Abstract

The scyphozoan Pelagia noctiluca reproduces by direct development without a benthic stage. Typically, this jellyfish is found offshore with a holoplanktonic lifecycle, vertical migration and feeding behaviours. Frequent outbreaks have been well documented on the Mediterranean shores since the 19th century; however, the offshore distribution of this species remains mostly unknown. In this study, we performed a bimonthly monitoring of P. noctiluca surface density, at high resolution, from a sailboat, along a 35-km coastal to offshore transect in the Ligurian Sea, between February and October 2011. During daylight, P. noctiluca was rarely seen. At night, offshore, P. noctiluca was always present, while within 5 km of the coast, P. noctiluca was rarely observed. Pelagia noctiluca aggregations were most abundant within the Northern Current of the Ligurian Sea. Our findings suggest that P. noctiluca outbreaks observed on Mediterranean shores may result from the transport of the permanent offshore population inshore by specific hydrodynamic conditions.

INTRODUCTION

Reports of jellyfish blooms worldwide have increased dramatically in both the scientific literature and mass media since the 1950s (Condon et al., 2012). These blooms have become increasingly problematic with conferences organized to discuss their consequences worldwide (e.g. Pitt and Purcell, 2009; Mianzan et al., 2012). In many cases, the abundances have become a real economic problem for local populations (reviewed in Purcell et al., 2007). These increases result in a simultaneous negative impact on tourism, aquaculture and fisheries (Mills, 2001) and have been potentially attributed to climate change (Brodeur et al., 1999; Purcell, 2005), eutrophication (Arai, 2001) and overfishing (Purcell and Arai, 2001; Hay, 2006; Lynam et al., 2011). In the Mediterranean Sea, problems were experienced in the early 1980s and several United Nations programmes were set up to address the issues (UNEP, 1984; UNEPMA, 1991; CIESM, 2001). In the absence of background data, the study of jellyfish abundance, physiology, distribution and population dynamics are of high priority (Sabatés et al., 2010).

In many cases, regular sampling of gelatinous zooplankton populations has found considerable interannual variability related to climatic factors, e.g. North Atlantic Oscillation (Lynam et al., 2004; Brodeur et al., 2008; Lynam et al., 2011). In the Mediterranean, it is thought that similar climatic drivers affect the occurrences of the mauve stinger Pelagia noctiluca (Molinero et al., 2005), particularly the Atlantic surface water (Licandro et al., 2010). Warm and dry conditions have been correlated with the abundance of P. noctiluca across the Mediterranean over a 200-year timescale (Goy et al., 1989). Gelatinous zooplankton typically undergo short lifecycles and have the ability to colonize empty ecological niches rapidly (Boero et al., 2008); however, these same variables also result in considerable spatial variability of populations. Although the benthic polyps drive the abundance of most scyphozoan jellyfish species in coastal waters, the holoplanktonic lifecycle of P. noctiluca, i.e. without a benthic polyp stage, leads to a wide distribution across ocean basins (Russell, 1970; Arai, 1997; Purcell, 2005), which is not limited to nearshore reproductive areas. Among jellyfish, P. noctiluca is the most abundant and the most venomous jellyfish species in the Western Mediterranean (Mariottini et al., 2008). However, its distribution in this basin remains largely unknown.

Pelagia noctiluca lives offshore, migrating vertically in response to the migration pattern of their zooplankton prey (Giorgi et al., 1991; Zavodnik, 1991; Malej et al., 1993). This migration pattern results in medusae being reported at considerable depth by day and reaching the surface at night (Franqueville, 1971; Larson et al., 1991; Mariottini et al., 2008). In the Western Mediterranean, it has been suggested that P. noctiluca is abundant mostly in the vicinity of the Northern Current (Morand et al., 1992), a permanent geostrophic current present in the Ligurian Sea; however, this hypothesis was based on irregular sampling over several years and poor data resolution. Moreover, the few available observations of P. noctiluca suggest that their presence in the Mediterranean follows a pluriannual cycle of ∼11–12 years, with 5–6 years presence/absence oscillations (Goy, 1984; Morand and Dallot, 1985; Goy et al., 1989).

Contrasting with this cycle, P. noctiluca has been quasi continuously observed on the southern coasts of France since the 1990s (Bernard et al., 2011). These coastal outbreaks are sporadic (Bernard et al., 2011) and may originate from local patchy populations or from a single permanent offshore population (Vucetic, 1984). Mechanisms leading to these coastal outbreaks are still poorly understood, mainly because of a lack of observations and knowledge on the annual P. noctiluca distribution in the northwestern Mediterranean Sea.

In order to fill this gap, we monitored the abundance of P. noctiluca bimonthly from February to October 2011, at night on a transect from Villefranche sur Mer, France, and heading towards Calvi, on the island of Corsica, and compared the observed distributions with the hydrological characteristics of the area surveyed.

METHOD

Study site

Abundance of P. noctiluca was monitored in the Ligurian Sea on a ∼35-km bimonthly transect from Villefranche sur Mer (43°41′N, 7°18′E) heading towards Calvi (42°34′N, 8°45′E) (Fig. 1). This area was selected because it is well known in terms of its hydrodynamics and hydrology. The Ligurian Sea has a permanent cyclonic circulation (Millot, 1999) with an associated thermohaline front enclosing a central divergence zone. The French and Italian Rivieras to the north, and Corsica to the south, bound the Ligurian Sea. This basin is characterized by three main hydrographic zones (Prieur, 1981; Béthoux and Prieur, 1983; Prieur and Tiberti, 1985): (i) a peripheral zone (Pz) with weak and variable current; (ii) a frontal zone (Fz) characterized by a sharp horizontal change in density and a ∼ 0.4 m/s jet called the Northern Current; (iii) an offshore central zone (Cz) where the surface water density and salinity are high (∼28.9 kg/m3 and ∼38.3‰, respectively; Fig. 1).

Fig. 1.

Map of the study area showing the location of the monitored transect and the geostrophic current field from AVISO (aviso.oceanobs.com) for 22 June 2011. The background shows the 300, 1000 and 2000 m bathymetry isocontours. The triangle indicates the DYFAMED point (43°25′N, 7°52′E).

Fig. 1.

Map of the study area showing the location of the monitored transect and the geostrophic current field from AVISO (aviso.oceanobs.com) for 22 June 2011. The background shows the 300, 1000 and 2000 m bathymetry isocontours. The triangle indicates the DYFAMED point (43°25′N, 7°52′E).

Monitoring strategy

The monitoring of abundance and distribution was carried out bimonthly from February 2011 to October 2011 (Table I), on board of the “Alchimie”, an 11-m long sailboat. Each survey started in the evening around 6 p.m. and ended at ∼3 a.m. of the next day. The outward and return routes lasted 4 h each. The boat cruised on the Nice-Calvi transect at an average speed of 5 knots (maximum cruising speed: 6.5 knots), allowing good observations of the sea surface. Timing and location of our monitoring were constant for all our surveys (except two) to limit the variables of our study, to facilitate comparisons and guarantee the statistical significance of our findings.

