Subterranean Termite Social Alarm and Hygienic Responses to Fungal Pathogens

Abstract

In social insects, alerting nestmates to the presence of a pathogen should be critical for limiting its spread and initiating social mechanisms of defense. Here we show that subterranean termites use elevated vibratory alarm behavior to help prevent fatal fungal infections. The elevated alarm leads to elevated social hygiene. This requires that termites coalesce so that they can groom each other's cuticular surfaces of contaminating conidial spores. Groups of 12 Reticulitermes flavipes workers varied in their response when immersed in conidia solutions of nine different strains of Metarhizium. Pathogen alarm displays of short 2-7-second bursts of rapid longitudinal oscillatory movement (LOM), observed over 12 min following a fungal challenge, were positively correlated with the time that workers spent aggregated together grooming each other. The frequency of these LOMs was inversely correlated with fatal fungal infections. The variation in fatalities appeared to be largely attributable to a differential response to Metarhizium brunneum and Metarhizium robertsii in the time spent in aggregations and the frequency of allogrooming. Isolated workers challenged with conidia did not display LOMs, which suggests that the alarm is a conditional social response. LOMs appear to help signal the presence of fungal pathogens whose virulence depends on the level of this emergency alert.

Keywords: Metarhizium; alarm behavior; allogrooming; entomopathogens; social immunity.

Figure 1

Workers exposed to a sporulating or control cadaver. For the left-hand side dish, arrow points to the sporulating cadaver. For the right-hand side dish, arrow points to the control cadaver (https://zenodo.org/record/3240589#.XPltDdNKgW8).

Figure 2

Hazard ratios of death relative to controls are predicted by the frequency of the pathogen alarm behavior (LOMs). Groups of 12 workers were challenged by brief immersion in the conidial suspensions of nine different strains of Metarhizium (for two colonies, n = 18). The strains corresponded with three different species. Open circles, M. brunneum; open squares, M. roberstsii; open triangles, M. guizhouense; solid circles, controls. The line of regression does not include controls. After controlling for colony effects, standardized β = −0.609, p = 0.008.

Figure 3

Hazard ratios of death relative to controls are predicted by the time workers spent in aggregations. Groups of 12 workers were challenged by brief immersion in the conidial suspensions of nine different strains of Metarhizium (for two colonies, n = 18). The strains corresponded with three different species. Open circles, M. brunneum; open squares, M. roberstsii; open triangles, M. guizhouense; solid circles, controls. The line of regression does not include controls. The time in seconds that workers spent in aggregations of greater than eight was log-transformed. After controlling for colony effects, standardized β = −0.580, p = 0.013.

Figure 4

Increased allogrooming is predicted by the time workers spent in aggregations. Groups of 12 workers were challenged by brief immersion in the conidial suspensions of nine different strains of Metarhizium (for two colonies, n = 18). The strains corresponded with three different species. Open circles, M. brunneum; open squares, M. roberstsii; open triangles, M. guizhouense; solid circles, controls. The line of regression does not include controls. The time in seconds spent in aggregations was log-transformed. After controlling for colony effects, standardized β = 0.615, p = 0.003.

Figure 5

The frequency of the alarm displays (LOMs) in response to different concentrations of conidia of M. brunneum (open circles) or M. robertsii (open squares).