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All issues No 420 (2019) Knowl. Manag. Aquat. Ecosyst., 420 (2019) 21 Full HTML
Issue
Knowl. Manag. Aquat. Ecosyst.
Number 420, 2019
Topical Issue on Fish Ecology
Article Number 21
Number of page(s) 7
DOI https://doi.org/10.1051/kmae/2019013
Published online 30 April 2019

© V. Rakauskas et al., Published by EDP Sciences 2019

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (http://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

1 Introduction

In Europe, the Chinese Sleeper Perccottus glenii, Dybowski, 1877, has been recognized as a highly invasive fish species since its first introduction from East Asia in 1912 (Reshetnikov, 2004). The ongoing species invasion is probably the outcome of deliberate and non-deliberate stocking, which is thought to be facilitated by P. glenii opportunism, flexible life-history characteristics, and aggressive behaviour as well as by its ability to survive in degraded environmental conditions (Ćaleta et al., 2011; Reshetnikov and Ficetola, 2011). The ability of P. glenii to effectively use trophic resources ranging from ciliates to vertebrates (Reshetnikov, 2003; Koščo et al., 2008; Grabowska et al., 2009; Kati et al., 2015) coupled with the prolonged reproductive period allows the coexistence of individuals of multiple sizes. The species is able to escape competition and predation by inhabiting water bodies unsuitable for most other freshwater fishes in Northern Europe. It has been suggested that isolated water bodies with abundant macrophytes, thick mud layer and repetitive oxygen-deficit events are the optimal habitat for this species (Jurajda et al., 2006; Reshetnikov and Chibilev, 2009). Furthermore, P. glenii dramatically affects invaded communities by reducing diversity of local macroinvertebrate, amphibian and fish species (Reshetnikov, 2003), thus eventually affecting functioning of the whole ecosystem (Reshetnikov, 2013). Disease transmission and facultative parasitism cause additional concern (Kvach et al., 2013, 2016; Sokolov et al., 2014).

The current research into P. glenii invasion biology is primarily focused on the elucidation of threats and the underlying mechanism of species invasions rather than on provision of sustainable and practical solutions for management of this invasive species (Grabowska et al., 2011; Reshetnikov and Ficetola, 2011; Nehring and Steinhof, 2015). Besides preventive measures, such as trade legislation, there is a need for effective methods for the eradication or suppression of local P. glenii populations and the hold-up of their further establishment and wider dispersal in Europe (Nehring and Steinhof, 2015). So far, only a limited number of programmes for P. glenii eradication, mainly involving the use of chemical methods (Reshetnikov and Ficetola, 2011), have been reported.

The objective of this study was to investigate the potential of native piscivorous fishes, such as the Northern pike Esox lucius Linnaeus, 1758, and the European perch Perca fluviatilis Linnaeus, 1758, to eradicate or suppress populations of P. glenii in small eutrophic lakes.

2 Materials and methods

2.1 Study site

Biocontrol experiments were performed in 2012–2017 in natural lakes Beržuvis, Bevardis, Cirkliškis and Stūgliai pond, located in eastern Lithuania. All the water bodies studied are similar in their physical characteristics: they are all shallow, have a thick (> 3 m) sediment (sapropel) layer and the littoral zone that is densely overgrown with macrophytes. All the four water bodies are subjected to irregular oxygen depletion events during prolonged ice cover (Tab. 1).

The first official record of P. glenni in Lake Bevardis (as well as in Lithuania) dates back to 1986 (Virbickas, 2000). According to anglers, the presence of P. glenni in the other water bodies studied was recorded before 2000 (personal communication). The preliminary analysis performed in 2010 showed that already at that time the species was well established in the water bodies surveyed and dominant in their fish communities. At that time Perccottus glenii constituted 66–95% of the total fish number in all the water bodies investigated (more than 300 ind./100 m2).

Table 1

Characteristics of studied lakes: coordinates, surface area (S); mean depth (H); maximal depth (H max); dissolved oxygen at 1 m depth (February) (DO).

2.2 Biocontrol

Lakes were repeatedly stocked in the spring or autumn of 2013, 2014 and 2015. The stocking material was provided by local fish farms. The largest numbers of E. lucius and P. fluviatilis specimens per unit area were stocked into Lake Beržuvis, followed by those into Bevardis and Stūgliai. Lake Cirkliškis was stocked only with E. lucius, the number of stocked fish individuals per unit area being the smallest among the lakes studied (Tab. 2). According to piscivorous fish stocking dates, the whole study period was subdivided into the following three periods: pre-stocking (2012–2013), transitional (2014–2015), and post-stocking (2017) periods.

