Fujii, Hisashi

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RIGHT:URL:CITATION:AUTHOR(S):ISSUE DATE:TITLE:Ethological Studies on the Flower-visiting Behavior of LuehdorfiaButterflies (Lepidoptera ;Papilionidae) (III) : Learning FlowerColorFujii, HisashiFujii, Hisashi. Ethological Studies on the Flower-visiting Behavior of Luehdorfia Butterflies (Lepidoptera ; Papilionidae)(III) : Learning Flower Color. Memoirs of the Faculty of Science, Kyoto University. Series of biology. New series 2000,17(1): 1-92000-06http://hdl.handle.net/2433/258935Ment. Fac. Sci. Kyoto Uniu (Sen BiolJ, 17: 1-9, Jun., 2000Ethological Studies on the Fkower-visiting Behavior ofLuehdorlla              Butterflies (Lepidoptera; Papvaonidae)                    I[I. Leaming ptower CelorHIsAsm FuJIIDepartment of Zoology, Faculty of Science, Kyoto University,           Sakyo, Kyoto, 606-8502 Japan            (Received Aprii 21, 2000)Abstrast Luehdotfujaponica butterfiies were trained to initiate feeding behavior by white(or bee-white), red and yellow (or bee-purple) for more than 7 days in the laboratory. Thebutterfiies were then tested to aseertain whether they had memorized each color. The resultsof experiments indicated that they could learn to distinguish yellow but neither vvhite nor red.Similarly, L. puziloi were conditioned fer yellow (or bee- purple) flowers for only 2 hours inan outdoor cage. Before conditioning, the butterfiies visited bluish papers more frequentlythan yellowish ones, but they began to visit yellowish papers during the conditioning. Afterconditioning, the butterthes changed their preference to visit yellowish papers and bluishpapers equally.Key words I.,earning, Flower-visiting Behavior, Memory, LuehdorLfia, ButterfiyIRtreductio"    Most diurnal insects should be able to discriminate several colors. Some butterfiyspecies are known to use particular color(s) or color patterns in feeding aRdlor matingbehaviors alse 1928, 1932; Hidaka & Obara 1968; S. L. Swihart 1969, 197e, 1972; Swihart& Swihart 1970; C. A. Swihart 1971; Hidaka & Yamashita 1976; Miyakawa 1976; Llltowski1977; Shilberglies & Taylor 1978; Fujii 1999a, b). Tl}ough some studeRts believe thatiRsects are largely at the mercy of their instincts (e.g. Shields 1967), several insects areable to memorize or learn color, shape, location and so on (e.g. Matthews & Matthews1978). As far as butterflies are concerned, several species are believed to learn the colorof fiowers (Ilse 1928; S. L. Swihart 1970, 1972; Swihart & Swihart 1970; C. A. Swihart1971), the location of food flowefs and larval host plants (Gilbert 1975; Matthews &Matthews 1978), the leaf shape of hest plants (Rausher 1978; Papaj 1986) and how toextract Rectar from fiowers (Lewis 1986, 1989).    My pfevious studies have shownthatLuehdoifia butterflies visit flowers primarily inrespoRse to blue-violet refiection from flowers so that they should visit purplish fiowersmost often in their Ratural habitat. Adults ofL. puziloi have a minor color preference foryellow, whereas those ofL. japonica do not have a preference for either yellow or white.2 HtsAsHl FUJIIThe odor of fiowers attracts LuehdorLfia butÅíerflies when the fiower color is less attractive(Fujii 1999b). Thus, LuehdorLfin butterfiies might visit yellowish or whitish fiowers mainlyin response to odor, at least before they have experienced a number of visits to thosefiowers.   Butterfiies of both Luehdorfia species began to visit yellow or white fiowers in acage soon after I had presented such fiowers, and kept visiting the same flowers repeat-edly (Fujii unpublished). The butterflies are likely to have learned some traits, particu-larly fiower color. The objective of this study is to examine whetherLuehdoifia butter-thes could memorize or learn the color(s) of flowers.Materials and MethodsExperiments 1:   FemaleLuehdorfia japonica were collected in Kyoto in April 1984. Eggs were ob-tained frorn them in the laboratory. Larvae were reared on the fresh leaves of Heterotropaaspera. Pupae were kept in a refrigerator at 4eC frorn February 2e until March 23 or 28,1985. Afterwards, they were restored to room temperature for emergence.   