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Brief Report

One Year Monitoring of Ecological Interaction of Silurus glanis in a Novel Invaded Oligotrophic Deep Lake (Lake Maggiore)

1
Department of Theoretical and Applied Sciences, University of Insubria, Via H. Dunant 3, 21100 Varese, Italy
2
Department of Biotechnology and Life Sciences, University of Insubria, Via Monte Generoso 71, 21100 Varese, Italy
*
Author to whom correspondence should be addressed.
Water 2022, 14(1), 105; https://doi.org/10.3390/w14010105
Submission received: 15 November 2021 / Revised: 2 December 2021 / Accepted: 31 December 2021 / Published: 4 January 2022
(This article belongs to the Section Biodiversity and Functionality of Aquatic Ecosystems)

Abstract

:
The European catfish (Silurus glanis) was introduced in Italy during the last century for aquaculture purposes, and now it is well-established. S. glanis is an invasive species and a top predator that can deplete prey supply in the surrounding habitat, leading to changes in the aquatic food web. Consequently, its presence is considered a threat to native fish populations. Its presence in the Lake Maggiore (Northern Italy) is recent and there is a lack of knowledge about its ability to completely exploit this new ecosystem throughout the year. This study corroborated the ability of European catfish to exploit both pelagic and littoral habitats, promoting trophic interactions in both habitats. Over 2019, multiple sampling approaches have been applied by collecting S. glanis and analysing its stomach contents with the aim of inferring interactions with the freshwater community. Its diet was mainly based on crayfish (Orconectes limosus), followed by six prey fish and the genus Corbicula; two fish species (Padogobius bonelli and Salaria fluviatilis) were added to the list of known prey fish. Notably and alarmingly for the early potential top-down pressure towards all trophic levels, young individuals were proved to also feed on fish and crayfish. S. glanis showed the ability to hunt at deep depths (>60 m) and a high growth rate, despite Lake Maggiore being oligotrophic.

1. Introduction

The introduction of non-native fish into the freshwater system has a long history across Europe [1], the successful introduction of the European catfish (Silurus glanis, L., 1758) being one of the most widespread [2]. Its introduction in Italy was for aquaculture purposes in the early 20th century, but was also introduced in ponds of private fishing reserves, and subsequently reported in rivers since the 1930s onward [3,4]. The first certain catch of an individual S. glanis was reported in the late 1960s in the River Po basin [3], of which catches became more frequent from the following decades. From the 1980s, the presence of S. glanis can be considered common and continuous in the Po valley, artificial channels included [5], and nowadays it is well-established in the eutrophic sub-alpine lakes, such as Lake Varese, Lake Comabbio, and Lake Monate [6,7]. The first reports of its presence in the oligotrophic and deep Lake Maggiore dated back to the early 1990s [8], which is now successfully colonised by S. glanis, demonstrating its remarkable ecological plasticity.
S. glanis is considered an opportunistic predator [2], and the most important factor affecting its diet is the spatial and temporal availability of prey, thus reflecting the most abundant prey available [2,9]. It is a top predator with a wide trophic niche [10,11,12], which makes its diet unpredictable. Furthermore, S. glanis can adapt its diet to novel and available resources, including developing new feeding behaviour [13]; thus, its presence in a newly invaded habitat is considered a potential threat. Across a range of dietary studies on S. glanis, almost 60 fish species have been reported [2,9]. However, its diet can also include benthic or mid-water column organisms [2,14,15], such as Chironomidae, Hemiptera, and Diptera, with macrobenthos being the main food for juveniles [2,16]. Adults are mainly ichthyophages, even though they can occasionally eat birds, insects, reptiles, and small mammals [17]. Cannibalism phenomena has been observed in S. glanis aquaculture since the juvenile stage [18]. Moreover, its diet can vary with season [9] and from the earliest to the latest stage of invasion [19]. However, proper knowledge on S. glanis trophic ecology in its invasive range is scarce, mainly restricted to riverine or reservoir populations where the fish is more easily captured [20].
Notably, very little is known about oligotrophic and deep lakes (such as the Lake Maggiore), an ecosystem very different from its original (big rivers), and only about a limited period (wintertime) [7]. Difficulties of sampling lentic ecosystems, especially big lakes, has led to a scarcity of data, with only one recent study which started to fill the gap on the ecology of S. glanis in this novel environment [7]. Taking advantage of support by professional fishermen, and the experimental usage of large mesh gillnets suitable for catching S. glanis, the authors provided a first glimpse into the trophic interaction of S. glanis with the lake community, but only over a limited period of time (wintertime) [7]. Thus, for setting management plans, it is essential to understand how the species is able to exploit the new ecosystem in its entirety with regard to both the pelagic and littoral habitat throughout the year. The aim of this study is to contribute additional knowledge about habitat exploitation of S. glanis in a novel environment, as well as its interactions with the inhabiting freshwater community. Over a year of sampling in 2019, multiple sampling approaches were put in place to (i) establish the ability of S. glanis to exploit the entire lake ecosystem by collecting individuals from littoral and pelagic habitats, and (ii) establish interactions with the freshwater community by stomach content analysis. Considering the recent invasion of this species in the Lake Maggiore, this data will provide essential baseline information to promote further in-depth investigations on S. glanis ecology in the Lake Maggiore and improve strategies for biodiversity management.

