Iranian Journal of Veterinary Research, Shiraz University, Vol. 12, No. 3, Ser. No. 36, 2011

Scientific Report

Metazoan parasite community of Capoeta damascina (Valenciennes in Cuvier and Valenciennes, 1842), Basin, Mesopotamian region- a checklist

Jalali Jafari, B.1 and Miar, A.2*

1Department of Aquatic Animal Disease, School of Veterinary Sciences, Islamic Azad University, Science and Research Branch, Tehran, ; 2Ph.D. Student in Fisheries, Department of Fisheries, School of Natural Resources, Islamic Azad University, Science and Research Branch, Tehran, Iran

*Correspondence: A. Miar, Ph.D. Student in Fisheries, Department of Fisheries, School of Natural Re- sources, Islamic Azad University, Science and Research Branch, Tehran, Iran. E-mail: Argha- [email protected]

(Received 4 Aug 2010; revised version 13 Feb 2011; accepted 1 Mar 2011)

Summary

In this paper, the metazoan parasite community system of Capoeta damascina in the Tigris basin (Meso- potamian region) in the Middle-East is presented. Overall, 54 species have been identified. Between 2005 and 2008, Iranian surveys of Capoeta damascina found a total of 47 metazoan parasites species, most identi- fied to species level. In addition, 6 parasite species from Iraq and 1 species from occupied Palestine have been reported. Among these, 16 species belong to Monogenea (30%), including Dactylogyrus 9, Gyrodacty- lus 4, Paradiplozoon 1 and Dogielius 2 species. The remaining 70% belong to: Cestoda (7.4%) including Ligula, spp Caryophyllaeus and Coelobothrium 1 species each; Crustacea (5.55%) comprising Lernaea, Ar- gulus Ergasilus 1 species each; Digenea (11.11%) containing Allocreadium spp, Diplostomum, Clinostomum tylodelphis, 1 species each; Acanthocephala (5.55%) 3 species; Nematoda (14%) 8 species; Myxozoa (18%) including Myxobolus with 9 species, Myxidium with 1 species and, Hirudinea 3 species; and at last, Bivalva, Unio as 1 species.

Key words: Dactylogyrus, Metazoan, Parasites, Capoeta damascina

Introduction halnandi” , a tributary north of Ahwaz. Gonzáles-Solies et al. Capoeta damascina is found in Turkey, (1997) reported the nematodes Rhabdocho- Syria, Lebanon and from occupied Palestine na denudata and Rhabdochona fortunatowi to Iran. In Iran it is reported from the Tigris from this species in the Mand river, Fars. river and its headwaters in Kurdestan and Amin et al. (2003) identified the acanthoce- Kermanshah provinces, from the ba- phalan Acanthocephalorhynchoides cholod- sin (Dez, Karkheh), Zayandeh-Rood kowskyi from specimens collected in the river (Esfahan basin) and waters in Kavir- Mand river west of Shiraz, Fars. Jalali et al. Namak-Ghom and Maharlu basins (8 basins) (2005) and Jalali and Barzegar (2006) rec- (Fig. 1). Parasitological investigation of Ca- orded Trichodina pediculus, Dogielius mol- poeta damascina in Iran is recent, as it was nari, Gyrodactylus sp., Dactylogyrus caras- first started by Dollfus (1970) who described sobabrbi and D. lenkorani from this species a new cestode, Coelobothrium monodi, from in Lake Zarivar. Barzegar et al. (2008) found this species at “Nasratabad”, possibly from Dactylogyrus lenkorani, Gyrodactylus sp., the Lut basin. After many years, Jalali et al. Dactyolgyrus pulcher, Allocreadium isopo- (1995) described two new species of mono- rum and Myxobolus molnari from the Be- geneans - Dactylogyrus rohdeianus and D. heshtabad river. Mehdipoor et al. (2004) capoetae - from fish caught in the “Chag- recorded the monogeneans Dactylogyrus

