THE FRESHWATER JELLYFISH CRASPEDACUSTA SOWERBII LANKESTER, 1880: AN OVERVIEW OF ITS DISTRIBUTION IN - FRANCE

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THE FRESHWATER JELLYFISH CRASPEDACUSTA SOWERBII LANKESTER, 1880: AN OVERVIEW OF ITS DISTRIBUTION IN - FRANCE
Vie et milieu - Life and environment, 2019, 69 (4): 201-213

                The freshwater jellyfish Craspedacusta sowerbii
               Lankester, 1880: an overview of its distribution in
                                                           France

                                                    G. Marchessaux 1,4*, J. Gadreaud 2, B. Belloni 3,4
   1
       Université de Franche-Comté – Laboratoire Chrono-Environnement, UMR CNRS/UFC6249, F-25211 Montbéliard cedex, France
                                                           2
                                                             Aix Marseille Univ, Univ Avignon, CNRS, IRD, IMBE, Marseille, France
                                                   3
                                                     GIS Posidonie, Aix-Marseille University, OSU Pythéas, 13288 Marseille, France
                                                             4
                                                               See The Sea Production, 26 rue de Friedland, 13006 Marseille, France
                                                                      * Corresponding author: guillaume.gmarchessaux@gmail.com

                 INVASIVE JELLYFISH    ABSTRACT. – Over the last few decades, reports of the freshwater jellyfish Craspedacusta
          CONTINENTAL WATER BODIES
               SPATIAL DISTRIBUTION
                                       sowerbii have increased worldwide. This invasive alien species, native to China, has invaded
                                       France’s freshwater systems. The present article reports the following information regarding
                                       this jellyfish: (i) distribution across the French metropolitan territory, (ii) life cycle, physiology
                                       and reproductive mode, and (iii) ecology and impact. The main aim of this article is to establish
                                       an updated inventory of invaded areas in order to better understand how and why its occurrence
                                       is reported with increasing frequency in France. In the 1970s, only 36 sites for Craspedacusta
                                       sowerbii were identified. In our study, we observed a widespread distribution of these freshwa-
                                       ter jellyfishes in France: 123 sites. Craspedacusta sowerbii was mainly observed in closed eco-
                                       systems (ponds – temporary or permanent; basins): 38 ponds, 35 lakes, 14 water-filled quarries
                                       and 7 basins and a few in rivers and canals (29 stations).

INTRODUCTION                                                            its geographical distribution remains uncertain in France
                                                                        as there is a lack of information on its distribution in vari-
    Non-indigenous species constitute a major source of                 ous aquatic environments.
biological pollution, as some become invasive and have
a significant ecological and economic impact on the bio-                Introduction vectors of Craspedacusta sowerbii
diversity, the ecosystem functioning (e.g. competition,
predation) and human activities (e.g. fisheries, industrial                The main introduction vectors of the freshwater jel-
complex, tourism). Observed in fossil forms (Gant et al.                lyfish Craspedacusta sowerbii are through aquatic plants
1996) since the end of the 19th century, ­Craspedacusta                 and birds where the polyp form is attached (Howmiller &
sowerbii was observed in Europe, then in North Amer-                    Ludwig 1970, Duggan 2010). Moreover, it seems that the
ica and elsewhere. For more than 20 years, reports of                   artificialization of the river flow circulation – construction
Craspedacusta sowerbii have been increasing in Europe,                  of canals linking rivers – is conducive to the geographical
North America and Australia, with sightings in Finland,                 spread of C. sowerbii.
Sweden and Lithuania (2002), Poland (1999), Russia
                                                                           The freshwater jellyfish C. sowerbii originates from
(1949, 1994) and near Lake Baikal (Arov 2004). The
                                                                        East Asia (Didžiulis 2006, Parent 1982), but some authors
freshwater jellyfish C. sowerbii (Hydrozoa, Limnomedu-
                                                                        indicate native populations from South America (Prota-
sae, Olindiidae) was first observed and described in Lon-
                                                                        sov et al. 1981, Ludoski et al. 2004). The discovery of
don, in 1880, in the basins of the Royal Botanic Garden,
                                                                        freshwater jellyfish in the Yangtze River (China) in 1907
documented by William Sowerby. From the beginning of
the 20th century, there were increasing numbers of scien-               by Carle Sowerby suggests that this jellyfish is native to
tific publications listing Craspedacusta sowerbii Lank-                 Asia. The introduction vector of this species would cer-
ester, 1880 in French lakes and rivers (Germain 1934,                   tainly be the importation of aquatic plants such as the
Denis 1950, Goy 1971, Colin et al. 1995). Later, new                    water lily Victoria regia, imported into Europe by the bot-
sightings were reported in Finland, Lithuania and Canada                anist Aimé Bonpland in 1819. In 1849, V. regia was plant-
(Arbaciauskas & Lasutiene 2005, El Moussaoui & Beis-                    ed in the Royal Botanic Garden in London. In France,
ner 2017). Despite its occasional presence in the pelagic               Victoria regia was imported and planted in the basins of
phase and its limited impact, Craspedacusta is still inten-             the Lyon Botanical Garden in 1888, where C. sowerbii
sively studied worldwide, 130 years after its discovery: its            individuals were observed shortly afterwards (in 1891)
biology, life cycle and ecology are well known. However,                (Pelosse 1918).
THE FRESHWATER JELLYFISH CRASPEDACUSTA SOWERBII LANKESTER, 1880: AN OVERVIEW OF ITS DISTRIBUTION IN - FRANCE
202                                   G. MARCHESSAUX, J. GADREAUD, B. BELLONI

