Translator Disclaimer
1 December 2005 The host and geographical range of the grasshopper pathogen Paranosema (Nosema) locustae revisited
Carlos E. Lange
Author Affiliations +
Abstract

Host and geographical ranges are updated for the microsporidium Paranosema locustae; this pathogen was developed in the USA as a long-term microbial control agent of grasshoppers. Currently known to be susceptible to P. locustae, either naturally or experimentally, are 121 species of Orthoptera from North and South America, Africa, Australia, China, and India. Most belong to the Acrididae (112), and within this family, to the Melanoplinae (36), Oedipodinae (35), and Gomphocerinae (35). The host range of P. locustae, as presently understood, is based largely on morphology and could change if molecular techniques revealed cryptic species. The North American isolate is not only the best studied, but the one established after its introduction into Argentina, and produced and used in China: it can be considered a generalist pathogen. As such, P. locustae may have the ability to alter, through differences in host susceptibilities, the structure of grasshopper assemblages in areas where it was not present before. Long-term careful monitoring of key grasshopper species in areas of pathogen introduction/establishment may reveal such effects.

Introduction

Paranosema locustae is a spore-forming pathogen of the adipose tissue of orthopterans that was isolated, selected, and developed in the USA as a long-term microbial control agent of grasshoppers (Henry & Oma 1981, Johnson 1997, Lockwood et al. 1999). P. locustae belongs to the Microsporidia, a group of unicellular eukaryotes that are obligate intracellular parasites of animals and some protists (Wittner & Weiss 1999). Microsporidia were historically regarded as Protozoa or Archezoa, but recent studies at the molecular level have shown they are actually related to Fungi (Keeling & Fast 2002).

In North America, Steinhaus (1951) first noticed P. locustae, albeit without naming it, in 3 species of grasshoppers of the genus Melanoplus from Montana. Soon after, Canning (1953) described P. locustae as Nosema locustae, using diseased African migratory locusts, Locusta migratoria migratorioides, from a rearing colony at the Imperial College Field Station in London. Sokolova et al. (2003), while erecting the new genus Paranosema for another microsporidian pathogen of Orthoptera from the cricket Gryllus bimaculatus, transferred N. locustae to Paranosema, based on molecular and ultrastructural grounds, erecting the new combination P. locustae. Even more recently, Slamovits et al. (2004) proposed another new combination, Antonospora locustae; but Sokolova et al. (2005) provided reasons for favoring the name P. locustae.

One of several factors that permitted the selection of P. locustae for its development as a microbial control agent, is its wide host range among acridomorphs. While the host range of most Microsporidia is relatively narrow (Solter et al. 2005), host specificity is a species-based character in Microsporidia, that should be considered individually (Solter & Becnel 2003). The unusually broad host range of P. locustae was observed early in its development as a biocontrol agent (Henry 1969), and judged to be desirable (Henry 1977). This was because many grasshopper species are considered pests, and frequently, when outbreaks occur, more than one (and sometimes several) species are involved.

Henry (1969) provided the first list of hosts that he knew to be susceptible, which included 55 North American species, 53 of them acridomorphs, one cricket, and one tetrigid. Almost 2 decades later, Brooks (1988) presented a new list of worldwide susceptible insects, all of them Orthoptera, expanding the known host range of P. locustae to 95 species. Since then, additional work has been conducted on P. locustae, much of it outside of North America, in Argentina, China and South Africa. The present update compiles the current available knowledge on the host and geographical range of P. locustae. Caution should be exerted when assessing the currently known host range of P. locustae because it is largely based on morphological grounds. The possibility that a scrutiny of different isolates at the molecular level could reveal the occurrence of cryptic species cannot be ruled out.

