Aquatic invasion patterns across the North Atlantic

Biological invasions are a major driver of biodiversity loss and socioeconomic burden globally. As invasion rates accelerate worldwide, understanding past invasion dynamics is essential to inform predictions of future invaders and impacts. Owing to a high diversity of pathways and current biosecurity gaps, aquatic systems near urban centres are especially susceptible to alien species establishments. Here, we compiled and compared alien species lists for three different aquatic recipient regions spanning the North Atlantic: Chesapeake Bay, Great Lakes‐St. Lawrence River and North and Baltic Seas. Each system is a major trade centre, with a history of invasions, and characterized by a strong natural salinity gradient. Our goal was to compare the alien species across systems, to test for similarities in the taxonomic composition and geographic origin as well as species overlap among the three regions. We selected specific macroinvertebrate, algal and fish taxa for analysis, to control for uneven taxonomic and biogeographic resolution across regions. Cumulatively, we identified 326 individual alien species established in these aquatic systems, with the North and Baltic Seas most invaded overall (163), followed by Great Lakes‐St. Lawrence River (84) and Chesapeake Bay (79). Most invasions were from Ponto‐Caspian, Eurasian, Northwest Pacific, Northwest Atlantic and North American origins, and mostly comprised Arthropoda, Chordata, Mollusca and Annelida. However, origins and taxonomies differed significantly among destinations, with Ponto‐Caspian species particularly successful invaders to the North and Baltic Seas then Great Lakes‐St. Lawrence River, but less so to Chesapeake Bay. Nevertheless, approximately eight‐tenths of invaders established in only one region, indicating disparate invasion patterns and a high potential for future aliens to accrue from increasingly diverse source pools and pathways. These results support biosecurity strategies that consider a broad range of geographic origins and taxonomic groups to limit the translocation, arrival and spread of alien species worldwide.