Morphology and life cycle of Craspedacusta sowerbii                 diameter of individuals varies between 9-10 mm (Colin
                                                                    & Delahaye 1995). Mature jellyfish release their gametes
   As observed in the Olindiidae hydrozoan family, the              in the water. After external fertilization, fertilized eggs
medusa form of Craspedacusta sowerbii has a slightly                are transformed into ciliated planula larvae, which attach
flattened hemisphere shape and shows a radial symme-                themselves to solid structures and metamorphosing on
try with gonads developing along each of the four radial            metamorphic conversion substrate into polyps and repro-
canals (Fig. 1). It has a large central stomach opening             ducing asexually and metamorphose on metamorphic
into a mouth composed of 4 lips. It is surrounded by 4              conversion substrate into polyps and reproduce asexually
long fleshy oral arms and up to 400 peripheral tentacles,           (Matthews 1966, Didžiulis 2006).
arranged in several lines to facilitate swimming and posi-             The environmental factors that induce the asexual or
tional stability. This small jellyfish does not exceed 20 mm        sexual reproduction of C. sowerbii are the temperature
in diameter and 4 g fresh weight (99 % water). Gadreaud             and the quantity of available food in the environment
et al. (2017) observed many morphological alterations in            (McClary 1959, 1961, 1964, Acker & Muscat 1976,
the related cnidarian Aurelia sp. and in another Oindiidae          Rayner 1988, Slobodkin & Bossert 1991, Boothroyd
species, Gonionemus vertens: 10 % of the population in              et al. 2002). Turquin (2010) undertook a survey of the
the Berre Lagoon (southern France) had altered symme-               knowledge regarding the factors that trigger the meta-
try: some individuals having five gonads and 40 tentacles           genesis of C. sowerbii (Fig. 3). The asexual budding of
unevenly distributed around the umbrella (Marchessaux et            frustules producing polyps does not appear to be tem-
al. 2017). Such alteration in body symmetry has not been            perature-dependent: the same production of frustules at
reported or observed yet in C   ­ raspedacusta but it would         12 °C, 20 °C, 25 °C, 28 °C and 33 °C (McClary 1959,
be interesting to see whether this species also shows mor-          1961, 1964), at the optimum temperature for the devel-
phological alterations.                                             opment (size and growth) of polyps frustules, would be
   The life cycle of Craspedacusta sowerbii has two                 up to 25 °C. Development of frustules into polyps was
reproductive phases (Fig. 2): an asexual phase (benthic             observed between 12 °C and 20 °C (Turquin 2010).
polyp stage) and a sexual phase (pelagic jellyfish phase).          Between 26 °C and 33 °C, the production of medusa buds
The complete life cycle from the egg to the pelagic free            by polyps was observed (McClary 1959, 1961, 1964) with
jellyfish lasts between 34 and 51 days (de Larambergue              high food concentration which stimulates this process
1945, Acker & Muscat 1976, Colin & Delahaye 1995,                   according to Acker & Muscat (1976). Under unfavorable
Wang et al. 2006, Didžiulis & ŻŽurek 2013). Asexual                 environmental conditions (low temperatures, little food),
reproduction is carried out by budding, where a polyp               resistant polyps called podocysts are observed. The podo-
(measuring 1-2 mm) will bud to give either (1) a new                cyst encysted forms can survive forty years of desiccation
attached polyp to form a colony, or (2) frustules that              (Bouillon 2000, Brancotte & Vincent 2002).
separate from the initial polyp and form a new colony,                 The sexual reproduction of the pelagic jellyfish trig-
or (3) immature jellyfish. The medusa bud will develop,             gered with a high quantity of food (Acker & Muscat 1976)
attached to the polyp, then will detach and swim in the             and a very short temperature range (28 °C and 29 °C) (Xu
open water once the metamorphosis is complete. The                  & Wang 2009) qualifies this species as a thermophilic
rest of its growth occurs in the pelagic phase, resulting in        stenotherm (Goy 1971). The environmental temperature
adults measuring up to 5 cm in diameter. Craspedacusa               also plays a role by keeping pelagic jellyfish in the water
sowerbii reaches the full mature jellyfish stage when the           column: jellyfish can swim in open water when the tem-

Fig 1. – Morphology of Craspedacusta. A: Picture of jellyfish © Jean-François Cart; B: Labelled diagram. Data taken from literature
(partially traced from Oka 1907).

