Diversity and Distribution of Freshwater Gobies from

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2.6 Diversity and Distribution of Freshwater Gobies from the Mediterranean, the Black and Caspian Seas

Jörg Freyhof

INTRODUCTION Data on freshwater gobies from the Mediterranean, the Black and Caspian Seas have been summarized recently by Kottelat and Freyhof (2007). There are also detailed species accounts available in the books edited by Miller (2003) and Miller (2004). These books comprise some original views and much past data especially from relatively inaccessible eastern European and Russian sources, not only systematic and distributional but much general biology. Western and northern European freshwaters are rarely colonized by gobies and only one euryhaline species, Pomatoschistus microps, is widely known also from the North, Baltic and Atlantic Sea basins as well as from some areas in the western Mediterranean Sea. On the contrary, freshwater Author’s address: Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, 12587 Berlin, Germany. E-mail: [email protected]

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The Biology of Gobies

gobies are common and often dominant in littoral habitats even far from the sea in Italy and the Eastern Mediterranean and especially in the basins of the Black and Caspian Seas. In these areas, there are about 50 goby species being restricted to freshwater habitats or regularly enter freshwaters. With two exceptions (Padogobius), these gobies can be grouped within so called sand gobies (Economidichthys, Knipowitschia, Pomatoschistus) and Paratethyan gobies (Babka, Benthophiloides, Benthophilus, Caspiosoma, Mesogobius, Neogobius, Ponticola, Proterorhinus). The monophyly of Paratethyan gobies was recently supported also by molecular evidence (Neilson and Stepien, 2009). Freshwater sand gobies are most diverse in the Adriatic and Aegean Sea basins from northern Italy south to Greece and West Anatolia. In this area, two euryhaline species are commonly found in estuaries and adjacent freshwaters (Knipowitschia panizzae, Pomatoschistus canestrinii). Both are related to a number of local endemics which are characterized by reduced patterns of head canals and squamation. Paratethyan gobies are restricted to the tributaries of the Marmara, Black and Caspian Seas and none of them is ever recorded to permanently inhabit full marine waters. In this ecologically and morphologically diverse group of species, there are several real freshwater endemics (as Ponticola kesslerii) and several species which never enter pure freshwaters but are restricted to the brackish waters of the seas (as Ponticola ratan). Several species are euryhaline and are able to inhabit the sea as well as a wide range of freshwater habitats. Paratethyan gobies are a large radiation of real brackish- and freshwater gobies which has evolved in the today Black and Caspian Seas. They are connected to one of the key events forming the today diversity of Western Palearctic freshwater biota, the palaeographic processes dividing the Tethys into the Mediterranean and Paratethys Seas. While the Mediterranean fell dry during the late Miocene (Messinian), the Paratethys became more and more freshened during this time. During the Pliocene, the Paratethys was divided into the Black-, Azov-, Caspian and Aral Seas. These seas experienced massive water level fluctuations during the Pleistocene when they were disconnected from each others and from the Marmara and Mediterranean Seas during glacial phases, but connected by eight brief phases of high global sea levels corresponding with glacial melting phases and interglacial’s. During the last glacial maximum, Paratethyan seas were fresh or slightly brackish lakes for at least 150,000 years and the sea level was about 150 m lower than today (see Aksu et al., 1999 for overview).

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Several species of Paratethyan gobies are actually expanding their range very fast following the massive habitat alternations and artificial river connections of the 20th century. Two of them were transported by ships from Europe to North America. The exact reasons for and modes of these massive upriver expansions of some Paratethyan gobies are still unknown. There are speculations, that there is partly an active upriver migration in rivers which have been transformed into shipping canals. But obviously, Paratethyan gobies are also able to use ships as vectors as there are several observations, that gobies are recorded suddenly far upriver or from places very distant from the closed distribution area. Recent examples are the records of Babka gymnotrachelus in the Danube close to Vienna, far upriver from the closed distribution area, Neogobius melanostomus from the lowermost Rhine (van Beek, 2006), which is a major harbour area and these fishes can only have been imported by ships or the first record of N. fluviatilis for the North sea basin from a harbour at the lower Rhine. Such initial introductions usually lead to a very fast downriver colonization of the major river and Paratethyan gobies as some Neogobius, Ponticola or Proterorhinus develop huge populations within one or two years and may spread several hundreds of km downriver in this time.

GOBIOID GENERA IN THE REGION Family Odontobutidae One species is introduced to Eastern Europe and is spreading to the west. Micropercops swinhonis is sometimes reported to have been introduced from East Asia to Eastern Europe, but there is no evidence that it has established somewhere.

