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From Africa to the Alps: risk assessment on an invasion by Cacyreus marshalli (Butler, 1898)

  • Paradiso Federica
  • Martelli Francesca
  • Cerrato Cristiana
  • Ghidotti SilviaEmail author
  • Viterbi Ramona
  • Canterino Sara
  • Ferracini Chiara
  • Bonelli Simona
ORIGINAL PAPER
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Abstract

Cacyreus marshalli (Butler, 1898) is the only alien butterfly species in Italy, introduced from Southern Africa via the trade of ornamental Pelargonium plants (family Geraniaceae). In 2008, Quacchia and colleagues demonstrated that if Pelargonium plants are not available, females can lay eggs on Geranium spp., developing fertile offspring. C. marshalli is a thermophilous species, but in recent years some adults have been observed flying far from villages and at high altitudes (up to 2400 m a.s.l.) in the Orco valley (Gran Paradiso National Park, Aosta Valley). Due to the potential threat to native Geranium-consuming lycaenids and to evaluate the risk of naturalisation, we investigated: (i) dispersal abilities of gravid females, outside the National Park to avoid accidental establishment of the invasive species; (ii) pelargonium distribution and abundance; (iii) oviposition behaviour and preimaginal distribution; (iv) citizen care practices with pelargoniums. Pelargoniums were counted in the Orco Valley (5455 plants) and eggs and larvae were counted on 348 pelargoniums chosen on the basis of isolation and altitude. Flight experiments suggested that females were able to overcome barriers and fly at least 550 m looking for host plants. Eggs and larvae were unexpectedly abundant, but models showed that there was a temperature limit which prevented upward expansion of C. marshalli. Citizens were given a questionnaire to complete to investigate their propensity to replace pelargonium with other ornamental plants. We discuss the possibility of eradicating C. marshalli in the protected area in the light of our results.

Keywords

Geranium Bronze Invasive species Species naturalisation Pelargonium 

Notes

Acknowledgements

The project is a collaboration between Gran Paradiso National Park and the Department of Life Sciences and Systems Biology of Turin University, and was funded by the Gran Paradiso National Park (Italian Ministry for the Environment, Land and Sea Protection) within the project “A multi-taxa approach to study the impact of climate change on the biodiversity of Italian ecosystems”. We are grateful to Andrea Barbi, Daniele Aimar and Davide Morando for collaborating in the sampling of preimaginal stages, and to Emanuel Rocchia and Massimo Meregalli for their precious help in dispersal experiments.

Author contributions

All authors are in agreement with this submission.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human and animal participants

No animal was harmed by “test flights” experiments. People freely drafted questionnaires in an anonymous way.

Supplementary material

10841_2018_124_MOESM1_ESM.docx (632 kb)
Supplementary material 1 (DOCX 631 KB)

