Differences between the European carp (Cyprinus carpio carpio) and the coloured carp (Cyprinus carpio haematopterus) in susceptibility to Thelohanellus nikolskii (Myxosporea) infection


Molnár, K.

Acta Veterinaria Hungarica 50(1): 51-57

2002


Thelohanellus nikolskii infection of the common carp (Cyprinus carpio L.) has been a common parasitosis in the Central European fish farms since the first detection of the parasite about 20 years ago. This parasite, introduced from the Far East, causes intensive infection on the fins of fingerlings of the carp subspecies cultured in Europe (European carp, Cyprinus carpio carpio). This infection of the common carp occurs in the Hungarian fish farms every year. Until the present study, this parasite had not been recorded from the fins of koi or coloured carp (Cyprinus carpio haematopterus), a carp of Far Eastern origin, which is cultured in Hungary as an ornamental fish. A recent survey conducted in common carp, koi and goldfish stocks demonstrated that T. nikolskii infection of low prevalence and intensity occurs also in koi populations, but its prevalence and intensity are markedly lower than in common carp kept in the same ponds. It is suggested that the observed differences are due to disparities in the susceptibility of the two carp subspecies to T. nikolskii, and that the koi is less susceptible to this infection. Other signs of susceptibility can also be observed in the European subspecies, since in 15% of the fish plasmodium development was arrested at an early stage. Thelohanellus nikolskii infection could not be demonstrated on goldfish (Carassius auratus).

Acta
Veterinaria
Hungarica
50
(1),
pp.
51-57
(2002)
DIFFERENCES
BETWEEN
THE
EUROPEAN
CARP
(Cyprinus
carpio
carpio)
AND
THE
COLOURED
CARP
(Cyprinus
carpio
haematopterus)
IN
SUSCEPTIBILITY
TO
Thelohanellus
nikolskii
(MYXOSPOREA)
INFECTION
K.
MOLNAR
*
Veterinary
Medical
Research
Institute,
Hungarian
Academy
of
Sciences,
H-1581
Budapest,
P.O.
Box
18,
Hungary
(Received
November
15,
2001;
accepted
December
13,
2001)
Thelohanellus
nikolskii
infection
of
the
common
carp
(Cyprinus
carpio
L.)
has
been
a
common
parasitosis
in
the
Central
European
fish
farms
since
the
first
detection
of
the
parasite
about
20
years
ago.
This
parasite,
introduced
from
the
Far
East,
causes
intensive
infection
on
the
fins
of
fingerlings
of
the
carp
subspe-
cies
cultured
in
Europe
(European
carp,
Cyprinus
carpio
carpio).
This
infection
of
the
common
carp
occurs
in
the
Hungarian
fish
farms
every
year.
Until
the
pres-
ent
study,
this
parasite
had
not
been
recorded
from
the
fins
of
koi
or
coloured
carp
(Cyprinus
carpio
haematopterus),
a
carp
of
Far
Eastern
origin,
which
is
cultured
in
Hungary
as
an
ornamental
fish.
A
recent
survey
conducted
in
common
carp,
koi
and
goldfish
stocks
demonstrated
that
T.
nikolskii
infection
of
low
prevalence
and
intensity
occurs
also
in
koi
populations,
but
its
prevalence
and
intensity
are
markedly
lower
than
in
common
carp
kept
in
the
same
ponds.
It
is
suggested
that
the
observed
differences
are
due
to
disparities
in
the
susceptibility
of
the
two
carp
subspecies
to
T.
nikolskii,
and
that
the
koi
is
less
susceptible
to
this
infection.
Other
signs
of
susceptibility
can
also
be
observed
in
the
European
subspecies,
since
in
15%
of
the
fish
plasmodium
development
was
arrested
at
an
early
stage.
Thelohanellus
nikolskii
infection
could
not
be
demonstrated
on
goldfish
(Caras-
sius
auratus).
Key
words:
Common
carp,
koi,
goldfish,
Thelohanellus
nikolskii,
suscep-
tibility
Thelohanellus
infection
of
the
European
carp
(Cyprinus
carpio
carpio)
was
first
reported
in
Hungary
by
Jeney
(1979),
who
identified
the
plasmodia
found
on
the
fins
of
carp
fingerlings
and
the
spores
located
within
the
plasmodia
with
the
species
Thelohanellus
dogieli
Akhmerov.