Table I:

Summary of the surveys

Survey date Departure Astronomical twilight Arrival Transect distance (km) Instrumentsa Date of ADCP records Date of glider transect Waves height (m) Moonb 
25–26 February 06:50 p.m. 07:49 p.m. 03:00 a.m. 32.4 ADCP, Gd, M 25 February 24–26 February 0.1–2 nv 
9–10 March 06:40 p.m. 08:04 p.m. 03:00 a.m. 28.2 Gd, M  6–9 March 0.1–0.15 nv 
31 March–1 April 06:15 p.m. 08:35 p.m. 03:15 a.m. 22.7 M   0.05 nv 
9–10 April 06:04 p.m. 09:49 p.m. 03:30 a.m. 28.2 M   0.05–0.15 nv 
28–29 April 05:45 p.m. 10:21 p.m. 03:00 a.m. 31.8 ADCP, Gd, M 28 April 25–28 April 0.05–0.1 nv 
18–19 May 05:40 p.m. 10:58 p.m. 03:00 a.m. 34.9 ADCP, M 18 May  0.1 
25–26 May 06:45 p.m. 11:10 p.m. 03:00 a.m. 30.3 M   0.1–0.15 nv 
15–16 June 06:25 p.m. 11:37 p.m. 03:40 a.m. 29.3 ADCP, Gd, M 15 June 13–14 June 0.15–0.35 
9–10 Julyc 11:00 a.m. 11:31 p.m. 18:15 p.m. 38.4 ADCP, M 9 July  0.15–0.20 vd 
2–3 August 08:15 p.m. 10:53 p.m. 04:15 a.m. 25.0 M   0.05 nv 
24–25 September 06:30 p.m. 09:02 p.m. 03:30 a.m. 28.5 Gd, M  23–25 September 0.1 nv 
2 Octobere 02:05 a.m. – 06:30 a.m. 26.8 ADCP, Gd, M 3 October 30 September–2 October 0.1–0.15 nv 
11–12 October 06:30 p.m. 08:30 p.m. 03:30 a.m. 28.5 Gd, M  10–12 October 0.1 
Survey date Departure Astronomical twilight Arrival Transect distance (km) Instrumentsa Date of ADCP records Date of glider transect Waves height (m) Moonb 
25–26 February 06:50 p.m. 07:49 p.m. 03:00 a.m. 32.4 ADCP, Gd, M 25 February 24–26 February 0.1–2 nv 
9–10 March 06:40 p.m. 08:04 p.m. 03:00 a.m. 28.2 Gd, M  6–9 March 0.1–0.15 nv 
31 March–1 April 06:15 p.m. 08:35 p.m. 03:15 a.m. 22.7 M   0.05 nv 
9–10 April 06:04 p.m. 09:49 p.m. 03:30 a.m. 28.2 M   0.05–0.15 nv 
28–29 April 05:45 p.m. 10:21 p.m. 03:00 a.m. 31.8 ADCP, Gd, M 28 April 25–28 April 0.05–0.1 nv 
18–19 May 05:40 p.m. 10:58 p.m. 03:00 a.m. 34.9 ADCP, M 18 May  0.1 
25–26 May 06:45 p.m. 11:10 p.m. 03:00 a.m. 30.3 M   0.1–0.15 nv 
15–16 June 06:25 p.m. 11:37 p.m. 03:40 a.m. 29.3 ADCP, Gd, M 15 June 13–14 June 0.15–0.35 
9–10 Julyc 11:00 a.m. 11:31 p.m. 18:15 p.m. 38.4 ADCP, M 9 July  0.15–0.20 vd 
2–3 August 08:15 p.m. 10:53 p.m. 04:15 a.m. 25.0 M   0.05 nv 
24–25 September 06:30 p.m. 09:02 p.m. 03:30 a.m. 28.5 Gd, M  23–25 September 0.1 nv 
2 Octobere 02:05 a.m. – 06:30 a.m. 26.8 ADCP, Gd, M 3 October 30 September–2 October 0.1–0.15 nv 
11–12 October 06:30 p.m. 08:30 p.m. 03:30 a.m. 28.5 Gd, M  10–12 October 0.1 

aInstruments available to determine the position of the hydrological zone (ADCP, Acoustic Doppler Current Profiler; Gd, glider; M, Mercator model outputs); the one selected for the analysis is in bold.

bPresence/visibility of the moon (v, visible; nv, not visible). In case of moon absent or covered by clouds we have recorded moon “not visible” (nv).

cNocturnal monitoring on board of the Téthys-II starting 5 km away from the coastline.

dVisible on the outward leg, but not on the return leg.

eUnusual departure and return times.

Surveys were conducted only under very good sea conditions (wave height < 0.20 m). This criterion was been selected because, during other studies and preliminary personal observations, we noted that P. noctiluca individuals tend to stay deeper in the water when the wave height exceeds 0.20 m, preventing their detection from the boat and biasing the estimation of their abundance. To plan the surveys, forecasts of wave heights from PREVIMER system website (Lecornu and De Roeck, 2009) and real-time measurements from the Cote d'Azur meteorological buoy were used (Rolland and Blouch, 2002). Wind and sea conditions during surveys were always low (wave height < 0.20 m), with the exception of the return leg on 25 February and 15 June (Table I).

Observations were conducted from the side of the deck of the sailboat, at a height of ∼2 m above the sea surface. At night, a floodlight mounted on deck illuminated an area of 10–12 m2, for a depth of ∼2 m. The jellyfish abundance was estimated by eye count as the number of adult individuals observed in the illuminated area and reported as an index from 0 to 2: 0 for zero individuals, 1 for 1–10 individuals and 2 for more than 10 individuals. These three categories of abundance were considered sufficient to describe realistically the offshore distribution of P. noctiluca. We used abundance classes of the same order of magnitude as Doyle et al. (Doyle et al., 2008), but the maximum observed never exceeded 30–40 individuals per unit of surface, so we considered that further categories were not necessary. Two observers were on the deck of the boat and at least one constantly observed the sea surface along the outward and the return legs of the surveys. Only adult P. noctiluca were considered for abundance estimations, because only adults were detectable.

Global positioning system (GPS) coordinates were noted when the density of P. noctiluca changed or at least every 10 min. Sunset, astronomical twilight, civil twilight, sunrise, astronomical dawn, civil dawn, moonrise, moon to the meridian and moonset local time were noted for every cruise.

We defined three periods during each day depending on the sun illumination: “day” corresponded to the time from astronomical dawn until the sunset, “dusk” to the time between the sunset and astronomical twilight and “night” to the time between astronomical twilight and the astronomical dawn.

Exceptions to the regular protocol occurred on 9 July and 2 October 2011. On 2 October, the survey started at 2 a.m. and ended at 6:30 a.m. during sunrise. On 9 July, we combined the nocturnal monitoring with another scientific campaign, in the same area of the Ligurian Sea, but requiring a larger boat. This survey was carried out starting 25 km away from the shoreline at 11 p.m., going further offshore than usual (38.4 km) and ending 5 km from the coast at 4 a.m., on board Téthys-II, a 24.9-m long oceanographic vessel cruising at 10 knots (observational area ∼20 m2). The use of powerful lighting and good sea conditions allowed accurate monitoring at this cruising speed.

Identification of the hydrological zones

Because the vessel was not equipped for physical and hydrographical measurements, data from parallel projects/campaigns or models of the Ligurian Sea were used to identify the hydrological zones crossed during the cruises.

