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ORIGINAL ARTICLE
Size-specific effects of bighead carp predation across the
zooplankton size spectra
Scott F. Collins
|
David H. Wahl
Kaskaskia Biological Station, Illinois Natural
History Survey, Sullivan, IL, USA
Correspondence
Scott F. Collins, Kaskaskia Biological Station,
Illinois Natural History Survey, Sullivan IL,
USA.
Email: collscot@illinois.edu
Funding information
Illinois Natural History Survey; Great Lakes
Research Initiative; Illinois Department of
Natural Resources, Grant/Award Number:
CAFWS-93
Abstract
1. Bigheaded carp (Cyprinidae: Hypophthalmichthys spp.) were brought to North
America for aquaculture and eventually escaped captivity. Since their liberation,
they have dispersed northward through the Mississippi River Basin and its tribu-
taries. Although bigheaded carp are omnivorous filter-feeding planktivores, their
predatory effects on zooplankton are of principal concern because many native
fishes feed on planktonic invertebrates during some phase of their life history.
The aim of our study was to quantify the magnitude of effect of bighead carp
(Hypophthalmichthys nobilis) on zooplankton body size and daily secondary pro-
duction across a range of body lengths.
2. We conducted an experiment where we compared responses of zooplankton in
the presence of a native fish assemblage (control, n= 5 ponds) and a native fish
assemblage plus bighead carp (invaded, n= 5 ponds). The experiment lasted
3 months (June–September, 2014) and was conducted in clay-lined ponds
(0.04 ha. wetted area; 1.5–1.75 m water depths). We quantified the predatory
effects of bighead carp on overall changes to the size structure of zooplankton
assemblages, body lengths of zooplankton taxa and taxa-specific changes to
standing crop biomass and daily secondary production.
3. The size structure of zooplankton assemblage shifted towards smaller invertebrates
in the presence of bighead carp. Bighead carp reduced the individual body sizes of
Diaphanosoma (Sididae) (19%) and Daphnia (Daphniidae) (9%) after 3 months.
Moreover, the standing crop biomass (92% to 98%) and daily production (65%
to 74%) of Diaphanosoma,Daphnia and Calanoida were reduced in the presence of
bighead carp. Bighead carp reduced immature copepod nauplii by 75% when com-
pared to controls and may have affected recruitment to the adult stage.
4. Our experiment indicated that the magnitude of predation by bighead carp
increased with zooplankton body size, although rotifers and nauplii were excep-
tions to this pattern. The combined effects of reduced body sizes of some taxa
and direct predation on immature and adult life stages of larger taxa suggest that
bighead carp may be affecting zooplankton demographics through additional
mechanisms such as reduced egg production, mate limitation, and recruitment.
KEYWORDS
Asian carp, Hypophthalmichthys, invasive species, planktivory, size-specific predation
Accepted: 20 March 2018
DOI: 10.1111/fwb.13109
Freshwater Biology. 2018;1–9. wileyonlinelibrary.com/journal/fwb ©2018 John Wiley & Sons Ltd
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1
1
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INTRODUCTION
Human activities have greatly expedited the rate of species introduc-
tions across the globe (Ricciardi, Steiner, Mack, & Simberloff, 2000;
Ruiz & Carlton, 2003; Vitousek, Mooney, Lubchenco, & Melillo,
1997). Although many invasions are rather benign in terms of overall
impacts to the environment (Williamson & Fitter, 1996), others
involve species whose presence is characterised by disproportionate
alterations to food-web structure and function (Mack et al., 2000;
Moyle & Light, 1996; Vitousek et al., 1997). Bigheaded carp (Cyprini-
dae: Hypophthalmichthys spp.) are known for their ability to effi-
ciently control plankton (Chapman & Hoff, 2011; Kolar et al., 2007;
Smith, 1985). Consequently, these planktivorous cyprinids have been
transported across the globe for aquaculture applications. As is often
the case, those bigheaded carp that were brought to North America
eventually escaped captivity (Chick & Pegg, 2001; Naylor, Williams,
& Strong, 2001). Since their liberation, bighead (Hypophthalmichthys
nobilis) and silver carp (Hypophthalmichthys molitrix) have dispersed
northward through the Mississippi River Basin and its tributaries
towards the Laurentian Great Lakes of North America (Chick & Pegg,
2001; Naylor et al., 2001). During this period of expansion, big-
headed carp populations have increased substantially and have
become one of the predominant fish encountered in many locations
(Collins, Butler, Diana, & Wahl, 2015; Collins, Diana, Butler, & Wahl,
2017; MacNamara, Glover, Garvey, Bouska, & Irons, 2016; Sass
et al., 2010).
Bigheaded carp are filter-feeding planktivores that have been
shown to reduce zooplankton and thus pose a substantial ecological
threat to many native fishes that rely on zooplankton during larval,
juvenile and adult life stages (Chapman & Hoff, 2011; Kolar et al.,
2007; Sass et al., 2014). These cyprinids use comb-like gill rakers
and epibranchial organs (i.e., accessory feeding structures that accu-
mulate food particles) to feed on planktonic invertebrates and phyto-
plankton (Callan & Sanderson, 2003; Kolar et al., 2007). Filter-
feeding planktivores consume many prey at once, often in propor-
tion to prey densities (Lazzaro, 1987), although some prey are better
adapted to avoid consumption (Drenner, de Noyelles, & Kettle,
1982). Moreover, some prey populations may also benefit from a
competitive release from other species experiencing enhanced pre-
dation pressure (Neill, 1975). The magnitude of predation across the
size spectrum of prey may be an abrupt (i.e., sigmoidal pattern) tran-
sition between readily exploited and unexploited prey, with potential
compensatory increases by those less exploited prey populations. In
contrast, the magnitude of predation may scale with body size (i.e.,
linearly) as larger, longer-lived and less abundant prey are dispropor-
tionately affected and slower to recover (Drenner, Mummert, de
Noyeiles, & Kettle, 1984).
