Rapid growth at lower temperatures by the larvae of Celastrina sugitanii (Lepidoptera, Lycaenidae)

2007·0.63 MB·

TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society ooff JJaapapnan
ueLL[gk7irans,tepidS.oc.Japan 58(2):245-251,March 2007

Rapid growth at lower temperatures by the larvae of Celastrin asugitanii
(Lepidoptefryac,aenidae)"

Saki KoMEyAMA and Kazuo HosHIKAwA**
Division of Environmental Ecology, Facult, yof Life and Environmental Scicnce S,himane Univcrsity,
Matsue 690-8S04,Japan

Abstract Celastrin asugitanii in the San-in Distric tof Japan is a specialist dependin gon flower osf
Aesculus turbinata, A ficl sdurvey carried out in Misasa, Tettori Prefectur eduring 2003-2005 indi-
cated that they laj deggs in ]at eApril .In late May the mature ]arvae lef tthe host tree and fe1 1to the
ground surface, as was demonstrate bdy more than a hundred 1arva ecollected with littcr-f atlralps
under the host tree .The perio dfor cgg and larva lstages in thc field was thus estimated to be ca 36
days. Rearing tests under differe tnetmperature conditions "8, 2], 24, 27"C; all 16L8D) in the lab-
oratory revealed an extraerdinary developmental zero point of the ]arvae ,-O.9'C ,despit oef a nor-
mal value of 7,8"C for thc congeneric C, argiotus, The extrcme value, eaused by rapid larval
growth at lower temperatures, should imply a climatic adaptation devclope din C. sugitanii which
needs to accemplish almost all it sfood ussimilation within a restricted flowerin pgeriod ofAeseuttis
turbinatainMay.

Key words Celastrin asugitanii, development azlero point c,limatic adaptatien, lif ecyc]e synchro-
mzat]on.
Introduction
Almost all Ceiastrin bautterfl ideespend on fiower sin the lanJa lstage, Within the genus in
which multivoltinism and polyphagy prevai lC,elastrina sugitanii Matsumura in Japan
(Fukuda
shows unique ecological trait sof univoltinism associated with virtual monophagy
rlb
et al,, 1984). understand how these traits have been acquired, some biologic af]eatures
of C. sugitanii were investigate din comparison with those of C. aJgioZus (Linnaeu sa) m,ul-
tivoltin eand polyphagou scongener.
Distinc ftrom multivoltine species in whieh inclusiv efitne sshsould be evaluated as annually
accumulative or as an average yalue, univoltine species in every generatio hnave to realize
sound fitnes sin a restricted period under changeable environmental conditions, Predictab]e
climatic variations in the temperate zone may continue to exercise selection prcssur eon
ecologi ¢al trait sin univo]tine species, and hence may develop some unique feature sin such
species. Here we report rapid growth at lower tcmperatures in larva eof C. sugitanii, which
should be an adaptation to cope with the sherter flowerin gperiod of the host tree, Aesculus
'Ib
turhinata, synchronize the lif ecycle with food resources can be a significant norm not
only in determinin tghe diapausin gperiod but also in the active period (Masak i19,80),
Materials and methods
Field survey
To estimate the larva lperiod in the fiel dn,umbers of adults and mature larva efallin fgrom
the host tree were counted in a populatio nat Oshika-ke iM,isasa-Cho, near Kurayosh iCity,
"Life cycles of the genus Cetastri nian Japan ,II
**Corresponding author. E-mail: hosikawa@]ife.shimane-u.ac.]p
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246 Saki KoMEyAMA and Kazuo HosH[KAwA
[[btto Prriefectur (eal tca. 640 m). Adult censuses were canied out from early April to inid
May with interva lo'sf several days, in 2003-2005 ,by two observers from 1O: OO-16: OO. As
the females tended to remain close to host trees, ditferi nfgrom the males, the censuses were
performed around a host tree .Some adults were collected in order to obtain eggs for the
fo]lowin grearing test .[[ bcount fallin mgature larvae w,e set 1arg eC`litter-fa11 traps" under
the host tree .The tree was 28 m in height ,1.55 m in trunk diamete rand covered 389 m2.
Eight sheets fOr agricultural use were extended (127 m2 in total area) and la-'a etrapped
weTe collected every second day during May 24-28, 2004.
Rearingtest

