Advertisement

Insectes Sociaux

, Volume 59, Issue 4, pp 487–498 | Cite as

Ventilation of the giant nests of Atta leaf-cutting ants: does underground circulating air enter the fungus chambers?

  • M. BollazziEmail author
  • L. C. Forti
  • F. Roces
Research Article

Abstract

Nest ventilation should be particularly relevant for the huge colonies of leaf-cutting ants, genus Atta. Considerable amounts of O2 are consumed and CO2 produced by both the fungus gardens and the ants inside nest chambers, which are located at deep soil layers characterized by high CO2 and low O2 concentrations. In this work, passive nest ventilation was investigated in field Atta capiguara and Atta laevigata nests, first, by evaluating air movements through the nest using propane as tracer gas as well as the CO2 and O2 concentrations of the circulating air, and second, by exposing the internal nest morphology with the use of cement casts and excavations. Results showed that even though outflow of CO2-rich air and inflow of O2-rich air occurred at high-placed and low-placed openings, respectively, supporting a wind-induced interpretation of air movements through the nest, circulating air was never detected inside fungus chambers. The CO2 and O2 levels inside the fungus chambers increased and decreased with increasing soil depth, respectively, and were in the range observed in the soil phase. Based on the underground nest architecture, it is concluded that although the external shape of the nest induces underground air circulation, the inflowing air is unable to directly reach the fungus chambers. It is argued that colony respiration completely depends on diffusive flows between the chamber air and the adjacent nest and soil atmospheres. Circulating air, although not directly renewing the air inside the nest chambers, may contribute to colony respiration by increasing the capacity of the nest and soil airs to act as an O2-source and a CO2-sink, because of the decrease in the CO2 and the increase in the O2 levels in the underground air phase. Possible adaptations of both ants and fungus to the high CO2 and low O2 concentrations usually found in soils are discussed.

Keywords

Ants Atta Nest Ventilation Respiration Diffusion 

Notes

Acknowledgments

We thank Christoph Kleineidam (Univ. Konstanz) for comments on a previous draft. Thanks are due to Angel Vidal (Univ. Buenos Aires) for developing and constructing the propane-datalogger, to Scott Turner (SUNY-ESF, Syracuse) for advice on propane sensors, to Ana Paula P. Andrade for the excavation of the large A. capiguara nest used to illustrate the general nest morphology in this species, to Sinara Moreira for the excavation of small A. laevigata nests, and to Nelson Carneiro, Antonio Marcos de Lima and Donizete de Almeida for much help during nest excavations. This study was performed in the framework of the co-operation agreement between the UNESP-Botucatu and the University of Würzburg (Ref. 910-2007). Financial support was provided by funds from the German Research Foundation (DFG, Grant SFB 554/TP E1), the São Paulo State Research Foundation FAPESP (2010/00204-7), and the Brazilian National Research Council CNPq (4726712008-1).

