Biomimetic composite materials inspired by wood

Biomimetic composite materials inspired by wood

14

P. Alam

14.1 Introduction 14.1.1 The breadth and scope of biomimetics Although the etymological root for the term biomimetics is essentially derived from Greek, literally meaning life-imitation; the breadth and scope of utility for this term is considerably vast. When reading through the large quantity of biomimetic works available in the public domain, it becomes very clear that this term has been interpreted as literally bio-mimesis, more esoterically as bioinspired, and in some cases as biologically utilising. Resultantly, there is considerable reading material available on the topic of biomimetic composites. This chapter attempts to collect key publications that can best explain biomimetics in relation to composites inspired by, or made of, wood- and cellulosic-based materials and organisms. One might begin to question rather broadly: what makes wood a biomimetic material? Certainly, cellulose is nature’s oldest structural material and exists in a myriad of different organisms each exhibiting a different quality, characteristic or functional use for the cellulose. These characteristics minimally include sense and response to a number of very different external stimuli, high levels of fracture toughness through hierarchical structure, growth development patterns for function optimisation, the ability to move in specific directions without musculature – even when the plant is dead, and much more. We begin by elucidating how the hierarchical structure of plants and trees affects mechanical performance and in particular, fracture toughness.

14.2 Hierarchy, structure and the principles of biomimetic design The physico-chemical qualities of wood and natural fibres are the key reasons for why such materials are able to enhance toughness and have the properties of self-healing (Alam, 2014a). These materials are hierarchically structured and exhibit particular attributes and characteristics at every length scale. It is essentially the overall interaction of characteristics at every length scale that gives rise to the final material property. Figure 14.1 (from Harrington, 1996) artistically depicts the hierarchical structure of wood. If we consider the structure of wood using a top-down approach we find that at the macro-scale, wood is a laminar material with each lamina consisting of hollow Wood Composites. http://dx.doi.org/10.1016/B978-1-78242-454-3.00014-7 Copyright © 2015 Elsevier Ltd. All rights reserved.

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Figure 14.1  The hierarchical structure of wood. At the macroscale, wood is a porous fibre reinforced laminated composite. At the cellular scale, wood comprises a polymer matrix reinforced by cellulose microfibrils and arranged into microlaminae. At the molecular scale, cellulose can occupy both crystalline and amorphous forms, and is a structural biopolymer with the ability to develop numerous stabilising electrostatic interactions. Art work by Mark Harrington, Copyright University of Canterbury, 1996 (re-print permission granted).

fibres embedded in a polymer matrix. This laminated arrangement has the advantage of dissipating fracture energy while the fibrous composite arrangement further serves to retard crack growth. By redirecting mechanical energy and blunting the progress of fracture, both laminated and fibrous arrangements give rise to heightened absorption of mechanical energy and contribute to the overall toughness of wood. At the fibrous level, wood is a lignocellulosic composite with stiffness and strength provided by the fibres, which are glued together essentially, by a ductile lignin-based biopolymer. This is a secondary macro level composite attribute that couples to the laminated arrangement to retard crack growth and thus serves to increase the amount of mechanical energy that the material can absorb. Each lignocellulosic fibre is also a fibrous laminated composite. Deconstructing each macro-fibre cell wall reveals its laminated arrangement. Each lamina is made up of cellulose micro-fibrils with layer-specific orientation. In similitude to the growth rings and macro-fibres, these micro-laminates and micro-fibrils serve to redistribute mechanical energy and retard cell wall fracture. However, they also turn the cell wall into a material with stable global mechanical

Biomimetic composite materials inspired by wood359

properties since each layer exhibits a different micro-fibril orientation. Thus, from a structural perspective, we find wood is composed of composites arrangements at different length scales, each interconnected and each contributing to the overall mechanical performance of the material. Looking more closely, we find that at the molecular level, cellulose exists in both amorphous and crystalline forms. This allows the molecule itself to exhibit composite properties at very low length scales through variations in its own crystallinity. Importantly, the molecular structure of the cellulose polysaccharide provides numerous sites for hydrogen bonding along the length of its chain. This is a critical feature for (a) increased energy absorption at the molecular level through intermolecular chain entanglements (Whitney et al., 1999) and (b) the qualities of self-healing through hydrophobic interactions of the cellulose molecules with surrounding materials (Duan et al., 2014). Moreover, these sites also give rise to secondary interactions with the soft matter molecules namely; lignin, hemicelluloses, pectin and structural proteins. Figure 14.2 (from Teeri et al., 2007) provides the structures for common molecular components of plant cell walls. Figure 14.2a shows the structure of cellulose, the O–H

OH OH

HO O

O

H

O

O HO

O

n

X

HO

O OH O

OH

HO n

CO2R

O OH

O

O

O O

O O

OH OH

OH

O

O HO

OH

OH

R OH

HO

O OH OH

OH

y n

(b) H3CO

OH

HO

(d)

OH

HO O

HO

O

OH

(c)

O

O HO

O

H

R = H or CH3

OH

OH O

HO O CO2R

O O

HO

H O

x,y = 0 or 1 R = H or α-L-Fuc

OH OH

OH

HO

(a)

HO HO

OH

H3CO

OH

HO

OH

HO OCH3

Ara1-4

Ara1-4

Ara1-4

Ara1-4

Ser-Hyp-Hyp-Hyp-Hyp-Ser-Hyp-Ser-Hyp-Hyp-Hyp-Hyp-Tyr-Tyr-Tyr-Lys

(e)

Ara1-4

Ara1-4

Gal

Ara1-4

Ara1-4 TRENDS in Biotechnology

Figure 14.2  (a) The structure of cellulose; (b) the molecular structure of xyloglucan, a hemicellulose found in the primary cell walls of dicotyledenous trees; (c) the structure of a monomeric repeat unit of polygalacturonan, a branched pectic polysaccharide that effectively cements together the primary cell walls of adjacent plant cell walls; (d) the building blocks of lignin in the order of coniferyl alcohol, sinapyl alcohol and paracoumaryl alcohol and (e) the structure of a proline rich structural protein from a plant cell wall. Taken from Teeri et al. (2007). Re-printed by permission of Elsevier.