Genus Perccottus Dybowski, 1877 The only species of this freshwater genus, P. glenii, is native to the Pacific basin of East Asia from Tugur drainage (Sea of Okhotsk) to northeastern Korea. It is an invasive species in Eastern Europe and Central Asia. It was first introduced in 1916 in St. Petersburg as an ornamental fish. In 1960s, it was also introduced to Kazakhstan, Uzbekistan, Turkmenia and Lake Baikal mixed with Chinese carps. This species is fast spreading and abundant in northern Russia, Belarus, Poland and Ukraine. There are also local records from Danube basin and an invasion of Central and Western Europe is expected. Perccottus glenii spreads actively via navigation canals and introduced with stocked fish.

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Familie Gobiidae Genus Babka Iljin, 1927 Babka is a monophyletic genus including the well known racer goby called Neogobius gymnotrachelus before (see under Neogobius). Babka gymnotrachelus is widespread all over the Marmara, Black and Caspian Sea basins and inhabits mostly freshwater and brackish waters with low salinity (< 2 %). This species belong to the group of invasive gobies and it is expanding its range since the late 1990s, when it invaded the rivers of northern Black Sea basin. In the Middle 1990th, it found its way to the Vistula River in the Baltic Sea basin in Poland, where it arrived from Dniepr via a navigation canal. Babka gymnotrachelus inhabits large rivers as well as medium sized and fast flowing streams.

Genus Benthophiloides Beling and Iljin, 1927 This monotypic genus is endemic to the Azov and Black Seas. Benthophiloides brauneri is very rarely observed and inhabit deep waters of estuaries, coastal lakes and lower part of rivers, at depths up to 15 m, in still, fresh and brackish water. It seems to be closely related to Benthophilus and Caspiosoma.

Benthophilus Eichwald, 1831 There are some 20 species of Benthophilus and the genus was recently revised by Boldyrev and Bogutskaya (2004). Benthophilus are known from the Caspian, Azov and Black Seas. They do not enter fully marine conditions and are therefore absent from the Mediterranean Sea. Some are strictly marine (in littoral zone or in deep waters), others inhabit the estuaries and freshwaters. Two species (B. durrelli, B. nudus) are invasive in the large tributaries of the Caspian and Black Sea. All Benthophilus species inhabit marine habitats, lowland rivers, deltas and coastal lakes. Many species are euryhaline but some are restricted to brackish waters. In rivers, they are usually abundant in main stream. Benthophilus can dig themselves into fine sediments and usually inhabit muddy, silty or sandy bottoms with mollusc shells. They live only about 1 year, spawning in spring inside or under a mollusc shell. Adults die soon after spawning. All species feeds mainly on chironomid larvae, amphipods and molluscs, some are specialized on molluscs. Phylogenetic relationships of Benthophilus and the related genera Benthophiloides and Caspiosoma are still unresolved but Neilson and Stepien

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(2009) suggest, that they are closely related to Neogobius, Ponticola and other Paratethyan gobies. Benthophilus profundorum a deep-water endemic from the Caspian Sea, is sometimes placed in the monotypic genus Anatirostrum but treated as a species of Benthophilus here.

Genus Caspiosoma Iljin, 1927 Caspiosoma caspium is the only species of this genus which is found in the lower reaches, deltas and limans of rivers draining to northern Black Sea, Sea of Azov and Caspian Sea. This small goby which grow to 50 mm SL is poorly known, but locally abundant, especially in marine habitats.

Genus Economidichthys Bianco, Bullock, Miller and Roubal 1987 With a size up to 25 mm SL, E. trichonis, which is endemic to Greek Lakes Trichonis and Lysimachia, is the smallest European freshwater fish species. There are two species in Economidichthys, both endemic to Western Greece. Both share a large peri-anal organ, distinguishing them from superficially similar Knipowitschia. Both are strict freshwater gobies with an extended pelagic phase.

