Abstract
Microcera coccophila has been regarded as an entomopathogen of armoured scales in Australia since the late 1800s. We confirmed its identity and presence in Australia using morphological and molecular data. We also confirmed that a related species, M. larvarum, is an entomopathogen of armoured scales in Australia. M. coccophila was recorded as a parasite of Aonidiella aurantii, A. citrina, Lepidosaphes beckii, L. gloverii and Unaspis citri in citrus orchards on the Central Coast of New South Wales. We recorded M. larvarum in these orchards in association with A. aurantii and one or more hosts that could not be identified due to their condition. The sexual and asexual morphs of both species are described. Genetic variation suggested that the taxa could represent various phylogenetic species. We fulfilled Koch’s postulates for both fungi in separate bioassays with Aspidiotus nerii. Infection was not dependent on the reproductive status of the scale. A laboratory study showed that Iridomyrmex rufoniger, a common ant in Australian citrus orchards, can passively disperse conidia of M. coccophila. Field observations suggested that the prevalence of the two fungal parasites in orchards is influenced by host scale densities, climate, and foraging by I. rufoniger workers on honeydew produced by their sternorrhynchan trophobionts, particularly Saissetia oleae. These foraging activities induced dense populations of A. aurantii by disrupting the activities of the scale’s natural arthropod enemies; this was followed by epizootics of M. coccophila that decimated populations of the scale.
Similar content being viewed by others
References
Annecke DP (1963) Observations on some citrus pests in Mozambique and Southern Rhodesia. J Entomol Soc S Afr 26:195–225
Bailey FM (1888) A synopsis of the Queensland flora. Second supplement. James C. Beal Government Printer, Brisbane
Bills GF, Platas G, Overy DP, Collado J, Fillola A, Jiménez MR, Martín J, del Val AG, Vicente F, Tormo JB, Peláez F, Calati K, Harris G, Parish C, Roemer T (2009) Discovery of the parnafungins, antifungal metabolites that inhibit mRNA polyadenylation, from the Fusarium larvarum complex and other hypocrealean fungi. Mycologia 101:449–472. doi:10.3852/08-163
Bird AE, Hesketh H, Cross JV, Copland M (2004) The common black ant, Lasius niger (Hymenoptera: Formicidae), as a vector of the entomopathogen Lecanicillium longisporum to rosy apple aphid, Dysaphis plantaginea (Homoptera: Aphididae). Biocontrol Sci Tech 14:757–767. doi:10.1080/09583150410001720716
Booth C (1971) The genus Fusarium. Commonwealth Mycological Institute, Kew
Booth C (1981) Nectria aurantiicola. CMI Descr Pathog Fung Bact 714:1–2
Burgess LW, Summerell BA, Bullock S, Gott KP, Backhouse D (1994) Laboratory manual for Fusarium research. Fusarium Research Laboratory Department of Crop Sciences, University of Sydney and Royal Botanic Gardens, Sydney, p 133
Coles RB, Talbot PHB (1977) Septobasidium clelandii and its conidial state Harpographium corynelioides. Kew Bull 31:481–488
Dao TH (2012) Ecology of red scale (Aonidiella aurantii (Maskell) [Hemiptera: Sternorrhyncha: Diaspididae]) in citrus orchards on the Central Coast of New South Wales. PhD thesis, University of Western Sydney
Dao TH, Meats AM, Beattie GAC, Spooner-Hart R (2013) Ant-coccid mutualism in citrus canopies and its effect on natural enemies of red scale, Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae). Bull Entomol Res 19:1–6. doi:10.1017/s0007485313000187
DeBach P, Hendrickson RM, Rose K (1978) Competitive displacement: extinction of the yellow scale, Aonidiella citrina (Coq.) (Homoptera: Diaspididae), by its ecological homologue, the California red scale, Aonidiella aurantii (Mask.) in Southern California. Hilgardia 46:1–35
Desmazières JBHJ (1848) Seizième notice sur les plantes cryptogames récemment découvertes en France. Ann Sci Nat Bot Biol Veg 10:342–361
Dingley JM (1951) The hypocreales of New Zealand. II. The genus Nectria. Trans Roy Soc NZ 79:177–202
