The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae)
Morphophysiological and Biochemical ParametersComplex influence of infection by myxosporeans Myxidium gadi Georgevitsch, 1916; Ceratomyxa merlangi Zaika, 1966 and nematode Hysterothylacium aduncum (Rudolphi, 1802) on the morphophysiological and biochemical parameters of the Black sea whiting Merlang...
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irk-123456789-1097922016-12-15T03:02:12Z The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae) Skuratovskaya, E.N. Yurakhno, V.M. Zavyalov, A.V. Экология Morphophysiological and Biochemical ParametersComplex influence of infection by myxosporeans Myxidium gadi Georgevitsch, 1916; Ceratomyxa merlangi Zaika, 1966 and nematode Hysterothylacium aduncum (Rudolphi, 1802) on the morphophysiological and biochemical parameters of the Black sea whiting Merlangius merlangus euxinus (Nordmann, 1840) were studied. Significant decrease of spleenosomatic index and increase of hepatosomatic index in fish with average and high intensity of infection were found. The dependence of hepatic antioxidant enzyme activities on intensity of infection was observed. Increase of superoxidismutase, catalase, glutation-S-transferase activities in fish with average and high intensity of infection and decrease of peroxidase activity in specimens with average intensity of infection were shown. Исследовали комплексное влияние инвазии миксоспоридиями Myxidium gadi Georgevitsch, 1916; Ceratomyxa merlangi Zaika, 1966 и нематодой Hysterothylacium aduncum (Rudolphi, 1802) на морфофизиологические и биохимические показатели черноморского мерланга, Merlangius merlangus euxinus (Nordmann, 1840). Обнаружено снижение индекса селезёнки и увеличение индекса печени у рыб со средней и максимальной степенью заражённости. Выявлена зависимость активности антиоксидантных ферментов печени от интенсивности инвазии рыб. Показано снижение активности супероксиддисмутазы, каталазы, глутатион-Sтрансферазы у рыб со средним и высоким уровнем заражённости, повышение активности пероксидазы у особей со средней интенсивностью инвазии. 2013 Article The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae) / E.N. Skuratovskaya, V.M. Yurakhno, A.V. Zavyalov // Вестник зоологии. — 2013. — Т. 47, № 4. — С. 309–317. — Бібліогр.: 25 назв. — англ. 0084-5604 DOI 10.2478/vzoo-2013-0032 http://dspace.nbuv.gov.ua/handle/123456789/109792 597.555.5:576.8:591.1:577.1(262.5) en Вестник зоологии Інститут зоології ім. І.І. Шмальгаузена НАН України |
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Экология Экология Skuratovskaya, E.N. Yurakhno, V.M. Zavyalov, A.V. The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae) Вестник зоологии |
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Morphophysiological and Biochemical ParametersComplex influence of infection by myxosporeans Myxidium gadi Georgevitsch, 1916; Ceratomyxa merlangi Zaika, 1966 and nematode Hysterothylacium aduncum (Rudolphi, 1802) on the morphophysiological and biochemical parameters of the Black sea whiting Merlangius merlangus euxinus (Nordmann, 1840) were studied. Significant decrease of spleenosomatic index and increase of hepatosomatic index in fish with average and high intensity of infection were found. The dependence of hepatic antioxidant enzyme activities on intensity of infection was observed. Increase of superoxidismutase, catalase, glutation-S-transferase activities in fish with average and high intensity of infection and decrease of peroxidase activity in specimens with average intensity of infection were shown. |
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Article |
| author |
Skuratovskaya, E.N. Yurakhno, V.M. Zavyalov, A.V. |
