Infant hybrids in a newly formed mixed-species group of howler monkeys (Alouatta guariba clamitans and Alouatta caraya) in northeastern Argentina

Natural hybridisation between species has been reported in several primate taxa. In the Neotropics, there is increasing evidence of this phenomenon in howler monkeys (genus Alouatta) in contact zones between species. We describe the first known case of formation of a mixed-species group, and two cases of putative infant hybrids between the brown howler (Alouatta guariba clamitans) and the black howler (A. caraya) in Misiones, Argentina. For 2 years, we followed a group consisting of one adult male and two adult female brown howlers and one adult female black howler. The adult female black howler was observed to copulate twice with brown howler males, and never with black howler males. In December 2006, this female was carrying an infant with a hybrid morphotype. This infant died at approximately 1.5 months of age. In November 2007, the same female had another putative hybrid newborn. This infant male died together with all members of his group during a yellow fever outbreak in early 2008. The lower frequency of mixed-species groups and hybrids at our site compared with other contact zones reported in the literature, suggests that the incidence of natural hybridisation between howler species differs depending on local factors such as population demography and landscape fragmentation.     

Mandible/basihyal relationships in red howler monkeys (Alouatta seniculus): A craniometrical approach

The morphological relationships between the cranium and basihyal of red howler monkeys (Alouatta seniculus) were analyzed based on measurements of 36 cranial and 3 basihyal dimensions and observations of the female specimen in spirits. In this study, 115 crania from 111 red howler monkeys and 4 mantled howler monkeys (Alouatta palliata) were used. The analyses from the standpoints of the correlation coefficients, principal component analysis, discriminant function analysis, age changes and sex differences were performed and the following results were obtained: (1) The cranial measurements closely related to the basihyal measurements were mandibular length, occipital breadth, facial length, ramus height, cranial base length, bigonial breadth and pr-i length. (2) Age changes for the mandibular measurements in males of red howler monkeys were remarkable, and, in particular, the development of the gonion toward posterior and lateral directions were characteristic. (3) The largest sex differences were found in the mandibular measurements of red howler monkeys among the Anthropoidea of seven genera compared. (4) The existence of a “cline” in the cranial measurements of the red howler monkey was recognized. (5) The inter-species differences in the crania between the red howler monkey and mantled howler monkey are obvious, metrically and non-metrically. Based on the results mentioned above, the morphological relationships between the mandible and basihyal in the red howler monkey are discussed.     

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.     

Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus).

We monitored the birth patterns of sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus) during a 4‐yr period from October 1996 to August 2000 at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Brown howler monkey births (n = 34) occurred throughout the year, and birth frequencies did not differ between rainy and dry season months. The aseasonal birth patterns of the howler monkeys differed significantly from the dry season concentration and dry month peak in muriqui births (n = 23). We found no effects of infant sex or the number of females on interbirth intervals (IBIs) in our 10 howler monkey study troops. IBIs of brown howler monkeys averaged 21.2 ± 2.5 mo (n = 8, median = 21.0 mo), and were significantly shorter following dry season births than rainy season births. Their IBIs and yearling survivorship (74%) were similar to those reported for other species of howler monkeys, but yearling survivorship was much lower than that of muriquis (94%), whose IBIs were more than 12 mo longer than those of the howler monkeys. Our study extends comparative knowledge of birth patterns in Alouatta to a poorly known species, and provides insights into the different ways in which diet and life history may affect the timing of births in large‐bodied platyrrhines under the same seasonal ecological conditions. Am. J. Primatol. 55:87–100, 2001. © 2001 Wiley‐Liss, Inc.     

Male Relationships and Infant Deaths in Red Howler Monkeys (Alouatta seniculus)

For decades howler monkeys were considered to be among the most peaceful animals. Recent investigators, however, have noted that, although male aggression is rare, it may be extremely severe; the criteria used to quantify howler relationships should therefore be different from those used for other primates. This paper describes the pattern of male relationships in the red howler monkey Alouatta seniculus, and examines its effect on reproductive success within the troop and the ability of troop males to resist intrusion by competing males. 4 of the 8 infants born during the study period were killed or disappeared when change occurred in relative status between two adult males.     

