The Role of the European Bitterling (Rhodeus Amarus, Cyprinidae) in Parasite Accumulation and Transmission in Riverine Ecosystems
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Aquat Ecol (2011) 45:377–387 DOI 10.1007/s10452-011-9361-0 The role of the European bitterling (Rhodeus amarus, Cyprinidae) in parasite accumulation and transmission in riverine ecosystems Martina Da´vidova´ • Radim Blazˇek • Teodora Trichkova • Emmanuil Koutrakis • O¨ zcan Gaygusuz • Ertan Ercan • Marke´ta Ondracˇkova´ Received: 23 December 2010 / Accepted: 30 May 2011 / Published online: 17 June 2011 Ó Springer Science+Business Media B.V. 2011 Abstract In aquatic ecosystems, fish play a key role showed significantly higher proportions of allogenic in parasite accumulation and transmission to preda- parasites in comparison with autogenic. The sup- cious animals. In the present study, realized on seven posed co-occurrence of parasite species with identical populations of a small cyprinid fish species, the final host groups showed only a weak association. European bitterling Rhodeus amarus, we investigated The adjacent reservoir areas were a significant (1) the role of the European bitterling as a potential determinant of both the total and infracommunity intermediate or paratenic host, (2) the ability of the parasite species richness and for the mean parasite fish to accumulate parasites with similar final host abundance. No relationship between the distance of group, and (3) its significance as a potential source of sampling site from the adjacent reservoir and parasite parasite infection in the ecosystem in respect to community characteristics was found. As a small- habitat characteristics. A total of 36 parasite species sized fish with a wide distribution range and high were recorded; 31 species (90% of all parasite local abundances, the European bitterling can repre- specimens) were classified as endoparasites. Most sent a natural prey for a wide range of piscivorous of the endoparasites were found in the larval life predators. Due to its susceptibility to the number of stage, using bitterling as an intermediate or paratenic larval endoparasites, this fish species may therefore host. In particular, parasite community structure fulfill the role as important transmitter of parasites to their final hosts. Handling Editor: Thomas Mehner. M. Da´vidova´ (&) Á R. Blazˇek Á M. Ondracˇkova´ E. Koutrakis Department of Botany and Zoology, Faculty of Science, Fisheries Research Institute, National Agricultural Masaryk University, Kotla´rˇska´ 2, 611 37 Brno, Research Foundation, Nea Peramos, 640 07 Kavala, Czech Republic Greece e-mail: [email protected] O¨ . Gaygusuz R. Blazˇek Á M. Ondracˇkova´ Faculty of Fisheries, Istanbul University, Ordu Cad. Institute of Vertebrate Biology v.v.i., Academy of No 200, Laleli, 34470 Istanbul, Turkey Sciences of the Czech Republic, Kveˇtna´ 8, 603 65 Brno, Czech Republic E. Ercan Faculty of Aquaculture and Fisheries Biology, University T. Trichkova of Mugla, 48000 Ko¨tekli, Turkey Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Gagarin str. 2, 1113 Sofia, Bulgaria 123 378 Aquat Ecol (2011) 45:377–387 Keywords European bitterling Á habits contribute significantly to the rate of parasite Freshwater habitat Á Metazoan parasites Á species accumulation in intermediate or paratenic Parasite transmission Á Intermediate host hosts (Valtonen and Gibson 1997; Morand et al. 2000; Johnson et al. 2004;Da´vidova´ et al. 2008 etc.). In the present study realized on a small cyprinid fish, the European bitterling (Rhodeus amarus Bloch), we investigated (1) the role of the European Introduction bitterling as a potential intermediate and/or paratenic host for metazoan parasites, (2) the ability of the fish Transmission and dispersal are two basic processes in to accumulate parasites with similar final host group, the life cycle of parasites, in which the fundamental and (3) its significance as a potential source of objective is to find a suitable host (Bush et al. 2001). parasite infection within the ecosystem in respect to Parasite life cycles show a variety of forms. habitat characteristics. While studies in marine eco- Throughout evolution, the original direct life cycles systems indicate that small-sized fishes figure as have become more complex, where intermediate intermediate or paratenic hosts for a wide range of hosts play an important role (Park et al. 2007; Poulin parasite species more frequently than larger species 2007). However, a number of parasites may employ (Zander 1998), as far as we know, similar observa- hosts in which development does not occur and that tions in freshwater systems have not yet been are not always obligatory for the completion of published. parasite life cycles. These paratenic hosts (transport hosts) are frequently used to bridge an ecological or trophic gap (Bush et al. 2001). Intermediate and Materials and methods paratenic hosts are probably the most important components of parasite transmission and dispersion. Study system The main advantages in using intermediate or paratenic hosts are the protection of certain parasite The European