Prey Selection of Pseudorasbora parva (Temminck and Schlegel, 1846) in a Freshwater Ecosystem (Lake Eğirdir/Turkey)

Abstract

In the present study, food spectrum of the topmouth gudgeon, Pseudorasbora parva and it food preference to different prey species were investigated in Lake Eğirdir, Turkey. Fish specimens were collected in April, May, June, July and August (2010–2011). Diet analysis was carried out on 88 fish specimens. The benthic larvae of Chironomus sp., the corophiid amphipod Chelicorophium curvispinum and the zooplankter Nitocra hibernica were found to dominate food items. In addition, the fish consumed zooplankton (especially cladocera and copepoda), phytoplankton, annelida, malacostraca and insecta species. Unindentified eggs were also found in the stomachs. Phytoplankton, particularly Gomphonema (V = 0.255, X2 = 13.058, p < 0.01) sp. due to its abundance, was a significant component in the 8.0- to 8.9-cm length sized topmouth gudgeon with distinct preference to the cladocerans Daphnia cucullata (V = 0.191, X2 = 7.331, p < 0.01) and Bosmina longirostris (V = 0.228, X2 = 10.404, p < 0.01), annelids (V = 0.201, X2 = 8.105, p < 0.01) and Trichoptera larvae (V = 0.157, X2 = 4.963, p < 0.01) in 2010 food diet. In return, invasive species topmouth gudgeon is preferable to Cladoceran in the diet of other planktivorous fish (especially Anatolian endemics Aphanius anatoliae type) in Lake Eğirdir. High value of Shannon diversity index was determined in May (H′=1.80) and August (H′=1.70). Fullness index was highest in April, whereas feeding density was lowest in July. Schoener’s indices of diet overlap were estimated between different size classes and months for topmouth gudgeon. The high value of these indices (C = 0.87) indicates that the species principally feeds on the similar in the size classes >8 cm (8.0–8.9 cm, 9.0–9.9 cm, 10.0–10.9 cm, 11.0–11.9 cm).

1. Introduction

The topmouth gudgeon, Pseudorasbora parva (Temminck and Schlegel, 1846) (sub fam. Gobioninae) is a small cyprinid fish distributed in Japan, China, Korea, Hungary, Germany, Serbia, Austria, Greece, Poland, North Africa, Romania, Czech Republic, United Kingdom, Azerbaijan and Ukraine [1, 2, 3, 4, 5, 6, 7, 8, 9, 10]. It usually occupies a range of lotic and lentic habitats, including rivers, reservoirs, canals, ponds, shallow lakes and oxbows [11, 12, 13]. This species is one of the most effective invasive species to have been introduced into inland waters in Turkey for the past 30 years [14, 15, 16, 17, 18, 19, 20, 21, 22, 23]. Generally, the topmouth gudgeon is considered as an important predator on crustaceans, zooplankton, ostracods, molluscs, chironomid larvae, rotifers and benthic organisms. It also feeds on phytoplankton (diatoms and other algae), zooplankton (cladocerans, copepods), the larvae and eggs of native fish species, insects and detritus [7, 24, 25, 26]. Although there are some data available on its age, growth, reproduction and habitat [27, 28, 29, 30, 31, 32, 33], published information on the diet of topmouth gudgeon is still scarce.

Feeding habits and feeding ecology of topmouth gudgeon were studied by Wolfram-Wais et al. [4] in Neusiedler See (Austria) and Xie et al. [34] in the Biandangtang Lake of China. Hliwa et al. [35] studied the diet of the species in the Kis-Balaton Reservoir, whereas Nikolova et al. [36] investigated seasonal variation in the diet of topmouth gudgeon from shallow eutrophic lakes along River Vit in Bulgaria. Yalçin-Özdilek et al. [37] carried out research on the feeding ecology of the species from Gelingüllü Reservoir and Karakuş [22] studied dietary interactions between non-native species topmouth gudgeon and some native fish species in Sarıçay Stream in Turkey. Didenko and Kruzhylina [10] investigated trophic interaction between topmouth gudgeon and the co-occurring species during summer in the Dniprodzerzhynsk Reservoir in Ukraine.

