Benefits do not balance costs of biological invasions

Abstract

Biological invasions negatively affect biodiversity, ecosystem functioning, and ecosystem services (Simberloff et al. 2013, Pyšek et al. 2020, IPBES 2023). Although not all alien species have reported negative impacts (Bacher 2023), the subset that becomes invasive negatively affects social well-being, reduces cultural diversity, and burdens human well-being and the economy with large costs (Stoett et al. 2019, Diagne et al. 2021). Minimum estimates of the monetary cost of biological invasions are on the order of trillions of dollars (Diagne et al. 2021), comparable to the losses incurred from natural hazards (Turbelin et al. 2023). Preventing and managing invasions are therefore integral to the sustainable development agenda, as is reflected in target 6 of the Kunming–Montreal Biodiversity Framework (Convention on Biological Diversity 2023) and in the recent Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) assessment on invasive alien species and their control (IPBES 2023).

However, some invasive species can occasionally bring benefits to some sectors of society, such as monetary gains (Shackleton et al. 2019a). Therefore, actors from different sectors, practitioners, and scientists often have contrasting perceptions about the net sign of their effects on ecosystems or recipient communities and management actions (Jeschke et al. 2014, Shackleton et al. 2022). These perceptions of benefits have led to claims that the field of invasion science is focused exclusively on the negative effects of invasive species and overlooks their positive contributions to economies and ecosystems (Boltovskoy et al. 2022, Sax et al. 2022, 2023). Although these arguments are flawed because they conflate alien with invasive alien species, the fact that some invasive species have benefits is undisputed (Vimercati et al. 2020, Kourantidou et al. 2022, IPBES 2023). Consequently, considering the occurrence of and relationships between costs and benefits is necessary to contextualize the management of invasive species. In this regard, we explain that this must be done with caution because a direct, quantitative balance of benefits and costs is overly simplistic and misleading for three main reasons we describe in detail in the following sections of this Forum: The benefits of invasive species as a collective have never been demonstrated to be as high as their massive documented costs, the benefits do not offset the costs (they only exist in parallel with them), and the benefits always come at a price, because they are context-dependent and affect different stakeholders or regions at different times. Emphasizing economic benefits over negative impacts, drawing from ambiguities, and uncertain or unpredictable effects can be risky to conservation goals, because they can bias and hinder the proper assessment of all impacts, ultimately undermining the management of biological invasions.

Benefits are rarer than costs

Invasive species are plants, animals, pathogens, and other organisms that have evolved outside of a recipient ecosystem and that can cause economic or environmental harm or adversely affect human health (Convention on Biological Diversity 2021, IPBES 2023). Importantly, nonnative species or populations that are farmed or cultivated are generally not included in this category when they do not spread outside human-controlled environments. This means that the economic benefits of agriculture, aquaculture, and forestry are, for the most part, unrelated to biological invasions, and therefore, many of these benefits are extraneous and irrelevant to the invasions discourse. In addition, because invasive species are associated with negative impacts, they inherently imply the presence of costs, whether as a direct result of their negative consequences on ecosystems or indirectly through expenditure on their control. The documented benefits of invasive species are therefore typically by-products. In fact, any benefits are exceptions or special cases in the face of the massive ecological impacts of invasive species (Simberloff et al. 2013, IPBES 2023) or are the result of management seeking their control or removal. Although systematic comparisons of the costs and benefits of biological invasions are sparse, a recent systematic review analyzing the number of cases of the costs and benefits (labeled as undesirable and desirable effects, respectively) confirmed the expectation that the presence of the costs is more frequent and affects more sectors than the benefits (figure 1; Kelsch et al. 2020, IPBES 2023). Similarly, the recent IPBES assessment on invasive species highlights reports from some Indigenous peoples and local communities documenting that 92% of the impacts on nature from invasive alien species were negative, with only 8% being positive (IPBES 2023). More broadly, of 3783 documented impacts of invasive alien species on quality of life in the IPBES report, more than 85% are negative, and far fewer (15%) contribute positively to a good quality of life (Bacher 2023). In addition, the overall benefits of invasive species have never been demonstrated to be anything other than small compared with their quantified costs. The more than US$2 trillion (2017 currency value) costs of biological invasions already recorded in the (still expanding; Ahmed et al. 2023) InvaCost database represent a massive but conservative estimate, which could conceal a much higher true cost (Diagne et al. 2021, Leroy et al. 2022, Ahmed et al. 2023).

Figure 1.

