Magnitude of positive impacts

The 5 scenarios used in EICAT+ to assign alien taxa to impact categories structurally resemble those reported in EICAT (Table 1 and Fig 1).

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Table 1. Scenarios used in EICAT and EICAT+ to assign alien taxa to impact categories.

Detailed description of the 5 semiquantitative scenarios used in EICAT [24] and EICAT+ to assess negative and positive impacts caused by alien taxa on native taxa at different levels of organization. The scenarios are used in EICAT and EICAT+ to assign alien taxa to one of 5 ascending categories of impact magnitude. Note that when there is no or inadequate information to classify an alien taxon to one of the 5 impact categories, the taxon should be classified as Data Deficient (DD).

https://doi.org/10.1371/journal.pbio.3001729.t001

The first EICAT+ scenario, Minimal positive impact (ML+), describes negligible increases in the individual performance of native taxa. Minimal positive impacts describe cases in which the alien and native interact through one of the mechanisms that can potentially lead to a positive impact (Fig 3), but no increase in performance (or higher-level impact) has been detected. This may occur when alien taxa simply fulfill the same functional role of other taxa without increasing the performance of native individuals [35]. For instance, alien plants can provide pollen and nectar to native pollinators [42,62,63], or alien fish can become a food source for native predatory fish [64,65], but there is no detectable evidence that these interactions improve the survival, growth, or body size of the native consumers. Note that taxa classified as Minimal positive under EICAT+ should not be confused with those classified as Data Deficient (DD), i.e., when no information is available to measure an impact or there are methodological issues with the evidence available such that it is not sufficiently reliable to classify the positive impact magnitude (see dedicated paragraph below). Note also that taxa classified as Minimal positive under EICAT+ should also not be confused with those classified as Minimal Concern under EICAT, i.e., when the alien and native taxa interact through one of the mechanisms that can lead to a negative impact (e.g., competition; Fig 3), but no decrease in the performance of the native taxa has been detected (Table 1 and Fig 1).

The second EICAT+ scenario, Minor positive impacts (MN+), describes increases in the performance of native individuals caused by alien taxa (Table 1 and Fig 1), such as increases in rates of growth, fecundity, photosynthesis, or hunting success of the native organisms, but no increase in the population size of the native taxon, due to the alien taxon, is detected. Examples of MN+ impacts include the following: an alien plant increasing the growth rate of a native plant (here the taxon of interest) through the production of allelochemicals suppressing pathogenic fungi [66]; an alien plant improving the hunting success of native spiders by providing foraging habitats [67]; an alien fish decreasing the abundance of a competitively dominant native fish, thus indirectly increasing the juvenile growth rate of competitively subordinate native fish [68] (here the entity of interest); or an alien plant increasing pollen availability in a native plant by attracting pollinators to the location (magnet species effect), thus increasing the reproductive success of the native plant [69].

The third EICAT+ scenario, Moderate positive impacts (MO+), describes cases in which an alien taxon increases the population size of at least 1 native taxon (or prevents/mitigates an ongoing population decline) (Table 1 and Fig 1). MO+ examples include the following: increases in the abundance of native frugivorous birds due to the provision of fleshy fruits from alien shrubs [70]; increases in the abundance of a native mayfly due to epibiosis on the surface of an alien bivalve [71]; increases in the abundance of mussels due to enhanced recruitment and survival caused by an alien green alga through the creation of a novel microhabitat on breakwaters [72]; or increases in the abundance of multiple native ground-dwelling invertebrates from different feeding guilds in the litter under alien plants [73].

The fourth and fifth EICAT+ scenarios, Major positive impacts (MR+) and Massive positive impacts (MV+), respectively, refer to increases in species occupancy of at least 1 native taxon through local reestablishment of native populations (or extinction prevention; see Supporting information C in S1 File) within their native ranges (Table 1 and Fig 1). Alien taxa may contribute to native taxa reestablishment that could not have occurred in their absence. To be considered in EICAT+, such reestablishment may occur via natural colonization or reintroduction by humans (either accidental or deliberate). Reintroductions that lead to reestablishment will be considered in EICAT+ only if no additional conservation effort to reintroduce native individuals has been made since the introduction of the alien taxon, i.e., if reintroductions occurred at rates similar to those before the alien was introduced [24] and if there is a clear evidence that reestablishment would not be successful in the absence of the alien taxon (i.e., any extra conservation effort to recolonize would be necessary but not sufficient). Impacts are not classified in EICAT+ when an alien taxon renders areas outside the native range of the native taxon suitable to the latter, e.g., when the alien would allow a species to expand beyond its range (a so-called “neonative” [74]; Supporting information A in S1 File). The distinction between Major and Massive impacts for EICAT+ is in their reversibility. When evidence indicates that the reestablished native population, or the native population whose extinction was prevented, would go extinct if the alien taxon was no longer present, the positive impact is only transient and would be classified as Major (MR+). If the reestablished native population, or the native population whose extinction was prevented, would persist even if the alien taxon was no longer present, the positive impact is long lasting and would be classified as Massive (MV+). Because all populations go extinct eventually and population trajectories can only be reliably forecasted for the near future, positive impacts are classified as Massive only if the reestablished native population, or the native population whose extinction was prevented, would persist for at least 10 years or 3 generations (whichever is longer) after the disappearance/removal of the alien taxon. Such practical time intervals are analogous to the intervals chosen in EICAT to judge the reversibility of local extinctions caused by the alien and distinguish between Major and Massive negative impacts [24].

