Drivers of future alien species impacts: An expert‐based assessment

Abstract

1. INTRODUCTION

The impacts caused by alien species on biodiversity and human livelihoods are substantial (Bacher et al., 2018; IPBES, 2019; Shackleton, Shackleton, & Kull, 2019; Simberloff et al., 2013; Vilà et al., 2011), and the numbers of alien organisms are still increasing worldwide (Seebens et al., 2017, 2018). Accordingly, much research effort has been devoted to understanding the historical trajectories of alien species accumulation, their impacts and the underlying drivers (e.g. Dawson et al., 2017; Dyer et al., 2017; Seebens et al., 2017; Vilà et al., 2011). What is lacking, however, is an assessment and understanding of the potential future impacts of alien species on biodiversity and human livelihoods (Lenzner et al., 2019; Roura‐Pascual, Richardson, Chapman, Hichert, & Krug, 2011). This is in stark contrast to other drivers of global biodiversity loss, such as climate or land‐use change, for which detailed assessments of potential future impacts have been developed (Hurtt et al., 2011; Moss et al., 2010).

This gap persists for several reasons. First, biological invasions, like other global change aspects, are a complex and context‐dependent phenomenon; so far limited data availability severely constrained the development of general predictive models, especially because of the need to consider large areas, long time periods and a large number of alien species across many taxonomic groups and habitat types. Second, impacts caused by alien species on biodiversity (Blackburn et al., 2014) and human livelihoods (Bacher et al., 2018) differ markedly among invaded regions, and variations in perceptions, values and interests provide additional context and further complicate the assessment and projection of impacts (Essl et al., 2017). This context dependency largely affects and complicates coordinated management efforts of biological invasions across regions and scales (Crowley, Hinchliffe, & MacDonald, 2017; Epanchin‐Niell et al., 2010). Finally, in most cases, there are large uncertainties about how a given alien species (or group of alien species) will respond in range and abundance to particular changes in the environment or human activities, and how such changes in distribution will affect interactions with resident biota and human activities that may ultimately translate into impacts (Hui & Richardson, 2019). Consequently, quantitative projections of how biological invasions may unfold in the decades to come under alternative trajectories of environmental change are missing (IPBES, 2016; Lenzner et al., 2019).

While the development of quantitative models to analyse the range of potential future impacts of alien species is challenging due to the complex interactions underlying biological invasions, other approaches that can shed light on future trajectories of biological invasions are more feasible. In particular, different methods, such as horizon scanning (Roy et al., 2018; Sutherland et al., 2018), the Delphi approach (MacMillan & Marshall, 2006), analytical hierarchy processes (Drescher et al., 2013) or Bayesian networks (Uusitalo, 2007), capture expert knowledge and generate predictions for potential future developments of specific components of global environmental change and have been successfully applied (e.g. Rowland, Cross, & Hartmann, 2014). Recently, expert elicitation has been used to identify future emerging issues in biological invasions (Ricciardi et al., 2017), create a watch list of future invaders (Roy et al., 2018) and identify priority issues in invasion science and management (Caffrey et al., 2014; Dehnen‐Schmutz et al., 2018).

Here, we provide an assessment of how particular drivers may affect biological invasions in contrasting contexts and under different scenarios over the next three decades (until 2050), drawing upon the knowledge of 36 biological invasions experts. Specifically, we address the following questions: (a) What is the minimum proportional increase from the current state of biological invasions that will cause major impacts on biodiversity? Furthermore, we construct two alternative futures, that is, plausible best‐case and worst‐case scenarios, both regarding the 15 most relevant drivers of future potential impacts of biological invasions in different contexts. Then, we ask (b) how likely is it that individual drivers will enable such major impacts on the environment under a best‐ or worst‐case scenario?

2. MATERIALS AND METHODS

Before providing a detailed description, we summarize our approach that consisted of the following four main steps. (a) We began by developing invasion scenarios under plausible futures of socio‐economic development and identifying drivers of invasions through a facilitated workshop with 25 experts. (b) Following the workshop, we developed contrasting scenarios of the drivers through the mid‐21st century. (c) We then developed and administered a survey to elicit expert judgements about thresholds for major impacts of invasions on biodiversity along with likelihoods that potential impacts of alien species will exceed these thresholds under each driver scenario. (d) Finally, we conducted statistical analyses of the survey data to examine the research questions.