Table 2

Dates of piscivorous fish stocking into bioregulated lakes in 2013–2014 and numbers of the piscivorous fish individuals stocked. Age of the stocked fish: 0+: one-summer-old fish; 1+: two-summer-old fish; etc.

2.3 Analysis of fish communities

The composition of fish communities was investigated during the vegetation season in 2012–2015, and in 2017. Fish were sampled using battery-powered electric fishing gear (Samus Special Electronics, Samus-725 mp). Electric fishing using the same gear and fishing mode was performed from a boat in the water depth range of 0.2–2.0 m. For catch per unit of effort (CPUE), 10 min of actual operational electrofishing was applied. All fish were identified to species level and counted. Pursuant to state fishing laws and sampling licensing, after sampling, all native fish were released into the same water bodies, except for the representative number of E. lucius and P. fluviatilis specimens from Lake Beržuvis, which were intended for diet analysis, and all non-indigenous P. glenii. All fish were killed by overdosing on anaesthetics (1.5–2.0 mL · L−1 solution of 2-phenoxyethanol for 5 min).

The total number and weight were determined for the P. glenii specimens caught per each unit of effort (CPUE), whereas the total body length (TL) and age were assessed only for fish specimens from representative sub-samples (up to 30 specimens per each CPUE). The age of P. glenii specimens was estimated from scales (Thoresson, 1993). In addition, we measured TL (to the nearest mm) and body weight (to the nearest 0.1 g) of all the E. lucius and P. fluviatilis specimens intended for diet analysis. All fish sampling and examination procedures were carried out in strict accordance with regulations of the Republic of Lithuania. The fish taxonomy used in the present study follows the one provided in FishBase (Froese and Pauly, 2018).

2.4 Analysis of piscivorous fish diet

Analysis of the piscivorous fish diet was carried out on fish individuals sampled from Lake Beržuvis during the transitional period (2014–2015) of piscivorous fish stocking. Piscivorous fish from standardized catches, i.e. E. lucius (n = 28, TL = 33.0 ± 10.3) and large-sized individuals of P. fluviatilis (n = 8, TL = 19.6 ± 0.8), were subjected to gut content analysis. Stomachs of selected fish were removed and preserved in 10% formaldehyde solution until examination in the laboratory. Stomach contents were weighed to the nearest 0.1 mg using an electronic balance (ABJ 120-4M, Kern and Sohn GmbH) to obtain wet weight. Then food items were extracted, identified, grouped and again wet-weighed, their proportions in weight of the total gut content being assessed.

2.5 Statistical analyses

Non-parametric Mann-Whitney U-tests were used to test for differences in the numbers of fish species sampled during biocontrol periods. As the data obtained did not meet the normality assumption for parametric methods (Shapiro-Wilk's tests, P < 0.05), we used non-parametric tests. The analyses were performed using STATISTICA 12.0 software. The significance level of P < 0.05 was specified for all statistical analyses a priori.

3 Results

3.1 Pre-stocking period

Before the piscivorous fish stocking, fish assemblages in the studied lakes were poor in terms of species richness and consisted of two or three species (Tab. 3). The mean number of fish per standard CPUE ranged from 39.3 to 138.9. Perccottus glenii dominated fish assemblages in all the lakes studied, on average accounting for 80.9–97.7% of total fish communities. The total body length of the sampled P. glenii specimens ranged from 3.2 to 26.0 cm (0+–11+ year old). The mean number of P. glenii specimens per CPUE varied from 31.8 to 135.7 ind. and their body weight from 17.2 to 22.1 g (Tabs. 3 and 4). Meanwhile, the total catch of other fish species accounted for less than 20% of the total pre-stocking fish catch in all the lakes studied (Tab. 3).

Table 3

Catch per unit of effort (CPUE) of different fish species in studied water bodies during 2012–2017 (mean ± SD): pre-stocking period 2012–2013 (Pre), transitional period 2014–2015 (Transitional), and post-stocking period 2017 (Post).

Table 4

Metrics of Perccottus glenii populations in studied water bodies during 2012–2017: pre-stocking period 2012–2013 (Pre), transitional period 2014–2015 (Transitional), and post-stocking period 2017 (Post).

