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SPECIAL FEATURE: PERSPECTIVE PERSPECTIVE SPECIAL FEATURE: Science for a wilder : Synthesis and future directions for trophic rewilding research Jens-Christian Svenninga,1,2,PilB.M.Pedersena,1, C. Josh Donlanb,c, Rasmus Ejrnæsd, Søren Faurbya,MauroGalettie, Dennis M. Hansenf, Brody Sandela, Christopher J. Sandomg, John W. Terborghh, and Frans W. M. Verai aSection for Ecoinformatics & , Department of Bioscience, Aarhus University, DK-8000 Aarhus C, Denmark; bAdvanced Conservation Strategies, Midway, UT 84049; cDepartment of and Evolutionary Biology, Cornell University, Ithaca, NY 15853; dSection for Biodiversity & Conservation, Department of Bioscience, Aarhus University, DK-8410 Rønde, Denmark; eDepartamento de Ecologia, Universidade Estadual Paulista, 13506-900 Rio Claro, São Paulo, Brazil; fInstitute of Evolutionary Biology and , University of Zurich, 8057 Zurich, Switzerland; gWildlife Conservation Research Unit, Department of Zoology, Oxford University, The Recanati-Kaplan Centre, Oxfordshire OX13 5QL, United Kingdom; hCenter for Tropical Conservation, Nicholas School of the Environment and Earth Sciences, Duke University, Durham, NC 27708; and iCommunity and Conservation Ecology, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Cocon, 9700 CC Groningen, The Netherlands

Edited by Yadvinder Malhi, Oxford University, Oxford, United Kingdom, and accepted by the Editorial Board August 5, 2015 (received for review March 16, 2015)

Trophic rewilding is an ecological restoration strategy that uses introductions to restore top-down trophic interactions and associated trophic cascades to promote self-regulating biodiverse . Given the importance of large in trophic cascades and their widespread losses and resulting trophic downgrading, it often focuses on restoring functional . 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 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, , and , 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. conservation | megafauna | reintroduction | restoration | trophic cascades

Human impacts are so pervasive that a new focused on establishment of core overcoming the massive prehistoric extinc- geological epoch has been proposed: the areas, enhanced connectivity, and restoration tions linked to Homo sapiens’ global expan- Anthropocene (1). The effects on ecosystems of keystone species (9–11). Subsequently, sion (2, 4). The merits of this pre-Homo sa- and biodiversity are one of the biggest chal- rewilding has become an increasingly popular piens baseline relative to more recent ones lenges facing modern society. Large-bodied term, but with varied meanings (12, 13). We have been much discussed (12). A key point animals are particularly affected, with massive here focus on rewilding as trophic rewilding, in its favor is that rich post-Mesozoic mega- prehistoric (2–4) and severe de- defined as species introductions to restore faunas evolved by 40 million y ago (19) and clines in many extant species (5). Over the top-down trophic interactions and associated have been characteristic of Earth’s ecosystems last decades it has become increasingly clear trophic cascades to promote self-regulating until the spread of Homo sapiens (20, 21). that large animals are often important for biodiverse ecosystems. An important alterna- function and biodiversity via tro- tive rewilding concept is passive management Author contributions: J.-C.S., P.B.M.P., and S.F. designed research; phic cascades, the propagation of consumer without any human interference (12, 14, 15). J.-C.S., P.B.M.P., S.F., and D.M.H. performed research; P.B.M.P. and impacts downward through food webs (6, 7). Most or all approaches to rewilding as an S.F. analyzed data; and J.-C.S., P.B.M.P., C.J.D., R.E., S.F., M.G., D.M.H., B.S., C.J.S., J.W.T., and F.W.M.V. wrote the paper. Their widespread losses have led to trophic ecological restoration method involve restor- The authors declare no conflict of interest. downgrading on a global scale, with negative ing natural processes to promote ecosystems – This article is a PNAS Direct Submission. Y.M. is a guest editor effects on ecosystems and biodiversity (6 8). that maintain biodiversity with little or no invited by the Editorial Board. These observations have inspired a new need for ongoing human management. A 1J.-C.S. and P.B.M.P. contributed equally to this work. ecological restoration approach that we here key development for trophic rewilding has 2To whom correspondence should be addressed. Email: svenning@ refer to as “trophic rewilding.” The rewilding been the proposal for “ rewilding,” bios.au.dk. concept was introduced in the late 20th cen- advocated to restore ecosystem function by This article contains supporting information online at www.pnas.org/ tury as a large-scale conservation strategy, rebuilding rich megafaunas (16–18), thereby lookup/suppl/doi:10.1073/pnas.1502556112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1502556112 PNAS Early Edition | 1of7 Hence, most extant species have evolved in rewilding. An increasing body of literature (29–31), including further rare global extinc- megafauna-rich ecosystems and should be documents the existence of trophic cascades, tions (32). On islands, the first phase often adapted to such conditions (22, 23). A further where apex consumers shape ecosystems via occurred in the mid- or late (3). controversial aspect is the proposed use of effects on prey and other resources, as well These losses have had strong ecosystem nonnative species as ecological replacements as competitors, and their multidirectional effects, notably via trophic cascades. The for globally extinct species (24, 25). However, propagation through food webs (6, 27). These initial extinctions affected vegetation, fire this also exemplifies that letting pre-Homo apex consumers are often large-bodied car- regimes, biogeochemical cycling, and possi- sapiens conditions guide rewilding can be nivores and . Trophic cascades bly even climate (33–36), and are linked to done pragmatically. Indeed, it is not only dis- have been truncated by humans, with strong losses among dependent species, such as – cussed and applied in relation to wild lands, effects on ecosystems and often negative scavenging birds and dung beetles (37 40). but also human-occupied landscapes (13, 25, consequences for biodiversity (6, 7). Trophic Later and current megafauna losses have 26), aiming to increase the ability of ecosys- rewilding attempts to remedy this by re- also had strong ecological impacts via, for tems to maintain biodiversity with minimal storing the missing top-down–mediated example, abundance increases in medium- management, but recognizing that some in- processes. We note that these need not all sized herbivores (41), mesopredator release terference may be needed. be strictly trophic, but also include associ- (7), and disperser losses (42). Although We here provide an overview of the ated processes (e.g., nonfeeding related dis- proceeds in most places (5), scientific basis for trophic rewilding, discus- turbances, such as wallows) (28). some regions are recovering: for example, Europe (43, 44). sing theory and practical lessons, providing a Since the expansion of Homo sapiens Large carnivores and herbivores play im- systematic review of the international scien- across the world, megafaunas have un- portant roles in trophic cascades. Although tific literature, and highlighting underused dergone progressive simplification (2, 4), a now rare because of persecution, large car- sources of information. We then outline process that is still ongoing (5). This loss has nivores were ubiquitous until recently (6, 7). research priorities and finally discuss how to had two, sometimes overlapping phases: (i) Large carnivores may control the density and select species for rewilding introductions. severe and early Holocene losses of a broad range of megafauna, often behavior of herbivores and mesopredators Current Scientific Basis for Trophic leading to complete loss of herbivores (7). For example, limit densities of Rewilding ≥1,000 kg (2, 4); (ii) continuing range con- nonmigratory and may do so even more strongly when co-occurring with other large Trophic Cascades. Trophic cascades of- tractions in remaining continental mega- ≥ fer a key theoretical framework for trophic fauna from the mid-Holocene onwards predators (45). Herbivores weighing 1,000 kg (megaherbivores) are thought to be largely immune to adult predation and limited by resources (46, 47). They can have strong A ≥ B ≥ vegetation and ecosystem impacts because of their abundance and sheer size (28, 46). Formerly cosmopolitan, they are now lim- ited to parts of Africa and Asia (Fig. 1). It is possible that predation on their juveniles may have provided greater regulation of their abundances during the Pleistocene (48), al- though stable isotope evidence suggests that megaherbivores rarely formed a major part C D of Pleistocene carnivore diets (49, 50). Intermediate-size (100–999 kg) herbivores are also not always top-down–regulated. For example, in some African savanna ecosys- tems large herbivores >150 kg experience only limited predation and are largely bot- tom-up regulated (47). More generally, herd- forming migratory often escape predation regulation (47, 51). Irrespective of top-down or bottom-up regulation, large EF≥ ≥ herbivores can have pervasive ecosystem ef- fects, impacting primary production, nutrient cycling, disturbance regimes, habitat hetero- geneity, and seed dispersal (28, 42, 52, 53). Pre- megafaunas in large parts of the world were as species-rich as any extant megafauna, with multiple species of megaherbivores and high diversities of intermediate-size herbivores and large car- Fig. 1. Current and estimated present-natural diversity patterns for (A and B) megaherbivores (≥1,000 kg), (C and D)large herbivores (45–999 kg), and (E and F) large carnivores (>21.5 kg). The term “present-natural” refers to the state that a nivores (Fig. 1). The exact functioning of phenomenon would be in today in the complete absence of human influence through time (111). For this mapping, om- trophic cascades in these ecosystems is un- nivores were classified as carnivores when constitutesamajorpartoftheirdietandasherbivoresotherwise. certain (54), although intact current African

