Survey of Helminth Parasites in Populations of <Emphasis Type="Italic">Alouatta palliata mexicana</Emphasis> and <Emphasis Type="Italic">A. pigra</Emphasis> in Continuous and in Fragmented Habitat in Southern Mexico

The 2 howler species that occur in southern Mexico, Alouatta palliata mexicana and Alouatta pigra are endangered, mainly as a result of habitat loss and fragmentation from human activity. Little is known about the gastrointestinal parasite communities affecting their populations, and lack of baseline information for populations of howler species in continuous forest habitats, makes evaluations of gastrointestinal parasite prevalence in populations in fragmented landscapes difficult. We report the results of a one-time broad survey of gastrointestinal parasites in fecal samples of individuals from several demographically stable populations of Alouatta palliata mexicana and A. pigra existing in continuous and/or protected forests. We further report similar data for populations of both species in human-fragmented landscapes. We detected 6 parasites for each howler monkey species, but only 3 of them (Trematode I, Controrchis biliophilus, Trypanoxyuris sp.) were common to both species. While parasitic prevalence in populations of both howler species was, in general, higher in the fragmented habitat than in continuous and/or protected forests. The difference is only marginally significant in Alouatta pigra. Some parasites (Coccidia and Strongylid) only appeared in populations in fragmented landscapes. Preliminary data suggest that adult males tended to have higher parasite prevalence values than those of adult females in both howler species. Parasite prevalence is associated to average group size, but not to population density in Alouatta pigra.     

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.     

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.     

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.     

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.     

Infant–Nonmother Interactions of Free-Ranging Mantled Howlers (Alouatta palliata) in Costa Rica

Proximate and ultimate explanations of interactions between infants and nonmothers vary depending upon the relatedness of the interactors. We investigated interactions of infants and nonmothers from a 22-month continuous study and from the long-term monitoring of the mantled howler population of La Pacifica, Guanacaste Province, Costa Rica. Relatedness is low or absent in these mantled howler groups. Juvenile females appeared to practice care skills with older infants, but as most first infants died, they failed to benefit. Infant positive interactions with adults occurred with the mother and probable father. Other adult females behaved aggressively toward the youngest infants. Mothers were retentive of infants and responded negatively to these interactions, suggesting that they perceived them as threatening. Interactions with infants appear to reflect competition in groups of unrelated adults. A review of other populations of Alouatta palliata and other species of howlers indicate variability in social group size and suggest variability in intragroup relatedness. We suggest that further study will confirm that social behavior (including interactions with infants) will vary by resource availability (group size) and associated demographic patterns (male and female migration) that affect relatedness in howler social groups.     

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.     

Effects of Fruit Patch Availability on Feeding Subgroup Size and Spacing Patterns in Four Primate Species at Tinigua National Park, Colombia

We examined the effects of fruit patch size, density, and distribution on feeding subgroup size and feeding bout duration in four Neotropical primates—Lagothrix lagotricha, Ateles belzebuth, Cebus apella, and Alouatta seniculus—based on 2494 hr of focal animal sampling in Tinigua National Park, Colombia. All four species show positive correlations between patch size (tree diameter at breast height; DBH) and subgroup size (maximum number of individuals from the focal group feeding at the same time), but the determination coefficients are very low and this relationship does not seem to influence strongly the actual size of the groups. Ateles showed the weakest correlation between patch size and feeding party size, and their fission–fusion sociality is best explained as a mechanism to reduce intragroup competition rather than to adjust the subgroup size to the availability of patches. Feeding associations as well as proximal spacing patterns, in general, are more alike in species with similar ecological requirements.     

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.     

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.     

