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Pontogammarus robustoides

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Pontogammarus robustoides

Summary

  • Last modified
  • 08 November 2018
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Pontogammarus robustoides
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Arthropoda
  •       Subphylum: Crustacea
  •         Class: Malacostraca
  • Summary of Invasiveness
  • P. robustoides is a small pale yellow amphipod about 12 mm in length. In the native range it inhabits fresh and oligohaline waters of coastal zones of Caspian, Azov and Black Seas, lower reaches and estuaries o...

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Pictures

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PictureTitleCaptionCopyright
Adult specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006
TitleAdult specimen
CaptionAdult specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006
Copyright©Evgeny A. Kurashov-2006
Adult specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006
Adult specimenAdult specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006©Evgeny A. Kurashov-2006
Adult specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006
TitleAdult specimen
CaptionAdult specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006
Copyright©Evgeny A. Kurashov-2006
Adult specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006
Adult specimenAdult specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006©Evgeny A. Kurashov-2006
Juvenile specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006
TitleJuvenile specimen
CaptionJuvenile specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006
Copyright©Evgeny A. Kurashov-2006
Juvenile specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006
Juvenile specimenJuvenile specimen of Pontogammarus robustoides caught in Lake Ladoga, Russia. 05 August 2006©Evgeny A. Kurashov-2006
Pontogammarus robustoides; chracteristic groups of spines on urosome somites (arrowed)
TitleSpecies identity chracteristics
CaptionPontogammarus robustoides; chracteristic groups of spines on urosome somites (arrowed)
Copyright©Evgeny A. Kurashov-2006
Pontogammarus robustoides; chracteristic groups of spines on urosome somites (arrowed)
Species identity chracteristicsPontogammarus robustoides; chracteristic groups of spines on urosome somites (arrowed)©Evgeny A. Kurashov-2006

Identity

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Preferred Scientific Name

  • Pontogammarus robustoides G.O. Sars, 1894

Summary of Invasiveness

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P. robustoides is a small pale yellow amphipod about 12 mm in length. In the native range it inhabits fresh and oligohaline waters of coastal zones of Caspian, Azov and Black Seas, lower reaches and estuaries of their affluents, coastal lakes and limans in Russia, Ukraine, Caucasus, Romania, Bulgaria and Turkey (Mordukhaj-Boltovskoj et al., 1969; Dedju, 1980; Jazdzewski, 1980; Grabowski, 2011). Constantly expanding its range of distribution, the species is now considered as non-indigenous and invasive in Baltic and middle reaches of Volga river regions. The invasion of the species in the regions is mainly a result of human activity (deliberate introduction, shipment, changing ecological condition due to pollution or climate shifts) and natural spread along the watercourses. Tolerance to heavy pollution and to low water mineralization, an ability to quickly establish high densities and large population sizes and to adapt to different salinities ensures high dispersal potential of the species. Most authors (Gumuliauskaite and Arbaciauskas, 2008; Arbaciauskas et al., 2011a, b; etc.) point to an adverse impact of the species on the richness, biodiversity and biomass of native macroinvertebrate assemblages, particularly due to an ability to suppress local species and to cause severe biocontamination. P. robustoides have been designated as a high-impact species and assigned as a ‘blacklist’ species for European inland waters (Arbaciauskas and Gumuliauskaite, 2007; Panov et al., 2009; Arbaciauskas, 2011b.) It is forecasted to spread despite any management initiated.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Arthropoda
  •             Subphylum: Crustacea
  •                 Class: Malacostraca
  •                     Subclass: Eumalacostraca
  •                         Order: Amphipoda
  •                             Suborder: Gammaridea
  •                                 Family: Gammaridae
  •                                     Genus: Pontogammarus
  •                                         Species: Pontogammarus robustoides

Notes on Taxonomy and Nomenclature

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The seminal review of gammarids was undertaken by Sars (1894-1895), who considered Ponto-Caspian amphipod fauna to form a part of the family Gammaridae sensu lato. Later, Martinov (1924, 1925) and Carausu (1943) added greater detail. Birstein (1945) proposed a modern classification concept which was later developed by Birstein and Romanova (1968) and, for the Black Sea area, by Mordukhaj-Boltovskoi et al. (1969). From the later work Stock (1974) derivated his key to the genera of the Dikerogammarus-Pontogammarus complex, which includes Dikerogammarus, Pontogammarus, Stenogammarus, Obesogammarus,Niphargoides and several other genera. Bousfield (1977) named the group ‘family Pontogammaridae’ and included it in the superfamily Gammaroidea. Pjatakova and Tarasov (1996) suggested simplifying the taxonomy of the genus Gammarus, grouping the Caspian gammarids in only 4 genera. In the latest revision by Lowry and Myers (2013)Pontogammarus included in the family Pontogammaridae Bousfield (1977) together with 11 other genera.

P. robustoides was fully described by GO Sars in 1894, but seems to be mentioned earlier by Grimm (1876, cited from Sars). In modern systematics Gammarus robustoides GO Sars (1894) is accepted as a basionym (WORMS, 2013). In earlier sources, especially Russian and Eastern European, the binomial name Gammarus robustoides (Grimm, 1894) is common. In 1924 a subspecies P. robustoides aestuarius was described by Derzhavin, but it is now classified as an independent species of Pontogammarus (Barnard and Barnard, 1983).

