An experimental study of microbial nest associates of borneo's exploding ants (Camponotus [Colobopsis] species)

Journal of Hymenoptera Research

Volumn 18, Issue 2, 2009, Pages 341-360

  Davidson, D W ^a   Anderson, N F ^a   Cook, S C ^a,d   Bernau, C R ^a,e   Jones, T H ^b   Kamariah, A S ^c   Lim, L B ^c   Chan, C M ^c   Clark, D A ^b,f  

^a UNIVERSITY OF UTAH   (United States)

^b VIRGINIA MILITARY INSTITUTE   (United States)

^c UNIVERSITI BRUNEI DARUSSALAM   (Brunei Darussalam)

^d TEXAS A AND M UNIVERSITY   (United States)

^e UNIVERSITY OF IDAHO   (United States)

^f MAX PLANCK INSTITUT FÜR KOHLENFORSCHUNG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIDESMA; BACTERIA (MICROORGANISMS); BURKHOLDERIA; CAMPONOTUS; CAMPONOTUS CYLINDRICUS; CLEISTANTHUS; COLOBOPSIS; FORMICIDAE; FUNGI; HEXAPODA; PHYLLANTHACEAE; TRICHODERMA;

EID: 78651499752     PISSN: 10709428     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (85)

1. Arnold, A. E. and F. Lutzoni. 2007. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88: 541-549.
2. -, L. C. Mejia, D. Kyllo, E. I. Rojas, Z. Maynard, N. Robbins, and E. A. Herre. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, USA 100: 15649-15654.
3. Atagana, H. I., R. J. Haynes, and F. M. Wallis. 2002. Batch culture enrichment of indigenous soil microorganisms capable of catabolizing creosote components. Water, Air, and Soil Pollution 141: 233-246.
4. Bailey, B. A., H. Bae, M. D. Strem, D. P. Roberts, S. E. Thomas, J. Crozier, G. J. Samuels, I-Y. Choi, and K. A. Holmes. 2006. Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224: 1449-1464.
5. Birch, A. J. and F. W. Donovan. 1953. Studies in relation to biosynthesis: I. Some possible routes to derivates of orcinol and phloroglucinol. Australian Journal of Chemistry 6: 360-368.
6. Bot, A. N. M., C. R. Currie, A. G. Hart, and J. J. Boomsma. 2001a. Waste management in leafcutting ants. Ethology Ecology and Evolution 13: 225-237.
7. -, D. Ortius-Lechner, K. Finster, R. Maile, and J. J. Boomsma. 2002. Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants. Insectes Sociaux 49: 363-370.
8. -, S. A. Rehner, and J. J. Boomsma. 2001b. Partial incompatibility between ant and symbiotic fungi in two sympatric species of Acromyrmex leafcutting ants. Evolution 55: 1980-1991.
9. Brazier, C. M. 1971. Induction of sexual reproduction in single A isolates of Phytophthora species by Trichoderma viride. Nature New Biology 231: 283.
10. Bruce, A. and T. H. Highly. 1991. Control of growth of wood decay basidiomycetes by Trichoderma spp. and other potentially antagonistic fungi. Forest Products Journal 41: 63-67.
11. -, R. E. Wheatley, S. N. Humphris, C. A. Hackett, and M. E. J. Florence. 2000. Production of volatile organic compounds by Trichoderma in media containing different amino acids and their effect on selected wood decay fungi. Holzforschung 54: 481-486.
12. 2-fixing rhizospheric and endophytic species. International Journal of Systematic and Evolutionary Microbiology 54: 1165-1172.
13. -, J. Onofre-Lemus, P. Estrada-de los Santos, and L. Martínez- Aguilar. 2007. The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Applied and Environmental Microbiology 73: 5308-5319.
14. Carroll, G. 1988. Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69: 2-9.
15. Coenye, T. and P. Vandamme. 2003. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environmental Microbiology 5: 719-729.
16. Cole, L. K., M. S. Blum, and R. W. Roncadori.. Antifungal properties of the insect alarm pheromones, citral, 2-heptanone, and 4-methyl-3-heptanone. Mycologia, 67: 701-708.
17. Compant, S., B. Duffy, J. Nowak, C. Clément, and E. A. Barka. 2005a. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Applied Environmental Microbiology 71: 4951-4959.
18. -, B. Reiter, A. Sessitsch, J. Nowak, C. Clément, and E. A. Barka. 2005b. Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Applied and Environmental Microbiology 71: 1685-1693.
