Trait matching and sampling effort shape the structure of the frugivory network in Afrotropical forests.

Frugivory in tropical forests is a major ecological process as most tree species rely on frugivores to disperse their seeds. However, the underlying mechanisms driving frugivore-plant networks remain understudied. Here, we evaluate the data available on the Afrotropical frugivory network to identify structural properties, as well as assess knowledge gaps. We assembled a database of frugivory interactions from the literature with > 10 000 links, between 807 tree and 285 frugivore species. We analysed the network structure using a block model that groups species with similar interaction patterns and estimates interaction probabilities among them. We investigated the species traits related to this grouping structure. This frugivory network was simplified into 14 tree and 14 frugivore blocks. The block structure depended on the sampling effort among species: Large mammals were better-studied, while smaller frugivores were the least studied. Species traits related to frugivory were strong predictors of the species composition of blocks and interactions among them. Fruits from larger trees were consumed by most frugivores, and large frugivores had higher probabilities to consume larger fruits. To conclude, this large-scale frugivory network was mainly structured by species traits involved in frugivory, and as expected by the distribution areas of species, while still being limited by sampling incompleteness.

Biodiversity and vector-borne diseases: Host dilution and vector amplification occur simultaneously for Amazonian leishmaniases.

Changes in biodiversity may impact infectious disease transmission through multiple mechanisms. We explored the impact of biodiversity changes on the transmission of Amazonian leishmaniases, a group of wild zoonoses transmitted by phlebotomine sand flies (Psychodidae), which represent an important health burden in a region where biodiversity is both rich and threatened. Using molecular analyses of sand fly pools and blood-fed dipterans, we characterized the disease system in forest sites in French Guiana undergoing different levels of human-induced disturbance. We show that the prevalence of Leishmania parasites in sand flies correlates positively with the relative abundance of mammal species known as Leishmania reservoirs. In addition, Leishmania reservoirs tend to dominate in less diverse mammal communities, in accordance with the dilution effect hypothesis. This results in a negative relationship between Leishmania prevalence and mammal diversity. On the other hand, higher mammal diversity is associated with higher sand fly density, possibly because more diverse mammal communities harbor higher biomass and more abundant feeding resources for sand flies, although more research is needed to identify the factors that shape sand fly communities. As a consequence of these antagonistic effects, decreased mammal diversity comes with an increase of parasite prevalence in sand flies, but has no detectable impact on the density of infected sand flies. These results represent additional evidence that biodiversity changes may simultaneously dilute and amplify vector-borne disease transmission through different mechanisms that need to be better understood before drawing generalities on the biodiversity-disease relationship.

Arboreal camera trap reveals the frequent occurrence of a frugivore-carnivore in neotropical nutmeg trees.

Arboreal and flying frugivorous animals represent primary dispersers in the Neotropics. Studies suggest a possible compensation for the loss of large species by smaller ones with expanding rampant anthropogenic pressures and declining populations of larger frugivores. However, studies on seed dispersal by frugivores vertebrates generally focus on the diurnal, terrestrial, canopy, and flying species, with the nocturnal canopy ones being less studied. Setting camera traps high in the canopy of fruiting nutmeg trees revealed for the first time the high frequency of the kinkajou (Potos flavus, Schreber, 1774, Procyonidae), an overlooked nocturnal frugivore species (Order Carnivora) in the Guianas. The diversity of the fruit species consumed by the kinkajou calls for considering it as an important seed disperser. The overlap of the size of seeds dispersed by frugivores observed in nutmeg trees suggests that the small (2-5 kg) kinkajou may compensate for the loss of large (5-10 kg) frugivorous vertebrates in the canopy. Camera traps visualise how the kinkajou is adapted to forage in the nutmeg tree crown and grab the fruit. Such information is vital for conservation because compensation of seed dispersal by small frugivores is crucial in increasing anthropogenic stressors.

Modifications of the rain forest frugivore community are associated with reduced seed removal at the community level.

