Behavioural evidence for a putative oviposition-deterring pheromone in the butterfly, Phengaris (Maculinea) teleius (Lepidoptera: Lycaenidae)

European Journal of Entomology

Volumn 110, Issue 1, 2013, Pages 71-80

  Sielezniew, Marcin ^a   Stankiewicz Fiedurek, Anna M ^b  

^a WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^b MUSEUM AND INSTITUTE OF ZOOLOGY   (Poland)

Author keywords

Host plant marking behaviour; Host plant selection; Maculinea teleius; Myrmecophily; Oviposition; Oviposition deterring pheromone; Phengaris teleius; Sanguisorba officinalis; Social parasite

Indexed keywords

ABUNDANCE; ANT; BUTTERFLY; FEEDING BEHAVIOR; FOOD PREFERENCE; HERB; HOST SELECTION; OVIPOSITION; PHEROMONE;

EID: 84875074611     PISSN: 12105759     EISSN: 18028829     Source Type: Journal    
DOI: 10.14411/eje.2013.009     Document Type: Article

References (69)

1. ANDERSON P. 2002: Oviposition pheromones in herbivorous and carnivorous insects. Hilker M. & Meiners T. (eds): Chemoecology of Insect Eggs and Egg Deposition. Blackwell, Oxford, pp. 235-264.
2. ÁRNYAS E., BERECZKI J., TÓTH A., VARGA K., PECSENYE K., TARTALLY A., KÖVICS G., KARSA D. & VARGA Z. 2009: Oviposition preferences of Maculinea alcon as influenced by aphid (Aphis gentianae) and fungal (Puccinia gentianae) infestation of larval host plants. - Ecol. Entomol. 34: 90-97.
3. BUSZKO J., SIELEZNIEW M. & STANKIEWICZ A.M. 2005: The distribution and ecology of Maculinea teleius and M. nausithous in Poland. In Settele J., Kühn E. & Thomas J.A. (eds): Studies on the Ecology and Conservation of Butterflies in Europe. Vol. 2: Species Ecology along a European Gradient: Maculinea Butterflies as a Model. Pensoft, Sofia, Moscow, pp. 210-213.
4. DEMPSTER J.P. 1992: Evidence of an oviposition-deterring pheromone in the orange-tip butterfly, Anthocharis cardamines (L.). - Ecol. Entomol. 17: 83-85.
5. DEVRIES P.J. & PENZ C.M. 2000: Entomophagy, behavior, and elongated thoracic legs in the myrmecophilous neotropical butterfly Alesa amesis (Riodinidae). - Biotropica 32: 712-721.
6. EBERT G. & RENNWALD E. 1991: Die Schmetterlinge Baden-Württembergs, Vol. 1 & 2, Tagfalter I & II. Eugen Ulmer, Stuttgart, 552 + 535 pp.
7. ELMES G.W. & THOMAS J.A. 1992: Complexity of species conservation in managed habitats: Interactions between Maculinea butterflies and their ant hosts. - Biodiv. Conserv. 1: 155-169.
8. ELMES G.W., THOMAS J.A., WARDLAW J.C., HOCHBERG M.E., CLARKE R.T. & SIMCOX D.J. 1998: The ecology of Myrmica ants in relation to the conservation of Maculinea butterflies. - J. Insect Conserv. 2: 67-78.
9. FIGURNY E. & WOYCIECHOWSKI M. 1998: Flowerhead selection for oviposition by females of the sympatric butterfly species Maculinea nausithous and M. teleius (Lepidoptera, Lycaenidae). - Entomol. Gen. 23: 215-222.
10. FRIC Z., WAHLBERG N., PECH P. & ZRZAVÝ J. 2007: Phylogeny and classification of the Phengaris-Maculinea clade (Lepidoptera: Lycaenidae): total evidence and phylogenetic species concepts. - Syst. Entomol. 32: 558-567.
11. FÜRST M.A. & NASH D.R. 2009: Host ant independent oviposition in the parasitic butterfly Maculinea alcon. - Biol. Lett. 6: 174-176.
12. GARCÍA-BARROS E. & FARTMANN T. 2009: Butterfly oviposition: sites, behaviour and modes. In Settele J., Shreeve T.G., Konvicka M. & Van Dyck H. (eds): Ecology of Butterflies in Europe. Cambridge University Press, Cambridge, pp. 29-42.
13. GOULSON D. & CORY J.S. 1993: Flower constancy and learning in foraging preferences of the green-veined white butterfly Pieris napi. - Ecol. Entomol. 18: 315-320.
