Tamarins and Dung Beetles: An Efficient Diplochorous Dispersal System in the Peruvian Amazonia

Dung beetles fulfill several key functions in ecosystems but their role as secondary seed dispersers is probably one of the most complex ones. Various factors, such as seed characteristics, dispersal pattern induced by the primary disperser, season, and habitat, can affect the seed–beetle interaction. Particularly little is known about the fate of seeds primarily dispersed in small feces. The aim of this study was to investigate the effects of these factors on the dung beetle community (species composition, number and size of individuals) and its consequences on burial occurrence and depth of seeds primarily dispersed by two tamarin species. We captured dung beetles in a Peruvian rain forest with 299 dung‐baited pitfall traps to characterize the dung beetle community. Seed burial occurrence and depth were assessed by marking in situ 551 dispersed seeds in feces placed in cages. Among these seeds, 22.5 percent were buried by dung beetles after 2 d. We observed a significant effect of the amount of dung, season, time of deposition, and habitat on the number of individuals and species of dung beetles, as well as on seed burial occurrence and depth, while the tamarin species significantly influenced only the number and the size of dung beetles. This seed dispersal loop is particularly important for forest regeneration: small to large seeds dispersed by tamarins in secondary forest can be buried by dung beetles. These seeds can thus benefit from a better protection against predation and a more suitable microenvironment for germination, potentially enhancing seedling recruitment.     

Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers

Abstract 1. The role of several factors that affect the composition of the dung beetle assemblages in an Amazonian rainforest was quantified, together with the effect of these factors on the role that dung beetles play as secondary seed dispersers. 2. A total of 61 dung beetle species was captured during 3360 h of trapping. During nocturnal trapping periods, more dung beetles, of larger mean size, and more species were captured per trap than during diurnal trapping periods. 3. During the rainy season, more dung beetle species were captured per trap than during the dry season, but the number of individuals and their mean size did not vary between seasons. 4. Bait size had a significant effect on the mean number of beetles and mean number of species but not on mean beetle size. As bait size increased from 5, 10, 25, to 50 g, more beetles and more species were captured per trap. 5. Between 6 and 73% of plastic beads, used as seed mimics, were buried by dung beetles at depths that ranged from 0.5 to 7 cm. Both the proportion of beads buried and burial depth decreased with increasing bead size, and increased with increasing amounts of dung surrounding each bead (5, 10, and 25 g). 6. The proportion of buried seeds for three species varying in size between 5 and 27 mm, increased with increasing dung beetle size, using beetles of seven sizes, varying between 10 and 25 mm. 7. Seeds surrounded by dung were buried more often and more deeply when placed on the forest floor during the late afternoon than when placed during the early morning. Seeds were also buried more often when placed on the forest floor during the rainy season than when placed during the dry season, but season had no effect on burial depth. 8. Forests in Central Amazonia hold a rich dung beetle community that plays an active role in secondary seed dispersal, and consequently in plant regeneration. The interaction between seeds and beetles is complex because it is affected by many factors.     

Secondary dispersal mechanisms of winged seeds: a review

Winged seeds, or samaras, are believed to promote the long‐distance dispersal and invasive potential of wind‐dispersed trees, but the full dispersive potential of these seeds has not been well characterised. Previous research on the ecology of winged seeds has largely focussed on the initial abscission and primary dispersal of the samara, despite it being known that the primary wind dispersal of samaras is often over short distances, with only rare escapes to longer distance dispersal. Secondary dispersal, or the movement of the seeds from the initial dispersal area to the site of germination, has been largely ignored despite offering a likely important mechanism for the dispersal of samaras to microhabitats suitable for establishment. Herein, we synthesise what is known on the predation and secondary dispersal of winged seeds by multiple dispersive vectors, highlighting gaps in knowledge and offering suggestions for future research. Both hydrochory and zoochory offer the chance for samaroid seeds to disperse over longer distances than anemochory alone, but the effects of the wing structure on these dispersal mechanisms have not been well characterised. Furthermore, although some studies have investigated secondary dispersal in samaroid species, such studies are scarce and only rarely track seeds from source to seedling. Future research must be directed to studying the secondary dispersal of samaras by various vectors, in order to elucidate fully the invasive and colonisation potential of samaroid trees.     

Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical forest

Much of the literature on the relationship between species richness or functional group richness and measures of ecosystem function focuses on a restricted set of ecosystem function measures and taxonomic groups. Few such studies have been carried out under realistic levels of diversity in the field, particularly in high diversity ecosystems such as tropical forests. We used exclusion experiments to study the effects of dung beetle functional group richness and composition on two interlinked and functionally important ecological processes, dung removal and secondary seed dispersal, in evergreen tropical forest in Sabah, Malaysian Borneo. Overall, both dung and seed removal increased with dung beetle functional group richness. However, levels of ecosystem functioning were idiosyncratic depending on the identity of the functional groups present, indicating an important role for functional group composition. There was no evidence for interference or competition among functional groups. We found strong evidence for overyielding and transgressive overyielding, suggesting complementarity or facilitation among functional groups. Not all mixtures showed transgressive overyielding, so that complementarity was restricted to particular functional group combinations. Beetles in a single functional group (large nocturnal tunnellers) had a disproportionate influence on measures of ecosystem function: in their absence dung removal is reduced by approximately 75%. However, a full complement of functional groups is required to maximize ecosystem functioning. This study highlights the importance of both functional group identity and species composition in determining the ecosystem consequences of extinctions or altered patterns in the relative abundance of species.     

Edge Effects Act Differentially on Multiple Early Regeneration Stages of a Shade‐tolerant Tree Tapirira mexicana

Forest fragmentation is pervasive in tropical landscapes, and one pathway by which fragmentation may negatively impact populations is via edge effects. Early life‐stages are particularly important for species regeneration as they act as bottlenecks, but how edge effects may act differentially on different life‐stages is unknown. This study evaluated edge effects on multiple early life‐stages of a currently common animal‐dispersed, shade‐tolerant tree Tapirira mexicana (Anacardiaceae). The study was conducted in tropical premontane wet forest fragments in a highly deforested region of Costa Rica. The stages assessed were pre‐dispersal predation, primary dispersal, post‐dispersal predation, secondary dispersal, ex situ germination, in situ seed longevity, first and second year seedling abundance, second year seedling survivorship, and basal diameter growth. Results showed that impacts of edge effects were not equal across stages, but were limited to specific stages and times. One stage which may act as a bottleneck for species regeneration was pre‐dispersal predation. Over 60 percent of the seeds were predated by larvae, and predation was higher near the edge than interior habitat. Seeds lost viability within 10 d in the forest. Germination to first year seedling stage was also lower near edges, but such effect was eliminated within a year after that. Primary dispersal, seedling survivorship, and growth were not affected by proximity to edges, and both secondary dispersal and post‐dispersal predation were rare. This study demonstrates that current population abundance may not guarantee future species persistence and the importance of considering multiple life‐stages for a comprehensive assessment of forest fragmentation effects on species regeneration.     

Directed seed dispersal towards areas with low conspecific tree density by a scatter‐hoarding rodent

Scatter‐hoarding animals spread out cached seeds to reduce density‐dependent theft of their food reserves. This behaviour could lead to directed dispersal into areas with lower densities of conspecific trees, where seed and seedling survival are higher, and could profoundly affect the spatial structure of plant communities. We tested this hypothesis with Central American agoutis and Astrocaryum standleyanum palm seeds on Barro Colorado Island, Panama. We radio‐tracked seeds as they were cached and re‐cached by agoutis, calculated the density of adult Astrocaryum trees surrounding each cache, and tested whether the observed number of trees around seed caches declined more than expected under random dispersal. Seedling establishment success was negatively dependent on seed density, and agoutis carried seeds towards locations with lower conspecific tree densities, thus facilitating the escape of seeds from natural enemies. This behaviour may be a widespread mechanism leading to highly effective seed dispersal by scatter‐hoarding animals.     

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.     

The full path of Janzen-Connell effects: genetic tracking of seeds to adult plant recruitment

