Nordic Society Oikos
Trophic Control across a Natural Productivity Gradient with Sap-Feeding Herbivores
Author(s): Maria Uriarte and Oswald J. Schmitz
Reviewed work(s):
Source: Oikos, Vol. 82, No. 3 (Sep., 1998), pp. 552-560
Published by: Wiley-Blackwell on behalf of Nordic Society Oikos
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OIKOS 82: 552-560. Copenhagen1998
gradientwith
Trophiccontrolacrossa naturalproductivity
herbivores
sap-feeding
Maria Uriarteand Oswald J. Schmitz
0. J. 1998.Trophiccontrolacrossa naturalproductivity
M. and Schmitz,
Uriarte,
- Oikos83: 552-560.
herbivores.
withsap-feeding
gradient
damage
herbivore
playin controlling
therolethatpredators
examining
Experiments
and
ofproductivity
effect
to plantbiomassarecommonin ecology.The interactive
remains
however,
ecosystems,
predationon standingplantbiomassin terrestrial
on the
and productivity
Herewe examinetheroleof predation
poorlyunderstood.
are thedominant
herbivores
inflict
on goldenrod.
Sap feeders
damagesap-feeding
and does notcarrymanyof
in thiscommunity.
Sap is poorin nutrients
herbivores
shouldthenbe sensitive
Sap-feeders
defense
ofgoldenrod.
thechemical
compounds
to theproduction
of chemical
impervious
and relatively
to changesin productivity
across
on goldenrod
ofpredation
and fertilization
theeffect
We examined
defenses.
on
of predators
We foundthattheeffect
and successional
gradient.
a productivity
Someof these
withincreasing
productivity.
herbivore
damageincreased
controlling
proposedby Oksanenwhile
hypothesis
withtheExploitation
resultsare consistent
of trophic
controlacrossproductivity
mechanisms
alternative
othersseemto reflect
siteswhileplant
Top-downcontrolwas strongin highproductivity
gradients.
interactions
mayhave obscuredany patternof top-downcontrolin
competitive
sites.
and lowproductivity
intermediate
Studies, Yale
M. Uriarteand 0. J. Schmitz,School of Forestryand Environmental
Univ.,370 ProspectSt., New Haven, CT 06511, USA (presentaddressof MU: Section
of Ecology and Systematics,Corson Hall, Cornell Univ.,Ithaca, NY 14853, USA
[mu16@cornell.edu]).
Many studieshave examinedthe role predatorsplay in
food web dynamics(Sih et al. 1985,Brettand Goldman
1996,Polis and Winemiller1996). This body of research
indicatesthat theremay be considerablevariationin
the influencetop predatorsexert withinand among
fieldsites.An importantchallengeis to understandthe
(sensu Hunter and Price
source of this heterogeneity
1992) in food web dynamics.
recognizedby
One potentialsource of heterogeneity
early theory(Oksanen et al. 1981) is the net primary
of a location.Accordingto thistheory,the
productivity
determinesthe numberof trophic
level of productivity
levels that persist in a given system.For instance,
energy
willhave insufficient
systemsof low productivity
to support herbivoresand consequentlyno predator
increases,
effectsshould be observed.As productivity
enablingherbivorepopulationsto gain a footholdin a
system,we should see a correlatedincrease in the
degree to which plants are limitedby herbivoreconsumers (Oksanen et al. 1981). In highlyproductive
carnivorespersist,limitingherbivorepopenvironments
ulationsand helpingplants overcomestronglimitation
by herbivoreconsumers.Hence carnivoresexert an
indirectmutualisticeffecton plantsvia top-downcontrol of herbivorepopulations.
