Mycophagy in Coccinellidae: Review and synthesis

Biological Control

Volumn 51, Issue 2, 2009, Pages 284-293

  Sutherland, Andrew M ^a   Parrella, Michael P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biological control; Erysiphales; Halyzia; Illeis; Integrated disease management; Macroilleis; Mechanical disease transmission; Mycophagy; Plant pathogen; Powdery mildew; Psyllobora; Vibidia

Indexed keywords

COCCINELLIDAE; COCCINELLINAE; COCCINELLINI; ERYSIPHALES; FUNGI; HALYZIINI; HEXAPODA; MAGNOLIOPHYTA; PSYLLOBORA;

EID: 70349283016     PISSN: 10499644     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocontrol.2009.05.012     Document Type: Review

References (103)

1. Ahmad M., Younis G., and Ali N. Biology of the coccinellid Psyllobora (Thea) bisoctonotata Muls. (Coleoptera: Coccinellidae) a predator of powdery mildew fungi (2003), Proceedings of the Eighth Arab Congress of Plant Protection, Elbeida City, Libya
2. Almeida L.M. Study of 17 species of the genus Psyllobora Chevrolat, 1837 (Coleoptera: Coccinellidae). Acta Biologica Paranaense Curitiba 14 (1985) 47-102
3. Almeida L.M., and Milleo J. The immature stages of Psyllobora gratiosa Mader, 1958 (Coleoptera: Coccinellidae) with some biological aspects. Journal of the New York Entomological Society 106 (1998) 170-176
4. Amano K. Host Range and Geographical Distribution of the Powdery Mildew Fungi (1986), Japan Scientific Societies Press, Tokyo
5. Anderson J.M.E. Seasonal habitat utilization and food of the ladybirds Scymnodes lividigaster (Mulsant) and Leptothea galbula (Mulsant) (Coleoptera: Coccinellidae). Australian Journal of Zoology 30 (1982) 59-70
6. Bado S.G., and Rodriguez S.M. Aspectos morfologicos y biologicos de una vaquita micetofaga Psyllobora bicongregata B. (Coleoptera: Coccinellidae). Revista de la Facultad de Agronomia Universidad de Buenos Aires 3 (1998) 181-184
7. Borner C., and Heinze K. Aphidina. In: Sorauer P. (Ed). Handbuch der Pflanzenkrankheiten (1957), Berlin-Hamburg
8. Braun U., Cook R.T.A., Inman A.J., and Shin H.D. The taxonomy of powdery mildew fungi. In: Belanger R.R., Bushnell W.R., Dik A.J., and Carver T.L.W. (Eds). The Powdery Mildews: A comprehensive treatise (2002), St. Paul, APS Press 13-55
9. California Department of Pesticide Regulation, 2004. Summary of pesticide use report data 2003. Available from: .
10. Carter M.C., and Dixon A.F.G. Honeydew: an arrestant stimulus for cocinellids. Ecological Entomology 9 (1984) 383-387
11. Casey T.L. A revision of the American Coccinellidae. Journal of the New York Entomological Society 7 (1899) 71-169
12. Chapuis F. Genera des Coleopteres ou expose methodique et critique de tous les genres proposes jusqu'ici dans cet ordre d'insectes. (Coccinellides). Paris 12 (1876) 149-259
13. Chase, A.R., 2004. Making the grade: new fungicides for ornamentals. In: Society of American Florists Proceedings for 20th Annual Conference on Pest Management on Ornamentals, pp. 1-5.
14. Cividanes T.M., Cividanes F.J., and Matos B.A. Biologia de Psyllobora confluens alimentada com o fungo Erysiphe cichoracearum. Pesquisa Agropecuaria Brasileira, Brasilia 42 (2007) 1675-1679
15. Coop L.B., and Croft B.A. Neoseiulus fallacis: dispersal and biological control of Tetranychus urticae following minimal inoculations into a strawberry field. Experimental and Applied Acarology 19 (1995) 31-43
16. Crowson R.A. The Biology of Coleoptera (1981), New York, Academic Press
17. Cruz B., Gonzalez-Avila M., and Soto L. Psyllobora nana (Coleoptera: Coccinellidae), biological control agent of dusty mildew. Ciencias de la Agricultura 36 (1989) 151
18. Davidson W.M. Observations on Psyllobora taedata LeConte, a coccinellid attacking mildews. Entomology News 32 (1921) 83-89
19. Dejean, P.F.M.A., 1837. Catalogue des coleopteres de la collection M. le Conte Dejean, third ed. Paris, Mequignon-Marvis, pp. 1-458.
