Nordic Society Oikos
Venue and Outcome in Ecological Experiments: Manipulations of Larval Anurans
Author(s): David K. Skelly and Joseph M. Kiesecker
Reviewed work(s):
Source: Oikos, Vol. 94, No. 1 (Jul., 2001), pp. 198-208
Published by: Wiley-Blackwell on behalf of Nordic Society Oikos
Stable URL: http://www.jstor.org/stable/3547268 .
Accessed: 25/09/2012 20:47
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp
.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact support@jstor.org.
.
Wiley-Blackwell and Nordic Society Oikos are collaborating with JSTOR to digitize, preserve and extend
access to Oikos.
http://www.jstor.org
FORUM
FORUM
M~l
FORtJI\U
It
existing
information.
FORUM is intended
fornewideas or newwaysof interpreting
on
currentthinking
and for challenging
hypotheses
providesa chancefor suggesting
Formal
prose,designedto attractreaders,willbe permitted.
ecologicalissues.A lighter
and all contributions
shouldbe concise
albeitshort,willnotbe accepted,
research
reports,
A summary
is notrequired.
shortlistof references.
witha relatively
of
manipulations
Venueand outcomein ecologicalexperiments:
larval anurans
Studiesand Dept of Ecologyand
David K. Skelly and JosephM. Kiesecker,School of Forestryand Environmental
Biology,Yale Univ.,370 ProspectStreet,New Haven, CT 06520, USA (david.skelly(yale.edu)(present
Evolutionary
Park, PA 16802, USA).
addressof JMK: Dept of Biology,MuellerLab, PennsylvaniaState Univ.,University
The choice of venue is believedto be a criticaldecisionfor ecological research programs (Peters 1991, Werner
ecologistsconducting
experiments,
yettheexistenceof tradeoffs 1998, Wootton and Pfister1998).
in designand the impactof venueon outcomehave not been
There is a broad perceptionamong ecologiststhat
quantitatively
evaluated.To theseendswe revieweda set of 227
venue is a criticaldecision
comparisonsfrom52 studiesdesignedto quantifythe effectof the choice of experimental
of larval anurans.We pre- thatcan constrainotherattributes
densityon the growthperformance
of an experiment.
In
dictedthatbothdesignand outcomewouldbe relatedto experia
number
of
particular,
have
that
ecologists
suggested
mentalvenue(laboratory,mesocosm,and field).We foundthat,
tendto be limitedto less complicated
in contrastto our predictions,
did not fieldexperiments
laboratoryexperiments
includemorefactorsor yieldmorepreciseestimatesof responses designs and lower levels of replication(Mertz and
comparedwith mesocosmand field manipulations.In partial
McCauley 1980, Hairston 1989a, Jaeger and Walls
we foundthatlaboratoryexperiments
supportof our prediction,
did utilizesomewhatlargernumbersof replicatesand included 1989,Peters1991,Morin 1998). In addition,it has been
more levels per factorcomparedto the alternativevenues.In hypothesizedthat the fieldenvironment
is more variadditionwe foundthat,as predicted,raisingtadpolesat higher able leading to less precision among replicates
densitiesof conspecifics,
or in the presenceof heterospecifics
tendedto decreasegrowth.This effect,consistent
withcompeti- (Hairston 1989a, b, Morin 1998). Finally,exposureto
venue.In particu- the naturalenvironment
tion,was strongly
dependenton experimental
is thoughtto limitthe ability
lar, we foundthat interspecific
effectswere muchstrongerin of an experimenter
to controlconditionsexperiencedby
mesocosmversusfieldmanipulations.
This resultis particularly
relevantbecause conceptionsof amphibianassemblageshave the subjectsof the manipulation(Mertz and McCauley
includedinterspecific
competition
as integralto naturalpatterns 1980, Morin 1989, 1998, Peters 1991). These perceived
of amphibiandistribution.
We concludethathypothesized
trade- tradeoffs,
coincidentwithrisingstandardsforstatistical
offsamongexperimental
venueshave notacted in a particularly
rigor,
have
motivatedecologiststo experimentwithin
strongway in shapingthe designof tadpoledensitymanipulations.However,venuemay mediatestrongeffectson the out- laboratories(e.g. Mertz and McCauley 1980).
come of such experiments.
of such methodology
Quantification
Even as the benefitsof laboratorymanipulationhave
based biases willhelpecologistsmoreeffectively
matchthegoals
been
repeatedlyasserted,criticsalso have been nearly
of theirexperiments
withdecisionsregardingvenue.
Over thelast threedecades ecologyhas becomebroadly
experimental.As experimentation
has become part of
the culture of ecology, ecologists have contemplated
strategiesforchoosingamong the various optionsthat
confrontall experimenters.
Importantexamplesinclude
theselectionof experimental
venue,thechoice of experimentaldesign, and the degree of replication.At the
same time, the wider use of experimentshas led to
considerationof the role of experimentationwithin
198
unanimous in contendingthat field experimentsare
morerealisticand thatonlyfieldexperiments
can tellus
about the quantitativeimportanceof factorsin natural
populations (e.g. Carpenter 1996). Perhaps for this
reason, major reviewsof ecological experimentsoften
have been limitedto field experiments(e.g. Connell
1983,Schoener1983,Goldbergand Barton 1992,Gurevitchet al. 1992,2000). In responseto theirperceptions
of these tradeoffsin experimentation,
some ecologists
turnedto a compromisesolutionin the formof hybrid
experimentsconducted in mesocosms (Wilbur 1989,
1997, Morin 1998). For experimenters
employingthis
hybridapproach, a major goal has been the developOIKOS 94:1 (2001)
techniquesthat captureat- represent
ment of experimental
a widearrayof designsand venues.In adwithoutsufferingdition,we havetargeted
of thenaturalenvironment
tributes
thatincludemaexperiments
of fieldex- nipulations
limitations
as acutelyfromtheattendant
on
of density.
The impactof competition
perimentation.
duringthe
populationshas been a focusof interest
The backdropfor decisionsabout experimentalentirehistoryof experimental
ecology (Kingsland
venuesare the goals whichmotivateecologiststo 1995). As a resultof thisresearch,
for
competition
in thefirstplace (Woottonand foodresources,
conductexperiments
betweenspecies,continues
particularly
conductedto test to be considered
Pfister1998). Thus, experiments
the
an important
factorin regulating
set- abundanceand distribution
ecologicaltheoryoftentake place in laboratory
of species(e.g. Rowe and
tings.It has been reasonedthat it is simplytoo Dunson 1994, Wilbur 1997, Resetaritsand Fauth
to deal with the challengesof replicating1998, Alford 1999, Fauth 1999, Petranka and
difficult
sufficiently
againsta noisybackgroundto conduct Kennedy1999).
in thefield(e.g. Morin1998).By
suchinvestigations
allowsus to
Finally,a focuson anuranexperiments
designedto quan- construct
experiments,
contrast,
mensurative
each
venuecategories
threenonoverlapping
of an interaction,
oftenhave been represented
tifythe strength
numberof studies:laboby a substantial
in thefield(e.g. Paine 1992).In thiscase, ratory,
conducted
experiments
mesocosm,and field.Laboratory
it is believedthatthe fieldsettingwill yieldresults includethose manipulations
conductedindoorsin
thecon- small containers.Mesocosmexperiments
whichare moreapplicableto understanding
have been
In all cases,the conducted
ditionsfacedby naturalpopulations.
