Feeding preference of Heliconius erato (Lep.: Nymphalidae) in relation to leaf age and consequences for larvarl performance

6 Pages·1999·3.3 MB·English

by  Daniela Rodrigues

JournaloftheLepidopterists'Society
53(3),1999,108-113
FEEDING PREFERENCE OF HELICONIUSERATO (LEE: NYMPHALIDAE) IN RELATION TO
LEAF AGE AND CONSEQUENCES FOR LARVAL PERFORMANCE
Daniela Rodriguesand Gilson Rudinei Pires Moreira1
DepartamentodeZoologia,Institute)deBiociSncias,UFRGS,Av.PauloGama,40,90046-900,PortoAlegre, RS, BRAZIL
ABSTRACT. InSouthBrazil,femaleHeliconiuseratophyllis (Fabricius)layisolatedeggsonbranchtipsofPassiflorasuberosa Linnaeus,
leadingtoearlylarvaefirstcontactingyounghostplanttissues.Thesefeedonyoungtissues,buttheadaptivemeaning,ifany,forsuchanasso-
ciationisstillunknown. Inthispaper,wedeterminewhatleafagesareusuallyconsumedbyeachinstar,theexistenceoffeedingpreferencein
relationtoleafage,andtheperformanceofH.eratowhenfedeitheronyoungoroldleavesofP.suberosaunderlaboratoryconditions.Freshly-
hatchedlarvaeweretransferredtotheterminalportionofisolated, intactshoots, andobserveddailyfororderofleafchoiceuntil pupation.
Feedingpreferenceinrelationtoleafagewasevaluatedforallinstarsthroughchoicetestsusingleafdisksfromyoungandmatureleaves.Ad-
ditionallytoevaluateinductionoffeedingpreference,larvaewererearedthroughfourthinstaroneitheryoungormatureleavesandthentested
usingthesamechoiceprocedure.Growthperformancewasassessedbyprogressivelytransferinglarvae,accordingtoinstarnumber,fromintact
shootstosectionswhereapicalportionwascutoff. Larvaefedstartingattheterminalbud(youngtissues) andmovingprogressivelytolower
leavesofincreasingage(matureleaves). Larvaeofallinstarsconsumedmoreyoungleafdisks,andpreferenceforoldleavescouldnotbein-
duced.Larvaerearedinitiallyonyoungtissueshadgreatersurvivorshipandgrewfasterthanthoseonmature,andthismayexplaintheoviposi-
tionsiteselectionandlarvalfeedingpreferenceofthisbutterfly.
Additionalkeywords:host-plantselection,heliconianbutterflies,passionvines,leafageeffects.
Heliconius erato phyllis (Fabricius) (Nymphalidae) calportion ofhost-plants is also relatedto higher suit-
is common inthe forests ofsouthern Brazil (Brown & abilityofthe correspondingtissues as larval food.
Mielke 1972). Ituses anumberofpassionvine species In this paper, we address the latterhypothesis from
as larvalhosts, afewbeingpreferredin agivenlocality a behavioral ecologyperspective. Feeding ofH. erato
(Bensonetal. 1976, Brown 1979, 1981, Ramos &Frei- phyllis larvae and its consequences are evaluated re-
tas 1999). Isolated eggs are laidprimarilyon terminal garding variation in leaf age on shoots of Passiflora
buds of Passiflora shoots, young tendrils and young (Plectostemma) suberosa. This widely spread passion
leaves (Benson 1978, Perico 1995, Mugrabi-Oliveira& vine is a primary host ofH. erato phyllis, and one of
Moreira 1996a). Larvae feed initially on young leaves the most abundant passion vine species in southern
near the apical portion of shoots (Alexander 1961, Brazil (Menna-Barreto & Araujo 1985, Perico &
Benson 1978). Ovipositing females reject shoots de- Araujo 1991, Perico 1995). Informationonthephenol-
privedoforwith adamagedapicalportion, andprefer ogyofP. suberosa and correspondingeffects on H. er-
to lay on large shoots compared to small (Mugrabi- ato phyllis oviposition site selection are provided by
Oliveira & Moreira 1996a). They also assess egg- and Mugrabi-Oliveira & Moreira (1996a). Specific goals of
larval-load, and reduce daily oviposition rates under the current study are 1) to characterize the natural
low host-plant availability (Mugrabi-Oliveira & Mor- feedingpatternofH. eratophyllislarvalinstars inrela-
eira 1996b). tion to P. suberosa leafage, 2) to evaluate the feeding
There are at least three hypotheses to explain Heli- preference ofeach instar regardingleafage, and 3) to
conius oviposition and early larval feeding on young determine the consequences of feeding on leaves of
Passiflora tissue, which are not necessarily mutually variableageonsurvivorship, growthrateandadultsize.
