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Acta Ichtiologica Romanica SUCCESSIONS OF THE ICHTHYOFAUNA IN AN EUTROPHIC SERBIAN RESERVOIR Goran MARKOVIC, Mirjana LENHARDT and Zoran GACIC KEYWORDS: Danube Basin, Serbia, Gruža Reservoir, ichthyofauna, non-native species, changes. ABSTRACT Anthropogenic activities, primarily the intensification of eutrophication and introduction of new species, often affect crucially the qualitative and quantitative structure of the ichthyofauna of a reservoir. This study presents basic characteristics of the ichtyofauna of the eutrophic reservoir constructed in 1984 on the Gruža River (the Danube Basin, Serbia). The results on the icthyological investigations conducted in 2004-2005 suggested the presence of 19 species of 6 families, being dominated by representatives of the Cyprinidiae family (accounting for 80.95% of the total number of individuals and 74.41% of the biomass of the icthyofauna). Great changes have been observed during the two decades of the ecosystem existence. REZUMAT: Succesiunea ihtiofaunei într-un bazin din Serbia. Activităţile antropice, în primul rând Rezultatele investigaţiilor ihtiologice intensificarea eutrofizării şi introducerea de realizate în 2004 - 2005 suggerează prezenţa noi specii, afectează adesea crucial structura a 19 specii din 6 familii, fiind dominate de calitativă şi cantitativă a ihtiofaunei unui reprezentanţi ai familiei Cyprinidiae bazin. (însumând 80.95% din totalul numărului de Acest studiu prezintă caracteristicile indivizi şi 74.41% din biomasa ihtiofaunei). de bază a ihtiofaunei unui bazin eutrofizat Modificări mari au fost observate de-a construit în 1984 pe râul Gruža (Bazinul lungul a două decade de existenţă a Dunării, Serbia). ecosistemului. ZUSSAMENFASUNG/RESUMEN/RESUME: Die Ichtiophauna Succesion in einem Basin aus Serbia. Anthropogenic Tätigkeiten, Die Ergebnisse auf den icthyological hauptsächlich die Verstärkung von Untersuchungen geleitet in 2004-2005 hat eutrophication und Einführung neuer die Anwesenheit von 19 Spezies von 6 Spezies, beeinflusst oft entscheidend die Familien vorgeschlagen, beherrscht durch qualitative und quantitative Struktur des Vertreter die der Familie Cyprinidiae ichthyofauna von einem Behälter. (80,95% von der gesamten Zahl von Dieses Studium überreicht Individuen und 74,41% von der Biomasse grundlegende Kennzeichen des ichtyofauna des icthyofauna zu werden erklärend). vom eutrophic Behälter gebaut in 1984 auf Große Änderungen sind während der zwei dem Gruža Fluss (dem Donau Becken, Jahrzehnte von der Ökosystemexistenz Serbien). beobachtet worden. Successions of the ichthyofauna in an eutrophic Serbian reservoir; -1- Acta Ichtiol. Roman. . INTRODUCTION Damming rivers and the construction of reservoirs or man-made lakes are unique phenomena in nature. The conversion of running water ecosystems into poorly running or standing water ecosystems induces drastic changes in exposed hydrobiont communities. Eutrophication is intensified by the inflow of nutrient salts, phosphate and nitrate, as well as by the prolongation of the lake basin retention time (Hutchinson 1967). Most Serbian reservoirs have exhibited signs of eutrophication (Bogdanović 2006, Karadžić and Mijović 2007). Consequently, fish communities undergo substantial changes in these biotopes. Some species adapt rapidly and increase in abundance under the newly emerged conditions, others disappear (Lenhardt et al. 2008). The Gruža reservoir (43054’35’’ 0 ’ ’’ 43 57 51 N, 20037’35’’ – 200 41’50’’E) was created in 1984 by damming of the middle course of the Gruža River, a tributary of the Zapadna Morava River (Danube Basin, Serbia) (Figure 1). The reservoir was built to supply water to the City of Kragujevac (180,000 inhabitants). The lake has a surface area of 9.34km2, a length of 10 km, a maximum width of 1.5 km, a maximum depth of 31 m and water-level fluctuations of 3-5 m. The total volume of the reservoir is 64 x 106m3. The Gruža Reservoir has a drainage basin of 318 km2. The reservoir is characterized by a low flow rate (1 m3sec-1)(Ostojić et al. 2005). There are