References

  1. Amante E. 1964. Nota prévia sôbre a estrutura do niho de uma nova formiga saúva (Atta sp.) (Hymenoptera, Formicidae). O Biológico 30: 96-97Google Scholar
  2. Amante E. 1967. A formiga saúva Atta capiguara, praga das pastagens. O Biológico 33: 113-120Google Scholar
  3. Andrade A.P.P., Forti L.C., Roces F., Camargo R. and Verza S.S. 2005. Arquitetura interna do ninho de Atta capiguara Gonçalves 1944 (Hymenoptera: Formicidae). In: XVII Simpósio de Mirmecologia, Campo Grande, Brazil. pp 490-493Google Scholar
  4. Bollazzi M. and Roces F. 2002. Thermal preference for fungus culturing and brood location by workers of the thatching grass-cutting ant Acromyrmex heyeri. Insect. Soc. 49: 153-157Google Scholar
  5. Cherrett J.M. 1986. The biology, pest status and control of leaf-cutting ants. Agric. Zool. Rev. 1: 1-27Google Scholar
  6. Cosarinsky M.I. and Roces F. 2012. The construction of turrets for nest ventilation in the grass-cutting ant Atta vollenweideri: import and assembly of building materials. J. Insect Behav. 25: 222-241Google Scholar
  7. Currie J.A. 1984. Gas diffusion through soil crumbs: the effects of compaction and wetting. J Soil Sci. 35: 1-10Google Scholar
  8. Forti L.C. 1985. Ecologia da atividade forrageira da saúva, Atta capiguara Gonçalves, 1944 (Hymenoptera: Formicidae), e seu impacto em pastagem. Escola Superior de Agricultura Luiz de Queiroz-USP. Piracicaba, Brazil. Thesis.Google Scholar
  9. Gonçalves C.R. 1944. Descrição de uma nova saúva brasileira (Hym., Form.). Rev. Brasil. Biol. 4: 233-238Google Scholar
  10. Han B.Z. and Nout R.M.J. 2000. Effects of temperature, water activity and gas atmosphere on mycelial growth of tempe fungi Rhizopus microsporus var. microsporus and R-microsporus var. oligosporus. World J. Microbiol. Biotechnol. 16: 853-858Google Scholar
  11. Hansell M. 2005. Animal Architecture. Oxford University Press, OxfordGoogle Scholar
  12. Hebling M.J.A., Penteado C.H.S. and Mendes E.G. 1992. Respiratory regulation in workers of the leaf-cutting ant Atta sexdens rubropilosa Forel, 1908. Comp. Biochem. Physiol. 101A: 319-322Google Scholar
  13. Hillel D. 1998. Environmental Soil Physics. Academic Press, LondonGoogle Scholar
  14. Jacoby M. 1935. Erforschung der Struktur des Atta-Nestes mit Hilfe des Cementausguss-Verfahrens. Rev. Entomol. 5: 420-424Google Scholar
  15. Jacoby M. 1939. A renovação do oxigênio no ninho da Atta sexdens L. Bol. Min. Agr. Rio de Janeiro 28: 1-7Google Scholar
  16. Jonkman J.C.M. 1980. The external and internal structure and growth of nests of the leaf-cutting ant Atta vollenweideri Forel, 1893 (Hym.: Formicidae). Part II. The internal nest structure and growth. Z. ang. Entomol. 89: 217-246Google Scholar
  17. Kennard C.P. 1965. Control of leaf-cutting ants (Atta sp.) by fogging. Exp Agric. 1: 237-240Google Scholar
  18. Kleineidam C., Ernst R. and Roces F. 2001. Wind induced ventilation of the giant nests of the leaf-cutting ant Atta vollenweideri. Naturwissenschaften 88: 301-305Google Scholar
  19. Kleineidam C. and Roces F. 2000. Carbon dioxide concentrations and nest ventilation in nests of the leaf-cutting ant Atta vollenweideri. Insect. Soc. 47: 241-248Google Scholar
  20. Kleineidam C. and Tautz J. 1996. Perception of carbon dioxide and other “air-condition” parameters in the leaf cutting ant Atta cephalotes. Naturwissenschaften 83: 566-568Google Scholar
  21. Lapointe S.L., Serrano M.S. and Jones P.G. 1998. Microgeographic and vertical distribution of Acromyrmex landolti (Hymenoptera: Formicidae) nests in a neotropical savanna. Environ. Entomol. 27: 636-641Google Scholar
  22. Mariconi F.A.M. 1970. As Saúvas. Agronômica Ceres, São PauloGoogle Scholar
  23. Mariconi F.A.M., Zamith A.P.L. and Paiva Castro U. 1961. Contribuição para o conhecimento da saúva parda Atta capiguara Gonçalves, 1944. Anais da Escola Superior de Agricultura ‘Liuz de Queiroz’, Piracicaba. 18: 301-312Google Scholar