2.2. Selection of respondents and performing the survey

The first author of this study compiled a list of potential participants for the survey aiming for a balanced composition in terms of geographic regions, career stages and complementary expertise (taxonomic, geographic, environment, research focus). This resulted in a list of 50 experts of invasion science who were invited to contribute to the survey; 36 of them completed the survey between December 2017 and March 2018 (72% response rate).

The survey was circulated as an Excel workbook (Supplementary Material 2, Table A) to potential respondents. Using an offline survey was the most practical option in a pretest of the survey, allowing the respondents to revisit their assessments during any stage of completing the survey. First, respondents were asked to score the list of 15 preselected key drivers (Table 1) proposed to shape biological invasions until the mid‐21st century (2050) under contrasting socioecological contexts, and to assess the importance and uncertainty for each driver. Definitions of categories for each survey question were provided by the coordinator (F.E.) in a separate document that was circulated alongside the table (see survey instructions in Supplementary Material 1, Table B). Second, respondents were asked to provide a self‐assessment of their background and expertise (Supplementary Material 3). Overall, highest expertise among participants was concentrated in Europe (58% of the respondents) and North America (47%) followed by South America (17%), the Pacific Islands (17%), Australia (14%), Africa (14%) and Asia (11%) and taxonomic expertise was highest for plants (61%), invertebrates (47%), followed by vertebrates (44%) and microorganisms (14%). Expertise by realm was strongest in terrestrial (78%) regions followed by freshwater (36%) and marine (19%).

TABLE 1

Top three most important drivers of alien species impacts until 2050 under the best‐case scenario. The ranking is context dependent and based on the coefficient estimates of the ordinal logistic regression models fit to survey data from 36 experts (see Supplementary Material 5A). Each different driver is highlighted by an individual color to increase readibility

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3. RESULTS

3.1. The threshold of major impacts on biodiversity across different contexts

The 36 respondents provided thresholds on what level of increase would result in future major negative impacts of alien species on biodiversity relative to the current impacts of invasive alien species for 14 different socioecological contexts (Figure 1; Supplementary Material 4). These thresholds thus provide an assessment of relative increases (in %), but not of absolute changes. Median thresholds in most contexts ranged between 20% and 30% increase compared to the current conditions (Figure 1; Supplementary Material 4). The lowest thresholds were for terrestrial and freshwater environments, countries with emerging economies and vertebrates and microorganisms (+20%), the highest were for marine environments, developed countries and countries with emerging economies, tropical, temperate and polar regions and plants (+30%). Although there are minor differences in medians among environments (i.e. freshwater, marine, terrestrial), there are moderate differences among taxonomic groups (plants have a higher median than the other taxonomic groups) and among socio‐economic contexts (countries with emerging economies having a lower median than developing and developed countries). Among climate contexts, the median is the highest for tropical climates, while polar, temperate and subtropical climates have somewhat lower medians. However, the pairwise Kolmogorov–Smirnov test showed significant differences between the density distributions of vertebrates and plants and between freshwater and marine realms. All other tests generated non‐significant results (Supplementary Material 5).

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FIGURE 1

Density distribution of the increase in alien species compared to the current conditions required to cause major impacts on biodiversity, as estimated by 36 experts. Vertical red lines indicate the median value of the density distributions. Columns correspond to zonobiomes, taxonomic groups, realms and socio‐economic development (from left to right); see Supplementary Material 4. Uncertainty estimates are the mean uncertainty values provided by the experts using a five‐point Likert scale

The uncertainty ratings provided by experts averaged between 2.3 (for microorganisms) and 3.4 (for vertebrates, freshwater and terrestrial environments; Figure 1). The highest uncertainties among zonobiomes were for tropical zones, microorganisms among taxonomic groups, marine among realms, whereas essentially no difference in uncertainty was observed among countries classified by socio‐economic development.

