Brooding by the female is not required for the normal growth from eggs in the butterfly Hypolimnas anomala

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axY.va 7Lt'anst.epidS.oc..lapan59 (])4:9-54, Januttry2008

Brooding by the female is not required for the normal growth from eggs in the
butterflHylypolimnas
anomala
Masami SHiMAzAKi±i･ ) Yti. IjRiTNo 2a)nd Minoru KANEKo"'
,
i'Matsunami-cho440-114,Takasago-choT,akasago,Hyogo.676-O023japan

]'Kabira12l6-265,Ishigaki,Okinawa, 907-0453Japan

"iU{sukushigaok1a-5-1A,oba-ku,Yokohama,225-OO02Japan

Abstract An unexplained behavior of the butterfi yH>volimn aanbomaia has been observed occa-
sionally in the subtropical Yaeyama Islands ot' souLhem Okinawa, where the female stays with her
egss on the leaf of the food plan tafter oviposition. On the islan dof Guam Nafus and Schreiner
(1988 r)eported that some e.eg masses of this species deve]o pnormal]y ",ithout guarding b} ,thc fc-
ma]e. However, in the absence of such evidence in Japa- it has been accepted that without guard-
ing by the femal ethc cggs cHnnot hatch ur thc fir sitnsta ]rarva ceannot gruw if lhe.v hatch .XNJ eear-
lie rreporzed on a case where all eggs hatched norma]iy and grew to adu]t butterfii ewisthout fema]e
presenc ein the fiel dS.ubscque- tstudics rcpoTtcd here confirm the findin tghat the protecti oofn
eggs by the 'fEenmga]e is not always necessary for the hatching of cggs er thc growth or newly hatched
larvae ,]eav the female behavior unexplai ned,
Key words Butterl lHyr,,polimn aasnoinala, mtttemal care, Pipturb carsboresc'ens, Yaeyama is-
lands.
Introduction
H>polimnas anomala (Walla cies )a nymphaline butterf lofy the Old World tropics, known
to straggle to northern Australia (Common, 1978) in the southern hemisphere and to the
seuthern island sof Okinawa (Fulcu deat al., 1983: 306) in the northem hemisphere,
Although it i,s considered to be a rare migrant to subtropical Japan ,H. anomata (Fig .1) has
been recorded at leas t60 times (4 1females and 93 males) on the Yaeyama Island osf south-
Okinawabetween1986 1994 food hasbeen fre-
ern and and oviposition on plants observed
quentl y(Shoj i1,995: 253-255), The female of this species is known to remain on the leaf
of the food plant Pipturus arborescens (Urticace aafet)er she has lai da cluster of eggs
(Fukud aet al., 1983: Hama, 2001). Nafus and Schreiner (1988 )and Schreiner and Nafus
(1991 )reported that the guardin gof eggs significantly increased the hatching rate of H,
anomaia on Guam though it was normal for some egg masses to develop successfu11y with-
out guarding ,On the Yaeyama islands ,however, it ig generall yconsidered that maternal
care is necessary for the hatching of eggs and healthy growth of the newly hatched larvae
(Shir6 z2u00,6: 200-201) .There is some evidence ofparentul care in this species for suc-
hatching by Hama (2001f)ound
cessful of eggs either maternal protectio nor stimulation.
that when the female died after layin gon the ]ea fQf a potted food plant in his laborator iyn
Osaka, almost all the eggs failc dto hatch and the few that hatched could not survive. We
report on our case studies to throw light on the function of the female in staying with the
eggs after oviposition.
Materials
and methods
We observed the fat eof thre eegg batche sof H. anomaZa without attendant femalcs ,as well
*'Con'esponding authur/ [email protected]
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and
as observing the post-laying behavio rof females .In Case 1, we foI]owe dthe development
of eggs on a lea fwithout female presence in the fal lof 1999, The leaf with the egg batch
had been torn off in the wild on Ishigaki Island ,and was brought back int othe laboratory
fbr rearing. In Case 2, we observed a fomale layin ga cluster of eggs on I'ipturu sar-
