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464 http://journals.tubitak.gov.tr/zoology/ Turkish Journal of Zoology Turk J Zool (2018) 42: 464-474 © TÜBİTAK doi:10.3906/zoo-1710-16 e invasive Ameiurus nebulosus (Lesueur, 1819) as a permanent part of the fish fauna in selected reservoirs in Central Europe: long-term study of three shallow lakes Jacek RECHULICZ*, Wojciech PŁASKA Department of Hydrobiology and Protection of Ecosystems, University of Life Sciences in Lublin, Lublin, Poland * Correspondence: [email protected] 1. Introduction In recent decades, the presence of invasive species of fish has become a significant problem in many countries in Europe. e causes and pathways of the invasions of new species to other continents or to new nonnative areas are well known. Among them we can distinguish: aquaculture—increasing fish production, fishing and other hobbies related to fish, ignorance, and lack of knowledge (Holčík, 1991). e brown bullhead, Ameiurus nebulosus (Lesueur, 1918), comes from North America, where it naturally occurs in the Mississippi and Missouri river catchment areas. In the second half of the 19th century, it was introduced to several European countries (e.g., Germany, UK, France, Netherlands, Belgium, and Austria) (Welcomme, 1988). One of the main reasons for the introduction of the brown bullhead into Europe was aquaculture along with developing new resources for fishing and angling (Wheeler, 1978; Witkowski, 2002; Nowak et al., 2008; Grabowska et al., 2010). However, this species, due to its biological and physiological features, spread almost throughout Europe and became a problem for many aquatic ecosystems of areas it invaded (Holčík, 1991). Possible reasons for the success of this invasion of the brown bullhead populations are their potential to survive in sediment during short periods of drought, a high degree of parental care (Blumer, 1985), and also a lack of natural enemies due their ability to erect dorsal and pectoral spines as a defense against predators (Scott and Crossman, 1973; Kornijów, 2001; Moldowan et al., 2015), and their tolerance of a variety of environmental stressors such as contaminants (Pyron et al., 2001) and very low oxygen concentration (less than 0.2 mg L –1 ). According to many sources cited by Rutkayova et al. (2013), the brown bullhead is found in many European countries. As reported by Holčík (1991), in water bodies in many regions, it creates a stable population and has a large share in the fish fauna. However, in the available sources, there is no information about the range of its occurrence, abundance, or other features that characterize its populations. In particular, this applies to the regions where the brown bullhead has made a successful colonization as an invasive species. e study of this species is undoubtedly hampered by a lack of adequate sampling methods (Michaletz and Dillard, 1999). In Poland, the presence of the brown bullhead was recorded for the first time in 1885 in ponds in the province of Western Pomerania (Horoszewicz, 1971). However, the information about the spread of this species in Poland was not documented but it is known that in the early 1920s Abstract: e invasive brown bullhead (Ameiurus nebulosus (Lesueur, 1918)) has been present in Europe since the late 19th century, but there is still a lack of reliable information about its distribution in Europe and the condition of its population. A long-term study (from 2000 to 2011) in three shallow lakes in Central Europe (eastern Poland) was carried out to determine the occurrence of the brown bullhead and its participation in the fish community. e brown bullhead was present in almost all the sampling fishing in all the lakes studied (C i = 72%–82%). Its mean abundance and share in the fish biomass ranged from 4.2% to 13.6% and from 9.4% to 18.9%, respectively. e relative numbers of the brown bullheads ranged from 6.4 to 9.1 NPUE (ind. net –1 12 h –1 ) and relative biomass from 197.9 to 430.2 WPUE (g net –1 12 h –1 ). In total, the brown bullheads with a total length from 12 to 20 cm were the most common in the surveyed lakes. e results showed that the brown bullhead, because of the constancy of occurrence and the size class structure of specimens, had stable populations in the selected lakes in Poland. Key words: Ameiurus nebulosus, invasive species, shallow lake, population state, long-term study Received: 20.10.2017 Accepted/Published Online: 16.05.2018 Final Version: 26.07.2018 Research Article

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Page 1: The invasive Ameiurus nebulosus (Lesueur, 1819) as a ...journals.tubitak.gov.tr/zoology/issues/zoo-18-42-4/zoo-42-4-12-1710-… · sampling methods (Michaletz and Dillard, 1999)

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

Turkish Journal of Zoology Turk J Zool(2018) 42: 464-474© TÜBİTAKdoi:10.3906/zoo-1710-16

The invasive Ameiurus nebulosus (Lesueur, 1819) as a permanent part of the fish fauna in selected reservoirs in Central Europe: long-term study of three shallow lakes

Jacek RECHULICZ*, Wojciech PŁASKADepartment of Hydrobiology and Protection of Ecosystems, University of Life Sciences in Lublin, Lublin, Poland

* Correspondence: [email protected]

1. IntroductionIn recent decades, the presence of invasive species of fish has become a significant problem in many countries in Europe. The causes and pathways of the invasions of new species to other continents or to new nonnative areas are well known. Among them we can distinguish: aquaculture—increasing fish production, fishing and other hobbies related to fish, ignorance, and lack of knowledge (Holčík, 1991).

