Received: 9 November 2018 | Revised: 7 March 2019 | Accepted: 11 March 2019

DOI: 10.1111/eff.12481

ORIGINAL ARTICLE

When alien catfish meet—Resource overlap between the North

American Ictalurus punctatus and immature European Silurus
glanis in the Arno River (Italy)

Phillip Joschka Haubrock1,2,3 | Martina Azzini4 | Paride Balzani4 |

3,4 4
Alberto Francesco Inghilesi | Elena Tricarico

1
Department of River Ecology and
Conservation, Senckenberg Research Abstract
Institute and Natural History Museum Due to the increasing globalisation and ongoing introduction of alien species specifi‐
Frankfurt, Gelnhausen, Germany
2 cally regarding European freshwater ecosystems, native and already present alien
Faculty of Fisheries and Protection
of Waters, South Bohemian Research species will be confronted with competitors with unknown outcomes. One such case
Center of Aquaculture and Biodiversity of
is the situation of the European catfish Silurus glanis introduced in the Arno River
Hydrocenoses, University of South Bohemia
in České Budějovice, Vodňany, Czech (Central Italy), a species sought after by anglers, which is facing competition from the
Republic
later introduced alien North American channel catfish Ictalurus punctatus. Large cat‐
3
NEMO, Nature and Environment
Management Operators s.r.l., Florence, Italy
fish species are highly valued among anglers, but their interspecific interactions and
4
Department of Biology, University of potential ecosystem‐level impacts are still poorly known. We used stomach contents
Florence, Florence, Italy and stable isotope analyses to study niche partitioning between these two alien cat‐
Correspondence fish species, coexisting in the Arno River. The results suggest partial niche segrega‐
Phillip Joschka Haubrock, Department tion, with immature S. glanis showing a narrower dietary and isotopic niche and a
of River Ecology and Conservation,
Senckenberg Research Institute and Natural slightly higher trophic position than I. punctatus. Monitoring the catfish population
History Museum Frankfurt, Gelnhausen, sizes, trophic niches and effects on lower trophic levels are essential for future man‐
Germany.
Email: [email protected] agement and mitigation of their potential impacts on invaded freshwater
ecosystems.
Funding information
2020 Marie Sklodowska‐Curie, Grant/Award
Number: ITN-2014-ETN-642197 KEYWORDS
alien species, dietary analysis, interactions, isotope analyses, niche overlap, niche partitioning

1 | I NTRO D U C TI O N Britton, 2017; Strayer, 2010), the current issue is to understand in‐
teractions among alien species (Bissattini & Vignoli, 2017 ; Ricciardi,
In some cases, introduced species served human well‐being (Ewel 2001). Particularly interesting, even if difficult to address, is the sce‐
et al., 1999) without significantly affecting the recipient environ‐ nario of a top predator confronted with the introduction of another
ment (Jerscke & Strayer, 2005; Williamson & Fitter, 1996a,1996b). potential alien top predator that originates from a different area, and
Nonetheless, many alien species become invasive and dominate na‐ how relationships with other present species are affected (Griffen,
tive communities (Crooks, 2002; Kolar & Lodge, 2001), leading to‐ Guy, & Buck, 2008; Wei, Wu, & Guo, 2012).
wards a homogenisation of ecosystems (Mack et al., 2000; Rahel, As in many Europeans countries (Gherardi, Gollasch, Minchin,
2000). While interactions among alien and native species have re‐ Olenin, & Panov, 2009), alien fish rapidly increased over the past
cently received increasing attention (Balzani et al., 2016; Busst & 25 years (e.g., Italy: 40 out of 105 species—38% are alien species;

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2019 The Authors. Ecology of Freshwater Fish Published by John Wiley & Sons Ltd

Ecol Freshw Fish. 2019;1–14. 

wileyonlinelibrary.com/journal/eff | 1
2 | HAUBROCK et al.

