Seasonal variation in the positional behavior of red howling monkeys (Alouatta seniculus)

Recent studies on the positional behavior of primates reveal that significant seasonal variation occurs in both locomotion and postures that is related to changes in diet and foraging techniques. Howling monkeys (genusAlouatta), which also have a seasonally varied diet, are predicted to have correspondingly varied positional behaviors. Two groups of red howling monkeys were studied in a primary rain forest in French Guinana during the dry and wet seasons. During the dry season, when howler diet is based mainly on leaves, howlers traveled more frequently by quadrupedal walking on large supports, a mode of progression that is probably inexpensive energetically and relatively stable. During feeding, quadrupedal and tripedal stand contributed considerably, a posture probably associated with the equal distribution of leaves within a tree crown. In contrast, during the wet season, when fruit was abundant, howlers fed very frequently by sitting on large supports, probably because fruit consumption required more time for special manipulation. However, most seasonal changes in feeding postures, and in travel and feeding locomotion, were difficult to associate directly with dietary shifts. These behavioral changes may be more highly correlated with slight modifications in microhabitat use (horizontal and vertical daily ranges, similar and alternative arboreal pathways) that are not considered in this paper.     

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.     

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.     

Diets of some French guianan primates: Food composition and food choices

We studied food choices of black spider monkeys (Ateles paniscus) and red howlers (Alouatta seniculus) in an undisturbed tropical forest of French Guiana for 6 months in the rainy season. We made additional observations on tufted capuchins (Cebus apella) and examined the differences and similarities in feeding behavior with respect to the plant specific composition of the habitat and the biochemical characteristics of their food. Capuchins and spider monkeys mainly fed on ripe fruit pulp, to which they added invertebrates (capuchins) or young leaves (spider monkeys); their plant diet was more varied than that of howlers, which contained approximately equal proportions of ripe fruits and young leaves of many species, with large monthly variations in these food categories. BothAteles andAlouatta tended to feed preferentially on abundant plant species, with a large overlap in their fruit choices. The former species included a high proportion of soluble sugars and a low proportion of protein in its diet compared, to howlers. Leaves of several species selected byAlouatta reacted positively when screened for alkaloids and phenolic compounds. Besides specific metabolic requirements and adaptations to deriving nutrients from distinct food types, we hypothesize that the ability to taste sugars, which varies among primates, affects the range of foods appearing to be palatable and, consequently, contributes to the differentiation of feeding niches.     

Diet of the brown howler monkeyAlouatta fusca in a semi-deciduous forest fragment of southeastern Brazil

The diet of a group of six brown howlers was studied weekly during 12 months in a reserve of 250 ha of secondary, mesophytic, semi-deciduous forest. The phenology of 186 trees of 72 species and 29 families was monitored simultaneously. Scan sampling was used to record the diet from dawn until dusk on a total of 60 days of observation, yielding 718 hr of animal-observer contact and 2,943 feeding scans. The diet was composed of leaves (73%), flowers (12%), and fruits (5%), from 68 identified plant species.Celtis iguanae, Cassia ferruginea, andInga spp. were the main food sources, accounting for approximately 50% of the diet. Young leaves (59%) were preferred to mature leaves (31%), trees contributing 56% and lianas 41% of the leaf diet. The ingestion of young leaves was correlated to the availability of these items, however, the correlations were not significant for flowers and fruits. The diet was poorer in fruits and richer in young leaves of lianas in comparison to other howler monkey species studies, probably as a consequence of the liana abundance in this forest fragment.     

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.     

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.     

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.     

Dietary Flexibility of the Brown Howler Monkey Throughout Its Geographic Distribution

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

Birth Seasonality in Alouatta caraya in Northern Argentina

Given appropriate ecological and social conditions, natural selection should favor individuals that can concentrate their reproductive events to a particular time of the year that offers high opportunities for infant survivorship. Previous studies on births in Alouatta caraya in Northern Argentina revealed the existence of a peak during the dry season—a period with scarcity of food resources—in mainland gallery forest (G. E. Zunino, Extra 133: 1–10, 1996). The time of conception and the period of independence of the offspring are positively correlated with precipitation, temperature and availability of food. Offspring became independent from their mothers when the availability of resources was high, and conception coincided with the peak of fruit production. Our goal was to examine patterns of birth seasonality in Alouatta caraya in flooded forest on an island in Northern Argentina for comparison with the mainland population. Both sites are at similar latitudes, but differ in forest type. The results indicate that the availability of new and mature leaves is more consistent throughout the year in the flooded forest (p<0.05); however, there was no difference in the availability of fleshy fruits between sites (p>0.05). The pattern of births differed between the gallery forest and the flooded forest (2-way Anova, p<0.001). In the flooded forest births occurred throughout the year, which supports the contentions that howlers do not have a fixed birth season and that the observed variation in the timing of births appears to represent a facultative behavioral response to changes in food availability.     

