Table Of Content.
JournalofRi'searrhon theI.(‘j>idol)lera 39: 8-17,2000 (2006)
Flight Patterns and Mating Behavior in a Zephyrus Hairstreak,
Neozephyrusjaponicus (Lepidoptera: Lycaenidae)
Michk) Imaflikh
Departnieiitof Zoology,(’iiaduateSchoolof'Science, Kyoto L'niversity,.Sakyo, Kyoto,606-8502Japan
[email protected]
Yasutoshi Matsui '
Institutef’ofEtivironinental ManagementTechnology,National fnstititteof'Advaticed IndustrialScienceandTechnology, 16-1 Onogawa,
Tsiiknba, Ibaraki, 305-8569Japati
Hideko Matsui "
.5-102, 740Santiki, Ryngasaki, Ibaniki, 301-0033Japan
' Present address: 7-106, 1-2-63 Enjimi. Iligashitnnrayama,Tokyo, 189-002IJapati
Abstract: Elight patternsatid tnatingbehaviorsofa/ephyritshairstreak, Neozephyrusjaponkus,were
itivestigated in awoodland in Rvngasaki (lity,Ja|)an. dtiritigitsadult flight period in lateJuneand
|nlv, Iroin 2000to2003. Thisspecieswasmostactivearounddusk,fiom 17:00to 18:00hrs,during
which malesactivelyflewaround thecanopyandedgesoftheforest. (Circlingflightsperformedby
two individitals were lre(|itentlyobserved, as were chase flights, sometitnes cotnposed ofmitlti|tle
individuals. (Circles flowti chiringcirclingflightsaveraged 14can in diameterand 2.9 rotations/s,
tints the velocity ofthese flights averaged about 130 cm/s. Ehe directioti ofrotatioti sometitnes
changedditringcirclingllights. Athirdindividttaloccasionallyjoinedacirclingflight,whichwould
sometimes disrupt the flight, or rarely, would replace one ofthe origitial circlets, (lhase llights,
sometimes in a zig/ag pattein, ttsualK' included a female, atid sometimes led to the initiation of
courtship. Uourtshipatid copulation sometitnesoccutred jitst afterchase flights. Coitrtship time
wasbetween30secondsandoneminute,andcoptilationtittlevaiiedfrom45minutestooverthree
hours. Examinationofthebitrsaco|iulatrixof femalesofN.japonkusfrom thesttidysiteindicated
thesporadicoccutfenceof imiltiplematings.
Keyword.s:activitvtitne,circlingflight,chase flight, mating, Lycaenidae,sperniatophore
Introduction tion. Some species ofChrysozephyrns, NeozephyrusAnd
Favoniussd\o\s^themostconspicuouscolordifferences
Butterflie.s in the tribeTheclini, commonlycalled between sexes amongbutterflies occurring inJapan.
“zephyrtrs haiustreaks” in Japan, are biologically These colorvariationsmaybe related to the behavior
intere.sting for a variety of rea.sons. This relatively and ecology of the various species. Males of some
small grotip shows great variation in adult and larval species are territorial, and mate-locate by guarding
morphologies, life histories, physiology, behavior perches, whereas others mate-locate through patrol-
and ecology (Saigtisa 1988). In Japan, this group ling. Adult activity times vaiy among the different
includes 2,5 species in 13 genera such as CJirysozephy- species; some are active early in the morning, some
rus, NeozeJ)hynis and Favonius, whose phylogenetic during midday, and others are most active at dusk
relationships have been sttidied, using morphologi- (Fuktida et al. 1984). However, published informa-
cal (Shirozn &Yamamoto 1956) and molecular data tion on the behavior and ecology of the zephyrus
(Saigusa & Odagiri 2()()()) hairstreaks is incomplete, and systematic stitches on
An intriguing aspect of the Theclini in Japan is the ecology ofthese hairstreaks have not been previ-
variation in wing colors; 13 species show sexttal di- ously conducted. This is partly because adults are
morphism, 11 species are nearly or perfectly mono- largely arboreal, and thus, makedifficult subjects for
morphic, and 1 species is in an intermediate situa- behavioral or ecological studies.