2. Materials and Methods

A total of 59 sampling efforts regularly took place between the end of January 2019 and mid-November 2019 in the Lake Maggiore at Golfo della Quassa (Ispra, Va, Italy) (Figure 1), divided in two macro categories: (i) pelagic and (ii) littoral sampling. Sampling was not performed in the littoral environment between 15th March and 1st June, and between 15 November to 24 January, due to fishing law restrictions. Thus, the former period corresponds to the breeding time of Esox sp., S. lucioperca and P. fluviatilis; the latter corresponds to Coregonus sp. spawning time. Technical equipment adopted for professional fishing in inland waters were used, mainly the bottom and flying nets for littoral and pelagic sampling, respectively (Supplementary Material S1). A 5.85 long and 2 m wide boat approved for professional fishing in inland waters was used for lowering and withdrawal of the nets. All nets adopted in this study were certified by the “Italian–Swiss Commission for Fisheries (C.I.S.P.P.)” in the “regulation implementing the convention for fishing in Italian–Swiss waters between the Italian Republic and Swiss Confederation”.
Fish retrieved in the nets with S. glanis individuals were recorded and released. All S. glanis individuals caught were measured and underwent laparotomy (Table 1). For sexually mature specimens, the sex was recorded, and in the case of female individuals, the degree of maturation of the gonads was specified. Stomach content was analysed for each individual, and the names of the species found in the stomachs were reported only in the absence of taxonomic doubts assignment; otherwise, if digestion was too advanced, it was just recorded that the stomach was full. Stomachs were weighed both when full and after content removal.

