Changes in native fish communities in response to the presence of alien brown bullhead (Ameiurus nebulosus) in four lakes (Poland)

The aim of the study was to determine changes in the abundance of Ameiurus nebulosus and native fish in four lakes after 4–7 years. It was hypothesised that A. nebulosus would be the dominant species of fish in various types of lakes. The study was conducted in the summer of 2014 and 2018–2021, using Nordic multi-mesh gillnets. We indicated that relative numbers and biomass of A. nebulosus decreased in the oligo-mesotrophic lake, while increased in lakes of higher trophic conditions. Body weight and total length of A. nebulosus fluctuated from 3.2 to 283.3 g and 64 to 267 mm, respectively. The coefficient of condition of this species varied widely from 0.2 to 1.8 with the highest and lowest values in the meso-eutrophic lake. Ameiurus nebulosus accounted for 0.2–34.1% of the total numbers and 2.4–36.5% of the total biomass of the fish community. In the mesotrophic and meso-eutrophic lakes, A. nebulosus was a dominant component of the fish community after 7 years. The percentage contribution of A. nebulosus to the total numbers of fish decreased with the increasing trophic status of the studied lakes. Our study showed that A. nebulosus could be one of the factors responsible for a decrease in the number of native fish species and a change in the taxonomic structure of native fish in lakes of different trophic status (from oligo-mesotrophy to eutrophy).


Introduction
The brown bullhead, Ameiurus nebulosus (Lesueur, 1819), belongs to the family Ictaluridae. It is a native fish species in North America, where it naturally occurs in the Mississippi and Missouri River catchment areas. In the second half of the nineteenth century, the A. nebulosus was introduced to several European countries, e.g., Spain, Germany, England, France, Holland, Belgium and Austria (Welcomme 1988;Elvira and Almodóvar 2001;Copp et al. 2005), from where it quickly spread to almost all inland waters of the continent (e.g. Rutkayová et al. 2013). In Poland, this alien invasive fish species was introduced in 1885 and quite quickly spread, especially after World War II, in many rivers and lakes (see Grabowska et al. 2010). There are several papers on the appearance, occurrence, spread, abundance, and characteristics of A. nebulosus populations in Polish inland waters (Kolejko 1998;Kapusta et al. 2010;Hliwa and Błażejewski 2016;Rechulicz and Płaska 2019). However, only a few papers, both in Polish and world literature (Kornijów et al. 2003;Płaska 2018, 2021;Ulikowski et al. 2022) have considered the contribution of A. nebulosus to fish community in lakes.
A wide range of tolerances for the environmental conditions (Keast 1985;Kolejko 1998), high reproduction and unique phenotypic plasticity of A. nebulosus may result in an ecological and economic threat (Hliwa and Błażejewski 2016). These include, for example, hybridisation with native species, damage or destruction of spawning grounds and habitats of many aquatic organisms, the decline in the breeding of native fish and introduction of parasites and diseases, and extinction of some native species (Grabowska et al. 2010). In some waters, this species can rapidly become a dominant component of the fish community as a result of feeding on eggs and fry of other fish species (Kornijów 2001;Kornijów et al. 2003). On the other hand, a long-term study (from 2000 to 2011) performed in the three shallow lakes of eastern Poland demonstrated that the abundance of A. nebulosus varied considerably from year to year, accounting, on average, for 4.2-13.6% of the total numbers and 9.4-18.9% of the total biomass of fish community (Rechulicz and Płaska 2018).
Invasive species may have significant negative effects on ecosystems and diversity (Balirwa et al. 2003). It is known that A. nebulosus inhabits the same environment as native fish, thereby increasing the competition for habitat and food. This alien species is also very resistant, more than native species, to unfavourable living conditions and changes in water reservoirs. It is documented that the presence of A. nebulosus in combination with climate change can cause changes in the structure and functioning of aquatic food webs (Mieczan et al. 2022). It may also affect the communities of native fish, becoming a dominant component of fish in low-productivity waters (Kornijów et al. 2003).