Asian cyprinid, Pseudorasbora parva, causes increased mortality and totally inhibiting spawning of endangered native fish, the European cyprinid Leucaspius delineatus. This threat is caused by an infectious pathogen, a rosette-like intracellular eukaryotic parasite that is a deadly, non-specific agent. It is probably carried a vector of an emergent infectious disease and could decrease fish biodiversity in Europe [38].

The topmouth gudgeon is successfully inhabited invasive fish in Lake Eğirdir. However, its feeding properties have not been sufficiently studied yet. The aim of the present study was to determine the diet composition of Pseudorasbora parva and its prey selectivity in the Lake Eğirdir, Turkey.

2. Materials and methods

2.1. The study area

Lake Eğirdir is the second largest freshwater reservoir in Turkey with a total of 457 km² (48 km x 16 km) surface area [39, 40] and located in the lakes region, southwestern part of Turkey. The maximum depth of lake is 13 m. The water income of the lake is supported from underground water source, surface springs, runoff water, rain and small streams. Evaporation and water flow into Lake Kovada through a channel are main outflows of the lake [41]. The lake is an important source of drinking water as well as tourism and agricultural irrigation. The previous fauna and flora studies carried out in the lake yielded a rich biodiversity. According to the QB/T [42], the Rotifera index showed that the lake has mesotrophic features in terms of zooplankton. Carlson’s trophic state index also supports that the lake shows both mesotrophic and eutrophic characteristics. Annual mean concentration of chlorophyll-a (3.0 ± 0.2 mg/m³) also supported the proposed trophic status of the lake [43]. Zooplanktonic organisms, which is significant part of the lakes, consisted of Rotifera (40 species), Cladocera (22 species) and Copepoda (3 species). Rotifers, Poyarthra dolichoptera and Keratella cochlearis known as indicator of mesotrophic conditions, were reported to occur predominantly in the lake [43].

A total of 129 algal taxa belonging to six groups Ochrophyta (65 species), Chlorophyta (30 species), Charophyta (13 species), Cyanophyta (12 species), Euglenophyta (6 species) and Myzozoa (3 species) were determined [44]. The average abundance of 24 zoobenthic species was recorded recently as 4.195 individuals/m². Dominant species were Oligochaeta with 53.4% relative density. The proportions of Insecta, Bryozoa and Malacostraca were reported as 17.6%, 11.7% and 10.6%, respectively [45].

In the first and most comprehensive study on lake, it was reported that the lake fish fauna consisted of 10 different (Cyprinus carpio, Schizothorax prophylax, Varicorhinus pestai, Acanthorutilus handlirschi, Vimba vimba, Thylognathus klatti, Aphanius chantrei, Cobitis taenia, Nemachilus angorae, Pararhodeus niger) species [46]. In fact nine species occurs in the lake since S. prophylax and V. pestai are synonyms of each other. Perch (Sander lucioperca) was the first fish introduced into the lake in 1955. A total of nine different non-native species were reported at different times over a period of about 70 years. Today, there are totally 14 fish species (2 native, 6 endemic, 7 non-native) belonging to 8 families in the lake. These species are listed as Cyprinus carpio, Vimba vimba (native), Oxynoemacheilus mediterraneus, Seminemacheilus ispartensis, Cobitis turcica, Capoeta pestai, Pseudophoxinus egridiri, Aphanius anatoliae (endemic), Atherina boyeri, Carassius gibelio, Pseudorasbora parva, Knipowitschia caucasica, Gambusia holbrooki and Sander lucioperca (non-native) [41, 47, 48, 49].