The brown bullhead, Ameiurus nebulosus (Lesueur, 1918), comes from North America, where it naturally occurs in the Mississippi and Missouri river catchment areas. In the second half of the 19th century, it was introduced to several European countries (e.g., Germany, UK, France, Netherlands, Belgium, and Austria) (Welcomme, 1988). One of the main reasons for the introduction of the brown bullhead into Europe was aquaculture along with developing new resources for fishing and angling (Wheeler, 1978; Witkowski, 2002; Nowak et al., 2008; Grabowska et al., 2010). However, this species, due to its biological and physiological features, spread almost throughout Europe and became a problem for many aquatic ecosystems of areas it invaded (Holčík, 1991). Possible reasons for the success of this invasion of the brown bullhead populations are their potential to survive in sediment during short

periods of drought, a high degree of parental care (Blumer, 1985), and also a lack of natural enemies due their ability to erect dorsal and pectoral spines as a defense against predators (Scott and Crossman, 1973; Kornijów, 2001; Moldowan et al., 2015), and their tolerance of a variety of environmental stressors such as contaminants (Pyron et al., 2001) and very low oxygen concentration (less than 0.2 mg L–1).

According to many sources cited by Rutkayova et al. (2013), the brown bullhead is found in many European countries. As reported by Holčík (1991), in water bodies in many regions, it creates a stable population and has a large share in the fish fauna. However, in the available sources, there is no information about the range of its occurrence, abundance, or other features that characterize its populations. In particular, this applies to the regions where the brown bullhead has made a successful colonization as an invasive species. The study of this species is undoubtedly hampered by a lack of adequate sampling methods (Michaletz and Dillard, 1999).

In Poland, the presence of the brown bullhead was recorded for the first time in 1885 in ponds in the province of Western Pomerania (Horoszewicz, 1971). However, the information about the spread of this species in Poland was not documented but it is known that in the early 1920s

Abstract: The invasive brown bullhead (Ameiurus nebulosus (Lesueur, 1918)) has been present in Europe since the late 19th century, but there is still a lack of reliable information about its distribution in Europe and the condition of its population. A long-term study (from 2000 to 2011) in three shallow lakes in Central Europe (eastern Poland) was carried out to determine the occurrence of the brown bullhead and its participation in the fish community. The brown bullhead was present in almost all the sampling fishing in all the lakes studied (Ci = 72%–82%). Its mean abundance and share in the fish biomass ranged from 4.2% to 13.6% and from 9.4% to 18.9%, respectively. The relative numbers of the brown bullheads ranged from 6.4 to 9.1 NPUE (ind. net–1 12 h–1) and relative biomass from 197.9 to 430.2 WPUE (g net–1 12 h–1). In total, the brown bullheads with a total length from 12 to 20 cm were the most common in the surveyed lakes. The results showed that the brown bullhead, because of the constancy of occurrence and the size class structure of specimens, had stable populations in the selected lakes in Poland.

Key words: Ameiurus nebulosus, invasive species, shallow lake, population state, long-term study

Received: 20.10.2017 Accepted/Published Online: 16.05.2018 Final Version: 26.07.2018

Research Article

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in Silesia (southwestern Poland) it was found (Pax, 1925). Then, before World War II, it was also found in the Bug River basin (the eastern part of Poland). Currently, as reported by Grabowska et al. (2010), knowledge of the occurrence of the brown bullhead in Poland is very poor. We can only find a mention of its occurrence in different water ecosystems, both lentic and lotic, in the work by Kusznierz et al. (1994), who caught it in the river basins of the Stobrawa and Smotrawy rivers. Furthermore, single individuals of this species in the upper Warta River were noted by Kruk et al. (2001) and also by Kapusta et al. (2010) in the catchment basin of the River Lyna. It was also found in some lakes in the Masurian Lake District (Brylinski and Chybowski, 2000) and in fish ponds in the Karkonosze Mountains (Witkowski et al., 2014).

