AEAdvances in Entomology2331-1991Scientific Research Publishing10.4236/ae.2020.83010AE-100843ArticlesBiomedical&Life Sciences Interactions between Entomopathogenic Fungi and Entomophagous Insects MohamedSamir Tawfik Abbas1*Plant Protection Research Institute, Agricultural Research Centre, Giza, Egypt02062020080313014617, April 20208, June 2020 11, June 2020© Copyright 2014 by authors and Scientific Research Publishing Inc. 2014This work is licensed under the Creative Commons Attribution International License (CC BY). http://creativecommons.org/licenses/by/4.0/

Direct treatment of predators with entomopathogenic fungi (EPF) at different concentrations revealed that some species, like Beauveria bassiana and Metarhizium anisopliae, were found to have detrimental effects on all developmental stages of some predator species. Other species, like Numoraea rileyi and Paecilomycis fumosorosius, showed little or no effect on treated predators. Adult predators were found to avoid feeding on fungi-infected prey. EPF could be isolated from hibernating or field-collected coccinellids. Some studies indicated that combining a fungus with a predator could increase the rate of insect control in the field. As for parasitoids, this review indicates that the developmental stages of the egg parasitoids can develop successfully in host eggs treated with fungi. However, fungus-infected hosts negatively impact the development of larval parasitoids inside such hosts and this impact depends on the species and concentration of the fungus as well as the time between infection and parasitism. Some parasitoid females can discriminate between fungus-infected and uninfected hosts and do not parasitize the infected hosts. With appropriate timing, the parasitoids or predators could be combined with fungi for the biological control of insects in the field.

Entomopathogenic Fungi Predators Parasitoids Natural Enemies Intraguild Predation1. Introduction

The interactions between insect pathogens, parasitoids and predators have been termed “Intraguild predation (IGP)” [1]. It occurs when two species share a host or prey (and therefore may compete), or engage in a trophic interaction with each other (parasitism or predation). This interaction may impact the population dynamics of biological control agents and target pests. Common forms of IGP include pathogens that infect both herbivores and parasitoids of the herbivores; facultative hyperparasitoids which can parasitize either a herbivore or a primary parasitoid of the herbivore; predators that attack herbivores which harbor a developing parasitoid, and predators that attack each other. Thus, IGP can be intense resulting in high levels of mortality for one or both of natural enemies, while the total mortality imposed on the target pest populations is minimal. Despite such negative interactions demonstrated in the laboratory, it is less often documented in the field [2].

The interactions between entomopathogens and other bio-control agents can be synergistic, additive or antagonistic depending on the specific biological control agents as well as their concentrations, timing of application and host species [3]. Synergistic interactions result in a higher mortality than the combined individual mortalities of the pest population. Additive interactions occur if the natural enemies do not interact and, thus, the total level of mortality is equivalent to the combined individual mortalities caused by each agent. The antagonistic interactions occur if the total mortality is less than when either natural enemy acts alone [4].

2. Entomopathogenic Fungi (EPF)

EPF are associated with insects, in almost all orders, living in diverse habitats. They are one of the most common pathogens that cause diseases in insects infesting vegetables, field crops, orchards and ornamentals. Insect adults as well as the newly molted larvae and the newly formed pupae are more susceptible to infection than those in which the cuticle has fully hardened. The egg stage is rarely infected. Over 700 EPF species have been recorded, however, very few commercial products of fungi was proved to be successful insecticides [5]. This fact is attributed to that the virulence of EPF depends on limits of environmental conditions including 20˚C - 30˚C and 90% or above relative humidity (R.H.).

3. Mode of Infection of EPF

EPF can infect insects through body cuticle, spiracles mouth parts and other external openings of the insect. In general, when the environmental conditions are suitable (mainly temperature of 20˚C - 30˚C) and 90% or above relative humidity as mentioned earlier) are suitable, the infective spore of the fungus, which is attached to host cuticle, germinates forming a germ tube that penetrates the insect epicuticular layer. Enzymes activity as well as mechanical force is involved in cuticle penetration and hyphal bodies are generally produced and apparently multiply within the hemocoel of the host. Some fungal species and strains produce sufficient toxins at this time causing death of the host although no vital organs have been invaded. The fat body is generally the preferred site for hyphal invasion. After death of the insect, the fungus grows saprophytically in the hemocoel to form a mycelial mass that turns into a hard sclerotium, and the reproductive spores are produced within the sclerotium or on sporophores. The sporophores and the hyphae emerge from the cadavers to form the characteristic mycelial growth on the host’s integument and sporulation occurs on the cadavers [6].

4. Parasitoids and Predators

Parasitoids and predators are among the biological control agents that play an important role, naturally, against agricultural pests infesting field crops, vegetables, orchards and ornamentals. They constitute a considerable part within IPM programs which include suitable timing of plantation, suitable agricultural practices, using biological control agents (parasitoids, predators and entomopathogens) and finally selective chemical insecticides if needed.

5. Interactions between EPF and Predators5.1. Laboratory Experiments5.1.1. Effect of EPF on Treated Predators

1) The eggs

Metarhizium anisopliae (Ascomycota, Hypocrealis) and Hesperomyces virescens (Ascomycota, Laboulbenialis) caused 14.66% and 11.53% mortality, respectively, in the egg stage of the coccinellid, Harmonia axyridis (Pallas) [7]. However, the fungus, Lecanicillium muscarium (previously known as Verticillium lecanii) did not affect the eggs of the coccinellid, Eriopis connexa (Germar) when treated at concentrations of 1.6 × 103 or 1 × 107 conidia/ml [8].

2) The larvae

50% of the coccinelid, Cryptolaemus montrouzieri Muls larvae died when they fed on mealybugs sprayed with 1% Boverin (a commercial product of Beauveria bassiana (Balsamo), (Ascomycota, Hypocrealis) [9]. At 5 concentrations of 4 fungal species (ranging from 104 to 108 conidia/ml), B. bassiana, Metarhizium anisopliae and Paecilumyces fumosoroseus caused up to 95, 97 and 56% mortalities, respectively, in 1st and 2nd instar larvae of the coccinellid, Hypodamia convergens Guerin-Meneville whereas Numoraea rileyi did not cause mortality in such larvae [10]. At a concentration of 3 × 107 conidia/ml, B. bassiana caused 35.7% mortality in 2nd instar larvae of Chrysoperla carnea [11]. Also, different strains of M.anisopliae caused up to 67.50% mortality in different larval instars of the coccinellid predator, Menochilus sexmaculatus (F.) [12].

