Marek Barta

Aphid-pathogenic Entomophthorales (their taxonomy, biology and ecology)

Fungi of the order Entomophthorales (Zygomycota, Zygomycetes) constitute a group of mostly insect pathogenic species, which attracts attention of insect pathologists because of their high capacity for use in biological control of pest insects. This work primarily focuses on entomophthoralean species attacking aphids. The Entomophthorales are considered major pathogens of aphids in nature. In fact, the fungi are the only pathogens that regularly and effectively can affect aphid populations in natural ecosystems as well as in agroecosystems. Up to now, 33 entomophthoralean species organized into 9 genera have been recorded in aphid hosts. All fungal species are listed and organised by genus in the work. Descriptions are presented for all the fungal genera and species, including a nomenclature genesis, a geographical distribution, a host specificity/host range, a capability of cultivation in vitro, and possible prospects for their use in biological control strategies. A key to identification of the pathogens is provided as well. A general life cycle outline of the pathogens is followed by fundamental facts on biology and ecology of the fungi and analysis of primary factors that are involved in the study of epizootiology of infectious diseases in insect populations. The abiotic and biotic elements of the environment, which interfere in the pathogen-host interactions, are also underlined. In the last chapter, several examples are reviewed when the Entomophthorales were used against aphids within the four strategies of biological control, namely classical biological control, inoculation biological control, inundation biological control, and conservation biological control. The aim of this review is to cover the present status of knowledge about the natural enemies of aphids and to stimulate an interest of insect pathologists in this group of entomopathogenic fungi.

Entomophthoralean fungi associated with the common nettle aphid (Microlophium carnosum Buckton) and the potential role of nettle patches as reservoirs for the pathogens in landscape

Populations of the common nettle aphid, Microlophium carnosum Buckton, inhabiting nettle patches in an agricultural landscape were surveyed for entomophthoralean infection during 1998, 1999 and 2001. Five pathogenic species were identified from the aphid in the course of the survey. Erynia neoaphidis Remaudière & Hennebert, Neozygites fresenii (Nowakowski) Remaudière & Keller, and Neozygites microlophii Keller affected aphid colonies every year. Two minor pathogens, Entomophthora planchoniana Cornu and Conidiobolus obscurus (Hall & Dunn) Remaudière & Keller, were observed only in 2001.An artificial transmission of the three main fungi was carried out to prove horizontal transmission of infection between the common nettle aphid and different aphid species co-occurring in landscape. N. microlophii, probably monophagous pathogen, did not infect any of the six recipient aphid species in the experiment. Transmissions of E. neoaphidis and N. fresenii conidia were successful with five and four aphid species, respectively. The average mortality of tested aphids after transmission ranged from 0 to 33.33 % for E. neoaphidis and from 0 to 15 % for N. fresenii.The potential of nettle patches as natural reservoirs for pathogens in the agroecosystem is discussed.

Effects of combining Beauveria bassiana and Nosema pyrausta on the mortality of Ostrinia nubilalis.

We tested the combined effect of the fungus Beauveria bassiana and the microsporidium Nosema pyrausta on the European corn borer larvae, Ostrinia nubilalis, in the laboratory. The first instar of O. nubilalis larvae was the most sensitive to the B. bassiana infection followed by the fifth, second, third, and fourth instar (LC50s were 4.91, 6.67, 7.13, 9.15, and 6.51 × 105 conidia/ml for the first to fifth instars, respectively). Mortality of each instar increases positively with concentration of conidia. When B. bassiana and N. pyrausta were used in combination, mortality increased significantly in all instars. Relative to the B. bassiana treatment alone, the B. bassiana + N. pyrausta treatment decreased the LC50s by 42.16%, 37.63%, 21.60%, 27.11%, and 33.95% for the first to fifth instars, respectively. The combined effects of the two pathogens were mostly additive. However, at the two highest concentrations the pathogens interacted synergistically in the first and second instar. Individuals that survived the B. bassiana and B. bassiana + N. pyrausta treatments and developed into adults had significantly shorter lifespans and females oviposited fewer eggs than non-exposed insects. The effects on the longevity and the egg production were most pronounced at high concentration of B. bassiana conidia.

The potential for Entomophaga maimaiga to regulate gypsy moth Lymantria dispar (L.) (Lepidoptera: Erebidae) in Europe

Gypsy moth, Lymantria dispar L., is one of the most important pests of deciduous trees in Europe. In regular cycles, it causes large‐scale defoliation mostly of oak, Quercus spp., forests. Government authorities in the most infested countries in Europe conduct large‐scale applications of pesticides against gypsy moth. In 1999, a new natural enemy, the entomopathogenic fungus Entomophaga maimaiga, was successfully introduced into a gypsy moth population in Bulgaria. Recent investigations suggest that now E. maimaiga is quickly spreading in Europe. Herein, past studies are reviewed regarding this fungus with special emphasis on its potential for becoming an important factor regulating gypsy moth populations in Europe, focusing on the hosts population dynamics in relation to the fungus, the influence of environmental conditions on fungal activity, the influence of E. maimaiga on the native entomofauna, including other gypsy moth natural enemies, and spread of the fungus. Based on this analysis, the potential of E. maimaiga for providing control in European gypsy moth populations is estimated.

