Howler Monkey Species Research Articles

Does home range use explain the relationship between group size and parasitism? A test with two sympatric species of howler monkeys

Group size is related to parasite infections in primates. This relationship probably reflects the fact that group size is associated with body contact between group members and with contact with contaminated items in the environment. The latter is highly associated with range use. In the present study we hypothesized that if infection by directly transmitted parasites (DTP) is mainly determined by the exposure of individuals to parasites that accumulate in the environment, and group size correlates negatively with the intensity of home range use, then smaller groups should be more infected by DTP. Additionally, groups that share a higher proportion of their home range with other groups should be more infected. To test our hypothesis we observed and collected fecal samples of two groups of Alouatta palliata (large group size) and two groups of A. pigra (small group size) that live sympatrically in a forest fragment located in Macuspana (Mexico). Group size was positively correlated with range area size and negatively correlated with the intensity of home range use. Range use variables were not related to either DTP prevalence or load. However, there were significant differences in DTP loads between groups, which were positively correlated with group size. Our results suggest that the intensity of home range use is a poor predictor of DTP infection parameters in groups with marked differences in size. Therefore, it is possible that the individual or combined effects of other ecological (e.g., microclimate), social (e.g., contact rate), or physiological (e.g., immune function) factors are more important in the dynamics of DTP in free-ranging primates.

Seed dispersal patterns in two closely related howler monkey species (<i>Alouatta palliata</i> and <i>A. pigra</i>): a preliminary report of differences in fruit consumption, traveling behavior, and associated dung beetle assemblages

Two-phased seed dispersal by primates and dung beetles is crucial for tropical rainforest regeneration. Two species of howler monkey exist in the tropical rainforests of southern Mexico: the mantled howler monkey (Alouatta palliata), and the black howler monkey (A. pigra). Differences between these species in foraging and traveling behavior, as well as associated dung beetle assemblages, may influence seed dispersal patterns. In this paper we present the results of a preliminary four-month study comparing the above aspects between a group of A. palliata (N = 15) in Los Tuxtlas, Veracruz and a group of A. pigra (N = 7) in Palenque National Park, Chiapas, Mexico. We observed each group in alternating months using focal sampling, fecal examination, and trapping of dung beetles. Results showed that the A. palliata group consumed more mature fruit, but both groups dispersed similar numbers of seeds over the study period (ca. 13,000 seeds). The total number of seed species collected from the feces of the A. palliata group was lower than for the A. pigra group (13 vs. 31 species). The A. palliata group had a larger home range (33 vs. 6.25 ha) and average day range (202 vs. 126 m). More dung beetles from more species were associated with the A. palliata group (357 v. 99 beetles, 16 v. 8 species). The A. palliata group attracted more ball-rolling dung beetles (75.1% of total), while the A. pigra group attracted more burrowers (80.8% of total). Our results suggest important differences between black and mantled howler monkeys of southern Mexico as seed dispersers and highlight the need to consider foraging and ranging patterns, as well as associated secondary dispersers, when assessing seed dispersal by primates.

Coalescent analysis of mtDNA indicates Pleistocene divergence among three species of howler monkey (Alouatta spp.) and population subdivision within the Atlantic Coastal Forest species, A. guariba

We have used coalescent analysis of mtDNA cytochrome b (cyt b) sequences to estimate times of divergence of three species of Alouatta--A. caraya, A. belzebul, and A. guariba--which are in close geographic proximity. A. caraya is inferred to have diverged from the A. guariba/A. belzebul clade approximately 3.83 million years ago (MYA), with the later pair diverging approximately 1.55 MYA. These dates are much more recent than previous dates based on molecular-clock methods. In addition, analyses of new sequences from the Atlantic Coastal Forest species A. guariba indicate the presence of two distinct haplogroups corresponding to northern and southern populations with both haplogroups occurring in sympatry within Sao Paulo state. The time of divergence of these two haplogroups is estimated to be 1.2 MYA and so follows quite closely after the divergence of A. guariba and A. belzebul. These more recent dates point to the importance of Pleistocene environmental events as important factors in the diversification of A. belzebul and A. guariba. We discuss the diversification of the three Alouatta species in the context of recent models of climatic change and with regard to recent molecular phylogeographic analyses of other animal groups distributed in Brazil.