Doyle JJ, Doyle JL (1990) A rapid total DNA preparation procedure for fresh plant tissue. Focus 12:13–15
Earle FS (1899) Orchard notes. Ala Agric Exp Station Bull 106:163–176
Ebeling W (1959) Subtropical fruit pests. Division of Agricultural Sciences, University of California, Los Angeles, p 436
Fawcett HS (1908) Fungi parasitic upon Aleyrodes citri. Masters thesis. The University of the State of Florida
Fisher FE (1950) Entomogenous fungi attacking scale insects and rust mites on citrus in Florida. J Econ Entomol 43:305–309
Fisher FE, Thompson WL, Griffiths JT (1949) Progress report on the fungus diseases of scale insects attacking citrus in Florida. Fla Entomol 32:1–10
Fisher NL, Burgess LW, Toussoun TA, Nelson PE (1982) Carnation leaves as a substrate and for preserving cultures of Fusarium species. Phytopathology 72:151–153
Fuller C (1901) First report of government entomologist 1899–1900. Department of Agriculture Natal, South Africa, p 99
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
Ghajar FGK (2004) Stimulatory and inhibitory effects of UVA and UVB radiation on some physiological and pathogenic characteristics of fungal biocontrol agents to enhance mycoherbistat effectiveness. PhD thesis. University of Western Sydney
Gracia-Garza JA, Fravel DR, Bailey BA, Hebbar PK (1997) Dispersal of formulations of Fusarium oxysporum f. sp. erythroxyli and F. oxysporum f. sp. melonis by ants. Biol Control 88:185–189
Gräfenhan T, Schroers H-J, Nirenberg HI, Seifert KA (2011) An overview of the taxonomy, phylogeny, and typification of nectriaceous fungi in Cosmospora, Acremonium, Fusarium, Stilbella, and Volutella. Stud Mycol 68:79–113. doi:10.3114/sim.2011.68.04
Hely PC, Pasfield G, Gellatley JG (1982) Insect pests of fruit and vegetable in NSW. Inkata Press, Melbourne
Jaklitsch WM, Voglmayr H (2011) Nectria eustromatica sp. nov., an exceptional species with a hypocreaceous stroma. Mycologia 103:209–218. doi:10.3852/10-178
Joffe AZ (1974) A modern system of Fusarium taxonomy. Mycopathol Mycol Appl 53:201–228
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Koebele A (1892) Expert’s trip to foreign countries. In: Report on the importation of parasites and predaceous insects by the State Board of Horticulture. AJ Johnston, Superintendent State Printing, Sacramento, California, USA. pp. 7–12. 1 pl
Koebele A (1893) Studies of parasitic and predaceous insects in New Zealand, Australia, and adjacent islands. United States Department of Agriculture. Government Printing Office, Washington, D.C, p 39
Kuno G, Ferrer MAC (1973) Pathogenicity of two Fusarium fungi to an armored scale insect, Selenaspidus articulatus. J Invertebr Pathol 22:473–474
Mabberley DJ (2004) Citrus (Rutaceae): a review of recent advances in etymology, systematics and medical applications. Blumea 49:481–498
Mauchline N, Hallett I, Hill G, Casonato S (2011) Process of infection of armored scale insects (Diaspididae) by an entomopathogenic Cosmospora sp. J Invertebr Pathol 108:46–51. doi:10.1016/j.jip.2011.07.002
McAlpine D (1896) The sooty mould of citrus trees: a study in polymorphism. Proc Linnean Soc NSW 21:469–499, pl. xxxiv
McAlpine D (1899) Fungus diseases of citrus trees in Australia and their treatment. Robt. S. Brain, Government Printer, Melbourne
McKenzie HL (1938) The genus Aonidiella (Homoptera; Coccoidae; Diaspididae). Microentomology 3:1–36
Meyling NV, Hajek AE (2010) Principles from community and metapopulation ecology: application to fungal entomopathogens. BioControl 55:39–54. doi:10.1007/s10526-009-9246-5
O’Donnell K, Humber RA, Geiser DM, Kang S, Park B, Robert VARG, Crous PW, Johnston PR, Aoki T, Rooney AR, Rehner AS (2012) Phylogenetic diversity of insecticolous fusaria inferred from multilocus DNA sequence data and their molecular identification via FUSARIUM-ID and Fusarium MLST. Mycologia 104:427–445. doi:10.3852/11-179
O’Donnell K (1993) Fusarium and its near relatives. In: Taylor JW, Reynolds DR (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233
