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Enhancement of Symbioses Between 血Lp lGt上 皿elJ 1990VO 川。 248, PP 1 104-11 ， s 三 C 互 ETqCE Enhancement of SymbiosesBetween Butterfly CateT 田打 5 川 d t5 も y vi も ra 丘 Qon寸 CO Ca 丘 On P ・ ) 、 DEVMES 山 p 川如 [ ｩ 1卯 Oby 山eAme iCanAs「 ， ぴニ石onfor 山eA 血狙 。 加 entofSdenCe A 2 寸6 II'll I" 11111『 W11111 A 0・ 44 0・ 46 0・ 48 0・ 50 Se ノ Ln 』ヰ B .02 十o 巳 2000 4000 咋市 Fig. 1. Waveformof the substrate-bome call produced by a fifth instar Thisbe irmea caterpillar. (A) An oscillogramtrace of two pulses of a typical Enhancementof Symbioses Between Butterfly cal1.A typical call consists of approximately 16 single pulses per second with an interval between Caterpillarsand Ants by Vibrational Communication each pulse. (B) An amplitude-frequencyspectrum showing the dominant frequencies of a typical cal1. P ・ ) ・ DBVMES Butterflycaterpillars produce calls that appear to play a role in maintaining symbiotic and rarely when at rest; previous observa ﾂ associations with ants. A survey of butterfly species from South and Central America, tions have indicated that the vibratory papil ﾂ NorthAme iCa,EUpope@Thaiiand@andA「 山 ， suQQest@that 小 。， bil@ヴ 6@forCat叫 u- lae are most frequently used at these times lars to call has evolved independently at least three times, and that calling may be w- ubiquitous among ant-associated species. Because ants use substrate-home sound in The calls typically consisted of a simple, their communication systems, this study points to the possibility that the calls of one repeatedpulse stridularion (Fig. 1). The insect species have evolved to attract other, unrelated species. mean pulse rate for the calls of 38 individual caterpillars (2-s segment per call) was 16.5 MONG BUTTERFLY CATERPILLARS, lars function as organs for producing acous- pulsesper second (SE, 0.45; maximum, the ability to form symbioses with tic calls, (ii) caterpillars unable to produce 21.7; minimum, 11.1). Slight variation in A 皿 L iS 卜 OW Ody 而山 C famjlies 。 川5 ぴe mF ， 卜 e。 My sho 帆 (O a血 a了 number of pulses per second occurred with- Riodinidae and Lycaenidae (1, 2). The na- fewer ants, and (iii) comparativedata sug- in and between individual caterpillars; this ture of these symbioses is that caterpillars gest that caterpillar calls have evolved at least was probably due to the variation in walking provide ants with food secretions in ex- three dmes, always as part of symbiotic speed of each caterpillar or the stress level Changeforp 山t<QeCddQn [email protected] i， donswlthants. whilebeing recorded. Analyses of 76 pulses use of analogous organs, caterpillars from Caterpillar calls of a typical ant-associated from 20 individual caterpillars showed a 山 o g「 oups may medlate 5ym 卜 lぴ Q h""id butternny, 川 M。 im 也 (7), we ， e mean dominant frequency of 896 Hz and with antS by produClng ammo acid and 5山田 ed on B OCOlorado Island,Panama, mean high and low frequencies of 1480 and sugar secretions or semiochcmicals(3, 4). and surrounding mainland habitats. Cater- 370 Hz, respectively (10). Studies indicate that if caterpillars are found pillar calk were detected and recorded by The ability to call was eliminated in cater ﾂ by 卜s pr 田 atow 小 Outm は， 山cy have 山山g a p Cl 。 