Despite the key role that Oksanen et al's (1981)
exploitation hypothesishas played in shaping our
thinkingof trophicinteractions,few studies describe
how top-downeffectschange across space or time in
three trophic level systems(but see Carpenter and
Kitchell 1987, Hartvingtsenet al. 1995, Wardle et al.
is the succes1995). One determinantof productivity
sional state of the field. In our study system,early
successionalfieldshave typicallysustainedagricultural
Accepted 19 January1998
? OIKOS 1998
Copyright
ISSN 0030-1299
Printedin Ireland - all rightsreserved
552
OIKOS 82:3 (1998)
exploitation,have low soil nutrientcontent,and exhibit
low productivity.Productivityseems to increase with
successionaltime.We used the naturalchangesin productivityacross a successionalgradientto examinethe
We studiedthetrophic
variationin trophicinteractions.
interactionsin goldenrod(Solidago rugosa) communities dominatedby sap-feedinginsectsalong a successional productivity
gradient.
Oksanen's model assumesthat(a) grazersmove over
a largearea, and (b) grazershave highenergydemands.
Sap-feedersare immobileduringtheirlarval stagewhen
theyare mostdamagingto theplantsand vulnerableto
predationso theydo not complywiththe firstassumption of the Exploitation hypothesis.However, their
sedentarylarvae and thepoor nutritional
qualityof sap
necessitatea fairlyproductivehost and make them
herbivoreswith"high energydemands" relativeto the
nitrogenavailable in the host. Host plants are more
nitrogenrich in highlyproductiveenvironmentsand
thus more likelyto meet the energyrequirementsof
sap-feeders.
In summary,sap-feedersin our systemmeetsome of
of grazersin Oksanen's model but
the characteristics
not others. Our observed patterns of variation in
do not always suptrophicdynamicswithproductivity
alterportOksanenet al.'s (1981) hypothesissuggesting
native mechanisms of trophic control across
productivity
gradientsfor sap feedingherbivores.
Naturalhistory
timefortwo reasons.First,theirsuccessionaltrajectory
is well documented(Lutz 1928,Bard 1952). Second,the
natural historyof many of the goldenrodinsectshas
been studied(Messina 1978, Messina and Root 1980,
McBrien et al. 1983, Abrahamsonand McCrea 1986,
McEvoy 1986, 1988,Cappuccino 1987, 1991,Abrahamson et al. 1988, Hamilton 1989, Root and Cappuccino
1992, Abrahamsonand Weis 1996) and it is relatively
simpleto manipulatecommunitiesin the field.
There are linkagesbetweenthe successionalstage of
a field,and the two variablesthathave been linkedto
trophiccontrol mechanisms:its productivityand the
documentedtrophicstructureof the community.For
example,changesin nutrientavailabilityduringsuccession can affectherbivorepopulationdynamics.Studies
on carbon and nitrogencyclingin some old-fieldshave
shown that nitrogenavailabilitymay change during
succession(Inouye et al. 1987, Tilman 1986,Zak et al.
1990). Increased nitrogenavailabilityhas a positive
effecton the densitiesof some goldenrodherbivores
(Meyer and Root 1996).
Both productivityand successional stage may also
affectthe lightregimeof a goldenrodstand and, as a
consequence,the mechanismsof trophicdynamicsincludingherbivoreand predatorbehavior.Competition
for light during succession affectsthe allocation of
nitrogento various parts of the plant. This allocation
patternaffectsthe foragingbehaviorof both herbivores
and predators.Researchon goldenrodphysiologyindicates thatleafnitrogenconcentration
is proportionalto
lightincidence(Hirose and Werger1987, Schievinget
al. 1992). Goldenrodtendsto formdense monocultures
in mid- and late-successionalstages or at highlyproductivesites.As a result,lightincidenceto the middle
and lower leaves of thick stands is low which cause
nitrogento concentratein the canopy of the goldenrod
stand. Foragerstryingto optimizetheirnitrogenintake
willmostlikelymove to thehigherpartsof theplantas
theclonesgetmoredense,but foragingat thetop of the
plant is costly. Insects must travel higherthan they
would have to in sparse stands, shade may not be
readilyavailable,and vulnerability
to predatorsmay be
greater(Loeffler1992).