Parkin J (1906) Fungi parasitic upon scale-insects (Coccidae and Aleurodidae): a general account with special reference to Ceylon forms. Ann R botanic Gard Peradeniya 3:11–82
Petch T (1921a) Fungi parasitic on scale insects. Trans Br Mycol Soc 7:18–40
Petch T (1921b) Studies in entomogenous fungi. I. The Nectriae parasitic on scale insects. Trans Br Mycol Soc 7:89–167
Rabenhorst L (1862) Cosmospora coccinea. Hedwigia 2:59
Reinking OA (1921) Citrus diseases of the Philippines, South China, Indo-China, and Siam. Philipp Agric 9:121–183
Rolfs PH (1897) A fungus disease of San José scale. Bull Florida Agric Exp Station 41:513–541, 1 plate
Rossman AY (1978) Podonectria, a genus in the Pleosporales on scale insects. Mycotaxon 7:163–182
Scott LA (1982) Citrus spray guide—coastal districts. Agfact H2.3.1, 1st edn. Department of Agriculture New South Wales, Sydney
Smith D, Beattie GAC, Broadley R (eds) (1997) Citrus pests and their natural enemies: integrated pest management in Australia. Queensland Department of Primary Industries, Brisbane
Summerville WAT (1934) Queensland citrus scale insects and their control. Queensland Department of Agriculture and Stock, Division of Entomology and Plant Pathology. Bulletin 10:101
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729
Thompson WL (1939) Cultural practices and their influence upon citrus pests. J Econ Entomol 32:782–789
Tryon H (1889) Report on insect and fungus pests. James C. Beal, Government Printer, Brisbane
Tryon H (1894) The disease affecting the orange orchards of wide Bay, and the insect pests prevalent therein. Edmund Gregory, Government Printer, Brisbane
Tulasne L-R, Tulasne C (1861–1865) Selecta Fungorum Carpologia, vol 3. Paris: Imperial Press
Tyson JL, Henderson RC, Fulertoon RA, Jamieson LE, Froud KJ (2005) Distribution and new host records for Cosmospora aurantiicola and Cosmospora flammea: entomopathogens of Disapididae in New Zealand. NZ Plant Prot 58:283–287
Voigt K, Cigelnik E, O’Donnell K (1999) Phlogeny and PCR identification of clinically important Zygomycetes based on nuclear ribosomal-DNA sequence data. J Clin Microbiol 37:3957–3964
Waterhouse DF, Sands DPA (2001) Classical biological control of arthropods in Australia. Australian Centre for International of Agricultural Research, Canberra
Watson IR, Berger EW (1932) Citrus Insects and their Control. Cooperative Extension Work in Agriculture and Home Economics Bulletin 67 (A revision of Florida Agricultural Experiment Station Bulletin 183). pp 135
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York
Zhang DX, Hartley TG, Mabberley DJ (2008) Rutaceae. In: Wu ZY, Raven PH, Hong DY (eds), Flora of China, Vol. 11 (Oxalidaceae through Aceraceae). Science Press, Beijing, Peoples Republic of China, Missouri Botanical Garden Press, St. Louis, Missouri, USA
Ziegler LW (1949) The possible truer status of the red-headed scale fungus. Fla Entomol 32:151–157
Acknowledgments
The study was undertaken as part of postgraduate studies funded by an AusAID scholarship awarded to Dao Thi Hang. We thank the owners of study orchards on the Central Coast of New South Wales: Ted and Sylvia Lister, and Ross and Maureen Hitchcock at Kulnura, Max and Kevin Britten at Somersby, Jeromy Wallis and Gerry Whitmont at Lower Portland, Bruce and Phillip Gardiner at Cornwallis, and Deidre Hartog at Castlereagh. Ms Sandra Hardy (formerly Industry Leader Citrus, New South Wales Department of Primary Industries) is thanked for her enthusiastic support and interest. Oleander scale cultures were established from scale-infested butternut pumpkins kindly supplied by Dan Papacek, Bugs for Bugs, Integrated Pest Management Pty Ltd, Mundubbera, QLD, Australia. Typhlodromips montdorensis was also kindly supplied by Dan Papacek.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Dao, H.T., Beattie, G.A.C., Rossman, A.Y. et al. Systematics and biology of two species of Microcera associated with armoured scales on citrus in Australia. Mycol Progress 14, 17 (2015). https://doi.org/10.1007/s11557-015-1044-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11557-015-1044-0