Prevalence of Ligula intestinalis Larvae in Barbus Fish Genera at Lake Tana, Ethiopia

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1 World Journal of Fish and Marine Sciences 6 (5): , 014 ISSN IDOSI Publications, 014 DOI: /idosi.wjfms Prevalence of Ligula intestinalis Larvae in Barbus Fish Genera at Lake Tana, Eiopia Emaminew Tizie, Dereje Baye and Abdu Mohamed Jimma University College of Agriculture and Veterinary Medicine, P.O. Box: 307 Jimma, Eiopia Abstract: There are many parasitic diseases of fishes in e world. Among em e disease caused by larvae of L. intestinalis is one of e most common parasitic diseases which cause huge economic losses. A cross sectional study wi simple random sampling technique was conducted from October 013 to March 014 to determine e prevalence of L. intestinalis larvae in Barbus fishes found in Lake Tana. Three hundred (300) Barbus fishes wi different leng categories (short, medium and long ); weight categories (small, medium and large) fishes were collected from fish supplier associations and using Minnow trap and Scoop net and eviscerated in laboratory to investigate e parasite (L. intestinalis), e parasite burden in each fishes. A total of 87 Fishes were parasitized by L. intestinalis and e results showed at e overall prevalence of e disease was 9.00 % in Barbus fishes in e study area. Variation in parasite detection and identification between sex groups was not observed; and it was 0.85% and.00% in male and female fishes respectively. The rest 84 fishes out of e total 87 positive fishes were difficult to determine eir sexes as e sex organs were affected by e parasite; so at e 84 positive fishes were eier male or female. The parasite burden (number of parasite per fish) was also determined and it was found at out of 87 positive fishes 83 (94.50%) fishes were infested by one parasite larvae and e rest 4 (5.50%) by two parasite larvae. The rate of parasite detection and identification was different in different leng categories of fishes. The parasite was detected and identified wi prevalence of 40.60%, 4.40% and 1.15% in short; medium and large leng categories of fishes respectively. There was statistically significant difference ( = 10.90, P = 0.004) in different leng categories of fishes. The rate of parasite detection was also different in different weight categories of fishes. It was found at e prevalence of e parasite was 40.56%, 5.50% and 13.33% in small, medium and large fish categories respectively. There was highly statistically significant difference ( = 13.13, P=0.001) in different weight categories of fishes. There have been economic losses in fishery production due to L. intestinalis larvae. So e prevalence of e disease should be studied furer to set appropriate control measures. Key words: Barbus Fish Lake Tana L. intestinalis Scoop Net and Minnow Trap INTRODUCTION years. Fish is important to human population in trade and economy; it is of importance in e diet of different Globally, fish provides for more an 1.5 billion countries especially in e tropics and subtropics where people wi almost eir entire average per capital intake malnutrition is a major problem [4, 5]. As e human of animal protein and 3.0 billion people wi at least 15 population inevitably increases, e demand for fish as percent of such protein [1]. Global demand and source of protein will grow [6]. In recent times, ere has consumption of fresh fish have increased [, 3] for been tremendous increase in e development of fish instance a significant grow in fresh fish market has been farming and culture attributable to e increased need for observed in e United Kingdom (UK) during recent affordable animal protein especially in e tropics [7]. Corresponding Auor: Abdu Mohamed, Jimma University College of Agriculture and Veterinary Medicine, P.O. Box: 307 Jimma, Eiopia. 408

