Phylogenetic, habitat, and behavioural aspects of possum behaviour in European lepidoptera

2006·3.8 MB·English

by  Tim G Shreeve

journalofResearch ontheLej)idol)l('ra 39; 80-85,2000 (2006)
Phylogenetic, habitat, and behavioural aspects of possum behaviour
in European lepidoptera
Tim G. Shref:vp:
Oxford Brookes University, De|)artinent of Biological and MolecularSciences, Headinglon,Oxford0X3OBP, U.K.
[email protected]
Roger L.H. Dennis
Oxford BrookesL'niversity, De|rartinent of Biological and MolecularSciences, Headington, Oxford0X3OBP, U.K.
NERCCentreforEcologyand Hydrology', MonksWood,Abbots Ripton, Huntingdon,Cainbridgesbire PE282ES, U.K.
[email protected]
Andrew Waki-.ham-Dawson
rite International Coininission on Zoological Nonienclatnre, c/o The Natural History Mtisentn, Cromwell Road, London SW7 5BD,
U.K.
[email protected]
Abstract: We describe the behavioin of|tlaying possum, or tbanatosis, in mate rejection by non-
receptive female btitterflies ofthe Satvrinae of the Palearactic. In this behaviour females feign
deathwith closedwingsand releasethemselvesfrom thestibstrateonwhich theyaresettled. This
behaviour only occurs with extreme male ]tersistence and is the final part of a mate-rejection
behaviotiral setpience. Wesuggest that this behaviourmaybe relatively rare, possiblyrestricted to
the tribes Elvmiini and Maniolini. There are potential associationswith female matingfreqtiency,
male mate-locating mechanisms and the physical strttctnre of habitats wbere attempted mating
occurs. Westiggestthatthebehaviotirocctirsinspecieswherefemalesoccasionallymatemorethan
once,wherethe|)redominantmalematingstrategyisaperchitigsit-and-wait tacticandthespecies
occupywoodlandstrnctnres. Instichcirctimstancesmaleshaverelativelyfewopportunitiestomate,
male-femaleencounterrates maybe relativelyinfrequentand thephysicalstrncttireofthe habitat
allowsfemalesthatadojrtposstimmate-rejection toescapefrommalesbvdroppingintovegetation.
W'eencouragefurtherobservationson thisbehaviourtoallowa thorotigh analysisofitsfrequency
amongstspeciesin ordertoallowaphylogeneticanalysis.
Key words: |5redation, mate location, mate rejection, Pararge, La.siommata, Kirinia, Esperarge,
Maniola.
Playing possum (tbanatosis: feigning deatli) in currently known; in doing so we focus attention on
butterflies bas been described for two very differejit possumbehaviourin materejection, theobjectivebe-
circumstances. It was first described as a predator ing to encourage further observations (Table 1).
escape mecbanism in Govepteryx rhamni L. Pieridae In the Lepidoptera possum behaviour is a wide-
(Dennis 1984) and Inachis io L. Nymphalidae (Den- spread secondarydefence mechanism (Scoble 1992)
nis 1998). More recently, it bas also been shown to and in the butterflies it has been recorded in species
have a role in mate refusal byfemales ofParargeAnd ofNymphalinaeandPieridae. Onbeingcaughtbythe
iMsiommata species (Satyrinae) (Sbreeve 1985, Den- wings, thesespeciesundergotbanatosisandeffectively
nis 2003) and bas l)een described for EsperagecUmene play dead. When released they will lie on their side
(Satyrinae) (Wakeliam-Dawson etal. 1999). As faras inertforsome timebeforetakingflight (Dennis 1984,
we are aware it bas not been described in mate rejec- 1998). Specieswhich adopt thisbehaciourtend to be
tion foranyotherliutterflytaxonapartfromSatyrinae long-livedandhaverelativelyrobustwings.Asmanipu-
(nomenclatureasinKtirsbolt&Ra/.owski 1996) Here, lation bybirdscan lead towingdamage, evidencedin
.
