A review of wing reduction in Lepidoptera

46 Pages·1991·16.9 MB·

by  K Sattler

Bull. Br. Mus.nat. Hist. (Ent.)60(2):243-288 Issued19December1991
A
review of wing reduction in Lepidoptera
K. SATTLER,
DepartmentofEntomology, The Natural History Museum, CromwellRoad, London SW75BD
CONTENTS
Introduction 243
Terminology 245
Phasesofwingreduction 245
Correlationbetweenthereductionofwingsandreductioninotherorgans 246
Teratologicalwingreduction 246
Feedingandflight 247
Courtshipandflight 248
Ovipositionandflight 248
Flightasanescapemechanism 248
Sedentaryhabitandlocomotioninwing-reducedmoths 249
Ovarialdevelopmentandflightlessness 250
Wingreductioninmales 251
Wingreductionincoldseasonmoths 252
Wingreductioninorealmoths 254
Flightinahightemperatureenvironment 255
Wingreductioninforestmoths 256
Wingreductioninsteppeanddesertmoths 256
Wingreductioninaquaticmoths 256
Flightlessnessincavernicoles 256
Flightlessnessinabutterflyinhabitingthecommunalnestofitslarvae 257
FlightinSaturniidae 257
Checklistoffamily-grouptaxainwhichwingreductionoccurs 258
ChecklistoftheMicrolepidopteraspecies,includingPyralidae,withwingreduction . 258
Discussionofwingreductionindifferentfamilies 260
Acknowledgements 282
References 282
Index 285
SYNOPSIS. In Lepidoptera, wing reduction associated with loss of flight has evolved in
manyindependentlineagesin25ofabout 120currentlyrecognizedfamilies;however,less
thanonepercentofallknownspeciesareaffected,reductionusuallybeingconfinedtothe
female sex. The phenomenon of wing reduction is here examined throughout the
Lepidoptera, the literature on the subject is reviewed, implicationsofflightlessness are
discussed and the major hypotheses on the evolution of wing reduction are critically
evaluated. A systematic list of family-group taxa in which wing reduction occurs is
provided together with a list ofall Microlepidoptera, including Pyralidae, known to be
wing-reduced. An overview of the 25 families with wing-reduced taxa is given and a
numberofexamplesare illustrated.
part in the evolution of insects and is a major
INTRODUCTION reason for their success. The advantage of flight
lies in greatly enhanced possibilities for the loca-
tion of food sources for the adults and host-
The acquisition of wings suitable for sustained substrates for their early stages, mate location,
directional flight undoubtedly played a crucial dispersalandescapefrompredators.Thepossible
244 K. SATTLER
role of the wings in maintaining the thermal In the Lepidoptera flightlessness coupled with
balance of an insect by providing a large surface some degree ofwing reduction, usually brachyp-
area for the exchange of heat with the environ- tery, is an exception and affectslessthan one per
mentmustalsobeconsidered. Yetinspiteofsuch cent of the currently known 150,000-200,000
seemingly obvious benefits, a smaller or larger species. Nevertheless, wing-reduced species are
numberofspecieswithin mostmajorinsectorders, recorded in 25 out of the 120 or so currently
for example Hemiptera, Coleoptera, Hymenop- recognised families, representing 11 of the 38
tera, Diptera, NeuropteraandLepidoptera, have superfamilies. In the primitive, non-ditrysian
secondarily lost the ability to fly, sometimes in families wing reduction is unknown except in a
only one sex, whilst the wings have undergone fewHepialidae;itisalsounknownintheditrysian
various degrees ofreduction culminating in their superfamilies Cossoidea, Castniodea, Sesioidea,
complete loss. Immoidea, Alucitoidea, Pterophoroidea, Calli-
TheLepidopteraarecharacterisedbytwopairs duloidea,Hedyloidea,Hesperioidea,Papilionoidea,
of scale-covered wings, but within the order a Mimallonoidea and Sphingoidea.
considerabledegreeofwingshapediversitycanbe Although wing reduction in Lepidoptera is not
observed. The most primitive Lepidoptera have a uniform phenomenon, and each case shouldbe
broadly lanceolate wingswith a short fringe; fore looked at on its own merit, a number of general
andhindwingsareofthesameshapeandsizeand principles are recognizable. It has evolved many
have similar (homoneurous) venation. In higher, timesindependentlyandisapositivestrategy,not
heteroneurous Lepidoptera the number of wing an evolutionary blind alley that leads to early
veins is somewhat reduced and, as the hind wing extinction. There is no apparent phylogenetic
haslostmore veinsthan the fore wing, both pairs predisposition to such reduction; it can evolve in
are dissimilar. In many Microlepidoptera, for any family, provided specific preconditions are
example Nepticulidae, Gracillariidae and Cole- met. Wing reduction is almost exclusive to the
ophoridae, the hind wing is very narrow, but this female sex, but in rare instances has evolved in
reduction is compensated by a greatly extended both sexes. Reduced wings are frequently corre-
fringe. Similarly in Alucitidae and Pterophoridae latedwithreducedmouthpartsand,whereapplic-
both pairs of wings are divided into narrow able,reducedtympanalorgans;infemalesthereis
brancheswhich areconnectedandsurroundedby alsoacorrelation with an extension oftheovaries
longfringes. Ifthe wingsplay a significantpart in into the thorax. In most instances reduction has
heat regulation such modifications oftheir shape occurred either as a consequence of sedentary
may be a means ofreducing the heat-exchanging habit or in response to certain environmental
wing surface without losing the aerodynamic factors. Speciesofthe firstcategory have moreor
benefits of the larger wing area. In numerous less reduced legs whilst those of the second
groupsofLepidopterasomegenuine reductionof category have retained full use of their legs and
one pair ofwings, usually the hind wings, can be are able to run and sometimes jump. Wing
observed,forexampleinthemalesoftheAustralian reduction in response to environmental condi-
genera Tympanota Warren and Sauris Guenee tionsoccursmainlyin speciesthat are endemicto
(Geometridae) (Dugdale, 1980). Amongst the smalloceanicislands,orinhabitthealpinezoneof
moreextremeexamplesarethe Indian himantop- highmountains,orhavetheiradultactivityperiod
terineZygaenidaewithfiliformhindwingsandthe in the cold season.
