Trends of aquatic alien species invasions in Ukraine

This review is a first attempt to summarize data on the records and distribution of 240 alien species in fresh water, brackish water and marine water areas of Ukraine, from unicellular algae up to fish. A checklist of alien species with their taxonomy, synonymy and with a complete bibliography of their first records is presented. Analysis of the main trends of alien species introduction, present ecological status, origin and pathways is considered.


Introduction
The range of organisms of different taxonomic groups varies with time, which can be attributed to general processes of phylogenesis, to changes in the contours of land and sea, forest and deserts, to elevation and isolation of mountains, to changes in water bodies and water flows.These historical activities may be enhanced or slackened under global climate changes.Continental drift, the elevation and lowering of large areas of the Earth, the origin and transformation of oceans, inner lake-seas have led to the formation on the Earth, in the Paleocene and Neocene periods of isolated water bodies with distinct flora and fauna.As a result of active geological processes and global climate changes (especially in the glacial age) a natural shift and transformation of fauna occurred.However, with the origin of man and with the progress of civilization including extensive travel, the introduction of plants and animals to new areas increased over the ages.
From the beginning of the 19th century, due to rising technical progress, the influence of man on nature has increased in geometrical progression, gradually becoming comparable in dimensions to climate impact.
In the past, even when aquatic 'stepping stones' existed across continents, very often negative environmental factors created natural obstacles hindering the spread of different species of aquatic bacteria, fungi, plants and animals.For example water salinity serves as a barrier impeding the entry of hydrobionts from the Mediterranean to the Black Sea and Sea of Azov.However, aquatic habitats with salinities of 5-26‰ similar to the Black Sea and therefore suitable for brackish organisms are widely distributed on the Earth (Vinogradov 1986).Thus as these areas are geographically isolated, spread by man can lead to successful colonization of new comers.So the Black Sea has high risk in naturalization of exotic species in comparison with other areas of world ocean.
Once the natural obstacle can be overcome, species can spread over a new territory and expand its range.Often this occurs with the help of intentional or accidental human introductions.As an example of accidental introduction (simultaneously with intentional introduction of valuable species) data can be obtained that of the 36 species brought to the Black Sea from the USA, only 4-6 have been applied in fisheries and in angling and 10 for aquarium fishes.The rest, which penetrated into natural water bodies, are to some degree dangerous for aboriginal fauna (Zaitsev and Ozturk, 2001).The most common way of accidental introduction of new species is via ocean-going ships that transfer organisms through natural barriers.According to the International Marine Organisation (IMO) 80% of world cargoes are transported by shipping.Annually, about 85 000 ships carry 3-10 billion tons of ballast water in which more than 3,000 species of algae, invertebrates and fish have been recorded (IMO Bulletin 1998).
The dispersal of species is accompanied by a simultaneous decrease in native species diversity in the entire biosphere and in separate locations unifying the genetic fund of the planet.The successful invasive species inevitably leads to heavy competition squeezing out weaker often native species, resulting in a decline of biological diversity (Convention on Biological Diversity: June 5, 1992, Rio de Janeiro, Brasil).
The Black Sea -as a brackish water basin, semi-isolated from the Mediterranean Sea has been closely studied for biological invasions.Not only has a high biodiversity of alien species been established -more than 140 -but also their substantial impact on the marine ecosystem (Gomoiu et al. 2002;Alexandrov 2004) is evident.The invasion of the comb jelly Mnemiopsis leidyi Agassiz, 1865 was characterized as an ecological disaster (GESAMP 1997).The risk of entry of alien organisms into the Black Sea has been promoted by the dredging of shipping channels.These include the Danube-Main-Rhine Canal, connecting the Black and North Seas in 1836, and the Volga-Don Canal connecting it with the Caspian Sea in 1952.
An important factor simplifying the naturalization of alien species in the Black Sea is the instability of its ecosystem.Wide scale eutrophication, observed first in the northwestern sea in the early 1970s, spread almost all over the coastal shelf especially close to river estuaries and large cities.These changes in the trophic status of the sea led to a decline in biological diversity (losses of immunity due to a reduction in the number of predators) the freeing of ecological niches and their occupation by highly productive alien species (Alexandrov and Zaitsev 1998).
Of all the lacustrine states in the Black Sea basin, Ukraine, due to its physical-geographic position and economic development, has all the conditions necessary for becoming the main testing area for control the introduction of aquatic alien species.
The aim of this paper is to illustrate, with the help of data from the literature, the chronology of biological invasions of freshwater, brackish and marine species in Ukraine ranging from unicellular algae to fish, with synonyms included.