exclusive. First, Benson et al. (1976) suggested that
Materials and Methods
Heliconius oviposition on passion vine tendrils would
help to prevent egg-predation, because eggs on ten- Insects and plants. Larvae used in the experi-
drils are less likelyto be attackedbyants. In addition, ments came from eggs obtained from an H. erato
Benson (1978) hypothesized that the feeding pattern phyllis outdoor insectary maintained at the Zoology
of heliconian larvae that use young tender growth, Department ofFederal University ofRio Grande do
such as H. erato, was in part shaped by interspecific Sul, Porto Alegre, RS (see Mugrabi-Oliveira & Mor-
competition with species specialized on older leaves. eira 1996a). P. suberosaplantswereobtainedfromcut-
Also, it is known that host-plant selection by phy- tings that were transplanted into plastic pots. The
tophagous insects is linkedtoplant suitabilityas larval plants originatedfromapopulationatAguas Belas Ex-
food (Jones 1991, Bernays &Chapman 1994). Thus, it perimental Station, Viamao County. The plastic pots
is expectedthatH. eratophyllis ovipositionontheapi- wereprovidedwith50cmhighwoodenframe support
for shoot growth, coveredwith a fine mesh cloth and
1Fromwhomreprintsshouldberequested. maintained in an outdoor screened cage. Priorto the
Volume 53, Number 3 109
tests,plantswere standardizedforsizebyremovingall
branches except the main shoot in each pot. Experi-
ments were conducted in alarge laboratory chamber,
adopting the prevailing abiotic conditions for the re-
gion duringthe summer (photoperiod 14L:10D, tem-
perature 25 ± 1°C, humidity75 ± 5%).
Feedingpattern. Todetermine larvalfeedingpat-
tern in relation to leafage, twentyfreshlyhatched H.
erato phyllis larvae were individually placed on the
terminal bud of healthy growing shoots bearing 12
open leaves. Additional studies thathavebeen carried
&
out in ourlaboratory (S. S. Borges G. R. P. Moreira
unpubl. data) showedthatin allcaseswhenyounglar-
vae areputon anymatureleaf, theymove tothetip of
P. suberosa shoots, always starting feeding on the ter-
minal bud. Larvae were inspected for molting daily
untilpupation. Ateachinspection,wenotedtheageof
leafbeing consumed. To make sure that molts were
not overlooked, larvae were gently markedwith small
colored dots of enamel paint (Testors) on the dorsal
part ofthe penultimate abdominal segment. Leafage
was determinedbyleafposition in relation to the ter-
minalbud(madeupofapicalmeristem, leafprimordia
andunopen leaves) (Fig. 1A).
Choice experiments. Feedingpreference in rela-
tion to leafagewas evaluatedthrough leafdiskchoice Fig. 1. Schematic representation ofPassiflora suberosa shoots
used to determine influence ofleafage on Heliconius erato larval
tests. Trials were conducted in plastic pots, following performance. A, intact, with terminal budandten open leaves; B,
the methodology described in Hanson (1983). The lowersection,withfivematureleaves (terminalbudandfiveapical
same twenty larvae were used over all instars; corre- openleaveswerecutout).TB,terminalbud;L,openleaf. Numbers
indicate position in relation to shoot apex. Tendrils and stipules
sponding rearing procedure followed that descrived associatedwithopenleaveswerenotdrawn.
above. Unless noted, two leaf age categories were
adopted: young (consisting of the first and second
open leaves on actively growing branch) and mature using the leaf-disk choice test described above (18
(sixth andseventh open leaves). Disks were cutwith a disks ofeach ageperlarvae).