This studywas conducted at the Yale-Myers ExperimentalForestin Union, Connecticut,USA in old fields
dominated by goldenrod (Solidago rugosa) but also
inhabited by Poa pratensis,Aster novaeangliae,Trifoliumrepens,Daucus carota and Phleumpratense.Herbivorous insects include the generalist grasshopper
Melanoplusfemurrubrum,
the grass specialistgrasshopthe specialist goldenrod
per Chorthippuscurtipennis,
beetle Trirhabdavirgata,the generalistsap-feedingspittlebugPhilaneusspumarius,the sap-feedingplant bugs
Leptoternadolobrata(grass),Lyguslineolarisand Lopidea media(goldenrod).Thereare also assortedpentatomid bugs and various chrysomelidbeetles. Predators
includethe jumpingspidersPhidippusrimator,various Methods
small lycosids,i.e. Schizocosa sp., Pirata sp., the nursExperimentaldesign
ery web spider Pisaurina mira, and the crab spider
Misumenavatia.
We conducteda seriesof experiments
in threefieldsof
Goldenrod is a native,clonal rhizomatousperennial increasingsuccessionalage: field1 was plowed in 1995;
(Cronquist 1980, Werner et al. 1980) with a highly field2 was last cultivatedin 1985; and field3 in 1979.
diverseinsectfauna ( > 100 species) (Root 1996). This These fieldsrepresentearly-,mid-and late-successional
plant is highlysuccessfulin disturbedenvironments, stages in thisexperiment.Field 3 had the highestprocommonlydominatingold fieldsthroughouttheNorth- ductivitywhile field 2 had the lowest. Field 1 had
easternUnitedStates.Goldenrodfieldsprovidean ideal surprisingly
high plant biomass, perhaps owing to the
systemfor studyingtrophicdynamicsin successional competitivereleasecreatedby plowing.
OIKOS 82:3 (1998)
553
made et al. 1980,Mumtazand Menzer1986,Louda and
We usedstandard0.1 m x 1 m tallenclosures
(Belovsky1986,Ritchieand Rodman 1996),is rapidlydegraded(Miyamotaand
of aluminumscreening
(Joneset al. 1986).
Tilman 1992, Schmitz1994) to createexperimentalMikami1983)andis notphytotoxic
The
inmid-June.
changewiththedevelopmental
at eachofthethreefields
Trophicinteractions
communities
in all threefields.We stageof insectsand plantphenology(Belovskyand
wereplacedrandomly
exclosures
treat- Slade 1993,Schmitz1997).Insectemergence
at oursite
withone of thefollowing
stockedtheenclosures
alone is concentrated
at two time periods:early insects
ments:(1) no insects("Control"),(2) herbivores
and predators emergein late May or earlyJunewhilelate insects
and (3) bothherbivores
("Herbivores")
periods,
10 times. emerge
thesetwoemergence
in July.To reflect
was replicated
Each treatment
("Predators").
werestockedtwice:onceat thebeginvia a trophiccas- theexperiments
If top-downcontrolwas occurring
(Hairstonet al. ningoftheseason,in earlyJuneand againin lateJuly
to classicaltheory
cade,thenaccording
startedto emerge.
thatHerbivore whenthe late summerherbivores
1960,Oksanenet al. 1981)we expected
werecountedat regularintervals
plotswouldcontainless plantbiomassthanControl Insectsin exclosures
on to ensure that herbivoreand predatornumbers
inflicted
plotsbecauseofthedamagethatherbivores
used
Manyoftheinsects
inthefields.
densities
the plants.We also expectedthatin Predatorplots, matched
of herbi- to stock the cages earlyin the season declinedin
wouldreleasesomeof thepressure
predators
We conducted
resulting abundanceor diedlaterin thesummer.
density,
herbivore
voreson plantsbyreducing
to montheexperiment
throughout
fieldsurveys
weekly
plots.
plantbiomassthanin Herbivore
in higher
cageswerestockedat thedensities itor how the abundanceof variousinsectschanged
The experimental
thesummer.