2 Eiopia covers a land area of 1.13 million km, of Ligula intestinalis is a cosmopolitan tapeworm at which 99.3 percent is a land area and e remaining 0.7 infects cyprinid fishes and fish eating birds and is percent is covered wi water bodies and comprises 10 indigenous to souern Africa [18]. The eggs of e major lakes in e country [8]; from ese inland water parasite shed togeer wi e birds faces and hatch in bodies for fish supply, Lake Tana is e leading and e water to form infective coracidia, which are ingested by biggest lake wi potential of about 13,000 to 15,000 tons copepods [19]. Cyprinid fish become e second of fish per year [] Current annual per capita fish intermediate hosts when ey eat parasitized copepods production is less an 40g in Eiopia [9]. Despite is, and are infected by e second stage larva called based on only a single factor; population current annual plerocercoid [19]. The plerocercoid is matured in intestine demand for fish in e country is estimated at 65,344 of e ird host, birds and laid eggs are released and tones, equivalent to 1 kg/person. Future demand at e hatched into e water and again are ingested by present population grow rate will reach 94,56 tons in copepods [0]. Fish ligulosis is a food borne zoonosis. 015 and 117,586 tons in 05 [10]. There have been recently reported a number of human Diseases rarely affect fish under ideal circumstances infestations wi is parasite especially when raw or not but when someing in e environment is not right e properly cooked fish is utilized [1]. stress weakens e fish us become susceptible to many Many research works in different countries of e diseases. Parasitic diseases are very common in fish all world show at e larvae of Ligula intestinalis is over e world and are of particular importance in e prevalent and causes high economic loss in fish tropics and subtropics [11]. Parasitic diseases are an production due to high morbidity, mortality, loss of essential part of e aquatic environment and represent a production and high treatment cost, but e prevalence of significant proportion of aquatic biomass. Their presence e disease has not been quantified in Eiopia. So e in eir host is generally at equilibrium in aquatic present study was planned wi e following main organisms and e most common life style on e planet objectives: [1]. Parasitic infection and diseases are some of e factors hindering high productivity in fish farming [13, 14]. To determine e current prevalence of e larvae of Fish parasites result in huge economic losses as ey Ligula intestinalis in genera of Barbus fish found in increase mortality; increase farm inputs via increased Lake Tana. treatment expenses and cause reduction in grow rate To study severity of infection (burden of e and possibly weight loss during and after e period of parasite) and organs of fish at are affected by parasitic disease outbreak. All ese militate against e larvae of e parasite expansion of aquaculture [14]. To study e association of different risk factors wi Togeer wi nematodes and flukes, tapeworms prevalence of e parasite. (Class: cestoda) are among e most important helmines parasites of fish [11]. These cestodes are internal (endo) MATERIALS AND METHODS parasitic platyhelmines at parasitize fish, amphibians and reptiles [15]. Cestodes (tape worms) are ribbon like Description of e Study Area: The study was conducted flat worms in which all adults inhabit e vertebrate from October 013 to March 014 in Bahir Dar town, at intestine. They required at least one intermediate host to Lake Tana. Bahir Dar is located in Amhara Regional State complete eir life cycle. Helmine parasites frequently about 565 km Nor West of Addis Ababa at an altitude occur wiin e body cavity and viscera of fish and some range of 156 meters to 341 meters above sea level of e largest and e most harmful parasites of e body (Fig. 1). It is found at 11 9 N latitude and 37 9 E cavity of fish are cestode plerocercoides [16]. Among e longitudes. The annual minimum and maximum plerocercoides e genus Ligula has a global distribution, temperature and rainfall ranges from 15 C to.5 C and mainly as parasites of cyprinid fish. The parasite causes 10 mm to 180 mm respectively. Lake Tana is one of e compression and distortion of e viscera and inhibited highlands lakes and is e source of e Blue Nile River gonadal maturation. Infected fish do not enter spawning and is e largest lake in Eiopia( Figure 1). Lake Tana is shoals, often swim poorly and more susceptible to located nearer to Bahir Dar city and it has approximately predation. Often infected fish may be recognized by eir 84 kilometers long and 66 kilometers wide, wi a maximum swollen abdomen [17]. dep of 15 meters and it covers e area at ranges from 409