In 1937, the brown bullhead was transferred to eastern Poland to Lake Łukie (Polesie region) (Witkowski, 1996) and from there spread out to the lakes of Łęczna-Włodawa Lakeland through many channels. In this region, this fish occurs in both rivers (Danilkiewicz, 1973) and lakes (Adamczyk, 1975; Kolejko, 1998). The modest information that is available about the presence of the brown bullhead in eastern Poland testifies to the fact that this species is present, and sometimes forms a large component of the fish fauna (Kornijów et al., 2003). At the same time, in some lakes in this region, the brown bullhead has established stable populations (Rechulicz et al., 2015).

The brown bullhead as a nonindigenous invasive species in Europe can negatively affect the native ecosystems. This influence may be direct by predation and competition for food, or indirectly by occupying the same habitat. In either case, the brown bullhead must share habitats with native fish species (Coop et al., 2005; Gozlan, 2008; Grabowska et al., 2010).

The presence of an invasive species of fish is often recorded during the conducting of a regular inventory or the monitoring of water ecosystems. Usually, the single individuals are recorded as evidence of the spread of undesirable species in a new area. However, observations of new invasive species are extremely difficult in the newly invaded areas often due to imperfect methodology, usually because they are small in number, as well as the need for long-term observation. All these arguments contribute to a great underestimation of the number of invasive species and their participation in the fish community. Similarly, for the brown bullhead, where there is still limited information about the distribution of the species and the lack of publications concerning the state of the population in Central Eastern Europe. Accordingly, the long-term observation (for a period of 10 years) was carried out in three lakes where the occurrence of the brown bullhead was recorded. The aims of our study were to: i) verify the thesis that the brown bullhead was a permanent part of the

fish fauna of the lakes studied for a period of 10 years, ii) determine the occurrence, abundance, and relative share of the brown bullhead in the fish fauna in the three shallow lakes of eastern Poland, iii) identify the characteristics of the selected parameters of the populations of the brown bullhead as a nonindigenous species in Central Eastern Europe.

2. Materials and methods2.1. Study area The studies were conducted in three lakes: Rotcze, Sumin, and Głębokie Uścimowskie (also known as Głębokie), situated in eastern Poland in the Łęczna–Włodawa Lakeland (Central Eastern Europe) (Figure 1). The lakes are small and shallow. The surface area of the lakes studied does not exceed 100 ha and the maximum depth ranges from 1.3 to 7.1 m (Table 1). The land use in their drainage basin differs substantially. In consequence, they differ much in terms of the content of nutrients, and so in fertility and represent different trophic statuses: mesotrophic, Lake Rotcze; eutrophic, lakes Sumin and Głębokie Uścimowskie (Kornijów et al., 2003). The abundance of submerged and floating leaved macrophytes strongly differed among the lakes, being the highest in Lake Rotcze (Table 1). In this lake, the most abundant were charophytes (Chara fragilis and Ch. hispida), in Lake Głębokie Uścimowskie - elodeids (mostly Myriophyllum spicatum and Elodea canadensis), and in Lake Sumin - mainly nymphaeids, represented by Nymphaea candida and Potamogeton natans (Kornijów et al., 2002).

In Lakes Rotcze and Sumin, regular fishery management is carried out by the Polish Angling Association (PAA) Chełm (annual fish stocking) and fishing is limited to amateur angling; however, Lake Głębokie has multiple

Figure 1. Locations of the lakes studied.

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owners and the fish fauna is poorly managed (e.g., lack of fish stocking) and is sometimes used by amateur anglers.2.2. Fish sampling and data analysisThe studies were conducted three times each year (during vegetation season) from 2000 to 2011. In 2000 and 2001, fish were caught using S-REV Norden multimesh gill nets (14 segments with different mesh sizes: 10, 60, 30, 6.25, 43, 22, 50, 33, 12.5, 25, 8, 38, 75, and 16.5 mm). From 2007 to 2011, the samples were collected using multimesh gillnet type of new standard (1.5 m deep, 30 m long, 12 mesh sizes from 5 mm to 55 mm knot-to-knot) (Appelberg, 2000; CEN document, 2005). In all the lakes studied the nets were located at the depth of 0.7–3 m, both parallel as well as perpendicularly to the lake shore, starting from

the outer edge of the helophyte belt. The nets were set in the evening and retrieved the following early morning. In Table 2, the years of research and the number of gill nets used in each lake are shown.

