Nature-Inspired Chemical Engineering

C H A P T E R

2 Nature-Inspired Chemical Engineering: A New Design Methodology for Sustainability Panagiotis Trogadas, Marc-Olivier Coppens Centre for Nature Inspired Engineering, Department of Chemical Engineering, University College London, London, United Kingdom

O U T L I N E 1. Sustainability in Chemical Engineering

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2. Sustainability: Design Philosophy 2.1 Why Should We Use Nature as a Source for Inspiration? 2.2 Ways to Connect Nature to Design: Inspiration Versus Imitation

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3. Nature-Inspired Structuring at the Nanoscale: Confinement Effects

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4. Bridging Nano- and Macroscale: Hierarchical Transport Networks

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5. Nature-Inspired Structuring at the Macroscale

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6. Conclusions

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Acknowledgments

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References

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1. SUSTAINABILITY IN CHEMICAL ENGINEERING The concept of sustainability was first mentioned in the scientific literature by H. C. von Carlowitz referring to sustainable forestry in Sylvicultura oeconomica in 1713 [1]. The meaning of the term sustainability in this book was to cut only as much timber as was regrowing, applying forestry practices to ensure that soil fertility was maintained or increased. In the following decades, the emerging idea of sustainable development was engendered among visionaries such as R. Carson in her book Silent Spring during the 1960s [2]. During the 1980s, the idea of sustainability was embraced by the international scientific community with the publication of the Our Common Future report by the Brundtland Commission in 1987 [3,4], which defined sustainable development as “development which meets the needs of the present without compromising the ability of future generations to meet their own needs” [4]. Purposely, the definition of sustainability provided by the commission left space for various interpretations. At the Rio Conference in 1992 and over the following years, the term “sustainability” was defined more precisely, and it has been confirmed since through a wide range of agreements, national programs, and scientific studies [1]. Sustainable development is a continuing process, during which definitions and resulting activities have been constantly evolving. The main aim of this process is to ensure a bright future for our descendants, although there is the underlying risk that theory is put into practice in different ways, creating a highly complex situation. It is for this reason that there are many different interpretations of what constitutes sustainability and sustainable development, a term that is often misused to serve particular interests.

Sustainable Nanoscale Engineering https://doi.org/10.1016/B978-0-12-814681-1.00002-3

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Copyright © 2020 Elsevier Inc. All rights reserved.

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2. NATURE-INSPIRED CHEMICAL ENGINEERING: A NEW DESIGN METHODOLOGY FOR SUSTAINABILITY

One of the most widely used definitions for sustainability was proposed by Liverman [5]: “Sustainability is the indefinite survival of the human species through the maintenance of basic life support systems (air, water, land, biota) and the existence of infrastructure and institutions which distribute and protect the components of these systems.” Currently, the goal of sustainability would not be perceived as attractive to many stakeholders if it were not exceedingly advantageous [1,6,7]. Sustainability implies a threefold added valuedeconomic, social, and environmental profitdall in one. Only few companies would have promoted sustainable production system and process development, without economic incentives. Moving toward sustainability in the design of products, processes, and production systems entails to reinforce the foundations of chemical engineering, adding novel disciplines, design guidelines, and creating dynamic interconnectivity among them. During the last decade, new disciplines and design philosophies for materials and reactor systems have been developed to serve as inspiration for sustainable design in chemical engineering; examples include biomimicry, green chemistry, resilience engineering, and ecological design [1]. In the following sections, we introduce the concept of nature-inspired chemical engineering (NICE), a new design philosophy leading to the redesign of catalytic materials and processes, displacing conventional blueprints and promoting sustainable solutions to engineering challenges.

2. SUSTAINABILITY: DESIGN PHILOSOPHY 2.1 Why Should We Use Nature as a Source for Inspiration? Scientific research becomes increasingly demanding as we attempt to solve, with a sense of urgency, many more technical problems than in previous decades and aim to answer more challenging scientific questions, regardless of the advances made in synthesis and manufacturing [8]. Usually, the number of variables in these complex problems of the problem under examination, with limited time and resources. Developing methodologies to optimize the management of time, cost of energy and materials, synthesis of materials, man power, and maintenance cost is crucial in research. Computational approaches have their limitations (such as number of processors and storage available, number of variables used in a specific problem, etc.) and do not necessarily provide fundamental understanding. If there were to be a guideline for strategies and methodologies that could increase the efficiency of research and development, and lead to more sustainable solutions, its impact on scientific advancement would be immeasurable. One powerful way is to study nature more closely. Natural systems contain many characteristics and mechanisms that can be studied and used to give us hints to the solution of critical problems [9e11]. Careful examination of the structure and dynamics of natural systems reveals certain patterns that are key to underlying desirable properties. For example, the branching of trees, riverbeds, the vascular network, and the human lung contains repeated divisions that are similar over many length scales. In many cases, such features result from optimization processes of energy, matter, and space in natural systems, via self-organization or evolution. Processes in the aforementioned examples are scalable as a result of the self-similar branching. Just like the periodic repetition of unit cells in crystals helps to predict their physical and chemical properties, also the observation of fractal and other patterns in nature helps us to describe objects and dynamic behavior mathematically, and start investigating the underlying reasons for the observations. This, in turn, is the basis for developing a systematic approach to understand natural materials and processes, in relation to function, which, for the engineer, carries additional interest when these functions are superior to what is observed in current artificial materials and processes. Hence, deeper insights in nature can form the basis for nature-inspired solutions for engineering.

2.2 Ways to Connect Nature to Design: Inspiration Versus Imitation Nature is an excellent guide to redesign processes and catalytic materials, as it exemplifies hierarchical structures that are intrinsically scaling, efficient, and robust. This, however, should not reduce to mindless imitation: the biological example needs to be properly chosen, and the different context of technological applications should be accounted for. Hence, there are two distinct categories of research, based on how the natural component is used: (i) nature-inspired and (ii) nature-imitating design. The term “nature” infers a broader definition than “bio,” as features of living and nonliving natural systems are included for materials and process design. We avoid the term “biomimetics,” as we feel it is important to distinguish nature-inspired and nature-imitating designs, and thus avoid misrepresentations or misinterpretations.