However,
Molnar
and
Kovacs-Gayer
(1981-1982)
held
that
the
above
parasite
belonged
to
the
species
Thelohanellus
nikolskii
Akhmerov
and,
besides
this
typical
fin
parasite,
detected
the
occurrence
of
a
connective
tissue
parasite,
T.
hovorkai
Akhmerov
in
the
same
*
E-mail:
kalman@vmri.hu;
Fax:
+36
(1)
252-1069
0236-6290/2002/$
5.00
©
2002
Akadennai
Kiad6,
Budapest
52
MOLNAR
fish
species.
They
suggested that
the
two
parasite
species
had
probably
been
brought
into
Hungary
with
the
Amur
wild
carp
introduced
into
Europe,
and
they
soon
caused
very
intensive
infection
in
the
Hungarian
carp
stocks.
The
pathology
of
the
infection
caused
by
the
parasite
and
its
location
associated
with
the
carti-
laginous
tissue
of
the
finrays
were
studied
histologically
by
Molnar
(1982)
and
electron
microscopically
by
Desser
et
al.
(1983).
Since
the
first
report
of
Jeney
(1979),
Thelohanellus
infection,
and
particularly
T.
nikolskii
infection
well
visi-
ble
even
with
the
unaided
eye,
has
been
a
permanent
and
important
parasitosis
of
cultured
common
carp
fingerlings
in
Hungary,
and
it
rates
as
one
of
the
com-
monest
carp diseases
also
in
the
neighbouring
countries
(eirkovie,
1986;
Dykova
and
Lom,
1988).
Moshu
and
Molnar
(1997)
have
pointed
out
that
the
occurrence
of
T.
nikolskii
infection
is
not
restricted
to
fingerlings,
as
in
Moldova
it
is
quite
often
detected
in
older
wild
carp
populations
living
in
natural
waters.
However,
in
the
latter
the
plasmodia
of
the
parasite
develop
at
the
tip
of
the
scales,
in
the
cartilage
of
collagenic
origin
which
is
composed
of
the
same
substance
as
the
finrays,
rather
than
in
the
cartilaginous
substance
of
the
finrays.
The
above
authors
supposed
that
older
fish
infected
in
this
way
are
responsible
for
the
in-
fection
of
fingerlings,
which
occurs
regularly
each
year.
Regarding
the
source
of
infection,
Szekely
et
al.
(1998)
conducted
investigations
and
found
the
auran-
tiactinomyxon
stages
of
T.
nikolskii
and
T.
hovorkai,
responsible
for
causing
in-
fection
in
fish,
in
common
Tubifex
and
Branchiura
worms
in
fish
farms.
This
paper
reports
the
results
of
a
survey
which
revealed
substantial
dif-
ferences
between
common
carp
and
koi
specimens
of
the
same
age
and
reared
in
the
same
pond
with
respect
to
the
prevalence
and
intensity
of
T.
nikolskii
infec-
tion.
Materials
and
methods
Since
the
first
occurrence
of
T.
nikolskii
in
Hungary
in
1979,
during
routine
examinations
of
other
purpose
(pathological
observations,
life-cycle
experiments,
molecular
biological
studies)
the
author
collected
unpublished
data on
T.
nikolskii
infection
of
several
hundred
carp
fingerlings
every
year.
Most
of
these
studies
were
conducted
in
the
Warm-water
Fish
Farm
of
Szazhalombatta,
where
finger-
lings
are
produced,
and
the
fingerlings
of
common
carp
(Cyprinus
carpio
carpio),
coloured
carp
(koi,
Cyprinus
carpio
haematopterus)
and
goldfish
(Carassius
auratus
L.)
are
reared
in
the
ponds.
The
survey
reported
in
this
paper
was
con-
ducted
in
2001
in
fish
ponds
of
the
farm
populated
with
the
above
three
species.
Two
types
of
studies
were
performed.
In
the
first
type
of
investigations,
the
characteristics
of
infection
of
carp
fingerlings
with
Thelohanellus
plasmodia
were
studied
on
100
fish
specimens
collected
from
an
intensively
infected
pond
of
the
farm.