3. Results

In total, 59 sampling efforts took place, and S. glanis was caught in 23 of them (Table 2; Supplementary Tables S1–S4). A total of 72 individuals—23 pelagic and 49 littorals—were collected for analysis (except one pelagic individual who escaped from the net, Table 1). The number of littoral individuals was higher than pelagic ones, but the biomass of littoral individuals was less than the pelagic ones, being 121 kg and 138 kg, respectively. Pelagic individuals were mainly bigger than 60 cm in body length, except individual P19 that was caught during summertime (54.5 cm), and the maximum body length measured was 122 cm. On the contrary, the majority of littoral S. glanis (28 individuals) measured less than 60 cm in body length, mainly caught during summertime. The longest S. glanis, 149 cm in body length, was caught using a fishing rod (Table 1). Five individuals were juvenile, 30 immature, 21 male, and 15 female; all but one pelagic individuals were sexually mature. Female individuals caught at the end of June showed highly developed gonads, suggesting the individuals were close to spawning, whilst individuals caught in mid-July had empty gonads, indicating the end of the spawning season. Biometric data of all specimens allowed to investigate the growing rate, which showed a high rate, also considering the littoral and pelagic habitats separately (Figure 2a–c).
The minority of littoral individuals (16 in total) had empty stomachs, whilst the majority (30 individuals) presented with content in their stomachs at different stages of digestion (Table 1), of which the contents retrieved varied between 0.27 g up to 326 g. As most of the stomach content did not allow species identification, the investigation is mainly descriptive. The invasive American crayfish Orconectes limosus (Rafinesque, 1871) was found to be the predominant prey, found in 19 specimens (63%), and for 12 specimens, it was the only content in the stomach. In two samples, some freshwater clams belonging to the invasive genus Corbicula were retrieved, whilst the other components of the stomach content were fish. Specifically, S. glanis inhabiting the littoral area of the Lake Maggiore resulted to prey on S. fluviatilis, P. bonelli, A. alburnus, R. rutilus, A. agone and P. fluviatilis, mainly present as a single component of the stomach. For six specimens, it was impossible to determine the stomach content composition due to the high digestion stage. Most pelagic individuals (16 specimens) had an empty stomach, and a full stomach only for six individuals. Stomach content was exclusively composed of fish, but it was possible to identify the species in only two individuals (both cases A. agone), because of the high digestion stage. However, it seemed plausible to think that some of the preys were Coregonus sp., since, whilst catching S. glanis, Coregonus sp. individuals often were found either in the mouth of some individuals of S. glanis, or in the nets presenting obvious wounds caused by S. glanis, suggesting predation of this genus. The wounds indeed displayed the imprint of a dental arch of S. glanis, recognizable by the characteristic abrasions causing scale removal, instead of lacerations typical of other predators present in the Lake Maggiore, such as Esox sp. In two individuals with empty stomachs, it was possible to notice the presence of decapod crustaceans in their faeces.
Whilst sampling for S. glanis, a total of 14 species were found in the littoral habitat, of which seven were native, whilst only six were in the pelagic habitat, of which two were native (Table 2). In the pelagic habitat, observations of Coregonus sp. were predominant, as the nets available for sampling were specific to that genus. There was no opportunity to catch A. alburnus, S. fluviatilis and P. bonelli due to their small size, although their presence was confirmed by stomach content analysis. Interestingly, two invasive species that are not considered pelagic species, R. rutilus and S. lucioperca, were caught by flying nets (pelagic environment) during summertime (Supplementary Table S4).