2. SUSTAINABILITY: DESIGN PHILOSOPHY

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FIGURE 2.1 The design of the front end of the Shinkansen 500 Series bullet train in Japan was inspired by the action of a kingfisher diving into the water [1]. Copyright © 2007 Elsevier Ltd.

Research based on the imitation of nature tends to mimic isolated features of biological or nonbiological structures for product or process design, which often leads to suboptimal results. In most cases, the actual physical processes or mechanistic features that govern the system are neglected. Despite this, there are successful examples of implementation of bio-imitating design for the solution of engineering problems. Indeed, it does not mean that imitating nature is not leading to a better design, it just limits the design space and often ignores the difference in application context. In Japan, severe noise is caused when a high-speed (w320 km/h) train exits a tunnel. At such high speed, sudden pressure changes occur, leading to the creation of low frequency waves and eventually to a sonic boom when the train exits the tunnel. The kingfisher, a skillful bird that hunts its prey by diving into the water, provided the solution to this noise challenge. Due to the specific shape of its beak and head, a kingfisher slides through the water with extraordinary ease without creating any turbulence. It is a remarkably efficient animal in terms of transition from a low pressure (air) to a high pressure medium (water); its long beak increases gradually in diameter from the tip to the back as it plunges to catch its next meal. Hence, by imitating the shape of the kingfisher’s beak, engineers equipped high-speed trains with a 50-foot-long tapering nose, resulting in the elimination of the sonic boom issue, faster operating speed, and lower consumption of electricity (Fig. 2.1). Another successful example of bio-imitating design is based on the unique characteristics of the external structure of shark skin, which led to the attachment of 3D printed, bio-mimicking shark skin surfaces on swimsuits and on the hull of boats and surfaces of hospitals and airplanes to prevent bacterial growth [12e15]. Shark skin comprises numerous overlapping scales, called dermal denticles, which have grooves across their length that align with the water flow. These riblets can prevent the formation of vortices, allowing the water to flow through the shark skin quickly. The rough shape of dermal denticles discourages parasitic growth, such as algae and barnacles. The difference in context between nature and technology, for example, in size, medium, and velocity, is not explicitly accounted for in the above examples. On the contrary, nature-inspired engineering is based on taking a scientific approach to uncover fundamental mechanisms underlying desirable traits. These mechanisms are subsequently applied to design and synthesize artificial systems that borrow the traits of the natural model [11]. Thus, nature-inspired designs may not even resemble their natural counterparts, but rather function as such. Such designs adopt some of the features of the systematic model, after suitable adaptation to fulfill the different contexts of nature and technology. A great example for inspiration from nature when designing chemical reactors is a typical tree (Fig. 2.2). At the macroscale, its roots branch and spread out widely below the ground to anchor the tree and extract nutrients from the soil. These nutrients are transferred via its fractal root network throughout its volume. Above ground, the crown of the tree divides into increasingly smaller branches and twigs following fractal, self-similar scaling. The twigs bear leaves with a veinal architecture at the mesoscale for further chemical transport, and they contain, at the microscale, molecular complexes that are used to capture sunlight and convert CO2 into sugars via photosynthesis at the nanoscale, providing the food for the growth of the tree. The Centre for Nature Inspired Engineering (CNIE) at University College London (UCL) draws inspiration from such natural processes to create innovative solutions to engineering challenges in energy, water purification, functional materials, health, and living space [8,16e19]. Research in the CNIE is currently based on three themes, corresponding to three fundamental mechanisms, of wide applicability: (i) hierarchical transport networks, (ii) force balancing, and (iii) dynamic self-organization (Fig. 2.3). Employing these mechanisms can lead to the development of new materials and technologies with minimal resource consumption and environmental impact. As a result, the reach of nature-inspired design in science and engineering is vast and expanding. A few examples of our research at CNIE, ranging from nano- to macroscale, are presented in the following sections.

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FIGURE 2.2 A tree as an example of nature inspiration for the design of chemical reactors.

FIGURE 2.3 The broad scope of application of the nature-inspired chemical engineering (NICE) approach, as demonstrated by the research being conducted at the UCL Centre for Nature Inspired Engineering.

3. NATURE-INSPIRED STRUCTURING AT THE NANOSCALE: CONFINEMENT EFFECTS Nature’s catalysts, enzymes, are known to be extremely efficient catalysts under mild conditions. For many reactions under equivalent conditions, enzymes outperform synthetic catalysts by a wide margin, both in activity and selectivity. Enzymes have evolved over millennia to operate optimally within their host organisms in a typically close to neutral, aqueous solution at moderate temperature. However, these reaction conditions are incompatible with most industrial processes, and exposure to extreme conditions (high temperature, acidic pH, detergents, etc.) will result in the denaturation of the enzyme. Enzyme immobilization (such as covalent binding, cross-linking, and physical adsorption) [20e23] is the most widely used solution to enhance its stability, because it allows the enzyme to be easily removed and recycled. Even though immobilization usually results in a decrease in enzymatic activity and selectivity, this attenuation can be significantly decreased or even inverted [24,25]. Molecular chaperonins can inspire the design of an effective enzyme immobilization material. Chaperonins are proteins that bind unfolded polypeptide chains to help them fold correctly [26]. Their effectiveness is based on their following unique characteristics: (i) a narrow, cylindrical pore structure large enough to fit a single protein, (ii) an electrostatic environment promoting facile protein adsorption, and (iii) a hydrophilic core allowing the correct folding of newly synthesized proteins [27,28]. Inspired by this natural solution, mesoporous silica SBA-15 with different pore diameters was used as a support material for immobilizing and protecting enzymes [26]. Myoglobin and lysozyme have been used as model enzymes, physically adsorbed to SBA-15 and exposed to a range of buffered pH conditions. Their activity was

