Isotope niche dimension and trophic overlap between bigheaded carps and native filter-feeding fish in the lower Missouri River, USA
Isotope niche dimension and trophic overlap between bigheaded carps and native filter- feeding fish in the lower Missouri River, USA
Jianzhu Wang 0 1
Duane Chapman 1
Jun Xu 1
Yang Wang 1
Binhe Gu 0 1
0 Engineering Research Center of Eco-environment in Three Gorges Reservoir Region, Ministry of Education, China Three Gorges University , Yichang, China, 2 U.S. Geological Survey , Columbia Environmental Research Center , Columbia , MO, United States of America, 3 Institute of Hydrobiology, the Chinese Academy of Sciences , Wuhan , China , 4 Department of Geological Sciences, Florida State University & National High Magnetic Field Laboratory , Tallahassee, FL , United States of America, 5 Soil and Water Science Department, University of Florida , Gainesville, Florida , United States of America
1 Editor: Masami Fujiwara, Texas A&M University , UNITED STATES
Stable carbon and nitrogen isotope values (δ13C and δ15N) were used to evaluate trophic niche overlap between two filter-feeding fishes (known together as bigheaded carp) native to China, silver carp (Hypophthalmichthys molitrix) and bighead carp (Hypophthalmichthys nobilis), and three native filter-feeding fish including bigmouth buffalo (Ictiobus cyprinellus), gizzard shad (Dorosoma cepedianum) and paddlefish (Polyodon spathula) in the lower Missouri River, USA, using the Bayesian Stable Isotope in R statistics. Results indicate that except for bigmouth buffalo, all species displayed similar trophic niche size and trophic diversity. Bigmouth buffalo occupied a small trophic niche and had the greatest trophic overlap with silver carp (93.6%) and bighead carp (94.1%) followed by gizzard shad (91.0%). Paddlefish had a trophic niche which relied on some resources different from those used by other species, and therefore had the lowest trophic overlap with bigheaded carp and other two native fish. The trophic overlap by bigheaded carp onto native fish was typically stronger than the reverse effects from native fish. Average niche overlap between silver carp and native species was as high as 71%, greater than niche overlap between bighead carp and native fish (64%). Our findings indicate that bigheaded carps are a potential threat to a diverse and stable native fish community.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Funding: Data analysis and manuscript preparation
were supported by National Natural Science
Foundation of China (grant No. 51179094 and
30700091) to JW and (grant No. 41376158) to BG.
The funders had no role in study design, data
collection and analysis, decision to publish, or
preparation of the manuscript.
Trophic structure of a biological community was typically described in the past as the number
of species, size range, abundance and feeding habits. However, this information seldom
provides significant insights as to the stability and function of a consumer community for
biological conservation and management. The effects of biological invasion on a consumer
community must be quantified not only from the viewpoint of species abundance and
richness, but also from the interactions of introduced species with the native community. New
theory and methodologies have helped increase understanding of ecosystem structure and
function under various scenarios of natural conditions and anthropogenic disturbances [1±3].
Stable isotope natural abundance provides insights into carbon sources and trophic
positions of consumers in aquatic food webs. Stable carbon isotopes (δ13C) of organic matter of
different origins are often distinct from one another due to differences in photosynthetic
pathways and growth conditions [
]. Transfers of organic matter to consumers do not result in
substantial isotope fractionation and hence δ13C is used as an indicator for carbon flow and
resource diversity. Stable nitrogen isotopes (δ15N) are useful in determining consumer trophic
position because δ15N increases during each trophic transfer [
]. Furthermore, consumer
δ13C and δ15N provide a record of animal feeding and incorporation of dietary carbon and
nitrogen during growth, thereby providing more accurate and integrated information on
animal use of resources and trophic connections at different time and space scales.
Early use of stable isotope data in trophic ecology was limited to tracking carbon flow and
to describing feeding relationships [6±8]. Later applications of stable isotope trophic ecology
include the quantifications of food chain length [
], dietary overlaps  and animal
]. With the introduction of advanced statistical tools, consumer stable isotopes are
used to quantify omnivory, trophic niche, and niche overlap [12±14]. Layman [
] proposed a
set of trophic niche metrics to describe community trophic structure. A number of studies
have used this approach to quantify the changes in food web structure [
] as the results of
ecosystem fragmentation [
], hydrological changes [
] and trophic niche overlap between
native and nonnative fish [
]. More recently, a Bayesian approach has been used to quantify
trophic metrics proposed by Layman [
] at species and community levels [
approach has also been used to identify patterns of trophic structure , species invasion [
] and trophic overlap [
The introduction of fish into aquatic ecosystems leads to changes in species composition,
relative abundance and use of native resources. Risk assessments [
12, 26, 27
] have consistently
predicted that bighead carp (Hypopthalmithys nobilis) and silver carp (H. molitrix) are highly
likely to cause environmental problems where they invade and reach high abundance.