V。 l山町 C ， Ophone 川 d pillars that had their vibratory papillae re ﾂ no chance of survival {1,2). Thus, there is a amplifier connected to a tape recorder, and moved{11). Except for their loss of cal1, premiumfor any caterpillarspecies involved the recordings were subsequently analyzed thesecaterpillars fed, oscillated their heads, in ， 田 M山 aaot5to malntaln a の n- forwaveform andf 「 equenCy 小打a 口 eriStiG 血 e， aQed 市山川 ほ ， pupated@and even 口d- I Cadpe ofant 四 れ山・ In ad山 a 川口 (8) ly produced adult butterflies. Because new secretory organs, riodinidcaterpillars that Third through fifth instar caterpillars of vibratory papillae are produced at each in- form symbioses with ants often have a pair Thisbe irenea all produced low amplitude star, the ability to call returned to all mute of nonsecretory structures termed vibratory calls (9). The calls were detectable within a caterpillars when they molted to the next papulae( 刀 wh 山emovementhasbeenspcC- 5- 口田山ノ山 e CatcT 山aT w卜 n 山c 卜5t ぴ・ Thus,eachln 山vidu 刃 a[epiM 卜 - ulated to convey vibrations to ants (4, 6). microphonewas in contact with the record- came its own control during the course of However, the functionof vibratory papillae ing substrate (8), or if held in direct contact the study. Those caterpillarswith only a has never been demonstrated. I report that with the caterpillar's body. When the micr0- single vibratory papilla removed all pr0- (i) the vibratory papillae of riodinid caterpi1- phonewas held1 mm away fromcaterpillars duced calls (11). Vibratory papillae do not or substrate, no calls were detected, indicat ﾂ deve@opunddl山 eethird 卜st 打け ) ， 川 d COne- ing that they were entirelysubstrate-bome. spondingly, first and second instar caterpi1- lars were all found to be mute. The obvious 帯弍 "' 血 ， m ， 川 十千二 " 苫酊 ， : Caterpillarsorwhen theycalledwere constantlyprodded by when the observer, walking head movements associated with sound pr0- 1104 SCIENCE, VOL. 248 ぴee 山Cば山 r甲山 e二O2 nn田 rp あ。u( Table 1. Call production by riodinid and lycaenid butterfly caterpillars. Abbreviations for countries: Pan for Panamaand CR for Costa Rica. The My COpMouSreLmtoSFc 卜士 aI ヴ piC 川Y 卜 Symbi M山川 L ， abtlityof 山eCa 低 T 川町 口 p「 M肛 e b5ho byY 卜rC 川5pF 田 uCcd川 d and nonmynnecophilous are species that do not associate with ants. The N for no calls produced. Depending on the species, from 1 to more than 50 の川 ofohg 血卜r 口士 sFC 卜 IeStedk 卜 p打 en 小めcS ぬuowhg 卜 n e・ 市山 祈 du寸 Qぼ T 川 awweresuweyed 卜 rab 山ヴ to 田而 dae Lycaemdae Mynnecophilous Nonmyrmecophilous Myrmecophilous NO ywecoph 而山 Eurybia lycisca (Pan) Y Leu 。ぴト而 onahp ， a(C 川 N C川 or 瓜呵川onShae 小iS(P 川)Y E川 a.ae山 g田 げm ， CR)N uC onasp.(P )N Eurybia patrona (Pan) Y レ 山 川 Strymon yojoa (Pan) Y 5ymbiopSist 川ぬ ぽ川)i E呵 biae@"hnaぽ狙 )Y Leucochimonaiphias (Pan) N ， w，。 