All the fish caught were determined as to their species, and their total length (Tl) (in cm) and body mass (W) (in g) were measured. The coefficient of occurrence (Ci) of the brown bullhead was calculated by the following formula: Ci = 100 × si/st, where si is the number of samples where the brown bullhead was present and st is the total number of samples (nets). The abundance (D%) and biomass dominance (W%) of the brown bullhead in the total ichthyofauna of the lakes were calculated using the following formulae: D% = 100 × ni/N and W% = 100 × wi/W;

Table 1. Characteristics of lakes, their catchment basin, hydrochemical properties of water, and the development of submerged and floating-leaved macrophytes expressed as percentage volume infested (PVI) (Kornijów et al., 2002; Smal et al., 2005 – modified).

Lake Rotcze Sumin Głębokie

GPS coordinates 23°6′44.43″E51°22′32.43″N

23°8′19.96″E51°22′32.48″N

22°55′23.04″E51°28′34.08″N

Lake surface (ha) 45.8 85.6 20.3Maximal depth (m) 4.3 6.5 7.1Mean depth (m) 1.9 1.6 3.4Total catchment area (ha) 157.2 1403.6 173.8Forests and shrubs (%) 10.5 9.5 1.0Arable land (%) 26.2 35.6 73.5Total P (µg dm–3) 41.4 75.5 146.6Total N (mg dm–3) 1.19 1.56 1.41Chlorophyll a (µg dm–3) 4.8 16.3 102.1Macrophytes (PVI, %) 34.50 3.30 0.75

Table 2. The years of fish sampling, numbers of used nets, total numbers (NPUE), and biomass (WPUE) of caught fishes in the lakes studied.

Lake 2000 2001 2007 2008 2009 2010 2011 Total

GłębokieNo. of nets 4 4 - 7 7 8 8 38Total NPUE 156 282 - 226 110 329 102 1205Total WPUE 5964 4539 - 4384 3666 9052 3607 31,212

SuminNo. of nets 4 4 10 10 10 12 - 50Total NPUE 352 364 5348 1188 815 846 - 8913Total WPUE 6815 5471 82,040 20,971 22,115 17,668 - 155,080

RotczeNo. of nets 4 4 10 10 10 12 - 50Total NPUE 80 42 572 175 676 1020 - 2565Total WPUE 2730 1452 18,378 5585 22,659 21,925 - 72,729

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where ni is the number of brown bullhead individuals, N is the total number of all fish, wi is the biomass of the brown bullhead, and W is the total biomass of all fish.

All the fish data that were obtained in control net fishing were converted to catch per unit effort (NPUE and WPUE). For the relative numbers, the NPUE, it was the number per unit effort, i.e. the number of individual fish caught in one net after 12-h fishing (ind. net–1 12 h–1), and for the relative biomass, WPUE, it was weight per unit effort, i.e. fish biomass (in g) of the fish caught in one net after 12 h of fishing (g net–1 12 h–1).

The coefficients of condition (Fulton’s condition factor; K) for the brown bullhead from the three lakes studied were calculated using the following formula: K = W105 × Tl–3 (Mills and Eloranta, 1985; Williams, 2000).

The distribution of normality and homogeneity of variance were calculated for all examined parameters. The share of the brown bullhead in the total number and biomass of all fish and also its relative numbers (NPUE) and relative biomass (WPUE) between the lakes using the nonparametric Kruskal–Wallis ANOVA were compared. Moreover, the statistical significance of the differences between the brown bullhead total length (Tl), body weight (W), and coefficient of condition (K) of fish from all the lakes studied was examined. The relationship between log-transformed data of the relative number of brown bullhead and relative numbers of all fish from the lakes studied was calculated. In addition, Spearman correlation was calculated between the abundance and biomass of A. nebulosus and other fish species. This could give information on the possible occupation of the same habitat by the brown bullhead and other species of fish.

Frequency of the brown bullhead Tl was determined using the Kolmogorov–Smirnov test and fitting for log-normal distribution. All the analyses and statistical tests

described above were carried out using the StatSoft Statistica package for Windows at a significance level of P ≤ 0.05.

3. ResultsIn total in the study, over 12 000 fish individuals belonging to 17 species and 4 families (Cyprinidae, Percidae, Esocidae, and Ictaluridae) were caught. The highest species richness was recorded in Lake Głębokie (14) and the smallest in Lake Sumin (10). The fishing results showed that the brown bullhead in all the lakes studied was constantly present. The calculated coefficient of occurrence for the brown bullhead in the lakes Głębokie, Sumin, and Rotcze reached 81.8%, 72.0%, and 74.0%, respectively (Table 3).

