SavedAdd your journal

Journals / Türkiye Teknoloji ve Uygulamalı Bilimler Dergisi / 2026 / Cilt: 6 Sayı: 2

Interactions Between Parasitoids and Entomopathogenic Fungi: Approaches for Sustainable Agriculture

Parazitoidler ve Entomopatojenik Mantarlar Arasındaki Etkileşimler: Sürdürülebilir Tarıma Yönelik Yaklaşımlar

Pınar Güner(BALIKESİR ÜNİVERSİTESİ, FEN-EDEBİYAT FAKÜLTESİ)0000-0001-6922-7009
Aylin Er(BALIKESİR ÜNİVERSİTESİ)0000-0002-8108-8950
Tülin Aşkun(BALIKESİR ÜNİVERSİTESİ)0000-0002-2700-1965
Pages
143–164
Publication Date
2025-10-19
🏛️Bibliographic metadata and full text access for this article are provided via DergiPark.
DergiPark Record ↗
✨

AI Summary & Key Takeaways

AI Insight
⚡ TL;DR(Too Long; Didn't Read)

Some entomopathogenic fungi infect both host insects and parasitoids, reducing parasitoid survival rates, development processes, and overall efficiency.

📌 3 Key Takeaways

🎯
Objective & Hypothesis:Fungi play a significant role in agroecosystems by directly or indirectly influencing parasitoid-host dynamics, thereby contributing to biological control.
📊
Key Findings & Data:Some entomopathogenic fungi infect both host insects and parasitoids, reducing parasitoid survival rates, development processes, and overall efficiency.
💡
Conclusion & Impact:This review highlights the roles of some entomopathogenic fungal species associated with parasitoids in these multifaceted interactions and discusses their potential applications in integrated pest management.
🔬Design:Review & Systematic Survey
📍Scope:Comprehensive Sample
⚙️Variables:Entomopatojen · parazitoit · biyolojik mücadele

Abstract

Fungi play a significant role in agroecosystems by directly or indirectly influencing parasitoid-host dynamics, thereby contributing to biological control. Some entomopathogenic fungi infect both host insects and parasitoids, reducing parasitoid survival rates, development processes, and overall efficiency. Other fungi can alter host physiology and immune systems, either enhancing or diminishing the success of parasitoid infection. These processes are crucial factors in determining the effectiveness of pest control and maintaining ecological balance. Understanding the interactions between fungi, parasitoids, and hosts is essential for improving biological control programs and developing sustainable pest management strategies. This review highlights the roles of some entomopathogenic fungal species associated with parasitoids in these multifaceted interactions and discusses their potential applications in integrated pest management.

Özet

Funguslar, agroekosistemlerde parazitoit-konak dinamiklerini doğrudan veya dolaylı yollarla etkileyerek biyolojik mücadelede önemli roller üstlenmektedir. Bazı entomopatojenik funguslar, hem konak böcekleri hem de parazitoitleri enfekte ederek parazitoitlerin hayatta kalma oranlarını, gelişim süreçlerini ve etkinliğini azaltabilir. Diğer bazı funguslar ise konağın fizyolojisini ve bağışıklık sistemini değiştirerek parazitoitlerin konağı enfekte etme başarısını artırabilir veya azaltabilir. Bu süreçler, zararlı kontrolünün etkinliğini ve ekolojik dengenin korunmasını doğrudan belirleyen unsurlardır. Fungusların parazitoitler ve konaklarla olan etkileşimlerini anlamak, biyolojik mücadele programlarının daha etkin hale getirilmesi ve sürdürülebilir zararlı yönetimi yaklaşımlarının geliştirilmesi açısından büyük önem taşımaktadır. Bu derleme, parazitoitler ile ilişki içinde olan bazı entomopatojen fungus türlerinin bu çok yönlü etkileşimlerdeki rollerini vurgulamakta ve entegre zararlı yönetimindeki potansiyel uygulamalarını ele almaktadır.