Most often, the top-down effects of these planktivores are char-
acterised via changes to prey densities (e.g., Collins, Nelson,
Deboom, & Wahl, 2017; Cooke, Hill, & Meyer, 2009; Sass et al.,
2014). Other prey responses, such as plastic changes to body length
and alterations to energy flow via secondary production, are seldom
assessed. The threat of predation can affect prey body size by influ-
encing prey feeding activity and growth (e.g., Peckarsky et al., 2008;
Tollrian & Dodson, 1999), which has implications for egg and clutch
sizes and fitness (Green, 1956; Lynch, 1977). Predators also affect
prey recruitment, particularly when early life stages are susceptible
to predation (e.g., Gaines & Roughgarden, 1987). The culmination of
direct and indirect predator effects on prey populations should
ultimately affect the accumulation of new prey biomass (i.e., energy
flow via secondary production) within the ecosystem. Thus, know-
ledge of each is needed to better characterise the effects of invasive
bigheaded carp in freshwater ecosystems.
Here, we conducted an experiment to quantify the magnitude of
effect of bighead carp on zooplankton body size and daily secondary
production across a range of body lengths. Specifically, we examined
the predatory effects of bighead carp on (1) overall changes to the
size structure of zooplankton assemblages, (2) body lengths of zoo-
plankton taxa and (3) taxa-specific changes to standing crop biomass
and daily secondary production. Finally, we tested whether the rela-
tionship between the magnitude of predation by filter-feeding big-
head carp and prey body size was linear or sigmoidal. Because
strong predation effects on larger taxa can also influence interactions
within the zooplankton assemblage, we considered that smaller taxa
with faster population turnover (i.e., egg to adult) may be released
from regulatory constraints (e.g., predation, competition) and, in turn,
their populations may increase or dampen predation effects (Collins,
Detmer, Nelson, Nannini, & Wahl, 2018; Cooke et al., 2009; Sass
et al., 2014).
2
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METHODS
2.1
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Experimental design
We tested our hypothesis with an additive experiment, which is rec-
ommended for evaluating the effects of non-native fishes because it
hold all factors equal except for the invader (Fausch, 1998). Additive
experimental designs have an inherent logical limitation which pre-
cludes separating the effect of an invader from simply having more
individuals within a treatment (Collins, Nelson, et al., 2017). Conse-
quently, the rationale for an experiment must compliment the design
and any inferential limitations. The logic and design of this experi-
ment reflects patterns observed in nature, where large numbers of
bigheaded carp are imposed over native communities of fishes (Col-
lins et al., 2015; Collins, Diana, et al., 2017; Irons, Sass, McClelland,
& Stafford, 2007). Presumably, a hyperabundance of native plankti-
vores could impart similar effects; however, such a scenario does
not reflect conditions in many locations where bigheaded carp are
abundant.
We compared responses of zooplankton in the presence of a
native fish assemblage (control, n=5 ponds) and a native fish
assemblage plus bighead carp (invaded, n=5 ponds; Table 1). The
experiment lasted 3 months (June–September, 2014) and was con-
ducted in clay-lined ponds (0.04 ha. wetted area; 1.5–1.75 m water
2
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COLLINS AND WAHL
depths) at the Sam Parr Biological Station, Kinmundy, IL, USA. Ten
ponds were filled 5 weeks prior to start of the experiment, at ran-
dom, with filtered water (300-lm sieve to remove larval fishes) from
Forbes Lake (UTM: 38.726, 88.779) to ensure similar inoculums of
zooplankton assemblages. Water temperatures (average SD) were
21.9 1.1°C during the experiment and did not differ between
treatments (ANOVA, F
1, 9
=0.44, p=.76).
All 10 ponds were stocked with juvenile native fishes with func-
tional traits representative of large river–floodplain ecosystems and
included representative taxa of the Illinois River and the upper Mis-
sissippi River. Native fishes encompassed a range of functional traits,
including a benthic predator (channel catfish, Ictaluridae: Ictalurus
punctatus), a planktivore (golden shiner, Cyprinidae: Notemigonus
crysoleucas) and taxa that forage on both benthic and pelagic inver-
tebrates (red shiner, Cyprinidae: Cyprinella lutrensis; largemouth bass,
Centrarchidae: Micropterus salmoides); see Table 1 for experimental
densities. Field surveys by Illinois Natural History Survey biologists
determined that juvenile bigheaded carp comprised a large compo-
nent of fish assemblages in floodplain lakes of the Illinois River (Col-
lins, Diana, et al., 2017). Five ponds were randomly stocked with
juvenile bighead carp so that their densities comprised 58% of the
fish assemblage and 84% of the fish biomass. Juvenile bighead carp
(H. nobilis, 7.62 1.78 g) were obtained from a regional commercial
hatchery (Osage Catfisheries Inc., Osage Beach, MO, USA).
2.2
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Zooplankton sampling and analyses
Zooplankton samples were collected monthly at three random loca-
tions (1–1.5 m depths) within each pond with a depth-integrated
tube sampler. Samples were filtered through 20-lm-mesh sieve to
collect zooplankton (Chick, Levchuk, Medley, & Havel, 2010) and
then stored in Lugol’s solution. Zooplankton samples were counted
and identified to genera when possible (Thorp & Covich, 2010).
Because predation by fishes can affect invertebrate recruitment (e.g.,
Gaines & Roughgarden, 1987) and bighead carp are capable of con-
suming small invertebrates, we examined their potential effect on
copepod recruitment from immature to adult life stages by
comparing densities of copepod nauplii (i.e., free-swimming larvae).
Subsets of 50 individuals were measured using an optical microme-
tre to determine body length (mm). Taxa-specific body lengths were
used as input in length–mass regressions to obtain biomass (dry
mass; McCauley, 1984). To characterise the impact of bighead carp
on the size spectra of planktonic invertebrates, histograms (columns
represent average counts SE;n=5) were generated for invaded
and control ponds. We used ANCOVA to test whether treatment
(categorical factor) influenced the slope of the line between counts
(dependent variable) and length size bins (independent variable).
Secondary production is an integrative measurement of energy
flow through an ecosystem (Dolbeth, Cusson, Sousa, & Pardal,
2012). Despite calls for production-based approaches to aquatic-
and fisheries-related issues, inferences pertaining to production rely
heavily on changes to standing crop biomass. Zooplankton secondary
production was calculated with a regression model for the produc-
tion of freshwater invertebrates (R
2
=.79; Plante & Downing, 1989).
