Seediscussions,stats,andauthorprofilesforthispublicationat:http://www.researchgate.net/publication/269759152

NAUČNIRAD–OriginalPaperSKINECTOPARASITESOFFISHFROMTHELOWERFLOWOFTHESAVARIVEREKTOPARAZITINAKOŽIRIBAIZDONJEGTOKARIJEKESAVE

ARTICLE·JANUARY2014

DOWNLOADS

84

VIEWS

205

3AUTHORS,INCLUDING:

ZlatkoNedićUniversityofTuzla

13PUBLICATIONS2CITATIONS

SEEPROFILE

SanelRiđanovićUniversityDzemalBijedicMostar

17PUBLICATIONS0CITATIONS

SEEPROFILE

Availablefrom:ZlatkoNedićRetrievedon:10July2015

Nedić Z. i sar.: Skin ectoprasites of fish from the lower flow of the Sava river

Veterinaria 63 (1-4), 45-53, Sarajevo 2014. 45

NAUČNI RAD – Original Paper

SKIN ECTOPARASITES OF FISH FROM THE LOWER FLOW OF THE

SAVA RIVER

EKTOPARAZITI NA KOŽI RIBA IZ DONJEG TOKA RIJEKE SAVE

Nedić Z., Skenderović I., Riđanović S.1

Sažetak – Istraživanje kožnih ektoparazita riba donjeg toka rijeke Save pokazalo

je ekstremno visok stupanj biodiverziteta kožnih ekotparazitskih protozoa. Tokom

perioda istraživanja uzorkovali smo 120 riječnih riba. Determinirali smo 15 vrsta pri

čemu je većina njih klasificirana u porodicu Cyprinidae. Ostale su klasificirane u

porodice: Percidae, Siluridae, Ameiuridae, Esocidae i Gobiidae. Ukupno, 49 individua je

pokazalo prisustvo različitih vrsta kožnih ektoparazita iz carstva protozoa. Determinacija

protozoa bila je utvrđena do nivoa vrste za tri parazitske protozoe (Ichthyobodo necator,

Chilodonella cyprini i Ichthyophthirius multifiliis), dok je za dvije utvrđena do nivoa roda

(Trichodina i Apiosoma).

Ključne riječi: rijeka Sava, Općina Orašje, kožne ektoparazitske protozoe

Abstract – Research on the skin ectoparasites of fish from the lower flow of the

Sava River showed an extremely high level of biodiversity of the skin ectoparasitic

protozoa. During the study period, we sampled 120 freshwater fish. We deteremined 15

fish species and most of them were classified in the family Cyprinidae. The others were

classified in the fish families: Percidae, Siluridae, Ameiuridae, Esocidae and Gobiidae.

In total, 49 individuals showed the presence of different types of the skin ectoparasites

from the protozoa kingdom. Determination of the protozoa was done to the species level

for three parasitic protozoa (Ichthyobodonecator, Chilodonellacyprini and

Ichthyophthiriusmultifiliis), and for two of them to the genus level (Trichodina and

Apiosoma).

Zlatko Nedić, magistar primjenjene biologije, (zlatko8679@hotmail.com), Srednja

strukovna škola Orašje; Isat Skenderović, docent, Prirodno-matematički fakultet,Univerzitet u

Tuzli; Sanel Riđanović; docent,Nastavnički fakultet, Univerzitet Džemal Bijedić, Mostar

Zlatko Nedić, Master of Applied Biology, (zlatko8679@hotmail.com), Secondary

vocational school of Orašje; Isat Skenderović, PhD, Assistant Professor, Faculty of Science,

University of Tuzla; Sanel Riđanović; PhD, Assistant Professor, Faculty of Education, University

of Džemal Bijedić, Mostar

Nedić Z. i sar.: Skin ectoprasites of fish from the lower flow of the Sava river

46

Key words: Sava River, Orašje Municipality, protozoa skin ectoparasites

Introduction

The Sava River is the largest river which makes the border between Croatia and

Bosnia and Herzegovina (3). In biological sense, that fact speaks of the importance of

research of such ecosystem. The study of the skin ectoparasitic protozoa of fish in the