Description

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P. robustiodes has a typical amphipod body that is segmented throughout and laterally compressed, with a curved or hook-like profile. The body consists of a cephalothorax with two pairs of antennas, two eyes and mouthparts; pereon with 7 pairs of appendages (pereopods) mainly designed for movement; pleon with another 3 pairs (pleopods) and urosome carrying 3 pairs of uropods. The average body length is about 12 mm (range 4.5 - 21 mm) (Eggers and Martens 2001; Konopacka and Jazdzewski, 2002; Konopacka, 2004). Body colour is usually pale yellow.

Both pairs of antennae (A1 and A2) of the species are ‘Pontogammarus type’, i.e. short, more or less the same length, with the first segment of the A1 widened (Stock, 1974).

The pereopod 7 basis has a broad lobe, reaching not further than to the end of the next segment (ischium). The posterior-distal margin of basis P7 as well as the lower margins of coxal plates 1-4 have numerous long setae.

The armature of the urosomal segment 1 varies from a fan of delicate setae in medial part, to a row of 5-7 spines (Grabowski, 2011; Dobson, 2012). On urosome segment 2 there are always more than 2 spines in mid-dorsal group, usually 4-6. The center of urosome 3 holds a pair of slender spines close together. The endopod of uropod 3 has three clusters of spines on its outer edge and no spines visible on its inner edge; the urosome setae are straight, often with multiple small side branches (Dobson, 2012).

Distribution

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P. rubustoides belongs to a complex of Ponto-Caspian relic gammarids (Mordukhaj-Boltovskoj, 1960, 1964; Dedju, 1967; Greze, 1977). In its native range the species has been found in the brackish and freshwater bays of the Black Sea, the Azov Sea and the Caspian Sea; coastal lakes; and lagoons, lower courses and estuaries of major rivers of the Ponto-Caspian basin: Volga, Don, Kuban, Bug, Terek, Kura, Kuban, Dnieper, Dniester, Danube, Prut (Mordukhaj-Boltovskoj, 1964; Grabowski, 2011). The native range covers Russia, Turkey, the Caucasus, Romania, Bulgaria and Ukraine territories (Carausu et al., 1955; Mordukhaj-Boltovskoj et al., 1969; Dedju, 1980; Jazdzewski, 1980).

It is currently the most widely distributed amphipod in Lithuania, occuring in high abundance in: the Nemunas River below the Kaunas water reservoir and above it to the river-reservoir transition zone; Sesupe River and the lowest stretched of the Minija; the Nevezis, Neris and Sventoji Rivers; and the lower sections of the Merkys and Baltoji Ancia Rivers, including the damned-up stretch of the latter. It has been detected in small rivers and streams downstream of lakes where it occurs; stagnant waters of lakes and the Elektrenai and Antaliepte water reservoirs; and has been observed in the quarry close to Neman River.

Three new localities in Turkey have been identified by Ozbek (2011) which presently represent one of the southernmost points in distributional area of P. robustoides. Findings in Ladoga (Kurashov and Barbashova, 2008) are now its most northern locations.

As Gurianova (1951) and Mordukhaj-Boltovskoj (1960) suggested, this highly adaptable gammarid continues to spread outside the borders of its native range naturally. Nevertheless, human activity favours greatly the spread of P. robustoides along large rivers (Vistula, Oder, Neman, Elbe) and navigable canals and into artificial reservoirs as well as lakes (Grabowski, 2011). Since the middle of 20th century the distribution pattern of the species was affected by intentional introductions in water reservoirs in the Ponto-Caspian and Baltic region. Further information on the distribution is available in History of Introduction and Spread.

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, NortheastPresentIntroduced1960s Invasive Ezhova et al., 2005; Grabowski et al., 2006; Arbaciauskas, 2008; Grabowski, 2011; Strode et al., 2013South-Eastern Baltic Sea
Mediterranean and Black SeaWidespreadNative Invasive Markovskij, 1954; Carausu et al., 1955; Mordukhaj-Boltovskoj, 1960; Dedju, 1980; Özbek and Ustaoglu, 2006; Grabowski, 2011Native to fresh and brackish water coastal lakes and limans, estuaries (Volga, Don, Bug, Dnepr, Prut, Dniester, Kura, Danube, Terek, Kuban, etc), coastal zones, of Caspian, Azov and Black seas; lakes near the Marmara Sea

Asia

Georgia (Republic of)PresentNativeCarausu et al., 1955Lake Paleostom
TurkeyPresentNativeMordukhaj-Boltovskoj, 1964; Özbek and Ustaoglu, 2006; Ozbek, 2011Lakes of the southern and eastern coasts of the Sea of Marmara

Europe

BelarusPresentIntroduced Invasive Mastitsky and Makarevich, 2007Belarusian section of the Dnieper River
BulgariaPresentNativeCarausu et al., 1955Lake Sabla
EstoniaIntroduced Not invasive Timm, 2005; Herkül et al., 2009lake Võrtsjärv, did not establish a population
GermanyPresent1991Introduced Invasive Rudolph, 1997; Martens et al., 1999; Reinhold and Tittizer, 1999; Zettler, 2002Inland waters
LatviaPresentIntroduced1960 Invasive Grudule et al., 2007; Kalinkina and Berezina, 2010; Strode et al., 2013From Lithuanian waters; from 1999-2005 established in the lower reaches or mouths of Latvian rivers emptying into the Baltic Sea
LithuaniaPresentIntroduced1960s Invasive Arbaciauskas et al., 2011a; Gasiunas, 1972; Arbaciauskas, 2002; Arbaciauskas and Gumuliauskaite, 2007Introduced to Kaunas reservoir on the Neman river, then to regions located to the north
PolandWidespreadIntroduced Invasive Gruszka, 1999; Jazdzewski and Konopacka, 2000; Grabowski et al., 2006; Surowiec and Dobrzycka-Krahel, 2008; Dobrzycka-Krahel and Rzemykowska, 2010Inland waters
RomaniaCarausu et al., 1955Danube delta and canals, Lake Brates
Russian FederationPresentPresent based on regional distribution.
-Central RussiaPresentIntroduced Invasive Kurashov et al., 2012a; Berezina and Panov, 2003; Kurashov and Barbashova, 2008; Yakovleva and Yakovlev, 2010; Berezina et al., 2012; Gusev et al., 2012; Zuev and Malavin, 2012Upper reaches of Kuybyshev Water Reservoir
-Southern RussiaPresent2012Carausu et al., 1955; Kurina, 2012Saratov Water Reservoir
UkrainePresent2012Native Invasive Martinov, 1925; Carausu et al., 1955; Emelyanova, 1994Dnieper, low reaches

