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 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.     

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.     

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.     

The capuchin, the howler, and the Caatinga: seed dispersal by monkeys in a threatened Brazilian forest

Regeneration of the Brazilian Caatinga forest may be restricted by the naturally low diversity and density of fruit-eating animals, which has been aggravated by local faunal extinction induced by human activities. We made a preliminary evaluation of the potential seed-dispersal role of capuchin (Cebus apella libidinosus) and howler monkeys (Alouatta caraya) in Serra da Capivara National Park. The monkeys dispersed at least 26 species. Alouatta dispersed larger seeds than Cebus, and the two species apparently dispersed seeds in different local habitats. Seed dispersal by monkeys potentially makes a significant contribution to Caatinga regeneration.     

Seasonal rhythms of seed rain and seedling emergence in two tropical rain forests in southern Brazil

Seasonal tropical forests show rhythms in reproductive activities due to water stress during dry seasons. If both seed dispersal and seed germination occur in the best environmental conditions, mortality will be minimised and forest regeneration will occur. To evaluate whether non-seasonal forests also show rhythms, for 2 years we studied the seed rain and seedling emergence in two sandy coastal forests (flooded and unflooded) in southern Brazil. In each forest, one 100 x 30-m grid was marked and inside it 30 stations comprising two seed traps (0.5 x 0.5 m each) and one plot (2 x 2 m) were established for monthly monitoring of seed rain and a seedling emergence study, respectively. Despite differences in soil moisture and incident light on the understorey, flooded and unflooded forests had similar dispersal and germination patterns. Seed rain was seasonal and bimodal (peaks at the end of the wetter season and in the less wet season) and seedling emergence was seasonal and unimodal (peaking in the wetter season). Approximately 57% of the total species number had seedling emergence 4 or more months after dispersal. Therefore, both seed dormancy and the timing of seed dispersal drive the rhythm of seedling emergence in these forests. The peak in germination occurs in the wetter season, when soil fertility is higher and other phenological events also occur. The strong seasonality in these plant communities, even in this weakly seasonal climate, suggests that factors such as daylength, plant sensitivity to small changes in the environment (e.g. water and nutrient availability) or phylogenetic constraints cause seasonal rhythms in the plants.     

Seed rain and advanced regeneration in a tropical rain forest

By comparing seed rain, seedling and sapling community structures we assessed the possible role played by vertebrate seed dispersal as a structuring factor in advanced regeneration of closed-canopied sites in the tropical rain forest of Los Tuxtlas, Mexico. Seed weight, initial morphology of seedlings and species abundance were also analyzed to determine if these traits influenced the probability of establishment in the shade.About half of the seed species falling in five closed forest sites (25×25 m) during one year came from fruiting trees growing within the sites (local seeds) and half from fruiting trees found outside the sites (immigrant seeds). Seeds of liana and upper-canopy species were over-represented among immigrant seeds compared with seeds of understory tree species. This probably reflects the activity of frugivorous arboreal mammals, bats, and birds. Species with immigrant seeds had both a lower abundance and a narrower spatial distribution than locally produced seeds. Therefore, immigrant seeds showed higher diversity values than locally produced seeds.Average seed size and the proportion of epigeous seedlings were similar in local and immigrant species. Under closed-canopied sites, factors affecting community organization seem to operate selectively, favoring the establishment of large-seeded, local abundant species in the advanced regeneration. However, the fact that some saplings of immigrant species were found in the plots suggest that a slow species infiltration may be occurring leading to a slow shift in the advanced regeneration species composition. We propose that the influence of seed dispersal on advanced regeneration structure depends on the disturbance history of the patches where seeds land.     

Seed rain from forest fragments into tropical pastures in Los Tuxtlas,Mexico

Deforestation has resulted in the fragmentation of forests. Remnant fragments are widely assumed to be sources of seeds for forest regeneration in abandoned pastures. The seed rain in 12 pastures at Los Tuxtlas, Mexico, their relationship with riparian vegetation adjacent to them, and their closeness to the reserve is described. For all the species found in the seed rain, we classified them by typical habitat (pasture or rain forest), life form, dispersal syndrome, and plant strategy (pioneer or non-pioneer species). In addition, germinability was evaluated for all seeds. We also assessed the correlation in composition of the seed rain and the riparian vegetation. Only 11% of the total species that occur in the Los Tuxtlas region reach pastures via dispersal from forest fragments. However, nearly 80% of the species in the seed rain did not come from the fruiting individuals in the adjacent riparian vegetation. The proportion of dispersal syndromes, life forms and plant strategies of the species in the seed rain was similar to those observed in the rain forest. On average, the germinability of forest species was less than 30%.The forest species richness was similar in the seed rain in pastures and inside the forest, but the pasture seed rain contained fewer seeds per species. Pastures have a high potential for natural regeneration because of seed dispersal from adjacent forest. However, the forest that regenerates in pastures close to the reserve is expected to contain different species than the forest regenerating far away from it.     

