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Biopesticides

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What is biological control?

Biological control or biocontrol is a method of managing pests and plant diseases through the use of natural enemies. A classical approach to biological control is called inoculative introduction where an agent not previously present is introduced to perform predation, parasitism, herbivory, or other biological methods to kill an unwanted organism. Inoculative augmentation is the application of an indigenous agent to accumulate in the biocontrol agent population. Another method is inundative augmentation, the mass application of an agent with the primary objective of high initial kill. [1]

Biopesticides

A biopesticide is a type of pesticide derived from natural materials, such as animals, plants, bacteria, or minerals, that is used to control pests, including insects, weeds, fungi, and other harmful organisms. Unlike conventional chemical pesticides, biopesticides are generally considered to be environmentally friendly and have less impact on non-target organisms, humans, and the ecosystem.

Metarhizium acridum

The genus Metarhizium (class Sordariomycetes, order Hypocreales, family Clavicipitaceae) includes entomopathogenic fungi, often with a narrow host range. Researchers have identified and classified Metarhizium isolates and species using anatomical observations, PCR DNA tests [2] [3], and spectroscopy.[4] These findings have paved the way for the development of effective biopesticides utilizing Metarhizium, commonly applied as conidia mixed with oil, oil-water emulsion, or in a dry form.

Since this biopesticide is host-specific, it responds to specific chemical cues associated with locusts and grasshoppers. When it comes into contact with a locust, the spores start germination and the fungus grows inside the locust. This infection causes the locust to slow down, stop eating and ultimately die. Most infected locusts die within 1–3 weeks, depending on temperature and humidity. The time lag from spraying to the locusts dying remains a major challenge to widespread implementation. The high cost compared to synthetic chemicals also makes it a less desirable alternative despite its shown environmental benefits.

Development of Metarhizium acridum as a biopesticide

Metarhizium anisopliae, initially employed for insect control in Russia more than a century ago (as reviewed by Lord [5]), has demonstrated its effectiveness in eliminating locusts and grasshoppers through internal infection after penetrating the insects' outer layer.[6] Extensive research has been conducted for over a century on the isolation, formulation, and efficacy testing of Metarhizium for microbial pest control, including recent studies focused on locust control. [1] [7]

Research on M. acridum began in the late 1980s leading to the discovery of the most effective isolate IMI8033. [8] [9] From this, a commercial product, Green Muscle®, was developed by the late 1990s (see LUBILOSA ). Metarhizium acridum is currently produced as a biopesticide by Eléphant Vert under the name Novacrid® in their factory in Meknès, Morocco. In 2019, Eléphant Vert secured the license to produce Green Muscle®, originally developed by LUBILOSA. Green Muscle® has been used in Madagascar, Niger, Senegal and Sudan. A similar product is used in China. Another variation, Green Guard, is produced by BASF of Australia for the control of Australian plague locusts and other grasshoppers. In 2000–2001, the Australian Plague Locust Commission (APLC) treated nearly 25,000 ha of locust bands, the first operational use of locust biopesticides in the world.[7]

In Brazil, the use of M. acridum to control locusts was considered as early as 1993.[10] Until 2006, studies conducted by the Brazilian Agricultural Research Corporation (Embrapa) focused on the production, formulation, and field evaluation of the efficacy of a local strain of Metarhizium and its effects on non-target insects.[10] The Matto Grosso locust, Rhammatocerus schistocercoides was effectively killed by Metarhizium but the efforts never reached an operational stage. [11] [12]

Trials were also conducted with M. acridum in Mexico [13] [14] and in China [15], with both Green Guard® and local isolates. In Mexico, a local M. acridum product has been incorporated into treatment programs for the Central American locust and is applied as barrier treatments, either by air as Ultra-Low Volume (ULV) (2,000 to 4,000 ha per year) or by ground (50–350 ha).[10]

China is able to keep the price of M. acridum comparable to chemical pesticides with local production.[10] The use of ULV formulations and application techniques ensures a high level of mortality. [15] [16] [17] Biopesticides are therefore a formidable part of locust and grasshopper population management with about 100,000 ha treated each year. [18]

There have been applications of M. acridum during specific campaigns under the supervision of the FAO in East Timor (Green Guard® against L. migratoria, 2004) and Tanzania (Green Muscle® in 2009 against the red locust, Nomadacris septemfasciata).[10] M. acridum was determined the best choice in both cases because of concerns over the proximity to water. [10]