14. GOULSON D., OLLERTON J. & SLUMAN C. 1997: Foraging strategies in the small skipper butterfly, Thymelicus flavus; when to switch? - Anim. Behav. 53: 1009-1016.
15. JAENIKE J. 1990: Host specialization in phytophagous insects. - Annu. Rev. Ecol. Syst. 21: 243-273.
16. JORDANO D., RODRIGUEZ J., THOMAS C.D. & HAEGER J.F. 1992: The distribution and density of a lycaenid butterfly in relation to Lasius ants. - Oecologia 91: 439-446.
17. KEVAN P.G. & BAKER H.G. 1983: Insects as flower visitors and pollinators. - Annu. Rev. Entomol. 28: 407-453.
18. KLIJNSTRA J.W. & ROESSINGH P. 1986: Perception of the oviposition deterring pheromone by tarsal and abdominal contact chemoreceptors in Pieris brassicae. - Entomol. Exp. Appl. 40: 71-79.
19. MCNEELY C. & SINGER M.C. 2001: Contrasting the roles of learning in butterflies foraging for nectar and oviposition sites two. - Anim. Behav. 65: 847-852.
20. MUNGUIRA M.L., GARCÍA-BARROS E. & CANO J.M. 2009: Butterfly herbivory and larval ecology. In Settele J., Shreeve T.G., Konvicka M. & Van Dyck H. (eds): Ecology of Butterflies in Europe. Cambridge University Press, Cambridge, pp. 43-54.
21. MUSCHE M., ANTON C., WORGAN A. & SETTELE J. 2006: No experimental evidence for host ant related oviposition in a parasitic butterfly. - J. Insect Behav. 19: 631-643.
22. NOWICKI P., WITEK M., SKÓRKA P. & WOYCIECHOWSKI M. 2005a: Oviposition patterns in the myrmecophilous butterfly Maculinea alcon Denis & Schiffermüller (Lepidoptera: Lycaenidae) in relation to characteristics of foodplants and presence of ant hosts. - Pol. J. Ecol. 53: 105-111.
23. NOWICKI P., WITEK M., SKÓRKA P., SETTELE J. & WOYCIECHOWSKI M. 2005b: Population ecology of the endangered butterflies Maculinea teleius and M. nausithous, and its implications for conservation. Popul. Ecol. - 47: 409-417.
24. NUFIO C.R. & PAPAJ D.R. 2001: Host marking behavior in phytophagous insects and parasitoids. - Entomol. Exp. Appl. 99: 273-293.
25. PAPAJ D.R. & RAUSHER M.D. 1987: Genetic differences and phenotype plasticity as causes of variation in oviposition preference in Battus philenor. - Oecologia 74: 24-30.
26. PATRICELLI D., BARBERO F., LA MORGIA V., CASACCI L.P., WITEK M., BALLETTO E. & BONELLI S. 2011: To lay or not to lay: oviposition of Maculinea arion in relation to Myrmica ant presence and host plant phenology. - Anim. Behav. 82: 791-799.
27. PFEIFER M.A., ANDRICK U.R., FREY W. & SETTELE J. 2000: On the ethology and ecology of a small and isolated population of the Dusky Large Blue Butterfly Glaucopsyche (Maculinea) nausithous (Bergsträsser, 1779) (Lep., Lycaenidae). - Nota Lep. 23: 147-172.
28. PIERCE N.E. & ELGAR M.A. 1985: The influence of ants on host plant selection by Jalmenus evagoras, a myrmecophilous lycaenid butterfly. - Behav. Ecol. Sociobiol. 16: 202-222.
29. PIERCE N.E., BRABY M.F., HEATH A., LOHMAN D.J., MATHEW J., RAND D.B. & TRAVASSOS M.A. 2002: The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). - Annu. Rev. Entomol. 47: 733-771.
30. PILSON D. & RAUSHER M.D. 1988: Clutch size adjustment by a swallowtail butterfly. - Nature 333: 361-363.
31. PORTER K. 1982: Basking behaviour in larvae of the butterfly Euphydryas aurinia. - Oikos 38: 308-312.
32. RENWICK J.A.A. & CHEW F.S. 1994: Oviposition behavior in Lepidoptera. - Annu. Rev. Entomol. 39: 377-400.
33. ROITBERG B.D. & PROKOPY R.J. 1981: Experience required for pheromone recognition by the apple maggot fly. - Nature 292: 540-541.
