94

http://journals.tubitak.gov.tr/zoology/

Turkish Journal of Zoology Turk J Zool(2019) 43: 94-105© TÜBİTAKdoi:10.3906/zoo-1806-26

New location, food composition, and parasitic fauna of the invasive fishPseudorasbora parva (Temminck & Schlegel, 1846) (Cyprinidae) in Poland

Przemysław CZERNIEJEWSKI1, Agnieszka RYBCZYK2

, Angelika LINOWSKA3,*, Ewa SOBECKA3

1Department of Fisheries Management and Water Protection, Faculty of Food Sciences and Fisheries,West Pomeranian University of Technology in Szczecin, Szczecin, Poland

2Departament of Aquatic Sozology, Faculty of Food Sciences and Fisheries,West Pomeranian University of Technology in Szczecin, Szczecin, Poland

3Department of Hydrobiology, Ichthyology, and Biotechnology of Breeding, Faculty of Food Sciences and Fisheries,West Pomeranian University of Technology in Szczecin, Szczecin, Poland

* Correspondence: angelika.linowska@zut.edu.pl

1. IntroductionStone moroko (Pseudorasbora parva (Temminck & Schlegel, 1846)) is a cyprinid endemic to eastern Asia: Japan, China, the Korean Peninsula, and the Amur River basin. The fish was first unintentionally introduced into common carp ponds in the Danube Delta in 1961 (Banarescu, 1999). Thereafter, the fish was transferred with stocking material to ponds and natural bodies of water in Germany, Albania, and Lithuania (Holčik, 1991), and also in Israel (Welcomme, 1981). In the late 1970s, stone moroko was recorded from France (Allardi and Chancerel, 1988), and finally in the 1980s from Poland (Witkowski, 2009). The species’ rapid dispersal has been facilitated by growing international aquaculture logistics; however, the fish owes it to itself that invading water bodies outside its endemic range may be so successful, as its life history traits allow adaptation and survival in new environments. These mainly include a strong reproductive capability, parental care, and a wide spectrum of tolerated food (Pollux et al., 2006). The dynamic spreading process of the invader has

been under scrutiny of a number of authors, including Witkowski (2009), Gozlan et al. (2002), and Ekmekçi and Kırankaya (2006). Recently, the knowledge on the species has been enriched with new facts discovered about the behavior, age structure, and growth rates of some novel P. parva populations (Sunardi and Manatunge, 2007; Záhorská and Kováč, 2009; Záhorská et al., 2009, 2010).

Much less attention, though, has been devoted to the parasites affecting stone moroko in its new regions. The presence of a new host organism in the habitat means that the parasites it carries may be introduced, too (Williams et al., 2013). Alien parasites may be hazardous to native fishes, which have a weak immunological barrier against parasites they have never experienced (Kelly et al., 2009). The danger should not be neglected, as parasites that are pathogenic to native fishes have already been found in stone moroko, namely Anguilloides crassus, a European eel (Anguilla anguilla) nematode, for which stone moroko is a paratenic host, as well as the rosette agent, Sphaerothecum destruens (Cesco et al., 2001; https://nas.er.usgs.gov/).

Abstract: Stone moroko (Pseudorasbora parva) is considered to be one of the most invasive fishes, dispersing rapidly all over Europe and also in the freshwaters of the Baltic Sea basin. A recent survey carried out in the catchment of the lower part of the Odra River (Poland) in 2015 and 2016 revealed a large new population of stone moroko, which had colonized the creek Wardynka. The sample of 518 fish caught was dominated by age groups 1+ (341 specimens) and 2+ (99 specimens); however, older fish were also present, which means that at the moment of analysis the species had been in the Wardynka for at least 5 years. The diet was composed of copepods, amphipods, ostracods, and cladocerans, with Daphnia sp. being most frequent, which also showed the highest index of relative importance and percentage by weight in the food. The parasitic fauna composition of stone moroko in the new location involves local parasites only. Trichodinella subtilis, Diplozoon paradoxum, Apatemon gracilis, and Caryophyllaeus laticeps were found for the first time ever. The lack of parasitic species that normally occur in fish of this species was probably caused by the lack of intermediate hosts, which are necessary to complete their life cycles.

Key words: Stone moroko, age structure, diet composition, new parasites, Wardynka creek

Received: 19.06.2018 Accepted/Published Online: 07.12.2018 Final Version: 11.01.2019

Research Article

This work is licensed under a Creative Commons Attribution 4.0 International License.

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The consequences of introducing new parasites to the ecosystem will vary, depending on many factors, including the age and the composition of food organisms of the target fish, the complexity of the parasite’s life cycle, and, linked to it, the presence or absence of intermediate host organisms in the parasite’s new environment.

