Rapid shifts in Atta cephalotes fungus-garden enzyme activity after a change in fungal substrate (Attini, Formicidae)

Insectes Sociaux

Volumn 58, Issue 2, 2011, Pages 145-151

  Kooij, P W ^a,b   Schiott M ^a   Boomsma, J J ^a   de Fine Licht, H H ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

AZCL assay; Enzyme activity; Leucocoprinus gongylophorus; Mutualism; Plant degradation

Indexed keywords

ANT; CELLULOSE; DEGRADATION; DIET; ENZYME ACTIVITY; FUNGUS; LEAF; MUTUALISM; PROTEIN; STARCH; SUBSTRATE; SYMBIONT;

ATTA; ATTA CEPHALOTES; ATTINI; BASIDIOMYCOTA; FORMICIDAE; FUNGI; LEUCOCOPRINUS; RUBUS;

EID: 79952695901     PISSN: 00201812     EISSN: 14209098     Source Type: Journal    
DOI: 10.1007/s00040-010-0127-9     Document Type: Article

References (38)

1. Bass M. and Cherrett J. M. 1994. The role of leaf-cutting ant workers (Hymenoptera, Formicidae) in fungus garden maintenance. Ecol. Entomol. 19: 215-220.
2. Bass M. and Cherrett J. M. 1995. Fungal hyphae as a source of nutrients for the leaf-cutting ant Atta sexdens. Physiol. Entomol. 20: 1-6.
3. Boyd N. D. and Martin M. M. 1975. Faecal proteinases of the fungus-growing ant, Atta texana: their fungal origin and ecological significance. J. Insect Physiol. 21: 1815-1820.
4. rdEd (Champagne E. T., Ed). American Association of Cereal Chemists Inc, St. Paul, Minnesota. pp 77-107.
5. Chapin III F. S. and Shaver G. R. 1988. Differences in carbon and nutrient fractions among Arctic growth forms. Oecologia 77: 506-514.
6. Currie C. R., Scott J. A., Summerbell R. C. and Malloch D. 1999. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: 701-704.
7. De Fine Licht H. H., Schiøtt M., Mueller U. G. and Boomsma J. J. 2010. Evolutionary transitions in enzyme activity of ant fungus gardens. Evolution 64: 2055-2069.
8. De Fine Licht H. H. and Boomsma J. J. 2010. Forage collection, substrate preparation and diet composition in fungus-growing ants. Ecol. Entomol. 35: 259-269.
9. Erthal Jr. M., Silva C. P. and Samuels R. I. 2004. Digestive enzymes of leaf-cutting ants, Acromyrmex subterraneus (Hymenoptera: Formicidae: Attini): distribution in the gut of adult workers and partial characterization. J. Insect Physiol. 50: 881-891
10. Erthal Jr. M., Silva C. P. and Samuels R. I. 2007. Digestive enzymes in larvae of the leaf cutting ant, Acromyrmex subterraneus (Hymenoptera: Formicidae: Attini). J. Insect Physiol. 53: 1101-1111.
11. Erthal Jr. M., Silva C. P., Cooper R. M. and Samuels R. I. 2009. Hydrolytic enzymes of leaf-cutting ant fungi. Comp. Biochem. Phys. B 152: 54-59.
12. D'Ettorre P., Mora P., Dibangou V., Rouland C. and Errard C. 2002. The role of the symbiotic fungus in the digestive metabolism of two species of fungus-growing ants. J. Comp. Physiol. B 172: 169-176.
13. Gomes de Siqueira C., Bacci Jr. M., Pagnocca F. C., Bueno O. C. and Hebling M. J. A. 1998. Metabolism of plant polysaccharides by Leucoagaricus gongylophorus, the symbiotic fungus of the leaf-cutting ant Atta sexdens L. Appl. Environ. Microb. 64: 4820-4822.
14. Hart A. G., Bot A. N. M. and Brown M. J. F. 2002. A colony-level response to disease control in a leaf-cutting ant. Naturwissenschaften 89: 275-277.
15. Hasper A. A., Trindade L. M., van Der Veen D., van Ooyen A. J. J. and De Graaff L. H. 2004. Functional analysis of the transcriptal activator XlnR from Aspergillus niger. Microbiol-SGM150: 1367-1375.
16. Johnson R. A. 2001. Biogeography and community structure of North American seed-harvester ants. Annu. Rev. Entomol. 46: 1-29.
17. Leal, I. R. and Oliveira, P. S., 2000. Foraging ecology of attine ants in a neotropical savanna: seasonal use of fungal substrate in the cerrado vegetation of Brazil. Insect. Soc. 47: 376-382.
