FAUNA OF MONOGENEAN TREMATODS - PARASITES IN BLEAK Alburnus alburnus belvica Karaman, 1924 (PISCES: CYPRINIDAE) FROM THE LAKE PRESPA (MACEDONIA)
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1 FAUNA OF MONOGENEAN TREMATODS - PARASITES IN BLEAK Alburnus alburnus belvica Karaman, 1924 (PISCES: CYPRINIDAE) FROM THE LAKE PRESPA (MACEDONIA) Stojmir STOJANOVSKI 1, Nikola HRISTOVSKI 2, Predrag CAKI] 3, Mi{o HRISTOVSKI 4 & R. A. BAKER 5 1. Hydrobiological Institute, Ohrid, R. Macedonia; 2. Faculty of Biotechnical Sciences, Bitola, R. Macedonia; 3. Institute of Biological Researches, Belgrade, Serbia and Montenegro; 4. Faculty of Veterinary Medicine, Skopje, R. Macedonia; 5. School of Biology, University of Leeds, UK ABSTRACT Stojanovski S., Hristovski N., Caki} P., Hristovski M. & Baker R.A. (2004). Fauna of monogenean trematods - parasites in bleak Alburnus alburnus belvica Karaman, 1924 (pisces: Cyprinidae) from the Lake Prespa (Macedonia). Proceedings of the 2 nd Congress of Ecologists of the Republic of Macedonia with International Participation, , Ohrid. Special issues of Macedonian Ecological Society, Vol. 6, Skopje. During the parasitological investigations on the fishes from the Lake Prespa (Macedonia), in bleak (Alburnus alburnus belvica Karaman, 1924) are found 4 species of the class Monogenea: Dactylogyrus alatus f. typica, Dactylogyrus minor, Diplozoon paradoxum and Paradiplozoon alburni. Totally are examined 174 fish specimens, of which 72 specimens (41,38%) are infested. Prevalence is the highest with Dactylogyrus alatus f. typica (22,41% of the total number of examined bleaks are infested), then Dactylogyrus minor (17,24%), then Diplozoon paradoxum and Paradiplozoon alburni (3,45% each one). The average intensity of infestation is the highest in the cases of infestation with: Dactylogyrus minor (5,0), then Dactylogyrus alatus f. typica (3,77), then Diplozoon paradoxum and Paradiplozoon alburni (1 each one). The greatest pathological influence is associated with the monogeneans Diplozoon paradoxum and Paradiplozoon alburni. All monogenean species represents the first record for the parasite fauna of fishes in Macedonia. Introduction The Lake Prespa is situated in south-western part of Macedonia. It is divided on 2 parts: Macro and Micro Prespa. It has an average depth of 18,74 m and the biggest is 54,2 m. The lake has several small rivers as tributaries. The water sinks at the abyss Zavir, in Small Prespa. According by its trophic state, it is on the bounder between oligotrophic and mesotrophic (Naumovski et al. 1997). The surface level of the lake is significantly decreased in the last decade, because of long-term dried period that leads to eutrophication. Thus, in 1992, comparing to the average, Lake Prespa water level was 4,15 m, and even 6,6 m lower in relation to the maximal level. The lake, which was formed in pliocen is old as Lake Ohrid and is rich with endemic species, from the low plants and invertebrates, as well as among the fishes. Monogenean trematods have a great importance in the fish pathology. Certain species cause very serious diseases of fishes, particularly in the young ones. A great number of monogenean species has very clear speciality to a respective host - fish or a narrow circle of related hosts. Monogenean trematods are presented in a vast number in the environment, because of their being ectoparasites, they are even more subject to changes of the physical-chemical characteristics of the aquatic habitat, which they have to adjust to. Monogenean trematods could be a sensitive indicator for the changes of the lake' ecosystems, because the data about their prevalence and intensity of infestation, together with the knowledge of the biology of parasites reveal on the health of the environment. Hristovski (1975), who found 9 species of helminths at fishes from Lake Prespa, carried out primarily investigations on the parasite fauna of the fishes. Further investigations were carried out by Hristovski and Stojanovski (1983, 1984, 1989, 1997, 2000, 2001). Dupont and Lambert (1986), investigating the fishes from Lake Mikro Prespa (Greece) found the followed dactylogyrid species: Dactylogyrus alatus, D. anchoratus, D. balkanicus n.sp., D. caucasicus, D. chondrostomi, D. crivellius n.sp., D. dyki, D. elegantis, D. erhardovae, D. ergensi, D. extensus, D. Proceedings of the 2 nd Congress of Ecologists of Macedonia 281
