Hydrobiologia (2007) 590:3–14 DOI 10.1007/s10750-007-0752-0 INVASIVE CRUSTACEA Invasion biology of Ponto-Caspian onychopod cladocerans (Crustacea: Cladocera: Onychopoda) Vadim E. Panov Æ Natalie V. Rodionova Æ Pavel V. Bolshagin Æ Eugene A. Bychek Ó Springer Science+Business Media B.V. 2007 Abstract We review the patterns of recent range possess adaptive life cycles, switching to early expansions and the biology of the invasive Ponto- gamogenetic reproduction which enables their Caspian predatory onychopod cladocerans: establishment in recipient ecosystems and further Cercopagis pengoi, Evadne anonyx, Podonevadne dispersal. Analysis of temperature and salinity trigona, Cornigerius maeoticus and Cornigerius ranges of the Ponto-Caspian onychopod species bicornis. Recent invasions of C. pengoi, E. anonyx in native and invaded habitats, indicates that they and C. maeoticus into the Baltic Sea can be are potentially able to form populations in a wide attributed to the climate change, facilitating range of inland and coastal water ecosystems in invasibility of the eastern Baltic Sea coastal temperate zones. Ponto-Caspian onychopods can ecosystems by the warm water Ponto-Caspian be considered as ‘‘high risk’’ invasive species, in species and intensive shipping activities via the terms of their potential for range expansion and Volga-Baltic waterway (European ‘‘northern impact on recipient ecosystems. invasion corridor’’). All three species can be considered to be established in pelagic communi- Keywords Invasive crustaceans Á Onychopoda Á ties of the eastern Gulf of Finland. Only one Ponto-Caspian species Á Invasion history Á onychopod species, C. pengoi has invaded the Risk assessment North American Great Lakes via an existing invasion corridor between the eastern Baltic and the Great Lakes. Invasive onychopods may Introduction The Ponto-Caspian region (the Black, Azov seas Guest editors: Elizabeth J. Cook and Paul F. Clark Invasive Crustacea and the Caspian Lake, including their basins) is serving as an important donor for invasive aquatic V. E. Panov (&) Á N. V. Rodionova Á alien species worldwide, specifically for European P. V. Bolshagin and North American inland waters, with shipping- Zoological Institute of the Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg related activities as a main vector of both inter- and 199034, Russia intracontinental dispersal (Mordukhai-Boltovskoi, e-mail: [email protected] 1964a; Panov et al., 1999; Ricciardi & MacIsaac, 2000; Reid & Orlova, 2002; Vanderploeg et al., E. A. Bychek Institute of Ecology of the Volga River Basin, RAS, 2002; Ketelaars, 2004; Galil et al., 2007). Within Togliatti 445003, Russia Europe, inland and coastal waters in the Baltic Sea 123 4 Hydrobiologia (2007) 590:3–14 and North Sea basins are the main recipient areas euryhalinity due to their evolution and, conse- for invasions of Ponto-Caspian species (Jazdzewski, quently, they are well adapted to invade new 1980; Bij de Vaate et al., 2002; Jazdzewski & environments, specifically C. pengoi, P. trigona and Konopacka, 2002; Ketelaars, 2004; Galil et al., C. maeoticus, which were found spreading outside 2007). At present, 22 fish and aquatic invertebrate their native range already in the mid 20th century species of Ponto-Caspian origin are successfully following the construction of reservoirs in the established in the Baltic Sea basin, comprising Dniepr, Don and Volga rivers (Mordukhai-Boltov- almost a third of all established non-indigenous skoi, 1979; Dumont, 2000). Moreover, Dumont aquatic species in the Baltic (Olenin et al., 2006). (2000) considered the origin of all known onycho- In the Laurentian Great Lakes during the last two pod species monophyletic; all 33 onychopod species decades, 8 Ponto-Caspian species have successfully were found to have originated in the Ponto-Caspian established themselves, causing significant ecolog- basin, with two freshwater and seven marine species ical impacts (Vanderploeg et al., 2002; Grigorovich possessing either a world-wide, or wide distribution et al., 2003a). Invasion success of Ponto-Caspian in the northern hemisphere as a result of natural species in inland and coastal waters outside their range expansion from the Ponto-Caspian area. native range can be attributed primarily to the Genetic studies of onychopods have revealed that euryhalinity of the Ponto-Caspian biota (Morduk- diversification of this group has occurred over the hai-Boltovskoi, 1964b; Dumont, 1998, 2000). past 10–20 million years and that disruptive selec- Intensive shipping activities in the Ponto-Cas- tion by predators is considered as the main driving pian region itself have also resulted in a number force in shaping the body plane diversity of onycho- of biological invasions in the