The
occurrence
of
plasmodia
on
the
fins,
the
intensity
of
infection,
and
the
stage
of
development
of
the
individual
plasmodia
were
determined.
Acta
Veterinaria
Hungarica
50,
2002
DIFFERENT
SUSCEPTIBILITY
OF
CARP
SUBSPECIES
TO
Thelohanellus
nikolskii
53
In
the
second
survey,
100
specimens
each
of
7-week-old
and
9-week-old
fingerlings
of
carp,
koi
and
goldfish
stocks
(a
total
of
600
specimens)
were
ex-
amined
for
7'.
nikolskii
infection.
In
that
study,
carp
and
koi
fingerlings
were
collected
from
a
pond
with
a
mixed
population,
while
goldfish
specimens
from
several
small
ponds
located
next
to
the
former.
Most
of
the
examinations
were
performed
under
stereomicroscope,
on
live
fish
narcotised
with
MS-222
solution,
but
on
20
fish
specimens
of
each
category
postmortem
examinations
were
also
carried
out.
In
the
latter
case,
the
fish
were
killed,
then
their
fins
were
cut
off
and
examined
at
10-fold
magnification
under
stereomicroscope.
Some
of
the
infected
fins
were
fixed
in
Bouin's
solution
for
histology,
embedded
in
paraffin
wax,
cut
to
5
gm
thin
sections
and
stained
with
haema-
toxylin
and
eosin.
Results
According
to
the
results
of
the
present
author's
surveys
spanning
several
years,
Thelohanellus
infection
of
the
fins
occurs
regularly,
every
year,
with
al-
most
100%
prevalence
on
6-
to
9-week-old
carp
in
different
fish
farms
of
Hun-
gary,
including
the
warm-water
fish
farm.
In
some
cases
the
intensity
of
this
in-
fection
was
very
high,
and
the
development
of
30-50
plasmodia
per
fish
could
be
considered
typical.
It
was
striking
that
during
the
regular
veterinary
inspections
by
external
examination
no
Thelohanellus
plasmodia
could
be
detected
on
the
koi
fingerlings
kept
in
the
same
ponds.
In
the
first
survey,
plasmodia
containing
spores
of
mostly
the
same
devel-
opmental
stage,
or
emptied
plasmodia,
occurred
on
the
finrays,
primarily
on
the
tail
fins,
of
75
common
carp
specimens.
The
number
of
these
plasmodia
varied
between
8
and
35
(average:
27)
per
fish
(Fig.
1).
In
the
finrays
of
the
same
fish
bright
areas
of
cartilage
deformation
were
seen,
which
could
be
regarded
as
traces
of
abortive
development.
In
histological
sections
this
abortive
develop-
ment
was
indicated
by
small
nodules
containing
broken
pieces
of
the
fin
cartilage
(Fig.
2).
Fifteen
fish
exhibited
only
areas
of
cartilage
deformation
indicative
of
arrested
development,
while
ten
fish
proved
to
be
free
of
infection.
Carp
that
showed
only
cartilage
deformation
considered
to
represent
arrested
parasite
de-
velopment
were
examined
repeatedly
after
keeping
them
in
aquaria
for
one
month;
however,
they
did
not
show
signs
of
plasmodium
development.
In
the
second
survey,
an
examination
involving
200
carp
and
200
koi
fin-
gerlings
(Table
1)
showed
that
by
more
thorough,
primarily
stereomicroscopic,
inspection
Thelohanellus
plasmodia
can
be
found
also
on
the
fins
of
koi
finger-
lings;
however,
such
plasmodia
can
be
collected
from
much
fewer
fish,
the
inten-
sity
of
infection
is
far
lower
than
in
carp
fingerlings,
and
the
plasmodia
are
of
smaller
size.
While
out
of
one
hundred
7-week-old
and
9-week-old
carp
73
and
84
specimens,
respectively,
proved
to
be
infected
and
the
mean
intensity
of
in-
Acta
Veterinaria
Hungarica
50,
2002
54
MOLNAR
fection
reached
22-24
plasmodia
per
fish,
in
koi
the
prevalence
of
infection
was
only
18-20%
and
none
of
the
fish
had
more
than
3
plasmodia.