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.     

Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa

The threat that forest fragmentation and habitat loss presents for several Alouatta taxa requires us to determine the key elements that may promote the persistence of howler monkeys in forest fragments and to evaluate how changes in the availability of these elements may affect their future conservation prospects. In this study we analyzed the relationship between the availability of both big trees of top food taxa (BTTFT) (diameter at breast height>60) and fruit of top food taxa (FrTFT) in the home ranges of two groups of Alouatta palliata mexicana occupying different forest fragments in Los Tuxtlas, Mexico, and their diet and activity pattern. Both study groups preferred big trees for feeding and the group with lower availability of BTTFT in their home range fed from more, smaller food sources. Furthermore, both study groups also increased the number of food sources when their consumption of fruit decreased, and the group with lower availability of FrTFT in their home range fed from more food sources. The increase in the number of food sources used under such conditions, in turn, set up a process of higher foraging effort and lower rest. In summary, our results support other studies that suggest that the availability of big trees and fruit may be two important elements influencing the persistence of howler monkeys in forest fragments. Am. J. Primatol. 71:654–662, 2009. © 2009 Wiley‐Liss, Inc.     

Effective Solutions for Howler Conservation

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

Survey and census of howler monkeys (Alouatta palliata) in the rain forest of “Los Tuxtlas,” Veracruz,Mexico

Howler monkey troops were censused at the biological reserve “Los Tuxtlas” in Veracruz, Mexico. The reserve includes 700 ha of rain forest. Twenty howler monkeys were also trapped, measured, marked, and released. Censuses were conducted for a period of 26 months, and they indicated the existence of 17 troops. The mean troop size was 9.12 (SD ± 2.93), and mean troop composition was 3.0 adult males, 4.12 females, 1.56 juveniles, and 1.54 infants. Ecological density was 0.23 howlers/ha or 23.29 howlers/km². The male to female ratio was 1:1.37. No discrete seasonality in births was noted. Howler monkeys in this locality inhabit the northernmost limit of the neotropical rain forest. The population parameters fall within those reported for Alouatta palliata at other sites.     

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.     

Diet of Alouatta belzebul discolor in an Amazonian Rain Forest of Northern Mato Grosso State, Brazil

Prior field studies of Alouatta showed the highest frugivory in A. belzebul. During 10 mo between October 1999 and October 2000, we studied the feeding ecology of a group of 7–9 red-handed howlers (Alouatta belzebul discolor) in a primary forest on the banks of a tributary of the Teles Pires River, near Paranaíta, MT, Brazil (9°34S; 56°19W). The howlers used 3 types of habitat: upland (terra firme) forest, flood plain forest (igapó) and palm forest (açaizal). During 45 complete days of observation, the group fed on 67 plant species (N = 2039 feeding records) in 24 families. The 2 most used families were Leguminosae and Moraceae, with 17 species each. Fruits predominated (40–80%) in every month, except June, when young leaves accounted for 54% of the diet. Dialium guianense (Leguminosal, Caesalpinioideae) was the most consumed species. Flower (6%) and mature leaf (5%) consumptions were low. Tree bark, live and decayed wood, and woody twig monthly consumption varied from 0 to 26%, and occurred only in igapó, where they used mostly Macrolobium acaciaefolium (Leguminosae, Caesalpinioideae), Clitoria amazonum (Leguminosae, Papilionoideae) and Licania cf. canescens (Chrysobalanaceae). Our study on Alouatta belzebul discolor complements the high frugivory in A. b. belzebul and documents uncommon dietary items for the species. Although there is intraspecific variation in howler diets and new studies have shown higher frugivory for more folivorous species, Alouatta belzebul seems to be the most frugivorous howler species, in spite of its wide geographical distribution and, in this case, sympatry with Ateles chamek, a frugivore.     

