The highly toxic and cryptogenic clinging
jellyﬁsh Gonionemus sp. (Hydrozoa,
Limnomedusae) on the Swedish west coast
Annette F. Govindarajan
*, Björn Källström
*, Erik Selander
and Thomas G. Dahlgren
1Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
2Department of Marine Sciences, University of Gothenburg, Göteborg, Sweden
3GGBC Gothenburg Global Biodiversity Centre, Göteborg, Sweden
4Gothenburg Marine Biological Laboratory, Göteborg, Sweden
5Evolutionary Biology Centre, EBC, Department of Organismal Biology, University of Uppsala,
6NORCE Norwegian Research Centre, Bergen, Norway
*These authors contributed equally to this work.
The clinging jellyﬁsh Gonionemus sp. is a small hydromedusa species known
historically from the Swedish west coast but not reported in recent times. This
species is thought to be native to the northwest Paciﬁc where it is notorious
for causing severe stings in humans and is considered invasive or cryptogenic
elsewhere. This year, unlike in the past, severe stings in swimmers making contact
with Gonionemus sp. medusae occurred in Swedish waters from a sheltered eelgrass
bed in the inner Skagerrak archipelago. To the best of our knowledge, this is
only the second sting record of Gonionemus sp. from the Northeast Atlantic—with
the ﬁrst record occurring off the Belgian coast in the 1970s. Stinging Gonionemus
sp. medusae have also been recently reported from the northwestern Atlantic
coast, where, like on the Swedish coast, stings were not reported in the past.
We analyzed sea surface temperature data from the past 30 years and show that
2018 had an exceptionally cold spring followed by an exceptionally hot summer.
It is suggested that the 2018 temperature anomalies contributed to the Swedish
outbreak. An analysis of mitochondrial COI sequences showed that Swedish
medusae belong to the same clade as those from toxic populations in the Sea of
Japan and northwest Atlantic. Gonionemus sp. is particularly prone to human-
result of anthropogenic factors either through a climate-driven northward
range shift or an introduction via shipping activity. We examined medusa growth
rates and details of medusa morphology including nematocysts. Two types of
penetrating nematocysts: euryteles and b-mastigophores were observed, suggesting
that Gonionemus sp. medusae are able to feed on hard-bodied organisms like
copepods and cladocerans. Given the now-regular occurrence and regional spread
of Gonionemus sp. in the northwest Atlantic, it seems likely that outbreaks in
Sweden will continue. More information on its life cycle, dispersal mechanisms,
and ecology are thus desirable.
How to cite this article Govindarajan AF, Källström B, Selander E, Östman C, Dahlgren TG. 2019. The highly toxic and cryptogenic
clinging jellyﬁsh Gonionemus sp. (Hydrozoa, Limnomedusae) on the Swedish west coast. PeerJ 7:e6883 DOI 10.7717/peerj.6883
Submitted 18 January 2019
Accepted 1 April 2019
Published 13 May 2019
Thomas G. Dahlgren,
Additional Information and
Declarations can be found on
2019 Govindarajan et al.
Creative Commons CC-BY 4.0
Subjects Biodiversity, Biogeography, Marine Biology, Taxonomy, Zoology
Keywords Sea grass, Zostera, Taxonomy, Biogeography, Climate change, Burn, Nematocyst,
Ultrastructure, Microscope, Tentacle
There is increasing concern over the highly toxic cryptogenic clinging jellyﬁsh Gonionemus
sp. (Hydrozoa, Limnomedusae) due to outbreaks in scattered temperate coastal areas
worldwide, where the jellyﬁsh are either previously unrecorded, or where they have not
been observed for decades (Rodriguez et al., 2014;Govindarajan & Carman, 2016;Gaynor
et al., 2016;Govindarajan et al., 2017;Marchessaux et al., 2017). These hydromedusae
can have a potent sting that causes severe pain and other symptoms to humans (Pigulevsky &
Michaleff, 1969;Otsuru et al., 1974;Yakovlev & Vaskovsky, 1993;Govindarajan &
Carman, 2016;Marchessaux et al., 2017). As well, they can be lethal to their predators
(Carman, Grunden & Govindarajan, 2017).
