skip to main content


Title: Computational exploration of treadmilling and protrusion growth observed in fire ant rafts
Collective living systems regularly achieve cooperative emergent functions that individual organisms could not accomplish alone. The rafts of fire ants (Solenopsis invicta) are often studied in this context for their ability to create aggregated structures comprised entirely of their own bodies, including tether-like protrusions that facilitate exploration of and escape from flooded environments. While similar protrusions are observed in cytoskeletons and cellular aggregates, they are generally dependent on morphogens or external gradients leaving the isolated role of local interactions poorly understood. Here we demonstrate through an ant-inspired, agent-based numerical model how protrusions in ant rafts may emerge spontaneously due to local interactions. The model is comprised of a condensed structural network of agents that represents the monolayer of interconnected worker ants, which floats on the water and gives ant rafts their form. Experimentally, this layer perpetually contracts, which we capture through the pairwise contraction of all neighboring structural agents at a strain rate of d ˙ . On top of the structural layer, we model a dispersed, on-lattice layer of motile agents that represents free ants, which walk on top of the floating network. Experimentally, these self-propelled free ants walk with some mean persistence length and speed that we capture through an ant-inspired phenomenological model. Local interactions occur between neighboring free ants within some radius of detection, R , and the persistence length of freely active agents is tuned through a noise parameter, η as introduced by the Vicsek model. Both R and η where fixed to match the experimental trajectories of free ants. Treadmilling of the raft occurs as agents transition between the structural and free layers in accordance with experimental observations. Ultimately, we demonstrate how phases of exploratory protrusion growth may be induced by increased ant activity as characterized by a dimensionless parameter, A . These results provide an example in which functional morphogenesis of a living system may emerge purely from local interactions at the constituent length scale, thereby providing a source of inspiration for the development of decentralized, autonomous active matter and swarm robotics.  more » « less
Award ID(s):
1761918
NSF-PAR ID:
10401009
Author(s) / Creator(s):
;
Editor(s):
Maini, Philip K.
Date Published:
Journal Name:
PLOS Computational Biology
Volume:
18
Issue:
2
ISSN:
1553-7358
Page Range / eLocation ID:
e1009869
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Fire ants ( Solenopsis invicta ) are exemplary for their formation of cohered, buoyant and dynamic structures composed entirely of their own bodies when exposed to flooded environments. Here, we observe tether-like protrusions that emerge from aggregated fire ant rafts when docked to stationary, vertical rods. Ant rafts comprise a floating, structural network of interconnected ants on which a layer of freely active ants walk. We show here that sustained shape evolution is permitted by the competing mechanisms of perpetual raft contraction aided by the transition of bulk structural ants to the free active layer and outward raft expansion owing to the deposition of free ants into the structural network at the edges, culminating in global treadmilling. Furthermore, we see that protrusions emerge as a result of asymmetries in the edge deposition rate of free ants. Employing both experimental characterization and a model for self-propelled particles in strong confinement, we interpret that these asymmetries are likely to occur stochastically owing to wall accumulation effects and directional motion of active ants when strongly confined by the protrusions' relatively narrow boundaries. Together, these effects may realize the cooperative, yet spontaneous formation of protrusions that fire ants sometimes use for functional exploration and to escape flooded environments. 
    more » « less
  2. null (Ed.)
    We introduce a model for ant trail formation, building upon previous work on biologically feasible local algorithms that plausibly describe how ants maintain trail networks. The model is a variant of a reinforced random walk on a directed graph, where ants lay pheromone on edges as they traverse them and the next edge to traverse is chosen based on the level of pheromone; this pheromone decays with time. There is a bidirectional flow of ants in the network: the forward flow proceeds along forward edges from source (e.g. the nest) to sink (e.g. a food source), and the backward flow in the opposite direction. Some fraction of ants are lost as they pass through each node (modeling the loss of ants due to exploration observed in the field). We initiate a theoretical study of this model. We note that ant navigation has inspired the field of ant colony optimization, heuristics that have been applied to several combinatorial optimization problems; however the algorithms developed there are considerably more complex and not constrained to being biologically feasible. We first consider the linear decision rule, where the flow divides itself among the next set of edges in proportion to their pheromone level. Here, we show that the process converges to the path with minimum leakage when the forward and backward flows do not change over time. On the other hand, when the forward and backward flows increase over time (caused by positive reinforcement from the discovery of a food source, for example), we show that the process converges to the shortest path. These results are for graphs consisting of two parallel paths (a case that has been investigated before in experiments). Through simulations, we show that these results hold for more general graphs drawn from various random graph models; proving this convergence in the general case is an interesting open problem. Further, to understand the behaviour of other decision rules beyond the linear rule, we consider a general family of decision rules. For this family, we show that there is no advantage of using a non-linear decision rule, if the goal is to find the shortest or the minimum leakage path. We also show that bidirectional flow is necessary for convergence to such paths. Our results provide a plausible explanation for field observations, and open up new avenues for further theoretical and experimental investigation. 
    more » « less
  3. Ants are millimetres in scale yet collectively create metre-scale nests in diverse substrates. To discover principles by which ant collectives self-organize to excavate crowded, narrow tunnels, we studied incipient excavation in small groups of fire ants in quasi-two-dimensional arenas. Excavation rates displayed three stages: initially excavation occurred at a constant rate, followed by a rapid decay, and finally a slower decay scaling in time as t −1/2 . We used a cellular automata model to understand such scaling and motivate how rate modulation emerges without global control. In the model, ants estimated their collision frequency with other ants, but otherwise did not communicate. To capture early excavation rates, we introduced the concept of ‘agitation’—a tendency of individuals to avoid rest if collisions are frequent. The model reproduced the observed multi-stage excavation dynamics; analysis revealed how parameters affected features of multi-stage progression. Moreover, a scaling argument without ant–ant interactions captures tunnel growth power-law at long times. Our study demonstrates how individual ants may use local collisional cues to achieve functional global self-organization. Such contact-based decisions could be leveraged by other living and non-living collectives to perform tasks in confined and crowded environments. 
    more » « less
  4. Animals are often faced with time-critical decisions without prior information about their actions’ outcomes. In such scenarios, individuals budget their investment into the task to cut their losses in case of an adverse outcome. In animal groups, this may be challenging because group members can only access local information, and consensus can only be achieved through distributed interactions among individuals. Here, we combined experimental analyses with theoretical modeling to investigate how groups modulate their investment into tasks in uncertain conditions. Workers of the arboreal weaver ant Oecophylla smaragdina form three-dimensional chains using their own bodies to bridge vertical gaps between existing trails and new areas to explore. The cost of a chain increases with its length because ants participating in the structure are prevented from performing other tasks. The payoffs of chain formation, however, remain unknown to the ants until the chain is complete and they can explore the new area. We demonstrate that weaver ants cap their investment into chains, and do not form complete chains when the gap is taller than 90 mm. We show that individual ants budget the time they spend in chains depending on their distance to the ground, and propose a distance-based model of chain formation that explains the emergence of this tradeoff without the need to invoke complex cognition. Our study provides insights into the proximate mechanisms that lead individuals to engage (or not) in collective actions and furthers our knowledge of how decentralized groups make adaptive decisions in uncertain conditions. 
    more » « less
  5. Abstract

