Transactions of the American Fisheries Society 144:491–501, 2015
Ó American Fisheries Society 2015
ISSN: 0002-8487 print / 1548-8659 online
DOI: 10.1080/00028487.2015.1017656
ARTICLE
Diel Cycle and Effects of Water Flow on Activity and Use
of Depth by Common Carp
Josep Benito, Lluıs Benejam, Lluıs Zamora, and Emili Garcıa-Berthou*
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Institute of Aquatic Ecology, University of Girona, E-17071 Girona, Catalonia, Spain
Abstract
Common Carp Cyprinus carpio is among the most popular and commercially important fishes globally. For this
reason, it has been introduced worldwide and is invasive in many regions, with well-known ecosystems impacts.
Like many other freshwater invaders it is thought not to tolerate strong flows well, but knowledge of the effects of
flow on their activity, habitat use, and diel cycles are limited, despite this being crucial information for management
and control. By means of ultrasonic telemetry we investigated depth use and activity of Common Carp in a small
reservoir with a very low water residence time on the main stem of the Ebro River, the largest river by discharge in
the Iberian Peninsula, over a 19-month period. The activity of carp and their use of depth displayed low seasonality
compared with abiotic factors. However, carp exhibited diel vertical migration patterns, mostly in the warm season,
shifting from deep positions near the reservoir bottom during the night (with decreased activity) to shallow waters
during the day. This pattern included extensive use of hypoxic waters (<1.1 mg/L dissolved oxygen) and occurred
largely at night. Activity and habitat use also varied among individuals and were significantly related to water flow;
carp were less active and used shallower water during increased flows. The individual variability, the behavioral
adaptation to refuge from high floods flows, and the extraordinary resistance to hypoxic waters might help explain
why Common Carp is one of the most successful invasive freshwater fish species.
Common Carp Cyprinus carpio is among the most popular
and commercially important fish species globally. It is currently the third most-cultured fish in the world (FAO 2004)
and is a popular sport fish in many countries (Arlinghaus and
Mehner 2003). Common Carp is also the oldest domesticated
fish, having been cultured many centuries ago, and its ornamental varieties (e.g., koi carp) are the most expensive fish in
the pet trade (Balon 2004). For these reasons, the Common
Carp has been introduced to all continents except Antarctica
and is invasive in many countries (Koehn 2004; GarcıaBerthou et al. 2005), although the species is native only to the
Ponto–Caspian region (part of the Danube River and the
Black, Caspian, and Aral sea basins) and the Far East (Vilizzi
2012). This cyprinid has often been considered an ecological
engineer and has well-known ecological impacts including
causing increases of turbidity and phytoplankton, mobilization
of nutrients, and decreases of macrophytes, macroinvertebrates, and fishes (Matsuzaki et al. 2009; Weber and Brown
2009).
Although many aspects of Common Carp have been well
investigated (e.g., age and growth, aquaculture, nutrition and
feeding, and ecological effects), limited information is available on its population ecology and its behavioral and numerical response to abiotic variables such as water flow,
temperature, or dissolved oxygen concentrations (Weber et al.
2010). For example, the response of carp to water flow appears
complex and poorly understood. Some authors classify the
Common Carp as limnophilic, i.e., preferring standing waters
and not well adapted to tolerate strong flows (Oberdorff et al.
2002), whereas others regard it as eurytopic, i.e., with all life
history stages occurring in both lotic and lentic waters (Aarts
and Nienhuis 2003). Wetlands and inundated floodplain habitats are especially important habitats for carp recruitment,
which peaks in years that have major flood events in spring
and summer (King et al. 2003; Macdonald and Crook 2014).
However, flow regulation provides long-term refuge from
mortality associated with high flows (Driver et al. 2005).
Therefore, restoring or managing flow regimes might reduce
*Corresponding author: [email protected]
Received August 27, 2014; accepted January 24, 2015
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BENITO ET AL.
the abundance and impact of Common Carp and other invasive
species, but further understanding of the response of carp to
water flows is needed (Propst and Gido 2004; Humphries et al.
