Non-Native Fish Species in Slovak Waters

Biologia 65/6: 1057—1063, 2010 Section Zoology DOI: 10.2478/s11756-010-0114-7

Non-native ﬁsh species in Slovak waters: origins and present status

Ján Koščo1,LenkaKošuthová2 , Peter Košuth2 & Ladislav Pekárik3

1Faculty of Human and Natural Sciences, University of Prešov, 17. novembra 1,SK-08116 Prešov, Slovakia; e-mail: [email protected] 2Institute of Breeding and Diseases of Game and Fish, University of Veterinary Medicine and Pharmacy, Komenského 73, SK-04181 Košice, Slovakia 3Institute of Zoology, Slovak Academy of Sciences, Dúbravská cesta 9,SK-84506 Bratislava, Slovakia

Abstract: Freshwater fishes recorded in the territory of Slovakia include 95 fish species. As many as one third of these are allochthonous fish species belonging to 14 families, among which several have not occurred in Slovakia recently. Historically, there were three main periods of introduction: the first is the beginning of the 20th century, the second includes two decades between 1955 and 1975 and the third period is from the year 1990 up to the present time. The origins of the exotic species seen in Slovakia are the four continents – Africa (3), North America (7), Central America (3), and Asia (13) and ten of them are from different regions in Europe. The purpose of intentional introductions of non-native species was to occupy vacant ecological niches in the ecosystems reshaped by human activities, fish stocking, angling or fish farming. Some of these species spread from their original ranges or they penetrated spontaneously from the adjacent countries via the river network system. At the present time, 76 fish species in total form populations in Slovakia. There are 54 autochthonous and 22 allochthonous species, 14 of them are exotic fishes. The invasive characters in 13 fish species were considered, the recent native/total fish ratio is 0.71. Key words: introduced fishes; Danube; Tisa; Dunajec; biological invasion

Introduction Material and methods In the case of absence of a national monitoring network on Both, destruction of natural habitats and introduc- introduced fish species, the data used in this study origi- tions of alien species, led to the changes in biodiver- nated from various sources. sity noted during the last century. Aquatic ecosys- The status of the species was established from histori- tems disturbed by human activities seem to be par- cal research and actual fish sampling. The ratio of the num- ticularly vulnerable to these invasions (Alimov 1998; ber of native species to the total number of species cur- Dgebuadze & Skoromokhov 2002; Moyle & Light 1996; rently recorded (called the „zoogeographic integrity coeffi- Panov et al. 1999; Welcomme 1991). Among the ver- cient“) by Bianco (1990) was calculated. The terms “non- tebrates, introductions of freshwater fish species have indigenous” and “non-native”, “alien” or “exotic” according to Copp et al. (2005) and ecological groups of fishes follow- been the most numerous (Cowx 1997; Gido & Brown ing Holčík (1998) are used. Only species able to overwinter 1999). Introductions of exotic freshwater fishes are one were taken into account. of the main threats to native fish species around the The nomenclature and taxonomical status of fish world. species used follow the papers by Boguckaja & Naseka Many exotic fish species have been introduced to (2004), Kottelat & Freyhof (2007) and Neilson & Stepien Europe, and many more have been translocated among (2009). European countries (Holčík 1991; Lehtonen 2002; Copp et al. 2005). In Slovakia, only preliminary and incom- Results and discussion plete lists of non-native fishes are available (Hensel & Mužík 2001; Kováč et al. 2007) and only a few stud- The introduction of species and their transfer in Slo- ies on interactions between exotic and native fishes vakia have been performed (Žitňan 1974; Lusk et al. 2004; The history of introductions and transfers of alien Košuthová et al. 2008). The aim of the present study species to Slovak waters can be divided into three was to collect, as far as possible, all existing informa- main periods. Except for Rhodeus amarus (Bloch, tion on alien fish in Slovakia by using published data, 1782) and Proterorhinus marmoratus (Pallas, 1814) data from fish farms, fish research institutions, admin- syn. Protherorhinus semilunaris (Heckel, 1837) that istrations and consultants. probably spread via the Danube River hundreds of

c 2010 Institute of Zoology, Slovak Academy of Sciences 1058 J. Koščo et al.