| author_facet |
Skuratovskaya, E.N. Yurakhno, V.M. Zavyalov, A.V. |
| author_sort |
Skuratovskaya, E.N. |
| title |
The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae) |
| title_short |
The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae) |
| title_full |
The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae) |
| title_fullStr |
The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae) |
| title_full_unstemmed |
The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae) |
| title_sort |
influence of parasitic infection on the black sea whiting, merlangius merlangus euxinus (gadidae) |
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Інститут зоології ім. І.І. Шмальгаузена НАН України |
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2013 |
| topic_facet |
Экология |
| url |
http://dspace.nbuv.gov.ua/handle/123456789/109792 |
| citation_txt |
The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae) / E.N. Skuratovskaya, V.M. Yurakhno, A.V. Zavyalov // Вестник зоологии. — 2013. — Т. 47, № 4. — С. 309–317. — Бібліогр.: 25 назв. — англ. |
| series |
Вестник зоологии |
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597.555.5:576.8:591.1:577.1(262.5)
THE INFLUENCE OF PARASITIC INFECTION ON THE BLACK
SEA WHITING MERLANGIUS MERLANGUS EUXINUS (GADIDAE)
MORPHOPHYSIOLOGICAL AND BIOCHEMICAL PARAMETERS
E. N. Skuratovskaya, V. M. Yurakhno, A. V. Zavyalov
A. O. Kovalevsky Institute of Biology of the Southern Seas of NAS of Ukraine,
Nakhimov av., 2, Sevastopol, 99011 Ukraine
E-mail: skuratovskaya2007@rambler.ru; viola_taurica@mail.ru; andrej-zavyalov@yandex.ua
The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus (Gadidae),
Morphophysiological and Biochemical Parameters. Skuratovskaya E. N., Yurakhno V. M., Zavya -
lov A. V. – Complex influence of infection by myxosporeans Myxidium gadi Georgevitsch, 1916;
Ceratomyxa merlangi Zaika, 1966 and nematode Hysterothylacium aduncum (Rudolphi, 1802) on the
morphophysiological and biochemical parameters of the Black sea whiting Merlangius merlangus euxi-
nus (Nordmann, 1840) were studied. Significant decrease of spleenosomatic index and increase of hep-
atosomatic index in fish with average and high intensity of infection were found. The dependence of
hepatic antioxidant enzyme activities on intensity of infection was observed. Increase of superoxidismu-
tase, catalase, glutation-S-transferase activities in fish with average and high intensity of infection and
decrease of peroxidase activity in specimens with average intensity of infection were shown.
Key wo r d s: intensity, morphophysiological parameters, antioxidant system, fish.
Âëèÿíèå ïàðàçèòàðíîé èíâàçèè íà ìîðôîôèçèîëîãè÷åñêèå è áèîõèìè÷åñêèå ïàðàìåòðû ÷åðíîìîð-
ñêîãî ìåðëàíгà, Merlangius merlangus euxinus (Gadidae). Ñêóðàòîâñêàÿ Å. Í., Þðàõíî Â. Ì.,
Çàâüÿëîâ À. Â. –Èññëåäîâàëè êîìïëåêñíîå âëèÿíèå èíâàçèè ìèêñîñïîðèäèÿìè Myxidium gadi
Georgevitsch, 1916; Ceratomyxa merlangi Zaika, 1966 è íåìàòîäîé Hysterothylacium aduncum
(Rudolphi, 1802) íà ìîðôîôèçèîëîãè÷åñêèå è áèîõèìè÷åñêèå ïîêàçàòåëè ÷åðíîìîðñêîãî ìåð-
ëàíãà, Merlangius merlangus euxinus (Nordmann, 1840). Îáíàðóæåíî ñíèæåíèå èíäåêñà ñåëåç¸íêè
è óâåëè÷åíèå èíäåêñà ïå÷åíè ó ðûá ñî ñðåäíåé è ìàêñèìàëüíîé ñòåïåíüþ çàðàæ¸ííîñòè.
Âûÿâëåíà çàâèñèìîñòü àêòèâíîñòè àíòèîêñèäàíòíûõ ôåðìåíòîâ ïå÷åíè îò èíòåíñèâíîñòè
èíâàçèè ðûá. Ïîêàçàíî ñíèæåíèå àêòèâíîñòè ñóïåðîêñèääèñìóòàçû, êàòàëàçû, ãëóòàòèîí-S-
òðàíñôåðàçû ó ðûá ñî ñðåäíèì è âûñîêèì óðîâíåì çàðàæ¸ííîñòè, ïîâûøåíèå àêòèâíîñòè
ïåðîêñèäàçû ó îñîáåé ñî ñðåäíåé èíòåíñèâíîñòüþ èíâàçèè.
Êëþ÷åâûå ñ ëîâ à: èíòåíñèâíîñòü èíâàçèè, ìîðôîôèçèîëîãè÷åñêèå ïîêàçàòåëè, àíòèîêñè-
äàíòíàÿ ñèñòåìà, ðûáû.
