In temperate regions, insect pathogenic fungi face the challenge of surviving through the winter. Winter is a time when hosts are immobile, low in number or are present in a stage which is not susceptible to infection. Fungi from Entomophthoromycota have so far been known to survive the winter in two ways: either as (1) thick-walled resting spores released into environment from dead hosts, or as (2) structures inside the dead host (e.g.,？hyphal bodies). Here we report, from the Danish environment, a third way to survive the winter, namely a slow progression and transmission of Entomophthora schizophorae in adult dipteran Pollenia hosts that hibernate in clusters in unheated attics, sheltered areas outdoors (under bark etc.). Fungus-killed sporulating flies were observed outside very early and very late in the season. By sampling adults at the time of their emergence from hibernation in late winter/early spring we documented that the fungus was naturally prevalent and killed flies after a period of incubation. Experimentally we documented that even at the low temperature of 5 °C, the fungus was able to maintain itself in Pollenia cohorts for up to 90 days. From these observations the full winter cycle of this fungus is？elucidated. The three types of winter survival are discussed in relation to fungus epidemic？development.
References
[1]
Eilenberg, J.; Michelsen, V. Natural host range and prevalence of the genus Strongwellsea (Zygomycota : Entomophthorales) in Denmark. J. Invertebr. Pathol. 1999, 73, 189–198, doi:10.1006/jipa.1998.4795.
[2]
Keller, S. The genus Entomophthora (Zygomycetes, Entomophthorales) with a description of five new species. Sydowia 2002, 54, 157–197.
[3]
Humber, R.A. Identification of entomopathogenic fungi. In Manual of Techniques in Invertebrate Pathology, 2nd ed.; Lacey, L.L., Ed.; Academic Press: Amsterdam, The Netherlands, 2012; pp. 151–187.
[4]
Hajek, A.E.; Tatman, K.M.; Wanner, P.H.; Wheeler, M.M. Location and persistence of cadavers of gypsy moth, Lymantria dispar, containing Entomophaga maimaiga azygospores. Mycologia 1998, 90, 754–760, doi:10.2307/3761315.
[5]
Humber, R.A. Systematics of genus Strongwellsea (Zygomycetes-Entomophthorales). Mycologia 1976, 68, 1042–1060, doi:10.2307/3758721.
[6]
Keller, S. Observations on the overwintering of Entomophthora planchoniana. J. Invertebr. Pathol. 1987, 50, 333–335, doi:10.1016/0022-2011(87)90103-0.
[7]
Klingen, I.; Waersted, G.; Westrum, K. Overwintering and prevalence of Neozygites floridana (Zygomycetes: Neozygitaceae) in hibernating females of Tetranychus urticae (Acari: Tetranychidae) under cold climatic conditions in strawberries. Exp. Appl. Acarol. 2008, 46, 231–245, doi:10.1007/s10493-008-9178-2.
[8]
Balazy, S. Entomophthorales; Polish Academy of Sciences: Krakow, Poland, 1993; Volume 24.
[9]
Keller, S.; Kalsbeek, V.; Eilenberg, J. Redescription of Entomophthora muscae (Cohn) Fresenius. Sydowia 1999, 51, 197–209.
[10]
Kramer, J.P. The housefly mycosis caused by Entomophthora muscae—Influence of relative-humidity on infectivity and conidial germination. J. New York Entomol. Soc. 1980, 88, 236–240.
[11]
Mullens, B.A.; Rodriguez, J.L.; Meyer, J.A. An epizootiological study of Entomophthora muscae in muscoid fly populations on southern-California poultry facilities, with emphasis on Musca domestica. Hilgardia 1987, 55, 1–41.
[12]
Thomsen, L.; Jensen, A.B. Application of nested-PCR technique to resting spores from the Entomophthora muscae species complex: Implications for analyses of host-pathogen population interactions. Mycologia 2002, 94, 794–802, doi:10.2307/3761694.
[13]
Thomsen, L.; Bresciani, J.; Eilenberg, J. Formation and germination of resting spores from different strains from the Entomophthora muscae complex produced in Musca domestica. Can. J. Bot. 2001, 79, 1076–1082.