4. Discussion

This study corroborated the ability of S. glanis to exploit both pelagic and littoral habitats in the Lake Maggiore, and its capability to hunt in the deep area of the lake. Indeed, an individual (L2) was caught at more than 60 m depth, supporting its ecological plasticity [9]. Although due to fishing law restrictions, it was not possible to catch S. glanis in the littoral habitat during springtime, the presence of S. glanis in the pelagic habitat was preponderant towards that time (Supplementary Table S4), and the presence of A. agone in the stomach confirmed its interaction at the pelagic trophic level. All pelagic individuals except one were found sexually mature, suggesting the presence of S. glanis in the pelagic habitat before spawning season, usually when the temperature reaches at least 18–19 °C around June, possibly due to the higher trophic contribution this habitat can provide. In the pelagic habitats, individuals bigger than the littoral ones retrieved, where a lack of individuals under 60 cm body length could suggest the absence of S. glanis in the pelagic habitat of younger individuals.
A total of 60 fish species, of which cyprinids are predominant, were identified in the diet of S. glanis [2,7,9], and this study added two more fish species, P. bonelli and S. fluviatilis, as well as Corbicula sp. The diet of S. glanis in the Lake Maggiore described here was based on six fish species (A. agone, A. alburnus, P. bonelli, P. fluviatilis, S. fluviatilis and R. rutilus), and Coregonus sp. was suspected. However, the invasive crayfish O. limosus was predominant in the stomach content, suggesting its relevant importance in the S. glanis diet. This might be due to the high abundance of this species in the Lake Maggiore and the ease of its capture compared to other prey [2,9,19]. O. limosus is an invasive species whose presence in Italy has been recorded since 1991 when it was accidentally introduced from Poland [21], and which is proliferating well in lakes of Northern Italy; its presence is considered a major threat to biodiversity and considered of Union Concern [22]. Another invasive crayfish considered of Union Concern [22], and thus a threat for biodiversity, is Procambarus clarkii (Girard, 1985), regularly found in Lake Maggiore since 2001. Unexpectedly, it was not found in any S. glanis individuals analysed in this study. This finding may be justified by the fact that its occurrence seemed to be more restricted to the southern part of the Lake [21], and further investigations are required to infer the pressure S. glanis may have on this invasive species. Another invasive species of the Lake Maggiore retrieved in stomach content is Corbicula spp., first recorded in 2010, and well-established in the southern basin [23]. P. bonelli and S. fluviatilis were mainly retrieved in smaller individuals, probably because small S. glanis tend to spend much of their time hiding among stones and rocks, which is the habitat of P. bonelli and S. fluviatilis.
Previous studies reported the diet of S. glanis being mainly based on macrobenthos before shifting to preying upon cyprinids at a larger size, that is, until reaching 30–35 cm body length [6,16,17], as well as crayfish [19]. On the contrary, in this study, the minimum size of S. glanis with a full stomach was 11.8 cm in body length (individual L42), and it was possible to recognise its presence in the stomach of a S. fluviatilis which was 4 cm in length, as well as for individual L43 (13.4 cm body length) in which it was possible to find a S. fluviatilis and individual L46 (12.8 cm body length) which had stomach content composed of S. fluviatilis and P. bonelli, revealing the ability of young S. glanis to eat not just macrobenthos. Notably, it is thus the absence of macrobenthos in the stomach content of S. glanis, especially for younger individuals, which represents the main diet component of young S. glanis individuals inhabiting the nearby Lake Varese and Ticino River [16]. This feeding ability of young individuals poses the need for a better understanding of the trophic ecology of S. glanis. Furthermore, the growing rate of S. glanis individuals was high, comparable to one of the nearby, but eutrophic, Varese and Comabbio Lakes [16]. Growth in S. glanis is highly variable, depending on their habitat [2]; individuals from both pelagic and littoral habitats in this study showed a high growth rate, which is interesting considering that Lake Maggiore is oligotrophic, demanding an in-depth focus of this species in this novel invaded environment.
Despite the limited number of individuals caught and number of sites investigated, due to sampling difficulties in lentic environments without widespread support from commercial and professional fishermen, this study stresses the need to further investigate the potential pressure of this species, with special attention on the population growth trend in the pelagic habitat. Although there are many difficulties in gathering more information due to limited logistic support (i.e., difficulties in catching samples from both habitats covering the whole ecosystem), the involvement of fishermen, citizen scientists, and more refined analysis (i.e., DNA barcoding of stomach content, stable isotope analysis, environmental DNA) could offer focal tools to further study biological invasions [24,25]. Considering the recent invasion of this species, this study added important baseline information to justify the collection of more refined quantitative data over a long period, to better investigate how S. glanis could affect native fauna, and aim to plan proper strategies for biodiversity management.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/w14010105/s1, “Sampling methods for littoral environment” and “Sampling methods for pelagic environment”, supported by Table S1: Details of littoral sampling through “voltana” nets. date of net lowering (d1) and time (t1), date of net withdrawal (d2) and time (t2), water depth and water temperature (T) are detailed, Table S2: Details of littoral sampling through “Reet de pes bianc” nets. Date of net lowering (d1) and time (t1), date of net withdrawal (d2) and time (t2), water depth and water temperature (T) are detailed. Table S3: Details of littoral sampling through “Reet de bundela” nets. Date of net lowering (d1) and time (t1), date of net withdrawal (d2) and time (t2), water depth and water temperature (T) are detailed, and Table S4: Details of pelagic sampling through “Reet de bundela volante” nets. Date of net lowering (d1) and time (t1), date of net withdrawal (d2) and time (t2), water depth and water temperature (T) are detailed.

