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Limnomysis benedeni

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Limnomysis benedeni

Summary

  • Last modified
  • 25 September 2018
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Limnomysis benedeni
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Arthropoda
  •       Subphylum: Crustacea
  •         Class: Malacostraca
  • Summary of Invasiveness
  • L. benedeni is a mysid shrimp native to the brackish and freshwaters of the Ponto-Caspian region. Shortly before 1946, it spread across continental Europe by both intentional (for fish feeding) and unintentional...

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Identity

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Preferred Scientific Name

  • Limnomysis benedeni Czerniavsky, 1882

Other Scientific Names

  • Limnomysis behningi Zhadin and Gerd, 1961
  • Limnomysis brandti Czerniavsky, 1882
  • Limnomysis schmankewiczi Czerniavsky, 1882
  • Mysidella bulgarica Valkanov, 1936
  • Onychomysis mingrelica Czerniavsky, 1882

Local Common Names

  • Austria: Donau-Schwebgarnele
  • Germany: Donau-Schwebgarnele
  • Hungary: pontusi tanúrák
  • Netherlands: kaspische slanke aasgarnaal; slanke aasgarnaal
  • Slovakia: vidlonožec dunajský

Summary of Invasiveness

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L. benedeni is a mysid shrimp native to the brackish and freshwaters of the Ponto-Caspian region. Shortly before 1946, it spread across continental Europe by both intentional (for fish feeding) and unintentional introductions, and arrived in the coastal brackish waters of the Baltic and the North Sea. It is soon to be expected on the Mediterranean coast. The westward spread occurred mainly through multiple invasion waves along waterways of the southern corridor, from the Danube Delta, through the Main-Danube Channel, and in the River Rhine down to the North Sea. Main vectors of expansion are ships (in cooling water filters or bilge or ballast water), with construction of navigation canals as the main associated factor. Overland transfers are evident but probably of minor importance. Estimates of invasiveness are mainly based on local, often transient, mass occurrences in colonized waters, where this species has become, for limited periods, by number or biomass, the most dominant macrozoobenthic component, with potential consequences on habitat structure, food webs, and biodiversity.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Arthropoda
  •             Subphylum: Crustacea
  •                 Class: Malacostraca
  •                     Subclass: Eumalacostraca
  •                         Order: Mysidacea
  •                             Family: Mysidae
  •                                 Genus: Limnomysis
  •                                     Species: Limnomysis benedeni

Notes on Taxonomy and Nomenclature

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Scientific names in use

Limnomysis benedeni Czerniavsky, 1882 is the only currently acknowledged species of the genus Limnomysis Czerniavsky, 1882. Together with the first description of this genus and species, Czerniavsky (1882) produced a great number of additional names at the generic, specific, subspecific, and infrasubspecific level, all of which are currently considered as junior synonyms. In addition, Mysidella bulgarica described by Valkanov (1936) from freshwater populations in Bulgaria was also synonymized by Bacescu (1940) based on examination of the type material. Since then, the genus Limnomysis has remained monotypic in the primary scientific literature.
 
Common names
 
The English terms 'mysid', 'mysid shrimp', or 'opossum shrimp' designate any species belonging to the family Mysidae.
 
Specific common names are used for L. benedeni in several countries along rivers Rhine and Danube:
 
The Dutch name ‘(Kaspische) slanke aasgarnaal’ means ‘(Caspian) slender mysid’.
The German name ‘Donau-Schwebgarnele’ means ‘Danube mysid’.
The Hungarian name ‘pontusi tanúrák’ means ‘Pontian mysid’.
The Slovakian (Czech) name 'vidlonožec dunajský' means 'Danubian mysid', or more literally 'Danubian schizopod'.
 
In each case the English term 'mysid' may be replaced by 'mysid shrimp' or by 'opossum shrimp'.

Description

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A detailed description of L. benedeni is available in Bacescu (1954). These mysids are distinguished from other species of the family Mysidae by the following set of morphological characters: eyes normal, the cylindrical eyestalks are 1.4-2.3 times the length of the cornea. Antennal scale setose all around, with distinct, sexually dimorph apical segment, tip rounded with indistinct or weak ventral flexure in females, whereas more acute and with stronger flexure in males. Anterior margin of the carapace extends into a pair of lateral spine-like processes. Pleopods reduced to small setose plates in both sexes, except third and fourth pleopods in males. Third male pleopod fused to a two-segmented plate; fourth male pleopod with small, distinct endopod, exopod much longer but basally fused with the two-segmented sympod, exopod terminally of unique shape (occasionally with bifid tip). Telson short, stout and subtriangular with 14 spines along lateral margins; the short, rounded apical incision armed with 4-10 laminar processes (some additional information from Kelleher et al., 1999). The coloration is dark brown to translucent (R. Stubbington, Nottingham Trent University, Nottingham, UK, personal communication, 2011).

Body size of adults, measured as total length from the tip of the rostrum to the end of the telson, is typically in the range of 6-13 mm, in rare cases 5-15 mm. Maximum sizes are typically observed when the over-wintering generation matures in spring to early summer, and minimum sizes in late summer to early autumn. Males were on average larger than females in waters of Moldavia (Dediu, 1965) and in the Danube floodplain of Vienna (Wittmann, 2002a) whereas the opposite pattern was found in Lake Constance in Germany (Gergs et al., 2008). The young leave the brood pouch already resembling miniature adults, although lacking secondary sexual characteristics.