Genus Knipowitschia Iljin, 1927 With 16 actually recognized species, Knipowitschia is one of the large genera of Western Palearctic gobies and all species are found in the Adriatic, Aegean, Black and Caspian Sea basins. Only one species, K. iljini, from the Caspian basin is strictly ‘marine’ inhabiting only the brackish water of that sea. There are additional four euryhaline species and 11 strict freshwater species, often with a very small distribution area in freshwater habitats adjacent to the habitat of an euryhaline species. Such local endemics are usually diagnosed by reduced head canals and/or reduced squamation and some seem to be very closely related to adjacent euryhaline species. While it might be speculated, that some of them are (as K. ephesi, K. milleri, K. radovici, K. montenegrina or K. mrakovcici) the result of allopatric speciation from an euryhaline ancestor identically or very similar to K. panizzae or K. caucasica, this seems to be unlikely for some other freshwater endemics. Due to the often very small distribution ranges, several Knipowitschia are of conservation concern. One species, K. goerneri, was not found again since 1983 in its only known habitat in a spring on Corfu Island (Greece) and a second species, K. cameliae, was not found since 1994 in its only habitat

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in Romania. Both species are for sure extirpated in their known habitats, but it cannot be excluded, that they exist still somewhere else. It can also not be excluded that they have gone extinct. Hyrancogobius, endemic to the Caspian basin is treated here as a synonym of Knipowitschia. Molecular data presented by Penzo et al. (1998) and Huyse et al. (2004) suggest, that at least one of the freshwater endemic species, K. punctatissima, might be related to Pomatoschistus canestrinii and this group is not closely related to Knipowitschia or to Pomatoschistus and might represent an own genus Ninnigobius Whitley, 1951 (see also Miller and Sanda, 2008). More data on the phylogeny of sand gobies are needed to resolve this problem.

Genus Mesogobius Bleeker, 1874 Only two large (up to 345 mm SL) predatory gobies (M. batrachocephalus, M. nonultimus) are actually placed in Mesogobius. The validity of M. nigronotatus from the Caspian Sea is questionable. They are found in inshore habitats, estuaries, brackish- and freshwater lagoons on sand or rock bottom; often very deep in summer (down to 100 m). While M. batrachocephalus, endemic to the Black Sea, locally enter pure freshwater, the Caspian species M. nonultimus is only found in brackish waters. Due to their large size, they have a certain commercial value in some areas and are popular for sport fishers.

Genus Neogobius Iljin, 1927 While Neogobius was long known as an artificial assemblage of Paratheyan gobies, only recently, Neilson and Stepien (2009) presented sufficient data to allow to split the Paratethyan gobies into natural, monophyletic groups which are treated as own genera as suggested by Neilson and Stepien (2009). Only four species remain in Neogobius (N. fluviatilis, N. pallasi, N. caspicus and N. melanostomus). All other species widely known as Neogobius are now placed in Ponticola or Babka. Neogobius is endemic to the Marmara, Black and Caspian Seas. Neogobius caspicus is restricted to the Caspian Sea and seems not to enter tributaries, while all others inhabit the sea as well as various kinds of freshwater bodies. No Neogobius species enter fully marine conditions and the genus is therefore absent from the Mediterranean Sea, but N. fluviatilis and N. melanostomus are known from the Marmara basin. Neogobius fluviatilis and N. melanostomus have reached the North and Baltic Sea basins through artificial waterways. Neogobius melanostomus has entered the Baltic Sea itself and is found to be abundant in the Sea in some areas. Beside the invasion of European rivers, this species is also invasive

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in the Great Lakes area in North America (Charlebois et al., 1997). The invasion of Neogobius into new areas is often well documented. It is usually a very fast process downriver and a slow process upriver. Some species have colonized several hundreds km of large rivers within one or two years. Due to its large size of about 200 mm SL, N. melanostomus has a major commercial value in some areas, especially in the Azov Sea. It is usually salted, dried and consumed with beer.

Genus Padogobius Berg, 1932 There are actually two species in Padogobius, both distributed in Italy. While one of them, P. nigricans, is endemic to Central and Northern Italy, the second species, P. bonelli, is known from northern Italy and adjacent areas in Switzerland, Slovenia and Croatia. P. bonelli is also well known to be invasive in Italy and has massively expanded its range south since the last decades. Both species are pure freshwater inhabitants and known from a wide range of habitats. While all Paratethyan gobies seem to form one monophyletic lineage and all freshwater sand gobies are closely related to only two or three euryhaline species, both Padogobius species are not closely related to these groups. It is speculated, that both have independently originated from marine ancestors (see Penzo et al., 1998) and molecular results by these authors also suggest, that Padogobius might be related to the marine rock goby Gobius paganellus.