265

Iranian Journal of Veterinary Research, Shiraz University, Vol. 12, No. 3, Ser. No. 36, 2011 lenkorani and D. pulcher in Zayandeh-Rood dies of freshwater bodies. Further data was river fish. Barzegar and Jalali (2006) re- gathered from related papers published in ported parasitic from Kaftar Lake as Dacty- reliable scientific research journals and cred- logyrus lenkorani. Masoumian et al. (2007) ible research work of fisheries research or- recorded the myxosporean parasites Myx- ganizations or universities in Iran. Metazoan obolus samgoricus and M. varicorhini from parasites from our research work (see Table this species in the Zayandeh-Rood river. 1) are referred to as present work. Those not yet published were collected recently from various locations on examined fish including skin, fins, gill and bucal cavity. Samples were stained and mounted according to Fer- nando et al. (1972). Identification of parasites specimens was carried out in accordance with the keys giv- en by Gussev (1983), Moravec (1994), and Jalali (1998). The identification of fish host was car- ried out by an Iranian Ichthyologist in ac-

cordance with Coad (1992), Abduli (1999) Fig. 1: Blue colors indicate riverine basin and and then the results were confirmed with the red colors indicate main area (Basins) where help of Dr. S. Holoik. Capoeta damascina is found, (Abduli, 1999) Data concerning species from Iraq was collected from published papers in reliable Ali et al. (1987) investigated the parasite scientific journals. fauna of this species (as Barbus belayewi) in the lower Diyala river and found Dactylogy- Results rus cornu on the gills and Neoechinorhyn- chus rutili in the intestine. Amin et al. Table 1 shows the 46 metazoan parasites (2003) summarized the monogenetic trema- reported during the present study in Iran and tode Dactylogyrus species of Iraqi fish and 6 species in Iraq, with no overlap. In addi- reported D. cornu on this fish species (as B. tion, Paperna (1961) described Dogielius belayewi). Balasem et al. (1995) surveyed planatus in Galilee Lake in occupied Pales- fish parasites from the Tigris river at tine, for the first time. Overall, 54 metazoan Za’faraniyah, south of Baghdad, and found parasites species have been shown to occur the myxozoan Myxobolus pfeifferi on this in these study countries (Fig. 2). These me- species (as B. belayewi). Amin et al. (2003) tazoan parasites represent different systemat- describe a new species of Acanthocephalan, ic groups including 16 monogenean, 9 Myx- Neoechinorhynchus zabensis, from the intes- ozoa, 6 digenean, 8 nematoda, 4 Cestoda, 3 tine of fish from the Lesser and Greater Zab Acanthocephala, 3 crustacean, 3 hirudinean, river. Recently, Amin et al. (2003), Bilal and 1 bivalvida (Fig. 3). (2006), and Bilal and Abdullah (2008) iden- The community of monogenean para- tified and reported several nematodes, acan- sites, with 16 species, constituted the most thocephalan and pleistophora species in C. common metazoan parasite group, account- damascina. According to data collected by ing for (30%). various authors so far, 53 metazoan parasites Capoeta damascina was found to be in- species belonging to 9 classes were found fected by 4 zoonotic metazoan parasite lar- and appear in scientific journals. vae species, serving as an intermediate host. These larvae include 2 digenean (metacerca- Materials and Methods ria) and 2 Cestoda (plerocercoid) which are commonly found parasitizing cyprinid fish. Collection of data for preparation of the The community of ectoparasites in- present review primarily originated from cludes23 species, all with complete life fish health studies in different natural and man-made lakes during comprehensive stu-

266

Iranian Journal of Veterinary Research, Shiraz University, Vol. 12, No. 3, Ser. No. 36, 2011

Table 1: List of metazoan parasite species found in Capoeta damascina in Iran, Iraq, and occupied Palestine

Monogenea Digenea Cestoda Nematoda+ Acanthocephala+ Myxozoa Crustacea Hirudinian+ Bivalve

