The jellyfish P. noctiluca can be considered ‘invasive’ as the periodic occurrence of extraordinary abundances in coastal waters occurs when this typically offshore species is advected shoreward in years when pop...
The jellyfish P. noctiluca can be considered ‘invasive’ as the periodic occurrence of extraordinary abundances in coastal waters occurs when this typically offshore species is advected shoreward in years when population densities appear to be exceptionally high. Consequently, it is problematic at the very periphery of its ‘natural range’, thus differing from truly invasive species that have been introduced into a new area.
P. noctiluca gained notoriety in the Mediterranean and Adriatic Seas as a result of the periodic blooms that negatively impact swimmers (reviewed by Purcell, 2005). Goy et al. (1989) analysed many data sources for the presence and absence of medusae in the Mediterranean Sea between 1885 and 1986, and showed that such events occur with a periodicity of recurrence of about 12 years. The consensus of scientific opinion at two international workshops was that such blooms were related to ocean circulation patterns, and that eutrophication and reduction of zooplanktivorous fish (anchovy) may have contributed to prevalence of the medusae (UNEP, 1984, 1991).
Constrained by a benthic polyp stage, most scyphozoan jellyfish have a predominantly coastal distribution. However, the scyphozoan P. noctiluca lacks a benthic polyp stage and this species consequently has a very broad distribution across ocean basins (Arai, 1997; Purcell, 2005). Unlike most other scyphozoan jellyfish, P. noctiluca is not common in coastal waters but is found predominantly in offshore areas (e.g. Doyle et al., 2008), encroaching upon coastal seas when abundances are high and current / meteorological conditions drive it shoreward.
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
Nuisance blooms of P. noctiluca in coastal waters are a natural occurrence (albeit enhanced in many cases by anthropogenic factors) and cannot be traced, like many ‘invasive’ species, to a single event or locality. In the Mediterranean Sea, where the temporal pattern of P. noctiluca outbreaks is best documented, major aggregations appear for several consecutive years in a row and then largely disappear for a decade or more, with distribution centered in open-water areas.
The movement of P. noctiluca into coastal waters is a natural phenomenon in years of high abundance where aggregations are transported coastally by climatic conditions. However, there is certainly scope for the introduction of P. noctiluca into new areas through the dumping of ballast waters by commercial shipping.
P. noctiluca is an open water jellyfish with a poorly defined geographical range at present; although medusae are thought to be widely distributed in subtropical to temperate waters of the Atlantic and Pacific oceans (Kramp, 1961; Angel and Pugh, 2000; Doyle et al., 2008). Although the northerly limit of the species has not yet been critically defined it does appear that water temperature may be a determining factor in habitat preference. Laboratory tests have been performed on the behaviour of the jellyfish P. noctiluca as a function of the water temperature. It has been found that the usual contractions of the umbrella are almost completely missing at 6°C; they begin to appear at about 7–8°C and they reach frequencies of about 10 and 40 per minute at 11 and 15°C, respectively. An ambient temperature of about 11°C appears to be a threshold value below which this kind of medusa ceases to move actively and sinks, while at higher temperatures it gradually begins to shift, showing a positive thermotropism in the presence of temperature gradients greater than about 0.01°C/cm (Rottini-Sandrini, 1982).
The DNA barcode form the mitochondrial cytochrome oxidase I gene of this species is described by Ortman et al. (2010).
P. noctiluca is a scyphozoan and adapted to a pelagic mode of life. This class of organisms has adapted in such a way that the polyp stage is shortened or in some cases such as that of the genus Pelagia this is absent, thus direct development following sexual reproduction exists. Four gonads arise as elongated endodermal proliferations, developing into ribbon-like folds in the inter-radial sectors of the stomach wall slightly distal to the rows of gastric filaments. Male and female gonads vary only slightly and the main difference is the thickness of the follicle.
Within the Mediterranean Sea, the reproduction of P. noctiluca has been shown to occur from April to December, with a peak in late summer and autumn with ephyrae growing to an average diameter of 7mm in December (Malej and Malej, 1992). Most probably growth slows down or even ceases during winter months owing to relatively low water temperatures (less than 10°C). However, the presence of extensive aggregations around the northern coast of Ireland in November and December 2007 (when temperatures were far below 10°C) (Doyle et al., 2008) shows that the species can abound in waters much beyond the thermal ranges experienced in the Mediterranean Sea.
