Seed Dispersal by Monkeys and the Fate of Dispersed Seeds in a Peruvian Rain Forest1

Primary seed dispersal by two species of monkeys and the effects of rodents and dung beetles on the fate of dispersed seeds are described for a rain forest in southeastern Perú. During the six-month study period (June–November 1992) spider monkeys (Ateles paniscus) dispersed the seeds of 71 plant species, whereas howler monkeys (Alouatta seniculus) dispersed seeds of 14 species. Spider and howler monkeys also differed greatly in their ranging behavior and defecation patterns, and as a consequence, produced different seed rain patterns. Monkey defecations were visited by 27 species of dung beetles (Scarabaeidae). Dung beetles buried 41 percent of the seeds in the dung, but the number of seeds buried varied greatly, according to seed size. Removal rates of unburied seeds by rodents varied between 63–97 percent after 30 d for 8 plant species. The presence of fecal material increased the percentage of seeds removed by seed predators, but this effect became insignificant with time. Although seed predators found some seeds buried in dung balls (mimicking burial by dung beetles), depth of burial significantly affected the fate of these seeds. Less than 35 percent of Brosimum lactescens seeds buried inside dung balls at a depth of 1 cm remained undiscovered by rodents, whereas at least 75 percent of the seeds escaped rodent detection at a depth of 3 cm and 96 percent escaped at 5 cm. Both dung beetles and rodents greatly affected the fate of seeds dispersed by monkeys. It is thus important to consider postdispersal factors affecting the fate of seeds when assessing the effectiveness of frugivores as seed dispersers.     

Seed Dispersal by Salvin's Curassow,Mitu salvini (Cracidae), in a Tropical Forest of Colombia: Direct Measurements of Dispersal Distance1

Seed dispersal by Salvin's curassows (Mitu salvini) was studied in a lowland tropical forest at La Macarena on the border of the Macarena and Tinigua National Parks, the Department of Meta, Colombia. Continuous observations were made on the feeding and ranging behavior of a well-habituated pair of birds from 0600 to 1800 h for 19 days. Ibtal observation time was 222 h. The daily distance traveled by the birds ranged from 630 to 3750 m, with a mean of 1959 m (± 776 m). The total home range was ca 34.4 ha. Although curassows were observed consuming fruits of 13 species belonging to the families Rubiaceae, Meliaceae, Moraceae, Burseraceae, Leguminosae, and Lecythidaceae, only seeds of Geophila re fens (Rubiaceae) and Picas spbenophylla (Moraceae) were found in their feces. For G. repens, the mean and maximum retention times were 1 h 52 min (± 1 h 20 min) and 6 h 08 min, and the mean and maximum direct dispersal distances were 245 m (± 164 m) and 633 m. More than half the seeds were dispersed in canopy gaps. For F. sphenophylla, the mean and maximum retention times were 3 h 1 5 mm (± .37 min) and 7 h 08 min, and the mean and maximum direct dispersal distances were 329 m (± 46 m) and 451 m. Nearly 60 percent of the estimated seed intake of G. repens and 92-94 percent of F. sphenophylla were digested or damaged. The retention times and the dispersal distances for Streptogyna americana, which has adhesive burrs, were also measured. The mean and maximum retention times were 1 h 55 min (± 1 h 56 min) and 9 h 11 min, and the mean and maximum direct dispersal distances were 128 m (± 68 m) and 280 m. This is the first study in which direct measurements were made for retention times and dispersal distances of the epizoochory and endozoochory for birds in the field.     

