Next Article in Journal
Chinese Urban Carbon Emission Correlation Network: Construction, Structural Characteristics, and Driving Factors
Previous Article in Journal
How Does Participation in AI Standardisation Affect the Sustainable Development of Strategic Emerging Enterprises Under the Background of Uncertainty? Evidence from China
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Comparative Analysis of the Occurrence of Entomopathogenic Fungi in Soils from Flower Strips and Lawns in Urban Space

by
Cezary Tkaczuk
*,
Anna Majchrowska-Safaryan
and
Maciej Dadak
Faculty of Agricultural Sciences, Institute of Agriculture and Horticulture, University of Siedlce, 08-110 Siedlce, Poland
*
Author to whom correspondence should be addressed.
Sustainability 2025, 17(17), 7819; https://doi.org/10.3390/su17177819 (registering DOI)
Submission received: 16 July 2025 / Revised: 26 August 2025 / Accepted: 28 August 2025 / Published: 30 August 2025

Abstract

The changing structure of modern cities intensifies anthropopressure, resulting in the need to create plans for the protection of biodiversity in cities. This can be achieved by establishing lawns and flower strips along the streets and maintaining parks and squares in cities, creating green infrastructure and contributing to sustainable urban development. However, this vegetation also requires protection that is safe for the environment and city residents. Entomopathogenic fungi (EPF) are among the most well-known and effective microorganisms that infect plant pests and conduct the disease process leading to their death. The aim of the study was to conduct a comparative analysis of the generic composition of EPF and determine the density of their colony-forming units (CFUs) in soils from flower strips and lawns located along the main communication routes of the city of Siedlce (Poland). Soil samples collected from two sites and two habitats (a flower strip and a lawn directly adjacent to it)—Site No. 1, Wyszyńskiego Street; Site No. 2, Jagiełły Street—in the spring and autumn of 2021/2022 and 2024. At each site within the habitat, three zones (repeats) were designated, spaced approximately 10–15 m apart. Approximately six samples were collected from each replication, and then a mixed sample was prepared. Four genera of EPF were found in the soil samples: Beauveria, Metarhizium, Cordyceps, and Akanthomyces. The location, habitat type, and season had a significant effect on the diversity of individual genera of fungi and the density of colony-forming units (CFUs) in the studied soils. The dominant types of EPF, forming the most CFUs in the soils from the studied flower strips and the adjacent lawns, were Metarhizium spp. and Beauveria spp. It was found that EPF occurred in higher densities in the soil from the studied habitats (flower strips and lawns) in autumn than in spring. Both of these semi-natural habitats constitute forms of urban greenery that increase biodiversity and provide valuable ecosystem services that support sustainable urban development.

1. Introduction

The extensive structure of modern cities, increasing anthropopressure, and the reclamation of degraded areas have given rise to the need to create plans for the protection of biodiversity in cities. One example of preserving biodiversity is the establishment of lawns and flower strips along the streets and the maintenance of parks and squares in cities, creating green infrastructure (GI) [1,2,3]. This occurs in both urban and rural areas and consists of multiple or single fragments of the natural environment [4,5,6]. Szulczewska [7], analyzing various ways of defining urban greenery, emphasized the principle of the hierarchical shaping of ecological networks and the differentiation of elements constituting GI depending on the scale, ranging from continental, through regional and local, to the scale of the place. The core of GI on an urban scale is constituted by greenery systems (primarily municipal parks and forests, as well as ecological and protected areas), but meadows and flower strips are also important as, unlike lawns, they ensure a significant increase in biodiversity. Maintaining the above forms of urban greenery promotes the diversification of native flora and fauna species, vertebrates, and invertebrates, as well as the occurrence of various groups of microorganisms, including EPF, which are natural enemies of insect pests. These bigger, large-scale areas, such as parks and gardens, are characterized by high biodiversity, providing habitats for numerous plant and animal species. They offer a wide range of ecosystem services, such as air and water purification, climate regulation, recreation, and leisure. Smaller area, such as flower strips, green roofs, and green stops, are an effective way to green cities, increase biodiversity, and improve aesthetics, and can also contribute to reducing the urban heat island effect, improving air quality, and retaining rainwater [1,4,6].
The genera composition and the number of infectious units of EPF in the soil are influenced by various factors, such as soil type and related habitat; presence of heavy metals in soils; applied agricultural technology; the amount of fertilizers and plant protection products; as well as plant species composition [8]. Entomopathogenic fungi are among the most well-known and effective microorganisms that infect plant pests and conduct the disease process leading to their death of [9,10,11,12]. Under temperate climate conditions, the most frequently isolated EPF that effectively limit the pest population are fungi of the genera Beauveria, Metarhizium, and Cordyceps [9,13]. Entomopathogenic fungi can also enter into synergistic interactions with some beneficial arthropods (predators, parasitoids, pollinators), which is of particular importance in urban spaces [14,15], as well as with other entomopathogens (bacteria and nematodes) [16] and synthetic insecticides [17,18], which can be used in Integrated Plant Protection Programs [19]. Cuthbertson and Audsley [20] report that EPFs are important biological control agents in many natural and anthropogenically modified ecosystems.
The aim of this study was to conduct a comparative analysis of the generic composition of EPF and to determine their infectious potential in soils from flower strips and lawns located along the main communication routes of the city of Siedlce, Eastern Poland.