| INTRODUC TI ON
Human-mediated movements of species have significantly altered biogeography, biodiversity and community structure worldwide, as well as caused substantial socioeconomic burdens and losses of ecosystem services (Blackburn et al., 2019;Capinha et al., 2015;Turbelin et al., 2017). Alien species accumulations have accelerated among many taxonomic groups and locations in recent centuries (Seebens et al., 2017). These anthropogenic introductions have stemmed from increased globalization of trade and transport networks (Bonnamour et al., 2021;Hulme, 2009), greater accessibility of alien species source pools (Seebens et al., 2018), habitat modifications (Pauchard & Alaback, 2004) and climate changes (Hellman et al., 2008). As these processes intensify, rates of invasion are expected to continue in future, with alien species establishment projected to increase by 36% in coming decades worldwide (Seebens et al., 2021). In tandem, biological invasions have accrued massive economic costs across a range of human activity sectors , culminating in a stark economic burden to national economies (Cuthbert, Bartlett, et al., 2021). To aid predictive efforts for future invasions and their impacts, it is essential to understand the past geographic and taxonomic patterning of invasion dynamics.
Historically, alien species have been transported through a range of pathways, both deliberately and accidentally. Accidental introductions have arisen due to commercial trade and travel, such as via ship ballast (Briski et al., 2013), wooden packing materials (Brockerhoff & Liebhold, 2017) and soils for horticulture (Hulme et al., 2008).
Intentional introductions have arisen due to perceived benefits of alien species associated with past colonialism (Pipek et al., 2020), pet trades (Toomes et al., 2020), religious activities (Wasserman et al., 2019) and classical biological control (Shine et al., 2020), among others. Whilst many species fail to establish following introduction along the stage-based invasion process (Blackburn et al., 2011;Colautti & MacIsaac, 2004), aliens from certain regions might be more likely to succeed than others (Casties et al., 2016;Cuthbert et al., 2020).
Centrally, the importance of propagule (i.e. numbers and viability of individuals) and colonization (i.e. numbers of species) pressures for invasion success (Briski et al., 2012;MacIsaac & Johansson, 2017) means population characteristics such as tolerance to diverse environmental conditions and phenotypic plasticity may facilitate the probability of invasion (Lande, 2015). In turn, these traits may be inextricably linked to the environmental origin and taxonomic grouping of species, whereby past environmental heterogeneity could promote traits that enhance invasion success (Reid & Orlova, 2002).
Aquatic ecosystems are particularly vulnerable to invasions and their impacts (Darwall et al., 2018), with detection rates of aquatic invasions rising rapidly in recent decades and showing little sign of saturation (Bailey et al., 2020). In recent centuries, distinct aquatic biogeographic regions have been principally connected via global shipping networks (Kaluza et al., 2010), but shipping intensities vary markedly along different routes. In particular, regions such as Northern Europe (Northeast Atlantic) and Northwest Atlantic have been found to exhibit among the highest invasion risks associated with shipping intensity worldwide (Seebens et al., 2013). Similarly, over time the taxonomic composition of aliens and their pathways (i.e. the processes that facilitate introduction) may shift with changing trade patterns and regulations (Ellis et al., 2013;Ricciardi, 2006). This may contribute to asynchronous invasion dynamics spatiotemporally. For example, changes from solid ballast to ballast water systems caused reduced translocations of terrestrial plants, but increased aquatic animal invasions in the Great Lakes (Ricciardi, 2006).
However, considerations for factors other than shipping intensity and trade patterns are needed to robustly predict invasions.
Recent work has proposed that aquatic taxa from certain geographical origins are better able to invade than others, with invasion rates exceeding expectations based simply on propagule supply or shipping intensity (Casties et al., 2016). Ponto-Caspian taxa from the Black, Caspian and Azov Seas have been identified as alien species with such a propensity to invade northern Europe and the Great Lakes-St. Lawrence River in North America (Leppäkoski et al., 2002;Ricciardi & MacIsaac, 2000). Similarly, studies have highlighted the disproportionate contributions from the Ponto-Caspian region globally when considering invasion dynamics of key taxonomic groups, such as gammarid crustaceans . The evolution of tolerance to harsh salinity-temperature heterogeneities may predispose Ponto-Caspian species to invade wide-ranging aquatic conditions worldwide Pauli et al., 2018).
However, tests of generalities in invasion dynamics according to species origin lack examination across a broad range of recipient regions, hampering effective management actions and predictive power.
Here, we examined trends in invasion dynamics in three major aquatic regions with very high shipping intensity across the North Atlantic Ocean (Kaluza et al., 2010): Chesapeake Bay, Great Lakes-St. Lawrence River and North and Baltic Seas. Shipping has historically been a pervasive pathway for the introduction of alien species among these regions, and the composition of aliens introduced reflects distinct phases associated with the nature of ships' ballast (Ricciardi, 2006 (Ricciardi, 2006). However, recent improvements to ballast management systems have reduced numbers of species invading to the Great Lakes substantially (Sturtevant et al., 2019). Whereas Chesapeake Bay has only received relatively recent connection to the Great Lakes via canals, major ports such as Baltimore and Norfolk have among the highest ship arrival numbers in the United States, and particularly from Europe, resulting concurrently in a high rate of invasion (Fofonoff et al., 2013;Seebens et al., 2013).
These three systems have received high research effort compared to other regions, enabling sufficient data quality for analyses with a relatively high quantity of reported alien species. Salinity regime is a primary mediator of aquatic invasions Ojaveer et al., 2010;Paiva et al., 2018), and each of these aquatic regions is also characterized by a marked natural salinity gradient ranging from the ocean to freshwater (Figure 1 in multiple regions, and in doing so, examined whether the majority of invasions to these regions are from unique species, or whether alien species co-occur among destinations. The former would suggest that, hitherto, invasions follow a seeming independent pattern at the species level, whilst the latter would indicate that invasions are dominated by a select group of recurrently successful taxa. Overall, these findings help to characterize dominant donor regions and taxonomic groupings for aquatic alien taxa, informing future predictions and management strategies that seek to limit translocations and introductions via early-stage invasion management (Leung et al., 2002).

