The year in which the Chinese mitten crab was first reported in a new region was extracted from the Online Information System on Aquatic Non-Indigenous and Cryptogenic Species (AquaNIS, http://www.corpi.ku.lt/databases/index.php/aquanis/). To identify additional new regional records and map the Chinese mitten crabs’ current distribution, the scientific literature and the Global Biodiversity Information Facility (GBIF, www.gbif.org) were queried. In addition, the following databases were considered as they were not – or not completely – represented in GBIF: Invasive Species Northern Ireland (http://invasivespeciesireland.com), Mitten Crab Watch (http://mittencrabs.org.uk), Centre de Ressources Espèces exotiques envahissantes (http://especes-exotiques-envahissantes.fr), and the Smithsonian Environmental Research Center’s National Estuarine and Marine Exotic Species Information System (https://invasions.si.edu/nemesis) (see Suppl. material 1 for a complete list).

Information on changes in abundance was extracted from scientific publications, reports of researchers, natural resource managers and interviews with fishermen. In particular, the year in which abundance began to increase or decrease was noted. This is a metric that is independent of the way crab abundance was estimated, e.g. catch per unit effort or number of crabs caught per day, and these measures are not comparable across studies.

If the abundance-distribution relationship holds for non-native species, a significant, positive relationship between the number of regional expansion events and the number of regional increases in abundance is expected. All statistical analyses were carried out in the R statistical environment (R Core Team 2019). The years 2010 to present were omitted from the analysis, as new reports on range expansions and abundance fluctuations may not have been published yet (publication time lag) and may therefore be incomplete. We conducted a generalized linear model (GLM) between the annual number of geographic expansions and reported number of regional increases in abundance with a Poisson error distribution. This distribution is best suited to analyse count data.

The Elbe River and associated estuarine ecosystem was used as a case study for the trends occurring in many other large waterways at a European and global scale (Cane et al. 1997; European Environment Agency 2012; Stets et al. 2012; Lopez et al. 2020), partly due to the impulse of the EU Water Framework Directive (2000/60/EG). Moreover, the first non-native discovery of the Chinese mitten crab was near the Elbe, and the Chinese mitten crab has been a continuous resident there since 1914 (Panning and Peters 1933; Fladung 2000). The Elbe is a 1164 km long river that springs in Czech Republic and flows through Germany before mouthing in the North Sea at the Dutch-German border. Taken together, this makes this large river system a core habitat for the invasive Chinese mitten crab. The port of Hamburg on the Elbe is one of the largest harbours worldwide and may therefore act as a dispersal hub. Long-term data for the Elbe River was collated to investigate three factors that may influence abundance and geographic expansion of the Chinese mitten crab: average annual oxygen concentration, an indicator of overall riverine water quality, from a station near Magdeburg (European Environment Agency 2012), average annual sea surface temperature (SST) from a near-shore North Sea station close to the Elbe Estuary (van Aken 2008; BNSC Uni Hamburg https://icdc.cen.uni-hamburg.de/, accessed Sept 17, 2020), average annual Elbe River water discharge at a station near Darchau (Klein et al. 2018; Fladung 2000). The abundance of the Chinese mitten crab in the Elbe River was categorised as high or low for each year from 1912 to 2021. Logistic regressions between each potential driver and the abundance were carried out. The potential drivers were not combined into a model as they were strongly correlated (Pearsons correlation coefficient > 0.7), and several tightly correlated variables within the same model can lead to erratic model outcomes, also known as collinearity.

Data were extracted from 28 reports and scientific articles, and six online databases. Detailed, referenced accounts of the introduction history and current distribution for each region are available in the Suppl. material 2, and a tabular view is available in Suppl. material 3. In summary, introductions to new regions occurred from 1912 to 1914 (Weser and Elbe Rivers in Germany), 1927 to 1935 (remaining North Sea region including the Scheldt River and several observations in Belgium and The Netherlands, and the Baltic Sea region), 1945 to 1959 (Seine, Loire and Gironde Rivers in France), 1970 to 1976 (Laurentian Great Lakes, Caspian Sea, Norway), and from the late 1980s onwards (Guadalquivir River in Spain, Tagus river in Portugal, Northern Dvina River in Russia, Danube River in Serbia, Romania and Ukraine, Hudson River in the USA, San Francisco Bay in the USA, and several observations in Scotland, Ireland, and Italy) (Suppl. materials 2, 3). The English Rivers Thames and Humber did not become colonised until the 1970s, despite two single specimens caught in 1935 and 1949 (Suppl. material 3). Curiously, few of the introductions of the late 1950s to 1970s became established in the long-term (only the Thames River and possibly the Seine and Loire Rivers) (Fig. 1). Until the end of 2021, the Chinese mitten crab has been observed in Europe in the North Sea area including the British Isles, Baltic Sea, East and West Atlantic, Mediterranean, Caspian Sea, Black Sea, and White Sea (Fig. 2). In North America, the crab occurred on both the west and the east coast, as well as in the Laurentian Great Lakes (Fig. 2B). Single records for the Chinese mitten crab also exist from Japan (Suppl. material 2).