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groups lying along the side of the chain being the sites for H-bonding. Figure 14.2b shows the molecular structure of xyloglucan, a hemicellulose found in the primary cell walls of dicotyledenous trees and a biopolymer that has shown great potential in the biomimetic engineering of cellulosic materials. Figure 14.2c shows the structure of a monomeric repeat unit of polygalacturonan, a branched pectic polysaccharide that effectively cements together the primary cell walls of adjacent plant cell walls. Figure 14.2d shows the building blocks of lignin in the order of coniferyl alcohol, sinapyl alcohol and paracoumaryl alcohol. Lignin acts as a matrix material to the cellulose fibres and consequently gives bulk form, structure and property to the plant cell wall. Figure 14.2e shows the structure of a proline rich structural protein from a plant cell wall. Proline has a special structure which allows it to twist easily and it is an amino acid that essentially gives rise to many intriguing biopolymer characteristics such as supercontraction (Liu et al., 2008a,b). Glycine rich proteins also exist in plant cell walls. Glycine has been shown to have at least two structural functions in nature. The first is that it provides extra H-bonding sites and thus can increase the stickiness of a material in which it is present (Schwarz et al., 1982). The second important feature of glycine is that it readily develops into 31 helices, which in turn allow it to function as a soft amorphous spring (Pahlevan et al., 2014), giving rise to characteristics of heightened extensibility and greater malleability. The 31 helix is essentially a right handed helix with three residues per turn and ten atoms in the final ring that forms. Whether these attributes of twisting, stickiness and extensibility are the primary purpose for their existence in plant cell walls is unknown. It is possible that these proteins have been misinterpreted as solely structural proteins, when in fact they may have certain other qualities still to be discovered, such as was the case with keratin. Keratin is a structural protein but is now understood to be bi-functional and appears to be intimately involved in cell signal-reaction pathways (Paramio and Jorcano, 2002; Alam et al., 2013a). Since structural proteins in plant cell walls are predominantly amorphous, their structural benefits are perhaps limited to the qualities of binding and malleability. Polymer properties are defined by secondary interactions. Wood is also almost entirely a polymeric material yet it has unique properties by which it is able to divert cracks and absorb considerable mechanical energy. It is evident that each individual attribute of wood, from molecular to macro scales, has a distinct and interconnected purpose, and it is this hierarchical interconnected quality that holistically results in a mechanically superior polymeric structural material. When we consider the complexity of molecular species available within wood fibres and at their surfaces, we can consider methods of fibre treatment that will give rise to improved fibre matrix interactions in, for example, natural fibre reinforced composites. The following section considers biomimetic methods of fibre functionalisation.

14.3 Biomimetic functionalisation of natural fibres Considerable efforts have been undertaken to improve and functionalise the surfaces and bulk of natural fibres. Predominantly, fibre functionalisation has been geared ­towards a mechanical enhancement of biocomposites and many forms of fibre

Biomimetic composite materials inspired by wood361

f­ unctionalisation have been biomimetic or bioinspired. The mechanical effectiveness of a composite relies greatly on the strength of bonding at fibre–matrix interfaces. To that effect, maximisation of interfacial bond strengths has been somewhat of a focal point. Common methods of natural fibre surface treatment include acetylation (Sassy and Chanzy, 1995), etherification (Biardo et al., 2001), peroxide treatment (Sapieha et al., 2003), alkalisation (Mwaikambo and Ansell, 2002), silane treatments (Bisanda and Ansell, 1991), silylation (Pei et al., 2010) and graft co-polymerisation (polymer grafting). Methods based on polymer grafting to natural fibre surfaces essentially hold the greatest potential for their biomimetic functionalisation as it allows for the mimicry of direct chemical interactions observed in nature, it allows for the development of surface hierarchy observed often in many advanced natural composites (Alam, 2014b), and it is a method that effectively preserves the bulk-crystalline structure of cellulose (Teeri et al., 2007). It is important that the crystalline quality of cellulose is preserved, especially in mechanical applications and treatments such as acetylation, which have been shown to destroy this important intrinsic structure (Klemm et al., 2005) and reduces the strength of the fibres. Many natural biopolymers have evolved function-specific molecular structures. Table 14.1 from Laaksonen et al. (2012) describes the biological roles and key structural features for a number of elastomeric biopolymers (proteins). Spider dragline silks are by example, optimised for the absorption of mechanical energy (Keten et al., 2010; Gosline et al., 2002; Alam, 2014a,b, 2015) and more recently has been shown to have an additional electrical sensitivity (Pahlevan et al., 2014). Bombyx mori silks contain sericin proteins which have a high content of polar uncharged serine (Garel et al., 1997) and are excellent at gluing together the silk cocoon fibroins (Takasu et al., 2002). Biopolymers of the jumbo squid (Dosidicus gigas) beak are not mineralised, but rather have important l-3,4-dihydroxyphenylalanine (DOPA) to histidine covalent crosslinks that gives rise to exceptional mechanical stability (Miserez et al., 2010). DOPA is also key to crosslinking and consequently produce, strong adhesive qualities of mussel proteins (Silverman ad Roberto, 2007), which have also been found to functional well as wood adhesives (Messersmith and Barrett, 2014). In cases such as those described and others, the most important concepts involve an understanding of the mechanism of adhesion, the side chain functionality and the folding behaviour of the biopolymer in question. If we thence consider polymer grafting, or surface organo-acid treatments as biomimetic means by which adhesion between a natural fibre and a matrix material can be improved; we must also consider the molecular mechanisms of attachment, the malleability of the attaching polymer (as a long folded or short rigid molecule), the form of attachment (chemical or secondary) and the intermolecular strength of attachment (polar, non-polar, electrostatic and hydrophobic). Polymer grafting to cellulose has most typically been achieved through treatment with trizaine agents, isocyanates or malaeic anhydride (Pickering, 2008). Organoacids minimally include peptide derivatives of proteins, proteins, fatty acids or carboxylic acids. One objective in surface functionalising cellulose fibres is to reduce hydrophilicity, since doing so would improve compatibility with many hydrophobic polymer matrix materials such as polypropylene and polylactic acid (Pommet et al., 2008; Li et al., 2007; Baltazar-y-Jimenez et al., 2008a,b). Lee et al. (2011) report

Examples of biological elastic proteins, their functions and their structural features

Protein

Biological role

Structural features

References

Repeats of elastic and compact amorphous hydrophobic domains (e.g. repeats of VPGVG alternating with crosslinked (via Lys residues) hydrophilic domains Repetitive hydrophilic sequence (e.g. repeats of GGRPSDSYGAPGGGN in fruit fly resilin) crosslinked between Tyr residues Gly-, Met- and Phe-rich repeats crosslinked by Lys and Tyr residues within the repeat motifs

Li and Daggett (2002)

Amorphous hydrophilic regions forming β turns (e.g. GPGXX repeats) and helical structures (e.g. GGX repeats) alternating with β-sheetrich hydrophobic regions (Ala-rich) that form noncovalent crosslinks Very large protein comprising of random coil regions (PEVK and N2B regions), flanked by folded domains in tandem (immunoglobulin and fibronectin III-like domains) Reversible crosslinking using metal coordination by His residues or 3,4-dihydroxyphenylalanine modified Tyr residues in preCol protein and mussel foot protein 1, respectively

Omenetto and Kaplan (2010) and Nova et al. (2010)

362

Table 14.1 

Energy storage properties: high resilience and strain Elastin (and elastin-like peptides)

Yields elasticity to vertebrate connective tissue (e.g. in skin and blood vessel walls)

Resilin

Energy storage and fast release for insect flight, locomotion and sound production Abductin Compressible elasticity for the ligament that opens the mollusc shell on muscle relaxation Shock-absorbing properties: low resilience and high strain and tensile strength Protective cocoons produced by silkworms, as well as webs and escape lines by spiders

Titin

Yields elasticity in muscle myofibrils

Byssal thread proteins

Toughness and extensibility of the thread that anchors molluscs to solids

Taken from Laaksonen et al. (2012). Re-printed by permission of Elsevier.

