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Journal of Chemical Ecology

, Volume 24, Issue 10, pp 1697–1706 | Cite as

Inhibitory Effect of Termite Fecal Pellets on Fungal Spore Germination

  • Rebeca B. Rosengaus
  • Matthew R. Guldin
  • James F. A. Traniello
Article

Abstract

The dampwood termite Zootermopsis angusticollis lines nest chambers and galleries with fecal pellets. The antifungal properties of feces were tested by recording germination rates of spores of the fungus Metarhizium anisopliae that had been incubated with various concentrations of fecal material. The presence of fecal pellet material significantly decreased the germination rates of spores relative to those of control spore solutions lacking fecal material. Spore germination rates were inversely proportional to the amount of fecal matter present in the spore–feces suspensions but were independent of incubation time. The fungistatic effect of the fecal material is virtually immediate and does not require prolonged contact with spores to inhibit germination. This mechanism of biochemical protection may reduce risks of fungal infection in termite nests.

Termite fungal pathogen Zootermopsis angusticollis Metarhizium anisopliae disease spore germination 

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REFERENCES

  1. Attygalle, A. B., Siegel, B., Vostrowsky, O., Bestmann, H. J., and Maschwitz, U. 1989. Chemical composition and function of metapleural gland secretion of the ant Crematogaster deformis Smith (Hymenoptera: Myrmicinae). J. Chem. Ecol. 15:317–327.Google Scholar
  2. Batra, L. R., and Batra, S. W. T. 1966. Fungus-growing temites of tropical India and associated fungi. J. Kans. Entomol. Soc. 39:725–738.Google Scholar
  3. Batra, L. R., and Batra, S. W. T. 1979. Termite-fungus mutualism, pp. 117–163, in L. R. Batra (ed.). Insect-Fungus Symbiosis, Nutrition, Mutualisms, and Commensalism. Wiley, New York.Google Scholar
  4. Batra, L. R., Batra, S. W. T., and Bohart, G. E. 1973. The mycoflora of domesticated and wild bees (Apoidea). Mycopathol. Mycol. Appl. 49:13–44.Google Scholar
  5. Beattie, A. J., Turnbull, C., Hough, T., Jobson, S., and Knox, R. B. 1985. The vulnerability of pollen and fungal spores to ant secretions: evidence and some evolutionary implications. Am. J. Bot. 72:606–614.Google Scholar
  6. Beattie, A. J., Turnbull, C., Hough, T., Jobson, S., and Knox, R. B. 1986. Antibiotic production: A possible function of the metapleural glands of ants (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am. 79:448–450.Google Scholar
  7. Blackwell, M., and Rossi, W. 1986. Biogeography of fungal ectoparasites of termites. Mycotaxon 25:581–601.Google Scholar
  8. Burges, A., and Fenton, E. 1953. The effect of carbon dioxide on the growth of certain soil fungi. Trans. Br. Mycol. Soc. 36:104–108.Google Scholar
  9. Clerk, G. C. 1969. Influence of soil extracts on the germination of conidia of the fungi Beauveria bassiana and Paecilomyces farinosus. J. Invertebr. Pathol. 13:120–124.Google Scholar
  10. Dykes, G. A. 1995. Bacteriocins: Ecological and Evolutionary Significance. Tree 10:186–189.Google Scholar
  11. Eutik, M. L., Veivers, P., O'Brien, R. W., and Slaytor, M. 1978. Dependence of the higher termite Nasutitermes exitosus and the lower termite, Coptotermes lacteus on their gut flora. J. Insect Physiol. 24:363–368.Google Scholar
  12. Gambino, P. 1993. Antibiotic activity of larval saliva of Vespula wasps. J. Invertebr. Pathol. 61:110.Google Scholar
  13. Gonnet, M., and Lavie, P. 1960. Influence du chauffage sur le facteur antibiotique présent dans les miels. Ann. Abeille 3:349–364.Google Scholar
  14. GrassÉ, P. P. 1982. Termitologia. Anatomie-Physiologie-Reproduction des Termites. Masson, Paris.Google Scholar
  15. GrassÉ, P. P. 1984. Termitologia. Fondation des Sociétés Construction. Masson, Paris.Google Scholar
  16. GrassÉ, P. P. 1986. Termitologia. Comportement-Socialité-Ecologie-Evolution-Systématique. Masson, Paris.Google Scholar
  17. Hajeck, A. E., and Renwick, J. A. A. 1993. Incorporation of Quercus rubra foliage into artificial diet alters development of a fungal pathogen of Lymantria dispar. Entomol. Exp. Appl. 68:265–267.Google Scholar
