Table Of ContentTThheLee piLdeoppteirdoloopgitcaelrSooclieotygical Society ooff JJaapapnan
uetwh LepidopteraScience64(4)1:68-171D,ecember2013
A unique relationship between air temperature and reproductiye activity time of butterflie fsound
in CZhrysozephyru ssmaragdinus (Lepidopte Lryac:aenidae)
TsuyoshiTAKEucHIi)2･)
i)Center forEcologicalResearch,KyotoUniversityH,irano2-509-3,Otsu520-2113,Japan
'lechn ology
2)Department of Biofunction aSlcience and Graduate School of Biosphere Science,HiroshimaUniversity,
Kagamiyama,Higashihiroshima,737-8528Japan
Abstract Climati cfactor shave larg eefi'eets on the activity of ectotherrns. I investigat ethde effects of air temperature
on the territoria blehavior of a lycaeni dbutterf lCyhrysozephyru ssmaragdinus. Males initiat ethdeir territori aalctivity
late ron hotte rdays. Apparentl ysimilar shjfts arc known in some butterf isypecies, and regarded as heat avoidance. In
the case of C smanigdinus, this shift cannot be regarded as heat avoidance because ,on hotte rdays, they ceased territorial
activity in the relatively cooler hours between 1O:OO and 12:OO and hold territorie bsetween 12:OO and 17:OO during which
theairtemperaturereachesitsdailymaximum.Thisisauniquerelationshipbetweenairtemperatureandthereproductive
activity time of butterfli Peoss.sibl yC. smarugdinus mud-puddle in the mornings of hot days, which might delay the start
of their tenitoria lactivity on such days.
Key words Climati cfacto rd,airy activity, ectotherm,territory, solar irradiance.
Introduction inhabitintgemperate deciduoufsorestisnJapan,Males
Rceerptariondtiumcestoifvt heaecdtiavyi.tFyor eoxfa mbpulet,tmaelrefsoif iithes esohfatiernst rreesatkricted to otfhe tmhe w ibtuhtt oetrhefrl y hmaoilesd ma tbiengtwe etner rcia.t o1riOe:s OaOnd and co m1pe7t:eOO. Tohveery
F(e(otasieaa(2wlainxlccvwcpinb0ini.tetTKeotet ts,ii u0knichtt v.vsaeei vieiiivh2eu2rntg tnienemskr0ocy)lyWgtsfe me. 1t ny.yiena ece s3v m Ts ar 2cirabataupap )urhkiet0u iye ers.lot om c,ne c0safmecoafI aabcias e3ohxni r.(nwe ne. fpdlf.tie) s t ,ini(Thlc eas Te.t1. Uoia bnMtycKarn hs3 Irlatut Iidukeir m:fltofta1nc oea neeOs aroir t9tottdffssesouOucfm ,8 e uuihpse na8t ,o cacrdrkrnondfe1;oheoo tuh icsf e sd9d Mei2r,e b pyfm iupe9Fm ore0atcLsfe ltca i2ft,ialmir1eh.tcnti2yav ) satcgas0inoeale0e,,rtgdvne-)huc u0seseil i,gaes,l h5 aola tsohy e natec afpnpf dith tcac)a ereodbaest etl ac,ucci rul ermiin tgtlviahhtirnmediuiomiaewit gatatnhdvmsoylutted piaeia mroitnFett nsirte d rchyiat sisfiri aors ici btieae.cHooe rnfe stfsu itrd nocfobciag b teeie aalwovtahuah cssruinti teeemhetulc t nhtttaoir ers ya ytlu aeyhe orttefel2ted,rp( eeoc hsdrfre tat 0 ceroFer oamslem(ar d0cota,roe .ssn urhlftnr vdare1coie eneto tiei r tsine; 1f imdm onipmlvibv5 sagnlro eIaeag:eeltte isrna dieOaothasheyrdellftOtees,g,yetd)lmdNtNbpamSm(bswfoodahbeeaouaaerrieauy2isscannglceigtentcitht0hrvdanlawdvcwtegen 0 a .yneae eeaotdoasa tx5 isaIoete erc pmoejat nm lb antnon,sP rorta igk soiotr it)ethrrnAnv sesn swtahhytiittsdeoonehaeetptu hfr.gm ye tp o t l as aa.Jcproworrtitt ti ifteafa otathi see T tnS repeha daps d CsslhCasa seali.ih .pgi eatid.ym tp n Te iioteunkaeseis c n,ehnavjsmcrysaftmoedf rsateianecamre.i uufdnrarpstT u da gnc aeeai ia ydhlaot grtosfhl ,ir,trtsfhnideetansl u ooctihee"i,ni Ioee s sruenetf dn co p rdu lhendimeic t aesi eeivsdrsaaI ioeh frietafr r,waefmnft nfya hf ydof it et a attebeufhNanearafee tlthrrgar atreTbrcttt Uer mrorgnae htNih nk iee, cktatJeesoaetxas u eeowduieh nwoinierg roue ahn(rfrsd oonrisatfssceo itetta2 eie oalae,nhnh tctli rnrelnt0ateeiro The- coc r 0 i a ttalteat taca thAaudetoiao5tnnnoerm fuumiv shddarelbv cpigo t tiitlat eatf o u) taawi-rlI ybntS Sy rslo ssnaarismcopphhhteftcig leae ywa.u iaeitiyfrc fmssr tiiaveteonaioTufo eivletteritnjj tshrmki eedcxosetheaaueiitr,tyterrrnii,.
