Native range of the zebra mussel and quagga mussel and new data on their invasions within the Ponto-Caspian Region

This is a special review on the native ranges of the zebra mussel (Dreissena polymorpha polymorpha) and quagga mussel (Dreissena bugensis). Revision of museum collections showed that the Dniepr Delta is a native locality of the quagga mussel, for example in the Lower Southern Bug and that Dreissena presbensis occurs in the Aegean Sea Basin in Greece. The native range of the zebra mussel includes Danube, Dniestr, Berezan, Southern Bug, Dniepr, Molochnaya, Don, Kuban, Kamchia, and Veleca river basins; isolated and semi-isolated relic estuarian reservoirs along the Bulgarian, Romanian, Ukrainian, and Russian Black and Azov seas coasts; and in zones of these seas influenced by freshwater. Invasive dreissenids in Turkish rivers are local species and subspecies. More recent locations of the dreissenid expansion within the Ponto-Caspian region (Lake Sasyk, Baraboj River, and Sukhoj Liman Basin for the zebra mussel; Dniestr River Basin for the quagga mussel) are described. One empty valve of Dreissena polymorpha andrusovi was found in the Taganrog Bay.


Introduction
Freshwater dreissenids have attracted attention for a long time.Two species of freshwater Dreissena: Dreissena polymorpha (Pallas, 1771) and Dreissena bugensis (Andrusov, 1897) have been indicated as invaders in different continents (Kharchenko 1995, Bobat 2004, Orlova 2004, Therriault et al. 2005, Gelembiuk et al. 2006, May et al. 2006, Molloy et al. 2007).Interest in both species is enormous: and the bibliography on their ecology and impact according to Schloesser et al. (1994) numbers thousands of papers.
While the overwhelming majority of publications on Dreissena concerns invasive range, information on distribution within their native range is limited.Even in a special review on the distribution of dreissenids in Ukraine (Kharchenko 1995) there is almost no data present on their native range.Knowledge about borders of dreissenid native range and nearby expansion is very important for both studies and prediction of their widespread expansion.
These studies did not include some regions with autochthonous populations of freshwater dreissenids: rivers and relic lakes along the Bulgarian Black Sea Coast (Hubenov 2005), Lake Volvi and the Aliakmon River from the environs of Thessaloniki in the Aegean Sea Basin (Greece) (Zarfdjian 2000).
Our study on dreissenids from Lake Volvi (collection of Zoological Institute of Russian Academy of Sciences, St.-Petersburg; coll. A. Yu.Karatayev, N 40°37´50" -40°41´50", E 23°21´10" -23°36´40"; 27 October 1995) showed these to be D. presbensis (Figure 1).According to labels, the late Starobogatov intended further revisions in the identification of these specimens.Data on D. polymorpha from Bulgarian Black Sea Coast was not used in taxonomic revisions, and will be considered as D. polymorpha polymorpha unless disproved.So, the native range of D. polymorpha polymorpha is limited by the Northern Black Sea Region and the Caspian Basin.
With rare exceptions, only dreissenids from the Northern Black Sea Region are known as invasive species.Expansion of other dreissenids is localized in nature and mainly of concern to Turkey.Local dreissenids invaded many reservoirs in the Turkish Euphrates River Basin, Aegean, Mediterranean, and Black Sea coasts (Bobat 2004), but data on the expansion of separate species and subspecies are absent.As is generally known, the dreissenids which invaded the Seyhan Dam Reservoir were D. caputlacus and D. polymorpha anatolica (Gelembiuk et al. 2006).According to Bobat (2004) at least some cases of dreissenid expansion in the Turkish Black Sea Basin (Lakes Acarlar in the Sakarya Basin and dams on the Kizilirmak Basin) concerned D. polymorpha gallandri (native to the surroundings of Istanbul and Lake Uluabat in the Marmara Sea Basin).
Among Caspian dreissenids, we found one empty valve of Dreissena polymorpha andrusovi (Brusina in Andrusov, 1897) in the western part of Taganrog Bay (Figure 2).The subspecies is wide-spread in the Northern Caspian Sea.This shell might have been being dropped as empty valve with building sand or by a ship.