Molecular systematics and biogeography of the Neotropical monkey genus,Alouatta

We take advantage of the broad distribution of howler monkeys from Mexico to Argentina to provide a historical biogeographical analysis on a regional scale that encompasses the entire Neotropics. The phylogenetic relationships among 9 of the 10 recognized Alouatta species were inferred using three mitochondrial and two nuclear genes. The nuclear gene regions provided no phylogenetic resolution among howler monkey species, and were characterized by very low levels of sequence divergence between Alouatta and the Ateles outgroup. The mtDNA genes, on the other hand, produced a well-resolved phylogeny, which indicated that the earliest split among howler monkeys separated cis- and trans-Andean clades. Eight monophyletic mtDNA haplotype clades were identified, representing six named species in South America, including Alouatta seniculus, Alouatta sara, Alouatta macconelli, Alouatta caraya, Alouatta belzebul, and Alouatta guariba, and two in Mesoamerica, Alouatta pigra and Alouatta palliata. Molecular clock-based estimates of branching times indicated that contemporary howler monkey species originated in the late Miocene and Pliocene, not the Pleistocene. The causes of Alouatta diversification were more difficult to pin down, although we posit that the initial cis-, trans-Andean split in the genus was caused by the late Miocene completion of the northern Andes. Riverine barriers to dispersal and putative forest refuges can neither be discounted nor distinguished as causes of speciation in many cases, and one, the other or both have likely played a role in the diversification of South American howler monkeys. Finally, we estimated the separation of Mesoamerican A. pigra and A. palliata at 3Ma, which corresponds to the completion date of the Panama Isthmus promoting a role for this earth history event in the speciation of Central American howler monkeys.     

Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest

This paper presents and discusses aspects of fruit selectivity by red howler monkeys (Alouatta seniculus) in relation with morphological characteristics of fruits. These data are used to provide an answer to the following questions: which are the fruit characteristics that lead fruit choice of howler monkeys and to what extent fruit characteristics play a role in seed dispersal by monkeys? The frugivorous diet of a troop of red howler monkeys was determined during a 2-year field study in French Guiana. The selection of fruit by howler monkeys was analyzed in relation to the fruit availability. Results showed that, although consumption followed availability, fruit species could be classified in three categories according to their selection ratio (percentage of consumption/percentage of abundance) as “high ranking,” “middle ranking,” and “low ranking” species. Also, the 97 species of fruit eaten by the monkeys were grouped according to the morphological characteristics thought to influence the monkeys' choice. This showed that howler monkeys consumed essentially fruits with juicy pulp, bright color, and a small number of well-protected seeds. Most of high ranking species had medium-sized fruits with yellow color, and low ranking species often had small fruits. However, howler monkeys are associated with the dispersal of seeds from fruit with a hard and indehiscent pericarp and/or large seeds, like those of the Sapotaceae family. Consequently, they can be considered as “specialized” frugivores for this fruit syndrome. © l996 Wiley-Liss, Inc.     

Seed predation ofCariniana estrellensis (Lecythidaceae) by black howler monkeys,Alouatta caraya

Seed predation by howler monkeys is poorly documented. Here we report the seed predation onCariniana estrellensis (Lecythidaceae) fruits by the black howler monkeyAlouatta caraya in south-east Brazil during an intense dry season. This observation suggests that even non-specialized seed predators such as howlers can use seeds in critical periods of dry season.     

Squirrel monkey cytomegalovirus antibodies in free-ranging black howler monkeys (Alouatta caraya), Misiones, Argentina

Serum from four black howler monkeys (Alouatta caraya) was screened for antibodies to seven viruses by dot immunoassay. Cytomegalovirus antibodies were detected in three of four individuals and provide the first evidence of exposure by black howler monkeys to this virus.     

Tropical rain forest fragmentation,howler monkeys (Alouatta palliata), and dung beetles at Los Tuxtlas,Mexico

In Neotropical rain forests, fresh mammal dung, especially that of howler monkeys, constitutes an important resource used by dung beetles as food and for oviposition and further feeding by their larvae. Tropical rain forest destruction, fragmentation, and subsequent isolation causing reductions in numbers of and the disappearance of howler moneys may result in decreasing numbers of dung beetles, but this has not been documented. In this study, we present information on the presence of howlers and dung beetles in 38 isolated forest fragments and 15 agricultural habitats. Howler monkeys were censused by visual means, while dung beetles were sampled with traps baited with a mixture of howler, cow, horse, and dog dung. Results indicated that loss of area and isolation of forest fragments result in significant decrements in howlers and dung beetles. However, dung beetle abundance was found to be closely related to the presence of howler monkeys at the sites and habitats investigated. Scenarios of land management designed to reduce isolation among forest fragments may help sustain populations of howler monkeys and dung beetles, which may have positive consequences for rain forest regeneration. Am. J. Primatol. 48:253–262, 1999. © 1999 Wiley‐Liss, Inc.     