Conceptual examples of Major positive impacts promoted by an alien taxon through local reestablishment or extinction prevention can be found in Fig 2. Cases reported in the literature are as follows: the return of a native bird into areas within its native range from which it temporarily disappeared and where the bird now uses fledging sites provided by an alien plant [75] or the reestablishment of native plants caused by changes to the chemical, physical, and structural soil properties caused by an alien tree [51]. Additionally, alien taxa might prevent the extinction of native populations that were observed to be in decline before the introduction of the alien taxon. MR+ examples in which alien taxa might have prevented the extinction of native species include the following: the provision of roosting sites by an alien tree to a native butterfly that lost its historical roosting sites due to logging and habitat alteration [62]; the provision of refugia by an alien plant to 3 critically endangered and protected native snails suffering from alien rat predation [50]; or the mutualism established by alien zooxanthellae with bleached native corals, thus preventing the disappearance of photosynthetic corals under climate change–induced thermal stress [76,77].

Massive positive impacts (MV+) can be caused by the demographic rescue effect (i.e., populations persist due to a boost in population size [78]) that an alien producer might have on the population of a native consumer previously trapped in an extinction vortex. Other real-world examples can include the following: the long-lasting impact that an alien biocontrol beetle had on a declining endemic plant by eradicating an alien scale pest [79,80]; and the genetic or evolutionary rescue induced by alien individuals on native populations through hybridization [81,82]. In these examples, the positive impacts of the alien taxa on the native populations would persist even if the alien taxa are removed or disappear naturally from the area.

Note that as in EICAT, if there is no or inadequate information to classify an alien taxon to one of the 5 categories of impact magnitude, the taxon should be classified as DD [24,25]. As a consequence, studies reporting mechanisms by which an alien taxon may cause positive impacts on native taxa, but that do not measure, or provide information on, changes in biodiversity attributes relevant to EICAT+ (e.g., performance of individuals), do not contribute information that would allow an impact to be scored, implying a DD classification. However, we strongly recommend that when available such information still be reported (e.g., in supplementary materials), to document research gaps which might inspire future studies around positive impacts of alien species (see Supporting information E in S1 File).

Analogous to EICAT, EICAT+ assigns confidence scores (high, medium, low) to each impact record depending on how confident the assessor is that the assigned impact magnitude reflects the true situation [25,83]. A general discussion about why and how to account for uncertainty when assessing alien species impacts can be found in Probert and colleagues [83], while more detailed explanations of how to assign confidence can be found in the Supporting information F in S1 File.

Mechanisms of positive impacts

The mechanisms through which alien taxa increase native biodiversity attributes are grouped similarly to the mechanisms described in EICAT [24,25], facilitating high consistency and comparability between both assessment schemes. Note that not all mechanisms that occur in EICAT also exist in EICAT+; positive impacts may also be caused through facilitative interactions [35,37,39,84,85] that have no negative equivalent in EICAT. In Fig 3, we provide a list of mechanisms (and submechanisms) describing all interactions through which an alien taxon (A) can positively impact a native taxon (N). The alien taxon itself can either be positively (mutualistic interactions; N+/A+), negatively (antagonistic interaction N+/A−), or neutrally (commensalistic interactions; N+/A0) impacted by such interactions. Additional details around the rationale behind the formulation of the EICAT+ mechanisms and submechanisms can be found in Fig 3 and Supporting information G in S1 File. Real-world examples of positive impacts caused by alien taxa through different EICAT+ mechanisms and submechanisms can be found in the Supporting information D and E in S1 File.