4. BRIDGING NANO- AND MACROSCALE: HIERARCHICAL TRANSPORT NETWORKS

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FIGURE 2.4 Peroxidase activities of free myoglobin and myoglobin immobilized to mesoporous silica SBA-15, with pore diameters of 6.1 (green [light gray in print version] color), 6.6 (light blue [gray in print version] color), and 8.1 nm (dark blue [dark gray in print version] color), in solutions of varying pH (3.6-5.1) at ionic strength 0.1 [26]. Copyright © 2016 American Chemical Society.

compared against nonimmobilized enzymes in the same solution conditions. It has been observed that myoglobin immobilized on SBA-15 is protected from acidic denaturation for pH values between 3.6 and 5.1 (Fig. 2.4), exhibiting a relative activity of up to 350%. Immobilized lysozyme is protected from unfavorable conditions from pH 6.6 to 7.6, with a relative activity of up to 200% [26]. These results indicate that the electrostatic attraction of the enzymes to the surface of SBA-15 is responsible for their stability in acidic conditions. The pore diameter of SBA-15 also affects the stability of these immobilized enzymes, but its contribution remains unclear at different pH values [26]. Rhodium (Rh) complexes were also immobilized by anchoring them to the pore surface of SBA-15 [17]. Conservation or enhancement of hydroformylation activity was observed when compared with the activity of the homogeneous Rh complex in solution [29]. The Rh complex immobilized on amorphous silica exhibited the lowest activity, larger than one order of magnitude lower than that of the homogeneous complex. On the contrary, the activity of immobilized Rh on SBA-15 was similar to the homogeneous complex, while exhibiting high stability and selectivity, showcasing the positive impact of controlled confinement of these Rh catalysts [29]. Silica imprinting is another method of creating confinement with the additional feature of pore functionalization [30,31]. This technique was used to generate microporous platforms with isolated amine sites with varying acidity and dielectric constants [30,31]. The above examples demonstrate the positive effect of confinement on the activity and stability of a catalyst; such confinement effects are also generated within an enzyme itself, induced by its three-dimensional structure. This raises the question whether structural aspects of an enzyme around its active site can be constructed using organic molecules bound to a metal cluster surface? To realize this, calixarene bound via functional groups on gold clusters has been synthesized [32e34]. Calixarene creates points of accessibility on the surface of gold clusters for substrate binding and tunes their electronic state through phosphine groups binding [33]. Such preliminary results demonstrate the great potential of this method toward the synthesis of new catalysts with improved activity, selectivity, and stability.

4. BRIDGING NANO- AND MACROSCALE: HIERARCHICAL TRANSPORT NETWORKS Porous materials are used in several processes in chemical engineering, such as in separations and heterogeneous catalysis. The transport properties of these materials depend on the structure of the pore network, which has to be optimized to minimize transport limitations and increase their catalytic performance. Mass transport in porous media occurs predominantly via convective flow in wide pore channels and diffusion in narrower channels [35]. Continuum and discrete theoretical models have been developed to describe these transport processes: continuum models consider the porous space as an effective continuum of reduced permeability, and discrete models specifically account for the pores [35]. Can the design of these pore networks be improved to facilitate transport? Nature can serve as a guide, as it is full of hierarchical structures, bridging nano- to macroscale, with, in several cases in biology, optimized networks of wide and narrow pores, essential to the functioning of the organism [35]. An example (discussed in detail in the following Section 5) is the unique architectural design of the lung, which achieves scalable, uniform distribution of oxygen to the alveoli, in thermodynamically optimal way.

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FIGURE 2.5 Monodisperse (left), bidisperse (center), and bimodal (right) pore networks in a nanostructured catalyst (nanoporous catalytic material: black; large diffusion channels: white) [36]. Copyright © 2007 Elsevier Ltd.

Inspired by the transport networks in lungs and trees, diffusion limitations in nanostructured catalysts can be minimized via an optimized network of broad and narrow pores. Oftentimes, the size of porous catalyst pellets is determined by hydrodynamic constraints in chemical reactor applications, e.g., pressure drop in a fixed bed reactor. A high catalytic activity per unit volume also requires a high specific surface area; this is realized by nanopores, covered by active sites. Molecular transport through nanopores occurs by diffusion, however, and is very slow. Thus, broad pore channels are required to reduce diffusion limitations in a catalyst pellet. A 2D theoretical model was developed to investigate the effect of a broad pore size distribution in a nanostructured catalyst pellet for a first-order, isothermal chemical reaction [37]. A fractal-like network of large pores led to a higher conversion than a uniform pore network: w40% and 5% increase for molecular and Knudsen diffusion, respectively [37]. This fractal-like structure also achieved the highest effectiveness factor, which was indistinguishable from the factor corresponding to a globally optimized structure [37]. However, the number of pores that could be considered in the optimization of the pore networks was limited, due to the high computational cost of the overall geometric optimization. Therefore, the performance of a nanostructured catalyst with varying large pore network structures was also investigated for a first-order, isothermal chemical reaction via a continuum modeling approach [36], and later generalized to arbitrary kinetics [38]. Monodisperse, bidisperse, and bimodal pore size distributions were considered. The monodisperse network contained only nanopores of known size and specific catalytic activity; the bidisperse network also contained large diffusion channels of the same size, within the nanoporous catalytic medium, whereas the bimodal network contained large diffusion channels of variable size distribution (Fig. 2.5) [36]. Global optimization showed that the yield of catalysts with a bidisperse pore distribution was very similar to that of catalysts with a bimodal distribution (<5% difference in yield), but that it could be one order of magnitude higher than that of catalysts with a monodisperse distribution of nanopores, due to the optimized network of large pore channels [36,38]. The optimization of porosity and large average pore size are crucial, while the distribution around the optimum average is shallow, hence less important. This is similar to the distribution of veins in leaves, capillaries in blood vessel networks, and alveoli in the lung, where the channel size matters, but channels and cells tend to be uniformly distributed when diffusion is the limiting transport mechanismddifferent from the fractal networks observed when convection dominates transport [35]. The image of a tree, shown in Fig. 2.2, epitomizes the parallel between optimal hierarchical transport networks in nature and in catalysis and reaction engineering. At large length scales, discussed in the next section, fractal networks appear, but at intermediate scales, the channel distribution is much more uniform. These results show that the utilization of a nature-inspired design can decrease diffusion limitations in nanostructured catalysts via an optimized network of broad and narrow pores. Continuum models are unsuitable to model multiphase reactions in hierarchically structured catalysts. Recently, a discrete pore network modeling approach has been developed to examine multiphase reactions in porous catalysts. Pore blocking was taken into account using a HosheneKopelman algorithm [39]. Simulation results demonstrated that pore blocking plays an important role in multiphase reactions, because it contributed up to 50% to the hysteresis in effectiveness factor [39]. This cannot be observed using continuum models. Such pore-blocking effects are less pronounced when the connectivity of the pore network is high and for narrow pore size distributions [39,40]. However, the hysteresis loop in catalysts with monomodal, narrow pore size distributions and large volume-averaged pore radius is also steeper, which could pose difficulties for the operation of multiphase reactors. For catalysts with a bimodal pore size distribution, changes in hysteresis loop could be more significant, as hysteresis is affected by pore blocking and capillary condensation phenomena. The spatial distribution of the large pores plays a much more important role than for single-phase reactions [40].

