Vie et milieu - Life and environment, 2019, 69 (4): 201-213

The freshwater 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: [email protected]

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 , 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 were identified. In our study, we observed a widespread distribution of these freshwa- ter 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 th 1996) since the end of the 19 century, ­Craspedacusta and birds where the 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 (, Limnomedu- indicate native populations from South America (Prota- sae, ) 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). 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 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 , (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 Craspedacusta­ 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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Fig. 2.– Life cycle of Craspeda- custa sowerbii. Modified and based on a drawing in Lytle (1982). (Photos: G Marches- saux).

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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 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 . 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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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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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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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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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

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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

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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.

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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 hundreds or even thousands of jellyfishes per cubic meter, REFERENCES but their sting is not really harmful for humans (Yésou et al. 2014); tingling and hives have however been reported Acker TS, Muscat AM 1976. The Ecology of Craspedacusta sowerbii Lankester, a Freshwater Hydrozoan. Am Midl Nat in Lake Annecy (DORIS 2017). In humans, few cases of 95(2): 323-336. toxicity by C. sowerbii had been reported in the literature Acolat L 1961. Bref aperçu sur les Méduses d’eau douce et before by Loeuillet et al. (2017), who reported the first découverte de l’une d’entre elles, Craspedacusta sowerbii case of a cutaneous envenomation by this freshwater jel- Lankester, dans la région de Montbéliard. Bull Soc Nat lyfish in a lake in southwestern France. Doubs 63(2): 31-36. Adams IB 2009. The effect of light and prey availability on the activity of the freshwater jellyfish, Craspedacusta sowerbii (Hydrozoan). Mém BSc Univ James Madison Harrisonburg, CONCLUSION Virginie: 21 p. Arbačiauskas K, Lasutiene J 2005. The freshwater jellyfish This bibliographical survey on the distribution of the (Craspedacusta sowerbii) in Lithuanian waters. Acta Zool introduced and invasive jellyfish Craspedacusta sowerbii Litu 15(1): 54-57. highlights its geographical distribution in the metropoli- Arov I 2004. On finding jellyfish Craspedacusta in East- tan French territory. Due to its life cycle and ecology, this ern Siberia. http://zooex.baikal.ru/bidermat/craspedacusta. htm (consulted on 14 October 2019). freshwater jellyfish seems to prefer closed and shallow environments that provide all the optimum conditions for Arvy L 1972. Sur la présence de Craspedacusta sowerbyi Lan- kester, 1880 (Limnoméduse: Olindiidae), associé à un com- its development. Our study recorded only observations of mensal (Trichodinia pediculus Ehrenberg, Cilié: Peritrichia) this species in medusa phase in pelagic zones during sum- dans le canal de Briare. Ann Sci Nat Zool 14: 131-146. mertime. This new inventory can be fed by new observa- Bailly JP, Girardi H, Moulet P 1987. Craspedacusta sowerbyi tions of this species, offering a basis to determine whether Lank., 1880 (Hydrozoaire), une station nouvelle dans le sud- the population will increase with currently ongoing cli- est de la France et données écologiques complémentaires sur cette Méduse. Bull Soc Linn Lyon 56(6): 192-198. mate change. It is also important to note that this new Balvay G 1990. Présence de la Méduse d’eau douce Craspeda- map only shows areas where pelagic phases have been custa sowerbyi Lankester, 1880 dans le lac d’Annecy. Arch observed. The spatial distribution of Craspedacusta sow- Sci Genève 43(2): 335-338. erbii could be much more extensive if we also consider Balvay 2007. Microfaune de la zone littorale du Léman de 2004 the polyp phase. A study of different life cycle stages is à 2006. Arch Sci 60: 55-58. currently being conducted in our laboratory. Balvay G 2008. Quelques données sur le zooplancton et autres microorganismes du lac du Bourget. Actes du colloque Acknowledgements. – We would like to thank anonymous “Autour du lac du Bourget”, Le Bourget du Lac, 15-17 mai reviewers and the editor for their helpful comments. We also 2006: 154-166. thank M Bejean from La Citadelle de Besançon for his help in Bavard JP, Clémens A 2008. Le Rhône en 100 questions. ZABR, polyp cultures. Thanks too to JF Cart for his beautiful picture of GRAIE, Villeurbanne: 295 p.

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