Estimates of annual production were then converted to daily produc-
tion by dividing each estimate by the number of experimental days
(g m
2
day
1
). Regression-based production models have been used
to contrast differences in ecological systems (e.g., Kelly, Solomon,
Weidel, & Jones, 2014), but estimates can differ from classical
approaches (Morin, Mousseau, & Roff, 1987; Stockwell & Johanns-
son, 1997). For instance, production estimates of larger-bodied cope-
pods can be inflated when compared to other production
approaches (i.e., egg ratio method; Stockwell & Johannsson, 1997).
Nevertheless, we reason that the environmental characteristics (e.g.,
temperature, inoculum sources) were similar between experimental
units and any biases would be consistent across controls and treat-
ments. To assess the effects of bighead carp on zooplankton body
lengths, we analysed responses in the last sample date of the experi-
ment using a one-way analysis of variance (ANOVA), with treatment
as the fixed factor. Similarly, daily secondary production was an inte-
grative metric that encompassed the whole duration of the experi-
ment and was analysed with a one-way ANOVA with treatment as
the fixed factor. Standing crop biomass was analysed using a
repeated-measures ANOVA, where the effect of treatment, time and
their interaction was assessed. For all statistical tests, p-values <.05
were considered significant. All response variables were log
10
-trans-
formed to correct for any non-normality of residuals and
heteroscedasticity. All ANOVA’s were conducted using SAS v.9.3
(SAS Institute, Cary, North Carolina, USA).
The magnitude of experimental effect was determined for
ANOVA main effect means via Glass’sD[(Average
control
Average
in-
vaded) SDcontrol
]. Glass’sDwas used because the metric is con-
strained by the variability (SD, standard deviation) of prey
populations in the experimental control (Ferguson, 2009). Effect
sizes for responses (dependent variables: Glass’sDstanding crop bio-
mass and daily production) were examined along the zooplankton
body length spectra (independent variable) to determine whether the
pattern was linear, quadratic or sigmoidal (Logistic 3 parameter, Pro-
bit 4 parameter). Positive values indicate reductions in prey biomass
and production by bighead carp, whereas negative values would
TABLE 1 Average individual body weight (g SD), standing crop
biomass (g/m
2
SD) and density (# m
2
SD) of fishes added to
native (control, n=5) and invaded (treatment, n=5) ponds during
the 3-month experiment (June–September 2014)
Treatment Species Body weight Biomass Density
Control Channel catfish 6.24 2.19 0.32 0.03 0.05
Golden shiner 0.78 0.21 0.10 0.01 0.12
Largemouth bass 1.31 0.94 0.13 0.01 0.10
Red shiner 2.11 0.79 0.08 0.01 0.04
Invaded Bighead carp 7.62 1.78 3.19 0.07 0.42
Channel catfish 6.24 2.19 0.30 0.02 0.05
Golden shiner 0.78 0.21 0.09 0.02 0.12
Largemouth bass 1.31 0.94 0.13 0.01 0.10
Red shiner 2.11 0.79 0.08 0.01 0.04
COLLINS AND WAHL
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3
indicate potential compensatory increases for respective metrics. We
fit and contrasted models using a corrected Akaike information crite-
ria (AICc) model selection approach (Burnham & Anderson, 2003).
The model with the smallest AICc value was considered the best fit.
If the models were within D2 AICc, we determine them to be
equally informative (Burnham & Anderson, 2003). Finally, effect sizes
of standing crop biomass and daily production were regressed to
determine whether effects scaled proportionately or departed from a
1:1 relationship (linear regression: adj. R
2
, RMSE, F,p).
3
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RESULTS
The size structure of the zooplankton assemblage shifted towards
smaller individuals in ponds invaded by bighead carp, whereas the
zooplankton size structure in ponds with only native fishes had a
higher frequency of large-bodied individuals (ANCOVA: treat-
ment 9length bin, F=7.17, p=.01; Figure 1). Shifts towards smal-
ler size distributions were influenced, in small part, by a reduction in
individual body lengths of Diaphanosoma (Family: Sididae) and Daph-
nia (Family: Daphniidae) in ponds where bighead carp were present
(Table 2; Figure 2a). Average (SD) body lengths of Diaphanosoma
decreased by 19% and Daphnia decreased by 9% in the presence of
bighead carp, relative to controls.
The strongest driver of changes to the size distribution of zoo-
plankton assemblage was the direct effect of predation by bighead
carp on the standing crop biomass and secondary production of zoo-
plankton. Larger zooplankton (>0.55 mm) exhibited stronger reduc-
tions in standing crop biomass and daily production when bighead
carp were present (Table 2, Figure 2b,c). For instance, Cyclopoida
standing crop biomass and daily production were reduced by 79%
and 47%, respectively. Diaphanosoma,Daphnia and Calanoida all
responded similarly, with biomass reduced from 92% to 98% and
daily production by 65–74%. Calanoida standing crop biomass also
varied through time, which differed between treatments (time:
F=26.31, p<.001; time 9treatment: F=16.11, p<.001). Con-
trary to our predictions, we detected no compensatory increases by
smaller invertebrates. Bighead carp had no effect on the biomass
and daily production of small-bodied Bosmina (Family: Bosminidae),
Ostracoda and Ceriodaphnia (Family: Daphniidae; Table 2, Figure 2b,
c). Although rotifers were smaller than bosminids and ostracods,
their standing crop biomass and daily production were reduced in
ponds with bighead carp (Table 2, Figure 2b,c). Densities of imma-
ture copepod nauplii, which were similar in size to rotifers, were
75% lower in ponds invaded by bighead carp (F
1, 9
=17.85,
p=.002; Figure 3).