D. capoetae Diplostomum spata- Coelobothrium mo- Rabdochona denu- Acanthorhychoides Myxobolus samgori- Lernaea cyprinicea Cystobranchus Unio sp. ceom (metacercaria) nody date choldchowski cus (Masoumian et (Jalali et al., 1995) respirans (Jalali et al., 1995) (Barzegar et al., 2008) al., 2007) D. carasobarb Allocreadium isopo- Kawia armenica R. fortunatowi Neoechinorhinchus M. varicorhini (Ma- Argulus foliaceus Hellobdella sp. rum rutili (Bilal and soumian et al., 2007) Abdullah, 2008) D. cornu A. laymani L. intestinalis Rhabdochona Neoechinorhynchus M. pfefferi (Bilal and Ergasilus sp. Trachobdella sp. zabensis (Amin et al., Abdullah, 2008) gnedini 2003) D. lenkorani A. trandversasli Ligula sp. Rabdochona sp. M. molnari (Jalali et al., 2000) D. linstowi Tylodelphis sp. (meta- R. macrostoma M. musajevi (Jalali cercaria) (Barzegar et et al., 2000) al., 2008) D. pulcher Clinostomum compla- Hepaticola M. cristatus (Ma- natum (metcercaria) soumian et al., 2007) petruschewkii D. rohdeianus Contracaecum M. karelicus (Ma- soumian et al., 2007) (Jalali et al., 1995) micropapilatum Dactylogyrus sp1 Rhabdochona tigrae M. buckei (Masou- (Bilal, 2006) mian et al., 2007) Dactylogyrus sp2 M. suturalis (Ma- soumian et al., 2007) Do. Molnari Myxidium rhodei (Jalali et al., 2000) (Jalali and Barzegar, 2006) Do. Planates (Paperna, 1961) Paradiplozoon sp. (Jalali et al., 2005) Gyrodactylus spp4 (Jalali and Barzegar, 2006) +: Parasites found in riverine habitat 267

Iranian Journal of Veterinary Research, Shiraz University, Vol. 12, No. 3, Ser. No. 36, 2011 spans; 16 mongenean, 3 hirudinean, 3 crus- plains- was studied. The structure of the me- tacean and 1 bivalvida. Endoparasite com- tazoan community where monogeneans are munities were composed of 9 myxzoa, 8 the dominant component indicates a high nematode, 6 digenean, 3 Acanthocephalan eutrophication of water bodies down streams and 4 Cestoda; in total 30 species, all with in the Tigris region. In these parts of the re- indirect life spans. gion, 16 Monogenean, 6 digenan, 4 Cestods, Additionally, several protozoan parasites 3 Crustacean and 3 Hirdinian species were were also identified in gills, muscles and found in examined fish (also confirmed by skin which were not taken into account. Pa- Dzika et al., 2007). The community of para- rasite fauna of Capoeta damascina, species sites up stream, situated in the highlands of with wide host ranges are not common (Dip- the region, is mainly composed of 3 acan- lostomum sp., Allocreadium spp, Kawia and thocephalan, 10 Myxozoa and 1 Nematoda ligula sp.), but host specific monogeneans which are mostly rheophilic species. Such a which included around 30% of metazoan phenomenon can be interpreted from the parasites species are numerous. biology and feeding behavior of C. damas- Among various parasites species found, cina, which is mainly classified as a phyto- 34.4% of species occur in gills, (Monoge- benthophagus fish. A variety of insects are nea, crustacean, bivalvida). A few species also found in its long intestine; for instance attach to skin and fins, (9.40%)(Hirudinian, Chironomidae, Formicidae, Epididae and crustacean). Histozoic metazoans constitute Simulidae (Coad, 1992). Furthermore, other 22.6% (Myxozoa, Digenean metacercaria) zoobenthic fauna, like mollusks and a few and these species inhabit the intestinal lu- suspended copepods, are also eaten by C. men where they reach maturity (30.10%) damascina, some of which serve as an in- (includes adult digenea, adult Cestoda and termediate host of the mentioned parasites nematode). The remainders are two coelo- with incomplete life cycle (Myxozoa, Acan- zoic species from genus Ligula spp. thocephala). When comparing metazoan parasite richness in C. damascina in two different environments, it becomes evident that the prevalence of fauna found in some parasitic groups, specifically those tropically trans- mitted, such as the digenean parasites (3 adults and 3 larva) and cestodes (2 larvae and 2 adults), may be due to the presence of mollusks and cyclops in the down stream, lentic habitat of C. damascina, in rather pol- Fig. 2: Proportion of metazoan parasites re- ported from Mesopotamian region countries luted part of the Tigris region. Conversely, the parasitic community in C. damascina up stream and in cleaner waters, is mainly po- pulated by Acanthocephalan and some Ne- matoda. Three crustacean specimens (in low in- tensity) were found on the examined fish. They were Lernaea cyprinidea on the fins, Argulus foliaceus on skin, and Ergasilus sp.

