Harmonia axyridis is an invasive alien ladybird in North America and Europe. Studies show that multiple natural enemies are using Ha. axyridis as a new host. However, thus far, no research has been undertaken to study the effects of simultaneous infection by multiple natural enemies on Ha. axyridis. We hypothesized that high thallus densities of the ectoparasitic fungus Hesperomyces virescens on a ladybird weaken the host's defenses, thereby making it more susceptible to infection by other natural enemies. We examined mortality of the North American-native Olla v-nigrum and Ha. axyridis co-infected with He. virescens and an entomopathogenic fungus-either Beauveria bassiana or Metarhizium brunneum. Laboratory assays revealed that He. virescens-infected O. v-nigrum individuals are more susceptible to entomopathogenic fungi, but Ha. axyridis does not suffer the same effects. This is in line with the enemy release hypothesis, which predicts that invasive alien species in new geographic areas experience reduced regulatory effects from natural enemies compared to native species. Considering our results, we can ask how He. virescens affects survival when confronted by other pathogens that previously had little impact on Ha. axyridis.

Agricultural Research Service Southeastern Fruit and Tree Nut Research Laboratory United States Department of Agriculture Byron GA United States of America

Department of Botany and Plant Pathology Purdue University West Lafayette IN United States of America

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Farlow Reference Library and Herbarium of Cryptogamic Botany Harvard University Cambridge MA United States of America

Institute of Evolutionary Ecology and Conservation Genomics University of Ulm Ulm Germany

Natuurmuseum Brabant Tilburg The Netherlands

Zobrazit více v PubMed

Applebaum SW, Kfir R, Gerson U, Tadmor U. Studies on the summer decline of Chilocorus bipustulatus in citrus groves of Israel. Entomophaga. 1971;16:433–444. doi: 10.1007/BF02370924. DOI

Bates D, Maechler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. Journal of Statistical Software. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

Blackwell M, Haelewaters D, Pfister DH. Laboulbeniomycetes: evolution, natural history, and Thaxter’s final word. Mycologia. 2020 doi: 10.1080/00275514.2020.1718442. In Press. PubMed DOI

Brown PMJ, Roy HE. Native ladybird decline caused by the invasive harlequin ladybird Harmonia axyridis: evidence from a long-term field study. Insect Conservation and Diversity. 2018;11:230–239. doi: 10.1111/icad.12266. DOI

Brown PMJ, Roy DB, Harrower C, Dean HJ, Rorke SL, Roy HE. Spread of a model invasive alien species, the harlequin ladybird Harmonia axyridis in Britain and Ireland. Scientific Data. 2018;5 doi: 10.1038/sdata.2018.239. Article 180239. PubMed DOI PMC

Camacho-Cervantes M, Ortega-Iturriaga A, Del-Val E. From effective biocontrol agent to successful invader: the harlequin ladybird (Harmonia axyridis) as an example of good ideas that could go wrong. PeerJ. 2017;5:e3296. doi: 10.7717/peerj.3296. PubMed DOI PMC

Ceryngier P, Nedvěd O, Grez AA, Riddick EW, Roy HE, San Martin G, Steenberg T, Veselý P, Zaviezo T, Zúñiga-Reinoso Á, Haelewaters D. Predators and parasitoids of the harlequin ladybird, Harmonia axyridis, in its native range and invaded areas. Biological Invasions. 2018;20:1009–1031. doi: 10.1007/s10530-017-1608-9. DOI

Christian E. The coccinellid parasite Hesperomyces virescens and further species of the order Laboulbeniales (Ascomycotina) new to Austria. Annalen des Naturhistorischen Museums in Wien. 2001;103 B:599–603.

Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ. Is invasion success explained by the enemy release hypothesis? Ecology Letters. 2004;7:721–733. doi: 10.1111/j.1461-0248.2004.00616.x. DOI

Cottrell TE, Riddick EW. Limited transmission of the ectoparasitic fungus Hesperomyces virescens between lady beetles. Psyche. 2012;2012 doi: 10.1155/2012/814378. Article 814378. DOI

Cottrell TE, Shapiro-Ilan DI. Susceptibility of a native and an exotic lady beetle (Coleoptera: Coccinellidae) to Beauveria bassiana. Journal of Invertebrate Pathology. 2003;84:137–144. doi: 10.1016/j.jip.2003.09.003. PubMed DOI

Cottrell TE, Shapiro-Ilan DI. Susceptibility of endemic and exotic North American ladybirds (Coleoptera: Coccinellidae) to endemic fungal entomopathogens. European Journal of Entomology. 2008;105:455–460. doi: 10.14411/eje.2008.058. DOI

Furlong MJ, Pell JK. Interactions between entomopathogenic fungi and other arthropods natural enemies. In: Vega FE, Blackwell M, editors. Insect-fungal associations, ecology and evolution. Oxford: Oxford University Press; 2005. pp. 51–73.

Garcés S, Williams R. First record of Hesperomyces virescens Thaxter (Laboulbeniales: Ascomycetes) on Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) Journal of the Kansas Entomological Society. 2004;77:156–158. doi: 10.2317/0304.18.1. DOI

Haelewaters D, Blackwell M, Pfister DH. Laboulbeniomycetes: intimate fungal associates of arthropods. Annual Review of Entomology. 2021;66(1):13.1–13.20. doi: 10.1146/annurev-ento-013020-013553. PubMed DOI

Haelewaters D, De Kesel A. De schimmel Hesperomyces virescens, een natuurlijke vijand van lieveheersbeestjes. Entomologische Berichten. 2017;77:106–118.

Haelewaters D, De Kesel A, Pfister DH. Integrative taxonomy reveals hidden species within a common fungal parasite of ladybirds. Scientific Reports. 2018;8:15966. doi: 10.1038/s41598-018-34319-5. PubMed DOI PMC

Haelewaters D, Zhao SY, Clusella-Trullas S, Cottrell TE, De Kesel A, Fiedler L, Herz A, Hesketh H, Hui C, Kleespies RG, Losey JE, Minnaar IA, Murray KM, Nedvěd O, Pfliegler WP, Raak-van den Berg CL, Riddick EW, Shapiro-Ilan DI, Smyth RR, Steenberg T, van Wielink PS, Viglášova S, Zhao Z, Ceryngier P, Roy HE. Parasites of Harmonia axyridis: current research and perspectives. BioControl. 2017;62:355–371. doi: 10.1007/s10526-016-9766-8. DOI

Harding S, Poinar GO, Dimitrova DV, Steenberg T. Parasitylenchus sp. (Tylenchomorpha: Allantonematidae) parasitizing field populations of Harmonia axyridis (Coleoptera: Coccinellidae) European Journal of Entomology. 2011;108:487–488. doi: 10.14411/eje.2011.062. DOI

Herz A, Kleespies RG. Occurrence of natural enemies in different populations of the invasive ladybird Harmonia axyridis (Pallas, 1771) (Coleoptera, Coccinellidae) in Germany. Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie. 2012;18:201–206.

Hiller T, Haelewaters D. A case of silent invasion: citizen science confirms the presence of Harmonia axyridis (Coleoptera, Coccinellidae) in Central America. PLOS ONE. 2019;14:e0220082. doi: 10.1371/journal.pone.0220082. PubMed DOI PMC

Hokkanen HMT, Pimentel D. New associations in biological control: theory and practice. The Canadian Entomologist. 1989;121:829–840. doi: 10.4039/Ent121829-10. DOI

Honěk A, Martinkova Z, Dixon AFG, Roy HE, Pekar S. Long-term changes in communities of native coccinellids: population fluctuations and the effect of competition from an invasive non-native species. Insect Conservation and Diversity. 2016;9:202–209. doi: 10.1111/icad.12158. DOI

Jeffries MJ, Lawton JH. Enemy free space and the structure of ecological communities. Biological Journal of the Linnean Society. 1984;23:269–286. doi: 10.1111/j.1095-8312.1984.tb00145.x. DOI

Kamburov SS, Nadel DJ, Kenneth R. Observations on Hesperomyces virescens Thaxter (Laboulbeniales), a fungus associated with premature mortality of Chilocorus bipustulatus L. in Israel. Israel Journal of Agricultural Research. 1967;17:131–134.