2of7 | www.pnas.org/cgi/doi/10.1073/pnas.1502556112 Svenning et al. Controversy exists over the exact role of 3D and SI Appendix, Tables S1 and S2). A PERSPECTIVE wolves in these dynamics (59), but similar majority were positive to reintroduction of SPECIAL FEATURE: effects are reported elsewhere in North species extirpated regionally within the last America (61, 62) and Europe (63). Other 5,000 y (Fig. 3C). Support for reintroducing experiments have focused on large herbi- species extirpated >5,000 y ago or in- vores. The 56-km2 ex- troducing ecological replacements for ex- periment in the Netherlands was initiated at tinct species was weaker (Fig. 3C). Large a time when closed woodland was assumed carnivorous and herbivorous , as to be the naturally dominant vegetation in well as reptiles (tortoises), are the focus of the much of Europe. In 1983, populations of current literature (Fig. 4A and SI Appendix, primitive and breeds were in- Table S3), reflecting the importance attrib- troduced as proxies for their extirpated wild uted to them in generating trophic cascades ancestors, along with red deer (Cervus ela- and, for tortoises, also ease of implementation phus), with a major—successfully achieved— (25). Furthermore, most cases concern rein- aim being maintaining in drier troduction of species regionally or locally parts as feeding habitats for greylag geese extirpated during the last 5,000 y (Fig. 4B), (Anser anser) (64). The geese are themselves likely reflecting their greater acceptance. Still, important for local bird diversity, because a substantial proportion concerns intro- during molting they withdraw to the marshy duction of ecological replacements (Fig. 4B), parts, reed beds and creating a mo- mostly substituting species extinct <5,000 y saic of shallow water and vegetation that fa- ago (SI Appendix,TableS3), illustrating at- Fig. 2. Examples of reintroductions or extant functional cilitates many other species (64). Largely tention to rewilding with large tortoises counterparts to replace extinct species in ongoing or pro- regulated by food availability, the herbivores on islands. posed rewilding projects on islands and continents: Island have strongly reduced the predominantly Among the empirical studies, many cover examples include (Bottom to Top): Snares Island snipe nonthorny woody vegetation (64–66). In the most studied island rewilding experi- (Coenocorypha huegeli) replacing the South Island snipe – (Coenocorypha iredalei) on Putauhinu Island, New Zealand; time a dynamic tree mosaic might ments to date, the introduction of exotic giant Aldabra tortoise (Aldabrachelys gigantea)replacing establish if grazing refuges develop (65) [e.g., tortoises (Astrochelys radiata, Aldabrachelys giant Cylindraspis tortoises on Rodrigues Island, Mauritius; via temporary declines in abun- gigantea)onsmallislandsnearMauritius African sulcata tortoises (Centrochelys sulcata)replacinga dance and thorn scrub establishment (66)]. as replacements for extinct giant tortoises flightless bird, the moa-nalo (Chelychelynechen quassus)on – Kaua’i, Hawai’i. Continental examples include (Bottom to In , and other herbivores have (Cylindrapsis) (e.g., refs. 25, 70 72), and giant Top): (Sus scrofa), experimental reintroduction to been reintroduced to a site, with the goal tortoise (Chelonoidis spp.) translocations a fenced rewilding site in the Scottish Highlands; European of restoring grazing-dependent - within the Galapagos Islands (e.g., ref. 73). Bison (Bison bonasus), an increasing number of rewilding vegetation (67). Results to date in- These studies document that large and giant reintroductions of this species are being implemented across Europe, here in Vorup Enge, Denmark (all ongoing projects); dicate a shift from shrub- to grass-dominance tortoises are low-, high-impact rewilding (Elephas maximus) replacing straight-tusked in experimental enclosures (68). In recent candidates that provide key ecological func- elephant (Elephas antiquus) in Eskebjerg Vesterlyng, Denmark years, many more trophic rewilding projects tions as dispersers of large seeds, herbivores, (3-d pilot experiment, 2008). Approximate times because are being implemented (Fig. 2). Notably, in- and disturbance agents. These factors and the local or regional extinction of the original taxa are given. troduction of nonnative large tortoises as initial successes have led to proposals for Images courtesy of (Top Right) J. Kunstmann and (Bottom Left) C. Miskelly. replacements for extinct species is being tortoise rewilding efforts on other islands tested on several oceanic islands (25). (25). An important point comes from a These constitute functional megaherbivore >30-y reintroduction project for a Galapagos ecosystems are useful models (46, 47). Im- reintroductions, as tortoises were the larg- tortoise (Chelonoidis hoodensis)toEspañola portantly, trophic complexity (55), such as est native vertebrates on many islands (69). Island, showing successful population estab- diversity within trophic levels, can be im- Several studies have documented their lishment but limited ecosystem recovery be- portant (7, 56). It is clear, however, that successful establishment (70) and found cause of self-reinforcing past anthropogenic large herbivores were numerically abundant them to improve dispersal and recruitment vegetation changes (74). The authors con- in the Late Pleistocene and had strong im- in endemic trees (71) and suppress invasive clude that functional reinstatement of eco- pacts on vegetation structure and ecosystem plants (72). system engineers may necessitate large-scale dynamics (35, 57, 58). habitat restoration efforts jointly with pop- State of Literature Focused on Trophic ulation restoration (74). The nontortoise em- Lessons From Major Trophic Rewilding Rewilding. Tofurtherassessthestateof pirical studies cover a broad range of topics, Experiments. Explicit trophic rewilding ex- trophic rewilding science, we carried out a such as climatic suitability, biodiversity im- periments are few in number, but have pro- systematic review of the international sci- pacts, and public acceptance, but are too few vided important lessons. The reintroduction entific literature, identifying 91 rewilding- and scattered in focus to allow generalization of wolves to Yellowstone National Park in focused publications (Methods). Despite an (SI Appendix,TableS1). the mid-1990s is perhaps the most widely ongoing increase in publications (Fig. 3A), known example (59). The wolves restored a empirical studies are few whereas essays and Insights from Unintentional Trophic tritrophic cascade, where direct predation opinion pieces predominate (Fig. 3B and SI Rewilding. Building on Wilder et al. (75), and behavioral impacts on American Appendix,TableS1). There is strong geo- we define unintentional trophic rewilding as (Cervus elaphus) have increased regeneration graphic bias in the literature and the fea- introduction of a species or functional type of Populus and Salix spp., with indirect effects tured projects, with most focusing on North of relevancy for restoring trophic cascades on other wildlife and geomorphology (60). America, Europe, and oceanic islands (Fig. done without knowledge that it was once

