Susceptibility of seven termite species (Isoptera) to the entomopathogenic fungus Metarhizium anisopliae

Sociobiology

Volumn 54, Issue 3, 2009, Pages 723-748

  Chouvenc, Thomas ^a   Su, Nan Yao ^a   Robert, Alain ^b,c  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Disease resistance; Metarhizium anisopliae; Nesting ecology; Pathogen; Termite

Indexed keywords

FUNGI; HODOTERMES MOSSAMBICUS; HODOTERMITIDAE; HODOTERMOPSIS SJOESTEDTI; ISOPTERA; KALOTERMES; KALOTERMITIDAE; MASTOTERMES DARWINIENSIS; MASTOTERMITIDAE; METARHIZIUM ANISOPLIAE; NASUTITERMES; PRORHINOTERMES; RHINOTERMITIDAE; TERMITIDAE; TERMOPSIDAE;

EID: 72249116887     PISSN: 03616525     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Abe, T. 1987. Evolution of life types in termites. In: Evolution and Coadaptation in Biotic Communities. (S. Kawano, J. H. Connell and T. Hidaka, Eds.), University of Tokyo Press, Tokyo, pp. 125-148.
2. Abe, T., D. E. Bignell & M. Higashi 2000. Termites: Evolution, Sociality, Symbiosis, Ecology, Kluwer Academic, Dordrecht/Norwell.
3. Arruda, W., I. Lubeck, A. Schrank & M. H. Vainstein 2005. Morphological alterations of Metarhizium anisopliae during penetration of Boophilus microplus ticks. Exp. Appl. Acarol. 37: 231-244.
4. Bidochka, M. J. & C. L. Small 2005. Phylogeography of Metarhizium, an insect pathogenic fungus. In: Insect-Fungal Associations, Ecology and Evolution (F. E. Vega and M. Blackwell, Eds.), Oxford University Press, New York. pp. 28-50.
5. Bridge, P. D., C. Prior, J. Sagbohan, C. J. Lomer, M. Carey & A. Buddie 1997. Molecular characterization of isolates of Metarhizium from locusts and grasshoppers. Biodivers. Conserv. 6: 177-189. (Pubitemid 27164743)
6. Brugerolle, G. & C. Bordereau 2006. Immunological and ultrastructural characterization fo spirotrichonymphidflagellates from Reticulitermes grassei and R. flavipes (syn. R. santonensis), with special reference to Spirotrichonympha, Spironympha and Microjoenia. Org. Divers. Evol. 6: 109-123.
7. Bulmer, M. & R. H. Crozier 2004. Duplication and diversifying selection among termite antifungal peptides. Mol. Biol. Evol. 21: 2256-2264.
8. Chouvenc, T., N.-Y. Su & M. L. Elliott 2008a. Interaction between the subterranean termite Reticulitermes flavipes (Isoptera: Rhinotermitidae) and the entomopathogenic fungus Metarhizium anisopliae in foraging arenas. J. Econ. Entomol. 101: 885-893.
9. Chouvenc, T., N.-Y. Su & M. L. Elliott 2008b. Antifungal activity of the termite alkaloid norharmane against the mycelial growth of Metarhizium anisopliae and Aspergillus nomius. J. Invertebr. Pathol. 99: 345-347.
10. Chouvenc, T., N.-Y. Su & A. Robert 2009a. Cellular encapsulation in the eastern subterranean termite, Reticulitermes flavipes (Isoptera), against infection by the entomopathogenic fungus Metarhizium anisopliae. J. Invertebr. Pathol. 101: 234-241.
11. Chouvenc, T., N.-Y. Su & A. Robert 2009b. Inhibition of Metarhizium anisopliae in the alimentary tract of the eastern subterranean termite Reticulitermes flavipes. J. Invertebr. Pathol. 101: 130-136.
12. Cremer, S., S. A. O. Armitage & P. Schmid-Hempel 2007. Social immunity. Curr. Biol. 17: 693-702.
13. Culliney, T. W. & J. K. Grace 2000. Prospects for the biological control of subterranean termites (Isoptera: Rhinotermitidae), with special reference to Coptotermes formosanus. Bull. Entomol. Res. 90: 9-21.
