Culture and Growth of the Jellyfish Pelagia Noctiluca in the Laboratory
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Vol. 510: 265–273, 2014 MARINE ECOLOGY PROGRESS SERIES Published September 9 doi: 10.3354/meps10854 Mar Ecol Prog Ser Contribution to the Theme Section ‘Jellyfish blooms and ecological interactions’ FREEREE ACCESSCCESS Culture and growth of the jellyfish Pelagia noctiluca in the laboratory Martin K. S. Lilley1,2,3, Martina Ferraris3,4, Amanda Elineau3,4, Léo Berline3,4,5, Perrine Cuvilliers3,4, Laurent Gilletta6, Alain Thiéry1, Gabriel Gorsky3,4, Fabien Lombard3,4,* 1IMBE UMR CNRS 7263, Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale (IMBE), Aix-Marseille Université, Avenue Louis Philibert, BP 67, 13545 Aix en Provence Cedex 04, France 2Institut Méditerranéen d’Océanologie (MIO), Aix-Marseille Université, UMR 7294, Campus de Luminy, 13288 Marseille Cedex 9, France 3Sorbonne Universités, UPMC Univ Paris 06, UMR 7093, LOV, Observatoire océanologique, 06230 Villefranche sur mer, France 4CNRS, UMR 7093, LOV, Observatoire océanologique, 06230 Villefranche sur mer, France 5Université du Sud Toulon-Var, Aix-Marseille Université, CNRS/INSU, IRD, Institut Mediterraneen d’Oceanologie (MIO), UM 110, 83957 La Garde Cedex, France 6CNRS, Sorbonne Universités, UPMC Univ Paris 06, Laboratoire de Biologie du Développement de Villefranche sur mer, Observatoire Océanographique, 06230 Villefranche sur mer, France ABSTRACT: Four cohorts of the scyphozoan jellyfish Pelagia noctiluca were grown in the labora- tory. For the first time, P. noctiluca was grown from eggs through to reproductive adults. The max- imum life span in the laboratory was 17 mo. Pelagia noctiluca were first observed to release gametes at an umbrella diameter of 2.4 cm. Laboratory growth under steady feeding conditions showed initial growth followed by stagnation until dietary conditions were altered. A mismatch between the availability of optimal food and the presence of developmental stages may signifi- cantly increase the mortality rates of the young stages. Non-motile prey improved survival of ephyrae stages compared with zooplankton, but good survival and ephyrae growth were only obtained with a high-energy sea urchin egg diet. Maximal growth rates were up to 30% d−1 for young ephyrae and 1.5−4% d−1 for adults. Maximal growth rates were comparable between labo- ratory and in situ growth observations in the Ligurian Sea during 1969 and 2013. Combining observations would suggest that 230 d of continuous growth are required to reach the largest mean size observed in the wild (June 2013, mean ± SD = 15.6 ± 2.8 cm, range = 12−21 cm). We sug- gest that 90−120 d of continuous growth from planula larvae would yield reproductive individuals under ideal growing conditions. We discuss the daily prey abundances required by each individ- ual to sustain basal metabolism and the observed growth rates. KEY WORDS: Mauve stinger · Ligurian Sea · Mediterranean · Bloom · Life cycle · Mortality · Ephyra · Predation Resale or republication not permitted without written consent of the publisher INTRODUCTION 1910). The species has a negative impact on tourism (Bernard et al. 2011) because of its painful stings Found at frequently high abundances, the mauve (Maretic et al. 1991, Mariottini et al. 2008), on aqua- stinger Pelagia noctiluca is a holoplanktonic scypho- culture by overwhelming fish farms and killing fish zoan jellyfish with a wide distribution. Populations (Doyle et al. 2008, Delannoy et al. 2011), and poten- occur in both the North and South Atlantic (Miller et tially on the success of fish stocks such as tuna (Gor- al. 2012), as well as in all the major oceans (Mayer doa et al. 2013). In the Mediterranean Sea, P. noc- *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 266 Mar Ecol Prog Ser 510: 265–273, 2014 tiluca has been a recurrent problem for centuries luca spawned daily, with fertilised eggs used to initi- (Goy et al. 1989). It has historically been observed to ate new growth experiments. Gametes and ephyrae be present or absent for several consecutive years, were transferred between culture containers using with a periodicity of 10−12 yr (Goy et al. 1989, Kogov- a 0.5 cm wide glass pipette. On one occasion, wild šek et al. 2010) attributed to climatic forcing. How- ephyrae were collected by plankton net (Regent net, ever, since 1994 this species has been present almost 1 m diameter, 680 µm mesh size). continuously in the Ligurian Sea, NW Mediterranean During 2013, all collected individuals were meas- (Bernard et al. 2011, L. Berline & F. Lombard pers. ured (bell diameter including lappets), sexed and obs.), suggesting a prolonged period of more favour- weighed (wet weight, precision 0.1 g) on return to able environmental con ditions. Pelagia noctiluca is a the laboratory. Mature male individuals have purple holoplanktonic species, developing directly from gonads with parallel transverse lines of tissue; female planula larvae (Russell 1970, Rottini Sandrini & gonads are