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

Asian elephants as ecological filters in Sundaic forests

Megaherbivores exert strong top-down influence on the ecosystems they inhabit, yet little is known about the foraging impacts of Asian elephants (Elephas maximus) on the structure of Southeast Asia’s rainforests. Our goal was to document Asian elephants’ dietary composition, selectivity, and foraging impacts in a Sundaic rainforest and test whether these differed between habitats. We conducted controlled direct observations of five wild-born captive elephants feeding on six plant types (bamboo, grass, monocot herbs, palms, lianas, and trees) of different age 2 in two habitats (mature vs. early successional forest) in Krau, Peninsular Malaysia. Palms, trees, and lianas formed the bulk of the elephants’ diet. In the mature forest, elephants showed a strong preference for monocots (preference ratio, PR = 5.1), particularly large palms (PR = 5.4), while trees were negatively selected (PR = 0.14). Conversely, in early successional habitats, large tree saplings were positively selected (PR = 1.6). Elephants uprooted (30%) and broke the main stem (30%) of the dicot trees, mainly large saplings, that they handled. Tree saplings broken by elephants had an average diameter of 1.7 ± 1.1 cm (up to 7 cm), with breaks happening at 1.1 ± 0.5 m of height. We estimated that, in a year, an elephant could damage (i.e., either uproot or break) around 39,000 tree saplings if it fed entirely in mature forest, and almost double the number (73,000) if it fed solely in early successional habitats. Assuming a density of 0.05–0.18 elephants/km2, elephant foraging could damage 0.2–0.6% of the tree sapling population per year. Slow growth rates of understory plants in mature forests could result in negative feedbacks, whereby elephants suppress palms, other monocots, and highly preferred tree species. Alternatively, elephants may initiate positive feedbacks by impeding succession along forest edges and in semi-open environments, thereby increasing the size of gaps and the availability of their preferred foodplants. Overall, our results show that Asian elephants act as ecological filters by suppressing the plants they prefer in Southeast Asia’s rainforests

Asian elephants as ecological filters in Sundaic forests

Megaherbivores exert strong top-down influence on the ecosystems they inhabit, yet little is known about the foraging impacts of Asian elephants (Elephas maximus) on the structure of Southeast Asia’s rainforests. Our goal was to document Asian elephants’ dietary composition, selectivity, and foraging impacts in a Sundaic rainforest and test whether these differed between habitats. We conducted controlled direct observations of five wild-born captive elephants feeding on six plant types (bamboo, grass, monocot herbs, palms, lianas, and trees) of different age 2 in two habitats (mature vs. early successional forest) in Krau, Peninsular Malaysia. Palms, trees, and lianas formed the bulk of the elephants’ diet. In the mature forest, elephants showed a strong preference for monocots (preference ratio, PR = 5.1), particularly large palms (PR = 5.4), while trees were negatively selected (PR = 0.14). Conversely, in early successional habitats, large tree saplings were positively selected (PR = 1.6). Elephants uprooted (30%) and broke the main stem (30%) of the dicot trees, mainly large saplings, that they handled. Tree saplings broken by elephants had an average diameter of 1.7 ± 1.1 cm (up to 7 cm), with breaks happening at 1.1 ± 0.5 m of height. We estimated that, in a year, an elephant could damage (i.e., either uproot or break) around 39,000 tree saplings if it fed entirely in mature forest, and almost double the number (73,000) if it fed solely in early successional habitats. Assuming a density of 0.05–0.18 elephants/km2, elephant foraging could damage 0.2–0.6% of the tree sapling population per year. Slow growth rates of understory plants in mature forests could result in negative feedbacks, whereby elephants suppress palms, other monocots, and highly preferred tree species. Alternatively, elephants may initiate positive feedbacks by impeding succession along forest edges and in semi-open environments, thereby increasing the size of gaps and the availability of their preferred foodplants. Overall, our results show that Asian elephants act as ecological filters by suppressing the plants they prefer in Southeast Asia’s rainforests

The functional response of a generalist predator

Peer reviewedPublisher PD

Rarity of monodominance in hyperdiverse Amazonian forests.

