Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T08:54:15.108Z Has data issue: false hasContentIssue false
  • English
  • Français

Sexual communication in day-flying Lepidoptera with special reference to castniids or ‘butterfly-moths’

Published online by Cambridge University Press:  05 April 2016

V. Sarto i Monteys ,
C. Quero ,
M.C. Santa-Cruz ,
G. Rosell  and
A. Guerrero
V. Sarto i Monteys*
Affiliation:
Institute of Environmental Science and Technology (ICTA), Entomology, Plants and Health-Room Z/141, Building Z – ICTA-ICP, Autonomous University of Barcelona, 08193 Bellaterra, Barcelona, Spain Department of Agriculture, Livestock, Fisheries, Food and Environment (DAAM), Catalonian Government – Service of Plant Health, Avda. Meridiana, 38, 08018 Barcelona, Spain
C. Quero
Affiliation:
Department of Biological Chemistry and Molecular Modelling, IQAC (CSIC), Jordi Girona 18. 08034, Barcelona, Spain
M.C. Santa-Cruz
Affiliation:
Department of Cell Biology, Physiology and Immunology, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
G. Rosell
Affiliation:
Department of Pharmacology and Therapeutic Chemistry (Unit Associated to CSIC), Faculty of Pharmacy, University of Barcelona, Av. Diagonal s/n, 08028 Barcelona, Spain
A. Guerrero*
Affiliation:
Department of Biological Chemistry and Molecular Modelling, IQAC (CSIC), Jordi Girona 18. 08034, Barcelona, Spain
*
*Author for correspondence Phone: +34-93-4006120 Fax: +34-93-2045904 E-mail: agpqob@cid.csic.es and Phone: +34 -93-5868647 (ext. 8647) Fax: +34-93-5813331 E-mail: victor.sarto@uab.cat
*Author for correspondence Phone: +34-93-4006120 Fax: +34-93-2045904 E-mail: agpqob@cid.csic.es and Phone: +34 -93-5868647 (ext. 8647) Fax: +34-93-5813331 E-mail: victor.sarto@uab.cat
Get access Rights & Permissions [Opens in a new window]

Abstract

Butterflies and moths are subject to different evolutionary pressures that affect several aspects of their behaviour and physiology, particularly sexual communication. Butterflies are day-flying insects (excluding hedylids) whose partner-finding strategy is mainly based on visual cues and female butterflies having apparently lost the typical sex pheromone glands. Moths, in contrast, are mostly night-flyers and use female-released long-range pheromones for partner-finding. However, some moth families are exclusively day-flyers, and therefore subject to evolutionary pressures similar to those endured by butterflies. Among them, the Castniidae, also called ‘butterfly-moths’ or ‘sun-moths’, behave like butterflies and, thus, castniid females appear to have also lost their pheromone glands, an unparallel attribute in the world of moths. In this paper, we review the sexual communication strategy in day-flying Lepidoptera, mainly butterflies (superfamily Papilionoidea), Zygaenidae and Castniidae moths, and compare their mating behaviour with that of moth families of nocturnal habits, paying particular attention to the recently discovered butterfly-like partner-finding strategy of castniids and the fascinating facts and debates that led to its discovery.

