Abstract
Four gobiid species, Babka gymnotrachelus, Neogobius melanostomus, Neogobius fluviatilis, and Proterorhinus semilunaris, were parasitologically studied in different localities of the Dnieper and Vistula river basins. The highest number of parasitic species was found in N. fluviatilis (35 taxa). The parasite fauna of N. melanostomus, B. gymnotrachelus, and P. semilunaris consists of 23, 22, and 15 taxa, respectively. The species accumulation curves show stable accumulation of parasite species by all four fish hosts along the studied part of the corridor, from the Dnieper Estuary to the Vistula River delta. The plot reveals also that the studied gobies lose the parasites common in the host native range and accept new parasites from the colonized area. In the case of N. melanostomus, it complies with the enemy release hypothesis, as the parasite load was low in the invaded area if compared to the native range. The three other alien gobies are vector for Gyrodactylus proterorhini in the Baltic basin. Moreover, populations of this alien monogenean tend to be more abundant in their new range in comparison with the Black Sea basin. In general, the number of parasite species in the colonized area was of the same rank as in the native one for N. fluviatilis, and even higher for B. gymnotrachelus. This results from accumulating new parasite species along the gobiid invasion route. In particular, the N. fluviatilis, B. gymnotrachelus, and P. semilunaris lost some of their native parasites and gained the local ones after entering the post-dam part of the Vistula River; it can be interpreted as a partial escape from parasites.
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References
Ahnelt H, Bănărescu P, Spolwind R, Harka A, Waidbacher H (1998) Occurrence and distribution of three gobiid species (Pisces: Gobiidae) in the middle and upper Danube region – example of different dispersal patterns? Biológia (Bratislava) 53:661–674
Bij de Vaate A, Jazdzewski K, Ketelaars HAM, Gollasch S, Van der Velde G (2002) Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Can J Fish Aquat Sci 59:1159–1174
Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83(4):575–583
Chernova TN (1970) K izucheniyu parazitofauny ryb oz. Paleostomi [in:] Abstracts of 1st Symp “Voprosy morskoy parazitologii”, VA Vodyanitskiy (ed), Kiev, pp 132–134 (in Russian)
Ciurea I (1933) Sur quelques larves des vers parasites de l'homme, des mammifères et de oiseaux ichtyophages, trouvas chez des grands lacs de la Bessarabie, du Dniestr et de son liman. Arch Roum Pathol Exp 6(1–2):151–170
Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733
Copp GH, Bianco PG, Bogutskaya NG, Erös T, Falka I, Ferreira MT, Fox MG, Freyhof J, Gozlan RE, Grabowska J, Kováč V, Moreno-Amich R, Naseka AM, Peňáz M, Povž M, Przybylski M, Robillard M, Russell IC, Stakėnas S, Šumer S, Vila-Gispert A, Wiesner C (2005) To be, or not to be, a non-native freshwater fish? J Appl Ichthyol 21:242–262
Danilkiewicz Z (1996) Babka lysa (gologlowa), Neogobius gymnotrachelus (Kessler, 1857) (Perciformes, Gobiidae), nowy gatunek w ichtiofaunie zlewiska Morza Bałtyckiego. Komunikaty Rybackie 2:27–29
Danilkiewicz Z (1998) Babka szczupła, Neogobius fluviatilis (Pallas, 1811), Perciformes, Gobiidae – nowy, pontyjski element w ichtiofaunie zlewiska Morza Bałtyckiego. Fragm Fauna 41(21):269–277
Ergens R (1967) New species of the genus Gyrodactylus (Monogenoidea) from the Danube basin. Folia Parasitol 14:377–379
Gaevskaya AV, Dmitrieva ED (1997) Overview of Black Sea monogenean fauna. Ekologiya Morya 46:7–17 (in Russian with English summary)
