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Functional Ecology. 2017;1–10. wileyonlinelibrary.com/journal/fec
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© 2017 The Authors. Functional Ecology
© 2017 British Ecological Society
Received:9August2016
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Accepted:17May2017
DOI: 10.1111/1365-2435.12922
STANDARD PAPER
A response- surface examination of competition and facilitation
between native and invasive juvenile fishes
Kirsten A. Nelson1,2 | Scott F. Collins1 | Greg G. Sass2 | David H. Wahl1,2
1Illinois Natural History Survey, Kaskaskia
Biological Station, Sullivan, IL, USA
2Illinois Natural History Survey, University of
IllinoisChampaign-Urbana,Champaign,IL,
USA
Correspondence
Scott F. Collins
Email: collscot@illinois.edu
Present address
GregG.Sass,WisconsinDepartmentof
Natural Resources, Boulder Junction, WI, USA
HandlingEditor:DustinMarshall
Abstract
1. Ecologicaltheoryhaslongrecognisedtheimportanceofpositiveandnegativespe-
cies interactions as drivers of food web structure, yet many studies have only fo-
cused on competition. Because competitive and facilitative mechanisms operate
simultaneously, but through different food web pathways, the balance of their
combinedeffectscanproducecomplexandvariableresponses.
2. Weusedaresponse-surfaceexperimentaldesigntoassesstherolesofnegative
(e.g.intra-,interspecificcompetition)andpositive(e.g.facilitation)interactionsbe-
tween native and invasive juvenile fishes. We tested whether these interactions
alterthedensitiesof planktonicandbenthicinvertebratesto evaluatethe magni-
tudeandmechanism(s)influencingtheacceptanceorresistanceofbiologicalinvad-
ers. Interactions between bighead carp (Hypophthalmichthys nobilis) and bluegill
(Lepomis macrochirus) or common carp (Cyprinus carpio) were evaluated in
mesocosms.
3. Intraspecific interactions were 1.5–2.4 times stronger than interspecific interac-
tionsbetweencarpspecies.Theonlyinstanceofinterspecificcompetitionresulted
inbigheadcarpreducingthedailygrowthofbluegill,whereasthereciprocalinter-
action resulted in facilitation. Facilitation occurred when bluegill increased the daily
growth of low density bighead carp treatments, despite increased numbers of
fishes.BigheadcarpalsoincreaseddensitiesofbenthicChironomidaelarvae,which
were subsequently consumed by bluegill, but did not result in enhanced bluegill
growth.Thesesuitesofinteractionswerenotobservedbetweencommonandbig-
headcarp.
4. Ourresponse-surface designprovedusefulfor comparingtherelative magnitude
of intra- vs. interspecific competition, identifying facilitation among species, and
tracing attendant effects on invertebrate communities. By accounting for the direc-
tionalityofinteractionswithinourexperimentalframeworkandtrackingresponses
ofpreyatlowertrophiclevels,weprovideaclearerunderstandingofhowcompeti-
tive effects and stressed consumers alter prey communities and influence
facilitation.
KEYWORDS
bigheadcarp,bluegill,commoncarp,invasionmeltdownhypothesis,invasivespecies,
planktivory,zooplankton
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Functional Ecology
NELSON Et aL.
1 | INTRODUCTION
Understandingtheoutcomesofspeciesinteractionshasbeenfunda-
mental in describing why certain organisms thrive while others falter.
Ecologicaltheoryhaslongrecognisedtheimportanceofpositiveand
negativespeciesinteractionsasdriversoffoodwebstructure(Bruno,
Stachowicz, & Bertness, 2003). However, processes such as com-
petition and predation typically receivemore attention than others
likefacilitation,althoughthis disparityis diminishing(e.g.Bertness&
Callaway,1994;Michalet& Pugnaire,2016;Simberloff &VonHolle,
1999).Because competitiveand facilitativemechanismscan operate
simultaneously through unique food webpathways, the balance of
theircombinedeffectsoftenproducescomplexandvariableresponses
(Callaway&Walker,1997).
Experimentalassessments ofspeciesinteractionshavelongused
additive and substitutive frameworks (reviewed in Connell, 1983;
Connolly,1986; Gibson, Connolly, Hartnett, & Weidenhamer, 1999;
Goldberg & Barton, 1992; Gurevitch, Morrow, Wallace, & Walsh,
1992). More recently, response-surface designs have been used,
which manipulate species across a range of differingdensities (e.g.
Inouye,2001).Aresponse-surfacedesignis ideal forevaluating spe-
ciesinteractionsbecause itallows fortheappraisal ofthemagnitude
of intra- and interspecific interactions between species (Forrester,
Evans,Steele,&Vance,2006;Inouye,1999,2001).Thisexperimental
approachmay be particularly useful forthe study of biological inva-
sions, as the numbers of native and invasive organisms can vary greatly
acrossestablishedrangesandneartheperipheryofaninvasionfront.
Moreover, it can provide needed insight into the roles of negative
andpositivespeciesinteractionsandhowtheyshapecommunitiesof
organisms.
