Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik Vernadsky”, Argentine Islands, West Antarctica
Monitoring studies of the species diversity in marine ecosystems provide important data on ecological changes caused by global warming and anthropogenic influence. The present work was aimed to analyze the species diversity of the helminths parasitic in teleost fishes inhabiting the area near the Uk...
Saved in:
| Published in: | Zoodiversity (Vestnik Zoologii) |
|---|---|
| Date: | 2021 |
| Volume: | 55 |
| Issue: | 3 |
| Pages: | 251–264 |
| ISSN: | 2707-7268 |
| Author Affiliations: |
|
| Main Authors: | , , , , , |
| Format: | Article |
| Language: | English |
| Published: |
Publishing House "Akademperiodyka" of the National Academy of Sciences of Ukraine
2021
|
| Online Access: | https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/181 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Journal Title: | Zoodiversity |
| Download file: |
|
Institution
Zoodiversity| _version_ | 1874092693423915008 |
|---|---|
| author | Kuzmina, T. Dykyy, I. V. Salganskij, O. O. Lisitsyna, O. I. Korol, E. M. Kuzmin, Yu. I. |
| author_facet | Kuzmina, T. Dykyy, I. V. Salganskij, O. O. Lisitsyna, O. I. Korol, E. M. Kuzmin, Yu. I. |
| author_institution_txt_mv | [
{
"author": "T. Kuzmina",
"institution": "I. I. Schmalhausen Institute of Zoology NAS of Ukraine",
"orcid": "0000-0002-5054-4757"
},
{
"author": "I. V. Dykyy",
"institution": "Zoological Museum of Lviv National University, 4, Grushevsky Street, Lviv, 79005, Ukraine",
"orcid": ""
},
{
"author": "O. O. Salganskij",
"institution": null,
"orcid": ""
},
{
"author": "O. I. Lisitsyna",
"institution": "I. I. Schmalhausen Institute of Zoology NAS of Ukraine; 15, Bogdan Khmelnytskyi Street, Kyiv, 01030, Ukraine",
"orcid": ""
},
{
"author": "E. M. Korol",
"institution": "National Museum of Natural History NAS of Ukraine; 15, Bogdan Khmelnytskyi Street, Kyiv, 01030, Ukra",
"orcid": ""
},
{
"author": "Yu. I. Kuzmin",
"institution": "I. I. Schmalhausen Institute of Zoology NAS of Ukraine; 15, Bogdan Khmelnytskyi Street, Kyiv, 01030, Ukraine",
"orcid": ""
}
] |
| author_orcid_str_mv | 0000-0002-5054-4757 |
| author_sort | Kuzmina, T. |
| baseUrl_str | https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/oai |
| collection | OJS |
| container_end_page | 251–264 |
| container_issue | 3 |
| container_start_page | 251–264 |
| container_title | Zoodiversity (Vestnik Zoologii) |
| container_volume | 55 |
| datestamp_date | 2026-08-20T12:37:23Z |
| description | Monitoring studies of the species diversity in marine ecosystems provide important data on ecological changes caused by global warming and anthropogenic influence. The present work was aimed to analyze the species diversity of the helminths parasitic in teleost fishes inhabiting the area near the Ukrainian Antarctic Station "Akademik Vernadsky" (Galindez Island, Argentine Islands, West Antarctica). During April – January of 2014–2015 and 2019–2020, 156 specimens of six fish species (Notothenia coriiceps, N. rossii, Chaenocephalus aceratus, Parachaenichthys charcoti, Trematomus bernacchii, and Harpagifer antarcticus) were examined. Totally, 21,166 specimens of 31 helminth species were collected and assigned to five taxonomic groups: Monogenea (1 species), Digenea (10), Nematoda (5), Cestoda (4), and Acanthocephala (11). Twenty-six helminth species were found in N. coriiceps,14 in N. rossii, 27 in P. charcoti, 23 in Ch. aceratus, 16 in T. bernacchii, and six in H. antarcticus. Larval stages of anisakid nematodes prevailed in helminth community of Ch. aceratus (66%) and P. charcoti (40%), while other fish species were mostly infected with acanthocephalans, trematodes and cestodes. The present data on the species diversity of helminth communities can be used as a baseline for long-term monitoring studies of fish parasites in the region of Argentine Islands. |
| doi_str_mv | 10.15407/zoo2021.03.251 |
| first_indexed | 2025-07-17T12:35:19Z |
| format | Article |
| fulltext |
UDC UDC 595.1:597.5(1-15:9)
HELMINTH DIVERSITY IN TELEOST FISHES
FROM THE AREA OF THE UKRAINIAN ANTARCTIC STATION
“AKADEMIK VERNADSKY”, ARGENTINE ISLANDS,
WEST ANTARCTICA
T. A. Kuzmina1,2, I. V. Dykyy2,3, O. O. Salganskij2, O. I. Lisitsyna1, E. M. Korol4,
Yu. I. Kuzmin1,5
1Schmalhausen Institute of Zoology NAS of Ukraine,
vul. B. Khmelnytskogo, 15, Kyiv, 01030 Ukraine
E-mail: taniak@izan.kiev.ua
2State Institution National Antarctic Scientifi c Center,
Taras Shevchenko Blvd, 16, Kyiv, 01601 Ukraine
3Zoology Department of Lviv National University,
4 Grushevsky St., Lviv, 79005 Ukraine
4National Museum of Natural History NAS of Ukraine,
15 Bogdan Khmelnytskyi St., Kyiv, 01030 Ukraine
5African Amphibian Conservation Research Group, Unit for Environmental
Sciences and Management, North-West University, Potchefstroom, South Africa
T. A. Kuzmina (https://orcid.org/0000-0002-5054-4757)
I. V. Dykyy (https://orcid.org/0000-0003-3625-8567)
O. I. Lisitsyna (https://orcid.org/0000-0002-2975-3300)
E. M. Korol (https://orcid.org/0000-0002-4061-5179)
Yu. I. Kuzmin (https://orcid.org/0000-0002-1723-1265)
Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik
Vernadsky”, Argentine Islands, West Antarctica. Kuzmina, T. A., Dykyy, I. V., Salganskij, O. O.,
Lisitsyna, O. I., Korol, E. M., Kuzmin, Yu. I. — Monitoring studies of the species diversity in marine
ecosystems provide important data on ecological changes caused by global warming and anthropogenic
infl uence. Th e present work was aimed to analyze the species diversity of the helminths parasitic in teleost
fi shes inhabiting the area near the Ukrainian Antarctic Station “Akademik Vernadsky” (Galindez Island,
Argentine Islands, West Antarctica). During April–January of 2014–2015 and 2019–2020, 156 specimens
of six fi sh species (Notothenia coriiceps, N. rossii, Chaenocephalus aceratus, Parachaenichthys charcoti,
Trematomus bernacchii, and Harpagifer antarcticus) were examined. Totally, 21,166 specimens of
31 helminth species were collected and assigned to fi ve taxonomic groups: Monogenea (1 species),
Digenea (10), Nematoda (5), Cestoda (4), and Acanthocephala (11). Twenty-six helminth species were
found in N. coriiceps, 14 in N. rossii, 27 in P. charcoti, 23 in Ch. aceratus, 16 in T. bernacchii, and six in
H. antarcticus. Larval stages of anisakid nematodes prevailed in the helminth community of Ch. aceratus
(66 %) and P. charcoti (40 %), while other fi sh species were mostly infected with acanthocephalans,
trematodes and cestodes. Th e present data on the species diversity of helminth communities can be used
as a baseline for long-term monitoring studies of fi sh parasites in the region of the Argentine Islands.
Key words : Helminths, Acanthocephala, Nematoda, Cestoda, Trematoda, teleost fi shes, Antarctica.
Zoodiversity, 55(3): 251–264, 2021
DOI 10.15407/zoo2021.03.251
Parasitogy
252 T. A. Kuzmina, I. V. Dykyy, O. O. Salganskij, O. I. Lisitsyna, E. M. Korol, Yu. I. Kuzmin
Introduction
Biodiversity in Antarctica and the Southern Ocean is much more extensive, ecologically diverse and
biogeographically structured than it was previously thought (Chown et al., 2015). Moreover, the fauna of
this region is highly endemic; recent estimates suggest that 50 to 97 % of Southern Ocean species in various
taxonomic groups such as sponges, polychaetes, amphipods, molluscs, isopods, pantopods, and notothenioid
fi sh are endemic (De Broyer et al., 2014). Th e fi sh fauna in the Southern Ocean around Antarctica is dominated
by the perciform suborder Notothenioidei, which comprise up to 90 % of the fi sh biomass and about 77 % of
fi sh species diversity (Near, 2009; Near et al., 2012). Notothenioidei is a group uniquely adapted to the cold
environment being endemic for the Antarctic and sub-Antarctic regions (Eastman, 1991; Near, 2009).