rlb examine oviposition preferenc en,ine females collected from the above fiel dwere al-
lowed to oviposit on flower sofAesculMs tt{rbinat aandlor Swicin controverts'a for a given
time in a cage (30× 30× 30 cm). Flower species offered were alternatively changed every
hour or unchanged for several hours ,Numbers o'f eggs laid were counted every hour .Eggs
obtained in the above oviposition choice test were reared in plasti cpetri-dishe splaced in in-
cubators each set at 18, 2I, 24, 270C (ai l16L8D), to determin edeyelopmenta lzero point
and thermal constant (=etfec tcuimuvlaetive temperature) fbr egg and larva lperiod .Fresh
flower sof A, turbinata were given intermittentl ays food, and hatch and mort were daily
recorcled. [Ib compare with the values of developmental zero point and thermal constant ob-
tained ,the third and fourt hgeneratio nofs C, argiolus were also reared in August-September
of the year under the same temperature/photoperiod condition but with fiowers of Pueraria
tohata.
Results
1 . 0viposition preference
The results of ovipositien choice test are given in Table ] and show obvious preference for
Aesculvt tsurhinata. In the alternative tes t101 eggs werc laid on floxNT eorfAs. turhinata
during 30 hours, whilc only one egg on those of Swida controversa. Even in the continuous
test two out of fiv efemale srejected the latte crompletely. The values for S, conltvversa in
the continuous test in Tlabl e1, where 47 eggs were lai din 1O trials ,might be overestimated
due to one female, who laid 38 eggs in 5 trial sand died the next day. Although females of
the population examined have a physiologic aplotentia lto utilize S. connvversa, it shouid
be seldom to realize under natural conditions, Indeed, we have never fbund any egg or
1arv aof the butterf lony flowers of S, controversa in the habitat.
2. Larva] period in the fiel dwi,th notes on the fa11in lgarvae
Figure 1 depict sseasonal fluctuation sin numbers of adults and falli nlgarva ein 2004.
Table 1. 0vipositi Qchnoice by 1'emal eCelastri nstatgitanii (]vTis paospualation).
Females allowed to contact the fiowe rduring one hour in each trial.
Flower species No, of tria]s No. eggslaidltrial' Females
offerred eggslaidltrials (mcan±s,d.) ttccepted
AlternativeAesculuh 'turhinata 13130 7.77±7.42 5/51154/4315O12
Swida c'ontrovenTa lf3013f2410f27 1,OO -5.77
ContinuougAesculustttrhinata 4.07
±
Svvid aconiro ve rsa 4.70±6.53
Wisteria,ftoribundd O/8
*trials not laid eggs are excludcd.
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Larval Growth in Celastrin saugitanii 247
2eoL=PasLoQ
leEo-.L<

