General costs of invasive ant species
Our findings have documented actual costs attributed to ant invasions of at least US$ 11.13 billion between 1930 and 2020 with additional potential costs (expected and/or predicted) of US$ 45.79 billion from 1980 until 2084. Most reported costs were associated with two invasive ant species, S. invicta, the red imported fire ant, and W. auropunctata, the little fire ant, which mainly occurred in two countries, USA and Australia. Most of the reported costs were associated with damages, in particular, impacting the agriculture and public and social welfare sectors. Management costs constituted only 3.74% of the total amount, the majority of which was spent in post-invasion actions, such as control or eradication. Also, costs were geographically biased: on average 76.67% of invaded countries per species lacked cost reports, and within invaded countries the mean geographic coverage of reported costs per species and country was only 17.65%.
With respect to previous estimates describing invasive ants as causing losses and expenditures reaching > US$ 1 billion annually in specific countries (Pimentel et al. 2005; Gutrich et al. 2007, Wylie and Janssen-May 2017), our more conservative estimates show that we lose and/or spend annually US$ 121 million due to invasive ant species all around the world. This estimate could increase by US$ 444 million annually when including potential costs (i.e., costs planned, expected or predicted to occur). Note that our annual estimations are on a global scale for all invasive ant species and over the whole time range of available costs (see Online Resource 1). Cost extrapolations to the USA from Pimentel et al. (2005) were examined and not considered as they overlapped with the estimates provided by Lard et al. (2006). More specifically, both articles used data from Texas (Lard et al. 2002) to extrapolate to other US states, and we considered only Lard et al. (2006) which documented the estimation method used and detailed costs for each activity sector.
Information on the economic costs incurred by invasive ants is critically needed as it aids cost-benefit analysis to determine timely management actions. Here, we have shown that incurred costs constituted less than 20% of the total costs reported for invasive ants across the world. Nevertheless, better information on these observed costs can help to further develop predictive models of the monetary impacts of invasive species under different scenarios, thus providing data-oriented suggestions for improved management. In fact, most of the potential costs reported here for invasive ants were extrapolations based on observed data, across both time and space. For example, extrapolations to predict future costs under different management scenarios for Solenopsis in Queensland (Australia, Hafi et al. 2014), or for Wasmannia in Hawaii (USA, Motoki et al. 2013), or extrapolations to predict costs (past, present or future costs) in other areas where the same ant species invades, such as using the costs caused by Solenopsis in Texas to predict costs in other invaded states in the USA (Lard et al. 2006; Gutrich et al. 2007) or in Australia (Wylie and Janssen-May 2017). Also, all the reported costs for Solenopsis in the Pacific islands were extrapolated - such areas are expected to be invaded in the near future due to their trade history with other areas where ant invasions are prevalent, such as Australia or China (Gruber et al. 2021). While extrapolation is deemed to be useful, they are by nature highly uncertain; thus, our study highlights the urgent need to provide actual observed costs through accurate monitoring and reporting. Moreover, improved cost reporting by managers, practitioners and researchers can be used to raise awareness on the impacts of ant invasions and in turn, better inform policy makers and enhance public education.
Economic activity sectors impacted by invasive ants
The activity sectors incurring the most damages from invasive ants were mainly agriculture, and public and social welfare. Unfortunately, a large part of the documented costs was not detailed to specific economic sectors in the source information, and thus a high proportion of costs had to be classified as diverse or unspecified. Total costs for agriculture amounted US$ 3.61 million for A. octospinosus in the French Caribbeans, where this ant is known to be a serious pest (Mikheyev 2008; Celini et al. 2012). Reported economic losses in agriculture have also been reported for W. auropunctata in Hawaii (USA) where the nursery floristic exporting sector is expected to be mostly affected (Motoki et al. 2013; Vanderwoude et al. 2015). The most detailed costs in the agriculture sector were reported for S. invicta where both damage loss and damage repair as well as control actions have been quantified, affecting different crops, livestock, farm equipment, or the health of farmers or their animals (Lard et al. 2002; Lard et al 2006; Gruber et al. 2021). Agricultural impacts of invasive ants could mainly be attributed to the mutualistic relationship of ants with sap-sucking insects, such as aphids and mealybugs, which directly damage the plants and spread plant diseases (Eubanks 2001). Although some benefits to crops from invasive ants have also been reported, for example S. invicta feeding on other pests, such as insects that feed on corn, cotton or sugarcane crops, when all crop types and interactions are considered together, the overall influence of invasive ants in the agricultural sector is overwhelmingly negative (Lard et al 2002; Lard et al. 2006). Also, invasive ants can negatively impact livestock production by making it difficult for animals such as chickens to eat or sleep, and may also kill and eat newly hatched chicks (Wylie and Janssen-May 2017).
