The structure and organisation of an Amazonian bird community remains little changed after nearly four decades in Manu National Park.

Documenting patterns of spatiotemporal change in hyper-diverse communities remains a challenge for tropical ecology yet is increasingly urgent as some long-term studies have shown major declines in bird communities in undisturbed sites. In 1982, Terborgh et al. quantified the structure and organisation of the bird community in a 97-ha. plot in southeastern Peru. We revisited the same plot in 2018 using the same methodologies as the original study to evaluate community-wide changes. Contrary to longitudinal studies of other neotropical bird communities (Tiputini, Manaus, and Panama), we found little change in community structure and organisation, with increases in 5, decreases in 2 and no change in 7 foraging guilds. This apparent stability suggests that large forest reserves such as the Manu National Park, possibly due to regional topographical influences on precipitation, still provide the conditions for establishing refugia from at least some of the effects of global change on bird communities.

Disappearance of an ecosystem engineer, the white-lipped peccary (Tayassu pecari), leads to density compensation and ecological release.

Given the rate of biodiversity loss, there is an urgent need to understand community-level responses to extirpation events, with two prevailing hypotheses. On one hand, the loss of an apex predator leads to an increase in primary prey species, triggering a trophic cascade of other changes within the community, while density compensation and ecological release can occur because of reduced competition for resources and absence of direct aggression. White-lipped peccary (Tayassu pecari-WLP), a species that typically co-occurs with collared peccary (Pecari tajacu), undergo major population crashes-often taking 20 to 30-years for populations to recover. Using a temporally replicated camera trapping dataset, in both a pre- and post- WLP crash, we explore how WLP disappearance alters the structure of a Neotropical vertebrate community with findings indicative of density compensation. White-lipped peccary were the most frequently detected terrestrial mammal in the 2006-2007 pre-population crash period but were undetected during the 2019 post-crash survey. Panthera onca (jaguar) camera trap encounter rates declined by 63% following the WLP crash, while collared peccary, puma (Puma concolor), red-brocket deer (Mazama americana) and short-eared dog (Atelocynus microtis) all displayed greater encounter rates (490%, 150%, 280%, and 500% respectively), and increased in rank-abundance. Absence of WLP was correlated with ecological release changes in habitat-use for six species, with the greatest increase in use in the preferred floodplain habitat of the WLP. Surprisingly, community-weighted mean trait distributions (body size, feeding guild and nocturnality) did not change, suggesting functional redundancy in diverse tropical mammal assemblages.

Tropical forests can maintain hyperdiversity because of enemies.

Explaining the maintenance of tropical forest diversity under the countervailing forces of drift and competition poses a major challenge to ecological theory. Janzen-Connell effects, in which host-specific natural enemies restrict the recruitment of juveniles near conspecific adults, provide a potential mechanism. Janzen-Connell is strongly supported empirically, but existing theory does not address the stable coexistence of hundreds of species. Here we use high-performance computing and analytical models to demonstrate that tropical forest diversity can be maintained nearly indefinitely in a prolonged state of transient dynamics due to distance-responsive natural enemies. Further, we show that Janzen-Connell effects lead to community regulation of diversity by imposing a diversity-dependent cost to commonness and benefit to rarity. The resulting species-area and rank-abundance relationships are consistent with empirical results. Diversity maintenance over long time spans does not require dispersal from an external metacommunity, speciation, or resource niche partitioning, only a small zone around conspecific adults in which saplings fail to recruit. We conclude that the Janzen-Connell mechanism can explain the maintenance of tropical tree diversity while not precluding the operation of other niche-based mechanisms such as resource partitioning.

Megafauna and ecosystem function from the Pleistocene to the Anthropocene.

Large herbivores and carnivores (the megafauna) have been in a state of decline and extinction since the Late Pleistocene, both on land and more recently in the oceans. Much has been written on the timing and causes of these declines, but only recently has scientific attention focused on the consequences of these declines for ecosystem function. Here, we review progress in our understanding of how megafauna affect ecosystem physical and trophic structure, species composition, biogeochemistry, and climate, drawing on special features of PNAS and Ecography that have been published as a result of an international workshop on this topic held in Oxford in 2014. Insights emerging from this work have consequences for our understanding of changes in biosphere function since the Late Pleistocene and of the functioning of contemporary ecosystems, as well as offering a rationale and framework for scientifically informed restoration of megafaunal function where possible and appropriate.