Introduction of fishes of the genus Hypophthalmichthys (known together as bigheaded carps)
around the world, including in North America, have consistently resulted in large reductions
in the abundance of crustacean zooplankton and changes in the abundance of other plankton,
including substantial changes in other aspects of the plankton community [27±29], commonly
including changes in size of the phytoplankton community towards nano- and
picophytoplankton, which are likely too small to be effectively preyed upon by North American
filterfeeding fishes [
]. Indeed, the invasion and extreme population growth of silver carp
(Hypophthalmichthys molitrix) and bighead carp (Hypophthalmichthys nobilis) in the
Mississippi River basin has coincided with declines in condition [
] and abundance [
native planktivores including bigmouth buffalo (Ictiobus cyprinellus), gizzard shad (Dorosoma
cepedianum) and emerald shiner (Notropis atherinoides). The recreationally important
filterfeeder American paddlefish (Polyodon spathula) has been shown to be outcompeted by
bighead carp in ponds [
]. Effects on other unstudied species are likely. Millions of dollars are
spent annually in North America for the control of bighead and silver carp population and
range. If diets overlap and resources are limiting, then competition between bigheaded carps
and native fishes is likely.
The objective of this study was to elucidate niche characteristic and trophic overlaps of two
bigheaded carps with three native fishes in the lower Missouri River (Fig 1). This was
accomplished by calculating trophic niche metrics and overlap using the Bayesian stable isotope
]. Information discussed in this study might add important insights of
potential effects of biological invasion on native species and management of natural ecosystems.
2 / 13
Fig 1. Sample collection site map for the lower Missouri River and adjacent tributaries, Missouri, USA.
Materials and methods
All fish handling and euthanization was performed according to relevant guidelines and
regulations and the Columbia Environmental Research Center Animal Care and Use Policy.
Experimental protocols were approved by the Columbia Environmental Research Center's Animal
Care and Use Committee and this study was approved by the committee.
Sampling and laboratory analysis
Fish were collected in November and December of 2005. The majority of fish samples were
collected from the Missouri River in central Missouri. A small number of fish were collected
from within the Lamine and Osage Rivers, near their confluences with the Missouri River (Fig
1). There was a total of approximately 121 river km between the most distant sample sites,
including distance up the tributaries. Fish were collected using trammel nets set in the low
water-velocity environments preferred by all of these fish [
] and were measured to the
nearest millimeter (total length, except paddlefish, where the eye-to-fork measurement was used).
A sample of white muscle tissue was taken from above the lateral line and posterior to the
dorsal fin of each fish, rinsed with deionized water, and placed in a scintillation vial. All samples
were placed on ice for transport back to laboratory. To calculate fish trophic position, pink
papershell (Potamilus ohiensis), a freshwater mussel, was collected as a baseline organism. The
adductor muscle tissue was used, cleaned with deionized water and placed in a scintillation
Muscle tissue was freeze-dried and powdered at the USGS Columbia Environmental
Research Center at Columbia, MO. Approximately 1 mg of fine powder was loaded into a tin
3 / 13
capsule for analysis. All samples were analyzed using a Carlo Erba Elemental Analyzer
interfaced to a Finnigan MAT Delta Plus XP stable isotope ratio mass spectrometer at the Florida
State University. The results were reported in the standard δ notation relative to the Vienna
Pee Dee Belemnite (PDB) standard for 13C/12C and atmospheric nitrogen for 15N/14N ratios,
respectively. The analytical precision (based on replicate analyses of lab standards processed
with each batch of samples and on sample replicates) was ± 0.1½ for both 13C and 15N
Stable isotope data from the five filter-feeding fish were used to characterize trophic structure
and potential resource competition among filter-feeding fish in the Lower Missouri River.
Among them bighead and silver carp are considered invasive and the other three (gizzard
shad, bigmouth buffalo and paddlefish) are native to the Lower Missouri River (Table 1). We
only obtained sufficient samples of silver carp and gizzard shad to explore the difference and
similarity of δ13C and δ15N across all locations. Results indicate that the relative proportions of
δ13C and of δ15N for silver carp and gizzard shad collected from 2 to 3 river sections do not
show significant difference within each species. Therefore, all data from same species collected
from different locations were pooled for trophic niche analysis.