History of Introduction and Spread

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In addition to the natural ability of P. robustoides to extend its distribution, the process was speeded up by intentional transfers of potential fish food gammarids to hydropower reservoirs. P. robustoides was among 17 amphipod species that were used in these transfers during 1940–1970 in the Soviet Union (Jazdzewski, 1980). In the Ponto-Caspian region the intentional transfers took place in the Crimea water reservoirs (Zuravel, 1970) and Dnjepr water reservoirs (Mordukhaj-Boltovskoj, 1960; Emelyanova, 1994); in Baltic region the first transfers occurred during 1960–1961 into the newly constructed Kaunas water reservoir in the middle reach of the Nemunas River (Arbaciauskas and Gumuliauskaite, 2007). The rate and range of the invasions seems to have dramatically increased since the late 1980s, and from the 2000s many North and Central European river communities have been undergoing major change with the aggressive expansion of the species (Grabowski, 2011).

In the Ponto-Caspian region the spread was recorded for middle reaches of Dnjepr (Mordukhaj-Boltovskoj, 1960) and Volga Rivers. Filinova and Sonina (2012) suggested that in the latter the spread of gammarids could have been stimulated by intensive macrophyte growth which developed after a number of Volga water reservoirs were created in 1950-60s. For example, in the Volgogradsky water reservoir only a few specimens of P. robustoides were reported in the beginning of 1980s, but by 2000 the species had spread up and established in a number of Volga Water Reservoirs (Zynchenko et al., 2008, Zinchenko and Kurina, 2011) as far as Kuybyshev water reservoir (Yakovleva and Yakovlev, 2010; Kurina, 2012).

The history of P. robustoides in the Baltic Sea basin begins in the 1960s, when it was introduced from the Black Sea basin (from the Dnjepr Reservoir and the Simferopol Reservoir, Crimea) to Kaunas Reservoir on the Neman River, as well as a number of local lakes in Lithuania (documented by Gasiunas, 1972). In the same period several undocumented introductions in the same region occurred (Arbaciauskas, 2002). Arbaciauskas et al. (2011a) summarized the invasion pattern of the species in the Neman River basin. They suggested that there was no upstream expansion from the Kaunas Water Reservoir, but that invasion of the middle section of the river happened by downstream dispersal from Lake Daugai where it was introduced in 1965. P. robustoides was observed in the stream flowing from Lake Daugai and further downstream, and in 2007 in Merkys Rivers, characterized as a cold-water river. An expansion rate of the species is considered to be about 2 km per year. In some rivers such as the Šešupe and Minija, P . robustoides has been detected quite far upstream, showing an ability of the species to spread upstream. Probably due to this ability, the crustacean was found in Lake Lušiai, which it penetrated from Lake Žeimenys through a narrow canal with strong flow velocity upstream.

Arbaciauskas et al. (2011a) presumed that the presence of P. robustoides in the mouth of the Šventoji River indicated that their local spread may have been facilitated by marine shipping or that the species may be capable of migration through coastal Baltic waters. The idea that P. robustoides dispersed from the Neman drainage system through Baltic waters (Curonian Lagoon) by passive dispersion and/or shipping into other European water systems has been supported by data from many sources (Gasiunas, 1972; Jazdzewski and Konopacka, 2000; Arbaciauskas 2002; Grabowski, 2011; Kurashov et al., 2012b).

From 1999-2005 this species was recorded as an established biological component of the lower reaches or mouths of Latvian rivers emptying into the Baltic Sea (Grudule et al., 2007). The spread of P. robustoides in the lower reaches of the Daugava River and its water reservoirs must have originated from the intentional introduction of this species into the Keguma Water Reservoir in the 1960s. Meanwhile, the invasion of P. robustoides into the lower reaches of other Latvian rivers and nearshore lakes, including the vicinities of the Baltic Sea ports Ventspils and Liepaja, was probably due to hull fouling of ships. The closest source populations which might have contributed to the dispersal of this aquatic invader are in the Curonian Lagoon and the mouth of the Daugava River.

The species is thought to have reached Baltic waters in the 1980s and 1990s, before spreading further southwest. It possibly entered Vistula lagoon with ballast or littoral waters via Curonian Lagoon or through the Pregola river system which connects the Vistula river delta with the lagoon (Arbaciauskas and Gumuliauskaite, 2007; Dobrzycka-Krahel and Surowiec, 2001). A possible alternative route, via the Pripet-Bug canal from Dnieper into the Vistula, has also been suggested (Jazdzewski and Konopacka, 2000; Panov et al., 2009). Since the 1990s the gammarid fauna of this river has almost completely been dominated by the Ponto-Caspian species Dikerogammarus haemobaphes Eichwald (1841) and P. robustoides Sars (1894) (Konopacka, 1998; Jazdzewski et al., 2004). The species was found in the lower stretches of rivers emptying directly into the Baltic Sea (Jazdzewski et al., 2004), in the Wloclawski Reservoir, the central Polish lakes Lucienskie and Zegrzyn´skie (Jazdzewski et al., 2004; Grabowski and Bacela, 2005; Grabowski et al., 2006, 2007) and the Great Masurian Lakes (Jazdzewska and Jazdzewski, 2008). Zuev and Malavin (2012) found P. robustoides in Luga river and Luga bay, Kaliningrad, Russia.