Recent successes

Metarhizium acridum was used during the 2019–2021 desert locust outbreak across Somalia, Kenya, and Ethiopia, and samples of the pathogen were sent to Uganda, Pakistan, and India for trial use.[19] Somalia decided to use only M. acridum and the insect growth regulator (IGR) teflubenzuron due to concerns of pastoral communities and beekeepers over the use of more toxic pesticides. Field evaluations of the Somali campaign have proven challenging to conduct however valuable insights emerged on best practices for aerial application, including what time, temperature, and growth stage is best for application.[20] The campagin has been seen as a major breakthrough as the largest surface area treated with biopesticides in a single campaign anywhere in the world, with more than 100,000 hectares sprayed with M. acridum.[21]

CABI Green Muscle education videos

Green Muscle overview, storage, dosage, application, PPE and cleaning. videos available in English, French, Russian, and Arabic

Paranosema locustae

Paranosema locustae (synonyms: Antonospora locustae, Nosema locustae) is a entomopathogenic fungus that causes moderate direct mortality after treatment to locust and grasshoppers. [22] Although N. locusta is slow to kill its locust and grasshopper hosts (nearly 3 weeks), its sub-lethal effects—reductions in fecundity, longevity, food consumption, disruption of aggregation behavior and phase change, and activity [23] [24] [25] [26] can make a difference to population dynamics. N. locustae infections begin in the midgut and spreads to the hindgut, fat body, nervous tissues, hemocytes, and gonads. [27] The pathogen works by inhibiting locust growth, development, and reproduction. [28] [29] Eventually, it infects the nervous system and alters neurotransmitter levels that can impact behavioral phase change. [30] [31] [24]

Development of Paranosema locustae as a biopesticide

P. locustae was the first commercial microsporidian product developed in the 1960s and 1970s as an alternative to chemical pesticides. [32] [33] [34] The aim was to reduce the frequency and severity of outbreaks by having effects over a number of years, but the slow activity (nearly 3 weeks) combined with a low final mortality of 60-70% routinely obtained with bait formulations limited its use [35] [36]. However, this product is sometimes used at smaller scales, by organic producers [37], or in environmentally sensitive areas. It has been used in the field against locusts and grasshoppers in Argentina, Australia, and China, and some cases have shown it to persist and spread in grasshopper communities, inducing mortality over several years. [38] [39] [40] found the opposite in Canada where low virulence of P. locustae could not be readily overcome by repeated applications. P. locustae has also been used in Cape Verde, Mali, Mauritania, Niger, and Senegal [41] [42] [43] but with limited long-term follow-up monitoring only in Cape Verde and Senegal where P. locustae was actually found between 13–23 years after applications.

In recent years, there has been a renewed interest in P. locustae, mainly due to China, where a more virulent strain is produced in large quantities and used extensively. Also in Argentina, where its long-term persistence appears to reduce the intensity of grasshopper outbreaks. [44] Because of the time it takes to kill its target, combined with low final mortality (60–70%) there has been limited use in the United States, [35] [45] [36] In addition to its persistence, P. locustae has sub-lethal effects including reductions in fecundity, longevity, food consumption and activity [46] that can have important effects on populations.[47] In Argentina, some areas that were treated with P. locustae did not have any grasshopper outbreaks for many years, with P. locustae being present and causing epizootics decades later.[48]  In China, there were decreases in grasshopper numbers and increases in natural enemies for several seasons after treatments. [49] [50] These good results led to breeding experiments to select more virulent strains of P. locustae which were then produced in a factory with high-yield technologies.  A water-based suspension formulation for ULV was developed and application methods for rangeland, crops, and forest systems. Large-scale field applications resulted in mortalities of >80% with Migratory locusts (Locusta migratoria) in China [49] [51], and with yellow-spined bamboo locust (Ceracris Kiangsu) in Laos and Vietnam. As in Argentina, sublethal effects were detected: P. locustae disrupts aggregation behavior and phase change in Migratory locusts [52] [53] [54]; effects that may have profound implications in control. In China, a moderate dose at a price comparable to many chemicals, gives sufficient initial mortality (60-80%), combined with sublethal effects and subsequent season mortality, so that P. locustae forms a significant part of control programs there. In addition, P. locustae use has recently expanded into Laos and Vietnam against the Yellow spined bamboo locust, which have caused substantial damage since 2014. A pilot program of bamboo locust management was established mainly using P. locustae and mortalities of >80% were obtained in locust infestations in bamboo trees when applications were at the 2nd nymphal instar.