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CRASPEDACUSTA SOWERBII NEW DISTRIBUTION MAP IN France                         203

                                                  Fig. 2.– Life cycle of Craspeda-
                                                  custa sowerbii. Modified and
                                                  based on a drawing in Lytle
                                                  (1982). (Photos: G Marches-
                                                  saux).

                 Vie Milieu, 2019, 69 (4)
THE FRESHWATER JELLYFISH CRASPEDACUSTA SOWERBII LANKESTER, 1880: AN OVERVIEW OF ITS DISTRIBUTION IN - FRANCE
204                                    G. MARCHESSAUX, J. GADREAUD, B. BELLONI

Fig. 3. – Temperature ranges for asexual and sexual reproduction of Craspedacusta sowerbii. Data taken from literature (Turquin 2010
and references included).

perature is above 14.5 °C, otherwise they sink to the bot-           Cooper 1983). The ad hoc nature of freshwater jellyfish
tom and retract into a ball (Thomas 1951).                           blooms does not appear to have a significant impact on
                                                                     the trophic functioning of invaded areas. On the other
Ecology and impact                                                   hand, in the case of a large bloom, 13 % of the copepod
                                                                     resource could be eaten or killed by C. sowerbii (Jankows-
    This species is distinguished by its global distribution         ki 2000). According to Dodson (1983), nearly 10 % of the
(Dumont 1994) in diverse habitats, ranging from small                cladocean population are ingested daily by freshwater
ponds to lakes. The dispersal of Craspedacusta sowerbii,             jellyfish. The high summer blooms of C. sowerbii could
like many other aquatic alien species, would mainly occur            have a significant impact on fish eggs consumed by the
through bird migration and importation of decorative                 jellyfish stage (Dumont 1994). Craspedacusta sowerbii is
aquatic plants and pet animals. Craspedacusta sowerbii               also preyed on by two fish species (Crassius sp., ­Lebistes
is able to thrive in various aquatic ecosystems with differ-         sp.) and two species of crayfish (Orconectes rusticus,
ent environmental conditions (Stefanelli 1948, Goy 1971,             Orconectes propinquis) but can cause necrosis on their
Rayner 1988, Arbačiauskas & Lesutienė 2005, Gophen                   fins (Dodson & Cooper 1983).
& Shealtiel 2012, El Moussaoui 2015). Proliferations of                 First observed in Lyon (France) in 1891 by M. Chiffot,
C. sowerbii are often massive and short in duration (Pen-            the range of geographical distribution of Craspedacusta
nak 1956, Matthews 1966, Acker & Muscat 1976, Dethier                sowerbii has increased. This geographical expansion
& Kalbermatter 1989, Arov 2004). According to Lund-                  remains the subject of considerable scientific debate. The
berg & Svensson (2003), the occurrence of C. ­sowerbii               main aim of this article is therefore to summarize the cur-
appears to be on the increase in fresh waters, mainly                rent distribution of the species in metropolitan French ter-
because of climate change: warmer and longer summers                 ritorial waters on the basis of scientific articles and popu-
would favour the proliferation of the jellyfish stage. How-          lar information and media reports.
ever, there is still no scientific evidence to confirm or
reject this hypothesis, or even to explain the recent spread
of this exotic species.                                              MATERIALS AND METHODS
    There are few studies on the diet of C. sowerbii in the
scientific literature. Bushnell & Porter (1967) and Lewis                Our study recorded only observations of this species in
et al. (2012) indicate that polyps of this freshwater jelly-         medusa phase in pelagic zones during summertime. The medu-
fish feed on a wide range of prey: nauplii larvae, rotifers          sa stage is the only one visible, the polyps being too small
(Brachionus sp., Asplanchna sp.), crustaceans (copep-                (~200 μm) to be visually identified. The analysis of the spatial
ods), nematodes and insects (Dodson & Cooper 1983,                   distribution of Craspedacusta sowerbii in France is based on
Spadinger 1999, Boothroyd et al. 2002, Jankowski et al.              bibliographical research in international scientific journals, and
2005, Smith & Alexander 2008). The pelagic jellyfish                 also local newspaper articles which have reported sightings of
stage feeds mainly on zooplankton (Spadinger & Maier                 this urticant jellyfish (Fig. 4). Keywords were used (in French or
1999, Smith & Alexander 2008, Figueroa & De los Rios                 English) on various platforms (Google Scholar; Web of Science;
2010) ranging in size from 0.1 mm to 3 mm (Dodson &                  Research Gate; Google; social networks such as Facebook,

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THE FRESHWATER JELLYFISH CRASPEDACUSTA SOWERBII LANKESTER, 1880: AN OVERVIEW OF ITS DISTRIBUTION IN - FRANCE
CRASPEDACUSTA SOWERBII NEW DISTRIBUTION MAP IN France                                              205

                                                                    Table I. – Observation sources for the distribution of Craspeda-
                                                                    custa sowerbii in France.
                                                                             Type or sources            Numbers of articles
                                                                                  Scientific articles           26
                                                                                      Press articles            17
                                                                                          Websites              14
                                                                                  Naturalist reports             9
                                                                                               Total            66

Fig. 4. – Research strategy to survey the distribution of Craspe-
dacusta sowerbii in France.