Distribution

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Native areas: Up to the 1940s, L. benedeni was confined to coastal waters and tributaries of Lake Caspian and the Azov, Black and Marmora seas (Bacescu, 1940; Wittmann, 2007). From the oligohaline mouth area it penetrated several hundred kilometres into the large Ponto-Caspian river systems. For example, the original distribution in the River Danube reached up to about 460 river-km (Bacescu, 1940; by convention, 0 km is at the city of Sulina on the Black Sea coast). The only possible mention of a native population outside the Ponto-Caspian basin is an unclear comment by Bacescu (1948) made in Romanian and interpreted by Mordukhay-Boltovskoy (1964), Kelleher et al. (1999), and Wittmann and Ariani (2000) as a record for Lake Beysehir in the highlands of Anatolia (southern Turkey, Levantine Basin, eastern Mediterranean). However, inspection of this lake in June 2006 yielded no Limnomysis (KJ Wittman, Medical University of Vienna, Austria, personal communication, 2009).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Sea Areas

Atlantic, NortheastLocalisedIntroduced1960 Invasive Ioffe, 1968; Razinkovas, 1996; Kelleher et al., 1999; Arbaciauskas, 2002; Olenin et al., 2007; Audzijonyte et al., 2009In estuarine coastal waters of the Baltic (first recorded 1963) and the North Sea (first recorded 1998 from Haringvliet - Netherlands). Populations of the Curonian Lagoon (Baltic) originate from intentional introductions into the Kaunas resevoir in 1960 (Ioffe, 1968) and also found downstream
Mediterranean and Black SeaLocalisedNative Not invasive Bacescu, 1954; Komarova, 1989; Daneliya, 2003; Özbek and Ustaoglu, 2006; Wittmann, 2007; Audzijonyte et al., 2009In small rivers, estuaries and lakes on the coasts of the Sea of Azov, Black Sea, and the Marmora Sea

Asia

AzerbaijanLocalisedNative Not invasive Czerniavsky, 1882; Bacescu, 1954In tributaries and coastal waters of Caspian Lake
Georgia (Republic of)LocalisedNative Not invasive Czerniavsky, 1882; Derjavin, 1924; Bacescu, 1954River Rioni and Lake Palaeostom on the Black Sea coast
IranLocalisedNative Not invasive Bacescu, 1954In tributaries (rivers Sefid Rud and Rud Amol) of the Caspian Lake
KazakhstanLocalisedMordukhai-Boltovskoi, 1979a; Behning, 1938; Zhadin and Gerd, 1961; Aladin et al., 2003Native in coastal waters and tributaries of the Caspian Lake. Introduced into the middle reach of the River Ural. Inadvertently introduced into Lake Aral (first recorded 1975)
TurkeyLocalisedNative Not invasive Bacescu, 1954; Wittmann, 1995; Özbek and Ustaoglu, 2006; Wittmann, 2007; Audzijonyte et al., 2009In small rivers, estuaries and lakes on the coast of the Black sea and the Marmara Sea
TurkmenistanLocalisedIntroducedAkmurdov et al., 2006Intentionally introduced into inland waters
UzbekistanLocalisedIntroducedMordukhai-Boltovskoi, 1979a; Aladin et al., 2003Inadvertently introduced into Lake Aral (first recorded 1975)

