Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-24T12:23:24.710Z Has data issue: false hasContentIssue false

Virulence of the insect-pathogenic fungi Metarhizium spp. to Mormon crickets, Anabrus simplex (Orthoptera: Tettigoniidae)

Published online by Cambridge University Press:  08 October 2021

Drauzio E. N. Rangel*
Affiliation:
Department of Biology, Utah State University, Logan, UT84322-5305, USA Universidade Brasil, São Paulo, SP08230-030, Brazil
Helen G. Bignayan
Affiliation:
Department of Biology, Utah State University, Logan, UT84322-5305, USA Bureau of Plant Industry, National Mango Research and Development Center, Jordan, Guimaras5045, Philippines
Hernani G. Golez
Affiliation:
Department of Biology, Utah State University, Logan, UT84322-5305, USA Bureau of Plant Industry, National Mango Research and Development Center, Jordan, Guimaras5045, Philippines
Chad A. Keyser
Affiliation:
Department of Biology, Utah State University, Logan, UT84322-5305, USA AgBiome, Inc., Research Triangle Park, NC27709, USA
Edward W. Evans
Affiliation:
Department of Biology, Utah State University, Logan, UT84322-5305, USA
Donald W. Roberts
Affiliation:
Department of Biology, Utah State University, Logan, UT84322-5305, USA
*
Author for correspondence: Drauzio E. N. Rangel, Email: drauzio@live.com

Abstract

The Mormon cricket (MC), Anabrus simplex Haldeman, 1852 (Orthoptera: Tettigoniidae), has a long and negative history with agriculture in Utah and other western states of the USA. Most A. simplex populations migrate in large groups, and their feeding can cause significant damage to forage plants and cultivated crops. Chemical pesticides are often applied, but some settings (e.g. habitats of threatened and endangered species) call for non-chemical control measures. Studies in Africa, South America, and Australia have assessed certain isolates of Metarhizium acridum as very promising pathogens for Orthoptera: Acrididae (locust) biocontrol. In the current study, two isolates of Metarhizium robertsii, one isolate of Metarhizium brunneum, one isolate of Metarhizium guizhouense, and three isolates of M. acridum were tested for infectivity to MC nymphs and adults of either sex. Based on the speed of mortality, M. robertsii (ARSEF 23 and ARSEF 2575) and M. brunneum (ARSEF 7711) were the most virulent to instars 2 to 5 MC nymphs. M. guizhouense (ARSEF 7847) from Arizona was intermediate and the M. acridum isolates (ARSEF 324, 3341, and 3609) were the slowest killers. ARSEF 2575 was also the most virulent to instar 6 and 7 nymphs and adults of MC. All of the isolates at the conidial concentration of 1 × 107 conidia ml−1 induced approximately 100% mortality by 6 days post application of fungal conidia. In conclusion, isolates ARSEF 23, ARSEF 2575, and ARSEF 7711 acted most rapidly to kill MC under laboratory conditions. The M. acridum isolates, however, have much higher tolerance to heat and UV-B radiation, which may be critical to their successful use in field application.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Deceased.