3.2 Transitional period

In the transitional biocontrol period, the mean number of P. glenii per standard CPUE decreased significantly in all the water bodies studied except one, ranging from 1.5 to 42.5 ind. (Tab. 3) (Figs. 1A, 1C and 1D). P. glenii numbers per standard CPUE in Lake Bevardis also declined (from 94.0 ± 33.8 ind. in the pre-stocking period to 48.2 ± 48.2 ind. in the transitional biocontrol period (Fig. 1B), but this change was not significant (Mann-Whitney U test: Z = 1.86, P = 0.06). Overall, all P. glenii populations underwent drastic changes as the mean body weight of P. glenii per standard CPUE remarkably decreased. The average body weight of P. glenii decreased more than two-fold ranging from 5.1 to 10.7 g in all the water bodies studied except one. In Stūgliai pond, the mean body weight of P. glenii specimens was found to increase from 17.2 g in the pre-stocking period to 28.4 g in the transitional biocontrol period (Tab. 4). The change observed in the maximum length and age of the captured P. glenii specimens followed the same pattern. After piscivorous fish stocking, both characteristics markedly decreased in the lakes studied; meanwhile in Stūgliai pond, they remained similar (Tab. 4). Overall, although suppressed, P. glenii populations were still dominant in Bevardis and Cirkliškis lakes. Meanwhile, fish assemblages of the other studied water bodies (Tab. 3) were dominated by belica Leucaspius delineatus (Heckel, 1843).

Total fish numbers per CPUE remained unchanged during the transitional period in all the water bodies studied except Lake Cirkliškis (Tab. 3). After E. lucius stocking into this lake, the mean fish number per CPUE sharply decreased, from 138.9 ± 28.8 ind. in the pre-stocking period to 43.0 ± 37.0 ind. in the transitional biocontrol period (Mann-Whitney U test: Z = 2.57, P = 0.010). The number of fish species increased in all the lakes and ranged from four to seven species.

thumbnail Fig. 1

Catch per unit of effort (CPUE) of Perccottus glenii in lakes Beržuvis (A), Bevardis (B), Cirkliškis (C), and Stūgliai (D) studied before (Pre: 2012–2013), during (Transitional: 2014–2015), and after (Post: 2017) the implementation of biocontrol measures, i.e. the introduction of native piscivorous fish species (median, quartiles, range). Small letters (a, b) denote homogeneous groups according to Mann-Whitney U tests.

3.3 Post-stocking period

After the biocontrol period, the number of species in fish assemblages of the studied lakes dropped and was comparable with that in the pre-stocking period (Tab. 3). In the post-stocking period, P. glenii disappeared from the investigated fish assemblages in most cases, suggesting that the biocontrol process was successful (Tab. 3). However, P. glenii remained in the fish catches landed from Lake Cirkliškis, though significantly reduced (1.9% of a total fish catch) compared with the pre-stocking period (Mann-Whitney U test: Z = 1.96, P = 0.04) (Fig. 1C). The surviving P. glenii specimens remained in this lake and reached the age of maturity. The largest specimens reached up to 18.0 cm in length and were 5+ year old (Tab. 4). Overall, in the post-stocking period, native species dominated fish assemblages in all the lakes studied, but fish community diversity remained poor.

3.4 Piscivorous fish diet

The diet analysis of E. lucius and large-sized P. fluviatilis specimens (TL > 17 cm) showed that small P. fluviatilis (TL < 5 cm), constituting more than 47 and 63% of the diet of piscivorous E. lucius and P. fluviatilis, respectively, were the dominant prey item. Leucaspius delineatus made up a substantial part (38%) of E. lucius diet, but was not found in the diet of P. fluviatilis. Surprisingly, only 14.3% of all the analysed E. lucius specimens consumed P. glenii. The contribution of P. glenii to the diet of E. lucius reached only 14%. On the contrary, its share in the diet of P. fluviatilis was significant and constituted 38%, as 37.5% of the analysed P. fluviatilis specimens consumed P. glenii. Additionally, larvae of dragonfly (Odonata) constituted 0.7% of the E. lucius diet, meanwhile only two prey-species (P. glenii and P. fluviatilis) were found in the diet of P. fluviatilis.

4 Discussion

The development of effective management programmes for invasive species control is a challenge currently facing invasion biology (Hulme, 2006, 2009). Despite some important initiatives, the geographical expansion of P. glenii is still continuing and there is an urgent need for cost-efficient strategies for containing, suppressing or eradicating P. glenii populations (Nehring and Steinhof, 2015). The native piscivorous fish stocking experiment carried out on a lake level during our study proved effectiveness of piscivorous fish in controlling P. glenii populations. Within a four-year period of biocontrol measures' implementation, the initially abundant populations of P. glenii were eradicated in three of the studied water bodies and highly suppressed in one of them.