5. NATURE-INSPIRED STRUCTURING AT THE MACROSCALE

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Such simulation-based design criteria for optimal porosity and pore size distributions of hierarchically structured catalysts are a helpful guide to catalyst synthesis, as they can lead to significantly superior performance over catalysts with monodisperse pore distribution or nonoptimized macroporosity. Further details are provided in the cited articles and a recent book chapter [35]. From the perspective of ease of synthesis, it is attractive that catalysts with a bidisperse pore network can be close to optimal, with no need to further optimize the large pore channel size distribution around the optimal average large pore channel size. However, as discussed, this only strictly holds for single-phase reactions, as the situation for multiphase reactions is more complicated. A wide range of synthesis techniques (such as templating, scaffolding, etc.) is available to synthesize these catalysts [41e45]. Recently, the pore network representation of hierarchical materials has been greatly improved, thanks to easier access to spatially resolved imaging techniques, such as X-ray tomography, which allow for 3D reconstruction of porous materials, showcasing pore connectivity, pore volume, throat lengths, and radii [46e48]. Imaging and spectroscopic techniques help the structural investigation of porous materials, and inform the design of hierarchical structures with improved transport properties, higher catalytic yields, better selectivities, and stability. For example, hierarchically structured, sponge-like silicoaluminophosphates could be synthesized with very high isomer yield (79%) in the hydroisomerization of n-heptane. This was achieved by redesigning the hierarchical structure in such a way that the intrinsic reaction controlled regime is widened, and overall diffusion is enhanced, which reduces the cracking probability [49].

5. NATURE-INSPIRED STRUCTURING AT THE MACROSCALE A representative example of the NICE approach at the macroscale is illustrated through the design of flow fields for proton exchange membrane fuel cells (PEMFCs) [50]. Prior to our work on electrochemical devices, the scalable, fractal architecture of tree crowns was used as the basis to design a fractal fluid injector that facilitates the scale-up of fluidized bed reactors and increases their efficiency, due to reduced bubble size and improved, more uniform mixing [51,52]. In the case of fuel cells, we use a similar concept, based on the main characteristics of the human lung to address transport limitations and scalability issues [50]. Lessons from nature to design fluidized beds with bettercontrolled hydrodynamics hence serve a different application in energy technology. Flow field design is vital to fuel cell performance, as it is responsible for the transport of reactants and products to and from the membrane electrode assembly (MEA). The commercial flow fields employed currently (e.g., serpentine, parallel, and interdigitated) result in nonuniform distribution of reactants across the MEA and large pressure drops between their inlets and outlets, leading to fuel cell performance losses. To circumvent these issues, we employed a nature-inspired design based on key characteristics of the human lung, including the fractal structure of the upper airway tree and its thermodynamic optimality (minimal

FIGURE 2.6 (A) The unique characteristics of the lung (fractal structure proportioned to lead to minimum entropy production) are implemented into the design of lung-inspired flow fields for proton exchange membrane fuel cells (PEMFCs). Experimental validation of the lung-inspired flow fieldebased PEMFCs (10 cm2 flow field area) demonstrate improved performance at 50% and 75% RH (N ¼ 4) compared with conventional, serpentine flow fieldebased PEMFCs (B and C) [50]. Symbols represent single serpentine, double serpentine, and lung inspired with N ¼ 3, 4, and 5 generations, respectively. Copyright © 2018 The Royal Society of Chemistry.