containers.
outdoorsin replicated,
artificial
choices Most commonly,
appearto reflect
decisionsmadeby ecologists
mesocosms
used foranuranexperibased on personalassessmentsof the costs and mentshave been constructed
using cattlewatering
in differenttanks.Fieldexperiments
benefitsof conductingan experiment
bymahavebeendominated
havebeen nipulations
venues.However,to date,thosereckonings
in meshenclosures
butalso inconducted
made largelyin theabsenceof formalanalyses.Nei- clude manipulations
of entirewetlands(e.g. Smith
therthe degreeto whichvenuemediatedtradeoffs 1983).Note thatwhilethe definitions
describedhere
affectexperimental
design,nor thesize of venueme- are consistent
with usage by amphibianecologists
outcomehave been
diated effectson experimental
(e.g. Wilbur1997, Morin 1998),it is obviousthat
Thus,we may not knowhow
previously.
quantified
fordifferent
ecolthesetermshavedifferent
meanings
of one venueoveranotherreally
largetheadvantages
ogists(e.g. mesocosm:Odum 1984, Petersenet al.
data it is possible
are. In theabsenceof quantitative
et al. 1992,2000).
1999;field:Gurevitch
theadvantages
maydistort
thatprevailing
perceptions
regardIn thisstudy,we evaluatethreepredictions
of different
venues.
and disadvantages
on widelyheld
of
based
attributes
experiments
ing
in
venuemediatedtradeoffs
In orderto quantify
we expect
Relativeto fieldexperiments,
we reviewdesignsand perceptions.
on outcome,
designand effects
and
of
mesocosm
laboratory
experithe
design
(1)
To meet
resultsfroma set of publishedexperiments.
within
more
(2)
replication
ments
to
be
complex,
we have focusedon a singletaxon,
theseobjectives,
to
be
higher,
experiments
mesocosm
and
laboratory
anuranlarvae.Anuranlarvaehave been used extenexwithinmesocosmand laboratory
designedto elucidateprinciples and (3) precision
sivelyin experiments
Within
each
to
be
reviewed,
study
higher.
periments
of
communities
the structure ecological
concerning
as thenumberof experimen(e.g. Morin1983),and of therole of com- we measuredcomplexity
generally
the
numberof levelsperfacincluded
and
tal
factors
(e.g. Morinand Johnson1988).
petitionin particular
as
number
of replicatesof the
the
tor,
replication
Anuranlarvae also are closelyassociatedwiththe
and precisionas
control
treatment
below),
(defined
to exploittheuse of mesoof techniques
development
of thecontrol
of
variation
the
coefficient
%
(%
CV)
mediated
tradeoffs
to
venue
in
order
cosms
mitigate
(e.g. Wilbur1997).For thesereasons,we believethat treatment.
the
We also evaluatedtwo predictions
regarding
taxonin
appropriate
larvalanuransare a particularly
in
conducted
of
outcomes
experiments
tadpole
density
of venue.In addition,
theeffects
whichto investigate
These
were
and
venues.
field
mesocosm,
laboratory,
chance
focusprovidesthegreatest
a sharptaxonomic
of conspeto venue,ratherthan (1) thattadpolesraisedat higherdensities
attributable
of isolatingeffects
of cifics,or in thepresenceof additionalheterospecifics
to the mechanicaldistinctions
those attributable
would grow more slowlythan tadpolesraised at
withdifferent
typesof organisms.
working
and (2) that
lowerdensityor withoutheterospecifics,
additional
advanOur choiceconfersa numberof
on
on larval the measuredimpactof densitymanipulations
tages as well. Ecological experiments
venue.
of experimental
anuransbeganin the 1960s(Dumas 1964)and their growthwouldbe independent
were evaluatedusing
mirrorsthat of ecologyas a whole. These lattertwo predictions
development
of In responseratios of growthreStudiesare numerousand, owing to the relative meta-analyses
theseexperimentssponses.
of larval amphibians,
tractability
OIKOS 94:1 (2001)
199
We have focusedon growthresponsesbecause growth
is a sensitiveindicatorof performanceand a strong
Literaturesearch
predictor of metamorphic traits among anurans
listof studiesby searching (Werner 1986). These metamorphictraits, in turn,
We compileda preliminary
Agri- have been related to survivorshipand reproductive
databases(AquaticBiology,
a setofcomputerized
Biological& Agriculturalsuccess (e.g. Smith 1987). In addition, growth reResources;
& Fisheries
culture
Index;BIOSIS; ScienceCitationIndex).In each data- sponses have been reportedby virtuallyall authorsof
base, we used the searchstring"(tadpole?or anuran experimentsfocused on larval anurans, while other
ordensity)". measures (e.g. survival, developmentrate) are reand(competition
larvae?orlarvalanuran?)
duringthe portedless frequently.
listsof all papersidentified
The reference
databasesearchesalso weresearchedand potentially Following the standardconventionfor meta-analypaperswerealso includedin thepreliminaryses we have focused on comparisonsof control and
relevant
1999. experimentaltreatmentsfrom each study. We desigthrough
paperspublished
list.Oursampleincludes
We paredour listto includeonlythosestudiesthat nated the lowest densitytreatmentto be the control
fivecriteria in intraspecificexperimentsand the single species
meeting
includedone or morecomparisons
comparitreatmentto be the control in interspecific
directly
manipulated
experimenter
(1)
the
(Appendix):
densitiesof at least one larvalanuran;(2) a growth sons. In both cases, if the experimentaltreatment
relatedresponse(growth
rate,finalsize)was measured mean is lower than the control treatmentmean, the
ofthelarvalperiod trend is consistentwith a competitiveeffect.Most
on a givenspeciesfortheremainder
timeperiod,(3) the studiesincludedmore than one comparison.In some
or untiltheendofa predetermined
publishedgrowthresponseincludedthe mean,some cases a single control treatment(the one with the
stan- lowest density) was compared with more than one
standard
ofvariance(variance,
deviation,
estimate
(4) the experimental treatment (following convention of
andsamplesizesforeachtreatment,
darderror),
and in the Gurevitchet al. 1992). Experimentaltreatmentswere
wereconductedsimultaneously
treatments
treat- neverused more than once.
pairsof density
samelocation;and (5) relevant
inothermanip- We gleaned the necessarydata from the text and
werenotconfounded
byvariation
ments
additional tables of each paper where possible. In some cases,
predators,
ulatedfactors(e.g. fooddensity,
manipulations).
hydroperiod
competitors,
growthresponses were presentedonly in figures.In
intraspe- these instances,we estimatedmeans and errors by
as including
Each studywas characterized
orboth. digitizingthe image and comparingthe lengthof bars
manipulations,
cificmanipulations,
interspecific
meso- (or position of symbols)relativeto the scale on the
as laboratory,
venuewasdesignated
Experimental
in the response axis. Stems estimatingerrorwere quantified
presented
cosm,or fieldbasedon thedefinitions
Introduction.
of this techsimilarly.We verifiedthe effectiveness
nique by digitizingthe relevantfiguresfromour own
papers (e.g. Skelly 1995b) and comparingthe resulting estimateswiththe originaldata.