Bochicchio et al. (2005)

Li et al. (2002)

Harrington et al. (2010)

Wood Composites

Silk fibroin and spider silk protein

Elvin et al. (2005)

Biomimetic composite materials inspired by wood363

that hydrophilic cellulose surfaces can be converted to hydrophobic surfaces by esterification reaction with acetic, hexanoic or dodecanoic acid. Importantly, they find that the carbon backbone of these organo-acids can be used to control the extent of surface hydrophobicity without affecting the crystallinity of the cellulose. This is an important finding since heterogeneous esterification reactions with organo-acids to cellulose-based fibres will cause a reduction in the cellulose crystallinity (Ifuku et al., 2007). Homogenous esterification in the production of cellulose acetate and in the presence of ionic 1-N-butyl-3-methylimidazolium chloride furthermore is found to reduce the crystalline nature of cellulose (Schlufter et al., 2006). By confining their reactions to the surfaces of cellulose, Lee et al. (2011) managed to retain the important crystalline structure of cellulose fibres. Coupling organo-acids to cellulose surfaces can also be important in the biomedical materials sector as it is a means of bio-activating cellulose-based biomaterials. In the important work of Kalsakar et al. (2008), amino acids were coupled via esterification reaction, to the surfaces of fibrous cellulose networks. Notably, Kalsakar and co-workers found that aromatic amino acids (in particular tryptophan) were more effective in developing well spread fibroblast cell structures. Fibroblasts are the primary cells involved in wound healing and their growth morphology and regulation is induced through a heparin-FGF (fibroblast growth factor) coupling. Heparin is a polyaromatic compound and its mimicry (Benezra et al., 2002) has been a subject of interest for well over a decade. When contemplating the research of Kalsakar and co-workers, we can postulate that perhaps the mimicry of specific chemical features within functional molecules such as heparin may be of greater importance than mimicry of an entire molecular structure. The key to simplified chemical biomimicry of cellulose-based composites is thus the identification of function specific chemicals and their interactions. This in turn may be of use in relation to other biomaterial surface issues such as blood adhesion (Véliz et al., 2014), blood clotting potential (Wanna et al., 2013), anti-bacterial properties (Hou et al., 2009) and moisture regulation (Czaja et al., 2006). As mentioned earlier, one of the key factors affecting the toughness, fracture toughness and strength of wood and plant materials is structural hierarchy. Hierarchy as a critical design feature for modern composites design is acknowledged (Bismarck, 2008), and a number of recent attempts have been made to improve natural fibre composite properties by manufacturing hierarchical surfaces. Surface functional groups can be attached to cellulose using enzymatically modified xyloglucan, which in turn permits the attachment of longer polymers and gives rise thus, to structural hierarchy at fibre surfaces (Brummer et al., 2004; Zhou et al., 2005; Lönnberg et al., 2006). Figure 14.3 (from Teeri et al., 2007) provides an overview of xyloglucan-mediated cellulose surface modifications. In (a), xylogluco-oligosaccharides with R functional groups (XGO-R) are incorporated into xyloglucan (XG) through an enzymatic reaction with xylogucan endo-transglycosylase (XET). The XG-R conjugate is adsorbed to the cellulosic surface (b). Through further chemical reactions (c), the XG-R conjugate may then be converted to achieve a desired effect, for example: (i) optical brightening agents; (ii) amino groups; (iii) thiol groups (a reversible modification); (iv) biomolecule capture agents including ligands and (v) radical polymerisation initiators. Surface bonded cross linking natural proteins can be used to from cross bridges that enhance

XG R XGO-R

XET, EC 2.4.1.207

(a) R XG-R

Cellulose surface

(b) R

+

NH 3

S

N H H

HS

–

O3S

H H N

Br O

O

O O

–

SO 3 NH+2

UV light

(c)

(i)

NH2

Electrophile (e.g. FITC)

(ii)

O NH

O

Thiol-specific reagent (e.g. MTS-rhodamine)

DTT

(iii)

O

NH

Streptavidinphosphatase conjugate plus substrate

(iv)

NH

ATRP

(v) TRENDS in Biotechnology

Figure 14.3  An overview of xyloglucan-mediated cellulose surface modifications. In (a), xylogluco-olidosaccharides with R functional groups (XGO-R) are incorporated into xyloglucan (XG) through an enzymatic reaction with xylogucan endo-transglycosylase (XET). The XG-R conjugate is adsorbed to the cellulosic surface (b). Through further chemical reactions (c), the XG-R conjugate may then be converted to achieve a desired effect, e.g. (i) optical brightening agents, (ii) amino groups, (iii) thiol groups (a reversible modification), (iv) biomolecule capture agents including ligands and (v) radical polymerisation initiators. Taken from Teeri et al. (2007). Re-printed by permission of Elsevier.

Biomimetic composite materials inspired by wood365

the interactions between reinforcing and matrix phases thereby improving composite strength (Levy and Soseyov, 2002). Pommet et al. (2008) and Juntaro et al. (2008) report on a novel eco-friendly method for creating structural hierarchy on natural fibre surfaces. In their work they grew bacterial cellulose nanofibres to sisal fibres creating a greater surface area of contact and considerably more interlocking sites. When incorporated into a polymer matrix, hierarchical ‘hairy’ sisal fibre composites showed improved mechanical performance over untreated sisal fibre reinforced composites. Gradwell et al. (2004) consider polymer adsorption as a simple means to replicating hierarchical biomimetic surfaces on cellulosic substrates. In their research, they elucidate the existence of a critical aggregation concentration, above which polymer molecules aggregate prior to adsorption, which in turn alters the surface structure and properties. The roughness of a cellulose surface was furthermore shown to be a parameter that can be easily manipulated by changing the adsorbing polymer. Surface hierarchy has also been approached by means of biomimetic mineralisation of calcium carbonate. In nature, the morphology of calcium carbonate is commonly controlled via template polymers. A number of crystal structures have successfully been manufactured by the addition of polymer molecules into the crystallisation process of calcium carbonate. Included amongst the structures manufactured to date are spherical crystals (Liu et al., 2008a,b; Qi et al., 2002; Yu et al., 2004; Zhang et al., 2006; Cheng et al., 2010), acicular (Liu and Yates, 2006; Kim et al., 2005), urchin-like (Zhang et al., 2005) and twin peanut/apple core-like structures (Cölfen and Qi, 2001; Ren et al., 2010). Figure 14.4 (from Liu et al., 2008a,b) shows an example of how porous spherical calcium carbonate can be manufactured via a phosphatidylglycerol template while Figure 14.5 (from Qi et al., 2002) shows hollow spherical calcium carbonate crystals, created via double hydrophilic block co-polymer templates. Urchinlike calcium carbonate crystals shown in Figure 14.6 (from Zhang et al., 2005) are created via sodium dodecyl benzene sulfonate templates. The twin peanut/apple corelike structure shown in Figure 14.7 (from Cölfen and Qi, 2001) is created via a PEGb-PMAA template. Kato (2000) applied a layer by layer poly-acrylic acid template to control the crystallisation of calcium carbonate onto the surfaces of natural (chitin) fibres. Similarly to cellulose, chitin is derived from basal glucose units and as such has similar hydrogen bonding potential. Acicular calcite particles have also been grown to the surfaces of electrospun nanocellulose fibres (Liu et al., 2011), which evidences the size-versatility of mineralisation methods. Alam et al. (2013b) tested the mechanical improvement of composites reinforced by acetic acid template-mineralised flax fibres. Alam and co-workers were inspired by Sclerospongiae, which are a rare group of sponges exhibiting blocky surface mounted calcium carbonate reinforcements, shown in Figure 14.8. This figure shows SEM micrographs of the sponge (a–c), calcium carbonate coated flax fibres dissolved and then crystallised using acetic acid (d and e) and unmineralised flax fibre (f). The x and y values appended to each micrograph provide elemental information acquired by EDS. Importantly, Alam and co-workers identified thickness as being a key design parameter for use in composites. Small mineral deposits on fibre were reported to improve the mechanical properties of a composite due to improved mechanical interlocking of adhesion (Figure 14.9a and b). In this figure, C1, C2 and C3 refer to lightly coated, unmineralised and heavily coated