Twitter, YouTube; French media websites) since the 2000s to
find relevant documents on C. sowerbii: “freshwater jellyfish”,
“Craspedacusta sowerbii”, “Craspedacusta”, “freshwater
jellyfish France”, “Craspedacusta sowerbii France”. For the
popular media (radio, TV, newspapers), local media were iden-
tified per region (for example: France 3 Régions, La Nouvelle
République, France Bleue Radio, Sud Ouest, La Montagne, Le
Dauphiné, Ouest France, L’Alsace, La Dépêche, L’Yonne Répu-
blicaine, Le Progrès) and keywords were used to find articles on
Craspedacusta sowerbii. To ensure proper identification of the
species, the pictures in the articles were analyzed and consid-
ered compliant when there was confirmation by experts.
    The date, the type of site and localization were recorded. To
map the spatial distribution of C. sowerbii, the GPS coordinates
of each localization were identified and spatialized on QGIS
Lyon software.

RESULTS

   There are still increasing numbers of reports in the
local press. Generally one-off, sightings are reported by
fishermen, swimmers, divers and naturalists; in artificial
aquatic environments – quarries, basins, reservoirs, sew-
age treatment plants (Augustin et al. in Fritz et al. 2007) –
and in natural environments along the shores of lakes, in
the stagnant backwaters of rivers, in canals and standing
water in canal constructions. The vector of introduction is
by being attached to bird legs, fish or plant introductions,
public works machinery, and canals (Bouillon 2000,
Brancotte & Vincent 2002).                                          Fig. 5. – A: Distribution of the introduced freshwater jellyfish
   A total of 26 scientific articles referring to C. sowerbii       Craspedacusta sowerbii in France. Numbers represent sites as
were collected (Table I). In addition, 17 press articles and        reported in Table II; waterways and water bodies are in blue;
                                                                    B: Number of sites with Craspedacusta observed per region.
23 other sources – photo websites and naturalist reports
– were found. Since its first observation in Lyon in 1891,
the geographical distribution of C. sowerbii has increased          1970s. Nearly 50 years later, our study reports a total of
(Fig. 5A): Goy (1971) listed 36 stations in France in the           123 stations on the metropolitan French territory where

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THE FRESHWATER JELLYFISH CRASPEDACUSTA SOWERBII LANKESTER, 1880: AN OVERVIEW OF ITS DISTRIBUTION IN - FRANCE
206                                      G. MARCHESSAUX, J. GADREAUD, B. BELLONI

