Dikerogammarus villosus - Killer shrimp

Initially, the Killer shrimp could be found in the rivers of the Danube basin, in the so-called Ponto-Caspian region. This is the area surrounding the Black Sea and the Caspian Sea ^[2].

First observation in Belgium

In 1997, the Killer shrimp was recorded for the first time in the Albert Canal and the Dessel-Kwaad-Mechelen Canal ^[3]. However, as this observation took place in freshwater, it is located outside our study area. The first report of this amphipod species in our study area was in 2005 when this exotic species was found in the Ghent-Terneuzen Canal ^[4].

Spreading in Belgium

After the first sighting in the Albert Canal in 1997, the Killer shrimp was found in 1998 in large numbers in the Meuse – from Chokier (south of Liège) to Dinant, close to the Belgian-French border ^[5]. After its introduction, the species dispersed upstream in the Meuse at an estimated speed of 30-40 km per year ^[6]. From 2000 onwards, the Killer shrimp was present in Belgian-Limburg waterways and canals connecting the Meuse basin to the Scheldt basin in western Wallonia ^[7].

From 2005 onwards, the species has been reported in our study area. After the Ghent-Terneuzen Canal [4], the Killer shrimp was seen in the brackish parts of the Yser (near Nieuwpoort) and the harbour of Ostend ^[8-10]. In many cases – such as in the canals of Ostend and Ghent-Terneuzen – this species can dominate both non-native and native amphipods ^[4]. No data is available on its distribution from the past five years.

Spreading in neighbouring countries

The Killer shrimp began its conquest of Europe in the early 1990s. Unlike other Ponto-Caspian species, which used a northern, central and southern route of introduction, Dikerogammarus villosus spread in Europe via two independent invasion routes: a western (Danube, Rhine, Meuse, etc.) and an eastern route (Dnieper, Pripyat, Vistula) ^[11].

Along the western route, the Killer shrimp was first recorded in the German section of the Danube in 1992. The Main-Danube Canal, which was opened in the same year, connected the Danube to the Rhine and opened the gateway to Western Europe. Via the Rhine, this species quickly spread in large numbers to the freshwater and brackish water regions of Western Europe ^[12]. In 1994, this exotic species reached the German rivers Weser, Elbe and Oder ^[13]. In the same period (1994-1995), the Killer shrimp was observed in the Rhine at the German-Dutch border ^[12] and shortly afterwards the Meuse (1996), the Dutch Rhine delta and border lakes (1996-1997) ^{[6, 14]}, and Szczecin Bay on the Oder estuary (on the Polish-German border) ^[13] were colonized.

The first observation in France was in 1997, in the Saône river. In the following years, new observations followed from, among others, the Rhone and Moselle rivers ^{[15, 16]}. From the Rhone, this exotic species found its way to various French alpine lakes and finally to Lake Garda in Italy ^[2]. In 2000, this amphipod had crossed the Belgian-French border via the Meuse ^[6].

The first sighting of the Killer shrimp in Great Britain wasn’t until the 3^rd of September 2010. The species was found in the drinking water reservoir Grafham Water, near the River Great Ouse (eastern England, Cambridgeshire) ^[17]. This was followed by sightings from Cardiff Bay and a reservoir at Port Talbot, South Wales ^[18].

Given its rapid spread in Europe, it is expected to migrate to Ireland in the same way and reach North America via shipping ^{[19, 20]}. There it is assumed to re-enter fresh water, eventually reaching the Great Lakes of North America ^[20].

The Ukrainian river Dnieper was the starting point for the inland spread of this amphipod along the eastern route. This route allowed the expansion of its current distribution to Belarus and the Polish Vistula River ^[21]

The introduction of the Killer shrimp into Western Europe – like other Ponto-Caspian species – was heralded by the opening of the Main-Danube Canal ^[22]. In addition, the construction of canals between the major rivers in Europe facilitated the spread of this species. How this exotic species eventually spread through the European inland waterway network is not entirely clear. Scientists suspect that this species travelled on the hulls of inland navigation vessels or pleasure craft. Transport in ballast water could also have facilitated its further spread to European ports ^{[20, 23]}.

In addition, active upstream migration cannot be excluded, nor can dispersal due to intentional release and movement of fish stocks ^[24].

Its great adaptability to different environmental conditions (salinity and temperature) and substrates means that this species can successfully establish itself in almost all freshwater and brackish water environments. The artificial waterways in Belgium are no exception.