Acoustic Doppler Current Profiler (ADCP) current velocity and direction were obtained from the INSU SAVED database (saved.dt.insu.cnrs.fr), for the BOUSSOLE cruises (Antoine et al., 2008) simultaneous to our campaigns (Table I), along a transect between Nice and the DYFAMED station, very close to our transect (Fig. 1).

Physical properties of the water were obtained from gliders cruising monthly along a similar transect (Fig. 1), as part of the MOOSE project (Niewiadomska et al., 2008). Conductivity, temperature and depth data were used to characterize the density and slope of isopycnals and identify the location of the Northern Current.

Finally, the location of the Northern Current was also identified using ocean circulation model outputs from the Mercator forecasting system (Bahurel, 2006). The MERCATOR system is based on three components: the ocean model, the surface forcing fields and the observations (remotely sensed sea surface temperature and altimetry; in situ temperature and salinity profiles). These components are routinely integrated through an assimilation method, the objective being to provide the best possible description of the real ocean (Brasseur et al., 2005).

A transect across the Northern Current would be segmented in three zones: a Pz (low current velocity, <0.2 m/s and weak 28.9 isopycnal slope); an Fz (high current velocity, ≥0.2 m/s and significant 28.9 isopycnal slope) and a Cz (low current velocity, <0.2 m/s and weak 28.9 isopycnal slope) (Prieur, 1981; Béthoux and Prieur, 1983; Prieur and Tiberti, 1985; Boucher et al., 1987; Niewiadomska et al., 2008; Stemmann et al., 2008). The Cz was never crossed during this survey and therefore was not considered during analysis.

The hydrological zones were identified using the available data on (i) current velocity estimations from ADCP, (ii) slope of the 28.9 isopycnal from gliders density section and (iii) the Mercator surface current models outputs. Current velocity from ADCP at 28 m depth is considered as the most reliable parameter, followed by the slope of the 28.9 isopycnal. Mercator velocity outputs were used when none of the previous information was available. Table I summarizes the available instruments and the one selected to determine the hydrological zones for each survey.

We fixed the coastal zone (Co) at 5 km off Villefranche sur Mer, because of the lack of hydrological data in this area, whatever the source of data taken into account.

To map the along-track distribution of P. noctiluca, the distance from Villefranche sur Mer harbour was computed for each GPS position. Along track abundance data were binned in 5 km bins. For each bin, frequencies of the abundance indices (0, 0 ind./10 m2; 1, ≤10 ind./10 m2; 2, >10 ind./10 m2) were computed. Frequencies of the abundance indices were also computed for each survey and each zone (Co, Pz and Fz).

RESULTS

Adult P. noctiluca were observed on all 13 surveys conducted between 25 February and 11 October in the Ligurian Sea. Abundances of P. noctiluca varied as a function of the distance from the coast, and with the time of day (Figs 2 and 3).

Fig. 2.

Pelagia noctiluca abundance for the 13 surveys from 25 February to 2 October 2011 as a function of distance to Villefranche sur Mer harbour along outward and return tracks. Jellyfish abundance is coded as the size and colour of the dot (white, 0; grey, ≤ 10 ind./10m2; black, > 10 ind./10m2) along forward (upper line) and return (lower line) tracks of the transect. The location at the time of sunset (star), astronomical twilight (triangle) and astronomical dawn (square) are plotted on the track. The Co is fixed at 5 km off Villefranche sur Mer as a grey vertical line. The limit between Pz and Fz is indicated as a black vertical line.

Fig. 2.

Pelagia noctiluca abundance for the 13 surveys from 25 February to 2 October 2011 as a function of distance to Villefranche sur Mer harbour along outward and return tracks. Jellyfish abundance is coded as the size and colour of the dot (white, 0; grey, ≤ 10 ind./10m2; black, > 10 ind./10m2) along forward (upper line) and return (lower line) tracks of the transect. The location at the time of sunset (star), astronomical twilight (triangle) and astronomical dawn (square) are plotted on the track. The Co is fixed at 5 km off Villefranche sur Mer as a grey vertical line. The limit between Pz and Fz is indicated as a black vertical line.

Fig. 3.

Frequency of the abundance index for all surveys as a function of the distance from the coast: (A) day (total number of observations: 96), (B) dusk (total number of observations: 155), (C) night (total number of observations: 414). Abundance indices: 0, 0 ind./10 m2; 1, ≤10 ind./10 m2; 2, >10 ind./10 m2.

Fig. 3.

Frequency of the abundance index for all surveys as a function of the distance from the coast: (A) day (total number of observations: 96), (B) dusk (total number of observations: 155), (C) night (total number of observations: 414). Abundance indices: 0, 0 ind./10 m2; 1, ≤10 ind./10 m2; 2, >10 ind./10 m2.

Co, Pz and Fz positions

Positions of the three hydrological zones were identified using current velocities from ADCP (6 of 13 surveys, Table I), automated glider density sections (three surveys) and Mercator surface current model alone for the remaining surveys, when no in situ data were available (Table I).

The Mercator currents were compared using ADCP and glider data for all available survey dates and agreed in seven of nine cases (e.g. Fig. 4B and D), except on 18 May and 2 October. In all the surveys, the Fz was always entered but never totally crossed, and the Cz of the Ligurian basin has never been reached. Considering our data set, the boundary between the peripheral region and the Fz of the Northern Current displayed a strong spatial oscillation from 5 km (15 June) to 19.4 km (2 August) offshore, with an average of 11.2 km.

Fig. 4.

Jellyfish abundances (circles: white, 0; grey, ≤10 ind./10 m2; black, >10 ind./10 m2) are represented along outward and return routes of the transect. We fixed the Co at 5 km off Villefranche sur Mer. Only nocturnal observations are considered, i.e. dusk and night data. (A) Example of P. noctiluca increasing distribution offshore, observed on 28 April 2011. The Pz and Fz have been identified using ADCP data (thin solid lines) overlaid on surface currents from Mercator. (BD) Example of P. noctiluca ubiquitous distribution, observed on 9 March 2011. Mercator surface currents are shown in (B) for comparison with the hydrological zones identified using the slope of the 28.9 isopycnal (bold black line) from the glider density section (D).

Fig. 4.

Jellyfish abundances (circles: white, 0; grey, ≤10 ind./10 m2; black, >10 ind./10 m2) are represented along outward and return routes of the transect. We fixed the Co at 5 km off Villefranche sur Mer. Only nocturnal observations are considered, i.e. dusk and night data. (A) Example of P. noctiluca increasing distribution offshore, observed on 28 April 2011. The Pz and Fz have been identified using ADCP data (thin solid lines) overlaid on surface currents from Mercator. (BD) Example of P. noctiluca ubiquitous distribution, observed on 9 March 2011. Mercator surface currents are shown in (B) for comparison with the hydrological zones identified using the slope of the 28.9 isopycnal (bold black line) from the glider density section (D).

On 9 July, 24 September and 2 October, the current, i.e. the near edge of Fz, was very close to the coast (Fig. 2), shrinking Pz to the point that it could not be detected, as on the 15th June survey, when the Fz reached the coastal limit (Fig. 2).