wesummarisethebebaMonral,morphological,habitat tearsandscoredbeakmarksacrosswingsofbutterflies
and phylogenetic attributes for these behaviours as caught bybirds (Collenette 1935, Bowers&Wiernasz
1979, Bengston 1981, Dennis et al. 1984), thiswould
Received:3September'2()(H givebutterflies with tougherwingsanadvantageover
Accepted:21)June2005 those with weaker structures. Butterflies described
39: 80-85, 2000 (2006) 81
displayingpossum behaviourin relation topredation fallingfromasrrbstrate. W’hen arefusirrgfemaleplays
typically hibernate as adults and have under-surfaces possitm itwill remain qrtiescetU after the irrale leaves
and wing shapes that characteristically mimic dead before resumingitsactivities (flightorbaskirrg). The
leaves.Theyspendmuch ofthelatersummerfeeding twostagesoforientatiorr and droppingmake possitm
avidly on nectar and in such situations are particu- behaviour unique. It appears to be part offerrrales’
larlyvulnerable to predation. G. rhamniare often so mate-rejection repertoireswhen the total duration of
engrossed in feeding that they can be picked offthe male har'assment is very long (Dermis 2003).
flower heads with ease (Dennis 1984). Experiments Recorded instances (Table 1) of females inlay-
on possumbehaviourindicate thatthebehaviourmay ing possum behavioirr in response to attempted
be triggered more easily in autumn brood adults in- copulation by males is possibly restricted to the tribe
tent on accumulatingresourcesforhibernation than Elymniini and one member of the tribe Maniolini,
in early summer broods actively engaged in mating. Maniola jurtina L. (Satyrirrae, Maniolini). In tbe
Although described thusfarfor G. rhamni'And /. io, it case ofM. furtina, this behavioirr has been recorded
is expected that this behaviourwill extend to closely in 4 instances out of27 attempted courtships in dry
relatedspecieswithsimilarlife histories, morphology Mediterraneanscrub/woodland in Provence, France
and behaviour (e.g., Aglais uriicae). obsei'ved between 27Julyand 1 1 August 1988 byone
Possum behaviour in mate rejection is the hnal ofus (TGS). Asfarasweareaware possum behavioirr
stage of a behavioural sequence, with common ele- linkedtomate-rejection hasnotbeen recorded inany
ments to more normally widespread mate rejection higher taxa. Instances of similar', but not identical,
behaviour. First, when harassed by a male attempt- behaviour are described in Garterocephalus palaemon,
ing to copulate, a settled female may simply rai.se its Hesperiidae (Ravenscroft 1994: 1 185) andfemalesof
abdomen to prevent copulation (e.g.. Finis napi L. otherspecieswill reject malesbyremainingquiescent
Pieridae; Plehejus argus, L. Lycaenidae; Wilcockson during attempted courtships (e.g., Leptidea sinapis
2002,Dennis,pers.obseiwation). Thismayormaynot L. Disrnorphiinae; Wikhrnd 1977). In the case of
involvewingflutteringaswell. Thisbehaviour,which G.palaemon unreceptive females dro]) to the ground
may involve exposure of the genitalia with j)ossible with closed wings when pursrred by a flying male
chemicalsignalling, iscommon tomanybutterflytaxa and the behavioirr of1..sinapis is different from true
(Obara 1982, Obara 1984), but notall. In butterflies possirrn behavioirr in that irnreceptive flying females
thatadoptabdominal raising, there maybea second detectedbyflyingmalessail to thevegetation and rest
stage ofmate-rejection in which a non-receptive fe- quiescentwithclosedwings. Restrictingtheanalysisto
male may attempt to prevent mating by completely the Satyrinae reveals that there are jjotential associa-
closingitswingsiftheinitialabdominal-raisingproves tionswith female matingfrequency, male mate-locat-
unsuccessful. Inbutterfliesthatdonotadoptabdomi- ingmechanismsand thephysical structureofhabitats
nal raising, wing closing is usually the first stage to where attempted mating occirrs. Po.ssirrn behavioirr
prevent mating by a persistent male. The genitalia hasnotbeenrecordedin thosetaxawheremaleaccess
ofa closed wing female are then completely inacces- toalreadymatedfemalesis physicallyobstrrrcted bya
sible to thecourtingmale. Where possum behaviour sphragis (matingplirg) (e.g., Ilipparchia, /leteronympha:
differsfromordinarywingclosingisin thesubsequent Orr 2002). On the other hand, it has been recorded
stages. Inpossum-playingfemalestheharassedfemale in those members of the Elymniini {Fararge aegeria,
may lean over onto the substrate, effectively playing F xiphia Fabriciits, F. xiphiodes Standinger) and in
dead. Should the male persist then the female may Maniola jurtina, (Shr'eeve 1985, Dennis 2003, Ten-
J.
