Ecological niche differences betweenAlouatta palliata andCebus capucinus comparing feeding modes,branch use,and diet

During the wet season, two sympatric species of primates,Alouatta palliata (mantled howlers) andCebus capucinus (white-faced capuchins), were assayed for feeding niche differences through behavioral and habitat use patterns at Refugio de Fauna Silvestre Curu in Costa Rica. Differences in the use of relative diameter and thickness of branches and five different modes of feeding were compared between the species. White-faced capuchins used more manipulative modes of obtaining food, a wider range of arboreal habitat, and had a more diverse diet than mantled howlers. Mantled howlers may be more restricted than white-faced capuchins in arboreal microhabitat use due to their possible need for large support branches during feeding bouts and resting periods. We report that differences in feeding behaviors, diet, and arboreal habitat use seem to play a large role in separating these species niches.     

Cougar Predation on Black-and-Gold Howlers on Mutum Island,Southern Brazil<Superscript>1</Superscript>

Researchers consider predation rates by terrestrial animals to be lower in the case of arboreal primates, particularly among large-bodied species. We recorded the consumption of black-and-gold howlers (Alouatta caraya) by cougars (Puma concolor) as evidence of predation on an island of the upper Paraná River. We collected and processed fecal samples of the felid in 2004 and 2005. We identified items in the laboratory by comparison with museum specimens. We considered each species in a fecal sample as a single occurrence. Based on analysis of the cuticle scale pattern, we identified the felid as cougar. Howlers occurred in 4 out of the 8 fecal samples (40% of the occurrences). In addition to howlers, we also recorded 5 occurrences of agouti (Dasyprocta azarae; 50%) and a small unidentified sigmodontine rodent (10%). The abundance of howlers and the low forest canopy in a successional vegetation might have facilitated the predation of the large primates by a primarily terrestrial predator. The versatility of cougars is corroborated by the consumption of prey species that were abundant in the region and that were available in different forest strata, such as howlers and agoutis.     

Fruit diet of Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil: comparison of fruit type, color, and seed size

Fruit is an important food resource for neotropical primates. In this study I compare the fruit diet of sympatric brown howlers (Alouatta guariba) and southern muriquis (Brachyteles arachnoides). Feeding behavior was studied over 12 months and fruit species consumed were identified and assigned to the categories fruit type, fruit color, and seed size. Observed-fruit feeding records were compared with expected records determined from local availability of the fruit of the tree species. I also determined dietary overlap. Fruit consumption occupied 8 and 12% of the feeding time of A. guariba and B. arachnoides, respectively. Fruit from eight tree species were consumed by the former and fruit from twenty-two species by the latter. Patterns of fruit selection of A. guariba and B. arachnoides varied widely. Although howlers and muriquis converge behaviorally by selecting fruit with common attributes (fleshy/unprotected, violet and brown/black-colored), unlike A. guariba, B. arachnoides fed on immature seeds of fleshy/protected and dry fruit. Large seeds were ingested, and defecated intact, by B. arachnoides only. There was little overlap of fruit diet even within categories that had been selected by both, suggesting that dietary divergence is occurring at the interspecific level. Different resource exploitation probably mediates the coexistence of A. guariba and B. arachnoides in low diversity, semideciduous forests, where the environment imposes narrow limits on primate food choices.     

Serum Nutritional Profiles of Free-Ranging <Emphasis Type="Italic">Alouatta Caraya</Emphasis> in Northern Argentina: Lipoproteins; Amino Acids; Vitamins A,D, and E; Carotenoids; and Minerals

Quantifying circulating nutrient concentrations in sera of free-ranging subjects will help to establish a basis from which we can evaluate the nutritional status and needs of the captive population. We collected serum samples from 26 free-ranging black-and-gold howlers (Alouatta caraya) in San Cayetano forest in northern Argentina. We analyzed them for concentrations of lipoproteins; amino acids; vitamins A, D, and E; carotenoids; and minerals. There are a few significant differences between sexes in concentrations of high-density lipoprotein cholesterol, certain amino acids, vitamin E, lutein + zeaxanthin, and copper. Most nutritional parameters are similar to the ones measured in free-ranging Mexican mantled howlers (Alouatta palliata mexicana) and in captive New World primates (NWPs). Carotenoid, vitamin D, and phosphorus concentrations are the exceptions. Carotenoid concentrations are higher in free-ranging Alouatta caraya than reported for other free-ranging and captive species. Vitamin D concentrations are 14 times greater in the free-ranging black-and-gold howlers than in captive NWPs. Phosphorus concentrations are also higher than expected and higher than typically occur in captive primates, leading to a 1:1.6 calcium:phosphorus ratio. Because we based our study on a small number of free-ranging howlers, additional samples from different regions and throughout the year would better define desirable nutritional parameters for captive howlers.     

