Canals provide wide-ranging economic benefits, while also serving as corridors for the introduction and spread of aquatic alien species, potentially leading to negative ecological and economic impacts. However, to date, no comprehensive quantifications of the reported economic costs of these species have been done. Here, we used the InvaCost database on the monetary impact of invasive alien species to identify the costs of those facilitated by three major canal systems: the European Inland Canals, Suez Canal, and Panama Canal. While we identified a staggering number of species having spread via these systems, monetary costs have been reported only for a few. A total of $33.6 million in costs have been reported from species linked to European Inland Canals (the fishhook waterflea Cercopagis pengoi and the zebra mussel Dreissena polymorpha) and $8.6 million linked to the Suez Canal (the silver-cheeked toadfish Lagocephalus sceleratus, the lionfish Pterois miles, and the nomad jellyfish Rhopilema nomadica), but no recorded costs were found for species facilitated by the Panama Canal. We thus identified a pervasive lack of information on the monetary costs of invasions facilitated by canals and highlighted the uneven distribution of costs.

aquatic environment, habitat connectivity, inequality, InvaCost, invasive alien species, monetary costs

Aquatic invasive alien species (IAS) are a major threat to biodiversity and ecosystem functioning (Ricciardi and Rasmussen 1999; Molnar et al. 2008; Strayer 2010), as well as human health (Galil 2018; Souty-Grosset et al. 2018). New alien species continue to be introduced at increasing rates (Seebens et al. 2017), and the share that becomes invasive brings considerable and increasing economic costs (Diagne et al. 2021a). Recently, an open database which compiled the economic costs of biological invasions (Diagne et al. 2020) has allowed quantification across a variety of geographical regions (e.g. Haubrock et al. 2022a), ecosystems (e.g. Cuthbert et al. 2021) taxa (e.g. Angulo et al. 2022) and languages (Angulo et al. 2021).

Aquatic IAS spread through multiple vectors and pathways, intentionally or unintentionally, through either active or passive transport. For example, they can escape from confinement (Lockwood et al. 2013), be unintentionally translocated as contaminants or parasites of a certain goods item (e.g. food, plants, timber; Lockwood et al. 2013), through hull fouling (Sylvester and MacIsaac 2010; Sylvester et al. 2011) or ballast waters of ships (Briski et al. 2012, 2013). Also, breaching biogeographical barriers allows new or additional species invasions (Gollasch et al. 2006; Kourantidou et al. 2015; Kaiser and Kourantidou 2021) or the further spread of IAS to secondary invaded areas from primary ‘stepping stones’ (Bertelsmeier and Keller 2018). For example, roads and railways represent important corridors for IAS (Hulme 2009), also increasing their propagule pressure (Woodford et al. 2013).

One of the most important pathways that allow the spread of IAS are canals connecting geographically-isolated aquatic systems (e.g. Asth et al. 2021), such as the trans-isthmian Suez and Panama Canals, and the cross continental North Sea-to-Black Sea Rhine-Main-Danube Canal. These highly trafficked strategic canals connect transport networks of critical economic and socio-political value, mainstays of global trade and globalisation (Amato 2020). They considerably reduce travel time and distance (therefore also CO₂ emissions), as well as operating costs to shippers and consumers, thus increasing commerce and economic growth (e.g. Lloyd 2018; Park et al. 2020; Cordoba 2022). Nonetheless, these economic benefits are counterbalanced by facilitated introduction and spread of IAS in goods, vessels, and in water due to increased connectivity. If established, IAS can have detrimental ecological consequences, as well as negative economic impacts (Bij de Vaate et al. 2002; Leuven et al. 2009; Galil et al. 2017; Turbelin et al. 2021).

This paper aims to quantify the known economic costs associated with IAS considered to have been facilitated by canals, enabling active (i.e. self-moving species) or passive (i.e. hitchhiker species) spread of these species. For this study, we focused on three major canal systems: Suez, Panama, and European Inland Canals (Fig. 1), as these represent major circumventions of important biogeographical barriers, and for which greater information is available. In particular, we hypothesised that (i) the Suez Canal majorly contributed to IAS economic costs, that (ii) these costs are not evenly distributed among countries of the same canal system, and that (iii) these costs are attributed to different taxa in different canal systems.

