An example of “apparent” dominance-submission behavior between adult male howler monkeys (Alouatta palliata)

On Barro Colorado Island, Panama, two adult male howler monkeys (Alouatta palliata) belonging to the same troop were observed performing a sequence of behaviors typical of dominance-submission situations. The occurrence of these behaviors supports the hypothesis of an agegraded-male social organization for this species. There may also be a correlation between the appearance of these newly-reported behaviors and high population densities.     

Copulation-interrupting behavior between females within a howler monkey troop

On Barro Colorado Island, Panama, howler monkeys (Alouatta palliata) were observed copulating on numerous occasions. In one case, however, the copulation was interrupted by a female member of the same troop. This newly reported behavior may be a social mechanism related to high population densities. Supported by the Environmental Sciences Program, Smithsonian Institution; and the National Zoological Park, Washington, D.C.     

Genetic Variation of Mantled Howler Monkeys (Alouatta palliata) from Costa Rica1

We examined genetic diversity of howler monkeys (Alouatta palliata) from Costa Rica. Blood samples of howler monkeys were collected at various locations in Costa Rica, and electrophoresis of total plasma proteins yielded no variation. We also conducted starch gel electrophoresis of red cell isozymes and did not find variation for any of the 14 loci analyzed (i.e., ACP, ADA, CA2, EST, GPI, IDH, LDH‐1, LDH‐2, MDH, PGD, PGM‐1, PGM‐2, SOD, and TPI). These findings were compared with the levels of genetic variation for A. seniculus and A. belzebul from one Brazilian population. Four of the 14 isozymes (ADA, GPI, PGD, and SOD) showed more than one allele for these species. Both A. seniculus and A. belzebul from Brazil showed similar levels of genetic variation. The potential causes of the low genetic variation in A. palliata from Costa Rica are discussed.     

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.     

Tree-rubbing behavior of a solitary male howler monkey

On Barro Colorado Island, Panama, a solitary male howler monkey (Alouatta palliata) was observed copulating with a female member of a troop. A unique tree-rubbing behavior was then performed by the male. Within two weeks he was the dominant male in that troop.     

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.     

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.     

Successional loss of two key food tree species best explains decline in group size of Panamanian howler monkeys (Alouatta palliata)

Negative impacts of discrete, short‐term disturbances to wildlife populations are well‐documented. The consequences of more gradual environmental change are less apparent and harder to study because they play out over longer periods and are often indirect in their action. Yet, they can drive the decline of wildlife populations even in seemingly pristine and currently well‐protected habitats. One such environmental change is a successional shift in a community's species composition as it regenerates from disturbance caused by past human land use. Early and middle successional tree species often provide key foods to folivores and frugivores, but the abundance of these resources drops as the forest matures, with adverse repercussions for these consumers. Our 44‐year record (1974–2018) of howler monkey (Alouatta palliata) group sizes and demographic composition from Barro Colorado Island, Panama, a protected reserve, documents an example of this phenomenon. After 70 years of relative stability, the mean size of howler monkey groups exhibited a marked decline, beginning in 2003. This downward trajectory in group size has continued through the most recent census in 2018. The composition of howler groups also changed significantly during the study period, with the patterns of decline differing among age/sex classes. There is no evidence that these changes were caused by increased rates of emigration, group fission, predation, parasitism, or disease. Rather, they are best explained by an island‐wide, succession‐driven decline in the densities of two species of free‐standing fig trees, Ficus yoponensis and F. insipida, which together were providing ~36% of BCI howlers’ annual diet. Abstract in Spanish is available with online material.     

Chasing behavior between males within a howler monkey troop

On Barro Colorado Island, Panama, a mature male howler monkey (Alouatta palliata) was observed chasing a young adult male howler, both members of the same troop. Detailed observations on births, deaths and solitary males before and after the chase suggest a strong correlation between an unstable social structure within the troop and overt aggression between different-aged males. Support for this field work was received from the Environmental Sciences Program, Smithsonian Institution; and the National Zoological Park, Washington, D.C.     

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.     