summer generations avoid the hotte$t time$ (Ide 2,002), effect of air temperature on their tenitoria alctivity pattern,
Simi1a rshifts of territorial activity periods towards earlier
morning or late arfternoon in hotte rseason are known in Materials and methods
o1t9he9r6 b) u.Itt ties rrefasio in(aebBlseitz e atrnod t Shhianw k,th a1t9 9t5he; sReu tshoiwftssk ia reet atlh.e, Study sites and periods
result of avoiding overheating, The observations of tenitoria lactivity were conducted
Cht),sozephyr ussmaragdinus is a univoltine butterfiy bemeertgewdeen 1 u1n tJilu nmeo astnd 1ma2l eJsul y d2i0s0a8 p(pbeearfeo d Cr)i. nes mMaartasgudimnoutso
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Tetnperatur eet'fects on butterf iayclivity 169
Fig ,1 .The study sitc. Matsutnoto ,Nagano, Japan. Fig, 2.A territori amlate ot' Chtlvso.-,eph .svmtrtitu.tadsiittts.
(36 '1 5'N, 138000'E, 800 m alt), Nagano Prcft}ctur cJ,apan. air tcmperuture. Kendall runk-order correlation between
1 assigned a value of 1 to the fir sdtay of observation of the start, peak, end time and mean air tempcraturc was
the buttcrf liyn the adult season (Jun e17) ,and rescaied calculated. Kendal lrunk-order correlation between the
all late rdate saccordin,o,ly. The study arca is in a south- three times und date was also caleulated. For this analysis,
facin gvalley in tcmpcratc deciduous fores t(Fis ,1.). days when their territori aacltivity was inten'upt eatd ,least
Territor ibaultterfl iweerse found on the twigs of trees temporarily by rain were excluded. All statistica lanalyses
along the stream (Fig 2.). were performed using R 2.15. 0(R Development Core
Tcam,2012).
Observatien
1 observed butterfl ibeessid ea trunsec tupproximately 350 ResultsThe
m in length along thc strcam once per hour between 1O:OO
and 17:OO every day. exccpt for rainy periods .In each average air temperatures and the averag ¢ numbcr of
hourly census, I recorded the number of males occupying active males are shown in Fig. 3. Males start territorial
atenitoryandthoseengagingincontests.Airtemperatures activity in thc morning, are most active the around 14iOO,
were measured once per hour with a mercury thermometer and disappear in the evening. Seasonal changes in
hung in the shade at a height of 1.5 m.tcaptured rnales temperature and ma]e activity time are shewn in Fig. 4.
when they firs tappeared at the study area, markccl them
tndividual alndy, released them upon the spot. This rnarking 20 ''rr""-n" -T-･'1/-
procedur ewas performed for another study ([[bkeu canhdi s 24
Honda,2009). ..--e--N e--t
Statisti canaallyses 15 ,,
I tested the efTects of not only air temperature but al so the e.86 fi 6?:--
edects of date on their territori aalctivity becaus etherc m]'v
rnay be seasonal effects othcr than thc effccts of air rtO6z 9-wy
tcmperature. These analyses were pertbrme don a daily E-R{1
basis .The census hour when the firs tterritoria lmale was T s 9'-Iil
observed on each day was defined as the start timc. Thc 5 t-
census hour when the maximum number of males was i1/ 41o
observcd was define das the peak time. The census hour
when the las tterritori amalle was observed was defined o /
as the end time. 1 used mean air temperature between aO at a2 t3 14 15 16 IT
10:OO and 17:OO (territo raicati]vity time. Fig .3) as an TLmeofday
index of air temperatures of the day. Other measurcment Fig.3. Daily territoriat activity of Chrs";.el)h.vrt ,fssniaragdinLfs.
