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Secondary extinctions of biodiversity Jedediah F. Brodie1,2,3, Clare E. Aslan4, Haldre S. Rogers5, Kent H. Redford6, John L. Maron7, Judith L. Bronstein8, and Craig R. Groves9 1

Department of Botany, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada 3 Biodiversity Research Centre, University of British Columbia, Vancouver BC, V6T 1Z4, Canada 4 Conservation Education and Science Department, Arizona-Sonora Desert Museum, Tucson AZ, 85743, USA 5 Department of Ecology and Evolutionary Biology, Rice University, Houston, TX, 77005, USA 6 Archipelago Consulting, Portland, ME, 04112, USA 7 Division of Biological Sciences, University of Montana, Missoula MT, 59803, USA 8 Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, 85721, USA 9 The Nature Conservancy, Bozeman, MT, 59715, USA 2

Extinctions beget further extinctions when species lose obligate mutualists, predators, prey, or hosts. Here, we develop a conceptual model of species and community attributes affecting secondary extinction likelihood, incorporating mechanisms that buffer organisms against partner loss. Specialized interactors, including ‘cryptic specialists’ with diverse but nonredundant partner assemblages, incur elevated risk. Risk is also higher for species that cannot either evolve new traits following partner loss or obtain novel partners in communities reorganizing under changing environmental conditions. Partner loss occurs alongside other anthropogenic impacts; multiple stressors can circumvent ecological buffers, enhancing secondary extinction risk. Stressors can also offset each other, reducing secondary extinction risk, a hitherto unappreciated phenomenon. This synthesis suggests improved conservation planning tactics and critical directions for research on secondary extinctions. Extinctions beget extinctions For nearly half a century, ecologists have theorized that the human-driven loss of species could trigger cascades of secondary extinctions (see Glossary) among, for example, parasites deprived of their hosts or plants bereft of pollinators (e.g., [1,2]). Simultaneously, a largely separate body of literature has highlighted numerous ecological mechanisms and evolutionary adaptations that buffer organisms against decline following the loss of these interaction partners [3–6], raising the possibility that secondary extinctions are less likely than has been predicted. Reconciling these viewpoints is critical for understanding the degree to which ongoing primary extinctions will induce further erosion of biodiversity and for helping inform conservation policy to address extinction threats. Here, we synthesize available evidence to create a conceptual model illustrating how ecological and eco-evolutionary Corresponding author: Brodie, J.F. ([email protected]). Keywords: co-extinction; conservation planning; extinction debt; functional redundancy; mutualism; resilience; species interactions; trophic cascade. 0169-5347/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2014.09.012

conditions affect the probability of secondary extinctions, when the loss of one species through anthropogenic impacts causes the loss of the taxa with which it had formerly interacted. We review the literature to assess factors that are associated with risk of secondary extinctions. Prior work has discussed pathways to interaction breakdown [7], assessed evolutionary implications of changing interactions [8], and shown clear examples of secondary extinctions in several taxa [9]. We build upon this literature and demonstrate that the likelihood of secondary extinctions can be predicted based on Glossary Co-extinction: the simplest type of secondary extinction, when the loss of a species leads to loss of one other, often a specialist and obligate interactor, such as a parasite. Cryptic specialist: a species that interacts with a diverse assemblage of partners, but where low functional redundancy in the assemblage ensures that only one or a few partners have high species impact. Demographically obligate interaction: an interaction where loss of one species (that is not replaced by others) dooms the interaction partner to extinction. Extinction cascade: a situation where the loss of one species triggers a chain of further loss, usually across different trophic levels. For example, extinction of pollinator could drive loss of an outcrossing plant, followed by disappearance of the specialist herbivores on that plant and the parasitoids of the herbivores. Functional extinction: when a species is reduced in abundance, short of outright extirpation, to the point where it no longer interacts significantly with other species in the community. Functional redundancy: when two or more species have the same ecological relation with, and demographic impacts on, a mutual interaction partner. Interaction partner: a species that interacts with another species directly, for example, as a mutualist or antagonist, or indirectly, such as a predator protecting plants by suppressing herbivory. Primary extinction: loss of a species due to anthropogenic impacts. Extinction can occur at a variety of scales from global to regional or local. Most of the evidence we compile relates to local extirpation, and we specify when we intend the term to refer to other scales. Secondary endangerment: when loss or decline of one species through anthropogenic impacts causes a severe decline in the taxa with which it had formerly interacted. Secondary extinction: when loss of one species through anthropogenic impacts (primary extinction) causes loss of the taxa with which it had formerly interacted. As with primary extinctions, this can occur at several scales; our focus is on local extirpation. Secondary extinction debt: when a species is inexorably declining due to loss of its interaction partner(s) but has not yet disappeared. Species impact: the cumulative effect of one species on the population growth rate of another. This represents the product of the abundance and per-capita interaction strength of the interactor. Trophic cascade: indirect influence of one species on the abundance or biomass of another at least two trophic levels away. For example, a predator might increase plant abundance via suppressing herbivory.