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entropy production) during air transport, properties that are desired for fuel cell flow fields as well (Fig. 2.6A). In the lung, air is transported uniformly through a scalable, fractal architecture, from the trachea via the bronchioles to the alveoli, and into the bloodstream to oxygenate the blood cells [53e55]. In addition, the upper airway’s fractal branching structure obeys Murray’s law, according to which the cube of the diameter (di, i ¼ 1 . n) of a parent vessel is equal to the sum of the cubes of the diameters of the two daughter vessels at each level of bifurcation, i, leading to minimal mechanical energy losses: d3i ¼ 2d3iþ1 . As a result, air gradually slows down when flowing from the trachea to the bronchioles. At some generation, n (14e16 in an adult human lung), the convection driven air flow in the bronchioles is equal to the diffusion driven air flow entering the acini, so that the Pe´clet number becomes unity [55]. Further reduction in channel diameter would lead to additional flow resistance, which is undesirable; interestingly, just at this level where Pe´w1, further branching within the acini does not lead to appreciable reduction in channel size, as diffusion is now the dominating transport mechanism. Furthermore, the length of each channel in the upper airway tree is such that the pressure drop is equal over each channel, while in the lower airway tree concentration drop is constant. This leads to equipartition of entropy production, making the lung thermodynamically optimally proportioned [52,55]. The abovementioned, remarkable characteristics of the lung served as the design principle to manufacture 3D printed, lung-inspired flow fields (10 cm2) for PEMFCs with N ¼ 3, 4, and 5 generations. The proportioning of channels in the fractal flow field results in constant entropy production at each branching level, and in minimal overall entropy production over the lung-inspired structure [44,50,56]. Flow fields with N ¼ 4 generations demonstrated a w30% increase in fuel cell performance and power density over commercial serpentine flow fields at 50% and 75% RH (Fig. 2.6 B and C) [50]. In terms of pressure drop, these lung-inspired flow fields exhibited w75% lower values (<2 kPa) than commercial serpentine flow fields (5 kPa) for all RH tested, resulting in the minimization of parasitic losses, and thus to increased fuel cell performance. These improvements in pressure drop and fuel cell performance were maintained at large scale (25 cm2), whereas the large pressure drop (25 kPa) in serpentine flow fieldebased PEMFCs is detrimental to their fuel cell performance. Lung-inspired flow fieldebased PEMFCs with N ¼ 3 generations exhibited the worst performance under all experimental conditions, due to the large spacing between adjacent outlets leading to insufficient oxygen concentration across the MEA. The flow field design with N ¼ 5 generations demonstrated lower fuel cell performance than commercial serpentine flow fields, because its narrow channels in the final generation were prone to flooding [50]. At very high RH (100%) conditions, all lung-inspired flow fieldebased PEMFCs exhibited flooding, which lowered corresponding fuel cell performance. Hence, utilization of new effective water removal mechanisms is needed to overcome this issue, because current antiflooding measures cannot be easily incorporated into these lung-inspired flow fields [57]. However, this extreme humidity condition is rarely employed in practice, favoring the use of lung-inspired flow fields. Table 2.1 provides a detailed comparison of the most common flow field designs currently used in PEMFCs against lung-inspired design. Finally, this proposed nature-inspired approach is not limited to PEMFCs but extends to all electrochemical devices in which flooding is alleviated, such as redox flow batteries and high temperature fuel cells.

6. CONCLUSIONS At the beginning of the 21st century, when sustainability has become a priority, business as usual is untenable, and we must develop novel design guidelines, methods, and procedures. The NICE approach discussed in the previous sections offers opportunities to innovate by redesigning materials and processes, replacing conventional designs, and leading to sustainable solutions to engineering challenges. NICE provides an avenue to sustainable design that combines creativity with engineering fundamentals, allowing for environmental, economic, and social benefits. Currently, biomimetic research is too often focused on imitating isolated features of biological structures to synthesize products, like heterogeneous catalysts or flow fields for electrochemical devices, with suboptimal results. In most cases, the actual physical processes that govern the system are neglected, indicating that the full potential of learning lessons from nature has yet to be realized. In following the NICE methodology, solutions to the above applications are devised by not directly mimicking nature, but rather learning first from it and working within the constraints of each system. The nature-inspired engineering methodology provides a step-by-step approach of deriving mechanisms from the natural system as a model to create a nature-inspired concept, leading to a proposed nature-inspired design, and its implementation, conscious of the differences between the natural context and that of engineering applications. Introducing these nature-inspired design guidelines can lead to sustainable

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6. CONCLUSIONS

TABLE 2.1 Comparison of Different Flow Field Designs for Proton Exchange Membrane Fuel Cells. Flow Field Design

Advantages

Disadvantages

Serpentine

• Efficient water removal • Designed for small active area

• High pressure drop • Water build-up in bends • Uneven reactant distribution

Interdigitated

• Efficient water removal • High fuel cell performance at high current density

• Highest pressure drop of all flow field designs • Uneven reactant distribution • Difficult to scale

Parallel

• Increased power density at high current density

• Uneven reactant distribution • Poor water management • High pressure drop in stack configuration

Pin

• Low pressure drop

• Uneven reactant distribution • Inadequate water removal • Poor fuel cell performance

Lung inspired

• Low pressure drop • Uniform reactant distribution for low and high temperature fuel cells • Higher electrocatalyst stability than serpentine • Easily scalable

• More prone to flooding than serpentine at high relative humidity • High cost of the flow fields made by additive manufacturing, requiring cheaper alternatives

processes and products and, hereby, to a sustainable future. We especially suggest focusing research on the fundamental understanding of hierarchical structure/function relationships in biological systems, as well as properties emerging from synergistic systems behavior. As illustrated here, this understanding can then, for example, guide the development of novel, nature-inspired catalysts and chemical and electrochemical reactors. Furthermore, the engineering principles of NICE can greatly benefit additional research areas, such as biomaterials, tissue engineering [58e62], and healthcare technologies [63], as well as architectural design for the built environment. A review on the prospects of nature-inspired design of biomaterials and devices for healthcare applications is beyond the scope of this chapter, but has been recently published, with further references therein [8]. Some extensively studied examples include materials that mimic shark skin (antifouling and drag reduction) [15,64e67], nacre (remarkable mechanical properties) [67e80], or gecko feet (reversible adhesion) [67,81e85]. Such properties are induced by hierarchical, composite structures, and the surface geometry. Current applications of biomimetic and bio-inspired materials include antimicrobial coatings and biocompatible adhesives. By adopting the systematic approach of NICE, we see opportunities that go beyond case-by-case mimicry for innovation in tissue engineering, drug delivery, osseointegration, and other biomedical applications [8]. As to applications in the built environment, the NICE methodology could aid in the development of building components, which self-regulate the urban environment, absorbing pollutants and providing environmental control in each room (humidity, temperature, light) [86e98].