First record of Entomophaga maimaiga (Entomophthorales: Entomophthoraceae) in Slovakia

The entomopathogenic fungus Entomophaga maimaiga was found for the first time in Slovakia in 2013. Late instar larvae of gypsy moth, Lymantria dispar, from two sites with different population densities were dissected to evaluate the presence of pathogens. The presence of conidia and resting spores of E. maimaiga in gypsy moth cadavers was confirmed from both sites.

Neozygites osornensis sp. nov., a fungal species causing mortality to the cypress aphid Cinara cupressi in Chile

An entomophthoralean fungus causing epizootics in populations of the cypress aphid, Cinara cupressi Buckton, in Chile is described as a new species, Neozygites osornensis Montalva et Barta. The aphid pathogen is described based on morphological characters. An exhaustive description, illustrations and a comparison with closely related species are provided. The fungus differs from similar Neozygites species by smaller hyphal bodies, nuclei, primary conidia, capilliconidia and capilliphores and by noticeably different shape of capilliconidia. A key to aphid-pathogenic species of Neozygites is also included.

Natural control of Diuraphis noxia and Rhopalosiphum maidis (Aphidoidea) by parasitic entomophthorales (Zygomycota) in Slovakia.

Seasonal development of entomophthoralean infection in colonies of Diuraphis noxia and Rhopalosiphum maidis was evaluated on summer barley under conditions of south-western Slovakia in 2001 and 2002. D. noxia was infesting summer barley during both years, while R. maidis was only recorded in 2002. Further three cereal aphids, Rhopalosiphum padi, Metopolophium dirhodum and Sitobion avenae, were also observed on summer barley. Complex of entomophthoralean fungi identified in cereal aphid colonies included four species, Pandora neoaphidis, Entomophthora planchoniana, Conidiobolus obscurus and Neozygites fresenii, with P. neoaphidis as the most prevalent fungus during both years. Two parasitic fungi, P. neoaphidis and E. planchoniana, were identified from D. noxia, but P. neoaphidis was predominant. Infection rate in D. noxia colonies was low, not exceeding 15% and 10% in 2001 and 2002, respectively. Only nine R. maidis individuals were killed with entomophthoralean fungi. The fungi were identified as P. neoaphidis and C. obscurus. No epizootics were observed in the aphid colonies. The fungi could not control development of the aphid populations since they did not appear until high host densities had been established in the crops.

Phytophagous larvae occurring in Central and Southeastern European oak forests as a potential host of Entomophaga maimaiga (Entomophthorales: Entomophthoraceae) – A field study

We evaluated the presence and impact of Entomophaga maimaiga on both target and non-target phytophagous larvae. All six study plots, with low gypsy moth population density, were situated in Central and Southeastern European oak forests and E. maimaiga had previously been reported from these plots. Totally, 45 of 4,045 (1.13%) collected non-target larvae died due to fungal infections. No non-target insect specimen was infected by E.maimaiga, although the presence of the pathogen could not be fully excluded in three cadavers. Out of 1,780L.dispar larvae collected, 15individuals (0.84%) were infected by E.maimaiga.

The Factors Influencing Seasonal Dynamics and Spatial Distribution of Stable Fly Stomoxys calcitrans (Diptera, Muscidae) within Stables

The biology of the stable fly is fairly well known, but factors influencing the distribution of adult stable flies within stables are still inadequately investigated. The four experimental stables were located in south western Slovakia. Within each stable, five sticky traps were localized along the stable, and the flies were weekly counted during the flight season of years 2015–2017. Seasonal activity and stable fly abundance in relation to temperature, rainfall, light conditions, relative air humidity, and cows per stable were evaluated. The seasonal activity of the stable fly shows one large peak at the end of summer and a second smaller peak just before the end of the flight season. The spatial distribution of stable flies was unique for each stable. All of the environmental variables had significant and mostly positive effect on stable fly abundance. The strongest and most positive effect on stable fly counts was temperature and rainfall five weeks prior to collecting session. Within the stable, cow number, air humidity, and light conditions are the strongest candidates to influence their distribution.

Hypocrealean fungi associated with populations of Ips typographus in West Carpathians and selection of local Beauveria strains for effective bark beetle control

In Slovakia, a diversity of entomopathogenic fungi (Ascomycota, Hypocreales) associated with outbreaks of Ips typographus was studied in 81 localities and as many as 113 in vitro cultures of five entomopathogenic species were isolated from infected individuals: Beauveria bassiana (87 isolates), B. pseudobassiana (14 isolates), B. caledonica (6 isolates), Lecanicillium lecanii (4 isolates) and Isaria farinosa (2 isolates). B. pseudobassiana is recorded in natural populations of I. typographus for the first time. Biological properties of selected Beauveria isolates, including colony growth, biomass production, conidia yield and pathogenicity to I. typographus adults, were studied in a series of laboratory bioassays and much intra- and interspecific variability was detected. B. bassiana isolates produced biomass or conidia at significantly higher rate than B. pseudobassiana and B. caledonica isolates. Two B. bassiana isolates were selected as the most virulent to bark beetle adults, demonstrating a mean LC50 ranging from 0.72 to 2.05 × 106 conidia ml−1, and were qualified as promising candidates for biocontrol of I. typographus. Their virulence was significantly higher than that of the mycoinsecticides Boverol®, which was used as a reference strain in the virulence bioassays.