Eur. J. Entomol. 105 (3): 391-398, 2008 | DOI: 10.14411/eje.2008.049

Forgotten natural enemies: Interactions between coccinellids and insect-parasitic fungi

Helen E. ROY1, Ted E. COTTRELL2
1 NERC Centre for Ecology and Hydrology, Monks Wood, Huntingdon, Cambridgeshire, PE28 2LS, UK; e-mail: hele@ceh.ac.uk
2 USDA, Agricultural Research Service, Southeastern Fruit and Tree Nut Research Laboratory, 21 Dunbar Road, Byron, GA 31008 USA; e-mail: Ted.Cottrell@ars.usda.gov

The role of predators and parasitoids in the regulation of insect populations is widely reported in the context of both pest and non-pest insects. However, this is not the case for pathogens (entomopathogens). Indeed, most studies on insect life history refer only to predators and parasitoids when considering natural enemy guilds, even though naturally occurring entomopathogens are undoubtedly more diverse and widespread. This is certainly the case with the Coccinellidae; the natural enemies of coccinellids have been the subject of a number of review articles but pathogens receive only brief mention. In this review we attempt to address the balance and consider the interactions of natural populations of Coccinellidae with entomopathogenic fungi. Most research on entomopathogens and Coccinellidae focuses on the non-target impact of biorational insecticides against coccinellids and the impact of fungal infections upon aggregations of overwintering coccinellids; with the former overwhelmingly dominating the literature. Given the prominence of coccinellids in classical and conservation biological control, it is surprising that studies have not measured the natural impact of pathogenic fungi upon introduced species or natural populations of Coccinellidae, as has been done with numerous insect pest species. Here we review the literature on the intriguing interactions between coccinellids and fungal pathogens. We examine the literature on direct infection (sub-lethal and lethal) of coccinellids by pathogenic (Beauveria bassiana, Metarhizium anisopliae, Paecilomyces fumosoroseus) or parasitic (Hesperomyces virescens). We also consider the role of intra-guild predation (on the aphid-specific fungus Pandora neoaphidis and Beauveria bassiana) and finally indirect interactions such as coccinellids dispersing P. neoaphidis. We suggest that fungal pathogens are all too often forgotten natural enemies and future research should address the profound absence of knowledge in this field.

Keywords: Entomopathogenic fungi, ladybeetles, ladybirds, Coccinellidae, Beauveria bassiana, Hesperomyces virescens

Received: October 11, 2007; Revised: December 4, 2007; Accepted: December 4, 2007; Published: July 31, 2008  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
ROY, H.E., & COTTRELL, T.E. (2008). Forgotten natural enemies: Interactions between coccinellids and insect-parasitic fungi. EJE, 105(3), 391-398. doi: 10.14411/eje.2008.049
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. APPELBAUM S.W., KFIR R., GERSON U. & TADMOR U. 1971: Studies on the summer decline of Chilocorus bipustulatus in citrus groves of Israel. Entomophaga 16: 433-444 Go to original source...
    2. ASHER J., WARREN M., FOX R., HARDING P., JEFFCOATE G. & JEFFCOATE S. 2001: The Millennium Atlas of Butterflies in Britain and Ireland. Oxford University Press, 433 pp
    3. AYRES M.P. & LOMBARDERO M.J. 2000: Assessing the consequences of global change for forest disturbance from herbivores and pathogens. Sci. Total Environ. 262: 263-286 Go to original source...
    4. BALMFORD A., BENNUN L., TEN BRINK B., COOPER D., COTE I.M., CRANE P., DOBSON A., DUDLEY N., DUTTON I., GREEN R.E., GREGORY R., HARRISON J., KENNEDY E.T., KREMEN C., LEADERWILLIAMS N., LOVEJOY T., MACE M., MAY R., MAYAUX P., PHILLIPS J., REDFORD K., RICKETTS T.H., RODRIGUEZ J.P., SANJAYAN M., SCHEI P., VAN JAARSVELD A. & WALTHER B.A. 2005: Science and the Convention on Biological Diversity's 2010 target. Science 307: 212-213 Go to original source...
    5. BARRON A. & WILSON K. 1998: Overwintering survival in the seven spot ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae). Eur. J. Entomol. 95: 639-642
    6. BAUER L.S. & NORDIN G.L. 1988: Nutritional physiology of the eastern spruce budworm Choristoneura fumiferana, infected with Nosema fumiferanae, and interactions with dietary nitrogen. Oecologia 77: 44-50 Go to original source...