Hence, this study focused on the selected population variables (length, weight, and age structure) and growth and food composition of the fish as well as a survey of species composition and prevalence, mean intensity of infection, intensity range, and relative density of parasites counted in stone moroko in the creek Wardynka (Odra River basin, Poland).

2. Materials and methodsThe catches were carried out in a creek called Wardynka, located in the Ina-Odra catchment area, in northwestern Poland. The Wardynka, which is a 17.9-km-long tributary of the stream Stobnica, begins in peat bogs and continues its flow over a varied landscape: from lowland fields, where the stream is sluggish, to hilly areas, where it flows more lively, in places resembling highland rapids. Stone moroko were found in the upper flow of the creek (12.63 km from

the springs, 15°33′40.2″N, 53°09′11.5″E) in the vicinity of a common carp pond farm (Figure 1). The average depth at the catching site was 1.6 m, unit riverbed gradient 11%, both banks distinctly delimited, strengthened with fascine, bed surface leveled, without major hollows or other hiding places for fish, bottom covered with a layer of sand.

The catches were carried out using approved electrofishing equipment in May 2015 and June 2016, the operators waded upstream for 100 m, and the catch covered the entire width of the riverbed.

A total of 518 stone moroko were caught (in 2015, 196 ind.; in 2016, 322 ind.). In the laboratory, the fish were measured for total length (TL, mm) and standard length (SL, mm), with precision to the nearest 0.1 mm, and weighed with precision to 0.1 g, using an AXIS digital scale. Fulton’s factor (KF = W/TL3 × 100) was calculated in order to evaluate the body condition of the fish (Ritterbusch-Nauwerck, 1995). The length–weight relationship (WLR) in fishes is usually expressed by the equation W = aLb, where W is body weight (g), L is total length (cm), a is a coefficient related to body form, and b is an exponent indicating isometric growth when equal to 3. The parameters a and b of WLR were estimated by

Electrofishing site in WardynkaFigure 1. Location of electrofishing site in Wardynka creek (NW Poland).

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the least-square method from logarithmically transformed data, and the correlation between weight–length variables was calculated by the determination coefficient (R2). The statistical significance of R2 and 95% confidence limits of parameters a and b were estimated (Froese, 2006).

Six well-developed scales were removed from between the lateral line and dorsal fin of each specimen. Scales were cleaned by alkaline immersion method (Huang et al., 2015) and compressed between two glass slides for age determination by counting the number of completely developed annual rings (Rosecchi et al., 1993). Both the scale diameter and annual increments were measured using a Nikon Eclipse E600 stereo microscope, equipped with an HD-video camera, and Lucia image analysis software (Nikon). Growth in previous years was determined by back calculation from scale measurements, following the Lee method (Záhorská et al., 2010). The growth curves in males and females were described by applying the von Bertalanffy equation. The von Bertalanffy equation coefficients were calculated by producing a Walford plot of Lt + 1 against Lt (Ogle and Isermann, 2017). The casual relationship of independent variable TL and dependent variables (scale caudal diameter) was examined through ordinary linear regression modeling (Ricker, 1975).

Food composition was analyzed in the contents of the digestive tracts of 150 fish, sampled proportionally from each length class. The digestive tracts were preserved in 80% ethanol and, after dilution in 20 mL of water, contents were transferred to the plankton counting chamber. The analysis involved taxa identification and counts by viewing the specimens under the Nikon Eclipse E600 stereo microscope with magnification 100×. The result was converted per entire volume of the digesta found in one fish. Diet composition data were expressed as percent by number (%N), percent by weight (%W), percent frequency of occurrence (%O), and the index of relative importance (%IRI) (Hyslop, 1980; Liao et al., 2001).

Parasitological examinations of dead fish (total 111, including 37 in 2015 and 74 in the following year) focused on the skin, vitreous humor, eye lens, mouth and nasal cavities, gills, heart, gonads, gastrointestinal tract, kidneys, gallbladder, and peritoneum. The parasites were identified by viewing the specimens immersed in glycerin under transient light with the Olympus BX50 microscope equipped with an AxioVision camera and its software, or preserved in 75% ethyl alcohol.

The qualitative analysis of the parasite communities involved the taxonomic unit (based on their morphological features) and species diversity according to Moravec (1994) and Niewiadomska (2003). Other original works with taxonomic descriptions were also referred to. Besides these, Fauna Europaea (https://fauna-eu.org/) was also used as a source of the taxonomic names of the parasites.

The nomenclature for the parasite community structures was based on the studies by Bush et al. (1997).