Tropical rain forests worldwide are under increasing pressure from human activities, which are altering key ecosystem processes such as plant-animal interactions. However, while the direct impact of anthropogenic disturbance on animal communities has been well studied, the consequences of such defaunation for mutualistic interactions such as seed dispersal remains chiefly understood at the plant species level. We asked whether communities of endozoochorous tree species had altered seed removal in forests affected by hunting and logging and if this could be related to modifications of the frugivore community. At two contrasting forest sites in French Guiana, Nouragues (protected) and Montagne de Kaw (hunted and partly logged), we focused on four families of animal-dispersed trees (Sapotaceae, Myristicaceae, Burseraceae, and Fabaceae), which represent 88% of all endozoochorous trees that were fruiting at the time and location of the study. We assessed the abundance of the seed dispersers and predators of these four focal families by conducting diurnal distance sampling along line transects. Densities of several key seed dispersers such as large-bodied primates were greatly reduced at Montagne de Kaw, where the specialist frugivore Ateles paniscus is probably extinct. In parallel, we estimated seed removal rates from fruit and seed counts conducted in 1-m2 quadrats placed on the ground beneath fruiting trees. Seed removal rates dropped from 77% at Nouragues to 47 % at Montagne de Kaw, confirming that the loss of frugivores associated with human disturbance impacts seed removal at the community level. In contrast to Sapotaceae, whose seeds are dispersed by mammals only, weaker declines in seed removal for Burseraceae and Myristicaceae suggest that some compensation may occur for these bird- and mammal-dispersed families, possibly because of the high abundance of Toucans at the disturbed site. The defaunation process currently occurring across many tropical forests could dramatically reduce the diversity of entire communities of animal-dispersed trees through seed removal limitation.

Pollination by the locally endangered island flying fox (Pteropus hypomelanus) enhances fruit production of the economically important durian (Durio zibethinus).

Fruit bats provide valuable pollination services to humans through a unique coevolutionary relationship with chiropterophilous plants. However, chiropterophily in the Old World and the pollination roles of large bats, such as flying foxes (Pteropus spp., Acerodon spp., Desmalopex spp.), are still poorly understood and require further elucidation. Efforts to protect these bats have been hampered by a lack of basic quantitative information on their role as ecosystem service providers. Here, we investigate the role of the locally endangered island flying fox Pteropus hypomelanus in the pollination ecology of durian (Durio zibethinus), an economically important crop in Southeast Asia. On Tioman Island, Peninsular Malaysia, we deployed 19 stations of paired infrared camera and video traps across varying heights at four individual flowering trees in a durian orchard. We detected at least nine species of animal visitors, but only bats had mutualistic interactions with durian flowers. There was a clear vertical stratification in the feeding niches of flying foxes and nectar bats, with flying foxes feeding at greater heights in the trees. Flying foxes had a positive effect on mature fruit set and therefore serve as important pollinators for durian trees. As such, semi-wild durian trees-particularly tall ones-may be dependent on flying foxes for enhancing reproductive success. Our study is the first to quantify the role of flying foxes in durian pollination, demonstrating that these giant fruit bats may have far more important ecological, evolutionary, and economic roles than previously thought. This has important implications and can aid efforts to promote flying fox conservation, especially in Southeast Asian countries.

Coexistence and Conflict between the Island Flying fox (Pteropus hypomelanus) and Humans on Tioman Island, Peninsular Malaysia.

As tropical landscapes become increasingly human-dominated, conflicts between people and wildlife threaten ecological processes. Old World fruit bats such as flying foxes are especially susceptible to extinction risk because there is low interest in their conservation, particularly when they are considered pests. In order to arrest fruit bat declines, there is an urgent need to understand human-bat conflict and its implications. On a tropical island in Peninsular Malaysia, we conducted a questionnaire survey to investigate coexistence between people and the island flying fox (Pteropus hypomelanus). Among 119 respondents, knowledge of ecosystem services provided by flying foxes was extremely low. Most respondents held negative attitudes towards the bats, and older male locals were more likely to support killing them. This was also true for older owners of fruit trees who derived income from selling fruit, and experienced flying fox raids. Our results can be used to design appropriate interventions to support conservation efforts, and has important implications for managing conflicts between humans and synanthropic wildlife.

Elucidating the diet of the island flying fox (Pteropus hypomelanus) in Peninsular Malaysia through Illumina Next-Generation Sequencing.