Parasite fauna of Antarctic fi shes presently includes about 250 species found in more than 142 species of
hosts (Oğuz et al., 2015). Several economically valuable members of the family Notothenioidae — the Antarctic
toothfi sh Dissostichus mawsoni Norman, 1937, the Patagonian toothfi sh Dissostichus eleginoides Smitt, 1898,
the humped rockcod Gobionotothen gibberifrons Lönnberg, 1905, etc., were the subjects of a variety of parasi-
tological studies (Parukhin & Lyadov, 1982; Brickle et al., 2005; Gordeev & Sokolov, 2016); while unexploited
families have so far been rarely a focus of the research (Münster et al., 2017; Kvach & Kuzmina, 2020). Likewise,
parasites of main benthic and demersal fi shes: Notothenia coriiceps Richardson, 1844, Trematomus newnesi
Boulenger, 1902, T. bernacchii Boulenger, 1902, Parachaenichthys charcoti (Vaillant, 1906), Lindbergichthys
nudifrons (Lönnberg, 1905), etc. which could be easily caught using simple fi shing gear — rods and nets, were
also investigated in several regions of Antarctica (Wojciechowska, 1993; Zdzitowiecki, 1979, 1987, 2001; Zdzi-
towiecki & White, 1996; Zdzitowiecki & Laskowski, 2004; Laskowski & Zdzitowiecki, 2005; Laskowski et al.,
2007; 2012; Palm et al., 2007; Kuzmina et al., 2020). Most of the parasitological studies were focused on the de-
scription of new helminth species from Antarctic fi sh or single parasite taxa e.g. Digenea, Cestoda, Nematoda,
or Acanthocephala (Zdzitowiecki, 1983, 1986, 1987, 1991, 1997 a, b, 1998, 2002, 2003; Zdzitowiecki & White,
1992; Rocka & Zdzitowiecki, 1998; Rocka, 2003, 2004, 2006, 2017; Sokolov & Gordeev, 2016; Sokolov et al.,
2016, 2019; Laskowski & Zdzitowiecki, 2017). Nowadays, populational and ecological studies of parasites of
various Antarctic vertebrates and marine fi shes, in particular, are the most promising direction of parasitologi-
cal studies in Antarctica (MacKenzi, 2017; Kvach & Kuzmina, 2020). Complex studies of changes in species
diversity and the structure of parasite communities provide the monitoring of global ecological and anthro-
pogenic changes in marine ecosystems that are pronounced in the polar regions of the Arctic and Antarctic
(Clarke et al., 2007; Chown et al., 2015; Klimpel et al., 2017).
Metazoan parasites of various taxonomic groups are known as one of the most sensitive indicators of
the state of ecosystems, especially in the marine environment (Mouritsen & Poulin, 2002; Hudson et al., 2006;
Poulin & Mouritsen, 2006; Poulin, 2006). Th is is primarily associated with their complex life cycles, which
involve various species of invertebrates and vertebrates as intermediate, paratenic and defi nitive hosts. Th e
decrease in the species diversity of parasite communities has been noted as an important indicator of ecological
changes in marine ecosystems (Khan & Th ulin, 1991; Daszak et al., 2001; Barnes & Peck, 2008). Th erefore, the
acquisition of new data on the species diversity of the parasite fauna in Antarctic teleost fi sh species is important
for monitoring the marine ecosystems in this region. Comparative analysis of modern data on fi sh parasite
communities with data collected in previous decades allows revealing the main trends in the marine ecosystems
changes.
For more than 100 years of parasitological studies of Antarctica, the main part of researches on the
parasites of Antarctic fi sh has been carried out in West Antarctica (MacKenzie, 2017). In the region of the
Argentine Islands near the Ukrainian Antarctic station (UAS) “Akademik Vernadsky”, parasitological studies
were performed only in 2002 (Zdzitowiecki & Laskowski, 2004; Laskowski & Zdzitowiecki, 2005). In 2004–
2005, some collections of helminths from various fi sh species were carried out; however, only fi sh leeches were
studied in details (Utevsky, 2007). Later, the parasitological studies in 2014–2015 revealed some changes in the
structure of the helminth community of the most common fi sh species, Notothenia coriiceps (Kuzmina et al.,
2020); however, the insuffi cient amount of data did not allow associating these changes with the state of the
coastal ecosystem of Galindez Island. Th erefore, parasitological studies of various teleost fi sh species in the
Argentine Islands area were continued to collect a suffi cient amount of data for a comprehensive analysis of the
impact of climatic and anthropogenic changes on the marine ecosystems of the region. Th is work was aimed to
analyze the modern data on the species diversity of helminth fauna of main species of teleost fi sh inhabiting the
region of the UAS “Akademik Vernadsky”, Argentine Islands, and West Antarctica.
Material and methods
Field studies and material collection were carried out in April 2014–January 2015 and in April 2019–
January 2020 during the 19th and 24th Ukrainian Antarctic expeditions to the UAS “Akademik Vernadsky”on
Galindez Island, Argentine Islands, West Antarctica (65˚15′ S, 64˚16′ W). Totally, 156 specimens of six fi sh
species from the Order Perciformes, namely Antarctic black rockcod Notothenia coriiceps Richardson, 1844,
marbled rockcod N. rossii Richardson, 1844, blackfi n icefi sh Chaenocephalus aceratus (Lönnberg, 1906), Ant-
arctic dragonfi sh Parachaenichthys charcoti (Vaillant, 1906), emerald rockcod Trematomus bernacchii Bou-
253Helminth diversity in teleost fi shes from the area of the Ukrainian Antarctic Station “Akademik Vernadsky”…
lenger, 1902, and Antarctic spiny plunderfi sh Harpagifer antarcticus Nybelin, 1947 were examined (table 1).
Th e fi shes were caught using a fi shing rod off the shore of Galindez Island at depths from 10 to 30 m. All fi shes
collected were immediately transported to the laboratory, measured and examined using the standard parasi-
tological techniques (see Zdzitowiecki & Laskowski, 2004; Weber & Govett, 2009). Th e fi shes were processed
on the same day they were caught; all precautions were followed to prevent confusion of the parasites between
fi sh specimens.
Parasites were collected manually from the body cavity, stomach, intestine, liver and mesentery; all ecto-
parasites were carefully collected from the fi sh body and gills. All helminths were washed in saline and fi xed in
70 % ethanol. Acanthocephalans were kept in tap water for 30 min to 3 hours for proboscis evagination prior
to their fi xation in 70 % ethanol. Helminths belonging to main taxonomic groups (monogeneans, nematodes,
cestodes, trematodes and acanthocephalans) were counted, fi xed and stored separately. Identifi cation of the
parasites was performed in the laboratory of the Department of Parasitology, I. I. Schmalhausen Institute of
Zoology in Kyiv, Ukraine, using the Zeiss Axio Imager M1 compound microscope equipped with DIC optics
and a digital imaging system. Prior to identifi cation, all nematodes, cestodes and trematodes were clarifi ed in
lactophenol (25 % lactic acid, 25 % phenol, 25 % glycerin, and 25 % distilled water); acanthocephalans were
studied on temporary total mounts in the Berlese medium (Swan, 1936; Kuzmina et al., 2020).
Identifi cation of nematodes was performed according to Mozgovoy (1951) and Rocka (1999, 2017);
cestodes were identifi ed according to Wojciechowska (1993) and Rocka (2003, 2017); trematodes were identifi ed
according to Zdzitowiecki (1996), Zdzitowiecki and Cielecka (1997 a, b), Gibson et al. (2002), and Jones et al.
(2005). Identifi cation of acanthocephalans was performed according to Zdzitowiecki (1983, 1984 a, b, 1987,
1996) and Laskowski and Zdzitowiecki (2017). Th e helminth specimens were deposited in the Parasitological
collection of the Department of Parasitology of the I. I. Schmalhausen Institute of Zoology NAS of Ukraine
(Kyiv, Ukraine) and the Helminthological Collection of the Institute of Parasitology, Czech Academy of
Sciences (České Budějovice, Czech Republic).
Data summaries and descriptive analyses were performed using Microsoft Excel and Paleontological
Statistics Soft ware (PAST v. 3.0) (Hammer et al., 2001). Th e prevalence, mean abundance, means and median
intensity were calculated for each helminth species following the defi nitions of Bush et al. (1997). Th e species
richness in the helminth community estimated using Chao1 and bootstrap methods were calculated using the
PRIMER 6 soft ware (Clarke & Gorley, 2006). Th e Sørensen similarity index was used to compare the helminth
species composition in separate fi sh hosts. Th e results were visualised by the cluster analysis in the PRIMER 6
soft ware.
Results
All fi sh specimens examined were infected with helminths; each fi sh individual
harboured from 3 to 21 helminth species and from 9 to 1418 helminth specimens. In total,
21,166 specimens of helminths were collected and assigned to 31 species belonging to
fi ve taxonomic groups: Monogenea (1 species), Digenea (10), Nematoda (5), Cestoda (4),
and Acanthocephala (11) (table 2). Host specifi city of the helminth species to their fi sh
hosts was estimated as low, for most species were found in several fi sh hosts. Five species
(nematodes Pseudoterranova sp. and Contracaecum sp., acanthocephalans Corynosoma
evae, C. pseudohamanni, and Metacanthocephalus rennicki) were registered in all six fi sh
species; three species of trematodes and two species of acanthocephalans were found in fi ve
fi sh species; four helminth species were found in four fi sh species (table 2).