🔖

Cite This Article

Güner, P., Er, A., Aşkun, T. (2025). Interactions Between Parasitoids and Entomopathogenic Fungi: Approaches for Sustainable Agriculture. Türkiye Teknoloji ve Uygulamalı Bilimler Dergisi, Cilt: 6 Sayı: 2, 143–164. https://doi.org/10.70562/tubid.1683699

📄 Full Text PDF Viewer

📄

PDF görüntüleyici hazırlanıyor...

References (100)

  1. Labauda S, Griffin CT. Transmission Success of Entomopathogenic Nematodes Used in Pest Control. Insects. 2018;9:72-91. doi.org/10.3390/insects9020072.
  2. Gonzalez F, Tkaczuk C, Dinu MM, Fiedler Z, Vidal S, Zchori-Fein E, Messelink GJ. New opportunities for the integration of microorganisms into biological pest control systems in greenhouse crops. J Pest Sci. 2016;89(2):295–311. doi.org/10.1007/s10340-016-0751-x.
  3. Mesquita ALM, Lacey LA. Interactions among the entomopathogenic fungus, Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes), the parasitoid, Aphelinus asychis (Hymenoptera: Aphelinidae) and their aphid host. Biol Control. 2001;22(1):51–59. doi. org/10.1006/bcon.2001.0950.
  4. Rashki M, Kharazi-Pakdel A, Allahyari H, Van Alphen, JJM. Interactions among the entomopathogenic fungus, Beauveria bassiana (Ascomycota: Hypocreales), the parasitoid, Aphidius matricariae (Hymenoptera: Braconidae), and its host, Myzus persicae (Homoptera: Aphididae). Biol Control. 2009;50(3):324–328. doi.org/10.1016/j. biocontrol.2009.04.016.
  5. Hochberg ME. Intra-host interactions between a braconid endoparasitoid, Apanteles glomeratus, and a baculovirus forlarvae of Pieris brassicae. J Anim Ecol. 1991a;60(1):51-63. doi.org/10.2307/5444.
  6. Hochberg ME. Extra-host interactions between a braconid endoparasitoid, Apanteles glomeratus, and a baculovirus forlarvae of Pieris brassicae. J Anim Ecol. 1991b;60, 65-77. doi.org/10.2307/5445.
  7. Powell W, Wilding N, Brobyn PJ, Clark SJ. Interference between Parasitoids (Hym.: Aphidiidae) and Fungi (Entomophthorales) Attacking Cereal Aphids. Entomophaga. 1986;31:293-302. doi.org/10.1007/BF02373339.
  8. Fransen JJ, van Lenteren JC. 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. Entomol Exp Appl.1993;69:239-249. doi.org/10.1111/j.1570-7458.1993.tb01747.x.
  9. Beline T. Entomopathogenic Nematodes as Biocontrol Agents of Insect Pests. CAB Reviews. 2018;13:58. doi.org/10.1079/PAVSNNR201813058.
  10. Straub CS, Finke DL, Snyder WE. Are the conservation of natural enemy biodiversity and biological control compatible goals. Biol Control. 2008;45:225-237. doi.org/10.1016/j.biocontrol.2007.05.013.
  11. Roy HE, Pell JK. Interactions between entomopathogenic fungi and other natural enemies: Implications for biological control. Biocontrol Sci Technol. 2000;10:737–752. doi.org/10.1080/09583150020011708.
  12. Roy H, Steinkraus DC, Eilinberg J, Hajek AE, Pell JK. Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol. 2006;51:331–357. doi.org/10.1146/annurev.ento.51.110104.150941.
  13. Ormond E, Thomas APM, Pell JK, Freeman SN, Roy HE. Avoidance of a generalist entomopathogenic fungus by the ladybird, Coccinella septempunctata. FEMS Microbiol Ecol. 2011;77:229–237. doi.org/ 10.1111/j.1574-6941.2011.01100.x.