References

  1. Anastassiu HT, Ghavalas N, Coutsis JG (2010) First record of Cacyreus marshalli in Greece, and comments on the potential occurrence of Zizeeria karsandra on the Greek island of Crete (Lepidoptera: Lycaenidae). Phegea 38(3):85–92Google Scholar
  2. Andersson S (2003) Foraging responses in the butterflies Inachis io, Aglais urticae (Nymphalidae), and Gonepteryx rhamni (Pieridae) to floral scents. Chemoecology 13(1):1–11CrossRefGoogle Scholar
  3. Barton K (2016) MuMIn: multi-model inference. R package version 1.15.6. https://cran.r-project.org/package=MuMIn
  4. Becker RA, Chambers JM, Wilks AR (1988) The new S language. Wadsworth & Brooks/ColeGoogle Scholar
  5. Beniston M (2006) Mountain weather and climate: a general overview and a focus on climatic change in the Alps. Hydrobiologia 562(1):3–16CrossRefGoogle Scholar
  6. Bonney R, Cooper CB, Dickinson J, Kelling S, Phillips T, Rosenberg KV, Shirk J (2009) Citizen science: a developing tool for expanding science knowledge and scientific literacy. Bioscience 59(11):977–984CrossRefGoogle Scholar
  7. Clark GC, Dickson CGC (1971) Life histories of the South African lycaenid butterflies. Purnell, Cape TownGoogle Scholar
  8. Crall AW, Jordan R, Holfelder K, Newman GJ, Graham J, Waller DM (2013) The impacts of an invasive species citizen science training program on participant attitudes, behavior, and science literacy. Public Underst Sci 22(6):745–764CrossRefGoogle Scholar
  9. Crall AW, Jarnevich CS, Young NE, Panke BJ, Renz M, Stohlgren TJ (2015) Citizen science contributes to our knowledge of invasive plant species distributions. Biol Invasions 17(8):2415–2427CrossRefGoogle Scholar
  10. Dennis RL, Dapporto L, Dover JW, Shreeve TG (2013) Corridors and barriers in biodiversity conservation: a novel resource-based habitat perspective for butterflies. Biodivers Conserv 22(12):2709–2734CrossRefGoogle Scholar
  11. Dormann CF, Schymanski SJ, Cabral J, Chuine I, Graham C, Hartig F, Kearney M, Morin X, Römermann C, Schröder B, Singer A (2012) Correlation and process in species distribution models: bridging a dichotomy. J Biogeogr 39(12):2119–2131CrossRefGoogle Scholar
  12. Fang JY, Yoda K (1988) Climate and vegetation in China: changes in the altitudinal lapse rate of temperature and distribution of sea level temperature. Ecol Rses 3:37–51CrossRefGoogle Scholar
  13. Favilli L, Manganelli G (2006) Life history of Cacyreus marshalli, a South African species recently introduced into Italy. Boll Soc Entomol Ital 138(1):51–61Google Scholar
  14. García-Barros E, Fartmann T (2009) Butterfly oviposition: sites, behaviour and modes. In: Ecology of butterflies in Europe. Cambridge University Press, Cambridge, pp 29–42Google Scholar
  15. Haddad NM (1999) Corridor and distance effects on interpatch movements: a landscape experiment with butterflies. Ecol Appl 9:612–622CrossRefGoogle Scholar
  16. Junker M, Wagner S, Gros P, Schmitt T (2010) Changing demography and dispersal behaviour: ecological adaptations in an alpine butterfly. Oecologia 164(4):971–980CrossRefGoogle Scholar
  17. Kiritani K, Yamamura K (2003) Exotic insects and their pathways for invasion. In: Invasive species: vectors and management strategies. Island Press, Washington, pp 4–67Google Scholar
  18. Kosmač M, Verovnik R (2009) First record of Cacyreus marshalli (Lycaenidae) from the Balkan Peninsula. Nota lepid 32(1):81–82Google Scholar
  19. Maistrello L, Dioli P, Bariselli M, Mazzoli GL, Giacalone-Forini I (2016) Citizen science and early detection of invasive species: phenology of first occurrences of Halyomorpha halys in Southern Europe. Biol Invasions 18(11):3109–3116CrossRefGoogle Scholar
  20. Miller DM (2003) The taxonomy of Pelargonium species and cultivars, their origins and growth in the wild. In: Geranium and Pelargonium. CRC Press, Boca Raton, pp 61–91Google Scholar
  21. Öckinger E, Schweiger O, Crist TO, Debinski DM, Krauss J, Kuussaari M, Petersen JD, Pöyry J, Settele J, Summerville KS, Bommarco R (2010) Life-history traits predict species responses to habitat area and isolation: a cross-continental synthesis. Ecol Lett 13(8):969–979Google Scholar