The magnitude (Glass’sD) of bighead carp predation on zoo-
plankton was best characterised as a linear relationship with prey
body length (Table 3). Standing crop biomass (adj. R
2
=.34,
RMSE =1.08, F
1, 7
=4.61, p=.07; biomass effect =1.0069 +
5.56359 9body length) and secondary production (adj. R
2
=.44,
RMSE =1.90, F
1, 7
=6.5, p=.04; production effect =2.1908 +
11.5757 9body length) were generally related to prey body length
(Figure 4a). In general, effect sizes increased with body size and the
strength of this relationship was stronger for daily production. Fur-
thermore, relationship between standing crop biomass and sec-
ondary production effect sizes was not proportional (adj. R
2
=.85,
RMSE =0.51, F
1, 7
=42.0, p=.0006; biomass effect =0.0351 +
0.47747 9production effect). Instead, top-down effects of bighead
carp were skewed towards greater impacts on secondary production
Body length (mm)
0 – 0.1
0.1 – 0.2
0.2 – 0.3
0.3 – 0.4
0.4 – 0.5
0.5 – 0.6
0.6 – 0.7
0.7 – 0.8
0.8 – 0.9
0.9 – 1
1 – 1.1
1.1 – 1.2
0
50
100
150
200
250
300
350
Count (±SE)
Invaded
Control
FIGURE 1 Average count (SE) of planktonic invertebrates
within specific body length bins (mm). Black columns represent the
zooplankton size spectra of ponds invaded (n=5) by bighead carp
Hypophthalmichthys nobilis and white columns represent controls
(n=5) with only native fishes
TABLE 2 Statistical responses (F-value, p-value) examining the
effects of bighead carp on the body length (mm; one-way ANOVA),
standing crop biomass (g/m
2
; rmANOVA) and daily secondary
production (g m
2
day
1
; one-way ANOVA) of zooplankton and
rotifers from a 3-month experiment (June–September, 2014). In all
cases, bighead carp had a negative effect on a response variable
when a significant effect was detected (indicated with bold). For the
repeated-measures ANOVA of standing crop biomass, both time and
time 9treatment interactions were non-significant for all taxa
(p>.05), except Calanoida (time: F=26.31, p<.001;
time 9treatment: F=16.11, p<.001)
Taxa
Body length
Standing crop
biomass Daily production
FpF pF p
Rotifera 2.13 .18 5.46 .04 11.01 .01
Ostracoda 0.13 .74 0.94 .35 <0.001 .98
Bosmina 0.35 .58 1.26 .29 4.07 .07
Ceriodaphnia 0.03 .87 1.32 .28 1.35 .27
Cyclopoida 0.09 .77 8.62 .01 26.43 <.001
Calanoida 0.10 .75 107.6 <.001 83.48 <.001
Diaphanosoma 19.44 .002 62.12 <.001 112.3 <.001
Daphnia 6.35 .05 15.28 .004 29.45 <.001
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COLLINS AND WAHL
rather than the more common metric of standing crop biomass (Fig-
ure 4b).
4
|
DISCUSSION
Our findings indicate intense predation by bighead carp reduced the
body size of individuals, shifted community size structure towards
smaller individuals, reduced the biomass and daily production of zoo-
plankton and reduced immature copepod nauplii. Although filter-fee-
ders can consume many prey at a time, we did not detect an abrupt
threshold between exploited and unexploited prey. Our experiment
indicated that the magnitude of predation increased linearly with
prey body size such that the strongest effects were observed for the
largest prey taxa. Findings from our experiment align with patterns
from the Illinois River (La Grange reach), where densities of Clado-
cerans and Copepods were 9.8 and 26.3 times lower, respectively,
following the invasion of bighead and silver carp (Sass et al., 2014).
Filter-feeding planktivores typically consume more slower prey and
fewer evasive prey like copepods (Drenner et al., 1982; Lazzaro,
1987). Yet, bighead carp had the strongest effect on copepod bio-
mass and daily production, perhaps because of strong negative
effects on immature and less mobile nauplii. Interestingly, filter-feed-
ing bighead carp imparted size-specific changes to the zooplankton
assemblage, producing patterns similar to particulate feeding plankti-
vores (e.g., Brooks & Dodson, 1965; Greene, 1983), despite the fact
that bighead carp do not visually select individual prey. Because big-
head carp are planktivorous throughout their life (Kolar et al., 2007),
feeding on zooplankton as both juveniles and adults, we expect
effects between life stages to be similar. However, such comparisons
Body length (mm)
0.00
0.20
0.40
0.60
0.80
0.0
1.0
2.0
3.0
4.0
Invaded
Control
0.000
0.005
0.010
0.015
0.020
Standing crop biomass (g/m2)
Daily production (g/m2/day)
Rotifera
Bosmina
Ostracoda
Ceriodaphnia
Cyclopoida
Diaphanosoma
Daphnia
Calanoida
(a)
(b)
(c)
FIGURE 2 Effects of invaded (black circles) and native (white
circles) fish assemblages on zooplankton: (a) average individual body
length (mm); (b) standing crop biomass (g/m
2
); (c) daily secondary
production (g m
2
day
1
). Error bars represent 1SE (n=5)
0
100
200
300
400
Control Invaded
Copepod nauplii (# L–1)
a
b
FIGURE 3 Average density of immature copepod nauplii in
ponds with native fishes (control) and ponds with native fishes and
bighead carp (invaded). Error bars represent 1SE (n=5)
TABLE 3 Models selected under AICc model selection to explain
relationships between taxa-specific effect sizes (metrics: standing
crop biomass, g/m
2
; secondary production, g m
2
day
1
) in relation
to prey body length at the end of the 3-month experiment. Each
point represents the effect of bighead carp on a specific
zooplankton taxon. P =parameter
Metric Model AICc DAICc AICc weight BIC
Biomass Linear 33.76 –0.85 27.99
Logistic 3P 37.76 4.00 0.11 24.74
Quadratic 40.02 6.26 0.04 27.00
Probit 4P 56.07 22.31 0.00 26.47
Production Linear 42.70 –0.90 36.94
Quadratic 48.00 5.30 0.06 34.98
Logistic 3P 48.89 6.19 0.04 35.88
Probit 4P 66.18 23.47 0.00 36.58
COLLINS AND WAHL
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5
require further evaluation because other factors such as metabolic
requirements and differences in habitat associations between life
stages may also influence overall effects.
The magnitude of predation by bighead carp scaled positively
with prey body size, except for rotifers. Effect sizes were generally
greater for daily production than for standing crop biomass, suggest-
ing inferences based solely on standing crop biomass may
underrepresent the top-down effect of predation and associated
impacts to energy flows within the planktonic food web. The bio-
mass and production of five zooplankton taxa declined in the pres-
ence of bighead carp. Overall, these effects are consistent with
others demonstrating reduced densities or standing crop biomass of
zooplankton by bigheaded carp (e.g., Fukushima et al., 1999; Sass
et al., 2014; Shao, Xie, & Zhuge, 2001). Our findings indicate that
predation by bighead carp affect zooplankton populations through
multiple mechanisms. Larger and more susceptible zooplankton taxa
such as Calanoida, Daphnia and Diaphanosoma appear to be
exploited faster than their populations (i.e., generation times) could
resupply adults (Gillooly, 2000; Sanoamuang, 1993); thus, their popu-
lations could not overcome predation by bighead carp. For smaller
taxa, the weaker effects observed may have been dampened by fas-
ter population turnover or because they were less abundant and
encountered less often. For such minor differences, the functional
consequences, such as changes to the volumes of water filtered by
suspension-feeding taxa, may be minimal when compared to greater
effects on larger suspension-feeding taxa (e.g., Collins et al., 2018).
