Underground nest building: the effect of CO2 on digging rates, soil transport and choice of a digging site in leaf-cutting ants

Abstract

By reacting to local environmental stimuli, ant workers excavate a nest that offers suitable climatic conditions. Workers may face increasing CO2 levels while digging across the soil profile, and it is an open question whether these levels are used as cues during nest excavation. Here, we explored the influence of different underground CO2 concentrations on digging behavior in the leaf-cutting ant Acromyrmex lundii. We first quantified digging rates and transport of excavated material as a function of CO2 levels, ranging from atmospheric values to 11% CO2. The mass of both the excavated soil and the pellets transported out of the digging chamber were quantified. CO2 preferences for excavation were investigated in a second experiment, in which workers were presented with a choice of two digging sites that differed in their CO2 levels, ranging from atmospheric to 4% CO2, and the mass of excavated material was quantified. Digging rates were similar for all tested CO2 levels up to 7%, and only significantly lower for 11%. The transport of excavated soil increased with increasing CO2 levels up to 7%, and then decreased at 11%. Workers preferred digging at 1% CO2 and avoided levels of 4%. We suggest that the observed CO2 preferences are likely driven by the requirements of their symbiotic fungus, and could be one of the reasons why colonies of A. lundii excavate superficial nest chambers.

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References

  1. Beckmann HE (1974) The damaging effect of supercooling, narcosis and stress on the memory of the honeybee. J Comp Physiol 94:249–266

    Article  Google Scholar 

  2. 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? Insectes Soc 59:487–498. https://doi.org/10.1007/s00040-012-0243-9

    Article  Google Scholar 

  3. Bollazzi M, Kronenbitter J, Roces F (2008) Soil temperature, digging behaviour, and the adaptive value of nest depth in South American species of Acromyrmex leaf-cutting ants. Oecologia 158:165–175. https://doi.org/10.1007/s00442-008-1113-z

    Article  PubMed  Google Scholar 

  4. Bollazzi M, Roces F (2002) Thermal preference for fungus culturing and brood location by workers of the thatching grass-cutting ant Acromyrmex heyeri. Insectes Soc 49:153–157. https://doi.org/10.1007/s00040-002-8295-x

    Article  Google Scholar 

  5. Bollazzi M, Roces F (2007) To build or not to build: circulating dry air organizes collective building for climate control in the leaf-cutting ant Acromyrmex ambiguus. Anim Behav 74:1349–1355. https://doi.org/10.1016/j.anbehav.2007.02.021

    Article  Google Scholar 

  6. Bonabeau E (1998) Fixed response thresholds and the regulation of division of labor in insect societies. Bull Math Biol 60:753–807. https://doi.org/10.1006/bulm.1998.0041

    Article  Google Scholar 

  7. Coelho Junior A, Geremias LD, Alves GR et al (2017) The biology of Trichogramma pretiosum as atmospheric O2 becomes depleted and CO2 accumulates. Biol Control 105:1–5. https://doi.org/10.1016/j.biocontrol.2016.11.005

    Article  Google Scholar 

  8. Coelho Junior A, Parra JRP (2013) Effect of carbon dioxide (CO2) on mortality and reproduction of Anagasta kuehniella (Zeller 1879), in mass rearing, aiming at the production of Trichogramma spp. An Acad Bras Cienc 85:823–831. https://doi.org/10.1590/S0001-37652013000200021

    Article  PubMed  Google Scholar 

  9. Deneubourg JL, Franks NR (1995) Collective control without explicit coding: the case of communal nest excavation. J Insect Behav 8:417–432. https://doi.org/10.1007/BF01995316

    Article  Google Scholar 

  10. Falibene A, Roces F, Rössler W, Groh C (2016) Daily thermal fluctuations experienced by pupae via rhythmic nursing behavior increase numbers of mushroom body microglomeruli in the adult ant brain. Front Behav Neurosci 10:1–12. https://doi.org/10.3389/fnbeh.2016.00073

    Article  Google Scholar 

  11. Grassé P-P (1959) La reconstruction du nid et les coordinations interindividuelles chez Bellicositermes natalensis et Cubitermes sp. La theorie de la stigmergie. Insectes Soc 6:41–83

    Article  Google Scholar 

  12. Guerenstein PG, Hildebrand JG (2008) Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178. https://doi.org/10.1146/annurev.ento.53.103106.093402

    CAS  Article  PubMed  Google Scholar 

  13. Halboth F, Roces F (2017) The construction of ventilation turrets in Atta vollenweideri leaf-cutting ants: carbon dioxide levels in the nest tunnels, but not airflow or air humidity, influence turret structure. PLoS One 12:e0188162. https://doi.org/10.1371/journal.pone.0188162

    Article  PubMed  PubMed Central  Google Scholar 

  14. Hamada Y, Tanaka T (2001) Dynamics of carbon dioxide in soil profiles based on long-term field observation. Hydrol Process 15:1829–1845. https://doi.org/10.1002/hyp.242

