Ceci est une version archivée de Batary2008 à 2009-08-10 16:19:30.
Egg distribution of the Southern Festoon (Zerynthia polyxena) (Lepidoptera, Papilionidae)
Par BATARY P., OERVOESY N., KOROSI A., PEREGOVITS L., 2008. In Acta Zoologica Academiae Scientiarum Hungaricae, 54 (4) : 401-410.
> Article original en PDF http://actazool.nhmus.hu/54/4/Azh54_4_Batary.pdf
P. BATÁRY(1,2), N. ÖRVÖSSY (1), Á. KŐRÖSI (3) and L. PEREGOVITS (1)
2 Current address: Agroecology, Georg-August University Waldweg 26, D-37073 Göttingen, Germany
3 Animal Ecology Research Group of the Hungarian Academy of Sciences and the Hungarian Natural History Museum, H-1083 Budapest, Ludovika tér 2, Hungary
We investigated environmental factors groupe da long hierarchical spatial scales influencing the egg density of a monophagous papilionid, the southern festoon (Zerynthia polyxena) on its food-plant, the birth wort (Aristolochia clematitis). Two patch level variables were considered : habitat type (black locust plantation, clearing and hummock) and food-plant patchsize. We
measured several plant variables at the egg-bearing shoots. We counted the number and measured the mean heigh to birth worts within the micro-environment of the egg-bearing shoots. We also measured the height and counted the leaves of each egg-bearing shoot itself. Plant apparency was defined as the height difference between egg-bearing shoots and the surround-ingones. Twovariablesweremeasuredontheegg-bearingshoots(henceatfood-plantscale):
numberofleavesandpositionofeggsontheleaf-storeys. Habitattypeaffectedthedistribu-
tionofeggs; blacklocust plantationsandhummockswerepreferredagainst clearings. At a
smallerscale,neithershootdensity,norfood-plantapparencyaffectedeggdistribution.Atthe
plantlevel,thenumberofeggsincreasedwiththenumberofleaves,andthepositionofeggs
alsoco-variedwitheggdensity,havingfewereggsinclusterspositionedhigheronshoots.We
concludethatspatiallycorrelateddataonbutterflyeggdistributionshouldbeanalysedconsid-
ering the intrinsically hierarchical structure of environmental factors.
Keywords:Zerynthiapolyxena (interwiki inconnu),oviposition,plant–insectinteraction,Aristolochiaclematitis,
food-plant, spatial scale
INTRODUCTION
Egg-layingisaparticularlyimportantecologicalinteractionbetweenphyto-
phagousinsectsandtheirfood-plants(RABASAetal.2005),therefore,oviposition
preferenceandlarvalperformancearecentraltopicsininsect–plantbiology(XUE
etal.2007).Femaleimagoescandiscriminateamongsitesbasedoncharacteristics
likeclimaticregimes, foodqualityandpotentiallevelsofcompetitionandpreda-
tion(BERNARDO1996). Variationintheseaspectsofoffspringenvironmentsaf-
fectsoffspringperformanceaswell.Incaseofbutterflies,egg-layingfemalesmay
exhibitbiasedpreferencestowardparticularplantspecies,towardparticularplant
Acta zool. hung. 54, 2008
Hungarian Natural History Museum, Budapest
individualsandeventowardcertainpartsofthefood-plant, whichwilldetermine
thephysical andchemical attributes towhichinsects respond(THOMPSON&
PELLMYR1991,BERNAYS&CHAPMAN1994).Sincetheemergingcaterpillarsare
relativelyimmobile, thekeytotheirsurvival anddevelopment isthefood-plant
choice of the female (PORTER1992).