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several traits of the interacting species and the communities in which they reside. Such information could be immediately applicable to conservation planning and community viability analysis (cf. [10]). We restrict our synthesis to cases with identifiable direct causal links between extinctions; we do not consider cases in which extinctions happen contemporaneously due to identical or correlated causes, or situations in which primary extinctions trigger changes in ecosystem structure or function that indirectly affect other species. We focus on empirical evidence related to secondary extinction risk rather than on predictions from models; therefore, we do not discuss the considerable, but mostly untested, theory and predictions from analyses of interaction networks (e.g., [11–15]). While extinction can occur at local, regional, or global scales, most of the evidence we assemble focuses on extirpation of local populations. We also discuss cases in which loss of interaction partners has caused population declines or compromised species persistence without causing actual extinction (i.e., ‘secondary endangerment’). Species and interaction traits that shape secondary extinction risk In our conceptual model (Figure 1), the risk of extinction of a species following the loss of its interaction partners depends on the degree of specialization of the interaction, the dependence on the interaction partners for population persistence, and the rapidity with which the species can either adapt to the absence of the interaction or replace the previous partner with a different one. For display purposes, we present these factors as orthogonal (Figure 1), although in reality the factors might be correlated. For example, specialized interactions might often be obligate rather than facultative, leading to a correlation between degree of specialization and the dependence of the population on the interaction. However, correlations among these three axes are not perfect or fully understood. Certain plants in Hawai’i, for instance, have highly derived and morphologically complex corollas, suggesting specialization for particular pollinators, and yet are also able to

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Figure 1. Conceptual model detailing positive (+) and negative ( ) relations between interaction factors and the likelihood of secondary extinction. Relations that are highly dependent, highly specialized, and/or slow to respond evolutionarily are likely to exhibit higher probability of secondary extinction. Meanwhile, external factors may also affect secondary extinction. Multiple stressors could either increase the likelihood of secondary extinction, by combining to elevation overall threat rates, or could reduce the likelihood by offsetting one another. The presence of novel partnerships could in some cases reduce the likelihood of secondary extinctions by replacing lost ecological functions.