2 Stojmir STOJANOVSKI et al. Fig. 1. Photographic review of the Lake Prespa. folkmanovae, D. minor, D. prespensis n.sp.,, D. prostae, D. sphyrna and D. vistulae D. vistulae. During that, 3 species of dactylogyrids: D. balkanicus n.sp., D. crivellius n.sp. and D. prespensis n.sp. dyki in Barbus cyclolepis prespensis are new to the science generally. Materials and methods Fish material was sampled over several years, from the Macedonian part of Lake Prespa. Fishing was carried out by seasons, in the period from spring 2000 to spring Fishes were subjected to the routine methods of identification, dissection and observation (Hotenovsky 1985, Stojanovski 2003), during that is important the fact that fishes for investigations should be fresh. Cleaned parasites were separated and put in certain fixatives, prepared for determination with determined techniques of staining and clearing. For an identification of the parasite species we used the following keys: Bauer, (1985, 1987) and Hotenovsky (1985). The most successful preparations for every parasite species are photographed and displayed. Results and discussion The presence of 4 species of the class Monogenea is established: Dactylogyrus alatus f. typica (Fig. 2), Dactylogyrus minor (Fig. 3), Diplozoon paradoxum (Fig. 4) and Paradiplozoon alburni (Fig. 5). Bleak (Alburnus alburnus belvica Karaman, 1924) A total prevalence with monogeneans is 41,38 %, i.e. 72 infested fishes of 174 examined The mean intensity of infestation is 4,25. 4 monogenean species are found: Dactylogyrus alatus f. typica in 39 fishes (22,41 %), with intensity of infestation of 3,77; Dactylogyrus minor in 30 fishes (17,24%) with intensity of infestation of 5,0; Diplozoon paradoxum and Paradiplozoon alburni in 6 roaches each one (3,45 %) with intensity of infestation of 1,0 (Table 1). Results of determination of the Fulton's condition coeficient among infested and uninfested fishes from the Lake Prespa show that it is 0,95 at uninfested fishes, while at infested is 0,93. These data reveal the influence of monogenean trematods, and parasites in general, on the health and conditional state of fishes, and are confirmed by a great number of investigators in the world. The highest prevalence and intensity of infestation with monogeneans in the Lake Prespa' fishes occur Fig. 2-a.Dactylogyrus alatus f. typica - adhesive disk (original), x 360 Fig. 2-b.Dactylogyrus alatus f. typica - copulatory organ (original), x Zbornik na trudovi od 2-ot Kongres na ekolozite na Makedonija
3 Fig. 3-a.Dactylogyrus minor - adhesive disk (original), x 320 Fig. 3-b.Dactylogyrus minor - copulatory organ (original), x 340 during the spring (75,0 %) and summer (21,43 %), because of the spawning. This conclusion complies with the findings of Thomas (1964), who, likewise, holds the opinion that maximum prevalence and intensity of parasites occur in the course of a vernal period. Alongside that, he emphasizes 3 factors because of which the female trout are physiologically less resistant to parasites during the spawning period: weaker condition, stress and disruption in the production of estrogen. Also, after the winter period, which is a latent period, the vernal period provides better conditions for development and reproduction of the parasites, which is mainly why they increase in number (Tab. 1). The greatest pathological influence is associated with the monogeneans Diplozoon paradoxum and Paradiplozoon alburni. But, other monogenean trematods too, when are met in enough number, act negatively on the health and condition of fish. The monogenean fauna of fishes from the Lake Prespa is in common with that of the fishes of corresponding families from the Balkan Peninsula and more widely (Bauer, 1985; Bihovskaya-Pavlovskaya et al. 1962; Vasiljkov 1983; Dupont and Lambert 1986; Kaka~eva-Avramova 1983; Nedeva-Menkova 1991, 1999; Caki} 1992; Ergens 1960; 1970; Ki{karoly 1982, 1987; Ki{karoly and Tafro 1988; Stojanovski 1997, 2003). All monogenean species mentioned in this paper represent the first record for the fishes from Macedonia. a) b) Fig. 4-a.Diplozoon paradoxum - clapms (original), x 200 Fig. 4-b.Diplozoon paradoxum - egg (original), x 160 c) Fig. 4-c. Diplozoon paradoxum - widening of the middle part (original), x 63 Proceedings of the 2nd Congress of Ecologists of Macedonia 283