Gherardi et al., 2008; Nocita & Zerunian, 2007). This process has re‐ LIFE03NAT/IT/000113 and LIFE15 NAT/IT/000989). Furthermore,
shaped most freshwater communities. Although some introductions these two species of catfish have different feeding strategies. With a
might have occurred accidentally, a significant proportion of species fast expansion of the mouth while keeping opercular valves closed in
has been voluntarily introduced by anglers and sport fishing associ‐ the beginning to maximise the sucked volume, S. glanis imbibes prey
ations to improve recreational fishing. inside its oral opening (Bruton, 1996). In contrast, the exact morpho‐
One such species is the European or Wels catfish Silurus glanis dynamic prey mechanism of I. punctatus has not been studied, but a
(Linnaeus, 1758), a fish native to north‐eastern Europe and Asia. It combination of sucking and pursuing‐and‐biting is possible (Pavlov &
is known to be the largest freshwater Osteichthyes in Europe (max Kasumyan, 2002). Moreover, length–weight relationships and thus
size 2.7 m and 130 kg; Stone, 2007; Boulêtreau & Santoul, 2016). growth rates might differ between both species. However, they are
In the last decades, S. glanis experienced a drastic increase in pop‐ ecosystem and factor depending. Moreover, information for both
ulation size and distribution due to angling activities (Copp et al., I. punctatus in Europe as well as S. glanis from the Arno River has not
2009; Cunico & Vitule, 2014). It was introduced in Italy in the 1990s yet been assessed and remains anecdotal. Furthermore, such infor‐
(Balma, Delmastro, & Forneris, 1989) and was subsequently spread mation is needed to better understand the impact these species have
throughout the Italian peninsula with diverse impacts on native and on recipient ecosystems (Haubrock, Balzani, Johovic, et al., 2018b).
also newly introduced species (Castaldelli et al., 2013). In the Arno However, the diet of I. punctatus has been recently analysed by col‐
River Basin, it was most likely introduced to Bilancino Lake and then lecting stomach contents of specimens in the Arno River (Haubrock,
spread downstream towards the Sieve River (a tributary of the Arno Balzani, Johović, et al., 2018a; Haubrock et al., 2017). In contrast,
River; Gualtieri, Mecatti, & Cecchi, 2010). In the Florentine stretch recent and relevant data for S. glanis’ feeding habit from Central Italy
of the Arno River, S. glanis has been reported by anglers since 2004 are preliminary or anecdotal (Gualtieri & Mecatti, 2005), making
(Gualtieri & Mecatti, 2005). In the course of a few years, this species investigating facilitation processes or interfering competition pro‐
has become the target of many anglers. The increased investiga‐ cesses difficult.
tion into invasive S. glanis revealed considerable positive economic Interactions between alien top predators are very likely, be‐
(Cucherousset et al.., 2017; Rees et al., 2017) but negative environ‐ cause in fish communities, resource partitioning mainly occurs along
mental impacts (Castaldelli et al., 2013; Copp et al., 2009). the trophic dimensions, that is across trophic levels (Ross, 1986).
At the same time, the North American channel catfish Ictalurus According to the competitive exclusion principle (Hardin, 1960),
punctatus (Rafinesque, 1818) was also introduced to Italy. However, coexistence can only be possible if utilised resources and occupied
information on pathways and means of introduction remain scarce dimensions (activity time, habitat use) are different (Chase & Leibold,
(Haubrock, Balzani, Johović, Inghilesi, & Tricarico, 2018a; Haubrock 2003; Schoener, 1986). Studies investigating dietary and, thus, di‐
et al., 2017; Ligas, 2008). In the Arno River, according to catches by etary niche partitioning mostly focused on either mature life stages
local authorities and anglers, it is likely that I. punctatus was intro‐ (Schulze, Dörner, Baade, & Hölker, 2012; Zaia Alves et al., 2017) or
duced near Pisa for the purpose of angling and was subsequently ontogenetic variations (Davis, Blanchette, Pusey, Jardine, & Pearson,
transported upriver (G. Castaldelli pers. comm.) as it is increasingly 2012; Tarkan et al., 2018). However, immature life stages in catfish
favoured by anglers due to its high reproduction rate and catchabil‐ species can dominate an ecosystem and have a considerable impact
ity (T. Busatto pers. comm.). In the inner‐Florence stretch of the Arno on other species as well as the potential to become a target to man‐
River, it first appeared in 2004 (A. Nocita pers. comm.). ifold interaction with other species (Alp, Kara, & Büyükçapar, 2004;
Catfish such as S. glanis have specific functions in ecosystems, Alp, Kara, Üçkardeş, Carol, & García‐Berthou, 2011; Elrod, 1974;
affecting various ecological groups with their presence. S. glanis is Persson, 1988).
known to be a generalist that is capable of rapidly adapting to new Stomach content analyses can provide a direct insight into re‐
prey sources (Vejřík et al., 2017). However, data about the diet of im‐ cently consumed items and, consequently, feeding behaviour of
mature (<60–80 cm) S. glanis from alien populations (but see Gualtieri different life stages, while stable isotope analysis (SIA) provides long‐
& Mecatti, 2005, and Syväranta et al., 2010, for a basic analysis of term dietary information. Both combined allow a reconstruction of
S. glanis’ diet) and about interactions with other catfish species are the studied communities’ trophic web and the investigation of niche
scanty. Similarly, much more information is available about genetics partitioning (Boecklen, Yarnes, Cook, & James, 2011; Layman et al.,
and physiology of I. punctatus in regard to aquaculture usage, but 2012). This is possible because isotopic signatures relate with the
most studies that investigated the behaviour of I. punctatus are con‐ trophic position (nitrogen, N) and with the main energy source (car‐
siderably old, with a minority of studies focusing on its invasiveness bon, C) of a consumer (Layman et al., 2012). Additionally, SIA allows
and diet (Busbee, 1968; Haubrock, Balzani, Johović, et al., 2018a; the estimation of trophic levels (Post, 2002) and quantification of
Rosen, Schwalbe, Parizek, Holm, & Lowe, 1995). feeding niches (Jackson, Parnell, Inger, & Bearhop, 2011; Newsome,
Although these two catfish species are morphologically unequal, Martinez del Rio, Bearhop, & Phillips, 2007; Swanson et al., 2015).
with S. glanis reaching larger sizes, they are highly tolerant to environ‐ The degree of overlap among isotopic niches of different species
mental factors and show high invasive capabilities (Copp et al., 2009; can therein be assessed to evaluate the potential food competition
Hilge, 1985). Control activities on S. glanis have been carried out in between species (Balzani et al., 2016; Layman et al., 2012) and niche
countries such as Italy (see, e.g., Pascale et al., 2013; LIFE‐Project partitioning (Barbour et al., 2009; Werner, 1979).
HAUBROCK et al. | 3

FIGURE 1 Sampling areas within the inner‐city section of the Arno River in Tuscany (N43.7648903, E11.2697444)