Globally, accidental or purposeful introductions of fishes into
aquatic ecosystems has greatly homogenised fish communities (Rahel
2002; Ricciardi & Kipp, 2008; Strayer & Dudgeon, 2010). Success
or failure ofa newly introduced fish (or anyorganism) may depend
onthesuite of negativeandpositive interactions an invaderexperi-
ences within a community and its associated habitat characteristics
(Rodriguez, 2006; Simberloff& VonHolle, 1999). If competition for
shared and limited resourcessufficiently stresses one or many spe-
cies, negative species interactions and attenuating effects on food
webstructuremayproducecomplexfeedbacksthatresultinpositive
effects for some organisms and additional negative effects for others
(e.g.Bertness&Callaway,1994).Predictingindirectecologicaleffects
can be difficult, and as a consequence, there is a poormechanistic
understanding of how species interactions might elicit feedbacks
withinpreycommunities thatresultinfacilitationofonefishspecies
by another.
We testedfor negative and positive interactions between juve-
nilebighead carp (Hypophthalmichthys nobilis),bluegill(Lepomis mac-
rochirus),andcommoncarp(Cyprinus carpio)intwoexperiments.Each
speciesiswidelydistributedacrosstheglobeandrepresentsanative
orexoticspeciestomanyfreshwaterenvironments.IntheMississippi
River Basin of North America, bluegill are a native centrarchid, whereas
commoncarpandbigheadcarpareinvasivecyprinids.Juvenilebluegill
andcommon carparefacultativeplanktivoresthatgenerallyfeedon
zooplankton,butalsoshifttobenthicinvertebratesthroughontogeny
(Britton etal. 2007; Spotte,2007). Bighead carp are obligate plank-
tivoresthat efficientlyfilterzoo- and phytoplankton (Kolar& Lodge,
2002; Sampson, Chick, & Pegg, 2009; Collins& Wahl, 2017). Using
replicated mesocosmexperiments, we quantified and compared the
magnitudesofthepercapitainfluenceofinter-andintraspecificcom-
petition,alongwith potential facilitation among juvenilebluegilland
bigheadcarp (Experiment 1) andjuvenilecommon and bigheadcarp
(Experiment2).Wealsoexaminedhowfishinteractionsinfluencedthe
structure of aquatic invertebrate communities. Because these fishes
consume similar preyresources, we predicted that strong competi-
tionwould produce a stressful environmentfor one or both species
withineachexperiment.Hence,ourstudyteststhegeneralhypothesis
thatintensecompetitionforprey resourcescreates a stressed envi-
ronment, with feedbacks within the food web that drive facilitation
betweenspecies.
2 | MATERIALS AND METHODS
2.1 | Study design and system
Response-surface designs have been used to examine the relative
roles of intra- and interspecific species interactions (e.g. Forrester
etal., 2006; Inouye, 1999); however, focus has largely been limited
to negative species interactions. Such studies have reasoned that
significantnegativeslopesgeneratedfrom statisticalmodelsindicate
thepresenceofcompetitionwithinorbetweenspecies(e.g.Forrester
etal., 2006). We extended this reasoning to account for positive
slopes,which we interpreted asthepresence of positive species in-
teractions, specifically facilitation within or between species. Here,
weusedaresponse-surfaceexperimentaldesigntotestfornegative
(intra-andinterspecificcompetition)andpositive(interspecific facili-
tation)effects between juvenile fishes in twoseparateexperiments.
Experiment 1 was conducted in August 2011 and used eight treat-
ments (1–8; n=5replicatespertreatment;seeFigure1)totestfor
positiveandnegativeinteractionsbetweenjuvenilebigheadcarpand
bluegill.WeconductedExperiment2duringAugust 2012 and used
ninetreatments(1–9;5replicatespertreatment;Figure1)totestfor
interactionsbetweenjuvenilebigheadcarpandcommoncarp.Growth
offisheswereevaluatedintheabsence(conspecific)orpresence(het-
erospecific)ofanotherspeciesthatalsovariedbylow(5fishpermes-
ocosm)andhigh(10fishpermesocosm)densities.Thus,combinations
ofnumbersoffishesweresymmetricalforeachexperiment.
Both experimentswere conducted in mesocosms (1,325-L poly-
ethylenetanks)attheSamParrBiologicalStation,Kinmundy,IL,USA.
MesocosmswereplacedundercoverandfilledwithwaterfromForbes
Lake, Kinmundy, IL, USA. Water was filtered through a 64 μm mesh net
topreventlarvalfishintroduction.Macrozooplanktonfromlocallakes
were collected and introduced to the mesocosms after two weeks and
thenallowedtopopulateforfourweeksbeforefishwereintroduced.
During these four-week periods during 2011 and 2012, conditions
werehomogenisedbyexchangingwateramongmesocosms.
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Functional Ecology
NELSON Et aL.
Age-1bluegillandage-0commoncarpwerecollectedfromnearby
source populations. We obtained age-0 bighead carp from Osage
Catfisheries,Inc., Missouri,USA.Bluegillandcommon carpdensities
werewithintherangeofnaturalsystemsandpreviousstudies(Carey&
Wahl,2010).Bigheadcarpdensitieswerematchedtothoseofbluegill
andcommoncarp.Totalfishbiomasswasheldconstantwithinlowand
high- density treatments. Initial lengths (±SD)of bluegill and bighead
carpwere66±6mmand76±1mmrespectively.Initiallengths(±SD)
ofbighead carpand common carpwere 56±6mmand50±16mm
respectively. During the firstweek of each experiment, mortalities
werereplacedwithsimilarlysizedfishes.