Gaevskaya AV, Gusev AV, Delyamure SL, Donets ZS, Iskova NI, Kornyushin VV, Kovaleva AA, Margaritov NM, Markevich AP, Mordvinova TN, Naidenova NN, Nikolaeva VM, Parukhin AM, Pogoreltseva TP, Smogorzhevskaya LA, Solonchenko AI, Shtein GA, Shulman SS (1975) Opredelitel’ parazitov pozvonochnyh Chernogo i Azovskogo morey. Naukova Dumka, Kiev, 552 p. (in Russian)
Grabowska J, Pietraszewski D, Ondračková M (2008) Tubenose goby Proterorhinus marmoratus (Pallas, 1814) has joined three other Ponto-Caspian gobies in the Vistula River (Poland). Aquat Inv 3(2):261–265
Harka Á, Bíró P (2007) New patterns in Danubian distribution of Ponto-Caspian gobies – a result of global climatic change and/or canalization? Electronic J Ichthyol 1:1–14
Janković DV (1996) Ichthyofauna of the Danube in the Djerdap Area after the construction of the Iron Gate I Hydroelectric Power system. Acta Univ Carol (Biol) 40:123–131
Kostrzewa J, Grabowski M (2001) Babka łysa (gołogłowa), Neogobius gymnotrachelus (Kessler, 1857) (Gobiidae, Perciformes) – nowy gatunek ryby w Wiśle. Przegl Zool 45(1–2):101–102
Kostrzewa J, Grabowski M (2002) Babka szczupła, Neogobius fluviatilis (Pallas, 181 l), w Wiśle – fenomen inwazji pontokaspijskich Gobiidae. Przegl Zool 46(3–4):235–242
Kostrzewa J, Grabowski M, Zięba G (2004) Nowe inwazyjne gatunki ryb w wodach Polski. Arch Polish Fish 12:21–34
Koval VP (1961) Parazyty ryb Dniprovskogo lymanu. Visnyk Kyiv Univ (Ser Biol Sci) 4(2):81–86 (in Ukrainian)
Koval VP (1962) Parazyty ryb delty Dnipra. Visnyk Kyiv Univ (Ser Biol Sci) 5(1):98–104 (in Ukrainian)
Koval VP, Gerus MM (1968) Parazitofauna ryb Kakhovskogo vodoskhovyshcha (v rayoni ponyzzya) na odynadtsiatomu rotsi yogo isnuvannya. Visnyk Kyiv Univ (Ser Biol Sci) 10:149–152 (in Ukrainian)
Koval VP, Maksay VV (1970) Do vyvchennya parazitofauna ryb r. Ros. Visnyk Kyiv Univ (Ser Biol Sci) 12:162–168 (in Ukrainian)
Koval VP, Pashkevychute AS, Boshko OG, Kovalenko AA, Stavrovskyi KB (1973) Parazitofauna ryb Kakhovskogo vodoskhovyshcha (v rayoni ponyzzya) na shistnadtsiatomu rotsi yogo isnuvannya. Visnyk Kyiv Univ (Ser Biol Sci) 15:135–138 (in Ukrainian)
Koval VP, Vagushchenko AM, Seregina LY, Pashkevychute AS (1975) Parazitofauna ryb Kakhovskogo vodoskhovyshcha (v rayoni verkhivya) na chotyrnadtsiatomu rotsi yogo isnuvannya. Visnyk Kyiv Univ (Ser Biol Sci) 17:105–108 (in Ukrainian)
Krasnovyd V, Kvach Y, Drobiniak O (2012) The parasite fauna of the gobiid fish (Actinopterygii, Gobiidae) in the Sykhyi Lyman, Black Sea. Vestn Zool 46(6):483–490
Kvach Y (2002) Helminthes of goby fish of the Hryhoryivsky Estuary. Vestn Zool 36(3):71–76
Kvach Y (2010) Communities of metazoan parasites of gobiids fishes (Actinopterygii: Gobiidae) of the water complex of lower Dniester River. Visnyk Lviv Univ (Biol) 54:208–215 (in Ukrainian with English summary)
Kvach Y, Oğuz MC (2009) Communities of metazoan parasites of two fishes of Proterorhinus genus (Actinopterygii: Gobiidae). Helminthology 46(3):168–176
Kvach Y, Skóra KE (2007) Metazoa parasites of the invasive round goby Apollonia melanostoma (Neogobius melanostomus) (Pallas) (Gobiidae: Osteichthyes) in the Gulf of Gdańsk, Baltic Sea, Poland: a comparison with the Black Sea. Parasitol Res 100:767–774
Kvach Y, Stepien CA (2008) Metazoan parasites of introduced round and tubenose gobies in the Great Lakes: support for the “enemy release hypothesis”. J Great Lakes Res 34:23–35
Kvach Y, Winkler HM (2011) The colonization of the invasive round goby Neogobius melanostomus by parasites in new localities in the southwestern Baltic Sea. Parasitol Res 109:769–780
Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 362(8):1535–1545
Machkevsky VK, Mordvinova TN, Parukhin AM (1990) The helminth fauna of gobiids of the Gulf of Yegorlyk and Donuzlav Lake—places of the mussel farms. Ekologiya Morya 36:69–75 (in Russian with English summary)
Markevich OP (1949) Gelmintofauna ryb r. Dnipra v rayoni m. Kaniv. Nauk Zap Kyiv Univ 8(6):73–83 (in Ukrainian)
Mierzejewska K, Martyniak A, Kakareko T, Dzika E, Stańczak K, Hliwa P (2011) Gyrodactylus proterorhini Ergens, 1967 (Monogenoidea, Gyrodactylidae) in gobiids from the Vistula River—the first record of the parasite in Poland. Parasitol Res 108:1147–1151
Molnár K (2006) Some remarks on parasitic infections of the invasive Neogobius spp. (Pisces) in the Hungarian reaches of the Danube River, with a description of Goussia szekelyi sp. n. (Apicomplexa: Eimeriidae). J Appl Ichthyol 22:1–6
Moskalkova KI (1996) Ekologicheskiye i morfo-fiziologicheskiye predposylki k rasshireniyu areala u bychka-kruglyaka Neogobius melanostomus v usloviyah antropogennogo zagryazneniya. Vop Ihtiologii 36(5):615–621 (in Russian)
Naidenova NN (1974) Parazitofauna ryb semeystva bychkovyh Chernogo i Azovskogo morey. Naukova Dumka, Kiev (in Russian)
Ohayon JL, Stepien CA (2007) Genetic and biogeographic relationships of the racer goby Neogobius gymnotrachelus (Gobiidae: Teleostei) from introduced and native Eurasian locations. J Fish Biol 71:360–370
Ondračková M, Dávidová M, Blažek R, Gelnar M, Jurajda P (2009) The interaction between an introduced fish host and local parasite fauna: Neogobius kessleri in the middle Danube River. Parasitol Res 105:201–208
Ondračková M, Francová K, Dávidová M, Polačik M, Jurajda P (2010) Condition status and parasite infection of Neogobius kessleri and N. melanostomus (Gobiidae) in their native and non-native area of distribution of the Danube River. Ecol Res 25:857–866
Ovcharenko NA (1985) K faune i ekologii mikrosporidiy ryb Sem. Gobiidae nizovyev Dniepra, Dniepro-Bugskogo i Berezanskogo limanov. Gidrobiologicheskiy Zh 21(4):103–108 (in Russian)
Ovcharenko M (2009) Microsporidia infecting the muscle tissues of native and invasive gammarids (Gammaroidea, Amphipoda) in Poland [in:] Różnorodność oddziaływania układów pasożyt-żywiciel w środowisku. XVIII Wrocławska Konferencja Parazytologiczna. Wrocław–Karpacz, 21–23 maja 2009, p. 23
Ovcharenko M, Codreanu-Bălcescu D, Grabowski M, Konopacka A, Wita I, Czaplińska U (2009) Gregarines (Apicomplexa) and microsporidians (Microsporidia) of native and invasive gammarids (Amphipoda, Gammaroidea), occurring in Poland. Wiad Parazytol 55(3):237–247
Panov VE, Alexandrov B, Arbačiauskas K, Binimelis R, Copp GH, Grabowski M, Lucy F, Leuven RSEW, Nehring S, Paunović M, Semenchenko V, Son MO (2009) Assessing the risks of aquatic species invasions via European inland waterways: from concepts to environmental indicators. Integr Environ Assess Manag 5(1):110–126
Pinchuk VI, Smirnov AI, Koval NV, Shevchenko PG (1985) O sovremennom rasprostaranenii bychkovyh ryb (Gobiidae) v basseyne Dnepra [in:] Gidrobiologicheskiye issledovaniya presnyh vod. Naukova Dumka, Kiev, pp 121–130 (in Russian)
Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19(7):385–390
Rolbiecki L (2006) Parasites of the round goby, Neogobius melanostomus (Pallas, 1811), an invasive species in the Polish fauna of the Vistula Lagoon ecosystem. Oceanologia 48(4):545–561
