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RESEARCH ARTICLE
Adult Atlantic salmon have a new freshwater
predator
Ste
´phanie Boulêtreau
1
, Adeline Gaillagot
1
, Laurent Carry
2
, Ste
´phane Te
´tard
3
, Eric De
Oliveira
3
, Fre
´de
´ric Santoul
1
*
1EcoLab, Universite
´de Toulouse, CNRS, Toulouse, France, 2MIGADO, Saint-Orens-de-Gameville,
France, 3LNHE, EDF—R&D, Chatou, France
*frederic.santoul@univ-tlse3.fr
Abstract
The Atlantic salmon (Salmo salar) is one of the world’s most emblematic freshwater fish.
Despite conservation and rehabilitation plans, populations of this species are dramatically
declining due to human impacts such as habitat fragmentation, overfishing and water pollu-
tion. Owing to their large body size, anadromous adults were historically invulnerable to fish
predation during their spawning period migration. This invulnerability has disappeared in
Western Europe with the introduction of a new freshwater predator, the European catfish
(Silurus glanis). Here we report how adults of Atlantic salmon are predated in the fishway of
a large river of SW France, where the delayed and narrow passage created by the structure
increases the probability of predator-prey encounter. We assessed predation risk by moni-
toring salmon and catfish in one fishway of the River Garonne, using video fish-counting
from 1993 to 2016. We analysed the predation strategy of catfish using observations made
with acoustic camera and RFID telemetry in 2016. Our results demonstrate a high predation
rate (35%—14/39 ind.) on salmon inside the fishway during the 2016 spawning period
migration. Our results suggest that a few specialized catfish individuals adapted their hunt-
ing behaviour to such prey, including their presence synchronized with that of salmon (i.e,
more occurrences by the end of the day). Such results suggest that the spread of European
catfish will potentially impact migration of anadromous species through anthropized
systems.
Introduction
The main causes of global Salmonid decline are well identified. Habitat fragmentation, habitat
alteration, acidification and overexploitation seriously threaten populations of species such as
the Atlantic salmon [1,2]. Furthermore, climate change, introduced fish species or predation
are now considered as potential threats, but there is limited information on how these factors
and their interactions will affect salmonid populations [2]. Introductions of large-bodied pred-
ator fish that forage at the apex of food webs are known to impact native fish populations and
modify prey assemblages as well as food web structure [3,4]. A well-known example is given by
the introduction of the Nile perch in African lakes that negatively impacted cichlid populations
and the food web through top-down effects [5].
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OPEN ACCESS
Citation: Boulêtreau S, Gaillagot A, Carry L, Te
´tard
S, De Oliveira E, Santoul F (2018) Adult Atlantic
salmon have a new freshwater predator. PLoS ONE
13(4): e0196046. https://doi.org/10.1371/journal.
pone.0196046
Editor: Dennis M. Higgs, University of Windsor,
CANADA
Received: November 30, 2017
Accepted: April 5, 2018
Published: April 19, 2018
Copyright: ©2018 Boulêtreau et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: This study was funded by the Adour-
Garonne water agency (AEAG) and Electricity of
France (EDF). The funder "EDF" provided support in
the form of salaries for authors [EDO and ST], but
did not have any additional role in the study design,
data collection and analysis, decision to publish, or
preparation of the manuscript. The specific roles of
these authors are articulated in the ‘author
contributions’ section.
Largely introduced in the 1970s’ the European catfish Silurus glanis is now widespread in
western and southern European freshwaters where it has established self-sustaining popula-
tions in most large rivers [6]. Large individuals can measure over 2.7 m total length and weigh
130 kg [7]. With its large gape size, the European catfish is a potential predator to many if not
all native fishes, including anadromous species so that native species would no longer benefit
from the size-refuge that protected them against native top-predators (e.g., pike; [8]).
In this context, human activities that affect fish movement may increase the exposure of
Atlantic salmon to predators. Artificial structures (e.g., dams and weirs), even where equipped
with fish passage devices, are suspected to reduced survival of prey fish species by increasing
prey residence time and predator density [9] and therefore, encounter rates. Increased food
resource availability, smaller passage width and and simplified structure inside fish ladders
may trigger the emergence of trophic specialization among consumers [9,10]. Moreover, intra-
specific variation in trophic specialization might explain the ability of introduced species to
establish populations. In European catfish populations, some individuals have been observed
to adapt their behaviour to forage on novel prey, leading to behavioural and trophic specializa-
tion [11].