2.2 | Data collection and analyses
2.2.1 | Fish interactions
Fish lengths and weights (nearest mm, 0.1g) were recorded at the
start and end of each experiment and used to estimate mean daily
growth (length, mm/day; weight, g/day).Weusedlinearfixedmodels
to evaluate the net effect (positive or negative) of interactions be-
tweennativeandinvasivespeciesonmeanfishgrowth(e.g.Forrester
etal.,2006).Thefixedeffectmodelincludedbluegillandbigheadcarp
densities(Experiment 1) and common carp and bighead carp densi-
ties(Experiment 2) asfixedeffects (SAS 9.2;PROCMIXED). Due to
limited space, mesocosms were setup at two locations at the Sam
ParrBiologicalStation.Wedetected noeffectofmesocosmlocation
onfishgrowth(i.e.blockeffect)foreitherExperiment1(block;blue-
gill, F = 1.94, p=.28;bighead carp, F = 0.29, p=.60)or Experiment
2 (block; common carp, F = 0.11, p=.73; bighead carp, F = 1.64,
p=.21).Additionally,no interaction between block and densitywas
detectedforeither Experiment 1 (bluegill, F = 1.19, p = .29; bighead
carp, F = 0.24, p=.62) or Experiment 2 (common carp, F = 0.22,
p=.64; bighead carp, F = 0.38, p=.54).Slope coefficients (β) were
estimatedandusedtodescribethepercapitaeffects ofconspecifics
andheterospecificsonfishgrowthrates. Separatemodelswere con-
structedforeachspeciesandforeachresponsevariable.Errorswere
testedfornormality(Shapiro-Wilktest)andhomogeneityofvariance
(Brownand Forsythe’s Testfor Homogeneity ofVariance).We used
a log10transformationwhenresidualsfailedtomeettheassumptions
of ANOVA. The sign of β coefficients (+, −) and the significance of
conspecifics,heterospecifics, and their interactionswereused to in-
terpretwhethertheneteffectofspeciesinteractionsresultedinfacili-
tationorcompetitionbetweenspecies.Here,asignificantinteraction
termfrom the linear fixed effectmodelsindicates that the effect of
addingone individual ofeitherspecies depends uponthedensity of
the other species. When coefficients indicated a negative effect of
conspecificsand heterospecifics,andno statisticalinteractionswere
detected,comparisons ofthe relativemagnitudeof interspecificand
intraspecificinfluences on fishgrowthwere assessed astheratio of
theformertothelatter(Forresteretal.,2006).
2.2.2 | Limnological and invertebrate sampling
Within each mesocosm, water temperature (°C), dissolved oxygen
(mg/L), total phosphorus, chlorophyll-a, turbidity (nephelometric
units,NTU), phytoplankton,and zooplanktonwerecollected priorto
fish introduction and then weekly until the end of the experiment.
Total phosphorus concentrations in the water column were col-
lected (2×45ml subsamples per mesocosm) and determined using
thecolorimetric molybdenum blueascorbicacid method withaper-
sulfate digestion. Chlorophyll-a was obtained by filtering 100 ml of
water through glass fibre filters (0.7 μmporesize[Millipore,Billerica,
Massachusetts, USA]), extracting chlorophyll-a in 90% acetone for
24hr,and then measuring fluorescence using afluorometer(Turner
Design, model TD700). Zooplankton were sampled with a vertical
tubesampler (70mm diameter×0.4m long; 1.5L)andpreservedin
a10%buffered formalinandrose Bengalsolution.Oneachsampling
date,threetubesampleswerecollectedfromrandomlocationswithin
the mesocosm, combined, and filtered through a 20 μm mesh net
(Chick,Levchuk,Medley,&Havel,2010).Inthelaboratory,macrozoo-
planktonandrotiferswereseparatedbyfiltrationofsamplesthrough
55 and 20 μm mesh nets. Tests for changes in limnological condi-
tionsand inzooplanktonand rotiferdensitieswere conductedusing
repeated-measuresANOVA(SAS 9.2,PROCMIXED; Treatmentand
Time,fixedeffects)totestforoveralldifferencesbetweentreatments,
changesthroughtime,andfor potentiallagged effectsoftreatments
manifesting through time. Densities of benthic macroinvertebrates
werequantifiedbyplacingtwowhitetiles(116.6cm2 pertile) atthe
bottomof eachmesocosm.At theendof theexperiment, tiles were
removed from each mesocosm and macroinvertebrates were stored
in ethanol with rose Bengal, then identified and counted. Given the
durationoftheexperiment,onlyChironomidae(Order:Diptera)colo-
nisedmesocosmsinsufficientquantitiestotestforbenthicresponses.
Chironomidaedensitieswereevaluatedusingaone-wayANOVAwith
treatmentasthefixedfactor.Specificcomparisonsamongtreatment
FIGURE1 Experimentaldesignoftreatmentsfortheassessment
ofcompetition(intra-,inter-)andfacilitationamongjuvenilenative
andinvasivefishes.Theresponse-surfacedesignvariesthenumbers
offishes.Experiment1usedthisdesigntotestfortheeffectsof
bluegill (Lepomis macrochirus)andbigheadcarp(Hypophthalmichthys
nobilis)(Treatments1–8).Experiment2evaluatedtheeffectsof
commoncarp(Cyprinus carpio)andbigheadcarp(Treatments1–9).
Treatment9wasaddedtoExperiment2,butnotpartofExperiment1
Bighead carp density
Density of bluegill
or common carp
0510
0
5
10
1 4 5
2 6 8
3 7 9
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Functional Ecology
NELSON Et aL.
groupswereinvestigatedusingCONTRASTstatements.Log10 trans-
formations were applied to response variables when necessary to
satisfythe assumptionsofANOVA. Forall statisticalanalyses(linear
fixedeffect models, repeated measures ANOVA,one-wayANOVA),
significance was determined at p < .05.