The number of cases of costs and benefits of invasive species as indicated by respondents from local communities and recorded in the database of Kelsch and colleagues (2020) and the flows toward the sectors they affect. We have labeled the desirable positive effects as beneficial and those effects described as undesirable as costs. There are more cases of costs than benefits, and different sectors are implicated. The database, which separates the desirable and undesirable effects of invasive species, was reclassified as benefits and costs (economic, social, ecological) related to sectors (local community, health, tourism, fishery, farmers, environment, agriculture). The social costs are nonmonetizable, such as impediments to movement, health problems, and cultural practices. The ecological costs include biodiversity loss and environmental degradation. The economic costs include the loss of arable lands, production (e.g., crops, fisheries, livestock), primary resources, and water supply. The social benefits include cultural practices, resource provisioning (e.g., food and fuel), and medicinal uses. The economic benefits include the commercial use of resources (e.g., fuel, fishery, timber) and tourism. The ecological benefits are reported for increasing water supply, soil fertility, and control of other invasive species, although they are secondary to the previous impacts reported (e.g., drought, ecosystem degradation, introduction of invasive species).

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Moreover, the benefits related to financial gains can often be easily quantifiable for some stakeholders, such as those in fisheries and tourism (Kerr 2019), but the costs are typically not as straightforward to assess and quantify. These difficulties are particularly large when pertaining to the ecological damages to recipient ecosystems (IPBES 2023). Figure 1 shows that the greatest costs of biological invasions are those that affect the environment, whereas most of their economic benefits are present in local communities (e.g., businesses), fisheries, and livestock farming—more visible, anthropocentric, and quantifiable sectors.

The temporal scale at which the benefits and costs are generated is also necessary for comparison. The magnitude and range of social and environmental impacts (and the potential associated economic costs) typically manifest over longer durations than any associated economic benefits, thereby presenting an immense challenge to management and policy. Indeed, the ecological effects are often undetectable when invasive populations are first introduced (Daly et al. 2023), and although evidence for monetary impacts alone should not underpin conservation actions, assigning monetary values to their negative impacts can be challenging or impossible in these early stages. For example, the short-term economic gains from commercial fisheries targeting the Nile perch (Lates niloticus) in Lake Victoria have ultimately come at the vastly larger, long-term expense of the ecological and socioeconomic integrity of large lake areas, driving one of the greatest extinction events of hundreds of native and endemic fish species in modern history (Aloo et al. 2017).

Finally, although monetary metrics allow for the quantification of some of the benefits and costs, the effects of biological invasions are often complex and difficult to value in monetary terms, with invasions sometimes benefitting certain taxa or ecosystem services while concurrently affecting others negatively.

Benefits do not negate costs

Even when generated by the same invasive population, the costs versus benefits of invasive species should not be compared with the expenditures versus revenue in a simple accounting framework (IPBES 2023), particularly because they usually target different sectors (figure 1) that can be affected over different periods. Benefits can stem from exploiting the invasive species directly and from profitable activities indirectly leading to an introduction. In the first case, intentional introductions of species such as the red swamp crayfish (Procambarus clarkii) in Europe and the Atlantic salmon (Salmo salar) in Chilean Patagonia for aquaculture have indeed brought economic benefits for the companies commercially exploiting them (Souty-Grosset et al. 2016, Figueroa-Muñoz et al. 2022). However, these species have had substantial negative impacts in the wild across multiple sectors, including costs to agriculture, water management, and fishing livelihoods. In the second case of trade-driven accidental introductions, examples include profitable timber imports or agricultural products that can precipitate unintended insect invasions. There can also be unintentional escapes of species used in fur farming, in insect farming, in ornamental horticulture, or as pets (Carpio et al. 2020, Hulme 2021, Bang and Courchamp 2021). Therefore, the resultant economic costs are generally borne by other industries than those responsible for the introductions or by end consumers, who are faced with higher prices, which account for the invasion externality of yield losses, damage to infrastructure, or other types of costs (Diagne et al. 2021, Kourantidou et al. 2022). When economic profits are generated by the invasive species, the costs of invasions continue to exist, even if they are implicit.