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self-pollinate (i.e., they are facultative outcrossers that, when they do outcross, specialize on particular pollinating animals [16]). How often species with highly specialized interactions exhibit such bet-hedging mechanisms remains an important question. Rethinking specialization Numerous studies have highlighted that secondary extinctions are more likely to occur following the loss of a specialist, rather than generalist, interaction partner (e.g., [9,17,18]). Specialized interactions are generally considered to be particularly vulnerable to disruption because species dependent on only a few interaction partners could lose all of their partners with only a few primary extinctions. For example, black-footed ferrets (Mustela nigripes) were pushed to the verge of extinction by the decline of prairie dogs (Cynomys spp.), their sole prey [19]. However, we argue that the number of interaction partners a species has is not the only, or necessarily even the most important, component of specialization. A more germane measure is the cumulative risk of extinction of all of the partners. The level of vulnerability to extinction following loss of interaction partners likely depends on the phylogenetic and functional diversity of the assemblage of partners [20], which might or might not be related to the number of taxa the assemblage contains. For example, generalists that interact with numerous related species, all of which are vulnerable to extinction, are themselves susceptible to decline [20]. Conversely, a specialized parasite, such as Columbicola extinctus, might have survived the extinction of one of its two hosts (the passenger pigeon, Ectopistes migratorius) because the other host (band-tailed pigeon, Patagioenas fasciata) is resilient to human impacts [9]. It also seems likely that the evolution of specialized interactions would be accompanied by adoption of bethedging traits to buffer those interactions against loss; this would help explain the long-term persistence of many highly obligate interactions. For instance, the plant Dillenia indica is considered specialized on elephants for seed dispersal, but its hard fruits, available initially only to strong-jawed pachyderms, slowly soften if they are not eaten and become available to successively smaller frugivores [21]. As another example, highly specialized ant– fungus mutualisms have persisted for tens of millions of years and, over this time span, these ant lineages have diversified through periods of massive environmental changes [22]. To better understand the role of specialization in secondary extinction risk, we need more knowledge about how species richness within an assemblage of interaction partners affects the vulnerability of species to interaction disruption. A second critical factor in determining the degree of specialization in an interaction is the functional redundancy within the assemblage of interaction partners. A species could interact with numerous partners (appearing to make it a generalist), but if functional redundancy is low, then it is possible that only one or a few of those partners could be providing ecological or demographic benefits. Such a species could be described as a cryptic specialist. As an example, fruits of the canopy tree Prunus javanica are dispersed by at least 20 vertebrates, but only a small fraction of these

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Review frugivores provide high-quality seed dispersal [23]. Marked differences have also been demonstrated in species impact (sensu [24]) of ant species in their protective services for plants [25] and predators in their efficiency in regulating prey [26]. Indeed, empirical food web studies have long shown that many communities comprise many weak and only a few strong interactions (e.g., [24]). Weakly interacting partners might be incapable of compensating for the loss of strongly interacting ones either due to overall rarity or lower per-capita interaction strength [27]. Improving our understanding of the relation (if any) between diversity and functional redundancy within assemblages of interaction partners should be a top research priority. Accurately assessing interaction dependency Secondary extinction risk depends on whether a particular species has an obligate dependence upon its partners. For most animals, interaction dependency is tightly linked to the degree of dietary specialization (see above). However, many plants interact with mutualists and, while these mutualists might enhance the fitness or abundance of the plant, the plant can in many cases still persist without them [21]. Disruption of pollination or seed dispersal services due to the loss of one partner might have limited effects on plant abundance, even over timescales of centuries, if population growth of the species is driven by vital rates not impacted by the interaction [28,29]. Even normally outcrossing plant species might be able to resort to autonomous self-pollination when pollinators are reduced [3,30], such as when habitat degradation reduces pollinator density [31]. Alternatively, a species would be demographically obligate if unreplaced loss of interaction partners doomed the species to extinction. This is a critical point generally overlooked by the expanding literature on interaction network theory, which is concerned with mapping interactions between species in a community, but seldom includes information about the functional importance of the different interactions. Several species traits in plants allow us to predict the degree to which interactions are demographically obligate. Clonal growth [32,33], the ability to resprout [34], and high adult survival and longevity [35,36] make plants relatively resilient to the disruption of interactions with their animal vectors (although such disruptions might impede population spread). As one example of the relevance of these traits, anthropogenic reduction of pollinator abundance in South Africa has led to reduced orchid diversity, with the order of extinction proceeding from the least to the most clonal species [37]. It is also critical to note that an interaction between a pair of species might be demographically obligate at one location or time but not another. There is substantial year-to-year turnover in interaction networks [38]. Moreover, species frequently shift in distribution, causing interactions among species to occur within temporally and spatially dynamic mosaics [39]; thus, interactions that are necessary for species persistence in some places or times might be facultative in others. Just as spatial and temporal heterogeneity can be key to the coexistence of competitors [40], it might also have a strong buffering role for how species respond to the loss of interaction partners [41]. However, this dynamic context is