3 | RESULTS
3.1 | Experiment 1: Test of competition and
facilitation between juvenile native bluegill and
invasive bighead carp
3.1.1 | Fish interactions
Juvenile bluegill growth decreased with increasing conspecific and
heterospecificdensity(Figure2a),indicatingthatthenumbersoffish
within a mesocosm was a major determinant of growth. The nega-
tive slopes and overlapping confidence intervals describing bluegill
growthindicatedinter-andintraspecificeffectsweresimilar(Table1).
Bigheadcarpgrowthwasunaffectedby densitiesof theirconspecif-
ics(Table1).However,lowdensitybigheadcarp treatments experi-
enced increased growth as densities of bluegill increased, indicating
thatlowdensitiesofbigheadcarpwerefacilitatedbybluegill(Table1;
Figure2b).Athighbigheadcarpdensities,growthofbigheadcarpwas
similarbetween0and5bluegilldensities(Figure2b).
3.1.2 | Invertebrates
Pronounced changes in total macrozooplankton density were ob-
served between treatments, through time, and with treatment effects
manifesting through time (Time, F4,123 = 80.48, p<.001; Treatment,
F7,31 = 8.83; p<.001; Treatment×Time, F28,23 = 5.06, p < .001;
Figure3a). The presence of the filter-feeding bighead carp greatly
reduced macrozooplankton densities below those observed in fish-
less controls (BHC vs. Control, F1,30 = 14.36, p<.001;Mixvs.Control,
F1,30 = 27.52, p<.001;Figure3a).Yet,densitiesofmacrozooplankton
didnotdifferbetweenbigheadcarponlytreatmentsandmixedspecies
(i.e.bluegill andbighead carp)treatments(BHC vs.MIX, F1,30 = 2.40,
p=.13), indicating bighead carp were the key driver of changes to
planktonicprey. Filter-feedingbybigheadcarpreduced totalmacro-
zooplanktonbelow treatments withthevisual-foraging bluegill (BLG
vs. BHC, F1,30 = 15.54, p<.001;BLG vs.Mix,F1,30 = 34.35, p<.001).
Within the macrozooplankton community, four of five zooplankton
taxawere greatly reduced inthepresenceof predatory fishes, each
contributing to the overall reduction in planktonic invertebrates
(Table2).
FIGURE2 Meandailygrowth(mm/day,
±1 SE)of(a)bluegill(Lepomis macrochirus)
and(b)bigheadcarp(Hypophthalmichthys
nobilis)fromExperiment1,and(c)common
carp(Cyprinus carpio)and(d)bigheadcarp
fromExperiment2.Foreachexperiment,
“low” and “high” refers to a fish density
offiveandtenfishpermesocosm,
respectively
Bighead carp density
0510
Daily growth (mm/day)
–0.2
–0.1
0.0
0.1
0.2
Bluegill density
0510
(a) (b)
–0.05
0.00
0.05
0.10
0.15
0.20
Common carp density
0510
Bighead carp density
0510
(c) (d)
Experiment 1: Native vs. invasive
Experiment 2: Invasive vs. invasive
Low Bluegill
High Bluegill
Low Bighead carp
High Bighead carp
Low Common carp
High Common carp
Low Bighead carp
High Bighead carp
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Functional Ecology
NELSON Et aL.
Small-bodied rotifersexhibited divergent responsestopredation
by bluegill and bighead carp (Treatment, F7,33 = 2.84, p=.02; Time,
F4,64 = 1.98, p=.11;Treatment×Time,F28,89 = 1.06, p=.40).Rotifers
in bluegill only treatments were similar to fishless controls indicating
limitedpredatoryeffects ofthesevisualforagersonsmall bodiedin-
vertebrates (BLG vs. Control, F1,30 = 1.65, p=.21). Densities of roti-
ferswereelevatedatgreaterbluegilldensities(Figure3b).Treatments
containingfilter-feedingbigheadcarpreducedrotiferdensitiesbelow
those observed in fishless controls (BHC vs. Control, F1,30 = 15.16,
p<.001)andbluegilltreatments(BLGvs.BHC,F1,30 = 16.44, p<.001).
Rotifer densities were similar between treatments containing bighead
carp(BHC vs.MIX,F1,30 = 0.11, p=.75), indicatingtheirpresenceas
the driver of rotifer reductions.
BenthicChironomidae(Order:Diptera)larvaewerethemostcom-
mon sessile taxa sampled from tiles at the end of the experiment.