Material and Methods
This paper is based on material collected by the author as well as on literature data.Original material is deposited in the mollusk collection of the Odessa Branch Institute of Biology of the Southern Seas (OB IBSS).All collected material  was fixed in 70% ethanol.Danube, Dniepr, Dniestr, Don, and Volga river basins, small rivers and reservoirs of the Azov and Black sea coasts were investigated annually from 1999 to 2007.Field research was undertaken according to standard methods (Zhadin 1965).

Borders between native and invasive ranges of the zebra mussel
The modern native range of D. polymorpha polymorpha includes different habitats in the Ponto-Caspian Region.
In the rivers of the Caspian Sea Basin (Volga and Ural deltas) D. polymorpha polymorpha occurs in biotopes of river channel and wetlands (Pirogov 1974, Pirogov et al. 1994).
In the Azov-Black Sea Basin (where estuarian biotopes are characterized by higher diversity, than in the Caspian Sea Basin) the native range of the zebra mussel has a complicated disjunctive structure.This kind of native range causes high geographical variability in D. polymorpha polymorpha (Figure 3).
In eastern Bulgarian lakes the zebra mussel was situated within the Sinoie-Razim lagoonal complex (Romania) connected with Danube Delta.
In the Danube Basin it occupied riverine lentic habitats and associated estuarine reservoirs -Kagul, Kugurluj, Yalpug, Katlabug, and Kitaj (Grossu andPaladian 1956, Milashevich 1908, new data).Along the Danube channel it was located as a native species up to the Middle Danube (Mordukhay-Boltovskoy 1960).We found it also in a zone of the Black Sea, freshened by the Danube (shallows Kurilskije).
The zebra mussel occurred in branches of the Dniestr Delta and in the main channel of the Lower and Middle Dniestr, and in estuarine reservoirs -Dniestr Liman and Kuchurgan Liman.In the Middle Dniestr we observed the largest specimens of the zebra mussel (length of the shell = 49 mm) found in all native habitats (Figure 4).
Along the coasts of the Dniestr Liman, D. polymorpha polymorpha was found in streams (the first records of Ponto-Caspian bivalves in this type of habitat).It now seems to have disappeared from the floodplain lakes of the Dniestr, where it was recorded in last century (Grinbart 1967).This is probably connected with disimproved oxygen levels in these reservoirs.In the Dniestr Liman the zebra mussel was recorded in the northern (freshwater) and central (brackishwater) parts and in springs in its basin.
In the Tiligul Liman, where D. polymorpha polymorpha was identified in the early twentieth century (Grinbart 1967) it disappeared after a rise in salinity when the liman was connected by channel with the Black Sea.
In the Berezan Liman, the zebra mussel occurs in brackish water in central and northern parts of the liman (Grinbart 1955).We found it also in the Lower Berezan River.
In the Southern Bug River and Dniepr River the zebra mussel was located in the lower and middle stretches including a zone upstream of rapids (up to Vinnitsa City and Kiev accordingly) (Polishchuk 1978, Krasheninnikov 1929).This species also occurred in their large tributaries: Ingul River, Ingulets River, and Saxagan River (tributary of the Ingulets River) (Polishchuk 1978).All these streams were situated on locations of former large brackishwater resevoirs or coastal bays that are established on paleontological data (Polishchuk 1978).The zebra mussel is a dominant species in estuaries of these rivers, which form an estuarine complex -the Dniepr-Bug Liman.
On the Northern Azov Sea Coast it was noted in the Molochnaya River (Lubyanov 1954) and in the mouth of the Kalmius River (Mordukhay-Boltovskoy 1960).At present, this mollusc is absent in the last river; this absence is probably connected with the construction of a giant industrial complex in this place.
The zebra mussel was widespread in the estuarine system of the Don River, including the brackishwater Taganrog Bay of the Azov Sea, Mius Liman, Yejsk Liman, and the Don Delta; along the Don River its native range spread upstream to Voronezh City (Mordukhay-Boltovskoy 1960).It also was recorded from the Manych River (tributary of the Don River) and in large reservoirs of the Don and the Manych (Ust-Manych, Proletarskoye reservoir, and Tsimlyansk reservoirs) (Zhulidov et al. 2004).
In the nineteenth century the zebra mussel was recorded in the Severskij Donets River (tributary of the Don River) (Krynicki 1837).Later this species was not recorded in this river until construction of the Dniepr-Donbass Channel.Probably it was occasionally acclimatization.
In the Eastern Don River, the zebra mussel lives in the Kuban River from its mouth to Krasnodar City (Rosen 1911) and in the estuarine reservoirs: Ahtanizovskij Liman (Puzanov 1929) and Dolgij Liman (Povazhnyj and Semin 2005).
These basins in the Black Sea Region are the most eastern native locations of dreissenids' population.According to Mordukhay-Boltovskoy (1960) dreissenids have not been found in the relic lakes of the Caucasian Region (Abrau and Paleostomi) where other Ponto-Caspian species are known.Now the zebra mussel is a major species in Lake Abrau (M.V. Nabozhenko, personal communication).
In the time of acclimatization of aquatic invertebrates into Georgian reservoirs (Hramskoje and Tkibulskoje) the zebra mussel was introduced there (Sergeyeva 1968) but has not since been recorded.
During the twentieth century, range expansion for the zebra mussel was described in a number of channels and reservoirs, associated with the Lower Dniepr Basin (Kahovka Meliorative System, Ingulets Channel, North Crimean Channel, etc).This spread took place only within artificial systems and has not impacted on natural ecosystems.Penetration of this species to new Ponto-Caspian Rivers began at the end of the twentieth century (Figure 5).