borescen sin the fiel don Ishigaki Islan din the fal lof 2001. As the female disappeare adfter
oviposition, we wrapped the lcaf with eggs on it with thin cloth to preveR tthe attack of par-
asites and predator s.The sleeving was kept until the hatched larvae grew to pupate in the
field .In Case 3, we removed the female protectin gher cggs, and reared the eggs on the leaf
without female presenc ein the laborator iyn the Kabira Distric tof Ishjgaki Island,
Results
1, Hatching of eggs and growing of larva ewithout female presence
Case 1: A cluster of eggs on the leaf of the fbod plan t(P ,arborescens) was collected on
Ishigak Iislan don September 17, 1999. In rearing the eggs in the laborator wye divided the
cluster into two batches ,One batch (abo u1t50, Ishigaki group) was reared on Ishigaki
Islan dand the other (abou t50, [kLkasago group) was taken to [Iletkasa gCoity of Hyogo
Prefectur eT.he Ishigaki group hatched and, although some cannibalism occurred, most lar-
'few
vae grew to adult butterfli ebsy October 20, In the Takasago group a eggs hatched but
all larva edied without feeding .The temperature in the laborator ayt Takasago City had
been kept at 200C or slightly higher during the observation,
Case 2: (A case previousl ryeported in par t(Shimaza kanid Kaneko, 20e2)) ,We found a fe-
ma]e starting to lay her eggs on the underside of a lea fof P. arhorescens (Fig .2) jn the
Kabira Distri cotf Ishigaki Island on November 13, 2001. She laid about 200 eggs taking
approximately three hours and took up the well-known brooding positio nto stay en the
leat 'I.n the middle of November, the fiel din the Kabira Distric twas exposed to stormy
conditions with winds and rain, in which the dail yminimum temperatures ranged from
17.8eC to 200C. The female kept her positio nover the eggs (Fi g3.), enduring gale-fbrce
winds til ]November 15. 0n the next day, however ,we could not find the female ,either on
the leaf or nearby, and she never returned. Wk) took the opportunity to protect the eggs by
covering the lea fwith a sleeve made of thin cloth, and fbllowe dthe fat eof the larva ewith-
eut female presence in the field,
All eggs hatched normally on November 23 (1 1days after egg-laying), and the newly
hatche dlarva ebegan to feed on the leaf .On November 27, after 2 days of rest, all 1arvae
shed thei rskin to become the second instar ,The number of larva ehad decrease dto about
150 due to cannibalism. The dail yminimum temperatures ranged from 18,50C to 22.80C
during these 5 days. They molted to the third insta ron December 1, after 1 day's rest (2nd
insta rperiod :4 days) ,and to the fourt hinsta ron December 6 (3r dinsta rperiod :5 days).
They final] ymolted to the fu11y-grow nfift hinsta ron December 12 (4t hinsta rperiod: 6
days, Fig. 4). At this stage we separated them int othree batche swith enough fres hleaves
to complete development and each batch was newly sleeved (Fig .5) ,The fiel dtempera-
tures decreased to 15,40C and 15.8DC on December 14 and 15, respectively. Despit ethe
lowered temperature, all larva econtinued to feed and about 80% of them showed signs of
settling down to pupate on December 17. They all pupated on the fol]owin gday, On
December 20, 80 pupae were observed either on the underside of lcave sor on twigs (Fig.
6) ,Thereafte rco,oler days ensued with dail yminimum temperatures ranging from 11.90C
to 14.00C .However, adult butterfl ieemesrged from 80% of the pupae on January 4, 18
days after pupatio nand 53 days after oviposition.
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a 1
Fig, 1,FHi)gp,otimnas anomala: (a )rnale, (b )female.
2.FAi gf.emale H. anomala tayin geggs on the underside of a Pipturu asrborescens leaf.
3.FAig f,emale shielding eggs from strong winds.
4.FFiogu,rthinstarlaryae.