Data were extracted from 14 reports and scientific articles and three online databases. In addition, three researchers and one fisherman were interviewed. Detailed, referenced accounts of abundance fluctuations for each region are available in Suppl. material 2, and a tabular view is available in Suppl. material 4. Overall, newly established populations followed different patterns of abundance fluctuations: the Chinese mitten crab in the Elbe had an initial boom with high abundance shortly after its establishment, followed by a phase of lower but persistent abundance (Suppl. material 2). At its peak abundance in the 1930s, over 100,000 crabs were trapped per day (Panning 1939). This pattern is the classical expectation for an invasive species (Boudouresque 1999; Gothland et al. 2014; Geburzi and McCarthy 2018). In the Scheldt, the Gironde, San Francisco Bay and the Hudson, initially abundant populations disappeared completely or were subsequently only found in coastal areas, recapitulating a boom-and-bust cycle (Fig. 1, Suppl. materials 2, 4). The rivers Scheldt and Gironde were re-colonised in 1990 and 2000, respectively. The Scheldt population is currently at a very high density, but the Gironde has remained at low density ever since (Suppl. material 2). Other populations (rivers Seine, Guadalquivir, Humber, Dvina, Danube, Thames) have been at low abundance throughout much of their invasion history (Suppl. material 2).

At a global scale, increases in abundance of established populations occurred between 1924 and 1930 (rivers Elbe and Scheldt), and have been especially common since the 1990s (Baltic Sea countries, rivers Elbe, Thames and Scheldt) (Figs 1, 3B, Suppl. material 2). New regional records that resulted in established populations were most common between 1927 and 1935 and from the 1970s on. The annual number of reported geographic expansions explained the annual number of reported increases in abundance (p-value = 0.034, z-value = 2.119, df = 109), but not vice versa (p-value = 0.105, z-value = 1.622, df = 109).

At a regional level, within a river system or geographically close rivers, the temporal sequence of geographic expansion and abundance increases could be reconstructed in detail for two cases. The first appearance of the Chinese mitten crab in Europe in 1912 was an expansion from the native range. This initial expansion was likely facilitated by increased shipping activity, and especially increased trade with China between 1840 and 1950 (Fravel 2005). Following this initial introduction, the Chinese mitten crab increased in abundance in its non-native range in the Elbe and Weser Rivers (from 1924 on), followed by regional expansion in the 1930s (Peters and Panning 1933; Panning 1939; Panning 1952). This means that an increase in abundance was followed by geographic expansion. The more recent expansion throughout the United Kingdom also follows the same sequence: after the Chinese mitten crab became abundant in the Thames River starting in 1992 (Clark et al. 1998; Herborg et al. 2005), it spread further across Britain, reaching Scotland and neighboring Ireland in the 2000s (see Suppl. material 2 for detailed account). Therefore, our data show that the temporal sequence at the regional scale is: 1. introduction, 2. abundance increase, 3. geographic expansion.

Oxygen concentration in the Elbe River was low in the 1950s and 1960s, and increased at the end of the 1980s (Fig. 4A), whereas SST peaked in the 1930s, and increased again since the end of the 1980s (Fig. 4B). River water discharge fluctuated throughout the last century, but no clear trends are recognisable (Fig. 4C). Crab abundance was generally low between 1955 to 1990, with a few short increases in abundance. This matched the oxygen content of the Elbe River and SST reasonably well. The binomial GLM models found significant positive relationships for both oxygen content (p-value = 0.0122, z-value = 2.506, df = 69) and SST (p-value = 0.000768, z-value = 3.364, df = 84), but not for riverine water discharge (p-value = 0.861, z-value = 0.176, df = 84) (Fig. 4D, F). In other words, crab abundance increased with increasing oxygen content and rising SST.