Expansion in the Danube-Dniestr Meliorative system
In the 1960s the creation of a common meliorative system was planned between the Danube and Dniepr.The building of the Danube-Dniestr Meliorative system was planned as the first stage of its creation.The marine gulf -Sasyk Lake (in this project -a reservoir in the Danube-Dniestr Meliorative system) was desalinated by separating it from the Black Sea and by building the Danube-Sasyk Channel, which connected Lake Sasyk and the Danube River.This remedial plan included a large lagoonal complex Tuzly Limans between the Danube and Dniestr basins.
In 1981 the project began, but irrigation by mineralized water made a catastrophic impact on local soils and the project was disrupted.
As result of the desalination of Lake Sasyk and its connection with the Danube many freshwater species invaded this reservoir.D. polymorpha polymorpha is widespread in this reservoir and found along all its length (more than 30 km).
Both the zebra mussel and other Ponto-Caspian bivalves have a very specific impact on the ecosystem of Lake Sasyk: their empty shells make enormous deposites which have caused shallowing and transformation of a southwestern part of this reservoir into a swamp.
The next penetration of Danubian species was through Lake Sasyk into the higher part of the Danube-Dniestr Meliorative system (channels and transformed Rivers Kogilnik and Sarata) is this is complex, because introduced species in Lake Sasyk include mainly species with high sensivity to hypoxia.This interferes with their penetration to the above-mentioned streams which have a variation in oxygen concentration.

Expansion in the Lower Dniestr Meliorative System
The Baraboj River was connected by channels with the Dniestr River to the Lower Dniestr Meliorative System in the second half of the twentieth century.During this time the upper part of the Baraboj River was turned into the Baraboj Reservoir.This reservoir has two applications: as part of a meliorative system and as a cooler of a planned power plant.Before this building, the Baraboj River was temporarily dry and many species, occurring in large rivers, would not live in this river.
The population of zebra mussels there was formed as a result of water transferring from the Odessa Channel (water-mine with pumping station on the Dniestr River near Belyajevka City) to the Baraboj Reservoir and Baraboj River.Now this species is found in the Baraboj Reservoir and in a little pond in the river mouth.

