The invasive freshwater medusa Craspedacusta sowerbii Lankester

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
Aquatic Invasions Records
The invasive freshwater medusa Craspedacusta sowerbii Lankester, 1880
(Hydrozoa: Olindiidae) in Israel
Avital Gasith 1, Sarig Gafny 2 , Yaron Hershkovitz 1, Hava Goldstein 3 and Bella S. Galil 4*
1
Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel
School for Marine Sciences, Ruppin Academic Center, Michmoret, Israel
3
Israel Nature and Parks Authority, Megiddo National Park, 19230, Israel
4
National Institute of Oceanography, Israel Oceanographic & Limnological Research, POB 8030, Haifa 31080, Israel
E-mail: A v i t a l G @ t a u e x . t a u . a c . i l ( A G ) , s a r i g @ r u p p i n . a c . i l ( S G ) , Y a r o n H e @ t a u e x . t a u . a c . i l ( Y H ) ,
[email protected] (HG), [email protected] (BSG)
2
*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
S147
A. Gasith et al.
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.
S148
Craspedacusta sowerbii in Israel
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
0.3
Zygoptera
Ischnura elegans
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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A. Gasith et al.
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, microcosm experiments and observational evidence
suggest a decrease in abundances of nauplii and
S150
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; PinelAlloul 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 EcosystemBased 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
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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A. Gasith et al.
Appendix 1. Records of Craspedacusta sowerbii Lankester, 1880 in the Middle East.
Site
No.
(Map
Ref.)
1
2
3
4
5
6
S152
Record coordinates
Site name
Thawra
Park
Kralkizi
Dam Lake
Topçam
Reservoir
Nozha
hydrodrome
Lake
Kinneret
Iris pond,
Zavitan
stream
Habitat type
artificial
lake
artificial
lake
artificial
reservoir
artificial
lake
Location
Baghdad, Iraq
Anatolia,
Turkey
Aydin,
Turkey
Alexandria,
Egypt
Record date
Reference
Latitude,°N
Longitude,°E
33°21'21.36"
44°26'22.10"
ix 2002
Saadalla 2006
38°21'
39°35'
viii 2008
Bekleyen et al. 2011
37°41'
28°00'
vi 1999 - vi 2000
31°11'21.96"
29°58'35.66"
vi 1956
natural lake
Israel
32°45'
35°35'
1994
natural
pond
Israel
32°59'58.50"
35°44'22.20"
2003, 2004, 2006,
2009, viii - x 2011
Balik et al. 2001
Elster et al. 1960
fide Dumont 2009
Dembo 1996
Gasith et al. (present
paper)