After four to eight weeks, juvenile Killer shrimps can reach a length of 6 mm and by then are sexually mature. A single female can produce up to 50 juveniles every fortnight throughout the year. This fast reproduction rate surpasses that of our native amphipods ^{[15, 25]}. The high growth rate (1.3-2.9 mm per month), early sexual maturity, high fertility and long reproductive season make the Killer shrimp a very successful invasive species that can spread rapidly ^[21].

Although an omnivore, the Killer shrimp is particularly notorious for its voracious appetite for all kinds of invertebrates, such as other amphipods, mayflies, water fleas and snails ^{[16, 26]}. This species also consumes the eggs and larvae of fish and sometimes even feeds on small fish ^{[15, 27]}. This ravenous behaviour manifests itself primarily in areas where it is not yet dominant ^[16]. Although the jaws of the Killer shrimp are not specifically adapted for predation – it also uses them to filter food from the water column and scrape organic material from the bottom ^{[26, 28]} – they do enable this amphipod to tear up prey, whether or not to eat it ^{[15, 25]}.

This species can hide between stones and beds of the zebra mussel, where its dark colour serves as camouflage. Furthermore, this species of amphipod appears to be less active than its native counterpart ^[29]. They can detect predators and food from a distance ^[30]. The combination of these factors gives the Killer shrimp a competitive advantage over other amphipods and, therefore, could become a successful invasive species in Europe.

The Killer shrimp prefers salinities between 0 and 10 PSU but can tolerate salinities slightly over 20 PSU ^[13]. By way of comparison, the salt concentration of the North Sea is 35 PSU. Therefore, this amphipod is only found in the freshwater of lakes, rivers and canals and the slightly brackish water at river mouths.

This non-native species tolerates temperatures between 0 and 30 °C but prefers temperatures around 20 °C ^[13]. It prefers slow-flowing or still waters with good water quality. In such waters, this species can be found on all kinds of hard substrates, from natural stones to artificial pillars ^[26]. Since the 1990s, the quality of our inland waters has improved considerably, and this went hand in hand with the increasingly successful spread of several species, including the Killer shrimp ^[31].

The predatory behaviour of this non-native species – among others present in the Meuse ^[5] – has led to a sharp decline (even disappearance) in the numbers of the native amphipod Gammarus pulex ^{[3, 32]}, and of the previously established non-native Gammarus tigrinus ^[33]. This has an impact on the local biodiversity and ecosystem functioning, and may also affect fauna higher up the food chain through changes in the food sources ^[3]. Because of all this, the amphipod was nicknamed the 'Killer shrimp'. Climate change is believed to be promoting the predation pressure of the Killer shrimp. Thus, its impact on the local ecosystem is likely to increase in the future ^[34].

In its region of origin, the Killer shrimp is viewed in an entirely different way. In the Pontine-Caspian region, it is not the most abundant of the amphipod species present and it doesn’t exhibit the same aggressive predatory behaviour ^{[12, 16]}. Instead, it behaves more like an omnivore. Recent studies have shown that this amphipod does not always have a detrimental effect on the ecosystem and that positive species interactions are as important as negative ones. ^[35]. However, it is suspected that Killer shrimps act as an intermediate host for thorny-headed worms (Acanthocephala). These are wormlike creatures, parasitic to fish and birds ^[12].

To limit the further spread of the Killer shrimp in Great Britain, where it was detected for the first time in September 2010, fishermen and water sport enthusiasts are asked to thoroughly inspect and clean their equipment before and after use. They are requested not to move their bait or water between different areas ^[32]. With this measure, Britain is trying to protect itself from the additional economic damage caused by non-native species.

To prevent the introduction of these and other species to other places via the ballast water of international shipping, the International Convention for the Control and Management of Ships' Ballast Water and Sediments was established in 2017 (see Introduction) ^[36]. An exchange of ballast water further at sea, preferably beyond 200 nautical miles from the shore, can reduce the transfer of harmful organisms to the port of destination. Any freshwater organisms in the ballast water are thus discharged into the saltwater and die. The ballast water is then replenished with salt water at sea. However, as many species tolerate varying salt levels, this measure is not always very effective

Compared to our native species, the Killer shrimp is one of the largest freshwater amphipod species. Males are on average 1 to 2 cm in length, with a maximum of 3 cm, while females are slightly smaller ^[13]. Specimens of this species can have one of four different patterns on their body: a striped, a spotted, a solid coloured pattern, or a pattern with only stripes on the dorsal side. Each of these patterns can appear in a variety of colours ranging from orange-yellow to brown-black ^[37].

In addition, Killer shrimps have large gnathopods – a pair of head appendages with hooks at the end – and strongly developed mouthparts. Very distinctive is the presence of conical protrusions (tubercles) on top of the 'tail' ^[38].

