Economic costs of invasive bivalves in freshwater ecosystems

To assess spatio‐temporal and taxonomic patterns of available information on the costs of invasive freshwater bivalves, as well as to identify knowledge gaps.


| INTRODUC TI ON
Freshwater ecosystems have been identified as among the most threatened worldwide, owing to their sensitivity to the effects of climate change (Woodward et al., 2010) and a range of other anthropogenic pressures (Darwell et al., 2018;Haubrock et al., 2021), including invasive species (Poulin et al., 2011;Strayer, 2010). Globally, invasive non-native species are a major driver of erosion of native biodiversity and the disruption of ecosystem functioning (Blackburn et al., 2019;Malcolm & Markham, 2000;Stigall, 2010). Furthermore, they are a burgeoning economic stressor on virtually all resource sectors-especially those associated with inland waters, where they are several times more likely than natives to become socio-economic pests (Hassan & Ricciardi, 2014). Indeed, invasion rates worldwide have been steadily increasing with no sign of saturation (Seebens et al., 2017), owing to increasing globalization, intensification of global transport networks and accessibility of new non-native source pools (Seebens et al., 2018). At present, most countries have limited capacity to manage invasions (Early et al., 2016) and are increasingly forced to make decisions regarding investment in biosecurity versus other societal needs.
In recent years, the ecological impacts of invasive species on recipient ecosystems have been quantified (e.g., Crystal-Ornelas et al., 2021;Dick et al., 2017;Kumschick et al., 2015). However, while categorizations for invader socio-economic impacts have been designed , there remains a paucity of quantified socioeconomic costs for key taxonomic groups, hampering effective cost-benefit analysis and rationale for policymakers to invest the sparse available resources towards prevention and control (but see Cuthbert, Pattison, et al., 2021;Diagne et al., 2021, for analyses at the global scale across taxa). This constraint to invest still exists even though it has been shown that preventive measures are generally considered more cost-effective than long-term damages and control Keller et al., 2008), with pre-invasion management remaining underfunded (Leung et al., 2002). Indeed, proactive preventative measures have the potential to yield trillion-dollar savings over just a few decades compared with delayed management actions . Accordingly, as invasions are increasing globally (Seebens et al., 2017;, it is important to document the economic costs of taxonomic groups known to include damaging invasive species, as it could help to inform decision-making at the national level and thus provide appropriate economic incentives for proactively managing the arrival and spread of such species. A group of aquatic invasive species that has caused significant ecological and socio-economic impacts are freshwater bivalves Sousa et al., 2009Sousa et al., , 2014, including, inter alia, several hyper-successful invasive species from the genera Dreissena, Limnoperna and Corbicula (Bódis et al., 2014;Boltovskoy et al., 2006;Karatayev et al., 2007;Sousa et al., 2008). These taxa have caused a broad range of impacts, such as macrofouling, habitat modification, restructuring communities and food webs, nutrient mineralization, contaminant transfer, alteration of oxygen availability and sedimentation rates, and promotion of excessive macrophyte and algal growth (see reviews by Boltovskoy et al., 2006;Karatayev et al., 2007;Ward & Ricciardi, 2007). Recognized as ecosystem engineers, invasive bivalves have a particularly marked effect on suspended particle concentrations and water clarity by filter feeding, as well as sediment bioturbation and the provisioning of shells, which alter habitat . In turn, they affect various sectors of society (e.g., infrastructure, municipal and industrial water supply systems, and fisheries; Hoyle et al., 1999;Minchin et al., 2002;Waterfield, 2009). Arguably, the enormous costs associated with invasive bivalves such as the Asian clam Corbicula fluminea and the zebra mussel Dreissena polymorpha have done more to raise public awareness of aquatic invasions than their respective ecological impacts, although the economic and ecological impacts are often linked (e.g., Kao et al., 2016). On the contrary, invasive freshwater bivalves have, on occasion, been associated with certain perceived beneficial effects for human activities, as with other invaders . For instance, their filtration capacity can substantially increase water clarity (Boltovskoy et al., 2009;Higgins & Vander Zanden, 2010;Phelps, 1994), which may benefit certain recreational activities (e.g., scuba diving and angling), while at the same time causing food web disruptions that harm fisheries (Kao et al., 2016).
Despite the notoriety of invasive freshwater bivalves in invasion science, information on their economic costs has not been synthesized. To broadly address this pervasive lack of information and provide a basis for quantifications of costs associated with invasive species worldwide, the InvaCost database has recently been developed (Diagne et al., 2020). This database contains extensive information on the costs (e.g., cost types, impacted sectors, regional attributes, cost estimation reliability) associated with ~500 invasive species. In the present study, we use a subset of the database to describe global costs associated with invasive freshwater bivalves and how they are structured, anticipating unevenness in cost reporting towards a few regions and a few highly conspicuous invasive species.

