Invasive planktivores as mediators of organic matter exchanges within and across ecosystems

Abstract

Bighead carp (Hypophthalmichthys nobilis) are an invasive planktivore that can greatly deplete planktonic resources. Due to the inefficient conversion of food into fish tissue, large portions of consumed materials are egested and shunted to benthic habitats. We explored how bighead carp alter pools of organic matter between planktonic and benthic habitats, and across ecosystem boundaries. Here, we report evidence from a manipulative experiment demonstrating that bighead carp greatly reapportion pools of organic matter from planktonic to benthic habitats to such a degree that additional effects propagated across ecological boundaries into terrestrial ecosystems. Strong direct consumption by bighead carp reduced filamentous algae, biomass and production of zooplankton, and production of a native planktivorous fish within planktonic habitats. Reduced herbivory indirectly increased phytoplankton (chlorophyll a). Direct consumption of organic matter by bighead carp supported high carp production and concomitant losses of materials due to egestion. Perhaps in response to organic matter subsidies provided by fish egestion, ponds having bighead carp had higher standing crop biomass of Chironomidae larvae, as well as cross-boundary fluxes of their adult life stage. In contrast, we detected reduced cross-boundary fluxes of adult Chaoboridae midges in ponds having bighead carp. Consideration of bighead carp as mediators of organic matter exchanges provides a clearer framework for predicting the direct and extended impacts of these invasive planktivores in freshwater ecosystems. The perception of bighead carp must evolve beyond competitors for planktonic resources, to mediators and processors of nutrients and energy within and across ecosystems.

Full text

1 3
Oecologia (2017) 184:521–530
DOI 10.1007/s00442-017-3872-x
ECOSYSTEM ECOLOGY – ORIGINAL RESEARCH
Invasive planktivores as mediators of organic matter exchanges
within and across ecosystems
Scott F. Collins1 · David H. Wahl1
Received: 18 July 2016 / Accepted: 15 April 2017 / Published online: 27 April 2017
© Springer-Verlag Berlin Heidelberg 2017
ponds having bighead carp. Consideration of bighead carp
as mediators of organic matter exchanges provides a clearer
framework for predicting the direct and extended impacts
of these invasive planktivores in freshwater ecosystems.
The perception of bighead carp must evolve beyond com-
petitors for planktonic resources, to mediators and proces-
sors of nutrients and energy within and across ecosystems.
Keywords Asian carp · Invasive species · Cross-boundary
flux · Insect emergence · Indirect effect
Introduction
Unraveling the complex processes that structure food webs
has historically been addressed under two epistemologi-
cal approaches: an individualistic and community-based
approach that emphasizes the organism, population, or com-
munity as the central foci and a holistic ecosystem-based
approach concerned with the fluxes and exchanges of energy
and materials (Pickett et al. 2007; Moore and de Ruiter 2012).
Bridging these sub-disciplines to address pressing ecological
issues such as biological invasions can be powerful, as dif-
fering perspectives can better inform questions of organisms
and their impacts on ecological processes (Jones and Law-
ton 1995; Loreau and Holt 2004). Food web ecologists have
expanded the traditional adage, who-eats-whom, to further
consider the flows and fluxes of materials through interacting
species and across trophic levels (Lindeman 1942; Moore and
de Ruiter 2012), which invites the question, what of the con-
sumed? For instance, when a predator consumes prey, there
is a reduced pool of prey, but the constituent materials of the
prey (i.e., nutrients, organic matter) are not immediately lost
to the ecosystem; rather, they are re-packaged as assimilated
consumer biomass, respired, or expelled as physiological
Abstract Bighead carp (Hypophthalmichthys nobilis)
are an invasive planktivore that can greatly deplete plank-
tonic resources. Due to the inefficient conversion of food
into fish tissue, large portions of consumed materials are
egested and shunted to benthic habitats. We explored how
bighead carp alter pools of organic matter between plank-
tonic and benthic habitats, and across ecosystem bounda-
ries. Here, we report evidence from a manipulative experi-
ment demonstrating that bighead carp greatly reapportion
pools of organic matter from planktonic to benthic habitats
to such a degree that additional effects propagated across
ecological boundaries into terrestrial ecosystems. Strong
direct consumption by bighead carp reduced filamentous
algae, biomass and production of zooplankton, and produc-
tion of a native planktivorous fish within planktonic habi-
tats. Reduced herbivory indirectly increased phytoplankton
(chlorophyll a). Direct consumption of organic matter by
bighead carp supported high carp production and concomi-
tant losses of materials due to egestion. Perhaps in response
to organic matter subsidies provided by fish egestion, ponds
having bighead carp had higher standing crop biomass of
Chironomidae larvae, as well as cross-boundary fluxes
of their adult life stage. In contrast, we detected reduced
cross-boundary fluxes of adult Chaoboridae midges in
Communicated by Robert O. Hall.
Electronic supplementary material The online version of this
article (doi:10.1007/s00442-017-3872-x) contains supplementary
material, which is available to authorized users.
* Scott F. Collins
collscot@illinois.edu
1 Illinois Natural History Survey, Kaskaskia Biological Station,
Sullivan, IL, USA