[1]         World Register of Marine Species (WoRMS) (2020). Dikerogammarus villosus (Sowinsky, 1894). [http://www.marinespecies.org/berms/aphia.php?p=taxdetails&id=148586] (2020-11-17).

[2]         Grabowski, M.; Barcela, K.; Wattier, R. (2007). Dikerogammarus villosus (Sowinsky, 1894) (Crustacea, Amphipoda) colonizes next alpine lake – Lac du Bourget, France. Aquat. Invasions 2(3): 268-271. [www.vliz.be/en/imis?module=ref&refid=207880]

[3]         Messiaen, M.; Lock, K.; Gabriels, W.; Vercauteren, T.H.; Wouters, K.; Boets, P.; Goethals, P.L.M. (2010). Alien macrocrustaceans in freshwater ecosystems in the eastern part of Flanders (Belgium). Belg. J. Zool. 140(1): 30-39. [http://www.vliz.be/en/imis?module=ref&refid=206040]

[4]         Boets, P.; Lock, K.; Goethals, P.L.M. (2011). Using long-term monitoring to investigate the changes in species composition in the harbour of Ghent (Belgium). Hydrobiologia 663(1): 155-166. [http://www.vliz.be/en/imis?module=ref&refid=201947]

[5]         Van den Bossche, J.P. (2001). First record of the Pontocaspian invader Hypania invalida (Grube, 1860) (Poychaeta: Ampharetidae) in the river Meuse (Belgium). Belg. J. Zool. 131(2): 183-185. [http://www.vliz.be/en/imis?module=ref&refid=37613]

[6]         Josens, G.; Bij de Vaate, A.; Usseglio-Polatera, P.; Cammaerts, R.; Chérot, F.; Grisez, F.; Verboonen, P.; Vanden Bossche, J.P. (2005). Native and exotic Amphipoda and other Peracarida in the River Meuse: new assemblages emerge from a fast changing fauna. Hydrobiologia 542(1): 203-220. [http://www.vliz.be/en/imis?module=ref&refid=207710]

[7]         Vercauteren, T.H.; De Smedt, S.; Warmoes, T.; Goddeeris, B.; Wouters, K. (2005). Drie nieuwe Ponto-Kaspische inwijkelingen dringen door tot in kanalen in de provincie Antwerpen: De zoetwaterpolychaet Hypania invalida (Grube, 1860) en, voor het eerst in België, de platworm Dendrocoelum romanodanubiale (Codreanu, 1949) en de Donaupissebed Jaera istri Veuille, 1979., in: Nieuwborg, H. Natuurstudie in de provincie Antwerpen. Antwerpse Koepel voor Natuurstudie (ANKONA) Jaarboek 2003: Antwerpen, Belgium: pp. 83-97. [http://www.vliz.be/en/imis?module=ref&refid=206031]

[8]         Vercauteren, T.H.; Sablon, R.; Wouters, K. (2006). Exotische ongewervelden in vijvers en grachten van het Provinciaal Groendomein Prinsenpark in Retie: een eerste bilan, in: Nieuwborg, H. et al. Natuurstudie in de provincie Antwerpen: Antwerpse Koepel voor Natuurstudie (ANKONA) Jaarboek 2004-2005. Antwerpse Koepel voor Natuurstudie (ANOKA): Antwerpen, Belgium: pp. 27-39. [http://www.vliz.be/en/imis?module=ref&refid=206260]

[9]         Hebbelinck, L. (2010). Monitoring van exotische macro-invertebraten in de Vlaamse havens. MSc Thesis. Universiteit Gent, Faculteit Bio-Ingenieurswetenschappen: Gent. 87 pp. [http://www.vliz.be/en/imis?module=ref&refid=197447]

[10]       Boets, P.; Lock, K.; Goethals, P.L.M. (2011). Shifts in the gammarid (Amhipoda) fauna of brackish polder waters in Flanders (Belgium). J. Crust. Biol. 31(2): 270-277. [http://www.vliz.be/en/imis?module=ref&refid=211034]

[11]       Rewicz, T.; Wattier, R.; Grabowski, M.; Rigaud, T.; Bącela-Spychalska, K. (2015). Out of the Black Sea: Phylogeography of the Invasive Killer Shrimp Dikerogammarus villosus across Europe. PloS one 10(2): 267-288. [http://www.vliz.be/nl/catalogus?module=ref&refid=296746]