References

Alder-Rangel, A (2021) Dr Donald W. Roberts: International Insect Pathologist. In press.Google Scholar
Alston, DG, Rangel, DEN, Lacey, LA, Golez, HG, Kim, JJ and Roberts, DW (2005) Evaluation of novel fungal and nematode isolates for control of Conotrachelus nenuphar (Coleoptera: Curculionidae) larvae. Biological Control 35, 163171.CrossRefGoogle Scholar
Altre, JA, Vandenberg, JD and Cantone, FA (1999) Pathogenicity of Paecilomyces fumosoroseus isolates to diamondback moth, Plutella xylostella: correlation with spore size, germination speed, and attachment to cuticle. Journal of Invertebrate Pathology 73, 332338.CrossRefGoogle ScholarPubMed
Ansari, MA, Brownbridge, M, Shah, FA and Butt, TM (2008) Efficacy of entomopathogenic fungi against soil-dwelling life stages of western flower thrips, Frankliniella occidentalis, in plant-growing media. Entomologia Experimentalis et Applicata 127, 8087.CrossRefGoogle Scholar
Bailey, NW, Gwynne, DT and Ritchie, MG (2005) Are solitary and gregarious Mormon crickets (Anabrus simplex, Orthoptera, Tettigoniidae) genetically distinct? Heredity 95, 166173.CrossRefGoogle ScholarPubMed
Bateman, RP, Carey, M, Moore, D and Prior, C (1993) The enhanced infectivity of Metarhizium flavoviride in oil formulations to desert locusts at low humidities. Annals of Applied Biology 122, 145152.CrossRefGoogle Scholar
Bateman, R, Carey, M, Batt, D, Prior, C, Abraham, Y, Moore, D, Jenkins, N and Fenlon, J (1996) Screening for virulent isolates of entomopathogenic fungi against the desert locust, Schistocerca gregaria (Forskal). Biocontrol Science and Technology 6, 549560.CrossRefGoogle Scholar
Bidochka, MJ, St. Leger, RJ and Roberts, DW (1997) Mechanisms of deuteromycete fungal infections in grasshoppers and locusts: an overview. In Goettel, MS and Johnson, DL (eds), Microbial Control of Grasshoppers and Locusts. Memoirs of the Entomological Society of Canada, pp. 213–224.Google Scholar
Bischoff, JF, Rehner, SA and Humber, RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101, 512530.CrossRefGoogle ScholarPubMed
Blanford, S and Thomas, MB (2001) Adult survival, maturation, and reproduction of the desert locust Schistocerca gregaria infected with the fungus Metarhizium anisopliae var acridum. Journal of Invertebrate Pathology 78, 18.CrossRefGoogle ScholarPubMed
Bruck, DJ and Donahue, KM (2007) Persistence of Metarhizium anisopliae incorporated into soilless potting media for control of the black vine weevil, Otiorhynchus sulcatus in container-grown ornamentals. Journal of Invertebrate Pathology 95, 146150.CrossRefGoogle ScholarPubMed
Bruck, DJ, Snelling, JE, Dreves, AJ and Jaronski, ST (2005) Laboratory bioassays of entomopathogenic fungi for control of Delia radicum (L.) larvae. Journal of Invertebrate Pathology 89, 179183.CrossRefGoogle ScholarPubMed
Dias, LP, Araújo, CAS, Pupin, B, Ferreira, PC, Braga, GÚL and Rangel, DEN (2018) The Xenon Test Chamber Q-SUN® for testing realistic tolerances of fungi exposed to simulated full spectrum solar radiation. Fungal Biology 122, 592601.CrossRefGoogle ScholarPubMed
Enserink, M (2004) Can the war on locusts be won? Science (New York, N.Y.) 306, 18801882.CrossRefGoogle ScholarPubMed
Faria, MR, Magalhães, BP, Alves, RT, Schimidt, FGV, Tavares da Silva, JB and Frazão, H (2002) Effect of two dosages of Metarhizium anisopliae var. acridum against Rhammatocerus schistocercoides Rehn. Pesquisa Agr Brasil Pesqui Agropecu 37, 15311539.CrossRefGoogle Scholar