Attributes
of experiments
In meta-analysisthe standard deviation is used as
(twostudiescontained the estimate of error about treatmentand control
For each of the54 experiments
in morethanone venue)we recordedthe means. In cases where authors reportedthe standard
experiments
oflevelsper error (SE) instead,we calculated the standard deviathenumber
factors,
number
ofexperimental
used. Whenthe tion as (( i/n)SE) where n is the sample size for the
factor,and thenumberof replicates
we treatment.In a few cases whereno estimateof error
variedwithintheexperiment,
numberof replicates
In addi- was reported,it was possible to estimatethe standard
usedthenumberfromthecontroltreatment.
the% CV ofgrowth
ofthe deviationby calculatingthe square root of the within
responses
tion,wecalculated
as thelowestdensity group mean square as reportedin an ANOVA table
"control"treatment
(designated
in intraspecific
treatment
and the single (Gurevitchet al. 1992).
experiments
These
in interspecific
comparisons).
speciestreatment
Data from each study were analyzed using
attributes
were analyzedindividually
usingone-way MetaWin (Rosenberg et al. 1997) and effectsizes
ANOVAs to determine
whethertheyvariedamong were calculated and analyzed as In response ratios
venues.
experimental
(Hedges et al. 1999). In all of the comparisonsused
in this meta-analysis,a positive effectsize indicates
that growthtendedto be reducedat higherdensityor
in the presence of the heterospecific(followingthe
Meta-analysisof growthresponses
convention of Gurevitchet al. 1992). Comparisons
We performed
a meta-analysis
on growthresponses among subgroups were evaluated using the homoof tadpolessubjectedto different
densitytreatments.geneitystatistic,Qb (Hedges and Olkin 1985).
Methods
200
OIKOS 94:1 (2001)
We also predictedthat laboratoryand mesocosm
experimentswould be more precise than fieldexperiOur reviewincludeddata collectedfroma totalof 52 ments. However, % CV did not vary among venues
137intraspecific
and 90 interspe- (Fig. 3; one-wayANOVA: df= 2.149, F= 1.02, P=
studiesincorporating
cificcomparisons
(Table 1, Appendix).Studieswere 0.36).
conductedon four continents(Australia,Europe, We made a second set of predictionsfocusedon the
NorthAmerica,
SouthAmerica)and includedanurans outcome of experimentsconductedin different
experifromsix familiesand 35 species.Withinthe sample, mentalvenues.The firstof thesepredictionswas that,
weremostnumerous irrespective
manipulations
in thelaboratory
of venue,tadpolesof a givenspeciesreared
Results
followedby those conductedin
(85 comparisons),
mesocosms
(79), and in thefield(63). Whileall experi- (a) 3
of density,
additionalfacmentssharedmanipulations
and
torsfocusedon bioticmanipulations
of predators
and abioticmanipulations
suchas pH and
pathogens,
hydroperiod.
based on expected 0
We made a set of predictions
in theattributes
in
of experiments
conducted
tradeoffs
different
venues.Contraryto the first
experimental
to labowe foundno evidencethat,relative
prediction
Laboratory Mesocosm
Field
fieldexperiments
ratoryand mesocosmexperiments,
factors(Fig. la, one-way
includedfewerexperimental
Experimental
Venue
ANOVA:df= 2.51,F= 1.61,P = 0.21).In partialsup- (b) 7
of
we did findthatthenumber
portof thisprediction,
6levelsperfactorwas relatedto venue(Fig. lb; one-way
ANOVA: df= 2.51, F= 3.56, P < 0.04). Laboratoryex5
tendedto includemorelevelsperfactorthan
periments
venues(TukeyHSD test:P < 0.05); there
alternative
was no evidencethatmesocosmand fieldvenuesdifferedin thenumberof levelsper factor(TukeyHSD
2test:P > 0.05).
In this
focusedon replication.
The secondprediction
between
case we foundsomesupportfora relationship
0venue(Fig. 2; one-way
and experimental
replication
Laboratory
Mesocosm
Field
exANOVA:df= 2.51,F= 4.97,P < 0.01).Laboratory
Venue
Experimental
a higherdegreeof
tendedto incorporate
periments
replication
comparedwithmesocosmor fieldexperias (a) thenumberof
Fig. 1. Designcomplexity
represented
ments(TukeyHSD test:P < 0.05). Therewas no evi- experimental
and (b) thenumberof levels
factorsemployed
in perfactorin 54 experiments
differed
dencethatmesocosmand fieldexperiments
in laboas occurring
categorized
or fieldvenues.Errorbarsrepresent
1 SE.
mesocosm,
theirdegreeof replication
(TukeyHSD test:P > 0.05). ratory,
Table 1. Attributesof comparisonsincludedin meta-analysisof competitionexperimentsfocusingon larval anurans. Each
In
or heterospecifics
(interspecific).
comparisonhas been characterizedas an additivemanipulationof conspecifics(intraspecific)
venue:laboratory,mesocosm,or field(see Methodsfordetails).
addition,manipulationswerecharacterizedby theexperimental
The total numberof comparisonsconsideredis includedin parenthesesfollowingthe venue description.Experimentalunit
volume(liters)is the volume of a singlecontaineror enclosureused in the manipulation.Stockingdensityis the total density
added). Densityfactoris the ratioof
(conspecificsor heterospecifics
treatment
of tadpolesin the experimental
(individuals/liter)
would result
or conspecifics
densityand thecontroldensity.An additionof an equal densityof heterospecifics
the experimental
in a densityfactorof two. For each measurethe mean + 1 SE is presented.
Manipulation/Venue
Intraspecific
Laboratory(73)
Mesocosm (34)
Field (30)
Interspecific
Laboratory(12)
Mesocosm (45)
Field (33)
OIKOS 94:1 (2001)
Experimentalunit volume
Stockingdensity
Densityfactor
5+ 1
712 + 66
346 + 35
43.8 + 19.8
0.3 + 0.1
1.4 + 0.3
7.0 + 0.9
2.7 + 0.2
4.6 + 0.7
5+ 1
637 + 57
577 + 39
5.4 + 1.6
0.7 + 0.1
1.4 + 0.5
2.2 + 0.1
3.8 + 0.8
2.0 + 0.1
201
6
0.4
T~~~
U
-
v0.
0
X -0.2 S
Laboratory
Mesocosm
Experimental
Venue
Field
-0.4 -
Laborato
Mesocosm
Field
foreach
ofreplicates
ofthecontrol
treatment
Fig.2. Number
Erpe entalVenue
in laboratory,
of 54 experiments
categorized
as occurring
1
SE.
Error
bars
represent
or
field
venues.
mesocosm,
ratios)in tadpole
effect
sizes(In response
Fig.4. Cumulative
as inwerecategorized
Experiments
experiments.
competition
(filledbars)manipula(openbars)or interspecific
at higherdensityor in the presenceof a heterospecific, traspecific
or
mesocosm,
venue.laboratory,
tions,and by experimental
grow more slowly.This predictionwas supportedfor field.Positiveeffect
sizesindicatethattadpolegrowthwas
both intraspecific
(n = 137, In Response ratio= 0.1I,
or when
of conspecifics
was increased
reducedwhendensity
wereadded.
heterospecifics
P < 0.05) and interspecific
(n 90, In Response ratio=
0.06, P < 0.05) manipulations.Overall,the growthrethe designof
duction was larger for tadpoles subjected to the way decisionsare made regarding
inproducplay
and
role
experiments
of
the
experiments
intraspecific
manipulations.Whilemostindividualcomabout the naturalworld(e.g. Morin
parisons were consistentwith the overall effectsde- ing inferences
ecologists
have
scribed,a total of 33 (15%) showedthe oppositetrend. 1998,Werner1998).Broadlyspeaking,
We also predictedthatexperimental
outcomewould cometo believethatchoicesmadeaboutone aspectof
otheraspectsof
designmayconstrain
be independentof venue. This predictionwas rejected an experimental
the
thedesign,and thatsuchchoicescouldinfluence
for both intraspecific
(Fig. 4; Qb = 108.8, df= 2, P <
and theinferences
drawn.
outcomeof theexperiment
comparisons (Fig. 4; Qb=
0.001), and interspecific
the
1504, df- 2, P < 0.001). In both cases, effectsizes Of all the decisionsmade by an experimenter,
as
one
the
of
rank
of
must
venue
experimental
choice
tendedto be highestamong mesocosmmanipulations,
in thisregard.In thisstudywe setout to
intermediateamong field manipulations,and lowest mostcritical
in thedesignand outcomeof experipatterns
quantify
among laboratorymanipulations.
