Fungal Garden Making inside Bamboos by a Non-Social Fungus-Growing Beetle

Wataru Toki,Yukiko Takahashi,Katsumi Togashi,Judith Korb

doi:10.1371/journal.pone.0079515

Abstract

In fungus-growing mutualism, it is indispensable for host animals to establish gardens of the symbiotic fungus as rapidly as possible. How to establish fungal gardens has been well-documented in social fungus-farming insects, whereas poorly documented in non-social fungus-farming insects. Here we report that the non-social, fungus-growing lizard beetle Doubledaya bucculenta (Coleoptera: Erotylidae: Languriinae) transmits the symbiotic yeast Wickerhamomyces anomalus from the ovipositor-associated mycangium into bamboo internode cavities and disperses the yeast in the cavities to make gardens. Microbial isolation and cryo-scanning electron microscopy observation revealed that W. anomalus was constantly located on the posterior ends of eggs, where larvae came out, and on the inner openings of oviposition holes. Direct observation of oviposition behavior inside internodes revealed that the distal parts of ovipositors showed a peristaltic movement when they were in contact with the posterior ends of eggs. Rearing experiments showed that W. anomalus was spread much more rapidly and widely on culture media and internodes in the presence of the larvae than in the absence. These results suggest that the ovipositors play a critical role in vertical transmission of W. anomalus and that the larvae contribute actively to the garden establishment, providing a novel case of fungal garden founding in non-social insect-fungus mutualism.

Highlights

In a mutualism where a host animal depends obligately on a symbiont, it is critically important to manage and inherit the symbiont
At the highest level of cultivation mutualism observed in social insects such as ants, termites, and ambrosia beetles, the host adults directly promote the construction of a fungal garden by inoculation as well as reinoculation of suitable substrate with symbiotic fungi [1,2,3,4,5,6]
This study demonstrated that (i) the symbiotic yeast cells were consistently present at the posterior ends of eggs and on the edges of the inner openings of D. bucculenta oviposition holes, (ii) the ovipositors of D. bucculenta showed peristaltic movement when they were in contact with the posterior ends of the eggs, (iii) newly hatched larvae, which came out of the posterior ends of eggs, acquired the yeast cells from the egg surface and dispersed them in the internode cavities, and (iv) the symbiotic yeast was spread much faster and wider on culture media and in the bamboo internode when a D. bucculenta larva was present than when it was absent

Summary

Introduction

In a mutualism where a host animal depends obligately on a symbiont, it is critically important to manage and inherit the symbiont. At the highest level of cultivation mutualism observed in social insects such as ants, termites, and ambrosia beetles, the host adults directly promote the construction of a fungal garden by inoculation as well as reinoculation of suitable substrate with symbiotic fungi [1,2,3,4,5,6]. In cultivation mutualism exhibited by nonsocial organisms such as a marine snail [7], several damselfish species [8], a slime mold [9], and several insects [10,11,12,13,14,15], we have poorly understood to what extent farmers contribute to garden making and management of cultivars. Fungal inoculation is due to the ovipositor-associated mycangium directly onto the oviposition substrate

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