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Interactions among endophytic fungal entomopathogens (Ascomycota: Hypocreales), the green peach aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the aphid endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae)
Abstract and Figures
Entomopathogenic fungi are typically applied as innundative sprays with the expectation of short-term pest control, but a growing number of studies demonstrate the potential of these fungi to endophytically colonize a wide variety of plants and confer longer-term protection. Endophytic colonization of plants by fungal entomopathogens can also enable these fungi to establish intricate interactions in a tritrophic context; thus affecting other groups of natural enemies such as parasitoids. Yet to date, effects of endophytic plant colonization on parasitoids have mostly been investigated using the grass-endophyte organism systems. The present study investigates the effects of the fungal entomopathogens Beauveria bassiana and Metarhizium brunneum, following their endophytic colonization of sweet pepper Capsicum annum, on the development and fecundity of two successive generations of the green peach aphid Myzus persicae in addition to parasitism by the aphid endoparasitoid Aphidius colemani in two replicate greenhouse experiments. Plant roots were drenched with the conidial suspension of each fungal strain or sterile water, and the endophytic colonization of different plant parts (root, stem, and leaf) was confirmed 7 (when 1st generation M. persicae started feeding on caged treatment plants) and 17 (when A. colemani started parasitizing 2nd generation M. persicae reared on caged treatment plants) days post-inoculation (dpi). Inoculation with the tested fungal entomopathogens enhanced several plant growth parameters that were sampled 7 dpi (before M. persicae infestation) and all plant growth parameters sampled 35 dpi (following infestation with two successive generations of M. persicae). Fewer numbers of aphids were found when sampling plants inoculated with both fungal strains in comparison to the control during the development and reproduction of 1st and 2nd generations of M. persicae. The negative effects of plant colonization with the inoculated fungal strains on aphid development and fecundity also included prolonged development time, delayed onset of reproduction, and reduced birth rate. On the other hand, the percentage mummification and adult emergence of A. colemani progenies parasitizing 2nd generation aphid reared on inoculated or control plants were not affected by plant colonization with B. bassiana and M. brunneum. In addition, no differences were observed in development time, percentage female, and adult longevity of A. colemani progenies among inoculated and control plants. This study presents one of very few reports of the compatible use of endophytic fungal entomopathogens with other biological control agents, particularly parasitoids, for aphid suppression under controlled greenhouse conditions as part of an Integrated Pest Management (IPM) approach.
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... All other combinations appeared in one to three laboratory experiments each. Trichogramma pretiosum [24,47,52] and E. formosa [29,38,40,51] were the most researched parasitoids, followed by A. colemani [23,30,32,35,46], C. flavipes [55,58], and Diaeretiella rapae [18,43]. In terms of microorganisms, B. bassiana [17,18,24,26,32,33,35,40,42,43,48,51,52,54,55,[57][58][59][60][61][63][64][65] was the most studied fungus, followed by M. aniso-pliae [30,34,36,37,[48][49][50][51]53,55,57,58] and L. muscarium [18,23,38,41,46]. ...
... Trichogramma pretiosum [24,47,52] and E. formosa [29,38,40,51] were the most researched parasitoids, followed by A. colemani [23,30,32,35,46], C. flavipes [55,58], and Diaeretiella rapae [18,43]. In terms of microorganisms, B. bassiana [17,18,24,26,32,33,35,40,42,43,48,51,52,54,55,[57][58][59][60][61][63][64][65] was the most studied fungus, followed by M. aniso-pliae [30,34,36,37,[48][49][50][51]53,55,57,58] and L. muscarium [18,23,38,41,46]. Bacillus thuringiensis var. ...
... Thirty-eight out of forty-nine combinations of biocontrol agents were reported as compatible [18][19][20]22,[24][25][26]29,32,[34][35][36][37]39,41,[43][44][45]47,49,50,[52][53][54][55][56][57][58][59][60][62][63][64][65] (Table 1). Six combinations were reported as incompatible [17,27,28,42,51], often due to a lower emergence rate caused either by bad timing, direct infection, or too high dosage. ...
Biological pest control is an environmentally friendly alternative to synthetic pesticides, using organisms such as viruses, bacteria, fungi, and parasitoids. However, efficacy is variable and combining different biocontrol agents could improve success rates. We conducted a systematic review of studies combining a parasitoid with an entomopathogenic microorganism, the first of its kind. We searched in Web of Science and extracted data from 49 publications matching the pre-defined inclusion criteria. Combinations of 36 hymenopteran parasitoids with 17 entomopathogenic microorganisms used to control 31 target pests were found. Trichogramma pretiosum and Encarsia formosa were the most frequently studied parasitoids, while Beauveria bassiana, Metarhizium anisopliae, Lecanicillium muscarium, Bacillus thuringiensis var. kurstaki, the Spodoptera exigua multiple nucleopolyhedrovirus, and the Spodoptera frugiperda multiple nucleopolyhedrovirus were the main microbial agents assessed. Out of 49 parasitoid–microorganism combinations assessed in the laboratory experiments, thirty-eight were reported as compatible and six as incompatible. Timing and dosage of biopesticides played a crucial role, with later application and appropriate dosage minimizing adverse effects on parasitoid development. More research is needed to assess compatibility and efficacy under real-world conditions. Our review provides valuable insights for researchers and practitioners to optimize the combined use of micro- and macroorganisms for effective pest control.
... In particular, EPFs reduce insect pest populations by reducing their performance, penetrating their body, and feeding on them [142]. Accumulating evidence shows that EPFs have the potential to control M. persicae populations by affecting its prefeeding behaviour [142] and reducing its development and fecundity rate [143], as well as causing high mortality in bioassays using cultural filtrates of EPF (B. bassiana and M. anisopliae) [141,144]. ...
... An accumulating body of evidence has reported the economic loss caused by M. persicae across a wide range of crop plants, and several studies have been performed to develop control strategies to manage this pest. However, the majority of these studies have focused on a single control measure, either a biological or chemical control, such as the effect of host plants [165,178]; predators [179,180]; EPFs [143,144,181]; EPNs (157); EPVs Figure 7. Adult Myzus persicae survival (mean ± SE) out of the original 10 individuals and after 7 days in clip cages on cultivated and wild potatoes (n = 10). Asterisk indicates statistically significant difference among combinations (p < 0.05) (one-way ANOVA). ...
... An accumulating body of evidence has reported the economic loss caused by M. persicae across a wide range of crop plants, and several studies have been performed to develop control strategies to manage this pest. However, the majority of these studies have focused on a single control measure, either a biological or chemical control, such as the effect of host plants [165,178]; predators [179,180]; EPFs [143,144,181]; EPNs (157); EPVs [150,152]; and push-pull strategies (intercropping and trap crops) [182]. A few pioneering studies used combined biocontrol agents, such as three species of EPF along with 1% azadirachtin [144,181], or biocontrol recruitment via host-plant-induced defence [3]. ...
The peach–potato aphid, Myzus persicae (Sulzer), is one of the most important pests of economic crops. It damages the plant directly by consuming nutrients and water and indirectly by transmitting plant viruses. This pest has the unenviable title of having resistance to more insecticides than any other herbivorous insect pest. Due to the development of its resistance to chemical pesticides, it is necessary to find other control options. Consequently, increased efforts worldwide have been undertaken to develop new management approaches for M. persicae. In this review, we highlight the problems associated with the peach–potato aphid, its economic importance, and current management approaches. This review also describes the challenges with current management approaches and their potential solutions, with special focus given to the evolution of insecticidal resistance and sustainable pest management strategies, such as biocontrol agents, entomopathogens, the use of natural plant-derived compounds, and cultural methods. Furthermore, this review provides some successful approaches from the above eco-friendly pest management strategies that show high efficacy against M. persicae.
... For example, beneficial fungi like Trichoderma have been shown to increase plant defense against diverse pathogens, including Colletotrichum, Phytophthora, Pythium and Rhizoctonia (De la Cruz-Quiroz et al. 2018), and herbivores like the Southern green stinkbug (Nezara viridula) (Alınç et al. 2021;Woo et al. 2022). Likewise, inoculation of sweet pepper with endophytic entomopathogenic fungi such as Beauveria bassiana and Metarhizium brunneum significantly reduced Fusarium crown and root rot (Jaber and Alananbeh 2018) and negatively affected the development and fecundity of aphids (Myzus persicae) (Francis et al. 2022;Jaber and Araj 2018;Wilberts et al. 2022). ...
... Trichoderma harzianum T22 (recently re-classified as Trichoderma afroharzianum (Chaverri et al. 2015); for consistency with previous research further referred to as T. harzianum in this manuscript) is the active ingredient of a variety of biopesticides and biofertilizers, including Trianum-P (Koppert Biological Systems, The Netherlands), from which it was isolated. Beauveria bassiana ARSEF 3097 and M. brunneum ARSEF 1095 have been shown to colonize plant tissues from different hosts endophytically upon artificial inoculation, including tomato (Jaber and Araj 2018;Klieber and Reineke 2016;Wilberts et al. 2022), while T. harzianum T22 is mainly known to colonize and form an intimate association with plant roots (Harman et al. 2004). All three strains have been shown to provide plants with important benefits, like enhanced plant growth and enhanced resistance against phytopathogens and herbivorous insects (Alınç et al. 2021;Jaber and Alananbeh 2018;Jaber and Araj 2018;Sani et al. 2020;Wilberts et al. 2022Wilberts et al. , 2023. ...
... Beauveria bassiana ARSEF 3097 and M. brunneum ARSEF 1095 have been shown to colonize plant tissues from different hosts endophytically upon artificial inoculation, including tomato (Jaber and Araj 2018;Klieber and Reineke 2016;Wilberts et al. 2022), while T. harzianum T22 is mainly known to colonize and form an intimate association with plant roots (Harman et al. 2004). All three strains have been shown to provide plants with important benefits, like enhanced plant growth and enhanced resistance against phytopathogens and herbivorous insects (Alınç et al. 2021;Jaber and Alananbeh 2018;Jaber and Araj 2018;Sani et al. 2020;Wilberts et al. 2022Wilberts et al. , 2023. Fungal strains were stored on potato dextrose agar plugs in 35% glycerol at -80 °C until further use. ...
Aims
Plant-beneficial fungi are non-pathogenic fungi that provide a variety of benefits to crops, including improved nutrition and increased resistance against biotic and abiotic stresses. However, to what extent these beneficial effects depend on fungal strain or host cultivar is not well known.
Methods
In this study, we investigated the effects of different species of plant-beneficial fungi on plant nutrient composition and resistance against zoophytophagous predators, and assessed whether effects are mediated by plant cultivar. We evaluated how seed inoculation of three tomato (Solanum lycopersicum L.) cultivars (Micro-Tom, Moneymaker and Pearson) with three fungi (Beauveria bassiana ARSEF 3097, Metarhizium brunneum ARSEF 1095 and Trichoderma harzianum T22) affected the leaf sap nutrient composition and feeding damage (number of necrotic rings) and mortality rate of Nesidiocoris tenuis.
Results
Plant nutrient composition was mainly determined by cultivar, but was also affected by fungal treatment. Significantly less necrotic rings were formed in fungus-inoculated plants compared to control plants. However, out of the nine cultivar-fungus combinations tested only the combination of Micro-Tom and B. bassiana showed less feeding damage by N. tenuis along with increased insect mortality.
Conclusions
We conclude that plant-beneficial fungi affect plant nutrient composition, but this has little effect on plant defense against N. tenuis, suggesting that differences in insect damage are most likely not mediated by changes in nutrient composition. Moreover, effects depended largely on the cultivar and fungal strain used, indicating that generalizations based on single strain or cultivar studies should be made with caution.
... Moreover, benzoxazinoids and flavonoids were identified in host plants in response to EIPF inoculation and associated with a reduction in aphid infestation, helping to elucidate the role of specific plant secondary metabolites in plant-fungus-herbivore interactions [63]. Finally, the accumulation of mycotoxins in plant tissues colonized by EIPF, such as L. lecanii, is another example of a reduction in aphid survival rates [74]. Antibiosis due to the production of fungal secondary metabolites within plants has been previously suggested to be the main mechanism of action of endophytic entomopathogenic fungi in several studies [64]. ...
... Most of the studies have reported that, regardless of the mode of application, EPF has a very high impact on mortality and reproduction. The variation in the level of impact for the population growth parameter is probably related to the fact that there have been very few studies that have tested this parameter [74,84]. Table 1. ...
... Level of impact on the studied parameters (mortality, reproduction, population growth and behavior) is represented by different color codes: red for high; orange for moderate; yellow for low; white for not tested. Gibberella moniliformis Acyrthosiphon pisum [84] Aphis fabae [84] Hypocrea lixi Acyrthosiphon pisum [84] Isaria fumosorosea Myzus persicae [52] Lecanicillium lecanii Aphis gossypii [57] Metarhizium anisioplaie Acyrthosiphon pisum [84] Myzus persicae [52] Metarhizium brunneum Aphis gossypii [61] Myzus persicae [74] Neotyphodium lolii Metopolophium dirhodum [95] Rhopalosiphum padi [95] Not identified Diuraphis noxia [96] Purpureocillium lilacinum Aphis gossypii [70] Trichoderma asperellum Acyrthosiphon pisum [84] Aphis fabae [84] ...
Entomopathogenic fungi (EPF) are cosmopolitan species of great interest in pest management due to their ability to cause epizooty in soil-dwelling and aboveground insects. Besides their direct effect against a wide host range of serious agricultural insect pests, such as aphids, a major emphasis has been placed on investigating the impact of EPF with endophytic traits (EIPF) on aboveground tripartite interactions between host plants, herbivores and beneficial insects. However, despite their valuable role in biocontrol processes, there is still more to explore about their diverse potential as ecofriendly biological control agents. Herein, we provide an overview of the meaningful role and faced challenges following the use of EPF and EIPF to control aphids.
... Metarhizium is also a symbiont of agriculturally and economically important plants, such as tomato, bean, corn, wheat and soybean [7]. When Metarhizium colonizes plants, it can confer benefits such as growth promotion [14][15][16], nutrient transfer [3] and protection against insect pests [15,16] and diseases [17,18]. In turn, the host plant provides the fungus with photosynthetic compounds [19]. ...
... Metarhizium is also a symbiont of agriculturally and economically important plants, such as tomato, bean, corn, wheat and soybean [7]. When Metarhizium colonizes plants, it can confer benefits such as growth promotion [14][15][16], nutrient transfer [3] and protection against insect pests [15,16] and diseases [17,18]. In turn, the host plant provides the fungus with photosynthetic compounds [19]. ...
... It is worth noting, however, that the initial stages of Metarhizium endophytic colonization involve rhizosphere colonization [56]. Likewise, in both associations, fungi can promote plant growth and protection against pests [3,4,15]. ...
Metarhizium species can be mutualistic symbionts of plants. They are able to colonize roots, promote plant growth and provide protection against pests. We previously found Metarhizium robertsii and M. brunneum associated with coffee roots in a diversified coffee system. Here, we investigated whether these fungi, when inoculated in coffee seedlings, can associate with roots, improve seedling growth and indirectly protect against the coffee leaf miner (CLM) Leucoptera coffeella (Lepidoptera: Lyonetiidae). We performed a greenhouse experiment with coffee seedlings using suspensions of each Metarhizium species applied as soil drenches to potted seedlings. We also challenged these plants with CLM infestation (two adult couples per plant). We recovered Metarhizium spp. from most of the seedling roots 43 days after fungal inoculation. Plants inoculated with M. robertsii showed a 30% leaf area increase compared to the control. Both isolates promoted protection against CLM in coffee seedlings, reducing the percentual of leaf area mined and prolonging CLM development time by two days versus controls. Besides this protection provided by Metarhizium, M. robertsii also improves seedling growth. Therefore, these Metarhizium species could be considered for the development of inoculants for coffee seedlings.
... Beauveria bassiana ARSEF 3097 was acquired from the Agricultural Research Service Collection of Entomopathogenic Fungal Cultures (ARSEF; New York, USA), and represents the active ingredient in several commercially available bioinsecticides such as Naturalis 1 (Intrachem, Italy). The strain can colonize diverse plant species endophytically following artificial inoculation, including sweet pepper, besides its direct entomopathogenic capability [25,54]. The fungal strains were preserved at -80˚C in 35% glycerol on potato dextrose agar (PDA) plugs, until used in the experiments. ...
... Together, our findings thus indicate that fungal inoculation does not always benefit the plant, at least from an indirect defensive perspective. Indeed, in line with previous research, our study confirms that the outcome of plant-mediated interactions between plant-beneficial fungi and parasitoids depends on a multifaceted interplay involving the herbivore and parasitoid species, as well as the plant and microbial species (or strain) [12,27,32,37,54,70,71]. ...