Average day–night P. noctiluca distribution

All surveys left Villefranche sur Mer harbour before sunset (except 9 July and 2 October) thereby observing the transition between both day- and night-time distributions of P. noctiluca.

During the day, P. noctiluca was encountered only during one survey, on 9 April, between 10 and 15 km offshore (Figs 2 and 3A). Additionally, on 2 October, we were able to span astronomical dawn and noted an absence of P. noctiluca immediately after this time (Fig. 2).

Typically, P. noctiluca started to appear in the surface layer after twilight (Figs 2 and 3B) and mostly away from the coast. During the night, higher densities were more frequent for all distance bins (Fig. 3C). During dusk and night, abundances increased to seaward. On average, largest abundances were observed during the night between 30 and 35 km offshore (Fig. 3C).

Pelagia noctiluca was only observed within 5 km from the coast during the night-time on 9 and 31 March. For the whole transect, differences of abundances between day, night and dusk were significant (χ2 test, P < 0.001), with higher abundances when the moon was not visible at night (Table I; two-sample t-test, P = 0.015).

In some cases, the jellyfish abundances detected on the outward and the return tracks were different and resulted from changing sea conditions, in addition to the effect of light already noted. For example, on 25 February, sea conditions deteriorated rapidly during the monitoring, waves increased from a height of 0.1–2 m, in less than an hour, at ∼20 km offshore, rendering the detection of P. noctiluca difficult on the return track (Fig. 2). On other occasions, small changes in the sea state were noted, but their effect was less clear. On 9 July, because of a parallel experiment, the vessel was stopped between dusk and sunset thus covering a shorter distance during this period than for the other surveys (Fig. 2).

Pelagia noctiluca along-track distribution versus hydrological zones

In the majority of surveys (8 of 13 cases, Fig. 5), P. noctiluca was absent at the coast and increased in abundance to seaward (e.g. 28 April; Fig. 4A). In two cases, 9 and 31 March (Fig. 5), we observed a homogeneous distribution of the jellyfish throughout the transect (e.g. 9 March; Fig. 4C and D). In addition to these general trends, there were three notable variations. On 15 June, P. noctiluca abundance was very low in Co and Fz, but totally absent in Pz. On 2 August, jellyfish were absent in Co but considerably more abundant in Pz than in Fz. Finally, on 9 July, abundance was recorded in both Pz and Fz, but Co was not explored therefore preventing the classification of this part of the transect. Overall, P. noctiluca were most abundant in the Fz in most cases (Fig. 5) with significant differences between the abundances in the three zones (χ2 test, P < 0.001).

Fig. 5.

Frequency of P. noctiluca abundance index (0, 0 ind./10 m2; 1, ≤10 ind./10 m2; 2, >10 ind./10 m2) observed per Co, Pz and Fz, and per survey. Only nocturnal data are considered, i.e. since astronomical dusk.

Fig. 5.

Frequency of P. noctiluca abundance index (0, 0 ind./10 m2; 1, ≤10 ind./10 m2; 2, >10 ind./10 m2) observed per Co, Pz and Fz, and per survey. Only nocturnal data are considered, i.e. since astronomical dusk.

DISCUSSION

Adult P. noctiluca were present offshore in the Ligurian Basin throughout the 9-month period surveyed in 2011. However, spatially and temporally their distribution varied with the time of day, distance from the coast and the location of the Northern Current.

Impact of light on P. noctiluca vertical distribution

Our observations showed that, in the open sea, P. noctiluca is visible at the surface layer after dark. This confirms the few previous observations, suggesting that P. noctiluca perform daily vertical migrations from considerable depth (Pérès, 1958; Franqueville, 1971), reaching the surface at night (Morand et al., 1992). Our surveys confirm this behaviour over 9 months for P. noctiluca. These migrations can be attributed to feeding (following the zooplankton community; Lampert, 1989) or survival strategies (avoiding predator during day; Harrison, 1984; Purcell and Arai, 2001). Pelagia noctiluca have been identified as a prey of a number of Mediterranean apex predators, including tuna, swordfish, sunfish and loggerhead turtles (Cardona et al., 2012); however, depth is unlikely to provide a refuge from these deep-diving predators (e.g. Teo et al., 2007; Sims et al., 2009). Most likely the migration of P. noctiluca is to maximize the feeding duration on planktonic crustacean prey (Giorgi et al., 1991). Diel vertical migration (DVM) is a common trait within many zooplankton species to avoid predation by larger visual predatory organisms while utilizing the prey resources at the surface (reviewed by Hays, 2003), but it is less common in scyphozoan jellyfish which are frequently observed at the surface by day, e.g. from aerial surveys (Graham et al., 2003; Houghton et al., 2006) or ship observations (Doyle et al., 2007; Bastian et al., 2011). The tactile predation by cruising predators, such as jellyfish, removes the need for visual predation. Indeed, other deep water species such as Periphylla periphylla have also shown regular DVM (Kaartvedt et al., 2011).

Cohen and Forward (Cohen and Forward, 2009) reviewed the factors controlling causes of DVM and noted that some gelatinous species followed constant isolumes. In our study, P. noctiluca were less abundant when at least one quarter of the moon rose on the horizon. This type of situation was only detected during 3 and a half of the 13 surveys (Table I), but nevertheless P. noctiluca were 50% more likely to be seen when there was no moon visible. Moonlight has also been demonstrated to negatively affect the vertical migration of other planktonic organisms (Tarling et al., 1999; Anokhina, 2006). This apparent behavioural change as a response to increasing light has also been seen in laboratory studies (Axiak, 1984; Schuyler and Sullivan, 1997) and would further support the isolume hypothesis; however, the mechanism of light reception has yet to be identified in P. noctiluca. Salps (Salpa sp.) have also been observed to respond to a decrease in downwelling irradiance, ascending over 100 m through the water column following a constant isolume as a result of a turbid water influx (Frank and Widder, 2002). Potentially, P. noctiluca may also follow similar isolumes, explaining their appearance at the surface around twilight and disappearance at dawn on 2 October, but equally chemical stimuli emitted by prey could also be a significant driver. Future parallel studies of the predator and prey fields could elucidate this further.

In other areas, P. noctiluca has been recorded offshore at the sea surface also during daytime, e.g. in western Irish offshore waters (Doyle et al., 2008) and in the Adriatic Sea (Zavodnik, 1987). Such findings suggest that other factors, in addition to light and prey/predator relationships, affect the distribution and the migration of this scyphomedusa in the water column. The reproductive behaviour could be one of these factors. Ephyra and young stages of P. noctiluca are mostly observed in the sea surface layers (Morand et al., 1992), but they are thought to be unable to make large migrations (Hecq et al., 2009). It may be plausible that adults migrate in the superficial layers of the water column to release gametes, providing the new larvae with a suitable environment for their development.