2008; Taylor et al. 2012). Similarly, although a number of
telemetric studies on Common Carp have been conducted
(e.g., Penne and Pierce 2008; Butler and Wahl 2010; Daniel
et al. 2011; Taylor et al. 2012), as far as we know none of
them seem to have described circadian cycles in natural systems. Diel vertical migration is a common behavioral phenomenon in aquatic organisms and is generally motivated by
bioenergetic efficiency, foraging opportunities, or predator
avoidance (Scheuerell and Schindler 2003). The knowledge of
diel patterns of carp is important to understand their general
ecology and effects on native ecosystems and to improve
aquaculture and management of the species (e.g., eradication,
control, or monitoring programs).
We investigated depth use and activity of Common Carp
using automatic, ultrasonic telemetry in a small, main-stem
reservoir (Flix Reservoir) at the lower reaches of the Ebro
River, which is the river in the Iberian Peninsula with the highest water flow. The small size of the reservoir relative to the
river discharge produces a mean water residence time of 0.29
d and thus mimics conditions of a regulated river. We aimed
to assess the role of water flow on habitat use and activity of
Common Carp using outflow as a proxy for water flow through
the reservoir. We also aimed to test for the existence of diel
cycles in carp activity and their use of depth.
METHODS
Study area.—The Ebro River is the second longest river in
the Iberian Peninsula, being more than 900 km in length, and
has a drainage area of approximately 85,000 km2. It has been
extensively dammed resulting in 187 reservoirs (Batalla and
Vericat 2009), and one of the lowermost impoundments is Flix
Reservoir, built in 1948 for electricity generation (12,600
Mm3/year passes throughout its hydroelectric plant). It is a
small reservoir, with a maximum depth of 12 m and maximum
width of 300 m, and is formed by a low-head dam. The relatively small capacity of Flix Reservoir relative to the size and
discharge of the Ebro River creates conditions similar to those
of a regulated river: the reservoir capacity is 11 hm3 (11 £ 106
m3) and its mean water residence time only 0.29 d (Navarro
et al. 2006), thus suggesting an average outflow of 439 m3/s,
which is very similar to the mean annual discharge (435 m3/s)
at the farthest downstream gauging station on the Ebro River
(Batalla and Vericat 2011). Common reed Phragmites australis and other aquatic vegetation (Ceratophyllum sp., Potamogeton sp., and Myriophyllum sp.) dominate the macrophyte
community and are particularly abundant in summer. The fish
assemblage is dominated by cyprinids not native to the Iberian
Peninsula but widespread and abundant throughout Europe,
such as Common Carp, Roach Rutilus rutilus, Rudd Scardinus
erythrophthalmus, Bleak Alburnus alburnus, and other exotic
species such as European Catfish Silurus glanis and Pumpkinseed Lepomis gibbosus (see Carol et al. 2006 and Benejam
et al. 2010 for further data on the fish assemblage).
Fish tagging.—Twenty Common Carp, 8 males and
12 females (FL range, 497–720 mm; total weight range,
2,500–8,150 g), were captured within the littoral zone of Flix
Reservoir near the dam and tagged during two sampling
periods: 15 carp in May–June 2006 and five in February 2007.
Carp were captured by boat electrofishing (5.0-GPP, SmithRoot, Vancouver, Washington) and transported in a tank containing aerated water to the laboratory (located about 3 km
from the capture site) for surgery. Transmitter implantation
and surgery were conducted mostly following Summerfelt and
Smith (1990). Fish were anesthetized using MS-222 (tricaine
methanesulfonate; 100 mg/L), measured to the nearest millimeter (FL), weighed (g), sexed, and marked with an external
T-bar anchor tag to allow visual identification in case of recapture. The sex of each fish was determined by visual inspection
during the insertion of the transmitter or by the extraction of
milt or eggs. Fish were placed with ventral side up in a
V-shaped surgery table, and the gills were continuously irrigated
with a diluted dose of MS-222 (10 mg/L) and oxygenated water
during surgery. Prior to surgery, scales were removed from the
ventral side of each fish between the pelvic fins and the anus.
An incision of 3 cm was made in the center of the scaleless
region for transmitter insertion. Before suturing, a dose of antibiotic (Baytril, 10 mg/kg) was applied intraperitoneally to minimize infection risk (Bauer 2005). The incision was closed with
simple interrupted sutures using absorbable material (2/0, Ethicon, Somerville, New Jersey); surgery time was 2–3 min. After
surgery, fish were placed in aerated tanks containing water from
the reservoir for a minimum of 12 h or until total recovery and
then released at the capture site.