There is increasing evidence that plant-associated microorganisms play important roles in defending plants against insect herbivores through both direct and indirect mechanisms. While previous research has shown that these microbes can modify the behaviour and performance of insect herbivores and their natural enemies, little is known about their effect on egg parasitoids which utilize oviposition-induced plant volatiles to locate their hosts. In this study, we investigated how root inoculation of sweet pepper (Capsicum annuum) with the plant-beneficial fungi Beauveria bassiana ARSEF 3097 or Trichoderma harzianum T22 influences the olfactory behaviour of the egg parasitoid Trissolcus basalis following egg deposition by its host Nezara viridula. Olfactometer assays showed that inoculation by T. harzianum significantly enhanced the attraction of the egg parasitoid, while B. bassiana had the opposite effect. However, no variation was observed in the chemical composition of plant volatiles. Additionally, fitness-related traits of the parasitoids (wasp body size) were not altered by any of the two fungi, suggesting that fungal inoculation did not indirectly affect host quality. Altogether, our results indicate that plant inoculation with T. harzianum T22 can be used to enhance attraction of egg parasitoids, which could be a promising strategy in manipulating early plant responses against pest species and improving sustainable crop protection. From a more fundamental point of view, our findings highlight the importance of taking into account the role of microorganisms when studying the intricate interactions between plants, herbivores and their associated egg parasitoids.
... Trichoderma harzianum strain T22, which has recently been re-classified as Trichoderma afroharzianum Rifai (Hypocreales: Hypocreaceae) (Chaverri et al., 2015) (for consistency with previous research further referred to as T. harzianum in this study) is the active ingredient in various biofertilizers and biopesticides, including Trianum-P (Koppert Biological Systems, The Netherlands), from which it was isolated for this study. While predominantly known as entomopathogenic fungi, B. bassiana ARSEF 3097 and M. brunneum ARSEF 1095 are also able to endophytically colonize plant tissues from several hosts upon artificial inoculation, including tomato (Klieber and Reineke, 2016;Jaber and Araj, 2018;Wilberts et al., 2022;Meesters et al., 2023). Trichoderma harzianum T22 is primarily known to colonize plant roots epiphytically but has also been found to colonize plant tissues endophytically (Harman et al., 2004). ...
... Trichoderma harzianum T22 is primarily known to colonize plant roots epiphytically but has also been found to colonize plant tissues endophytically (Harman et al., 2004). The three selected strains have been found to offer plants various benefits, including enhanced plant growth (Sani et al., 2020;Van Hee et al., 2023;Wilberts et al., 2023) and increased resistance against pathogens and/or herbivorous insects (Jaber and Alananbeh, 2018;Jaber and Araj, 2018;Alınçet al., 2021;Wilberts et al., 2022;Meesters et al., 2023;Van Hee et al., 2023). The fungal strains were preserved on potato dextrose agar (PDA) plugs in 35% glycerol at -80°C until further use. ...
Biological control using plant-beneficial fungi has gained considerable interest as a sustainable method for pest management, by priming the plant for enhanced defense against pathogens and insect herbivores. However, despite promising outcomes, little is known about how different fungal strains mediate these beneficial effects. In this study, we evaluated whether inoculation of tomato seeds with the plant-beneficial fungi Beauveria bassiana ARSEF 3097, Metarhizium brunneum ARSEF 1095 and Trichoderma harzianum T22 affected the plant’s volatile organic compound (VOC) profile and the host-choice behavior of Nesidiocoris tenuis, an emerging pest species in NW-European tomato cultivation, and the related zoophytophagous biocontrol agent Macrolophus pygmaeus. Results indicated that fungal inoculation did not significantly alter the VOC composition of tomato plants. However, in a two-choice cage assay where female insects were given the option to select between control plants and fungus-inoculated plants, N. tenuis preferred control plants over M. brunneum-inoculated plants. Nearly 72% of all N. tenuis individuals tested chose the control treatment. In all other combinations tested, no significant differences were found for none of the insects. We conclude that inoculation of tomato with plant-beneficial fungi had limited effects on plant volatile composition and host-choice behavior of insects. However, the observation that N. tenuis was deterred from the crop when inoculated with M. brunneum and attracted to non-inoculated plants may provide new opportunities for future biocontrol based on a push-pull strategy.
... While the primary focus of research on plant-beneficial fungi has been on plant growth promotion and protection against plant pathogens, there is increasing evidence that plant-beneficial fungi also protect crops from insect herbivores (Pineda et al. 2010). For instance, it has been demonstrated that plant inoculation with arbuscular mycorrhizal fungi (AMF), root-colonizing fungi like Trichoderma or endophytes negatively influences the performance of aphids, spider mites, whiteflies, caterpillars, and stink bugs, correlating with enhanced defensive plant responses (Alınç et al. 2021;Contreras-Cornejo et al. 2018;Coppola et al. 2019;Getman-Pickering et al. 2021;Gupta et al. 2022;Jaber and Araj 2018;Rasool et al. 2021a, b;Wilberts et al. 2022). The use of plant-beneficial fungi has therefore become an emerging strategy to boost sustainable agriculture, but their persistence and functionality under field conditions are sometimes inconsistent and beneficial effects are often context-dependent (Baron and Rigobelo 2022;Lee Díaz et al. 2021). ...
... Beauveria bassiana ARSEF 3097 is the active ingredient in the commercial bioinsecticide Naturalis ® , and was obtained from the Agricultural Research Service Collection of Entomopathogenic Fungal Cultures (ARSEF; New York, USA). The strain has been shown to colonize diverse plant species endophytically upon artificial inoculation, including sweet pepper, in addition to its direct insect-killing capability (Jaber and Araj 2018;Vega et al. 2008;Wilberts et al. 2022). Trichoderma harzianum T22 (recently re-classified as Trichoderma afroharzianum (Chaverri et al. 2015); for consistency with previous research further referred to as T. harzianum in this manuscript) is a fungal strain produced by protoplast fusion (Harman et al. 2004). ...
AimsPlant-beneficial fungi play an important role in enhancing plant growth and protecting plants from biotic and abiotic stresses. However, context-dependency of such effects and differences among fungi often lead to inconsistent results that hamper their widespread use. Here, we investigated the effect of plant-beneficial fungi on plant growth and herbivore resistance, and how effects are mediated by fertilization.Methods
Sweet pepper (Capsicum annuum L.) plants were root-inoculated with the plant-beneficial fungi Beauveria bassiana ARSEF 3097 and Trichoderma harzianum T22 and grown in a low-nutrient potting mix, with or without additional nutrients. Plant growth and herbivore resistance against the southern green stink bug (Nezara viridula L.) were compared between fungal treatments and fertilization levels by measuring several growth traits and quantifying feeding damage and plant defense-related gene expression.ResultsFertilization significantly increased plant growth, but at the same time made plants more susceptible to herbivory. Irrespective of fertilization, T. harzianum stimulated growth and reduced feeding damage (number of leaf punctures), while B. bassiana only enhanced growth. For both strains, fungal inoculation generally increased the expression of marker genes involved in salicylic acid- and jasmonic acid-dependent defense responses upon herbivory, but this was less pronounced for salicylic acid-dependent defense signaling under fertilization.Conclusions
We conclude that fungal inoculation improved plant growth and generally elicited a stronger defense response to stink bug feeding. Accordingly, plant damage was reduced by T. harzianum. Overall these results show that plant-beneficial fungi have the potential to promote plant growth and reduce feeding damage, irrespective of fertilization.
... Gadhave et al. (2016) indicated that B. bassiana does not affect the parasitoid species associated with pea leafminer. Similar results were obtained for Myzus persicae (Hemiptera: Aphididae) and its parasite Aphidius colemani (Hymenoptera: Braconidae) (Jaber and Araj, 2018). However, we found that the B4 strain had a constraining effect on the growth, development, and reproduction of A. cucumeris and A. japonicus populations. ...
Entomopathogenic fungi (EPF) are economical and environmentally friendly, forming an essential part of integrated pest management strategies. We screened six strains of Beauveria bassiana (B1–B6) (Hypocreales: Cordycipitaceae), of which B4 was the most virulent to Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). We further assessed the biological characteristics of strain B4 and the environmental factors influencing its ability to infect B. dorsalis. We also evaluated the effects of B4 on two of the natural predators of B. dorsalis. We found that strain B4 was the most virulent to 3rd instar larvae, pupae, and adult B. dorsalis, causing mortality rates of 52.67, 61.33, and 90.67%, respectively. B4 was not toxic to B. dorsalis eggs. The optimum B4 effects on B. dorsalis were achieved at a relative humidity of 91–100% and a temperature of 25°C. Among the six insecticides commonly used for B. dorsalis control, 1.8% abamectin emulsifiable concentrate had the strongest inhibitory effect on B4 strain germination. B4 spraying affected both natural enemies (Amblyseius cucumeris and Anastatus japonicus), reducing the number of A. cucumeris and killing A. japonicus adults. We found a valuable strain of EPF (B4) that is virulent against many life stages of B. dorsalis and has great potential for the biological control of B. dorsalis. We also provide an important theoretical and practical base for developing a potential fungicide to control B. dorsalis.
... These fungi can also form symbiotic associations with plants (endophytes), living in plant tissues without symptoms through colonization [56,57]. Furthermore, EPFs have the potential to endophytically colonize a variety of plant species, improving plant growth and enhancing yields, while being harmful to pests [55,[58][59][60]. There is evidence that EPFs make plants more resistant to stress caused by biotic or abiotic factors, enhance plant nutrient uptake, and excite hormone production, thereby contributing to plant growth [59,61,62]. ...
Tetranychus urticae is an important pest of tomato crops globally, affecting plant yield and growth. Beauveria bassiana and Metarhizium robertsii have the potential to control T. urticae. We investigated the influence of two B. bassiana (i.e., WG-12 and WG-19) isolates and one M. robertsii (WG-02) isolate when colonizing different plant organs (leaves, stems, and roots) and their influence on the growth of tomato plants, through foliar, root-dipping, and seed-soaking application techniques. We also examined the acaricidal activity of the three isolates against T. urticae (female adults), spraying tomato leaf discs with each isolate separately. After 28 days, WG-12 and WG-19 colonized 97 and 91% of the leaves after foliar inoculation, whereas WG-02 exhibited the lowest leaf colonization (76%). The height of the tomato plants, the root length, the number of leaves, and the weight of the biomass above and below the ground were enhanced significantly after inoculation with WG-02 vs. B. bassiana isolates and control. The complete mortality of T. urticae was caused by WG-12 and WG-02 after 10 days, whereas WG-19 killed 94% of the adults. For the effective management of T. urticae, we propose the application of the WG-02 isolate since it provides complete protection and promotes the growth of tomato plants.
... The Solanaceae family, comprising over 2000 species across 90 genera, has substantial commercial value in both the food and medicinal industries, as reported by Petkova et al. (2021). Previous research on other Solanaceae members has revealed systematic colonization by endophytic fungi within these plants (Tefera and Vidal, 2009;Jaber and Enkerli, 2016;Jaber and Araj, 2018). The ability of endophytic fungi to colonize Solanaceae plants suggests that specific growth requirements are adequately met within this family. ...
The rise of multidrug resistance among microorganisms, where they develop resistance against formerly effica-cious drugs, has led to increased disease prevalence and mortality rates, posing a growing challenge. Globally, antibiotic resistance has made a significant impact, causing millions of fatalities each year. Endophytic fungi have gained considerable attention in research due to their potential to produce a wide variety of secondary metabo-lites, including natural substances with antimicrobial capabilities. The genera Aspergillus and Penicillium stand out as the most prevalent species of endophytic fungi. Filamentous fungi, such as these are responsible for the production of 45% of known microbial metabolites. This review focuses on exploring the bioactive substances produced by endophytic fungi from these two genera, particularly in conjunction with medicinal plants. Emphasis is placed on their antimicrobial activity and their ability to inhibit multidrug-resistant pathogens. As the need for alternative treatments to combat drug-resistant infections continues to grow, endophytic fungi have the potential to provide a valuable source of bioactive molecules for medical applications.
... Entomopathogenic fungi used as insect pathogens colonize endophytically a wide array of host plant tissues and subsequently confer benefits such as plant growth enhancement and suppression of disease pathogens as found for B. bassiana. Plant growth mediated by the endophytic colonization by diverse fungal genera of entomopathogens has resulted from inoculated seed treatment, foliar spray, and root drench [19,26,[61][62][63] . B. bassiana has been reported to suppress the soil-borne pathogens caused by damping off by Rhizoctonia solani and Pythium myriotylum in tomato [33] . ...
The saprophytic white muscardine fungus Beauveria bassiana (Balsamo) Vuillemin is a potential biocontrol agent against varied insect pests, is a commercially available mycopesticide in many countries, and is extensively used for insect pest management. It produces several metabolites, such as antibacterial, antifungal, cytotoxic, and insecticidal compounds that protect against insect pests and plant pathogens, with dual-purpose crop protection, a new concept in plant disease management. This insect pathogen is also beneficial to plant endophytes that are antagonistic to plant diseases and promote rhizosphere colonizers and plant growth, inducing systemic resistance. The induced systemic responses of fungal endophytes enhance genes that are expressed in pathogenesis and increase the production of pathogenesis-related proteins and defense enzymes. The fungus infects the insects by degrading mechanically and chemically their cuticles. It promotes plant growth, provides systemic protection against pests and pathogens in sustainable agricultural crop production, and reduces the usage of chemical pesticides.
... Germination was quantified after 8, 10, 14, 18, and 24 hours by counting the first 100 conidia seen; this was replicated three times across different fields of view and for three slides per isolate. The conidia were considered germinated when the germ tube was twice the length of the conidium width [48,54]. Additionally, spore viability was determined by plating 100 μL of the conidial suspension, diluted to 10 −6 on SDA, incubating at 21, 27, and 33˚C, respectively, and counting CFUs after 5 days [26,55]. ...
Queensland fruit fly, Bactrocera tryoni , Froggatt (Diptera: Tephritidae) is Australia’s primary fruit fly pest species. Integrated Pest Management (IPM) has been adopted to sustainably manage this polyphagous species with a reduced reliance on chemical pesticides. At present, control measures are aimed at the adult stages of the fly, with no IPM tools available to target larvae once they exit the fruit and pupate in the soil. The use of entomopathogenic fungi may provide a biologically-based control method for these soil-dwelling life stages. The effectiveness of fungal isolates of Metarhizium and Beauveria species were screened under laboratory conditions against Queensland fruit fly. In bioassays, 16 isolates were screened for pathogenicity following exposure of third-instar larvae to inoculum-treated vermiculite used as a pupation substrate. The best performing Metarhizium sp. isolate achieved an average percentage mortality of 93%, whereas the best performing Beauveria isolate was less efficient, with an average mortality of 36%. Susceptibility to infection during different development stages was investigated using selected fungal isolates, with the aim of assessing all soil-dwelling life stages from third-instar larvae to final pupal stages and emerging adults. Overall, the third larval instar was the most susceptible stage, with average mortalities between 51–98% depending on the isolate tested. Moreover, adult mortality was significantly higher when exposed to inoculum during pupal eclosion, with mortalities between 56–76% observed within the first nine days post-emergence. The effect of temperature and inoculum concentration on insect mortality were assessed independently with candidate isolates to determine the optimum temperature range for fungal biological control activity and the rate required for application in field conditions. Metarhizium spp . are highly efficacious at killing Queensland fruit fly and have potential for use as biopesticides to target soil-dwelling and other life stages of B . tryoni .
... Existen varios antecedentes del uso de entomopatógenos en el control de áfidos de modo general a nivel internacional (Boni et al., 2021;Ek-Ramos et al., 2021;Gebreyohans et al., 2021;Jaber y Araj, 2018;Mukherjee et al., 2020). En Perú, es escasa la información relacionada al tema, esto podría ser por la poca información a nivel nacional y el desconocimiento de los agricultores sobre la efectividad de los microorganismos en el manejo de las plagas; no se ha encontrado reportes sobre el éxito del manejo de los pulgones con el uso de los entomopatógenos, más aún bajo las condiciones ambientales de los valles interandinos de Perú. ...
El uso de hongos y bacterias con capacidad patogénica hacia los insectos se considera una alternativa agroecológica sostenible de lucha eficiente contra las plagas por ser microorganismos de fácil producción en escala industrial, formulación y uso; entonces, el objetivo ha sido evaluar cuatro formulados entomopatógenos en el control de Brevicoryne brassicae L, plaga clave de la col (Brassica oleracea L.), en diseño de bloques completos al azar de 4 tratamientos, sumado un testigo absoluto y 4 réplicas, siendo las variables evaluadas la cantidad de pulgones muertos y vivos por planta y cantidad de plantas infestadas. Los formulados comerciales Biosafe, BesT-K, Metarrizo y Yurak que contenían cepas de Bacillus subtilis, Bacillus thuringiensis var kurstaki (Btk), Metarhizium anisopliae y Bauveria bassiana, respectivamente, son los que fueron utilizados mediante la aplicación por aspersión al cultivo en dos épocas de siembra, temporada agosto-diciembre 2019 y agosto-diciembre 2021. Entre los resultados se registró al M. anisopliae con hasta 91,11 % de eficiencia, seguida por B. bassiana con 89,50 % y Bs con 79,38 % en la reducción de las poblaciones en condiciones de campo; en laboratorio el Btk y M. anisopliae alcanzaron el 100 % de mortalidad en un lapso de siete días, por lo que se concluye que a mediano plazo los hongos entomopatógenos en campo resultan ser más eficientes en el control del pulgón, sin embargo, en condiciones controladas el Btk también es eficiente.
