National checklist for aquatic alien species in Germany

More than 140 aquatic alien species (AAS) have been reported from coastlines of the North Sea and the Baltic Sea and from inland waters within the national borders of Germany. The majority of these species has established self-sustaining populations. The most important vectors of introduction are shipping, species imports for aquaculture purposes and species imports as part of the ornamental trade. Several AAS have reached German waters via shipping canals. Many species show a locally limited distribution, but almost half of all AAS have spread successfully across larger areas. Several introduced species are abundant and approximately 20 % of all AAS in Germany can be considered as invasive. Prime source regions are the north-western Atlantic, the Indo-Pacific, and the Ponto-Caspian region. For all source regions considered, the invasion rate has been increasing since the end of the last century.


Introduction
Invasive alien species may threaten native species, alter habitats, and even affect ecosystem function (e.g. Eno et al. 1997, Nehring and Leuchs 1999, Wolff 2005, and thus represent a significant risk to the receiving environments. Following direct habitat destruction, invasive alien species are considered as the second most important cause of global biodiversity change (CBD 2000).
One of the first summaries of aquatic invaders in German coastal waters was prepared by Gollasch (1996). In 1997 Eno et al. published a summary of coastal aquatic alien species in the United Kingdom. Nehring and Leuchs (1999), Nehring (2000a), andTittizer et al. (2000) published overviews on "neozoans" of the German macroinvertebrate fauna. In 1999, Reise et al. published a summary of invasive species in the North Sea and several regional updates were published thereafter: e.g. Weidema (2000) for Nordic countries, Nehring (2005) and AeT umweltplanung (2006) for Germany, Jensen and Knudsen (2005) for Denmark and Wolff (2005) for The Netherlands. In 2006 Gollasch published an overview on introduced aquatic species known from European coasts. Here we update the earlier summaries of alien species in German inland and coastal waters. Another data set of aquatic invaders, which contains more comprehensive information for each species listed, is prepared by the authors for the currently ongoing EU-Programme Delivering Alien Invasive Species Inventories for Europe (DAISIE, see http://www.daisie.se for details).

