Background

Scientific research and the knowledge gained from it can guide societal responses to various economic and environmental challenges (Rosen Reference Rosen2018). Biological invasion is considered to be a defining feature of the Anthropocene (Stoett et al. Reference Stoett, Roy and Pauchard2019). Since the beginning of modern invasion science in the mid-1980s (Simberloff Reference Simberloff and DM2011), many studies have been conducted aiming to characterize the negative impacts of invasive alien species (IAS; self-sustaining populations in the wild with individuals dispersing, surviving and reproducing across multiple habitats; Blackburn et al. Reference Blackburn, Pyšek, Bacher, Carlton, Duncan and Jarošík2011) on native species, ecosystems and human well-being (e.g., Pyšek et al. Reference Pyšek, Hulme, Simberloff, Bacher, Blackburn and Carlton2020). The studies that focus solely on ecological processes and entities recommend the eradication of IAS to protect biodiversity (e.g., Jones et al. Reference Jones, Holmes, Butchart, Tershy, Kappes and Corkery2016). The negative economic impacts of IAS have also led many to advocate strongly for IAS management in numerous countries (e.g., Fantle-Lepczyk et al. Reference Fantle-Lepczyk, Haubrock, Kramer, Cuthbert, Turbelin and Crystal-Ornelas2022).

Yet some IAS have always been regarded as valuable assets because of their aesthetic, ecological and economic values (e.g., Acacia species; Shackleton et al. Reference Shackleton, Shackleton and Kull2019). Due to the continued change in recipient communities due to rapid globalization, the ‘novel ecosystems’ concept has been proposed (Hobbs et al. Reference Hobbs, Higgs and Harris2009). The last decade has seen increasing numbers of studies exploring how to harness the potential positive effects and usefulness of these novel ecosystems, including the IAS introduced by human actions. This school of research highlights the ability of some of these species to provide environmental benefits and improve human well-being by providing novel resources (e.g., Vimercati et al. Reference Vimercati, Kumschick, Probert, Volery and Bacher2020, Kourantidou et al. Reference Kourantidou, Haubrock, Cuthbert, Bodey, Lenzner and Gozlan2022).

That some IAS can have both negative and positive impacts in different socio-economic and spatiotemporal contexts has gradually been recognized by both academic (scientists and academics) and non-academic (practitioners and policymakers) communities (Osborne & Gioria Reference Osborne and Gioria2022, Shackleton & Vimercati Reference Shackleton and Vimercati2022). However, divergence in opinions between these two communities persists. For example, a survey has shown that practitioners and policymakers are less likely to acknowledge the benefits of IAS than scientists and academics, and a higher percentage of respondents think that the beneficial impacts of IAS are understated than those who do not (Shackleton & Vimercati Reference Shackleton and Vimercati2022). Multiple attempts have been made to consider the beneficial effects of some IAS in order to make better regulatory decisions. For example, the Environmental Impact Classification for Alien Taxa (EICAT+) framework has been proposed to categorize the magnitude of such positive impacts (Vimercati et al. Reference Vimercati, Probert, Volery, Bernardo-Madrid, Bertolino and Céspedes2022), whereas the Risk Analysis for Alien Taxa (RAAT) framework includes beneficial impacts as one of the criteria for the risk management of alien taxa (Kumschick et al. Reference Kumschick, Wilson and Foxcroft2020). Ideally, the trade-offs between the overall costs and benefits of IAS on sustainable livelihoods (i.e., livelihoods that can cope with economic, environmental and social stresses and maintain or enhance their capabilities and assets both now and in the future while not undermining natural resource bases; DFID 2000) should be integrated into IAS-specific studies (Shackleton et al. Reference Shackleton, Shackleton and Kull2019). Practically, these issues are often outside the specific scopes of research activities, particularly in the empirical studies (e.g., Wang et al. Reference Wang, Zhao, Zhang, Zhao, Lu and Wei2021).

We ask how future science communications can address the gap between scientific research and societal perceptions of beneficial IAS. We first investigate the reported beneficial aspects of invasive alien plant species (IAPS) and argue that, over time and space, the detrimental impacts of IAS might endanger sustainable livelihoods. We acknowledge that both the positive and negative impacts of IAS are very much context dependent and therefore propose that it is time for scientists to acknowledge diverse possibilities regarding these complex human–nature interactions in order to better inform decisions about them.