14. Davidson, G. & D. Chandler 2005. Laboratory evaluation of entomopathogenic fungi against larvae and adults of onion maggot (Diptera: Anthomyiidae). J. Econ. Entomol. 96: 1848-1845.
15. Delate, K. M., J. K. Grace & C. H. M. Tome 1995. Potential use of pathogenic fungi in baits to control the Formosan subterranean termite (Isopt., Rhinotermitidae). J. Appl. Entomol. 119: 429-433.
16. Dong, C., J. Zhang, W. Chen, H. Huang & Y. Hu 2007. Characterization of a newly discovered China variety of Metarhizium anisopliae (M. anisopliae var. dcjhyium) for virulence to termites, isoenzyme, and phylogenic analysis. Microbiol Res. 162: 53-61.
17. Fargues, J., P. H. Robert & A. Vey 1976. Rôle du tégument et de la défense cellulaire des coléoptères hôtes dans la spécifité des souches entomopathogènes de Metarhizium anisopliae (Fungi imperfecti). C. R. Hebd. Seances Acad. Sci. Ser. D. 282: 2223-2226.
18. Fefferman, N. H., J. F. A. Traniello, R. B. Rosengaus & D. V. II Calleri 2007. Disease prevention and resistance in social insects: modelingthe survival consequences of immunity, hygienic behavior, and colony organization. Behav. Ecol. Sociobiol. 61: 565-577.
19. Grace, J. K. 1997. Biological control strategies for suppression of termites. J. Agric. Entomol. 14: 281-289.
20. Hänel, H. & J. A. L. Watson 1983. Preliminary field tests on the use of Metarhizium anisopliae for the control of Nasutitermes exitiosus (Hill) (Isoptera: Termitidae). Bull. Entomol. Res. 73: 305-313.
21. Inward, D. J. G., G. Beccaloni & P. Eggleton 2007a. Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol. Let. 3: 331-335.
22. Inward, D. J. G., A. P. Vogler & P. Eggleton 2007b. A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol. Phyl. Evol. 44: 955-967.
23. Jones, W. E., J. K. G race & M. Tamashiro 1996. Virulence of seven isolates of Beauveria bassiana and Metarhizium anisopliae to Coptotermes formosanus (Isoptera: Rhinotermitidae). Environ. Entomol. 25: 481-487.
24. Klass, K.-D., C. Nalepa & N. Lo 2008. Wood-feeding cockroaches as models for termite evolution (Insecta: Dictyoptera) : Cryptocercus vs. Parasphaeria boleiriana. Mol. Biol. Evol. 46: 809-8017.
25. Kramm, K. R., D. F. West & P. G. Rockenbach 1982. Termite pathogens: transfer of the entomopathogen Metarhizium anisopliae between Reticulitermes sp. termites. J. Invertebr. Pathol. 40: 1-6.
26. Lai, P. Y., M. Tamashiro & J. K. Fujii 1982. Pathogenicity of six strains of entomogenous fungi to Coptotermes formosanus. J. Invertebr. Pathol. 39: 1-5.
27. Langewald, J., J. D. Mitchell, N. K. Maniania & C. Kooyman 2003. Microbial control of termites in Africa. In: Biological Control in IPM Systems in Africa (Neuenschwander, P., Borgemeister, C, Langewald, J. Eds.),. Cromwell Press, Trowbridge, UK. pp. 227-242.
28. Lamberty, M., D. Zachary, R. Lanot, C. Bordereau, A. Robert, J. A. Hoffmann & P. Bulet 2001. Insect immunity constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J. Biol. Chem. 276: 4085-4092.
29. Maketon, M., P. Sawangwan & W Sawatwarakul 2007. Laboratory study on the efficacy of Metarhizium anisopliae (Deuteromycota: Hyphomycetes) in controlling Coptotermes gestroi (Isoptera: Rhinotermitidae). Entomol. Gener. 30: 203-218.