  14. Martins ICF, Silva RJ, Alencar DCC, Silva KP, Polanczyk RA. Interactions between the Entomopathogenic Fungi Beauveria bassiana (Ascomycota:Hypocreales) and the Aphid Parasitoid Diaeretiella rapae (Hymenoptera: Braconidae) on Myzus persicae (Hemiptera: Aphididae). J Econ Entomol. 2014;107:933-938. doi.org/10.1603/EC13542.
  15. Bayissa W, Ekesia S, Mohameda SA, Kaayab GP, Wagachab JM, Hanna R, Maniania NK. Interactions among vegetable infesting aphids, the fungal pathogen Metarhizium anisopliae (Ascomycota: Hypocreales) and the predatory coccinellid Cheilomenes lunata (Coleoptera: Coccinellidae). Biocontrol Sci Technol. 2016;26(2): 274–290. doi.org/ 10.1080/09583157.2015.1099148.
  16. Baverstock J, Clark SJ, Alderson PG, Pell JK. Intraguild Interaction between the Fungus, Pandora neoaphidis and an Aphid Predator at PopulationScales. J Invertebr Pathol. 2009;102:167-172.
  17. Kim JJ, Kim KC, Roberts DW. Impact of the entomopathogenic fungus Verticillium lecanii on development of an aphid parasitoid, Aphidius colemani. J Invertebr Pathol. 2005;88:254-256. doi.org/ 10.1016/j.jip.2005.01.004.
  18. Aiuchi D, Saito Y, Tone J, Kanazawa M, Tani M, Koike M. The effect of entomopathogenic Lecanicillium spp. (Hypocreales: Cordycipitaceae) on the aphid parasitoid Aphidius colemani (Hymenoptera: Aphidiinae). Appl Entomol Zool. 2012;47:351-357. doi.org/10.1007/s13355-012-0125-7.
  19. Emami F, Alichi M, Minaei K. Interaction between the Entomopathogenic Fungus, Beauveria bassiana (Ascomycota: Hypocreales) and the Parasitoid Wasp, Aphidius colemani Viereck (Hymenoptera: Braconidae). J Entomol Acarol Res. 2013;45:205-209. doi.org/10.4081/jear.2013.e4.
  20. Demirbağ Z, Nalçacıoğlu R, Katı H, Demir İ, Sezen K, Ertürk O. Entomopatojenler ve Biyolojik Mücadele. Trabzon, Esen Ofset Matbaacılık; 2008.
  21. Güner P, Aşkun T, Er A. Entomopathogenic Fungi and Their Potential Role In The Sustainable Biological Control of Storage Pests. Commagene J Biol. 2023;7(1):90-97. doi.org/10.31594/commagene.1284354.
  22. Chen W, Xie W, Cai W, Thaochan N, Hu Q. Entomopathogenic Fungi Biodiversity in the Soil of Three Provinces Located in Southwest China and First Approach to Evaluate Their Biocontrol Potential. J Fungi. 2021;7:984. doi.org/10.3390/jof7110984.
  23. Humber RA. Evaluation of Entomopathogenicity in Fungi. J Invertebr Pathol. 2008;98:262-266. doi.org/10.1016/j.jip.2008.02.017.
  24. Cho EM, Kirkland BH, Holder DJ, Keyhani NO. Phage display cDNA cloning and expression analysis of hydrophobins from the entomopathogenic fungus Beauveria bassiana (Cordyceps). Microbiol. 2007;153(10):3438–3447. doi.org/10.1099/mic.0.2007/008532-0.
  25. Ye C, Song ZT, Wu W, Zhang NU, Saba L, Xing L. Endocuticle is involved in caste differentiation of the lower termite. Curr Zool. 2021;67(5):489–499. doi.org/10.1093/cz/zoab005.
  26. Skinner M, Parker BL, Kim JS. Role of Entomopathogenic Fungi in Integrated Pest Management. J Integr Pest Manag. 2014;169–191. doi.org/10.1016/B978-0-12-398529-3.00011-7.
  27. Ortiz-Urquiza A, Keyhani, NO. Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects. 2013;4(3):357–374. doi.org/10.3390/insects4030357.
  28. Soliman NA. Toxicological and biochemical Effects of Beauveria bassiana (Bals.) on Peach fruit fly, Bactrocera zonata (Saunders) Immature Stage. J Plant Prot Pathol. 2020; 11(11):579–585. doi.org/10.21608/jppp.2020.133805.