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.     

Conservation Biology of the Genus Alouatta

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

Effects of Seed Dispersal by Three Ateline Monkey Species on Seed Germination at Tinigua National Park, Colombia

We examined the effect of seed ingestion by three ateline primates: woolly monkeys, Lagothrix lagothricha; spider monkeys, Ateles belzebuth; and, red howler, Alouatta seniculus on germination rates and latency periods of seeds of several plant species in Tinigua National Park, Colombia. We collected dispersed seeds from feces and control seeds from the parental trees and washed them for germination trials. For the majority of plants, dispersed seeds germinated as well or better than control seeds did. Although spider monkeys depend more heavily on fruits than the other monkey species do, they were not more efficient than howlers or woolly monkeys at improving germination rates. A considerable proportion of the seeds dispersed by howlers and woolly monkeys showed reduced latency periods to germination, but spider monkeys showed less effect on reducing germination time. This result may be related to longer gut retention times, but such a trend has not been observed in other primate species. We conclude that, like many other primates, ateline monkeys are effective seed dispersers in terms of their effects on the seeds they swallow because they rarely decrease their germination rates. We discuss problems that make interspecific comparisons difficult, such as inappropriate control seeds and differences associated with germination substrates, and we stress the importance of studying other components of seed dispersal effectiveness.     

Telemetry System for Assessing Jaw-Muscle Function in Free-ranging Primates

In vivo laboratory-based studies describing jaw-muscle activity and mandibular bone strain during mastication provide the empirical basis for most evolutionary hypotheses linking primate masticatory apparatus form to diet. However, the laboratory data pose a potential problem for testing predictions of these hypotheses because estimates of masticatory function and performance recorded in the laboratory may lack the appropriate ecological context for understanding adaptation and evolution. For example, in laboratory studies researchers elicit rhythmic chewing using foods that may differ significantly from the diets of wild primates. Because the textural and mechanical properties of foods influence jaw-muscle activity and the resulting strains, chewing behaviors studied in the laboratory may not adequately reflect chewing behaviors of primates feeding in their natural habitats. To circumvent this limitation of laboratory-based studies of primate mastication, we developed a system for recording jaw-muscle electromyograms (EMGs) from free-ranging primates so that researchers can conduct studies of primate jaw-muscle function in vivo in the field. We used the system to record jaw-muscle EMGs from mantled howlers (Alouatta palliata) at Hacienda La Pacifica, Costa Rica. These are the first EMGs recorded from a noncaptive primate feeding in its natural habitat. Further refinements of the system will allow long-term EMG data collection so that researchers can correlate jaw-muscle function with food mechanical properties and behavioral observations. In addition to furthering understanding of primate feeding biology, our work will foster improved adaptive hypotheses explaining the evolution of primate jaw form.     

Group size in folivorous primates: ecological constraints and the possible influence of social factors

The ecological-constraints model assumes that food items occur in depletable patches and proposes that an increase in group size leads to increased day range due to more rapid patch depletion. Smaller groups become advantageous when an increase in travel costs is not repaid by an increase in energy gained or some other fitness advantage. On the other hand, we also know that group size can be influenced by social factors. Here we contrast the diet and group size of red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) in Kibale National Park, Uganda to consider how ecological and social factors are affecting their group sizes. Subsequently, we examine whether the insights gained from this detailed comparison can provide an understanding of why the social organization and group size of mantled howlers (Alouatta palliata) and black howlers (A. pigra) differ. Two groups of red colobus and two groups of black-and-white colobus were studied over 10 months. Red colobus groups were larger (48 and 24) than black-and-white colobus groups (9 and 6). The two groups of red colobus overlap home ranges with the two groups of black-and-white colobus; 75% and 95% of their home ranges were within red colobuss home range. There was a great deal of similarity in the plant parts eaten by the two species and both species fed primarily on young leaves (red colobus 70%, black-and-white colobus 76%). In terms of the actual species consumed, again there was a great deal of similarity between species. The average dietary overlap among months for the two neighboring groups of red colobus was 37.3%, while the dietary overlap between the red colobus and the black-and-white colobus group that had its home range almost entirely within the home range of the red colobus groups averaged 43.2% among months. If ecological conditions were responsible for the difference in group size between the two colobine species, one would expect the density of food trees to be lower in the home ranges of the black-and-white colobus monkeys, since they have the smaller group size. We found the opposite to be true. Both black-and-white colobus groups had more food trees and the cumulative size of those trees was greater than those in the red colobuss home ranges. We quantify how these differences parallel differences in mantled and black howlers. The average group size for mantled howlers was 12.9 individuals, and for black howlers it was 5.3 individuals. We explore possible social constraints, such as infanticide, that prevent black-and-white colobus and black howlers from living in large groups.This revised version was published online in April 2005 with corrections to the cover date of the issue.     