20. del Pino, D., Olalla, L., Canovas, I., Cazorla, F.M., deVicente, A., Tores, J.A., 1999. Resistance to fungicides of Sphaerotheca fuliginea strains isolated from southern Spain. International Powdery Mildew Conference, 1st, Avignon, France, 42.
21. Delp C. Effect of temperature and humidity on the grape powdery mildew fungus. Phytopathology 44 (1954) 615-626
22. Dharpur S.R., Rao M.K., and Sagar R.B.S. New record of a mycophagous beetle, Thea cincta Fabr. on powdery mildew of niger. Journal of Oilseeds Research 7 (1990) 124-125
23. English-Loeb G., Norton A., Gadoury D.M., Seem R.C., and Wilcox W.F. Control of powdery mildew in wild and cultivated grapes by a tydeid mite. Biological Control 14 (1999) 97-103
24. Falk S.P., Gadoury D.M., Cortesi P., Pearson R.C., and Seem R.C. Partial control of grape powdery mildew by the mycoparasite Ampelomyces quisqualis. Plant Disease 79 (1995) 483-490
25. Food and Agricultural Organisation, 1967. Crop losses due to disease and pests. F.A.O., Rome.
26. Fulmek L. Insekten als Blattlausfeinde. Annalen des Naturhistorischen Museums, Wien 61 (1957) 110-227
27. Fursch H. Taxonomy of Coccinellidae. Coccinella 6 (1996) 28-30
28. Giorgi J.A., Vandenberg N.J., McHugh J.V., Forrester J.A., Ślipiński S.A., Miller K.B., Shapiro l.R., and Whiting. The evolution of food preferences in Coccinellidae. Biological Control 51 (2009) 215-231
29. Glawe D.A. The powdery mildews: a review of the world's most familiar (yet poorly known) plant pathogens. Annual Review of Phytopathology 46 (2008) 27-51
30. Gordon R.D. The Coccinellidae (Coleoptera) of America north of Mexico. Journal of the New York Entomological Society 93 (1985) 1-912
31. Gubler W.D., Ypema H.L., Ouimette D.G., and Bettiga L.J. Occurrence and development of resistance in Uncinula necator to triadimefon, myclobutanil and fenarimol in California grapevines. Plant Disease 80 (1996) 902-909
32. Heaney, S.P., Hall, A.A., Davies, S.A., Olaya, G., 2000. Resistance to fungicides in the QoI-STAR cross-resistance group: current perspectives. In: Conference Proceedings: British Crop Protection Council Conference on Pests and Diseases, pp. 755-762.
33. Hed B.E., Windham M.T., and Grant J.F. Survival of conidia of Discula destructiva in frass of the convergent lady beetle. Plant Disease 83 (1999) 806-809
34. Hodek, I., 1973. Biology of Coccinellidae. Prague, 260 pp.
35. Hodek I., and Honěk A. Ecology of Coccinellidae (1996), Kluwer Academic Publishers, Netherlands 464 pp
36. Hukusima S., and Itoh K. Pollen and fungus as food for some coccinellid beetles. Research Bulletin of the Faculty of Agriculture, Gifu University 39 (1976) 31-38
37. Kaltenbach J.H. Die Pflanzenfeinde aus der Klasse der Insecten (1874), Julius Hoffmann, Stuttgart
38. Korner O., and Challa H. Process-based humidity control regime for greenhouse crops. Computers and Electronics in Agriculture 39 (2003) 173-192