Introduction
The investigation of consequences of fish infection by parasites is one of the actual problems. Infection
considerably worsens fish condition and weakens protective functions. Changes taking place in contaminat-
ed organism are connected with disturbances in metabolic processes, physiological state and development of
the adaptive response reactions. Host adaptations to parasite are provided by protective systems, which activ-
ity is directed to lowering the negative influence and destruction of toxic metabolites. These are immune and
antioxidant systems (Skuratovskaya, Zavyalov, 2008; Dautremepuits et al., 2003; Mertinez-Alvares et al.,
2005; Sitja-Bobadilla et al., 2008).
Studies of parasites influence on fish organisms seems to be necessary for understanding the mechanisms
of host response reactions, directed on maintenance of functioning of infected organs and the whole organism.
This is especially important for fisheries and aquaculture, because infection can be the reason of mass fish death
and lowers fish production (Rudneva et al., 2010; Dautremepuits et al., 2003; Mertinez-Alvares et al., 2005).
In most cases parasites in the host organism are represented by several species, attributed often to dif-
ferent systematic groups, which must be taken into consideration during the investigations. Myxosporeans and
parasitic nematodes, often living together in the host organism take a special place among the parasites, some-
times reaching high intensity in commercial fish species. Myxosporeans are primitive multi-cell micropara-
site organisms located in different organs and tissues mostly of the Osteichthyes, but as well of
Vestnik zoologii, 47(4): 309—317, 2013
DOI 10.2478/vzoo-2013-0032
Ýêîëîãèÿ
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Chondrichthyes, marine and fresh water fish; sometimes they are found in amphibians, reptiles, birds and
mammals (Dudin, 2010; Lom, Dykova, 2006). It is known that myxosporean in fish muscles can consider-
ably deteriorate fish meat quality in results of post-mortem lysis of muscle tissue (milky fish condition or
myoliquefaction) or macroscopic cysts forming, giving the resemblance of “wormy” meat. When Myxosporea
locate in tissues and different inner organs of fish they can cause quite different diseases, leading even to mass
mortality of their hosts.
Parasitic nematodes are distributed widely and met in vertebrate as well as in invertebrate animals.
Separate species are the parasites with high ecological plasticity and wide specificity. They locate as a rule in
fish stomach, pyloric appendices, intestine, and in body cavity and muscles tissue. Great number of parasitic
nematodes leads to development of serious pathologies, considerably decreasing fish mass and other symp-
toms of the fish health deterioration. That is why studies of complex influence of myxosporeans and nema-
todes on the hosts organism is of great interest.
The Black sea whiting Merlangius merlangus euxinus (Nordmann, 1840) is one of numerous hosts for
myxosporeans and nematodes. The Black sea whiting is a representative of cods, playing an important role
in feeding of predatory fish, dolphins, as well as in transfer of parasites through the food chains. Whiting is
of fishery importance. Near the shores of Crimea according to the data of fishery inspection the catches of
M. merlangus euxinus make only a tenth part of a percent if compared with other ichthyofauna species.
However, in Turkey, where representatives of this species are of greater size and its taste is traditionally esti-
mated, whiting is a favorite object of fishery and its price exceeds that of salmon and many other fish species
grown in mariculture.
In a whole whiting catches in the Black Sea at the end of 1960s – beginning of 1970-ties made 2.1 %
(Ivanov, Beverton, 1985), in 1988 – 4.5 % (Prodanov et al., 1997). During those years M. merlangus euxi-
nus was among four the most caught fish along with anchovy, sprat and horse-mackerel. From the end of
1980s four-fold decrease in the volume of the fish caught was observed in the Black Sea, which caused great
losses in economics of all the Black Sea riparian countries. The reasons of this were disturbance of water
exchange between the Azov, Black and Marmara seas as a result of decrease and over —regulation of rivers
runoffs, complex pollution and eutrophication of waters, decrease in foodbase for fish-planktophages due to
mass development of alien ctenophore Mnemiopsis leidyi, eating fish eggs and larvae, over-catches of fish due
to insufficient regulation of intensive fishery, long-term climatic changes (Eremeev, Zuev, 2005).
