Aquatic Invasions (2011) Volume 6, Supplement 1: S147–S152 doi: 10.3391/ai.2011.6.S1.033 © 2011 The Author(s). Journal compilation © 2011 REABIC

Open Access

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Aquatic Invasions Records

The invasive freshwater medusa Craspedacusta sowerbii Lankester, 1880 (Hydrozoa: Olindiidae) 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: A v i t a l G@ t a u ex . t a u .a c . i l (A G ) , s a r ig@ r u pp in .a c . i l (S G) , Ya r o n He@ t a u ex . t a u .a c . i l (YH ) , h a vag @npa .org . i l (HG ) , b e l la @ o cea n . or g . i l (BS G ) *Corresponding author

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

Abstract

The freshwater jellyfish Craspedacusta sowerbii, 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 species, Middle East, Israel

Introduction

The freshwater jellyfish Craspedacusta sowerbii Lankester, 1880, native to China, has colonized since the end of the 19th century water bodies in subtropical to temperate regions worldwide (Kramp 1950; Dumont 1994). It is frequently found in disturbed or artificial bodies of water e.g. quarry ponds and gravel pits, reservoirs, aquaria and even wastewater treatment facilities, in addition to natural lentic and lotic habitats (Tattersall 1933; Augustin et al. 1987; Fritz 2007). Its chitin-covered drought resistant resting stage enables it to withstand long periods of food shortage and tolerate extreme environmental conditions, as well as serve as a convenient life-stage for anthropogenic transport (Jankowski 2001). The species reproduces asexually, via a budding polyp and a motile frustule, and produces sexually reproducing free swimming medusae, which bud off from the polyp (Reisinger 1957).

A considerable number of reports on new C. sowerbii occurrences have been published in the past twenty years, greatly increasing our knowledge of the species spatial extent.

However, our knowledge of its occurrence in the Middle East is limited to four records (Figure 1, Appendix 1). Dumont (2009) reported that a 1956 record (Elster et al. 1960) of “a brief mass occurrence of medusae in the Nozha hydrodrome”, near Lake Mariut, Alexandria, Egypt, previously ascribed to Limnocnida, may have been in fact C. sowerbii. Saadalla (2006) recorded its presence in June-September 2002 in an artificial recreational lake north of Baghdad, Iraq. In 1999 it was found in the Topcam Reservoir in the Büyük Menderes River Basin in SW Turkey, and in August 2008 in the Kralkizi Dam Lake in SE Turkey (Balik et al 2001; Bekleyen et al 2011).

In this paper we report the presence of an established population of Craspedacusta sowerbii from one of the perennial streams flowing into Lake Kinneret, Israel.

Study area

Lake Kinneret (Sea of Galilee), in the northern part of the Jordan Rift Valley, is a warm monomictic lake, stratified from mid-May to 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, serving as the principal storage and supply reservoir (Serruya 1978). The lake surface is 166 km², its average volume 4100 Mm³ (million cubic meters), of which ~300 Mm³ are used annually for drinking and irrigation (Rimmer 2009). The salinity (190–280 ppm Cl-) is higher than the salinity of the streams in the lake’s catchment area (20–30 ppm Cl-). Zavitan stream is a tributary of the Meshushim stream, one of five perennial streams flowing into Lake Kinneret. The streams cut deep ravines through the basalt rock, forming a series of waterfalls and ponds used as popular swimming holes. One of these sites is the Iris pond (32°59′58.50″N 35°44′22.20″E), a natural pool with a surface area of 300 m² and a maximal depth of 3 m (Figure 2). In mid September 2011 the surface water temperature at the Iris pond was 25°C, salinity 0.2 psu, D.O. concentration 8.6 mg/l (102% saturation) and Secchi transparency 84 cm (greenish coloration). The results of the plankton and macroinvertebrates analysis are given in Table 1.

History of Craspedacusta sowerbii in the region

A photograph of a polyp of Craspedacusta sowerbii (as Calpasoma dactyloptera) found in a freshwater aquarium at the Department of 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 (‘Microhydra’) and tentacular (‘Calpasoma’) polyps at the Hebrew University of Jerusalem (Spira 1963; Rahat and Campbell 1974). Hydranth-type ‘Calpasoma’ is considered a polyp form of C. sowerbii, though molecular studies are required for substantiation (Jankowski 2001).

In 1994 polyps and medusae of C. sowerbii were discovered in a freshwater aquarium at the laboratory of the senior author (AG), Department of Zoology, Tel Aviv University. The aquarium was used to rear sponges collected on cobbles in Lake Kinneret littoral zone (Dembo 1996). There were no further records of the species from Lake Kinneret in subsequent routine plankton sampling (T. Zohary, head of the Kinneret Limnological Laboratory, Israel Oceanographic and Limnological Research, pers. comm.).

