Effects of temperature on the development of overwintering pupae of Pelopidas jansonis (Butler) (Lepidoptera, Hesperiidae)

2009·0.62 MB·

TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society ooff JJaapapnan
eeLma 71uns.IepidS.oc,Jopan 60 (3)1:96-202,September2009

Ethcts of temperature en the development of overwintering pupae of
l'lelopitlasJ'anso(nBiustle(rL)epidoptHeersape,riidae)

TakenariINouE

Tarna Forest Scienc eGarden, Forestry and Forest Products Research Institut e(FFPRI),
HachiojiT,okyo 193-0843 Japan

Abstract Overwinterin ggeneratio 1narva eof Pelopidasjanson imsatured arrd pupated from early
October to mid-December with a peak in late Oetober/early Nov'ernber under outdoor conditions in
Tsukuba cit>J ,Ibarak iprefectur ece,ntral Japan .Overwinterin pgupae were reared under varkous
constant and fluctuatin gtemperatures superimposed on a photoperie odf 12L: 12D (12 h light 1:2 h
dark) or 15L: 9D. The pupal diapause terminated in January, The photoperiod did not have asig-
nificant efiect on the duratio onf the pupal stage, but the thermoperio hdad a significant effect on the
development of pupae. When pupae were kept under fluctuatin gtemperatures, the pupal period
was shorter than tha tat cQnstant ternperature scorresponding to the mean of fiuctuati tnegmpera-
tures ,especially under ]ower temperature conditions. The developmenta zlero and the therma lcon-
stant of pupae were 13.0-13.3eC and 158-16S day-degrees and 12.2-12.3"C and 171-173 day-de-
grees w,hen pupae were reared under constant and fiuctuati tnegmperature conditions, respectively,
Pupae may develop faste irn the fiel dby using this mechanism in early spring when the surrounding
temperature islow.

Key words Developmental zero, diapaii steermination ,grasslan bdutterfi pyh,otoperio dp,upation,
seasonal adaptation, thermal constant, thermoperiod.
Introduction
Pkilopidajsansoni(sButleirs)distributeidnKorea,NortheastChina Japan(Honshu,
and
Shikoku amd Kyushu). In most of the Japanese localiti etshi,s species is bivoltin ewi,th hi-
bernatio noccurring during the pupal stage (Fukud aet at., 1984b; Shir6zu ,2006; Chiba,
2007), In Japan, P, jansoni iss generally regarded as a rare species (Shir6 z2u0,06; Chiba,
2007), has been decliningin (TheJapaneseSociety Environmental
and recent years of
Entomology Zoology,199g;Inoue,20e5).P. is
and J'ansoni s recognized as an endangered
species in some prefecture osf Japan (Sunos aend Eda, 2003), although the species is not
liste din the National Red Data List (Minist rofy the Environment Japan, 2007).
Identifyin tghe physiologic aclharacteristics of an insec tspecies may otfer us basi cdata to
understand the causes of decline w,hich would be particular ulsyefu1 if the conservation of
the species is needed in the future .Although the lif ecycles in the wild have been clarified
for almost every Japanese butterf lspyecies (Fukud aet at., 1982, 1983, 1984a, b), the funda-
rnental physiological characters such as developmenta lzero and thermal constant are
known fbr only a few species (Kirit a1n9i97,) .The present study mainly reports on the time
of diapause termination and the parameters of the law of total efiective temperature (devel-
opmental zero and thermai constant) in oyerwintering pupae of P. janson isBa.sed on the
data ,the importance of thermoperiod to adult emergence in the spring is discussed.
Materials and methods
lnsects
Larvae livin gin tube-1ike shelters (Fukud aet al., 1984b) made of Miscanthus sinensis
NNIII-IE-leEcltreoncitcronic LMbirabrryary Service
TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society ooff JJaapapnan
Develepment of Peiopidas J'ansonis Pupae 197
(Gramineae l)eaves ,one of the major larva lfood plants ,were collected fror nfield sin the
southern part of Ibaral dPrefectur ec,entral Japan in October-November of 2006 and 20e7.
They were reared individual lunyder quasi-natur acolnditions; i .e. they were kept in trans-
parent cups (12 5× l25 mm at the base, 57 mm height )which were placed in a wire-mesh
cage (4 m2 × 2.5 m in height )in the fiel dof the Forestr yand Forest Products Research
Institu t(eFFPRI )T,sukuba City, Ibaraki Prefecture (36"OO' N1,40e08'E ,25 m a.s.1.). M.
sinensis leave swere provided as fbod, The development of Iarva ewas checked every 2-3
days until they pupated .Pupae were kept in the same cage until the start of experiments
conducted in winter.
Experimentalconditions
Pupae were reared at constant (17 ,20, 23, 25 or 28"C) Qr fiuetuati n(gcryophase/ther-
mophase=14120, 17123 ,20126, 22/28, 25/31 or 17129eC) temperatures superimposed en a
photoperio dof 12L: 12D (sho rdaty condition; 12 h light :12 h dark) or 15L: 9D (lon dgay
condition). [[Ih efluctuati ntgemperature was composed of 12 h thermopase and 12 h
cryophase. The midpoint of thermophase coincided with the midpoint of photophase. The
emergence of adults was checked every day and the duratio nof the pupal period was deter-
mined,rtme
ofdmpausetet:mination