39. Korschefsky, R., 1932. Coleopterorum Catalogus. XVI {120}, Coccinellidae II. W. Junk. Berlin, pp. 565-570.
40. Kovar I. Phylogeny. In: Hodek I., and Honěk A. (Eds). Ecology of Coccinellidae (1996), Kluwer Academic Publishers, Netherlands 19-31 464 pp
41. Kreiter S., Sentenac G., Barthes D., and Auger P. Toxicity of four fungicides to the predaceous mite Typhlodromus pyri (Acari: Phytoseiidae). Journal of Economic Entomology 91 (1998) 802-810
42. Krishnakumar R., and Maheswari P. Management of powdery mildew in mulberry using coccinellid beetles, Illeis cincta (Fabricius) and Illeis bistigmosa (Mulsant). Journal of Entomological Research 28 (2004) 241-246
43. Kuznetsov, V.N., 1997. Lady Beetles of the Russian Far East. Memoir No.1, Center for Systematic Entomology, Sandhill Crane Press, Gainesville, 248 pp.
44. Lamari L. ASSESS: Image analysis software for plant disease quantification (2005), American Phytopathological Society Press, St. Paul, MN, USA
45. Lawrence J.F. Mycophagy in the coleoptera. In: Wilding N., Collins N.M., Hammond P.M., and Webber J.F. (Eds). Insect-Fungus Interactions vol. 14 (1989), Symposium of the Royal Entomological Society, London 2-23
46. Lawrence J.F., and Hlavac T. Review of the Derodontidae (Coleoptera: Polyphaga) with new species from North America and Chile. Coleopterists Bulletin 33 (1979) 369-414
47. Leschen R.A.B. Beetles feeding on bugs (Coleoptera, Hemiptera): repeated shifts from mycophagous ancestors. Invertebrate Taxonomy 14 (2000) 917-929
48. Lichteinstein J.L. Observations sur les Coccinellides mycophages (Col.). Bulletin of the Society of Entomology of France, Paris 29 (1917) 8-302
49. Lima A.C. Coccinellideos mycophagos. (Coccinellidae: Psylloborini). Revista Entomologia, Rio de Janeiro 1 (1931) 428-430
50. Liu C.L. Studies on the feeding capacity and life history of a mycophagous coccinellid, Halyzia hauseri Mader, in Kunming. Annales Entomologici Sinici 1 (1951) 1-15
51. Liu H.L. Management of rose powdery mildew with automatic water sprays. Plant Protection Bulletin Taichung 43 (2001) 7-16
52. Lundgren J.G. Relationships of Natural Enemies and Non-prey Foods (2009), Springer, Dordrecht, The Netherlands
53. Lundgren J.G. Nutritional aspects of non-prey foods in the life histories of predaceous Coccinellidae. Biological Control 51 (2009) 294-305
54. Lundgren J.G., and Wiedenmann R.N. Nutritional suitability of field corn pollen as food for the predator, Coleomegilla maculata (Coleoptera: Coccinellidae). Journal of Insect Physiology 50 (2004) 567-575
55. Majerus M.E.N. Ladybirds (1994), Harper Collins Publishers, London 367 pp
56. Majka C.G., and McCorquodale D.B. The Coccinellidae (Coleoptera) of the maritime provinces of Canada: new records, biogeographic notes, and conservation concerns. Zootaxa 1154 (2006) 49-68
57. Martelli G. Sulla micofagia del Coccinellide Thea vigintiduopunctata L. Bollettino del Laboratorio di Entomologia, Portici 4 (1910) 292-294
58. Martelli G. Notizie su due Coccinellido micofagi. Bollettino del Laboratorio di Zoologia, Portici 5 (1914) 151-160
59. Martinson T., Williams III L., and English-Loeb G. Compatibility of chemical disease and insect management practices used in New York vineyards with biological control by Anagrus spp. (Hymenoptera: Mymaridae), parasitoids of Erythroneura leafhoppers. Biological Control 22 (2001) 227-234
60. McGrath M.T. Fungicide resistance in cucurbit powdery mildew: Experiences and challenges. Plant Disease 85 (2001) 236-246
61. Michaud J.P. Responses of two ladybeetles to eight fungicides used in Florida citrus: Implications for biological control. Journal of Insect Science 1 (2001) 1-6
62. Michaud J.P., and Grant A.K. Suitability of pollen sources for the development and reproduction of Coleomegilla maculata (Coleoptera: Coccinellidae) under simulated drought conditions. Biological Control 32 (2005) 363-370
63. Mulsant, M.E., 1850. Species de Coleopteres trimeres securipalpes. Annales des Sciences physiques et naturelles de Lyon 2, 1104 pp.