    Bacterial symbionts are known to facilitate a wide range of physiological processes and ecological interactions for their hosts. In spite of this, caterpillars with highly diverse life histories appear to lack resident microbiota. Gut physiology, endogenous digestive enzymes, and limited social interactions may contribute to this pattern, but the consequences of shifts in social activity and diet on caterpillar microbiota are largely unknown.Phengaris alconcaterpillars undergo particularly dramatic social and dietary shifts when they parasitizeMyrmicaant colonies, rapidly transitioning from solitary herbivory to ant tending (i.e., receiving protein‐rich regurgitations through trophallaxis). This unique life history provides a model for studying interactions between social living, diet, and caterpillar microbiota. Here, we characterized and compared bacterial communities withinPalconcaterpillars before and after their association with ants, using 16S rRNA amplicon sequencing and quantitative PCR. After being adopted by ants, bacterial communities withinP. alconcaterpillars shifted substantially, with a significant increase in alpha diversity and greater consistency in bacterial community composition in terms of beta dissimilarity. We also characterized the bacterial communities within their host ants (Myrmica schencki), food plant (Gentiana cruciata), and soil from ant nest chambers. These data indicated that the aforementioned patterns were influenced by bacteria derived from caterpillars’ surrounding environments, rather than through transfers from ants. Thus, while bacterial communities are substantially reorganized over the life cycle ofP. alconcaterpillars, it appears that they do not rely on transfers of bacteria from host ants to complete their development.

     
    more » « less