Taking into account the above knowledge, the aim of this study was to determine whether the presence and substantial percentage contribution of A. nebulosus to the fish community may affect changes in native fish communities in lakes of different morphometry and trophic status. It was hypothesised that the A. nebulosus would be the dominant species of fish in various types of lakes.

Materials and methods
The study was conducted in four lakes of different morphometry and trophic status (Łęczna-Włodawa Lake District, Poland; Fig. 1) in the summer of 2014 and then after 4 years (2018-Lake Uściwierz), 6 years (2020-lakes Piaseczno and Sumin) and 7 years (2021-lakes Bikcze and Uściwierz). The characteristics of the studied lakes are given in Table 1.
Water parameters, such as temperature and oxygen content were measured at 1.0 m depth intervals with a YSI multiparameter ProDSS probe (Yellow Spring Instruments, USA). The transparency of the water was determined with a Secchi disc. The trophic state index (TSI) of the lakes was calculated from the depth of the Secchi disc (Carlson 1977). Lake Piaseczno was characterised by TSI values of 35.4 (2014) and 39.6 (2020), indicating oligo-mesotrophic characteristic. Lake Bikcze with TSI values of 45.7 in 2014 and 49.6 in 2021 was classified as mesotrophic. Lake Uściwierz with varying TSI of 54.2 in 2014, 58.6 in 2018 and 49.0 in 2021 indicated different trophic conditions. However, according to the mean TSI value of 53.9, this lake was classified as meso-eutrophic. Lake Sumin displayed TSI values from 60.0 in 2014 to 67.4 in 2020 indicating eutrophic characteristic (Table 1).
Fish was captured using benthic and pelagic Nordic multi-mesh gillnets (European standard protocol, EN 14,757). Detailed information on the characteristics of both gillnets is presented in Ulikowski  (2022). Nets time exposition was 12 h (between 18:00 and 6:00). A total of 30 benthic and 6 pelagic gillnets were used in deep Lake Piaseczno, while 8, 22 and 10 benthic gillnets were used in the shallow lakes Bikcze, Uściwierz and Sumin, respectively. The caught individuals were identified to species, counted, and measured. Total length (TL) and body weight (W) were measured with an accuracy of 1.0 mm and up to 0.1 g, respectively. For the A. nebulosus, randomly selected individuals (20-100%) were measured and weighed.
The condition factor (K) of A. nebulosus was calculated according to Fulton's formula. The number of individuals per unit effort (NPUE) and weight of individuals per unit effort (WPUE) were calculated per 100 square meters of gillnet.
The distribution of normality (Kolmogorov-Smirnov test) and homogeneity of variance (Levene's test) were tested for all data obtained. The differences in the total length, body weight, NPUE, WPUE, and condition factor of A. nebulosus between years in the studied lakes were analysed using the nonparametric Mann-Whitney (lakes Piaseczno, Bikcze, and Sumin) and Kruskal-Wallis tests (Lake Uściwierz). Pearson's correlation coefficients were calculated between A. nebulosus abundance (relative numbers-NPUE and biomass-WPUE, contribution to the total numbers and biomass) and trophic conditions (TSI) of the studied lakes. Correlations were performed for all combined lakes and years (n = 9). Statistical analyses were carried out with the use of the Statistica software (StatSoft, Inc., St Tulsa, USA).