Thelohanellus
in-
fection
did
not
occur
on
the
200
goldfish
specimens
collected
from
the
neigh-
bouring
ponds
of
the
farm;
however,
it
was
interesting
to
note
that
in
the
goldfish
a
Myxobolus
infection
could
be
observed
in
the
same
finray
location.
1
Fig.
1.
Tail
end
of
a
common
carp
fingerling
with
Thelohanellus
nikolskii
plasmodia
in
the
carti-
laginous
finrays.
Magnification
x
1.5
5.
-
m"
Fig.
2.
Developing
plasmodium
(p)
and
an
abortive
nodule
of
Thelohanellus
nikolskii
in
the
fin
of
a
common
carp
fry.
Broken
pieces
of
the
cartilage
(arrows)
indicate
the
abortive
development.
Histological
section.
Haematoxylin
and
eosin
(H.-E.),
x
60
Acta
Veterinaria
Hungarica
50,
2002
DIFFERENT
SUSCEPTIBILITY
OF
CARP
SUBSPECIES
TO
Thelohanellus
nikolskii
55
Table
1
Infection
of
the
fins
of
carp
and
koi
fingerlings
with
Thelohanellus
nikolskii
plasmodia
No.
of
fish
Prevalence
(%)
Intensity
(plasmodia/fish)
Carp
(7
weeks
old)
100
73
1-35
(22)
Koi
(7
weeks
old)
100
20
1-3
(1.3)
Carp
(9
weeks
old)
100
84
8-30
(24)
Koi
(9
weeks
old)
100
18
1-3
(1.4)
Discussion
Today
Thelohanellus
infection
introduced
from
the
Far
East
can
be
consid-
ered
a
common
parasitosis
in
Europe.
The
fact
that
the
detection
of
this
infection
has
been
limited
to
Central
Europe
can
primarily
be
explained
by
the
lesser
im-
portance
of
carp
in
Western
Europe;
however,
the
infection
has
been
documented
to
occur
also
in
other
European
countries
where
carp
breeding
is
conducted.
While
the
disease
caused
by
the
parasite
is
sometimes
alarming,
infection
is
rarely
diag-
nosed
because
it
takes
place
in
a
period
of
fry
rearing
when
there
is
no
fishing
off
Infection
passes
off
relatively
quickly,
and
the
fms
undergo
rapid
regeneration.
The
prevalence
and
high
intensity
of
carp
thelohanellosis
caused
by
T.
nikolskii
in
Hungary
were
first
reported
by
Molnar
(1982)
and
by
Molnar
and
Kovacs-Gayer
(1981-1982).
The
present
survey
reveals
that
this
high
prevalence
and
intensity
of
infection
have
not
changed
in
the
20
years
that
have
elapsed
since
that
first
report.
At
the
same
time,
it
is
remarkable
that,
besides
the
devel-
oping
or
spore-containing
mature
plasmodia,
not
infrequently
plasmodia
of
ar-
rested
development
can
also
be
found
on
the
infected
fins.
These
latter
plasmodia
have
already
produced
the
cartilage
deformation
described
by
Molnar
(1982),
but
their
development
was
arrested
at
an
early
stage.
Some
of
the
examined
carp
fin-
gerlings
showed
such
infection
manifested
in
clinical
signs
but not
resulting
in
spore
formation,
indicating
that
in
some
fish
the
parasite
failed
to
reach
the
stage
of
sporogenesis
despite
the
actual
presence
of
infection.
Carp
collected
from
a
given
pond
showed
the
same
stage
of
infection
and,
disregarding
cases
of
infec-
tion
resulting
in
mild
cartilage
deformation,
on
fish
of
the
same
age
plasmodia
of
identical developmental
stage
could
only
be
found.
The
aquarium
experiment
performed
in
this
study
disproved
the
hypothesis
that
cartilage
deformations
would
correspond
to
a
delayed
development
or
a
secondary
infection;
namely,
the
abortive
forms
did
not
start
to
develop
even
after
prolonged
keeping
in
aquaria.
Until
the
present
study,
Hungarian
specialists
had
commonly
held
the
view
that
the
koi
was
completely resistant
to
7'.
nikolskii,
and
that
apart
from
its
original
host,
the
Amur
wild
carp,
T.
nikolskii
caused
infection
in
the
European
carp
only.