Europe

AustriaWidespreadIntroduced Invasive Wittmann, 2002b; Weish and Türkay, 1975; Wittmann, 1995; Wittmann et al., 1999; Gergs et al., 2008; Moog et al., 2008River Danube drainage system (first recorded 1973), also in Lakes Constance and Neusiedlersee
BelarusLocalisedIntroducedSemenchenko et al., 2007Pripyat River (first recorded 2007)
BelgiumLocalisedIntroducedVercauteren and Wouters, 2008Ponds in Prinsenpark (Retie; first recorded 2005)
BulgariaWidespreadNative Not invasive Bacescu, 1949; Russev and Kaneva-Abadjieva, 1973; Wittmann, 2007; Audzijonyte et al., 2009In waters of the River Danube drainage system; in coastal lakes and estuaries of the Black Sea
CroatiaLocalisedIntroducedBogut et al., 2007; Wittmann, 2007Rivers Danube and Drava, nature reserve Kopacki rit (first recorded 2004)
FranceLocalisedIntroducedWittmann and Ariani, 2000; Wittmann and Ariani, 2009In waters of the River Rhine drainage system (including River Moselle) and in navigation canals of NE France (first recorded 1998)
GermanyWidespreadIntroduced Invasive Wittmann, 1995; Geissen, 1997; Reinhold and Tittizer, 1998; Wittmann et al., 1999; Tittizer et al., 2000; Wittmann, 2003; Bernauer and Jansen, 2006; Fritz et al., 2006; Gergs et al., 2008; Audzijonyte et al., 2009In waters of the Danube (first recorded 1993) and Rhine systems; also in navigation canals, lakes etc. of northern Germany, also in tributaries of the North Sea
HungaryWidespreadIntroduced1946 Invasive Dudich, 1947; Woynárovich, 1955; Borza, 2007In waters of the River Danube drainage system, including River Tisa; intentionally introduced into Lake Balaton
LithuaniaLocalisedIntroduced1960 Invasive Ioffe, 1968; Razinkovas, 1996; Arbaciauskas, 2002; Olenin et al., 2007; Audzijonyte et al., 2009In hydropower resevoirs along River Kaunas (first recorded 1961), in the Curonian Lagoon (first recorded 1963), in lakes Simnas and Daugai. Populations originate from intentional introductions in the 1960s (Ioffe, 1968) and following this, secondary spread
MoldovaWidespreadNative Not invasive Dediu, 1966a; Dediu, 1966b; Makarov, 1938; Bacescu, 1940; Dediu, 1965; Komarova, 1991; Audzijonyte et al., 2006Native in Black Sea tributaries (rivers Prut and Dniestr; Kuchurgan and Dniestr limans). Intentionally introduced into hydropower resevoirs belonging to the Danube and Dniestr drainage system
NetherlandsWidespreadIntroduced Invasive Kelleher et al., 1999; Vaate et al., 2002; Usseglio-Polatera and Beisel, 2003Lower Rhine and its tributary system, including rivers Ljssel and Meuse; navigation canals
PolandLocalisedIntroduced2003Michels, 2005River Odra and some of its backwaters
RomaniaWidespreadNative Not invasive Bacescu, 1940; Popescu and Prunescu-Arion, 1960; Wittmann, 2007; Audzijonyte et al., 2009In waters of the River Danube drainage system; in coastal lakes and estuaries of the Black Sea; also in navigation canals
Russian FederationPresentPresent based on regional distribution.
-Central RussiaLocalisedIntroduced1947Zhuravel, 1955; Borodich, 1976Intentionally introduced into hydropower reservoirs, rivers (Volga Seym)
-Southern RussiaWidespreadNative Not invasive Mordukhai-Boltovskoi, 1979b; Behning, 1938; Borodich, 1976; Alekseev, 1995; Grigorovich et al., 2002; Audzijonyte et al., 2006; Petryashev and Daneliya, 2006; Audzijonyte et al., 2009Endemic in tributaries and coastal waters of the Black Sea, Sea of Azov, and Caspian Lake. Intentionally introduced into a great number of hydropower reservoirs, rivers and lakes
SerbiaWidespreadIntroduced1977 Invasive BTF, UNEP/UNCHS Balkans Task Force; Wittmann, 2007In waters of the River Danube drainage system, including River Tisa; in navigation canals connecting Tisa and Danube
SlovakiaLocalisedIntroduced1953Brtek, 1953; Šporka, 2003; Wittmann, 2007In waters of the River Danube drainage system
SwitzerlandLocalisedIntroduced2005Wittmann, 2007; Gergs et al., 2008Upper Rhine (harbour Basel), Lake Constance
UkraineWidespreadNative Not invasive Dediu, 1966a; Bacescu, 1940; Zhuravel, 1950; Zhuravel, 1955; Zhuravel, 1960; Komarova, 1991; Daneliya, 2001; Grigorovich et al., 2002; Daneliya, 2003; Cristescu and Hebert, 2005; Alexandrov et al., 2007; Audzijonyte et al., 2009Native in tributaries and coastal waters of the Black Sea and the Sea of Azov. Possibly invasive along artificial waterways. Intentionally introduced into a number of hydropower reservoirs, rivers and lakes

History of Introduction and Spread

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Spread in the Danube system

In 1946, L. benedeni surprisingly appeared in the winter harbour of Budapest (first record for Hungary (Dudich, 1947; Woynárovich, 1955)), this was almost 1200 km beyond the previously known, native distribution range. In 1950, specimens from the newly discovered populations near the Danube were successfully transplanted to seven stations in Lake Balaton in order to enrich the basis of fish food (Woynárovich, 1955). During the following five decades, L. benedeni expanded its upstream distribution in 14 documented stages (Wittmann, 2007) up to the root of the Main-Danube Canal in Kelheim, Germany,  at km 2410 in 1998. These expansions were probably not influenced by intentional transfers and yielded the first records for Slovakia (Brtek, 1953), Austria (Weish and Türkay, 1975), and Germany (Wittmann, 1995). The city of Kelheim marks the end of the navigable reach in the main course of the Danube, and remarkably this species has not spread further upstream (documented up to 2008 (Wittmann and Ariani, 2009); additional sampling stations summarized in Wittmann (2008)). Most Danubian expansions are attributed to unintentional transport by ships, for example in cooling water filters or bilge or ballast water (Wittmann, 1995, 2007; Reinhold and Tittizer, 1997). Genetic diversity (Audzijonyte et al. 2009) suggests at least three westward invasion waves through the middle and upper reaches of the Danube from differentiated sources in the delta area.
 
