To lay or not to lay: Oviposition of Maculinea arion in relation to Myrmica ant presence and host plant phenology

Animal Behaviour

Volumn 82, Issue 4, 2011, Pages 791-799

  Patricelli, Dario ^a   Barbero, Francesca ^a   La Morgia, Valentina ^a   Casacci, Luca P ^a   Witek, Magdalena ^a   Balletto, Emilio ^a   Bonelli, Simona ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Host selection; Maculinea; Myrmecophily; Origanum vulgare; Oviposition; Social parasite

Indexed keywords

ANT; BUTTERFLY; ENVIRONMENTAL FACTOR; EVOLUTIONARY BIOLOGY; FITNESS; FLOWER VISITING; HOST PLANT; HOST SELECTION; LARVA; LIFE CYCLE; MYRMECOPHILY; NEST SITE; OBLIGATE BEHAVIOR; OVIPOSITION; PERSISTENCE; PHENOLOGY; SOCIAL INSECT; SURVIVAL; WORKER CASTE;

FORMICIDAE; MACULINEA; MACULINEA ARION; MYRMICA; ORIGANUM; ORIGANUM VULGARE; PAPILIONOIDEA;

EID: 80052737224     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2011.07.011     Document Type: Article

References (69)

1. Aebischer N.J., Robertson P.A., Kenward R.E. Compositional analysis of habitat use from animal radiotracking data. Ecology 1993, 74:1313-1325.
2. Akino T., Knapp J.J., Thomas J.A., Elmes G.W. Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proceedings of the Royal Society B 1999, 266:1419-1426.
3. Atsatt P.R. Ant dependent food plant selection by the mistletoe butterfly Ogyris amaryllis (Lycaenidae). Oecologia 1981, 48:60-63.
4. Barbero F., Thomas J.A., Bonelli S., Balletto E., Schönrogge K. Queen ants make distinctive sounds that are mimicked by a butterfly social parasite. Science 2009, 323:782-785.
5. Baylis M., Pierce N.E. The effect of host-plant quality on the survival of larvae and oviposition by adults of an ant-tended lycaenid butterfly, Jalmenus evagoras. Ecological Entomology 1991, 16:1-9.
6. Binzenhöfer B., Schröder B., Strauss B., Biedermann R., Settele J. Habitat models and habitat connectivity analysis for butterflies and burnet moths: the example of Zygaena carniolica and Coenonympha arcania. Biological Conservation 2005, 126:247-259.
7. Bolker B.M., Brooks M.E., Clark C.J., Geange S.W., Poulsen J.R., Stevens M.H.H., White J.S.S. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 2008, 24:127-135.
8. Bonelli S., Crocetta A., Barbero F., Balletto E. Oviposition behaviour in the myrmecophilous butterfly Maculinea alcon (Lepidoptera: Lycaenidae). Vol. 2 Species Ecology along a European Gradient: Maculinea Butterflies as a Model 2005, 65-68. J. Pensoft, Sofia-Moscow. J. Settele, E. Kühn, J.A. Thomas (Eds.).
9. Braun-Blanquet J. Plant Sociology: the Study of Plant Communities 1932, McGraw Hill, New York.
10. Burnham K.P., Anderson D.R. Model Selection and Multimodel Inference: a Practical Information-theoretic Approach 2002, Springer-Verlag, New York. 2nd edn.
11. Casacci L.P., Witek M., Barbero F., Patricelli D., Solazzo G., Balletto E., Bonelli S. Habitat preferences of Maculinea arion and its Myrmica host ants: implications for habitat management in Italian Alps. Journal of Insect Conservation 2011, 15:103-110.
12. Calenge C. The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecological Modelling 2006, 197:516-519.
13. Czechowski W., Radchenko A., Czechowska W. The Ants (Hymenoptera, Formicidae) of Poland 2002, Museum and Institute of Zoology PAS, Warsaw.
14. Diggle P., Heagerty P., Liang K., Zeger S. Analysis of Longitudinal Data 2002, Oxford University Press, Oxford. 2nd edn.
15. Elmes G.W., Thomas J.A., Wardlaw J.C. Larvae of Maculinea rebeli, a large blue butterfly, and their Myrmica host ants: wild adoption and behaviour in ant-nests. Journal of Zoology 1991, 223:447-460.
