Pathogen-mediated natural and manipulated population collapse in an invasive social insect

Boom-bust population dynamics are a recurrent, widespread, and typically unexplained property of many species invasions. Declines also occur in invasive social insects from unknown causes. Nevertheless, social insects have proved intractable to biological control. Tawny crazy ants, an environmentally damaging invasive pest in several countries globally, are spreading in North America. Examining 15 local populations spanning 9 y, we document both the collapse of local populations of this ant in North America and a strong association of collapse with infection by the microsporidian pathogen, Myrmecomorba nylanderiae. Over the observation period, all longitudinally sampled local populations that harbored the pathogen declined, with 62% of these populations disappearing entirely. We test the causality of this relationship by introducing this pathogen into two local populations. At both sites, within 7 mo the pathogen was nearly universally prevalent, and within 2 y, tawny crazy ants were eliminated. In contrast, uninfected populations showed no tendency to decline over a similar period. Concurrent laboratory studies indicate that colony fragments died out because infected workers do not survive long enough to bridge the gap created by normal, winter cessation of immature ant production. Population-level collapse occurred because the pathogen spread faster than colony fragments declined, eliminating the density-dependent regulation seen with many pathogens. Invasive species beset by such pathogens may collapse if factors favoring transmission, like genetic homogeneity, high population density, or socially facilitated intragroup transmission, allow virulent pathogens to spread widely before disease impacts occur. These invasive species may be susceptible to boom-bust dynamics and pathogen-driven local extinction.

Automated summary

Boom-bust population dynamics are a common feature of species invasions, but the reasons behind it are usually unexplained. Invasive social insects also experience population declines, but they have been resistant to biological control. This study found a strong association between the collapse of local populations of tawny crazy ants in North America and infection by a microsporidian pathogen. Infected populations declined and even disappeared, while uninfected populations showed no decline. Laboratory studies showed that infected workers could not survive the winter cessation of immature ant production, leading to population-level collapse. The rapid spread of the pathogen eliminated density-dependent regulation. This study suggests that invasive species with high transmission rates of virulent pathogens may be susceptible to boom-bust dynamics and pathogen-driven local extinction.