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often overlooked in predictions of when interaction loss might lead to extinctions. Understanding trait evolution and novel interaction partners Trait evolution can also buffer species against the loss of interaction partners. For example, several pathways have been proposed by which corals might adapt to the loss of their algal symbionts [42]. In Brazil, functional extinction [43] of frugivorous birds has led to the rapid evolution of reduced seed sizes (facilitating dispersal by smaller extant frugivores), rather than to secondary extinction, of a palm species [5]. Following experimental removal of pollinators, an outcrossing herb, Mimulus guttatus, suffered reduced fitness at first but then evolved increased self-pollination ability within five generations [4] (Figure 2). Over much longer timescales, phylogenetic analyses suggest that evolution of self-pollination is a common response to pollinator limitation [3] or population bottlenecks [30]. Some plants can be pollinated by both wind and insects [44,45]. In other cases, plant lineages originally pollinated by animals can switch to wind pollination in habitats with fewer pollinators [46]. The secondary ‘abandonment’ of traits promoting mutualistic associations with other species is common across phylogenies [7]; many partners in mutualisms are not evolutionary obligate and can ‘escape’ when conditions no longer favor the interaction [7]. While we do not know how many lineages have gone extinct because they were unable to recover from loss of their interactions, these phylogenetic studies do demonstrate that long-term persistence following the loss of interaction partners is common in many taxa. Species can also adapt to the loss of interaction partners by acquiring new ones. Introduced dingoes have replaced the large marsupial carnivores in much of Australia, and can increase biodiversity at lower trophic levels [47,48]. By one estimate, over half of California could be occupied by novel bird assemblages by 2070 [49]; some of the new partnerships that will form seem likely to help prevent secondary extinctions (cf. [50]). Introduced pigs and invasive rats can act as seed dispersers for native plants, replacing lost avian dispersers [6,51]. Exotic birds are now important pollinators of endemic Hawai’ian plants that have lost their original pollinators [52]. Environmental changes or loss of interacting species can drive partner switching [7,53,54] or lead to an increase in the generality of interactions [55]. The rise of synthetic biology also raises the possibility of rescuing extinct alleles or even recreating species [56], including important interaction partners that could help stave off secondary extinctions. However, the issue of functional redundancy is also important in the context of novel interactors. Recolonizing wolves (Canis lupus) can differ markedly from pumas (Puma concolor) or grizzly bears (Ursus arctos) in their impacts on ungulate populations [57]. Seed dispersal by exotic mammals does not support populations of an island shrub in one well-studied case in which the plant had lost its native seed-dispersing lizards [58]. In many cases, members of a guild that all seem to have the same ecological role can differ strongly in their interaction strengths [27], or each provide unique services [23]. Novel partners might also tend to be generalists and, therefore, unable to 3

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Figure 2. Mechanisms that can buffer systems from secondary extinctions. (A) Carnegiea gigantea is pollinated by bats in the southern portion of its range, but expands its pollinator suite to encompass birds and invertebrates in the north where bat presence is unreliable. (B) The fruit of Dillenia indica is typically dispersed by elephants, yet softens and becomes available to smaller dispersers in the absence of elephants. (C) After being experimentally deprived of pollinators, an outcrossing herb, Mimulus guttatus, rapidly evolved increased self-pollination ability. (D) In Hawai’i, the endemic Clermontia parviflora is now pollinated by non-native birds, following extinction of its native mutualists. (E) Extirpation of predators such as Sunda clouded leopard (Neofelis diardi) does not lead to release of ungulate prey when humans regulate populations of ungulates, such as red muntjac (Muntiacus muntjak). Reproduced, with permission from, A. Aslan (A,D), Wikimedia Commons (B), B. Roels (C), and J. Brodie (E).

adequately replace lost specialized interactions [50], although additional research is needed to determine the strength of this pattern. Importantly, evaluations of the species impact of interaction partners (novel or original, native or exotic) generally assume static conditions over time. However, given massive environmental changes and altered selection pressures, it is difficult to assess the strength and stability of new partnerships. Exotic honeybees might provide lower quality pollination services compared with native animals in certain intact habitats [55], for example. However, they are more abundant in degraded areas, particularly in the tropics [59], potentially enhancing plant persistence in human-altered landscapes. Finally, it bears noting that ‘novel’ usually simply refers to interaction partners that have appeared since research began on that organism; except in the most specialized interactions, species have probably associated with a diversity of partners over time [7]. In the face of myriad environmental changes, understanding functional redundancy in guilds of interacting species and assessing whether newly arrived taxa can maintain populations that have lost their native interaction partners are some of our most pressing research needs. 4