werefoundin field throughout
and predators
thattheherbivores
in late Sepwe sampledthe threefields The plantsin each cage wereharvested
surveys.Beforestocking,
Non-goldenhad flowered.
afterthegoldenrod
the tember
anddetermined
surveys
sweepnet
usingindependent
foreach site.In rod plantswereclippedto groundlevel.Goldenrod
and predators
of herbivores
densities
and plantsweredug out of the soil to includerootsand
fieldsweresampledin themorning
thesesurveys,
shoots,
structures,
becauseinsectsaremostactiveat rhizomes.Goldenrodbelowground
in thelateafternoon
whileall non-goldenwereseparated
area at leavesandflowers
thistime.We swept30 timesovera 0.5-iM2
randomlocationsin each of thethreefields.We con- Table1. Numberofindividuals
ofeacharthropod
speciesand
at leasttwicea relativeabundances(in parentheses)
thesummer,
in
throughout
ductedsurveys
stockedin exclosures
fields.Densiinsectdensi- early(1), medium(2), and late(3) successional
was madeto homogenize
week.No effort
each
sweepnetsampleswithin
wereobtainedbyrepeated
tiesacrossfieldsbecauseour intentwas to determine ties
field.
and trophicdyin productivity
thenaturalvariability
namiceffectsarisingfromexistingfieldconditions. Insectsstockedin early Field 1 Field2 Field3
Insectsthatwerepresentin morethan 50% of the summer
surveysampleswerestockedin each of thecages at Leafchewers
2 (12%)
Table 1 liststhespeciesthat
0 (0)
0 (0)
larvae
Trirhabda
theirnormalfielddensities.
1 (0.9%) 1 (0.6%)
caterpillar0 (0)
Lepidoptera
in eachof thefieldsand
wereusedto stockenclosures
at which Phloem-feeders
abundances
theabsoluteand relative
provides
dolobrata 1 (14%) 2 (18%) 4 (23%)
Leptoterna
theywerefoundin eachfield.
1 (14%) 2 (18%) 4 (23%)
sp.
Adelphocoris
3 (43%) 3 (27%) 3 (17%)
Leafhoppers
in
of eachtreatment
In additionto the10 replicates
of Xylem-feeders
a secondset of replicates
each field,we fertilized
spumarius 2 (29%) 3 (27%) 3 (18%)
Philaneus
(plantsonly)with20:20:20NPK at
Controlexclosures
(nymphs)
the Predators
increases
10 g m-2 yr-l. Thislevelof fertilization
1
1
0
of the fieldand does not have direct Orbweaver
productivity
1
1
2
Salticidspider
on planttissue(Schmitz1997).Thisset
effects
negative
I
2
Field
3
Field
in
late
sum-Field
Insects
stocked
the degreeof
of exclosureswas used to determine
mer
those
that
We
expected
on plants.
resourcelimitation
wouldhavehigherbiomass Leafchewers
plotstreatedwithfertilizer
femurru- 1 (14%) 2 (22%) 0 (0)
Melanoplus
than those leftuntreatedand that this increasein
brum
limitation Chorthippus
thedegreeof nutrient
biomasswouldreflect
0 (0)
curtipennis1 (14%) 0 (0)
limitsa site,the
1 (11%) 1 (12%)
0 (0)
of the field.The moreproductivity
Chrysomelidae
more its biomasswill increasewhenprovidedwith Phloemfeeders
1 (14%) 1 (11%) 0 (0)
Pentatomidae
in theformof fertilizer.
additionalnutrients
2 (28%) 2 (22%) 1 (12%)
Lopideasp.
