Multitrophic Interactions of Entomopathogenic Fungi, Crops, and Insects: Comparison
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MThe influltitrophicence between microorganisms and insects has led to the establishment of different types of interaction that can be summarised in various forms of interactions link. De Bary first defined symbiosis as “the cohabitation of distinct organisms”. Symbiosis isever here intended as a significant biological liaison between orophic levels, including plants, phytophagous, predators, parasitoids, and/or pathogens among species. Symbiosis is one of the leading evolutionary drivers promoting natural biological novelty. Symbiotic relationships between prokaryotes and eukaryotes are present in all kingdoms of life.

  • alien
  • invasive or quarantine pest
  • Integrated Farming
  • resilience

1. Introduction

Insects have inhabited the Earth for approximately 480 million years, representing the dominant life form as species and biomass [[1],[2],[3],[4]]. Their presence expresses the high biodiversity of insects in a wide range of ecological niches and results from their genetic plasticity, adaptability, and co-evolutionary processes with other organisms.

Trophic levels represent a hierarchical stratification through which organisms are positioned in the food chain. Producers (plants) are the basal resource, herbivores feed on plants and form a secondary trophic level (primary consumers), carnivores eat herbivores, forming a third trophic level (secondary consumers), and additional increasing apex levels defined by how many consumers we find in that given community.

Multitrophic interactions link multiple trophic levels, describing how the exchange of matter and energy occurs. They include simple tri-trophic relationships (producers, herbivores, consumers) but extend to more levels, such as higher-order predators preying on intermediate predators and hyperparasitoids attacking primary parasitoids.

Omnivory (the consumption of plants and animals) is a widespread feeding strategy, represented in 12 insect orders and at least 40 families [5]. This behavior increases the complexity of possible trophic links for each species. Price et al. [6] remind us that insects complicate the placement of species into individual functional groups because of their ontogenetic development. Several insects, changing from juvenile to adult, shift food habits placing themselves in different food guilds depending on their stage of development.

Microbes greatly affect the terrestrial ecosystem at the multitrophic level; they link plants to other trophic levels, e.g., heterotrophs degrade the organic matter waste from the higher trophic levels to the producers, making it possible for plants to return inorganic nutrients (degraders trophic level).

Microorganisms can also establish relationships among animals or plants that become their hosts.
The influence between microorganisms and insects has led to the establishment of different types of interaction that can be summarised in various forms of interactions. De Bary [[75]] first defined symbiosis as “the cohabitation of distinct organisms”. Symbiosis is here intended as a significant biological liaison between or among species. Symbiosis is one of the leading evolutionary drivers promoting natural biological novelty. Symbiotic relationships between prokaryotes and eukaryotes are present in all kingdoms of life [86]].
Symbioses between two organisms can be broadly classified as mutualism, commensalism, or antagonism, depending on the interaction between the species involved. The impact of the symbiont on the amphitryon can highlight an evolutionary continuum between antagonism (negative interaction), commensalism (neutral interaction), and mutualism (beneficial interaction) [[97]]. Symbiotic relationships drive many interesting biological processes, both within individuals and at the ecological system level.
For the sake of this contribution, researchers consider ectosymbiont as the guest living out of the host body and endosymbiont as a guest living in the host body. Inside the amphitryon body, the guest may live within specializsed host cells [[108],[119],[1210]].
Mutualism provides an advantage for both species involved. Mutualistic microorganisms can give the host essential nutrients, protection from enemies, increase fitness, and mediate the host’s interaction with other species [[1311]]. Mutualists can be divided into obligate and facultative. Obligate or primary symbionts are microorganisms necessary for the host’s survival. They tend to improve the nutritional aspects of unbalanced diets on which the host feed [[1412]]. Facultative symbionts are not essential for the survival of their host and have broader effects ranging from modifying nutritional aspects to manipulating reproduction. Secondary mutualists can often only be found in a fraction of the host population [[1311],[1412]].
Commensal symbiosis represents a symbiotic relationship in which one organism benefits without associated costs [[1412],[1513]].
Finally, parasitism or antagonism represents an unbalanced interaction in favour of the guest microorganism that takes advantage of the insect, generating a loss of fitness or causing host death. Antagonists may be obligate (host-specific) or facultative generalists. Antagonism between insects and entomopathogenic organisms results from co-evolution in which the pathogen aims to host exploitation better and improve its transmission. In contrast, the insect seeks to exclude the pathogen more effectively by improving its defensce strategies [[1614]]. Both actors involved in antagonism adopt physiological, ecological, and ethological adaptations to maximizse their fitness [[1715]].
The following chapters will discuss the interactions between plant-damaging insects and entomopathogenic fungi and how multitrophic relationships exist between plant insects and their pathogens