Besideexperimental studies(e.g. SINGERet al. 1993), therearetwowide-
spreadmethodstostudytheegg-layingpreferencesoffemalebutterflies. Oneof
themisbasedontrackingthefemaleimagoesanddirectobservationofoviposition
(e.g.GRUNDELetal.1998,BERGMAN1999,ZIMMERMANNetal.2005,KŐRÖSIet
al.2008).Theothermethodtakesthepresence-absence,orthedistributionofob-
servableeggsonfood-plants(e.g.FLOATER&ZALUCKI2000,ELLIS2003,RABA-
SAet al. 2005). Thisindirect methodismoreflexibleallowingtheresearcherto
planthesamplingdesignandtohaveamuchlargersamplesize(dependingonthe
visibilityandidentificationabilityofeggs).However,theevidentdisadvantageof
thelattermethodcomparedtothefirst oneisthat it takesonlytheknownhost-
plantsintoaccountandleavesoutofconsiderationtheacceptablenon-hostplant
species (DEBOER& HANSON1984).
Severalstudieshaveinvestigatedthefactorsinfluencingeggdistributionat
different spatial scales. MCKAY(1991) studiedtheegg-layingrequirementsof
Brimstonebutterfly(Gonepteryxrhamni)inwetwoodlandsconsideringdifferent
food-plant–relatedspatial,physicalandchemicalfactors,andfoundthatmosteggs
werelaidonjuvenilehost-plant treesgrowinginsunnysites. Further, butterflies
appearedtoprefer host-treeswithlowconcentrationof secondarycompounds.
Similarly, FLOATERandZALUCKI (2000) exploredthe host-tree qualityand
apparencypreferencesof anAustralianmoth, Ochrogasterlunifer. Theyfound
moreeggbatchesonhigh-qualitytreesinopenhomogeneoushabitats,whileindi-
versemixed-specieshabitats, moreeggbatcheswerelaidonlow-qualityhighly
apparenttrees.InthecaseofNorthernBrownArgusbutterfly ’s(Ariciaartaxerxes)
oviposition,ELLIS(2003)describedtheeffectsofdifferentfood-plantcharacteris-
tics,microenvironmentalfactors,suchasfood-plantversusbaregroundcover,and
swardheight.Theeggsofthisbutterflyweremorecommononyoungerandlarger
food-plantleavesandonunmanagedvsmanagedsites(shortervegetation),while
food-plantdensityandbare-groundcoverdidnotaffectoviposition.Furthermore,
FARTMANN(2006)studiedtheeffectsoffood-plant,microenvironmentandmicro-
climateontheeggdistributionoftheDukeofBurgundyFritillary(Hamearisluci-
na).Hefoundalowerdepositionheightofeggsonthehost-plant(Primulaveris)
andthatmajorityofeggclutchessituatedatsitesthatreceivedirectinsolationbe-
tween09:00–17:00, andwhichhavemorethan60%herbcover. DENNIS(1996)
studiedtheovipositioninZerynthiacreticainrelationtofood-plantleaves,shoots
402 BATÁRY, P., ÖRVÖSSY, N., KŐRÖSI, Á. & PEREGOVITS, L.
Acta zool. hung. 54, 2008
andpatches.Hefoundthatfemaleslaidmoreeggsonlargeplantpatcheswithlarge
leaves, typically at the plant patch margin.
Wefoundonlytwostudiesthat focusedonmonophagousbutterfliesand
usedthepresence-absencedataofbutterflyeggsinrelationtofactorsatdifferent
spatial scalesinhierarchical nestedmodels. KÉRYet al. (2001)studiedthepres-
enceofMaculinearebelieggsacrossGentianacruciatafruits,genetsandpopula-
tions, andfoundthatthefactorsmeasuredatthegenetlevelweremoreimportant
thanthosemeasuredatpopulationlevel.RABASAetal.(2005)usedasimilarnested
designtoinvestigatetheeggpresenceofIolanaiolasontheColuteahispanica
shrubsatfruit,plantandpatchlevels.Theyshowedimportantfactorsinfluencing
the egg presence in each level.