3.2. Driver impacts on biodiversity under best‐ and worst‐case scenarios

Under the best‐case scenario for the respective drivers, trade & transport, socio‐economic development and climate change emerged as significant drivers of future biological invasions across all socioecological contexts (Table 1). Demography & migration is expected to have a significant effect in 11 socioecological contexts, that is, all except developed countries, polar regions and temperate regions. It was followed by recreation & tourism with significant effects in 10 socio‐ecological contexts (all except vertebrates, marine and terrestrial regions, and developed countries) and land use & land cover change with significant effects in eight socioecological contexts (all except polar and temperate regions, microorganisms, vertebrates, the marine realm and developed countries). Furthermore, ocean acidification emerged as a significant driver in tropical regions, while cooperation, legislation & agreements drive biological invasions by invertebrates. Finally, biodiversity loss & degradation emerged as a significant driver of biological invasions in countries with emerging economies (see Figure 2; Supplementary Materials 5 and 6).

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FIGURE 2

Importance of drivers of major alien species impacts on biodiversity under a best‐case and worst‐case scenario among socioecological contexts as estimated by 36 experts on biological invasions. Responses are summarized by socioecological context: (a) zonobiomes, (b) taxonomic groups, (c) realm and (d) socio‐economic development. Estimates indicate the probability of respondents answering in lower uncertainty categories, meaning they are more certain that the driver is likely to surpass the threshold of major impact on biodiversity. Significant estimates are indicated by asterisks (significance levels: * < 0.05, ** < 0.01, *** < 0.001). Darker whiskers represent estimates under a best‐case scenario for the respective drivers, and lighter whiskers represent estimates under a worst‐case scenario. In panel (d), socioecological contexts are defined as (i) developed countries: socio‐economically highly developed countries; (ii) developing countries: socio‐economically poor countries with mostly slow rates of economic growth; (iii) countries with emerging economies: socio‐economically rapidly developing countries and middle income countries (for all definitions, see Table S2)

For the worst‐case scenarios, most respondents were certain that each driver would play a significant role in surpassing the threshold for major impact on biodiversity by alien species (Figure 3). The only driver that was not highly significant across all socioecological contexts was ocean acidification with only a medium significant effect for vascular plants, likely reflecting the paucity of species of this taxonomic group in marine environments (see Figure 2; Supplementary Material 6).

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FIGURE 3

Distribution of uncertainty if 15 major drivers of biological invasions will exhibit major impacts on the environment by 2050 under a best‐ and worst‐case scenario, based on answers provided by 36 experts. The uncertainty categories follow a five‐point Likert scale. The estimates shown include all responses across 14 contexts regarding taxonomic groups, zonobiomes, realms and socio‐economic status (see Supplementary Material 1, Table 1). The stacked bars represent the uncertainty categories, with the bars and percentage value for the medium certain category centred at 0% on the x‐axis. Bars and percentage values on the left refer to the uncertainty categories extremely and moderately uncertain, and bars and percentage values on the right refer to the answers in the categories highly and extremely certain. Categories sum up to 100%

4. DISCUSSION

This study provides the first global assessment of potential future impacts of biological invasions on biodiversity. Specifically, we examined these potential impacts under best‐ and worst‐case scenarios in differing environmental, taxonomic and socio‐economic contexts based on a large number of drivers and considering plausible differences in how the drivers might develop (i.e. best‐ vs. worst‐case scenarios). The assessment is based on the collective knowledge across a diverse group of invasion scientists and thus reflects current understanding on the future fate of biological invasions in the Anthropocene. Experts agreed that in a worst‐case scenario, all focal drivers will contribute strongly to potential future impacts of alien species, while under the best‐case scenario, the results show a more diverse and heterogeneous pattern. Our findings therefore imply that there are substantial opportunities under best‐case scenarios to reduce potential future impacts of biological invasions. Among the three most important drivers of potential impacts of biological invasions until the mid‐21st century, respondents agreed that trade & transport, climate change and socio‐economy are consistently and highly relevant across socioecological contexts while assuming the best‐case scenario.