Feng, Z, Carruthers, RI, Roberts, DW and Robson, DS (1985) Age-specific dose mortality effects of Beauveria bassiana (Deuteromycotina, Hyphomycetes) on the European corn borer, Ostrinia nubilalis (Lepidoptera, Pyralidae). Journal of Invertebrate Pathology 46, 259264.CrossRefGoogle Scholar
Fernandes, EKK, Keyser, CA, Chong, JP, Rangel, DEN, Miller, MP and Roberts, DW (2010) Characterization of Metarhizium species and varieties based on molecular analysis, heat tolerance and cold activity. Journal of Applied Microbiology 108, 115128.CrossRefGoogle ScholarPubMed
Foster, RN, Jaronski, S, Reuter, KC, Black, LR, Schlothauer, R, Harper, J and Jech, LE (2011) Simulated aerial sprays for field cage evaluation of Beauveria bassiana and Metarhizium brunneum (Ascomycetes: Hypocreales) against Anabrus simplex (Orthoptera: Tettigoniidae) in Montana. Biocontrol Science and Technology 21, 13311350.CrossRefGoogle Scholar
Gao, Q, Jin, K, Ying, SH, Zhang, Y, Xiao, G, Shang, Y, Duan, Z, Hu, X, Xie, XQ, Zhou, G, Peng, G, Luo, Z, Huang, W, Wang, B, Fang, W, Wang, S, Zhong, Y, Ma, LJ, St Leger, RJ, Zhao, GP, Pei, Y, Feng, MG, Xia, Y and Wang, C (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genetics 7, e1001264.CrossRefGoogle ScholarPubMed
Garrido-Jurado, I, Resquín-Romero, G, Yousef-Naef, M, Ríos-Moreno, A and Quesada-Moraga, E (2020) Soil drenching with entomopathogenic fungi for control of the soil-dwelling life stages and adults of the same generation of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). Bulletin of Entomological Research 110, 242248.CrossRefGoogle Scholar
Gillespie, JP, Burnett, C and Charnley, AK (2000) The immune response of the desert locust Schistocerca gregaria during mycosis of the entomopathogenic fungus, Metarhizium anisopliae var acridum. Journal of Insect Physiology 46, 429437.CrossRefGoogle ScholarPubMed
Goettel, MS and Inglis, GD (1997) Fungi: hyphomycetes. In Lacey, LA (ed.), Manual of Techniques in Insect Pathology. San Diego: Academic Press, pp. 213249.CrossRefGoogle Scholar
Gwynne, DT (2001) Katydids and Bush-Crickets: Reproductive Behaviour and Evolution of the Tettigoniidae. Ithaca, NY: Cornell Univ. Press.Google Scholar
Hartley, WG (1970) Mormons, crickets, and seagulls: a new look at an old story. Utah Historical Quarterly 38, 224239.Google Scholar
Humber, RA (2014) USDA-ARS Collection of Entomopathogenic Fungal Cultures – Catalog of Strains Ithaca, USDA-ARS Biological Integrated Pest Management Research, Robert W. Holley Center for Agriculture and Health.Google Scholar
Hunt, VL and Charnley, AK (2011) The inhibitory effect of the fungal toxin, destruxin A, on behavioural fever in the desert locust. Journal of Insect Physiology 57, 13411346.CrossRefGoogle ScholarPubMed
Hunter, DM, Milner, RJ and Spurgin, PA (2001) Aerial treatment of the Australian plague locust, Chortoicetes terminifera (Orthoptera: Acrididae) with Metarhizium anisopliae (Deuteromycotina: Hyphomycetes). Bulletin of Entomological Research 91, 9399.Google Scholar
Keyser, CA, Fernandes, ÉKK, Rangel, DEN, Foster, RN, Jech, LE, Reuter, KC, Black, LR, Jaronski, S, Flake, DD, Evans, EW and Roberts, DW (2017) Laboratory bioassays and field-cage trials of Metarhizium spp. isolates with field-collected Mormon crickets (Anabrus simplex). Biocontrol 62, 257268.CrossRefGoogle Scholar
Li, ZZ, Alves, SB, Roberts, DW, Fan, MZ, Delalibera, I, Tang, J, Lopes, RB, Faria, M and Rangel, DEN (2010) Biological control of insects in Brazil and China: history, current programs and reasons for their successes using entomopathogenic fungi. Biocontrol Science and Technology 20, 117136.CrossRefGoogle Scholar