Sava River ecosystem can contribute to a better understanding of biotic environmental

factors that occur as a product of joint relations between ectoparasitic protozoa and fish

specimens in this watercourse. Protozoa represent a very heterogeneous group of

invertebrates where a lot of them build complex ecological relationships (parasitism,

commensalism, etc.) (18). Determination of the number of skin ectoparasitic protozoa

which parasitize on fish may prove their biological diversity, and therefore, the

heterogeneity of the lower flow of the Sava River in terms of ichthyofauna, parasitofauna

and parasites that are more or less specific to the certain types of fish. By doing this, we

can determine the health status of the fish individuals of the Sava River in the area

because some of the ectoparasitic protozoa produce certain metabolic products

(appearance of mucus on the skin, minor wounds, hematoma, etc.) that can be harmful to

the health of fish (4). The main objective of our research is to determine which type of

ectoparasitic protozoa exists on the fish skin and the intensity of infection. Our

hypothesis is that in lower flow of the Sava River several species of ectoparasitic

protozoa, which are indicators of polluted water, exist.

Material and methods

For the research purposes, ectoparasitic protozoa sampling was conducted at

four locations near Orašje town (Fig. 1). We sampled 120 fish individuals and determined

15 fish species: Abramis brama L., Cyprinus carpio, Silurus glanis L., Leuciscus

cephalus L., Ictalurus nebulosus Le Sueur, Sander lucioperca L., Carassius gibelio Fl.,

Esox lucius L., Ctenopharyngodon idella Val., Neogobius fluviatilis L., Scardinius

erythrophthalmus L., Alburnus alburnus L., Vimba Vimba L., Aspius aspius L. and Perca

fluviatilis L. In research we measured temperature and water level as the basic physical

parameters of the river water, which are also important for the survival of ectoparasitic

protozoa (4). Temperature was measured by the mercury thermometer, and the height of

water level data were used from the Water Management Enterprise Central Posavina. We

also used Olympus microscope and native preparations.

Sampling was carried out in the summer and autumn period, and fish was caught

in cooperation with the local fishermen. After systematic determination of the fish

species by the identification key for freshwater fish species (20), all sampled individuals

were examined and parasitologically searched for the presence of skin ectoparasitic

Nedić Z. i sar.: Skin ectoprasites of fish from the lower flow of the Sava river

Veterinaria 63 (1-4), 45-53, Sarajevo 2014. 47

protozoa. For parasitological examinations we made native preparations of the samples

taken from the skin. Native preparations were microscopically analyzed using an

electrical microscope (Olympus) under magnification 10x and 40x, and ectoparasitic

protozoa were determined (4). Statistical analysis was performed using a non-parametric

statistical tests (chi-square test) in the computer program Statistica 7TM

.

Figure 1. Sampling locations on the lower flow of the Sava River near Orašje town. Figure shows

northern Bosnia and Herzegovina bordering on the Republic of Croatia. This area has continental

climate. L1, L2, L3 and L4 indicate sampling locations from west to east

Slika 1. Lokacije uzorkovanja na donjem toku rijeke Save u blizini grada Orašja. Slika prikazuje

sjevernu Bosnu i Hercegovinu koja graniči sa Republikom Hrvatskom. Ovo je područje

kontinentalne klime. L1, L2, L3 i L4 označavaju lokacije uzorkovanja od zapada prema istoku

Results

Study of the skin ectoparasites of fish from the lower flow of the Sava River was

conducted at four locations, where we sampled 120 fish individuals, approximately 30

individuals per location. By measuring the fundamental physical parameters of the Sava

River, we determined the average water temperature of 25 °C in summer, and 19 °C in

autumn.

The contribution of individual fish species to the total sample in the study area is

presented in Table 1. It is clear that most of the examined species (65 individuals or

54.16%) belong to the family Cyprinidae (bream, carp, chub, crucian carp, grass carp,

roach, bleak, asp and vimba bream). The smaller contribution is by the fish species

belonging to the families Gobiidae (goby, 30%), Percidae (perch and pike-perch, 5.83%),

Esocidae (pike, 5%), Siluridae (catfish, 2.5%) and Ameiuridae (American catfish, 2.5%).

Nedić Z. i sar.: Skin ectoprasites of fish from the lower flow of the Sava river

48

It is important to emphasize the lack of available data on the ichthyofauna of the lower

flow of the Sava River.