| Original data
To estimate the cost of bivalve invasions of freshwaters on the global economy, we considered data from the latest version of the InvaCost database at the time of writing this manuscript (version 4.0; full database and descriptive files are available at https://doi.org/10.6084/

K E Y W O R D S
Cyrenidae, Dreissenidae, InvaCost, macrofouling, mussel, non-native, socio-economic impact m9.figsh are.12668570). We note that although some IAS can provide both benefits and costs to economies (Kouranditou et al., 2022), InvaCost does not quantify benefits provided by IAS and potential beneficial effects are thus outside the scope of this study. This database (13,123 entries; Diagne et al., 2020;Angulo et al., 2021) compiles entries that extensively describe documented costs globally, enabling large-scale cost syntheses associated with invasive species in different spatial and temporal frames. Grey and published references were retrieved from standardized searches in online repositories (Web of Science, Google Scholar and Google search engine) and opportunistic collection based on targeted searches. Full information on the search terms (see Appendix S1) is provided in Diagne et al. (2020) and Angulo et al. (2021). Gathered references were thoroughly examined to assess relevance and then scrutinized for collating cost estimates associated with invasive species. Every cost entry was recorded, depicted by 64 parameters, and finally converted to a common and upto-date currency (US dollars (US$) 2017; see Diagne et al., 2020, for detailed information; Appendix S2). From this full database, 241 cost data entries were identified as exclusively belonging to the Bivalvia class using the "Class" column filter and 233 cost data entries belonging to bivalves which impact freshwaters (see Figure 1). We therefore excluded fully marine species, but focused on various taxa such as D.

| Estimating the total costs
Deriving the total cumulative cost of invasions over time requires consideration of the probable duration time of each cost occurrence. This duration consisted of the number of years between those mentioned in the "Probable_starting_year_adjusted" and the "Probable_ending_year_adjusted" columns. When information was missing for the "Probable_starting_year_adjusted" column, we conservatively considered the publication year of the original reference. For the "Probable_ ending_year_adjusted" column, information was missing only for potentially ongoing costs ("Occurrence" column), which are costs likely to be repeated over years (contrary to one-time costs occurring only once along a precise period). We used this temporal information to annualize the invasion cost entries (3 rd step in Figure 1). This was done by "expanding" the database via the expandYearlyCosts function of the "invacost" R package )-a process that causes each entry in the database to correspond to a single year, thereby increasing the number of entries beyond that of the original data.
For example, an initial single cost between 2000 and 2009 that totalled at $ 10,000 would become ten entries at $ 1,000 each after the expansion. All analyses were performed using this version of the database. A full explanation of this and other functions used is available in Leroy et al. (2021). For one cost entry, the probable ending year was presumably after 2020. Hence, all resulting cost estimates projected beyond 2020 were not taken into account.
Similarly, costs were not available before 1980. This resulted in a subset of 461 expanded database entries ( Figure 1). The dataset was then reduced to 461 entries by removing entries before 1980 to ensure comparability of currency translations ("recent" in F I G U R E 1 Successive steps of filtering from the entire InvaCost database to the subset analysed for annualized costs of freshwater bivalves between 1980 and 2020. Each step is detailed in the text (i) Method reliability: illustrating the perceived reliability of cost estimates based on the type of publication and method of estimation. Estimates in peer-reviewed publications or official reports, or with documented, repeatable and/or traceable methods were designated as high reliability; all other estimates were designated as low reliability (Diagne et al., 2020). We acknowledge that this approach, which categorizes costs as high reliability based on their presence in peer-reviewed or official material, may not be fully representative of the diverse forms of method reliability of cost estimates. Nevertheless, these criteria provided clear, objective and reproducible means of assessing material, as it was not feasible to assess method reliability on a broader categorical scale; (ii) Implementation: referring to whether the cost estimate was actually realized in the invaded habitat (observed) or whether it was extrapolated (potential), based on the methods reported in the underlying study (i.e. we did not perform extrapolations ourselves); (iii) Geographic region: describing the geographic origin of the listed cost; (iv) Type of cost merged: grouping of costs according to the categories: (a) damage costs referring to damages or losses incurred from invasion (e.g., costs for damage repair, resource losses, medical care), (b) management costs comprising control-related expenditure (e.g., monitoring, prevention, management, eradication) and money spent on education, research and maintenance costs, and (c) mixed costs including mixed damage and management costs (cases where reported costs were not clearly distinguished among cost types). We note that management costs include also research spending, irrespective of the findings, because this work often aims to better understand the ecology of invaders and their impacts, in turn informing management options; (v) Management type: breaking down if management costs were incurred by pre-invasion management (i.e. costs inferred from, e.g., early detection, biosecurity and/or monitoring efforts) and postinvasion management (i.e. costs inferred from control and/or eradication efforts), or rather originated from research-related efforts (knowledge funding); and (vi) Impacted sector (i.e. the activity, societal or market sector where the cost occurred; see Appendix S4). Individual cost entries not allocated to a single sector were modified to "mixed or unspecified".

