Aquatic Invasions (2011) Volume 6, Supplement 1: S147–S152 doi: 10.3391/ai.2011.6.S1.033 Open Access

© 2011 The Author(s). Journal compilation © 2011 REABIC

Aquatic Invasions Records

The invasive freshwater medusa sowerbii Lankester, 1880 (: ) in Israel

Avital Gasith1, Sarig Gafny2, Yaron Hershkovitz1, Hava Goldstein3 and Bella S. Galil4* 1Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel 2School for Marine Sciences, Ruppin Academic Center, Michmoret, Israel 3Israel Nature and Parks Authority, Megiddo National Park, 19230, Israel 4National Institute of Oceanography, Israel Oceanographic & Limnological Research, POB 8030, Haifa 31080, Israel E-mail: [email protected] (AG), [email protected] (SG), [email protected] (YH), [email protected] (HG), [email protected] (BSG) *Corresponding author

Received: 17 September 2011 / Accepted: 20 October 2011 / Published online: 27 October 2011

Abstract

The freshwater , native to China, has been introduced to lentic and lotic habitats in artificial and natural bodies of water, in subtropical to temperate regions worldwide. In the Middle East it has been recorded from an artificial lake in the Nile Delta, Egypt, a recreational lake in Iraq, a reservoir and a dammed lake in Turkey. The first record in Israel dates back half a century – to an aquarium at the Hebrew University in Jerusalem. Since 2003 medusae of C. sowerbii have been observed in a perennial stream flowing into Sea of Galilee – Israel’s principal freshwater storage and supply reservoir. The possible impacts of a substantial bloom are discussed. Key words: Craspedacusta sowerbii, freshwater jellyfish, invasive , Middle East, Israel

Introduction However, our knowledge of its occurrence in the Middle East is limited to four records (Figure 1, The freshwater jellyfish Craspedacusta sowerbii Appendix 1). Dumont (2009) reported that a Lankester, 1880, native to China, has colonized 1956 record (Elster et al. 1960) of “a brief mass since the end of the 19th century water bodies in occurrence of medusae in the Nozha subtropical to temperate regions worldwide hydrodrome”, near Lake Mariut, Alexandria, (Kramp 1950; Dumont 1994). It is frequently Egypt, previously ascribed to Limnocnida, may found in disturbed or artificial bodies of water have been in fact C. sowerbii. Saadalla (2006) e.g. quarry ponds and gravel pits, reservoirs, recorded its presence in June-September 2002 in aquaria and even wastewater treatment facilities, an artificial recreational lake north of Baghdad, in addition to natural lentic and lotic habitats Iraq. In 1999 it was found in the Topcam (Tattersall 1933; Augustin et al. 1987; Fritz Reservoir in the Büyük Menderes River Basin in 2007). Its chitin-covered drought resistant SW Turkey, and in August 2008 in the Kralkizi resting stage enables it to withstand long periods Dam Lake in SE Turkey (Balik et al 2001; of food shortage and tolerate extreme Bekleyen et al 2011). environmental conditions, as well as serve as a In this paper we report the presence of an convenient life-stage for anthropogenic transport established population of Craspedacusta (Jankowski 2001). The species reproduces sowerbii from one of the perennial streams asexually, via a budding and a motile flowing into Lake Kinneret, Israel. frustule, and produces sexually reproducing free swimming medusae, which bud off from the Study area polyp (Reisinger 1957). A considerable number of reports on new Lake Kinneret (Sea of Galilee), in the northern C. sowerbii occurrences have been published in part of the Jordan Rift Valley, is a warm the past twenty years, greatly increasing our monomictic lake, stratified from mid-May to knowledge of the species spatial extent. November, with plankton restricted to the

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Figure 1. Distribution records of Craspedacusta sowerbii Lankester, 1880 in the Middle East, shown on Google map. Numbers corresponding to sites in Annex1.

Figure 2. Iris pond, Zavitan stream, 12 September 2011. Photograph Sarig Gafny.

Figure 3. Craspedacusta sowerbii Lankester, 1880. A specimen collected in the Iris pond, Zavitan stream, 12 September 2011. Photograph Liron Goren and Yaron Hershkovitz.