Aquatic alien species (AAS) in Germany
A total of 141 non-native taxa were reported from the waters considered in this overview, i.e. the coasts of the North Sea and the Baltic Sea and the inland waters within the national borders of Germany (Annex). The vast majority of these species were introduced by ship traffic and, intentionally, by stocking or for aquaculture. Species which reached the region on their own i.e. via drift with currents, swimming, or other ways of natural range expansion, were excluded from this overview. Most AAS have been reported from inland waters, followed by the coastal waters of the North Sea and the Baltic Sea.
More than two thirds of the known introduced species have established self-sustaining populations (Table 1). Some species were only recorded over a certain time period (e.g. the Hydrozoa Bougainvillia macloviana Lesson, 1830 the Anthozoa Haliplanella luciae (Verrill, 1898) and the Bivalvia Crassostrea virginica (Gmelin, 1791) and have since become extinct (Annex). Intentional fish introductions were predominantly motivated by a perceived improvement to the inland fisheries. About 70 "alien" fish species have been recorded in German waters (Geiter et al. 2002). A two century history of fish stocking and translocation makes it impossible to reconstruct the native range of most alien commercial fish species and their phylogeographic structure might also have been obscured. Consequently, some of these 70 species are considered as cryptogenic (see below). At present, ten fish species have been recognized as aliens and are established in selfsustaining populations with locally restricted distribution.
Major natural hydrographical and topograhical differences exit between the three aquatic ecosystems considered (i.e., inland waters, North Sea and Baltic Sea coasts). These differences are also reflected in a distinct occurrence of alien species.
Some species where only found in single or a few records, i.e. the decapod Callinectes sapidus Rathbun, 1896, the anthozoan Cereus pedunculatus (Pennant, 1777), the hydroid Gonionemus vertens Agassiz, 1862, the horseshoe crab Limulus polyphemus Linnaeus, 1758 and the fish Neogobius kessleri (Günther, 1861) (Annex). The relationship between salinity and species diversity is well known. In contrast to freshwater and pure seawater, brackish waters are characterized by the lowest number of indigenous species ("Artenminimum" sensu Remane 1934) and seem to provide opportunities for alien species invasions. It has recently been shown for German waters that the brackish areas of estuaries have been invaded more frequently by alien macroinvertebrate species than rocky or sandy sea shores or inland waters (Nehring 2006a). The author also stated that a low indigenous species richness in aquatic communities facilitates invasions of 'new' species, but the frequency and intensity (or size) of the inoculation are critical components in determining colonization success. Brackish waters seem to have many open ecological niches and are often exposed to intensive international ship traffic. Thus, these habitats have the highest potential for species introductions. In addition, estuaries are subjected to a two-sided invasion pressure by alien species via the ocean (e.g., due to shipping) and via inland waters (e.g., canal constructions).
Since the 1980s, polychaetes of the genus Marenzelleria have appeared in the North Sea and Baltic Sea. The taxonomic identification of the species, which were introduced with ballast water discharge of ocean going ships, was rather difficult and led to confusions and misidentifications. Sikorski and Bick (2004) showed that at least two Marenzelleria species occur in German waters: Marenzelleria neglecta Sikorski et Bick, 2004 andM. viridis (Verrill, 1873)  Although we have some information about some of the direct impacts of AAS, the longerterm ecological consequences for native plant and animal communities and the scale on which biodiversity is modified by invasive species is still poorly understood. Analyses of the economic effects of AAS are also needed.  The most important vectors for species introductions in the Baltic Sea and the North Sea are shipping and species imports for aquaculture. In inland waters most AAS invasions are attributed to canal constructions facilitating species migrations, to the release of species that have been imported with the ornamental trade, stocking and ship traffic ( Figure 3).
Prime source regions for AAS that have invaded German waters are the Ponto-Caspian area, the north-western Atlantic and the Indo-Pacific for the Baltic Sea, the northern Pacific, the Indo-Pacific, the north-western Atlantic for the North Sea, and north America and the Ponto-Caspian area for inland waters (Figure 4).

Cryptogenic species
The native range of some of the species which have been considered as alien is controversial. These species are referred to as cryptogenic species, i.e., species that are neither native or introduced (Carlton 1996  Another interesting case is a turbellarian sampled from a ship hull in a German port. After careful taxonomic consideration it was found that this species is new to science and it was described as Cryptostylochus hullensis Faubel et Gollasch, 1996 (Polycladida, Acotylea, Plathelminthes). Because this flatworm is only known from this single sample, the native range remains unclear (Faubel and Gollasch 1996). The species was never found again in German waters and is therefore not included in the species list attached.

Species introductions and climate change
We excluded species that reached German waters from their known distribution range by natural means such as range expansion from e.g., the north-east Atlantic or the Mediterranean Sea. It has been hypothesized that temporary or permanent climate change facilitates natural range expansion (Nehring 1998a, Stachowicz et al. 2002. Franke et al. (1999) and Franke and Gutow (2004)  The cord-grass Spartina anglica, a fertile hybrid of the European species S. maritima (Curtis) Fernald, 1916 and the North-American species S. alterniflora Loiseleur-Deslongchamps, 1807, was introduced into the Wadden Sea in the 1920s to promote sediment accumulation. However, the intended stabilization of mudflats was not always achieved. Recently this alien species has spread naturally into the tidal zone, where it displaces the native glass-word Salicornia stricta Dumort, 1868 ( Figure 5). This range extension may have been promoted by higher spring temperatures. S. anglica may further benefit from climate change and may become more abundant in the near future, resulting in unforseeable consequences for coastal protection (Nehring 2003, Nehring andAdsersen 2006).