Table 1. Origin of the non-native species in the ichthyofauna of Slovakia.

Family Species First report Original area Origin Present status

I Polyodontidae 1 Polyodon spathula (Walbaum, 1792) 1992 North America IF 1R II Acipenseridae 2 Acipenser baerii Brandt, 1869 2006 Asia IF 1R III Cyprinidae 3 Carassius auratus (L., 1758), ca.1900 Asia AR I 4 Carassius gibelio (Bloch, 1782) 1961 Asia S I 5 Cyprinus rubrofuscus Lacepède, 1803 1996 Asia S ? 6 Ctenopharyngodon idella (Valenciennes, 1844) 1961 Far East IFAS S, AR 7 Pseudorasbora parva (Temminck et Schlegel, 1846) 1974 Far East S I 8 Hypophthalmichthys molitrix (Valenciennes, 1844) 1965 Far East IFAS S, AR 9 Hypophthalmichthys nobilis (Richardson, 1845) 1964 Far East IFAS S, AR 10 Rhodeus amarus (Bloch, 1782) ca. 1200 Asia S WS IV Ictaluridae 10 Ameiurus melas (Rafinesque, 1820) 1999 North America S I 11 Ameiurus nebulosus (Lesueur, 1819) 1926 North America S I V Clariidae 12 Clarias gariepinus (Burchell, 1822) 1989 Africa IF E VI Coregonidae 13 Coregonus albula (L., 1758) 1957 North Europe IVEN E 14 Coregonus migratorius (Georgi, 1775) 1960 Asia IVEN E 15 Coregonus maraena (Bloch, 1779) 1929 North Europe IVEN O 16 Coregonus peled (Gmelin, 1789) 1970 Russia IVEN E 17 Coregonus wartmanni (Bloch, 1784) 1955 Russia IVEN E 18 Coregonus renke (Schrank, 1783) 1992 North Europe AE 1R VII Salmonidae 19 Oncorhynchus mykiss (Walbaum, 1792) ca. 1900 North America IFAS S, O 20 Salvelinus fontinalis (Mitchill, 1814) ca. 1900 North America IFAS S, AR VIII Thymallidae 21 Thymallus baicalensis Dybowski, 1874 1959 Asia IVEN E IX Cyprinodontidae 22 Poecilia reticulata Peters, 1859 1970 Central America AR O 23 Poecilia sphaenops (Valenciennes, 1846) 1970 Central America AR E? 24 Xiphophorus helleri Heckel, 1848 1970 Central America AR E? XGasterosteidae 25 Gasterosteus aculeatus (L., 1758) 1967 Holarctic Region S I XI Centrarchidae 26 Lepomis gibbosus (L., 1758), 1956 North America S I 27 Micropterus salmoides (Lacepède, 1802) 1957 North America AE 1R XII Cichlidae 28 Haplochromis niloticus Greenwood, 1960 1995 Africa IF E 29 Oreochromis mossambicus (L., 1758) 2003 Africa AR O XIII Odontobutidae 30 Perccottus glenii Dybowski, 1877 1998 Far East S I XIV Gobiidae 31 Apollonia fluviatilis (Pallas, 1814) 2001 Danube delta S I 32 Apollonia melanostoma (Pallas, 1814) 2003 Danube delta S I 33 Babka gymnotrachelus (Kessler, 1857) 1999 Danube delta S I 34 Ponticola kessleri (Günther, 1861) 1996 Danube delta S I 35 Proterorhinus semilunaris (Heckel,1837) ca. 1870 Danube delta S I

