Fruit eating and seed dispersal by howling monkeys (Alouatta palliata) in the tropical rain forest of Los Tuxtlas,Mexico

The frugivory and ranging habits of howling monkeys living in the rain forest of Los Tuxtlas, Veracruz, Mexico, were studied for 5 consecutive years with the aim of investigating the role of seed dispersal agents played by the howling monkeys. The howling monkeys' consumption of fruit occupied half of their feeding time, and 80% of this time was spent feeding on mature fruit. Observations confirmed use of 19 tree species and a preference for a few species of Moraceae and Lauraceae. Fruit exploitation was very seasonal; only two species provided fruit year-round. Home range size was about 60 ha, and animals in the troop (N = 16) showed a day range of 10–893 m. Monthly collection of fecal samples during 2 years indicated that 90% of the seeds (N = 7,928) in the samples belonged to eight tree species and to one liana; the rest belonged to 15 unidentified species of vines. Germination success for the seeds in the feces was about 60% and for control seeds was 35%. Howling monkeys created diverse seed shadows in the vicinity of their leaf and fruit sources, and while they dispersed the seeds of some plant species, they also produced a great deal of fruit and seed waste for others.     

Longitudinal Assessment of Immature-to-Adult Ratios in Two Groups of Costa Rican Alouatta palliata

We used immature-to-adult female ratios (IFR), which indicate replacement rates, to assess changes in and viabilities of nonhuman primate groups and populations. Heltne et al. (1975) concluded that the howling monkey (Alouatta palliata) population at La Pacifica (Guanacaste, Costa Rica) was declining, as the IFR was <1.5, the ratio thought needed for a sustainable population. Our population surveys of 1984, 1991, and 1998 revealed that the number of monkeys in the population was stable, but the number of groups had increased and mean group size decreased. To examine these group-level changes, we present the IFR and immature-to-adult (IAR) ratios for La Pacifica Groups 2 and 18, which we have studied longitudinally for 18 and 10 years, respectively. Group 2 was larger than Group 18, but both groups showed similar mean IFRs for the study periods. The mean IFR for each group exceeded the population IFR. The annual IFRs varied more in the smaller group than in the larger group, and the IARs for these groups varied more than the IFRs did. All annual IFRs in the groups were below the hypothesized critical value of 1.5. Given these group and population values, we examined this critical IFR value with respect to mantled howler life history characteristics, particularly interbirth intervals and juvenile emigration, both of which preclude ratios 1.5, and compared the La Pacifica mantled howler population ratios with those of other populations. Group size, in conjunction with these ratios, might be more predictive of sustainable groups and populations.     

A preliminary study of resource overlap between howling monkeys (Alouatta palliata) and other arboreal mammals in the tropical rain forest of Los Tuxtlas,Mexico

Potential resource overlap between howling monkeys and other arboreal mammals was studied in the rain forest of Los Tuxtlas, Veracruz, Mexico. Eight species of mammals belonging to the orders Primates, Carnivora, Rodentia, and Marsupialia were found to share the canopy and to overlap trophically with howling monkeys. These mammals made up 77% and Alouatta 23% of the arboreal mammalian biomass under consideration. The arboreal porcupine and spider monkey were the only mammals that also fed on leaves. However, in this feeding niche, Alouatta is the only important mammalian folivore in Los Tuxtlas, and resource depression derived from leaf-eating insects is more important. The eight arboreal mammals may exert more pressure upon fruit resources, for they consumed 75% of the estimated total dry weight of fruit/ha/yr consumed by arboreal mammals.     

Behavioural development of howling monkey twins (Alouatta palliata) in Santa Rosa National Park,Costa Rica

Twins born to a young female howling monkey in Santa Rosa National Park, Costa Rica were observed during the first 96 days of their life. The comparison of their development to that of single infants and the comparison of the behaviour of the mother of the twins to that of mothers of single infants revealed few differences. However, qualitative observations suggests that high costs are associated with maternal care of infant twins. The mother had difficulty carrying both infants and was the only female observed to become sick during the study. Increased costs of lactation were not compensated for by an increase in foraging time. It would seem that howling monkey mothers possess a maternal care system which is capable of providing suitable care to twins. However, the costs on the mother of raising twins is suggested as a factor selecting for a litter size of one.     