Inthepresent studyweaimedtoinvestigatehierarchicallystructuredenvi-
ronmentalfactorsinfluencingthedensityanddistributionofZ.polyxenaeggsina
blacklocust –poplarplantationcomplex, wherethefood-plant ofthisbutterfly
was abundant.
MATERIALS AND METHODS
Study species
Thesouthernfestoon(ZerynthiapolyxenaDENISet SCHIFFERMÜLLER, 1775)isapapilionid
speciesthatreachesitsnorthernrangeinCentralEurope(TOLMAN1997).Thespeciesisprotectedby
lawinHungary.ItisamonophagousspeciesinHungaryfeedingonaherbaceousplant ,thebirthwort
(AristolochiaclematitisLINNEAUS ,1753,Aristolochiaceae).Thisfood-plantiscommonondisturbed
habitats, likefloodplains, orchards, roadsidesor blacklocust (RobiniapseudoacaciaLINNEAUS ,
1753,Fabaceae)andhybridpoplar(Populus×euramericana,Salicaceae)plantations.Theflightpe-
riodofthebutterflystartsfrommid/endAprilandlastsuntilthemid/endofMay.Thefemalesoviposit
ontheabaxialsurfaceofthefood-plantleaves,layingeitherasingleegg,orasmallerorlargercluster
ofeggs. ContrarytoZerynthiaruminaLINNEAUS , 1758whichhastwofood-plant species(Aristo-
lochiabaeticaLINNEAUS,1753,AristolochiaceaeandAristolochialongaLINNEAUS ,1753,Aristolo-
chiaceae),theZ.polyxenaismonophagousatleastinHungary;botheggsandlarvaewereobserved
onlyonA.clematitis(ROTHSCHILDetal.1972,JORDANO&GOMARIZ1994,ÖRVÖSSYetal.unpubl.)
Study area and sampling design
ThestudyareawassituatedontheHungarianGreatPlainnearCs évharaszt(CentralHungary ,
47°18’N, 19°26’E), inalandscapecomprisingoftreeplantations, mainlyblacklocust andpoplar
cultivarplantationsinterruptedbyclearings.The0 .02–0.03km2largeplotswereseparatedbyhum-
mocksoriginatingfromthelastharvestoftheplantationsandconsistedofstumpsandrootscovered
bysoil,providinganidealplaceforthebirthwort.Aclumpoffood-plantsconsistingofatleastfive
shootsperm2andseparatedbyatleast10mfromotherfood-plantswasconsideredasapatch. We
chose4–4food-plant patchesforsamplinginthethreeavailablehabitat types, i.e. inblacklocust
EGG DISTRIBUTION OF ZERYNTHIA POLYXENA (LEPIDOPTERA, PAPILIONIDAE) 403
Acta zool. hung. 54, 2008
plantations, in clearings and in hummocks. In our earlier study on the same study area, we found that
the imagoes avoided the poplar plantations (ÖRVÖSSY et al. 2005). Each of these food-plant patches
were covered by several thousands of birthwort shoots. We randomly selected 10 points within each
patch, where we checked food-plant shoots for eggs in a 5-meter radius circle. Since relatively few
food-plant shoots had leaves loaded by eggs, we stopped further searching after finding the first shoot
with eggs. These circles were covered by an average of 775 food-plant shoots. From the total of 120
randomly chosen circles, 98 contained eggs, and circles without eggs were excluded from the analy-
ses. The flight period (26 April to 15 May) ended before the egg searching (17–23 May), thus new
ovipositions during the sampling period could not cause a bias. No larvae were found during the egg
survey.
