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The EICAT+ framework enables classification of positive impacts of alien taxa on native biodiversity [1]

['Giovanni Vimercati', 'Department Of Biology', 'University Of Fribourg', 'Fribourg', 'Anna F. Probert', 'Lara Volery', 'Ruben Bernardo-Madrid', 'Department Of Integrated Biology', 'Estación Biológica De Doñana', 'Ebd']

Date: 2022-08 

Species introduced through human-related activities beyond their native range, termed alien species, have various impacts worldwide. The IUCN Environmental Impact Classification for Alien Taxa (EICAT) is a global standard to assess negative impacts of alien species on native biodiversity. Alien species can also positively affect biodiversity (for instance, through food and habitat provisioning or dispersal facilitation) but there is currently no standardized and evidence-based system to classify positive impacts. We fill this gap by proposing EICAT+, which uses 5 semiquantitative scenarios to categorize the magnitude of positive impacts, and describes underlying mechanisms. EICAT+ can be applied to all alien taxa at different spatial and organizational scales. The application of EICAT+ expands our understanding of the consequences of biological invasions and can inform conservation decisions.

Funding: This research was funded through the 2017–2018 Belmont Forum and BIODIVERSA joint call for research proposals, under the BiodivScen ERANet COFUND program, through the InvasiBES ( http://elabs.ebd.csic.es/web/invasibes ) and AlienScenarios ( https://alien-scenarios.org/ ) projects, with the funding organisations: Spanish State Research Agency (MCI/AEI/FEDER, UE, PCI2018-092939 and PCI2018-092986 to RBM, VC, BG and MV), Swiss National Science Foundation (SNSF grant numbers 31003A_179491 and 31BD30_184114 to GV, AFP, LV, and SBa), Austrian Fonds zur Förderung der Wissenschaftlichen Forschung (FWF project no I 4011-B32 to FE), German Bundesministerium für Bildung und Forschung (BMBF, 16LC1803A to JMJ and W-CS, and 01LC1807C to IK), French National Research Agency (ANR, ANR-18-EBI4-0001-06 to LG and MCG) and the US National Science Foundation (ICER-1852060 to CS). RBM was also supported by MICINN through the European Regional Development Fund (SUMHAL, LIFEWATCH-2019-09-CSIC-13, POPE 2014-2020). JRUW and SKu thank the South African Department of Forestry, Fisheries and the Environment (DFFE) for funding noting that this publication does not necessarily represent the views or opinions of DFFE or its employees. SKu also thanks the DSI-NRF Centre of Excellence for Invasion Biology for funding. TE acknowledges funding from the Alexander von Humboldt Foundation. CH was supported by the National Research Foundation of South Africa (NRF grant 89967), the Australian Research Council Discovery Project (DP200101680) and the Natural Environment Research Council (through the UK CEH project “GLiTRS”, NE/V007548/1). SKa was supported by the Hellenic Foundation for Research and Innovation (H.F.R.I.) - Project Number: HFRI-FM17-1597 (“ALAS”; ‘ALiens in the Aegean—a Sea under siege’). PP and JP were supported by EXPRO grant no. 19-28807X (Czech Science Foundation), project “DivLand” (SS02030018; Technology Agency of the Czech Republic) and long-term research development project RVO 67985939 (Czech Academy of Sciences). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

To fill this current gap, in this Consensus View, we propose a framework for assessing the degree to which alien taxa positively affect native biodiversity: the positive Environmental Impact Classification for Alien Taxa, or EICAT+. The framework structurally resembles EICAT, using 5 semiquantitative scenarios to describe the magnitude of observed positive impacts of alien taxa on native biodiversity attributes (specifically, increases in individual performance, population size, and area of occupancy). In EICAT+, the highest levels of impact magnitude are assigned to alien taxa increasing the area of occupancy of native taxa through local population reestablishment or preventing local extinction. The framework also describes the underlying impact mechanisms by which alien taxa can increase native biodiversity attributes, such as through food and habitat provision, dispersal facilitation, or disease reduction. To illustrate the functionality and utility of the proposed framework, we apply EICAT+ to case studies reporting positive impacts of alien taxa on native biodiversity across different taxonomic groups and ecosystems. Advantages and applications, as well as limits and potential misuses of the scheme, are also discussed.

The assessment of positive environmental impacts can clarify the degree to which already established alien populations mitigate adverse effects of other global anthropogenic stressors, such as habitat loss and alteration [ 51 ] or climate change and pollution [ 52 ], on native taxa and ecosystem functioning. This seems particularly important for alien taxa that have been intentionally introduced to restore ecological functions [ 53 , 54 ] or to act as biological control agents against native or alien pests [ 55 ]. Similar considerations can be made for thermophilic alien species securing ecological functions that would have been lost otherwise due to sea warming–induced declines or extinctions of key native species, as, for example, in the eastern Mediterranean Sea [ 56 , 57 ].