There is an urgent need to identify and understand the ecosystem services of pollination and seed dispersal provided by threatened mammals such as flying foxes. The first step towards this is to obtain comprehensive data on their diet. However, the volant and nocturnal nature of bats presents a particularly challenging situation, and conventional microhistological approaches to studying their diet can be laborious and time-consuming, and provide incomplete information. We used Illumina Next-Generation Sequencing (NGS) as a novel, non-invasive method for analysing the diet of the island flying fox (Pteropus hypomelanus) on Tioman Island, Peninsular Malaysia. Through DNA metabarcoding of plants in flying fox droppings, using primers targeting the rbcL gene, we identified at least 29 Operationally Taxonomic Units (OTUs) comprising the diet of this giant pteropodid. OTU sequences matched at least four genera and 14 plant families from online reference databases based on a conservative Least Common Ancestor approach, and eight species from our site-specific plant reference collection. NGS was just as successful as conventional microhistological analysis in detecting plant taxa from droppings, but also uncovered six additional plant taxa. The island flying fox's diet appeared to be dominated by figs (Ficus sp.), which was the most abundant plant taxon detected in the droppings every single month. Our study has shown that NGS can add value to the conventional microhistological approach in identifying food plant species from flying fox droppings. At this point in time, more accurate genus- and species-level identification of OTUs not only requires support from databases with more representative sequences of relevant plant DNA, but probably necessitates in situ collection of plant specimens to create a reference collection. Although this method cannot be used to quantify true abundance or proportion of plant species, nor plant parts consumed, it ultimately provides a very important first step towards identifying plant taxa and spatio-temporal patterns in flying fox diets.

Meta-analysis of the effects of human disturbance on seed dispersal by animals.

Animal-mediated seed dispersal is important for sustaining biological diversity in forest ecosystems, particularly in the tropics. Forest fragmentation, hunting, and selective logging modify forests in myriad ways and their effects on animal-mediated seed dispersal have been examined in many case studies. However, the overall effects of different types of human disturbance on animal-mediated seed dispersal are still unknown. We identified 35 articles that provided 83 comparisons of animal-mediated seed dispersal between disturbed and undisturbed forests; all comparisons except one were conducted in tropical or subtropical ecosystems. We assessed the effects of forest fragmentation, hunting, and selective logging on seed dispersal of fleshy-fruited tree species. We carried out a meta-analysis to test whether forest fragmentation, hunting, and selective logging affected 3 components of animal-mediated seed dispersal: frugivore visitation rate, number of seeds removed, and distance of seed dispersal. Forest fragmentation, hunting, and selective logging did not affect visitation rate and were marginally associated with a reduction in seed-dispersal distance. Hunting and selective logging, but not fragmentation, were associated with a large reduction in the number of seeds removed. Fewer seeds of large-seeded than of small-seeded tree species were removed in hunted or selectively logged forests. A plausible explanation for the consistently negative effects of hunting and selective logging on large-seeded plant species is that large frugivores, as the predominant seed dispersers for large-seeded plant species, are the first animals to be extirpated from hunted or logged forests. The reduction in forest area after fragmentation appeared to have weaker effects on frugivore communities and animal-mediated seed dispersal than hunting and selective logging. The differential effects of hunting and selective logging on large- and small-seeded tree species underpinned case studies that showed disrupted plant-frugivore interactions could trigger a homogenization of seed traits in tree communities in hunted or logged tropical forests.

Averting biodiversity collapse in tropical forest protected areas.

The rapid disruption of tropical forests probably imperils global biodiversity more than any other contemporary phenomenon. With deforestation advancing quickly, protected areas are increasingly becoming final refuges for threatened species and natural ecosystem processes. However, many protected areas in the tropics are themselves vulnerable to human encroachment and other environmental stresses. As pressures mount, it is vital to know whether existing reserves can sustain their biodiversity. A critical constraint in addressing this question has been that data describing a broad array of biodiversity groups have been unavailable for a sufficiently large and representative sample of reserves. Here we present a uniquely comprehensive data set on changes over the past 20 to 30 years in 31 functional groups of species and 21 potential drivers of environmental change, for 60 protected areas stratified across the world's major tropical regions. Our analysis reveals great variation in reserve 'health': about half of all reserves have been effective or performed passably, but the rest are experiencing an erosion of biodiversity that is often alarmingly widespread taxonomically and functionally. Habitat disruption, hunting and forest-product exploitation were the strongest predictors of declining reserve health. Crucially, environmental changes immediately outside reserves seemed nearly as important as those inside in determining their ecological fate, with changes inside reserves strongly mirroring those occurring around them. These findings suggest that tropical protected areas are often intimately linked ecologically to their surrounding habitats, and that a failure to stem broad-scale loss and degradation of such habitats could sharply increase the likelihood of serious biodiversity declines.