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These additional examples showcase the diversity of applications of the NICE methodology and how embracing this methodology could provide innovative solutions to engineering challenges, complemented by parallel advances in additive manufacturing, computation, and robotics. In the case of fluid injection devices, hierarchical catalyst architectures, and certain biomedical materials, NICE is already leading to products that are ready for industrial adoption, or are in an advanced stage of development. The timeframe of large-scale incorporation of NICE as a design framework for industrial applications will depend on the maturity of the sector, and how risk averse or progressive that sector is. In bulk process engineering, several years might be required until NICE designs are implemented, due to the fear of adopting unconventional technology, unless thoroughly tested. Nevertheless, even there, NICE is a toolbox that may result in great benefits with little modification, as the examples in catalysis and fluidization demonstrate. Cost reduction, ease of scale-up, and stable, reliable operations are drivers to meet environmental, economical, and safety challenges. In the distributed energy, specialties, fine chemicals, and biomedical sectors, NICE is an enabler for new technology, as well as offering significant improvement over existing processes and products. The fact that nature contains examples so much ahead of current technology (materials properties, systems behavior, scalability, resilience, or efficiency) is enough of a reason to probe the underlying mechanisms to inspire innovation, and NICE offers a uniquely systematic methodology to do so.

Acknowledgments The authors gratefully acknowledge the financial support from an EPSRC “Frontier Engineering” Award (EP/K038656/1).

References [1] J. Garcı´a-Serna, L. Pe´rez-Barrigo´n, M.J. Cocero, New trends for design towards sustainability in chemical engineering: green engineering, Chemical Engineering Journal 133 (1) (2007) 7e30. [2] R. Carson, Silent Spring, Hamish Hamilton, London, 1963 xix + 304 pp. [3] R.J. Batterham, Sustainabilitydthe next chapter, Chemical Engineering Science 61 (13) (2006) 4188e4193. [4] G.H. Brundtland, UN World Commission on Environment and Development: Our Common Future, Oxford University Press, Oxford; New York, 1987. [5] D.M. Liverman, M.E. Hanson, B.J. Brown, R.W. Merideth, Global sustainability: toward measurement, Environmental Management 12 (2) (1988) 133e143. [6] A.S. McKim, Overcoming sustainability barriers within the chemical industry, Current Opinion in Green and Sustainable Chemistry 14 (2018) 10e13. [7] M. Narodoslawsky, Chemical engineering in a sustainable economy, Chemical Engineering Research and Design 91 (10) (2013) 2021e2028. [8] A.S. Perera, M.-O. Coppens, Re-designing materials for biomedical applications: from biomimicry to nature-inspired chemical engineering, Philosophical Transactions of the Royal Society A 377 (2018) 20180268. [9] J. Aizenberg, P. Fratzl, Biological and biomimetic materials, Advanced Materials 21 (4) (2009) 387e388. [10] E. Dujardin, S. Mann, Bio-inspired materials chemistry, Advanced Materials 14 (11) (2002) 775e788. [11] P. Fratzl, Biomimetic materials research: what can we really learn from nature’s structural materials? Journal of The Royal Society Interface 4 (15) (2007) 637e642. [12] Y.F. Fu, C.Q. Yuan, X.Q. Bai, Marine drag reduction of shark skin inspired riblet surfaces, Biosurface and Biotribology 3 (1) (2017) 11e24. [13] J. Oeffner, G.V. Lauder, The hydrodynamic function of shark skin and two biomimetic applications, The Journal of Experimental Biology 215 (5) (2012) 785e795. [14] X. Pu, G. Li, Y. Liu, Progress and perspective of studies on biomimetic shark skin drag reduction, ChemBioEng Reviews 3 (1) (2016) 26e40. [15] L. Wen, J.C. Weaver, G.V. Lauder, Biomimetic shark skin: design, fabrication and hydrodynamic function, The Journal of Experimental Biology 217 (10) (2014) 1656e1666. [16] M.-O. Coppens, A nature-inspired approach to reactor and catalysis engineering, Current Opinion in Chemical Engineering 1 (3) (2012) 281e289. [17] P. Trogadas, M.M. Nigra, M.-O. Coppens, Nature-inspired optimization of hierarchical porous media for catalytic and separation processes, New Journal of Chemistry 40 (5) (2016) 4016e4026. [18] E. Arzt, Biological and artificial attachment devices: lessons for materials scientists from flies and geckos, Materials Science and Engineering: C 26 (8) (2006) 1245e1250. [19] M.A. Meyers, P.-Y. Chen, M.I. Lopez, Y. Seki, A.Y.M. Lin, Biological materials: a materials science approach, Journal of the Mechanical Behavior of Biomedical Materials 4 (5) (2011) 626e657. [20] U. Hanefeld, L. Cao, E. Magner, Enzyme immobilisation: fundamentals and application, Chemical Society Reviews 42 (15) (2013) 6211e6212. [21] U. Hanefeld, L. Gardossi, E. Magner, Understanding enzyme immobilisation, Chemical Society Reviews 38 (2) (2009) 453e468. [22] R.A. Sheldon, S. van Pelt, Enzyme immobilisation in biocatalysis: why, what and how, Chemical Society Reviews 42 (15) (2013) 6223e6235. [23] D.N. Tran, K.J. Balkus, Perspective of recent progress in immobilization of enzymes, ACS Catalysis 1 (8) (2011) 956e968. [24] L. Cao, Immobilised enzymes: science or art? Current Opinion in Chemical Biology 9 (2) (2005) 217e226. ´ . Berenguer-Murcia, R. Torres, R. Ferna´ndez-Lafuente, Modifying enzyme activity and selectivity by [25] R.C. Rodrigues, C. Ortiz, A immobilization, Chemical Society Reviews 42 (15) (2013) 6290e6307.