19. Cook, S. C. 2008. Functional and Nutritional Biology of Exudaie-Feeding Ants. Ph.D Thesis, University of Utah Press.
20. Currie, C. R. 2001. Prevalence and impact of a virulent parasite on a tripartite mutualism. Oecologia 128: 99-106.
21. -and A. E. Stuart. 2001. Weeding and grooming of pathogens in agriculture by ants. Proceedings of the Royal Society of London, Series B 268:1033-1039.
22. -, A. N. M. Bot, and J. J. Boomsma. 2003a. Experimental evidence of a tripartite mutualism: bacteria protect ant fungal gardens from specialized parasites. Oikos 101: 91-102.
23. -, A. N. M. Bot, and J. J. Boomsma. 2003b. Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites. Oikos 101: 91-102.
24. -, U. G. Mueller, and D. Malloch. 1999a. The agricultural pathology of ant fungus gardens. Proceedings of the National Academy of Sciences, USA 96: 7998-8002.
25. -, J. A. Scott, R. C. Summerbell, and D. Malloch. 1999b. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: 701-704.
26. -, B. Wong, A. E. Stuart, T. R. Schultz, S. A. Rehner, U. G. Mueller, G. H. Sung, J. W. Spatafora, and N. A. Straus. 2003. Ancient tripartite co-evolution in the attine ant-microbe symbiosis. Science 299: 386-388.
27. Davidson, D. W. 2005. Ecological stoichiometry of ants in a New World rain forest. Oecologia 142: 221-231.
28. -, S. C. Cook, and R. R. Snelling. 2004. Liquidfeeding performances of ants (Formicidae): ecological and evolutionary implications. Oecologia 139: 255-266.
29. -and D. McKey. 1993. The evolutionary ecology of symbiotic ant-plant relationships. Journal of Hymenoptera Research 2: 13-83.
30. -, J-P. Lessard, C. R. Bernau, and S. C. Cook. 2007. The tropical ant mosaic in a primary Bornean rain forest. Biotropka 39: 468-475.
31. do Nascimento, R. R., E. Schoeters, E. D. Morgan, J. Billen, and D. J. Stradling. 1996. Chemistry of metapleural gland secretions of three attine ants, Atta sexdens rubropilosa, Atta cephalotes, and Acromyrmex octospinosus (Hymenoptera: Formicidae). Journal of Chemical Ecology 22: 987-1000.
32. Emery, C. 1925. Hymenoptera fam. Formicidae, subfam. Formicinae (No. 183). In: P. Wytsman, ed. Genera lnsectorum, Louis Desmet-Verteneuil, Brussels, 302 pp.
33. Fernández-Marín, H., J. K. Zimmerman, S. A. Rehner, and W. T. Wcislo. 2006. Active use of the metapleural glands by ants in controlling fungal infection. Proceedings of the Royal Society of London, Series B 273: 1689-1695.
34. Fog, K. 1988. The effect of added nitrogen on the rate of decomposition of organic matter. Biological Reviews 63: 433-462.
35. GeneCodes. 2005. Sequencher 4.5 for Windows. GeneCodes Corporation, Ann Arbor, MI
36. Gerardo, N. M. and E. J. Caldera. 2007. Labile associations between fungus-growing ant cultivare and their garden pathogens. The ISME Journal 1: 373-384.
37. -, U. G. Mueller, and C. R. Currie. 2006. Complex host-pathogen coevolution in the Apterostigma fungus-growing ant-microbe symbiosis. Evolutionary Biology 6: 88-97.
38. Gilbert, G. S. and C. O. Webb. 2007. Phylogenetic signal in plant pathogen-host range. Proceedings of the National Academy of Sciences 104: 4979-4983.
39. Gomes De Siqueira, C., M. Bacci, Jr., F. C. Pagnocca, O. Correa Bueno, and M. J. A. Hebling. 1998. Metabolism of plant polysaccharides by Leucoagaricus gongylophorus, the symbiotic fungus of the leaf-cutting ant Atta sexdens L. Applied Environmental Microbiology 64: 4820-4822.
40. Hamilton, W. D. 1972. Altruism and related phenomena, mainly in social insects. Annual Review of Ecology and Systematics 3:193-232.
41. Hansen, L. D., W. J. Spangenberg, and M. M. Gaver. 1999. The infrabuccal chamber of Camponotus modoc (Hymenoptera: Formicidae): ingestion, digestion, and survey of bacteria. In: W. H. Robinson, F. Rettich, and G. W. Rambo, eds. Proceedings of the 3rd International Conference on Pests, pp. 211-219.
42. Harman, G. E., C. H. Howell, A. Viterbo, I. Chet, and M. Lorito. 2004. Trichoderma species - opportunistic, avirulent plant symbionts. Nature Reviews 2: 43-56.
