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.

The Effects of Trichoderma Fungi on the Tunneling, Aggregation, and Colony-Initiation Preferences of Black-Winged Subterranean Termites, Odontotermes formosanus (Blattodea: Termitidae)

“…In addition, termites rely on altered behaviors to protect themselves from microbial pathogens. For example, the odor of entomopathogenic fungi has been shown to trigger alarm responses [7,8], grooming [8][9][10][11], attacking and cannibalism [12], cadaver burying [13], and spatial avoidance [14][15][16][17] in termites. These anti-pathogen responses, referred as "behavioral immunity" or "social immunity," have received increasing attention in recent years [18][19][20][21].…”

Inhibition of a Secreted Immune Molecule Interferes With Termite Social Immunity

“…The data from the current study suggest that while GNBP-2 is unlikely to be the main mechanism by which termites detect fungal PAMPs, its activity can nonetheless influence collective behavior once the host has become sick, potentially via the release of fungal PAMPs from damaged host cuticle. It is possible that GNBP-2 inhibition does not strongly discourage grooming because termites could employ a variety of host and/or pathogen-derived signals, involving behavioral, chemical or even oscillatory cues (e.g., body vibrations) to initiate collective defense tasks (Rosengaus et al, 1999;Wilson-Rich et al, 2007;Zhukovskaya et al, 2013;Davis et al, 2018;Bulmer et al, 2019). In this scenario, although GNBP-2 activity may itself accelerate the transition from a caring to a killing response, it represents just one component of a complex repertoire of social immune mechanisms that termites could use to regulate infectious threats exposed to the colony.…”

“…This may help to explain why epizootics that can kill entire social insect colonies are in fact quite rare (Chouvenc and Su, 2012;Schmid-Hempel, 2017). Social insect individuals are able to limit infection using their individual immune systems (Cotter and Kilner, 2010;Meunier, 2015) but they have also evolved a variety of collective disease defenses to mitigate the occurrence and dissemination of infectious diseases (Cremer et al, 2007;Wilson-Rich et al, 2009) including both behavioral and physiological adaptations (Cremer et al, 2018;Bulmer et al, 2019;Liu et al, 2019). Social actions resulting in the control or elimination of infections are examples of "social immunity."…”

“…In ants, termites as well as other social insect groups, behavioral defenses can be supplemented with the secretion and spread of antimicrobial substances onto body surfaces, where they function as a potent external disinfectants (Hamilton et al, 2011;López-Riquelme and Fanjul-Moles, 2013;Otti et al, 2014;He et al, 2018;Pull et al, 2018). Termites in particular can deploy a wide repertoire of social immune responses including alarm behaviors, avoidance, prophylactic, or antimicrobial secretions, burial of dead bodies, necrophagy, mutual grooming, and cannibalism (Rosengaus et al, 1998(Rosengaus et al, , 1999(Rosengaus et al, , 2011Yanagawa and Shimizu, 2007;Chouvenc et al, 2008;Chouvenc and Su, 2010;He et al, 2018;Bulmer et al, 2019). Antimicrobial secretions in termites are produced by sternal as well as head glands, and can include antimicrobial compounds found in rectal fluids and feces (Rosengaus et al, 2011;Bulmer et al, 2019).…”

“…Termites in particular can deploy a wide repertoire of social immune responses including alarm behaviors, avoidance, prophylactic, or antimicrobial secretions, burial of dead bodies, necrophagy, mutual grooming, and cannibalism (Rosengaus et al, 1998(Rosengaus et al, , 1999(Rosengaus et al, , 2011Yanagawa and Shimizu, 2007;Chouvenc et al, 2008;Chouvenc and Su, 2010;He et al, 2018;Bulmer et al, 2019). Antimicrobial secretions in termites are produced by sternal as well as head glands, and can include antimicrobial compounds found in rectal fluids and feces (Rosengaus et al, 2011;Bulmer et al, 2019).…”