Quantitative structure analysis was performed by determining the quantitative composition of each of the qualitative groups (species or higher taxa). The following parameters were evaluated: prevalence (% of fish infected), mean intensity of infection (the mean number of parasites found in the infected hosts), relative density (the average number of parasites per one host in a sample), and dominance ratio, which defines the role of the parasite in the community. Habitat preferences (topical structure) and cooccurrence of parasite species were also studied.

Analysis of the material for possible correlations between the presence of particular parasites and total length (TL), body weight, or body condition as measured with Fulton’s condition factor (KF) was made.

Statistical data analysis included the mean (X), standard deviation (SD), and their distributions within size classes. The package STATISTICA 12.0 PL (StatSoft, Poland) was used for statistical computations. In order to compare means between the sexes, the Student t-test was used, following testing of the normality of distributions of the variables, using the Kolmogorov–Smirnov test, and the equality of variances, using the Levene test (Sokal and Rohlf, 2012).

3. Results3.1. Body length, weight, and conditionThe mean total length (TL) of the fish was 52.9 ± 13.1 mm (range: 31.2–86.0 mm), while the standard length (SL) averaged 43.9 ± 10.0 mm (range: 25.6–72.3 mm). There was a statistically significant linear correlation between TL and SL, with SL = 0.837TL – 0.0414 (R = 0.9911, P < 0.001). After division into standard length (TL) 5-mm classes, the fish were recorded in 12 classes (Figure 2). The mean unit weight (W) of the fish was 1.81 ± 1.66 g (range: 0.21–7.2 g), and mean Fulton condition (KF) was 1.03 ± 0.34 (range: 0.74–1.28).

The mean total lengths (TL), unit body weights, and Fulton condition factors of the studied fish did not differ significantly between the years of catch (Student t-test, P > 0.05). However, after separation of the sexes, statistically significant differences were observed in TL (t = –3.44199, P = 0.00082) and unit weight W (t = –3.765232, P = 0.000536), but condition factor did not differ between sexes (P > 0.05). The changes of TL, W, and KF plotted against age group of males and females of stone moroko are presented in Figure 3. The ratio of females to males (sex ratio) for the whole sample was 1 to 0.95.

The TL–W relationship for the total sample was W = 0.0042TL3.487862 ± 0.077 (R2 = 0.94939). The b (slope) value of the TL–W regressions was significantly higher than 3 (t = 45.4395; P < 0.001), indicating positive allometric growth.

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The following fitted models hold for males and females, respectively: W = 0.0049TL3.494216 ± 0.069 (R2 = 0.965329) and W = 0.0051TL3.43442 ± 0.079 (R2 = 0.89532).3.2. Age and growth of fishFive age groups were found in the sampled fish, with predominant groups 1+ and 2+. Age groups 1+ and 2+ were again dominated by females, which represented 56.16% and 66.67% of the samples, respectively. On the other hand, only males were found in groups 4+ and 5+.

The scale caudal radius ranged within 0.54–2.56 mm (1.50 mm on average). A strong correlation was found between total length (TL) and the scale caudal radius (R = 0.93208; P < 0.0001) with linear regression (R = 0.0408TL – 0.2834). This was used to determine total length at the onset of scale formation, 6.95 mm.

The growth rate of stone moroko estimated by von Bertalanffy method is typical for short-lived fishes (Figure 4). Moreover, significant differences were found in the total length (TL) between males and females of the same age (t-test, significant at P < 0.05; Table 1). 3.3. Diet compositionThe diet included the following crustaceans: Copepoda, Amphipoda, Ostracoda, and Cladocera. Apart from these, we found blue-green algae (Cyanobacteria), chironomid, trichopteran, and dipteran larvae, as well as rotifers and oligochaetes (Table 2). The most frequently occurring (%O) food organisms were Daphnia sp. (100% O), rotifers (94.2% O), and dipteran larvae (80.4% O). Daphnia sp. was also a prevailing food item by weight, attaining 15.9% W of the entire stomach content. The relative importance (%IRI) of Daphnia sp., Cyanobacteria, and rotifers in the diet was high, 19.0%, 12.2%, and 8.6% IRI, respectively,

which also demonstrated the predominance of these food organisms in the diet of stone moroko.

