Insectes Sociaux

, Volume 58, Issue 1, pp 65–75 | Cite as

Caste specialization in behavioral defenses against fungus garden parasites in Acromyrmex octospinosus leaf-cutting ants

  • D. Abramowski
  • C. R. Currie
  • M. Poulsen
Research Article


Division of labor and caste specialization plays an important role in many aspects of social insect colony organization, including parasite defense. Within leaf-cutting ant colonies, worker caste specialization permeates colony tasks ranging from foraging, substrate incorporation, brood care, and chemical defenses via glandular secretions and mutualistic bacteria. Leaf-cutting ants rely on protecting a mutualistic fungus they grow for food from microfungi in the genus Escovopsis that parasitizes the ant–fungus relationship. Here, we examine whether Acromyrmex octospinosus leaf-cutter ant castes (minors and majors) display task specialization in two behavioral defenses against Escovopsis: fungus grooming (the removal of Escovopsis spores) and weeding (the removal of large pieces of Escovopsis-infected fungus garden). Using behavioral observations, we show that minors are the primary caste that performs fungus grooming, while weeding is almost exclusively performed by majors. In addition, using a sub-colony infection experimental setup, we show that at the early stages of infection, minors more efficiently remove Escovopsis spores from the fungus garden, thereby restricting Escovopsis spore germination and growth. At later stages of infection, after Escovopsis spore germination, we find that major workers are as efficient as minors in defending the fungus garden, likely due to the increased importance of weeding. Finally, we show, using SEM imaging, that the number of sensory structures is similar between minor and major workers. If these structures are invoked in recognition of the parasites, this finding suggests that both castes are able to sense Escovopsis. Our findings support that leaf-cutter ant behavioral defense tasks against Escovopsis are subject to caste specialization, likely facilitated by worker sizes being optimal for grooming and weeding by minors and majors, respectively, with important consequences for cultivar defense.


Escovopsis Fungus-growing ants Grooming Social immunity Task specialization Weeding Worker caste 



We thank J. Heinz and the BBPIC Laboratory at the University of Wisconsin, Madison, for assistance with SEM imaging, and S. Adams, S. Marsh, G. Suen, and J.M. Thomas for comments on a draft of this manuscript. We acknowledge the Smithsonian Tropical Research Institute for providing logistical help during fieldwork in Panama, and the Autoridad Nacional del Ambiente of the Republic of Panama for facilitating the research and granting collecting permits. This work was supported by the University of Wisconsin-Madison Hilldale Research Grant to DA, The Carlsberg Foundation to MP, and NSF CAREER grant DEB-747002 to CRC.