Benefits to some are costly to others

Despite biological invasions being one of the five major direct drivers of biodiversity loss (e.g., IPBES 2019, 2023) and incurring damage costs analogous to those of natural disasters (Turbelin et al. 2023), the emphasis on benefits—ecosystem, social, or monetary—makes them an oddity in the fields of global change research. As a parallel, it is possible to think of the economic benefits of climate change (e.g., for sectors involved in climate-change adaptation), of habitat destruction (e.g., for real-estate developers and, more generally, any industry benefiting from urban populations or agriculture), and of overexploitation (e.g., for recreation or commerce). It is doubtful that the researchers studying these benefits would assign biases to the collation of costs or would present global change as desirable because of such restricted benefits. Such is, however, the status quo in critiques of invasion science. An undue emphasis on the benefits of biological invasions can also prevent or delay their management, ultimately leading to higher long-term economic costs and negative ecological and health impacts (Leung et al. 2002). Indeed, the recent estimates for delayed management, even of a single species, are tens of millions of dollars per year (Ahmed et al. 2022).

In a world where economic growth is still prioritized over nature conservation, promoting such sporadic and short-term benefits might also create dependencies within affected communities, undermining management and ultimately disrupting ecosystem structure and functioning (Vitule and Pelicice 2023). For example, the development of the charcoal industry and biopower plants around invasive species such as the shrub mesquite (Prosopis juliflora) was intended to improve livelihoods, generate energy, and manage the species sustainably in low- to middle-income Asian and African nations (Mwangi and Swallow 2008, Walter and Armstrong 2014). Nevertheless, the introduced shrub outcompeted native plants and disrupted an entire ecosystem, threatening local community resources and cultural values. The perceptions can also be influenced by other context dependencies (Kourantidou et al. 2022)—for example, previous land use and features of landscapes where invasive trees in barren grasslands (Acacia dealbata in South Africa) are perceived as valuable assets for soil erosion regulation and resource provision but cause damage to households, reduce crop production, and serve as hideouts for criminals (Ngorima and Shackleton 2019). However, treating an invasive species as a resource is often not the preference of local communities (IPBES 2023) and has shifted the focus to perpetuating the benefit instead of eradicating the problem, often leading to privatization of the benefits and socialization of the costs.

Ethical management must integrate all positive and negative effects

Despite the three major shortcomings detailed above, managing biological invasions does require accounting for any potentially positive effects and the implications to community members who will be affected one way or another. In general, nonmonetary evaluation methods such as qualitative assessments, social impact analyses, and environmental impact assessments could be used to infer environmental and other costs across invaded systems. This can be done by combining semiquantitative approaches integrating the positive and beneficial effects of biological invasions in existing frameworks (Shackleton et al. 2019a, Vimercati et al. 2020), such as EICAT+ (for environmental impact classification for alien taxa; IUCN 2020, Vimercati et al. 2022) and SEICAT (for socio-economic impact classification for alien taxa; Bacher et al. 2018), with quantitative approaches through databases like InvaCost (Diagne et al. 2020, Ahmed et al. 2023).

Decision-makers should strive to communicate the risks and impacts, negative and positive, of biological invasions across different sectors of the communities directly affected and should involve affected community members in decision-making processes (IPBES 2023, Reed et al. 2023). Equally, they should identify and raise awareness of alternative native resources that could provide similar benefits. The nature's contributions to people framework (Diáz et al. 2018) acknowledges that nature has a plurality of values, including intrinsic, instrumental, and relational values, and that decision-making and policy design should be informed by these different and complementary perspectives (IPBES 2019). For example, Indigenous peoples and local communities might perceive the introduction of a nonnative fish as an opportunity for fishing (Lima et al. 2010) or a nonnative tree species as a source of shade and timber (Kull et al. 2019) without being immediately aware of the negative impacts on native species populations, the loss of arable land, or health issues (Shackleton et al. 2019b). Differences in perspectives between regions can be due to differences in socioeconomic development and access to natural resources (Meyer and Fourdrigniez 2019). That the public is sometimes more aware of direct, positive effects than of indirect, negative ones (Sax et al. 2022) is not a good reason to abandon the management of biological invasions.

Conclusions

Positive effects of biological invasions do occasionally exist and should not be ignored by policymakers (Shackleton et al. 2019a, Vimercati et al. 2020). However, acknowledging these benefits does not negate the necessity of evaluating the overall impact (IPBES 2023). Moreover, global efforts to create evidence for the benefits of biological invasions are lacking and do not match the recently collated evidence for their costs. In the absence of such matching evidence, it is incorrect to propose comparability of the benefits and costs of biological invasions. Although benefits, unlike costs, lack a monetary synthesis, it is important to recognize that benefits and costs often affect different stakeholders, operate over divergent time scales, and are viewed through diverse socioecological perspectives. Promoting the benefits of biological invasions can also hinder management and therefore increase costs in the long term. The evidence and arguments we provide in the present article demonstrate that it is ethically and scientifically dubious to argue for prioritizing the limited economic benefits of biological invasions in the face of their overwhelming negative ecological, economic, and social impacts. Calls for shifting focus to the monetary benefits of biological invasions risks undermining the much-needed awareness and support to mitigate them.