The composition of particular food organisms changed with the length of the fish (Table 2). Fish eggs and scales were found in the stomachs of the largest fish.3.4. Parasitological examinationsThe parasite community of P. parva comprised 91 individuals of Metazoa (5 species) and two species of uncountable parasites belonging to Protista. The latter included single specimens of Chilodonella piscicola (Zacharias, 1894; Jankowski, 1980) and Trichodinella subtilis Lom, 1959 (Ciliophora), which were found on the gills of, respectively, one and six fish. Metazoa were represented by a single specimen of Diplozoon paradoxum von Nordman, 1832 (Monogenea) found on a gill, as well as 11 encysted larvae (metacercariae) of the trematode Apatemon gracilis (Rudolphi, 1819) Szidat, 1928 (Digenea), found in the vitreous humor of the eye in two stone moroko. In the anterior part of the gut, we found eight specimens of Caryophyllaeus laticeps (Pallas, 1871) (Cestoda) and 13 juvenile nematode forms (L3) of Cystidicola farionis Fischer, 1798; in the middle part of the intestine, three specimens of Rhabdochona ergensi Moravec, 1968, were found; and 61 nematode specimens of Pseudocapillaria tomentosa (Dujardin, 1843) were counted in the posterior part of the gut. The prevalence for the entire sample reached 36.04% (Table 3). Most parasites were located in the gastrointestinal tract (Table 4), with the most frequently occurring nematode being P. tomentosa (Table 5). Trichodinella subtilis, Diplozoon paradoxum, Apatemon gracilis, and Caryophyllaeus laticeps were found in stone moroko for the first time.

Figure 2. Frequency distributions of total length (TL, mm) of females and males of stone moroko.

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Figure 3. Changes of total length (TL, mm), weight (W, g), and Fulton coefficient (KF) for males and females of stone moroko in particular age groups. Number of males and females in particular age groups was respectively 149 and 191 ind. (1+), 33 and 65 ind. (2+), 20 and 9 ind (3+), 33 and 0 ind. (4+), and 18 and 0 (5+).

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When it comes to P. parva parasitic fauna analysis by year, there is a difference in both species composition and numbers. The prevalence and mean intensity of infection were higher in 2015, when most fish were also infected by gut parasites (Tables 3 and 4). The relative density of the parasites in stone moroko caught in 2016 was lowest and definitely fewer fish were infected with nematodes C. farionis and P. tomentosa, whereas the relative density of the tapeworm C. laticeps was higher compared to 2015.

A significant (P < 0.05) and positive correlation between body lengths (TL, SL), body weight, condition

factor KF, and the community of parasites was found in relation to the occurrence of C. farionis. The presence of P. tomentosa was also related to the size and weight of fish, although correlation coefficients were lower (Table 6).

4. DiscussionThe presence of the fish in the Wardynka creek is the first documented occurrence in this part of Poland; unsurprisingly, however, the fish were caught in the vicinity of fish farms, since the stocking material is one of the vehicles of this invader fish (Ekmekçi and Kırankaya,

Figure 4. Von Bertalanffy growth curve for males and females of stone moroko from War-dynka creek.

Table 1. Mean total length (TL) of males and females of stone moroko in different age groups (L1–L5) (back calculated method).

Age group Sex

Total length (mm)

L1 L2 L3 L4 L5

I MaleFemale

36.833.6

--

--

--

--

II MaleFemale

38.535.7

58.153.1

--

--

--

III MaleFemale

40.236.1

59.249.4

67.461.2

--

--

IV MaleFemale

42.0-

61.3-

70.4-

78.2-

--

V MaleFemale

38.8-

59.3-

70.3-

73.2-

81.4-

L (mean) MaleFemale

38.434.6

59.552.6

69.561.2

76.4-

81.4-

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Tabl

e 2.

Per

cent

wei

ght (

%W

), pe

rcen

t occ

urre

nce

(%O

), pe

rcen

t num

ber (

%N

), an

d pe

rcen

t ind

ex o

f rel

ativ

e im

port

ance

(%IR

I) in

the

diet

of s

tone

mor

oko.

 Le

ngth

clas

s

 To

tal l

engt

h (n

= 8

7)25

.1–3

5.0

mm

35.1

–45.

0 m

m45

.1–5

5.0

mm

55.1

–65.

0 m

m65

.1–7

5.0

mm

75.1

–85.

0 m

m

 Foo

d co

mpo

nent

s(n

= 1

2)(n

=17

)(n

=17)

(n =

11 )

(n =

16 )

(n =

14)

%W

%O

%IR

I%

N%

W%

O%

IRI

%N

%W

%O

%IR

I%

N%

W%

O%

IRI

%N

%W

%O

%IR

I%

N%

W%

O%

IRI

%N

%W

%O

%IR

I%

N

Oth

er C

yano

bact

eria

15.0

8.3

12.3

23.2

19.7

11.7

19.4

8.5

10.0

4.6

8.9

8.2

23.2

13.3

27.2

11.4

19.7

11.7

19.4

8.5

31.7

18.8

42.9

11.2

--

- -

Spiru

nella

sp.