Table II. – Overview of the distribution of Craspedacusta sowerbii in France (literature survey).
                                                                                  Type of
 N°       Localization                 Region             Date       Site                                        Sources
                                                                                  sources
                                                                                Naturalist
  1   Abbaretz               Pays-de-la-Loire             2005       Lake                       Yésou et al. (2014)
                                                                                report
  2   Agen                   Nouvelle-Aquitaine             –        Pond       Website         Freshwater Jellyfish
                                                                                Scientific
  3   Aiguillon              Nouvelle-Aquitaine             –        Pond                       Granereau & Cahuzac (2013)
                                                                                article
                                                                                Scientific
  4   Aix-les-Bains          Auvergne-Rhône-Alpes         2005       Lake                       Balvay (2008)
                                                                                article
  5   Angers                 Pays-de-la-Loire             2010       Lake       Website         Photo website
                                                                                Scientific
  6   Annecy                 Auvergne-Rhône-Alpes         1962       Lake                       Balvay (1990)
                                                                                article
                             Bourgogne-Franche-
  7   Arceau                                              2016       Pond       Press article   France 3 Régions TV
                             Comté
  8   Argenton-sur-Creuse Centre-Val-de-Loire             2012       Pond       Website         Youtube
                                                                                Naturalist      Commission Nationale Environnement
  9   Arras                  Hauts-de-France              2009       Lake
                                                                                report          et Biologie Subaquatiques
                                                                                Naturalist      Muséum national d’Histoire naturelle
 10   Aubusson               Auvergne-Rhône-Alpes         2007       River
                                                                                report          [Ed]. 2003-2019
                             Provence-Alpes-Côte                                Scientific
 11   Avignon                                             1985       Pond                       Bailly et al. (1987)
                             d’Azur                                             article
 12   Avrillé-les-Ponceaux   Centre-Val-de-Loire          2013      Basin       Press article   La Nouvelle République Journal
                                                                                Naturalist      Revue Mensuelle des Naturalistes
 13   Bagneaux-sur-Loing     Île-de-France                1990       River
                                                                                report          Orléanais (1997)
                                                                                Scientific
 14   Bâle                   Grand-Est / Suisse           1932       Pond                       Grzymek (1975)
                                                                                article
                                                                                Naturalist      Muséum national d’Histoire naturelle
 15   Barraux                Auvergne-Rhône-Alpes           –        Pond
                                                                                report          [Ed]. 2003-2019
                                                                 Water-filled
 16   Beffes                 Centre-Val-de-Loire          2005                  Website         Photo website
                                                                  quarry
 17   Bernin                 Auvergne-Rhône-Alpes         2008       River      Website         Aqua portail
                                                                                Naturalist
 18   Biscarrosse            Nouvelle-Aquitaine           1977       Pond                       GEREA
                                                                                report
                                                                 Water-filled
 19   Bischheim              Grand-Est                    2019                  Website         Youtube
                                                                  quarry
                                                                                Scientific
 20   Bordeaux               Nouvelle-Aquitaine             –       Basin                       Granereau & Cahuzac (2013)
                                                                                article
                                                                                Naturalist
 21   Bouguenais             Pays-de-la-Loire             1986       Pond                       DRAE (1986)
                                                                                report
                             Bourgogne-Franche-                                 Scientific
 22   de Bourgogne                                        1950      Canal                       Denis (1950)
                             Comté                                              article
 23   Brégnier-Cordon        Auvergne-Rhône-Alpes         2003       River      Website         Aqua portail
                                                                                Scientific
 24   Briare                 Centre-Val-de-Loire            –       Canal                       Arvy (1972)
                                                                                article
 25   Brossac                Nouvelle-Aquitaine           2008       Pond       Website         Freshwater Jellyfish
                             Provence-Alpes-Côte                 Water-filled   Scientific
 26   Cannes                                              1970                                  Goy (1971)
                             d’Azur                               quarry        article
                                                                 Water-filled   Scientific
 27   Cannes-Ecluse          Ile-de-France                1962                                  Girard & Poplin (1970)
                                                                  quarry        article
                                                                                Scientific
 28   Captieux               Nouvelle-Aquitaine             –        Pond                       Granereau (2000)
                                                                                article
 29   Cerizay                Nouvelle-Aquitaine             –        Pond       Website         Photo website
                                                                 Water-filled   Naturalist
 30   Chalonnes-sur-Loire    Pays-de-la-Loire             1986                                  Yésou et al. (2014)
                                                                  quarry        report
                             Bourgogne-Franche-
 31   Champagney                                          2013       Lake       Press article   France Bleue Radio
                             Comté

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CRASPEDACUSTA SOWERBII NEW DISTRIBUTION MAP IN France                                                 207

Table II. – Continued.
                                                                               Type of
 N°         Localization              Region           Date      Site                                         Sources
                                                                               sources
                                                                             Naturalist      Revue Mensuelle des Naturalistes
 32   Château Landon       Île-de-France                –        Pond
                                                                             report          Orléanais (1997)
                                                                             Scientific
 33   Codolet              Auvergne-Rhône-Alpes        2008      River                       Bavard & Clémens (2008)
                                                                             article
                                                                             Naturalist      Revue Mensuelle des Naturalistes
 34   Couziers             Centre-Val-de-Loire         1981      Pond
                                                                             report          Orléanais (1997)
                                                                             Naturalist      Revue Mensuelle des Naturalistes
 35   Culoz                Auvergne-Rhône-Alpes        2009      River
                                                                             report          Orléanais (1997)
                                                                             Scientific
 36   Dagueys              Nouvelle-Aquitaine          2006      Pond                        Granereau & Cahuzac 2013
                                                                             article
 37   Der                  Grand-Est                   2010      Lake        Press article   France Bleue
                                                                             Scientific
 38   Deux Sèvres          Nouvelle-Aquitaine          1949      Pond                        Goy (1971)
                                                                             article
                                                              Water-filled   Naturalist      Revue Mensuelle des Naturalistes
 39   Dordive              Centre-Val-de-Loire         1996
                                                               quarry        report          Orléanais (1997)
 40   Douai                Hauts-de-France             2010      Pond        Website         Youtube
                                                                             Scientific      Feytaud & Cadenat (1930), Feytaud
 41   Dropt                Nouvelle-Aquitaine          1929      River
                                                                             articles        (1934), de Larambergue (1945)
                                                              Water-filled
 42   Eguzon Chatôme       Centre-Val-de-Loire         2004                  Website         Photo website
                                                               quarry
                           Provence-Alpes-Côte
 43   Esparron-de-Verdon                               2017      Lake        Website         Doris FFESSM
                           d’Azur
 44   Fougères             Bretagne                    1923      Basin       Website         Actu.fr
                                                                             Naturalist
 45   Gétigné              Pays de la Loire            2008      Pond                        Yésou et al. (2014)
                                                                             report
                                                                             Naturalist
 46   Gizeux               Centre-Val-de-Loire         2010      Pond                        Manche (2007)
                                                                             report
                                                                             Scientific
 47   Gour de Tazenat      Auvergne-Rhône-Alpes        1987      Pond                        Balvay (1990)
                                                                             article
                                                                             Scientific
 48   Hagetmau             Nouvelle-Aquitaine           –        Pond                        Granereau & Cahuzac (2013)
                                                                             article
                                                              Water-filled
 49   Hommes               Centre-Val-de-Loire          –                    Website         Freshwater Jellyfish
                                                               quarry
                                                                             Scientific
 50   Hourtin              Nouvelle-Aquitaine           –        Lake                        Granereau & Cahuzac (2013)
                                                                             article
 51   Jazeneuil            Nouvelle-Aquitaine          2019      Basin       Press article   La Nouvelle République Journal
 52   La Brède             Nouvelle-Aquitaine          2015      Basin       Press article   Sud-Ouest Journal
 53   La Fresnaies         Bretagne                    2016      Lake        Website         Youtube
 54   La Roche Sur Yon     Pays-de-la-Loire            2015      Lake        Website         Youtube
                                                                             Scientific
 55   Lacanau              Nouvelle-Aquitaine           –        Lake                        Dussart (1955)
                                                                             article
 56   Laffrey              Auvergne-Rhône-Alpes        2016      Lake        Website         Youtube
                                                              Water-filled   Naturalist
 57   Lavau-sur-Loire      Pays-de-la-Loire            1990                                  Yésou et al. (2014)
                                                               quarry        report
 58   Le Pouzin            Auvergne-Rhône-Alpes        2016      Lake        Website         Youtube
                                                                             Scientific
 59   La Têt               Occitanie                    –        River                       Granereau & Cahuzac (2013)
                                                                             article
                                                                             Scientific
 60   Le Thouet            Pays-de-la-Loire            1949      River                       Goy (1971)
                                                                             article
                                                                             Scientific
 61   Léman                Frontière France / Suisse   1962      Lake                        Balvay (2007)
                                                                             article
                                                                             Scientific
 62   Lencouacq            Nouvelle-Aquitaine           –        Pond                        Granereau & Cahuzac (2013)
                                                                             article
 63   Les Gourgs           Occitanie                   2012      Lake        Website         Freshwater Jellyfish

