Regulation of Harvester Ant Foraging as a Closed-Loop Excitable System

Abstract

Ant colonies regulate activity in response to changing conditions without using centralized control. Harvester ant colonies forage in the desert for seeds, and their regulation of foraging manages a tradeoff between spending and obtaining water. Foragers lose water while outside in the dry air, but the colony obtains water by metabolizing the fats in the seeds they eat. Previous work shows that the rate at which an outgoing forager leaves the nest depends on its recent experience of brief antennal contact with returning foragers that carry a seed. We examine how this process can yield foraging rates that are robust to uncertainty and responsive to temperature and humidity across minutes to hour-long timescales. To explore possible mechanisms, we develop a low-dimensional analytical model with a small number of parameters that captures observed foraging behavior. The model uses excitability dynamics to represent response to interactions inside the nest and a random delay distribution to represent foraging time outside the nest. We show how feedback of outgoing foragers returning to the nest stabilizes the incoming and outgoing foraging rates to a common value determined by the "volatility" of available foragers. The model exhibits a critical volatility above which there is sustained foraging at a constant rate and below which there is cessation of foraging. To explain how the foraging rates of colonies adjust to temperature and humidity, we propose a mechanism that relies on foragers modifying their volatility after they leave the nest and get exposed to the environment. Our study highlights the importance of feedback in the regulation of foraging activity and points to modulation of volatility as a key to explaining differences in foraging activity in response to conditions and across colonies. Our results present opportunities for generalization to other contexts and systems with excitability and feedback across multiple timescales. Author SummaryWe investigate the collective behavior that allows colonies of desert harvester ants to 1 regulate foraging activity in response to environmental conditions. We develop an 2 analytical model connecting three processes: 1) the interactions between foragers 3 returning to the nest and available foragers waiting inside the nest, 2) the effect of these 4 interactions on the likelihood of available foragers to leave the nest to forage, and 3) the 5 return of foragers to the nest after finding seeds. We propose a mechanism in which 6 available foragers modify their response to interactions after their first exposure to the 7 PLOS 1/23 environment. We show how this leads to colony foraging rates that adjust to 8 environmental conditions over time scales from minutes to hours. Our model may prove 9 useful for studying resilience in other classes of systems with excitatory dynamics. 10 Introduction 11 Social insect colonies operate without central control. Colonies maintain coherence and 12 plasticity in the face of perturbation and change, even though individuals have limited 1...

Movement, Encounter Rate, and Collective Behavior in Ant Colonies

“…Colony differences in the regulation of foraging in response to dry conditions are associated with differences in the expression of genes related to dopamine ( Friedman et al 2020 ). A forager’s response to encounters appears to depend on its hydration status ( Friedman et al 2019 ), apparently influenced by the humidity conditions it experienced on its previous trip ( Pagliara et al 2018 ). In colonies that reduce foraging more when dry, workers are more sensitive to water loss ( Friedman et al 2019 ) which presumably influences how much encounters with returning foragers stimulate them to leave the nest on the next trip.…”