The fungus, Verticilium lecanii was found to be highly pathogenic to the 3rd instar larvae of C. carnea and decreased the emergence rate of adults as well as the fecundity of females [13]. Similarly, infection of the aphid, Rhopalosiphum padi (L.) with V. lecanii, 72 h before exposing to larvae of its predator, H. axiridis reduced the consumption rate of the aphid by such larvae [14]. Lecanicillium longisporum, did not cause detrimental effects on survival or prey consumption of the dipteran aphid predator, Aphidoletes aphidimyza (Rondan) when sprayed directly on the 4-day old larvae [15]. In contrast, at a concentration of 1 × 107 conidia/ml, L. muscarium caused 45% and 30% mortality in the 1st and 2nd instar larvae, respectively, of the coccinellid, preadator, Eriopis connexa (Germar) [8].

3) The pupae

At a concentration of 1 × 107 conidia/ml, L. muscarium did not cause mortality in the pupae of E. connexa (8). However, B. bassiana proved to be pathogenic to the pupae of the same predator [16].

4) The adults

N. rileyi did not infect the treated adults of the predators, H. convergens, C. carnea and the pentatomid, Podisus maculiventris (Say) [17]. In contrast, up to 95.8% mortality in adults of Teretrius nigrescens Lewis (Col.: Hesteridae) a predator of the larger grain borer, Prostephanus truncates (Horn) (Col.: Bostrichidae) occurred after direct exposure to 1 × 109 conidia/ml of B. bassiana [18]. Percentage of mortality in the adults of the coccinellids, Coccinella septimpunctata (L.), Harmonia axyridis (Pallas) (from Japan and Britain) and Adalia bipunctata (L.) was assessed when treated with B. bassiana [19]. Mortality of both C. ceptempunctata and A. bipunctata was high relative to H. axyridis. The impact of B. bassiana on H. axyridis Britain strain was detected via reduced fecundity at all tested doses (105, 107 and 109 conidia/ml) [19].

The susceptibility of adults of 6 coccinellid species to B.bassiana was estimated at a concentration of 2.5 × 105 conidia/ml [20]. It was found that Olla v-nigrum (Mulsant), Cycloneda munda (Say) and H. convergens were susceptible to infection; 63%, 60% and 35% mortality, respectively. In contrast, Coleomegilla maculata (Degeer), C. septempunctata, and H. axiridis were resistant to infection. The fertility, pre-oviposition, oviposition and post-oviposition periods as well as life span of the coccinellid, E. connexa were negatively affected by B. bassiana [21]. Similarly, adults of E. connexa were found to be susceptible to B. bassiana infection and the daily fecundity of female was significantly reduced compared to the control [16].

The impact of B. bassiana and Metarhizium brunneum on the adults of Dalotia coriaria (Kratz) (Col.: Staphylinidae) and the two mites, Strateolaelaps scimitus (Womer) and Gaeolaelaps gillespiei Beaulieu (Acarina: Acaridae) was studied at 2 concentrations (1 × 105 and 1 × 10)7 conidia/ml [22]. The results showed that mortality in D. coriaria was not significantly higher than the control at both concentrations of B. bassiana and the concentration of 1 × 105 conidia/ml of M. brunneum. However, the 1 × 107 concentration of M. brunneum caused significant higher mortality in the predator (41%). The treated S. scimitus was not significantly affected by both fungi species while G. gillespiei was significantly adversely affected by both fungi; 36% and 31% mortality by M. brunneum and 61% and 51% by B. bassiana at the concentrations of 1 × 105 and 1 × 107 conidia/ml, respectively.

V. lecanii was found to have no significant effect on fecundity and longevity of the coccinellid, Delphastus catalinae (Horn), a predator of whiteflies [23]. When the mirid predator, Dicyphus Hesperus Knight (Hemiptera) females were exposed to leaf discs treated with the fungus, Paecilomyces fumosoroseus at a concentration of 100 fold of LC50 of the nymphs of the whitefly, Trialeurodes vaporariorum (Westwood) nymphs, 38% of the females died. In addition, the survived females showed 38% feeding reduction [24].

5.1.2. Discrimination between Fungi-Infected and Uninfected Prey

In non-choice experiments, adults of C.septempunctata and the carabid, Pterostichus madidus (F.) were shown to consume aphids at a late stage of infection by the fungus, Erynia neoaphidis [25] [26]. However, larvae of the syrphid predator, Episyrphus balteatus De Geer and the chrysopid, C. carnea never consumed E. neoaphidis-infected aphids [26]. Similarly, H. convergens avoided feeding on the wheat aphid, Diuraphis noxia (Mordvilko) infected with P. fumosoroseus [27]. The females of the mirid predator, Dicyphus hesperus, were able to discriminate between healthy and P. fumosorosius-infected nymphs of the whitefly, Trialeurodes vaporariorum when the latter nymphs were offered to them 5 days post treatment [24]. Similarly, both male and female of C. septempunctata avoided B. bassiana spores through contact with leaf surfaces, soil-inoculated, and mycosed cadavers [28].

5.1.3. Isolation of Fungi from Predators

B. bassiana could be isolated from hibernating and/or collected adults of the coccinellids, C.septempunctata [29]; Adalia bipunctata [30]; Cycloneda sanguinea (L.) [31]; Olla v-nigrum (Mulsant) [32].

Hesperomyces virescens could be isolated from Harmonia axyridis [33] [34]; Chilocorus stigma (Say), C. bipustulatus (L.), Adalia bipunctata (L.) and H. convergens [35], as well as E.connexa [34]. The fungus, Isaria farinosa (Ascomycota: Hypocreales) could be isolated from Harmonia axyridis [36].

5.2. Field Experiments5.2.1. Compatibility between Predators and Fungi as Bio-Control Agents

Field application by B. bassiana against alfalfa pests revealed that the fungus caused 75% - 93% mortality in H. convergens when applied early in the season but the application late in the season had little impact [37]. The authors related this little impact late in the season to the prevailing temperature which exceeded 25˚C. In a greenhouse experiment, enhanced control was recorded against the thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) on pepper when the adult of the predatory mite, Neoseiulus (=Amblyseius) cucumeris (Oudemans) was combined with B. bassina with no significant effects of the fungus on the predator [38]. Similarly, in a greenhouse trial on tomato, the simultaneous use of the predator, Dicyphus Hesperus and the fungus, P. fumosoroseus resulted in additive whitefly mortality; they reduced the whitefly densities by 62% relative to the control plants in 6 weeks [24]

The combined effect of the dipteran predator, Aphidoletes aphidimyza (Rondani) (Fam.: Cicedomyiidae) and the fungus, L. longisporum on the aphid, Myzus persicae was estimated in cages in a greenhouse [15]. The results showed an additive effect of both natural enemies as a higher reduction of aphid population was observed in treated cages compared to the treatment with the predator or the fungus alone. Similarly, the rove beetle, D. coriaria, was found to be compatible with M. anisopliae in greenhouse experiments as the fungus did not inhibit the ability of the predator to consume its prey [39]. Also, the compatibility between the fungus, M. anisopliae and the coccinellid, Cheilomenes lunata (Fab.) could provide a sustainable strategy for effective management of aphids on crucifers [40]. A. aphidimyza and the fungus, M. brunneum could be combined against the aphid, Rhopalosiphum padi infesting sweet corn in the greenhouse. A. aphidimyza applied alone suppressed the aphid population more effectively than M. brunneum applied alone. However, the aphid population was most suppressed when both agents were combined [41].