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

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

     

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.     

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.     

Survey of Alouatta caraya, the black-and-gold howler monkey, and Alouatta guariba clamitans, the brown howler monkey, in a contact zone, State of Rio Grande do Sul, Brazil: evidence for hybridization

Sympatry and natural hybridization between howler monkey taxa (Alouatta spp.) has only recently being confirmed in the wild. Surveys in areas of potential contact between the distribution of two taxa have shown that sympatry is rare, although more common than previously known. Here we report the results of a survey conducted in a contact zone between the only two sexually dichromatic howler monkey taxa, Alouatta caraya and A. guariba clamitans, in São Francisco de Assis, State of Rio Grande do Sul, Brazil. Our survey, covering an area of about 400 ha at the Cerro dos Negros (29°33′50″–29°35′10″S, 54°58′40″–54°59′50″W; ~100–279 m a.s.l.), was successful in locating seven black-and-gold and one brown howler monkey social groups living syntopically. Black-and-gold group size ranged from 5 to 15 individuals, whereas the brown group was composed of 7 individuals. The pelage color of three adult males belonging to different black-and-gold groups and another adult male belonging to the brown howler group presented a mosaic of red or rufous and black. These adult males and an adult female living in another black-and-gold group are putative hybrids. Therefore, it appears that pre-zygotic reproductive isolation has not evolved, at least not completely, between these howler monkey species, corroborating previous reports for these and other Alouatta taxa. Future genetic studies need to confirm the occurrence of hybridization in this contact zone, and to determine the viability and fertility of hybrids and their possible offspring. In addition, there is no evidence supporting the existence of significant segregation in habitat and resource utilization by black-and-gold and brown howler monkeys.     

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.     

Seasonal and age-related differential mortality by sex in the Mantled Howler monkey,Alouatta palliata

Age-specific, differential mortality occurs between male and female mantled howler monkeys, Alouatta palliata,on Barro Colorado Island, Panama. A peak in mortality between 5 and 7 years is seen in males but not infernales. Dates when howler cadavers have been found suggest a seasonal mortality, with peaks in July and perhaps also in December through January.     

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.     

A case of adoption of a howler monkey infant (Alouatta villosa) by a female spider monkey (Ateles geoffroyi)

A case of adoption of a 1-month-old howler infant by an adult female spider monkey living in captivity and its development over a six-month period are reported. The female had adopted a spider monkey infant two years before the interspecific adoption reported here. The female displayed a strong maternal response toward the howler infant and also produced milk and fed the infant.     

Population of the black howler monkey (Alouatta pigra) in a fragmented landscape in Palenque,Chiapas, Mexico

Little is known about the population characteristics of Alouatta pigra under conditions of forest fragmentation-information that is important to understanding its tolerance to habitat loss. In this work we present data on forest loss and on troop size, age, and sex composition for a population of black howler monkeys existing in the fragmented landscape surrounding the Mayan site of Palenque, Chiapas, Mexico. Two aerial photos (1:70,000) of the study area (261 km(2)) taken in 1984 and 2001 were examined to assess forest loss. Between June and December 2001 and January and March 2002 we surveyed 44 forest fragments for the presence of howler monkeys. Examination of aerial photos showed that 33% of the forest present in 1984 had disappeared by 2001, and detected an increment in the number of forest fragments present in the landscape. We discovered a total of 115 howler monkeys living in 22 of the 44 forest fragments studied, of which 107 were members of 18 troops. The rest were solitary males or small groups of males living in isolated forest fragments. Troop size ranged from two to 15 individuals (mean 5.9+3.0 ind). 31% and 15% of individuals in the troops were juveniles and infants, respectively, suggesting continued reproductive activity. Howler monkey troops in the forest fragments were on average smaller (5.9+/-3.0 ind) than troops in the nearby protected forest of the Mayan site (7.0+/-2.8 ind). The mean density of howlers in the forest fragments was 119+/-82.9 ind/km(2). The establishment of corridors is suggested as a possible conservation scenario for the fragmented howler population investigated, and as a conservation measure to connect this population with the howler population found in the protected forest of the Mayan site.