We present evidence that bighead carp reduced the body size of
zooplankton at the end of our 3-month experiment. Body lengths of
Diaphanosoma and Daphnia experienced a 9–19% reduction in body
size, presumably from reduced activity, foraging and growth (e.g.,
Lind & Cresswell, 2005; O’Brien, 1987; Van Buskirk & Yurewicz,
1998). In a companion study, we documented a trophic cascade
resulting in increased phytoplankton (Collins & Wahl, 2017), which
indicates that there was abundant food for these zooplankton. Zoo-
plankton will phenotypically reduce body size and age at maturation,
which also reduces clutch size (Green, 1956; Havel & Dodson, 1987;
Lynch, 1977). Despite being smaller, Diaphanosoma and Daphnia
remained susceptible to predation by bighead carp. Based on these
findings, such plastic reductions were inconsequential because stand-
ing crop biomass and daily production of both Diaphanosoma and
Daphnia were reduced.
Fish predation can reduce the recruitment of early life stages of
invertebrates into the population by altering the reproductive output
of adults and by enhancing mortality of larval nauplii (Sebastidae:
Sebastes spp., Gaines & Roughgarden, 1987; Salmonidae spp., Sar-
nelle & Knapp, 2004). Findings from our study suggest juvenile big-
head carp may negatively affect copepod recruitment by reducing
numbers of immature stages, yet the observed pattern may have
been influenced by direct and indirect mechanisms. Copepod nauplii
were similar in size to rotifers, and yet densities of nauplii were
more strongly affected by bighead carp. Both nauplii and rotifers are
readily consumed by bighead carp, based on diet assessments from
the Illinois River, USA (Sampson, Chick, & Pegg, 2009), so direct pre-
dation is an important factor. Additionally, indirect predation effects
may also influence nauplii densities. For instance, numbers of nauplii
depend on the reproductive success of adults and the presence of
egg-bearing females from the population. Finally, carp may have
altered processes that influence the contribution of eggs to the sedi-
ments or survival from egg to naupliar stage. Although we cannot
distinguish direct from indirect influences, our findings suggest that
Body length (mm)
(a)
Effect size: production
1:1
(b)
Effect size
Effect size: biomass
Production
Biomass
–1
1
3
5
7
9
0.0 0.2 0. 4 0.6 0.8
–1
1
3
5
7
9
–113579
FIGURE 4 Experimental effect sizes (Glass’sD;
(Average
control
Average
treatment
)SD
control
) of bighead carp on the
(a) standing crop biomass (linear regression: adj. R
2
=.34,
RMSE =1.08, F
1, 7
=4.61, p=.07; biomass
effect =1.0069 +5.56359 9body length) and daily secondary
production (linear regression: adj. R
2
=.44, RMSE =1.90, F
1, 7
=6.5,
p=.04; production effect =2.1908 +11.5757 9body length) of
zooplankton taxa in relation to average body length (mm). (b) The
relationship between experimental effect sizes (Glass’sD) for each
zooplankton taxa was plotted to determine whether bighead carp
predation effects on standing crop biomass and daily secondary
production scaled in a 1:1 relationship (linear regression: adj.
R
2
=.85, RMSE =0.51, F
1, 7
=42.0, p=.0006; biomass
effect =0.0351 +0.47747 9production effect)
6
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COLLINS AND WAHL
alterations to copepod recruitment limited the production of new
copepod tissue and, ultimately energy flow through the planktonic
environment, as evidenced in their daily secondary production. The
effects of bighead carp on these life history processes are unknown
and warrant further exploration because of the implications for the
dynamics of invertebrate populations and for the flow of energy
through freshwater food webs.
Planktonic rotifers play a significant role in carbon transfer
between the microbial food web and higher trophic levels (Arndt,
1993) and are often an underrepresented component of aquatic
food webs (Chick et al., 2010). By altering the size structure of prey
communities, predators further influence competitive interactions
among prey (Collins et al., 2018; H€
ulsmann, Rinke, & Mooij, 2011).
Although we anticipated compensatory increases by rotifers (Collins
et al., 2018), the removal of large zooplankton did not release roti-
fers from regulatory constraints. Instead, densities of rotifers
declined, indicating these small invertebrates were suppressed during
our experiment. The reduced biomass of rotifers in our experiment
is consistent with several studies (e.g., Fukushima et al., 1999; Shao
et al., 2001), but opposite of others (e.g., Sass et al., 2014), suggest-
ing compensation by rotifer assemblages does vary and the reasons
remain elusive. Similar responses have been observed by other inva-
ders such as zebra mussels (Dreissenidae: Dreissena polymorpha),
which reduced rotifer numbers in the Hudson River, USA (Pace,
Findlay, & Fischer, 1998). Despite their small size, these inverte-
brates are an important component of the diets of bighead and silver
carp in the wild (Sampson et al., 2009; Williamson & Garvey, 2005).
Owing to their short generation times and rapid biomass turnover,
these small invertebrates may provide an efficient pathway of
energy flow to bigheaded carp through the aquatic food web (Nel-
son, Collins, Sass, & Wahl, 2017), particularly if native fishes are
poorly suited to exploit rotifers.
