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See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/269138875 Ectoparasitic crustaceans are not responsible for decreasing of fish populations from the Sava River ARTICLE · DECEMBER 2014 DOWNLOADS 110 VIEWS 74 8 AUTHORS, INCLUDING: Zlatko Nedić University of Tuzla 13 PUBLICATIONS 2 CITATIONS SEE PROFILE Rifet Terzić University of Tuzla 45 PUBLICATIONS 335 CITATIONS SEE PROFILE Isat Skenderović University of Tuzla 13 PUBLICATIONS 0 CITATIONS SEE PROFILE Avdul Adrović University of Tuzla 31 PUBLICATIONS 2 CITATIONS SEE PROFILE Available from: Zlatko Nedić Retrieved on: 10 July 2015

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EctoparasiticcrustaceansarenotresponsiblefordecreasingoffishpopulationsfromtheSavaRiver

ARTICLE·DECEMBER2014

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ZlatkoNedićUniversityofTuzla

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RifetTerzićUniversityofTuzla

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IsatSkenderovićUniversityofTuzla

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Basic Research Journal of Agricultural Science and Review ISSN 2315Available online http//www.basicresearchjournals.orgCopyright ©2014 Basic Research Journal

Full Length Research Paper

Ectoparasitic crustaceansdecreasing of fish populations from the Sava River1Zlatko Nedić, 2Emir Halilović

Hadžiahmetović

1Secondary vocational school of Orašje; University of Tuzla, Faculty of

2Clinical Center Tuzla, Microbiology department3University of Tuzla, Faculty of Nature science and Mathematics

4Agency for education of Bosnia and Herzegovina; University of Mostar, Faculty of Nature science and education

Corresponding author: [email protected]

The Sava River is known as one of the most to its high variety of life forms. The present study was conducted in northern Bosnia and Herzegovina(Posavina region) during summer and autumn of 2013. crustaceans parasitize on fish fromwere collected and analyzed. Study showed that sampled fish individuals belong to six fish families: Cyprinidae, Percidae, Siluridae, Ameiuridae, Esocidaeof two ectoparasitic crustacean species: reveal possible consequences on infected fish individuals crustaceans and the decrease of fish populations. Keywords: Sava River, Bosnia and Herzegovina, ectoparasitic crustaceans, Posavina.

INTRODUCTION Bosnia and Herzegovina is very heterogeneous country regarding biodiversity and special ecological relationships which exist in hydro-ecosystems, especially in watercourses (Nedić 2013). Particularly aquatic ecosystem of the whole country is the Sava River(Figure 1 and 2) which constitutes between Bosnia and Herzegovina and Croatian Republic(Nedić et al., 2014). Also, Sava River hasother hydro-ecosystems in Bosnia and Herzegovina, especially concerning water level supply because the water level of Sava River affects water leveltributaries and other hydro-accumulationsAgency for water of Bosnia and Herzegovina, personal

Published by Basic Research Journal of Agricultural Science and Review

Basic Research Journal of Agricultural Science and Review ISSN 2315-6880 Vol. 3(12) pp. 161-166 DecAvailable online http//www.basicresearchjournals.org

crustaceans are not responsible for decreasing of fish populations from the Sava River

Emir Halilović, 3Rifet Terzić, 3Isat Skenderović, 3Avdul Adrovi

Jurida, 4Mato Živković, 5Jasmin Ferizbegovi

Orašje; University of Tuzla, Faculty of Nature science and Mathematicsbiology.

Clinical Center Tuzla, Microbiology department ity of Tuzla, Faculty of Nature science and Mathematics, department of biology

Agency for education of Bosnia and Herzegovina; University of Mostar, Faculty of Nature science and education5Veterinary station of Tuzla

Corresponding author: [email protected]

Accepted

Abstract

The Sava River is known as one of the most important hydro-ecosystem in Bosnia and Herzegovina

. The present study was conducted in northern Bosnia and Herzegovinasummer and autumn of 2013. Primary aim was to reveal which ectoparasitic

from the Sava River and for that purpose total of 120 fish individuals were collected and analyzed. Study showed that sampled fish individuals belong to six fish families: Cyprinidae, Percidae, Siluridae, Ameiuridae, Esocidae and Gobiidae. Study also showed the presence

species: Argulus foliaceus and Ergasilus sieboldi. on infected fish individuals as well as any relation between ectoparasiticof fish populations.