Tb determine the time of diapause termination under natural conditions, overwintering
pupae were transferred from the outdoors to an incubato rmaintained at a rnean temperature
of 20 (17f23 O)C under either a short or long day condition. Mansfers were conducted seven
times from 26 Decernber 2006through 6March 2e07.

Developmenlal thermal
zero and constant
Incubatio nwas started on 28 January 2008. Pupae were kept at 11 diffbren tconstant and
fluctuati ntegmperature regimes under the short day condition ([fab 3l)e. The developmental
zere and the thermal constant were estimated by the conventional equation and the equation
proposed by Ikemoto and 'fakai (2000 ,2001).
Conventional equation: IID = - <ti k+) (1/ kT), k = 1rs, t = aus
lkemoto-Taka iequation: (D7) = k+tD, k = a, t =f3
where D, Z t and k represent the durati oonf development (days )e,nvironmental (mean)
temperature ("C )t,he estimated developmenta lzero temperature and the thermal constant,
respectively. Also, 6 and a represent the slope and intercep otf the regression line ,respec-
tively.
Resulbs
fime ofpuptmi ounnder quasi-natura clonditions in autumn
Pupae of P. janson iarse covered with a white waxy powder (Fukud eat al. 19g4b) .In the
presen tstudy, prepupae were aiso covered with the similar powder; thus larval maturation
was judge bdy the presence of the powder. Larvae matured and pupated from early October
to mid-Decermber with a peak in lat eOctober/earl Nyovember (Fi g1,) .The duratio nof the
prepupal period (larv maatluration to pupation )increased as the date of 1arva lmaturation
was delayed (Thbl 1e) .When 1arva ematured in October, the mean duratio nof the prepupal
period was less than 5 days. The las tpupation occurred in mid-Decemher after a long pre-
pupal period (mor ethan 20 days) .Eight larva ernatured in or after late November, but they
NII-Electronic Library Service
TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society oofJfap anJapan
198 Takenari INouE

Tuble1, Duratio] (d )of the prepupa lperio dunder a quasi-natural
condition, Three hundred seventy pupae obtained in 2007
were used for the caleulations.
Date ef maturationRangeMea/nVarianceNo, efpupae tested
before Oct. 20 2-7 4.54.7 5.1 6155145
Oct, 21-31 2-92TIO41912-26 2.7
Nov, L-10 6.3 1.913.S23.2
Nov.11-15 9.419.8 S2
Nov. 16-20 12
Table 2. Performance of oveTwintering pupae transferred from outdoor conditions to an incubato rregulated at
a mean temperature of 20"C (Cryophasellrhermophase=1 7f/r2om3 'DCe)c,ember 2006 through
March2007.12L:12D

15L: 9D Difference
D tar ta en s off e rNP ou .p a oef Ra:dautlt%er goefMnceeDuuTnda)etriioncnubat ioofn pupal period N go . x of U aRadauPtlte :oflu･ndenr ein cdouf b:pautp%iaol Mnpereio)dbert wtwgeoephneotthon-.peecrioeds#Duration
exami ned RangeMeantVariance Range Mean'Varlanee