| Temporal dynamics of costs
We analysed the economic costs of invasive macrofouling bivalves over time. For this, we used the summarizeCosts-function implemented in the R package "invacost" .
With this method, we calculated the observed cumulative and average annual costs between 1980 and 2020 considering 10year intervals.

| Economic costs among bivalve families
The

| Economic costs among method reliability and implementation types
Although constituting the majority of cost entries (n = 346), highly reliable cost estimates comprised only 10% of the documented total cost ($ 6.2 billion), with the remaining costs not originating from accessible peer-reviewed or official sources. Observed costs accounted for 77% of costs from freshwater bivalves ($ 49.0/63.7 billion; n = 340/461), whereas other potential costs were derived in the absence of the invader in the study area based on observed costs in other regions (i.e. in the case the species were to be introduced) or based on extrapolated predictions of an existing impact over time (see Diagne et al., 2020, for details

| Economic costs among geographic regions and cost types
Approximately 98% of the total costs were incurred in North Cyrenidae costs were also mostly in North America ($ 12.4 billion; n = 9), with some coverage in Europe ($ 6.2 million; n = 19). No invasive bivalve costs were reported for Africa, Asia or Oceania. All costs of the family Mytilidae (L. fortunei; n = 46; $ 0.14 billion) were incurred in South America, while the two cost entries of Unionidae (S. woodiana, $ 0.02 million) were incurred in Europe.
With respect to cost types, 48% of the total bivalve-related cost was categorized as due to damages or resource losses ($ 30.5 billion; n = 98), with relatively little (3%; $ 1.7 billion; n = 293) spent on management singularly (Figure 3b). The largest share of the total cost (49%; $ 31.5 billion; n = 70) was, however, categorized as general (mixed) as F I G U R E 3 Global costs of recorded invasive freshwater bivalve taxa according to the affected continent (a) and cost type (b). The colour ramp corresponds to cost entries they contained elements relating to several cost types and were thus not specific. Dreissenidae costs were largely mixed in type, followed by exclusive damages, then management. For Cyrenidae, the majority of costs was due to damages, whereas most of the remainder was associated with mixed management and damages. Mytilidae costs were distributed relatively minorly across all cost types, whereas Unionidae was solely management-related. For the $ 1.7 billion in total management costs, $ 1.6 billion was invested reactively post-invasion, whereas only $ 0.002 billion was invested proactively pre-invasion, and with just $ 0.04 billion spent on knowledge funding.

| Economic costs across North American sectors
In North America specifically, where the vast majority of bivalve costs were reported, 10% ($ 6.2 of 62.4 billion) of the total bivalve cost was incurred by mixed or unspecified socio-economic sectors

| Economic cost accumulations through time
Average costs between 1980 and 2020 are presented in Figure 5. In total, these costs remained at a consistent magnitude over the past decade and amounted to $ 63.7 billion, with an average annual cost over the entire period of $ 1.55 billion. Whereas the effects of timelags in cost reporting were not incorporated into analyses, average cost estimates became reduced slightly towards the end of the last decade, indicating a temporal gap in cost reporting.