Figure 1. 

Locations of the main canal systems studied (a) the European Inland Canals (b), the Panama Canal (c), and the Suez Canal (d). Red lines represent single canals. As for the European Inland Canals, only the three major canals (the Rhine-Main-Danube Canal, the Volga-Don Canal, and the Volga-Baltic Canal) are represented, for simplicity.

A total of 34 established species for the European Inland Canals, 411 for the Suez Canal, and 98 for the Panama Canal were listed to have been facilitated in their introduction and spread by these canals. In the InvaCost database, we identified in total 19 database entries: 8 for European Inland Canals and 11 for Suez. By way of contrast, no recorded costs were available for Panama. After expansion, these entries resulted in 34 annualised cost entries, encompassing 5 species (the fishhook waterflea Cercopagis pengoi and the zebra mussel Dreissena polymorpha for the European Inland Canals and the silver-cheeked toadfish Lagocephalus sceleratus, the lionfish Pterois miles, and the nomad jellyfish Rhopilema nomadica for the Suez Canal) for a total of $42.2 million ($33.6 for European Inland Canals and $8.6 for Suez). The most surprising result is that costs were recorded for only a few species facilitated by the three canals (9% for European Inland Canals, 0.5% for the Suez Canal, and none for the Panama Canal), and this seems not to depend upon the choice of the countries that could be affected by canal-facilitated invaders, but by the general lack of costs reported for those species. Indeed, only a few cost records associated with the listed species were present in the entire InvaCost database (12% for European Inland Canals, 5% for Panama, and 1% for Suez), even for distant countries.

Fig. 2 summarises the recorded costs for European Inland Canals and Suez Canal. There was a clear difference between the two sites in the taxa associated with the costs. In European Inland Canals, all costs were attributed to invertebrates, specifically almost all to molluscs (Dreissena polymorpha, $33.3 million) and just $0.3 million to crustaceans (Cercopagis pengoi). In the case of the Suez Canal, most costs were attributed to vertebrates (Lagocephalus sceleratus and Pterois miles, $8.6 million) with two very high-cost entries recorded and the remainder belonging to Cnidaria (Rhopilema nomadica, about $59,000).

Figure 2. 

Proportions of monetary costs (outer circle) and cost entries (inner circle) between canals analysed (i.e. European Inland Canals and Suez Canal), according to the cost descriptors studied: species, affected countries, method reliability, implementation, type of costs and impacted sectors.

Our analysis also revealed an uneven distribution of the recorded costs. Out of the total 26 countries investigated for the European Inland Canals, only the United Kingdom ($33.3 million), Finland (about $146,000), Russia (about $74,000), and Denmark (about $58,000) reported costs associated with canal-facilitated invasive species. Similarly, only Turkey ($5.5 million), Cyprus ($3.1 millions), and Israel (about $59,000) reported economic costs associated with the Suez Canal, out of the total 23 countries considered. Despite the low number of recorded costs, most of them were attributed to the high reliability category ($31.5 million for the European Inland Canals and $8.2 million for the Suez Canal) rather than the low reliability one ($2.1 million for the European Inland Canals and about $459,000 for the Suez Canal).

The total costs were differently attributed to observed and potential costs in the two canal systems. In European Inland Canals, about $16.4 million of observed costs were recorded against about $17.2 million of potential costs (though this latter result is mostly due to a single very high potential cost recorded). In contrast, in the Suez Canal, costs were mostly associated with observed entries ($8.2 million, with two very high costs recorded) rather than potential costs ($0.4 million). As for the type of costs, the recorded costs for the European Inland Canals were mostly attributed to management ($31.4 million), followed by damage ($2.1 million), and mixed (about $55,000). The recorded costs for the Suez Canal, instead, were mainly associated with damage ($5.5 million) and management ($3.1 million). The invasive species associated with the European Inland Canals were recorded to impact multiple sectors: authorities-stakeholders ($24.4 million), environment ($1.9 million), and fishery (about $220,000). Moreover, additional costs were recorded for other sectors (diverse: $6.9 million). Similarly, the invasive species facilitated by the Suez Canal had recorded impacts on authorities-stakeholders (about $0.5 million), fishery ($6.2 million, with two very high reported costs), and public and social welfare ($1.9 million).

