The presence of the ctenophore Mnemiopsis leidyi in the Oslofjorden and considerations on the initial invasion pathways to the North and Baltic Seas

The ctenophore Mnemiopsis leidyi is one of the most cited invasive species due to its ecological and economical impact that occurred in the Black and Caspian Seas in previous years. Recent reports on the species presence in the Baltic and North Seas alarmed the scientific community. While the earliest report of M. leidyi in the Baltic was spring 2006, this paper indicates of the presence of M. leidyi in the Oslofjorden as early as autumn 2005, and discusses the possible invasion routes from its native range along the eastern coast of the Americas.


Introduction
Mnemiopsis leidyi A. Agassiz, 1865 is a lobate ctenophore, originally distributed along the American coast of the Atlantic, from Narragansett Bay, USA (41°N) to the Valdez Peninsula, Argentina (42°S) (GESAMP 1997).The species is a simultaneous hermaphrodite, able to perform self-fecundation (Oliveira and Migotto 2006) and can live and reproduce in a wide salinity and temperature range (Baker andReeve 1974, GESAMP 1997), inhabiting both coastal and estuarine waters (GESAMP 1997).Feeding mainly on copepods, fish eggs and larvae (Burrell and Van Engel 1976), M. leidyi populations rapidly grow when food is abundant (cf.Purcell et al. 2001).
In the early 1980's, M. leidyi was introduced in the Black Sea, possibly transported from its native area in ships ballast water (cf. GESAMP 1997).Due to suitable living conditions in the receiving environment (food abundance and a physical environment similar to the estuaries in the native region), populations established and grew in the Black Sea (Purcell et al. 2001, Shiganova et al. 2001).The absence of potential predators and the favorable environmental conditions allowed M. leidyi to spread along the Black Sea and adjacent areas, as the Azov, Marmara and northeastern Mediterranean Seas (GESAMP 1997, Shiganova et al. 2001, Kideys 2002).The invasion of the Caspian Sea occurred in the mid of the 1990's.The species was likely transported in ballast water through the Volga-Don Channel (Kideys 2002, Bilio andNiermann 2004).Population explosions in the Black Sea were observed in 1989 and 1995 (Shiganova et al. 2001), a time period when fisheries of anchovies drastically decreased in the area, apparently due to trophic competition and feeding on eggs and larvae by M. leidyi (GESAMP 1997).Overfishing and increased water pollution have also contributed to the decline of the Black Sea fisheries.
In the late 1990's, another ctenophore, Beroe ovata Chamisso & Eysenhardt, 1821 (a natural predator of M. leidyi), was accidentally introduced to the Black Sea.Its predatory behavior resulted in a biological control of the M. leidyi population and an environmental equilibrium (Shiganova et al. 2001, Kideys 2002).Nowadays, M. leidyi populations are still affecting the environmental equilibrium in the Caspian Sea, due to the absence of the predator B. ovata there (Stone 2005).
The recent reports on the M. leidyi presence in the Baltic (Javidpour 2006, Hansson 2006, Kube et al. 2007) and North Sea (Faasse andBayha 2006, Boersma et al. 2007) alarmed the scientific community, since those are some of the most productive fishery areas of the world.The region presents large rates of catch on planktotrophic fishes as herrings (Jansson 2003, Sea Around Us Project 2007), which were probably the most affected organisms by M. leidyi populations explosions in the Black Sea.Along the Dutch coast, sole and plaice fisheries are also potentially threatened during high abundances of M. leidyi (Faasse and Bayha 2006).
This study presents new records of M. leidyi for the Oslofjorden (Norway) and discusses possible invasion routes from its native range along the eastern coast of the Americas.

Materials and Methods
Mnemiopsis leidyi specimens were photographed underwater by two divers in the Oslofjorden between November 2005 and March 2007 (see Annex).Photos were taken in dives up to 10 m depth.Most of the register locations are on the east side of the fjord (except for the Pumpehuset, Drøbak register), areas constantly affected by inflow streams with higher temperatures (see Meteorologisk Institutt 2007).