522 Oecologia (2017) 184:521–530
1 3
byproducts (i.e., egesta, excreta). With respect to the latter,
the inefficient acquisition of nutrients and energy by consum-
ers can have considerable impacts on food webs (e.g., Wotton
and Malmqvist 2001; Vanni 2002).
Biological invasions are stressors to ecosystem pro-
cesses (Crooks 2002), and are an integral driver of global
environmental change (Vitousek et al. 1997). Invasive spe-
cies can greatly alter their surroundings by exploiting lim-
iting resources (e.g., Kennedy and Hobbie 2004; Baxter
et al. 2004), by altering nutrient cycles (e.g., Collins et al.
2011), and changing organic matter budgets (e.g., Mineau
et al. 2012), to name a few. Although the negative effects
of exotic species have been described for individuals and
whole ecosystems alike, simultaneous investigations of
impacts across biological levels of organization are rare
(Simon and Townsend 2003). Understanding the mecha-
nisms through which biological invasions alter ecological
processes (e.g., trophic dynamics, energy flows) should
aid in predicting the range of direct, indirect, positive, and
negative effects that occur within invaded habitats as well as
in adjacent habitats connected through material exchanges
(Polis et al. 1997; Reiners and Driese 2001). Unfortunately,
few studies actually test the processes or pathways through
which impacts occur, which is a critical shortcoming of bio-
logical invasion research (reviewed in Levine et al. 2003).
Bigheaded carp (Hypophthalmichthys spp.) is a collec-
tive name designated to the species bighead carp (H. nobi-
lis) and silver carp (H. moltrix). These fishes are highly pro-
ductive planktivores whose northward expansion through
the Mississippi River basin poses a threat to the Laurentian
Great Lakes ecosystem (Chick and Pegg 2001). Extremely
high densities of bigheaded carp have been observed in
river–floodplain ecosystems, with estimates of 5500 kg wet
mass river km−1 of silver carp in the Illinois River (Sass
et al. 2010) and nightly catches in some floodplain lakes
in excess of 1000 kg wet mass (Collins et al. 2015b). Con-
siderable quantities of organic matter must be consumed
to produce and sustain the observed levels of fish biomass.
Bigheaded carp efficiently filter plankton particles from the
water column (e.g., phyto-, zooplankton; Radke and Kahl
2002; Sass et al. 2014), which removes a food resource for
some native fishes (Irons et al. 2007; Sampson et al. 2009).
To date, the direct effects of these invasive fishes within
planktonic habitats are generally appreciated (i.e., who eats
whom?). What remains unclear are the attendant effects
of bigheaded carp in other aquatic habitats that are linked
through the exchange of organic matter (i.e., what of the
consumed?).
Migratory fishes are vectors and mediators of material
exchanges in river–floodplain ecosystems (e.g., Flecker
et al. 2010). The quantities of resources consumed by
mobile fishes and the fates of these resources (i.e., assim-
ilated as biomass, egested) may have impacts in adjacent
habitats. Consumed but unassimilated materials from fishes
like bigheaded carp can subsidize organisms in benthic
habitats via the sedimentation of egested particles (Polis
et al. 1997; Wotton and Malmqvist 2001; Schindler and
Scheuerell 2002). These effects can further propagate into
adjacent ecosystems as organisms mature or redistribute.
Other non-native fishes also alter the cross-boundary move-
ments of aquatic insects (Baxter et al. 2004; Epanchin et al.
2010; Collins et al. 2016a) and amphibians (Bradford 1989;
Knapp et al. 2001). Because studies have largely focused
on planktonic responses to bigheaded carp invasions, it
remains unclear how these fishes impact the coupling of
habitats (e.g., benthic-pelagic, aquatic-terrestrial).
Here, we present the results of a manipulative experi-
ment that examined how an invasive planktivore altered
pools and fluxes of organic matter between habitats (i.e.,
benthic, planktonic) and across ecosystem boundaries (i.e.,
aquatic to terrestrial ecosystems). We report evidence dem-
onstrating that bighead carp greatly reapportion pools of
organic matter from planktonic to benthic habitats to such a
degree that additional effects propagated across ecological
boundaries into terrestrial ecosystems. Most notably, these
cross-boundary impacts indicate that the effects of big-
headed carp may not be constrained to aquatic ecosystems.
Methods
Hypotheses and study design
By consuming, assimilating, and egesting organic matter,
bigheaded carp may play an integral role influencing food
web dynamics. We tested the hypothesis that bighead carp
alter material exchanges between planktonic and benthic
habitats within aquatic ecosystems, with effects that prop-
agate from aquatic to terrestrial ecosystems. We predicted
strong and negative direct effects of bigheaded carp on
planktonic food resources, which would reduce the produc-
tion of native fishes. Furthermore, increased production of
bighead carp and corresponding contributions of egested
particles would subsidize benthic habitats. Thus, we pre-
dicted benthic Chironomidae larvae and channel catfish
would respond positively. Finally, emergence of aquatic
insects serves as a flux of material from aquatic to terres-
trial ecosystems. We predicted that egested material by big-
head carp indirectly increases export of organic matter from
aquatic to terrestrial ecosystems via adult insect emergence.
We tested these hypotheses with an additive experi-
ment, which is recommended for evaluating the effects of
non-native fishes (Fausch 1998). The experiment lasted
3 months and was conducted during June–September of
2014 in earthen ponds (0.04 ha. wetted area; clay-lined sed-
iment; 1.5–1.75 m water depths) at the Sam Parr Biological