Science for a wilder Anthropocene: Synthesis and future directions for trophic rewilding research.

Trophic rewilding is an ecological restoration strategy that uses species introductions to restore top-down trophic interactions and associated trophic cascades to promote self-regulating biodiverse ecosystems. Given the importance of large animals in trophic cascades and their widespread losses and resulting trophic downgrading, it often focuses on restoring functional megafaunas. Trophic rewilding is increasingly being implemented for conservation, but remains controversial. Here, we provide a synthesis of its current scientific basis, highlighting trophic cascades as the key conceptual framework, discussing the main lessons learned from ongoing rewilding projects, systematically reviewing the current literature, and highlighting unintentional rewilding and spontaneous wildlife comebacks as underused sources of information. Together, these lines of evidence show that trophic cascades may be restored via species reintroductions and ecological replacements. It is clear, however, that megafauna effects may be affected by poorly understood trophic complexity effects and interactions with landscape settings, human activities, and other factors. Unfortunately, empirical research on trophic rewilding is still rare, fragmented, and geographically biased, with the literature dominated by essays and opinion pieces. We highlight the need for applied programs to include hypothesis testing and science-based monitoring, and outline priorities for future research, notably assessing the role of trophic complexity, interplay with landscape settings, land use, and climate change, as well as developing the global scope for rewilding and tools to optimize benefits and reduce human-wildlife conflicts. Finally, we recommend developing a decision framework for species selection, building on functional and phylogenetic information and with attention to the potential contribution from synthetic biology.

Toward a trophic theory of species diversity.

Efforts to understand the ecological regulation of species diversity via bottom-up approaches have failed to yield a consensus theory. Theories based on the alternative of top-down regulation have fared better. Paine's discovery of keystone predation demonstrated that the regulation of diversity via top-down forcing could be simple, strong, and direct, yet ecologists have persistently failed to perceive generality in Paine's result. Removing top predators destabilizes many systems and drives transitions to radically distinct alternative states. These transitions typically involve community reorganization and loss of diversity, implying that top-down forcing is crucial to diversity maintenance. Contrary to the expectations of bottom-up theories, many terrestrial herbivores and mesopredators are capable of sustained order-of-magnitude population increases following release from predation, negating the assumption that populations of primary consumers are resource limited and at or near carrying capacity. Predation sensu lato (to include Janzen-Connell mortality agents) has been shown to promote diversity in a wide range of ecosystems, including rocky intertidal shelves, coral reefs, the nearshore ocean, streams, lakes, temperate and tropical forests, and arctic tundra. The compelling variety of these ecosystems suggests that top-down forcing plays a universal role in regulating diversity. This conclusion is further supported by studies showing that the reduction or absence of predation leads to diversity loss and, in the more dramatic cases, to catastrophic regime change. Here, I expand on the thesis that diversity is maintained by the interaction between predation and competition, such that strong top-down forcing reduces competition, allowing coexistence.

Gaps contribute tree diversity to a tropical floodplain forest.

Treefall gaps have long been a central feature of discussions about the maintenance of tree diversity in both temperate and tropical forests. Gaps expose parts of the forest floor to direct sunlight and create a distinctive microenvironment that can favor the recruitment into the community of so-called gap pioneers. This traditional view enjoys strong empirical support, yet has been cast into doubt by a much-cited article claiming that gaps are inherently "neutral" in their contribution to forest dynamics. We present concurrent data on seedfall and sapling recruitment into gaps vs. under a vertically structured canopy in an Amazonian floodplain forest in Peru. Our results strongly uphold the view of gaps as important generators of tree diversity. Our methods differed significantly from those employed by the neutralist group and can explain the contrasting outcomes. We found that seedfall into gaps differs both quantitatively and qualitatively from that falling under a multi-tiered canopy, being greatly enriched in wind-dispersed and autochorus species and sharply deficient in all types of zoochorous seeds. Despite a reduced input of zoochorous seeds, zoochorous species made up 79% of saplings recruiting into gaps, whereas wind-dispersed species made up only 1%. Cohorts of saplings recruiting into gaps are less diverse than those recruiting under a closed canopy (Fisher's alpha = 40 vs. 100) and compositionally distinct, containing many light-demanding species that rarely, if ever, recruit under shaded conditions. Saplings recruiting into gaps appear to represent a variable mix of shade-tolerant survivors of the initiating treefall and sun-demanding species that germinate subsequently.