Biopesticides and non-target organisms

The use of Metarhizium for managing grasshoppers and locusts is regarded as environmentally sustainable and highly effective. M. acridum, mainly used in Africa and Australia, along with M. brunneum (South America, North America, China, among others), exhibits significantly lower virulence towards insects belonging to other taxonomic orders and does not pose any threat to birds through direct contact, ingestion of conidia, or consumption of infected grasshoppers.[55] Consequently, M. acridum is particularly valuable for treating environmentally sensitive areas, organic farms, and locations where landowners are preparing to market their animals or crops.[7] However, there is still a need for more research on non-target organisms as there can be consequences of P. locustae use for other orthoptera.[56]

Nomenclature disputes

Paranosema locustae is often been referred to as Nosema locustae in the literature [57] [58] [59]. This has caused confusion and disagreements over the correct nomenclature. Canning's (1953) original description of the taxon placed it in the genus Nosema based on superficial similarities to the type species Nosema bombycis, a pathogen of the silkworm. However, in the early 2000s, two research groups independently, but in parallel, published data demonstrating that the taxon in question is only distantly related to “true” Nosema [60] [61]. To solve this issue, Sokolova et al. [60] proposed transferring P. locustae into a newly erected genus, Paranosema, whereas Slamovits et al. [61] proposed transferring N. locustae to the existing genus Antonospora. Subsequently, and most recently in 2005, Sokolova et al. [62] made arguments for retaining the taxon in Paranosema (as opposed to Antonospora) citing, among other things, additional meaningful differences in morphology and genetic separation between Paranosema (including P. locustae) and Antonospora. Regardless, both Paranosema and Antonospora are closely related. Thus, we refer to the taxon described by Canning in 1953 as P. locustae throughout the wiki.

Biopesticides used in locust and grasshopper control

The use of chemical pesticides against locusts was developed by the Anti-Locust Research Centre (ALRC), established in 1945. Dieldrin was the preferred control agent because of its efficiency, affordability, and long persistence. [63] However as public awareness of the negative environmental impact of organochlorine pesticides increased, dieldrin began to be phased out. Organophosphate, carbamate, and pyrethroid pesticides replaced dieldrin for locust and grasshopper control. However, these substances were not tested in Africa at the time because locust populations were in recession. Their replacements of organophosphate pesticides, such as fenitrothion and malathion, used in the early 1980s may have caused greater environmental damage than the organochlorine treatments they were designed to replace, due to their repeated blanket applications over large areas. [1]

Control operations have relied on broad-spectrum organophosphates such as chlorpyrifos, fenitrothion, malathion, carbamates such as bendiocarb (no longer approved by the Locust Pesticide Referee Group [64]), pyrethroids such as deltamethrin and lambda-cyhalothrin, the phenylpyrazole insecticide, fipronil, and insect growth regulators such as diflubenzuron (dimilin), and teflubenzuron. [1] [64]

However, biopesticides are being used on a larger scale than every before. More people are interested in, and demanding, alternatives to synthetic pesticides that are safer for the environment and human health. Entire countries, like Somalia in the 2019-2022 desert locust outbreak, are making the decision to use only biopesticides and IRGs.

See a list of synthetic pesticides used in locust and grasshopper management here.

Using Metarizium in the field

The application of biopesticides is most effective when focused on younger locusts spraying in the morning or at dusk as the locusts have lower body temperatures. [65][66] An important discovery in Somaliland 2019-2021 revolved around the efficient utilization of aerial M. acridum application. This approach aimed at newly hatched and less agile fledglings before their wings fully matured for flight. It was particularly effective when employed on dense roosting swarms during the early morning hours. By acting before temperatures rose sufficiently to enable flight, the swarms were still closely packed. This made them a more manageable target compared to when they grew larger, more dispersed, and harder to reach as the day progressed. [66]

It was also suggested that M. acridum be applied earlier in the breeding season, targeting the locusts before they formed larger and more agile swarms, which would facilitate more effective control. [66]

View Desert locust control in Somalia between 2019 and 2021

Read about Optimum Flight Height for the Control of Desert Locusts Using Unmanned Aerial Vehicles (UAV)

Videos on biological control

Click "Expand" ➡️ to view videos on biological control
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Barriers to biopesticide use

Challenges with current locust biopesticides include 1) economic and logistical feasibility surrounding production, transportation, and application in often remote regions, 2) on-the-ground non-target testing and approval in locust-prone countries prior to the onset of a crisis, 3) effectiveness in warmer temperatures since grasshoppers and locusts are very good at inducing behavioral fever to suppress infections.