Svenning et al. PNAS Early Edition | 3of7 AB C rable to that of space research, it would be easy to conduct strong factorial-design ex- periments in replicated 100- to 1,000-km2 enclosures to rigorously test key issues. Pragmatically, an increasing number of re- wilding programs are being implemented (Fig. 2), providing important opportunities if designed to allow scientific assessment of their effects and with a monitoring program to follow their dynamics (e.g., ref. 89). It is important that assessments provide broad coverage of biodiversity and ecosystem pro- cesses: for example, also more rarely assessed D species-rich groups, such as insects and fungi. In the following, we discuss key priorities for rewilding research.

Global Scope. The potential ecological im- pact of trophic rewilding should increase with the degree to which megafaunas have been impoverished. We provide a global es- timate of such deficits (Fig. 1) by comparing the current species richness for three key Fig. 3. Characteristics of international scientific publications focused on trophic rewilding (n = 91) (see Methods for terrestrial megafauna functional groups with further details on the systematic review): (A) number published per year, (B) literature categories, (C) attitude toward their estimated species richness given the rewilding using reintroduction of species extirpated <5,000 y, reintroduction of species extirpated >5,000 y ago, or present climate, but in the absence of Late ecological replacements, (D) geographical focus. Pleistocene and Holocene extinctions and extirpations: megaherbivores (≥1,000 kg – native. Large-scale examples include the re- After millennia of declines (2, 3), large body mass), large herbivores (45 999 kg), ≥ introduction of equids (Equus spp.) to the mammals are making a comeback in Europe and large carnivores ( 21.5 kg), corre- New World (75, 76), fallow deer (Dama and , with legal protection, sponding to the size where predators switch dama) across Europe (76), (Ovibos targeted species conservation, supportive from small to large prey (90). Mega- herbivores are absent from most areas today, moschatus) across the Eurasian and North public opinion, and land abandonment as except in increasingly small parts of South- American (76, 77), and certain in- drivers (e.g., 43, 44). It is important to assess east Asia and Africa. However, most conti- troduced birds in New Zealand (78). the impacts. For example, are the recoveries nental areas had megaherbivore richness Unintentional rewilding offers an under- of apex predators sufficient to restore trophic comparable to or higher than those currently exploited research opportunity, often on cascades in human-dominated landscapes? seen in Africa and Asia (Fig. 1). Because larger spatiotemporal scales than possible Outside large reserves, human impacts proboscideans were members of this guild in with experiments. North American feral could limit their ecological role (85). How- all regions except Australia, extant elephant constitute one of the best-studied ever, there are examples of restored trophic species are relevant to consider as ecological cases. Local effects on vegetation and wild- cascades in such landscapes (43). The re- replacements in most areas (16, 18, 91). life have been documented (79, 80), but our covery of large herbivore populations has Major diversity deficits are also widespread current understanding on how feral horses been even more pronounced than carnivores for large carnivores and large herbivores, al- influence ecosystems nevertheless remains and often has strong ecological effects. Deer though most areas still have some represen- limited [e.g., in terms of geographic vari- have expanded dramatically in many areas tatives (Fig. 1). The strongly reduced diver- ability, scale dependency, and predation ef- and can suppress tree regeneration as well as sities in all three groups in most regions fects (81)]. Studies of introduced species affect plant and diversity (41, 86), suggest a global relevancy of trophic rewild- generally also have potential to inform re- and not always negatively (41, 87). Again, ing, and a need for overcoming the strong wilding; for example, as seen in a recent human activities are likely to influence geographic research biases. study comparing native and introduced these effects. plant mutualists, concluding that ecologi- Trophic Complexity. The complexity of cal replacements may benefit native plants Priorities for Research on Trophic restored trophic networks is likely highly when native mutualists have been lost (82). Rewilding important (55), but not well understood in Exemplifying this, feral pigs (Sus scrofa)in There is a clear need for developing a larger, the context of rewilding: that is, how do the Pantanal have helped restore dispersal of more systematic research program to develop simple pair-wise systems, such as a -red plants adapted for dispersal by extinct the scientific basis for trophic rewilding, with deer, differ from complex networks involving megafauna (83, 84). trophiccascadesasakeyframework(6,27). multiple carnivores and a broad range of A difficulty is that to assess its role as a herbivores, some partially immune to pre- Insights from Wildlife Comebacks. An- large-scale restoration tool, large experimental dation (6, 45, 47)? Importantly, outside Africa other underexploited source of information areas are needed (cf. ref. 88). If ecological and Asia no experiment has yet assessed the comes from spontaneous wildlife comebacks. research received a level of funding compa- effects of restoring full Pleistocene-like