Improving the understanding of the positive impacts that an alien taxon causes on native biodiversity attributes can help to identify possible undesired effects that its removal might have on native communities [ 47 ]. For instance, the removal of aliens may release herbivorous pests or meso-predators controlled by alien predators [ 48 ], decrease the density of predators feeding on alien preys [ 49 ], or reduce the availability of predator-free refugia provided by an alien plant and exploited by endangered species [ 50 ].

The assessment of positive impacts of alien taxa on native biodiversity attributes can improve the understanding of transient and stable interactions between native and alien taxa [ 39 ]. Better understanding of multidirectional changes induced by alien taxa will shed light on how such interactions affect ecological and ecosystem dynamics [ 40 ], and provide valuable insights for adaptive management. For instance, the use of a common scheme to compare the outcomes of novel mutualistic interactions between alien and native taxa—e.g., the interaction between an alien plant and native arbuscular fungi [ 41 ], or between alien plants and native pollinators [ 42 ]—can help to identify which native taxa facilitate the establishment, or hamper the removal, of certain alien taxa. Similarly, a systematic assessment of the antagonistic interactions between alien taxa and their native consumers can help to identify which native species promote biotic resistance against established alien taxa [ 43 , 44 ] and might also be used in biological control [ 45 , 46 ].

Identifying which (and how) alien taxa decrease certain native biodiversity attributes does not fully capture the multifaceted environmental changes induced by the introduction of alien species; in particular, such attributes can also increase. For instance, an alien taxon may increase the performance of individuals or the size of a population of a native taxon by providing additional trophic resources or creating novel habitats that are suitable for the native taxon [ 5 , 35 – 37 ] ( Fig 1 ). Clear and transparent evaluation of all impacts, negative and positive, on native taxa will help to achieve a better understanding of the dynamics and mechanisms of impacts. Such increased understanding would benefit scientists, managers, policymakers, and the general public; for example, it may enable the identification of societal or nature conservation conflicts associated with alien taxa and provide an objective evidence base to underpin discussions and debates [ 16 , 38 ]. The identification of conflicts between different conservation targets is particularly important when alien taxa harm certain native taxa while benefiting others, enabling robust and appropriate management interventions to reach conservation goals. We see 3 main reasons for developing a framework compatible with EICAT that assesses positive environmental impacts [ 8 ]:

Conceptual scheme for the 5 semiquantitative scenarios used in EICAT and EICAT+ to assess negative impacts (on the left) and positive impacts (on the right) caused by a focal alien taxon (here, a shrub species) on native taxa of interest (a grass species and a bird species). Black arrows indicate the introduction and establishment of the alien taxon into a recipient ecosystem. The blue arrow indicates the reestablishment or extinction prevention of a native taxon due to an alien taxon (see also Fig 2 ). Shaded red figures indicate locations unoccupied by the native taxon (e.g., because of local extinctions in EICAT). Symbols were courtesy of the Integration and Application Network, University of Maryland Center for Environmental Science ( ian.umces.edu/media-library ).

The International Union for Conservation of Nature (IUCN) Environmental Impact Classification for Alien Taxa (EICAT) framework was developed to categorize and assess negative impacts caused by alien taxa to native biodiversity at different levels of organization [ 10 , 23 – 26 ] (i.e., decreases in performance of individuals, population size, and area of occupancy through local population extinction). EICAT relies on the premise that the biogeographic origin of species matters in conservation. A clear distinction between native and alien taxa is justified by multiple conceptual and practical arguments associated with, for example, coevolutionary histories, ecological functions, or human responsibilities for nature [ 11 , 27 , 28 ]. Accordingly, EICAT entities of interest are native taxa, whose attributes recorded prior to the introduction or in the absence of an alien taxon are used as a baseline to assess impacts ( Fig 1 ). Changes caused by alien taxa to abiotic ecosystem attributes, such as soil nitrogen content or water chemistry, are considered under the EICAT framework only if such changes lead to a decrease in attributes of native biodiversity. EICAT has been used to compare impact magnitudes of alien taxa across geographic regions and taxonomic groups [ 26 , 29 – 30 ] and to support evidence-based prioritization and other management decisions [ 31 – 33 ]. EICAT is conceptually and structurally related to the IUCN Red List of Threatened Species, with the Red List categorizing a focal native species based on its risk of extinction, and EICAT categorizing a focal alien taxon based on the degree to which it has negatively impacted native taxa [ 34 ].