A more dated account of P. noctiluca reproduction in the Mediterranean is provided by Metschnikoff (1886). In this study eggs were laid during daylight hours in December, developing into a planula after three days. After seven days planulae develop into ephyra, which develop into young medusa after a month. A detailed description of the reproductive cycle of P. noctiluca is also provided by Rottini-Sandrini and Avian (1983).
Physiology and Phenology
Outbreaks of P. noctiluca are best documented for the Mediterranean where they have received considerable attention. The most extensive analysis was conducted by the Station Zoologique at Villefranche-sur-Mer based on records of "years with Pelagia noctiluca" and "years without Pelagia". These records, plus additional data, indicate that over the past 200 years (1785-1985) outbursts of P. noctiluca have occurred about every 12 years. Using a forecasting model, climatic variables, notably temperature, rainfall and atmospheric pressure, appear to predict "years with Pelagia" (Goy et al., 1989).
Beyond the Mediterranean the phonological picture is less clear and limited to individual reports of periodic incursions of the species into coastal waters. A recently funded four-year EU project entitled Ecogel will attempt to unravel the phenology of the species in the wider northeast Atlantic (Doyle et al., 2008)
P. noctiluca appears to be an opportunistic feeder having a wide ranging diet (Malej, 1989; Malej et al.,1993). Gut contents of P. noctiluca from the Adriatic Sea (Mediterranean) suggested Cladocera, Apendicularia, Copepoda, Hydromedusae, Siphonophora and fish eggs were amongst the most common food items of adult medusa (Malej, 1982). Similar results were obtained by Giorgi et al. (1987) and Zavodnik (1991). These prey items are much smaller than P. noctiluca and therefore individual medusa are required to spend long periods foraging each day for prey to satisfy daily food requirements (Valiela, 1984). However, it has been shown that P. noctiluca compensate for such activity by adopting an energetically efficient mode of swimming (Davenport and Trueman, 1985).
The presence of P. noctiluca in coastal waters has not been attributed to any biological associations with other species, although the persistence of aggregations is obviously linked to the availability of suitable prey. (see Nutrition section).
The conditions that are conducive to medusa bloom formation are temperatures above 10°C in winter and below 27°C in summer, and salinities of 35–38 psu (reviewed in Purcell et al., 1999b).
P. noctiluca has no natural enemies per se but may be opportunistically preyed upon by a wide range of vertebrate and invertebrate species (Arai, 2005). However, only two obligate predators are known, namely: (1) the ocean sunfish, Mola mola and, (2) the leatherback turtle, Dermochelys coriacea. Ocean sunfish occur in significant numbers in the Mediterranean (Silvani et al., 1999), and some a lesser degree throughout British and Irish waters (Houghton et al., 2006b) although their top-down effect upon P. noctiluca aggregations has yet to be quantified. Leatherback turtles are widely dispersed oceanic predators and are not present in any specific region to have a noticeable effect upon abundances of P. noctiluca (Houghton et al., 2006c). It is often suggested that the removal of sea turtles through fisheries by-catch is a contributing factor to increases in jellyfish abundances in the Mediterranean Sea. However, although loggerhead turtles (Caretta caretta) and green turtles (Chelonia mydas) (the two nesting species in the Mediterranean Sea) feed opportunistically on jellyfish (Arai, 2005) they constitute only a minor part of their diet with benthic invertebrates and sea grass their preferred respective prey. Conversely, leatherback turtles (Dermochelys coriacea) are considered obligate predators of gelatinous zooplankton but this species does not breed in the Mediterranean and so numbers are restricted to a few roaming individuals, restricting their contribution to the top down control of jellyfish. One predator that may have a noticeable effect on jellyfish numbers is the ocean sunfish (Mola mola). Like leatherback turtles, ocean sunfish feed largely on jellyfish, yet within the Mediterranean (in particular) are subjected to incredibly high rates of by-catch with extensive by-catch figures from Spanish drift gill-net fisheries within the Mediterranean, revealing that ocean sunfish comprised between 70% and 93% of the total catch between 1992 and 1994 (Silvani et al., 1999). Although, a reduction in these by-catch figures would not prevent the occurrence of ‘outbreak years’ it would nonetheless increase potential jellyfish predators in the Mediterranean by an order of magnitude.