4of7 | www.pnas.org/cgi/doi/10.1073/pnas.1502556112 Svenning et al. A ecosystems (e.g., refs. 47 and 92), research of tools—such as culling, targeted feeding, PERSPECTIVE needs to address how this restoration ap- and fencing—to maximize benefits and re- SPECIAL FEATURE: 0−9 kg 100−499 kg proach can best be implemented in different duce costs (93, 101, 102). 10−49 kg 500−999 kg 50−99 kg ≥ 1000 kg landscape settings. One important issue is how constraints on animal movement (e.g., Climate Change. Strong changes in climate seasonal migration), such as fences, will affect are expected for the next 100 y and beyond, its ecological effects, and how these con- and are already now driving shifts in species straints can be overcome if needed (93). Al- ranges and ecosystem changes (103). These though fences sometimes have negative ef- dynamics will impact all conservation man-

Number of proposals fects [e.g., limiting the ability of large agement, including trophic rewilding. It will 010305070 010305070 herbivores to disperse seeds across landscapes be important to assess how climate changes (cf. ref. 94)], they may also have positive ef- may affect the outcome of rewilding efforts, fects, by excluding negative anthropogenic for example altering the suitability of a given Birds effects (93). More generally, it needs to be locality for a candidate species. Trophic re- Reptiles

mammals addressed how trophic rewilding integrated wilding has the potential to help mitigate Herbivorous Carnivorous Omnivorous Omnivorous Invertebrates with other conservation approaches (92) may negative effects of climate change. Free- be best implemented to promote biodiverse ranging large herbivores will increase seed- ecosystems that are as self-regulating as dispersal distances for many plants (94), in- B possible within the constraints of limited creasing their ability to track climate. Trophic space and human needs in urban or agri- cascades established by rewilding may also 0−9 kg mammals 100−499 mammals kg 10−49 kg 500−999 kg cultural areas. Whether a land-sparing or sometimes halt detrimental ecosystem changes. 50−99 kg ≥ 1000 kg land-sharing approach should be adopted to (Rangifer tarandus)andmuskoxen achieve these goals remains an open question (Ovibos moschatus) can limit shrub expan- (95, 96), although some land sparing seems sion in , reducing negative effects essential (96). Related to this, there is a need on herbaceous plants (104). It is even hypo- to assess how rewilding will impact ecosystem thesized that restoration of Pleistocene-like services. Agricultural land is a dominant land megafaunas in the Arctic may re-establish Number of proposals use over much of Earth’s terrestrial surface grasslands, slow thawing, and 010010 30 30 50 50 70 70 (97) and returning it to wild land will likely increase , reducing warming (68). decrease the provision of food but restore However, it is also plausible that megafauna other services, particularly regulating and restoration in some cases may trade-off function Novel Novel

<5000 ya >5000 ya cultural services (98). Understanding the against climate change mitigation, decreasing Range restriction Extirpation Extirpation Ecological

replacement balance of such costs and benefits and the carbon sequestration (105) and increasing factors determining them will be important (33). There is a strong Fig. 4. Characteristics of species mentioned for re- for guiding policies on rewilding. Finally, in wilding introductions in international scientific publica- need for research to further our under- tions focused on trophic rewilding (n = 91) (see Methods landscapes dominated by nonanalog novel standing of these issues. for further details on the systematic review). (A) Organism ecosystems (99), it may also be relevant to group and body mass. (B) Introduction geography [range- consider rewilding introductions to establish Species Selection for Trophic Rewilding restricted species (species extirpated locally, but still ex- novel trophic cascades to promote self-regu- Systematic Framework. Introducing a tant within the focal zoogeographic region, with reduced species into an ecosystem to restore a process range), species extirpated <5,000 y ago (species com- lating biodiverse ecosystems (100). Such a pletely extirpated from the focal region within the last radical approach would clearly require a solid inherently involves uncertainty. Therefore, a 5,000 y, but still extant elsewhere), species extinct >5,000 y scientific base. science-based decision framework that allows ago (species completely extirpated from the focal region practitioners to systematically evaluate po- more than 5,000 y ago, but still extant elsewhere), ecological Management Targets and Tools. Many tential costs and benefits of a given rewilding replacement for a globally extinct species, novel function (introduction to achieve novel ecological function without a trophic rewilding projects most logically introduction would be of high utility. Existing past analog)], and body mass. should be implemented as open-ended con- guidelines for conservation translocations are servation projects, acknowledging the limits an appropriate starting point, providing best of our knowledge and unavoidable future practices on aspects, such as monitoring, trophic complexity. Notably, experimental changes, for example, in climate (89). Nev- feasibility assessment, and release strategies rewilding studies on megaherbivores are ertheless, direct management decisions will (106). However, guidelines for the key aspect lacking, despite their high functional im- continue to play an important role in many of species selection for rewilding are lacking. portance and former omnipresence. cases because of societal requirements or A systematic framework should consider spatial constraints. Hence, research on func- three aspects: (i) Match between the ecology Landscape Setting and Interplay with tional rewilding targets is needed (e.g., ref. of the candidate species and the focal func- Society. Trophic rewilding projects range 35), preferably combining paleoecological tions to be restored, with functional traits as from small fenced biotopes to large landscapes and historical evidence with experimental an important source of information. (ii) and are situated in a variety of environ- studies. Although trophic rewilding may Phylogenetic relatedness, to restore the evo- ments and landscape structures. As land- benefit natural ecosystems and recreational lutionary potential of a lineage but also to scape factors—such as area, climate, envi- values, it may also cause human–wildlife capture subtle functional aspects. Still, there ronmental gradients, and disturbance, as well conflicts: for example, damages to crops and may be relevant ecological replacements even as societal circumstances—may be highly . There is a need to collect empirical when no closely related species is available important for the ecology of megafauna-rich evidence for effectiveness and consequences (100, 107). (iii) Suitability of the present and