Warm water effluents as hot spots of species invasions
Alien species, native to warmer climate regimes, may also have colonised the North Sea in localities with unusual high water temperatures, e.g. near cooling water outlets of power plants. One example is the Pacific polychaete Ficopomatus enigmaticus (Fauvel, 1923). This brackish water species was first recorded in the London Docks, United Kingdom in 1922(Eno et al. 1997, in the port of Vlissingen, The Netherlands in 1967 near a power plant (Wolff 2005) and also in the German Port of Emden in close vicinity of a power plant (Kühl 1977a). Today, F. enigmaticus is widespread in coastal areas of all North Sea countries.
Another species which "benefited" from locally heated waters is the freshwater Asiatic clam Corbicula fluminea (O.F. Müller. 1756) which was first found in Europe in 1989 near the  . It has been suggested that the successful dispersal of the Asiatic clam in European waters is correlated with winter water temperature minima of 2 °C (Schöll 2000). In Germany, temperatures of inland waters frequently drop below 2 °C in winter and consequently C. fluminea should have limited opportunities for establishment. However, industrial and residential discharges of warm water into many German rivers have raised winter temperature almost permanently above 2°C, thereby promoting the establishment of C. fluminea in high abundances (Galil et al. 2007).

Species findings attributed to drift
Newly recorded species may also have reached German coastal regions by drift with exceptional water inflow due to rare hydrodynamic situations or storms. In some cases, such as for the Station, His, Norway) pers. comm.), but not yet along the German North Sea coast. This western Atlantic species was possibly transported into the Baltic by easterly directed water currents or introduced by human activities, however, its current alien status is unkown.

Canals as invasion corridors
The natural barriers between river and sea basins that have existed since the end of the Pleistocene have been largely eliminated by canals built during the last centuries. The occurrence of 26 alien species in German waters can be attributed to canal construction. The following examples highlight the importance of shipping canals as invasion corridors.
The opening of the Bug-Prypjat Canal in 1784, which connects the Dnieper-Pripyat system to the rivers Bug and Vistula, was of crucial importance for the early and frequent occurrence of Ponto-Caspian species in northern Europe (e.g., the invasive zebra mussel Dreissena polymorpha). After the opening of the Main-Danube Canal in Germany in 1992, which connects the Rhine River and the Danube River, this southern corridor is today the most important link between the Ponto-Caspian area and western Europe. Recently, several Ponto-Caspian species have been found in increasing abundances in the German rivers Main and Rhine (e.g. the isopod Jaera istri [Schleuter and Schleuter 1995]). In contrast Bernauer and Jansen (2006)  This dynamic geographic expansion of D. villosus in Germany was facilitated by several man-made canals in northern Germany which created connections to all large river systems (Rhine, Weser, Elbe, Odra). Due to the rapidly increasing population density of this invasive amphipod it became a major component of the macrobenthic fauna in German freshwater systems, eliminating both native and other alien amphipod species (Tittizer et al. 2000, Haas et al. 2002, Nehring 2005.
More Ponto-Caspian species, mainly invertebrates and fishes, are expected to migrate into the North Sea basin via the Main-Danube-Canal. Especially those species which already occur in the upper and middle Danube will likely arrive in the North Sea basin soon.
The Chinese mitten crab (Eriocheir sinensis), introduced with ships and first recorded in the Aller River in 1912 (Schnakenbeck 1924, Marquard 1926, was reported from the North Sea coast in 1915 (Schnakenbeck 1924), and from the Baltic Sea in 1932 (Boettger 1933a, Peters 1933. E. sinensis was also found in the Kiel Canal in the 1920s (Neubaur 1926) and it is likely that the crab used the canal as the main invasion corridor to migrate from the North Sea into the Baltic Sea (Gollasch et al. 2006). Today the mitten crab can be found in the northern and easternmost parts of the Baltic (Ojaveer et al. accepted). Using the same invasion corridor as E. sinensis, the north-American amphipod Gammarus tigrinus Sexton, 1939 may have reached the Baltic Sea from inland waters in the catchment of the North Sea, where it was intentionally introduced in 1957 (Schmitz 1960) and first recorded in Germany. G. tigrinus successfully spread and reached the North Sea coast by 1965 (Klein 1969) and the Baltic Sea in 1975(Bulnheim 1976, 1980, Wawrzyniak-Wydrowska and Gruszka 2005.
An east-west (i.e., opposite to the more common direction of invasions) directed migration through the Kiel Canal may have occurred in the case of the decapod Rhithropanopeus harrisii (Gould, 1841). This crab was first recorded along the Baltic shores near Kiel and adjacent inland waters (Flemhuder Lake and Kiel Canal) in 1936 (Neubaur 1936), and it was subsequently recorded from the Wadden Sea (Cole 1982, Kühl 1977b, Adema 1991, Nehring 2000b, Van der Velde et al. 2000.

