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'Perfect' Invader – the Case of Killer Shrimp, Dikerogammarus Villosus

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'Perfect' Invader – the Case of Killer Shrimp, Dikerogammarus Villosus Aquatic Invasions (2014) Volume 9, Issue 3: 267–288 doi: http://dx.doi.org/10.3391/ai.2014.9.3.04 Open Access © 2014 The Author(s). Journal compilation © 2014 REABIC Proceedings of the 18th International Conference on Aquatic Invasive Species (April 21–25, 2013, Niagara Falls, Canada) Review The profile of a ‘perfect’ invader – the case of killer shrimp, Dikerogammarus villosus Tomasz Rewicz1*, Michal Grabowski1, Calum MacNeil2 and Karolina Bącela-Spychalska1 1Department of Invertebrate Zoology and Hydrobiology, University of Lodz, 12/16 Banacha, 90-237 Lodz, Poland 2Department of Environment, Food and Agriculture, The Isle of Man Government, Thie Slieau Whallian, Foxdale Road, St. Johns IM4 3AS, Isle of Man, The British Isles E-mail: [email protected] (TR), [email protected] (MG), [email protected] (CML), [email protected] (KBS) *Corresponding author Received: 26 May 2014 / Accepted: 7 July 2014 / Published online: 2 August 2014 Handling editor: Vadim Panov Abstract The ‘killer shrimp’, Dikerogammarus villosus, has been recognised as one of the 100 worst alien species in Europe, in terms of negative impacts on the biodiversity and functioning of invaded ecosystems. During the last twenty years, this Ponto-Caspian amphipod crustacean has rapidly spread throughout Europe’s freshwaters and its invasion and continued range expansion represents a major conservation management problem. Although a great deal of research has focused on this almost ‘perfect’ invader as its damaging impacts, realised and potential, have become evident, we now present the first comprehensive review of D. villosus taxonomy, morphology, distribution, community impacts, parasites, life history, physiological tolerance and finally, possible eradication methods. We show the direct and indirect ecosystem impacts of this invader can be profound, as it is a top predator, capable of engaging in a diverse array of other feeding modes. It can quickly dominate resident macroinvertebrate communities in terms of numbers and biomass, with subsequent large-scale reductions in local biodiversity and potentially altering energy cycling, such as leaf litter processing. This damaging European invader has the potential to become a key invader on a global scale as it may be capable of reaching North American freshwaters, such as the Great Lakes. One positive aspect of this invader’s spread and impact is increased interest in alien species research generally, from decision-makers, stakeholders and the general public. This has resulted in greater financial support to study invasion mechanisms, preventative measures to stop invasion spread and ways to minimise damaging impacts. Our review provides a specific example, that studies identifying management strategies that mitigate against a potential invader’s spread should be undertaken at the earliest possible opportunity in order to minimise potentially irreversible ecosystem damage and biodiversity loss. Key words: biological invasions, non-indigenous species, Amphipoda, Ponto-Caspian, risk assessments, aquatic invasive species (AIS) Introduction functioning on various levels (Bollache et al. 2008; MacNeil et al. 2010; Piscart et al. 2010). Within Alien species represent a major threat to two decades, it has succeeded in colonising most conservation management on both a continental of the major European inland waterways replacing and global scale (Leppäkoski et al. 2002; Chandra many resident amphipod ‘shrimp’ species, including and Gerhadt 2008; Richardson and Ricciardi 2013). previously successful invaders (Bij de Vaate et Invasion by alien species is increasingly recognised al. 2002; Bollache et al. 2004; Grabowski et al. as one of the major threats to biodiversity in fresh- 2007c; Bącela et al. 2008). In 2011 the species water ecosystems (Sala et al. 2000; Holdich and was detected outside mainland Europe for the Pöckl 2007; SCBD 2010; Lambertini et al. 2011). first time, namely in Great Britain, in an English The ‘killer shrimp’, Dikerogammarus villosus reservoir called Grafham Water (MacNeil et al. (Sowinsky, 1894), is a euryoecious amphipod 2012). Subsequently, several more populations crustacean of Ponto-Caspian origin, regarded as were detected in quick succession in other parts one of the worst one hundred invasive species in of England and Wales (Environmental Agency Europe (DAISIE 2009). It is a highly voracious, 2012; MacNeil et al. 2012). If D. villosus spread physiologically tolerant and adaptable species, follows the pattern of many other aquatic invaders, threatening freshwater biodiversity and ecosystem its range could expand beyond Europe to 267 T. Rewicz et al. Figure 1. The number of publications dealing with various aspects of Dikerogammarus villosus invasion, published up to 2013 and registered in the SCOPUS database. eventually reach North American freshwaters, such definition and loss of type materials, further as the Great Lakes, as has previously happened taxonomic revisions are required that will probably with the zebra (Dreissena polymorpha (Pallas, reduce this number. However, more recent studies 1771)) and quagga mussels (Dreissena rostriformis have also revealed the presence of cryptic species bugensis (Andrusov, 1897)), as well as another within the genus (Grabowski and Jażdżewska amphipod, Echinogammarus ischnus (Stebbing, unpublished data), adding further to the confusion. 