523Oecologia (2017) 184:521–530
1 3
Station, Kinmundy IL, USA. Ponds had vegetation that
extended 1.5 m from the wetted edges. Ten ponds were
filled 5 weeks prior to start of the experiment, at random,
with filtered water (300 μm sieve to remove larval fishes)
from Forbes Lake (UTM: 38.726099, −88.779831) to
ensure similar inoculums of plankton communities and
to allow for colonization by benthic macroinvertebrates.
Water temperatures averaged (±SD) 21.9 ± 1.1 °C dur-
ing the experiment and did not differ between treatments
(ANOVA, F1, 9 = 0.44, p = 0.76). The additive press design
sought to compare how a highly productive planktivore act-
ing as a stressor within an invaded ecosystem directly and
indirectly alters pools and fluxes of organic matter with an
aquatic environment and across ecosystem boundaries rela-
tive to a native fish community. Henceforth, we use a native
versus invaded dichotomy when describing the effects of
bighead carp, where native fish assemblages are controls
and ponds of native fishes plus bighead carp are invaded.
For this experiment, we distinguish benthic from planktonic
habitats within ponds, and refer to cross-boundary fluxes of
organic matter from aquatic to terrestrial ecosystems.
All ten ponds were stocked with juvenile native fishes
with functional traits representative of floodplain lake habi-
tats of large river ecosystems, and included representative
taxa of the Illinois River and the upper Mississippi River
ecosystem. Native fishes encompassed a range of func-
tional traits, including benthic predators (Channel catfish
Ictalurus punctatus), obligate planktivores (Golden shiner
Notemigonus crysoleucas), and taxa that forage on both
benthic and planktonic invertebrates (Largemouth bass
Micropterus salmoides; Red shiner Cyprinella lutrensis).
Field surveys by Illinois Natural History Survey biologists
determined that juvenile bigheaded carp can dominate (65–
98%) juvenile fish assemblages in floodplain lakes of the
Illinois River (Collins et al. 2017). Juvenile bighead carp
(average ± SD, 7.62 ± 1.78 g) were stocked at a density
of 0.42 fish m−2 in five randomly selected ponds. Bighead
carp were obtained from a regional commercial hatchery
(Osage Catfisheries, Inc., Osage Beach, MO, USA). Big-
head carp abundance comprised 58% of the fish assem-
blage of invaded ponds.
Food web sampling and analyses
We quantified changes in dominant organic matter pools
within the water column over the duration of the experi-
ment. Algal communities were sampled monthly as float-
ing filamentous algae and phytoplankton. Filamentous
algae were sampled at random from the top 5 cm of the
water column within floating quadrats (0.5 × 0.5 m float-
ing frame, 2 subsamples per pond). Samples were dried
and weighed to the nearest 0.1 g. Strong winds pushed all
filamentous algae into the vegetated margins of the ponds
near the end of the experiment. Therefore, only a 2-month
response for filamentous algae is reported. Phytoplankton
was quantified monthly, based on chlorophyll a concentra-
tions from a depth-integrated water sample. Water was fil-
tered through 0.7 μm glass fiber filters. Chlorophyll a was
extracted with 90% acetone for 24 h, and then measured
via fluorometry (Turner Design, model TD700, Sunnyvale,
California, USA; APHA 2005). Turbidity (nephelometric
units, NTU; electronic turbidimeter) was assessed from 1-L
samples collected at the midpoint of the water column.
Zooplankton samples were collected monthly at three
random locations within each pond from a depth-integrated
water sample. Samples were filtered through a 20-μm
sieve, and then stored in Lugol’s solution. Zooplankton
samples were counted and identified to Family. Subsets of
50 individuals were measured using an optical micrometer
to determine body length. Taxa-specific body lengths were
used as input in length–mass regressions to obtain biomass
(dry mass; McCauley 1984). Daily zooplankton produc-
tion was estimated with a regression model for freshwater
invertebrates (Plante and Downing 1989; R2 = 0.79). We
estimated production as per unit area to make compari-
sons across trophic levels in similar units. Exploitation
efficiency was calculated as the amount of zooplankton
production consumed by fishes (see below) relative to the
amount produced, to examine the top-down influence of
fish predation.
To estimate how much bighead carp subsidized benthic
habitats, macroinvertebrate larvae were sampled monthly.
For each sample period, offshore habitats (subsam-
ples) >1 m deep were sampled within each pond using a
15 × 15 × 15 cm Ekman Bottom Grab (Wildco, Wildlife
Supply Co.). In the laboratory, larvae were separated from
detritus, identified to Order, and measured to the nearest
0.5 mm. Biomass was calculated from length to weight
relationships (Benke et al. 1999).
Survival and growth rates for each fish species were
used to estimate secondary production (g m−2 day−1) dur-
ing the experiment. Survival was determined as the num-
ber and percent of individuals remaining at the conclusion
of the experiment relative to the numbers stocked. Growth
rates (g day−1) were quantified as the difference between
the initial and final mean weights of all individuals over
the duration of the experiment. Gut contents were sampled
monthly from a minimum of five individuals (collected
via seining) of each species via gastric lavage. Proportions
of fish gut contents were identified and grouped into four
dominant pools of organic matter: (1) amorphous materi-
als including phytoplankton cells, particulate matter, and
other unidentifiable materials; (2) filamentous algae; (3)
macroinvertebrates; (4) zooplankton. To quantify path-
ways of organic matter flow through fishes and how they
were affected by the presence of bighead carp, we used the

524 Oecologia (2017) 184:521–530
1 3
trophic basis of production approach (Benke and Wallace
1980) that accounts for both the quality and quantity of a
diet item in its contribution to production. Fish production
and gut content proportions were used to quantify the pro-
duction attributable to diet items consumed, the total quan-
tity of each item consumed, and the total egested materials
(Benke and Wallace 1980; All equations in S1). Proportions
of diet items consumed during our experiment were aver-
aged for each sample period for each pond. The portion of
production attributed to a given diet item (Eq. 1; Fi) was
calculated as:
where Gi is the proportion of food type i in the consumers
diet, AEi is the assimilation efficiency of food type i, and
NPE is the net production efficiency (Cross et al. 2011).
Assimilation efficiencies for fishes were: amorphous detri-
tus 0.3; filamentous algae 0.33; macroinvertebrates 0.75;
zooplankton 0.95 (Benke and Wallace 1980; Chen et al.
1985). The net production efficiency of age-0 fish was 0.24,
which is consistent with other studies examining the con-
sumptive effects of juvenile fishes (Cross et al. 2011; Col-
lins et al. 2016b).
To determine the relative contribution of each diet item
to fish production (Eq. 2; PFij) for each sampling interval,
we used
where Pj is the total sum of production estimates for each
fish species. The total consumption of food resources by
fishes during the experiment for each food type i to species
j was calculated by dividing PFij by the product of AEi and
NPE. Finally, we estimated the flux of egested organic mat-
ter (Eq. 3; Ej) to benthic habitats by species, as:
These methods allowed us to isolate the contributions of
bighead carp egestion from other fishes, and also were use-
ful because shallow ponds are poorly suited for sediment
traps because of wind-driven re-suspension of materials
(Kozerski 1994).
Finally, to test the indirect effect of bighead carp on
cross-boundary fluxes of organic matter, we measured the
emergence rates (mg DM m−2 week−1) of adult aquatic
insects with cylindrical sticky traps suspended under a
plastic enclosure. The bottom edge of each enclosure
was submerged below the surface of the water to ensure
a closed environment and allowed us to quantify flux per
unit area. Transparency sheets were constructed into cylin-
ders (0.062 m2), and coated in Tanglefoot resin. Traps were
(1)
Fi
=
(Gi
×
AEi
×
NPE)
(2)
PF
ij =
F
i