Discussion
fromthechoiceofvenue.
mentsflowing
Ourfirst
goalwas to evaluatethreewidelyprofessed
whendesigning
encountered
tradeoffs
beliefs
regarding
wefound
Muchto oursurprise,
ecologicalexperiments.
we reviewed.Rellittlesupportamong the experiments
As experimentation
has becomeingrainedin theirdisci- ative to theirmesocosmand fieldcounterparts,
laborapline,ecologistshave begun to more closelyscrutinize tory experimentsutilized more levels per factor and
more replicates,but were equivalentin the numberof
factorsevaluated and in the precision of responses.
16
in
Therewas no evidenceof venuemediateddifferences
designbetweenmesocosmand fieldexperiments.
12deThe suppositionthatmorecomplexexperimental
signs can be accomplishedin the laboratoryor in
U8to add
mesocosmsis based on theidea thatit is difficult
additional factorsor levels, and thereforeadditional
4
experimentalunits, to experimentsconducted in the
field.However, most of the experimentswe reviewed
includedone, two or threefactors,and therewas no
0_ -.
containedfewerfactors
evidencethatfieldexperiments
Field
Laboratory Mesocosm
withinthis range. As has been pointed out, factorial
designs explode into large numbersof experimental
Venue
Experimental
units when extended beyond three factors (Wilbur
of variation(/o CV) of growth 1997). Perhaps the difficulty
Fig. 3. Per centcoefficient
of conducting(and interResponseswerecollected
responses
amongcontrolreplicates.
of thissize has moderatedthe
as occurring
in laboratory, preting)any experiments
categorized
from54 experiments
1 SE.
or fieldvenues.Errorbarsrepresent
impositionof a complexitybased tradeoff.
mesocosm,
202
OIKOS 94:1 (2001)
One of the primaryrationalesfor using mesocosms
and laboratorycontainershas been the relativeease of
replication.In practice,it appears thattheseadvantages
have been expressedmoderatelyat best. There is no
evidence from the structureof the experimentswe
reviewedthat mesocosmsare easier to replicate.And
while the typicallaboratoryexperimentalunit is more
thanorderof magnitudesmallerthanthetypicalmesocosm or fieldenclosure,the relativeease of settingup
extra laboratorycontainershas yielded just a small
These patternsmay
increasein replicatesper treatment.
imply that the two to five replicatesused in most
regardlessof venuehave suppliedstatistical
experiments
power adequate to researchers'goals. An alternative
explanationis that the degree of replicationmay be
determinedby otherconsiderations,(such as limitson
thenumberof mesocosms,shelfspace, or availabilityof
fieldsites),or even rules of thumb.
Among our most puzzlingfindingsis the lack of a
gradientin precision.We fullyexpectedto see more
"noise" in responsesemanatingfromfieldversusmesoThese resultsdeserve
cosm and laboratoryexperiments.
additional investigation.Laboratory experimentson
tadpoles are done in small,identicalcontainersusually
in environments
that impose some control over light
and thermalregimesand where food is carefullymetered out. The fact that responsesfromthis environmentare as variableas thosefrommesocosmand field
environments
suggestsone of threelikelymechanisms.
First,it may be that the largernumberof individuals
that compriseexperimentalpopulations in mesocosm
and field experimentsfoster an averaging effecton
responsesnot foundamongsmallernumbersof individuals in laboratorycontainers(see discussionby Petersen
thefieldenvironment
may be
et al. 1999). Alternatively,
attributes
more variable,but importantenvironmental
may not vary in a synchronizedfashion. Thus, a
more rapid growthalso may
warmerlocationfostering
have a lowerdissolvedoxygenor a lowerabundanceof
food resourcesresultingin littlenetvariationin growth
may be inamong replicates.Finally,experimentalists
attributesthatmost
correct.Among the environmental
directlyimpactthe responseswe analyzed,the environmentsprovidedby alternatevenues may not vary the
way we pre-supposed.Whatevertheirorigin,our findings suggestthat precisionhas not been a particular
problem in field experimentson larval anurans and
offerno mealaboratoryand mesocosmenvironments
surableadvantagein thisregard.
hypothOverall,our resultssuggestthatthetradeoffs
esized to constrain researchers'abilities to conduct
complex,powerful,and precise experimentshave not
acted in an especiallystrongway to structureexperimental designs. Phrased another way, there is little
evidencefromour analysesthatthereare strongadvantages or disadvantagesto usingone venueover another
based on considerationsof designcomplexity,replicaOIKOS 94:1 (2001)
tion, and precision.While thereis no guaranteethat
conductedon othertaxa or otherinteracexperiments
tions will produce the same message, our findings
stronglysuggestthatthesewidelyheld beliefsshouldbe
further
evaluated.The advantagesof such scrutinyare
several. Most notably, if venue does not constrain
experimentaldesigns as much as is typicallythought,
then ecologistscan choose experimentalvenues based
on otherconsiderations.
one of themostcritical
Of all possibleconsiderations,
to many ecologistsis the notion of realism.This conto define,but undeniably
difficult
cept is frustratingly
importantto muchthatecologistsdo. When measuring
the strengthof an interaction,and even when testing
ecologicaltheory,manyecologistswould like to believe
resultsoffera realisticpictureof
thattheirexperimental
the factorsthataffectnaturalpopulationsand communities. Unfortunately,realism is one of the most
attributesto calibrate.An ecolodifficult
experimental
a manipulationunavoidablydecreases
gist performing
realismin hard to defineways.Whileit is oftenimplied
in the fieldare morerealisperformed
thatexperiments
tic than those performedin mesocosmsor laboratory
mechanisms,at base, this can only be called an
assumption.
A numberof ecologistshave dealt with this thorny
approach. By rooting
issue by adoptingan integrative
and conducttheirresearchin a conceptualframework
in different
venues,theyseek to evaluing experiments
ate hypothesesthroughconsensusin outcomesthatcan
extendacross venues(e.g. Sarnelle1997,Werner1998).
Consequently,one metricof theimportanceof venueis
conductedin different
the degreeto whichexperiments
venuesachievecongruencein outcomes.If experimental
outcomeis largelyindependentof venue,thenthereis
some reason to think that resultingconclusions are
more likelyto reflecta process or patternof interest
rather than the methodological artifacts of our
manipulations.