The community context of secondary extinction risk Out of necessity, most empirical studies on species interaction disruption have focused on single anthropogenic stressors (e.g., [60]). However, in reality, nearly all ecosystems are subject to multiple human-driven threats, and consideration of this broader context is essential for assessing secondary extinction risk [9,61]. Reduction of risk through interactions with other stressors A largely overlooked point is that, in some cases, loss of interaction partners can be countered by other human impacts on the food web, reducing the likelihood of secondary extinctions. For example, large carnivores have become functionally extinct in many areas, but consequent release of their ungulate prey, which can drastically reduce plant abundance [62] and thereby increase plant extinction risk, seldom occurs [63] because these herbivores are intensely harvested by humans [64]. Indeed, survival rates of elk (Cervus elaphus) in western North America are lower in areas without wolves and pumas because human harvest levels are higher in these areas [57]. However, predator loss could drive secondary extinctions where prey populations are naturally regulated by predation but not harvested or

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Review otherwise negatively affected by humans [65]. The overfishing of marine predators might have contributed to explosions of crown-of-thorns starfish (Acanthaster planci), which is not eaten by humans, and these have led to extinction cascades in coral reefs [66]. Reduction of secondary extinction risk could also occur in mutualistic interactions. Although we know of no evidence for this yet, plants negatively affected by human-induced loss of their pollinators or seed dispersers could potentially be ‘rescued’ if declines in reproduction were offset by enhanced growth or survival via anthropogenic nitrogen deposition or atmospheric CO2 enrichment. It is also possible that climatic and other global changes could increase species resilience to secondary extinctions. Increases in climatic variability can spur the evolution of greater phenotypic plasticity [8], which in turn could help species tolerate the simultaneous threat of loss of their interaction partners. A European herb, Capsella rubella, evolved selfing ability and expanded its range relatively quickly during a period of rapid climatic changes and agricultural development [30], suggesting that abandonment of sexual reproduction does not always limit the performance of species in changing environments. Exacerbation of risk through interactions with other stressors Alternatively, interactions between multiple anthropogenic stressors can alter species interactions [2] in ways that exacerbate secondary extinction risk [9,67]. For example, habitat disturbance can enhance the impact of invasive species on native taxa [67]. However, do such altered interactions necessarily increase secondary extinction risk? Colwell et al. [9] provided several examples of how primary extinctions and other anthropogenic stressors additively increase the probability of secondary extinctions. We note here that such interactions can also be synergistic, when traits that buffer species against declines following the loss of their interaction partners also limit their ability to respond to other human impacts. For example, some plants can respond to pollinator loss by facultatively or evolutionarily resorting to self-pollination. However, the abandonment of sexual reproduction can reduce genetic variability and offspring fitness [68], which can limit the capability of species to evolve to new conditions [32], such as those created by climate change. When historically outcrossing species suddenly have to resort to selfing, they often experience inbreeding depression [69]. Furthermore, inbreeding effects might be stronger in more stressful conditions, such as at the edge of the distribution of a species [70,71]. Consequently, species that are negatively affected by humans both directly (e.g., by climate change) and via the loss of interaction partners could face substantially elevated extinction risk. While numerous plants experience direct impacts from climate change [72], extinction risk might be particularly severe for species that have lost their native pollinators (cf. [52]) or for those that respond phenologically to climate change and, thus, become temporally mismatched to their pollinators [13]. Moreover, direct human threats such as habitat loss might increase the susceptibility of a population to the loss of interaction partners by reducing abundance