Over the last years, many anglers and local authorities reported rains, negatively affecting the sampling. The far west end of the
steadily decreasing catches of S. glanis (abundance and biomass) in inner‐Florence river stretch was chosen due to its accessibility for
the Arno River within Florence while simultaneously the amount of fishing and the low human activity on both riversides (Figure 1).
I. punctatus increased (Gherardi et al., 2008; Nocita, 2007; Nocita The sampling area was characterised by high turbidity and no
& Zerunian, 2007). Hence, the present work uses a combined ap‐ aquatic vegetation with scarce vegetation on river banks during
proach of stomach content and stable isotope analyses from both the first half of the sampling period due to seasonal patterns and
co‐occurring species (immature and mature I. punctatus, immature anthropogenic disturbance. Fish were caught using standard fish‐
S. glanis) in order to investigate the degree of interspecific interac‐ ing rods (2.20–3.90 m), 0.30–0.44 mm monofilament line and size
tions (e.g. feeding competition or prey partitioning), thereby aiming 2–26 fishing hooks baited with a variety of food (maggots, worms,
to determine whether the presence of I. punctatus potentially affects and freshly cut liver or baitfish) placed (a) on the bottom, (b) in the
the population of S. glanis. middle water and (c) below the surface. Caught specimens were
euthanised (gill cuts) and put on ice before being transported to
the laboratory for further processing. In total, 40 individuals of
2 | M ATE R I A L S A N D M E TH O DS
I. punctatus were sampled and the stage of maturity was set ac‐
cording to Haubrock, Balzani, Johovic, et al. (2018b) as 31.9 cm,
2.1 | Sampling
resulting in 20 “immature I. punctatus” and 20 “mature I. puncta‐
Sampling was conducted twice a week, once in the morning tus.” Additionally, 39 individuals of “immature S. glanis,” recognised
(3–8 a.m.) and evening (4–11 p.m.) between May and June 2018, by the lack of mature and visible gonads and size ranges for im‐
as these months are considered an ideal activity period for both mature individuals in this species identified by Copp et al. (2009),
species (samples were taken after the initial 2‐month period of re‐ were sampled and are referred to as “S. glanis.” Older and bigger
sumed activity, following the inactive winter months). These times S. glanis were not sampled due to (a) their rarity in the sampled
were chosen because S. glanis shows its activity mostly during stretch and (b) local pressure by anglers.
the night with peaks of activity before sunrise and after sunset
(Carol, Zamora, & García‐Berthou, 2007) while I. punctatus shows
2.2 | Sample preparation
diurnal and nocturnal activity with highest feeding activity during
dusk and dawn (Boujard & Leatherland, 1992). Moreover, February For all specimens, total length (TL; cm) was measured with an accu‐
and March are typically periods of high water currents and strong racy of 1 mm and body weight (FW ) with an accuracy of 1 g. Values
4 | HAUBROCK et al.

reported in the text are average plus or minus the standard devia‐ are the proportions of the ith resource used by the jth and kth species.
tion. Specimens were stored in a freezer (−20°C) until stomach con‐ Both estimates for diet overlap were used together, as Pianka's mea‐
tents were extracted for dietary analyses. For SIA, a sample of dorsal sure of niche overlap alone can be insufficient to identify a relation
muscle tissue was taken from each specimen, preserved without any between niche overlap and competition, that is resource partitioning
chemicals and stored in a freezer (−20°C). Samples were dried in an (Krebs, 1999). We utilised a permutational analysis of variance
oven at 60°C for 48 hr and ground into a fine and homogenised pow‐ (PERMANOVA; S17 Bray–Curtis similarity, 3 fixed factor, three lev‐
der with an agate mortar and pestle. For each sample, approximately els: “immature I. punctatus,” “mature I. punctatus” and “S. glanis”; Type
0.25 mg of powder was weighed and packed into a tin capsule for III (partial) sum of squares, unrestricted permutation of raw data, 1
isotopic analyses. Samples were analysed with an elemental analyser dummy variable) and pairwise comparisons using the software
(FlashEA 1112) connected to an isotope ratio mass spectrometer PRIMER (Clarke & Warwick, 2001) to determine whether diets var‐
(Thermo Finnigan Delta Plus Advantage) at the National Research ied between species and life stages.
Council in Montelibretti, Rome.

2.4 | Stable isotope analyses

2.3 | Growth and dietary analyses
The trophic position of every individual (TPc) was calculated by ap‐
As fish length affects fish weight, examination of the length– plying the equation TPc = ((δ15 Nc − δ15 Nbase )∕ΔN) + 𝜆, where δ15Nc is
weight relationship was achieved with a logarithmic transformation the mean δ15N of the consumer, δ15Nbase the mean δ15N of primary
of fish weight and length. Applying a linear regression model, the producer (Potamogeton nodosus, n = 5), ΔN the standard enrichment
slope of both linear models was used as a proxy to identify growth of 3.4 ‰ between trophic levels, and λ the basal trophic level (=
types (allometric vs. isometric; Karachle & Stergious, 2012). Thus, 1 for plants) (Britton et al., 2018; Post, 2002). A primary producer
the species‐specific growth was compared by testing for homoge‐ was chosen rather than a primary consumer (e.g., molluscs) due to
neity of slopes in an analysis of covariance (ANCOVA; Dhillon & the lower variability of stable isotope values in plants (Bissattini, &
Fox, 2004) with the state “species” used as categorical independ‐ Vignoli, 2017 ; McClelland, Valiela, & Michener, 1997) and the pos‐
ent variable. To compare the weight gained with increased length, sibility of high as well as variable δ15N values in primary consum‐
weight was set as the dependent variable and length as covariate. ers due to the nitrogen‐accumulating nature of the also present
The weight of ingested food (ST W ) was expressed as the percen‐ Phragmites australis.
tal weight of the specimens total weight (FW ) following the approach A linear regression model was applied to investigate potential re‐
of Hureau (1969): FI = (100*ST W )/FW, where FI is considered as the lationships between TL of S. glanis as well as I. punctatus and stable
fullness index. Only cardiac, caecum and pyloric parts were consid‐ isotope values, while the relationship between the two was anal‐
ered without discarding contents of the intestine. The feeding inten‐ ysed for potential correlations (Spearman, statistic: rs). Additionally,
sity was calculated using the vacuity index (VI), as the percentage of to estimate and quantify intraspecific niche width and, thus, being
empty stomachs with respect to stomachs that contained prey items able to compare species, Layman's metrics (Layman, 2007; Layman,
(Batistić et al., 2005). The diet breadth was estimated based on Arrington, Montaña, & Post, 2007) were calculated with the R‐pack‐
Levin's index formula (Whittaker, Levin, & Root, 1973): Bi = 1
∑ 2 age SIAR (Stable Isotope Analysis in R; Parnell, Inger, Bearhop, &
pi
Jackson, 2010).
where Bi is the standardised index of diet breadth for specimen i and
δ15N and δ15C ranges (NR and CR) as well as the mean distance
p the sum of the squared proportion of each prey item of specimen I
to the centroid (CD) are measurements of the extent of the δ15N/
(Levins, 1968). For further analyses, the stomach content data were
δ15C bi‐plot, reflecting the community niche width. The mean nearest
expressed as frequency of occurrence (F% = number of stomachs
neighbour distance (MNND) and the standard deviation of the near‐
containing each food item in relation to total number of full stom‐
est neighbour distance (SDNND) relate to the distance of species and
achs) and abundance (N% = the number of individuals of each food
indicated the degree of trophic redundancy. While Layman's metrics
item with respect to the total number of individuals). With these, the
are usually employed in community‐wide analyses, they can be used
prominence value (PV) for each dietary component was estimated
to compare species present within one ecosystem without consid‐
following the approach of Hickley, North, Muchiri, and Harper
√ eration of the entire species community (Bissattini, & Vignoli, 2017;
(1994): PV = N% ∗ F% to estimate the diet overlap index α using the
�n
∑�
� Jackson et al., 2011; Layman, 2007). Additionally, the corrected stan‐
formula of Schoener (1986): ∝ = 1 − 0.5 �PVxi − PVyi � , with n
�
i=1
� � dard ellipse area (SEAc; considering 40% of central data points) and
being the number of food items, PVxi the prominence value of food the corresponding 95% ellipse area (SEAb), which are convex hull areas
item i in species xi and PVyi the prominence values of food item i in encompassing a sampled population in a δ15N/δ15C bi‐plot space and
species y. The estimated index varies between 0, that is no overlap, serve as measures of total isotopic niche space occupied, were calcu‐
and 1, when diets are identical (Wallace, 1981). Pianka's measure of lated for both species and life stages for I. punctatus. With these, the
diet‐based niche overlap (Pianka, 1974) for species j and species k degree of isotopic niche overlap (which lays between 0, i.e., no over‐
lapping, and 1, completely overlapping) can be estimated and subse‐
∑n
pp
using the formula Oj&k = √∑n j ∑k n
j
was calculated, where pij and pik
quently used as a quantitative measure for similarity within the diet of
2 2
i pj i pk
HAUBROCK et al. | 5