2. Materials and Methods

2.1. Research Location

The research material consisted of soil samples collected in 2021/2022 and 2024 from two sites and two habitats (a flower strip and a lawn directly adjacent to it) located near the road in the city of Siedlce, Eastern Poland. Site No. 1, (coordinates 52°10′01″ N, 22°17′21″ E, Wyszyńskiego Street) included a flower strip 250 m long and 6 m wide and an adjacent perennial lawn approximately 35 m wide, on which trees also grew, mainly linden trees and maples. Site No. 2 (coordinates 52°10′38″ N, 22°16′40″ E, Jagiełły Street) included a flower strip approximately 260 m long and 4 m wide, located between two lanes of Jagiełły Street, and a 1000 m long and 25 m wide lawn directly adjacent to the street, with linden and maple trees. The species composition of plants sown in the flower strips includes Plantago lanceolata L., Melandrium album L., Melandrium rubrum L., Betonica officinalis L., Centaurea scabiosa L., Centaurea jacea L., Coronilla varia L., Prunella vulgaris L., Silene floscuculi L., Prunella vulgaris, Dianthus carthusianorum, Ranunculus acris L., Carum carvi L., Lotus corniculatus L., Tragopogon pratensis L., Lythrum salicaria L., Achillea millefolium L., Sanguisorba minor L., Origanum vulgare L., Silene vulgaris (Salisb.) Sm., Medicago lupulina L., Daucus carota L., Saponaria officinalis L., Crepis biennis L., Anthyllis vulneraria L., Galium album Mill., Galium verum L., Anthemis tinctoria L., Agrimonia eupatoria L., Salvia pratensis L., Rhinanthus minor, Malva sylvestris L., Malva moschata L., Knautia arvensis L. Coult, Vicia cracca L., Leucanthemum vulgare L., Echium vulgare L., Trifolium repens L., Trifolium pratense L., Vicia sativa L., and Melilotus albus.

2.2. Soil Analysis

Samples for testing at Site No. 1 were collected in autumn 2021, spring 2022, and spring and autumn 2024. At Site No. 2, samples were collected in spring and autumn of 2024. In the tested soils, pH in 1 mol KCl was determined using the potentiometric method, with the following results. Site No. 1: spring—flower strip, 5.63; lawn, 4.22; autumn—flower strip, 5.40; lawn, 4.30; Site No. 2: spring—flower strip, 5.32; lawn, 4.67; autumn—flower strip, 5.55; lawn, 4.50. Soil samples for testing were collected using a soil stick to a depth of approximately 15–20 cm. At each site within the habitat (flower strip and lawn), three zones (repeats) were designated, spaced approximately 10–15 m apart. Approximately six samples were collected from each replication, and then a mixed sample was prepared, constituting 1 kg of soil.

2.3. Isolation of Fungi

The EPF from individual soil samples were isolated using the selective medium method developed by Strasser et al. [21], which is commonly used for the isolation of entomopathogenic fungi from soil [13,22,23,24,25,26,27,28,29] or plant material [30]. In order to determine the generic composition and quantitative assessment of infectious units of EPF in the tested soils, tests were carried out using a selective medium with the following composition: 20 g of glucose (Biomus, Białystok, Poland), 10 g of peptone (Becton, Dickinson and Company, Le Pont de Claix, France), and 18 g of agar (Sigma, St. Louis, MO, USA), which were dissolved in 1 dm3 of distilled water and then sterilized in an autoclave at 121 °C for 20 min. The following selective components were added to the prepared substrate after cooling to 50 °C: 0.6 g of streptomycin (Serva, Heidelberg, Germany), 0.05 g of tetracycline (Sigma, St. Louis, MO, USA), 0.05 g of cycloheximide (Sigma, St. Louis, MO, USA), and 0.1 g of dodine (Arysta LifeScience, Seraing, Belgium). The selective medium was poured into Petri dishes. From the collected soil sample, 2 g of soil was weighed and then covered with 18 mL of distilled water, with the addition of a surface-tension reducing agent (Triton X-100, Sigma, St. Louis, MO, USA). Using an automatic pipette, 0.1 mL of soil solution was collected and transferred to the surface of the selective substrate. Inoculations were performed in four replicates for each soil sample. The dishes with the applied soil solution were transferred to a heat chamber at 21 °C without access to light, and after 10 days, the number of colony-forming units (CFUs) of EPF developing on the culture medium was determined. The number of EPF was presented in CFU g−1 of dry matter in soil. Entomopathogenic fungi were identified microscopically based on the morphology of their microstructures (by determining the size and shape of conidia and conidiogenic cells) and the morphology of colonies, using standard keys [31,32,33,34]. Considering that only morphological methods were used to identify the fungi, they were assigned to the rank of genus because, as shown by the latest phylogenetic studies based on DNA sequencing [35,36,37], there are many species of fungi within the genera Beauveria, Metarhizium, and Cordyceps, the distinguishing of which is almost impossible without the use of molecular methods.

2.4. Statistical Analysis

The obtained results were statistically processed using the Statistica 13.3 TIBCO Software Inc., Palo Alto, CA, USA. One-way analysis of variance (ANOVA) and Tukey’s post hoc test were performed. The calculated means were combined into homogeneous groups at the significance level of α < 0.05. In the statistical analysis, the obtained CFU values of the identified EPF genera were averaged for each site within the habitat (flower strip, lawn). The standard deviation was calculated. Microsoft Excel version 2019 was used to prepare the charts.