: Sava River, Bosnia and Herzegovina, ectoparasitic crustaceans, Posavina.

Bosnia and Herzegovina is very heterogeneous country ical relationships

, especially in ). Particularly significant

aquatic ecosystem of the whole country is the Sava River natural border

between Bosnia and Herzegovina and Croatian Republic Also, Sava River has high impact on

ecosystems in Bosnia and Herzegovina, water level supply because the

water levels of its accumulations (R. Erkapić,

and Herzegovina, personal

communication). Primary role of the Sava River

possibilities of cultivation of some freshwater fish speciwhich are necessary for fishing and(Nedić, et al., 2014). The rapid prosperity in the worlds manufacturing processeslifestyle changes in the whole world, as well as the increasing occurrence of stress caused by work habitslead to the need for increasedhealthier way of eating (Nedić et al., 20recognisable as an excellentphosphate, iron, calcium, amino acids and vitamins which all are important nutrients (Mansoor and

Agricultural Science and Review

166 December 2014

are not responsible for decreasing of fish populations from the Sava River

Avdul Adrović, 3Elvira Jasmin Ferizbegović

and Mathematics, department of

, department of biology Agency for education of Bosnia and Herzegovina; University of Mostar, Faculty of Nature science and education

in Bosnia and Herzegovina due . The present study was conducted in northern Bosnia and Herzegovina

Primary aim was to reveal which ectoparasitic Sava River and for that purpose total of 120 fish individuals

were collected and analyzed. Study showed that sampled fish individuals belong to six fish families: and Gobiidae. Study also showed the presence

sieboldi. Second aim was to as well as any relation between ectoparasitic

Sava River in agriculture lies in the possibilities of cultivation of some freshwater fish species

fishing and healthy food products , et al., 2014). The rapid development and

s manufacturing processes, n the whole world, as well as the

increasing occurrence of stress caused by work habits, increased intake of light food and

edić et al., 2014). Fish meat is excellent source of proteins, fat,

phosphate, iron, calcium, amino acids and vitamins which all are important nutrients (Mansoor and Al-Shaikh, 2011).

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Figure 1. Sampling locations on the lower reaches of the Sava River. Figure shows northern Bosnia and Herzegovina bordering with Republic of Croatia. Sampling locations are explaned on the map. Posavina canton is marked with yellow color.

Figure 2.Typical

Fish culture is an old branch of animal health condition of fish species depends othat are responsible for normal life cycle (Mansoor and Al-Shaikh, 2011).

Many organisms can have a significanthealth of fish species due to their coactions with the (fish species) and in mentioned common life they can damage fish tissue, organs and can induce mortalityThese organisms are parasites (Harisson et al., 2006; Alaş et al., 2008; Notash, 2012; Pekmezci

Fish parasites can be classified into three most important groups: parasitic protozoa, parasitic trematodes and parasitic crustaceans (Skenderović, 20102013).

Ectoparasitic crustaceans are heterogeneous group of living organisms with impressive structural anadaptations during their life cycle (Dezfuli et al., 2003). One of the most common crustacean parasitic species is Argulus foliaceus L., 1758 also known as a(Figure 3) (Pekmezci et al., 2011). This parasite species

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Sampling locations on the lower reaches of the Sava River.

Figure shows northern Bosnia and Herzegovina bordering with Republic of Croatia. Sampling locations are explaned on the map. Posavina canton is marked with yellow color.

Typical habitats at the four sampling locations

husbandry and cies depends on many factors

and fish health

significant impact on health of fish species due to their coactions with the hosts (fish species) and in mentioned common life they can damage fish tissue, organs and can induce mortality.

arisson et al., 2006; et al., 2008; Notash, 2012; Pekmezciet al., 2011).