  18. Haverty, M. I., and Howard, R. W. 1979. Effects of insect growth regulators on subterranean termites: Induction of differentiation, defaunation, and starvation. Ann. Entomol. Soc. Am. 72:503–508.Google Scholar
  19. Hendee, E. C. 1934. The association of termites and fungi, pp. 105–116, in C. A. Kofold (ed.). Termites and Termite Control. University of California, Berkeley.Google Scholar
  20. HÖlldobler, B., and Engel-Siegel, H. 1984. On the metapleural gland of ants. Psyche 91:201–224.Google Scholar
  21. HÖlldobler, B., and Wilson, E. O. 1990. The Ants. Harvard University Press, Cambridge, Massachusetts.Google Scholar
  22. Jouvenaz, D. P. 1986. Diseases of fire ants: Problems and opportunities, pp. 327–338, in C. S. Lofgren and R. K. Vander Meer (eds.). Fire Ants and Leaf-cutting Ants. Westview Press, Boulder, Colorado.Google Scholar
  23. Keller, S., and Zimmermann, G. 1989. Mycopathogens of soil insects, pp. 239–270, in N. Wilding, N. M. Collins, P. M. Hammond, and J. F. Webber (eds.). Insect-Fungus Interactions. Academic Press, San Diego.Google Scholar
  24. Kermarrec, A., Febvay, G., and Decharme, M. 1986a. Protection of leaf-cutting ants from biohazards: Is there a future for microbiological control?, pp. 339–356, in C. S. Lofgren and R. K. Vander Meer (eds.). Fire Ants and Leaf-cutting Ants. Westview Press, Boulder, Colorado.Google Scholar
  25. Kermarrec, A., Decharme, M., and Febvay, G. 1986b. Leaf-cutting ant symbiotic fungi: A synthesis of recent research, pp. 231–266, in C. S. Lofgren and R. K. Vander Meer (eds.). Fire Ants and Leaf-cutting Ants. Westivew Press, Boulder, Colorado.Google Scholar
  26. Khuong, B. N., and Smart, G. C. 1994. Neosteinernema longicurvicuda n. gen. n. sp. (Rhabditida: Steinemematodae), a parasite of the termite Reticulitermes flavipes. J. Nematol. 26:162–174.Google Scholar
  27. Lavie, P. 1960a. Les substances antibactriennes dans colonie d'abeilles (Apis mellifica) (Ire partie). Ann. Abeille 3:103–184.Google Scholar
  28. Lavie, P. 1960b. Les substances antibactriennes dans colonie d'abeilles (Apis mellifica) (fin). Ann. Abeille 3:201–306.Google Scholar
  29. Lavie, P. 1960c. Les antibiotiques chez les insectes sociaux. Ann. Abeille 3:270–276.Google Scholar
  30. Lutikova, L. I. 1990. The influence of soil substrates from the Anacanthotermes ahngerianus Jac. termite-house on the development of enthomorathogenic fungi. Mycol. Physiol. 24:520–528. (In Russian).Google Scholar
  31. Ljutikova, L. I., and Judina, T. G. 1996. Antibacterial activity of some exudates of Anacanthotermes ahngerianus Jacobson (Isoptera: Hodotermitidae). XX International Congress of Entomology, Firenze, p. 105.Google Scholar
  32. Maschwitz, U., and Tho, Y. P. 1974. Chinone als Wehrsubstanzen bei Einigen Orientalische Macrotermitinen. Insectes Soc. 21:231–234.Google Scholar
  33. Maschwitz, U., Koob, K., and Schildknecht, H. 1970. Ein Beitrag zur Funktion der Metathoracaldrüse der Ameisen. J. Insect Physiol. 16:387–404.Google Scholar
  34. Mauldin, J. K., and Rich, N. M. 1980. Effect of chlorotetracycline and other antibiotics on protozoan numbers in the eastern subterranean termite. J. Econ. Entomol. 73:123–128.Google Scholar
  35. Michener, C. D. 1974. The Social Behavior of Bees. A Comparative Study. Belknap Press, Cambridge.Google Scholar
  36. Noirot, C. 1969. Glands and secretions. pp. 89–123, in K. Krishna and F. M. Weesner (eds.). Biology of Termites. Academic Press, New York.Google Scholar
  37. Obin, S. M., and Vander Meer, R. K. 1985. Gaster flagging by fire ants (Solenopsis spp.): Functional significance of venom dispersal behavior. J. Chem. Ecol. 11:1757–1768.Google Scholar
  38. Olagbemiro, T. O., Lajide, L., Sani, K. M., and Staddon, B. W. 1988. 2-Hydroxy-5-methyl-1,4-benzoquinone from the salivary gland of the soldier termites Odontotermes magdalenae. Experientia 44:1022–1025.Google Scholar
  39. Rich, S. 1969. Quinones, pp. 647–648, in D. C. Torgeson (ed.). Fungicides: An Advanced Treatise, Vol. 2. Academic Press, New York.Google Scholar
  40. Rosengaus, R. B., and Traniello, J. F. A. 1993. Disease risk as a cost of outbreeding in the termite Zootermopsis angusticollis. Proc. Natl. Acad. Sci. U.S.A. 90:6641–6645.Google Scholar
