Skip to main content
SpringerLink
Log in

Volatile terpenoids from male wings lacking scent scales in Anthocharis scolymus (Lepidoptera: Pieridae)

  • Original Research Paper
  • Published:
Applied Entomology and Zoology Aims and scope Submit manuscript

Abstract

Pierinae, the major subfamily of Pieridae, is characterized by possessing scent scales as androconia on male wings, which are most likely to disperse volatile substances. However, the chemistry of androconial substances is known for very few species. The yellow tip Anthocharis scolymus Butler (Pierinae: Anthocharidini) is a univoltine pierine butterfly distributed in East Asia. Male adults of this species emit a subtle floral scent, while females are scentless. We revealed that the male-specific scent consists of (S)-(+)-linalool and (E)-β-farnesene, which had never been discovered in Pieridae. Moreover, these volatile terpenoids were more abundant in the wings than in the body, and were distributed from the basal to the distal regions of each wing. Unlike other pierine species, A. scolymus males lacked alar scent scales but had round saccular structures connected to the socket of the ordinary scale in the wing membrane. The morphology of this structure was very similar to those of the intermembranous scent-producing organs of male wings in the subfamily Coliadinae. Although scent scales are found in the genus Anthocharis, the presence of male-specific scents has not been reported so far. The present study illustrates unique characters of A. scolymus in both androconial chemistry and morphology in Pierinae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andersson J, Borg-Karlson A-K, Vongvanich N, Wiklund C (2007) Male sex pheromone release and female mate choice in a butterfly. J Exp Biol 210:964–970. doi:10.1242/jeb.02726

    Article  CAS  PubMed  Google Scholar 

  • Bergström G, Lundgren L (1973) Androconial secretion of three species of butterflies of the genus Pieris (Lep., Pieridae). Zoon Suppl 1:67–75

    Google Scholar 

  • Bolg-Karlson A-K, Tengö J, Valterová I, Unelius CR, Taghizadeh T, Tolasch T, Francke W (2003) (S)-(+)-Linalool, a mate attractant pheromone component in the bee Colletes cunicularius. J Chem Ecol 29:1–14. doi:10.1023/A:1021964210877

    Article  Google Scholar 

  • Braby MF (2005) Provisional checklist of genera of the Pieridae (Lepidoptera: Papilionoidea). Zootaxa 832:1–16

    Google Scholar 

  • Braby MF, Vila R, Pierce NE (2006) Molecular phylogeny and systematics of the Pieridae (Lepidoptera: Papilionoidea): higher classification and biogeography. Zool J Linn Soc 147:239–275. doi:10.1111/j.1096-3642.2006.00218.x

    Article  Google Scholar 

  • Chew FS, Watt WB (2006) The green-veined white (Pieris napi L.), its pierine relatives, and the systematics dilemmas of divergent character sets (Lepidoptera, Pieridae). Biol J Linn Soc 88:413–435. doi:10.1111/j.1095-8312.2006.00630.x

    Article  Google Scholar 

  • Dawson GW, Griffiths DC, Merritt LA, Mudd A, Pickett JA, Wadhams LJ, Woodcock CM (1990) Aphid semiochemicals—a review, and recent advances on the sex pheromone. J Chem Ecol 16:3019–3030. doi:10.1007/BF00979609

    Article  CAS  PubMed  Google Scholar 

  • Dixey FA (1932) The plume-scales of the Pierinae. Trans Entomol Soc Lond 80:57–75. doi:10.1111/j.1365-2311.1932.tb00082.x

    Article  Google Scholar 

  • Dötterl S, Burkhardt D, Weißbecker B, Jürgens A, Schütz S, Mosandl A (2006) Linalool and lilac aldehyde/alcohol in flower scents, electrophysiological detection of lilac aldehyde stereoisomers by a moth. J Chromatogr A 1113:231–238. doi:10.1016/j.chroma.2006.02.011

    Article  PubMed  Google Scholar 

  • Ehrlich PR (1958) The comparative morphology, phylogeny and higher classification of the butterflies (Lepidoptera: Papilionoidea). Univ Kansas Sci Bull 39:305–370

    Google Scholar 

  • Geiger HJ (1980) Enzyme electrophoretic studies on the genetic relationships of pierid butterflies (Lepidoptera: Pieridae) I. European taxa. J Res Lepid 19:181–195

    Google Scholar 

  • Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414. doi:10.1038/nchembio.2007.5