Previously, the senior author observed mating
behaviors ofone ofthe sexually dimorphic zephyrus
Recewed: 10June200-4
Acrepled: 10March 2005 hairstreaks, Neozephyrusjaponicus (Murray, 1845),
39:8-17,2000 (2006) 9
malesofwhichhavemetallicgreenscaleson thedorsal bya narrow lane into two sections; one composed of
surfaceofthewings,whilefemaleshavemostlybrown tall (10-15 m) aldertrees, AlnusjaponicaSteude], and
orblackwingsabove. Twoattemptsatcourtship,and the other composed ofwillow trees (4-6 m), includ-
one copulation eventwerewitnessed, among22 indi- ing Salix subfragilis Andersson and S. cliaenomcloiclcs
viduals releasedin alargecage (Imafuknetal. 2()()()). Kimura (fig. 1). Alnus japonica is a local foodplant
Stibsequently, thejuniorauthorsobservedcopulation for larvae oi'Neozephyrusjajwnicus. The studysite was
eventsamongwild pairsofTV. japonicus. Theirresults surrounded by grasses such as the reed Phragmites
were reported at the meetings of the Lepidoptero- co?»wunisTrinius, the goldenrod SolidagoallissimaL.,
logical Society ofJapan from 2()()() to 2002. Since and also by cultivated fields.
then,wehaveconductedasystematicinvestigationof
matingand related behaviors ofawild population of Observation ofdiurnal activity
TV. japonicus. Herein we present the results of those
studies, includingdetailsofmatingbehaviorfrom the The number ofbutterflies observed in flight was
initiation ofcourtship to final copulation, alongwith recorded every 15 to 60 minutes, from dawn to dusk,
information on diurnal activity, circling and chase byslowlywalkingalongthelane. Theairtemperature
flights, and experimental results on male responses wasrecordedevery5minuteswith atemperaturedata
to female models. logger (Gemini DataLogger, temperature) settledin
the willowgrove (T in fig. 1). The light intensitywas
Materials and Methods recorded by an illuminator situated in open space
(shown with L in fig. 1), and datawere stored every5
Studyarea minutesinaseconddatalogger (Gemini DataLogger,
voltage) ThesecountswereconductedfromJune 30
.
Thisstudyon thebehavioroi'Neozephyrusjaponicus toJuly 2, 2002.
was conducted in a small wooded area in Ryugasaki
City, Ibaragi Pref.,Japan (35T55’N 14()‘’1()’E), during Observation offlight activityusingavideo camera
thebutterfly’sadultflightseason,from theendoffline
toJuly, 2000 to 2003. The wooded area was divided Tliese sinweyswere conducted on 4 days between
July 2 and 7, 2002. During the peak time of adult
activity, near dusk, many butterflies were observed
flying over the canopy and edges of trees, occasion-
ally performing chase flights and circling flights (or
thespiral flightdescribedbyDavies 1978). Torecord
a detailed temporal seqitence of changes in these
activities, a digital video catnera (Sony, DGR-rRV20)
was set at a fixed point (Ci in fig. 1) to record flying
bittterflies. The camera remained stationary, and
recorded individuals that appeared on the north
side of the alder woods. Numbers of butterflies, of
circling flights and of chase flights appearing every
10 minutes were recorded from 16;3() to 19:00 hrs.
Numbers of butterflies were estimated by treating
each individual appearing on the .screen, until the
time itdisappearedfromview,asseparateindividuals.
Theairtemperatureandlightintensitywererecorded
with a thermometer and illuminator (Mother Tool,
LX-lOO).
Detailed observations and experiments
Fig. 1. Studysitein RyugasakiCity, IbaragiPref.,Japan.
Patches of willow and alder trees were separated by a
path. A thermometer (T) and an illuminator (L) were In ordertodocumentdetailed patternsofcircling
placed as indicated. A digital video camera (C) was and chase flights, butterflies were recorded with a
installed for observations of a fixed area, north of the hand-held digital video camera. Recorded images
alder grove. A and B indicate sites at which individuals
ofN.japonicusweremarked(seeResults). Wil.=willow; were then incorporated into a personal computer
Ches. =chestnut. using “iMovie, 2.1.1” (Microsoft), and flight paths
10 J. Res.Lepid.
were plotted using “NIH images, .62” (courtesy of individuals. With increasing darkness, numbers of
1
the National Institute of Health, USA). For draw- flying hairstreaks decrea.sed, and no butterflies were
ings in figs. 5 and 6, and in measurements of flight observed by 19:30 hrs.