3. Results

In soil samples collected in spring and autumn from two studied sites and two types of habitats (a flower strip and an adjacent lawn), four genera of EPF were found: Beauveria, Metarhizium, Cordyceps, and Akanthomyces. The site, habitat type, and date of soil sample collection impacted the type of isolated fungi and the density of their colony-forming units (CFUs) in the studied soils (Table 1 and Table 2). Among the EPF isolated in the soils collected from Site No. 1, the dominant genus was Metarhizium spp., which formed infection units on each study date and at each site (Table 1). The highest number of CFUs of this genus, 11.9 CFU × 103 g−1, was found in the soil collected in spring 2024 from a perennial lawn, differing significantly from the levels noted for other identified genera (F  =  9.1159; p < 0.0049).
Also, in the earlier study dates, fungi of the Metarhizium spp. genus occurred more frequently in the lawn soils than in the flower strip, which is probably due to the fact that these are perennial sites. The exception is the very low number of infectious units in soils collected in autumn 2024 (0.33 CFU × 103 g−1), which could have been influenced by very low rainfall, especially in September. The conducted studies have shown that in Site 1, EPF of the genus Beauveria spp. formed CFUs in soil samples taken from the lawn on each of the study dates, except autumn 2024. The highest number, 23.5 CFU × 103 g−1, was determined in the spring of 2024, and the difference was statistically significant in relation to the results for the other determined genera (F  =  9.1159; p < 0.0049). Fungi of the genus Cordyceps spp. were found only in soils collected from lawns, and their concentration was low. The tested soils also contained fungi of the genus Akanthomyces spp., which occurred in the soils of both habitats, with the highest CFU content determined in 2024 in the soil collected from the flower strips (Table 1).
In the studied soils of Site No. 2, the dominant genus was Metarhizium spp., isolated from the lawn, which formed 7.40 CFUs × 103 g−1, and this difference was statistically significant (F  =  11.280; p < 0.0442), whereas in the autumn the number of CFUs of this genus was negligible (Table 2). The genus Beauveria spp. formed the largest number of infectious units in autumn in the soil collected from the flower strip. For none of the study dates and habitats were infectious units of the genus Cordyceps spp. found. Fungi of the genus Akanthomyces spp. formed more CFUs in the soils of the flower strip than in the soils of the perennial lawn on both study dates. These differences were statistically significant in relation to the other isolated EPF genera (F  =  15.264; p < 0.0020; F  =  15.906; p < 0.0017). Also, in the case of soils collected from Site No. 2 in autumn, we noted no or very low CFUs of the designated EPF genera, which may be due to weather conditions (a relatively dry summer and autumn). Moisture and thermal conditions in the autumn of 2024 were as follows: the average monthly temperature in September was 18.1 °C, and the monthly total precipitation was 25.5 mm (3rd decade of September, 1.6 mm of precipitation) [data from the Automatic Meteorological Station at the Agricultural Experimental Station, named after Prof. Feliks Ceglarek in Zawady].
The average density of colony-forming units of all EPF genera combined in the soils collected from Site No. 1 was several times higher in the samples from the lawn than from the adjacent flower strip, except for in autumn of 2024 (Figure 1). On average, the highest number of CFUs was found in the spring of 2024, where the difference between the lawn and the flower strip was greater than 80%. At each test date, statistically significant differences in the number of CFUs were found between the soils taken from the flower strip and the perennial lawn (F  =  10.180; p < 0.0372).
In soils collected in the spring from Site No. 2, the average CFU density of all EPF genera together showed a clear, statistically significant dominance in soils collected from the lawn (F  =  13.275; p < 0.0298) (Figure 2). The opposite trend was observed in the autumn, where in the flower strip soil, the total CFU density of the marked EPF species was 90% higher than in the lawn soil.
The dominant EPF genera, regardless of the sampling date, in the soils of Site No. 1 were Metarhizium spp. and Beauveria spp., with significantly more CFUs formed by these fungi in the soils collected from the lawn than from the flower strip (65% and 80% more, respectively) (Figure 3). In soils collected from Site No. 2, the genus Metarhizium spp. formed the highest number of CFUs on average, both in the soil collected from the perennial lawn and the flower strip (Figure 4). Entomopathogenic fungi of the genus Cordyceps spp. did not form CFUs in the habitat of the perennial lawn in the soils from either Sites 1 or 2.