then release its tarsal claws from the substrate on nent, per'sonal communication) wher'e females may
which it is settled and drop to lower vegetation or occasionallymate more than once {Faegeria 4- 10%
even the ground. In mostinstanceswhen this occurs Wickman &Wiklund 1983, Shreeve 1985; F.xiphiab%
in Fararge aegeria L., and in the described behaviorrr and Fxiphioides 8%, Shreeve unpirblished; AT jurlina
oiEsperageclimeneEspev, the malewill lose thefenrale 4%, Maier, 1998) The mating frequency ofEsperage
and fly off (Shreeve 1985, Wakehanr-Dawsotr et al. climene, in which possirrn behaviour occurs, is not
1999). In other instances the male will pursite the known.Withoneexception,femalejrossirmbehavioirr
female to the lower substrate or groirnd and persist in mate-rejection has only been recorded in species
in trying to enforce copulation before eventirallygiv- in which the primary rnecharrisrn of mate-locating
ing rtp and flying off. This persistence may be lorrg by males is perching and where perching occurs in
(max 65 sec. in Fararge aegeria, Shreeve 1985). In no predictable woodland strirctures, with males prima-
instance has srtccessful copulation ofthe appar'ently rily settled on vegetation above the ground. Partial
‘dead’ female been recorded, either before or after possum behaviour (in which females do not release
.
82 /. Res.Lepid.
mating
with 5 -
hostplants
of V Qj XbiO Xbc 5bcibrc XbeXbeXbe XMMXbXc SbCxMbScSbeSbe Xbe HighHighHigh
congruence
03
^
and -w.0b>TZ3.e etr2-o oUboziD sO5J XX 5 j <u -cJ oJo^ XbeSbeXbCXbe5bJD Sbe HighHighHigh
frequencies
<u
V
"be
mating S s s s ? ? ?
'(7) c75
qj be
female
be- be be be be
methods, Cl, C ^C ^ § b - Ch0o-3 ho C’7Qu-j!. ^uC^ n.. O Cj PerchingPerchingPerching
locating
mate
scrub grasslandgrasslandgrassland
associations, pioneer,0]>en
OpenOpen
structural
- - -
habitat
to
relation
p
C I' L.paramegaera
c I,.petropilana
in
O O Ss ^K £ JS3 Cb aH; S>o L.maera
behaviour
cCa J5d u^
cL qj G
possumtaxa Q^£S •V£ U•^"-3 -£ “0; a. JpS U^ri <;aa.
of ii: i-J c/^
butterfly
occurrence GJ
Palearctic
X
I.The
in
Table areas
39:80-85, 2000 (2006) 83
laying
location
by
Hostplantselectivityfemales SbC 5C o o ^?o Jc Jo^ Xbo SbOSbOSbJDXbo£bO
and
location
Egg-laying congruence
mating XboXbo o uo ^X ^ XbO D JO o c O 0
V. .J
Female matingfrequency I bo bo bGe.bGo^Sbo
.. CO «
male
mate-locatingmechanism bCo bCo bCo p bCCuo bGCuo '^c 'bpO bCo bGO bGo bGo bGo bGo.