corkborer (diameterof6.75 mm; 35.78 mm2in area), Feeding was measured as area of disk eaten,
and a fixed number offered (3, 3, 6, 12 or 18 disks of recorded by placing the disks against graph paper at
each age per larvae tested from first to fifth instar, re- the endofeachfeedingtrialandcountingthenumber
spectively). Young leaf disks alternated with mature of square millimeters corresponding to the missing
ones in the pot. To keep leaf disks from drying out, leafarea. Ifonlyyoung leaves were damaged, or over
potswerecoveredwith aplasticfilm. Leaveswerecol- twice the area of young as mature leaves was con-
lectedfrom differentplants everytime. Totalleafarea sumed, larvae were scored as having discrimated in
offeredagiveninstarwas adjustedto double the aver- favour of young leaves. Conversely, if only mature
ageleafareaconsumedbyagiveninstarin5hours (C. leaves were consumed, or over twice the area ofma-
A. Barcellos & G. R. P. Moreiraunpubl. data). All tri- ture as young leaves was missing, then larvae were
alslastedfor5hours, afterwhichlarvaewerereturned scored as having chosen mature leaves. Feedingtrials
to theiroriginal rearingplants. were recorded as neutral when neither leaf-age cate-
To evaluate possible induction of feeding prefer- goryhadmorethantwicethedamageoftheother(see
ence in relation to leafage, additional 40 larvae were Thomas 1987). To test the hypothesis that consump-
reared up to third instaronyoung leaves. After molt- tion ofyoung leaves was greater than mature, scores
ing to fourth instar, halfofthem were transferred to were tested using one-tailed sign tests, following the
cuttings containing only mature leaves; the remaining procedure describedin Conover (1980).
20 larvae were kept on cuttings bearingyoung leaves. Larval performance and adult size. To deter-
Theywereallthenindividuallytestedinthefifthinstar mine leafage effects on performance, larvae were in-
; 1
110 Journalofthe Lepidopterists' Society
Table 1. ExperimentalschemeadoptedtotestinfluenceofPas- (Fig. 1). Six different treatments were used. Larvae
siflora suberosa leaf age on Heliconius erato larval performance. were transferred from plants with intact shoots (type
Treamentscorrespondtonumbersofinstarstayingonintactshoots.
1) tothosewith matureleaves (shoottype2) according
Shoottypeoffered sfood to instarcompletion (Table 1). Forexample: "In treat-
Treatment Intact Lowersection ment0, larvaewereplaceddirectlyonshootswith ma-
allinstars ture leaves; in treatment 5, larvae were allowed to
1 instarI instarsII-V complete all five instars on intact shoots". A com-
23 iinnssttaarrssII-aInIIdII iinnssttaarrssIIIVIa-nVdV pletely randomizedblock designwas adopted; the ex-
4 instarsI-IV instarV periment was carried out ten times (dates = block ef-
5 allinstars fect), one replicate per treatment was conducted on
each occasion. Since there was no block effect, data
were treated within an one-way design (10 replicates
dividuallyrearedonpottedplants receivingone ofthe pertreatment). Larvaewere checkeddailyformolting
following shoot types: 1) intact, with ten leaves and until death, or up to emergence to the adult stage.
terminalbud; 2) lowersection,with five matureleaves Forewing length offreshly emerged adults was mea-
(terminalbudandfiveapicalopenleaveswerecutout) sured with callipers. Data from development rates
(L.
hi
IV
L10
L1
10 11 12 13 14 IS
age of larvae (days)
Fig.2. SequentialfeedingpatternofHeliconiuseratolarvae(n=20)inrelationtoPassiflorasuberosaleafageandinstarnumber.TB,ter-
minalbud;L,openleaf. Arabicnumbersdesignatepositionofleafinrelationtoshootapex. Romannumbersrepresentlarvalinstars. Closed
circlesandassociatedbarsdenotethemedianandcorrespondingintervalofleafageeatenbyagiveninstar.
Volume 53, Number 3 111
Table2. SelectionbydifferentinstarsofHeliconiuseratolarvae uu
(n = 20) foryoungvs. oldleaves ofPassiflorasuberosa. Datashow
numberoflarvaefallingintoeachpreferencecategory. Seetextfor
80
descriptionofdiscriminationcategories.
Preferredleafcategory 60
Instar Younger Neutral Older p* o
I 20 <0.001 E> 40
II 19 1 <0.001 3
in 18 1 1 < 0.001 (0 20
IV 18 1 1 <0.001
V 9 9 2 <0.04
*probabilitiescalculatedfromsigntests. I II III IV V c
instaroftransfertomatureleaves
were logtransformed forthe analysis ofvariance, fol- Fig. 3. Heliconius erato larval stage survivorship when trans-
lowing the criteria described in Sokal and Rohlf ferredfromyoungtomatureleavesofPassiflorasuberosashoots.C,
(1981). Differences amongtreatmentsweretestedus- control =treatment5.