Ameiurus nebulosus abundance, biomass and size structure
The relative numbers (NPUE) of A. nebulosus increased in three lakes (Fig. 2a). The most pronounced increase was observed in mesotrophic Lake Bikcze, slightly lower in meso-eutrophic Lake Uściwierz, while the lowest in eutrophic Lake Sumin. In one lake only (oligo-mesotrophic Lake Piaseczno), the NPUE decreased threefold. Similar trends were observed in the relative biomass (WPUE; Fig. 2b). In all lakes, the differences in NPUE and WPUE Table 1 Morphometric and trophic characteristics of the studied lakes. Trophic conditions of the studied lakes were based on trophic state index (TSI) calculated from Secchi disc depth according to Carlson (1977) Lake Latitude Longitude Area (
In the studied lakes, the total length of A. nebulosus varied between 64 and 267 mm (Fig. 3a), whereas body weight (W) ranged from 3.2 to 283.3 g (Fig. 3b). The highest mean TL of this species was recorded in eutrophic Lake Sumin in 2014 (227 mm), while the lowest in meso-eutrophic Lake Uściwierz in 2021 (138 mm). In three lakes (oligo-mesotrophic, meso-eutrophic and eutrophic), the TL of A. nebulosus was significantly (p < 0.01) higher in 2014 than in 2020 and/or 2021, except in mesotrophic Lake Bikcze in which TL of A. nebulosus was significantly (p < 0.001) lower in 2014 than in 2021. Similarly, the mean value of WPUE was the highest in eutrophic Lake Sumin in 2014 (143.6 g), while the lowest was in meso-eutrophic Lake Uściwierz in 2021 (35.8 g). The differences in the weight of A. nebulosus between years were significant in all of the studied lakes (p < 0.01). The coefficient of condition (K) of A. nebulosus decreased over time in all of the studied lakes (Fig. 3c). The lowest value of K was found in oligomesotrophic Lake Piaseczno in 2020 (0.98), while the highest in eutrophic Lake Sumin in 2014 (1.27). The differences in K between years were significant in all of the studied lakes (p < 0.05). The percentage contribution of A. nebulosus to the total numbers correlated negatively with the TSI of the studied lakes (r = − 0.75, p = 0.02, n = 9).

Fish community
The relative numbers (NPUE) of native fish were very similar in the studied years in oligo-mesotrophic Lake Piaseczno, distinctly increased in mesotrophic Lake Bikcze, while decreased in two other lakes (Fig. 4a). The relative biomass (WPUE) decreased slightly in oligo-mesotrophic Lake Piaseczno, increased markedly in mesotrophic Lake Bikcze, increased initially and then decreased in meso-eutrophic Lake Uściwierz, while decreased twofold in eutrophic Lake Sumin (Fig. 4b).
In oligo-mesotrophic Lake Piaseczno, the number of fish species was slightly higher in 2014 than in 2020 (Table 2). In this lake, nine species were common for both years. In mesotrophic Lake Bikcze, the number of species was the same in both years. However, six species only were common for both the studied periods. In meso-eutrophic Lake Uściwierz, the number of fish was lower in 2014 than in 2018 and 2021. In this lake, ten fish species were common for all three studied years. In eutrophic Lake Sumin, the Fig. 3 Total length a, body weight b, and condition factor c of A. nebulosus in the studied lakes (oligo-mesotrophic Lake Piaseczno, mesotrophic Lake Bikcze, meso-eutrophic Lake Uściwierz, and eutrophic Lake Sumin). Differences between years in all of the studied lakes were significant (Mann-Whitney test, p < 0.05) number of species was markedly higher in 2014 than in 2020 and 11 species were common for two years.
In oligo-mesotrophic Lake Piaseczno, in the first year of the study, the fish community was numerically dominated by A. nebulosus and Coregonus albula (33 and 32%, respectively) (Fig. 5). In the following year, there was observed decreases in the contribution of these species, while the distinct increases in the contributions of Rutilus rutilus and Perca fluviatilis (to 30 and 33%, respectively). Similar trends were observed in fish biomass (Fig. 5).
In mesotrophic Lake Bikcze, the contribution of A. nebulosus to the total numbers increased slightly, while to the total biomass quite distinctly, becoming the dominant component of fish in 2021 (36% of the total biomass; Fig. 5). The contribution of Alburnus alburnus to the total numbers and biomass increased, while Scardinius erythrophthalmus markedly decreased.