male ofthe South American Diptilon culexDraudt AccordingtoDierl&Reichholf(1977: 30)wing
(Arctiidae,Ctenuchinae)withhindwingvestigesso reduction mainly occurs within small systematic
small that they are concealed in the metathoracic unitssuchasgeneraorgroupsofgenerainwhichit
haircover. However,assuchspecialisations,even affectsallormostspecies. Examplesinsupportof
when extreme, do not renderthe affected insects thiscontention are Diurnea Haworth and Cheim-
flightless,thisphenomenonisnotpursuedfurther ophila Hiibner (Oecophoridae), Ceuthomadarus
in this paper. By contrast, the presence of fully Mann (Lecithoceridae) and many genera of
developed, seeminglyfunctional wingsis no indi- Geometridae. However, an analysis on a world
cation that they are actually used, and there is basisindicatesthatwing-reducedspeciesaremore
ampleevidencethatsome speciesare moreactive frequently the exception within large genera of
fliersthanothers. Femalesespeciallyarefrequently fully winged species, for example Pharmacis
sluggish and those ofmany species rarely take to Hiibner (Hepialidae); Tinea Linnaeus, Eudarcia
the air before they have mated and deposited at Clemens (Tineidae); Kessleria Nowicki (Ypono-
least partoftheireggcomplement; butflightless- meutidae); EthmiaHiibner, ThyrocopaWalsingham,
ness without wing reduction is also outside the Borkhausenia Hiibner, Pleurota Hiibner (Oeco-
scope ofthis review. phoridae); Elachista Treitschke (Elachistidae);
AREVIEWOFWINGREDUCTIONINLEPIDOPTERA 245
—
SymmocaHiibner(Symmocidac); KiwaiaPhilpott, Stenopterous specieswiththe fore wingstrongly
Ephysteris Meyrick, Caryocolum Gregor & reduced in width but without any significant
Povolny,StomopteryxHeinemann(Gelechiidac); reductioninlength. The hindwingisalsoreduced
Oxypteron Staudinger (Tortricidae); Synaphe and may be vestigial although the frenulum is
Hiibner, Catoptria Hiibner, Orocrambus Purdic usually present. Stenoptery is very rare but is
(Pyralidae); Xanthorhoe Hiibner, Elophos observed, forexample, in the femalesofPleurota
Boisduval (Geometridae); Orgyia Ochsenheimer marginella (Denis & Schiffermiiller) (Oecophori-
(Lymantriidae); Xestia Hiibner, Agrotis Ochsen- dae)(Fig. 10;Spuler, 1910: 341,pi. 88,fig. 69b,as
heimer (Noctuidae) and others. It should there- P. rostrella Hiibner) and Spartopteryx kinder-
fore not be assumed automatically that wing mannaria (Staudinger) (Geometridae) (Fig. 45;
reduction affects all members of a genus if it is Wchrli, 1941: 466, pi. 41b). Stenopterous moths
known to occur in one of them. For example, are incapable offlight.
Died (1983: 141) implies that the females of all —
Micropterous species with both pairs ofwings
species of Estimata Kozhanchikov (Noctuidae)
reducedtosmall unstructuredlobes (Figs32, 60).
are brachypterous, although those of all but one
All tubularveinsare lostandthe upperandlower
species are still unknown. wing membranes are often separated. The hind
Inalmostallcaseswingreductionisrestrictedto
wing vestige has also lost the frenulum, for
the female sex whilst the male retains fully
example, Erannis defoliaria (L.) (Geometridae);
developed wings and the ability to fly. Wing
Chondrostega species (Lasiocampidae).
reduction in both sexes is extremely rare; it is —
recorded in 10 different families and affects only Apterous species without any external rem-
about 25 species, most of them inhabitants of nants ofwings. Aptcry is very rare and, where it
southern ocean islands. Flightlessness with wing occurs, isconfinedtothe females; nospecieswith
reduction affecting solely the male sex is so far apterous males is known. Certain species some-
unknown in Lepidoptcra. times referred to in the literature as 'apterous' or
'wingless' still have external wing vestiges,
Terminology for example some geometrid winter moths. An
example oftrue aptery is the female ofCheimop-
Depending on the state of their wings and the tena pennigera Danilevsky (Danilcvsky, 1969a:
degreeofreduction, Lepidoptcracanbeclassified 182, fig. 10).
as macropterous, brachypterous, stcnopterous,
micropterousorapterous; however,theseare not
Phases ofwing reduction
clear-cut categories and the terminology is often
appliedloosely, in particulartheterm brachyptery, In various Lepidoptcra sexually dimorphic wing
whichmayencompassstenopteryandmicroptcry. shapes can be observed. Such dimorphism may
The classification is restricted to the wing itself reflect the different flight requirements of the
and disregards the associated flight musculature sexes resulting, for example, from their different
and the actual ability to fly. See also Hackman bodyweight;however,evenifsmall,itmaybethe
(1966: 2). first indication ofa trend towards wing reduction
— in the female.
