The introduction and spread of alien fish species pose a major threat to native communities and ecosystem functioning in freshwaters. Black bullhead is one of the most successful invaders in European waters with several detrimental effects on native biota and ecosystems. In this study, we used stable isotope analysis to compare the body size and season-dependent diet, trophic position, isotopic niche size, and niche overlap of the invasive black bullhead with two native fish species (roach and European perch) in Lake Balaton, Hungary. We found that black bullhead could be characterized by invertivore-piscivorous feeding habit with a high rate of fish consumption. The rate of fish predation by invasive black bullhead increased with body size, while no seasonal differences were observed in fish consumption. Contrary to our hypothesis, little evidence of actual feeding competition was found between black bullhead and native fishes. Our results suggest that the studied species assimilate distinct energy resources in different proportions leading to a substantial amount of niche partitioning among them. We conclude that black bullhead may represent a threat for native, small-sized fishes primarily through predation and recommend urgent management actions (e.g. selective removal of the species) to minimize its adverse impacts on native communities.

Biotic interactions, fish, non-native, piscivory, predation, trophic position

The occurrence and spread of invasive species are leading drivers of biodiversity loss and pose major threats to ecosystem integrity. Adverse impacts of invasive species can be various and may occur at multiple ecological levels from single prey-predator relationships and competition (Bergstrom and Mensinger 2009; Seiler and Keeley 2009; Remon et al. 2016; Somogyi et al. 2023) to shifts in ecosystem functioning (Dietrich et al. 2006; Crowl et al. 2008; Linders et al. 2019). Freshwaters, and especially lakes, are often subject to high rates of species introductions, despite these ecosystems being known to be particularly vulnerable and susceptible to human activities and biological invasions (Gozlan et al. 2010; Mandrak and Cudmore 2010; Miró and Ventura 2013). Lakes cover only a limited area worldwide but support diverse species, including endemic taxa, and contribute substantially to ecosystem services (Dudgeon et al. 2006; Heino et al. 2021). However, habitat degradation, climate change and biological invasions have led to a considerable decline in species richness in these ecosystems occurring at a faster rate than in terrestrial and marine counterparts (Johnson et al. 2008; Strayer and Dudgeon 2010).

Several non-native fish species have been introduced into European freshwaters during the past decades mainly to support for commercial purposes, sport fishing or the ornamental market (Holčík 1991; Gozlan 2008). These species adversely affect the structure and functioning of native fish assemblages (Cucherousset and Olden 2011; van der Veer and Nentwig 2015) by altering natural aquatic food webs and competing for food resources with native species (Khan and Panikkar 2009; Britton et al. 2010; Bezerra et al. 2018). Black bullhead (Ameiurus melas Rafinesque, 1820) is one of the most successful invaders in European waters with detrimental ecological and socio-economic impacts (Leunda et al. 2008; Copp et al. 2016; Ferincz et al. 2016). The species was introduced to Europe from North America in the late 19^th and early 20^th centuries. Its fast spread was supported by physiological and life-history traits such as high fecundity, parental care, omnivory and tolerance to water pollution and low oxygen concentration (Ribeiro et al. 2008; Novomeská and Kováč 2009).

Black bullhead is an effective competitor and predator of native fish species. For example, Jaćimović et al. (2021) highlighted the opportunistic generalist feeding of the species with fish as a main prey item in its diet, followed by aquatic invertebrates. Similarly, Leunda et al. (2008) and Ruiz-Navarro et al. (2015) indicated that the species consumed co-occurring fish beside plant material and invertebrates affecting negatively the native ichthyofauna through both direct predation and competition. Additionally, Kreutzenberger et al. (2008) found the reduced predatory efficiency of pike (Esox lucius Linnaeus, 1758) in the presence of black bullhead and emphasized the potential adverse impact of this invasive species on native communities. However, there is a dearth of information on the position and specific role of black bullhead in the food web in its introduced range. While general knowledge suggests that black bullhead is an omnivorous species, there is less information about the seasonal and body size-dependent variation of its diet. In addition, the lack of detailed information on diet-based niche overlap between black bullhead and native fishes may hinder the planning of effective management strategies to control the negative impacts of this invasive species.