The species was first recorded from the Szczecin Lagoon, which is a part of the Oder River basin, in 1988 (Gruszka, 1999). Later it was registered from a number of waterbodies and canals in north-eastern Germany (Rudolph, 1997; Zettler, 1998; Martens et al., 1999). Zettler (2002) noted that P. robustoides shows a wide dispersion in its main distribution area in the lakes of Mecklenburg-Vorpommern. As an alternative hypothesis for its dispersion into central Europe and Germany, the initial invasions of P. robustoides in central Europe might have been stimulated by the creation of canal networks in the late 18th century, connecting the major eastern and western European river systems. In this way Vaate et al. (2002) suggested that P. robustoides could have reached the Oder systems, as well as northeastern Germany, via the so called ‘central corridor’, covering the route from the River Dnieper through the Vistula to the Oder and later to the Mittellands-kanal.

During the 1990s P. robustoides continued to spread along the Baltic shore in the north-east direction. In the mid-1990s it was recorded from the easternmost part of the Gulf of Finland (Berezina and Panov, 2003). In 2009 it was found also in the shallow waters of Gulf of Riga, near Yurmala, in Latvia (Kalinkina and Berezina, 2010). P. robustoides has also been found in Ladoga lake (Kurashov and Barbashova, 2008). Berezina et al. (2012) reported the species from many locations on the south shore of Neva bay (Gulf of Finland) as well as in the northern part of the bay, near Repino-Ushkovo.

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Baltic states Krymskaya Oblast 1960s Interconnected waterways (pathway cause) ,
Self-propelled (pathway cause)
Yes Arbaciauskas (2002); Arbaciauskas and Gumuliauskaite (2007); Gasiunas (1972); Grudule et al. (2007); Gruszka (1999) From the Black Sea basin (from Dnepr Reservoir and Simferopol Reservoi) to The Baltic Sea basin
Latvia Baltic states After 2000 Interconnected waterways (pathway cause) ,
Self-propelled (pathway cause)
Kalinkina and Berezina (2010); Strode et al. (2013) First established in lower reaches of Latvian rivers emptying into Baltic Sea; in 2009 found in Gulf of Riga; in 2013 in coastal lake Liepaja
Poland Before 1990 Interconnected waterways (pathway cause) ,
Self-propelled (pathway cause)
Yes Grabowski and Bacela (2005); Gruszka (1999); Jazdzewski et al. (2002) After 1990 colonised some lakes in Vistula Valley

Risk of Introduction

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P. robustoides exhibits the high dispersal potential and is constantly expanding its range of distribution. Many authors (Herkul et al., 2009; Panov et al., 2009; Strode et al., 2013) indicate that further spread is possible across European freshwater bodies and gulfs of the Baltic Sea in the near future.

Arbaciauskas (2005; 2011a) expected that distributions of P. robustoides in the Lithuanian fresh waters were likely to increase. However, its expansion across small, stagnant waters may be limited, because the species is only able to survive long-term in large lakes.

Dobrzycka-Krahel and Surowiec (2011) indicated that the species will soon colonize Swedish and Danish waters, although it has not yet been recorded there. The presence of this species in the Mittelland canal may already signal its present in the North Sea basin (Arbaciauskas and Gumuliauskaite, 2007).

Kurashov et al. (2012a) predicted that P. robustoides may extend its range in Lake Ladoga, particularly in the littoral habitats.

In the UK P. robustoides is considered as a potentially invasive species (Dobson, 2012).

Based on experimental data of Santagata et al. (2008), P. robustoides may be more likely to be introduced to freshwater and estuarine waters of the eastern United States than other any other northern Europe amphipod species.

Habitat

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The species is usually found in the open shallow waters among macrophytes growing on a sand or silted sand bottom (Emelyanova, 1994). Zytkowicz et al. (2008) observed that P. robustoides was the only amphipod species to live on very shallow < 1 m) sandy subtrates, near the shore of the Wloclawek Dam Reservoir on the lower Vistula River (central Poland). With increasing distance from the shore P. robustoides represented a smaller portion of total amphipods, but affinity for plant substratum became higher.

Czarnecka et al. (2010) studied the preferences of P. robustoides for various macrophyte species. It was discovered that juvenile and adult gammarids exhibited different habitat preferences. Adults did not discriminate between artificial and natural substrata, or among most of the tested species of plants (Myriophyllum spicatum, Ceratophyllum demersum, Potamogeton perfoliatus, Elodea canadensis), whereas juveniles preferred all tested macrophytes over artificial substrata and preferred plants with finer leaf elements, i.e. M. spicatum and C. demersum over the other plants and E. canadensis over P. perfoliatus. The authors suggested that the habitat separation between juvenile and adult stages may help survival in a new environment and increase P. robustoides’ invasive potential by reducing intraspecific competition and cannibalism.