... In recent years, entomopathogenic fungi, primarily from the genera Metarhizium and Beauveria, have been explored as potential endophytes (reviews: [29][30][31]). It has been experimentally proven that plant endophytic colonization by entomopathogenic fungi negatively affects the development and number of phytophages and leads to the stimulation of plant growth, a decrease in their damage from phytopathogens, a change in immune status, and an increase in plant productivity [32][33][34][35][36]. For Solanaceae plants, similar effects have been registered in conjunction with the application of entomopathogenic endophytes [37][38][39][40][41]. Nonetheless, only a limited number of articles show an increase in resistance to osmotic stress, including salinity and drought stress, in plants colonized by the entomopathogenic endophytes Metarhizium and Beauveria [42][43][44][45][46][47]. ...
The considerable decrease in crop productivity associated with the expansion of saline soils is an acute problem in agriculture. Endophytic fungi positively affect plant fitness under salinity conditions. The effects of potato inoculation with the conidia of the Beauveria bassiana strain Sar-31 on growth (the weight of fresh and dry biomass, shoot and root length, numbers of stolons and leaves, and the leaf surface) and physiological indices (the concentration of pigments, free proline and malondialdehyde, and antioxidant enzymes’ activity) were evaluated under moderate chloride salinity (100 mM). The results indicated that the plant’s association with the fungus mitigated the negative impact of salinity probably because of the activation of antioxidant enzymes and accumulation of free proline in potato tissues. Moreover, under the influence of B. bassiana Sar-31, the number of stolons significantly increased, which is one of the main characteristics of potato as an agricultural crop. Thus, Sar-31 may be a promising candidate for further investigation of its ability to stimulate growth and increase the stress tolerance of potato plants.
... The endophytic behavior of entomopathogenic fungi has been reported in numerous cultivated and non-cultivated plant species, both naturally colonized and artificially inoculated by diverse methods, and several of these fungi have the potential to improve the plant's response to biotic and abiotic stresses (Vega, 2008;Vidal and Jaber, 2015;Vega, 2018;Gange et al., 2019;Francis et al., 2022). For example, banana and common bean plants inoculated with entomopathogenic fungi showed reduced reproduction rates and higher mortality rates of the banana root borer (Cosmopolites sordidus), one of the most important pests on bananas (Akello et al., 2008), and the pea leaf miner (Liriomyza huidobrensis) (Akutse et al., 2013), respectively, while endophytic colonization of sweet pepper by entomopathogenic fungi had negative effects on the development and fecundity of aphids (Myzus persicae) (Jaber and Araj, 2018;Wilberts et al., 2022). Moreover, endophytic entomopathogenic fungi have been shown to reduce pathogen infestation (Jaber and Alananbeh, 2018;Jaber and Ownley, 2018) and provide plants with drought stress tolerance (Ferus et al., 2019). ...
As endophytes, entomopathogenic fungi can protect plants against biotic and abiotic stresses and at the same time promote plant growth and plant health. To date, most studies have investigated whether Beauveria bassiana can enhance plant growth and plant health, while only little is known about other entomopathogenic fungi. In this study, we evaluated whether root inoculation of the entomopathogenic fungi Akanthomyces muscarius ARSEF 5128, B. bassiana ARSEF 3097 and Cordyceps fumosorosea ARSEF 3682 can promote plant growth of sweet pepper (Capsicum annuum L.), and whether effects are cultivar-dependent. Plant height, stem diameter, number of leaves, canopy area, and plant weight were assessed four weeks following inoculation in two independent experiments using two cultivars of sweet pepper (cv. ‘IDS RZ F1’ and cv. ‘Maduro’). Results showed that the three entomopathogenic fungi were able to enhance plant growth, particularly canopy area and plant weight. Further, results showed that effects significantly depended on cultivar and fungal strain, with the strongest fungal effects obtained for cv. ‘IDS RZ F1’, especially when inoculated with C. fumosorosea. We conclude that inoculation of sweet pepper roots with entomopathogenic fungi can stimulate plant growth, but effects depend on fungal strain and crop cultivar.
... Our results showed that larvae and pupae had a prolonged developmental period, and both fecundity and survival rates were reduced. Previous studies have also reported the effectiveness of various EPFs, such as B. bassiana and M. anisopliae, in suppressing insect pests [14,52,[61][62][63][64]. ...
The fall armyworm, Spodoptera frugiperda (Noctuidae; Lepidoptera), is a serious threat to food security as it has the potential to feed on over 353 plant species. To control this insect pest, endophytic colonization of entomopathogenic fungi (EPF) in plants is being considered as a safer and more effective alternative. This study evaluated the efficacy of two EPFs, Beauveria bassiana and Metarhizium anisopliae, for endophytic colonization using foliar spray and seed treatment methods on maize plants, and their impact on the survival, development, and fecundity of S. frugiperda. Both EPF effectively colonized the maize plants with foliar spray and seed treatment methods, resulting in 72–80% and 50–60% colonization rates, respectively, 14 days after inoculation. The EPF negatively impacted the development and fecundity of S. frugiperda. Larvae feeding on EPF-inoculated leaves had slower development (21.21 d for M. anisopliae and 20.64 d for B. bassiana) than the control treatment (20.27 d). The fecundity rate was also significantly reduced to 260.0–290.1 eggs/female with both EPF applications compared with the control treatment (435.6 eggs/female). Age-stage-specific parameters showed lower fecundity, life expectancy, and survival of S. frugiperda when they fed on both EPF-inoculated leaves compared with untreated leaves. Furthermore, both EPFs had a significant effect on population parameters such as intrinsic (r = 0.127 d−1 for B. bassiana, and r = 0.125 d−1 for M. anisopliae) and finite rate (λ = 1.135 d−1 for B. bassiana, and λ = 1.1333 d−1 for M. anisopliae) of S. frugiperda compared with the control (r = 0.133 d−1 and λ = 1.146 d−1). These findings suggest that EPF can be effectively used for the endophytic colonization of maize plants to control S. frugiperda. Therefore, these EPFs should be integrated into pest management programs for this pest.
... Endophytic application of EPF controls the insects that perforate and feed inside the leaves, roots, stems, seeds, and rhizomes (Resquín-Romero et al., 2016). Foliar spray of EPF like Metarhizium brunneum and Beauveria bassiana has been found to temporarily colonize plants like alfalfa, tomato, sweet pepper, and melons, endophytically (Jaber & Araj, 2018). The endophytic presence of EPF in tomato plants through artificial inoculation showed effective control of Tuta absoluta (Leaf miner) (Klieber & Reineke, 2016;Resquín-Romero et al., 2016). ...
The use of entomopathogenic fungi (EPF) like Beauveria, Metarhizium, Lecanicillium, and Isaria is upsurging in recent years for the management of crop insect pests. EPF are considered better than synthetic insecticides as they are safe for humans, sustainable to the environment, and target-specific in nature. Many of these EPF are pathogenic to economically important insect pests and thus are capable of controlling them. They are cheaper in long run, show lesser residual effects, and are able to overcome the problem of resistance. EPF degrades the host cuticle and proliferates in hemolymph as hyphal bodies, secreting the toxins responsible for the death of host insects. The later saprophytic growth leads to the production of fungal spores capable of reinfecting other hosts. Different commercial formulations of EPF are available globally such as liquid formulation, wettable powder, suspensible granules, and so on. These available formulations under different trade names can be used for several crops and pests at the recommended dosage to obtain optimum results. The storage conditions should be maintained to retain the viability of EPF. Modern biotechnological interventions could be vital in enhancing the efficacy of these entomopathogens by manipulating their traits. Specialized researches are necessary to understand the interaction between EPF, host insects, crops, and their environment in order to explore the best formulation of mycoinsecticides. This review explores the overview of EPF, its mode of action, significance, commercial formulations, future prospects, and the summary of recent findings. Readers could realize the essence of EPF in sustainable agriculture through this review.
... Endophytic application of EPF controls the insects that perforate and feed inside the leaves, roots, stems, seeds, and rhizomes (Resquín-Romero et al., 2016). Foliar spray of EPF like Metarhizium brunneum and Beauveria bassiana has been found to temporarily colonize plants like alfalfa, tomato, sweet pepper, and melons, endophytically (Jaber & Araj, 2018). The endophytic presence of EPF in tomato plants through artificial inoculation showed effective control of Tuta absoluta (Leaf miner) (Klieber & Reineke, 2016;Resquín-Romero et al., 2016). ...
The use of entomopathogenic fungi (EPF) like Beauveria, Metarhizium, Lecanicillium, and Isaria is upsurging in recent years for the management of crop insect pests. EPF are considered better than synthetic insecticides as they are safe for humans, sustainable to the environment, and target-specific in nature. Many of these EPF are pathogenic to economically important insect pests and thus are capable of controlling them. They are cheaper in long run, show lesser residual effects, and are able to overcome the problem of resistance. EPF degrades the host cuticle and proliferates in hemolymph as hyphal bodies, secreting the toxins responsible for the death of host insects. The later saprophytic growth leads to the production of fungal spores capable of reinfecting other hosts. Different commercial formulations of EPF are available globally such as liquid formulation, wettable powder, suspensible granules, and so on. These available formulations under different trade names can be used for several crops and pests at the recommended dosage to obtain optimum results. The storage conditions should be maintained to retain the viability of EPF. Modern biotechnological interventions could be vital in enhancing the efficacy of these entomopathogens by manipulating their traits. Specialized researches are necessary to understand the interaction between EPF, host insects, crops, and their environment in order to explore the best formulation of mycoinsecticides. This review explores the overview of EPF, its mode of action, significance, commercial formulations, future prospects, and the summary of recent findings. Readers could realize the essence of EPF in sustainable agriculture through this review.
... Plant height, weight, and other growth parameters have been reported in some studies (e.g. Kabaluk and Ericsson 2007, Elena et al. 2011, Sasan and Bidochka 2012, Liao et al. 2014, Lopez and Sword 2015, Jaber and Enkerli 2016, Jaber and Araj 2018, Jaber and Enkerli 2017. ...
The world is facing severe consequences of chemical fertilizers and synthetic pesticides. As a safer and eco-friendly option for crop nutrition and pest control, endophytic fungi (EFs) are now hotpots in sustainable crop production research. This comprehensive review elucidated the potentials of EF in sustainable crop production amid various biotic and abiotic stress conditions as well as their extraordinary role in phyto- and bioremediation. A critical investigation on how climatic factors such as temperature, rainfall, nutrient level, pH and storage condition affect the survival and performance of EFs are also presented. On-going research majorly focused on the application of endophytic fungi as crop growth promoters, biocontrol agents, and stress mediators. However, a lack of in-depth understanding of the underlying mechanism is predominant. Nevertheless, challenges of successful isolation and identification of EFs hinder their commercialization. Modern genomic technologies and nanotechnology-based applications of EFs can help in overcome the barriers. This review will provide direction for future research where EFs will lead next-generation sustainable strategies to cope with climate change.
... Forty-four potted grapevine plants were inoculated with either M. robertsii strain ARSEF-2575-GFP or EF3.5(2) by watering the roots with 50 mL of a 1 × 10 7 conidia·mL −1 suspension split into two doses of 20 mL on the first day and 30 mL on the 6th day. The concentration was judged optimal to successfully establish several strains of EIPF including Metarhizium spp. as endophyte with root drenching treatment according to [56]. Twentyeight control plants were treated with the same volume of a sterile suspension solution. ...
Characterizing the association of endophytic insect pathogenic fungi (EIPF) with plants is an important step in order to understand their ecology before using them in biological control programs. Since several methods are available, it is challenging to identify the most appropriate for such investigations. Here, we used two strains of Metarhizium robertsii: EF3.5(2) native to the French vineyard environment and ARSEF-2575-GFP a laboratory strain expressing a green fluorescent protein, to compare their potential of association with non-grafted grapevine Vitis vinifera. Three methods were used to evaluate the kinetics of rhizosphere and grapevine endospheric colonization: (i) Droplet Digital (ddPCR), a sensitive molecular method of M. robertsii DNA quantification in different plant parts, (ii) culture-based method to detect the live fungal propagules from plant tissues that grew on the medium, (iii) confocal imaging to observe roots segments. Both strains showed evidence of establishment in the rhizosphere of grapevines according to the culture-based and ddPCR methods, with a significantly higher establishment of strain EF3.5(2) (40% positive plants and quantified median of exp(4.61) c/μL) compared to strain ARSEF-2575-GFP (13% positive plants and quantified median of exp(2.25) c/μL) at 96–98 days post-inoculation. A low incidence of association of both strains in the grapevine root endosphere was found with no significant differences between strains and evaluation methods (15% positive plants inoculated with strain EF3.5(2) and 5% with strain ARSEF-2575-GFP according to culture-based method). ddPCR should be used more extensively to investigate the association between plants and EIPF but always accompanied with at least one method such as culture-based method or confocal microscopy.
... Vuill. (Hypocreales: Cordycipitaceae), is the best-studied EPF and has a wide range of plant hosts and can be found as a natural endophyte, suggesting that it has complex life cycles that can be completed in plants, soil, or invertebrates [16]. Moreover, recent studies on commercial endophytic strains of B. bassiana have highlighted its ability to not only promote plant growth but also provide systemic protection against pests and pathogens [17,18], placing this EPF at the top of the list of promising biological agents to improve crop production. ...
Entomopathogenic fungi (EPF) can colonize plant tissues and serve crops not only as biopesticides but also as biostimulants that promote plant growth and trigger defense mechanisms. In this context, field trials were conducted evaluating two commercial strains of the entomopathogen Beauveria bassiana (Hypocreales: Cordycipitaceae), GHA (Botanigard) and PPRI 5339 (Velifer® ES) and a wild strain (AP0101) isolated from Achaia, Greece. The three strains were investigated in the field for their endophytic effects on melon Cucumis melo (Cucurbitales: Cucurbitaceae) and strawberry Fragaria sp. (Rosales: Rosaceae) plants and in particular for their ability to colonize plant tissues, control infestations of sucking insects Aphis gossypii (Hemiptera: Aphididae), Chaetosiphon fragaefolii (Hemiptera: Aphididae) and Frankliniella occidentalis (Thysanoptera: Thripidae), and improve plant growth parameters (plant height, number of flowers and fruits). All experimental fungal strains successfully colonized both plants. A significant decrease in the aphid and thrip populations was observed in the treated plants compared to the untreated control. As for plant growth, the number of flowers and fruits was significantly increased in plants treated with B. bassiana strains AP0101 and PPRI 5339. Our results clearly indicate that fungal endophytes can efficiently act as dual action agents demonstrating both insecticidal and growth-promoting effects.
... Vuill. (Hypocreales: Cordycipitaceae), is the best-studied EPF and has a wide range of plant hosts and can be found as a natural endophyte, suggesting that it has complex life cycles that can be completed in plants, soil, or invertebrates [16]. Moreover, recent studies on commercial endophytic strains of B. bassiana have highlighted its ability to not only promote plant growth but also provide systemic protection against pests and pathogens [17,18], placing this EPF at the top of the list of promising biological agents to improve crop production. ...
Entomopathogenic fungi (EPF) can colonize plant tissues and serve crops not only as bi-opesticides but also as biostimulants that promote plant growth and trigger defense mechanisms. In this context, field trials were conducted evaluating two commercial strains of the entomopatho-gen Beauveria bassiana (Hypocreales: Cordycipitaceae), GHA (Botanigard) and PPRI 5339 (Velifer ® ES) and a wild strain (AP0101) isolated from Achaia, Greece. The three strains were investigated in the field for their endophytic effects on melon Cucumis melo (Cucurbitales: Cucurbitaceae) and strawberry Fragaria sp. (Rosales: Rosaceae) plants and in particular for their ability to colonize plant tissues, control infestations of sucking insects Aphis gossypii (Hemiptera: Aphididae), Chaetosiphon fragaefolii (Hemiptera: Aphididae) and Frankliniella occidentalis (Thysanoptera: Thripidae), and improve plant growth parameters (plant height, number of flowers and fruits). All experimental fungal strains successfully colonized both plants. A significant decrease in the aphid and thrip populations was observed in the treated plants compared to the untreated control. As for plant growth, the number of flowers and fruits was significantly increased in plants treated with B. bassiana strains AP0101 and PPRI 5339. Our results clearly indicate that fungal endophytes can efficiently act as dual action agents demonstrating both insecticidal and growth-promoting effects.
... It has been well documented that artificially inoculated endophytes established themselves in crop plants and improved the plant growth by improving plant biomass and other parameters [86][87][88] . There are different inoculation methods that may vary with plant variety as well as the type of endophyte. ...
Microbial communities in nature involve complex interactions with several biotic and abiotic components. An endo-symbiotic association is one in which one organism lives within the host plant for at least a part of its life. It is often obligate and does not create visible disease and has been reported to exist for at least 400 million years. Beneficial endophytes promote plant nutrient uptake, host plant growth, reduce disease severity, inhibit plant pathogens and improve tolerance to environmental stresses. Stresses like salinity, alkalinity, drought, global warming, temperature and pollution will increase in prominence and endophytes are predicted to play a significant role and offer eco-friendly techniques to increase productivity under such conditions. There also exists the potential for genetic modification of endophytes to impart additional stress tolerance traits in hosts. The present review discusses the beneficial effect of fungal and bacterial endophytes, emphasizing improving crop productivity under abiotic stress conditions. The review also discusses the various aspects of physiological and molecular mechanisms determining the interaction and stress tolerance, enhancing plant functions and productivity.