5.2.2. Transmission of Fungi by Predators

The potential of coccinellid adults to transmit the fungus, Erynia neoaphidis in aphid populations in the field (in caged plants) was demonstrated [42]. It was found that the contaminated coccinellids caused 5% infection in the aphid population. However, despite this low percentage of infection, an epizootic was initiated by such a level of infection [26]. C. septempunctata adults which foraged on plants with different densities of sporulating aphid cadavers became contaminated with the fungus, E. neoaphidis conidia. Such adults carried the conidia to uninfected aphid populations and initiated infection [43].

5.2.3. Discrimination between Healthy and Fungus-Infected Prey

From field observations, it was found that no visibly E. neoaphidis-infected aphids were consumed by either larvae or adults of C. septempunctata [42].

6. Interactions between EPF and Parasitoids

There is a fungistatic substance secreted by the parasitoids into the hemolymph of the host insect that impedes the development of mycosis and enable normal parasitoid development and emergence. This fungistatic substance is linked to the time interval between parasitism and contamination of the host by the fungus [44].

6.1. Laboratory Experiments6.1.1. Effect of Fungi on the Development of the Parasitoids

The fungus N. rileyi inhibited the development of the braconid parasitoid, Microplitis croceipes (Cresson) if larvae of Heliothis zea (Boddie) were infected one day after parasitism [45]. Similarly, when the aphids were infected with the fungus, Pandora neoaphidis, less than 4 days after being parasitized by the parasitoid, Aphidius rhopalosiphi, the parasitoid did not complete its development [46]. However, when infection occurred more than 4 days after parasitism, development of the parasitoid was significantly impaired but no histological evidence that the fungus invaded the tissues of the parasitoid. Spraying the fungus, Paecilomyces fumosoroseus against the whitefly, Trialeurodes vaporariorum (Westwood) on seedlings of beans at the recommended rate for the greenhouses did not affect the development of the parasitoid, Encarsia formosa Gahan inside its host nymph [47].

The interaction between the aphid parasitoid, Aphidius nigripes (Ashmead) and the fungus, V. lecanii was found to be dependent on the relative timing between parasitism and infection. A high proportion of the parasitoid developed successfully when aphids were exposed to the fungus 4 days after parasitism [48]. The effects of V. lecanii on cereal aphids, Rhopalosiphum padi (L.) and Sitibion avenae (Fab.) and whether the fungus affects the performance of the parasitoid, Aphidius colemani (Viereck) were studied [14]. The study revealed that percent parasitism by A. colemani in both insects was not affected by the fungus when aphids were first treated with V. lecanii and then exposed to the parasitoid. However, the emergence % of adults from the mummies was lower in infected hosts than in uninfected ones when the aphids were first exposed to the parasitoid and then treated with the fungus. The female ratio in the emerging adults was lower in fungus-treated aphids in both species than in untreated ones.

Similarly, the impact of B. bassiana on the biological characters of Aphidius matricariae (Haliday), a braconid parasitoid of the peach aphid, Myzus persicae (Sulzer) was evaluated [49]. Aphids were first infected with B. bassiana at a concentration of 2 × 108 conidia/ml and then exposed to parasitoid females for one day at 1, 2, 3 and 4 days post infection. The number of mummies produced per female parasitoid varied from 11.8 to 24.8 and was significantly different according to intervals between infection and exposure to the parasitoid (1 - 4 days). The possibility of combined use of the same fungus and the same parasitoid against the same aphid was investigated [50]. The mummies of parasitized aphids were treated with the fungus suspension on the same day of their formation at the recommended application rate (5.5 × 107 conidia/ml). The results showed that percent of adult emergence, females ratio and longevity of adults from treated mummies did not differ significantly from those from untreated ones. However, when parasitized aphids were treated with the fungus, at the same concentration, immediately or 2-day post parasitism, the numbers of formed mummies were 38 and 39, respectively, compared to 62 mummies in the control aphids.

In another experiment, the interactions between B. bassiana and the aphid braconid parasitoid, Diaeretiella rapae (Maclntosh) were studied [51]. Nymphs of M. persicae were first exposed to parasitoid females for 24 h and then sprayed with B. bassiana (1 × 1010 conidia/ml) at 0, 24 and 48 h after parasitism. Likewise, aphids were sprayed with the fungus and exposed to the parasitoid at 0, 24 and 48 h post infection. The results showed that % parasitism varied from 13% to 66.5% and it was lower, significantly, in both treatments within 0 - 24 h compared to the control. Percentage of parasitoid emergence was negatively affected when fungus-treatment occurred before exposure to the parasitoid. In addition, a decrease of longevity of female parasitoid F1 generation was observed when the parasitized aphids were treated with the fungus.

Three isolates of B. bassiana and 2 isolates of M. anisopliae were tested against larvae and pupae of the ecto-larval parasitoid, Habrobracon hebetor (Say) [52]. The results showed that the isolates EUT105 of B. bassiana and M396 of M. anisopliae did not cause mortality in larvae of H. hebetor at 6 tested concentrations (106 - 1011 conidia/ml). The EUT116 and IRAN187C isolates of B. bassiana at the concentration of 1010 conidia/ml caused 6.67% and 51.1% mortalitiy, respectively, to the parasitoid larvae. All tested isolates of both fungi did not affect the treated pupae of the parasitoid. The life table parameters of H. hebetor were studied when reared on 3rd instar larvae of Helicoverpa armigera (Hubner) previously infected at 0, 24, 48, and 72 h with a sub-lethal concentration (LC30) of M. anisopliae [53]. It was found that fungal infection adversely affected life table parameters of the parasitoid depending on the time between infection and parasitism. Statistically, different variations for parasitoid infection increased when the time between infection and parasitism was longer than 24 h.

Rate of parasitism of the eulophid ecto-nymphal parasitoid, Tamarixia sp. on nymphs of Bactericera cockerelli (Sulk) (Hemiptera: Triozidae) that were previously infected with three isolates of B. bassiana was evaluated [54]. The results showed that rates of parasitism in fungus-treated nymphs did not differ significantly from those of the untreated ones. Laboratory experiments were carried out to investigate the effects of application of two B. bassiana isolates on Tamarixia sp. during its development on its host, B. cockerelli [55]. Three concentrations (LC20, LC50 and LC90 of the fungus were applied to the 4th nymphal instars parasitized with Tamarixia sp. 3, 5, 8 or 12 days earlier at 25˚C. The greatest infection of the parasitoid larvae was observed when LC90 was used regardless the isolate, and when parasitism occurred 3 or 5 days before infection. The lowest infection rate of the parasitoid larvae was observed when parasitism occurred 8 or 12-day before infection regardless the isolate or concentration. The highest parasitoid emergence percent was achieved at the lowest B. bassiana concentration and applied to B. cockerelli at 12-day before infection. Longevity of adult parasitoids emerged from treated hosts was greater when parasitism occurred 12 days before infection.