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208                                  G. MARCHESSAUX, J. GADREAUD, B. BELLONI

Table II. – Continued.
                                                                           Type of
 N°       Localization            Region           Date      Site                                         Sources
                                                                           sources
                                                                         Scientific
 64   Libourne           Nouvelle-Aquitaine        1953      Lake                        Granereau & Cahuzac (2013)
                                                                         article
 65   Limoges            Nouvelle-Aquitaine        2014      River       Website         Limoges aquarium
 66   Loire River        Pays-de-la-Loire          1991      River       Website         Freshwater Jellyfish
                                                                         Scientific
 67   Lormay             Centre-Val-de-Loire       1995      Pond                        Colin & Delahaye (1995)
                                                                         article
 68   Louroux-Hodement   Auvergne-Rhône-Alpes      2016      Lake        Press article   La Montagne Journal
                                                                         Scientific
 69   Lyon               Rhône Alpes               1891      Basin                       Vaney & Conte (1901)
                                                                         article
 70   Malafretaz         Auvergne-Rhône-Alpes      2019      Pond        Press article   Le Dauphiné Journal
                                                                         Naturalist      Muséum national d’Histoire naturelle
 71   Marsac-sur-Don     Pays-de-la-Loire          2013      Pond
                                                                         report          [Ed]. 2003-2019
                                                                         Naturalist
 72   Mayenne            Pays-de-la-Loire          1933      River                       Yésou et al. (2014)
                                                                         report
 73   Mervent            Pays-de-la-Loire          2010      Lake        Press article   Ouest-France Journal
 74   Mine du Carnier    Centre-Val-de-Loire       2014      Lake        Website         Freshwater Jellyfish
                                                                         Scientific
 75   Miribel            Auvergne-Rhône-Alpes      1981      Pond                        Turquin (1987)
                                                                         article
                                                                         Naturalist      Muséum national d’Histoire naturelle
 76   Miribel-Jonage     Auvergne-Rhône-Alpes      2012      Pond
                                                                         report          [Ed]. 2003-2019
                         Provence-Alpes-Côte
 77   Mondragon                                    2007      River       Website         Aqua portail
                         d’Azur
                                                                         Scientific
 78   Monségur           Nouvelle-Aquitaine        1958      Pond                        Dupéré (1958)
                                                                         article
                         Bourgogne-Franche-                              Scientific
 79   Montbéliard                                  1960      River                       Acolat (1961)
                         Comté                                           article
      Montereau-Fault-                                    Water-filled   Scientific
 80                      Île-de-France             1962                                  Girard & Poplin (1970)
      Yonne                                                quarry        article
      Montereau-Fault-
 81                      Île-de-France             2002      River       Website         Freshwater Jellyfish
      Yonne
      Montmelas-Saint-
 82                      Auvergne-Rhône-Alpes      1962      Pond        Website         Freshwater Jellyfish
      Sorlin
                                                                         Scientific
 83   Moreuil            Hauts-de-France           2010      Pond                        Meire & Nauche (2018)
                                                                         article
                                                                         Scientific
 84   Moselle            Grand-Est                 2004      River                       Devin et al. (2005)
                                                                         article
 85   Mulhouse           Grand-Est                 2018     Canal        Press article   L’Alsace Journal
                                                          Water-filled
 86   Mussey             Grand-Est                 2003                  Website         Carnalor
                                                           quarry
 87   Nantua             Auvergne-Rhône-Alpes      2013      Lake        Website         Youtube
                                                                         Naturalist
 88   Nozay              Pays de la Loire          2009      River                       Yésou et al. (2014)
                                                                         report
                                                                         Scientific
 89   Pas du Braou       Nouvelle-Aquitaine        2013      Pond                        Granereau & Cahuzac (2013)
                                                                         article
                         Provence-Alpes-Côte
 90   Paty                                         2012      Lake        Website         Freshwater Jellyfish
                         d’Azur
 91   Pélussin           Auvergne-Rhône-Alpes      2008      River       Website         Aqua portail
                                                                         Naturalist      Muséum national d’Histoire naturelle
 92   Peyriat            Auvergne-Rhône-Alpes      2015      Lake
                                                                         report          [Ed]. 2003-2019
                                                                         Scientific
 93   Pincevent          Île-de-France             1969     Canal                        Girard & Poplin (1970)
                                                                         article
                                                                         Scientific
 94   Poitier            Nouvelle Aquitaine        1951      River                       de Larambergue & Origny 1955
                                                                         article