Trophic position of fish is estimated as TP = (δ15NF - δ15NB)/Δ δ15N+2, where δ15NF is the
mean δ15N value of a fish species, δ15NB is the mean δ15N value of the baseline organism
which is pink papershell in this analysis (S1 Table). Δ δ15N is the nitrogen stable isotope
fractionation factor per trophic transfer during animal feeding. We used the mean value of 3.4½
reported by Minagawa and Wada [
]. The trophic level of pink papershell is 2 (primary
All data were tested for normality (Shapiro-Wilk test) before further statistical analysis (α =
0.05 in all cases). Kruskal-Wallis One Way Analysis of Variance on Ranks was used to detect
differences between species. Except for R Bayesian analysis, all other statistical analyses were
performed in Sigma Plot 13. (Systat Software, Inc, San Jose, CA). Five population niche metrics
derived from stable isotope data were used to evaluate trophic structure of the invasive and
native filter-feeding fish during this study. These metrics were adapted from community wide
metrics proposed by Layman [
] and were calculated using the Bayesian approach in R21.
The six niche metrics are measures of the total extent of spacing and trophic redundancy
within a δ13C and δ15N bi-plot for community or species. The δ13C range (CRB) is the
difference between the individuals with the most enriched and most depleted δ13C values and is a
measure of basal resource diversity. The δ15N range (NRB) is the difference between the
species with the most enriched and most depleted δ15N values and is a measure of trophic length
within a population. The total area (TA) of the δ13C and δ15N bi-plot space describes the total
space occupied by a population and was calculated using the standard Ellipse Area (SEAB).
4 / 13
The mean distance to the δ13C- δ15N centroid (CDB) provides a measure of trophic diversity.
The mean nearest neighbor distance (MNNDB) is the mean of the Euclidean distances to each
species' nearest neighbor in bi-plot space and thus a measure of the overall density of species
packing. Small MNNDB suggests increased trophic redundancy. Finally, the standard
deviation of nearest neighbor distance (SDNNDB) is a measure of the evenness of species packing
in bi-plot space. Low SDNNDB values mean more even distribution of trophic niches.
To measure the trophic niche size and to test whether trophic niche overlap were not
equivalently weighted among species, we used a probabilistic method developed by Swanson et al.
]. The method measures a given 95% (or user-defined α) probability niche size and
provides directional estimates of pairwise niche overlap in multivariate space. Swanson et al. [
defined the niche overlap of species A onto species B as the fraction of the intersection area
between niche A and niche B over the total niche area of B and vice versa. We used a 95%
probability niche size and overlap for results and discussion.
A total of 104 fish belonging to the five species were collected from the lower Missouri River
between the confluence of the Lamine River, nine river km upstream of Boonville, Missouri
and the confluence of the Osage River, 22 km downstream of Jefferson City, Missouri or
within those two tributaries, near their confluences with the Missouri (S1 Table). Sample size
and mean δ13C and δ15N values of each fish species can be found in Table 1. Silver carp,
bighead and paddlefish shared similar size range followed by bigmouth buffalo and gizzard shad
which had the smallest size as adults among the five filter feeders (Table 1). The δ15N values
differed significantly among species (Kruskal-Wallis One-way ANOVA, H = 19.79, df = 4,
p<0.001). The highest mean value was found in paddlefish and the lowest in gizzard shad
(Table 1). The δ13C values also differed significantly among species (Kruskal-Wallis One-way
ANOVA, H = 48.77, df = 4, p<0.05). The highest mean value was found in gizzard shad and
the lowest in paddlefish (Table 1).
δ15N in four of the five species spanned a range (NRB) greater than the magnitude of the
average isotope fractionation (3.4½) per trophic transfer [
], indicating that some individuals of
each species differed by one full trophic level (Table 2). Trophic position was lowest for gizzard
shad (2.6) and highest for paddlefish (3.5) with an average of 3.1 for all species studied
(Table 2). The δ13C in each species spanned a range (CRB) from 3.7 to 4.9½ which is over
10-fold greater than the isotope fractionation (0.4½) during each trophic transfer [
CRB among species appeared more uniform than trophic length, with smallest CRB in
bigmouth buffalo and greatest in silver carp.
All species except for bigmouth buffalo shared similar niche space size (SEAB; Table 2 and
Fig 2). Bigmouth buffalo had a much smaller niche space. As the result of small NRB and CRB,
Fig 2. Dual stable isotope plot and 95% Bayesian standard ellipses (SEAB) of total trophic area for two invasive
carps and three native fishes from the lower Missouri River. Please refer to Table 1 for species codes.
bigmouth buffalo had the lowest trophic diversity (CDB). Paddlefish possessed the greatest
NRB and one of the highest CRB, and also displayed the highest CDB, higher MNNDB (low
trophic redundancy) and SDNNDB (low trophic evenness) than other fish. CDB for other
species other than bigmouth buffalo varied slightly. MNNDB and SDNNDB were nearly identical
for all species except paddlefish (Table 2).