Author Contributions

Conceptualization, C.M.A. and S.Z.; sampling T.C.; methodology, T.C., M.C. validation, formal analysis, investigation C.M.A., T.C., M.C.; resources, data curation, C.M.A.; writing—original draft preparation, C.M.A.; review and editing, C.M.A., T.C., M.C. and S.Z.; visualization and supervision, S.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Full raw data are available from authors upon reasonable request.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Sampling location in the Lake Maggiore near the town Ispra. The grey rectangle indicates the area where littoral sampling took place, whilst the white ellipse indicates the area of pelagic sampling.
Figure 1. Sampling location in the Lake Maggiore near the town Ispra. The grey rectangle indicates the area where littoral sampling took place, whilst the white ellipse indicates the area of pelagic sampling.
Water 14 00105 g001
Figure 2. Growing rate of (a) Silurus glanis in the Lake Maggiore based on weight and length of all individuals. (b) only for individuals caught in the littoral habitat. and (c) only in the pelagic habitat.
Figure 2. Growing rate of (a) Silurus glanis in the Lake Maggiore based on weight and length of all individuals. (b) only for individuals caught in the littoral habitat. and (c) only in the pelagic habitat.
Water 14 00105 g002
Table 1. Description of Siluro glanis individuals caught in this study. Name of the individual (ID), habitat of sampling, depth of sampling (metres) specimen weight (grams), specimen length (millimetres), water temperature (T), sex and stomach status, and species identified in the stomachs are indicated.
Table 1. Description of Siluro glanis individuals caught in this study. Name of the individual (ID), habitat of sampling, depth of sampling (metres) specimen weight (grams), specimen length (millimetres), water temperature (T), sex and stomach status, and species identified in the stomachs are indicated.
IDHabitatDepth
(m)
Weight
(g)
Length
(mm)
T
(°C)
SexStomachAlosa agoneAlburnus alburnusPadogobius bonelliPerca fluviatilisSalaria fluviatilisRutilus rutilusCorbicula sp.Orconectes limosus
L1Littoral3765010507.2MaleEmpty
L2Littoral>6035808008.7ImmatureEmpty
L3LittoralNa501435NaImmatureFull
L4LittoralNa50943522.5ImmatureFull
L5Littoral3–6279575717MaleFull
L6Littoral3–6221570517MaleFull
L7Littoral3–6320081018.3MaleFull
L8Littoral3–6330084018.3MaleFull
L9Littoral4–614827017.9ImmatureEmpty
L10Littoral4–621933017.9ImmatureEmpty
L11Littoral4–671847817.9ImmatureFull
L12Littoral5–87200101519.8FemaleFull
L13Littoral5–88925112019.8MaleFull
L14Littoral5–811,150116019.8FemaleEmpty
L15Littoral6–8702098519.6FemaleEmpty
L16Littoral4–614327022.2ImmatureEmpty
L17Littoral4–631835522.2ImmatureFull
L18Littoral3–6650099023FemaleFull
L19Littoral3–6520087023FemaleFull
L20Littoral4–792150523.4ImmatureFull
L21Littoral824,8001490NaMaleEmpty
L22Littoral5–78400109025.5MaleFull
L23Littoral3–581050525.5ImmatureFull
L24Littoral3–534538225.5ImmatureFull
L25Littoral3–519730025.5ImmatureFull
L26Littoral3–579048023.7ImmatureFull
L27Littoral3–5325380NaImmatureEmpty
L28Littoral3–5880510NaImmatureEmpty
L29Littoral3270365NaImmatureEmpty
L30Littoral3–583553022.7ImmatureFull