Trade & transport was consistently ranked as the most relevant driver in all contexts other than for polar regions (Table 1). The importance of changes in global trade for biological invasions is well known (Dawson et al., 2017; Reino et al., 2017; Sardain, Sardain, & Leung, 2019; van Kleunen et al., 2015; Winter et al., 2009). Alterations in trade (e.g. in terms of volume, regions of origin and destination, composition of traded goods) will increase the number of potential new arrivals and might increase propagule pressure (Sardain et al., 2019; Seebens et al., 2015). Changes in the global trade network may also lead to novel source pools for new alien species, and climate change will likely lead to the establishment of new trade routes (e.g. through the Arctic) that will dramatically reduce travel times and increase species survival (Eguíluz, Fernández‐Gracia, Irigoien, & Duarte, 2016; Melia, Haines, & Hawkins, 2016; Miller & Ruiz, 2014). Finally, the emergence of new trade modes (e.g. internet trade) will provide novel pathways for species trade and subsequent introduction as such pathways are likely more difficult to regulate compared to conventional modes (Humair, Humair, Kühn, & Kueffer, 2015). National and international policy on prevention efforts can be explicitly developed to counter the increased propagule pressure associated with an increase in diversity and frequency of trade routes (Reaser, Meyerson, & von Holle, 2008; Wonham, Byers, Grosholz, & Leung, 2013).

Climate change, with associated changes in mean annual temperatures, precipitation and occurrence and magnitude of extreme events, will undoubtedly shape the impacts of biological invasions on biodiversity in the future. Several modelling studies predict an increase in climatically suitable areas for alien species (e.g. Bellard et al., 2013; Dullinger et al., 2017; Gallardo & Aldridge, 2013) and increased establishment rates of alien species have been attributed to climate change, even when accounting for propagule pressure (Huang, Haack, & Zhang, 2011). However, substantial variation in the effects of climate change among geographic regions or taxonomic groups might occur. A systematic review by Bellard, Jeschke, Leroy, and Mace (2018) showed that there are also many alien plants and animals that might have less climatically suitable areas in the future. Based on the expert assessment, potential impacts from alien species invasions on biodiversity will be especially likely in polar regions. This expectation coincides with climate change projections, indicating some of the most severe effects of future climate change in these regions (IPCC, 2014).

Socio‐economic activity serves as a proxy for many human‐induced environmental changes (Essl et al., 2011; Pyšek et al., 2010). Often this variable is substituted with metrics such as per capita gross domestic product, human footprint index or human development index. These variables can be related to diverse environmental changes relevant for biological invasions, like resource and energy use, consumption or land use. With a projected future increase in global material footprint of around 75% by 2050 compared to 2015 (IRP, 2017), a substantial increase in impacts from biological invasions is very likely, as supported by the expert assessment in this study.

Aside from the three main drivers that emerged from this expert assessment, several others were deemed important in specific contexts. Human demography & migration was identified as having major impacts on biodiversity in several contexts. For tropical and subtropical regions, it was ranked as the second most important driver. In these regions, changes in human population density and migration are projected to be especially pronounced throughout the 21st century (Lutz, Butz, & Samir, 2014; Rigaud et al., 2018). Increasing human population sizes likely result in more degraded habitats and intensification of land use, which generally favour alien plant establishment and spread (Essl et al., 2011; Pyšek et al., 2010). Additionally, human intra‐ and intercontinental migration (e.g. due to climate change, economic inequalities or armed conflicts) are projected to increase (Lutz et al., 2014; Rigaud et al., 2018). Human migration has, in turn, been associated with increased spread of alien species (Di Castri, 1989).

For invertebrates, vertebrates and vascular plants, demography & migration ranked third. Invertebrates are generally spread unintentionally, in the terrestrial environment mostly as contaminants in commodities, and in the aquatic environment as stowaways in vessels (Katsanevakis et al., 2014; Pergl et al., 2017). With increasing population density and increased trade & transport, the likelihood of invertebrate introductions and subsequent spread is expected to increase (Aukema et al., 2010).

For vertebrates and vascular plants, mechanisms of invasions are more complex. While some species are introduced unintentionally as stowaways (e.g. some reptiles like the brown tree snake Boiga irregularis or the house gecko Hemidactylus frenatus, Rodda, Fritts, & Conry, 1992) or contaminants (e.g. seeds in agricultural products, Frick et al., 2011), others are introduced and subsequently spread as a result of intentional introductions from the pet (Blackburn, Dyer, Su, & Cassey, 2015; Bush, Baker, & Macdonald, 2014; Hulme et al., 2015) or horticultural (Dehnen‐Schmutz, Touza, Perrings, & Williamson, 2007; Dullinger et al., 2017; van Kleunen et al., 2018) trades. For many species, propagule pressure is much more important than their ecological characteristics (Jeschke & Starzer, 2018; Pyšek et al., 2015).