The relationship between abundance increase and geographic expansion could be assessed at the regional and the global scale. At the regional scale within a river system or several proximate rivers, the temporal sequence of events appears to be: 1. introduction, 2. abundance increase, 3. geographic expansion. A probable cause of this sequence is that at times of high abundance, many individuals are available to disperse, resulting in high propagule pressure. Within a river system or between neighboring river systems, they can disperse naturally through larval dispersal and juvenile migration. Juveniles appear to migrate further upstream when densities are high, likely to avoid competition for resources (Fladung 2000). In these expansions, man-made channels play a significant role: crabs reached the Baltic Sea via the Kiel Canal (Panning and Peters 1933), the Maas river probably via the Albert canal (La Nation Belge 1-2-1939), the Saimaa Lake District via a channel that connects it to the eastern Gulf of Finland (Ojaveer et al. 2007), and lagoons along the Mediterranean coast via artificial channels (Petit and Mizoule 1973).

At a global scale, two concerted peaks of abundance increase and geographic expansion exist, one in the 1930s, and a second peak from the 1990s on. The statistical analysis indicated that geographic expansion drives the increase in abundance but not vice versa. Therefore, in the temporal sequence at the global scale abundance increase is preceded by geographic expansion. This is the opposite pattern to the sequence of events at the regional scale that was reconstructed descriptively, not statistically. The difference in scale between regional and global relationships itself may explain the differences in causality between increases in abundance and geographic spread. In local (nearby) systems, crabs may disperse more when abundance is high (thus abundance increase is followed by geographic expansion). At a global scale, however, natural dispersal capacity is limited in comparison to e.g. dispersal via shipping. Increases in abundance within regions then, may not lead to global scale expansion. On the other hand, global expansion via e.g. shipping lends itself to creating a new population whereby abundance will only increase if the introduction is successful.

Another possibility is that the second peak in abundance increase and geographic expansion were caused by a cryptic invasion of crabs with different ecological preferences. These crabs were able to establish populations in regions that could not be colonised by the non-native Chinese mitten crabs. In this case, the subsequent increase in abundance of already established populations would have been caused by an introduction wave of these “new” crabs. This hypothesis may be the case for the Belgian and Dutch population, where crabs are morphologically identical to Chinese mitten crab, but about two thirds carry Japanese mitten crab mitochondrial DNA (Hayer et al. 2019; Homberger et al. 2022). This indicates a cryptic invasion of the Japanese mitten crab with subsequent introgression, which could have altered their ecological tolerance (Homberger et al. 2022). But neither the German nor Portuguese population, which expanded and were newly founded at the end of the 1980s, respectively, show signs of a cryptic invasion of Japanese mitten crabs (Herborg et al. 2007; Hayer et al. 2019; Homberger et al. 2022). Unfortunately, no data on the detailed colonisation pathways of the Chinese mitten crab are available to test this hypothesis. Alternatively, but not exclusive to the cryptic invasion hypothesis, environmental conditions for the Chinese mitten crab improved at a global scale.

For four decades between 1940 and 1980, no increases in abundance were recorded, but a few geographic expansion attempts were noticed. None of them were successful, which may indicate that ecological conditions were not favourable for the establishment of Chinese mitten crabs. Such ecological mismatch is apparent for crabs found in the Laurentian Great Lakes and the Caspian Sea, where salinity is assumed too low for reproduction (Ricciardi 2006). Invasion attempts in Norway, Denmark and Japan may have been unsuccessful due to low temperatures (Anger 1990; Zhang et al. 2019, 2020).

In the late 1980s, the establishment of populations in Portugal and Spain marked the beginning increase of successful invasion attempts and increasing abundance across the non-native range of the Chinese mitten crab. Our case study in the Elbe River indicates that environmental change, i.e. an improvement of riverine water quality and rising sea surface temperatures, contributed to the increase of abundance of mitten crabs in this river. River quality improved in many parts of the world in the 1990s (Cane et al. 1997; European Environment Agency 2012; Stets et al. 2012; Lopez et al. 2020) Increasing SST is also a global phenomenon (Bulgin et al. 2022), whereby climate change may play a significant role in the current increase of abundance and geographic expansion of this highly invasive species. In support of this hypothesis, ecological niche models for the Chinese mitten crab indicate that water temperature is the most important predictor of its present-day distribution (Herborg et al. 2007; Zhang et al. 2019, 2020). Thus this case study could hint at reasons for the global causes in the Chinese mitten crab invasion process: global-scale changes in the environmental conditions.