Large-scale distribution

Adult P. noctiluca were observed on every survey throughout this study, with no obvious seasonal cycle in abundance. This confirms the hypothesis of a permanent offshore population in the Ligurian Sea and supports the view of Morand et al. (Fig. 1 in Morand et al., 1992) that there is a permanent jellyfish belt in the Ligurian Sea. However, long-term studies have found interannual oscillations in the abundance of P. noctiluca in the Mediterranean and some years when the species is absent (Goy et al., 1989; Kogovšek et al., 2010). This apparent disparity is likely to be the result of the source of the historical data. The long-term time-series come predominantly from shore-based or near-shore observations, which may not record the presence of P. noctiluca if it is only present offshore. Certainly, the population within the Adriatic Sea is not self-sustaining and the population is sourced from the Mediterranean (Kogovšek et al., 2010), with no genetic differences between the Adriatic and Mediterranean individuals (Stopar et al., 2010). Whether the P. noctiluca population studied here is permanently entrained in the cyclonic circulation observed in the Ligurian Sea (Millot, 1999) or part of a Mediterranean-wide population as suggested by Licandro et al. (Licandro et al., 2010) is not proven.

The lifecycle of P. noctiluca has been suggested to be between 9 months (Kogovšek et al., 2010) and 1 year (Franqueville, 1971; Morand et al., 1992). Licandro et al. (Licandro et al., 2010) suggested that P. noctiluca abundance peaks near Villefranche sur Mer in summer, while ephyrae observed in the water column peaked in April and June (Morand et al., 1992), making a continuous annual cycle feasible; however, further research is required to establish where the various life stages occur. With a strong NE-SW Northern Current, it is unlikely that the lifecycle is completed entirely in the Ligurian Sea, but across different regions of the Western Mediterranean basin. The population offshore near Villefranche sur Mer will be fed by source populations located upstream in the current, e.g. in the East Ligurian Sea, Western Corsica Current and Tyrrhenian Sea, and will feed populations downstream along the path of the Northern Current (Licandro et al., 2010). To extend this study, particle tracking models could be used for predicting the path of jellyfish particles, including a DVM of ∼500 m. A particle tracking model developed by Qiu et al. (Qiu et al., 2010) for the region showed a small proportion of particles being retained in the Ligurian Sea over a 90-day particle life. Such models should significantly affect our understanding of P. noctiluca distribution and the capacity for stranding along the Mediterranean shoreline.

Coastal-open sea distribution with respect to the Fz

Excluding particular situations and the light effect discussed above, the density of P. noctiluca often differed between the outward and the return legs of the surveys. This may be due to the typical patchiness of zooplankton in general (Omori and Hamner, 1982) and jellyfish in particular (Graham et al., 2001; Magome et al., 2007). For the same transect, Molinero et al. (Molinero et al., 2008) found across shelf patch size ranging from 1 km (euphausiids) to 10 km (salps). Another factor that could presumably affect the presence of P. noctiluca is the wave height, with two of our surveys potentially supporting this assertion. While the wind did not change significantly during any of the surveys (except 25 February), the sea conditions worsened in two cases, on 25 February and 15 June (Fig. 2), with an apparently concomitant decrease in P. noctiluca detectable. The presence of P. noctiluca may be disturbed by the sea state, disappearing from the surface when the sea surface is not completely smooth, as is the case with Rhizostoma octopus, which responds to vibrations by diving (Russell, 1970). Zavodnik (Zavodnik, 1987) also noted that P. noctiluca individuals rarely swam at the surface to avoid wave damage. This presumed sensitivity to the conditions could be an interesting aspect to explore more in detail.

In terms of average abundances, P. noctiluca were more abundant in the Fz than in the Co and Pz (Fig. 5). A seaward increase in zooplankton abundance was also observed in the Ligurian Sea for P. noctiluca by Morand et al. (Morand et al., 1992) and for several copepod species (Boucher, 1984; Molinero et al., 2008). While P. noctiluca may increase with distance from the shore, we would expect a lower abundance in the Cz of the Ligurian Sea, resulting from declining current intensity (Fig. 1 in Morand et al., 1992). Whether this higher abundance associated with the Fz is a result of the biological prey field or caused by physical aggregating factors requires further study. Biologically, this Fz is a favourable feeding environment, indeed upwelling of nutrients by divergent circulation cells occurs parallel to the front (Prieur, 1979; Boucher, 1984; Stemmann et al., 2008). The surface nutrient enrichment fuels primary (Béthoux and Prieur, 1983) and secondary production (Boucher, 1984; Boucher et al., 1987; Ibanez and Boucher, 1987; McGehee et al., 2004; Molinero et al., 2008); therefore, the whole Northern Current path is a favourable region for P. noctiluca growth and maintenance (Morand et al., 1992; Sabatés et al., 2010). Physically, vertical circulation coupled with the Fz of the Northern Current is characterized by divergent and convergent flows (Boucher et al., 1987; Stemmann et al., 2008). These cross-frontal flows are weak; however, they may have an influence on migrating and swimming organisms (Franks, 1992). A model developed by Franks (Franks, 1992) showed that in a convergent flow an increase in the concentration of vertical migrators is found at the surface and near the convergence for strong swimmers (maximal speeds of ca. 2–20 mm/s) during the upward phase of the migration, since the surface forms a barrier to migration. P. noctiluca are strong swimmers sensu Franks (Franks, 1992), as they migrate at ∼33 mm/s (i.e. 2 m/min; Arai, 1997); therefore, convergence zones would aggregate both crustacean prey and jellyfish predators in this region. Unfortunately with our in situ observations, the convergent cells cannot be easily identified, as they are a three-dimensional phenomenon constantly evolving with time.

Pelagia noctiluca was present only episodically in the Co (3 of 13 surveys, Fig. 5), while it was always present in the frontal one. Abundance onshore is also known to be erratic (Bernard et al., 1988; Bernard et al., 2011) and may be associated with strong wind effects driving individuals ashore. Frequently observed in poor condition close to shore (Zavodnik, 1987; Hecq et al., 2009), it is unknown whether these individuals are damaged during transport or transported as a result of damage or starvation. In any case, there is an apparent uncoupling between offshore and onshore abundance. The hypothesis of a permanent population of P. noctiluca offshore with sporadic transport to the coast is therefore plausible. Episodic transport could be linked to coastal intrusions of the current. In this regard, modelling studies coupling physical transport and coastal jellyfish outbreak monitoring for the Ligurian basin should be pursued. A better understanding of the population dynamics of P. noctiluca and conditions leading to its major outbreaks close to shore may allow anticipation and the taking of precautions prior to their arrival, perhaps limiting potential damage to the tourism industry.

CONCLUSIONS

We have shown the importance of night-time observations to study the distribution of vertically migrating P. noctiluca. Pelagia noctiluca were found throughout the year, but rarely in close proximity to the coast. Surface occurrence of this species in the Ligurian Sea was driven by the physical conditions of the Northern Current and may be linked to the presence of the moon.

Future work should extend the surveys into the Cz of the Ligurian Basin, possibly utilizing autonomous vehicles, and explore the coastal region to determine the physical forces affecting the occurrence of P. noctiluca. Finally, an understanding of the vertical distribution and the association of medusae with the prey field will complement the observed surface distributions.

FUNDING

This study was supported by the projects JELLYWATCH, funded by Region Provence-Alpes-Côte d'Azur - PACA (France) and the FEDER EU fund, MEDAZUR, funded by Conseil Général Alpes Maritimes – CG06 (France), and the program ANR-10-PDOC-005-01 ECOGELY (France). M.F. was financially sustained by a PhD fellowship from the JELLYWATCH and the MEDAZUR projects.

