Fungal artillery of zombie flies: infectious spore dispersal using a soft water cannon

Jolet de Ruiter, Sif Fink Arnbjerg-Nielsen, Pascal Herren, Freja Høier, Henrik H. De Fine Licht, Kaare H. Jensen*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Dead sporulating female fly cadavers infected by the house fly-pathogenic fungus Entomophthora muscae are attractive to healthy male flies, which by their physical inspection may mechanically trigger spore release and by their movement create whirlwind airflows that covers them in infectious conidia. The fungal artillery of E. muscae protrudes outward from the fly cadaver, and consists of a plethora of micrometric stalks that each uses a liquid-based turgor pressure build-up to eject a jet of protoplasm and the initially attached spore. The biophysical processes that regulate the release and range of spores, however, are unknown. To study the physics of ejection, we design a biomimetic 'soft cannon' that consists of a millimetric elastomeric barrel filled with fluid and plugged with a projectile. We precisely control the maximum pressure leading up to the ejection, and study the cannon efficiency as a function of its geometry and wall elasticity. In particular, we predict that ejection velocity decreases with spore size. The calculated flight trajectories under aerodynamic drag predict that the minimum spore size required to traverse a quiescent layer of a few millimetres around the fly cadaver is approximately 10 µm. This corroborates with the natural size of E. muscae conidia (approx. 27 µm) being large enough to traverse the boundary layer but small enough (less than 40 µm) to be lifted by air currents. Based on this understanding, we show how the fungal spores are able to reach a new host.

Original languageEnglish
Article number20190448
Number of pages10
JournalJournal of the Royal Society, Interface
Volume16
Issue number159
DOIs
Publication statusPublished - 31 Oct 2019

Fingerprint

Spores
Diptera
Fungal Spores
Aerodynamic drag
Cadaver
Water
Biomimetics
Projectiles
Fungi
Elasticity
Boundary layers
Physics
Inspection
Trajectories
Biophysical Phenomena
Entomophthora
Fluids
Geometry
Liquids
Pressure

Keywords

  • biomimetic soft cannon
  • dispersal range
  • Entomophthora muscae
  • force-balance model
  • fungal spore ejection
  • high-speed videography

Cite this

de Ruiter, J., Arnbjerg-Nielsen, S. F., Herren, P., Høier, F., De Fine Licht, H. H., & Jensen, K. H. (2019). Fungal artillery of zombie flies: infectious spore dispersal using a soft water cannon. Journal of the Royal Society, Interface, 16(159), [20190448]. https://doi.org/10.1098/rsif.2019.0448
de Ruiter, Jolet ; Arnbjerg-Nielsen, Sif Fink ; Herren, Pascal ; Høier, Freja ; De Fine Licht, Henrik H. ; Jensen, Kaare H. / Fungal artillery of zombie flies: infectious spore dispersal using a soft water cannon. In: Journal of the Royal Society, Interface. 2019 ; Vol. 16, No. 159.
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de Ruiter, J, Arnbjerg-Nielsen, SF, Herren, P, Høier, F, De Fine Licht, HH & Jensen, KH 2019, 'Fungal artillery of zombie flies: infectious spore dispersal using a soft water cannon', Journal of the Royal Society, Interface, vol. 16, no. 159, 20190448. https://doi.org/10.1098/rsif.2019.0448

Fungal artillery of zombie flies: infectious spore dispersal using a soft water cannon. / de Ruiter, Jolet; Arnbjerg-Nielsen, Sif Fink; Herren, Pascal; Høier, Freja; De Fine Licht, Henrik H.; Jensen, Kaare H.

In: Journal of the Royal Society, Interface, Vol. 16, No. 159, 20190448, 31.10.2019.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - de Ruiter, Jolet

AU - Arnbjerg-Nielsen, Sif Fink

AU - Herren, Pascal

AU - Høier, Freja

AU - De Fine Licht, Henrik H.

AU - Jensen, Kaare H.

PY - 2019/10/31

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AB - Dead sporulating female fly cadavers infected by the house fly-pathogenic fungus Entomophthora muscae are attractive to healthy male flies, which by their physical inspection may mechanically trigger spore release and by their movement create whirlwind airflows that covers them in infectious conidia. The fungal artillery of E. muscae protrudes outward from the fly cadaver, and consists of a plethora of micrometric stalks that each uses a liquid-based turgor pressure build-up to eject a jet of protoplasm and the initially attached spore. The biophysical processes that regulate the release and range of spores, however, are unknown. To study the physics of ejection, we design a biomimetic 'soft cannon' that consists of a millimetric elastomeric barrel filled with fluid and plugged with a projectile. We precisely control the maximum pressure leading up to the ejection, and study the cannon efficiency as a function of its geometry and wall elasticity. In particular, we predict that ejection velocity decreases with spore size. The calculated flight trajectories under aerodynamic drag predict that the minimum spore size required to traverse a quiescent layer of a few millimetres around the fly cadaver is approximately 10 µm. This corroborates with the natural size of E. muscae conidia (approx. 27 µm) being large enough to traverse the boundary layer but small enough (less than 40 µm) to be lifted by air currents. Based on this understanding, we show how the fungal spores are able to reach a new host.

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KW - dispersal range

KW - Entomophthora muscae

KW - force-balance model

KW - fungal spore ejection

KW - high-speed videography

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