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Figure 14.4  Porous spherical calcium carbonate manufactured via a phosphatidyglycerol template. Taken from Liu et al. (2008a,b). Re-printed with permission from the American Chemical Society.

fibres, ­respectively. Contrarily, thick mineral deposits were shown to be detrimental to the strength and stiffness of fibre reinforced composites because the mineral-coating around the fibre was more prone to premature cracking, as shown in Figure 14.9b and c. Stillfried et al. (2013) mimicked solitary standing Crispatotrochus corals using polyacrylic acid as a template and means by which calcium carbonate could attach to and coat flax fibre surfaces. In their research, the fibre coating thickness was again shown to be a critical design parameter for solitary fibre bundles tested in flexion.

14.4 Genetic engineering Synthetic biology is a novel discipline that is gaining impetus with regards to its potential for application in engineered materials systems. Synthetic biology is grounded essentially in genetic engineering and its scope and utility is thus vast. The objectives

Biomimetic composite materials inspired by wood367

(a)

(b)

(c) Figure 14.5  Hollow spherical calcium carbonate crystals, created via double hydrophilic block co-polymer templates. Taken from Qi et al. (2002). Re-printed by permission of John Wiley and Sons Inc.

with synthetic biology are to genetically tailor materials inspired by nature, including materials that are non-existent in nature. Genetic engineering may thus serve in the development of improved cellulose-based composites, or indeed, trees and plants may act as the hosts for the production of novel genetically engineered materials. Synthetic proteins for example, have been engineered to incorporate both hydrophobin and cellulose-binding blocks (Laaksonen et al., 2011). Cellulose-binding blocks anchor microbial hydrolytic enzymes (containing aromatic groups) to cellulose sugar rings (Laaksonen et al., 2012). With this cleverly designed protein, Laaksonen and co-­ workers were able to create strongly adhered nanocomposites containing both graphene

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5 µm

(a)

(b)

2.5 µm

Figure 14.6  Urchin-like calcium carbonate crystals are created via sodium dodecyl benzenesulfonate templates. Taken from Zhang et al. (2005). Re-printed by permission of Elsevier.

5 µm

1 µm

Figure 14.7  Twin peanut/apple core-like structure created via a PEG-b-PMAA template. Taken from Cölfen and Qi (2001). Re-printed by permission of John Wiley and Sons Inc.

and nanocellulose. Graphene attaches strongly to the hydrophobin block (Linder, 2009; Laaksonen et al., 2010) while cellulose joins to the cellulose binding block (Linder and Teeri, 1997). Their objectives in developing a genetically engineered proteinous matrix for graphene and nanocelluloses at different length scales, was to mimic hierarchical structures found in nature that have high fracture toughness and superior mechanical properties. Similar bi-functional genetically engineered proteins have been used for the self-assemblage and tighter packing of nanocellulose fibre films (Varjonen et al., 2011). In these composites, the soft proteinous matrix is very low in volume fraction, which makes them comparable to natural composites. Regardless of how low this fraction is nevertheless, soft proteinous materials in nature and in these composites are indispensable for high toughness (Alam, 2014a; Currey, 1977). Table 14.2 (from Laaksonen et al., 2012) lists a few examples of natural solid material binding proteins and, furthermore,

(a)

(c)

(b)

Porifera structure Mag 30 ×

(d)

Porifera: Partly mineralised Mag 500 ×

Porifera: Highly mineralised Mag 1k ×

x – C 37%, O 20%, Si 0%, S 1%, Ca 1%

x – C 54%, O 18%, Si 0%, S 2%, Ca 1%

y – C 17%, O 12%, Si 14%, S 0%, Ca 7%

y – C 18%, O 17%, Si 2%, S 1%, Ca 8%

(e)

Flax: Scattered mineral deposits Mag 1k × Scattered deposits shown in dotted circles x – C 59%, O 47%, Si 0.3%, Ca 0.4%

(f)

Flax: Thick mineral crust Mag = 1k ×

Unmineralised flax fibre Mag 1k × (C3)

x – C 53%, O 47%, Si 0%, Ca 0.3% y – C 31%, O 31%, Si 7%, Ca 2% (C2)

y – C 50%, O 40%, Si 0.5%, Ca 2% (C1)

Figure 14.8  SEM micrographs showing structures of Sclerospongiae (a–c), acetic acid templated calcium carbonate minerlaised flax (d and e) and untreated flax fibres (f). Taken from Alam et al. (2013b). Re-printed with permission from Springer. F – Flax M – Mineralised deposit R - Rubber

F M R

Interfacial shear

Anchor sites between the mineral compound deposits C2 increase resistance to shear

60

Stress (MPa)

50

C1

40

(b)

M R

Cracking through F mineralised envelope

R

Interfacial shear

C3

30 C1 20

C2 C3

10

0

(a)

F

0

0.2

0.4

Strain

0.6

(c)

Figure 14.9  (a) Stress–strain curves of lightly mineralised flax reinforced composites (C1), heavily mineralised flax reinforced composites (C2) and unmineralised flax reinforced composites (C3). (b) Mechanisms associated with C1–3 and (c) SEM micrograph showing that overly thick mineral coatings on fibres fracture prematurely and actually weaken a composite. Taken from Alam et al. (2013b). Re-printed with permission from Springer.

Examples of natural material binding proteins, their biological functions and properties

Protein domain

Target material

Biological function

Properties

Refs

Hydrophobin

Hydrophonbichydrophilic Interface Cellulose

Fungal adhesive and control of surface energy

Strongly amphiphilic, stabilised by intramolecular disulfides

Linder (2009), Wösten (2001)

Anchoring of microbial hydrolytic enzyme on cellulose substrate

Aromatic groups bind to cellulose sugar rings

Anchoring of hydrolytic enzyme on chitin substrate in bacteria, plants and invertebrates Attachment of mussel to solids in water

Aromatic groups presumably bind to chitin sugar rings

Levy and Shoseyov (2002), Linder et al. (1996) and Guillen et al. (2010) Guillen et al. (2010)

Cellulose-binding domain

Chitin

Mussel byssus adhesive proteins (e.g. Mfp-3 and Mfp-5)

Nonspecific

Barnacle cement proteins (e.g. cp-19 k) Molluse biomineralbinding proteins (e.g. Pif) Amelogenin

Nonspecific Calcium carbonate

Antifreeze protein

Ice

Calcium phosphate

Attachment of barnacle body to solid surfaces under water Binding to and control of biomineral morphology in mollusc shells Control of hydroxyapatite mineralisation in vertebrate tooth enamel Protects the organism by preventing ice crystal growth; found in bacteria, plants, insects and fish

Taken from Laaksonen et al. (2012). Re-printed by permission of Elsevier.