Explanations: IF – intentional import (farming), S – spontaneous expansion, IFAS –intentional import (farming, angling, stocking), AE – accidental (escape), AR – aquarists’ release, IVEN – imported to fill the vacant ecological niche. Present status: 1R – one record, I – invasive, O – one population, E – extinct, S – stocked, AR – artificial reproduction, WS – wide spread. years ago (Harka & Bíró 2007; Van Damme et al. Coregonus albula (L., 1758), Coregonus migratorius 2007), the first introductions occurred in the beginning (Georgi, 1775), Coregonus peled (Gmelin, 1789) (Kirka of the 20th century, when Oncorhynchus mykiss (Wal- & Bastl 1963; Holčík 1998), three herbivorous species baum, 1792) and Salvelinus fontinalis (Mitchill, 1814) Ctenopharyngodon idella (Valenciennes, 1844), Hy- followed by Coregonus maraena (Bloch, 1779) a few pophthalmichthys molitrix (Valenciennes, 1844), Hy- years later (Table 1) were imported (Holčík 1969; Volf pophthalmichthys nobilis (Richardson, 1845) (Kokorďák & Hubáček 1930). In the same period Ameiurus neb- 1969; Holčík & Pár 1970) and Thymallus baicalensis ulosus (Lesueur, 1819) penetrated from neighbouring Dybowski, 1874 were introduced (Pavlík 1963). Other countries (mainly Hungary) (Balon 1966). species such as, Lepomis gibbosus (L., 1758) (Balon In the second period (1955–1975), four species & Mišík 1956), Carassius auratus (L., 1758), Caras- of whitefishes Coregonus wartmanni (Bloch, 1784), sius gibelio (Bloch, 1782) (Balon 1962), Gasterosteus Non-native fishes of Slovakia 1059 aculeatus (L., 1758) (Balon 1967) and Pseudorasbora or 13th century (Kottelat & Freyhof 2007; Van Damme parva (Temminck & Schlegel, 1846) (Žitňan & Holčík et al. 2007). 1975) spread spontaneously from adjacent countries. At the end of the 19th and beginning of the 20th The occurrence of Micropterus salmoides (Lacepède, century, European angling and fishery organisations in- 1802) – only one specimen (Mišík 1958) and Coregonus troduced several species mainly from North America renke (Schrank, 1783) – four specimens was accidental (Oncorhynchus mykiss, Salvelinus fontinalis, Ameiurus (Holčík 2003), and the distribution area of three or- melas, Ameiurus nebulosus, Micropterus salmoides,and namental species Poecilia reticulata Peters, 1859, Poe- later Polyodon spathula). Some of these species were cilia sphaenops (Valenciennes, 1846), Xiphophorus hel- also introduced to Slovakia (Oncorhynchus mykiss, leri Heckel, 1848 was limited to the thermal brook near Salvelinus fontinalis, Polyodon spathula). Other species the spa in Bojnice town (Hensel & Brtek 1971). occurring here resulted from accidental escapes from The other species – Polyodon spathula (Walbaum, fish farms in neighbouring countries and natural spread- 1792) (Áč & Šubjak 2005), Cyprinus rubrofuscus La- ing. The main purposes of these introductions were to cepède, 1803 (hybrid form), Haplochromis niloticus increase the attractiveness of recreational angling and Greenwood, 1960 and Clarias gariepinus (Burchell, improve the yields of commercial fisheries. Increased 1822) were introduced, and other species – 4 gobiid water eutrophification, mainly in the agricultural low- species Neogobius kessleri (Gunther, 1861) syn. Ponti- lands led to the introduction of three herbivorous cola kessleri (Stráňai 1997), Neogobius gymnotrachelus fishes (Ctenopharyngodon idella, Hypophthalmichthys (Kessler, 1857) syn. Babka gymnotrachelus (Kautman molitrix, and Hypophthalmichthys nobilis). In order to 2001), Neogobius fluviatilis (Pallas, 1814) syn. Apol- conduct aquaculture in thermal waters, Clarias gariepi- lonia fluviatilis (Stráňai & Andreji 2001), Neogobius nus and Haplochromis niloticus were introduced. Illegal melanostoma (Pallas, 1814) syn. Apollonia melanos- imports of Micropterus salmoides for biological control toma (Stráňai & Bitter 2003), and Perccottus glenii of invasive Ameiurus melas have been carried out in Dybowski, 1877 (Koščo et al. 1999) and Ameiurus recent years (Krajč, in