n
i=1
F
i
×P
j
(3)
E
j=

P×

1−AEij


AEij ×NPEij
.
deployed for 7 days, and then were replaced, ensuring con-
tinuous sampling during the experiment. In the laboratory,
adult insects were counted. Subsets of individuals (20 per
pond per sample period) were measured to determine aver-
age length. Length–weight regressions were used to esti-
mate biomass (Sabo et al. 2002).
Direct and indirect effects of bighead carp were ana-
lyzed using analysis of variance (ANOVA), with treatment
as the fixed factor and fish production, benthic macroin-
vertebrate biomass, zooplankton biomass and production,
chlorophyll a, total egestion, and insect emergence as
response variables. Because ecological effects may require
time to manifest, the treatment × time interaction was used
to assess the responses of food web components to detect
any lagged effects of bighead carp. For all statistical tests, p
values <0.05 were considered significant. All response vari-
ables were log10 transformed to correct for any non-nor-
mality of residuals and heteroscedasticity. Analyses were
conducted using SAS v.9.3 (SAS Institute, Cary, North
Carolina, USA).
Results
Reduced pools of organic matter within the water col-
umn coincided with high rates of bighead carp produc-
tion. Bighead carp accrued 4.35 ± 0.36 g DM m−2 (aver-
age ± SE) of biomass during the experiment, with survival
averaging 90% ± 0.03. Bighead carp reduced standing
crop biomass of free-floating filamentous algae by 91%,
relative to controls after 2 months (Fig. 1a; F1, 9 = 95.76,
p < 0.001). Filamentous algae averaged about 26.8% of
the diets of bighead carp. Bighead carp consumed an esti-
mated 4.09 g DM m−2 of filamentous algae throughout
the experiment (Table 1). Zooplankton constituted 22.1%
of bighead carp diets. Direct predation of zooplankton by
bighead carp resulted in an 88% reduction in zooplankton
standing crop biomass (F1, 9 = 147, p < 0.001) and a 61%
reduction in zooplankton secondary production (Fig. 1b;
F1, 9 = 13.87, p = 0.005), relative to controls. Bighead carp
consumed an estimated 0.05 ± 0.002 g DM m−2 day−1
of zooplankton, and a total of 5.31 ± 0.32 g DM m−2 of
zooplankton production over the duration of the experi-
ment. Exploitation efficiency of zooplankton production by
bighead carp averaged 64.3 ± 5.1% (Table 2). Top-down
control of zooplankton by bighead carp was also associated
with increased chlorophyll a concentrations (Fig. 1c; F1,
9 = 4.43, p = 0.06). However, turbidity (abiotic and biotic
particles) did not differ between treatments (F1, 9 = 0.67,
p = 0.48).
Exploitation of food resources in planktonic habitats
by bighead carp corresponded with reduced production of
the total native fish assemblage (F1, 9 = 4.76, p = 0.06);

525Oecologia (2017) 184:521–530
1 3
a pattern driven by golden shiners, whose production
was 54% lower in ponds with bighead carp (Fig. 1d; F1,
9 = 10.01, p = 0.01). Strong reductions in zooplankton
by bighead carp resulted in fewer zooplankton being con-
sumed by golden shiners and ultimately less production
(Table 1). No effects of bighead carp were detected for
the production of largemouth bass (Fig. 1d; F1, 9 = 0.79,
p = 0.39). Red shiners experienced high mortality rates in
all ponds and accurate estimates of production could not be
calculated.
Bighead carp shunted a sizeable portion of unassimi-
lated organic matter from planktonic to benthic habitats.
We estimated that total egestion by all fish species was
425% greater in ponds with ponds invaded by bighead
carp, relative to controls (Fig. 2a; F1, 9 = 97.2, p < 0.001).
Bighead carp egested 16.03 DM g m−2 of organic matter
(i.e., sum of all diet categories) over the 3-month experi-
ment. Reduced production of golden shiners also resulted
in lower rates of egestion in ponds with bighead carp (F1,
9 = 9.57, p = 0.014). Though egestion by golden shiners
was reduced in ponds with bighead carp, the net impact
was positive, as contributions by bighead carp exceeded
losses by golden shiners. Egestion did not differ between
ponds for largemouth bass or channel catfish (p > 0.05).
Larval Chironomidae had 90% higher biomass in
ponds with bighead carp relative to controls (Fig. 2b, F1,
26 = 4.70, p = 0.04), which was consistent with our pre-
diction. However, no differences were observed for
Trichoptera, Odonata, or Ephemeroptera (p > 0.05). In con-
trast to our predictions, production of channel catfish (ben-
thic predators) did not respond to increased egested mate-
rial (Fig. 1d; F1, 9 = 2.13, p = 0.18).
Impacts of bighead carp on cross-boundary fluxes of
aquatic insects varied. Emergence of adult Chironomidae
midges across the aquatic-terrestrial boundary increased by
228% in ponds with bighead carp (Fig. 3a, F1, 9 = 49.73,
p < 0.001). In contrast, average weekly emergence of
Chaoboridae was reduced by 79% in ponds with bighead
carp (Fig. 3b, F1, 9 = 23.18, p < 0.001). No changes were
observed for Culicidae, nor for the Orders Trichoptera,
Ephemeroptera, or Odonata (p > 0.05; Fig. 3c–f).
Discussion
Bighead carp were associated with reduced filamentous
algae, reduced biomass and production of zooplankton,
and reduced production of a native planktivore. In addi-
tion, emergence of adult Chaoboridae midges was reduced
whereas Chironomidae midges increased relative to con-
trols. In some cases, the effects of bighead carp were visu-
ally striking when compared to controls (Fig. 4). Reduc-
tions in pools of organic matter within planktonic habitats
were accompanied by a high degree of carp secondary pro-
duction and egestion of consumed materials. We detected
positive responses in benthic habitats which propagated
Fig. 1 Effects of bighead
carp on standing crop biomass
or secondary production of
major organic matter pools
within water columns of
experimental ponds. Values are
mean ± standard error (n = 5).
a Standing crop biomass of
filamentous algae on the surface
on ponds after 2 months. b
Secondary production of the
total zooplankton community. c
Phytoplankton responses based
on changes in chlorophyll a
concentrations within water col-
umn. d Secondary production
of native golden shiner (GOS),
largemouth bass (LMB), and
channel catfish (CCF) within
experimental ponds. Letters
above columns denote signifi-
cant treatment effects. Asterisk
on panel (d) indicates species-
specific significant differences
between treatment and control
0.0
0.2
0.4
0.6
0.8
1.0
1.2 a
b
Fish secondary production
(g DM
m-2 3-mo-1)
0
1
2
3
4
5
Control Invaded
a
b
0.0
0.5
1.0
1.5
2.0
2.5
Control Invaded
GOS
LMB
CCF
*
Chlorophyll a
(μg L-1)
Zooplankton secondary production
(g DM m-2 3-mo-1)
Filamentous algae biomass
(g DM m-2)
(a) (b)
(d)(c)
a
b
0
5
10
15
20
25