Two most common species of myxosporeans inhabit the Black sea whiting gall bladder: Myxidium gadi
Georgevitsch, 1916 and Ceratomyxa merlangi Zaika, 1966; they often are met in mixed infection. It has been
stated earlier that high intensity of infection with the parasite M. gadi led to morphological and functional
changes of the damaged host organ, described as myxidiosis of the Black sea whiting (Yurakhno, 2009). It is
demonstrated by the change of strongly infected bladders color from transparent green to white, yellowish or
brown – non-transparent, growing of their size, thickening of walls and dying of numerous cells of their
epithelium, replacement of bile by the parasite spores and plasmodia. Histological studies revealed the fact
that thickness of the subepithelial tissue of gall bladders of whiting strongly infected with M. gadi was
4–12 times larger than that of uninfected (0.021–0.056 mm contrary to 0.00175–0.014 mm, correspondingly).
The thickness of epithelial tissue of strongly infected bladders was 2—3 times larger than that in uninfected
(0.084–0.126 contrary to 0.028–0.056 mm correspondingly).
Thickening of the walls is accompanied with dying of numerous cells of bladder epithelium. Using the
biochemical methods it has been stated that whiting myxidiosis causes total lipids decrease in liver 2–3 times
and triacylglycerols 3–4 times exclusively in males during their spawning and fatting. In strongly infected
females such differences were not revealed; any changes in liver and muscles lipid composition in strongly
and weakly infected fish were not found as well (Shchepkina, Yurakhno, 2008). The recent studies showed
that in some cases mass development of C. merlangi in whiting bladder also can lead to the painful condi-
tions.
Nematode Hysterothylacium aduncum (Rudolphi, 1802) is another common parasite of the Black sea
whiting. It is localized in the intestine, body cavity and sometimes in gall bladder. We have stated earlier,
that H. aduncum can influence significantly on the antioxidant system of sprat muscle tissue (Skuratovskaya,
Zavyalov, 2006) and it’s blood (Skuratovskaya, Zavyalov, 2008).
After the analysis of all available information on negative influence of the above-mentioned parasites
on the host fish organism it will be interesting to study complex influence of complex infection by myxospore-
ans M. gadi, C. merlangi and nematode H. aduncum on morphophysiological parameters and antioxidant
enzyme activities of the Black sea whiting liver.
Material and methods
Fish were collected in the Streletskaya Bay (Sevastopol), in winter period of 2009. Freshly caught non-
living fish was brought to the laboratory in the morning. Females prevailed in a catch, therefore only females
were studied. The biological analysis, including measuring of total (13.1 ± 0.9) and standard (11.75 ± 0.1)
length (cm), determination of fish weight (15.99 ± 0.34), fish weight without internals (12.31 ± 0.23), liver
(0.524 ± 0.03) and spleen (0.013 ± 0.001) weight (g), state of maturation (IV—V) and age (2—3 years) of
fish, was made.
310 E. N. Skuratovskaya, V. M. Yurakhno, A. V. Zavyalov
Unauthenticated
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Parasitological analysis was performed by method of I. E. Bihovskaya-Pavlovskaya (1985) – by partial
parasitological dissection of fish for revealing of myxosporeans in the gall-bladder and nematodes in the intes-
tine, body cavity, stomach and in gall-bladder.
The specimens were subdivided in three groups, depending on intensity of infection. The first (I) group
included free of Myxosporea and weakly infected (with low intensity) fish, with few or tens of myxosporean
spores and plasmodia in the gall bladder smears and up to two nematodes in the body cavity, intestine and
stomach. The second (II) group included specimens with average intensity of infection, with hundreds of
myxosporean spores and plasmodia in the gall-bladder smears and up to 3—9 nematodes in the body cavity,
intestine and stomach. The third (III) group included highly infected fish with thousands of Myxosporea
spores and (or) great number of plasmodia in the gall bladder smears and 10—12 nematodes in the body cav-
ity, intestine and stomach (table1).
The morphophysiological parameters – spleenosomatic index (SI), hepatosomatic index (HI) and fat-
ness index (FatI) were calculated using the following formulas:
Sl = Ps/ Pf*100 (%),
HI = Pl/ Pf*1000 (‰),
FatI = Pf/ L3
st*100 (%),
where Pf – fish weight without internals (g), Pl – liver weight (g), Ps – spleen weight (g), Lst – stan-
dard length (cm).