The interactions between Tamarixia radiate (Waterston) and the fungus, Isaria fumosorosea, on the psyllid, Diaphorina citri Kuwayama (Hem.: Liviidae) were investigated [56]. Three interactions were studied: 1) Parasitoid survival when parasitized nymphs were exposed to the fungus blastospores before or after host mummification; 2) Parasitoid survival when mummies containing larvae or pupae were exposed to the fungus hyphae; 3) Parasitoid oviposition on fungus-infected hosts with or without visible hyphae. It was found that topical application of blastospore formulation (7 × 106 spores/ml) onto the nymphs parasitized with 2nd instar parasitoid larvae (3-day after parasitism) reduced host mummification by 50% and parasitoid emergence by 85%. However, fungus-application on mummies containing 4th instar parasitoid larvae (6-day after parasitism) did not affect parasitoid emergence. Likewise, fungus application on mummies containing parasitoid pupae (9-day after parasitism) and covered with blastospores formed by the fungus hyphe did not affect parasitoid emergence.

6.1.2. Effect of Fungi on the Treated Adults

The fungus, Nomuraea rileyi did not affect the adults of the parasitoids, Voria ruralis (Fallen), Cotesia margiventris (Cresson), Campoletis sonorensis (Cameron) and Telenomus proditor Nixon when exposed to high concentrations of conidia (25 times higher than used in field experiments) [17]. Similar results were obtained for V. lecanii which did not infect the treated adults of whitefly parasitoid, Encarsia formosa [57]. Also, adult of Cotesia plutellae (Kurdjumov), a larval parasitoid of P. xylostella, was proved to be not susceptible to Zoophthora radicans (Zygomycetes: Entomophthorales) [58]. In contrast, 90% mortality in adults of the parasitoid, Diadegma semiclausum (Hellen), a larval parasitoid of P. xylostella was recorded when sprayed with the fungus, Z. radicans [59]. Also, the fungus, P. neoaphidis took 8 - 9 days to kill the adults of the aphid parasitoid, Aphidius rhopalosiphi De Stefani-Perez [46].

Applying B. bassiana and M. anisopliae at a concentration of 107 conidia/ml killed 48% and 40%, respectively, of the adults of Cephalonomia stephanoderis Betrem (Hym.: Bethylidae), the parasitoid of the coffee berry borer, Hypothenemus hampei Ferrari (Col.:Curculionidae) [60]. However, exposure of adults of the parasitoids, Bracon hebetor and Anagyrus lopezi (De Santis) (Hym.: Encyrtidae) to one isolate of B. bassiana and 11 isolates of M. anisopliae resulted in 100% mortality of both parasitoids [61]. The effect of direct spraying of B. bassiana at a concentration of 2 × 108 conidia/ml on longevity and fecundity of D. semiclausum was investigated [62]. The results showed that all fungus-treated wasps died within 4 days and all incubated cadavers showed characteristic mycosis. However, when the female was introduced immediately after treatment to healthy P. xylostella host larvae, the average number of parasitoid pupae produced/female was 5.1 compared to 18 pupae/untreated female in 4 days. The LC50 values for adults of the larval parasitoid, Trybliographa rapae Westwood (Hym.: Figitidae) of Delia radicum (L.) (Dipt.: Anthomyiidae) were 1.83 × 107 and 1.57 × 107conidia/ml by B. bassiana and M. brunneum, respectively [63].

6.2. Field Experiments6.2.1. Direct Effect of Fungi on Parasitoids

A commercially formulated isolate of B. bassiana was found to be highly efficient in greenhouses against whiteflies, thrips and mites but with no impact on beneficial insects [61]. Similarly, in a large scale experiment, it was found that the reproductive success of Aphidius ervi (a parasitoid of the pea aphid, Acyrthosiphon pisum) was not affected by applying the fungus, P. neoaphidis [64].

6.2.2. Combined Effects of EPF and Parasitoids

The fungus, Hirsutella cryptoscleroium reduced levels of parasitism by Gyranusoidea tebya (Hym.: Encyrtidae) on the mealybug, Rastrococcus invadens Williams (Homoptera: Pseudococcidae) but the overall mortality of the mealybug was greater than when both natural enemies acted separately [65]. B. bassiana and M. anisopliae were applied on artificially infested coffee branches by the coffee borer, Hypothenemus hampei (Col.: Curculionidae), at a concentration of 7.9 × 109 conidia/tree [60]. Application was carried out 21, 14, 7 and 0 days before releasing the parasitoid, Cephalonomia stephanoderis (Hym.: Bethylidae), and 2, 4 and 7 days after release. The results showed that the highest mortality of the parasitoids (24% by B. bassiana and 5% by M. anisopliae) occurred when fungi were sprayed on the same day of the parasitoid release. In all other treatments, however, the mortalities were less than 7% and did not differ significantly from the untreated control.

In contrast, there was an additive effect with regard to aphid control with no detrimental effects on percentage of parasitism or parasitoid emergence when the fungus, P. fumosoroseus and the parasitoid, Aphelinus asychis (Walker) (Hym.: Aphelinidae) were used together for the control of wheat aphid, Diuraphis noxia Kurdjumov under field conditions [66]. Similarly, in a large scale experiment, it was found that the reproductive success of Aphidius ervi Haliday (a parasitoid of the pea aphid, Acyrthosiphon pisum (Harris) was not affected by the fungus, Pandora neoaphidis [64]. Also, in greenhouses over an extended time experiments, the combined use of the fungus B. bassiana (BotaniGard Commercial Product) and the parasitoid Aphidius matricariae as bio-control agents for the peach aphid, M. persicae had synergistic effects on aphid suppression. In addition, the numbers of parasitoids presented at the end of longer scale experiments were higher in treatments with B. bassiana and the parasitoid than in treatments with the parasitoid alone [50].

With appropriate timing, each of the parasitoids, Aphidius matricariae (Haliday) and A. colemani (Dalman) could be combined with B. bassiana for the biological control of the aphid, M. persicae [44]. Likewise, B. bassiana or M. brunneum were found to be compatible with A. colemani against M. persicae without any negative interactions between them [67]. Also, the parasitoid, A. colemani and the fungus, Lecanicillium muscarium (Ascomycota: Hypocreales) could be used together for the control of the aphid, M. persicae [68].

