Musty odor of entomopathogens enhances disease-prevention behaviors in the termite Coptotermes formosanus

Abstract

Termites often eliminate pathogens directly through mutual grooming, and are thereby prevent infections from entomopathogenic fungi. Our previous study confirmed that the antennae of Coptotermes formosanus sensitively responded to the musty odor of entomopathogenic fungi. However, it is unclear if this odor has any effect on termite behavior. The purpose of this study was to clarify the effects of fungal odor on termite behavior, especially on conidia removal. The musty odor was prepared as an aqueous solution by immersing conidia in distilled water. When untreated termites were mixed with fungal-odor-treated termites at a ratio of 4:1, mutual grooming and attack of treated termites were frequently observed. This indicated that the fungal odor triggered these behavioral responses. While some components of the fungal odor were found in all of the entomopathogenic fungi tested, the odor profiles differed among the isolates.

Introduction

Hygiene behavior plays a key role in insect prevention against pathogens (Oi and Pereira, 1993, Swanson et al., 2009). Mutual grooming behavior, which has been well studied in termites, is a typical hygiene behavior (Kramm and West, 1982, Boucias et al., 1996, Shimizu and Yamaji, 2003). Through mutual grooming, termite workers ingest fungal conidia on the cuticle of a nestmate with the glossae and dispose of them through their alimentary tract (Yanagawa and Shimizu, 2007, Chouvenc et al., 2009). When together with nestmates, mutual grooming reduces the chances of termites getting infected by entomopathogenic fungi. This aspect of termite behavior is one of the key reasons that control of termite populations with entomopathogenic fungi had so far only limited if any effect. Since such biological approaches are an environment-friendly alternative to the current chemical control (Verma et al., 2009), it is important to identify the cues that induce termite hygiene behavior. Although microbes vary greatly with regard to competitive strength, attachment pattern, germination ability, environmental adaptability, and so on (Clarkson and Charnley, 1996), it is not yet clear what cues lead termites to notice the presence of entomopathogenic fungi on the cuticle of their nestmates.

Termite hygiene behaviors are most likely triggered by chemical information, since most termites are blind. Recent studies have revealed that termite antennae sensitively respond to the musty odors of entomopathogenic fungi (Yanagawa et al., 2009, Yanagawa et al., 2010). To understand the role played by chemical perception in Coptotermes formosanus behavior, we investigated whether odor from entomopathogenic fungi may be the cue that induces termite hygiene behavior. We report here the results from a laboratory study.