Demographic population structure of black howler monkeys in fragmented and continuous forest in Chiapas,Mexico: Implications for conservation

For wild primates, demography studies are increasingly recognized as necessary for assessing the viability of vulnerable populations experiencing rapid environmental change. In particular, anthropogenic changes such as habitat loss and fragmentation can cause ecological and behavioral changes in small, isolated populations, which may, over time, alter population density and demographic structure (age/sex classes and group composition) in fragment populations relative to continuous forest populations. We compared our study population of Endangered black howler monkeys (Alouatta pigra) in 34 forest fragments around Palenque National Park (PNP), Mexico (62 groups, 407 individuals), to the adjacent population in PNP, protected primary forest (21 groups, 134 individuals), and to previous research on black howlers in fragments in our study area (18 groups, 115 individuals). We used χ² and Mann–Whitney U tests to address the questions: (a) what is the current black howler demographic population structure in unprotected forest fragments around PNP? (b) How does it compare to PNP's stable, continuous population? (c) How has it changed over time? Compared to the PNP population, the fragment populations showed higher density, a significantly lower proportion of multimale groups, and significantly fewer adult males per group. The population's age/sex structure in the fragmented landscape has been stable over the last 17 years, but differed in a higher proportion of multifemale groups, higher density, and higher patch occupancy in the present. In the context of conservation, some of our results may be positive as they indicate possible population growth over time. However, long-term scarcity of adult males in fragments and associated effects on population demographic structure might be cause for concern, in that it may affect gene flow and genetic diversity. The scarcity of adult males might stem from males experiencing increased mortality while dispersing in the fragmented landscape, whereas females might be becoming more philopatric in fragments.     

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.     

Population trends of the mantled howler groups of La Pacifica,Guanacaste, Costa Rica

A complete survey of La Pacifica in Guanacaste Province, Costa Rica was conducted in July 1984 in order to determine whether the howler (Alouatta palliata) population had declined since 1972 as a result of deforestation. During the 6-day survey, 257 howlers were located, representing 16 different social groupings and nine solitary animals. The total number of howlers, the number and location of groups, and the age-sex composition were very similar to a 1972–1976 survey of the same population. Age-sex composition of La Pacifica howler groups was similar to those of another population of mantled howlers in Costa Rica and of populations in Mexico and in Panama, although La Pacifica had a higher mean number of adult females per group. There was no evidence to support the hypothesis that the La Pacifica howler population has declined in recent times.     

Interspecific interaction and predator avoidance behavior in response to tayra (<Emphasis Type="Italic">Eira barbara</Emphasis>) by mantled howler monkeys (<Emphasis Type="Italic">Alouatta palliata</Emphasis>)

This paper reports the response of one howler monkey group (Alouatta palliata) to a group of potential predators, the tayra (Eira barbara). The apparently successful predator avoidance behavior of the monkeys was recorded in detail. We observed a group of four adult tayras moving around theAlouatta group displaying a species-typical aggressive behavioral pattern. The two adult females of the howler group successfully chased the tayras away by repeatedly moving closer to the mustelids and even following them until the predators moved off.     

Growth of Mantled Howler Groups in a Regenerating Costa Rican Dry Forest

We examined population dynamics in mantled howlers (Alouatta palliata palliata) in a regenerating tropical dry forest in Santa Rosa National Park (SRNP), Costa Rica. The population has grown at a rate of about 7% per annum during the past decade. The growth in numbers from 342 in 1984 to 554 in 1992 reflects an increase in the number of groups (from 25 to 34) and a slight increase in their average size (from 13.6 to 16.3). Population density has increased from 4.9 to 7.9 individuals per km ². Santa Rosa's population density and group compositions are similar to those at several other mantled howler sites, but densities of mantled howlers are much higher at two other well-studied sites: La Pacifica and Barro Colorado Island (BCI). We relate the low density of howlers at Santa Rosa to local historical and ecological factors. Howler populations at high and low densities differ in average group size and sex ratio. At high population densities, groups are larger and include more adult females. The number of male howlers per group appears to be more strictly limited and less variable than the number of females is. However, there is greater variation in male group membership at Santa Rosa than at La Pacifica or BCI, and at Santa Rosa there are more generating forests available into which males and females can disperse and form new groups. We present case studies describing two ways in which new howler groups are formed, and we suggest that, compared to females and compared to males at high density sites, males are relatively advantaged in the uncrowded habitats at Santa Rosa and other low density sites.     

Parasites of Wild Howlers (Alouatta spp.)