The indiscrimination of adult stages regarding substrate may also explain why the species, considered to be strictly phytophilous by some authors (Mordukhaj-Boltovskoj, 1960; Dedju, 1980), is often found on stony or sand-muddy bottom (Carausu et al., 1955, Berezina and Panov, 2003; Grabowski, 2011; Kurina, 2012). Berezina and Panov (2003) also noted that P. robustoides individuals living on the open stone littoral of Neva Bay (Gulf of Finland) tend to be an active predators because in such habitat plant food is limited.

Habitat List

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CategoryHabitatPresenceStatus
Brackish
Estuaries Principal habitat Harmful (pest or invasive)
Estuaries Principal habitat Natural
Inland saline areas Principal habitat Harmful (pest or invasive)
Inland saline areas Principal habitat Natural
Lagoons Principal habitat Harmful (pest or invasive)
Lagoons Principal habitat Natural
Freshwater
Lakes Present, no further details Harmful (pest or invasive)
Lakes Present, no further details Natural
Reservoirs Secondary/tolerated habitat Harmful (pest or invasive)
Rivers / streams Present, no further details Harmful (pest or invasive)
Rivers / streams Present, no further details Natural
Littoral
Coastal areas Present, no further details Harmful (pest or invasive)
Coastal areas Present, no further details Natural

Biology and Ecology

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Genetics

Bragin (2006) undertook molecular-genetic analysis of amphipod populations in the zone of secondary contact within 50 years of the construction of the Volga-Don canal, with the aim of studying the role of geographical isolation in speciation and establishment of reproductive isolation. Methods of molecular identification have been developed to distinguish the origin of mitochondrial genotypes for some amphipods of the Ponto-Caspian complex. The species was analyzed by sequencing the Folmer fragment of gene COI and then comparing it with Azov-Black Sea and Caspian populations. The author found that P. robustoides with Caspian and Asov-Black Sea types of mitochondrial DNA coexisted in a mixed population, thus suggesting the absence of reproductive barriers between the original population and immigrants from the Volga, and active penetration of P. robustoides from the Volga to the Don.

Reproductive Biology

The life cycle of P. robustoides consists of direct development with no independent larval stage. Females carry their embryos in a brood chamber between the pereopods. When released, the juveniles reach maturity after several molts, without any metamorphosis.

The fecundity of the species is very high. Berezina and Panov (2003) observed  30 to 106 eggs per female, which resulted in the successful establishment of the species in the eastern Gulf of Finland during a short period. In Lithuaniana (Arbaciauskas and Gumuliauskaite, 2007) the fecundity was estimated at 34 to 167 eggs per female, higher than other amphipods in the region; similar estimates (11 – 185 eggs) have come from Poland (Bacela and Konopacka, 2005).

In its native habitat P. robustoides produces no less than two generations per year, and sometimes up to 5-6 generations per year (Mordukhaj-Boltovskoj, 1960). In Central Europe (Bacela and Konopacka, 2005), P. robustoides has a multivoltine life cycle, with three generations per year (spring, summer and autumn). Reproduction lasts from March/April until October, when the last breeding females are found. The first juveniles appear in May and are present in the population until the end of October. Spring and summer generations mature in a very short time (4–5 weeks). Females born in May and July start breeding at a body length of 8.5 mm, whereas the length of overwintering females breeding in spring ranges from 11 to 18 mm. The number of eggs laid is exponentially correlated with the size of a female. A similar tri-annual generation pattern was observed for populations in Curonian lagoon and has been suggested for Lithuanian populations (Arbaciauskas and Gumuliauskaite, 2007).

Physiology and Phenology

Poznanska et al. (2013) surveyed an effect of substratum drying on the survival and migrations of P. robustoides. P. robustoides was the most resistant to substratum drying (out of three Ponto-Caspian invaders and the native Gammarus fossarum) and was the only species which buried into the substratum, while G. fossarum usually migrated following the retreating waterline. This ability allows the species to invade and persist in habitats which experience water level fluctuations.

P. robustoides inhabits numerous water bodies with a wide range of salinities and displays flexible osmotic capacity. Dobrzycka-Krahel and Surowiec (2001) described the osmoregulatory curve of P. robustoides as ranging from 0 to 23 PSU. The wide range indicates the hyperosmotic nature of osmoregulation in this species and its considerable ability to adapt to different environmental salinities.

Population Size and Density

In its native habitat P. robustoides may be characterised by large population size and high densities. For example, in the Don estuary, maximum density was 4280 ind/square meter, and biomass 70.100 g/square meter (Mordukhaj-Boltovskoj, 1960).

The ability of this species to quickly establish large and high-density populations when invading a new environment is well known. Herkul et al. (2009) noted that when P. robustoides first found in 2006 in Estonia, it was present only in one sample. The abundance and biomass were 300 ind/square meter and 0.698 g/square meter, respectively. In 2007 and 2008 it was found about 7 km eastwards of the location of the first record. The abundance and biomass increased up to 1200 ind. m(-2) and 2.044 g (-2), respectively.

In the Neva Estuary, Berezina and Panov (2003) observed 4-fold increase of alien gammarids (P. robustoides and Gmelinoides fasciatus) from 2000 to 2002. From 2002 to 2005 P. robustoides, together with G. fasciatus, accounted for 73% of the total biomass of zoobenthos (Berezina et al., 2007). The absolute abundance of the gammarids G. fasciatus and P. robustoides ranged from 200 to 4800 ind/m(-2), with the highest levels in June and July of 2003 (Berezina et al., 2005).

From the time P. robustoides was first recorded in the Szczecin Lagoon (between Poland and Germany) in 1988 its density has exceeded 10,000 ind/m(-2), while the biomass was 140 g/ m(-2) (Wawrzyniak-Wydrowska and Gruszka, 2005).

