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Protistology 11 (3), 170-174 (2017)
Protistology
The development of the microsporidium Paranosema (Nosema) locustae for grasshopper control: John Henry's innovation with worldwide lasting impacts.*
Carlos E. Lange1 and Yuliya Y Sokolova23
1 Comisión de Investigaciones Científicas de la Provincia de Buenos Aires, Centro de Estudios Parasitológicos y de Vectores, CCT La Plata CONICET-Universidad Nacional de La Plata, Argentina
2 Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russia
3 Louisiana State University, Baton Rouge LA, USA
| Submitted October 2, 2017 | Accepted October 16, 2017 |
In this issue of "Protistology" we bring a tribute to the Society for Invertebrate Pathology (SIP) that this year celebrated its 50th anniversary (Fig. 1). The SIP have been always playing an important and global role in studies on unicellular eukaryotic symbionts of invertebrates, in particular on microsporidia. The Microsporidia Division was established in 1970 (see the Table 1) as the first official division of the SIP, and most of researchers in the field of Microsporidiology have been SIP members and published in the Journal of Invertebrate Pathology, an official publishing organ of the Society. Beneath we provide a table with some major landmarks of the SIP history. In this issue we also publish the paper prepared by Dr. John Henry (Fig. 2), an outstanding scholar in the fields of insect pathology, microbiological control, and microsporidia research, who developed the only one commercially successful biological insecticide based on microsporidian spores. His paper includes the materials presented at the Microsporidia Division symposium "The past and future frontiers in microsporidiology" at the 50th Annual Golden Jubilee Meeting of the Society for Invertebrate Pathology that was held in August of this 2017 year in San Diego, CA, USA <http://www.sipweb.org/ pastmtg.html>. Besides John Henry, many other
* A preamble to Dr. John Henry's "The path to registration of a microbial pesticide" in this issue of "Protistology".
outstanding microsporidiologists, such as James Becnel, Ann Cali, Joseph Maddox, Emily Troemel, Charles Vossbrinck, Louis Weiss (Fig. 3), shared their memories, ideas and research achievements at this symposium. In the following preamble to Dr. Henry's paper co-authored by Dr. Carlos Lange (Argentina), John's junior friend and colleague, we explain in more depth the importance of the impact ofJohn's research to the problem of microbiological control of insect pests, the problem that gave rise to extensive microsporidia research all over the World.
At a time when chemical control of noxious insects was seeing as close to a panacea (early 1960s) few had the foresight to look for viable alternatives. Among those few was John who not only appreciated the environmental problems posed by chemical insecticides, but also put his hands on finding ways to keep grasshoppers at bay without relying on synthetic insecticides. After years of meticulous field observations on grasshopper communities and their natural enemies in northwestern USA and laboratory experiments at the USDA Rangeland Insect Laboratory at Montana State University in Bozeman, he and collaborators opted among several other candidates discovered for a microorganism to be developed as a biocontrol agent for the long-term management of grasshopper populations. Paranosema (Nosema) locustae is indeed an exceptional microbial within a quite unique group of fungal-affiliated, spore-
doi:10.21685/1680-0826-2017-11-3-3 © 2017 The Author(s)
Protistology © 2017 Protozoological Society Affiliated with RAS
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Fig. 1. Logo of the Society for Invertebrate Pathology and the one of the 50th Annual Meeting and Golden Jubilee Celebration of the SIP <http:// www.sipweb.org/>.
forming intracellular parasites of animals and some protists, the Microsporidia. It infects primarily the cells of the host's adipose (fat) tissue causing depletion of energy reserves and alterations in intermediate metabolism. Uniqueness of P. locustae, conferred by a set of attributes, was unraveled by Henry during his studies and exploited to its maximum in order to end up with a useful tool for grasshopper management. Few if any of the approximate 1300 known species of Microsporidia show the combination of attributes of P. locustae:
(i) extremely wide host range among acridomorphs (at least 123 species worldwide are susceptible to infection) which allows use against a variety of pest grasshopper species, (ii) efficient horizontal and vertical transmission that facilitates long-term field
persistence, (iii) intermediate virulence permitting heavy spore loads per individual host, (iv) and good tolerance to freezing that enables storage for extended periods (years). Two drawbacks, the apparent impossibility ofin vitro production and the low viability of spores under field conditions were cleverly circumvented by establishment of protocols for in vivo production in grasshopper colonies and the use of baits for field delivery, respectively.
