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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: [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 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 th 1996) since the end of the 19 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). 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 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). Vie Milieu, 2019, 69 (4) 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) 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
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