That
view
was
supported
by
the
lack
of
reliable
data
on
this
parasite
Acta
Veterinaria
Hungarica
50,
2002
56
MOLNAR
from
Japan
and
China,
while
the
species
T.
hovorkai,
which
is
much
more
diffi-
cult
to
diagnose,
had
been
studied
thoroughly
in
both
countries
(Yokoyama
et
al.,
1998;
Chen
and
Ma,
1998).
In
the
light
of
the
present
studies
the
supposed
ab-
solute
resistance
of
the
koi
to
Thelohanellus
infection
requires
revision;
however,
it
can
be
proved
beyond
doubt
that
the
Asian
carp
subspecies
is
much
less
sus-
ceptible
to
infection
than
the
European
variant.
Obviously,
T.
nikolskii
recorded
from
the
river
Amur
has
much
wider
distribution
in
Asia,
but
it
is
difficult
to
di-
agnose
this
infection
because
of
its
low
prevalence
and
intensity.
The
species
de-
scribed
in
Japan
by
Hoshina
and
Hosoda
(1957)
under
the
name
of
Thelohanellus
cyprini
presumably
corresponds
to
T.
nikolskii,
and
it
is
not
impossible
that
one
of
the
11
Thelohanellus
species
described
from
carp
in
China
is
synonymous
with
T.
nikolskii
(Chen
and
Ma,
1998).
The
lower
prevalence
of
infection
in
Asia,
and
the
low
susceptibility
of
Far
Eastern
carp
subspecies
to
this
parasite
typically
adapted
to
the
species
Cyprinus
carpio
are
supported
by
the
fact
that
the
koi,
the
coloured
carp
introduced
from
Asia,
develops
an
infection
of
lower
prevalence
and
intensity
even
in
the
Hungarian
fish
ponds,
while
the
European
carp,
which
had
been
free
from
this
parasite
before
the
1970s,
shows
highly
prevalent
infection.
The
studies
revealed
signs
of
a
developing
resistance
also
in
the
European
carp;
namely,
one-fifth
of
the
fish
proved
to
be
infection
free,
and
even
the
infected
fish
included
specimens
exhibiting
signs
of
an
abortive
infec-
tion.
The
cartilaginous
thickenings
of
the
fm,
which
is
indicative
of
abortive
de-
velopment,
were
observed
already
by
Molnar
(1982)
who,
however,
regarded
these
changes
as
signs
of
a
passed-off
infection.
The
present
studies,
which
included
long-term
controlled
laboratory
experiments,
undoubtedly
prove
that
the
changes
indicating
disruption
of
the
fmrays
are
the
result
of
an
abortive
development.
The
high
host
specificity
of
Thelohanellus
species
and
the
special
affinity
of
individual
species
to
different
organs
have
already
been
pointed
out
by
Akhmerov
(1955).
The
results
of
this
study
confirm
Akhmerov's
statement
con-
cerning
host
specificity.
On
the
basis
of
the
studies
on
goldfish,
and
according
to
the
findings
of
a
survey
conducted
by
Szekely
and
Molnar
(1996-1997)
on
gibel
carp
(Carassius
auratus
gibelio
Bloch)
in
the
Kis-Balaton
water
reservoir
it
seems
to
be
likely
that
Thelohanellus
species
cannot
colonise
even
the
members
of
the
genus
Carassius,
which
is
most
closely
related
to
the
common
carp.
Acknowledgements
The
author
thanks
Dr.
Csaba
Szekely
for
his
help
in
collecting
fish
and
preparing
digitised
photos,
and
Dr.
Pin
Nie,
Vice
Director
of
the
Institute
of
Hydrobiology,
Wuhan,
China
for
information
on
the
Chinese
special
literature.
The
study
was
rendered
possible
by
a
grant
of
the
Hungarian
Scientific
Research
Fund
(project
no.
T
029200)
and
by
the
programme
entitled
'The
quality
development
of
the
biological
and
technological
bases
of
the
Hungarian
fishing
sector',
4/039/2001.
Acta
Veterinaria
Hungarica
50,
2002
DIFFERENT
SUSCEPTIBILITY
OF
CARP
SUBSPECIES
TO
Thelohanellus
nikolskii
57
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