Sapota MR (2004) The round goby (Neogobius melanostomus) in the Gulf of Gdańsk—a species introduction into the Baltic Sea. Hydrobiologia 514:219–224
Sapota M, Skóra KE (2005) Spread of alien (non-indigenous) species Neogobius melanostomus in the Gulf of Gdańsk (South Baltic). Biol Invasions 7:157–164
Semenchenko V, Grabowska J, Grabowski M, Rizevsky V, Pluta M (2011) Non-native fish in Belarusian and Polish areas of the European central invasion corridor. Oceanol Hydrobiol Stud 40(1):57–67
Skóra KE, Stolarski J (1993) New fish species in the Gulf of Gdańsk Neogobius sp. [cf. Neogobius melanostomus (Pallas 1811)]. Bull Sea Fish Inst 1(128):83
Slynko YV, Dgebuadze YY, Novitskiy RA, Kchristov OA (2011) Invasions of alien fishes in the basins of the largest rivers of the Ponto-Caspian basin: composition, vectors, invasion routes, and rates. Rus J Biol Inv 2(1):49–59
Smirnov AI (1986) Okuneobraznye (bychovye), skorpenoobraznye, kambaloobraznye, prisoskoobraznye, udilshchikoobraznye [in:] Fauna of Ukraine, Vol. 8, No 5, Naukova Dumka, Kiev, 320 p (in Russian)
Sokolov LI, Tsepkin EA, Sokolova EL, Golovatyuk GY (1989) Novye zhiteli Moskvy-reki. Priroda 9:80–81 (in Russian)
Sørensen TA (1948) A new method of establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analysis of vegetation on Danish commons. K Dan Vidensk Selsk Biol Skr 5:1–34
Tanaka S, Nishida T, Ohsaki N (2007) Sequential rapid adaptation of indigenous parasitoid wasps to the 404 invasive butterfly Pieris brassicae. Evol 61:1791–1802
Tompkins DM, White AR, Boots M (2003) Ecological replacement of native red squirrels by invasive greys driven by disease. Ecol Lett 6:189–196
Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630
Ugland KI, Gray JS, Ellingsen KE (2003) The species-accumulation curve and estimation of species richness. J Anim Ecol 72:888–897
Wiesner C (2005) New records of non-indigenous gobies (Neogobius sp.) in the Austrian Danube. J Appl Ichthyol 21:324–327
Yurakhno VM, Gorchanok NV (2011) Myxosporea Kudoa nova (Myxosporea: Kudoidae)—parasite of the Black Sea and the Sea of Azov fish. Morskoy Ekologichekyi Zh 10(2):68–77 (in Russian with English summary)
Yurakhno V, Mierzejewska K, Rubtsova N, Grabowska J, Ovcharenko M (2012) First registration of Trichodina domerguei (Ciliophora, Trichodinidae) from Ponto-Caspian gobies in Poland [in:] Abstracts of 7th European Conference on Biological Invasions “Neobiota” (Pontevedra, Spain 12–14 September 2012), Leon, p. 216
Zander CD (2004) Four-year monitoring of parasite communities in gobiid fishes of the south-western Baltic.II. Infracommunity. Parasitol Res 93:17–29
Acknowledgments
The study was supported by a grant NN 304409239 from the Ministry of Sciences and Higher Education of Poland. We thank Dr. Andrzej Martynyak (University of Warmia and Mazury, Olsztyn, Poland), Dr. Michal Grabowski (University of Łódź), and Dr. Zynoviy Petrovych (Regional Landscape Park “Kinburnska Kosa”, Ochakiv, Ukraine) for their help in the organization of sampling. Also, we thank Agnieszka Cyrson, Oleksandra Drobinyak, Mikhail Kornyychuk, Yuliya Kutsokon, Karolina Nicijewska, Valentyna Ovcharenko, and Galina Zolotaryova for their support and assistance.
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Kvach, Y., Kornyychuk, Y., Mierzejewska, K. et al. Parasitization of invasive gobiids in the eastern part of the Central trans-European corridor of invasion of Ponto-Caspian hydrobionts. Parasitol Res 113, 1605–1624 (2014). https://doi.org/10.1007/s00436-014-3791-2
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DOI: https://doi.org/10.1007/s00436-014-3791-2