The responses to shade of seedlings of very small-seeded tree and shrub species from tropical rain forest in Singapore

1. Newly germinated seedlings of six tree and shrub species with very small seeds (31–460 μg dry mass), one light-demanding and five shade-tolerant at the stage of establishment in the wild, were grown for 5 months in neutral shade houses with 0·5, 1, 3·5 and 7·5% daylight.
2. The ratio of yield in 7·5% to that in 1% was 8:1 for the light-demanding Melastoma malabathricum but only 2:1 for the confamilial shade-tolerator Pternandra echinata. The Pternandra, Urophyllum hirsutum, Ficus chartacea, Ficus grossularioides and Pellacalyx saccardianus showed a graded series of responses to irradiance, generally consistent with their apparent demands for light in the wild. In contrast, survival of very deep shade was not clearly related to light demand in nature.
3. The results support the conclusion drawn from observational studies that large seed size is not primarily adaptive in resisting shade but in resisting the associated risks of burial by litter, desiccation during dry spells, uprooting by birds and other kinds of damage by animals or falling debris.     

The effect of seed mass and gap size on seed fate of tropical rain forest tree species in guyana

Abstract: For eleven tree species, differing in seed mass, germination success (emergence success for two small-seeded species) and the causes of failure to germinate were studied in the forest understorey and in logging gaps in the tropical rain forests of Guyana. In the forest understorey, germination success increased with seed mass. However, as gap size increased the difference between smaller and larger seeded species diminished because germination success of smaller-seeded species increased slightly, while that of larger-seeded species decreased dramatically. The negative effect of gap size on germination success of larger-seeded species was caused by an increased risk of desiccation with gap size, which was a far more important seed mortality agent for larger than for smaller-seeded species. Generally, seeds of smaller-seeded species suffered more from insect predation and were removed at higher rates than larger-seeded species. On the other hand, larger-seeded species were eaten more by mammals than smaller-seeded species. It is concluded that logging can result in shifts in the species composition in the tropical rain forests of Guyana which are dominated by species with large seeds, since germination success of larger-seeded species is dramatically reduced in large logging gaps.     

Group size and composition influence male and female reproductive success in black howler monkeys (Alouatta pigra)

It has been argued that grouping patterns might influence the reproductive performance of individuals. Increasing group size results in greater travel costs and competition over depletable food resources, which could lead to reduced individual reproductive success. However, in groups with an increasing number of males, female reproductive success is predicted to augment because larger male groups might better protect immatures from infanticidal attacks. In contrast, male reproductive success is predicted to decrease with number of males in a group because fertilization cannot be shared between males. In this paper, we test these predictions on the Mesoamerican black howler monkey (Alouatta pigra) with data on group size and composition for 120 groups from eight populations of black howler monkeys existing in eight protected forests in Mexico and Guatemala. Male and female reproductive success were calculated as a deviation of the observed number of infants (or immatures) from the expected number of infants (or immatures), relative to the number of males and females in a group. Results indicate that both male and female reproductive success decreased with group size. Male reproductive success decreased with an increasing number of males in a group and with increasing proportion of males relative to females in a group. Decreased female reproductive success was associated with increasing number of females in a group, and female reproductive success had a tendency to increase with increasing number of males in a group. These results suggest that in black howler monkeys, living in larger groups might negatively affect the reproductive success of each member. Our findings are similar to those reported for a population of a sister species, Alouatta palliata, living in larger groups.     

Sources of variation in fecal cortisol levels in howler monkeys in belize

High cortisol levels are known to cause low fecundity and increased mortality; thus, the prospect of using cortisol as a measure of population health is an exciting one. However, because so many factors can interact to influence cortisol release, it can be difficult to interpret what exactly is creating changes to cortisol levels. This study investigates variation in fecal cortisol levels in a population of black howlers (Alouatta pigra) from 350 fecal samples collected from 33 individuals in more than 4 years. A general linear mixed model revealed that cortisol varied significantly with fruit availability and contact with tourists. When fruit availability was low, cortisol increased, likely because when fruit availability is low monkeys eat less fruit, thus obtaining less sugar. This result may simply reflect cortisol's metabolic function of mobilizing glucose. It also indicates that these monkeys may be experiencing periods of food stress throughout the year, which was earlier thought to be minimal for a primarily folivorous species. Presence of tourists was the only other factor found to lead to high cortisol; with exposure to tourists increasing stress levels. These results highlight the importance of understanding how physiological factors can influence cortisol, making it easier to interpret results and determine the external social or ecological stressors that may increase cortisol. Am. J. Primatol. 72:600–606, 2010. © 2010 Wiley‐Liss, Inc.     