30. Milner, R. J. 2000. Improved formulation of Metarhizium for biological control of termites. CSIRO Division of Entomology Technical Report no. 86. pp. 37.
31. Milner, R. J. 2003. Application of biological control agents in mound building termites (Isoptera: Termitidae) - Experiences with Metarhizium in Australia. Sociobiology 41: 419-428.
32. Milner, R. J., J. A. Staples & G. G. Lutton 1998a. The selection of an isolate of the Hyphomycete fungus, Metarhizium anisopliae for control of termites in Australia. Biol. Control. 3: 240-247.
33. Milner, R. J., J. A. Staples, T. R. Harley, G. G. Lutton, F. Driver & W. A. L. Watson 1998b. Occurrence of Metarhizium anisopliae in nests and feeding sites of Australian termites. Mycol. Res. 102: 216-220.
34. Milner, R. J., P. Samson & R. Morton 2003. Persistence of conidia of Metarhizium anisopliae in sugarcane fields: effect of isolate and formulation on persistence over 3.5 years. Biocontrol. Sci. Technol. 13: 507-516.
35. Moore, B. P. 1968. Studies on the chemical composition and function of the cephalic gland secretion in Australian termites. J. Ins. Physiol. 14: 33-39.
36. Myles, T. G. 2002a. Alarm, aggregation, and defense by Reticulitermes flavipes in response to a naturally occurring isolate of Metarhizium anisopliae. Sociobiology 40: 243-255.
37. Myles, T. G. 2002b. Laboratory studies on the transmission of Metarhizium anisopliae in the eastern subterranean termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae), with a method for applying appropriate doses of Conidia to trapped termites for release. Sociobiology 40: 265-276.
38. Neves, P. M. O. J & S. B. Alves 2004. External events related to the infection process of Cornitermes cumulans (Kollar) (Isoptera: Termitidae) by the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae. Neotrop. Entomol. 33: 051-056.
39. Pachamuthu, P., S. T. Kamble & G. Y. Yuen 1999. Virulence of Metarhizium anisopliae (Deuteromycotina: Hyphmycetes) strain ESC-1 to the German cockroach (Dictyoptera: Blatettellidae) and its compatibility with insecticides. J. Econ. Entomol. 92: 340-346.
40. Pie, M. R., R. B. Rosengaus & J. F. A. Traniello 2004. Nest architecture, activity pattern, worker density and the dynamics of disease transmission in social insects. J. Theor. Biol. 226: 45-51.
41. Prestwich, G. D. 1979a. Chemical defense by termite soldiers. J. Chem. Ecol. 5: 459-480.
42. Prestwich, G. D. 1979b. Interspecific variation in the defence secretions of Nasutitermes soldiers. Biochem. Syst. Ecol. 7: 211-221.
43. Quesada-Moraga, E., R. Santos-Quiros, P. Valverde-Garcia & C. Santiago-Alvarez 2004. Virulence, horizontal transmission, and sublethal reproductive effects of Metarhizium anisopliae (Anamorphic fungi) on the German cockroach (Blattodea: Blattellidae). J. Invertebr. Pathol. 87: 51-58.
44. Rath, A. C. 2000. The use of entomopathogenic fungi for control of termites. Biocontrol Sci Technol. 10: 563-581.
45. Rath, A. C. & C. A. Tidbury 1996. Susceptibility of Coptotermes acinaciformis (Isoptera: Rhinotermitidae) and Nasutitermes exitiosus (Isoptera: Termitidae) to two commercial isolates of Metarhizium anisopliae. Sociobiology 28: 67-72.
46. Rosengaus, R. B. & J. F. A. Traniello 1997. Pathobiology and disease transmission in dampwood termites [Zootermopsis angusticollis (Isoptera: Termopsidae)] infected with the fungus Metarhizium anisopliae (Deuteromycotina: Hypomycetes). Sociobiology 30: 185-195.