2.2. Specimen sampling and data analysis

Fish samples were collected between April and August in the years of 2010 and 2011. All fish caught by the gill nets and purse seine were evaluated in the diet study. Fishing nets with mesh size 10, 16, 45 and 0.9 mm were used. Sampling was performed at two different sites (Figure 1), one in the southern of the lake (St 1, 5–7 m of depth) and the other in the southeast (St 2, with 2–5 m depth). Fish specimens were measured to the nearest 0.1 mm fork length (FL) and weighed to the nearest 0.001 g. The contents of the stomach were removed and the empty stomach was reweighed to the nearest 0.001 g. A total of 88 topmouth gudgeon were analyzed. Each prey item was determined to the lowest possible taxonomic level and counted. Proportion of full and empty stomachs was also determined. Volume calculation was used in Malacostraca, Annelida and Insecta. In addition, average volume was estimated [50] for Disparalona rostrata, Chydorus sphaericus and Nitocra hibernica, Mesocyclops leuckarti (1.0 × 10⁷ μ³), Graptoleberis testudinaria, Alona quadrangularis, Alona guttata, Coronatella rectangula, Pleuroxus aduncus and Nauplii (5.0 × 10⁷ μ³),Bosmina longirostris (4.0 × 10⁷ μ³), Daphnia cucullata (1.0 × 10⁸ μ³), Gomphonema sp., (6.0x10⁴ μ³) and Pediastrum sp. (8.0 × 10³ μ³). All topmouth gudgeon caught were divided into six size classes according to fork length (FL) measuring 6.0–6.9 cm, 7.0–7.9 cm, 8.0–8.9 cm, 9.0–9.9 cm, 10.0–10.9 cm and 11.0–11.9 cm. Fish weight were classified into four groups: ≤5.0 g, 5.1–9.9 g, 10.0–14.9 g and ≥15.0 g.

Figure 1.

Location of the Lake Eğirdir and sampling sites.

Feeding intensity (stomach fullness) was estimated by I_F = (W_SC/W_F)*10,000 [51]. Where, I_F is the fullness index, W_SC is the weight of the stomach contents and W_F is the weight of the fish. Percentage and frequency of occurrence were used to estimate the dietary importance of each prey category [52, 53]. The percentage of the relative importance index [54] and three-dimensional graphical representations [55] were used to express prey importance. IRI_i = (N_i% + W_i%) * O_i%, where W_i and N_i are the total net weight and number of prey and O_i is the number of stomachs containing prey i. Shannon-Weaver (H^′) were used to evaluate the variety of foods in stomach. This index provides a general indication of changes in species diversity [56]. In the first step of statistical analysis, the normality of data was tested for each parameter using the Shapiro-Wilk test, and it was shown that dataset was non-normally distributed. Therefore, those non-normally distributed data were compared using Wilcoxon signed-rank test, followed by Tukey-Kramer honestly significant difference test (HSD). Wilcoxon test displayed a Wilcoxon rank sums test if there were two groups and a Kruskal-Wallis nonparametric one-way analysis of variance if there were more than two groups. To estimate prey selectivity of topmouth gudgeon, Pearre’s selection index (V) [57] was calculated.

$\mathrm{Va}=\frac{\left({\mathrm{ad}}^{\ast }\mathrm{be}\right)-\left({\mathrm{ae}}^{\ast }\mathrm{bd}\right)}{\sqrt{\left(a^{\ast }{b}^{\ast }{d}^{\ast }e\right)}}$

Where Va is Pearre’s index for topmouth gudgeon selectivity of species a, a_d is relative abundance of species a in the diet, b_e is the relative abundance of all other species in the environment, a_e is the relative abundance of species a in the environment and b_d is the relative abundance of all other species in the diet. a = a_d + a_e, b = b_d + b_e, d = a_d + b_d, e = a_e + b_e. The selection index (Va) is statistically tested using the chi-squared test. (X² = n*V²) where, n = a_d + a_e + b_d + b_e. Diet similarity among size classes and months was estimated using the Schoener Overlap Index (C) [58]. Cry = 1–0.5 ∑ |pxi-pyi|; where pxi and pyi are the proportions by number of prey type i in the diets of groups (length or season) x and y, respectively. If the C value is bigger than 0.80, it means that the diet of the two groups is similar.

3. Results

3.1. The size and weight ranges of topmouth gudgeon

In this study, topmouth gudgeon ranged from 6.1 to 11.1 cm in fork length (FL) with an average value of 7.71 ± 0.18 cm and their total weight ranged from 3.52 g to 25.49 g, with an average value of 8.13 ± 0.78 g. The number of species, minimum and maximum fork length and minimum and maximum weights from different months in the lake are presented in Table 1.

		Fork length (FL, cm)		Weight (W, g)
Sampling date	The number of fish	Min–Max	Mean value ±SD	Min–Max	Mean value ± SD
April	9	6.2–10.0	7.30 ± 0.48	3.85–20.17	7.65 ± 2.15
May	46	6.1–11	7.71 ± 0.18	3.52–25.20	8.13 ± 0.78
June	6	7.4–11.1	9 ± 0.58	7.06–25.49	11.65 ± 2.80
July	10	6.8–9.6	7.88 ± 0.29	4.74–13.05	7.18 ± 0.82
August	17	6.5–10	8.15 ± 0.25	3.7–16.2	8.48 ± 0.89

Table 1.