  29. Aşkun T, Er A, Güner P, Deniz M. The Role of Fungal Chitinases in Biological Control: Advances in Science and Mathematics;2024.
  30. Pedrini N, Crespo R, Juárez MP. Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comparative Biochemistry and Physiology Part C. Toxicol Pharmacol. 2007;146(1-2):124–137. doi.org/10.1016/j.cbpc.2006.08.003.
  31. Santi L, Beys da Silva WO, Berger M, Guimarães JA, Schrank A, Vainstein MH. Konidial surface proteins of Metarhizium anisopliae: Source of activities related with toxic effects, host penetration and pathogenesis. Toxicon. 2010;55(4):874–880. doi.org/10.1016/j.toxicon.2009.12.012.
  32. Litwin A, Nowak M, Różalska S. Entomopathogenic fungi: unconventional applications. Rev Environ Sci Bio. 2020;19(1):23–42. doi.org/10.1007/s11157-020-09525-1.
  33. Rahman MM, Roberts HLS, Schmid O. Factors affecting growth in the Venturia canescens in the flour moth Ephestia kuehniella. J Insect Physiol. 2007;53:463–467. doi.org/10.1016/j.jinsphys.2007.01.007.
  34. Beckage NE, Gelman DB. Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu Rev Entomol. 2004;49:299-330. doi.org/10.1146/annurev.ento.49.061802.123324.
  35. Er A. Endoparazitoit Pimpla turionellae (L.) (Hymenoptera; Ichneumonidae) Zehiri ve Parazitlemesinin Konak Hemositlerine Etkileri [Yayınlanmamış Doktora Tezi]. Balıkesir, Üniversitesi, Balıkesir;2011.
  36. Ueno T. Selective host-feeding on parasitized hosts by the parasitoid Itoplectis naranyae (Hym: Ichneumonidae) and its implication for biological control. Bull Entom Res.1998;88:461-466. doi.org/10.1017/S0007485300042206.
  37. Lauziere I, Pérez-Lachaud G, Brodeur J. Effect of female body size and adult feeding on the fecundity and longevity of the parasitoid Cephalonomia stephanoderis Betrem (Hymenoptera: Bethylidae). Ann Entomol Soc Am. 2000;93(1):103–109. doi.org/10.1603/0013-8746(2000)093[0103:EOFBSA]2.0.CO;2.
  38. Corley JC, Villacide JM. Ecology and biological control. In Biological Control of Insect Pests in Plantation Forests Cham. 2025. Springer Nature Switzerland, pp. 95-113.
  39. Oliveira CM, Auad, A.M., Mendes, S.M. and Frizzas, M.R. (2014) Crop Losses and the Economic Impact of Insect Pests on Brazilian Agriculture. Crop Protection, 56:50-54.
  40. Kumar P, Tiwari B, Singh S, Mishra SK, Mishra AK. Biological Control Predator and Parasitoids: An Overview 2024
  41. Harvey JA. Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity. Entomol Exp Appl. 2005;117:1–13. doi: 10.1111/j.1570-7458.2005.00348.x.
  42. Santos AMC, Quicke DLJ. Large-scale diversity patterns of parasitoid insects: parasitoid diversity patterns. Entomol Sci. 2011;14:371–382. doi.org/10.1111/j.1479-8298.2011.00481.x.
  43. Van Lenteren JC. The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl. 2012;57(1):1-20.
  44. Mackauer M. Growth and developmental interactions in some aphids and their hymenopteran parasites. J Insect Physiol. 1986;32:275-280. doi.org/10.1016/0022-1910(86)90039-9.
  45. Harvey JA, Harvey IF, Thomson DJ. Flexsible larval feeding allaws use of a range of host sizes by aparazitoit wasp. Ecology. 1994;75:1420-1428. doi.org/10.2307/1937465.