Considerable effort has been devoted to study the direction, magnitude, and mechanisms underlying impacts of alien taxa on ecosystems [ 3 , 6 ]. This effort has been driven primarily by the urgent need to limit the harm that certain alien taxa cause to various entities of interest within recipient ecosystems, such as native species or habitats [ 7 , 8 ] (Supporting information A and B in S1 File ). Various cultural value systems and motivations, however, determine which entities we are interested in, whether negative or positive changes in biodiversity attributes are perceived as harmful or beneficial [ 4 , 8 , 9 ] ( Box 1 , Supporting information B in S1 File ), and, consequently, how alien taxa should be managed (Supporting information B in S1 File ). Some people might want to primarily protect taxa in their native range [ 10 , 11 ], rescue range-contracting taxa through translocations [ 12 ], uphold ecosystem functions [ 13 ] or improve biodiversity indicators regardless of species origin [ 14 ]. Others will evaluate conservation actions in terms of the suffering caused, e.g., to sentient taxa [ 15 ], rather than in utilitarian terms [ 16 ]. Alien taxa can therefore be opposed, tolerated, or even promoted as a function of specific environmental and sociocultural contexts (Supporting information B in S1 File ). Such a variety of approaches in conservation is not surprising, given that conservation targets are usually defined in accordance with different values and motivations [ 17 – 19 ]. Once these values and motivations are openly recognized, conservation-related disciplines such as invasion science can adopt standardized and systematic approaches to measure the degree to which specific entities of interest are affected by certain drivers of change (e.g., alien taxa), so that informed and coherent management decisions (e.g., prioritization) can be made. However, the majority of impact assessment frameworks developed and applied in invasion science do not consider the ways of assessing increases to native biodiversity [ 8 ], and the field has been criticized for focusing on, and overemphasizing, the harmful impacts of alien taxa [ 20 – 22 ].

Impact: any change caused by an alien taxon to the recipient system. Impacts are generally quantified by measuring how certain attributes of the recipient system (such as the amount of nitrogen or the number of fish in a lake) change due to the introduction of the alien taxon. In EICAT+, only impacts on the individual performance, population size, and area of occupancy of a native species are considered.

Biodiversity attribute: any feature or component of biological diversity that can be measured, quantified, and compared, such as the taxonomic richness, phylogenetic diversity, and functional diversity of a community or the abundance, total biomass, and average body size of individuals in a population. In EICAT and EICAT+, the biodiversity attributes to quantify impacts caused by alien taxa on native taxa are performance of individuals, population size, and area of occupancy [ 10 , 24 , 25 , 117 ].

Taxa introduced beyond the limits of their native range (termed alien taxa) are a primary driver of global environmental change [ 1 , 2 ]. Once introduced to new areas, alien taxa can cause changes to their recipient ecosystems [ 3 , 4 ] ( Box 1 , Supporting information A in S1 File ). These changes, called environmental impacts [ 3 ], are generally estimated by quantifying how certain attributes (i.e., measurable features or components; Box 1 ) of the recipient ecosystem vary due to the presence and abundance of alien taxa [ 4 ]. Increases or decreases in specific ecosystem attributes (e.g., in population size of a native species) can thus be described from a value-free perspective as positive or negative impacts, respectively ( Box 1 ). In addition, the same alien taxon can have negative impacts on certain attributes of native biodiversity and positive impacts on others, with different levels of magnitude and underlying mechanisms [ 3 , 5 ].

Development process and structure of EICAT+

The development of EICAT+ involved a 4-stage process of expert elicitation. At stage 1, a core panel of experts who had previously contributed to develop and improve EICAT [10,24,25,61] and were familiar with its application across various invasion contexts formulated a preliminary version of EICAT+. At stage 2, multiple experts from the invasion science community, many of which contributed to the development of the EICAT framework [10], were contacted and asked to provide input and feedback toward the core concepts of the framework under development. These experts were selected due to their extensive knowledge regarding the impacts of alien species and mechanisms through which these impacts are generated. At stage 3, and once a general consensus was reached between the experts, the core panel led the writing of the first and subsequent drafts of a manuscript regarding EICAT+. Several versions of the manuscript were produced, and, at each round, the experts involved were asked to provide substantial input into ideas, text, and figures. Importantly, experts also provided and reviewed real-world examples of positive impacts caused by alien species based on their taxonomic and ecological expertise; such examples were critical for testing the applicability of EICAT+ across various invasion contexts (see Supporting information D and E in S1 File). At stage 4, the final version of the framework and related manuscript were finalized and approved by all experts involved in this Consensus View.