    7. BROWN P.M.J., ADRIAENS T., BATHON H., CUPPEN J., GOLDARAZENA A., HAGG T., KENIS M., KLAUSNITZER B.E., KOVAR I., LOOMANS A.J., MAJERUS M.E.N., NEDVED O., PEDERSEN J., RABITSCH W., ROY H.E., TERNOIS V., ZAKHAROV I., ROY D.B., WARE R.L. & MAJERUS M.E.N. 2008: Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl 53: 5-21 Go to original source...
    8. CAGAN L. & UHLIK V. 1999: Pathogenicity of Beauveria bassiana strains isolated from Ostrinia nubilalis Hbn. (Lepidoptera: Pyralidae) to original host larvae and to ladybirds (Coleoptera: Coccinellidae). Plant Prot. Sci. 35: 108-112 Go to original source...
    9. CERYNGIER P. & HODEK I. 1996: Enemies of Coccinellidae. In Hodek I. & Honek A. (eds): Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, pp. 319-350 Go to original source...
    10. CLAY K. 2003: Parasites lost. Nature 421: 585-586 Go to original source...
    11. COTTRELL T.E. & SHAPIRO-ILAN D.I. 2003: Susceptibility of a native and an exotic lady beetle (Coleoptera: Coccinellidae) to Beauveria bassiana. J. Invert. Pathol. 84: 137-144 Go to original source...
    12. COTTRELL T.E. & SHAPIRO-ILAN D.I. 2008: Susceptibility of endemic and exotic North American ladybirds (Coleoptera: Coccinellidae) to endemic fungal entomopathogens. Eur. J. Entomol. 105: 455-460 Go to original source...
    13. FEDERICI B.A. & MADDOX J.V. 1996: Host specificity in microbe-insect interactions. Bioscience 46: 410-421 Go to original source...
    14. FUXA Y. & TANADA J.R. 1987: Epizootiology of Insect Diseases. Wiley, New York, 555 pp
    15. GARCES S. & WILLIAMS R. 2004: First record of Hesperomyces virescens Thaxter (Laboulbeniales: Ascomycetes) on Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). J. Kans. Entomol. Soc. 77: 156-158 Go to original source...
    16. GINSBERG H.S., LEBRUN R.A., HEYER K. & ZHIOUA E. 2002: Potential nontarget effects of Metarhizium anisopliae (Deuteromycetes) used for biological control of ticks (Acari: Ixodidae). Environ. Entomol. 31: 1191-1196 Go to original source...
    17. GORDON R.D. 1985: The Coccinellidae (Coleoptera) of America north of Mexico. J. N. Y. Entomol. Soc. 93: 1-912
    18. HAJEK A. 2004: Natural Enemies: An Introduction to Biological Control. Cambridge University Press, Cambridge, 388 pp Go to original source...
    19. HAJEK A.E., BUTLER L. & WHEELER M.M. 1995: Laboratory bioassays testing the host range of the Gypsy moth fungal pathogen Entomophaga maimaiga. Biol. Cont. 5: 530-544 Go to original source...
    20. HAJEK A.E., BUTLER L., WALSH S.A.R., SILVER J.C., HAIN F.P., HASTINGS F.L., ODELL T.M. & SMITLEY D.R. 1996: Host range of the Gypsy moth (Lepidoptera: Lymantriidae) pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) in the field versus laboratory. Environ. Entomol. 25: 709-721 Go to original source...
    21. HARWOOD J.D., RICCI C., ROMANI R., PITZ K.M., WEIR A. & OBRYCKI J.J. 2006: Prevalence and association of the laboulbenialean fungus Hesperomyces virescens (Laboulbeniales: Laboulbeniaceae) on coccinellid hosts (Coleoptera: Coccinellidae) in Kentucky, USA. Eur. J. Entomol. 103: 799-804 Go to original source...