All controlcages weresprayedwitha pyrethroidXylem-feeders
2 (28%) 3 (33%/o) 4 (50%/6)
Philaneusspumarius
insectlarvae
everytwo weeksto eliminate
insecticide
(adults)
This
insectifrom
from
years.
previous
eggs
emerging
Predators
on goldenrod
growth(Root 1996),
cide has no effect
1
1
I
Salticidaespider
in animalsor plants(Onkawa
does notbioaccumulate
554
OIKOS 82:3 (1998)
(A)
80
70
w
c 60
0
FD
w
50
U LEAFCHEWERS
40
30
U PHLOEM
FEEDERS
was the
(Fig. 1). Philaneusspumarius,a xylem-feeder,
most abundant herbivorein the late successionalfield
during late summer,although densitiesin the three
fieldswere similarin earlysummer.Similarly,phloemfeeders(e.g. Miridae) became less abundantin the late
fieldtowardsthe end of the summer,althoughdensities
were similarin all threefieldsin July.
XYLEM
FEEDER
~~~~~~~~~0
o(0)20
on goldenrodbiomass
Effectof trophicstructure
in unfertilized
plots
10
0
According to the exploitationhypothesis,herbivores
should decrease the biomass of naturallyoccurring
SUCCESSIONAL STAGE
vegetationin the absence of predators.Predatorscan
increasevegetationbiomass by reducingherindirectly
(B)
bivore
and releasingpressureon vegetation.
foraging
60
(n
The strength
of thiseffectshouldvaryacrossproductivw
a: 50
ity gradients.We comparedthe biomass of vegetation
0
in Control, Herbivores,and Predator treatmentsto
W
LEAFCHEWERS
IN~~~~~~~~
on
obtaina measureof theeffectof trophicinteractions
FEEDERS
M PHLOEMA
vegetationbiomass.
FEEDERS
O:1XYLEM
020
effecton goldenTrophic structurehad a significant
IIL
rod shoot biomass in the middle and late successional
o0
fieldsbut not in the early ones (Fig. 2A, Table 2).
0
Herbivores significantlydecreased goldenrod shoot
EARLY
MID
LATE
biomass onlyin the late successionalfield.The effectof
SUCCESSIONAL STAGE
increasedgoldenpredatorson herbivoressignificantly
in
and late-succesthe
midbiomass
both
rod
shoot
of relative
abundanceof threefeeding
guilds
Fig. 1. Patterns
in
fieldsdominated
in early,middle,and late successional
by sional field. Flower biomass varied significantly
in early(A) and latesummer
(B).
goldenrod
response to trophicstructurein the mid-successional
but not in the earlyor late fields(Fig. 2B, Table 2). In
rod plants were harvestedand their biomass pooled this case the introductionof predators significantly
together.All plantmaterialwas driedat 60'C for48 h, increasedgoldenrodflowerbiomass above the herbivore treatment.Belowgroundbiomass did not signifithenweighed.
cantly differamong trophic treatmentsfor all three
fields.
EARLY
MID
LATE
Statisticalanalysis
on goldenrodbiomass
Statisticalanalyses of all data were performedusing Effectof fertilization
SYSTAT forWindowsversion5 (Wilkinson1992). We
effecton goldenrodshoot
Fertilizerhad a significant
of fertilization
used MANOVA to testfor significance
biomass in the earlyand mid fields(Fig. 3A, Table 2),
and trophicstructureon goldenrodshoot, flowerand
but not in the late-successionalfield.Flower biomass
root biomass. We conductedplanned comparisonsbedid not respond to fertilizationin any of the fields
tween all possible pairs of Control, Herbivores and
(Table 2), and the response of belowgroundbiomass
in
Predatortreatments.
We also compared differences
in the mid-successionalfieldonly (Fig.
was significant
the biomass of all non-goldenrod plants, mostly
3B, Table 2).
plots.The biomass
grasses,includedin theexperimental
of non-goldenrodplants was pooled forthis analysis.