Canals are important corridors for many aquatic IAS, as revealed by the long list of established species that we obtained. The connection of multiple water bodies with distinct ecological communities is well-known to have promoted the spread of numerous invaders (Galil et al. 2008; Leuven et al. 2009; Hulme et al. 2017). These numbers are expected to increase with time, especially after the enlargement of the Suez and the Panama Canals (Galil et al. 2015; Muirhead et al. 2015; Castellanos-Galindo et al. 2020). However, when searching in the InvaCost database for the costs associated with these species, very few entries for very few species (five) were found, even if we opted for an “extensive approach” by including all the countries potentially affected by canal-passing invaders, i.e. not bordering the receiving system directly. This might be unsurprising, as impacts of those species are not well known (hidden below water) or documented in monetary terms, e.g. for the killer shrimp Dikerogammarus villosus, which is widely distributed in Europe (Soto et al. 2022) but only had reported costs from Italy (Tricarico et al. 2010). Also, many of these species could take decades to cause tangible impacts from the moment of their establishment. Moreover, cost data deficiency is common, especially for marine species across many taxa (e.g. Haubrock et al. 2022b; Kouba et al. 2022), countries (e.g. Haubrock et al. 2021a; Renault et al. 2021), and entire regions (e.g. Kourantidou et al. 2021). However, it is very important to stress that this massive lack of data does not mean that there are only a few costs caused by IAS facilitated by the opening of canals, but only that just a few have been recorded or estimated so far. A lack of costs also does not reflect large ecological impacts incurred in these invaded systems, given the challenges for monetisation of environmental effects.

By contrast, the economic benefits arising from commerce through canals such as those examined here can be easily materialised (e.g. Kaluza et al. 2010; Kenawy 2016; Chirosca and Rusu 2021), so that the general perception may be that the benefits far outweigh the drawbacks (Bereza et al. 2020; Cordoba 2022). Indeed, the value from canals includes numerous components that go beyond just income and employment opportunities created locally, but also encompass economic benefits for exporters and consumers of goods at various stages (i.e. from raw materials to consumer goods). Also, some IAS that spread through canals are perceived to have localised benefits, for example for local fisheries (Castellanos-Galindo et al. 2019; van Rijn et al. 2020), without knowledge of their impact. Nevertheless, the results of our analysis show that the data available is insufficient for a trade-off analysis and does not by any means suggest that the benefits of trade facilitated by the canals outweigh the costs of invasions. Since cost-benefit analyses of biological invasions remain difficult, and since beneficiaries are often far removed geographically from the site of environmental damage, this could potentially lead to disparities and social injustices between those parties (countries, stakeholders, economic sectors, and other individuals such as consumers or members of local communities) that benefit from commerce and those that incur the costs of the associated IAS. In turn, this highlights the concepts of environmental accountability, telecoupling and liability from the involved parties at a transnational or even global level (Shafer 2006; Kramarz and Park 2017; Hull and Liu 2018).