During the egg-survey several environmental variables were measured in the close proximity
of the egg-bearing shoots. We grouped these variables according to spatial scales. The habitat type of
a given food-plant shoot (black locust plantation, clearing or hummock) was interpreted as a patch
level variable, and incorporated into the model as a factor. To characterise the habitat types we
counted the food-plant shoot density on 20 randomly selected 2×2 m squares in each food-plant
patches. We measured the size of patches. To characterise the microenvironment of the selected
food-plant shoots, we counted the number of shoots and measured the mean shoot height in a 1×1 m
square. We also measured the height and counted the leaves of egg-bearing shoots. We expressed
food-plant apparency as the height difference between an egg-bearing shoot and the mean of sur-
rounding shoots in the 1×1 m square. On the egg-bearing shoots two variables were measured; the
number of food-plant leaves and the position of the egg or the egg cluster (hence we call the scale of
these variables as food-plant level to differentiate from the scale of variables measured in the direct
proximity of the egg-bearing shoots, i.e. microenvironment level). The latter one was expressed as
the number of leaves below the leaf bearing the egg(s) divided by the total number of leaves.
Statistical analysis
The effects of above mentioned environmental variables on egg distribution were analysed in
general linear mixed-effects models with the Restricted Maximum Likelihood method. The normal-
ity of the distribution of eggs per leaf was assessed using normal quantile plots. Log-transformation
was applied to handle non-normal distribution. The following non-correlated variables were consid-
ered in the statistical model: 1) habitat type as a factor and patch size as a co-variable at patch level; 2)
at the microenvironment level, the food-plant shoot density around the egg-bearing shoot and
apparency; 3) the number of food-plant leaves and the position of eggs at food-plant level. Since
food-plants were nested within food-plant patches, the latter was used as a random factor. Although
food-plant leaves were also nested within food-plants, we could not include food-plant as a random
factor in the model, because it would have had too large effect relative to the residual. Altogether
there were only five food-plant shoots with eggs on two leaves and one food-plant shoot with eggs on
three leaves. Leaves without eggs (1036) were excluded from the analysis. Furthermore, we com-
pared models with and without the inclusion of food-plant as a random factor. We found that the two
models were significantly different (L-ratio = 59.8; P < 0.0001), and the model without food-plant
had smaller AIC value, indicating that this model was more supported. By right of these, we decided
to apply the latter model. The calculations were made using R (version 2.2.1; R DEVELOPMENT CORE
TEAM 2006) and the nlme package for R (version 3.1, PINHEIRO et al. 2007).
404 BATÁRY, P., ÖRVÖSSY, N., KŐRÖSI, Á. & PEREGOVITS, L.
Acta zool. hung. 54, 2008
RESULTS
We registered 597 eggs of Z. polyxena laid either singly, or in small (2–8
eggs) or large (10–99 eggs) clusters on the underside of food-plant leaves. During
the survey we did not find any larvae nor hatched eggshells. The habitat type sig-
nificantly affected the distribution of eggs (Table 1). When we compared the
food-plant shoot density between habitat types with a one-way ANOVA, we found
significant difference between them (F = 23.207, P < 0.001, N = 240, Fig. 1, Tukey
HSD post-hoc tests showed that all habitat types differed significantly from each
other regarding food-plant shoot density). There were significantly more eggs on
food-plants in black locust plantations and hummocks than in clearings (Fig. 2). At
the microenvironment level, neither food-plant shoot density, nor food-plant appar-
EGG DISTRIBUTION OF ZERYNTHIA POLYXENA (LEPIDOPTERA, PAPILIONIDAE) 405
Acta zool. hung. 54, 2008
Table 1. Linear mixed models for testing the effects determining the egg-laying preference of Z.
polyxena at different levels. Bold p values indicate significant effects.