Greater top-down pressure may, however, be exerted upon ephyrae (Malej, 1989). In laboratory experiments, Avain (1986) observed that ephyrae were eaten by some pelagic crustaceans (Cladocera, Copepoda). By staying within an aggregation containing adult medusae it has been suggested that ephyrae would gain some protection against these predators, as predators on ephyrae are themselves prey items for adult P. noctiluca.
The dispersal and formation of problematic coastal jellyfish aggregations in the Adriatic Sea was the subject of a bespoke study by Zavodnik (1987). Key factors are summarized below:
1. Swarming aspects: It is known that the transport of swarms is the result of wind and sea currents, as related to their direction, speed and endurance (Rottini-Sandrini et al., 1980; Legovic and Benovic, 1984; Vucetic, 1984). Field observations in the Adriatic Sea revealed several aspects of P. noctiluca massing in the coastal areas in detail (Zavodnik, 1987). Wind effects appeared the most conspicuous aspect of swarming. It was observed that after a few days of continuous winds, large assemblages of jellyfish appeared along the mainland and island shores of Croatia. In the Adriatic Sea, the areas most affected by jellyfish swarms are those exposed to the open sea. However, surface swarms of medusae are also driven to the windward shore of bays and islands after a few hours of the daily maestral, a northwestern offshore wind.
2. Tidal and current effects: The importance of tides and tidal currents in concentrating P. noctiluca populations along the shore has been documented in the Adriatic Sea (Zavodnic, 1987). Jellyfish appeared to accumulate at the sea surface during the flooding tide, sometimes at densities approaching hundreds per square meter. On the ebbing tide, they disappeared from the surface, and were driven, en mass, along the sloping bottom into deeper layers (Zavodnic, 1987). Long distance transport of P. noctiluca was recently illustrated by the transport of extraordinary numbers of jellyfish from offshore waters to the North of Ireland through the North Channel (between Northern Ireland and Scotland) and into the Irish Sea (Doyle et al., 2008).
3. Island effect: When transported by currents, or drifted by wind, medusae can accumulate behind large obstructions, such as a cliff, a small island, or a pier. Accumulations form in the shelter of these objects, owing to eddies in the water body; and for the same reason, floating refuse, together with jellyfish, also accumulated at such sites (Zavodnic, 1987).
4. Trap effect: The shoreward drift of jellyfish swarms through tidal transport is also affected by the interaction of the shoreline and decreasing water depth. Through pulsing pumping, the jellyfish tend to avoid contact with the surface and bottom, thus accumulating just below the surface and 0.5 m or so above the shallow bottom (Zavodnic, 1987).
For the 2007 inundation of County Antrim in Northern Ireland the most likely cause of dispersal was a combination of exceptional high numbers of P. noctiluca (through undetermined factors at present) and the predominant westerly winds experienced during the late autumn / early winter driving the jellyfish towards Scotland and then down through the North Channel into the Irish Sea. Considering the ensuing salmon farm fish kill in Northern Ireland and the projected expansion of finfish aquaculture in Ireland, some way of routinely providing synoptic maps of P. noctiluca distribution would clearly be useful (Doyle et al., 2008).
No incidences to date, although ballast water from commercial shipping constitutes a significant risk for transporting the species to new areas.
P. noctiluca outbreaks are characteristically boom and bust, although periods of exceptionally high abundance can span many consecutive years. The ability of the marine environment to recover after major outbreaks is not fully understood, yet it must be acknowledged that such events are natural occurrences so cannot in their own right be viewed as detrimental to their habitat.
Impact on Biodiversity
P. noctiluca predominantly feed upon a variety of zooplankton species that are highly abundant and not susceptible to long term depletion through predation. Of greater concern are the incidental fish kills within wild populations, which are yet to be estimated, and those associated with coastal aquaculture facilities where animals are constrained and unable to move away from the encroaching jellyfish aggregation.