Group takeover by a natal male howling monkey (Alouatta palliata) and associated disappearance and injuries of immatures

As part of a long-term study on howling monkey behavior and social dynamics, a known natal male was observed taking over his group from his putative sire. Due to the accidental death of one of the adult males, this natal male had matured in a one-male group and had never observed juvenile male emigration nor adult male immigration and associated behaviors. Nevertheless, the behaviors associated with the takeover were indistinguishable from those of an immigrant male, including disappearance of immatures, one of whom was found with extensive injuries. While it cannot be said that the natal male inherited these behaviors from his presumed father, it can be said that he exhibited species-typical behaviors associated with male takeover in the absence of observational learning.     

Behavioral development and socialization of infants in a free-ranging group of howling monkeys (Alouatta palliata)

A 22-month field study was carried out on free-ranging mantled howlers in Costa Rica. Six female and 5 male infants were observed systematically from birth until they died, left the group, or the study ended. Interaction patterns, activity patterns, and proximity data were analyzed from 703 h of focal observations and 753 h of ad lib observations. Developmental trends in weaning and nonmother care were associated with mothers' feeding patterns, suggesting an increase in maternal feeding efficiency. As howler immigration patterns resulted in groups of adults of low relatedness, analyses based on social bonding or kin selection were inappropriate, and socialization patterns instead appeared to prepare howler infants to respond predictably in an adult world. Females, which were more sociable as adults, were also more sociable as infants, initiating interactions and reacting positively. They also exhibited less weaning stress than males. Males, which were forced out of the group sooner, remained solitary longer, and primarily interacted with adult females as adults, were forced to be independent sooner, reacted negatively to interactions, and ceased interacting with adult males by 3 months of age. Ecological constraints on development could not be determined from this study, although there was no evidence for developmental trends being influenced by predator stress.     

Comparison of frugivory by howling monkeys (Alouatta palliata) and bats (Artibeus jamaicensis) in the tropical rain forest of Los Tuxtlas,Mexico

Information on the fruit diets of howling monkeys and fruit-eating bats in the tropical rain forest of Los Tuxtlas, Mexico was collected for a year to compare the plant species used. Howling monkeys used 19 plant species whereas bats used 32 plant species as fruit sources. Eleven species were common in the diet of both mammals. A rank analysis at the plant species level showed that the fruit diets of Alouatta and Artibeus were very different. In contrast to bats, howling monkeys displayed a seasonal pattern in fruit consumption. Diet overlap between the two mammals was highest during the monkeys' fruit-eating season. Measures of fruit production in eight trees (four species) indicated marked variations in fruit biomass produced and in length of fruiting from tree to tree and species to species. Peaks in fruit production were typical both at the species and the individual tree levels, demonstrating the very patchy nature of the fruit available to the monkeys and the bats.     

Agonistic and Affiliative Relationships of Adult Female Howlers (Alouatta palliata) in Costa Rica Over a 4-Year Period

We observed 12 adult female mantled howlers (Alouatta palliata), which have been part of Group 2 at Hacienda La Pacifica, Guanacaste Province, Costa Rica, via focal animal sampling during portions of July and August of 1988 and 1990–1992 (7–9 females/year, 955.3 hr of observation). We used agonistic interactions and time in proximity (<1 m) as indices of social relationships. The rate of female–female agonistic interactions was 0.38/hr (yearly range: 0.24 to 0.51/hr). Yearly dominance hierarchies, based on outcomes of dyadic agonistic interactions, varied in linearity between 60.7 and 94.6%. Adult females spent 7.10% of their time in proximity to another adult female (yearly range: 1.04–15.64%) and 4.95% of their time in proximity to an adult male (yearly range: 2.27–7.51%). Using yearly dominance ranks, we tested proximity patterns for differences based on rank and presence of dependent offspring. In 3 of the 4 years, high-ranking females spent significantly greater proportions of their time in proximity with other females than did low-ranking females. Time in proximity with the 3 or 4 adult males was not associated with rank. Having a dependent infant was not related to the proportion of time in proximity to females or males, and females, especially top-ranking ones, spent more time in proximity to females with dependent infants than to females without infants. These results show that social relationships in mantled howler groups are dynamic and generally support predictions made by von Schaik (1989) regarding scramble-type, female competitors. We also discuss the roles of immigrations, infants, and male relationships in the patterning of social relationships.     