6.2.3. Transmission of EPF by Parasitoids

Adults of the ichneomonid larval parasitoid, D. semiclausum, contaminated with the spores of the fungus, Z. radicans was not infected and did not transmit the fungus to the populations of its host P. xylostella [59]. However, treatment of D. semiclusum adult by the same fungus prior to exposure to P. xylostella larvae significantly reduced the number of parasitoid cocoons developed from host larvae [58]. In a large scale experiment, enhancing of transmission of B. bassiana to the pea aphid, Acyrthosiphon pisum, in the presence of its parasitoid, Aphidius ervi was observed [64].

6.2.4. Discrimination between Healthy and Fungi-Infected Hosts

The females of the aphid parasitoid, Aphidius rhopalosiphi (De Stephani-Perez) could discriminate between B. bassiana-infected and uninfected hosts and deposited lower numbers of eggs in the infected hosts [69]. Similar results were obtained with the egg parasitoid, Anagrus atomus (L.) of the green leafhopper, Emposca decipines Paoli treated with B. bassiana [70]. Also, the female of the parasitoid, Encarsia formosa was able to detect and reject the whitefly T. vaporariorum nymphs treated with the fungus, Aschersonia aleyrodis (Deuteromycotina: Coelomycetes) 7 days post fungus application [71].

In contrast, the females of Cotesia plutellae (Kurdjumov) and D. semiclausum did not discriminate between Z. radicans-treated and untreated P. xylostella larvae and no difference in oviposition attempts was noticed [58]. Similarly, adult females of the bethylid ecto-parasitoid, Cephalonomia tarsalis (Ashmead) laid eggs on B. bassiana-infected larvae of its host, Oryzaephilus surinamensis (L.) (Col.: Silvanidae) up to within one day of the host-death [72]. However, D. semiclausum could recognize B. bassiana-infected P. xylostella larvae and did not attempt to oviposit in dead larvae [62]. Also, Trybliographa rapae females, (Hym.: Figitidae) could discriminate between healthy and infected Delia radicum (L.) (Dipt.: Anthomyiidae) larvae and laid significantly more eggs in healthy larvae than in the M. brunneum-infected ones. In contrast, the numbers of eggs laid in healthy larvae and in those infected with B. bassiana did not differ significantly [63].

7. Conclusions

Laboratory experiments revealed that fungi-treatment of larvae and adults of predators may cause mortality or detrimental effects on such insects depending on the species of the fungus and its concentration. Mostly, the predators avoid feeding on fungus-infected prey. Different fungi species could be isolated from hibernating and field collected adult predators. Some field studies proved that EPF can be combined with different predator species as bio-control agents of insect pests.

In general, the negative impact of fungi on the development of the parasitoids on or inside the treated hosts depends on the time between infection and parasitism. Fungus-treatment of parasitoids’ adults causes different rates of mortality in such adults. The field studies demonstrated the success of the combination between fungi and parasitoids as bio-control agents against insect pests. Despite such results, efforts should be done to obtain EPF products capable of acting at lower R.H. in order to expand the commercial use of fungi as bio-control agents.

Conflicts of Interest

The author declares that he has no competing interests.

Cite this paper

Abbas, M.S.T. (2020) Interactions between Entomopathogenic Fungi and Entomophagous Insects. Advances in Entomology, 8, 130-146. https://doi.org/10.4236/ae.2020.83010

Abbreviations

Entomopathogenic Fungi (EPF), Intraguild Predation (IGP)