in gills. All of them are Limnophilic species, Fig. 3: Percentages of systematic groups of which is not the environment preferred by C. metazoan parasites found in C. damascina damascina. More attention should be paid to Mono- Discussion genean parasites found on the gills, fins and skin of the examined specimens. Among the The metazoan parasite community of C. identified Monogenean species found, 3 damascina from two ecologically different Dactylogyrus species (D. rohdianus, D. Ca- systems-lotics in mountains and lentics on poeta, and D. carassobarbi) and 2 Dogielius

268

Iranian Journal of Veterinary Research, Shiraz University, Vol. 12, No. 3, Ser. No. 36, 2011 species (Do. molnari and Do. planatus) are from freshwater fish in northern of Iraq. Folia native to and are highly spe- Parasitol., 50: 293-297. cific to C. damascina. Balasem, A; Mhaisen, T; Adday, T; Juwdat, M; Morphological peculiarities of Dactylo- Al-Juwda, M and Asmar, KR (1995). A gyrus spp fauna of C. damascina clearly second survey of parasitic infections in freshwater fishes from the al-Qadisiyah prove its Mesopotamian origin. Endemic lake, river, Iraq. Marina Mesopo- Monogenean species of this sub region pos- tamica. 18: 123-140. sess the elements of both Palaearctic fauna Barzegar, M and Jalali, B (2006). Helminthes, and African fauna at the same time, having Acanthocephala and Crustacean parasites of undergone an independent evolution (Gus- fishes in Vahdat reservoir. Iran. J. Vet. Sci., 3: sev, 1983). 229-234 (in Persian). These monospecific parasite species, Barzegar, M; Raisi, M; Bozorgnia, A and Jalali, which only infect single host species, can be B (2008). Parasites of the eyes of freshwater interpreted as a situation in that the host and fishes in Iran. Iranian J. Vet. Res., 9: 256-261. parasites have evolved and specified togeth- Bilal, SJ (2006). Parasitic fauna of some cyprinid fishes from Bahdinan river in Kurdistan re- er (Kennedy, 1975). This type of monospeci- gion-Iraq. MSc Thesis, Science Education ficity is therefore generally held to indicate a College, University of Salahaddin. P: 90. long-term association between Dactylogyrus Bilal, SJ and Abdullah, SMA (2008). Protozoa spp as parasites and C. damascina as host, and crustacea infesting some cyprinid fishes reflecting the phylogeny of both host and from Bahdinan river in Kurdistan region-Iraq. parasites. Kurdistan 2nd conference on biological In conclusion, on the basis of the present science University of Duhok, Dohuk, Iraq. P: data, we suggest that species composition 70. and species richness of metazoan parasite Coad, AW (1992). Freshwater fishes of Iran. A communities of C. damascina appear to vary checklist and bibliography. Ichthyology Sec- tion. Ottawa, Ontario, Canada, Canadian Mu- significantly on a large geographical scale seum of Nature. P: 66. (Mesopotamian fauna region). The extent to Dollfus, RPh (1970). D’un cestode ptychoboth- which these differences are truly geographi- rien parasite de cyprinide en Iran. Mission cal or reflect concentrating degrees of envi- C.N.R.S. (Théodore Monod), février (1969). ronmental alteration between basins is an Bulletin du Muséum National d’Histoire Na- open question. turelle, Paris. Série 2. 41: 1517-1521. It is obvious that a clearer picture of me- Dzika, E; Kusztala, A and Kusztala, M (2007). tazoan parasite diversity and species compo- Parasites of common bream Abramis brama, sition, especially in monogenean species in from a shallow, brackish-water coastal lagon C. damascina, must await a better under- (Lake), Poland. ISFP 7th Abstract. Viterbo, Italy. P: 337. standing of all parasite fauna from speci- Fernando, CH; Furtado, JR; Gussev, AV; Hanek, mens inhabiting the Tigris basin in Iran and G and Kakonge, SA (1972). Methods for the additionally in Iraq, Syria, Turkey and Oc- study of fresh water fish parasites. 1st Edn., cupied Palestine. Current studies suggest Canada, University of Waterloo. Biology this basin is the ancestral home of C. damas- Sources. P: 76. cina. Gonzáles-Solies, J; Jover, L; Rviz, X and Pe- drocchi, V (1997). Trophic niche width and overlap of two sympatric gulls in the south- References western Mediterranean. Oecologia. 112: 75- 80. Abduli, A (1999). The Inland Water fishes of Gussev, AV (1983). The methods of collection Iran. Nature Museum and World Wild of and elaboration of fish parasitic monogenean Iran. P: 377 (in Persian). material. Leningrad, Nauka. P: 48 (in Rus- Ali, NM; Al-Jafary, AR and Abdul-Ameer, KN sian). (1987). Parasitic fauna of freshwater fishes in Jalali, B (1998). Parasites and parasitic diseases Diyala river, Iraq. J. Bio. Sci. Res., 18: 163- of fresh water fishes of Iran. Fisheries Co. of 181. Iran. P: 564 (in Persian). Amin, OM; Abdullah, SMA and Mhaisen, T Jalali, B and Barzegar, M (2006). Fish parasites (2003). Neoechinorhynchus zabensis sp. n. in Zarivar Lake. J. Agric. Sci. Techno., 8: 47- (Acanthocephala: Neoechinorhynchidae) 59.