no water inflows from the main river and MATERIALS AND METHODS The ichthyological research was conducted in the studied area (Fig. 1) during spring (April-May) and summer (JulyAugust) in 2004-2005. The fish were caught using standard fishing gear – nets, 30 – 100m long, 1 to 5m wide, having different mesh size ranging from 10 to 75mm. The samples were determined by standard methods (Banarescu 1964, Wheeler 1978, -2- tributaries into the reservoir during the summer months of drought years. Intensive agriculture in the riparian areas induces a high nutrient inflow causing overeutrophication and accompanying consequences, such as «blooms» of Cyanobacteriophyta. This process is facilitated by the low depth and low amount of water, as well as by minimum movement. Water quality deteriorates due to continuous faecal pollution, particularly with the Clostridium perfrigens species (Ćurčić and Čomić 2002). The sediment of the shallow parts of the lake is heterogeneous, consisting of loam, clay, sand and plant detritus. The deeper parts of the lake have a silty bottom and a higher amount of detritus, being generally derived from plants. Apart from the developed macrophyte vegetation (Topuzović and Pavlović 2004), the biota of the ecosystem include a diverse zooplankton community composed of 99 species (Ostojić 2000) and a macrozoobenthos community comprising 32 species being dominated by Oligochaeta and Chironomidae (Simić 2005). The lake is marked by an occasional oxygen deficiency in deeper parts. There have been several records of the reservoir water being loaded with nitrites, ammonia and pesticides (Ostojic et al. 2007). Despite the above limitations, the general environmental conditions in the area enable the development of a diverse fish community, making the Gruža Reservoir the major recreational fishing area in Central Serbia (Simović and Marković 2005). Ladiges und Vogt 1979, Simonović 2006). The diversity of the fish community was used to calculate Margalef (Margalef 1958) and Shannon-Weiner indices (Krebs 1994). The results obtained in this study were compared to previous ones (Simović 1995 and 2001, Simović and Marković 1996 and 2005, Šorić 1996). G. Markovic, M. Lenhardt and Z. Gacic Acta Ichtiologica Romanica Figure 1: Studied area localization. Successions of the ichthyofauna in an eutrophic Serbian reservoir; -3- Acta Ichtiol. Roman. . RESULTS During the ichthyological investigations conducted in 2004-2005, a total of 1926 fish samples having a total weight of 379,160 kg were caught. The fish belonged to 19 species and 6 families (Cyprinidae, Siluridae, Esocidae, Percidae, Centrarchidae and Ictaluridae) (Table 1). The representatives of the family Cyprinidae predominated both in terms of the total number of individuals (80.95%) and biomass (74.41%) (Figure 2). The reservoir was inhabited by 6 allochthonous species. The high occurrence of Carassius gibelio (28.35% of individuals and 43.29 % of the total biomass of ichthyofauna) contributed to the significant proportion of allochthonous species in the total number (39.97%) and biomass (45.32%) of the icthyofauna. Table 1: Qualitative and quantitative composition of the Gruža reservoir ichthyofauna: * non-native (allochthonous) species. Fam. Number % Biomass % (g) CYPRINIDAE Alburnus alburnus 357 18.54 4900 1.29 Abramis brama 185 9.61 11750 3.10 Aspius aspius 5 0.26 3950 1.04 Carassius gibelio* 546 28.35 164120 43.29 Chondrostoma nasus 11 0.57 3200 0.84 Cyprinus carpio 77 4.00 71200 18.78 Ctenopharyngodon idella* 1 0.05 470 0.12 Hypophthalmichtys molitrix * 2 0.10 950 0.25 Leuciscus cephalus 16 0.83 3250 0.86 Pseudorasbora parva* 137 7.11 2800 0.74 Rhodeus sericeus 54 2.80 350 0.09 Rutilus rutilus 168 8.72 15200 4.01 SILURIDAE Silurus glanis 48 2.49 59800 15.77 ESOCIDAE Esox lucius 16 0.83 17100 4.51 PERCIDAE Perca fluviatilis 180 9.35 14000 3.70 Acerina cernua 13 0.67 320 0.08 Sander lucioperca 26 1.35 2300 0.61 Fam. CENTRARCHIDAE Lepomis gibbosus* 47 2.44 380 0.10 Fam. ICTALURIDAE Ictalurus nebulosus* 37 1.92 3120 0.82 TOTAL 1926 100 379160 100 -4- G. Markovic, M. Lenhardt and Z. Gacic Acta