Thus, the second goal of our reviewwas to evaluate
the outcomeof tadpole densitymanipulations,particuvenue employed.
larlywithrespectto the experimental
As in manymodel systems,amphibianecologistshave
measuredtheimpactof densityusingexperifrequently
between
ments.In thissystem,competition,
particularly
species,has been a cornerstoneof hypothesesof community structurein amphibian assemblages (Morin
1983,Wilbur 1997, Alford1999).
thatmanipulaThe resultsof our reviewdemonstrate
tions of tadpole densitieshave regularlyyieldedeffects
consistentwith competition.Overall, larval anurans
raised at higherdensitiesof conspecifics,and those
raised in the presence of additional heterospecifics,
experiencedreduced growth.However, it is equally
clear that the measured impact of densityis highly
As we discussbelow,our resultssuggest
heterogeneous.
thatdecisionsmade regardinghow to conducta density
203
manipulationmay have sizable impactson estimatesof
Given that mesocosmswere firstimplementedas a
more tractable,but quasi-naturalalternativeto field
competitiveeffect.
in estimated manipulations(Resetaritsand Fauth 1998), perhapsit
Specifically,we found large differences
effectsize among the threeexperimental
venues.Meso- is not surprisingthat researchershave been successful
cosm experimentswere associated with largerdeclines at mimickinga numberof aspectsof fieldexperiments.
to
in growththan eitherlaboratoryor fieldexperiments. These similaritiesmake it that much more difficult
As seen in Fig. 4, estimatesof the impact of interspe- understandthe sharp distinctionin experimentaloutcific manipulationsare highly variable. Why would comes betweenvenues. Nevertheless,thereare at least
interspecific
effectsizes divergeso widely?A negative two possibilitiesthat bear furtherinquiry.First,it is
workingin the two venues
estimate(facilitation)for laboratorymanipulationsis clear that experimenters
species (Appendix).
derived fromjust two studies,both focusingon the have tended to focus on different
same two species (Smith-Gilland Gill 1978, Werner Perhaps some specieswhichhave been examinedsolely
1992). As in mostlaboratorystudiesof tadpole compe- within mesocosms will also compete stronglywhen
tition(and unlike the mesocosm and fieldstudies re- evaluated in the field.Second, we know of no studies
viewed), these researchers provided tadpoles with comparing the composition and abundance of food
regularlyreplenished,per-capitafood rations and in resourceswithinmesocosmsand naturalponds (or field
both cases it appeared that tadpoles sometimes enclosures).If mesocosmscontain a lower diversityof
benefitedfromincreasedtadpole density,perhaps be- food resources,or if resourcesbecome depletedduring
cause it was associatedwitha greaterabsolute amount an experimentmore rapidly,the measuredimpact of
of food. In addition,laboratoryexperiments
have been densityon growthcould be increasedbecause of heightconductedin containersaveragingjust a fewliterswhile ened resourceoverlap. Whatevertheirorigin,the exisin outcomebetween
difference
both mesocosm and fieldexperimentshave been con- tenceof a characteristic
mesocosm
and
field
experiments
has
importantimplicaducted in experimentalunits of severalhundredliters.
tions
for
amphibian
ecologists.
The impactof scaling,in theabsenceof otherfactors,is
Of even largerrelevanceis our abilityto use any of
capable of affectingresponsesmeasuredby ecologists
the
experimentsto make inferencesabout conditions
(Petersenet al. 1997, 1999). These or otherdifferences
betweenlaboratoryand fieldexperimentscould be re- experiencedby natural populations. Currently,such
inferencesabout anuran communitiesoftenappear to
sponsiblefor an observedswitchin competitivedomibe based on the predominantpatternemanatingfrom
nance betweenexperiments
conductedon leopard frogs
mesocosm experiments(e.g. Wilbur 1997, Resetarits
(Rana pipiens) and wood frogs(R. sylvatica)(Werner
and Fauth 1998, Petrankaand Kennedy 1999). How1998).
ever, if fieldexperimentsare assumed to be the most
While mesocosmand fieldvenues yieldedsignificant
appropriategauge of the naturalcondition(e.g. Coneffectsizes consistentwithcompetition,the effectsize
nell 1983, Schoener 1983, Goldberg and Barton 1992,
frommesocosm studies was severalfoldthat for field
Gurevitchet al. 1992, Carpenter1996), then a much
experiments.In fact, interspecific
field manipulations
different
pictureemerges.Interspecific
competitionmay
wereassociatedwithextremely
small effects,
equivalent occur in natural
populations,but it may oftenbe of
to a 2% changein growth.The outcomeof straightformoderateeffect.Patterns,such as segregateddistribuward densitymanipulationsis highlycontextdependent
tions,previouslyattributedto interspecific
competition
promptingtwo importantquestions:What factorscon- may be due to other
factors(Wellbornet al. 1996).
tributeto differencesin outcome betweenmesocosm
To what extentis the assumptionof greaterrealism
and fieldexperiments?
and, How do resultsfromthese valid forthefieldexperiments
reviewedhere?A particuexperimentsrelate to the conditions experiencedby larly relevantconcern is that the mechanicsof field
naturalpopulations?
manipulationsmay, forwhateverreason,tend to mitiOne potential explanation for the discrepancyin gate the impacts of increased density.One common
outcomes between mesocosm and field experiments criticismis thatthemeshwalls of enclosuresmay allow
could be differences
in stockingdensities(Jaegerand nutrientsand food resourcesto enterthus preventing
Walls 1989). While mesocosm studieshave been criti- depletion.There are two counterarguments
to thissugcized as havingunrealistically
highdensities,we found gestion. First, there are usually tadpoles and other
that stockingdensitieswithinmesocosm experiments grazersliving outside of enclosurewalls so it is not
weresimilarto and tendingto be even lowerthanthose clear, a priori,whetherthe net flowof food resources
foundin fieldexperiments
(Table 1). Experimentscon- and nutrients
will be into or out of enclosures.Second,
ductedin mesocosmsand in the fieldwerecomparable singlespeciesfieldexperiments
conductedunderidentiin otherrespectsas well. The volume of experimental cal conditionshave tendedto yield sizable impactsof
units, the duration of experiments,and the density intraspecific
densitymanipulations(Fig. 4). This differfactorof the manipulationswere each broadly similar ence in outcomesmightbe expectedfroma theoretical
(Table 1, Appendix).
perspective,and demonstratesthatfieldenclosurescan
204
OIKOS 94:1 (2001)
A. 1991.InterC., Rundle,S. D. and Erlandsson,
subjectlarvaeto theimpactsassociatedwithincreased Brdnmark,
snailsand tadpoles:competiactionsbetweenfreshwater
density.
- Oecologia87: 8-18.
tionand facilitation.
inter- Carpenter,
thecontinued
As Morin(1998)has suggested,
havelimited
experiments
S. R. 1996.Microcosm
venue
est of ecologistsin theimpactof experimental
ecology.- Ecoland ecosystem
forcommunity
relevance
ogy77: 677-680.
of the
maystempartlyfroma lack of understanding
of
and importance
J. H. 1983.On the prevalence
Connell,
of theavailablealternaand disadvantages
advantages
evidencefromfieldexperiments.
competition:
interspecific
fromthisfirst
tives.However,the pictureemerging
- Am. Nat. 122: 661-696.
of pH
theeffects
between
does Cummins,
C. P. 1989.Interaction
analysisof venuemediatedtradeoffs
quantitative
in Rana tempoand development
on growth
and density
goals of
conflicted
not matchtheimageof inevitably
- Funct. Ecol. 3: 45-52.
raria L.
presented Dash, M. C.tadpoles.
and realismtypically
precision,
complexity,
on the
and Hota, A. K. 1980.Densityeffects
(Hairston1989a,b,Peters1991,Morin1998).Thisdoes
of Rana tigrina
survival,
growth
rate,and metamorphosis
tadpoles.- Ecology61: 1025-1028.
not mean thatone venueshouldhold primacyover
between
competition
P. A. 1974.Interspecific
it does suggestthattheroleof venue DeBenedictis,
others;however,
tadpolesofRana pipiensandRana sylvatica:an experimenThegoalsofsomeexpercloserscrutiny.
shouldreceive
tal fieldstudy.- Ecol. Monogr.44: 129-151.
in thegeneraRana
venue Dumas,P. C. 1964.Speciespairallopatry
experimental
imentsmake decisionsregarding
178-180.