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and, thus, genetic variability and capacity for evolutionary rescue [73,74], in essence creating a ‘secondary extinction vortex’. The effects of multiple human impacts on secondary extinction risk are critical to understand, but remain difficult to predict. Concluding remarks Secondary extinctions are often difficult to detect, but they are occurring (Box 1), and their likelihood can be enhanced by multiple anthropogenic stressors. Moreover, secondary endangerment and secondary extinction debts in diverse systems suggest that the loss of interaction partners is a key factor affecting the persistence of many species. We suggest that secondary extinction risk can be predicted from a relatively few ecological attributes of the interacting species and their communities, although accurately measuring these attributes might not be straightforward in some systems. In general, understanding how, when, and where secondary extinctions unfold given the presence of numerous ecological and eco-evolutionary buffering mechanisms remains critical and warrants further investigation. An important consideration, and not one that has been well developed in the literature, is distinguishing which Box 1. Evidence for secondary extinctions Past and ongoing secondary extinctions are difficult to quantify; many might have gone un-noticed, while in other cases, secondary extinctions might be inevitable but simply have not happened yet (secondary extinction debt). Extinction risk could be strong in understudied taxa that critically depend on specialized interaction partners [61], such as parasites that have lost their hosts and specialist predators deprived of their prey (reviewed recently in [9]). One well-documented case involves the extinction of the moa birds of New Zealand, which led to the loss of several of their internal parasite species [75]. Secondary extinctions have perhaps received the most attention in disrupted mutualisms. Although loss of pollinators [76,77] or seed dispersers [60,78–81], can clearly impact plant populations, we have only a rudimentary understanding of how often these effects are strong enough to drive plant extinction. Loss of avian seed dispersers in New Zealand led to a 55% reduction in juvenile shrub abundance but not extinction [82], and removal of seed-dispersing vertebrates elsewhere has generated shifts in species composition of tree seedlings and saplings from those with animal dispersal to those dispersed abiotically [79,80,83]. However, it is not well known whether disperser loss ultimately affects adult plant abundance or long-term community diversity. Indeed, Harrison et al. [80] recently found similar population growth rates in large-seeded tropical trees, whose seed-dispersing animals had been extirpated through overhunting, and small-seeded species whose seed dispersers have likely persisted. Impacts of disrupting interactions also vary in space and time [84]. Secondary extinctions can also occur in antagonistic interactions across trophic levels. Human impacts on top predators can indirectly trigger reductions in abundance at lower trophic levels via the release of herbivores [85] or mesopredators [65]. Yet, the substantial literature on this topic has focused on altered ‘performance’ following predator loss; there are few examples of actual extinction at lower trophic levels driven by trophic cascades [85]. This could be partly a sampling issue, because detecting signals of altered trophic cascades can be difficult within the complexity of natural ecosystems [86]. Yet, that same complexity can also attenuate impacts from one trophic level to the next. For instance, despite initial evidence that wolf extirpation in Yellowstone (USA) had indirectly hindered the recruitment of woody shrubs, such indirect effects of predation, are now thought likely to be weak relative to climatic controls over ungulate herbivory [87,88]. 5

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Figure 3. Types of secondary extinction, where gray arrows show the direction of demographic impacts among interacting species. In co-extinctions, direct impacts on species A lead to its extirpation, which in turn causes the secondary loss of species B (broken black arrow). In extinction cascades, the secondary extinction(s) can also occur farther along the food chain (species C through n; unbroken black arrow). Multiple human impacts generally occur concurrently, affecting species (red arrows) and modifying the interactions between them (yellow arrows). The direction and strength of all of these impacts cumulatively will determine whether secondary extinctions occur.

anthropogenic threats are likely to have additive versus synergistic effects on secondary extinction risk. As an example, for species that are highly specialized to utilize only one interaction partner, habitat disturbance might be expected to impact both of the interacting partners. Therefore, there could be additive effects of both habitat degradation and interaction disruption for the target species. There could also be synergistic interactions if the habitat degradation increased demographic reliance on the interaction, thereby exacerbating the impacts of interaction disruption. With other anthropogenic threats, such as hunting and seed dispersal disruption, the habitat quality would remain unaltered but the interaction could be severely compromised. Identifying which types of perturbation

