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 i...
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.
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.
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'.
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.
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).
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.
In 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
Native 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
In 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
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.
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).
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.
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.
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).
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).
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., 2000; Velde 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.
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.
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.
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).
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.
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.
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.
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).
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
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.
Alekseev VR, 1995. Tom 2. Crustacea. Petersburg, Russia: Russ. Akad. Nauk. In: Key to freshwater invertebrates of Russia and adjacent lands [ed. by Tsalolikhin SJ] St. Petersburg, Russia: Russ. Akad. Nauk., 631 pp.
Dediu II, 1967. Amphipods and mysids of the basins of the rivers Dneister and Prut. (Amfipodi i misidi bassejnov rek Dnestra i Pruta.) In: Sistematika, ekologija, zoogeograficeskij analiz i chozjastvennoe znacenie [ed. by Akademija Nauk Moldavskoj S. S. R., Institut Zoologii (Kischinjow)]. Moskva, Russia: Izd. Nauka, 172 pp.