velocity, a reducedscalewascalculatedbycomparing
the image size ofa butterfly oil the computerscreen Eveningflight activity
to the average natural size ofbutterflies collected at
the studysite. Two arbitrarilydetermined reference Observations recorded with the fixed video cam-
points were also plotted to compensate for changes era during the evening period of peak activity are
in images caused by zooming and movement ofthe shown in fig. 3. Flying butterflies first appeared at
camera during recordings. 16:55 brs., when the light intensity was 13,000 lux,
As chase flights were inferred to occur on par- and numbers offlyingbutterfliesgraduallyincreased
ticipation ofa female, two model experiments were with a peak around 18:15 hrs. (fig. 3b). The average
performed. In thefirstexperiment (“female model,” time ofpeak adult activity was calculated to be 18:07
July 4, 2001), a female hairstreak was allowed to fly, hrs. The lightintensity at this time was about 4,000
but was tied to the tip ofa 3.3 m fiberglass rod with lux. After this time, the number offlying butterflies
60 cm ofcotton string (#50) secured to her thorax, gradually decreased.
between the fore-and hindwings. In the second Circling flights started to occur as number offly-
experiment (“female wing model,” July 7, 2001), ing butterflies increased, and continued until flight
female wings were pasted on both sides of a plastic activityended (fig. 3a) Thefrequencyofchaseflights
.
figure (made from a plastic plate), shaped to mimic
afemale hairstreakholdingitswingsopen,whichwas
Lightint.
secured to a rod and rotated with a small motor. In XIO^lux
each experiment, modelsweresituatedinareaswhere
male hairstreakswere active.
In order to determine the sexes of butterflies
involved in chase flights, capture with an iirsect net
wasattempted. Forobservationsofmatingbehaviors,
binocularsandatddeocamerawereused,anddetailed
\erbaldescrijttionsofvariousprocesseswere recorded
on the latter.
Results
Diurnal activity
Adults of Neozephyrus japouicris were most active
from 17:00 to 18:00 hrs., just before dusk (fig. 2).
This period of peak activity was essentially the same
on clear days (e.g.,June 30 andJuly 2, with the high-
estairtemperatureover28”Candthemaximtim light
intensity exceeding 60,000 lux) as it was on cloudy
days (e.g., July 1,with temperatureslowerthan 25.5‘’C
through thedaytimeand themaximumlightintensity
lower than 20,000 lux). On clear days, some adult
activitywas observed in the morning. Shortly before
the period of peak adult activity, around 16:00 hrs.,
females were frequently observed on grasses around
the woods, sometimes basking with open wings. As
Time (hrs.)
time elapsed, they moved to highersites in the trees.
Around 16:30 hrs., males started to fly over the sides
and canopy ofthe alder and willow groves, andocca- Fig. 2. Changes in the number of flying individuals of
N. japonicus (thick line) on three days in 2002. Thin
sional circling flights by two males were performed. and dotted lines indicate light intensityandtemperature,
As it became darker, chase flights occurred, in which respectively.Twodays(June30andJuly2)weresunny,
somebutterfliesappeared tobe rapidlychasingother whileJuly 1 wascloudy.
39: 8-17,2000 (2006) 11
Table 1. Diameterandrotationspeedofcirclingflightsin third individual. Among these, six were continued
Neozephyrusjaponicus. by the original circlers with the third butterfly fly-
ing away (fig. 5e), six were broken up, and two were
continuedbytheoriginal and the newlyarrived third
Sample Sampling Diameter Rotation individual (fig. 5f) At theendofcirclingflights, one
time (cm) .speed .
of the circlers flew away sometimes, chased by the
(s) (roimds/s)
other (fig. 5d).
#1 1..30 11 3.8
#2 l.-TO 12 2.9
#3 2.77 16 2.6
#4 2.93 15 2.4
#5 3.73 19 2.6
#6 2.07 12 3.2
#7 2.63 11 3.1
#8 2.63 20 2.1
#9 .3.13 12 3.3
#10 1.97 15 3.1
Average 2.47 14 2.9
Range 1.,30-3.73 11-20 2.1-3.8
was greater in the later half of the evening activity
period. The greatest average number of circling
flights occurred at about 18:05 hrs., while the great-
est number ofchase flights occurred slightly later, at
about 18:20 hrs.
