Chinese Science Bulletin

, Volume 59, Issue 5–6, pp 528–532 | Cite as

Hesperomyces virescens (Fungi, Ascomycota, Laboulbeniales) attacking Harmonia axyridis (Coleoptera, Coccinellidae) in its native range

  • Haelewaters Danny
  • Richard F. Comont
  • Serena Y. Zhao
  • Donald H. Pfister
Article Entomology


This study intended to find data on obligate ectoparasitic Laboulbeniales (Fungi, Ascomycota) on Chinese Harmonia axyridis (Coleoptera, Coccinellidae). After having screened over four thousand dried specimens of H. axyridis and close relatives, we present the first (historical) record of Chinese H. axyridis infected with Hesperomyces virescens. We suggest that H. virescens is a historically globally distributed species and hypothesize that (native) infection was lost when H. axyridis was introduced in North America.


Coccinellidae Distribution Ectoparasitic fungi Harmonia axyridis Hesperomyces virescens Historical data Invasive species Native range 


  1. 1.
    Blackburn TM, Cassey P, Duncan RP et al (2004) Avian extinction and mammalian introductions on oceanic islands. Science 305:1955–1958CrossRefGoogle Scholar
  2. 2.
    Gaertner M, Den Bree A, Hui C et al (2009) Impacts of alien plant invasions on species richness in Mediterranean-type ecosystems: a meta-analysis. Prog Phys Geog 33:319–338CrossRefGoogle Scholar
  3. 3.
    Koch RL, Venette RC, Hutchinson WD (2006) Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the Western hemisphere: implications for South America. Neotrop Entomol 35:421–434CrossRefGoogle Scholar
  4. 4.
    Gordon RD (1985) The Coccinellidae (Coleoptera) of America North of Mexico. J New York Entomol Soc 93:1–912Google Scholar
  5. 5.
    Chapin JB, Brou VA (1991) Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera, Coccinellidae). Proc Entomol Soc Washington 93:630–635Google Scholar
  6. 6.
    Brown PMJ, Thomas CE, Lombaerts E et al (2011) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. Biocontrol 56:623–641CrossRefGoogle Scholar
  7. 7.
    Colautti RI, Ricciardi A, Grigorovich IA et al (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  8. 8.
    Roy HE, Lawson Handley LJ, Schonrogge K et al (2011) Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? BioControl 56:451–468CrossRefGoogle Scholar
  9. 9.
    Ceryngier P, Hodek I (1996) Enemies of Coccinellidae. In: Hodek I, Honěk A (eds) Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, pp 319–350CrossRefGoogle Scholar
  10. 10.
    Roy HE, Rhule E, Harding S et al (2011) Living with the enemy: parasites and pathogens of the ladybird Harmonia axyridis. Biocontrol 56:663–679CrossRefGoogle Scholar
  11. 11.
    Ceryngier P, Twardowska K (2013) Harmonia axyridis (Coleoptera: Coccinellidae) as a host of the parasitic fungus Hesperomyces virescens (Ascomycota: Laboulbeniales, Laboulbeniaceae): a case report and short review. Eur J Entomol 110:549–557CrossRefGoogle Scholar
  12. 12.
    Magro A, Lecompte E, Magne F et al (2010) Phylogeny of ladybirds (Coleoptera: Coccinellidae): are the subfamilies monophyletic? Mol Phylogenet Evol 54:833–848CrossRefGoogle Scholar
  13. 13.
    Benjamin RK (1971) Introduction and supplement to Thaxter’s contribution toward a monograph of the Laboulbeniaceae. Bibl Mycol 80:1–155Google Scholar
  14. 14.
    Santamaría S, Balazuc J, Tavares II (1991) Distribution of the European Laboulbeniales (Fungi, Ascomycotina). An annotated list of species. Treb Inst Bot Barcelona 14:1–123Google Scholar
  15. 15.
    Riddick EW, Cottrell TE, Kidd KA (2009) Natural enemies of the Coccinellidae: parasites, pathogens, and parasitoids. Biol Control 51:306–312CrossRefGoogle Scholar
  16. 16.
    Raak-van den Berg CL, van Wielink PS, de Jong PW et al Invasive alien species under attack: natural enemies of Harmonia axyridis in the Netherlands. BioControl, acceptedGoogle Scholar
  17. 17.
    Garcés S, Williams R (2004) First record of Hesperomyces virescens Thaxter (Laboulbeniales: Ascomycetes) on Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). J Kansas Entomol Soc 77:156–158CrossRefGoogle Scholar
  18. 18.
    Riddick EW, Schaefer PW (2005) Occurrence, density, and distribution of parasitic fungus Hesperomyces virescens (Laboulbeniales: Laboulbeniaceae) on multicolored Asian lady beetle (Coleoptera: Coccinellidae). Ann Entomol Soc Am 98:615–624CrossRefGoogle Scholar