Moving forward, ecologists need to identify the habitats that
supply zooplankton inoculums to mainstem habitats of river–flood-
plain ecosystems (Wahl, Goodrich, Nannini, Dettmers, & Soluk,
2008) and to determine whether bigheaded carp are present within
these habitats and whether their predatory impacts alter zooplank-
ton similarly. If bigheaded carp regulate zooplankton recruitment, or
disparities are observed between taxa, the varied effects on zoo-
plankton may be far reaching, both spatially and temporally. What
are the long-term ramifications of intense exploitation of zooplank-
ton by bigheaded carp? Consumption of females may impact the via-
bility of ephippial and parthenogenetic eggs during digestion (e.g.,
Conway, McFadzen, & Tranter, 1994). Do bigheaded carp reduce the
supply of zooplankton eggs to seed banks in the sediments of large
river–floodplain ecosystems and are ephippia resistant to digestion
(e.g., Mellors, 1975)? Moreover, how might these impacts affect the
resilience of zooplankton communities in the coming decades (e.g.,
Hairston, 1996; Jarnagin, Kerfoot, & Swan, 2004)? Pervasive preda-
tion on nauplii may adversely affect recruitment, limiting the num-
bers of individuals that survive to adulthood, potentially causing
depensation within populations (e.g., Liermann & Hilborn, 2001).
Experimental evaluations, including our own, largely focus on the
immediate or seasonal effects of these invasive planktivores. Future
studies will require examining population dynamics of wild popula-
tions of zooplankton at longer timescales.
ACKNOWLEDGMENTS
We thank M. Diana, S. Butler and M. Nannini for their logistical and
intellectual contributions. Additionally, we thank B. Diffin for his
technical assistance in processing zooplankton samples. Partial sup-
port was provided by the Illinois Natural History Survey and the
Great Lakes Research Initiative, administered through the Illinois
Department of Natural Resources (CAFWS-93). Finally, we thank
members of the Kaskaskia, Ridge Lake and Sam Parr Biological Sta-
tions of the Illinois Natural History Survey, as well as graduate stu-
dents from the University of Illinois for their intellectual discussions
and feedback. Institutional Animal Care and Use Committee
(#14069) approval was obtained before commencement of the
study. All fishes were acquired, retained and used in compliance with
federal, state and local laws and regulations.
AUTHOR CONTRIBUTIONS
SFC and DHW conceived and designed the experiment. SFC per-
formed the experiment. SFC analysed the data and wrote the manu-
script.
ORCID
Scott F. Collins http://orcid.org/0000-0002-9405-1495
REFERENCES
Arndt, H. (1993). Rotifers as predators on components of the microbial
web (bacteria, heterotrophic flagellates, ciliates)—a review. Hydrobi-
ologia,255, 231–246. https://doi.org/10.1007/BF00025844
Brooks, J. L., & Dodson, S. I. (1965). Predation, body size, and composi-
tion of plankton. Science,150,28–35. https://doi.org/10.1126/scie
nce.150.3692.28
Burnham, K. P., & Anderson, D. R. (2003). Model selection and multimodel
inference: A practical information-theoretic approach. New York, NY:
Springer.
Callan, W. T., & Sanderson, S. L. (2003). Feeding mechanisms in carp:
Crossflow filtration, palatal protrusions and flow reversals. Journal of
Experimental Biology,206, 883–892. https://doi.org/10.1242/jeb.
00195
Chapman, D. C., & Hoff, M. H. (2011). Invasive Asian carps in North
America. American Fisheries Society, Symposium 74. American Fish-
eries Society, Bethesda, MD.
Chick, J. H., Levchuk, A. P., Medley, K. A., & Havel, J. H. (2010). Underes-
timation of rotifer abundance a much greater problem than previ-
ously appreciated. Limnology and Oceanography Methods,8,79–87.
https://doi.org/10.4319/lom.2010.8.0079
Chick, J. H., & Pegg, M. A. (2001). Invasive carp in the Mississippi River
basin. Science,292, 2250–2251. https://doi.org/10.1126/science.292.
5525.2250
Collins, S. F., Butler, S. E., Diana, M. J., & Wahl, D. H. (2015). Catch rates
and cost effectiveness of entrapment gears for Asian carp: A
COLLINS AND WAHL
|
7
comparison of pound nets, hoop nets, and fyke nets in backwater
lakes of the Illinois River. North American Journal of Fisheries Manage-
ment,35, 1219–1225. https://doi.org/10.1080/02755947.2015.
1091799
Collins, S. F., Detmer, T. M., Nelson, K. A., Nannini, M. A., & Wahl, D. H.
(2018). The release and regulation of rotifers: Examining the preda-
tory effects of invasive juvenile common and bighead carp. Hydrobi-
ologia,813, 199–211. https://doi.org/10.1007/s10750-018-3526-y
Collins, S. F., Diana, M. J., Butler, S. E., & Wahl, D. H. (2017). A comparison
of sampling gears for capturing juvenile Silver Carp in river-floodplain
ecosystems. North American Journal of Fisheries Management,37,
94–100. https://doi.org/10.1080/02755947.2016.1240121
Collins, S. F., Nelson, K. A., Deboom, C. S., & Wahl, D. H. (2017). The
facilitation of the native bluegill sunfish by the invasive bighead carp.
Freshwater Biology,62, 1645–1654. https://doi.org/10.1111/fwb.
12976
Collins, S. F., & Wahl, D. H. (2017). Invasive planktivores as mediators of
organic matter exchanges within and across ecosystems. Oecologia,
184, 521–530. https://doi.org/10.1007/s00442-017-3872-x
Conway, D. V., McFadzen, I. R., & Tranter, P. R. (1994). Digestion of
copepod eggs by larval turbot Scophthalmus maximus and egg viability
following gut passage. Marine Ecology Progress Series,106, 303–309.
https://doi.org/10.3354/meps106303
Cooke, S. L., Hill, W. R., & Meyer, K. P. (2009). Feeding at different
plankton densities alters invasive bighead carp (Hypophthalmichthys
nobilis) growth and zooplankton species composition. Hydrobiologia,
625, 185–193. https://doi.org/10.1007/s10750-009-9707-y
Dolbeth, M., Cusson, M., Sousa, R., & Pardal, M. A. (2012). Secondary
production as a tool for better understanding of aquatic ecosystems.
Canadian Journal of Fisheries and Aquatic Sciences,69, 1230–1253.
https://doi.org/10.1139/f2012-050
Drenner, R. W., de Noyelles, F., & Kettle, D. (1982). Selective impact of
filter-feeding gizzard shad on zooplankton community structure. Lim-
nology and Oceanography,27, 965–968. https://doi.org/10.4319/lo.
1982.27.5.0965
Drenner, R. W., Mummert, J. R., de Noyeiles, F., & Kettle, D. (1984).