45:
Ecology
and
Phrynosoma.
will
considerations
Logistical
straightforward.
relatively
fromfield
keystones
potential
Fauth,J. E. 1999.Identifying
in somecasesor
in thelaboratory
working
necessitate
ponds.- Ecol. Lett.2:
data - an examplefromtemporary
in thefieldin others.However,in manyothercases
36-43.
on
phenology
of reproductive
makethe Gascon,C. 1992.The effects
goals willnot,by themselves,
experimental
assemblage
of
traitsin a three-species
larval
performance
cases,
In
those
obvious.
choiceof venueimmediately
Amazonian
tadpoles.- Oikos65: 307-313.
central
option?Or Gascon,C. and Travis,J. 1992.Does the spatialscale of
choosethemostexpedient
shouldecologists
A testwithtadpolesand dragomatter?
shouldtheymorecloselyconsiderthe morecryptic experimentation
- Ecology73: 2237-2243.
nflies.
costs and benefitsof workingin one venue over
andconseA. M. 1992.Patterns
D. E. and Barton,
Goldberg,
another?
in naturalcommunicompetition
quencesof interspecific
At theveryleast,theresultsof our analysissuggest
withplants.- Am.Nat.
offieldexperiments
ties:a review
139:771-801.
thatvenuemediatedimpactson designand outcome
thecommonfrog,
between
R. A. 1991.Competition
in othersystems.While Griffiths,
will be worthinvestigating
and natterjack
toad,Bufo calamita,tadRana temporaria,
to
larvaemaynotapplydirectly
resultson amphibian
level
andinteraction
density
ofcompetitor
poles:theeffect
- Oikos61: 187-196.
on tadpoledevelopment.
thatwe
heresuggest
presented
othertaxa,thefindings
R. A., Edgar,P. W. and Wong,A. L.-C. 1991.
fromadditional
analy- Griffiths,
ifresults
shouldnotbe surprised
and
inhibition
growth
intadpoles:
competition
Interspecific
regarding growthretrieval
to longheldconventions
sesdo notconform
in natterjack
toads,Bufo calamity.- J.
Regardlessof theiroutecologicalexperimentation.
Anim.Ecol. 60: 1065-1076.
R. A., Denton,J. and Wong,A. L.-C. 1993.The
comes,suchanalyseswillhelp ecologistsmakemore Griffiths,
intadpoles:interference
offoodlevelon competition
effect
experiments.
designing
when
decisions
informed
algae? - J. Anim.Ecol. 62:
mediatedby protothecan
274-279.
- We thankJ. Collins,H. zu Dohna,K.
Acknowledgements
J.,Murrow,L. L., Wallace,A. and Walsh,J. S.
0. Ovadia,M. McPeek, Gurevitch,
A. Halverson,
J.Grover,
Freidenburg,
in fieldexperiments.
ofcompetition
1992.A meta-analysis
J.Travis,
0. Schmitz,
A. Richardson,
P. Morin,J.Petersen,
on themanuscript. - Am. Nat. 140: 539-572.
forcomments
M. Urban,and E. Werner
J.A. and Hedges,L. V. 2000.The
J.,Morrison,
Fellowship Gurevitch,
by a DonnellyPostdoctoral
JMK was supported
a metaand predation:
betweencompetition
interaction
Studies,Yale Univ.Our
fromtheYale Inst.forBiospheric
analysisof fieldexperiments.- Am. Nat. 155: 435-453.
by a generousgift
amphibianresearchhas been supported
purpose,deN. G. 1989a.Ecologicalexperiments:
Hairston,
fromMrs.E. S. Dwyerto Yale Univ.
- Cambridge
Univ.Press.
sign,and execution.
N. 1989b.Hardchoicesin ecologicalexperimentaHairston,
tion. - Herpetologica45: 119-122.
methodsfor
Hedges,L. V. and Olkin,I. 1985. Statistical
References
- AcademicPress.
meta-analysis.
J. and Curtis,P. S. 1999.The
and Hedges,L. V., Gurevitch,
use,competition,
Alford,R. A. 1999.Ecology:resource
ecology.ratiosinexperimental
ofresponse
meta-analysis
R. W. and Altig,R. (eds),
- In: McDiarmid,
predation.
Ecology80: 1150-1156.
Tadpoles:the biologyof Anuranlarvae.ChicagoUniv.
ofkinship
A. R. 1994.Theeffects
Hokit,D. G. andBlaustein,
Press,pp. 240-278.
in tadpolesofRana cascadac.
anddevelopment
on growth
in
effects
Alford,R. A. and Wilbur,H. M. 1985.Priority
- Evolution
48: 1383-1388.
Bufo
between
competition
pondcommunities:
experimental
guildsand
R. G. andWalls,S. C. 1989.On salamander
Jaeger,
and Rana. - Ecology 66: 1097-1105.
45: 111-119.
- Herpetologica
ecologicalmethodology.
in
variation
K. A. and Gill,D. E. 1983.Interpreting
Berven,
reverses
A. R. 1999.Pathogen
J.M. and Blaustein,
Kiesecker,
traits.- Am.Zool. 23: 85-97.
life-history
- Ecology80:
betweenlarvalamphibians.
competition
in tempoeffects
J. 1996.Priority
L. and Margalit,
Blaustein,
2442-2448.
rarypools:natureand outcomeof mosquitolarvae-toad
S. E. 1995.Modelingnature:episodesin thehisdependon orderof entrance.- J. Kingsland,
tadpoleinteractions
2nded. - ChicagoUniv.Press.
ecology,
toryofpopulation
Anim.Ecol. 65: 77-84.
S. J. 1997.Bullfrog
(Rana catesbeiana)invasion
and Kupferberg,
effects
W. Y. 1969.An analysisof density
Brockelman,
river:the role of larvalcompetition.
of a California
predation in Bufo americanustadpoles. - Ecology 50:
Ecology78: 1736-1751.
632-644.
OIKOS 94:1 (2001)
205
Lawler, S. P. and Morin, P. J. 1993. Temporal overlap,
competition,and priorityeffectsin larval anurans.- Ecology 74: 174-182.
Martinez,1. P., Alvarez,R. and Harraez, M. P. 1996. Growth
and metamorphosisof Rana perezi in culture:effectsof
larval density.- Aquaculture 142: 163-170.
Mertz, D. B. and McCauley, D. E. 1980. The domain of
laboratoryecology. - Synthese43: 95-110.
Morin, P. J. 1983. Predation,competition,and the composition of larval anuran guilds. - Ecol. Monogr. 119-138.