Modified amino acids (dihydroxyphenylalanine and hydroxyarginine; adhesion to metals and crosslinking), crosslinking Multiprotein complex, not relying on poss-translational modifications Highly negatively charged

Lin et al. (2007)

Kamino (2008) Suzuki et al. (2009)

Self-assembles into nanospherus, glutamine residue rich

Snead et al. (2006)

Binding to ice is contributed by high shape complementarily with a crystal face together with hydrophobic interactions and H bonds

Garnham et al. (2011)

Wood Composites

Chitin-binding domain

370

Table 14.2 

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briefly describes their biological functions and properties. The target materials are usually specific; however, some proteins (e.g. Mfp-3, Mfp-5 from mussels, and cp-19k from barnacles) are more versatile and can bind to many materials. Understanding the mechanisms by which such proteins function in order to fulfil their role in nature is critical in the production of synthetic (hybridised) proteins. Proteins in natural materials are extremely diverse. Many of them quite importantly have particular, repeating sequences of proteinogenic amino acids. The way in which these amino acids interact, and the functionality of their side chains are important considerations when engineering ‘binding’ proteins. Plant gene manipulation, is one way by which artificial spider silk-like protein manufacture is being researched. Spider silks for example, have very particular amino acid sequences that give rise to secondary and super-secondary structures of high toughness. Strong and stretchy dragline silks have oligopetide motifs in repeat sequences of GGX forming 31 helices in their amorphous domains, and [GA]n and [A]n forming stable β-sheet nanocrystals which reinforce the amorphous matrix. Here, G is glycine, A is alanine and X is typically any of alanine, leucine, tyrosine or glutamine. Contrarily, the sticky glue-like flagelliform silks are predominantly comprised of repeat sequences of GPGGX and GPX (where P is proline). Figure 14.10 (from Hirman et al., 2000)

Elastic β-turn spiral GPGXX GPGGX GPGQQ

Crystalline β sheet Ala-rich (GA)n An

310 Helix GGX

?

Spacer

Flag MaSp2 ADF-3 ADF-4 MaSp1 MiSp1 MiSp2 ADF-1 ADF-2 trends in Biotechnology

Figure 14.10  Secondary structure variations in spider silk proteins from the flagellate gland (flag), from the major ampullate gland (MaSp1 and 2 – N. clavipes, ADF-3 and 4 – A. diadematus) and from the minor ampullate gland (MiSp1 and 2 – N. clavipes, ADF-1 and 2 – A. diadematus). Taken from Hirman et al. (2000). Reprinted with permission from Elsevier.

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shows secondary structure ­variations in spider silk proteins from the flagellate gland (Flag), from the major ampullate gland (MaSp1 and 2 – N. clavipes, ADF-3 and 4 – A. diadematus) and from the minor ampullate gland (MiSp1 and 2 – N. clavipes, ADF-1 and 2 – A. diadematus). The flagellate gland produces sticky glue-like silks while the major and minor ampullate glands are responsible for the structural silks. Unlike Flag, the structural silks are defined by their crystallinity. Numerous attempts have been made to form recombinant silk-like proteins but the genetic manipulation of plants for this same purpose is less well known. Yang et al. (2005) produced synthetic dragline silk-like protein using A. thaliana, a small flowering plant that grows natively in Europe and Asia. Protein expression was targeted to the leaf tissues and silk fractions as high as 6.7% were reported to have been produced within the leaves. Other gene manipulated plants explored in the production of biomimetic silks include tobacco and potato (Scheller et al., 2004; Van Beilen and Poirier, 2008) wherein elastin-like proteins were conjoined with silk-like proteins. A model for bacteria-mediated transformation into plants (from Gevlin, 2003) is shown in Figure 14.11, in this case through Agrobacterium. In this figure, several steps are elucidated for the transformation process from bacteria to plant. These include the steps within the bacterium itself, notably, the perception of phenolic and sugar signals from wounded plants cells, virulence gene induction, T-strand processing from plasmids and finally the exportation of the T-strand and virulence proteins. Steps related to the host plant undergoing genetic modification include; bacterial attachment, transference of T-strands and Virulence proteins, cytoplasmic

Phenolic Signal perception Sugars viv Gene induction

Attachment Nuclear targeting Integration

Transfer

T-DNA processing

Cytoplasmic trafficking

Agrobacterium tumefaciens

Plant cell TRENDS in Biotechnology

Figure 14.11  A model for the process of bacterium-mediated transformation highlighting important steps within the bacterium and the plant for successful engineering of genes. Taken from Gevlin (2003). Re-printed by permission of Elsevier.

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Unfolded chain

3-D native state

Secondary structure fluctuating around its native position

Native-like secondary structure

Figure 14.12  The process of protein folding from an unfolded state, through its secondary structure and to a 3D native state (where it is at a low energy state). Super-secondary structures are interactions between secondary structures (such as β-sheets and α-helices). Quaternary structures are interactions between the 3D native states, sometimes called, protein complexes. Taken from Amani and Naeem (2013).

trafficking, targeting of the T-complex to the nucleus and T-DNA integration into the genome of the plant. Two areas of improvement are still needed to correctly mimic spider silk. First, the molecular weights of dragline silks (ca. 300 kDa) have not been nearly reached in plant manipulated or bacteria manipulated sources. Secondly, the secondary to quaternary (interacting 3D-native protein states) structures (see Figure 14.12) of silk typically self-construct through an extrusion process that occurs during spinning. Simply re-creating the proteins does not satisfy the coupled necessity of mimicking the actual process by which the individual protein molecules can align and interact. A major component of the United States economy is bound to forestry. In recent US industrial developments, genetically modified trees are being cultivated. The modified Australian eucalyptus trees are being forested in the south-east of the USA and are expected to replace native pines. These new trees grow faster, produce more timber, require less space and have reduced requirements in soil and pest control (Voosen, 2010). Complete sterilisation or at least male sterilisation may result in a faster rate of wood production (Strauss et al., 1995); however, in general the effects these trees and their pollen may have on the environment and on local organisms are currently unknown. Delignification has been a focal point in genetically engineered forestry. Lignin causes problems when fibres need to be separated. It is a biopolymer with bonds that are difficult to breakdown in both mechanical and chemical separation techniques, which is common practice in, for example, the pulp and paper industry. Figure 14.13 (from Beckermann and Pickering, 2008) exemplifies low to high levels of delignification (through an alkali treatment) and with respect to fibre

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Figure 14.13  Effects of delignification on fibre separation (top to bottom = low to high separation = low to high delignification, respectively). Taken from Beckermann and Pickering (2008). Re-printed by permission of Elsevier.