Svenning et al. PNAS Early Edition | 5of7 forecasted future climate, ecosystem, and (spontaneous ecological dynamics without The systematic review was based on English-language societal circumstances to accommodate the management) (12, 14, 15), abiotic rewilding scientific papers published by December 2014, found in Web of Science and Scopus using the search terms candidate species (108). This would include (restoration of natural physical processes, e.g., “rewilding” and “re-wilding.” Additionally,toexpandcover- evaluating conservation and societal benefits river dynamics), and open-ended manage- age, for the 10 highest-cited papers, we used Google and . ment (89). Scholar to provide lists of citing articles and reviewed these, too. To ensure that the systematic review was focused on Integrating Synthetic Biology and Methods publications on rewilding in the sense of trophic rewilding as defined here, we only included articles treating conservation Rewilding. Although trophic rewilding has We compared current distributions following the International Union for Conservation of Nature with translocations explicitly aimed to restore ecological function. focused on reintroducing regionally extir- estimated present-natural distributions. The term “pre- For each paper we then assessed: (i) author attitude towards pated species or ecological replacements for sent-natural” refers to the state that a phenomenon rewilding, separately for the following introduction geogra- extinct species, an alternative approach that would be in today in the complete absence of human phies: reintroductions of extant species that have been leverages synthetic biology (109, 110) is influence through time (111). Present-natural distribu- completely extirpated from the focal zoogeographical region tions were estimated for all mammal species with oc- within the last 5,000 y, reintroductions of extant species emerging. It appears likely that it will become > currence records from within the last 130,000 y completely extirpated from the focal region 5,000 y ago, or possible to engineer organisms to resemble [following a recently revised (112)], as the far introductions of ecological replacements for globally extinct extinct species genetically, phenotypically, or majority of extinctions in this period can be linked to species; (ii) type of publication (essay or opinion piece; re- functionally (108, 110). It therefore makes Homo sapiens’ global expansion (2–4). A full description view; experiment; nonexperimental empirical); (iii)geo- graphic focus; (iv) rewilding projects mentioned; and (v) sense to begin integrating the discipline with of the estimated ranges can be found in Faurby and Svenning (113). For extant species, these were based on species for rewilding mentioned. Species were characterized trophic rewilding (110). Synthetic biology historical range estimates when available or alternatively by organism group, diet, introduction geography (as above, could become a powerful component of on a combination of historic knowledge and climate. For plus reintroductions of locally extirpated species still extant trophic rewilding by overcoming limits to prehistoric extinct species, ranges were generally based elsewhere within a given region, and introductions to what can be achieved with extant species, as a on a co-occurrence approach, assuming that they would achieve novel ecological functions), body mass, and time since disappearance from the focal zoogeographical region. substantial proportion of extinct species have have responded to the late-Quaternary climatic changes similarly to the species with which they used to co-occur. The SI Appendix provides an overview of the methodology no close substitutes: for example, mega- Hence, we estimated their present-natural distributions for the systematic review as well as the resulting data. herbivores capable of tolerating and based on those of the extant species with which they co- arctic climates. Hence, a framework for in- occurred. To evaluate this approach, we compared the ACKNOWLEDGMENTS. This work was supported in part by European Research Council Grant ERC-2012-StG- tegrating synthetic biology and trophic re- range of 39 extant species in North America estimated with this approach to their historical (pre-Columbus) 310886-HISTFUNC (to J.-C.S.); Aarhus University and the Aage V. Jensen Foundations (P.B.M.P.); and Conselho wilding science is needed to evaluate risks distributions. The correlation between present-natural and benefits (108). ρ = Nacional de Desenvolvimento Científico and Fundação de and historic diversity ( 0.856) was higher than be- Amparo à Pesquisa do Estado de São Paulo (M.G.). We ρ = tween historic and current diversity ( 0.762) (113). The consider this article a contribution to the Danish National Outlook resulting megafauna diversity patterns are broadly con- Research Foundation Niels Bohr professorship project We believe trophic rewilding has strong cordant with earlier studies (114). Aarhus University Research on the Anthropocene. scope for ecological restoration in the Anthropocene, to remedy defaunation and restore trophic cascades that promote self- 1 Crutzen PJ (2002) Geology of mankind. Nature 415(6867):23. 15 Schnitzler A (2014) Towards a new European wilderness: 2 Sandom C, Faurby S, Sandel B, Svenning J-C (2014) Global late Embracing unmanaged growth and the decolonisation of regulating biodiverse ecosystems. 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Svenning et al. PNAS Early Edition | 7of7 Fig. S1: Overview of methodology for the systematic review. Step 1: Literature search Step 2: Filtering Step 3: Google Scholar Step 4: Included Expansion and filtering

Search of Removal of English‐language duplicates, books, Expanding literature lists literature book reviews, from Google Scholar by Included in containing conference screening citations from subsequent data “rewilding OR re‐ abstracts, the 10 most cited analysis: wilding” on WoS editorials, and publications from the WoS and Scopus and Scopus until irrelevant databases and removing (n=69) December 2014 literature irrelevant literature Google Scholar (22) WoS (n=116) according to according to rewilding In total: (n=91) Scopus (n=112) rewilding criteria criteria (n=22) (n=69)

1. Attitude (“Pro”, “Con”, and “Neutral”) towards rewilding with species extirpated <5000 years ago, species extirpated >5000 years ago, and ecological replacements.

2. Literature categories: “Essay or Opinion piece”, “Experiment”, “Review”, and “Non‐ 1. Attitude experimental empirical”. 2. Literature category 3. Geographic focus of paragraphs concerning rewilding. 3. Geographic focus

4. Rewilding initiatives referred to or reported in the rewilding literature that 4. Rewilding projects fulfills the rewilding criteria (country‐level if possible). 5. Species used in rewilding 5. Species used in rewilding projects or suggested as rewilding candidates were categorized into projects or suggested as organism groups (“Carnivorous mammals”, “Herbivorous mammals”, “Omnivorous rewilding candidates mammals”, “Reptiles”, “Birds”, and “Invertebrates”), introduction geography (“Range restricted,” “Extirpated <5000 years ago”, “Extirpated >5000 years ago”, ”Ecological replacement”, and “Novel function”), body mass (“0‐9kg”, “10‐49kg”, “50‐99 kg”, “100‐ 499kg”, “500‐999kg”, “≥1000kg”), and times since disappearance (“Partly present”, “0‐99 years ago”, “100‐499 years ago”, “500‐1.999 years ago”, “2.000‐4.999 years ago”, “>5000 years ago”, and “Never present”).

Step 6: Scoring Step 5: Data extraction Table S1: Characteristics of the articles used in the systematic review (n=91). Characteristics include our assessment of the authors’ attitude (neutral, positive, negative, and NA (not available)) towards trophic rewilding (separately considering reintroductions of extant species that have been extirpated from the focal zoogeographical region within the last 5000 years, reintroductions of extant species that have been extirpated from a given region >5000 years ago, and introductions of ecological replacements for a globally extinct species), literature categories (essay or opinion, review, experiment, non-experimental empirical), and geographical focus of rewilding section in the publication.

No. Publication Source Attitude Literature Geographic Extirpated Extirpated Ecological categories focus <5000 years >5000 years replacement ago ago 1 Aslan CE, Zavaleta ES, Croll Google NA NA Pro Essay/Opinion Whole DON & Tershy B (2012) Effects Scholar world of native and non-native vertebrate mutualists on plants. Conservation Biology 26(5):778-789.

2 Biello D (2011) Tortoises to the WoS/Scopus Pro NA Pro Essay/Opinion Many rescue. Rewilding islands and even different continents could prove an effective places method for reversing ecological catastrophe. Scientific American 305(1):16. 3 Bowman D (2012) Conservation: Google NA NA Pro Essay/Opinion Australia Bring elephants to Australia? Scholar Nature 482(7383):30-30. 4 Brown C, McMorran R & Price WoS/Scopus Pro NA NA Essay/Opinion Europe MF (2011) Rewilding - A new (Scotland) paradigm for nature conservation in Scotland? Scotish Geographical Journal 127(4):288-314. 5 Buck HJ (2015) On the WoS/Scopus Neutral Neutral Neutral Review North possibilities of a charming America Anthropocene. Annals of the (plus Association of American Europe) Geographers 105(2):369-377.1 6 Burney DA & Burney LP (2007) Google Pro Pro Pro Essay/Opinion Hawaii Paleoecology and “inter-situ” Scholar restoration on Kaua'i, Hawai'i. Frontiers in Ecology and the Environment 5(9):483-490. 7 Cajal JL & Tonni EP (2006) Re- WoS/Scopus NA NA Neutral Essay/Opinion South wilding in South America: Is it America possible? Mastozoologia (Argentina) Neotropical 13:281-282.