64. Norton A.P., English-Loeb G., and Belden E. Host plant manipulation of natural enemies: leaf domatia protect beneficial mites from insect predators. Oecologia 126 (2001) 535-542
65. Omkar, and Pervez A. New record of coccinellids from Uttar Pradesh. Journal of Advanced Zoology 20 (1999) 106-112
66. Pakaluk J., Ślipiński S.A., and Lawrence J.F. Current classification and family-group names in Cucujoidea (Coleoptera). Genus 5 (1994) 223-268
67. Paulitz T.C., and Belanger R.R. Biological control in greenhouse systems. Annual Review of Phytopathology 39 (2001) 103-133
68. Pearson R.C., and Goheen A.C. Compendium of Grape Diseases (1988), American Phytopathological Society Press, St. Paul, Minnesota 93 pp
69. Poorani J.K., and Ślipiński A. Notes on the genus Protothea Weise with redescription of P. Quadripunctata (Mulsant) (Coleoptera: Coccinellidae: Coccinellini). Annales Zoologici 55 (2005) 329-333
70. Pope R.D. A revision of the Australian Coccinellidae (Coleoptera) Part 1. Subfamily Coccinellinae. Invertebrate Taxonomy 2 (1988) 633-735
71. Prasad R., and Rai M. New record of a mycophagous beetle, Thea cincta Fabr., on powdery mildew of linseed. Farm Science Journal 3 (1988) 89-90
72. Putman W.L. Occurrence and food of some coccinellids (Coleoptera) in Ontario peach orchards. The Canadian Entomologist 96 (1964) 1149-1155
73. Ratti E. Coleoptera associated with Oidium evonymi-japonici (Arc.) Sacc. (fungi imperfecti) in the urban gardens of Venice. Bollettino del Museo Civico di Storia Naturale di Venezia 45 (1996) 47-51
74. Ricci C. Sulla costituzione e funyione delle mandibole delle larve di Tytthaspis sedecimpunctata (L.) e Tytthaspis trilineata (Weise). Frustula Entomologica 3 (1982) 205-212
75. Ricci C. Seasonal food preferences and behavior of Rhyzobius litura. In: Hodek I. (Ed). Ecology of Aphidophaga (1986), Academia, Prague & Dr. W. Junk, Dordrecht 119-123
76. Ricci C., Fiori G., and Colazza S. Regime alimentare dell'adulto di Tytthaspis sedecimpunctata (L.) (Coleoptera: Coccinellidae) in ambiente a influenza antropica primaria: prato polifita. Atti XIII Congresso Nazional Italiano Entomologia Sestriere-Torino 69 (1983) 1-698
77. Samways M.J., Osborn R., and Saunders T.L. Mandible form relative to the main food type in ladybirds (Coleoptera: Coccinellidae). Biocontrol Science and Technology 7 (1997) 275-286
78. Sasaji H. Phylogeny of the family Coccinellidae (Coleoptera). Etizenia. Occasional Publication of the Biological Laboratory Fukui University 35 (1968) 1-37
79. Savoiskaya G.I. Investigation of the biology of the Coccinellidae of southeastern Kazakhstan. Uchenye Zapiski Toksk Gosudarstvennogo Pedagogicheskogo Instituta 19 (1961) 107-117
80. Schilder F.A., and Schilder M. Die nahrung der Coccinelliden und ihre Beziehung zur Verwandtschaft der Arten. Arbeiten aus der Biologischen Reichsanstalt fur Land- und Forstwirtschaft 16 (1928) 213-282
81. Sivapalan A. Effects of impacting rain drops on the growth and development of powdery mildew fungi. Plant Pathology 42 (1993) 256-263
82. Ślipiński S.A., and Pakaluk J. Problems in the classification of the cerylonid series of Cucujoidea (Coleoptera). In: Zunino M., Belles X., and Blas M. (Eds). Advances in Coleopterology (1991), Silvestrelli and Cappelletto, Torino 79-88
83. Solomon M.E. The natural control of animal populations. Journal of Animal Ecology 18 (1949) 1-35
84. Soylu S., and Yigit A. Feeding of mycophagous ladybird, Psyllobora bisoctonotata (Muls.) on powdery mildew infested plants. Biological Control of Fungal and Bacterial Plant Pathogens. International Organization for Biological Control Western Palearctic Regional Section Bulletin 25 (2002) 183-186
85. Stanghellini M.E., Rasmussen S.L., and Kim D.H. Aerial transmission of Thielaviopsis basicola, a pathogen of corn-salad, by adult shore flies. Phytopathology 89 (1999) 476-479
86. Strouhal H. Pilzfressende Coccinelliden (Tribus Psylloborini). Zeitschrift für wissenschaftlichen Insekten-biologie 21 (1926) 131-143
87. Sutherland, A.M., 2005. Evaluation of Psyllobora vigintimaculata (Say) (Coleoptera: Coccinellidae) for Biological Control of Powdery Mildew Fungi (Erysiphales). M.S. thesis, University of California, Davis
88. Sutherland, A.M., Parrella, M.P., 2006. Quantification of powdery mildew consumption by a native coccinellid: implications for biological control? In: Hoddle, M.S., Johnson, M.W. (Eds.), California Conference on Biological Control 5 (Riverside). Proceedings, pp. 188-192.