Knapp M, Řeřicha M, Maršíková S, Harabiš F, Kadlec T, Nedvěd O, Teder T. Invasive host caught up with a native parasitoid: field data reveal high parasitism of Harmonia axyridis by Dinocampus coccinellae in Central Europe. Biological Invasions. 2019;21:2795–2802. doi: 10.1007/s10530-019-02027-4. DOI

Koch RL, Venette RC, Hutchison WD. Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the Western Hemisphere: implications for South America. Neotropical Entomology. 2006;35:421–434. doi: 10.1590/S1519-566X2006000400001. PubMed DOI

Konrad M, Grasse AV, Tragust S, Cremer S. Antipathogen protection versus survival costs mediated by an ectosymbiont in an ant host. Proceedings of the Royal Society B: Biological Sciences. 2015;282 doi: 10.1098/rspb.2014.1976. Article 20141976. PubMed DOI PMC

Lee JC, Bruck DJ, Dreves AJ, Ioriatti C, Vogt H, Baufeld P. In focus: spotted wing drosophila, Drosophila suzukii, across perspectives. Pest Management Science. 2011;67:1349–1351. doi: 10.1002/ps.2271. PubMed DOI

Lüdecke D. sjstats: statistical functions for regression models. 2018. https://CRAN.R-project.org/package=sjstats. https://CRAN.R-project.org/package=sjstats

Nalepa CA, Weir A. Infection of Harmonia axyridis (Coleoptera: Coccinellidae) by Hesperomyces virescens (Ascomycetes: Laboulbeniales): role of mating status and aggregation behavior. Journal of Invertebrate Pathology. 2007;94:196–203. doi: 10.1016/j.jip.2006.11.002. PubMed DOI

Nentwig W, Bacher S, Kumschick S, Pyšek P, Vilà M. More than 100 worst alien species in Europe. Biological Invasions. 2018;20:1611–1621. doi: 10.1007/s10530-017-1651-6. DOI

R Core Team . Vienna: R Foundation for Statistical Computing; 2018. R: a language and environment for statistical computing.

Raak-van den Berg CL, van Wielink PS, De Jong PW, Gort G, Haelewaters D, Helder J, Karssen G, van Lenteren JC. Invasive alien species under attack: natural enemies of Harmonia axyridis in the Netherlands. BioControl. 2014;59:229–240. doi: 10.1007/s10526-014-9561-3. DOI

Renkema JM, Cuthbertson AGS. Impact of multiple natural enemies on immature Drosophila suzukii in strawberries and blueberries. BioControl. 2018;63:719–728. doi: 10.1007/s10526-018-9874-8. DOI

Riddick EW. Ectoparasitic mite and fungus on an invasive lady beetle: parasite coexistence and influence on host survival. Bulletin of Insectology. 2010;63:13–20.

Riddick EW, Cottrell TE. Is the prevalence and intensity of the ectoparasitic fungus Hesperomyces virescens related to the abundance of entomophagous coccinellids? Bulletin of Insectology. 2010;63:71–78.