Table 1. Records of invertebrates collected in the Iris pond, Zavitan stream, 12 September 2011 (Sarig Gafny).

Taxonomic group Taxon

Relative abundance (%) N=698

Oligochaeta Tubificidae 1.6 Copepoda Cyclops sp. 28.7 Copepoda Arctodiaptomus sp. 12.8 Cladocera Daphnia sp. 25.8 Ostracoda sp. 1 1.7 Ostracoda sp. 2 0.9 Isopoda Asellus sp. 0.7 Hydracarina sp. 1 3.4 Hydracarina sp. 2 0.1 Ephemeroptera Caenis sp. 2.6 Ephemeroptera Cloeon dipterum 1.7 Notonectidae Notonecta maculata 0.1 Corixidae Micronecta scutellaris 2.3 Gerridae Gerris paludum 0.6 Zygoptera Ischnura elegans 0.3 Anisoptera Brachythemis sp. 0.3 Anisoptera Crocothemis erythrea 1.1 Anisoptera Orthetrum sp. 0.4 Coleoptera Hydrochus sp. 0.1 Tricoptera Ecnomus sp. 0.6 Chironominae Chironomus sp. 12.6 Tanypodiinae Tanypus sp. 1.3 Ceratopogonidae 0.1 Psychodidae 0.1

During the summer months of 2003, 2006, 2009 medusae of C. sowerbii were observed in ponds along the Zavitan and Meshushim streams. On October 4th 2004, a specimen was collected at the Iris pond, Zavitan, and deposited in the National Collections at Tel Aviv University (TAU CO 32351). On August 21st 2009 medusae were photographed at the same location, and on September 28th 2009 a single specimen was collected from the pond (TAU CO 35310). In the summer of 2010 (August – October) that pond was surveyed several times and no medusae were found. However, during August and September 2011, C. sowerbii medusae were again reported in the Iris pond. In September 12th 2011 specimens were collected at the Iris pond by one of the authors (SG) (Figure 3), but a survey of other sites in the Zavitan and in Meshushim revealed no specimens.

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Discussion

The numerous records of C. sowerbii in aquaria suggest that 'escape' from aquaria is an important human-mediated vector (Stadel 1961; Duggan 2010). Parent (1982) proposed that the American waterweed, Elodea canadensis (Michaux, 1803), a common aquarium plant, may have been a vehicle for Craspedacusta transport, with a time lag of ca 50 years to establishment in the natural environment. Indeed, C. sowerbii was first recorded in Israel from an aquarium used to raise the axolotl, Ambystoma mexicanum (Shaw & Nodder, 1798), and the polyp was attached to stems of E. canadensis (Rahat 1961). The author hastened to distance himself from the introduction: “Attempts to trace the origin of these polyps to that of the plants or Amphibia present in the aquaria, proved unsuccessful. Thus neither of these two species of polyps could be found in the aquaria that provided the stock of plants and Amphibia for the aquaria examined by us.”(Rahat 1961: 172). Yet, the foreign origin of both its aquarium mates provides an interesting clue to the possible vector. Dumont (1994) proposed that ornithochory or aerial dispersal of the species’ drought-resistant resting stages may serve as means of upstream and inter-valley dispersal.

More than 50 years have passed since C. sowerbii was first recorded in Israel, but its distribution seems to be restricted to few lentic habitats in one stream in the catchment area of Lake Kinneret, where relatively low abundances of its medusae were recorded in late summer (August–October). Although the species is a successful invader world-wide, its occurrence may be restricted by habitat conditions such as water temperature, flow velocity and specific food sources (e.g. eutrophic ponds, Jankowski 2001).

Little is known about the trophic interactions of zooplanktivorous freshwater hydromedusae and their role in aquatic food webs. Both polyps and medusae of Craspedacusta sowerbii are zooplanktivorous, and their prey is often the pivotal link between primary producers and higher trophic levels. It has been proposed that though its predation rates are too small to cause zooplankton population declines, the medusae could, if abundant, restructure zooplankton composition (Dodson and Cooper 1983; Spadinger and Maier 1999). However, micro-cosm experiments and observational evidence suggest a decrease in abundances of nauplii and

adult copepods (Davis 1955; Jankowski and Ratte 2002; Jankowski 2004; Jankowski et al. 2005; Smith and Alexander 2008). Thus, while blooms of C. sowerbii are infrequent, they may significantly impact aquatic food webs: a related shift in the composition of the algal grazers may result in higher algal biomass with cascading effects on primary productivity and dissolved oxygen (Smith and Alexander 2008).