Macropterous species with fully developed
The reduction of the wings follows a distinct
wings (e.g. Figs 1, 3, 5, 9). Macropterousspecies evolutionary(butnotphylogenctic)sequenceand
are usually but not always capable of flight. For
example the macropterous female of Lymantria examples of all intermediate stages between
macroptery and aptery are found. Initially the
dispar(L.)(Lym—antriidae)ismoreorlessflightless. distal halfofthe forewingbecomesnarrower; ifa
Brachypterous speciesshowingvariousdegrees distincttornuswaspresentthisisreduceduntilthe
of wing reduction (e.g. Figs 2, 4, 6-8, 12). In a wing margin (dorsum and termen) is an even
living brachypterous moth the wings are usually curve from base to apex and the formerly tri-
exceeded to a greater or lesser extent by the angular wing has become broadly lanceolate.
abdomen. The wing shape is broadly lanceolate Simultaneously the hind wing changes shape and
and one or more veins are lost, although some in broad-winged forms also becomes lanceolate.
tubular veins are retained, at least in the fore The slightsexualwingdimorphism in Chionodes
wing. Thehindwingmaybefurtherreducedthan pergrandella (Rebel) (Gelechiidae) (Burmann,
the fore wing and may have lost all tubular veins 1977: figsB2 6,B3 9, asC. decolorella) fromthe
(forexample in Sattleria 9), but often retainsthe European Alps and Central Asia is seen as an
frenulum. Brachypterous moths are incapable of example of an early stage in the development of
sustained flight. female brachyptery (Sattler, 1986: 258-259). In
246 K.SATTLER
the malethecostal anddorsal marginsofthefore example the stenopterous female of Pleurota
wingdivergetowardsthe termen, andthe wingis marginella (Denis & Schiffermuller) and brachy-
distinctly wider at two-thirds than at one-third pterousfemalesofSattleriaspp. retainstillmostof
whereas in the female both margins run almost theiroriginalvenationin theforewingswhilstthe
parallel andthewingisnotwiderat2/3. The hind vestigial hind wings have lost all tubularveins.
wing termen of the female is more oblique than
that ofthe male and the apex is more pointed. Correlation between the reduction ofwings
In Thyrocopa apatela (Walsingham) (Oeco-
and reduction in other organs
phoridae, Xyloryctinae) (Figs 7, 8; Zimmerman,
1978: figs 645, 650, $) from Hawaii wing reduc- The correlation between wing reduction and
tionisfurtheradvanced. Bothwingshavebecome reduction ofthe mouthpartswasinvestigatedand
lanceolate and the venation in the distal half is discussedindetailbyNaumann(1937). Atendency
much condensed. In the forewing R4and R5 are towards reduction of the mouthparts is wide-
M
almost coincident and one vein is lost; in the spread in the Lepidoptera, and examples of a
hind wing M3 and CuAl, which are usually reduced proboscis are found in most families,
connate in Thyrocopa Meyrick, have migrated althoughthere arefeweringroupsofstrongfliers
ontoacommonstalk. Thehindwingissignificantly such as the Sphingidae and Noctuidae and, as to
smaller than the fore wing, whereas in other be expected, very few in the butterflies, for
members of this genus they are of about equal example some African Lycaenidae of the sub-
size. family Lipteninae (Eliot, 1973: 394). In fully
Furthersimplificationofthevenation isfollowed winged species the mouthparts are mostly de-
by withdrawal of the veins from the wing margin veloped equally in both sexes whereas in those
(accompanied by loss of the marginal sensilla with wing reduction in the female the male has a
campaniformia) and gradual loss of the tubular longer proboscis. Nevertheless, in such species
structureofthe remainingveins(Baus, 1936: 45). themaleproboscis(inrelationtothebodylength)
For example, in the fore wing of Areniscythris is shorter than in related fully winged species,
brachypteris Powell (Scythrididae) from California which indicates that mouthpart reduction affects
only part of Sc, the R stem with traces of R5 and both sexes, even though it is distinctly more
sometimesR4,andthepartlyobsoleteM3and2A advancedinthe female. Differencesin the length
are present whilst the hind wing venation is oftheproboscisbetweenmacropterousmalesand
reduced to just traces of Rs and 2A (Powell, wing-reduced females raise the question whether
19766: figs 2, 3, 9). in some instances the former maystill feedwhilst
Withthelossofthetubularveinsthe upperand the latter no longer do so.
lower membranes of the wing vestiges become Aclosecorrelationbetweenwingreductionand
separatedandthesensillacampaniformiaare lost the reduction ofthe tympanal organs in Geome-
exceptforsome ofthose on the wing base (Baus, tridae, Lymantriidae, Arctiidae and Noctuidae
1936: 45). This stage is reached in the vestigial wasobservedanddiscussedindetailbyHeitmann
wings of Erannis defoliaria (L.) (Geometridae) (1934) and Gohrbandt (1938) (see also p. 250).
female. Completelossofthewingsisknowninthe
females of certain Psychidae (Dierl, 1973) and
Heterogynidae (Daniel & Dierl, 1966, figs 2, 3) Teratological wing reduction
but is also recorded, forexample in Cheimoptena In most macropterous Lepidoptera individuals
pennigera Danilevsky (Geometridae) (Danilevsky, withimperfectlydevelopedwingsareoccasionally
1969a: 183, fig. 10), Orgyia ericae (Germar) and observed. Failure to expand the wings properly,
O. dubia (Tauscher) (Lymantriidae) (Heitmann, followingemergencefromthepupa,isusuallythe
1934: 180). No cases of aptery in male Lepidop- resultofmechanicaldamageorotherunfavourable
tera are known. influences,suchaslackofmoistureduringthepupal
The frenulum is lost at a very late stage in the or perhaps larval stage. According to some ob-
reduction process. It is still present on the rudi- servers the females are more susceptible to such
mentaryhindwingsofPleurotamarginella(Denis damage than the males. Crippled individuals fre-
& Schiffermuller) (= rostrella Hiibner) (Oeco- quently resultfrompupaethatwerekepttoodry,
phoridae) and Sattleria Povolny (Gelechiidae), and even the condition of the host-plant during
which have lost all tubular veins, but is absent the larval stage may be significant. For example,
from the hind wing vestiges of Erannis defoliaria Loritz (1952) considered casual brachyptery in
(L.) and others. females of Thaumetopoea pityocampa (Denis &
Thereductionofthehindwinganditsvenation Schiffermuller) (Thaumetopoeidae) reared in cap-
progresses faster than that of the fore wing. For tivity to be the result ofdesiccated larval food.