Chironomidae densities were greatest in the sole presence of big-
headcarp(Treatment,F7,32 = 7.39, p=.021;Figure3c)and aboutten
timesgreaterwhencomparedtobluegillonlytreatments.Incontrast,
TABLE1 Summarystatisticsfromregressionmodelstestingforeffectsofconspecificandheterospecificdensity,andtheirinteraction,on
changes in length and biomass of juvenile bluegill (Lepomis macrochirus),bigheadcarp(Hypophthalmichthys nobilis),andcommoncarp(Cyprinus
carpio).DisplayedaremodelR2 values, regression coefficients (β),andp- values for an associated significance test (H0: β=0)foreachtermin
the model
Response
R²Intercept
βpβpβp
Experiment 1 Bluegill Bighead carp Interaction
Bluegill(g/day) .73 0.050 −0.006 <.001 −0.009 <.001 0.001 .001
Bluegill(mm/day) .56 0.150 −0.017 .002 −0.025 .002 0.003 .03
Bigheadcarp(g/day) .45 −0.008 0.006 .04 −0.001 .64 −0.001 .14
Bigheadcarp(mm/day) .45 0.014 0.024 .03 −0.003 .71 −0.003 .09
Response
R²Intercept
βpβpβp
Experiment 2 Common carp Bighead carp Interaction
Commoncarp(g/day) .36 0.031 −0.003 <.01 −0.002 .26 0.0001 .43
Commoncarp(mm/day) .50 0.254 −0.019 <.01 −0.008 .24 0.001 .51
Bigheadcarp(g/day) .27 0.027 −0.001 .30 −0.002 .05 0.0001 .51
Bigheadcarp(mm/day) .30 0.236 −0.011 .33 −0.018 .07 0.0006 .66
FIGURE3 Responseof
macrozooplankton,rotifer,andbenthic
Chironomidae invertebrates to the
varyingconfigurationsofconspecificand
heterospecificfishdensities.Experiment
1 tested for the effects of bluegill
(Lepomis macrochirus)andbigheadcarp
(Hypophthalmichthys nobilis)(Treatments
1–8).Experiment2testedtheeffectsof
commoncarp(Cyprinus carpio)andbighead
carp(Treatments1–9).Diametersof
bubble-plotsrepresenttheexperimental
mean and letters (w, x, y, z)represent
treatment differences within each
respectivepanel
0
5
10
0
5
10
0
5
10
0510
0
5
10
0510
Bighead carp density
Bluegill densityCommon carp density
100 200 400Scale
(a) (b)
(d)
0
5
10
(c)
(e) (f)
0.08 0.42 0.85Scale
panels: a, b, d, e
panel: c
# L–1 # cm–2
xyz
x
xy
z
zz
zyz
xy
xy
xz
zz
zyz
xyxyz
yz yz
yz
z
z
w
xy
xyz
xyz
xy
yz yz
z
xy
xy
xy xyx
x
yy
y
0
5
10
0510
Macrozooplankton Rotifers Benthic Chironomidae
6
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Functional Ecology
NELSON Et aL.
Chironomidae densities solely within bluegill treatments were similar
tomixedspeciestreatments(Figure3c).
3.1.3 | Limnological conditions
Limnological conditions (e.g. temperature, dissolved oxygen) were
similar between treatments (Table2). Although these metrics did
vary through time, no treatment effects manifested through time,
exceptforturbiditywhichwaslowinfishlesscontrolswithhighden-
sitiesof zooplanktonand elevatedin mesocosmswithfishes atthe
conclusionoftheexperiment(Table2).Chlorophyll-a concentrations
weresimilaramongtreatments(Treatment;F7,32 = 1.14; p=.36),but
decreased through time (Time; F4,28 = 15.07; p<.001), with con-
centrations 3 to 5+ times greater in treatments with fishes relative
to fishless controls (Treatment×Time; F28,57 = 2.01; p=.01). Total
phosphorus concentrations varied over time (Time; F4,123 = 4.83;
p<.001); however, concentrations did not vary between treat-
ments(Treatment; F7,36 = 1.05; p=.41) and no specific treatments
showedincreasedconcentrationsthroughtime(Treatment×Time;
F28,122 = 0.86; p=.67).
TABLE2 Resultsfromrepeated-measuresANOVAtestingforchangesinbiotic(phytoplankton,invertebrates)andabiotic(temperature,
dissolvedoxygen,turbidity,totalphosphorus)variablesinresponsetothepresenceofbigheadcarp(Hypophthalmichthys nobilis)andbluegill
(Lepomis macrochirus;Experiment1)andbigheadcarpandcommoncarp(Cyprinus carpio;Experiment2)
Response Effect
Experiment 1 Experiment 2
df F p df F p
Biotic Chlorophyll-a Treatment 7 1.14 .36 8 1.38 .24
Time 4 15.07 <.0001 4 50.6 <.0001
Treatment×Time 28 2.01 .01 32 2.42 <.0001
Cyclopoid Treatment 7 4.12 .003 8 1.72 .13
Time 4 8.84 <.0001 4 54.54 <.0001
Treatment×Time 28 3.5 <.0001 32 1.35 .12
Nauplii Treatment 7 8.6 <.0001 8 11.57 <.0001
Time 4 103.76 <.0001 4 77.71 <.0001
Treatment×Time 28 6.42 <.0001 32 2.6 <.0001
Bosminidae Treatment 7 2.93 .02 8 1.14 .36
Time 4 2.61 .04 4 17.63 <.0001
Treatment×Time 28 1.12 .33 32 0.6 .95
Ceriodaphnia Treatment 7 5.19 <.001 8 10.19 <.0001
Time 4 32.77 <.0001 4 77.78 <.0001
Treatment×Time 28 2.14 .002 32 1.71 .02
Chydoridae Treatment 7 1.69 .15 8 2.02 .07
Time 4 25.98 <.0001 4 17.63 <.0001
Treatment×Time 28 1.19 .25 32 1.27 .18
Rotifera Treatment 7 2.84 .02 8 2.46 .02
Time 4 1.98 .11 4 35.55 <.0001
Treatment×Time 28 1.06 .4 32 2.23 .002
Abiotic Temperature Treatment 7 0.85 .55 8 0.86 .56
Time 4 2,364.52 <.0001 4 1,567.13 <.0001
Treatment×Time 28 1.02 .45 32 0.54 .98
Dissolvedoxygen Treatment 7 0.86 .54 8 2.39 .03
Time 4 49.47 <.0001 4 70.54 <.0001
Treatment×Time 28 0.75 .76 32 0.53 .98
Turbidity Treatment 7 0.74 .63 8 0.99 .45
Time 4 7.8 <.001 4 27.66 <.0001
Treatment×Time 28 1.79 .04 32 0.48 .99
Phosphorus Treatment 7 1.05 .41 8 0.76 .64
Time 4 4.83 <.001 4 0.89 .47
Treatment×Time 28 0.86 .67 32 0.77 .8
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Functional Ecology
NELSON Et aL.