How mammalian predation contributes to tropical tree community structure.

The recruitment of seedlings from seeds is the key demographic transition for rain forest trees. Though tropical forest mammals are known to consume many seeds, their effects on tree community structure remain little known. To evaluate their effects, we monitored 8,000 seeds of 24 tree species using exclosure cages that were selectively permeable to three size classes of mammals for up to 4.4 years. Small and medium-bodied mammals removed many more seeds than did large mammals, and they alone generated beta diversity and negative density dependence, whereas all mammals reduced diversity and shaped local species composition. Thus, small and medium-bodied mammals more strongly contributed to community structure and promoted species coexistence than did large mammals. Given that seedling recruitment is seed limited for most species, alterations to the composition of the community of mammalian seed predators is expected to have long-term consequences for tree community structure in tropical forests.

A keystone ecologist: Robert Treat Paine, 1933-2016.

Robert T. Paine, who passed away on 13 June 2016, is among the most influential people in the history of ecology. Paine was an experimentalist, a theoretician, a practitioner, and proponent of the "ecology of place," and a deep believer in the importance of natural history to ecological understanding. His scientific legacy grew from the discovery of a link between top-down forcing and species diversity, a breakthrough that led to the ideas of both keystone species and trophic cascades, and to our early understanding of the mosaic nature of biological communities, causes of zonation across physical gradients, and the intermediate-disturbance hypothesis of species diversity. Paine's influence as a mentor was equally important to the growth of ecological thinking, natural resource conservation, and policy. He served ecology as an Ecological Society of America president, an editor of the Society's journals, a member of and contributor to the National Academy of Sciences and the National Research Council, and an in-demand advisor to various state and federal agencies. Paine's broad interests, enthusiasm, charisma, and humor deeply affected our lives and the lives of so many others.

Historical effects on beta diversity and community assembly in Amazonian trees.

We present a unique perspective on the role of historical processes in community assembly by synthesizing analyses of species turnover among communities with environmental data and independent, population genetic-derived estimates of among-community dispersal. We sampled floodplain and terra firme communities of the diverse tree genus Inga (Fabaceae) across a 250-km transect in Amazonian Peru and found patterns of distance-decay in compositional similarity in both habitat types. However, conventional analyses of distance-decay masked a zone of increased species turnover present in the middle of the transect. We estimated past seed dispersal among the same communities by examining geographic plastid DNA variation for eight widespread Inga species and uncovered a population genetic break in the majority of species that is geographically coincident with the zone of increased species turnover. Analyses of these and 12 additional Inga species shared between two communities located on opposite sides of the zone showed that the populations experienced divergence 42,000-612,000 y ago. Our results suggest that the observed distance decay is the result not of environmental gradients or dispersal limitation coupled with ecological drift--as conventionally interpreted under neutral ecological theory--but rather of secondary contact between historically separated communities. Thus, even at this small spatial scale, historical processes seem to significantly impact species' distributions and community assembly. Other documented zones of increased species turnover found in the western Amazon basin or elsewhere may be related to similar historical processes.

How many seeds does it take to make a sapling?

Tall canopy trees produce many more seeds than do understory treelets, yet, on average, both classes of trees achieve the same lifetime fitness. Using concurrent data on seedfall (8 years) and sapling recruitment (12 years) from a long-established tree plot at the Cocha Cashu Biological Station in Peru, we show that a 40-m canopy tree must produce roughly 13 times the mass of seeds to generate a sapling as a 5-m understory treelet. Mature tree height accounted for 41% of the variance in seed mass per sapling recruit in a simple univariate regression, whereas a multivariate model that included both intrinsic (seed mass, tree height, and dispersal mode) and extrinsic factors (sapling mortality as a surrogate for microsite quality) explained only 31% of the variance in number of seeds per sapling recruit. The multivariate model accounted for less variance because tall trees produce heavier seeds, on average, than treelets. We used "intact" (mostly dispersed) seeds to parameterize the response variable so as to reduce, if not eliminate, any contribution of conspecific crowding to the difference in reproductive efficiency between canopy trees and treelets. Accordingly, a test for negative density dependence failed to expose a relationship between density of reproductive trees in the population and reproductive efficiency (seed mass per recruit). We conclude that understory treelets, some of which produce only a dozen seeds a year, gain their per-seed advantage by failing to attract enemies à la Janzen-Connell, either in ecological or evolutionary time.