| DISCUSS ION
The present study demonstrates massive economic costs associated with invasive freshwater bivalves, estimated at a total of $ 63.7 billion over the period 1980-2020. The resulting average annual cost of $ 1.55 billion is approximately half the 2020 United Nations budget (https://news.un.org/en/story/ 2019/12/1054431).
Invasive freshwater bivalves can transform entire ecosystems, thereby affecting fisheries and other resources of economic importance (Hansen et al., 2020;Kao et al., 2018;Strayer et al., 1999). fluminea are global invaders (Sousa et al., 2008), and thus, a lack of cost estimation for such taxa on a wide scale is surprising and indicates a profound lack of reporting. Furthermore, few documented costs were reported for the golden mussel L. fortunei, which is invasive in South-East Asia and South America (e.g., Boltovskoy & Correa, 2015;Sousa et al., 2014). Accordingly, the current availability of costs identified is inherently species-specific, and thus, costs likely represent a gross underestimation of the full scale of economic impacts across taxonomic groups, given the range of impact types associated with many macrofouling freshwater species and entirely unreported groups (Sousa et al., 2009. This is further evidenced by our results, in that just six known freshwater invasive bivalves had reported costs-which are themselves likely underestimated numbers. On a taxonomic level, the present study found that some key species of freshwater bivalves with well-known invasion histories (e.g., the golden mussel L. fortunei, the false mussel Mytilopsis trautwineana, the Chinese pond mussel Sinanodonta woodiana) account for only a few entries in the InvaCost database, owing to a lack of published or traceable cost data. Macrofouling induced by L. fortunei and M. leucophaeta (a predominantly brackish-water species that was not represented in InvaCost), in particular, has been recognized as an economic problem for South America and Europe, respectively, where they foul municipal and industrial water supply systems (Verween et al., 2010). Concomitantly, the lack of costs of clogging due to Dreissena sp. invasions in, for example, Europe is an obvious lack of reported cost data (Adams, 2010). Indeed, the zebra mussel invaded most of the waterways in central and western Europe well before the mid-20th century (Dedi ͡ u, 1980;Padilla, 1997).
Moreover, the geographic unevenness of cost estimations towards North America and the complete lack of documented cost estimation within Asia, Africa and Oceania reflect major knowledge gaps in the economic costs of invasive bivalves spatially. In the case of North America, it may be possible that early estimates for invasion costs in the United States led to greater reporting efforts for invasion economic effects in the last two decades (Pimentel et al., 2000). Furthermore, there is a characteristic discrepancy in the importance, valuation and the spatial size of lakes in North America (i.e. the Laurentian Great Lakes) and riverine ecosystems in Europe, which has likely led to an imbalance in the research effort and impacted sectors. Accordingly, we speculate that this produced a baseline bias leading to unevenly reported costs in Europe-in contrast to the sudden incursion and recognition of massive costs following the more recent invasion of North America. Moreover, zebra mussel densities in the Great Lakes reached peaks that were 1 -2 orders of magnitude larger than what is typically reported in Europe, probably because as invasions progress, mussel densities tend to level off at a lower equilibrium density (Burlakova et al., 2006;Jernelöv, 2017). Less than 1% of the globally reported costs of invasive bivalves was estimated from solely within Europe or South America, but an absence of evidence is not evidence of absence, suggesting that the real costs may be several magnitudes higher. In line with this argumentation, it is likely that regional biases are-at least in partexplainable by language barriers, and thus, relevant costs have not yet been identified in some regions . The annual average cost of $ 1.5 billion is lower than the previous annual cost estimation ($ 2 billion) for the zebra mussel and Asian clam in the United States (Pimentel et al., 2005). However, here we explicitly account for temporal dynamics in costs over a longer period, using a more conservative methodology and more robust data than the heavily criticized approach presented by Pimentel et al. (Hoffmann & Broadhurst, 2016). Our analyses indicated that studies reporting invasive freshwater bivalve costs have remained at a similar magnitude in recent decades. While average decadal cost estimates tended to decline slightly in recent years, this is likely to be an artefact of time-lags in cost estimation, rather than an empirical reduction in economic impact. The relative stability in cost increases for freshwater bivalves might also relate, in some cases, to improved management efficiencies-in spite of increases in both invasive species numbers (Seebens et al., 2017) and global invasion costs ( Isom (1986) to exceed $ 1 billion per year, based on various anecdotal costs recorded primarily before 1980. Our approach led us to ignore all costs prior to 1980, despite C. fluminea having invaded the United States and other regions many decades before (Crespo et al., 2015). Further, these costs only pertain to power plants in the United States, whereas C. fluminea is globally invasive and has fouled water supply systems in other countries. In addition to impacts on technological systems, C. fluminea is known to negatively impact native bivalve abundance and diversity (Sousa et al., 2008), and to alter physical habitat structure including water quality, sediment composition and submerged vegetation (Phelps, 1994), thus producing ecosystem impacts that can be difficult to quantify in monetary terms (Darrigan, 2002). It should be emphasized therefore that we consider the presented costs to be highly conservative overall, particularly given the prominent cost reporting gaps, both taxonomically and spatially. Inclusion of less reliable material, such as that with unclear temporal duration, could cause costs to be substantially higher than documented here.