4. Discussion

Green spaces in urban area are an important component of the environment and are crucial to meeting the challenges posed by rapid urbanization and climate change. They provide significant environmental [3,38] as well as social and economic [39,40] benefits that improve the quality of life in urban areas. Proper spatial planning and management of urban green areas and their appropriate protection are essential for strengthening the resilience and sustainable development of cities [41]. Flower strips can be defined as deliberately created strips of profusely flowering plants which attract beneficial arthropods and become a habitat for various groups of organisms living in urban areas [6]. While flower strips are a relatively new element of green architecture in cities, lawns have certainly been a constant element for years, providing more stable habitats.
Biological protection, which reduces the exposure of the environment and humans to synthetic pesticides, is becoming an increasingly preferred system of plant protection against pests, which seems to be particularly important in densely populated urban spaces. One of the most important directions for the development and implementation of biological methods in plant protection in various environments is the use of biopreparations based on beneficial microorganisms [9,11,42,43]. Among biocontrol agents, entomopathogenic fungi constitute an important group. The anamorphic entomopathogenic fungi B. bassiana and M. anisopliae, from the order Hypocreales (Ascomycota), are natural enemies of a wide range of insects and arachnids, and both fungi display a cosmopolitan distribution [31]. Much effort has been put into research on the development of B. bassiana and M. anisopliae as biological control agents (for inundation and inoculation biological control) to be applied in agriculture and forestry in temperate regions, but also specifically in urbanized areas, where the use of chemical pesticides is limited [10,44]. Natural greenery and artificial green complexes play an important role in the functioning of this urban agglomeration. There are many insect species that function as food sources for EPF in urban green areas. These fungi most often attack soil-dwelling insects. Individuals who die due to mycosis are sources of disease spread and often become hotbeds of epizootic diseases [45]. They can act as pathogens or parasites of other organisms, but can also live in symbiosis with plants, algae, and animals. There is a huge group of fungi that demonstrate beneficial effects on other organisms, especially plants [9,12,27]. The species composition and density of infectious units of EPF in soils from different environments have been the subject of many studies conducted in different countries [9,24,25,26,28,29,44,46].
In the soil samples collected in spring and autumn from two studied sites and two types of habitats (a flower strip and an adjacent lawn), four genera of EPF were found: Beauveria, Metarhizium, Cordyceps, and Akanthomyces. It was determined that the site, habitat type, and season in which the samples were collected influenced the diversity of individual types of fungi and the density of their colony-forming units (CFUs) in the tested soils. It should be noted that the available literature does not provide information on the generic composition and intensity of EPF occurrence in soils from flower strips and a comparative analysis with the neighboring perennial lawns in urban spaces. When assessing the diversity and population of the examined fungi in these two habitats, it should also be taken into account that the flower strips were created in the urban space of Siedlce relatively recently, in 2021 (Site No. 1), and in the second site in 2022. These are therefore unstabilized sites in terms of soil and microbiology, created and separated from earlier lawns. In turn, the lawns adjacent to them have been in the urban space for at least several decades. Perhaps for this reason, in this study, it was observed that EPF, especially the genus Metarhizium, create significantly more infectious units in soil collected from under lawns, where a constant population of potential hosts has been present for years. Furthermore, the soil in these habitats appears to be more humid due to the dense cover created by grasses, which limits evaporation. On the other hand, flower strips increase biodiversity in urban spaces and agrocenoses because the flowering plants growing there attract a greater number of beneficial and pollinating insects, thus increasing the diversity of arthropods, including insects, living there. The dominant genera of EPF, forming the largest number of infectious units in the soils from the studied flower strips and adjacent lawns, were Metarhizium spp. and Beauveria spp. The dominance of these two genera of EPF in various soils in Poland was noted previously in the studies by Miętkiewski et al. [47], Tkaczuk [9], Tkaczuk et al. [13], and Majchrowska-Safaryan et al. [26], among others. Jarmuł-Pietraszczyk [8] studied the occurrence of EPF in selected parks and urban forests in the Warsaw municipality of Ursynów and found that the dominant species were B. bassiana and M. anisopliae, which were isolated from the soils of both urban green areas and forests. The fungus B. bassiana preferred natural and undisturbed areas, and its occurrence decreased in habitats with higher levels of human activity (e.g., fields or meadows). This preference was described by many authors, including Vänninen [48], Chandler et al. [49], and Quesada-Moraga et al. [50]. M. anisopliae is generally more resistant to intensive agricultural practices, and numerous studies have shown that it is much more prevalent in cultivated areas than in natural habitats [50,51,52,53]. Vänninen [48] suggested that B. bassiana requires frequent serial passage through insects to survive and that the relative scarcity of hosts in heavily cultivated (and sprayed) areas puts B. bassiana at a disadvantage in those soils. In contrast, M. anisopliae conidia are capable of longer-term persistence in the absence of arthropod hosts and exhibit a higher survival rate in the soil than that for B. bassiana [54,55]. Temperature is a factor that determines the EPF–host relationship, largely determining the success of plant pest control [56], and thermal requirements often vary, even within a single species [57,58]. Studies on the thermal requirements of EPF are mainly related to determining the minimum and maximum temperatures at which the pathogen is able to function [59,60]. It is extremely important to create appropriate habitat conditions (e.g., refuges) to enable survival of species susceptible to man-made changes in the landscape. Such an approach would allow for maintaining the richest possible gene pool of potential entomopathogenic microorganisms [50].
Entomopathogenic fungi are important biological agents of insect pest control in both urban and agroecosystem settings [49]. An improved comprehension of the ecology of endemic populations of fungal insect pathogens may be advantageous for evaluating their role in biological pest control strategies that are safe for both humans and the environment.

5. Conclusions

Four genera of entomopathogenic fungi, Beauveria ssp., Metarhizium spp., Cordyceps ssp., and Akanthomyces spp., were identified in soil samples collected in spring and autumn from two studied sites and two habitat types. The number of CFUs in the tested soils and the diversity of individual genera of fungi were significantly influenced by the location, habitat type, and season in which the samples were collected. The dominant genera of EPF forming the highest number of CFUs in the soils from the examined flower strips and adjacent lawns at Site No. 1 were Metarhizium spp. and Beauveria spp., whereas at Site No. 2, they were Metarhizium spp. and Akanthomyces spp. In soil samples from lawns, the presence of CFUs of fungi of the genus Cordyceps spp. was observed, but their presence was not recorded in the soil from flower strips. It was found that EPF occurred in higher densities in the soil from the studied habitats (flower strips and lawns) in autumn than in spring. Our research has shown that flower strips and lawns can harbor a variety of EPF. Both of these semi-natural habitats constitute a form of urban greenery that increases biodiversity and provides valuable ecosystem services that support sustainable urban development.

Author Contributions

Conceptualization, C.T.; writing—original draft preparation, C.T., A.M.-S. and M.D.; writing—review and editing, C.T. and A.M.-S. All authors have read and agreed to the published version of the manuscript.