Population niche overlap
There are various degrees of trophic overlap between species and between invasive and native
species with an overall average of 54% (Fig 3). High trophic overlaps (over 90%) are all
involved with one of the invasive carp. The highest trophic overlap is found between silver
carp and bigmouth buffalo (94.1%) and between bighead carp and bigmouth buffalo (93.6%)
followed by gizzard shad onto bighead carp (91.3%) and silver carp onto gizzard shed (90.6%).
The lowest trophic overlap between bigheaded carps and native fish is found between bighead
and paddlefish (26.8%) while overlap between silver carp and paddlefish is higher (35.4%).
Average trophic overlap between silver carp and native species was as high as 71%, greater
than trophic overlap between bighead and native fish (64%) (Fig 4).
Trophic overlap between native fish averaged 31%, which is considerably lower than
overlap between bigheaded carp and native fish, which averaged 67.7% (Fig 4) largely because of
the different trophic space of paddlefish. The overlap between paddlefish and bigmouth
buffalo, and between paddlefish and gizzard shad are 7.2% and 33.0%, respectively. However,
6 / 13
Fig 3. Probabilistic niche overlap (%) for a standard eclipse niche space (NR) of 95%. The means and 95% intervals are
displayed in green. Please refer to Table 1 for species codes.
trophic overlap between gizzard shad and bigmouth buffalo was as high as 88.0%. The
Bayesian approach provided by Swanson et al. [
] allowed evaluation of species interactions for
trophic overlap. The effects of trophic overlap by bigheaded carp on native fish were on average
stronger than the effects of overlap by native fish (Fig 4). For example, trophic overlap of
bighead carp onto bigmouth buffalo was 93.6% while the reverse was only 46.8%. High overlap in
both directions was found between silver carp and gizzard (90.6 and 88.3% respectively). On
the other hand, there were also cases in which native fish posed greater overlap onto bigheaded
carps. The trophic overlap between bighead and gizzard shad was high but the effect of gizzard
shad on bighead carp was slightly greater than the effect of bighead carp on gizzard shad. This
also occurred in the interaction between bighead carp and paddlefish, although effects in both
directions were minimal. However, the trophic overlap by silver carp onto native fish was all
greater than the overlap from native fish (Fig 4).
This study revealed potentially high degree of trophic overlap between two bigheaded carps
and three native filter-feeding fish in the Lower Missouri River. The probabilistic method for
trophic overlap analysis developed by Swanson et al. [
] allows evaluation of species A onto
species B or vice versa. Higher degrees of trophic overlap by both species of bigheaded carps
with native fish (Fig 4) indicate that bigheaded carps were more competitive and aggressive in
7 / 13
Fig 4. Average trophic overlap interactions of invasive and native fishes from the lower Missouri River. Please refer
to Table 1 for species codes.
resource use than the native fish when resources are limiting. These findings provide
additional insights of biological invasion ecology and management of invasive fish in US rivers.
The five species collected in this study have been reported to move long distances in US
rivers [38±41], much longer than the distance between our sampling points, which may integrate
the stable isotope signals of the natural resources used during their feeding movement. Our
results are based on data collected in a single season during the study period. Since stable
isotope signals in large fish reflect feeding and growth over a multiple year period, seasonal
changes in dietary isotope signals have been incorporated into fish tissues and reveal the use of
natural resources during their growth period. Annual collection of fish samples on a multiple
year scale may reveal long-term changes in environmental conditions, use of natural resources,
niche characteristics and trophic overlap between native and invasive fish [
18, 24, 42
Trophic metrics derived from dual stable isotope analysis may provide novel ways of
quantifying interactions among populations in aquatic food webs [
]. Except for bigmouth
buffalo, the trophic niche space, trophic diversity, individual trophic packing and redundancy for
all species was similar. Similarly, Hill et al.  also found isotope metrics of the invasive fish
were similar to or consistently mid-range in comparison with their native counterparts in the
8 / 13
Nseleni River, South Africa. Resource competition depends largely on the intensity of trophic
overlap between species and resource abundance. The resources available for water column
filter feeders are limited to plankton and detritus in freshwaters. Bigheaded carps are well
established in Missouri River [
] and are likely capable of fully utilizing the available natural
resources. The similarity of trophic niche space between invasive and native fish in the Lower
Missouri River would suggest that the two bigheaded carps were highly competitive, assuming
a limited resource. Decrease in condition of gizzard shad in the Missouri River [
] since the
invasion suggests that the planktonic food resource is now limiting. In addition, extremely
rapid growth rates of bighead and silver carp in the Mississippi and Illinois Rivers were
reported early in the invasion [
], but growth rates and condition factors have declined as the
number of bigheaded carp has increased [
]. This is a likely indication of intraspecific or
intrageneric competition, and thus of a limited resource in those nearby rivers, which are
characterized by greater chlorophyll concentrations and higher planktonic productivity than the
Missouri River [
]. However, without the knowledge of the trophic niche size of the native
fish prior to the invasion of the carps, it is impossible to know if the current niche size has
changed and is the result of resource competition with the bigheaded carps.