T a b l e 1 . Parameters of samples and number of helminths collected from six species of teleost fi shes off
the area of the UAS “Akademik Vernadsky”, Argentine Islands, West Antarctica
Fish species Number Weight,
gram
Size of fi sh*,
cm
Number of helminths collected
No. specimens No. species
Notothenia coriiceps 125 165–1,233 21.5–44.5 11,277 28
Notothenia rossii 3 173–696 24.0–38.5 769 14
Parachaenichtys charcoti 15 490–943 42.0–52.0 4,005 26
Trematomus bernacchii 6 89–197 18.5–27.5 266 16
Chaenocephalus aceratus 6 673–1,484 47.0–60.0 4,830 23
Harpagifer antarcticus 1 21 10.8 19 6
Total: 156 21,166 30
*Size of fi sh mean the total body length.
254 T. A. Kuzmina, I. V. Dykyy, O. O. Salganskij, O. I. Lisitsyna, E. M. Korol, Yu. I. Kuzmin
T
ab
le
2
. H
el
m
in
th
sp
ec
ie
s f
ou
nd
in
si
x
te
le
os
t fi
sh
sp
ec
ie
s i
n
co
as
ta
l w
at
er
s o
f t
he
G
al
in
de
z I
sla
nd
(A
rg
en
tin
e I
sla
nd
s,
W
es
t A
nt
ar
ct
ic
a)
. P
ar
am
et
er
s o
f fi
sh
in
fe
ct
io
n:
P
—
p
re
va
le
nc
e,
I
—
m
ea
n
in
te
ns
ity
w
ith
ra
ng
e (
m
in
im
um
–m
ax
im
um
)
N
H
el
m
in
th
sp
ec
ie
s
P,
%
N
. c
or
iic
ep
s (
n
=
14
0)
N
. r
os
sii
(
n=
3
)
P.
ch
ar
co
ti
(n
=
1
5)
Ch
. a
ce
ra
tu
s
(n
=
6
)
T.
b
er
na
cc
hi
i
(n
=
6
)
H
. a
nt
-
ar
ct
i-c
us
(n
=
1
)
I (
m
in
–
m
ax
)
P*
I (
m
in
–
m
ax
)
P,
%
I (
m
in
–
m
ax
)
P,
%
I (
m
in
–
m
ax
)
P,
%
I (
m
in
–
m
ax
)
+/
—
**
PL
A
TY
H
EL
M
IN
TH
ES
: M
O
N
O
G
EN
EA
1.
Ps
eu
do
be
ne
de
ni
a
no
to
th
en
ia
e
Jo
hn
sto
n,
19
31
36
,8
6.
7
(1
–4
2)
1/
3
1
–
–
–
–
–
–
–
PL
A
TY
H
EL
M
IN
TH
ES
: T
RE
M
A
TO
D
A
2.
El
yt
ro
ph
al
lo
id
es
o
at
es
i
(L
ei
pe
r e
t A
tk
in
so
n,
1
91
4)
43
.2
5.
6
(1
–3
6)
2/
3
62
.0
(2
8–
96
)
40
.0
22
.8
(1
–7
1)
10
0.
0
12
.4
(1
–4
8)
50
.0
6.
3
(1
–6
6)
–
3.
Ge
no
lin
ea
b
ow
er
si
(L
ei
pe
r e
t A
tk
in
so
n,
1
91
4)
68
.0
10
.1
(1
–4
2)
2/
3
30
.5
(3
–5
8)
53
.3
27
.7
(1
–1
13
)
10
0.
0
23
.2
(1
–6
9)
50
.0
5.
0
(2
–7
)
+
4.
Gl
om
er
ici
rr
us
m
ac
ro
ur
i
(G
ae
vs
ka
ja
, 1
97
3)
–
–
–
–
6.
7
2
16
.7
1
33
.3
1.
5
(1
–2
)
–
5.
Le
cit
ha
ste
r m
ac
ro
co
ty
le
Sz
id
at
et
G
ra
ef
e,
19
67
2.
4
2.
0
(1
–3
)
–
–
13
.3
2.
0
(1
–3
)
33
.3
6.
0
(4
–8
)
16
.7
1
–
6.
Le
pi
da
pe
do
n
ga
rr
ar
di
(L
ei
pe
r e
t A
tk
in
so
n,
1
91
4)
7.
2
1.
4
(1
–3
)
–
–
6.
7
1
–
–
–
–
–
7.
M
ac
vi
ca
ria
ge
or
gi
an
a
(K
ov
al
jo
va
et
G
ae
vs
ka
ya
,1
97
4)
80
.8
25
.2
(1
–1
22
)
1/
3
1
–
–
66
.7
3.
8
(1
–9
)
–
–
–
8.
M
ac
vi
ca
ria
p
en
ne
lli
(L
ei
pe
r &
A
tk
in
so
n,
1
91
4)
–
–
–
–
73
.3
5.
6
(1
–1
9)
–
–
–
–
–
9.
N
eo
leb
ou
ria
ge
or
gi
en
sis
G
ib
so
n,
1
97
6
4.
8
2.
8
(1
–7
)
1/
3
1
93
.3
70
.0
(4
–2
22
)
83
.3
34
.0
(2
–1
15
)
–
–
–
10
.
Le
cit
op
ha
llu
m
sp
.
–
–
–
–
6.
7
2
–
–
–
–
11
.
D
er
og
en
es
jo
hn
sto
ni
Pr
ud
ho
e e
t B
ra
y,
1
97
3
4.
0
1.
8
(1
–5
)
1/
3
15
6.
7
1
16
.7
1
33
.3
2.
5
(1
–4
)
–
PL
A
TY
H
EL
M
IN
TH
ES
: C
ES
TO
D
A
12
.
D
ip
hy
llo
bo
th
riu
m
sp
.
78
.4
11
.1
(1
–5
8)
–
–
46
.7
10
.3
(1
–3
3)
10
0.
0
36
.0
(8
–7
5)
10
0.
0
15
.0
(2
–4
1)
–
13
.
M
on
ol
oc
ul
ar
m
et
ac
es
to
de
11
.2
1.
5
(1
–4
)
–
–
13
.3
1.
0
(1
–1
)
50
.0
1.
0
(1
–1
)
–
–
–
14
.
Bi
lo
cu
la
r m
et
ac
es
to
de
34
.4
2.
3
(1
–8
)
–
–
80
.0
8.
8
(1
–2
6)
50
.0
5.
7
(1
–1
4)
–
–
–
255Helminth diversity in teleost fi shes from the area of the Ukrainian Antarctic Station “Akademik Vernadsky”…
15
.
Tr
ilo
cu
la
r m
et
ac
es
to
de
13
.6
1.
4
(1
–3
)
–
–
40
.0
1.
2
(1
–2
)
–
–
–
–
–
N
EM
A
TO
D
A
: C
H
RO
M
A
D
O
RE
A
16
.
As
ca
ro
ph
is
no
to
th
en
ia
e
Jo
hn
sto
n
et
M
aw
so
n,
1
94
5
9.
6
12
.4
(1
–4
9)
–
–
33
.3
18
.0
(1
–3
9)
66
.7
36
.3
(1
4–
65
)
66
.7
4.
9
(1
–8
)
–
17
.
D
ich
ely
ne
fr
as
er
i (
Ba
yl
is,
1
92
9)
5.
6
1.
3
(1
–3
)
–
–
–
–
–
–
–
–
–
18
.
An
isa
ki
s s
p.
4.
8
1.
5
(1
–2
)
–
–
13
.3
1.
0
(1
–1
)
16
.7
1
16
.7
1
–
19
.
Co
nt
ra
ca
ec
um
sp
.
40
.0
5.
1
(1
–3
1)
2/
3
23
.0
(9
–3
7)
10
0.
0
43
.3
(2
–2
80
)
10
0.
0
30
8.
5
(1
–7
01
)
66
.7
2.
5
(1
–5
)
+
20
.
Ps
eu
do
te
rr
an
ov
a
sp
.
96
.0
14
.2
(1
–7
4)
3/
3
11
.0
(2
–2
1)
10
0.
0
57
.7
(1
3–
17
8)
10
0.
0
18
5.
5
(5
9–
40
3)
66
.7
3.
8
(2
–8
)
+
A
CA
N
TH
O
CE
PH
A
LA
: P
A
LA
EA
CA
N
TH
O
CE
PH
A
LA
21
.
As
pe
rs
en
tis
m
eg
ar
hy
nc
hu
s
(L
in
sto
w
, 1
89
2)
=
sy
n.
A
. a
us
t-
rin
us
V
an
C
le
av
e,
19
29
11
.2
4.
0
(1
–1
7)
1/
3
1
–
–
–
–
–
–
–
22
.
Co
ry
no
so
m
a
bu
llo
su
m
(L
in
sto
w
, 1
89
2)
–
–
–
–
33
.3
2.
8
(1
–6
)
66
.7
2.
5
(2
–3
)
–
–
–
23
.
C.
ev
ae
Z
dz
ito
w
ie
ck
i,
19
84
15
.2
5.
2
(1
–1
3)
3/
3
5.
7
(1
–1
3)
26
.7
5.
5
(2
–8
)
83
.3
16
.4
(7
–5
1)
66
.7
5.
0
(1
–1
7)
+
24
.
C.
h
am
an
ni
(L
in
sto
w
, 1
89
2)
3.
2
5.
0
(1
–1
4)
–
–
20
.0
7.