ing Fisher's Protected Least Significant Difference
multiple comparison tests, when analyses ofvariance preferred young over mature leaves when reared ei-
were significant. theronyoung(p < 0.002) ormature (p < 0.005) leaves
To determine specific effects of leaf age on adult ofP. suberosa.
size, 40 additional larvae were tested. These were Leafage affectedH. erato survivorship during early
rearedonyoungleavesuptothirdinstar, andaftermolt- instars (Fig. 3). Therewas asignificant associationbe-
ingforthefourthinstar, halfofthemwerekeptfeeding tweenthe ageoftransferto matureleaves andpercent
on young leaves while the remaining fed on mature survivorship (Spearman's rank correlation test, Rho =
leaves untilpupation. Afteremergence, adult forewing 0.975, n = 5, p < 0.05). When transferred to mature
lengthwas measured, anddatawerecomparedthrough leaves during first and second instars only 30% and
unpaired, two-tailed t-tests. There was no indication 60% of larvae respectively survived until pupation
that size ofmales and females differedin these exper- (Fig. 3). When transferred to mature leaves during
iments, and thus data were grouped. Unless noted third, fourth and fifth instars, larvae had similar sur-
measurements are given as mean ± standarderror. vivorshiptothosekeptonintactshoots (Fig. 3). Larval
development rates were significantlylongerwhen lar-
Results
vaewere transferred to shoots containingonlymature
Ingeneral, the larvae first ate the terminalbud, fol- leaves as firstorsecondinstars, buttherewasnoeffect
lowed by the first open leaf and progressively de- on laterinstars (Fig. 4).
voured older leaves, as they grew (Fig. 2). They con-
sumed all P. suberosa shoot parts, including tendrils, 18
stipules and stem. In general, the terminal bud pro-
to
videdenough foodto complete the firstinstar. During i>. 16
this instar some larvae ate partofthe firstopen leafas
0)
well. Leafdamage extended to the third, fourth and E
£
fifthopenleaves duringinstars two, three andfour,re- 14
a>
spectively(Fig. 2). Therewasconsiderablevariationin E
Q. t be
fifth instar consumption rates. This variation in leaf § 12 f
consumptionwasexpected, becauseleavesvaryinsize. a>
About half the larvae required seven open leaves to
10
complete larval development; however, some con-
sumedup toten leaves before pupation. I II III IV V c
instaroftransferto mature leaves
Larvae rearedon intactP. suberosa shoots discrimi-
natedbetweenthetwoleafcategoriestested(Table2). Fig. 4. Heliconius erato larval stage development time when
All instars preferred young over mature leaves in the transferred from young to mature leaves of Passiflora suberosa
leaf-disk choice test. Type ofleafage offered during shoots. Ccontrol = treatment5.Values followedbythesameletter
arenotsignificantlydifferent(Anova-logtransformeddata,n=48,
fourth instar did not influence choice oflarvae during
p < 0.001; Fisher's ProtectedLeast Significant Difference multiple
fifth instar (one-tailed sign tests, alpha = 0.05); they comparisontests,p<0.001).
112 Journalofthe Lepidopterists' Society
The size ofadults that emerged from larvae trans- (Hanson 1983, Bernays & Chapman 1994; but see
ferred during fourth instar to cuttings containing ma- Bernays &Weiss 1996). Contraryto mostoftheselep-
tureleaves (36.97 ± 0.42mm)was notsignificantlydif- idopterans that are polyphagous, H. erato is oligopha-
ferentfrom that ofthosekeptfeedingonyoungleaves gous, using a few Passiflora species as larval hosts in
(38.08 ± 0.37mm) (unpaired, two-tailedt-test, n = 36, southern Brazil (Perico & Araujo 1991, Perico 1995).
p > 0.06). Similarly, the size attainedin the adult stage In an additional study carried out in our laboratory,
was not affectedbytransferenceimposedon allinstars Kerpel (1999) failed to showinduction oflarval feed-
intheexperimentdesignedtotesteffectsofleafageon ingpreferenceregardingthetwopreferredhosts (Pas-
larvalperformance (one-wayAnova, n = 35, p > 0.37). siflora misera and P. suberosa) ofH. erato phyllis in
Rio Grande do Sul State.