One sixth of Amazonian tree diversity is dependent on river floodplains.

Amazonia's floodplain system is the largest and most biodiverse on Earth. Although forests are crucial to the ecological integrity of floodplains, our understanding of their species composition and how this may differ from surrounding forest types is still far too limited, particularly as changing inundation regimes begin to reshape floodplain tree communities and the critical ecosystem functions they underpin. Here we address this gap by taking a spatially explicit look at Amazonia-wide patterns of tree-species turnover and ecological specialization of the region's floodplain forests. We show that the majority of Amazonian tree species can inhabit floodplains, and about a sixth of Amazonian tree diversity is ecologically specialized on floodplains. The degree of specialization in floodplain communities is driven by regional flood patterns, with the most compositionally differentiated floodplain forests located centrally within the fluvial network and contingent on the most extraordinary flood magnitudes regionally. Our results provide a spatially explicit view of ecological specialization of floodplain forest communities and expose the need for whole-basin hydrological integrity to protect the Amazon's tree diversity and its function.

Multiscale phenological niches of seed fall in diverse Amazonian plant communities.

Phenology has long been hypothesized as an avenue for niche partitioning or interspecific facilitation, both promoting species coexistence. Tropical plant communities exhibit striking diversity in reproductive phenology, but many are also noted for large synchronous reproductive events. Here we study whether the phenology of seed fall in such communities is nonrandom, the temporal scales of phenological patterns, and ecological factors that drive reproductive phenology. We applied multivariate wavelet analysis to test for phenological synchrony versus compensatory dynamics (i.e., antisynchronous patterns where one species' decline is compensated by the rise of another) among species and across temporal scales. We used data from long-term seed rain monitoring of hyperdiverse plant communities in the western Amazon. We found significant synchronous whole-community phenology at multiple timescales, consistent with shared environmental responses or positive interactions among species. We also observed both compensatory and synchronous phenology within groups of species (confamilials) likely to share traits and seed dispersal mechanisms. Wind-dispersed species exhibited significant synchrony at ~6-month scales, suggesting these species might share phenological niches to match the seasonality of wind. Our results suggest that community phenology is shaped by shared environmental responses but that the diversity of tropical plant phenology may partly result from temporal niche partitioning. The scale-specificity and time-localized nature of community phenology patterns highlights the importance of multiple and shifting drivers of phenology.

Mapping density, diversity and species-richness of the Amazon tree flora.

Using 2.046 botanically-inventoried tree plots across the largest tropical forest on Earth, we mapped tree species-diversity and tree species-richness at 0.1-degree resolution, and investigated drivers for diversity and richness. Using only location, stratified by forest type, as predictor, our spatial model, to the best of our knowledge, provides the most accurate map of tree diversity in Amazonia to date, explaining approximately 70% of the tree diversity and species-richness. Large soil-forest combinations determine a significant percentage of the variation in tree species-richness and tree alpha-diversity in Amazonian forest-plots. We suggest that the size and fragmentation of these systems drive their large-scale diversity patterns and hence local diversity. A model not using location but cumulative water deficit, tree density, and temperature seasonality explains 47% of the tree species-richness in the terra-firme forest in Amazonia. Over large areas across Amazonia, residuals of this relationship are small and poorly spatially structured, suggesting that much of the residual variation may be local. The Guyana Shield area has consistently negative residuals, showing that this area has lower tree species-richness than expected by our models. We provide extensive plot meta-data, including tree density, tree alpha-diversity and tree species-richness results and gridded maps at 0.1-degree resolution.

Unraveling Amazon tree community assembly using Maximum Information Entropy: a quantitative analysis of tropical forest ecology.