Otherplantbiomass
The biomass of non-goldenrodplants in the plots was
not significantly
affectedby trophicstructureor fertilization (Fig. 2C, 3C). Otherplant biomass variedfrom
Patternsof herbivoreabundance
8% in the late-successionalsite to 45% in the mid-successionalfield.Non-goldenrodvegetationincludedboth
phloem-feeders
The relative
abundanceofleaf-chewers,
the summer grassesand otherforbs.
and xylem-feeders
changedthroughout
Results
OIKOS 82:3 (1998)
555
(A) EARLYSUCCESSIONAL
FIELD
50
40'
MID-SUCCESSIONAL
FIELD
LATESUCCESSIONAL
FIELD
40'
40'
30'
~20'2
~20,
10,
0
CONTROL
00
HERBIVORE PREDATOR
(B) EARLYSUCCESSIONAL
FIELD
l0,
12
u
1o
10(
CONTROL
HERBIVORE PREDATOR
__
0
(C)
2
CONTROL HERBIVOREPREDATOR
of
lo-
b~~~~~~~~
0
2'
~~~~~~~~~~~~~~~~~~~~12
a
a
HERBIVORE PREDATOR
LATESUCCESSIONAL
FIELD
MID-SUCCESSIONAL
FIELD
o
CONTROL
0
EARLYSUCCESSIONAL
FIELD
2
CONTROL HERBIVOREPREDATOR
0
CONTROL HERBIVOREPREDATOR
LATESUCCESSIONAL
FIELD
MID-SUCCESSIONAL
FIELD
10,
2
0
..
CONTROL HERBIVOREPREDATOR
0
CONTROL HERBIVOREPREDATOR
0
CONTROL HERBIVOREPREDATOR
oftrophic
structure
on S. rugosashoot(A), flower
Fig.2. Effect
(B), and(C) non-goldenrod
plantbiomass.Meansandstandard
errorsin early,middle,and late successional
fieldsare presented.
Different
lettersdenotestatistically
differences
significant
(ANOVA,p < 0.05).
Discussion
Classical food chain theory(Oksanen et al. 1981) predictsa straightforward
relationshipbetweenproductivityand the existenceof top-downcontrolvia a trophic
cascade. However,thereis certainskepticismthat topdown controlwill occur in natural terrestrial
systems
because of the heterogenousrangeof factorsthatlikely
interactionsremitigatethe strongconsumer-resource
quired to produce trophiccascades (Strong 1992,Polis
and Strong1996). We observedtop-downcontrol,man-
556
ifestas a tropiccascade in goldenrodshoot biomass,in
our experimentalsystembut only in the late-successional field.Our resultsindicatethat the likelihoodfor
trophiccascades is dependenton factorsin additionto
productivity
includingresourceavailability,plant competition and plant diversity,which influenceinsect
abundance and predator-prey
interactions.
We found differences
in the relativeabundance of
phloem-and xylem-feeding
guilds among fieldsof differentsuccessionalage. This can be explainedby differences in productivity
betweenfields.Fertilizationdata
OIKOS 82:3 (1998)
and predation
on herbivores
on plantbiomass(g) in early,middle,and late
Table2. Summary
effects
offertilizer,
herbivory,
biomassforSolidagorugosa.Non-goldenrod
plants
shootand belowground
successional
fields.Data areseparated
intoflower,
are clumpedintoone measure.
Dependent
variable
Responsevariables
S. rugosaflower
S. rugosashoot
p
Early-successional
field F
df
Trophicstructure
Herbivore-Control
Predator-Herbivore
9.76
Fertilization
field
Mid-successional
NS
NS
NS
1,17
Trophicstructure
3.45
Herbivore-Control
Predator-Herbivore6.58
Fertilization
103.27
Late-successional
field
2,29 0.045
NS
1,20 0.018
1,18 0.0001
6.11
Trophicstructure
Herbivore-Control 11.94
Predator-Herbivore7.87
Fertilization
2,27
1,18
1,18
NS
F
0.006
0.00647
0.00028
0.011
3.44
4.94
df
p
S. rugosabelowground
F
df
p
Non-goldenrod
plants
F
df
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
2,29 0.046
NS
1,20 0.037
NS
NS
NS
NS
1,18
NS
NS
NS
NS
NS
NS
NS
NS
4.19
NS
NS
NS
NS
0.0192
p
NS
NS
NS
NS
show mineral nutrientslimit plants in the late field accounted for 45% of the total plant biomass. Herbimuch less than in the younger-agedfields (Tilman vores at this site are generalistor may have preferred
1986). As a resultplants in late-successionalfieldsare otherplants over goldenrod.In late-successionalfield,
likelyto be of highernutritionalquality. High plant the introductionof predatorsreleased herbivorepresnutritionalqualityhas implicationsfor the patternsof sure on goldenrod shoot biomass. Spittlebugs acherbivoreabundance. For example,xylem-feeders
have countedfora largeproportionof the herbivoresat this
the highestdaily consumptionrates of any herbivores: site; theyare knownto have a strongeffecton golden100-1000 times their body weight (Mattson 1980). rod relativegrowthand photosynthetic
rate(Meyerand
Xylem,however,is verylow in nitrogen( < 0.01%) and Whitlow1992, Meyer and Root 1993).