    22. HIBBETT D.S., BINDER M., BISCHOFF J.F., BLACKWELL M., CANNON P.F., ERIKSSON O.E., HUHNDORF S., JAMES T., KIRK P.M., LUCKING R., THORSTEN LUMBSCH H., LUTZONI F., BRANDON MATHENY P., MCLAUGHLIN D.J., POWELL M.J., REDHEAD S., SCHOCH C.L., SPATAFORA J.W., STALPERS J.A., VILGALYS R., AIME M.C., APTROOT A., BAUER R., BEGEROW D., BENNY G.L., CASTLEBURY L.A., CROUS P.W., DAI Y.C., GAMS W., GEISER D.M., GRIFFITH G.W., GUEIDAN C., HAWKSWORTH D.L., HESTMARK G., HOSAKA K., HUMBER R.A., HYDE K.D., IRONSIDE J.E., KOLJALG U., KURTZMAN C.P., LARSSON K.-H., LICHTWARDT R., LONGCORE J., MIADLIKOWSKA J., MILLER A., MONCALVO J.M., MOZLEY-STANDRIDGE S., OBERWINKLER F., PARMASTO E., REEB V., ROGERS J.D., ROUX C., RYVARDEN L., SAMPAIO J.P., SCHUSSLER A., SUGIYAMA J., THORN R.G., TIBELL L., UNTEREINER W.A., WALKER C., WANG Z., WEIR A., WEISS M., WHITE M.M., WINKA K., YAO Y.J. & ZHANG N. 2007: A higher-level phylogenetic classification of the Fungi. Mycol. Res. 111: 509-547 Go to original source...
    23. HICKLING R., ROY D.B., HILL J.K., FOX R. & THOMAS C.D. 2006: The distributions of a wide range of taxonomic groups are expanding polewards. Glob. Change Biol. 12: 450-455 Go to original source...
    24. HODEK I. & HONEK A. (eds): Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, 484 pp
    25. IPERTI G. 1966: Protection of coccinellids against mycosis. In Hodek I. (ed.): Ecology of Aphidophagous Insects. Academia Prague & Dr W. Junk, Dordrecht, The Hague, pp. 189-190
    26. JAMES R.R. & LIGHTHART B. 1994: Susceptibility of the convergent lady beetle (Coleoptera: Coccinellidae) to four entomogenous fungi. Environ. Entomol. 23: 190-192 Go to original source...
    27. JAMES R.R., SHAFFER B.T., CROFT B., LIGHTHART B. 1995: Field evaluation of Beauveria bassiana: its persistence and effects on the pea aphid and a non-target coccinellid in alfalfa. Biocon. Sci. Technol. 5: 425-438 Go to original source...
    28. JAMES R.R., CROFT B.A., SHAFFER B.T. & LIGHTHART B. 1998: Impact of temperature and humidity on host-pathogen interactions between Beauveria bassiana and a coccinellid. Environ. Entomol. 27: 1506-1513 Go to original source...
    29. KAMBUROV S.S., NADEL D.J. & KENNETH R. 1967: Observations on Hesperomyces virescens Thaxter (Laboulbeniales), a fungus associated with premature mortality of Chilocorus bipustulatus L. in Israel. Israel J. Agric. Res. 17: 131-134
    30. KOCH R.L. 2003: The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. J. Insect Sci. 3: 1-16 Go to original source...
    31. KOCH R.L. & GALVAN T.L. 2008: Bad side of a good beetle: The North American experience with Harmonia axyridis. BioControl 53: 23-35 Go to original source...
    32. KUZNETSOV V.N. 1997: Lady Beetles of the Russian Far East. Memoir no. 1, Center for Systematic Entomology, The Sandhill Crane Press, Gainesville, 248 pp
    33. LACEY L.A., FRUTOS R., KAYA H.K. & VAIL P. 2001: Insect pathogens as biological control agents: do they have a future? Biol. Contr. 21: 230-248 Go to original source...
    34. MAJERUS M.E.N. 1994: Ladybirds. Harper Collins, London, 367 pp
    35. MEYLING N.V. & PELL J.K. 2006: Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecol. Entomol. 31: 162-171 Go to original source...
    36. NALEPA C.A. & 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: 196-203 Go to original source...
    37. ORMOND E.L., THOMAS A.P.M., PELL J.K. & ROY H.E. 2006: Overwintering ecology of Coccinella septempunctata, Beauveria bassiana and Dinocampus coccinellae. In Walter A.H., Rossing W.A.H., Eggenschwiler L. & Poehling H.-M. (eds): Working Group "Landscape management for functional biodiversity" at Zuerich-Reckenholz (Switzerland), 16-19 May 2006. IOBC/WPRS Bulletin 29(6): 85-88
    38. OSTFELD R.S., GLASS G.E. & KEESING F. 2005: Spatial epidemiology: an emerging (or re-emerging) discipline. Trends Ecol. Evol. 20: 328-336 Go to original source...
    39. PARMESAN C. & YOHE G. 2003: A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37-42 Go to original source...
    40. PELL J.K. & VANDENBERG J.D. 2002: Interactions among the aphid Diuraphis noxia, the entomopathogenic fungus Paecilomyces fumosoroseus and the coccinellid Hippodamia convergens. Biocontrol Sci. Techn. 12: 217-224 Go to original source...