| Alien species lists
Lists of aquatic alien species were compiled for three aquatic regions in two continents (North America and Europe) with substantial natural salinity gradients: (i) Chesapeake Bay; (ii) Great Lakes-St. Lawrence River; and (iii) North and Baltic Seas (see Cuthbert, Kotronaki, et al., 2021; Figure 1). We selected these systems because they (i) are well-studied invasion hotspots with sufficient data for comparison; (ii) exhibited historic trade connectivity in recent centuries; and (iii) represent the geographic scale over which their data have been aggregated in previous studies (Casties et al., 2016;Fofonoff et al., 2020). For each system, we synthesized available data (as below), and corrected any errors discovered (i.e. homogenizing taxonomic names, refining geographic origins and removing species which were not evidently established), based on current information available in 2021. Furthermore, owing to differences in how aquatic habitats and taxa were defined among lists, we standardized the taxa included in our analyses, focusing on larger taxa that are more easily detected and recognized. Specifically, we opted to remove flowering plants, insects and mammals, as often their habitats are located away from bays, and the boundaries for each system were not consistently defined among databases. We also removed phytoplankton as they are often cryptogenic, as well as microorganisms. We acknowledge that this caused conservative estimation of alien species numbers, but permitted comparability among regions.
Species lists for Chesapeake Bay were initially obtained from the National Exotic Marine and Estuarine Species Information System (NEMESIS; Fofonoff et al., 2020). This database is the most comprehensive account of alien species in Chesapeake Bay and the adjacent Atlantic water and coastal bays. The coverage area also includes F I G U R E 1 Salinity of Chesapeake Bay, Great Lakes-St. Lawrence River, North Atlantic Ocean, North, Baltic, Mediterranean, Black, Azov and Caspian Seas, constructed using average annual salinity data with a 1° × 1° spatial resolution from the World Ocean Atlas database (Antonov et al., 2006;Casties et al., 2016) and Wei (2019) (a). Close-up maps of Chesapeake Bay (b), the Great Lakes-St. Lawrence River (c) and the North and Baltic Seas (d) are shown. Note that although the salinity of the Great Lakes is shown in the range from 0.0 to 4.1 (i.e. dark blue), the salinity of the Great Lakes is under 0.5 ppt (i.e. freshwater). The solid line on (c) demarks the Gulf of St. Lawrence the tributaries of the bay up to the head of tidewater, as well as tidal wetlands up to the monthly mean high tide line (0-32 ppt).

The Great Lakes-St. Lawrence River and North and Baltic Seas lists
were compiled as per Casties et al. (2016). For the Great Lakes-St.

| Geographic origins
To examine whether aliens from a particular origin region or taxonomic group were contributed more than others, we compiled geographic origin information and taxonomic grouping (kingdom, phylum and class) for each listed alien species. For Chesapeake Bay, alien origins were determined from the NEMESIS database , whereas origin information for the Great Lakes-St.
Lawrence River and North and Baltic Seas was taken from GLANSIS (2014) and AquaNIS (2015) respectively. Where information for species origins was absent, a general internet search was conducted using a search engine.
Each alien species was assigned an origin based on one or more of the following regions (Casties et al., 2016) Rivers), South America (inland freshwaters), Ponto-Caspian region and unknown region. Where a species invading a given region was native to several origins, the contribution from that species was divided by the number of origins (i.e. ratio of 1 over the number of origins). For example, a species with two origins was assigned a value of 0.5 per origin. This ensured that each species' contribution was balanced among regions, however, we did not divide species contributions among recipient regions (i.e. if the same species invaded multiple regions), as they represent independent invasion events.
Nevertheless, we acknowledge that not all origin regions contribute equally to invasion events given differences in vectors and timings.
For most invasions, however, the relative importance of each origin is not documented, and therefore, the simple ratio methodology was employed here. We assigned taxonomic information for each species using several sources [e.g. Barcode

| Formal analyses
Compositions of alien species were examined and compared among the three recipient regions according to geographic origins and taxonomic groupings. Separate pairwise Chi-square tests were used to test the null hypotheses that invasions to each aquatic system were proportionally from the same groups of species origins and phyla.
That is, we compared numbers of alien species to each of the three regions pairwise according to the top five most common species origins (two recipient regions × six origin groups, per pair). Similarly, we repeated these tests to compare the top five phyla compositions among recipient regions. Furthermore, we examined similarities in invasion patterns among systems by determining individual species that invaded more than one region, with respect to their geographic origin and taxonomic grouping.