F I G U R E 2 Log‐transformed
length–weight relationship of Ictalurus
punctatus (black; y = 3.1177x − 2.2405;
R2 = 0.9874) and Silurus glanis (grey;
y = 2.4836x − 1.5297; R2 = 0.84)

different species (Jackson et al., 2012). Calculations were computed was positive; however, growth type was significantly different
using the R package SIBER (Jackson et al., 2011). Furthermore, the per‐ among species (ANCOVA, T = 74.376; df = 1; p < 0.001; Figure 2).
centual isotopic niche overlap between groups was calculated using Resultant, I. punctatus growth type can be seen as nearly isomet‐
the formula of Stasko, Johnston, and Gunn (2015). ric (similar length–weight growth), while “S. glanis” grow slower in
The directional pairwise probability of species to exert overlap‐ weight than in length.
ping niche width was estimated for I. punctatus and S. glanis using the
R‐package “nicheROVER,” which applies a Monte Carlo estimation
3.1 | Dietary analyses
(chain length: 10,000 steps) on the potential overlap. Thus, the pack‐
age computes the directional pairwise probability of the niche of one From the 40 sampled I. punctatus, all contained prey items (VI = 100%),
species (not either species) overlapping onto the niche of another to while from the collected S. glanis, 19 stomachs (VI = 48.7%) were
quantify trophic relationships (Swanson et al., 2015). found empty. FI of I. punctatus was 8.4 ± 3.3% (immature 8.2 ± 3.5;
Lastly, a PERMANOVA (1 fixed factor, three levels: “immature mature 8.7 ± 3.1) and 3.2 ± 1.8 for “S. glanis.” The diet of both spe‐
I. punctatus,” “mature I. punctatus” and “S. glanis”; Type III (partial) sum cies as well as life stages of I. punctatus was significantly differ‐
of squares, unrestricted permutation of raw data) was performed ent (PERMANOVA, F = 9.0434; df = 2; p < 0.05; post hoc tests:
15 13
to test for significant differences in δ N and δ C levels among t = 1.4282; p < 0.05). The most common food source for I. punctatus
life stages as well as species and to eventually determine whether was the easily accessible prey items, detritus and plants (F% = 0.55;
groups and/or species are clearly distinguishable by either isotope. N% = 0.28), followed by Palaemonetes sp. (F% = 0.35; N% = 0.20),
Additionally, a canonical analysis of principal coordinates (CAP) for terrestrial (F% = 0.40; N% = 0.18) and aquatic insects (F% = 0.35;
factors whose levels were identified by the PERMANOVA test to N% = 0.09), and lastly small cyprinids (juvenile Cyprinus carpio
be significantly different was applied to identify how δ15N and δ13C Linnaeus, 1758, Alburnus alburnus Linnaeus, 1758, Pseudorasbora
contribute to differentiate the levels. Pearson correlations with CAP parva Temminck & Schlegel, 1846; F% = 0.20; N% = 0.05). The oc‐
axis for each variable are reported. For all tests, the level of signifi‐ currence of detergent in I. punctatus, potentially remnants from
cance under which the null hypothesis was rejected is α = 0.05. water cleaning plants or fishermen's bait, was previously discussed
(Haubrock, Balzani, Johovic, et al., 2018b). Utilising the estimated
prominence value (PV) as an indicator of the importance of a prey
3 | R E S U LT S item indicated that Palaemonetes sp., terrestrial insects and plants
were most important for the diet of I. punctatus. For S. glanis, small
Overall, 40 individuals of I. punctatus (mean TL = 33.8 ± 2.2 cm; cyprinids and plant material were dominant food items (Table 1).
mean FW = 538.5 ± 672.1 g) consisting of 20 immature (mean The diet‐based niche breadth for I. punctatus was 8.1 for immatures,
TL = 22.4 ± 1.4 cm; mean FW = 117.8 ± 96.3 g) and 20 mature speci‐ 6.7 for mature specimens and 8.8 for the overall population, while
mens (mean TL = 45.2 ± 2.1 cm; mean FW = 959.2 ± 738.5 g) were S. glanis showed a lower niche breadth (B = 5.6) than I. punctatus.
collected. S. glanis (n = 39; mean TL ± SD = 27.1 ± 1.1 cm; mean The niche overlap was moderately high between “immature I. punc‐
FW ± SD = 122.8 ± 89.9 g) matched the size range of sampled I. punc‐ tatus” and “mature I. punctatus” as well as “mature I. punctatus” or be‐
tatus, enabling a direct comparison. The growth type of both species tween the total population of I. punctatus and “S. glanis.” In contrast,
6 | HAUBROCK et al.