    41. PELL J.K., PLUKE R., CLARK S.J., KENWARD M.G. & ALDERSON P.G. 1997: Interactions between two aphid natural enemies, the entomopathogenic fungus Pandora neoaphidis Remaudiere & Hennebert (Zygomycetes: Entomophthorales) and the predatory beetle Coccinella septempunctata L. (Coleoptera: Coccinellidae). J. Invertebr. Pathol. 69: 261-268 Go to original source...
    42. PELL J.K., BAVERSTOCK J., ROY H.E., WARE R.L. & MAJERUS M.E.N. 2008: Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl. 53: 147-168 Go to original source...
    43. PINGEL R.L. & LEWIS L.C. 1996: The fungus Beauveria bassiana (Balsamo) Vuillemin in a corn ecosystem: its effect on the insect predator Coleomegilla maculata De Geer. Biol. Control 6: 137-141 Go to original source...
    44. POLIS G.A. & HOLT R.D. 1992: Intraguild predation: the dynamics of complex trophic interactions. Trends Ecol. Evol. 7: 151-154 Go to original source...
    45. POPRAWSKI T.J., LEGASPI J.C. & PARKER P.E. 1998: Influence of entomopathogenic fungi on Serangium parcesetosum (Coleoptera: Coccinellidae), an important predator of whiteflies (Homoptera: Aleyrodidae). Environ. Entomol. 27: 785-795 Go to original source...
    46. RIDDICK E.W. 2005: 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: 1-15 Go to original source...
    47. RIDDICK E.W. & SCHAEFER P.W. 2005: Occurrence, density and distribution of parasitic fungus Hesperomyces virescens (Laboulbeniales: Laboulbeniaceae) on multicoloured Asian beetle (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Am. 98: 615-624 Go to original source...
    48. ROY H.E. 1997: Interactions Between Aphid Predators and the Entomopathogenic Fungus Erynia neoaphidis. PhD Thesis, University of Nottingham
    49. ROY H.E. & J.K. PELL 2000: Interactions between entomopathogenic fungi and other natural enemies: Implications for biological control. Biocontrol Sci. Techn. 10: 737-752 Go to original source...
    50. ROY H.E., PELL J.K., CLARK S.J. & ALDERSON P.G. 1998: Implications of predator foraging on aphid pathogen dynamics. J. Invert. Pathol. 71: 236-247 Go to original source...
    51. ROY H.E., PELL J.K. & ALDERSON P.G. 1999: Effects of fungal infection on the alarm response of pea aphids. J. Invert. Pathol. 74: 69-75 Go to original source...
    52. ROY H.E., PELL J.K. & ALDERSON P.G. 2001: Targeted dispersal of the aphid pathogenic fungus Erynia neoaphidis by the aphid predator Coccinella septempunctata. Biocontrol Sci. Techn. 11: 101-112 Go to original source...
    53. ROY H.E., PELL J.K. & ALDERSON P.G. 2002: Effect of Erynia neoaphidis infection and coccinellid foraging on the spatial distribution of aphids on plants. J. Invert. Pathol. 81: 127-129 Go to original source...
    54. ROY H.E., PELL J.K. & ALDERSON P.G. 2003: Effect of spatial heterogeneity on the role of Coccinella septempunctata as an intra-guild predator of the aphid pathogen Pandora neoaphidis. J. Invert. Pathol. 82: 85-95 Go to original source...
    55. ROY H.E., STEINKRAUS D., EILENBERG E., HAJEK A. & PELL J.K. 2006a: Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu. Rev. Entomol. 51: 331-357 Go to original source...
    56. ROY H.E., BROWN P. & MAJERUS M.E.N. 2006b: Harmonia axyridis: A successful biocontrol agent or an invasive threat? In Eilenberg J. & Hokkanen H. (eds): An Ecological and Societal Approach to Biological Control. Kluwer Academic Publishers, Dordrecht, pp. 295-309 Go to original source...
    57. ROY H.E., BAVERSTOCK J., WARE R.L., CLARK S.J., MAJERUS M.E.N., BAVERSTOCK K.E. & PELL J.K. 2008a: Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis. Ecol. Entomol. 33: 175-182 Go to original source...
    58. ROY H.E., BROWN P.M.J., ROTHERY P., WARE R.L. & MAJERUS M.E.N. 2008b: Interactions between the fungal pathogen Beauveria bassiana and three species of ladybird: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. BioControl. 53: 265-276 Go to original source...