Number of the fish caught during the study, their minimum, maximum and average fork length and minimum, maximum and average weight.

3.2. The diet composition of topmouth gudgeon

The diet of topmouth gudgeon in the lake was found to consist of phytoplankton, zooplankton, Insecta, Malacostraca, Annelida and unidentified eggs (Table 2).

	N	%N	O	%O	W	%W	IRI	%IRI
Zooplankton taxa
Alona guttata	54	3.78	15	16.85	0.0027	0.0318	64.31	0.985
Alona quadrangularis	14	0.98	8	8.99	0.0007	0.0082	8.89	0.136
Coronatella rectangula	6	0.42	4	4.49	0.0003	0.0035	1.91	0.029
Daphnia cucullata	13	0.91	1	1.12	0.0013	0.0153	1.04	0.016
Disparalona rostrata	2	0.14	1	1.12	0.0001	0.0012	0.16	0.002
Graptoleberis testudinaria	32	2.24	14	15.73	0.0016	0.0188	35.57	0.545
Pleuroxus aduncus	2	0.14	1	1.12	0.0001	0.0012	0.16	0.002
Bosmina longirostris	17	1.19	4	4.49	0.0006	0.0080	5.39	0.083
Chydorus sphaericus	43	3.01	16	17.98	0.0004	0.0050	54.26	0.831
Mesocyclops leuckarti	3	0.21	2	2.25	0.0000	0.0004	0.47	0.007
Nitocra hibernica	480	33.64	30	33.71	0.0048	0.0565	1135.74	17.397
Nauplii	1	0.07	1	1.12	0.0000	0.0000	0.08	0.001
Insecta
Trichoptera larvae	7	0.49	7	7.87	0.6200	7.3020	61.29	0.939
Chironomus sp.	616	43.17	39	43.82	4.0260	47.4161	3969.39	60.801
Chironomus (pupa)	37	2.59	12	13.48	1.0020	11.8010	194.07	2.973
Malacostraca
Chelicorophium curvispinum	63	4.41	28	31.46	2.2300	26.2638	965.17	14.784
Annelida
Annelid	15	1.05	3	3.37	0.6000	7.0664	27.36	0.419
Phytoplankton
Gomphonema sp.	19	1.33	2	2.25	0.0000	0.0000	2.99	0.046
Pediastrum sp.	2	0.14	1	1.12	0.0000	0.0000	0.16	0.002
Unidentified
Unidentified egg	1	0.07	1	1.12	0.0000	0.0005	0.08	0.001
Total	1427	100	190		8.49	100	6528.51	100

Table 2.

Diet composition of topmouth gudgeon in Lake Eğirdir between 2010 and 2011.

N, prey number; W, prey weight; O, frequency of occurrence and IRI, Relative Importance Index.

Total weight of 1427 prey items was 8.49 g. Insects were the most frequently ingested prey with 66.52% by weight. Chironomus sp. (47.42%) was the dominant prey insects followed by Chelicorophium curvispinum (26.26%) and Chironomus pupa (11.80%) in terms of weight. Relative Importance Index (IRI) showed that prey Insecta (64.71%) had more importance than the zooplankton prey categories (20.03%) and C. curvispinum (14.78%). Chironomus sp. had the highest index value (IRI = 60.80%) followed by N. hibernica (IRI = 17.40%). In April and May, the main diet of topmouth gudgeon was composed of zooplankton, Insecta and Malacostraca. Insecta was particularly consumed in relatively high numbers. Insecta was also the main prey item of topmouth gudgeon in June. The main diet of topmouth gudgeon consisted of insect together with zooplankton. However, in August, members of Insecta, Annelida, zooplankton and phytoplankton were the main prey items of topmouth gudgeon (Figure 2).

Figure 2.

Monthly diet variations of topmouth gudgeon in Lake Eğirdir between 2010 and 2011 (IRI: Relative importance index).

