Biomechanics of selected arborescent and shrubby monocotyledons

Main aims of the study are a deepened understanding of the mechanically relevant (ultra-)structures and the mechanical behaviour of various arborescent and shrubby monocotyledons and obtaining the structure–function relationships of different structurally conspicuous parts in Dracaena marginata stems. The stems of five different “woody” monocotyledon species were dissected and the mechanical properties of the most noticeable tissues in the five monocotyledons and, additionally, of individual vascular bundles in D. marginata, were tested under tensile stress. Results for Young’s moduli and density of these tissues were assessed as well as the area, critical strain, Young’s modulus and tensile strength of the vascular bundles in Dracaena marginata. These analyses allowed for generating a model for the mechanical interaction of tissues and vascular bundles of the stem in D. marginata as well as filling major “white spots” in property charts for biological materials. Additionally we shortly discuss the potential significance of such studies for the development of branched and unbranched bio-inspired fibre-reinforced materials and structures with enhanced properties

Scattering pattern of spores, sporangia and sporangium fragments.

<p>(A) Dissemination pattern of a single false indusium. The arrows indicate sporangial fragments or spore clumps. (B) Left images: Spore clumps observed during the experiments. Right images: Sporangial fragments with spores. (C) During recordings for kinematic analyses we often witnessed the detachment of whole sporangia from the respective false indusium (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0138495#pone.0138495.s014" target="_blank">S13 Video</a>).</p

False indusia on <i>A</i>. <i>peruvianum</i>.

<p>(A) A leaflet with several pinnules. (B) The false indusia are being developed on the underside of the pinnule. Several developmental stages of false indusia (note the colors) are shown. The lamina of older pinnules with open false indusia shows signs of degradation (lowermost image). (C) Mature false indusia open completely by desiccation and the exposed sporangia release their spores.</p

Non-mature and mature false indusia and supplying pinnule veinlets.

<p>(A) When non-mature false indusia desiccate (by cutting off the respective pinnule margins), they do not open completely but remain in a semi-open position. No spores become shed (see also <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0138495#pone.0138495.s002" target="_blank">S1 Video</a>). (B) View on the adaxial, marginal surface of a pinnule. The connection line between a false indusium, which is situated underneath the lamina, and the pinnule is indicated. The veinlets supplying the false indusium are clearly visible. (C) Details of some of the open and of some of the still closed false indusia after the desiccation experiment described in paragraph 3b). (D) Pinnules with open false indusia show signs of desiccation and degradation in the vicinity of the false indusia (indicated by the arrow).</p

Cellular changes taking place during desiccation of a false indusium.

<p>(A-B) LM transverse sections of false indusia in the closed (A) and open (B) state. It is functionally built as a bilayer, with the adaxial layer comprising a single row of large tubular cells and the abaxial functional layer consisting of three rows of tangentially elongated, smaller cells. Especially the adaxial, tubular cells undergo a marked deformation during dehydration. The scale in (A) and (B) is identical. (C-D) The collapse of the adaxial cell walls of the tubular cells (i.e, their curvature inversion towards the cell lumen) is well visible after desiccation (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0138495#pone.0138495.s005" target="_blank">S4 Video</a>). The scale in (C) and (D) is identical.</p

Sporangium motion sequences and spore dissemination.

<p>The sporangia have been gripped at their stalks with tweezers and adjusted vertically. Sporangium 2 in (D) is still situated on a false indusium. ac = apical cup; bc = basal cup; s1 = spores from apical cup; s2 = spores from basal cup. (A) The slow passive nastic movement of the annulus includes rupture of the sporangium (i,ii) and formation of the apical cup and basal cup (iii). The annulus relaxes after this tensioning process (including a first ultrafast relaxation step), but does not immediately reset to its initial position, stopping approximately halfway (iv). Afterwards, the annulus further resets; the extent of this step varies and can lead to a nearly initial annulus curvature, or may stop much earlier. (B) First, ultrafast annulus relaxation step which leads to rapid spore ejection from the apical cup. This step lasts only 40 μs until spores emerge in the respective frame. Afterwards the sporangium bounces and spores from the basal cup also become shed (t = 50–70 μs). Frames were taken from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0138495#pone.0138495.s008" target="_blank">S7 Video</a>, cropped and digitally resized without interpolation. (C) The dissemination pattern during spore ejection from a sporangium is shown. At the beginning, the tensioned annulus is turned in such a way that the apical cup points left backwards. After relaxation, spores of the apical cup are forcibly ejected almost straight downwards, whereas those from the basal cup are shed in an irregular pattern. Frames from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0138495#pone.0138495.s012" target="_blank">S11 Video</a> were cropped and digitally resized without interpolation. (D) Tracked spores from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0138495#pone.0138495.s010" target="_blank">S9</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0138495#pone.0138495.s011" target="_blank">S10</a> Videos (images rotated 90° anti-clockwise). Still frames of sporangium 1 and 2 at t = 0, which depict the last frames before the respective annuli start to move, and at t = 0.5 ms respective t = 0.3 ms. The six tracked spores are visible and marked. Spore 5 from the basal cup of sporangium 2 is already visible at t = 0.</p

Loss of mass during the movement of a detached false indusium.

<p>The movement of the false indusium could not be quantified and is, therefore, qualitatively depicted by presenting single frames in 40 min time steps (the respective <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0138495#pone.0138495.s004" target="_blank">S3 Video</a> is recorded with a speed of 1 frame per 5 minutes). The motion is continuous and accompanied by an asymptotic mass loss of up to ~42%.</p

Sporangium Exposure and Spore Release in the Peruvian Maidenhair Fern (<i>Adiantum peruvianum</i>, Pteridaceae)

<div><p>We investigated the different processes involved in spore liberation in the polypod fern <i>Adiantum peruvianum</i> (Pteridaceae). Sporangia are being produced on the undersides of so-called false indusia, which are situated at the abaxial surface of the pinnule margins, and become exposed by a desiccation-induced movement of these pinnule flaps. The complex folding kinematics and functional morphology of false indusia are being described, and we discuss scenarios of movement initiation and passive hydraulic actuation of these structures. High-speed cinematography allowed for analyses of fast sporangium motion and for tracking ejected spores. Separation and liberation of spores from the sporangia are induced by relaxation of the annulus (the ‘throwing arm’ of the sporangium catapult) and conservation of momentum generated during this process, which leads to sporangium bouncing. The ultra-lightweight spores travel through air with a maximum velocity of ~5 m s^-1, and a launch acceleration of ~6300g is measured. In some cases, the whole sporangium, or parts of it, together with contained spores break away from the false indusium and are shed as a whole. Also, spores can stick together and form spore clumps. Both findings are discussed in the context of wind dispersal.</p></div

Kinematics of false indusia situated on cut-off pinnule margins.

<p>(A) Motion of a false indusium recorded from lateral, frontal and top view in our microscopy lab (~23° Celsius, ~50%rh). The false indusium performs a curvature inversion, rotates around its connection line to the pinnule, and its lateral regions flap towards the middle part. (B) Motion of another false indusium in greater detail. (C-E) When the false indusium is in its fully open state (as seen here from different angles), the sporangia (here empty already) point into different directions, an arrangement for which we hypothesize that it promotes spore scattering. (F) The desiccation-driven opening motion is reversible because open false indusia completely re-close under water.</p