BIOTROPICA 24(2a): 211-214
1992
NOTES
of Young and MatureLeaves to Leaf-Cutter
The Acceptability
AntsVaries withLightEnvironment
to
on its susceptibility
in whicha plantis growingcan have a stronginfluence
The physicalenvironment
in leaftraitscan affecttheselection
differences
(Coley et al. 1985). For example,light-induced
herbivores
of leaves by herbivores(Watermanet al. 1984; Harrison1987; Ernest1989; Nichols-Orians1991a,
of matureleavesof
b). In a previousstudy,I foundthatas lightavailabilityincreases,the acceptability
also increases(Nicholsant, Atta cephalotes,
a tropicallegume tree,to the leaf-cutter
Inga oerstediana,
Orians 1991a, b).
ants
leafage mayaffecttheselectionof leavesby leaf-cutter
In additionto environmental
conditions,
(Cherrett1972; Rockwood 1976, 1977; Waller 1982; Shepard1985; Nichols-Orians& Schultz1989,
usuallyattacktreeswhenyoungleavesare mostavailable (Cherrett1972), because
1990). Leaf-cutters
(Barrer& Cherrett1972, Littledyke& Cherrett
youngleaves are easierto cut and more nutrient-rich
between1. oerstediana
1978, Waller 1982, Nichols-Orians& Schultz1989). In studyingtheinteractions
and A. cephalotes
(Nichols-Orians& Schultz 1990), it was foundthatyoungleaves,despiteveryhigh
wereless chemicallyacceptablethan matureleaves; thiswas apparentlydue
of nutrients,
concentrations
have identified
ofcondensedtanninin theyoungleaves.A numberofresearchers
to a higherconcentration
systems(Ikeda et al. 1977, Raupp & Denno 1983, Meyer&
similarpatternsin otherplant/herbivore
Montgomery1987).
of young
Mole & Waterman(1988) suggestthatlightavailabilitycan alterthe relativeacceptability
of
mediatesthe acceptability
and matureleaves,but fewstudieshave assessedif and how environment
(Ernest1989). Becausetheproductionof secondarychemicals(in
youngand matureleavesto herbivores
is dependentupon lightavailability(Chandler& Goosem
this case condensedtannins)and nutrients
of youngand matureleavesof
1982, Mole et a!. 1988, Denslow et al. 1990), the relativeacceptability
I. oerstedianato leaf-cutter
ants may be modifiedby lightavailability.Althoughyoung leaves of I.
ants than matureleaves fromthe same
oerstedianaplantsin full sun are less acceptableto leaf-cutter
thatforplantsin the shaded understory,
plant (sensuNichols-Orians& Schultz 1990), I hypothesized
youngleaveswould be moreacceptablethanmatureleaves.Shaded youngleavesare thoughtto have a
to tanninratiothando shaded matureleaves (Mole & Waterman1988).
highernutrient
(L.) werelocatedat theLa Selva BiologicalStation
In May of 1988 threecoloniesof Atta cephalotes
in theAtlanticlowlandsof Costa Rica (10?26'N, 83?59'W). I used saplingsof Inga oerstedianaBenth.
Inga edulisvar. minutulaSchery(Nichols-Orians& Schultz 1990),
(Fabaceae: Mimosoideae),formerly
and becausetheyare naturally
lightenvironments
becausethesaplingscan be foundgrowingin different
ants (C. Nichols-Orians,pers. obs.). Six saplingswere locatedgrowingin the
attackedby leaf-cutter
and six growingin largegaps. Saplingswere 0.5 to 1.0 m in height.I employeda paired
understory
design,collectingboth matureand youngleaves fromthe same plant. Mature leaves were definedas
those that were fullyexpanded and dark green,but devoid of epiphyllsbecause epiphyllsaffectthe
of leavesof leaf-cutter
ants (Mueller& Wolf-Mueller1991). Young leaveswerethosethat
acceptability
wereclose to fullyexpandedand stillslightlyred in color.
to the studycoloniesand used in a behavioralassayto determinehow
The leavesweretransported
of a plant influences
the selectionof youngand matureleaves by foragingants.
the lightenvironment
of plantsto leaf-cutter
ants. The
Two typesof assaysare oftenemployedto evaluatethe susceptibility
or nutritional,
defensive
basedon chemicaldifferences,
preferences
"pickup" assayis designedto determine
betweenleaftypes(Howard 1987). In thisassayprecutleafdiscsare presentedto the antsand removal
of the discs monitored.Conceivablywatercontent,physicalfeaturesof a leaf (e.g., trichomes),or leaf
disc removal.Water contentdoes not appear to affectdisc removalin thissystem
mass could influence
any physicalfeaturesin I. oerstedianawhich
(C. Nichols-Orians,pers.obs.). Also, I have not identified
The leafdiscsweresmall enough
could interefere
withremoval.Finally,leafmass appearsunimportant.