269

Iranian Journal of Veterinary Research, Shiraz University, Vol. 12, No. 3, Ser. No. 36, 2011

Jalali, B; Papp, M and Molnar, K (1995). Four Asadollah, S and Jalali, B (2007). First record new Dactylogyrus species (Monogenea: Dac- of Myxobolus spp (Myxosporea: Myxoboli- tylogyridae) from Iranian fishes. Folia Parasi- dae) from fishes of Zayandeh-Rud river (Es- tol., 42: 97-101. fahan) and description of M. varicorhini as Jalali, B; Shamsi, Sh and Barzegar, M (2005). new species in Iran. Iranian J. Fish Sci., 7: Occurrence of Gyrodactylus spp (Monoge- 89-100. nea: Gyrodactylidae) from Iranian freshwater Mehdipoor, M; Barzegar, M and Jalali, B (2004). fishes. Iranian J. Fish Sci., 4: 19-30. A survey on monogenean parasites of gills of Jalali, B; Shamsi, Sh and Molnar, K (2000). New fishes in Zayandeh-Rud river. Iranian J. Vet. Dactylogyrus species (Monogenea: Dactylo- Sci., 2: 19-28 (in Persian). gyridae) from cyprinid fishes of Bahu-Kalat Moravec, F (1994). Parasitic nematode of fresh- river in southeastern, Iran. Acta Parasitol., 45: water fishes of Europe. The Netherlands, 289-294. Kluwer Academic Publishers. P: 473. Kennedy, CR (1975). The natural history of Spla- Paperna, I (1961). Studies on monogenetic tre- ton ley nature reserve VIII. The parasites of matodes in occupied Palestine. 3. Monoge- fish, with special reference to their use of in- netic trematodes of the Cyprinidae and Cla- formation about the aquatic community. Fld. ridae of the lake of Galilee. Bull. Fish Cull. Stud., 4: 177-189. Israel. Bamidgeh. 13: 14-29. Masoumian, M; Barzegar, M; Mehdipoor, M;

270