The abundance (D%) of the brown bullhead varied depending on the lake and the year of sampling. The significantly higher (Kruskal–Wallis test: H (2, N = 137) = 9.82, P = 0.007) overall average abundance of the brown bullhead was noted in Lake Rotcze (13.6%) as compared with lakes Głębokie and Sumin, where it amounted to 10.2% and 4.2%, respectively (Table 3). The greatest variability of abundance of the brown bullhead in each year of research was also recorded in Lake Rotcze (SD ± 14.77). In 2000 and 2001, the average abundance was close to 35%, while the smallest abundance was recorded in 2008 (4.6%). Similarly, the largest share in the biomass of this species was in Lake Rotcze (average 18.9%) and the lowest in Lake Sumin (average 9.40%) (Table 3).

The greatest relative numbers of the brown bullhead in the lakes were recorded in Lake Rotcze (9.13 NPUE). Slightly less (P > 0.05) on average NPUE values in the range 6.4–6.6 were noted in the other two lakes (Table 3). Exceptionally increased numbers of the brown bullhead were observed in Lake Głębokie in 2008, in Lake Sumin in 2007 and 2008, and in Lake Rotcze between 2007 and 2010

Table 3. Abundance (D%), share in biomass of all fish (W%), relative numbers (NPUE), relative biomass (WPUE), and coefficient of occurrence (Ci) of the brown bullhead from lakes studied; SD – standard deviation; A, B – means in row marked with the same letter do not differ significantly at P ≤ 0.05.

Lake Głębokie Sumin Rotcze

D%Mean ± SD 10.20AB ± 10.40 4.17B ± 6.91 13.64A ± 14.77Min–Max 0.00–36.57 0.00–37.11 0.00–54.31

W%Mean ± SD 12.10 ± 13.90 9.40 ± 13.87 18.93 ± 27.04Min–Max 0.00–59.69 0.00–54.69 0.00–100.00

NPUEMean ± SD 6.43 ± 11.28 6.57 ± 10.65 9.13 ± 14.09Min–Max 0.00–49.00 0.00–46.00 0.00–63.00

WPUEMean ± SD 197.89 ± 321.59 327.28 ± 556.47 430.20 ± 815.36Min–Max 0.00–1347.00 0.00–2660.00 0.00–3514.50

Ci 81.81 72.00 74.00

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(Figure 2). Relative standard biomass, despite the different values among the lakes, was similar (P > 0.05). The greatest value (430.2 WPUE) was determined in Lake Rotcze and the smallest (197.9 WPUE) in Lake Głębokie (Table 3).

Analysis of the values of all parameters of the population of the brown bullhead within individual lakes in all years of the study showed that in Lake Głębokie significant differences in the abundance (D%) and the relative numbers of fish (NPUE) were noted (for D%, K–W test: H (6, N = 37) = 13.71, P = 0.033; for NPUE, K–W test: H (6, N = 37) = 13.53, P = 0.035). In Lake Sumin, only the relative biomass of the brown bullhead (WPUE)

varied in individual years of the research (K–W test: H (6, N = 49) = 13.40, P = 0.037), whereas in Lake Rotcze all these parameters such as abundance, biomass, and share in the fish community of the brown bullhead were significantly different (P < 0.05) over the years.

The abundance of the brown bullhead (D%) in lakes Rotcze and Głębokie decreased from 2000 to 2011, but, as analysis of regression showed, these changes were significant only in Lake Rotcze (P = 0.002) (Figure 3a; Table 4). As for the share of the brown bullhead in the fish biomass (W%) from all the lakes studied, the changes were less diverse. A slight increase in the share of the brown bullhead in the fish biomass was recorded only in Lake Rotcze (Figure 3b).

Analysis of the results showed that the relative numbers of the brown bullhead were positively correlated (P < 0.05) with the total numbers of fish in only two of the lakes studied (lakes Rotcze and Głębokie) (Figure 4). In all the lakes, the abundance of the brown bullhead was mostly positively correlated with the abundance of some fish species (Table 5). In particular, in Lake Głębokie, a high positive correlation was found between A. nebulosus and the roach (P < 0.05). In Lake Sumin, a high positive correlation was determined between A. nebulosus and the white bream and a slightly lower one between A. nebulosus and the bleak, roach, and pike-perch. In Lake Rotcze, the number of the brown bullhead was highly and significantly (P < 0.05) correlated with the bleak, roach, and European perch, and slightly less (but significantly) with the white bream and rudd (Table 5).

