Report on anisakid nematodes in polar regions e Preliminary results
Joanna Dzidoa, Agnieszka Kijewskab, Magdalena Rokickac,
Agnieszka S´wia ˛talska-Kosedad, Jerzy Rokickia,*
aUniversity of Gdan ´sk, Department of Invertebrate Zoology, Gdynia, Poland
bInstitute of Oceanology PAS, Department of Genetics and Marine Biotechnology, Sopot, Poland
cUniversity of Gdan ´sk, Biological Station, Gdan ´sk, Poland
dVeterinary Hygiene Station, Gdan ´sk-Oliwa, Poland
Received 3 December 2008; revised 27 July 2009; accepted 25 August 2009
Available online 7 October 2009
The aim of this study is to extend our knowledge of the distribution of anisakid nematode parasites in Arctic and Antarctic polar
regions. We examined vertebrate (fish) taxa characteristic of the faunas in both polar regions for the presence of parasitic nema-
todes. The material was collected from Svalbard (Arctic) between July and August 2008 and from King George Island (South
Shetland Islands, Antarctic Peninsula) between November 2007 and January 2008. In addition, faecal, bird, and invertebrate
samples were collected and examined for the presence of anisakid nematodes or eggs. Anisakis simplex s.s. was found in the body
cavity of Arctic cod, and Contracaecum sp. and Pseudoterranova sp. were found in Antarctic notothenioids. Eggs of Anisakis
sp. and Contracaecum sp. were recovered from the faeces of Mirounga leonina. We present the first record of the occurrence of
A. simplex C in the Antarctic fishes Notothenia coriiceps and Notothenia rossii.
? 2009 Elsevier B.V. and NIPR.
Keywords: Anisakid nematodes; Polar regions; Arctic; Antarctic
The polar regions include the land and water
located north of 60?N (Arctic) and south of 60?S
(Antarctic). There are no land mammals in the
Antarctic, where the main inhabitants are marine
mammals (whales, porpoises, seals) and birds. In
contrast, the Arctic is home to terrestrial mammals
such as reindeer, fox, wolf, lemming, caribou, musk
ox, hare, and polar bear.
Members of the family Anisakidae (Nematoda:
Secernentea) include parasitic species that occur in
both the Northern and Southern Hemispheres, and that
are of veterinary, medical, and economic importance.
Some species are also known to be dangerous to
humans (van Thiel, 1962). Adults of most of these
parasites live in the alimentary tract of the vertebrate
host (mammals, birds, fish), and are present in both
marine and freshwater environments. The life cycles of
numerous taxa involve the development of larval stages
in one or more intermediate hosts (fish, invertebrates).
The differences between southern and northern trophic
webs may affect the distribution of parasites in these
* Corresponding author.
E-mail address: firstname.lastname@example.org (J. Rokicki).
1873-9652/$ - see front matter ? 2009 Elsevier B.V. and NIPR.
Available online at www.sciencedirect.com
Polar Science 3 (2009) 207e211
The aim of this study and short report is to extend
knowledge of the distribution of anisakid parasites in
both polar regions.
2. Materials and methods
The study material was collected on King George
Island (South Shetland Islands, Antarctic Peninsula)
and on Svalbard (Table 1).
2.1. Arctic material
The Arctic study material was collected close to the
Polish Polar Station at Hornsund on Svalbard during
the summer of 2008 (13 July to 20 August).