Activities of five antioxidant enzymes: superoxidismutase, catalase, peroxidase, glutationreductase and
glutation-S-transferase were determined in fish liver according to the methods described previously, with
some modifications (Rudneva, 1999).
Superoxide dismutase (SOD, EC 1.15.1.1) was assayed spectrophotometrically on the basis of inhibi-
tion of the reduction of nitroblue tetrasolium with NADH mediated by phenazine methosulfate under basic
conditions.
Catalase (CAT, EC 1.11.1.6) was measured by the method involving the reaction of hydroperoxide
reduction.
Peroxidase (PER, EC 1.11.1.7) activity was detected by spectrophotometric method using benzidine
reagent.
Glutathione reductase (GR, EC 1.6.4.2) activity was assayed spectrophotometrically by reaction of the
NADPH degradation.
Glutathione-S-transferase (GST, EC 2.5.1.18) activity was determined spectrophotometrically by the
conjugate 1-chloro-2, 4-dinitrobenzene (CDNB) using as substrate at the presence of reduced glutathione.
The enzyme activity was calculated in terms of protein concentration. Protein content in fish liver was
determined by the Lowry method.
Statistical differences were processed using Student’s t-test which was applied for pair-wise testing for
antioxidant enzymes between different groups. All numerical data are given as means (M) ± standard error
(SE) (Halafyan, 2008). The significance level was 0.05.
Results
Parasitological studies of three fish samples taken in January (15 specimens stud-
ied) and in February (41 specimens studied) 2009 in the Streletskaya Bay showed, that
in the January sample there were no myxosporean-free fish; in February their number
was 14 specimens. Prevalence of M. gadi and C. merlangi in the January sample was
50 % correspondingly; there was no mixed infestation. In February prevalence of
M. gadi was 58 %, C. merlangi – 10 %, mixed infection by both species – 10 %. In
January nematodes were found only in the intestine (prevalence 46 %). In February
helminthes were found in the intestine, stomach and body cavity with prevalence 65 %.
The analysis of morphophysiological and biochemical parameters revealed differ-
ences between specimens from different groups.
Significant decrease of spleenosomatic index and increase of hepatosomatic index
in fish with average (II group) and high (III group) intensity of infection as compared
311The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus...
Ta b l e 1. Distribution of fish by the intensity of infection
Ò à á ëèö à 1. Ðàñïðåäåëåíèå ðûá ïî ñòåïåíè çàðàæ¸ííîñòè
Group, N Myxosporeans Nematodes Number of fish, ex
I No, or few or tens of spores and plasmodia No, 1—2 16
II Hundreds of spores and plasmodia 3—9 15
III Thousands of spores and (or) great number of plasmodia 10—12 25
Unauthenticated
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with specimens from I group was found (ð ≤ 0.05). Fatness indexes of fish from three
groups were not different (fig. 1).
Variations of the hepatic antioxidant enzyme activities in fish from different groups
were observed. General tendency was determined for CAT, SOD and GST activities:
CAT and SOD activities were significantly lower in fish from the group II, GST activ-
ity – in specimens from the groups II and III as compared with the group I (ð ≤ 0.05).
For PER activity reversal tendency was observed: enzyme activity in fish with average
312 E. N. Skuratovskaya, V. M. Yurakhno, A. V. Zavyalov
Fig. 1. Morphophysiological parameters of whiting with different intensity of infection (M ± SE; nI = 16,
nII = 15, nIII = 25); * – differences are significant as compared with fish from the group I (ð ≤ 0.05).
Ðèñ. 1. Ìîðôîôèçèîëîãè÷åñêèå ïîêàçàòåëè ìåðëàíãà ñ ðàçíîé ñòåïåíüþ çàðàæ¸ííîñòè (M ± SE; nI =
16, nII = 15, nIII = 25); * – ðàçëè÷èÿ äîñòîâåðíû ïî ñðàâíåíèþ ñî çíà÷åíèÿìè ðûá èç I ãðóïïû
(ð ≤ 0,05).