Invasive ants widely affect human infrastructure in different ways and to varying degrees, e.g. destroy electrical equipment, cause damages to property (e.g., cars, TV, telecommunication), resulting in high economic losses (Bradshaw et al. 2016). Costs specifically linked to impacts on human health are also frequently reported in the literature, in particular for those invasive ants that bite humans if disturbed, and whose sting can induce anaphylactic or allergic reactions (Boase 2007). For instance, more than 14 million people are stung annually in the US alone (Taber 2000), and of these more than 200,000 people require medical treatment (Holway et al. 2002). In our data, only S. invicta was reported as having quantified economic impacts specifically in the health sector in the USA (Lard et al. 2002), while potential medical costs were estimated for the Pacific islands, where outdoor activities are frequent, given that ant invasions could occur in such countries in the near future (e.g. Gruber et al. 2021). However, damage loss caused by Wasmannia, assigned to the public and social welfare sector, such as reduced property values or lodging in Hawaii (USA), are due to a reduction in recreational activities in outdoor areas, as this sector is prone to biting and stinging insects (Motoki et al. 2013; Lee et al. 2015). Ant species can also act as pathogen vectors, with some species carrying diseases that can be transmitted to humans, likely causing a wide range of serious infections (Moreira et al 2005). For instance, several ant species collected in Brazilian hospitals showed associated bacterial growth, e.g., the invasive species Pheidole megacephala (Fontana et al. 2010). Despite the above implications for health impacts, economic costs are scarcely available, demonstrating yet another important knowledge gap that needs urgent attention.
Economic damages and the costs of management
Although the economic costs of management were substantially lower in comparison with the cost of damages, the literature reports that the management of invasive ants itself is difficult, and can be very expensive (Hoffmann et al. 2010; 2016). However, early responses and other prevention measures implemented to avoid the expansion of early introductions can reduce post-invasion costs and damages, that are in many cases much higher (Leung et al. 2002, 2012; Essl et al. 2020; Diagne et al. 2021). With our data, we found that the already incurred costs of post-invasion management of invasive ants greatly exceed the costs spent for pre-invasion management measures. Clearly current ant invasions should be managed, and budgeting post-invasion management is necessary; however, budgets should also prioritize prevention, as preventing incursions or avoiding further expansion might be more cost effective than eradication attempts (Faulkner et al. 2020). Interestingly, when focusing on potential costs, expected or planned pre-invasion management actions were more expensive than post-invasion actions (US$ 147.08 million vs 70.42 million). Higher post-invasion costs stand for all the species, although it is notable that for S. invicta for which US$ 87.81 million are already spent in pre-invasion strategies (versus US$ 1.60 billion spent in post-invasion management), and it is planned to further invest US$ 147.08 million for pre-invasion measures (while only US$ 53.93 million for post-invasion actions) (Janssen 2017).
Many reports of invasive ant control focus on studies from the USA or Australia (Holway et al. 2002; Sanders and Suarez 2011; Hoffmann et al. 2016), which is in line with the fact that higher reported economic costs of invasive ants are found in these regions. Moreover, the spatial coverage of the reported costs of management measures is very similar to the spatial coverage of ant eradication programs reported by Hoffmann et al. (2016), indicating that at least the costs for eradication programs are well reported, although some species for which eradications were described in Hoffmann et al. (2016) had no reported costs (i.e. Tapinoma melanocephalum, Monomorium indicum or Myrmecia brevinoda). For example, in the USA, incurred costs especially concerned with the eradication program of W. auropunctata in Hawaii (US$ 10.63 million), and the control strategies in the continent for S. invicta (~ US$ 3 billion). Similarly, in Australia the eradication plan of Solenopsis invicta in Queensland constituted the majority of observed costs, together with the control and eradication programs of A. gracilipes in Queensland, Northern Territory and on Christmas Island (Hoffmann et al. 2016).
Interestingly, costs reported for L. humile, which is widely distributed worldwide and causes massive ecological impacts in urban, agricultural and natural environments (Holway et al. 2002; Sanders and Suarez 2011) were much lower than for Solenopsis spp., W. auropunctata and A. gracilipes. Additionally, all costs for this species were incurred and mostly (~ US$ 4 million) in post-invasion management actions, such as eradication programs on the Channel Islands (USA), Norfolk Island (Australia), Tirititi Matangi Island (New Zealand), and mainland Japan. Given the global notoriety of this invasive species it remains unclear why reports have not been produced that estimate its financial implications. Potentially it is because this species became widespread so long ago that focus has instead been given to the other newly arrived or ‘horizon’ species.
Notably, most of these eradication programs are ongoing, which is in agreement with the increasing trend in the number of reported cost entries for invasive ants worldwide (Fig. 1b) and with the high amount of potential - expected- costs described before. Accordingly, the cost of these programs may not be available as long as they are ongoing. Most of the costs mentioned were obtained directly from the managers of the eradication programs, proving the fundamental importance of the communication between scientists and practitioners and of combining data from different sources and languages (Angulo et al. 2021).