Organizations involved in biological control

Organization Acronym Focus keywords Geographic purview Website
Data:Organization Biological control • Fertilizer • Control • Chemical manufacturing Ivory Coast • France • Kenya • Mali • Morocco • Senegal https://www.elephant-vert.com/
Data:Organization GLI Sustainable development • Ecology • Nutrition • Social science • Natural sciences • Agriculture • Agroecology • Biology • Behavior • Biological control • Climate change • Education • Sustainability science • Geometric framework • Grazing • Governance • Food security • Arts and humanities • Land use management • Landscape ecology • Locusts • Migration • Phase polyphenism • Phenotypic plasticity • Soil science United States • Senegal • Australia • China • Argentina • Bolivia • Paraguay • Uruguay • Mali https://www.locust.asu.edu
Data:Organization VIZR Biological control • Monitoring • Control • Natural sciences Russia https://www.vizrspb.ru/en/about-institute/


References

[10]

  1. ↑ 1.0 1.1 1.2 1.3 Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas M (2001) Biological control of locusts and grasshoppers. Annual Review of Entomology 46: 667–702. https://doi.org/10.1146/annurev.ento.46.1.667
  2. ↑ Entz SC, Johnson DL, Kawchuk LM (2005) Development of a PCR-based diagnostic assay for the specific detection of the entomopathogenic fungus Metarhizium anisopliae var. Acridum. Mycological Research, 11: 1302–1312. https://doi.org/10.1017/S0953756205003746
  3. ↑ Entz SC, Kawchuk LM, Johnson DL (2008) Discovery of a North American genetic variant of the entomopathogenic fungus Metarhizium anisopliae var. anisopliae pathogenic to grasshoppers. BioControl 53: 327–339. https://doi.org/10.1007/s10526-006-9061-1
  4. ↑ Hetjens BT, Tewes TJ, Platte F, Wichern F (2022) The application of Raman spectroscopy in identifying Metarhizium brunneum, Metarhizium pemphigi and Beauveria bassiana. Biocontrol Science and Technology 32: 329–340. https://doi.org/10.1080/09583157.2021.2007851
  5. ↑ Lord JC (2005) From Metchnikoff to Monsanto and beyond: The path of microbial control. Journal of Invertebrate Pathology 89: 19–29. https://doi.org/10.1016/j.jip.2005.04.006
  6. ↑ Milner RJ (1997) Metarhizium flavoviride (FI985) as a promising mycoinsecticide for Australian acridids. Memoirs of the Entomological Society of Canada 171: 287–300. https://doi.org/10.4039/entm129171287-1
  7. ↑ 7.0 7.1 7.2 Hunter DM (2004) Advances in the control of locusts (Orthoptera: Acrididae) in eastern Australia: from crop protection to preventive control. Australian Journal of Entomology 43: 293–303. https://doi.org/10.1111/j.1326-6756.2004.00433.x
  8. ↑ Lomer RP, Bateman RP, Godonou I, Kpindou D, Shah PA, Paraiso A, Prior C (1993) Field infection of Zonocerus variegatus following application of an oil-based formulation of Metarhizium flavoviride conidia. Biocontrol Science and Technology 3: 337-346. https://doi.org/10.1080/09583159309355288
  9. ↑ Langewald J, Kooyman C, Douro-Kpindou O, Lomer JC, Dahmoud AO, Mohamed HO (1997) Field treatment of desert locust (Schistocerca gregaria Forskål) hoppers in Mauritania using an oil formulation of the entomopathogenic fungus Metarhizium flavoviride. Biocontrol Science and Technology 7: 603-12. http://dx.doi.org/10.1080/09583159730659