Host range and distribution

Table 1 shows, by continent, family, and subfamily, all the species reported to be susceptible, either naturally or experimentally, to P. locustae, which at present total 121. Of these, 112 species are Acrididae, and the remaining 9 susceptible species belong to the families Romaleidae (3), Gryllidae (1), Oecanthidae (1), Tetrigidae (1), Tettigonidae (1), and Pyrgomorphidae (2). Among the Acrididae, susceptible species are in the subfamilies Acridinae (2), Calliptaminae (1), Catantopinae (2), Cyrtacanthacridinae (5), Copiocerinae (1), Eyprepocnemidae (3), Gomphocerinae (23), Melanoplinae (36), Oedipodinae (35), Oxyinae (3), and Tropidopolinae (1). Based on the host species involved in the natural infections (ecological host range, Solter et al. 2005), on the natural and induced (after field applications) prevalences, the results of laboratory bioassays (physiological host range, Solter et al. 2005), and on the intensity of infections (spore loads per individual), it appears that species in the subfamilies Melanoplinae, Oedipodinae, and Gomphocerinae are generally more susceptible than species in other subfamilies (Canning 1953; Henry 1969; Henry et al. 1973; Ewen 1983; Lockwood 1988; Whitlock & Brown 1991; Bomar et al. 1993; Wang & Yu 1994; Yuhua 1997; Lange 2003 a, b). It is important to note that in the earlier literature on host range of P. locustae (Henry 1969), most species that by then were treated as Cyrtacanthacridinae are now considered to be within the Melanoplinae.

P. locustae has been reported to be native in North America, India and South Africa (Henry 1969, Ewen 1983, Srivastava & Bhanotar 1985, Raina et al. 1987, Whitlock & Brown 1991). It has been mentioned for the Irkutsk region of Russia (Issi & Lipa 1968), but later apparently treated by Issi & Krylova (1987) as a different species, Nosema chorthippi. However, aside from the original description by Canning (1953), virtually all available knowledge on P. locustae comes from research on the North American isolate, while the records for India were poorly diagnosed.

The North American isolate of P. locustae has become established after its introduction in the Pampas of Argentina (Sokolova & Lange 2002, Lange 2003a, Lange & De Wysiecki 2005), and it is produced and used in China for the control of grasshoppers and locusts (Long 1995, Wangpeng et al. 2001, Shi & Njaqi 2004). Unfortunately, the fate of introductions conducted in other countries, such as Australia, Cape Verde, Mali, Niger, and Mauritania has not been explored.

The present update shows the significant, relatively recent, expansion in host and geographical ranges of P. locustae, mostly as a result of applied use. Due to the extremely wide host range acknowledged at present for P. locustae, this microsporidium clearly qualifies as a generalist pathogen. In assessing the significance of this, those infections recorded in field-collected individuals, either naturally (labeled as N in Table 1), or as induced infections following an introduction or augmentation event (labeled as I and A in Table 1), are of particular relevance. Although the physiological host range can be used as an indicator of ecological host range, it needs to be carefully observed and evaluated. When forced into experimental hosts during bioassays, some microsporidia are known to develop atypical infections that are not likely to occur or persist in the field (Solter et al. 2005).

A generalist pathogen has the ability to alter, through differences in host susceptibilities, the structure of insect assemblages when established in areas where it was not present before (Bonsall 2004). In this sense, regular, long-term monitoring in grasshopper communities of Argentina and China should prove very informative in the long run. Key grasshopper species, in terms of known or potential susceptibility, rareness, and range of geographical distribution, should be designated within areas of pathogen establishment and surroundings. Careful attention should be paid in future surveys to their populations and eventual infection status.

Acknowledgments

I am grateful to Dr. G. Morris and the anonymous reviewers for the suggestions and comments that improved the manuscript. This work was in part possible through a grant (number 2062) from “Consejo Nacional de Investigaciones Cientificas y Técnicas (CONICET)”.

References

1.

ChR. Bomar, J. A. Lockwood, M. A. Pomerinke, and J. D. French . 1993. Multiyear evaluation of the effects of Nosema locustae (Microsporidia:Nosematidae) on rangeland Grasshopper (Orthoptera: Acrididae) population density and natural biological controls. Environmental Entomology 22:489–497. Google Scholar

2.

M. B. Bonsall 2004. The impact of diseases and pathogens on insect population dynamics. Physiological Entomology 29:223–236. Google Scholar

3.

W. M. Brooks 1988. Entomogenous Protozoa. pp. 1–149. In: Ignoffo, C.M. (Ed.), Microbial Insecticides, Vol. 5, Handbook of naturally occurring pesticides. CRC, Boca Raton. Google Scholar

4.