The Janzen-Connell (J-C) model (Janzen 1970; Connell 1971) has been a dominant yet controversial paradigm for forest community dynamics for four decades, especially in the tropics. With increasing distance from the parent plant, the density of dispersed seeds decreases and, because of a reduced impact of distance- and density-responsive seed and seedling enemies, propagule survival increases, resulting in peak recruitment at some distance from the parent and little recruitment near adult conspecifics. This spacing generates gaps near adult trees for the recruitment of heterospecifics, enhancing species coexistence and species richness. Field studies, primarily focused on seeds and young seedlings, have repeatedly demonstrated increasing survival with increasing distance from parents or decreasing density of propagules (e.g. Clark & Clark 1984; Gilbert et al. 1994; Swamy & Terborgh 2010). Yet a meta-analysis of distance-dependent propagule survival failed to support a general pattern of survival increasing with distance from adult conspecifics, suggesting that there is no need for further experimental tests of the J-C hypothesis in terms of diversity enhancement-results are species-specific, not general (Hyatt et al. 2003). However, a lack of consistent experimental results is not surprising. The outcome of tests of the hypothesis can vary as a function of many factors that can affect successive recruitment stages differently (Schupp 1992; Hyatt et al. 2003; Swamy & Terborgh 2010). This highlights a critical gap-a full test of the J-C model requires data demonstrating that effects carry over to recruitment of new reproductive adults, yet few studies have gone beyond early stages. There is strong inferential evidence that adult trees can show the imprint of J-C effects (e.g. Nathan et al. 2000; Howe & Miriti 2004), and focal individual modelling has clearly demonstrated that J-C effects can operate from sapling through adult stages in a significant number of species (Peters 2003). It is likely that such results are not unusual, but there have been few attempts to demonstrate J-C spacing at the adult stage. In this issue of Molecular Ecology, Steinitz et al. (2011) studied the Mediterranean pine Pinus halepensis (Aleppo pine) and combined a unique situation with an innovative approach to provide the most elegant demonstration yet that adult recruits are spaced further from parents than expected from the initial seed distribution, clear evidence of a J-C effect carrying over to reproductive adults. A major advancement of this study is that it incorporates estimates of the initial patterns of seed dispersal and parentage analysis of adult-offspring relationships, illustrating the value of combined field and genetic approaches.     

浙江省典型天然次生林主要树种空间分布格局及其关联性

松阔混交林和常绿阔叶林是亚热带地区天然次生林代表性的森林类型,通过研究主要树种分布变动趋势,可以有效地指导森林经营措施。在该地区4个1hm~2典型样地,在0—30m尺度范围内综合分析了主要树种的空间分布格局及种间关联性,并对同一树种分发育阶段在不同森林群落中的种群空间分布格局进行了比较,以探讨亚热带地区天然次生林群落空间格局形成和种群维持机制。样地1和2为松阔混交林,其中样地1的马尾松密度较低,样地3和4为常绿阔叶林。研究结果表明:(1)以完全随机模型为零假设时,样地1的主要种群在小尺度(10 m)呈聚集分布,随尺度增加呈随机分布;样地2—4的主要种群在所有尺度呈聚集分布,随尺度增加聚集强度逐渐减弱;以异质泊松模型为零假设时,4个样地的主要种群在大部分尺度呈随机分布;(2)青冈和苦槠的小树(5.0 cm≤DBH10.0 cm)在4样地的所有尺度以聚集分布为主,大树(DBH≥10.0 cm)在松阔混交林样地呈随机分布趋势,但在常绿阔叶林样地青冈在0—20 m尺度、苦槠在所有尺度呈聚集分布;(3)松阔混交林中建群种马尾松和其他树种的种间关联性,在样地1的小尺度为负相关,随尺度增加为不相关,在样地2的所有尺度为负相关;常绿阔叶林中建群种青冈和其他树种的种间关联性在在样地3的小尺度为负相关,随尺度增加为不相关,在样地4的所有尺度为负相关;所有伴生树种的种间关联性以负相关为主。结果说明,种群空间分布格局及其关联性随群落结构和空间尺度的不同而出现变化,在松阔混交林和常绿阔叶林群落格局形成中除了扩散限制和生境异质性以外,密度制约机制在松阔混交林中发挥了重要作用,而在常绿阔叶林中其作用随着树木生活史阶段的提高而减弱。     

Halting Regime Shifts in Floristically Intact Tropical Forests Deprived of Their Frugivores

Ecological restoration typically focuses on promoting vegetation recovery in degraded habitat or reintroducing endangered animals to enhance their regional or global persistence. Here, we argue that attention should also be devoted to vertebrate reintroductions in overhunted but floristically intact tropical forests in order to prevent insidious regime shifts in these systems. Growing evidence suggests that tropical forests deprived of seed‐dispersing animals exhibit replacement of fleshy fruiting trees by species with abiotic seed dispersal. Left unchecked, this process could eventually render the forest uninhabitable by frugivores through reduced density and diversity of their food plants. In tropical areas where hunting can be controlled, we contend that frugivore reintroduction, regulation of wild fruit harvest by humans, and outplanting of native fruiting trees should be deployed as management tools long before the systems are in need of traditional habitat restoration.     