43. - and C. P. Kubicek. 1998. Trichoderma and Gliocladium, Vol 2, Enzymes, Biological Control and Commercial Applications. Taylor and Francis, London. 393 pp.
44. Hart, A. G. and F. L. W. Ratnieks. 2001. Task partitioning, division of labour and nest compartmentalisation collectively isolate hazardous waste in the leaf cutting ant Atta cephalotes. Behavioral Ecology and Sociobiology 49: 387-392.
45. Hölldobler, B. and H. Engel-Siegel. 1984. On the metapleural gland of ants. Psyche 91: 201-224.
46. - and E. O. Wilson. 1990. The Ants. Belknap Press, Cambridge, MA. 732 pp.
47. Howell, C. R. 2003. Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Disease 87: 4-10.
48. Hughes, W. O. H., J. Eilenberg, and J. J. Boomsma. 2002. Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proceedings of the Royal Society, Series B 269: 1811-1819.
49. Humar, M., M. Petrič, and F. Pohleven. 2001. Changes of the pH value of impregnated wood during exposure to wood-rotting fungi. Holz als Roh-und Werkstoff 59: 288-293.
50. Jones, T. H., S. R. Brunner, A. Edwards, D. W. Davidson, and R. R. Snelling. 2005. 6-alkylsalicylic acids from Crematogaster ci. difformis. Journal of Chemical Ecology 31: 407-417.
51. -, D. A. Clark, A. Edwards, D. W. Davidson, T. F. Spande, and R. R. Snelling. 2004. The chemistry of exploding ants, Camponotus spp. (cylindricus complex). Journal of Chemical Ecology 30: 1479-1492.
52. Kaltenpoth, M. 2007. Life within insect antennae: symbiotic bacteria protect wasp larvae against fungal infestation. Comparative Biochemistry and Physiology 146: S66-67.
53. Karetnikova, E. A. and A. D. Zhirkova. 2005. Degradation of phenols formed during lignin pyrolysis by microfungi of genera Trichoderma and Penicillium. Biology Bulletin 32: 445-449.
54. Kopper, B. J., B. L. Illman, P. J. Kersten, K. D. Klepzig, and K. F. Raffa. 2005. Effects of diterpene acids on components of a conifer bark beetle-fungal interaction: tolerance by Ips pini and sensitivity by its associate Ophiostoma ips. Environmental Entomology 34: 486-493.
55. Kredics, L., Z. Antal, L. Manczinger, A. Szekeres, F. Kevei, and E. Nagy. 2003. Influence of environmental parameters on Trichoderma strains with biocontrol potential. Food Technology and Biotechnology 41: 37-42.
56. Kubicek, C. P. and G. E. Harman. 1998. Trichoderma and Gliocladium. Vol. 1. Basic Biology, Taxonomy and Genetics. Taylor and Francis, London. 278 pp.
57. Little, A. E. and C. R. Currie. 2007. Symbiotic complexity: discovery of a fifth symbiont in the attine ant-microbe symbiosis. Biology Letters 3: 501-504.
58. - and C. R. Currie. 2008. Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants. Ecology 89: 1216-1222.
59. -, T. Murakami, U. G. Mueller, and C. R. Currie. 2006. Defending against parasites: fungus-growing ants combine specialized behaviours and microbial symbionts to protect their fungus gardens. Biology Letters 2: 12-16.
60. Mackintosh, J. A., J. E. Trimble, M. K. Jones, P. H. Karuso, A. J. Beattie, and D. A. Veal. 1995. Antimicrobial mode of action of secretions from the metapleural gland of Myrmecia gulosa (Australian bull ants). Canadian Journal of Microbiology 41: 136-144.
61. Martínez-Aguilar, L., R. Díaz, J. J. Peña-Cabriales, P. Estrada-de los Santos, M. F. Dunn, and J. Caballero-Mellado. 2008. Multichromosomal genome structure and confirmation of diazotrophy in novel plant-associated Burkholderia species. Applied and Environmental Microbiology 74: 4574-4579.
62. Maschwitz, U. 1974. Vergleichende Untersuchungen zur Funktion der Ameisenmetathorakaldrüse. Oecologia 16: 303-310.
63. -, K. Koob, and H. Schildknecht. 1970. Ein Beitrag zur Funktion der Metathoracaldrüse der Ameisen. Journal of Insect Physilogy 16: 387-404.
64. Mueller, U. G., N. M. Gerardo, D. K. Aanen, D. L. Six, and T. R. Schultz. 2005. The evolution of agriculture in insects. Annual Review of Ecology and Systematics 36: 563-569.