3.3. Fullness, diversity and similarity indices

Maximum fullness index was in April, whereas minimum fullness index was observed in July (Figure 3). According to Shannon-Weaver index (H^′), the maximum values (H^′=1.80) were found in May and the minimum values (H^′=0.79) were determined in April. A Wilcoxon matched-pairs signed rank test was conducted to determine whether there was a spatial difference in the ranking of two stations. The results revealed significant effects of spatial variation on occurrence of Mesocyclops leuckarti and nauplii in stomach content (Z = 3.39, p < 0.001 and Z = 2.37, p < 0.05, respectively). A post-hoc test using Tukey-Kramer HSD tests showed the significant differences between Station 1 and 2 (p < 0.05). The results showed spatial changes of M. leuckarti and nauplii in the lake that they were only recorded in stomach content of fishes at Station 1.

Figure 3.

Variations in fullness index and empty stomach of topmouth gudgeon.

A Kruskal-Wallis test was operated to determine whether there was a temporal difference in occurrence of taxa in stomach content. The results of analysis revealed significant differences in occurrence of C. curvispinum, M. leuckarti and N. hibernica (x²(4) = 18.54, p < 0.01; x²(4) = 15.78, p < 0.01 and x²(4) = 24.09, p < 0.001, respectively). A post hoc rank sums test indicated that there were significant differences between April and all other months for N. hibernica and C. curvispinum, whereas significant differences occurred between July and April, May, August for M. leuckarti (Tukey–Kramer HSD, p < 0.05). Indeed, the ratios of N. hibernica and C. curvispinum in stomach content were significantly higher in April, and M. leuckarti only occurred in July. This analysis showed that there was a clear temporal variation in occurrence of species. A Kruskal-Wallis test also showed the significant monthly differences for Alona guttata, Chironomus sp., Chironomus (pupa), Chydorus sphaericus and Graptoleberis testudinaria whose ratios in stomach content were significantly higher in May than the other months. However, a post-hoc test did not correct the significant differences (Tukey-Kramer HSD, p > 0.05). A Kruskal-Wallis test revealed that there were significant effects on occurrence of N. hibernica in stomach content due to both fish weight and length (x²(3) = 24.57, p < 0.001 and x²(5) = 26.88, p < 0.001, respectively). A post hoc rank sums test also corrected that there was a significant difference between the group ≤5 g and all other weight groups for N. hibernica (Tukey-Kramer HSD, p < 0.05). In addition, Tukey-Kramer HSD showed a significant difference between the length group of 6.0–6.9 cm and 7.0–7.9 cm together with 8.0–8.9 cm (p < 0.05). The longer groups (P.parva) in whose stomach contents N. hibernica was not recorded were not significantly differentiated than length group of 6.0–6.9 cm.

Although similar differences were determined for N. hibernica and Chironomus sp. with a Wilcoxon test, a post-hoc test did not correct the significant differences (Tukey-Kramer HSD, p > 0.05). Topmouth gudgeon was significantly different for months because of high Schoener Overlap Index (C < 0.80). Diet composition showed similarities between 7.0–7.9 cm and 10.0–10.9 cm (C = 0.80) and 8.0–8.9 cm and 10.0–10.9 cm (C = 0.87) size classes of topmouth gudgeon.

3.4. Different size classes of diet composition

Different size classes of topmouth gudgeon were characterized by different diet compositions (Figure 4). Prey zooplankton species was consumed by 58.90% of the 6.0- to 6.9-cm sized topmouth gudgeon, with a large weight (0.39%) percentage. However, it consumed in the 6.0–6.9 cm size class in the diet in terms of numbers (75.12%). In the stomachs of topmouth gudgeon of the 8.0–8.9 cm size class, only phytoplankton species was determined. In >10 cm sized topmouth gudgeon prey, Insecta species was identified (Figure 4).

Figure 4.

Stomach contents in different size classes of topmouth gudgeon in Lake Eğirdir between 2010 and 2011. Zoo, zooplankton; Chr, Chironomus sp.; Chr. (pup), Chironomus (pupa); Cor, C. curvispinum; Tr, Trichoptera larvae; An, Annelida; Ph, phytoplankton and Un.eg., unidentified egg.