Acknowledgments

LC was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (Capes)—(001). RNC is funded by the Leverhulme Trust (grant no. ECF-2021-001). CJAB is supported by the Australian Research Council (grant no. CE170100015). SB was supported by the Swiss National Science Foundation through grants no. 31003A_179491 and no. 31BD30_184114. FC is supported by the Biological Invasion Chair of the AXA Research Fund of University Paris Saclay and a salary from the French CNRS.

Author contributions

Laís Carneiro (Conceptualization, Supervision, Visualization, Writing – original draft, Writing – review & editing), Philip E. Hulme (Writing – original draft, Writing – review & editing), Ross N. Cuthbert (Writing – original draft, Writing – review & editing), Melina Kourantidou (Writing – original draft, Writing – review & editing), Alok Bang (Writing – original draft, Writing – review & editing), Phillip J. Haubrock (Writing – original draft, Writing – review & editing), Corey J. A. Bradshaw (Writing – original draft, Writing – review & editing), Paride Balzani (Writing – original draft, Writing – review & editing), Sven Bacher (Writing – original draft, Writing – review & editing), Guillaume Latombe (Writing – original draft, Writing – review & editing), Thomas W. Bodey (Writing – original draft, Writing – review & editing), Anna F. Probert (Writing – original draft, Writing – review & editing), Claudio S. Quilodrán (Writing – original draft, Writing – review & editing), and Franck Courchamp (Conceptualization, Supervision, Writing – original draft, Writing – review & editing)

Author Biography

Laís Carneiro ([email protected]) was affiliated with the Laboratory of Ecology and Conservation and with the Graduate Program in Ecology and Conservation at the Universidade Federal do Paraná, in Curitiba, Brazil. Philip E. Hulme is affiliated with Bioprotection Aotearoa, at Lincoln University, in Lincoln Canterbury, New Zealand. Ross N. Cuthbert is affiliated with the Institute for Global Food Security, in the School of Biological Sciences at the Queen's University Belfast, in Belfast, Ireland, in the United Kingdom. Melina Kourantidou is affiliated with the Department of Sociology, Environmental, and Business Economics at the University of Southern Denmark, in Esbjerg Ø, Denmark, and with the Université de Bretagne Occidentale, in Plouzané, France. Alok Bang is affiliated with the School of Arts and Sciences at Azim Premji University, in Bangalore, India; with the School of Arts and Sciences, Azim Premji University, in Bhopal, India; and with the Society for Ecology, Evolution, and Development, in Wardha, India. Phillip J. Haubrock is affiliated with the Department of River Ecology and Conservation at the Senckenberg Research Institute and Natural History Museum Frankfurt, in Gelnhausen, Germany, and with the Center for Applied Mathematics and Bioinformatics, in the Department of Mathematics and Natural Sciences, at the Gulf University for Science and Technology, in Hawally, Kuwait. Phillip J. Haubrock and Paride Balzani are affiliated with the South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, in the Faculty of Fisheries and Protection of Waters at the University of South Bohemia, in České Budějovice, in Vodňany, in the Czech Republic. Corey J. A. Bradshaw is affiliated with the Global Ecology Laboratory, Partuyarta Ngadluku Wardli Kuu, at the College of Science and Engineering, at Flinders University, in Adelaide, South Australia, and with the ARC Centre of Excellence for Australian Biodiversity and Heritage, in Wollongong, New South Wales, Australia. Sven Bacher is affiliated with the Department of Biology at the University of Fribourg, in Fribourg, Switzerland. Guillaume Latombe is affiliated with the Institute of Ecology and Evolution at The University of Edinburgh, in Edinburgh, Scotland, in the United Kingdom. Thomas W. Bodey is affiliated with the School of Biological Sciences at King's College, at the University of Aberdeen, in Aberdeen, Scotland, in the United Kingdom. Anna F. Probert is affiliated with the Zoology Discipline, in the School of Environmental and Rural Science, at the University of New England, in Armidale, Australia. Claudio S. Quilodrán is affiliated with the Department of Genetics and Evolution at the University of Geneva, in Geneva, Switzerland. Franck Courchamp is affiliated with the Université Paris–Saclay, CNRS, AgroParisTech, Ecologie Systématique Evolution, in Gif-sur-Yvette, France.

References cited