During the transitional period, the number of P. glenii individuals decreased 2–46 fold. Only small-sized P. glenii specimens remained in dense vegetation, while elder (> 5+ year old) individuals were eradicated during the first year of biocontrol implementation in all the lakes except one. After four years of biocontrol implementation, P. glenii was no longer recorded in CPUEs in the studied lakes, except for Lake Cirkliškis, where the population of P. glenii was strongly suppressed, but not eradicated. It should be pointed out that this lake was stocked only with E. lucius, and fish stocking numbers per unit area were the lowest among all the lakes studied (see Tab. 2).

The analysis of piscivorous fish diet in Lake Beržuvis showed that the contribution of P. glenii to the diet of E. lucius was unexpectedly low, but it constituted a substantial part of the diet of large-sized P. fluviatilis specimens. This fact somehow contradicts the findings obtained in other studies, showing that P. glenii may be preferable prey for E. lucius (Litvinov and O‘Gorman, 1996; Telcean and Cicort-Lucaciu, 2016), whereas the ability of P. fluviatilis to regulate the abundance of P. glenii has not been studied yet. The existing sparse data indicate that P. fluviatilis is capable of preying on P. glenii although its share in perch diet is trivial, (Litvinov and O‘Gorman, 1996; Didenko and Gurbyk, 2016; Mérö, 2016). According to our observations, P. fluviatilis alone is not capable of eradicating P. glenii, which is proved by the fact that in several lakes of Lithuania, both species have been coexisting for decades (unpublished data).

The low number of P. glenii in the diet of E. lucius may be attributed to the time lag between the first predatory fish stocking and their diet analysis. The average share of P. glenii in the total fish catch during the piscivorous fish diet sampling was only 0.1%. This fact indicates that the majority of P. glenii individuals had been already consumed by that time. The surviving small-sized P. glenii specimens were possibly suppressed by large-sized individuals of E. lucius in a very shallow littoral zone overgrown with dense macrophytes, i.e. in the habitats where large-sized E. lucius cannot easily hunt due to the limited space for ambush-type predation (Pers. observation). Apparently, piscivorous P. fluviatilis were still able to prey on small-sized P. glenii individuals in shallow waters overgrown with macrophytes, while larger individuals of E. lucius switched to feeding on L. delineatus and P. fluviatilis in open waters.

Overall, E. lucius and P. fluviatilis are predators with pronounced opportunism and feeding plasticity. Both species consume the prey that is available, easy to catch and is suitable as food owing to its size (Rakauskas et al., 2010; Pedreschi et al., 2015). Unfortunately, to date, there is no information on how selective E. lucius and P. fluviatilis are in their predation on P. glenii, and to what extent these predators display preference for feeding on P. glenii compared with other prey-fish species. Owing to the specific structure of its snout and larger body size, E. lucius should be better at controlling larger P. glenii specimens, while P. fluviatilis has proved to be able to effectively prey on small P. glenii individuals. Predating strategies of these two species also differ. E. lucius usually stays in solitude and relies on ambush predation (Harper and Blake, 1991; Eklöv, 1992), while P. fluviatilis actively seeks for prey and hunts in a group (Eklöv, 1992; Turesson and Brönmark, 2004). Therefore, the use of these both predators simultaneously produced the best biocontrol effect and might be an explanation, why the eradication of P. glenii in Lake Cirkliškis, stocked solely with E. lucius, was not successful.

The results of the present biocontrol experiment provide evidence that the native piscivorous fish E. lucius and P. fluviatilis can strongly contribute to the effective suppression of invasive P. glenii, at least on a scale of small eutrophic shallow lakes. In comparison with eradication programmes involving the use of chemical biocides and other direct measures such as netting, electrofishing or draining of habitats, the reintroduction of native piscivorous fish species is a feasible, cost-effective, uncontroversial, and sustainable management approach. The use of fish as biocontrol agents has generally been applied for managing mosquitoes (Martinez-Ibarra et al., 2002; Pyke, 2008), invasions of non-native crayfishes (Musseau et al., 2015), or invasions of non-indigenous amphibians (Louette, 2012). Previous studies have also shown that E. lucius and P. fluviatilis can negatively affect populations of the invasive stone moroko Pseudorasbora parva (Temminck and Schlegel, 1846), reducing its abundance and biomass, without affecting native species (Davies and Britton, 2015; Lemmens et al., 2015). However, there are no reports on large-scale biocontrol programmes that have successfully utilized piscivorous fish to suppress the invasion of P. glenii populations (Britton et al., 2011). Furthermore, extensive understanding of how to enhance and manage E. lucius populations, given the longstanding tradition of pike stocking in the restoration of shallow ponds and lakes, is available (Skov and Nilsson, 2007; Jeppesen et al., 2012). Results of this study show that there is a considerable potential for suppressing populations of small, invasive fishes such as P. glenii. Although such biocontrol action is less immediate than fish removals, it has the potential benefit of negligible long-term management costs. Therefore, we believe that stocking of E. lucius and P. fluviatilis can be a valuable measure in specific cases, e.g. when the aim is to eradicate populations of invasive P. glenii in small eutrophic lakes.

