Conservation Genetics

, Volume 9, Issue 6, pp 1431–1437 | Cite as

DNA-based confirmation that the parasitic wasp Cotesia glomerata (Braconidae, Hymenoptera) is a new threat to endemic butterflies of the Canary Islands

  • Aurel I. LozanEmail author
  • Michael T. Monaghan
  • Karel Spitzer
  • Josef Jaroš
  • Martina Žurovcová
  • Václav Brož
Research Article


Island-endemic species can be particularly vulnerable to alien invasion. There are many examples of introduced insect parasitoids having a serious impact on endemic butterflies and moths. In 2006, a population of parasitic wasps was reared from larvae of the Canary Island Large White butterfly (Pieris cheiranthi), an endemic inhabitant of laurel forests unique to the Canary Islands of Macaronesia. Parasitoids were tentatively identified as Cotesia glomerata (Braconidae, Hymenoptera), a widely introduced agricultural bioagent. To corroborate this finding we sequenced 632 bp of mitochondrial cox1 from parasitoids and hosts from La Palma and from the native range of C. glomerata in continental Europe. These were combined with GenBank sequences and a character-based, phylogenetic approach was used to assess the species status of parasites and hosts. The La Palma parasitoid could unambiguously be assigned to C. glomerata under the criterion of diagnosibility with corroboration from multiple lines of evidence (DNA, morphology). We suggest that this opportunistic, non-native parasitoid wasp will be a threat to P. cheiranthi and other endemic Canarian butterflies. Parasitoid populations were recorded from P. cheiranthi in marginal forest habitats but not in central forest areas, suggesting that comprehensive habitat conservation of the Canarian laurel forests could prevent penetration of the alien parasitoid wasps and subsequent mortality of endemic butterfly populations.


Alien parasitoids Threatened butterflies Laurel forests Island endemics Mitochondrial DNA 



Laboratory studies were supported by an EU SYNTHESYS grant (GB-TAF-2063) and by the Czech Academy of Sciences (1QS500070505 and Z50070508). MTM was supported by the UK Biotechnology and Biological Sciences Research Council (BBS/B/04358). The Environmental Authority of La Palma provided permission for field studies of Lepidoptera.