  10. ↑ 10.0 10.1 10.2 10.3 10.4 10.5 10.6 Ries MW, Adriaansen C, Aldobai S, Berry K, Bal AB, Catenaccio MC, Cigliano MM, Cullen DA, Deveson T, Diongue A, Foquet B, Hadrich J, Hunter D, Johnson DL, Pablo Karnatz J, Lange CE, Lawton D, Lazar M, Latchininsky AV, Lecoq M, Le Gall M, Lockwood J, Manneh B, Overson R, Peterson BF, Piou C, Poot-Pech MA, Robinson BE, Rogers SM, Song H, Springate S, Therville C, Trumper E, Waters C, Woller DA, Youngblood JP, Zhang L, Cease A (2024) Global perspectives and transdisciplinary opportunities for locust and grasshopper pest management and research. Journal of Orthoptera Research 33(2): 169–216. doi:10.3897/jor.33.112803.
  11. ↑ Magalhães BP, Lecoq M, de Faria MR, Schmidt FGV, Guerra WD (2000). Field trial with the entomopathogenic fungus Metarhizium anisopliae var. acridum against bands of the grasshopper Rhammatocerus schistocercoides in Brazil. Biocontrol Science and Technology 10: 427–441.
  12. ↑ Magalhães BP, Lecoq M (Sc. Ed.) (2006). Bioinseticida e gafanhotos-praga: relatorio final do projeto Desenvolvimento de bioinseticidas para contrôle de gafanhotos-praga no Brasil. Brasilia, DF: Embrapa Recursos Genéticos e Biotecnologia; Montpellier, France: CIRAD. 123 p. https://docplayer.com.br/52769742-Bioinseticida-e-gafanhotos-praga.html
  13. ↑ Hernández-Velásquez VM, Hunter DM, Barrientos-Lozano L, Lezama-Guiterrez R, Reyes-Villanueva F (2003) Susceptibility of Schistocerca piceifrons (Orthoptera: Acrididae) to Metarhizium anisopliae var. acridum (Deuteromycotina: Hyphomycetes): laboratory and field trials. Journal of Orthoptera Research 12: 89–92. https://doi.org/10.1665/1082-6467(2003)012[0089:SOSPOA]2.0.CO;2
  14. ↑ Barrientos-Lozano L, Hunter DM, Alvila-Valdez J, Garcia-Salazar P, Horta Vega JV (2005) Control biológico de la langosta Schistocerca piceifrons (Orthoptera: Acrididae) en el noroeste de Mexico. Vedalia 12: 119–128.
  15. ↑ 15.0 15.1 Zhang L, Hunter DM (2005) Laboratory and field trials of Green GuardTM Metarhizium anisopliae var. acridum (Deuteromycotina: Hyphomycetes) against the oriental migratory locust (Locusta migratoria manilensis) (Orthoptera: Acrididae) in China. Journal of Orthoptera Research 14: 27–30. https://doi.org/10.1665/1082-6467(2005)14[27:LAFTOG]2.0.CO;2
  16. ↑ Ding XY, Zhang L (2009) Virulence of Metarhizium anisopliae and Nosema locustae against nymphs of Locusta migratoria manilensis. Journal of Beijing University of Agriculture 24: 9–14.
  17. ↑ Zhang L (2011) Advances and prospects of strategies and tactics of locust and grasshopper management. Chinese Journal of Applied Entomology 48: 804–810. https://doi.org/10.1146/annurev-ento-011118-112500
  18. ↑ Zhang L, Hunter DM (2017) Management of locusts and grasshoppers in China. Journal of Orthoptera Research 26: 155–159. https://doi.org/10.3897/jor.26.20119
  19. ↑ CABI (2020) Green Muscle providing strength against devastating locusts in the horn of Africa—CABI.org. CABI.org https://www.cabi.org/news-article/green-muscle-providing-strength-against-devastating-locusts-in-the-horn-of-africa/
  20. ↑ Owour A, McRae HD (2022) Desert locust control in Somalia between 2019 and 2021. international-pest-control.com. Research Information Ltd. September/October 64: 5.
  21. ↑ CABI (n.d.) Biopesticide helps safeguard food crops of 15 million people from desert locusts. CABI.org https://www.cabi.org/stories-of-impact/biopesticide-helps-safeguard-food-crops-of-15-million-people-from-desert-locusts/
  22. ↑ Lockwood JA, Bomar CR, Ewen AB (1999) The history of biological control with Nosema locustae: Lessons for locust management. International Journal of Tropical Insect Science 19: 333–350.
  23. ↑ Shi W-P, Wang X-Y, Yin Y, Zhang Y-X, Rizvi U-H, Tan S-Q, Cao C, Yu H-Y, Ji R (2019) Dynamics of Aboveground Natural Enemies of Grasshoppers, and Biodiversity after Application of Paranosema locustae in Rangeland. Insects 10: 224. https://doi.org/10.3390/insects10080224