Tropical Montane Forest Restoration in Costa Rica: Overcoming Barriers to Dispersal and Establishment

Tropical forests are being cleared at an alarming rate although our understanding of their ecology is limited. It is therefore essential to design restoration experiments that both further our basic knowledge of tropical ecology and inform management strategies to facilitate recovery of these ecosystems. Here we synthesize the results of research on tropical montane forest recovery in abandoned pasture in Costa Rica to address the following questions: (1) What factors limit tropical forest recovery in abandoned pasture? and (2) How can we use this information to design strategies to facilitate ecosystem recovery? Our results indicate that a number of factors impede tropical forest recovery in abandoned pasture land. The most important barriers are lack of dispersal of forest seeds and seedling competition with pasture grasses. High seed predation, low seed germination, lack of nutrients, high light intensity, and rabbit herbivory also affect recovery. Successful strategies to facilitate recovery in abandoned pastures must simultaneously overcome numerous obstacles. Our research shows that establishment of woody species, either native tree seedlings or early‐successional shrubs, can be successful in facilitating recovery, by enhancing seed dispersal and shading out pasture grasses. On the contrary, bird perching structures alone are not an effective strategy, because they only serve to enhance seed dispersal but do not reduce grass cover. Remnant pasture trees can serve as foci of natural recovery and may enhance growth of planted seedlings. Our results highlight the importance of: (1) understanding the basic biology of an ecosystem to design effective restoration strategies; (2) comparing results across a range of sites to determine which restoration strategies are most generally useful; and (3) considering where best to allocate efforts in large‐scale restoration projects.     

Seed Availability as a Limiting Factor in Forest Recovery Processes in Costa Rica

Abandoned pastures and secondary forests are increasingly prominent features of tropical landscapes. Forest regrowth on abandoned pastures is generally slow and virtually limited to regeneration from seeds from external sources, since agricultural activities alter site conditions. We hypothesize that seed availability is a major limiting factor in forest recovery on abandoned pastures. This hypothesis was tested by studying the seed bank, seed rain, and seed predation in a small pasture (1 ha) situated in a forest‐pasture mosaic in northwestern Costa Rica. The tree seed density in the pasture seed bank was much lower (21/m²) than the density in the seed bank of a neighboring secondary forest (402/m²). Within a period of five weeks, 23 tree seeds entered the pasture by seed rain. This number is low compared to densities found in closed forests but higher than densities reported in other studies where virtually no seeds were found beyond 20 m from the forest edge. Possibly the small size of the pasture with seed sources nearby and the small‐scale landscape mosaic enhance seed dispersal. Predation limits the seed density in pastures, with 42% of the woody species consumed by predators. The low seed density in the seed bank, and hampered recruitment combined with significant losses, pose severe restrictions to forest recovery on abandoned pastures. Moderate land use, and small sized clearings with seed sources nearby may increase the pace of recovery. Nevertheless, forest establishment may still take a considerable time. Thus, enlarging the available pool of species may be a worthwhile management strategy.     

Fruit Removal and Natural Seed Dispersal of the Brazil Nut Tree (Bertholletia excelsa) in Central Amazonia,Brazil

Experimental approaches to study seed dispersal of the Brazil nut tree have hitherto relied on exposed seeds deposited on the forest floor. Here we use a new method to study the natural dispersal by large rodents such as agoutis; tracking experimentally manipulated and tagged fruits containing individually marked seeds. Fruit manipulation did not deter agoutis from handling fruits. We found that agoutis usually moved intact fruits away from their original location below the parent tree before either hiding them or gnawing through the pericarp to access the seeds inside. Most fruits were moved to distances of 15–30 m from their original position, but some fruits could be taken as far as 60 m. A large number of seeds extracted from manipulated fruits appeared to be eaten immediately. Only 27 out of 1740 experimental seeds were found buried in shallow caches, generally within 5 m of the opened fruit. Fruit removal distance accounted for a disproportionate amount of total seed movement and seeds in the current study were dispersed significantly farther than in a previous experiment using exposed seeds, suggesting that classic dispersal experiments of this character may severely underestimate seed dispersal distances. We therefore conclude that the new method provides a more realistic and accurate approach to investigate natural seed dispersal of Brazil nuts and that the removal of fruits from underneath parent trees before being opened is the key to the significantly increased distances at which seeds are dispersed. Abstract in Portuguese is available at http://www.blackwell‐synergy.com/loi/btp .     