The narrative that follows, "The path to registration of a microbial pesticide" by Henry himself, is a concise account of the reasoning and work that lead to the development and registration (1980) of P. locustae which holds the distinctions as both the only microsporidium to reach that status, and the first organism that become available as a biocontrol agent of grasshoppers. Henry's work and approach was not only innovative (especially at its time) and lasting but also truly international in scope and repercussion. It was innovative because it departed from the environmentally disrupting application of indiscriminate, fast-killing chemical insecticides. International because it prompted interest and programs worldwide (notably China, West Africa, India, Argentina, Australia, Canada) (Fig. 4) not only about the use of P. locustae itself but also about the discovery of other pathogens and on environmental friendly initiatives based on his approach that disease-causing microorganisms would be useful for grasshopper management. In the words of acridologist J.A. Lockwood: "Research,
Table 1. Some major historical landmarks of the Society for Invertebrate Pathology (SIP).
1945 Edward Steinhaus (1914-1969) established the Laboratory of Insect Pathology at the University of California, Berkeley.
1958 The First International Conference on Insect Pathology and Biological Control organized by Jaroslav Weiser, and held in Prague, Czechoslovakia.
1959 The first issue of the Journal of Insect Pathology (Journal of Invertebrate Pathology from 1965) is published, edited by Edward Steinhaus.
1967 Edward Steinhaus proposed the formation of a new Society for Invertebrate Pathology (SIP).
1967 (May) The founding meeting of the SIP in Seattle, Washington. Edward Steinhaus was elected first President, and Albert K. Sparks - first Vice president.
1967 (Dec) The first issue of the SIP Newsletter was published.
1968 The first annual meeting of the SIP, hosted by John Briggs, was held in Columbus, Ohio with the annual meeting of the American Institute of Biological Sciences.
1970 The first Division of the SIP, Microsporidia, was officially established at the annual meeting in College Park, Maryland.
1996 Two divisions of the SIP, the Bacteria Division and the Virus Division, were officially established at the annual meeting in Cordoba, Spain.
1999 The Division of Diseases of Beneficial Invertebrates was officially established at the annual meeting in Park City, Utah.
2000 The Nematode Division of the SIP was officially established at the annual meeting in Guanajuato, Mexico.
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Fig. 2. John Henry, Joe Maddox and Ann Cali at the Microsporidia Symposium at the 50th Annual Meeting of the Society for Invertebrate Pathology at UC San Diego, August, 15, 2017 (photo by YS).
development, and marketing of biological control strategies for acridid pests have been and will be affected by the history of P. locustae". In fact, the development of a second biocontrol agent during the late 1980s and early 1990s, the fungus Metarhizium acridum, widely used in Australia, was greatly inspired and influenced by Henry's pioneering work. In recent years there has been a resurgence of interest in P. locustae due mainly to work in China, where it is produced in large quantities and used extensively, and Argentina where its long-term persistence seems to reduce the frequency and intensity ofgrasshopper outbreaks.
We hope the reader enjoys the narrative by J. Henry and appreciates the innovative and pioneering work performed on a very unusual microorganism.
Selected references for further reading
Bardi C., Mariottini Y., Plischuk S. and Lange C.E. 2012. Status ofthe alien pathogen Paranosema locustae (Microsporidia) in grasshoppers of the Argentine Pampas. Biocontrol Science and Technology. 22, 497-512.
Bjornson S. and Oi D. 2014. Microsporidia biological control agents and pathogens ofbeneficial
insects. In: Microsporidia: Pathogens of opportunity. (Eds Weiss L.M. and Becnel J.J). Wiley-Blackwell, Ames, Iowa, pp. 635—670.
Bomar C.R., Lockwood J.A., Pomerinke M.A. and French J.D. 1993. Multiyear evaluation of the effects of Nosema locustae (Microporida: Nosema-tidae) on rangeland grasshopper population density and natural biological controls. Environ. Entomol. 22, 489-497.
Feng Y.J., Ge Y., Tan S.Q., Zhang K.Q., Ji R. and Shi W.P.. 2014. Effect of Paranosema locustae (Microsporidia) on the behavioral phases of Locusta migratoria (Orthoptera: Acrididae) in the laboratory. Biocontrol Sci. Technol. 25, 48-55.
Fu X.J., Hunter D. and Shi W.P. 2010. Effect of Paranosema (Nosema) locustae (Microsporidia) on morphological phase transformation of Locusta migratoria manilensis (Orthoptera: Acrididae). Biocontrol Sci. Technol. 20, 683-693.
Henry J.E. 1990. Control of insects by Protozoa. In: New directions in biological control: Alternatives for suppressing agricultural pests and diseases. (Eds Baker R. and Dunn P.E.). Alan Liss, NY, pp. 161-176.
Henry J.E. and Oma E.A. 1981. Pest control by Nosema locustae, a pathogen of grasshoppers and
Fig. 3. Participants of Microsporidia Division sessions at the SIP meeting in San Diego, August 2017 (Photo by Julie Hopper, University of California, Berkeley, USA). From left to right, upper row: George Kyei-Poku, Carlos Lange, Pattana Jaroenlak, Wei-Fone Huang, Louis Weiss, Jimmy Becnel, Sebastian Gisder; second row: Joseph Maddox, Ann Cali, Bettina Vossbrinck, Jonathan Snow, Charles Vossbrinck; lower row: Kelly Bateman, Julie Hopper, Emily Troemel, Sarah Biganski, Yuliya Sokolova, Leellen Solter.
crickets. In: Microbial control of pests and plant diseases 1970-1980. (Ed. Burges H.D.). Academic Press, NY, pp. 573-585.