526 Oecologia (2017) 184:521–530
1 3
Table 1 Comparison of total consumption of dominant organic matter pools and corresponding contributions of diet items to fish secondary
production (assimilated) and egestion of unassimilated organic matter by fish assemblages in native controls vs. invaded ecosystems
Due to high mortality rates in treatment and controls, red shiners were not evaluated. All values are reported mean ± standard error, g m−2 dry
mass
Response Species Treatment Amorphous materials Filamentous algae Macroinvertebrates Zooplankton
Total consumption Bighead carp Control – – – –
Invaded 17.81 ± 2.81 4.09 ± 0.41 2.2 ± 0.34 5.31 ± 0.21
Golden shiner Control 0.13 ± 0.03 0.01 ± <0.01 <0.01 ± <0.01 0.61 ± 0.06
Invaded 0.06 ± 0.02 <0.01 ± <0.01 <0.01 ± <0.01 0.28 ± 0.08
Largemouth bass Control 0.78 ± 0.09 0.03 ± <0.01 1.25 ± 0.06 0.98 ± 0.04
Invaded 0.79 ± 0.1 0.02 ± <0.01 1.1 ± 0.24 0.87 ± 0.13
Channel catfish Control 2.24 ± 0.18 0.1 ± 0.01 5.89 ± 0.41 0 ± 0
Invaded 2.44 ± 0.35 0.09 ± 0.01 4.87 ± 0.4 0 ± 0
Contribution to fish production Bighead carp Control – – – –
Invaded 1.28 ± 0.2 0.32 ± 0.03 0.4 ± 0.06 1.21 ± 0.05
Golden shiner Control 0.01 ± <0.01 <.01 ± <0.01 0.01 ± <0.01 0.14 ± 0.01
Invaded 0.01 ± <0.01 0.01 ± <0.01 0.01 ± <0.01 0.06 ± 0.02
Largemouth bass Control 0.06 ± 0.01 <.01 ± <0.01 0.22 ± 0.01 0.22 ± 0.01
Invaded 0.06 ± 0.01 <.01 ± <0.01 0.2 ± 0.04 0.2 ± 0.03
Channel catfish Control 0.16 ± 0.01 0.01 ± <0.01 1.06 ± 0.07 0 ± 0
Invaded 0.18 ± 0.03 0.01 ± <0.01 0.88 ± 0.07 0 ± 0
Total egestion Bighead carp Control – – – –
Invaded 12.47 ± 1.97 2.74 ± 0.28 0.55 ± 0.09 0.27 ± 0.01
Golden shiner Control 0.09 ± 0.02 0 ± 0 <.01 ± <0.01 0.03 ± <0.01
Invaded 0.04 ± 0.01 0 ± 0 <.01 ± <0.01 0.01 ± <0.01
Largemouth bass Control 0.55 ± 0.06 0.02 ± <0.01 0.31 ± 0.02 0.05 ± <0.01
Invaded 0.56 ± 0.07 0.01 ± <0.01 0.27 ± 0.06 0.04 ± 0.01
Channel catfish Control 1.57 ± 0.13 0.07 ± 0.01 1.47 ± 0.1 0 ± 0
Invaded 1.71 ± 0.24 0.06 ± 0.01 1.22 ± 0.1 0 ± 0
Table 2 Estimated production (g m−2) and consumption (g m−2) of zooplankton by bighead carp and the native fish assemblage over the dura-
tion of the 12-week experiment during summer 2014
SE = standard error. Exploitation efficiency = consumption of prey: prey production
Treatment Pond Estimated zooplank-
ton production
Consumption of zoo-
plankton by bighead
carp
Exploitation effi-
ciency by bighead
carp (%)
Consumption of
zooplankton by all
fishes
Exploitation efficiency
by all fishes (%)
Control 2 23.40 1.33 5.7
3 23.96 1.51 6.3
4 19.45 1.68 8.6
8 19.75 1.73 8.8
9 23.09 1.71 7.4
Mean ± SE 21.9 ± 1.0 1.6 ± 0.1 7.4 ± 0.6
Invaded 1 7.34 5.25 71.5 6.25 85.1
5 7.44 4.75 63.9 5.38 72.4
6 7.04 5.58 79.3 7.03 99.8
7 10.84 5.94 54.8 7.23 66.7
10 9.66 5.01 51.9 6.39 66.1
Mean ± SE 8.5 ± 0.8 5.3 ± 0.2 64.3 ± 5.1 6.5 ± 0.3 78.0 ± 6.4

