Advertisement

The Science of Nature

, 106:3 | Cite as

Waste deposition in leaf-cutting ants is guided by olfactory cues from waste

  • Daniela RömerEmail author
  • Flavio Roces
Original Paper

Abstract

Social insects often use olfactory cues from their environment to coordinate colony tasks. We investigated whether leaf-cutting ants use volatiles as cues to guide the deposition of their copious amounts of colony refuse. In the laboratory, we quantified the relocation of a small pile of colony waste by workers of Atta laevigata towards volatiles offered at each side of the pile as a binary choice, consisting of either waste volatiles, fungus volatiles, or no volatiles. Fungus volatiles alone did not evoke relocation of waste. Waste volatiles alone, by contrast, led to a strong relocation of waste particles towards them. When fungus and waste volatiles were tested against each other, waste particles were also relocated towards waste volatiles, and in a high percentage of assays completely moved away from the source of fungus volatiles as compared to the previous series. We suggest that deposition and accumulation of large amounts of refuse in single external heaps or a few huge underground waste chambers of Atta nests is due to both olfactory preferences and stigmergic responses towards waste volatiles by waste-carrying workers.

Keywords

Volatiles Waste chamber Stigmergy Nest hygiene Orientation Atta laevigata 

Notes

Acknowledgements

We would like to thank Isabel Reuter and Annette Laudahn for their help during the experiments, and Bo Leberecht for video editing. Special thanks to Prof. L. Forti (UNESP Botucatu, Brazil) for providing the colonies and two anonymous reviewers, whose comments improved the manuscript.

Compliance with ethical standards

All international, national, and institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

114_2018_1599_MOESM1_ESM.xlsx (12 kb)
ESM 1 (XLSX 11 kb)