AREVIEWOFWINGREDUCTIONINLEPIDOPTERA 247
Apart from the failure to expand an otherwise and other usually liquid substances, and flight
normally developed wing completely, the loss of plays so important a part in the search for such
one or more wings, usually a hind wing, is also non-ubiquitous food sources that non-feeding
known and is commonest in the Geometridae. must be considered one of the preconditions for
During a mass occurrence of Eulype hastata (L.) the evolution offlightlessness. It is therefore not
(Geometridae) in Finland in 1947 Hackman (1966: surprising to find that certain species with wing
2) observed that for an unknown reason about reductionwerepre-adaptedinthatrespect,because
25% ofall specimens lacked one or both oftheir theyare membersofgenerallynon-feedingfamilies
hindwings. Burmann linkedasimilarobservation inwhichmouthpartreductionisafamilycharacte-
on Semiothisa clathrata (L.) (Geometridae) in ristic, for example Hepialidae, Psychidae, Lasio-
Austria to the influence ofan unidentified herbi- campidae and Lymantriidae. However, other
cide on the host-plantsofthe larvae. Manyofthe wing-reduced species, although themselves having
clathrata examined in a locality near Innsbruck reduced mouthparts, are more or less closely
lacked one or rarely both of their hind wings related to taxa which have fully developed appa-
(Burmann, 1973: figs 1-5); two individuals of rently functional mouthparts. For example, in
Perizoma blandiata (Denis & Schiffermullcr) Apocheima Hiibner and Lycia Hiibner, both
(Geometridae) with the same defect were also genera with wing-reduced females, the mouth-
observed. Amongst the defective individuals parts are reduced, whereas in the closely related
both sexes were represented in about equal but fully macropterous genus Biston Leach
numbers and the affected wings were lost com- (Geometridae) they are well developed.
pletely, without any trace ofexternal rudiments. Similarly, in Ethmia charybdis Powell (Oeco-
The Fl generation reared from one normal phoridae,Ethmiinae),aspecieswithbrachypterous
and two defective clathrata females had normal females, the mouthparts are reduced (Powell,
wings. 1971: 31) whereas in other species of Ethmia
Knatz (1891) assumed accidental deformation Hiibnerthey arewell developed. Forexample, in
of the wings, resulting from unfavourable in- E. aurifluella (Hiibner) and E. lineatonotella
fluences during the larval or pupal period, to be (Moore), both sexes fully winged, the distal
the primary cause ofwing reduction. Males thus portion of the proboscis bears characteristic sen-
affected would simply perish without a chance of silla styloconica (Sattler, 1967: pis 12, 13), which
finding a mate, whereas females rendered flight- are chcmoreccptors, possibly sensitive to sucrose
less wouldstill be fertilized. Continuedover long (Stiidleret«/., 1974: 63). Their presence suggests
periods this effect would be increased and finally that such species may feed; however, within
lead to wing reduction in the female. As a result Ethmia various degress of reduction of the pro-
thethoraxwouldbecomesmallerandtheabdomen boscis and the labial and maxillary palpi are
larger with the ovaries increasing in size. The known (Sattler, 1967: 10, pi. 11) and indicatethat
mouthpartsofthe malesofsuch specieswould be theremaybe ageneralshiftawayfrom feeding. It
reduced because the male would have to spend ispossible that even asomewhat reduced probos-
moretime in search ofthe non-motile female and cis is still used to take in water, which is readily
consequently would have less time for feeding. availableasrainorcondensation inmosthabitats,
Moreover, its chancesofmeeting the (non-motile) to counteract desiccation. Non-feeding may have
female at the food source would be diminished. been an important pre-adaptation in certain moths
However, it is unlikely that accidental wing de- thatfacilitatedashiftoftheiradultactivityperiod
formation has played a significant role, if any at to the cold season with its absence offlowers and
all, in the evolution of flightlessness and wing paucity ofotherenergy sources.
reduction because no selective advantage to the According to Twcedie (1976) abstention from
female can be demonstrated. feeding as an adult is the main cause of wing
reduction in the female. A non-feeding female
Feeding and flight will have a heavy abdomen as a consequence of
havingtostoreenough nutrientin the larval stage
For reasonsoflongevity, slowprogressive matur- foritsfulleggcomplement. Thiscausesreduction
ingoftheovaafteremergenceofthe femalefrom of flight activity and eventually results in reduc-
the pupa, energy-intensive courtship, search and tionofunusedflightorgans. However,whilstnon-
dispersal flights, migration etc., many adult feeding is a precondition to flightlessness, it is
Lepidoptera must feed to supplement the energy unlikely to be the main factor in its evolution,
that was stored at the larval stage. They take becausetherearesuccessfulstrategiesavailableto
energyintheformofpollen,nectar,decayingfruit maintainthe abilitytoflywhen thebodyweightis
and other plant material, sap from injured trees increased.
,
248 K.SATTLER
Courtship and flight sufficiently permanent and continuous to allow
The importance offlight in the courtship process non-selective oviposition. Such acondition ismet
in species with larvae that are omnivorous (Prin-
oftheLepidopteraandthecrucialroleofthemale
gleophaga Enderlein, Tineidae), scavengers
in matelocatingmustbeseen asthemajorreason
(various Tineidae, Psychidae, Oecophoridae,
why flightlessness and wing reduction are usually
Lecithoceridae, Symmocidae), polyphagous (most
restricted to the female and are only found
cold season Oecophoridae and Geometridae;
exceptionally in the male (see p. 251). In most
Lymantriidae) orhost-specificbutinhabitingsingle
Lepidoptera the male alone is responsible for species plant communities or sites in which their
findingamate. It isusuallyguidedtoitstarget by host-plant dominates.