Lomer, CJ, Bateman, RP, Johnson, DL, Langewald, J and Thomas, MB (2001) Biological control of locusts and grasshoppers. Annual Review of Entomology 46, 667702.CrossRefGoogle ScholarPubMed
Lorch, PD and Gwynne, DT (2000) Radio-telemetric evidence of migration in the gregarious but not the solitary morph of the Mormon cricket (Anabrus simplex: Orthoptera: Tettigoniidae). Naturwissenschaften 87, 370372.CrossRefGoogle Scholar
Lorch, PD, Sword, GA, Gwynne, DT and Anderson, GL (2005) Radiotelemetry reveals differences in individual movement patterns between outbreak and non-outbreak Mormon cricket populations. Ecological Entomology 30, 548555.CrossRefGoogle Scholar
MacVean, C (1991) Mormon crickets: a brighter side. Rangelands 12, 234235.Google Scholar
MacVean, CM and Capinera, JL (1991) Pathogenicity and transmission potential of Nosema locustae and Vairimorpha n. sp. (Protozoa: Microsporida) in Mormon crickets (Anabrus simplex; Orthoptera: Tettigoniidae): a laboratory evaluation. Journal of Invertebrate Pathology 57, 2336.CrossRefGoogle Scholar
MacVean, CM and Capinera, JL (1992) Field evaluation of two microsporidian pathogens, an entomopathogenic nematode, and carbaryl for suppression of the Mormon cricket, Anabrus simplex Hald. (Orthoptera: Tettigoniidae). Biological Control 2, 5965.CrossRefGoogle Scholar
McClatchie, GV, Moore, D, Bateman, RP and Prior, C (1994) Effects of temperature on the viability of the conidia of Metarhizium flavoviride in oil formulations. Mycological Research 98, 749756.Google Scholar
Moore, D, Bridge, PD, Higgins, PM, Bateman, RP and Prior, C (1993) Ultra-violet radiation damage to Metarhizium flavoviride conidia and the protection given by vegetable and mineral oils and chemical sunscreens. Annals of Applied Biology 122, 605616.CrossRefGoogle Scholar
Oliveira, AS and Rangel, DEN (2018) Transient anoxia during Metarhizium robertsii growth increases conidial virulence to Tenebrio molitor. Journal of Invertebrate Pathology 153, 130133.CrossRefGoogle ScholarPubMed
Oliveira, AS, Braga, GUL and Rangel, DEN (2018) Metarhizium robertsii illuminated during mycelial growth produces conidia with increased germination speed and virulence. Fungal Biology 122, 555562.CrossRefGoogle ScholarPubMed
Pfadt, RE (1994) Mormon cricket. In USDA-ARS (ed.) Field Guide to Common Western Grasshoppers. Laramie, WY: Animal and Plant Health Inspection Service and Wyoming Agricultural Experiment, US Department of Agriculture Station, pp. 14.Google Scholar
Quinn, DM (1997) The Mormon Hierarchy: Extensions of Power. Salt Lake City: Signature Books.Google Scholar
Rangel, DEN and Roberts, DW (2018) Possible source of the high UV-B and heat tolerance of Metarhizium acridum (isolate ARSEF 324). Journal of Invertebrate Pathology 157, 3235.CrossRefGoogle Scholar
Rangel, DEN, Braga, GUL, Flint, SD, Anderson, AJ and Roberts, DW (2004) Variations in UV-B tolerance and germination speed of Metarhizium anisopliae conidia produced on artificial and natural substrates. Journal of Invertebrate Pathology 87, 7783.CrossRefGoogle Scholar
Rangel, DEN, Braga, GUL, Anderson, AJ and Roberts, DW (2005) Variability in conidial thermotolerance of Metarhizium anisopliae isolates from different geographic origins. Journal of Invertebrate Pathology 88, 116125.CrossRefGoogle ScholarPubMed