65. Ortius-Lechner, D., R. Maile, E. D. Morgan, and J. J. Boomsma. 2000. Metapleural gland secretion of the leaf-cutter ant Acromyrmex. Journal of Chemical Ecology 26: 1667-1683.
66. Poulsen, M., A. N. M. Bot, C. R. Currie, and J. J. Boomsma. 2002. Mutualistic bacteria and a possible trade-off between alternative defence mechanisms in Acromyrmex leafcutting ants. Insectes Sociaux 49: 15-19.
67. -, A. N. M. Bot, C. R. Currie, M. G. Nielsen, and J. J. Boomsma. 2003. Within colony transmission and the cost of a mutualistic bacterium in the leafcutting ant Acromyrmex octospinosis. Functional Ecology 17: 260-269.
68. -, M. Cafaro, J. J. Boomsma, and C. R. Currie. 2005. Specificity of the mutualistic association between actinomycete bacteria and two sympatric species of Acromyrmex leaf-cutting ants. Molecular Ecology 14: 3597-3604.
69. Redman, R. S., D. D. Dunigan, and R. J. Rodriguez. 2001. Fungal symbiosis: from mutualism to parasitism, who controls the outcome, host or invader? New Phytologist 151: 705-716.
70. Reis, V. M., P. Estrada-de los Santos, S. TenorioSalgado, J. Vogel, M. Stoffels, S. Guyon, P. Mavingui, V. L. D. Baldani, M. Schmid, J. I. Baldani, J. Balandreau, A. Hartmann, and J. Caballero-Mellado. 2004. Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. International Journal of Systematic and Evolutionary Microbiology 54: 2155-2162.
71. Rodrigues, A., M. Bacci Jr., U. G. Mueller, A. Ortiz, and F. C. Pagnocca. 2008. Microfungal "weeds" in the leafcutter ant symbiosis. Microbial Ecology 56: 604-614.
72. Rogerson, C. T. and S. L. Stephenson. 1993. Myxomyceticolous fungi. Mycologia 85: 456-469.
73. Sánchez-Peña, S. R. 2005. New view on origin of attine ant-fungus mutualism: exploitation of a preexisisting insect-fungus symbiosis (Hymenoptera: Formicidae). Annals of the Entomological Society of America 98: 151-164.
74. Santos, A. V., R. J. Dillon, V. M. Dillon, S. E. Reynolds, and R. I. Samuels. 2004. Occurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiology Letters 239:319-323.
75. SAS Institute. 2001. JMP Version 4.0.4. SAS Institute, Carey, NC
76. Schiøtt, M., H. H. De Fine Licht, L. Lange, and J. J. Boomsma. 2008. Towards a molecular understanding of symbiont function: identification of a fungal gene for the degradation of xylan in the fungus gardens of leaf-cutting ants. BMC Microbiology 8: 40.
77. Schulz. B., A. K. Rommert, U. Dammann, H. J. Aust, and D. Strack. 1999. The endophyte-host interaction: a balanced antagonism? Mycological Research 103: 1275-1283.
78. Shields, M. S., M. J. Reagin, R. R. Gerger, R. Campbell, and C. Somerville. 1995. TOM, a new aromatic degradative plasmid from Burkholderia (Pseudomonas) cepacia G4. Applied Environmental Microbiology 61: 1352-1356.
79. Shigo, A. L. 1989. A New Tree Biology, Ed. 2. Shigo and Trees, Associates, Durham, NH. 618 pp.
80. Shykoff, J. A. and P. Schmid-Hempel. 1991. Parasites and the advantage of genetic variability within social insect colonies. Proceedings of the Royal Society of London B 243: 55-58.
81. Van Borm, S., A. Buschinger, J. J. Boomsma, and J. Billen. 2002. Tetraponera ants have gut-symbionts related to nitrogen-fixing symbionts. Proceedings of the Royal Society of London B 269: 2023-2027.
82. van Loon, L. C., P. A. H. M. Bakker, and C. M. J. Pieterse. 1998. Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology 36: 453-483.
83. Wang, Z., P. R. Johnston, Z. L. Yang, and J. P. Townsend. 2009. Evolution of reproductive morphology in leaf endophytes. PLoS ONE 4: e4246.
84. Wurdack, K. J., P. Hoffmann, R. Samuel, A. De Bruijn, M. van der Bank, and M. W. Chase. 2004. Molecular phylogenetic analysis of Phyllanthaceae (Phyllanthoideae pro parte, Euphorbiaceae sensus lato) using plastid RBCL DNA sequences. American Journal of Botany 91: 1882-1900.
85. Zhang, M. M., M. Poulsen, and C. R. Currie. 2007. Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants. ISME Journal 1: 313-320.