    Article  Google Scholar 

  15. Hangartner W (1969) Carbon dioxide, a releaser for digging behavior in Solenopsis geminata (Hymenoptera: Formicidae). Psyche (Stuttg) 76:58–67. https://doi.org/10.1155/1969/58428

    Article  Google Scholar 

  16. Hansell MH (1984) Animal architecture and building behavior. Longman Inc., New York

    Google Scholar 

  17. Hebling MJA, Penteado CHS, Mendes EG (1992) Respiratory regulation in workers of the leaf cutting ant Atta sexdens rubropilosa Forel, 1908. Comp Biochem Physiol 101:319–322

    Article  Google Scholar 

  18. Hillel D (1998) Environmental soil physics. Academic Press, London

    Google Scholar 

  19. Klaiber J, Najar-Rodriguez A, Dialer E, Dorn S (2013) Elevated carbon dioxide impairs the performance of a specialized parasitoid of an aphid host feeding on Brassica plants. Biol Control 66:49–55

    CAS  Article  Google Scholar 

  20. Kleineidam C, Roces F (2000) Carbon dioxide concentrations and nest ventilation in nests of the leaf-cutting ant Atta vollenweideri. Insectes Soc 47:241–248. https://doi.org/10.1007/PL00001710

    Article  Google Scholar 

  21. Kleineidam C, Romani R, Tautz J, Isidoro N (2000) Ultrastructure and physiology of the CO2 sensitive sensillum ampullaceum in the leaf-cutting ant Atta sexdens. Arthropod Struct Dev 29:43–55

    CAS  Article  PubMed  Google Scholar 

  22. Kleineidam C, Tautz J (1996) Perception of carbon dioxide and other “air-condition” parameters in the leaf cutting ant Atta cephalotes. Naturwissenschaften 83:566–568. https://doi.org/10.1007/BF01141981

    CAS  Google Scholar 

  23. Moreira AA, Forti LC, Andrade APP et al (2004a) Nest architecture of Atta laevigata (F. Smith 1958) (Hymenoptera: Formicidae). Stud Neotrop Fauna Environ 39:109–116. https://doi.org/10.1080/01650520412331333756

    Article  Google Scholar 

  24. Moreira A, Forti L, Boaretto M et al (2004b) External and internal structure of Atta bisphaerica Forel (Hymenoptera: Formicidae) nests. J Appl Entomol 128:204–211. https://doi.org/10.1111/j.1439-0418.2004.00839.x

    Article  Google Scholar 

  25. Moser JC (1963) Contents and structure of Atta texana nest in summer. Ann Entomol Soc Am 56:286–291

    Article  Google Scholar 

  26. Nicolas G, Sillans D (1989) Immediate and latent effects of carbon dioxide on insects. Annu Rev Entomol 34:97–116. https://doi.org/10.1146/annurev.en.34.010189.000525

    CAS  Article  Google Scholar 

  27. Nielsen MG, Christian K, Henriksen PG, Birkmose D (2006) Respiration by mangrove ants Camponotus anderseni during nest submersion associated with tidal inundation in Northern Australia. Physiol Entomol 31:120–126. https://doi.org/10.1111/j.1365-3032.2005.00492.x

    CAS  Article  Google Scholar 

  28. Pielström S, Roces F (2012) Vibrational communication in the spatial organization of collective digging in the leaf-cutting ant Atta vollenweideri. Anim Behav 84:743–752. https://doi.org/10.1016/j.anbehav.2012.07.008

    Article  Google Scholar 

  29. 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

    Article  PubMed  PubMed Central  Google Scholar 

  30. Pielström S, Roces F (2014) Soil moisture and excavation behaviour in the chaco leaf-cutting ant (Atta vollenweideri): digging performance and prevention of water inflow into the nest. PLoS One. https://doi.org/10.1371/journal.pone.0095658

    PubMed  PubMed Central  Google Scholar 

  31. Powell RJ, Stradling DJ (1986) Factors influencing the growth of Attamyces bromatificus, a symbiont of attine ants. Trans Br Mycol Soc 87:205–213. https://doi.org/10.1016/S0007-1536(86)80022-5

    CAS  Article  Google Scholar 

  32. Quinlan RJ, Cherrett JM (1978) Aspects of the symbiosis of the leaf-cutting ant Acromyrmex octospinosus (Reich) and its food fungus. Ecol Entomol 3:221–230. https://doi.org/10.1111/j.1365-2311.1977.tb00877.x doi

    Article  Google Scholar 

  33. Rasse P, Deneubourg JL (2001) Dynamics of nest excavation and nest size regulation of Lasius niger (Hymenoptera: Formicidae). J Insect Behav 14:433–449. https://doi.org/10.1023/A:1011163804217