It appears likely that the current Gonionemus outbreaks are facilitated by anthropogenic
transport (Govindarajan & Carman, 2016;Marchessaux et al., 2017). The adult Gonionemus
medusae which reach approximately three cm in diameter, have adhesive structures
positioned toward the distal ends of their tentacles (Edwards, 1976), which they use to
cling to the eelgrass such as Zostera marina (Perkins, 1903;Uchida, 1976). Thus, while the
medusa occasionally swim out of the eelgrass meadows, natural or anthropogenic medusa
dispersal, while possible, may not be the primary mechanism for its spread. Gonionemus
sp. has a complex life history that includes minute benthic asexual stages (Perkins, 1903;
Kakinuma, 1971;Uchida, 1976) that may be amenable to human-mediated transport on ship
hulls (Tambs-Lyche, 1964), shellﬁsh (Edwards, 1976), and debris (Choong et al., 2018).
An understanding of the dispersal history and spread of clinging jellyﬁsh has been
hampered by a complex taxonomic history. The name Gonionemus vertens Agassiz, 1862
has been used recently to refer to “clinging jellyﬁsh”from throughout the northern
hemisphere but was originally described from material collected in Puget Sound, the
North East Paciﬁc(Agassiz, 1862). In the Atlantic the clinging jellyﬁsh were originally
described as G. murbachii Mayer, 1901, and were considered distinct from G. vertens
(Mayer, 1901). They were later synonymized (Kramp, 1959) and the Atlantic populations
were hypothesized to have been founded by anthropogenic introductions from the Paciﬁc
(Tambs-Lyche, 1964;Edwards, 1976;Bakker, 1980), although this was not accepted
by all. Based on consistent morphological characters, some authors either maintained
the murbachii name (Rottini, 1979) or considered the two forms to be subspecies
(Naumov, 1960). Govindarajan et al. (2017) found that differences in mitochondrial COI
sequences were also consistent with the vertens—murbachii forms; but noted that these
differences do not correspond to the Atlantic—Paciﬁc division suggested by Naumov
(1960). Owing to their episodic nature and the lack of continuity in observations
of late 19th and early 20th century G. murbachii and contemporary populations in the
G. murbachii type locality, Govindarajan et al. (2017) conservatively referred to the more
toxic, putative murbachii lineage as Gonionemus sp. until the taxonomy can be
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 2/18
Gonionemus sp. has been previously reported from Scandinavian and North Sea waters
(reviewed in Bakker, 1980;Wolff, 2005), but we are not aware of any stings associated
with past observations. Here, using morphological and molecular evidence, we document
blooms of the highly toxic lineage Gonionemus sp. in the summer of 2018 associated with a
sheltered eelgrass (Z. marina) bed on the Swedish west coast. We report the ﬁrst case
of a Gonionemus sp. envenomation in Scandinavian waters and discuss the possible origins
of these apparently new and highly toxic Gonionemus sp. populations. We also suggest that
warmer than average sea surface temperatures may have contributed to the 2018
Gonionemus sp. outbreaks.
MATERIALS AND METHODS
Sample collection and field observations
The ﬁrst reports of an unknown stinging medusae came from swimmers through media
on 27th July 2018 (SVT, 2018). Several swimmers had been stung at Knuten on the
Figure 1 Map of the study area indicating new records of Gonionemus sp. Red dots are records
associated with stings. Historical records of Gonionemus sp., which are not associated with stings,
indicated by blue dots. The blow up shows the area on the Swedish coast where stinging Gonionemus
were found during 2018. Near the location where they were found are two international harbors, shown
as black ﬁlled triangles. The sea surface temperature monitoring station in Åstol is indicated by a star.
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 3/18
northeastern (leeward) side of the island Tjörn (58.0782N; 11.7065E, Fig. 1). On two
occasions, the 2nd and 18th of August, we sampled medusae by snorkeling in the eelgrass
bed with a small hand-held net (120 150 mm, mesh size 0.5 mm; JBL GmbH & CO,
Neuhofen, Germany). Medusae were transported live in aerated 20 l tanks to the
laboratory for analysis and maintained on a diet of copepods and frozen Artemia naupli
larvae, fed once every day. Samples were preserved in 96% ethanol for DNA analysis.
Medusa size and nematocyst identifications
The diameter of the Gonionemus medusae was measured by imaging the uncontracted
medusae when resting on the bottom of a white plastic box with 50 mm of natural sea water
using a DSLR camera (Nikon D7100; Nikon Corporation, Tokyo, Japan). A plastic
millimeter ruler in the box was used for reference to measure the bell diameter in Image J
(Schneider, Rasband & Eliceiri, 2012). Some of the Gonionemus medusae and their
nematocysts were examined and photographed with a Leica M205C (Leica Microsystems,
Wetzlar, Germany) stereomicroscope and a Leitz DMRBE (Leica Microsystems,
Wetzlar, Germany) light microscope (LM) equipped with interference-contrast optics,
100/1.30 PL, ﬂuotar objectives. Both microscopes were connected to the digital photo
equipment Leica application suite, version 3.8 (LAS V3.8). Measurements on different
medusa structures were made in the stereomicroscope, and measurements on the
nematocysts were made from the LM using live tissue carefully squashed under a cover
glass. All pictures and measurements are from living hydromedusae.