3
(1
–1
8)
50
.0
15
.7
(4
–2
6)
16
.7
1
–
25
.
C.
p
se
ud
oh
am
an
ni
Zd
zi
to
w
ie
ck
i,
19
83
37
.6
26
.8
(1
–1
38
)
3/
3
12
8.
7(
38
–
24
4)
86
.7
20
.9
(1
–8
9)
83
.3
14
6.
2
(8
0–
30
1)
10
0.
0
8.
5
(1
–1
6)
+
26
.
C.
sh
ac
kl
et
on
i Z
dz
ito
w
ie
ck
i,
19
78
8.
8
1.
2
(1
–2
)
–
–
–
–
16
.7
1
–
–
–
27
.
Ec
hi
no
rh
yn
ch
us
p
et
ro
tsc
he
nk
oi
(R
od
ju
k,
1
98
4)
–
–
–
–
13
.3
1.
0
(1
–1
)
–
–
–
–
–
28
.
M
et
ac
an
th
oc
ep
ha
lu
s d
al
m
or
i
Zd
zi
to
w
ie
ck
i,
19
83
39
.2
4.
7
(1
–3
3)
–
–
73
.3
1.
0
(1
–1
)
16
.7
1
–
–
–
29
.
M
. c
am
pb
ell
i
(L
ei
pe
r &
A
tk
in
so
n,
1
91
4)
30
.4
3.
4
(1
–1
4)
3/
3
2.
0
(1
–3
)
66
.7
5.
5
(1
–1
8)
66
.7
4.
3
(1
–7
)
66
.7
2.
5
(1
–6
)
–
30
.
M
. j
oh
ns
to
ni
Z
dz
ito
w
ie
ck
i,
19
83
83
.2
10
.4
(1
–6
2)
3/
3
15
.7
(9
–2
3)
73
.3
6.
2
(1
–2
0)
66
.7
5.
5
(1
–1
1)
33
.3
2.
5
(2
–3
)
–
31
.
M
. r
en
ni
ck
i
(L
ei
pe
r &
A
tk
in
so
n,
1
91
4)
85
.6
9.
3
(1
–7
9)
2/
3
15
.0
(8
–2
2)
93
.3
17
.3
(2
–7
8)
83
.3
10
.4
(2
–3
5)
50
.0
1.
0
(1
–1
)
+
*P
re
va
le
nc
e i
s i
nd
ic
at
ed
as
a
nu
m
be
r o
f i
nf
ec
te
d
sp
ec
im
en
s o
f 3
ex
am
in
ed
fi
sh
es
.
**
Pr
es
en
ce
(+
) o
r a
bs
en
ce
(—
) o
f t
he
h
el
m
in
th
sp
ec
ie
s i
n
H
A
h
os
t.
C
on
ti
ni
ed
T
ab
le
2
.
256 T. A. Kuzmina, I. V. Dykyy, O. O. Salganskij, O. I. Lisitsyna, E. M. Korol, Yu. I. Kuzmin
In terms of species diversity, the proportion of separate parasite taxa varied in diff erent
fi sh species. Nevertheless, in all fi sh species studied, the largest numbers of species were
recorded for acanthocephalans and digenean trematodes (fi g. 1).
In term of the intensity of fi sh infection, nematodes prevailed in predacious fi sh species
Ch. aceratus (up to 66 % of total helminth number) and P. charcoti (up to 40 %); while
N. coriiceps, N. rossii and T. bernacchii which feed on macroalgae and benthic invertebrates
(amphipods, isopods, euphausiids, polychaetes, molluscs) were infected mostly with
acanthocephalans, trematodes and larval stages of cestodes (fi g. 2).
Twenty-six helminth species were recorded in N. coriiceps (table 2). Eleven
species including all cestodes, nematodes of the genera Anisakis, Contracaecum and
Pseudoterranova, and acanthocephalans of the genus Corynosoma parasitize this fi sh host
at their larval stages; therefore, N. coriiceps is considered to be a defi nitive host for 15 out
of 26 helminth species recorded. In three specimens of the another species of the genus
Notothenia, N. rossii, 14 helminth species were found, six of them parasitized this host on
their larval stages (table 2). Th us, N. rossii is considered to be a defi nitive host for eight out
of 14 helminth species recorded.
Twenty-seven helminth species were found in P. charcoti (table 2); it is considered to
be a defi nitive host for 15 out of 27 helminth species recorded. In Ch. aceratus, 23 helminth
species were found; the blackfi n icefi sh is a defi nitive host of 13 out of 23 helminth species
recorded. In T. bernacchii, 16 helminth species were found; the emerald rockcod is a defi nitive
host for nine out of 16 helminth species. Th e smallest number of helminths was found in one
examined specimen of H. antarcticus: six species of three taxonomic groups (table 2).
Th ree helminth species were fi rst registered in separate teleost fi shes: cercoids of
monolocular metacestode were fi rst found in P. charcoti and Ch. aceratus; monogenean
Derogenes johnstoni was fi rst recorded in P. charcoti and Ch. aceratus, and the larval stages
of Anisakis sp. in P. charcoti, Ch. aceratus and T. bernacchii. All three helminth species
were rather rare in all fi sh hosts, just single specimens of them were found in all infected
fi sh individuals (table 2).
Fig. 1. Proportion (%) of fi ve parasite taxa found in teleost fi sh off the area of the UAS “Akademik Vernadsky”,
Argentine Islands, West Antarctica.
257Helminth diversity in teleost fi shes from the area of the Ukrainian Antarctic Station “Akademik Vernadsky”…
Proportion of helminth species parasitizing teleost fi sh species on larval stages was
42–44 %, while 56–58 % of helminths found in fi ve fi sh species were adult parasites (fi g. 3).
Data on the prevalence and intensity of infection of fi ve teleost fi sh species
with separate helminth species (see table 2) demonstrated that trematodes E. oatesi,
G. bowersi, Macvicaria spp., larvae of Diphyllobothrium sp., nematodes from the genera
Contracaecum and Pseudoterranova and acanthocephalans from the genera Corynosoma
and Metacanthocephalus were prevalent in fi ve fi sh species examined (parameters of
H. antarcticus infection are not estimated).
We analyzed the species richness in the parasite communities from four fi sh species
examined (table 3). Expectedly, larger host samples contained a comparatively larger
number of helminth species. On the other hand, the helminth species richness in P. charcoti
appeared to be similar to that in N. coriiceps, despite the diff erence in the sample size. Th e
helminth species richness in Ch. aceratus, both observed and estimated, was higher than
that in T. bernacchii, while the host sample size was the same. Even though the sample size
of Ch. aceratus and T. bernacchii (n = 6) could not yield statistically signifi cant estimation of
the helminth species richness, it may be presumed that the richness is higher in the former
host species. Th is observation is confi rmed by the higher average species richness in the
helminth infracommunities in Ch. aceratus, 13.7 vs. 8.3 (table 3). Besides, this parameter
Fig. 2. Intensity of teleost fi sh infection off the area of the UAS “Akademik Vernadsky” by fi ve parasite taxa
(proportion of diff erent parasite taxa is in %).
T a b l e 3 . Parameters of the helminth species richness in separate fi sh species examined off the area of the
UAS “Akademik Vernadsky”, Argentine Islands, West Antarctica
Parameters of species richness N. coriiceps
(n = 140)
P. charcoti
(n = 15)
Ch. aceratus
(n = 6)
T. bernacchii
(n = 6)
Observed number of species 26 27 23 16
Estimated species richness (Chao1 ± SD) 28 ± 2.6 28 ± 0.9 23 ± 9.5 16 ± 6.6
Estimated species richness (bootstrap) 29 29 25 17
Species richness in infracommunities:
mean [median] (min–max)
9.0 [8]
(3–15)
13.2 [13]
(10–20)
13.8 [13.5]
(8–20)
8.3 [8]
(6–12)
258 T. A. Kuzmina, I. V. Dykyy, O. O. Salganskij, O. I. Lisitsyna, E. M. Korol, Yu. I. Kuzmin
was higher in helminth infracommunities in P. charcoti (13.2) compared to those in
N. coriiceps (9.0), though the species richness in the helminth component community was
similar in two hosts.
Similarity of the helminth communities of fi ve fi sh species examined, excluding a
single specimen of H. antarcticus, was rather high; the Sørensen index between all samples
was higher than 0.50. Th e maximum similarity was noted for helminth communities of
Ch. aceratus and P. charcoti (Sørensen index = 0.88); the helminth community of N. rossii
was the least similar to other host species (Sørensen index = 0.67). Th e cluster analysis
confi rmed the similarity of the helminth communities of Ch. aceratus and P. charcoti
(fi g. 4); the helminth community N. coriiceps was found to be the closest to the cluster of
Ch. aceratus and P. charcoti.
Discussion
Our study provides new data on the species diversity of helminths parasitize the main
teleost fi sh species in the region of Argentine Islands, West Antarctica; these data extend
the list of helminth species to 31 species. In previous parasitological studies performed at
the UAS “Akademik Vernadsky” in 2002, 21 species of helminths were found in teleost
fi shes, in particular, 21 in N. coriiceps, 14 in T. bernacchii, and seven in H. antarcticus
(Zdzitowiecki & Laskowsky, 2004; Laskowsky & Zdzitowiecki, 2005). Any information on
the parasite fauna of N. rossii, P. charcoti, and Ch. aceratus from the Argentine Islands area
has not been published till now.