xylem-feeders
It is also possible that in the presenceof predators,
requirelarge quantitiesof plantmaterial.
A highlyproductiveenvironment
may be able to sup- herbivoresavoid moving up to the canopy of the
such as spittle- goldenrodstand where theycan bask in the sun and
port a higherdensityof xylem-feeders
site. Higher densitiesof develop and feed more efficiently.
bugs than a low productivity
Consequently,the
xylem-feeders
may resultin a decreasein thenumberof riskof predationdrivesthemto starvation.The vegetaphloem-feeders
(Maddox and Root 1990). In our exper- tion at the late-successionalsite was dense and the
imentwe foundevidencethatxylem-feeders
weremost insectenvironment
more shaded. A shaded understory
abundantat highlyproductivesites.
decreasesthe abilityof insectsto move to otherplants
The impact of predators also may have manifest withoutincreasingtheirmetabolicdemands.Other rethemselvesin different
fields.In early- searchhas shown that the riskof predationcan affect
ways in different
successional plots, neitherthe introductionof herbi- the foragingbehaviorof herbivorousinsectsand limit
vores nor the introductionof predators changed movementin the top of plants (Porter 1982, Loeffler
goldenrodshoot biomass. Insectsstockedin earlysuc- 1992, Beckerman et al. 1997, Schmitz et al. 1997).
cessional cages were generalistherbivoresthat may Spiders,the experimentalpredators,are vulnerableto
have preferredgrasses over forbs,particularlyin the desiccationand tolerantof shadedenvironments.
Hence
presenceof predators.In mid-successional
stagespreda- spider predators would have an advantage in latetorsincreasedgoldenrodshoot biomass withrespectto successionalsites,and thepredationeffecton herbivore
herbivore-only
cages and herbivoreshad no effecton plant consumptionwould be strongerat thesesites.
goldenrod shoot biomass. Herbivores,however, did
The effectof trophicstructureon flowerbiomass in
decrease other plant biomass in both herbivoreonly the mid-successionalfieldcan be explainedby the parand herbivore-predator
treatmentsin the mid-succes- ticularnutrientlimitationsspecificto flowering.
Flower
sional fields.This suggeststhat the patternof plant productionrequirestranslocationof K to the infloresabundancewithtrophicmanipulationin thisfieldarose cence (Abrahamsonand McCrea 1986). This fieldwas
from herbivore-mediatedgoldenrod-non-goldenrod the one that increased biomass most when fertilized
plant interactions.Non-goldenrodforbs in this field (almost 100% increase),demonstrating
strongnutrient
OIKOS 82:3 (1998)
557
(A)
EARLYSUCCESSIONAL
FIELD
i
50
60'
MID-SUCCESSIONAL
FIELD
~~~b
b
50,
a
00
|
20-
40
|
20-
10,
0
0
(B)
~~~~~~~~~~~~~~~~~E~
20
10
UNFERTILIZED
EERTILIED
0
EARLYSUCCESSIONAL
FIELD
10,
UNFRIE
04-
FERTID
MID-SUCCESSIONAL
FIELD
12
1
10,
10
10,
6'0
6-6
2.