Ichtiologica Romanica Figure 2: Proportion of fish families (number of individuals) in the ichthyofauna of the Gruža reservoir (%). Figure 2: Proportion of fish families (biomass) in the ichthyofauna of the Gruža reservoir (%). Successions of the ichthyofauna in an eutrophic Serbian reservoir; -5- Acta Ichtiol. Roman. . DISCUSSIONS The first ichthyological investigations of the Gruža reservoir were conducted in 1987. The reservoir was inhabited by 16 species of 6 families. The fish community in the first period of the lake existence was comprised of, among others, lothic species such as Barbus peloponnesius, Alburnoides bipunctatus, Gobio gobio, Sabanejewa aurata balcanica and Barbatula barbatula (Table 2). Among the non-native species found in the reservoir, a massive abundance of C. gibellio and the presence of individual specimens of Lepomis gibbosus were reported (Šorić 1996). Table 2: Qualitative composition of the Gruža reservoir ichthyofauna (1987-2005); * non-native (allochthonous) species Period Taxon Family Cyprinidae Alburnus alburnus (Linnaeus, 1758) Alburnoides bipunctatus (Bloch, 1782) Abramis brama (Linnaeus, 1758) Abramis sapa (Pallas, 1811) Aspius aspius (Linnaeus, 1758) Barbus peloponnesius (Valenciennes,1844) Carassius auratus gibelio (Bloch, 1783)* Chondrostoma nasus (Linnaeus, 1758) Ctenopharyngodon idella (Valenciennes,1844)* Cyprinus carpio (Linnaeus, 1758) Gobio gobio (Linnaeus, 1758) Hypophthalmichthys molitrixis (Valenciennes, 1844)* Leuciscus cephalus (Linnaeus, 1758) Phoxinus phoxinus (Linnaeus, 1758) Pseudorasbora parva (Schlegel, 1842)* Rhodeus sericeus amarus (Bloch, 1782) Rutilus rutilus (Linnaeus, 1758) -6- 1987 1991 1995 1998-1999 2004-2005 + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + G. Markovic, M. Lenhardt and Z. Gacic Acta Ichtiologica Romanica Period Taxon Family Cobitidae Barbatula barbatula (Linnaeus, 1758) Sabanejewa aurata balcanica (Karaman, 1922) Family Esocidae Esox lucius (Linnaeus, 1758) Family Siluridae Silurus glanis (Linnaeus, 1758) Family Percidae Perca fluviatilis (Linnaeus, 1758) Acerina cernua (Linnaeus, 1758) Sander lucioperca (Linnaeus, 1758) Family Centrarchidae Lepomis gibbossus (Linnaeus, 1758) * Family Ictaluridae Ictalurus nebulosus (Lesueu, 1819) * Number of species 1987 1991 1995 1998-1999 2004-2005 + + + + + + + + + + + + + + + + + + + + 16 The location of the reservoir and a high nutrient inflow from surrounding agricultural land induced rapid eutrophication of the ecosystem and high bioproductivity of the ichthyofauna. However, a huge fishkill caused by the Branchiomyces sanguinus fungus occurred on 5 April 1988, involving particularly the carp (Cyprinus carpio) population. The emptied ecological niche was filled by C. gibelio, a predominant species in the ecosystem since the date (Simović 2001). 14 15 18 19 Later studies (1991-1995) showed evidence of recovery of the icthyofauna, but also of significant changes in the fish structure – the disappearance of a number of rheophilic species and a pronounced dominance of stagnophilic species. The predator species Esox lucius was not reported in the 1995 fish catches, which most likely contributed to a massive increase in «trash» fish abundance. A total of 15 species representing 5 families were reported for the ichthyofauna, being dominated by C. gibelio which accounted for 61.35 % and 75.30% of the total number and biomass of the ichthyofauna, Successions of the ichthyofauna in an eutrophic Serbian reservoir; -7- Acta Ichtiol. Roman. . respectively (Simović 1995). The first record of the occurrence of Pseudorasbora parva (Simović and Marković 1996), an allochthonous species widely distributed in Serbian watercourses ((Maletin 1997, Cakić et al. 2004) was reported. Studies conducted in 1998-1999 showed an increase in species diversity. The ichthyofauna comprised 18 species of 5 families, being dominated by Cyprinidae representatives (84.3 % of the total number of individuals and 74.68% of the biomass of the ichthyofauna). The allochthonous ichthyofauna was enriched with Asian herbivores Ctenopharyngodon idella and