16. Elmes G.W., Thomas J.A., Wardlaw J.C., Hochberg M.E., Clarke R.T., Simcox D.J. The ecology of Myrmica ants in relation to the conservation of Maculinea butterflies. Journal of Insect Conservation 1998, 2:67-78.
17. Elmes G.W., Akino T., Thomas J.A., Clarke R.T., Knapp J.J. Interspecific differences in cuticular hydrocarbon profiles of Myrmica ants are sufficiently consistent to explain host specificity by Maculinea (large blue) butterflies. Oecologia 2002, 130:525-535.
18. Fraser A.M., Tregenza T., Wedell N., Elar M.A., Pierce N.E. Oviposition tests of ant preference in a myrmecophilous butterfly. Journal of Evolutionary Biology 2002, 15:861-870.
19. Fraser A.M., Mutsaers A.P., Bullard B., Beckett J.S., Hofferberth J.E. Butterfly olfactory responses to ant volatiles: potential cues for host ant recognition in the obligately ant-associated butterfly Jalmenus evagoras (Lepidoptera: Lycaenidae). Proceedings of the 24th International Society of Chemical Ecology Meeting, 17-22 August 2008 2008, International Society of Chemical Ecology, State College, Pennsylvania, page 114. J. Todd (Ed.).
20. Fürst M.A., Nash D.R. Host ant independent oviposition in the parasitic butterfly Maculinea alcon. Biology Letters 2009, 6:174-176.
21. Garcia Barros E., Fartmann T. Butterfly oviposition: sites, behaviour, modes. Ecology of Butterflies in Europe 2009, 29-42. Cambridge University Press, Cambridge. J. Settele, T. Shreeve, M. Konvička, H. Van Dyck (Eds.).
22. Gillies C.S., Hebblewhite M., Nielsen S.E., Krawchuk M.A., Aldridge C.L., Frair J.L., Saher D.J., Stevens C.E., Jerde C.L. Application of random effects to the study of resource selection by animals. Journal of Animal Ecology 2006, 75:887-898.
23. Hofferberth J.E., Beckett J.S., Beckett J.D., Fraser A.M. Synthesis and GC-EAD analysis of semiochemicals putatively used by the obligately ant-associated butterfly Jalmenus evagoras in host ant selection. Proceedings of the 24th International Society of Chemical Ecology Meeting, 17-22 August 2008 2008, International Society of Chemical Ecology, State College, Pennsylvania, page 115. J. Todd (Ed.).
24. Johnson D.H. The comparison of usage and availability measurements for evaluating resource preference. Ecology 1980, 61:65-71.
25. Johnson J.B., Omland K.S. Model selection in ecology and evolution. Trends in Ecology & Evolution 2004, 19:101-108.
26. Jordano D., Rodŕiguez J., Thomas C.D., Fernández H.J. The distribution and density of a lycaenid butterfly in relation to Lasius ants. Oecologia 1992, 91:439-446.
27. Jutzeler D. Kann das Weibchen von Plebejus argus (Linnaeus, 1761) Ameisen riechen? (Lepidoptera, Lycaenidae). Mitteilungen Entomologischen Gesellschaft Basel 1989, 39:150-159.
28. Manly B.F.J., McDonald L.L., Thomas D.L., McDonald T.L., Erickson W.P. Resource Selection by Animals. Statistical Design and Analysis for Field Studies 2002, Kluwer Academic, Dordrecht. 2nd edn.
29. Meyer M., Zeileis A., Hornik K. vcd: Visualizing Categorical Data. R package version 1.2-9 2010, http://cran.r-project.org/web/packages/vcd/index.html.
30. Mouquet N., Thomas J.A., Elmes G.W., Clarcke R.T., Hochberg M.E. Population dynamics and conservation of a specialized predator: a case study of Maculinea arion. Ecological Monographs 2005, 75:525-542.
31. Musche M., Anton C., Worgan A., Settele J. No experimental evidence for host ant related oviposition in a parasitic butterfly. Journal of Insect Conservation 2006, 19:631-643.
32. Munguria M.L., Martin J. Action Plan for the Maculinea Butterflies in Europe 1997, Council of Europe Publishing, Strasbourg.
33. Nowicki P., Witek M., Skórka P., Woyciechowski M. Oviposition patterns in the myrmecophilous butterfly Maculinea alcon Denis & Schiffermüller (Lepidoptera: Lycaenidae) in relation to characteristics of food plant and presence of ant hosts. Polish Journal of Ecology 2005, 53:409-417.