Telemetry data.—Each carp was implanted with 69-kHz
ultrasonic transmitters (model V13P; VEMCO, Bedford, Nova
Scotia; 44 £ 13 mm, weight D 6 g in water) that were individually coded and calibrated with a pressure sensor to estimate
continuously the swimming depth of the fish. The transmitters
were programmed to emit an identification signal at randomly
spaced periods of 30–60 s and had a minimum battery life
expectancy of 305 d. Tracking began on March 17, 2006 and
ended on October 22, 2007. To monitor movements of the
tagged carp, 10 stationary omnidirectional receivers (VR2
Single Channel Monitoring Receiver, VEMCO) were anchored
in a telemetry array at depths of approximately 1–1.5 m. These
receivers logged the date, time, fish identification, and depth of
any acoustic tag within the detection range (about 400 m
radius). The range of installed receivers covered the last 5 km
near the reservoir dam (see Figure 1). The monitoring receivers
were checked and the data downloaded bimonthly for later analysis. Before the analysis, the raw database was filtered to
remove erroneous data points, e.g., simultaneous localizations
in nonadjacent receivers, large distance movements in very
short periods of time, and data that showed no change in depth
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ACTIVITY AND DEPTH USE BY COMMON CARP
493
FIGURE 1. Study area in Flix Reservoir, Ebro River, Spain, showing location of the 10 stationary telemetry receivers.
or position for long time periods (part of the data for six carp,
likely from fish that had died or had expelled the transmitter).
The two-dimensional position of the fish was estimated as the
position of the receivers that detected them, weighted by the frequency of detection (if detected by more than one receiver). We
averaged two-dimensional hourly positions and depths for each
fish to match limnological data. From the two-dimensional
hourly positions we estimated the relative activity of fish
(minimum distance traveled per hour). Although the telemetry
array may not have been able to detect when an individual
remained near a single receiver, our objective was not to estimate absolute activity or distance traveled but to compare diel
patterns of activity and depth use among hours and seasons.
Activity was not computed for consecutive locations that had
elapsed for more than 24 h for a fish because we assumed these
corresponded to fish that had moved out of range of the
receivers.
Limnological data.—Water quality data were obtained
(unless stated otherwise) from the Catalan Water Agency
(http://aca-web.gencat.cat/aca) at the monitoring station in the
reservoir hydropower plant, where seven limnological variables (water temperature, dissolved oxygen [DO], conductivity,
turbidity, pH, total organic carbon [TOC], and ammonium)
were measured hourly at the surface. To complement this with
deepwater data, we obtained vertical profiles (every 1 m) quarterly, but these were not used for statistical analysis. Water
flow data from the Asc
o gauging station, only 7 km downstream from Flix Reservoir, were provided by the Ebro River
Hydrographic Administration (Confederacion Hidrografica del
Ebro). Water flow measurements in the gauging station were
taken every 15 min and were averaged to hourly mean values.
We consider these outflow measurements to approximate
flows within the reservoir.
Statistical analyses.—The bivariate relationship among the
different limnological variables was analyzed with
Spearman’s correlation coefficients (rs), adjusting the P-values
for multiple inference using Holm’s method, which is generally more powerful than the Bonferroni method because it
sequentially adjusts the P-values (although in our case the conclusions were identical using both methods) (Rice 1989). Principal component analyses (PCAs) were used to understand the
main sources of variation and the relationships among limnological variables. A partial PCA was also performed to
describe the main variation in the data after accounting for seasonality (with month as a categorical factor). To improve linearity and normality, water flow, turbidity, and ammonium
were log10 transformed. To quantify the strength of seasonality
in the limnological and telemetry variables we followed Moineddin et al. (2003) and used a linear regression model with
11 dummy predictors for the months and the coefficient of
determination R2Autoreg (which ranges between 0 and 1) as a
measure of the strength of seasonality (see also Caritat et al.
2006; Carmona-Catot et al. 2014).
We applied additive modeling (AM) with a Gaussian distribution and identity link function (Wood 2004; Zuur et al.
2009) to model the response variables (depth use and activity
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BENITO ET AL.