pheromones emitted by a stationary female, and Anumberofspecieswithbrachypterousfemales
tacking against the wind, often flyingclose to the
or with wing reduction in both sexes inhabit
ground, is the most effective meansofscanning a grassland, which constitutes a permanent, con-
large areaforapheromone plume. Even inthose
tinuous habitat. Their larvae feed on roots or
groupsinwhichthefemaleisattractedtothemale
green tissue, often apparentlywithout specializa-
at some stage in the courtship process, flight
tion on a particular grass species. Grassland
remainsessentialforthelattertofulfilitsrole,for inhabitants are Pharmacis spp. (Hepialidae),
example by congregating with other males on
Embryonopsis halticella Eaton (Yponomeutidae),
flowers, where the sexesmeet (Micropterigidae), &
Pleurota marginella (Denis Schiffermuller)
performingcourtship dances (Hepialidae), form-
(Oecophoridae), Elachista spp. (Elachistidae),
ingcourtshipswarms(Adelidae)orsettingupand Megacraspedusspp. andprobablyEphysterisspp.
defending territories (butterflies) to which the
(Gelechiidae), Catoptria spp. and Exsilirarcha
females are attracted. Intrasexual competition in graminea Salmon & Bradley (Pyralidae, Cram-
that process acts as a powerful effective barrier binae,Scopariinae)andothers. Afewcoldseason
againstflightlessnessinthemale,whereasinmost species are apparently monophagous on certain
Lepidoptera no such constraints act upon the
trees,e.g. Exapateduratella(Heyden)(Tortricidae)
female. Similarly, a mate locating system that
on Larixandthe Geometridae Erannisankeraria
requires active participation of the female is an (Staudinger) on Quercus and Alsophila quadri-
obstacle to the evolution of flightlessness in that
punctaria (Esper) on Acer, and it is likely that a
sex.
single tree of adequate size can act as an island
large enough to sustain a viable population over
many years.
Oviposition and flight
Most Lepidoptera live in a non-homogeneous Flight as an escape mechanism
environment where flight is essential or at least
highly advantageous to the female in locating a Many Lepidoptera react to disturbance of their
suitable oviposition site. The larvae of many immediatevicinity,forexamplevibrationscaused
species,inparticularthoseofmostMicrolepidop- by an approaching person or animal, by flying
tera, are highly host-specific. They often feed on away.Thequestionhastobeaskedwhetherflight
annual plants and other non-permanent, discon- isessentialinavoidingdangerorwhetheraspecies
tinuous food sources, and their respective host- could adequately protect itself by other means
plants are not always available in the immediate were it to lose the ability to fly. The greatest
vicinityofafreshlyemergedfemale.Forexample danger to adult Lepidoptera is predation, pri-
annual plants die offduringthe winter, and fresh marily by vertebrates (insectivorous birds,
plants may have appeared elsewhere when the mammals and reptiles), but whilst flying un-
female emerges from an overwintered pupa. doubtedlyprovidesanimportantescapemechanism,
Some larvae also undergo a change of diet, as a there are also numerous other successful strate-
consequenceofwhich pupation maytakeplaceat gies. These include living under conditions of
some distance from their initial host-plant. For naturally reduced predator pressure as they pre-
example, the first instar larvae of Adelidae mine vail, forexample, on lowdiversityoceanicislands
the leaves of certain living plants whilst later (Gressitt, 1970: 316),possiblyonhighmountains,
instars are scavengers amongst leaf litter on the or during the cold season of the northern hemi-
ground. Inallsuchinstancesthefemalehastofind sphere (Died & Reichholf, 1977: 33). When at
the host-plant ofthe first instar larva for oviposi- rest individuals can hide in inaccessible places
tion, and the selective advantage offlight in this such as scree, dense vegetation, under bark etc.,
process is so great that flightlessness would only or rely on cryptic coloration. Many species are
have a chance to evolve in a habitat that is protected by unpalatable or poisonous hairs or
AREVIEWOFWINGREDUCTIONINLEPIDOPTERA 249
substances and advertise this fact by aposematic all the offspring of one female so that some
coloration. The loss of flight still leaves other motility is advantageous.
forms of motility such as running, jumping or Several observers have specifically commented
simply dropping to the ground, often followed ontheremarkableabilityofcertainbrachypterous
by feigning death. All these strategies, indivi- mothsformakingshortjumps,coveringdistances
dually or in combination, are widely and success- of about 5 cm or more; however, jumping is
fully employed in Lepidoptera and indicate that sometimes also observed in species that normally
the need to avoid predators would be no insur- fly. Petry (1904: 6) described the movements of
mountable obstacle to fiightlessness. There is the males of Acompsia dimorpha Petry (Gele-
even evidence that the wing-reduced sex some- chiidae), which approached a freshly emerged
times may be better protected from predators female in early morning, as more hopping than
than the fully winged one. For example, in flying ('mehr hiipfend als fliegend'). Jumping as
theAlps, Pinker(1953: 179)andBurmann (1956) an escape mechanism was observed in Scythris
observed very heavy bird predation on the mac- inspersella (Hiibner) (Scythrididae), a fully winged
ropterous males of Lycia alpina (Sulzcr) species that normally flies; the adults visit various
(Geometridae) whilst the equally common brachy- flowersfromwhichtheyjumptothegroundrather
pterous females were apparently ignored by the than fly away when disturbed (Sattler, 1981: 16).