Black, Azov seas pods (Cristescu & Hebert, 2002). and the Caspian, with severe economic and This group of obviously invasive species, how- ecological consequences for their ecosystems ever, has attracted serious attention of invasion (Shiganova et al., 2001; Grigorovich et al., 2002; biologists comparatively recently, after human- Grigorovich et al., 2003b; Dumont et al., 2004). mediated spread of the ‘‘freshwater Palearctic’’ As a consequence, the Ponto-Caspian region may Bythotrephes longimanus Leydig 1860 from east- serve as a secondary donor for these invasive ern Europe to North America and the ‘‘euryha- species via existing corridors, specifically to the line Ponto-Caspian’’ C. pengoi to the Baltic Sea Baltic and North seas. and North American Great Lakes (see reviews by Dispersal patterns of Ponto-Caspian species had Krylov et al., 2004 and Panov et al., 2004). been recently reviewed by Bij de Vaate et al. (2002) In the present paper, we have summarized and Ketelaars (2004). These reviews have further available information on invasion histories and developed the concept of inland European water- biology of Ponto-Caspian onychopods, which have ways as intracontinental invasion corridors from the expanded their native ranges in geographic Eur- Ponto-Caspian region to inland and coastal waters ope comparatively recently as a result of human- in the Baltic and North sea basins, an idea which was mediated invasions. This background information initially suggested for the Volga-Baltic inland water- is essential for developing approaches to risk way (Panov et al., 1999). These reviews, however, assessment of further spread and determining the have focused on benthic macroinvertebrate organ- ecological impacts of these invasive species. isms and comparatively low attention has been given to the invasive planktonic Ponto-Caspian predatory ‘‘cladocerans’’ (Crustacea: Branchiopoda: Onycho- Invasion history of Ponto-Caspian onychopods poda), which include 5 onychopod species found in the Black, Azov seas and the Caspian Lake, namely Cercopagis pengoi Cercopagis pengoi (Ostroumov, 1891), Evadne anonyx Sars, 1897, Podonevadne trigona (Sars, Cercopagis pengoi (Ostroumov, 1891) (Superor- 1897), Cornigerius maeoticus (Pengo, 1879) and der Cladocera: order Onychopoda: family Cerco- Cornigerius bicornis (Zernov, 1901) (Mordukhai- pagidae) is native to the Sea of Azov, Caspian Boltovskoi, 1964b; 1979). These species possess and Aral lakes (C. pengoi disappeared from the 123 Hydrobiologia (2007) 590:3–14 5 latter after an increase in salinity of the lake along et al., 2002; Krylov et al., 2004) (Fig. 1). In the with most other onychopods—see Rivier (1998)), Gulf of Finland, in areas of mass development of certain river estuaries of the Black Sea (Danube, C. pengoi (hundreds and thousands of ind. m3), Dnieper and Bug rivers) and the Gebenjinskoe fishing nets are often clogged by this species Lake in Bulgaria (Rivier, 1998). Between 1960– which results in severe economic losses for the 1975, after construction of the dams on the local coastal fishery (Panov et al., 1999). Don and Dnieper rivers in the Black Sea basin, In summer 1998, C. pengoi was found outside C. pengoi invaded the freshwater reservoirs of Eurasia for the first time, where it was recorded Kakhovka, Zaporozhsk, Kremenchug, Tsyml- snagged on sport fishing lines and in zooplankton yansk and Veselovsk (Krylov et al., 1999). Most samples in Lake Ontario in North America recently, in 2000–2005, C. pengoi was recorded (MacIsaac et al., 1999; Barbiero & Tuchman, in zooplankton samples from the Volga River 2000). Most likely, this is a result of secondary reservoirs; Volgograd, Saratov and Kuibyshev introduction by ships ballast water from the (Eugene A. Bychek unpubl.) (Fig. 1). eastern Baltic via an existing invasion corridor, In 1992, C. pengoi was first found outside the identified in case of Bythotrephes longimanus Ponto-Caspian basin in the Baltic Sea area (Gulf invasion by Berg et al. (2002). A recent genetic of Riga and Gulf of Finland), possibly as a result study by Cristescu et al. (2001) demonstrated that of the discharge of ballast water (Ojaveer & the population of C. pengoi in the North Amer- Lumberg, 1995; Ojaveer et al., 2000). After these ican Great Lakes is most likely to have originated first records, C. pengoi was found in the Neva from the Baltic Sea source population, namely the River estuary in 1995, already at high densities Neva Estuary (eastern Gulf of Finland). From and has since become a common zooplankton Lake Ontario, C. pengoi has spread in only a few species in the eastern Gulf of Finland (Panov, years to Lake Michigan, western Lake Erie and 1996; Avinsky, 1997; Krylov et al., 1999; Panov some adjacent inland lakes (Charlebois et al.,