REFERENCES

29

[26] M.M. Lynch, J. Liu, M. Nigra, M.-O. Coppens, Chaperonin-Inspired pH protection by mesoporous silica SBA-15 on myoglobin and lysozyme, Langmuir 32 (37) (2016) 9604e9610. [27] K. Braig, Z. Otwinowski, R. Hegde, D.C. Boisvert, A. Joachimiak, A.L. Horwich, P.B. Sigler, The crystal structure of the bacterial chaperonin ˚ , Nature 371 (1994) 578. GroEL at 2.8 A [28] G.G. Tartaglia, C.M. Dobson, F.U. Hartl, M. Vendruscolo, Physicochemical determinants of chaperone requirements, Journal of Molecular Biology 400 (3) (2010) 579e588. [29] F. Marras, J. Wang, M.-O. Coppens, J.N.H. Reek, Ordered mesoporous materials as solid supports for rhodiumediphosphine catalysts with remarkable hydroformylation activity, Chemical Communications 46 (35) (2010) 6587e6589. [30] J.D. Bass, A. Solovyov, A.J. Pascall, A. Katz, AcidBase bifunctional and dielectric outer-sphere effects in heterogeneous catalysis: a comparative investigation of model primary amine catalysts, Journal of the American Chemical Society 128 (11) (2006) 3737e3747. [31] A. Katz, M.E. Davis, Molecular imprinting of bulk, microporous silica, Nature 403 (2000) 286. [32] J.-M. Ha, A. Solovyov, A. Katz, Synthesis and characterization of accessible metal surfaces in calixarene-bound gold nanoparticles, Langmuir 25 (18) (2009) 10548e10553. [33] N. de Silva, J.-M. Ha, A. Solovyov, M.M. Nigra, I. Ogino, S.W. Yeh, K.A. Durkin, A. Katz, A bioinspired approach for controlling accessibility in calix[4]arene-bound metal cluster catalysts, Nature Chemistry 2 (2010) 1062. [34] M.M. Nigra, A.J. Yeh, A. Okrut, A.G. DiPasquale, S.W. Yeh, A. Solovyov, A. Katz, Accessible gold clusters using calix[4]arene N-heterocyclic carbene and phosphine ligands, Dalton Transactions 42 (35) (2013) 12762e12771. [35] M.-O. Coppens, G. Ye, Nature-Inspired optimization of transport in porous media, in: A. Bunde, et al. (Eds.), Diffusive Spreading in Nature, Technology and Society, Springer International Publishing, Cham, 2018, pp. 203e232. [36] G. Wang, E. Johannessen, C.R. Kleijn, S.W. de Leeuw, M.-O. Coppens, Optimizing transport in nanostructured catalysts: a computational study, Chemical Engineering Science 62 (18) (2007) 5110e5116. [37] S. Gheorghiu, M.-O. Coppens, Optimal bimodal pore networks for heterogeneous catalysis, AIChE Journal 50 (4) (2004) 812e820. [38] G. Wang, M.-O. Coppens, Calculation of the optimal macropore size in nanoporous catalysts and its application to DeNOx catalysis, Industrial & Engineering Chemistry Research 47 (11) (2008) 3847e3855. [39] G. Ye, X. Zhou, W. Yuan, M.-O. Coppens, Probing pore blocking effects on multiphase reactions within porous catalyst particles using a discrete model, AIChE Journal 62 (2) (2016) 451e460. [40] G. Ye, X. Zhou, J. Zhou, W. Yuan, M.-O. Coppens, Influence of catalyst pore network structure on the hysteresis of multiphase reactions, AIChE Journal 63 (1) (2017) 78e86. [41] Y. Liu, J. Goebl, Y. Yin, Templated synthesis of nanostructured materials, Chemical Society Reviews 42 (7) (2013) 2610e2653. [42] C. Perego, R. Millini, Porous materials in catalysis: challenges for mesoporous materials, Chemical Society Reviews 42 (9) (2013) 3956e3976. [43] J. Pe´rez-Ramı´rez, C.H. Christensen, K. Egeblad, C.H. Christensen, J.C. Groen, Hierarchical zeolites: enhanced utilisation of microporous crystals in catalysis by advances in materials design, Chemical Society Reviews 37 (11) (2008) 2530e2542. [44] P. Trogadas, V. Ramani, P. Strasser, T.F. Fuller, M.-O. Coppens, Hierarchically structured nanomaterials for electrochemical energy conversion, Angewandte Chemie International Edition 55 (1) (2015) 122e148. [45] A. Walcarius, Mesoporous materials and electrochemistry, Chemical Society Reviews 42 (9) (2013) 4098e4140. [46] F. Larachi, R. Hannaoui, P. Horgue, F. Augier, Y. Haroun, S. Youssef, E. Rosenberg, M. Prat, M. Quintard, X-ray micro-tomography and pore network modeling of single-phase fixed-bed reactors, Chemical Engineering Journal 240 (2014) 290e306.  epa´nek, P. Koc´ı, M. Marek, M. Kubı´cek, Evaluation of local pore sizes and transport properties in porous catalysts, Chemical [47] V. Nova´k, F. St Engineering Science 65 (7) (2010) 2352e2360. [48] P. Trogadas, O.O. Taiwo, B. Tjaden, T.P. Neville, S. Yun, J. Parrondo, V. Ramani, M.-O. Coppens, D.J.L. Brett, P.R. Shearing, X-ray micro-tomography as a diagnostic tool for the electrode degradation in vanadium redox flow batteries, Electrochemistry Communications 48 (2014) 155e159. [49] D. Jin, G. Ye, J. Zheng, W. Yang, K. Zhu, M.-O. Coppens, X. Zhou, Hierarchical silicoaluminophosphate catalysts with enhanced hydroisomerization selectivity by directing the orientated assembly of premanufactured building blocks, ACS Catalysis 7 (9) (2017) 5887e5902. [50] P. Trogadas, J.I.S. Cho, T.P. Neville, J. Marquis, B. Wu, D.J.L. Brett, M.O. Coppens, A lung-inspired approach to scalable and robust fuel cell design, Energy & Environmental Science 11 (1) (2018) 136e143. [51] K. Wu, L. de Martı´n, M.-O. Coppens, Pattern formation in pulsed gas-solid fluidized beds e the role of granular solid mechanics, Chemical Engineering Journal 329 (2017) 4e14. [52] K. Wu, L. de Martı´n, L. Mazzei, M.-O. Coppens, Pattern formation in fluidized beds as a tool for model validation: a two-fluid model based study, Powder Technology 295 (2016) 35e42. [53] S. Gheorghiu, S. Kjelstrup, P. Pfeifer, M.O. Coppens, Is the lung an optimal gas exchanger? in: G.A. Losa, et al. (Eds.), Fractals in Biology and Medicine Birkha¨user Basel, Basel, 2005, pp. 31e42. [54] B. Mauroy, M. Filoche, E.R. Weibel, B. Sapoval, An optimal bronchial tree may be dangerous, Nature 427 (2004) 633. [55] B. Sapoval, M. Filoche, E.R. Weibel, Smaller is betterdbut not too small: a physical scale for the design of the mammalian pulmonary acinus, Proceedings of the National Academy of Sciences 99 (16) (2002) 10411e10416. [56] S. Kjelstrup, M.-O. Coppens, J.G. Pharoah, P. Pfeifer, Nature-Inspired energy- and material-efficient design of a polymer electrolyte membrane fuel cell, Energy & Fuels 24 (9) (2010) 5097e5108. [57] T. Yoshida, K. Kojima, Toyota MIRAI fuel cell vehicle and progress toward a future hydrogen society, The Electrochemical Society Interface 24 (2) (2015) 45e49. [58] A.K. Capulli, M.Y. Emmert, F.S. Pasqualini, D. Kehl, E. Caliskan, J.U. Lind, S.P. Sheehy, S.J. Park, S. Ahn, B. Weber, J.A. Goss, S.P. Hoerstrup, K.K. Parker, JetValve: rapid manufacturing of biohybrid scaffolds for biomimetic heart valve replacement, Biomaterials 133 (2017) 229e241. [59] D.E. Ingber, Developmentally inspired human ‘organs on chips’, Development 145 (16) (2018) p. dev156125. [60] B.M. Maoz, A. Herland, E.A. FitzGerald, T. Grevesse, C. Vidoudez, A.R. Pacheco, S.P. Sheehy, T.-E. Park, S. Dauth, R. Mannix, N. Budnik, K. Shores, A. Cho, J.C. Nawroth, D. Segre`, B. Budnik, D.E. Ingber, K.K. Parker, A linked organ-on-chip model of the human neurovascular unit reveals the metabolic coupling of endothelial and neuronal cells, Nature Biotechnology 36 (2018) 865.

