in Tikal. Mean spider monkey subgroup size varied from 4.7±2.6 individuals in Tikal to 5.6±3.0 individuals in Yaxchilán to 7.7±3.8 individuals in Calakmul. Spider monkey density varied from 17.0 individuals/km² in Yaxchilán to 17.2 individuals/km² in Calakmul to 56.4 individuals/km² in Tikal. All sightings of both howler and spider monkeys at the three sites were in undisturbed rain forest vegetation and spider monkeys in general were more frequently sighted at higher tree heights than howlers. We discuss the value of further acquiring data on howler and spider monkey populations existing in extensive forest tracts and on the conservation value for both primate species of the forests surrounding the Mayan ruins found in this area of Mesoamerica.     

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.     

What limits primates?

Recently ecological data on spider and howler monkeys at Tikal, Guatemala, have been used in an attempt to demonstrate that primate populations are not limited by food resources. Those data are shown here to be inadequate for testing hypotheses about population limitation, and the problem of discerning limiting factors is explored.     

Group size and stability: Why do gibbons and spider monkeys differ?

Gibbons and spider monkeys have similar diets, body size, and locomotor patterns. They are therefore expected to be subject to similar socioecological rules. However their grouping patterns differ. Gibbons live in small stable groups, whereas spider monkey form unstable sub-groups that vary from small to large during different seasons. If similar principles apply to the two species, food abundance should vary more for spider monkeys than for gibbons; food density should be similar for the two species when spider monkey sub-groups are the same size as gibbon groups; and the highest level of food abundance should be higher for spider monkeys than for gibbons. These predictions are upheld for a comparison of particular populations ofHylobates muelleri andAteles geoffroyi.     

Nutritional status of free‐ranging Mexican howler monkeys (Alouatta palliata mexicana) in Veracruz,Mexico: Serum chemistry; lipoprotein profile; vitamins D,A, and E; carotenoids; and minerals

The purpose of this work was to measure important nutritional status parameters for a group of free‐ranging Mexican mantled howler monkeys (A. palliata mexicana) and compare those data to published data for primates. The nutritional status of six free‐ranging Mexican mantled howler monkeys was examined using biochemical analysis. Blood samples were analyzed for serum chemistry; lipids; vitamins D, A, and E; carotenoids; and minerals. Serum chemistries were somewhat different from published values, but did not indicate clear abnormalities. Circulating lipids were not different from those in captive primates. Circulating vitamin D metabolites (83±16.3 for 25(OH)D ng/mL; 563±53.8 for 1,25(OH)₂D pg/mL) were similar to those in wild‐caught tamarins (Saguinus oedipus), lower than some published data for captive Cebidae and Callitrichidae, and higher than for Old World primates. Serum concentrations of retinol (16.5±1.64 μg/dl) were similar to those in captive spider monkeys (Ateles geoffroyi). Retinyl palmitate and retinyl stearate was present in howler samples and may have reflected recent dietary intake. Circulating α‐tocopherol (997±97.6 μg/dl) was similar to published values for other primates. Carotenoid levels in howlers were within the ranges reported for many primates. A significant finding was the presence of cadmium in samples that should be further studied. The number of individuals sampled was limited, and further investigation into the effects of seasonality is needed. However, this information provides new data for howler monkeys and for free‐ranging primates in general. Zoo Biol 22:239–251, 2003. © 2003 Wiley‐Liss, Inc.     

Do Fruit Nutrients Affect Subgrouping Patterns in Wild Spider Monkeys (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>)?

One of the main costs of group living is feeding competition. Fission–fusion dynamics are thought to be a strategy to avoid overt competition for food resources. We tested whether food abundance and quality affected such dynamics in a species characterized by a high degree of fission–fusion dynamics. We collected data on 22 adult and subadult spider monkeys (Ateles geoffroyi) living in a large community in the protected area of Otoch Ma’ax Yetel Kooh, Yucatan, Mexico. We recorded subgroup size and fission events as well as fruit abundance during 12 mo and conducted nutritional analyses on the fruit species that the study subjects consumed most. We found no effect of fruit abundance or nutritional quality of recently visited food patches on individual fission decisions, but the amount of protein in the food patches visited over the course of the day was a good predictor of subgroup size. While the absence of support for a relationship between fruit characteristics and fission decisions may be due to the short temporal scale of the analysis, our findings relating subgroup size to the amount of protein in the visited food patches over the course of the day may be explained by individual spider monkeys attempting to obtain sufficient protein intake from their fruit-based diet.     

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.     

Foraging habits of Alouatta palliata mexicana in three forest fragments

The activity patterns and diet of howler monkeys (Alouatta palliata mexicana) were studied in 3 forest fragments in south-eastern Mexico: Playa Escondida (PLA), Agaltepec Island (AGA) and Arroyo Liza (LIZ). Intersite differences offered the opportunity to investigate the foraging adaptations of howler monkeys in response to population and habitat size. In the largest fragment (PLA), the howlers' diet was based on high-quality items (fruit and young leaves). In AGA, where the density of howlers was the highest, their diet was mostly folivorous with a marked exploitation of uncommon food items such as vines, lianas, shrubs and herbs. The dietary differences in AGA were accompanied by more time spent travelling and less time spent resting. Although LIZ was the smallest fragment and had a high howler density, the small group size and the use of energy-minimizing strategies (less time spent travelling and more time spent resting) probably allowed howlers to maintain a frugivorous diet.