Hypophthalmichthys molitrix, which were introduced into the reservoir to reduce the development of macrophytes and planktons. Apart from the marked dominance of C. gibelio (26.42% of the total number of individuals and 36.83% of the biomass of the ichthyofauna), a increase in C. carpio (4.50 % of individuals and 21.09 % of biomass) abundance was another consequence of fish stocking. Interestingly, the reservoir was not inhabited by tench (Tinca tinca), unlike a number of reservoirs in Central Serbia, irrespective of the relatively favourable conditions of the ecosystem for its survival. Table 3: Temporal variation in the diversity of the fish assemblage of the Gruža reservoir. Years 1995 1998 - 1999 2004 - 2005 Diversity index Margalef 2.3537 2.2829 2.5121 Shannon-Weiner 0.9504 1.8941 1.8004 (biomass) Shannon-Weiner 1.1482 2.1824 2.2306 (total number) The results presented in this paper suggest the increased species diversity of the reservoir ichthyofauna (Table 3), being enhanced by the planned introduction of the predatory Sander lucioperca species into the ecosystem in 2002 aimed at restraining the production of «trash» species, as well as by the unplanned introduction of Ictalurus nebulosus. The high proportion of C. carpio and Silurus glanis in the fish productivity of the reservoir is due to fish stocking, successfull acclimatization and, also, selectivity of the fishing tools used (use of nets of larger mesh size). CONCLUSIONS The Gruža Reservoir on the Gruža river (the Danube Basin, Serbia) shows characteristics of lowland reservoirs and a high degree of eutrophication favouring the development of stagnophilous species. The ichthyofauna of this ecosystem is composed of 19 species of 6 families, dominated by Cyprinidae. The excessive increase in the -8- Continuous nutrient inflows and a high primary production of plankton and macrophytes facilitate the development of the reservoir fish community. The minimum flow rate favours the development of stagnophilous species, which are, therefore, pronouncedly dominant, occasionally tending to proliferate in mass numbers. It is generally recognized that a large amount of fish excrement may significantly enhance eutrophication of ecosystems (Horppila and Kairesalo 1992). The abundance of the ichthyofauna representatives and their physiologial activity, coupled with the above factors, most likely lead to more rapid ageing of this relatively young reservoir. abundance of C. gibelio leads to a high proportion of allochthonous fish species. Anthropogenic activities have affected the ichthyofauna structure of this reservoir characterized by a low flow rate and overproductivity of herbivorous and planktofagous species. G. Markovic, M. Lenhardt and Z. Gacic Acta Ichtiologica Romanica AKNOWLEDGEMENTS This study has been completely supported by the Ministry of Science, of the REFERENCES Banarescu P., - Fauna Republicii Populare Romine, Pisces – Osteichthyes. Academia Republicii Populare Romine, Bucaresti, 959 pp, 1964. Bogdanović D., - The role of phosphorus in eutrophication. Proc. Nat. Sci. Matica Srpska, 110: 75-85, 2006. Cakić P., Lenhardt M., Kolarević J., Mićković B., Hegediš A., Distribution of the Asiatic cyprinid Pseudorasbora parva in Serbia and Montenegro. J. Fish Biol., 65(5): 1431-1434, 2004. Horppila J., Kairesalo T., - Impact of bleak (Alburnus alburnus) and roach (Rutilus rutilus) on water quality, sedimentation and internal nutrient loading. Hydrobiologia, 243/244: 323-331, 1992. Hutchinson G.E., - A treatise on limnology. Vol.II – Intoduction to lake biology and the limnoplankton. John Wiley & Sons, Inc., New York, 1048 pp, 1967. Ćurčić,S., Čomić,Lj., - A microbiological index in estimation of surface water quality. Hydrobiologia, 489: 219222, 2002. Karadžić B., Mijović A., - Environment in Serbia: an indicator – based review. Serbia Environmental Protection Agency, CICERO, Belgrade, 160 pp, 2007. Krebs C.J., - Ecology: The Experimental Analysis of Distribution and Abundance. 