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.     

Seasonal variation in the positional behavior of red howling monkeys (Alouatta seniculus)

Recent studies on the positional behavior of primates reveal that significant seasonal variation occurs in both locomotion and postures that is related to changes in diet and foraging techniques. Howling monkeys (genusAlouatta), which also have a seasonally varied diet, are predicted to have correspondingly varied positional behaviors. Two groups of red howling monkeys were studied in a primary rain forest in French Guinana during the dry and wet seasons. During the dry season, when howler diet is based mainly on leaves, howlers traveled more frequently by quadrupedal walking on large supports, a mode of progression that is probably inexpensive energetically and relatively stable. During feeding, quadrupedal and tripedal stand contributed considerably, a posture probably associated with the equal distribution of leaves within a tree crown. In contrast, during the wet season, when fruit was abundant, howlers fed very frequently by sitting on large supports, probably because fruit consumption required more time for special manipulation. However, most seasonal changes in feeding postures, and in travel and feeding locomotion, were difficult to associate directly with dietary shifts. These behavioral changes may be more highly correlated with slight modifications in microhabitat use (horizontal and vertical daily ranges, similar and alternative arboreal pathways) that are not considered in this paper.     

Intestinal parasites in howler monkeys Alouatta palliata (Primates: Cebidae) of Costa Rica

Fecal samples of 102 howler monkeys (Alouatta palliata) from several sites of Costa Rica were studied for intestinal parasites. The zones studied were: Central Valley (San Ramón, Alajuela), Central Pacific (Chomes and Manuel Antonio National Park. Puntarenas), North Pacific (Palo Verde Park and Playa Potrero, Guanacaste). Chira Island in the Nicoya Gulf and Caribean area (Cahuita. Limón). Animals were anesthetized with dards containing Telazol in order to collect the fecal material; some monkeys defecated spontaneously and others by direct stimulation. Samples were studied in saline solution (0.85%) and a Iodine solution, or stained with Haematoxylin. The material was also cultured in Dobell culture medium to determine the presence of amoeba and flagellates. Strongvloides. Controrchis. Trypanoxyuris genera were found in 3.4% of the samples. In addition 16.7% to 80% of the animals showed protozoa infection with Endolimax, Entamoeba, Trichomonas and Giardia. It is discussed the relationships of parasite infection with environmental conditions, animal population and human presence, specially in the monkey conservation programs point of view.     

A study of a black howling monkey (Alouatta caraya) population in northern Argentina

A population of Alouatta caraya in northern Argentina had an ecological density of 130 animals per km². Mean troop size varied from 7.2 to 8.9 individuals, and the ratio of adult males to adult females from 0.58 to 0.51. Infants comprised from 6% to 14% of the population, juveniles from 16% to 21%. These percentages probably vary seasonally in response to a birth peak at the beginning of the dry season. Males were age-graded in multi-male troops. Sexual dimorphism was extreme in this species. Males were all black and averaged 6.7 kg; females were yellow-brown and averaged 4.4 kg. Juvenile males retained the pelage color of the female until approximately 4.5 yr of age and 5 kg in weight. No genital mimicry or exaggeration occurred in this species. Vocalizations of A. caraya were similar to those of A. seniculus, both of which tend to be lower pitched than those of A. palliata.     

