Shape transition during nest digging in ants

Abstract

Nest building in social insects is among the collective processes that show highly conservative features such as basic modules (chambers and galleries) or homeostatic properties. Although ant nests share common characteristics, they exhibit a high structural variability, of which morphogenesis and underlying mechanisms remain largely unknown. We conducted two-dimensional nestdigging experiments under homogeneous laboratory conditions to investigate the shape diversity that emerges only from digging dynamics and without the influence of any environmental heterogeneity. These experiments revealed that, during the excavation, a morphological transition occurs because the primary circular cavity evolves into a ramified structure through a branching process. Such a transition is observed, whatever the number of ants involved, but occurs more frequently for a larger number of workers. A stochastic model highlights the central role of density effects in shape transition. These results indicate that nest digging shares similar properties with various physical, chemical, and biological systems. Moreover, our model of morphogenesis provides an explanatory framework for shape transitions in decentralized growing structures in group-living animals.self-organization | nest building | branching pattern | modeling | collective behavior T he building of structures by animals is a widely spread phenomenon, from protozoa to primates (1). These structures can be considered an extension of the animal body: They have an adaptive value by improving the regulation of energetic exchanges with the outer environment (2), by ensuring the management of waste compounds (3), and by allowing food storage or protection against predation, but also by shaping the spatial distribution of social interactions (4). The nests of social insects take over all of these functions and show a robust relationship between nest volume and colony size (5-9). In ants, every nest is made of the same basic building modules (9-11) (i.e. chambers, tunnels), the sameness of which contrasts with the diversity of nest architecture (number and proportion of different modules, nest topology, and pattern regularity) that varies not only interspecifically but also intraspecifically according to the colony growth process (7, 9).Although a dynamic study of nest building is essential to understand how the diversity of patterns is generated, there are few such studies (5, 6) addressing this issue. Most research describes final nest structures (7, 9, 12) or focuses on particular digging behaviors (13, 14) but provides few insights on the building process as a whole or on the mechanisms that generate a diversity of nest shapes.The prevailing questions, therefore, are: Does the shape diversity find its origin in the complexity of the building behaviors of the insects, a specific behavior being associated to a specific shape or in quantitative changes in digging activity? Does it result from changes in the insect environment due to the building process itself? Or does the nest pa...

Excavated substrate modulates growth instability during nest building in ants

“…We have previously highlighted the fundamental mechanisms of the morphological transitions during nest building (Toffin et al 2009). For a given material (sand) and whatever the population size, the density of activity r ¼ R/A is a predictor of the morphological transition.…”

“…For a given material (sand, granular substrate) and whatever the population size, the first transition is known to occur at a characteristically low value of density of activity defined as r ¼ R/A (Toffin et al 2009). Here, for both materials, the r values remained close, suggesting that this ratio was still a good predictor of the first morphological transition.…”

“…However, we have recently shown (Toffin et al 2009) that a characteristic sequence of events occurs during nest excavation in ants. Two extreme morphologies successively appear through a morphological transition process: an initially rounded and smooth chamber is initially dug before it becomes more irregular as buds appear on the nest walls.…”

Morphogenesis of an extended phenotype: four-dimensional ant nest architecture

“…Previous studies of excavation dynamics, involving indirect measures of three-dimensional nest growth [20] or two-dimensional scenarios, identified logistic dynamics with an initial exponential growth phase followed by a plateau [22][23][24][25]. Such studies suggested that excavation could be mediated by recruitment with ants being stimulated to excavate by pheromones, carbon dioxide concentrations or physical contacts among ants [20,22,23,41].…”

Stigmergic construction and topochemical information shape ant nest architecture

“…Theoretical models have been proposed to account for 3D nest construction in wasps and termites (17)(18)(19), indicating that stigmergic interactions can potentially explain the coordination of nest building in these animal groups. However, a detailed and experimentally founded understanding of the interactions between the animals and the structures that they are building is limited to the construction of simple 2D structures produced by ants and termites, either by digging the substrate (20)(21)(22)(23)(24)(25) or piling soil particles (26)(27)(28). In ants, 3D nest construction remains poorly documented and so far no study has attempted to connect a detailed quantitative description of individual building behavior with the growth dynamics and the resulting shape of nests.…”