  24. ↑ 24.0 24.1 Li A, Yin Y, Zhang Y, Zhang L, Zhang K, Shen J, Tan S, Shi W (2020) Effects of Paranosema locustae (Microsporidia) on the development and morphological phase transformation of Locusta migratoria (Orthoptera: Acrididae) through modulation of the neurotransmitter taurine. Journal of Integrative Agriculture 19: 204–210. https://doi.org/10.1016/S2095-3119(19)62637-7
  25. ↑ Feng YJ, Ge Y, Tan SQ, Zhang, KQ, Ji R, Shi WP (2014) Effect of Paranosema locustae (Microsporidia) on the behavioral phases of Locusta migratoria (Orthoptera: Acrididae) in the laboratory. Biocontrol Science and Technology 25: 48-55. https://doi.org/10.1080/09583157.2014.945902
  26. ↑ Lange CE, Cigliano MM (2005) Overview and perspectives on the introduction and establishment of the grasshopper biocontrol agent Paranosema locustae (Microsporidia) in the western Pampas of Argentina. Vedalia 12: 61-84.
  27. ↑ Solter LF, Becnel JJ, Oi DH (2012) Microsporidian entomopathogens. In: Vega FE, Kaya HK, eds., Insect Pathology. 2nd ed. Academic Press. Elsevier Inc., San Diego.
  28. ↑ Lange CE, Sanchez NE, Wittenstein E (2000) Effect of the pathogen Nosema locustae (Protozoa: Microspora) on mortality and development of nymphs of the South American locust, Schistocerca cancellata (Orthoptera: Acrididae). Journal of Orthoptera Research 9: 77–80.
  29. ↑ Raina SK, Das S, Rai MM, Khurad AM (1995) Transovarial transmission of Nosema locustae (Microsporida: Nosematidae) in the migratory locust Locusta migratoria migratorioides. Parasitology Research 18: 38–44.
  30. ↑ Shi W, Guo Y, Xu C, Tan S, Miao J, Feng Y, Zhao H, St Leger RJ, Fang W (2014) Unveiling the mechanism by which microsporidian parasites prevent locust swarm behavior. Proceedings of the National Academy of Sciences of the United States of America, 111: 1343–1348.
  31. ↑ Fu XJ, Hunter DM, Shi WP (2010) Effect of Paranosema (Nosema) locustae (Microsporidia) on morphological phase transformation of Locusta migratoria manilensis (Orthoptera: Acrididae). Biocontrol Science & Technology 20: 683–693.
  32. ↑ Henry JE (2017) The path to registration of a microbial pesticide. Protistology 1: 175-182.
  33. ↑ Lange C, Sokolova Y (2017) The development of the microsporidium Paranosema (Nosema) locustae for grasshopper control: John Henry’s innovation with worldwide lasting impacts. Protistology 11. https://doi.org/10.21685/1680-0826-2017-11-3-3
  34. ↑ Zhang L, Lecoq M (2021) Nosema locustae (Protozoa, Microsporidia), a biological agent for locust and grasshopper control. Agronomy 11: 711. https://doi.org/10.3390/agronomy11040711
  35. ↑ 35.0 35.1 Streett DA (1996–2000) Technical Bulletin No. 1809. I.2 Nosema locustae. In: Cunningham GL, Sampson MW (Eds) Grasshopper Integrated Pest Management User Handbook. U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Washington DC. I.2-1-3
  36. ↑ 36.0 36.1 Lockwood J, Bomar C, Ewen A (1999) The history of biological control with Nosema locustae: lessons for locust management. Insect Science and Its Application 19: 333–350. https://doi.org/10.1017/S1742758400018968
  37. ↑ Altieri MA, Davis J, Burroughs K (1983) Some agroecological and socio-economic features of organic farming in California. A Preliminary Study. Biological Agriculture & Horticulture 1: 97–107. https://doi.org/10.1080/01448765.1983.9754384
  38. ↑ Solter LF, Becnel JJ, Oi DH (2012) Microsporidian entomopathogens. In: Vega FE, Kaya HK (Eds.), Insect Pathology, 2nd edition, Elsevier, London. 221–263 pp. https://doi.org/10.1016/B978-0-12-384984-7.00007-5