90C
o
Aescu
608l$Do
4egB.-)Pt
2o

zd
o
UN
2004
Fig. 1. Annual fluctuation lsn observed numbcrs of adults and mature ]arvae cV' Celastrin asugitanii
in Oshikakei (a] t64.0 m>, Misasa, Tottori Prefecture ,in 2004 (below )F,lowering season of
the host tree, Aescutus tttrbinata, and change in air temperaturc estimated are also given
(above )A.ir tempcrature is estimated from that at Kurayoshi Meteorological Station (al t8.
rn) by reducing 3.6'C fbr altitudinal ditferencc ,See Table 3 and relevant text for meshed
area of temperature.
Adults began to appear from mid Apri1 and ceased in early May with a peak on Apri1 21 in
this year. The adult appearance varied annually, however ,and the peak was on ApriI 28 and
May 3 in 2003 and 2005, respectively, The peak of oviposition activity should be close to
the peak presence of females ,and was presumed to be on Apri 121 fbr 2004.
The larva ematured, at leas tmost of them, fel lfrom the canopy of the host tree Aesct-{tus
turbinata ca 25 m in height ,Flowers of the host tree were at their best in mid May and fell
in Iat eMay (Fig .1) .Although we are not sure whether the larv alef tthe fiower ssponta-
neously or fe1 1passivel tyogether with fa11in fgiower s(so-cal l"pearachduting"), a total of
114 larva e(96 of 4th insta r9, of 3rd insta rand 9 of 2nd instar w)as collected by "litter-fall
traps" mostly during May 24-28, 2004. Two out of 96 fourt hinsta lrarva ewere parasitized
by a parasitoi d(unidenti fTihecd f)ac.t that 94% (88/(96- 2of) >the 4th insta lrarvae collect-
ed pupated within the next day, at midnight, suggests their spontaneous fa11in gT,he ratio
also suggcsts a very low mortality due to the falling d,espite that a fallin sgpeed could bc es-
timated to be ca 9 mis or 30 kmthr (referr tio nragin drops with 5mm diameter ),The pres-
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248 Saki KoMEy.an{A and Kazuo Hosi{iKAwA
18212427 Cc
v
O.08
o
,07
g10
e x, .06 24D ?
10Fig. Cc o 5 10 IS212427 Oc
2.1E4gg periods (lcf atti)d Iam,a lpcriods (righ itn )days (D) of Cetastrin asitgitanii (blac hkar)
and C, aigiottts <ope nbar) under various temperature s(abscis sRae)g.ression line sof dc-
velopnienCal rate (VL Vdays) in relative to temperatures are shown with mean V valucs for
C. sugi.tanii (blac ckircle) and those ror C, af',gioliis (ope ncircle). Regression ot' 1arva lperi-
od of C. acgiotus was calcu]ated using three TLvalue sa,s slightly arrested growth was ob-
served jn 27eC.
Table2. Egg period and larva ]perio dof Celastrin abutterfii cisn days under
various teinperaturc ('C ).Photoperiod=16L8 DG.iven in mean ±sd (A).
Rcgression fbfinul aaere given below with correlation coefficient in
pareiithe siVlsl,ldays.
StageTemp.< sLtgitanii rearcd with C. ar. oi.olus rearcd with
℃)C.Aesculu, stturbinata Pueraria lobata
Egg(day1s8)212427 1 826,13234±2O7.52 (6) 6.61±O.50 (28)
4,OO±O.00 (5) 5.08±O.29 (] 2)
4.00±O,OO (8) 3.95±O.40 (19)
3.00±O.OO (9) 3.47±O.51(19>
Lurva(days) 21.75±O.96 (4) 22.60±1.34 (5)
19.00±O.7 1(5) 17,70±1.0 6(IO)
16.50±O.58 C4)** 14.25±1.16(8)
an1480 5 12.86 1.0ZgL
±
Regressions
EggLarva V=O.O]75T-O.1469 (O,948) I7LO.Ol55T70,1273(O.996)