When maleswere active in circlingflights, captur-
ingattemptsweremadeforbutterfliesstrayingaround
acanopyorsub-canopylevel,witharesultthat4outof Time
5 captured individualswerefemales. Flight behavior
offemales appeared to be somewhat diflerent than
that ofmales, in that they flew slightly slower, and at
a lower altitude. Fig.3. a.Temporaldistributionofcirclingflights(graybar)
and chase flights (solid bar) during the evening activity
Circlingflights period of N. japonicus at the study site. b. Temporal
distribution of flying butterflies at the study site. Light
intensityandtemperatureareshownwithsolidanddotted
Circlingflightsinvolvedtwomalebutterflies,each
lines, respectively.
flying rapidly in a small circle. Most circling flights
werecompletedinafewseconds,whereassomelasted
longer. Durationsof46circlingflightsobservedfrom
July 12 to 17, 2002, are shown in hg. 4. Most circling
flights (72 %) were completedwithin 30s. The long-
est circling flight lasted 6 min 18 s. The diameter of
thecirclevariedfrom 11 cm to20cm,with anaverage
of 14 cm (Table 1). Butterflies engaged in a circling
flightrotated2.1 to3.8timespersecond, 2.9timeson
average. Thus, their flight velocity in circling flights
was calculated to be about 130 cm/s.
A trace ofa typical circling flight is shown in hg.
5b. Circling flights were frequently initiated when
males happened upon each other, either through
random movements (fig. 5a), or through a chase. Duration (sec.)
Rotation directionwasnotalwaysfixed,andasshown
in fig. 5c, sometimes changed. In some cases, a third
individualjoined into ongoing circling flights. Out Fig.4. Frequencyofcirclingflightsin N.japonicus,plotted
of46 circling flights observed, 14 were invaded by a againsttheirduration.
12 /. Res.I.epid.
Fig. 5. Traces of flight patterns related to circling flights of N. japonicus. In each figure, alphabetical letters (upper cases)
indicate individual butterflies and their positions in the first frame of the figure. Each point on the trace line represents the
position ofthe butterfly in successive frames, thus, every 1/30s. A scale barbeloweach figure indicates 10cm. a. Initiation
of a circling flight (17:12:55, July 1, 2002). b. Typical circling (18:09:44, July 1, 2002). c. Change of rotation direction; the
initial right rotation forthe butterfly (left rotation forthe observerbelow) changesto a left rotation (17:48:11, July 1, 2002). d.
End ofcircling, resulting in achaseofonebutterfly(A) bytheother(B) (18:14:52, July 1, 2002). e. Approach andsubsequent
retreat of athird butterfly (C) to acircling flight (17:34:21, July 1, 2002). f. Replacement ofcirclers. One ofthe initial circlers
(A) continuestocirclewith the invader(C), whiletheothercircler(B) retreats (18:00:37, July 12, 2002).
Residency day of the study. Thrrs, butterflies in the study field
exhibited a certain degree of esidency.
r
(Circling flight.s or .spiral flights are usually shown
by territorial species (see Discu.ssion). Males of Ne- Chase flight
ozrphyrii.sjaponicusin thestudyareadid notshowclear
territorial behavior, but some males repeatedly flew Chase flights were occasionally initiated immedi-
around a specific jjarts of the canopy. Therefore, ately after circling flights, and sometimes involved
residerrcywasexaminedfororrrpoprrlation. Twobut- multiple individirals (fig. 6d). Some chase flights
terflies at pointsAatrd B on fig. 1 were captured and were very persistent, covering a lar'ger distanceim-
markedwith ablack felt-tip pen on the irndersidesof mediately after circling flights. Rarely, zigzag flights
the wings at aborrt 18:00 hrs onJrrne 29, 2002. The involving two irtclivicliralswere observed. A trace ofa
birtterlly marked at point A was recaptured at the zigzag flight is shown in fig. 6b, whei'e one birtterfly
same site arrd at similar times the following 3 days, (A) approaches another (F), and proceeds to follow
irntil observations at the site were terminated. The it closely. The chasingbirtterfly (A) showed asimilar
brrtterfly rrrarked at point B was recorded from the tirrning pattern to that ofthe butterfly being chased
sarrre site the following 2 days, brrt not on the last (F), with a delay of 2 to 3 frames (67 to 100 msec).
Fig.6. TracesofflightpatternsrelatedtochaseflightsofN.japonicus. PresentationsarethesameasinFig.5,unlessotherwise
noted, a. Apersistentchaseofapresumedfemale (F) bya male (A). Traceswere interrupted becauseoftree branches; 12,
31 and24frameswere lackedatcircles 1, 2and 3, respectively. Thischasecontinuesat least5.8s (17:51:26, July2, 2002).
b. Azigzag flight. A presumedfemale (F) ischased bya male (A) which approachesfrom below (17:02:56, July2, 2002). c.