Methodology
All species of aliens can be divided into two groups: 1) Distant aliens -species which never previously inhabited the Black Sea-Azov basin, In other words these have a different origin, and were introduced into the water bodies of Ukraine unintentionally or intentionally with human help.2) Neighbouring aliens -inhabitants of the Black Sea -Azov basin, or adjacent areas expanding by chance within Ukranian waters or with spread accelerated by human activities (this is mostly freshwater species).
Alien species have subsequently been grouped into four categories namely casual, invasive, established and cryptogenic (questionable).
 Casual: In this paper alien is used in the sense of CIESM: Alien species are identified as having been recorded only once (no more than twice for fishes) in the scientific literature: they are presumed to be not established in a river basin.http://www.ciesm.org/online/atlas/index.htm  Invasive: These are the introduced species that, having overcome biotic and abiotic barriers, can propagate away from their area of initial introduction through the production of fertile offspring without any reference to impact (Richardson et al. 2000).In many definitions the term invasive is also considered as established species which are agents of change and threaten native biological diversity (IUCN 2002) or as species that threaten the diversity or abundance of native species, the ecological stability of infested ecosystems, economic activities dependent on these ecosystems and/or human health (EPA 2001).It is in this last meaning that the term IAS (Invasive Alien Species is used here). Established (synonym: naturalized): These include an introduced or feral population of a species.Species established in the wild with free-living, self-maintaining and selfperpetuating populations unsupported by and independent of humans (European Commission 2004). Cryptogenic species are species with no definite evidence of their native or introduced status according to Carlton (1996).Species whose probable introduction has occurred prior to 1800, i.e. has not been witnessed, have also been included in our compiled list.Often these species are excluded from lists of aliens or included among the established ones.In this review we considered it best to separate them.

Physical and Geographical Features
Among the Black Sea countries Ukraine has the longest shoreline -4,431 km making up 36.7% of the total (Shujskiy 1989).Ukraine has the greatest shelf area as opposed to its territorial waters (to 200m isobaths), equal to 55,750 km 2 or 57% of the total Black Sea shelf (Zaitsev 1992).
The dense indentations of the shore line and the high number of water body types (lagoons, bays, embayments, limans, lakes) provide various habitats for aquatic organisms.These aquatic habitats are of varying salinity (0.2-300 ‰), depth (0.8-36.0 m), substrate and vegetation (Zaitsev and Alexandrov 1998).Ukraine has 17 large limans with a total area of 1952 km 2 , 8 bays -1770 km 2 , 19 coastal wetlands -6350 km 2 (Conservation.2003).A liman is the former mouth of a river now covered with sea water.This definition is very close to a estuary, but as a tide-less sea, the Black Sea does not have estuaries.
The largest rivers of the Black Sea (Danube, Dnieper, Dniester) make up more than 50% of the total river runoff into the Black Sea (Nikolaenko and Reshetnikov 1991), and their catchments create a zone of maximum biological productivity in most of the shelf of Ukraine.In total, Ukraine has about 73,000 rivers.The highest number are present in the western mountainous area including the Dniester and Danube basins.The density of the river network there is 1-1.5 km/km 2 .In the Crimea, rivers are relatively rare, with many areas lacking natural water flow.The density of the Crimean river networks is 0.22 km/km 2 .
The continental waters of the Ukraine pertain to two of the largest zoogeographical areas, i.e.Palearctic and Ponto-Caspian brackish areas (Starobogatov 1970).The Palearctic includes North Eurasia and Northwest Africa.Within the boundaries of Ukraine, there are two zoogeographic provinces: the Baltic and Danube-Don.The former includes the rivers of the Visla basin and Shatskie lakes.The Ponto-Caspian area includes the Caspian Sea, limans and the lower reaches of the rivers of the Black and Azov Seas.According to some data a number of relict lakes in Macedonia, Greece, Italy, Iran, Iraq, Central and Western Turkey, i.e.Eastern Mediterranean coast and Asia Minor (Wilke et al. 2007) should be included.
The Crimean peninsula could be included in the Ponto-Caspian area.Up until the 20th century it lacked the relict Ponto-Caspian fauna as zoogeographically it is not a peninsula, but an island and its isolation from the lower basins of the Dnieper and Don occurred before the introduction of Ponto-Caspian fauna.The Crimea can actually be considered to be a faunal isolate of the European-Siberian subarea of Palearctic.However, the Crimean hydrofauna contains a number of Asian elements.The Crimea itself was never considered in large zoogeographical classifications (Figure 1).