Fish parasites can be classified into three most : parasitic protozoa, parasitic trematodes

and parasitic crustaceans (Skenderović, 2010; Nedić,

Ectoparasitic crustaceans are heterogeneous group of living organisms with impressive structural and functional

life cycle (Dezfuli et al., 2003). One of the most common crustacean parasitic species is

so known as a carp louse . This parasite species

is most often determined on gills and skin offish species, but sometimes amphibian species (Alas et al., 2010is the cause of argulosis, symptoms like lesion on the skin, decreasing of condition factor, swimming problems ect. (Pekmezci etAlaş et al., 2010).

Species Ergasilus sieboldi, Nordmann is also known as ectoparasitic species on freshwater fishes. It is possible to localize it on fish gills and skin, and its presencecauses very severe fish disease symptoms like haemorrhages and inflammation of fish skin and gills with tissue damaging (Dezfuli eEinszporn-Orecka, 1973). There is significantly small number of scientific articles that discuss ectoaprasitic crustaceans, especially in Bosnia and Herzegovina. For that reason it is very important to study the presence of two described crustacean species for scientific development and better understanding of ecological relationships in one of the

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Nedić et al. 162

is most often determined on gills and skin of fresh water fish species, but sometimes can be determined on

species (Alas et al., 2010). Mentioned species cause of argulosis, a disease with different

symptoms like lesion on the skin, decreasing of condition swimming problems ect. (Pekmezci et al., 2011;

, Nordmann is also known as species on freshwater fishes. It is possible

to localize it on fish gills and skin, and its presence severe fish disease called ergasilosis with

haemorrhages and inflammation of fish skin and gills with tissue damaging (Dezfuli et al., 2003;

There is significantly small number of scientific articles that discuss ectoaprasitic crustaceans, especially in Bosnia and Herzegovina. For that reason it is very important to study the presence of two described

acean species for scientific development and better understanding of ecological relationships in one of the

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163. Basic Res. J. Agric.Sci. Rev.

Figure 3of Cyprinus carpio

largest watercourses in the country. For that purpose we established our hypothesis that species foliaceus and Ergasilus sieboldi are most often ectoparasitic crustaceans on fishes from Sava River and based on that fact, first aim of present study them on fish skin and gills and describe pathological changes that are induced by two mentioned parasitic species. After that, this study will reveal if the ectoparasitic crustaceans are causing the decrease of fish populations in the Sava River. MATERIALS AND METHOD For research on ectoparasitic crustaceans, sampling was conducted at four locations near Orašje town between Bosanski Šamac from the west and Brčside (Figure 1). Total longitudinal length of searched locations was approximately 40 km. The samples were taken near three villages: Domaljevac, Tolisa and DonjaMahala, and one city area, Orašje (marked as L1, L2, L3and L4).

We randomly sampled 120 fish individualswas carried out in the summer and autumn2013, and we caught fish in cooperationfishers.

After systematic determination by identification key fordetermining freshwater fish species (Vukovisampled individuals were examined and searchedpresence of ectoparasitic crustaceans. First step was toanaesthetize fish individuals using chemical substance marked as MS 222. For parasitological examinationsmade native preparations of samples takenand gills. Native preparations were analysed using an electrical microscope (Olympus) magnification 10x, 20x and 40x. After that analysis,determined ectoparasitic crustaceans health condition of fish species and possibilities of tissue damage caused by the presence of ectoparasitic crustacean species.

After that analysis, calculation of infestation prevalencewas done. Prevalence of infestation by ectoparasitic

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Figure 3.Argulus foliaceus taken from the skin

Cyprinus carpio under magnification 40x.

largest watercourses in the country. For that purpose we established our hypothesis that species Argulus

are most often ectoparasitic crustaceans on fishes from Sava River and based on that fact, first aim of present study is to localize them on fish skin and gills and describe pathological changes that are induced by two mentioned parasitic species. After that, this study will reveal if the ectoparasitic crustaceans are causing the decrease of

For research on ectoparasitic crustaceans, sampling was conducted at four locations near Orašje town between Bosanski Šamac from the west and Brčko to the east