527Oecologia (2017) 184:521–530
1 3
into the terrestrial environment through the emergence of
Chironomidae midges. Such patterns are similar to other
riverine invaders like zebra mussels (Dreissena polymor-
pha), which greatly transformed large river food webs by
altering planktonic resources for some taxa while facilitat-
ing others (Thayer et al. 1997; Strayer et al. 1999).
Bighead carp’s exploitation of planktonic resources
propagated effects across trophic levels and ecological
boundaries. By reducing zooplankton, bighead carp indi-
rectly increased the phytoplankton community via trophic
cascade. Moreover, by consuming a shared prey resource
and reducing golden shiner production, bighead carp indi-
rectly reduced the quantity of materials egested by shiners,
thus impacting material exchanges between planktonic and
benthic habitats. These reductions were offset by the strong
contributions of egested materials by bighead carp. As pre-
dicted, egested materials subsidized benthic habitats, which
increased larval Chironomidae, and resulted in a substan-
tial increase in the emergence of their adult life stage.
These findings indicate that large river planktivores can
affect organisms in adjacent habitats by altering benthic–
planktonic coupling, with effects that can propagate across
ecosystems boundaries (Flecker et al. 2010). In contrast,
Chaoboridae emergence decreased in the presence of big-
head carp. The mechanism is unclear but may have resulted
because Chaoboridae feed on zooplankton or because
they were directly consumed by fishes. Increased emer-
gence of Chironomidae offset reductions of Chaoboridae
midges by nearly an order of magnitude. Overall, the net
effect of bighead carp resulted in a higher export of aquatic
insects, which is opposite of other non-native fishes (c.f.,
Baxter et al. 2004; Epanchin et al. 2010). Theoretically, by
increasing these cross-boundary exchanges, bighead carp
could indirectly subsidize terrestrial insectivores, thereby
altering terrestrial community dynamics (e.g., Murakami
and Nakano 2002). Because Chironomidae can disperse
considerable distances (Muehlbauer et al. 2014), the effects
of bighead carp may extend into the terrestrial landscape.
Such impacts warrant further exploration.
Reconciling the observed and sometimes counter-intu-
itive responses in our experiment required knowledge of
the composition (i.e., who eats whom?), quantities (i.e.,
organic matter flows), and fates (i.e., what of the con-
sumed?) of materials consumed by bighead carp. For
instance, zooplankton constituted only 22% of bighead carp
diets, yet accounted for 39% of their production because
they are a high quality food source. Complementary esti-
mates of daily and total zooplankton production indicated
reduced energy flows through that food web component,
and allowed us to further quantify exploitation efficiency
(e.g., the ratio of the consumption of prey to their produc-
tion) of these fishes—a metric seldom estimated. Bighead
carp alone consumed 64% of zooplankton production
over the experiment (78% when including native fishes).
Strong exploitation by an invader is not unprecedented,
as non-native brown trout (Salmo trutta) also exploit a
greater proportion of benthic invertebrate production rela-
tive to native fishes (Huryn 1998). Estimates of consump-
tion of zooplankton by fishes in our experiment were close
to estimates of zooplankton production, despite using two
differing analytic methods. By estimating secondary pro-
duction of zooplankton in response to bighead carp, our
experiment empirically supports what many have suspected
and inferred through changes in density and standing crop
biomass—bighead carp substantially reduce energy flow
through zooplankton assemblages.
Most fisheries management agencies neglect to sam-
ple or calculate ecosystem processes, relying instead on
changes in densities or standing crop biomass (e.g., Meyer
1997; Collins et al. 2015a; Skern-Mauritzen et al. 2015).
Snapshots of standing crops inadequately account for turno-
ver of new biomass, leading to disparities between biomass
and production. Consider the sampling metrics and treat-
ment effect sizes between larval (standing crop biomass)
and adult Chironomidae (rate of flux). Standing crop bio-
mass of Chironomidae larvae was 90% greater in invaded
0
5
10
15
20
25
30
Bighead carp
Native fishes
0
10
20
30
40
50
60
Chironomidae biomass
(mg DM m-2)
a
b
Total egested material
(g DM m-2)
(a)
(b)
Control Invaded
Control Invaded
Fig. 2 Effects of bighead carp on organisms associated with ben-
thic habitats. a Estimated flux of egested material from native fishes
and bighead carp. b Standing crop biomass (n = 5; mean ± standard
error) of Chironomidae larvae

528 Oecologia (2017) 184:521–530
1 3
ponds. In contrast, the flux of adult Chironomidae biomass
emerging from invaded ponds increased by 228%. In our
case, inferences based solely on standing crop biomass
would underestimate the impacts of bighead carp, when
in reality effects were far greater. Production estimates
allowed us to calculate organic matter flows and exploita-
tion efficiencies based on relatively simple calculations.
Without these metrics, we would not have been able to
estimate bighead carps ability to exploit zooplankton
resources. For the trophic basis of production, reliable esti-
mates are dependent on accurate diet and secondary pro-
duction data (Cross et al. 2011). Fortunately, the ponds had
a simple food web structure, which is advantageous from
an experimental perspective. Moreover, juvenile bigheaded
carp exhibit schooling behavior, so they forage in similar
locations, which likely contributed to homogeneity of diets.
The use of regression models to estimate zooplankton pro-
duction introduces some biases based on the predictive
capabilities of the model (Morin et al. 1987). For instance,
estimates of larger bodied Copepods can be inflated when
compared to other production approaches (i.e., egg ratio
method; Stockwell and Johannsson 1997). These large
bodied taxa are also more susceptible to predation by big-
headed carp (Sass et al. 2014). Nevertheless, we reason any
biases would be consistent across controls and treatments.
Animals play a crucial role in altering movements of
nutrients and energy (Polis et al. 1997). Recycling and
translocation of materials by fishes have largely focused
on nutrient contributions via excretion and responses by
primary producers (e.g., Vanni 2002), yet coupling of
habitats via sedimentation of particulates is widely recog-
nized as ecologically important (Polis et al. 1997; Wotton
and Malmqvist 2001; Schindler and Scheuerell 2002). We
Time (week)
0
2
4
6
8
10
0
25
50
75
100
0
20
40
60
12345678910 11 12
0
100
200
300
400
0
5
10
15
12345678910 11 12
(e) Trichoptera
Emergence (mg DM m-2 week-1)
(d) Odonata
(f) Ephemeroptera
(a) Chironomidae
(b) Chaoboridae
(c) Culicidae
Invaded Control
0
10
20
30
40
50
Fig. 3 Emergence (mg DM m−2 week−1; mean ± standard error) of adult aquatic insects from ponds with (invaded; n = 5) and without (native
controls; n = 5) bighead carp. All responses are in dry mass
Fig. 4 Ponds adjacent to one another stocked with native fishes (top)
and an invaded pond, stocked with the same native fish assemblage
plus bighead carp (bottom). Visual differences were observed in free-
floating filamentous algal mats after 2 months. Photo credit: Scott F.
Collins