Results and Discussion
On the base of collected information 169 species of distant aliens and 71 neighbouring aliens have been registered in aquatic areas of the Ukraine (Annex).Check-list of aquatic alien species of Ukraine have been compiled according to available data published before May 2007.For this reason some recent data are not included in the results of our investigations.For example,

Analysis of distant species registration
In relation to salinity many of the encountered species are brackish organisms encountered both in the sea and in freshwater bodies.However, 59% of the registered species were attributed to the coastal ecosystem of the Black and Azov seas, 29% to brackish and 16% to freshwater areas.Most of the distant alien species (23 species of fish) were registered in the period from the beginning of 1950 to 1975 due to wide scale introduction of valuable varieties of fish in the water bodies of Ukraine and neighboring countries (Russian, Moldova, Belarus).Of the number of aliens observed in that period, 44% relate to introductions.However, of the above mentioned 23 fish species brought to Ukraine, only 4 species became naturalized.These were able to reproduce in new conditions without the help of man.These species include spotted silver carp A. nobilis, silver carp H. molitrix and grass carp C. idella among the freshwater hydrobionts and haarder L. haematocheila in the marine species (see Annex).
The process of successful introduction is linked with a number of biological, physical and chemical factors which at present cannot be accurately forecasted.Of the total number of registered species of distant aliens, only 30% (or 50 species) were naturalized, and today are part of the food web of Ukranian aquatic ecosystems able to support their populations.Almost half of   the species (41% or 69 species) were discovered no more than twice and in small amounts, and that is why they are placed in the casual category (Figure 2).
In total, most of the registered number recorded in Ukranian water bodies are distant aliens (Figure 3), with the majority of the species being either planktonic or fouling organisms (Figure 4).
This confirms the key role of shipping in transferring aliens.Usually, benthic animals entered Ukranian water bodies as result of ships' hull fouling.The maximum number of recorded aliens occurred before the early 1970s (Figure 5).It is possible to explain the subsequent decline due to the widespread introduction of hull antifouling coatings.For example, in the 1970s, the overwhelming majority of ships' hulls were coated with tributyltin (TBT), which protected the hulls from fouling for 18 to 24 months.Since then the number of cases of recorded planktonic organisms invasions has risen, due to ballast water exchange in tanker fleets (see Figure 5).The total tonnage of tankers in the 1980s made up 42% of the world total and determined their priority in cargo turnover (Marine encyclopedic reference.1986).
Since 1973, subsequent to the adoption of MARPOL -73/78, a measure to prevent pollution from ships, conditions for survival of hydrobionts in ballast tanks were much better due to isolation from oil products.This was another reason why the probability of transferring planktonic hydrobionts to new ecosystems has increased.
