A mechanistic, stigmergy model of territory formation in asocial animals: Territorial behavior can dampen disease prevalence but increase persistence

Abstract

Mechanistic portrayals of how animals form and maintain territories remain rare, and as a discipline, collective movement ecology has tended to focus on synergistic (e.g., migration, shoaling) rather than agonistic or territorial interactions. Here we ask how dynamic territory formation and maintenance might contribute to disease dynamics in an asocial territorial animal for an indirectly transmitted pathogen. We developed a mechanistic individual-based model where stigmergy-the deposition of signals into the environment (e.g., scent marking, scraping)-dictates not only local movement choices and long-term territory formation, but also the risk of pathogen transmission. Based on a variable importance analysis, the length of the infectious period was the single most important variable in predicting outbreak success, maximum prevalence, and outbreak duration. Population size and rate of pathogen decay were also key predictors. We found that territoriality best reduced maximum prevalence in conditions where we would otherwise expect outbreaks to be most successful: slower recovery rates (i.e., longer infectious periods) and higher conspecific densities. However, at high enough densities, outbreak duration became considerably more variable. Our findings therefore support a limited version of the "territoriality benefits" hypothesis-where reduced home range overlap leads to reduced opportunities for pathogen transmission, but with the caveat that reduction in outbreak severity may increase the likelihood of pathogen persistence. For longer infectious periods and higher host densities, key trade-offs emerged between the strength of pathogen load, strength of the stigmergy cue, and the rate at which those two quantities decayed; this finding raises interesting questions about the evolutionary nature of these competing processes and the role of possible feedbacks between parasitism and territoriality. This work also highlights the importance of considering social cues as part of the movement landscape in order to improve our understanding of the consequences of individual behaviors on population level outcomes. 2 Author summaryMaking decisions about conservation and disease management relies on our understanding of what allows animal populations to be successful. However, movement ecology, as a field, tends to focus on how animals respond to their abiotic environment. Similarly, disease ecology often focuses on the social behavior of animals without accounting for their individual movement patterns. We developed a simulation model that bridges these two fields by allowing hosts to inform their movement based on the past trajectories of other hosts. As hosts navigate their environment, they leave behind a scent trail while avoiding the scent trails of other individuals. We wanted to know if this means of territory formation could heighten or dampen disease spread when infectious hosts leave pathogens in their wake. We found that territoriality could inhibit disease spread under conditions that we would normally expect ...