Within the Mediterranean Sea, P. noctiluca outbreaks are responsible for the loss of millions of dollars to the combined tourist industries of national states bordering the western basin and Adriatic Sea. P. noctiluca may also cause fish mortalities in aquaculture cages possibly by irritating the fish gills (Merceron et al., 1995). For example, in November 2007, the only salmon farm in Northern Ireland lost its entire population of more than 100,000 fish, worth US $2 million through the encroachment of an enormous jellyfish aggregation (Doyle et al., 2008). This has led to the near collapse of the northern Irish finfish aquaculture industry, which had a lucrative export trade to across Ireland, the UK, continental Europe and the US.
The broader environmental impacts of P. noctiluca ‘outbreaks’ are not fully understood at present. However, care must be taken not merely to consider the species as a mere pest (which it is from our perspective) but an ancient and poorly understood component of pelagic food webs. What is of concern, however, is the potential for regime shifts within pelagic environments with large-scale removal of commercially valuable finfish (competitors with prey with jellyfish) has greatly expanded the niche that jellyfish can fill. In areas such as the Benguela upwelling off West Africa such shifts have already occurred, which even in the event of reduced commercial fishing effort, may prevent over-exploited fish stocks from re-establishing themselves.
The significant sting given by P. noctiluca prevents their utilization as a human (or animal) food source. However, there is some scope in exploring their use within cosmetic industries as many jellyfish are rich in type II collagen, which is a valuable commodity that is becoming increasingly harder to source from abattoir derived animal by-products (through tightening legislation). Interest has been expressed in other jellyfish species within the European Union, and trials are underway.
Aggregations are visually detectable and do not require diagnosis.
Jellyfish reporting programmes using the general public as observers have been used successfully in recent years throughout the Irish Sea. Stranding data were reported via an online reporting website. This proved extremely useful in identifying when a particular jellyfish species was present in an area or had moved into a previously unknown site and has wide applicability as an early warning mechanism.
Given the inferred role of currents in driving P. noctiluca distribution, oceanographic particle tracking models, which have been applied to various species in the North Atlantic (e.g. Hays and Marsh, 1997; Kettle and Haines, 2006) may have some utility for predicting the fate of oceanic P. noctiluca blooms and so provide an early warning-system for predicting deleterious coastal blooms. Indeed, a particle tracking model to track jellyfish around the waters of Shetland under an EU-funded research project called Eurogel has already been developed (Elzeir and Hay, 2005).
A second EU-funded project named Ecogel will commence in 2008 and run until 2012. A key aspect of this program will be to test the utility of aerial surveys to detect the presence of P. noctiluca prior to its arrival in economically important coast areas (i.e. those linked with significant income from tourism or aquaculture) following the established protocol of Houghton et al. (2006a).
The Ecogel programme will also attempt to unravel the climatic drivers (e.g. North Atlantic Oscillation) that lead to exceptional abundances of P. noctiluca in particular years. Such linkages have been shown for more coastal species of jellyfish (Lynam et al., 2005) but the typical offshore distribution and logistical demands of regular oceanic sampling have prevented bespoke investigations of P. noctiluca to date.
By similarity we hereby refer to open water species of gelatinous zooplankton that are periodically advected in coastal waters en mass or to truly invasive species (i.e. those operating beyond their native range) that impinge upon human activities in coastal waters (see Mills, 2001 for full review):
Apolemia uvaria along the Norwegian Coast
Båmstedt et al. (1998) reported an unusual mass occurrence of the virulent and very long siphonophore Apolemia uvaria along much of the Norwegian west coast beginning in November 1997 and lasting at least into February 1998. The primary effect reported of this invasion was killing of penned (farmed) salmon, although such high numbers of large siphonophores probably also preyed heavily on the coastal zooplankton community.
Nanomia cara in the Gulf of Maine
Twice in the last two decades, unusually high numbers of the siphonophore Nanomia cara have been reported by observers in manned submersibles in the Gulf of Maine (Rogers et al., 1978; Mills, 1995). The 1975 observations were corroborated by fishermen whose trawl nets were being clogged by the high numbers of siphonophores. The authors respectively reported maximum densities of 1–8 siphonophores per m3 in 1975–1976 and up to 50–100 per m3 (concentrated near the bottom) in 1992–1993. In both cases, access to submersibles for observations was limited and follow-up counts were not performed. It is not known if such high numbers of N. cara occur with some regularity or if some special ecological factors in the environment, for instance the poor fishing conditions of the early 1990s (resulting from decades of overfishing), might be related (Mills, 2001).