The Atlantic salmon, considered as an endangered species in Western Europe, was elimi-
nated in the mid 1900s from many large, heavily anthropized and fragmented rivers [12,13],
such as the River Garonne (Southwest France). In the 1980s, a sustainable reintroduction plan
and restoration programs to facilitate passage over obstacles were begun in the Garonne basin.
The lower-most obstacle on the River Garonne (Golfech power plant) was therefore equipped
in 1987 with a fish lift as fishway. The Atlantic salmon population was monitored since 1993 in
the fishway where adult returns are counted with video [14]. However, potential predation by
the European catfish inside the fishway is now raising concerns that introduced predators may
challenge conservation efforts. The aim of this study is to assess the risk for the Atlantic salmon
to be predated by the European catfish inside an anthropized system. To this end, we hypothe-
sized that some specialized catfish individuals could adapt their foraging behaviour to this
restricted and anthropized spatial environment leading to Atlantic salmon predation in the
fishway.
Materials and methods
Study area
Located in southwestern France, the Garonne River runs over 580 km from its source in the
Pyrenees to the Atlantic Ocean. The Golfech–Malause hydroelectric complex was built in 1971
on the Garonne River (southwestern France) about 270 km from the river mouth (0˚
55’22.3”E; 44˚06’37.6”N), downstream from the confluence with the Tarn River (Fig 1; see [15]
for more details). This diversion-type hydropower facility is the first barrier for upstream
migration of anadromous species in the Garonne River. The Golfech power plant structure
was equipped in 1987 with a fish lift on the right bank of the tailrace. Fish are attracted into a
9-m long, 2.5-m wide and 1.5–4.5-m deep holding pool. At regular intervals (depending on
fish passage frequency), fish are trapped and concentrated into a 3.3-m
3
tank. This tank is
raised (fish lift) and emptied upstream of the plant into a 250-m long, 2-m wide and 2.5-m
deep transfer canal (Fig 1). Fish pass into this transfer canal before joining the headrace canal.
Fish counting
A permanent video fish-counting station was installed in the fishway to monitor the number
and timing of fish passage since 1993 (Fig 1). Migado, the association in charge of analysing
these records, provided the daily numbers of net passages of European catfish and Atlantic
A new predator for the Atlantic salmon
PLOS ONE | https://doi.org/10.1371/journal.pone.0196046 April 19, 2018 2 / 12
Competing interests: The authors have declared
that no competing interests exist. This does not
alter our adherence to PLOS ONE policies on
sharing data and materials.
salmon in front of the fish-counting station (i.e., for each fish species and each day, the number
of upstream movements minus the number of downstream movements) between January 1
st
1993 and December 31
st
2016. The annual (or monthly) number of fish passing through the
fishway was obtained by summing the daily net passages of the year (or month). We also
obtained the number of catfish and salmon upstream and downstream passages for each hour
from 2004 to 2016. We used these long-term data to describe the annual and seasonal timing
of salmon and catfish and their behaviour in the fishway.
A temporary acoustic camera BlueView (Teledyne Blueview M900-2250 Dual Frequency
series) was installed from the 4
th
of April to the 26
th
of May 2016 in the headrace canal at the
upstream exit of the transfer canal in order to examine catfish and salmon behaviour in this
unknown place where waters are deep and cloudy (Fig 1). The acoustic camera was placed at
the exit of the fishway in order to the camera view range covered the area of the canal outlet
(2.25 m wide per 1 m high) and therefore ensure that no fish could be missed. Moreover, spe-
cific morphological characteristics of Atlantic salmon and European catfish (body size and
form, catfish head shape and salmon dorsal fin) can allow easily and undoubtedly distinguish-
ing these two species from others. Salmon were counted at this place to be compared with
salmon counted at the video counting station during the same period in order to estimate
Fig 1. Location and overview of the Golfech fishway on the River Garonne.
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catfish predation on salmon inside the fishway. During this period, the transfer canal was emp-
tied twice a week to ensure that no salmon remained in the fishway.