Flightpathofthepresumedfemalepriortochasebyamale,showinga“swinging”flight. Thefinalpointofthisfigurecontinues
to the start point offigure b (17:02:54, July2, 2002). d. A group chase. A presumed female (F) is always at the lead. “The
male“C”appearsinthefigureafteratthe 12thframe (17:22:07, July2, 2002). e. Chaseflightbytwo males (A& B)tothetied
female model (M) (18:28:29, July4, 2001). f. Simultaneous approach ofa solitary male (A) and circling males (B & C) to the
femalewing model (shown with across nearthecenter) rotated bya motor (17:58:03, July7, 2001).
Zigzag flights observed at the study site are thought (chasing) and female (leading) hairstreak, and the
to involve the chasingofafemale bya male (see Dis- reactionsofmalesupon identifyingapotentialfemale
cussion). Prior to the zigzag flight shown in hg. bb, mate. Multiple males were attracted to the “female
the presumed female (F) descended from the alder model” tied with thread, and closely followed her
canopyintoan openspace,whereshe flewin aswing- flight when she turned sharply (fig. be). In fig. be,
ing flight (fig. 6c). the chasing male followed the abrupt turn of the
Occasionally, a hairstreak was observed to ap- tied femalewith a delayofabout 2 frames (67 msec).
proach a circling flight involving two males, which When the “female wing model” rotated by a motor
resulted in the chasing ofthe third individual by the wasrevealedatthestudysite, oneormore maleswere
twomalesthathadbeencircling. Incasessuchasthis, frequentlyattracted (fig. bf). It should be noted that
the approaching individual may have been a male males engaged in circling flights were sometimes at-
(as seen in figs. 5e and 5f), but in several cases it was tracted by both ofthe models.
thought to be a female, because the resulting chase Finally, thecaptureofbutterfliesengaged inchase
by maleswas vei'y persistent. flights was attempted, using an insect net. Among
The model experiments sought to test the idea each ofthe threesuccessful captures, onefemaleand
that chase flights are frequentlycomposed ofa male one male was involved.
14 /. Res.Lepid.
Table2. Copulation statisticsfor Neozephyrusjaponicus
(^ase Date Time Temp. Duration Site (from theground)
#1 l()-7-’()0 18:46 24.5“!: on an alderleafat3.8m
#2 12-7-’()l 18:20 27..6°C ca. 3:20 on agoldenrodleafat 1.2 m
#3 15-7-’()l 18:20 28..5°C .3:18-21 on agoldenrodleafat0.9 m
#4 12-7-’()2 18:20 25.5°C - on an alderleafat4.0m
#5 l.'i-7-’()2 18:13 28..5"C 3:07* on awillowleafat 1.8m
#6 17-7-’()3 17:13 21.6”C 3:43-4:27 onan alderleafin4-5 m
#7 17-7-'()3 17:48 21.6“C 5:12-6:08 onan alderleafin4-5in
#8 18-7-’()3 17:22 20.9“C 3:40-4:38 onan alderleafin4.5 m
*Pairswerecaretiillybroiiglit toaroom (30.()"C) andcontinuouslyobsen'ed.
Courtship and copulation goldenrod leafand the time they assumed a normal
end-to-end copulation posture.
During the study period from 2000 to 2003, eight Pairs ofhairstreaks landing togetherafterachase
instances of copulation were witnessed (Table 2). flightsometimes did not couple. In three such cases
("opulation usuallyoccurredon leaves,between 3to5 (17:45 and 17:55 on July 11, and 18:00 on July 12,
m aboveground level. OnJuly 10, 2000, at 18:46 hrs, 2000) copulation attemptsended in failurewhen the
achaseflightinvolvingfourbutterflieswasbroken up female flew away, even though in one case the male
when a male and a female split awayfrom the group, attempted copulation. In most ofthe copulation at-
andlaudedon an alderleaf3.8mabovegroundlevel. tempts observed, males did not open or flutter their
Subsequently, tlie male situated himself at a right wings. However, onJuly 12, 2002, one male slightly
angle to the female. About 30 seconds after laud- but rapidly and repeatedly fluttered his wings, while
ing, the male walked toward the female and aligned situated nextto thefemale, priortosuccessfulcopula-
himselfnext to the female, in a parallel position, so tion. Asshown inTable 2, copulation timesobserved
that theywereboth facingthesamedirection. Five to for Neozephyrus varied from about 45 minutes to 3
sixseconds later, the male curved the tip ofhisabdo- hoursand20minutes. Tocheckformultiplematings,
men toward the female’s genitalia, and afteranother the btirsacopulatrixof8femaleswasexamined. Five
five to six seconds, succeeded in connectingwith the ofthese females possessed one spermatophore, one
female, toassumeaV-shapedbodyposition. At 18:47, female had two, and two females had three.