Genus Pomatoschistus Gill, 1863 Sand gobies of the genus Pomatoschistus are widespread inhabitants of coastal water in Europe. There are only three species regularly found in freshwater habitats. From these, P. canestrinii, endemic to the Adriatic basin and P. microps, widespread in western and northern Europe are euryhaline inhabitants of coastal waters. While P. canestrinii is able to inhabit freshwaters permanently (see Kovačić, 2005 for details), P. microps seem to be an obligatory catadromous species. There is only one pure freshwater Pomatoschistus in Europe, P. montenegrensis, endemic to Lake Skadar basin in Montenegro and Albania. In fact, the position of both species within this genus is still a matter of discussion (see in Knipowitschia).

Genus Ponticola Iljin, 1927 Recently, Neilson and Stepien (2009) presented a molecular study suggesting, that Ponticola represents a monophyletic lineage within the radiation of

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Paratethyan gobies. Ponticola is endemic to the Black and Caspian Seas and does not enter the Marmara or Mediterranean Seas. From the 13 species recognized, P. ratan, P. platyrostris, P. bathybus and P. cephalargoides are restricted to brackish water habitats and P. eurycephalus and P. syrman are usually found in the sea only, but enter estuaries in some areas. Ponticola kessleri and P. gorlap are invasive in tributaries of the Black and Caspian Seas following the massive river alternations in the 20th century. Ponticola kessleri has reached the North Sea basin through an artificial waterway connecting the Danube with the Rhine. This invasion is welldocumented and within four years, the species colonized all suitable river habitats downstream of the invasion site. In Ponticola, there is a group of strict inhabitants of freshwater streams and rivers and some have a small distribution range as the N. constructor species complex, which include five species (N. constructor, N. cyrius, N. rhodioni, N. rizensis and N. turani), all endemic to small areas at or close to the Caucasus mountains. These species often inhabit cold mountain streams where they occur sympatric with trouts (Salmo).

Genus Proterorhinus Smitt, 1900 Four species of tubenose gobies are distributed in the Black and Caspian Seas and one of them; P. semilunaris, belong to the invasive Paratethyan gobies, which have massively expanded their range since the middle of the 20th century. It has also reached North America, where it is now invasive. One species, P. marmoratus seem to be a pure inhabitant of brackish waters while P. semilunaris and P. tataricus are found in freshwaters only (Stepien and Tumeo, 2006). All tubenoses are relatively small gobies which inhabit densely vegetated habitats or coarse stone fields as usually found on artificial river shores. The diversity of this genus is still not fully resolved and several undescribed species seem to exist.

Conclusion Freshwater gobies from the Mediterranean, the Black and Caspian Seas are species rich and inhabit a diverse range of habitats. With the exception of Padogobius, they belong to two evolutionary lineages only. The first lineage is the large group of Paratethyan gobies, which is basically a freshwater and euryhaline radiation. It has its evolutionary roots in the Paratethys and its adaptation to brackish and freshwaters is likely to be related to the process of isolation of the Paratethys from the Tethys in the Middle Miocene

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(about 13 MY ago) and the subsequent freshening of the Paratethys in the latest Miocene (finally freshened about 6 MY ago) (Popov et al., 2004). The second group are Mediterranean sand gobies which are related to sand gobies in the seas west and north of the Mediterranean. But in fact, sand gobies have their highest diversity in the Mediterranean and there are several endemics in the Black and Caspian Seas also. Therefore, Paratethyan origin of sand gobies with subsequent colonization of the Mediterranean is as speculative as their invasion of this area from the Atlantic. In contrast to Paratethyan gobies, the evolution of freshwater species might have been happened in several independent events in sand-gobies and there is some empirical evidence, that some species are the result of very recent allopatric speciation.

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Penzo, E., G. Gandolfi, L. Bargelloni and L. Colombo. 1998. Messinian salinity crisis and the origin of freshwater lifestyle in western Mediterranean gobies. Molecular Biology and Evolution 15: 1472-1480. Popov, S.V., F. Rögl, A.Y. Rozanov, F.F. Steininger, I.G. Shcherba and M. Kovac. 2004. Lithological-Paleogeographic maps of Paratethys 10 maps Late Eocene to Pliocene. Courier Forschungsinstitut Senckenberg 250: 46 pages, maps 1-10. Stepien, C.A. and M.A. Tumeo. 2006. Invasion genetics of Ponto-Caspian gobies in the Great Lakes: A “cryptic” species, absence of founder effects, and comparative risk analysis. Biological Invasions 8: 61-78. van Beek, G.C.W. 2006. The round goby Neogobius melanostomus first record in the Netherlands. Aquatic Invasions 1: 42-43.