TA B L E 1 Frequency of occurrence (%F), abundance (%N), and prominence value (PV) of food items analysed for Ictalurus punctatus and
Silurus glanis

Ictalurus punctatus Ictalurus punctatus

(immature) (mature) Ictalurus punctatus (Total) Silurus glanis (immature)

Prey items [F%] [N%] [PV] [F%] [N%] [PV] [F%] [N%] [PV] [F%] [N%] [PV]

Detritus 0.30 0.08 0.05 0.25 0.04 0.02 0.30 0.06 0.03 0.10 0.09 0.03
Plants 0.45 0.09 0.05 0.60 0.14 0.11 0.45 0.12 0.08 0.13 0.11 0.04
Detergent 0.20 0.08 0.05 0.05 0.01 0.00 0.20 0.04 0.02 0.00 0.00 0.00
Palaemonetes sp. 0.25 0.18 0.11 0.15 0.04 0.02 0.25 0.10 0.05 0.03 0.02 0.00
Dikerogammarus villosus 0.18 0.14 0.05 0.20 0.03 0.02 0.18 0.08 0.03 0.05 0.07 0.02
Procambarus clarkii 0.10 0.01 0.00 0.15 0.03 0.01 0.10 0.02 0.01 na na na
unid. Crustaceans 0.08 0.14 0.05 na na na 0.08 0.06 0.02 0.03 0.02 0.00
Terr. insects 0.43 0.16 0.10 0.45 0.29 0.19 0.43 0.23 0.15 na na na
Aq. insects 0.13 0.00 0.00 0.25 0.06 0.03 0.13 0.03 0.01 0.03 0.02 0.00
Hirudinea 0.03 0.00 0.00 0.05 0.01 0.00 0.03 0.00 0.00 0.00 0.00 0.00
Fish larvae 0.08 0.02 0.01 0.05 0.01 0.00 0.08 0.01 0.00 na na na
unid. fish na na na na na na na na na 0.03 0.02 0.00
Small cyprinids 0.25 0.05 0.02 0.30 0.08 0.04 0.25 0.06 0.03 0.18 0.16 0.07
Large cyprinids 0.03 0.00 0.00 0.05 0.01 0.00 0.03 0.00 0.00 na na na
Ictalurus punctatus na na na na na na na na na 0.08 0.09 0.03
Molluscs 0.05 0.00 0.00 0.10 0.04 0.01 0.05 0.02 0.01 na na na
Small mammals 0.03 0.00 0.00 0.05 0.01 0.00 0.03 0.00 0.00 0.03 0.02 0.00
Small birds 0.08 0.01 0.00 0.10 0.02 0.01 0.08 0.01 0.00 0.03 0.02 0.00
Testudines 0.03 0.00 0.00 0.05 0.01 0.00 0.03 0.00 0.00 na na na

Note. “0.00” indicates that the specific prey items in the fish's diet were considerably low; “na” indicates that respective prey item was not present.

all groups of I. punctatus expressed moderate‐to‐high diet overlap I. punctatus. In contrast, both I. punctatus showed a narrower
index with “S. glanis” (α range: 0.612–0.839; Table 2). C range (Table 3). The applied linear regression model for δ15N
and total length of both species indicated a decreasing trophic
position with increasing size that was significant for I. punctatus
3.2 | Stable isotope analyses
(p < 0.05; Figure 3). Regarding TL and δ13C, statistically signifi‐
With a trophic score of 3.3, S. glanis occupied a slightly higher cant regressions (p < 0.05) as well as negative correlations were
trophic position than immature (3.1) and mature I. punctatus (2.9). found for S. glanis (rs = −0.512; n = 39; p = 0.001) and I. punc‐
Silurus glanis, however, had a lower variability in Layman's met‐ tatus (rs = −0.665; n = 40; p < 0.001). Calculating the overlap
rics and lower N range compared to both immature and mature of SEAc and SEAb revealed different results (Table 3): while

TA B L E 2 Estimated niche (Levins’ Index) and diet overlap based on stomach content data

Ictalurus punctatus Ictalurus punctatus Ictalurus punctatus Silurus glanis

Index (immature) (mature) (Total) (immature)

Pianka's measure of niche overlap

Ictalurus punctatus (immature) x 0.634 x 0.363
Ictalurus punctatus (mature) 0.634 x x 0.591
Ictalurus punctatus (Total) x x x 0.549
Silurus glanis (immature) 0.363 0.591 0.549 x
Diet overlap index a
Ictalurus punctatus (immature) x 0.740 x 0.779
Ictalurus punctatus (mature) 0.740 x x 0.839
Ictalurus punctatus (Total) x x x 0.612
Silurus glanis (immature) 0.779 0.839 0.612 x
HAUBROCK et al. | 7

F I G U R E 3 Linear regression between total length (TL) and δ15N and δ13C for Ictalurus punctatus (a, b) and Silurus glanis (c, d) from the
inner‐Florence section of the Arno River