  41. Rosengaus, R. B., and Traniello, J. F. A. 1994. Pathogens and termite population biology, p. 184. XII Congress of the International Union for the Study of Social Insects IUSSI, Université Paris Nord, Paris.Google Scholar
  42. Rosengaus, R. B., and Traniello, J. F. A. 1997. Pathobiology and disease transmission in dampwood termites [Zootermopsis angusticollis (Isoptera: Termopsidae)] infected with the fungus Metarhizium anisopliae (Deuteromycotina: Hypomycetes). Sociobiology 30:185–195.Google Scholar
  43. Rosengaus, R. B., Maxmen, A. B., Coates, L. E., and Traniello, J. F. A. Disease resistance: A benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav. Ecol. Sociobiol. in press.Google Scholar
  44. Sannasi, A., and Sundara Rajulu, G. 1967. Occurrence of antimicrobial substance in the exudate of physogastric queen termites, Termes redemanni Wasmann. Curr. Sci. 16:436–437.Google Scholar
  45. Schmidt, J. O. 1986. Chemistry, pharmacology, and chemical ecology of ant venoms, pp. 425–508, in T. Piek (ed.). Venoms of the Hymenoptera. Academic Press, Orlando, Florida.Google Scholar
  46. Sikorowski, P. P., and Lawrence, A. M. 1994. Microbial contamination and insect rearing. Am. Entomol. 40:240–253.Google Scholar
  47. SPSS. 1990. SPSS/PC + 4.0 Advanced Statistics Manual. Chicago.Google Scholar
  48. Sreng, L. 1984. Morphology of the sternal and tergal glands producing the sexual pheromones and the aphrodisiacs among the cockroaches of the subfamily Oxyhaloinae. J. Morphol. 182:279–294.Google Scholar
  49. Sreng, L. 1993. Cockroach mating behaviors, sex pheromones, and abdominal glands (Dictyoptera: Blaberidae). J. Insect Behav. 6:715–735.Google Scholar
  50. Stuart, A. M. 1969. Social behavior and communication, pp. 193–232, in K. Krishna and F. M. Weesner (eds.). Biology of Termites, Vol. 1. Academic Press, New York.Google Scholar
  51. Thaxter, R. 1914. On certain peculiar fungus parasites of living insects. Bot. Gaz. 58:235–253.Google Scholar
  52. Thomas, R. J. 1987. Factors affecting the distribution and activity of fungi in the nests of Macrotermitinae (Isoptera). Soil Biol. Biochem. 19:343–349.Google Scholar
  53. Thorne, B. L., and Carpenter, J. M. 1992. Phylogeny of the Dictyoptera. Syst. Entomol. 17:253–268.Google Scholar
  54. Toumanoff, C. 1966. Observations sur les affections bacteriennes des termites en saintonge (Reticulitermes santonensis de Feytaud). Insectes Soc. 13:155–164.Google Scholar
  55. Vander Meer, R. K. 1983. Semiochemicals and the red imported fire ant (Solenopsis invicta Buren) (Hymenoptera: Formicidae). Fla. Entomol. 66:139–161.Google Scholar
  56. Veal, D. A., Trimble, J. E., and Beattie, A. J. 1992. Antimicrobial properties of secretions from the metapleural glands of Myrmecia gulosa (the Australian bull ant). J. Appl. Bacteriol. 72:188–194.Google Scholar
  57. Waller, D. A., and La Fage, J. P. 1987. Nutritional ecology of termites, pp. 487–532, in F. Slansky and J. G. Rodriguez (eds.). Nutritional Ecology of Insects, Mites, and Spiders. Wiley, New York.Google Scholar
  58. Watson, A. G., and Ford, E. J. 1972. Soil fungistasis-a reappraisal. Annu. Rev. Phytopathol. 10:327–348.Google Scholar
  59. Wilson, E. O. 1971. The Insect Societies. Harvard University Press, Cambridge, Massachusetts.Google Scholar
  60. Wood, T. G., and Thomas, R. J. 1989. The mutualistic association between Macrotermitinae and Termitomyces, pp. 69–92, in N. Wilding, N. M. Collins, P. M. Hammond and J. F. Webber (eds.). Insect-Fungus Interactions. Academic Press, San Diego.Google Scholar
  61. Young, S. Y., Yang, J. G., and Felton, G. W. 1995. Inhibitory effects of dietary tannins on the infectivity of a nuclear polyhedrosis virus to Helicoverpa zea (Noctuidae: Lepidoptera). Biol. Control 5:145–150.Google Scholar
  62. Zoberi, M. H. 1995. Metarhizium anisopliae, a fungal pathogen of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Mycologia 87:354–359.Google Scholar

Copyright information

© Plenum Publishing Corporation 1998

Authors and Affiliations

  • Rebeca B. Rosengaus
    • 1
  • Matthew R. Guldin
    • 1
  • James F. A. Traniello
    • 1
  1. 1.Biology DepartmentBoston UniversityBoston

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