3.2 | Experiment 2: Test of competition and
facilitation between juvenile invasive common
carp and bighead carp
3.2.1 | Fish interactions
Foreachcarpspecies,growthwasunaffectedbyincreasingheterospe-
cifics, but declined with increasing conspecifics (Table1; Figure2c),
indicatingthatintraspecificcompetitionhadagreaterimpactforeach
species.Forinstance,thepercapitaeffectofincreasingcommoncarp
density reduced common carp growth 1.5 (weight) and 2.4 (length)
timesmorethan similar density increases by bighead carp (Table1).
Likewise,thepercapitaeffectofincreasingbigheadcarpdensityre-
duced bighead carp growth 1.6 (length) and 2 (weight) times more
thansimilarchangestoheterospecificdensities(Table1;Figure2d).
3.2.2 | Invertebrates
Total macrozooplankton density varied between treat-
ments (Treatment, F8,35 = 12.55, p<.001), through time (Time,
F4,142 = 109.68, p<.001), and responses manifested by treatments
through time (Treatment×Time, F32,142 = 3.44, p<.001; Table2;
Figure3d). Densities of macrozooplankton were similar between
bighead and common carp treatments (CCP vs. BHC, F1,34 = 0.02,
p=.89), indicating filter-feeding by each species had similar effects
on prey. Combined predatory effects of common and bighead carp
(mixed)further reduced macrozooplankton densities relative to big-
head carp-only treatments (MIX vs. BHC, F1,35 = 29.16, p<.001).
Threeofthefivemacrozooplanktontaxaweregreatlyreducedinthe
presenceofcarp,relativetofishlesscontrols(Table2).
Rotifer densities differed by treatment (Treatment, F8,53 = 2.46,
p=.02)andthroughtime(Time,F4,64 = 35.55, p<.001),with rotifers
increasingwithin select treatments through time (Treatment×Time,
F32,90 = 2.23, p=.002; Figure3e).Bighead carp only treatments had
lower rotifer densities than common carp only treatments(BHC vs.
CCP, F1,53 = 12.57, p=.001) and mixed species treatments (BHC
vs. MIX, F1,53 = 4.01, p=.05), but were similar to controls(BHC vs.
Control, F1,53 = 0.04, p=.83).Mixedspeciestreatmentswerealsosim-
ilartocontrols(MIXvs.Control,F1,53 = 1.76, p=.19).Incontrast,roti-
ferdensitiesincommoncarponlytreatmentswereeighttimeshigher
thancontrols(CCPvs.Control,F1,53 = 7.21, p=.01).
Chironomidae larvae were the most abundant sessile inverte-
bratessampledontilesduringtheexperiment;however,meandensi-
ties of Chironomidae were about 8 times lower than those observed in
Experiment1forpre-andpost-samplingperiods.Chironomidaeden-
sity did not differ among treatments (F8,34 = 0.93; p=.50;Figure3f).
3.2.3 | Limnological conditions
There were no significant differences in limnological parameters
among treatments, but conditions did vary through time (Table2).
Chlorophyll-a was similar among treatments, declined over the course
oftheexperiment,andhadconcentrations in fish treatments 1.5–2
timesgreater than fishless controls(Treatment×Time;F32,57 = 2.42;
p<.001).No effectsweredetected forphosphorous concentrations
duringtheexperiment(Table2).
4 | DISCUSSION
Ourresponse-surface designproveduseful inidentifyingthe netef-
fect of interactions between juvenile native and invasive fishes, for
comparingthe relativemagnitudeof intra- vs. interspecificcompeti-
tion,identifying facilitationamongspecies, andtracing attendantef-
fectson invertebratecommunities.Strong exploitationof planktonic
resourcesby invasivebighead carpcreated interspecificcompetition
with bluegill, as evidenced by their reduced growth. The recipro-
cal effect of bluegill on bighead carp actually increased the growth
ofbighead carpatlow, butnothigh densities.Interestingly,the lack
ofenhancedbigheadcarpgrowthathigh densitiessuggests thatthe
mechanism(s) promoting enhanced growth at low densities have a
diminished effect as fish numbers increase and density-dependent
processes limit growth. Similar effects were not observed between
commoncarpand bighead carp perhaps because of differences be-
tween bluegill and common carp in terms of niche partitioning, be-
cause intraspecific competition was dominant for both taxa, and/or
because cyprinids are generally more tolerant of stressful environ-
ments than centrarchids.
4.1 | Magnitude of intra- and interspecific
competition among juvenile native and invasive fishes
Experimentshave long been usedtoquantify the effectsofcompe-
tition on organism growth or survival. However, many assessments
have largely focused on either intra- or interspecific interactions
(Connell,1983;Goldberg&Barton,1992;Gurevitchetal.,1992),with
assessmentsof both occurring less frequently(Inouye,1999,2001).