Medusae and ctenophores in the Black Sea
Pollution, eutrophication and many anthropogenic alterations of the natural environment have vastly altered the Black Sea and its adjacent Sea of Azov in the past 50 years (Zaitsev and Mamaev, 1997). This system provides the most graphic example to date of a highly productive ecosystem that has converted from supporting a number of valuable commercial fisheries to having few fishes and high numbers of ‘jellyfishes’ – medusae and ctenophores (Mills, 2001). By the 1960s, largely owing to the effects of pollution combined with over fishing, many of the native fishes in the Black Sea had become uncommon, including the jellyfish-eating mackerel Scomber scombrus. Perhaps directly related to the loss of this and other fishes, and to increasing eutrophication, the Black Sea has experienced severe outbreaks of three different species of ‘jellyfish’ in the past three decades (Zaitsev and Mamaev, 1997).
Chrysaora hysoscella and Aequorea aequorea populations in the Benguela Current, Southern Africa and Namibia
Similar increases in populations of Chrysaora hysoscella and Aequorea aequorea medusae are implied to have taken place in the Benguela Current off the west coast of Southern Africa during the 1970s (Fearon et al., 1992). The evidence in that case is circumstantial; in fact, the increase is hypothesized only in that these prominent members of the 1980s Benguela Current plankton did not even appear in comprehensive data records from the 1950s and 1960s, and thus their populations are assumed to have previously been very low or nonexistent. High numbers seen in the 1970s have persisted through the 1980s and into the late 1990s off Namibia where both species are still abundantly present, to the point of negatively impacting the fishing industry (Sparks et al., 2001; Lynam et al., 2006).
Rhopilema nomadica in the Eastern Mediterranean
R. nomadica is a large (up to 80 cm diameter) scyphomedusa that has become increasingly abundant in the eastern Mediterranean over the past two decades (Lotan et al., 1992). Like P. noctiluca, R. nomadica’s presence creates an environmental hazard to fishermen and bathers alike, because it has an unpleasant sting and can be present in such large numbers as to clog fishing nets. First recorded in 1976 in the Mediterranean, the origin of this new hazardous jellyfish is surprisingly unclear. Although assumed to have arrived via the Suez Canal, R. nomadica is rare in the Red Sea and is not known from elsewhere [it was only recently described, after its arrival to the Mediterranean (Galil et al., 1990)]. Its reproductive potential in the eastern Mediterranean appears to be very high (Lotan et al., 1992) and it has been present in large numbers off the coast of Israel every summer since 1986 (Lotan et al., 1994).
Stomolophus nomurai in the Sea of Japan
Shimomura (1959) described a very large bloom of very large rhizostome medusae, Stomolophus nomurai, in the Sea of Japan in 1958. This species seems to be tolerant of a wide temperature range, occurring that year in temperatures from 12–28oC, and the bloom extended from the Sea of Japan even to waters off Hokkaido. The bloom, which was a serious fisheries nuisance, lasted well into the winter, ending in December in the Sea of Japan and in January on the Pacific side of Japan. Individual medusa were to 200 cm in diameter, weighed up to 40 kg, and were visible every few metres of surface at peak abundance. Fishermen are reported to have caught 20,000–30,000 S. nomurai medusae per day during the yellow tail fishery in October and November 1958. While Shimomura (1959) reported that local occurrences of this species occur most years, he also cited a bloom of similar magnitude from 20 years earlier, when hindsight indicates that it signaled a regime shift and the end of a several-year sardine peak. Another very large and unpredicted bloom of S. nomurai occurred in the Sea of Japan in 1995, with small numbers seen also in 1972 and 1998 (Mills, 2001). The biology of this species is so little known that the whereabouts of the polyps and whether or not there is a small annual production of medusa somewhere is not known (Mills, 2001).
P. noctiluca is driven into areas that impinge on human coastal activities (tourism, coastal fisheries, aquaculture) by a combination of hydrographic and meteorological conditions. Such broad scale factors are not possible to control and, as such, preventive measures can only focus on inshore mitigation of detrimental effects on coastal communities.