                                                Vie Milieu, 2019, 69 (4)
CRASPEDACUSTA SOWERBII NEW DISTRIBUTION MAP IN France                                                  209

Table II. – Continued.
                                                                                Type of
 N°        Localization                  Region         Date      Site                                         Sources
                                                                                sources
                              Bourgogne-Franche-                              Scientific
 95    Pontailler-sur-Saône                             1990      River                       Balvay (1990)
                              Comté                                           article
 96    Pontcharra             Auvergne-Rhône-Alpes      2019      Lake        Website         Youtube
                                                                              Naturalist      Muséum national d’Histoire naturelle
 97    Pont-Saint-Pierre      Normandie                 2017      River
                                                                              report          [Ed]. 2003-2019
                                                                              Scientific
 98    Précy                  Centre-Val-de-Loire       1944      Pond                        Fauré-Frémiet (1945)
                                                                              article
 99    Puivert                Occitanie                 2017      Lake        Website         Freshwater Jellyfish
 100 Questember               Bretagne                  2017      Pond        Press article   Ouest-France Journal
 101 Reynerie                 Occitanie                 2009      Lake        Press article   La Dépêche Journal
                                                                              Naturalist      Muséum national d’Histoire naturelle
 102 Romagnieu                Auvergne-Rhône-Alpes       –        Lake
                                                                              report          [Ed]. 2003-2019
                                                                              Scientific
 103 Saint Cassien            Auvergne-Rhône-Alpes      1987      Lake                        Bailly et al. (1987)
                                                                              article
       Saint-Barthélémy-                                       Water-filled                   ACPC Club de plongée carrière
 104                          Pays-de-la-Loire           –                    Website
       d’Anjou                                                  quarry                        website
       Saint-Fargeau en       Bourgogne-Franche-
 105                                                     –        Lake        Press article   L’Yonne Républicaine
       Puisaye                Comté
 106 Saint-Gaudens            Occitanie                 2016      Lake        Website         Youtube
       Saint-Jean-de-
 107                          Occitanie                  –        Pond        Website         Data Atlas.com
       Crieulon
       Saint-Martin-de-la-    Bourgogne-Franche-                              Naturalist      Parc Naturel Régional du Morvan
 108                                                    1997      Lake
       Mer                    Comté                                           report          (2001, 2002)
                              Bourgogne-Franche-               Water-filled   Naturalist      Muséum national d’Histoire naturelle
 109 Saint-Vit                                          2019
                              Comté                             quarry        report          [Ed]. 2003-2019
                                                                              Scientific
 110 Sanguinet                Nouvelle-Aquitaine        1982      Lake                        Granereau & Cahuzac (2013)
                                                                              article
                                                                              Scientific
 111 Seignosse                Nouvelle-Aquitaine         –        Lake                        Granereau & Cahuzac (2013)
                                                                              article
                                                                              Scientific
 112 Strasbourg               Grand-Est                 2005      Lake                        Granereau (2000)
                                                                              article
                                                                              Naturalist      Muséum national d’Histoire naturelle
 113 Tarbes                   Occitanie                 2010      River
                                                                              report          [Ed]. 2003-2019
                                                                              Scientific
 114 Toulouse                 Occitanie                 1945     Canal                        Despax (1945)
                                                                              article
 115 Tour                     Centre-Val-de-Loire       2013      Basin       Press article   La Nouvelle République Journal
                                                               Water-filled
 116 Trélazé                  Pays de la Loire           –                    Website         Photo website
                                                                quarry
 117 Vannes                   Bretagne                  2015      Pond        Press article   Ouest-France Journal
                                                                              Scientific
 118 Vaulx en Velin           Auvergne-Rhône-Alpes      1982      Pond                        Turquin (1987)
                                                                              article
       Villefranche-sur-                                                      Scientific
 119                          Auvergne-Rhône-Alpes      2016      River                       Bavard & Clémens (2008)
       Saône                                                                  article
 120 Villeneuve-sur-Lot       Nouvelle-Aquitaine        2015      River       Press article   La Dépêche
                                                                              Scientific
 121 Viviers                  Auvergne-Rhône-Alpes       –        Pond                        Bailly et al. (1987)
                                                                              article
                              Hauts-de-France /
 122 Vodelée                                             –        Pond        Website         Doris FFESSM
                              Belgique
                              Bourgogne-Franche-
 123 Vouglans                                           2010      Lake        Press article   Le Progrès Journal
                              Comté