Spread to and within the Rhine system
 
Probably shortly before 1997, L. benedeni passed through the Main-Danube Canal (officially opened in 1992) where it was first recorded in 1998 by Reinhold and Tittizer (1998). In 1997-1998 it suddenly appeared in vast areas of the Rhine system probably due to downstream expansion (drift) from this channel within the Main Rhine system (first record for the Netherlands in 1997 by Kelleher et al., 1999). By subsequent upstream spread it had already appeared in 1998 in the French reach (Wittmann and Ariani, 2000) and in 2005 in the Swiss reach (Wittmann, 2007) of the River Rhine. Further expansions within and from the Rhine system continued into tributaries and navigation canals in France (Wittmann and Ariani, 2009), Germany (Wittmann, 2007), and the Netherlands (Usseglio-Polatera and Beisel, 2003), yielding the first record for Belgium in 2005 (Vercauteren and Wouters, 2008). A recent surprise in the Rhine system was the appearance of the species in Lake Constance, marking the common borders of Austria, Germany, and Switzerland, in 2006 (Fritz et al., 2006; ANEBO, 2007). Most range expansions to, within, and from the Rhine system are attributed to the break-up of natural hydrographic barriers by construction of waterways in combination with ship traffic and passive drift. However, other modes of transfer may have played a role (Tittizer, 1997; Reinhold and Tittizer, 1997; Kelleher et al., 1999; Tittizer et al., 2000Velde et al., 2000; Wittmann and Ariani, 2000, 2009; Vaate et al., 2002; Dumont, 2006; Wittmann, 2007). Three major corridors are considered possible routes for the unintentional anthropogenic spread of Ponto-Caspian aquatic species to Western Europe (Schleuter et al., 1998Vaate et al., 2002). Before the availability of genetic data it was not clear (Wittmann, 2007) whether the Limnomysis populations in northwest Germany originated from invasions only along the southern corridor via the Danube, the Main-Danube Canal, and the Rhine, or in part also from non-indigenous populations in tributaries of the Baltic. The genetic analyses of Audzijonyte et al. (2009) finally indicated that Western Europe had so far only been invaded along the southern corridor.
 
Spread in Eastern Europe
 
Starting in 1947 with a hydropower reservoir in the Dnieper River (Ukraine), a great number of water bodies in the former Soviet Union were intentionally stocked with L. benedeni in order to enrich the food supply for fish (Zhuravel, 1950; 1959; Ioffe, 1968; Grigorovich et al., 2002; Minchin and Rosenthal, 2002). In 1960, stocks taken from the introduced population in the Dnieper hydropower reservoir, and used to stock the Kaunas Reservoir (Lithuania), spread along the River Neman down to the Curonian Lagoon at the Baltic coast (Olenin and Leppäkoski, 1999; Arbaciauskas, 2002). Genetic data from Audzijonyte et al. (2009) confirmed the origin of the Curonian population as being the Dnieper Reservoir. This clade has so far not been found anywhere in Western Europe. Surprisingly, the Limnomysis taken in 2004 from the Tsymliansk Reservoir (above the native range of this species in the River Don (Azov Sea drainage)) belong genetically to a Caspian clade (Audzijonyte et al., 2006, 2009). Spread from populations in the River Volga via the Volga-Don Canal (finished in 1951-1952) could plausibly explain this case. In 2003, the species was found for the first time in Poland, in the River Odra, by Michels (2005). These stations are almost equidistant from known populations in Lithuania and northwest Germany, so possible source areas of the Polish population cannot be judged unless genetic analysis is undertaken. In 2007, L. benedeni appeared at three stations along the River Pripyat (first records for Belarus by Semenchenko et al., 2007) where it may have spread via the central corridor from introduced populations in hydropower reservoirs of the River Dnieper.
 
Spread to Lake Aral
 
The Asian populations were originally confined to coastal waters and the lower reaches of tributaries of the Black Sea and Lake Caspian. The appearance of the species in Lake Aral (Kazakhstan and Uzbekistan) in 1975 was possibly due to inadvertent stocking (Aladin et al., 2003) of this lake with fish and diverse invertebrates mainly in the late 1950s and the 1960s -- among the mysids, several species of Paramysis were intentionally stocked from River Don (Aladin et al., 2003).

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Austria Slovakia before 1973 Interconnected waterways (pathway cause) Yes Weish and Türkay (1975); Wittmann (1995)
Belarus Ukraine before 2007 Interconnected waterways (pathway cause) Yes Semenchenko et al. (2007)
Belgium Netherlands before 2005 Interconnected waterways (pathway cause) Yes Vercauteren and Wouters (2008)
Croatia Serbia before 2004 Yes Bogut et al. (2007); Wittmann (2007)
France Germany before 1998 Interconnected waterways (pathway cause) Yes Wittmann and Ariani (2000)
Germany Austria before 1993 Interconnected waterways (pathway cause) Yes Wittmann (1995); Wittmann (2007) Range expansion recorded in six steps of 1-173 km length along River Danube (1973-1993)
Hungary before 1946 Yes Dudich (1947); Woynárovich (1955) From Romania or Serbia
Lithuania Ukraine 1960 Intentional release (pathway cause) ,
Stocking (pathway cause)
Yes Arbaciauskas (2002); Audzijonyte et al. (2009); Ioffe (1968); Olenin et al. (2007); Razinkovas (1996)
Netherlands Germany before 1997 Interconnected waterways (pathway cause) Yes Audzijonyte et al. (2009); Kelleher et al. (1999); Vaate et al. (2002); Wittmann and Ariani (2009)
Poland 2003 Interconnected waterways (pathway cause) Yes Michels (2005) Source areas (Germany or Lithuania) discussed in the text section
Serbia Romania before 1977 Yes Wittmann (2007)
Slovakia Hungary 1947-1952 Yes Brtek (1953)
Switzerland Germany before 2005 Interconnected waterways (pathway cause) Yes Wittmann (2007)
Turkmenistan Russian Federation   Intentional release (pathway cause) ,
Stocking (pathway cause)
Akmurdov et al. (2006)
Uzbekistan Russian Federation before 1975 Stocking (pathway cause) Yes Aladin et al. (2003); Mordukhai-Boltovskoi (1979a) Lake Aral

Risk of Introduction

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L. benedeni is not listed as a quarantine pest. Extrapolations from its range extensions in the 1990s and 2000s suggest that it is only a question of time until it will be present in all major river systems of the European subcontinent with appropriate environmental conditions. As in the past, future range extensions will probably occur mainly along navigable waterways. However, increasing importance of overland transfers was recently noted by Wittmann and Ariani (2009). Considering that natural modes of overland transport are highly unlikely (Woynárovich, 1955), such transfers probably result from human activities such as inadvertent stocking with plants or commercially interesting animals, runoff from aquaria (aquarium trade), and quick overland transport of boats (Wittmann and Ariani, 2009).