EICAT+ helps to forecast unwanted consequences of alien taxa control

Alien taxa are often ranked in priority lists according to the degree to which they harm certain entities of interest such as species or ecosystems. Such lists can be used to inform which species should be prevented, contained, or eradicated and how management efforts should be allocated to mitigate deleterious impacts [87]. Often, however, taxa that are prioritized for management because of their negative impacts, and which might be perceived as unwanted, also cause positive impacts, which might be perceived as favorable (Fig 1) (see also Milanović and colleagues [88]). For instance, in a review of impacts by alien marine taxa on biodiversity and ecosystem services, out of 87 high-impact taxa, only 17 had exclusively negative and 7 exclusively positive impacts, whereas 63 had both negative and positive impacts [5]. High-impact taxa can also have negative effects on biodiversity within 1 trophic level, e.g., through antagonistic interactions (competition and predation), but positive effects on higher trophic levels, e.g., through habitat and food provisioning [89,90] or predator release [91]. Given such multidirectional impacts, the EICAT+ assessment will have practical utility (especially when used in combination with EICAT) for managers, policymakers, and the public, as it allows forecasting whether, and how, alien taxa management may yield unwanted consequences for native biodiversity [47]. For example, the eradication of alien cats (Felis catus) on Macquarie Island in the South Pacific to lessen their predation pressure on native seabirds led to an increase in the abundance of alien rabbits (Oryctolagus cuniculus) and, consequently, caused the local disappearance of native large-leaved herbs and grasses [92]. Similarly, the removal of alien trees, Casuarina spp., on the Japanese Ogasawara Islands led to the local disappearance of endangered snail species that found refugia from predatory alien rats (Rattus rattus) in the Casuarina litter [50]. In both cases, it would have been useful to promptly report and systematically assess indirect positive impacts caused by the target species so that countermeasures could have been implemented to avoid or mitigate undesirable outcomes.

More generally, an EICAT+ assessment will provide stakeholders (including managers, policymakers, and the public) with evidence-based information that can guide the implementation of adequate countermeasures and avoid or minimize undesirable outcomes in 2 principal ways. First, the benefits of removing a certain deleterious alien species can be compared to the costs that the removal imposes on other native species [49,54,93,94]. The necessity of conducting such a cost–benefit analysis has been recently stressed by Rees and colleagues [95], who suggested that the choice of removing dingoes (Canis lupus dingo) in some parts of Australia should be assessed case by case, as these apex predators increase the abundance of native small mammal species and a native owl species by suppressing 2 alien mesopredators (Vulpes vulpes and F. catus). Similar considerations have been made by Gomes and colleagues [96], who noted the need for careful evaluation of management decisions regarding alien jackfruit trees (Artocarpus heterophyllus) in a secondary forest of Brazil, where these plants contribute to the maintenance of frugivore populations and promote seed rain and seedlings of native plants. Second, the identification of alien taxa that mitigate the harmful impacts of other alien taxa can be used to design adaptive management strategies with a specific removal order. In the above examples, the removal of alien cats and Casuarina trees should be preceded by, or carried out in tandem with, the removal of alien rabbits [92] and rats [50], respectively. Mapping alien–alien antagonistic interactions and their effect on native taxa has been proven to be useful in several cases, for instance, in designing an adaptive eradication program for alien rats on a tropical Pacific island [97]. Here, since data from different trophic levels showed that the rats competed with alien mice and consumed an alien plant species, rats and mice were removed simultaneously and only after the alien plant eradication, so that unwanted cascading effects on the insular ecosystem could be prevented.

EICAT+ helps to assess functional restoration and biological control

Only a subset of alien animals, plants, and microorganisms cause severe harmful impacts on biodiversity [7,98], and while many alien taxa are inconsequential, some might even facilitate restoration. Many populations have disappeared, or are currently heading toward extinction, within their native range as a consequence of various anthropogenic stressors such as climate change, alien taxa, pollution, habitat loss, and habitat degradation [99,100]. Certain species have been deliberately introduced to restore lost ecological functions, while others have been tolerated due to their capacity to counterbalance or mitigate environmental stressors or disturbance. Examples are as follows: an alien tortoise species (Aldabrachelys gigantea) introduced to the Mascarene Islands east of Madagascar to restore seed-dispersal functions of recently extinct species promoted seedling patches of endangered trees through endozoochory [101]; males from a subspecies of boobook owl (Ninox novaeseelandiae novaeseelandiae) introduced to Norfolk Island rescued another subspecies of boobook owl from extinction [82]; or an alien oyster (Crassostrea gigas) increased water clarity, provided substrate and shelter, and acted as a food source for native species in deteriorated and heavily modified ecosystems in the Netherlands [102]. In addition, the use of alien taxa as classical biological control agents to limit or suppress introduced weeds and pests and protect native biodiversity has been carried out on multiple occasions [55,103]. For instance, an alien predatory lady beetle (Hyperaspis pantherine) was used in successful biological control of an alien scale insect on St. Helena Island in the South Atlantic, thus preventing the extinction of a native endemic gumwood tree [80]. Analogously, the introduction of an alien weevil (Cyrtobagous salviniae) has been advocated to suppress an alien floating aquatic fern and, therefore, to promote the recovery of native aquatic algae and macroinvertebrates in South Africa [104]. Each biocontrol release requires extensive research on host specificity, a comprehensive evaluation of potential and actual impacts, and post-release monitoring to track the impacts (both positive and negative) [105]. EICAT+ promises to be a powerful and transparent means to quantify to what degree restoration and biocontrol programs based on alien species offer positive outcomes to native biodiversity conservation. Quantifying positive impacts will be instrumental in indicating which of these management programs should be maintained or enhanced and on the contrary, which should be revised or even avoided in the future. Alien taxa used in restoration and biocontrol that score high with EICAT+ (i.e., having positive impacts at the population level that can be classified as Moderate, or higher), and without relevant negative impacts, could also be subjected to specific conservation actions (for instance, see the mitigation strategies proposed to reduce the effects of climate change on rewilded populations of tortoises [106]), so that their positive impacts on native biodiversity are maintained in the future.

