The scales of seed-bearing pine cones move in response to changes in relative humidity. The scales gape open when it is dry, releasing the cone's seeds1. When it is damp, the scales close up. The cells in a mature cone are dead, so the mechanism is passive: the structure of the scale and the walls of the cells composing the scale respond to changing relative humidity. Dissection of cones from the Monterey pine, Pinus radiata, revealed to us two types of scale growing from the main body of the cone — the ovuliferous scale and the bract scale. The larger ovuliferous scales respond to changes in relative humidity when removed from the body of the cone.
The scale consists of two tissues distinguishable with the naked eye (Fig. 1a). The inner surface of the scale is composed of sclerenchyma fibres (8-12 μm in diameter, 150-200 μm long), grouped in bundles reminiscent of cables. The outer surface of the scale is composed of sclerids (20-30 μm diameter, 80-120 μm long).
We mounted a scale on a rigid metal frame and exposed it to controlled and changing relative humidity at 23 °C in an enclosed chamber. Using image analysis, we measured the angle between the scale and the base of the frame, and the distance that the tip of the scale moved. The scale moves towards the centre of the cone in high relative humidity and away from the centre in low relative humidity (Fig. 1b).
We exposed sclerid and fibre cells to a range of relative humidities in a microbalance with a controlled environment and measured the weight changes with time. There were no differences between the two cell types. Chemical analysis2 showed that each cell type has roughly a 20% volume fraction of cellulose in its cell wall. The rest is lignin, hemicellulose and pectin.
There are large differences in the tensile stiffness (fibre 4.53±0.90 GPa; sclerid 0.86±0.05 GPa). With a 1% change in relative humidity at 23 °C the coefficient of hygroscopic expansion of fibres (0.06±0.02) is significantly lower than that of sclerids (0.20±0.04). Modelling the scale as a simple bilayer structure requires that three parameters are known3: the stiffness of the two tissue types, the relative dimensions of each layer and their coefficient of hygroscopic expansion. The movement of the tips of the scales is not significantly different from that predicted by the model4 (mean, 16.2 mm; predicted, 20.6 mm; t=2.25; 8 d.f.; not significant).
It is not possible to dissect individual cells from the scale as the material is extremely tough. We removed cells using chemical maceration but this removes water and some of the other components of the cell wall. This may affect the observed angle of winding of the microfibrils relative to the long axis of the cell (θ), as may the extremely dry condition under which the cells were observed. Scanning electron micrographs show that θ is considerably lower in fibre cells than in sclerids (Fig. 1c, d). This was confirmed by polarizing light microscopy5, which indicated that θ is 30° (±2°) for fibre cells and 74° (±5°) for sclerid cells.
The mechanism of bending therefore seems to depend on the way that the orientation of cellulose microfibrils controls the hygroscopic expansion of the cells in the two layers. In sclerids, the microfibrils are wound around the cell (high winding angle) allowing it to elongate when damp. Fibres have the microfibrils orientated along the cell (low winding angle) which resists elongation. The ovuliferous scale therefore functions as a bilayer similar to a bimetallic strip, but responding to humidity instead of heat.
Eichholz, G. Jb. Wiss. Bot. 17, 543–588 (1886).
Bradbury, S. Peacock's Elementary Microtechnique (Arnold, London, 1973).
Witztum, A. & Schulgasser, K. J. Theor. Biol. 176, 531–542 (1995).
Rees, D. W. A. Mechanics of Solids and Structures 149–153 (McGraw-Hill, London, 1947).
Preston, R. D. The Physical Biology of the Plant Cell Wall (Chapman and Hall, London, 1974).
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Journal of Materials Chemistry B (2021)
Journal of the Mechanics and Physics of Solids (2021)
Advanced Functional Materials (2021)
ACS Applied Materials & Interfaces (2021)
From Understanding Mechanical Behavior to Curvature Prediction of Humidity‐Triggered Bilayer Actuators
Advanced Materials (2021)