Dec. 26Jan. 87781010613086868287940592019-023762,04-a22S31.6883-b.228121.70-b2,2c1169-.82670b81･76c1r10m912. 006g13b0,c18.22c91-76.17 e40.6e 171.3 NSNSNSNSNS
I5jan. 4,6 86100 22-34 24.7b 2i.5
25Feb. 3.2 21-35 24.3b 20.5
4Feb. 1.6 861.0020-22 20,7b O.7
14Feb. 3.7 18-22 19.7b 1.8
24Mar. 1.9 90 ]&30 21.4b 11.8 *NS
'i' 6 2.3 80 16--20 r7.9b 2.]
Means followe dby the same lette ramong the same phQtoperio dare not significantl ydifferen tlp>O.O Sby;
Tukey's HSD test).
# '': significantly (lifferent by t-test (p<O.05).
Tal)Ie 3. Pupal perio dunder various constant and fiuctuati tnegmperatures,
Overwinterin gpupae were transferre dfror nthe outdoors to an incu-
bator on 28 January 2008 and kept under a photoperio odf 12L: 12D.
Experiment Temperature(Oc) No. ofindividuaDlsuration of pupal period
under incubation
group Cryophase Thermophase examined Range Mean Variance
C17C20C23C25C271720232527 2026232S2354562C301339-.2412141.-91135781..008T1135.311.4
8.7

5.4
Ll

1.8
F17F20F23AF12431B7M250F127722220423262928301918232S22172-74517m23651.39-2313.1631-1719.8.11S115-.1661130.-311415
6.717.9

2.1
1.6

1.2
Means were siglli dilferen tbetween C20and MO and between C23
and F23B (p<O.0; 5byf it-ctaesnt)t.iy
NII-Electronic Library Service
TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society oofJfap anJapan
Development of Pelopitlasjanson Piuspae 199
Table4. Developmental zeros (t )and the total effective temperatures (k )for
emergence as adult jn overwintering pupa of P. janson iasfter dtapanse
termination estimated by the conventional and lkemoto-Takai methods.
Conventional methodlkemoto-Takaimethod
t("C) k(day-degrees) t(℃) k(day-degrees)
Constanttemperature' 157.5717e.9612.9712.20 164.79172.95
Fluctuat intem eraturet13,3412.31
"The results of F23B (Tab l3e) were excluded from the calculation.
i:
m12;12itlO
f
':
:t:
o
Fig, 1.Times of 1arva lmaturation and pupation of Pelopiclasjansoni sunder quasi-natura ]eonditions
in 2007 based on 147 !arvae collected on 3 October 2007 at one localit yof Ushiku-shi,
IbarakPirefecture.

diedbeforepupation.

fime ofdmpausetermination

When the transfer was conducted in lat eDecember, the rate of adult emergence was rela-
tivel ylow (63%) and the mean incubatio ntime to adult emergence (durat iofo nthe pupal
period) was more than 30 days under both short and long day conditions (Thbl 2e). After
mid-January, the rate of successful emergence rose to 80% or rnore. The duratio nof the
pupal period was shorter for late rstart of incubatio n.Under short day conditions, when the
t'ransfe wras conducted between lat eJanuary and early March, the duratio nef the pupal pe-
riod was approximately 20 days and means did net ditfe rsignificantly among the five
groups (by Tukey's HSD test ,p>O,05). Under long day conditions, when the transfer was
between March, the did differ
conducted mid-January and early means not significantly
among the six groups ,The mean duratio nof the pupal period under long day conditions
was slightly lenger than that under short day conditions on most occasions, but the means
under the two photo regimes did not dilfe rsignificantly from each other except in one case
(when the transfer was conducted in late February).
EOlect ofLi7uctu attemipnergature on pupal tlevetopment
The mean duration sof the pupal period of the F20 and F17 groups were 3.3 and 3.5 days
shorter than those of the C20 and C17 groups, respectively (Tabl 3e). The mean of F20 was
significantly differe nftrom that of C20 ip<O.O lby, t-test) ,but the difference between the
F17 and C17 was only marginally significant (p=O.05 1)Th,e mean of the F23A group
NII-Electronic Library Service
TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society ooff JJaapapnan
2oe TakenariINouE