Funding

The research carried out under research theme No. 159/23/B was financed by a science grant from the Ministry of Science and Higher Education.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Bolund, P.; Hunhammar, S. Ecosystem services in urban areas. Ecol. Econ. 1999, 29, 293–301. [Google Scholar] [CrossRef]
  2. Dudkiewicz, M.; Kopacki, M.; Iwanek, M.; Hortyńska, P. Problems with the experience of biodiversity on the example of selected Polish cities. Agron. Sci. 2021, 76, 67–84. [Google Scholar] [CrossRef]
  3. Zhang, F.; Qian, H.A. Comprehensive review of the environmental benefits of urban green spaces. Environ. Res. 2024, 252, 118837. [Google Scholar] [CrossRef]
  4. Belčáková, I.; Świąder, M.; Bartyna-Zielińska, M. The green infrastructure in cities as a tool for climate change adaptation and mitigation: Slovakian and Polish experiences. Atmosphere 2019, 10, 552. [Google Scholar] [CrossRef]
  5. Pauleit, S.; Andersson, E.; Anton, B.; Buijs, A. Advancing Urban Green Infrastructure in Europe: Outcomes and Reflections from the GREEN SURGE Project. Urban For. Urban Green. 2019, 40, 4–16. [Google Scholar] [CrossRef]
  6. Kowalska, J.; Sienkiewicz, P.; Antkowiak, M.; Krzymińska, J. Flower Strips as an Element of Green Infrastructure That Enhances the Biodiversity of the Ecosystem; Instytut Ochrony Roślin-Państwowy Instytut Badawczy: Poznań, Poland, 2024; p. 87. [Google Scholar]
  7. Szulczewska, B. Green Infrastructure—The End of History; Komitet Przestrzennego Zagospodarowania Kraju Polskiej Akademii Nauk: Warszawa, Poland, 2018; pp. 48–59. [Google Scholar]
  8. Jarmuł-Pietraszczyk, J.; Kamionek, M.; Wilkowski, P. Effect of long fertilisation on seasonal variability of occurrence of entomopathogenic nematodes and fungi. Ecol. Chem. Eng. 2011, 18, 359–363. [Google Scholar]
  9. Tkaczuk, C. Occurrence and Infective Potential of Entomopathogenic Fungi in Soils of Agrocenoses and Seminatural Habitats in the Agricultural Landscape. D. Sc. Thesis, Akademia Podlaska w Siedlcach, Siedlce, Poland, 2008. [Google Scholar]
  10. Augustyniuk-Kram, A.; Kram, K.J. Entomopathogenic fungi as an important natural regulator of insect outbreaks in forests (Review). In Forest Ecosystems—More Than Just Trees; Blanco, J.A., Lo, Y.-H., Eds.; IntechOpen: Rijeka, Croatia, 2012; pp. 265–294. [Google Scholar]
  11. Sosnowska, D. The contribution of conservation biological control method to integrated plant protection and organic farming. Prog. Plant Prot. 2018, 58, 288–293. [Google Scholar] [CrossRef]
  12. Sosnowska, D. Parasitic and antagonistic fungi in biological plant protection in Poland. Prog. Plant Prot. 2019, 59, 223–231. [Google Scholar] [CrossRef]
  13. Tkaczuk, C.; Majchrowska-Safaryan, A.; Harasimiuk, M. The occurrence and infective potential of entomopathogenic fungi in the soil of arable fields, meadows and forest habitats. Prog. Plant Prot. 2016, 56, 5–11. [Google Scholar] [CrossRef]
  14. Labbè, R.M.; Gillespie, D.R.; Cloutier, C.; Brodeur, J. Compatibility of an entomopathogenic fungus with a predator and a parasitoid in the biological control of greenhouse whitefly. Biocontrol Sci. Technol. 2009, 19, 429–446. [Google Scholar] [CrossRef]
  15. Al-Mazra’aw, M.S.; Al-Abbadi, A.M.; Shatnawi, M.; Ateyyat, M. Effect of application method on the interaction between Beauveria bassiana and neem tree extract when combined for Thrips tabaci (Thysanoptera: Thripidae) control. J. Food Agric. Environ. 2009, 7, 869–873. [Google Scholar]
  16. Wraight, S.P.; Ramos, M.E. Characterization of the synergistic interaction between Beauveria bassiana strain GHA and Bacillus thuringiensis morrisoni strain tenebrionis applied against Colorado potato beetle. J. Invertebr. Pathol. 2017, 144, 47–57. [Google Scholar] [CrossRef]
  17. Niassy, S.; Maniania, N.K.; Subramanian, S.; Gitonga, M.P.; Ekesi, S. Performance of a semiochemical-baited autoinoculation device treated with Metarhizium anisopliae for control of Frankliniella occidentalis on French bean in field cages. Entomol. Exp. Appl. 2012, 142, 97–103. [Google Scholar] [CrossRef]
  18. Duarte, R.T.; Gonçalves, K.C.; Espinosa, D.J.L.; Moreira, L.F.; Bortoli, S.A.; Humber, R.A. Potential of entomopathogenic fungi as biological control agents of diamondback moth (Lepidoptera: Plutellidae) and compatibility with chemical insecticides. J. Econ. Entomol. 2016, 109, 594–601. [Google Scholar] [CrossRef]
  19. Khun, K.K.; Wilson, B.A.L.; Stevens, M.M.; Huwer, R.K.; Ash, G.J. Integration of Entomopathogenic Fungi into IPM Programs: Studies Involving Weevils (Coleoptera: Curculionoidea) Affecting Horticultural Crops. Insects 2020, 11, 659. [Google Scholar] [CrossRef] [PubMed]
  20. Cuthbertson, A.; Audsley, N. Further screening of entomopathogenic fungi and nematodes as control agents for Drosophila suzukii. Insects 2016, 7, 24. [Google Scholar] [CrossRef] [PubMed]