3 Fig. 1: Map of e study area [30] Km up to 3500 km² depending on seasonal variation. predominate flora. They are only loosely rooted and can Lake Tana is located at an altitude of 1788 meters above also be found in larger quantities, sometimes floating e sea level []. The sources of water for Lake Tana are freely in e water column [5]. Since ere are no inflows different rivers including e small Abay, Reb and Gumara at link e lake to oer large water ways and e main rivers. The water temperature fluctuates depending on e outflow, e Blue Nile, is obstructed by e Blue Nile Falls, season. It has an average minimum temperature of 19 C e lake supports a highly distinctive fish fauna, which from July up to March and an average maximum generally is related to species from e Nile Basin [6]. temperature of 4 C from May up to June. The lake level About 70% of e fish species in e lake are endemic [6] has been regulated since e construction of e control This includes one of only two known cyprinid species weir where e lake discharges into e Blue Nile. This flocks (e oer, from Lake Lanao in e Philippines, has controls e flow to e Blue Nile Falls (Tis Abbay) and been decimated by introduced species) which consists of hydro electric power station. Lake Tana is an important fifteen relatively large which has e leng of 1 m is source of fish bo for e people immediately around e Labeo barbus barbs [6, 7]. Eight of ese are lake and elsewhere in e country. Its unique and isolated piscivorous and an important prey is e small Barbus landscape includes forested islands, immense and varied tanapelagius, anoer endemic of e lake are B. humilis, wetlands and high mountain areas. The region is B. pleurogramma also occur in Lake Tana, but neier of renowned for its biodiversity and it is also e home of em is endemic [7, 8]. churches and monasteries dating from e 14 to e 16 Lake Tana supports a large fishing industry, mainly century. Ninety percent of e area s rapidly growing based on e Labeo barbus barbs (formerly in genus population of.5 million people depends on subsistence Barbus), Nile tilapia and sharp too catfish (a large agriculture for eir livelihoods. The productivity and catfish at is widespread in Africa). According to e sustainability of mixed farming practices depend on Eiopian Department of Fisheries and Aquaculture, 1,454 ecosystem goods and services, which rely on e tons of fish are landed each year at Lake Tana which is functional integrity of e watershed s ecosystems, rivers, 15% of its sustainable amount [9]. Among oer fauna, e wetlands, lake, forests, pastures and soils [3]. The lake supports relatively few invertebrates. There are phytoplankton of Lake Tana is dominated by fifteen species of molluscs, including one endemic and Cyanobacteria and Bacillariophyceae; however also an endemic freshwater sponge [6]. Numerous Chlorophyta and e green algae are less abundant [4] wetland birds such as e great white pelican and African while Papyrus (Ceprus papyrus) and water lilies are e darter, reside at Lake Tana. It is an important resting and 410

4 Fig. : Study populations and equipments (scoop net and minnow trap) at were used to trap small sized fishes feeding ground for many migrant water birds [6]. There eir daily production (Kg of fish/day). The study are no crocodiles, but e African soft shell turtle has population of large, medium and small sized fishes, wi been recorded near e Blue Nile outflow from e lake e techniques of trapping of small sized fishes in e lake [9]. is showed in Figure. Study Population: The study animals were fishes of one genus Barbus at were collected from Lake Tana. Large, medium and small sized fishes were included in my study. Large and medium sized fishes were selected by simple random sampling from e two fish supplier associations at are found in Bahir Dar, while e small sized fishes were collected from e lake and were selected by simple random sampling. The number of large and medium sized fishes for each association was divided by considering Study Design: The study was cross sectional wi simple random sampling technique to determine e prevalence of Ligula intestinalis on e Barbus fish genera. Sample Size Determination: The sample size required for is study was determined depending on e expected prevalence of e parasite and e desired absolute precision. The sample size was computed using e formula given in Thrusfield [31] as follows 411