Level Variable numerator
DF denomi-
nator DF F P
Patch Habitat type 2 8 15.777 0.002
Patch Food-plant patch size 1 8 0.442 0.525
Microenvironment Food-plant density 1 89 1.347 0.249
Microenvironment Food-plant apparency 1 89 1.219 0.273
Food-plant Number of food-plant leaves/shoot 1 89 5.668 0.019
Food-plant Egg place 1 89 28.657 < 0.001
0
2
4
6
8
10
12
Black locust Clearing Hummock
Habitat types
N
um
be
r
o
f
fo
od
-p
la
n
t
sh
oo
ts
pe
rm
2
a
b
c
Fig. 1. Mean (±SE) number of food-plant shoots per m2 in the three habitat types. The different letters
indicate significant differences at P < 0.05
406 BATÁRY, P., ÖRVÖSSY, N., KŐRÖSI, Á. & PEREGOVITS, L.
Acta zool. hung. 54, 2008
0
2
4
6
8
10
Blacklocust Clearing Hummock
Habitattypes
N
um
be
r
o
fe
gg
s
pe
r
fo
od
-p
la
n
t
le
a
f
a
b
a
Fig.2.Mean(±SE)numberofeggsofZ.polyxenaperfood-plantleafinthethreehabitattypes.The
different letters indicate significant differences at P < 0.05
0.2 0.4 0.6 0.8 1.0
1
2
3
4
Eggposition
Fig.3.Eggpositionontheplant’sleaf-storeys(thenumberofleavesbelowtheleafbearingtheegg(s)
dividedbythetotalnumberofleaves)isplottedagainstlognumberofeggs.Smallervalueofeggpo-
sitionindicatesthattheeggsareonlowerleaves.Thesolidlinerepresentsthefixeffectofeggposi-
tion of the fitted model
encyaffectedtheeggdistribution(Table1 ).Atthefood-plantlevel,thenumberof
eggsincreasedsignificantlywiththenumberoffood-plantleaves/shoot(Table1 ).
Finally, thepositionofeggsalsoaffectedsignificantlythenumberofeggs;there
were more eggs on the lower part of the food-plants than upward (Fig. 3).
DISCUSSION
Thebehaviourleadingtooviposition, i.e. selectionofovipositionsite, isa
complexprocess,becausesuccessfulovipositiongreatlycontributestoindividual
fitness(SCHOWALTER2006).However,femalesdonotalwaysselectthemostap-
propriatehostandnewlyhatchedlarvaemayrejecttheplantonwhichtheyhatch
(BERNAYS&CHAPMAN1994).Soegg-layingfemalescanmakeerrorsandlarvae
cancorrectittosomedegree, butiftheyaretosurvive, i.e. tomaximisetheirfit-
ness,thefemales’preferenceandthelarvae’sperformanceshouldoverlapasmuch
aspossible.Inthecurrentstudy,theeggdistributionofZ.polyxenawasaffectedon
twolevels,basicallybyhabitattypeandalsobycharacteristicsatfood-plantlevel,
but not by factors at the microenvironment level.
Thehabitatdifferencesfoundinthepresentstudy,i.e.theblacklocustplanta-
tionandhummocksweremorepreferredthanclearings,maywellbeinterpretedas
thebutterflies’preferenceagainstareasthatweremoreexposedtodirectsunshine
orcold. FARTMANN(2006)reportedthat H. lucinapreferredthosesitesforovi-
positionincalcareousgrasslands,wherethefood-plant(Primulaveris)potentially
receiveddirect insolationbetween09:00and17:00. MCKAY(1991) foundthat
mosteggsofG.rhamniwerelaidonisolatedjuveniletrees(Frangulaalnus)grow-
ingatsunnysites.Thesestudiesshowthatovipositionsitepreferencesmayensure
an optimal microclimate for the development of the larvae.
Inourcase,patchsizedidnotaffectthenumberofeggslaid,whileinthecase
ofZ.creticaDENNIS(1996)showedthatlargerfood-plantpatcheshadmoreeggs.
However,wehavetocalltheattentiontothefactthatinthelatterstudythepatches
weremappedonamuchfinerscale(food-plantpatchsizerange:25to2400cm2)
than in our case (food-plant patch size range: 661 to 11954 m2, mean: 3384 m2).