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epilimnic and metalimnic layers. The lake plays a vital role in Israel’s freshwater balance, Table 1. Records of invertebrates collected in the Iris pond, serving as the principal storage and supply Zavitan stream, 12 September 2011 (Sarig Gafny). reservoir (Serruya 1978). The lake surface is 166 Relative Taxonomic km², its average volume 4100 Mm³ (million Taxon abundance group cubic meters), of which ~300 Mm³ are used (%) N=698 annually for drinking and irrigation (Rimmer - Oligochaeta Tubificidae 1.6 2009). The salinity (190–280 ppm Cl ) is higher Copepoda Cyclops sp. 28.7 than the salinity of the streams in the lake’s Copepoda Arctodiaptomus sp. 12.8 catchment area (20–30 ppm Cl-). Zavitan stream Cladocera sp. 25.8 is a tributary of the Meshushim stream, one of five perennial streams flowing into Lake Ostracoda sp. 1 1.7 Kinneret. The streams cut deep ravines through Ostracoda sp. 2 0.9 the basalt rock, forming a series of waterfalls Isopoda Asellus sp. 0.7 and ponds used as popular swimming holes. One Hydracarina sp. 1 3.4 of these sites is the Iris pond (32°59′58.50″N Hydracarina sp. 2 0.1 35°44′22.20″E), a natural pool with a surface Ephemeroptera Caenis sp. 2.6 area of 300 m² and a maximal depth of 3 m Ephemeroptera Cloeon dipterum 1.7 (Figure 2). In mid September 2011 the surface Notonectidae Notonecta maculata 0.1 water temperature at the Iris pond was 25°C, Corixidae Micronecta scutellaris 2.3 salinity 0.2 psu, D.O. concentration 8.6 mg/l Gerridae Gerris paludum 0.6 (102% saturation) and Secchi transparency 84 Zygoptera Ischnura elegans 0.3 cm (greenish coloration). The results of the Anisoptera Brachythemis sp. 0.3 plankton and macroinvertebrates analysis are Anisoptera Crocothemis erythrea 1.1 given in Table 1. Anisoptera Orthetrum sp. 0.4 Coleoptera Hydrochus sp. 0.1 History of Craspedacusta sowerbii in the region Tricoptera Ecnomus sp. 0.6 Chironominae Chironomus sp. 12.6 A photograph of a polyp of Craspedacusta Tanypodiinae Tanypus sp. 1.3 sowerbii (as Calpasoma dactyloptera) found in a Ceratopogonidae 0.1 freshwater aquarium at the Department of Psychodidae 0.1 Zoology, Hebrew University of Jerusalem, was the first record of the species in Israel (Rahat 1961, Figure 1). These polyps were propagated, cultured and used for studies on atentacular During the summer months of 2003, 2006, (‘Microhydra’) and tentacular (‘Calpasoma’) 2009 medusae of C. sowerbii were observed in polyps at the Hebrew University of Jerusalem ponds along the Zavitan and Meshushim streams. (Spira 1963; Rahat and Campbell 1974). On October 4th 2004, a specimen was collected Hydranth-type ‘Calpasoma’ is considered a at the Iris pond, Zavitan, and deposited in the polyp form of C. sowerbii, though molecular National Collections at Tel Aviv University studies are required for substantiation (TAU CO 32351). On August 21st 2009 medusae (Jankowski 2001). were photographed at the same location, and on In 1994 polyps and medusae of C. sowerbii September 28th 2009 a single specimen was were discovered in a freshwater aquarium at the collected from the pond (TAU CO 35310). In the laboratory of the senior author (AG), Department summer of 2010 (August – October) that pond of Zoology, Tel Aviv University. The aquarium was surveyed several times and no medusae were was used to rear sponges collected on cobbles in found. However, during August and September Lake Kinneret littoral zone (Dembo 1996). There 2011, C. sowerbii medusae were again reported were no further records of the species from Lake in the Iris pond. In September 12th 2011 Kinneret in subsequent routine plankton specimens were collected at the Iris pond by one sampling (T. Zohary, head of the Kinneret of the authors (SG) (Figure 3), but a survey of Limnological Laboratory, Israel Oceanographic other sites in the Zavitan and in Meshushim and Limnological Research, pers. comm.). revealed no specimens.