Invasion Myths
The following section focuses on the importance of ships as species invasion vectors. Fact is that shipping continues since centuries and that ballast water is in use for more than 100 years. Some issues, formerly entitled "Invasions Myths" (J.T. Carlton (Williams College, Mystic, USA) pers. comm.), may arise: "All species, which could have been introduced, are here by now!" This is not the case. The "window of introduction" theory explains that all factors need to be right to enable a successful species introduction. These factors include e.g. temperature, salinity, food availability, lack of predators and the number of specimens for a founder population. It is believed that a successful invasion only occurs when all factors involved form the right environment for the candidate invader. However, the factors listed are highly varying and one can easily think of thousands of theoretical combinations indicating how rarely optimum conditions may occur in the receiving environment.
Further, ship improvements result in larger ballast water tanks, more frequent ship arrivals and shorter voyage durations thereby increasing the survival rate of species in transit. It should be noted that the zebra mussel was first recorded in the North American Great Lakes in the 1980s, but ships from its donor region arrived in the lakes since many decades before the species was introduced, i.e. it took quite some time and probably multiple discharge events until all factors triggering the invasion were right.
"Why do we need to go active right now?" The number of invaders was increasing towards the end of the last century. Several investigations have shown that since 1950s the number of new records of invaders have clearly increased (Figure 1). Further new free trade agreements and ship improvements (see above) may have increased the invasion rate even further, thereby indicating the need for immediate action with the aim to reduce the number of new alien species arrivals.

"Biological invasions are a natural phenomenon and happen anyway. The only thing we do is to speed up the process"
This is simply not true as there is no natural means to transport a species from e.g. North America to Australia. Biogeographical textbooks describe the Pacific Ocean as a migration barrier as the duration of the zooplankton larval phase is too short to enable a distribution across the Pacific with natural means. Human mediated vectors, such as ballast water or hull fouling transports, are essential for a species to become dispersed across the Pacific. Also, freshwater species cannot reach new habitats separated by marine waters. However, ballast water releases from e.g. the freshwater port of St. Petersburg (Russia) in the port of Hamburg (Germany) may introduce species which could not reach the area by natural means due to the higher salinity in the western Baltic and North Sea.

"Humans should not interfere with species distributions"
Invasion biologists know that biological components and their interaction in an environment are not a stable process. It was also agreed that initiatives should not be undertaken to hinder natural migration activities of species. However, human mediated species introductions should be kept to a minimum as a precautionary approach. Case histories have shown severe, unwanted impacts of invaders which were introduced unintentionally with e.g. ballast water or associated with aquaculture imports. Natural migrations and human mediated species introductions should clearly be treated separately.