2. Interactions between Entomopathogenic Fungi and Pests

Biological control of invasive pests also relies on certain entomopathogenic fungi (EFs) that can infect hosts in agroecosystems and appear suitable for plant protection exploitation. For many years, the search for such species used their isolation from insect carcasses, followed by identification using conventional light or electron microscopy techniques. Thanks to the development of molecular methods, especially DNA sequencing and omics technologies, it is now possible to identify the most crucial EFs species and detect their presence in different ecological niches, including the soil or plant environments. EFs number around 1000 species [[1816]], the best-known being Aspergillus spp., Penicillium spp., Fusarium spp., and Acremonium spp. [[1917]]. Infection usually occurs through propagules that germinate and invade the host body after contact; the invasive mycelium then colonizses the host until it dies. Conidiation from emerging hyphae and/or the production of resting propagules follow the host death [[2018]]. Among the EFs primarily used for pest control, some Beauveria spp. (Hypocreales, Cordycipitaceae) are widely used against, for example, the coffee berry weevil Hypothenemus hampei (Ferrari, 1867) (Coleoptera, Curculionidae) [[1715]], the Asian corn borer Ostrinia furnacalis Guenée, 1854 (Lepidoptera, Crambidae), and the sweet potato weevil Cylas formicarius (Fabricius, 1798) (Coleoptera, Brentidae) [[2119]]. Many studies have deepened the knowledge about the role of Beauveria bassiana (Bals.) Vuill, 1912, as its insecticidal activity is due not only to the hyphae penetrating and spreading in the host body but also to the effect caused by various toxins [[2220]]. This fungus demonstrated its relevance in banana crops protection from Cosmopolites sordidus (Germar, 1824) (Coleoptera, Dryophthoridae) [[2321],[2422],[2523]] due to its ability to significantly reduce the weevil survival [[2523]]. Beauveria bassiana products are widely applied on banana plantations to manage C. sordidus and use pheromone for mass trapping. Another Beauveria species, Beauveria caledonica, is responsible for the lethal infections of C. sordidus in banana plantations in South America. This fungus produces various secondary metabolites and can modulate the pest immune response [[2523],[2624]]. Studies with Metarhizium anisopliae (Metschn.) Sorok, 1883 reported the potential of this fungus in controlling adult weevils [[2725]]. Several studies are underway to control P. spumarius, indicated as the main vector of the bacterium Xylella fastidiosa Wells, Raju et al., 1986 involved in the OQDS (Olive Quick Decline Syndrome) in the Salento Peninsula (southern Italy). The insect can acquire and inoculate the bacterium from/to different host plants [[2826]]; therefore, it is essential to limit the transmission of X. fastidiosa by managing its vector. Recent studies analyzse the ability of some Trichoderma spp. isolates in decreasing the survival of P. spumarius [[29]27]]. An innovative IPM approach may include developing EF-based biocontrol actions. EF also represents an essential source of natural molecules capable of affecting P. spumarius metabolism and reproduction, thus limiting the pests’ indirect damage to plants [[2927]]. Species of the genus Trichoderma are among the most studied and used biocontrol agents worldwide. They not only produce benefits as plant growth promoters but also act, with various mechanisms, against other microorganisms in plant defensce. Volatile and non-volatile compounds produced by some species of Trichoderma can be perceived by the olfactory structures of P. spumarius [[2927]], modifying and directing the insect’s food preferences towards other areas of reduced agricultural interest [[2927],[3028],[3129]]. Although supported by valid research data, the information available in the literature on the exploitation of EFs as biocontrol agents still needs to be comprehensive. Critical data on the exploitation of EFs as practical means of biological control and information on the mechanisms involved in fungal-insect interactions still need to be included in many world regions. Therefore, efforts are still required to identify and characterizse new fungal strains to investigate their entomopathogenic capacity as an alternative to pesticides.

