© The Author(s) 2014 Published by Polish Botanical Society Grazing preference of Ceratophysella sp. 1 (Collembola) for Pseudoperonospora cubensis – fungal pathogen of Cucumis sativus A. CHLEBICKI1 and J.M. RADWAŃSKI2 1Department of Mycology, W. Szafer Institute of Botany, Polish Academy of Sciences Lubicz 46, PL-31-512 Kraków, a.chlebicki@botany.pl 2Institute of Systematics and Evolution of Animals, Polish Academy of Science Sławkowska 17, PL-31-016 Kraków, jmr1@o2.pl Chlebicki A., Radwański J.M.: Grazing preference of Ceratophysella sp. 1 (Collembola) for Pseudoperonospora cubensis – fungal pathogen of Cucumis sativus. Acta Mycol. 49 (1): 93–97, 2014. Grazing preferences of collembolans Ceratophysella sp. 1 were noted. The collembolans feed on the sporangia of Pseudoperonospora cubensis growing on plants Cucumis sativus in greenhouses in Esfahan province in Iran. Sporangia of Pseudoperonospora cubensis were the preferred food of all fungal species noted in the alimental tract of the springtails. All digestive tracts of the springtails contained sporangia of P. cubensis. Key words: cucurbit downy mildew, Pseudoperonospora cubensis, springtails, feeding preferences INTRODUCTION There are many interactions between insects, fungi and plants, i.e. Botanophila, Ep- ichloë and Dactylis/Puccinellia (Górzyńska et al. 2010, 2011) or Phalacrus, Anthra- coidea and Carex (Steiner 1984; Chlebicki 2007, 2011). Many microarthropods are mycophagous. Some species of collembolans feed on the mycelium of pathogenic fungi (Sabatini, Innocenti, 2000, Lootsma, Scholte, 1997). Also grazing preferences of collembolans for endomycorrhizal fungi are well known (Timm, Larink 1995). There is single article devoted collembolan species Sinella curviseta which feeding of mycelium of Fusarium oxysporum f. sp. cucumerinum parasitizing cucumber seed- lings (Nakamura et al. 1992). We found the next collembolan species feeding on plant pathogen Pseudoperonospora cubensis (Berk. & M.A. Curtis) Rostovzev grow- ing on leaves of Cucumis sativus. The collected springtails belong to the unknown species of the genus Ceratophysella from C. denticulata group that might be a new species to the world (Nematollahi et al. 2009). ACTA MYCOLOGICA Vol. 49 (1): 93–97 2014 DOI: 10.5586/am.2014.009 Dedicated to Professor Maria Ławrynowicz on the occasion of the 45th anniversary of her scientific activity 94 A. Chlebicki and J.M. Radwański © The Author(s) 2014 Published by Polish Botanical Society MATERIAL AND METHODS Collembolans were found feeding on cucumber seedlings in greenhouses in Esfa- han province during 2005-2006. Juvenile individuals was preserved on 96% ethanol. Then, they were prepared as fallow: 18 hours in lactophenol (lactic acid 100 ml, glyc- erol 200 ml, distilled water 100 ml, phenol 100 g), 10-40 minutes in 10% KOH, few seconds of heating in lactophenol. At the end of the specimen was closed on a slide in the medium Marc André II (distilled water 50 ml, chloral hydrate 200 gram, glyc- erol 30 gram, gum arabic 20 gram). 70 specimens of collembolans were checked up for fungal sporangia. 