Stability and Responsiveness in a Self-Organized Living Architecture

Abstract

Robustness and adaptability are central to the functioning of biological systems, from gene networks to animal societies. Yet the mechanisms by which living organisms achieve both stability to perturbations and sensitivity to input are poorly understood. Here, we present an integrated study of a living architecture in which army ants interconnect their bodies to span gaps. We demonstrate that these self-assembled bridges are a highly effective means of maintaining traffic flow over unpredictable terrain. The individual-level rules responsible depend only on locally-estimated traffic intensity and the number of neighbours to which ants are attached within the structure. We employ a parameterized computational model to reveal that bridges are tuned to be maximally stable in the face of regular, periodic fluctuations in traffic. However analysis of the model also suggests that interactions among ants give rise to feedback processes that result in bridges being highly responsive to sudden interruptions in traffic. Subsequent field experiments confirm this prediction and thus the dual nature of stability and flexibility in living bridges. Our study demonstrates the importance of robust and adaptive modular architecture to efficient traffic organisation and reveals general principles regarding the regulation of form in biological self-assemblies.

Army ants dynamically adjust living bridges in response to a cost–benefit trade-off

“…larger gaps (19). The ants use these bridges as the leaf-litter terrain demands, such that long stretches of tens of meters over relatively smooth terrain (e.g., large logs and fallen branches) may contain no bridges, whereas areas of particularly rough and broken terrain may contain multiple bridges per meter of trail.…”

Optimal construction of army ant living bridges

“…In order to improve the efficiency of their trails, army ants are capable of linking their own bodies together to dynamically create physical structures along 35 the foraging path [18,19,27,28,16]. These structures may be used to widen paths to increase the flux of ants, or to form bridges over gaps in the terrain (reaching spans of over 12 cm, or approximately 12 ant body lengths) to decrease the tortuosity of their trails [29,16].…”

“…These structures may be used to widen paths to increase the flux of ants, or to form bridges over gaps in the terrain (reaching spans of over 12 cm, or approximately 12 ant body lengths) to decrease the tortuosity of their trails [29,16]. Ants modulate their bridge-building behavior in response to local information, allowing these bridges to adapt to current 40 traffic conditions, recover from damage, and dissemble when underused [28], so that they exist as needed at particular points along the trail.…”

“…The ants forming the bridges are locked into the structure, sometimes for several minutes at a time [28], 45 preventing them from participating in other important foraging activities such as capturing and killing prey or transporting food items along the trail. Understanding the overall effect of these living structures on the colony's foraging rate requires a quantification of both the benefit (here, shortening the travel distance) and cost (here, removing ants from the foraging pool) of each structure, In a recent study, Reid et al [16] experimentally manipulated living bridges built by colonies of E. hamatum and measured these benefits and costs.…”

Selection favors incompatible signaling in bacteria

“…To do so, it has provided the members of cooperative groups with communication tools, which are critical for effective cooperation. For example, some ants form bridges with their bodies to help their nest-mates cross a gap (1,2). But this admirable behavior only makes sense when many ants mass along the same route; a lone scout that stayed put across a gap instead of wandering off in search for food would do a disservice to the colony.…”