The nematocysts were identiﬁed by size, structure and shape of their undischarged
and discharged capsule and shaft, and on the spine-pattern of the shaft. The classiﬁcation
system and nematocyst nomenclature of Östman (2000, and references therein)
Sea surface temperature data were downloaded from the Swedish repository for
environmental monitoring data (Swedish Meteorological and Hydrological Institute
(SMHI), 2018). The closest monitoring station with sufﬁcient resolution and duration was
“Åstol,”23 km from the collection site (57.922N; 11.590E, Fig. 1). Sea surface
temperature from 1986 to 2018 was binned into monthly averages. The monthly mean
temperatures for 2018 were graphically superimposed to identify anomalies.
Molecular procedures and analyses were conducted at the Woods Hole Oceanographic
Institution (Woods Hole, MA, USA) except where indicated. Genomic DNA was
extracted from 15 preserved hydromedusae collected from the leeward side of Tjörn
Island, Skåpesund (Fig. 1) using a DNeasy Blood & Tissue Kit (Qiagen, Los Angeles,
CA, USA) according to the manufacturer’s protocol. A ∼650 base pair portion of the
mitochondrial COI gene was ampliﬁed and sequenced using primers from Folmer et al.
(1994) using the approach described in Govindarajan et al. (2017). PCR conditions were
3 min at 95 C; 35 cycles of 95 C30s;48C30s,72C 1 min; and 5 min at 72 C.
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 4/18
PCR products were visualized on a 1% agarose gel stained with GelRed, puriﬁed with
QIAquick PCR Puriﬁcation Kit (Qiagen, Los Angeles, CA, USA) according to the
manufacturer’s protocol, and quantiﬁed using a NanoDrop 2000 spectrophotometer
(Thermo Fisher Scientiﬁc, Waltham, MA, USA). Puriﬁed products were sequenced in both
directions (Euroﬁns, https://www.euroﬁns.com/). An additional specimen was ampliﬁed
using a similar protocol in Sweden and sent for sequencing using the GATC LightRun
Barcode service (www.euroﬁnsgenomics.eu). Sequence chromatograms were evaluated
and assembled using Geneious version 9.0.5 (https://www.geneious.com/). Assembled
sequences were aligned with sequences representing the seven haplotypes in Govindarajan
et al. (2017;Table 1). Representatives of additional haplotypes from Gonionemus sp.
sequences that were deposited on GenBank after Govindarajan et al. (2017) were identiﬁed
in a preliminary alignment and were then added to the alignment dataset with the
Swedish sequences. Alignments were conducted using Clustal W (Larkin et al., 2007)in
the Geneious platform with default parameters. The alignments were conﬁrmed by eye
and the ends were trimmed to 501 base pairs to standardize sequence length and facilitate
a direct comparison with the analysis conducted by Govindarajan et al. (2017) and the new
GenBank sequences that were also that length. Neighbor-joining trees based on Kimura
two-parameter distances (to be consistent with previous analyses; Zheng et al., 2014;
Table 1 Gonionemus sp. COI haplotypes.
Haplotype Genbank accession
Known localities References
Haplotype 1 KF962139 China (unspeciﬁed) He et al., unpublished GenBank entry
Haplotype 2 KY437853 Paciﬁc coast of Japan; Yellow Sea Govindarajan et al. (2017)
Haplotype 3 KY437979 Sea of Japan (Vostok Bay) Govindarajan et al. (2017)
Haplotype 4 KY437944 Sea of Japan (Vostok Bay, Amur Bay); Paciﬁc
coast of Japan; Northwest Atlantic coast of
USA (New Hampshire, Massachusetts,
Rhode Island, Connecticut); Sweden
Govindarajan et al. (2017); This study
Haplotype 5 KY437888 Northwest Atlantic coast of USA
(Massachusetts, New Hampshire)
Govindarajan et al. (2017)
Haplotype 6 KY437842 Northwest Atlantic coast of USA
(Massachusetts, Rhode Island, Connecticut)
Govindarajan et al. (2017)
Haplotype 8 MK158933 Sweden This study
Haplotype 9 MK158944 Northwest Atlantic coast of USA; Sweden This study
Haplotype 10 MH020743 China (Yellow Sea) Liu & Dong, unpublished GenBank entry
Haplotype 11 MH020707 China (Bohai Sea) Liu & Dong, unpublished GenBank entry
Haplotype 12 MH020652 China (unspeciﬁed) Liu & Dong, unpublished GenBank entry
Haplotype 13 MH020717 China (Yellow Sea) Liu & Dong, unpublished GenBank entry
Haplotype 14 MH020722 China (Yellow Sea) Liu & Dong, unpublished GenBank entry
Haplotype 15 MH020725 China (Yellow Sea) Liu & Dong, unpublished GenBank entry
Haplotype 16 MH020640 China (unspeciﬁed) Liu & Dong, unpublished GenBank entry
Known haplotypes of Gonionemus sp. COI and locations where they have been documented. The GenBank accession numbers are for the representative sequences used to
construct the neighbor—joining tree in Fig. 6.