Fish samples, including Liparis liparis (Montagu’s
sea snail), Salvelinus alpinus (Arctic char), Myox-
ocephalus scorpius (short-spined sea scorpion), and
Boreogadus saida (polar cod, Arctic cod), were
collected in the Hornsund Fjord area, mainly from
Isbjornhamna and Ariebukta. Further samples of Arctic
char were collected from two freshwater lakes,
Revvatnet and Sartvatnet (Sorkapp Land), and from the
Revelva River. All the fish were examined for the
presence of anisakid nematodes. Nematodes were fixed
in either 70% ethanol or 70% ethanol with 5%
We alsocollected vertebrate
including that of Ursus maritimus (polar bear), Rissa
tridactyla (black-legged kittiwake), Sterna paradisaea
(Arctic tern), Uria lomvia (Bru ¨nnich’s guillemot), and
Branta leucopsis (barnacle goose). All samples were
obtained from the Ariedalen Valley and Fugle-
bergsletta, except for those of polar bear, which were
collected near Gnalberget. Two methods were used for
parasite egg recovery: flotation and decanting. In the
flotation method, the faecal material was strained
through a sieve (1 mm mesh) into a Petri dish con-
taining a salt solution. After 15e20 min, the liquid was
transferred to centrifuge tubes and a coverslip was
placed in contact with the meniscus. The coverslip was
then placed on a slide, and examined for parasite eggs
under the microscope (5e10? magnification). For
decanting, the collected material was placed in water,
Anisakid nematode eggs/nematodes found in samples investigated in the present study.
Region Sample type Host species Anisakids found/no.
of samples examined
(location within host bodya)
Rangifer tarandus playrhynchus
Sterna paradisaea, Uria lomvia
A. sim. (bc)
A. sp. (f); C. sp. (f)
P. sp. (bc, l, s)
A. sim. C (bc); P. sp. (bc, l)
A. sim. C (bc); P. sp. (bc, l); C. sp. (bc)
abc: body cavity; l: liver; s: stomach; f: faeces.
bA. sim.: Anisakis simplex s.s.; A. sp.: Anisakis species; A. sim. C: Anisakis simplex C; C. sp.: Contracaecum species; P. sp.: Pseudoterranova
J. Dzido et al. / Polar Science 3 (2009) 207e211
and the supernatant was poured off after 30, 50, and
70 min; the sediments were then examined under
Fifty-nine individuals of the crustacean Gammarus
oceanicus were examined for the presence of parasitic
nematodes; we also examined dead specimens of two
bird species: Larus hyperboreus (glaucous gull) and
Alle alle (little auk).
2.2. Antarctic material
The Antarctic material was collected between
November 2007 and January 2008 near Arctowski
Station on King George Island, where fish were caught
in Admiralty Bay.
Seven fish species were examined: Chaenocephalus
aceratus (blackfin icefish), Notothenia rossii (marbled
rockcod), Notothenia coriiceps (black rockcod), Har-
pagifer antarcticus (Antarctic spiny plunderfish), Lep-
idonotothen nudifrons (gaudy notothen), Trematomus
newnesi (dusky notothen), and Trematomus bernacchii
(emerald rockcod). Vertebrate faecal samples were
obtained from Mirounga leonina (southern elephant
seal), Pygoscelis adeliae (Ade ´lie penguin), Pygoscelis
papua (gentoo penguin), Pygoscelis antarcticus (chin-
strap penguin), Stercorarius antarctica (brown skua),
and Macronectes giganteus (southern giant petrel).
Each faecal sample contained between 10 and 15
stools, and was examined as described above.
2.3. Nematode identification
Parasitic nematodes and their eggs were identified
based on morphological characteristics (Hartwich,
1974; Stefan ´ski et al., 1952). In addition, PCR-RFLP
(Restriction Fragment Length Polymorphism) analysis
of the nuclear rDNA region containing Internal Tran-
scribed Spacers and the 5.8S rDNA gene were used to
aid species identification of Anisakis spp. larvae from
fish (D’Amelio et al., 2000; Pontes et al., 2005),
following the method of Kijewska et al. (2009). PCR
products were digested with three restriction endonu-
cleases (TaqI, HinfI, HhaI; Fermentas, Lithuania).
Restriction with TaqI and HinfI produced characteristic
bands representing three fragments (430, 400, and
100 bp) and two fragments (620 and 250 bp), respec-
tively, for both Anisakis simplex s.s. and A. simplex
C. Restriction with HhaI produced two fragments for
A. simplex s.s. (550 and 430 bp) and three fragments
for A. simplex C (550, 430, and 130 bp). Previous
studies have shown that the use of these three enzymes
enables the differentiation of all Anisakis species that
cannot be discriminated based on morphological
characteristics alone (D’Amelio et al., 2000; Pontes
et al., 2005).