Benefits of invasive alien species: the evidence lists are growing longer

We used the Institute for Scientific Information (ISI) Web of Science literature database to search for peer-reviewed studies highlighting the positive impacts of IAPS published within the last two decades (see Appendix S1 for the detailed workflow). We found 154 studies reporting on 33 countries, among which South Africa, the USA and China were the most represented (Fig. 1). Most of the studies for which country information was available (n = 134) originated from 26 mainland nations (n = 114), whereas 20 studies were from 7 island nations. The number of studies on the positive impacts of IAPS has increased over time (Fig. 2a). Most studies reported these positive impacts on a regional scale (Fig. 2b). Some notorious IAPS such as Lantana camara, Eichhornia crassipes and Acacia mearnsii have been reported to have beneficial impacts in a large number of studies (Fig. 2c). Most of the species reported as having positive impacts belonged to the legume family Fabaceae (Fig. 2d).

Fig. 1. Global pattern of peer-reviewed studies (n = 154) that have highlighted beneficial impacts of invasive alien plant species during 2000–2020: countries having at least five studies are in bold, island nations are in blue.

Fig. 2. Number of studies indicating positive impacts of invasive alien plant species (IAPS): (a) cumulative number of studies over time; (b) number of studies conducted at regional, national and global scales; (c) taxonomic identities of 10 IAPS having more than five records; and (d) 10 families having more than 10 records.

The positive impacts reported in these studies were categorized according to the Level-1 states (the first of three economic botany data collection standards that covers all uses of plants; Cook Reference Cook1995). A large number of the studies reported environmental uses (Fig. 3a), among which positive impacts of the IAPS were reported in terms of both human (e.g., Prosopis juliflora, one of the world’s 100 most dominant IAPS, as a source of fuel, food, fodder and medicine) and non-human (excluding domestic animals; e.g., Lonicera tatarica in North America providing resources for the hybridization of two native fly species; Jachuła et al. Reference Jachuła, Denisow and Strzałkowska-Abramek2019) livelihood strategies. Some IAPS improve human livelihood strategies by providing regulatory (e.g., erosion control, Charbonneau et al. Reference Charbonneau, Wootton, Wnek, Langley and Posner2017; urban landscape regeneration, Rastandeh et al. Reference Rastandeh, Zari, Brown and Vale2018) and cultural services, while some provide provisioning services (e.g., raw material for producing environmentally benign fertilizer; Wang et al. Reference Wang, Zhao, Zhang, Zhao, Lu and Wei2021). Reports of IAPS providing resources for vertebrate (Nelson et al. Reference Nelson, Coon, Duchardt, Fischer, Halsey and Kranz2017) and invertebrate (Salisbury et al. Reference Salisbury, Al-Beidh, Armitage, Bird, Bostock and Platoni2017) taxa and providing refugia for rare and endangered animal species are plentiful.

Fig. 3. Overview of the uses reported for invasive alien plant species (IAPS): (a) bar graph showing the number of studies for each of the 13 uses categorized as Level-1 states (the first of three economic botany data collection standards that covers all uses of plants; Cook Reference Cook1995); (b) comparative assessment of TDWG Level-1 uses between the six countries with the greatest number of studies; the pie charts within the bar graphs show the percentages of environmental uses of the IAPS for improving human and non-human livelihood strategies.

Categories of uses were more diverse in countries such as South Africa and Kenya than in the USA and Australia (Fig. 3b). Studies on the role of IAPS in improving human livelihoods have originated primarily from southern and eastern Africa (e.g., Ugya et al. Reference Ugya, Imam, Hua and Ma2019) and South and South-East Asia (e.g., Wang et al. Reference Wang, Zhao, Zhang, Zhao, Lu and Wei2021). High-income countries such as the USA and Australia have explored the possible roles of IAPS in providing faunal habitats and resources (e.g., Utz et al. Reference Utz, Slater, Rosche and Carson2020) and in conserving native and endangered flora and fauna (e.g., Dunwiddie et al. Reference Dunwiddie and Rogers2017). This geographical pattern of beneficial impacts could be because numerous IAS were introduced and are still being promoted for the economic development of local rural livelihoods in lower-, lower-middle- and upper-middle-income countries (e.g., in Africa; Shackleton & Vimercati Reference Shackleton and Vimercati2022).

Benefits, but at what cost?

With so many positive impacts of IAPS being reported and the ‘novel ecosystems’ concept gaining support, it is unsurprising to see the increased denialism of their negative impacts (Boltovskoy et al. Reference Boltovskoy, Sylvester and Paolucci2018), and invasion biologists are struggling to translate their findings into meaningful management actions (Russell & Blackburn Reference Russell and Blackburn2017). The ‘novel ecosystems’ concept has met with strong opposition from invasion biologists, who have recognized the disastrous effects that IAS can have on a community if the ‘novel ecosystems’ attitude is followed inconsiderately (Murcia et al. Reference Murcia, Aronson, Kattan, Moreno-Mateos, Dixon and Simberloff2014, Miller & Bestelmeyer Reference Miller and Bestelmeyer2016).