Primate and Dung Beetle Communities in Secondary Growth Rain Forests: Implications for Conservation of Seed Dispersal Systems

Conservation efforts are often aimed at one or a few species. However, habitat sustainability relies on ecological interactions among species, such as seed dispersal. Thus, a community-scale conservation strategy may be more valuable in some settings. We describe communities of primary (primates) and secondary (dung beetles) seed dispersers from 5 sites in the Brazilian Amazon. We estimate community biomass of these taxa and, using multivariate ordination, examine the potential for natural reforestation at each site, given the communities of seed dispersers present. Since disturbed habitat is increasingly common and increasingly the focus of conservation efforts, we also examine differences among seed disperser communities between primary forest and secondary growth at each site. Analyses of faunal biomass in different localities and habitats indicate that secondary growth receives nearly as much use by primates as primary forest; given the dominant groups of dung beetles in secondary growth, disturbed habitat should show a pattern of seed burial that is clumped and deep. Areas with high biomass of Alouatta spp. and the large nocturnal dung beetle species may have the greatest potential for natural reforestation of secondary growth particularly for large seeded species. The data suggest that knowledge of the biomass of primary and secondary dispersing fauna facilitates predictions for the likelihood of disturbed habitat to regenerate and comparisons of sites in broader geographical areas e.g., Neotropical vs. Paleotropical forests.     

Fragmentation and Alteration of Seed Dispersal Processes: An Initial Evaluation of Dung Beetles, Seed Fate, and Seedling Diversity1

Given current accelerated trends of tropical land conversion, forest fragments are being incorporated into many conservation programs. For investing in fragments to be a viable conservation strategy, forest fragments must maintain their ecological integrity over the long term. Based on fieldwork in 22 forest fragments in the crater lakes region of western Uganda and in the continuous forest of Kibale National Park, we examined (1) seed predation on experimentally dispersed seeds, (2) abundance and composition of the dung beetle community that may play a major role in removing seeds from sites of high seed predation, and (3) compared the fragments’ seedling community composition to adult tree community composition and the seedling community in continuous forest. First, the rate of seed removal at experimental stations was lower in forest fragments (85% remaining after 1 day) than at stations in the continuous forest (79% remaining) and the probability of stations being discovered by seed predators was lower in fragments (23%) than in the intact forest (41%). Second, there was a 62 percent decline in fragment dung beetle abundance. The magnitude of this decline varied among dung beetle guilds that process dung and seeds in different fashions. The abundance of large rollers that move large seeds away from sites of defecation did not differ, but medium and smaller rollers and burying beetles that process small and medium‐sized seeds were less common in the fragments than in the intact forest. Finally, we compared the seedling community composition relative to adult tree community composition by identifying all adult trees in each fragment and by sampling the composition of the seedling community. We found some evidence to suggest that there was movement of seeds among forest fragments by large‐bodied dispersers, particularly chimpanzees (Pan troglodytes) and hornbills (Ceratogymna subcylindricus).     

Multiple natural enemies cause distance‐dependent mortality at the seed‐to‐seedling transition

Specialised natural enemies maintain forest diversity by reducing tree survival in a density‐ or distance‐dependent manner. Fungal pathogens, insects and mammals are the enemy types most commonly hypothesised to cause this phenomenon. Still, their relative importance remains largely unknown, as robust manipulative experiments have generally targeted a single enemy type and life history stage. Here, we use fungicide, insecticide and physical exclosure treatments to isolate the impacts of each enemy type on two life history stages (germination and early seedling survival) in three tropical tree species. Distance dependence was evident for five of six species‐stage combinations, with each enemy type causing distance dependence for at least one species stage and their importance varying widely between species and stages. Rather than implicating one enemy type as the primary agent of this phenomenon, our field experiments suggest that multiple agents acting at different life stages collectively contribute to this diversity‐promoting mechanism.     

The Plight of Large Animals in Tropical Forests and the Consequences for Plant Regeneration

We introduce a special section that addresses the bushmeat or wild meat crisis, its direct impact on game species, and its indirect impact on plants in tropical forests.     