529Oecologia (2017) 184:521–530
1 3
detected strong associations between bighead carp growth,
egestion, and Chironomidae biomass in benthic habi-
tats, which was consistent with our predictions. Egested
material subsidized benthic habitats and appears to have
increased the standing crop biomass and productivity
(inferred via flux of emergence) of Chironomidae (r-strate-
gists). In addition, sedimentation of other materials such as
phytoplankton cells (also indirectly enhanced by bighead
carp) may have also contributed to observed responses. The
lack of response by channel catfish (benthic predator) may
be due several factors including insufficient quantities of
egested material relative to their body size, poor resource
quality relative to other food resources, and availability of
other food resources. Our study focused primarily on larger
animals, but additional steps are needed to examine how
these subsidies alter other ecosystem processes including
decomposition rates, ecosystem metabolism, and biogeo-
chemical transformations.
Additive designs are useful for studying the effects of
invasive species because they hold all factors equal except
for the invader (Fausch 1998). A salient critique of additive
designs is the confounding effect of adding more individu-
als, irrespective of the invader. Thus, it can be difficult to
determine whether an effect was due to the invader or add-
ing more individuals. For instance, would similar effects
occur had we added equivalent numbers of native plankti-
vores such as gizzard shad (Dorosoma cepedianum), big-
mouth buffalo (Ictiobus cyprinellus), American paddlefish
(Polyodon spathula), river carpsucker (Carpiodes carpio),
etc.? Presumably so; but to do so would be artificial and
would not reflect patterns observed in nature. Populations
of these native large river fishes pale in comparison to the
numbers of bigheaded carp within the Mississippi River
and its tributaries (Irons et al. 2007; Collins et al. 2015b).
With the substantial numbers of bigheaded carp inhabit-
ing large river (Sass et al. 2010) and floodplain lakes (Col-
lins et al. 2015b) of the Mississippi River and tributaries,
it is logical to further consider how population dynamics
of these invaders are shaping river–floodplain ecosystems.
The large numbers of bigheaded carp are undoubtedly
contributing large quantities of egested material to these
ecosystems. Our experiment indicated that these contri-
butions could have substantial food web effects, but these
patterns need to be evaluated in more hydrologically com-
plex ecosystems (e.g., variable flows among river–flood-
plain habitats). Although bighead carp were restricted to
the confines of the pond environment, in river–floodplain
ecosystems, the movements of these mobile consumers are
dynamic and will dictate where these egested particles are
delivered. Hydrologic conditions (e.g., velocity) should fur-
ther mediate the area over which these particles ultimately
settle. Consideration of bigheaded carp as mediators of
organic matter exchanges provides a clearer framework
for predicting the impacts of these invasive planktivores
in river–floodplain ecosystems. If the observed ecological
processes from our experiment scale to river–floodplain
ecosystems, our perception of bighead and silver carp
should evolve beyond competitors for planktonic resources,
to facilitators, mediators, and processors of nutrients and
energy within and across ecosystems.
Acknowledgements We specifically thank M. Diana, S. Butler, M.
Naninni, B. Van Ee, M. Stanton, B. Smith for their logistical, field,
and laboratory assistance. We also thank members of the Kaskaskia,
Ridge Lake, and Sam Parr Biological stations of the Illinois Natural
History Survey, as well as graduate students from the University of
Illinois for their intellectual discussions and feedback.
Author contribution statement SFC and DHW conceived and
designed the experiment. SFC performed the experiment. SFC and
DHW analyzed the data. SFC wrote the manuscript.
References
APHA (American Public Health Association) (2005) Standard meth-
ods for the examination of water and wastewater, 21st edn.
APHA, Washington, DC
Baxter CV, Fausch KD, Murakami M, Chapman PL (2004) Fish inva-
sion restructures stream and forest food webs by interrupting
reciprocal prey subsidies. Ecology 85:2656–2663
Benke AC, Wallace JB (1980) Trophic basis of production among net-
spinning caddisflies in a southern Appalachian stream. Ecology
61:108–118
Benke AC, Huryn AD, Smock LA, Wallace JB (1999) Length-mass
relationships for freshwater macroinvertebrates in North Amer-
ica with particular reference to the southeastern United States. J
N Am Benthol Soc 18:308–343
Bradford DF (1989) Allotopic distribution of native frogs and intro-
duced fishes in high Sierra Nevada lakes of California: impli-
cation of the negative effect of fish introductions. Copeia
1989:775–778
Chen S, Hu C, Tian L, Shun X (1985) Digestion of silver carp (Hypo-
thalmichthys moltrix) and bighead carp (Aristichthys nobilis) for
Daphnia pulex. Collect Treatise Icthyol 4:163–170
Chick JH, Pegg MA (2001) Invasive carp in the Mississippi River
Basin. Science 292:2250–2251
Collins SF, Moerke AH, Chaloner DT, Janetski DJ, Lamberti GA
(2011) Response of dissolved nutrients and periphyton to spawn-
ing Pacific salmon in three northern Michigan streams. J N Am
Benthol Soc 30:831–839
Collins SF, Marcarelli AM, Baxter CV, Wipfli MS (2015a) A critical
assessment of the ecological assumptions underpinning compen-
satory mitigation of salmon-derived nutrients. Environ Manag
56:571–586
Collins SF, Butler SE, Diana MJ, Wahl DH (2015b) Catch rates and
cost effectiveness of entrapment gears for Asian carp: a compari-
son of pound nets, hoop nets, and fyke nets in backwater lakes of
the Illinois River. N Am J Fish Manag 35:1219–1225
Collins SF, Marshall B, Moerke AH (2016a) Aerial insect responses
to non-native Chinook salmon spawning in a Great Lakes tribu-
tary. J Great Lakes Res 42:630–636
Collins SF, Baxter CV, Marcarelli AM, Wipfli MS (2016b) Effects
of experimentally added salmon subsidies on resident fishes via
direct and indirect pathways. Ecosphere 7(3):1–17