8 Caro T (2007) The Pleistocene re- WoS/Scopus Neutral Neutral Neutral Review North wilding gambit. Trends in Ecology America and Evolution 22(6):281-283. 9 Caro T & Sherman, P (2009) WoS/Scopus Pro NA Con Essay/Opinion North Rewilding can cause rather than America solve ecological problems. Nature 462:985. 10 Chapron G (2005) Re-wilding: WoS/Scopus NA NA Neutral Essay/Opinion Africa, Other projects help carnivores stay Asia wild. Nature 437(7057):318. 11 Corlett RT (2013) The shifted WoS/Scopus Pro Pro Pro Review Lowland baseline: Prehistoric defaunation tropics in the tropics and its consequences for biodiversity conservation. Biological Conservation 163(1): 13-2.

1 This article was Early View in 2014 12 Chrulew M (2011) Reversing WoS/Scopus Neutral Neutral Neutral Essay/Opinion Siberia extinction: restoration and resurrection in the Pleistocene rewilding projects. Humanimalia 2(2):4-27 13 Dinerstein E & Irvin WR (2005) WoS/Scopus Pro NA Con Essay/Opinion North Re-wilding: No need for exotics as America natives return. Nature 437: 476. 14 Donlan J, et al. (2005) Re-wilding WoS/Scopus NA Pro Pro Essay/Opinion North North America. Nature 436:913- America 914. 15 Donlan CJ, et al. (2006) WoS/Scopus NA Pro Pro Essay/Opinion North Pleistocene rewilding: an America optimistic agenda for twenty-first (plus whole century conservation. American world) Naturalist 168(5):660-681. 16 Downer CC (2014) The horse and Google Pro Pro NA Essay/Opinion North burro as positively contributing Scholar America returned natives in North America. American Journal of Life Sciences 2(1):5-23. 17 Driscoll CA, et al. (2012) A Google Pro NA NA Essay/Opinion Central and postulate for recovery: the Scholar East Asia case of the Caspian Tiger. Journal of Threatened Taxa 4(6):2637– 2643. 18 Edwards T, et al. (2014) Genetic WoS/Scopus NA Pro NA Experiment North assessments and parentage America analysis of captive Bolson (New tortoises (Gopherus Mexico) flavomarginatus) inform their "rewilding" in New Mexico. PLoS One 9(7):e102787. 19 Estrada A (2014) Reintroduction WoS/Scopus Pro NA NA Experiment Central of the scarlet macaw (Ara macao America cyanoptera) in the tropical (Mexico) rainforests of Palenque, Mexico: project design and first year progress. Tropical Conservation Science 7(3):342-364. 20 Featherstone A, (2004) Rewilding WoS/Scopus Pro NA NA Essay/Opinion Scotland in the north-central Highlands - An update. Ecos 25(3-4):4-10. 21 Foreman D (1999) The wildlands WoS/Scopus Pro NA NA Review North project and the rewilding of North America America. Denver University Law Review 76:535-553. 22 Fredrickson EL, Estell RE, Google NA NA Pro Essay/Opinion North Laliberte A & Anderson DM Scholar America (2006). Mesquite recruitment in the Chihuahuan Desert: historic and prehistoric patterns with long- term impacts. Journal of Arid Environments 65(2):285-295. 23 Fuhlendorf SD, Engle DM, Kerby WoS/Scopus Pro NA Pro Essay/Opinion North J & Hamilton R (2009) Pyric America herbivory: Rewilding landscapes through the recoupling of fire and grazing. Conservation Biology 23(3):588-598. 24 Gerlach J, Rocamora G, Gane J, Google NA NA Pro Review Seychelles Jolliffe K & Vanherck L (2013) Scholar Giant tortoise distribution and abundance in the Seychelles Islands: Past, present, and future. 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Table S2: Summary of rewilding projects mentioned in the articles used in the systematic review (SI Appendix, Table S1). These include initiatives fulfilling the criteria for trophic rewilding used in the systematic review (ecological restoration involving conservation translocations explicitly aimed to restore ecological function) as well as initiatives otherwise referred to as rewilding projects in the articles themselves. The species introduction column lists both already introduced taxa (including temporary experimental introductions) and, in parentheses, taxa that are only mentioned as candidates for future introductions.

Geographic Name Species introductions Publications (cf. SI location Appendix, Table S1) Chile Nature Reserve Guanaco 50 Altos de Cantillana, central Chile (0.496 ha) England Knepp Estate, West Tamworths/red-brown pig, 82 Sussex (1400ha) English longhorn cattle, fallow deer, Exmoor pony (Heck cattle, beaver, , red deer)

Europe Rewilding Europe 2, 35, 64 (10 areas, aiming to reach 1,000,000 ha in total) Galapagos Pinta Island (6000 Galapagos giant tortoise 25, 33 ha), Floreana Island (17,300 ha), and Espaniola island (6000 ha) Hawaii Makauwahi Cave African spurred tortoise 6, 64, 75 Reserve (6.9 ha) Holland Oostvaardersplassen Konik horse, red deer, Heck 2, 15, 35, 52, 53, 62, 64 (5600 ha) cattle (European bison, wild 75, 78, 82 boar) Latvia Pape (250 ha) Konik horse 35

Madagascar Beanka Nature Aldabran tortoise 33, 60 Reserve (14,000 ha) Mascarene Islands Ile aux Aigrettes Aldabran tortoise, 11, 15, 24, 26, 27, 29, (25 ha), Round Madagascan radiated 32, 33, 44, 55, 60, 64, Island (215 ha) tortoise 66, 69, 86, Rodrigues (19 ha) Mexico Palenque National Scarlet macaw 19 Park (1800 ha) New Zealand Putauhinu Island Snare Island snipe 55 (141 ha) Pleistocene Park , bison, musk 12,15, 47, 64, 68 (1600 ha) ()

Scotland Alladale Wilderness Wild boar 47, 70 Reserve (9300 ha - attempt to achieve 20,000 ha fenced reserve) Scotland Knapdale Forest, Beaver 47 Argyll (19,800 ha)

Scotland Trees for Life, Glen None 20, 70 Afric (260,000 ha)

Seychelles ~17 small islands Aldabran tortoise 24, 26, 33 (maximum size: 460 ha) USA Yellowstone Wolf 14, 15, 47, 62, 64 National Park (~900,000 ha) USA Armendaris Ranch, Bolson tortoise 15, 18, 67, 85 New Mexico (~147000 ha)

Table S3: Species mentioned for rewilding in the articles used in the systematic review (SI Appendix, Table S1). Characteristics include organism group (invertebrates, reptiles, birds, and mammals; the latter is further divided according to diet), introduction geography (range restriction [extant within the focal zoogeographic region, but with reduced range], species extirpated <5000 years ago [extant species that have gone extinct within the focal region within the last 5000 years], species extinct >5000 years ago [extant species that have gone extinct within the focal region more than 5000 years ago], ecological replacement for a globally extinct species, and novel function [introduction to achieve novel ecological function]), body mass, and times since disappearance (partly present, 0-99 years ago, 100-499 years ago, 500- 2000 years ago, 2000-5000 years ago, >5000 years ago, and never present).