ACKNOWLEDGEMENTS

We wish to thank the captain and the crew of the “Alchimie”, respectively, Alain Garcia, Chantal Dumas and Laurent Gilletta, for the essential technical support and above all for their commitment during all our surveys. We also thank the entire crew of the Téthys-II for the monitoring of the night between 9 and 10 July 2011. We are grateful to Lars Stemmann for his teaching aid and support for the good interpretation of the data. Thanks to Florent Besson for his advice and practical assistance. We are particularly thankful to the two reviewers for improving and enriching our manuscript. MERCATOR-OCEAN is thanked for providing velocity field outputs.

REFERENCES

Anokhina
L. L.
Influence of moonlight on the vertical migrations of benthopelagic organisms in the near-shore area of the Black Sea
Oceanology
 , 
2006
, vol. 
46
 (pg. 
385
-
395
)
Antoine
D.
d'Ortenzio
F.
Hooker
S. B.
, et al.  . 
Assessment of uncertainty in the ocean reflectance determined by three satellite ocean color sensors (MERIS, SeaWiFS and MODIS-A) at an offshore site in the Mediterranean Sea (BOUSSOLE project)
J. Geophys. Res.
 , 
2008
, vol. 
113
 pg. 
C07013
 
Arai
M. N.
A functional Biology of Scyphozoa
 , 
1997
Springer, Chapman & Hall, Suffolk, Great Britain
pg. 
336
 
Arai
M. N.
Pelagic coelenterates and eutrophication: a review
Hydrobiologia
 , 
2001
, vol. 
451
 (pg. 
69
-
87
)
Axiak
V.
Effect of decreasing light intensity on the activity of the scyphomedusa Pelagia noctiluca (Forskal)
Workshop on Jellyfish Blooms in the Mediterranean, Athens, 31 October–4 November 1983
 , 
1984
United Nations Environment Programme, Arhens, Greece
(pg. 
121
-
127
)
Bahurel
P.
Chassignet
E. P.
Verron
J.
MERCATOR OCEAN global to regional ocean monitoring and forecasting
Ocean Weather Forecasting
 , 
2006
Springer, Netherlands
(pg. 
381
-
395
)
Bastian
T.
Haberlin
D.
Purcell
J. E.
, et al.  . 
Large-scale sampling reveals the spatio-temporal distributions of the jellyfish Aurelia aurita and Cyanea capillata in the Irish Sea
Mar. Biol.
 , 
2011
, vol. 
158
 (pg. 
2639
-
2652
)
Bernard
P.
Berline
L.
Gorsky
G.
Long term (1981–2008) monitoring of the jellyfish Pelagia noctiluca (Cnidaria, Scyphozoa) on Mediterranean coasts (Principality of Monaco and French Riviera)
Journal of Oceanography, Research and Data
 , 
2011
, vol. 
4
 (pg. 
1
-
10
)
Bernard
P.
Couasnon
F.
Soubiran
J.
, et al.  . 
Summer monitoring of the jellyfish Pelagia noctiluca (Cnidaria, Scyphozoa) on the French Mediterranean coast
Ann. Inst. Oceanogr.
 , 
1988
, vol. 
64
 (pg. 
115
-
125
)
Béthoux
J. P.
Prieur
L.
Hydrobiologie et circulation en Méditerranée nord-occidentale
Pétrole Et Techniques
 , 
1983
, vol. 
299
 (pg. 
25
-
34
)
Boero
F.
Bouillon
J.
Gravili
C.
, et al.  . 
Gelatinous plankton: irregularities rule the world (sometimes)
Mar. Ecol. Prog. Ser.
 , 
2008
, vol. 
356
 (pg. 
299
-
310
)
Boucher
J.
Localization of zooplankton populations in the Ligurian marine front: role of ontogenic migration
Deep-Sea Res. Pt A
 , 
1984
, vol. 
31
 (pg. 
469
-
484
)
Boucher
J.
Ibanez
F.
Prieur
L.
Daily and seasonal variations in the spatial distribution of zooplankton populations in relation to the physical structure in the Ligurian Sea Front
J. Mar. Res.
 , 
1987
, vol. 
45
 (pg. 
133
-
173
)
Brasseur
P.
Bahurel
P.
Bertino
L.
, et al.  . 
Data assimilation for marine monitoring and prediction: the MERCATOR operational assimilation systems and the MERSEA developments
Q. J. R. Meteorol. Soc.
 , 
2005
, vol. 
131
 (pg. 
3561
-
3582
)
Brodeur
R. D.
Decker
M. B.
Ciannelli
L.
, et al.  . 
Rise and fall of jellyfish in the eastern Bering Sea in relation to climate regime shifts
Prog. Oceangr.
 , 
2008
, vol. 
77
 (pg. 
103
-
111
)
Brodeur
R. D.
Mills
C. E.
Overland
J. E.
, et al.  . 
Evidence for a substantial increase in gelatinous zooplankton in the Bering Sea, with possible links to climate change
Fish. Oceanogr.
 , 
1999
, vol. 
8
 (pg. 
296
-
306
)
Cardona
L.
Alvariz de Quevedo
I.
Borrell
A.
, et al.  . 
Massive consumption of gelatinous plankton by Mediterranean apex predators
PLoS One
 , 
2012
, vol. 
7
 pg. 
e31329
 
Briand
F.
CIESM
Gelatinous zooplankton outbreaks: theory and practise
CIESM Workshop Series
 , 
2001
CIESM Publishers, Monaco
pg. 
112
 
