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.     

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.     

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.     

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.     

Resource use by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas,Veracruz, Mexico

The feeding preferences of howler monkeys at their northernmost distribution in the Neotropics are reported for an annual cycle. A remarkable selectivity for 27 species representing 15 families was observed. The Moraceae and Lauraceae plant families were the most important in the diet. The howlers spent an almost equal proportion of their feeding time eating leaves and fruit, and displayed a marked preference for young leaves and mature fruit. The consumption of different plant parts was markedly seasonal and the howlers’ ranging behavior was closely associated with the availability of young leaves and mature fruit. Their home range was unusually large (ca. 60 ha) for howlers and the food species exploited occur at very low densities (93%, ≤ 4 ind/ha). They chose food items richer in protein and energy. Alkaloid compounds, present in some of the leaves, play a secondary role in their dietary selectivity.     

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.     

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.     

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.     

Brief report: Infant-killing and infant disappearance following male takeovers in a group of free-ranging howling monkeys (Alouatta palliata) in Costa Rica

Events surrounding an infant-killing following a male takeover are described for a group of free-ranging howling monkeys in Costa Rica, and additional evidence is presented for infant disappearances following three previous male takeovers. Infant-killing is best interpreted in this context as a male reproductive strategy, as infant-killing did effectively shorten the interbirth interval, and only infants of high-ranking females died or disappeared following a male takeover. Due to the exclusive access of the dominant male to high-ranking estrous females, an incoming male who had lived as a peripheral male before taking over the group would run little risk of eliminating his own offspring in the course of killing the offspring of high-ranking females.     

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.     

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.     

Bird species richness in vegetation fences and in strips of residual rain forest vegetation at Los Tuxtlas, Mexico

Fragmentation of the lowland tropical rain forest has resulted in loss of animal and plant species and isolation of remaining populations that puts them at risk. At Los Tuxtlas, Mexico, lowland rain forests are particularly diverse in the avian fauna they contain and while most of the forests have been fragmented by human activity, many of the fragments still harbor diverse assemblages of bird species. In these landscapes, linear strips of residual rain forest vegetation along streams as well as linear strips of vegetation fences (live fences) crossing the pastures might provide some connectivity to bird populations existed in forest fragments. We investigated bird species richness and relative abundance in one 6-km long section of live fences (LF) bordering a dirt road and in two 6-km long sections of residual forest vegetation along a river (MR) and one permanent stream (BS). We used point count procedures which resulted in the count of 2984 birds representing 133 species. At the LF site we detected 74% of the species, 72% at the BS site and 57% at the MR site. Only 38% of the species were common among sites. Neotropical migratory birds accounted for 34–41% of the species counted at all sites. While edge and open habitat birds accounted for 6–10% of the species and for 50% of the records at the three vegetation strips, about 90% of the species were forest birds. Distance to forest fragments and degree of disturbance of the vegetation seemed to negatively influence bird species presence at the BS and MR strips. Rarefaction analysis indicated that the LF strip was richer in species than the other two sites, but the occurrence of the three vegetation strips in the landscape seem to favor the presence of many more species. We discuss the value of these vegetation strips to birds as stepping stones in the fragmented landscape.     

Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas,Mexico

In view of the extensive destruction, fragmentation, and conversion of primate habitats to anthropogenic vegetation, information on Neotropical primate ability to use a landscape consisting of forest fragments and agricultural habitats is necessary to understand the ecological flexibility of the species involved and it is of relevance to the design of conservation scenarios at the landscape level. We censused howlers and spider monkeys in 126 forest fragments and in 44 agricultural sites at Los Tuxtlas, southern Veracruz, Mexico, and used the IDRISI Geographic Information System to assess the extent of primate habitat remaining. We conducted economic surveys to assess the productivity of several systems of land management, including cattle ranching. Seventy- five percent of native habitat has been lost at Los Tuxtlas, 20% remains in the form of isolated fragments of vegetation, and only 5% consists of contiguous rain forest at high elevations (> 800 m). Howlers and spider monkeys were present in only 60 and 8% of the forest sites investigated, respectively, attesting to extensive local extinction. Populations of both species are small and found in a fragmented and isolated condition throughout the landscape. A large number of howlers were detected in artifactual habitats such as cacao, coffee and mixed (cacao and coffee) plantations shaded by rain forest trees. Residual rain forest vegetation along streams, rivers, and lakes facilitated the interfragment and interhabitat movement of howlers. Economic surveys showed that some of the agricultural habitats were more productive than cattle ranching. Conservation of spider monkeys requires large areas of contiguous forest, but only small areas are present at high elevations. Howlers are restricted to elevations < 800 m, where most of the forest has disappeared, but can apparently exist in a matrix of forest fragments, arboreal agricultural habitats, and pasture lands. Structural aspects of the vegetation and connectivity among habitat islands may be indispensable components of both landscape scenarios.     