  46. Güner P. Penicillium mallochii’nin DNA barkodlaması ve sürdürülebilir biyolojik mücadelede parazitoit Venturia canescens ile etkileşimleri [Yayınlanmamış Doktora Tezi]. Balıkesir, Balıkesir Üniversitesi;2024.
  47. Harvey JA. Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity. Entomol Exp Appl. 2005;117(1), 1-13.
  48. Abbas MST. Interactions between Entomopathogenic Fungi and Entomophagous Insects. Adv Ent. 2020;8:130-146. doi.org/10.4236/ae.2020.83010.
  49. Jarrahi A, Safavi SE. Sublethal effects of Metarhizium anisopliae on life table parameters of Habrobracon hebetor parasitizing Helicoverpa armigera larvae at different time intervals. BioControl. 2016;61(2):167–175. doi.org/10.1007/s10526- 015-9707-y.
  50. Araujo ES, Poltronieri AS, Poitevin CG, Mirás-Avalos JM, Zawadneak MAC, Pimentel IC. Compatibility between entomopathogenic fungi and egg parasitoids (Trichogrammatidae): A laboratory study for their combined use to control Duponchelia fovealis. Insects. 2020;11:630. doi.org/10.3390/insects11090630.
  51. Tamayo-Mejia F, Tamez-guera P, Guzman-Franco AW, Gomez-Flores R. Can Beauveria bassiana and Tamarixia triozae (Hym.: Eulophidae) Be Used Together for Improved Biological Control of Bactericera cockerelli (Hemiptera: Triozidae)? Biol Control. 2015;90:42-48. doi.org/10.1016/j.biocontrol.2015.05.014
  52. Oreste M, Bubici G, Poliseno M, Tarasco E. Effect of Beauveria bassiana and Metarhizium anisopliae on the Trialeurodes vaporariorum-Encarsia formosa system. J Pest Sci. 2016;89:153-160.
  53. Fernandez-Grandon GM, Harte SJ, Ewany J, Bray D, Stevenson PC. Additive effect of botanical insecticide and entomopathogenic fungi on pest mortality and the behavioral response of its natural enemy. Plants. 2020;9:173. doi.org/10.3390/plants9020173.
  54. Santos ALZ, Pinto CPG, Fonseca SS, de Azevedo EB, Polanczyk RA, Rossi GD. Immune interactions, risk assessment and compatibility of the endoparasitoid Cotesia flavipes parasitizing Diatraea saccharalis larvae exposed to two entomopathogenic fungi. Biol Control. 2022;166:104836. doi.org/10.1016/j.biocontrol.2022.104836.
  55. Akbari S, Mirfakhraie S, Aramideh S, Safaralizadeh MH. Effect of fungal isolates and imidacloprid on cabbage aphid Brevicoryne brassicae and its parasitoid Diaeretiella rapae. Zemdirbyste-Agriculture. 2020;107:255–262. doi.org/10.13080/z-a.2020.107.033.
  56. Aguila LCR, Akutse KS, Ashraf HJ, Bamisile BS, Lin J, Dai J, Wang H, Wang L. The survival and parasitism rate of Tamarixia radiata (Hymenoptera: Eulophidae) on its host exposed to Beauveria bassiana (Ascomycota: Hypocreales). Agronomy. 2021;11:1496. doi.org/10.3390/agronomy11081496.
  57. Ibarra-Cortes KH, González-Hernández H, Guzmán-Franco AW, Ortega-Arenas LD, Villanueva-Jiménez JA, Robles-Bermúdez A. Interactions between entomopathogenic fungi and Tamarixia radiata (Hymenoptera: Eulophidae) in Diaphorina citri (Hemiptera: Liviidae) populations under laboratory conditions. J Pest Sci. 2018;91:373–384. doi.org/10.1007/s10340-017-0870-z.