[14]
Six, D.L.; Mullens, B.A. Seasonal prevalence of Entomophthora muscae and introduction of Entomophthora schizophorae (Zygomycotina: Entomophthorales) in Musca domestica (Diptera: Muscidae) populations on California dairies. Biol. Contr. 1996, 6, 315–323, doi:10.1006/bcon.1996.0040.
[15]
Kalsbeek, V.; Mullens, B.A.; Jespersen, J.B. Field studies of Entomophthora (Zygomycetes : Entomophthorales) - induced behavioral fever in Musca domestica (Diptera : Muscidae) in Denmark. Biol. Contr. 2001, 21, 264–273, doi:10.1006/bcon.2001.0943.
[16]
Eilenberg, J.; Philipsen, H. The Occurrence of Entomophthorales on the Carrot Fly [Psila rosae F] in the Field during 2 Successive Seasons. Entomophaga 1988, 33, 135–144, doi:10.1007/BF02372648.
[17]
Eilenberg, J. The culture of Entomophthora muscae (C) Fres. in carrot flies (Psila rosae F.) and the effect of temperature on the pathology of the fungus. Entomophaga 1987, 32, 425–435, doi:10.1007/BF02372452.
[18]
Jewiss-Gaines, A.; Marshall, S.A.; Whitworth, T.L. Cluster flies (Calliphoridae: Polleniinae: Pollenia) of North America. Can. J. Arthropod. Identif. 2012, 19, doi:10.3752/clai.2012.3719.
[19]
Goulson, D.; Hughes, W.O.H.; Chapman, J.W. Fly populations associated with landfill and composting sites used for household refuse disposal. Bull. Entomol. Res. 1999, 89, 493–498.
[20]
Rognes, K. Blowflies (Diptera, Calliphoridae) of Fennoscandinavia and Denmark; Scandinavian Science Press Ltd.: Leiden, The Netherlands, 1991; Volume 24.
Jensen, A.B.; Thomsen, L.; Eilenberg, J. Value of host range, morphological, and genetic characteristics within the Entomophthora muscae species complex. Mycol. Res. 2006, 110, 941–950, doi:10.1016/j.mycres.2006.06.003.
[23]
Eilenberg, J.; Bresciani, J.; Latge, J.P. Ultrastructural Studies of Primary Spore Formation and Discharge in the Genus Entomophthora. J. Invertebr. Pathol. 1986, 48, 318–324, doi:10.1016/0022-2011(86)90060-1.
[24]
Hajek, A.E.; Bauer, L.; McManus, M.L.; Wheeler, M.M. Distribution of resting spores of the Lymantria dispar pathogen Entomophaga maimaiga in soil and on bark. Biocontrol 1998, 43, 189–200, doi:10.1023/A:1009933525540.
[25]
Thomsen, L.; Eilenberg, J. Entomophthora muscae resting spore formation in vivo in the host Delia radicum. J. Invertebr. Pathol. 2000, 76, 127–130, doi:10.1006/jipa.2000.4961.
[26]
Lihme, M.; Jensen, A.B.; Rosendahl, S. Local scale population genetic structure of Entomophthora muscae epidemics. Fungal Ecol. 2009, 2, 81–86, doi:10.1016/j.funeco.2009.01.004.
[27]
Hajek, A.E.; Humber, R.A. Formation and germination of Entomophaga maimaiga azygospores. Can. J. Bot. 1997, 75, 1739–1747, doi:10.1139/b97-888.
[28]
Nielsen, C.; Hajek, A.E.; Humber, R.A.; Bresciani, J.; Eilenberg, J. Soil as an environment for winter survival of aphid-pathogenic Entomophthorales. Biol. Contr. 2003, 28, 92–100, doi:10.1016/S1049-9644(03)00033-1.
[29]
Eilenberg, J.; Bresciani, J; Latgé, J.P. Primary spore and resting spore formation in vitro of Entomophthora schizophorae and E. muscae, both members of the E. muscae-complex (Zygomycetes). Cryptogamic Botany 1990, 1, 365–371.
[30]
Scorsetti, A.C.; Jensen, A.B.; Lastra, C.L.; Humber, R.A. First report of Pandora neoaphidis resting spore formation in vivo in aphid hosts. Fungal Biol. 2012, 116, 196–203, doi:10.1016/j.funbio.2011.11.002.