(temperatu rranege was 60C) was nearly equal to that of C23, but that of F23B (temperature
range was 12"C) was signifi¢antly differen ftrQm that of C23 (p<O.05 )T.he means of F25
and F27 were nearly equal to those of C25 and C27, respectively.
Devetopmental thennal
zero and constant
The developmenta lzero Emd the thermal constant were 13.CP-13,3 "anCd 158-165 day-degrees
and 12.2-12.30 Cand 171-173 day-degrees ,when pupae were reared under constant and
fiuctuati ntgemperature conditions, respectively (Thbl 4e). There were few differenc ebse-
tween parameter sestimated by the conventional equation and those estimated by the
Ikemoto-Takai equation, especially when data obtained from the fiuctuatin gtemperature
condition were used for the calculation.
Discussion
The presen tstudy showed that the pupation of the overwintering generatio nof P. junsonis
takes place mainly in lat eOctober to early November in the lowlands of the Kanto region in
central Japan. A similar result has been obtained in [[bchigi ,the adjacent prefectur eto
Ibaraki (Kuzuya ,2000). Overwintering pupae are in astate of diapause. As diapause pro-
ceeds, insect susually show a progressiv eloss in their sensitivity to photoperiod ,and by
mid-winter ,photoperiodi csensitivity has ceased in many species <[[bu baenrd Tauber,
1976). Althoug hthe photoperiodi ccondition did not affect the development of overwinter-
ing pupae of P, janson iins any season, the diapause seems to have terminated by mid-win-
ter (lat Jeanuary) in the fiel dbecause the rate of successfuI adu]t ernergence be¢arne higher
and the dnratio nof the pupal period did not diffe rsignificantly after thi sseason under either
short or long day conditions.
Beck (1983 s)hQwed that deve]opmenta ]responses to thermoperiods (dai lcyycles of tem-
perature) vary among differe nitnsec tspecies. In some cases, developmenta lperiod sare
shortened by therrnoperiods (e ,g. Yamashiro et al,, 1998). For example, jn butterfli etshe,
developmenta lperiod (eg gto adult emergence) of Ndnathuva bazalus (lycaenid raeaere)d
under fluctuati ntegmperature was significantiy shorter than that under constant temperatures,
especially when the rearing temperatures were relatively low (Aso et al., 2006). Bryant et
al, (1999 s)howed that the development under fluctuati ntgemperatures (cryephaseXther-
mophase=10f200C) was faste rthan at a constant temperature of 15"C in fbur species of
Nymphalidae.
In the presen tstudy, the fluctuati ntegrnperatur ealso shortened the pupal period of P. J'ansonis
in some experimental groups ,As the mean temperature decreased, the accelerating effect of
fluctuati ntegmperature became more conspicuous, Moreover, under a mean temperature of
230C, a wide range of diumal temperatures hastened the deyeloprnent.
In most butterf isypecies, the developmental zeros are around 100C (Kirita n1i99,7; Kato,
2005), although there are some exceptions (e .g. Komeyama and Hoshikawa, 2007). The
developmenta lzero of P. jansoni psupae estimated by the conventional and Ikemoto-[Ihkai
methods was 12-13"C and thi sis slightly bigher than those in pupae of other Japanese but-
terfi yspecies.
P. janson ilisve sin sunny grass]unds and pupae sometimes pass the winter near the ground
(Fukud aet al,, 1984b) .At overwintering sites that are exposed to the direc trays ef the sun,
the range of diurna ltemperatures may be very wide during winter and spring (inou 2e0,08).
The accelerating effect of the fluctuatin gtemperatures may enal)le pupae to develep rapidly
after diapause termination. As a result, adults of P. janson imasy be al)l eto emerge ear]y in
NII-Electronic Library Service
TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society ooff JJaapapnan
Development of Pelopidosjunsonis Pupae 201
the thedevelopmental js high,
spring, although zero re]atively
Most Hesperiidae, Ryngus Leptatina
grassland species of e. g. maculatus, unicolor,
Pbtanthus flavu mand folytremi spetlucida, usually become multivoltine in warmer regions
but univoltine in northern or mountainous habitat s(Fukud eat al., 1984b) .However, P. jan-
sonis can produce two generations per year even in Aomori, the northem limi tof it sgeo-
graphica ldistributi o(nFukud eat al., 1984b; Shir6zu ,2006). Further studies are needed to
reveal the regulation mechanism of the Iif ecycle in P, janson iessp,ecially the larva lre-
sponse to photoperiod .Also, the effects of temperature on the development of more species
of butter[fi iine rselation to thei roverwintering sites must be studied.
Acknowledgments
I thanl (Mlr :K. Tanaka (Tsukub Caity) for teaching the cellecting method of P. .ian,soni s1arvae,
I also thank Ms K. Takano (FFPRI )for assistance with the experiment.
References
Aso, H., Inoue, T. and T. Koyama, 2006. Effect of thermoperiod on immature development of powdered oak-
blue ,IVtiruthu braazalu s(Hewitso n()Lepidopte Lryac:aenidae) .JLrp J.. mpl. Iint .Z)ol. 50: 241-246 (in
Japanese with English summary).
Beck, S,D,,1983, Insectthermoperiodism. Ann. Rev.Ent.28:91-108.