Parasitic nematodes were recovered from N. cor-
iiceps, N. rossii, C. aceratus, and B. saida. Preliminary
morphological analyses revealed the presence of Ani-
sakis sp., Contracaecum sp., and Pseudoterranova
sp. Contracaecum sp. was found in the body cavity of
N. coriiceps. Pseudoterranova sp. was found in the
body cavity and liver of N. coriiceps, N. rossii, and
C. aceratus. A single anisakid nematode (A. simplex
s.s.) was found in the body cavity of B. saida. Indi-
viduals of A. simplex C were found in the body cavity
of N. coriiceps and N. rossii.
Parasite eggs were found only in faecal samples of
M. leonina. A total of 70 eggs were found, and
morphological examination confirmed the presence of
Anisakis sp. (95% of eggs) and Contracaecum sp. (5%
of eggs). Future work to confirm species identities will
be based on the application of molecular techniques.
In the present study, A. simplex C was obtained for
the first time from N. coriiceps and N. rossii. Previ-
ously, it has been reported from Delphinidae, Gem-
pylidae, Moridae, and Pinguipedidae (from the South
African coast, North-East Pacific, New Zealand, and
Tasman Sea), and occasionally from M. leonina (sub-
Antarctic area) and Mirounga angustirostris (North-
East Pacific) (Mattiucci et al., 1997; Mattiucci and
Nascetti, 2006, 2008; Nadler et al., 2000). The present
study extends the range of occurrence of this species to
include Admiralty Bay, South Shetland Islands (mari-
The marine fauna of the Antarctic is highly endemic
(Rogers, 2007), comprising many species that do not
occur elsewhere, and excluding many familiar species
from lower-latitude faunas. This generalization applies
to both host and parasite species. In the Antarctic, six
species of anisakid nematodes have been reported to
date, of which five are currently thought to be endemic:
Contracaecum radiatum, Contracaecum osculatum D
and E, Pseudoterranova decipiens E, and Contra-
caecum. miroungae (Bullini et al., 1997; Kloser et al.,
1992; Nadler et al., 2000; Orecchia et al., 1994; Palm,
1999). In the Arctic, C. osculatum A (Nascetti et al.,
1993) and Pseudoterranova bulbosa (Paggi et al.,
1991) have been reported, and several other species
J. Dzido et al. / Polar Science 3 (2009) 207e211
occur in sub-Arctic areas (Mattiucci and Nascetti,
2008). These parasites are characterized by their
specificity, being limited to a small number of final
hosts, and, indirectly, a life cycle with specific
Antarctic or Arctic intermediate hosts. Anisakid
nematodes have a complex life cycle involving several
host species. Depending on the species, the definitive
hosts of these nematodes include marine mammals,
birds, and fish. The life cycle also involves one or more
intermediate or paratenic hosts such as invertebrates
(euphausiids, squid) and fish. Other species, such as the
polar bear, can potentially become infected by anisakid
nematodes by eating infected seal or fish. Crustaceans
form part of the diets of the fish and seal species
identified in this study to be infected with anisakids
(Iken et al., 1997; McKenna, 1991). Euphausiids (krill)
and squid are known to be intermediate hosts of marine
nematode parasites worldwide. Little is known of the
infection of invertebrates by anisakid nematodes in the
Antarctic; consequently, our knowledge of trans-
mission mechanisms remains limited.
The Antarctic fish examined in this study belong to
three families: Harpagiferidae (H. antarcticus), Chan-
nichthyidae (C. aceratus), and Nototheniidae (all other
species). All belong to the suborder Notothenioidei,
of this region (Eastman, 2005). Due to their dominance,
these species are considered as the most likely inter-
mediate hosts for anisakids. This hypothesis was sup-
ported by the data obtained in the current study, and
turn, the Arctic fishes (Gadidae (B. saida), Cottidae
(M. scorpius), Liparidae (L. liparis), and Salmonidae
(S. alpinus)) were classified as typical intermediate
hosts for Anisakidae species. These species are also
commonly found in temperate waters of the Northern
Hemisphere; however, in this study we found only
a single specimen of A. simplex s.s. in the body cavity of
a B. saida from Hornsund Fjord. This specimen was
a juvenile and its size suggested that this fish originated
from shoal feeding on offshore grounds inside the fjord,
possibly explaining the poor parasitic fauna found
during the examination. The distribution of eggs and
larvae in animals other than fishes revealed the presence
of Anisakidae in the faecal matter of M. leonina,
whereas birds and terrestrial mammals, including polar
bears, appeared to be free from anisakids.