Species diversity of the helminth communities in teleost fi sh registered in our study
was rather high: 27 helminth species were found in P. charcoti, 26 in N. coriiceps, and
23 in Ch. aceratus (table 2). Th e lower number of helminth species found in N. rossii,
T. bernacchii, and H. antarcticus is apparently associated with a small number of specimens
of each of these fi sh species examined in the present study. Th ese three fi sh species are rare
in the Argentine Islands region; in scientifi c catches in the waters of the UAS “Akademik
Vernadsky” the proportions of these fi sh species were from 0.6 % to less than 10 % (Manilo,
Fig. 3. Proportion (in %) of helminth species parasitize fi ve Antarctic teleost fi shes off the area of the UAS
“Akademik Vernadsky” on larval and adult stages.
259Helminth diversity in teleost fi shes from the area of the Ukrainian Antarctic Station “Akademik Vernadsky”…
2006; Veselskyy & Khoetskyy, 2018). Analysis of the published data on the parasites of
these rare fi sh species from other regions of West Antarctica revealed that the number of
specimens in samples studied by other researchers was also small, from single specimens to
10–15 specimens caught from one place (Zdzitowiecki, 2001; Laskowsky & Zdzitowiecki,
2005; Palm et al., 2007). Th us, our data on the helminth species diversity of teleost fi shes
collected in the present study are comparable with those from other regions of West
Antarctica.
Of the fi ve taxa of metazoan parasites found in Antarctic fi shes in this study, the
greatest species diversity was recorded for acanthocephalans (11 species) and digenean
trematodes (10 species). Th e intensity of fi sh infection by diff erent helminth taxa diff ered
signifi cantly. In the predatory blackfi n icefi sh Ch. aceratus, nematodes accounted for 66 %
of the total helminth number, with 95.4 % of them being larval stages of anisakid nematodes
of the genera Contracaecum (58.4 %) and Pseudoterranova (37.0 %). Th ese nematodes are
parasites of pinnipeds; they use teleost fi shes are their paratenic hosts (Mozgovoy, 1951;
Palm et al., 1998; Anderson, 2000; Rocka, 2006). Other fi sh species feeding mostly on
benthic invertebrates and macroalgae were mainly infected with acanthocephalans and
trematodes which are transmitted via various species of amphipods, isopods, euphausiids
and molluscs as their intermediate hosts.
In the present study, the helminth community of Antarctic rockcod N. coriiceps
included 26 species from fi ve taxonomic groups (monogeneans, trematodes, cestodes,
nematodes and acanthocephalans). In the studies conducted at UAS “Akademik Vernadsky”
in 2002, 21 helminth species were found in this fi sh species (Zdzitowiecki & Laskowsky,
2004). Previously, the helminth fauna of N. coriiceps was investigated in diff erent regions of
Antarctica. Twenty-two parasites species including 18 species of helminths were recorded
in N. coriiceps in the Potter Cove of the King George Island (Palm et al., 1998); 27 helminth
species were found in the Admiralty Bay region of the King George Island and South
Shetland Islands (Zdzitowiecki & Laskowsky, 2004). In recent research in the Fildes Bay
area near King George Island, 12 helminth species have been found (Muñoz & Rebolledo,
2019). Th us, of the 41 helminth species registered in total in N. coriiceps (see Oğuz et al.,
Fig. 4. Cluster analysis of the similarity between the helminth communities in fi ve teleost fi sh species off the area
of the UAS “Akademik Vernadsky”, Argentine Islands, and West Antarctica.
260 T. A. Kuzmina, I. V. Dykyy, O. O. Salganskij, O. I. Lisitsyna, E. M. Korol, Yu. I. Kuzmin
2015), 63 % were found in the present study. Th is indicates a rather high helminth species
richness in this fi sh species in the region of the Argentine Islands.
Th e second fi sh species of the genus Notothenia, N. rossii, is rare in the area of the
Argentine Islands; its proportion in catches is about 1 % (Manilo, 2006; Veselskyy &
Khoetskyy, 2018). Only 3 specimens of N. rossii were caught and examined in the present
study; this number does not allow a reliable assessing of the main parameters of its
infection with helminth. However, 14 species of helminths were found in the three studied
specimens, which constitutes 41.2 % of the 34 helminths species previously recorded in
N. rossii (Oğuz et al., 2015; Muñoz & Rebolledo, 2019). In East Antarctica, 19 helminth
species of helminths were collected from 30 specimens of N. rossii (Parukhin, 1986); while
in recent studies near King George Island, West Antarctica, only 13 species were recorded
in this host (Muñoz & Rebolledo, 2019). We believe that more helminth species would be
found in larger fi sh samples of N. rossii from the Argentine Islands area.
Th e highest species diversity was registered in Antarctic dragonfi sh P. charcoti —
27 species of helminths representing 93 % of the total helminth species number recorded
in this fi sh species (Oğuz et al., 2015; Münster et al. 2017). Data on the helminth species
richness in P. charcoti signifi cantly diff er in diff erent studies performed in West Antarctica.
Zdzitowiecki (2001) registered 18 species of helminths in the Antarctic dragonfi sh from
the Bransfi eld Strait and Joinville shelf. In the studies conducted by Palm et al. (2007), and
later by Münster et al. (2017) on the German research vessel Polarstern at the depth of 80–
480 m and 100-300 m, each of the researchers found 11 species of helminths in P. charcoti;
the total number of species detected and identifi ed by these authors was 13. We believe
that the greater species richness in the P. charcoti helminth community in our study is
connected with comparatively higher diversity of invertebrates (crustaceans and molluscs)
in the coastal waters near Galindez Island; these invertebrates are intermediate hosts of
trematodes and acanthocephalans and participate in the transmission of these parasites in
coastal ecosystems.
Twenty-three helminths species were recorded in six specimens of the blackfi n icefi sh,
Ch. aceratus in the present study; this number comprises 79 % of the total number of
29 species recorded in this host (Oğuz et al., 2015). Th e blackfi n icefi sh were mainly infected
with nematodes (66 % of the total helminth number), mostly with larval stages of anisakid
nematodes of the genera Contracaecum and Pseudoterranova (see table 2). Various authors
noted that Channichthyids, including blackfi n icefi sh, occupy a key position in the life
cycles of anisakids in the Antarctic (Kock, 1992; Oğuz et al., 2012; Kuhn et al., 2018); their
defi nitive hosts are marine mammals (Weddel seal, Antarctic fur seal, etc.). Predacious
Ch. aceratus feeds mostly on small pelagic fi shes and krill; therefore it actively accumulates
anisakid larvae as the paratenic host. High infection of Ch. aceratus by anisakid nematodes
was also recorded in previous studies (Siegel, 1980; Palm et al., 2007; Rokicki et al., 2009;
Oğuz et al., 2012).
In emerald rockcod, T. bernacchii 16 helminth species were recorded; this number
corresponds to 64 % of a total of 25 species reported in this fi sh (Oğuz et al., 2015). From
eight to 14 helminth species were recorded in the helminth community of T. bernacchii
in separate studies previously (Moser & Cowen, 1991; Laskowski & Zdzitowiecki, 2005;
Zdzitowiecki & Ozouf-Costaz, 2013); thus, our data indicate a rather high helminth species
diversity in this fi sh species from the Argentine Islands region.
Only one specimen of rare demersal fi sh species H. antarcticus, was examined in the
present study. Accordingly, six helminth species were found. Th is represents only 35 %
of the 17 species recorded in this host (Zdzitowiecki & Zadrozny 1999; Oğuz et al., 2015).
In the previous parasitological study of two H. antarcticus specimens from the Galindez
Island area, seven helminth species were found (Laskowski & Zdzitowiecki, 2005). Also,
seven helminth species were identifi ed in ten specimens of this fi sh from the Fildes Bay of
King George Island (Muñoz & Cartes, 2020). Earlier, Zdzitowiecki and Zadrozny (1999)
261Helminth diversity in teleost fi shes from the area of the Ukrainian Antarctic Station “Akademik Vernadsky”…
identifi ed 15–16 species and larval forms of helminths from 50 specimens of H. antarcticus.
Th e material collected in our study does not allow us to perform any analysis of the parasite
community; therefore, this fi sh species was excluded from the data analysis.
Analysis of the species richness in the helminth communities from four fi sh species
represented by larger samples in the present study revealed the similarity of this parameter
in the communities from P. charcoti and N. coriiceps, despite the diff erence in the sample
size of these hosts. Also, a comparatively high helminth species richness was recorded
in six specimens of the predatory fi sh Ch. aceratus (table 3). We assume that the higher
species richness in the infracommunities of predatory fi sh species Ch. aceratus (13.8 species
per host) and P. charcoti (13.2 species per host) is associated with the accumulation of
helminths in predatory fi shes due to their feeding on both invertebrate intermediate and
fi sh paratenic hosts of helminths.