Supporting the argument that unintentional introductions increase the future risk of impacts (Pergl et al., 2017), our survey revealed that respondents consider recreation & tourism, where the argument runs along the same lines (Hulme, 2015), as an additional important driver for increased future impacts from invertebrates and microorganisms. For the latter taxonomic groups, recreation & tourism was considered as the second most important driver for potential future impacts on biodiversity. A doubling of global tourism is projected from 2010 to 2050 under the best‐case scenario (UNWTO, 2018), which will likely lead to several synergistic effects with other drivers such as infrastructure development in the respective regions (Anderson, Rocliffe, Haddaway, & Dunn, 2015). Based on our findings, recreation & tourism was an important driver in subtropical and tropical regions along with countries having emerging economies (which are mostly situated in subtropical and tropical regions). Especially in these regions, where many natural areas are still less modified by humans, increasing infrastructure development like roads—which can act as corridors for alien species—will likely lead to increased spread and potential impacts of alien species (Seebens, 2019). Furthermore, many resorts and other tourist accommodations use ornamental (often alien) plants in their green spaces. This mode of horticulture provides a significant opportunity for alien species to escape, establish and spread in the surrounding environments (Anderson et al., 2015; Pickering, Bear, & Hill, 2007).

Finally, our assessment revealed that in aquatic and terrestrial socioecological contexts, eutrophication and pollution are assumed to become a major driver of potential future impacts of alien species. Changes in ecosystem chemistry and resource availability (especially nitrogen availability) can have dramatic effects on species composition in a wide range of ecosystems (Bobbink et al., 2010). In many cases, opportunistic species, including many alien species, benefit most from higher levels of nutrient availability (Preston, Hedman, & Johnson, 2018). Results from our assessment did not indicate that eutrophication and pollution will strongly drive future invasive species impacts in marine environments. This contradicts findings from empirical investigations showing that marine litter (i.e. plastic debris) can act as a vector of alien species (Carlton et al., 2017; Rech, Borrell, & García‐Vazquez, 2016) and that marine pollution can increase invasive species success (Crooks, Chang, & Ruiz, 2011).

5. CONCLUSIONS

Understanding how and why the impacts of invasive alien species might change in the future is a daunting task that has so far defied the development of quantitative scenarios and models (Lenzner et al., 2019). We suggest that expert‐based assessments provide a valuable tool to support quantitative assessments and may help identify emerging threats and directions for future research. We demonstrated that, based on expert knowledge, there is a high risk of increased potential future impacts of biological invasions due to many drivers, especially increased trade and transport (Hulme, 2009), climate change (Walther et al., 2009) and socio‐economic change (Pyšek et al., 2010). Our assessment can be used to develop recommendations for policy‐makers and environmental managers. In particular, our findings provide a scientific basis for the prioritization of actions to mitigate potential future impacts of biological invasions in the context of the Post‐2020 Framework of the Convention on Biological Diversity (CBD, 2020) and the United Nations 2030 Agenda for Sustainable Development (United Nations, 2016). Most importantly, our study provides expert‐derived benchmarks for thresholds of major impacts in different socioecological contexts, identifies which drivers are most likely to cause substantial impacts and identifies potential options under best‐case scenarios to reduce potential future impacts of biological invasions.

AUTHOR CONTRIBUTION

F.E., N.R‐.P., Be.L. and W.R. organized the workshop that formed the basis for this manuscript. F.E. conceived the ideas and designed the study, with input from several other authors. All authors (except B.J.M.) completed the survey. Be.L. led the analysis with help from F.E., S.D. and B.J.M., F.E. and Be.L. wrote the paper with major inputs from S.D. All authors commented on the manuscript.

Supporting information

ACKNOWLEDGEMENTS

Notes

Essl F, Lenzner B, Bacher S, et al. Drivers of future alien species impacts: An expert-based assessment. Glob Change Biol. 2020;26:4880–4893. 10.1111/gcb.15199 [PMC free article] [PubMed] [CrossRef] [Google Scholar]

Franz Essl and Bernd Lenzner contributed equally to the manuscript.

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