Naive adults (30 males and 30 females) were prepared for the experiments. Theywere divided into three groups, one trained for yellow (Series 1), one for white (Series 2)and one for red (Series 3), respectively. A simple apparatus (Fig. 1-a) was used to allowthem Iearn a given color. Sugar solution was supplied every night uiltil the insects fin-a Colored papar b2525 2020        SugersolutionTransparent pla$tic board         Suger selutionTra&sipaorlaensAptst:tict}eardÅ~ tt1211"rz7,BlaÅëkFig. 1. a) ExperimegÅíal apparatus for coior conditioning, and b) experimental board for the color preferencetest in Experiment 1.Flower-visitingBehaviorofLuehdorfia III 3n?l ?a R !n RO o roa?} Rr?; v?2 GrY v-a?p rGBi B2 GB BGI se2 B-g eFig. 2. Arrangement of color papers in Experiment 2, Abbreviations, see Fig. 3.ished feeding. This traifiing continued for over a week until the experiment was com-pleted. Ten individuais (5 males and 5 females) were used in each experiment, and theremaining ten were reserved. When a trained butterfly died, a reserved individual of thesame sex was added to the cage, so that the number of butterflies in the experiments wasalways ten. The experiments were carried out in a laboratory cage ffom the 8th through10th days after ernergence (for details of the cage, see Fujii 1999a). The duratioR ef theexperirnents was 6 h a day (0900-1500), with a tota1 of 18 h. The experimental board (Fig.1-b) was used in every experiment. The behavior of butterflies was recorded with a videocamera (National MacLord). The number of butterflies that touched and/or alighted oneach colored paper was counted from the video records.Experiment 2:    Eggs ofL. puziloi were collected in Hiraka, Aomori in May 1987. Larvae werereared on the leaves ofAsiasarum Shieboldii. Pupae were kept in a refrigerator at 40C tilIearly April 1988, and then moved to an outdoor cage, in Hiraka (for details see Fujii1999a) for emergence. The experiment was canied out in the cage from 1 to 2 May 1988.Early in the moiniRg, a number of purplish fiowers such as Erythronium and Viota wereplaced on the ground of the cage. Naive butterflies were then released into the cage. Theyfreely visited these fiowers for about 4 hours. I theit conditioned the butterflies for yellowfor two hours by replacing the fiowers with many yellow dandelions (Taraxacum oXfiCijzale).The butterflies soon began to visit the dandelions. lhe fiowers were changed again whentwo hour conditioning period had fiRished. I tested for color preferences before condi-tioning, during coRditioning and one day after conditioning.   'IiweRty-four square colored papers (5 Å~ 5 cm2 in size) were used for the color prefer-ence test. The papers were arranged iR circle-square so that the colors changed gradually,and were fixed on the ground of the cage (Fig. 2). The refiectioR spectra of each colorpapef, measured with a spectrophotometer (Shimadzu UV-visible Recording Spectropho-tometer UV-240, Graphicord), are shown in Fig. 4. The behaviors of the butterflies wasrecorded throughout the experimeRt with a 8mm video camera (SONY V-900). After-wards, the number of contacts for each color paper was tabulated.4 HtsAsm Fujfileo503-1"-eN,       iuf.5Z?    2g ,o2eo fiootoesg4oe eoo3-2sut4,E,-GB'e2ee qeo 6ee seeloeselk 3-3    GY           ',x JY X`xN VS.,-..,ti'i"".,i'lli::'G-y(f'100se02co- -"qoe eoo sgo3-4e.-   E  tti$iX' o02DOter---"-Pr----4eo 6ee 800lgo503--5ygRO-•rt..•l,:100o200 600504oe soo3-6e200.7-v`x,-llL N    -- -gk'       Pl       P2     l     t    l   Le---RP1" .efi'""gP2 -'x-.S400 6ee soo                                   Wavelength (nm)Fig. 3. Refiection spectra of color papers used in Experiment 2. PR: vivid purplish red, R: vivid red, YR:vivid yellowish red, Re: vivid reddish orange, O: vivid orange, YO: vivid yellowish orange, RY vivid red-dish yellow, Y vivid yellew, GY vivid greenish yellow, Y-G: vivid yellow green,YG: vivid yellowish green,G: vivid green, B-G: vivid blue green, BG2: vivid bluish green 1, BGI: vivid bluish green 2, GB: vividgreenish blue, B2: vivid blue 2, Bl: vivid blue 1, PB: vivid purplish blue, V vivid violet, P2: vivid purple 2,Pl: vivid purple 1, RP2: vivid reddish purple 2, RPI:vivid reddish purple 1.Flower-visitingBehaviorofLuehdorfia Ill 5ResultsExperimeRt 1:Series 1   When trained for yellow, the butterfiies visited yellow more frequently than others(P<O.OOI, Chi-square test; Fig. 4). Their color preference was significantly different fromthose in Series 2 and 3 (P<O.Ol). Tl}e butterflies appeared to have memorized or learnedyellow as the color of nectar sources.Series 2   When trained for white.