Increases in Chinese mitten crab abundance could also have been facilitated by other ecological factors, such as predator relief, lack of specific pathogens and parasites, decline of interspecific competition or the removal of migration obstacles, especially dams which have been hypothesized to limit the spread of the Chinese mitten crab in the Weser in the 1930s (Panning and Peters 1933). Macro-predators of juvenile and adult crabs include birds, fish, amphibians, and mammals including humans (Veldhuizen and Stanish 1999; Rudnick et al. 2003; Weber 2008; Bouma and Soes 2010), while larvae are likely eaten by any planktivore in the sea. Anthropogenic activities, for example overfishing of wild fish stocks, could also cause changes in predator pressure. Competitors of the Chinese mitten crab in freshwater are crayfish, which also burrow riverbanks, and have a similar food spectrum (Rosewarne et al. 2016), while in estuaries its competitors are other species of crabs, e.g., the green shore crab Carcinus maenas (Gilbey et al. 2008). Despite the fact that Chinese mitten crabs are threatened in their native range by many different viral and parasitic diseases (Cohen 2003; Li et al. 2011; Ding et al. 2017), invasive crabs carry few of them. The only known parasites of European populations are the microsporidian Hepatospora eriocheir (Stentiford et al. 2011) and the crayfish plague Aphanomyces astaci (Schrimpf et al. 2014).

Fishing and removal of crabs may play a particular role in preventing large-scale outbreaks of the Chinese mitten crab. In the 1930s, crabs were systematically caught and removed from German rivers draining into the North Sea (Panning 1952; Fladung 2000). Following these efforts, mass occurrences ceased. At a regional scale, fishing may therefore be a way to limit the negative impacts of the Chinese mitten crab that are mostly driven by mass occurrences.

The fact that introduction attempts have been reported throughout the introduction history of the Chinese mitten crab shows that propagule pressure must have been relatively high at all times. The implementation of vessel discharge regulations in North America in 2008 (U.S. Environmental Protection Agency 2013) and the Ballast Water Management Convention entry into force (IMO 2022) aim to reduce the propagule pressure of e.g. larval mitten crabs in ballast tanks. It will be very interesting to investigate future pattern of geographic expansion and if the spread of the Chinese mitten crab can be slowed down by these actions.

We would like to point out that especially in more recent times with increased globalisation, other routes of anthropogenic dispersal may become more important. Besides crabs moving coincidentally in ballast water or on the hulls of ships, active release of crabs may become a prevalent mode of anthropogenic dispersal, but only anecdotal data exist (Cohen and Carlton 1997; per. obs. H.K.). Due to its value as a delicacy for the Asian community, the Chinese mitten crab has been transported repeatedly alive across borders, both legally and illegally (Cohen and Carlton 1997; Ebersole 2020; Sessa et al. 2020). The USA seized more than 14,000 live crabs that were illegally shipped to the USA in 2019 (Fig. 5A). Subsequent release of imported live crabs may well have been the cause of the San Francisco Bay invasion, and the recent appearance of the Chinese mitten crab in Italy (Cohen and Carlton 1997; Crocetta et al. 2020).

The effect of fishing on crab dispersal has not been assessed thoroughly. Intentional fisheries for the Chinese mitten crab have become more common in the last decades, and are present at least in Germany, Portugal, and the Netherlands (van Overzee et al. 2011; Tsiamis et al. 2017; pers. comm. Filip Ribeiro and Paula Chainho [University of Lisbon] and pers. obs. by H.K. and C.E.) (Fig. 5B), but other countries are also considering it as a management tool (Clark 2011). This increased availability of crabs at markets may further increase the rate of active release into non-native habitats, a scenario proposed for the recent Italian introduction event (Crocetta et al. 2020). Taken together, this means that fishing could increase the anthropogenic dispersal of the Chinese mitten crab while reducing its local abundance.

Our study shows that increases in abundance correlate positively with geographic range expansions of the Chinese mitten crab across its non-native range. This means the double-trouble hypothesis (sensu Gaston 1990) holds in this globally invasive species. If this hypothesis holds for non-native species in general, some species may emerge as “super invaders” that expand across the globe at high densities, while others occur in low abundance at few non-native sites. At a regional scale, monitoring of the Chinese mitten crab should pay attention to increases in abundance, as they precede geographic expansion via natural dispersal. Unfortunately, despite being one of the most invasive aquatic species in the world, the Chinese mitten crab is still not included in continuous and comprehensive monitoring in many of the countries to which it has been introduced. On the other hand, long-term data on geographic expansion patterns and dynamics as well as current distribution of the species are the elements necessary to carry out a risk assessment which in turn is prerequisite to any control and management actions. By incorporating global data from scientific sources and citizens science together with information obtained from local stakeholders, our study provides a wider picture of the spatiotemporal fluctuations in the geographic expansion and abundance of the Chinese mitten crab and for this reason could be of high importance to various levels (national, international or regional) of decision-makers.