the male straightened his figure, and the butterflies
faced opposite directions in a normal end-to-end Discussion
copulation posture. Then, they remained stationary
forseveral hours. At 4:25 hrs the followingmorning, Activity time
the pair was found separated. Anatomical examina-
tionofthefemale revealedonespermatophorein the Differentspeciesofzephyrus hairstreaksare most
bursa copulatrix. active at different times during the day. Previously,
On July 15, 2001, acopiilation eventwaswitnessed Neozephyrus japonicus has been described as being
after a pair of hairstreaks landed on a goldenrod most active around dusk (Fukuda et al. 1984), but
m
leaf 0.9 above ground level, permitting close ob- no detailed observations were presented. Herein,
servations. Upon landing of the female, the male we have documented that the peak activity period of
barelyclungto the leafonwhich thefemale normally wild N.japonicus'AdnXxsisbetween 17:00hrsand 18:00
perched. After the male climbed up the leaf, it ap- hrs.These results agree with those ofan earlierstudy
proached the female from behind at an angle of60°. on a captive population ofN.japonicus, where adults
Oncethe malehadoriented himselftobesidebyside remained inactive until 16:00 hrs, and were most ac-
with the female, in a parallel position, he retreated tive after 17:00 hrs (Imafuku et al. 2000).
slightly, sharply curving the posterior part ofhis ab- Peak periods ofactivity for some other zephyrus
domen to contact her genitalia. About 30 seconds hairstreaks have been determined usingquantitative
elapsedbetween thetimewhen thepairlandedon the data. As shown by Koda (1982) for Chrysozephyrus
39;8-17, 2000 (2006) 15
bnllnntinus (Staudinger, 1887) and by Takeuchi & 1758) flying in a circle with a diameter of50 cm to
Imafuku (2005) ior Favonius taxila (Bremer, 1864), 1 meter. Bitzer & Shaw (1979) figured a trace from
some species are most active during the morning, theflightofaredadmiral, Vanessaatedanta (L., 1758),
from 7:00 to 11;00 hrs. Hirowatari and Ishii (2001) flyinginanascendinghelicalpath,aslargeas9meters
showed that Favonius cognatus (Staudinger, 1892) is in diameter.
most active during midday, from 10:00 to 14:00 hrs. Circling individuals of N. japonicus occasionally
According to Koda (1982), adults of Chrysozephyriis changed the direction ofthe spiral, as shown in fig.
smaragdinus (Bremer, 1864) and Favonius orienlalis 5c. Suchchangeswerealsoobservedincirclingflights
(Murray, 1875) are most active from 8:00 or 9:00 to ofM. gotama (Sibatani 1998). However, twointeract-
16:00 hrs, with suppression ofactivityduring periods ingindividuals of V. atedantareportedlycircled “most
ofgreat light intensity. Abimodal pattern with activ- often in a counter clockwise direction as seen from
ity peaks in the morning and evening is known for below” (Bitzer & Shaw 1979).
Artopoetespryeri (Murray, 1873) (Koda 1982),Antigius As for circling or spiral flights, some functions
attilia (Bremer, 1861) (Koda 1982; Hirowatari 8c Ishii have been proposed. A contest for occupation of
2001) and Favonius saphirinus (Staudinger, 1887) territories by males of territorial species has been
(Hirowatari & Ishii 2001). As shown by Akiyama et widely accepted (Baker 1972; Davies 1978; Bitzer &
al. (1969) and Hirowatari & Ishii {2^01), Japonica Shaw 1979; Wickmann & Wiklund 1983; Takeuchi &
saepestriata (Hewitson, 1865) is most active during Imafuku (2005). Neozephyrusjaponicuswusdescribedas
the evening hours. Thus, times ofpeak adult activity a territorial species byFukuda etal. (1984). The two
are very different among different species ofzephy- individuals ofN. jafx)7iicus that were marked during
rus hairstreaks. Species-specific activity times might our study and observed for several days persisted in
be explainable in terms of predation pressures and guarding the same perching sites, day after day.