Stable isotope analysis (SIA) of carbon (δ¹³C) and nitrogen (δ¹⁵N) is a powerful method to examine the general feeding habits of fish (Vander Zanden et al. 1999; Britton et al. 2010; Dominguez Almela et al. 2021). Unlike gut-content analysis, which provides information about the recently consumed preys and is biased towards the underestimation of the importance of easily digestible food items, SIA provides longer-term and time-mediated information about a species’ diet and trophic niche (Balzani et al. 2020; McCue et al. 2020). In fact, stable nitrogen isotope ratio is an appropriate measure of consumer trophic position as it becomes enriched by 3–4‰ between prey and predator tissues (Cabana and Rasmussen 1994; Vander Zanden et al. 1999). Stable carbon isotope ratios exhibit little or no trophic level enrichment and are similar between the prey and the consumer providing a useful indicator of nutrient and energy source (Vander Zanden et al. 1999; Cucherousset et al. 2012). Stable isotope analysis thus can allow inferences regarding competition and niche partitioning among species and has been shown to be a useful method in determining the ecological impacts of alien fishes (Post 2002; Cucherousset et al. 2012).

The objective of this study was to compare the diet and the isotopic niche size and niche overlap of the invasive black bullhead and two native fish species. Since previous gut content analysis-based studies suggested that black bullhead is typically omnivorous with a dominance of invertebrate and fish preys in its diet (Leunda et al. 2008; Jaćimović et al. 2021), we chose another omnivorous cyprinid fish, the roach (Rutilus rutilus Linnaeus, 1758) and an invertivore-piscivorous percid fish, the European perch (Perca fluviatilis Linnaeus, 1758, perch hereafter) to infer potential competition between black bullhead and the native fish species in Lake Balaton, Hungary. We were especially interested to explore the seasonal and/or body size-dependent pattern in niche size and niche overlap among the species. Our predictions were as follows: (i) black bullhead will exhibit omnivorous feeding (i.e., broad niche size) with a preference to animal prey (ii) it will occupy an intermediate trophic position between perch and roach, and therefore acts as a strong competitor of both native fishes, (iii) the rate of predation on fish by black bullhead will increase with body size, and (iv) the adverse effects of black bullhead will be permanent throughout the year, that is the level of potential competition (niche overlap) with native fishes and the rate of fish in diet will not show seasonal differences.

ANOVA showed that δ¹³C differed significantly among species (F_2,252 = 116.80, P < 0.0001). Generally, black bullhead was more depleted in δ¹³C than perch and roach (contrast tests: P < 0.0001) (Fig. 1), while there was no significant difference between the two native species (contrast test: P = 0.3711). Although, species:season (F_4,252 = 9.52, P < 0.0001) and species:size group (F_2,252 = 23.04, P < 0.0001) interactions proved to be also significant, black bullhead δ¹³C was the lowest throughout the year and in both size groups (Fig. 1). δ¹³C varied also among seasons (F_2,252 = 3.92, P = 0.0211) as spring samples had significantly higher values than summer samples (contrast test: P = 0.0255). δ¹⁵N differed significantly among species (F_2,252 = 262.36, P < 0.0001), seasons (F_2,252 = 21.40, P < 0.0001) and size groups (F_1,252 = 81.57, P < 0.0001). Although species:season (F_4,252 = 4.76, P = 0.0010) and species:size group (F_2,252 = 15.24, P < 0.0001) interactions were also significant, perch had the highest, while roach had the lowest δ¹⁵N throughout the year and in both size groups (contrast test: black bullhead vs. perch: P = 0.0017, black bullhead vs. roach: P < 0.0001, perch vs. roach: P < 0.0001) (Fig. 1). Regarding seasonality, summer samples were generally more enriched while spring samples were more depleted in δ¹⁵N than autumn samples (contrast test: spring vs. summer: P < 0.0001, spring vs. autumn: P = 0.0005, summer vs. autumn: P = 0.0201) except for black bullhead where autumn samples were more enriched than summer and spring samples. Finally, large size group of species were generally more enriched in δ¹⁵N than small size group in each season (F_1,252 = 81,57, P < 0.0001), except for large roach which was slightly more δ¹⁵N depleted than small one.

Figure 1.

Isotopic niches (SEAc) and their centroids (+) of large and small size groups of black bullhead (Ameiurus melas), perch (Perca fluviatilis) and roach (Rutilus rutilus) collected in Lake Balaton (Hungary) in spring (from 26 May to 28 May), summer (from 15 August to 25 August) and autumn (from 29 October to 3 November) of 2022. Axes show the δ¹³C and δ¹⁵N values of individuals.