VkO.O024T)-O.O02I(e.999)VLO.O0477LO.042S(1.000)*

"excluding a value of 27"C due to slightly arrested growth.
**two individua elmesrged without diapause.
ence of 18 immature larva esimultaneously collected, however ,indicate stha ta part of the
]arva eat least fe] 1passivel y[.Ib nof the 18 pupated later b,ut 4 of the 3rd insta rand 4 of the
2nd insta rdied under rearing, of which one and 4 larva ewere parasitize d,respectively,
Based on these observations, we estimated that the peak of pupation in the fiel dpopulation
should be on May 27 in the year.
These estimated peaks indicate tha tmost of C. sugitanii passed their egg and larva lstages
within 36 days (Apri 211-May 27) in the fiel cdonditions of 2004,
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Larval Growth in Celastrin saugitanii 249
OC)
Table 3, A comparison of devclopment azlero point s(Z, ; and corresponding thennal constant (K ;CC-day)
between Celastrin asugitanii aiid C. argioltts. Calculat efdrom data given in Table 2. Confidence
limit of 7h values (95%) "are in parenthesis.
Egg Larva
n K L K
C. sugitanii 8.38 (3,96112. 1457).5 (72.5f42.S) 412.4(423,2f401.9)
C.argiolus 8.19C7.1719.22 ) 64,4(69.3159.5)-O.8 87(,r8l2 .(468/.-6O2.3f08), 95)23S.2 (254,6f211.7)
"temperatures at which upperAower limit sof regressiun (959 bof confidence) across the axis VIO.
3. Effec tof temperature on egg and larva lgrowth
The period sof egg and larva lstage under various temperatures are shown in Fig. 2 and val-
ues obtained are compiled in [[lab l2e, with a reference to the closely re]ated C. ailgiolt{s.
For egg period ,though the observation interv aolf one day was coarse for the period of 3-7
days observed, both insect sshowed similar responses to the temperatures to which they
were exposed. Developmental zero points were ca 8,30C ,and thermal constants were ea
600C-day in both species, however, the confidence range of the developmenta lzero point
inC. (Tabl3e).
was vcry wide svtgitanii
Developmental zero point for larva pleriod was obviously diffk)re bnettween C. sugitanii and
C. argiolzas (Tabl e3). Although the latte srhowed a developmenta lzero point of 7.80C ,a
value similar to that of the egg perio d(calcula ftrionm gperiod sat 18, 21, 240C since slight-
ly arrested growth was observed at 270C), the former revealed an extraordinary develop-
mental zero point of -O.90C. Despit ethat C. s"gitanii spent larva lperiods 1.3-2. 2days
longe rthan C, argiolus at 21, 24, and 27eC, while at r1l8bebCl ethe larva lperiod of C. sugitanii
was O.85 days shorter than that of C, argiolus (Fig 2., 2), No arrested grewth was de-
tected in C, sugitanii even at 27'C, revealing a good linearit yin regression (Fi g2,). In C.
sugitanii, because of the low developmenta lzero peint ,the value of the thermal constant for
larva ldeve]opment became large rb,eing ca 4100C-day (Tabl 3e).
Discussion
The extreme value of developrnent zaelro point in C. sb{gitanii describe dabove may or may
not be caused by arrested growth in a wide range of higher temperatures above 21OC, since
the larva eof the species grow under lower temperatures in spring. This view, however, can
not explain the annual fiuctuati oobnserved in the fiel d(Fig .1) .If larva eof C. sttgitanii
grew at the same rate as C. argiolus, they should spend more than 39 days as 1arva eunder
the fiel dtemperature conditions given in Fig. 1, and the female swould have to oviposit in
Marcb! This is obviously not the case. Adopting the values of developmenta lzero point
and thermal constant for C, sugitanii obtained in tbe presen tstudy ([fa b3l)e ,the egg and