Primary 3j 3j O r3
o- Cl. O- Cl C- G,
c
OJ
a,
'V o 3 "5 = 3 3 2
£ y = S S 5
structure u ^ O ^ ^
sbe^s jbO::o cS?o cSSo -Z u S- oP os ^ M
C XJ c c
Habitat OoQj-P^O OOh O oOrs o(/-Ut c)o O ^ .^0 ^O CgO o 3. ccc- =<u;
once
than
behaviour more
Possum .£ ^
4-
mating
females
of
Tribe/Species faC c o 32 -Ss ^2= SE -sS s :G CG ^s
S- o ^ b. -2-^ GJ •CSSQ-. O instances
known
=
Subfamily
frequency
o G
mating
Family
C3 female
"g;
Multiple
Super-family
8-1 /. Rn.Lepid.
from thesubstrates theyarcon) occurswithin the La- behaviours may not be developed.
siomniaUigenus, but in all instancesoccurrences have In species in which female possum behaviour
taken placeon baregroundsubstrates (T.G. Shreeve, occurs the primary male mate locating mechanism
jjersonalobservation). Recordedinstancesofpossum is perching. Perching males sit and wait for females
behaviour by females of Maniola jurtina have been and their persistence with individual females may
in woodland structures in southern Europe where be high to try and enforce copulation with relatively
summer aestivation occurs. With the exception of scarce females. Ifmated females flyinto areaswhere
Maniolajurtina,femalesthat ado]Dt jDossnmbehaviour perching males detect them they do so because they
arealso highlyselectiveofthe locationsinwhich they are searching for other resources (e.g. egg-laying
layeggs, even ifplantspeciesonwhich larvaefeedare sites, nectar sources). In the case ofPamrgcspecies,
themselves widespread. females are highly selective of egg-laying sites (e.g.
Whilst information on the details of mate rejec- Shreeve 1985, 1986, Shreeve & Smith 1992) and pos-
tion byfemalesofthe majorityofspeciesisextremely sum behaviour may be the only sure mechanism of
scant, the provisional analysis that we supply here is deterringacourtingmale ifthefemale isin asuitable
it.selfrevealingofapossible phylogeneticcomponent egg-layiug location. Time spent playing po,ssum may
with links to the overall behavioursofboth sexes and be less than time spent searching for alternative re-
the physicalstructureofthe habitats in which species sources elsewhere. In the case ofParargeaegetia, the
occur. The occurrence offemale possum behaviour maximumrecordedtimeplayingpossum (65seconds)
as a male rejection behaviour can be explained by iswithin the range oftimes spent on searching flight
a common set ofcharacteristics; females potentially between egg-laying locations (Shreeve 1985).
matingmore than once,occupation ofspecificwood- Eemalepossumbehaviourmaybeabsentinstrictly
landstructures, theoccurrenceofperchingwithin the patrolling species. We suggest that it has not devel-
male locatingrepertoireandselectivitybyfemalesfor oped in this circumstance because in such species
specific egg-laying locations. y\ common element of females are readily a])]iarent to males bycolouration
female possum behaviour is that it only occurs after (Dennis & Shreeve 1988) or are abundant. Thus it
othermate-rejection postures,such asabdominal rai.s- may be unproductive for males to persistwith an im-
ing, wing fluttering and wing closing, have failed to receptive female since otherswill be readilydetected
deter the male. It is also potentially time consuming orencountered. Similararguments apply to lekking
for both the male and even more so for the female, species (e.g. someTheclinae) themajorityoffemales
;
whichwill tend toremain (|uiescentafterthecourting entering a lek will be receptive.