Invasion to the Sukhoy Liman Basin
A population of D. polymorpha polymorpha was recorded in the Sukhoy Liman Basin in July 2006 in a small rapid stream.This stream is the remains of the Gross-Libental River (the middle section) which flowed into the Sukhoy Liman.The connection between the Gross-Libental River and Sukhoy Liman was disrupted by the building of a road.Now the lower part of the river is a small floodplain.The total sampled population consisted of juvenile specimens only (some at pediveliger stage).Adult shells were not found.Molluscs occurred on the stones and on other hard substrates.
In the Black Sea Region, this record is a unique case of dreissenid invasion to a small stream.Upstream of the sampling site, a limnic reservoir feeds water to the stream via pipework and hence the stream flow is artificially sped up.Range expansion in the human-made rheophilic biotopes of small stream was also noted for other species.
In this biotope we also found the exotic mudsnail Potamopyrgus antipodarum (Gray, 1843) and an aquarium snail Physella heterostropha (Say, 1817).Both these species were also found in all small rivers of the Sukhoy Liman Basin (Son, 2007a).In similar biotopes in the Baraboj River we found the rheophilic Viviparus vivparus (Linnaeus, 1758) and the Ponto-Caspian species Euxinipirgula lincta (Milashevitch, 1908), both of which are nonindigenous for this river (Son, 2007a).
To summarise these facts we conclude that this type of biotope is characterized by high invasibility.Similar biotopes probably play an important role in the expansion of rheophilic species into steep droughted rivers.

The native range of the quagga mussel
The question on chronology of the quagga mussel invasion history is extremely confusing.The data published till now on its distribution testifies, that its native range is in a lower stretch of the Southern Bug, whence it has been described, and its expansion in the Dniepr and moving on the cascade of reservoirs date from the 1930-1940s (Tseeb et al. 1966, Zhuravel 1967).
The designation of its native range as "a lower stretches of the Southern Bug and Dniepr rivers" in some English-written literature was based on a vagueness of the term "Dniepr-Bug Liman".This name is modular for estuaries of the Dniepr and Southern Bug rivers.D. bugensis has been described from the Lower Southern Bug, and the introduction of the concept "Dnepr-Bug Liman" in the twentieth century has resulted in the beginning of a designation of this species locus typicus as Dniepr-Bug Liman and the subsequent transferral to the English-written literature as "lower stretches of the Dniepr River".This is absolutely inadmissible, because the locus typicus of D. bugensis is the estuarine Southern Bug -Bug Liman (expanded river mouth), whereas the estuarine system of the Dniepr River includes two parts -Dniepr Delta -the expanded river mouth and Dniepr Liman (part of Dniepr-Bug Liman) -the freshened sea gulf between the Bug Liman and Dniepr Delta.
For this reason, the occurrence of D. bugensis in the Dniepr Delta may be considered as the beginning of the quagga mussel's expansion into the Dniepr Basin.
However malacological investigations of the Dniepr and Southern Bug basins at the time of the quagga mussel's description were fragmen-tary and the two similar species concerned could not simply be differentiated.
In Lindgolm's article (1908), the first complex malacological investigation in the given region, D. bugensis was not sampled at all in the south of the Russian Empire.
While this author was processing collection of Zoological Institute of Russian Academy of Sciences, D. bugensis was found among them; this was collected by Brauner in the Dniepr Delta (Lake Beloje, surrounding Kherson City).The sample year was absent from the label but Lindgolm (1908) indicated it as 1899 in a publication.Thus, D. bugensis was already present in the Lower Dniepr practically at the same time, when it had been described from the Southern Bug.This raises doubts as to whether this species is alien to the Dniepr Basin.
References on recent native localities of the quagga mussel in the Ingulets River are consistent with ambiguity in reporting by Polishchuk for the Soviet malacological meeting.This was reprinted by Malacological Review (Polishchuk 1978).In the original text it states clearly that D. bugensis was recorded in geological sediments of the Ingulets River.