1899) (Ricciardi and MacIsaac 2000). Taking into Fortunately, for this current review, among the account the ever increasing amount of research Dikerogammarus species, Dikerogammarus villosus that the scientific community has focussed on the is the most completely defined in morphological killer shrimp, we conducted the first comprehensive terms. An established and comprehensive literature review of the literature, including searching the allows for its unambiguous identification among Scopus database with the keywords Dikero- other congeneric species alien in Central and gammarus villosus and ‘killer shrimp’, as well as Western Europe, such as Dikerogammarus haemo- sourcing unpublished reports and local Russian baphes (Eichwald, 1841) or Dikerogammarus literature. We thus aim to both summarise and bispinosus Martynov, 1925 (Eggers and Martens critically evaluate all the major published studies 2001; Konopacka and Jażdżewski 2002; Mordukhai- dealing with this species, its invasion history, Boltovskoi et al. 1969; Özbek and Özkan 2011). ecology, interaction with local communities, its Contrary to the singular opinion of Pjatakova and invasion potential and issues of control and Tarasov (1996) that D. villosus should be eradication (Figure 1). synonymised with D. haemobaphes, other studies have shown the clear differentiation of D. villosus Taxonomic remarks and potential reasons for from D. haemobaphes and also from D. bispinosus, the success and range expansion of Ponto- both on morphological and molecular bases Caspian invaders in European watercourses (Carauşu 1943; Carauşu et al. 1955; Müller et al. 2002; Wattier et al. 2006) (Figure 2). According to Bousfield (1977), genera such as Dikerogammarus villosus belongs to the ‘Ponto- Dikerogammarus, Pontogammarus, and Obeso- Caspian faunistic complex’, which includes predo- gammarus, are grouped in the family Ponto- minantly euryoecious animal species, originally gammaridae and all include species which are endemic to the coastal areas of the Caspian Sea, invasive to numerous parts of Europe. The Azov Sea, Black Sea, their brackish lagoons taxonomy of the Dikerogammarus genus remains (limans), and associated lower reaches of rivers a source of both confusion and contention. For which drain to these seas (Mordukhai-Boltovskoi instance, some 12 species are ascribed to this 1964; Stock 1974; Jażdżewski 1980; Barnard and genus in various papers (summarised by Grabowski Barnard 1983). The Ponto-Caspian basin resulted et al. 2011), but as a consequence of weak species from the transformation of the Neogene 268 Dikerogammarus villosus - profile of the invader Distribution in native and colonized range Native range of Dikerogammarus villosus In its native range, i.e. the Ponto-Caspian area, Dikerogammarus villosus inhabits lower courses of big rivers, such as Danube, Dnieper, Dniester, Don and Volga as well as coastal lagoons and limans, however its distribution has not been studied in details, particularly in the Caspian Sea area (eg. Carauşu 1943; Carauşu et al. 1955; Mordukhai-Boltovskoi 1960, 1969; Birstein and Romanova 1968; Mordukhai-Boltovskoi et al. 1969; Pjatakova and Tarasov 1996) (Figure 3). Figure 2. Live specimen of Dikerogammarus villosus (picture Presumably, it is present in most of the major by Michal Grabowski). rivers and limans of the Black, Azov and Caspian sea basins. epicontinental Sea of Parathetys (Dumont 2000). Invasion routes of D. villosus in continental Europe Tectonic movements followed by sequential regressions/transgressions then transformed the Jażdżewski (1980) and Bij de Vaate et al. (2002) sea into a number of brackish and freshwater distinguished three main aquatic migration lakes. Since the beginning of the Pleistocene (ca. corridors: southern, central and northern, which 2.5 Mya), rapid climatic and geological changes provide access routes through Central Europe for resulted in reformation of the Ponto-Caspian basin. Ponto-Caspian fauna. The southern corridor covers This in conjunction with glaciation/deglaciation the Danube and Rhine rivers connected by Main– events, resulted in temporal connections with the Danube
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