5.1

5.7

2.6

10.6

--

--

6.5

6.0

3.0

3.3

10.6

12.1

10.2

6.8

--

--

8.1

9.6

5.0

3.7

--

--

Oth

er C

lado

cera

5.4

9.2

10.0

4.3

4.5

8.3

6.5

6.9

4.4

6.3

4.8

6.0

4.3

7.6

5.9

7.6

4.5

8.3

6.5

6.9

4.4

8.0

5.3

5.6

4.9

15.4

14.5

11.0

Dap

hnia

cucu

llata

4.1

6.9

4.7

-4.

27.

74.

75.

44.

36.

23.

84.

9-

--

-4.

27.

74.

75.

44.

58.

24.

54.

73.

310

.55.

76.

3

Chyd

orus

sp.

8.3

9.1

9.6

4.9

8.4

10.0

9.3

6.9

2.2

2.1

0.5

1.6

4.9

5.6

3.1

4.6

8.4

10.0

9.3

6.9

12.6

14.9

17.5

8.4

7.1

14.6

12.3

8.7

Bosm

ina

sp.

6.1

6.8

7.8

6.0

4.5

5.3

3.8

5.4

9.6

8.9

14.3

10.3

6.0

6.9

7.1

8.3

4.5

5.3

3.8

5.4

4.7

5.6

3.7

4.7

0.0

0.0

0.0

0.0

Dap

hnia

sp.

16.0

9.8

19.0

17.6

22.8

15.1

36.1

13.1

17.2

8.9

16.9

8.7

17.6

11.2

21.5

11.4

22.8

15.1

36.1

13.1

4.1

2.7

1.0

1.9

15.0

17.1

26.2

12.6

Lept

odor

a ki

ndtti

11.6

3.8

6.3

10.8

12.5

4.4

6.7

5.4

12.6

3.5

6.0

4.9

10.8

3.7

5.0

5.3

12.5

4.4

6.7

5.4

8.0

2.8

2.3

2.8

3.7

2.2

0.9

2.4

Alon

a sp

.0.

33.

32.

40.

10.

22.

61.

36.

20.

43.

83.

310

.30.

11.

60.

54.

60.

22.

61.

36.

20.

33.

41.

86.

50.

23.

51.

77.

1

Oth

er O

stra

coda

9.2

5.1

4.6

9.3

17.8

10.6

16.0

7.7

9.9

4.6

4.1

3.8

9.3

5.3

4.4

4.6

17.8

10.6

16.0

7.7

--

--

--

--

Oth

er C

opep

oda

9.4

6.9

5.3

11.1

11.0

8.7

6.6

4.6

10.2

6.3

4.7

3.8

11.1

8.5

6.8

5.3

11.0

8.7

6.6

4.6

--

--

--

--

Lim

andi

a len

ticul

aris

0.5

3.9

0.9

0.6

0.5

4.0

0.8

2.3

0.7

4.2

1.0

2.7

0.6

4.5

1.0

3.0

0.5

4.0

0.8

2.3

0.3

2.0

0.2

0.9

0.1

1.6

0.1

0.8

Oth

er A

mph

ipod

a1.

43.

11.

30.

81.

22.

80.

93.

10.

71.

30.

21.

60.

81.

70.

42.

31.

22.

80.

93.

13.

58.

26.

67.

53.

012

.411

.811

.8

Oth

er O

ligoc

haet

a5.

06.

24.

13.

02.

63.

41.

02.

39.

710

.011

.27.

63.

03.

81.

43.

02.

63.

41.

02.

32.

63.

40.

91.

90.

61.

40.

10.

8

Oth

er C

hiro

nom

idae

2.2

0.4

0.6

-3.

30.

71.

13.

9-

--

--

--

-3.

30.

71.

13.

94.

91.

02.

14.

758

.520

.024

.14.

7

Chiro

nom

us sp

.1.

10.

20.

31.

21.

10.

20.

33.

10.

20.

00.

00.

51.

20.

20.

43.

81.

10.

20.

33.

12.

40.

51.

25.

60.

90.

30.

33.

9

Tric

hopt

era

larv

ae1.

10.

20.

60.

31.

20.

20.

66.

20.

10.

00.

00.

50.

30.

10.

01.

51.

20.

20.

66.

22.

50.

52.

310

.31.

40.

51.

411

.0

Dip

tera

larv

ae1.

70.

31.

20.

91.

00.

20.

44.

61.

00.

20.

33.

80.

90.

20.

34.

61.

00.

20.

44.

62.

10.

41.

47.

51.

20.

40.

87.

9

Rotif

era

3.3

9.1

8.7

3.4

0.3

0.9

0.1

0.8

4.8

11.0

12.8

10.9

3.4

9.6

8.4

9.9

0.3

0.9

0.1

0.8

1.8

5.3

0.5

0.9

--

--

Leca

ne q

uadr

iden

tata

2.4

6.7

2.6

1.4

1.1

3.2

0.5

1.5

5.2

12.1

8.4

6.5

1.4

4.1

0.8

2.3

1.1

3.2

0.5

1.5

1.6

4.8

0.9

1.9

--

--

Fish

egg

s0.