                                                     Vie Milieu, 2019, 69 (4)
210                                   G. MARCHESSAUX, J. GADREAUD, B. BELLONI

Fig. 6. – Type of sites invaded by
Craspedacusta sowerbii in
France. A: Rivers and canals;
B: Lakes and ponds; C: Basins
and quarries.

the freshwater jellyfish C. sowerbii occurs (Fig. 5A,            rock surface to allow polyps to attach themselves (Fig. 7).
Table II).                                                       In addition, these enclosed environments are isolated
    Nouvelle-Aquitaine and Auvergne-Rhône-Alpes (west-           from other rivers, restricting the supply of cold water that
ern and eastern France) are the regions where C. sowerbii        could limit the reproduction of C. ­sowerbii. The low tem-
is mostly frequently reported (24 and 26 respectively;           perature and high light intensity allow the water to reach
Fig. 5B). We identified 15 stations in Pays-de-la-Loire          temperatures above 25 °C, promoting asexual and sexual
(north-west), 12 stations in Centre-Val de Loire (central        reproduction of this freshwater jellyfish (Adams 2009).
France) and 10 stations in Bourgogne-Franche-Comté               Currently, we are working on the polyp stages under con-
(eastern France). Craspedacusta sowerbii was observed            trolled conditions in the laboratory, and we have found
in less than 10 stations in the other French regions.            strong population growth (from 30 polyps to 482 polyps
    On the basis of the results of the literature review con-    in 3 months; ~50 new polyps per week; data not shown)
ducted in this study, C. sowerbii was mainly observed in         at 29 °C with high light intensity.
the following ecosystems: 38 ponds, 35 lakes, 14 water-             In Miribel-Jonage lake (Turquin 1987), these condi-
filled quarries and 7 basins (Fig. 6).                           tions are highly variable and rarely reached each year,
                                                                 resulting in the absence of regular blooms. In the Royal
                                                                 Botanic Garden in London, breeding occurs more regu-
DISCUSSION                                                       larly as temperatures increase more strongly. In contrast,
                                                                 the great depth of Lake Geneva seems to limit the prolif-
   In the present study, only 29 stations were rivers and        eration of Craspedacusta sowerbii (Balvay 1991). Nowa-
canals. Shallow closed environments were more favorable          days, in a context of global warming, it is not excluded
for the development of Craspedacusta sowerbii. This is           that the strong summer heatwaves will favour the recur-
due to a unique life cycle and environmental characteris-        rence of C. sowerbii blooms. For example, an average
tics. As observed in the spatial distribution of C. ­sowerbii    increase of 1.5 °C in the upper Rhône River and 3.0 °C in
in France, small environments (water-filled quarry, lake,        the lower Rhône River has been observed over 30 years
pond, basin) seem to be favorable environments for its           (Khalanski et al. 2008). Confined environments are also
development. These environments must have a large bed-           highly productive of plankton, the prey of C. sowerbii.

                                                   Vie Milieu, 2019, 69 (4)
CRASPEDACUSTA SOWERBII NEW DISTRIBUTION MAP IN France                                              211

                                                                                                   Fig. 7. – Habitat characteristics
                                                                                                   favorable for sightings of
                                                                                                   Craspedacusta sowerbii medusa.

Finally, Wang et al. (2006) indicated that an oxygen con-            Craspedacusta, and to M Paul, a native English speaker, for
centration higher than 0.26 mg/dm3 is required for this              proof-reading the text.
freshwater jellyfish to survive.
   Craspedacusta sowerbii can cause large blooms with
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   47-63.                                                                                             Associate editor: Aline Migné

                                                     Vie Milieu, 2019, 69 (4)
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