predators. Asa regular behaviourjumpingisknown in both
sexes of the fully winged but nevertheless flight-
Sedentary habit and locomotion in wing- less Gelechiidac Gnorimoschema bodillum
Karsholt & Nielsen from Denmark (Karsholt &
reduced moths
Nielsen, 1974: 96) andScrobipalpulasp. from the
Without the need to fly for purposes of feeding, Falkland Islands (Kirke, pcrs. comm.); excep-
mating or ovipositing the females of certain tionally it also occurs in the male of Sattleria
species, for example Psychidae, Heterogynidae, melaleucella (Constant) (pers. obs.), which is
LymantriidaeandArtiidae,havebecomemoreor capable of normal flight. Jumping as a regular
lesssedentary, in extreme caseseven followed by meansoflocomotionorinresponsetodisturbance
a partial reduction of their legs. The sedentary hasbeenrecordedinthebrachypterousfemalesof
females remain near, on or inside the pupal Kessleria zimmermanni Nowicki (Yponomcutidae);
cocoon; those of certain Psychidae do not even Thyrocopa apatela (Walsingham) (both sexes),
emergefromthepupa,forexample Thyridopteryx Atomotricha ommatias Mcyrick, Pleurota mar-
ephemeraeformis(Haworth)(Davis, 1964: 11,figs ginella(Denis& Schiffermuller) (Oecophoridae);
144, 145) or Megalophanes viciella (Denis & Elachista galatheae (Viette) (Elachistidae) (both
Schiffermuller) andothers (Died, 1973: 3). Mating sexes); Kiwaia jeanae Philpott (both sexes),
takesplaceinsituandtheeggsaredepositedinone Caryocolum laceratella (Zeller), Sattleria species
batchon the pupal cocoon (Orgyia Ochsenheimcr, (Gclcchiidae); Areniscythris brachypteris Powell
Lymantriidae), in the larval/pupal case (many (Scythrididae) (both sexes); Sorensenata agilitata
Psychidae)orinthepupalexuviae(somePsychidae; Salmon & Bradley (probably both sexes, female
Heterogynidae). By contrast, the brachypterous unknown), Sphaleroptera alpicolana (Frolich)
femalesofmostotherspecieshave retainedsome (Tortricidae); Campbellana attenuata Salmon &
degree of motility and normally are capable of Bradley(Carposinidae)(bothsexes)andExsilirarcha
running and climbing. The larvae of many cold graminea Salmon & Bradley (Pyralidae) (both
season moths, such as Diurnea Haworth (Oeco- sexes). The presence ofthis habit in atleast eight
phoridae), Exapate congelatella (Clerck) (Tortri- different families, representing the superfamilies
cidae) and many Geometridae, are polyphagous Yponomeutoidea, Gelechioidea, Tortricoidea,
on deciduous trees and pupate on the ground. Copromorphoidea and Pyraloidea, is an indica-
After emerging from the pupae such females are tion that it may have evolved many times in-
able to find and ascend a tree, where mating and dependently from the moths' normal take-off
ovipositingtakeplace. In sparselyvegetatedalpine mechanism for flying.
habitats with limited stands of the host-plant, Although widespread in wing-reduced Lepi-
flightless females of the motile type are able to doptera, jumping appears to be restricted to
move between plantsanddisperse theireggcom- species that live on the ground in places with
plement. For example, in the almost barren exposed soil and sparse vegetation, for example
habitat ofSattleria melaleucella (Constant) in the Thyrocopaapatela(Walsingham), Sattleriaspecies,
LechtalerAlpenthemainhost-plantinthatlocality, AreniscythrisbrachypterisPowell,orindensegrass,
Saxifraga biflora subsp. macropetala grows in forexampleElachistagalatheae(Viette), Pleurota
,
clusterswhichareoftentoosmalltoaccommodate marginella(Denis& Schiffermuller), Exsilirarcha
250 K.SATTLER
graminea Salmon & Bradley, sometimes Sattleria maturity the eggs have reached when the adult
species.Thishabitisnotdevelopedinmotiletree- emerges from the pupa. Those species in which
living moths such as Diurnea species and the theymaturegraduallyafterthefemalehasleftthe
various geometrid winter moths {Alsophila pupa must be relativelylong-livedanddependon
Hiibner, Operophtera Hiibner, Erannis Hiibner feeding to sustain themselves and obtain extra
andothers), norinthe Psychidae andthefemales energy for the development of the eggs. The
of heavy-bodied moths (Lasiocampidae, Lyman- importanceofflightinthesearchforfoodsources
triidae, Arctiidae), many ofwhich are sedentary. makes it unlikely that flightlessness evolves in
AccordingtoHarper(1990:44)thebrachypterous such moths or, for the same reason, in many
femaleofDiurneafagella(Denis&Schiffermiiller), butterflies. Bycontrast,femalesthatemergefrom
when disturbedwhile at reston atree trunk, drops the pupa with afully mature eggcomplement are
slowly, its fall apparently controlled by the out- abletomate andovipositimmediately, beforethe
stretched wings. Although the descent is not firstflight,ifotherconditionspermit. Forexample,
vertical but proceeds at an angle it cannot be ifthe male is attractedtothe female andthe larvae
described as true gliding. Little is known about are generalist rather than specialist feeders, ovi-
locomotion in the wing-reduced Noctuidae on position can take place more or less on the spot
southern ocean islands, but it would not be withoutthefemalehavingtosearchforamateora
surprising if at least the micropterous Dimorphi- specific host-plant and therefore without gaining
noctuacunhaensisViettewerecapableofjumping. any significant advantage from the ability to fly.
Whilst in the wing-reduced females of certain Such speciescan affordto beshort-lived and thus
Psychidae, Heterogynidae, Lasiocampidae, need not feed. A short adult life span would also
Lymantriidae and Arctiidae the legs are more or reduce the exposure of the egg-laden female to
less strongly reduced as a consequence of their predators.
sedentary habit, there is little evidence that in An increase in the number of fully developed
wing-reduced but motile species the legs are eggsisaccompaniedbyanincreaseinovarialsize,
betteradaptedtorunningorjumpingthanintheir and the growing ovaries gradually displace the
fully winged close relatives that fly. Accordingto tracheal air sacs and tympanal organs, where
Powell (19766: 328) Areniscythris brachypteris present,resultinginaheavierabdomen.Themain
Powell (brachypterous in both sexes) possesses function ofthe tympanal organs being the detec-
longer tarsi and a 1.5 times thicker hind femur tion of ultrasonic cries of insectivorous bats
than several other Scythrididae of comparable (Spangler, 1988), the loss ofthat organ isoflittle
size; however, those differences are relatively consequence to non-flying moths, whilst con-
slight. Moreover, the systematic position ofAre- verselyitisadvantageoustoamoththathaslostits
niscythrisPowellisstill somewhatunclearanditis hearingabilitytoavoidflyingandthusnotexpose
therefore uncertain whetherthe examined Scythris itselftosuchpredators. With afurtherincreasein
species are systematically close enough for a sizethe ovariesofvariousspeciesextend more or
meaningful comparison. The legs of Thyrocopa lessdeeplyintothe thorax,forexamplein Orgyia
apatela (Walsingham) (brachypterous in both Ochsenheimer (Lymantriidae) (Heitmann, 1934:
sexes) do not differnoticeablyfrom those offully 174-180) and Ocnogyna Lederer (Arctiidae)
winged Thyrocopa species and there are no (Heitmann, 1934: 180-183), until they finally fill
appreciable differences in leg structure between the entire cavity of the thorax, for example in
the macropterousflyingmalesandbrachypterous Heterogynis penella (Hiibner) (Heterogynidae)
running andjumping females ofSattleria species. (Dierl, 1966: 459) and Erannis defoliaria (L.)