Gaps in the economic data for invasive ants: taxonomy, geography and research
We only have costs reported for the 12 ant species stated, yet most of the costs (76.93% of the cost entries and 99.83% of the economic amount) are for S. invicta and W. auropunctata, and costs for the rest of highly invasive ants are lacking. Lower or nonexistent costs for other invasive ant species could be due to them being less destructive, or to significant underreporting. Most certainly, a lot of economic costs are neglected, especially of those invasive ant species that are not yet referenced as invasive in the global lists of invasive species, such as Tetramorium tsushimae (Steiner et al. 2006), Cardiocondyla obscurior (Heinze et al. 2006), Plagiolepis alluaudi (Wetterer 2014), Formica paralugubris (Frizzi et al. 2018) among others. Although only 19 invasive ant species are referenced in the IUCN database, Lach et al. (2010) already considered that 147 ant species had successfully established populations outside their native range, and 186 species are registered as introduced in the Antweb “Introduced” project in 2020. Moreover, recent studies proposed more than 200 ant species that have established outside of their native range through human-mediated transport (Bertelsmeier et al. 2017), while around ~ 20 more ant species have been identified as potentially invasive based on their life history traits, i.e. at risk of becoming the next invaders such as Lepisiota canescens or Technomyrmex difficilis (Bertelsmeier et al. 2013; Fournier et al. 2019). The economic costs associated with these species have been, as a consequence, less studied, whereas they could constitute an economic black hole.
Some invasive alien species have even identifiable characteristics leading them to be more susceptible to induce economic costs. For instance, the invasive garden ant L. neglectus, which invaded all over Europe from Asia Minor (Espadaler et al. 2007), is an opportunistic species with intensive exploitation of aphids, that could cause massive damage to infested greenhouses (Rey and Espadaler 2005). Lasius neglectus ants also have continual presence within homes, inducing food contamination in the catering facilities, and is attracted to electrical installations, light switches, power sockets and electrical security systems, damaging them by its activity (Rey and Espadaler 2005). As a result, this pest species could have an economic impact comparable to the Argentine ant L. humile, although the costs reported were much lower given that its geographic expansion is only starting (Espadaler et al. 2007; Ugelvig et al. 2008).
With respect to the geographic coverage of the reported costs even for the most-studied invasive species, many costs are lacking. On average, 77% of the number of invaded countries per species had no reports of costs. Further, when costs were reported in a country, less than 18% of locations on average in those invaded countries had reported costs. In addition, we only mapped occurrence records that were readily available with geographic coordinates compiled for each ant species, which excluded many records that would have increased the gap if included. Beside these taxonomic and geographic gaps, many costs were also ignored in this paper because they were published collectively with other taxa and not only ants. For example, Hequet (2009) presented some costs specifically for W. auropunctata in New Caledonia, but other costs linked to population sensitization to invasive alien species or linked to control of Wasmannia were considered together with rodent and plant control in isolated islands.
There are certainly many other types of costs related to invasive alien ants that are not recorded in InvaCost, or under-recorded, and that likely contributes to a gross underestimation of their global economic costs. As an example, research grants for scientists studying invasive alien ants are typically not recorded as economic costs and therefore largely absent from the InvaCost database. When asking colleagues worldwide about their research grants on invasive alien ants throughout the last 30 years, we came up with 45 responses providing an estimated US$ 27,000 average per research article (Online Resource 6). If one considers about 4,742 research articles during this period on this topic (with the same keyword search in WoS as described in the Methods, except for the economic components), this suggests that this research grants component alone could be in the order of US$ 127 million (Online Resource 6). This crude estimation does not account for the true cost of a research project (typically a fraction of the money received by researchers), nor the researchers salary (often not included in grants), both of which could significantly increase this estimated amount. This information underlines the existence of substantial additional costs that are not taken into account in the global estimate we provide in this study, and should be considered as an invitation to make publicly available all possible monetary costs related to ant invasions.
The limited cost information that we are reporting also highlights the difficulty to value the impacts caused by invasive ants. Ants most likely hold multiple negative effects, and these impacts may differ from one species to another. Multiple assessment efforts are thus required for improving our understanding of the costs caused by these insects.
In conclusion, we present the most comprehensive assessment of the worldwide economic costs of invasive ants to date. Our description suggests that the global costs of invasive ants are massive, yet largely underreported, and as a result the actual costs are most likely grossly underestimated. We found economic costs documented mainly for two invasive ant species from mainly two countries, despite many other ant species being aggressive invaders worldwide. We also highlight the potential difficulty of obtaining a reliable assessment of the total economic costs incurred by invasive ants and advocate for improved cost reporting from managers, practitioners and researchers. Such efforts will help to understand ant invasions costs at the global scale and in turn, improve management performance and coordination amongst experts from different countries, which is urgently needed as impending ant invasions are expected to increase worldwide.