Morin, P. J. 1986. Interactionsbetweenintraspecific
competition and predationin an amphibianpredator-prey
system.
- Ecology 67: 713-720.
Morin, P. J. 1987. Predation,breedingasynchrony,and the
outcome of competitionamong treefrogtadpoles. - Ecology 68: 675-683.
Morin, P. J. 1989. New directionsin amphibiancommunity
ecology. - Herpetologica45: 124-128.
Morin,P. J. 1998. Realism,precision,and generality
in experimentalecology. - In: Resetarits,W. R. and Bernardo,J.
(eds), Ecological experiments:
issues and perspectives.OxfordUniv. Press,pp. 50-70.
Morin,P. J. and Johnson,E. A. 1988. Experimentalstudiesof
asymmetric
competitionamong anurans.- Oikos 53: 398407.
Morin,P. J.,Lawler,S. P. and Johnson,E. A. 1988. Competition betweenaquatic insects and vertebrates:interaction
strengthand higher order interactions.- Ecology 69:
1401-1409.
Newman, R. A. 1998. Ecological constraintson amphibian
metamorphosis:
of temperature
interactions
and larvaldensity with responsesto changingfood level. - Oecologia
115: 9-16.
Odum, E. P. 1984. The mesocosm.- Bioscience34: 558-562.
Paine, R. T. 1992. Food-web analysisthroughfieldmeasurement of per-capita interactionstrength.- Nature 355:
73-75.
Parris,M. J. and Semlitsch,R. D. 1998. Asymmetric
competition in larval amphibiancommunities:conservationimplications for the northerncrawfishfrog, Rana areolata
circulosa.- Oecologia 116: 219-226.
Peacor, S. D. and Werner,E. E. 1997. Trait-mediated
indirect
interactionsin a simpleaquatic food web. - Ecology 78:
1146-1156.
Pehek, E. L. 1995. Competition,pH, and the ecologyof Hyla
andersonii.- Ecology 76: 1786-1793.
Peters,R. H. 1991. A critiqueforecology.- CambridgeUniv.
Press.
Petersen,J. E., Chen, C.-C. and Kemp, W. M. 1997. Scaling
aquatic primaryproductivity:
experimentsundernutrientand light-limited
conditions.- Ecology 78: 2326-2338.
Petersen,J. E., Cornwell, J. C. and Kemp, W. M. 1999.
Implicit scaling in the design of experimentalaquatic
ecosystems.- Oikos 85: 3-18.
Petranka,J.W. and Kennedy,C. A. 1999. Pond tadpoleswith
generalizedmorphology:is it timeto reconsidertheirfunctional roles in aquatic communities?- Oecologia 120:
621-631.
Relyea, R. A. and Werner,E. E. 1999. Quantifyingthe relation betweenpredator-inducedbehavioral responses and
growth performancein larval anurans. - Ecology 80:
2117-2124.
Reques, R. and Tejedo, M. 1997. Reaction normsfor metamorphic traitsin natterjacktoads to larval densityand
pond duration.- J. Evol. Biol. 10: 829-851.
Resetarits,W. R. and Fauth, J. E. 1998. From cattletanksto
Carolina bays: the utilityof model systemsforunderstanding natural communities.- In: Resetarits,W. R. and
Bernardo,J. (eds), Ecological experiments:
issues and perspectives.OxfordUniv. Press,pp. 133-151.
Riha, V. F. and Berven,K. A. 1991. An analysisof latitudinal
variationin the larvaldevelopmentof thewood frog(Rana
sylvatica).- Copeia 1991: 209-221.
206
Rosenberg, M. S., Adams, D. C. and Gurevitch,J. 1997.
MetaWin:statisticalsoftwareformeta-analysis
withresampling tests.Ver. 1.0. - Sinauer.
Rowe, C. L. and Dunson, W. A. 1994. The value of simulated
pond communitiesin mesocosmsforstudiesof amphibian
ecologyand toxicology.- J. Herpetol.28: 346-356.
Sarnelle,0. 1997. Daphnia effectson microzooplankton:
comparisonsof enclosureand whole-lakeresponses.- Ecology
78: 913-928.
Schoener,T. W. 1983. Field experiments
on interspecific
competition.- Am. Nat. 122: 240-285.
Semlitsch,R. D. 1993. Asymmetriccompetitionin mixed
populations of tadpoles of the hybridogenetic
Rana esculentacomplex. - Evolution47: 510-519.
Semlitsch,R. D. and Caldwell,J.P. 1982. Effectsof densityon
growth,metamorphosisand survivorshipin tadpoles of
Scaphiopusholbrooki.- Ecology 63: 905-91 1.
Semlitsch,R. D. and Reyer, H.-U. 1992. Performanceof
tadpoles fromthe hybridogenetic
Rana esculentacomplex:
interactionswith pond dryingand interspecific
competition. - Evolution46: 665-676.
Skelly,D. K. 1995a. A behavioral trade-offand its consequencesforthedistribution
of Pseudacristreefrog
larvae. Ecology 76: 150-164.
Skelly, D. K. 1995b. Competitionand the distributionof
springpeeperlarvae. - Oecologia 103: 203-207.
Smith,D. C. 1983. Factors controllingtadpole populationsof
the chorus frog (Pseudacris triseriata)on Isle Royale,
Michigan. - Ecology 64: 501-510.
Smith,D. C. 1987. Adult recruitment
in chorusfrogs:effects
of size and date of metamorphosis.- Ecology 68: 344350.
Smith, D. C. 1990. Population structureand competition
among kin in the chorus frog (Pseudacris triseriata).Evolution44: 1529-1541.
Smith-Gill,S. J. and Gill, D. E. 1978. Curvilinearities
in the
competitionequations: an experiment
withranidtadpoles.
- Am. Nat. 112: 557-570.
Sredl,M. J. and Collins,J. P. 1991. The effectof ontogenyon
interspecific
interactionsin larval amphibians.- Ecology
72: 2232-2239.
Sredl, M. J. and Collins, J. P. 1992. The interactionof
predation,competition,
and habitatcomplexity
in structuring an amphibiancommunity.- Copeia 1992: 607-614.
Steinwascher,K. 1978. Interference
and exploitationcompetition among tadpoles of Rana utricularia.- Ecology 59:
1039-1046.
Tejedo, M. and Reques, R. 1992. Effectsof egg size and
densityon metamorphictraitsin tadpolesof thenatterjack
toad (Bufo calamita). - J. Herpetol.26: 146-152.
Tejedo, M. and Reques, R. 1994. Plasticityin metamorphic
traitsof natterjacktadpoles: the interactiveeffectsof densityand pond duration.- Oikos 71: 295-304.
Travis,J., Keen, W. H. and Julianna,J. 1985. The effectsof
multiple factors on viabilityselection in Hyla gratiosa
tadpoles. - Evolution39: 1087-1099.
Warner,S. C., Dunson, W. A. and Travis,J. 1991. Interaction
of pH, density,and priorityeffectson the survivorship
and
growthof two species of hylidtadpoles. - Oecologia 88:
331-339.
Warner,S. C., Travis,J. and Dunson, W. A. 1993. Effectof
pH variation on interspecific
competitionbetween two
species of hylidtadpoles. - Ecology 74: 183-194.
Wellborn, G. A., Skelly, D. K. and Werner,E. E. 1996.
Mechanismscreatingstructureacross a freshwater
habitat
gradient.- Annu. Rev. Ecol. Syst. 27: 337-363.