[12]       Bij de Vaate, A.; Jazdzewski, K.; Ketelaars, H.A.M.; Gollasch, S.; van der Velde, G. (2002). Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Can. J. Fish. Aquat. Sci./J. Can. Sci. Halieut. Aquat. 59(7): 1159-1174. [http://www.vliz.be/en/imis?module=ref&refid=127047]

[13]       Naylor, M. (2006). Alien species in Swedish seas: Killer shrimp (Dikerogammarus villosus). Informationscentralerna för Bottniska viken, Egentliga Östersjön och Västerhavet. Sweden.  pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=207013]

[14]       Noordhuis, R.; Van Schie, J.; Jaarsma, N. (2009). Colonization patterns and impacts of the invasive amphipods Chelicorophium curvispinum and Dikerogammarus villosus in the IJsselmeer area, The Netherlands. Biol. Invasions 11(9): 2067-2084. [http://www.vliz.be/en/imis?module=ref&refid=207071]

[15]       Devin, S.; Beisel, J.N. (2006). Dikerogammarus villosus. Delivering Alien Invasive Species for Europe (DAISIE). 3 pp. [http://www.vliz.be/en/imis?module=ref&refid=207875]

[16]       Casellato, S.; La Piana, G.; Latella, L.; Ruffo, S. (2006). Dikerogammarus villosus (Sowinsky, 1894) (Crustacea, Amphipoda, Gammaridae) for the first time in Italy. Ital. J. Zoolog. 73 (1): 97-104. [www.vliz.be/en/imis?module=ref&refid=207869]

[17]       MacNeil, C.; Platvoet, D.; Dick, J.D.A.; Fielding, N.; Constable, A.J.; Hall, N.; Aldridge, D.; Diamond, M. (2010). The Ponto-Caspian ‘Killer shrimp’, Dikerogammarus villosus (Sowinsky, 1894), invades the British Isles. Aquat. Invasions 5(4): 441-445. [http://www.vliz.be/en/imis?module=ref&refid=207868]

[18]       Constable, D.; Fielding, N. (2011). Dikerogammarus villosus: An Anglian Perspective. In Pract. 72: 9-11. [http://www.vliz.be/nl/catalogus?module=ref&refid=296754]

[19]       Arundell, K.; Dunn, A.; Alexander, J.; Shearman, R.; Archer, N.; Ironside, J.E. (2015). Enemy release and genetic founder effects in invasive Killer shrimp populations of Great Britain. Biol. Invasions 17(5): 1439-1451. [http://www.vliz.be/nl/catalogus?module=ref&refid=296747]

[20]       Ricciardi, A.; Ramsmussen, J.B. (1998). Predicting the identity and impact of future biological invaders: a priority for aquatic resource management. Can. J. Fish. Aquat. Sci./J. Can. Sci. Halieut. Aquat. 55(7): 1759-1765. [http://www.vliz.be/en/imis?module=ref&refid=184855]

[21]       Pöckl, M. (2009). Success of the invasive Ponto-Caspian amphipod Dikerogammarus villosus by life history traits and reproductive capacity. Biol. Invasions 11(9): 2021-2024. [http://www.vliz.be/en/imis?module=ref&refid=207952]

[22]       Wolff, W.J. (2005). Non-indigenous marine and estuarine species in the Netherlands. Zool. Meded. 79(1): 3-116. [http://www.vliz.be/en/imis?module=ref&refid=101200]

[23]       Dick, J.T.A.; Platvoet, D.; Kelly, D.W. (2002). Predatory impact of the freshwater invader Dikerogammarus villosus (Crustacea: Amphipoda). Can. J. Fish. Aquat. Sci./J. Can. Sci. Halieut. Aquat. 59(6): 1078-1084. [http://www.vliz.be/en/imis?module=ref&refid=27715]

[24]       Rewicz, T.; Grabowski, M.; MacNeil, C.; Bącela-Spychalska, K. (2014). The profile of a ‘perfect’ invader – the case of Killer shrimp, Dikerogammarus villosus. Aquat. Invasions 9(3): 267-288. [http://www.vliz.be/nl/catalogus?module=ref&refid=299358]

[25]       Crosier, D.; Molloy, D.P. (2006). Killer Shrimp - Dikerogammarus villosus. New York State Museum: New York. 5 pp. [http://www.vliz.be/en/imis?module=ref&refid=208440]

[26]       Boets, P.; Lock, K.; Messiaen, M.; Goethals, P.L.M. (2010). Combining data-driven methods and lab studies to analyse the ecology of Dikerogammarus villosus. Ecological Informatics 5(2): 133-139. [http://www.vliz.be/en/imis?module=ref&refid=201802]