might lead to secondary extinctions more than others, and when multiple effects might be synergistic as opposed to additive, would be key steps forward. The conceptual model presented here suggests that secondary extinction risk is highest in the presence of multiple types of anthropogenic threat. Plants deprived of vertebrate-mediated seed dispersal or exposed to elevated herbivory via loss of top carnivores are most likely to go extinct when they are also subject to habitat loss or temperature increases. Therefore, in many cases, it will be the synergistic interactions among stressors that determine secondary extinction risk, rather than the magnitude of any single stressor. In these cases, multiple impacts act as another exogenous factor, pushing the vulnerability threshold lower by increasing the risk of secondary extinctions at each given level of specialization, evolutionary rate, and dependence. In other cases these impacts can offset each other, ameliorating secondary extinction risk. The prevailing outcome will depend on the strength and direction of all human impacts cumulatively (Figure 3). This broader context of multiple threats to multiple species is often ignored in reductionist ecological studies but will prove crucial to understanding the fate of global biodiversity. We appreciate that nonreductionist experiments are often logistically difficult. In Box 2, we present a series of feasible research questions that, if answered, would provide important bigger-picture information on secondary extinctions in nature. Ameliorating the impacts of loss of interaction partners could prove an important tool for reducing extinction risk in numerous species, and assessing and accounting for secondary extinctions in science and conservation planning is well warranted. In Box 3, we present tactics by which secondary extinction risk can be incorporated into conservation planning to help ameliorate the additional risk posed by loss of interaction partners to species that are already stressed by direct human impacts. As we have

Box 2. Future directions for research Research along several fronts would help us better understand, and potentially stave off, secondary extinctions. We particularly need to know:  Are there critical thresholds in abundance below which species no longer interact significantly with others in the community? Such ‘functional extinction’ [43] might be more prevalent than outright extinction; how often will it cause secondary extinctions? Could functional extinction thresholds be incorporated into population viability analysis?  Which types of threat interact synergistically and positively (exacerbating each other) versus negatively (offsetting each other) to influence secondary extinction risk?  Which interaction partners can be lost with minimal impact, as opposed to those whose loss would precipitate secondary extinctions?  When is loss of diversity among the interaction partners of a species likely to induce extinction? This depends critically on determining how common functional redundancy is in assemblages of interaction partners. Under what conditions does the amount of functional redundancy increase or decrease as the distributions and population dynamics of species change? How do interaction guilds rearrange in response to loss of individual guild members, and what are the consequences for the shared partner? 6

 Are specialized (or cryptically specialized) interactions less likely to be replaced by novel partners when disrupted, or less able to evolve novel traits to avoid species decline following partner loss?  Beyond those listed in the main text, what traits affect the relative vulnerability to secondary extinctions across species and ecosystems? This could be addressed using data from the Center for Tropical Forest Science network of large-scale forest plots around the world (http://www.ctfs.si.edu/) with long-term demographic data for thousands of species subject to myriad environmental changes.  How common are secondary extinction debts in altered communities, and to what extent are they reversible?  How common and rapid are evolutionary responses to loss of different types of interaction partner? For which interactions is novel trait evolution likely to have an important role in reducing secondary extinctions?  How do we balance the potential risks of secondary extinction against the risks associated with taxon substitution or maintenance of non-native interactors?  What potential does synthetic biology have to restore important interactors that have been lost? Are there some species or traits that are particularly important to restore ecologically, such as extinct species that might have had important interaction roles? How will recreated species interact with existing organisms, ecosystems, and human societies?

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Box 3. Conservation planning for secondary extinctions Secondary extinctions are rarely explicitly addressed in conservation planning or discussed by government agencies and nongovernmental organizations in the planning process. We can facilitate greater consideration of secondary extinctions in conservation plans by: (i) Re-emphasizing species-level conservation for taxa that provide consistently strong demographic benefits for other species (e.g., large-bodied frugivores that disperse plant seeds), and the ecological processes critical to their interactions (e.g., seed dispersal), in conservation planning [89]. While some planning approaches emphasize conservation of vegetation communities or physical land units rather than particular species [90,91], increased efforts to incorporate ecological processes such as pollination into conservation planning [92] could help species strongly dependent on species interactions. (ii) Actively managing species in places or conditions where we know or strongly suspect that their loss would incur secondary extinctions. Special attention must be paid to the source of resiliency; if entire guilds are threatened and no other taxa can take over the role of that guild, conservation biologists should pay special attention to that group. For example, many tropical trees depend on vertebrate seed dispersers for regeneration, and those frugivores depend on fruit resources. Thus, long-overhunted forests might require special protection, and sometimes

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