1arva pleriods can be predicte ads 16 days and 26 days in the fiel dr,espectively; eggs laid on
April 16 should hatch on May 2, and pupatio ntakes place on May 27 (Fi g1.) .This pheno-
logica lreconstruction should be corrected in thc egg perio dsince developmenta lzero point
for the period was not well detennine d(Tabl e3). Presuming the developmenta lzero for
eggs as 40C and the corresponding thermal constant as 72.50C-day t,he egg perio dis expect-
ed to be 11 days, hence for individua ltshat pupate on May 27 oviposition should have taken
place on Apri1 21 which coincides well with the fiel odbseryation shown in Fig ,1, below.
,
The value of developmenta lzero point ,-O,90C, in larvae of C. sv{gitanii is unusual within
butterfli e(sBryan ett at,, 1999; Kato, 2005) or even in whole insect s(c: Kfilritan i1,997,
2001; Ito ,1975), In a monograph compiling developmenta lzero point of 430 insects,
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250 Saki KobeTEyA.N auAnd Kazuo Hos}iiKAw,x
Kiritan i(1997 d)escribe dthe mean value of 83 lepidopteran species as 10.4aC±2,4 s,d, So
far as we are aware, developmenta lzero point at subzero temperatures is hithert oknown in
aphids, Macrosiphu, neuphorbiae in Canada (-0,03 "RCar:low ,1962) and Aphis goss.iv )inii
Japan (-O,4 0KCo:mazaki, 1982) ,and also a diptera nspecies, Delia flora l(-i2s,4' Cci:ted in
Kiritan i1,997) ,The presen tcase in a Cetastrina butterfi ymay or may not be biased since it
is estimated by a large extension of the regression lin econcerned (Fi g2.) . Confidence
limit lines of the regression (95%) h,owever ,cross an X-axis of V!O at -L480C for thc
upper limi tlin eand -O.300C for the lo"Je ]rimi tline .Data given by the presen tstudy expect
that for C. sttgitanii a larva pleriod of 26 days at 15DC, 32 days at 120C and 42 days at 9'C.
A futur eexperiment examining Iarva lperiod sunder such lower temperatures wi]1 provide
crucial evidence, Irrespecti ovfe the absolute value of the deyelopmenta lzero, rapid growth
by larva eof C sugitanii at lower tcmperatures should be true .We believ ethat in C. sugi-
tanii the distin cadtttptation has been acquired to utilize the seasonally restricted fiowe rre-
source ofAescul"s turbinata. Due to their univoltine lif ecycle with a long diapausin pgeri-
od, C st{gitanii in Japan have to accomplish a]most all food assimilation within the restrict-
ed flowerin pgeriod ofAescttl"s turbinata in May (Hoshikaw aand Komeyama, 2007).
C. sttgitanii might be bivolti nien the Koretm Peninsul a(Wakabayas uhnpiub,l.; gee Fukuda
et al,, 1984) ,and some non-diapausing pupae were also observed in the present study; out
of 4 indivjdua lresared at 240C, 2 adults emerged without diapause (Tabl 2e) and 3 adults
emerged from 12 stock cultures reared under room temperature (24-27aC )A.lthough such
was never observed at other temperatures ([fa b2)l, ethis exceptional phenomenon may sug-
gest the occurrence of non-diapause gene(s) in the population osf Japan .The species may
be strengthening (o rhave strengthened) the univoltinel monophagous trend within the
Japanese Arehjpelago. Severa lloca lpopulation osf the butterfl yutilize Swida controversa
and Phetlodendion amuiense as subsidiary hosts (Fukud aet al., l984) ,and utilizatien of
other leguminosi dhost sin some field wsas recently reported (rwaT eito al., 2006) .Tb un-
derstan dthe precess of host shift in the butterf lsyea,sonal restriction in resource materials
or climatic adaptation of the species should be of significance. Geographic variation in the
flowerin gperiod ofAescutus tttrhinat acould a]so strongly atiect the lif ecycle of the but-