"Only 10% of the invaders show a significant impact"
This statement refers to the "10s-rule". The rule was originally postulated based on invasion histories in terrestrial habitats. The figure was revised frequently. No matter how detailed these revisions were it has to be noted that each invasion has its impact on the recipient region. In some cases the impact is quite clear, in other instances the impact is not as obvious. Further, in many cases an impact is only noted when the invader forms a mass development which may occur long time after the initial introduction. In invasion biology it is not the quantity which matters, but the quality, i.e. just one introduced species may severely impact the receiving environment.
"Phytoplankton species are not matter of discussion as these species are distributed world-wide anyway" It was documented that the number of phytoplankton blooms increased during the last two decades world-wide and it was suggested that this was supported not only by eutrophication but also by biological invasions. The recent occurrence of potentially toxin producing phytoplankton species in the North Sea is a good indication that we should be prepared for additional invaders of this kind.
"Keep the ballast water onboard as long as possible and the species will die over time" Although many species die during the first days in ballast tanks, scientific studies have shown that after more than 4 months living zooplankton can be found in ballast tanks and under certain circumstances zooplankton species even reproduce in ballast tanks (Gollasch et al. 2000a,b, Gollasch et al. 2002. Further, some plankton species are enabled to form resting stages that survive unfavourable conditions for years or decades. Therefore, keeping ballast water onboard for longer periods of time is not a measure to significantly reduce the risk of species invasions.

"The exchange of ballast water in high seas is an appropriate means to reduce the number of invaders"
The exchange of ballast water in mid-ocean can reduce the abundance and diversity of taxa in ballast water. It is further unlikely that coastal organisms taken up in ports survive open ocean conditions where ballast water is exchangedand plankton from high seas is unlikely to survive in coastal areas. In contrast to this assumption scientists showed that the exchange of ballast water could increase the species diversity in ballast tanks, especially in many domestic shipping routes, where no deep water exchange zones occur. Also the number of individuals in ballast tanks may increase when ballast water exchange is undertaken in zones with e.g. phytoplankton blooms. Ballast water exchange is therefore recommended as a very first management option, but effective treatment measures are urgently needed to avoid ballast water mediated species invasions in the future.

The future of alien species introductions into German waters and their potential impacts
The publication of recently introduced species in scientific journals is sometimes a time consuming process, and it is likely that by the time this checklist is published new alien species have already invaded German waters.
These may include the Rapana venosa (Valenciennes, 1846) (Gastropda), which was observed for the first time in the south-western North Sea in 2005(Kerckhof et al. 2006), but outside German national waters. This species was already known from European waters and the new findings in the North Sea likely represent a secondary introduction. However, the occurrence of this species in various locations in Europe may also be a result of multiple introductions from its native range. Noting its potential to spread, it is anticipated that this species may be found in German waters soon.
In 1999 Reise et al. prepared an overview of introduced species in the North Sea and concluded that most alien species can be considered "additive" and that they do not cause major unwanted impacts. However, there is evidence to the contrary. For example, the introduced Pacific oyster Crassostrea gigas is spreading in the Wadden Sea (Reise et al. 2005) with competitive effects on the Mytilus edulis Linnaeus, 1758 mussel beds (Figure 7). The recent spread of C. gigas is likely triggered by (a) recent warm summers which support its recruitment and by (b) the absence of cold winters which promote recruitment of M. edulis. In northern Europe the Pacific oyster may benefit from global warming and may become more abundant than mussel beds have ever been (Diederich et al. 2005, Nehring 2006b). Because the impact of introduced species is potentially enormous, and very unpredictable, we should be aware of new species introductions. One known source of alien species is ship´s ballast water which can contain millions of organisms and that is discharged in our coastal waters every day. Other vectors of introductions include species that are transported in the hull fouling of ships (Gollasch et al. 2000a, b, Nehring 2001, Gollasch 2002, Gollasch et al. 2002 and canal migrations. The latter have increased in magnitude and frequency over the past decade(s) (Harka and Biro 2004, Nehring 2005, Galil et al. 2007).
Similar to a worldwide trend, the rate of invasion of AAS has also increased in German waters since the 1950s, and will probably continue to rise due to the effects of climate change and further improvements in ship design. It is hoped that measures, such as ballast water treatment to reduce the organism load or the installation of migration barriers such as deterrent electrical systems, salt or freshwater water locks, and air bubble curtains to reduce the uncontrolled range expansion of alien species via canals are taken soon to protect our waters from new species invasions and their potentially detrimental effects.