34. Nowicki P., Witek M., Karwowski K., Woyciechowski M. Myrmekofilne motyle z rodzaju Maculinea (Lycaenidae, Lepidoptera) w Pienińskim Parku Narodowym i jego otoczeniu [Myrmecophilous butterflies of the genus Maculinea in the Pieniny National Park and its surrounding]. Pieniny-Przyroda i Człowiek 2006, 9:11-112.
35. Nowicki P., Pe{ogonek}pkowska A., Kudłek J., Skórka P., Witek M., Settele J., Woyciechowski M. From metapopulation theory to conservation recommendations: lessons from spatial occurrence and abundance patterns of Maculinea butterflies. Biological Conservation 2007, 140:119-129.
36. Nowicki P., Bonelli S., Barbero F., Balletto E. Relative importance of density-dependent regulation and environmental stochasticity for butterfly population dynamics. Oecologia 2009, 161:227-239.
37. Pech P., Fric Z., Konvicka M. Species-specificity of the Phengaris (Maculinea) - Myrmica host system: fact or myth? (Lepidoptera: Lycaenidae; Hymenoptera: Formicidae). Sociobiology 2007, 50:1-21.
38. Pierce N.E. Predatory and parasitic Lepidoptera: carnivores living on plants. Journal of the Lepidopterist's Society 1995, 49:412-453.
39. Pierce N.E., Elgar M.A. The influence of ants on host plant selection by Jalmenus evagorus, a myrmecophilous lycaenid butterfly. Behavioral Ecology and Sociobiology 1985, 21:237-248.
40. Pierce N.E., Braby M.F., Heath A., Lohman D.J., Mathew J., Rand D.B., Travassos M.A. The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annual Review of Entomology 2002, 47:733-771.
41. R Development Core Team R: A Language and Environment for Statistical Computing 2010, R Foundation for Statistical Computing, Vienna. http://www.R-project.org.
42. Renwick J.A.A., Chew F.S. Oviposition behaviour in Lepidoptera. Annual Review of Entomology 1994, 39:377-400.
43. Scheper M., Van der Made J.G., Wynhoff I. Maculinea alcon: interactions between a myrmecophilous butterfly its larval foodplant and its host ant. Proceedings of the Experimental and Applied Entomology NEV Amsterdam 1995, 6:77-78.
44. Schönrogge K., Wardlaw J.C., Peters A.J., Everett S., Thomas J.A., Elmes G.W. Changes in chemical signature and host specificity from larval retrievial to full social integration in the myrmecophilous butterfly Maculinea rebeli. Journal of Chemical Ecology 2004, 30:91-107.
45. Scoble M.J. The Lepidoptera: Form, Function and Diversity 1995, Oxford University Press, Oxford.
46. Scrucca L. qcc: an R package for quality control charting and statistical process control. R News 2004, 4:11-17.
47. Seymour A.S., Gutiérrez D., Jordano D. Dispersal of the lycaenid Plebejus argus in response to patches of its mutualist ant Lasius niger. Oikos 2003, 103:162-174.
48. Settele J., Kühn E. Insect conservation. Science 2009, 325:41-42.
49. Sielezniew M., Stankiewicz A. Myrmica sabuleti (Hymenoptera: Formicidae) not necessary for the survival of the population of Phengaris (Maculinea) arion (Lepidoptera: Lycaenidae) in eastern Poland: lower host-ant specificity or evidence for geographical variation of an endangered social parasite?. European Journal of Entomology 2008, 105:637-641.
50. Sielezniew M., Dziekańska I., Stankiewicz-Fiedurek A.M. Multiple host-ant use by the predatory social parasite Phengaris (=Maculinea) arion (Lepidoptera, Lycaenidae). Journal of Insect Conservation 2010, 14:141-149.
51. Sielezniew M., Włostowski M., Dziekańska I. Myrmica schencki (Hymenoptera: Formicidae) as the primary host of Phengaris (Maculinea) arion (Lepidoptera: Lycaenidae) at heathlands in eastern Poland. Sociobiology 2010, 55:95-106.