L31Littoral3–553547222.7ImmatureFull
L32Littoral383048523.2ImmatureFull
L33Littoral332039023.2ImmatureFull
L34Littoral3–573850022.8ImmatureFull
L35Littoral3–539739522.8ImmatureFull
L36Littoral3–519831222.8ImmatureEmpty
L37Littoral3–51085540NaImmatureFull
L38Littoral3–5624465NaImmatureEmpty
L39Littoral5–1082950022.5ImmatureFull
L40Littoral5–1084550021.5ImmatureFull
L42Littoral0.1–115.3118NaJuvenileFull
L43Littoral0.1–121.85134NaJuvenile-
L44Littoral0.1–18.87106NaJuvenile-
L45Littoral0.1–112.78117NaJuvenile-
L46Littoral0.1–117.86128NaJuvenile-
L47Littoral5–10219070518.5MaleFull
L48Littoral5–10170064018.5MaleFull
L49Littoral5–1534637818ImmatureEmpty
L50Littoral5–1585151018ImmatureEmpty
P1Pelagic3513,20012208.1FemaleFull
P2Pelagic3548008308.1FemaleFull
P3Pelagic3518006708.1MaleFull
P4Pelagic3522007408.1MaleEmpty
P5Pelagic3013,60012109FemaleEmpty
P6Pelagic3011,30012109MaleEmpty
P7Pelagic3058409309FemaleFull
P8Pelagic3035108009FemaleEmpty
P9Pelagic3033507809MaleEmpty
P10Pelagic3048509009FemaleFull
P11Pelagic3034208259.1MaleEmpty
P12Pelagic3049508809.1MaleEmpty
P13Pelagic3063709709.1FemaleEmpty
P14Pelagic3010,40011609.1MaleEmpty
P15Pelagic30774010089.1FemaleFull
P16Pelagic147210102012.2MaleEmpty
P17¥Pelagic25--15.7--
P18Pelagic1574501040NaMaleEmpty
P19Pelagic9110054516ImmatureEmpty
P20Pelagic206350970NaFemaleEmpty
P21Pelagic2069801005NaFemaleEmpty
P22Pelagic20226568813MaleEmpty
P23Pelagic209750115013MaleEmpty
Table 2. Littoral and pelagic fish community description. Species found during sampling, its native or invasive status, and number of sampling occasions the species were retrieved in each environment (cf. Supplementary Tables S1–S4).
Table 2. Littoral and pelagic fish community description. Species found during sampling, its native or invasive status, and number of sampling occasions the species were retrieved in each environment (cf. Supplementary Tables S1–S4).
SpeciesStatusLittoralPelagic
Alosa agoneNative228
Carassius carassiusInvasive3-
Coregonus sp.Invasive246
Esox sp.Native6-
GymnocephaluscernuusInvasive4-
Lepominus gibbosusInvasive5-
Lota lotaNative2-
Perca fluviatilisNative20-
Rutilus rutilusInvasive242
Salmo trutta complexNative-4
Sander luciopercaInvasive214
Scardinius erythrophthalmusNative7-
Siluro glanisInvasive2312
Squalius cephalusNative3-
Tinca tincaNative5-
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Antognazza, C.M.; Costantini, T.; Campagnolo, M.; Zaccara, S. One Year Monitoring of Ecological Interaction of Silurus glanis in a Novel Invaded Oligotrophic Deep Lake (Lake Maggiore). Water 2022, 14, 105. https://doi.org/10.3390/w14010105

AMA Style

Antognazza CM, Costantini T, Campagnolo M, Zaccara S. One Year Monitoring of Ecological Interaction of Silurus glanis in a Novel Invaded Oligotrophic Deep Lake (Lake Maggiore). Water. 2022; 14(1):105. https://doi.org/10.3390/w14010105

Chicago/Turabian Style

Antognazza, Caterina M., Tommaso Costantini, Monica Campagnolo, and Serena Zaccara. 2022. "One Year Monitoring of Ecological Interaction of Silurus glanis in a Novel Invaded Oligotrophic Deep Lake (Lake Maggiore)" Water 14, no. 1: 105. https://doi.org/10.3390/w14010105

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