20
UNFETLZED
FERTILE
10-
UNFERTILIZED
0
FERTILIZED
MID-SUCCESSIONAL
FIELD
UNFERTIIZED
FERTILIZED
LATESUCCESSIONAL
FIELD
0
20-
0
6'
Fig.
3.Effect
offertilization
onS.rugosa
FERTIZD
2
~~~~~~~~~~~~~~~~~~~~~~~0
EARLYSUCCESSIONAL
FIELD
(C)
UNFERTIED
LATESUCCESSIONAL
FIELD
12-
00
LATESUCCESSIONAL
FIELD
40'
30~~~~~~~~~~~~~~~~~~~~~~~~<3
Ii ,
50
shoot (a), root (b), and (c) non-goldenrod
plant biomass.
Means
and standard
errors
in early,middle,and late successionalfieldsare presented.Differentlettersdenote statistically
significant
differences
(ANOVA,
p<0.05)-
limitation.If the plants must live in a resourcepoor
environment
theymightbe forcedto lowerflowerproductionwhenfaced withthe added stressof herbivory.
This fieldwas also richin the forbsAsternovaeangliae
and Daucus carota with floweringphenologies that
parallelthatof goldenrod.The added effectof competition between plants for resources at floweringtime
mighthave createdthe patternswe observedin flower
phenologywithtrophicstructure.
The effect of fertilizationon goldenrod shoot
558
biomass increasedfromthe early-to the mid-successional fieldand thendecreasedin the late-successional
field.These resultsare not surprising
whenone considers the natureof the disturbanceintroducedto createa
successionalgradient.The early-successional
fieldwas
plowed in 1995, but had not been used foragriculture
in thelast 15 years.Typicallyearly-successional
fieldsin
thisarea are colonized aftermanyyearsof agricultural
use; thus soil resourcesare depleted.This was not the
case in thisstudy.Furthermore,
manyof thegoldenrod
OIKOS 82:3 (1998)
plantsin the earlysuccessional
plotsgrewfromrhi- References
zomesthathad remained
viableafterplowingand did Abrahamson,W. G. and McCrea, K. D. 1986. Nutrientand
not represent
trueearly-successional
goldenrod.This
biomass allocation of Solidago altissima: effectsof two
stem gallmakers,fertilization
and ramet isolation. - Oepatternof successiononly represents
recovery
from
cologia 68: 174-180.
agricultural
disturbance
and mightnoraccurately
rep- Abrahamson,
W. G. and Weis, A. E. 1996. The evolutionary
resentrecovery
fromotherdisturbances,
suchas fire.
ecology of a tri-trophiclevel interaction:goldenrod,the
The positiveeffectof fertilization
on belowground stemgallmaker,and its naturalenemies.- PrincetonUniv.
Press,Princeton,NJ.
biomassin themid-successional
fieldsuggests
thatadAbrahamson,W.G., Anderson,S. S. and McCrea, K. D. 1988.
ditionalresources
mayimprovegoldenrod
asexualreEffectsof manipulationof plant carbon nutrientbalance
production.
Goldenrodestablishment
fromseed in a
on tall goldenrodresistanceto a gallmakingherbivore.Oecologia 77: 302-306.
fieldof thisage is rare(Werneret al. 1980).It seems
G. E. 1952. Secondarysuccessionon the Piedmontin
plausiblethatadditional
resources
areusedforasexual Bard,
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reproduction
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The ob- Beckerman,A. P., Uriarte, M. and Schmitz, 0. J. 1997.
Experimental
servedflowerproduction
evidencefora behavior-mediated
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trophiccascade in a terrestrial
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on
corroborates
thislogic.The lackof fertilizer
effects
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G. E. 1986. Optimalforagingand community
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responsein shootbiomassin themiddlefieldall sugG. E. and Slade, J. B. 1993. The role of vertebrate
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Our resultssupporttheconverse
A. 1980. Vascular floraof the southeasternUnited
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Herbivory
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The exploitation
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does
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Cornell Univ., New York.
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G., Wait, D. A. and Coleman, J. S. 1995.
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tioneffect
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