FIGURE 2. Daily mean water temperature (solid line), dissolved oxygen (dotted line), and water flow (gray area) in Flix Reservoir during the study period.
of carp) as a function of the explanatory variables (hour of the
day, month, and water flow). Because of preliminary analyses
and plots, we aimed at demonstrating the existence of a seasonally dependent diel cycle of carp behavior and understanding the effect of water flow. Following Cronin et al. (2009)
and similar approaches in time series modeling, we compared a series of models decomposing the variation in
short-term (time of day) and long-term (months) variations,
using a smoothing function of time of day and month as a
categorical factor (with dummy variables), respectively. To
account for variability across different individual fish, we
also tested whether an additive mixed model (AMM), with
“fish individual” as a random effect, improved the fit of
the best model. Models were compared using the Akaike
information criterion (AIC), a tool that balances the goodness of fit of a model and its complexity; if competing
models fitted to the same data set are ranked according to
their AIC, the ones having the lowest AIC are the most
likely. Nested models (i.e., two models that contained the
same terms except one or more additional term) were also
compared with likelihood ratio (chi-square) tests.
All analyses were done with R software (R Development
Core Team 2012): AMs were fitted using the “gamm” function
of the “mgcv” package (Wood 2004) and PCAs were obtained
with the package “vegan” (Oksanen et al. 2010).
RESULTS
Seasonal Dynamics of Limnological Variables
Surface water temperatures in Flix Reservoir varied from
a maximum of 24.8 C in August to 8.1 C in February
(Figure 2), whereas DO presented the opposite pattern, in
which DO was at a maximum of about 14.8 mg/L in March
and then fell to levels below 2 mg/L during summer months,
thus showing a strong negative correlation with water temperature (Spearman’s rs D ¡0.68, n D 14,055, Holm’s corrected
P < 0.0001). Water flow in the reservoir exhibited a base flow
of around 180–200 m3/s, which was interrupted by two abrupt
artificial flushing flows of short duration in November 2006
and June 2007 and also by a long period of natural high water
flow between March and May 2007, reaching maxima above
1,800 m3/s in April 2007 (Figure 2). In fact, all limnological
variables were significantly correlated (P < 0.001) and
two axes of a PCA explained 75.5% of the total variation
(Figure 3a). The first PCA axis revealed the seasonal dynamics of the physicochemical properties of the reservoir, corresponding to the winter–summer cycle, described above: water
temperature decreased whereas dissolved oxygen, pH, water
flow, and turbidity increased with the first axis. The second
dimension of the PCA was related to temporal changes from
organic to inorganic pollution of the reservoir water: TOC was
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ACTIVITY AND DEPTH USE BY COMMON CARP
TABLE 1. Strength of seasonality (R2Autoreg, see Methods) for the different
limnological and telemetry variables in Flix Reservoir. Variables are ordered
from higher to lower strength of seasonality. Water flow, turbidity, ammonium, TOC, depth use, and activity were log transformed for the regression
analyses. All regression models were highly significant (P < 0.0001). Mean
and range values of the variables are also shown.
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Variables
Water
temperature
( C)
pH
Dissolved
oxygen
(mg/L)
Conductivity
(mS/cm)
Turbidity
(NTU)
Water Flow
(m3/s)
TOC (mg/L)
Ammonium
(mg/L)
Depth use (m)
Activity (m/h)
R2Autoreg
F11, 14,043
Mean
Range
0.977
5.5 £ 104
14.97
8.1–24.8
0.929
0.902
1.7 £ 104
1.2 £ 104
7.87
7.62
7.4–8.2
0.1–14.8
0.799
5,095.0
1,045
622–1,656
0.711
3,150.0
9.92
1–113
0.686
2,791.0
353.4
100.6–1,880
0.462
0.324
1,100.0
615.0
2.36
0.08
0.2–4.6
0–1.9
0.067
0.054
93.8
74.4
3.16
140.9
0–9.9
0–2,535
71% of the variation), in contrast to the other limnological variables (Table 1), which fluctuated more frequently and peaked
at certain months (e.g., ammonium in February 2007). By contrast, depth use and activity of Common Carp displayed the
lowest seasonality (less than 7% of the variation). A partial
PCA (Figure 3b), removing the seasonal variation (month
effects), also distinguished the two limnological variables
(TOC and ammonium) that had less seasonality and more frequent temporal variation from the rest of the variables that had
stronger seasonality (in the center of the PCA diagram,
Figure 3b).