terfly .We are now interest eidn the host utilization by population isn Hokkaido, the north-
ern boundary of the species; whether or not the flowering period ofA. tt{rbinata in southern
Hokkaido is sufTiciently long to breed the larvae of C. sugitanii.
Acknowledgments
We express our cordial thanks to Pirofesso Hridetosh iIwano (Niho nUniversity )for his kind
adyice in the presen tstudy and Dr Hideyuki Kawaguchi (Shima nUeniversit ywh)o kindly
informed us about the fa11in ogf the larva etogether with the phenQlogy ofAescttlets turhina-
ta, Mr Akio Tamura (Kurayo shCiity) ,and colleagues of our laborator yKensuke
Shinozaki, Hiroyuki Nakazono, Yinki Ishizuka, and Midori Yauchi kindl yhe]ped us in the
fiel dcensus, [[btto Froirestr yOffic eprovide dus various facilit ifeosr the presen tstudy.
References
Bryant S. R., Bale, J. S. and C. D. Thomas, 1999 .Compariso nof development and growth of nettle-feeding
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Fukuda, H., Hama, E., Kuzuya, T., Takahashi, A., Takahashi, M., Tanaka, B,, Tanaku ,H., Wakabayashi, M.
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Hoshikawa, K. and S. Komeyama, 2007. Sugar economy in diapausin pgupae of Celastri nsaugitanii
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Larval　Growth　in　Celastriαnsu8itanii 251
　　〔Lepidopte，r　Laycaenidae，，　with 　notcs 　on　their　cold 　tolerance．　Trans．　lepi，d　Soe．／ct」fan．，58：97一近04，
ltQ，　Y．，1975．　Aninial正「ω 1（丿g＞，．480　pp．　Kokin−Shoin　PubL　Co．，Tokyo ．（ln　Japanese）．
Iwano，　H ．，　Yamarnot〔，，　Y．，　Umelnura，　M ．　alld　Y ，　Hatakeyama ，2006．　Food　plant　sand 　host　plant　diversion　of
　　Calastrin　asugitanii 　Matsumura （L¢pidopter、　aLycaenida）ein　1he　southern 　KantQ　populatiQn，　 Trαns ．
　Kat　o，l　Yep．i，d2．　0S0o5c．．ノ7ap，a2n．5．，D5e7v：e3b27p−m3e3n4ta〔il　n　zJearopa．　lilne　sH　ewQn仙daE，　nKgl　iansdh　　sYum．　mKaartyo （）E．ds）．　Bio　togyげB“tte：itli，se：190−192、
　　Tokyo　Univ．　Pres8．（ln　Japanese）．
K　ir　itnaenl，ni　aKto，，de1s99　7in．　　JTahpca　ln〔．　｝wl　ld4ie．svce．　⊥Poupmわe’nst　Il　attThz、r　Iensshto，　lad　gtreoln−peenrviartu，r　cS　cain．d（　2t1h）e；　t1h−e7r2mal（i　nc　oJnastpaantncs　ie　n　wiitnhs　eEcngt，　lsmiisしhe　ss　uamlld−
．
　　Inary ）
　Ko　maz　aki，2，　0S〔，〕，11，9l8n2s．　ecEt　fafne．dc　C　tolsfi　tconnastta．ent17　7t　epmppe．　raSteuirezsan｛dm−oS　phooptuol　raPdluobnl　．g　Croow．，t　hT　ookfy　othr．e（le　na亅pahpiadne　ssepec＞i．es．　T〔）xoρiera
　　cintricidus （Kirkaldy），Ap’！li　scitricota 　Van　der　Gooz　and　Aphis　go∬）：pii　Glover（Homoptera ：Aphididae），
　Ma　saAkpi，ρ　S’．　．E，n1t98．　0Zo．　oSlu．m17皿1e7r5　−D8iaLpausc．　A．Rev，　Ent．　25：1−25・ ’
Rarlow，　C．　A，，1962．　 Developrnen，　tgurvival 　and 　fecundity　of　the　potato　aphid ，　Macrosiphum　evfphof biae
　　（Thomas ），　at　constant 　temperatures ．　Can，　Ent．94：667−671．
摘 要
・
ス ギタニ ル リシジミ幼虫の低温 ドで の 速い 成長 〔米11［沙希 星川和夫）
山陰地方の ス ギタニ ルリシジ ミは トチ ノキのみに依存してい るが，本種の生活史を解析する目的で 野
外落調下査すると室成内熟飼幼育虫のを行リっタたー．ト成ラ虫ッのプ発で生の消採長集か最らの野変外化でかのら産，幼卵虫時が期トはチ4月ノキ下旬を離とれ推る定のさはれ，5樹月下Lか句らと
計測された．採集された成熟幼虫のほとんどは直後に蛹化 した．これらから調査地（小鹿渓；三朝；鳥取
県中部）での本種の卵 ・幼虫期間は約36日と推定された．
異なる温度条件 （18，21，24，27℃；い ずれ も16L8D ）で トチノキ花を与えて本種幼虫を飼育 したとこ
ろ，その発育零点は一〇．9℃ と極端に低い 値とな り，そのため発育有効温量は412日度と大きな値とな
っ た．この発育零点は昆虫類全体の ritで も極めて低い 値であるが，室内飼育実験で得 られた温度発育速
度回帰か ら野外調査地における幼虫期間を予測すると約26 日とな り（当該期間の平均気温は約 15℃），
一
ll口問の卵期間を考慮すれば 野外調査 に基づ くE記推定期間とよく 致した，
同条件で クズを用い て飼育 したル リシジミ幼虫の発育零点は7，8℃ だっ たので，スギ タニ ル リシジ ミは
特異的に低温域にお ける速い幼虫発育を発達させたこ とが示唆される．これは まだ低温の春の トチ
ノキの限られた開花期間中に，ほとんど全ての 同化代謝を行わなければならない 本種における著 しい
生活史適応の ひ とつ と考えられ る．
（Accepte　dNo、・ember 　3，2006）
Publishe　bdy　the　Lepidopter〔〕oglical　Society　of　Japun，
5−20，Moteyokoyama2，Hachioji，Tokyo ，192−0063．Japan

一
NNI工I工-EElleoetcrotniroonic　 LLiibrbarryary 　Service