4 Stojmir STOJANOVSKI et al. Fig. 5-a.Paradiplozoon alburni - clamps (original), x 160 Fig. 5-b.Paradiplozoon alburni - clamps (original), x 280 Tab. 1. Prevalence and intensity of infestation with monogenean trematods in bleak (Alburnus alburnus belvica Karaman, 1924) from the Lake Prespa. Tab. 1. Ekstenzitet i intenzitet na infestacija so monogeni trematodi kaj nivi~kata (Alburnus alburnus belvica Karaman, 1924) od Prespanskoto Ezero. 284 Zbornik na trudovi od 2-ot Kongres na ekolozite na Makedonija
5 Literature Bauer, O. N Opredelitelj parazitov presnovodnih ryb fauni SSSR. Tom II (Paraziti~eskie mnogokleto~nie. Pervaja ~ast). Akademia Nauk SSSR. Izdateljstvo Nauka, Leningrad. pp ; 33-34; 52-53; 86-89; ; Caki}, P., 1992: Paraziti riba u vodama Sjeni~ko- Pe{terske visoravni i mogu}nosti njihovog suzbijanja. Doktorska disertacija. Veterinarski fakultet Univerziteta u Beogradu. Katedra za parazitologiju. Dupont F., Lambert A., 1986: Etude des communautes de Monogenes Dactylogyridae parasites des Cyprinidae du Lac Mikri Prespa (Nord de la Grece). Description de trois nouvelles especes chez un Barbus endemique: Barbus cyclolepis prespensis Karaman, Ann. Parasitol. Hum. Comp.; 61 (6): Ergens R., 1960: Helmintofauna nekotoryh ryb Albanii. ^eskosl. parasitologie; VII: Ergens R., 1970: Parazitofauna ryb iz territorii ^ernogorii. I. Polyonchoinea (Monogenoidea) nekotoryh ryb Skadarskogo Ozera i Bolj{ogo^ernogo Ozera. Poljoprivreda i {umarstvo; XVI (1-2): HotenovskiŸ I.A., 1985: Fauna SSSR. Monogenei (podotred Octomacrinea Khotenovsky). Akademia Nauk SSSR. IzdatelÍstvo Nauka, Leningrad. pp Hristovski, N. D Fauna endohelminata riba u jezerima SR Makedonije. Doktorska disertacija. Prirodno - matemati~ki fakultet, Novi Sad. Hristovski, N., 1975: Endohelminti ciprinidnih riba Prespanskog jezera. Magistarski rad. Prirodno - matemati~ki fakultet, Novi Sad. Hristovski, N., 1984: Karakteristike faune endohelminata riba Prespanskog jezera. III Kongres ekologa Jugoslavije. Radovi i rezimea. Sarajevo: pp Hristovski, N., Stojanovski, S., 1997: Dinamika na endohelmintite na ciprinidnite ribi od Prespanskoto Ezero. Me unaroden Simpozium kon integralna za{tita i odr`iv razvoj na transgrani~nite ezera: Golema i Mala Prespa. Kor~a, Albanija, pp Hristovski N., Jovanovska M., Stojanovski S., 2000: Pregled na dosega utvrdenite paraziti vo Prespa. Me unaroden simpozium: Odr`liv razvoj na Prespanskiot region. Zbornik na trudovi. Ote{evo. pp Hristovski N., Stojanovski S., Cakic P., Hristovski M., 2001: Parasite fauna of the common carp (Cyprinus carpio Linnaeus, 1758) from the Prespa Lake, Macedonia. Journal of Animal Sciences; 5: Bulgaria. Kaka~eva-Avramova D., 1983: Helminti na slatkovodnite ribi v Bulgaria. Izdatelstvo na Bulgarskata AkademiÔ na Naukite, SofiÔ. pp ; 74-75; 76-77; Ki{karoly M., 1982: Istra`ivanje parazitofaune slatkovodnih ribnjaka Bosne i Hercegovine. Monogeni Trematodi 4. Veterinaria; 31(1-2): Ki{karoly, M., 1987: Istra`ivanje parazitofaune slatkovodnih ribnjaka Bosne i Hercegovine. Monogeni Trematodi 5. Veterinaria; 36 (3-4): Ki{karoly M., Tafro A., 1988: Prilog poznavanju helmintofaune nekih riba jednog dijela Dunava. Veterinaria; 37 (2-3): Naumovski T., Novevska V., Lokoska L., Miti} V., 1997: Trofic state of Prespa Lake. International Symposium: Towards Integrated Conservation and Sustainable Development of Transboundry Macro and Micro Prespa Lakes. Proceedings.. pp Nedeva-Lebenova I., 1991: Morfologia, fauna i ekologia na helminti na ribi ot jazovir P~elina. Doktorska disertacia. Bugarska Akademia na Naukite. Institut po Parazitologia, Sofia. Nedeva I, Babacheva T., 1999: New Bulgarian fauna species belonging to Monogenea (Van Beneden, 1858) Bychowsky, Experimental pathology and parasitology. 3: Stojanovski, S Ekto i endoparaziti riba Ohridskog jezera. Magistarska teza. Veterinarski fakultet, Beograd. S. Stojanovski, 2003: Fauna na monogenite trematodi - paraziti kaj ribite od prirodnite ezera vo Makedonija. Doktorska disertacija. Fakultet za veterinarna medicina. Skopje. Thomas J.D., 1964: A comparation between the helminth burden of male and female brown trout Salmo trutta L. from natural population in the River Teify, West Wales. Parasitology; 54: Vasiljkov, G. V., 1983: Gelmintozi ryb. Izdateljstvo Kolos, Moskva. pp Proceedings of the 2 nd Congress of Ecologists of Macedonia 285
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