ReferencesRosenheim, J.A., Kaya, H.K., Ehler, L.E., Marois, J.J. and Jaffee, B.A. (1995) Intraguild Predation among Biological Control Agents: Theory and Evidence. Biological Control, 5, 303-335. https://doi.org/10.1006/bcon.1995.1038Labauda, S. and Griffin, C.T. (2018) Transmission Success of Entomopathogenic Nematodes Used in Pest Control. Insects, 9, 72-91. https://doi.org/10.3390/insects9020072Beline, T. (2018) Entomopathogenic Nematodes as Biocontrol Agents of Insect Pests. CAB Reviews, 13, No. 58. http://www.cabi.org/cabreviews http://www.iobcwprs.org/ip_ipm/03021_IOBCWorkingDocumentPesticides_Explanation.pdf https://doi.org/10.1079/PAVSNNR201813058Ferguson, K.I. and Stiling, P. (1996) Non-Additive Effects of Multiple Natural Enemies on Aphid Populations. Oecologia, 108, 375-379. https://doi.org/10.1007/BF00334664Hajek, A.E. and Butler, L. (2000) Predicting the Host Range of Entomopathogenic Fungi. In: Follete, P.A. and Duan, J.J., Eds., Non Target Effect of Biological Control, Kluwer Academic Publishers, Dordrecht, 263-276. https://doi.org/10.1007/978-1-4615-4577-4_15Pendland, J.C. and Boucias, D.G. (1982) Ultrastructural Aspects of Conidogenesis in the Entomogenous Hyphomycete, Nomuraea rileyi. Canadian Journal of Botany, 60, 26-33. https://doi.org/10.1139/b82-004Nalepa, C.A. and Weir, A. (2007) Infection of Harmonia axyridis (Coleoptera: Coccinellidae) by Hesperomyces virescens (Ascomycetes: Laboulbeniales): Role of Mating Status and Aggregation Behavior. Journal of Invertebrate Pathology, 94, 196-203. https://doi.org/10.1016/j.jip.2006.11.002Scorsetti, A.C., Pelizza, S. and Cabello, M.N. (2012) New Records of Hypocrealean Fungi Infecting Aphids and Whiteflies: Pathogenicity against Myzus persicae and Interaction with Its Predator, Eriopis connexa. Biocontrol Science and Technology, 22, 1099-1105. https://doi.org/10.1080/09583157.2012.710320Kiselek E.V. ,et al. (1975)The Effect of Bio-Preparations on Insect Enemies Zashchita Rastenii 12, 23-25.James, R.R. and Lighthart, B. (1994) Susceptibility of the Convergent Lady Beetle (Coleoptera: Coccinellidae) to Four Entomogenous Fungi. Environmental Entomology, 23, 190-192. https://doi.org/10.1093/ee/23.1.190Mahmoud B.A. ,et al. (2011)The Effects of Beauveria bassiana and Methylamineavermectin (Radical) on Spodoptera littoralis and Two Non-Target Insects, Coccinella septempunctata and Chrysoperla carnea Journal of the Egyptian Society of Parasitology 44, 85-93.Trizelia, L., Munzir, B. and Agung, P. (2017) Pathogenicity of Entomopathogenic Fungi, Metarhizium spp. against Predator, Menochilus sexmaculatus Fabricius (Coleoptera: Coccinelidae). Asian Journal of Agriculture, 1, 1-5. https://doi.org/10.13057/asianjagric/g010101Sewify, G.H. and El-Arnaouty, S.A. (1998) The Effect of Verticillium lecanii (Zimm.) on Larvae of Chrysoperla carnea in the Laboratory. Acta Zoologica Fennica, 209, 233-237.Aqueel, M. and Leather, S.R. (2013) Virulence of Verticillium lecanii (Z.) against Cereal Aphids: Does Timing of Infection Affect the Performance of Parasitoids and Predators? Pest Management Science, 69, 493-498. https://doi.org/10.1002/ps.3398Valez, M.P.J. (2008) Compatibility of the Entomopathogenic Fungus, Lecanicillium longisporum with the Predatory Midge, Aphidoletes aphidimyza. M.Sc. Thesis, Dept. Biological Sciences, Simon Fraser University, Burnaby.Scorsetti, A.C., Pelizza, S., Fogel, M.N., Vianna, F. and Schneider, M.I. (2017) Interactions between the Entomopathogenic Fungus, Beauveria bassiana and the Neotropical Predator, Eriopis connexa (Coleoptera: Coccinellidae): Implications in Biological Control of Pests. Journal of Plant Protection Research, 57.https://doi.org/10.1515/jppr-2017-0053Ignoffo, C.M. (1981) The Fungus Nomuraea rileyi as a Microbial Insecticide. In: Burges, H.D., Ed., Microbial Control of Pests and Plant Diseases, 1970-1980, Academic Press, San Diego.Bourassa, C., Vincent, C.J. and Mauffette, Y. (2001) Effect of Entomopathogenic Hyphomycetes against the Larger Grain Borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae), and Its Predator, Tretriosova nigriscens Lewis (Coleoptera: Histeridae). Journal of Invertebrate Pathology, 77, 75-80. https://doi.org/10.1006/jipa.2000.4986Roy, H.E., Brown, P.M.J., Rothery, P. and Majerus, M.E.N. (2008) Interaction between the Fungal Pathogen, Beauveria bassiana and Three Species of Coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. Bio-Control, 53, 265-276. https://doi.org/10.1007/s10526-007-9122-0Cottrell, T.E. and Shapiro-Ilan, D.I. (2008) Susceptibility of Endemic and Exotic North American Ladybirds (Coleoptera: Coccinellidae) to Endemic Fungal Entomopathogens. European Journal of Entomology, 105, 455-460. https://doi.org/10.14411/eje.2008.058Ana, C.S., Sebastian, P., Marilina, N.F., Florencia, V. and Marcela, I.S. (2017) Interactions between the Entomopathogenic Fungus, Beauveria bassiana, and the Neotropical Predator, Eriopis connexa (Coleoptera: Coccinellidae) Implications in Biological Control of Pests. Journal of Plant Protection Research, 57, 389-395.Saito, T. and Brownbridge, M. (2016) Compatibility of Soil-Dwelling Predators and Microbial Agents and Their Efficacy in Controlling Soil-Dwelling Stages of Western Flower Thrips, Frankleniella occidentalis. Biological Control, 92, 92-100. https://doi.org/10.1016/j.biocontrol.2015.10.003Wang, L., Huang, J., You, M. and Liu, B. (2005) Effect of Toxins from Two Strains of Verticillium lecanii (Hyphomycetes) on Bio-Attributes of Predatory Ladybeetle, Delphastus catalinae (Col., Coccinellidae). Journal of Applied Entomology, 129, 32-38. https://doi.org/10.1111/j.1439-0418.2005.00929.xAlma, C.R. (2005) Intraguild Interactions between Two Natural Enemies of the Greenhouse Whitefly, Trialieurodes vaporariorum (Hom.: Aleyrodidae), the Predator, Dicyphus hesperus (Het.: Miridae) and the Fungus Paecilomyces fumosoroseus. M.Sc. Thesis, Dept. of Biological Sciences, Simon Fraser University, Burnaby.Pell, J.K., Pluke, R., Clark, S.J., Kenward, M.G. and Alderson, P.G. (1997) Interactions between Two Aphid Natural Enemies, the Entomopathogenic Fungus Erynia neoaphidis Remaudière & Hennebert (Zygomycetes: Entomophthorales) and the Predatory Beetle Coccinella septempunctata L. (Coleoptera: Coccinellidae). Journal of Invertebrate Pathology, 69, 261-268. https://doi.org/10.1006/jipa.1996.4651Roy, H.E., Pell, J.K., Clark, S.J. and Alderson, P.G. (1998) Implication of Predator Foraging on Aphid Pathogen Dynamics. Journal of Invertebrate Pathology, 71, 236-247. https://doi.org/10.1006/jipa.1997.4736Pell, J.K. and Vandenberg, J.D. (1998) Paecilomyces fumosoroseus, Convergent Ladybirds and Russian Wheat Aphid: Potential Interactions. Insect Pathogens and Insect Parasitic Nematodes. IOBC Bulletin, 21, 133.Ormond, E.L., Thomas, A.P.M., Pell, J.K., Freeman, S.M. and Roy, H.E. (2011) Avoidance of a Generalist Entomopathogenic fungus by the Ladybird, Coccinella septempunctata. FEMS Microbiology Ecology, 77, 229-237. https://doi.org/10.1111/j.1574-6941.2011.01100.xOrmond, E.L., Thomas, A.P.M., Pell, J.K. and Roy, H.E. (2006) Overwintering Ecology of Coccinella septempunctata, Beauveria bassiana and Dinocampus coccinellae. In: Rossing, W.A.H., Eggenschwiler, L. and Poehling, H.