Use of leaf resources by howling monkeys (Alouatta palliata) and leaf-cutting ants (Atta cephalotes) in the tropical rain forest of Los Tuxtlas,Mexico

Use of leaf resources by a troop of howling monkeys and two colonies of leaf cutting ants was studied for an annual cycle in the rain forest of Los Tuxtlas, Mexico. Howling monkeys spent half their annual foraging time feeding on leaves; leaf-cutting ants spent at least 80% of their recorded foraging time harvesting leaves. Both herbivores preferred young leaves over nature ones, and chemical analysis showed that the protein: fibre ratio of the leaves used was correlated with these preferences. Howling monkeys used 34 tree species as leaf sources. Leaf-cutting ants used 40 plant species of which 38 were trees. Eighteen species used by Alouatta were also used by Atta; species of Moraceae and Lauraceae were among the most important in their foraging preferences. The plant species used by monkeys and ants occurred at low densities (? 4.0 ind/ha). The seasonal production of leaves, the high density of leaf-cutting ant colonies at the study site, and the high amounts of young foliage harvested by the ants from tree species, and individual trees used by howling monkeys as sources of young leaves suggest that the foraging activities of Atta may represent a significant pressure upon leaf resources available to Alouatta.     

Tropical rain forest conversion and perspectives in the conservation of wild primates (Alouatta and Ateles) in Mexico

The original distribution of the tropical rain forest and of the populations of Alouatta palliata, Al. pigra, and the two subspecies of Ateles geoffroyi in southern Mexico have been reduced by at least 90% in the last 40 years as a result of conversion of natural habitat to pasture and agricultural fields. This dramatic conversion has been caused mainly by the rapid growth of the human population in the southern states of the country. In the region of Los Tuxtlas in southern Veracruz, where the only longitudinal popululational and ecological studies of A. palliata and At. g. vellerosus have taken place, only 15% of the original extension of the tropical rain forest remains today. The intensive destruction of suitable primate habitat in this region has resulted in an accelerated process of extinction of the primate species. It is estimated that only about 200 At. g. vellerosus and about 1200 Al. palliata exist in the remaining small portion of their original habitat. Today, the distribution of the three primate species in Mexico is intensively and extensively fragmented, and only five potential foci for conservation exist in the country. Urgent action is required to protect the primate populations in the region of Los Tuxtlas and at the other four foci, as some of these populations may disappear by 1995.     

Responses to Deforestation in a Group of Mantled Howlers (Alouatta palliata) in Costa Rica

To evaluate the effects of partial deforestation of the home range of a group of free-ranging howlers on Hacienda La Pacifica, Costa Rica, we compared activity patterns, social interactions, daily travel lengths, group sizes and migration patterns before, during, and after habitat destruction. Immediate responses were a decrease in social interactions and increase in start to travel. Long-term responses included an increase in feeding time and longer daily path length. The long-term responses were associated with the adjustment to a new home range which was longer and narrower, with the patchiest resources at the furthest end points. Group size decreased due to a significant decrease in adult males and females and a significant increase in infant deaths between the predeforestation period and the deforestation/postdeforestation periods. Significant increase in adult female deaths/emigration continues, though emigration of immatures remains unchanged. Reduced group size could be due to reduced resources or disturbed migration routes throughout the farm due to the construction of a major canal system.     

Feeding and general activity patterns of a howler monkey (Alouatta palliata) troop living in a forest fragment at Los Tuxtlas,Mexico

The feeding behavior and general activity patterns of a howler monkey troop living in a 3.6 ha forest fragment were studied at Los Tuxtlas, Mexico, for an annual cycle. Monthly samples of their feeding behavior indicated that they used 52 species of 24 plant families as sources of food. Of these, 67% were trees, which accounted for 96% of total feeding time recorded. Ten species of Moraceae, Cecropiaceae, Anacrdiaceae. and Sapotaceae contributed to 70% of the trees used and to almost 90% of feeding time. The number of plant species used per monthly record varied from 7 to 31 with an average of 19.9 species. Young leaves and ripe fruit were the principal items in the monthly diet of howlers and average percent of time spent consuming these plant parts was 46.7% and 34.8%, respectively. The use of tree species was found to be associated to their importance value and to their pattern of spatial dispersal in the study site. Availability of young leaves was fairly constant from month to month, but it presented a seasonal pattern, and there was a significantly lower number of tree species bearing ripe fruit through the year with brief pulses of production. The monthly activity pattern was found to be related to variations in the availability of young leaves and ripe fruit as well as to the values of the intermonthly overlap in plant species used. Resting and feeding presented a bimodal pattern of occurrence throughout the day that seemed to be related to variations in maximum ambient temperatures. Results are discussed in light of the small size and shape of the forest fragment inhabited by the howler troop. Am. J. Primatol. 48:167–183, 1999. © 1999 Wiley‐Liss, Inc.     

