A blooming jellyfish in the northeast Atlantic and Mediterranean

A long-term time series of plankton records collected by the continuous plankton recorder (CPR) Survey in the northeast Atlantic indicates an increased occurrence of Cnidaria since 2002. In the years 2007 and 2008, outbreaks of the warm-temperate scyphomedusa, Pelagia noctiluca, appeared in CPR samples between 45° N to 58° N and 1° W to 26° W. Knowing the biology of this species and its occurrence in the adjacent Mediterranean Sea, we suggest that P. noctiluca may be exploiting recent hydroclimatic changes in the northeast Atlantic to increase its extent and intensity of outbreaks. In pelagic ecosystems, Cnidaria can affect fish recruitment negatively. Since P. noctiluca is a highly venomous species, outbreaks can also be detrimental to aquaculture and make bathing waters unusable, thus having profound ecological and socio-economic consequences.


INTRODUCTION
Pelagic, true jellyfish (Cnidaria) form an abundant guild of top predators in marine ecosystems along with fish (Purcell & Arai 2001). Cnidaria vary in size from a few millimetres to a few metres, and they may be solitary (i.e. medusae of Hydrozoa, Scyphozoa and Cubozoa) or colonial (i.e. hydrozoan siphonophores), and have a life cycle that is either truly planktonic or that includes a benthic polyp stage (Boero et al. 2008). Cnidaria are important planktonic predators of fish larvae and their zooplankton food, so they can affect fisheries by bottom-up and top-down control of fish larval survival (Daskalov et al. 2007;Purcell et al. 2007).
Recent years' evidence indicates that Cnidaria have increased in abundance throughout the world's oceans and blooms (outbreaks of tens to hundreds of medusae per cubic metre) now occur more frequently in many seas (Purcell et al. 2007); these outbreaks have been attributed variously to alterations in the trophic structure of marine ecosystems owing to overfishing, and to hydroclimatic effects, since sea temperature can influence jellyfish life cycles and reproductive output (Purcell et al. 2007;Boero et al. 2008). The socioeconomic effects of cnidarian outbreaks are not solely confined to pelagic fisheries, however. Since all Cnidaria possess stinging nematocysts, they are toxic and so can be detrimental to coastal aquaculture through damage to caged fish, and to tourism by curtailing bathing activities (Purcell et al. 2007).
Analysis of data collected by the continuous plankton recorder (CPR), the most temporally and spatially extensive plankton survey in the world, has revealed significant changes in northeast Atlantic plankton communities over the last two decades that appear to be related to hydroclimatic variability (Beaugrand 2004). While it has been suggested that hydroclimatic forcing has an important influence on the abundance of some North Sea cnidarian species (Lynam et al. 2005), the taxa in northeast Atlantic CPR samples are unknown, as their morphological identification is impossible.
Here, using molecular methods, we identify the Cnidaria in northeast Atlantic and northern North Sea CPR samples collected during 2007 and 2008 between 458 N to 588 N and 18 W to 268 W. To help understand the changes that have occurred, we compare our results to observations of Cnidaria in the western Mediterranean where long-term records are also available.

MATERIAL AND METHODS
(a) Plankton sampling in the northeast Atlantic Data on cnidarian distributions and material for genetic analysis were obtained from the CPR survey (Batten et al. 2003). Each CPR sample represents the plankton from 3 m 3 of water taken during 18 km of tow at an average depth of 7 m. Visual identification of cnidarian tissue and/or nematocysts was used as an index of presence and mapped for the period 1958-2007 using a 28 grid, where the nodes were calculated using the inverse-distance interpolation method (Isaaks & Srivastava 1989). A Kruskal-Wallis test was applied to detect the significance of changes in yearly, winter (November to April) and summer (May to October) averages for the periods 1958-1963, 1964-2001 and 2002-2007; these periods were identified by a cumulative sums analysis, which graphically detects local changes in a time series (Kirby et al. 2009). Data were then divided into two periods, 1958-2001 and 2002-2007, and the mean spatial distribution in each period, and the anomaly between them calculated.

(b) Genetic analysis of Cnidaria in CPR samples
Genetic methods were used to identify Cnidaria in CPR samples. DNA was extracted from 34 samples of cnidarian tissue, collected from 15 separate CPR samples that were covered fully in cnidarian material, using standard protocols (Kirby et al. 2006). A 540-bp partial, mtDNA 16S rDNA sequence was then amplified by PCR using the primers of Cunningham & Buss (1993) and Schroth et al. (2002). The PCR involved an initial denaturation step of 948C (1 min), 50 cycles of 948C (1 min), 518C (1 min) and 728C (1 min) and a final extension of 728C (10 min). The PCR products were sequenced using the forward amplification primer and their identity was established by comparison with GenBank. To help identification, a number of DNA sequences were also obtained from Cnidaria sampled by plankton net off Plymouth (England) and Stonehaven (Scotland). These sequences were obtained for both DNA strands (GenBank accession numbers EU999219-EU999230). This journal is q 2010 The Royal Society of Calvi and the Bay of Villefranche (inshore only). The abundance of adult Pelagia noctiluca was also estimated visually in the Balearic and Alboran Seas and from the shore in the Bay of Calvi (table S1, electronic supplementary material). Records of scyphomedusae from the Mediterranean were used to help understand the seasonal progression of the main Cnidaria in northwest Atlantic CPR samples.
(d) Temperature data Sea surface temperature (SST) (18 grid) was obtained from the Hadley Centre, UK.