bitterling is a small ostracophillous stages from the external environment, the channeling (deposing its eggs in the cavity of bivalves) fish of the parasite toward the final host if the interme- species and the most common representative of the diate/paratenic host is a prey of the definitive host East Asian cyprinid subfamily Acheilognathinae in and, furthermore, the transmission of the same Europe (Holcˇ´ık 1999). This species is characterized genetic information to many different host individu- by enormous changes in its distribution and abun- als (Poulin 2007). Many trophically transmitted dance over time. Although the parasite fauna of the parasites have complex life cycles; they pass through European bitterling is relatively well known through at least one intermediate host before reproducing in its range of distribution (Gelnar et al. 1994; Kadlec their final host. In addition, the mobility of the host et al. 2003;Da´vidova´ et al. 2005, 2008), studies over its geographical range is responsible for the concerning parasites of bitterling around the Aegean dispersal of the parasites (Sousa and Grosholz 1991). Sea drainage area are still limited (Akmirza 2007). In aquatic ecosystems, fish play a key role in parasite transmission to predacious animals (Zander Host and parasite collection et al. 1993; Groenewold et al. 1996; Zander 1998; Zander et al. 1999; Zander 2005; Valtonen et al. Fish were sampled from seven locations in south- 2010). Small-sized fish figure as effective mediators eastern Europe (Turkey, Greece and Bulgaria). between these two levels, because birds and mam- R. amarus populations were collected in running mals that may feed on tiny planktonic copepods or waters (small rivers or streams) to minimize the small snails are rare (Zander 1998). The importance effect of habitat type on parasite communities. All of fish as paratenic host species has been confirmed in sampling sites were located within a maximum many ecological studies (Moravec et al. 1995; distance of 10 km from the adjacent reservoir Moravec et al. 1998; Ondracˇkova´ et al. 2009 etc.). (Table 1). Except for the Nestos River associated The external environment, host age, and feeding with the Toxotes Dam (Greece), the sampling sites 123 Aquat Ecol (2011) 45:377–387 Table 1 Characteristics of sampling sites and fish collected Sampling site Country Drainage Coordinates Adjacent reservoir Distance to Year Water Mean SL Mean W (surface area) reservoir temperature (mm) (g) range (°C) range Eski Riva Stream TU Black Sea N 41°0001600 E29°2600700 O¨ merli Dam (23.9 km2) 9.5 km 2008 15.1 43 (30–70) 2.1 (0.5–8.4) Ballica Stream TU Black Sea N 41°0000200 E29°2500800 O¨ merli Dam (23.9 km2) 7.8 km 2008 16.5 53 (39–64) 3.7 (1.1–7.4) Kurtkoy Stream TU Black Sea N 40°4202000 E30°1105700 Sapanca Lake (45 km2) 0.2 km 2008 15.7 41 (31–56) 1.5 (0.5–3.8) Masukiye Stream TU Black Sea N 40°4300100 E30°0802500 Sapanca Lake (45 km2) 0.8 km 2008 16.0 36 (25–53) 1.0 (0.3–2.9) Nestos River GR Aegean Sea N 41°0502400 E24°4602000 Toxotes Dam (0.25 km2) 0.1 km 2009 15.6 52 (40–65) 3.2 (1.4–6.5) Struma River BG Aegean Sea N 42°2903600 E23°5501700 Pchelina Dam (5.4 km2) 4.5 km 2009 14.2 46 (32–61) 2.3 (0.7–5.6) Iskar River BG Black Sea N 42°3201700 E23°2905800 Pasarel Dam (0.34 km2) 1.4 km 2009 14.0 48 (29–61) 2.8 (0.6–5.9) TU Turkey, GR Greece, BG Bulgaria, SL fish standard length, W fish weight fish characteristics are0.1 shown g) in were Table caudal fin) measured. and Sampling total1 body mm; site weight (W; measurement detailstransport. to the and excludes nearest Standard thespinal transaction length length prior towater (SL; of dissection to within the to the 24collected. h laboratory the Fish of and wereA nearest individually total transported killed of by 239 alivevaried adult between in individuals sampling of riverine during sites October from 2008reservoir. 14 and to 2009. Fish 16.5 Waterbility temperature were of collectedwere fish located by upstream migration the electrofishing between reservoirs with the a possi- river and nation (Ergens and Lom Analysis. In addition, theence keys contrast for parasiteequipped (DIC) determi- with and phase-contrast,Parasites Olympus differential were Digital identified interfer- into Image using ‘‘Canada’’ a balsamdehydrated light in (Ergens microscope gradual andcestodes alcohol were Lom series, stained and inglycerin–water ferric mounted solution. acetocarmine (IAC), cleared Preserved in clove digeneans oilPrior and and to nematodes species were identification, cleared acanthocephalansand in were in a a mixture ofture glycerin of and ammonium alcohol picrate (Nematoda). andthocephala, glycerin Digenea, (Monogenea) Cestoda, Crustacea),parasites in were preserved a in mix- 4%standard formaldehyde methods (Acan- (Ergens andfor Lom the presence of metazoan parasites according to 1987 calculated as theper percentage individual of fish host. sampling Frequencycommunity of sites richness occurrence as with was the numberparasites of parasite per species host (infectedsample; and mean non-infected); abundance infra- age as of the fish average infectedet number by al.