Forcompetingbigheadandcommoncarp(Experiment2),conspecifics
affected growth 1.5–2.4 times greater than interactions with hetero-
specifics.Themagnitudeofdifferencesobservedinourstudywere
similar, though slightly less, than the competitive interactions ob-
served between coral reef fishes (intra > inter by 2–3 times; Forrester
etal., 2006). In general, density-dependent effects of conspecifics,
and the associated high degree of niche overlap, had the greatest
influenceongrowthofcommonandbigheadcarp.
Resource-partitioningand nichedifferentiationcanreducethein-
tensityof interspecific competition during times of resource scarcity,
allowingforspeciestocoexist.Bigheadandcommoncarpeachpreyed
upon zooplanktonic resources; however, differenceswere observed
betweenspecies.Bigheadcarpstronglyreducedrotifers,whereascom-
moncarphadnodetectableeffect.Bigheadcarppossessmucus-coated
gillrakers, whichallowsthem to filterandremove smallparticleslike
rotifersandphytoplanktonfromthewatercolumn(Kolaretal.,2007).
Thus,evenifcommoncarpmoreefficientlyexploitedmacrozooplank-
ton, bighead carp possess the functional traits required to consume
smaller and more productive (i.e. higher rates of biomass-turnover)
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Functional Ecology
NELSON Et aL.
food items such as rotifers and phytoplankton.By partitioning food
resources,interspecificcompetition betweencarpspecieswasdamp-
ened.In turn, intraspecificcompetition wasenhancedas conspecifics
competedforlimitedinvertebrateswithinthepartitionednichesofthe
foodweb.Becausethesecarpsappeartotolerateoneanotherduring
juvenile stages, theircombined predatory effects maybe particularly
troubling in environmentswhere preyproductivity is low, or at loca-
tionswheretheirinvadedrangesalreadyoverlaporareincloseproxim-
ity, such as in the Laurentian Great Lakes of North America.
Bighead carp reduced the growthof bluegill, providing the only
instancewhere interspecificexceeded intraspecificcompetition.The
suppression of large zooplankton by bighead carp was consistent
across our experiments, othercontrolled experiments (e.g. Schrank,
Guy,&Fairchild,2003),andwithpatternsfromaninvadedlargeriver
(e.g.Sassetal.,2014).Incontrasttothefilterfeedingofbigheadcarp
andcommoncarp,bluegillrelyonvisualacuity.Bluegillindividuallyse-
lectlargeconspicuouspreyforconsumption(Spotte,2007).Therefore,
theremovaloftheirpreferredzooplanktonprey,coupledwithan in-
abilityto exploit rotifersorphytoplankton, created a foodwebwith
few prey choices for bluegill. Although bluegillwere negatively af-
fectedbybigheadcarp,theirgrowthwasalsosensitivetoconspecific
densities. Model coefficients (i.e. slopes representing growth) were
similar,yet heterospecifics did produce a slightlysteeper slope. The
presenceofastatisticalinteractionprecludedcalculatingamagnitude
ofeffect, but did indicatenonlinearper capita effectswerepresent.
Whethertheseobservedpatternscarry-overtothefieldhasyettobe
determined.Presently,largenumbersofjuvenileandadultbigheaded
carpinhabitriver-floodplainecosystemsoftheMississippiRiverBasin
anditstributaries(Collins,Butler,Diana,&Wahl,2015;Collins,Diana,
Butler,&Wahl,2017;Sass etal. 2010).These riversystems harbour
diverseassemblagesoffunctionallysimilarfishspeciesthatdependon
zooplanktonduringearlylifestages.
4.2 | Facilitation among fishes
There is critical need in the study of biological invasions to better
understand the circumstances that promote the facilitation of one
species by another (Bascompte, 2010; Griffen, Guy, & Buck, 2008;
Rodriguez,2006;Simberloff &VonHolle,1999).Predicting howone
predator might facilitate another can be difficult, especially when
resourcesareshared.Yet,predatorsdirectly,indirectly,positively,or
negatively alter prey densities, behaviours, or distributions in com-
plex ways (Kerfoot & Sih, 1987; Werner & Peacor, 2003). In some
cases,howapredatoralterscommunitystructurecanconferbenefits
to other predators (e.g. Adams, Pearl, & Bruce Bury, 2003; Huss &
Nilsson, 2011; Thayer, Haas, Hunter, & Kushler, 1997). Here, blue-
gill indirectly increased the growth of invasive bighead carp at low
densities, but not at high densities. Interestingly, facilitated growth
of a small number of invasive fishes should shorten the duration they
arevulnerableto larger predators, which would be advantageous in
newly colonised habitats. Based on the responses of invertebrates,
themechanismsenhancing bigheadcarpgrowthappearstohaveoc-
curredthroughbenthicChironomidaelarvaeandplanktonicrotifers.
Fishes that shift foraging to alternate food resources to lessen the
effectsofinterspecificcompetitionmayalsoaltertheirlocalenviron-
ment by recycling nutrients, which feedback to alter the food web (e.g.
viamicrobialloop,primaryproducers;Glaholt&Vanni,2005).Because
bigheadcarpcanexploitverysmall foodparticles (e.g.rotifers),rapid
changesinbiomass-turnovermaybereadilyexploited.Althoughblue-
gillfacilitatedthe growth of bighead carp,wefound no evidence of
facilitation between common carp and bighead carp, suggesting
thatcharacteristicsofthefoodweb itselfalso mediatethesespecies
interactions.