00.

0-

-0.

00.

0-

0.8

--

--

--

--

0.0

0.0

-0.

80.

10.

10.

15.

60.

00.

1-

0.1

Fish

scal

es-

0.0

--

-0.

0-

1.5

--

--

--

--

-0.

0-

1.5

0.0

0.0

0.0

3.7

0.0

0.0

-0.

0

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2006; Witkowski 2009). It is likely that the fish will move downstream to spread in the other streams of the Ina and Odra basin, because its rate of expansion in rivers has been estimated to approx. 7.5 km per year (Ahnelt and Tiefenbach, 1991). In the Wardynka, stone moroko attains the maximum total length (TL) of 86.0 mm, with peak unit weight of 7.2 g. These values do not deviate from those observed in other population inhabiting European waters, where TL max ranges between 60 and 100 mm according to Záhorská et al. (2009, 2010). Like in other sites, this particular population is dominated by age groups 1+ and 2+, with maximum age 5+ (Rosecchi et al., 1993; Britton et al., 2007; Záhorská et al., 2010). This means that a large part of the population has reached sexual maturity (Záhorská et al., 2009) and, considering its high fecundity, the population maintains a strong reproductive potential (Katano and Maekawa, 1997; Záhorská and Kováč, 2009).

Males found in our catches had both greater lengths (SL and TL) and body weights. This sexual dimorphism (Barus et al., 1984; Britton et al., 2007) is linked with the reproductive behaviors of nest building and guarding by large, dominant males and batch spawning by females (Maekawa et al., 1996). Thus, it is reproductively advantageous for mature males to invest energy in somatic growth so that they may develop dominance through large body size, while mature females must invest heavily in gonad development throughout the breeding season so as to facilitate the production of several batches of eggs, reducing the available energy to invest in somatic growth (Maekawa et al., 1996; Britton et al., 2007). This explains the difference in the growth rates of males and females of stone moroko. Average total lengths attained at age 1 by males and females in the Wardynka creek were, respectively, 38.4 and 34.6 mm, remaining within the wide range (26–76 mm) reported in the literature for the species (Gozlan et al., 2010). The great variability of stone moroko body sizes at age 1 and older attained in various areas (Záhorská et al., 2010; Britton et al., 2007) result from the geographic latitude of the location, but

primarily from water temperature (Gozlan et al., 2010), population density (Britton et al., 2007), and hydrological conditions. A strong current in the river makes the fish spend more energy to maintain its body position in the flow and to catch quickly moving food organisms, which makes feeding harder and more costly in terms of energy (Sunardi and Manatunge, 2007).

The composition of food consumed by P. parva changes depending on the season (Adámek et. al., 1996) and body length (Kozlov, 1974). Juvenile fish are typical planktivores, mostly feeding on rotifers and copepods, less often on phytoplankton (Kozlov, 1974; Adámek et al., 1996; Hliwa et al., 2002; Yalçın-Özdilek et al., 2013). Moreover, our analysis shows that rotifers were the dominant food component of smaller stone moroko, although copepods and Chydorus cladocerans were also important dietary items. Along with the growth of length, greater feeding plasticity is observable. In the diet of adult fish, Muchaeva (1950) reported planktonic crustaceans of the families Chydoridae, Leptodotidae, and Bosminidae, but also chironomid larvae. Movchan and Kolzov (1978) also found algae, pieces of vascular plants, and larvae of Lochoptera, Trichoptera, and Chironomidae, whereas Giurca (1970) reported Oligochaeta, Chironomidae, and benthic forms of Cladocera. If we compare our findings with the dietary data reported by Adámek et al. (1996), the stone moroko in the Wardynka creek prefers invertebrates (Daphnia sp., Bosmina sp., Leptodora kindtti, and Chironomidae larvae). Wolfram-Wais et al. (1999) claimed that P. parva feeds nearly entirely on chironomids larvae and does not reveal significant seasonal changes in the share of this taxon in the diet. The most frequent benthic zone chironomid found in the stomachs of stone moroko living in the Wardynka creek was Chironomus sp. Moreover, the diet of largest-sized fish contained eggs and scales of other fishes, which corresponds with the findings of Jin et al. (1996) and Rosecchi et al. (1997). Adámek et al. (1996) described cases when stone moroko devoured scales and even injured skin and muscles of adult common carp (Cyprinus carpio carpio) and Prussian carp (Carassius gibelio). Libosvárský et al. (1990) emphasized that the shape of the jaw in stone moroko facilitates such type of behavior. Thus, besides its negative impact on native fish

Table 3. Prevalence, mean intensity of infection, intensity range, and relative density of parasites of stone moroko.