Expansion of Limnomysis along waterways from northeast France down to the Mediterranean coast is to be expected within a few years (Wittmann, 2007), with unknown consequences for the indigenous populations of the closely related genus Diamysis represented by a number of species and subspecies in freshwater and brackish to metahaline waters all around the Mediterranean (Ariani and Wittmann, 2000; Wittmann and Ariani, 2000, 2009).
 
Ricciardi and Rasmussen (1998) listed L. benedeni among 17 Ponto-Caspian animals that due to their salinity tolerance are likely to be transported overseas in ship ballast water (legislation designed to prevent this tends to be ineffective -- R. Stubbington, Nottingham Trent University, Nottingham, UK, personal communication, 2011), and could appear as future invaders of the Laurentian Great Lakes and other inland waters of North America. One of the five mysid species listed by these authors, Hemimysis anomala, fulfilled this prediction in 2006 (Pothoven et al., 2007). So far, there is no clear evidence that L. benedeni has crossed any sea basins outside its native range.
 
For invasion success a single female with fertilized eggs or with larvae in the brood pouch may suffice for founding a new population.

Habitat

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In most water bodies, Limnomysis is found in shallow (0.5-5 m) near-shore locations (Kelleher et al. (1999) note great densities at depths of 0-0.5m), unless disturbed by strong currents or wave motion (Kelleher er al. (1999) note a preference for still water, and Wittmann (1995) notes a maximum velocity tolerance of 0.5 m/s). Under conditions of bright light, it shows a generally phytophilic habit, preferring stands or spots of dense submerged vegetation, such as macrophytes, stonewort, roots of trees, and flooded terrestrial weeds (Bacescu, 1954; Dediu, 1966a; Weish and Türkay, 1975; Wittmann, 1995; Wittmann et al., 1999; Gergs et al., 2008). It shows, however, a great plasticity by selecting many other types of structured habitats, if dense vegetation is not closely available. Such structures may include spaces between stones or boulders, stones overgrown by mussels, empty shells, branches of submerged trees, coarse debris, etc. Such structures may be rare in harbours; nonetheless high densities of mysids may be found there in the shadow of pontoons, or in and on the coat of filamentous algae covering concrete walls (Wittmann, 2007). A few specimens are regularly found even on the bare surfaces of soft sediments or concrete walls.

In shallow habitats, the animals are usually solitary or found in small groups of weak cohesiveness. They tend to stay a few cm above the substrate or to rest directly on it. In the turbid waters of coastal lakes or in the dim deep waters of clear continental lakes (Limnomysis was found up to 33 m depth by Steinmann (2009)) they may form aggregations of hundreds or thousands of individuals. Aggregation densities have been observed over a wide distribution range in summer as well as in winter (KJ Wittman, Medical University of Vienna, Austria, personal communication, 2009).
 
At night, L. benedeni shows a more scattered distribution, part of the population is found at the surface of the water column, and part lower down (i.e. there is some diel verticel migration). In coincidence with this, catches of drift nets exposed in rivers overnight are larger than in those exposed during the day (Wittmann et al., 1999). However, the relative yield of daytime drift nets is larger in L. benedeni compared to the other two mysid species, Hemimysis anomala and Katamysis warpachowskyi, currently abundant in the upper reaches of the River Danube. This suggests an overall stronger daytime swimming activity in L. benedeni compared to the two other species.

Habitat List

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CategoryHabitatPresenceStatus
Brackish
Estuaries Principal habitat Natural
Lagoons Principal habitat Harmful (pest or invasive)
Lagoons Principal habitat Natural
Freshwater
Irrigation channels Secondary/tolerated habitat Productive/non-natural
Lakes Principal habitat Natural
Ponds Principal habitat Natural
Reservoirs Secondary/tolerated habitat Productive/non-natural
Rivers / streams Principal habitat Harmful (pest or invasive)
Rivers / streams Principal habitat Natural

Biology and Ecology

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Genetics

Based on sequencing a fragment of the mitochondrial COI gene, Audzijonyte et al. (2006) found a clear genealogical split between populations of the Caspian Basin versus the Black Sea/Azov Basin. As an exception, haplotypes from the Tsymliansk Reservoir (River Don, Azov Drainage) were of the Caspian type. Spread from populations in the River Volga (Caspian Drainage) via the Volga-Don Canal (finished 1951-1952) could be a plausible explanation of this finding. Additional sequencing by Audzijonyte et al. (2009) indicated a strong genetic differentiation among populations in tributaries of the Black Sea. A high diversity and differentiation of haplotypes in the Lower Danube and its delta was reflected by an unexpectedly high differentiation between invaded localities, suggesting that at least three invasion waves from differentiated sources have occurred along the southern corridor from the Danube Delta to the North Sea. Most invaded sites showed only one or two lineages, often different from other invaded sites, suggesting that there is only limited genetic contact between the populations of invaded localities (Audzijonyte et al., 2009).
 