-M., Eds., Working Group ‘‘Landscape Management for Functional Biodiversity’’, IOBC/WPRS Bulletin 29, 85-88.Mills, N.J. (1981) The Mortality and Fat Content of Adalia bipunctata during Hibernation. Entomologia Experimentalis et Applicata, 30, 265-268. https://doi.org/10.1111/j.1570-7458.1981.tb03109.xToledo, A.V., Remes Lincov, A.M.M. and Lopez Lastra, C.C. (2008) Host Range Findings on Beauveria bassiana and Metarhizium anisopliae (Ascomycota: Hypocreales) in Argentina. Boletin de la Sociedad Argentina de Botanica, 43, 211-220.Cottrell, T.E. and Shapiro-Ilan, D.I. (2003) Susceptibility of a Native and an Exotic Lady Beetle (Coleoptera: Coccinellidae) to Beauveria bassiana. Journal of Invertebrate Pathology, 84, 137-144. https://doi.org/10.1016/j.jip.2003.09.003Harwood, J.D., Ricci, C., Romani, R., Weir, A. and Obrycki, J.J. (2006) Prevalence and Association of the Fungus, Hesperomyces virescens (Laboulbenialis: Laboulbeniaceae) on Coccinellid Hosts (Coleoptera: Coccinellidae) in Kentucky, USA. European Journal of Entomology, 103, 799-804. https://doi.org/10.14411/eje.2006.109Reddick, E.W., Cottrell, T.E. and Kidd, K.A. (2009) Natural Enemies of the Coccinellidae: Parasites, Pathogens and Parasitoids. Biological Control, 51, 306-312. https://doi.org/10.1016/j.biocontrol.2009.05.008Roy, H.E. and Cottrell, T.E. (2008) Forgotten Natural Enemies: Interactions between Coccinellids and Insect Parasitic Fungi. European Journal of Entomology, 105, 391-398. https://doi.org/10.14411/eje.2008.049Steenberg, T. and Harding, S. (2009) Entomopathogenic Fungi Recorded from the Ladybird, Harmonia axiridis. Journal of Invertebrate Pathology, 102, 88-89. https://doi.org/10.1016/j.jip.2009.07.002James, R.R., Shaffer, B.T., Croft, B. and Lighthart, B. (1995) Field Evaluation of Beauveria bassiana: Its Persistence and Effects on the Pea Aphid and Non-Target Coccinellids in Alfalfa. Bio-Control Science and Technology, 5, 425-437. https://doi.org/10.1080/09583159550039620Jacobson, R.J., Chandler, D., Fenlon, J. and Russell, K.M. (2001) Compatibility of Beauveria bassiana (Balsamo) Vuillemin with Amblyseius cucumeris Oudemans (Acarina: Phytoseiidae) to Control Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) on Cucumber Plants. Biocontrol Science and Technology, 11, 391-400. https://doi.org/10.1080/09583150120055808Cloyd, R.A., Timmons, N.R., Goebel, J.M. and Kemp, K.E. (2009) Effect of Pesticides on Adult Rove Beetle Atheta coriaria (Coleoptera: Staphylinidae) Survival in Growing Medium. Journal of Economic Entomology, 102, 1750-1758. https://doi.org/10.1603/029.102.0504Bayissa, W., Ekesia, S., Mohamed, S.A., Kayaab, G.P., Wagachab, J.M. and Maninia, N.K. (2016) Interactions among Vegetable-Infesting Aphids, the Fungal Pathogen Metarhizium anisopliae (Ascomycota: Hypocreales) and the Predatory Coccinellid Cheilomenes lunata (Coleoptera: Coccinellidae). Biological Science and Technology, 26, 274-290. https://doi.org/10.1080/09583157.2015.1099148Compos de Azevedo, A.G., Steinwender, B.M., Eilenberg, J. and Sigsgaard, L. (2017) Interactions among the Predatory Midge, Aphidoletis aphidimyza (Dip.: Cecidomyiidae), the Fungal Pathogen, Metarhizium brunneum (Ascomycota: Hypocreales) and Maize-Infesting Aphids in Greenhouse Mesocosms. Insects, 8, 44. https://doi.org/10.3390/insects8020044Roy, H.E. (1997) Interaction between Aphid Predators and the Entomopathogenic Fungus, Erynia neoaphidis. PHD Thesis, Nottingham University, Nottingham.Roy, H.E. and Pell, J.K. (2000) Interactions between Entomopathogenic Fungi and Other Natural Enemies: Implication for Biological Control. Biocontrol Science and Technology, 10, 737-752. https://doi.org/10.1080/09583150020011708Emami, F., Alichi, M. and Minaei, K. (2013) Interaction between the Entomopathogenic Fungus, Beauveria bassiana (Ascomycota: Hypocreales) and the Parasitoid Wasp, Aphidius colemani Viereck (Hymenoptera: Braconidae). Journal of Entomological and Acarological Research, 45, 205-209. https://doi.org/10.4081/jear.2013.e4King, E.G. and Bell, V. (1978) Interaction between a Braconid, Microplitis croceipes, and a Fungus, Nomuraea rileyi, in Laboratory-Reared Bollworm Larvae. Journal of Invertebrate Pathology, 31, 337-340. https://doi.org/10.1016/0022-2011(78)90225-2Powell, W., Wilding, N., Brobyn, P.J. and Clark, S.J. (1986) Interference between Parasitoids [Hym.: Aphidiidae] and Fungi (Entomophthorales) Attacking Cereal Aphids. Entomophaga, 31, 293-302. https://doi.org/10.1007/BF02373339Van de Vier, M. and Degheee, D. (1996) Toxicity of the Fungal Pathogen, Paecilomysces fumosoroseus to the Greenhouse Whitefly, Trialeurodes vaporariorum and the Parasitoid, Encarsia formosa. The First Results of a Control Experiment in Glasshouses. OILB/SROP Bulletin: Proc. of the Meeting: Integrated Control in Glasshouses, Vienna, 20-25 May 1996, 191-194.Askary, H. and Brodeur, J. (1999) Susceptibility of Larval Stage of the Aphid Parasitoid, Aphidius nigripes to the Entomopathogenic Fungus Verticillium lecanii. Journal of Invertebrate Pathology, 73, 129-132. https://doi.org/10.1006/jipa.1998.4824Rashki, M., Kharazi-Pakdel, A., Allahyari, H. and Van Alphen, J.J.M. (2009) Interactions among the Entomopathogenic Fungus, Beauveria bassiana (Ascomycota: Hypocreales), the Parasitoid, Aphidius matricariae (Hymenoptera: Braconidae), and Its Host, Myzus persicae (Homoptera: Aphididae). Biological Control, 50, 324-328. https://doi.org/10.1016/j.biocontrol.2009.04.016Narouzi, Y. (2013) Compatibility of the Parasitoid, Aphidius matricareae with BotaniGard for the