(p<o.ool; Fig. 4).the butterfiies visited blue more frequently than othersSeries 3   When trained for rea the butterfiies visited blue more frequently than others (P<O.OOI;Fig. 4). Their color preference was no difference from that in Series 2 (P>O.05).igsee2329525BW Y*R   Se r, lseoss22 238seB W*YR   Ser.2o26176 7BWY Rt   Ser. 3Ser.tSer. 2Ser. 3B w Y# RBW* YRB w Y R*P<O.OOIN. S.ptig. 4. O 50 tOO%Results of Experiment 1. ': the coler conditioned.6 HISAsHl FUJIIExperiment 2:   Before conditioning, the butterfiies clearly preferred blue to other colors. This didnot change during the lst one hour of conditioning. However, their preference shiftedfrom blue to orange-yellow during the second hour of coRditioning. The butterflies stillvisited orange-yellow frequently even one day after the conditioning. This therefore sug-gests that Luehdorfia puziloi can memorize the color yellow as nectar sources in a matterof 2 h (Fig. 5).actoe1co•20Åítoe23ie5o4  R ncPR \R Oyo RYYYG GY YGG BG2 BG Bi V Pi RPI Se BGf ee ma re RP2Fig. 5. Changes in color preference. 1: before conditioning.coRditioning. 4: 1 day after conditioning.2: lst 1 h during conditioning. 3: 2nd 1 h duringFlower-visitingBehaviorofLuehdorfia III 7Discassion    As Ilse (1928) noted, the color preference of feeding butterthes may have two at-tributes: (1) innate preference, and (2) acquired preference. The previous studies havealready proved the first attribute in Luehdorfia (Fujii 1999a, b). The results of this studyjustified the second attribute in Luehdorfia.    Innately, adultL. iaponica prefer blue-violet to yellow, red and white (Fujii 1999a).The results of Experiment 1 suggest that adultL. japonica can learpto recognize yellow(or bee-purple) but cannot learn to recognize white nor red as the color of Rectar sources.It should be noted that, in both Series 2 aRd 3, the butterfiies visited vivid blue rr}ostfrequently regardless of the trained color. This means adultL. japonica have innate colorpreference for blue-violet (or bee-blue) as my previous studies have already suggested(Fujii 1999a, b). Nevertheless, the proportions of contacts on white and yellow papers arelarger than those in the previous study (Fujii 1999a). Because the training lasted for morethan 7 days, thebutterfiies might have slightly changed innate colorpreference as a resultof my training.    AdultL. japonica are unlikely to have innate color prefereilce for yellow (Fujii 1999a;this study). This is a probable explanation for their rare visits to yellowish fiowers innature (e.g. Fukuda et aL 1982). However, asa result of leaming, an adultL. japonicamay begin to visit yellowish fiowers iR response to yellow refiection if many yellowishfiowers are available in its habitat.   As for L. puziloi, they are likely to have not oRly ifinate color preference for blue-violet but also minor preference for yellow (Fujii 1999a; this study). This shouid explainwhy adultL. puziloi visit not oRly puiplish fiowers but also yellowish fiowers occasion-ally (in most habitats) or frequently (in several habitats in Hokkaido) in the natural habitat(e.g. Fukuda et aL 1982; Watanabe 1985; Kanda 1987). The result of Experiment 2 sug-gests that L. puziloi can change their color preferences fairly easily from imate prefereRcefor blue-violetto acquired preference for yellow (or orange-yellow) if yellowish fiowersare more abundant than purplish fiowers. Thus, acquired preference for yellow shouldconstitute another reason for occasional or frequent visits oil the yellowish fiowers.   As pointed out in the previous paper (Fujii 1999b), the odor of yellowish flowers mayalso attractLuehdorLfi'a butterflies. After conditioning, however, the butterflies began tovisit yellow or yellowish papers that lacked odor. Therefore, the odor of flowers seemsimportant oniy before the butterflies leam the color of fiowers. This would constituteadaptive nature, because recogRition time would be shorter if the iRsect recoginizes foodvisually than when it recognizes it through its olfactory sensors (e.g. Krebs 1978).8 HtsAsHI FUJllAcknowledgemefits   'IThe author wishes to express his appreciation to Mr. Y. Kikuchi who kindly reared L.puziloi and permitted me to use his outdoor cage for experiments. This work was sup-ported in part by a Grant-in-Aid (No. 58121003) for Special Project Research on Biologi-cal Aspects of Optimal Strategy aild Social Structure from the Japan Ministry of Educa-tion, Science and Culture.ReferencesFujii, H. 1999a Ethological studies on the flower-visiting behavior ofLuehdorLt}'a butter-   fiies (Lepidoptera; Papilionidae). I. Color preference of butterthes and reflection   spectra of fiowers. Mem. Fac. Sci. Kyoto Univ. (Sen Biol.) 16: 67-86.Fujii, H. 1999b Ethological studies on the flower-visiting behavior ofLuehdorfia butter--   fiies (Lepidoptera; Papilionidae). II. Effects of the size, shape and odor of flowers.   