Phylogenetic density dependence and environmental filtering predict seedling mortality in a tropical forest.

Negative density dependence (NDD) and environmental filtering (EF) shape community assembly, but their relative importance is poorly understood. Recent studies have shown that seedling's mortality risk is positively related to the phylogenetic relatedness of neighbours. However, natural enemies, whose depredations often cause NDD, respond to functional traits of hosts rather than phylogenetic relatedness per se. To understand the roles of NDD and EF in community assembly, we assessed the effects on seedling mortality of functional similarity, phylogenetic relatedness and stem density of neighbouring seedlings and adults in a species-rich tropical forest. Mortality risks increased for common species when their functional traits departed substantially from the neighbourhood mean, and for all species when surrounded by close relatives. This indicates that NDD affects community assembly more broadly than does EF, and leads to the tentative conclusion that natural enemies respond to phylogenetically correlated traits. Our results affirm the prominence of NDD in structuring species-rich communities.

Fruit availability, frugivore satiation and seed removal in 2 primate-dispersed tree species.

During a mast-fruiting event we investigated spatial variability in fruit availability, consumption, and seed removal at two sympatric tree species, Manilkara bidentata and M. huberi (Sapotaceae) at Nouragues Natural Reserve, French Guiana. We addressed the question of how Manilkara density and fruits at the community level might be major causes of variability in feeding assemblages between tree species. We thus explored how the frugivore assemblages differed between forest patches with contrasting relative Manilkara density and fruiting context. During the daytime, Alouatta seniculus was more often observed in M. huberi crowns at Petit Plateau (PP) with the greatest density of Manilkara spp. and the lowest fruit diversity and availability, whereas Cebus apella and Saguinus midas were more often observed in M. bidentata crowns at both Grand Plateau (GP), with a lowest density of M. bidentata and overall greater fruit supply, and PP. Overall, nearly 53% and 15% of the M. bidentata seed crop at GP and PP, respectively, and about 47% of the M. huberi seed crop were removed, otherwise either spit out or defecated beneath trees, or dropped in fruits. Small-bodied primates concentrated fallen seeds beneath parent trees while large-bodied primate species removed and dispersed more seeds away from parents. However, among the latter, satiated A. seniculus wasted seeds under conspecific trees at PP. Variations in feeding assemblages, seed removal rates and fates possibly reflected interactions with extra-generic fruit species at the community level, according to feeding choice, habitat preferences and ranging patterns of primate species.

Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction.

The 5th Symposium on Frugivores and Seed Dispersal, held in Montpellier (France), 13-18 June 2010, brought together more than 220 researchers exemplifying a wide diversity of approaches to the study of frugivory and dispersal of seeds. Following Ted Fleming and Alejandro Estrada's initiative in 1985, this event was a celebration of the 25th anniversary of the first meeting in Veracruz, Mexico. Frugivory and seed dispersal are active research areas that have diversified in multiple directions since 1985 to include evolution (e.g. phylogenetic diversity and dispersal adaptations), physiology (e.g. sensory cues and digestion), landscape ecology (movement patterns), molecular ecology (e.g. gene flow, genetic diversity and structure), community ecology (e.g. mutualistic interaction networks) and conservation biology (effects of hunting, fragmentation, invasion and extinction), among others. This meeting provided an opportunity to assess conceptual and methodological progress, to present ever more sophisticated insights into frugivory in animals and dispersal patterns in plants, and to report the advances made in examining the mechanisms and consequences of seed dispersal for plants and frugivores.

Primates in 21st century ecosystems: does primate conservation promote ecosystem conservation?

Contributors to this issue of the American Journal of Primatology were among the participants in an invited symposium at the 2008 Association for Tropical Biology and Conservation meeting in Paramaribo, Suriname. They were asked to assess how essential primates are to tropical ecosystems and, given their research interests, discuss how primate research contributes to the broader understanding about how ecosystems function. This introduction to the issue is divided into three parts: a review of the roles that nonhuman primates play in tropical ecosystems; the implementation of large-scale landscape methods used to identify primate densities; and concerns about the increasingly porous boundaries between humans, nonhuman primates, and pathogens. Although 20th century primate research created a rich database on individual species, including both theoretical and descriptive approaches, the dual effects of high human population densities and widespread habitat destruction should warn us that creative, interdisciplinary and human-related research is needed to solve 21st century problems.