Rangel, DEN, Butler, MJ, Torabinejad, J, Anderson, AJ, Braga, GUL, Day, AW and Roberts, DW (2006) Mutants and isolates of Metarhizium anisopliae are diverse in their relationships between conidial pigmentation and stress tolerance. Journal of Invertebrate Pathology 93, 170182.CrossRefGoogle ScholarPubMed
Rangel, DEN, Alston, DG and Roberts, DW (2008) Effects of physical and nutritional stress conditions during mycelial growth on conidial germination speed, adhesion to host cuticle, and virulence of Metarhizium anisopliae, an entomopathogenic fungus. Mycological Research 112, 13551361.CrossRefGoogle ScholarPubMed
Rangel, DEN, Dettenmaier, SJ, Fernandes, EKK and Roberts, DW (2010a) Susceptibility of Metarhizium spp. and other entomopathogenic fungi to dodine-based selective media. Biocontrol Science and Technology 20, 375389.CrossRefGoogle Scholar
Rangel, DEN, Fernandes, EKK, Dettenmaier, SJ and Roberts, DW (2010b) Thermotolerance of germlings and mycelium of the insect-pathogenic fungus Metarhizium spp. and mycelial recovery after heat stress. Journal of Basic Microbiology 50, 344350.CrossRefGoogle Scholar
Rangel, DEN, Piedrabuena, AE, Roitman, I and Messias, CL (2020) Laboratory and field studies for the control of Chagas disease vectors using the fungus Metarhizium anisopliae. Archives of Insect Biochemistry and Physiology 105, e21745.CrossRefGoogle ScholarPubMed
Schwarz, FD (1998) 1848 – Miracle of the birds (Sea gulls save crops of Utah's Mormon pioneers by devouring plague of crickets). American Heritage 49, 104106.Google Scholar
Simpson, SJ, Sword, GA, Lorch, PD and Couzin, ID (2006) Cannibal crickets on a forced march for protein and salt. Proceedings of the National Academy of Sciences of the United States of America 103, 41524156.CrossRefGoogle Scholar
Sosa-Gomez, DR and Moscardi, F (1998) Laboratory and field studies on the infection of stink bugs, Nezara viridula, Piezodorus guildinii, and Euschistus heros (Hemiptera: pentatomidae) with Metarhizium anisopliae and Beauveria bassiana in Brazil. Journal of Invertebrate Pathology 71, 115120.CrossRefGoogle Scholar
Souza, RKF, Azevedo, RFF, Lobo, AO and Rangel, DEN (2014) Conidial water affinity is an important characteristic for thermotolerance in entomopathogenic fungi. Biocontrol Science and Technology 24, 448461.CrossRefGoogle Scholar
Streett, DA and Woods, SA (2001) Beauveria bassiana for Mormon crickets. In Branson, D and Redlin, B (eds), Grasshoppers: Their Biology, Identification and Management. USDA-ARS-APHIS. Laramie: University of Wyoming, pp. VII 6-1-5.Google Scholar
Sword, GA, Lorch, PD and Gwynne, DT (2005) Insect behaviour: migratory bands give crickets protection. Nature 433, 703.CrossRefGoogle ScholarPubMed
Tefera, T and Pringle, KL (2003) Effect of exposure method to Beauveria bassiana and conidia concentration on mortality, mycosis, and sporulation in cadavers of Chilo partellus (Lepidoptera: Pyralidae). Journal of Invertebrate Pathology 84, 9095.CrossRefGoogle Scholar
Wright, MS, Raina, AK and Lax, AR (2005) A strain of the fungus Metarhizium anisopliae for controlling subterranean termites. Journal of Economic Entomology 98, 14511458.CrossRefGoogle ScholarPubMed
Zimmermann, G (1986) The 'Galleria bait method' for detection of entomopathogenic fungi in soil. Journal of Applied Entomology 102, 213215.CrossRefGoogle Scholar

Rangel et al. supplementary material

Rangel et al. supplementary material 1

Download Rangel et al. supplementary material(Audio)
Audio 1.3 MB

Rangel et al. supplementary material

Rangel et al. supplementary material 2

Download Rangel et al. supplementary material(Video)
Video 5 MB