Riddick EW, Cottrell TE, Kidd KA. Natural enemies of the Coccinellidae: parasites, pathogens, and parasitoids. Biological Control. 2008;51:306–312. doi: 10.1016/j.biocontrol.2009.05.008. DOI

Roy HE, Brown PMJ, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S, Comont RF, De Clercq P, Eschen R, Estoup A, Evans EW, Facon B, Gardiner MM, Gil A, Grez AA, Guillemaud T, Haelewaters D, Herz A, Honek A, Howe AG, Hui C, Hutchison WD, Kenis M, Koch RL, Kulfan J, Lawson Handley L, Lombaert E, Loomans A, Losey J, Lukashuk AO, Maes D, Magro A, Murray KM, San Martin G, Martinkova Z, Minnaar I, Nedved O, Orlova-Bienkowskaja MJ, Rabitsch W, Ravn HP, Rondoni G, Rorke SL, Ryndevich SK, Saethre M-G, Sloggett JJ, Soares AO, Stals R, Tinsley MC, Vandereycken A, van Wielink P, Viglášová S, Zach P, Zaviezo T, Zhao Z. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biological Invasions. 2016;18:997–1044. doi: 10.1007/s10530-016-1077-6. DOI

Roy HE, Brown PMJ, Rothery P, Ware RL, Majerus MEN. Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. BioControl. 2008;53:265–276. doi: 10.1007/s10526-007-9122-0. DOI

Roy HE, Cottrell TE. Forgotten natural enemies: interactions between coccinellids and insect-parasitic fungi. European Journal of Entomology. 2008;105:391–398. doi: 10.14411/eje.2008.049. DOI

Roy HE, Lawson Handley L-J, Schönrogge K, Poland RL, Purse BV. Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? BioControl. 2011;56:451–468. doi: 10.1007/s10526-011-9349-7. DOI

Roy HE, Wajnberg E. From biological control to invasion: the ladybird Harmonia axyridis as a model species. BioControl. 2008;53:1–4. doi: 10.1007/s10526-007-9127-8. DOI

Sandoval-Aguilar JA, Guzmán-Franco AW, Pell JK, Clark SJ, Alatorre-Rosas R, Santillán-Galicia MT, Valdovinos-Ponce G. Dynamics of competition and co-infection between Zoophthora radicans and Pandora blunckii in Plutella xylostella larvae. Fungal Ecology. 2015;17:1–9. doi: 10.1016/j.funeco.2015.04.003. DOI

Sarfraz M, Keddie AB, Dosdall LM. Biological control of the diamondback moth, Plutella xylostella: a review. Biological Science and Technology. 2005;15:763–789. doi: 10.1080/09583150500136956. DOI

Schultheis EH, Berardi AE, Lau JA. No release for the wicked: enemy release is dynamic and not associated with invasiveness. Ecology. 2015;96:2446–2457. doi: 10.1890/14-2158.1. PubMed DOI

Shapiro-Ilan DI, Bruck DJ, Lacey LA. Principles of epizootiology and microbial control. In: Vega FE, Kaya HK, editors. Insect pathology. Second Edition. Amsterdam: Elsevier; 2012. pp. 29–72. DOI

Shapiro-Ilan DI, Cottrell TE. Susceptibility of lady beetles (Coleoptera: Coccinellidae) to entomopathogenic nematodes. Journal of Invertebrate Pathology. 2005;89:150–156. doi: 10.1016/j.jip.2005.04.002. PubMed DOI

Therneau T, Lumley T. Package ‘survival’, version 2.44-1.1. 2019. https://cran.r-project.org/web/packages/survival/survival.pdf https://cran.r-project.org/web/packages/survival/survival.pdf

van Wielink PS. Harmonia axyridis (Coleoptera: Coccinellidae): 13 jaar gevolgd met lichtvangsten in De Kaaistoep. Entomol. Ber. 2017;77:97–105.

Weir A, Beakes GW. Correlative light- and scanning electron microscope studies on the developmental morphology of Hesperomyces virescens. Mycologia. 1996;88:677–693. doi: 10.1080/00275514.1996.12026705. DOI

Fungal ectoparasites increase winter mortality of ladybird hosts despite limited effects on their immune system

Ectoparasitic fungi of Myrmica ants alter the success of parasitic butterflies