Core niche size of black bullhead was significantly (>0.95 probability) smaller in spring for the small and in autumn for the large size group, compared to other seasons (Fig. 1, Appendix 1). Regarding native species, only the small size group of perch showed seasonal changes in niche size; it was largest in autumn and smallest in summer with an intermediate value in spring. Roach had larger niche size than black bullhead in each season and in each size group, although this difference was not significant in spring and summer in the large size group (Fig. 1, Appendix 1). Niche size variability between black bullhead and perch did not show a clear pattern. In spring and summer large black bullhead had a significantly larger niche size than large perch, while in autumn, their niche sizes were similar. In small size groups, black bullhead had significantly larger niche size in summer, while significantly smaller niche size in spring and autumn than perch. Overlap between core niches of black bullhead and perch varied among seasons and size groups (Figs 1, 2A, B). Diet niche of both large and small perch was slightly overlapped with large black bullhead showing a decreasing pattern throughout the year with a negligible overlap in autumn (Fig. 2A, B). Diet niche of small perch was also minimally overlapped with small black bullhead in each season (Fig. 2B). Overlap between the core niches of black bullhead and roach was negligible (Fig. 2C, D).

Figure 2.

The proportion of isotopic area of large perch (Perca fluviatilis) (A), small perch (B), large roach (Rutilus rutilus) (C) and small roach (D) overlapping with the isotopic area of large and small black bullhead (Ameiurus melas) collected in Lake Balaton (Hungary) in spring (from 26 May to 28 May), summer (from 15 August to 25 August) and autumn (from 29 October to 3 November) of 2022. Axes show seasons and the proportion of diet overlap. Whiskers indicate 95% credible intervals with outliers (black dots). Boxplots indicate 25^th, 50^th and 75^th percentiles. Grey dots indicate the mean proportion of overlap. Each value was calculated from model posterior distributions (see Materials and Methods for details).

Centroid locations of fish species in the isotopic space varied significantly (P < 0.05) in each season, suggesting that species occupy unique trophic niches relative to each other throughout the year. Size groups within species were also separated significantly except for summer black bullhead and summer roach for which Euclidian distance between centroids of their large and small size groups were not significantly different from zero (Fig. 1, Appendix 2).

The most important dietary component of large black bullhead and large perch was fish in each season (Fig. 3). As secondary diet, large individuals of both species consumed macro invertebrates; diet of black bullhead contained mainly chironomid larvae and mussels, while the proportion of different macro invertebrate components distributed more equally in the diet of perch. Diet of small individuals of both species included both macro invertebrates and fish as main dietary components. Similarly to large conspecifics, small black bullhead fed mainly on mussels and chironomid larvae, while small perch fed on various macro invertebrates throughout the year. Proportion of fish in the diet of large black bullhead was significantly higher than in the diet of small black bullhead in each season (>0.95 probability), while there were no significant differences between seasons (spring vs. summer: probability = 0.56; spring vs. autumn: probability = 0.85; summer vs. autumn: probability = 0.77). Roach diet comprised both plant-based components and macro invertebrates in both size groups. The main macro invertebrates consumed by roach were chironomid larvae and mussel in each season. Regarding plants, only cladophora was consumed by roach in spring, while in summer and autumn, when developed aquatic macrophytes became abundant in the lake, roach shifted its plant-based diet to this food item. Although each studied fish species relied predominantly on the pelagic production in each season (77–95%, Appendix 3), the two source-one biotracer (δ¹³C) Bayesian mixing models indicated some differences in the use of primary carbon sources between black bullhead and the studied native fishes. Specifically, black bullhead utilized pelagic-based food web at a higher rate than native species independently of size group and season.

Figure 3.

Estimated seasonal contributions of food sources to the diet of large and small size groups of black bullhead (Ameiurus melas), perch (Perca fluviatilis) and roach (Rutilus rutilus) based on Bayesian stable isotope mixing models. Fish were collected in Lake Balaton (Hungary) in spring (from 26 May to 28 May), summer (from 15 August to 25 August) and autumn (from 29 October to 3 November) of 2022. Axes show different food sources and their estimated contributions to the diet. Whiskers indicate 95% credible intervals. Boxplots indicate 25^th, 50^th and 75^th percentiles. Each value was calculated from model posterior distributions (see Materials and methods for details).

Large perch occurred in the highest trophic position in each season followed by large black bullhead (Fig. 4), but these differences were not significant (spring: probability = 0.62, summer: probability = 0.83, autumn: probability = 0.85). Similarly, trophic position of small black bullhead and small perch did not differ significantly (spring: probability = 0.66, summer: probability = 0.79, autumn: probability = 0.68), while large perch had a significantly higher trophic position (>0.95 probability) than small black bullhead and small perch in each season and in autumn, respectively. Both species had a significantly higher trophic position than roach in each season and size group.