1). Total longitudinal length of searched locations was approximately 40 km. The samples were taken near three villages: Domaljevac, Tolisa and Donja Mahala, and one city area, Orašje (marked as L1, L2, L3

sampled 120 fish individuals. Sampling summer and autumn period of fish in cooperation with local

determination by identification key for Vuković, 1973), all

searched for the First step was to

chemical substance parasitological examinations we

samples taken from the skin microscopically

Olympus) under ter that analysis, we

and assessed possibilities of tissue

presence of ectoparasitic

of infestation prevalence of infestation by ectoparasitic

crustacean is measured by the1982): Prevalence (%) =

������������

������������������

Statistical analysis was performedstatistical test (chi-square test) Statistica 7TM. RESULTS Studies of ectoparastic crustaceans of the Sava Riverwere conducted at four locations, where we sampled 120 fish individuals, approximately 30 indivlocation (Table 1). It has determined six fish families and 15 fish species.

Totally, Cyprinidae is the largestidentified species, precisely: Linnaeus, 1758), carp (Cyprinuschub (Squalius cephalus, Linnaeus(Carassius gibelio, Bloch, 1782), (Ctenopharyngodon idella, Valencienesroach (Scardinius erythrophthalmusbleak (Alburnus alburnus, (Leuciscusaspius, Linnaeus, 1758), (Vimba vimba, Linnaeus, 1758)

Family Percidae was represented by two species: European perch (Perca fluviatilispike-perch zander (Sander lucioperca(Table 1).

Family Siluridae represented one species of wels(Silurus glanis, Linnaeus, 1758), while the family Ameiuridae represented a kind of american catfish (Ameiurus nebulosus, Lesueur, 1819) (

Family Esocidae was represented by the type of pike (Esox lucius, Linnaeus, 1758), while the family Gobiidae was represented by monkey goby (Pallas, 1814) (Table 1). After systematic analysis procedure, microscopic analysis of native preparation taken from the fish skin andperformed. Mentioned analysis localized two

Agricultural Science and Review

the formula (Margolis et al.,

����� � � ����

������ � � ����X100

was performed using a non parametric square test) in the computer program

Studies of ectoparastic crustaceans of the Sava River conducted at four locations, where we sampled 120

fish individuals, approximately 30 individuals at each ). It has determined six fish families and

largest family, with nine of : bream (Abramis brama

Cyprinus carpio, Linnaeus, 1758), Linnaeus, 1758), crucian carp

, 1782), grass carp Valencienes, 1844), rudd

erythrophthalmus, Linnaeus, 1758), , Linnaeus, 1758), asp , 1758), vimba bream fish

, 1758) (Table 1). Family Percidae was represented by two species:

luviatilis, Linnaeus, 1758) and Sander lucioperca, Linnaeus, 1758)

represented one species of wels catfish , Linnaeus, 1758), while the family

Ameiuridae represented a kind of american catfish , Lesueur, 1819) (Table 1).

Family Esocidae was represented by the type of pike , Linnaeus, 1758), while the family Gobiidae

was represented by monkey goby (Neogobius fluviatilis,

After systematic analysis procedure, microscopic analysis of native preparation taken from the fish skin and gills was

entioned analysis localized two ectoparasitic

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Table 1.Biodiversity of the total fish sample

Fish speciesAbramis bramaAlburnus alburnusAmeiurus nebulosusCarassius gibelioCtenopharyngodon idellaCyprinus carpioEsox lucius Leuciscus aspiusNeogobius fluviatilisPerca fluviatilisSander luciopercaScardinius erythrophtalmusSilurus glanisSqualius cephalusVimba vimba

Total sample

Table 2. Number of infested fish from the total fish; (+) means presence of ectoparasitic crustaceans, (presence of ectoparasitic crustaceans

Fish species No of fish

Abramis brama 5 Alburnus alburnus 26 Ameiurus nebulosus 3 Carassius gibelio 14 Ctenopharyngodon idella 1 Cyprinus carpio 7 Esox lucius 6 Leuciscus aspius 2 Neogobius fluviatilis 36 Perca fluviatilis 5 Sander lucioperca 2 Scardinius erythrophtalmus 5 Silurus glanis 3 Squalius cephalus 4 Vimba vimba 1 Total sample 120

Figure 4.fish individuals from total sample

crustacean species: Argulus foliaceus (Ergasilus sieboldi.