  24. Mitchell D.J. and Zentmyer G.A. 1971. Effects of oxygen and carbon dioxide tensions on growth of several species of Phytophthora. Phytopathology 61: 787-791Google Scholar
  25. Moreira A.A., Forti L.C., Boaretto M.A.C., Andrade A.P.P., Lopes J.F.S. and Ramos V.M. 2004a. External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae) nests. J. Appl. Ent. 128: 204-211Google Scholar
  26. Moreira A.A., Forti L.C., de Andrade A.P.P. and Castellani Boaretto M.A. 2004b. Architecture of nests of the Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud. Neotrop. Fauna Environ. 39: 109-116Google Scholar
  27. 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: 169-197Google Scholar
  28. Nicolas G. and Sillans D. 1989. Immediate and latent effects of carbon dioxide on insects. Annu. Rev. Entomol. 34: 97-116Google Scholar
  29. Nielsen M.G., Christian K. and Birkmose D. 2003. Carbon dioxide concentrations in the nests of the mud-dwelling mangrove ant Polyrhachis sokolova Forel (Hymenoptera : Formicidae). Aust. J. Entomol. 42: 357-362Google Scholar
  30. Nielsen M.G., Christian K., Henriksen P.G. and Birkmose D. 2006. Respiration by mangrove ants Camponotus anderseni during nest submersion associated with tidal inundation in Northern Australia. Physiol. Entomol. 31: 120-126Google Scholar
  31. Nielsen M.G., Christian K. and Malte H. 2009. Hypoxic conditions and oxygen supply in nests of the mangrove ant, Camponotus anderseni, during and after inundation. Insect. Soc. 56: 35-39Google Scholar
  32. Nielsen M.G. and Christian K.A. 2007. The mangrove ant, Camponotus anderseni, switches to anaerobic respiration in response to elevated CO2 levels. J. Insect Physiol. 53: 505-508Google Scholar
  33. Reu de J.C., Rombouts F.M., Griffiths A.M. and Nout M.J.R. 1995. Effect of oxygen and carbon dioxide on germination and growth of Rhizopus oligosporus on model media and soya beans. Appl. Microbiol. Biotechnol. 43: 908-913Google Scholar
  34. Roces F. and Kleineidam C. 2000. Humidity preference for fungus culturing by workers of the leaf-cutting ant Atta sexdens rubropilosa. Insect. Soc. 47: 348-350Google Scholar
  35. Sparringa R.A., Kendall M., Westby A. and Owens J.D. 2002. Effects of temperature, pH, water activity and CO2 concentration on growth of Rhizopus oligosporus NRRL 2710. J. App. Microbiol. 92: 329-337Google Scholar
  36. Stahel G. and Geijskes D.C. 1940. Observations about temperature and moisture in Atta-nests. Rev. Entomol. 11: 766-775Google Scholar
  37. Turner J.S. 2001. On the mound of Macrotermes michaelseni as an organ of respiratory gas exchange. Physiol. Biochem. Zool. 74: 798-822Google Scholar
  38. Vogel S. 1978. Organisms that capture currents. Sci. Am. 239: 108-117Google Scholar
  39. Vogel S. and Bretz W.L. 1972. Interfacial organisms: passive ventilation in the velocity gradients near surfaces. Science 175: 210-211Google Scholar
  40. Weber N.A. 1972. Gardening Ants - The Attines. The American Philosophical Society, PhiladelphiaGoogle Scholar
  41. Weidenmüller A. 2004. The control of nest climate in bumblebee (Bombus terristris) colonies: interindividual variability and self reinforcement in fanning response. Behav. Ecol. 15: 120-128Google Scholar
  42. Wells J.M. and Uota M. 1970. Germination and growth of 5 fungi in low-oxygen and high-carbon dioxide atmospheres. Phytopathology 60: 50-53Google Scholar
  43. Withers P.C. 1978. Models of diffusion-mediated gas exchange in animal burrows. Am. Nat. 112: 1101-1112Google Scholar
  44. Wyatt Hoback W. and Stanley D.W. 2001. Insects in hypoxia. J. Insect Physiol. 47: 533-542Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2012

Authors and Affiliations

  1. 1.Unidad de Entomología, Departamento de Protección Vegetal, Facultad de AgronomíaUniversidad de la RepublicaMontevideoUruguay
  2. 2.Laboratorio de Insetos Sociais-PragaState University of São Paulo, Rua José Barbosa de Barros 1780BotucatuBrazil
  3. 3.Department of Behavioural Physiology and Sociobiology, BiocenterUniversity of WürzburgWürzburgGermany

Personalised recommendations