The lack of seals and whales or dolphins in the
northern sample introduces some uncertainty into our
conclusions. However, available data indicate a high
probability that the most important group in terms of
anisakid distribution in polar regions is fish-eating
mammals, as also concluded by Mattiucci and Nascetti
(2008), although the presence of fish within the diet of
potential final hosts does not necessarily mean that
these species are able to serve as final hosts. Exami-
nation of the faeces of various fish-eating birds and
mammals (polar bear), and examinations of the bodies
of some birds (Table 1), revealed that these species are
not anisakid hosts.
Anisakid nematodes occur worldwide, including the
Arctic and Antarctic regions; however, while these two
regions appear to be similar in terms of environmental
and parasite taxa. This discrepancy possibly reflects
species divergence and the narrow specificity of para-
sites living in only one or several hosts, as with
C. radiatum and Anisakis physeteris (Mattiucci and
of wide-specificity parasites such as A. simplex s.s. and
Anisakis pegreffii. The known phylogenies of Anisaki-
dae, constructed based on various molecular genetic
datasets (Kijewska et al., 2009; Nadler et al., 2000; Zhu
may be strongly related to the geographical distribution
of the host. This factor determines the distribution of
parasites and affects the number and choice of inter-
mediate hostspecies,although there existsalackofdata
regarding the distribution of some species (for example
A. simplex C, reported here for the first time in N. cor-
iiceps and N. rossii).
Theresearch was supportedbythePolishMinistryof
Education and Science (grant no. 1182/IPY/2007/01).
Bullini, L., Arduino, P., Cianchi, R., Nnascetti, G., D’amelio, S.,
Mattiuchi, S., Paggi, L., Orecchia, P., 1997. Genetic and
ecological research on anisakid endoparasites of fish and marine
mammals in the Antarctic and ArticeBoreal regions. In:
Battaglia, B., Valencia, J., Walton, D.W.H. (Eds.), Antarctic
Communities: Species, Structure and Survival. Cambridge
University Press, Cambridge, pp. 362e383.
D’Amelio, S., Mathiopoulos, K.D., Santos, C.P., Pugachev, O.N.,
Webb, S.C., Picanc ¸o, M., Paggi, L., 2000. Genetic markers in
ribosomal DNA for the identification of members of the genus
Anisakis (Nematoda: Ascaridoidea) defined by polymerase chain
reaction-based restriction fragment length polymorphism. Int.
J. Parasitol. 30, 223e226.
Eastman, J.T., 2005. The nature of diversity of Antarctic fishes. Polar
Biol. 28, 93e107.
Hartwich, G., 1974. Keys to genera of the Ascaridoidea. In:
Anderson, R.C., Chabaud, A.G., Wilmott, S. (Eds.), CIH Keys to
J. Dzido et al. / Polar Science 3 (2009) 207e211
the Nematode Parasites of Vertebrates. Commonwealth Agricul- Download full-text
tural Bureau, Farnham Royal, p. 153. Richmond.
Grazing by the Antarctic fish Notothenia coriiceps: evidence for
selective feeding on macroalgae. Antarct. Sci. 9, 386e491.
Kijewska, A., Dzido, J., Shukhgalter, O., Rokicki, J., 2009. Anisakid
parasites of fishes caught on the African shelf. J. Parasitol. 95,
Kloser, H., Plotz, J., Palm, H., Bartsch, A., Hubolcf, G., 1992.
Adjustment of anisakid nematode life cycles to the high Antarctic
food web as shown by Contracaecum radiatum and C. osculatum
in the Weddell Sea. Antarct. Sci. 4, 171e178.