References

  1. Andryszak NA, Payne TL, Dickens JC, Moser JC, Fisher RW (1990) Antennal olfactory responsiveness of the Texas leaf cutting ant (Hymenoptera: Formicidae) to trail pheromone and its two alarm substances. J Entomol Sci 25:593–598CrossRefGoogle Scholar
  2. Arenas A, Roces F (2016) Learning through the waste: olfactory cues from the colony refuse influence plant preferences in foraging leaf-cutting ants. J Exp Biol 219:2490–2496.  https://doi.org/10.1242/jeb.139568 CrossRefPubMedGoogle Scholar
  3. Arenas A, Roces F (2017) Avoidance of plants unsuitable for the symbiotic fungus in leaf-cutting ants: learning can take place entirely at the colony dump. PLoS One 12:e0171388.  https://doi.org/10.1371/journal.pone.0171388 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Arenas A, Roces F (2018) Appetitive and aversive learning of plants odors inside different nest compartments by foraging leaf-cutting ants. J Insect Physiol 109:85–92.  https://doi.org/10.1016/j.jinsphys.2018.07.001 CrossRefPubMedGoogle Scholar
  5. Arenas A, Fernández VM, Farina WM (2007) Floral odor learning within the hive affects honeybees’ foraging decisions. Naturwissenschaften 94:218–222.  https://doi.org/10.1007/s00114-006-0176-0 CrossRefPubMedGoogle Scholar
  6. Ballari SA, Farji-Brener AG (2006) Refuse dumps of leaf-cutting ants as a deterrent for ant herbivory : does refuse age matter ? Entomol Exp Appl 121:215–219.  https://doi.org/10.1111/j.1570-7458.2006.00475.x CrossRefGoogle Scholar
  7. Bollazzi M, Forti LC, Roces F (2012) Ventilation of the giant nests of Atta leaf-cutting ants : does underground circulating air enter the fungus chambers ? Insect Soc 59:487–498.  https://doi.org/10.1007/s00040-012-0243-9 CrossRefGoogle Scholar
  8. Bot ANM, Currie CR, Hart AG, Boomsma JJ (2001) Waste management in leaf-cutting ants. Ethol Ecol Evol 13:225–237CrossRefGoogle Scholar
  9. Côté IM, Poulin R (1995) Parasitism and group-size in social animals: a meta-analysis. Behav Ecol 6:159–165.  https://doi.org/10.1093/beheco/6.2.159 CrossRefGoogle Scholar
  10. Currie CR, Stuart AE (2001) Weeding and grooming of pathogens in agriculture by ants. Proc R Soc B Biol Sci 268:1033–1039.  https://doi.org/10.1098/rspb.2001.1605 CrossRefGoogle Scholar
  11. Currie CR, Mueller UG, Malloch D (1999) The agricultural pathology of ant fungus gardens. Proc Natl Acad Sci U S A 96:7998–8002CrossRefGoogle Scholar
  12. Farji-Brener AG, Elizalde L, Fernández-Marín H, Amador-Vargas S (2016) Social life and sanitary risks: evolutionary and current ecological conditions determine waste management in leaf-cutting ants. Proc R Soc B Biol Sci 283:20160625.  https://doi.org/10.1098/rspb.2016.0625 CrossRefGoogle Scholar
  13. Forti LC, de Andrade APP, Camargo R d S et al (2017) Discovering the giant nest architecture of grass-cutting ants, Atta capiguara (Hymenoptera, Formicidae). Insects 8:39.  https://doi.org/10.3390/insects8020039 CrossRefPubMedCentralGoogle Scholar
  14. Grassé P-P (1959) La reconstruction du nid et les coordinations interindividuelles chez Bellicositermes natalensis et Cubitermes sp. La theorie de la stigmergie: Essai d’interpretation du comportement des termites constructeurs. Insect Soc 6:41–83CrossRefGoogle Scholar
  15. Hart AG, Ratnieks FLW (2002) Waste management in the leaf-cutting ant Atta colombica. Behav Ecol 13:224–231CrossRefGoogle Scholar
  16. Heyman Y, Shental N, Brandis A, Hefetz A, Feinerman O (2017) Ants regulate colony spatial organization using multiple chemical road-signs. Nat Commun 8:1–11.  https://doi.org/10.1038/ncomms15414 CrossRefGoogle Scholar
  17. Howard DF, Tschinkel WR (1976) Aspects of necrophoric behavior in the red imported fire ant Solenopsis invicta. Behaviour 56:157–178CrossRefGoogle Scholar
  18. Jaffé K (1982) Chemical communication systems in the ant Atta cephalotes. From: social insects in the tropics. In: Jaisson P (ed) Proceedings of the first international symposium by the International Union for the Study of social insects and the Sociedad Mexicana de Entomología. Université Paris-Nord, Paris, pp 165–180Google Scholar
  19. Jonkman JCM (1980) The external and internal structure and growth of nests of the leaf-cutting ant Atta vollenweideri Forel, 1893 (Hym.: Formicidae), part II. Z Angew Entomol 89:217–246CrossRefGoogle Scholar
  20. Kelber C, Rössler W, Roces F, Kleineidam CJ (2009) The antennal lobes of fungus-growing ants (Attini): neuroanatomical traits and evolutionary trends. Brain Behav Evol 73:273–284.  https://doi.org/10.1159/000230672 CrossRefPubMedGoogle Scholar
  21. Kleineidam CJ, Rössler W, Hölldobler B, Roces F (2007) Perceptual differences in trail-following leaf-cutting ants relate to body size. J Insect Physiol 53:1233–1241.  https://doi.org/10.1016/j.jinsphys.2007.06.015 CrossRefPubMedGoogle Scholar
  22. Moreira AA, Forti LC, Andrade APP et al (2004) Nest architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud Neotropical Fauna Environ 39:109–116CrossRefGoogle Scholar
  23. Pielström S, Roces F (2013) Sequential soil transport and its influence on the spatial organisation of collective digging in leaf-cutting ants. PLoS One 8:e57040.  https://doi.org/10.1371/journal.pone.0057040 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Provecho Y, Josens R (2009) Olfactory memory established during trophallaxis affects food search behaviour in ants. J Exp Biol 212:3221–3227.  https://doi.org/10.1242/jeb.033506 CrossRefPubMedGoogle Scholar
  25. Ribeiro PL, Navas CA (2007) The leaf-cutting ant Atta sexdens rubropilosa, FOREL, 1908 prefers drier chambers for garbage disposal. J Insect Behav 20:19–24.  https://doi.org/10.1007/s10905-006-9052-1 CrossRefGoogle Scholar
  26. Rifkin JL, Nunn CL, Garamszegi LZ (2012) Do animals living in larger groups experience greater parasitism? A meta-analysis. Am Nat 180:70–82.  https://doi.org/10.1086/666081 CrossRefPubMedGoogle Scholar
  27. Roces F (1990) Olfactory conditioning during the recruitment process in a leaf-cutting ant. Oecologia 83:261–262CrossRefGoogle Scholar
  28. Sachse S, Krieger J (2011) Olfaction in insects. e-Neuroforum 17:49–60.  https://doi.org/10.1007/s13295-011-0020-7 CrossRefGoogle Scholar
  29. Stahel G, Geijskes DC (1939) Ueber den Bau der Nester von Atta cephalotes L. und Atta sexdens L. (Hym. Formicidae). Rev Entomol 10:27–78Google Scholar
  30. Wilson EO, Durlach NI, Roth LM (1958) Chemical releasers of necrophoric behavior in ants. Psyche (Stuttg) 65:108–114CrossRefGoogle Scholar
  31. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54:405–423.  https://doi.org/10.1146/annurev.ento.53.103106.093301 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Behavioral Physiology and Sociobiology, BiocenterUniversity of WürzburgWürzburgGermany

Personalised recommendations