Environmental barriers within the respective canal can nevertheless limit the spread of IAS. For example, the Panama Canal is a freshwater canal (mainly composed of Lake Gatun) that marine species need to cross to invade either side. The similar salinity barrier also applies to the Rhine-Main-Danube Canal and the other European Inland Canals, as freshwater conditions in them should prevent the spread of saline species from the Ponto-Caspian region to the North European seas, and the other way around. However, this barrier can halt only stenohaline species actively spreading or fouling the ship hulls, while not impeding biological invasions through ballast waters and sediments (Sylvester and MacIsaac 2010; Briski et al. 2011, 2013). On the other hand, euryoecious species can overcome these barriers. Ponto-Caspian euryhaline taxa have done particularly well in the eastern Baltic Sea because it has low salinity, and many of them have been established in freshwater systems en route from the Ponto-Caspian region to the North and Baltic Seas (Bij de Vaate et al. 2002). In the case of the Suez Canal, the dissolution of the saltbed of the formerly hypersaline ‘Bitter Lakes’, which served as an effective barrier up to the 1960s, and the accelerated seawater warming in the Mediterranean, boosted by ever more frequent and severe marine heat waves, have likely enhanced the rate of successful invasions (Biton 2020; Galil et al. 2022). While the overwhelming majority of species traversed the Suez Canal northwards (the so-called Lessepsian migrations), a few species, for which monetary impacts are yet unknown, have been considered to traverse it southwards (anti-Lessepsian migrations; Bos et al. 2020; Azzurro et al. 2022). Considering the economic and socio-political importance of canals, and that the commerce through them cannot be easily impeded, we suggest that prevention and mitigation measures should be undertaken or reinforced by the canal authorities, to reduce the ecological and economic impact of IAS.

Some limitations of this study originate from the species and the countries considered. Indeed, in most cases, it can only be presumed that an invader was facilitated by a canal during its spread, especially for species established for a long time, which could have been introduced or spread through other pathways. Other, not easily disentangled, intricacies can also occur. For example, Ponto-Caspian species were sometimes intentionally introduced after canalisation in Europe to stabilise or enrich these new habitats (Arbačiauskas et al. 2010). Also, some IAS further spread from these hubs as secondary, ‘stepping stone’ invaders (e.g. Gammarus tigrinus, introduced from North America; Rewicz et al. 2019). Moreover, many stowaway species (like those transported via ballast water, or fouling species) have by now become cosmopolitan, being widely and repeatedly translocated. This makes it difficult to attribute them to specific geographic locations, and therefore to follow their spread and their associated costs (e.g. Amphibalanus amphitrite; Wrange et al. 2016). Ultimately, we note that species spreading in the opposite direction, i.e. towards the Ponto-Caspian region or the Red Sea, had no recorded economic costs, likely because movements of alien species from these systems are predominantly unidirectional (e.g. Galil et al. 2015; Cuthbert et al. 2020). However, documented cost flows may also reflect the availability of data, which may be limited due to sources in certain languages not included in InvaCost, inaccessible or very recent literature, or not having been captured in the search terms underlying the database (Diagne et al. 2020; Angulo et al. 2021). As for the countries considered, it should be acknowledged that even those not directly involved through canals can be affected by their facilitation.

Although we tried to be as inclusive as possible, our results underline the paucity of available data. As such, our estimations should be taken with caution, as complex trading relationships and interconnected introduction pathways meant that not all countries invaded as a consequence of canals could be accounted for, i.e. those not immediately bordering the regions linked by canals and those affected by secondary spread (see fig. 6 in Galil et al. 2021). As the canals considered here are utilised by ships from all over the world, even a very distant country can be affected by hitchhiking species. More focused research is required to elucidate source-sink dynamics for biological invasions and the large-scale effects of pathways and vectors, as well as to quantify the importance of ‘stepping stones’ for invasion events. In an era of economic uncertainty (Baker et al. 2020), severe economic disparities between those benefiting and those negatively affected will have staggering consequences. Highlighting the magnitude of economic costs and sectors affected due to biological invasions (Cuthbert et al. 2021; Diagne et al. 2021b; Haubrock et al. 2021b) evidences the potential threat to economies and human wellbeing. Here, our results highlight the potential for canals to cause substantial economic costs, in addition to their intended economic benefits, as a result of biological invasions – even for the few species with reported impacts – for which knowledge gaps should be further addressed in future. Thus, we are calling for an increasing effort in (i) identifying the ecological impacts and associated costs of biological invasions in canals and the affected parties, as well as (ii) limiting their staggering increase given the predicted intensification in the use of these infrastructures in the future.