Analysis of the size structure of the brown bullhead of the individual populations demonstrated that in Lake Głębokie specimens with a total length (Tl) of 12–14 cm dominated, while in the other two lakes fish with a total length of 16–20 cm dominated. Simultaneously, the analysis of normality of length distributions showed that the distribution of the total length of the brown bullhead from all three populations studied was nonnormal (Lake Głębokie, K–S: D = 0.202, P < 0.01; Lake Sumin, K–S: D = 0.155, P < 0.01; Lake Rotcze, K–S: D = 0.173, P < 0.01) (Figure 5).

Overall, the larger and heavier brown bullhead individuals were caught in lakes Rotcze and Sumin. Their average total lengths were 16.0 cm and 15.6 cm and weights were 53.2 g and 47.7 g, respectively. Significantly shorter and lighter individuals of this species in Lake Głębokie were caught (for Tl, K–W test: H (2, N = 599) = 26.76, P < 0.001; for W, H (2, N = 599) = 24.91, P < 0.001) (Table 6), whereas the analyzed fish had a similar coefficient of condition (K) and it amounts to an average of 1.14 for the fish from lakes Sumin and Rotcze and 1.13 for the fish from Lake Głębokie (Table 6).

Figure 2. The relative numbers of the brown bullhead (NPUE) in the lakes studied in 2000–2011; the box plots with different letters are significantly different at P ≤ 0.05.

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4. DiscussionThe current paper documents one of the first studies describing the occurrence and characteristics of selected populations of the brown bullhead in Central Eastern Europe. In eastern Poland the brown bullhead was repeatedly noted, but the information on the status of

its population was often perfunctory. It was limited to determining the occurrence and share in the abundance and biomass of the fish community in selected water bodies. As demonstrated by the present study, the brown bullhead was a constant element in the selected lakes of the Łęczna-Włodawa Lakeland, but often had varied participation in the fish community (Table 3). According to the results reported by Kolejko (1998) and Kornijów et al. (2003), in some water bodies in this region the brown bullhead may be the dominant species in the abundance and biomass of caught fish. For example, between 2003 and 2005 in Lake Skomielno, which is also located in the Łęczna-Włodawa Lakeland, by selective fishing using fyke nets, over 6000 kg of the brown bullhead was harvested (Rechulicz, 2012). Our research showed that in the lakes studied the brown bullhead occurred in small but regular and repeated numbers in the fish fauna (Table 3; Figure 2). In all three of the surveyed lakes, this was also demonstrated by high values of coefficient of occurrence determined for this species (Table 3). In recent years in Lake Domaszne, located near the surveyed lakes, 100% stability of the occurrence of the brown bullhead was determined. Moreover, the participation of this species in abundance and total biomass in the fish fauna was comparable, as in the lakes studied, and had average values of 2.7% and 7.5%, respectively (Rechulicz et al., 2015).

The relatively small quantities of the brown bullhead found in the lakes studied may have been due to the method of sampling, viz. the use of gill nets. So far, to evaluate the occurrence of the brown bullhead, as well as a relative with similar habitat requirements, the black bullhead (Movchan et al., 2014), different methods of sampling have been used. Amongst these are such things as a survey by angling (Miranda, 1999); seining, dip-netting, and cage trapping (Harvey and Fortin, 1982); gill-netting and electro-fishing (Michaletz and Dillard, 1999); and fyke netting (Brazner et al., 1998; Hanchin et al., 2002). However, as reported by Louetta and Declerck

Figure 3. Regression describing the changes in abundance (D%) (a) and share in the biomass of the brown bullhead (W%) (b) in the total fish biomass in the lakes studied.

Table 4. Values of regression parameters describing the changes in abundance (D%) and share in biomass (W%) of the brown bullhead in all fish in the lakes studied; *statistical differences at P ≤ 0.05.