  58. Allahyari R, Aramideh S, Michaud JP, Safaralizadeh MH, Rezapanah MR. Behavioral and developmental responses of Habrobracon hebetor (Hymenoptera: Braconidae) to larvae of Helicoverpa armigera (Lepidoptera: Noctuidae) inoculated with various concentrations of Bacillus thuringiensis var. kurstaki (Bacillales: Bacillacae). J Insect Sci. 2020;20:129. doi.org/10.1093/jisesa/ieaa129.
  59. Cai Y, Fan J, Sun S, Wang F, Yang K, Li G. Pang Y. Interspecific interaction between Spodoptera exigua multiple nucleopolyhedrovirus and Microplitis bicoloratus (Hymenoptera: Braconidae: Microgastrina) in Spodoptera exigua (Lepidoptera: Noctuidae) larvae. J. Econ. Entomol. 2012;105:1503–1508. doi.org/10.1603/EC12077.
  60. Escribano A, Williams T, Goulson D, Cave RD, Chapman JW, Caballero P. Consequences of interspecific competition on the virulence and genetic composition of a nucleopolyhedrovirus in Spodoptera frugiperda larvae parasitized by Chelonus insularis. Biocontrol Sci Technol. 2001;11:649–662. doi.org/10.1080/09583150120076193.
  61. Ferguson KI, Stiling P. Non-additive effects of multiple natural enemies on aphid populations. Oecologia. 1996;108, 375-379.
  62. Brodeur J, Rosenheim JA. Intraguild interactions in aphid parasitoids. Entomol Exp Appl. 2000;97(1),93–108. https://doi.org/10.1046/j.1570-7458.2000.00721.x
  63. Vidal S, Fargues J. Impact of fungal entomopathogens on parasitoids. In L. A. Lacey (Ed.), Field Manual of Techniques in Invertebrate Pathology. 2007. Springer; pp. 339–361.
  64. Faria MR, Wraight SP. Mycoinsecticides and Mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biol Control. 2007;43(3), 237–256. https://doi.org/10.1016/j.biocontrol.2007.08.001
  65. Pasandideh A, Talebi AA, Hajiqanbar H, Tazerouni Z. Host stage preference and age-specific functional response of Praon volucre (Hymenoptera: Braconidae, Aphidiinae) a parasitoid of Acyrthosiphon pisum (Hemiptera: Aphididae). J Crop Prot. 2015;4:563–575.
  66. Stacconi MVR, Buffington M, Daane KM, Dalton DT, Grassi A, Kacar G, Miller B, Miller JC, Baser N, Ioriatti C, Walton VM. Host stage preference, efficacy and fecundity of parasitoids attacking Drosophila suzukii in newly invaded areas. Biol Control. 2015;84:28-35.
  67. Grasman J, Van Herwaarden OA, Hemerik L, Van Lenteren JC. A two-component model of host–parasitoid interactions: determination of the size of inundative releases of parasitoids in biological pest control. Math. Biosci. 2001;169(2), 207-216.
  68. Van Lenteren JC. Integrated pest management in protected crops. Integrated pest management: principles and systems development, 1995.
  69. Rakhshani E, Talebi AA, Kavallieratos N, Fathipour Y. Host stage preference, juvenile mortality and functional response of Trioxys pallidus (Hymenoptera: Braconidae, Aphidiinae). Biologia. 2004; 59 (2): 197-204.
  70. Isenhour DJ. Campoletis sonorensis [Hym.: Ichneumonidae] as a parasitoid of Spodoptera frugiperda [Lep.: Noctuidae]: Host stage preference and functional response. BioControl. 1985;30(1):31-36.
  71. Yazdani M, Feng Y, Glatz R, Keller MA. Host stage preference of Dolichogenidea tasmanica (Cameron, 1912) (Hymenoptera: Braconidae), a parasitoid of Epiphyas postvittana (Walker, 1863) (Lepidoptera: Tortricidae). Austral Entomol. 2015;54(3):325-331.