  1. Aguiar AMF, Karsholt O (2006) Systematic catalogue of the entomofauna of the Madeira Archipelago and Selvagens Islands. Lepidoptera 1. Bol Mus Municip Funchal Suppl 9:5–139Google Scholar
  2. Ahrens D, Monaghan MT, Vogler AP (2007) A DNA-based taxonomy for establishing species limits and larval–adult association in chafers (Coleoptera: Scarabaeidae). Mol Phylog Evol 44:436–439CrossRefGoogle Scholar
  3. Altschul S, Madden T, Schaffer A et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nuc Ac Res 25:3389–3402CrossRefGoogle Scholar
  4. Asquith A (1995) Alien species and the extinction crisis of Hawaii’s invertebrates. Endangered Species Update 12(6)Google Scholar
  5. Balevski NA (1999) Catalogue of the Braconid parasitoids (Hymenoptera: Braconidae) isolated from various phytophagous insect hosts in Bulgaria. Pensoft Publishers, SofiaGoogle Scholar
  6. Benson J, Pasquale A, Van Driesche R et al (2003) Assessment of risk posed by introduced braconid wasps to Pieris virginiensis, a native woodland butterfly in New England. Biol Control 26(1):83–93CrossRefGoogle Scholar
  7. Borges PAV, Cunha R, Gabriel R et al (eds) (2005) A list of the terrestrial fauna and flora from the Azores. Universidade dos Acores, Angra do HeroismoGoogle Scholar
  8. Bramwell D, Bramwell Z (2001) Wild flowers of the Canary Islands. Editorial Rueda, MadridGoogle Scholar
  9. Brunton CFA, Hurst GDD (1998) Mitochondrial DNA phylogeny of Brimstone butterflies (genus Gonepteryx) from the Canary Islands and Madeira. Biol J Linn Soc 63:69–79Google Scholar
  10. 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 88:413–435CrossRefGoogle Scholar
  11. Costea G, Mustata G, Lozan A (2002) Role of Braconidae (Hymenoptera) in limitation of Lepidoptera cabbage pests populations in Romania. In: Melika G, Thuroczy C (eds) Parasitic wasps: evolution, systematics, biodiversity and biological control, 2001, pp 391–395Google Scholar
  12. Davis J, Nixon K (1992) Populations, genetic variation, and the delimitation of phylogenetic species. Syst Biol 41:421–435CrossRefGoogle Scholar
  13. DeBach P (1974) Biological control by natural enemies. Cambridge University PressGoogle Scholar
  14. DeBach P, Schlinger EI (eds) (1964) Biological control of insect pests and weeds. Chapman and Hall, LondonGoogle Scholar
  15. DeSalle R, Egan M, Siddall M (2005) The unholy trinity; taxonomy, species delimitation and DNA barcoding. Philos Trans R Soc, Biol Sci 360:1905–1916CrossRefGoogle Scholar
  16. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonGoogle Scholar
  17. Folmer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299PubMedGoogle Scholar
  18. Gardiner B (2003) The possible cause of extinction of Pieris brassicae wollastoni Buttler (Lepidoptera: Pieridae). Entomol Gaz 54:267–268Google Scholar
  19. Gillespie RG, Roderick GK (2002) Arthropods on islands: colonization, speciation and conservation. Annu Rev Entomol 47:595–632PubMedCrossRefGoogle Scholar
  20. Henneman ML, Memmott J (2001) Infiltration of a Hawaiian community by introduced biological control agents. Science 293(5533):1314–1316PubMedCrossRefGoogle Scholar
  21. Hoddle M (2004) The strength of biological control in the battle against invasive pests: a reply. Cons Biol 18:61–64CrossRefGoogle Scholar
  22. Jiang ShuangLin (2001) Biology of Aporia crataegi and its control. Entomol Know 38(3):198–199Google Scholar
  23. Jones MJ, Lace LA, Hounsome MV, Hamer K (1987) The butterflies and birds of Madeira and La Gomera: taxon cycles and human influence. Biol J Linn Soc 31:95–111CrossRefGoogle Scholar
  24. Juan C, Emerson BC, Oromí P, Hewitt GM (2000) Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands. Trends Ecol Evol 15(3):104–109PubMedCrossRefGoogle Scholar
  25. Kankare M, Van Nouhuys S, Hanski I (2005a) Genetic divergence among host-specific cryptic species in Cotesia melitaearum aggregate (Hymenoptera : Braconidae), parasitoids of checkerspot butterflies. An Ent SocAm 98:382–394CrossRefGoogle Scholar
  26. Kankare M, Stefanescu C, Van Nouhuys S, Shaw MR (2005b) Host specialization by Cotesia wasps (Hymenoptera: Braconidae) parasitizing species-rich Melitaeini (Lepidoptera: Nymphalidae) communities in north-eastern Spain. Biol J Lin Soc 86:45–65CrossRefGoogle Scholar
  27. Kankare M, Shaw M (2004) Molecular phylogeny of Cotesia Cameron, 1891 (Insecta: Hymenoptera: Braconidae: Microgastrinae) parasitoids associated with Melitaeini butterflies (Insecta: Lepidoptera: Nymphalidae: Melitaeini). Mol Phylogen Evol 32:207–220CrossRefGoogle Scholar