Table 1. Biodiversity of the total fish sample

Tabela 1. Biodiverzitet ukupnog ihtiouzorka

Fish species No of fish Percentage

Abramis brama 5 4,16

Alburnus alburnus 26 21,66

Aspius aspius 2 1,66

Carassius gibelio 14 11,66

Ctenopharyngodon idella 1 0,83

Cyprinus carpio 7 5,83

Esox lucius 6 5,00

Ictalurus nebulosus 3 2,50

Neogobius fluviatilis 36 30,00

Perca fluviatilis 5 4,16

Sander lucioperca 2 1,66

Scardinius erythrophtalmus 5 4,16

Silurus glanis 3 2,50

Squalius cephalus 4 3,33

Vimba vimba 1 0,83

Total sample 120 100

Graph 1. Percentage of infected and non-infected fish

Grafikon 1. Postotak inficiranih i neinficiranih riba

Microscopic analysis of the native fish skin preparations for the presence of

ectoparasites discovered three species of protozoa: Ichthyobodo necator, Chilodonella

cyprini and Ichthyophthirius multifiliis. We determined two genera of the skin

ectoparasitic protozoa, Trichodina and Apiosoma (Table 2). The number of infected and

non-infected fish individuals is statistically significant (p<0,05) (Graph 1).

40%

60%

Percentage of infected and non-infected fish

Infected fish Non infected fish

Nedić Z. i sar.: Skin ectoprasites of fish from the lower flow of the Sava river

Veterinaria 63 (1-4), 45-53, Sarajevo 2014. 49

Table 2. Representation of ectoparasitic protozoa species of analyzed fish species from the Sava

River(+ positive for parasite; – negative for parasite)

Tabela 2. Predstavljanje ektoparazitskih protozoa analiziranih ribljih vrsta rijeke Save (+ pozitivno

na parazita; - negativno na parazita)

Discussion

The temperature values and water level in summer were extremely favorable for

the development of skin ectoparasitic protozoa, while the autumn temperatures were less

favorable for their development (19, 4).

Rueckert et al. (16) found the presence of four types of the protozoa on the skin

bream. The most dominant species were from the genus Trichodina and the other species

from the genus Chilodonella and Ichthyophtirius. Our results showed that the bream

species were infested with species from the genus Chilodonella, Trichodina, Apiosoma

and Ichthyophthirius multifiliis.

Parasite

Fish species

Ich

thyo

bo

do

nec

ato

r

Ch

ilo

do

nel

la c

ypri

ni

Tri

cho

din

a s

p.

Ich

thyo

ph

thir

ius

mu

ltif

ilii

s

Ap

ioso

ma

sp

.

Abramis brama - + + + +

Cyprinus carpio + + + - +

Silurus glanis + - - - -

Squalius cephalus - + + - -

Ictalurus nebulosus + + + + +

Sander lucioperca + + + - -

Carassius gibelio - + + - +

Esox lucius - - - - -

Ctenopharyngodon idella + - + + -

Neogobius fluviatilis - - - + -

Scardinius erythrophthalmus + + + - +

Alburnus alburnus + + + - +

Vimba vimba - - - - -

Aspius aspius - + + - -

Perca fluviatilis - + - - -

Nedić Z. i sar.: Skin ectoprasites of fish from the lower flow of the Sava river

50

Nikolić and Simonović (10) found the presence of Trichodina nobilis in carp as

well as Özer and Erden (13) who, in addition to species of the genus Trichodina, found

species of the genus Apiosoma and Epistylis.

Skenderović (17) found a kind Ichthyobodo necator as ectoparasites of the carp

skin. Individual carps we analyzed were contaminated with species Ichthyobodo necator,

Chilodonella cyprini, Trichodina sp. and Apiosoma sp. By comparing our results with the

results of the aforementioned research, it is possible to observe a large compliance. Nash

et al. (9) found two ectoparasitic protozoa on the skin of catfish, Trichodina sp. and

Trichodinella sp. while in our study, none of the aforementioned ectoparasites are found.

Instead, we found Ichthyobodo necator and, therefore, we can say that our results are not

consistent with the results of the aforementioned authors.

Kurtović et al. (6) found the presence of two types of ectoparasitic protozoa on

chub from the Sava River: Ichthyophthirius multifiliis and Trichodina sp. In our research,

on chub we found genus Trichodina, while Ichthyophthirius multifiliis was not found.