male has left. Although we have limited data, it is possible that
Iffemales easily and unecjuivocally communicate female possum behaviour may be restricted to spe-
their non-receptivity then it is jiointless for any male cies that use a specific set of woodland structures,
tospend time attempting to court a non-receptive fe- though not universally so. Eor example, it has not
male. In such circumstances it is unlikelythat female been recordedforspecies thatlocate matesprimarily
po.ssum behaviourwill be employed oreven develop. within the woodland canopy (e.g. Argynnis species,
Thus the behaviour isabsent where there is the clear Nymphalidae; Neozephyrusspecies, Lycaenidae) oron
signal of a sphragis in single mating females (e.g., thegroundlayerofwoodland (e.g. Arelhiisenaspecies,
Hi/)j>airhia-, Satyrinae). It is also absentwhere there is Nymphalidae).. One key characteristic ofthose spe-
multiplemating,butunreceptivefemalesareplugged cies that use this form ofpossum behaviouris the re-
with a sphagris and males have limited resources to semblance ofthewingunderside todryleaves,which
make plugs (e.g. Helnonyniplia species) or where ef- arepredictablecomponentsofthegroundlayer.Asex-
fectivechemical signallingassociatedwith abdominal amples,Argv?n?Aand Neozephyrusspeciesmaybehighly
raisingoccurs in potentially multiple matingfemales conspicuous to conspecifics and predators when on
(e.g. /-’/cm spp.; Pieridae, Ohara & Hidaka 1964). It the ground layer and adoption ofpossum behaviour
is also a|)parentlyabsent in species suin which recep- mayincrease predation risk. The absence ofpossum
tivefemaleshavespecihcbehaviourstoadvertisetheir behaviourfrom multiple matingspecies ofgrassland
receptivene.ss to males such as the jumping flights of andmoreopenstructuressuchasrockslopesmayalso
virgin AphantopushyperantusL. (Maniolini)(Wikhmd be related towingandsubstratecolouration,with the
1982). Efficient communication of receptivene.ss is latter tending to be more variable than in woodland.
advantageous to females since they will not spend In such circumstancesanyindividual playingpossum
time harassed by males. When males are given an may renderitselfconspicuous andvulnerable to pre-
unambiguous early cue of non-receptivity then they dation. We suggest that contrast ofunderside wing
are unlikely to harass, so more complex rejection colouration with background is itselfa constraint on
.
39: 80-85, 2000 (2006) 85
the development ofpossum behaviour. changesin thedispersal |tatternof thesatyrinebutterflyLethi’
Whilst the informationon thisbehaviouris rather (liana. Ecological Entomology27: 33-40.
Kvrsholt.O.&J.R\zowski 1996. TheLepidopteraofEurope.Apollo
limited there are indications that it may also have a Books,Svenborg.
phylogenetic component. The adoption of possum M.vier,C. 1998.Thebehaviourandwingmoiphologyofthemeadow
behaviour in mate-rejection appears restricted to brownbutterfly{ManiolajurlinaL.) inBritain,theinfluenceof
one or perhaps two tribes ofthe Satyrini. It mayalso weatherandlocation. PhDThesis,Oxford BrookesUniversity,
Oxford.
be a derived trait associated with their adoption of Obar/V, Y. 1982. Mate refusal hormone in the cabbage white
woodland structures from ancestral open grassland butterfly?Naturwissenschaften 69: 551-552.
structures (Dennis&Shreeve 1988). Evidenceforthe . 1984. Key stimuli eliciting the mate refusal |50sture in
possible restriction ofpossum behaviour to the tribe the mated female ofthe cabbage white butterfly, Pieri.s rapae
crudvora. Proceedingsofthcja|)anAcademy,60: 145-148.
Elymiini within the Satyrinae comes from its appar- Orr,a.G.2002.ThesphragisofIlol('rnnympha Waterhouse
ent absence from the behavioural repertoire ofLethe (Lepidoptera: Satyridae): its structure, function and role in
(liana, which also occupieswoodland structures (Ide s|>ermguarding.JournalofNatural History36: 185-196.
2002) Wherepossumbehaviouroccursinothertaxa RwENSCRorr, N. O. M. 1994. Environmental influences on mate
. locationinmalechequeredskipperbutterflies, Carterocephahis
(e.g. NymphalinaeandPieridae),asindicatedabove, palaemon (Lepidoptera: 1lesperiidae). Animal Behaviour 47:
it is a primary response to predator attack and the 1179-1187.
species which adopt such a behaviour are long lived ScoBiE,M.J. 1992. fhe Lepidoptera:form,functionanddiversity.
andhaverelativelythickerandmorerobustwingsthan Oxford UniversityPress, Oxford.