Selective particle ingestion by a filter-feeding fish and its impact on
phytoplankton community structure. Limnology and Oceanography,29,
941–948. https://doi.org/10.4319/lo.1984.29.5.0941
Fausch, K. D. (1998). Interspecific competition and juvenile Atlantic sal-
mon (Salmo salar): On testing effects and evaluating the evidence
across scales. Canadian Journal of Fisheries and Aquatic Sciences,55,
218–231. https://doi.org/10.1139/d98-006
Ferguson, C. J. (2009). An effect size primer: A guide for clinicians and
researchers. Professional Psychology: Research and Practice,40, 532–
538. https://doi.org/10.1037/a0015808
Fukushima, M., Takamura, N., Sun, L., Nakagawa, M., Matsushige, K., &
Xie, P. (1999). Changes in the plankton community following intro-
duction of filter-feeding planktivorous fish. Freshwater Biology,42,
719–735. https://doi.org/10.1046/j.1365-2427.1999.00507.x
Gaines, S. D., & Roughgarden, J. (1987). Fish in offshore kelp forests
affect recruitment to intertidal barnacle populations. Science,235,
479–480. https://doi.org/10.1126/science.235.4787.479
Gillooly, J. F. (2000). Effect of body size and temperature on generation
time in zooplankton. Journal of Plankton Research,22, 241–251.
https://doi.org/10.1093/plankt/22.2.241
Green, J. (1956). Growth, size and reproduction in Daphnia (Crustacea:
Cladocera). Journal of Zoology,126, 173–204.
Greene, C. H. (1983). Selective predation in freshwater zooplankton
communities. Internationale Revue der gesamten Hydrobiologie und
Hydrographie,68, 297–315. https://doi.org/10.1002/iroh.1983068
0302
Hairston, N. G. (1996). Zooplankton egg banks as biotic reservoirs in
changing environments. Limnology and Oceanography,41, 1087–1092.
https://doi.org/10.4319/lo.1996.41.5.1087
Havel, J. E., & Dodson, S. I. (1987). Reproductive costs of Chaoborus-
induced polymorphism in Daphnia pulex.Hydrobiologia,150, 273–281.
https://doi.org/10.1007/BF00008708
H€
ulsmann, S., Rinke, K., & Mooij, W. M. (2011). Size-selective predation
and predator-induced life-history shifts alter the outcome of competi-
tion between planktonic grazers. Functional Ecology,25, 199–208.
https://doi.org/10.1111/j.1365-2435.2010.01768.x
Irons, K. S., Sass, G. G., McClelland, M. A., & Stafford, J. D. (2007).
Reduced condition factor of two native fish species coincident with
invasion of non-native Asian carps in the Illinois River, USA Is this
evidence for competition and reduced fitness? Journal of Fish
Biology,71, 258–273. https://doi.org/10.1111/j.1095-8649.2007.
01670.x
Jarnagin, S. T., Kerfoot, W. C., & Swan, B. K. (2004). Zooplankton life
cycles: Direct documentation of pelagic births and deaths relative to
diapausing egg production. Limnology and Oceanography,49, 1317–
1332. https://doi.org/10.4319/lo.2004.49.4_part_2.1317
Kelly, P. T., Solomon, C. T., Weidel, B. C., & Jones, S. E. (2014). Terrestrial
carbon is a resource, but not a subsidy, for lake zooplankton. Ecology,
95, 1236–1242. https://doi.org/10.1890/13-1586.1
Kolar, C. S., Chapman, D. C., Courtenay, W. R. Jr, Housel, C. M., Williams,
J. D., & Jennings, D. P. (2007). Bigheaded carps: A biological synopsis
and environmental risk assessment. Bethesda, MD: American Fisheries
Society.
Lazzaro, X. (1987). A review of planktivorous fishes: Their evolution,
feeding behaviours, selectivities, and impacts. Hydrobiologia,146,97–
167. https://doi.org/10.1007/BF00008764
Liermann, M., & Hilborn, R. (2001). Depensation: Evidence, models and
implications. Fish and Fisheries,2,33–58. https://doi.org/10.1046/j.
1467-2979.2001.00029.x
Lind, J., & Cresswell, W. (2005). Determining the fitness consequences of
antipredation behavior. Behavioral Ecology,16, 945–956. https://doi.
org/10.1093/beheco/ari075
Lynch, M. (1977). Fitness and optimal body size in zooplankton popula-
tions. Ecology,58, 763–774. https://doi.org/10.2307/1936212
Mack, R. N., Simberloff, D., Lonsdale, W. M., Evans, H., Clout, M., & Baz-
zaz, F. A. (2000). Biotic invasions: Causes, epidemiology, global con-
sequences, and control. Ecological Applications,10, 689–710.
https://doi.org/10.1890/1051-0761(2000)010[0689:BICEGC]2.0.
CO;2
MacNamara, R., Glover, D., Garvey, J., Bouska, W., & Irons, K. (2016).
Bigheaded carps (Hypophthalmichthys spp.) at the edge of their
invaded range: Using hydroacoustics to assess population parameters
and the efficacy of harvest as a control strategy in a large North
American river. Biological Invasions,18, 3293–3307. https://doi.org/
10.1007/s10530-016-1220-4
McCauley, E. (1984). The estimation of the abundance and biomass of
zooplankton in samples. In J. A. Downing, & F. H. Rigler (Eds.), A
manual on methods for the assessment of secondary productivity in
fresh waters (pp. 232–240). London: Blackwell Scientific Publications.
Mellors, W. K. (1975). Selective predation of ephippal Daphnia and the
resistance of ephippal eggs to digestion. Ecology,56, 974–980.
https://doi.org/10.2307/1936308
Morin, A., Mousseau, T. A., & Roff, D. A. (1987). Accuracy and precision
of secondary production estimates. Limnology and Oceanography,32,
1342–1352. https://doi.org/10.4319/lo.1987.32.6.1342
Moyle, P. B., & Light, T. (1996). Biological invasions of fresh water:
Empirical rules and assembly theory. Biological Conservation,78, 149–
161. https://doi.org/10.1016/0006-3207(96)00024-9
Naylor, R. L., Williams, S. L., & Strong, D. R. (2001). Aquaculture –A
gateway for exotic species. Science,294, 1655–1656. https://doi.org/
10.1126/science.1064875
Neill, W. E. (1975). Experimental studies of microcrustacean competition,
community composition and efficiency of resource utilization. Ecol-
ogy,56, 809–826. https://doi.org/10.2307/1936293
8
|
COLLINS AND WAHL
Nelson, K. A., Collins, S. F., Sass, G. G., & Wahl, D. H. (2017). A
response-surface examination of competition and facilitation between
native and invasive juvenile fishes. Functional Ecology,31, 2157–
2166. https://doi.org/10.1111/1365-2435.12922
O’Brien, W. J. (1987). Planktivory by freshwater fish: Thrust and parry in
the pelagic. In W. C. Kerfoot, & A. Sih (Eds.), Predation: Direct and
indirect impacts on aquatic communities (pp. 3–16). Hanover, NH:
University Press of New England.