5.FSilge.eve sused to protec etggs in the field.
6.FPiugp.ae on twigs of the food plant.
7.An ant attacking eggs brooded by the butterfly,
Case 3: (repe aobtservations of Case 1 and Case 2). On October 9, 2006, we repeated the
Case 1 study jn the Sokobaru Disnic ton Ishigak Ijsland .We removed about half the num-
ber of eggs immediatel yafter laying ,and reared them in the laborator wyithout femal epres-
ence, They hatched on October 13 and the larva eshowed signs of settling down to pupate
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and
on October 28. Adult butterfl iemeesrged on November 15 from all pupae. Repeat observa-
tions of Case 2 were made on Ishigak ilsland from June to July in 2005 and again from
October to November in 2006, when the female disappeared from the leaf ,However, the
eggs hatched normally and the larvae grew to adult butterfl icoemspletely without any pro-
tection bythe female,

2, Behavior of the fema]e to protect her eggs
On November 18, 1999, we investigate dthe pessibili tthyat the female would retum to her
cgg batch and take up the original position to brood her eggs again if she was fbrce dto fiy
away, We removed a female from her eggs by forcin gher to fly away out of our sight in the
Komi DistrictIriomoteIsland, Okinawa.When 1.5hourslater,
of southern we returned we
cou]d cenfirm that the female had returned tmd continued to brood her eggs on the original
leaf,During
our fiel dobservation we recorded the guarding behavio rof the female on video, the
resulting sequences suggesting that the female actively attempted to protec tthe eggs from
parasiti cfiie asnd wasps. The female covered thc eggs with her wings and flappe dthem to
turn the parasit eaway. Tn spite of her threatenin gflappin gbehavior a,ll eggs were taken
away by predatory ants on one occasion (Fi g7.). We found that about 50% of fully-grown
larva ehad been attacked by the parasit ifciy Conrpsiluiz ;concinnata in the fie] don Ishigaki
Island .Although it is uncertain which stage was attacked, the fac tthat the eggs were para-
sitised implies that guradin gby the female was not very effective.
Discussion
Daterna lcare occurs rarely among insect sb,ut is found in several Orders ;e, g, the bug
Eiasm"cha signoreti (Kudo and Nakahira, 1993) ,the lea fbeetl e(}oniocten jaqponica
(Kubo and Ishibashi ,1995) and the sawfly Cephalci aisshik i(iKudo et at,, 1992) .Among
the butterfli etshe female H.vpoiimnas antilope (possi bHl. yanomata) of Leyte Islan d(the
Philippines )has becn observed to brood the eggs on the food plant R)Ltzolz -sipa.
(Urticace aweit)hout being able to preven tattacks by ants and hymenopteran parasites
(Anon. 1,979), The brooding behavio rof H. aizomala on the food plan tPiptL{ru sai:genteits
has been studied extensively on Guam (Nafu asnd Schreine r1,988; Schreine rand Nafus,
1991) .They followe dthe development of 282 egg masses, a half of them guarded by fe-
males and the rest unguarded, over a perio dof 19 months, They found that the guardin gof
eggs significantly increase dthe percentag eof eggs hatching from 47% to 669, and that pre-
datio nby ants and other insect swas greatl ydecrease dwhen the eggs were guarded, Wc
made a fiel dsurvey of female sof H. anomala remaining on the leaf of the food plan t(P .ar-
bore,s'cen sa)fter oviposition tM death in the Yacyama Island s.We had several opportunities
to observe cases where a female disappeare fdrom the lea fafter laying ,The fat eof the eggs
without female presence was fbllowed in thc winter of 2001 to 2002 and again in the sum-
mer to fa1 1of 2005 and 2006. In all cases the eggs hatched normally without female pres-
ence and grew to adult butterfl isuecscessfuIly in the field even during the winter, Females
always remained on the leaf until the larvae shed their skin to becomc thc sccond insta rand
this perio dwas longe rthan that reported by Nafus and Schreiner ( 1988),
Nafus and Schreine (r1988 o)bserved that the female did not fl yaway in response to distur-
bance but that she did not return to the Ieaf if she lef tthe leaf at any time during the brood-
ing period. In our observation the female could be forced to fi yaway but she returned to
broodher
eggs again when safe.
We cannot explain why wc could not rear eggs collected on Ishigaki Island and taken to
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Takasago City (Cas e1) .As the rearing temperature at [fakasag woas kept at or above 200C
during the observation, which should have been high enough for normal development, there
may have been other factor isnfiuenci ntghe development ,Ishigak (i2004 )reported on suc-
cessfu1 rearing of eggs taken away firo mthe attendant foma]e on Ighigak Iisland .The larN'ae
were reared on the food plan tBoehnteria niphonivertt (Urticacc aaet )Taichi-cho in
Wakayama Prefecture .This seems to be the only successful case of rearing this species
away from the Yaeyama Island sin southern Okinawa.
In conclusion, xly' esuggest that the presenc eof the female en the food plant after layin ghcr
eggs is not always necessary or essential for the hatchin gof the rested eggs or normal
growth of the larvae .Thus the behavio rof the female in staying with her eggs, suggesting
materna] carc, remains a mystery and requires furthe rstudy.
Acknowledgments
We are indebte dto the lat eDr Takashi Shir6z ufbr pointing out the uniqueness among the
butterfl ioefs the behavio rof the female Ilypolimnas anomala and to Professo rMyron
Zaluck iof School of Integrati vBeiology ,the Universi toyf Queenslan df,or his useful com-
ments and advice on an earlier draft .We are also gratcfu 1to Emeritus Professor Jiro
Kiklcawa and Dr Gcoff Montcith for their advice on the literat uarned editorial assistance
and to Mrs Yinmi Esterii nfeor her help with the preparati oonf the manuscript.
References
Anun,, 1979, Femalebutterfly guardin geggs. Anten,z 3a: 94.
Common, I. E B., 1978, The distincti obnetween H.)'polimna santi.lope (Crame ra)nd ll. anoinala (NN'altace)
(Lepidopt eNrymap:ha]idae), and the eccurrence ofH, anomala in Australia .Aust ent Mltg. 5: 41-44.
Fukuda. H..Hama, E.,Kuzuya, T.,Takahashi,A.,Takahnshi,M.,Tunaka, B,,Tanaka,H,,Wakabayashi, M.