Keywords

CastniidaePaysandisia archonbutterfliesZygaenidaechemical communicationmating behaviour
Type
Review Article
Information
Bulletin of Entomological Research , Volume 106 , Issue 4 , August 2016 , pp. 421 - 431
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acín, P. (2009) Identificación de feromonas y proteínas implicadas en la percepción feromonal de lepidópteros plaga . PhD Thesis, University of Barcelona, Barcelona.Google Scholar
Bergman, M., Gotthard, K., Berger, D., Olofsson, M., Kemp, D.J. & Wiklund, C. (2007) Mating success of resident versus non-resident males in a territorial butterfly. Proceedings of the Royal Society of London B, Biological Sciences 274, 1659–1665.Google Scholar
Boppré, M. (1984) Chemically mediated interactions between butterflies. pp. 259–275 in Vane-Wright, R.I. & Ackery, P.R. (Eds) XI Symposium Royal Entomological Society of London. London, Academic Press.Google Scholar
Charlton, R.E. & Cardé, R.T. (1982) Rate and diel periodicity of pheromone emission from female gypsy moths, (Lymantria dispar) determined with a glass-adsorption collection system. Journal of Insect Physiology 28, 423–430.Google Scholar
Costanzo, K. & Monteiro, A. (2007) The use of chemical and visual clues in female choice in the butterfly Bicyclus anynana . Proceedings of Biological Sciences 274, 845–851.Google Scholar
Davies, N.B. (1978) Territorial defence in the speckled wood butterfly (Pararge aegeria): the resident always wins. Animal Behaviour 26, 138–147.CrossRefGoogle Scholar
Delle-Vedove, R., Beaudoin-Ollivier, L., Hossaert-McKey, M. & Frérot, B. (2012) Reproductive biology of the palm borer: Paysandisia archon . European Journal of Entomology 109, 289–292.Google Scholar
Delle-Vedove, R., Frérot, B., Hossaert-McKey, M. & Beaudoin-Ollivier, L. (2014) Courtship behavior of the castniid palm borer, Paysandisia archon: potential roles of male scents and visual cues in a day-flying moth. Journal of Insect Science 14, 1–14. Available online at http://www.insectscience.org Google Scholar
Douglas, F. (2004) A dedicated reserve for conservation of two species of Synemon (Lepidoptera: Castniidae) in Australia. Journal of Insect Conservation 8, 221–228.Google Scholar
Edwards, E.D., Gentili, P., Horak, M., Kristensen, N.P. & Nielsen, E.S. (1998) The Cossoid/Sesioid assemblage. pp. 181–197 in Kristensen, N.P. (Ed.) Lepidoptera, Moths and Butterflies. Vol. 1. Evolution, Systematics and Biogeography. Berlin, New York, Walter de Gruyter.Google Scholar
Eisner, T. & Meinwald, J. (1987) Alkaloid-derived pheromones and sexual selection in Lepidoptera. pp. 251–269 in Preswitch, G.D. & Blomquist, G.J. (Eds) Pheromone Biochemistry. Orlando, Academic Press.Google Scholar
El-Sayed, A.M. (2014) The Pherobase: Database of Insect Pheromones and Semiochemicals. Available online at http://www.pherobase.com.Google Scholar
Frérot, B., Delle-Vedove, R., Beaudoin-Ollivier, L., Zagatti, P., Ducrot, P.-H., Grison, C., Hossaert, M. & Petit, E. (2013) Fragrant legs in Paysandisia archon males (Lepidoptera, Castniidae). Chemoecology 23, 137–142.CrossRefGoogle Scholar
Friedrich, E. & Friedrich-Polo, A. (2005) Zygaena fausta L. im Tauberland (Main-Tauber-Kreis) (Lepidoptera, Zygaenidae). Eine verhaltensorientierte Feldstudie. Mitteilungen des Entomologischen Vereins Stuttgart 40, 123–130.Google Scholar
Hall, D.R., Cork, A., Lester, R., Nesbitt, B.F. & Zagatti, P. (1987) Sex pheromone of rice moth, Corcyra cephalonica Stainton. II. Identification and role of female pheromone. Journal of Chemical Ecology 13, 1575–1589.CrossRefGoogle ScholarPubMed