“immature I. punctatus” and “S. glanis” showed a moderate over‐ while no overlap was estimated between “mature I. punctatus”
lap (SEAc = 0.22/SEAb = 0.28), “mature I. punctatus” overlap with and “S. glanis” or the total population of I. punctatus and “S. glanis.”
“S. glanis” was very low (0.00/0.09). Overall, immature and mature Pairwise overlaps (95%) between groups indicated that “immature
I. punctatus presented a medium overlap (0.27/0.42), considerably I. punctatus” showed the highest probability to occur in the niche
higher than the SEAc overlap of the overall population of I. punc‐ of “mature I. punctatus” (95%) and “S. glanis” (97%), followed by the
tatus with “S. glanis” (0.01/0.19; Table 4; Figure 4). probability of “mature I. punctatus” to fall into the niche of “imma‐
Moreover, the percentual isotopic niche overlap was low be‐ ture I. punctatus” (80%). However, S. glanis showed lower proba‐
tween “immature I. punctatus” and “S. glanis” (14.3%) as well as be‐ bilities to fall in either niche of immature (68%) or mature (33%)
tween “immature I. punctatus” and “mature I. punctatus” (13.4%), I. punctatus.

TA B L E 3 Estimated Layman's metrics and stable isotope results for δ15N and δ13C of all groups of Ictalurus punctatus and immature Silurus
glanis

Layman metrics and stable isotope analysis results

Mean δ15N Mean δ13C

Group (±SD) (±SD) TP NR CR TA CD MNND SDNND SEAc

Ictalurus punctatus 16.2 (±1.0) −27.0 (±0.7) 3.1 4.1 3.0 8.76 0.93 0.45 0.49 2.20
(immature)
Ictalurus punctatus 15.6 (±1.2) −26.2 (±0.5) 2.9 4.1 2.0 5..39 0.91 0.29 0.24 1.84
(mature)
Ictalurus punctatus 15.9 (±1.1) −26.6 (±0.7) 3.0 5.7 3.0 11.55 1.11 0.34 0.35 2.59
(Total)
Silurus glanis 17.1 (±0.6) −25.5 (±0.6) 3.3 2.8 4.1 4.09 0.79 0.19 0.17 0.87
(immature)

Note. CD: mean distance to centroid; CR: δ13C range; MNND: mean nearest neighbour distance; NR: δ15N range; SDNND: standard deviation of the
nearest neighbour distance; SEAc: standard ellipse area; TA: convex hull area.
8 | HAUBROCK et al.

TA B L E 4 Estimated niche overlap for all groups using the maximum likelihood fitted standard ellipse area (SEAc) and the overlap
between the corresponding 95% ellipse area (SEAb)

Ictalurus punctatus
(immature) (SEAc/ Ictalurus punctatus (mature) Ictalurus punctatus (Total) Silurus glanis (immature)
Index SEAb overlap) (SEAc/SEAb overlap) (SEAc/SEAb overlap) (SEAc/SEAb overlap)

SEAc overlap
Ictalurus punctatus x 0.27/0.42 x 0.22/0.28
(immature)
Ictalurus punctatus 0.27/0.42 x x 0.00/0.09
(mature)
Ictalurus punctatus x x x 0.01/0.19
(Total)
Silurus glanis (immature) 0.22/0.28 0.00/0.09 0.19 x

The PERMANOVA main test confirmed significant differences Syväranta et al., 2010). Moreover, S. glanis was identified to be less
among groups, and the post hoc comparisons showed that the three of a generalist than I. punctatus, which showed a more diverse diet
levels are clearly different (Table 5). Considering the results from including insects, plant material, crayfish and fish that was highly
CAP analysis (Figure 5), group differences are well explained by variable among life stages. Additionally, all specimens of I. punctatus
the first axis (CAP1, squared canonical correlation of δ12 = 0.5957; contained prey in their stomach, while almost half of S. glanis’ stom‐
CAP 2 δ22 = 0.004). Both δ13C (rs = −0.926) and δ15N (rs = −0.771) are achs were empty. The observed high number of empty stomachs in
highly inversely correlated to CAP1 and effectively contribute to the immature S. glanis was unexpected as especially smaller fish feed
differentiation of the groups, suggesting in particular that S. glanis is every day (Ricker, 1946). However, this result could be linked to the
clearly different to other two groups for higher values for δ15N and utilised sampling methods, inducing a lot of stress on hooked spec‐
δ13C. Overall, mature I. punctatus have lower values while immature imens and potentially resulting in vomiting of previously ingested
I. punctatus lay in an intermediate position (see Figure 4). prey, rather than on the time of sampling. Moreover, the length‐to‐
weight ratio of I. punctatus was higher than that of S. glanis and the
fullness index estimated for I. punctatus was in all three cases (imma‐
4 | D I S CU S S I O N ture, mature and all specimens) more than twice than that measured
for S. glanis. Concerning I. punctatus, omnivorous feeding with insec‐
Interactions among alien fish species, especially with different life tivorous tendency agrees with its diet and feeding behaviour from
histories, are an understudied topic. More specifically, there is a lack the native area (Busbee, 1968; Franssen & Gido, 2006). The high
of studies concerning trophic relationships among alien top preda‐ occurrence of plants (terrestrial as well as aquatic leaves) within the
tor's native to different geographic areas while co‐occurring in a new diet of sampled S. glanis is highly unusual (Carol, Benejam, Benito, &
region, making this, at least to our knowledge, the first study assess‐ García‐Berthou, 2009). However, alien species (and especially S. gla‐
ing this issue. nis) are known to adapt to new and easily accessible prey (Copp et al.,
In this study, S. glanis was observed to mainly feed on small cypr‐ 2009; Strayer, 2010). Abundant algae or plants could potentially be a
inids and Dikerogammarus villosus, fitting to this species early devel‐ response to either scarce animal prey or an adaptation to abundant
oping piscivorous diet with generalist tendencies (Copp et al., 2009; vegetation as a replacement to avoid intra‐ as well as interspecific