verb). A few specimens of non- melas (Rafinesque, 1820) (Koščo et al. 2000) occurred identified Coregonids were caught in the water reservoir in the third period (from 1990). The record of Acipenser at Hriňová (Slovakia) around the same time (Rybár, in baerii Brandt, 1869 was accidental (only one specimen) verb). (Masár et al. 2006) and one population of Oreochromis Several other species were introduced accidentally mossambicus (L., 1758) in the thermal brook near Bo- together with species for aquaculture or spread from jnice was registered (Májsky 2007). adjacent countries (Carassius gibelio, Lepomis gibbosus, The first and second periods correspond to the Gasterosteus aculeatus, Pseudorasbora parva), or they global peaks of introductions (Welcomme 1988; Lehto- were released by Slovak aquarists (Carassius auratus, nen 2002). The third peak is characteristic for the Oreochromis mossambicus, Poecilia reticulata, Poecilia Danube River basin, where goby species occurred in sphaenops, Xiphophorus helleri). the middle Danube (Ahnelt et al. 1998; Simonovićetal. The major motivation for introductions of “lake 1998; Holčík et al. 2003; Uzunova & Zlatanova 2007). species” (mainly genus Coregonus and Thymallus bai- In other European countries, the first period is similar calensis) was to fill a vacant niche in the new man-made to that in Slovakia. In the second period, the number of habitats in reservoirs. In several cases, fish introduc- introductions has gradually increased up to the present tions for more than one reason were carried out. (Crivelli 1995; Elvira & Almodovar 2001; Copp et al. During recent years, the invasions of four goby 2007; Hesthagen & Sandlund 2007; Verreycken et al. species (Ponticola kessleri, Babka gymnotrachelus, Apol- 2007; Lusk et al. 2010). lonia fluviatilis, Apollonia melanostoma), spreading from the lower Danube has been observed. Simultane- The goal of introduction ously, spreading of the sleeper Perccottus glenii from According to Holčík (1991), the main motivations for the Ukraine and Ameiurus melas from Hungary in the fish introduction in Central and Eastern Europe are as Tisa River basin was also registered. follows: aquaculture (also experimental), accident, im- provement of the wild stock, sport, biomanipulation, re- Origin of non-native species lease of ornamental fishes and other unknown reasons. Until now, 36 non-native species representing 14 fam- Similarly, Crivelli (1995) defined the five reasons for in- ilies have been recorded in Slovakia. The native ar- troduction in the North and Mediterranean region: to eas of these alien species are on four continents (Ta- improve angling catches, increased yields in commer- ble 1). Asia is the principal origin of introduced fishes cial fisheries, accidental (escapes from fish farms, live with 13 species (Acipenser baerii , Cyprinus rubrofus- bait, and ornamental fishes), wetland management and cus, Carassius auratus, Carassius gibelio, Pseudoras- mosquito control. bora parva, Rhodeus amarus, Ctenopharyngodon idella, The first introductions were associated with the Hypophthalmychthis molitrix, Hypophthalmychthis no- domestication of the common carp Cyprinus carpio bilis, Coregonus migratorius, Coregonus peled, Thymal- (L., 1758) in Europe. Common carp that is native to lus baicalensis, Perccottus glenii), followed by Amer- Danube was probably translocated together with bitter- ica with 10 species, seven from north America (Poly- ling (Rhodeus amarus) throughout Europe in the 12th odon spathula, Ameiurus melas, Ameiurus nebulo- 1060 J. Koščo et al. sus, Oncorhynchus mykiss, Salvelinus fontinalis, Lepo- Table 2. The number of native (N), non-native (NN) and inva- mis gibbosus, Micropterus salmoides), three from cen- sive (I) species in constituent guilds according to their relation to current (C), reproduction guilds (RG) and in feeding groups tral America (Poecilia reticulata, Poecilia sphaenops, (FG)inSlovakianwaters. Xiphophorus helleri) and three species have been in- A troduced from Africa (Oreochromis mossambicus, Hap- lochromis niloticus, Clarias gariepinus). C NNNI The source of spreading European gobies species Re 34 7 1 istheDanubedelta(Ponticola kessleri, Babka gymno- Li 9115 trachelus, Apollonia fluviatilis, Apollonia melanostoma, Et 16 13 6 Proterorhinus semilunaris). The origin of translocated Total 59 31 12 coregonids is Russia (Coregonus albula, Coregonus peled), Poland (Coregonus maraena), Alpine lakes B (Coregonus renke) (Holčík 2003) and only once, the fer- RG NNNI tilized eggs of Coregonus wartmanni from Switzerland were transferred. A.1.1. 