Indeed, the impacts of IAS as perceived by humans are very much scale dependent and context specific (Kapitza et al. Reference Kapitza, Zimmermann, Martín-López and von Wehrden2019), as evidenced by most studies reporting beneficial impacts at a regional scale (Fig. 2b). The impacts of IAS on islands are greater in terms of biodiversity, agriculture, economy, health and culture than on continents (Russell et al. Reference Russell, Meyer, Holmes and Pagad2017). However, very little is known about the beneficial impacts of IAS on islands (20 studies compared to 114 conducted on continents). In addition, the positive impacts of IAS are often reported at a single time point, thereby providing no information regarding how these IAS–human interactions may change over time (Pergl et al. Reference Pergl, Pyšek, Essl, Jeschke, Courchamp and Geist2020). The few studies that empirically investigated human–IAS interactions at a temporal scale have revealed decreasing benefits and increasing negative impacts of IAS on human livelihoods over time if the IAS populations are left unchecked (Shackleton et al. Reference Shackleton, Witt, Nunda and Richardson2017).

An IAS having a positive impact on one organism does not necessarily mean that it will be beneficial to others (Vimercati et al. Reference Vimercati, Probert, Volery, Bernardo-Madrid, Bertolino and Céspedes2022). However, using IAS to improve human livelihoods often ignores the requirements of a broad spectrum of other life forms that are directly or indirectly affected by the IAS. For example, Robinia pseudoacacia is regarded as a species with high socio-economic value in both the Northern and Southern Hemispheres (Martin Reference Martin2019), but it has severe detrimental impacts on the richness and diversity of the plant–soil communities of the invaded ecosystems (Lazzaro et al. Reference Lazzaro, Mazza, d’Errico, Fabiani, Giuliani and Inghilesi2018). Lantana camara growing at the periphery of a protected area for use in the handicraft industry improves rural community livelihoods (Negi et al. Reference Negi, Sharma, Vishvakarma, Samant, Maikhuri, Prasad and Palni2019), although it can also reduce rural livelihoods through reducing incomes, increasing the fragmentation of farmlands and damaging grasslands and trees in the core and buffer regions of forests (Ranjan Reference Ranjan2019). These detrimental impacts on biodiversity, both direct (loss of species richness) and indirect (impacts on species inhabiting these ecosystems), cannot be fully evaluated in monetary terms (but see Hanley & Roberts Reference Hanley and Roberts2019) and therefore are often unaccounted for when assessing impacts on human livelihoods.

Another point of view advocates for using IAS as resource providers for non-human life forms. However, these studies often do not view the community in its entirety. IAS that may help in the conservation of rare fauna may still threaten the existence of groups of marginal species and might even lead to irrecoverable losses of biodiversity. For example, although L. tatarica provides resources for the hybridization of native insects, it decreases plant species richness and abundance (Maynard-Bean & Kaye Reference Maynard-Bean and Kaye2019) and reduces the nesting success of forest birds in urbanizing landscapes through increased nest predation (Borgmann & Rodewald Reference Borgmann and Rodewald2004).

With evidence increasing regarding the contrasting impacts of some IAS, a third research trend is emerging rapidly, focusing on selected IAS having positive impacts and suggesting their management through the utilization or overexploitation of these ‘beneficial’ IAS (e.g., Borokini & Babalola Reference Borokini and Babalola2012). Such ideas provide the fuel to drive utilization initiatives of IAS at multiple scales. Various non-governmental organizations often promote utilizing IAS, primarily for marginalized people in rural economies of lower- and lower-middle-income countries (Sharma & Raghubanshi Reference Sharma and Raghubanshi2012). Although this sounds promising, scientific evidence to support this management approach is rare, if not absent entirely (but see Wakie et al. Reference Wakie, Hoag, Evangelista, Luizza and Laituri2016). In fact, the very few studies that empirically tested this notion have revealed the ineffectiveness of this approach beyond a very localized scale for managing abundant IAS (Kannan et al. Reference Kannan, Shackleton, Krishnan and Shaanker2016).