In Gulf of Riga (near Jurmala City, Latvia), the abundance ranged from 1–70 ind/m(-2) in 2011-2012 (Strode et al., 2013). From eighteen observed sites in the littoral areas in 2012, P . robustoides was found at more than half the sites.

When the species was recorded for the first time in Lake Ladoga in August 2006 (Kurashov and Barbashova, 2008), its biomass accounted for 15% of the total macrobenthos, or 864 mg/ m(-2) (24 ind/ m(-2).

Gumuliauskaite and Arbaciauskas (2008) noted that in some Lithuanian lakes P. robustoides accounted for 10-90% of total benthic animal biomass, reaching a maximum 3347 ind/m(-2) in Lake Dusia.

Environmental Requirements

In its native regions P. robustoides lives in freshwater and oligohaline zones but not in mesohaline waters (Mordukhaj-Boltovskoj, 1960). The osmoregulatory curve of P. robustoides ranges from 0 to 23 PSU (Dobrzycka-Krahel and Surowiec, 2011), which allows the species to survive in the wide range of salinities.

In the Baltic region P. robustoides is recorded from brackish waters (Dobrzycka-Krahel and Rzemykowska, 2010), such as Szczecin Lagoon (between Poland and Germany), where the salinity (1-2 PSU) is regulated by the inflow of both seawater and fresh waters and at the Vistula mouth and the Vistula Lagoon (0.3-4 PSU). Investigations have shown that this species can also survive at salinities from 5.8 to 6.1 PSU in the Gulf of Gdansk (Dobrzycka-Krahel and Rzemykowska, 2010).

The spread of the species in Europe indicates that it is capable of colonizing waters of ever higher salinities. In 1999, P. robustoides was found in Neva Bay (Gulf of Finland) (Berezina and Panov, 2003), where salinity ranges up to 7 PSU. It has been recorded successfully reproducing at 0.2 – 7 PSU in Narva Bay in 2006 (Herkül et al., 2009), and in 2009 in the Gulf of Riga, where the salinity is 7.7 PSU at the bottom of the Irbe Strait in spring and summer (Kalinkina and Berezina, 2010). Laboratory investigations have shown that this species can survive in fully saline sea water (up to 34 PSU) (Santagata et al., 2008).

It appears that low levels of total dissolved salt concentration also affect P. robustoides distribution. Kurashov and Barbashova (2008) discovered that among the 28 habitats surveyed on the perimeter of Lake Ladoga (northwestern Russia), P. robustoides was discovered only in Volkhov Bay, where water conductivity (0.241 mS/m, corresponding TDS=0.154 g/l) was more than twice the maximum value of the majority of the other investigated littoral stations. Low total dissolved salt concentration is therefore thought to be the reason for P. robustoides absence in other areas of the Lake Ladoga littoral zone. This speculation is in accordance with the data on the distribution of P. robustoides in Neva Bay (Gulf of Finland), where it was absent in its northern part, which had the lowest salt content (TDS=0.042-0.075 g/l, corresponding conductivity 0.066-0.117 mS/m), due to the strong influence of the Neva River (Berezina et al., 2007). Later, however, the species was found by Kurashov et al. (2012a) in Ladoga water with even lower salt content (0.074 g/l), which indicates the possibility of further expansion of P. robustoides along the littoral areas of Lake Lagoda. In Poland the species is usually found in waters with salinity greater than 0.4 PSU, but may enter and reproduce in waters with salinity as low as 0.2 PSU (Grabowski and Bacela, 2005).

The impact of different concentrations of various salts should be subject of future research. Chekunova (1960) revealed the importance of K and Ca metabolism on the survival of the species. Berezina and Panov (2003) found that the concentration Na+ should be at least 17 mg/L(-1) for successful reproduction of P. robustoides; however, the species has been found in Lithuanian lakes with Na+ as low as 3.4 mg/L(-1) (Arbaciauskas and Gumuliauskaite, 2007).

Usually occupying shallow waters, P. robustoides is characterized as a species of high oxygen demand (Mordukhaj-Boltovskoj, 1960; Arbaciauskas, 2005; Arbaciauskas and Gumuliauskaite, 2007; Gumuliauskaite and Arbaciauskas, 2008). Nevertheless, it has an ability to withstand the lowest oxygen content when compared to other amphipods (Arbaciauskas and Gumuliauskaite, 2007), which allows the species to be successful in stagnant waters. In higher latitudes, however, where stagnant waters may be ice-covered for a part of year, oxygen content may be eliminating factor for the long-term survival of P. robustoides.

Mordukhaj-Boltovskoj (1960) noted that water velocity in typical a river habitat for gammarids is 0.3-0.6 m/sec. Arbaciauskas and Gumuliauskaite (2007) noted that the species tries to avoid lotic waters.

Effect of temperature on P. robustoides has not yet been studied in detail. In its native habitat water temperature may vary from 0 to 30ºC (Mordukhaj-Boltovskoj, 1960). Kurashov et al. (2012b) noted that increasing average annual temperatures of upper water levels in European lakes (such as Lake Lagoda) in the 20th century favours their invasion by Ponto-Caspian species.