Lake a b r2 P

GłębokieD% 983.596 −0.485 0.037 0.391W% −227.821 0.119 0.001 0.875

SuminD% −394.542 0.199 0.006 0.588W% −1107.424 0.556 0.012 0.449

RotczeD% 4566.391 −2.268 0.173 0.002*W% −4142.679 2.073 0.043 0.132

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(2006), no efficient standard technique is currently available. The most effective, though not perfect, seems the use of trap nets, for example fyke nets. According to many authors, it is a very effective tool for the removal of brown bullhead populations from small to medium-sized shallow water bodies (Declerck et al., 2002; Hanchin et al., 2002; Kornijów et al., 2003; Louette and Declerck,

2006). However, these tools, because of their construction and operation, are not suitable for the assessment of the whole fish fauna in water bodies. Therefore, as reported by Louette and Declerck (2006), the recapture efficiency of fyke nets was higher for the brown bullhead than for other species of fish communities. In turn, the standard tool for research of the fish fauna in the lake (gill net) can be a little understated, but yield the only possible results in order to know the whole fish community (Hanchin et al., 2002). The effectiveness of using different types of tools (gill nets and fyke nets) for sampling of the black bullhead was studied by Hanchin et al. (2002). It turned out that the trap nets and experimental gill nets provided similar indices of population size structure, but the trap nets might provide a better index of relative abundance for black bullhead population monitoring.

Several years of observation of the changes in the participation of the brown bullhead in the total fish fauna indicate that its share showed a decreasing trend in two of the lakes surveyed (i.e. Rotcze and Głębokie). Simultaneously, the share of the brown bullhead in the total biomass of fish slightly increased (Figure 3; Table 4). This trend was observed especially in Lake Rotcze. This may indicate an aging of the brown bullhead population and an increasing individual mass of specimens. This phenomenon could be explained by way of the use of Lake Rotcze. Lake Rotcze is a small reservoir and due to its location and management it is appealing recreationally, including intensive usage by anglers (PAA Chełm, 2011). The location provides access to the lake from almost every side, and it is also confirmed by numerous platforms used for amateur fishing. By contrast, the other two lakes, due to their location or management, are not as intensively used by anglers. In Lake Sumin, only a small portion of the shoreline (the southeast side) is suitable for angling (PAA Chełm, 2011). This is a major limitation because the majority of anglers must use a boat for fishing. In turn, Lake Głębokie is poorly managed; no fishery management is carried out on it. Moreover, its location near the center of the village is not conducive to angling (Płaska and Rechulicz, 2012). The brown bullhead, because of its participation in the fish fauna and high voracity, is a frequent trophy for anglers. Additionally, because of its delicious meat and the small amount of fish bones, it is eagerly fished by them and taken away. Probably, in Lake Rotcze, this may have the effect of reducing its abundance and consequently decreased its share in the fish community. Simultaneously, it could also cause an increase in its individual mass by reducing intraspecific competition for habitat and food (Figure 3; Table 6).

The current study showed that the brown bullhead occupied habitats similar to those of some native fish species (Table 5). This may indicate that A. nebulosus is

0.6 0.8 1.0 1.2 1.4 1.6 1.8 2.0 2.2log Total NPUE

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Figure 4. Relationship between the relative numbers of the brown bullhead and the total relative numbers of fish (data log-transformed) in the lakes studied; a) Głębokie, b) Sumin, c) Rotcze.

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staying in places where the potential food, small specimens of fish such as the bleak and roach, are present (Declerck et al., 2002). However, these relationships require a more accurate and deeper analysis.

The introduction of the brown bullhead as a new species into Europe not only created new interactions between it and the ecosystem but also affected some of its morphological features. According to Scott and Crossman (1973), adults of this species reach a much larger body size in its natural range of occurrence. As reported by Breckels and Neff (2010), the total length of the brown bullhead in southwestern Ontario was in the range of 24.9 to 26.2 cm. Similarly, Meier et al. (2015), examining the brown bullhead from two rivers in northeastern Ohio (USA), noted that their lengths ranged from 27.0 to 35.4 cm. This suggests that these fish were almost twice the size of the brown bullhead caught in our research (Table 6). In other studies conducted in Poland by Pokorny et al. (2015) (Stawno Fishing Farm in the Milicz Ponds in southwestern Poland), brown bullheads with a slightly larger total length (up to 30 cm) were caught. Despite this, the determined condition factor (K = 1.13) was the same as for the brown bullhead from lakes Głębokie, Sumin, and Rotcze (Table 6). Similar to the results of our study,

in another relatively recently (early 80s) invaded area in New Zealand, Lake Taupo (Barnes and Hicks, 2003) and Waikato drains (Bannon HJ (2001). Biological responses to grass carp (Ctenopharyngodon idella) in Waikato drains. Unpublished MSc thesis, University of Waikato, Hamilton, New Zealand.), brown bullheads with smaller body sizes (<13 cm FL) were found. Interestingly Craig et al. (2015) caught brown bullheads with a total length of 13.8 cm in North America, but beyond the reach of their natural occurrence, in Texas. As it turned out, the sizes of the fish were smaller than those naturally found on this continent. According to Keast (1985) and Rypel (2011), a major influence on the growth and size of this species may have been climatic conditions, in particular temperature, which is conditioned by geographical location. Maybe the climate was decisive in limiting the growth of the brown bullhead in Europe. On the other hand, according to Rypel (2014), comparison of the growth rate of the population of native and invasive brown bullheads showed no significant differences depending on the area occupied.