山 COidQ(P 川)Y 凡ぽ@a 田 5卜 n(P 川)N Eurybia sp. (Ecuador) Y Mesosemia telegone (Pan) N 0l 川士山 n 打 も山 ぽ川)Y P丈 udolyCaenad O(P )N Thisbe irenea (Pan) Y Mめ aSp ・ ( ぬuador)N Thereus pedusa (Pan) Y Synar 甲 SmV(o 瓜ぽ狙 )Y Euselasia sp. (Pan) N 町山 menema(P 川)Y Synargis gela (Ecuador) Y Cぽ a 小as 山 (P 川)N Pan小 iadiad め b旧 L(P 如)Y L 山小 ;am 川卜 (P )Y Napaea eucharilla (Pan) N Rekoa palegon (Pan) Y Menander menander (Pan) Y Ancyluris inca (Pan) N Tmolus legytha (Pan) Y Calospila cilissa (CR) Y Rhcms arcius (Pan) N cdasp ・ (CR)Y OSpuae 山川山 (L 皿doI)Y Chans sp. (Pan) N Lycaeides melissa samuelis (U.S.) Y U而 Own 年nu5 ぽ川)Y Mcsene sp. (Pan) N Hypolycaenaerylius (Thailand) Y Theope thcstias (Pan) Y Mclanis pixie (CR) N Jalmenus "価。 evaeoras打 ion ぽぼOr(Australia) 川ld) YY Y 而 co 卜 m狐 ta(P 司 Y Mesenopsis bryaxis (Pan) N 血 ku Ce@ TheopeYirgLuaぽ川 )Y ES山 enop ぬ 丈 riCha(P 川)N 。" Le 川 Thcopc sp. (Pan) Y Symachia tricolor (Pan) N Maculinea alcon (France)Y Theope nr. decorata (CR) Y 品， O[a 叩a! (P 呵 N Cupido minimus (England) Y NympM 山川 m川 m5(P 川)Y Mter 山卜血 os ぼけ 川)N Lysandra bellargus (England) Y Emesis lucinda (CR) N Polyommatus icarus (England) Y I J E Ig90 REPORTS 1105 even be maintained in Ac face of parasitic 山山 vidu 寸 hhad 山 e 必 b口山 7 PapuIae ov 屯 interactions. For whereas the other individual retained them. Paired example,the caterpillars of 可eT 川め we eplacedonlndIvIdualpIantswhCre『 at least three species of Maculinea (Table 1) allQtCT 山如如dan[ShadbQen emovedlmmQdl『 ﾂ atCly bcfopeCx 卜 cn 口 h川 ・ ep 寸 nw 山 en live inside Myrmicaant nests to feed on the CCn5山 cocdsimUltanoously fbr [he number ofanTs larval brood of their host ant species (22). Iend 卜 e ぬ 山 C， [。中川 ぴ aI 「dme ht 。 W小 g]ng Hence, this study points to the possibility m l Q0 l2hours,andcaChpairwasleftQn[he planlforlto4daysofcensusCs.During 山 estudy that under selection for symbiotic associa ﾂ eachplanthadonly 山 。 palrCdCaterp[IIarsonit ・ 川 tions, the calls of one insect species have 以 en ほ usCd 小 eeS Cs 卜 ofanI ， 。 mm 。 @ evolved to attract other, distantly related m市 m (PonFnaC) ， and 川 caterPIllar p山卜 川 insectspecies. 口出 Cr 6ourth Or f6fIh in@t 如・F. The Cumulatlven - knof 如ほ ICn g 口CT 川打 p wcLComp byawuCoxonmatchcd-palrstcst@ 13. Quantifying the attenuation of substrate-bome sig- Lp 山 bk 山 ad ， s@ 寸寸 donvL M H。 " N "' n小 田 『 低n 皿 卜 M山 subs 也[e ， 山 e 山 5FFOnn[e ， f u如 C 卜 ， 川 d ヴ卜寸waV 卜 p uC 口 and 小 c 山 scanCe 而山 signal [Sec M. Gogala (20)]. The natural substrate caterpillars and ants live on is a combination of ぬ" ト ， o 卜 ， stems,bark@and ぬl@l ﾑ allwith" 山ぬ 。。 '"c 。。 """ 。。。 "" 。 "" 。 " ' 口旧@ insects may receive directional information from " 。 " 。 如。 " 甲。 "w'Eh 坤 " 。 " 。 "slm[lar 。 o 。 取 刀 L d in CaI mL $ [S叶 M・ a 四 H 川 thou如山 C clsIitttedoubt『 小 atna 口 dsu 卜血口 LP h， Yc 山 m t ， 血由Onp 山ト田卜山 an 山 Csub stratc on which calls were recorded (8), it is likely 4567 (b 瓜 nory ば r口 ed) 山 atm 卜 COdd て 。 wCCaLT 川 L Calls fpQm 山 L 。 卜 On avF 。 fsu 卜 " 也 1l45 P・ J・ ぬ vH 卜 ， pLbush o ado 卜 H.
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