RESULTS
Analyses of CPR samples from the North Sea reveal an increase in frequency of Cnidaria since the early 1980s (figure 1a), coincident with a change from a cold to a warm hydroclimatic regime (Beaugrand 2004). In the northeast Atlantic the frequency of Cnidaria is greater during the winter months since 2002 than previously (p , 0.001), i.e. Cnidaria appear earlier in the year and persist for longer (figure 1b). The greatest increases in cnidarian abundance in this region occurred predominantly between 408 N to 588 N and 108 W to 308 W (figure 2a).
Genetic analysis of selected northeastern Atlantic CPR samples collected between 2007 and 2008 revealed four different species of siphonophore and the scyphomedusa P. noctiluca, which was the dominant Cnidaria (table S2,

DISCUSSION
Jellyfish have increased in frequency in CPR samples from the northeast Atlantic since 2002, especially during winter. Molecular analyses of jellyfish in CPR samples reveal that P. noctiluca occurs over a large area coincident with where recent changes in Cnidaria are greatest (figure 2a). At this same time, outbreaks of P. noctiluca were reported in 2007 to cause mortalities of farmed fish in northeast Ireland and on the Scottish west coast (Doyle et al. 2008).
Pelagia noctiluca is a warm-temperate holoplanktonic scyphozoan and it is distributed widely from coastal to oceanic waters as far north as the northern North Sea (Hay et al. 1990). Pelagia noctiluca can acclimate to a wide range of temperatures (from less than 88C to greater than 228C in the Mediterranean, (Sandrini & Avian 1991), varying its metabolism to enhance the recruitment of young medusae (Morand et al. 1992), features that enable it to reproduce rapidly under favourable conditions to reach high densities the whole year round. Long-term records from the Mediterranean since the late nineteenth century reveal that outbreaks of this species, that tended to occur only once every 12 years and with 4 years duration before 1998, are now more frequent (Daly Yahia et al. 2010). As outbreaks of P. noctiluca appear to be associated with warm winters (Goy et al. 1989), the recent increase in western Mediterranean SST (up to 0.58C increase since 2002 (figure 2d )) may explain their increasing frequency in this region. Warmer waters in the northeast Atlantic (up to 18C increase in winter SST since 2002 (figure 2d )) may have influenced P. noctiluca similarly.
The seasonal occurrence of high densities of P. noctiluca in the western Mediterranean and northeast Atlantic also appears to be influenced by surface hydrography. In the western Mediterranean, the occurrence of P. noctiluca swarms follows the progression of the Atlantic surface water stream, which flows eastwards from the Atlantic through the Strait of Gibraltar along the North African coast (close to the Tunisian coast in winter) before circulating anticlockwise around the western Mediterranean basin (Pinardi & Masetti 2000) (figure 2b). In the northeast Atlantic, outbreaks of P. noctiluca appear to follow the progression of the North Atlantic Current (NAC) and the surface continental slope current (CSC), a northward branch of the Azores Current that flows along the eastern slope boundary of the European basin Predictions of global climate change suggest that the northeast Atlantic and North Sea will continue to warm (IPCC 2007). Owing to hydroclimatic change, warmer southern waters and species are now both recorded regularly further north penetrating into shelf regions (Beaugrand 2009;Graham & Harrod 2009). Increased advection and mixing of warmer and offshore waters into coastal shelf seas will also carry P. noctiluca and other jellyfish into environments with higher food resources, promoting jellyfish blooms. Outbreaks of P. noctiluca, along with other jellyfish, may therefore become more frequent and extend over a greater proportion of the year than previously. Any increase in jellyfish blooms may influence zooplankton production and fish recruitment to alter the pelagic food web. Since P. noctiluca is one of the most venomous species in waters around the British Isles (Mariottini et al. 2008), changes in its abundance may also have significant socio-economic effects. R.R.K. is a Royal Society Research Fellow. We thank the owners, masters and crews of the ships that tow CPRs, the observation service RADEZOO in Villefranche and STARESO in Calvi, and scientific colleagues, A. Collignon, O. Daly Yahia-Kéfi, A. Goffart, S. Hay, R. Pingree and F. Prejger. We are also grateful to S. Hay and an anonymous referee for improvements to the manuscript.