530 Oecologia (2017) 184:521–530
1 3
Collins SF, Diana MJ, Butler SE, Wahl DH (2017) A comparison of
sampling gears for capturing juvenile Silver Carp in river-flood-
plain ecosystems. N Am J Fish Manag 37:94–100
Crooks JA (2002) Characterizing ecosystem-level consequences of
biological invasions: the role of ecosystem engineers. Oikos
97:153–166
Cross WF, Baxter CV, Donner KC, Rosi-Marshall EJ, Kennedy TA,
Hall RO Jr, Wellard Kelly HA, Rogers RS (2011) Ecosystem
ecology meets adaptive management: food web response to a
controlled flood on the Colorado River, Glen Canyon. Ecol Appl
21:2016–2033
Epanchin PN, Knapp RA, Lawler SP (2010) Nonnative trout impact
an alpine-nesting bird by altering aquatic-insect subsidies. Ecol-
ogy 91:2406–2415
Fausch KD (1998) Interspecific competition and juvenile Atlantic
salmon (Salmo salar): on testing effects and evaluating the evi-
dence across scales. Can J Fish Aquat Sci 55:218–231
Flecker AS, McIntyre PB, Moore JW, Anderson JT, Taylor BW, Hall
RO Jr (2010) Migratory fishes as material and process subsidies
in riverine ecosystems. Am Fish Soc Symp 73:559–592
Huryn AD (1998) Ecosystem-level evidence for top-down and bot-
tom-up control of production in a grassland stream system. Oec-
ologia 115:173–183
Irons KS, Sass GG, McClelland MA, Stafford JD (2007) Reduced
condition factor of two native fish species coincident with inva-
sion of non-native Asian carps in the Illinois River, U.S.A. Is
this evidence for competition and reduced fitness? J Fish Biol
71:258–273
Jones C, Lawton JH (1995) Linking species and ecosystems. Chap-
man and Hall, New York
Kennedy TA, Hobbie SE (2004) Saltcedar (Tamarix ramosissima)
invasion alters organic matter dynamics in a desert stream.
Freshw Biol 49:65–76
Knapp RA, Corn PS, Schindler DE (2001) The introduction of nonna-
tive fish into wilderness lakes: good intentions, conflicting man-
dates, and unintended consequences. Ecosystems 4:275–278
Kozerski HP (1994) Possibilities and limitations of sediment traps
to measure sedimentation and resuspension. Hydrobiologia
284:93–100
Levine JM, Vilà M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S
(2003) Mechanisms underlying the impacts of exotic plant inva-
sions. Proc R Soc Lond B: Biol Sci 270:775–781
Lindeman RL (1942) The trophic-dynamic aspect of ecology. Ecol-
ogy 23:399–417
Loreau M, Holt RD (2004) Spatial flows and the regulation of ecosys-
tems. Am Nat 163:606–615
McCauley E (1984) The estimation of the abundance and biomass
of zooplankton in samples. In: Downing JA, Rigler FH (eds) A
manual on methods for the assessment of secondary productiv-
ity in fresh waters. Blackwell Scientific Publications, London, pp
232–240
Meyer JL (1997) Conserving ecosystem function. In: Pickett STA,
Ostfeld RS, Shachak M, Likens GE (eds) The ecological basis of
conservation. Chapman and Hall, New York, pp 136–145
Mineau MM, Baxter CV, Marcarelli AM, Minshall GW (2012) An
invasive riparian tree reduces stream ecosystem efficiency via a
recalcitrant organic matter subsidy. Ecology 93:1501–1508
Moore JC, de Ruiter PC (2012) Energetic food webs: an analysis of
real and model ecosystems. Oxford University Press, Oxford
Morin A, Mousseau TA, Roff DA (1987) Accuracy and preci-
sion of secondary production estimates. Limnol Oceanogr
32:1342–1352
Muehlbauer JD, Collins SF, Doyle MW, Tockner K (2014) How wide
is a stream? Spatial extent of the potential “stream signature” in
terrestrial food webs using meta-analysis. Ecology 95:44–55
Murakami M, Nakano S (2002) Indirect effect of aquatic insect emer-
gence on a terrestrial insect population through by birds preda-
tion. Ecol Lett 5:333–337
Pickett ST, Kolasa J, Jones CG (2007) Ecological understanding: the
nature of theory and the theory of nature. Academic Press, New
York
Plante C, Downing JA (1989) Production of freshwater invertebrate
populations in lakes. Can J Fish Aquat Sci 46:1489–1498
Polis GA, Anderson WB, Holt RD (1997) Toward an integration of
landscape and food web ecology: the dynamics of spatially sub-
sidized food webs. Annu Rev Ecol Syst 28:289–316
Radke RJ, Kahl U (2002) Effects of a filter-feeding fish [silver carp,
Hypophthalmichthys molitrix (Val.)] on phyto- and zooplankton
in a mesotrophic reservoir: results from an enclosure experiment.
Freshw Biol 47:2337–2344
Reiners WA, Driese KL (2001) The propagation of ecological influ-
ences through heterogeneous environmental space. Bioscience
51:939–950
Sabo JL, Bastow JL, Power ME (2002) Length–mass relationships for
adult aquatic and terrestrial invertebrates in a California water-
shed. J N Am Benthol Soc 21:336–343
Sampson SJ, Chick JH, Pegg MA (2009) Diet overlap among two
Asian carp and three native fishes in backwater lakes on the Illi-
nois and Mississippi rivers. Biol Invasion 11:483–496
Sass GG, Cook TR, Irons KS, McClelland MA, Michaels NN, O’Hara
TM, Stroub MR (2010) A mark-recapture population estimate
for invasive silver carp (Hypophthalmichthys molitrix) in the La
Grange Reach, Illinois River. Biol Invasion 12:433–436
Sass GG, Hinz C, Erickson AC, McClelland NN, McClelland MA,
Epifanio JM (2014) Invasive bighead and silver carp effects on
zooplankton communities in the Illinois River, Illinois, USA. J
Great Lakes Res 40:911–921
Schindler DE, Scheuerell MD (2002) Habitat coupling in lake ecosys-
tems. Oikos 98:177–189
Simon KS, Townsend CR (2003) Impacts of freshwater invaders at
different levels of ecological organization, with emphasis on sal-
monids and ecosystem consequences. Freshw Biol 48:982–994
Skern-Mauritzen M, Ottersen G, Handegard NO, Huse G, Ding-
sør GE, Stenseth NC, Kjesbu OS (2015) Ecosystem processes
are rarely included in tactical fisheries management. Fish Fish
17:165–175
Stockwell JD, Johannsson OE (1997) Temperature-dependent allo-
metric models to estimate zooplankton production in temperate
freshwater lakes. Can J Fish Aquat Sci 54:2350–2360
Strayer DL, Caraco NF, Cole JJ, Findlay S, Pace ML (1999) Trans-
formation of freshwater ecosystems by bivalves: a case study of
zebra mussels in the Hudson River. Bioscience 49:19–27
Thayer SA, Haas RC, Hunter RD, Kushler RH (1997) Zebra mussel
(Dreissena polymorpha) effects on sediment, other zoobenthos,
and the diet and growth of adult yellow perch (Perca flavescens)
in pond enclosures. Can J Fish Aquat Sci 54:1903–1915
Vanni MJ (2002) Nutrient cycling by animals in freshwater ecosys-
tems. Annu Rev Ecol Syst 33:341–370
Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human
domination of Earth’s ecosystems. Science 277:494–499
Wotton RS, Malmqvist B (2001) Feces in aquatic ecosystems. Biosci-
ence 51:537–544