5 1.96 Pexp (1-Pexp) Data Management and Analysis: The data were entered N = and managed in Microsoft Excel. All e data analysis was d done by Statistical Package for Social Science (SPSS) Where: software version 16. Descriptive statics such as N = required sample size percentages and frequency distribution were used to Pexp = expected prevalence describe e nature and e characteristics of e data. d = desired absolute precision The prevalence of L. intestinalis was analyzed using percentages. The association of different risk factors wi There is one previous study which indicates e prevalence of parasite was computed by Chi-square ( ) prevalence of Ligula intestinalis in genus Barbus fish in test. e study area which was.5%. Therefore, an expected prevalence.5% was used to estimate e sample size. RESULTS Using desired 95% confidence interval, 5% precision and.5% expected prevalence, e necessary numbers of Prevalence of L. Intestinalis in Barbus Fish: fishes needed to determine e prevalence, severity of infection (burden of parasite) and e affected organs of fish by e parasite were 68 fishes. However, 3 more fishes were added and 300 fishes were included in my study to improve e precision. Study Meodology: A total of 300 different sized fishes were included in my study. Big and medium size fishes were collected from two fish supplier associations found in Bahir Dar; while e small size fishes were collected directly from e lake by using Scoop net and Minnow trap. All samples of fishes were clearly labeled wi e date of sampling and e name of associations [3]. Thus, all samples were transported immediately in ice box to Bahir Dar Fishery and To Aquatic Life Research Center Laboratory. In e laboratory, e necessary parameters including leng and weight were taken and sex of e fishes was determined [33].Finally each sample of fish was evaluated visually and postmortem examination was done using appropriate postmortem kits using standard evisceration/incision technique [33]; to assess e parasite; affected organs of fish, e burden e parasite and e sex of e fishes were determined. Based on e above procedures fishes were categorized in different groups. In respect to eir leng, fishes wi e leng of 5-0 cm, 1-9 cm and cm were categorized as small, medium and large fishes respectively. In addition, e weights of e fishes were measured and fishes wi e weight of gm, gm; gm were categorized in different groups. Sex of e fishes was identified after post mortem evisceration of fishes; and ey were categorized as male, female and undetermined sex (Sex organ of e fishes are affected by parasite and difficult to identify e sex). A total of 87 samples out of 300 fishes were positive for L. intestinalis larvae. The overall prevalence L. intestinalis larva in Barbus fish was found 9.00 %. Prevalence of L. intestinalis in Respect to Leng of Fishes: The prevalence of L. intestinalis was determined in relation to eir total leng; and it was found different wi different leng groups. The prevalence of e parasite was 40.60%, 4.40% and 1.15% in small, medium and large fishes respectively as shown in Table 1. Prevalence of L. intestinalis in Respect to Body weight of Fishes: The prevalence of L. intestinalis was determined in different weight categories of fishes; and it was found at e prevalence of e parasite is different in different weight categories of fishes; and it was 40.56%, 5.50% and 13.33% wi eir 3-99 gm, gm and above 300 gm weight categories respectively as shown below in Table. Prevalence of L. intestinalis in Respect to Sex of Fishes: The prevalence of L. intestinalis was determined in different sex groups of fishes; and it was found at e prevalence of e parasite is almost similar wi different sex groups; and it was found at 0.85% and % in male and female fishes respectively. The higher prevalence was found in sex undetermined groups of fishes (84.00%) as shown in Table 3. The reason why e prevalence of e parasite was higher in sex undetermined group is at e parasite affects e sex organs of fishes and it was difficult to determine eir sex; however sex undetermined fishes were eier male or female. 41