The quagga mussel invasion within the Ponto-Caspian region
The quagga mussel has grasped, within Ponto-Caspian region, some large river basins and has expanded its distribution to the Dnepr Basin.
In the Dniepr Basin, the quagga mussel is widespread in the Dniepr Cascade of Reservoirs which occupy almost all the Ukrainian part of the Dniepr River and the associated artificial systems of hydrotechnical buildings (Kahovka Meliorative System, Ingulets Channel, North Crymean Channel, etc).
In the Don River Basin (first record in the 1980) it occurs in the Lower and Middle Don River, Manych River and large reservoirs of the Don and Manych (Ust-Manych, Proletarskoye reservoir, and Tsimlyansk reservoirs) (Zhulidov et al. 2004(Zhulidov et al. , 2005)).
In the Volga River Basin (first record -1981) it occurs in the Volga River (including Volga Delta) and Volga Cascade of Reservoirs (Orlova et al. 2004, Zhulidov et al. 2005).
The quagga mussel also penetrates to freshened zones of the Azov and Caspian seas.In the Northern Caspian Sea it was recorded as recently as 1994-1997 (Orlova et al. 2004).In the Azov Sea it lives in the Taganrog Bay -a brackishwater part of sea which is an estuary of the Don River (see Annex).
More recently, the quagga mussel invasion has expanded in the western Ponto-Caspian rivers: Dniestr and Danube.
Invasion in the Danube River was recorded during recent years and is known from some local findings in the Lower (except delta) and Middle Danube (Micu andTelembici 2004, Popa andPopa 2006).
A very intensive expansion of the quagga mussel has taken place in the Dniestr Basin.The first record of D. bugensis in the Dniestr Basin was the invasion of the Dniestr Reservoir (Middle Dniestr) in 1992-1993 (Kharchenko, 1995).Now it occupies a number of habitats in the Dniestr River and Dniestr estuarine system.The quagga mussel has been recorded in the main channel of the Middle and Lower Dniestr River, branches of the Dniestr Delta, the northern part of the Dniestr Liman and streams entering to the Dniestr Liman (see Annex).Unique specimens of quagga mussel were recorded in the estuarine reservoir -Kuchurgan Liman (Filipenko and Lejderman 2006).