In meso-eutrophic Lake Uściwierz, the percentage contribution of A. nebulosus to the total numbers and biomass (Fig. 5) increased within 7 years. Fig. 4 Relative numbers (NPUE) a and biomass (WPUE) b of native fish communities in the studied lakes (oligo-mesotrophic Lake Piaseczno, mesotrophic Lake Bikcze, mesoeutrophic Lake Uściwierz, and eutrophic Lake Sumin) Table 2 List of fish species found in the studied lakes (oligo-mesotrophic Lake Piaseczno, mesotrophic Lake Bikcze, mesoeutrophic Lake Uściwierz, and eutrophic Lake Sumin) In 2021, this species formed a substantial part of the fish community (34 and 37% of the total numbers and biomass, respectively). The contribution of Abramis brama to the total numbers and biomass of fish decreased conspicuously, while P. fluviatilis fluctuated between the studied years.
In eutrophic Lake Sumin, in both of the studied periods, the contribution of A. nebulosus to the total numbers and biomass of fish was negligible (0.2-4.1%; Fig. 5). The contributions of P. fluviatilis, Blicca bjoerkna, and A. alburnus increased, while A. brama distinctly decreased.

Discussion
In the present study, we investigated the changes in abundance and size structure of non-native invasive A. nebulosus as well as the structure of native fish communities (number of species, abundance and composition) in lakes of different trophic status. It is known that alien invasive fish species can influence the structure of the native fish through competition for habitat and food, predation on eggs and fry, hybridisation with native species, environmental destruction, as well as the transfer of parasites and diseases (Grabowska et al. 2010) and cause significant changes in the structure and functioning of aquatic ecosystems (e.g. Henriksson et al. 2015Henriksson et al. , 2016Haubrock et al. 2021). The impact of alien species on native communities and food web structure is unpredictable (Volta et al. 2018). It may be especially important when alien invasive species of fish reach high abundance and affect food webs at different trophic levels, due to their omnivorous mode of nutrition (Collier et al. 2018). It is documented that A. nebulosus, occurring in two shallow eutrophic lakes (eastern Poland), is a food opportunist that can prey on various food (Rechulicz and Płaska 2021).
Results of this study showed that the abundance of A. nebulosus differed significantly between the studied periods. A distinct decline both in the relative numbers (threefold) and biomass (fourfold) was observed only in deep oligo-mesotrophic Lake Piaseczno. Similarly, a slight, but continuous decrease in the abundance of A. nebulosus in certain parts of Poland and Europe was also recorded (Kruk et al. 2001;Verreycken et al. 2007). In the studied oligo-mesotrophic lake, the total length, weight, and conditions of A. nebulosus as well as the relative numbers and biomass of native communities also slightly decreased. The contribution of A. nebulosus to the total numbers and biomass declined from 33 to 17% and 31 to 18%, respectively. It should be emphasised that the trophic status of this lake remained unchanged not only during the studied years but also over the last 20 years (Lenard and Solis 2009). That is why, a clear shift in the dominant structure of native fish from C. albula to P. fluviatilis and R. rutilus was probably the result of A. nebulosus dominance, limited food resources and/or changes in fish stocking rather than eutrophication. In three other lakes of higher trophic status, populations of A. nebulosus increased considerably. In addition, shifts in its size structure (total length and weight) were more pronounced compared to the oligo-mesotrophic lake. An increase in the numbers of A. nebulosus in the mesotrophic lake coincided with a strong increase in the relative abundance of the native fish community. In contrast, the increased numbers of this alien species in the meso-eutrophic lake resulted in a decrease in the numbers and biomass of the native community. In turn, a slight increase in its numbers in the eutrophic lake coincided with a strong decrease in native fish. Invasive species often cause rapid population declines and the extinction of native species (Mills et al. 2004). Our study indicated that the effect of alien species on native fish may cause visible shifts in the structure of fish species, but it does not necessarily lead to a significant reduction in numbers and/or biomass.