Werner,E. E. 1986. Amphibianmetamorphosis:growthrate,
predationrate,and the optimalsize at transformation.
Am. Nat. 128: 319-341.
Werner,E. E. 1992. Competitiveinteractionsbetweenwood
frogand northernleopard froglarvae: the influenceof size
and activity.- Copeia 1992: 26-35.
OIKOS 94:1 (2001)
Werner,E. E. 1998. Ecological experimentsand a research
W. R. and
programin community
ecology.- In: Resetarits,
Bernardo,J. (eds), Ecological experiments:
issues and perspectives.Oxford Univ. Press,pp. 3-26.
Werner, E. E. and Anholt, B. A. 1996. Predatorinduced behavioral indirecteffects:consequencesto competitiveinteractionsin anuran larvae. - Ecology 77: 157169.
Werner,E. E. and Glennemeier,K. S. 1999.Influenceof forest
of several
canopy cover on the breedingpond distributions
amphibianspecies. - Copeia 1999: 1-12.
Wilbur,H. M. 1976. Density-dependent
aspects of metamorphosis in Ambystomaand Rana sylvatica.- Ecology 57:
1289-1296.
Wilbur, H. M. 1977a. Density-dependent
aspects of growth
and metamorphosisin Bufo americanus.- Ecology 58:
196-200.
Wilbur,H. M. 1977b.Interactionsof food leveland population
densityin Rana sylvatica.- Ecology 58: 206-209.
Wilbur,H. M. 1989. In defenseof tanks. - Herpetologica45:
122-123.
Wilbur, H. M. 1997. Experimentalecology of food webs:
ponds. - Ecology78: 2279complexsystemsin temporary
2302.
Wilbur, H. M. and Alford,R. A. 1985. Priorityeffectsin
responsesof Hyla to Bufo
experimental
pond communities:
and Rana. - Ecology 66: 1106-1114.
Wiltshire,D. J. and Bull, C. M. 1977. Potentialcompetitive
bibroniand P.
interactions
betweenlarvae of Pseudophryne
semimarmorata
(Anura: Leptodactylidae).- Aust. J. Zool.
25: 449-454.
Woodward, B. D. 1987. InteractionsbetweenWoodhouse's
toad tadpoles (Bufo woodhousii)of mixedsizes. - Copeia
1987: 380-386.
Wootton,T. W. and Pfister,C. A. 1998. The motivationand
in ecology. - In: Resetarits,W. R.
contextof experiments
issues and
and Bernardo,J. (eds), Ecological experiments:
perspectives.OxfordUniv. Press,pp. 350-369.
the authors,
Appendix.Fifty-twostudiesincludedin meta-analysesof competitionamong larval anurans. For each reference,
codes definedat bottom of table), and experimentalvenue (field,lab, or
year of publication,species included (four-letter
comparisonsgleaned fromeach study.
and interspecific
mesocosm) are followedby the numberof intraspecific
Author(s)
Year
Species
Venue
No. of comparisons
Intraspecific
Alfordand Wilbur
Bervenand Gill
Blausteinand Margalit
Brockelman
Bronmarket al.
Cummins
Dash and Hota
DeBenedictis
Gascon
Gascon and Travis
Griffiths
Griffiths
et al.
Griffiths
et al.
Hokit and Blaustein
Kieseckerand Blaustein
Kupferberg
Lawler and Morin
Martinezet al.
Morin
Morin
Morin et al.
Newman
Parrisand Semlitsch
Peacor and Werner
Pehek
Reques and Tejedo
Relyea and Werner
Riha and Berven
Semlitsch
Semlitschand Caldwell
Semlitschand Reyer
Skelly
Skelly
Smith
Smith-Gilland Gill
Sredl and Collins
Sredl and Collins
Steinwascher
Tejedo and Reques
Tejedo and Reques
Travis et al.
Warneret al.
Warneret al.
OIKOS 94:1 (2001)
1985
1983
1996
1969
1991
1989
1980
1974
1992
1992
1991
1991
1993
1994
1999
1997
1993
1996
1986
1987
1988
1998
1998
1997
1995
1997
1999
1991
1993
1982
1992
1995a
1995b
1990
1978
1991
1992
1978
1992
1994
1985
1991
1993
BUAM, RASP
RASY
BUVI
BUAM
RATE
RATE
RATI
RAPI, RASY
EPFE, OSTA, PHTO
RAUT
BUCA, RATE
BUCA, RATE
BUCA, RATE
RACS
HYRE, RACS
HYRE, RABO, RACT
BUWO, PSCR
RAPE
PSCR
HYVE, PSCR
BUWO, HYAN
SCCO
RABL, RASP
RACL, RACT
HYAN, HYVE, RASP
BUCA
RACL, RACT
RASY
RAES, RALE
SCHO
RAES, RALE
PSCR, PSTR
PSCR, RACL
PSTR
RAPI, RASY
PSTR
HYEX
RAUT
BUCA
BUCA
HYGR
HYFE, HYGR
HYFE, HYGR
M
L
L
F
M
L
L
F
M
M
M
M
M
L
M
F
M
L
M
M
M
L
M
M
M
L, M
F
L
M
L
M
F
F
F
L
F
F
L
L
M
F
M
M
15
I
2
I
4
2
2
3
2
2
6
2
3
2
1
1,1
6
4
4
2
7
8
1
2
4
3
2
4
6
4
Interspecific
2
8
6
4
2
2
2
2
2
1
1
1
4
2
6
2
7
3
8
8
207
Appendix(Continued)
Author(s)
Year
Species
Venue
No. of comparisons
Intraspecific
Werner
Wernerand Anholt
Wernerand Glennemeier
Wilbur
Wilbur
Wilbur
Wilburand Alford
Wiltshireand Bull
Woodward
1992
1996
1999
1976
1977a
1977b
1985
1977
1987
RAPI, RASY
RACA, RACL
RAPI, RASY
RASY
BUAM, RAPA
RASY
BUAM, HYCR, RASP
PDBI, PDSE
BUWO
L
M
F
F
L, F
L
M
F
L
4
4
5
5,5
3
2
2
Interspecific
4
8
0,3
2
Species codes. BUAM Bufoamericanus,BUCA Bufocalamita,BUVI Bufoviridis,BUWO Bufowoodhousii,
EPFE Epipedobates
HYCR Hyla chrysoscelis,
HYEX Hyla eximia,HYFE Hylafemoralis,HYGR Hyla gratiosa,
femoralis,HYAN Hyla andersonii,
HYRE Hyla regilla,HYVE Hyla versicolor,OSTA Osteocephalustaurinus,PHTO Phyllomedusatomopterna,
PDBI Pseudophryne
bibroni,PDSE Pseudophryne
semimarmorata,
PSCR Pseudacris(= Hyla) crucifer,
PSTR Pseudacristriseriata,RABL
Rana blairi,RABO Rana boyl/i,RACL Rana clamitans,RACS Rana cascadae, RACT Rana catesbeiana,RAES Rana esculenta,
RALE Rana lessonae,RAPA Rana palustris,RAPE Rana perezi,RAPI Rana pipiens,RASP Rana sphenocephala,
RASY Rana
sylvatica,RATE Rana temporaria,RATI Rana tigrina,RAUT Rana utricularia,SCCO Scaphiopuscouchi,SCHO Scaphiopus
holbrooki.
208
OIKOS 94:1 (2001)