  72. Nielsen C, Skovgård H, Steenberg T. Effect of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) on survival and reproduction of the filth fly parasitoid, Spalangia cameroni (Hymenoptera: Pteromalidae). Environ Entomol. 2005;34(1):133-139.
  73. Mas NG, Medina MC, Sánchez FG, Moraga EQ. Bottom-up effects of endophytic Beauveria bassiana on multitrophic interactions between the cotton aphid, Aphis gossypii, and its natural enemies in melon. J Pest Sci. 2019;92:1271–1281. doi.org/10.1007/s10340-019-01098-5.
  74. Brobyn P, Clark SJ, Wilding N. The Effect of Fungus Infection of Metopolophium dirhodum [Hom.:Aphididae] on the Oviposition Behaviour of he Aphid Parasitoid Aphidius rhopalosiphi [Hym.: Aphidiidae]. Entomophaga. 1988;33:333-338. doi.org/10.1007/BF02372623.
  75. Askary H, Brodeur J. Susceptibility of Larval Stage of the Aphid Parasitoid, Aphidius nigripes to the Entomopathogenic Fungus Verticillium lecanii. J Invertebr Pathol. 1999;73:129-132. doi.org/10.1006/jipa.1998.4824.
  76. Quesada-Moraga E, Garrido-Jurado I, Yousef-Yousef M, González-Mas N. Multitrophic interactions of entomopathogenic fungi in biocontrol. BioControl. 2022;67:457–472. doi.org/10.1007/s10526-022-10163-5.
  77. Ou D, Ren LM, Liu Y, Ali S, Wang XM, Ahmed MZ, Qiu BL. Compatibility and efficacy of the parasitoid Eretmocerus hayati and the entomopathogenic fungus Cordyceps javanica for biological control of whitefly Bemisia tabaci. Insects. 2019;10(12):425. doi.org/10.3390/insects10120425.
  78. Avery PB, Jane Faull J, Simmonds MSJ. Effects of Paecilomyces fumosoroseus and Encarsia formosa on the control of the greenhouse whitefly: Preliminary assessment of a compatability study. BioControl. 2008;53(2):303–316. doi.org/10.1007/s10526-007-9073-5.
  79. Labbe RM, Gillespie DR, Cloutier C, Brodeur J. Compatibility of an entomopathogenic fungus with a predator and a parasitoid in the biological control of greenhouse whitefly. Biocontrol Sci Technol. 2009;19(4):429–446. doi.org/10.1080/09583150902803229.
  80. Huang Z, Sahar F, Ren S, Ali S. Effect of Isaria fumosoroseus on Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae), a Parasitoid of Bemisia tabaci (Hemiptera: Aleyrodidae). Pak J Zool. 2010;42(2):121–127.
  81. Mohammed AA, Hatcher PE. Combining entomopathogenic fungi and parasitoids to control the green peach aphid Myzus persicae. Biol Control. 2017;110:44-55.
  82. Garcia FRM, Brida AL, Martins LN, Abeijon LM, Luntinski CJ. Biological control of fruit flies of the genus Anastrepha (Diptera: Tephritidae): Current status and perspectives. In: Davenport L ed. Biological Control: Methods, Applications and Challenges. 2017; Nova Science Publishers; Hauppauge, NY, USA; pp. 29–71.
  83. Tanada Y, Kaya HK. Insect pathology.Academic press;2012.
  84. Danfa A, Van den Valk HCHG. Laboratory Testing of Metarhizium spp. and Beauveria bassiana on Sahelian Non-Target Arthropods. Biocontrol Sci Technol. 1999;9:187-198. doi.org/10.1080/09583159929776
  85. Jaber LR, Araj SE. 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). Biol Control. 2018;116:53-61. doi.org/10.1016/j.biocontrol.2017.04.005.
  86. Tamayo-Mejia F, Tamez-Guerra P, Guzman-Franco AW, Gomez-Flores R. Developmental Stage Affects Survival of the Ectoparasitoid, Tamarixia triozae Exposed to the Fungus Beauveria bassiana. Biol Control. 2016;93:30-36. doi.org/10.1016/j.biocontrol.2015.11.006.