European catfish tagging
A total of 35 European catfish were captured in the transfer canal in April 2015 (n = 10) and in
April 2016 (n = 25) to be tagged in order to monitor their presence inside the fishway. Catfish
were anaesthetised using a benzocaine solution at 10% (0.7 ml/l), measured and tagged with a
32 mm PIT tag (RI-TRP-WR2B, half duplex, 134 kHz, diameter 3.85 mm and weight 0.8 g in
air; Texas Instruments). The procedure took less than 5 minutes. Fish were transferred to a
tank of clean water to recover from anaesthesia and released just outside the upstream exit of
the transfer canal. Fish tagging was ensured by Migado, the association in charge of monitor-
ing fish at the fishway, in accordance with national legislation under the authorisation ‘Arrête
´
Pre
´fectoral 2015–230’. Three antennae were fixed inside the transfer canal to detect tagged fish
and to analyse the periods of catfish presence inside the fishway.
Results
Salmon and catfish numbers and timing
The annual number of returning adult Atlantic salmon averaged 166 (±131 SD), ranging from
a minimum of 45 individuals in 2005 to a maximum of 599 individuals in 2001 (Fig 2A). This
number of Atlantic salmon exhibited a slight peak between 1999 and 2002. First European cat-
fish passages at the video fish-counting station occurred in 1995, with three individuals. This
number progressively increased until 2004 to reach an average of 590 (±232 SD) individuals
per year during subsequent years. Years 2007 and 2012 exhibited the highest annual numbers
of European catfish with 1134 and 956 individuals respectively (Fig 2A).
Between 1995 and 2016, nearly 95% of the European catfish passed between April and July
with proportions reaching 35 and 31% in May and June (Fig 2B). The migration period of
salmon is only slightly earlier with 78% of salmon passing between March and July. A small
peak of salmon passages was first observed in autumn, but since 2003, this peak has disap-
peared and 96% of the salmon were observed to pass between March and July (data not
shown).
From 2004 to 2008, the frequency downstream passages by catfish was low. After 2009 it
strongly increased, reaching in 2015 a frequency nearly six times higher than in previous year
(Fig 3B). This suggests that catfish spent more and more time inside the fishway, going back
and forth in front of the video fish-counting station, leaving and entering back the fishway and
not only directly pass towards upstream. Similarly, the number of Atlantic salmon coming
back in front of the video station was particularly high in 2016 as compared with previous
years (Fig 3A).
Salmon preferentially came in front of the video fish-counting station during daytime
between 8am and 9pm (median value around 1pm; Fig 4A). By contrast, catfish preferentially
passed nightly between 11pm and 9am (median value at 4am). In 2014, 2015 and 2016, a
higher proportion of European catfish were observed at the end of the day, between 5pm and
10pm (Fig 4B).
European catfish visiting/occupancy in the fishway
Detections occurred from April 20
th
to July 14
th
, 2015 and from April 29
th
to August 16
th
,
2016. Among the 35 catfish tagged and monitored, 30 (86%) were detected at least once by one
of the antennae inside the transfer canal (Fig 5A). 23 catfish (66%) have performed only one
A new predator for the Atlantic salmon
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annual incursion inside the transfer canal staying inside from less than 1 minute to 17.6 hours
(Fig 5A). The other seven individuals (20%) have performed more than one incursion. The
number of incursions they performed, the time of their incursions and the cumulative time
they spent inside during the year of their release differed between individuals, with annual
incursion number ranging from one to 21 (Fig 5B), annual number of detections ranging from
Fig 2. Timings of passages of Atlantic salmon (dark grey) and European catfish (light grey) at the fishway in the River Garonne: (a) annual net number of fish
counted at the video fish-counting station since its installation in 1993; (b) month distribution (in %) of over the period 1993–2016.
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Fig 3. Number of Atlantic salmon (a) and European catfish (b) coming back in front of the video fish-counting station (in white) as compared with the annual net
number of passages of Atlantic salmon (dark grey) and European catfish (light grey).
https://doi.org/10.1371/journal.pone.0196046.g003
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179 to 2012 (Fig 5C) and cumulative annual time inside ranging from 10 hours to 10 days (Fig
5D). These seven most active catfish individuals inside the fishway were detected at night,
mainly at the beginning of the night from 9pm to 11pm (Fig 5E).
