Climate‐Dependent Heat‐Triggered Opening Mechanism of Banksia Seed Pods

Abstract Heat‐triggered fruit opening and delayed release of mature seeds are widespread among plants in fire‐prone ecosystems. Here, the material characteristics of the seed‐containing follicles of Banksia attenuata (Proteaceae), which open in response to heat frequently caused by fire, are investigated. Material analysis reveals that long‐term dimensional stability and opening temperatures of follicles collected across an environmental gradient increase as habitats become drier, hotter, and more fire prone. A gradual increase in the biaxial curvature of the hygroscopic valves provides the follicles in the driest region with the highest flexural rigidity. The irreversible deformation of the valves for opening is enabled via a temperature‐dependent reduction of the elastic modulus of the innermost tissue layer, which then allows releasing the stresses previously generated by shrinkage of the fiber bundles in the adjacent layer during follicle drying. These findings illustrate the level of sophistication by which this species optimizes its fruit opening mechanism over a large distribution range with varying environmental conditions, and may not only have great relevance for developing biomimetic actuators, but also for elucidating the species' capacity to cope with climatic changes.

[1]  S. Kelley,et al.  Lignin-Based Thermoplastic Materials. , 2016, ChemSusChem.

[2]  Peter Fratzl,et al.  Plants control the properties and actuation of their organs through the orientation of cellulose fibrils in their cell walls. , 2009, Integrative and comparative biology.

[3]  Tianhua He,et al.  Banksia born to burn. , 2011, The New phytologist.

[4]  B. Lamont,et al.  Biogeography of Banksia in southwestern Australia , 1996 .

[5]  R. Nicholson,et al.  Phenolic Compound Biochemistry , 2006 .

[6]  J. Fromm,et al.  Electrical signals and their physiological significance in plants. , 2007, Plant, cell & environment.

[7]  A. Wardrop The opening mechanism of follicles of some species of Banksia , 1983 .

[8]  Markus Rüggeberg,et al.  Bio-Inspired Wooden Actuators for Large Scale Applications , 2015, PloS one.

[9]  H. Edwards,et al.  Fourier-transform Raman spectroscopic study of unsaturated and saturated waxes , 1997 .

[10]  Samuel M. Felton,et al.  A method for building self-folding machines , 2014, Science.

[11]  R. Cowling,et al.  Flammable infructescences in Banksia: a fruit‐opening mechanism , 1984 .

[12]  R. Jetter,et al.  Composition differences between epicuticular and intracuticular wax substructures: how do plants seal their epidermal surfaces? , 2011, Journal of experimental botany.

[13]  N. Hayashi,et al.  Association of Catechin Molecules in Water: Quantitative Binding Study and Complex Structure Analysis. , 2016, Journal of natural products.

[14]  D. Fang,et al.  Origami by frontal photopolymerization , 2017, Science Advances.

[15]  B. Lamont,et al.  Fire temperatures and follicle-opening requirements in 10 Banksia species , 2006 .

[16]  L. Mahadevan,et al.  How the Venus flytrap snaps , 2005, Nature.

[17]  Sumin Kim,et al.  Curing behavior and viscoelastic properties of pine and wattle tannin-based adhesives studied by dynamic mechanical thermal analysis and FT-IR-ATR spectroscopy , 2003 .

[18]  Céline Douat-Casassus,et al.  Plant polyphenols: chemical properties, biological activities, and synthesis. , 2011, Angewandte Chemie.

[19]  A. Gill Fire and the opening of Banksia ornata F. Muell. Follicles , 1976 .

[20]  P. Chaplin,et al.  A Multicenter, Open-Label, Controlled Phase II Study to Evaluate Safety and Immunogenicity of MVA Smallpox Vaccine (IMVAMUNE) in 18–40 Year Old Subjects with Diagnosed Atopic Dermatitis , 2015, PloS one.

[21]  M. Calleja,et al.  How two-dimensional bending can extraordinarily stiffen thin sheets , 2016, Scientific Reports.

[22]  L. Feldkamp,et al.  Practical cone-beam algorithm , 1984 .

[23]  R. Elbaum,et al.  Insights into the microstructures of hygroscopic movement in plant seed dispersal. , 2014, Plant science : an international journal of experimental plant biology.

[24]  L. Foo Proanthocyanidins: Gross chemical structures by infrared spectra , 1981 .

[25]  Sindy K. Y. Tang,et al.  Bioinspired self-repairing slippery surfaces with pressure-stable omniphobicity , 2011, Nature.

[26]  M. J. Bukovac,et al.  Rheological Properties of Enzymatically Isolated Tomato Fruit Cuticle , 1995, Plant physiology.

[27]  R. Elbaum,et al.  The Role of Wheat Awns in the Seed Dispersal Unit , 2007, Science.

[28]  E. Maire,et al.  In Situ Experiments with X ray Tomography: an Attractive Tool for Experimental Mechanics , 2010 .

[29]  David T. Bell,et al.  Ecological response syndromes in the flora of southwestern Western Australia: Fire resprouters versus reseeders , 2001, The Botanical Review.

[30]  H. Tributsch,et al.  The Material Strategy Of Fire-resistantTree Barks , 2008 .

[31]  P. Reis,et al.  Geometry-induced rigidity in nonspherical pressurized elastic shells. , 2012, Physical review letters.

[32]  Hendrik Bargel,et al.  Structure-function relationships of the plant cuticle and cuticular waxes - a smart material? , 2006, Functional plant biology : FPB.

[33]  André R Studart,et al.  Bioinspired materials that self-shape through programmed microstructures. , 2014, Soft matter.

[34]  Chao Yuan,et al.  3D Printed Reversible Shape Changing Components with Stimuli Responsive Materials , 2016, Scientific Reports.

[35]  R. Cowling,et al.  Variation in serotiny of three Banksia species along a climatic gradient , 1985 .

[36]  M. Crisp,et al.  How Was the Australian Flora Assembled Over the Last 65 Million Years? A Molecular Phylogenetic Perspective , 2013 .

[37]  A. Versari,et al.  Application of Fourier Transform Infrared (FTIR) Spectroscopy in the Characterization of Tannins , 2015 .

[38]  R. Kupferman,et al.  Geometry and Mechanics in the Opening of Chiral Seed Pods , 2011, Science.

[39]  C. Dawson,et al.  How pine cones open , 1997, Nature.

[40]  Peter Fratzl,et al.  Origami-like unfolding of hydro-actuated ice plant seed capsules. , 2011, Nature communications.

[41]  C. Rice-Evans,et al.  Structure-antioxidant activity relationships of flavonoids and phenolic acids. , 1996, Free radical biology & medicine.

[42]  A. Wardrop,et al.  The opening and shedding mechanism of the female cones of Pinus radiata , 1964 .

[43]  H. Edwards,et al.  Fourier-transform Raman spectroscopic study of natural waxes and resins. I , 1996 .

[44]  L. Gibson Biomechanics of cellular solids. , 2005, Journal of biomechanics.