2 3 Most of the non-native species were introduced A.1.2 3 3 A.1.3 13 1 from the Czech Republic and Hungary. Only a few A.1.4 7 1 species were imported from the original areas. A.1.5 10 4 2 Welcomme (1991) referred to 113 and Holčík A.1.6 5 (1991) to 134 non-native fish taxons that have been A.2.3 11 2 A.2.5 1 introduced into European fresh waters. Excluding the B.1.4 2 native European species, at least 76 exotic species are B.2.2 3 3 recognized mainly of North American (34) and Asian B.2.4 1 1 (26) origin (Lehtonen 2002). B.2.5 3 1 B.2.7 2 7 6 C.1.3 2 Present status C.2.2 2 Analysing the data on fish species recorded in Slovakia, C.2.4 1 only 22 non-native species (of the total 36 species) were Total 59 31 12 recorded in the wild. It seems that only 18 species established self-sustaining populations in Slovakia, and four C species require continual restocking (for a summary see FG NNNI Table 1). Oncorhynchus mykiss is still found in the Morské Ca.1 36 13 7 Oko lake in the Vihorlat Mts (E Slovakia) since its Ca.2.1 10 2 th Ca.2.2 1 stocking at the beginning of the 20 century. Coregonus Ca.2.3 1 1 maraena is still recorded in the Štrbské pleso tarn in Eu 10 12 5 the High Tatras Mts, but monitoring of its population He.2.1 1 1 status is required. In general, the invasive characters He.2.2 1 1 showed 13 allochthonous species (Table 1). Total 59 31 12 The zoogeographic integrity coefficient for Slovakia reaches the value of 0.71. Following the differences within the three major river basins of Slovakia, the number of exotic species is highest in the Danube River four non-native gobies to the territory of Slovakia. Only basin (14) followed by the Tisa River basin (12). Only one invasive species, exotic Perccottus glenii,spread two species are distributed in the Dunajec River basin from the Ukraine. In general, all of these fishes spread (Vistula River basin). to Slovakia spontaneously from adjacent countries, no Holčík (1991) reported as many as 134 fish and species was imported directly. lampreys species introduced in Europe (including 74 exotic) till the end of the 1980s. With regard to the num- Proposed impact on native ichthyofauna ber of introduced fish species, Czechoslovakia with 36 Studies on the interactions between allochthonous and non-native fishes (24 exotic and 12 translocated) occu- autochthonous fish fauna are rare. Fortunately, most pied the 3rd position while, in relation to the area of the of the deliberately transferred alien species proved un- country, it occupied the 14th position. It was mainly the able to compete with the native ones, and when the Czech Republic that, as the part of the former common stocking ceased, they disappeared or their occurrence state (Czechoslovakia), was the source of introductions became limited to local populations. Almost half of the carried out in Slovakia (Lusk et al. 2010). Furthermore, invasive species belongs to the limnophilous fishes (Ta- Hungary was also the source of the spontaneous spread- ble 2A). It reflects the strong competitive pressure for ing of exotic invasive species such as Ameiurus nebulo- native limnophilous species. Despite used to be abun- sus, Ameiurus melas, Carassius gibelio, Pseudorasbora dant in the past, most of these species became threat- parva, Lepomis gibbosus, Gasterosteus aculeatus and ened recently such as Umbra krameri Walbaum, 1792, Non-native fishes of Slovakia 1061