thatall foragingants could easilypick up theseleaf discs. In fact,the toughestand heaviestleaf type
assayedto date was one of the mostacceptableleaftypes(Nichols-Orians& Schultz 1990).
with the
The second assay,the "cutting"assay,is used to determineif physicalfeaturesinterfere
ants(Howard 1988; Nichols-Orians& Schultz1989,
cuttingof leavesalreadyselectedby theleaf-cutter
211
This content downloaded from 128.206.166.171 on Thu, 07 Jan 2016 20:04:27 UTC
All use subject to JSTOR Terms and Conditions
212
Nichols-Orians
80
>
0
w
a:
LEAF AGE
6
60
Pc0
P0.00.o1:|
YOUNG
MATURE
C')
IL.
40
z
wL
20
~~~~~~~NS-
0.
SUN
SHADE
LIGHT ENVIRONMENT
of youngand
FIGURE 1. The relativeacceptability
fromsaplingsgrowingin
matureleavesof I. oerstediana,
(shade), to leafhigh light (sun) or in the understory
cutterants.A two-sidedsign testwas used to determine
in the acceptdifferences
whethertherewere significant
abilityof youngand matureleaves.
1990). I did not employ the "cutting" assay because I was only interestedin determininghow leaf age
influencethe initialselectionof leaves.
and environment
In the "pickup" assay,two leafdiscs(producedwitha standardpaperpunch) of each leaftypewere
placed along the trail.To insurethat the assaysinvolvingthe leaf typeswereindependent,I separated
each day. When one disc was
themspatiallyalong the trailand randomizedthe orderof presentation
of a givenleaf typewas expressedas
removedit was replacedby a like disc. The chemicalacceptability
the percentageof the totalnumberof leaf discsremovedin 30 min. The assaywas repeatedtwiceand
value foreach leaf type.The assayswere repeated
the replicatesaveragedto give a singleacceptability
six timeson colony1, threetimeson colony2, and twiceon colony3. Because I. oerstedianaleaves are
compound,I onlyused leafdiscsfromdistalleafletsin theassay,in orderto avoid possibleleafletposition
effects
(Gall 1987).
A nonparametric
sign test,SYSTAT statisticalpackage, was employedto determineif therewere
testwas used because the data werenot
A nonparametric
differences
among leaf typesin acceptability.
normallydistributed.
forthe fourdifferent
Bioassayswiththe ants indicatethatall coloniesshowedthe same preferences
withpreviousworkthatshowedthateven
P > 0.10). This resultis consistent
leaftypes(ColonyEffects
in theirwillingnessto acceptleaves of I. oerstediana(Nichols-Orians
ants may differ
thoughleaf-cutter
leaftypes(Nichols-Orians&
fordifferent
& Schultz1990), theystillshow the same relativepreferences
the data were analyzed
Schultz 1990, Nichols-Orians1991a). Because therewere no colonyeffects,
withoutcolonyas an effect.
leaf discs fromplantsgrowingin highlightover
Consistentwithpreviouswork,the ants preferred
(P ' 0.01), and leaf discs of maturesun leaves
leaf discs of plantsgrowingin the shaded understory
werefound
overthoseof youngsun leaves (Fig. 1) (Nichols-Orians1991a, b). However,no differences
to
plants(Fig. 1). This resultis contrary
of youngand matureleaves of understory
in the acceptability
I had hypothesized
thatyoungshade leaveswould be moreacceptableto theants
myoriginalhypothesis.
to tanninratio(sensuMole
thanmatureshade leaves,becauseyoungleaveswould have a highernutrient
leaf materialto do chemicalanalysesas well as
& Waterman1988). I was unable to collectsufficient
acceptability.
cannotprovidea possiblemechanismforthe differential
behavioralassays,and therefore
of youngand matureleavescan be modified
thedata indicatethattherelativeacceptability
Nevertheless,
by lightavailability.
This content downloaded from 128.206.166.171 on Thu, 07 Jan 2016 20:04:27 UTC
All use subject to JSTOR Terms and Conditions
Notes
213
The survivalof some herbivoresappears to depend upon the presenceof young leaves (Aide &
Londoiio1989). In thesecasesyoungleavesmightbe expectedto be preferred
underall lightenvironments.
Perhaps for herbivoreslike leaf-cutter
ants, that attack both young and matureleaves, the relative
of youngand matureleaves will be modifiedby lightavailability.Other environmental
acceptability
suchas soil quality,can affect
conditions,
leaftraits(e.g.,Denslowetal. 1990) and acceptability
(NicholsOrians 1991b), and may influencethe relativeacceptability
of leaves of different
ages as well. Clearly,
forsome herbivores,
on the acceptability
of youngand matureleaves may requirethat
generalizations
studiesbe conductedunderdifferent
environmental
conditions.