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 5/18
Govindarajan et al., 2017) were constructed using PAUP4(Swofford, 2003) accessed
Sample collection and field observations
Medusae were collected at two occasions from the Skåpesund location (Fig. 1) and
identiﬁed morphologically as Gonionemus sp. (Fig. 2). Medusae possessed adhesive pads
characteristic of the genus Gonionemus located toward the distal ends of their tentacles
Figure 2 Gonionemus sp. Macromorphology of medusae and tentacles. Medusae in apical dorsal
(A–C), lateral (D and E), and oral ventral view (F and G), showing gonads, radial canals, ring-canal,bell-rim
ﬂaps/lappets, statocysts, manubrium, tentacles with nematocyst batteries and adhesive pads, tentacle base
tentacle with tentacle-canal and yellow streak, and velum. Abbreviations: arrows, point at adhesive pads;
brf, bell-rim ﬂap/lappet; gmd, developing male gonad; gf, female gonad; m, manubrium; rac, radial canal;
ric, ring-canal; s,statocyst;sto, stomach; stoa, stomach attachment; tb, tentacle base;tc,tentacle-canal;
v, velum; ys, yellow streak. Photo credits: Carina Östman (A–F), Ulf Jondelius (G).
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 6/18
(Figs. 2 and 3, more detailed morphology in Figs. S1–S6), which allow them to “cling”
to the eelgrass. Similar to Gonionemus sp. from the Northwest Atlantic, Northwest Paciﬁc,
and the Sea of Japan (Kakinuma, 1971;Govindarajan et al., 2017), medusae were relatively
ﬂat and had relatively thin, dull orange—brown gonads.
One of us (BK) was stung several times while skin diving on the ﬁrst sampling date.
The stings left red marks at the site of contact and produced marked pain for several hours
and feelings of unease throughout the ﬁrst night afterward. As reported elsewhere
(Pigulevsky & Michaleff, 1969) stinging sensations where felt throughout the night even at
places on the body where no direct contact had occurred. Local newspapers also reported
stings in other swimmers, with similar outcomes and in a few cases the victims had
strong reactions that demanded medical attention (Aftonbladet, 2018).
Medusa size distributions
Our size distribution data were limited to two points in time, not including the time
of medusa release or the time of disappearance. This restrained our ability to assess the
growth rate. The data we obtained on the Gonionemus sp. population indicated slight
growth over the 16-day period between sampling dates (p< 0.001, Fig. 4). At the initial
time point, the mean diameter was 9.8 ± 2.7 mm. A total of 16 days later, at the second time
point, the mean size was 11 ± 1.8 mm suggesting an average growth rate of 0.08 mm
Detailed medusa and nematocyst morphology
Gonionemus sp. possesses a well-developed transparent velum (inward projecting rim
of tissue; Figs. 2A–2D). Four narrow radial canals form a noticeable cross centrally inside
the subumbrella cavity (Figs. 2B and 2C). The stomach with connecting manubrium
(tube-like projection with the mouth) is centrally attached to the cross-region of the
radial canals (Figs. 2B–2D). The gonads are arranged along most of the length of the radial
canals (Figs. 2A,2B and 2D). Mature female gonads are light yellow-brown; each gonad is
folded into six to eight broad bulbs (Fig. 2A;Figs. S5A–S5D). In the folds between the
gonad-bulbs, pores are present, from which eggs are ejected. The male gonads are darker
brownish-red and each folded into 9–13 smaller bulbs (Figs. 2B and 2D;Figs. S6A–S6D).
As the gonads mature, more and larger gonad-bulbs are developed.
Around 45–58 slender tentacles are attached to the subumbrella rim close to the ring
canal, which surrounds the bell close to the velum (Figs. 2A–2G). Contracted tentacles
are stubby (Fig. 2D) and are less than half the length of extended tentacles (Figs. 2F and 2G).