Bryant, S. R,, Bale, J. S. and C. D. Thomas. 1999. Comparison of developmen tand growth of nettle-feeding
1arvae of Nympharidae (Lepidepte urndaer) constant and alternating temperature regimes. Ettr .J, Ent.
96:143-l48,

Cbiba, H,, 2007. Hesperiidae. in Yata, O. (Supervised)Ib,onogmphia insectonim JaponicorumCotore

iVdturat iEdita 1: 130-144. Hokuyukan Co,, Ltd,, Tekyo, (I nJgpariese)
Fukuda, H.,Hama, E,,Kuzuya, T.,Takahashi,A,,Takahashi,M., Tanaka, B.,Tanaka, H..Wakabayashi,M.

and Y. Watanabe, 1982. TVie Lijl eHistories ofButteny 7iin eJsapan 1. 277 pp. Hoikusha, Osaka. (In
Japariese with Englis hsurmnay)
, 1983, TZte L(fe Histories qfButtenjIie sin Jtu,an 2. 325 pp. Hoikusha ,Osaka. (In Japanes ewith
English summary)
, 1984a. 77te Lijl eHistories ofButtei giln mipeasn 3, 373 pp. Hoikusha ,Osaka. (T nJapanes ewith
English summary)
, 1984b ,71I iLeij lHeistorie qsfButtei:17i eisn Jopan 4. 373 pp. Hoikusha ,Osaka, (l nJapanes ewith
English summary)
Ikemoto ,T. and K. Takai ,2000. A new linearize dformula for the low of total effective temperature and the
evaluation of line-fitt mienthgods with both variables subject to error. Envir. Ent. 29: 671-682.
, 2eOl. A new method for estimating the parameters of the law of total effective temperatures,
Shokubutsu-boek5i5:311-3l5,(inJapanese)

Inoue, T,. 2005. Causes of butterf idyecli, inne Japan ,Jap. J. Eit t(.N. S.) 8: 43-64. (i nJapanes ewith English
summary>
. 2008. A prelirninar ystudy on the overwlntering of Pelopidas mathias (Fabrici u(sL)epidoptera,
Hesperiidae) in the northeim Kanto region, central Japan. 7)'ans .Iqpid S.oc. Japan 59: 23-28.
Kato, Y., 2005. Hatsuiku reiten [Developmen tzearol]. In Honda, K. and Y. Kato (Eds) ,Cho no Seibutsugak"
[Biolog yofButtenj 719iee-s19]2: .To'kyo Univ. Press, Tokyo. (i nj'apanese)
Kjritani ,K,, 1997. The low development threshold temperature and the thermal constant in insect sm,ites and
nematodes in Japan .Misc. Puhts natn, 1its ta.gro-envir. Sciences (21) 1:-72. (i nJapanese with English
summary)
Komeyama, S. and K. Hoshikawa, 2007. Rapid growth at lower temperatures by the larvae of Celastrin saug-
itani i(Lepidopte Lrycaa,enidae). Ttzins .Iqpid ,Soc, mpan 58: 245-251.
Kuzuya, T., 2000. Miyamachabaneseser [iPelopid jaasnsoni s]in. Shin Tochigi-ken no Cho Henshu Iinkai
(Ed. )Bu,tteij7ie osfTbchi g(iNew Edn): 93-95. Insect Lover' sAssociatio Unt,sunomiya, (I nJapanese)
Ministry of the Environment Japan, 2007, [Red lis tof threatened wild animals in Japum: Insecta] .[home page
on the Internet] .Iupdat eAudgust 2007; cited August 2008]. AvaiIable from URL: http:ffwww.env.gojpl
(inJapanese)
pressfpress.php?sertal=864 8.
NII-Electronic Library Service
TThhee　 LLeepipdiopdteorpoltoegiroaollogical　 SSoooiceityety 　ooff　 JJaapapnan
202 TakenariINOUE

