Regulation of harvester ant foraging as a closed-loop excitable system

• Published in: PLoS computational biology 2018-12, Vol.14 (12), p.e1006200-e1006200
• Main Authors: Pagliara, Renato, Gordon, Deborah M, Leonard, Naomi Ehrich
• Format: Article
• Language: English
• Subjects: Aerospace engineering; Animal cognition; Animal Communication; Animals; Ants; Ants - physiology; Behavior, Animal; Biology and Life Sciences; Colonies; Computer and Information Sciences; Computer Simulation; Desert environments; Deserts; Dimensional analysis; Earth Sciences; Ecology and Environmental Sciences; Engineering and Technology; Excitability; Fats; Feedback; Feeding Behavior - physiology; Food; Forage; Foraging behavior; Harvesters; Harvesting; Humidity; Mathematical models; Models, Biological; Neural networks; Neurosciences; Physical Sciences; Research and Analysis Methods; Seeds; Social Behavior; Social Sciences; Temperature; Volatility
• ISSN: 1553-7358; 1553-734X; 1553-7358
• DOI: 10.1371/journal.pcbi.1006200

Ant colonies regulate activity in response to changing conditions without using centralized control. Desert harvester ant colonies forage for seeds, and regulate foraging to manage a tradeoff between spending and obtaining water. Foragers lose water while outside in the dry air, but ants obtain 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 rate of brief antennal contacts with incoming foragers carrying food. We examine how this process can yield foraging rates that are robust to uncertainty and responsive to temperature and humidity across minute-to-hour 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 from 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 foraging stops. To explain how foraging rates adjust to temperature and humidity, we propose that foragers modify their volatility after they leave the nest and become exposed to the environment. Our study highlights the importance of feedback in the regulation of foraging activity and shows how modulation of volatility can explain how foraging activity responds to conditions and varies across colonies. Our model elucidates the role of feedback across many timescales in collective behavior, and may be generalized to other systems driven by excitable dynamics, such as neuronal networks.