Close to or at a short distance from the tentacle tip, a small bending is present on each
tentacle, caused by the presence of an adhesive pad (Figs. 2D,2F and 2G). The adhesive pad
is located to one side of the tentacle and causes the tentacle to bend, thus pointing outward
(Figs. 2A,2F and 2G, detailed view in Fig. 3A–3C). One or two statocysts are present between
each tentacle pair (Fig. 2E;Fig. S2F).
The gracile tentacles are in their mid-region black colored along most of their length
(Figs. 3A–3C) and are armed with ring-shaped nematocyst batteries. Batteries with closely
packed nematocysts form rings around the tentacle (Fig. 3A). Small patches of nematocysts
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 7/18
Figure 3 Gonionemus sp. Micromorphology of tentacles and nematocysts. (A–C) Tentacle parts with
nematocyst batteries and adhesive pads. Note dark pigmented mid-line in tentacles, yellow-reddish
pigments in batteries and around adhesive pad. (Inset B) LM. Euryteles, note shaft and tubule. (D–K)
LMs. Tentacle nematocysts. Undischarged and discharged microbasic euryteles and small microbasic
b-mastigophores. Note shaft, tubule, lid and apical capsule opening (). (E) Microbasic eurytele with
broad, rod-shaped shaft, pointed apically and microbasic b-mastigophore with slightly bent, narrow
shaft, following the convex capsule side. (F and G) Microbasic b-mastigophores. Note shaft and tubule
pattern. (H–J, inset) Discharged microbasic euryteles. Notebroad shaft with spined distal swelling, rounded
lid, difference in diameter of shaft and distal tubule. (J) Note spine pattern on distal tubule. (I and K)
Microbasic b-mastigophores. Narrow shaft with unclear spine-pattern. Abbreviations: marks apical
capsule opening; ap, adhesive pad;b,b-mast, microbasic b-mastigophore; dt, distal tubule; eu, eurytele;
l, lid; nb, nematocyst battery; sh, shaft; sp, spines; tu, tubule. Photo credits: Carina Östman.
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 8/18
are scattered between the nematocyst rings, most clearly visible on the black pigmented
mid-streak of a tentacle (Figs. 3A and 3B).Towardthetentaclebasesthenematocystbatteries
are less dense, sometimes spiral-formed or missing (Figs. S1B and S2D). A yellow pigmented
streak is prominent at each tentacle base seen in dorsal view (Fig. 2E;Fig. S2A).
The yellow streak is less obvious on the tentacle bases seen in oral view (Figs. S2D and S2E).
Two nematocyst types, microbasic euryteles, and microbasic b-mastigophores, are
present in the nematocyst batteries around the tentacles (Figs. 3D–3K). The euryteles are
larger and by far the more abundant. Some small microbasic b-mastigophores were loosely
scattered among the euryteles. Euryteles are also densely present at the tentacle bases
and close to the ring-canal (Figs. S2B and S3). At the manubrial undulating rim euryteles
were abundant but loosely scattered on the remaining manubrium (Figs. S4E and S4F).
The capsules of both euryteles and the b-mastigophores are broad, rounded basally
and slightly narrower apically (Fig. 3E). The inverted eurytele shaft is broad, rod-shaped
with pointed apical tip. The pattern of the shaft is caused by its long, inverted spines,
all pointing toward the apical capsule opening with its lid. The inverted tubule makes
slightly oblique coils to the long capsule axis and almost ﬁlls the whole capsule, except for
Figure 4 Size distribution of Gonionemus sp. on August 2 and August 18. Size increase by 1.2 mm in
the 16 days between sampling, corresponding to a growth rate of 0.08 mm d
(p< 0.05). Each histogram
contains the bell diameters of 120 individuals. Full-size
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 9/18
Figure 5 Temperature data from Åstol, adjacent to the locations where Gonionemus sp. was found in
2018. The black line shows the monthly mean temperature ± standard deviations (shaded area) from
2000 to 2018. The red line with open circles shows the monthly mean temperature during 2018.
Figure 6 Gonionemus sp. Neighbor-joining tree of COI haplotypes based on Kimura two-parameter
distances. Haplotype numbering for haplotypes 1–7 corresponds to those in Govindarajan et al. (2017).
Haplotypes 8–16 are newly presented here based on Swedish specimens and Genbank (Table 1).