| DISCUSS ION
This study identified differences in invasion dynamics among three interconnected aquatic systems in the North Atlantic that have a natural salinity gradient. Invasions have originated from a broad range of geographic origins and taxonomic groups. We found that invasions to Chesapeake Bay were dominated by taxa of North are not universal characteristics that inform invasion success, and that management actions should seek to limit invasions from a broad range of source pools and taxonomic groups. Equally, a more limited approach that considers region-specific invasion contexts, from certain geographic origins or taxonomic groups, may aid finer scale predictive efforts.

The high levels of Eurasian origin species establishing in both
North American systems probably arise from the strength of connection between North America and Europe considering global shipping (Kaluza et al., 2010;Seebens et al., 2013). In turn, ballast water likely permitted increased introductions of Arthropoda and Mollusca, which are able to produce dormant life stages and/or occupy pelagic areas of waterbodies (Briski, Bailey, et al., 2011, Briski, Ghabooli, et al., 2011 and can sometimes withstand ballast water treatment (Lin et al., 2020). The burgeoning numbers of Chordata introduced, mostly fish (85%), are primarily intentional additions for recreational angling or fisheries, plus some movements through canals (Ricciardi, 2006), with few stowaways associated with shipping.
In general, the larger numbers of invaders in the North and Baltic F I G U R E 3 Numbers of individual alien species invading more than one recipient region, among Chesapeake Bay (CB), Great Lakes-St. Lawrence River (GLSL) and North and Baltic Seas (NBS). Fills correspond to alien origins (a) and phyla (b). Numbers correspond to the number of species in each fill category. Species in all three regions are not included in bars for two regions. 'Other' includes origins which contributed fewer than two alien species overall. Note that, within regions, if an alien had several origins, the contribution of that species was divided among those origins (i.e. ratio of 1 divided by the origin number) Seas likely also reflect differences in the size of that aquatic system relative to those examined from North America. These higher numbers may also reflect historical trade patterns associated with colonialism by Europe, facilitating alien species to accrue earlier than in North America.
Salinity tolerance is a major environmental context that influences invasion success and aquatic ecosystem structuring Stern & Lee, 2020). ports, promoting establishment of species with ranging salinity tolerances, whereas ballast water in Chesapeake Bay is predominantly discharged in higher salinity areas (e.g. Norfolk), which might constrain the establishment of Ponto-Caspian taxa that perform better at lower salinities .
Research has suggested that Ponto-Caspian origin taxa are evolutionarily predisposed to invade (Bij de Vaate et al., 2002;Leppäkoski et al., 2002;Ricciardi & MacIsaac, 2000), owing to historic environmental heterogeneities that permit tolerance to a wide range of aquatic environments (Reid & Orlova, 2002;Paiva et al., 2018; but see Paiva et al., 2020). Recent works have also highlighted the dominance of salt-tolerant taxa from the Ponto-Caspian region in freshwater invasions , and shown that their invasion success is significantly higher than expected based on shipping intensity and environmental match (Casties et al., 2016).
However, our results suggest that these proposed general patterns of invasion frequency by region are not observed for another highly connected aquatic ecosystem in North America, Chesapeake Bay.
Just six of the 79 known established aliens in Chesapeake Bay were of Ponto-Caspian origin, and five of these species also invaded the Great Lakes-St. Lawrence River and/or North and Baltic Seas regions. This indicates that their invasion to Chesapeake Bay may be secondary in source from other 'stepping stone' regions, or vice versa. Whilst Ponto-Caspian taxa are highly tolerant to freshwater and brackish conditions Pauli et al., 2018), this lack of invasion to the extensively brackish Chesapeake Bay suggests that other ecological or socioeconomic (e.g. trade and transport patterns) context dependencies are at play in mediating invasion success, and these require further elucidation. It is also possible that seasonal fluctuations in salinity regime in Chesapeake Bay, and higher salinity regimes at key ports, preclude the establishment of Ponto-Caspian taxa that show decreased performance at higher salinities . Accordingly, whilst Ponto-Caspian species have undoubtedly been disproportionately successful invaders to certain aquatic ecosystems (Casties et al., 2016 to ballast water-coupled with reported intentional species introductions to biologically enhance man-made ecosystems (Arbačiauskas et al., 2010).