Percentage of infestation of total fish sample was 10% i.e. from sample of 120 individuals, 12 individuals are

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Biodiversity of the total fish sample

Fish species No of fish Percentage Abramis brama 5 4,16 Alburnus alburnus 26 21,66 Ameiurus nebulosus 3 2,5 Carassius gibelio 14 11,66 Ctenopharyngodon idella 1 0,83 Cyprinus carpio 7 5,83

6 5 Leuciscus aspius 2 1,66 Neogobius fluviatilis 36 30 Perca fluviatilis 5 4,16 Sander lucioperca 2 1,66 Scardinius erythrophtalmus 5 4,16 Silurus glanis 3 2,5

cephalus 4 3,33 Vimba vimba 1 0,83 Total sample 120 100%

Number of infested fish from the total fish; (+) means presence of ectoparasitic crustaceans, (

No of fish Infested by Argulus foliaceus

Infested by Ergasilus sieboldi

Number of infested individuals

+ + 2- - 0+ + 2+ - 1- - 0+ + 3- - 0- - 0- - 0- - 0+ + 1+ - 1- - 0+ + 2- - 07 5 12

Figure 4. Number of infested and non infested fish individuals from total sample

(Figure 3) and

Percentage of infestation of total fish sample was 10% i.e. from sample of 120 individuals, 12 individuals are

infested by one or both mentioned parasitic species(Table 2).

Species Argulus foliaceus infestfrom total fish sample while species infests 6 (5%). Study showed that there are

Agricultural Science and Review

Nedić et al. 164

Number of infested fish from the total fish; (+) means presence of ectoparasitic crustaceans, (-) means non

Number of infested individuals

12

infested by one or both mentioned parasitic species

infests 9 (7.5%) individuals from total fish sample while species Ergasilus sieboldi

(5%). Study showed that there are 5 (more than

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165. Basic Res. J. Agric.Sci. Rev. 4%) infested fish individuals by both ectoparasitic crustaceans. Species Argulus foliaces is localized on 7 fish species while Ergasilus sieboldi is localized on 5 (Table 2). Statistical analysis showed that there is a small number of infested fish individuals by two mentioned ectoparasitic species, i.e. there are much more non infested individuals than infested individuals. Based on that, we agree that infestation by ectoparasitic crustaceans in the Sava River is very rare and the prevalence is low (p<0,05; x

2≈89,259). Species Ergasilus sieboldi is localized on fish gills

where its presence has very high impact on tissue damaging and very large amount of mucus production, while Argulus foliaceus is localized most often on the fish gills, but on infected species of Cyprinus carpio it is localized on the skin and gills (Table 2, Figure 4). DISSCUSION Although the major scaffold of overall biodiversity of Bosnia and Herzegovina is the Sava River, there is not a large number of fish species localized in Posavina region, only 15. If we consider overall diversity of Sava River we can emphasize that the number of fish species of Sava River in northern Bosnia and Herzegovina has decreased in the last several years (Sofradžija, 2009; Nedić et al., 2014; Habeković et al., 1990; Habeković and Popović, 1991; Habeković et al., 1997; A. Adrović, University of Tuzla, Faculty of Science, department of biology, personal communication). This could be serious problem for that watercourse referring to biodiversity and ecological relations. Present study shows that there is a high presence of invasive fish species like Neogobious fluviatilis. Presence of mentioned species could be harmful for the other fish species and other organisms because their coactions lead to the disturbance of natural equilibrium (Piria et al., 2011).

Ecological research focused on interactions of life forms has a big importance in ecological and biological sense where the special ecological relationships like parasitism, commensalism, symbiosis etc. have a primary role (Stanković, 1961). Parasitism is an ecological relationship between two organisms that are living together and one of them has a benefit while the other has damage from mentioned coactions (Stanković, 1961). Parasitism research on fish populations is quite intriguing and can contribute to better understanding of ecological coactions and relations in the nature hydro-ecosystems.