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 10/18
its basal end. The narrow shaft of the small microbasic b-mastigophore is slightly bent,
following the convex capsule side (Figs. 3E–3G). Discharged eurytele shaft is broad,
rod-shaped with distal swelling armed with long spines (Figs. 3H and 3I, inset). The
prominent rounded lid at apical capsule, and the difference of the diameter of shaft and
distal tubule are obvious (Figs. 3I and 3J). On discharged microbasic b-mastigophores
no clear spine-pattern on the narrow shaft and no obvious difference between the diameter
of distal tubule and shaft tubules are visible (Fig. 3I and 3K).
Additional morphological details are presented in Figs. S1–S6.
The 2018 spring and summer temperatures in Åstol were anomalous relative to the
previous 28 years (Fig. 5). The spring temperatures were approximately 2 Ccoolerthan
during 1986–2018; while the summer temperatures were approximately 2 Cwarmer
DNA Sequences were obtained for 16 Swedish Gonionemus sp. medusae and submitted to
GenBank (accession numbers MK158929–MK158944). These 16 sequences comprised
three haplotypes. Nine medusae possessed one haplotype, six medusae possessed a second
haplotype, and a single medusa possessed a third haplotype. The Swedish sequences were
aligned with representatives of each of the Gonionemus sp. haplotypes described in
Govindarajan et al. (2017) and additional haplotypes found in subsequently available
GenBank sequences. These newer GenBank sequences included one representative from
New Jersey on the USA mid-Atlantic coast (accession number KY451454;Gaynor et al.,
2016) and 104 sequences from three Chinese locations (accession numbers MH020640–
MH020743; Liu & Dong, unpublished GenBank entry).
An initial alignment and neighbor-joining tree of the new Chinese sequences from
GenBank showed that they comprised nine haplotypes (Fig. 6). Haplotypes were
labeled by number following Govindarajan et al. (2017) and new haplotypes were
given new numbers. Of the nine haplotypes, one matched Haplotype 9, one matched
Haplotype4,andsevenwereuniqueforSweden. One sequence representing each of the
sequences. The single New Jersey sequence matched one of the Swedish haplotypes,
as described below.
A neighbor-joining tree of the Swedish sequences and the unique COI haplotypes was
generated (Fig. 6). We found that the most abundant Swedish haplotype (found in nine out
of 16 specimens) exactly matched Haplotype 4 from Govindarajan et al. (2017) that
was possessed by medusae from the Northwest Atlantic (from the states of Connecticut,
Rhode Island, Massachusetts, and New Hampshire along the northeastern USA coast) and
the Northwest Paciﬁc (including the highly toxic Vladivostok-area populations from
the Sea of Japan). The second Swedish haplotype, termed “Haplotype 9”here and found in
six out of 16 specimens, matched the haplotype from New Jersey.
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 11/18
We documented a bloom of the highly toxic clinging jellyﬁsh Gonionemus sp. associated
with severe stings to humans on the Swedish west coast. To our knowledge, this is the
ﬁrst record of clinging jellyﬁsh envenomations to humans from this region. The symptoms
reported by one of the authors (BK) are consistent with those described from the
Northwest Atlantic and Sea of Japan (Mikulich & Naumov, 1974;Michaleff, 1974;
Yatskov, 1974;Govindarajan & Carman, 2016).
Clinging jellyﬁsh have been previously reported from European Atlantic, North Sea,
and Mediterranean coasts, as well as the northwestern Atlantic, the northwestern Paciﬁc
and Sea of Japan (reviewed in Govindarajan & Carman, 2016;Govindarajan et al., 2017;
Marchessaux et al., 2017). The records of clinging jellyﬁsh in Europe are sporadic. In Atlantic
coastal waters, observations date back to the early 1900s (Bakker, 1980), and in the
Mediterranean possibly back to the 1870s (as Cosmotira salinarium;Duplessis, 1879).
Gonionemus sp. has also been reported from several aquaria with Atlantic and
Mediterranean source water (reviewed in Edwards (1976) and Bakker (1980)). However, in
contrast to western Paciﬁc and Sea of Japan populations, where there is a long record
of severe stings, stings to humans have not been reported to our knowledge from European
populations until 2016 (from the French Mediterranean coast; Marchessaux et al., 2017).
The history of clinging jellyﬁsh in European Atlantic waters is comparable to that along
the Northwest Atlantic US coast and may similarly indicate a new, cryptic invasion of
a more toxic form. Both regions have a history of episodic clinging jellyﬁsh sightings,
but no record of stings until recently. However, the existence of multiple species and highly
episodic life cycle make drawing conclusions difﬁcult. Our genetic analysis conﬁrmed
our morphological identiﬁcation, placing the Swedish form into the Gonionemus sp. clade
that includes the highly toxic phenotype. Our morphological observations are consistent
with historical European observations of the apparently less toxic form (G. murbachii),
but it seems likely that toxicity varies within the Gonionemus sp. clade (Govindarajan et al.,
2017) so this discrepancy does not rule out a new introduction.