Figure 4.

Estimated posterior trophic position of large and small size groups of black bullhead (Ameiurus melas), perch (Perca fluviatilis) and roach (Rutilus rutilus) collected in Lake Balaton in spring (SP, from 26 May to 28 May), summer (SU, from 15 August to 25 August) and autumn (AU, from 29 October to 3 November). Axes show seasons and the trophic position of species in different size groups. Each value was calculated from model posterior distributions (see Materials and Methods for details).

The most prominent impact of invasive black bullhead on native fish and ecosystems is that it can act as a predator and a competitor of food resources simultaneously (Leunda et al. 2008; Ruiz-Navarro et al. 2015; Jaćimović et al. 2021). In this study we found that black bullhead in Lake Balaton could be characterised by invertivore-piscivorous feeding habits with a substantial rate of fish consumption. Large black bullhead consumed fish in a higher proportion than small ones and the rate of fish consumption was independent of the season, confirming our predictions. However, contrary to our hypothesis, substantial food niche partitioning occurred among black bullhead and native fish species suggesting that they assimilate distinct energy sources in different proportions and thus occupy different trophic positions in the food web. In sum, two (iii and iv) out of our four predictions (see Introduction for details) were supported, while two (i and ii) were not supported by our results.

Niche partitioning facilitates the local coexistence of native and alien species that divide available resources by separating along one or more niche dimensions (e.g., diet, habitat, activity time) (Schoener 1974). According to our results, core niche segregation of black bullhead and native fishes occurred along both the δ¹³C and δ¹⁵N axes indicating differences in the diet source and that they obtain resources at different trophic levels. Black bullhead consumed mussels and chironomid larvae in a high proportion. Since these invertebrates filter various suspended materials from the whole water column (Oliver 1971; Pinder 1986; MacIsaac et al. 1995; Spooner and Vaughn 2006), their assimilations could shift black bullhead’s isotopic signal towards a more negative direction along the δ¹³C axis. In contrast, the diet of perch was more heterogeneous regarding macro invertebrates, while the diet of roach included considerable amount of plant material, which contributed to the more enriched δ¹³C values of these species (Post 2002; Guinan Jr et al. 2015; Yu et al. 2016).

Variation in the foraging areas could also contribute to the variability of δ¹³C values. For example, Coulter et al. (2019) highlighted that niche partitioning of native and alien planktivorous fishes might have been driven by the distinct rate of using pelagic vs. littoral/benthic food sources. Similarly, Mumby et al. (2018) emphasized the role of habitat partitioning in the very limited extent of isotopic niche overlap in an offshore fish assemblage. However, our studied species relied predominantly on the pelagic production of the lake indicating little importance of foraging migration in niche partitioning. The dominance of pelagic-based food components in the diet could be unexpected considering that the studied fishes inhabit mainly the littoral zone (Specziár, 2010; Specziár et al. 2013). However, Lake Balaton is a shallow and turbid lake, and these properties facilitate the homogenization of the materials produced in different zones of the lake. This suggests that the isotopic signature of species living in the littoral zone can be affected by food components produced in the pelagic area (Monroy et al. 2014). Apparent niche segregation of perch and black bullhead from roach along δ¹⁵N axis was driven mainly by the distinct rate of piscivory. Although we found significant differences in δ¹⁵N values between black bullhead and perch, too, they still occupy the same trophic position, at least within size groups. These findings highlight that although different resource-consumer dynamics exist between black bullhead and perch, they play similar functional roles in the food web.