Shir6zu，　T．，2006．　The　Standard　qプB”tteiVlies　in　Japan ．336pp ，　Gald（en　Co ．，　Ltd．，　Tokyo ．（ln　Japanese）
Sunose，　T、　and 　K 　Eda，2003．　The　Red　Da重a　li重ss　of　bu韭terflies　in　each　prefectu，r　Jeapan，2002．肋 Sunose，　T．
　　and 　K 　Eda （Eds），　Decline　and 　conse エvation 　of　butterfii　esh1亅apan ，5．　 Ya【iori8a（spec ．1ssue）：1−169．
　　The　Lepidopterologi　cSaolciet　yof　Japan，　Tokyo．（ln　Japanes）e
Tauber，　MJ ．　and　C．　A．　Tauber，1976．　Insect　seasonality ：Diapause　maintenance ，　terrninatio　nand　post　dia−
　　pause　developmen．t、4ηη．　Rev．　E肛．21：81−107．
The　Japanese　Societ　yof　En嘘 onmental 　Entomology　and　ZoQlogy，】998．　 Cんo　no 　Shirabekata［ButterJ7y
　　Res砌 厂c乃Methods ］．288　pp．　Bunkyo 　Shuppan ，　Osaka ．（In　Japanose）
Y  ashiro，　C．，　Ando，　Y．　and　S．　Masaki，1998，　 Therrnoperio　dreduc 。s　the　tberrna　lconstant　req．Uired　for
　　oviposition 　in　the　leafbeetle　Atrachya 〃lan｛ltriesi．　Ent．　Sci．1：299−307．
摘 要
ミヤマ チ ャバ ネセ セ リ越冬蛹の 発育におよぼ す温度の影響 （井上大成）
ミヤマ チ ャバ ネセセ リの越冬世代幼虫の老熟 ・蛹化は，茨城県つ くば市の野外条件で 10月上旬か ら
12月中旬に起こ り，その ピークは10月下旬か ら11月上旬で あっ た．幼虫が 10月に老熟した場合には前
蛹期間は平均約5 日だっ たが，11月半ば を過 ぎて老熟 した場合には前蛹期間は平均約20 日になっ た，
越冬蛹が，12L：12D また は 15L：9D の 日長条件下の様々 な温度で飼育された．蛹休眠は野外条件で 1月
に覚醒 した．日長条件は蛹期間の長さにほとんど影響 しなかっ たが，温度の 日変化は蛹の 発育に影響を
与えた．変温条件で蛹が飼育された場合，平均温度が同じ恒温条件よりも 特に低温の場合に蛹期間が
短くなっ た．越冬蛹の発育零点と有効積算温度 は，恒温条件では13．0−13．3，℃ と158−165日度，変温条件
では 12．2−12．3DCと 171−173日度で，変温条件で発育零点が低か っ た．蛹は周囲の温度が低い早春 に，こ
の メ カニ ズム を使っ て 早 く羽化す ることがで きるだろ う．
（Accepted　January　8，2009）
P5u−b2l0isMhoetdo　yboyk　tohyea　mLaepid2o，pHtaecrhoiloojgiicTaol　Skoycoiet1y9　2of−0　J0a6p3anJ，apan
， 　 　 ，　 ， 　
一
NNI工I工-EElleoetcrotniroonic　 LLiibrbarryary 　Service