Tropical forests are known for their high diversity. Yet, forest patches do occur in the tropics where a single tree species is dominant. Such "monodominant" forests are known from all of the main tropical regions. For Amazonia, we sampled the occurrence of monodominance in a massive, basin-wide database of forest-inventory plots from the Amazon Tree Diversity Network (ATDN). Utilizing a simple defining metric of at least half of the trees ≥ 10 cm diameter belonging to one species, we found only a few occurrences of monodominance in Amazonia, and the phenomenon was not significantly linked to previously hypothesized life history traits such wood density, seed mass, ectomycorrhizal associations, or Rhizobium nodulation. In our analysis, coppicing (the formation of sprouts at the base of the tree or on roots) was the only trait significantly linked to monodominance. While at specific locales coppicing or ectomycorrhizal associations may confer a considerable advantage to a tree species and lead to its monodominance, very few species have these traits. Mining of the ATDN dataset suggests that monodominance is quite rare in Amazonia, and may be linked primarily to edaphic factors

Saving the world’s terrestrial megafauna

From the late Pleistocene to the Holocene, and now the so called Anthropocene, humans have been driving an ongoing series of species declines and extinctions (Dirzo et al. 2014). Large-bodied mammals are typically at a higher risk of extinction than smaller ones (Cardillo et al. 2005). However, in some circumstances terrestrial megafauna populations have been able to recover some of their lost numbers due to strong conservation and political commitment, and human cultural changes (Chapron et al. 2014). Indeed many would be in considerably worse predicaments in the absence of conservation action (Hoffmann et al. 2015). Nevertheless, most mammalian megafauna face dramatic range contractions and population declines. In fact, 59% of the world’s largest carnivores (≥ 15 kg, n = 27) and 60% of the world’s largest herbivores (≥ 100 kg, n = 74) are classified as threatened with extinction on the International Union for the Conservation of Nature (IUCN) Red List (supplemental table S1 and S2). This situation is particularly dire in sub-Saharan Africa and Southeast Asia, home to the greatest diversity of extant megafauna (figure 1). Species at risk of extinction include some of the world’s most iconic animals—such as gorillas, rhinos, and big cats (figure 2 top row)—and, unfortunately, they are vanishing just as science is discovering their essential ecological roles (Estes et al. 2011). Here, our objectives are to raise awareness of how these megafauna are imperiled (species in supplemental table S1 and S2) and to stimulate broad interest in developing specific recommendations and concerted action to conserve them

Consistent, small effects of treefall disturbances on the composition and diversity of four Amazonian forests

Summary 1. Understanding the resilience of moist tropical forests to treefall disturbance events is important for understanding the mechanisms that underlie species coexistence and for predicting the future composition of these ecosystems. Here, we test whether variation in the functional composition of Amazonian forests determines their resilience to disturbance. 2. We studied the legacy of natural treefall disturbance events in four forests across Amazonia that differ substantially in functional composition. We compared the composition and diversity of all free-standing woody stems 2-10 cm diameter in previously disturbed and undisturbed 20 9 20 m subplots within 55, one-hectare, long-term forest inventory plots. 3. Overall, stem number increased following disturbance, and species and functional composition shifted to favour light-wooded, small-seeded taxa. Alpha-diversity increased, but beta-diversity was unaffected by disturbance, in all four forests. 4. Changes in response to disturbance in both functional composition and alpha-diversity were, however, small (2 -4% depending on the parameter) and similar among forests. 5. Synthesis. This study demonstrates that variation in the functional composition of Amazonian forests does not lead to large differences in the response of these forests to treefall disturbances, and overall, these events have a minor role in maintaining the diversity of these ecosystems

Hyperdominance in Amazonian Forest Carbon Cycling

While Amazonian forests are extraordinarily diverse, the abundance of trees is skewed strongly towards relatively few ‘hyperdominant’ species. In addition to their diversity, Amazonian trees are a key component of the global carbon cycle, assimilating and storing more carbon than any other ecosystem on Earth. Here we ask, using a unique data set of 530 forest plots, if the functions of storing and producing woody carbon are concentrated in a small number of tree species, whether the most abundant species also dominate carbon cycling, and whether dominant species are characterized by specific functional traits. We find that dominance of forest function is even more concentrated in a few species than is dominance of tree abundance, with only ≈1% of Amazon tree species responsible for 50% of carbon storage and productivity. Although those species that contribute most to biomass and productivity are often abundant, species maximum size is also influential, while the identity and ranking of dominant species varies by function and by region

Variation in stem mortality rates determines patterns of above-ground biomass in Amazonian forests: implications for dynamic global vegetation models