Interactions between tayras (<Emphasis Type="Italic">Eira barbara</Emphasis>) and red-handed howlers (<Emphasis Type="Italic">Alouatta belzebul</Emphasis>) in eastern Amazonia

Two tayras (Eira barbara) were observed attacking an infant red-handed howler (Alouatta belzebul) on an island in eastern Brazilian Amazonia, as a nearby adult male watched passively. In a separate incident, four tayras were seen attacking a subadult female on the ground. Tayras were also observed in the vicinity of the two howler study groups on a number of occasions over a 9-month period. During this same period, the two groups lost a third of their members, including infants and subadults, and the remains of six animals were found at the study site. While tayras were the only predators seen attacking the howlers, it remains unclear to what extent they were responsible for apparently high mortality rates in this high-density, isolated howler population.     

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.     

Physiological Ecology of Howlers (Alouatta): Energetic and Digestive Considerations and Comparison with the Colobinae

Remarkably little attention has been focused on the physiological ecology of free-ranging primates. Yet without such information, it may prove difficult to advance our understanding of factors influencing the dietary behavior of wild primates much beyond its present state. Mantled howlers (Alouatta palliata) have been studied in terms of some features of physiological ecology. Results of this work have helped to clarify some factors influencing howler and other primate food choices in the natural environment and have called into question various assumptions about leaf-eating primates. For example, though howlers eat considerable foliage, they do not exhibit a lower than predicted basal metabolic rate, nor do available data suggest that secondary compounds strongly influence howler food selection. Comparison of howlers with members of the Colobinae reveals some differences in features of their respective energetic and digestive physiology and raises timely issues for future research.     

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 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.     

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.     

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.     

Determination of Fecal Glucocorticoid Metabolites to Evaluate Stress Response in <Emphasis Type="Italic">Alouatta pigra</Emphasis>

Measuring fecal glucocorticoid metabolites is now a common practice to assess the stress response in primates. Nevertheless, it is important to validate the utilized immunoassay for each primate species before the technique is applied to populations in the wild. We determined the stress response of black howlers (Alouatta pigra) via 2 different group-specific enzyme immunoassays (EIAs). 11-oxoetiocholanolone EIAs are suited to assess the stress response of black howlers via fecal glucocorticoid metabolites. Levels of fecal glucocorticoid metabolites increased after we applied a stressor, i.e. anesthesia, reaching peak concentrations 24–96 h poststressor. Both basal and stress-induced fecal glucocorticoid metabolite levels showed individual variations. The increase of fecal glucocorticoid metabolites after the stressor (paralleling increases in serum) indicates that one can effectively measure adrenocortical activity in Alouatta pigra via these 2 enzyme immunoassays. However, it is important to consider individual variations in the excretion of fecal glucocorticoid metabolites when planning field endocrinological research on Alouatta pigra. Fecal glucocorticoid metabolite excretion takes 1–3 d poststressor depending on the individual. Further, there is an important individual variability in the concentrations of glucocorticoid metabolites, which might reflect differences in stress reactivity or fecal glucocorticoid metabolite metabolism and excretion.     

Seismic activity response as observed in mantled howlers (Alouatta palliata), Cuero y Salado Wildlife Refuge, Honduras

This report documents the response of wild mantled howlers (Alouatta palliata) to coseismic activity (seismic activity at the time of an earthquake). During field work on the north coast of Honduras, data were collected on a habituated troop of mantled howlers as they responded to coseismic activity. The seismic event occurred on 13 February 2001 at 0822 hours local time with a magnitude of Richter scale 6.6, focus depth of approximately 15 km at a distance of 341 km from the epicentre to the field site, Cuero y Salado. At the field site, based upon Jeffreys and Bullen (1988), body waves, noted as P and S waves, arrived at 60 and 87 s, respectively, with surface waves arriving approximately 103 s post-origin time of the seismic event. While there are three reports on non-human primate response to coseismic activity in the literature, they report on captive non-human primates. This is the first documented response on a non-captive troop. In addition, this report compares the intensity measure encountered by a wild troop of howlers and one captive group of orangutans as set out by the Modified Mercalli Intensity scale. The Modified Mercalli measure of intensity is one of two standard measures of seismic activity and rates what a person sees and feels at their location (Wood and Neumann 1931; Richter 1958). Thus, arboreal nonhuman primates are found to respond to coseismic activity ranging from Level IV to Level VI as based upon the modified Mercalli intensity scale.     

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

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