47. Rosengaus, R. B. & J. F. A. Traniello 2001. Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angustkollis. Behav. Ecol. Sociobiol. 50: 546-556.
48. Rosengaus, R. B., A. B. Maxmen, L. E. Coates & J. F. A. Traniello 1998a. Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angustkollis (Isoptera: Termopsidae). Behav. Ecol. Sociobiol. 44: 125-134.
49. Rosengaus, R. B., M. R. Guldin & J. F. A. Traniello 1998b. Inhibitory effect of termite fecal pellets on fungal spore germination. J. Chem. Ecol. 24: 1697-1706.
50. Rosengaus, R. B., M. L. Lefebvre, C. Jordan & J. F. A. Traniello 1999a. Pathogen alarm behavior in a termite: A new form of communication in social insects. Naturwissenschaften 86: 544-548.
51. Rosengaus, R. B., J. F. A. Traniello, T. Chen, J. J. Brown & R. D. Karp 1999b. Immunity in a social insect. Naturwissenschaften 86: 588-591.
52. Rosengaus, R. B., M. L. Lefebvre & J. F. A. Traniello 2000. Inhibition of fungal spore germination by Nasutitermes: Evidence for a possible antiseptic role of soldier defensive secretions. J. Chem. Ecol. 26: 21-39.
53. Rosengaus, R. B., J. E. Moustakas, D. V. II Calleri & J. F. A. Traniello 2003. Nesting ecology and cuticular microbial loads in dampwood (Zootermopsis angusticollis) and drywood termites (Incisitermes minor, I. schwarzi, Cryptotermes cavifions). J. Insect. Sci. 3: 31-37.
54. Rosengaus, R. B., J. F. A. Traniello, M. L. Lefebvre & A. B. Maxmen. 2004. Fungistatic activity of the sternal gland secretion of the dampwood termite Zootermopsis angusticollis, Insect. Soc. 51: 259-264.
55. Rosengaus, R. B., T. Cornelisse, K. Guschanski & J. F. A. Traniello 2007. Inducible immune proteins in the dampwood termite Zootermopsis angusticollis. Naturwissenschaften. 94: 25-33.
56. SAS Institute 2002. SAS/STAT user's guide, version 9.1. SAS Institute, Cary, NC.
57. Shah, P. A. & J. K. Pell 2003. Entomopathogenic fungi as biological control agents. Appl. Microbiol. Biotechnol. 61: 413-423.
58. Siderhurst, M. S., D. M. James, T. D. Blunt & L. B. Bjostad 2005. Antimicrobial activity of norharmane against the entomopathogenic fungus Metarhizium anisopliae (Metsch.) and the caste and phylogenetic distribution of this defense in termites (Insecta: isoptera). Sociobiology. 46: 563-577.
59. St. Leger, R. J. 2008. Studies on adaptations of Metarhizium anisopliae to file in the soil. J. Invertebr. Pathol. 98: 271-276.
60. Thompson, G. J., Y. C. Crozier & R. H. Crozier 2003. Isolation and characterization of a termite transferrin gene up-regulated on infection. Ins. Mol. Biol. 12: 1-7.
61. Wright, M. S., A. R. Lax, G. Henderson & J. Chen 2000. Growth response of Metarhizium anisopliae to termite nest volatiles Nephthalene and Fenchone. Mycologia 92: 42-45.
62. Wright, M. S., A. K. Raina & A. R. Lax 2005. A strain of the fungus Metarhizium anisopliae for controlling subterranean termites. J. Econ. Entomol. 98: 1451-1458.
63. Xu, P., M. Shi & X.-X. Chen 2009. Positive selection on termicins in one termite species, Macrotermes barneyi (Isoptera: Termitidae). Sociobiology 53: 739-753.
64. vYanagawa, A. & S. Shimizu 2007. Resistance of the termite, Coptotermes formosanus Shiraki to Metarhizium anisopliae due to grooming. BioControl 52: 75-85.
65. Zoberi, M. H. 1995. Metarhizium anisopliae, a fungal pathogen of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Mycologia 87: 354-359.