Density‐dependent Survival in Seedlings Differs among Woody Life‐forms in Tropical Wet Forests of a Caribbean Island

Negative density dependence contributes to seedling dynamics in forested ecosystems, but the relative importance of this factor for different woody plant life‐forms is not well‐understood. We used 1 yr of seedling survivorship data for woody seedlings in 17 different plots of lower to mid‐montane rain forests on the island of Dominica to examine how seedling height, abiotic factors, and biotic factors such as negative density dependence are related to seedling survival of five different life‐forms (canopy, midstory, and understory trees; shrubs; and lianas). Across 64 species, taller seedlings in seedling plots with higher canopy openness, greater seedling density, lower relative abundance of conspecific seedlings, and lower relative abundance of conspecific adults generally had a greater probability of surviving. Height was the strongest predictor of seedling survival for all life‐forms except lianas. Greater seedling density was positively related to survival for canopy and midstory trees but negatively related to survival for the other life‐forms. For trees, the relative abundance of conspecific seedling and adult neighbors had weak and strong negative effects on survival respectively. Neither shrub nor liana seedling survival was affected by the relative abundance of conspecific neighbors. Thus, negative density dependence is confirmed as an important structuring mechanism for tree seedling communities but does not seem to be important for lianas and shrubs in Dominican rain forests. These results represent the first direct assessment of controls on seedling survival of all woody life‐forms – an important step in understanding the dynamics and structure of the entire woody plant community.     

Recruitment Distance from the Nearest Reproductive Conspecific Increases with Tree Size in Tropical Premontane Wet Forests

Studies have shown that median distances of plants from the nearest reproductive conspecific (recruitment distance) shifts outward with increasing age or size class, and that plant spatial distribution changes over time in a predictable manner. However, observations and empirical evidence for such predictable changes are limited, and underlying mechanisms explaining such patterns for a wide range of individual sizes are not fully explored. In Costa Rican premontane wet forests, I empirically tested whether recruitment distance changes in a predictable manner with increasing size for five animal‐dispersed tree species by considering all post‐germination sizes. Specifically, I tested the Janzen–Connell hypothesis and the colonization hypothesis by considering distance, density, size, herbivory, biotic infection, and light availability simultaneously. Recruitment distance increased with increasing size (16–22 m) for the four non‐pioneer species, suggesting eventual regeneration success for seeds dispersed away from reproductive conspecifics. During the 2 years of this study, I found positive distance‐dependent survivorship and light availability were important for post‐seedling survivorship, in agreement with the Janzen–Connell hypothesis and the colonization hypothesis, respectively, but only for seedlings. However, seedlings did not escape aboveground herbivory or biotic infection better when the seeds were dispersed greater distances. Results highlight the importance of seed dispersal for successful regeneration, and suggest that changes in spatial distribution over time may be predictable in the vicinity of maternal trees for some non‐pioneer tree species.     

Comparing the Dispersal of Large-seeded Tree Species by Frugivore Assemblagesin Tropical Montane Forest in Africa

We examined frugivore visitation and seed dispersal of five large-seeded (≥ 5 mm) tree species in tropical montane forest based on their occurrence in frugivorous primate diets: Ekebergia capensis, Olea capensis, Parinari excelsa, Prunus africana , and Syzygium guineense. A total of 21 frugivores in five assemblages ( i.e. , chimpanzees, cercopithecines, large-bodied birds, small-bodied birds, and squirrels) were observed over the study period (August 2006 and October–April 2007). We observed seed dispersal in four of five tree species studied; no dispersal was observed for P. excelsa . Frugivore assemblages did not visit tree species equally. Primates spent the most time in trees and had the largest group size. Large-bodied birds (LB) and chimpanzees dispersed the highest number of seeds per minute. LB and cercopithecines potentially dispersed the greatest number of seeds for E. capensis , and chimpanzees for S. guineense . Our analyses indicated that the mean fruiting duration of the focal tree, time in the tree, and number of species present are important predictor variables for seed dispersal by small- and large-bodied birds, and cercopithecines. The number of fruiting trees in the immediate vicinity of the focal tree further predicted seed dispersal for small-bodied birds (SB). Large-bodied birdseed dispersal also was predicted by time in tree by SB, and the number of individuals for SB and cercopithecines. Cercopithecines (CS) were further explained by the time in tree and number of species (SB & LB), and number of individuals for CS. Our study highlights the complexity of describing the relative importance of a frugivore assemblage to the dispersal of a tree species seeds.