This is the final version of the article. Available from Wiley via the DOI in this record.Understanding the processes that determine above-ground biomass (AGB) in Amazonian forests is important for predicting the sensitivity of these ecosystems to environmental change and for designing and evaluating dynamic global vegetation models (DGVMs). AGB is determined by inputs from woody productivity [woody net primary productivity (NPP)] and the rate at which carbon is lost through tree mortality. Here, we test whether two direct metrics of tree mortality (the absolute rate of woody biomass loss and the rate of stem mortality) and/or woody NPP, control variation in AGB among 167 plots in intact forest across Amazonia. We then compare these relationships and the observed variation in AGB and woody NPP with the predictions of four DGVMs. The observations show that stem mortality rates, rather than absolute rates of woody biomass loss, are the most important predictor of AGB, which is consistent with the importance of stand size structure for determining spatial variation in AGB. The relationship between stem mortality rates and AGB varies among different regions of Amazonia, indicating that variation in wood density and height/diameter relationships also influences AGB. In contrast to previous findings, we find that woody NPP is not correlated with stem mortality rates and is weakly positively correlated with AGB. Across the four models, basin-wide average AGB is similar to the mean of the observations. However, the models consistently overestimate woody NPP and poorly represent the spatial patterns of both AGB and woody NPP estimated using plot data. In marked contrast to the observations, DGVMs typically show strong positive relationships between woody NPP and AGB. Resolving these differences will require incorporating forest size structure, mechanistic models of stem mortality and variation in functional composition in DGVMs.This paper is a product of the European Union's Seventh Framework Programme AMAZALERT project (282664). The field data used in this study have been generated by the RAINFOR network, which has been supported by a Gordon and Betty Moore Foundation grant, the European Union's Seventh Framework Programme projects 283080, ‘GEOCARBON’; and 282664, ‘AMAZALERT’; ERC grant ‘Tropical Forests in the Changing Earth System’), and Natural Environment Research Council (NERC) Urgency, Consortium and Standard Grants ‘AMAZONICA’ (NE/F005806/1), ‘TROBIT’ (NE/D005590/1) and ‘Niche Evolution of South American Trees’ (NE/I028122/1). Additional data were included from the Tropical Ecology Assessment and Monitoring (TEAM) Network – a collaboration between Conservation International, the Missouri Botanical Garden, the Smithsonian Institution and the Wildlife Conservation Society, and partly funded by these institutions, the Gordon and Betty Moore Foundation, and other donors. Fieldwork was also partially supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico of Brazil (CNPq), project Programa de Pesquisas Ecológicas de Longa Duração (PELD-403725/2012-7). A.R. acknowledges funding from the Helmholtz Alliance ‘Remote Sensing and Earth System Dynamics’; L.P., M.P.C. E.A. and M.T. are partially funded by the EU FP7 project ‘ROBIN’ (283093), with co-funding for E.A. from the Dutch Ministry of Economic Affairs (KB-14-003-030); B.C. [was supported in part by the US DOE (BER) NGEE-Tropics project (subcontract to LANL). O.L.P. is supported by an ERC Advanced Grant and is a Royal Society-Wolfson Research Merit Award holder. P.M. acknowledges support from ARC grant FT110100457 and NERC grants NE/J011002/1, and T.R.B. acknowledges support from a Leverhulme Trust Research Fellowship

Geographic patterns of tree dispersal modes in Amazonia and their ecological correlates

Unidad de excelencia María de Maeztu CEX2019-000940-MAim: To investigate the geographic patterns and ecological correlates in the geographic distribution of the most common tree dispersal modes in Amazonia (endozoochory, synzoochory, anemochory and hydrochory). We examined if the proportional abundance of these dispersal modes could be explained by the availability of dispersal agents (disperser-availability hypothesis) and/or the availability of resources for constructing zoochorous fruits (resource-availability hypothesis). Time period: Tree-inventory plots established between 1934 and 2019. Major taxa studied: Trees with a diameter at breast height (DBH) ≥ 9.55 cm. Location: Amazonia, here defined as the lowland rain forests of the Amazon River basin and the Guiana Shield. Methods: We assigned dispersal modes to a total of 5433 species and morphospecies within 1877 tree-inventory plots across terra-firme, seasonally flooded, and permanently flooded forests. We investigated geographic patterns in the proportional abundance of dispersal modes. We performed an abundance-weighted mean pairwise distance (MPD) test and fit generalized linear models (GLMs) to explain the geographic distribution of dispersal modes. Results: Anemochory was significantly, positively associated with mean annual wind speed, and hydrochory was significantly higher in flooded forests. Dispersal modes did not consistently show significant associations with the availability of resources for constructing zoochorous fruits. A lower dissimilarity in dispersal modes, resulting from a higher dominance of endozoochory, occurred in terra-firme forests (excluding podzols) compared to flooded forests. Main conclusions: The disperser-availability hypothesis was well supported for abiotic dispersal modes (anemochory and hydrochory). The availability of resources for constructing zoochorous fruits seems an unlikely explanation for the distribution of dispersal modes in Amazonia. The association between frugivores and the proportional abundance of zoochory requires further research, as tree recruitment not only depends on dispersal vectors but also on conditions that favour or limit seedling recruitment across forest types