Discussion
The data showed that P. suberosa leafage strongly
Our data confirmed field observations in that H. affectsH. eratophyllis larvalperformance. Althoughit
erato phyllis larvae feed continuouslyfrom the termi- is not known to what degree mechanical and nutri-
nal bud (young tissues) to the basal portion (mature tionalfactorscontributetotheseeffects, theymaycon-
leaves) of P. suberosa shoots. Young tissues are pre- stitute the proximate cause forthe maintainance ofat
ferred by all instars, and this preference is related to leasttwoegg-layingbehaviorsofH. erato. First, itmay
larval survivorship and development rates. As already explain why females selectively oviposit on terminal
pointed out, young larvae move to the terminal bud portion ofintact P. suberosa shoots (Lopes 1991, Mu-
when placed on any mature leaf. Thus, larvae start grabi-Oliveira & Moreira 1996a); females thateventu-
feeding on the apical portion ofthe plant not simply allyoviposit on shoots lackingorwith damagedtermi-
because that is where the female laythe eggs. Larvae nalportion maybe in disadvantage comparedto those
begin feeding on the apical portion of P. suberosa layingon intact shoots due to lowerlarval survivorship
shoots because the corresponding tissues are more andperhaps inferiorperformance. Second, itmayelu-
suitable for development offirst larval instars. Larvae cidate why females lay only isolated eggs on P.
feedonawiderrangeofleafagesinthelaterinstars. A suberosa shoots (Mugrabi-Oliveira& Moreira 1996b,).
progressive loss in selectivity as larvae age has been By avoiding multiple oviposition they may reduce in-
found in some insects, howeverthe underlying mech- traspecific competition for the limited amount of
anisms forsuch an ontogenetic changes still not being leaves available on many host plants. H. erato larvae
clearly understood (Lewis & van Emden 1986). This are cannibalistic, which is also an adaptation to host-
ontogenetic change in feedingpreference maybe re- plant size limitation (Brower 1997). Mugrabi-Oliveira
lated to changes in nutrition, plant chemistry or me- and Moreira (1996a) found for a P. suberosa popula-
chanical barriers offered by young and mature P. tion ofViamao County, RS, that in more than halfof
suberosa leaves. Later instars may be better able to H. erato eggs arelaidonplantswhosetotalleafareais
overcome defenses ofolder leaves and differences in less than that required for larval development. Food
foodqualityhavemosteffectonthe earlyinstars; thus, shortage in the fifth larval instar has profound effects
the necessity to make the correct choices may be onsurvivorship andsize attainedintheadultstage (D.
&
greatestforearlyinstars (Reavey 1993). Rodrigues G. R. P. Moreiraunpubl. data).
The choice tests showedthatlaterinstarlarvaepre- Thus, we confirm the importance ofvariation in in-
feryoungleaves independentofthe experience in the traspecific attributes ofP. suberosa plants, more pre-
previous instar. Thus, they are expected to be found cisely leaf age, in relation to preference and perfor-
mostly on the youngest surviving portions of host- mance ofH. eratophyllis larvae. Feedingpreferences
plants under field conditions. Results also indicated for young Passiflora auriculata tissues had already
that the age ofleaves consumed in agiven instar does been demonstrated through choice experiments by
not influence choices made by larvae during subse- Denno and Donnelly (1981) for larvae ofHeliconius
quentinstar. Evenfifth instarlarvae,whichwerecom- sara in Costa Rica. The physiological basis for such a
parativelyless selective in relation to leafage, showed feeding specialization in earlierinstars remains unde-
preference for young leaves when fed mature leaves termined. Itisknownthatseveralchemicalandphysi-
duringfourth instar. Thus, H. eratophyllis larvalpref- caltraits ofleaftissues, such as pubescence, hardness,
erence couldnotbe inducedin relation to P. suberosa water content, nutrients and secondary metabolic
leafage. compounds, vary according to age. It is also known
Inductionoffeedingpreference, asaresultofprevi- that these leafcharacteristics can play amajor role in
ous experience regarding particular plant species of- host-plantselectionorperformance ofherbivorous in-
&
fered as larval food, has been demonstrated through sects (e.g., Scriber 1984, Slansky 1993, Bernays
choice tests performed with several lepidopterans Chapman 1994, Fernandes 1994), includingfleabee-
Volume 53, Number 3 113
W
tSimeisltehyatanudseWiPassdsiofmlo(r1a98as5)hofsotunpdlaantssig(niTfhiocamnatsco1r9r8e7l)a.- CDoennonWvoiel,ery,R,.NF.eJw&. YM1o9.r8k0.A.. DProancntieclallyn.on1p9a8r1a.mePtartiteersntsatoisftihcesr.b2invdo.ryedo.n,
tion between leaf nitrogen content of several sym- Passiflora leaf tissues and species by generalized feeding
patricPassiflora species andlarvalgrowthrates ofHe- insects. EcolW. Entomol.6:11-16.
liconius ismenius and Heliconius melpomene in Costa Fernandes, G. 1994. Plantmechanicaldefensesagainstinsect
herbivory. Revta.bras. Ent.38:421-433.