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Discussion adult (Davis 1955; Jankowski and Ratte 2002; Jankowski 2004; Jankowski et al. The numerous records of C. sowerbii in aquaria 2005; Smith and Alexander 2008). Thus, while suggest that 'escape' from aquaria is an important blooms of C. sowerbii are infrequent, they may human-mediated vector (Stadel 1961; Duggan significantly impact aquatic food webs: a related 2010). Parent (1982) proposed that the American shift in the composition of the algal grazers may waterweed, Elodea canadensis (Michaux, 1803), result in higher algal biomass with cascading a common aquarium plant, may have been a effects on primary productivity and dissolved vehicle for Craspedacusta transport, with a time oxygen (Smith and Alexander 2008). lag of ca 50 years to establishment in the natural It has been suggested that C. sowerbii blooms environment. Indeed, C. sowerbii was first may be associated with rising temperatures or recorded in Israel from an aquarium used to raise increased nutrient inputs (Rayner 1988; the axolotl, Ambystoma mexicanum (Shaw & Boothroyd et al. 2002). Were Lake Kinneret to Nodder, 1798), and the polyp was attached to experience a substantial bloom of C. sowerbii, its stems of E. canadensis (Rahat 1961). The author ecosystem could be significantly altered through hastened to distance himself from the direct (predation) and indirect (incidental introduction: “Attempts to trace the origin of mortality) effects. Cyclopoid copepods dominate these polyps to that of the plants or Amphibia the zooplankton in Lake Kinneret, followed by present in the aquaria, proved unsuccessful. Thus cladocerans and rotifers (Gophen 1978; Pinel- neither of these two species of polyps could be Alloul et al. 2004). Predation by C. sowerbii may found in the aquaria that provided the stock of depress abundances of the bosminids and plants and Amphibia for the aquaria examined by cyclopoid copepods, which constitute the diet of us.”(Rahat 1961: 172). Yet, the foreign origin of the numerically dominant fish, the endemic both its aquarium mates provides an interesting cyprinid, Kinneret bleak, Acanthobrama clue to the possible vector. Dumont (1994) terraesanctae Steinitz, 1952. proposed that ornithochory or aerial dispersal of the species’ drought-resistant resting stages may Acknowledgements serve as means of upstream and inter-valley dispersal. We are deeply grateful to our colleagues - Gal Dembo, Eldad More than 50 years have passed since Elron, Matan Golan, Lior and Michael Gur, Shlomo Horowitz, Sharone Levi, Paula Play, Yahel Porat, Liora Shaltiel - for sharing C. sowerbii was first recorded in Israel, but its with us their observations and for giving us access to specimens distribution seems to be restricted to few lentic of C. sowerbii they collected. Liron Goren photographed the 2011 habitats in one stream in the catchment area of specimens. We thank Henk Mienis for his remarks on an earlier Lake Kinneret, where relatively low abundances version of the manuscript. The research leading to these results has received funding from the European Community’s Seventh of its medusae were recorded in late summer Framework Programme (FP7/2007-2013) for the projects Vectors (August–October). Although the species is a of Change in Oceans and Seas Marine Life, Impact on Economic successful invader world-wide, its occurrence Sectors (VECTORS) and Options for Delivering Ecosystem- may be restricted by habitat conditions such as Based Marine Management (ODEMM) (BSG). water temperature, flow velocity and specific food sources (e.g. eutrophic ponds, Jankowski References 2001). Augustin H, Foissner W, Adam H (1987) A sewage plant as a Little is known about the trophic interactions remarkable new habitat of the fresh-water polyp of zooplanktivorous freshwater hydromedusae Craspedacusta sowerbii (Hydrozoa: Coelenterata). and their role in aquatic food webs. Both polyps Limnologica 18: 225–226 and medusae of Craspedacusta sowerbii are Balik S, Ustaoglu MR, Ozbek M (2001) A new locality for the freshwater jellyfish Craspedacusta sowerbii Lankester, zooplanktivorous, and their prey is often the 1880 in Turkey. 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Appendix 1. Records of Craspedacusta sowerbii Lankester, 1880 in the Middle East. Site Record coordinates No. Site name Habitat type Location Record date Reference (Map Latitude,°N Longitude,°E Ref.) Thawra artificial 1 Baghdad, Iraq 33°21'21.36" 44°26'22.10" ix 2002 Saadalla 2006 Park lake Kralkizi artificial Anatolia, 2 38°21' 39°35' viii 2008 Bekleyen et al. 2011 Dam Lake lake Turkey Topçam artificial Aydin, 3 37°41' 28°00' vi 1999 - vi 2000 Balik et al. 2001 Reservoir reservoir Turkey Nozha artificial Alexandria, Elster et al. 1960 4 31°11'21.96" 29°58'35.66" vi 1956 hydrodrome lake Egypt fide Dumont 2009 Lake 5 natural lake Israel 32°45' 35°35' 1994 Dembo 1996 Kinneret Iris pond, natural 2003, 2004, 2006, Gasith et al. (present 6 Zavitan Israel 32°59'58.50" 35°44'22.20" pond 2009, viii - x 2011 paper) stream

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