In this study, the bioinsecticidal action of a commercial formulation with Beauveria bassiana was evaluated on the new sucking pest in Greece: Halyomorpha halys, of the kiwifruit. Additionally, the biostimulant potential of the same formulation was studied on kiwi growth. The application was performed in three different ways in a commercial field of kiwi crop A. deliciosa “Hayward” field in Arta, Greece: (i) trunk spray, (ii) root injection, and (iii) trunk inoculation. During the 2 years seasons of the experiment, weekly measurements of the H. halys population were determined. The insect is sucking plants nutrients; therefore, the total chlorophyll content in the leaves of the treatments was recorded weekly. In addition, the percentage of infested kiwifruits was estimated at the end of the experiment. Moreover, to study the biostimulant potential of the formulation, growth measurements on stems and leaves were performed during the experiment. Finally, at the kiwi harvest point, the fruit biomass, dimensions, and weight were obtained, and the leaves’ proline content was evaluated. The results encourage us to further study this EPF formulation as the bioinsecticidal effect was noted by the reduction in H. halys population, and biostimulant action was perceived by the higher plant biomass.
Plant pathogens with their abundance are harmful and cause huge damage to different agricultural crops and economy of a country as well as lead towards the shortage of food for humans. For their management, the utilization of entomopathogenic fungi is an eco-friendly technique, sustainable to the environment, safe for humans and has promising effect over chemical-based pesticides. This process requires a biochemical mechanism, including the production of enzymes, toxins, and other metabolites that facilitate host infection and invasion. Essential enzymes such as chitinase, proteinase, and lipase play a direct role in breaking down the host cuticle, the primary barrier to EPF (Entomopathogenic Fungi) infection. Additionally, secondary metabolites such as destruxins in Metarhizium, beauvericin in Beauveria, hirsutellides in Hirsutella, isarolides in Isaria, cordyols in Cordyceps, and vertihemipterins in Verticillium, among others, act both directly and indirectly to disable the defense mechanisms of insect hosts, thereby accelerating the EPF infection process. The chemical composition of these secondary metabolites varies, ranging from simple non-peptide pigments such as oosporine to highly complex piperazine derivatives such as vertihemiptellides. The biocontrol efficacy of EPF is extensively studied, with numerous fungal strains commercially available on a large scale for managing arthropod pests. This review emphasizes the role of proteins and enzymes against crop pathogens, detailing their mode of action, and describing the metabolites from entomopathogenic fungi and their biological activities. In doing so, these findings contribute to establishing a symbiotic equilibrium between agricultural productivity and environmental conservation.
Graphical abstract
Os fungos promotores de crescimento apresentam potencial para serem utilizados na produção de mudas. O objetivo deste trabalho foi avaliar crescimento vegetativo de mudas de café arábica inoculadas com os fungos Trichoderma harzianum e Beauveria bassiana, e determinar o tempo de imersão das sementes na suspensão dos conídios. As sementes foram imergidas na suspensão de conídios (1 x 107 conídios.mL-1) por 0h, 6h, 12h, 24h, 48h e 96h, constituindo um arranjo fatorial 3 x 6 em blocos casualizados. Foram avaliados: altura da parte aérea, diâmetro do colo, número de pares de folhas, área foliar, comprimento de raiz, massa fresca e seca. O fungo B. bassiana promoveu maior altura de plantas nos tempos 0h, 6h e 96h e maior número de pares de folhas nos tempos de 6h e 96h. O fungo T. harzianum promoveu menor comprimento de raiz e ao fungo B. bassiana no tempo 6h, e em 96h. O fungo T. harzianum promoveu maior diâmetro do colo das mudas nos tempos 12h, 48h e 96h. O fungo B. bassiana promoveu maior massa fresca de parte aérea comparado ao fungo T. harzianum. Não houve diferença significativa entre os demais parâmetros. O tempo de imersão das sementes por 65h promoveu maior área foliar e não há relação com os fungos promotores de crescimento. Deve-se ampliar as pesquisas com os fungos B. bassiana e T. harzianum, uma vez que, há indícios de ganhos em determinados parâmetros de crescimento vegetativo, como altura de planta e diâmetro do colo. O tempo de imersão não é um fator determinante no crescimento vegetativo das mudas de café arábica, na presença dos fungos B. bassiana e T. harzianum.
Seed priming with beneficial endophytic fungi is an emerging sustainable strategy for enhancing plant resistance against insect pests. This study examined the effects of Beauvaria bassiana Bb20091317 and Metarhizium rileyi MrCDTLJ1 fungal colonization on maize growth, defence signalling, benzoxazinoid levels and gene expression. The colonization did not adversely affect plant growth but reduced larval weights of Spodoptera frugiperda . Maize leaves treated with M. rileyi exhibited higher levels of jasmonic acid, jasmonoyl‐Isoleucine, salicylic acid, and indole acetic acid compared to control. B. bassiana and M. rileyi accelerated phytohormone increase upon S. frugiperda herbivory. Gene expression analysis revealed modulation of benzoxazinoid biosynthesis genes. We further elucidated the immune regulatory role of the transcription factor zmWRKY36 using virus‐induced gene silencing (VIGS) in maize. zmWRKY36 positively regulates maize immunity against S. frugiperda, likely by interacting with defense‐related proteins. Transient overexpression of zmWRKY36 in tobacco‐induced cell death, while silencing in maize reduced chitin‐triggered reactive oxygen species burst, confirming its immune function. Overall, B. bassiana and M. rileyi successfully colonized maize, impacting larval growth, defense signalling, and zmWRKY36 ‐mediated resistance. This sheds light on maize‐endophyte‐insect interactions for sustainable plant protection.
The escalating global food demand driven by a gradually expanding human population necessitates strategies to improve agricultural productivity favorably and mitigate crop yield loss caused by various stressors (biotic and abiotic). Biotic stresses are caused by phytopathogens, pests, and nematodes, along with abiotic stresses like salt, heat, drought, and heavy metals, which pose serious risks to food security and agricultural productivity. Presently, the traditional methods relying on synthetic chemicals have led to ecological damage through unintended impacts on non-target organisms and the emergence of microbes that are resistant to them. Therefore, addressing these challenges is essential for economic, environmental, and public health concerns. The present review supports sustainable alternatives, emphasizing the possible application of fungal endophytes as innovative and eco-friendly tools in plant stress management. Fungal endophytes demonstrate capabilities for managing plants against biotic and abiotic stresses via the direct or indirect enhancement of plants’ innate immunity. Moreover, they contribute to elevated photosynthesis rates, stimulate plant growth, facilitate nutrient mineralization, and produce bioactive compounds, hormones, and enzymes, ultimately improving overall productivity and plant stress resistance. In conclusion, harnessing the potentiality of fungal endophytes represents a promising approach toward the sustainability of agricultural practices, offering effective alternative solutions to reduce reliance on chemical treatments and address the challenges posed by biotic and abiotic stresses. This approach ensures long-term food security and promotes environmental health and economic viability in agriculture.
Aphids are a major pest of cropping systems throughout the world. In most cases, crop aphids are controlled with broad-spectrum insecticides; although generally very effective at preventing yield loss, this approach risks non-target damage to beneficial organisms. In the last 20 years, a number of selective insecticides have become available to control aphids while minimising harm to other arthropods. Previous studies have found that two such insecticides, flonicamid and afidopyro-pen, cause only low-level acute mortality impacts on aphid parasitoids in Australian grain crops. However, little research has examined the sub-lethal effects of these chemicals, which could induce various physiological changes that impact pest control. We hypothesised that both flonicamid and afidopyropen have negative effects that extend beyond the immediate acute mortality previously published. To test this hypothesis, we undertook a series of experiments to determine the effects of flonicamid and afidopyropen, along with the synthetic pyrethroid gamma-cyhalothrin, on aphid parasitism (mummification) rate, emergence rate of the next generation and the next generation sex ratio in three important aphid parasitoids, Aphidius colemani (Viereck), Diaeretiella rapae (M'Intosh) and Aphelinus abdominalis (Dalman). Analogous with previous research, our acute toxicity bioas-says showed that all three insecticides had low (<30%) mortality impacts. Although sub-lethal impacts could not be assessed for D. rapae due to the low level of aphid parasitism by that species, our findings showed negative impacts on fecundity in surviving A. abdominalis and A. colemani. Of particular note is the increase in International Organisation for Biological Control ratings to moderate (30%-80% mortality and/or reproductive reduction) when mortality and reduced fecundity effects were combined to determine overall fitness impacts. Gamma-cyhalothrin typically resulted in higher negative impacts on A. abdominalis and A. colemani (compared with flonicamid and afidopyropen); however, quite surprisingly , these impacts were not rated as highly toxic. Taken together, our results suggest that, even when sub-lethal impacts are considered, flonicamid and afidopyropen are useful tools for farmers targeting aphid populations while mini-mising the non-target impacts on parasitoids. We recommend semi-field and/or field trials to further assess the impacts of these insecticides on aphid parasitoid populations.
The primary method for preventing postharvest fungal degradation of fruits and vegetables is the application of chemical fungicides. Increasing public concern regarding the lingering presence of fungicidal contamination of perishables and the emergence of resistant pathogen populations have been the main obstacles to the effective use of fungicides. Recent research has aimed to create and assess new substitute control methods to reduce dependency on synthetic fungicides. For the control of fungal deterioration, a number of nonchemical methods have been suggested. These methods have been found to lessen fruit and vegetable postharvest rots. However, they all have disadvantages that may make them less commercially viable. None of the nonchemical control approaches has consistently shown the ability to provide a reasonable level of disease control that supports acceptance as a replacement for synthetic fungicides. There has recently been a surge in interest in employing natural items to halt decomposition and extend the shelf life of perishables. Natural, biologically active compounds have the potential to replace synthetic fungicides. Significant genera of anamorphic postharvest infections include Penicillium, Aspergillus, Geotrichum, Botrytis, Fusarium, Alternaria, Colletotrichum, Dothiorella, Lasiodiplodia, and Phomopsis. Coordinated postharvest infection management strategies should be implemented to reduce the loss of fresh fruits and vegetables qualitatively and quantitatively during food supply chain.
The green peach aphid, Myzus persicae, is a significant insect pest worldwide. The potential for using Linum usitatissimum flax seed oil to control insects has been reported. However, no study has been conducted on the efficacy of flax seed oil against M. persicae. Therefore, this study aimed to evaluate the bioactivity of Linum usitatissimum flax seed oil at four concentrations (1.00, 3.00, 5.00, and 10.0 ml / 100 ml water). The highest mortality of adults (100%) was caused 4 days post-treatment with all tested concentrations. Similarly, the results demonstrate that foliar application of flax seed oil against all nymphal stages caused 100% mortality rates at all concentrations after 4 days of treatment. The rate of nymph production of aphids significantly decreased and reached 0.0 nymph per adult after 4 days. The results suggest that flax seed oil has the potential as a biological control agent of M. persicae. Keywords: botanicals, essential oil, insects, biological control
BACKGROUND
Nonpathogenic fungi associated with plants can enhance plant defenses against stress factors, including herbivory. This study assessed whether cotton plants grown from seeds treated with different fungi affected boll weevil, Anthonomus grandis grandis Boheman, development and reproduction along with plant tolerance. We used whole plants grown from seeds treated with different fungi (Chaetomium globosum TAMU520 and TAMU559, Phialemonium inflatum TAMU490, and Beauveria bassiana) versus non‐treated controls to test insect growth, reproduction, and plant tolerance assays in a greenhouse.
RESULTS
Regarding boll weevil reproduction, fewer larvae hatched and fewer adults emerged from fungal‐treated plants. In addition, the developmental time from oviposition to adult emergence was delayed in the plants treated with all fungi. For plant tolerance, B. bassiana‐treated plants attacked by boll weevils shed fewer squares than nonfungal‐treated plants.
CONCLUSION
Fungal treatments can affect boll weevil performance and reproduction on cotton plants, with potentially negative effects on population growth. Collectively, these results support the potential for cottonseed treatments with fungi as a novel tool for boll weevil management in the field. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
Biological control using natural enemies such as predatory insects and parasitoids has become an important alternative way of pest management and represents a crucial component in Integrated Pest Management (IPM). Although parasitoids are commonly used as biocontrol agents, their efficacy is not always sufficient to reduce pest populations to acceptable densities. Given that parasitoids can be attracted towards plants inoculated with entomopathogenic fungi, a combination of endophytic entomopathogenic fungi and parasitoids may lead to enhanced biocontrol efficacy, but information in this regard is scarce. Here, we used sweet pepper (Capsicum annuum L.), the entomopathogenic fungus Akanthomyces muscarius ARSEF 5128, the tobacco peach aphid Myzus persicae var. nicotianae and the aphid parasitoid Aphidius ervi to assess whether root inoculation with an entomopathogenic fungus has the potential to increase the biocontrol efficacy of an arthropod biological control agent. Results obtained over a five-weeks period revealed that a combination of the fungus and the parasitoid significantly improved biocontrol efficacy compared to the separate applications of the biocontrol agents, specifically by enhancing short-term parasitoid effectiveness. In greenhouse cages with A. muscarius and A. ervi, the aphid population was not able to produce progeny, and aphids were parasitized fast and efficiently. In cages with control plants and A. ervi, parasitism efficiency was significantly lower and the aphid population was able to increase by several generations. In these cages, the parasitoids could effectively control the aphid infestation after repeated parasitoid releases. We conclude that fungal inoculation improved parasitoid biocontrol efficacy, providing new opportunities for pest control.
Various techniques used by crop plants to evade insect pests and pathogen attacks have been documented. Among these, plant defense strategies induced by endophytic insect pathogenic fungi are arguably one of the most discussed. Endophytic fungi frequently colonize plants and inhabit their internal tissues for a portion of their lifespan without producing visible symptoms of the disease. This phenomenon is widespread and diverse in both natural and agricultural ecosystems, and is present in almost all plant organs. Many fungi can obtain nutrients by infecting and killing insects, and this ability has been developed numerous times in different fungal lineages. These species mainly consist of those in the order Hypocreales (Ascomycota), where the generalist insect pathogens, Beauveria sp. (Cordycipitaceae) and Metarhizium sp. (Clavicipitaceae) are two of the most studied endophytic entomopathogenic fungal genera. However, most fungi that kill insects do not survive in the tissues of living plants. The data published thus far show a high degree of variability and do not provide consistent explanations for the underlying mechanisms that may be responsible for these effects. This implies that available knowledge regarding the colonization of plant tissues by endophytic insect pathogenic fungi, the effects of colonization on plant metabolism, and how this contributes to a decrease in herbivore and pathogens damage is limited. To adequately utilize fungal-based products as biological control agents, these products must be effective and the reduction of pests and infection must be consistent and similar to that of chemical insecticides after application. This article discusses this possibility and highlights the benefits and the specific techniques utilized by endophytically challenged plants in invading insect pests and disease pathogens.
Background:
Although most biological control programs use multiple biological agents to manage pest species, to date only a few programs have combined the use of agents from different guilds. Using sweet pepper (Capsicum annuum L.), the entomopathogenic fungus Akanthomyces muscarius ARSEF 5128, the tobacco peach aphid Myzus persicae var. nicotianae and the aphid parasitoid Aphidius ervi as the experimental model, we explored whether root inoculation with an entomopathogenic fungus is compatible with parasitoid wasps for enhanced biocontrol of aphids.
Results:
In dual-choice behavior experiments, A. ervi was significantly attracted to the odor of M. persicae-infested C. annuum plants that had been inoculated with A. muscarius, compared to non-inoculated infested plants. There was no significant difference in attraction to the odor of uninfested plants. Myzus persicae-infested plants inoculated with A. muscarius emitted significantly higher amounts of indole, (E)-nerolidol, (3E,7E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT) and one unidentified terpene compared to non-inoculated infested plants. Coupled gas chromatography-electroantennography (GC-EAG), using the antennae of A. ervi, confirmed physiological activity of these elevated compounds. Inoculation of plants with A. muscarius did not affect parasitism rate nor parasitoid longevity, but significantly increased the speed of mummy formation in parasitized aphids on fungus-inoculated plants.
Conclusion:
Our data suggest that root inoculation of C. annuum with A. muscarius ARSEF 5128 alters the olfactory-mediated behavior of parasitoids, but has little effect on parasitism efficiency or life history parameters. However, increased attraction of parasitoids towards M. persicae-infested plants when inoculated by entomopathogenic fungi can accelerate host localization and hence improve biocontrol efficacy. This article is protected by copyright. All rights reserved.
Forests form rich biodiversity hubs that act as large reservoirs of natural carbon. The spatial and temporal heterogeneity of these complex habitats of forest floors provides ecological services of immense socio-economic importance. However, these socio-economic ecological hotspots are incessantly exposed to multifarious abiotic, biotic, and anthropogenic disturbances, amongst which unpredictable forest pest (i.e., bark beetle) outbreak account for the loss of vegetation and microbiome of measurable quantum. The importance of the microbiome in forming an inseparable functional unit of every host and shaping its interaction with other partners has been well realized. Interestingly, forest pests, including bark beetles, are also reported to rely on their endosymbiotic microbial partners to manipulate tree defense machinery. In contrast, the microbiome forming the holobiont of trees also regulates the overall function and fitness of the host and significantly contributes to tackling these challenging situations. Nevertheless, how the holobiont of trees directly or indirectly influence beetle holobiont is still an enigma. The present review shall elaborate on the role of microbial tools in enhancing tree performance and fitness, which helps counter beetle damage. Besides, it shall also emphasize exploiting the role of microorganisms in acting as biocontrol agents in shielding the trees against beetle destruction. The application of endosymbiont-mediated RNA interference (RNAi) in working with two-tier specificity for controlling beetle devastations shall be discussed as new-age technological advances. All explanations are expected to put forth the potential of the microbial toolbox in offering better and more sustainable beetle management strategies in the future.