6 Table 1: Prevalence of L. intestinalis in Barbus fishes wi different lengs Leng of fish in cm No of samples No of infected fish Prevalence (%) 95% of CI Total Table : Prevalence of L. intestinalis in Respect to Body Weight of Fishes Body weight (gm) No of samples No of positives Prevalence (%) 95% of CI Total Table 3: Prevalence of e Parasite in Respect to Sex of Fishes Sex of fishes No of samples No of positive Prevalence (%) 95% CI M F Sex Undetermined groups # * Total # and * = No need of determination as ey are eier male or female groups Table 4: Parasite burden (Number of Parasite larvae per Fish) No of parasite larvae per fish No of infected fishes Percent (%) from e total Total Table 5: Association of e prevalence of L. intestinalis wi different risk factors Body weight (gm) No of samples No of positives Prevalence (%) 95% of CI Total Burden of Parasite (Number of Parasite per Fish): The of fishes was statistically significant difference (P<0.005) parasite burden of e affected fishes was assessed by as shown in Table 5. Association of e prevalence of e counting e number of L. intestinalis larvae. It was found parasite wi different weight categories of fishes was at out of 87 positive fishes 83 fishes( %) were also assed; and it was found it had highly statistically infected by one larvae of e parasite; while 4( 5.50 %) significant difference (P<0.005) in different weight were infected by two larvae of e parasite as shown in categories of fishes as shown in Table 5. Table 4. DISCUSSION Association between Prevalence of L. intestinalis wi Different Risk Factors: Furer e association of e There are many parasitic diseases of fishes in e prevalence of L. intestinalis wi different risk factors was world. Among em e disease caused by larvae of L. assessed; and it was found at e association of e intestinalis is one of e most common parasitic diseases prevalence of e parasite wi different leng categories of fishes. Fish parasites result in huge economic losses as 413

7 ey increase mortality; increase farm inputs via increased was in total agreement wi e finding of Shargh et al. treatment expenses and cause reduction in grow rate [40] and Oguz et al. [41]. However, it contrasts wi e and possibly weight loss during and after e period of finding of Dejene [35] who found at small size fishes parasitic disease outbreaks. In is study, attempts were have a low ability in catching e infected copepods an conducted to determine e prevalence of L. intestinalis large fishes; and large size fish have been exposed for a in genera of Barbus fishes at Lake Tana. The results of longer period to e risk of being infected by e parasite. e present study showed at e prevalence of L. The association of e prevalence of e parasite wi intestinalis in genera of Barbus fishes in Lake Tana was different weight categories of fishes was assessed and it found to be (9.0%). Similar results had been reported by was found at e prevalence of e parasite varies wi Gholami et al. [34] which was (. %); e research work different weight categories of fishes; and it was %, at was done in Mehran River of sou of Iran. Barbus 5.50% and 13.33% in small, medium and large size fishes are zooplankton feeders most of e time and fishes respectively. The difference was statistically harbor e parasite by ingesting copepods which are e significant (P< 0.05). This could be due to e fact at e first intermediate host of L. intestinalis [35]. The copepods were e major part of small fishes diet; and prevalence of L. intestinalis was also determined in low weight is one of e susceptible factors for L. different sex groups of fishes; and it was found 0.85%, intestinalis [40]. The low infection level of large fishes.00 %, in male and female fishes respectively. The was e fact at large fishes are older in age and ey less prevalence of e parasite was % in undetermined consume copepods an small fishes, which was totally sex groups of fishes; is is e fact at e parasite disagrees wi e work of Dejen [35] and Geraudi et al. affects e sex organs of fishes and it was difficult to [4] who found e low ability of small fishes