However, the possibility of a strong effect on a local fish assemblage should also be considered. The experiments performed revealed that the local fish community of Lake Beržuvis, which was initially strongly unbalanced by P. glenii invasion, was finally exterminated as a result of piscivorous fish stocking in the fourth year of biocontrol implementation. It is worth noting that Lake Beržuvis was stocked with the largest number of predators. However, it remains unclear, whether it was the result of mass-stocking of predators or the outcome of the oxygen depletion observed at the end of the winter in 2016.

5 Concluding remarks

The current study suggests that both E. lucius and P. fluviatilis should be stocked in order to completely exterminate P. glenii. These species are able to forage on different-sized prey (different gape size limitation). Esox lucius shows a tendency to prey on larger-sized P. glenii specimens, while P. fluviatilis tends to forage on small P. glenii individuals in very shallows waters. Piscivorous fish should be stocked annually, at least for several successive years, so as to avoid the possible impact of unpredictable winter oxygen depletion events or other impacts that may significantly reduce abundance of stocked fish and their predation effect on P. glenii populations. In addition, permanent stocking for several successive years should help to prevent maturation and reproduction of the surviving P. glenii individuals, which usually occurs in the 2nd or 3rd year of their life, when TL reaches 6–8 cm (Froese and Pauly, 2018). To extend the period of predation on P. glenii and to reduce losses of stocked fish in the case of unpredictable winter oxygen depletion, it seems more expedient to carry out piscivorous fish stocking in Northern Europe countries in spring. Introduction of a large amount of piscivorous fish into P. glenii-invaded lakes might also lead to undesirable consequences for native fish assemblages. It is known that invaded communities, especially those with a low species diversity, are more susceptible to any kind of alterations. Stocked piscivorous fish may either increase the species richness of top predators or replace the local ones. This can cause additional predation pressure on native fish communities, increasing top-down effects (Eby et al., 2006). Our results indicate that after such intense native piscivorous fish stocking, fish communities remain unbalanced and species diversity therein is low. Thus on completion of biocontrol actions, it may be necessary to restock fish assemblages with the native species that are suitable for such habitats.

Acknowledgments

We cordially thank Egidijus Leliūna and Robertas Staponkus for their assistance in the fieldwork. This study was funded by the Ministry of Environment of Lithuania via the national project Preparation of an Action Plan for the Protection of Rare Species and Regulation of the Abundance of Invasive Species (Project No. VP3-1.4-AM-02-V-01-003) and by the Research Council of Lithuania, Project No. LEK-13/2012.

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Cite this article as: Rakauskas V, Virbickas T, Stakėnas S, Steponėnas A. 2019. The use of native piscivorous fishes for the eradication of the invasive Chinese Sleeper, Perccottus glenii. Knowl. Manag. Aquat. Ecosyst., 420, 21.

All Tables

Table 1

Characteristics of studied lakes: coordinates, surface area (S); mean depth (H); maximal depth (H max); dissolved oxygen at 1 m depth (February) (DO).

In the text
Table 2

Dates of piscivorous fish stocking into bioregulated lakes in 2013–2014 and numbers of the piscivorous fish individuals stocked. Age of the stocked fish: 0+: one-summer-old fish; 1+: two-summer-old fish; etc.

In the text
Table 3

Catch per unit of effort (CPUE) of different fish species in studied water bodies during 2012–2017 (mean ± SD): pre-stocking period 2012–2013 (Pre), transitional period 2014–2015 (Transitional), and post-stocking period 2017 (Post).

In the text
Table 4

Metrics of Perccottus glenii populations in studied water bodies during 2012–2017: pre-stocking period 2012–2013 (Pre), transitional period 2014–2015 (Transitional), and post-stocking period 2017 (Post).

In the text

All Figures

thumbnail Fig. 1

Catch per unit of effort (CPUE) of Perccottus glenii in lakes Beržuvis (A), Bevardis (B), Cirkliškis (C), and Stūgliai (D) studied before (Pre: 2012–2013), during (Transitional: 2014–2015), and after (Post: 2017) the implementation of biocontrol measures, i.e. the introduction of native piscivorous fish species (median, quartiles, range). Small letters (a, b) denote homogeneous groups according to Mann-Whitney U tests.
In the text

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