S I
**
0
0,02
0,04
0,06
0,08
0,1
0,12
0,14
%
HI
**
0
10
20
30
40
50
60
‰
Fa t I
0
0 ,1
0 ,2
0 ,3
0 ,4
0 ,5
0 ,6
0 ,7
0 ,8
0 ,9
I II III
groups
%
Unauthenticated
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313The Influence of Parasitic Infection on the Black Sea Whiting, Merlangius merlangus euxinus...
Fig. 2. Antioxidant enzyme activities in whiting liver with different intensity of infection (M ± SE; nI = 16,
nII = 15, nIII = 25); * - differences are significant as compared with fish from group I; ** – as compared
with fish from group II (ð ≤ 0.05).
Ðèñ. 2. Àêòèâíîñòü àíòèîêñèäàíòíûõ ôåðìåíòîâ â ïå÷åíè ìåðëàíãà ñ ðàçíîé ñòåïåíüþ çàðàæ¸ííîñòè
(M ± SE; nI = 16, nII = 15, nIII = 25); * – ðàçëè÷èÿ äîñòîâåðíû ïî ñðàâíåíèþ ñî çíà÷åíèÿìè ðûá
èç I ãðóïïû; ** – òî æå ïî ñðàâíåíèþ ñî çíà÷åíèÿìè ðûá èç II ãðóïïû (ð ≤ 0,05).
CÀÒ
*
0
0,05
0,1
0,15
0,2
0,25
m
g
H
2O
2
p
er
m
g
p
ro
te
in
p
er
m
in
GR
0
2
4
6
8
10
12
14
16
n
m
o
l
N
A
D
P
H
p
er
m
g
p
ro
te
in
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PER
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0,1
0,2
0,3
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1
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GST
*
*
0
10
20
30
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I II III
groups
n
m
o
l
co
n
ju
ga
te
p
er
m
g
p
ro
te
in
p
er
m
in
SOD
*
0
50
100
150
ar
bi
tr
ar
y
u
n
it
s
p
er
m
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pr
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intensity of infection (group II) was three times lower than in the specimens from other
groups (ð ≤ 0.05). No significant changes in GR activity were found (fig. 2).
Discussion
Parasite uses the host as a habitat and nutrition source and adapts to its peculiari-
ties. As a result of infection pathological processes develop in fish organism, leading in
some cases to their death. Changes in the host organism can display at different levels of
biological organization, including the molecular one. Infection causes biochemical reor-
ganization of metabolism in infected tissues, directed to selective uptake of nutritional
substances and can lead to serious structural and functional changes in organs. Due to
this host response reaction develops; it is directed to support of the infected organs func-
tioning as compensation of parasites effect (Dautremepuits et al., 2003; Vasilyeva et al.,
2010). That is why the diagnostics of parasitic infection using indicators of different bio-
logical level is necessary for evaluation of the infected host condition.
The organs‘ indices reflect fish physiological status and can characterize stress.
Index parameters depend on different factors: habitat conditions, substances in environ-
ment, infective diseases (Kuzminova, 2006; Zhidenko, 2008). Our investigations have
shown that spleenosomatic index in fish with average and high degree of intensity was
lower as compared with the I group, which, possibly, is conditioned by increased
income of blood from the spleen into blood channel and functional exhaustion of this
organ as a result of inflammatory process caused by the presence of parasites and dis-
charge of their metabolites (fig. 1).
Fish spleen is immune-competent and blood producing organ, it participates in pro-
viding the mechanisms of urgent adaptation, throwing into blood current “deposited” ery-
throcytes (Davydov et al., 2006). It is known that under stress factors stocks of blood get
from the spleen into blood channel, blood exhaustion and its size reduction take place,
in heavy cases dystrophy develops (Lapirova et al., 2004). Possibly, high infection inten-
sity is one of such stress-factors causing size decrease and, consequently, the decrease of
spleen index of the host-whiting.
Various liver functions (synthesis of proteins and carbohydrates, blood production,
detoxication etc.) cause lability of mass and variations in this organ index. Liver index
is widely used in the ichthyomonitoring as a sensitive indicator for evaluation of fish con-
dition and its habitat (Kuzminova, 2006; Zhidenko, 2008). Increase of liver index in fish
with average and high infection level can testify to the organ hypertrophy due to the tis-
sue transformation and strengthening of the function of parasites metabolites detoxica-
tion, as well as due to the products of peroxidation and free-radical oxidation (fig. 1).