Hallberg, E. & Poppy, G. (2003) Exocrine glands: chemical communication and chemical defense. pp. 361–375 in Kristensen, N.P. (Ed.) Lepidoptera, Moths and Butterflies. Vol. 2: Morphology, Physiology, and Development. Berlin, New York, Walter de Gruyter.Google Scholar
Hallberg, E. & Subchev, M. (1997) Unusual location and structure of female pheromone glands in Ino ampelophaga Bayle (Lepidoptera, Zygaenidae). International Journal of Insect Morphology and Embryology 25, 381–389.Google Scholar
Hansson, B.S. (1995) Olfaction in Lepidoptera. Experientia 51, 1003–1027.Google Scholar
Haynes, K.F., Gaston, L.K., Mistrot Pope, M. & Baker, T.C. (1983) Rate and periodicity of pheromone release from individual female Artichoke Plume Moths, Platyptilia carduidactyla (Lepidoptera: Pterophoridae). Environmental Entomology 12, 1597–1600.Google Scholar
Hofmann, A. & Kia-Hofmann, T. (2010) Experiments and observations on pheromone attraction and mating in burnet moths (Zygaena Fabricius, 1777) (Lepidoptera: Zygaenidae). Entomological Gazette 61, 83–93.Google Scholar
Jordan, K. (1923) On the scent-organs in the males of certain American Castniidae. Novitates Zoologicae 30, 159–162.Google Scholar
Kemp, D.J. & Wiklund, C. (2004) Residency effects in animal contests. Proceedings of the Royal Society of London B, Biological Sciences 271, 1707–1711.Google Scholar
Knudsen, J.T. (2002) Variation in floral scent composition within and between populations of Geonoma macrostachys (Arecaceae) in the western Amazon. American Journal of Botany 89, 1772–1778.Google Scholar
Koshio, C. (2003) Mating behaviour and activity patterns of the Japanese burnet moth Zygaena niphona Butler, 1877 (Lepidoptera: Zygaenidae, Zygaeninae). p. 360 in Efetov, K.A., Tremewan, W.G. & Tarmann, G.M. (Eds) Proceedings of the 7th International Symposium on Zygaenidae (Lepidoptera). Innsbruck, Austria, Crimean State Medical University Press, Simferopol.Google Scholar
Kristensen, N.P., Scoble, M.J. & Karsholt, O. (2007) Lepidoptera phylogeny and systematics: the state of inventorying moth and butterfly diversity. Zootaxa 1668, 699–747.Google Scholar
Landolt, P.J. & Heath, R.R. (1989) Attraction of female cabbage looper moths (Lepidoptera: Noctuidae) to male-produced sex pheromone. Annals of Entomological Society of America 82, 520–525.Google Scholar
Lauwers, K. & Van Dyck, H. (2006) The cost of mating with a non-virgin male in a monandrous butterfly: experimental evidence from the speckled wood, Pararge aegeria . Behavioral Ecology and Sociobiology 60, 69–76.Google Scholar
Le Cerf, F. (1936) Un type remarquable d'androconie chez certaines Gazera Boisduval (Lep., Castniidae). Bulletin de la Societé Entomologique de France 41, 191–195.CrossRefGoogle Scholar
Miller, J.Y. (1986) The Taxonomy, Phylogeny, and Zoogeography of the Neotropical Moth Subfamily Castniinae (Lepidoptera: Castnioidea: Castniidae) . PhD Thesis, University of Florida, Gainesville, USA.Google Scholar
Minet, J. (1991) Tentative reconstruction of the ditrysian phylogeny (Lepidoptera: Glossata). Entomologica Scandinavica 22, 69–95.Google Scholar
Mutanen, M., Wahlberg, N. & Kaila, L. (2010) Comprehensive gene and taxon coverage elucidates radiation patterns in moths and butterflies. Proceedings of the Royal Society of London B, Biological Sciences 277, 2839–2848.Google Scholar
Naumann, C.M. (1988) Zur Evolution und adaptiven Bedeutung zweier unterschiedlicher Partnerfindungsstrategien bei Zygaena trifolii (Esper, 1783) (Lepidoptera, Zygaenidae). Verhandlungen der deutschen Zoologischen Gesellschaft 81, 257–258.Google Scholar
