A biological hydraulic accumulator: How the squirting cucumber, Ecballium elaterium, squirts its seeds

TL;DR

The study addresses how Ecballium elaterium achieves rapid seed dispersal using a hydraulic accumulator. It combines microtomography, internal pressure sensing, and high-speed videography to quantify pod geometry, pressure time series, and seed-jet dynamics, revealing circadian and ultradian rhythms in pressure and a robust central-funiculus seed arrangement. The fruit wall stores elastic energy that is released upon detachment, producing a turbulent, particle-laden jet in which seeds reach velocities up to about $30$ m/s and spread over a broad dispersal cone, aided by wind and jet breakup. This work demonstrates a natural, energy-efficient dispersal strategy and offers insights with potential bioinspired applications in hydraulic-energy storage and jet dynamics for large particles in fluids.

Abstract

Seed dispersal is a fundamental process that allows offspring to reach suitable habitats and colonize new environments. While most plants rely on external vectors, some have evolved mechanisms that employ the buildup of liquid pressure in a closed compartment and its explosive release to disperse their seeds. This form of energy storage, reinvented by humans for engineering applications, is termed a hydraulic accumulator. Here we investigated the fluid mechanics involved in dispersal in the squirting cucumber, Ecballium elaterium integrating high-speed videography (up to 10 000 fps), microtomography, and internal pressure sensors. We recorded long-term pressure time series showing that E. elaterium exhibits circadian (24 hour) and ultradian (short-period) rhythms. Remarkably, the measurements revealed a lack of correlation between fruit and stem turgor; while the stem showed strong circadian cycles, the fruit often did not, suggesting isolated physiological processes in different tissues. The fruit's spongy wall tissue stores elastic potential energy as turgor pressure builds to nearly one atmosphere (92-99 kPa). Upon detachment, this energy is rapidly released to expel a turbulent, particle-laden liquid jet. Microtomography revealed that the seeds are packed around a central funiculus, a configuration that optimizes their exit through the basal orifice at velocities of up to 30 m/s. Seeds eventually move faster than the liquid droplets during the later stages of ejection as they shed their liquid coating. This sophisticated mechanism ensures a broad dispersal cone, effectively spreading offspring across space and environmental conditions.

Figures (13)

• Figure 1: Ecballium elaterium, from the large to the small scale: (a) field setup used to capture seed pod explosions; (b) squirting cucumber plants in flower; (c) ripe seed pods; (d) sequence showing explosion of seed pod.
• Figure 2: Tomography: transverse and longitudinal slices showing the disposition of seeds within the fruit.
• Figure 3: Tomography: 3D images. (a) Overall aspect; (b) Cut-away showing width of pressure vessel wall, (c) overall organization of seeds, and (d) showing the central funiculus.
• Figure 4: (e) (a--e) (upper panels) Pressure time series inside Ecballium elaterium fruits during their growth. Absolute pressure graphs (a--d) have been set to the same vertical scale to enable comparison; (e) is relative pressure. Midnight is marked by the dashed lines. (lower panels) Fourier and Welch spectra of the time series. The circadian (24h) peak is marked with a dashed line.
• Figure 5: Pressure measurements in the moment of explosion. a: Absolute pressure at the calyx end of the pod. b: Relative pressure measured at the same time in the stem above the fruit.