In other locations, silver carp has been found to depend on both phytoplankton and
zooplankton while bighead carp is largely a zooplankton feeder [47±49]. Our estimates of trophic
position for silver carp and bighead carp also confirmed their dietary preference in the lower
Missouri River. The high trophic overlap between silver carp and bighead carp found in this
study is supported by studies elsewhere [
]. The SEAB occupied by both carps essentially
encompassed the entire niche space occupied by bigmouth and gizzard shad. The greater
SEAB in silver carp resulted from their greater use of both primary and secondary trophic level
resources than bighead carp, and is reflected in its higher trophic overlap with native species
than bighead carp.
The least trophic overlap was found between paddlefish and other filter-feeding fish
including the two bigheaded carp. This finding is consistent with that reported by Sampson et al.
] who found clear diet dissimilarity between the two bigheaded carp and paddlefish.
Paddlefish displayed the lowest δ13C and highest δ15N among fish, indicating that they used a
portion of resources with higher trophic position than those used by carp. Schrank et al. [
reported negative effect on young paddlefish growth when held in ponds with young bighead
carp. However, an examination of existing historic and more recent Missouri River paddlefish
length/weight data from several sources did not identify a decrease in condition of paddlefish
after the invasion of bighead and silver carp (Chapman, unpublished data). Gizzard shad did
decrease in condition over a similar period [
]. Our data indicate that paddlefish can take
advantage of Missouri River food resources with a higher trophic position than those
consumed strongly by bighead carp and silver carp. If those higher trophic level foods were not
available in the pond study by Schrank et al. [
], it would explain why the interaction in that
study between bighead carp and paddlefish was detrimental to paddlefish. Sampson et al. [
also found that paddlefish had a higher trophic position and less overlap with bighead carp or
silver carp than the other native filter feeders in Illinois River backwaters. Paddlefish is listed
as a species of special concern by US Fish and Wildlife Service [
], thus it is important to
further study the trophic overlap between bighead carp, silver carp and Paddlefish under various
growth stages and environmental conditions.
Gizzard shad is capable of feeding benthically and also filter-feeding on seston. Their diets
include various plankton and large amount of detritus [
]. In this study, gizzard shad showed
resource diversity and niche space similar to the invasive carp, but their trophic level is the
lowest (2.5), which suggested that they are omnivores depending on both primary and
secondary consumers in the Lower Missouri River. Therefore, shad displayed greater trophic overlap
9 / 13
with silver carp than bighead carp, and this overlap is potentially responsible for the decline in
gizzard shad condition [
] after the carp invasion.
Trophic overlap between paddlefish and other two native filter feeders was very small. This
is not surprising because a community inhabiting in the same ecosystem must develop niche
separation to avoid resource competition. This could be accomplished by using different
resources and positioning at different trophic levels. For example, by using basal resources
depleted in δ13C, paddlefish distanced themselves in SEAB from all other species. The niche
space of bigmouth buffalo fell nearly completely within that of shad, while a large portion of
gizzard shad's niche space was located outside that of bigmouth buffalo, indicating high
overlap by shad onto bigmouth buffalo but low overlap by bigmouth buffalo onto gizzard had.
Bigmouth buffalo displayed smallest resource and trophic ranges, and trophic diversity than other
species and occupied a narrow niche within the niche space occupied by both bigheaded carps
in the lower Missouri River. Hence, their overlap was greatest among the filter feeding species
community. Differences in isotopic niche among these fish appear to result from their
differences in feeding habitats as discussed above.
Ecological effects of invasive fish, including silver carp and bighead carp, on native
communities have also been reported elsewhere [
]. However, because of the difficulties in
providing replication or controls, and in working in such large and variable systems, little
research has been performed that can validate the predictions  and perception [
undesirable effects on native species or link observed effects on native species [
] to the carp
invasion. Our results show trophic overlap between the invasive and native filter feeding fishes
especially for gizzard shad and bigmouth buffalo, and thus provide support for the hypothesis
that bighead carp and silver carp have undesirable effects on native species in the Lower
Missouri River. With the recent rapid increases in abundance of bighead and silver carp in the
Mississippi River system [
], our data indicate a potential threat to biodiversity and to
recreational and commercial fisheries in the major rivers of the United States.