Comparison of the helminth species diversity in six fi sh species studied revealed
very low host-specifi city of the helminths; only the trematode Macvicaria penelli and the
nematode Dichelyne fraseri were found each in one host species in our study. However,
both these species were found in several Antarctic fi shes in previos surveys (see Oğuz et
al., 2015). In our study, fi ve helminth species were recorded from all six fi sh hosts, fi ve
species — in 5 hosts, and 4 species — in 4 fi sh hosts (table 2). Low host specifi city was
previously reported for all groups of helminths of Antarctic fi shes (Rocka, 2006, 2017;
Faltýnková et al., 2017; Laskowski & Zdzitowiecki, 2017) except monogeneans (Klapper et
al., 2017). We suppose that low host specifi city in Antarctic helminths is associated both
with a wide range of invertebrate species, which can be intermediate hosts of helminths
(Rocka, 2006; Busch et al., 2012) as well as a wide variety of diets of the Antarctic fi sh
species that includes various invertebrates and small fi sh species (McKenna, 1991; Reid et
al., 2007; Kuhn et al., 2018; Barrera-Oro et al., 2019).
Comparison of the species composition of the helminth communities in fi ve fi sh species
examined in this study using the Sørensen index showed that even in a small number of
examined individuals, the helminth communities of the predatory fi sh species Ch. aceratus
and P. charcoti had the greatest similarity; the omnivorous species N. coriiceps was found
to be the closest to them. Th e diff erences in the species composition of the helminth
communities of N. rossii and T. bernacchii from other fi sh species observed in this study
should be verifi ed by investigation of large samples of these fi sh species.
As fi sh parasites are directly linked to the food chain in the Southern Ocean (Kuhn et
al., 2018; Barrera-Oro et al., 2019), and the Antarctic bony fi shes play an important role
in the completion of life cycles of many helminth species as their defi nitive, intermediate
and paratenic hosts (Palm et al., 1998; Rocka, 2006, 2017), the information on the species
diversity of teleost fi sh parasites and its temporal and spatial changes can provide valuable
information on ecology, trophic interactions and state of populations of various Antarctic
vertebrates, including marine mammals and fi sh-eating birds in the Argentine Islands
region. We believe that the current data on the species diversity of helminth communities of
the main teleost fi sh species obtained in our study can be used as a baseline for further long-
term monitoring studies of fi sh parasite communities and allow to estimate the changes in
the marine ecosystems of West Antarctica.
Th e authors thank Prof. Terry R. Spraker from Colorado State University for his valuable comments and
corrections to the manuscript. Th is study was partially supported by the National Research Foundation of
Ukraine (project number 2020.02/0074) and by the National Antarctic Scientifi c Center, Ministry of Education
and Science of Ukraine (project number H/12-2020).
References
Anderson, R. C. 2000. Nematode Parasites of Vertebrates. Th eir Development and Transmission. Second Edition.
CABI Publishing, Wallingford, 1–650.
262 T. A. Kuzmina, I. V. Dykyy, O. O. Salganskij, O. I. Lisitsyna, E. M. Korol, Yu. I. Kuzmin
Barnes, D. K. A., Peck, L. S. 2008. Vulnerability of Antarctic shelf biodiversity to predicted regional warming.
Climate Research, 37 (2–3), 149–163.
Barrera-Oro, E., Moreira, E., Seefeldt, M. A., Mariano, V. F., Quartino, M. L. 2019. Th e importance of macroal-
gae and associated amphipods in the selective benthic feeding of sister rockcod species Notothenia rossii
and N. coriiceps (Nototheniidae) in West Antarctica. Polar Biology, 42 (2), 317–334.
Brickle, P., MacKenzie, K., Pike, A. 2005. Parasites of the Patagonian toothfi sh, Dissostichus eleginoides Smitt
1898, in diff erent parts of the Subantarctic. Polar Biology, 28 (9), 663–671.
Busch, M. W., Kuhn, T., Munster, J., Klimpel, S. H. 2012. Marine Crustaceans as Potential Hosts and Vectors
for Metazoan Parasites. In: Mehlhorn, H., ed. Arthropods as Vectors of Emerging Diseases. Parasitology
Research Monographs 3, Springer, Berlin, Heidelberg, 239–360.
Bush, A. O., Laff erty, K. D., Lotz, J. M., Shostak, A. W. 1997. Parasitology meets ecology on its own terms:
Margolis et al. revisited. Journal of Parasitology, 83 (4), 575–583.
Chown, S. L., Clarke, A., Fraser, C. I., Cary, S. C., Moon, K. L., McGeoch, M. A. 2015. Th e changing form of
Antarctic biodiversity. Nature, 522 (7557), 431–438.
Clarke, K. R., Gorley, R. N. 2006. PRIMER v6: User Manual/Tutorial (Plymouth Routines in Multivariate
Ecological Research). PRIMER-E, Plymouth.
Clarke, A., Johnston, N. M., Murphy, E. J., Rogers, A. D. 2007. Introduction: Antarctic ecology from genes to
ecosystems: the impact of climate change and the importance of scale. Philosophical Transactions of the
Royal Society, B, 362, 5–9.
Daszak, P., Cunningham, A. A., Hyatt, A. D. 2001. Anthropogenic environmental change and the emergence of
infectious diseases in wildlife. Acta Tropica, 78 (2), 103–116.
De Broyer, C., Koubbi, P., Griffi hs, H. J., Raymond, B., Udekem d’Acoz, C. d’, Van de Putte, A. P., Danis, B.,
David, B., Grant, S., Gutt, J., Held, C., Hosie, G., Huettmann, F., Post, A., Ropert-Coudert, Y., eds. 2014.
Biogeographic Atlas of the Southern Ocean. Scientifi c Committee on Antarctic Research, Cambridge,
1–498.
Eastman, J. T. 1991. Evolution and diversifi cation of Antarctic notothenioid fi shes. American Zoologist, 31 (1),
93–109.
Faltýnková, A., Georgieva, S., Kostadinova, A., Bray, R. A. 2017. Biodiversity and Evolution of Digeneans of
Fishes in the Southern Ocean. In: Klimpel, S., Kuhn, T., Mehlhorn, H., eds. Biodiversity and Evolution of
Parasitic Life in the Southern Ocean. Parasitology Research Monographs, vol. 9. Springer, Cham, 49–75.
Gibson, D. I., Jones, A., Bray, R. A. 2002. Keys to the Trematoda. Volume 1. CABI & Natural History Museum,
Wallingford, UK, 1–544.
Gordeev, I. I., Sokolov, S. G. 2016. Parasites of the Antarctic toothfi sh (Dissostichus mawsoni Norman, 1937)
(Perciformes, Nototheniidae) in the Pacifi c sector of the Antarctic. Polar Research, 35, 29364.
Hammer, Ø., Harper, D. A. T., Ryan, P. D. 2001. PAST: Paleontological Statistics Soft ware Package for
Education and Data Analysis. Palaeontologia Electronica, 4, 9. http://palaeo-electronica.org/2001_1/past/
issue1_01.htm
Hudson, P. J., Dobson, A. P., Laff erty, K. D. 2006. Is a healthy ecosystem one that is rich in parasites? Trends in
Ecology and Evolution, 21 (7), 381–385.
Jones, A., Bray, R. A., Gibson, D. I. 2005. Keys to the Trematoda. Volume 2. CABI & Natural History Museum,
Wallingford, UK, 1–768.
Khan, R. A., Th ulin. J. 1991. Infl uence of pollution on parasites of aquatic animals. Advances in Parasitology,
30, 201–239.
Klapper, R., Münster, J., Kochmann, J., Klimpel, S., Kuhn, T. 2017. Biodiversity and Host Specifi city of
Monogenea in Antarctic Fish Species. In: Klimpel, S. et al., eds. Biodiversity and Evolution of Parasitic Life
in the Southern Ocean. Parasitology Research Monographs, vol. 9, 33–47.
Klimpel, S., Kuhn, T., Mehlhorn, H. 2017. Introduction: Biodiversity and evolution of parasitic life in the
Southern Ocean. In: Klimpel, S., Kuhn, T., Mehlhorn, H., eds. Biodiversity and Evolution of Parasitic Life
in the Southern Ocean. Parasitology Research Monographs. Springer, Cham, 9, 1–5.
Kock, K.-H. 1992. Antarctic fi sh and fi sheries. Cambridge University Press, 1–359.
Kuhn, T., Zizka, V. M. A., Münster, J., Klapper, R., Mattiucci, S., Kochmann, J., Klimpel, S. 2018. Lighten up
the dark: metazoan parasites as indicators for the ecology of Antarctic crocodile icefi sh (Channichthyidae)
from the north-west Antarctic Peninsula. PeerJ. 6: e4638.
Kuzmina, T. A., Salganskij, O. O., Lisitsyna, O. I., Korol, E. M. 2020. Helminths of Antarctic rockcod No-
tothenia coriiceps (Perciformes, Nototheniidae) from the Akademik Vernadsky Station area (Argentine
Islands, West Antarctica): new data on the parasite community. Zoodiversity, 54 (2), 99–110.
Kvach, Y., Kuzmina, T. 2020. Parasitological research in Antarctica: review of the issues and future prospects.
Ukrainian Antarctic Journal, 1, 102–110 [In Ukrainian].
Laskowski, Z., Zdzitowiecki, K. 2005. Th e helminth fauna of some notothenioid fi shes collected from the shelf
of Argentine Islands, West Antarctica. Polish Polar Research, 26 (4), 315–324.