  39. ↑ Bjornson S, Oi D (2014) Microsporidia biological control agents and pathogens of beneficial insects. In: Weiss, LM, Becnel JJ (Eds.). Microsporidia: Pathogens of opportunity. Wiley-Blackwell, Ames, Iowa. 635–670. https://doi.org/10.1002/9781118395264.ch25
  40. ↑ Johnson DL and Dolinski MG (1997) Attempts to increase the incidence and severity of infection of grasshoppers with the entomopathogen Nosema locustae (Microsporida: Nosematidae) by repeated field application. Memoirs of the Entomological Society of Canada 171: 391-400.
  41. ↑ Henry JE, Fowler JL, Wilson MC, Onsager JA (1985) Infection of West African grasshoppers with Nosema locustae (Protozoa: Microsporida: Nosematidae). Tropical Pest Management 31: 144–147.
  42. ↑ Tounou AK, Kooyman C, Douro-Kpindou OK, Poehling HM (2008) Combined field efficacy of Paranosema locustae and Metarhizium anisopliae var. acridum for the control of sahelian grasshoppers. BioControl 53: 813. https://doi.org/10.1007/s10526-007-9146-5
  43. ↑ Tounou AK, Kooyman C, Douro-Kpindou OK, Gumedzoe YM, Poehlingn HM (2011) Laboratory assessment of the potential of Paranosema locustae to control immature stages of Schistocerca gregaria and Oedaleus senegalensis and vertical transmission of the pathogen in host populations. Biocontrol Science and Technology 21: 605–617. https://doi.org/10.1080/09583157.2011.566323
  44. ↑ Lange C, Sokolova Y (2017) The development of the microsporidium Paranosema (Nosema) locustae for grasshopper control: John Henry’s innovation with worldwide lasting impacts. Protistology 11. https://doi.org/10.21685/1680-0826-2017-11-3-3
  45. ↑ Johnson DL (1997) Nosematidae and other Protozoa as agents for the control of grasshoppers and locusts: current status and prospects. The Memoirs of the Entomological Society of Canada 171: 375–389.
  46. ↑ Lange CE, Cigliano MM (2005) Overview and perspectives on the introduction and establishment of the grasshopper biocontrol agent Paranosema locustae (Microsporidia) in the western Pampas of Argentina. Vedalia 12: 61–84.
  47. ↑ Jaronski ST (2012) Microbial control of invertebrate pests. In: Sundh I. et al (eds.), Beneficial Microorganisms in Agriculture, Food and the Environment: Safety Assessment and Regulation. CAB International, 72–95 pp.
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  49. ↑ 49.0 49.1 Zhang L, Yan Y, Wang G, Zhang Z, Pan J, Yang Z (1995) A preliminary survey on the epizootics of infection of Nosema locustae among grasshoppers in rangeland. Acta Agrestia Sinica 3: 223–229. https://doi.org/10.11733/j.issn.1007-0435.1995.03.007
  50. ↑ Shi WP, Wang XY, Yin Y, Zhang YX, Rizvi UH, Tan SQ, Cao C, Yu HY, Rong J (2019) Dynamics of aboveground natural enemies of grasshoppers, and biodiversity after application of Paranosema locustae in rangeland. Insects 2019 10: 224. https://doi.org/10.3390/insects10080224
  51. ↑ Gong A, Liu X, Jiang X, Zhang L (2003) Transmission of Nosema locustae disease in grasshopper populations in Qinghai grassland. Chinese Journal of Biological Control 19: 118–21. http://en.cnki.com.cn/Article_en/CJFDTOTAL-ZSWF200303006.htm
  52. ↑ Shi WP, Njagi PGN (2004) Disruption of aggregation behaviour of oriental migratory locusts (Locusta migratoria manilensis) infected with Nosema locustae. Journal Applied Entomology 128: 414-418. https://doi.org/10.1111/j.1439-0418.2004.00865.x
  53. ↑ Fu XJ, Hunter DM, Shi WP (2010) Effect of Paranosema (Nosema) locustae (Microsporidia) on morphological phase transformation of Locusta migratoria manilensis (Orthoptera: Acrididae). Biocontrol Science and Technology 20: 683–693. https://doi.org/10.1016/S2095-3119(19)62637-7