Species (latin Species (common Reference Source Organism Introduction Body Time since name) name) (Appendix group geography mass (kg) disappearance SI, Table S1) (ya) Acinonyx jubatus Cheetah 15 WoS/Scopus Carnivorous Ecological 10-49 >5000 mammal replacement Acinonyx jubatus Cheetah 14 WoS/Scopus Carnivorous Ecological 10-49 >5000 mammal replacement Aldabrachelys Aldabran tortoise 32 WoS/Scopus Reptile Ecological 100-499 100-499 gigantea replacement Aldabrachelys Aldabran tortoise 33 WoS/Scopus Reptile Ecological 100-499 500-1999 gigantea replacement Aldabrachelys Aldabran tortoise 33 WoS/Scopus Reptile Range 100-499 Partly present gigantea restricted Aldabrachelys Aldabran tortoise 33 WoS/Scopus Reptile Ecological 100-499 100-499 gigantea replacement Aldabrachelys Aldabran tortoise 26 WoS/Scopus Reptile Ecological 100-499 100-499 gigantea replacement Aldabrachelys Aldabran tortoise 27 WoS/Scopus Reptile Ecological 100-499 100-499 gigantea replacement Aldabrachelys Aldabran tortoise 29 WoS/Scopus Reptile Ecological 100-499 100-499 gigantea replacement Aldabrachelys Aldabran tortoise 24 Google Reptile Range 100-499 Partly present gigantea Scholar restricted Aldabrachelys Aldabran tortoise 28 Google Reptile Ecological 100-499 100-499 gigantea Scholar replacement Aldabrachelys Aldabran tortoise 60 Google Reptile Ecological 100-499 500-1999 gigantea Scholar replacement Aldabrachelys Aldabran tortoise 60 Google Reptile Ecological 100-499 500-1999 gigantea Scholar replacement Aldabrachelys Aldabran tortoise 86 Google Reptile Ecological 100-499 100-499 gigantea Scholar replacement Anas laysanensis Laysan teal 6 Google Bird Range 0-9 Partly present Scholar restricted Ara macao Scarlet Macaw 19 WoS/Scopus Bird Range 0-9 Partly present cyanoptera restricted Astrochelys Madagascan radiated 33 WoS/Scopus Reptile Ecological 10-49 100-499 radiata tortoise replacement Astrochelys Madagascan radiated 26 WoS/Scopus Reptile Ecological 10-49 100-499 radiata tortoise replacement Astrochelys Madagascan radiated 29 WoS/Scopus Reptile Ecological 10-49 100-499 radiata tortoise replacement Astrochelys Madagascan radiated 28 Google Reptile Ecological 10-49 100-499 radiata tortoise Scholar replacement Axis Calamian Hog deer 54 WoS/Scopus Herbivorous Range 10-49 Partly present calamianensis mammal restricted Bison bison 12 WoS/Scopus Herbivorous Extirpated 500-999 500-1999 mammal <5000 Bison bonasus European bison 82 WoS/Scopus Herbivorous Range 500-999 Partly present mammal restricted primigenius Aurochs/Heck cattle 82 WoS/Scopus Herbivorous Extirpated 500-999 500-1999 mammal <5000 Buteo solitarius Hawaiian hawk 6 Google Bird Range 0-9 Partly present Scholar restricted Camelus Wild Bactrian 15 WoS/Scopus Herbivorous Ecological 500-999 >5000 bactrianus mammal replacement Camelus Wild 14 WoS/Scopus Herbivorous Ecological 500-999 >5000 bactrianus mammal replacement Canis lupus Wolf 4 WoS/Scopus Carnivorous Range 10-49 Partly present mammal restricted Canis lupus Wolf 20 WoS/Scopus Carnivorous Range 10-49 Partly present mammal restricted Canis lupus Wolf 47 WoS/Scopus Carnivorous Range 10-49 Partly present mammal restricted Canis lupus dingo Dingo 34 WoS/Scopus Carnivorous Ecological 10-49 0-99 mammal replacement Canis lupus dingo Dingo 3 Google Carnivorous Ecological 10-49 0-99 Scholar mammal replacement Castor fiber Beaver 4 WoS/Scopus Herbivorous Range 10-49 Partly present mammal restricted Castor fiber Beaver 20 WoS/Scopus Herbivorous Range 10-49 Partly present mammal restricted Castor fiber Beaver 82 WoS/Scopus Herbivorous Range 10-49 Partly present mammal restricted Castor fiber Beaver 47 WoS/Scopus Herbivorous Range 10-49 Partly present mammal restricted Centrochelys African spurred 64 WoS/Scopus Reptile Ecological 50-99 500-1999 sulcata tortoise replacement

