Field colonies of leaf-cutting ants select plant materials containing low abundances of endophytic fungi

Ecosphere

Volumn 4, Issue 5, 2013, Pages

  Coblentz, Kyle E ^a   Van Bael, Sunshine A ^a,b  

^a Tulane University   (United States)

^b SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

Author keywords

Atta colombica; Fungal endophytes; Interactions; Mutualism; Neotropics; Panama; Symbiosis

Indexed keywords

EID: 84900455607     PISSN: None     EISSN: 21508925     Source Type: Journal    
DOI: 10.1890/ES13-00012.1     Document Type: Article

References (47)

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. (Pubitemid 46597060)
2. Arnold, A. E., Z. Maynard, G. S. Gilbert, P. D. Coley, and T. A. Kursar. 2000. Are tropical fungal endophytes hyperdiverse? Ecology Letters 3:267-274. (Pubitemid 30597793)
3. Arnold, A. E., L. C. Mejá, 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. (Pubitemid 38021044)
4. Bacon, C. W., J. K. Porter, J. D. Robbins, and E. S. Luttrell. 1977. Epichloe typhina from toxic tall fescue grasses. Applied and Environmental Microbiology 34:576-581. (Pubitemid 8231324)
5. Bass, M., and J. M. Cherrett. 1994. The role of leafcutting ant workers (Hymenoptera: Formicidae) in fungus garden maintenance. Ecological Entomology 19:215-220. (Pubitemid 2117359)
6. Berish, C. W. 1986. Leaf-cutting ants (Atta cephalotes) select nitrogen rich forage. American Midland Naturalist 115:268-276. (Pubitemid 17250303)
7. Bittleston, L. S., F. Brockman, W. Wcislo, and S. A. Van Bael. 2010. Endophytic fungi reduce leaf-cutting ant damage to seedlings. Biology Letters 7:30-32.
8. Breen, J. P. 1994. Acremonium endophyte interactions with enhanced plant resistance to insects. Annual Review of Entomology 39:401-423.
9. Clay, K. 1988. Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10-16. (Pubitemid 19317504)
10. Coley, P. D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs 53:209-234.
11. Correa, M. M., P. S. D. Silva, R.Wirth, M. Tabarelli, and R. Leal. 2010. How leaf-cutting ants impact forests: drastic nest effects on light environment and plant assemblages. Oecologia 162:103-115.
12. Currie, C. R., J. A. Scott, R. C. Summerbell, and D. Malloch. 1999. Fungus-growing ants use antibioticproducing bacteria to control garden parasites. Nature 398:701-704. (Pubitemid 29197647)
13. Currie, C. R., and A. E. Stuart. 2001. Weeding and grooming of pathogens in agriculture by ants. Proceedings of the Royal Society B 268:1033-1039. (Pubitemid 32500476)
14. Estrada, C., W. T. Wcislo, and S. A. Van Bael. 2013. Symbiotic fungi alter plant chemistry that discourages leaf-cutter ants. New Phytologist doi: 10.1111/ nph.12140
15. Faeth, S. H. 2002. Are endophytic fungi defensive plant mutualists? Oikos 98:25-36. (Pubitemid 34877836)
16. Farji-Brener, A. G. 2001. Why are leaf-cutting ants more common in early secondary forests than in old-growth forests? An evaluation of the palatable forage hypothesis. Oikos 92:169-177. (Pubitemid 32160898)
17. Fernández-Marn, 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 B 273:1689-1695. (Pubitemid 46931057)
18. Herre, E. A., L. C. Mejá, D. A. Kyllo, E. Rojas, Z. Maynard, A. Butler, and S. A. Van Bael. 2007. Ecological implications of anti-pathogen effects of tropical fungal endophytes and mycorrhizae. Ecology 88:550-558. (Pubitemid 46597061)
19. Herz, H., W. Beyschlag, and B. Hölldobler. 2007a. Assessing herbivory rates of leaf-cutting ant (Atta colombica) colonies through short-Term deposition counts. Biotropica 39:476-481. (Pubitemid 47099879)
20. Herz, H., W. Beyschlag, and B. Hölldobler. 2007b. Herbivory rate of leaf-cutting ants in a tropical moist forest in Panama at the population and ecosystem scales. Biotropica 39:482-488. (Pubitemid 47099880)
21. Herz, H., B. Hölldobler, and F. Roces. 2008. Delayed rejection in a leaf-cutting ant after foraging on plants unsuitable for the symbiotic fungus. Behavioral Ecology 19:575-582. (Pubitemid 351847417)
22. Howard, J. J. 1988. Leafcutting ant diet selection: relative influence of leaf chemistry and physical features. Ecology 69:250-260. (Pubitemid 19317408)