When characterizing the long-term dynamics of alien introduction records into Ukranian water bodies, two maxima have been noted (Figure 6).
One of them, in the 1960-1970s, is connected with the introduction of fish in freshwater bodies and also with the establishment of new marine ports, increasing the risk of the introduction of aliens into the Black Sea.The second maximum has been recorded since the beginning of the new millenium and can be explained by two factors.On one hand, it can be explained by a large increase in ballast water transportation especially by the oil tanker fleet.On the other hand, there also has been a rise in scientific interest into the problems of biological pollution in the world's oceans resulting in a more comprehensive study of its biological structure.This can be illustrated by the increasing number of publications in the electronic abstract version of ASFA.In the past  decade the number of publications on alien species and invasion has increased by 6-7 times (Figure 7).
Due to more intense biological studies in Ukraine the list of alien species was extended adding marine fungi -7 species, infusorians -6, parasites -3 and unarmored Dynophyta -11 species (see Annex).Due to the study of new previously un-studied systematic groups, 3% (or 5 species) of the aliens discovered were placed in the category "Cryptogenic" (see Figure 2) The greatest numbers of distant species of freshwater hydrobionts were introduced and dispersed in the Ponto-Caspian basins.A small part moved up the Dnieper to the mid Dnieper -Danube province.Another fraction was introduced into northwestern Ukraine (Baltic province) and the Crimea.The Annex illustrates some species introduced into the upper Dnieper cascade from North Europe.These species are characteristic of the Baltic province.If the Ukrainian water bodies of the Baltic basin were closely studied, they would have most likely have been found there.Probably, these species entered the Dnieper basin through a system of channels connecting it with the Baltic.In this case, if borders are not taken into consideration, then the introduction is similar to that in Annex 2 (nearby aliens).
Separate attention is necessary to focus on aquarium species.Subsequent introductions to waterbodies may occur unintentionally when emptying aquariums.One of the famous examples is killer algae Caulerpa taxifolia (M.Vahl) C. Agardh, 1817 that penetrated into Mediterranean coastal ecosystems from the aquarium of Monaco Oceanographic Institute.
Most of the cultivated species in aquaria are of tropical or subtropical origin.As a rule, they survive in natural conditions of the area under study, being sensitive to lower temperatures.However, in the warm season they are encountered close to populated areas.Examples are aquarium fish like guppies and platies encountered episodically in the Dnieper Basin (Novitskij 2005), and piranha discovered in the summer, 2006, in Lake Kasyanka (Dnieper Basin) near Dnepropetrovsk.At present this invasion is being studied by specialists from Dnepropetrovsk National University (R. Novitskij, personal communication).
It is evident that most of the aquarium species of the populations formed in open water bodies are functional species (bloodfluke planorb B. glabrata, pewter physa Ph. heterostropha) and not cultivated decorative species which clean the aquarium of "aquarium weeds" entering from