E. U. Canning 1953. A new microsporidian, Nosema locustae n. sp., from the fat body of the African migratory locust, Locusta migratoria migratorioides. Parasitology 43:287–290. Google Scholar

5.

E. U. Canning 1962. The life cycle of Nosema locustae Canning in Locusta migratoria migratorioides, and its infectivity to other hosts. Journal of Invertebrate Pathology 4:237–247. Google Scholar

6.

A. B. Ewen 1983. Extension of the geographic range of Nosema locustae (Microspora) in grasshoppers (Orthoptera: Acrididae). The Canadian Entomologist 115:1049–1050. Google Scholar

7.

T. Habtewold, J. Landin, U. Wennergen, and K. O. Bergman . 1995. Life table for the tef grasshopper, Aiolopus longicornis under laboratory conditions and demographic effects of the pathogen Nosema locustae. Biological Control 5:497–502. Google Scholar

8.

J. E. Henry 1969. Extension of the host range of Nosema locustae in Orthoptera. Annals of the Entomological Society of America 62:452–453. Google Scholar

9.

J. E. Henry 1971. Experimental application of Nosema locustae for control of grasshoppers. Journal of Invertebrate Pathology 18:389–394. Google Scholar

10.

J. E. Henry 1977. Development of microbial agents for the control of Acrididae. Revista de la Sociedad Entomologica Argentina 36:125–134. Google Scholar

11.

J. E. Henry and E. A. Oma . 1974. Effect of prolonged storage of spores on field applications of Nosema locustae (Microsporidia: Nosematidae) against grasshoppers. Journal of Invertebrate Pathology 23:371–377. Google Scholar

12.

J. E. Henry and E. A. Oma . 1981. Pest control by Nosema locustae, a pathogen of grasshoppers and crickets. pp. 573–585. In: Burges D. (Ed.) Microbial control of pests and plant diseases 1970–1980 Academic Press, New York. Google Scholar

13.

J. E. Henry and J. A. Onsager . 1982. Experimental control of the Mormon cricket, Anabrus simplex, by Nosema locustae (Microsporidia: Nosematidae), a protozoan parasite of grasshoppers (Orthoptera: Acrididae). Entomophaga 27:197–201. Google Scholar

14.

J. E. Henry, K. Tiahrt, and E. A. Oma . 1973. Importance of timing, spore concentrations, and levels of spore carrier in applications of Nosema locustae (Microsporidia: Nosematidae) for control of grasshoppers. Journal of Invertebrate Pathology 21:23–272. Google Scholar

15.

J. E. Henry, J. L. Fowler, M. C. Wilson, and J. A. Onsager . 1985. Infection of West African grasshoppers with Nosema locustae (Protozoa: Microsporida: Nosematidae). Tropical Pest Management 31:144–147. Google Scholar

16.

I. V. Issi and J. J. Lipa . 1968. Report on identification of Protozoa pathogenic for insects in the Soviet Union (1961–1966), with descriptions of some new species. Acta Protozoologica 6:281–291. Google Scholar

17.

I. Issi and S. V. Krylova . 1987. Locusts microsporidia. In: Shumakov E.M. (Ed.) Locusts, ecology and control methods. Proceedings All-Union Institute for Plant Protection St. Petersburg 58–62 (In Russian). Google Scholar

18.

D. L. Johnson 1997. Nosematidae and other Protozoa as agents for the control of grasshoppers and locusts: current status and prospects. Memoirs of the Entomological Society of Canada 171:375–389. Google Scholar

19.

P. J. Keeling and N. M. Fast . 2002. Microsporidia: Biology and evolution of highly reduced intracellular parasites. Annual Reviews of Microbiology 56:93–116. Google Scholar

20.

C. E. Lange 2002. El desarrollo de Nosema locustae Canning (Protozoa: Microsporidia) para el control biológico de tucuras (Orthoptera: Acridoidea) y las consecuencias de su utilización en la Argentina. Revista de la Sociedad Entomologica Argentina 61:1–9. Google Scholar

21.