Naumann, C.M., Tarmann, G.M. & Tremewan, W.G. (1999) The Western Palaearctic Zygaenidae. Stenstrup, Denmark, Apollo Books, p. 304.Google Scholar
Nieberding, C.M., Fischer, K., Saastamoinen, M., Allen, C.E., Wallin, E.A., Hedenström, E. & Brakefield, P.M. (2012) Cracking the olfactory code of a butterfly: the scent of ageing. Ecology Letters 15, 415–424.Google Scholar
Percy-Cunningham, J. & MacDonald, J.A. (1987) Biology and ultrastructure of sex pheromone-producing glands. pp. 27–75 in Prestwich, G.D. & Blomquist, G.J. (Eds) Pheromone Biochemistry. Orlando, Academic Press.Google Scholar
Prinz, J. & Naumann, C.M. (1988) Optische Parameter bei der Partnerfindung von Zygaena trifolii (Esper, 1783). Verhandlungen der deutschen Zoologischen Gesellschaft 81, 258.Google Scholar
Rebouças, L.M.C., Caraciolo, M.S.B., Sant'Ana, A.E.G., Pickett, J.A., Wadhams, L.J. & Pow, E.M. (1999) Composição química da glândula abdominal da fêmea da mariposa Castnia licus (Drury) (Lepidoptera: Castniidae): Possíveis feromônios e precursores. Quimica Nova 22, 645–648.CrossRefGoogle Scholar
Regier, J.C., Zwick, A., Cummings, M.P., Kawahara, A.Y., Cho, S., Weller, S., Roe, A., Baixeras, J., Brown, J.W., Parr, C., Davis, D.R., Epstein, M., Hallwachs, W., Hausmann, A., Janzen, D.H., Kitching, I.J., Solis, M.A., Yen, S.-H., Bazinet, A.L. & Mitter, C. (2009) Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study. BMC Evolutionary Biology 9, 1–21.Google Scholar
Riolo, P., Verdolini, E., Anfora, G., Minuz, R.L., Ruschioni, S., Carlin, S. & Isidoro, N. (2014) Perching mate-locating strategy in Paysandisia archon (Lepidoptera: Castniidae): behavioral and morpho-physiological investigations. Journal of Economic Entomology 107, 1009–1021.Google Scholar
Rutowski, R.L. (2003) Visual ecology of adult butterflies. pp. 9–25 in Boggs, C.L., Watt, W.B. & Ehrlich, P.R. (Eds) Butterflies: Ecology and Evolution Taking Flight. Chicago, IL, The University of Chicago Press.Google Scholar
Sarto i Monteys, V. (2002) The discovery, description and taxonomy of Paysandisia archon (Burmeister, 1880), a castniid species recently found in southwestern Europe (Castniidae). Nota Lepidopterologica 25, 3–15.Google Scholar
Sarto i Monteys, V. & Aguilar, L. (2005) The Castniid Palm Borer, Paysandisia archon (Burmeister, 1880) in Europe: comparative biology, pest status and possible control methods (Lepidoptera: Castniidae). Nachrichten des Entomologischen Vereins Apollo 26, 61–94.Google Scholar
Sarto i Monteys, V., Acín, P., Rosell, G., Quero, C., Jiménez, M.A. & Guerrero, A. (2012) Moths behaving like butterflies. Evolutionary loss of long range attractant pheromones in castniid moths: a Paysandisia archon model. PLoS ONE 7, e29282.Google Scholar
Schulz, S., Beccaloni, G., Brown, K.S., Boppré, M., Freitas, A.V.L., Ockenfels, P. & Trigo, J.R. (2004) Semiochemicals derived from pyrrolizidine alkaloids in male ithomiine butterflies (Lepidoptera: Nymphalidae: Ithomiinae). Biochemical Systematics and Ecology 32, 699–713.Google Scholar
Scoble, M. (1986) The structure and affinities of the Hedyloidea: a new concept of the butterflies. Bulletin of the British Museum of Natural History (Entomology) 53, 251–286.Google Scholar
Scoble, M.J. & Aiello, A. (1990) Moth-like butterflies (Hedylidae: Lepidoptera): a summary, with comments on the egg. Journal of Natural History 24, 159–164.CrossRefGoogle Scholar
Scott, J.A. (1974) Mate-locating behavior of butterflies. American Midland Naturalist 91, 103–117.Google Scholar
Seitz, A. & Strand, E. (1913) Family Castniidae. pp. 5–19 in Seitz, A. (Ed.) The Macrolepidoptera of the World: The American Bombyces & Sphinges. Stuttgart, Alfred Kernen.Google Scholar