Analysis of neighbouring alien records
The main feature of neighbouring species, which differentiate them from distant species is the high percentage of naturalized species present -90% (Figure 8), and also the fact that most of the species records (68%) pertain to benthic organisms (Figure 9).The chronology of introducing species shows that their penetration into the water bodies of the Ukraine was linked with the wide scale melioration in 1950s, due to the withdrawal of runoff from the largest rivers of the Black Sea basins for agriculture purposes.
The subsequent introduction of hydrobionts in the late 1950s was not comparable in scale with the previous one (Figure 10).The dominant neighbouring species originated as Ponto-Caspian relicts, which due to the artificial integration of river systems have widespread in the Black -Azov sea basin (Figure 11).
When considering neighbouring aliens, cases of species introduction from adjacent biogeographically areas, such as the Ponto-Caspian into the European -Siberian area through the Dnieper reservoir cascade and inner waters of Crimea, should be of first priority.It is quite clear that first of all many freshwater, brackish Ponto-Caspian relicts were introduced, which were lacking previously from the European -Siberian sub-area.Hydrobionts were able to overcome the zoogeographical border along the Dneiper river bed after the removal of the barrier between Dnipropetrovsk and Zaporozhie following construction of a dam in Kichkas and after activating river shipping, dredging channels, setting up a reservoirs and after intentional introductions.This led to further distribution in the European-Siberian sub area: mid Dnieper (from it to the Don, then into the Volga) and upper Dnieper (from it the Baltic basin, then to West Europe and Britain).
It is known that separate species of hydrobionts with local areas in Europe as the cladocerans Cercopagis pengoi (Ostroumov, 1891), Limno-cletodes behning (Borutzky, 1926), Para-leptastacus spinicaudata (T.Scott et A. Scott, 1895), and the amphipods Rivulogammarus kischineffensis (Schell.),Synurella ambulans (Müller, 1846) (see Annex) appeared in the Dnieper cascade also at the time of introduction of Ponto-Caspian fauna.These species, which have very wide natural habitat, are made up of several interrupted localities.This is characteristic to Ukraine as in the lower Dniester and Danube where there are many separate relict localities of species, the main ranges of which are in South or West Europe.Possibly, these species were introduced into the Dnieper water reservoir simultaneous with the mass introduc-tion of Ponto-Caspian species as food resource for fish.
Besides being spread along the Dnieper, they penetrated to the Crimea.After the opening of the North-Crimean canal and as a result of introduction of food invertebrates in some water reservoirs in the peninsula, some species with a wide range of dispersal as crustaceans Daphnia cucullata Sars, 1862, Leptodora kindtii Focke, 1844, Mesocyclops leucarti Claus, 1857 and molluscs: river snail Viviparus viviparus Linnaeus, 1758; European fingernailclam Sphaerium corneum Linnaeus, 1758, S. rivicola Lamarck, 1818 were able to enter with representatives of the Ponto-Caspian fauna.Despite this there are some species, with a main range located in the European-Siberian sub area, which also entered the Crimea as Ponto-Caspian fauna, at the southern border of their distribution.The situation differs for three molluscs species Fagotia danubialis Bourguignat, 1884; gravel snail Lithoglyphus naticoides Pfeiffer, 1828 and freshwater nerite Th. fluviatilis.Their dispersal was first noted only in the Crimea but they, together with other species similar to the representatives of Ponto-Caspian fauna, have actively spread in Europe (see Annex).Often they are confused with Ponto-Caspian as most of the areas (lower Dnieper, South Bug, Dniester and Danube) coincide.However, in contrast to representatives of the Ponto-Caspian fauna, they have not been formed in the Sea of the Sarmat, but in rivers and are absolutely freshwater in nature.L. natcoides inhabits an isolated part of the area in the Baltic, while F. danubialis is found in the eastern tributaries of Pripyat.As for Th.fluviatilis, it pertains to a special zoogeographical group of the most ancient representatives of Ponto-Caspian fauna.It was formed like the zebra mussel D. polymorpha in the Eastern Mediterranean basins, but then migrated to the northwestern Black Sea from which many new species emerged -classical Ponto-Caspian.In origin it is like the zebra mussel as it is traditionally classified as a Ponto-Caspian species.However, in Annex this species is noted as European as in the summary table, its affinity as a species is not related to the zoogeographical group, but to its natural range.
The classification of the molluscs in the European species category is attributed to the time of paleoinvasion Th. fluviatilis has kept to its localities in the Baltic, as well as in Spain.At present, it is actively spreading in Europe.In the Ukraine it has been inhabiting limans and rivers (in contrast to classical representatives of the Ponto-Caspian fauna it is native in upper stretches of the large rivers) and also in several marine bays (Odessa, Egorlitsky, Tendrovsky) earlier forming the avandelta of the Dnieper (Son 2005).However, the marine part of its range does not border with the Chernaya River estuary.Evidently, it has been introduced to the Crimea like other species during faunal introductions from the lower Dnieper to mountainous water reservoirs.