Additional sampling and analysis of nuclear markers will be required to fully solve the
Gonionemus “zoogeographic puzzle.”However, our COI data provide several new insights.
One of the three Swedish haplotypes (Haplotype 4 in Fig. 6) is also found in the
northern Northwest Atlantic and the western Paciﬁc/Sea of Japan regions which contain
highly toxic individuals and may indicate a common origin. Another of our haplotypes
(Haplotype 9 in Fig. 6) has also been reported from New Jersey, USA, which is in the mid—
Northwest Atlantic region. Gonionemus sp. was ﬁrst reported in New Jersey in 2016
(Gaynor et al., 2016). Our analysis could indicate an independent origin of the New Jersey
population relative to the northern Northwest Atlantic populations. Our third haplotype
(Haplotype 8 in Fig. 6), found in only one individual, was unique.
Interestingly, our haplotype tree also shows that the Paciﬁc region contains the greatest
number of haplotypes (10) but only one of these (Haplotype 4) is found outside of the
region. This result is consistent with a scenario where a subset of the ostensibly native
Paciﬁc diversity inoculated other regions. However, the observation of several haplotypes
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 12/18
in Sweden and elsewhere that have not yet been found in the Paciﬁc, in combination with
the historical record of sightings from these same regions, suggests that we cannot rule out
that the Northwestern Atlantic and Mediterranean regions contain native diversity,
either instead of or in addition to introduced lineages.
There are ample pathways and opportunities for Gonionemus sp. to be introduced to the
Swedish coast. The life cycle of Gonionemus sp. includes minute polyp and cyst stages
(Perkins, 1903;Kakinuma, 1971;Uchida, 1976) that could have easily arrived unnoticed.
In a genetic survey of epifauna, Gonionemus sp. was recently identiﬁed from the North
American Paciﬁc coast on tsunami debris originating from Japan (Choong et al., 2018).
This suggests that polyp, frustule, and or cyst stages are capable of long-distance transport
on anthropogenic surfaces. There are two larger international harbors near our study site,
Wallhamn and Stenungsund (Fig. 1); thus, it is quite possible that a highly toxic lineage
arrived attached to ship hulls. Furthermore, there are many records of Gonionemus sp.
occurring in public aquaria, where they presumably establish from polyp stages
accompanying materials brought to the aquaria (Tambs-Lyche, 1964).
Another factor that may have played a role in the 2018 Swedish clinging jellyﬁsh
outbreak is temperature. Water temperature is a critical factor initiating seasonal
hydrozoan polyp activity (Calder, 1990). The year of the outbreak (2018) was exceptional
in that it had both an approximately two degrees colder than average spring and a
two-degrees warmer than average summer. Either or both of these anomalies could have
facilitated the Gonionemus sp. outbreak. Gonionemus sp. medusae are produced by polyps,
which may arise from frustules or cysts (Perkins, 1903;Uchida, 1976). In a detailed
study of the life cycle and development of G. vertens,Kakinuma (1971) observed that when
polyps were kept at 20 C with access to food they released medusae that developed to
10–12 mm in diameter in 5–6 weeks. Both temperature and salinity have also been
implicated in affecting Russian Sea of Japan populations (Yakovlev & Vaskovsky, 1993).
Surface water temperature data available to us (Fig. 5) originated from a temperature
monitoring station located in a less sheltered area and in deeper water than the area with
Zostera-beds where the current outbreak occurred (Fig. 1). We therefore hypothesize
that in the area of the observed outbreak the surface water temperature was above 20 C for
most of July and August, which would have allowed the release and development of
medusae from polyps present in the area.
It seems probable that, similar to the US Atlantic coast, Gonionemus sp. will spread
to new sites along the North Sea coast and potentially pose hazards to both humans and
ecosystems. Regular monitoring and surveys will be crucial for providing warnings to
protect bathers and others from potentially harmful interactions. Our two data points for
size distribution indicated a ∼12% increase in size over 16 days (Fig. 4). Temperature
and food availability are likely factors affecting growth rate and if comparable with
Kakinuma (1971), the size distribution in the studied population would imply that the
medusae release started roughly around 5 weeks earlier, or in late June.
