A blog post highlighting the article by D. Römer, F. Halboth, M. Bollazzi and F. Roces in Insectes Sociaux

By Daniela Römer

Watch a nature documentary of the South American tropics and it’s almost a given you will see some columns of leaf-cutting ants, busily carrying leaves back to their nest. Aside from their photogenic foraging behaviour these ants are also known for having developed the ability of farming, a feat only humans and some termite species have achieved. Perhaps less well known to the public, but equally as impressive, are their underground nests. The ants use the freshly cut plant material as a substrate to grow a symbiotic fungus, which is very voluminous and therefore needs a lot of space. Adding to the space demands of their nests are the high number of ‘citizens’ a single leaf-cutting ant colony can have, sometimes reaching millions (Moreira et al. 2004a, b). When scientists want to make casts of the nests to discover the intricate network of their nest chambers and connecting tunnels, they need tons and tons of cement to fill the complete structure (Forti et al. 2017). And yet, the tiny single workers measure less than a centimetre and weigh only 5-25 mg. How do these little, autonomous units coordinate their digging effort with thousands of other small units so that these huge functional nest structures are created?

The answer to this question is a process known as ‘self-organization’. The tiny workers with their very limited view of the nest structure react to very simply cues of their immediate environment and so decide where and when to excavate (Deneubourg and Franks 1995).

Worker of Acromyrmex lundii leaving a digging arena.       Photo: James Waters

Having encountered an underground environment to their liking, the workers dig with their mandibles into the earth and, as if it would be a piece of vegetation to harvest, ‘cut’ out little bits of soil, which they then discard outside of the nest. Digging is a strenuous process and a colony spends considerable energy excavating their nest. What the ants gain from such a herculean effort is a structure that offers the colony, and in the case of leaf-cutting ants, their symbiotic fungus (on whose survival colony success depends) an environment suitable for both.

Underground, the three main environmental factors are temperature, humidity and carbon dioxide. The latter is quite frequently mentioned in the media in connection with global warming, where even seemingly small increases in CO₂ levels can lead to dramatic environmental changes. Subterranean ants are confronted with CO₂ concentrations vastly exceeding atmospheric levels (currently ~0.04%), even very close to the soil surface. These levels increase even more with depth so that 5-6 meters underground ants encounter an environment with 6-7% CO₂ (Kleineidam and Roces 2000; Bollazzi et al. 2012). At these high levels, the growth of the farmed fungus seems to be compromised (Kleineidam and Roces 2000), so that leaf-cutting ants should try to control carbon dioxide levels to ensure the best possible fungus harvest. A recent study showed that when given the choice, the leaf-cutting ant Acromyrmex lundii indeed avoids such high CO₂ levels for fungus farming and, surprisingly, also atmospheric levels (Römer et al. 2017). Instead, it chose levels associated with soil strata close to the surface.

We therefore asked ourselves whether the ants also use the carbon dioxide concentration underground as a cue when they excavate their nests and examined this question by performing different experiments. In the first, we tested whether the ants’ digging activity and soil pellet transport was affected with increasing CO₂ concentrations (from atmospheric values to 11%). In the second experiment, we evaluated what CO₂ concentration workers prefer for nest digging, using a binary setup, offering atmospheric, shallow soil (1%) and deep soil (4%) CO₂ concentrations.

Digging arenas at end of  experiment 1. CO₂ levels L to R: atmospheric, 4%, 11%.           Photo: Daniela Römer

Acromyrmex lundii is a species whose nest is usually characterized by having only superficial nest chambers. This is apparently not due to the inability of the ants to excavate under higher CO₂ concentrations, as digging activity was comparable whether the ants excavated under atmospheric CO₂ concentrations or levels of deeper nesting leaf-cutting ants. Only at 11%, a level so high that it was never measured around any leaf-cutting ant nest (Nielsen et al. 2003), the ants reduced their digging activity. Therefore, a negative effect of CO₂ on digging activity does not seem to be the reason why this ant species only excavates superficial chambers. Soil pellet transport away from the digging site, on the other hand, increased when CO₂ concentration underground increased. We do not know whether this was because ants were physically unable to excavate and therefore switched to soil carrying (masked at most CO₂ levels by replacement workers) or whether ants ‘aimed’ to increase ventilation at the site by creating more open space. When creating a situation where workers could choose where they wanted to dig, they preferred superficial-soil CO₂ levels and avoided levels of deeper soil strata. These choices help to explain the ants’ nesting biology.

One might therefore ask ‘Then why do other leaf-cutting ants excavate deep nests if the high CO₂ concentrations there hinder the growth of their food source?’ The answer to this question might be a competition between the different environmental factors in the soil. Leaf-cutting ants should trade-off their microclimatic preferences to ensure the excavation of a suitable nest, but that is an experiment for another day

References

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. doi: 10.1007/s00040-012-0243-9

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

Forti LC, Protti de Andrade AP, Camargo R da S, et al (2017) Discovering the giant nest architecture of grass-cutting ants, Atta capiguara (Hymenoptera , Formicidae). Insects 8:39. doi: 10.20944/preprints201702.0027.v1

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. doi: 10.1007/PL00001710

Moreira AA, Forti LC, Andrade APP, et al (2004a) Nest architecture of Atta laevigata (F . Smith , 1858) (Hymenoptera : Formicidae). Stud Neotrop Fauna Environ 39:109–116.

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. doi: 10.1111/j.1439-0418.2004.00839.x

Nielsen MG, Christian K, Birkmose D (2003) Carbon dioxide concentrations in the nests of the mud-dwelling mangrove ant Polyrhachis sokolova Forel (Hymenoptera: Formicidae). Aust J Entomol 42:357–362. doi: 10.1046/j.1440-6055.2003.00372.x

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. doi: 10.1371/journal.pone.0174597