FIGURE 3. Principal component analyses (PCAs) of the limnological variables in Flix Reservoir: (a) biplot of sample scores and physicochemical loadings of a conventional PCA; (b) partial PCA, accounting for seasonality (using
month as a factor).
positively related to the second axis; however, in contrast, conductivity and ammonium both displayed maxima in November–December and minima in May–July.
Degree of Seasonality
Regression analyses that used months as dummy variables
(Table 1) revealed seasonal variation for the eight limnological variables (P < 0.001). Variables such as water temperature, pH, DO, conductivity, and turbidity showed strong
seasonality (R2Autoreg showed that month explained more than
Modeling the Depth Use and Activity of Common Carp
Common Carp presented a diel cycle in depth use and
activity mostly in the warm season (June to September) and
shifted from deep positions near the reservoir bottom (and
were also less active) during the night to shallow water
(<3 m) during the day (Figures 4, 5). During the rest of the
year, particularly from December to April, observed data and
fitted smooth functions showed almost no diel cycle (Figures 4, 5). Accordingly, the models for both depth use and
activity (D3–D6 and A3–A6 in Table 2) with smooth functions of hour that depended on month [i.e., with a “f(hour £
month)” term] were more likely according to AIC and significantly better according to likelihood ratio tests (Table 2).
These models with smooth functions also had considerably
BENITO ET AL.
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496
FIGURE 4. Average depth use by Common Carp in Flix Reservoir (y-axes) during the day cycle (x-axes) and the 12 months of the year (from January on the
bottom left to December on the top right). A smoothing (LOESS) curve with a span width of 0.5 is shown to aid visual interpretation. [Figure available online
in color.]
higher adjusted R2 values, although the best models only
explained 24% and 13% of the variability in depth use and
activity, respectively. The likelihood ratio tests supported that
adding several terms was justified, and the most complex
models had the lowest AIC and had significantly less deviance
(Table 2). These most complex models (D6 and A6) demonstrated that the diel cycle in depth use and activity depended
on seasonal variation (month) and that there was overall
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ACTIVITY AND DEPTH USE BY COMMON CARP
TABLE 2. Additive models of the effects of month, hour, and water flow on depth use (D models) and activity (A models) of Common Carp in Flix Reservoir.
An “f” indicates a smooth function, the “f(hour £ month)” term estimates a different smooth function of hour for each month (factor), whereas the “C month”
term adds further seasonal variation. A random effect for individual (ID) was included in models D6 and A6. Depth use, activity, and water flow data were log
transformed. The R2adj values indicate the adjusted proportion of the variance explained by the model; LRT D likelihood ratio test statistic, n D 14,055 location
data.
Model
D1
D2
D3
D4
D5
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D6
A1
A2
A3
A4
A5
A6
R2adj
Models compared
LRT
P-value
Depth use
¡296.1
¡300.0
¡1,475.4
¡2,809.9
¡3,089.0
0.07
0.06
0.15
0.23
0.25
D2 versus D3
D3 versus D4
D4 versus D5
1,218.5
1,356.5
283.1
<0.0001
<0.0001
<0.0001
40
¡6,307.8
0.24
D5 versus D6
3,220.8
<0.0001
4
4
26
37
39
Activity
37,680.0
38,235.8
38,102.5
37,405.4
36,663.3
0.05
0.01
0.03
0.08
0.13
A2 versus A3
A3 versus A4
A4 versus A5
177.3
719.0
746.2
<0.0001
<0.0001
<0.0001
40
36,270.4
0.13
A5 versus A6
394.9
<0.0001
Explanatory variables
df
f(month)
f(hour)
f(hour £ month)
f(hour £ month) C month
f(hour £ month) C f(water flow)
C month
f(hour £ month) C f(water flow)
C month C ID
4
4
26
37
39
f(month)
f(hour)
f(hour £ month)
f(hour £ month) C month
f(hour £ month) C f(water flow)
C month
f(hour £ month) C f(water flow)
C month C ID
AIC
seasonal variation, dependence on water flow, and variability
among individuals (“ID” term in Table 2).
Water Flow Effect on Common Carp Behavior
The best models to explain variation in depth use and activity of Common Carp also included flow as a predictor
(Table 2) and the smooth function illustrates the relationship
(Figure 6). The observed data and the estimated smooth function suggested that carp were less active and used shallower
water during high water flows (outflows > 1,000 m3/s). Noteworthy is that no carp were detected at depths greater than
3.5 m during the highest outflows.