More information is also needed to understand the impact of Gonionemus sp. in
eelgrass communities, but the morphological features we observed provide some insight
into their ecological roles. Gonionemus sp. medusae spend much of their time “clinging”to
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 13/18
eelgrass with their adhesive pads. Free (unattached) tentacles are often extended into the
ambient current. This pattern of passive drifting of tentacles is typically seen in
hydromedusae that are ambush predators (Madin, 1988;Colin, Costello & Klos, 2003).
Tethering to the seagrass will also increase encounter rate with prey if there is a current
passing the tethered medusa. The nematocyst types we observed, euryteles and microbasic
b-mastigophores, and their arrangement in raised clusters on the tentacles suggest that
Gonionemus sp. feeds on hard-body prey such as crustaceans (Purcell & Mills, 1988). This is
consistent with reports that Gonionemus sp. medusae feed on small zooplankton such as
copepods (Mills, 1983 (for G. vertens)) and observations in laboratory cultures that they feed
on copepods and Artemia nauplii (A.Govindarajan, C. Östman, 2018, personal observation).
Intriguingly, Gonionemus sp. may mediate the interactions of other species and
cause mortality in non-prey organisms. For example, along the Northwest Atlantic coast in
Massachusetts, Carman, Grunden & Govindarajan (2017) found that Gonionemus sp. was
consumed by a native spider crab but not by the invasive green crab. The authors also
found that Gonionemus ingestion resulted in crab death when large numbers of jellyﬁsh
were consumed. Thus, Gonionemus sp. may potentially impact native ecosystems via
differential predation by a native species (spider crabs) that may lead to a decline of that
species, while avoidance of Gonionemus by a destructive invasive species could potentially
facilitate its dominance.
We documented the presence of the cryptogenic limnomedusa Gonionemus sp. from an
eelgrass bed at the Swedish west coast during the summer of 2018. The presence of these
medusae were linked to several severe stings in local bathers. Using mitochondrial
COI sequences, we showed that the Swedish medusae belong to the same clade as highly
toxic populations previously found in the Sea of Japan and the northwestern Atlantic.
We also reported detailed features of the medusa morphology using light microscopy,
including details of the nematocysts. We suggested that the outbreak at the Swedish west
coast is linked to the exceptionally warm summer of 2018 following either a climate-driven
range shift or a direct introduction to the area via shipping activity. Given the harmful
stings associated with the medusae and the high risk of additional colonization along the
Swedish coast, further investigations on this species are warranted.
Hans Hällman is gratefully acknowledged for sampling assistance and Ulf Jondelius kindly
provided the photograph for Fig. 2G.
ADDITIONAL INFORMATION AND DECLARATIONS
Funding was provided by the Swedish Research Council (VR) to Erik Selander “Signals
in the Sea”and from the Faculty of Science of Uppsala University to Carina Östman.
Funding for the DNA sequencing analysis was provided by the Kathleen M. and
Govindarajan et al. (2019), PeerJ, DOI 10.7717/peerj.6883 14/18
Peter E. Naktenis Family Foundation and the Borrego Foundation. The funders had no
role in study design, data collection and analysis, decision to publish, or preparation of the
The following grant information was disclosed by the authors:
Swedish Research Council (VR) to Erik Selander “Signals in the Sea”.
Faculty of Science of Uppsala University.
Funding for the DNA sequencing analysis.
Family Foundation and the Borrego Foundation.
The authors declare that they have no competing interests.
Annette F. Govindarajan conceived and designed the experiments, performed the
experiments, analyzed the data, contributed reagents/materials/analysis tools,
prepared ﬁgures and/or tables, authored or reviewed drafts of the paper, approved
the ﬁnal draft.
Björn Källström conceived and designed the experiments, performed the experiments,
analyzed the data, contributed reagents/materials/analysis tools, prepared ﬁgures and/or
tables, authored or reviewed drafts of the paper, approved the ﬁnal draft, collected
samples in the ﬁeld.
Erik Selander conceived and designed the experiments, analyzed the data, contributed
reagents/materials/analysis tools, prepared ﬁgures and/or tables, authored or reviewed
drafts of the paper, approved the ﬁnal draft.
Carina Östman analyzed the data, contributed reagents/materials/analysis tools,
prepared ﬁgures and/or tables, authored or reviewed drafts of the paper, approved the
ﬁnal draft, conducted detailed ultrastructure work.
Thomas G. Dahlgren conceived and designed the experiments, analyzed the data,
contributed reagents/materials/analysis tools, prepared ﬁgures and/or tables, authored
or reviewed drafts of the paper, approved the ﬁnal draft.
The following information was supplied regarding data availability:
Data is available at Genbank (accession numbers MK158929–MK158944).
Supplemental information for this article can be found online at http://dx.doi.org/10.7717/
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