Laskowski, Z., Korczak-Abshire, M., Zdzitowiecki, K. 2012. Changes in acanthocephalan infection of the Ant-
arctic fi sh Notothenia coriiceps in Admiralty Bay, King George Island, over 29 years. Polish Polar Research,
33 (1), 99–108.
263Helminth diversity in teleost fi shes from the area of the Ukrainian Antarctic Station “Akademik Vernadsky”…
Laskowski, Z., Zdzitowiecki, K. 2017. Acanthocephalans in Sub-Antarctic and Antarctic. In: Klimpel, S.,
Kuhn, T., Mehlhorn, H., eds. Biodiversity and Evolution of Parasitic Life in the Southern Ocean. Parasitol-
ogy Research Monographs, vol. 9. Springer, Cham, 141–182.
Laskowski, Z., Rocka, A., Zdzitowiecki, K., Ozouf-Costaz, C. 2007. Occurrence of endoparasitic worms in
dusky notothen, Trematomus newnesi (Actinopterygii Nototheniidae), at Adelie Land, Antarctica. Polish
Polar Research, 28 (1), 37–42.
Manilo, L. G. 2006. Ichthyofauna and morphobiological characteristics of mass fi sh species of coastal waters of
Argentine Islands (Antarctica). Zbirnyk prats Zoologichnogo Muzeyu, 38 (1), 5–22 [In Ukrainian].
McKenna, J. E. Jr. 1991. Trophic relationships within the Antarctic demersal fi sh community of South Georgia
Island. Fishery bulletin U.S., 89 (4), 643–654.
MacKenzie, K. 2017. Th e history of Antarctic parasitological research. In: Klimpel, S., Kuhn, T., Mehlhorn, H.,
eds. Biodiversity and evolution of parasitic life in the Southern Ocean. Parasitology Research Monographs,
vol. 9. Springer Nature, Cham, 13–31.
Moser, M., Cowen, R. K. 1991. Th e eff ects of periodic eutrophication on parasitism and stock identifi cation of
Trematomus bernacchii (Pisces: Nototheniidae) in McMurdo Sound, Antarctica. Journal of Parasitology,
77 (4), 551–556.
Mouritsen, K. N., Poulin, R. 2002. Parasitism, climate oscillations and the structure of natural communities.
Oikos, 97 (3), 462–468.
Mozgovoy, A. A. 1951. Ascaridata of animals and man, and the diseases caused by them. Osnovy nematodologii.
Vol. II. Izd-vo AN SSSR, Moskva, 1–616 [In Russian].
Muñoz, G., Cartes, F. D. 2020. Endoparasitic diversity from the Southern Ocean: is it really low in Antarctic
fi sh? Journal of Helminthology, 94, e180, 1–10.
Muñoz, G., Rebolledo, M. 2019. Comparison of the parasite community of two notothens, Notothenia rossii
and N. coriiceps (Pisces: Nototheniidae), from King George Island, Antarctica. Journal of Helminthology,
93 (6), 732–737.
Münster, J., Kochmann, J., Grigat, J., Klimpel, S., Kuhn T. 2017. Parasite fauna of the Antarctic dragonfi sh
Parachaenichthys charcoti (Perciformes: Bathydraconidae) and closely related Bathydraconidae from the
Antarctic Peninsula, Southern Ocean. Parasites Vectors, 10, 2–35.
Near, T. J. 2009. Notothenioid fi shes (Notothenioidei). In: Hedges, S. B., Kumar, S., eds. Th e Timetree of Life.
Oxford University Press, 339–343.
Near, T. J., Dornburg, A., Kuhn, K. L., Eastman, J. T., Pennington, J. N., Patarnello, T., Zane, L., Fernández, DA,
Jones, CD. 2012. Ancient climate change, antifreeze, and the evolutionary diversifi cation of Antarctic fi sh-
es. Proceedings of the National Academy of Sciences of the United States of America, 109 (9), 3434–3439.
Oğuz, M. C., Heckmann, R. A., Cheng, C. H. C., El-Naggar, A., Tepe, Y. 2012. Ecto and endoparasites of some
fi shes from the Antarctic Region. Scientia Parasitologica, 13 (3), 119–128.
Oğuz, M. C., Tepe, Y., Belk, M. C., Heckmann, R. A., Aslan, B., Gürgen, M., Bray, R. A., Akgül, Ü. 2015.
Metazoan parasites of Antarctic fi shes. Türkiye Parazitoloji Derneği, 39, 174–178.
Palm, H. W., Reimann, N., Spindler, M., Plötz, J. 1998. Th e role of the rock cod Notothenia coriiceps (Richardson,
1844) in the life-cycle of Antarctic parasites. Polar Biology, 19 (6), 399–406.
Palm, H. W., Klimpe, S., Walter, T. 2007. Demersal fi sh parasite fauna around the South Shetland Islands; high
species richness and low host specifi city in deep Antarctic waters. Polar Biology, 30 (12), 1513–1522.
Parukhin, A. M. 1986. Helminthofauna peculiarities of commercial Nototheniodei from the SubAntarktic re-
gion of the Indian Ocean. Vestnik Zoologii, 3, 6–10.
Parukhin, A. M., Lyadov, V. N. 1982. Helminth fauna of food Nototheniidae fi shes from Kerguelen subregion.
Ekologija Morya. Kiev, 10, 49–57 [In Russian].
Poulin, R. 2006. Global warming and temperature-mediated increases in cercarial emergence in trematode
parasites. Parasitology, 132 (1), 143–151.
Poulin, R., Mouritsen, K. N. 2006. Climate change, parasitism and the structure of intertidal ecosystems. Jour-
nal of Helminthology, 80 (2), 183–191.
Reid, W. D. K., Clarke, S., Collins, M. A., Belchier, M. 2007. Distribution and ecology of Chaenocephalus aceratus
(Channichthyidae) around South Georgia and Shag Rocks (Southern Ocean). Polar Biology, 30 (12), 1523–1533.
Rocka, A. 1999. Biometrical variability and occurrence of Ascarophis nototheniae (Nematoda, Cystidicolidae), a
parasitic nematode of Antarctic and subantarctic fi shes. Acta Parasitologica, 44 (4), 188–192.
Rocka, A. 2003. Cestodes of the Antarctic Fishes. Polish Polar Research, 24 (4), 261–276.
Rocka, A. 2004. Nematodes of the Antarctic fi shes. Polish Polar Research, 25 (2), 135–152.
Rocka, A. 2006. Helminths of Antarctic fi shes: Life cycle biology, specifi city and geographical distribution. Acta
Parasitologica, 51 (1), 26–35.
Rocka, A. 2017. Cestodes and Nematodes of Antarctic Fishes and Birds. In: Klimpel, S., Kuhn, T., Mehlhorn,
H., eds. Biodiversity and Evolution of Parasitic Life in the Southern Ocean. Parasitology Research Mono-
graphs, vol. 9. Springer, Cham, 77–107.
Rocka, A., Zdzitowiecki, K. 1998. Cestodes in Fishes of the Weddell Sea. Acta Parasitologica, 43 (1), 64–70.
Rokicki, J., Rodjuk, G., Zdzitowiecki, K. 2009. Larval ascaridoid nematodes (Anisakidae) in fi sh from the South
Shetland Islands (Southern Ocean). Polish Polar Research, 30 (1), 49–58.
264 T. A. Kuzmina, I. V. Dykyy, O. O. Salganskij, O. I. Lisitsyna, E. M. Korol, Yu. I. Kuzmin
Siegel, V. 1980. Quantitative investigations on parasites of Antarctic Channichthyid and Nototheniid fi shes.
Meeresforschung, 28, 146–256.
Sokolov, S. G., Gordeev, I. I. 2016. Paralepidapedon variabile sp. n. (Trematoda, Lepocreadioidea, Lepidapedidae) and
other representatives of the genus Paralepidapedon from Antarctic fi sh. Biology Bulletin, 43 (7), 612–618.
Sokolov, S. G., Gordeev, I. I., Atopkin, D. M. 2016. Redescription of trematode Gonocerca muraenolepisi Pa-
rukhin et Lyadov 1979 (Hemiuroidea, Derogenidae), a body cavity parasite of Antarctic fi shes, with a
discussion of its phylogenetic position. Invertebrate Zoology, 13 (2), 191–202.
Sokolov, S. G., Lebedeva, D. I., Gordeev, I. I., Khasanov, F. K. 2019. Zdzitowieckitrema incognita gen. et sp. nov.
(Trematoda, Xiphidiata) from the Antarctic fi sh Muraenolepis marmorata Günther, 1880 (Gadiformes:
Muraenolepidae): ordinary morphology but unclear family affi liation. Marine Biodiversity, 49, 451–462.
Swan, D. C. 1936. Berlese’s Fluid: Remarks upon its Preparation and use as a Mounting Medium. Bulletin of
Entomological Research, 27 (03), 389–391.
Utevsky, А. 2007. Antarctic Piscicolid Leeches. Bonner Zoologische Monographien, 54, 1–80.
Veselskyy, M. V., Khoetskyy, P. B. 2018. Ichthyofauna of the waters of the archipelago of the Argentine Islands
(Ukrainian Antarctic expedition 2015–2016). Naukovi Zapysky Ternopilskogo Natsionalnogo Pedagigich-
nogo Universytety. Seria Biologia, 1 (72), 36–43.