Maximizing efforts focused on living with the invaded ecosystem also increases community dependency on the IAS and develops new markets. A positive attitude towards IAS begets more positivity, leading to more research exploring other IAS in terms of them yielding similar benefits (Sinclair et al. Reference Sinclair, Brown and Lockwood2020). The monetary incentives attached to this approach may facilitate the introduction and spread of IAS to hitherto uninvaded regions (e.g., Driscoll et al. Reference Driscoll, Catford, Barney, Hulme and Inderjit2014, van Wilgen & Richardson Reference van Wilgen and Richardson2014). The properties that make the aliens a treasured commodity also promote their successful establishment and naturalization in the wild (van Kleunen et al. Reference van Kleunen, Essl, Pergl, Brundu, Carboni and Dullinger2018), thereby creating one or more such ‘novel ecosystems’ where their impacts remain largely unknown. When these impacts on human livelihoods – not to mention on other life forms – are recognized, the damage is already done, and the feedback loop of IAS utilization makes effective management more complex. Exploiting IAS for resource provisioning therefore increases invasion debt (Essl et al. Reference Essl, Dullinger, Rabitsch, Hulme, Hülber and Jarošík2011), and ‘[n]ature is an expert in cost–benefit analysis. As for debts, she always collects in the long run’ (Atwood Reference Atwood2008).

Road ahead

With the predicted increase in novel introductions of alien species across the globe (Seebens et al. Reference Seebens, Blackburn, Dyer, Genovesi, Hulme and Jeschke2017) and the increasing exploration of the beneficial impacts of IAS, it is time for science communications to help readers make better-informed decisions regarding biological invasion. To do so, we suggest that the authors of future empirical studies push the boundaries of their personal opinions and disciplinary training and include value judgements regarding their findings in their publications; Table 1 offers advice as to how to prepare such statements.

Table 1. Potential factors to consider when providing an objective statement on the research findings focused on the positive impacts (beneficial impacts and control through utilization) and the negative impacts of an invasive alien species (IAS).

First, researchers and practitioners of the ‘beneficial’ school can acknowledge that utilizing IAS and leaving the invaded ecosystem as it stands will increase the invasion debt manyfold and may have irrecoverable consequences (e.g., loss of marginal life forms) and severely retard the progress of IAS management (e.g., by creating human dependence). Authors can explicitly mention the taxon and scale specificity of their studies to avoid generalization, highlight the potential risks involved with the species in focus and explain how the existing biosecurity infrastructure can regulate the further promotion and spread of the species. These studies could also encourage the exploration of native and near-native species for achieving similar benefits (e.g., Everard Reference Everard2020).

Second, studies reporting on IAS management through their utilization could highlight the possible impacts of the utilization measure on the local economy (e.g., creating economic dependence and shifting livelihood strategies; Kent & Dorward Reference Kent and Dorward2015). The authors of such studies could also evaluate existing and potential future measures to manage the promotion and spread of the IAS resulting from the revenue-generating practice in question. They could critically assess the economic and ecological feasibility of the proposed management measure at a large spatiotemporal scale, especially for widespread IAS, and provide information about previous management attempts, if any, and their successes and failures.

We also acknowledge that the harmful impacts associated with some IAS can also be context dependent (Catford et al. Reference Catford, Wilson, Pyšek, Hulme and Duncan2022). Thus, studies highlighting the detrimental impacts of the IAS could mention any positive roles they might play, especially if they have been previously reported at the specific scale of the study in question. The authors of such studies could emphasize the benefits gained from managing the IAS and the consequences of exploiting these resources without any regulatory mechanism. That the positive roles of the IAS in question might also hinder the implementation of the proposed management measures also needs to be acknowledged, and it would be important to suggest how best to overcome such hindrances. Studies highlighting the negative impacts of IAS should strive to present their arguments (negative over positive) as being supported by the available and most current scientific evidence (Russell & Blackburn Reference Russell and Blackburn2017).

While value judgements can be placed in the discussion sections of articles (e.g., Jachuła et al. Reference Jachuła, Denisow and Strzałkowska-Abramek2019), a dedicated section for such judgements might be more effective in terms of drawing readers’ attention. Importantly, this section should not be viewed as representing a caveat of the study; instead, the value judgements of the authors should complement the study’s findings to provide a more complete pictures of the IAS in question (Vimercati et al. Reference Vimercati, Probert, Volery, Bernardo-Madrid, Bertolino and Céspedes2022). Journal editors and reviewers should also encourage authors’ engagement with this practice. Many journals are already exercising a similar practice (e.g., encouraging authors to structure their study methods following a standard protocol). Such value judgements could be hindered by a lack of sufficient information on the species in question, which can be highlighted by authors to prevent further generalization of the impacts reported.