Sparks, A.N., Raulston, J.R., Lingren, P.D., Carpenter, J.E., Klun, J.A. & Mullinix, B.G. (1979) Field response of male Heliothis virescens to pheromonal stimuli and traps. Bulletin of the Entomological Society of America 25, 268–274.CrossRefGoogle Scholar
Subchev, M. (2014) Sex pheromone communication in the Family Zygaenidae (Insecta: Lepidoptera): a review. Acta Zoologica Bulgarica 66, 147–157.Google Scholar
Tarmann, G.M. (2004) Zygaenid Moths of Australia. A Revision of the Australian Zygaenidae (Procridinae: Artonini). Collingwood, Australia, CSIRO Publishing, 248 pp.Google Scholar
Tatjanskaitë, L. (1995) Pheromone gland of the clearwing, Synanthedon tipuliformis Cl., and Paranthrene tabaniformis kungessana Alph., females (Lepidoptera, Sesiidae). Pheromones 5, 53–60.Google Scholar
Toshova, T.B., Subchev, M.A. & Tóth, M. (2007) Role of olfactory and visual stimuli in the mating behaviour of male vine bud moths, Theresimima ampellophaga (Lepidoptera: Zygaenidae). European Journal of Entomology 104, 57–65.CrossRefGoogle Scholar
Trigo, J.R., Barata, L.E.S. & Brown, K.S. (1994) Stereochemical inversion of pyrrolizidine alkaloids by Mechanitis polymnia (Lepidoptera: Nymphalidae: Ithomiinae): specificity and evolutionary significance. Journal of Chemical Ecology 20, 2883–2899.Google Scholar
van Nieukerken, E.J., Kaila, L., Kitching, I.J., Kristensen, N.P., Lees, D.C., Minet, J., Mitter, C., Mutanen, M., Regier, J.C., Simonsen, T.J., Wahlberg, N., Yen, S.-H., Zahiri, R., Adamski, D., Baixeras, J., Bartsch, D., Bengtsson, B.A., Brown, J.W., Bucheli, S.R., Davis, D.R., De Prins, J., De Prins, W., Epstein, M.E., Gentili-Poole, P., Gielis, C., Hättenschwiler, P., Hausmann, A., Holloway, J.D., Kallies, A., Karsholt, O., Kawahara, A.Y., Koster, S.J.C., Kozlov, M.V., Lafontaine, J.D., Lamas, G., Landry, J.-F., Lee, S., Nuss, M., Park, K.-T., Penz, C., Rota, J., Schintlmeister, A., Schmidt, B.C., Sohn, J.-C., Solis, M.A., Tarmann, G.M., Warren, A.D., Weller, S., Yakovlev, R.V., Zolotuhin, V.V. & Zwick, A. (2011) Order Lepidoptera Linnaeus, 1758 pp. 237 pp in Zhang, Z.-Q. (Ed.) Animal Biodiversity: an Outline of Higher-level Classification and Survey of Taxonomic Richness. Zootaxa (3148). New Zealand, Magnolia Press.Google Scholar
Vassiliou, V. & Sarto i Monteys, V. (2014) Checking the Mating Behaviour of the Palm Borer Paysandisia Archon (Lepidoptera: Castniidae) Using Cossid's Leopard Moth Zeuzera pyrina Pheromone. X European Congress of Entomology. UK, University of York.Google Scholar
Warrant, E., Kelber, A. & Kristensen, N.P. (2003) Eyes and vision. pp. 325–359 in Kristensen, N.P. (Ed.) Lepidoptera, Moths and Butterflies. Berlin, Walter de Gruyter.Google Scholar
Wickman, P.-O. & Wiklund, C. (1983) Territorial defence and its seasonal decline in the speckled wood butterfly (Pararge aegeria). Animal Behaviour 31, 1206–1216.Google Scholar
Wiklund, C. (2003) Sexual selection and the evolution of butterfly mating systems. pp. 67–90 in Boggs, C.L., Watt, W.B. & Ehrlich, P.R. (Eds) Butterflies: Ecology and Evolution Taking Flight. Chicago, IL, The University of Chicago Press.Google Scholar
Zagatti, P. & Renou, M. (1984) Les pheromones sexuelles des zygènes. Le comportement de Zygaena filipendulae L. (Lepidoptera, Zygaenidae). Annales de la Societé Entomologique de France 20, 439–454.Google Scholar
Zagatti, P., Kunesch, G., Ramiandrasoa, F., Malosse, C., Hall, D.R., Lester, R. & Nesbitt, B.F. (1987) Sex pheromones of rice moth, Corcyra cephalonica Stainton. I. Identification of male pheromone. Journal of Chemical Ecology 13, 1561–1573.Google Scholar