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

Yanagawa, Aya; Fujiwara-Tsujii, Nao; Akino, Toshiharu; Yoshimura, Tsuyoshi; Yanagawa, Takashi; Shimizu, Susumu

doi:10.1016/j.jip.2011.06.001

Cited by 32 publications

(34 citation statements)

References 18 publications

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“…In flies, specific olfactory receptors are devoted to the detection of harmful microbes (Stensmyr et al, 2012). In termites, we have shown that odors from pathogenic spores are detected by the olfactory system (Yanagawa et al, 2009) and that such odors trigger allo-grooming (Yanagawa et al, 2010, 2011, 2012). This opens the possibility that contact chemicals related to microbes could also trigger grooming in insects.…”

Section: Introductionmentioning

confidence: 99%

Hygienic grooming is induced by contact chemicals in Drosophila melanogaster

Yanagawa

Guigue

Marion-Poll

2014

Front. Behav. Neurosci.

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In social insects, grooming is considered as a behavioral defense against pathogen and parasite infections since it contributes to remove microbes from their cuticle. However, stimuli which trigger this behavior are not well characterized yet. We examined if activating contact chemoreceptive sensilla could trigger grooming activities in Drosophila melanogaster. We monitored the grooming responses of decapitated flies to compounds known to activate the immune system, e.g., dead Escherichia coli (Ec) and lipopolysaccharides (LPS), and to tastants such as quinine, sucrose, and salt. LPS, quinine, and Ec were quite effective in triggering grooming movements when touching the distal border of the wings and the legs, while sucrose had no effect. Contact chemoreceptors are necessary and sufficient to elicit such responses, as grooming could not be elicited by LPS in poxn mutants deprived of external taste sensilla, and as grooming was elicited by light when a channel rhodopsin receptor was expressed in bitter-sensitive cells expressing Gr33a. Contact chemoreceptors distributed along the distal border of the wings respond to these tastants by an increased spiking activity, in response to quinine, Ec, LPS, sucrose, and KCl. These results demonstrate for the first time that bacterial compounds trigger grooming activities in D. melanogaster, and indicate that contact chemoreceptors located on the wings participate in the detection of such chemicals.

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Section: Introductionmentioning

confidence: 99%

Hygienic grooming is induced by contact chemicals in Drosophila melanogaster

Yanagawa

Guigue

Marion-Poll

2014

Front. Behav. Neurosci.

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“…Other reports, which suggested that more virulent isolates could repel termites more strongly [32], [33], also support this finding. On the other hand, an increase in grooming behavior induced by a musty odor occurred independent of virulence [34]. In addition, the termite aversion to fungal odor gradually increased with an increase in the conidia concentration in the high-virulence isolates of Beauveria and Isaria.…”

Section: Discussionmentioning

confidence: 91%

“…In addition, due to the new absorption method with a MonoTrap disc, we could collect more chemicals than with SPME [34]. In this analysis, no common volatile was associated with fungal virulence or species.…”

Section: Discussionmentioning

confidence: 99%

Odor Aversion and Pathogen-Removal Efficiency in Grooming Behavior of the Termite Coptotermes formosanus

et al. 2012

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The results of biocontrol with entomopathogens in termites have been discouraging because of the strong social hygiene behavior for removing pathogens from termite colonies. However, the mechanism of pathogen detection is still unclear. For the successful application of biopesticides to termites in nature, it would be beneficial to identify substances that could disrupt the termite’s ability to perceive pathogens. We hypothesized that termites can perceive pathogens and this ability plays an important role in effective hygiene behavior. In this study, pathogen-detection in the subterranean termite Coptotermes formosanus was investigated. We performed quantitative assays on conidia removal by grooming behavior using epifluoresence microscopy and Y-maze tests to examine the perception of fungal odor by termites. Three species each of high- and low-virulence entomopathogenic fungi were used in each test. The results demonstrated that termites removed conidia more effectively from a nestmate’s cuticle if its odor elicited stronger aversion. Highly virulent pathogens showed higher attachment rates to termite surfaces and their odors were more strongly avoided than those of low-virulence isolates in the same species. Moreover, termites appeared to groom each other more persistently when they had more conidia on their bodies. In brief, insect perception of pathogen-related odor seems to play a role in the mechanism of their hygiene behavior.

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“…The VOCs of Metarhizium and other fungi are repellents for several invertebrates including store grain pests ( Sitophilus zeamais Motschulsky) , and termites ( Coptotermes formosanus Shiraki) . Repellency is dependent upon the target since some insects are tolerant of higher quantities than others.…”

Section: Discussionmentioning

confidence: 99%

“…[21][22][23] Most notable are 1-octen-3-ol, 3-octanone and 1-octene, which are produced by a wide range of fungi including saprophytic molds, mushrooms and entomopathogenic fungi including species of Beauveria and Metarhizium. [24][25][26][27][28] Exactly why entomopathogenic fungi produce these compounds is unclear but the fact that so many insects exhibit avoidance behavior suggest that they are responding to VOCs. 20,29 This paper reports that these compounds are highly repellent or toxic to slugs and snails.…”

Section: Introductionmentioning

confidence: 99%

Fungal volatile organic compounds show promise as potent molluscicides

Khoja

Eltayef

Baxter³

et al. 2019

Pest Management Science

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BACKGROUND Slugs and snails constitute major crop pests. Withdrawal of metaldehyde has prompted a search for more environmentally friendly yet fast acting molluscicides. This study investigated the response of representative molluscs to conidia and volatile organic compounds (VOCs) of the insect pathogenic fungus Metarhizium brunneum Petch. RESULTS Conidia of M. brunneum had antifeedant/repellent properties with repellency being dependent upon the fungal strain and conidia concentration. Three commonly produced fungal VOCs, 1‐octene, 3‐octanone and 1‐octen‐3‐ol, were repellent at low doses (1–5 μL) but could kill slugs and snails on contact or fumigation. At the highest dose tested (10 μL), 100% mortality was achieved for Cornu aspersum Muller (garden snail) and Derocerus reticulatum Muller (grey field slug) within 1 h post‐treatment with the first deaths being recorded in <11 min. Aqueous formulations (20% v/v) of the most potent VOCs, 3‐octanone and 1‐octen‐3‐ol, could be sprayed onto plants to kill or drive the pest of the crop with no phytotoxic effects. CONCLUSION The sensitivity of terrestrial molluscs to 3‐octanone and 1‐octen‐3‐ol and the ephemeral nature of these compounds makes these excellent candidates for development as mollusc repellents or molluscicides. © 2019 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

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

Cited by 32 publications

References 18 publications

Hygienic grooming is induced by contact chemicals in Drosophila melanogaster

Hygienic grooming is induced by contact chemicals in Drosophila melanogaster

Odor Aversion and Pathogen-Removal Efficiency in Grooming Behavior of the Termite Coptotermes formosanus

Fungal volatile organic compounds show promise as potent molluscicides

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