Cohen
J. H.
Forward
R. B.
Jr
Zooplankton diel vertical migration—a review of proximate control
Oceanogr. Mar. Biol.
 , 
2009
, vol. 
47
 (pg. 
77
-
110
)
Condon
R. H.
Graham
W. M.
Duarte
C. M.
, et al.  . 
Questioning the rise of gelatinous zooplankton in the world's oceans
Bioscience
 , 
2012
, vol. 
62
 (pg. 
160
-
169
)
Doyle
T. K.
De Haas
H.
Cotton
D.
, et al.  . 
Widespread occurrence of the jellyfish Pelagia noctiluca in Irish coastal and shelf waters
J. Plankton Res.
 , 
2008
, vol. 
30
 (pg. 
963
-
968
)
Doyle
T. K.
Houghton
J. D. R.
Buckley
S. M.
, et al.  . 
The broad-scale distribution of five scyphozoan jellyfish species across a temperate coastal environment
Hydrobiologia
 , 
2007
, vol. 
579
 (pg. 
29
-
39
)
Franqueville
C.
Macroplancton profond (invertébrés) de la Méditerranée nord-occidentale
Tethys
 , 
1971
, vol. 
3
 (pg. 
11
-
56
)
Franks
P. J. S.
Sink or swim: accumulation of biomass at fronts
Mar. Ecol. Progr. Ser.
 , 
1992
, vol. 
82
 (pg. 
1
-
12
)
Frank
T. M.
Widder
E. A.
Effects of a decrease in downwelling irradiance on the daytime vertical distribution patterns of zooplankton and micronekton
Mar. Biol.
 , 
2002
, vol. 
140
 (pg. 
1181
-
1193
)
Giorgi
R.
Avian
M.
De Olazabal
S.
, et al.  . 
Feeding of Pelagia noctiluca in open sea
Jellyfish blooms in the Mediterranean: proceedings of the II Workshop on Jellyfish in the Mediterranean Sea, Trieste, 2–5 September 1987
 , 
1991
(pg. 
102
-
111
United Nations Environment Programme (eds.), Trieste, Italy
Goy
J.
Fluctuations climatiques de la scyphoméduse Pelagia noctiluca (Forsskal, 1775)
C.R. Acad Sci. III Sci. Vie
 , 
1984
, vol. 
299
 (pg. 
507
-
510
)
Goy
J.
Morand
P.
Etienne
M.
Long-term fluctuations of Pelagia noctiluca (Cnidaria, Scyphomedusa) in the western Mediterranean Sea. Prediction by climatic variables
Deep-Sea Res. Pt A
 , 
1989
, vol. 
36
 (pg. 
269
-
279
)
Graham
W. M.
Martin
D. L.
Felder
D. L.
, et al.  . 
Ecological and economic implications of a tropical jellyfish invader in the Gulf of Mexico
Biol. Invasions
 , 
2003
, vol. 
5
 (pg. 
53
-
69
)
Graham
W. M.
Pagès
F.
Hamner
W. M.
A physical context for gelatinous zooplankton aggregations: a review
Hydrobiologia
 , 
2001
, vol. 
451
 (pg. 
199
-
212
)
Harrison
N. M.
Predation on jellyfish and their associates by seabirds
Limnol. Oceanogr.
 , 
1984
, vol. 
29
 (pg. 
1335
-
1337
)
Hay
S.
Marine ecology: gelatinous bells may ring change in marine ecosystems
Curr. Biol.
 , 
2006
, vol. 
16
 (pg. 
R679
-
R682
)
Hays
G. C.
A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations
Hydrobiologia
 , 
2003
, vol. 
503
 (pg. 
163
-
170
)
Hecq
J. H.
Goffart
A.
Collignon
A.
, et al.  . 
La variabilité de la méduse Pelagia noctiluca (Forskål, 1775) en Baie de Calvi (Corse) en relation avec l'environnement
Rapport pour Agence de l'Eau Rhône Méditerranée et Corse
 , 
2009
pg. 
48 pp
 
Houghton
J. D. R.
Doyle
T. K.
Davenport
J.
, et al.  . 
Developing a simple, rapid method for identifying and monitoring jellyfish aggregations from the air
Mar. Ecol. Prog. Ser.
 , 
2006
, vol. 
314
 (pg. 
159
-
170
)
Ibanez
F.
Boucher
J.
Anisotropie des populations zooplanctoniques dans la zone frontale de Mer Ligure
Oceanol. Acta
 , 
1987
, vol. 
10
 (pg. 
205
-
216
)
Kaartvedt
S.
Titelman
J.
Røstad
A.
, et al.  . 
Beyond the average: diverse individual migration patterns in a population of mesopelagic jellyfish
Limnol. Oceanogr.
 , 
2011
, vol. 
56
 (pg. 
2189
-
2199
)
Kogovšek
T.
Bogunović
B.
Malej
A.
Recurrence of bloom-forming scyphomedusae: wavelet analysis of a 200-year time series
Hydrobiologia
 , 
2010
, vol. 
645
 (pg. 
81
-
96
)
Lampert
W.
The adaptive significance of diel vertical migration of zooplankton
Funct. Ecol.
 , 
1989
, vol. 
3
 (pg. 
21
-
27
)
Larson
R.
Mills
C.
Harbison
G.
Western Atlantic midwater hydrozoan and scyphozoan medusae: in situ studies using manned submersibles
Hydrobiologia
 , 
1991
, vol. 
216
 (pg. 
311
-
317
)
Lecornu
F.
De Roeck
Y. H.
PREVIMER—Observations & Prévisions Côtières
Houille Blanche–revue internationale de l'eau
 , 
2009
, vol. 
1
 (pg. 
60
-
63
)
Licandro
P.
Conway
D. V. P.
Daly Yahia
M. N.
, et al.  . 
A blooming jellyfish in the northeast Atlantic and Mediterranean
Biol. Lett.
 , 
2010
, vol. 
6
 (pg. 
688
-
691
)
Lynam
C. P.
Hay
S. J.
Brierley
A. S.
Interannual variability in abundance of North Sea jellyfish and links to the North Atlantic Oscillation
Limnol. Oceanogr.
 , 
2004
, vol. 
49
 (pg. 
637
-
643
)
Lynam
C. P.
Lilley
M. K. S.
Bastian
T.
, et al.  . 
Have jellyfish in the Irish Sea benefited from climate change and overfishing?
Global Change Biol.
 , 
2011
, vol. 
17
 (pg. 
767
-
782
)
Magome
S.
Yamashita
T.
Kohama
T.
, et al.  . 
Jellyfish patch formation investigated by aerial photography and drifter experiment
J. Oceanogr.
 , 
2007
, vol. 
63
 (pg. 
761
-
773
)
Malej
A.
Faganeli
J.
Pezdič
J.
Stable isotope and biochemical fractionation in the marine pelagic food chain: the jellyfish Pelagia noctiluca and net zooplankton
Mar. Biol.
 , 
1993
, vol. 
116
 (pg. 
565
-
570
)
Mariottini
G. L.
Giacco
E.
Pane
L.
The mauve stinger Pelagia noctiluca (Forsskål, 1775). Distribution, ecology, toxicity and epidemiology of stings. A review
Mar. Drugs
 , 
2008
, vol. 
6
 (pg. 
496
-
513
)
McGehee
D. E.
Demer
D. A.
Warren
J. D.
Zooplankton in the Ligurian Sea: part I. Characterization of their dispersion, relative abundance and environment during summer 1999
J. Plankton Res.
 , 
2004
, vol. 
26
 (pg. 
1409
-
1418
)
Mianzan
H.
Purcell
J. E.
Frost
J. R.
Preface: Jellyfish blooms: interactions with humans and fisheries
Hydrobiologia
 , 
2012
, vol. 
690
 (pg. 
1
-
2
)
Millot
C.
Circulation in the western Mediterranean Sea
J. Mar. Syst.
 , 
1999
, vol. 
20
 (pg. 
423
-
442
)
Mills
C. E.
Jellyfish blooms: are populations increasing globally in response to changing ocean conditions?
Hydrobiologia
 , 
2001
, vol. 
451
 (pg. 
55
-
68
)
Molinero
J. C.
Ibanez
F.
Nival
P.
, et al.  . 
North Atlantic climate and northwestern Mediterranean plankton variability
Limnol. Oceanogr.
 , 
2005
, vol. 
50
 (pg. 
1213
-
1220
)
Molinero
J. C.
Ibanez
F.
Souissi
S.
, et al.  . 
Surface patterns of zooplankton spatial variability detected by high frequency sampling in the NW Mediterranean. Role of density fronts
J. Mar. Syst.
 , 
2008
, vol. 
69
 (pg. 
271
-
282
)
Morand
P.
Dallot
S.
Variations annuelle et pluriannuelles de quelques espèces du macroplancton cotier de la Mer Ligure (1898–1914)
Rapp. Comm. Int. Mer Médit.
 , 
1985
, vol. 
29
 (pg. 
295
-
297
)
Morand
P.
Goy
J.
Dallot
S.
Recrutement et fluctuations à long-terme de Pelagia noctiluca (Cnidaria, Scyphozoa)
Ann. Inst. Océanogr.
 , 
1992
, vol. 
68
 (pg. 
151
-
158
)
Niewiadomska
K.
Claustre
H.
Prieur
L.
, et al.  . 
Submesoscale physical-biogeochemical coupling across the Ligurian Current (northwestern Mediterranean) using a bio-optical glider RID E-6877–2011
Limnol. Oceanogr.
 , 
2008
, vol. 
53
 (pg. 
2210
-
2225
)
Omori
M.
Hamner
W. M.
Patchy distribution of zooplankton: behavior, population assessment and sampling problems
Mar. Biol.
 , 
1982
, vol. 
72
 (pg. 
193
-
200
)
Pérès
J. M.
Trois plongées dans le canyon du Cap Sicié, effectuées avec le bathyscaphe FNRS III de la Marine Nationale
Bull. Inst. Océanogr.
 , 
1958
, vol. 
1115
 pg. 
21
 