Another factor contributing to uncertainty surrounding our estimate is the difficulty in quantifying types of economic damage associated with ecosystem services (Spangenberg & Settele, 2010).
Invasive freshwater bivalves can be ecosystem engineers where they have substantial effects on ecosystem structure and functionand thus the various services they can provide to humans (e.g., aquaculture, water purification, sourcing of raw materials). For instance, dreissenid mussels indirectly stimulate benthic algal growth (Boegman et al., 2008), invasive aquatic weed proliferation Zhu et al., 2006Zhu et al., , 2007 and harmful algal Microcystis blooms (Vanderploeg et al., 2001) The sparse economic data for invasive freshwater bivalves also inhibit recognition of any potential benefits these species provide to humans, and thus impede comprehensive cost-benefit analyses, which could further inform and direct management actions among different economic sectors or regions (Kouranditou et al., 2022).
For example, filtration activities of dense populations of Dreissena spp. and C. fluminea have been shown to substantially increase water clarity (Boltovskoy et al., 2009;Higgins & Vander Zanden, 2010;Phelps, 1994). These, while causing myriad ecological disruptions and harming fisheries whose focal species depend on prey that are competing with mussels for resources (Kao et al., 2018), could benefit certain recreational activities such as scuba diving.
Concomitantly, this could conceivably drive tourist revenue and increase the property value of neighbouring real estate. Conversely, accumulations of sharp shells on beach sands are a hazard to the feet of swimmers (Ilarri et al., 2011;Ilarri & Sousa, 2012). While many beneficial effects are difficult to quantify in monetary terms, or are yet to be shown, it is unlikely that they will outweigh the presently documented (and underestimated) costs of $ 63.7 billion.
Overall, our study highlights very fragmented data that call for national and regional authorities to produce more and better struc- investments-especially in pre-invasion management-increase the costs ultimately incurred via post-invasion management and damage . Therefore, the fact that management spending is a fraction of damages incurred suggests that not enough is being invested, and particularly in proactive biosecurity measures pre-invasion to prevent secondary spread, as well as in the few measures to rapidly eradicate populations at early invasion stages (e.g., Tang & Aldridge, 2019). Preinvasion biosecurity measures such as ballast-water managementtreatment (Bailey, 2015;Ricciardi & MacIsaac, 2022), the cleaning of boats and fishing equipment between waters (Coughlan, Bradbeer, et al., 2020), and the establishment of rapid response teams (Caffrey et al., 2018) could be effective yet less cost-intense means to prevent further spread and new arrivals.
Indeed, when specific cost types were known for invasive freshwater bivalves, damages and resource losses were an order of magnitude higher than control or management costs. Given that invasion rates are expected to keep increasing over time (Seebens et al., 2017;, we suppose that the costs of invasive macrofouling freshwater bivalves will increase substantially in future, leading to staggering costs for stakeholders and governments (Scalera, 2010). This calls for an increase in efforts to quantify costs of invasive freshwater bivalves to fill knowledge gaps and to improve the ability to prioritize targeted management interventions. These knowledge gaps could be partly resolved by improving the reporting of cost information in a publicly available form, such that data can be readily captured and included in InvaCost via systematic literature searches. Further research efforts are also required to quantify costs for understudied taxa and parts of the world with lower research capacity, where ecological but not economic impacts are known. Nevertheless, the already substantial costs warrant greater management efforts immediately to curtail the further arrival and spread of existing and emerging macrofouling freshwater bivalves, by providing rationale to invest for stakeholders and decision-makers.

ACK N OWLED G EM ENTS
The authors acknowledge the French National Research Agency (ANR-14-CE02-0021) and the BNP-Paribas Foundation Climate Initiative for funding the InvaCost project that allowed the construction of the InvaCost database. The present work was con-

CO N FLI C T O F I NTE R E S T
The authors declare no conflicts of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
The data used in this work are available as supporting information.