in catching determine eir sex; however sex undetermined fishes e large and invasive copepods wi parasites; and e were eier male or female, as e Ligula intestinalis larger and older fishes have been exposed for a longer affects bo sexes wiout preference. This result totally period to e risk of being infected by e parasite from agrees wi e finding of Mehmet et al. [36]; e research copepods. work at was done at Lake Mogan. Ligula intestinalis hampers e gonadal development and cause infertility of REFERENCES infected fish [37]. The parasite burden of e affected fishes was 1. SOWFA, 010. State of World Fisheries and assessed by counting e number of L. intestinalis larvae. Aquaculture. FAO, Rome. It was found at out of 87 positive fishes 83 fishes ( FAO, 009. Utilization and trade. In Fisheries Issues, %) were infected by one larvae; while 4 (5.50 %) were FAO Fisheries and Aquaculture Department, Rome. infected by two larvae of e parasite. The result agrees Available at wi e finding of Gholami [34]. He found at out of 63 en. Accessed April 8. dissected fish only two fish were infected wi 4 and 3 3. Vannuccini, S., 004. Overview of fish production, parasites respectively and e oers had only one utilization, consumption and trade: based on 00 parasite per fish. While it contrasts wi e finding data, FAO, Fishery Information, Data and Statistics of Dejen et al. [38]; who found only one parasite per fish Unit, Rome. in his study. This may be due to e increase in e final 4. Alune, E. and G. Andrew, Fishes. 8 ed. host (large white pelicans) population. Cambridge University Press, London, pp: This study was also focused to know e presence or 5. Osuigwe, D.I. and A.I. Obiekezie, 007. absence of association between e prevalence of L. Assessment of e grow performance and feed intestinalis wi different risk factors. The prevalence of utilization of fingering Heterobranchus ongifilis fed e parasite was %, 4.40 % and 1.15% in small, raw and boiled jack bean (Canavalia ensiformis) medium and large leng fishes respectively. The seed meal as fishmeal substitute. Journal of Fish difference was statistically significant (P<0.05). This could International, : be due to e fact at small and medium fishes are found 6. Abolarin, M.O., A new species of Henneguya on e shores of e lake where e birds and copepods (Myxosporida protozoa) from West African cat fish, are more. Small leng (juvenile) fishes were highly Clarias lazera (Vaal) wi a review of e genus susceptible to parasite infection due to e fact at Henneguya (Thelohan). The African Journal of eir immune system is not fully developed [39]; which Tropical Hydrobiology Fish, 1:

8 7. Davies, O.A., M.B. Inko-Tariah and D. Amachree, 1. Eslami, A., 006. Veterinary helminology: 006. Grow response and survival of Cestode. Vol, 6 ed. University of Tehran press, Heterobranchus longifilis fingerlings fed at different Iran, pp: feeding frequencies. African Journal of. Tesfahun, G. and S. Demissie, 004. Lake Tana: Biotechnology, 5: A socioeconomic synopsis. Amhara Regional 8. MoWR, 00. Water sector development program Agricultural Research Institute, Bahir Dar, (WSDP). Addis Ababa, Eiopia. Paper presented to The Lake Tana Resource 9. FAO, 003. Fishery country profile, Eiopia. Management Workshop, Bahir Dar, Eiopia. Available at 3. Berhanu, T., E. Ralphel and Z. Girma, 001. ETH/profile.htm. Development Initiatives and Challenges for 10. Christopher, E. and L. Delgado, 003. Fish supply and Sustainable Resource Management and Livelihood in demand in changing global markets. International e Lake Tana Region of Norern Eiopia. Food Policy Research Institute and World Fish Proceedings of e Wetland Awareness Creation and Center. Statistical Abstract of Eiopia. 1968/76. Activity; Identification Workshop in Amhara 11. Roberts, L.S. and J. Janovy, 000. Gerald D. Schmidt rd National Regional State. January 3 001, Bahar Dar, and Larry S. Roberts Foundations of parasitology, Eiopia. 6 International Editions. Boston, pp: Ayalew, W., S. Mengistu, J. Mengistu, Vijverberg 1. Marcogliese, D.J., 005. Parasites of e and E. Dejen, 007. Seasonal variation in primary super-organism: Are ey indicators of ecosystem production of a large high altitude tropical lake heal? International Journal of Parasitology, (Lake Tana, Eiopia): Effects of nutrient availability 35: and water transparency. Journal of Aquatic Ecology, 13. Doglel, V.A., G.K. Petrushevski and Y.I. Polyanski, 41: Translated by (Kabata) Parasitology of Fishes. 