It has been suggested that C. sowerbii blooms may be associated with rising temperatures or increased nutrient inputs (Rayner 1988; Boothroyd et al. 2002). Were Lake Kinneret to experience a substantial bloom of C. sowerbii, its ecosystem could be significantly altered through direct (predation) and indirect (incidental mortality) effects. Cyclopoid copepods dominate the zooplankton in Lake Kinneret, followed by cladocerans and rotifers (Gophen 1978; Pinel-Alloul et al. 2004). Predation by C. sowerbii may depress abundances of the bosminids and cyclopoid copepods, which constitute the diet of the numerically dominant fish, the endemic cyprinid, Kinneret bleak, Acanthobrama terraesanctae Steinitz, 1952.

Acknowledgements

We are deeply grateful to our colleagues - Gal Dembo, Eldad Elron, Matan Golan, Lior and Michael Gur, Shlomo Horowitz, Sharone Levi, Paula Play, Yahel Porat, Liora Shaltiel - for sharing with us their observations and for giving us access to specimens of C. sowerbii they collected. Liron Goren photographed the 2011 specimens. We thank Henk Mienis for his remarks on an earlier version of the manuscript. The research leading to these results has received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) for the projects Vectors of Change in Oceans and Seas Marine Life, Impact on Economic Sectors (VECTORS) and Options for Delivering Ecosystem-Based Marine Management (ODEMM) (BSG).

References

Augustin H, Foissner W, Adam H (1987) A sewage plant as a remarkable new habitat of the fresh-water polyp Craspedacusta sowerbii (Hydrozoa: Coelenterata). Limnologica 18: 225–226

Balik S, Ustaoglu MR, Ozbek M (2001) A new locality for the freshwater jellyfish Craspedacusta sowerbii Lankester, 1880 in Turkey. Zoology in the Middle East 22: 133–134

Bekleyen A, Varol M, Gokot B (2011) A new record of the freshwater jellyfish Craspedacusta sowerbii Lankester, 1880 (Hydrozoa) in Southeastern Anatolia (Turkey). Chinese Journal of Oceanology and Limnology 29(2): 366–368, http://dx.doi.org/10.1007/s00343-011-0047-1

Boothroyd I KG, Etheredge MK, Green JD (2002) Spatial distribution, size structure, and prey of Craspedacusta sowerbii in a shallow New Zealand lake. Hydrobiologia 468: 23–32, http://dx.doi.org/10.1023/A:1015206320300

Craspedacusta sowerbii in Israel

S151

Davis CC (1955) Notes on the food of Craspedacusta sowerbii in Crystal Lake, Ravenna, Ohio. Ecology 36: 364–366, http://dx.doi.org/10.2307/1933253

Dembo GM (1996) Kinneret sponges: characteristics and ecology of sponges in a warm lake. Master's Thesis, Tel Aviv University, Israel (in Hebrew, unpublished).

Dodson SI, Cooper SD (1983) Trophic relationships of the freshwater jellyfish Craspedacusta sowerbyi Lankester 1880. Limnology and Oceanography 28: 345–351

Duggan IC (2010) The freshwater aquarium trade as a vector for incidental invertebrate fauna. Biological invasions 12: 3757–3770, http://dx.doi.org/10.1007/s10530-010-9768-x

Dumont HJ (1994) The distribution and ecology of the fresh- and brackish water medusae of the world. Hydrobiologia 272: 1–12, http://dx.doi.org/10.1007/BF00006508

Dumont HJ (2009) The Cnidaria of the Nile Basin. In: Dumont HJ (ed), The Nile: Origin, environments, limnology and human use. Springer, 495-498

Elster HJ, Hawary M, Schroeder R, Schwoerbel I (1960) Population dynamics of zooplankton in the Nozha hydrodrome near Alexandria. Alexandria Institute of Hydrobiology Notes and Memoires 50: 1–27

Fritz GB, Schill RO, Pfannkuchen M, Brummer F (2007) The freshwater jellyfish Craspedacusta sowerbii Lankester, 1880 (Limnomedusa: Olindiidae) in Germany, with a brief note on its nomenclature Journal of Limnology 66(1): 54–59

Gophen M (1978) Zooplankton. In: Serruya C (ed), Lake Kinneret Monographiae Biologicae 32: 297–311. Junk publishers, The Hague

Jankowski T (2001) The freshwater medusae of the world – A taxonomic and systematic literature study with some remarks on the inland water jellyfish. Hydrobiologia 462: 91–113, http://dx.doi.org/10.1023/A:1013126015171

Jankowski T (2004) Predation of freshwater jellyfish on Bosmina: the consequences for population dynamics, body size, and morphology. Hydrobiologia 530/531: 521–528, http://dx.doi.org/10.1007/s10750-004-2648-6

Jankowski T, Ratte HT (2002) On the influence of the freshwater jellyfish Craspedacusta sowerbii on the zooplankton community. Internationale Vereinigung fuer Theoretische und Angewandte Limnologie Verhandlungen 27(6): 3287–3290