Mast fruiting is a frequent strategy in woody species of eastern South America.

BACKGROUND: It is thought that mast seeding is a rare reproductive strategy in the tropics, since tropical climates are less variable, and fruit consumers tend to be more generalist in these regions. However, previous tests of this hypothesis were based on only few tropical datasets, and none from tropical South America. Moreover, reproductive strategies have been quantified based on the coefficient of variation of interannual seed production, an index that potentially confounds masting and high interannual variability in seed production. METHODOLOGY/PRINCIPAL FINDINGS: We developed a new approach to model the monthly variability in seed production for 28 tree species, and 20 liana species monitored during 5 years in a tropical forest of Central French Guiana. We found that 23% of the species showed a masting pattern, 54% an annual fruiting pattern, and 23% an irregular fruiting pattern. The majority of masting species were trees (8 out of 11), most of them animal-dispersed. The classification into reproductive strategies based on the coefficient of variation was inconsistent with our results in nearly half of the cases. CONCLUSIONS/SIGNIFICANCE: Our study is the first to clearly evidence the frequency of the masting strategy in a tropical forest community of Eastern South America. The commonness of the masting strategy in tropical plants may promote species coexistence through storage dynamics.

Hunting increases dispersal limitation in the tree Carapa procera, a nontimber forest product.

The sustainability of seed extraction from natural populations has been questioned recently. Increased recruitment failure under intense seed harvesting suggests that seed extraction intensifies source limitation. Nevertheless, areas where more seeds are collected tend to also have more intense hunting of seed-dispersing animals. We studied whether such hunting, by limiting disperser activity, could cause quantitative dispersal limitation, especially for large crops and for crops in years of high seed abundance. In each of four Carapa procera (Meliaceae) populations in French Guiana and Surinam, two with hunting and two without, we compared seed fate for individual trees varying in crop size in years of high and low population-level seed abundance. Carapa seeds are a nontimber forest product and depend on dispersal by scatter-hoarding rodents for survival and seedling establishment. Hunting negatively affected the proportion of seeds dispersed and caused greater numbers of seeds to germinate or be infested by moths below parent trees, where they would likely die. Hunting of seed-dispersing animals disproportionally affected large seed crops, but we found no additional effect of population-level seed abundance on dispersal rates. Consistently lower rates of seed dispersal, especially for large seed crops, may translate to lower levels of seedling recruitment under hunting. Our results therefore suggest that the subsistence hunting that usually accompanies seed collection is at the cost of seed dispersal and may contribute to recruitment failure of these nontimber forest products. Seed extraction from natural populations may affect seedling recruitment less if accompanied by measures adequately incorporating and protecting seed dispersers.

Seed size, seedling morphology, and response to deep shade and damage in neotropical rain forest trees.

To investigate the existence of coordinated sets of seedling traits adapted to contrasting establishment conditions, we examined evolutionary convergence in seedling traits for 299 French Guianan woody plant species and the stress response in a shadehouse of species representing seed size gradients within five major cotyledon morphology types. The French Guianan woody plant community has larger seeds than other tropical forest communities and the largest proportion of hypogeal cotyledon type (59.2%) reported for tropical forests. Yet the community includes many species with intermediate size seeds that produce seedlings with different cotyledonal morphologies. A split-plot factorial design with two light levels (0.8% and 16.1% PAR) and four damage treatments (control, seed damage, leaf damage, stem damage) was used in the shadehouse experiment. Although larger-seeded species had higher survival and slower growth, these patterns were better explained by cotyledon type than by seed mass. Even larger-seeded species with foliar cotyledons grew faster than species with reserve-type cotyledons, and survival after stem grazing was five times higher in seedlings with hypogeal cotyledons than with epigeal cotyledons. Thus, to predict seedling performance using seed size, seedling morphology must also be considered.

Causes and consequences of a tropical forest gold rush in the Guiana Shield, South America.