3. Multitrophic Interactions of Entomopathogenic Fungi, Crops, and Insects

Insect pathogens were isolated from Mediterranean soils (Alicante, SE Spain) using Galleria mellonella L., 1758 (Lepidoptera, Pyralidae) larvae baits [[3230]]. Samples from 61 sites were from agroecosystems and forests, while soils under Nerium oleander L., 1753, gave results from natural environments and gardens. Entomopathogenic fungi (EFs) are the most frequent insect pathogens (32.8% soils). Beauveria bassiana is the most abundant species (21% soil). Metarhizium anisopliae (6.4%) and Akanthomyces lecanii (Zimm.) Spatafora, Kepler, and Shrestha, 2017 {Lecanicillium lecanii (Zimm.) Gams [=Verticillium lecanii Zimm.]} (4.8%) are less frequent. Beauveria bassiana also scored the highest virulence in a single soil sample (ca. 90% infected insects) and is the most frequent EF (77.8%) in soils under N. oleander. Soils from commercial crop fields of food security importance, such as bananas, are also reservoirs of EFs [[3331]]. Reports indicate that B. bassiana is a cosmopolitan entomopathogen, especially in warm areas [[3432]]. Economically important pests, such as thrips [[3533]], aphids [[3634]], or pine processionary (Thaumetopoea pityocampa [Denis and Schiffermüller, 1775] [Lepidoptera, Notodontidae]) [[3735]], were detected naturally infected with EFs. Beauveria bassiana (isolate Bb203) also infected adults of the Red Palm Weevil, Rhynchophorus ferrugineus Olivier, 1790 (RPW), in the field (palm groves) just at the first weevil introduction in south-eastern Spain [[3836]]. Beauveria bassiana 203 proved more pathogenic to R. ferrugineus than strains from other hosts and sources [[3937]]. The strain applied three times at three-month intervals to field palms naturally infested with RPW caused 70–85% insect mortality [[4038]]. Therefore, EFs are present in arid environments and have great potential for IPM of severe insect pests [[4139],[4240]]. EFs can also colonizse plants and plant waste. The latter is the most frequent component of soil organic matter. Evaluation of the growth and multiplication (conidiation) of common entomopathogens rises from inoculation (on almond peels) and gardening (palm waste) substrates obtained from Mediterranean ecosystems by-products of agriculture [[4341]]. The development of entomopathogens depends on the type of substrate. Akanthomyces lecanii grows and sporulates well on almond mesocarp, but Paecilomyces farinosus (Holmsk.) A.H.S.Br. and G.Sm., 1957 does not. Beauveria bassiana uses palm seed nutrients for growth and sporulation, and leaves of the Mediterranean dwarf palm Chamaerops humilis L., 1753 promote the growth and sporulation of both A. lecanii and B. bassiana. The date palm (Phoenix dactylifera L., 1753) has a mycobiota that includes-sporulating fungi (Penicillium spp. and Cladosporium spp.). Fusarium oxysporum Schltdl., 1824 saprotroph and an undescribed Lecanicillium c.f. psalliotae (Treschew) Zare and W. Gams, 2001 entomopathogen colonise leaves infested with Marlatt red-scale (Phoenicococcus marlatti Cockerell, 1899—Hemiptera, Phoenicococcidae) [[4442]]. Palm pathogens, entomopathogenic and saprotrophic fungi strongly interact with each other; B. bassiana strongly inhibits Penicillium vermoesenii [=Nalanthamala vermoesenii (Biourge) Schroers, 2005] (Figure 1), a fungal necrotrophy of palms.
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Figure 1. Beauveria bassiana (red arrows) inhibits the fungus palm pathogen Penicillium vermoesenii (green arrows). (A) Both fungi interact directly on the PDA medium. (B) The same two fungi on top of a dialysis membrane overlaid onto PDA.