5. BCEOM and Associates, Abay River Basin Oliver and Boyd, Edinburgh and London, pp: 384. Integrated Development Master Plan Project: 14. Kayis, S., T. Ozcelep, E. Capkin and I. Altinok, 009. Stage II-dam profiles. Protozoan and metazoan parasites of cultured fish in 6. Freshwater Ecoregions of e World, Turkey and eir applied treatments. The Israeli 008. Lake Tana Available at Journal of Aquaculture in Bamidgeh, 61: ecoregion. details. Php? Eco=56. Accessed Robert, R.J., 003. Fish paology. January 014. rd 3 ed. Philadelphia, USA, pp: De Graaf, Dejen, E. and Sibbing pand Osse, Khali, L. and L. Polling, Check list of e Barbus tanapelagius, A New Species from Lake helmins parasites of African freshwater fishes. Tana (Eiopia): its Morphology and Ecology. Department of Zoology/Biology/, University of Nor Environmental Biology of Fishes, 59(1): 1-9. Saverga, Sou Africa, pp: De Graaf, Megens and Samallo Sibbing, Lewis, G.W., Angler s guide to fish disease and Evolutionary origin of Lake Tana's (Eiopia) small parasite: Aens: Cooperative Extension Service, Barbus species: Indications of rapid ecological pp: 7. divergence and speciation. Journal of Animal 18. Prudhoe, S. and C.G. Hussey, Some parasitic Biology, 57(1): worms in freshwater fishes and fish predators 9. Largen, M.J. and S. Spawls, 010. The Amphibians from Transvaal, Sou Africa. Zoolgica Africana, and Reptiles of Eiopia and Eritrea. ISBN : Hoole, D., Parasitic diseases of fish. 30. Nagelkerke, L.A.J., M.V. Mina, W. Tesfaye, In: A.W. Pike and J.W. Lewis (ED.): F.A. Sibbing and J.W.M. Osse, In Lake Tana, Tapeworm Infections in Fish: Past and Future a unique fish fauna needs protection. Bioscience, Problems. Samara Publishing Limited, Tresai, 45: Dyfed, pp: Thrusfield, M., 005. Veterinary epidemiology 0. Innal, D., N. Keskin and F. Erkakan, 007. nd ed.uk, Black well science, pp: J.G. Van As Distribution of Ligula intestinalis larvae in Turkey. and L. Basson, Check list of freshwater fish Turkish Journal of Fisheries and Aquatic Sciences, parasites from souern Africa. Sou Africa Journal 7:19-. of Wild Life, 14:

9 3. OIE, 004. Diagnosis of fish parasites. Amanual of 38. Dejen, E., J. Vijverberg and F.A. Sibbing, 006. standards for parasitic diseases in aquatic animals, Spatial and temporal variation of cestode : 1-7. infection and its effects on two small barbs 33. Zhokhov, A.E. and Mironovsky, 007. Meods of (Barbus humilis and Barbus tanapelagius) in Lake e complete parasitological dissection of fish. Tana, Eiopia. Hydrobiologia, 566: Progress press, Moscow, Russia, pp: Bagge, A.M. and E.T. Valtonen, Gholami, Z., M. Akhlaghi and H.R. Esmaeili, 011. Development of monogenic communities on e gills Infection of Aphanius dispar wi Ligula intestinalis of roach fry (Rutilus rutilus). Journal of Parasitology, plerocercoids in Mehran River, Hormuzgan province, 118: sou of Iran. Iranian Journal of Fisheries Sciences, 40. Shargh, M., S. Shamsaii and Karimi, 008. Distribution 10(): of Parasitic Cestod "Ligula intestinalis" in 35. Dejen, E., 003. Ecology and potential for fisheries of Mazandaran Region. Iranian Journal Parasitology, e small barbs (Cyprinidae, Teleostae) of Lake Tana, 3(): Eiopia. Wageningen University, Belgium, PhD. 41. Oguz, M.C., M. Oguz and H. ÖztürkGüre, Thesis Seasonal variation of e Plerocercoid 36. Ergonul, M.B. and A. Altindag, 005. The effects of Ligula Intestinalis (L.) observed in roach Ligula intestinalis plerocercoids on e grow (Rutilus rutilus (L) from e Yenice Irrigation Pond, features of Tench, Tinca tinca. Turk J. Vet Anim Sci., Canakkale, Turkey. Vet. Glasnik, 58(): : Geraudie, P., C. Boulange, M. Gerbron, N. Hinfray, 37. Choudhury, A. and T.A. Dick, Fish F. Brion and C. Minier, 009. Endocrine effects of e diseases and disorders. Protozoan and metazoan tapeworm Ligula intestinalis in its teleost host, infection CABI. Vol.1, 8 ed. Walling ford. UK., e roach (Rutilus rutilus). Parasitology, pp: Cambridge University Press, Le Havre, France, 136:

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