Background
Fungal microbial biocontrol agent playing an important role in sustainable pest management with low cost. Conidial contact with cuticle is sufficient to cause disease in insects by entomopathogenic fungi (EPF) compared to bacteria and viruses which required ingestion of contaminated food. The field level application of fungi resulted inconsistent in their efficacy against insects as they withstand in the agroecosystem with adverse environmental conditions. To overcome this bottleneck, endophytic EPF, Beauveria bassiana (Bals.-Criv.) Vuill. (Cordycipitaceae: Hypocreales), is well-studied for the management of insects of cultivated crops and got promising results. The colonization of endophytic isolates varied from one host plant to another and virulence against insects too. Hence, the study was undertaken to know the colonization of indigenous B. bassiana UHSB-END1 isolate in cabbage plant and its efficacy against major insects of cabbage.
Results
The indigenous isolate of B. bassiana UHSB-END1 was able to colonize cabbage in all the methods of inoculations (seed treatment, seedling root dip, soil drenching, foliar spray and combination treatment) at 30, 45 and 60 days of post-inoculation (dpi). However, the colonization of the fungus inside the cabbage was restricted to tissues of inoculation, and movement from the site of inoculation to other parts of the plant was poor. In the present study, colonization was the highest at 30 dpi in all methods of colonization with restricted colonization to the site of exposure of fungus. Further, in vivo and in planta assay confirmed the effectiveness of B. bassiana UHSB-END1 colonized cabbage against Myzus persicae (Sulzer) and Plutella xylostella (Linnaeus). Under in vivo conditions the maximum mortality of M. persicae and P. xylostella was recorded at 30 dpi. It was decreased slightly at 45 dpi, and the lowest morality was recorded at 60 dpi. In planta experiment also proved better efficacy against both the test insects. Wherein mortality of M. persicae ranged from 22 to 36% five days after release (DAR), it was increased to 48–68% at 10 DAR and reached highest mortality rate at 15DAR (72–96%). Similarly, mortality of P. xylostella ranged from 14 to 24% after five DAR, and it was 27–44% at 10 DAR, and maximum mortality rate of larvae were recorded at 15 DAR (64–96%).
Conclusion
The present study reported 100% colonization of cabbage plant by indigenous B. bassiana UHSB-END1 at 30 dpi in combination of treatment and showed a maximum efficacy in managing the population of major insects of cabbage. Introducing this indigenous isolate will pave a ray of hope in managing the both key insects ( P. xylostella and M. persicae ) in cabbage agroecosystem without disturbing the environment and further helps in production of cabbage with minimum pesticide residue for consumers.
The whitefly Bemisia tabaci is a cosmopolitan, polyphagous agricultural pest that poses serious threats to agricultural production globally. Beauveria bassiana , an entomopathogenic fungi (EPF), cannot only directly kill a variety of pests but also inhibit the occurrence of pests as fungal endophytes within plants. In this study, we explored how the introduction of B. bassiana as endophytes into tomatoes ( Solanum lycopersicum ) affected the fitness and feeding behaviour of whiteflies. The results showed a significant difference in the fertility of B. tabaci on tomatoes treated with B. bassiana by root irrigation, B. bassiana by local leaf spraying, and 0.05% Tween 80 solution, among which the number of eggs laid was the lowest on tomatoes treated with B. bassiana by root irrigation. Furthermore, B. tabaci fed on tomatoes treated with EPF by root irrigation showed a significantly higher mortality rate in each stage than control plants treated with 0.05% Tween 80 by constructing an age-stage, two-sex life table. In addition, the intrinsic rate of increase ( r ), the finite rate of increase ( λ ) and the net reproductive rate ( R 0 ) of the B. tabaci population on tomatoes treated with EPF by root irrigation were all significantly lower than those of the control. Moreover, tomatoes treated by root irrigation had a significant negative effect on the feeding behaviour of B. tabaci by shortening the duration of watery salivation and phloem ingestion. Our results indicated that B. bassiana effectively inhibited the occurrence of whitefly as endophytes. These findings enhanced our understanding of the inhibition of endophytic EPF on pests.
The whitefly Bemisia tabaci is an invasive pest that causes extensive damage to
many vegetable crops and ornamental plants. To control this pest, the release of natural enemies has become increasingly important as an ecologically safe and effective method of biological control. Some species in the family Miridae are effective at controlling whitefly populations, but because they feed on both insect prey and plant tissue, their overall effect on plant performance is not well understood. In this study, the impact of the mirid predator Macrolophus pygmaeus on the morphological and physiological traits of Solanum melongena in the presence of Bemisia tabaci was evaluated. Overall, the results show how the presence of this natural enemy mitigates the damage caused by whitefly infestations. They also help to clarify the multitrophic relationships between plant, pest, and natural enemy, enabling the prediction of plant development in the presence of both pest and predator.
Horticultural production is a vital catalyst for economic growth, yet insect infestations reduce horticultural crop yield and quality. Pesticides and other pest control methods are used during planting to eliminate pests that cause direct and indirect losses. In such situations, endophytic entomo-pathogenic fungi (EEPF) can act as a potential tools for biological control. They protect plants by boosting growth, nutrition, morpho-physiology and salt or iron tolerance. Antixenosis, antibiosis and plant tolerance change insect performance and preferences. EEPF- plant colonisation slows herbivore development, food consumption, oviposition and larval survival. EEPF changes plant physio-chemical properties like volatile emission profile and secondary metabolite production to regulate insect pest defences. EEPF produces chitinases, laccases, amylases, and cellulases for plant defence. Recent studies focused on EEPF species’ significance, isolation, identification and field application. Realizing their full potential is difficult due to insufficient mass production, storage stability and formulation. Genetic-molecular and bioinformatics can help to build EEPF-based biological control systems. Metagenomics helps study microbial EEPF taxonomy and function. Multi-omics and system biology can decode EEPF interactions with host plants and microorganisms. NGS (Next Generation Sequencing), comparative genomics, proteomics, transcriptomics, metabolomics, metatranscriptomics and microarrays are used to evaluate plant-EEPF relationships. IPM requires understanding the abiotic and biotic elements that influence plant-EEPF interaction and the physiological mechanisms of EEPF colonisation. Due to restricted research, there are hundreds of unexplored EEPFs, providing an urgent need to uncover and analyse them.
Whitefly Bemisia tabaci is a polyphagous super pest, which causes serious threat to agricultural production globally. Beauveria bassiana , as entomopathogenic fungi (EPF), can not only directly kill a variety of pests, but also inhibit the occurrence of pests as fungal endophytes within plants. In this study, we explored how the introduction of B. bassiana as endophytes into tomatoes ( Solanum lycopersicum ) affected the fitness and feeding behavior of whitefly. The result showed that there was significant difference in the fertility of B. tabaci on tomatoes treated with B. bassiana by root irrigation, B. bassiana by local leaf spray, and 0.05% Tween 80 solution, among which the number of eggs laid was the lowest on tomatoes treated with B. bassiana by root irrigation. Furthermore, B. tabaci fed on tomatoes treated with EPF by root irrigation showed significantly higher mortality rate in each stage than control plants with 0.05% Tween 80, by constructing the age-stage, two-sex life table. In addition, the intrinsic rate of increase ( r ), the finite rate of increase ( λ ) and the net reproductive rate ( R 0 ) of B. tabaci population on tomatoes treated with EPF by root irrigation were all significantly lower than control. Moreover, tomatoes treated by root irrigation had a significant negative effect on the feeding behavior of B. tabaci , by shortening the watery salivation and phloem ingestion. Our results indicated that B. bassiana effectively inhibited the occurrence of whitefly as endophytes. These findings enhanced our understanding about the inhibition of endophytic EPF on pests.
Microbes are ubiquitous and can associate to colonize plants and exhibits different modes of interactions. Plant beneficial microbes could colonize both the phyllosphere and rhizosphere to promote the various aspect of plant growth and other various compartments in plants. These beneficial microbes are generally called plant growth-promoting microbes (PGPMs), they can become an excellent alternative to remove or reduce the use of various toxic agrochemicals including synthetic chemical fertilizers and biocides. The association of PGPMs provides nutrients, protection against pathogens as well as various environmental stress responses either direct or indirect mechanisms. The soil and rhizosphere microbes beneficially associate either the root surface or phyllosphere region of the plant and influence the growth and health fitness of crops. Some microbes directly interact with the plant to develop a symbiotic relationship (e.g., Rhizobium, mycorrhizal fungi), and few can interact at the surface of the root with either associative symbiosis (Azospirillum) or nonsymbiotic beneficial interactions such as nutrient acquisition, solubilization, and translocation of minerals and water, vitamin and growth hormone synthesis, mineralization of soil organic residues, inhibits harmful pathogens and nematodes, production of iron siderophores to chelate ions, and provide induced resistance against various biotic and abiotic stresses. This chapter describes the basic beneficial microbial interactions on the rhizosphere, phyllosphere, and their beneficial effects on the host for sustainable agriculture, specifically, bacterial nodulation, mycorrhizal infection, microbial endophytes, development of bioinoculums, and their benefits to the plant. Further, the functions of beneficial microbes to the plants and the soil have been discussed. Besides, rhizosphere microbiome engineering and its role in sustainable agriculture have been also discussed.KeywordsBeneficial microbesMicrobiome engineeringPhyllosphere microbial associationRhizosphere microbesSustainable agriculture
Biocontrol with hypocrealean entomopathogenic fungi (EF) is a key tool to develop Integrated Pest Management (IPM) programs for the progressive replacement of synthetic chemical insecticides with more environmentally friendly pest control measures. These fungi stand out among entomopathogens not only for their contact mechanism of infection through the arthropod integument, but also for developing close associations with plants including the endophytic lifestyle and rhizosphere competence that can enable them to make broader contributions to IPM and crop production. Anyhow, the interaction of EF with the plants incorporates multitrophic complexity at different levels including insect pests, plants, and their natural enemies. The aim of the present review was to gather and summarize all available data on multitrophic interactions of EF. These fungi can influence both the chemical ecology of host-plant selection by insect pests and the host or prey selection by parasitoid or predators, respectively. Moreover, EF treatments are compatible with natural enemies in terms of safety and effectiveness, which could allow biocontrol strategies for their synergistic application in IPM programs. A comprehensive understanding of the impact of these multitrophic interactions in longer term, farm-level real-life biocontrol implementation studies will provide new opportunities in plant protection and production.
This book presents topics on the development, improvement and commercialization of fungi for the biological control of pests, weeds and diseases which are of economic importance. Common themes such as production, formulation and application of technologies, biosafety, risk assessment and registration requirements are all covered. The book attempts to bring together scientists, industry and government agencies involved in all aspects of fungal biological control agents for the first time.
Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? An increasing number of recent studies demonstrate that entomopathogenic fungi, often solely considered as insect pathogens, play additional roles in nature, including endophytism, plant disease antagonism, plant growth promotion, and rhizosphere colonization. These newly emerging, but not yet fully understood, ecological roles hint at the possibility that we have been overlooking important attributes in our quest to develop fungal entomopathogens exclusively as inundative biopesticides against insect and other arthropod pests. Such additional roles recently-discovered to be played by entomopathogenic fungi provide opportunities for the multiple use of these fungi in integrated pest management (IPM) strategies. Of particular interest is the ability displayed by various genera of entomopathogenic fungi to colonize a wide variety of plant species in different families, both naturally and artificially following inoculation, and confer protection against not only insect pests but also plant pathogens. This article reviews the literature currently available on the endophytic colonization of different host plants by fungal entomopathogens, and summarizes the negative effects of such colonization on insect pests and plant pathogens that have been reported to date. It also addresses the possible mechanisms of protection conferred by endophytic fungal entomopathogens and explores the potential use of these fungi as dual microbial control agents against both insect and pathogen pests. Moreover, interactions amongst endophytic fungal entomopathogens and other endophytes are discussed. Finally, current limitations and future research directions for the innovative use of endophytic fungal entomopathogens as dual microbial control agents are summarized. [Lara R. Jaber, The University of Jordan and Bonnie H. Ownley, The University of Tennessee; Biological Control, Review article (in Press)].
Two experimental replicates were conducted to test whether strains
of Beauveria brongniartii (BIPESCO2 and 2843) and Metarhizium
brunneum (BIPESCO5) can endophytically colonise Vicia faba
plants and improve their growth by comparing them with an
endophytic strain of B. bassiana (NATURALIS®). The plants were
inoculated through foliar spray and the effect of inoculation on
plant height, leaf pair number, fresh root and shoot weights was
measured at 7 and 14 days post inoculation (dpi). Endophytic
colonisation of different plant parts with the tested fungal strains
were confirmed 7 and 14 dpi through re-isolation of inoculated
fungi onto selective media and subsequent Simple Sequence
Repeat (SSR) marker-based genetic identification. All tested strains
were able to endophytically colonise leaves, stems, and even roots
of inoculated plants 7 and 14 dpi, but per cent colonisation varied
significantly among strains and plant parts within each sampling
date. Foliar inoculation of plants with the tested strains increased
plant height, leaf pair number, fresh shoot and root weights;
however the increase was not always consistent across sampling
dates in both experimental replicates. This study provides the first
evidence for the endophytic colonisation of plants with two
strains of B. brongniartii, an important biocontrol agent of
Melolontha melolontha and other scarab beetles in several
European countries, and thus extends previous reports on the
ability of entomopathogenic fungi to act as endophytes. It also
presents possible explanations for the lack of consistency in the
plant growth promotion obtained by the foliar inoculation of
entomopathogenic fungi.
The effect of increased duration of seed treatment with two fungal entomopathogens, Beauveria bassiana (NATURALIS) and Metarhizium brunneum (BIPESCO5), on the growth and colonization of broad bean (Vicia faba) was assessed in two replicate greenhouse experiments. The plants were inoculated by soaking seeds in a concentration of 1 × 10⁷ conidia ml⁻¹ of each of the two fungal strains or in sterile distilled water containing 0.1% Tween 80 for 2, 8, and 16 h. Percent seed germination and seedling emergence as well as primary root length were determined seven days post inoculation. Effects of fungal strain and seed treatment duration on plant height, number of leaf pair, fresh root and shoot weight were measured 14 and 28 days post inoculation. Seed treatment with either fungal strain significantly enhanced almost all measured plant growth parameters. Overall, plant growth was also significantly enhanced as seed treatment duration increased; irrespective of fungal strain. Percent colonization of different plant parts (root, leaf, and stem) sampled 14 and 28 days post inoculation increased as the duration of seed treatment increased as well. The increase in colonization rate due to increased seed treatment duration varied significantly among plant parts, but not among both sampling dates. Our study demonstrates that M. brunneum can systemically colonize different plant parts and improve plant growth when applied as a seed treatment. This was also confirmed for the well-known endophytic B. bassiana strain used in this study. Our results also provide the first report for the effect of increased duration of seed treatment with both endophytic fungal entomopathogens on plant growth enhancement.
Effects of the fungal endophytes Beauveria bassiana (isolates ICIPE 279, G1LU3, S4SU1) and Hypocrea lixii (isolate F3ST1) on the life-history of Phaedrotoma scabriventris and Diglyphus isaea, parasitoids of the pea leafminer Liriomyza huidobrensis, were studied in the laboratory. Parasitoids were allowed to parasitize 2nd and 3rd instar L. huidobrensis larvae reared on endophytically-inoculated faba bean, Vicia faba. In the control, parasitoids were reared on non-inoculated host plants. Parasitism, pupation, adult emergence and survival were recorded. No significant difference was observed between the control and the endophyte-inoculated plants in terms of parasitism rates of P. scabriventris (p = 0.68) and D. isaea (p = 0.45) and adult' survival times (p = 0.06). The survival period of the F1 progeny of P. scabriventris was reduced (p<0.0001) in B. bassiana S4SU1 to 28 days as compared to more than 40 days for B. bassiana G1LU3, ICIPE 279 and H. lixii F3ST1. However, no significant difference (p = 0.54) was observed in the survival times of the F1 progeny of D. isaea. This study has demonstrated that together, endophytes and parasitoids have beneficial effects in L. huidobrensis population suppression.
It is now evident that entomopathogenic fungi are able to colonize plant tissues as symptomless endophytes. Although most data so far published in this regard refer to Beauveria bassiana as an endophytic fungus, two other entomopathogenic fungi, viz. Metarhizium anisopliae and Lecanicillium lecanii have also been shown to colonize plant tissues endophytically. Several recent studies have also shown reasonable detrimental effects on herbivorous insects feeding on plants harbouring these fungi as endophytes. However, data published so far are highly variable and not consistent with regard to the underlying mechanisms which would allow explaining these effects. Growth conditions, specific cultivar features, or interactions with other microorganisms may impact the effect of these endophytic entomopathogenic fungi on the herbivorous insects. Furthermore, other fungi may block the systemic growth of the fungi in plant parts distant to the point of inoculation. Other parameters which need to be taken into account for using these fungi as biocontrol agents are the level of mycotoxins produced in plants, the level of pest reduction and the nature of formulations allowing a consistent colonization of the crop plants. This review discusses these and other problems related to the use of entomopathogenic fungi as endophytic biocontrol agents.