of air temperatures. such as dail ymaximum temperature The tLveruge number of malc C. smairtgdin!fs observed
or temperature at 1O:OO (th eeariiest start time). were not in the study site "il]e bdars ,± S.E.) and average air
used because they were highl ycorrelated with the mean temperaturc (opc ncircles, ± S,D,) are shown.
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I70 T.TAKEUCHT
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6"S20 24 25 2627 2S 307it234567dO 11 12
Day 919 20 2G 22 23 24 25 26
Fig ,4.Tenitorialactivitytimeofeachday,Thestartandtheend Meanairtemperature(･C>
time of each day are indicate dby horizont al]ines T,he Fig .5. The relationship between mean airtemperatu rofethe day
peaktimeisindicatedbyfi11edcircles.Meanairtemperat u r e and tbe start tjme.
of the day is indicate bdy open circles.
Table 1. Kendall rank order correlation between male activity initia ttheeir tenitoria lactivity at 1O:OO on cooler days but
times and extcrnal factor s*. P < O.OS at 1 1:OO or 12:OO on hotte drays (Fi g5). .That is ,on hotter
Mean air tem erature Date days, they avoid the relatively cooler hours between 1O:OO
Start time T=O.693,P<O.OO1* T=e286,P=O.152 and 12:OO and hold territories between 12:OO and 17:OO
Peak time T=O.283,P=O.147 T=0263,P=O.176 during which the air temperature reaches it dsail ymaximum
End time T=O.181,P=O,357 T=O.471,P=O.O16* (Fig 3.) .Can other climatic factors explain the observed
patter inn C. smaragdinus? It is known that intense solar
irradian c(emor ethan 7OOOO lx) suppresses male territorial
The results of statistica lanalysis are summarized in [Iable activity of C. smaragdinus (Koda ,1982) .However, solar
1. The stan time was positive lcoyrrelated with average irradiancecouldnotexplaintheobservedpattern.Generally,
temperature, indicati ntghat the butterfi isetsarted their solar irradian creeaches it sdail ymaximum at noon. If
territori aacltivity late ron hotte drays (Fi g5.) .The peak males avoid intens esolar irradianc teh,ey should ayoid
time was not correlated with average temperature or date. around noon, not from 10:OO to 12:OO .Why do males of
The end time was correlated with date ,indicati nthgat the C. smaragdinus avoid the relatively cooler time zone on
butterfi ideeslaye dtermination of their territori aacltivity hotte rdays? One possibili its yas follows .I tis reported
late rin adult season (se Feig ,4). that C. smatzzgdinus and some other related species come
down to the ground and extend thei rprobosci osn dry mud
Discussion or stones in the mornings of hot days (Hama ,2002;
Nishioka,2005; Takeuchi,2007).Perhaps thisbehavior
Males of a smaragdinus exhibit tenitorial activity roughly corresponds to mud-puddling aimed to intake sodium andl
from morning to evening (Fig 3.). This is congruent with or nitrogen (Arms et al., 1974; Beck et al., 1999; Honda
previous reports (Koda ,1982; Tlakeuchi and Imafuku, et at., 2012). Mud-puddling in the morning may delay the
2005b). More detailed analyses revealed an interesting tenitorial activity of C. sma,ugdinus on hot days, although
pattern .As suggested by Tlakeuchi and Imafuku (2005b), I could not fin dmud-puddling indiyidua allosng my census
males of C. smarugdinus initiate dtheir territoria lactivity route.Contrary
lkantoewr onn ihno stotmeer d aoytshe (rF biug t5t.)e. Arpfpla i(reeBsnittlyz esainrmdil aSrha swhi,f t1s9 a9r5e; (2005b) t,om tahle essugdgeistdionnotd oefl Taaykteuecrhmii nanadt iIomanfoufkutheirtenitorial
Rtuhte bouwtstkei retf alt .is,he ifs1t9 t9h6e; Ti artkereruitcohrii a,2 la0c1ti0vi)t y.In ttoh ceosole erstu dtiiemse, activity on hot days ,However, they delaye dtermination
oftheirterritorialactivityonlaterdaysintheiradultseason.