    Article  CAS  PubMed  Google Scholar 

  • Grujic-Jovanovic S, Skaltsa HD, Marin P, Sokovic M (2004) Composition and antibacterial activity of the essential oil of six Stachys species from Serbia. Flavour Fragr J 19:139–144. doi:10.1002/ffj.1275

    Article  CAS  Google Scholar 

  • Grula JW, McChesney JD, Taylor OR Jr (1980) Aphrodisiac pheromones of the sulfur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae). J Chem Ecol 32:435–451. doi:10.1007/BF00987543

    Google Scholar 

  • Hall JPW, Harvey DJ (2002) A survey of androconial organs in the Riodinidae (Lepidoptera). Zool J Linn Soc 136:171–197. doi:10.1046/j.1096-3642.2002.00003.x

    Article  Google Scholar 

  • Hayashi N, Kuwahara Y, Komae H (1978) The scent scale substances of male Pieris butterflies (Pieris melete and Pieris napi). Experientia 34:684–685. doi:10.1007/BF01947255

    Article  CAS  Google Scholar 

  • Hayashi N, Nishi A, Murakami T, Maeshima K, Komae H, Sakao T (1985) The scent substances of pierid butterflies (Hebomoia glaucippe Linnaeus) and the volatile components of their food plants (Crataeva religiosa Forst.). Z Naturforsch C 40:47–50

    Google Scholar 

  • Heil M (2008) Indirect defense via tritrophic interactions. New Phytol 178:41–61. doi:10.1111/j.1469-8137.2007.02330

    Article  CAS  PubMed  Google Scholar 

  • Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120. doi:10.1663/0006-8101(2006)72[1:DADOFS]2.0.CO;2

  • Kristensen NP, Simonsen TJ (2003) ‘Hairs’ and cells. In: Kristensen NP, Simonsen TJ (eds) Lepidoptera, moths and butterflies. Vol. 2: Morphology, physiology, and development. Handbuch der Zoologie/Handbook of Zoology IV/36. Walter de Gruyter, Berlin and New York, pp 9–22

    Google Scholar 

  • Kuwahara Y (1979) Scent scale substances of male Pieris melete Ménétriès (Pieridae: Lepidoptera). Appl Entomol Zool 14:350–355. doi:10.1303/aez.14.350

    CAS  Google Scholar 

  • Larsdotter-Mellström H, Murtazina R, Borg-Karlson A-K, Wiklund C (2012) Timing of male sex pheromone biosynthesis in a butterfly—different dynamics under direct or diapause development. J Chem Ecol 38:584–591. doi:10.1007/s10886-012-0126-6

    Article  PubMed  Google Scholar 

  • Martin DM, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol 132:1586–1599. doi:10.1104/pp.103.021196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakai M, Honda K, Ueda H, Ômura H (2001) Is androconial secretion of Pieris napi (Lepidoptera: Pieridae) chemically dimorphic? Trans Lepid Soc Jpn 52:309–312

    Google Scholar 

  • Okamoto T, Kawakita A, Goto R, Svensson GP, Kato M (2013) Active pollination favours dimorphism in floral scent. Proc R Soc B 280:20132280. doi:10.1098/rspb.2013.2280

    Article  PubMed  PubMed Central  Google Scholar 

  • Ômura H, Honda K (2005) Chemical composition of volatile substances from adults of the swallowtail, Papilio polytes (Lepidoptera: Papilionidae). Appl Entomol Zool 40:421–427. doi:10.1303/aez.2005.421

    Article  Google Scholar 

  • Ômura H, Honda K (2011) Pungent odor of the adult skipper butterfly Erynnis montanus (Lepidoptera: Hesperiidae). Appl Entomol Zool 46:281–286. doi:10.1007/s13355-011-0039-9

    Article  Google Scholar 

  • Ômura H, Yotsuzuka S (2015) Male-specific epicuticular compounds of the sulfur butterfly Colias erate poliographus (Lepidoptera: Pieridae). Appl Entomol Zool 50:191–199. doi:10.1007/s13355-015-0321-3

    Article  Google Scholar 

  • Ômura H, Morinaka S, Honda K (2000) Chemical nature of volatile compounds from the valvae and wings of male Delias butterflies (Lepidoptera: Pieridae). Entomol Sci 2000:427–432