Aphidius colemani Viereck (Hymenoptera: Braconidae) is a solitary endoparasitoid used for biological control of many economically important pest aphids. Given its widespread use, a vast array of literature on this natural enemy exists. Though often highly effective for aphid suppression, the literature reveals that A. colemani efficacy within greenhouse production systems can be reduced by many stressors, both biotic (plants, aphid hosts, other natural enemies) and abiotic (climate and lighting). For example, effects from 3rd and 4th trophic levels (fungal-based control products, hyperparasitoids) can suddenly decimate A. colemani populations. But, the most chronic negative effects (reduced parasitoid foraging efficiency, fitness) seem to be from stressors at the first trophic level. Negative effects from the 1st trophic level are difficult to mediate since growers are usually constrained to particular plant varieties due to market demands. Major research gaps identified by our review include determining how plants, aphid hosts, and A. colemani interact to affect the net aphid population, and how production conditions such as temperature, humidity and lighting affect both the population growth rate of A. colemani and its target pest. Decades of research have made A. colemani an essential part of OPEN ACCESS Insects 2015, 6 539 biological control programs in greenhouse crops. Future gains in A. colemani efficacy and aphid biological control will require an interdisciplinary, systems approach that considers plant production and climate effects at all trophic levels.
Fungal endosymbionts in plants may influence interactions among plants, herbivores and their parasitoids through the production of secondary metabolites. We used a lepidopteran pest and its generalist parasitoid to test the effect of endophyte-infected plants on a third trophic level. Endophytic fungi, Aspergillus flavus and Aspergillus niger, isolated from Acacia arabica, were used to infect cauliflower plants. We found that the presence of the endophyte in the plants significantly extended the development period of Spodoptera litura (Fab.) larvae. Feeding of the host on endophyte-infected plants further adversely affected the development and performance of its parasitoid, Bracon hebetor (Say). A negative impact was also recorded for longevity and fecundity of endophyte-naive parasitoid females due to the parasitization of host larvae fed on endophyte-infected plants. The presence of endophytes in the diet of the host larvae significantly prolonged the development of the parasitoid. A strong detrimental effect was also recorded for larval survival and emergence of parasitoid adults. The longevity and parasitism rate of female wasps were reduced significantly due to the ingestion of endophyte-infected cauliflower plants by S. litura larvae. Overall, we found that both endophytic fungi had a negative impact on the parasitoid.
A study was conducted to examine whether Beauveria
bassiana (Balsamo) Vuillemin (Ascomycota: Hypocreales) can colonize grapevine leaf tissues and subsequently confer protection against downy mildew caused by Plasmopara viticola (Berk. and Curt.) Berl. and de Toni. Following the foliar inoculation of plants with conidial suspensions of selected B. bassiana strains, colonization of leaves by the fungus was determined using culture-based and PCR techniques at different time intervals. Seven days following B. bassiana inoculation, grapevine plants were challenged with P. viticola and symptoms were assessed by calculating the disease incidence and severity. Although all tested strains were able to colonize grapevine plants, percent colonization differed significantly among strains. Disease incidence and severity were, on the other hand, significantly reduced in B. bassiana-inoculated plants compared to control plants irrespective of strain. This study is one of very few studies investigating the promising role B. bassiana could play as a plant disease antagonist.
Biological control of pests in agroecosystems could be enhanced by combining multiple natural enemies. However, this approach might also compromise the control efficacy through intraguild predation (IGP) among the natural enemies. Parasitoids may be able to avoid the risk of unidirectional IGP posed by entomopathogenic fungi through selective oviposition behavior during host foraging. Trybliographa rapae is a larval parasitoid of the cabbage root fly, Delia radicum. Here we evaluated the susceptibility of D. radicum and T. rapae to two species of generalist entomopathogenic fungi, Metarhizium brunneum isolate KVL 04-57 and Beauveria bassiana isolate KVL 03-90. Furthermore, T. rapae oviposition behavior was assessed in the presence of these entomopathogenic fungi either as infected hosts or as infective propagules in the environment. Both fungi were pathogenic to D. radicum larvae and T. rapae adults, but with variable virulence. When host patches were inoculated with M. brunneum conidia in a no-choice situation, more eggs were laid by T. rapae in hosts of those patches compared to control and B. bassiana treated patches. Females that later succumbed to mycosis from either fungus laid significantly more eggs than non-mycosed females, indicating that resources were allocated to increased oviposition due to perceived decreased life expectancy. When presented with a choice between healthy and fungal infected hosts, T. rapae females laid more eggs in healthy larvae than in M. brunneum infected larvae. This was less pronounced for B. bassiana. Based on our results we propose that T. rapae can perceive and react towards IGP risk posed by M. brunneum but not B. bassiana to the foraging female herself and her offspring. Thus, M. brunneum has the potential to be used for biological control against D. radicum with a limited risk to T. rapae populations.
Endophytic fungi may display preferential tissue colonization within their plant hosts. Here we tested if the endophytic, insect pathogenic fungi (EIPF) Metarhizium and Beauveria showed preferential localization within plant tissues, in the field and under laboratory conditions. In the field, plants were sampled from three separate sites (Brock University, St. Catharines, Ontario; Pelham, Ontario; and Torngat Mountains National Park, Newfoundland, Canada) and EIPF were isolated from plant roots, the hypocotyl, and stem and leaves. Two genera of EIPF, Metarhizium spp. and Beauveria bassiana, were isolated from plants sampled, as well as the nematophagous fungus, Pochonia chlamydosporium. Metarhizium spp. were almost exclusively found in roots, whereas B. bassiana and P. chlamydosporium were found throughout the plant. The Metarhizium species were identified by RFLP and 95 % were Metarhizium robertsii, 4.3 % were M. brunneum, and 0.7 % were M. guizhouense. Lab studies with M. robertsii and B. bassiana reflected observations found in the field, that is, Metarhizium was restricted to the roots of plants while B. bassiana was found throughout the plant. Insect infection by these EIPF is preferential with respect to above and below ground insects, and the present study correlates above and below ground insect infections with endophytic colonization by these EIPF.
We investigated the potential of endophytic Beauveria bassiana to provide protection against Zucchini yellow mosaic virus (ZYMV), one of the most economically important viral diseases in cucurbits. Four selected B. bassiana strains were able to successfully colonise squash plants following foliar inoculation with the conidial suspension of each respective strain. However, no significant difference in percentage colonisation was observed among the tested B. bassiana strains. Disease incidence (percentage of plants showing ZYMV symptoms) and severity (rating based on a 5-point scale), sampled weekly for four weeks following the challenge inoculation of plants with ZYMV, were significantly lower in B. bassiana-inoculated plants as compared to control plants, regardless of the inoculated strain. This is, to our knowledge, the first report on the potential of endophytic B. bassiana to confer protection against plant viruses. Further studies should be conducted to determine whether such endophytic B. bassiana-mediated protection against ZYMV in squash extends to other cucurbits.
The effects of two entomopathogenic fungal endophytes, Beauveria bassiana and Purpureocillium lilacinum (formerly Paecilomyces lilacinus), were assessed on the reproduction of cotton aphid, Aphis gossypii Glover (Homoptera:Aphididae), through in planta feeding trials. In replicate greenhouse and field trials, cotton plants (Gossypium hirsutum) were inoculated as seed treatments with two concentrations of B. bassiana or P. lilacinum conidia. Positive colonization of cotton by the endophytes was confirmed through potato dextrose agar (PDA) media plating and PCR analysis. Inoculation and colonization of cotton by either B. bassiana or P. lilacinum negatively affected aphid reproduction over periods of seven and 14 days in a series of greenhouse trials. Field trials were conducted in the summers of 2012 and 2013 in which cotton plants inoculated as seed treatments with B. bassiana and P. lilacinum were exposed to cotton aphids for 14 days. There was a significant overall effect of endophyte treatment on the number of cotton aphids per plant. Plants inoculated with B. bassiana had significantly lower numbers of aphids across both years. The number of aphids on plants inoculated with P. lilacinum exhibited a similar, but non-significant, reduction in numbers relative to control plants. We also tested the pathogenicity of both P. lilacinum and B. bassiana strains used in the experiments against cotton aphids in a survival experiment where 60% and 57% of treated aphids, respectively, died from infection over seven days versus 10% mortality among control insects. Our results demonstrate (i) the successful establishment of P. lilacinum and B. bassiana as endophytes in cotton via seed inoculation, (ii) subsequent negative effects of the presence of both target endophytes on cotton aphid reproduction using whole plant assays, and (iii) that the P. lilacinum strain used is both endophytic and pathogenic to cotton aphids. Our results illustrate the potential of using these endophytes for the biological control of aphids and other herbivores under greenhouse and field conditions.
Metarhizium species have recently been found to be plant rhizosphere associates as well as insect pathogens. Because of their abundance, rhizospheric Metarhizium could have enormous environmental impact, with co-evolutionary implications. Here, we tested the hypothesis that some Metarhizium spp. are multifactorial plant growth promoters. In two consecutive years, corn seeds were treated with entomopathogenic Metarhizium spp. and field tested at the Beltsville Facility in Maryland. Seed treatments included application of green fluorescent protein (GFP)-tagged strains of Metarhizium brunneum, Metarhizium anisopliae, Metarhizium robertsii, and M. robertsii gene disruption mutants that were either avirulent (Δmcl1), unable to adhere to plant roots (Δmad2), or poorly utilized root exudates (Δmrt). Relative to seeds treated with heat-killed conidia, M. brunneum, M. anisopliae, and M. robertsii significantly increased leaf collar formation (by 15, 14, and 13 %), stalk length (by 16, 10, and 10 %), average ear biomass (by 61, 56, and 36 %), and average stalk and foliage biomass (by 46, 36, and 33 %). Their major impact on corn yield was during early vegetative growth by allowing the plants to establish earlier and thereby potentially outpacing ambient biotic and abiotic stressors. Δmcl1 colonized roots and promoted plant growth to a similar extent as the parent wild type, showing that Metarhizium populations are plant growth promoters irrespective of their role as insect pathogens. In contrast, rhizospheric populations and growth promotion by Δmrt were significantly reduced, and Δmad2 failed to colonize roots or impact plant growth, suggesting that colonization of the root is a prerequisite for most, if not all, of the beneficial effects of Metarhizium.
The peach–potato aphid Myzus persicae (Sulzer) can resist a wide range of insecticides, but until recently (1990) the only mechanism identified was the increase production of carboxylesterases (E4 or FE4), which cause enhanced degradation and sequestration of insecticidal esters. W have now identified two forms of target–site resistance involving changes in the acetylcholinesterase (AChE) and sodium channel (kdr) genes. Biochemical and DNA diagnostic methods can be used to identify all three mechanisms in individual aphids, and thereb establish their spatial distributions and temporal dynamics. Amplified genes underlie the increased production of esterase but their expression is modulated by DNA methylation. Amplification of the E4 gene is in strong linkage disequilibrium with the kdr mechanism. This may reflect strong insecticidal selection favourin aphids with multiple mechanisms, tight chromosomal linkage and/or the prominence of parthenogenesis in many M. persicae populations. The decreased fitness of resistant aphids under winter conditions may be a consequence of the altered sodium–channe gene affecting behaviour and/or the perception of external stimuli.
Ten fungal isolates belonging to the genera Beauveria (3), Hypocrea (1), Gibberella (1), Metarhizium (2), Trichoderma (1) and Fusarium (2) were evaluated in the laboratory to determine whether they could become endophytic in two pea leafminer (Liriomyza huidobrensis) host plants (Vicia faba and Phaseolus vulgaris), and to assess their possible negative effects on leafminers. Beauveria (ICIPE279), Hypocrea, Gibberella, Fusarium and Trichoderma isolates colonized roots, stems and leaves of both host plant species. Beauveria isolates G1LU3 and S4SU1 colonized roots, stems, and leaves of P. vulgaris but only the root and stem of V. faba. Isolates of Metarhizium failed to colonize the two host plants. The effects of endophytically colonized fungal pathogens on mortality, oviposition, emergence and longevity of L. huidobrensis were investigated after endophytic colonization of V. faba plants. All the fungal isolates that succeeded in colonizing the host plant were pathogenic to L. huidobrensis, causing 100 % mortality within 13.2 ± 0.7–15.0 ± 0.6 d. However, Hypocrea outperformed the other isolates (p < 0.0 001) in reducing longevity of the progeny (11.2 ± 1.0 vs. 17.8 ± 1.4 d in the control), the number of pupae (80.0 ± 6.7 vs. 387.0 ± 21.7 pupae in the control), and adult longevity (3.8 ± 1.0 vs. 9.9 ± 1.8 d in the control). Adult emergence was significantly reduced (p < 0.0 001) in Hypocrea (21.4 %) and Beauveria (38.0 %) treatments compared to the control (82.9 %).
Variation in plant quality has an impor-tant impact on insect growth and development and there is considerable evidence that plants can also influence an insect's natural enemies. Here we discuss the potential for plant-mediated effects on fungal entomopathogens. Fungi differ from other insect pathogens in that they infect an insect directly through its cuticle. This means that they are partic-ularly vulnerable to changes in microclimate and properties of the insect cuticle. Potential direct and indirect mechanisms for plant-mediated effects on fungal entomopathogens are discussed. It is clear from these studies that fungal entomopathogens could be affected by plant volatiles and plant surface chemistry. Plant secondary chemicals can also inhibit fungal growth, potentially protecting the insect herbivore. However, the site of action and the mechanism behind these effects in plant-based stud-ies is not always clear. The implications for biocon-trol using fungal entomopathogens are discussed.
Field experiments in Canterbury, New Zealand, investigated four levels of interaction involving the clavicipitaceous endophytic fungi Neotyphodium lolii measured as ppm of the alkaloid peramine in bulked samples of Lolium perenne, the weevil pest Listronotus bonariensis, and its braconid parasitoid Microctonus hyperodae. Weevil numbers were unusually low and the expected inverse relationship between ground densities and peramine concentration was not observed. There was, however, a highly significant tritrophic interaction whereby percent parasitism was inversely related to ppm of peramine. Possible mechanisms for this interaction are discussed and it is suggested that it may have been the result of reduced feeding intensity of L. bonariensis that led to a corresponding reduction in opportunity for the parasitoid to attack.
The present study aimed to evaluate the effect of the inoculation with Metarhizium anisopliae on the growth of tomato plants and to determine the endophytic activity of this fungus. The three isolates of M. anisopliae evaluated (Ma 8, Ma 10 and Ma 20) significantly increased plant height, root length, shoot and root dry weight when compared to the untreated control, although the response obtained depended on the isolate and the inoculation rate. In addition, the three isolates showed endophytic activity and were isolated from roots and shoots. Ma 8 was also found in leaves. This study reveals significant new data on the interaction between M. anisopliae and plants although there is a need for further research to understand the mechanisms through which M. anisopliae promotes plant growth.
Plant secondary chemicals can alter herbivore suitability for parasitoids by weakening or stunting the host, delaying its
development, or when larval parasitoids encounter ingested phytotoxins in the body of their host. Experiments with different
parasitoids that exploit the same host species feeding on the same plant may provide insight about how parasitoid life history
affects the strength of such interactions. The encyrtid wasp Copidosoma bakeri, a slow-developing polyembryonic egg-larval parasitoid, and the tachinid fly Linnaemya comta, a fast-developing solitary species, both parasitize Agrotis ipsilon, a generalist noctuid. We tested the hypothesis that of the two parasitoid species, the encyrtid, because of its more prolonged
developmental association with the host, would suffer greater fitness costs when A. ipsilon feeds on perennial ryegrass containing an alkaloid-producing fungal endophyte. Indeed, fewer parasitized cutworms yielded
C. bakeri broods, and those host mummies were smaller, formed more slowly, and contained fewer adults when the hosts fed on endophytic
as opposed to endophyte-free grass. In contrast, L. comta fitness parameters were similar regardless of the type of grass upon which their host fed. Our results highlight that the
outcome of endophyte-mediated tritrophic interactions may differ for different parasitoid species. Implications for integrating
the use of endophytic grasses and biological control are discussed.
KeywordsLife history strategy–
Neotyphodium
–Tritrophic interactions–Parasitoids–Tachinidae–Encyrtidae
A substantial number of mycoinsecticides and mycoacaricides have been developed worldwide since the 1960s. Here we present an updated, comprehensive list of these products. At least 12 species or subspecies (varieties) of fungi have been employed as active ingredients of mycoinsecticides and mycoacaricides for inundative and inoculative applications, although some are no longer in use. Products based on Beauveria bassiana (33.9%), Metarhizium anisopliae (33.9%), Isaria fumosorosea (5.8%), and B. brongniartii (4.1%) are the most common among the 171 products presented in this paper. Approximately 75% of all listed products are currently registered, undergoing registration or commercially available (in some cases without registration), whereas 15% are no longer available. We were unable to determine the status of the remaining 10%. Insects in the orders Hemiptera, Coleoptera, Lepidoptera, Thysanoptera, and Orthoptera comprise most of the targets, distributed among at least 48 families. A total of 28 products are claimed to control acarines (mites and ticks) in at least 4 families, although only three products (all based on Hirsutella thompsonii) were exclusively developed as acaricides. Eleven different technical grade active ingredients or formulation types have been identified, with technical concentrates (fungus-colonized substrates) (26.3%), wettable powders (20.5%) and oil dispersions (15.2%) being most common. Approximately 43% of all products were developed by South American companies and institutions. Currently, what may be the largest single microbial control program using fungi involves the use of M. anisopliae for control of spittlebugs (Cercopidae) in South American sugarcane and pastures.