  54. ↑ Feng YJ, Ge Y, Tan SQ, Zhang, KQ, Ji R, Shi WP (2014) Effect of Paranosema locustae (Microsporidia) on the behavioral phases of Locusta migratoria (Orthoptera: Acrididae) in the laboratory. Biocontrol Science and Technology 25: 48–55. https://doi.org/10.1080/09583157.2014.945902
  55. ↑ Johnson DL, Smits JS, Jaronski ST, Weaver DK (2002) Assessment of health and growth of ring-necked pheasants following consumption of infected insects or conidia of entomopathogenic fungi, Metarhizium anisopliae var acridum and Beauveria bassiana, from Madagascar and North American Journal of Toxicology and Environmental Health 65: 2145–2162. https://doi.org/10.1080/00984100290071847
  56. ↑ Bardi C, Mariottini Y, Plischuk S, Lange CE (2012) Status of the alien pathogen Paranosema locustae (Microsporidia) in grasshoppers (Orthoptera: Acridoidea) of the Argentine Pampas. Biocontrol Science and Technology 22: 497–512. https://doi.org/10.1080/09583157.2012.665023
  57. ↑ Zhang L, Lecoq M (2021) Nosema locustae (Protozoa, Microsporidia), a biological agent for locust and grasshopper control. Agronomy 11: 711. https://doi.org/10.3390/agronomy11040711
  58. ↑ Gong A, Liu X, Jiang X, Zhang L (2003) Transmission of Nosema locustae disease in grasshopper populations in Qinghai grassland. Chinese Journal of Biological Control 19: 118–21. http://en.cnki.com.cn/Article_en/CJFDTOTAL-ZSWF200303006.htm
  59. ↑ Ding XY, Zhang L (2009) Virulence of Metarhizium anisopliae and Nosema locustae against nymphs of Locusta migratoria manilensis. Journal of Beijing University of Agriculture 24: 9–14.
  60. ↑ 60.0 60.1 Sokolova YY, Dolgikh VV, Morzhina EV, Nassonova ES, Issi IV, Terry RS, Ironside JE, Smith JE, Vossbrinck CR (2003) Establishment of the new genus Paranosema based on the ultrastructure and molecular phylogeny of the type species Paranosema grylli Gen. Nov., Comb. Nov. (Sokolova, Selezniov, Dolgikh, Issi 1994), from the cricket Gryllus bimaculatus Deg. Journal of invertebrate pathology 84: 159–172. https://doi.org/10.1016/j.jip.2003.10.004
  61. ↑ 61.0 61.1 Slamovits CH, Williams BAP, Keeling PJ (2004) Transfer of Nosema locustae (Microsporidia) to Antonospora locustae n. comb. based on molecular and ultrastructural data. The Journal of Eukaryotic Microbiology 51: 207–213. https://doi.org/10.1111/j.1550-7408.2004.tb00547.x
  62. ↑ Sokolova YY, Issi IV, Morzhina EV, Tokarev YS, Vossbrinck CR (2005) Ultrastructural analysis supports transferring Nosema whitei Weiser 1953 to the genus Paranosema and creation a new combination, Paranosema whitei. Journal of Invertebrate Pathology 90: 122–126. https://doi.org/10.1016/j.jip.2005.06.009
  63. ↑ Bennett LV, Symmons PM (1972) A review of estimates of the effectiveness of certain control techniques and insecticides against the desert locust. Centre for Overseas Pest Research, London, 15 pp.
  64. ↑ 64.0 64.1 Locust Pesticide Referee Group (2021) Evaluation of Field Trials Data on the Efficacy and Selectivity of Insecticides on Locusts and Grasshoppers. Report to FAO, 59pp.
  65. ↑ Li H, Zhu J, Cheng Y, Zhuo F, Liu Y, Huang J, Taylor B, Luke B, Wang M, González-Moreno P (2023) Daily activity patterns and body temperature of the Oriental migratory locust, Locusta migratoria manilensis (Meyen), in natural habitat. Frontiers in Physiology 14. Available from: https://www.frontiersin.org/articles/10.3389/fphys.2023.1110998 (February 14, 2023).
  66. ↑ 66.0 66.1 66.2 Owuor A, McRae HD (2022) Desert locust control in Somalia between 2019 and 2021. Outlooks on Pest Management 33: 132–136. https://doi.org/10.1564/v33_aug_02
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