Cervus elaphus Red deer (elk/wapiti) 4 WoS/Scopus Herbivorous Range 100-499 Partly present mammal restricted Cervus elaphus Red deer (elk/wapiti) 82 WoS/Scopus Herbivorous Range 100-499 Partly present mammal restricted Chelonoidis Red-footed tortoise 33 WoS/Scopus Reptile Ecological 0-9 1999-5000 carbonaria replacement Chelonoidis nigra Galapagos giant 25 Google Reptile Range 50-99 Partly present tortoise Scholar restricted Chelonoidis nigra Galapagos giant 38 Google Reptile Range 50-99 Partly present tortoise Scholar restricted Chelonoidis nigra Galapagos giant 37 Google Reptile Range 50-99 Partly present tortoise Scholar restricted Chelonoidis nigra Galapagos giant 33 WoS/Scopus Reptile Range 50-99 Partly present tortoise restricted Chelonoidis nigra Galapagos giant 33 WoS/Scopus Reptile Range 50-99 Partly present tortoise restricted Chelonoidis nigra Galapagos giant 54 WoS/Scopus Reptile Ecological 50-99 1999-5000 tortoise replacement Coenocorypha Snares island nipe 55 WoS/Scopus Bird Ecological 0-9 0-99 huegeli replacement Coturnix Australian brown 59 Google Bird Ecological 0-9 100-499 ypsilophora quail Scholar replacement Dicerorhinus Sumatra rhinoceros 54 WoS/Scopus Herbivorous Range ≥ 1000 Partly present sumatrensis mammal restricted Elephas maximus Asian elephant 15 WoS/Scopus Herbivorous Ecological ≥ 1000 >5000 mammal replacement Elephas maximus Asian elephant 14 WoS/Scopus Herbivorous Ecological ≥ 1000 >5000 mammal replacement Elephas maximus Asian elephant 54 WoS/Scopus Herbivorous Range ≥ 1000 Partly present mammal restricted Elephas maximus Asian elephant 54 WoS/Scopus Herbivorous Ecological ≥ 1000 >5000 mammal replacement Equus africanus Burro 16 Google Herbivorous Ecological 100-499 >5000 asinus Scholar mammal replacement Equus ferus Yakutian horse 12 WoS/Scopus Herbivorous Extirpated 100-499 1999-5000 mammal <5000 Equus ferus Przewalski horse 16 Google Herbivorous Extirpated 100-499 >5000 przewalskii Scholar mammal >5000 Equus ferus Przewalski horse 15 WoS/Scopus Herbivorous Extirpated 100-499 >5000 przewalskii mammal >5000 Equus ferus Przewalski horse 14 WoS/Scopus Herbivorous Extirpated 100-499 >5000 przewalskii mammal >5000 Equus ferus Przewalski horse 42 WoS/Scopus Herbivorous Range 100-499 0-99 przewalskii mammal restricted Equus hemionus Asian wild ass 15 WoS/Scopus Herbivorous Ecological 100-499 >5000 mammal replacement Equus hemionus Asian wild ass 14 WoS/Scopus Herbivorous Ecological 100-499 >5000 mammal replacement Felis silvestris European wildcat 4 WoS/Scopus Carnivorous Range 0-9 Partly present mammal restricted Felis silvestris European wildcat 82 WoS/Scopus Carnivorous Range 0-9 Partly present mammal restricted Geograpsus geayi Land crab 6 Google Invertebrate Range 0-9 Partly present Scholar restricted Glaucopsyche Xerces butterfly 74 WoS/Scopus Invertebrate Extirpated 0-9 0-99 xerces <5000 Gopherus Bolson tortoise 15 WoS/Scopus Reptile Extirpated 10-49 >5000 flavomarginatus >5000 Gopherus Bolson tortoise 14 WoS/Scopus Reptile Extirpated 10-49 >5000 flavomarginatus >5000 Gopherus Bolson tortoise 18 WoS/Scopus Reptile Range 10-49 Partly present flavomarginatus restricted Lama guanicoe Guanaco 50 WoS/Scopus Herbivorous Range 100-499 Partly present mammal restricted Loxodonta African elephant 15 WoS/Scopus Herbivorous Ecological ≥ 1000 >5000 africana mammal replacement Loxodonta African elephant 14 WoS/Scopus Herbivorous Ecological ≥ 1000 >5000 africana mammal replacement Loxodonta African elephant (?) 3 Google Herbivorous Novel ≥ 1000 Never present africana (?) Scholar mammal function Lutra lutra European otter 82 WoS/Scopus Carnivorous Range 0-9 Partly present mammal restricted lynx 4 WoS/Scopus Carnivorous Range 10-49 Partly present mammal restricted Lynx lynx Eurasian lynx 20 WoS/Scopus Carnivorous Range 10-49 Partly present mammal restricted Lynx lynx Eurasian lynx 83 WoS/Scopus Carnivorous Range 10-49 Partly present mammal restricted Lynx lynx Eurasian lynx 82 WoS/Scopus Carnivorous Range 10-49 Partly present mammal restricted Melanoplus Rocky mountain 51 WoS/Scopus Invertebrate Extirpated 0-9 100-499 spretus locust <5000 Mustela putorius European polecat 4 WoS/Scopus Carnivorous Range 0-9 Partly present mammal restricted Ovibos moschatus Muskox 12 WoS/Scopus Herbivorous Ecological 100-499 1999-5000 mammal replacement Panthera leo Asiatic 15 WoS/Scopus Carnivorous Ecological 100-499 >5000 persica mammal replacement Panthera leo Asiatic lion 14 WoS/Scopus Carnivorous Ecological 100-499 >5000 persica mammal replacement Panthera tigris Tiger 54 WoS/Scopus Carnivorous Range 100-499 Partly present mammal restricted Panthera tigris Amur tiger 17 Google Carnivorous Range 100-499 Partly present altaica Scholar mammal restricted Pongo abelii Sumatran orangutan 54 WoS/Scopus Omnivorous Range 50-99 Partly present mammal restricted Pongo pygmaeus Bornean orangutan 54 WoS/Scopus Omnivorous Range 50-99 Partly present mammal restricted Rhinoceros Javan rhinoceros 54 WoS/Scopus Herbivorous Range ≥ 1000 Partly present sondaicus mammal restricted Rhinoceros Indian rhinoceros 54 WoS/Scopus Herbivorous Range ≥ 1000 Partly present unicornis mammal restricted Sarcophilus Tasmanian devil 54 WoS/Scopus Carnivorous Range 10-49 Partly present harrisii mammal restricted Sus scrofa Wild boar 4 WoS/Scopus Omnivorous Range 100-499 Partly present mammal restricted Sus scrofa Wild boar 20 WoS/Scopus Omnivorous Range 100-499 Partly present mammal restricted Sus scrofa Wild boar 82 WoS/Scopus Omnivorous Range 100-499 Partly present mammal restricted Sus scrofa Wild boar 70 WoS/Scopus Omnivorous Range 100-499 Partly present mammal restricted Sus scrofa Wild boar 71 WoS/Scopus Omnivorous Range 100-499 Partly present mammal restricted Sus scrofa Wild boar 77 Google Omnivorous Range 100-499 Partly present Scholar mammal restricted Tapirus indicus Malayan tapir 54 WoS/Scopus Herbivorous Range 100-499 Partly present mammal restricted Thylacinus Thylacine 74 WoS/Scopus Carnivorous Extirpated 10-49 0-99 cynocephalus mammal <5000 Ursus arctos Brown bear 4 WoS/Scopus Omnivorous Range 100-499 Partly present mammal restricted Ursus arctos 20 WoS/Scopus Omnivorous Range 100-499 Partly present mammal restricted Varanus Komodo dragon 3 Google Reptile Ecological 100-499 >5000 komodoensis Scholar replacement Zaglossus Sir David´s long- 54 WoS/Scopus Carnivorous Range 0-9 Partly present attenboroughi beaked echidna mammal restricted Zaglossus bartoni Eastern long-beaked 54 WoS/Scopus Carnivorous Range 0-9 Partly present echidna mammal restricted Zaglossus Western long-beaked 54 WoS/Scopus Carnivorous Range 10-49 Partly present bruijinii echidna mammal restricted