Mattiucci, S., Nascetti, G., 2006. Molecular systematics, phylogeny
and ecology of anisakid nematodes of the genus Anisakis
Dujardin, 1845: an update. Parasite 13, 99e113.
Mattiucci, S., Nascetti, G., 2008. Advances and trends in the
molecular systematics of anisakid nematodes, with implications
for their evolutionary ecology and hosteparasite co-evolutionary
processes. Adv. Parasitol. 66, 47e148.
Mattiucci, S., Nascetti, G., Clanchi, R., Paggi, L., Arduino, P.,
Margolis, L., Brattey, J., Webb, S., D’Amelio, S., Orecchia, P.,
Bullini, L., 1997. Genetic and ecological data on the Anisakis
simplex complex, with evidence for a new species (Nematoda,
Ascaridoidea, Anisakidae). J. Parasitol. 83, 401e416.
McKenna Jr., J.E., 1991. Trophic relationships within the Antarctic
demersal fish community of South Georgia Island. Fish. Bull. 89,
Nadler, S.A., D’Amelio, S., Fagerholm, H.P., Berland, B., Paggi, L.,
2000. Phylogenetic relationships among species of Contracaecum
Railliet & Henry, 1912 and Phocascaris Host, 1932 (Nematoda:
Ascaridoidea) based on nuclear rDNA sequence data. Parasi-
tology 121, 455e463.
Nascetti, G., Cianchi, R., Mattiucci, S., D’Amelio, S., Orecchia, P.,
Paggi, L., Brattey, J., Berland, B., Smith, J.W., Bullini, L., 1993.
Three sibling species within Contracaecum osculatum (Nem-
atoda, Ascaridida, Ascaridoidea) from the Atlantic Arctice
Boreal region: reproductive isolation and host preferences. Int.
J. Parasitol. 23, 105e120.
Orecchia, P., Mattiucci, S., D’Amelio, S., Paggi, L., Plo ¨tz, J.,
Cianchi, R., Nascetti, G., Arduino, P., Bullini, L., 1994. Two new
members in the Contracaecum osculatum complex (Nematoda,
Ascaridoidea) from the Antarctic. Int. J. Parasitol. 24, 367e377.
Palm, H.W., 1999. Ecology of Pseudoterranova decipiens (Krabbe,
1878) (Nematoda: Anisakidae) from Antarctic waters. Parasitol.
Res. 85, 638e646.
Paggi, L., Nascetti, G., Cianchi, R., Orecchia, P., Mattiucci, S.,
D’Amelio, S., Berland, B., Brattey, J., Smith, J.W., Bullini, L.,
1991. Genetic evidence for three species within Pseudoterranova
decipiens (Nematoda, Ascaridida, Ascaridoidea) in the North
Atlantic and Norwegian and Barents Seas. Int. J. Parasitol. 21,
Pontes, T., D’Amelio, S., Costa, G., Paggi, L., 2005. Molecular
characterization of larval anisakid nematodes from marine fishes
of Madeira by a PCR-based approach, with evidence for a new
species. J. Parasitol. 91, 1430e1434.
Rogers, A.D., 2007. Evolution and biodiversity of Antarctic organ-
isms: a molecular perspective. Philos. Trans. R. Soc. Lond.
B: Biol. Sci. 362, 2191e2214.
Stefan ´ski, W.,
_Zarnowski, E., So1tys, A., 1952. Zarys para-
zytologicznych metod rozpoznawczych. Pan ´stwowe Wydaw-
nictwo Rolnicze i Le? sne, Warszawa (in Polish).
van Thiel, P.H., 1962. Anisakiasis. Parasitology 52, 16e17.
Zhu, X.Q., D’Amelio, S., Palm, H.W., Paggi, L., George-
Nascimento, M., Gasser, R.B., 2002. SSCP-based identification
of members within the Pseudoterranova decipiens complex
(Nematoda: Ascaridoidea: Anisakidae) using genetic markers in
the internal transcribed spacers of ribosomal DNA. Parasitology
J. Dzido et al. / Polar Science 3 (2009) 207e211