DISCUSSION
Diel Rhythms in Common Carp
We observed diel rhythms in depth use and activity of
Common Carp, mostly during the summer months (June to
September), which revealed an occupancy of shallow waters
during the day and a shift to use deeper locations (with
decreased activity) near the bottom from dusk to dawn. In the
cold season, carp maintained a constant activity during the 24h cycle and the diel rhythm in depth use was not evident,
revealing seasonal variability in carp behavior. Previous
telemetry studies that generally described seasonality in habitat use of Common Carp have indicated that carp occupy more
littoral habitats during spring and summer and move to relatively deeper water to overwinter (Johnsen and Hasler 1977;
Otis and Weber 1982; Penne and Pierce 2008; Jones and Stuart
2009). To our knowledge, diel rhythms in feral Common Carp
populations have rarely been reported. Carlander and Cleary
(1949), in a study in which gill nets were lifted at 1–3-h intervals, reported migrations of Common Carp from deep water at
night to shallow water during the day. Bajer et al. (2010),
using a mesh bag experiment, showed diel patterns in food
consumption of carp in a lake. Research using aquaculture
tanks has also found clear differences between day and night
activity patterns in juvenile Common Carp; they spend more
time swimming in the water column at night than during the
day (Rahman and Meyer 2009).
Variation in fish behavior has been often related to spawning
activity, and the reproductive stage of each species may also
influence the diel horizontal and vertical migrations of fishes
(Lucas and Baras 2001). The spawning period of Common
Carp in southern France and the Iberian Peninsula begins in
April and lasts until late August (Crivelli 1981; FernandezDelgado 1990). Benejam et al. (2010) observed a decrease in
the size-adjusted means of gonadal weight of Common Carp
from May to August, for the same study site and year as this
study, confirming the same spawning season of carp in Flix
Reservoir. In fact, carp were observed displaying aggregation
behavior prior to spawning in the shallow vegetated areas of
the reservoir shoreline in summer (J. Benito, personal observation). Since carp spawning occurs mainly during daylight hours
BENITO ET AL.
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498
FIGURE 5. Average activity of Common Carp (log transformed) in Flix Reservoir (y-axes) during the diel cycle (x-axes) and the 12 months of the year
(from January on the bottom left to December on the top right). A smoothing (LOESS) curve with a span width of 0.5 is shown to aid visual interpretation.
[Figure available online in color.]
(Swee and McCrimmon 1966; Crivelli 1981) in shallow areas
with abundant fixed macrophytic vegetation (Stuart and Jones
2006; Bajer and Sorensen 2010), the continued use of shallow
waters (<3 m) during the day from June to September (Figure 4)
might be due, at least in part, to their reproductive behavior.
Moreover, the increase in the activity observed at dawn may be
linked to the swimming displacements from the deeper areas of
the reservoir at night to the shallow spawning habitats.
Interestingly, Common Carp used the hypoxic waters
extensively, largely at night. The DO concentrations of water
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ACTIVITY AND DEPTH USE BY COMMON CARP
499
the water column (e.g., Baldwin et al. 2002; Mitamura et al.
2008). Common Carp, however, thrive in eutrophic waters
(Carol et al. 2006), tolerate DO concentrations less than 2 mg/
L (Panek 1987), and can survive DO levels as low as 0.5 mg/L
for several days (Zhou et al. 2000). Common Carp have the
ability to withstand poor water quality; however, we hypothesize that the risks of their extensive use of hypoxic bottom of
the reservoir has two benefits. The hypoxic hypolimnion might
be rich in food resources less exploited by other fish species in
the reservoir and constitute a predation refuge for zooplankton
(De Meester and Vyverman 1997; Vanderploeg et al. 2009).
Previous studies have reported that Central Mudminnows
Umbra limi regularly enter a suboxic hypolimnion during short
periods of time to hunt for zooplankton prey (Rahel and Nutzman 1994). Garcıa-Berthou (2001) also described a depthdependent variation in Common Carp diet in which they had a
preference for profundal macrobenthos of the most hypoxic
basin of a lake, which confirms the capability of this species to
forage in hypoxic waters. Secondly, remaining on the reservoir
bottom at night might be a predation avoidance response of
carp due to the abundance of European Catfish in Flix Reservoir, which has can prey on large carp and deplete local fish
populations (Carol et al. 2009). Telemetry of catfish in the reservoir (Carol et al. 2007) showed marked nocturnal activity of
this large predator and inactivity during daytime. Since European Catfish are sensitive to low oxygen levels (Copp et al.