S1 Table. Stable isotope data for fish and invertebrates from the lower Missouri River.
Disclaimer: Any use of trade, firm, or product names is for descriptive purposes only and does
not imply endorsement by the U.S. Government.
We appreciate Joseph E. Deters for collecting invertebrates and fish samples. Xin Li for
stable isotope analysis. Data analysis and manuscript preparation were supported by National
Natural Science Foundation of China (grant No. 51179094 and 30700091) to JW and (grant
No. 41376158) to BG. The data set for this project has been archived by the U.S. Geological
Conceptualization: Jianzhu Wang, Duane Chapman, Binhe Gu.
Data curation: Duane Chapman, Jun Xu, Yang Wang, Binhe Gu.
Formal analysis: Jun Xu.
Funding acquisition: Duane Chapman, Binhe Gu.
Investigation: Duane Chapman.
10 / 13
Methodology: Yang Wang.
Project administration: Duane Chapman.
Visualization: Jun Xu.
Writing ± original draft: Jianzhu Wang, Binhe Gu.
Writing ± review & editing: Duane Chapman, Jun Xu, Yang Wang, Binhe Gu.
11 / 13
12 / 13
1. Lindeman RL ( 1942 ) The trophic-dynamic aspect of ecology . Ecology 23 : 399 ± 417 .
2. Montoya JM , Pimm SL , SoleÂ RV ( 2006 ) Ecological networks and their fragility . Nature 442 : 259 ± 264 . https://doi.org/10.1038/nature04927 PMID: 16855581
3. Polis GA , Strong DR ( 1996 ) Food web complexity and community dynamics . American Naturalist 147 : 813 ± 846 .
4. Peterson BJ , Fry B ( 1987 ) Stable isotopes in ecosystem studies . Annual Review of Ecology and Systematics 18 : 293 ± 320 .
5. Minagawa M , Wada E ( 1984 ) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age . Geochimica et Cosmochimica Acta 48 : 1135 ± 1140 .
6. Fry B ( 1991 ) Stable isotope diagrams of freshwater food webs . Ecology 72 : 2293 ± 2297 .
7. Kling GW , Fry B , O'Brien WJ ( 1991 ) Stable isotopes and planktonic trophic structure in arctic lakes . Ecology 73 : 561 ± 566 .
8. Rau G ( 1978 ) Carbon-13 depletion in a subalpine lake: carbon flow implications . Science 201 ( 4359 ): 901 ± 902 . https://doi.org/10.1126/science.201.4359.901 PMID: 17729568
9. Post DM ( 2002 ) Using stable isotopes to estimate trophic position: models, methods, and assumptions . Ecology 83 : 703 ± 718 .
10. Vander Zanden MJ , Casselman JM , Rasmussen JB ( 1999 ) Stable isotope evidence for the food web consequences of species invasions in lakes . Nature 401 : 464 ± 467 .
11. Gu B , Schelske CL , Hoyer MV ( 1996 ) Stable isotopes as indicators of diet and trophic structure of the fish community in a shallow hypereutrophic lake . Journal of Fish Biology 49 : 1233 ± 1243 .
12. Abrantes K , Sheaves M ( 2009 ) Food web structure in a near-pristine mangrove area of the Australian Wet Tropics . Estuarine and Coastal Shelf Science 82 : 597 ± 607 .
13. Bearhop S , Adams CE , Waldron S , Fuller RA , MacLeod H ( 2004 ) Determining trophic niche width: a novel approach using stable isotope analysis . Journal of Animal Ecology 73 : 1007 ± 1012 .
14. Newsome SD , Yeakel JD , Wheatley PV , Tinker MT ( 2012 ) Tools for quantifying isotopic niche space and dietary variation at the individual and population level . Journal of Mammalogy 93 : 329 ± 341 .
15. Layman CA , Arrington DA , Montaña CG , Post DM ( 2007 ) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88 : 42 ± 48 . PMID: 17489452
16. Cooper RN , Wissel B. ( 2012 ) Loss of trophic complexity in saline prairie lakes as indicated by stable-isotope based community-metrics . Aquatic Biosystems 8 : 6 . https://doi.org/10.1186/2046-9063-8-6 PMID: 22480379
17. Layman CA , Quattrochi JP , Peyer CM , Allgeier JE ( 2007 ) Niche width collapse in a resilient top predator following ecosystem fragmentation . Ecology Letters . 10 : 937 ± 944 . https://doi.org/10.1111/j.1461- 0248 . 2007 . 01087 . x PMID : 17845294
18. Delong MD , Thorp JH , Thoms MC , McIntosh LM ( 2011 ) Trophic niche dimensions of fish communities as a function of historical hydrological conditions in a Plains river . River Systems 19 : 177 ± 187 .