[27]       Platvoet, D.; van der Velde, G.; Dick, J.T.A.; Li, S. (2009). Flexible omnivory in Dikerogammarus villosus (Sowinsky, 1894) (Amphipoda) - Amphipod Pilot Species Project (AMPIS) Report 5. Crustaceana (82): 6. [http://www.vliz.be/en/imis?module=ref&refid=207885]

[28]       Mayer, G.; Maier, G.; Maas, A.; Waloszek, D. (2008). Mouthparts of the Ponto-Caspian invader Dikerogammarus villosus (Amphipoda: Pontogammaridae). J. Crust. Biol. 28(1): 1-15. [http://www.vliz.be/en/imis?module=ref&refid=208342]

[29]       Kobak, J.; Jermacs, Ł.; Płąchocki, D. (2014). Effectiveness of zebra mussels to act as shelters from fish predators differs between native and invasive amphipod prey. Aquat. Ecol. 48(4): 397-408. [http://www.vliz.be/nl/catalogus?module=ref&refid=296748]

[30]       Jermacz, L.; Dzierzynska-Bialonczyk, A.; Kobak, J. (2017). Predator diet, origin or both? Factors determining responses of omnivorous amphipods to predation cues. Hydrobiologia 785(1): 173-184. [http://www.vliz.be/nl/catalogus?module=ref&refid=296749]

[31]       Boets, P. (2013). Impact assessment of alien macroinvertebrates in Flanders (Belgium). PhD Thesis. Ghent University: Gent. 209 pp. [www.vliz.be/en/imis?module=ref&refid=224013]

[32]       van der Velde, G.; Rajagopal, S.; Kelleher, B.; Muskó, I.; Bij de Vaate, A. (2000). Ecological impact of crustacean invaders: general considerations and examples from the Rhine River, in: von Vaupel Klein, J.C. et al. The Biodiversity Crisis and Crustacea: Proceedings of the Fourth International Crustacean Congress, Amsterdam, Netherlands, 20-24 July 1998, volume 2. Crustacean Issues, 12. A.A. Balkema: Rotterdam, Brookfield: pp. 3-33. [http://www.vliz.be/en/imis?module=ref&refid=207016]

[33]       Dick, J.T.A.; Platvoet, D. (2000). Invading predatory crustacean Dikerogammarus villosus eliminates both native and exotic species. Proc. Royal Soc.m Biol. Sci. 267(1447): 977-983. [http://www.vliz.be/en/imis?module=ref&refid=208441]

[34]       Pellan, L.; Médoc, V.; Renault, D.; Spataro, T.; Piscart, C. (2015). Feeding choice and predation pressure of two invasive gammarids, Gammarus tigrinus and Dikerogammarus villosus, under increasing temperature. hydrobiologia 781(1): 43-54. [http://www.vliz.be/nl/catalogus?module=ref&refid=296753]

[35]       Hellmann, C.; Schöll, F.; Worischka, S.; Becker, J.; Winkelmann, C. (2017). River-specific effects of the invasive amphipod Dikerogammarus villosus (Crustacea: Amphipoda) on benthic communities. Biol. Invasions 19: 381-398. [http://www.vliz.be/nl/catalogus?module=ref&refid=296752]

[36]       Verleye, T.J.; Pirlet, H.; Mees, J. (2018). Marien Beleid - Marien Beleid en Wetgeving 2018. Vlaams Instituut voor de Zee (VLIZ): Oostende. ISBN 978-94-920436-6-5. 126 pp. [http://www.vliz.be/en/imis?module=ref&refid=303560]

[37]       Devin, S.; Bollache, L.; Beisel, J.N.; Moreteau, J.C.; Perrot-Minnot, M.J. (2004). Pigmentation polymorphism in the invasive amphipod Dikerogammarus villosus: some insights into its maintenance. J. Zool. 264(4): 391-397. [http://www.vliz.be/en/imis?module=ref&refid=208396]

[38]       Eggers, T.O.; Martens, A. (2001). Bestimmungsschlüssel der Süßwasser-Amphipoda (Crustacea) Deutschlands = A key to the freshwater Amphipoda (Crustacea) of Germany. Lauterbornia: Internationale Zeitschrift für Faunistik und Floristik des Süßwassers 42: 1-68. [http://www.vliz.be/en/imis?module=ref&refid=312319]

VLIZ Alien Species Consortium (2020). Dikerogammarus villosus – Killer shrimp. Non-native species of the Belgian part of the North Sea and adjacent estuaries anno 2020. Flemish Institute for the Sea (VLIZ). 8 pp.