Isotopic areas of native species overlapped only slightly or negligibly with the isotopic area of black bullhead throughout the year and in each size group suggesting relatively low potential for competition among them. It is important to note that our results do not rule out that black bullhead competes for food with other fishes in the lake. It does highlight, however, that the species’ omnivorous or invertivore-piscivorous feeding habit detected in other ecosystems do not necessarily predetermine that black bullhead would compete with co-occurring native fishes from similar feeding groups (Leunda et al. 2008; Jaćimović et al. 2021). The potential lack of competition among the studied species may emerge through different mechanisms. Firstly, black bullhead probably exploits open resource niches, which may exist in anthropogenically modified and intensively utilized ecosystems like Lake Balaton (see e.g. Czeglédi et al. 2019), or obtains resources that are underused by native species (Coulter et al. 2019). Alternatively, given that the first occurrence of the black bullhead in Lake Balaton dates back to the 1980s, it is possible that the native species has already undergone competition-induced niche shifts during their co-existence. For testing these assumptions, exploring historical isotopic signatures of preserved specimens from the pre-invasion period, and using a finer taxonomic resolution of potential prey items would be necessary (e.g. complement our SIA with gut-content analyses). However, niche size of black bullhead was significantly smaller than that of roach and did not show a clear distinction with the niche size of perch, of the three studied species, black bullhead was the only one that showed significant seasonal niche size variability in both size groups. Based on these results, we assume that black bullhead does not have a permanently wide foraging niche by feeding on a variety of prey items in Lake Balaton, which can be an advantageous strategy in the invasion process (Tonella et al. 2018), but instead varies its foraging niche size temporally. Plasticity in niche size also supports the avoidance of competition with native fish and may facilitate the fast spread and wide establishment of black bullhead, similarly to other successful invaders (Almeida et al. 2012; Pettitt-Wade et al. 2015; Dominguez Almela et al. 2021).

Although black bullhead was predicted to occupy intermediate trophic position between perch and roach, the preference towards animal-based food items raised the species into the same level where the invertivore-piscivorous perch occurs. By taking into consideration all fishes in Lake Balaton, only piscivore apex predators such as pike, pikeperch (Sander lucioperca Linnaeus, 1758), European catfish (Silurus glanis Linnaeus, 1758), and asp (Leuciscus aspius Linnaeus, 1758) are in a higher position in the food web (Specziár, 2010). The substantial rate of fish consumption revealed by this study suggests that black bullhead is likely to have a large impact on native fish assemblage through predation. Our results thus are in accordance with Ruiz-Navarro et al. (2015), who found no isotopic niche overlap between black bullhead and roach in the invaded area and emphasized the importance of direct predation as the main adverse effect of black bullhead on native fish. Similarly to Leunda et al. (2008), who also highlighted the potential detrimental effects of black bullhead on local native fish fauna through predation, we found an ontogenetic diet shift between the species’ size groups with an increasing rate of fish consumption with body size. For larger individuals, capturing protein-rich fish prey is probably more energetically profitable than choosing macro invertebrates with hardly digestible calcium carbonate shells and chitin exoskeleton. Here, it is important to note that neither SIA nor gut content analyses allow to ascertain the origin (i.e., live or carcass) of fish preys and, in recent laboratory experiments, Preiszner et al. (2020, 2024) revealed that black bullhead may exhibit scavenging behaviour. Thus, it is possible that some of the fish consumed by black bullhead were carcasses, although carcass feeding has been suggested to be rather a complementary foraging strategy and not pivotal in their diet (Preiszner et al. 2020).

In conclusion, we compared the diet of black bullhead with an omnivorous and an invertivore-piscivorous fish species and found proof for intensive fish predation but revealed little evidence of actual feeding competition with native fish in Lake Balaton. The high proportion of fish in the diet of black bullhead might raise concerns in its invaded range. For example, in Lake Balaton, its population size suddenly increased (relative abundance of the species was <1% between 1996 and 2018 and 14.5% in 2022, unpublished standard monitoring data), and thus the species may represent a threat for native, small-sized fishes. Its predation can be especially significant during the spawning period, in spring and early summer when juvenile native fish are recruiting in the lake. Moreover, current human-induced alterations in the environmental characteristics of the lake (e.g. establishing wave-free harbours where dense submerged macrovegetation can develop) may further facilitate the spread and population growth of black bullhead (Jenkins 1957; Copp et al. 2016). In light of our compelling evidence of potential risks posed by the black bullhead, in ecosystems where its population expands, we strongly recommend urgent management actions, such as the selective removal of the species (see e.g., Jaćimović et al. 2023) to minimize its adverse impacts on the native fish fauna.

We thank Ingrid Győri, Bendegúz Márton Tóth, Krisztina Krassován, Hajnalka Horváth and Izabella Battonyai Tátrainé for their assistance in laboratory works. István Czeglédi was supported by the OTKA PD 138296 grant (National Research, Development and Innovation Office – NKFIH). Péter Takács was supported by the OTKA FK 140902 project (National Research, Development and Innovation Office – NKFIH). The research presented in this article was supported by the Széchenyi Plan Plus program (RRF 2.3.1-21-2022-00008 project) and the Sustainable Development and Technologies National Programme of the Hungarian Academy of Sciences (FFT NP FTA).