Carassius carassius (L., 1758), Leucaspius delineatus troduction of lake form Oncorhynchus mykiss into the (Heckel, 1843) and Misgurnus fossilis (L., 1758) (Koščo Veľké Vihorlatské Lake was connected with a decrease & Holčík 2008). of native Salmo trutta (Koščo et al. 2000). According to the spawning substratum require- Some negative effects on the indigenous ichthy- ments, the most endangered reproductive guild is ofaunacanbepresumedalsointhecaseofPseudoras- speleophils (Table 2B). The number of invasive species bora parva (Pinder et al. 2005; Carpentier et al. 2007; from the speleophils is three times higher than the num- Beyer et al. 2007) or four gobies (Koščo et al. 2006). ber of native species from this reproductive guild. This Introduction of diseases and parasites is also a could be the major threat to C. gobio (L., 1758) which problem intimately connected with introduction of is protected by European legislation (92/43/EHS) in fishes in Slovakia. Several new parasite species have the Danube, where the population density of C. gobio spread in Europe as a consequence of fish transfers (see, could be decreased by invasive gobies (Černý 2006). e.g., Scholz & Cappelaro 1993; Scholz 1999; Kirk 2003; Most of the invasive species are omnivorous (41.7%) Oros et al. 2004), including the specific parasite of P. with a high ability to adapt to new diet components glenii – Nippotaenia mogurndae Yamaguti et Miyata, in novel environments. In view of this, invasive species 1940 (Cestoda: Nippotaeniidea), which have become could be considered as competitors for the majority of widely distributed in East Slovakia (Košuthová et al. the native ichthyofauna. Other invasive species (58.3%) 2004, 2008). feed on non-specific animal food (Table 2C). They are Preferentially, allochthonous fishes occupy lenitic classified into the same feeding group as most of the biotopes (Irz et al. 2004) in the low courses of the native fishes (61%). More than a half of these species main rivers (Baltz & Moyle 1993; Bianco & Ketmaier are threatened and listed in the most recent Red List 2001; Crivelli 1995; Elvira 1995). In many cases, intro- of the Slovak Republic (Koščo & Holčík 2008). duced species were more successful in disturbed habi- Koščo & Manko (2003) pointed out the negative tats (Marchetti & Moyle 2000; Rosecchi et al. 1997). effects of invasive species P. glenii on the native endan- The lower courses of the main rivers and their disturbed gered Umbra krameri. The native fish species (mainly habitats in the lowlands of south Slovakia (Tisa and U. krameri and Leucaspius delineatus) were suppressed Danube river systems) represent the areas with a high and their density decreased in some water bodies that degree of the endemism. Unfortunately, the diversity of were occupied by A. nebulosus, in the past. Similarly, native freshwater fish communities is threatened by in- A. melas may recently have had the same effects, al- troductions of exotic species (Koščo & Holčík 2008). In though there is no strong support for this hypothesis this case, the effective protection of native fish fauna (Hajdú et al. 2008). realised by the preservation of their biotopes followed The rapid spread and population increase of the by prevention of alien fish introductions have to be pri- Carassius gibelio population, which invaded floodplains orities within European and national conservation pro- or larger rivers, had a significant negative impact on grammes. the indigenous species – Carassius carassius and Tinca tinca (L., 1758) (Lusk et al. 2004). Carassius gibelio is an important trophic and spatial competitor for other Acknowledgements cyprinid species (e.g., Cyprinus carpio, L. delineatus). The authors are grateful to J. Masár, J. Šubjak and T. 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