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

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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.
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Aquatic Invasions (2007) Volume 2, Issue 3: 185-189
DOI 10.3391/ai.2007.2.3.5
© 2007 The Author(s)
Journal compilation © 2007 REABIC (http://www.reabic.net
)
This is an Open Access article
185
Research article
The presence of the ctenophore Mnemiopsis leidyi in the Oslofjorden and
considerations on the initial invasion pathways to the North and Baltic Seas
Otto M. P. Oliveira
Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, R. Matão, Trav. 14, 101, 05508-900, São Paulo,
SP, Brazil and Centro de Biologia Marinha, Universidade de São Paulo, Rodovia Manoel H. do Rego km 131,5, 11600-000, São
Sebastião, SP, Brazil
Email: ottompo@usp.br
Received 22 May 2007; accepted in revised form 8 August 2007
Abstract
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.
Key words: Ctenophora, invasive species, ballast water, North Atlantic Current, transoceanic spread
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 and
Reeve 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 and Niermann
Otto M. P. Oliveira
186
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, appa-
rently 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 intro-
duced 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). Nowa-
days, 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 and Bayha
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).
Water surface temperatures at the register
locations were obtained from Bundesamt für
Seeschifffahrt und Hydrographie (2007) and
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).
Discussion
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.
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 popu-
lation in the Oslofjorden. However, it is unclear,
Mnemiopsis leidyi in the Oslofjorden
187
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)
Otto M. P. Oliveira
188
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 tempera-
tures of more than 2°C in the last five years
(Hughes and Holliday 2006). Possibly the low
temperatures, a major factor against the trans-
oceanic 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 and Bayha 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
Acknowledgements
I gratefully acknowledge the two anonymous
referees for their important suggestions and
contributions, and two divers Asbjørn Hansen
and Vidar Aas for allowing the use of their
photos. This study was supported by FAPESP
(Proc. 2004/15300-0).
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Annex
Records of the ctenophore Mnemiopsis leidyi in the Oslofjorden waters
Location coordinates
Location
Latitude,°N Longitude,°E
Date of record
Water
temperature
*
Figure Photographer
Bjørnemyrdalen,
Akershus
59º50'40" 10º38'40" November 14, 2005 ~10°C
1A
Vidar Aas
Fjellstrand,
Akershus
59º48'18" 10º36'24" November 14, 2005 ~10°C
1B
Vidar Aas
Pumpehuset,
Drøbak
59º39'00" 10º36'00" November 17, 2005 ~10°C
1C
Asbjørn Hansen
Fabrikken,
Hvitsten
59º35'00" 10º39'00" November 20, 2005 ~7°C
1D
Asbjørn Hansen
Svestad,
Akershus
59º46'50" 10º35'38" May 5, 2006 ~11°C
1E
Vidar Aas
Alvern, Akershus 59º49'06" 10º36'04" November 16, 2006 ~9°C
1F
Vidar Aas
Alvern, Akershus 59º49'06" 10º36'04" March 20, 2007 ~4°C
1G
Vidar Aas
* Approximated values for water surface temperature, based on Bundesamt für Seeschifffahrt und Hydrographie (2007)
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... All these ecosystems underwent over the recent decades the significant changes of structure and functionality due to the climate warming impact and anthropogenic disturbances. Each of these ecosystems has been invaded by M. leidyi (Studenikina et al., 1991;Shiganova, 1993;Ivanov et al., 2000;Shiganova et al., 2001;Shiganova et al., 2004aShiganova et al., , 2004bShiganova et al., , 2004cJavidpour et al., 2006;Faasse and Bayha, 2006;Boersma et al., 2007;Tendal et al., 2007;Oliveira, 2007;Boero et al., 2009;Fuentes et al., 2009;Galil, 2009;Antajan et al., 2014). (See Table 2.) ...
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