34. ROITBERG B.D. & PROKOPY R.J. 1987: Insects that mark host plants. - BioScience 37: 400-406.
35. SATO Y., YANO S., TAKABAYASHI J. & OHSAKI N. 1999: Pieris rapae (Lepidoptera: Pieridae) females avoid oviposition on Rorippa indica plants infested by conspecific larvae. - Appl. Entomol. Zool. 34: 333-337.
36. SCHOONHOVEN L.M. 1990: Host-marking pheromones in Lepidoptera, with special reference to two Pieris spp. - J. Chem. Ecol. 16: 3043-3052.
37. SCHOONHOVEN L.M. & ROTHSCHILD M. 1977: Assessment of egg load by Pieris brassicae (Lepidoptera: Pieridae). - Nature 266: 352-355.
38. SCHOONHOVEN L.M., BEERLING E.A.M., BRAAKSMA R. & VAN VUGT Y. 1990a: Does the imported cabbageworm, Pieris rapae, use an oviposition deterring pheromone? - J. Chem. Ecol. 16: 1649-1655.
39. SCHOONHOVEN L.M., BEERLING E.A.M., KLIJNSTRA J.W. & VAN VUGT Y. 1990b: Two related butterfly species avoid oviposition near each other's eggs. - Experienta 46: 526-528.
40. SETTELE J., KÜHN E. & THOMAS J.A. (eds) 2005: Studies on the Ecology and Conservation of Butterflies in Europe. Vol. 2: Species Ecology along a European Gradient: Maculinea Butterflies as a Model. Pensoft, Sofia, Moscow, 250 pp.
41. SIELEZNIEW M. & STANKIEWICZ A.M. 2007: Differences in the development of the closely related myrmecophilous butterflies Maculinea alcon and M. rebeli (Lepidoptera: Lycaenidae). - Eur. J. Entomol. 104: 433-444.
42. STANKIEWICZ A. & SIELEZNIEW M. 2002: Host specificity of Maculinea teleius Bgstr. and M. nausithous Bgstr. (Lepidoptera: Lycaenidae). The new insight. - Ann. Zool. 52: 403-408.
43. STANTON M.L. 1984: Short-term learning and the searching accuracy of egg laying butterflies. - Anim. Behav. 32: 33-40.
44. STETTMER C., BINZENHÖFER B. & HARTMANN P. 2001: Habitatmanagement und Schutzmaßnahmen für die Ameisenbläulinge Glaucopsyche teleius und Glaucopsyche nausithous, Teil 2: Habitatansprüche, Gefährdung und Pflege. Nat. Landsch. - 76: 366-375
45. TARTALLY A. & VARGA Z. 2008: Host ant use of Maculinea teleius in the Carpathian Basin (Lepidoptera: Lycaenidae). - Acta Zool. Acad. Sci. Hung. 54: 257-268.
46. THOMAS J.A. 1984: The behaviour and habitat requirements of Maculinea nausithous (the Dusky Large Blue Butterfly) and M. teleius (the Scarce Large Blue) in France. - Biol. Conserv. 28: 325-347.
47. THOMAS J.A. 1995: The ecology and conservation of Maculinea arion and other European species of large blue butterfly. In Pullin A.S. (ed.): Ecology and Conservation of Butterflies. Chapman and Hall, pp. 180-197.
48. THOMAS J.A. & ELMES G.W. 1998: Higher productivity at the cost of increased host-specificity when Maculinea butterfly larvae exploit ant colonies through trophallaxis rather than by predation. - Ecol. Entomol. 23: 457-464.
49. THOMAS J.A. & ELMES G.W. 2001: Food-plant niche selection rather than the presence of ant nests explains oviposition patterns in the myrmecophilous butterfly genus Maculinea. - Proc. R. Soc. Lond. (B) 268: 471-477.
50. THOMAS J.A. & LEWINGTON R. 2010: The Butterflies of Great Britain & Ireland. British Wildlife Publishing, Milton on Stour, 288 pp.
51. THOMAS J.A. & SETTELE J. 2004: Butterfly mimics of ants. - Nature 432: 283-284.
52. THOMAS J.A. & WARDLAW J.C. 1992: The capacity of a Myrmica ant nest to support a predacious species of Maculinea butterfly. - Oecologia 91: 101-109.
53. THOMAS J.A., ELMES G.W., WARDLAW J.C. & WOYCIECHOWSKI M. 1989: Host specificity among Maculinea butterflies in Myrmica ant nests. - Oecologia 79: 452-457.