  87. Aristizabal I, Pardey A, Cordoba BC. Effect of Beauvaria bassiana and Metarhizium anisopliae on the Coffee Berry Borer Parasitoid, Cephalonomia stephannoderis. Rev Colomb Entomol. 1995;21:199-204.
  88. Madurappulige P. Effect of Beauveria bassiana on Diadegma semiclausum (Ichneumonidae), a Parasitoid of Plutella xylostella (Lep.: Yponomeutidae). [PhD Thesis]. Lincoln University, Lincoln; 2005.
  89. Rannback LM, Cotes B, Anderson P, Ramert B, Meyling, NV. Mortality Risk from Entomopathogenic Fungi Affects Oviposition Behavior in he Parasitoid Wasp Trybliographa rapae. J Invertebr Pathol. 2014;124:78-86. doi.org/10.1016/j.jip.2014.11.003.
  90. Tounou AK, Agboka A, Poehling HM, Ranpack K, Borgemeister C. Evaluation of the Entomopathogenic Fungi Metarhizium anisopliae and Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) for Control of he Green Leafhopper Empoasca decipiens (Homoptera: Cicadellidae) and Potential Side Effects on the Egg Parasitoid Anagrus atomus (Hymenoptera: Mymaridae). Biocontrol Sci Technol. 2003;13:715-728. doi.org/10.1080/09583150310001606534.
  91. Lord J. 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). Biol Cont 2001;21:300-304. doi.org/10.1006/bcon.2001.0942.
  92. Aqueel M, Leather SR. Virulence of Verticillium lecanii (Z.) against Cereal Aphids: Does Timing of Infection Affect the Performance of Parasitoids and Predators? Pest Manag Sci. 2013;69:493-498. doi.org/10.1002/ps.3398.
  93. Hall RA. The Fungus, Verticillium lecanii as a Microbial Insecticide against Aphids and Scales. In: Burges, HD, 1981. Ed., Microbial Control of Pest and Plant Diseases, 1970-1980, Academic Press, San Diego.
  94. King EG, Bell V. Interaction between a Braconid, Microplitis croceipes, and a Fungus, Nomuraea rileyi, in Laboratory-Reared Bollworm Larvae. J Invertebr Pathol. 1978;31:337-340. doi.org/10.1016/0022-2011(78)90225-2.
  95. Ignoffo CM. The Fungus Nomuraea rileyi as a Microbial Insecticide. In:Burges, HD, 1981. Ed., Microbial Control of Pests and Plant Diseases, 1970-1980, Academic Press, San Diego.
  96. Chow A, Dunlap CA, Jackson MA, Flores D, Patt JM, Setamou M. 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. J Econ Entomol. 2016;1-11.
  97. Furlong MJ, Pell JK. Conflicts between a Fungal Entomopathogen Zoophthora radicans and Two Larval Parasitoids of the Diamond-Back Moth. J Invertebr Pathol. 2000;76:85-94. doi.org/10.1006/jipa.2000.4943.
  98. Furlong MJ, Pell JK. Interaction between the Fungus Entomopathogen Zoophthora radicans Brefeld (Entomophthorales) and Two Hymenopteran Parasitoids Attacking the Diamond-Back Moth, Plutella xylostella. J Invertebr Pathol. 1996;68:15-21. doi.org/10.1006/jipa.1996.0053.
  99. Ormond E, Thomas APM, Pell JK, Freeman SN, Roy HE. Avoidance of a generalist entomopathogenic fungus by the ladybird, Coccinella septempunctata. FEMS Microbiol Ecol. 2011;77:229–237. doi.org/ 10.1111/j.1574-6941.2011.01100.x.
  100. Ignoffo CM. The Fungus Nomuraea rileyi as a Microbial Insecticide. In:Burges, HD, 1981. Ed., Microbial Control of Pests and Plant Diseases, 1970-1980, Academic Press, San Diego.