18. Littledyke, M. and Cherrett, J. M., 1976. Direct ingestion of plant sap from cut leaves by the leaf-cutting ants Atta cephalotes (L.) and Acromyrmex octospinosus (Reich) (Formicidae: Attini). B. Entomol. Res. 66: 205.
19. Mueller U. G., Schultz T. R., Currie C. R., Adams R. M. M. and Malloch D. 2001. The origin of the attine ant-fungus mutualism. Q. Rev. Biol. 76: 169-197.
20. Mueller U. G., Gerardo N. M., Aanen D. K., Six D. L. and Schultz T. R. 2005. The evolution of agriculture in insects. Annu. Rev. Ecol. Evol. S36: 563-595.
21. Pedersen M., Hollensted M., Lange L. and Andersen B. 2009. Screening for cellulose and hemicellulose degrading enzymes from the fungal genus Ulocladium. Int. Biodeter. Biodegr. 63: 484-489.
22. Pinto-Tomas A. A., Anderson M. A., Suen G., Stevenson D. M., Chu F. S., Cleland W. W., Weimer P. J. and Currie C. R. 2009. Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science326: 1120.
23. Poulsen M. and Boomsma J. J. 2005. Mutualistic fungi control crop diversity in fungus-growing ants. Science307: 741-744.
24. Price S. L., Murkami T., Mueller U. G., Schultz T. R. and Currie C. R. 2003. Recent findings in fungus-growing ants: evolution, ecology, and behavior of a complex microbial symbiosis. In: Genes, Behaviors and Evolution of Social Insects (Kikuchi T, Azuma N and Higashi S, Eds). Hokkaido University Press, Sapporo. pp 255-280.
25. Quinlan R. J. and Cherrett J. M. 1977. The role of substrate preparation in the symbiosis between the leaf-cutting ant Acromyrmex octospinosus (Reich) and its food fungus. Ecol. Entomol. 2: 161-170.
26. Quinlan R. J. and Cherrett J. M. 1979. The role of fungus in the diet of the leaf-cutting ant Atta cephalotes (L). Ecol. Entomol. 4: 151-160.
27. Richard F. J., Mora P., Errard C. and Rouland C. 2005. Digestive capacities of leaf-cutting ants and the contribution of their fungal cultivar to the degradation of plant material. J. Comp. Physiol. B175: 297-303.
28. Rønhede S., Boomsma J. J. and Rosendahl S. 2004. Fungal enzymes transferred by leaf-cutting ants in their fungus gardens. Mycol. Res. 108: 101-106.
29. Schiøtt M., De Fine Licht H. H., Lange L. and Boomsma J. J. 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 Microbiol. 8: 40.
30. Schultz T. R. and Brady S. G. 2008. Major evolutionary transitions in ant agriculture. P. Natl. Acad. Sci-Biol. 105: 5435-5440.
31. Scott J. J., Budsberg K. J., Suen G., Wixon D. L., Balser T. C. and Currie C. R. 2010. Microbial community structure of leaf-cutter ant fungus gardens and refuse dumps. PloS ONE5: e9922.
32. Selvendran R. R. 1984. The plant cell wall as a source of dietary fiber: chemistry and structure. Am. J. Clin. Nutr. 39: 320-337.
33. Silva A., Bacci Jr. M., Pagnocca F. C., Bueno O. C. and Hebling M. J. A. 2006a. Starch metabolism in Leucoagaricus gongylophorus, the symbiotic fungus of leaf-cutting ants. Microbiol. Res. 161: 299-303.
34. Silva A., Bacci M., Pagnocca F. C., Bueno O. C. and Hebling M. J. A. 2006b. Production of polysaccharidases in different carbon sources by Leucoagaricus gongylophorus Moller (Singer), the symbiotic fungus of the leaf-cutting ant Atta sexdens Linnaeus. Curr. Microbiol. 53: 68-71.
35. Valmir Santos A., Dillon R. J., Dillon V. M., Reynolds S. E. and Samuels R. I. 2004. Occurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol. Lett. 239: 319-323.
36. Weber N. A. 1966. Fungus-growing ants. Science153: 587-604.
37. Weber N. A. 1972. Gardening ants, the attines. American Philosophical Society, Philadelphia. 146 pp.
38. Winer B. J., Brown D. R. and Michaels K. M. 1991. Statistical Principles in Experimental Design. McGraw-Hill, New York. 928 pp.