  22. Ômura H, Honda K (2005) Priority of color over scent during flower visitation by adult Vanessa indica butterflies. Oecologia 142(4):588–596CrossRefGoogle Scholar
  23. Otto HHH, Gardiner AJ, Sharp IC (2013) New larval host plant records for butterflies of the Kruger National Park and its surrounds, Limpopo & Mpumalanga, South Africa. Metamorphosis 24:69–74Google Scholar
  24. Polak S (2009) Geranium Bronze (Cacyreus marshalli (Butler, 1898)): a new butterfly species for the Slovenian fauna. In: 2nd Slovenian entomological symposium, book of abstracts. Slovenian Entomological Society, Ljubljana, p 104Google Scholar
  25. Quacchia A, Ferracini C, Bonelli S, Balletto E, Alma A (2008) Can the Geranium Bronze, Cacyreus marshalli, become a threat for European biodiversity? Biodivers Conser 17(6):1429–1437CrossRefGoogle Scholar
  26. Quantum GIS Development Team - Version 2.14.2 (2016) Quantum GIS geographic information system. Open source geospatial foundation project. http://qgis.osgeo.org
  27. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  28. Rolland C (2003) Spatial and seasonal variations of air temperature lapse rates in Alpine regions. J Climate 16(7):1032–1046CrossRefGoogle Scholar
  29. Sammut P (2007) Cacyreus marshalli Butler (1898) reaches the Maltese Islands (Lepidoptera: Lycaenidae). SHILAP-Rev Lepidopt 35(139):317–319Google Scholar
  30. Sarto i Monteys V (1992) Spread of Southern African Lycaenid butterfly, Cacyreus marshalli Butler, 1898, (Lep: Lycaenidae) in the Balearic Archipelago (Spain) and considerations on its likely introduction to continental Europe. J Res Lepid 31:24–34Google Scholar
  31. Schäpers A, Carlsson MA, Gamberale-Stille G, Janz N (2015) The role of olfactory cues for the search behavior of a specialist and generalist butterfly. J Insect Behav 28(1):77–87CrossRefGoogle Scholar
  32. Sekar S (2012) A meta-analysis of the traits affecting dispersal ability in butterflies: can wingspan be used as a proxy? J Anim Ecol 81(1):174–184CrossRefGoogle Scholar
  33. Singer MC, Thomas CD, Parmesan C (1993) Rapid human-induced evolution of insect-host associations. Nature 366:681–683CrossRefGoogle Scholar
  34. Singer MC, Wee B, Hawkins S, Butcher M (2007) Rapid natural and anthropogenic diet evolution: three examples from checkerspot butterfl ies. In: Tilmon KJ (ed) Evolutionary aspects of pests, invasive species, and the environment. University of California Press, Berkeley, pp 311–329Google Scholar
  35. Tarrier M (1998) Cacyreus marshalli Butler, 1898, espece nouvele pour la France, le Portugal et le Maroc (Lepidoptera, Lycaenidae) Alexanor 20(3):143–144Google Scholar
  36. Tisserand R (1985) The art of aromatherapy. Daniel CW (ed) Co. Ltd, Saffron Walden p 231Google Scholar
  37. Trematerra P, Zilli A, Valentini V, Mazzei P (1997) Cacyreus marshalli, un lepidottero sudafricano dannoso ai gerani in Italia. Inftore Fitopatol 7–8:2–6Google Scholar
  38. Troukens W (1991) Cacyreus marshalli Butler, 1898, aangetroffen in Belge (Lepidoptera: Lycaenidae). Phegea 19(4):129–131Google Scholar
  39. Weiss MR (2001) Vision and learning in some neglected pollinators: beetles, flies, moths, and butterflies. In: Cognitive ecology of pollination. Cambridge University Press, Cambridge, pp 171–190CrossRefGoogle Scholar
  40. White PC, Jennings NV, Renwick AR, Barker NH (2005) Questionnaires in ecology: a review of past use and recommendations for best practice. J Appl Ecol 42(3):421–430CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Paradiso Federica
    • 1
  • Martelli Francesca
    • 1
  • Cerrato Cristiana
    • 2
  • Ghidotti Silvia
    • 2
    Email author return OK on get
  • Viterbi Ramona
    • 2
  • Canterino Sara
    • 3
  • Ferracini Chiara
    • 4
  • Bonelli Simona
    • 1
  1. 1.DBIOS, Department of Life Sciences and Systems BiologyUniversity of TurinTurinItaly
  2. 2.Gran Paradiso National ParkTurinItaly
  3. 3.Nino Costa Secondary School - Chiavazza - IC Biella IIBiellaItaly
  4. 4.DISAFA, Department of Agricultural, Forest and Food SciencesUniversity of TurinTurinItaly

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