3.5. Prey selection

Feeding rates was compared in the diet and in the ecosystems in 2010. Chironomus sp. was the commonly abundant prey in the ecosystem; it was a positively selected food item and was not statistically significant. Also, A. guttata (V = 0.062, X² = 0.781, p > 0.05), A. quadrangularis (V = −0.024, X² = 0.123, p > 0.05), C. curvispinum (V = −0.037, X² = 0.277, p > 0.05), C. rectangula (V = 0.098, X² = 1.931, p > 0.05), G. testudinaria (V = 0.055, X² = 0.616, p > 0.05), M. leuckarti (V = 0.049, X² = 0.499, p > 0.05) and nauplii (V = 0.015, X² = 0.047, p > 0.05) were found in the ecosystems, but was not preferred by topmouth gudgeon. Similarly, Pediastrum sp. (V = −0.141, X² = 4.016, p < 0.01) and N. hibernica (V = −0.221, X² = 9.818, p < 0.01) were avoided by topmouth gudgeon despite their high abundance in the lake Eğirdir ecosystem (Figure 5). Some organisms in the diet of topmouth gudgeon are shown in Figure 6.

Figure 5.

Percentages of the lake ecosystems and diet of topmouth gudgeon in Lake Eğirdir in 2010 (May, June, July, August).

Figure 6.

Some organisms in the diet of topmouth gudgeon (a) G. testudinaria, (b) D. cucullata, (c) C. curvispinum, (d) N. hibernica, (e) B. longirostris and (f) C. sphaericus (scale: 100 micron).

4. Discussions

The fish fauna of Lake Eğirdir was previously reported to consist of Cyprinus carpio, Carassius gibelio, Tinca tinca, Vimba vimba, Capoeta pestai, Sander lucioperca, Alburnus chalcoides, Pseudophoxinus egridiri, Pseudophoxinus handlirschi, Cobitis turcica, Barbatula mediterraneus, Seminemacheilus ispartensis, Aphanius anatoliae, Gambusia affinis, Knipowitschia cauca-sica, Hemigrammocapoeta kemali, Atherina boyeri and Pseudorasbora parva [41]. Total of 15 fish species, including P. parva, were observed from January to December 2010 in the Lake Eğirdir [59]. Among the 15 recorded fish species, sand smelt Atherina boyeri (65.72%), killifish Aphanius anatoliae (19.39%) and Caucasian dwarf goby Knipowitschia caucasica (3.01%) are not commercially precious. Fishing activities were very limited in the lake and the average of annual catch was approximately 21.19 kg ha⁻¹ in 2010. Fish species, which dominate in the catches, were crucian carp Carassius gibelio, pikeperch Sander lucioperca, common carp Cyprinus carpio and vimba, Vimba vimba [60]. Zooplankton abundance in the lake ranged from 42 ± 24 to 3092 ± 2435 individuals L⁻¹ from January to December 2010. Rotifera was the most abundant group dominated mainly by Polyarthra dolichoptera and Keratella cochlearis. Bosmina longirostris was also relatively abundant in the lake. In contrast, C. sphaericus showed lower abundance. The zooplankton abundance comprised as follows: Rotifera, 89.62%; Cladocera, 7.78% and Copepoda, 2.60% [43, 59]. The average number of zoobenthic organisms was 4.195 individuals/m², and Tubifex spp. were the most abundant taxa with 52.33% abundance, followed by Chironomus spp. (17.10%) in the Lake Eğirdir [45].

P. parva had a diversed diet composition mainly with Chironomus sp., N. hibernica, Chydorus sphaericus and Bosmina longirostris. We determined that the diet of topmouth gudgeon in Lake Eğirdir was dominated by Chironomus sp. Chironomus spp. are also one of the most important food in Neusiedler See from Austria [4]. It was also stated that the topmouth gudgeon feeds on Chironomid larvae, Ceratopogonid larvae and Gastropods in Austria. Our results are in accordance with Wolfram-Wais et al. [4] who stated that topmouth gudgeon showed reliance mean to Chironomus spp., according to the IRI index. Hliwa et al. [35] observed that the diet of topmouth gudgeon in the Balaton Reservoir was characterized by Bosmina sp., Chydorus sp., Copepoda and Daphnia sp. According to Xie et al. [34], the diet of the topmouth gudgeon from the Biandantang Lake from China was registered by Copepoda, Cladocera, Ostracoda, Chironomid larvae and Mollusca. Generally, these findings have many common points with the present study. However, according to Yalçin-Özdilek et al. [37], the diet of the topmouth gudgeon from Turkey in Gelingüllü Reservoir was based mainly on Cyanobacteria, Insecta and Cladocera.