At themicroenvironment level, neitherfood-plant shoot density, norfood-
plant apparencyseemedtoact asalimitingfactoroneggdensity. However, we
havetomentionthat food-plant shootsoccurredinaverylargenumberineach
habitat.Moreover,food-plantshootdensitywashighestintheclearings,generally
twotimeshigherthanintheblacklocustplantationandabout15%higherthanin
thehummocks(Fig. 1). Thisalsosuggeststhat thehabitat typeeffect isnot con-
nectedwiththefood-plant availability. Incontrast toourresults, DENNIS(1996)
EGG DISTRIBUTION OF ZERYNTHIA POLYXENA (LEPIDOPTERA, PAPILIONIDAE) 407
Acta zool. hung. 54, 2008
foundinhisfinescalestudythatfood-plantshootnumberwasoneofthemostim-
portant factorsaffectingtheeggdensityofZ. cretica. Regardingfood-plant ap-
parency, theheightofegg-bearingshootsweresignificantlyhigherthanthosein
themicroenviroment(pairedt-test,t=8.956,P<0.001),however,itprobablyin-
fluences only the food-plant selection of butterflies, but not the egg load.
Thenumberoffood-plantshootleavesshowedapositiveeffectoneggnum-
bersandmoreeggswerefoundonthelowerleavesoffood-plantshoots.Inourear-
lierstudy,weobservedthatatthebeginningofflightperiodthefood-plantswere
quitescarceandjuststartedtodevelop,therefore,thefirstfemaleshadlimitedchoices
(ÖRVÖSSYetal.2005).Thisprobablymeansthatearlysproutingfood-plantshave
someadvantagecomparedtothelatesproutingones,therefore,theycouldbemore
apparent.Sincefood-plantshootsreceiveeggsatayoungerstage,theeggsaresitu-
atedonlowerleaves. Moreover, at thisperiodthefemaleshavelargeeggload,
whichcouldalsocausethattheylayeggsinclustersratherthansingleeggs. This
result suggeststhat temporal aspectsarealsoimportant inoviposition. DENNIS
(1996)alsoemphasizedtheimportanceofthedurationoffood-plant patches; he
suspectedthat food-plant patchesavailableforlongerperiodsaremorelikelyto
havemorelarvae. Investigatingacongenericspecies, Z. rumina, JORDANO&
GOMARIZ(1994)foundthatthefreshlyhatchedlarvaeconsumedtheyoungerand
softer leaves of thefood-plants. This couldstandbehindthat theobservedZ.
polyxenafemalesalsolaidtheeggsonyoungleaves,however,witheggsearching
itwasnotpossibletoinvestigatethetemporaleffects. Anotherpotentialexplana-
tionfortheyoungleafselectioncouldbethatfemalesselectthesebecauseoflower
concentrationsofsomedefencechemicals. However, ROTHSCHILDet al. (1972)
describedthatZ. polyxenacontainedandstoredefficientlytwoaristolochicacids
which were presumably present in its food-plant, inA. clematitis.
InthisshortstudyweshowedthattheeggdistributionofZ .polyxenawasaf-
fected by several components acting at different spatial levels. We have to
emphasisethat suchacomplexprocess, likeoviposition, shouldalsobeinvesti-
gatedbythedirecttrackingoffemales, whichcouldilluminatefurtheraspectsof
eggdistribution.Asaconclusion,wealsounderlinethatspatiallycorrelateddatain
eggdistributionstudiesneedtobeanalysedconsideringanintrinsicallyhierarchi-
cal structure of environmental factors (RABASAet al. 2005).
*
Acknowledgements–Twoanonymousrefereesprovidedconstructiveremarksthatconsider-
ablyimprovedthemanuscript.WeareindebtedtoLAJOSR ÓZSAforvaluablecommentsandlinguis-
ticrevisionsonthemanuscript.ThestudywassupportedbytheNationalR &DProgramme,entitled
“TheoriginandgenezisofthefaunaoftheCarpathianBasin:diversity (interwiki inconnu),biogeographicalhotspotsand
natureconservationsignificance”(contract no. 3B023–04).
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