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

Two yellow fever outbreaks (YFOs) occurred 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.

Are howler monkey species ecologically equivalent? Trophic niche overlap in syntopicAlouatta guariba clamitansandAlouatta caraya

According to the principle of competitive exclusion, niche differentiation allows the stable coexistence of closely related species. We analyzed dietary profile and diversity, and dietary overlap between syntopic brown howlers (BR; Alouatta guariba clamitans) and black and gold howlers (BLG; A. caraya) in the Atlantic Forest of NE Argentina, with the objective of evaluating the degree of trophic niche overlap and potential interspecific competition for food. During 12 months, we collected data on feeding behavior of two groups of each howler species using the scan sampling method, together with data on food availability. Both at the group- and species-level, we analyzed feeding behavior in terms of monthly percentages of time spent feeding on each food type and specific food item, dietary diversity (Shannon index H'), and we estimated dietary overlap using the percentage index and the Morisita-Horn index (C(H)). Across months, both howlers showed species-specific preferences for certain food items, and BLG had a more diverse diet (mean+/-SE, H'=2.77+/-0.08) than BR (H'=2.39+/-0.09). However, diets of both species overlapped extensively (percentage index=45.64+/-2.97%; C(H)=0.6+/-0.05) and diets of conspecific groups did not overlap more than diets of groups of different species. Given their high degree of trophic overlap, syntopic BR and BLG meet one of the conditions necessary for interspecific food competition to occur. Although at present we lack direct evidence for interspecific competition in these howler species, we conclude that high levels of niche overlap may have an important role in maintaining the essentially parapatric distribution of howler species throughout the Neotropics.

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 degrees 33'50''-29 degrees 35'10''S, 54 degrees 58'40''-54 degrees 59'50''W; approximately 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.

Seed Dispersal and Ingestion of Insect‐Infested Seeds by Black Howler Monkeys in Flooded Forests of the Parana River, Argentina

ABSTRACTAll howler monkey species (Alouatta spp.) have a folivorous–frugivorous diet. Howler monkeys are reported to be seed dispersers in several areas, including black howlers (Alouatta caraya), which are important seed dispersers in northern Argentinean forests. The goal of this work was to study the three‐way interaction between insects, seeds, and black howlers, and assess the functional significance of this tri‐trophic interaction for seed dispersal. I determined through direct observation that fruits of species with a high proportion of insect infestation were important components of howler monkey diet. Ocotea diospyrifolia seeds from fresh faeces of black howlers contained dead larvae, but seeds were still able to germinate. Seeds in which larvae had reached an advanced stage of development did not germinate. Larvae of infested Eugenia punicifolia fruits were killed by digestion when they occurred in the pulp early in the fruiting season, but were dispersed alive with seeds later in the season. Banara arguta fruits contained both healthy and infested seeds; infested seeds were destroyed during digestion, while healthy seeds were dispersed. Black howlers' ingestion of infested fruits could result in the: (1) killing of larvae and dispersion of healthy seeds; (2) spread of larvae; or (3) destruction of infested seeds. This will depend on the relationship between the time at which fruit is consumed by black howlers, the time at which insect infestation occurs, and also probably on the hardness of the seed coat and the seed–insect size ratio.

Survey of Helminth Parasites in Populations of Alouatta palliata mexicana and A. pigra 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.

The Roaring of Southern Brown Howler Monkeys (Alouatta guariba clamitans) as a Mechanism of Active Defence of Borders

Our study aimed to understand the function(s) of roars of southern brown howler monkeys (Alouatta guariba clamitans). The study group called almost exclusively on its range borders and preferentially on early mornings, but with no dawn peak. Intergroup encounters were associated with 88% of all sessions. Predation deterrence and regulation of access to mating partners do not seem compatible with our findings, but more work is needed to reject the latter hypothesis. Their roars seem to be related to intergroup spacing, but through an active defence of borders, instead of mutual avoidance or regular advertisement of occupancy, as proposed for other howler monkey species.