    Google Scholar 

  • Ômura H, Yanai N, Honda K (2012) Sexual dimorphism in scent substances and cuticular lipids of adult Papilio protenor butterflies. Z Naturforsch C 67:331–341

    Article  PubMed  Google Scholar 

  • Ômura H, Itoh T, Wright DM, Pavulaan H, Schröder S (2015) Morphological study of alar androconia in Celastrina butterflies. Entomol Sci 18:353–359. doi:10.1111/ens.12126

    Article  Google Scholar 

  • Raguso RA, Pichersky E (1999) A day in the life of a linalool molecule: chemical communication in a plant-pollinator system. Part 1: Linalool biosynthesis in flowering plants. Plant Spec Biol 14:95–120. doi:10.1046/j.1442-1984.1999.00014.x

    Article  Google Scholar 

  • Robbins RK, Henson PM (1986) Why Pieris rapae is a better name than Artogeia rapae (Pieridae). J Lep Soc 40:79–92

    Google Scholar 

  • Rutowski RL (1977) Chemical communication in the courtship of the small sulphur butterfly Eurema lisa (Lepidoptera, Pieridae). J Comp Physiol A 115:78–85. doi:10.1007/BF00667786

    Google Scholar 

  • Savela M (2015) Lepidoptera and some other life forms. http://www.nic.funet.fi/pub/sci/bio/life/intro.html. Accessed 15 Dec 2015

  • Schulz S, Francke W, Edgar J, Schneider D (1988) Volatile compounds from androconial organs of danaine and ithomiine butterflies. Z Naturforsch C 43:99–104

    CAS  Google Scholar 

  • Scott JA (1972) Mating of butterflies. J Res Lepid 11:99–127

    Google Scholar 

  • Turlings TCJ, Loughrin JH, McCall PJ, Röse USR, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci USA 95:4169–4174

    Article  Google Scholar 

  • Vetter RS, Rutowski RL (1978) External sex brand morphology of three sulphur butterflies (Lepidoptera: Pieridae). Psyche 85:383–393. doi:10.1155/1978/78397

    Article  Google Scholar 

  • Wahlberg N, Rota J, Braby MF, Pierce NE, Wheat CW (2014) Revised systematic and higher classification of pierid butterflies (Lepidoptera: Pieridae) based on molecular data. Zool Scr 43:641–650. doi:10.1111/zsc.12075

    Article  Google Scholar 

  • Warren BCS (1961) The androconial scales and their bearing on the question of speciation in the genus Pieris (Lepidoptera). Entomol Tidskr Arg 82:121–148

    Google Scholar 

  • Wiklund C, Forsberg J (1985) Courtship and male discrimination between virgin and mated females in the orange tip butterfly Anthocharis cardamines. Anim Behav 34:328–332. doi:10.1016/S0003-3472(86)80100-2

    Article  Google Scholar 

  • Yildizhan S, van Loon J, Sramkova A, Ayasse M, Arsene C, ten Broeke C, Schulz S (2009) Aphrodisiac pheromones from the wings of the small cabbage white and large cabbage white butterflies, Pieris rapae and Pieris brassicae. Chem Bio Chem 10:1666–1677. doi:10.1002/cbic.200900183

    Article  CAS  PubMed  Google Scholar 

  • Yoshida A, Noda A, Yamana A, Numata H (2000) Arrangement of scent scales in the male wings of the small white cabbage butterfly (Lepidoptera: Pieridae). Entomol Sci 3:345–349

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Applied Biological Science, Hiroshima University, Higashihiroshima, 739-8528, Japan

    Yukiko Okumura & Yuki Ozeki

  2. Graduate School of Integrated Arts and Sciences, Hiroshima University, Higashihiroshima, 739-8521, Japan

    Takao Itoh

  3. Graduate School of Biosphere Science, Hiroshima University, Higashihiroshima, 739-8528, Japan

    Shinji Ohta & Hisashi Ômura

Authors
  1. Yukiko Okumura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuki Ozeki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takao Itoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shinji Ohta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hisashi Ômura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hisashi Ômura.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1698 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Okumura, Y., Ozeki, Y., Itoh, T. et al. Volatile terpenoids from male wings lacking scent scales in Anthocharis scolymus (Lepidoptera: Pieridae). Appl Entomol Zool 51, 385–392 (2016). https://doi.org/10.1007/s13355-016-0410-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13355-016-0410-y

Keywords

Search

Navigation