A minor role of Platyhelminthes in the topmouth gudgeon diet was also observed in Gelingüllü Reservoir by Yalçin-Özdilek et al. [37]. In addition, Karakuş [22] indicated that P. parva feeds dominantly on Insecta, detritus, Copepoda and other zooplankton groups, but rarely on Macrophyta, Nematode and Rotifers in Sarıçay Stream, Muğla, Turkey. Additionally, Karakuş [22] found that P. parva has a variety of diet spectrum and niche width, further it feeds on higher trophic levels.

Nikolova et al. [36] reported seasonal variations in the diet of P. parva from shallow eutrophic lakes along river Vit of Bulgaria. Diet of the topmouth gudgeon was dominated by Diptera/Chironomidae. The role of the Oligochaeta, Ephemeroptera, Copepoda/Calanoida Trichoptera and Nematoda as important additional food resource for topmouth gudgeon was recorded by Nikolova et al. [36]. In our study of temporal variation (monthly) of the diet revealed that the topmouth gudgeon diet in June and August was dominated by Chironomus sp., whereas in July there was an increase in the consumption of Bosmina longirostris. Gozlan et al. [7] confirmed that the fish prefers Chironomid larvae in Belgium. The consumption of fish eggs and fish larvae by topmouth gudgeon was well documented [34, 37]. Gozlan et al. [7] reported that eggs of native fish species and larvae were preferred the diet of topmouth gudgeon in China and Germany. In the present study, unidentified egg (1.37%) was also found in stomach contents of the fish. Additionally, the present study showed monthly variations in dominated food items and frequency occurrence of some food items significantly differed from month to month. Diet of topmouth gudgeon showed a great variety of food taxa in May except Chironomus sp. and C. curvispinum. The fish also preferred A. quadrangularis, C. sphaericus, P. aduncus, Annelida and Chironomus sp. (pupa). Shannon’s diversity was highest in May and lowest in April. The variety of food in May (H^′=1.80) was higher than in the other months. In August, Insecta (Chironomus sp.), Annelida and Phytoplankton (Gomphonema sp.) were determined in the stomach content. The ratio of Insecta was 54.42%. It is important to note that D. cucullata, Gomphonema sp. and Pediastrum sp. were present in stomach only in August. The variety of food in June was less than that in the other months. In addition, zooplankton (B. longirostris), Trichoptera larvae and Malacostraca (C. curvispinum) were the crucial prey for the feeding of topmouth gudgeon in July. The ratio of Trichoptera larvae was 42.09%. Typically, the dominant food item (frequency of occurrence) was Chironomus sp., with 66.67% of total individuals in size classes of 11.0–11.9 cm, followed by C. curvispinum (33.33%) in the size classes of 10.0–10.9 cm, Disparalona rostrata (1.37%) in the size classes of 6.0–6.9 cm, Annelida (14.29%) in the size classes of 9.0–9.9 cm, Nauplii and Pleuroxus aduncus (1.37%) in the size classes 7.0–7.9 cm and Daphnia cucullata (3.57%), Gomphonema sp. (7.14%) and Pediastrum sp. (3.57%) were noticeable in the size classes of 8.0–8.9 cm. Yalçin-Özdilek et al. [37] indicated that topmouth gudgeon individuals with lengths greater than 3 cm mainly consumed Cyanobacteria. The importance of zooplankton, Insecta and Malacostraca in the diet of topmouth gudgeon is differed in different size of fish classes in this study. Larger fish have fewer zooplankton, more insecta and malacostraca in their diet and vice versa for smaller fish.