Statistical and spatial analyses of both historical time series and remotely sensed data show a link between the spatial distribution and growth of gold production across the Guiana Shield in northeast Amazonia. Results indicate that an exponential rise in production across an expanding area is primarily a delayed response to the 1971-1978 market flotation of international gold prices. The subsequent 10-fold (2-fold) average nominal (real) price increase has provided a compelling economic incentive to mass exploitation of lower-grade gold deposits. The ground-based and remotely sensed distributions of mining activity are strongly attached to these deposits that dominate the region's gold geology. The presence of these gold-bearing formations in conservation and sustainable timber zones has sparked social conflict and environmental degradation across the region. Left unmanaged, more than a quarter-million square-kilometer area of tropical forest zoned for protection and sustainable management could ultimately be compromised by the price-driven boom in gold mining through poorly integrated resource use planning, lack of reclamation effort, and control of illegal operations. Serious public health issues propagated through the unregulated mining environment further erode the financial benefits achieved through gold extraction. This study demonstrates in part how international economic policies successfully stabilizing more conspicuous centers of the global economy can have unintended but profound environmental and social impacts on remote commodity frontiers.

Post-dispersal predation and scatterhoarding of Dipteryx panamensis (Papilionaceae) seeds by rodents in Panama.

In tropical rain forests of Central America, the canopy tree Dipteryx panamensis (Papilionaceae) fruits when overall fruit biomass is low for mammals. Flying and arboreal consumers feed on D. panamensis and drop seeds under the parent or disperse them farther away. Seeds on the ground attract many vertebrate seed-eaters, some of them potential secondary seed dispersers. The fate of seeds artificially distributed to simulate bat dispersal was studied in relation to fruitfall periodicity and the visiting frequency of diurnal rodents at Barro Colorado Island (BCI), Panama. The frequency of visits by agoutis is very high at the beginning of fruitfall, but in the area close (<50 m) to fruiting trees (Dipteryx-rich area) it declines throughout fruiting, whereas it remains unchanged farther (>50 m) away (Dipteryx-poor and Gustavia-rich area). Squirrels were usually observed in the Dipteryx-rich area. Along with intense post-dispersal seed predation by rodents in the Dipteryx-rich area, a significant proportion of seeds were cached by rodents in the Dipteryx-poor area. Post-dispersal seed predation rate was inversely related to hoarding rate. A significantly greater proportion of seeds was cached in March, especially more than 100 m from the nearest fruiting tree. This correlates with the mid-fruiting period, i.e. during the height of D. panamensis fruiting, when rodents seem to be temporarily satiated with the food supply at parent trees. Hoarding remained high toward April, i.e. late in the fruiting season of D. panamensis. Low survival of scatterhoarded seeds suggests that the alternative food supply over the animal's home-ranges in May-June 1990 was too low to promote survival of cached seeds. Seedlings are assumed to establish in the less-used area of the rodents' home-range when overall food supply is sufficient to satiate post-dispersal predators.

Comparative recruitment patterns of two non-pioneer canopy tree species in French Guiana.

A comparative study was conducted on the recruitment patterns of two non-pioneer tree species, one dispersed by arboreal mammals and birds (Virola michelii, Myristicaceae) and the other by rodents (Moronobea coccinea, Clusiaceae). These species differ in fruiting phenology, seed size, dispersal distance, germination time and seed nutrient exhaustion. In both species, establishment patterns were consistent with the escape hypothesis and the Janzen-Connell model. Virola seeds need not be buried to survive and germinate, and may produce a seedling carpet beneath the parent. Moronobea seedlings only establish from seeds buried by scatterhoarding rodents in the surrounding understory. One-year survival of Virola seedlings was 47.8% and was greater >10 m than < 10 m from the largest parent tree. In contrast, survival of Moronobea seedlings was 56% 3 years after seed dispersal. Survival of juveniles was greater in gaps than in the understory for Virola but not for Moronobea. Moronobea survival was greater than Virola survival in both microhabitats. Both species establish in the understory, yet both grew faster in gaps. Virola appeared to be more gap-dependent than Moronobea which may persist several years in the understory until a gap occurs. Virola and Moronobea illustrate two intermediate recruitment patterns along an hypothetical continuum of nonpioneer species replacement (Bazzaz and Pickett 1980; Swaine and Whitmore 1988).