  21. Strasser, H.; Forer, A.; Schinner, F. Development of media for the selective isolation and maintenance of virulence of Beauveria brongniartii. In Microbial Control of Soil Dwelling Pests; Jackson, T.A., Glare, T.R., Eds.; AgResearch: Lincoln, New Zealand, 1996; pp. 125–130. [Google Scholar]
  22. Kessler, P.; Enkerli, J.; Schweizer, C.; Keller, S. Survival of Beauveria brongniartii in the soil after application as a biocontrol agent against the European cockchafer Melolontha melolontha. Biocontrol 2004, 49, 563–581. [Google Scholar] [CrossRef]
  23. Shin, T.Y.; Choi, J.B.; Bae, S.M.; Koo, H.N.; Woo, S.D. Study on selective media for isolation of entomopathogenic fungi. Int. J. Indust. Entomol. 2010, 20, 7–12. [Google Scholar]
  24. Tkaczuk, C.; Tipping, C.; Majchrowska-Safaryan, A.; Król, A.; Wyrzykowska, M.; Wegensteiner, R. The occurrence of entomopathogenic fungi in soils from apple orchards protected in different farming systems. Fresenius Environ. Bull. 2019, 28, 7906–7914. [Google Scholar]
  25. Majchrowska-Safaryan, A.; Tkaczuk, C. Abundance of entomopathogenic fungi in leaf litter and soil layers in forested habitats in Poland. Insects 2021, 12, 134. [Google Scholar] [CrossRef]
  26. Majchrowska-Safaryan, A.; Tkaczuk, C.; Baj-Wójtowicz, B. Occurrence of entomopathogenic fungi in the soils of habitats of various use. Agron. Sci. 2023, 78, 5–18. [Google Scholar] [CrossRef]
  27. Kuźmiar, A.; Włodarczyk, K.; Gromadzka, P.; Siara, A.; Wolińska, A. Aktualny Stan Wiedzy Na Temat Biopreparatów Stosowanych W Rolnictwie; Wydawnictwo KUL: Lublin, Poland, 2021; 32p. [Google Scholar]
  28. Medo, J.; Cagáň, Ĺ. Factors affecting the occurrence of entomopathogenic fungi in soils of Slovakia as revealed using two methods. Biol. Control 2011, 59, 200–208. [Google Scholar] [CrossRef]
  29. Sporleder, M.; Lacey, L.A. Biopesticides. In Insect Pests of Potato; Alyokhin, A., Vincent, C., Giordanengo, P., Eds.; Elsevier: Oxford, UK, 2021; pp. 463–497. [Google Scholar]
  30. Meyling, N.V.; Eilenberg, J. Occurrence and distribution of soil borne entomopathogenic fungi within a single organic agroecosystem. Agric. Ecosyst. Environ. 2006, 113, 336–341. [Google Scholar] [CrossRef]
  31. Rehner, S.A.; Buckley, E.A. Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: Evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 2005, 97, 84–98. [Google Scholar] [CrossRef] [PubMed]
  32. Rehner, S.A.; Minnis, A.M.; Sung, G.H.; Luangsa-ard, J.J.; Devotto, L.; Humber, R.A. Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 2011, 103, 1055–1073. [Google Scholar] [CrossRef]
  33. Humber, R.A. Identification of Entomopathogenic Fungi. In Manual of Techniques in Invertebrate Pathology; Lacey, L.A., Ed.; Academic Press: London, UK, 2012; pp. 151–187. [Google Scholar] [CrossRef]
  34. Inglis, G.D.; Enkerli, J.; Goettel, M.S. Laboratory techniques used for entomopathogenic fungi: Hypocreales. In Manual of Techniques in Invertebrate Pathology; Lacey, L.A., Ed.; Academic Press: London, UK, 2012; pp. 189–253. [Google Scholar] [CrossRef]
  35. Bischoff, J.F.; Rehner, S.A.; Humber, R.A. Metarhizium frigidum sp. nov.: A cryptic species of M. anisopliae and member of the M. flavoviride complex. Mycologia 2006, 98, 737–745. [Google Scholar] [CrossRef]
  36. Bischoff, J.F.; Rehner, S.A.; Humber, R.A. A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 2009, 101, 512–530. [Google Scholar] [CrossRef]
  37. Kepler, R.M.; Luangsaard, J.J.; Hywel-Jones, N.L.; Quandt, C.A.; Sung, G.-H.; Rehner, S.A.; Aime, M.C.; Henkel, T.W.; Sanjuan, T.; Zare, R.; et al. A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). IMA Fungus 2017, 8, 335–353. [Google Scholar] [CrossRef]
  38. Nowak, D.J.; Hirabayashi, S.; Bodine, A.; Greenfield, E. Tree and forest effects on air quality and human health in the United States. Environ. Pollut. 2014, 193, 119–129. [Google Scholar] [CrossRef]
  39. Akbari, H.; Pomerantz, M.; Taha, H. Cool surfaces and shade trees to reduce energy use and improve air quality in urban areas. Sol. Energy 2001, 70, 295–310. [Google Scholar] [CrossRef]
  40. Kim, S.K.; Peiser, R.B. The economic effects of green spaces in planned and unplanned communities. J. Archit. Plan. Res. 2018, 35, 323–342. [Google Scholar]
  41. Poje, M.; Vukelić, A.; Židovec, V.; Prebeg, T.; Kušen, M. Perception of the vegetation elements of urban green spaces with a focuson flower beds. Plants 2024, 13, 2485. [Google Scholar] [CrossRef] [PubMed]
  42. Tomalak, M. Rynek biologicznych środków ochrony roślin i przepisy legislacyjne. Prog. Plant Prot. 2010, 50, 1053–1063. [Google Scholar]
  43. Fenibo, E.O.; Grace, N.I.; Weiz, N.; Tonderayi, M. The potential and green chemistry attributes of biopesticides for sustainable agriculture. Sustainability 2022, 14, 14417. [Google Scholar] [CrossRef]