Wolfram-Wais et al. [4] suggested that the diet of topmouth gudgeon changed with Chironomid larvae, especially epiphytic species in Neusiedler See from Austria. This result is in harmony with our study since the topmouth gudgeon >6 cm fed mainly on Chironomus sp. The fish was found to feed on Chironomus sp. intensively between April and June in Lake Eğirdir. Fullness index of topmouth gudgeon was also reported to be the highest in summer and spring [37]. Xie et al. [34] showed that topmouth gudgeon fed intensively during summer and autumn. However, fullness index of the topmouth gudgeon was high between April and June in Lake Eğirdir. Dietary overlap of topmouth gudgeon was reported by Yalçin-Özdilek et al. [37] from Gelingüllü reservoir. However, there was no dietary overlap between the smallest size class and the other classes [37]. Xie et al. [34] indicated that diet overlap of topmouth gudgeon individuals was low in summer and autumn. Our study showed that specimens belong to the <8 cm size classes were determined to ingest a great variety of prey items in comparison to other size classes. The specimens with >8 cm consumed mainly Annelida, Chironomus (pupa), C. curvispinum, Trichoptera larvae, principally Chironomus sp. However, zooplankton also was of importance in the diet of <8 cm size classes. Statistical analyses indicated that weight and length have the significant effects on nutrition habits of Pseudorasbora parva in Lake Eğirdir. Small-sized individuals preferred to feed on N. hibernica, whereas annelida was preferable food for large fish. M. leuckarti was found to be markedly dominant in stomach content of P.parva in May. Indeed, M. leuckarti showed spread across the temperate zone of the lake in April–June [61]. In addition, Demirhindi [62] and Aksoylar and Ertan [63] reported variation in distribution of M. leuckarti in the lake [43]. The rate recorded in the stomach contents showed that M. leuckarti changed by sampling sites. Pseudorasbora parva fed on harpacticoid copepods N. hibernica mainly in May.

The results also indicate that topmouth gudgeon feeds on zoobenthic organisms in the lake. Prey selection showed that D. cucullata, B. longirostris, Annelida, Tricoptera larvae and Gomphonema sp. positively selected by topmouth gudgeon in Lake Eğirdir; therefore, their selection indices were statistically significant (p < 0.01). Pearre’s selectivity indices showed that A. guttata, C. rectangula, Chironomus sp., C. curvispinum, G. testunidaria, M. leuckarti and Nauplii were neutrally selected. According to Didenko and Kruzhylina [10], Ivlev’s selectivity indices demonstrate that topmouth gudgeon positively selected zooplankters such as Chydorus sphaericus, Alona affinis, Pleuroxus sp. and Cyclops sp., but avoided Bosmina sp. Asplanchna priodonta was also positively selected among rotifers. Anatolian endemics Aphanius anatoliae was consumed with a rate of 63.91% in the Lake [64]. In this study, the diatom (from Bacillariophyta) Gomphonema sp. according to the selectivity index, diets low statistically significant (V = 0.225, p < 0.01). Ekmekçi and Kırankaya [17] concluded that P. parva develops dense populations in some water bodies and it is blamed for food competition with other species. Moreover, the impact of P. parva on natural food structure was shown in terms of zooplankton and zoobenthos and main fish production parameters [65]. Musil et al. [65] found that differences in mean zooplankton members and especially in Daphnia density between the seasons of 2003 and 2004 were highly significant in fish ponds (three different ponds). Tarkan [66] informed that the disease vectors, such as P. parva, damaging fishing capacity are too large. The topmouth gudgeon has a high reproductive potential and it was uncontrollably introduced into the water resources. In addition, topmouth gudgeon is evaluated in the status of pest species [26].

5. Conclusions

The observations in this study confirm that P. parva has diverse diet preferences. Therefore, the topmouth gudgeon should be considered a serious threat to the diversity of food chain in Lake Egirdir since the fish consumes all kinds of organisms in the chain. In addition, it has a potential to carry a variety of diseases. It also be noted that the fish have abilities to produce eggs in large diameters and grow rapidly in a dense population size in a short time. Sexual dimorphism and nest protection behavior are the other advantages of the fish to become a dominant fish population in the lake. Our study is expected to contribute to better knowledge of diet composition of topmouth gudgeon in Lake Eğirdir for future researches. We hope that future researchers can estimate the possible damages on the biomass and species composition of zooplankton in relation to their considerable consumption by the increasing population of P. parva in the lake. Finally, it is important to point out that invasive non-native fish species should be kept away from natural ecosystems since they constitute a great threat for native fish species for food and breeding grounds.

Acknowledgments

We like to thank all the technical staff for help in sampling from the Fisheries Research Institute, Eğirdir-Isparta, and Professor Dr. F. Güler Ekmekçi, Professor Dr. Ali Serhan Tarkan and Professor Dr. Andrzej Witkowski for their support to provide literature and Professor Dr. Nadezhda A. Berezina and Assist. Prof. Dr. Arda Özen for English polishing.