In a time of rapid global change, the question of what determines patterns in species abundance distribution remains a priority for understanding the complex dynamics of ecosystems. The constrained maximization of information entropy provides a framework for the understanding of such complex systems dynamics by a quantitative analysis of important constraints via predictions using least biased probability distributions. We apply it to over two thousand hectares of Amazonian tree inventories across seven forest types and thirteen functional traits, representing major global axes of plant strategies. Results show that constraints formed by regional relative abundances of genera explain eight times more of local relative abundances than constraints based on directional selection for specific functional traits, although the latter does show clear signals of environmental dependency. These results provide a quantitative insight by inference from large-scale data using cross-disciplinary methods, furthering our understanding of ecological dynamics.

Enemies maintain hyperdiverse tropical forests.

Understanding tropical forest tree diversity has been a major challenge to ecologists. In the absence of compensatory mechanisms, two powerful forces, drift and competition, are expected to erode diversity quickly, especially in communities containing scores or hundreds of rare species. Here, I review evidence bearing on four compensatory mechanisms that have been subsumed under the terms "density dependence" or "negative density dependence": (1) intra- and (2) interspecific competition and the action of (3) density-responsive and (4) distance-responsive biotic agents, as postulated by Janzen and Connell. To achieve ontological integration, I examine evidence based on studies employing seeds, seedlings, and saplings. Available evidence points overwhelmingly to the action of both host-generalist and host-restricted biotic agents as causing most seed and seedling mortality, implying that species diversity is maintained via top-down forcing. The overall effect of most host-generalist seed predators and herbivores is to even out the distribution of surviving propagules. Spatially restricted recruitment appears to result mainly, if not exclusively, from the actions of host-restricted agents, principally microarthropods and fungi, that attack hosts in a distance-dependent fashion as Janzen and Connell proposed. Near total failure of propagules close to reproductive conspecifics ensures that successful reproduction occurs through a scant rain of dispersed seeds. Densities of dispersed seeds and seedlings arising from them are so low as to generally preclude the operation of density dependence, at least during early ontogenetic stages. I conclude that Janzen and Connell were essentially correct and that diversity maintenance results from top-down forcing acting in a spatially nonuniform fashion.

Relationships between species richness and ecosystem services in Amazonian forests strongly influenced by biogeographical strata and forest types.

Despite increasing attention for relationships between species richness and ecosystem services, for tropical forests such relationships are still under discussion. Contradicting relationships have been reported concerning carbon stock, while little is known about relationships concerning timber stock and the abundance of non-timber forest product producing plant species (NTFP abundance). Using 151 1-ha plots, we related tree and arborescent palm species richness to carbon stock, timber stock and NTFP abundance across the Guiana Shield, and using 283 1-ha plots, to carbon stock across all of Amazonia. We analysed how environmental heterogeneity influenced these relationships, assessing differences across and within multiple forest types, biogeographic regions and subregions. Species richness showed significant relationships with all three ecosystem services, but relationships differed between forest types and among biogeographical strata. We found that species richness was positively associated to carbon stock in all biogeographical strata. This association became obscured by variation across biogeographical regions at the scale of Amazonia, resembling a Simpson's paradox. By contrast, species richness was weakly or not significantly related to timber stock and NTFP abundance, suggesting that species richness is not a good predictor for these ecosystem services. Our findings illustrate the importance of environmental stratification in analysing biodiversity-ecosystem services relationships.

Are all seeds equal? Spatially explicit comparisons of seed fall and sapling recruitment in a tropical forest.

Understanding demographic transitions may provide the key to explain the high diversity of tropical tree communities. In a faunally intact Amazonian forest, we compared the spatial distribution of saplings of 15 common tree species with patterns of conspecific seed fall, and examined the seed-to-sapling transition in relation to locations of conspecific trees. In all species, the spatial pattern of sapling recruitment bore no resemblance to predicted distributions based on the density of seed fall. Seed efficiency (the probability of a seed producing a sapling) is strongly correlated with distance from large conspecific trees, with a >30-fold multiplicative increase between recruitment zones that are most distant vs. proximal to conspecific adults. The striking decoupling of sapling recruitment and conspecific seed density patterns indicates near-complete recruitment failure in areas of high seed density located around reproductive adults. Our results provide strong support for the spatially explicit predictions of the Janzen-Connell hypothesis.