From the Costa del Sol in Spain to the French Riviera, P. noctiluca infestations have forced seaside resorts to set up defences to repel the jellyfish and protect the tourist industry. The city of Cannes on the Côte d’Azur employs a floating barrier to block the swarms of jellyfish that inflicted painful stings on thousands of bathers around the Mediterranean during 2007. In Spain, a network of volunteers with boats has been recruited for a pre-emptive effort to prevent encroachment of P. noctiluca in coastal waters, whereby aggregations are scooped up and deposited in deeper water.
During ‘outbreak years’ the sheer scale of P. noctiluca aggregations prevents eradication on all but the smallest localized scales. However, as the species causes problems on the periphery of its natural range it cannot be viewed as a typical invasive species that requires eradication given that our understanding of its ecosystem role is currently very poor.
Within the Mediterranean Sea the use of offshore nets to protect bathers and the economic interests of coastal communities are currently under trial. In Ireland, trials will commence in early 2009 to explore the use of bubble nets / curtains to protect fish farms under the Ecogel programme and through a project funded by the Irish Marine Institute in Galway.
Cultural control and sanitary measures
Coastal eutrophication is a major factor driving an increase in coastal phytoplankton and hence zooplankton production, particularly in areas of high tourist activity (e.g. the Mediterranean Sea). Increased zooplankton biomass can subsequently support the high numbers of P. noctiluca in ‘outbreak years’. Decreased input of nitrates and phosphates as runoff into coastal waters would be beneficial in reducing the abundance and carrying capacity of zooplankton populations (jellyfish prey) imparting increased bottom-up control (i.e. food limitation) on P. noctiluca aggregations.
See section on Containment and Zoning.
Broad distribution throughout oceanic waters and semi-enclosed seas (e.g. Mediterranean Sea) render movement control impossible. Particular attention must be paid to the potential of commercial shipping to transport P. noctiluca to new areas through ballast water expulsion. On a localized scale (particularly in the vicinity of coastal aquaculture facilities) further work is required on preventing large aggregations of P. noctiluca from entering sensitive coastal areas. Incidental reports suggest that nets provide limited utility as medusa may be as small as several millimeters, whilst air bubble nets and curtains (although promising) require further investigation.
The extensive scale of P. noctiluca invasions into coastal waters, and extraordinary abundance of individuals renders biological control impossible.
Control by utilization
There is some scope for exploring the use of P.noctiluca as a source of type II collagen for use in the cosmetics industry. The volatile sting that characterises the species renders it unsuitable for human consumption.
Monitoring and Surveillance
The Ecojel EU funded programme in the Irish Sea will test the utility of aerial surveys to identify the location of harmful blooms of P. noctiluca in offshore areas prior to their encroachment into economically sensitive coastal areas. Ship-borne plankton surveys and particular tracking models will also be used to understand the transport of the species from its more typical oceanic habitat. Once it is possible to correlate P. noctiluca with particular oceanic water masses there is additional scope for using remote sensing techniques to identify / predict problem years.
Mitigation trials will begin in early 2008 as collaboration between Queen’s University Belfast and University College Cork, and the Northern Salmon Company Ltd (County Antrim, Northern Ireland) to look at an array of potential methods for preventing major fish kills with coastal aquaculture facilities. Extensive trials to mitigate the effects of P. noctiluca blooms on tourist activities are underway at numerous locations throughout the Mediterranean Sea.
There is no evidence to suggest that P. noctiluca outbreaks cause irrevocable harm to the coastal ecosystems they periodically encroach upon. However, a reduction in fishing effort would potentially provide enhanced competition for the jellyfish although no specific recommendations relating to this can be made within the context of this document.
Given an apparent synchrony between outbreaks in the Mediterranean and North East Atlantic waters north of Ireland efforts must be made to understand the broad scale climatic drivers of such events. Molecular studies must also seek to elucidate the potential link between these two problematic sites given that P. noctiluca is considered a member of the ‘Lusitanian fauna’ which originates in the outflow from the Mediterranean and is modified through admixture with fauna from the Azores and Bay of Biscay on its course to the NE Atlantic.