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separation. High fibre separation is preferred for composite applications as the area of available interface for bonding should be as high as possible to maximise interaction between the composite components. Wróbel-Kwiatkoeska et al. (2009) characterised flax fibres that were genetically manipulated to produce lower fractions of lignin yet which retain high cellulose fractions. The fibres themselves were found to bear the same levels of stress to failure as ordinary flax fibres; however, with less lignin the fibres can be separated with greater relative ease. Enzymatic treatments are also a means to changing fractions of biopolymers in wood and plant cell walls (Parre and Geitmann, 2005a,b) though direct genetic modifications are considered to be the more effective methods (Burgert, 2006). Wilkerson et al. (2014) report that weak ester linkages can be created within the lignin backbone. These linkages are relatively easy to break down and require fewer chemicals than are ordinarily used in chemical separation methods. Wilkerson and co-workers manage this by isolating the transferase gene able to form monolignol ferulate transferase conjugates and genetically tailoring the trees to produce these conjugates. Monolignol ferulate transferase conjugates improve the rate at which the plant cell walls digest under the influence of mild alkali. Triglyceride oils from plant sources are a base source from which many composite matrix polymers are produced. Biomimetic insights may also be gained from genetic manipulations of cell wall components, even when the genetic alteration causes weakening of the cell wall. Pena et al. (2004) studied the effects of mutating hemicellulose (xyloglucan) side chains. In their work carried out using Arabidopsis hypocotyls, they found that changing the side chains caused both significant softening and significant weakening of the plant cell wall. The way in which the hemicellulose side chains actually function to rigidify the cell wall is unknown however, what is clear is that (a) xyloglucan side chains have specific characteristics that hold together the cell wall components more effectively, and (b) mutant hemicelluloses are another route whereby mechanical and chemical separation methods can be carried out more easily. Biodegradable structural polymers are an important novel area, one target application of which is for use as a matrix material in composites. To have mechanically superior biodegradable plastics with properties matching petroleum-based plastics would be a step towards more environmentally responsible engineering. Khot et al. (2001) report a variety of triglyceride oils from genetically manipulated plants which decrease the extent of molecular relaxations. The consequence of molecular relaxation is a very broad glass transition, which is typical of triglyceride oil-based structural polymers. Genetically engineered natural (triolein) polymers sharpen the storage modulus transition from glassy to rubbery states and this provides evidence that oilbased structural polymers from genetically modified plants can be manufactured to mimic the properties of petroleum-based structural polymers. Certain biodegradable polymers with sound mechanical properties can be produced through gene manipulated plants. Hydroxyalkanoate polyesters and hydroxybutyrates are amongst those that have been given special attention. Poly-hydroxybutyrates have properties analogous to polypropylenes, which are a common choice of natural fibre matrix material. Poly-hydroxyalkanoates are commonly used in paper-based composites and for the manufacture of films of differing thicknesses (Mooney, 2009). Numerous bacteria will

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naturally produce these polymers; however, genetically modified bacteria such as E. coli are used for higher yield production, usually with manipulations applied so as to vary the side chains and molecular structures (Eschenlauer et al., 1996; Nikel et al., 2006). Plants like A. eutropus are engineered to contain the synthase gene of A. caviaea to produce native and variant forms of poly-hydroxyalkanoates (Fukui and Doi, 1998) while A. thaliana plants transformed by the gene encoding of R. eutropha are also a source for poly-hydroxybutyrate production (Poirier et al., 1992). R. eutropha has also been used for poly-hydroxybutyrate synthesis, by combination with poly-­ hydroxyalkanoate synthesis operons (Lössl et al., 2003). Poly-hydroxyalkanoate operons were also employed by Nawrath et al. (1994) to produce poly-hydroxybutyrate through A. thaliana plants. In addition to direct gene insertions into three separate plants, Nawrath et al. fused the genetic traits of each plant by cross-pollination. A. thaliana plants are very p­ opular transgenic templates and the highest levels of polyhydroxybutyrates (40 wt% dry) have been produced through this species (Bohmert et al., 2000). Interestingly, poly-­hydroxybutyrates are also finding production in transgenic fibrous plants like switchgrass (Somleva et al., 2008), which is sometimes used to produce reinforcing fibres for natural fibre composites. Along the same lines, fibrous plants like flax, commonly used to produce reinforcing fibres in natural fibre composites, are being used to accumulate poly-hydroxyalkanoates (Van Beilen and Poirier, 2008), which in turn are easily converted to thermoplastics from plant oils (Mooney, 2009). There are clearly many recent advances in plant gene manipulation for the biomimetic production of naturally occurring or combined natural polymers. Genetically engineered forestry and farming therefore holds considerable potential in the development of property specific and characteristic specific trees, wood and wood products. A summary of what is required is carefully described in Figure 14.14 (from Strauss et al., 1995). The following section concerns biomimetic actuation as inspired by cellulose derived organisms.

14.5 Biomimetic systems of motion based on plants Plants and trees exhibit incredible examples of ‘motion without muscle’. Plants are able to react to changes in light intensity, heat, stress, touch and moisture. In a majority of cases, they are also able to sense and react to stimuli; however, reactive-motion is as present in dead cellulosic material as it is in living and receptive cells. The relative motion of plants may be categorised as either fast or slow. Examples of fast motion may include the explosive release of seeds (see Figure 14.15) (Edwards et al., 2005; Whitaker and Edwards, 2010) and the mechanically stimulated entrapment of insects in ‘meat-eating’ plants. Plant movement may be further divided into nastic or tropic motion (Brauner, 1954). Both forms of motion are in response to a stimulus, though nastic movement is more specifically, independent of direction, while tropic movement is a directional response to the external stimulus (Burgert and Fratzl, 2009). A well-known example of fast tropic motion is observed in the mechanism of trap closure in meat eating plants such as the Venus flytrap (Markin et al., 2008), shown in

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Steps in plant genetic engineering Production of of transgenic plants Gene identification

Promoters

Analysis & deployment Molecular verification of gene presence and expression

Coding regions

Sexual propagation

Asexual propagation

Splicing resynthesis Greenhouse & field tests Transfer into plant cells Ecological & biosafety analyses Incorporation into genome

Gene expression

Selection of transgenic cells

Plant regeneration

Regulatory permits for large scale use

Proprietary arrangements

Commercial deployment

Continued monitoring of efficacy & safety

Figure 14.14  Important steps in the genetic engineering plants and in their consequent utilisation. Taken from Strauss et al. (1995). Re-printed by permission of Springer.

Figure 14.16, which digests insects to fulfil its nitrogen requirements (Findlay, 1984; Fagerberg and Allain, 1991). In this particular species of plant, the stimulus of touch to response is the fastest growth process known in plants (Williams and Bennett, 1982) being considerably more rapid than, for example, light-responsive plant actuation. Hairs protruding from the Venus flytrap leaf epidermis trigger the activation of ion channels (Volkov et al., 2007, 2008) when mechanically stimulated. The trigger hairs

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convert essentially, an initial mechanical energy into an electrical energy (the signal). The electrical charge opens specialised pores of the inner layer cells. A simultaneous ionic flux (sodium, potassium, chloride and calcium) creates an osmotic potential between the outer and inner epidermises and water molecules resultantly flow towards the outer epidermis of the leaf (Taya, 2003), causing it to swell. The inner epidermis loses water and so reduces in volume and the result of inner layer shrinking coupled to outer layer swelling is that the leaf folds. The remarkable aspect of this closing process is that it happens at a very high velocity when compared to other forms of plant actuation (Williams and Bennett, 1982) though it remains unknown as to how the plant achieves such levels of speed in actuation. Stork’s bill awn is another example of fast motion. In this case, the plant has an explosive method for seed dispersal however, according to Abraham et al. (2012); the specific high velocity movement is directly reliant on a single specialised layer with a uniform tilted helical geometry. When the seed ‘fires’, all cells spiral collectively, which gives rise to explosive motion. In slow movement, we may include reaction wood growth responses to ambient stresses, the opening and closing of stomata in gaseous exchange, and the follower

Figure 14.15  Seeds catapulted when the bunchberry flower opens. Taken from Edwards et al. (2005). Re-printed by permission of Macmillan Publishers Ltd. Trap lobes invert their curvature

Straight midrib

~100 ms

(a)

Closed

Open

(b)

Hinge zone

Closed

Trapdoor perfoms buckling sequence prior to ultra-fast opening

Tentacle head

(c)

Open

Bent ~100 ms midrib

(d)

Closed

~0.5 ms

Open

Figure 14.16  High speed trap closure of the Venus flytrap. Taken from Poppinga et al. (2013). Re-printed by permission of John Wiley and Sons Inc.