19. CoÂrdova-Tapia F , Contreras M , Zambrano L ( 2015 ) Trophic niche overlap between native and nonnative fishes . Hydrobiologia 746 : 291 ± 301 .
20. Jackson AL , Inger R , Parnell AC , Bearhop S ( 2011 ) Comparing isotopic niche widths among and within communities: SIBER±Stable Isotope Bayesian Ellipses in R . Journal of Animal Ecology 80 : 595 ± 602 . https://doi.org/10.1111/j.1365- 2656 . 2011 . 01806 .x PMID: 21401589
21. Jackson MC , Donohue I , Jackson AL , Britton JR , Harper DM , Grey J ( 2012 ) Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology . PloS One 7 ( 2 ): e31757. https://doi.org/10.1371/journal.pone. 0031757 PMID: 22363724
22. Abrantes KG , Barnett A , Bouillon S ( 2014 ) Stable isotope-based community metrics as a tool to identify patterns in food web structure in east African estuaries . Functional Ecology 28 : 270 ± 282 .
23. Jackson MC , Britton JR , Cucherousset J , Guo Z , Stakėnas S , Gozlan RE , Copp GH ( 2016 ) Do nonnative pumpkinseed Lepomis gibbosus affect the growth, diet and trophic niche breadth of native brown trout Salmo trutta? Hydrobiologia 772 : 63 ± 75 .
24. Guzzo MM , Haffner GD , Legler ND , Rush SA , Fisk AT ( 2013 ) Fifty years later: trophic ecology and niche overlap of a native and non-indigenous fish species in the western basin of Lake Erie . Biological Invasions 15 : 1695 ± 1711 .
25. Spurgeon JJ , Paukert CP , Healy BD , Kelley CA , Whiting DP ( 2015 ) Can translocated native fishes retain their trophic niche when confronted with a resident invasive? . Ecology of Freshwater Fish 24 : 456 ± 466 .
26. Herborg L , Mandrak NE , Cudmore B , MacIsaac HJ ( 2007 ) Comparative distribution and invasion risk of snakehead (Channidae) and Asian carp (Cyprinidae) species in North America . Canadian Journal of Fisheries and Aquatic Sciences . 64 : 1723 ± 1735 .
27. Kolar CS , Chapman DC , Courtenay WR , Housel CM , Williams JD , Jennings DP ( 2007 ) Bigheaded Carps: A Biological Synopsis and Environmental Risk Assessment . American Fisheries Society Special Publication 33 : 208 .
28. Zhang X , Xie P , Huang X ( 2008 ) A review of nontraditional biomanipulation . The Scientific World Journal 8 : 1184 ± 1196 . https://doi.org/10.1100/tsw. 2008 .144 PMID: 19082415
29. Sass GG , Hinz C , Erickson AC , McClelland NN , McClelland MA , et al ( 2014 ) Invasive bighead and silver carp effects on zooplankton communities in the Illinois River, Illinois, USA . Journal of Great Lakes Research 40 : 911 ± 921 .
30. Sanderson BL , Tran CD , Coe HJ , Pelekis V , Steel EA , et al ( 2009 ) Nonlethal sampling of fish caudal fins yields valuable stable isotope data for threatened and endangered fishes . Transactions of the American Fisheries Society 138 : 1166 ± 1177 .
31. Ridenour CJ , Finley J , Hill TD ( 2008 ) Trends in gizzard shad population abundance and body condition from side-channel chutes of lower Missouri River within Big Muddy National Wildlife Refuge , 1997 ± 2007. U.S. Fish and Wildlife Service , Region 3, Data Series FDS- 2008-3 .
32. Irons KS , Sass GG , McClelland MA , Stafford JD ( 2007 ) Reduced condition factor of two native fish species coincident with invasion of non-native Asian carps in the Illinois River, U.S.A. Is this evidence for competition and reduced fitness ? Journal of Fish Biology 71 ( Supplement D ): 258 ± 273 .
33. Haupt KJ , Phelps QE ( 2016 ) Mesohabitat associations in the Mississippi River Basin: a long-term study on the catch rates and physical habitat associations of juvenile silver carp and two native planktivores . Aquatic Invasions 11 : 93 ± 99 .
34. Pendleton RM , Schwinghamer C , Solomon LE , Casper AF ( 2017 ) Competition among river planktivores: are native planktivores still fewer and skinnier in response to the silver carp invasion? Environmental Biology of Fishes 100 : 1213 ± 1222 .
35. Schrank SJ , Guy CS , Fairchild JF ( 2003 ) Competition interactions between age-0 bighead carp and paddlefish . Transactions of the American Fisheries Society 132 : 1222 ± 1228 .