  1. Bot A.N.M. and Boomsma J.J. 1996. Variable metapleural gland size-allometries in Acromyrmex leafcutter ants (Hymenoptera: Formicidae). J. Kansas Entomol. Soc. 69 (suppl): 375-383Google Scholar
  2. Bot A.N.M., Orthius-Lechner D., Finster K., Maile R. and Boomsma J.J. 2002. Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants. Insect. Soc. 49: 363-370Google Scholar
  3. Bot A.N.M., Rehner S.A. and Boomsma J.J. 2001. Partial incompatibility between ants and symbiotic fungi in two sympatric species of Acromyrmex leaf-cutting ants. Evolution 55: 1980-1991Google Scholar
  4. Beshers S.N. and Fewell J.H. 2001. Models of division of labor in social insects. Annu. Rev. Entomol. 46: 413-440Google Scholar
  5. Breed M., Robinson G. and Page R. 1990. Division of labor during honey bee colony defense. Behav. Ecol. Sociobiol. 27: 395-401Google Scholar
  6. Chapela I.H., Rehner S.A., Schultz T.R. and Mueller U.G. 1994. Science 266: 1691-1694Google Scholar
  7. Chouvenc T., Su N.-Y. and Elliott M.I. 2008. Antifungal activity of the termite alkaloid norharmane against the mycelial growth of Metarhizium anisopliae and Aspergillus nomius. J. Inv. Path. 99: 345-347Google Scholar
  8. Cremer S. and Sixt M. 2009. Analogies in the evolution of individual and social immunity. Phil. Trans. R. Soc. B 364: 129-142Google Scholar
  9. Currie C.R. 2001. Prevalence and impact of a virulent parasite on a tripartite mutualism. Oecologia 128: 99-106Google Scholar
  10. Currie C.R., Bot A.N.M. and Boomsma J.J. 2003. Experimental evidence of a tripartite mutualism: bacteria protect ant fungal gardens from specialized parasites. Oikos 101: 91-102Google Scholar
  11. Currie C.R. and Stuart A.E. 2001. Weeding and grooming of pathogens in agriculture by ants. Proc. R. Soc. B 268: 1033-1039Google Scholar
  12. Currie C.R., Mueller U.G. and Malloch D. 1999a. The agricultural pathology of ant fungus gardens. Proc. Natl. Acad. Sci. USA 96: 7998-8002Google Scholar
  13. Currie C.R., Scott J.A., Summerbell R.C. and Malloch D. 1999b. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: 701-704Google Scholar
  14. Eisner T. and Happ G. 1962. The infrabuccal pocket of a formicine ant: A social filtration device. Psyche 69: 107-116Google Scholar
  15. Feener Jr., D.H. and Moss K.A.G. 1990. Defense against parasites by hitchhikers in leaf-cutting ants: a quantitative assessment. Behav. Ecol. Sociobiol. 26: 17-29Google Scholar
  16. Fernández-Marín H., Zimmerman J.K., Rehner S.A. and Wcislo W.T. 2006. Active use of the metapleural glands by ants in controlling fungal infection. Proc. R. Soc. B 273: 1689-1695Google Scholar
  17. Fernández-Marín H., Zimmerman J.K., Nash D.R., Boomsma J.J. and Wcislo W.T. 2009. Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants. Proc. R. Soc. B 276: 2263-2269Google Scholar
  18. Gerstner A.T., Poulsen M. and Currie C.R. Atta cephalotes and A. sexdens majors recruit minor workers in colony defense against infection by a specialized parasite. Ethol. Ecol. Evol., in pressGoogle Scholar
  19. Hart A.G., Anderson C. and Ratnieks F.L.W. 2002. Task partitioning in leafcutting ants. Acta ethologica 5: 1-11Google Scholar
  20. Hojo M., Morioka M., Matsumoto T. and Miura T. 2005. Identification of soldier caste-specific protein in the frontal gland of nasute termite Nasutitermes takasagoensis (Isoptera: Termitidae). Insect Biochem. Mol. Biol. 35: 347-354Google Scholar
  21. Hölldobler B. and Wilson E. 1990. The Ants. Springer-Verlag, New York City, New York, 732 ppGoogle Scholar
  22. Hölldobler B. and Wilson E.O. 2009. The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies. W.W. Norton and Company, New York London, 522 ppGoogle Scholar
  23. Ivens A.B.F., Nash D.R., Poulsen M. and Boomsma J.J. 2009 Caste-specific symbiont policing by workers of Acromyrmex fungus-growing ants. Behav. Ecol. 20: 378-384Google Scholar
  24. Kelber C., Rössler W., Roces F. and Kleineidam C.J. 2009. The antennal lobes of fungus-growing ants (Attini): neuroanatomical traits and evolutionary trends. Brain Behav. Evol. 73: 273-284Google Scholar
  25. Kuebler L.S., Kelber C. and Kleineidam C.J. 2010. Distinct antennal lobe phenotypes in the leaf-cutting ant (Atta vollenweideri). J. Comp. Neurol. 518: 352-65Google Scholar
  26. Little T.J., Hultmark D. and Read A.F. 2005. Invertebrate immunity and the limits of mechanistic immunology. Nat. Immunol. 6: 651-654Google Scholar
  27. Little A.E.F., Murakami T., Mueller U.G. and Currie C.R. 2006. Defending against parasites: fungus-growing ants combine specialized behaviors and microbial symbionts to protect their fungus gardens. Biol. Lett. 1: 12-16Google Scholar
  28. Poulsen M., Bot A.N.M., Currie C.R. and Boomsma J.J. 2002. Mutualistic bacteria and a possible trade-off between alternative defense mechanisms in Acromyrmex leaf-cutting ants. Insect. Soc. 49: 15-19Google Scholar
  29. Poulsen M., Cafaro M.J., Erhardt D., Gerardo N.M., Little A.E.F., Tebbets B., Klein B. and Currie C.R. 2010. Variation in Pseudo-nocardia antibiotic defense helps govern parasite-induced morbidity in Acromyrmex leaf-cutting ants. Env. Microbiol. Rep. 2: 534-540 Google Scholar
  30. 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: 151-160Google Scholar
  31. Ratnieks F.L.W. and Anderson C. 1999. Task partitioning in insect societies. Insect. Soc. 46: 99-108Google Scholar
  32. Renthal R., Velasquez D., Olmos D., Hampton J. and Wergin W. 2003. Structure and distribution of antennal sensilla of the red imported fire ant. Micron 34: 405-413Google Scholar
  33. Reynolds H.T. and Currie C.R. 2004. Pathogenecity of Escovopsis weberi: The parasite of the attine ant-microbe symbiosis directly consumes the ant-cultivated fungus. Mycologia 96: 955-959Google Scholar
  34. Robinson G. 1992. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37: 637-665Google Scholar
  35. Simone M., Evans J.D. and Spivak M. 2009. Resin collection and social immunity in honey bees Evolution 63: 3016-3022Google Scholar
  36. Spivak M. and Reuter G.S. 2001. Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie 32: 555-565Google Scholar
  37. Ugelvig L.V. and Cremer S. 2007. Social prophylaxis: group inter-action promotes collective immunity in ant colonies. Curr. Biol. 17: 1967-1971Google Scholar
  38. Walker T.N. and Hughes W.O.H. 2009. Adaptive social immunity in leaf-cutting ants. Biol. Lett. 5: 446-448Google Scholar
  39. Weber N. 1972. Gardening Ants: the Attines. The American Philo-sophical Society, Philadelphia, Pennsylvania. 146pGoogle Scholar
  40. Wetterer J.K. 1999. The ecology and evolution of worker size-distri-bution in leaf-cutting ants (Hymenoptera: Formicidae). Socio-biology 34: 119-144Google Scholar
  41. Wilson E.O. 1983. Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). IV. Colony ontogeny of A. cephalotes. Behav. Ecol. Sociobiol. 14: 55-60Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2010

Authors and Affiliations

  1. 1.Department of BacteriologyUniversity of Wisconsin, MadisonMadisonUSA

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