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response of a plant in reaction to the strongest sun rays. Reaction wood is a load-­ induced phenomenon, and as such is an example of how mechanical stimulus gives rise to changes in cellular growth. The fibres of reaction wood tend to exhibit thicker cell wall layers than ordinary wood, as shown in Figure 14.17; furthermore, they develop an extra layer known as the G-layer, or gelatinous layer (Côté et al., 1969). This G-layer contains very low levels of lignin, high levels of water but almost no aromatic substances, except on approaching the inner lumen of the cell (Gierlinger and Schwanninger, 2006). The G-layer is thus cellulose rich, though this has been debated (Joseleau et al., 2004), as it may in fact be a species specific characteristic. Whether reaction wood grows to reinforce the tensile or compressive faces of a branch will depend on whether the tree is a hardwood or softwood variety, respectively (Wardrop, 1965; Barnett and Jeronimidis, 2003). The reaction wood itself appears to grow via certain signalling processes between cells. One of the more prominent theories on the chemical signal for reaction wood growth is based on variable local concentrations of auxin (a growth hormone) through prolonged mechanical stimulus. More specifically, the auxin will grow in regions of low indol-3-acetic acid concentration (Little and Savidge, 1987; Srivastava, 2002). This theory is nevertheless contested by Hellgren et al. (2004), who report that reaction wood forms irrespective of the local indol-3-­ acetic acid concentrations. In their research, they suggest that mechanical stimuli may interact with the indol-3-acetic acid signal transduction path, or that reaction wood is a response from signals other than those based on indol-3-acetic acid.

(b) V

V

T

R

RW

(a)

R V

NW

V

V

V

Figure 14.17  Visual variation in cell wall density from normal wood (NW) to reaction wood (RW). Taken from Yoshizawa et al. (1993). Re-printed by permission of Springer.

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The mechanisms of slow movement are often via internal water driven cellular pressure changes, otherwise termed turgor. Unequal turgor pressures give rise to uneven changes in volume for a plant material in continuum, which in turn generates torsional or bending type movements (Firn and Myers, 1989; Roeflsema and Hedrich, 2005). The architecture and alignment of cellulose-based fibres within a structure affects the way in which turgor works. Pine cone bract scales are a good example of how differential fibre alignment affects bract scale unfolding (see Figure 14.18). Each bract scale has an inner alignment along the axis of the scale, while fibres are aligned radially on the outer segment of the scale (Dawson et al., 1997). As a consequence, bract scales may open easily, since there is considerable compressive malleability on the outer side of the scale. At the same time, the scale can retain its open structure since its inner side is reinforced by tensile fibres. Notably, it is this same anisotropic physical structure that gives rise to unidirectional opening when the cone dries (Burgert and Fratzl, 2009). The axially reinforced inner layer deforms less on drying than the outer layer and the result is bending, or opening, of the scale. Biomimetic composites based on wood/plant actuation are a novel field currently researched by only a few groups worldwide. There is a great deal to consider in the mimicry of wood and plant actuation. Mechanisms of motion may be simplistic and based on turgor; however, sense and response systems, signalling mechanisms and physical–chemical–physical communication are considerably more complex. Wood density variations in bamboo have been a source of inspiration for the ­development of

Plasma membrane cell wall

Flexor cells

Wet

Dry s nu

H2O

Turgid extensor cells

Ca2+

lvi

Pu

TnV N

H+

O H2 +

Stretched flexor cells

Shrinking +

K

O H2

Swelling Flaccid state

(a)

(b)

Cl–

H+

H2O H2O H O 2 H2O

Flaccid extensor cells

K

Turgid state

Cl–

H2O TnV N

(c)

Figure 14.18  (a) Dry bract scales of pine cones open out, while moist bract scales close tightly around the core of the cone. As the extensor cells lose liquid they go from a turgid state to a flaccid state (b) and as a consequence the bract scales open. The movement of water, much like in the Venus flytrap, is through a changing osmotic potential (c). Taken from Poppinga et al. (2013). Re-printed by permission of John Wiley and Sons Inc.

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multilayer-piezoelectric actuators designed to have an optimal ­resistance to ­bending (Taya, 2003). Burgert and Fratzl (2009) suggest that any moving composite that is intended to mimic plant cells should consist of a swelling gel-like matrix tightly adhered to stiff fibres. In a system like this, the gel can swell but the stiff fibres are not deformable. The result is anisotropic, or complex composite movement, which has been confirmed empirically by Sidorenko et al. (2007), who report that covalently bound silicon needles in a hydrogel cumulatively incline on swelling or shrinkage of a gelatinous matrix. Li and Wang (2011) consider composite fibre orientation as key in plant cell wall inspired actuation, but primarily when coupled to fluid pressure changes (turgor) applied internally to the actuation system. Hydrogels that have been used in actuation devices and inspired by woody/plant materials include amphoteric acrylamides, ferroelectric gels and photo-active gels (Tamagawa and Taya, 2000; Popovic et al., 2001; Xu et al., 2001). Although in each case the function of actuation was developed, the response rate of the hydrogel was slow. Faster response hydrogels have been developed (Tamagawa et al., 1999) by increasing gel porosity. This porosity decreases the diffusion distance, which is proportional to the diffusion rate, and thus porous gels can swell or shrink faster than non-porous gels of the same material.

14.6 Biomimetic timber architecture Architectural design has an historic connection with biological form, shape and definition. Well known examples include the Eiffel Tower, the construct of which was based on trabecular bone (Sundaram and Ananthasuresh, 2009), Frei Otto’s ­spider-web architecture of the Munich Olympic Stadium and Rene Binet’s protozoan (Radiolara) inspired Porte Monumentale constructed at the turn of the twentieth century (Malek and Williams, 2013). The design and construction of biomimetic architecture has nevertheless progressed far beyond the essentials of aesthetics. Architectural designers now look to biology for inspiration in the fields of sustainability (El Ahmar, 2011; Zari, 2007), self-sensing (Pritchard and Ansell, 2000), sense–response functionality (Beesley et al., 2006), structure–shape performance (Schiftner et al., 2008) and self-generated energy or energy conversion (Todorovic and Kim, 2012). Each field is interlinked (Carrara et al., 2009), and the most holistic viewpoint is in an approach whereby biomimetics is ecosystem-based (Zari and Storey, 2007). El Ahmar et al. (2013) summarises ecosystem-based biomimetics as inclusive of five main factors. These include: (i) an ability to design a building with consideration for its direct adaptation to its surroundings, homonymous in fact with the adaptation qualities of biological organisms to their particular environments; (ii) a view to holistically optimise the performance of the material system, as opposed to individual material components; (iii) the utility of so-called genetic algorithms in the computationally aided design process as a means to mimicking the continuous uninterrupted ­evolutionary processes observed in nature; (iv) an ability to design a building such that its behaviour will affect its form, which unlike (iii) is based on