TA B L E 5 PERMANOVA main and post hoc tests results

Unique
Source df SS MS Pseudo‐F P (perm) perms

Gr 2 63.519 31.76 28.53 0.001 999

Res 80 89.057 1.1132
Total 82 152.58

Groups t P (perm) Unique perms

“Immature I. punctatus” “S. glanis” 4.3082 0.001 958

“Mature I. punctatus” “S. glanis” 7.6838 0.001 969
“Immature I. punctatus” “Mature I. punctatus” 2.4983 0.003 747

Note. Design: 1 fixed factor, three levels; resemblance matrix measure of distance: Euclidean distance; Type III (partial) sum of squares, unrestricted
permutation of raw data.
HAUBROCK et al. | 9

F I G U R E 5 Two‐dimensional scatter plot of the first and second

principal coordinate axis (after resemblance matrix with Euclidean
distance, n samples = 83, n variables = 2,) for immature and
mature Ictalurus punctatus and Silurus glanis. Vectors of the linear
correlations (Pearson) between individual variables (i.e., δ15N and
δ13C labelled in the graph as N and C isotopes) are superimposed on
the graph

F I G U R E 4 Standard ellipse area (SEAc; solid grey line); total

the overlap of SEAc, SEAb, nor percentual isotopic niche overlap re‐
convex hull area (TA; dashed black line) as well as 95% ellipse area
(SEAb; solid black line) for Silurus glanis (A), immature (B) and flected the results gained from direct dietary information. Analyses
mature (C) Ictalurus punctatus of diets are very focused and dependable on observable ingested
items that can be affected by activity times or responses of species
competition (Copp et al., 2009; Davidson, Jennions, & Nicotra, 2011; to being caught, while isotope analyses consider previously con‐
Haubrock, Balzani, Johovic, et al., 2018b). Nonetheless, the used sumed and assimilated prey, thus a considerably longer time (Tarkan
fullness index is potentially affected by physiological or morpholog‐ et al., 2018). Additionally, all three groups belong to approximately
ical differences, for example differing weight‐to‐length ratios, but the same estimated trophic position as expected from I. punctatus
since both species belong to the order Siluriformes, these can be and S. glanis (Gido & Franssen, 2007; Syväranta et al., 2010), but
considered of secondary importance. However, these results indi‐ “S. glanis” had a slightly wider δ13C range than the two life stages of
cate an advantageous adaptation to the invaded ecosystem, more I. punctatus. This observation reflects the consumption of a greater
efficient predation by I. punctatus or a comparably higher growth variety of carbon sources. A study on S. glanis in France found that
rate commonly found in majorly produced aquaculture fish species. S. glanis was considerably enriched and variable in δ13C with respect
to other fishes, explainable with the frequent predation on terres‐
trial birds and/or mammals (Syväranta et al., 2010). However, this
4.1 | Diet and niche overlap
study lacked large‐bodied individuals. Nonetheless, it seems rea‐
Schoener's diet overlap between all groups was considerably high sonable to expect similar results, as anglers’ observations confirm
(α > 0.6), but while Pianka's diet‐based niche overlap was similar be‐ the active predation on pigeons by large S. glanis in the Arno River
tween “mature I. punctatus” and “S. glanis,” “Immature I. punctatus” (T. Busatto, pers. comm.; Cucherousset et al., 2012). Similarly, δ15N
and “S. glanis” showed a lower diet‐based niche overlap value (0.36) values tend to increase with the length of catfish (Syväranta et al.,
with respect to Schoener's diet overlap value. This difference can be 2010), reflecting an increased piscivorous or animal diet. While this
due to the “prominence value” in the used formula, weighing the im‐ might be true for S. glanis (Syväranta et al., 2010), our results show
portance of prey items and, thus, being affected by the sample size. generally lower mean δ15N values and lower trophic position of “ma‐
In contrast, SIA and the derived estimated ellipse overlay of SEAc ture I. punctatus” with respect to “immature I. punctatus.” This can
indicated a higher similarity between niches occupied by “immature potentially be explained by the high level of eutrophication (Romero
I. punctatus” and “S. glanis” than between “mature I. punctatus” and et al., 2013) and the natural accumulation of nutrients (i.e., dead
“S. glanis.” matter) in the river bottom (Hansen & Kristensen, 1998; Hendrix
Opposed to the narrow time‐constrained information presented et al., 1986). Immature I. punctatus are benthivorous and often de‐
by stomach content analysis, SIA offers temporally integrated in‐ tritivorous, while mature individuals exert increased offshore feed‐
formation on diet as well as, with SEAc and SEAb, occupied feeding ing (as indicated by the difference in δ13C values; Gido, Franssen, &
niches. Thus, a moderate‐to‐high niche overlap can indicate that the Propst, 2006). Additionally, the lower mean δ15N values could be
compared species consume similar resources, while not stating if linked to a considerable competition for increasingly piscivorous
they can coexist over a longer time period nor whether they feed mature I. punctatus with other species like mature S. glanis (Fry et
on similar prey resources due to limited interference competition. al., 1999). Moreover, Fry et al. (1999) observed that especially δ15N
Hence, neither dietary similarity between groups estimated with values of I. punctatus tend to remain constant with increasing size,
10 | HAUBROCK et al.