54. THOMAS J.A., ELMES G.W., SCHÖNROGGE K., SIMCOX D.J. & SETTELE J. 2005: Primary hosts, secondary hosts and "non-hosts": common confusions in the interpretation of host specificity in Maculinea butterflies and other social parasites of ants. In Settele J., Kühn E. & Thomas J.A. (eds): Studies on the Ecology and Conservation of Butterflies in Europe. Vol. 2: Species Ecology along a European Gradient: Maculinea Butterflies as a Model. Pensoft, Sofia, Moscow, pp. 99-104.
55. THOMPSON J.N. & PELLMYR O. 1991: Evolution of oviposition behavior and host preference in Lepidoptera. - Annu. Rev. Entomol. 36: 65-89.
56. TOLMAN T. & LEWINGTON R. 2009: Collins Butterfly Guide of Britain and Europe. Harper Collins, London, 400 pp.
57. VAN DYCK H. & REGNIERS S. 2010: Egg spreading in the antparasitic butterfly, Maculinea alcon: from individual behaviour to egg distribution pattern. - Anim. Behav. 80: 621-627.
58. VAN DYCK H., TALLOEN W., OOSTERMEIJER J.G.B., FEENSTRA V., VAN DER HIDDE A. & WYNHOFF I. 2000: Does the presence of ant nests matter for oviposition to a specialized myrmecophilous Maculinea butterfly? - Proc. R. Soc. Lond. (B) 267: 861-866.
59. VAN LANGEVELDE F. & WYNHOFF I. 2009: What limits the spread of two congeneric butterfly species after their reintroduction: quality or spatial arrangement of habitat? - Anim. Conserv. 12: 540-548.
60. VAN SWAAY C.A.M. & WARREN M.S. 1999: Red Data Book of European Butterflies (Rhopalocera). Nature and Environment, No. 99. Council of Europe Publishing, Strasbourg, 260 pp.
61. VASCONCELLOS-NETO J. & MONTEIRO R.F. 1993: Inspection and evaluation of host-plant by the butterfly Mechanitis lysimnia (Nymph., Ithomiinae) before laying eggs: a mechanism to reduce intraspecific competition. - Oecologia 95: 431-438.
62. WEISS M.R. & PAPAJ D.R. 2003: Colour learning in two behavioral contexts: How much can a butterfly keep in mind? - Anim. Behav. 65: 425-434.
63. WIKLUND C. 1984: Egg-laying patterns in butterflies in relation to their phenology and the visual apparency and abundance of their host-plants. - Oecologia 63: 23-29.
64. WITEK M., NOWICKI P., ŚLIWIŃSKA E.B., SKÓRKA P., MOROŃ D., SETTELE J., SCHONROGGE K. & WOYCIECHOWSKI M. 2010: Local host ant specificity of Maculinea teleius butterfly, a obligatory social parasite of Myrmica ants. - Ecol. Entomol. 35: 557-564.
65. WITEK M., ŚLIWIŃSKA E., SKÓRKA P., NOWICKI P., SETTELE J. & WOYCIECHOWSKI M. 2006: Polymorphic growth in larvae of Maculinea butterflies, as an example of biennialism in myrmecophilous insects. - Oecologia 148: 729-733.
66. WITEK M., ŚLIWIŃSKA E.B., SKÓRKA P., NOWICKI P., WANTUCH M., VRABEC V., SETTELE J. & WOYCIECHOWSKI M. 2008: Host ant specificity of Large Blue butterflies Phengaris (Maculinea) (Lepidoptera: Lycaenidae) inhabiting humid grasslands in East-central Europe. - Eur. J. Entomol. 105: 871-877.
67. WYNHOFF I. 1996: Maculinea teleius (Bergstr., 1779). In Van Helsdingen P.J., Willemse L. & Speight M.C.D. (eds): Back-ground Information on Invertebrates of the Habitats Directive and the Bern Convention. Part I - Crustacea, Coleoptera and Lepidoptera. Nature and Environment No 79. Council of Europe Publishing, Strasbourg, pp. 172-179.
68. WYNHOFF I. 2001: At Home on Foreign Meadows: The Reintroduction of two Maculinea Butterfly Species. Ph.D. thesis, Wageningen Agricultural University.
69. WYNHOFF I., GRUTTERS M. & VAN LANGEVELDE F. 2008: Looking for the ants: selection of oviposition sites by two myrmecophilous butterfly species. - Anim. Biol. 58: 371-388.