Pitt
K. A.
Purcell
J. E.
Proceedings of the Second International Jellyfish Blooms Symposium, Held at the Gold Coast, Queensland, Australia, 24–27 June 2007
 , 
2009
Jellyfish blooms: Causes, consequences and recent advances
Springer Verlag, Australia
pg. 
289
 
Prieur
L.
Structures hydrologiques, chimiques et biologiques dans le bassin Liguro-Provençal
Rapp. Comm. Int. Mer Médit.
 , 
1979
, vol. 
25/26
 (pg. 
75
-
76
)
Prieur
L.
Hétérogénéité spatio-temporelle dans le bassin liguro-provençal
Rapp. Comm. Int. Mer Méd.
 , 
1981
, vol. 
27
 (pg. 
177
-
179
)
Prieur
L.
Tiberti
M.
Identification et échelles des processus physiques et biologiques responsables de l'hétéreogeneité spatial près du front de Mer Ligure
Rapp. Comm. Int. Mer Médit.
 , 
1985
, vol. 
29
 (pg. 
35
-
36
)
Purcell
J.
Climate effects on formation of jellyfish and ctenophore blooms: a review
J. Mar. Biol. Assoc. UK
 , 
2005
, vol. 
85
 (pg. 
461
-
476
)
Purcell
J. E.
Arai
M. N.
Interactions of pelagic cnidarians and ctenophores with fish: a review
Hydrobiologia
 , 
2001
, vol. 
451
 (pg. 
27
-
44
)
Purcell
J.
Uye
S.
Lo
W.
Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review
Mar. Ecol. Progr. Ser.
 , 
2007
, vol. 
350
 (pg. 
153
-
174
)
Qiu
Z. F.
Doglioli
A. M.
Hu
Z. Y.
, et al.  . 
The influence of hydrodynamic processes on zooplankton transport and distributions in the north western Mediterranean: estimates from a Lagrangian model
Ecol. Model.
 , 
2010
, vol. 
221
 (pg. 
2816
-
2827
)
Rolland
J.
Blouch
P.
Meteorological buoys; the example of Météo-France
La météorologie
 , 
2002
, vol. 
39
 (pg. 
83
-
88
)
Russell
F. S.
The Medusae of the British Isles: 2. Pelagic Scyphozoa with a supplement to the first volume on Hydromedusae
 , 
1970
London
Cambridge University Press
pg. 
283
 
Sabatés
A.
Pagès
F.
Atienza
D.
, et al.  . 
Planktonic cnidarian distribution and feeding of Pelagia noctiluca in the NW Mediterranean Sea
Hydrobiologia
 , 
2010
, vol. 
645
 (pg. 
153
-
165
)
Schuyler
Q.
Sullivan
B. K.
Light responses and die1 migration of the scyphomedusa Chrysaora quinquecirrha in mesocosms
J. Plankton Res.
 , 
1997
, vol. 
19
 (pg. 
1417
-
1428
)
Sims
D. W.
Queiroz
N.
Doyle
T. K.
, et al.  . 
Satellite tracking of the world's largest bony fish, the ocean sunfish (Mola mola l.) in the north east Atlantic
J. Exp. Mar. Biol. Ecol.
 , 
2009
, vol. 
370
 (pg. 
127
-
133
)
Stemmann
L.
Prieur
L.
Legendre
L.
, et al.  . 
Effects of frontal processes on marine aggregate dynamics and fluxes: an interannual study in a permanent geostrophic front (NW Mediterranean)
J. Mar. Syst.
 , 
2008
, vol. 
70
 (pg. 
1
-
20
)
Stopar
K.
Ramšak
A.
Trontelj
P.
, et al.  . 
Lack of genetic structure in the jellyfish Pelagia noctiluca (Cnidaria: Scyphozoa: Semaeostomeae) across European seas
Mol. Phylogenet. Evol.
 , 
2010
, vol. 
57
 (pg. 
417
-
428
)
Tarling
G. A.
Buchholz
F.
Matthews
J. B. L.
The effect of lunar eclipse on the vertical migration behaviour of Meganyctiphanes norvegica (Crustacea: Euphausiacea) in the Ligurian Sea
J. Plankton Res.
 , 
1999
, vol. 
21
 (pg. 
1475
-
1488
)
Teo
S. L. H.
Boustay
A.
Dewar
H.
, et al.  . 
Annual migrations, diving behavior, and thermal biology of bluefin tuna, Thunnus thynnus, on their Gulf of Mexico breeding grounds
Mar. Biol.
 , 
2007
, vol. 
151
 (pg. 
1
-
18
)
U.N.E.P.
Workshop on Jellyfish Blooms in the Mediterranean, Athens, 31 October–4 November 1983
 , 
1984
United Nations Environment Programme (eds.), Athens, Greece
pg. 
221
 
U.N.E.P.M.A
Jellyfish Blooms in the Mediterranean: Proceedings of the II Workshop on Jellyfish in the Mediterranean Sea, Trieste, 2–5 September 1987
 , 
1991
United Nations Environment Programme (eds.), Trieste, Italy
pg. 
320
 
Vucetic
T.
Some causes of the blooms and unusual distribution of the jellyfish Pelagia noctiluca in the Mediterranean (Adriatic)
Workshop on Jellyfish Blooms in the Mediterranean, Athens, 31 October–4 November 1983
 , 
1984
United Nations Environment Programme (eds.), Athens, Greece
(pg. 
167
-
176
)
Zavodnik
D.
Spatial aggregations of the swarming jellyfish Pelagia noctiluca (Scyphozoa)
Mar. Biol.
 , 
1987
, vol. 
94
 (pg. 
265
-
269
)
Zavodnik
D.
On the food and feeding in the North Adriatic of Pelagia noctiluca (Scyphozoa)
Jellyfish Blooms in the Mediterranean: Proceedings of the II Workshop on Jellyfish in the Mediterranean Sea, Trieste, 2–5 September 1987
 , 
1991
United Nations Environment Programme (eds.), Trieste, Italy
(pg. 
212
-
216
)

Author notes

Corresponding editor: Roger Harris