Despite the dominance of a few geographic origins and taxonomic groups, at the species level, invasions were found to be largely unique in each of the three regions. Over eight-tenths of established aliens were only reported in one region, despite the intensive interconnection between these three North Atlantic systems (Kaluza et al., 2010;Seebens et al., 2013). Globally, invasions are expected to increase markedly in the future (Seebens et al., 2021) owing to the increased availability of novel source pools that permit alien species translocations (Seebens et al., 2018). With aquatic invasive species also accumulating rapidly (Bailey et al., 2020), it is possible that many species simply have not had sufficient chances to invade multiple systems considering propagule and colonization pressures (Briski et al., 2012(Briski et al., , 2014MacIsaac & Johansson, 2017). Equally, abiotic and biotic characteristics might entirely negate invasion success in certain systems.
In any case, this seemingly random distribution of alien species among regions thus points to a substantial propensity for future invasions. This is because the numbers of 'chances' to invade will rise as globalization and diversification of trade and transport networks ensue, coupled with often inadequate biosecurity protocols for addressing vectors (Coughlan et al., 2020)-although rapid adoption of ballast water management in many countries may impede certain aquatic invasions (but see Lin et al., 2020).
A further critical consideration in the types of analyses reported here is that, depending on the region of study, the concomitant history of biological and ecological investigations and the availability of taxonomic expertise, many groups of aquatic invasive species remain to be assessed relative to whether they are native, cryptogenic or introduced (Carlton, 2009;Carlton & Fowler, 2018 particularly by Arthropoda, Mollusca and Chordata, may also reflect secondary introductions given the geographical proximity of these systems and connection via canals (e.g. Erie and Champlain canals). In turn, joint invasions to Chesapeake Bay and the North and Baltic Seas were most numerous overall, and largely comprised taxa of marine origin that were so far unable to invade the extensive freshwaters of the Great Lakes. Overall, these invasion dynamics point to complex patterns, suggesting a predominance of individual aquatic invasion events from a broad range of geographic origins and taxonomic groupings. Use of species lists in combination with risk models based on propagule supply and trade could yield further resolution and inform upon invasion dynamics. Considering these systems, there is no strong evidence for globally generalizing invasion probability from specific geographic origins or taxa, although a more limited approach that predicts invasion success in certain regions of certain species from specific sources may prove to be a powerful tool.

| CON CLUS IONS
Burgeoning global invasion rates (Bailey et al., 2020;Seebens et al., 2017)  invaded several systems concurrently. These findings suggest largely disparate pattern of invasions at more granular taxonomic scales, pointing to a high potential for invasions to continue rising in future from novel source pools and pathways (Seebens et al., 2018).
Accordingly, our results continue to strongly support a vector-based approach that seeks to reduce the number of arriving specieswhatever they are, and from wherever their source. Further work is needed to examine invasion patterning with origins and taxonomies across a broader range of recipient regions.

RNC and EB acknowledge funding from the Alexander von
Humboldt Foundation via a Humboldt Research Fellowship and Sofja Kovalevskaja Award respectively. Open access funding enabled and organized by ProjektDEAL.

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