Substrate evaporation drives collective construction in termites

Abstract

Termites build complex nests which are an impressive example of self-organization. We know that the coordinated actions involved in the construction of these nests by multiple individuals are primarily mediated by signals and cues embedded in the structure of the nest itself. However, to date there is still no scientific consensus about the nature of the stimuli that guide termite construction, and how they are sensed by termites. In order to address these questions, we studied the early building behavior of Coptotermes gestroi termites in artificial arenas, decorated with topographic cues to stimulate construction. Pellet collections were evenly distributed across the experimental setup, compatible with a collection mechanism that is not affected by local topography, but only by the distribution of termite occupancy (termites pick pellets at the positions where they are). Conversely, pellet depositions were concentrated at locations of high surface curvature and at the boundaries between different types of substrate. The single feature shared by all pellet deposition regions was that they correspond to local maxima in the evaporation flux. We can show analytically and we confirm experimentally that evaporation flux is directly proportional to the local curvature of nest surfaces. Taken together, our results indicate that surface curvature is sufficient to organize termite building activity and that termites likely sense curvature indirectly through substrate evaporation. Our findings reconcile the apparently discordant results of previous studies.

Keywords: collective behavior; complex systems; morphogenesis; networks; physics of living systems; self-organisation.

Figure 1.. Experimental setup.

Sketch of the experimental setup (left) and snapshot of one experiment (E66) before termites were added to the setup (right). The white marks on the picture give the scale of the setup, with the distance between successive marks being 1, 3, and 5 cm.

Figure 1—figure supplement 1.. Close-up on pillar structures built by our captive colony of Coptotermes gestroi within the plastic barrel that hosts the full colony.

Figure 1—figure supplement 2.. Temperature (blue) and humidity (red) within the Petri dish as a function of time.

The shaded area refers to a time interval where the probe was placed on the bottom plate of the Petri dish but outside the clay disk. During the remaining time, the probe was placed on the clay disk.

Figure 2.. Experimental results - heatmaps.

Top: (A) cumulative heatmaps of deposition ($P(D)$; blue) and collection activity ($P(C)$; yellow) normalized by their respective mean values for one experiment (E66), colorbars are the same as in panel (E); (B) cumulative depositions (top) and collections (bottom) per unit area as a function of the Petri dish radius for experiments E58, E63, E65, E66, and E76, all histograms have been normalized and sum up to 1; (C) comparison among experimental depositions (in red), surface curvature (in blue) shown in Figure 3C, and depositions predicted by simulations (black) shown in Figure 3C, all the quantities are computed along the radial cut shown in panel (A), depositions are normalized by their maximum value and curvature is in ${\mathrm{mm}}^{-1}$; (D) cumulative occupancy heatmap normalized by its mean value for E66; (E) depositions ($P(D|O)$; blue) and collections ($P(C|O)$; yellow) conditional to cumulative normalized occupancy for E66.

Figure 3.. Laboratory experiments and simulations of the growth model.

Top row: snapshots of a building experiment with ‘pillars’ cue (E66) (A) and a building experiment with ‘wall’ cue (E78) (B). Bottom row: snapshots of 3D simulations initiated with copies of the experimental setup E66 (C, D) and E78 (E, F) in which nest growth is entirely determined by the local surface curvature (based on our previously described model Facchini et al., 2020). Snapshots C and E refer to t=0, D and F refer to t=9 (dimensionless). The color map corresponds to the value of the mean curvature at the interface air-nest. White indicates convex regions and black indicates concave regions. The scale bars correspond to 1 cm.

Figure 3—figure supplement 1.. Snapshots of experiments with pillar cues.

Superimposed labels denote: the experiment ID (top left), the time after the start of the experiment at which the picture was taken (top right) and the ID of the master colony (bottom right).

Figure 3—figure supplement 2.. Snapshots of experiments with wall cues.

Superimposed labels denote: the experiment ID (top left), the time after the start of the experiment at which the picture was taken (top right) and the ID of the master colony (bottom right).

Figure 3—figure supplement 3.. Snapshots of experiments with no cues.

Superimposed labels denote: the experiment ID (top left), the time after the start of the experiment at which the picture was taken (top right) and the ID of the master colony (bottom right).

Figure 4.. Diffusive simulations and chemical garden experiments.

Top row: contour of the humidity gradient $\nabla h$ obtained solving the Laplace equation $\mathrm{\Delta }h=0$ in a cubic domain with a humid bottom boundary $h=100\%$ (in brown) which is mapped from 3D scans of the experimental setup in E66 (A) and E78 (B). At the top boundary $h$ is fixed to $h=70\%$ which was the average value of humidity in our experimental room. Note that $h$ is the relative humidity, thus the magnitude of the humidity gradient $|\nabla h|$ is measured in ${\mathrm{mm}}^{-1}$, i.e $|\nabla h|=0.1{\mathrm{mm}}^{-1}$ means a humidity variation of 10% over $1\mathrm{mm}$. Each contour corresponds to a variation of $0.015{\mathrm{mm}}^{-1}$. Pillar tips are associated with a strong humidity gradient; the top of the wall is also associated with a strong humidity gradient, although not as strong as at the pillar tips. Also note that humidity gradient at the top corners of the wall is 30% stronger than on the rest of the top edge. Bottom row: snapshots of chemical garden experiments initiated with ‘pillars’ cue (C), and with ‘wall’ cue (D). All the scale bars correspond to $1\mathrm{cm}$.

Appendix 1—figure 1.. Sketch of curvature definition on a saddle shaped surface.

Appendix 2—figure 1.. Sketch of the experimental setup showing the contrast between how sharp is the shape of the wet substrate (orange region) at the disk edge, and how flat the same region can appear to a walking termite.