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Fungal garden making inside bamboos by a non-social fungus-growing beetle.

Toki W, Takahashi Y, Togashi K - PLoS ONE (2013)

Bottom Line: In fungus-growing mutualism, it is indispensable for host animals to establish gardens of the symbiotic fungus as rapidly as possible.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Forest Science, Graduate School of Agricultural and Life Sciences, the University of Tokyo, Bunkyo, Tokyo, Japan.

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.

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Effects of Doubledaya bucculenta larvae on the dispersal of Wickerhamomyces anomalus yeast cells.(A) A W. anomalus colony formed by the cells that were inoculated in the center of a potato dextrose agar (PDA) plate in the absence of a D. bucculenta larva. (B) W. anomalus colonies formed by the cells that were inoculated in the center of a PDA plate in the presence of a D. bucculenta larva. (C) No W. anomalus colony formation on an autoclaved Pleioblastus simonii internode strip where a yeast-inoculated dead egg of D. bucculenta was placed. (D) W. anomalus colonies formed on an autoclaved P. simonii internode strip where a yeast-inoculated living egg of D. bucculenta was placed. PDA Plates and internode strips were photographed three and four days after the incubation at 25 °C, respectively. White and black arrows indicate a first instar larva of D. bucculenta and a place where a yeast-inoculated egg of D. bucculenta was placed, respectively. Arrowheads indicate the yeast colonies. Abbreviation: e, egg.
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pone-0079515-g004: Effects of Doubledaya bucculenta larvae on the dispersal of Wickerhamomyces anomalus yeast cells.(A) A W. anomalus colony formed by the cells that were inoculated in the center of a potato dextrose agar (PDA) plate in the absence of a D. bucculenta larva. (B) W. anomalus colonies formed by the cells that were inoculated in the center of a PDA plate in the presence of a D. bucculenta larva. (C) No W. anomalus colony formation on an autoclaved Pleioblastus simonii internode strip where a yeast-inoculated dead egg of D. bucculenta was placed. (D) W. anomalus colonies formed on an autoclaved P. simonii internode strip where a yeast-inoculated living egg of D. bucculenta was placed. PDA Plates and internode strips were photographed three and four days after the incubation at 25 °C, respectively. White and black arrows indicate a first instar larva of D. bucculenta and a place where a yeast-inoculated egg of D. bucculenta was placed, respectively. Arrowheads indicate the yeast colonies. Abbreviation: e, egg.

Mentions: When the yeast cells alone were placed in the centers of five PDA plates, a yeast colony roundly expanded within a limited area in the center (mean ± standard deviation of colony diameter = 3.5 ± 0.3 mm, n = 5) in three days (Figure 4A). By contrast, when four first instar larvae (mean ± standard deviation of body mass of 3-day-old larvae = 0.5 ± 0.1 mg, n = 4) were individually placed on PDA plates with the yeast cells inoculated in the center, abundant yeast colonies occurred along the larval wandering tracks on three PDA plates in three days (mean ± standard deviation of body mass of 7-day-old larvae = 1.2 ± 0.4 mg, n = 3) (Figure 4B), whereas a small, round yeast colony occurred in the center of the remaining PDA plate because a released larva did not visit an area with yeast cells inoculated due to injured legs (colony diameter after three days, 3.1 mm; body mass of 7-day-old larva, 0.5 mg).


Fungal garden making inside bamboos by a non-social fungus-growing beetle.

Toki W, Takahashi Y, Togashi K - PLoS ONE (2013)

Effects of Doubledaya bucculenta larvae on the dispersal of Wickerhamomyces anomalus yeast cells.(A) A W. anomalus colony formed by the cells that were inoculated in the center of a potato dextrose agar (PDA) plate in the absence of a D. bucculenta larva. (B) W. anomalus colonies formed by the cells that were inoculated in the center of a PDA plate in the presence of a D. bucculenta larva. (C) No W. anomalus colony formation on an autoclaved Pleioblastus simonii internode strip where a yeast-inoculated dead egg of D. bucculenta was placed. (D) W. anomalus colonies formed on an autoclaved P. simonii internode strip where a yeast-inoculated living egg of D. bucculenta was placed. PDA Plates and internode strips were photographed three and four days after the incubation at 25 °C, respectively. White and black arrows indicate a first instar larva of D. bucculenta and a place where a yeast-inoculated egg of D. bucculenta was placed, respectively. Arrowheads indicate the yeast colonies. Abbreviation: e, egg.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3818229&req=5

pone-0079515-g004: Effects of Doubledaya bucculenta larvae on the dispersal of Wickerhamomyces anomalus yeast cells.(A) A W. anomalus colony formed by the cells that were inoculated in the center of a potato dextrose agar (PDA) plate in the absence of a D. bucculenta larva. (B) W. anomalus colonies formed by the cells that were inoculated in the center of a PDA plate in the presence of a D. bucculenta larva. (C) No W. anomalus colony formation on an autoclaved Pleioblastus simonii internode strip where a yeast-inoculated dead egg of D. bucculenta was placed. (D) W. anomalus colonies formed on an autoclaved P. simonii internode strip where a yeast-inoculated living egg of D. bucculenta was placed. PDA Plates and internode strips were photographed three and four days after the incubation at 25 °C, respectively. White and black arrows indicate a first instar larva of D. bucculenta and a place where a yeast-inoculated egg of D. bucculenta was placed, respectively. Arrowheads indicate the yeast colonies. Abbreviation: e, egg.
Mentions: When the yeast cells alone were placed in the centers of five PDA plates, a yeast colony roundly expanded within a limited area in the center (mean ± standard deviation of colony diameter = 3.5 ± 0.3 mm, n = 5) in three days (Figure 4A). By contrast, when four first instar larvae (mean ± standard deviation of body mass of 3-day-old larvae = 0.5 ± 0.1 mg, n = 4) were individually placed on PDA plates with the yeast cells inoculated in the center, abundant yeast colonies occurred along the larval wandering tracks on three PDA plates in three days (mean ± standard deviation of body mass of 7-day-old larvae = 1.2 ± 0.4 mg, n = 3) (Figure 4B), whereas a small, round yeast colony occurred in the center of the remaining PDA plate because a released larva did not visit an area with yeast cells inoculated due to injured legs (colony diameter after three days, 3.1 mm; body mass of 7-day-old larva, 0.5 mg).

Bottom Line: In fungus-growing mutualism, it is indispensable for host animals to establish gardens of the symbiotic fungus as rapidly as possible.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Forest Science, Graduate School of Agricultural and Life Sciences, the University of Tokyo, Bunkyo, Tokyo, Japan.

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.

Show MeSH
Related in: MedlinePlus