Analysis of the hydrogenotrophic microbiota of wild and captive black howler monkeys (Alouatta pigra) in palenque national park, Mexico

Intestinal methanogenesis is one of the major pathways for consumption of hydrogen produced by bacterial fermentation and is considered to affect the efficiency of host energy harvest; however, little information is available regarding the hydrogenotrophic pathways of nonhuman primates in the wild, in general, and of howler monkeys, in particular. Microbial fermentation of plant structural carbohydrates is an important feature in wild howlers owing to the high fiber and low available energy content of leaves, which make up the primary component of their diet. In contrast, captive howlers may consume greater quantities of fruits and vegetables that are higher in water, lower in fiber, and, along with commercial monkey chow commonly added to captive monkey diets, more readily digestible than the natural diet. In this study, we analyzed the composition of methanogens and sulfate-reducing bacteria (SRB) from fecal samples of black howler monkeys (Alouatta pigra) in the wild and in captivity. The hydrogenotrophic microbiota of three groups of monkeys was evaluated by PCR-denaturing gradient gel electrophoresis (DGGE) fingerprinting, small clone library construction, and quantitative real-time PCR. Abundance of methanogens was lower than SRB in all howler monkey groups studied. DGGE banding patterns were highly similar within each wild and captive group but distinct among groups. Desulfovibrionales-enriched DGGE showed reduced microbial diversity in the captive animals compared with their wild counterparts. Taken together, the data demonstrate that environmental or dietary changes of the host imposed by captivity likely influence the composition of intestinal hydrogenotrophs in black howler monkeys.     

Germination and water dispersal of seeds from a threatened plant species Penthorum chinense

To conserve a threatened plant species (Penthorum chinense Pursh) in Japan, seed germination responses to pretreatment (imbibition and/or chilled), temperature and light, and seed dispersal by water were examined. The seeds collected from abandoned paddy fields in a warm temperate region, central Japan, germinated in light (14 h photoperiod; light 22°C, dark 21°C) after a moist-chilled treatment. After this pretreatment, the seeds germinated well at 10–25°C (optimum temperature 15°C), but did not germinate in darkness even at the optimum temperature. Most of the seeds floated on distilled water, but 20–60% of the seeds that were collected from several populations sank in distilled water, indicating dimorphism in seed dispersal by water. The floating and sunken seeds did not show significant differences in weight and germination rate within a population. The addition of a surface-active agent in distilled water submerged the seeds, indicating that the buoyancy of the seeds is attributable to an oil coating on the seed surface that enhances the interfacial tension on the seeds. Three times the number of seeds sank in river water collected from a rural area than in distilled water. A greater number of seeds also sank in water that had increasing concentrations of linear alkylbenzenesulfonate, which is a major component of synthetic detergents. This suggests that the water dispersal of this species is suppressed by surface-active agents, including detergents, in river water.     

Ecology of seed germination of eight non-pioneer tree species from a tropical seasonal rain forest in southwest China

We compared various aspects of the seed biology of eight non-pioneer tree species from a tropical seasonal rain forest in Xishuangbanna, SW China, that differ in time of dispersal, size and fresh seed moisture content (MC). Seeds were tested for germination under laboratory conditions after dehydration to different moisture levels and under 3.5, 10 and 30% solar irradiances in neutral-shade houses. For six species, germination was also compared in forest understory (3.5% light) and center of a forest gap (32.5% light). Under continuous dehydration over activated silica gel, 100% of seeds of four species had lost the ability to germinate after 48 h, and those of all species except Castanopsis hystrix (decreased from >90 to 30% germination) had lost the ability to germinate after 120 h. Four species did not differ in final germination percentages at the three irradiances (i.e. uniform germination). However, final germination percentages of Horsfieldia pandurifolia and Litsea pierrei var. szemaois were significantly lower in 30% than in 10 or 3.5% light, and seeds of Antiaris toxicaria and C. hystrix germinated to higher percentages in 30 and 10% than in 3.5% light. Mean time to germination (MTG) of the eight species (forest and shade house data combined) ranged from 5–5 days for Pometia tomentosa to 72–207days for L. pierrei; MTG for four species was ≤21 days. There was no obvious relationship between relative desiccation resistance and either time of dispersal, MTG or uniformity of germination at the three light levels, or between seed size and MC or MTG. However, the relationship between seed MC at maturity (25–60% fresh mass basis) and MC at 50% loss of seed viability (12.4–42.5%) was significant. Seven of the species fit Garwood’s (Ecol Monogr 53:159–181, 1983) rapid-rainy germination syndrome and one, L. pierrei, either her delayed-rainy or intermediate-dry germination syndrome. However, fresh, non-dehydrated seeds of all eight species germinated in ≤30 days at constant 30°C in light.