C. E. Lange 2003a. Long-term patterns of occurrence of Nosema locustae Canning and Perezia dichroplusae Lange (Microsporidia) in grasshoppers (Orthoptera: Acrididae) of the Pampas, Argentina. Acta Protozoologica 42:309–315. Google Scholar

22.

C. E. Lange 2003b. Niveles de esporulación experimentales y naturales del agente de biocontrol Nosema locustae (Microsporidia) en especies de tucuras y langostas (Orthoptera: Acridoidea) de la Argentina. Revista de la Sociedad Entomologica Argentina 62:15–22. Google Scholar

23.

C. E. Lange and M. L. De Wysiecki . 2005. Espectro hospedador, prevalencias y dispersion del entomopatogeno Paranosema locustae (Microsporidia) en tucuras (Orthoptera: Acridoidea) del Sudoeste de Buenos Aires. Revista de Investigaciones Agropecuarias 34:129–143. Google Scholar

24.

C. E. Lange, N. E. Sanchez, and E. Wittenstein . 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. Google Scholar

25.

W. X. Liu and Y-H. Yan . 2000. A preliminary investigation on sustainable management of Oxya chinensis (Thunb.) mainly with biological agents. Acta Entomologica Sinica 43:186–190. Google Scholar

26.

J. A. Lockwood 1988. Biology and recommendations for the use of Nosema locustae Canning: a biological control agent of grasshoppers. Wyoming Agriculture Experiment Station Bulletin B-917. Google Scholar

27.

J. A. Lockwood, C. R. Bomar, and A. B. Ewen . 1999. The history of biological control with Nosema locustae: lessons for locust management. Insect Science and Applications 19:333–350. Google Scholar

28.

Z. Long 1994. Epizootic and transmission of Nosema locustae in the populations of grasshoppers and locusts. Ph.D. Thesis, Dept Plant Protection, Beijing Agricultural University, Beijing. Google Scholar

29.

Z. Long 1995. A preliminary survey on the epizootics of infection of Nosema locustae among grasshoppers in rangeland. Acta Agrestia Sinica 3:223–229. Google Scholar

30.

Z. Long, S. Wangpeng, Y. Yuhua, L. Boneng, W. Manfeng, Y. Shuimei, and L. Deqing . 2001. Relationships between application rate of Nosema locustae and infection of Locusta migratoria manilensis in Hainan province. Journal of China Agricultural University 6:90–95. Google Scholar

31.

G. C. Luna, J. E. Henry, and R. A. Ronderos . 1981. Infecciones experimentales y naturales con protozoos patógenos en acridios de la Republica Argentina. Revista de la Sociedad Entomologica Argentina 40:243–247. Google Scholar

32.

D. S. Ma, S. L. Bai, and Z. H. Li . 2005. Studies on sustainable controlling rangeland grasshoppers with Nosema locustae in Chaidamu of Qinghai province. Natural Science Version 36:199–204. Google Scholar

33.

J. Moulden 1981. Disease could control grasshoppers. Journal of Agriculture 22:53–54. Google Scholar

34.

S. K. Raina, M. M. Rai, and A. M. Khurad . 1987. Grasshopper and locust control using microsporidian insecticides. pp. 345–365. In: Maramorosch K. (Ed.) Biotechnology in Invertebrate Pathology and Cell Culture, Academic Press, New York. Google Scholar

35.

S. K. Raina, S. Das, M. M. Rai, and A. M. Khurad . 1995. Transovarial transmission of Nosema locustae (Microsporidia: Nosematidae) in the migratory locust Locusta migratoria migratorioides. Parasitology Research 81:38–44. Google Scholar

36.

W. P. Shi and P. G. N. Njaqi . 2004. Disruption of aggregation behaviour of Oriental migratory locusts (Locusta migratoria manilensis) infected with Nosema locustae. Journal of Applied Entomology 128:414–418. Google Scholar

37.

C. S. Slamovits, B. A. P. Williams, and P. J. Keeling . 2004. Transfer of Nosema locustae (Microsporidia) to Antonospora locustae n. com. based on molecular and ultrastructural data. Journal of Eukaryotic Microbiology 51:207–213. Google Scholar

38.