    59. SANTAMARIA S. 2001: Taxonomy and morphology of Amorphomyces (Laboulbeniales). Mycol. Res. 104: 1389-1398 Go to original source...
    60. SHAPIRO-ILAN D.I. & COTTRELL T.E. 2005: Susceptibility of lady beetles (Coleoptera: Coccinellidae) to entomopathogenic nematodes. J. Invert. Pathol. 89: 150-156 Go to original source...
    61. SMITH S.F. & KRISCHIK V.A. 2000: Effects of biorational pesticides on four coccinellid species (Coleoptera: Coccinellidae) having potential as biological control agents in interiorscapes. J. Econ. Entomol. 93: 732-736 Go to original source...
    62. SOLTER L.F. & MADDOX J.V. 1998: Physiological host specificity of Microsporidia as an indicator of ecological host specificity. J. Invert. Pathol. 71: 207-216 Go to original source...
    63. TANADA Y. & KAYA H.K. 1993: Insect Pathology. Academic Press, San Diego, 666 pp
    64. TAVARES I.I. 1979: The Laboulbeniales and their arthropod hosts. In Batra L.R. (ed.): Insect-Fungus Symbiosis: Nutrition, Mutualism, and Commensalism. John Wiley & Sons, New York, pp. 229-258
    65. TAVARES I.I. 1985: Laboulbeniales (Fungi, Ascomycetes). Mycol. Mem. 9: 1-627
    66. THAXTER R. 1931: Contribution towards a monograph of the Laboulbeniaceae. Mem. Am. Acad. Arts Sci. 16: 1-435 Go to original source...
    67. TODOROVA S.I., COTE J.-C., MARTEL P. & CODERRE D. 1994: Heterogeneity of two Beauveria bassiana strains revealed by biochemical tests, protein profiles and bio-assays of Leptinotarsa decemlineata (Col.: Chrysomelidae) and Coleomegilla macultata lengi (Col.: Coccinellidae) larvae. BioControl 39: 159-169 Go to original source...
    68. TODOROVA S.I., COTE J.C. & CODERRE D. 1996: Evaluation of the effects of two Beauveria bassiana (Balsamo) Vuillemin strains on the development of Coleomegilla maculata lengi Timberlake (Col., Coccinellidae). J. Appl. Entomol. 120: 159-163 Go to original source...
    69. TODOROVA S.I., CODERRE D. & COTE J.C. 2000: Pathogenicity of Beauveria bassiana isolates toward Leptinotarsa decemlineata (Coleoptera: Chrysomelidae), Myzus persicae (Homoptera: Aphididae) and their predator Coleomegilla maculate lengi (Coleoptera: Coccinellidae) Phytoprotection 81: 15-22 Go to original source...
    70. UNDEEN A.H. & MADDOX J.V. 1973: Infection of nonmosquito host by injection with spores of the microsporidan Nosema algerae. J. Invert. Pathol. 22: 258-265 Go to original source...
    71. VAN DEN BOSCH R., SCHLINGER E.I., DIETRICK E.J., HAGEN K.S. & HALLOWAY J.K. 1959: The colonization and establishment of imported parasites of the spotted alfalfa aphid in California. J. Econ. Entomol. 52: 136-141 Go to original source...
    72. VAN DEN BOSCH R. 1968: Comments on population dynamics of exotic insects. Bull. Entomol. Soc. Am. 14: 112-115 Go to original source...
    73. WATSON R.T., HEYWOOD V.H., BASTE I., DIAS B., GAMEZ R., JANETOS T., REID W. & RUARK R. 1995: Global Biodiversity Assessment. Cambridge University Press, Cambridge, 1140 pp
    74. WEIR A. & BEAKES G.W. 1996: Correlative light- and scanning electron microscope studies on the developmental morphology of Hersperomyces virescens. Mycologia 88: 677-693 Go to original source...
    75. WEIR A. & HAMMOND P.M. 1997: Laboulbeniales on beetles: host utilization patterns and species richness of the parasites. Biodiv. Conserv. 6: 701-719 Go to original source...
    76. WELCH V.L., SLOGGETT J.J., WEBBERLEY K.M. & HURST G.D.D. 2001: Short-range clinal variation in the prevalence of a sexually transmitted fungus associated with urbanisation. Ecol. Entomol. 26: 547-550 Go to original source...
    77. YINON U. 1969: The natural enemies of the armored scale ladybeetle Chilocorus bipustulatus (Col. Coccinellidae). Entomophaga 14: 321-328 Go to original source...

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content