Rica. They however, failedto find anydeleterious ef- Hanson, F. E. 1983. Thebehavioralandneurophysiologicalbasis
fects ofpotential toxins (including alkaloids, tannins offoodplantselectionbyIepidopterouslarvae,pp. 3-23.In S.
andcyanogeniccompounds) onlarvalgrowthrates and Amehcmhaandis(emds..),AHceardbeimviocroPursesisn,seNcetsw:Yhoorskt.-seekingbehavior and
survivorship. Although not quantified precisely yet, Jones, R. E. 1991.WHost location and oviposition on plants, pp.
there is a substantial increase in tissue toughnesswith 139-171. In J. Bailey & J. Ridsditl-Smith (eds.),
advance in age in P. suberosa leaves. In consequence, CRehparpomduacnti&veHablelh,aNvieowrYoofrikn.sects: individualsandpopulations.
ontogeneticchangesinleafage selectioncouldalsobe Kerpel, S. M. 1999. Mecanismos ecologico-eomportamentais
associatedwith morphological constraints on H. erato envolvidosnaselegaodaplantahospedeiraporHeliconiuserato
phyllis feeding apparatus. Early instars of some phyllis (Lepidoptera: Nymphalidae). Unpublished M.Sc.
Dissertation,InstitutodeBiociencias,UniversidadeFederaldo
grasshoppers and lepidopterans do not feed upon fa- RioGrandedoSul,PortoAlegre.
vored tissue or mature leaves because the mandibles Lewis,A.C. &H. F.VanEmden. 1986. Assaysforinsectfeeding,
are eithernothard enough for effectivelychewing, or pinpt.er9a5c-t1io1n9s..ISnprJi.ngRe.r-MVielrllearg,&NTe.wA.YoMrikl.ler (eds.), Insect-plant
their gape is not wide enough to grasp thick tissues Lopes, F. S. 1991. Padroes sazonais e evolucaodousode plantas
(Bernays 1991). hospedeiras de larvas por Heliconius erato phyllis (L.)
(Lepidoptera, Nymphalidae) na Serra do Japi, Sao Paulo.
Acknowledgments Unpublished Ph.D. Dissertation, Instituto de Biologia,
UniversidadeEstadualdeCampinas,Campinas.
WethankEInaMugrabi-Oliveiraforsupplyingtheplantsandlarvae Menna-Barreto, Y. & A. M. Araujo. 1985. Evidence for host
used in the experiments. Cassiano S. Moreira and Andre Silva plant preferences in Heliconius erato phyllis from southern
Gomes assisted in building the wooden frame supports. We are Brazil(Nymphalidae). Res. Lepid.24:41-46.
especially grateful to Woodruff W. Benson (UNICAMP) for Mugrabi-Oliveira, E. & JG.. R. P. Moreira. 1996a. Size ofand
significant improvements in the final version ofmanuscript made damage on shoots of Passiflora suberosa (Passifloraceae)
possible by his comments. We also wish to thank, Andrew V.Z. influence oviposition site selection ofHeliconius eratophyllis
Brower(OregonStateUniversity), GilbertoAlbuquerque(UNFla), (Lepidoptera: Nymphalidae). Revtabras.Zool. 13:939-953.
Lenice Medeiros(UNIJUI) andNicoletaT.N. Sabetzki (EPAGBI), . 1996b. Conspecificmimicsandlowhostplantavailability
andtwoanonymousreviewers,forsuggestionsthatimprovedearlier reduce egg laying by Heliconius erato phyllis (Lepidoptera:
draftsofthemanuscript. Financialsupportforthestudycamefrom Nymphalidade). Revtabras.Zool. 13:929-937.
aFAPEBGS grant, number94/50941.7, to G.R.P. Moreira.Thisis Perico, E. 1995. Interacao entre quatro especies de Heliconiini
contribution number 315 ofthe Zoology Department ofFederal (Lepidoptera: Nymphalidae) e suas plantas hospedeiras
UniversityofRioGrandedoSul. (Passifloraceae)emumaflorestasecundariadoRioGrandedo
Sul,Brasil Biociencias2:3-18.
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