Index Total 2015 2016

P (%) 36.04 51.35 28.38MI 2.82 3.56 2.17IR 0–9 0–9 0–9A 0.86 1.54 0.53

P – Prevalence, MI – mean intensity of infection, IR – intensity range, A – relative density.

Table 4. Prevalence (%) of parasites from selected parts of fish body.

Parts of fish body Total 2015 2016

Eyes 1.80 0 2.70Gills 9.01 16.22 5.41Gastrointestinal tract 28.83 43.24 21.62

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communities as a food competitor (Holčik, 1991; Gozlan et al., 2010), stone moroko may also pose a direct threat to other fishes by injuring their tissues, which may cause infections, or by predation on fish eggs or larvae. For this reason, Trombicki and Kachowski (1987) consider the species a facultative parasite.

The main factor delimiting the distribution of a parasitic species is the presence of all the host organisms that the parasite needs to produce offspring and to survive in the inhabited ecosystem as a population. Parasites are able to invade new geographic regions and colonize new hosts; this, however, is usually possible with use of their

proper host organisms (Pojmańska and Niewiadomska, 2008). On the other hand, the plasticity of the parasite, i.e. its capability of finding a new host organism, is an important factor allowing the parasite to spread to new environments.

In its endemic region, stone moroko is a host organism for 56 pathogenic taxa (Yurishinets and Zaihenko, 2015), of which 73% are external parasites with a simple life cycle. Such organisms most easily succumb to the influences of the variable external environment, which is probably of importance when the host is transferred to distant geographical areas. The parasitic fauna of the

Table 5. Prevalence, mean intensity of infection, intensity range, and relative density of counted stone moroko parasite species.

SpeciesTotal 2015 2016

P MI IR A P MI IR A P MI IR A

Caryophyllaeus laticeps 4.50 1.60 0 -3 0.07 2.70 1.00 0 -1 0.03 5.41 1.75 0 -3 0.10Apatemon gracilis 1.80 5.50 0 -9 0.10 0 0 0 0 2.70 5.50 0 -9 0.15Cystidicola farionis 9.01 1.30 0 -2 0.12 18.92 1.29 0 -2 0.24 4.05 1.33 0 -2 0.05Pseudocapillaria tomentosa 19.82 2.77 0 -9 0.55 35.14 3.62 0 -9 1.27 12.16 1.56 0 -3 0.19Rhabdochona ergensi 1.80 1.50 0 -2 0.03 0 0 0 0 2.70 1.50 0 -2 0.04

P – Prevalence, MI – mean intensity of infection, IR – intensity range, A – relative density.

Table 6. Correlations between total length, standard length, weight, and Fulton index of fishes and the number of different parasites species (P < 0.05).

Caryophyllaeus laticeps

Apatemon gracilis

Cystidicola farionis

Pseudocapillaria tomentosa

Rhabdochona ergensi Total

Both yearsTL –0.041 0.155 0.335 0.204 –0.087 0.297SL –0.029 0.152 0.247 0.237 –0.078 0.307Weight –0.092 0.170 0.378 0.189 –0.087 0.291Fulton index –0.041 0.053 0.497 –0.004 –0.072 0.1142015TL –0.168 0.301 0.314 0.352SL –0.115 0.293 0.358 0.395Weight –0.148 0.370 0.310 0.365Fulton index –0.204 0.345 –0.143 –0.0722016TL 0.006 0.220 0.322 –0.139 –0.074 0.180SL –0.063 0.235 0.361 –0.169 –0.076 0.163Weight 0.018 0.226 0.119 –0.159 –0.065 0.138Fulton index –0.016 0.071 0.722 –0.125 –0.058 0.144

TL – Total length, SL – standard length.

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stone moroko in the Wardynka creek is composed of eight taxa, which are generalist species and in most cases infect other cyprinids as well (Lom and Dykova, 1992; Woo, 1995). In our catches other cyprinids like gudgeon (Gobio gobio), tench (Tinca tinca), bleak (Alburnus alburnus), and sunbleak (Leucaspius delineatus) were also noted. Besides the European waters, Trichodinella subtilis is found on the gills of cyprinid fishes in Asia (Wiles, 1968; Lom and Dykova, 1992), but not in stone moroko. The monogenean Diplozoon paradoxum has been spotted on other cyprinid fishes in Poland (Dzika, 2008), but P. parva is a new host organism for the platyhelminth.

The digenean Apatemon gracilis is a Holarctic species, in its adult form found in fish-eating birds, whereas its metacercariae have been noted in Poland’s waters in perch (Perca fluviatilis) and three-spined stickleback (Gasterosteus aculeatus). Presumably, A. gracilis is just beginning its colonization of stone moroko, as can be concluded from a very low prevalence of the parasite in 2016 and a complete lack of infections in the previous year.