Reproduction
 
As in all Mysidae species so far examined, L. benedeni shows a strictly amphigonic propagation. The eggs are fertilized upon or shortly after deposition in the brood pouch. The young undergo two larval stages in the brood pouch and moult to the fully mobile juvenile stage upon liberation. For invasion success a single female with fertilized eggs or with larvae in the brood pouch may suffice for founding a new population. In Romania, breeding females are found from March/April to October/November (Bacescu, 1954); in Moldavia they are found from early summer to winter (Dediu, 1965). Available data suggest a reproductive cycle near to that of ‘warm-season breeders’ (Wittmann, 1984) with an over-wintering generation reproducing in spring/summer, followed by one or two summer generations reproducing in summer to autumn (winter). Breeding females carry typically 12-40 eggs (range 2- 46) in the brood pouch, with egg or larvae numbers increasing with increasing body size of the parent (Kelleher et al., 1999; Wittmann and Ariani, 2000; Gergs et al., 2008). In addition, egg numbers and parental body sizes vary with season (Dediu, 1965; Gergs et al., 2008). The females are iteroparous, i.e. they produce several subsequent egg clutches, as can be directly observed through the partly transparent body of living specimens carrying an egg mass in the ovarian tubes simultaneously with larvae in the brood pouch.
 
High fecundity, together with iteroparity and plausibly more than one generation per year, give Limnomysis a very high reproductive potential. Besides ambient factors this potential is apparently an important prerequisite for local mass occurrences as observed by Wittmann (2007) and Wittmann and Ariani (2009).
 
Nutrition
 
Studies on stomach contents (Wittmann and Ariani, 2000) and feeding experiments (Gergs et al., 2008) unanimously showed that L. benedeni is mainly microphagous, feeding mostly on organic matter of small particle size, i.e. phytoplankton, epilithion, detritus, and biofilms on macrophytes (but not the plants themselves). Animal prey plays only a minor role.
 
Physiology and environmental requirements
 
As in many freshwater animals of remote marine origin, salinity is a primary limiting factor for L. benedeni. Most populations live in freshwater; however, mass occurrences were mainly observed in coastal and continental lakes with salinities of 0.5-5 PSU (salinity expressed as dimensionless equivalent of electric conductivity) (Wittmann, 1995, 2007). Only a few populations are known from habitats with salinity of 6-14 PSU (Bacescu, 1954; Komarova, 1991; Ovcarenko et al., 2006). A low tolerance for salinities above 10 PSU was found in the laboratory by Bacescu (1940). Sudden salinity changes in the laboratory were survived up to 19 PSU (Ovcarenko et al., 2006). Mass occurrences were only found at a pH of ≥ 7.7 (Wittmann, 2007). A favourable development in alkaline waters is also suggested by the lower oxygen consumption by juvenile Limnomysis at pH 8.4 compared to pH 5.4 (Szalontai et al., 2003).
 
A lower oxygen limit of 3.75 mg/L for the natural occurrence of Limnomysis in freshwater is comparatively high for freshwater invertebrates; however, it is below the values so far demonstrated for other species of freshwater Mysidae (Bacescu, 1940; Wittmann, 2007). Oxygen consumption of L. benedeni under comparable conditions in the laboratory was higher than in amphipods taken together with this species from Lake Balaton (Hungary) (Szalontai et al., 2003). The establishment of new populations in the 1990s-2000s may have been facilitated by the improved water quality (ionic content, oxygen, etc.) in the Rhine and Danube systems as compared to the 1960s-1980s (Kelleher et al., 2000Velde et al., 2000; Wittmann, 2007).
 
Their limited ability to swim against water current may have been the main reason why the natural occurrence of L. benedeni was limited to the lower reaches of rivers before human intervention. By far the most populations are found in standing waters. Normally the animals avoid currents greater than 0.5 m/s (Wittmann, 1995; Wittmann and Ariani, 2000). Not counting drift samples, this species has occasionally been found at velocities of 1.5 m/s (Wittmann, 2007) -- high velocities may be tolerated through physical contact with the substrate -- but it cannot be excluded that populations found at ‘high’ velocities might be mainly constituted and/or stabilized by the import of individuals drifting from upstream locations, and so the upper limit for the long-term existence of populations without import may possibly be lower than 1.5 m/s.

Climate

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ClimateStatusDescriptionRemark
BS - Steppe climate Tolerated > 430mm and < 860mm annual precipitation
BW - Desert climate Tolerated < 430mm annual precipitation
Cf - Warm temperate climate, wet all year Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Ds - Continental climate with dry summer Preferred Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)

Latitude/Altitude Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
40-56

Water Tolerances

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ParameterMinimum ValueMaximum ValueTypical ValueStatusLife StageNotes
Conductivity (µmhos/cm) 500 6000 Optimum 52-23,000 tolerated
Depth (m b.s.l.) 0.5 5 Optimum 0-33 tolerated
Dissolved oxygen (mg/l) >5.9 Optimum >3.7 tolerated
Hardness (mg/l of Calcium Carbonate) 100 200 Optimum 50-540 tolerated
Salinity (part per thousand) 0.1 3 Optimum 0-14 tolerated
Turbidity (JTU turbidity) 10 70 Optimum 1-300 tolerated, measured in the field as NTU (=nephelometric turbidity units)
Water pH (pH) 7.3 8.6 Optimum 5.5-9.6 tolerated
Water temperature (ºC temperature) 10 25 Optimum 0-31 tolerated

Notes on Natural Enemies

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Like other species of freshwater Mysidae, L. benedeni also plays an important role in the diet of fish (Bacescu, 1940, 1954; Zhuravel, 1956; Zhadin and Gerd, 1961; Mordukhai-Boltovskoi, 1979b; Kelleher et al., 1999), no matter if indigenous or introduced.