European catfish predation on salmon
Salmon migration was observed at the video fish-counting station. Without catfish inside the
fishway, direct upstream migration behaviour, with salmon swimming at the bottom of the
fishway, was observed. With catfish inside, the migration behaviour was disrupted with many
salmon going back and forth, swimming at the surface, staying for a long time inside before
exiting, and sometimes being predated. See “S1 Movie” for direct predation of an adult salmon
(80 cm total length) by a large European catfish (160 cm total length).
Acoustic camera records performed from April 4
th
to May 26
th
2016 (51 days) at the exit of
the fishway showed that there were often between one and six European catfish individuals
waiting at the exit of the transfer canal. During this period, a total of 187 European catfish
were observed exiting from the transfer canal and 86 coming back into the fishway.
During this same observation period (51 days), over the 39 salmon counted at the video
fish-counting station, only 25 were observed at the exit of fishway by the acoustic camera. The
remaining 14 salmon—unobserved with the acoustic camera (35%)—were predated by Euro-
pean catfish inside the transfer canal between the video station and the exit. None of them was
detected in front of the video fish-counting nor at the exit of the fishway from 9pm to 2am.
Among the 25 salmon that managed to exit, 12 (48%) spent less than 30 minutes, seven (28%)
spent between 30 minutes and 1 hour, five (20%) spent between 1 h and 6 h and one (4%)
spent near 14 h inside the transfer canal before exiting it. 18 of them (72%) were attacked by
European catfish when exiting but none of the predation acts was successful. Over the 67 other
individual fish of undetermined species that were observed exiting the transfer canal, 31 (46%)
were attacked. Image resolution did not allow us to determine whether attacks on other small-
est fish preys were successful or not.
Discussion
Most Atlantic salmon populations are declining, conversely European catfish populations are
increasing in western and southern European freshwaters. Despite ambitious rehabilitation
plans, the Atlantic salmon population of the Garonne River remains very low especially since
2003. The European catfish was observed in the fishway of Golfech since 1997 with increasing
passage numbers followed by an apparent stabilization since 2008.
The period of upstream migration of Atlantic salmon that mainly occurs from April to July
coincides with the period of European catfish passages at the dam. The European catfish is not
a migratory species but, as many other freshwater fish, upstream movements can be observed
before the spawning period [16]. The seasonality of this behaviour, from April to July, is linked
to warmer water temperature [17,18] and/or when more prey is available during the spring
migration [19]. Indeed, the present observations proved that returning adults of Atlantic
salmon are a prey for the European catfish in the River Garonne. In a preliminary study, using
DNA metabarcoding, Guillerault et al [20] have found DNA of Atlantic salmon in catfish fae-
ces in the River Garonne, but without certainty that prey were healthy and not already weak or
Fig 4. Hourly timings of Atlantic salmon (a) and European catfish (b) comings in front the video fish-counting
station between 2004 and 2016.
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A new predator for the Atlantic salmon
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dead. Here, we observed predation acts and we report that 35% of the 40 migrating salmon
observed at the dam here were consumed inside the fishway.
Predation inside the fishway is high, despite the observed mismatch between daytime activi-
ties of both species (diurnal for Atlantic salmon, nocturnal for European catfish) that should
limit the predation risk. Individual tagging suggested that predation was due to catfish individ-
uals that were staying at the exit, experiencing upstream and downstream movements inside
the fishway and/or anticipating comings inside the fishway at the end of the day to increase the
probability to encounter salmon inside. Slavı
´k et al [18] demonstrated that the European cat-
fish in a river is not strictly nocturnal in activity. The same authors demonstrated, from elec-
tromyogram biotelemetry records, that there is considerable individual variability in diel
activity depending on different individual behaviour and ability to use energy reserves [21].
Furthermore, the European catfish is known to display individual trophic specialisation
through foraging on terrestrial birds by intentional beaching [11]. Diet plasticity is a common
phenomenon in top predators with high-energy requirements and the ability to learn to utilize
new resources. As a long lifespan species with novel behaviours—massive aggregations [22],
beaching [11], predation in fishway (this study)—European catfish is distinct from many other
freshwater fish, and exhibits adaptations to its environment that are likely to contribute to its
invasive success.