and Y, Watanabe, 1983. 7V!e Life Historie sqfButteijlie sin Jc{l) a2n. 325 pp. Hoikusha ,Osaka ,(In
Japanes eand English),
Hama, Y., 2001. An obsen･'ation on the ecology of H.LvJolin't nanaosmala. Choker rFietd 16 <4) :28 (in
Japunese),
Ishigaki ,S., 2004. Successf ui1'earing of Il)potin'tn aansomaia on Bochmeric ntiphenivera. YZidorig a(202):
53-57 (i nJapanese with English summary).
Kudo, S, and E. Ishibashi ,1995. Notes en maternal care in the ovoviviparous leaf bectl eGoiltiocten Ja'aponica
(ColcepL±: cCrhir>･somclidac) .Can. Ent. 127: 275-277.
Kudo, S., Macto, K, and K. 0zaki ,l992. Maternal care in the red-headed spruce web-spinning sawfly,
Cephatcia isshikki (iHymenopte rPaam:philiidae) ..L Insect Behai, .5: 783-795.
Kudo, S. and T. Nakahira ,l993 .Broodin gbehavio rin the bug Elasmucha signoi'eti. Ps.v･ch 1e00: 121-126.
Nafus, D. M. and I .H, Schreillc r1,988, Parcnta lcure in the tropica] nymphalid butterf lHy),7)olimn aasnont-
alct. Anim. Behav. 36: 1425-143 1.
Shimazaki, M and M. Kaneko, 2002. Report on the eco]ogical survey of II)tpotimna sanomata (1) .Choken
Field 17 (6) :9-13 On Japanese).
Shir6zu, T,, 2006. The Standard Guide to the Japanes'e Btttteifli e3s3.6 pp. Gakushu-Kenkyush aT,okyo, (ln
Japancsc).
Shqji ,Y. (Ed. )l,995. Species Index. Jiiel dData-77te Index to Chvken Fietd Vots, J-9: 253-255 .Choken-
Shuppan,Osaka.(InJapanese).

Schreiner ,I, H. and D. M, Nafus, 1991. Evolution of suh-social behaviour in the nymphalld butterfly,
H.)polimnas Ecol.Ent,16:261-264.
anotnala.
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摘 要
ヤエ ヤ マ ム ラサキ の母蝶 によ る保護は卵か らの 正常生育に必須で はない （島Mf　iii一F美 ・入野裕
・
史 金子　實）
石垣島や西表島な どの八重山諸島で は，偶発的に発生するヤエ ヤマ ム ラサキ （H），potimnas　anomaJa ）の
母蝶が，産卵後の孵化か ら幼虫が 2令に成長する まで ずっ と葉裏に とどまっ てその ままの姿勢で死ぬ
こ とが多い とい う特異な習性 を示すこ とは広く知られて い て，日本で はその母蝶がい なければ全 く孵
化しない とか，例え孵化して もその後幼虫が川頁調に成育で きない と信 じられてい た．この蝶の上記習性
一
に関 しては，Nafus とSchreiner（1988）が，グアム島におい て本邦と同 ではない餌植物で発生 してい る
ヤエ ヤマ ム ラサキに関する生態研究結果を報告してい るが，本邦における母蝶に関する報告例はきわ
めて少ない ．筆者らは2001年から2002年にかけて卵保護状ー態にあっ た母蝶がい なくなっ たあとも正常
に蝶にまで生育できた野外観察結果を報告 した（蝶研フ ィ ル ド，2002）が，NafusとSchreineにrよる報
告とはい くらか異なる知見を含む複数の野外観察事例を追加して，母蝶がい なくなっ て も卵から蝶
まで正常に育つ ことは稀ではな く母蝶の保護が必須で はない との結論 を得た．ただし，本報告中で も述
べ たよ うに実際に母蝶の保護がない と正常に成育で きなかっ た例 もあり，母蝶が産卵後に葉裏に と
どまり続けることの真の 理由解明にはさらなる調査 ・研究が必要である．
（Accepted亅uiy　24，2007）
Publishe　bdy　the　Lepidopterologi　Scoacliet　yof　Japan，
5−20，Motoyokoyama2，Hachioji，Tokyo ，192−0063 Jupan

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