  28. Kunkel G (ed) (1976) Biogeography and ecology in the Canary Islands. Dr. W. Junk Publishers, The HagueGoogle Scholar
  29. Lozan A (2007) A new braconid parasitoid of the tortricid moth Cydia alazon (Diakonoff, 1976) from the Canary Islands, Spain (Hymenoptera, Braconidae: Microgastrinae). Entomol Mon Mag 143 (in press)Google Scholar
  30. Muirhead K, Murphy N, Sallam M et a1 (2006) Mitochondrial DNA phylogeography of the Cotesia flavipes complex of parasitic wasps (Hymenoptera : Braconidae). Ann Soc Entomol Fr 42:309–318Google Scholar
  31. Nafus DM (1993) Extinction, biological control, and insect conservation on islands. In: Gaston KJ, New TR, Samways MJ (eds) Perspectives on insect conservation. Intercept Ltd, Andover, pp 139–154Google Scholar
  32. Ohsaki N, Sato Y (1994) Food plant choice of Pieris butterflies as a trade-off between parasitoid avoidance and quality of plants. Ecology 75(1):59–68CrossRefGoogle Scholar
  33. Peck SB, Heraty J, Landry B, Sinclair BJ (1998) Introduced insect fauna of an oceanic archipelago: the Galápogos Islands, Ecuador. Am Entomol 1998:218–237Google Scholar
  34. Pons J, Barraclough T, Gomez-Zurita J et al (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609PubMedCrossRefGoogle Scholar
  35. Rozas J, Sánchez-DelBarrio J, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  36. Sands D, Van Driesche RG (2003) Host range testing techniques for parasitoids and predators. In: Van Driesche R (ed) Proceedings of the first international symposium on biological control of arthropods, Honolulu, Hawaii 2002, USDA Forest Service Publication, Morgantown, West Virginia, USA, pp 41–53Google Scholar
  37. Sands DPA, Van Driesche RG (2004) Using the scientific literature to estimate the host range of a biological control agent. In: Van Driesche R, Reardon R (eds) Assessing host ranges for parasitoids and predators used for classical biological control: A guide to best practice, 15–23Google Scholar
  38. Scaglia M, Brochetto-Braga MR, Chaud-Netto J, Gobbi N (2003) Haemolymph electrophoretic pattern of Ascia monuste orseis larvae (Lepidoptera: Pieridae) parasitized by Cotesia glomerata (Hymenoptera: Braconidae). J Venom Anim Toxins incl Trop Dis 9(1):89–103CrossRefGoogle Scholar
  39. Sharkey M, Finnell K, Leathers J, Frana J (2000) Microgastrinae (Hymenoptera: Braconidae) parasitoids of Colias lesbia (Fabricius) (Lepidoptera: Pieridae). J Hym Res 9:108–110Google Scholar
  40. Spitzer K, Jaroš J (2006) First record of Cydia alazon (Diakonoff, 1976) from La Palma Island (Canary Islands, Spain) with taxonomic and ecological notes (Lepidoptera: Tortricidae). SHILAP Rev Lepidopt 34(136):371–378Google Scholar
  41. Stokstad E (2001) Parasitic wasps invade Hawaiian ecosystem. Science 293(5533):1241PubMedCrossRefGoogle Scholar
  42. Swofford D (2003) PAUP*; Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  43. Tscharntke T, Steffan-Dewenter I, Kruess A et al (2002) Contribution of small habitat fragments to conservation of insect communities of grassland–cropland landscapes. Ecol Appl 12:354–363Google Scholar
  44. Tennent WJ (2005) A check-list of the butterflies of Macaronesia (Canary Islands, Madeira, Azores). Entomol Gaz 56:133–138Google Scholar
  45. Tobias VI, Belokobylskij SA, Kotenko AG (1986) Family Braconidae. In: Medvedev G (ed) Key of insects of European part of USSR, Nauka, Leningrad 3(4)Google Scholar
  46. Tolman T (1997) Collins field guide butterflies of Britain and Europe. HarperCollins Publishers Ltd., LondonGoogle Scholar
  47. Traugott M, Zangerl P, Juen A et al (2006) Detecting key parasitoids of lepidopteran pests by multiplex PCR. Biol Control 39:39–46CrossRefGoogle Scholar
  48. Vogler AP, Monaghan MT (2007) Recent advances in DNA taxonomy. J Zool Syst Evol Res 45:1–10CrossRefGoogle Scholar
  49. Wiemers M (1995) The butterflies of the Canary Islands. A survey on their distribution, biology and ecology (Lepidoptera: Papilionoidea and Hesperioidea). Linn Belg 15:63–118Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Aurel I. Lozan
    • 1
    Email author
  • Michael T. Monaghan
    • 2
    • 3
  • Karel Spitzer
    • 1
  • Josef Jaroš
    • 1
  • Martina Žurovcová
    • 1
  • Václav Brož
    • 4
  1. 1.Biological Centre, Institute of EntomologyCzech Academy of SciencesČeské BudějoviceCzech Republic
  2. 2.Entomology DepartmentNatural History MuseumLondonUK
  3. 3.Division of BiologyImperial College LondonAscotUK
  4. 4.Faculty of Biological SciencesUniversity of South BohemiaČeské BudějoviceCzech Republic

Personalised recommendations