Geographic Distribution of Red Howlers (Alouatta seniculus) in Southwestern Brazilian Amazonia, with Notes on Alouatta caraya

We surveyed howler (Alouatta) populations at 36 sites throughout the Brazilian state of Rondônia, in southwestern Amazonia, using quantitative (line transect surveys) and qualitative (interviews) methods. We recorded the red howler (Alouatta seniculus) at only one- third of the sites, and the species was relatively rare at most of them, especially in comparison with sympatric atelids (Ateles chamek and Lagothrix cana). In addition to local discontinuities, Alouatta was absent from a wide area (possibly as much as 100,000 km²) of northern Rondônia, south of the upper Madeira river. This lacuna apparently contradicts the typical association of the species with flooded forest ecosystems, but the ecological factors that may underlie it remain unclear. Competition with sympatric atelids does not appear to be a significant factor anywhere within the study area. Also, there is no evidence to suggest that the distribution patterns are related to recent human colonization of the state. We collected indirect evidence of the presence of a second howler species – Alouatta caraya – at two sites in southern Rondônia, where they are associated with highland savanna habitats and gallery forests in the Guaporé grasslands.     

Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory

Primates possess remarkably variable color vision, and the ecological and social factors shaping this variation remain heavily debated. Here, we test whether central tenants of the folivory hypothesis of routine trichromacy hold for the foraging ecology of howler monkeys. Howler monkeys (genus Alouatta) and paleotropical primates (Parvorder: Catarrhini) have independently acquired routine trichromacy through fixation of distinct mid‐ to long‐wavelength‐sensitive (M/LWS) opsin genes on the X‐chromosome. The presence of routine trichromacy in howlers, while other diurnal neotropical monkeys (Platyrrhini) possess polymorphic trichromacy, is poorly understood. A selective force proposed to explain the evolution of routine trichromacy in catarrhines—reliance on young, red leaves—has received scant attention in howlers, a gap we fill in this study. We recorded diet, sequenced M/LWS opsin genes in four social groups of Alouatta palliata, and conducted colorimetric analysis of leaves consumed in Sector Santa Rosa, Costa Rica. For a majority of food species, including Ficus trees, an important resource year‐round, young leaves were more chromatically conspicuous from mature leaves to trichromatic than to hypothetical dichromatic phenotypes. We found that 18% of opsin genes were MWS/LWS hybrids; when combined with previous research, the incidence of hybrid M/LWS opsins in this species is 13%. In visual models of food discrimination ability, the hybrid trichromatic phenotype performed slightly poorer than normal trichromacy, but substantially better than dichromacy. Our results provide support for the folivory hypothesis of routine trichromacy. Similar ecological pressures, that is, the search for young, reddish leaves, may have driven the independent evolution of routine trichromacy in primates on separate continents. We discuss our results in the context of balancing selection acting on New World monkey opsin genes and hypothesize that howlers experience stronger selection against dichromatic phenotypes than other sympatric species, which rely more heavily on cryptic foods.     

Habitat Impoverishment and Egg Predation by <Emphasis Type="Italic">Alouatta caraya</Emphasis>

Species response to habitat loss, fragmentation, or alteration ranges from intolerance and extinction to tolerance and population growth. An ability to increase trophic niche breadth is likely to play a key role in promoting tolerance to habitat change in many species. Howlers (Alouatta spp.) are good examples of these tolerant species. Researchers have related their capacity to thrive well in disturbed habitats to their ability to exploit an eclectic vegetarian diet. Despite >50,000 h of observation of habituated free-ranging groups throughout the distribution of Alouatta, no case of intentional ingestion of animal matter has ever been observed. Here, we report an unexpected trophic niche broadening for free-ranging groups of black-and-gold howlers (Alouatta caraya) living in small (≤2 ha) impoverished habitat islands in the State of Rio Grande do Sul, Brazil. We studied 3 isolated social groups (15–17, 12–14, and 5 individuals) and observed 1 of them preying on birds’ nests. We recorded 19 events of egg-eating during 2274 h of observation in 1 group and 2 suspected cases in another. Our findings highlight the dietary flexibility that characterize howlers and contrast with the widely held view that they observe a strictly vegetarian diet.