intraspecific mating behaviors. As noted by Sibatini (1989), circling flights are
The evening crepuscular activity of Neozephyrus also known for non-territorial butterfly species such
japonicusmayberelatedtopredatorevasion. Birdsare as Holochila helenita, Furema blanda (Boisduval, 1836)
known to be one ofthe most important predators of and Neptis sapfjho (Pallas, 1771). This suggests that
butterflies,andtheiractivitiesusuallydeclineatdusk. the behavior is not always related to the defense ofa
Swallows,however,weresometimeswitnessedtoattack territory, butthatitmayserve toaid in recognition of
circlingmalesot'N.japonicusduringourobservations, potential mates (Scott 1974; Suzuki 1976).
and some butterfly specimens collected during the Afurther possible explanation for circling flights
courseofthisstudyhad“beakmarks” (Johki 1985) on among males of N. jafmnicus could be to attract fe-
theirwings. Thus, it seems possible that the time of males. Such a scenario may parallel displays by two
peakactivityforadultN. japonicusissittiated between malestowardafemaleasseen in manakinbirds (Snow
the time in the eveningwhen most local bird species 1963; Grzimek et al.l968), where ornamented males
become inactive, and when it becomes too dark for show a specific synchronotis dance in front of a fe-
hairstreaks to see. male.This idea is discussed in further detail below.
Circlingflights Chase flights
In N. japonicus, the diameter of circling flights Chase flights between two individuals sometimes
averaged about 14 cm (Table 1). Apparently, the attractedtheattention ofotherhairstreaks,andsmall
diameterofcirclesflownbyotherspeciesofzephyrus groupswereoccasionallyinvolved inchases. Capture
hairstreaks has not been measured. However, Fiijii ofhairstreaks engaged in chase flights revealed that
(1982) illustratedflightsofChrysozephyrussmaragdinus, suchflightsincludedatleastonefemale. Chaseflights
Favonius taxila, Iratsume orsedice (Butler, 1881), and wereoftenterminatedwhen twoindividualsbreakout
(Hewitson, 1865) in “small circles.” In contrast, the ofthechase,andlandneareachother. Thisoften led
diameter ofcircles flown by another lycaenid, Holo- to subsequent courtship or copulation. Thus, chase
chilahelenita (Semper, 1879) extendsupto 1-2meters flightsare thoughttorepresentthepursuitofafemale
,
(Sibatiini 1998). Amongnymphalidbutterflies,Davies by males, and may be one ofthe steps in courtship.
(1978) depictedtwoindividualsofParargeaegeria(Lin- Zigzag flights observed in the j^resent study (fig.
naeus, 1758) spiraling in small circles, and Sibatani fib) seem to be a type ofchase flight, where a female
(1998) observed a co-rotating flight of 20-50 cm in is being chased by a male. A similar flight pattern
diameter for Mycalesisgotama Moore, 1857. Sibatani was observed in another zephyrns hairstreak, Chrys-
(1998) also observed Hyjwlimnas holina (Linnaeus, ozephyrussmaragdimis (Imafuku pers. obs.). Males of
e
Hi /. Ri’s.Lipd.
C. smaragdinushave brilliant green wings above, and (ref. Suzuki 1988), or the accjuisition ofnutrients by
are most active during midday, from 10:00 to 16:00 females from spermatophores contents (Boggs &
Ill's. Therefore,wecouldeasilydetermine thatzigzag Gilbert 1979).
nights were composed of a male and a female. It The function ofmale coloration deserves further
seems possible that females are exerting some selec- di.scussion. Since the fittest males in various animal
tivechoiceon males, perhapsasjudged through their populationsareoften thosewhosuccessfullycompete
maneuverability, during zigzag flights. for mates (Krebs & Davies 1981), male coloration in
sexually dimorphic species may serve to attract or
Courtship and copulation court females. Asearlyas 1874, Darwin (p. 505) pro-
j)osedthishypothesiswhenhenotedthat“whenwesee
Courtship and copulation events between pairs manymales pursuing thesame female,wecan hardly
—
ofN. japonicus were witnessed ihronghout the peak believe that the pairing is left to blind chance that
activityperiod ofadults, around dusk, and usuallyoc- the female exerts nochoice, and is not influenced by
curred on vegetation between three and five meters the gorgeous colours orotherornamentswith which
above ground level. The timing and placement of themaleisdecorated.” Scott (1973: 101) subsequently
theseevents mayprotectcoupled pairsofN.Japonicus noted that “this places selective pressure on males to
avoid diurnal predators, and tiiay help them avoid develop sexual characteristics to make the unrecep-
terrestrial predators, such as centipedes and carabid tive femalesreceptive, Thismayexplainwhymales
...