2009; Danek et al. 2014) the use of deep positions near the
bottom at night by carp might reduce predation risk. Juvenile
Sockeye Salmon Oncorhychus nerka can perform diel vertical
migrations in North American lakes to balance potential feeding rates and predation risk (Clark and Levy 1988; Scheuerell
and Schindler 2003). Bajer and Sorensen (2010) recently
showed that Common Carp move into winterkill-prone shallow regions of lakes for spawning, presumably because they
are relatively free of predators. Further studies are, however,
needed to clarify the frequency and reasons for the nocturnal
use of hypoxic bottom layers by carp.
FIGURE 6. Relationship of (a) activity and (b) depth use of Common Carp
with water flow in the reservoir. The fitted smoothing curves obtained by additive modeling (Gaussian errors) are also shown. [Figure available online
in color.]
in Flix Reservoir were quite low, mostly in the summer
months, with values between 2 and 4 mg/L at surface (Figure 2) and reaching levels less than 1.1 mg/L at the bottom.
These low DO levels are due to water inputs from the hypolimnion of the neighboring Riba–Roja Reservoir, located less
than 12 km from the Flix Reservoir dam (Figure 1), which
cause the deep circulation of oxygen-poor water (Navarro
et al. 2006). The observed behavior of carp inhabiting deep
hypoxic bottoms at night in the warm season contrasts with
previous telemetry studies for other freshwater fish species,
which have reported the inverse diel pattern with vertical
migrations in order to avoid increased hypoxia or anoxia in
Effect of Floods on Common Carp Behavior
The outflow from Flix Reservoir was quite stable at 180–
200 m3/s during the study. This low range of flow variability
in a site with such a large drainage area is largely determined
by the extensive occurrence of many large dams upstream,
which produce substantial reductions in flood frequency and
magnitude (Batalla et al. 2004). Nevertheless, during our
study, a period of high natural floods occurred in the spring of
2007, reaching outflow levels above 1,800 m3/s (up to
10 times the base flow). This scenario allowed us to analyze
the response of Common Carp activity and depth use in these
infrequent environmental conditions. Our results agree with
the preference and positive selection by carp for low current
velocities (Crook et al. 2001) and showed that at higher river
discharges, carp reduced their activity considerably and
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500
BENITO ET AL.
avoided waters deeper than 3 m during maximum floods. This
behavior is likely due to the search for refuge positions in the
shallow, littoral, vegetated habitats and avoiding the higher
water velocities in the main channel; it also may involve a little longitudinal or lateral movement depending on habitat
availability. During periods of high water discharge, Brown
et al. (2001) observed a similar strategy of Common Carp to
take refuge along the low velocity stream margins until floods
resumed. Jones and Stuart (2009) also reported that during rising river discharges carp moved laterally from the river channel onto the floodplain. Although in that case, those
investigators attributed that behavior to the exploration of new
available habitats and also to spawning. This behavior of
decreased activity and use of shallow habitats during high discharge events has been observed in a number of fish species,
such as other cyprinids like Barbel Barbus barbus, European
Chub Squalius cephalus, or Eurasian Dace Leuciscus leucisus,
among others (e.g., Clough and Beaumont 1998; Lucas and
Baras 2001; Slavık et al. 2009) that inhabit large regulated rivers. Overall, our results suggest that this behavioral adaptation
to refuge from extreme flows and the extraordinary resistance
to hypoxic waters helps explain why Common Carp is one of
the most successful invasive freshwater fish species.
ACKNOWLEDGMENTS
This study was financially supported by the Spanish Ministry of the Environment and the Catalan Water Agency (MOBITROF project to J. O. Grimalt), the Spanish Ministry of
Economy and Competitiveness (projects CGL2009-12877C02-01 and CGL2013-43822-R), the University of Girona
(project SING12/09), and the Generalitat of Catalonia (ref.
2014 SGR 484). L.B. held a doctoral fellowship from the University of Girona. We are grateful to everybody who helped in
the field, the Natural Reserve of Sebes for providing local
facilities, and K. D. Fausch, C. A. Murphy, and two anonymous reviewers for helpful comments on the manuscript.
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