I would like to thankthe OrganizationforTropicalStudies(OTS) forprovidinglogisticalsupport
whileI was at the La Selva BiologicalStation.This workwas supportedby a JesseSmithNoyes Grant
awardedby OTS, a USAID graduatestudentstrengthening
grantawardedby the Collegeof Agriculture
at Penn State,and two National ScienceFoundationgrants{BSR-8815648 to C. Nichols-Orians(DissertationImprovement
Grant),and BSR-8917752 to R. Fritz).
AIDE, T. M., AND E. C. LONDONO. 1989. The effects
of rapid leafexpansionon the growthand survivorship
of a
lepidopteranherbivore.Oikos 55: 66-70.
1972. Some factorsinfluencing
the site and patternof leaf-cutting
activity
in the ant Atta cephalotes.
J. Entomol.47: 15-27.
CHANDLER,G., AND S. GOOSEM. 1982. Aspectsof rain forestregeneration.
III. The interaction
of phenols,light
and nutrients.
New Phytol.92: 369-380.
CHERRErr,J. M. 1972. Some factorsinvolved in the selectionof vegetablesubstrateby Atta cephalotes(L.)
(Hymenoptera:Formicidae)in tropicalrainforest.J. Anim. Ecol. 41: 647-660.
COLEY, P. D., J.P. BRYANT, AND F. S. CHAPIN. 1985. Resourceavailability
and plantantiherbivore
defense.Science
230: 895-899.
DENSLOW,J. S., J. C. SCHULTZ,P. M. VITOUSEK,AND B. R. STRAIN. 1990. Growthresponsesof tropicalshrubsto
treefall
gap environments.
Ecology71: 165-179.
ERNEST, K. A. 1989. Insectherbivory
on a tropicalunderstory
tree:effects
of leafage and habitat.Biotropica21:
194-199.
GALL, L. F. 1987. Leafletpositioninfluence
caterpillar
feedingand development.Oikos 49: 172-176.
HARRISON,S. 1987. Treefallgaps versusforestunderstory
as environments
fora defoliatingmoth on a tropical
forestshrub.Oecologia (Berl.) 72: 65-68.
HOWARD,J. J. 1987. Leaf-cutting
ant diet selection:the roleof nutrients,
waterand secondarychemistry.
Ecology
68: 503-515.
1988. Leaf-cutting
ant dietselection:therelativeinfluence
ofleafchemistry
and physicalfeatures.Ecology
69: 250-260.
IKEDA, T., F. MATSUMURA, AND M. D. BENJAMIN. 1977. Mechanismsof feeding discrimination
betweenmatured
and juvenilefoliageby two speciesof pine sawflies.J. Chem. Ecol. 3: 677-694.
LITLEDYKE, M., AND J. M. CHERREIrr. 1978. Defencemechanismsin youngand old leaves againstcuttingby the
leaf-cutting
antsAtta cephalotes
(L.) and Acromyrmex
octospinosus
(Reich) (Hymenoptera:Formicidae).Bull.
Entomol.Res. 68: 263-271.
MEYER,G. A., AND M. E. MONTGOMERY. 1987. Relationshipsbetweenleafage and the foodqualityof cottonwood
foliageforthe gypsymoth,Lymantriadispar.Oecologia (Berl.) 72: 527-532.
MOLE, S., AND P. G. WATERMAN. 1988. Light-inducedvariationin phenoliclevelsin foliageof rain-forest
plants.
II. PotentialSignificance
to herbivores.
J. Chem. Ecol. 14: 23-34.
, J. A. M. Ross, AND P. G. WATERMAN. 1988. Light-inducedvariationin phenoliclevelsin foliageof rainforestplants.I. Chemicalchanges.J. Chem. Ecol. 14: 1-21.
MUELLER,U. G., AND B. WOLF-MUELLER. 1991. Epiphylldeterrence
to theleaf-cutter
antAtta cephalotes.
Oecologia
86: 36-39.
NICHOLS-ORIANS, C. M.
1991a. The effects
of lighton foliarchemistry,
growthand susceptibility of seedlings of
a canopytreeto an attineant. Oecologia 86: 552-560.
199 lb. Environmentally
in planttraits:consequencesforsusceptibility
induceddifferences
to a leaf-cutter
ant. Ecology72: 1609-1623.
AND J. C. SCHULTZ. 1989. Leaftoughnessaffects
leafharvesting
by the leaf-cutter
ant,Atta cephalotes
(L.)
(Hymenoptera:Formicidae).Biotropica21: 80-83.