Alterationstohabitatortrophicstructureareacommonmeansof
facilitation. For instance, seaweed (Ascophyllumn nodosum; Bertness,
Leonard, Levine, Schmidt, & Ingraham, 1999) and zebra mussels
(Dreissena polymorpha; Thayer etal., 1997) altered habitat structure
intheir respectiveenvironments,whichenhanced the fitnessof cer-
tain in situ taxa. Intraguild predation can also alleviate regulatory
constraintsand facilitatethe establishment ofother species,such as
whenbluegillconsumethepredators(dragonflies)oflarval bullfrogs
(Rana catesbeiana;Adams etal., 2003). Here, alterations to material
flowsviafishegestionandexcretionappear tohave stimulatedden-
sities of benthic macroinvertebrates via benthic-pelagic coupling, a
pattern observed byothers (Collins & Wahl, 2017). Byshunting or-
ganic matter to collector- gatherers, r- strategist Chironomidae larvae
increasedrapidlyinbigheadcarptreatments.Curiously,thesepositive
effectswere undetected in mixed treatments suggesting that either
noeffectoccurredorstarved bluegillquicklymaskedanybottom-up
effects.Because juvenile bighead carp consumed the same foodre-
sources(i.e.bigheadcarponlyvs.mixed),wereasonedthatbottom-up
(i.e.increaseddensitiesofbenthicChironomidaebybigheadcarp)ef-
fectslikelyoccurredandwerecroppedbybluegill,maskingtreatment
effects in a manner similar to other manipulative experiments (e.g.
Collins, Baxter,Marcarelli, & Wipfli, 2016). Comparison of this bot-
tom-up response between experimentsis difficult, as Chironomidae
densities were nearlyeight times greater in the bluegill experiment
relative to the common carp experiment (both pre and post).This
distinction highlights that the conditions of the food web are an im-
portantmediator offacilitation.Weacknowledgethat differencesin
fish feeding traits (bluegillvs. common carp), specifically their likeli-
hoodofexploitingbenthic orterrestrialprey,mayalsoinfluencethis
facilitation mechanism to some degree. Bluegill may have consumed
allochthonousinputsofterrestrialinvertebrates;however,wedidnot
samplethesecontributions.Nevertheless,consumptionofbenthicand
terrestrialpreywouldcontributetonutrientrecyclingwithinthewater
column,likelyinfluencingtheproductivityofmicrobes,phytoplankton,
andinvertebrates(e.g.Brabrand,Faafeng,&Nilssen, 1990;Glaholt&
Vanni,2005;Schindler&Scheuerell,2002).Althoughourexperiments
were shorter in duration than the growing season of juvenile fishes,
sustained exploitation of zooplankton and rotifers by bighead carp
wouldpresumablyhave similarimpacts onfish growththrough time.
Futurestudiesshouldaddresshowspecies interactionsandresource
partitioningmayalter ecosystemmetabolism,biomass turnover,and
energyflows among foodweb pathways(e.g.Collins etal., 2016) to
better characterise the bioenergetic basis that drives facilitation.
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Functional Ecology
NELSON Et aL.
5 | CONCLUSIONS
Response-surface designs can be logistically difficult; however, the
abilityto test for co-occurringpositiveandnegative mechanisms is
amajor strength. In a classic synthesis of interspecific competition
experiments, Connell (1983) described the prevalence of positive
interspecific responses in experiments otherwise focused on com-
petition. In many contexts, species thought to compete for limited
resources actually confer benefits to perceived competitors by al-
tering food web architecture. By accounting for the directionality of
species interactions within our experimental framework and track-
ingresponses of prey at lower trophic levels, we provide a clearer
understanding of how competitive forces act to influence facilita-
tionbetweenspecies.Bigheadcarp’s ability to filter small particles
madethemwellsuitedtoexploitanysurplusproductivityoccurring
fromfeedbackswithinthefoodweb.Yet,surpluspreywas shared
amongst bighead carp, and ultimately only low densities exhibited
enhanced growth. Ultimately, the magnitude of facilitation was con-
strainedbyfoodwebproductivityandthedensityofbighead carp
thatsharetheprey.
ACKNOWLEDGEMENTS
We specifically thank M. Diana, S. Butler, and M. Naninni for their
logistical, field, and laboratory assistance. We also thank members
oftheKaskaskia,RidgeLake,andSamParr Biologicalstations ofthe
Illinois Natural History Survey, as well as graduate students from the
University of Illinois for their intellectual discussions and feedback.
InstitutionalAnimalCareandUseCommittee(#11053)approvalwas
obtained before commencement of the study. All fishes were ac-
quired,retained,andusedincompliancewithfederal,state,andlocal
laws and regulations.
AUTHORS’ CONTRIBUTIONS
K.A.N., G.G.S., and D.H.W. conceived the ideas and designed the
experiments; K.A.N. collected the data; K.A.N. and S.F.C. analysed
thedata; K.A.N.andS.F.C. led thewritingof themanuscript.All au-
thors contributed critically to the drafts and gave final approval for
publication.
DATA ACCESSIBILITY
Data for this study are available through the University of Illinois:
https://doi.org/10.13012/b2idb-9706842_v1 (Nelson, Collins, Sass,
&Wahl,2017).
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How to cite this article: Nelson KA, Collins SF, Sass GG,
WahlDH.Aresponse-surfaceexaminationofcompetitionand
facilitation between native and invasive juvenile fishes. Funct
Ecol.2017;00:1–10.https://doi.org/10.1111/1365-2435.12922