    Article  Google Scholar 

  34. Roces F, Kleineidam C (2000) Humidity preference for fungus culturing by workers of the leaf-cutting ant Atta sexdens rubropilosa. Insectes Soc 47:348–350. https://doi.org/10.1007/PL00001728

    Article  Google Scholar 

  35. Roces F, Núñez J (1989) Brood translocation and circadian variation of temperature preference in the ant Camponotus mus. Oecologia 81:33–37. https://doi.org/10.1007/BF00377006

    Article  PubMed  Google Scholar 

  36. Römer D, Bollazzi M, Roces F (2017) Carbon dioxide sensing in an obligate insect fungus symbiosis: CO2 preferences of leaf-cutting ants to rear their mutualistic fungus. PLoS One 12:e0174597. https://doi.org/10.1371/journal.pone.0174597

    Article  PubMed  PubMed Central  Google Scholar 

  37. Römer D, Roces F (2014) Nest enlargement in leaf-cutting ants: Relocated brood and fungus trigger the excavation of new chambers. PLoS One 9:e97872. https://doi.org/10.1371/journal.pone.0097872

    Article  PubMed  PubMed Central  Google Scholar 

  38. Römer D, Roces F (2015) Available space, symbiotic fungus and colony brood influence excavation and lead to the adjustment of nest enlargement in leaf-cutting ants. Insectes Soc 62:401–413. https://doi.org/10.1007/s00040-015-0419-1

    Article  Google Scholar 

  39. Röschard J, Roces F (2003) Cutters, carriers and transport chains: Distance-dependent foraging strategies in the grass-cutting ant Atta vollenweideri. Insectes Soc 50:237–244. https://doi.org/10.1007/s00040-003-0663-7

    Article  Google Scholar 

  40. Schofield RMS, Emmett KD, Niedbala JC, Nesson MH (2011) Leaf-cutter ants with worn mandibles cut half as fast, spend twice the energy, and tend to carry instead of cut. Behav Ecol Sociobiol 65:969–982. https://doi.org/10.1007/s00265-010-1098-6

    Article  Google Scholar 

  41. Schwartz DM, Bazzaz FA (1973) In situ measurements of carbon dioxide gradients in a soil-plant-atmosphere system. Oecologia 12:161–167. https://doi.org/10.1007/BF00345515

    Article  PubMed  Google Scholar 

  42. Theraulaz G, Bonabeau E (1999) A brief history of stigmergy. Artif Life 5:97–116

    CAS  Article  PubMed  Google Scholar 

  43. Theraulaz G, Bonabeau E, Deneubourg J-L (1998) The origin of nest complexity in social insects. Complexity 3:15–25

    Article  Google Scholar 

  44. Tschinkel WR (2013) Florida harvester ant nest architecture, nest relocation and soil carbon dioxide gradients. PLoS One 8:e59911. https://doi.org/10.1371/journal.pone.0059911

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Tschinkel WR (2004) The nest architecture of the Florida harvester ant, Pogonomyrmex badius. J Insect Sci 4:21. https://doi.org/10.1672/1536-2442(2004)004

    Article  PubMed  PubMed Central  Google Scholar 

  46. Verza SS, Forti LC, Lopes JFS, Hughes WOH (2007) Nest architecture of the leaf-cutting ant Acromyrmex rugosus rugosus. Insectes Soc 54:303–309. https://doi.org/10.1007/s00040-007-0943-8

    Article  Google Scholar 

  47. Zolessi LC, González LA (1978) Observaciones sobre el género Acromyrmex en el Uruguay. IV. A. (Acromyrmex) lundi (Guérin, 1938) (Hymenoptera: Formicidae). Rev la Fac Humanidades y Ciencias Ser Ciencias Biológicas 1:9–28

    Google Scholar 

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Acknowledgements

We would like to thank David Urbaniec, Lisa Weidner and Baris Düdükcü for their help during the experiments, and Griselda Roces for the ant drawing. We are grateful to two anonymous reviewers, whose comments greatly improved the manuscript. Daniela Römer was supported by a grant from the Postdoc Plus funding program of the Graduate School of Life Sciences (GSLS) of the University of Würzburg, Germany, and a Grant of the Agencia Nacional de Investigación e Innovación (ANII, Grant Number PD_NAC_2015_1_108641), Uruguay. Florian Halboth was supported by a Grant from the German Excellence Initiative to the Graduate School of Life Sciences, University of Würzburg.

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Römer, D., Halboth, F., Bollazzi, M. et al. Underground nest building: the effect of CO2 on digging rates, soil transport and choice of a digging site in leaf-cutting ants. Insect. Soc. 65, 305–313 (2018). https://doi.org/10.1007/s00040-018-0615-x

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Keywords

  • Carbon dioxide
  • Nest excavation
  • Cue
  • Self-organization
  • Nest architecture