One of the protective systems is an antioxidant that protects the organism against
oxidative stress caused by biotic and abiotic factors. Parasites affecting the metabolism
of infected fish stimulate oxidative stress manifested by increasing free radical and per-
oxide processes modulating the host antioxidant status (Skuratovskaya, Zavyalov, 2006,
2008; Bello et al., 2000; Dautremepuits et al., 2003; Mertinez-Alvarez et al., 2005).
The literature data testify to changes of antioxidant enzyme activities in infected
fish. Character and direction of these changes depend on the species of host and par-
asite, and on the life cycle stage of parasite. As a result of infection synthesis of the
reactive oxygen forms increases in the host organism causing parasites elimination,
which can lead to the inhibition of the host antioxidant enzyme activities (Mikrjakov,
Silkina, 2006; Skuratovskaya, Zavyalov, 2006, 2008; Bello et al., 2000; Dautremepuits
et al., 2003; Mertinez-Alvarez et al., 2005).
In this study, decrease of the SOD, CAT and GST activities in the liver of fish
with average and high intensity of infection (II and III groups) can be the result of their
inhibition with reactive oxygen species of host macrophages and the high content of
314 E. N. Skuratovskaya, V. M. Yurakhno, A. V. Zavyalov
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parasites metabolites, causing oxidative stress and presenting great danger for fish
health. At the same time insignificant increase of the SOD, CAT and GST activities in
fish from the group III as compared with the group II can be the host adaptive response
directed to the organism functioning maintenance at the high intensity of infection
(fig. 2).
PER activity increase in the liver of fish from the group II at the background of
low SOD, CAT and GST activities can testify to a compensatory effect of the antiox-
idant system by unfavorable factors, which was found by us earlier (Skuratovskaya,
Rudneva, 2008). It demonstrates adaptive response, which is able to neutralize the
oxidative stress. But PER activity decrease in the liver of fish from group III testifies to
inhibition of the enzyme activity at high intensity of infection (fig. 2).
Similar results have been obtained by us earlier, when we studied muscle antioxi-
dant enzyme activities in the Black sea sprat Sprattus sprattus phalericus, depending on
intensity of infection by the nematode Hysterothylacium aduncum larvae. CAT activity
was significantly reduced in infected sprat as compared with healthy fish. The lowest
CAT activity was in specimens with high intensity of infection. PER activity decreased
with increase of infection intensity. The data obtained testified to the fact of inhibition
of the antioxidant enzyme activities with high infection by larvae of nematodes; these
data reflected suppressing effect of parasites on the host protective reactions and
appearance of toxic response (Skuratovskaya, Zavyalov, 2006).
The parasitic infections can lead to the inhibition of antioxidant enzyme activities
associated with the production of reactive oxygen species by macrophages at the infec-
tion site in order to eliminate the parasite. Such response was also noticed in fish by
Bello et al. (2000) who suggested that the freshwater fish Rhamdia quelen response to
infection by Clinostomum detruncatum could involve reactive oxygen intermediates and,
therefore, induced an oxidative stress, but without inducing significant differences in the
SOD and CAT activities between healthy and parasitized fish (Bello et al., 2000). The
other authors found that breams Abramis brama infected with plerocercoids of Ligula
intestinalis were characterized by high content of malondialdehyde and low antioxidant
activities, which is associated with an increase of under the influence of parasites and
the development of oxidative stress (Mikrjakov, Silkina, 2006).
In another study, the antioxidant enzyme activities measured in liver and head kid-
ney of Ptychobothrimum sp. – infected carp Cyprinus carpio were significantly higher as
compared to the healthy fish. This result could indicate that infection did not lead to
an oxidative stress and that it indeed is associated with an improvement of the antiox-
idant status of the parasitized fish (Dautremepuits et al., 2003).
Thus, the results of the study have shown that infection by myxosporeans Myxidium
gadi, Ceratomyxa merlangi and nematode Hysterothylacium aduncum affects the func-
tional status of the Black sea whiting, which is manifested by the change of morpho-
physiological parameters and antioxidant enzyme activities. The nature of these changes
depends on an intensity of infection.
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Received 16 April 2013
Accepted 20 May 2013
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