Weber, E. P. 3rd, Govett, P. 2009. Parasitology and necropsy of fi sh. Compendium on Continuing Education for
the Practising Veterinarian, 31 (2). E12.
Wojciechowska, A. 1993. Th e tetraphyllidean and tetrabothriid cercoids from Antarctic bony fi shes. I. Mor-
phology. Identifi cation with adult forms. Acta Parasitologica, 38 (1), 15–22.
Zdzitowiecki, K. 1979. Digenetic trematodes in alimentary tracts of fi shes of south Georgia and South Shetland
Islands (Antarctica). Acta Ichthyologica et Piscatoria, 9 (1), 15–30.
Zdzitowiecki, K. 1983. Antarctic acanthocephalans of the genus Metacanthocephalus. Acta Parasitologica
Polonica, 28 (4), 417–437.
Zdzitowiecki, K. 1984 a. Some Antarctic acanthocephalans of the genus Corynosoma parasitizing Pinnipedia,
with descriptions of three new species. Acta Parasitologica Polonica, 29 (4), 359–377.
Zdzitowiecki, K. 1984 b. Redescription of Corynosoma hamanni (Linstow, 1892) and description of
C. pseudohamanni sp. n. (Acanthocephala) from the environs of the South Shetlands (Antarctic). Acta
Parasitologica Polonica, 29 (4), 379–393.
Zdzitowiecki, K. 1986. Acanthocephala of the Antarctic. Polish Polar Research, 7 (1–2), 97–117.
Zdzitowiecki, K. 1987. Acanthocephalans of marine fi shes in the regions of South Georgia and South Orkneys
(Antarctic). Acta Parasitologica Polonica, 31 (4), 211–217.
Zdzitowiecki, K. 1991. Occurrence of digeneans in open sea fi shes off the South Shetland Islands and South
Georgia, and a list of fi sh digeneans in the Antarctic. Polish Polar Research, 12 (1), 55–72.
Zdzitowiecki, K. 1996. Acanthocephala in fi sh in the Weddell Sea (Antarctica). Acta Parasitologica, 41 (3),
199–203.
Zdzitowiecki, K. 2001. Occurrence of endoparasitic worms in fi sh, Parachaenichthys charcoti (Bathydraconidae),
off the South Shetland Islands (Antarctica). Acta Parasitologica, 46 (1), 18–23.
Zdzitowiecki, K. 2002. Occurrence of Digenea in fi shes of the family Nototheniidae in the Weddell Sea. Acta
Parasitologica, 47 (3), 154–158.
Zdzitowiecki, K. 2003. Occurrence of Digenea in fi shes other than Notothenioidei in the Weddell Sea and the
whole Antarctica. Acta Parasitologica, 48 (3), 195–199.
Zdzitowiecki, K., Cielecka, D. 1997 a. Digenea of fi shes of the Weddell Sea. II. Th e Genus Macvicaria
(Opecoelidae). Acta Parasitologica, 42 (2), 77–83.
Zdzitowiecki, K., Cielecka, D. 1997 b. Digenea of fi shes of the Weddell Sea. III. Th e Lepocreadiidae (genera
Neolepidapedon and Lepidapedon), parasites of Notothenioidea. Acta Parasitologica, 42 (2), 84–91.
Zdzitowiecki, K. 1998. Diversity of Digenea, parasites of fi shes in various areas of the Antarctic. In: Di Prisco,
G., Pisano, E., Clarke, A., eds. Fishes of Antarctica. Springer, Milano, 87–94.
Zdzitowiecki, K., Laskowski, Z. 2004. Helminths of an Antarctic fi sh, Notothenia coriiceps, from the
Vernadsky Station (Western Antarctica) in comparison with Admiralty Bay (South Shetland Islands).
Helminthologia, 41 (4), 201–207.
Zdzitowiecki, K., Ozouf-Costaz, C. 2013. Contribution to the knowledge of the parasitic fauna of fi sh off
Adelie Land, Antarctica. Polish Polar Research, 34 (4), 429–435.
Zdzitowiecki, K., White, M. G. 1992. Digenean Trematoda infection of inshore fi sh at South Georgia. Antarctic
Science, 4 (1), 51–55.
Zdzitowiecki, K., White, M. G. 1996. Acanthocephalan infection of insore fi shes at the South Orkney Islands.
Antarctic Science, 8 (3), 273–276.
Zdzitowiecki, K., Zadrozny, T. 1999. Endoparasitic worms of Harpagifer antarcticus Nybelin, 1947 of the South
Shetland Islands (Antarctic). Acta Parasitologica, 44, 125–130.
Received 16 February 2021
Accepted 5 May 2021
|
| id | oai:ojs.akademperiodyka.org.ua:article-181 |
| institution | Zoodiversity |
| issn | 2707-7268 |
| keywords_txt_mv | |
| language | English |
| last_indexed | 2026-08-21T01:01:08Z |
| publishDate | 2021 |
| publisher | Publishing House "Akademperiodyka" of the National Academy of Sciences of Ukraine |
| record_format | ojs |
| resource_txt_mv | ojsakademperiodykaorgua/c6/aac4e5ea179e05e14f49a84ccc1a38c6.pdf |
| spelling | oai:ojs.akademperiodyka.org.ua:article-1812026-08-20T12:37:23Z Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik Vernadsky”, Argentine Islands, West Antarctica Kuzmina, T. Dykyy, I. V. Salganskij, O. O. Lisitsyna, O. I. Korol, E. M. Kuzmin, Yu. I. Helminths, Acanthocephala, Nematoda, Cestoda, Trematoda, teleost fishes, Antarctica Monitoring studies of the species diversity in marine ecosystems provide important data on ecological changes caused by global warming and anthropogenic influence. The present work was aimed to analyze the species diversity of the helminths parasitic in teleost fishes inhabiting the area near the Ukrainian Antarctic Station "Akademik Vernadsky" (Galindez Island, Argentine Islands, West Antarctica). During April – January of 2014–2015 and 2019–2020, 156 specimens of six fish species (Notothenia coriiceps, N. rossii, Chaenocephalus aceratus, Parachaenichthys charcoti, Trematomus bernacchii, and Harpagifer antarcticus) were examined. Totally, 21,166 specimens of 31 helminth species were collected and assigned to five taxonomic groups: Monogenea (1 species), Digenea (10), Nematoda (5), Cestoda (4), and Acanthocephala (11). Twenty-six helminth species were found in N. coriiceps,14 in N. rossii, 27 in P. charcoti, 23 in Ch. aceratus, 16 in T. bernacchii, and six in H. antarcticus. Larval stages of anisakid nematodes prevailed in helminth community of Ch. aceratus (66%) and P. charcoti (40%), while other fish species were mostly infected with acanthocephalans, trematodes and cestodes. The present data on the species diversity of helminth communities can be used as a baseline for long-term monitoring studies of fish parasites in the region of Argentine Islands. Publishing House "Akademperiodyka" of the National Academy of Sciences of Ukraine 2021-05-04 Article Article application/pdf https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/181 10.15407/zoo2021.03.251 Zoodiversity; Vol. 55 No. 3 (2021): Zoodiversity; 251–264 Zoodiversity (Vestnik Zoologii); Том 55 № 3 (2021): Zoodiversity; 251–264 2707-7268 2707-725X 10.15407/zoo2021.03 en https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/181/98 Copyright (c) 2021 Zoodiversity |
| spellingShingle | Kuzmina, T. Dykyy, I. V. Salganskij, O. O. Lisitsyna, O. I. Korol, E. M. Kuzmin, Yu. I. Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik Vernadsky”, Argentine Islands, West Antarctica |
| title | Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik Vernadsky”, Argentine Islands, West Antarctica |
| title_full | Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik Vernadsky”, Argentine Islands, West Antarctica |
| title_fullStr | Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik Vernadsky”, Argentine Islands, West Antarctica |
| title_full_unstemmed | Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik Vernadsky”, Argentine Islands, West Antarctica |
| title_short | Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik Vernadsky”, Argentine Islands, West Antarctica |
| title_sort | helminth diversity in teleost fishes from the area of the ukrainian antarctic station “akademik vernadsky”, argentine islands, west antarctica |
| topic_facet | Helminths Acanthocephala Nematoda Cestoda Trematoda teleost fishes Antarctica |
| url | https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/181 |
| work_keys_str_mv | AT kuzminat helminthdiversityinteleostfishesfromtheareaoftheukrainianantarcticstationakademikvernadskyargentineislandswestantarctica AT dykyyiv helminthdiversityinteleostfishesfromtheareaoftheukrainianantarcticstationakademikvernadskyargentineislandswestantarctica AT salganskijoo helminthdiversityinteleostfishesfromtheareaoftheukrainianantarcticstationakademikvernadskyargentineislandswestantarctica AT lisitsynaoi helminthdiversityinteleostfishesfromtheareaoftheukrainianantarcticstationakademikvernadskyargentineislandswestantarctica AT korolem helminthdiversityinteleostfishesfromtheareaoftheukrainianantarcticstationakademikvernadskyargentineislandswestantarctica AT kuzminyui helminthdiversityinteleostfishesfromtheareaoftheukrainianantarcticstationakademikvernadskyargentineislandswestantarctica |