Means of Movement and Dispersal

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Natural Dispersal

The areal distribution up to the 1930s (Behning, 1938; Bacescu, 1940) suggests that active swimming and passive drift along waterways were once the only modes of natural spread in L. benedeni, and that swimming ability previously limited upstream spread. Simple experiments by Woynárovich (1955) make natural modes of overland spread, such as transfer by water birds, appear very unlikely.
 
After human-assisted introduction, populations can spread by natural dispersal.
 
Accidental Introduction
 
The time series of records (Wittmann, 1995, 2007; Wittmann and Ariani, 2009) together with genetic data (Audzijonyte et al., 2009) suggest that Western Europe was mainly colonized along the southern invasion corridor from the Danube Delta, via the Main-Danube Canal and River Rhine down to the North Sea. A high frequency of harbours as documented distribution limits (Wittmann, 1995, 2007) points to ships as main vectors of dispersal (this means that the rate of dispersal may be sporadic, but large distances can be crossed rapidly -- R. Stubbington, Nottingham Trent University, Nottingham, UK, personal communication, 2011), with construction and widening of navigation canals as associated factors.
 
Recent findings of L. benedeni in poorly accessible water bodies (Wittmann et al., 1999; Fritz et al., 2006; Iftime and Tatole, 2006; Wittmann and Ariani, 2009) indicate that overland transfers could play a minor but significant role in the spread of this species. The proposed vectors are inadvertent stocking with aquatic plants or commercially interesting animals (Velde et al., 2000; Dumont, 2006; Iftime and Tatole, 2006), the aquarium trade, and overland transport of boats (Wittmann and Ariani, 2009).
 
The appearance of L. benedeni in Lake Aral in 1975 was possibly due to inadvertent stocking with fish and diverse invertebrates in the 1950 and 1960s (Aladin et al., 2003). It is a matter of definition whether intentional stocking with mysids not sorted to species level is regarded as ‘inadvertent’ introduction of L. benedeni, as in the case of 35 million specimens, mainly belonging to diverse species of Paramysis, together with some Limnomysis, which were taken from 1957 to 1966 from the lower reaches of the Rivers Don and Volga, and transferred to hydropower reservoirs along the middle reaches of the Volga (Borodich and Havlena, 1973; Borodich, 1976).
 
Intentional Introduction
 
Starting in 1947 and culminating in the 1950-1960s, a great number of water bodies in the former Soviet Union were intentionally stocked with L. benedeni as part of fisheries management (Pauli, 1957; Zhuravel, 1959; Ioffe, 1968; Grigorovich et al., 2002). The most important stockings for the final distribution of Limnomysis were from 1947 to 1949 in reservoirs along the River Dnieper (Ukraine) (Zhuravel, 1950, 1965; Pligin and Yemel'yanova, 1989), in 1950 in Lake Balaton (Hungary) (Woynárovich, 1955), and in 1960 in the Kaunas Reservoir (Lithuania) (Olenin and Leppäkoski, 1999; Arbaciauskas, 2002). Most of these activities were stopped in the 1980s after it became clear that mysid introductions could have adverse effects at the ecosystem level (Rieman and Falter, 1981; Fürst et al., 1984; Ketelaars et al., 1999).

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Intentional releaseIn continental waters of eastern Europe to enrich food supply for fish, mostly in the 1950s-1960s. Yes Yes Aladin et al., 2003; Grigorovich et al., 2002; Ioffe, 1968
Interconnected waterwaysVia the Main-Danube Canal and the Mittellandkanal in Germany. Yes Yes
Internet salesOffers on aquarist internet sites Yes Yes Wittmann and Ariani, 2009
Pet tradeUse as fodder animals or as ornamental animals Yes Yes Piepiorka and Walter, 2006; Rey et al., 2005; Wittmann and Ariani, 2009
StockingInadvertent stocking with aquatic plants and with commercially interesting animals Yes Yes Aladin et al., 2003; Dumont, 2006; Iftime and Tatole, 2006; Velde et al., 2000; Wittmann and Ariani, 2009

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
LivestockInadvertent stocking with commercially interesting animals. Yes Yes Aladin et al., 2003; Dumont, 2006; Velde et al., 2000; Wittmann and Ariani, 2009
Plants or parts of plantsInadvertent stocking with aquatic plants. Yes
Ship ballast water and sedimentFor inland navigation of minor importance compared to bilge water and cooling water filters. Yes Yes Reinhold and Tittizer, 1997; Reinhold and Tittizer, 1998; Ricciardi and Rasmussen, 1998
Ship bilge waterBilge water and cooling water filters are probably the main factors for transcontinental spread. Yes Yes Reinhold and Tittizer, 1997; Reinhold and Tittizer, 1998; Vaate et al., 2002; Wittmann, 2007
Ship hull foulingMysids attached to the outside hull of ships Yes Yes Behning, 1938; Reinhold and Tittizer, 1997; Reinhold and Tittizer, 1998; Wittmann, 1995

Economic Impact

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Austin and Alderman (1987) listed L. benedeni among the host species of burn spot disease, a bacterial shell disease found in cultured shellfish, particularly lobsters. The frequency and severity of possible impacts on aquaculture are still unknown.