An important mechanism for insect pest control should be the use of fungal entomopathogens. Even though these organisms have been studied for more than 100 y, their effective use in the field remains elusive. Recently, however, it has been discovered that many of these entomopathogenic fungi play additional roles in nature. They are endophytes, antagonists of plant pathogens, associates with the rhizosphere, and possibly even plant growth promoting agents. These findings indicate that the ecological role of these fungi in the environment is not fully understood and limits our ability to employ them successfully for pest management. In this paper, we review the recently discovered roles played by many entomopathogenic fungi and propose new research strategies focused on alternate uses for these fungi. It seems likely that these agents can be used in multiple roles in protecting plants from pests and diseases and at the same time promoting plant growth.
Claims about the role of predator diversity in maintaining ecosystem function and providing ecosystem services such as pest control are controversial, but evaluative tests are beginning to accumulate. Empirical and experimental comparisons of species-rich versus species-poor assemblages of entomophagous arthropods and vertebrates range from strong suppression to facilitative release of herbivorous arthropod prey. Top-down control can be strengthened when natural enemies complement each other, dampened by negative interactions, balanced by both factors, and driven by single luential species. A meta-analytic synthesis shows a significant overall effect of enemy richness increasing top-down control of herbivores, which is consistent in agricultural studies conducted in tropical versus temperate zones, in studies using caged versus open-field designs, but not so in nonagricultural habitats. Synthetic analyses address theory and help set precautionary policy for conserving ecological services broadly, while characterizing uncertainty associated with herbivore response to changes in enemy diversity.
The relationships between the predatory mites, Amblyseius swirskii (Athias-Henriot) and Neoseiulus cucumeris (Oudemans) (Acari: Phytoseiidae), and their prey, western flower thrips (Frankliniella occidentalis Pergande) (Thysanoptera: Thripidae), were investigated to determine the effects of predation on intra-guild or extra-guild prey and predator preference. Life history characteristics of both predatory mites were measured when fed eggs and larvae of the other predator species and compared to data obtained when the predators were fed thrips larvae. In addition, choice tests were conducted to determine if the predators had a preference for different prey or if they were indiscriminate predators. Amblyseius swirskii appears to be an important intra-guild predator of N. cucumeris juveniles because of a high predation rate and a preference for N. cucumeris juveniles over thrips. Neoseiulus cucumeris is also an intra-guild predator of A. swirskii juveniles; however, it has a lower predation rate than A. swirskii. Contrary to intra-guild predation theory, intra-guild prey was an equally good or better food source than thrips (extra-guild prey) for both predators, based on high oviposition rates and fast development times. The results of this study indicate a high potential for negative interactions between A. swirskii and N. cucumeris when used together in biological control of thrips.
Field trials were carried out for two seasons in two sites (Sagana and Naromoru, Central province of Kenya) to evaluate the prospects of endophyte isolates of Beauveria bassiana (Balsamo) Vuillemin G1LU3 and Hypocrea lixii Patouillard F3ST1 for the control of Liriomyza leafminer in common bean Phaseolus vulgaris L. crops through seeds inoculation. Autodissemination device (AD) treated with conidia of Metarhizium anisopliae (Metschnikoff) Sorokin ICIPE 20 was also added as a treatment. Leafminer infestation was not significantly different during the first season but was higher in the controls than in endophtyte treatments at both sites during the second season. Three key Liriomyza species [(L. huidobrensis Blanchard, L. sativae Blanchard and L. trifolii (Burgess)] and six parasitoid species [(Opius dissitus Muesebeck, Phaedrotoma scabriventris Nixon, Diglyphus isaea Walker, Neochrysocharis formosa Westwood, Hemiptarsenus varicornis Girault and Halticoptera arduine (Walker)] were identified during the trials. Leafminer infestation, number of pupae, leafminer flies and parasitoids emergence and yield were the parameters evaluated. Both isolates successfully colonized different parts of P. vulgaris plants, although the colonization was higher with H. lixii F3ST1 than B. bassiana G1LU3 at both sites. The mean number of pupae from the infested leaves varied between 141–252 and 331–416 in endophyte and control treatments, respectively, during the first season and from 110–223 to 366–523, respectively, in endophyte and control treatments during the second season. There were no significant differences among the treatments in the number of parasitoids that emerged from pupae. Higher yield of P. vulgaris seeds was obtained in endophyte than in control treatments. The inclusion of AD treatment did not have significant effect on all the parameters evaluated, except yield. Results of the present study suggest that both fungal isolates hold potential for pest management and could be considered for the control of leafminer flies. However, there is the need to confirm these results on large-scale trials.
The current work reports how spray application of entomopathogenic fungi on alfalfa, tomato and melon plants may cause an additional Spodoptera littoralis larvae mortality due to a temporal colonization of the leaves and subsequent ingestion of those leaves by the larvae. Most entomopathogenic fungi (EF) (Ascomycota: Hypocreales) endophytes seem to colonize their host plants in a non-systemic pattern, in which case at least a transient endophytic establishment of the fungus should be expected in treated areas after spray application. In this work, all strains were able to endophytically colonize roots, stems and leaves during the first 96 h after inoculation. Whilst the treatment of S. littoralis larvae with a 108 ml−1 conidial suspension resulted in moderate to high mortality rates for the Metarhizium brunneum EAMb 09/01-Su (41.7–50.0%) and Beauveria bassiana EABb 01/33-Su (66.7–76.6%) strains, respectively, an additive effect was detected when these larvae were also fed endophytically colonized alfalfa, tomato, and melon leaves, with mortality rates varying from 25.0% to 46.7% as a function of the host plant and total mortality rates in the combined treatment of 75–80% and 33–60% for B. bassiana and M. brunneum, respectively. Fungal outgrowth was not detected in any of the dead larvae feeding on colonized leaves, whereas traces of destruxin A were detected in 11% of the insects fed tomato discs endophytically colonized by M. brunneum. The combined effects of the fungal spray with the mortality caused by the feeding of insects on transient EF-colonized leaves have to be considered to estimate the real acute impact of field sprays with entomopathogenic fungi on chewing insects.
The suppression of agricultural pests has often been proposed as an important service of natural enemy diversity, but few experiments have tested this assertion. In this study we present empirical evidence that increasing the richness of a particular guild of natural enemies can reduce the density of a widespread group of herbivorous pests and, in turn, increase the yield of an economically important crop. We performed an experiment in large field enclosures where we manipulated the presence/absence of three of the most important natural enemies (the coccinellid beetle Harmonia axyridis, the damsel bug Nabis sp., and the parasitic wasp Aphidius ervi) of pea aphids (Acyrthosiphon pisum) that feed on alfalfa (Medicago sativa). When all three enemy species were together, the population density of the pea aphid was suppressed more than could be predicted from the summed impact of each enemy species alone. As crop yield was negatively related to pea aphid density, there was a concomitant non-additive increase in the production of alfalfa in enclosures containing the more diverse enemy guild. This trophic cascade appeared to be influenced by an indirect interaction involving a second herbivore inhabiting the system – the cowpea aphid, Aphis craccivora. Data suggest that high relative densities of cowpea aphids inhibited parasitism of pea aphids by the specialist parasitoid, A. ervi. Therefore, when natural enemies were together and densities of cowpea aphids were reduced by generalist predators, parasitism of pea aphids increased. This interaction modification is similar to other types of indirect interactions among enemy species (e.g. predator–predator facilitation) that can enhance the suppression of agricultural pests. Results of our study, and those of others performed in agroecosystems, complement the broader debate over how biodiversity influences ecosystem functioning by specifically focusing on systems that produce goods of immediate relevance to human society.
We provide evidence that the symbiosis of fungal endophyte and plant host should only be defined in the broad sense as originally used by De Bary to mean the living together of organisms of different species. Using endophytic fungi that were isolated from healthy plant tissue, we tested for the potential pathogenicity of the fungal isolates and did physiological experiments to understand the endophyte-host association. Due to the variability of the interaction with respect to the role of the endophyte and with respect to the physiological status of both partners, only a definition of symbiosis that does not specify the advantages and disadvantages for the individual partners can accurately describe this interaction.
Various endophytic fungi of native plants and crops are important entomopathogens. The objective of this study was to investigate the entomopathogenic action of Beauveria bassiana (Balsamo) Vuillemin, Metarhizium robertsii (Metchnikoff) Sorokin, and Isaria fumosorosea (Wize) Brown & Smith (all Ascomycota: Hypocreales) against larvae of Sesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae) artificially introduced into Sorghum bicolor L. (Moench) (Poaceae) plants under natural environmental conditions. Sorghum bicolor is an economically important crop cultivated for grain, fiber, forage, and lately for biofuel, and S. nonagrioides is its main pest in Mediterranean areas. Young sorghum plants were inoculated with the entomopathogens by spraying in the field. Plant water status, chlorophyll concentration, photosynthesis, and transpiration were not affected. Thirty days after endophyte establishment, plants were infested with fourth instars of S. nonagrioides. The endophytes prevented 50–70% of larvae from entering stalks. Larval mortality was 70–100% and tunnel lengths were reduced by 60–87%. Larval infestation resulted in reduced electron transport capacity and net photosynthetic rate, which was ameliorated in the presence of I. fumosorosea and reversed by B. bassiana and M. robertsii. The growth of sorghum was unaffected in all treatments during the experimental period. Beauveria bassiana and M. robertsii can protect sweet sorghum from damage induced by S. nonagrioides under natural environmental conditions without affecting plant physiology and growth.
Beauveria bassiana ([Balsamo] Vuillemin [Ascomycota: Hypocreales] Botanigard 22WP® formulation]) shows potential as a bee-vectored microbial control agent for control of insect pests on greenhouse tomato and sweet pepper. To integrate this control strategy with existing beneficials used in greenhouse vegetable production, it is important to determine the impact of bee vectored Beauveria on commonly used biocontrol agents in greenhouse crops. Therefore, greenhouse trials were conducted to investigate the impact of bee-vectored B. bassiana on the survivorship and parasitism/predation level of Encarsia formosa Gahan (Hymenoptera: Aphelinidae), Eretmocerus eremicus Rose & Zolnerowich (Hymenoptera: Aphelinidae), Aphidius colemani Viereck (Hymenoptera: Braconidae), Orius insidiosus (Say) (Heteroptera: Anthocoridae) and Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae). Two treatments were evaluated: (bee-vectored inoculum [1.37 × 1010 conidia/g of inoculum] and a control [bees but no inoculum]). The experimental design was a completely randomized block design with three to four replications per treatment over time. The commercial bumblebee pollinator, Bombus impatiens (Cresson) (Hymenoptera: Apidae), was used to vector the microbial control agent to the crop. Over 95% of the flower and leaf samples from the tomato and sweet pepper crops contained detectable levels of Beauveria spores. No significant differences in mortalities were found between the two treatments for the parasitoid species and A. swirskii. Mortality for O. insidiosus was significantly greater in the Beauveria treatment compared to the control treatment. Parasitism and predation levels were not significantly different between to the two treatments. Also, Beauveria did not significantly impact bee mortality compared to the control treatment. Thus, based on the results presented in the current study, bee vectoring of the entomopathogen, B. bassiana, should be compatible with many of the beneficial arthropod control agents that are used in greenhouse integrated pest management.
Most terrestrial plants harbor endophytic fungi, and many of them could directly or indirectly influence insect behavior and community structures by altering plant defense mechanisms. Therefore we evaluated the systemic effects of endophyte seed treatment on aphid population growth rate, offspring performance and fecundity and its effects on Vicia faba in response to aphid feeding. Overall, endophyte treated fava beans had a significantly lower number of Acyrthosiphon pisum when compared to the untreated controls. The highest reduction effects were observed among plants treated with Trichoderma asperellum, Gibberella moniliformis and Beauveria bassiana isolates, while all Metarhizium anisioplaie and Hypocrea lixi isolates had the least effects on A. pisum population growth. Similarly, endophyte seed treatment had a detrimental effect on offspring fitness, development and fecundity. Irrespective of aphid species, the birth rate of all offspring arising from females fed on endophyte treated plants for two generations were significantly lower than those arising from females fed on control plants. As a result, all endophyte treated plants had between 1.6–14.6 and 3.7–11.0 times less number of Aphis fabae and A. pisum nymphs, respectively, compared to untreated controls at the final assessment day. Concurrently, endophyte seed treatment enhanced seedling survivorship with a survival rate of 20–100% compared to none in the control treatment at 20 days post infestation. The present study demonstrates that endophyte seed treatment can offer a protective role by enhancing the competitiveness of V. faba towards aphids, which can be manipulated as a tool in IPM systems.
Some 32 species of endophytic fungi were isolated from the stems of Salicornia perennis. Pleospora salicorniae colonized most parts of the plants; P. bjorlingii was mostly confined to old plant tissue. Two species of Stagonospora were largely confined to new plant tissue. A multiple regression model revealed that P. salicorniae, 2 species of Stagonospora and to a lesser extent Diplodina salicorniae mainly account for the colonization of new tissues. -from Authors
Fungal entomopathogens can directly regulate populations of various insects. The entomopathogen Beauveria bassiana can also endophytically colonize various plants. Endophytic colonization by entomopathogens might be more widespread than currently realized and may provide a source of indirect interactions between fungi and insects. We tested whether some common entomopathogens could colonize six crop plants. We also assessed whether the performance of two insects, Aphis gossypii and Chortoicetes terminifera, was affected by entomopathogens in plants. The entomopathogens B. bassiana, Lecanicillium lecanii and Aspergillus parasiticus individually colonized the leaves of all six crop plants when inoculated as conidia. L. lecanii also readily colonized five different cultivars of cotton. When the entomopathogens were present in the soil in which either cotton or wheat seedlings were grown, A. parasiticus was subsequently isolated from the leaves, stem and roots of both plants and B. bassiana from the leaves, stem and root of wheat only, whereas L. lecanii failed to colonize either plant through the soil. Of the three entomopathogens tested, endophytic presence of A. parasiticus reduced growth of cotton, but none reduced growth of wheat. Feeding by A. gossypii on cotton leaves colonized by either B. bassiana or L. lecanii slowed aphid reproduction, and consumption of wheat leaves colonized by either B. bassiana or A. parasiticus slowed the growth of C. terminifera nymphs. The life cycle of at least three entomopathogens potentially includes plants. The presence of entomopathogens as endophytes can influence growth and fecundity of insect herbivores, suggesting a possible role for endophytic entomopathogens in the regulation of insect populations.
Two commercially-marketed natural enemies of Frankliniella occidentalis (Pergande), a phytoseiid mite, Amblyseius (=Typhlodromips) swirskii (Athias-Henriot), and an anthocorid bug, Orius insidiosus (Say), were evaluated for their compatibility on cut roses, Rosa hybrida L. cv. ‘Tropicana’. Our goal was to evaluate the degree to which intraguild predation of A. swirskii by O. insidiosus could affect suppression of F. occidentalis. We conducted laboratory experiments to examine: (1) effects of prey densities, prey composition, and crop structure on predation by O. insidiosus, (2) prey switching by O. insidiosus, and (3) effects of Orius gender on prey preference. If relative densities of F. occidentalis and A. swirskii were varied on flowers or foliage, O. insidiosus always switched to the more abundant prey. Male and female O. insidiosus did not show preference for A. swirskii over immature or adult F. occidentalis, but females killed more prey than males. In greenhouse trials simulating thrips infestations of cut rose crops during commercial production, we compared control of F. occidentalis on roses with releases of only A. swirskii or both O. insidiosus and A. swirskii. Roses with or without predators produced similar numbers of harvestable flowers, but roses without predators had, on average, two to three times more thrips than roses with predators. Concurrent releases of O. insidiosus with A. swirskii did not appear to either interfere with or enhance suppression of F. occidentalis on cut roses because counts of thrips and predatory mites on flowers with both O. insidiosus and A. swirskii were not statistically different from similar counts on flowers with only A. swirskii.