89. Sutherland A.M., and Parrella M.P. Biology and co-occurrence of Psyllobora vigintimaculata (Coleoptera: Coccinellidae) and powdery mildews in an urban landscape of California. Annals of the Entomological Society of America 102 (2009) 484-491
90. Takamatsu S. Phylogeny and evolution of the powdery mildew fungi (Erysiphales, Ascomycota) inferred from nuclear ribosomal DNA sequences. Mycoscience 45 (2004) 147-157
91. Takeuchi M., Sasaki Y., Sato C., Iwakuma S., Isozaki A., and Tamura M. Seasonal host utilization of mycophagous ladybird Illeis koebelei (Coleoptera: Coccinellidae). Japanese Journal of Applied Entomology and Zoology 44 (2000) 89-94
92. Thomas M.C. A new species of Cryptolestes Ganglbauer from the Middle East and a new synonym (Coleoptera: Laemophloeidae [Cucujidae sensu lato]). Israel Journal of Entomology 27 (1993) 113-118
93. Timberlake P.H. The Coccinellidae or ladybeetles of the Koebele Collection. Part 1. Hawaiian Planters' Record. Honolulu 47 (1943) 1-67
94. Traquair J.A., Shaw L.A., and Jarvis W.R. New species of Stephanoascus with Sporothrix anamorphs. Canadian Journal of Botany 66 (1988) 929-933
95. Triltsch H. Food remains in the guts of Coccinella septempunctata (Coleoptera: Coccinellidae) adults and larvae. European Journal of Entomology 96 (1999) 355-364
96. Turian G. Coccinelles micromycetophages (Col.). Mitteilungen der Schweizerischen Entomologischen Gesellschaft 42 (1969) 52-57
97. Turian G. Thea 22-punctata et autres Coccinelles micromycetophages. Nature du pigment elytral jaune. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 44 (1971) 277-280
98. Vandenberg, N.J., 2002. Family 93. Coccinellidae Latreille 1807. In: Arnett, R.H. Jr., Thomas, M.C., Skelley, P.E., Frank, J.H. (Eds.), American Beetles. Polyphaga: Scarabaeoidea through Curculionoidea, vol. 2. CRC Press LLC, Boca Raton, FL, pp. 371-389.
99. Weber D.C., and Lundgren J.G. Assessing the trophic ecology of the Coccinellidae: Their roles as predators and as prey. Biological Control 51 (2009) 199-214
100. Weise J. Berichtigung von Beobachtungen über die Nahrung unserer Coccinelliden. Deutsche entomologische Zeitschrift 2 (1900) 297-301
101. Wu X.B., and Guo X.L. Primary study on control of powdery mildew by ladybugs. Journal of Northeast Forestry University China 15 (1987) 13-17
102. Yurtsever S. A preliminary study on the ladybirds (Coleoptera: Coccinellidae) of Edirne in north-western Turkey. Turkish Journal of Zoology 25 (2001) 71-75
103. Zoebelein G. Der Honigtau als Nahrung der Insekten. Zeitschrift für angewandte Entomologie 38 (1956) 369-416