Environmental Impact

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Impact on Habitats

Olenin and Leppäkoski (1999) judged the non-native population of Limnomysis in the strongly eutrophic Curonian Lagoon on the Baltic coast to be a biomass dominant component of the nektobenthic community with major significance in modifying sediment/habitat by pelletisation. For the same population, Olenin et al. (2007) assessed the effect by its invasion on habitats as weak (H1, i.e. alteration of habitat, but no reduction of spatial extent of a habitat). They classified the impact on ecosystem functioning as moderate (E2, i.e. weak modification of ecosystem performance and/or addition of a new, or reduction of existing, functional groups). Wittmann and Ariani (2000) found no marked effects at ecosystem level, following the invasion of L. benedeni into a backwater of River Danube in Vienna (Austria), whereas Gauer and Imesch (2008) did not exclude potential modifications of the food web in freshwaters of Switzerland.
 
Impact on Biodiversity
 
From basic information on the abundance and distribution of Limnomysis, Olenin et al. (2007) assessed the effect of its invasion in the Curonian Lagoon as moderate (C2, i.e. decline in abundance and reduction of the distribution range of native species). According to Wittmann and Ariani (2000), Limnomysis may outcompete species of the closely-related genus Diamysis if it succeeds in invading brackish and freshwater tributaries of the Mediterranean. Bernauer and Jansen (2006) noted a loss of native macroinvertebrate species in the upper Rhine River in Germany after the appearance of a number of invasive macroinvertebrates, including L. benedeni. According to Austin and Alderman (1987), Limnomysis shares vulnerability to burn spot disease (a bacterial shell disease) with a number of other higher crustacean taxa. Quantitative data on the importance of L. benedeni as a vector of this disease are still lacking.

Threatened Species

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Threatened SpeciesConservation StatusWhere ThreatenedMechanismReferencesNotes
DiamysisNo details No detailsCompetitionWittmann and Ariani, 2000

Risk and Impact Factors

Top of page Invasiveness
  • Proved invasive outside its native range
  • Has a broad native range
  • Abundant in its native range
  • Highly adaptable to different environments
  • Highly mobile locally
  • Has high reproductive potential
  • Gregarious
  • Has high genetic variability
Impact outcomes
  • Ecosystem change/ habitat alteration
  • Modification of natural benthic communities
  • Reduced native biodiversity
  • Threat to/ loss of native species
Impact mechanisms
  • Competition
  • Pest and disease transmission
  • Herbivory/grazing/browsing
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Highly likely to be transported internationally deliberately
  • Difficult/costly to control

Uses

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Economic Value

L. benedeni is often found in the stomach of freshwater fish in eastern Europe and is, therefore, often emphasized as important factor for the nutrition of fish, particularly foraging fish (e.g. Zhuravel, 1959; Rezsu et al., 2005). Increasing aquarist use (Piepiorka and Walter, 2006) of L. benedeni as fish fodder and as ornamental ‘shrimp’ is accompanied (Wittmann and Ariani, 2009) by increasing numbers of Internet offers for its sale.

Uses List

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Animal feed, fodder, forage

  • Fodder/animal feed
  • Forage
  • Invertebrate food

Similarities to Other Species/Conditions

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L. benedeniis the only species in its genus (R. Stubbington, Nottingham Trent University, Nottingham, UK, personal communication, 2011). Juveniles and adult females may be confused with Diamysis pengoi, which has an exclusively Ponto-Caspian distribution -- its distribution covers almost the entire native range of L. benedeni but is more restricted to freshwater. A detailed description of D. pengoi is available in Bacescu (1954). It is distinguished from L. benedeni by a non-dimorphic, much shorter, terminally rounded, and forward-oriented apical segment of the antennal scale. The cornea is slightly larger and visibly darker in living and freshly fixed specimens. The endopod of the fourth male pleopod is not fused with its sympod; it is rod-like, two-segmented, with a long, terminal, modified seta. The telson is more quadrangular, with a greater number of laminae on its only superficial apical incision. For sorting large quantities of any size class it has proved convenient to check the statoliths in the basis of the endopods of uropods with a low-power stereomicroscope. According to Ariani et al. (1993), the statoliths of D. pengoi are composed of the mineral fluorite (CaF2), which is transparent in transmitted light, and those of L. benedeni consist of vaterite, a metastable CaCO3 mineral, which is less transparent, almost opaque. Training is required for fast and secure sorting by this method. A UK identification guide to invasive freshwater shrimps and isopods includes species present in the UK and others that are invasive across Europe (Dobson, 2012).

Prevention and Control

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No specific prevention measures have so far been proposed for L. benedeni. Non-specific measures may be important such as exchange and treatment of ballast water (Taylor et al., 2002). No means (other than destructive ones on the environment) are known to remove L. benedeni once it has established as alien species in a water body.

References

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10/06/09 Original text by:

Karl Wittmann, Medizinische Universität Wien, Abteilung Ökotoxikologie (ZPH), Waehringer Strasse 10, Abteilung Ökotoxikologie (ZPH), A-1090 Wien, Austria

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