Nocomparative studies ofthe leg musculature in (Geometridae) (Heitmann, 1934: 165). Some re-
jumping and non-jumping moths are available, duction of the flight musculature was observed in
butifweconsiderjumpingasmerelyabehavioural the brachypterous females of Agrotis fatidica
remnant of the normal take-off for flight, the (Hiibner)and Ulochlaenahirta(Hiibner)(Noctuidae)
absence of special adaptions for that means of (Gohrbandt, 1938: 18) and can be expected
locomotion would not be surprising. whenevertheovariesextendasignificantdistance
into the thorax. It is thus likelythat the abilityto
Ovarial development and flightlessness flyisadverselyaffected notonlybytheincreasing
body weight, which may lead to decreasingly
Inbroadagreementwithseveralpreviousauthors favourable wing loading (i.e. wing: body ratio)
(Naumann, 1937; Eggers, 1939; Downes, 1964; andconsequentlylesssustainedflight, butalsoby
Hackman, 1966) the crucial initial factor in the direct interference ofthe expanding ovaries with
process that leads to flightlessness and wing theflightmusculature.Withdecreasingreadinessto
reduction in the females is seen in the degree of fly,thetrendtowardsearlymatingandoviposition
.
AREVIEWOFWINGREDUCTIONINLEPIDOPTERA 251
becomes stronger and the females of various towards stenoptery, for example Exsilirarcha
species deposit most of their egg complement graminea Salmon & Bradley (Pyralidae) (Fig. 40;
before the first flight takesplace, forexample the Salmon & Bradley, 1956: figs 24, 27), and it is
genus Setina Schrank (Arctiidae) (Burmann, 1957, likely that stenopterous wings are more effective
as Endrosa Hiibner). Continuation of this trend stabilizers to a jumping moth than are broader
leads eventually to flightlessness and sedentary wings. The resistanceofthe male toflightlessness
behaviourwith progressivereductionofthewings issogreatthateveninwindsweptalpineandarctic
andlegsasobservedinfamiliessuchasPsychidae, habitats no brachyptery has evolved in that sex.
Heterogynidae and Lymantriidae and Arctiidae Significantly, wing reduction in both sexes of a
where the females no longer leave the pupation speciesrestrictedtohighmountainhabitatsabove
site. the tree line (oreal species) is known only in the
two oceanic island species Thyrocopa apatela
(Walsingham) (Oecophoridae, Xyloryctinae)
Wing reduction in males
(HawaiianIslands,Maui)(Figs7,8;Zimmerman,
As a result of the division of functions between 1978:937,fig.560)andEphysterissp. (Gelechiidae)
male and female the sexes have different flight (Madeira)(Sattler, 1988:232). Itisnoteworthythat
requirements and consequently are subjected to Ephysteris curtipennis (Zcrny) (Morocco, High
different selective pressures with regard to their Atlas), which is closely related to the Madeiran
flight organs and their ability to fly. This is species and occurs under similar environmental
immediately obvious from the fact that wing conditions,hasmacropterousmales(Zerny, 1936:
reductionrarelyoccursinthemale. Ananalysisof 138). However, the reasons for that difference
those species that are wing-reduced in both sexes maybeconnectedwiththesmallerpopulationand
showsthattheyareall inhabitantsofmostlysmall limited size of the habitat on the oceanic island,
oceanic islands or restricted coastal habitats. The because a flying male that is removed from its
effect of continuous strong winds has long been habitat by the force ofstrong winds is unlikely to
invoked to explain the high incidence of wing find an alternative population as it might in the
reduction in island insects and provides also the much larger continental habitat.
most plausible explanation for brachyptery in Although Salmon (1956: 62) and Viette (1959:
Lepidoptcra males. The most important activity 22) accept the strong winds as the prime cause of
of the male involving flight is the search for a flightlessnessinsub-AntarcticislandLepidoptera,
mate; however, continuous high wind speeds, as they additionally assume a genetic predisposition
theyprevailforexampleonthesmall sub-Antarctic to brachyptery. Ifthis were so, one would expect
islands,makedirectionalflightimpossible. Indivi- to find some tendency towards wing reduction
duals attempting to fly will be carried out oftheir elsewhere amongst the nearest relatives of such
habitat without much chance of regaining it species,particularlywheretheseoccurinenviron-
(Grcssitt, 1970: 364). Moreover, very strong ments that normally favour brachyptery. One
winds must rapidly disperse the phcromones example in support of this view is the genus
emitted by a female to such an extent that no Asaphodes Meyrick (Gcomctridae) with two
pheromone trail would develop for the male to brachyptcroussub-Antarcticislandspecies,origi-
follow. Undersuch circumstancesthere would be nating from New Zealand stock, and several
noattractionoverlongdistanceswhilstovershort 'mainland'species,someofthemwithbrachyptery.