beetles, through periods of relative inactivity duritig havebrightercolors...” Rntowski (1985) showed that
the night. males of Colias eurytheme Boisduval, 1852 with strong
Duration ofcopulation between pairsofA^. japoni- LIV reflectance patterns were more readily accepted
ncsrangedfrom 3 to6 hours (Table 2). Thisdoesnot as mates byfemales than were maleswith weakor no
largelydifferfrom times observed amongindividuals UV reflectance. However, Silberglied (1984) could
ofN. japonicusin captivity, between 2.5 and 3.5 hours not confirm this for the nymphalid Anartia amathea
(Imafnknetal. 2000). Scott (1973) .summarizedcopu- (Linnaeus 1758), in which males preferred colorful
,
lation times for various butterfly species. Extremes females but females apparently exhibited no choice
included 10 mituites for PapiUo xulhulus, two days between colorful andcolorlessmales. Ifmalecolora-
for some Parnassius and Picris species, and among tion serves to attract or court females, it seems that
lycaenids, twotoeight hoursfor Pallophyrusaugustinus malesshouldactivelydisplaytheirwingsduringcourt-
(Westwood, 1852) and hourormoreforNojdmannia ship. Duringcourtship betw'een pairs ofthe sexually
1
iiicis (Esper, 1779). According to Wlklund (2003), dimoi'phiclycaenid Pseudozizema maha (Kollar, 1844),
copulation timesvaried from 10 min in Coenonympha the male’swingsareheldwddeopen,asseen in photos
panipliilus (Linnaeus, 1758) to a week in Goncpteryx by Wago et al. (1976) and Wago (1978), or may be
rJtamni (Linnaeus, 1758). violently fluttered, demonstrating the conspicuous
Multiple matitigs were conhrmed amongfemales blueuppersidecoloration (pers. obs.). However,such
of N. japonicus. This phenotnenon is widespread behaviorwasnotobservedamongcourtingmalesofN.
atnong butterfly species. Scott (1973) examined japonicus, although slight flutteringofwingswasseen
females of various butterlly species and found that on one occasion. In onr study, presumed females of
about 95 % of those species sometimes engaged in N. ja/)onicuswere occasionally observed to approach
multiple matings. Suzuki 1988) studied the number a pair of circling males, resulting in the formation
(
ofspermatophores in females of29 butterflyspecies, ofa chase flight. In such cases, the female may have
and found that all of them possessed two or more beenattractedbymalecoloration,butatthemoment,
s])ermatophores, except Lycacna jddaeas (Linnaeus, no evidence to support this idea has been presented.
1761) with had only one. The maximum number of Eurtherstudiesonthefunctionofmalecolorationand
spermatophores found in a single female butterfly ofcircling flights in N.jafmnicus'dr needed.
was 15 in a female oi'Danausgilijprus (Cramer, 1775).
Seventeen papilionid species studied by Matsumoto Acknowledgements
&Suzuki (1995) includedfemale individualsthathad
tnated more than once, atid some females ofPapilio We thank Dr. AndrewWarren ot the DepartmentofZoolog)’,
Linnaeus, 1758and /I bianorCAAmer, 1777had Oregon State University wlio elaltorately read and extensively
tnated 6 times. Thus, the phenomenon ofmultiple im|)roved the mantiscript together with valuable comments;
Messers Ktt/ito Matsubaraand Katsnyoshi lino, theownersofthe
matings seems to be general among butterflies. The sttidysite, for permittingtts towork there and also forarranging
function of multiple matings for females is thought thepath toallowforeasierobservations;Tasnkn Kitamnra,ofthe
toiuclude theproduction ofheterogeneousoffspring EthologicalLaboratory of Kyoto University, for assisting in onr
.
39:8-17, 2000 (2006) 17
study;andtheUnitedStatesNationalInstittiteol 1lealthloruseof Sieboldia 1: .329-421.
computersoftwaretocreateimagespresented herein. StBATANt, A. 1989. Conspecific recognition in male butterllies.
Co-rotatingand catenate llights. Rivistadi Biologia-Biology
Forum82:"l.5-.38.
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