Some observations on the present distribution and conservation of Alouatta and Ateles in Southern Mexico

Some information on the past and present distribution of Alouatta and Ateles in southern Mexico and on the impact of habitat destruction on their future existence is presented. Three surveys of primate populations and forest habitats were carried out between 1981 and 1983 in southeastern Mexico. Rapid destruction of the forest is reducing the number of forested areas where Alouatta and Ateles can exist and co-occur. Illegal hunting of the two primates also contributes to their rapid decline. Alouatta and Ateles live a precarious existence in a few large and small islands of forest, and efforts are needed to set aside some of these areas as reserves so that their future survival is ensured.     

Structure and floristic composition of the lowland rain forest of Los Tuxtlas,Mexico

Physiognomy, structure and floristic composition of one hectare of lowland tropical rain forest was studied in detail at Los Tuxtlas, Mexico. Physiognomically, the Los Tuxtlas forest should be classified as lowland tropical high evergreen rain forest. The forest showed a closed canopy at 30–35 m. Of all woody, non-climbing species with a DBH1.0 cm 89.4% (94.5% of all individuals) were evergreen, 25.4% (59.5% of the individuals) had compound leaves, and over 80% of species (and individuals) had leaves in the notophyll and mesophyll size classes. The forest structure was characterized by a low density (2976 individuals with a DBH1.0 cm, 346 individuals with a DBH10.0 cm, per ha, excluding vines) with an average basal area (38.1 m², DBH1.0 cm, 34.9 m², DBH10.0 cm, per ha, excluding vines). This was attributed to the relative maturity of the forest on the study plot. The study plot contained 234 species (11 208 individuals with a height 0.5 m), of which 55.1% (34.8% of individuals) were trees, 9.4% (6.8%) shrubs, 3.4% (44.3%) palms, 20.1% (5.2%) vines, 6.8% (8.7%) herbs and 5.1% (0.3%) of unknown lifeform. Furthermore, 58 species of epiphytes and hemi-epiphytes were found. Diversity of trees, shrubs and palms with a DBH1.0 cm was calculated as Shannon-Wiener index (4.65), Equitability index (0.65), and Simpson index (0.10). The dominance-diversity curve showed a lognormal form, characteristic for tropical rain forest. The community structure was characterized by a relative dominance of Astrocaryum mexicanum in the understorey, Pseudolmedia oxyphyllaria in the middle storeys, and Nectandra ambigens in the canopy. Species population structures of 31 species showed three characteristic patterns, differentiated by recruitment: continuously high, discontinuously high, and continuously low recruitment. Height/diameter and crown cover/diameter diagrams suggested a very gradual shift from height growth to crown growth during tree development. Forest turnover was calculated as 138 years. Compared to other tropical rain forests the Los Tuxtlas forest had 1. similar leaf physiognomical characteristics, 2. a lower diversity, 3. a lower density, 4. an average basal area, and 5. a slow canopy turnover.     

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.     

Non flying mammals and landscape changes in the tropical rain forest region of Los Tuxtlas, Mexico

The rapid and extensive conversion of Neotropical rain forests to a landscape consisting of pasture lands and other agricultural habitats has meant the local disappearance fragmentation and isolation of vertebrate populations To avoid further losses in biodiversity in Neotropical rain forests, it is imperative to determine how the different species that constitute the different vertebrate communities have responded to the anthropogenic alterations of their natural habitats To provide data in this direction we sampled non flying mammals in 35 forest fragments, in six disturbed forest sites in 12 regenerating forests, in 20 arboreal agricultural habitats (cacao coffee, mixed, citrus and allspice), in four live fence sites and in four pasture sites at Los Tuxtlas, Veracruz Mexico Sampling indicated that area of forest fragments and isolating distance were important variables influencing species richness Disturbed forest had fewer species and individuals present and supported a lower non flying mammal biomass than undisturbed and regenerating forests Shaded plantations (cacao coffee and mixed) were richer in species and in individuals than unshaded ones (citrus, allspice) Species richness in forests and agricultural habitats were associated to horizontal plant diversity and vertical foliage diversity Pasture habitats were the poorest man-made habitats in non flying mammal species Live fences supported a higher biomass and species of non flying mammals than pastures and were similar to forest and shaded man-made habitats in species assemblages     

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.