Analysis of size structure of the brown bullhead from the lakes studied showed that all these populations had different proportions of various length class (Figure 5). In two of the surveyed lakes (Sumin and Rotcze), the

Table 5. Spearman correlations between the abundance and the biomass of the brown bullhead and other fish species present in the lakes studied in 2000–2011; * — correlation significant at P ≤ 0.05.

Głębokie Sumin Rotcze

Abundance Biomass Abundance Biomass Abundance Biomass

Ruffe (Gymnocephalus cernua) 0.024 −0.056 0.168 −0.082 - -

Prussian carp (Carassius gibelio) −0.143 −0.068 −0.188 −0.181 −0.069 0.148

White bream (Blicca bjoerkna) −0.087 −0.090 0.684* 0.574* 0.339* 0.548*

Bleak (Alburnus alburnus) 0.331 0.416 0.348* 0.272 0.612* 0.740*

Roach (Rutilus rutilus) 0.541* 0.486* 0.284* 0.196 0.560* 0.801*

Common carp (Cyprinus carpio) 0.278 0.293 - - - -

Gudgeon (Gobio gobio) 0.260 0.120 - - - -

Rudd (Scardinius erythrophthalmus) −0.226 −0.053 - - 0.319* 0.690*

Belica (Leucaspius delineatus) −0.227 −0.047 - - - -

European perch (Perca fluviatilis) 0.304 0.119 0.204 −0.144 0.707* 0.621*

Northern pike (Esox lucius) 0.337 0.234 0.117 0.139 0.020 0.257

Freshwater bream (Abramis brama) 0.152 0.026 0.093 −0.234 −0.022 −0.170

Crucian carp (Carassius carassius) 0.330 0.259 - - 0.261 −0.023

Pike-perch (Sander lucioperca) - - 0.430* 0.174 - -

Bitterling (Rhodeus sericeus) - - - - −0.338* 0.131

Tench (Tinca tinca) - - - - 0.175 0.016

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individual fish with slightly larger overall lengths (>16 cm) were dominant. This may indicate an aging population and its stability in the lakes studied (Krebs, 2009).

The surveys carried out indicate that this species has colonized Europe and has, perhaps, not numerous but stable populations in many water bodies. Simultaneously,

in some regions of Poland and Europe, several authors indicate a slightly steady decrease in the abundance of this species (Kusznierz et al., 1994; Kruk et al., 2001; Verreycken et al., 2007).

A small number of studies on the occurrence and population status of the brown bullhead in Europe

Table 6. Total length (Tl, in cm), body weight (W, in g), and coefficient of condition (K) of the brown bullhead from lakes studied, SD – standard deviation, A, B – means in row marked the same letter are not significantly different at P ≤ 0.05.

Lake Głębokie Sumin Rotcze

N 126 245 228

TlMean ± SD 14.27B ± 2.54 15.66A ± 3.14 16.00A ± 3.71Min–Max 9.50–23.50 7.50–24.10 7.00–24.20

WMean ± SD 36.48B ± 24.23 47.72A ± 26.49 53.20A ± 32.53Min–Max 10.00–170.00 4.00–195.00 4.00–182.60

KMean ± SD 1.13 ± 0.19 1.14 ± 0.16 1.14 ± 0.23Min–Max 0.75–1.80 0.72–1.66 0.61–2.03

Figure 5. Distributions of total length (Tl) of the brown bullhead from the lakes studied; a) Głębokie, b) Sumin, c) Rotcze.

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indicate the need for further research on this topic. Particularly important may be a study to determine the potential impact of the occurrence of the brown bullhead on water ecosystems, especially on native fish species with which it coexists. Extremely important may be more accurate knowledge of their habitat preferences and diet composition, which directly affect native species in competition for habitat and food sources.

AcknowledgmentsThe field works in 2000 and 2001 were carried out as a part of the ECOFRAME project no EVK1-1999-00261, funded under the EU 5th Framework Program. The authors thank P Mazurek, R Kostelecki, M Woźny, and T Pawluk for their helpful assistance in the field work.

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