52. Sielezniew M., Patricelli D., Dziekańska I., Barbero F., Bonelli S., Casacci L.P., Witek M., Balletto E. The first record of Myrmica lonae (Hymenoptera: Formicidae) as a host of the socially parasitic large blue butterfly Phengaris (Maculinea) arion (Lepidoptera: Lycaenidae). Sociobiology 2010, 56:465-475.
53. Smiley J.T., Atsatt P.R., Pierce N.E. Local distribution of the lycaenid butterfly Jalmenus evagoras, in response to host ants and plants. Oecologia 1988, 76:416-422.
54. Stankiewicz A., Sielezniew M. Host specificity of Maculinea teleius Bgstr. and M. nausithous Bgstr. (Lepidoptera:Lycaenidae). The new insight. Annales Zoologici 2002, 52:403-408.
55. Thomas J.A. The behaviour and habitat requirements of Maculinea nausithous (the dusky large blue butterfly) and M. teleius (the scarce large blue) in France. Biological Conservation 1984, 28:325-347.
56. Thomas J.A. Larval niche selection and evening exposure enhance adoption of a predacious social parasite, Maculinea arion (large blue butterfly) by Myrmica ants. Oecologia 2002, 132:531-537.
57. Thomas J.A., Elmes G.W. Higher productivity at the cost of increased host-specificity when Maculinea butterfly larvae exploit ant colonies through trophallaxis rather than by predation. Ecological Entomology 1998, 23:457-464.
58. Thomas J.A., Elmes G.W. Food-plant niche selection rather than the presence of ant nests explains oviposition patterns in the myrmecophilous butterfly genus Maculinea. Proceedings of the Royal Society B 2001, 268:471-477.
59. Thomas J.A., Wardlaw J.C. The capacity of a Myrmica ant nest to support a predacious species of Maculinea butterfly. Oecologia 1992, 91:101-109.
60. Thomas J.A., Elmes G.W., Wardlaw J.C., Woyciechowski M. Host specificity among Maculinea butterflies in Myrmica ant nests. Oecologia 1989, 79:452-457.
61. Thomas J.A., Simcox D.J., Warlaw J.C., Elmes G.W., Hochberg M.E., Clarke R.T. Effects of latitude, altitude and climate on the habitat and conservation of the endangered butterfly Maculinea arion and its Myrmica ant hosts. Journal of Insect Conservation 1998, 2:39-46.
62. Thompson J.N., Pellmyr O. Evolution of oviposition behaviour and host preference in Lepidoptera. Annual Review of Entomology 1991, 36:65-89.
63. Van Dyck H., Regniers S. Egg spreading in the ant-parasitic butterfly, Maculinea alcon: from individual behaviour to egg distribution pattern. Animal Behaviour 2010, 80:621-627.
64. Van Dyck H., Talloen W., Oostermeijer J.G.B., Feenstra V., Van der Hidde A., Wynhoff I. Does the presence of ant nests matter for oviposition to a specialized myrmecophilous Maculinea butterfly?. Proceedings of the Royal Society B 2000, 267:861-866.
65. Van Swaay C., Cuttelod A., Collins S., Maes D., Lopez Munguira M., Šašić M., Settele J., Verovnik R., Verstrael T., Warren M., et al. European Red List of Butterfies 2010, Publications Office of the European Union, Luxembourg.
66. Witjes S., Eltz T. Hydrocarbon footprints as a record of bumblebee flower visitation. Journal of Chemical Ecology 2009, 35:1320-1325.
67. Witek M., Śliwińska E.B., Skórka P., Nowicki P., Wantuch M., Vrabec V., Settele J., Woyciechowski M. Host ant specificity of large blue butterflies Phengaris (Maculinea) (Lepidoptera: Lycaenidae) inhabiting humid grasslands of East-central Europe. European Journal of Entomology 2008, 105:871-877.
68. Wynhoff I., Grutters M., Van Langevelde F. Looking for the ants: selection of oviposition sites by two myrmecophilous butterfly species. Animal Biology 2008, 58:371-388.
69. Zuur A.F., Ieno E.N., Walker N., Saveliev A.A., Smith G.M. Mixed Effects Models and Extensions in Ecology with R 2009, Springer, New York.