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.     

Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana

A 2-year field study of the frugivorous diet of a howling monkey troop, in a tropical rain forest in French Guiana, shows that they disperse by endozoochory ≥95% of plant species from which they eat ripe fruit. Passage through the digestive tract of howlers does not significantly modify the germination success of most plant species samples. Their low digestion rate (X = 20 hr 40 min) is the ultimate cause of a bimodal defecation rhythm that results in the concentration of 60% of defecations being deposited under sleeping sites. The distance of seed dispersal can reach more than 550 m from parent trees,with a mean of 260 m. Although howling monkeys consume fruits differing in morphological characteristics, they are particularly able to disseminate seeds of species whose fruits have a hard and indehiscent external coat or large seeds or both. In French Guiana, they may be especially important dispersers of the Sapotaceae with fruits that simultaneously present both characteristics.     

Multimodal communication by male mantled howler monkeys (Alouatta palliata) in sexual contexts: a descriptive analysis

We analyzed continuously sampled focal and ad libitum data of male mantled howler monkeys (Alouatta palliata) observed in random order. Males resided in two groups in a Costa Rican tropical dry forest environment (riparian habitat group: 3 males, 15 females, 402 h observation; deciduous habitat group: 2 males, 8 females, 114 h observation). Samples were limited to sexual contexts, in particular, the 60-min periods before and after each copulation observed within each group for each male. Time samples for each male were distributed equally before and after their own copulations. Before statistical analyses were conducted, data were corrected for differences in time sampled for males within each group. Four types of multimodal signaling were resolved: (1) audiovisual, (2) olfactory-visual, (3) olfactory-visual-tactile and (4) tactile-gustatory. Olfactory and tactile signals were never observed in combination with auditory signals. Consistent with expectation for a Neotropical, arboreal species, audiovisual signals were the most frequently observed type of multimodal communication in both groups (riparian habitat group: n = 139; deciduous habitat group: n = 66). Our evidence strongly suggests that unimodal signals may be combined and recombined to form complex, multimodal signals. Subordinate males in each group were more likely than dominant males to emit audiovisual signals before their own copulations. Male dyads were compared to assess the relative rate of audiovisual signaling by one male before another male's copulations. On average, the subordinate male of the riparian habitat group exhibited audiovisual signals at a higher rate before his own copulations compared to the rate of audiovisual signaling by his dominant challengers. The same comparisons are not significant for males in the deciduous habitat group. The pattern of male response that we report whereby subordinates emit some complex signals at a higher rate than dominants supports the 'terminal investment hypothesis' predicting that organisms should increase reproductive effort with age since, in mantled howlers, age correlates negatively with dominance rank. Additional, qualitative observations suggested that subordinates in both groups were most likely to obtain copulations when they increased rates of complex signaling and/or escalated interactions with their male challengers. Group differences were apparent, however, and we suggest factors that may account for these patterns. We assessed responses by female receivers of complex signals emitted by males in sexual contexts. In general, higher-ranking males are more attractive to females and are more successful at monopolizing them. Findings for other, less frequently displayed, multimodal signals (olfactory-visual, olfactory-visual-tactile and tactile-gustatory) are presented and discussed. We conclude with the suggestion that howlers may be a robust model for the investigation of complex signals in Neotropical primates, including research on functionally referential communication and context-dependent syntax.