  44. Meyling, N.V.; Thorup-Kristensen, K.; Eilenberg, J. Below-and above ground abundance and distribution of fungal entomopathogens in experimental conventional and organic cropping systems. Biol. Control 2011, 59, 180–186. [Google Scholar] [CrossRef]
  45. Sánchez-Peña, S.R.; San-Juan Lara, J.; Medina, R.F. Occurrence of entomopathogenic fungi from agricultural and natural ecosystems in Saltillo, México, and their virulence towards thrips and whiteflies. J. Insect Sci. 2011, 11, 1. [Google Scholar] [CrossRef]
  46. Uzman, D.; Pliester, J.; Leyer, I.; Entling, M.H.; Reineke, A. Drivers of entomopathogenic fungi presence in organic and conventional vineyard soils. Appl. Soil Ecol. 2019, 133, 89–97. [Google Scholar] [CrossRef]
  47. Miętkiewski, R.; Tkaczuk, C.; Badowska-Czubik, T. Entomogenous fungi isolated from strawberry plantation soil infested by Otiorhynchus ovatus L. Rocz. Nauk Rol. Ser. E 1992, 22, 39–46. [Google Scholar]
  48. Vänninen, I. Distribution and occurrence of four entomopathogenic fungi in Finland: Effect of geographical location, habitat type and soil type. Mycol. Res. 1996, 100, 93–101. [Google Scholar] [CrossRef]
  49. Chandler, D.; Hay, D.; Reid, A.P. Sampling and occurrence of entomopathogenic fungi and nematodes in UK soils. Appl. Soil Ecol. 1997, 5, 133–141. [Google Scholar] [CrossRef]
  50. Quesada-Moraga, E.; Navas-Cortes, J.A.; Maranhao, A.A.; Ortiz-Urquiza, A.S.; Santiago-Alvarez, C. Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycol. Res. 2007, 111, 947–966. [Google Scholar] [CrossRef] [PubMed]
  51. Bidochka, M.J.; Kasperski, J.E.; Wild, G.A.M. Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Can. J. Bot. 1998, 76, 1198–1204. [Google Scholar] [CrossRef]
  52. Hummel, R.L.; Walegenbach, J.F.; Barbercheck, M.E.; Kennedy, G.G.; Hoyt, G.D.; Arellano, C. Effects of production practices on soil- borne entomopathogens in western North Karolina vegetable systems. Environ. Entomol. 2002, 31, 84–91. [Google Scholar] [CrossRef]
  53. Sun, B.D.; Yu, H.Y.; Chen, A.; Liu, X.Z. Insect- associated fungi in soils of field crops and orchards. Crop Prot. 2008, 27, 1421–1426. [Google Scholar] [CrossRef]
  54. Latch, G.C.M.; Fallon, R.E. Studies on the use of Metarhizium anisopliae to control Oryctes rhinoceros. Entomophaga 1976, 21, 39–48. [Google Scholar] [CrossRef]
  55. Vänninen, I.; Tyni-Juslin, J.; Hokkanen, H. Persistence of augmented Metarhizium anisopliae and Beauveria bassiana in Finnishagricultural soils. BioControl 2000, 45, 201–222. [Google Scholar] [CrossRef]
  56. Fargues, J.; Luz, C. Effects of fluctuating moisture and temperature regimes on the infection potential of Beauveria bassiana for Rhodinus prolixus. J. Invertebr. Pathol. 2000, 75, 202–211. [Google Scholar] [CrossRef] [PubMed]
  57. Devi, K.U.; Sridevi, V.; Mohan, C.M.; Padmavathi, J. Effect of high temperature and water stress on in vitro germination and growth in isolates of the entomopathogenic fungus Beauveria bassiana (Bals.) Vuillemin. J. Invertebr. Pathol. 2005, 88, 181–189. [Google Scholar] [CrossRef]
  58. Alexandre, T.M.; Alves, L.F.A.; Neves, P.M.O.J.; Alves, S.B. Effect of temperature and poultry litter on Beauveria bassiana (Bals.) Vuill. and Metarhizium anisopliae (Metsch) virulence against the lesser mealworm Alphitobius diaperinus (Panzer) (Coleoptera: Tenebrionidae). Neotrop. Entomol. 2006, 35, 75–82. [Google Scholar] [CrossRef]
  59. Polar, P.; Aquino de Muro, M.; Kairo, M.T.K.; Moore, D.; Pegram, R.; John, S.A.; Roach-Benn, C. Thermal characteristics of Metarhizium anisopliae isolates important for the development of biological pesticides for the control of cattle ticks. Vet. Parasitol. 2005, 134, 159–167. [Google Scholar] [CrossRef]
  60. Ibarra-Corteś, K.H.; Guzmán-Franco, A.W.; González-Fernández, H.; Suarez-Espinosa, J.; Baverstock, J. Selection of a fungal isolate for the control of the pink hibiscus mealybug Maconellicoccus hirsutus. Pest Manag. Sci. 2013, 69, 874–882. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Average density of colony-forming units (CFU × 103 g−1) of all entomopathogenic fungi in the soil from the flower strips and lawns (Site No. 1). ± = standard deviation; abc = within columns with the same lowercase letters, results are not significant at α < 0.05.
Figure 1. Average density of colony-forming units (CFU × 103 g−1) of all entomopathogenic fungi in the soil from the flower strips and lawns (Site No. 1). ± = standard deviation; abc = within columns with the same lowercase letters, results are not significant at α < 0.05.
Sustainability 17 07819 g001
Figure 2. Average density of colony-forming units (CFU × 103 g−1) of all entomopathogenic fungi in the soil from the flower strips and lawns (Site No. 2). ± = standard deviation; ab = within columns with the same lowercase letters, results are not significant at α < 0.05.