23. Hubbell, S. P., D. F. Wiemer, and A. Adejare. 1983. An antifungal terpenoid defends a neotropical tree (Hymenaea) against attack by fungus-growing ants (Atta). Oecologia 60:321-327. (Pubitemid 15275577)
24. Koh, S., and D. S. Hik. 2007. Herbivory mediates grassendophyte relationships. Ecology 98:2752-2757.
25. Mejá, L. C., E. I. Rojas, Z. Maynard, S. Van Bael, A. E. Arnold, P. Hebbar, G. J. Samuels, N. Robbins, and E. A. Herre. 2008. Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biological Contol 46:4-14.
26. 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, Evolution, and Systematics 36:563-595. (Pubitemid 43068871)
27. Mueller, U. G., and B. Wolf-Mueller. 1991. Epiphyll deterrence to the leafcutter ant Atta cephalotes. Oecologia 86:36-39.
28. Nichols-Orians, C. M., and J. C. Schultz. 1989. Leaf toughness affects leaf harvesting by the leaf cutter ant, Atta cephalotes (L.) (Hymenoptera: Formicidae). Biotropica 21:80-83.
29. Prestidge, R. A., and R. T. Gallagher. 1988. Endophyte fungus confers resistance to ryegrass: Argentine stem weevil larval studies. Ecological Entomology 13:429-435. (Pubitemid 19324822)
30. Quinlan, R. J., and J. M. Cherrett. 1977. The role of substrate preparation in the symbiosis between the leaf-cutting ant Acromyrmex octospinosus (Reich) and its food fungus. Ecological Entomology 2:161-170.
31. R Development Core Team. 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
32. Rasband, W. S. 1997-2012. ImageJ. U.S. National Institute of Health, Bethesda, Maryland, USA.
33. 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(3):705-716. (Pubitemid 32812103)
34. Rockwood, L. L. 1976. Plant selection and foraging patterns in two species of leaf-cutting ants (Atta). Ecology 57:48-61.
35. Rowan, D. D., and D. L. Gaynor. 1986. Isolation of feeding deterrents against argentine stem weevil from ryegrass infected with the endophyte Acremonium loliae. Journal of Chemical Ecology 12:647-658.
36. Saikkonen, K., S. H. Faeth, M. Helander, and T. J. Sullivan. 1998. Fungal endophytes: a continuum of interactions with host plants. Annual Review of Ecology and Systematics 29:319-343. (Pubitemid 29033035)
37. Saikkonen, K., M. Helander, S. H. Faeth, F. Schulthess, and D. Wilson. 1999. Endophyte-grass-herbivore interactions: the case of Neotyphodium endophytes in Arizona fescue populations. Oecologia 121:411-420.
38. Systat Software. 2003. Systat v. 11. Systat Software, San Jose, California, USA.
39. Tibbets, T. M., and S. H. Faeth. 1999. Neotyphodium endophytes in grasses: Deterrents or promoters of herbivory by leaf-cutting ants? Oecologia 118:297-305. (Pubitemid 29150693)
40. Van Bael, S. A., C. Estrada, F. Santos, S. Rehner, and W. Wcislo. 2012. Leaf endophyte load and fungal garden development in Atta colombica. BMC Ecology 12:23.
41. Van Bael, S. A., C. Estrada, and W. T. Wcislo. 2011. Fungal-fungal interactions in leaf-cutting ant agriculture. Psyche 2011:617478.
42. Van Bael, S. A., H. Fernández-Marn, M. C. Valencia, E. I. Rojas,W. T. Wcislo, and E. A. Herre. 2009. Two fungal symbioses collide: endophytic fungi are not welcome in leaf-cutting ant gardens. Proceedings of the Royal Society B 276:2419-2426.
43. Wilson, D. 1995a. Endophyte-The evolution of a term, and clarification of its use and definition. Oikos 73:274-276.
44. Wilson, D. 1995b. Fungal endophytes which invade insect galls: Insect pathogens, benign saprophytes, or fungal inquilines? Oecologia 103:255-260. (Pubitemid 26447972)
45. Wilson, D., and G. C. Carroll. 1997. Avoidance of highendophyte space by gall-forming insects. Ecology 78:2153-2163.
46. Wilson, D., and S. H. Faeth. 2001. Do fungal endophytes result in selection for leafminer ovipositional preference? Ecology 82:1097-1111. (Pubitemid 32333456)
47. Wirth, R., W. Beyschlag, R. J. Ryel, and B. Hölldobler. 1997. Annual foraging of the leaf-cutting ant Atta colombica in a semideciduous rain forest in Panama. Journal of Tropical Ecology 13:741-757. (Pubitemid 27447362)