zbaovunoeitsdte oirvenf rhhle oiasttteiotnspge, sretahsoe nHiso,r twee nvtiehterro,erf itoahr lieacs,t iiivnit tityse i rnapttr eherotptartt eeci ottr uotliednhmdaet s nt ohtteo SCo. msmear ucgldiinmuastic f aasc tthoer issne atshoen e vpenrionggr emsigshet tso gmeidt sbuemmtetr,e fror
be applied to the case of C. smaragdinus becaus emales The present study provide sa unique patter nbetween
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Temperature effects on butterf iayctivity 171
territorial activity time and air temperature in butterHies， Kuno ， E、，1992、 Competitive exclusion through reproductive
This finding indicates the existence of mechanisms other interferen， cRees． Poρul． Ecol．34：275−284，
tshhia食n sr eignu ltaetriornit oQfrbio daaylctiv itteymp etirmaetu orfe tbhuatt utnederrHlii．ee Is s esausgogneaslt N i shiunodkera， grNow．t，h2005， ．CRr「eucdoer 4d9s ：o2fT4h−ec3l1in，i〔ln JIaapnadniens goe）n a ground or
tidtoaflhhniCm aeodd s tm tnaaaoli te∫cl覘 h n yoarr αetnef毋 egpdenerraiogttd ゴotuiaど rcoo欄nit f aiae lftv 5d e偽a hwcaeetc ri itfeavsliec tytmfyo irfaeva ripletetaled hyyati ectt tn ifei svgmtmeieetie．mny mT．a ehI ．l i iOnme ns fata tyhci hctesoei bu vp crifesatrceiyueaseseu l tsep， d heaanan e t fdt sctfethe euamIrd nmayn hgaolea，n ledIes R R uDt eovwebsfChvalkuootrirotmti aptpp：s，t〃 metuiR月awoerttwn．yniiwLst nt（iA g孟，Cnsc．M， RoamtlVra−，e tipeJercer，oronqDm−ceepnilaaumaeotmlm，i ccop，nA．tango2aur gt0sgti1te！ n 2rai．ng a．idlRRαai．； ： iaIBLAFvSeo．liBpuTatnNie nydridg akno3 utap−tina9thoig0eneae 0nr da：0 ，aenNdf51syo19e rem9−rn 06pv tS7ihh，t raa−Sao0ncltemi，ki aesnUbdsttReaoiLrenc）raa．lyl
aaccttilvvilttyy ppaatttteemrn ，may have an ef飴ct on male reproductive Tak eu∫chiIn，s Tect，． 2B0e0h7（z． レE．c9o：l9og2y1＿ 9of31 C．hO ，sozephyrus smaragdinus ．
Daikon． Crude 51：40−43．（In Japanese），
Acknow 且edgments Takeuchi，T ，2010． Mate−locatin bgehavio rof the butterf iLyethe
diana （Lepidoptera：Satyridae）：do males diurnall yor
This work was partl ysupported by a Grant−in−Aid for seasonally change their mating strategy ？Zool． Sci，27：
Scientifi Rcesearch from the Japan Society for the 821−825．
Promotion of Science（JSPS）Research Fellowship for Takeuchi， T、 and M ． Imafuku，2005a． Territori ablehavior of
Young Scientis．ts 跏J．Rvoeπs．∫ κL∫e燃pidだ．α38（L；y5c9a−e6ni6d．ae ）：territor ysize and persisten．cy
Takeuchi， T and M ． Ima釦ku，2005b． Territori baelhavio rof a
References green hairstre aCkh［ソsozephyrus smar αgdinus （Lepidopter：a