Life table data for Aphis gossypii Glover (Homoptera: Aphididae), an important pest in glasshouse cucumber crops, were studied at 20, 25 and 30 °C on two cucumber cultivars (Cucumis sativus L.) in controlled climate cabinets. The development time on the cucumber cv. ‘Sporu’ ranged from 4.8 days at 20 °C to 3.2 days at 30 °C. Immature mortality was approximately 20% and did not differ between temperatures. Most mortality occurred during the first instar. Reproduction periods did not differ among temperatures, but at 25 and 30 °C more nymphs were produced (65.9 and 69.8 nymphs/♀, respectively) than at 20 °C (59,9 nymphs/♀) because of a higher daily reproduction. Intrinsic rate of increase was greatest at 25 °C (rm = 0.556 day⁻¹). At 20 and 30 °C the intrinsic rate of increase was 0.426 and 0.510, respectively. On cv. ‘Aramon’, the development time of A. gossypii was approximately 20% longer at all temperatures. Immature mortality did not differ between the two cultivars. The intrinsic rate of increase on cv. ‘Aramon’ was 15% smaller than on cv. ‘Sporu’. The use of cucumber cultivars partially resistant to aphids is discussed in relation to biological control of cotton aphid in glasshouses. Development time and immature mortality on leaves of the middle and upper leaf layer of glasshouse grown cucumber plants (cv. ‘Aramon’) were comparable to development in the controlled climate cabinets. On the lower leaves immature mortality was much higher (approximately 82%) than on leaves of the middle (24.0%) and upper leaf layer (24.5%). Reproduction was less on the lower leaf layer (45.9, 70.5 and 70.1 nymphs/♀ on leaves of the lower, middle and upper leaf layer, respectively).
Biological control of different species of pest with various species of generalist predators can potentially disrupt the control of pests through predator-predator interactions. We evaluate the impact of three species of generalist predatory mites on the biological control of green peach aphids, Myzus persicae (Sulzer) with the aphidophagous gall midge Aphidoletes aphidimyza (Rondani). The predatory mites tested were Neoseiulus cucumeris (Oudemans), Iphiseius degenerans (Berlese) and Amblyseius swirskii Athias–Henriot, which are all commonly used for pest control in greenhouse sweet pepper. All three species of predatory mites were found to feed on eggs of A. aphidimyza, even in the presence of abundant sweet pepper pollen, an alternative food source for the predatory mites. In a greenhouse experiment on sweet pepper, all three predators significantly reduced population densities of A. aphidimyza, but aphid densities only increased significantly in the presence of A. swirskii when compared to the treatment with A. aphidimyza only. This stronger effect of A. swirskii can be explained by the higher population densities that this predator reached on sweet pepper plants compared to the other two predator species. An additional experiment showed that female predatory midges do not avoid oviposition sites with the predator A. swirskii. On the contrary, they even deposited more eggs on plants with predatory mites than on plants without. Hence, this study shows that disruption of aphid control by predatory mites is a realistic scenario in sweet pepper, and needs to be considered when optimizing biological control strategies.Graphical abstractHighlights► Three species of predatory mites were found to feed on eggs of an aphidophagous midge. ► Hyperpredation of midge eggs by the predatory mite Amblyseiusswirskii disrupted aphid control. ► Female predatory midges do not avoid oviposition sites with the predator A. swirskii.
The effect of the entomopathogenic fungus Beauveria bassiana on the biological characteristics and life table of Aphidius matricariae, a parasitoid of the green peach aphid, Myzus persicae, was studied under laboratory conditions. Aphids were first infected with twice the LC95 of B. bassiana for third-instar M. persicae (2 × 108 conidia/ml). Subsequently, at different intervals they were exposed to 1-day-old mated parasitoid females for 24 h. The number of mummies produced per female and the percentage emergence of the F1 generation differed significantly as a function of the time interval between application of the fungus and exposure to the parasitoid. The interference of B. bassiana on parasitoid development was also studied by first exposing the aphid hosts to the parasitoid for 24 h and subsequently applying B. bassiana. The number of mummies produced by a female A. matricariae varied from 11.8 to 24.8 and was significantly different when the aphids were first exposed to the parasitoids and then treated with B. bassiana 24, 48, 72, and 96 h after exposure. There were no significantly different effects of B. bassiana on net reproductive rate (R0), mean generation time (T), intrinsic rate (rm) and the finite rate of increase (λ) of A. matricariae as a result of development in hosts exposed to low or high conidial concentrations (1 × 102, 2 × 108 conidia/ml). The parasitoids developed in infected hosts had lower rm, λ, T and DT (doubling time) values compared with those that developed in uninfected hosts but no differences were observed in R0 values. With proper timing, A. matricariae and B. bassiana can be used in combination in the successful biological control of M. persicae.
We qualitatively reviewed the biocontrol literature in two major journals, Biological Control and Environmental Entomology, over the past 10 years by scoring 878 studies into 11 biocontrol-oriented questions. Quantitative meta-analyses were then used on data from 145 studies to examine the effects of different types of biocontrol agents (parasitoids, predators, and pathogens) on several attributes of weed and pest populations. Results for our qualitative review showed that most biocontrol studies were focused on lepidopteran pests, and that parasitoids were the most common biocontrol agents used. Our quantitative review showed that, for weeds, biocontrol agents significantly reduced weed biomass (À82.0%), flower (À98.9%), and seed production (À89.4%). For pests, our quantitative review showed that biocontrol agents significantly reduced pest abundance by 130% compared to control groups, increased parasitism (+139.0%) and increased overall pest mortality (+159.0%) compared to targets not exposed to biocontrol agents. Effects on pest mortality tended to be stronger for parasitoids than predators, although reductions caused in pest abundance were much stronger when predators were used as biocontrol agents. Addition of two or more biocontrol agents increased mortality by 12.97% and decreased pest abundance by 27.17% compared to single releases. Separate sets of meta-analyses demonstrated that the negative impacts of biocontrol on non-target species were much smaller than those for target species, although adverse effects of biocontrol on non-target organisms are based on small sample sizes and should be interpreted with caution. Our results also showed that biocontrol efficacy tended to be higher when agents were generalists than when they were specialists. Large fail–safe numbers found for most of the estimated effects indicate the robustness of the results found for the efficacy of biological control programs.
Neotyphodium lolii , an endophytic fungus of perennial ryegrass, deters Argentine stem weevil, Listronotus bonariensis , an important insect pest of pastures in New Zealand. Deterrence is apparently due to several alkaloids the fungus produces. We asked if the fungus also affects the third trophic level. Specifically, we tested if several different isolates of the fungus altered the growth and survival of the parasitoid, Microctonus hyperodae . Adult weevils were collected from paddocks near Lincoln, New Zealand and maintained in an environmental chamber. Weevils were assorted into treatment groups and fed perennial ryegrass (cv. Nui) lacking endophyte infection (nil) or containing one of the following endophyte strains: ARW, AR1, AR6, AR37. All endophyte strains differed from one another with respect to the profile of alkaloids they produce. Following two weeks of acclimation, weevils were placed with M. hyperodae to allow for parasitization. Weevils were then placed into Petri dishes (10 per dish) and fed grass clippings from the appropriate treatment group. We collected weevils as they died and dissected them to assess the development of parasitoids. Emergence of prepupae from hosts and survival to adulthood were also recorded.
Fungal isolates did not differ in their influence on weevil feeding or survival. In contrast, the effect of the endophyte on the parasitoid varied among isolates of the fungus. Isolates ARW and AR6 reduced parasitoid adult emergence relative to nil endophyte. In contrast, AR37 had no negative effect on survival of the parasitoid. Furthermore, an index of developmental rate showed that parasitoids developed more slowly when reared from hosts fed grass containing any of the strains of N. lolii , except AR37, compared to endophyte‐free grass. Negative effects of the endophyte on parasitoid survival were associated with the presence of ergovaline while effects on parasitoid development rate were associated with the presence of any alkaloid.
Diseases form an important component of the natural enemy complex of aphids. The most common and obvious of these diseases
are entomophthoran fungi such asErynia neoaphidis Remaudiere & Herbert,Entomophthora planchoniana Cornu,Zoophthora radicans (Brefeld) Batko andConidiobolus obscurus (Hall & Dunn) Remaudiere & Keller. The pest status of some aphids such as the pea aphid,Acyrthosiphon pisum (Harris), is considerably reduced by natural epizootics of fungal disease. However, disease may contribute little to practical
control as it is mainly effective in high density populations when weather conditions are suitable. Introduction of exotic
diseases for classical biological control is only rarely possible since most diseases, like their aphid hosts, are distributed
world-wide. One exception was the successful introduction into Australia of a strain ofZ. radicans for control of spotted alfalfa aphid,Therioaphis trifolii (Monell) f.maculata in 1979. Attempts to manipulate entomophthoran fungi have had limited success because of problems with mass production, the
fragility of the conidia and the need for suitably moist conditions. Hyphomycete fungi such asVerticillium lecanii (Zimm.) Viegas,Metarhizium anisopliae (Metsch.) Sorokin,Beauveria bassiana (Bals.) Vuill. andPaecilomyces spp. are more suitable for development as mycoinsecticides as they are cheap to mass produce and form stable conidia. “Vertalec™”,
a formulation ofV. lecanii, has been sold in small quantities commercially in Britain and parts of Europe for many years and used mainly in glasshouses.
Recently promising results have been obtained with use ofM. anisopliae for control of lettuce root aphid,Pemphigus bursarius (L.) in the UK. Laboratory studies on selected isolates ofB. bassiana andPaecilomyces spp. show a promising level of activity. Problems may occur with these species as they can kill aphid predators such as coccinelids.
In addition, more research is needed on developing improved formulations which enable control to be achieved under low humidity
conditions.
Les maladies constituent une part importante du complexe des ennemis naturels des pucerons. Les plus communes et les plus
connues sont des champignons entomophthorales tels queErynia neoaphidis Remaudiere & Herbert,Entomophthora planchoniana Comu,Zoophthora radicans (Brefeld) Batko etConidiobolus obscurus (Hall& Dunn) Remaudiere & Keller. La nuisibilité de certains ravagurs comme le puceron du poisAcyrthosiphon pisum (Harris), est considérablement réduite par des épizooties naturelles de maladies fongiques. Cependant, les maladies ne contribuent
peut être que faiblement à la régulation naturelle au champ, vu qu’elles sont surtout efficaces sur des populations de densité
élevée et dans des conditions climatiques particulières. L’introduction de maladies exotiques dans le cadre d’une lutte biologique
classique n’est q ue rarement possible, puisque la plupart des maladies, à l’instar des pucerons-hôtes, sont cosmopolites.
Une exception a été celle de l’introduction réussie en Australie d’une souche deZ. radicans pour contrôlerTherioaphis trifolii (Monell) f.maculata en 1979. Les tentatives de manipulation des entomophthorales ont eu un succès limité en raison des problèmes de production
de masse, de la fragilité des conidies et de la nécessité de conditions d’humidité convenables. Les champignons hyphomycètes
tels queVerticillium lecanii (Zimm.) Viegas,Metarhizium anisopliae (Metsch.) Sorokin,Beauveria bassiana (Bals.) Vuill. etPaecilomyces spp. sont plus à même d’être utilisés comme mycoinsecticides, étant donné que le coût de leur production de masse est faible
et qu’ils forment des conidies stables. Le « Vertalec™ », une formulation deV. lecanii, est vendu dans le commerce, en petites quantités, en Grande-Bretagne et en d’utres parties de l’Europe depuis de nombreuses
années, pour étre utilisée prinicipalement sous serre. Récemment des résultats prometteurs ont été obtenus avec l’utilisation
deM. anisopliae pour lutter contre le puceron des racines de la laitue,Pemphigus bursarius (L.) en Grande-Bretagne. Des études en laboratoire d’isolats choisis deB. bassiana et dePaecilomyces spp. montrent un niveau d’activité prometteur. Des problèmes peuvent apparaître avec ces espèces car elles peuvent aussi
tuer les prédateurs de pucerons tels que les coccinelles. Par ailleurs, des recherches supplémentaires sont nécessaires pour
développer des formulations améliorées permettant l’emploi de ces champignons dans des conditions d’humidité basses.
In conservation biological control (CBC), we attempt to reduce pest problems by increasing the abundance and diversity of the natural enemy community. However, rather than consistently strengthening herbivore suppression, studies show that the conservation of natural enemy species richness sometimes weakens, or has no affect, on biological control. Evidence is mounting that this idiosyncratic mix of positive, negative, and neutral effects of enemy diversity is caused by niche complementarity, intraguild predation, and functional redundancy, respectively. While the balance of evidence suggests that the conservation of natural enemy diversity and biological control are compatible goals, CBC practitioners cannot ignore the fact that conserving intraguild predators can sometimes disrupt biological control. Recent studies have made important progress toward identifying the traits of enemies and their prey that promote intraguild predation, functional redundancy, and niche complementarity. However, intraguild predation has received more attention than niche complementarity, and more theoretical and empirical work is needed rectify this asymmetry. We suggest that a continued focus on natural enemy functional traits, particularly those that are expressed at larger spatiotemporal scales, will increase our ability to identify the “right” kind of diversity and may ultimately improve the practice of conservation biological control.
Theoretical and empirical evidence developed in four subdisciplines of biological control (biocontrol of plant pathogens, weeds, nematodes, and arthropods) is brought to bear upon a shared question: the significance of intraguild predation. Intraguild predation ("IGP") occurs when two species that share a host or prey (and therefore may compete) also engage in a trophic inter-action with each other (parasitism or predation). We describe the prevalence of IGP and its role in the population dynamics of biological-control agents and target pests. IGP is a widespread interaction within many, but not all, communities of biological-control agents. IGP appears to be pervasive among communities of control agents associated with nematode or arthropod pests. Common forms of IGP include pathogens that infect both herbivores and parasitoids of the herbivore; facultative hyperparasitoids, which can parasitize either an herbivore or a primary parasitoid of the herbivore; predators that attack herbivores that harbor a developing parasitoid; and predators that attach each other. In contrast, IGP appears to be relatively uncommon among biological-control agents of plant pathogens because trophic interactions are less important than competition or antibiosis. Likewise, biological-control agents of weeds interact primarily through competition alone because host ranges are mostly restricted to plant taxa. Empirically based simulation models and general analytical models of interactions involving arthropod pathogens or facultative hyperparasitoids yield variable and often conflicting predictions for the influence of IGP on the success of biological control. Models for predator-predator interactions, however, consistently predict that IGP disrupts biological control. All the field-documented cases of IGP leading to disruption of biological control stem from studies of predators, including mites, insects, and predatory fishes. IGP between two predators or between a predator anti an adult parasitoid does not require mortality of the shared prey/host (i.e., the target pest); thus, IGP can be intense, resulting in high levels of mortality for one or both of the natural enemies, while the total mortality imposed on the target pest population is minimal. For this reason, we hypothesize that IGP by predators is particularly likely to influence the efficacy of biological control. Our ability to develop successful programs of biological control will be enhanced by field studies that address the complexity of trophic interactions occurring in agroecosystems. There is a critical need for additional manipulative experiments conducted in the field that test not only population ecology theory for two-species interactions, but also community ecology theory for multispecies interactions.
This study evaluated the quaternary ammonium compound cetyl trimethyl ammonium bromide (CTAB) as an alternative to the chemically related dodecylguanidine (dodine) for the selective isolation of entomopathogenic fungi. Oatmeal agar (OA) with chloramphenicol was used as basal medium, and three concentrations of CTAB (0.5, 0.6, 0.7 g/L) were evaluated and compared against OA + 0.46 g/L dodine. Selective isolation and growth studies were performed with the entomopathogens Beauveria bassiana, Metarhizium anisopliae s.l. and Paecilomyces lilacinus and five common non-entomopathogenic non-target species. The three entomopathogenic fungi sporulated earlier on OA + 0.6 g/L CTAB than on OA + 0.46 g/L dodine, while none of the non-target fungi sporulated on OA + 0.6 g/L CTAB. All entomopathogenic fungal isolates grew on OA + 0.6 g/L CTAB, despite some intra-species variation, whereas non-target fungi showed no growth or sporulation. OA + 0.6 g/L CTAB resulted in an efficient medium to isolate B. bassiana, M. anisopliae s. l. and P. lilacinus from soil samples. Results of our study suggest that OA + 0.6 g/L CTAB is a suitable, simple and inexpensive to prepare medium to replace OA + 0.46 g/L dodine for the selective isolation of these fungi.
Premise of the study:
The soil-inhabiting insect-pathogenic fungus Metarhizium robertsii also colonizes plant roots endophytically, thus showing potential as a plant symbiont. Metarhizium robertsii is not randomly distributed in soils but preferentially associates with the plant rhizosphere when applied in agricultural settings. Root surface and endophytic colonization of switchgrass (Panicum virgatum) and haricot beans (Phaseolus vulgaris) by M. robertsii were examined after inoculation with fungal conidia.
Methods:
We used light and confocal microscopy to ascertain the plant endophytic association with GFP-expressing M. robertsii. Root lengths, root hair density, and lateral roots emerged were also observed.
Key results:
Initially, M. robertsii conidia adhered to, germinated on, and colonized roots. Furthermore, plant roots treated with Metarhizium grew faster and the density of plant root hairs increased when compared with control plants. The onset of plant root hair proliferation was initiated before germination of M. robertsii on the root (within 1-2 d). Plants inoculated with M. robertsii ΔMAD2 (plant adhesin gene) took significantly longer to show root hair proliferation than the wild type. Cell free extracts of M. robertsii did not stimulate root hair proliferation. Longer-term (60 d) associations showed that M. robertsii endophytically colonized cortical cells within bean roots. Metarhizium appeared as a mycelial aggregate within root cortical cells as well as between the intercellular spaces with no apparent damage to the plant.
Conclusions:
These results suggest that M. robertsii is not only rhizosphere competent but also displays a beneficial endophytic association with plant roots that results in the proliferation of root hairs.