Seed Dispersal Patterns by Large Frugivorous Mammals in a Degraded Mosaic Landscape

Seed dispersal by Red fox (Vulpes vulpes), Stone marten (Martes foina), and Wild boar (Sus scrofa) was analyzed in an extensively degraded mosaic landscape in Sierra Nevada (SE Spain). The main objective was to determine whether seed dispersal by mammals was related to habitat degradation within a mosaic of adjacent degraded patches mixed with native forest and thereby to determine the potential role of mammals as seed dispersers in degraded landscape units. For three consecutive years, mammal feces were collected in the fruit production period, extracting all seeds of woody species found therein and analyzing their viability. Feces were collected in three different plots for each of five different landscape units: shrubland, native forest, and dense, cleared, and fenced reforestation stands. Seeds from 16 woody species (which represent more than a half of the total fleshy‐fruited woody species available) were recorded, although some agrarian species are also introduced in a low percentage of the scats. Seeds showed a high viability rate for all dispersed species, irrespective of the mammal disperser. No differences in species composition appeared in the overall landscape units or in the seed density between degraded habitats. Due to the small patch size, the high viability of dispersed seeds, and the large home range of the large mammals, these three animal species act as efficient seed dispersers for a diverse assemblage of woody plant species regardless of the habitat type within this degradation framework. This fact has important consequences for the biodiversity recuperation in these degraded habitats, principally in pine plantations.     

Increased Productivity and Reduced Seed Predation Favor a Large‐seeded Palm in Small Atlantic Forest Fragments

Large‐seeded plants are especially vulnerable to the loss of seed dispersers in small forest fragments. The palm Attalea humilis goes against this trend by reaching high abundances in small remnants. Productivity, seed dispersal and seed predation of A. humilis were investigated in two large (2400 and 3500 ha) and three small (19, 26 and 57 ha) Atlantic Forest fragments in southeastern Brazil. Palms in the small fragments produced more female inflorescences, resulting in a higher fruit production in these places. Seed dispersal rates were higher in the large fragments, where scatter hoarding was more frequent. Scolytine beetles were the main seed predators and damaged a larger number of seeds in small fragments, but predation by rodents and bruchine beetles was low irrespective of fragment size. As scolytines do not necessarily kill the seeds, low predation by bruchines and rodents, together with its own high productivity, allow A. humilis to be more abundant in small fragments despite the scarcity of its main dispersers. This increased abundance, by its turn, can increase competitive interactions between A. humilis and other plants in small fragments. Thus, abundance patterns of A. humilis are a good example of fragmentation affecting the balance of ecological interactions in a complex way, emphasizing the role of preserving ecological processes for conserving biodiversity in fragmented tropical landscapes. Abstract in Portuguese is available at http://www.blackwell‐synergy.com/loi/btp .     

Size-Related Differential Seed Predation in a Heavily Defaunated Neotropical Rain Forest

Hunting and habitat loss represent an increasingly common anthropogenic impact. Available evidence suggests that defaunation is typically differential: medium/large mammals are most affected while small rodents are less affected, or even favored. In heavily impacted areas, such as Los Tuxtlas, the residual mammalian fauna is dominated by small rodents. We tested the expectation that if small rodents will preferentially attack small-seeded species, large-seeded species may escape predation in the absence of medium/large seed predators and that this may affect germination and, possibly, recruitment. Experiments with caged rodents ( Heteromys desmarestianus ) under laboratory conditions showed a preference for smaller seeds. A field experiment involving seeds of contrasting size showed that small, unprotected seeds experienced a predation risk 30-times larger than protected seeds, while the effect of protection was not significant for large seeds. These patterns of predation led to significant differences in germination: protected small-seeded species had a fourfold greater germination than unprotected small-seeded species, while germination was not significantly different between exposed and protected large seeds. The observed contrasts in germination suggest that under heavy defaunation, small-seeded species are likely to be penalized by the overabundance of small rodents, while large-seeded species escape predation. Our results are consistent with the observation of dense seedling carpets dominated by large-seeded species in the understory of Los Tuxtlas. We speculate that the patterns we uncovered may explain, at least partly, the impoverished diversity of the understory vegetation that characterizes heavily defaunated understories and that this has the potential to affect forest regeneration.     

The Role of Arboreal Seed Dispersal Groups on the Seed Rain of a Lowland Tropical Forest1

Most tropical plants produce fleshy fruits that are dispersed primarily by vertebrate frugivores. Behavioral disparities among vertebrate seed dispersers could influence patterns of seed distribution and thus forest structure. This study investigated the relative importance of arboreal seed dispersers and seed predators on the initial stage of forest organization–seed deposition. We asked the following questions: (1) To what degree do arboreal seed dispersers influence the species richness and abundance of the seed rain? and (2) Based on the plant species and strata of the forest for which they provide dispersal services, do arboreal seed dispersers represent similar or distinct functional groups? To answer these questions, seed rain was sampled for 12 months in the Dja Reserve, Cameroon. Seed traps representing five percent of the crown area were erected below the canopies of 90 trees belonging to nine focal tree species: 3 dispersed by monkeys, 3 dispersed by large frugivorous birds, and 3 wind‐dispersed species. Seeds disseminated by arboreal seed dispersers accounted for ca 12 percent of the seeds and 68 percent of the seed species identified in seed traps. Monkeys dispersed more than twice the number of seed species than large frugivorous birds, but birds dispersed more individual seeds. We identified two distinct functional dispersal groups, one composed of large frugivorous birds and one composed of monkeys, drop dispersers, and seed predators. These groups dispersed plants found in different canopy strata and exhibited low overlap in the seed species they disseminated. We conclude it is unlikely that seed dispersal services provided by monkeys could be compensated for by frugivorous birds in the event of their extirpation from Afrotropical forests.     

Seed Predation by Rodents and Implications for Plant Recruitment in Defaunated Atlantic Forests

Rodents are known to perform post‐dispersal seed predation in tropical rain forest, but there is little information on the identity of these seed predators and how they select their seeds. Using cafeteria experiments, we found that seed mass, rodent body mass, and the ratio of seed/rodent mass were determinants of seed consumption.     

Hunting of Mammals Reduces Seed Removal and Dispersal of the Afrotropical Tree Antrocaryon klaineanum (Anacardiaceae)

Throughout the tropics, mammalian seed dispersers are being driven to local extinction by intense hunting pressure, generating concern not only about the loss of these species, but also about the consequences for the plants they disperse. We compared two rain forest sites in Cameroon—one with heavy hunting pressure and one protected from hunting—to appraise the loss of mammalian seed dispersers and to assess the impact of this loss on seed removal and seed dispersal of Antrocaryon klaineanum (Anacardiaceae), a mammal-dispersed tree. Surveys of arboreal frugivores indicate that three of the five monkey species, as well as chimpanzee and gorilla, have been extirpated from the hunted forest. Diaspore counts underneath A. klaineanum adults (six trees per site) indicate that seed removal is severely reduced in the hunted forest. Finally, genetic maternity exclusion analysis (using 3–7 nuclear microsatellite loci) of maternally inherited endocarp tissue from diaspores collected under the canopies of 12 fruiting "mother" trees (six trees per site) revealed that seed dispersal in the hunted forest is also greatly reduced. In the hunted forest with reduced mammal dispersal agents, only 1 of the 53 assayed endocarps (2%) did not match the mother and was determined to be from a dispersed diaspore. By contrast, in the protected forest, 20 of the 48 assayed endocarps (42%) were from dispersed diaspores. This study provides strong evidence that loss of dispersal agents can lead to reduced seed removal and loss of seed dispersal, disrupting the seed dispersal cycle.     

Postdispersal Seed Fate of Tropical Montane Trees in an Agricultural Landscape, Southern Costa Rica

Variation in postdispersal seed fate is an important factor driving patterns of forest regeneration. Because most previous studies have not tracked final seed fate and have commonly equated seed removal with predation without considering the possibility of secondary dispersal, little is known about individual seed mortality factors in successional and degraded habitats. This study tracked the postdispersal fate of large-seeded tropical montane trees in abandoned pasture, young secondary forests, and small forest fragments during two consecutive years in an agricultural landscape in southern Costa Rica. The incidence of secondary dispersal by animals, scatterhoarding in particular, and the effects of seed burial on germination were measured. Overall, seeds survived through germination more often in secondary forests with high levels of mortality occurring in abandoned pastures and forest fragments. The majority of seed mortality was caused by rodent predation in forest fragments, insects and fungal pathogens in secondary forests, and a combination of desiccation, insects, and fungal pathogens in pastures. Seeds were frequently secondarily dispersed in larger forest fragments, whereas they were only rarely moved in pastures and secondary forests. Burial tended to improve germination in pastures and was important for an often scatterhoarded species, Otoba novogranatensis, in all habitats. The results of this study suggest that: (1) seed mortality factors differ in response to the type of habitat degradation; (2) large-seeded species have high potential for survival when dispersed to young secondary forests; and (3) seed removal is not a reliable proxy for seed predation, particularly in less degraded forest fragments.     

亚热带林区啮齿动物对樱桃种子捕食和搬运的作用格局

在都江堰林区,通过在原生林、次生林和灌丛3类生境释放野生和栽培樱桃(Cerasus pseudocerasus)的种子,研究了啮齿动物对樱桃种子的捕食及其对樱桃种群更新的作用。结果表明,啮齿动物对樱桃两类种子的搬运无显著差异,而啮齿动物对野生樱桃种子的收获则明显快于栽培樱桃种子,且在3类生境均有类似的趋势。这说明啮齿动物偏爱于收获具有较高收益(种仁重/种子重)的野生樱桃种子。啮齿动物在小于10 d的时间尺度收获了所有释放的樱桃种子,其中,70%以上为啮齿动物所搬运。春季食物的匮乏可能是导致啮齿动物对樱桃种子有较大捕食压力的主要原因,而生境类型间的差异较小。因此,啮齿动物是都江堰林区樱桃地表种子的主要捕食者,它们对野生樱桃种子的选择性捕食和搬运能影响樱桃种子/果实的进化及其种群更新。     

Seed Rain and Seed Limitation in a Planted Gallery Forest in Brazil

With seeds collected monthly during one year from 53 1‐m² seed traps, we investigated the seed rain and seed limitation in a gallery forest planted in 1994 in SE Brazil. Contrasting animal‐ (zoochorous) and wind‐dispersed (anemochorous) plants we investigated (1) which aspects of the composition and structure of the vegetation influence the abundance and species richness of the seed rain; (2) if such influences differ between zoochorous and anemochorous seeds; (3) if the abundance and richness of the seed rain sampled under zoochorous and nonzoochorous plant species differ; and (4) if seed limitation (given by the proportion of sites to which seeds were not dispersed) differs between zoochorous and anemochorous plant species, and also between species that have been planted and those that further colonized the area (colonists). Seed rain was intense and dominated by anemochorous species. The overall seed rain was not influenced by the vegetation parameters we analyzed (canopy height and cover, plant size, abundance, and richness) or by the plant species above the seed trap. The abundance and richness of zoochorous seeds in a given spot was influenced by the abundance and richness of zoochorous plants in its immediate vicinity. Seed limitation was higher for anemochorous than zoochorous species and higher for planted than for colonist species. We concluded with recommendations for the initial establishment of a planted forest, including the homogeneous distribution of zoochorous plants to permit a spatially homogeneous zoochorous seedfall, which will likely enhance the chances of survival and successful establishment of seeds.     

Seed dynamics of resprouting shrubs in grassy woodlands: Seed rain,predators and seed loss constrain recruitment potential

Abstract Measuring the fate of seeds between seed production and seedling establishment is critical in understanding mechanisms of recruitment limitation of plants. We examined seed fates to better understand the recruitment dynamics of four resprouting shrubs from two families (Fabaceae and Epacridaceae) in temperate grassy woodlands. We tested whether: (i) pre‐dispersal seed predation affected seed rain; (ii) post‐dispersal seed predation limited seed bank accumulation; (iii) the size of the seed bank was related to seed size; and (iv) viable seeds accumulated in the soil after seed rain. There was a distinct difference in seed production per plant between plant families with the legumes producing significantly more seeds per individual than the epacrids. Seed viability ranged from 43% to 81% and all viable had seed or fruit coat dormancy broken by heat or scarification. Pre‐dispersal predation by Lepidopteran larvae removed a large proportion of seed from the legume seed rain but not the epacrids. Four species of ants (Notoncus ectatomoides, Pheidole sp., Rhytidoponera tasmaniensis and Iridomyrmex purpureus) were major post‐dispersal seed removers. Overall, a greater percentage of Hardenbergia (38%) and Pultenaea (59%) seeds were removed than the fleshy fruits of Lissanthe (14%) or Melichrus (0%). Seed bank sizes were small (<15 seeds m^?2) relative to the seed rain and no significant accumulation of seed in the soil was detected. Lack of accumulation was attributed to seed predation as seed decay was considered unlikely and no seed germination was observed in our study sites. Our study suggests that seed predation is a key factor contributing to seed‐limited recruitment in grassy woodland shrubs by reducing the number of seeds stored in the soil.     

The Effects of Seed Dispersal on the Simulation of Long-Term Forest Landscape Change

The study of forest landscape change requires an understanding of the complex interactions of both spatial and temporal factors. Traditionally, forest gap models have been used to simulate change on small and independent plots. While gap models are useful in examining forest ecological dynamics across temporal scales, large, spatial processes, such as seed dispersal, cannot be realistically simulated across large landscapes. To simulate seed dispersal, spatially explicit landscape models that track individual species distribution are needed. We used such a model, LANDIS, to illustrate the implications of seed dispersal for simulating forest landscape change. On an artificial open landscape with a uniform environment, circular-shaped tree species establishment patterns resulted from the simulations, with areas near seed sources more densely covered than areas further from seed sources. Because LANDIS simulates at 10-y time steps, this pattern reflects an integration of various possible dispersal shapes and establishment that are caused by the annual variations in climate and other environmental variables. On real landscapes, these patterns driven only by species dispersal radii are obscured by other factors, such as species competition, disturbance, and landscape structure. To further demonstrate the effects of seed dispersal, we chose a fairly disturbed and fragmented forest landscape (approximately 500,000 ha) in northern Wisconsin. We compared the simulation results of a map with tree species (seed source locations) realistically parameterized (the real scenario) against a randomly parameterized species map (the random scenario). Differences in the initial seed source distribution lead to different simulation results of species abundance with species abundance starting at identical levels under the two scenarios. This is particularly true for the first half of the model run (0–250 y). Under the random scenario, infrequently occurring and shade tolerant species tend to be overestimated, while midabundant and midshade tolerant species tend to be underestimated. The over- and underestimation of species abundance diminish when examining long-term (500 y) landscape dynamics, because stochastic factors, such as fire, tend to make the landscapes under both scenarios converge. However, differences in spatial patterns, and especially species age-cohort distributions, can persist under the two scenarios for several hundred years. Received 24 November 1998; accepted 17 March 1999.     

The Effect of Dung and Dispersal on Postdispersal Seed Predation of Attalea phalerata (Arecaceae) by Bruchid Beetles1

Low postdispersal mortality of palm seeds in tapir dung is hypothesized to result from the mechanical barrier provided by dung against bruchid infestation and/or from the distance to adult palms at which seeds are dispersed. We tested these hypotheses by distributing endocarps of Attalea phalerata Mart. ex Spreng. in experimental dung piles in Beni, Bolivia. Predation rates were significantly lower for seeds covered by dung than for exposed or partially covered seeds, but did not differ between seeds placed below and 50 m away from palms. Thus, dung, not short‐distance dispersal, protects seeds against bruchid beetles, and may ultimately promote survival of palm seeds.