Distribution of the black howler monkey (<i>Alouatta pigra</i>) and the mantled howler monkey (<i>A. palliata</i>) in their contact zone in eastern Guatemala

We studied the geographic distribution of the endangered black howler monkey, Alouatta pigra, in its southeastern range in eastern Guatemala along its putative contact zone with the mantled howler monkey, A. palliata. A distributional survey of both species was conducted through direct observations and interviews, and the data analyzed with GIS to detect potentially limiting geographic and ecological factors. Alouatta pigra was not associated with any specific vegetation type or altitudinal range, as it occurred in many forest types from the lowlands up to elevations of 2705 m a.s.l., in contrast to prior reports of it being restricted to elevations below 400 m a.s.l. and having a strong affinity for riverine forests. Alouatta palliata did not occur at the higher elevations. Distribution of both howler monkey species was unaffected by the presence of Ateles, by protection status of the survey site, or by hunting activities. Deforestation appears to have restricted both species in some areas. Throughout the southeastern range of A. pigra, we found no evidence for current sympatry with A. palliata, as their distributions are separated by a river barrier and unsuitable dry shrubland. Ecological preferences also seem to reinforce allopatry, with only A. pigra occurring in wet and cold montane forests of the Sierra de las Minas. Our data indicate that highland habitats in Mexico and Guatemala, previously considered unsuitable for A. pigra, may need to be evaluated for distribution assessments and management plans. Populations of A. pigra in the diverse protected ecosystems in eastern Guatemala may be an important component for conservation of the species.

Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys.

Vertebrate pheromones are water-soluble chemicals perceived mainly by the vomeronasal organ (VNO) for intraspecific communications. Humans, apes, and Old World (OW) monkeys lack functional genes responsible for the pheromone signal transduction and are generally insensitive to vomeronasal pheromones. It has been hypothesized that the evolutionary deterioration of pheromone sensitivity occurred because pheromone communication became redundant after the emergence of full trichromatic color vision via the duplication of the X-chromosome-linked red/green opsin gene in the common ancestor of hominoids and OW monkeys. Interestingly, full trichromacy also evolved in the New World (NW) howler monkeys via an independent duplication of the same gene. Here we sequenced from three species of howler monkeys an essential component of the VNO pheromone transduction pathway, the gene encoding the ion channel TRP2. In contrast to those of hominoids and OW monkeys, the howler TRP2 sequences have none of the characteristics of pseudogenes. This and other observations indicate that howler monkeys have maintained both their systems of pheromone communication and full trichromatic vision, suggesting that the presence of full trichromacy alone does not lead to the loss of pheromone communication. We suggest that the ecological differences between OW and NW primates, particularly in habitat selection, may have also affected the evolution of pheromone perception.

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 3 Ma, 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.

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.

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.

The Systematic Status of the Black Howler Monkey, Alouatta Pigra Lawrence

An apparent case of sympatry between two supposed races of Alouatta pallida (Gray) was discovered near Macuspana, Tabasco, Mexico. Howler monkeys in the Tabascan series were easily separated into two distinct groups based on various characteristics of the cranium, dentition, and pelage. Further comparisons revealed that these two groups were identifiable as Alouatta palliata mexicana Merriam and Alouatta palliata pigra Lawrence. Several possible interpretations of this situation are discussed and, in view of the observed sympatry and distinctive morphological differences, pigra is elevated to specific status; the systematic status of Ahuatta villosa (Gray) also is discussed. Several admittedly speculative explanations are offered to account for the existence of two distinct species of howler monkeys in Middle America.

The susceptibility of howler monkeys to yellow fever virus.

Summary 1. Two species of Brazilian howler monkeys were found to be highly susceptible to the Olímpio Cristo strain of yellow fever virus when transmitted by mosquito bite. 2. Four cyclic transmissions were obtained with A. scapularis and three with A. leucocelaenus. 3. The facility with which laboratory transmissions were obtained with A. scapularis suggests a possible explanation for the survival of virus in the winter months in south Brazil.