Natural Food Sources

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Food SourceLife StageContribution to Total Food Intake (%)Details
Cladophora glomerata All Stages 100%

Climate

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ClimateStatusDescriptionRemark
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 Tolerated Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)

Water Tolerances

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ParameterMinimum ValueMaximum ValueTypical ValueStatusLife StageNotes
Dissolved oxygen (mg/l) 0.209 Harmful Arbac?iauskas, Gumuliauskaite, 2007
Salinity (part per thousand) 0 23 Harmful 0-4 PSU. The mean osmotic capacity is highest at the lowest salinities (0-3 PSU) and the lowest at 9 PSU, and the values are relatively low at salinities of 5, 7, 11, and 23 PSU (Dobrzycka-Krahel, Su

Notes on Natural Enemies

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Several microparasites of invasive gammarids in Polish waters have been recognized (Ovcharenko et al., 2009; Ovcharenko and Yemeliyanova, 2009). Four species of gregarines (Uradiophora ramosa, U. longissima, Cephaloidophora similis, C. mucronata) and five microsporidians (Nosema dikerogammari, N. pontogammari, Thelohania sp. 2, Thelohania sp. 5; Pleistophora muelleri) were associated with hosts of Ponto-Caspian origins. Infestation rates did not exceed 3%. The authors did not register any transition of parasites of the Ponto-Caspian hosts to the hosts of native fauna.

Means of Movement and Dispersal

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P. robustoides disperses both naturally and via human activity. It seems to have expanded in the Baltic Sea via jump dispersal, clearly suggesting strong involvement of anthropogenic factors (Arbaciauskas and Gumuliauskaite, 2007). Most probably, the species spreads along the inshore Baltic waters and penetrates inland waters through shipping (Reinhold and Tittizer, 1997, 1999; Jazdzewski et al., 2002; Grabowski et al., 2003; Grabowski and Bacela, 2005), either with ballast waters or in the hull fouling of ships. However, some authors note that the species is able to survive the salinity concentration in the Baltic Sea, so natural dispersion should not be discounted (Berezina and Panov, 2003).

Natural Dispersal

The species is able to disperse naturally, as was shown by Arbaciauskas et al. (2011a) in the Neman River basin. The authors suggested that there was no upstream expansion from the Kaunas Water Reservoir and that the invasion of the middle section of the river happened by downstream dispersal from Lake Daugai, where it was introduced in 1965. Further dispersial in rivers and lakes may have occurred both upstream and downstream. The ability to natural disperse through freshwater streams might contribute to the distribution of this species through rivers and channel routes in Europe (see Distribution).

Accidental Introduction

A number of accidental and unregistered introductions may have happened in some Lithuanian water reservoirs and lakes after intentional introductions in 1960s (Arbaciauskas, 2005; Arbaciauskas and Gumuliauskaite, 2007).

Intentional Introduction

Intentional introductions of P. robustoides into water reservoirs and lakes, such as in the Ponto-Caspian  Baltic regions, took place after 1960. In the Ponto-Caspian region the species was introduced in a number of Dniepr water reservoirs and in the Simpheropol water reservoir (Crimea). The first site of introduction in the Baltic region was the Kaunas water reservoir. There then followed a number of other reservoirs and lake in the region.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
AquacultureIntroduced in the middle of XX century as fish-food resource in Baltic region Yes Yes Arbaciauskas et al., 2010; Grabowski, 2011; Panov et al., 2009
HitchhikerIn ship fouling Yes Yes Arbaciauskas, 2005; Kurashov et al., 2012a
Intentional releaseIn waterreservoirs and lakes as fish-food Yes Yes Arbaciauskas et al., 2010; Grabowski, 2011; Jazdzewski et al., 1972
Interbasin transfers Yes Yes Grabowski, 2002
Interconnected waterwaysDistrbution through Europe via system of interconnected channels Yes Yes Panov et al., 2009

Impact Summary

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CategoryImpact
Economic/livelihood Negative
Environment (generally) Negative

Economic Impact

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During the period of active introductions of different marine invertebrates in Ponto-Caspian territories of the Soviet Union during the 1950s and 1960s, most authors considered the species to be an effective source of fish food (Markovskij, 1954; Emelyanova, 1994). Later, P. robustoides was noted in food chains of local and introduced fish. Investigation of fish nutrition in Keguma water reservoir during 1971-1972 showed that P. robustoides accounted for 36-48% of perch diet during certain periods (Grudule et al., 2007). In Poland (Vistula River, Szczecin Lagoon, Vistula Lagoon etc.), where native gammarids have disappeared, the species provides a food base for many local fish species (Kostrzewa and Grabowski, 2003; Grabowska and Grabowski, 2005) as well as invasive fish species (Grabowski et al., 2007), such as racer goby Neogobius gymnotrachelusKessler (1857) and monkey goby Neogobius fluviatilisPallas (1814). On the other hand, P. robustoides may be a vector of alien parasites and transfer them to local fish species (Ovcharenko, 2006).

Unfortunately, the gammarid aquaculture seems not to have been developed sustainably, and the large-scale consequences of the P. robustoides introductions have been rather adverse. Rakauskas et al. (2010) found that, although perch underwent an earlier diet shift from zooplankton to introduced macroinvertebrates in Lithuanian lakes, the abundance of introduced crustaceans had no impact on the breadth of the perch feeding niche. Moreover, Arbaciauskas et al. (2010), having compared littoral fish communities of different lakes in Lithuania, found that commercial catches in the lakes with the most numerous populations of introduced species showed no significant effect on fish production. The authors concluded that the introduction of alien fodder species was ill advised from an economic perspective and harmful from an environmental perspective.

Environmental Impact

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In many locations the activity of P. robustoides has had a significant impact on biodiversity.