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coerced morpho-­correction and (v) an ability to predict the overall functionality of a building given unexpected or emergent changes. In view of these current considerations, wood and timber-based composite architectures have considerable potential (Wiscombe, 2012). Certainly, empirically based analyses are critical in maximising the functionality and utility of biomimetic architectures; however, computational techniques such as CAD (computer aided design) and numerical methods like the FEM (finite element method) are currently intrinsic and indispensable. Computational methods are very often applied in m ­ orphogenetic-based design (Menges, 2012) and may be algorithmically intense, which in turn allows for radical advances in the generation, processing and evolution of architectural information (Gruber and Jeronimidis, 2012). Computational methods are particularly important when the biological entity under scrutiny is in fact in itself, a highly complex self-contained ecosystem. Analogies between cell biology and architecture are one example (Sabin et al., 2008) where the cell itself is an intrinsically complex but functioning construct with signalling processes, adaptation and response mechanisms, self-cleaning and energy generating capabilities. This single cellular system when existing within a larger organism functions within the local group to benefit the larger community, which in turn serves to benefit itself. These concepts of interdependency and energy manufacture through ambient energy sources are also prime concerns in the development of biomimetic architectures (Guiterrez, 2008). Morphogenetic design, or morphogenesis, is a term originally used in biology (Roudavski, 2009), but it has been both adopted and adapted to several other disciplines, including architectural engineering. The simplest definition of morphogenesis is that it is an iterative process for architectural development based on geometrical transformations as adapted to constructional and material constraints (Shadkhou and Bignon, 2009). Digital or computational morphogenesis employs computational tools for the derivation of such architectural development. The focus in the use of morphogenetic computational tools is in fact not visual, but generative, and as such can be algorithmically intensive (Kolarevic, 2000; Kolarevic and Malkawi, 2005). El Ahmar (2011) postulates several benefits for architectural design that may emerge through the direct study of biological morphogenesis. These include that (a) numerous problems and challenges in architectural design have already been resolved in nature and (b) contemporary architectural concepts such as growth and adaptation find parallels in nature that may be suitably mimicked. Shadkhou and Bignon (2011) define six variants in the shaping of morphogenetic timber architecture. The first is pilling-up, which involves the super-positioning of horizontal timber beams in modular arrays or as layers. Stratification is the second variant and is similar to pilling-up but leans more towards flatness and may employ either horizontal or vertical super-positions. A third variant is tessellation, which involves the segmenting of walls/surfaces using ­alternative geometrical constructs and angles. Meshing is the fourth variant and typically involves the cross-weaving of timber beams usually with unequal intersection lengths, resulting in unequal areas of space between beams. Armatures are the fifth variant that benefit from different structural elements to create a mixed form construction. The final variant is known as a membrane, and is a continuum surface constructed from flat timber sections and connected linearly.

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By assuming both biological and architectural evolution as non-deterministic processes (Knippers and Speck, 2012), a level of computational quasi-randomness can be implemented into morphogenetic design. Such algorithms permit variations to common patterns and constructs, as would typically be observed in the natural world. A good example would be that of cellular structures (Roudavski, 2009) or hexagons packed tightly in an array. Figure 14.19 provides examples of cellular wood composite structures. Even simple probabilistic methods such as Monte Carlo could be used to vary parameters such as angle, edge-to-edge connection and the number of sides. Erosion and growth algorithms can be used to deduct or extend parts of structures respectively. Tessellation of the resultant structures at each iterative step may then merge the structure back towards a continuum and patterns often observed in nature can be reproduced – for example, the FAZ Pavilion in Frankfurt (Menges and Reichert, 2012), which is a structure inspired by the microarchitectures of conifer cones. This structure is also designed to adapt to moisture variations in the same way the conifer cones move and is also hence an example of plant inspired non-motoric actuation as described earlier. Figure 14.20 (from Reichart et al., 2015) shows a number of biomimetic bract-scale designs for biomimetic wooden surfaces. Each design functions on the same ­turgid-flaccid principles found in pine cone bract scales. The extent to which one of these designs will actually open as a function of drying is shown in Figure 14.21. Conifer ­microarchitectures, much like numerous other ­biological ­architectures, can be deemed aesthetically pleasing (Rolston, 1998). Considerable research is still needed to develop our understanding of why, and indeed how, natural patterns, though ­often seemingly random, appear pleasant and invoke emotion in (a)

(b)

(c)

(d)

50 RH%

85 RH%

Figure 14.19  Examples of biomimetic cellular architectures. Taken from Reichart et al. (2015). Re-printed by permission of Elsevier.

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(a)

Type 1

(b)

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Figure 14.20  Wooden biomimetic architectural surface designs inspired by the turgor-flaccid action of pine cone bract scales. Taken from Reichart et al. (2015). Re-printed by permission of Elsevier.

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(a)

85 RH – 22 °C

(b)

75 RH – 22 °C

(c)

65 RH – 22 °C

(d)

55 RH – 22 °C

(e)

45 RH – 22 °C

(f)

35 RH – 22 °C

Figure 14.21  Examples of humidity-related opening of biomimetic surface architectures. Taken from Reichart et al. (2015). Re-printed by permission of Elsevier.

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humans. Certain s­ equences have nevertheless been discovered, perhaps the most famous of which is the Golden spiral, a close approximation of which is the Fibonacci spiral (Mainzer, 1996; Hemenway, 2005). These particular spiral patterns are found repeated in a great many materials and arrangements ranging from the spirals of galaxies to the spirals of sea shells, and of course the Fibonacci spirals are also manifest in conifers (Brousseau, 1969).

14.7 Conclusions Renewability, sustainability and biodegradability are key concerns amongst high-­ income nations in the twenty-first century. For this reason alone, wood-based materials are likely to have a very active future. As has been elucidated in this chapter; wood, plants and cellulosic materials provide both the inspiration for, and the materials needed to develop, advanced biomimetic composites and materials. Biomimetic composites will continue to develop, but there is a high probability that greater impetus will be placed on improving the performance of natural, sustainable and biodegradable materials. It may be that synthetic biology holds the key to developing specially designed proteins/protein complexes and other polymers that radically enhance the performance of cellulose-based composites. There indubitably exist both health and environmental dangers associated with genetically engineered products. However, provided that regulations are in place whereby thorough toxicological testing precedes utility, genetically engineered materials will most likely become as widespread as genetically engineered foods are at present. Biomimetic architecture is heading towards self-sufficiency and building will, in time, need to sense and respond to a plethora of environmental factors. Architectural design will also continue to lean towards sustainability and environmentally responsible engineering. As such, buildings may need to utilise advanced biomimetic cellulose-based composites in their construction. Perhaps advancements in the design of high-performance natural fibre composites will end up being based on deep sea organisms, on the chemistry of insect cuticles or on synthetically produced biopolymers. When we consider that such high-performance biomimetic materials will probably, in the future, also be coupled to bioinspired architectural designs that are able to sense, respond, self-clean, self-heal, manufacture natural energy and self-actuate, we may begin to envision a truly holistic future of wood-based biomimetics.

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