In some aquatic ecosystems, A. nebulosus can form stable populations (Rechulicz and Płaska 2018) and become a dominant component of the fish community (Holčik 1991). For example, in shallow mesotrophic Lake Rotcze (Łęczna-Włodawa Lakeland, eastern Poland), the percentage contribution of A. nebulosus to the total numbers and biomass was 71 and 43%, respectively (Kornijów et al. 2003). In turn, studies performed in the mesotrophic lake (Masurian Lakeland, north-eastern Poland) demonstrated that A. nebulosus was the third dominant species, accounting for 19 and 21% of the total numbers and biomass of all caught fish, respectively (Ulikowski et al. 2022). However, studies of other lakes, situated in eastern Poland, showed that the maximum percentage contribution of A. nebulosus to the total numbers and biomass did not exceed 14 and 19%, respectively (Kolejko 2010;Rechulicz et al. 2015;Płaska 2018, 2021). In the present study, A. nebulosus constituted 0.2-34.1% of the total numbers and 2.4-36.5% of the total biomass. It was the dominant component of the fish community in oligo-mesotrophic Lake Piaseczno in 2014 (33% of the total numbers), mesotrophic Lake Bikcze in 2021 (36% of the total biomass), and meso-eutrophic Lake Uściwierz in 2021 (34% of the total numbers and 37% of the total biomass).
The maximum lifespan of A. nebulosus is 4-6 years and the growth rate may be about two times faster than other fish species, which is attributed to high foraging and metabolism (Keast 1985;Kornijów 2001). Extinction or coexistence of native and alien invasive species may depend on the number of negative interactions (competition and predation) that occur at the same time and are related to the body size of species (Mills et al. 2004). Rechulicz and Płaska (2021) reported that in lakes of eastern Poland, larger individuals (above 135 mm in length) of A. nebulosus can feed on fish. In such individuals, the share of fish in the diet, regardless of lake type, increases even well above 50%. Our study showed that in the first year of the study in all lakes, the populations of A. nebulosus were mainly composed of large individuals (above 135 mm) that may be responsible for the reduction of some native fish species.
As mentioned above, the presence of an invasive alien species can cause changes in native fish communities, but this issue is very difficult to demonstrate (Lorenzoni et al. 2006) due to the lack of long-term data (Allan et al. 2005). It also requires knowledge about the fish stocking before and after the appearance of the invasive species (Gozlan 2008). In addition, many factors may affect the structure of fish communities. The most important are: eutrophication of the aquatic ecosystems, habitat destruction for fish reproduction and growth, fisheries management, climate change, and intensity and selectivity of fishing and angling pressure (e.g. Allan et al. 2005). As shown by Thomas (2013), some invasive species can disrupt the functioning of ecosystems and eliminate native species, but they can also lead to an increase in ecological diversity. On the other hand, it would seem that ecosystems with greater species richness can more easily protect themselves against the invasion of new species. However, Kennard et al. (2005) studying the rivers of Australia found that despite the high species richness, these rivers did not show increased resistance to invasion. The authors suggested that the abiotic parameters of ecosystems as well as the human activity may be factors supporting the invasion. In our study, the number of fish species decreased only in the eutrophic lake. The shifts in the taxonomic structure were observed in all lakes, irrespective of lake morphometry, productivity, and increased/decreased abundances of A. nebulosus. For example, the most apparent shift in dominance structure was observed both in oligo-mesotrophic Lake Piaseczno and eutrophic Lake Sumin. Our study showed that the numbers, biomass, and size structure of A. nebulosus were not related to lake productivity, but the percentage contribution of A. nebulosus to the total numbers of fish decreased with the increasing trophic status of the studied lakes. This fact may indicate that A. nebulosus prefers waters of low and moderate trophic conditions. Similarly, Kornijów (2003) showed that the contribution of A. nebulosus to the total numbers and biomass decreased with increasing eutrophication of lakes (from mesotrophy to hypertrophy), in contrast with the increasing average weight and coefficient of condition. It should be underlined that the trophic status of the studied shallow lakes, similarly as in the case of oligo-mesotrophic Lake Piaseczno, did not change distinctly between the studied years, suggesting that eutrophication was not probably a major factor influencing the structure of the native fish community. It is also documented that trophic conditions have not changed much over the last 20 years (e.g. Mieczan 2003;Lenard and Solis 2009;Pasztaleniec and Poniewozik 2010;Sender 2018;Ferencz et al. 2019).
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