Johnson D.L. 1997. Nosematidae and other Protozoa as agents for the control of grasshoppers and locusts: current status and prospects. Mem. Entomol. Soc. Can. 171, 375-389.
Lange C.E. and Azzaro F.G. 2008. New case of long-term persistence of Paranosema locustae (Microsporidia) in melanopline grasshoppers ofAr-gentina. J. Invertebr. Pathol. 99, 357-359.
Lange C.E. and Cigliano M.M. 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.
Miao J., Guo Y. and Shi W. 2012. The persistence of Paranosema locustae after application in Qinghai Plateau, China. Biocontrol Sci. Techn. 22, 733735.
Lockwood J.A., Bomar C.R. and Ewen A.B. 1999. The history of biological control with Nosema lo-custae: lessons for locust management. Insect Sci. Appl. 19, 333-350.
Plischuk S., Bardi C.J. and Lange C.E.. 2013. Spore loads of Paranosema locustae (Microsporidia) in heavily infected grasshoppers (Orthoptera: Acri-doidea) of the Argentine Pampas and Patagonia. J. Invertebr. Pathol. 114, 89-91.
Shi W.P. and Njaqi P.G.N. 2004. Disruption of aggregation behaviour of oriental migratory locusts (Locusta migratoria manilensis) infected with Nosema locustae. J. Appl. Entomol. 128, 414418.
Shi W.-P., Wang Y.-Y., Lv F., Guo Ch. and Cheng X. 2009. Persistence of Paranosema (Nosema) locustae (Microsporidia: Nosematidae) among grasshopper (Orthoptera: Acrididae) populations in the Inner Mongolia rangeland, China. BioControl. 54, 77-84.
Fig. 4. Carlos Lange, Mae, John's wife, John, Francisco Delgado (of Cape Verde Plant Protection, the outstanding local liaison), and John Evans (creator and owner of the private company producing P. locustae at the time, Evans BioControl) in 1989 in Cape Verde while conducting field trials with P. locustae. A photo from collection of CL.
Shi W., Guo Y., Xu Ch., Tan Sh, Miao J., Feng Y., Zhao H., Leger R. J. and Fang. W. 2014. Unveiling the mechanism by which microsporidian parasites prevent locust swarm behavior. Proc. Natl. Acad. Sci. 111, 1343-1348.
Senderskiy I.V., Timofeev S.A., Seliverstova E.V., Pavlova O.A. and Dolgikh V.V. 2014. Secretion of Antonospora (Paranosema) locustae proteins into infected cells suggests an active role of microsporidia in the control of host programs and metabolic processes. PLOS One. 9 (4), e93585.
Sokolova Y.Y. and Lange C.E. 2002. An ultrastructural study of Nosema locustae Canning (Microspora) from three species ofAcrididae (Orthoptera). Acta Protozool. 41, 221-237.
Sokolova Y.Y., Dolgikh V.V., Morzhina E.V., Nassonova E.S., Issi I.V., Terry R.S., Ironside J.E., Smith J.E. and Vossbrinck C.R. 2003. Establish-
ment of the new genus Paranosema based on the ultrastructure and molecular phylogeny of the type species Paranosema grylli gen. Nov., comb. Nov. from the cricket Gryllus bimaculatus. J. Invertebr. Pathol. 84, 159-172.
Solter L.F., Becnel J.J. and Oi D.H. 2012. Microsporidian entomopathogens. In: Insect pathology, 2nd ed. (Eds Vega F.E. and Kaya H.K.). Elsevier, London. 221-263.
Tan S-q., Zhang K-q., Chen H-x., Ge Y., Ji, R. and Shi. W-p. 2015. The mechanism for microsporidian parasite suppression of the hindgut bacteria of the migratory locust Locusta migratoria manilensis. Sci. Rep. 5:17365, DOI: 10.1038/ srep17365.
Weiss L.M. and Becnel J.J. (Eds.). 2014. Microsporidia: Pathogens of opportunity. Wiley-Blackwell, Ames, Iowa.
Address for correspondence: Carlos E. Lange. Comisión Investigaciones Científicas Provincia Buenos Aires (CICPBA), Centro de Estudios Parasitológicos y de Vectores (CEPAVE), Universidad Nacional La Plata (UNLP) - CONICET, Boulevard 120 S/N e/ Avda. 60 y Calle 64, La Plata (1900), Argentina; e-mail: carlosl@cepave.edu.ar