36. Swanson HK , Lysy M , Power M , Stasko AD , Johnson JD , Reist JD ( 2015 ) A new probabilistic method for quantifying n-dimensional ecological niches and niche overlap . Ecology 96 : 318 ± 324 . PMID: 26240852
37. Pflieger WL ( 1997 ) The fishes of Missouri . Missouri Department of Conservation. Jefferson City, Missouri, USA.
38. Clifford TJ ( 1969 ) Summer movements of bigmouth buffalo in Lake Poinsett, South Dakota . South Dakota State University, MS Thesis. 34 p. (http://openprairie .sdstate.edu/etd).
39. Degrandchamp KL , Garvey JE , Colombo RE ( 2008 ) Movement and habitat selection by invasive Asian carps in a large river . Transactions of the American Fisheries Society 137 : 45 ± 56 .
40. Zeug SC , Peretti D , Winemiller KO ( 2009 ) Movement into floodplain habitats by gizzard shad (Dorosoma cepedianum) revealed by dietary and stable isotope analyses . Environmental Biology of Fishes 84 : 307 ± 314 .
41. Zigler SJ , Dewey MR , Knights BC , Runstrom AL , Steingraeber MT ( 2003 ) Movement and habitat use by radio-tagged paddlefish in the upper Mississippi River and tributaries . North American Journal of Fisheries Management 23 : 189 ± 205 .
42. Perkin JH , Bonner TH ( 2011 ) Long-term changes in flow regime and fish assemblage composition in the Guadalupe and San Marcos rivers of Texas. River Research and Applications 27 : 566 ± 579 .
43. Hill JM , Jones RW , Hill MP , Weyl OL ( 2015 ) Comparisons of isotopic niche widths of some invasive and indigenous fauna in a South African river . Freshwater Biology 60 : 893 ± 902 .
44. Nuevo M , Sheehan RJ , Heidinger RC ( 2004 ) Accuracy and precision of age determination techniques for Mississippi River bighead carp Hypophthalmichthys nobilis (Richardson 1845) using pectoral spines and scales . Archiv fuÈr Hydrobiologie 160 : 45 ± 56 .
45. Irons KS , Sass GG , McClelland MA , O'Hara TM ( 2011 ) Bigheaded carp invasion of the La Grange Reach of the Illinois River: insights from the Long Term Resource Monitoring Program . In: Chapman DC , Hoff MH , editors. Invasive Asian Carps in North America. Bethesda , Maryland: American Fisheries Society.
46. Knowlton MF , and Jones JR ( 2000 ) Seston, Light, Nutrients and Chlorophyll in the Lower Missouri River , 1994 ±1998 : Journal of Freshwater Ecology 15 : 283 ± 297 .
47. Chen G , Wu Z , Gu B , Liu D , Li X , Wang Y ( 2011 ) Isotopic niche overlap of two planktivorous fish in southern China . Limnology 12 : 151 ± 155 .
48. Dong S , Li D ( 1994 ) Comparative studies on the feeding selectivity of silver carp Hypophthalmichthys molitrix and bighead carp Aristichthys nobilis . Journal of Fish Biology 44 : 621 ± 626 .
49. Xie P ( 1999 ) Gut contents of silver carp, Hypophthalmichthys molitrix, and the disruption of a centric diatom, Cyclotella, on passage through the esophagus and intestine . Aquaculture 180 : 295 ± 305 .
50. Sampson SJ , Chick JH , Pegg MA ( 2009 ) Diet overlap among two Asian carp and three native fishes in backwater lakes on the Illinois and Mississippi rivers . Biological Invasions 11 : 483 ± 496 .
51. Chick JH , Pegg MA ( 2001 ) Invasive carp in the Mississippi River basin . Science 292 : 2250 ± 2251 . PMID: 11424944
52. Baker CD , Schnitz EH ( 1971 ) Food habits of adult gizzard shad and threadfin shad in two Ozark reservoirs . In: Hall GE, editor. Reservoir fisheries and limnology. Special publication #8 . Bethesda , Maryland: American Fisheries Society. pp. 3 ± 11 .
53. Normile D ( 2004 ) Expanding trade with China creates ecological backlash . Science 306 : 968 ± 969 . https://doi.org/10.1126/science.306.5698.968 PMID: 15528424
54. Xie P , Chen Y. ( 2001 ) Invasive carp in China's plateau lakes . Science 294 : 999 ± 1000 .
55. Asian Carp Working Group ( 2007 ) Management and control plan for bighead, black, grass, and silver carps in the United States . Washington, D.C.: Asian Carp Working Group, Aquatic Nuisance Species Task Force . 223 p.