T. tubifex is a common species in Poland (https://fauna-eu.org/) and is probably a first host of C. laticeps, which infects numerous cyprinid species. We also did not observe that the biological traits of stone moroko might have a significant influence on the infection intensity by this cestode (Table 6). Although initially low, the mean intensity of infection rose in 2016; thus, either a larger population of intermediate hosts was available in that year or C. laticeps is another parasite that gradually expands the spectrum of its host organisms by including stone moroko. In Japan, the cestode Archigetes sieboldii Leuckart, 1878 (Scholz et al., 2001) was found in P. parva; this parasite also occurred in the fish’s endemic region, where Triaenophorun amurensis, T. nodulosus, and Bothriocephalus acheilognathi have been observed (Yurishinets and Zaihenko, 2015).

The parasite community of stone moroko was quantitatively dominated by the nematode Pseudocapillaria tomentosa (Dujardin, 1843), which infected this host in Bulgaria and Ukraine, but has not been found in the endemic range of P. parva (Yurishinets and Zaihenko, 2015). Many cyprinid fishes are definitive hosts of the nematode, whereas oligochaetes Tubifex tubifex, Limnodrilus hoffmeisteri, and Lumbriculus variegatus were by experimental infection found to serve as intermediate hosts (Moravec, 1994). Later laboratory studies (Kent et al., 2002), however, revealed that the parasite might have a direct life cycle.

Cystidicola farionis Fischer, 1798, most often infects the swim bladder of salmonid and osmerid fishes, in Poland occurring in smelt Osmerus eperlanus (Dmitryjuk and Dziekońska-Rynko, 2016). It sporadically occurs in fishes of various families, which are facultative hosts. Juvenile larvae (L3) resemble adult ones and locate in the

anterior part of the gut. Intermediate hosts include benthic amphipods: Gammarus pulex, Pontoporeia affinis, and Hyalella azteca (Moravec, 1994). In the digestive tracts of stone moroko, we found remains of Gammarus sp., which out of three host amphipods is the only genus occurring in Poland (https://fauna-eu.org/); thus, for stone moroko, it is a source of infection with the nematode C. farionis. It is possible that the positive significant correlation between parameters like TL, weight, KF, and number of C. farionis nematodes is related to the availability of ecological niches. As the host grows, the potential habitat for parasites increases; however, it is difficult to clearly pinpoint it (Poulin, 1999, 2000). The reduction in the number of parasites may be limited as a result of interspecies competition; this may be reflected in the lack of correlation between other intestinal parasites, such as C. laticeps, A. gracilis, or R. ergensi and the size and weight of the fishes. Significant negative correlation between the number of C. farionis and condition factor KF may indicate the harmful effects of this parasite.

Rhabdochona ergensi Moravec, 1968, was noted in stone moroko in Ukrainian waters; however, it never occurred in its endemic distribution area (Yurishinets and Zaihenko, 2015). An experiment demonstrated that the first intermediate host is the nymph of mayfly, Habroleptoides modesta, which does not occur in Poland (https://fauna-eu.org/); in the natural environment, however, other species may be hosts, too (Moravec, 1972). The diet of stone moroko from the Wardynka creek contained chironomid larvae, whose percentage by weight was highest in the largest fish, while the parasite was found in the sample from the second year only.

In conclusion, length and age compositions of stone moroko in the new site of its distribution are similar to those in other nonendemic populations of the fish, with a clear domination of age groups 1+ and 2+, at TL classes 40.1–45.0 mm (13.43%), 45.1–50.0 mm (23.22%), and 50.1–55 mm (12.66%). We also noted the previously described sexual dimorphism expressed as lower lengths (TL) and body weights of females compared to males. The growth rate was typical for short-lived fishes, more intensive in the first 1–2 years of life and weaker in the following years. Rotifers and copepods occurred most frequently in the diets of younger fish. Food composition changed with the length of the body; the dominant food components of older fish were planktonic crustaceans, mostly cladocerans, but also the larvae of insects like chironomids, trichopterans, and dipterans; however, fish eggs and scales were also found in the digesta.

Our studies on the parasitic fauna demonstrate that the transfer of the host to a new environment results in removal or reduced numbers of the parasites occurring in the endemic region of the fish. The fauna of parasitic

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organisms infecting the fish in its new location is formed by local, common species. This is also the case of the analyzed population of stone moroko, which is a host organism for four new parasites, native in the waters of

Poland. It is unclear whether the ciliate Ch. piscicola is an accidentally introduced species or not. Since P. parva is invading new areas, the general list of stone moroko parasites will probably expand.

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