Skeletal Pathologies in a Population of Alouatta palliata: Behavioral, Ecological, and Evolutionary Implications

We examined the pathological conditions in a sample of 200 skulls of Alouatta palliata recovered from Barro Colorado Island (BCI), Panama, to investigate the prevalence of disease and injury in a free-ranging monkey population. Forty-five individuals (22.5%) have some type of nondental pathological condition, indicating that illness and injury are relatively common in this population. Ten individuals, all older adult males, exhibit clear signs of antemortem trauma in the form of healed fractures. We attribute the trauma primarily to fighting, and its frequency (16.4% of adult males) contradicts previous assertions that BCI howlers are nonaggressive. Nine of the 37 scorable immature individuals (24%) have signs of a larval infestation, supporting the suggestion that ectoparasites play an important role in BCI howler mortality. Other pathological conditions in the sample include shifted muscle attachments, periostitis, arthritis, neoplasm, periapical abscesses, and facial deformity, as well as various dental abnormalities.     

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

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

Low genetic diversity and limited genetic structure across the range of the critically endangered Mexican howler monkey (Alouatta palliata mexicana)

Genetic diversity provides populations with the possibility to persist in ever-changing environments, where selective regimes change over time. Therefore, the long-term survival of a population may be affected by its level of genetic diversity. The Mexican howler monkey (Alouatta palliata mexicana) is a critically endangered primate restricted to southeast Mexico. Here, we evaluate the genetic diversity and population structure of this subspecies based on 83 individuals from 31 groups sampled across the distribution range of the subspecies, using 29 microsatellite loci. Our results revealed extremely low genetic diversity (H_O = 0.21, H_E = 0.29) compared to studies of other A. palliata populations and to other Alouatta species. Principal component analysis, a Bayesian clustering method, and analyses of molecular variance did not detect strong signatures of genetic differentiation among geographic populations of this subspecies. Although we detect small but significant F_ST values between populations, they can be explained by a pattern of isolation by distance. These results and the presence of unique alleles in different populations highlight the importance of implementing conservation efforts in multiple populations across the distribution range of A. p. mexicana to preserve its already low genetic diversity. This is especially important given current levels of population isolation due to the extreme habitat fragmentation across the distribution range of this primate.     

Intragroup Social Relationships of Male Alouatta palliata on Barro Colorado Island,Republic of Panama

We examined social and spatial relations of adult males in one group of mantled howling monkeys (Alouatta palliata) on Barro Colorado Island (BCI) in central Panama to document patterns of association. Beyond the existence of an alpha male, we could not distinguish any linear dominance hierarchy among the 6 study males. All males copulated with estrous females. Our findings contrast with reports of intragroup male behavior in Costa Rican howlers. Study males engaged in little or no affiliative or agonistic behavior with one another, but engaged in significantly more such interactions with females. The alpha male, the oldest male and a younger male were most frequently in association with females. Of group males, the oldest male associated significantly more with other males. Overall, male behavior in mantled howling monkeys on BCI generally followed the van Hooff and van Schaik (1994) model of male relationships. The low incidence of intragroup social interactions of any type in the focal males may reflect the energetic costs of social behavior. We suggest that intragroup social relationships among mantled howler males are structured by more subtle means than overt physical interactions, possibly including vocal communication, relationships with individual group females, and kinship.     

Is Meat Flavor a Factor in Hunters’ Prey Choice Decisions?

By focusing on the caloric composition of hunted prey species, optimal foraging research has shown that hunters usually make economically rational prey choice decisions. However, research by meat scientists suggests that the gustatory appeal of wildlife meats may vary dramatically. In this study, behavioral research indicates that Mayangna and Miskito hunters in Nicaragua inconsistently pursue multiple prey types in the optimal diet set. We use cognitive methods, including unconstrained pile sorts and cultural consensus analysis, to investigate the hypothesis that these partial preferences are influenced by considerations of meat flavor. Native informants exhibit high agreement on the relative appeal of different meats. Given the absence of other noteworthy differences between spider monkeys (Ateles geoffroyi) and howler monkeys (Alouatta palliata), the unappealing flavor of howler monkeys seems to be a factor in the partial preference for this species.     

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.     

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.     

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.

     

Group activity and population dynamics of the howler monkey on Barro Colorado Island

The mantled howler monkey (Alouatta palliata) of Barro Colorado Island, Panama Canal Zone, was studied in the late rainy season of 1970. Group ranges, group activity patterns and population size and structure were recorded for six groups in a 204 hectare study area. A new trail survey method was introduced to determine the population size of the entire island. Using this method, a population of 923±125 animals is estimated. Factors affecting group stability and group density are discussed. Rainfall appears to be a major determinant of howler activity and group movement in the late rainy season.     

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.