while sampling at several occasions resulted in two mature groups this hypothesis is supported by the wider trophic niche occupation
with clearly distinct niches; they linked this observation to varying and a less specialised diet paired with the observed higher full‐
feeding activities of different schools of I. punctatus. Furthermore, a ness index as well as a higher length–weight ratio in I. punctatus.
higher δ15N range was found in I. punctatus, underlying its generalist Additionally, while both species are usually active during the night,
and opportunistic behaviour. Thus, it is possible that the relationship I. punctatus (especially immatures) tend to extend their activity time
of shared niche space continues to weaken as larger age classes of into the day, thus giving it an advantage over S. glanis (Boujard,
S. glanis are included, because prey fish size increases with age and 1995; Boujard & Leatherland, 1992; Noeske‐Hallin, Richard, Nick,
size of S. glanis. This seems to suggest that the difference in niche & Suttle, 1985).
space may be exaggerated further by including larger size classes The observed differences in stomach content analyses and
and that S. glanis prey preference and feeding strategy may change SIA, based on the different information they provide, underline
as they grow from immature to mature. Indeed, S. glanis’ Layman's the opportunistic feeding behaviour of I. punctatus. Moreover,
metrics showed a less variable niche occupation linked to a more this opportunistic feeding behaviour leads to diet and niche over‐
specialised diet and niche placement compared to I. punctatus. The lap. Additionally, the results also highlight the potential for those
15
lower δ N values in “mature I. punctatus” could be due to the sam‐ two species that share a common habitat and overlap in their
ple, other disturbances (lack of prey, competition, etc.) or the op‐ activity time to compete for resources in the case they become
portunistic feeding of individual “immature I. punctatus,” therefore limited. Moreover, this observed niche overlap likely affects the
needing further investigations. more specialised S. glanis and could increase in times when re‐
The results presented by SIA indicate that “mature I. punctatus” sources are increasingly limited. Therefore, the potential of both
and “S. glanis” likely occupy different trophic niches with generally alien catfish species to compete could be among the main reasons
low similarity in their diet. However, both species show some de‐ why a decrease in the abundance of mature S. glanis was observed
gree of diet overlap for common prey items like small cyprinidae and after the introduction of I. punctatus, but more long‐term studies
Pianka's diet‐based measure for niche overlap, an observation likely covering the entire year while also including mature S. glanis will
linked to gape size‐limited predation in catfishes (Johnson, Martinez, be needed.
Hawkins, & Bestgen, 2008). While some analyses indicated low
probability of overlap (e.g., SEAc and SEAb), computing directional
probabilities using the nicheROVER package reported high proba‐ 5 | CO N C LU S I O N
bilities of overlap. This overlap could be related to the opportunistic
nature of very generalist I. punctatus (Busbee, 1968; Rosen et al., The presence of the alien North American catfish I. punctatus was
1995), while “S. glanis” showed a lower diet and diet‐based niche previously believed to have a negative impact on the population of
overlap but a more similar isotopic niche occupation. Considering S. glanis, indicated by the decreasing abundance of S. glanis and an
the estimation of higher probabilities for I. punctatus (immature and increase in catchments of I. punctatus (Arno River: A. Nocita and T.
mature) to occur within the niche of each other as well as within the Busatto pers. obs.; Po River: M. Fiedler, A. Battaglini and P. Haubrock
niche of S. glanis indicated that I. punctatus shows a higher plasticity pers. obs.). However, while results suggest partial niche segregation,
in its niche occupation. they also indicate the possibility for competition that might be due
The high number of empty stomachs in S. glanis and high fre‐ to the potential for immature I. punctatus, which are the dominat‐
quencies of certain prey items (e.g., detritus, plants, algae, small ing life stage (Haubrock, Balzani, Johovic, et al., 2018b; Haubrock et
cyprinids) in the diet of I. punctatus result in an overall similar prey al., 2017; Ligas, 2007), and immature S. glanis, a species that is more
assortment for the diet analyses, while the associated energy in‐ specialised in its niche occupation, to compete. Although both spe‐
take and thus isotope assimilation might differ. However, the es‐ cies are alien, S. glanis is a large body‐sized fish (Copp et al., 2009)
timated overlap and thus potentially arising competitions (aside and cherished among “catch‐and‐release anglers” (Arlinghaus et al.,
from competition for shelter) are only potential explanations for 2007) as a trophy fish. However, with the increasing distribution of
the observed decrease in S. glanis. Furthermore, it is possible that the fast‐growing and comparably more generalist as well as oppor‐
the feeding mechanism of “sucking‐in” of small‐sized S. glanis is tunistic I. punctatus (Olden & Poff, 2005; Tucker & Hargreaves, 2004),
less efficient compared to the more active predation mechanism the population of S. glanis could be negatively affected through com‐
used by I. punctatus. Also, Menzel (1945) observed that especially petition. Further studies should focus on the degree of predation be‐
immature I. punctatus predate eggs and larvae or fish species, as tween big‐sized Silurus glanis (>~70 cm) and the two life stages of the
they commonly share the same habitat, enabling this species to North American catfish under the consideration of differing age and
threaten entire populations in relative short time after its introduc‐ length classes.
tion (Lentsch, Converse, & Thompson, 1996; Marsh & Brooks, 1989;
Nesler, 1995). In the case of the Arno River, I. punctatus is seemingly
AC K N OW L E D G E M E N T S
more efficient in its prey consumption and shows signs of an advan‐
tageous biology, making it better adapted to the non‐native ecosys‐ We want to thank Laura Buonanno (Florida State University, USA)
tem that is slower‐growing S. glanis of similar lengths. Furthermore, and Lauren Tonelli (Invasive Species Centre, CA) for thorough
HAUBROCK et al. | 11

proofreading of the manuscript. Funding was provided by the Boecklen, W. J., Yarnes, C. T., Cook, B. A., & James, A. C. (2011). On the
Aquainvad‐ED project (2020 Marie Sklodowska‐Curie ITN‐2014‐ use of stable isotopes in trophic ecology. Annual Review of Ecology,
Evolution, and Systematics, 42, 411–440. https://doi.org/10.1146/
ETN‐642197). Lastly, we thank the three anonymous reviewers for
annurev-ecolsys-102209-144726
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time in fishes. Environmental Biology of Fishes, 35(2), 109–131. https://
PJH and ET conceived and designed the investigation. MA and PB
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performed field work. MA, PJH and AFI analysed the data. PJH, AFI Boulêtreau, S., & Santoul, F. (2016). The end of the mythical giant catfish.
and PB wrote the paper. Ecosphere, 7(11). https://doi.org/10.1002/ecs2.1606
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& Knecht, R. (2018). Stable carbon, nitrogen and sulphur isotope
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