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

Xiong Xiong,Liang Liang,Chen Chen,Wang Wang,Wen Wen,Cai Cai

doi:10.3390/f10111020

Xiong Xiong, Liang Liang + Show 4 more

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https://doi.org/10.3390/f10111020

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Abstract

The black-winged subterranean termite, Odontotermes formosanus Shiraki, is a severe pest of plantations and forests in China. This termite cultures symbiotic Termitomyces in the fungal combs, which are challenged by antagonistic microbes such as Trichoderma fungi. In a previous study we showed that O. formosanus workers made significantly fewer tunnels in sand containing commercially formulated conidia of Trichoderma viride Pers. ex Fries compared with untreated sand. Herein, we hypothesize that fungi in the genus Trichoderma exert repellent effects on O. formosanus. Different choice tests were conducted to evaluate the tunneling and aggregation behaviors of O. formosanus workers reacting to sand/soil containing the unformulated conidia of seven Trichoderma fungi (Trichoderma longibrachiatum Rifai, Trichoderma koningii Oud., Trichoderma harzianum Rifai, Trichoderma hamatum (Bon.) Bain, Trichoderma atroviride Karsten, Trichoderma spirale Indira and Kamala, and T. viride). We also investigated the colony-initiation preference of paired O. formosanus adults to soil treated with Trichoderma conidia (T. koningii or T. longibrachiatum) versus untreated soil. Tunneling-choice tests showed that sand containing conidia of nearly all Trichoderma fungi tested (except T. harzianum) significantly decreased tunneling activity in O. formosanus workers compared with untreated sand. Aggregation-choice test showed that T. koningii, T. atroviride and T. spirale repelled O. formosanus workers, whereas T. longibrachiatum and T. hamatum attracted termites. There was no significant difference in proportions of paired adults that stayed and laid eggs in the soil blocks treated with conidia of Trichoderma fungi and untreated ones. Our study showed that Trichoderma fungi generally repelled tunneling in O. formosanus, but may exert varied effects on aggregation preference by workers.

Highlights

Termites are eusocial insects that feed on various types of cellulose
We showed that O. formosanus workers made significantly shorter tunnels in the sand containing commercially formulated conidia of Trichoderma viride Pers. ex Fries than in untreated sand [29], which provided the first evidence of “spatial avoidance” performed by fungus-growing higher termites responding to an antagonistic fungus against Termitomyces
We found that O. formosanus workers made significantly fewer tunnels in sand containing conidia of six Trichoderma fungi (T. longibrachiatum, T. koningii, T. hamatum, T. atroviride, T. viride, and T. spirale) compared with untreated soil

Summary

Introduction

Termites are eusocial insects that feed on various types of cellulose. Based on foraging habitat or foraging environment, termites can be categorized into three types: (1) subterranean termites, which include wood-feeding lower termites and fungus-growing higher termites that construct underground nests or above-ground mounds attached the soil; (2) drywood termites, which live in and feed on dry wood above the soil levels; and (3) dampwood termites, which nest in the rotting wood with highForests 2019, 10, 1020; doi:10.3390/f10111020 www.mdpi.com/journal/forestsForests 2019, 10, 1020 moisture content. 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]

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