Control of Greenhouse Aphids. M.S. Thesis, Dept. Biological Science, Faculty of Science, Simon Fraser University, Burnaby.Martins, I.C.F., Silva, R.J., Alencar, D.C.C., Silva, K.P. and Polanczyk, R.A. (2014) Interactions between the Entomopathogenic Fungi Beauveria bassiana (Ascomycota: Hypocreales) and the Aphid Parasitoid Diaeretiella rapae (Hymenoptera: Braconidae) on Myzus persicae (Hemiptera: Aphididae). Journal of Economic Entomology, 107, 933-938. https://doi.org/10.1603/EC13542Mahdavi, V., Saber, M., Rafiee-Dastjerdi, H. and Mehrvar, A. (2013) Susceptibility of the Hymenopteran Parasitoid, Habrobracon hebetor (Say) (Braconidae) to the Entomopathogenic Fungi, Beauveria bassiana and Metarhizium anisopliae Sorokin. Jordan Journal of Biological Sciences, 6, 17-20. https://doi.org/10.12816/0000253Jarrahi, A. and Safavi, S.A. (2016) Sub-Lethal Effects of Metarhizium anisopliae on Life Table Parameters of Habrobracon hebetor Parasitizing Helicoverpa armigera Larvae at Different Time Intervals. Bio-Control, 61, 167-175. https://doi.org/10.1007/s10526-015-9707-yTamayo-Mejia, F., Tamezguera, P., Guzman-Franco, A.W. and Gomez-Flores, R. (2015) Can Beauveria bassiana and Tamarixia triozae (Hym.: Eulophidae) Be Used Together for Improved Biological Control of Bactericera cockerelli (Hemiptera: Triozidae)? Biological Control, 90, 42-48. https://doi.org/10.1016/j.biocontrol.2015.05.014Tamayo-Mejia, F., Tamez-Guerra, P., Guzman-Franco, A.W. and Gomez-Flores, R. (2016) Developmental Stage Affects Survival of the Ectoparasitoid, Tamarixia triozae Exposed to the Fungus Beauveria bassiana. Biological Control, 93, 30-36. https://doi.org/10.1016/j.biocontrol.2015.11.006Chow, A., Dunlap, C.A., Jackson, M.A., Flores, D., Patt, J.M. and Setamou, M. (2016) Oviposition Behavior and Survival of Tamarixia radiata (Hym.: Eulophidae), an Ectoparasitoid of Diaphorina citri (Hem.: Liviidae) on Hosts Exposed to the Entomopathogenic Fungus Isaria fumosorosea (Hypocreales: Cordycipitaceae) under Laboratory Conditions. Journal of Economic Entomology, 2016, 1-11.Hall, R.A. (1981) The Fungus, Verticillium lecanii as a Microbial Insecticide against Aphids and Scales. In: Burges, H.D., Ed., Microbial Control of Pest and Plant Diseases, 1970-1980, Academic Press, San Diego.Furlong, M.J. and Pell, J.K. (2000) Conflicts between a Fungal Entomopathogen Zoophthora radicans and Two Larval Parasitoids of the Diamond-Back Moth. Journal of Invertebrate Pathology, 76, 85-94. https://doi.org/10.1006/jipa.2000.4943Furlong, M.J. and Pell, J.K. (1996) Interaction between the Fungus Entomopathogen Zoophthora radicans Brefeld (Entomophthorales) and Two Hymenopteran Parasitoids Attacking the Diamond-Back Moth, Plutella xylostella. Journal of Invertebrate Pathology, 68, 15-21. https://doi.org/10.1006/jipa.1996.0053Aristizabal, I., Pardey, A. and Cordoba, B.C. (1995) Effect of Beauvaria bassiana and Metarhizium anisopliae on the Coffee Berry Borer Parasitoid, Cephalonomia stephannoderis. Revista Colombiana de Entomologia, 21, 199-204.Danfa, A. and Van den Valk, H.C.H.G. (1999) Laboratory Testing of Metarhizium spp. and Beauveria bassiana on Sahelian Non-Target Arthropods. Bio-Control Science and Technology, 9, 187-198. https://doi.org/10.1080/09583159929776Madurappulige, P. (2005) Effect of Beauveria bassiana on Diadegma semiclausum (Ichneumonidae), a Parasitoid of Plutella xylostella (Lep.: Yponomeutidae). PhD Thesis, Lincoln University, Lincoln, 171 p.Rannback, L.M., Cotes, B., Anderson, P., Rämert, B. and Meyling, N.V. (2014) Mortality Risk from Entomopathogenic Fungi Affects Oviposition Behavior in the Parasitoid Wasp Trybliographa rapae. Journal of Invertebrate Pathology, 124, 78-86. https://doi.org/10.1016/j.jip.2014.11.003Baverstock, J., Clark, S.J., Alderson, P.G. and Pell, J.K. (2009) Intraguild Interactions between the Fungus, Pandora neoaphidis and an Aphid Predator at Population Scales. Journal of Invertebrate Pathology, 102, 167-172. https://doi.org/10.1016/j.jip.2009.07.014Akalach, M., Fernandez-Garcia, E. and Moore, D. (1992) Interaction between Rastrococcus invadens (Hom.: Pseudococcidae) and Two Natural Enemies. Entomophaga, 37, 99-106. https://doi.org/10.1007/BF02372978Mesquita, A.L.M., Lacey, L.A. and Leclant, F. (1997) Individual and Combined Effects of the Fungus, Paecilomyces fumosoroseus and Parasitoid, Aphelinus asychis Walker (Hym., Aphelinidae) on Confined Populations of Russian Wheat Aphid, Diuraphis noxia (Mordvilko) (Hom., Aphididae) under Field Conditions. Journal of Applied Entomology, 121, 155-163. https://doi.org/10.1111/j.1439-0418.1997.tb01386.xJaber, R. and Araj, S.E. (2018) 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). Biological Control, 116, 53-61. https://doi.org/10.1016/j.biocontrol.2017.04.005Mohammed, A.A. and Hatcher, P.E. (2017) Combining Entomopathogenic Fungi and Parasitoids to Control the Green Peach Aphid, Myzus persicae. Biological Control, 110, 44-55. https://doi.org/10.1016/j.biocontrol.2017.03.012Brobyn, P.J., Clark, S.J. and Wilding, N. (1988) The Effect of Fungus Infection of Metopolophium dirhodum [Hom.: Aphididae] on the Oviposition Behaviour of the Aphid Parasitoid Aphidius rhopalosiphi [Hym.: Aphidiidae]. Entomophaga, 33, 333-338. https://doi.org/10.1007/BF02372623Tounou, A.K., Agboka, A., Poehling, H.M., Ranpack, K. and Borgemeister, C. (2003) Evaluation of the Entomopathogenic Fungi Metarhizium anisopliae and Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) for Control of the Green Leafhopper Empoasca decipiens (Homoptera: Cicadellidae) and Potential Side Effects on the Egg Parasitoid Anagrus atomus (Hymenoptera: Mymaridae). Biocontrol Science and Technology, 13, 715-728. https://doi.org/10.1080/09583150310001606534Fransen, J.J. and van Lenteren, J.C. (1993) Host Selection and Survival of the Parasitoid, Encarsia Formosa on Greenhouse Whitefly, Trialeurodes vaporariorum in the Presence of Hosts Infected with the Fungus, Aschersonia aleyrodis. Entomologia Experimentalis et Applicata, 69, 239-249. https://doi.org/10.1111/j.1570-7458.1993.tb01747.xLord, J. (2001) Response of the Wasp Cephalonomia tarsalis (Hymenoptera: Bethylidae) to Beauveria bassiana (Hyphomycetes: Moniliales) as Free Conidia or Infection in Its Host, the Sawtoothed Grain Beetle, Oryzaephilus surinamensis (Coleoptera: Silvanidae). Biological Control, 21, 300-304. https://doi.org/10.1006/bcon.2001.0942