A literature review of howler parasites provides the basis for an overview of the ecological significance of parasite surveys in primates. Within this framework, we have added insights into the interactions between primate hosts and their parasites from a long-term study in Costa Rica. We collected fecal samples from mantled howlers (Alouatta palliata) over a 9-year period (1986–1994 inclusive) and analyzed them for parasite eggs, larvae, cysts, and oocysts. We found many misperceptions inherent in the typical methodology of primate parasite surveys and in the reporting of the findings. Our work in Costa Rica suggests that a snapshot effect occurs with most surveys. A static view does not reflect the dynamic and changing ecological interaction between host and parasite. We describe some problems with parasite data analyses that emphasize the need for long-term longitudinal surveys in wild primate groups.     

Neotropical Primates in a Regenerating Costa Rican Dry Forest: A Comparison of Howler and Capuchin Population Patterns

Few data exist on how primate populations return to regenerating tropical forests. We compare the ways that two populations of neotropical monkeys, Alouatta palliata and Cebus capucinus, expanded over a 28-year period after the establishment of Santa Rosa National Park on reclaimed ranchlands in Costa Rica. We found that both howler and capuchin populations increased substantially in size subsequent to protection, but the howler population grew faster. This is likely due to their faster-paced life-history pattern than that of capuchins. The howler population increased mainly via the establishment of many new groups, whereas the capuchins expanded mainly by increasing the size of existing groups. We related this finding to the fact that capuchins are limited largely by their need to drink from water holes during the dry seasons whereas howlers are limited principally by their preference for larger-sized trees that occur in older forests. Proportions of adult male capuchins increased significantly during our study, likely due to skewed sex ratio at birth or male-biased immigration into the protected park or both factors. Our main finding is that, in as short a time period as 28 years, we can substantially enhance the size of monkey populations by allowing the regeneration of tropical forest. Furthermore, we provide a preliminary interpretation of how extrinsic factors—deforestation, hunting, crop-spraying, destruction of the watershed—and intrinsic variables, e.g., pace of reproduction; diet, differentially affect not only each species' vulnerability to extinction but also its capacity to recover when human disturbances are minimized.     

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

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

Tool use by a red howler monkey (Alouatta seniculus) towards a two-toed sloth (Choloepus didactylus)

Among New World monkeys, spontaneous tool use and object manipulation are commonly descirbed inCebus species only. We report here an occurrence of tool manipulation by a wild male red howler monkey (Alouatta seniculus), observed using a stick to softly but repeatedly hit a two toed sloth (Choloepus didactylus) resting in the same tree. The ecological context of this unusual behavior for this quiet species generally showing very little manipulative propensity is discussed.     

Primates Living Outside Protected Habitats Are More Stressed: The Case of Black Howler Monkeys in the Yucatán Peninsula

The non-invasive monitoring of glucocorticoid hormones allows for the assessment of the physiological effects of anthropogenic disturbances on wildlife. Variation in glucocorticoid levels of the same species between protected and unprotect areas seldom has been measured, and the available evidence suggests that this relationship may depend on species-specific habitat requirements and biology. In the present study we focused on black howler monkeys (Alouatta pigra), a canopy-dwelling primate species, as a case study to evaluate the physiological consequences of living in unprotected areas, and relate them with intragroup competition and competition with extragroup individuals. From February 2006 to September 2007 we collected 371 fecal samples from 21 adults belonging to five groups (two from protected and three from unprotected areas) in Campeche, Mexico. We recorded agonistic interactions within groups and encounters with other groups (1,200 h of behavioral observations), and determined fecal glucocorticoid metabolite (FGM) concentrations with radioimmunoassays. We used linear mixed models and Akaike''s information criterion to choose the best model explaining variation in FGM concentrations between protected and unprotected areas calculated from five categorical variables: habitat type (protected vs. unprotected), participation in agonistic interactions, intergroup encounters, sex and female reproductive state, and season. The best model included habitat type, the interaction between habitat type and agonism, and the interaction between habitat type and season. FGM concentrations were higher in unprotected habitats, particularly when individuals were involved in agonistic interactions; seasonal variation in FGM concentrations was only detected in protected habitats. High FGM concentrations in black howler monkeys living in unprotected habitats are associated with increased within-group food competition and probably associated with exposure to anthropogenic stressors and overall food scarcity. Because persistent high GC levels can be detrimental to health and fitness, populations living in disturbed unprotected areas may not be viable in the long-term.