, AND
.
1990. Interactions
among leaf toughness,chemistry,
and harvestingby attineants. Ecol.
Entomol. 15: 311-320.
RAUPP,M. J., AND R. F. DENNO. 1983. Leaf age as a predictorof herbivoredistribution
and abundance.In R. F.
Denno and M. S. McClure(Eds.). Variableplantsand herbivoresin naturaland managedsystems,pp. 91124. AcademicPress,New York, New York.
ROCKWOOD,
L. L. 1976. Plant selectionand foragingpatternsin two speciesof leaf-cutting
ants (Atta). Ecology
57: 48-61.
. 1977. Foragingpatternsand plantselectionin Costa Rican leaf-cutting
ants.J. N. Y. Entomol.Soc. 85:
222-233.
BARRER,P. M., AND J. M. CHERRETT.
This content downloaded from 128.206.166.171 on Thu, 07 Jan 2016 20:04:27 UTC
All use subject to JSTOR Terms and Conditions
214
Nichols-Orians
J. 1985. Adjustingforaging
effort
to resources
in adjacentcoloniesoftheleafcutting
ant,Attacolumbica.
Biotropica17: 245-252.
WALLER, D. A. 1982. Leaf-cutting
ants and live oak: the role of leaf toughnessin seasonaland intraspecific
host
choice.Entomol.Exp. Appl. 32: 146-150.
WATERMAN, P. G., J. A. M. Ross, AND D. B. MCKEY. 1984. Factorsaffecting
levelsof some phenoliccompounds,
digestibility,
and nitrogencontentof the matureleaves of Barteriafistulosa(Passifloraceae).
J. Chem. Ecol.
10: 387-401.
SHEPARD, D.
Colin Nichols-Orians'
Departmentof Entomology
PennsylvaniaState University
University
Park, Pennsylvania16802, U.S.A.
I Presentaddress:DepartmentofBiology,Box 312, Vassar College,Poughkeepsie,New York 12601, U.S.A.
BIOTROPICA24(2a): 214-216 1992
in Bird-DispersedGynodioeciousFicus
Fig Dimorphism
figs(Lambert1989).
at least 29 speciesof Ficus have bird-dispersed
In Malaysianlowlandrainforests,
Plantsof thesegynodioecious
Eightof thesespeciesbelongto thesubgenusFicus,and aregynodioecious.
but effectively
speciesproduceeithergall figsor seed figs.Gall figscontainbothmale and femaleflorets,
shortstylesand are predatedby the larvae of
become males because the femalefloretshave relatively
pollinatorsof Ficus. In contrast,the stylesof seed figsare
agaonid wasps,whichare the species-specific
but cannotovipositeggsin them.Seed figstherefore
longer,so thatincomingagaonidspollinatetheflorets
agaonids(Janzen1980, Verkerke1989).
produceseeds,but are not a sourceof pollen-carrying
Hill (1967), workingmainlyin Hong Kong, stated that therewere no externalmorphological
in the shape and size of the figs,and
betweengall and femaleplantsexceptfordifferences
differences
have not been
sometimesin theircolor and seasonal occurrence.In southeastAsia, these differences
previouslydocumented.
strangling
Ficusspecies[F. heteropleuA comparison
bird-dispersed
ofthefigsfromthreegynodioecious
ra BI., F. obscuraBl. (var. borneensis
Miq.) Corner,and F. parietalis BI.} at Kuala Lompat, West
consistent
differences
Malaysia(3?43'N, 102017'E, 50-80 m altitude)showedthatthereweredistinctive,
in color,texture,and morphologybetweenfigson male and femaleplants.
seed figs,and did notexhibitthestriking
Gall figswerealwayspalerin colorationthantheirrespective
colorchangesassociatedwiththe ripeningof the latter.Thus the gall figsof F. obscurawerewhitish,
becomingblotchybrownbeforedropping,in contrastto the brightorangeseed figswhichripeneddark
and F. parietaliswerepale orangeat all stages,whileboth
red to purple.The gall figsof F. heteropleura
speciesproducedorangeseed figswhichripeneddark red. The textureof gall figswas rubberyat the
seed figs.
soft,fleshynatureof bird-dispersed
stagebeforefalling,but neverdevelopedthe characteristic
Ostiolesof thegall figsof F. panietaliswerenotablylargeand appearedto open just beforethegall figs
fellto theground.The broad,open ostiolesof F. parietalispresumablyassistthe escape of pollen-laden
open ostiolesat any
seed figsof F. parietalisdid not have distinctive,
femaleagaonidwasps. In contrast,
stageof ripeness.
This content downloaded from 128.206.166.171 on Thu, 07 Jan 2016 20:04:27 UTC
All use subject to JSTOR Terms and Conditions