distances, for example in the shelter of grass However,otherspeciesonsub-Antarcticandother
tussocks and other dense, low-growing vegeta- oceanicislandsarcclearlytheonlybrachypterous
tion, alternative means of locomotion, such as membersoflarge, widespreadgenera ofmacrop-
jumping or running, are more effective. In an terousspecieswithout the tendencytowardswing
environment where high wind speeds arc the reduction elsewhere in the world (for example
norm a shift from flying to jumping and a reduc- Elachista Treitschke, Borkhausenia Hiibner, Udea
tionofthewingareaexposedtothewindbecomes Gucnee, Peridroma Hiibner). Considering all
advantageousbecause they increase the abilityof types of wing reduction in the Lepidoptera, and
the moth to stay in control ofits movements. At the manydifferent lineagesin which brachypterous
the same time the reduced wings probably fulfil formshavearisenindependently,itappearslikely
also an important function as stabilizers during a that many species would in time respond in that
jump, and the greater need ofthe male forspeed way to appropriate environmental pressures.
and manoeuvrability in the competitivecourtship Thelowtemperatureonsub-Antarcticislandsis
processmaybethereasonwhythemalewingsare sometimes also invoked toexplain the reluctance
occasionallylessreducedthanthoseofthefemale ofinsectstoflyinsuchhabitats. However,thecold
Bothmaleandfemalesometimesshowatendency cannot account for male flightlessness in the
252 K. SATTLER
Lepidoptera, because there areseveral successful intakeofenergy;theyhavefullydevelopedmouth
strategies that enable, for example, northern parts and feed. Many overwintering moths are
hemisphere winter-active Geometridae and Noc- capable of flying at low ambient temperatures.
tuidaetoflyinmuchlowerambienttemperatures, The importance of flight in the search for food
evenbelowfreezing. Moreover,severalLepidoptera sources, hiding places and oviposition sites acts
with male brachyptery occurin high temperature against flightlessness in such species, and no
environments,forexampleAmblomabrachyptera example of wing reduction in Lepidoptera over-
Walsingham (Symmocidae) and Areniscythris wintering as adults is known. Other species are
brachypterisPowell (Scythrididae)incoastalsand active in autumn and into the colder part of the
dunesonthe Canary Islands and in Californiare- year (forexample Agrochola Hiibner) or emerge
spectively,whereotherfactorsmustberesponsible. very early in the year but extend their activity
period into the warmer months (for example
Wing reduction in cold season moths Orthosia Ochsenheimer). In common with the
overwintering moths these species feed, for
The largest category with environmentally in- example early Noctuidae of the genus Orthosia
duced wing reduction in the female sex is that of Ochsenheimer at Salix catkins, and show no
the northern hemisphere cold season species tendency towards flightlessness.
('wintermoths')which areunivoltine andhavean The group in which wing reduction in females
adultactivityperiodsomewherebetweenaboutlate has evolved comprises those species that emerge
OctoberandApril. Examplesofthiscategoryare in late autumn, frequently after the first frost,
known in the Eriocottidae, Tineidae, Oecophoridae winterorearlyspringandcompletetheiradultlife
(Ethmiinae, Chimabachinae), Tortricidae, in the cold season. Both sexesofsuch speciesare
SomabrachyidaeandpossiblyLasiocampidaeand short-lived;theydonotfeedandtheirmouthparts
Arctiidae; they are particularly numerous in the are usually reduced. The males are capable of
Geometridae (Oenochrominae, Larentiinae, flying in very low air temperatures, often below
Ennominae). The severe conditions ofcontinental 0°C. The females of certain species are fully
winters usually act as a strict barrier that sharply winged, albeitwithamoreorlessstrongtendency
dividesthe cold season moths into a 'late' (moths towards flightlessness, for example Semioscopis
emerging October-December) and an 'early' oculella (Thunberg), 5. avellanella (Hiibner)
(mothsemergingJanuary-April)group;however, (Oecophoridae);Poecilocampapopuli(L.), Erio-
in the mild oceanic winter climate of the British gaster lanestris (L.) (Lasiocampidae); Lemonia
Islesbothgroupsmayoverlapandblendintoeach vallantini (Oberthiir) (Lemoniidae); however,
other. Even underextreme low temperatures the those of most species show various degrees of
breakisnotalwaysabsoluteasisdemonstratedby wing reduction, from brachypterous half-sized
Cheimoptenapennigera Danilevsky (Geometridae), wings in Protalcis Sato to microptery orapteryin
an inhabitant ofthe Central Asiatic deserts, with Erannis Hiibner (Geometridae) (for example
anadultactivityperiodthatextendsfromDecember Inoue, 1982: pi. 98). Theyaremotilewith normal
till February (see below). functional legsand are capable ofwalking, climb-
There is so far only moderate evidence of a ingandsometimesrunning,buttheydonotjump.
comparable southern hemisphere cold season The females emerge from pupae on the ground
element, for example in New Zealand the genus withtheireggcomplementfullydeveloped; those
AtomotrichaMeyrick (Oecophoridae), which has ofthe flightlessspecies ascendtree trunks, where
several winter species with adult activity periods they soon attract the males and mating takes
in about August-September, and a few diurnal place. The eggs are then depositedwithout much
Tortricidae(Dugdale,pers.comm.)andZermizinga delayhigh up in the canopyofthe same trees. As
indocilisariaWalker(Geometridae; also foundin the larvae of most cold season moths are poly-
Australia). phagous, usually on deciduous trees, there is no
AsignificantminorityoftheLepidopterainthe need for flight in search of an appropriate host-
temperate zone ofthe northern hemisphere pass plant on which to lay the eggs, and an important
thecoldseason asadults, andspeciesoverwinter- barriertoflightlessness andwing reduction in the
ing in that stage are known in many families, femaleisremoved. Thefemale'slossoftheability
forexampleOpostegidae, Gracillariidae, Ypono- to disperse is at least in part compensated by a
meutidae, Lyonetiidae, Oecophoridae (Depres- dispersalphase inthelarvalstagewhentheyoung
sariinae), Momphidae, Gelechiidae, Tortricidae, larvaeactivelymigratefromtheovipositionsiteto
Alucitidae, Pterophoridae, Pyralidae, Pieridae, other parts of the plant or are passively trans-
Nymphalidae and Noctuidae. Because of their ported through the air, ballooning on silken
longevityboth sexesofsuchspeciesdependon an threads. Such passive transport accounts for the