Overall, we have structured the novel framework to align with EICAT using semiquantitative scenarios to assign an alien taxon to one of 5 ascending categories of impact magnitude. The EICAT+ scenarios describe how alien taxa can increase native biodiversity attributes at different levels of biological organization. The scenarios are thus hierarchically organized to describe all observed positive impacts. In accordance with EICAT, EICAT+ (a) considers impacts at the level of individuals (Minimal and Minor) and populations (Moderate, Major, and Massive) of a native taxon (Fig 1); (b) distinguishes between Major and Massive impacts on the basis of the reversibility of an impact after the disappearance of the alien taxon from its recipient system (Fig 2); (c) assigns a confidence score for each recorded impact to provide an estimate of uncertainty; (d) describes the different mechanisms by which alien taxa can impact native individuals and populations (Fig 3); and (e) performs the global assessment of a taxon by collecting evidence of impact from the taxon’s entire alien range and classifying the taxon based on the highest criterion level met anywhere in the alien range and across any of the impact mechanisms [24]. It should be noted that an alien taxon can be assessed under EICAT+ as having a positive impact on 1 native taxon and under EICAT as having a negative impact on another native taxon or different impacts on the same taxon but at different locations or in different contexts.

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TIFF original image Download: Fig 2. Examples of Major positive impacts under EICAT+. Hypothetical examples of Major positive impacts (MR+) caused by an alien palm (A) and an alien parasitoid wasp (B) on a local population of a native bird species (taxon of interest) on an archipelago. (A) The alien palm causes the local reestablishment of the native bird species, e.g., via natural dispersal of birds across the archipelago. (B) The alien parasitoid wasp acts as a classical biocontrol agent against alien palm weevils and prevents the extinction of the bird population. Note that under EICAT+, the impact is classified as Major regardless of whether the palm weevil is alien or native (see also submechanisms 10.1 and 10.2 in Fig 3), as the indirect positive impact is caused by an alien taxon (the parasitoid wasp). Since it can be assumed that the newly established population (A) or the recovered population (B) would not persist if the alien taxon causing the positive impact was no longer present on the island, the impacts should not be classified as Massive (MV+), i.e., the alien palm or wasp must continue to be present on the island for the native bird species to survive. Black arrows indicate introduction and establishment of alien taxa into a recipient ecosystem. Blue arrows indicate the reestablishment (A) and extinction prevention (B) of a native taxon due to an alien taxon. Symbols were courtesy of the Integration and Application Network, University of Maryland Center for Environmental Science (ian.umces.edu/media-library). https://doi.org/10.1371/journal.pbio.3001729.g002

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TIFF original image Download: Fig 3. EICAT+ and EICAT mechanisms and submechanisms. List of EICAT+ mechanisms and submechanisms (A) and EICAT mechanisms (B). EICAT+ and EICAT mechanisms and submechanisms are also compared to each other (C) based on the outcome of the interaction for native and alien taxa. Colors of rows and connecting lines reflect different rationales behind the formulation of the EICAT+ mechanisms and submechanisms, with the different colors and symbols that indicate [yellow and asterisks “*”] mechanisms present in both EICAT+ and EICAT but in which the functional roles of alien and native taxa are reversed (e.g., in EICAT+, the alien taxon is the prey, whereas in EICAT, the alien is the predator); [green and degree signs “°”] mechanisms that are unique to EICAT+ (e.g., dispersal facilitation through pollination); [pink and daggers “†”] mechanisms present in both EICAT+ and EICAT but in which impact direction is reversed because of overcompensation (e.g., in EICAT+, the alien taxon increases growth of the native taxon through browsing-mediated overcompensation, whereas in EICAT, the alien taxon decreases growth of the native taxon through browsing; [blue and tildes “~”] mechanisms present in both EICAT+ and EICAT but in which impact direction is reversed (e.g., in EICAT, the alien taxon decreases a biodiversity attribute by impacting the chemistry of the ecosystem, and in EICAT+, the alien taxon increases a biodiversity attribute by impacting the chemistry of the ecosystem). The symbols +, −, 0 indicate positive, negative, and neutral outcomes of interactions between a native and an alien taxon. In C, arrows indicate impacts of an alien to a native taxon (orange arrow: positive impact; blue arrow: negative impact). Symbols were courtesy of the Integration and Application Network, University of Maryland Center for Environmental Science (ian.umces.edu/media-library). https://doi.org/10.1371/journal.pbio.3001729.g003

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