EICAT+ facilitates the distinction between real and unproven positive impacts

As opposed to negative impacts, positive impacts of alien species are claimed to often be described only anecdotally or not rigorously [20,107]. In many cases, the literature describes the existence of mechanisms by which alien taxa might cause positive impacts, for instance, by acting as a food source for native taxa [108,109], but fails (or avoids) measuring the actual consequences they have on native taxa (Supporting information E in S1 File). EICAT+ identifies such information gaps and flags the need to explicitly measure relevant biodiversity attributes (e.g., population size) so that inconsequential impacts (e.g., Minimal positive) and relevant, but currently unreported impacts (e.g., Minor positive, or higher), can be distinguished. A lack of in-depth knowledge may result in positive impacts being overlooked, and also in the erroneous classification of negative impacts as positive. For example, laboratory trials and field surveys showed that a native trout species readily consumed an alien New Zealand snail species in North America, although individuals feeding upon alien snails had lower growth and body condition than those which did not consume any alien snails [110]. Similarly, multiple native butterflies lay their eggs on alien plants in the US, although their larvae rapidly die because of the toxicity of the plants [58]. Although at first glance the impacts above seemed positive, they turned out to have negative consequences for native taxa due to eco-evolutionary traps, i.e., maladaptive responses made regardless of the availability of better options [111,112]. These examples indicate that positive impacts should not be automatically inferred from the mechanisms—as the latter could underlie negative impacts that can be assessed under EICAT, not EICAT+. Therefore, EICAT+ can be a useful guide to identify true positive impacts.

EICAT+ is not a framework to assess value-laden beneficial impacts and should not be used to offset or understate negative impacts

While it may be tempting to discount negative EICAT with positive EICAT+ scores for an alien taxon in an attempt to “offset” negative impacts with positive ones, this would be simplistic and even misleading for management decisions. Positive impacts assessed under EICAT+ should not be confused with beneficial impacts, i.e., impacts that are perceived as favorable or desirable in accordance with certain values and motivations (Box 1). Indeed, a large part of the positive impacts assessed under EICAT+ can be seen by some as harmful, for instance, by those who consider all changes caused by an alien taxon to the recipient ecosystem as unwanted alterations of its state. Under this conservation standpoint, an alien shrub species that simultaneously decreases and increases the population size in a native grass species and in a native bird species, respectively (as in Fig 1), would be considered harmful in both cases. Moreover, many positive impacts caused by alien taxa on native taxa can have cascading harmful effects on protected native taxa or human communities. For instance, local reestablishment of a native predatory bird favored by an alien taxon might put additional pressures on endangered native prey species, while increases in the abundance of a dominant native grass species might threaten rare subordinate species. Increases in the population size of a native weed species can hamper agricultural productivity or lead to acute allergic reactions, while deleterious consequences for human well-being can also be expected when native pests, such as wild boar, mosquitoes, or bark beetles, become more abundant. In the above examples, EICAT+ would assess the positive impacts of alien taxa on the native predatory bird, grass, weed, or pest species with value-free criteria, i.e., without evaluating whether such impacts are favorable or unfavorable from a certain perspective or for different stakeholders [8]. Such evaluation can be undertaken at a later stage by weighting or selecting EICAT+ data in accordance with specific values, motivations, or perceptions [113]. For instance, the conceptual framework proposed by Kumschick and colleagues [9], which combines objectively measured impacts with their importance for affected stakeholders, was developed to produce weighted impact scores and facilitate prioritization. Value-weighted scores can also help to identify societal or nature conservation conflicts associated with alien taxa [114,115] and inform risk analysis [31] or management decisions [8,116]. Future research should explore ways to link people’s perceptions with impact assessments generated under both EICAT and EICAT+, so that changes caused by alien taxa can be understood in their full complexity.