theSatyrini (Table 1).Wesuggest thatamoredetailed SiiREbEuVtEt,eTr.flGy.P1a9r8a5r.geI'aheegpeori|a)n(lLa.t)ion(Lbeipoildoogpyteorfat:heSSatpyercikdlaeed).WoPohDd
examinationofpossumbehaviourwouldreveal much Thesis (CNAA),Oxford Polytechnic, Oxford.
about the interrelationshipofbehaviourwith habitat . 1986. Egg-layingbytheSpeckledWood butterfly (Pararge
structural predictability and costs and benefits ofin- aegeria):theroleoffemalebehaviour,hostplantabundanceand
dividualbehavioural traits. Inparticular, information SiiREEtVe'mE,peT.raGt.u&reA..GE.cSomlioigiiica1l99E2.ntTohmeolroolgeyof1w1:ea2t2h9e-r2-3r6e.latedhabitat
on the extent ofits occurrence is required for a full use on the impact of the Enrojtean sjteckled wood Pararge
analysisandapropertestofhypothesestoaccountfor aegeria'AndtheendemicParagexiphiao\\theislandofMadeira.
its occurrence. We would welcome observations. WakI'B.iioilaomgi-cDaalwsJoonu,rnaa.l, oTf.BtehentLoinnn&eaVn.BSaocrineitiyam16:195999-.75.Butterflies
and dragonflies in northeiii Greece, 27June - 9July 1997.
Acknowledgements Entomologist’s Record&JournalofVariation 111: 121-128
Wickman, P.O. & G.Wikiunii 1983. Territorial defence and its
The authors thank John Tennent for his observations on seasonal decline in the speckled wood butterfly (Pararge
Parargexiphia in Madeira and two anonymous referees for their aegeria) Animal Behaviour31:1206-1216.
usefulcomments. WiKi.iiNi), C. 1977. Courtship behaviotir in relation to female
monogamy in Leplidea sinapis (Lepidoptera). Oikos 29: 27.5-
283.
Literature cited . 1982. Behaviouralshiftfromcourtshipsoficitationtomate
avoidanceinfemaleritigletbutterflies (Aphantopnshyperantus)
Benoston, S. a. 1981. Does bird predation influence the spot- aftercopulation.Animal Behaviour30: 790-793.
numbervariationinManiolajurtina?Biologicaljournalofthe Wtt.cocKSON, A. 2002. Phe ftinctional significance of wing
LinneanSociety 15: 23-27. morjtholog)'variationinthegreen-veinedwhitebutterfly(Pieri.s
Bowers, M. D. & D.C. Wiernasz 1979. Avian |)redation on the napi(L.)). PhDThesis, Oxford Brookes L’niversity,Oxford.
palatable butterfly, Cercyonis pegala (Satyridae). Ecological
Entomology4: 20.5-209.
CoLENEEiE,C.L. 1935.NotesconcerningattacksbyBritishbirdson
butterflies. Proceedings ofthe Zoological SocietyofLondon
1935:201-217.
Dennis,R.L.H. 1984.Brimstonebutterflies(Gonepleryxrharnni) (L.)
playingpo.ssum. Entomologist’sGazette,35: 6-7.
1998. Thanatosis in Inachis io (L.) Nymphalidae.
Entomologist’sRecord&JournalofVariation 110: 115-116.
. 2003. Playing possum as an alternative to mate-refusal
postureinParargeaegeria(L.),Satyrinae.Entomologist’sRecord
&JournalofVariation 115: 293.
Dennis, R. L. H., K.Porter & W.R.Wiii.iams 1984. Ocellation in
Coenonynmpha tullia (Midler) (Lepidoptera: Satyridae). 1.
Structures in correlation matrices. Nota Lepidopterologica
7: 199-219.
Dennis,R.L.H.&T.G.Siireeve1988.Uostplant-habitatstructureand
theevolutionofbutterflymate-locationbehaviour.Zoological
JournaloftheLinneanSociety94: 301-318.
Ii)E,J.Y.2002.Matingbehaviourandlightconditionscauseseasonal