Pace, M. L., Findlay, S. E., & Fischer, D. (1998). Effects of an invasive
bivalve on the zooplankton community of the Hudson River. Freshwa-
ter Biology,39, 103–116. https://doi.org/10.1046/j.1365-2427.1998.
00266.x
Peckarsky, B. L., Abrams, P. A., Bolnick, D. I., Dill, L. M., Grabowski, J. H.,
Luttbeg, B., ... Trussell, G. C. (2008). Revisiting the classics: Consid-
ering nonconsumptive effects in textbook examples of predator–prey
interactions. Ecology,89, 2416–2425. https://doi.org/10.1890/07-
1131.1
Plante, C., & Downing, J. A. (1989). Production of freshwater inverte-
brate populations in lakes. Canadian Journal of Fisheries and Aquatic
Sciences,46, 1489–1498. https://doi.org/10.1139/f89-191
Ricciardi, A., Steiner, W. W., Mack, R. N., & Simberloff, D. (2000). Toward
a global information system for invasive species. BioScience,50, 239–
244. https://doi.org/10.1641/0006-3568(2000)050[0239:TAGISF]2.
3.CO;2
Ruiz, G. M., & Carlton, J. T. (2003). Invasive species: Vectors and manage-
ment strategies. New York, NY: Island Press.
Sampson, S. J., Chick, J. H., & Pegg, M. A. (2009). Diet overlap among
two Asian carp and three native fishes in backwater lakes on the Illi-
nois and Mississippi rivers. Biological Invasions,11, 483–496.
https://doi.org/10.1007/s10530-008-9265-7
Sanoamuang, L. (1993). The effect of temperature on morphology, life
history and growth rate of Filinia terminalis (Plate) and Filinia cf. pejleri
(Hutchinson) in culture. Freshwater Biology,30, 257–267. https://doi.
org/10.1111/j.1365-2427.1993.tb00807.x
Sarnelle, O., & Knapp, R. A. (2004). Zooplankton recovery after fish
removal: Limitations of the egg bank. Limnology and Oceanography,
49, 1382–1392. https://doi.org/10.4319/lo.2004.49.4_part_2.1382
Sass, G. G., Cook, T. R., Irons, K. S., McClelland, M. A., Michaels, N. N.,
O’Hara, T. M., & Stroub, M. R. (2010). A mark-recapture population
estimate for invasive silver carp (Hypophthalmichthys molitrix) in the
La Grange Reach, Illinois River. Biological Invasions,12, 433–436.
https://doi.org/10.1007/s10530-009-9462-z
Sass, G. G., Hinz, C., Erickson, A. C., McClelland, N. N., McClelland, M. A.,
& Epifanio, J. M. (2014). Invasive bighead and silver carp effects on
zooplankton communities in the Illinois River, Illinois, USA. Journal of
Great Lakes Research,40, 911–921. https://doi.org/10.1016/j.jglr.
2014.08.010
Shao, Z., Xie, P., & Zhuge, Y. (2001). Long-term changes of planktonic
rotifers in a subtropical Chinese lake dominated by filter-feeding
fishes. Freshwater Biology,46, 973–986. https://doi.org/10.1046/j.
1365-2427.2001.00731.x
Smith, D. W. (1985). Biological control of excessive phytoplankton
growth and the enhancement of aquacultural production. Canadian
Journal of Fisheries and Aquatic Sciences,42, 1940–1945. https://doi.
org/10.1139/f85-240
Stockwell, J. D., & Johannsson, O. E. (1997). Temperature-dependent
allometric models to estimate zooplankton production in temperate
freshwater lakes. Canadian Journal of Fisheries and Aquatic Sciences,
54, 2350–2360. https://doi.org/10.1139/f97-141
Thorp, J. H., & Covich, A. P. (2010). Ecology and classification of North
American freshwater invertebrates. New York, NY: Academic Press.
Tollrian, R., & Dodson, S. I. (1999). Inducible defenses in cladocera: Con-
straints, costs, and multipredator environments. In R. Tollrian, & C. D.
Harvell (Eds.), The ecology and evolution of inducible defenses (pp.
177–202). Princeton, NJ: Princeton University Press.
Van Buskirk, J., & Yurewicz, K. L. (1998). Effects of predators on prey
growth rate: Relative contributions of thinning and reduced activity.
Oikos,1,20–28. https://doi.org/10.2307/3546913
Vitousek, P. M., Mooney, H. A., Lubchenco, J., & Melillo, J. M. (1997).
Human domination of Earth’s ecosystems. Science,277, 494–499.
https://doi.org/10.1126/science.277.5325.494
Wahl, D. H., Goodrich, J., Nannini, M. A., Dettmers, J. M., & Soluk, D. A.
(2008). Exploring riverine zooplankton in three habitats of the Illinois
River ecosystem: Where do they come from? Limnology and Oceanog-
raphy,53, 2583–2593. https://doi.org/10.4319/lo.2008.53.6.2583
Williamson, M. H., & Fitter, A. (1996). The varying success of invaders.
Ecology,77, 1661–1666. https://doi.org/10.2307/2265769
Williamson, C. J., & Garvey, J. E. (2005). Growth, fecundity, and diets of
newly established silver carp in the middle Mississippi River. Transac-
tions of the American Fisheries Society,134, 1423–1430. https://doi.
org/10.1577/T04-106.1
How to cite this article: Collins SF, Wahl DH. Size-specific
effects of bighead carp predation across the zooplankton size
spectra. Freshwater Biol. 2018;00:1–9. https://doi.org/
10.1111/fwb.13109
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