browner in colour, in a bunched, cauli- Avian 1983), and therefore cannot rely on polyps to flower-like form, and eggs are usually visible. survive through un favour able conditions. Pelagia noctiluca has been repeatedly studied be - cause of its high abundances and impact on the hu- Experimental trials man environment. Seasonal and spatial abundance estimates have been made (e.g. Bastian et al. 2011, Four cohorts of P. noctiluca were cultured in the lab- Ferraris et al. 2012, Rosa et al. 2013), including lo- oratory and measured repeatedly to obtain growth calised predictions of blooms (Berline et al. 2013). The rates for this species. One cohort was obtained from developmental stages have been well studied (Rottini wild-caught young ephyrae of 5 mm in diameter, Sandrini & Avian 1983, Avian 1986), along with gut while the remaining larvae were obtained by mixing contents and isotopic analyses (e.g. Giorgi et al. 1991, the gametes of fertile wild adult P. noctiluca and cul- Malej et al. 1993, Sabatés et al. 2010), but the quanti- turing the resulting planula larvae. All experiments tative needs to sustain growth are still unknown. were performed at 18°C using 1 µm filtered seawater Estimates of basal metabolic costs confirm that P. in 5−15 l containers, depending on the organism size. noctiluca is able to withstand periods of starvation Younger individuals required maintenance in suspen- (Larson 1987). Importantly though, the duration of sion using motorised PVC paddles rotating at 6 rpm the life cycle, the size at maturation and whether (Table 1). Individuals were fed ad libitum and as co- there are resting stages or adaptations to aid survival horts grew larger, larger prey items were offered, al- as a holoplanktonic species are all unknown. Like- though selective ingestion and digestion were subject wise, the rate of growth has only been observed in to individual variation. The prey offered was changed short-term studies (Larson 1987, Malej & Malej 1992), whenever growth within the experiment stagnated while the energy requirements to sustain growth have (Table 1). Non-motile prey items were offered initially not been quantified. in Runs 3 and 4 to improve survivorship. The objective of this study was to obtain reproduc- Food organisms mostly originated from daily zoo- tively viable P. noctiluca in the laboratory in order to plankton samples collected every morning by oblique estimate the duration of the life cycle and to compare (50−0 m) net tows in the bay of Villefranche-sur-Mer, growth rates between laboratory and in situ popula- using nets with 50, 200 or 680 µm mesh. For organ- tions. We hypothesised that growth rates would allow isms caught with the smallest mesh size (50 µm), only a life cycle of approximately 1 yr, to allow a direct swimming zooplankton were used. Other natural connection between successive generations. prey sources offered to ephyrae were fragments of jellyfish bells (frozen Cotylorhiza tuberculata; fresh Aurelia aurita and Leucothea multicornis) and fresh MATERIALS AND METHODS Paracentrotus lividus sea urchin eggs (~90 µm in dia - meter). Arti ficial diets offered included freshly Jellyfish collection hatched brine shrimp nauplii (Artemia sp., some en - riched with S. presso from Selco), frozen mysid Adult Pelagia noctiluca were collected individually shrimp, and a larval fish diet made up of fish and from the sea surface using a hand net during night yeast extracts (50−100 or 100−200 µm Golden Pearls, surveys in the Ligurian Sea (for details, see Ferraris Brine Shrimp Direct; see Table 1 for details). et al. 2012) or by kayak in the bay of Villefranche- Bell diameter was measured between opposite rho- sur-Mer, France (43.696° N, 7.307° E). Fed P. nocti - palia (RD; cm), with the aboral surface upwards, from Lilley et al.: Laboratory growth and culture of Pelagia noctiluca 267 Table 1. Experimental details of Runs 1−4 in the laboratory and wild populations sampled in 1968−1969 (Franqueville 1971) and 2013. Zooplankton offered to laboratory-grown juvenile Pelagia noctiluca was collected daily from the field with a verti- cally towed Regent net (1 m diameter, 680 µm), with 2 exceptions (a,b). All animals were fed daily, but prey composition and assimilation efficiency were not recorded. Water was changed 2−3 times per week and individuals were measured every 1−2 wk. −: no data recorded Run Ephyrae source Initial Start date Duration Tank Tank Food offered numbers (dd-mm-yy) (d) volume (l) stirring Laboratory growth 1 Eggs (lab) ~1000 26-05-10 45 15 Yes Mixed zooplankton (35−50 µm)a 4 10-07-10 117 5 No Mixed zooplankton (>200 µm)b 4 04-11-10 64 5 No Mixed zooplankton 4 07-01-11 129 5 No Mixed zooplankton + Cotylorhiza tuberculata 4 16-05-11 148 5 No Mixed zooplankton + enriched Artemia sp. 2 Ephyrae (field) 13 01-11-11 119 15 Yes Artemia sp., Aurelia aurita, frozen mysid shrimp 3 Eggs (lab) >1000 03-09-12 184 15 Yes Golden Pearls 4 Eggs (lab) >1000 29-03-13 46 15 Yes Paracentrotus lividus eggs ~90 µm − 14-05-13 38 15 Yes Artemia sp.