Economic prerequisites in biological invasions
The presence of an indented coastline, deep water bays and limans promoted the establishment of a maximum amount of sea ports following intensive agricultural and industrial development in the Ukraine (see Figure 1), the largest of which are Odessa, Yuzhny, Ilyichovsk.In 2004 their annual turnover was more than a half of the sum total of 19 marine ports of Ukraine and amount to >60 mln.t (M t).By the way it is necessary to stress on the fact that main volum of shipping transportation in the Black Sea comes through Ukraine.For example at the same period ( 2004) cargo traffic of two main ports of Russian Federation (Novorossisk and Tuapse) was 89.8 M t, largest Black Sea ports in Constanza (Romania) -50.43 M t, in Georgian ports (Poti, Supsa and Batumi) -20.55 M t, in Bulgarian ports (Varna and Burgas) -13.35 M t.Black Sea ports of Turkey (Istanbul, Darince, Zonguldag and Samsun) develop very quickly (Tokman 2005).
In the past 5 years (2001)(2002)(2003)(2004)(2005)(2006) the total turnover of Ukrainian ports has increased 1.6 fold.Simultaneously, the volume of ballast water exchange increased; this is determined by the numbers of export-import operations.For example, in the port of Odessa in 2001, it increased 17% in comparison to the previous period, while in the port of Ilyichovsk it dropped by 54%.It has been estimated that in 2001 alone, more than 11 M t of ballast waters were discharged in ten of the largest ports of Ukraine (Savusin 2002).
Another pathway for the introduction of alien species are the estuarine ports Ust-Dunaisk (near the Danube), Belgorod-Dnestrovsk (near the Dniester), the ports of Nikolaev and Kherson (near the Dneipro-Bug Liman).Although their cargo turnover is less than those mentioned previously, there is a greater risk of transferring alien species from a more dense marine environment to a less dense freshwater when ballast waters are discharged.This is evident in the high number of acclimatised species discovered in the Danube delta (Alexandrov 2004).It should be noted that most of the above mentioned ports, e.g.Ust-Dunaisk, Belgorod-Dnestrovskiy, Ilyichovsk and Yuzhny have been established in the past 50 years during the period 1958-1980.This should be taken into conside-ration when analyzing the chronology of invasions.
The Northern Crimean canal has become a powerful man-made source of biological invasions for the freshwater water hydrobionts of the Crimea.
The first Dneiper water came to the Crimean Peninsula in 1963.Having filled up 8 water reservoirs it is supplied to the cities of Kerch, Feodosiya, Simferopol and Sevastopol with maximum consumption of 300 m 3 /sec.The source of many biological invasions is the intentional introduction by man of valuable fish species for consumption.In addition to spreading naturalized fish e.g.haarder Liza haematocheila Temmnick and Schlegel, 1845 (=Mugil soiuy Basil and Europeski, 1855) and silver carp Hypophthalmichthys molitrix Valenciennes, 1844 which took place in the Black Sea basin, it allowed the simultaneous entry of other undesirable organisms.For example, some parasites, free-living algae, invertebrates and even fish as stone moroko Pseudorasbora parva Temminck and Schlegel, 1846 penetrated into the Black Sea.Fish introductions were carried out mostly in freshwater bodies.The existing network of rivers and streams in Ukraine is closely tied with those in the neighboring Moldova Republic and the Russian Federation, which should be taken into considerations in terms of fish breeding.During the Russian Empire, work for the introduction of species was conducted 150 years ago under the guidance of the Russian Society for Acclimatization founded in 1857.Before the disintegration of the USSR almost 250 introductions of 35 fish and 13 invertebrate species were performed annually.Before 2000 almost 100 introductions of 16 fish and 2 invertebrate species have been carried out in Russia (Stroganov and Zadoenko 2000).As an example, the river nerite Theodoxus fluviatilis Linnaeus, 1758, belongs to a special zoogeographical group of the most ancient Ponto-Caspian fauna representatives.Similar to zebra mussel Dreissena polymorpha Pallas, 1771 they evolved in the basins of the Eastern Mediterranean, but migrated to the Ponto-Caspian area producing many new classical Ponto-Caspian species (Gelembiuk et al. 2006).Introductions of fish from the Russian Federation were also carried out.In Moldova, the introduction of fish was carried out in three stages.In the first stage in [1950][1951][1952][1953][1954][1955][1956][1957][1958][1959][1960][1961]

Figure 1 .
Figure 1.Ukrainian part of the Black Sea.

Figure 6 .
Figure 6.Long-term changes in distant alien species introduction .

Figure 10 .
Figure 10.Long-term changes of neighbouring alien species introduction into Ukrainian aquatic ecosystems.