  19. 19.
    Riddick EW (2006) Influence of host gender on infection rate, density and distribution of the parasitic fungus, Hesperomyces virescens, on the multicolored Asian lady beetle, Harmonia axyridis. J Insect Sci 6:1–15CrossRefGoogle Scholar
  20. 20.
    Nalepa CA, Weir A (2007) Infection of Harmonia axyridis (Coleoptera: Coccinellidae) by Hesperomyces virescens (Ascomycetes: Laboulbeniales): role of mating status and aggregation behavior. J Invertebr Pathol 94:196–203CrossRefGoogle Scholar
  21. 21.
    Harwood JD, Ricci C, Romani R et al (2006) Prevalence and association of the Laboulbenialean fungus Hesperomyces virescens (Laboulbeniales: Laboulbeniaceae) on coccinellid hosts (Coleoptera: Coccinellidae) in Kentucky. USA Eur J Entom 103:799–804CrossRefGoogle Scholar
  22. 22.
    Harwood JD, Ricci C, Romani R et al (2006) Historic prevalence of a laboulbenialean fungus infected introduced coccinellids in the United States. Antenna 30:74–79Google Scholar
  23. 23.
    De Kesel A (2011) Hesperomyces (Laboulbeniales) and coccinellid hosts. Sterbeeckia 30:32–37Google Scholar
  24. 24.
    Riddick EW, Cottrell TE (2010) Is the prevalence and intensity of the ectoparasitic fungus Hesperomyces virescens related to the abundance of entomophagous coccinellids? Bull Insectol 63:71–78Google Scholar
  25. 25.
    Riddick EW (2010) Ectoparasitic mite and fungus on an invasive lady beetle: parasite coexistence and influence on host survival. Bull Insectol 63:13–20Google Scholar
  26. 26.
    Haelewaters D, De Kesel A. Laboulbeniales van De Kaaistoep D (2011) Natuurstudie in De Kaaistoep. In: Cramer T, van Wielink P (ed) 16e onderzoeksjaar. NV Tilburgsche Waterleiding-Maatschappij, KNNV-afdeling Tilburg & Natuurmuseum Brabant, Verslag 2010, Amsterdam, pp 107–112Google Scholar
  27. 27.
    Herz A, Kleespiel RG (2012) Occurrence of natural enemies in different populations of the invasive ladybird Harmonia axyridis (Pallas, 1771) Coleoptera, Coccinellidae) in Germany. Mitt Dtsch Ges Allg Angew Entomol 18:201–206Google Scholar
  28. 28.
    Steenberg T, Harding S (2010) Entomopathogenic fungi found in field populations of the harlequin ladybird, Harmonia axyridis. IOBC/wprs Bull 58:137–141Google Scholar
  29. 29.
    Haelewaters D, van Wielink P, van Zuijlen JW et al (2012) New records of Laboulbeniales (Fungi, Ascomycota) for the Netherlands. Entomol Ber 72:175–183Google Scholar
  30. 30.
    Cottrell TE, Riddick EW (2012) Limited transmission of the ectoparasitic fungus Hesperomyces virescens between lady beetles. Psyche 72:1–100CrossRefGoogle Scholar
  31. 31.
    Haelewaters D, Nuytinck J, De Kesel A (2012) Laboulbeniales (Fungi, Ascomycota) in the Netherlands: an introduction. Natuurh Maandblad 101:88–93Google Scholar
  32. 32.
    Ceryngier P, Roy HE, Poland RL (2012) Natural enemies of ladybird beetles. In: Hodek I, van Emden HF (eds) Ecology and behavior of the ladybird beetles (Coccinellidae). Blackwell Publishing Ltd, Hoboken, pp 375–443CrossRefGoogle Scholar
  33. 33.
    Thaxter R (1891) Supplementary note on North American Laboulbeniaceae. Proc Amer Acad Arts Sci 25:261–270CrossRefGoogle Scholar
  34. 34.
    Finlayson CJ, Alyokhin AV, Porter EW (2009) Interactions of native and non-native lady beetle species (Coleoptera: Coccinellidae) with aphid-tending ants in laboratory arenas. Environ Entomol 38:846–855CrossRefGoogle Scholar
  35. 35.
    Spegazzini C (1917) Revisión de las Laboulbeniales Argentinas. An Mus Nac Hist Nat Buenos Aires 29:445–688Google Scholar
  36. 36.
    Thaxter R (1931) Contribution towards a monograph of the Laboulbeniaceae. Mem Amer Acad Arts Sci 16:1–435Google Scholar
  37. 37.
    Lombaert E, Guillemaud T, Cormuet JM et al (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE 5:e9743CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Haelewaters Danny
    • 1
  • Richard F. Comont
    • 2
  • Serena Y. Zhao
    • 1
    • 3
  • Donald H. Pfister
    • 1
  1. 1.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA
  2. 2.NERC Centre for Ecology & HydrologyCrowmarsh GiffordUK
  3. 3.Kraus Natural Science BuildingUniversity of MichiganAnn ArborUSA

Personalised recommendations