EFs (B. bassiana, Lecanicillium dimorphum (J.D.Chen) Zare and W.Gams, 2001, and Lecanicillium c.f. psalliotae) artificially inoculated in living plants act as true endophytes [[4543]]; fungi survive and spread in date palm (P. dactylifera) petiole tissues (parenchyma and vascular tissue) at least 30 days after inoculation. Beauveria bassiana is a natural endophyte from date palm roots [[4644]]. This fungus was isolated from the roots of date palms in two coastal dune sites with high and low human impact in south-eastern Spain. Root colonizsation by endophytic insect-pathogenic fungi has recently been reviewed [[4745]]. Root and microbiota respiration [[4846]] depletes oxygen in the rhizosphere. Fungal parasites of invertebrates, such as the nematophagous Pochonia chlamydosporia (Goddard) Zare and W. Gams, 2001 or the entomopathogens B. bassiana and M. anisopliae, breach chitin-rich barriers to infect the host. These biocontrol fungi can also ferment chitosan, a chitin derivative [[4947]]. Apart from their application in biofuel production, this trait can be an adaptation for survival and insect infection by EFs in the rhizosphere. Entomopathogenic fungi are part of phylloplane and rhizosphere mycobiomes. Their endophytic behaviour allows them to colonizse plant-derived substrates, affecting plant-volatile emissions during insect infestations [[5048]]. Plant-derived substrates, such as rice grains, can be used for mass production and formulation of EFs [[5149],[5250]]. Based on previous reports (see above) on the endophytic behaviour of EFs, several studies tested the response of palms to inoculation with these biocontrol fungi. Beauveria bassiana, L. dimorphum, and L. cf. psalliotae induced proteins in plant defensce or stress response [[5351]]. The plant immune system responds to microbe-associated molecular patterns (MAMPs) derived from conserved structures (i.e., cell walls) of plant pathogens such as chitin [[5452]]. Chitosan can permeabilizse the membrane and kill plant pathogens such as bacteria and fungi in its deacetylated form [[55]53]]. EFs and nematophagous fungi (NFs) are compatible with chitosan since they have evolved low-fluidity membranes [[5654],[57]55]] and branched cell walls rich in β-1,3-glucan [[58]56]]. Moreover, EFs and NFs are in contact with chitin during host (insects and nematodes, respectively) infection. Chitosan modifies the transcriptome and biology of fungi and plants, causing cell stress [[5957]]. Chitosan can enhance the pathogenicity of fungal parasites of nematode eggs [[58],[59],[60][61][62]]. These are close relatives of EFs, such as Metarhizium spp. [[6361]]. Tests will explain the effect of chitosan on the EFs’ pathogenicity. Acoustics reveals that RPW larvae have briefer movement and feeding activity with B. bassiana infection [[6462]]. Researchers also have evidence that B. bassiana formulates used for RPW biocontrol in the field [[4038]] repel adults of this insect pest [[6563]]. Evidence suggested investigating entomopathogenic fungi and close fungal pathogens of invertebrates for volatiles capable of modifying the behaviour of insects of economic importance, such as weevils. Entomopathogenic fungi and close relative nematophagous fungi (Pochonia spp. egg parasites) emit volatile organic compounds (VOCs) capable of repelling C. sordidus [[33]31]] and RPW [[66]64]]. P201930831 and P202230103 insect repellents patented VOCs are on field trial for efficacy. Finally, EFs are a component of plant and soil microbiomes. They are efficient insect pathogens with a multitrophic lifestyle, including plant endophytism, inducing plant defensces, and modifying insect pest behaviour with their VOCs, which work as low environmental impact tools for insect pest management.

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