Most biologists emphasize that ectoparasitic crustacean species are one of the most prevalent ectoparasitic species on the fish populations (Ali Alaş et al., 2010; Mansoor and Al-Shaikh, 2011; Harrison et al., 2006; Pekmezci et al., 2011; Shahraki et al., 2014; Dezfuliet al., 2003; Notash, 2012). That fact speaks about

importance of study of mentioned organisms. The number of biologists who study ectoparasitic crustaceans of Balkans countries is not large and the consequence is a minor number of scientific articles that could be a valid indicator of real condition of fish populations, watercourses and other hydro-ecosystems.

Current study discovered two ectoparasitic species on fish from the Sava River, i.e. Argulus foliaceus and Ergasilus sieboldi with low prevalence (Table 2). Comparison of present study results with the results of other similar studies shows small difference. For example, infestation with Argulus foliaceus species in some studies is more than 20% (Notash, 2012; Pekmezci et al., 2011; Ali Alaş et al., 2010). Present study showed that the most often hosts of Argulus foliaceus are cyprinid fish (Abramis brama, Cyprinus carpio and Leuciscus cephalus) and that is in correlation with other similar studies (Ali Alaş et al., 2010; Mansoor & Al-Shaikh, 2011; Harrison et al., 2006; Pekmezci et al., 2011; Shahraki et al., 2014; Dezfuli et al., 2003; Notash, 2012). Also, study revealed something unusual, infestation of Carassius gibelio was very low and that is not in correlation with some studies (Skenderović, 2010; Notash, 2012). 14 individuals of mentioned species were localized, and just one of them was infected with mentioned parasite species. One of the reasons for that condition could be the size of the fish, because Carassius gibelio individuals localized in study were smaller, and some authors agree that large fishes are more infested than the small ones (Mansoor et al., 2011). Infested species, especially Cyprinus carpio, had the damage of gills, blood vessels were damaged and large amount of mucus were localized. That could be good indicator of health condition of cyprinid fish. Based on mentioned facts, we agreed that Argulus foliaceus species is seriously dangerous ectoparsitic parasitic species with negative impact on its host (Kabata, 1970; Kabata, 1984; Skenderović, 2010; Nedić, 2013; Mansoor and Al-Shaikh, 2011; Pekmezci et al., 2011).

Ergasilus sieboldi species was localized on 6 sampled individuals and 5 species (Table 2). Study showed very low prevalence of that species, only 5%. Some similar researches showed that prevalence of Ergasilus sieboldi can be higher (50%), especially on bream individuals (Dezfuli et al., 2003). Although the mentioned parasite species in our study is most prevalent on cyprinid fish species (Djikanović et al., 2011) some studies reveal it can parasite very often on the fish from Percidae family, most often on species Perca fluviatilis and Sander lucioperca (Tuuha et al., 2009; Molnar et al., 1997). These data show that Ergasilus sieboldi has very wide specter of specific hosts because it is adaptable species with very complicated life cycle with special adaptation for developing of parasites-host relation (Abdelhalim et al., 1991). For that reason this species could have harmful consequences for your host, and our study showed damaging of gills and inflammation with large mucus

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(Dezfuli et al., 2003).

We agree that infection with Argulus foliaceus and Ergasilus sieboldi could not be responsible for decreasing of fish populations from the Sava River because of their low prevalence. But we suppose that decreasing could be caused by infection with parasites species from other group, for example, ectoparasitic protozoa species (Nedić et al., 2014). We agreed that infested individuals could have metabolic disorder and tissue damage that could lead to mortality, although mortality of small number of individuals could not be the cause for the decreasing of the whole population (Fijan, 2006). CONCLUSION Present research was conducted in northern Bosnia and Herzegovina where 120 fish individuals from six families was sampled. Total number of sampled fish species was 15. Study showed that 10% individuals from total fish sample were infested by one or both of established ectoparasitic species, i.e. with Argulus foliaceus and Ergasilus sieboldi. Infected organs, most often gills, were histologically damaged and we suppose that the primary cause for that condition was negative impact of mentioned parasites. Also, present research revealed very low prevalence of both parasitic species and for that reason we cannot say that the infestation with ectoparasitic crustaceans in the Sava River can be the cause of decreasing fish populations from the same river. REFERENCES Abdelhalim AI, Lewis JW, Boxshall GA (1990). The life cycle of

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