Jankowski T, Strauss T, Ratte HT (2005) Trophic interactions of the freshwater jellyfish Craspedacusta sowerbii. Journal of Plankton Research 27: 811–823, http://dx.doi.org/10.10 93/plankt/fbi055

Kramp PL (1950) Freshwater medusae in China. Proceedings of the Zoological Society of London 120: 165–184, http://dx. doi.org/10.1111/j.1096-3642.1950.tb01469.x

Parent GH (1982) Une page d'histoire des sciences contemporaines: un siecle d'observations sur la meduse d'eau douce Craspedacusta sowerbyi Lank. Bulletin mensuel de la société Linnéenne de Lyon 51: 47–63

Pinel-Alloul B, Méthot G, Malinsky-Rushansky NZ (2004) A short-term study of vertical and horizontal distribution of zooplankton during thermal stratification in Lake Kinneret, Israel. Hydrobiologia 526: 85–98, http://dx.doi.org/10.1023/B: HYDR.0000041611.71680.fc

Rahat M (1961) Two polyps of Limnotrachylina from Israel. Bulletin of the Research Council, Israel 10B: 171–172

Rahat M, Campbell RD (1974) Three forms of the tentacled and non-tentacled fresh-water coelenterate polyp genera Craspedacusta and Calpasoma. Transactions of the American Microscopic Society 93: 235–241, http://dx.doi. org/10.2307/3225292

Rayner NA (1988) First record of Craspedacusta sowerbyi Lankester (Cnidaria: Limnomedusae) from Africa. Hydrobiologia 162: 73–77, http://dx.doi.org/10.1007/BF000 14334

Reisinger E (1957) Zur Entwicklungsgeschichte und Entwicklungsmechanik von Craspedacusta (Hydrozoa, Limnotrachylina). Zeitschrift für Morphologie und Ökologie der Tiere 45: 656–698, http://dx.doi.org/10.1007/BF00399599

Rimmer A (2009) System hydrology models for managing the salinity of Lake Kinneret, Israel. The Role of Hydrology in Water Resources Management, Proceedings of a workshop held in Capri, Italy, October 2008. International Association of Hydrological Sciences (IAHS) press, 327: 1–13

Saadalla HAA (2006) First record of the freshwater medusa Craspedacusta sp (Cnidaria, Hydrozoa) from an artificial lake in Baghdad, Iraq. Zoology in the Middle East 37: 107–110

Serruya C (1978) Introduction. In: Serruya C (ed), Lake Kinneret Monographiae Biologicae 32: 1–4. Junk publishers, The Hague

Smith AS, Alexander Jr. JE (2008) Potential effects of the freshwater jellyfish Craspedacusta sowerbii on zooplankton community abundance. Journal of Plankton Research 30(12): 1323–1327, http://dx.doi.org/10.1093/plankt/fbn093

Spadinger R, Maier G (1999) Prey selection and diel feeding of the freshwater jellyfish, Craspedacusta sowerbyi. Freshwater Biology 41: 567–573, http://dx.doi.org/10.1046/j.1365-2427. 1999.00408.x

Spira M (1963) The biology, morphology, and histology of Calpasoma dactyloptera (Trachylina). Master's Thesis, Hebrew University of Jerusalem, Israel (in Hebrew, unpublished)

Stadel O (1961) Neuere Kenntniss tiber die kologie und Verbreitung der Süsswassermeduse Craspedacusta sowerbyi. Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg NF 5: 157–192

Tattersall WM (1933) Occurrence of Craspedacusta sowerbyi Lankester in Monmouthshire. Nature 132: 570, http://dx.doi. org/10.1038/132570a0

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Appendix 1. Records of Craspedacusta sowerbii Lankester, 1880 in the Middle East.

Site No.

(Map Ref.)

Site name Habitat type Location Record coordinates

Record date Reference Latitude,°N Longitude,°E

1 Thawra Park artificial lake Baghdad, Iraq 33°21'21.36" 44°26'22.10" ix 2002 Saadalla 2006

2 Kralkizi Dam Lake artificial lake

Anatolia, Turkey 38°21' 39°35' viii 2008 Bekleyen et al. 2011

3 Topçam Reservoir artificial reservoir

Aydin, Turkey 37°41' 28°00' vi 1999 - vi 2000 Balik et al. 2001

4 Nozha hydrodrome artificial lake

Alexandria, Egypt 31°11'21.96" 29°58'35.66" vi 1956

Elster et al. 1960 fide Dumont 2009

5 Lake Kinneret natural lake Israel 32°45' 35°35' 1994 Dembo 1996

6 Iris pond, Zavitan stream

natural pond Israel 32°59'58.50" 35°44'22.20"

2003, 2004, 2006, 2009, viii - x 2011

Gasith et al. (present paper)