Figure 2. Average density of colony-forming units (CFU × 103 g−1) of all entomopathogenic fungi in the soil from the flower strips and lawns (Site No. 2). ± = standard deviation; ab = within columns with the same lowercase letters, results are not significant at α < 0.05.
Sustainability 17 07819 g002
Figure 3. Average density of colony-forming units (CFU × 103 g−1) of individual genera of entomopathogenic fungi in the soil from the flower strips and lawns (Site No. 1). ± = standard deviation; ab = within columns with the same lowercase letters, results are not significant at α < 0.05.
Figure 3. Average density of colony-forming units (CFU × 103 g−1) of individual genera of entomopathogenic fungi in the soil from the flower strips and lawns (Site No. 1). ± = standard deviation; ab = within columns with the same lowercase letters, results are not significant at α < 0.05.
Sustainability 17 07819 g003
Figure 4. Average density of colony-forming units (CFU × 103 g−1) of individual genera of entomopathogenic fungi in the soil from the flower strips and lawns (Site No. 2). ± = standard deviation; ab = within columns with the same lowercase letters, results are not significant at α < 0.05.
Figure 4. Average density of colony-forming units (CFU × 103 g−1) of individual genera of entomopathogenic fungi in the soil from the flower strips and lawns (Site No. 2). ± = standard deviation; ab = within columns with the same lowercase letters, results are not significant at α < 0.05.
Sustainability 17 07819 g004
Table 1. Number of the colony-forming units (CFU × 103 g−1) of individual genera of entomopathogenic fungi in the soils from the flower strips and lawns (Site No. 1).
Table 1. Number of the colony-forming units (CFU × 103 g−1) of individual genera of entomopathogenic fungi in the soils from the flower strips and lawns (Site No. 1).
Genera of EPFSite No. 1
Autumn 2021Spring 2022Spring 2024Autumn 2024
Flower StripLawnFlower StripLawnFlower StripLawnFlower StripLawn
Beauveria
spp.
0.15 ± 0.11
ab
1.13 ± 1.32
b
0.0 ± 0.0
b
0.06 ± 0.09
b
1.86 ± 1.51
ab
23.5 ± 33.1
a
2.0 ± 1.68
ab
0.06 ± 0.09
a
Metarhizium
spp.
1.30 ± 1.20
a
7.53 ± 5.75
a
0.7 ± 0.24
a
8.73 ± 7.52
a
5.1 ± 2.92
a
11.9 ± 12.4
b
2.5 ± 0.82
a
0.33 ± 0.34
a
Cordyceps
spp.
0.0 ± 0.0
b
0.13 ± 0.09
c
0.0 ± 0.0
b
0.0 ± 0.0
b
0.0 ± 0.0
b
0.36 ± 0.51
c
0.0 ± 0.0
c
0.1 ± 0.14
a
Akanthomyces
spp.
0.0 ± 0.0
b
0.06 ± 0.09
c
0.05 ± 0.04
b
0.0 ± 0.0
b
0.2 ± 0.16
b
0.13 ± 0.09
c
0.22 ± 0.13
bc
0.16 ± 0.12
a
F value5.76649.005334.4865.471118.9279.115925.08610.970
p value0.03310.01120.00050.03740.00090.00490.00030.0621
± = standard deviation; abc = within columns with the same lowercase letters, results are not significant at α < 0.05.
Table 2. Number of the colony-forming units (CFU × 103 g−1) of individual genera of entomopathogenic fungi in the soils from the flower strips and lawns (Site No. 2).
Table 2. Number of the colony-forming units (CFU × 103 g−1) of individual genera of entomopathogenic fungi in the soils from the flower strips and lawns (Site No. 2).
Genera of EPFSite No. 2
Spring 2024Autumn 2024
Flower StripLawnFlower StripLawn
Beauveria
spp.
0.03 ± 0.04
b
0.26 ± 0.17
b
0.33 ± 0.47
b
0.0 ± 0.0
b
Metarhizium
spp.
0.83 ± 0.89
a
7.40 ± 3.34
a
3.36 ± 2.88
a
0.02 ± 0.03
b
Cordyceps
spp.
0.0 ± 0.0
b
0.0 ± 0.0
b
0.0 ± 0.0
c
0.0 ± 0.0
b
Akanthomyces
ssp.
0.93 ± 0.20
a
0.33 ± 0.26
b
0.66 ± 0.09
b
0.3 ± 0.14
a
F value15.26411.28015.90619.692
p value0.00200.04420.00170.0008
± = standard deviation; abc = within columns with the same lowercase letters, results are not significant at α < 0.05.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Tkaczuk, C.; Majchrowska-Safaryan, A.; Dadak, M. Comparative Analysis of the Occurrence of Entomopathogenic Fungi in Soils from Flower Strips and Lawns in Urban Space. Sustainability 2025, 17, 7819. https://doi.org/10.3390/su17177819

AMA Style

Tkaczuk C, Majchrowska-Safaryan A, Dadak M. Comparative Analysis of the Occurrence of Entomopathogenic Fungi in Soils from Flower Strips and Lawns in Urban Space. Sustainability. 2025; 17(17):7819. https://doi.org/10.3390/su17177819

Chicago/Turabian Style

Tkaczuk, Cezary, Anna Majchrowska-Safaryan, and Maciej Dadak. 2025. "Comparative Analysis of the Occurrence of Entomopathogenic Fungi in Soils from Flower Strips and Lawns in Urban Space" Sustainability 17, no. 17: 7819. https://doi.org/10.3390/su17177819

APA Style

Tkaczuk, C., Majchrowska-Safaryan, A., & Dadak, M. (2025). Comparative Analysis of the Occurrence of Entomopathogenic Fungi in Soils from Flower Strips and Lawns in Urban Space. Sustainability, 17(17), 7819. https://doi.org/10.3390/su17177819

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop