Effects of canopy coverage on the immature stages of the Clouded Apollo butterfly [Parnassius mnemosyne (L.)] with observations on larval behaviour

2005·0.17 MB·

by  Panu Välimäki

©EntomologicaFennica.17June2005
Effects of canopy coverage on the immature stages
of the Clouded Apollo butterfly [Parnassius mnemosyne (L.)]
with observations on larval behaviour
PanuVälimäki&JuhaniItämies
Välimäki, P. & Itämies, J. 2005: Effects of canopy coverage on the immature
stagesoftheCloudedApollobutterfly[Parnassiusmnemosyne(L.)]withobser-
vationsonlarvalbehaviour.—Entomol.Fennica16:117–123.
The immature stages of the Clouded Apollo (Parnassius mnemosyne) are as-
sumed to be thermophilic due to the possible time limitations and variable
weatherconditionsduringtheirdevelopment.Thus,thedegreeofcanopycover-
agemayaffecthabitatusebythespecies.Weexploredthespatialdistributionof
larvaeandthedevelopmenttimeofpupaeundervariablecanopycoveragecondi-
tions. Larvae were most abundant in the areas exposed to direct sunlight, al-
thoughthelastinstarlarvaearemobile.Larvaealsobaskedunderlitterbetween
theirforagingperiods,probablytoenhancedigestionandthefoodintakerate.
Moreover,pupaldevelopmentwasretardedbyincreasingcanopycoverage.Pro-
longedpupaldevelopmentandlarvalavoidanceofCorydalisgrowthsundertree
canopiesindicatethatthespeciessuffersfromovergrowingandconsequentlyin-
creasingcanopycoverage.
P.Välimäki&J.Itämies,UniversityofOulu,DepartmentofZoology,P.O.Box
3000, FI-90014 University of Oulu, Finland; E-mail: [email protected],
[email protected]
Received28May2003,accepted13February2004
1.Introduction
natureconservationactin1976[Maa-jametsä-
talousministeriö (1976), see also Mikkola &
The Clouded Apollo butterfly [Parnassius Häkkinen(1977)].However,effectiveconserva-
mnemosyne(L.)]isconsideredathreatenedspe- tionisnotpossibleifthebiologyofthespeciesis
ciesinnorthernandcentralEurope(Heath1981, notadequatelyknown.
Aagaard et al. 1997, Konvicka & Kuras 1999, Adults prefer to breed and forage on open
Rassietal.2001).Itsdistributionhasdeclinedre- meadows with abundant larval food plant and
markablyinFinlandsincetheearly20thcentury nectar sources (Luoto et al. 2001). Larvae are
(Mikkola 1979, Väisänen & Somerma 1985). mostlyfoundatthesunnymarginsofhumidde-
Thistrendhasbeenrelatedtochangesinagricul- ciduousforests(Megléczetal.1999).Although
tural practices and, consequently, to decreasing thelarvalfoodplantsvaryspatially,theClouded
areaanddeterioratingqualityofformerlyhabit- Apolloislocally monophagous.InFinland,lar-
ablemeadows(Väisänen&Somerma1985).The vae feed only on Corydalis solida (Somerma
CloudedApollowasprotectedinFinlandbythe 1997), butinNorway andHungary, larvaefeed
118 Välimäki&Itämies (cid:127) ENTOMOL.FENNICAVol.16
on Corydalis intermedia (Aagaard & Hanssen andtobefoundonlyontheopenandsunnyparts
1989)andCorydaliscava(Megléczetal.1999), ofCorydalisgrowths.Ifdecreasingtemperature
respectively. delays pupal development as well, increasing
Corydalissolidagrowsinatleasttwodiffer- canopycoveragemaydecreasetheeffectivepo-
enthabitatsinSWFinland.Itisabundantinde- pulationsize.Thus,theCloudedApollomaysuf-
ciduousforestsdominatedbyAlnusspp.,Prunus ferfromovergrowing.
padusorBetulaspp.alongtheseashore.Onthe
other hand, it also grows on open or semi-open
2.Materialandmethods
mesic meadows, pastures and abandoned fields
(Välimäkietal. 2000, Luoto etal. 2001). Alo-
callymonophagousspecies,theCloudedApollo 2.1.Studyarea
isobligatorilydependentonC.solidathatflow-
ersveryearlyinthespring.Larvaemustdevelop ThestudyareaislocatedinSWFinland(61°13’
fastbecausetheirhostisavailableforonlyafew N,21°31’E).ThelandscapeistypicalofFinnish
weeksbeforesenescence.However,theweather agriculturalareas–mostlydenseNorwayspruce
isusuallyquiteunpredictableandcoldinFinland (Piceaabies)forestorverydryScotspine(Pinus
atthetimeofthelarvaldevelopment,whichre- sylvestris) heath forest fragmented by small
tardslarvalgrowth. meadows and cultivated fields. In spring 1999,
Inaddition,Corydalisspeciescontainawide wesurveyedthewholestudyarea(2.7km2)inde-
rangeofsecondarymetabolites,suchasalkaloids tail to map the distribution and location of C.
(Naruto & Kaneko 1972, Naruto et al. 1972, solidagrowths(Välimäkietal.2000).
Siegler1998).Theseplantcompoundsmayactas
a defence mechanism against herbivores
(Fraenkel 1959), and they may result in a plant 2.2.Distributionoflarvae
becominginadequateasfood(Scoble1995).The
effectsofsecondarymetabolitesonspecialisther- Theeffectofcanopycoverageonthespatialdis-
bivores are, nevertheless, not necessarily detri- tribution of larvae was studied in 2000 (18–19
mental(Maceletal.2002).Thisindicatesthatthe May)inalarge(ca.6,700m2)continuousCory-
evolutionofdefensivecompoundsmayratherbe dalisgrowthwithcanopycoveragebytreesand
drivenbygeneralistherbivores,whichalsosuffer bushes [mostly birches (Betula spp.) and hag-
most, as suggested by Hägele & Rowell-Rahier berry(Prunuspadus)]varyingfrom0%to100%.
(2000). Although Corydalis is available for lar- Atfirst,wedividedthestudypatchinto10mx10
vaeonlyephemerally,itmaybeaveryprofitable m squares that were classified according to the
host, because the detrimental secondary sub- canopycoveronascaleof1–3[1=<10%(open),
stances may create an almost competition-free 2 = 20–59% (semi-open), 3 = >60% (over-
spaceforaspeciesadaptedtothechemicalcom- grown)].Birchleaveshadreachedapproximately
positionoftheplant. three-fourth of their final size, and hagberry
Theaimofthispaper istwofold. (a) Firstly, leaveswerealmostfullygrownatthattime.Most
we study the effects of canopy coverage on the oftheCloudedApollolarvaecollectedforrearing
spatialdistributionoflarvaeandpupaldevelop- wereintheirfinalinstarandpupatedwithinthe
ment. (b) Secondly, we present observations on nextweek.
larvalbehaviourinthenaturalenvironment.Lar- Toexplorethedistributionoflarvae,wecal-
val development is not only affected by food culatedtherelativenumberofeatenshootsfrom
quality,butalsobytemperatureandtheinterac- 16 randomly-chosen squares in each coverage
tionsofthesetwofactors(Stamp&Yang1996). class.Bitingmarkswererecordedas1(detectable
Thus, overgrowing by trees and bushes and the bites)or0(nodetectablebites).Markswerere-
consequentlydecreasingdaytimetemperaturein cordedfromthe20shootsgrowingclosesttothe
thegroundlayerusuallyretardlarvalgrowth.If centrepointofeachsquare.Weassumedthatthe
thetimeavailableforlarvaldevelopmentisacru- relative number of eaten shoots would indicate
cialfactor,larvaeareexpectedtobethermophilic the relative abundance of larvae in each square
ENTOMOL.FENNICAVol.16 (cid:127) DistributionandbehaviourofP.mnemosynelarvae 119
with reasonable accuracy. Biting marks were 2.4.Larvalbehaviour
countedduringtwosuccessivedaystoensurethat
the ratio of eaten to intact shoots would not Observations on larval behaviour were made in
changeasthecountingproceeded. 2000 and 2002 in the natural environment. In
ThelarvalbitingmarksoftheCloudedApollo 2000, we made only subjective notes while
are species-specific and therefore easily distin- searchingforlarvaefortherearingexperiment(n
guishablefromothercausesofdefoliation,such =13).Themainaimwastoexploretheparasitoid
asdeerbites.Toexcludethepossibilityofother pressuretowardstheCloudedApolloinourstudy
insectherbivores,weexaminedcarefullythevi- area.Onthe14thofMay2002,westudiedlarval
cinityofhundredsofeatenCorydalisshoots,but behaviour in a more detailed way by observing
didnotfindanylarvaeofotherinsectspecies.The thefeedingbehaviourofthelastinstarlarvae(n=
onlyotherlepidopteranspeciesfoundfeedingon 10)onawarmandsunny day.Werecordedthe
C. solida was a polyphagous tortricoid moth, timespentbylarvaeinforaging,afterwhichwe
Cnephasiaasseclana(D.&S.).Thelarvaeofthis continuedtofollowlarvalbehaviourforanother
moth,unlikethoseoftheCloudedApollo,always 30minutes.Toexplainlarvalbehaviour,wemea-
spinafewleafletstogether.Althoughwecannot suredthetemperaturebothaboveandunderthe
be absolutely sure that all of the counted biting surface ofthe litter layer where the larvae were
markshadbeencausedbylarvaeoftheClouded hiding.Theaccuracy ofthesetemperaturemea-
Apollo,itseemsunlikelythatanyotherherbivore surementswas0.1degreesofcentigrade.
couldhavebeenresponsibleforthedefoliationof
C.solidainourstudyarea.
Temperaturemeasurementsinthethreecan- 2.5.Dataanalysis
opy-coverageclasseswerecarriedoutonthe14th
ofMayin2002.Temperatureinthegroundlayer Variation in therelativenumber ofeaten shoots
wasmeasuredat12randomlychosensites(4in among canopy coverage classes was compared
eachclass).Measurementswererepeatedatinter- with non-parametric Kruskal-Wallis one-way
valsof15minutesfrom10:00AMto12:10PM. ANOVA and non-parametric Tukey’s post hoc
Corresponding ambient temperatures were re- test.Theeffectofcanopycoverageonpupalde-
cordedattheheightof1.5maboveeachmeasure- velopmenttimewasexploredwithparametrict-
mentsite. test. Temperature comparisons among canopy
coverage classes were made with ANOVA and
LSDposthoctest.Thedifferencesintemperature
2.3.Developmenttime onandunderthesurfaceofthelitterlayerwere
tested with paired samples t-test. All statistical
Theeffectofcanopyshadingonpupaldevelop- analyses, excluding Tukey’s post hoc test, were
menttimewasstudiedin2002byrearingindivid- conductedwiththeSPSSforWindows10.0sta-
uals under different kinds of canopy coverage. tisticalsoftware.
Larvae(n=17)werecollectedonthe14thofMay
2002fromthestudyareaandrearedintopupaeon
3.Results
freshC.solida.Afterpupation,theoffspringwere
randomly divided into two treatments. Group 1
wasplacedonanopenfieldexposedtodirectsun- 3.1.Distributionoflarvae
shine.Group2wasplacedundertreeswith50%
canopy coverage to simulate an overgrown The relative number of eaten shoots varied
meadow. During the study, temperature in the amongcanopycoverageclasses(¤2=9.594,df=
ground layer was recorded continuously with 2,p=0.008)(Fig1).Inthesquaresclassifiedas
thermometers.Fromthermometerdata,wecalcu- open,11%oftheshootsweredefoliatedtosome
latedthecumulativeheatsummationrequiredfor extent by larvae, while only 7% and 3% of the
thedevelopmentofpupaeintoadults.Theresults shoots in thesemi-open and overgrown squares
arereportedasmeans±1S.E. wereeaten,respectively.Thisvariationwasnon-
120 Välimäki&Itämies (cid:127) ENTOMOL.FENNICAVol.16
Fig.2.Averagetemperature(°C)inthegroundlayer
atopen,semi-openandovergrownsites,andcorre-
spondingambienttemperature1.5mabovethe
groundbeforenoonon14thofMay2002.
significant between the open and semi-open
squares(q=2.189,p>0.05),butsignificantbe-
tween the open and overgrown squares (q =
4.214,p<0.05).
Averagetemperatureinthegroundlayervar-
ied among the canopy coverage classes (F =
3,12
65.699, p <0.001) and was evidently higher at
openthansemi-openandovergrownsites(LSD
posthoctest:p<0.001)(Fig.2).Althoughtheav-
erage temperature in the ground layer in semi-
opensiteswasconsistentlyhigherthantheambi-
ent temperature, the difference was non-signifi-
cant(LSDposthoctest:p=0.06).
3.2.Developmenttimeofpupae
Theaveragerequiredheatsummationfrompupa-
tion to the emergence of adults was 300° C
(±85.6)intreatment2(shade)and286°C(±42.0)
intreatment1(sunshine).Therewasnovariation
inthisrespectbetweenthetreatments(t=0.394,
df = 11, p = 0.701). However, it took longer to
reach the required heat summation under trees
thanonopenfield(Fig3).Consequently,thepu-
palstagewassignificantlylongerinshadethanin
sunshine(t=3.784,df=11,p=0.003)(Fig.4).
Fig.1.Distributionoftherelativenumbersofeaten Butterflieshatchedafteranaverageof16.5(±2.6)
Corydalissolidashootsundervariablecanopycover- and26.8(±7.2)daysafterpupationonopenfield
age. exposed to direct sunshine and under trees, re-
spectively.Inaddition,pupalsurvivalseemedto
belessgoodintheshadycomparedtothesunny
environment(62%vs.100%).
ENTOMOL.FENNICAVol.16 (cid:127) DistributionandbehaviourofP.mnemosynelarvae 121
Fig.3.Cumulativeheatsummationatasiteexposed
todirectsunshine(treatment1)andasitewith50%
canopycoverage(treatment2)16.V.–27.VI.2002.
Fig.4.Averagepupaldevelopmenttimeofthe
CloudedApollo(Parnassiusmnemosyne)atasiteex-
3.3.Larvalbehaviour
posedtodirectsunshine(treatment1)andasitewith
50%canopycoverage(treatment2).Asterisksshow
Larvaestartedtheirfeedingperiodatabout11:00 statisticalsignificancebetweentreatments(***=p
AM,whenambienttemperatureat1.5mheight <0.01).
was18°C.Atthesametime,theaveragetemper-
atureinthegroundlayeratopensiteswas26°C.
4.Discussion
Larvae in that particular patch started feeding
quitesimultaneuosly,indicatingthattheremight
be a threshold temperature that needs to be ex- Canopycoverageaffectssignificantlythespatial
ceededforefficientforaging.Larvaeforagedfor distribution of Clouded Apollo larvae within a
anaverageof10minutes(9.7±2.07),afterwhich continuous Corydalis growth, with most larvae
theydroppedtotheground.Whendonewiththeir inhabitingtheopenpartsofthemeadow,where
feeding, they crawled rapidly 10–30 cm away the average temperature in the ground layer is
fromtheeatenshoot.Theyusuallybaskedindi- higherthanintheshadyparts.Thelarvaldistribu-
rectsunshineforafewminutesandthenhidun- tionandbehaviouraswellastheretardedpupal
der detritus (usually old brownish leaves of de- developmentduetoincreasingshadingbyleaves
ciduoustrees)justbeneaththesurfaceofthelitter, indicatethatthespeciesisthermophilicandthere-
wheremoultingandpupationalsotakeplace.The foresuffersfromovergrowingofitshabitats.Asa
temperatureofthehidingplaceswasconsistently consequence,Corydalisshootsgrowingindense
higher (10% on average) than the ambient tem- deciduous forest are not of great value for the
peraturejustabovethelitterlayer(t=–4.164,df= CloudedApollo.
10,p=0.002).Larvaealwayshidformorethan The distribution of biting marks suggested
30 minutes between successive foraging ses- thatlarvaearemostabundantinareasexposedto
sions.Thenextforaginghardlyevertakesplace directsunlight.Therewerepracticallynosignsof
on the same plant as the previous session, but larvaein themostovergrown parts ofthestudy
ratheronarandomlychosenshootnearthehiding patch, although some mated females were ob-
place.Feedingwentonuntilthelateafternoonin servedtherein1999and2000.Thepatternmay
sunny weather. Early in the morning and in arise fromoffspring preference or performance,
cloudyweather,larvaewerefoundtoremainhid- but also from the oviposition behaviour of fe-
ingamonglitter. males.Femalesmaydeterminethehostusebythe
Larvaefedonleaves,flowersandfreshcores speciesiflarvaearerelativelyimmobileandcon-
ofC.solida,butseemedtoavoidseeds.Usually, sequently restricted to the resources and place
the whole leaflet and the attached petiole were chosen by the ovipositing female (Singer et al.
eaten, which made the biting marks less detect- 1991,Janz&Nylin1997).Nevertheless,thelast
able. instar larvae of the Clouded Apollo moved re-
122 Välimäki&Itämies (cid:127) ENTOMOL.FENNICAVol.16
peatedlyamongC.solidashoots,suggestingthat egy that maximizes the food intake rate. In that
larvae may be capable of moving, even quite sense, the short foraging sessions and the rela-
freely, within their habitat. However, the food tively long hiding phases seem quite peculiar.
plantsgrowingundertreesandbusheswerestill Several reasons may explain this larval behav-
mostly intact. This indicates that larvae may iour.Larvaemayhideinordertoavoid(a)preda-
avoidshadyCorydalisgrowths.Eveniffemales torsand(b)parasitoidattacks,or(c)theymayac-
did not lay any eggs on Corydalis growths in celeratetheirdigestionandincreasetheirfoodin-
overgrown areas, mobile larvae could be ex- takeefficiencybybaskingunderlitter.
pectedtocolonizethisresourcebeforeleafburst, Inthefirsttwocases,thereareapparentcosts
whenovergrownareasarepracticallyassunnyas intermsofincreasedmortalityrelatedtofeeding
openones.However,theearlylarvalinstarsmay visible to enemies. However, many papilionid
notbeequally mobilethanthelasttwo.Habitat larvae, including the Clouded Apollo, are dis-
useby CloudedApollolarvaemay thereforebe tasteful and aposematically patterned (Scoble
initially determined by the ovipositing female, 1995).Aposematismusually reducestheriskof
butbecauseoftheincreasinglarvalmobility,the predationorthedetrimentaleffectsofpredatorat-
observeddistributionmaylateractuallyrepresent tacksonlarvalsurvivalsignificantly(Wiklund&
larvalhabitatpreferenceaswell. Sillén-Tullberg 1985, Roper & Redston 1987,
Whatever the reason for this larval distribu- Tullrot & Sundberg 1991). The secretory prod-
tion,itisevidentthatopenareasareessentialfor ucts of the specialized defensive organs of
thespecies.Duetotheincreasingcanopycover- papilionid butterflies, the osmeteria, may affect
age, cumulative heat summation accumulates not only predators, but also parasitoids (Scoble
moreslowlyinovergrownthaninopenhabitats, 1995). In accordance, out of 30 reared larvae,
which explains the observed variation in pupal nonewereparasitized,indicatinglowparasitoid
development times between the two treatments. pressuretowardstheCloudedApollobutterflyin
Ourresultssuggestthata50%increaseincanopy our study area. Thus, predation pressure and
coveragedoesnotonlyincreasethepupaldevel- parasitoidattackshaveprobablyonlyaminoref-
opmenttime1.5-fold,butmayalsodecreasesur- fectonlarvalbehaviour.
vivalbyover30%.Theprolongedpupaldevelop- Theextenttowhichlarvalbehaviourwasaf-
mentpersemightnotbeanoverwhelmingpro- fectedbyavoidanceofnaturalenemiesneverthe-
blemforthespeciesbecausethelarvalhostplant lessremainswithoutfinalelucidation.Generally,
has already wilted before females begin to lay however,thefoodintakerateandthegrowthrate
eggs. However, the variable pupal development of the immature stages of ectothermic animals
timeduetounequally increasingcanopy cover- usually increase along with rising temperature
age decreases effective population size by de- (Heinrich1973).Becausetemperaturewascon-
creasingthenumberofcontemporarilyflyingin- sistentlyhigherjustbeneaththanabovethesur-
dividuals,whichmay alsoaffectpopulationdy- faceofthelitterlayer,theneedforincreasedfood
namicsbydecreasingthematingsuccessofindi- digestion seems the most plausible explanation
viduals[seeKuussaarietal.(1998)fortheeffects forthelarvalbehaviourobservedhere.Thedif-
ofdensity-dependentmatingsuccessonpopula- ference in temperature may be even more pro-
tionsurvival].Moreover,duetothelarvalavoid- nounced,especiallyincoastalareas,wherewind
anceofshadyhabitats,anincreasingproportion coolsambienttemperatureeffectively inspring.
offoodresourcesbecomesuselessduringlatelar- Inadditiontothepossibilityofmoreeffectivedi-
val development, when the food intake rate is gestion, larvaemay alsobenefitfromareduced
usually highest. Therefore, overgrowing might riskofdesiccationbyhidingamongthelitterwith
alsoincreaselarvalmortality,atleastifCorydalis highrelativehumidity.Thus,behaviourthatmay
isscarce. atfirstsightseemmaladaptivecouldactuallyturn
Theearlysenescenceofthehostisprobably outtomanifestadaptationtotheshortseasonof
the most evident problem faced by larvae. Fast thehostandtheunstablethermalconditionsdur-
developmentrequiresaneffectiveforagingstrat- inglarvaldevelopment.
ENTOMOL.FENNICAVol.16 (cid:127) DistributionandbehaviourofP.mnemosynelarvae 123
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