J. Sokolova and C. E. Lange . 2002. An ultrastructural study of Nosema locustae Canning (Microspora) from three species of Acrididae (Orthoptera). Acta Protozoologica 41:221–237. Google Scholar

39.

Y. Y. Sokolova, V. V. Dolgihk, E. V. Morzhina, E. S. Nassonova, I. V. Issi, R. S. Terry, J. E. Ironside, J. E. Smith, and C. R. Vossbrinck . 2003. Establishment 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. Journal of Invertebrate Pathology 84:159–172. Google Scholar

40.

Y. Y. Sokolova, I. V. Issi, E. V. Morzhina, Y. S. Tokarev, and C. R. Vossbrinck . 2005. Ultrastructural analysis supports transferring Nosema whitei Weiser 1953 to the genus Paranosema and creation [of] a new combination, Paranosema whitei. Journal of Invertebrate Pathology 90:122–126. Google Scholar

41.

L. F. Solter and J. J. Becnel . 2003. Environmental safety of Microsporidia. pp. 93–118. In: Hokkanen H, Hajek A. (Eds) Environmental Impacts of Microbial Insecticides. Kluwer Academic Publishers, Netherlands. Google Scholar

42.

L. F. Solter, J. V. Maddox, and C. R. Vossbrinck . 2005. Physiological host specificity: a model using the European corn borer, Ostrinia nubilalis (Hubner) (Lepdioptera: Crambidae) and microsporidia of row crop and other stalk-boring hosts. Journal of Invertebrate Pathology 90:127–130. Google Scholar

43.

Y. N. Srivastava and R. K. Bhanotar . 1985. A new record of a protozoan, Nosema locustae Canning infecting desert locusts from Rajasthan. Indian Journal of Entomology 45:500–501. Google Scholar

44.

E. A. Steinhaus 1951. Report on diagnoses of diseased insects 1944–1950. Hilgardia 20:629–678. Google Scholar

45.

L. Wang and X. Yu . 1994. The mass production and application of Nosema locustae against grasshoppers. Acta Agrestia Sinica 2:49–54. Google Scholar

46.

S. Wangpeng, Y. Yan, E. Zhu, and W. Zhang . 2001. Sustainable management of locust Locusta migratoria manilensis using Nosema locustae in Hainan Province. Journal of Plant Protection 28:207–212. Google Scholar

47.

V. H. Whitlock and S. T. Brown . 1991. First record for Nosema locustae in the Brown locust Locustana pardalina in South Africa, and the yield of spores in laboratory bioassays. Journal of Invertebrate Pathology 58:164–167. Google Scholar

48.

M. Wittner and L. M. Weiss . (Eds). 1999. The Microsporidia and Microsporidiosis. American Society of Microbiology Press, Washington, D.C. Google Scholar

49.

Y. Yuhua 1997. The sustainable management of grasshoppers and locusts in China. Metaleptea (The Orthopterists' Newsletter) 17:17. Google Scholar

50.

J. Zang, J. Cao, G. Li, Ch Li, and Y. Yan . 2001. Biological control of Oxya chinensis by using Nosema locustae. Chinese Journal of Biological Control 17:126–128. Google Scholar

Table 1.

Species of Orthoptera, by continent, family, and subfamily, known to be susceptible to Paranosema locustae. (N) natural infection in a wild host, (I) infection in a wild host after an introduction event of the pathogen, (E) experimental infection resulting from a laboratory bioassay, (S) spontaneous infection in a host rearing facility, (A) infection in a wild host after application in a general area where Paranosema locustae is known to be native.

i1082-6467-14-2-137-t101.gif

Table 1.

Continued

i1082-6467-14-2-137-t102.gif
Carlos E. Lange "The host and geographical range of the grasshopper pathogen Paranosema (Nosema) locustae revisited," Journal of Orthoptera Research 14(2), 137-141, (1 December 2005). https://doi.org/10.1665/1082-6467(2005)14[137:THAGRO]2.0.CO;2
Published: 1 December 2005
JOURNAL ARTICLE
5 PAGES


SHARE
ARTICLE IMPACT
Back to Top