Fish species Ictalurus nebulosus was contaminated with all established types of the skin

ectoparasitic protozoa. There are no available studies on the European rivers that can

confirm our results.

Robliecki (15) found on a sample of 2398 species of fish belonging to the family

Percida that these specimens were infested with a small number of ectoparasitic

protozoa. These results are consistent with our results because we found three

ectoparasitic protozoa on the skin of Sander lucioperca, and one ectoparasitic species on

Perca fluviatilis.

Basson et al. (2) found that the most common types of ectoparasites on the skin

of Carassius gibelio were Trichodina species. We found Trichodina sp., Chilodonella

and Apiosoma sp.

Abdel-Meguid (1) in his study of Ctenopharyngodon idella population proved a

large number of ectoparasitic protozoa on the skin of these species: Oodinium sp.,

Trichodina piscicum, Chilodonella hexasticha, Tetrahymena, Ichthyophthirius

Ichthyophthirius multifiliis, Glossatella sp., Epystilis sp. and Trichodina acuta. Our

sample had only one species of Ctenopharyngodon idella on which we found kinds

Ichthyobodo necator, Trichodina sp. and Ichthyophthirius multifiliis. Type Neogobius

fluviatilis was the largest in total sample, but we found that several individuals were

infested with Ichthyophthirius multifiliis.

Our study confirms the findings of Molnar (8) who also found this species on the

goby skin to be very frequent ectoparasites. Type Scardinius erythrophthalmus was

extremely susceptible to parasites as well as species Alburnus alburnus. On the skin of

these two species Ichthyophthirius multifiliis was not discovered, while all other species

were.

Skenderović (17) found species Chilodonella and Trichodina on the skin of

species Scardinius erythrophthalmus, and on the skin of Alburnus alburus he found

species from genus Apiosoma. Species of asp were infested with Chilodonella cyprini

Nedić Z. i sar.: Skin ectoprasites of fish from the lower flow of the Sava river

Veterinaria 63 (1-4), 45-53, Sarajevo 2014. 51

and Trichodina species, and we did not find any available data that could confirm our

results.

We found that the intensity of infestation was dependent on the sampling period,

tending to decline from summer to autumn around the year (Graph 2). One of the reasons

contributing to decrease of the parasites in the autumn period is the temperature, which is

not favorable for the maintenance of the normal life cycle of the parasites (19). Statistical

analysis showed that the intensity of infestation was statistically different throughout the

study period (p<0.05), one of the reasons being very favorable temperature in the summer

period.

Graph 2. Infestation intensity throught sampling period

Grafikon 2. Intenitet infestiranosti tokom perioda uzorkovanja

Conclusion

This preliminary study of the lower flow of the Sava River in the length of 15

km discovered 15 fish species from six families. Most species belong to the family

Cyprinidae, while the most abundant species in the sample was goby.

Parasitological examination for the presence of the ectoparasites skin protozoa

showed that the infestation was found in more than 40% of the fish examined. On this

occasion, we identified several species of ectoparasitic protozoa: Ichthyobodo necator,

Chilodonella cyprini, Ichthyophtirius multifiliis, Trichodina sp. i Apiosoma sp.

Based on discovered parasites as ecological indicators, we can conclude that the

water of the lower flow of the Sava River is polluted.

0

10

20

30

40

50

60

July August Semptember OctoberPerc

en

tag

e o

f in

fecte

d f

ish

Sampling period

Nedić Z. i sar.: Skin ectoprasites of fish from the lower flow of the Sava river

52

REFERENCES:

1. Abdel-Meguid M. Ectoparasite fauna of grass carp Ctenopharyngodon idella in Delta

breeding station, Egypt. Veterinary Medical Journal Giza 1995; 43 (1): 53-63.

2. Basson L, Van As J G, Paperna I. Trichodinid ectoparasites of cichlid and cyprinid

fishes in South Africa and Israel. Systematic Parasitology 1983; 5 (4): 245-257.

3. Đordić M. Bosanska Posavina. Zavičajni priručnik za osnovne i srednje škole,

Zagreb, 1999.

4. Fijan N. Zaštita zdravlja riba. Poljoprivredni fakultet Sveučilišta u Osijeku, Osijek,

2006.

5. Habeković D, Safner R, Aničić I, Treer T. Ihtiofauna dijela rijeke Save. Ribarstvo

1997; 55 (3): 99-110.

6. Kurtović B, Vardić I, Valić D, Kapetanović D, Teskeredžić Z, Teskeredžić E.

Zdravstveno stanje klena (Squalius cephalus) u odnosu na kvalitetu vode rijeke Save.

Ribarstvo 2009 67 (2): 63-75.

7. Mikavica D, Sofradžija A. Possibility of construction of a Salmonidae fish farm in the

hydrigraphic area of eastern Bosnia. Croatian Journal of Fisheries 1988; 43 (2): 33-37.

8. Molnar K. Some remarks on parasitic infections of the invasive Neogobius spp.

(Pisces) in the Hungarian reaches of the Danube River, with a description of

Goussiaszekelyi sp. (Apicomplexa: Eimeriidae). Journal of Applied Ichthyology 2006;

22 (5): 395-400.

9. Nash G, Nash M, Schlotfeldt H. J. Systemic amoebiasis in cultured European catfish,

Silurus glanis L. Journal of Fish Diseases 1988; 11 (1): 57-71.

10. Nikolić V, Simonović P. Seasonal dinamics of carp infestation by Trichodina nobilis

Chen. 1963 (Peritricha, Ciliata) in two fish-ponds in Banat. Tiscia 1998, 31 (5): 59-61.

11. Nikolić V, Simonović P, Marić S. Occurrence of Chilodonella hexasticha (Ciliophora,

Protista) on farmed rainbow trout (Onchorhyncusmykiss) throughout the season. Acta

Veterinaria (Belgrade) 2006; 56: 55 – 61.

12. Özer A. The relationship between occurrence of ectoparasites, temperature and

culture conditions: a comparison of farmed and wild common carp (Cyprinus carpio

L., 1758) in the Sinop region of northern Turkey. Journal of Natural History 2003; 33

(4): 483-491.

13. Özer A, Erden O. Ectoparasitic protozoa fauna of the common carp (Cyprinus

carpio L., 1758) caught in the Sinop region of Turkey. Journal of Natural History

1998; 32: 441-454.

14. Piria M, Šprem N, Jakovlić I, Tomljanović T, Matulić D, Treer T, Aničić I, Safner R.

First record of round goby, Neogobius melanostomus in the Sava River, Croatia.

Aquatic Invasions 2011; 6 (1): 153-157.

Nedić Z. i sar.: Skin ectoprasites of fish from the lower flow of the Sava river

Veterinaria 63 (1-4), 45-53, Sarajevo 2014. 53

15. Robliecki L. Diversity of the parasite fauna of cyprinid (Cyprinidae) and percid

(Percidae) fishes in the Vistula Lagoon, Poland. Wiadomosci Parazytologiczne 2003;

49 (2): 125-164.

16. Rueckert S, Klimpel S, Palm H. W. Parasite fauna of bream Abramis brama and roach

Rutilus rutilus from a man-made waterway and a freshwater habitati in northern

Germany. Diseases of aquatic organisms 2007; 74 (3): 225-233.

17. Skenderović I. Biodiverzitet parazitskih beskičmenjaka riba iz hidroakumulacije

Modrac. Doctoral dissertation. University of Sarajevo, Veterinary Faculty, 2010.

18. Stanković S. Ekologija životinja. Zavod za izdavanje udžbenika, Beograd, 1961.

19. Tomec M, Hacmanjek Z, Teskeredžić Z, Teskeredžić E, Čož-Rakovec R. Kvaliteta

vode i ektoparazitske bolesti ciprinidnih riba. Ribarstvo 1995; 53 (4): 129-139.

20. Vuković T. Slatkovodne ribe Bosne i Hercegovine. Zavod za izdavanje udžbenika,

Sarajevo, 1973.

21. Zrnčić S, Orajić D, Šoštarić B, Ćaleta M, Bulj I, Zanella D, Šurmanović D.

Occurrence of parasites in Cobitidae from Croatian rivers draining into two different

watersheds. Journal of Applied Ichthyology 2009; 25 (4): 447-450

Uredništvo primilo rukopis 03. 01. 2014. godine