Here, the anthropization of the river provides a local opportunity for European catfish to
exploit migrating Atlantic salmon. The continuous occurrence of several catfish individuals at
the exit of the fishway suggests that predators occupy this strategic location to capture other
fish prey. Indeed, unsuccessful predation acts on Atlantic salmon observed by acoustic camera
at the exit of the fishway suggest that Atlantic salmon escape more easily than other fish from
catfish predation thanks to its high-speed swimming performance. Further investigation
would be necessary to demonstrate selectivity or opportunism to consume prey. Our prelimi-
nary results show that 46% (31/67) of undetermined freshwater fish were attacked compare to
72% (18/25) for salmon. Large adult salmon (mean 80 cm total length), compare to generally
smaller freshwater fish prey, could be preferentially selected by large catfish.
Multiple stressors are known to interact synergistically to amplify the individual effects of
global change drivers on species and ecosystems [23,24,25]. The results suggest that the pres-
ence of dams (and fishways) and a new predator have additional impacts on the precarious
Atlantic salmon population of the River Garonne. In complex narrow fishways, introduced
European catfish can ambush and predate their prey, thus amplifying the ecological conse-
quences of an anthropogenic perturbation [9].
Due to human introduction coupled with future climate change, the range extension of the
European catfish, especially in the north of Western Europe, will continue. In this context,
even if no strong impact may appear for freshwater fish [6], the potential future risks for large
anadromous species should be taken into account. Indeed large anadromous fish species may
be more sensitive to catfish than other freshwater fish that do not need to use the fishway. Con-
versely to other freshwater species, large anadromous species may have not developed defence
strategies against predator before catfish establishment. Moreover, by predating reproductive
adults, the impact of catfish is certainly stronger on anadromous life cycle. The potential novel
predation pressure on these non co-evolved prey, coupled with increased human activity (e.g.
Fig 5. European catfish visiting in the fishway: (a) proportion of tagged individuals detected in the fishway and timings of the presence of the most active individuals
(n = 7) in terms of (b) number of incursions, (c) number of detections by one of the antennae, (d) cumulative time spent and (e) hourly period of their presence in the
fishway.
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dam, fisheries), is concerning, especially in the case of declining populations of anadromous
species.
Supporting information
S1 Movie. Adult Atlantic salmon have a new freshwater predator.
(MP4)
Acknowledgments
The authors wish to thank Se
´bastien Delmotte for statistical advice in the first part of this
study and Andrew MacDonald for English revisions.
Author Contributions
Conceptualization: Ste
´phanie Boulêtreau, Laurent Carry, Ste
´phane Te
´tard, Eric De Oliveira,
Fre
´de
´ric Santoul.
Data curation: Ste
´phanie Boulêtreau, Laurent Carry, Eric De Oliveira, Fre
´de
´ric Santoul.
Formal analysis: Adeline Gaillagot, Eric De Oliveira, Fre
´de
´ric Santoul.
Funding acquisition: Ste
´phane Te
´tard, Eric De Oliveira, Fre
´de
´ric Santoul.
Investigation: Ste
´phanie Boulêtreau, Adeline Gaillagot, Laurent Carry, Fre
´de
´ric Santoul.
Methodology: Ste
´phanie Boulêtreau, Adeline Gaillagot, Laurent Carry, Fre
´de
´ric Santoul.
Project administration: Fre
´de
´ric Santoul.
Supervision: Ste
´phanie Boulêtreau, Fre
´de
´ric Santoul.
Validation: Ste
´phanie Boulêtreau, Fre
´de
´ric Santoul.
Writing – original draft: Ste
´phanie Boulêtreau, Ste
´phane Te
´tard, Eric De Oliveira, Fre
´de
´ric
Santoul.
Writing – review & editing: Ste
´phanie Boulêtreau, Ste
´phane Te
´tard, Eric De Oliveira, Fre
´de
´ric
Santoul.
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A new predator for the Atlantic salmon
PLOS ONE | https://doi.org/10.1371/journal.pone.0196046 April 19, 2018 12 / 12
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