4th Edit., Harper Collings College Publishers, 801 pp, 1994. Ladiges W., Vogt D., - Die Süsswasserfishe Europas bis zum Ural und Kaspischen Meer. Paul Parey, Hamburg und Berlin, 299 pp, 1979. Lenhardt M., Markovic G., Gacic Z., Decline in the Index of Biotic Integrity of the Fish Assemblage as a Response to Reservoir Aging. Water Republic of Serbia, through the Grant No. 20107. Resour.Manage.,doi 10.1007/s11269-008-9348-3, 2008. Maletin S., Djukić N., Miljanović B., Ivanc B., - Status of allochthonous ichthyofauna of Pannonian basin in Yugoslavia. Ekologija, 32: 87-98, 1997. Margalef F., - Information theory in Ecology. Gen.Syst., 3:36-71, 1958. Ostojić A., - Contribution to knowledge on the zooplankton of Serbia – Faunistic composition in the Gruza reservoir. Arch.Biol.Sci., 52(1): 47-52, 2000. Ostojić A., Ćurčić S., Čomić Lj.,Topuzović,M., - Estimation of the Eutrophication Process in the Gruža Reservoir (Serbia nd Montenegro). Acta hydrochim.hydrobiol., 33 (6): 1-9, 2005. Ostojić A., Ćurčić S., Čomić Lj.,Topuzović M., - Effects of anthropogenic influences on the trophic status of two water supply reservoirs in Serbia. Lakes & Reservoirs: Res. & Manage., 12 (3): 175-185, 2007. Simić V., - Environmental characteristics of macrozoobenthos in the Gruža reservoir In: Čomić,Lj., Ostojić,A. (eds.). Monograph “Gruža Reservoir“, 99-111, (in Serbian), 2005. Topuzović M., Pavlović D., - Physical organization of two reservoirs in Serbia as a crucial factor in development of their hydrophilic flora: a comparative study. Hydrobiologia, 525: 239-245, 2004. Simonović P., - The Fishes of Serbia, 2nd edition. NNK International, School of Biology, Belgrade, 247 pp., 2006. Simović S., - The fish community of the Gruža reservoir. 1995 Conference on Yugoslav Fisheries, Kotor, 141-145, (in Serbian), 1995. Successions of the ichthyofauna in an eutrophic Serbian reservoir; - 145 - HABITATS DIRECTIVE URGENCY ORDER NR. 57 SPECIES ANNEXES Acta Ichtiol. Roman. AUTHORS’S PROPOSAL Acipenser gueldenstaedtii V IV IV Acipenser nudiventris V V Acipenser ruthenus V Simović S., Marković G., The ichtyofauna V Acipenser stellatus V of the Gruža reservoir. IV Acipenser sturio II, IV 27P-28P, V Alosa immaculata Arch.Biol.Sci., II, 48(3-4): V V 1996. Alosa tanaica II, V II (only for Finnish Aspius aspius II, V Simović S., - Ecology and cenotic relationships between populations). the speciesFor the others, No. Rutilus rutilus L. and Carassius Barbus barbus V auratus gibelio Bloch in Nothe Carassius carassius Medjuvršje and Gruža reservoir. PH. Chalcalburnus chalcoides II IV D. thesis, Faculty of Biology, No Cobitis danubialis Belgrade, 149 pp,II (in Serbian), 2001. II Eudontomyzon mariae II Simović S., Marković G., - Autochthonous IV Gobio albipinnatus II and allochthonous fish Gobio kesslerii II species in theIV community of the Gruža reservoir. IV Gymnocephalus baloni II, IV Gymnocephalus schraetser II, V IV V Huso huso V Lota lota Mesogobius batrachocephalus V Misgurnus fossilis II Neogobius eurycephalus Neogobius syrman Pelecus cultratus Percarina demidoffii II, V No Petroleuciscus borysthenicus Proterorhinus marmoratus Rhodeus amarus Sabanejewia bulgarica Sander volgensis Umbra krameri Zingel streber Zingel zingel ANNEXES . Morava (Danube Basin) I. The reproductive potential of the species 5A Leuciscus Nocephalus, Alburnus 4B 4B alburnus and Rutilus rutilus. 3 4A Ichthyologia, 28(1): 1-14 (in 3 No Serbian), 1996. 3 3 Wheeler A., - Key to the Fishes of Northern 3 4A Ltd, London, 380 3 Europe. Warner 4A pp, 1978. 3, 4A 4A 3 5A 4B 5B 3 5B 4A 5A AUTHORS: 4B 4B 5A MARKOVIĆ Goran 5B Faculty of Agronomy, 4B Cara Dušana 34, No 32000 Čačak, Serbia II II II, V No IV II IV IV 5B 3 4B 4B II II AUTHORS’S PROPOSAL 4A 5A 5A 4A 5A 5A Čomić,Lj., Ostojić,A.(eds.) 5A In: 5A “Gruža Reservoir“, 1375A Monograph 4A 151 (in Serbian), 3, 5A 5A 2005. Šoric V., - The ichthyofauna of the Gruža 3, 5A 5A 3 river, a tributary No of the Zapadna 4B 3 3 4B 4B 4B LENHARDT Mirjana InstituteNo for Biological Research, Bulevar No Despota Stefana 142, 4A11000 Belgrade, Serbia 4B GAČIĆ Zoran 3 3 3Institute for Multidisciplinary 4A Research, 3, 4A, 5A 4A Kneza Višeslava 1, 11000 Belgrade, Serbia - 146 - G. Markovic, M. Lenhardt and Z. Gacic