30 sporangia of P. cubensis were measured. The morphological characters of the fungi and collembolan body were examined using light microscopy (Nikon SMZ 1500, Nikon Eclipse 80i). Microphotographs were taken with these mi- croscopes equipped with a digital camera Nikon DS R1. Morphological terminology of the mildew was used after Savory et al. (2011). RESULTS AND DISCUSSION Pseudoperonospora cubensis (Berk. & M.A. Curtis) Rostovzev, Annals Inst. Agron. Moscow 9: 47, 1903. Sporangia elliptical, lemon-shaped, grey-purple 22-27(33) x 17-25 µm. Sporan- giophores slender, branches in the dichotomous manner, branches and tips straight, tips gradually tapering to a point (Fig. 1A). All digestive tracts of the springtails contain sporangia of P. cubensis (Fig. 2). Moreover spores of other species were found. Only three dark spores of Acremo- nium group (Gliomastix, Pseudogliomastix) together with spores of P. cubensis were found (Fig. 1B). The spores (Fig. 1B) were similar to these of plate 52 A (Seifert et al. 2011). In the same figure a single ornamented spore is presented. In the next picture (Fig. 1C) are showed pollen grains of unidentified plant. Some hyphae of dematiaceous fungus are illustrated in the Figure 1D. The cucurbit downy mildew (Pseudoperonospora cubensis) is currently the most destructive disease of cucumber which have been responsible for annual yield losses of up to 80% (Lebeda, Urban 2007; Savory et al. 2011). It has wide host range and occurs approximately on 20 different genera of Cucurbitaceae (Lebeda, Urban 2007). Sporangia of Pseudoperonospora cubensis became the preferred food of all fungal spe- cies noted in the alimental tract of the springtails. Sporangia lying in alimentary tract of collembolans are mostly disfigured. It suggest that Ceratophysella sp. 1 not disperse sporangia of the fungus via gut passage. Nematollahi et al. (2009) suggest that in the infested plants secondary roots were devoured completely by collembolans and the plants could be easily infected by pathogens. But our observations indicate that col- lembolans reduced number of fungal sporangia. However, the fungal sporangia can be transported by the springtails on their body and this way contributing to the spread of the disease. Amount of sporangia transported on springtail bodies is distinctly smaller than its amount in alimental tract. On the basis of our investigation it is difficult to precise determination of influence of the collembolan species on cucumber cultiva- tion in greenhouse. Ceratophysella sp. 1 is probably a rare species with occurrence Grazing preference of Ceratophysella for Pseudoperonospora cubensis 95 © The Author(s) 2014 Published by Polish Botanical Society Fig. 1. A – Sporangia and sporangiospores of Pseudoperonospora cubensis, B – 3 dark spores of Acremonium group fungus and single hyaline, ornamented spore, C – plant grains, D –dematiaceous hyphae. Fig. 2. Springtail Ceratophysella sp. 1 juv. with spores in the alimental track. 96 A. Chlebicki and J.M. Radwański © The Author(s) 2014 Published by Polish Botanical Society restricted to the Near East. Other species of the C. denticulata group have similar food preference (Babenko et al. 1994). Next investigation are necessary for recognition of influence of Ceratophysella sp. 1 on pathogenic fungi of greenhouse plants. It is possible that these collembolans can be used for protection against patho- genic fungi (biological control agent – BCA) as in the case of Proisotoma minuta (Isotomidae) used for suppression of Rhizoctonia solani on cotton in a greenhouse environment (Lartey et al. 1994, 2008). Acknowledgements. We thank Dr. Marcin Piątek for suggestions and two reviewers for comments. Finan- cial support was provided by the W. Szafer Institute of Botany of the Polish Academy of Sciences through its statutory fund. REFERENCES Babenko A.B., Chernova N.M., Potapov M.B., Stebaeva S.K. 1994. Opredelitel kollembol fauny Rossii i soprezhelnykh stran: Semeistvo Hypogastruridae. Moskva, Nauka. Chlebicki A. 2007. Notes on the distribution and ecology of fungi of the genus Anthracoidea (Ustilagino- mycetes) in Poland. Polish Bot. J. 52 (2): 151-158. Chlebicki A. 2011. Anthropogenic origin of the smut fungus Anthracoidea caricis population in the Gorce Mts (Poland). Polish Bot. J. 56 (2): 333-337. Górzyńska K., Lembicz M., Olszanowski Z., Leuchtmann A. 2010. An unusual Botanophila-Epichloë as- sociation in a population of orchardgrass (Dactylis glomerata) in Poland. Journal of Natural History 44: 2817-2824. Górzyńska K., Lembicz M., Olszanowski Z., Leuchtmann A. 2011. Botanophila-Epichloë interaction in a wild grass, Puccinellia distans lacks dependence on the fly vector. Annals of the Entomological Society of America 104 (4): 841-846. Lartey R.T., Curl E.A., Peterson C.M. 1994. Interactions of mycophagous collembolan and biological control fungi in the suppression of Rhizoctonia solani. Soil Biology and Biochemistry 26(1):81-88. http://dx.doi.org/10.1016%2F0038-0717%2894%2990198-8 Lartey R.T., Curl E.A., Peterson C.M., Williams J.L. 2008. Control of Rhizoctonia solani and Cotton Seed- ling Disease by Laetisaria nivalis and mycophagous insect Proisotoma minuta (Collembola). Journal of Phytopatology 133 (2): 89-98. Lebeda A., Urban J. 2007. Temporal changes in pathogenicity and fungicide resistance in Pseudoperono- spora cubensis populations. Acta Horticulturae 731: 327-336. Lootsma M., Scholte K. 1997. Effect of soil moisture content on the suppression of Rhizoctonia stem canker on potato by the nematode Aphelenchus avenae and the springtail Folsomia fimetaria. Plant Pathology 46 (2): 209-215. http://dx.doi.org/10.1046%2Fj.1365-3059.1997.d01-229.x Nakamura Y., Matsuzaki I., Itakura J. 1992. Effect of grazing by Sinella curviseta (Collembola) on Fusari- um oxysporum f. sp. cucumerinum causing cucumber disease. Pedobiologia 36 (3): 168-171. Nematollahi M., Bagheri M., Radwanski J.M. 2009. New reports of Collembola for Iran with surveying of the importance in the greenhouses of Esfahan province, Iran. Plant Protection Journal 1 (3): 327-335. Sabatini M.A., Innocenti G. 2000. Soil-borne plant pathogenic fungi in relation to some collembolan species under laboratory conditions. Mycological Research 104 (10): 1197-1201. http://dx.doi. org/10.1017%2FS0953756200003026 Savory E.A., Granke L.L., Quesada-Ocampo L.M., Varbanova M., Hausbeck M.K., Day B. 2011. The cucurbit downy mildew pathogen Pseudoperonospora cubensis. Molecular Plant Pathology 12 (3): 217-226. http://dx.doi.org/10.1111%2Fj.1364-3703.2010.00670.x Seifert K. Morgan-Jones G., Gams W., Kendrick B. 2011. The genera of Hyphomycetes. CBS-KNAW Fungal Biodiversity Centre, Utrecht. Steiner W.E. 1984. A review of the biology of phalacrid beetles (Coleoptera). (In): Q. Wheeler and Black- well M. (eds). Fungus-insect relationships. New York: Columbia University Press: 424-445. Timm T., Larink O. 1995. Grazing preferences of some collembolan for endomycorrhizal fungi. Biology and Fertility of Soils 19: 266-268. http://dx.doi.org/10.1007%2FBF00336171 Grazing preference of Ceratophysella for Pseudoperonospora cubensis 97 © The Author(s) 2014 Published by Polish Botanical Society Preferencje pokarmowe skoczogonka z rodzaju Ceratophysella do grzyba Pseudoperonospora cubensis – grzybowego patogena ogórków Cucumis sativus Streszczenie Preferencje pokarmowe skoczogonków z rodzaju Ceratophysella sp. 1 (nowy gatunek do opi- sania) zostały przedstawione. Skoczogonki spożywały sporangia grzyba Pseudoperonospora cubensis, który zaatakował rośliny Cucumis sativus rosnące w szklarni w prowincji Esfahan w Iranie. Sporangia grzyba Pseudoperonospora cubensis były notowane w układzie pokarmowym wszystkich badanych skoczogonków. 2014-06-30T22:45:21+0200 Polish Botanical Society