Biotopical distribution of dreissenids in the Azov-Black Sea Region, ecological barriers and vectors of invasions
Both species of dreissenids occur in the Black Sea region in various habitats, where hypoxia is absent (see Table 1).We also noted an interesting way of supporting dreissenids' populations in the shallows along coasts of the Dniestr Liman, where hypoxia, periodically takes place.Number of dreissenids accumulate in the streams, which enter the estuary, and in the shallows near the streams' mouths (Figure 6).Until 2007 we found only zebra mussel in these habitats, but in 2007 massive populations of the quagga mussel were located in the four streams along the southern coast of the Dniestr Liman.
Table 1 shows the significant extension of the quagga mussel's biotopical distribution in the range of invasion.Characteristically, the biotopical distribution of both dreissenids in the range of invasion is very similar, whereas in the native range D. polymorpha polymorpha occurred in more kinds of habitats than D. bugensis.
The widespread invasion of the dreissenids is caused by a diversity of successful vectors.
Dreissenids can use different modes of spread in different stages of their life cycle as they have  During these different stages dreissenids use different modes of invasion.Downstream drift is possible for planktonic larvae by current and for other life stages on aquatic plants drifting downstream (Sullivan et al. 2003, Son 2007a).Drift is a very rapid way of spread and it helps dreissenids penetrate through stretches which have unfavorable conditions.This vector of spread is not available to another highly invasive exotic bivalve genus, Corbicula.Corbicula fluminea (Müller, 1774) and Corbicula fluminalis (Müller, 1774), which at the end of the twentieth century had invaded the Lower Danube and were widespread through most of the Danube Delta branches, but similar to dreissenids (both genera have marine origin) had avoided colonizing stretches with variations in oxygen regime.Both species of Corbicula recorded in Europe lack a free-living larval stage and have not penetrated into Lake Sasyk, which is connected with various branches of the Danube Delta (Voloshkevitch andSon 2002, Son 2007b).Contrary to this, it appears that the zebra mussel has successfully overcome this barrier by larval drift.
Spread by shipping is typical for planktonic larvae via ballast water and also by biofouling by the adult stage on the hull.Water movement (flow and wave action) and animal vectors are also important for spread of pediveger and juvenile molluscs.Use of animal vectors is also notable in adult dreissenids; including birds, aquatic insects, amphipods, crayfish, and, probably some other animals (Mordukhay-Boltovskoy 1960, Dedyu 1963, McCauley and Wehrly 2007).
What kinds of ecological barriers have limited dreissenids' spread within native range?
It is obvious, that the native range of the zebra mussel and quagga is less than the basic ecological limiting factors would allow.
The last two factors prevent occurrence in some habitats, but do not limit distribution of dreissenids along river networks of the Ponto-Caspian Region (excluding drying rivers and salt lakes).However in the Ponto-Caspian Region salinity and high velocity in streams do not usually limit dreissenids' spread in situ.
The distribution of dreissenids within their native range is limited by the presence of all habitat requirements, necessary to form stable populations.
Such as many marine species with planktonic larvae, dreissenids can form a compound structure of metapopulations.The concept of metapopulation (where integral genetic system without free interbreeding but is not mixed on isolated populations) are discussed in detail in the issues of the "Helgoland marine research" (volume 56, number 4), which defined the metapopulation concept.In the Ponto-Caspian Region we observe some variants of spatial structure of the dreissenids' occurrence.
Three main genetic variants are showed in Figure 7. First variant (A) is known in the Ponto-Caspian Region from the Caspian Sea, Taganrog Bay, and from a lot of estuaries in the native and invasive ranges of the zebra mussel and quagga mussel.In these cases we observe the "classic population".
Even in the desalinated parts of the sea (such as the shallows of Kurilskije in the Black Sea) dreissenids don't form a metapopulation, because transfer by sea currents along coast, not only brings larvae to other freshened localites in the sea, but also passes through marine habitats which are characterized by high salinity.
A good example of the variant B occurs in the Volga and Dniepr cascades of reservoirs by both dreissenids (invasive ranges) or in the Lower Danube by D. polymorpha polymorpha (native range).In the cascades of reservoirs the dreissenids form an integral genetic system (metapopulation) with asymmetric genetic drift caused by drift of larval drift downstream.A similar situation was observed in the Ukrainian stretch of the Danube, where the river is connected by small channels with a series of separate estuarine lakes, which are a "donor fund" of the dreissenids for the main river channel.
Variant C was found in the first investigation of the Dniestr Liman.In some streams entering into this estuary the zebra mussel was record above sea level.In this case we suggest transfer by amphipods.A similar stream habitat for the zebra mussel was observed on the Uglich Reservoir (Volga River).Meanwhile we have not recorded this type of habitat for the quagga mussel.
Annex.Records of dreissenids in their range of invasion.

Figure 7 .
Figure 7. Different variants of spatial structure of the dreissenids' occurring: A -isolated lentic reservoirs, estuaries, freshened parts of seas; B -reservoirs and channel downstream; C -reservoirs and small streams upstream.

Table 1 .
Biotopical distribution of the zebra mussel and quagga mussel in their native and invasive range within Ponto-Caspian Region.