Results
All M. leidyi specimens photographed were adults, with a least 40 mm in length, biggest up to 80 mm.The position of the lobes insertion, near the aboral end of the body, attests the identification of the species (see Figure 1).
One of the divers (Vidar Aas) goes into water weekly, from March to November, every year.He observed more specimens in each location and in other occasions than that when they were photographed.However, dense agglomerations of adult comb-jellies were never observed in those locations.
At the register moments, water surface temperatures ranged from 4-11°C (Annex).Faasse and Bayha (2006) reported the presence of M. leidyi in the Netherlands estuarine regions and suggested that this species may have occurred in the area for several years, being misidentified as Bolinopsis infundibula (O.F.Müller, 1776), another lobate ctenophore.The authors also suggested that the resident population from Dutch estuaries could serve as a yearly supply of M. leidyi to the Baltic Sea, through Skagerrak and Kattegat or through the Kiel Canal, if the species was unable to overwinter in the Baltic (Faasse and Bayha 2006).Hansson (2006) agreed with the hypothesis of an annual reintroduction in the Baltic Sea originating from the North Sea.However, Kube et al. (2007) data suggested that M. leidyi survived the last winter in the southern Baltic Sea.

Discussion
The specimens observed in the Oslofjorden in different localities and occasions (see Figure 1, Annex), are well developed adults, suggesting that reproduction could have been occurring in the Oslofjorden.However, I cannot infer that the Oslofjorden population of M. leidyi survived the winters, once temperature reached about 1°C or lower in these periods (Bundesamt für Seeschifffahrt und Hydrographie 2007).A low temperature of that magnitude kills the Azov Sea population of M. leidyi every winter and the sea is reinvaded by Black Sea specimens in spring (Studenikina et al. 1991).It is therefore possible that the Faasse and Bayha (2006) hypothesis of annual reintroduction is correct for the population in the Oslofjorden.However, it is unclear, for instance, if the annual reinvasion of the Oslofjorden population originates from Baltic or the North Sea comb jelly populations.
Regarding the possible transport of M. leidyi from the native areas to the North and Baltic Seas, Faasse and Bayha (2006) suggest the possibility of the ballast water transfer once two of the largest European ports (Antwerp and Rotterdam), are near to the Dutch estuaries where they found M. leidyi.However, I believe that a discussion on natural oceanic transport, by the North Atlantic Current (NAC) should be considered.A recent study shows that surface water temperature of the North Atlantic, including the NAC, was more than 1°C warmer in the last five years than the historical means (cf.Hughes and Holliday 2006).The superficial waters of NAC arrive in the UK coast and in the North Sea with mean temperatures above 9°C (Hughes and Holliday 2006).The North Sea also presented an increase in mean water temperatures of more than 2°C in the last five years (Hughes and Holliday 2006).Possibly the low temperatures, a major factor against the transoceanic spread of M. leidyi, has not been the problem in recent years due to water temperature increase in NAC and in the recipient regions.
Mnemiopsis leidyi is known as a coastal ctenophore (GESAMP 1997, Mianzan 1999).However, there are some specimen records in oceanic waters (Harbison et al. 1978), including localities inside the inflow of the Gulf Stream (see collecting stations 509, 510 and 584 in Harbison et al. 1978).This certainly indicates the potential of transoceanic spreading of M. leidyi.The drifting from the northern Gulf Stream to the North Sea, through NAC, can least 15 to 60 days, depending on the season and wind oscillations (cf.Siedler et al. 2001).In a recent study, adult specimens were able to live up to 17 days under starvation in the laboratory (Oliveira 2007).In natural conditions of a transoceanic current, it is not expected that coastal species have an adequate food supply as natural coastal waters prey organisms are either absent or occur in much lower abundance.However, considering the M. leidyi predatory potential and trophic plasticity, I expect this ctenophore to be capable of such a way of dispersal.Furthermore, this transoceanic spread hypothesis needs to be tested.
The absence of M. leidyi records on the U.K. coast, as well as in the Atlantic coasts of France and Spain, are negative arguments for such hypothesis.However, the species could just have been misidentified as Bolinopsis infundibula in the area, as previously occurred in other European seas (Faasse andBayha 2006, Boersma et al. 2007).Samplings on the NAC, associated with molecular identification of M. leidyi lineages should be of great value to elucidate this question.
The presence of M. leidyi have been recorded for several points along the North and Baltic seas (see Kube et al. 2007, Figure 3), proving once more the species great spreading potential.Now, studies on its trophic interaction with native plankton organisms of such regions are strongly needed to evaluate its possible ecological and economical impacts

Figure 1 .
Figure 1.Mnemiopsis leidyi from the Oslofjorden, Norway.A-D, specimens observed in November, 2005; E, specimen observed in May, 2006; F, specimen observed in November, 2006; G, specimen observed in March, 2007.Arrows indicate the position of the lobes insertion, near the aboral end of the body in M. leidyi, a distinctive characteristic from Bolinopsis infundibula (other lobate ctenophore that also occurs in the Oslofjorden).Photos by Vidar Aas (A-B, E-G) and Asbjørn Hansen (C-D).