A B B meil ctskzgef，bma， it ，dr oenKJmaeRr．hri ua．p，r ．al，c asuREJuvlFd．s i． eadMo． n，e l？dUrnS ViiyhcO annKlie ngbee tc．e eanrnC∬onhobcdl，pa αee o iSv1Rrgcahi8gtai， αao5a lC lw ar：b1anb． 3，n1dyLut79 ］eatt 29di；tKe9−ge1r35e，（4 rhLr．7 0FosfeT4w−uiiepas．e1rliie：4lrdede8iliwso，tt，en po1a，risrt9le1i7ea9a4rr 9lcb ，a： bh9eSNuh，o aytdMovmtfiuipedou hrprmafr −；olipofst，iuitht Pedideemdaasiulplen iu ir）nsseoldgr1i．o T W aik ce u2eiiocLff2hnnyfw aiceae：anc aa 9h，tte l， h8iTn yeoP9lir fc−−dlara0ane9tdsee．9oj na d）4p1nKei：．dpn 9dcbs． i8 y iHubmtn8eoatug．ln tte dDtedetaexeyrnpenaaesfrc，in． lift2酒Ea，tyy lh0ytmeya0nhi cs9ocae． ni，lsZdE ooooaomon gfr〃lw y altl．rlmy seaaJlt trec．‘ 5ro1 Lmi：〃ioetf7−tnrose sn6egra7aeti． trr −Sra ccaib7loohtinie7co（tnnc3Leg．s9o．，t）3m． ：：eZ btd3ohe yooe5hwn 7nca’fae−，f vrem3Ssciti7csoci7us，：，r
The role of climatic 飴ctors and ear且y interacti fornequency
on territori asltart time． J．ノnsect ． Behav ．8：47−66， 摘 要
Fischer， K． and K． Fiedle，r200LResource−based territoriali tiyn
thebutterfly 正．ycaeua hippotho eand environmentally induced メ ス アカ ミ ドリシジ ミ （鱗翅 且 シジミチ ョウ科）で
behavioura slhifts． Ani〃t． Behav．61：723−732． 発見された，気温 と繁殖活動の独特な関係 （竹内 剛）
F H Hrao imnbadeaccOor，r s，uyY g，K rpattM，ksi，2，hcaiH0．． ，p 0bC． 0T2u厂，a ．．t u dmEkteLincaeeo．rog riei4tlf，my6 oHlas：gypr．ey1 Oc0 oaimefn−effdufse1ercm4 taC．as．l丿e〔 ，L sla nWEnda lnソJ kdaooHflp’ T，．au nhHBnienoeccidhlsnoei，ednt2．i ）a20s，6e12p ：3aa0rt．9 1a M7Ht2ii1e，Q −yPtn9aie’o7mr c9auobr．see， mptNeewontces且ieecn， チ縄けはる張，るこョ気．ウりと温メの活がスが動分よア高かうにカいな気っミ日変温たドほ温が．リど一動与縄シ見物えジ張類のるミ似活り影C活動h響しr動yたはをsoをパ，調ze気開pべタh候始yーたruすのsンと影るは こsm響時a，rろ刻をク，α大本がロgd種遅ヒきinのカくuくs受の雄ゲな
of exogenous ammonia by the swallowtail butterf，i Pyapilio Lethe dianaやA5斟ηc卿 ρα姻 如など他の種で も報告されて
p八oiとlzyttunevsi，s sfenosrc hparfioetnein b9i9：o6s9y5n−t70h3e ，sainds sperm production． おれてり，い暑るい．し日かにしは，気メ温スのア高カいミ時ド問リ帯シをジ避ミけでて見いらるれとた解パ 釈ターさ
I d e，」t． hYe s，a2ty0r0in2e． bSuetatseoMnyaIl cxhrantg hedseian ia na rteh mee dtieanteidtor bjay l tbeemhpaervaitour roef． 比ン較に的は，気こ温のの解低釈いは10適時用かでらき1な2時い ．になはぜ活な動せら，ず暑，い一・日円にのは最
」．Ethθ1．20：71−78． 高気温が記録される12時から17時に縄張り活動が見られ
Kemp ， D． J．，2003．Twiligh tfighti nign the evening brown buttedi，y るか らである．この ようなパ ターンは他の種で は知られて
Melanitis teda（L ）（Nymphalidae ）：age and residency ef飴cts． い ない ．本種は，暑い 日の午前中に地．ltに降りて口吻を伸
Ko daB， eNh．a，v1・9E8c2o．tO． bSsoecrivoa巨biono．l o5n4 ：th7e− m1a3，盈e actjvity offive Japanese 摂ば食して行い動るのパこ とタがー報ン告が変されわてり，いそるれ．そが縄の張日のり気活温動がに行よわっ てれ
species of zephyrus hairstrea， kwsith special reflectance to る時間帯に影響するのか もしれない ．
the inHuenc eofthe hght intensit（Lyepidopter， aLycaenidae）．
乃∂Gα33：29−39，（ln亅apanese with English abstract ） （Received October 24，2013． Accepted November l4，2013）
一
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