Berezina and Panov (2003) described the favourable impact of P. robustoides on food webs. By intensively consuming plant food, P. robustiodes produces abundant faeces which increase organic matter availability for benthic detritovores. In the Gulf of Finland, for example, at gammarid densities of 500-3000 ind/m(-2), the densities of deitritovores were 2-3 times as high. However, such activity also causes severe biocontamination, which was demonstrated by Arbaciauskas et al. (2011b) for Lithuanian rivers.

With increasing in gammarid densities, the replacement of previously co-existing species and shifts in the densities of native invertebrates occurs. Orlova et al. (2006) believed that P. robutsoides has strongly affected the community structure in the eastern Gulf of Finland since 1998. Berezina and Golubkov (2008) noted on significant impact of the species in the Neva Eastuary. In Lithuanian lakes, significant reductions in species richness (1.5- to 1.6-fold), in community diversity (more than twofold) and in the biomass of indigenous invertebrates (excluding chironomids, which exhibited high lake-specific biomass variation) in the places with well-established P. robustoides populations have been described by Gumuliauskaite and Arbaciauskas (2008).

The impact of P. robustoides on native crustaceans has been studied in detail. In the brackish Vistula Lagoon (in the Baltic Sea), a decline of native Gammarus zaddachi and Gammarus duebeni was reported parallel to the appearance of P. robustoides and other alien amphipods (Jazdzewski et al., 2004; Ezhova et al., 2005; Grabowski et al., 2006). Gumuliauskaite and Arbaciauskas (2008) observed a detrimental impact of the species upon the native isopod Asellus aquaticus and a negative correlation with most of the higher taxa of native invertebrates. Arbaciauskas (2005, 2008) described a decline of Gammarus lacustris and other native gammarids in Polish freshwaters as a result of adventive gammarid species. According to Dobrzycka-Krahel and Surowiec (2008), long-term studies in the Vistula Delta and Lagoon have shown a dramatic decline in the native gammarid species Gammarus duebeni, G. zaddachi, G. salinus, G. oceanicus and G. varsoviensis and the complete replacement of Chaetogammarus ischnus by other non-indigenous gammarids.

P. robustoides may also affect macroinvertebrates in a specific way. Kobak et al. (2012) discovered that Ponto Caspian gammarids within mussel colonies have the capacity to compromise the normal functioning of bivalves by inducing responses in them similar to their anti-predator defenses. The most likely factor causing these changes was mechanical irritation of their soft parts by amphipod appendages.

P. robustoides may serve as a vector for microparasites (See Notes on Natural Enemies); however, at present there are no reports on the possible transfer of pathogens to native species.

Apart from its influence on local fauna, P. robustoides also affects algae biomass. Gasiunas (1972) showed that an established population of P. robustiodes in littoral zones of Lithuanian lakes contributed to disappearance of Cladophora in five years. Berezina and Golubkov (2008) hypothesized that the alien amphipods Gmelinoides fasciatus and P. robustoides are able to control macroalgae biomass in the eastern Gulf of Finland. The data obtained clearly indicated that the grazing amphipods can have a dramatic impact on C. glomerata in the littoral zone of the eastern Gulf of Finland, and perhaps influence the macroalgal biomass when their populations are dense.

Generally, there is increasing evidence to suggest that P. robustoides has an adverse impact on the richness, biodiversity and biomass of native littoral assemblages. Possible reasons for the observed effects are increasing pollution and eutrophication, accompanied by competition between native and the alien species. The selective predation of invasive amphipods on native invertebrates is also considered to be a main impact mechanism.

Risk and Impact Factors

Top of page Invasiveness
  • Invasive in its native range
  • Proved invasive outside its native range
  • Abundant in its native range
  • Highly adaptable to different environments
  • Pioneering in disturbed areas
  • Capable of securing and ingesting a wide range of food
  • Fast growing
  • Has high reproductive potential
  • Gregarious
Impact outcomes
  • Altered trophic level
  • Ecosystem change/ habitat alteration
  • Modification of natural benthic communities
  • Modification of nutrient regime
  • Reduced native biodiversity
  • Threat to/ loss of native species
Impact mechanisms
  • Herbivory/grazing/browsing
  • Predation
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Uses

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Economic Value

The economic value of the species as fish fodder is noted by some authors (see Economic Impact), but remains understudied. Any economic value of P. robustoides is outweighed by the negative consequences of introductions.

Environmental Services

Emelyanova (1994) suggested the species could serve as a pollution indicator, based on its tolerance to different types of contamination, particularly radiation.

Uses List

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Animal feed, fodder, forage

  • Fishmeal

Detection and Inspection

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Some guides for invasive amphipod species identification are published in Germany (Eggers and Martens, 2001), Poland (Konopacka, 2004; Konopacka and Jazdzewski, 2002), the UK (Dobson, 2012) and Russia (Tsalolikhin, 1995). An identification guide of some pontogammarids from the Dikerogammarus-Pontogammarus complex is offered by Stock (1974).

Similarities to Other Species/Conditions

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P. robustoides may be confused with other gammarid species. The most characteristic details of P. robustoides morphology are given in the Description section. Descriptions useful for distinguishing similar species are given in Eggers and Martens (2001), Konopacka (2004), Konopacka and Jazdzewski (2002), Dobson (2012) and Stock (1974).

Prevention and Control

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Monitoring the spread of P. robustoides in Europe has already started in several countries (e.g. Poland, Germany, The Netherlands). At the moment, eradication and control of P. robustoides does not seem feasible (Grabowski, 2011).

Public Awareness

Development of simple identification keys and leaflets, with the aim of raising public awareness of P. robustoides, are recommended.

Monitoring and Surveillance (incl. Remote Sensing)

The species is difficult to monitor because specialist expertise is needed to identify it.

References

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