Mem. Fac. Sci. Kyoto Univ. (Ser. Biol.) 16: 87-94.Fukuda, H., E. Hama, T. Kuzuya, A. Takahashi, M. Takahashi, B. Tanaka, H. Tanaka, M.   Wakabayashi & Y. Watanabe 1982 The Iife histories of butterflies in Japan. Vol.I.   277pp., Hoikusha, Osaka (in Japanese with English summary).Gilbert, L. E. 1975 Ecological consequences of a coevolved mutualism between butter-   fiies and plants. In L. E. Gilbert & P. H. Raven (eds.) Coevolution ofAnimals and   Plants. pp. 141-158. University of Texas Press, Austin.Hidaka, T. & K. Yamashita 1976 Change of meaning of color in the Umwelt ofbutter-   fiies. Physiol. EcoL Japan. 17:15-21.Hidaka, T. & Y. Obara 1968 Small cabbage white -- Butterfly behavior "-- . A scientific   film by Iwanami ProductioRs, Inc.Ilse, D. 1928 Uber den Farbensinn der Tagfalter. Z. vergl. Physiol. 8: 658-692.Ilse, D. 1932 Zur "Formwahrnehniung" der Tagfalter. I. Spontane Bevorzugung von   Formmerkmalen. Z. vergl. Physiol. 17: 537-556.Kanda, S. 1987 "Chodan-Fuhatsu (2)": Dohoku no Hime-gifu-cho wa Kiiro ga Daisuki.   [Notes on butterflies (2): LuehdorLfiia puziloi yessoensis strongly prefer the color yel-   low in northem Hokkaido.l Usubain' (74): 1-2 (in Japanese).Krebs, J. R. 1978 Oprimal foraging: decision rules for predators. In J. R. Krebs & N. B.   Davies (eds.) BehaviouralEcology. An EvolutiOnaryApproach. pp.23-63, Blackwell   Scientific Publications Oxford.                    'Lewis, A. C. 1986 Memory constraints and flower choice in Pieris rapae. Science 232:   863-865.Flower-visitlngBehaviorofLuehdetiia lll 9Lewis, A. C. 1989 Flower visit consistency in Pieris rapae, the cabbage butterfiy. J.   Anim. Ecol. 58: 1-13.Lutowski, R. L. 1977 The use of visual cues in sexual and species discrimination by   males of the small sulphur butterfiy Eurema lisa (Lepidoptera, Pieridae). J. comp.   Physiol. 115: 61-74.Matthews, R. W. & J. R. Matthews 1978 Insect behavior. 507pp, Wiley-Interscience   Publication, New York.Miyakawa, M. 1976 Flower-visiting behavior of small white butterfiy, Pieris rapae   crucivora. Annot. ZooL Jap. 49: 261-273.Papaj, D. R. 1986 Conditioning of leaf-shape discrimination by chemical cues in the   butterfly, Battusphilenon Anim. Behav. 34: 1281-1288.Rausher, M. D. 1978 Search image for leafshape in a butteifiy. Science 200: 1071-1073.Shields, O. 1967 Hilltopping. J. Res. Lepid. 6(2):69-178.Silberglied, R. E. & O. R. Taylor, Jr. 1978 Ultraviolet refiection and its behavioral role in   the courtship of the sulfur butterflies Colias eui ytheme and C. philodice (Lepidoptera,   Pieridae). Behav. Ecot. Sociobiol. 3:203-243.Swihart, C. A. 1971 Colour discrimination by the butterfly, Heliconius charitonius Linn.   Anim. Behav. 19: 156-164.Swihart, C. A. & S. L. Swihart 1970 Colour selection and leamed feeding preferences in   the butterfly, Heliconius charitonius Linn. Anim. Behau 18: 60-64.Swihart, S. L. 1969 Colour vision and the physiology of the superposition eye of a butter-   fiy (Hesperiidae). J. InsectPhysiol. 15: 1347-1365.Swihart, S. L. 197e The neural basis of colour vision in the butterfiy, Papilio troilus. J.   InsectPhysioL 16: 1623-1636.Swihart, S. L. 1972 The Reural basis of colour vision in the butterfly, Heliconius erato. J.   InsectPhysiot. 18: 1015-1025.Watanabe, S. 1985 Nihon no Konchu. 1. Gifu-cho. [Insects of Japan. 1. Luehdorfi'a   japonica.] 148pp., 8pls., Bun'ichi-sogo-shuppan, Tokyo (in Japanese).

Ethological Studies on the Flower-visiting Behavior of Luehdorfia Butterflies (Lepidoptera ; Papilionidae) (III) : Learning Flower Color

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Ethological Studies on the Flower-visiting Behavior of Luehdorfia Butterflies (Lepidoptera ; Papilionidae) (III) : Learning Flower Color

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