30

2. NATURE-INSPIRED CHEMICAL ENGINEERING: A NEW DESIGN METHODOLOGY FOR SUSTAINABILITY

[61] S. Musah, N. Dimitrakakis, D.M. Camacho, G.M. Church, D.E. Ingber, Directed differentiation of human induced pluripotent stem cells into mature kidney podocytes and establishment of a Glomerulus Chip, Nature Protocols 13 (7) (2018) 1662e1685. [62] A. Sydney Gladman, E.A. Matsumoto, R.G. Nuzzo, L. Mahadevan, J.A. Lewis, Biomimetic 4D printing, Nature Materials 15 (2016) 413. [63] B.S. Gomes, B. Simo˜es, P.M. Mendes, The increasing dynamic, functional complexity of bio-interface materials, Nature Reviews Chemistry 2 (2018) 0120. [64] G. Domel August, M. Saadat, C. Weaver James, H. Haj-Hariri, K. Bertoldi, V. Lauder George, Shark skin-inspired designs that improve aerodynamic performance, Journal of The Royal Society Interface 15 (139) (2018) 20170828. [65] O.Z. Fisher, A. Khademhosseini, R. Langer, N.A. Peppas, Bioinspired materials for controlling stem cell fate, Accounts of Chemical Research 43 (3) (2010) 419e428. [66] L. Wen, J.C. Weaver, P.J.M. Thornycroft, G.V. Lauder, Hydrodynamic function of biomimetic shark skin: effect of denticle pattern and spacing, Bioinspiration & Biomimetics 10 (6) (2015) 066010. [67] B. Bhushan, Bioinspired structured surfaces, Langmuir 28 (3) (2012) 1698e1714. [68] R. Chen, C.-a. Wang, Y. Huang, H. Le, An efficient biomimetic process for fabrication of artificial nacre with ordered-nanostructure, Materials Science and Engineering: C 28 (2) (2008) 218e222. [69] A. Finnemore, P. Cunha, T. Shean, S. Vignolini, S. Guldin, M. Oyen, U. Steiner, Biomimetic layer-by-layer assembly of artificial nacre, Nature Communications 3 (2012) 966. [70] G.X. Gu, F. Libonati, S.D. Wettermark, M.J. Buehler, Printing nature: unraveling the role of nacre’s mineral bridges, Journal of the Mechanical Behavior of Biomedical Materials 76 (2017) 135e144. [71] T. Kokubo, H.-M. Kim, M. Kawashita, Novel bioactive materials with different mechanical properties, Biomaterials 24 (13) (2003) 2161e2175. [72] G.M. Luz, J.F. Mano, Biomimetic design of materials and biomaterials inspired by the structure of nacre, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences 367 (1893) (2009) 1587e1605. [73] E. Munch, M.E. Launey, D.H. Alsem, E. Saiz, A.P. Tomsia, R.O. Ritchie, Tough, bio-inspired hybrid materials, Science 322 (5907) (2008) 1516e1520. [74] J. Wang, Q. Cheng, Z. Tang, Layered nanocomposites inspired by the structure and mechanical properties of nacre, Chemical Society Reviews 41 (3) (2012) 1111e1129. [75] S. Xia, Z. Wang, H. Chen, W. Fu, J. Wang, Z. Li, L. Jiang, Nanoasperity: structure origin of nacre-inspired nanocomposites, ACS Nano 9 (2) (2015) 2167e2172. [76] H.-B. Yao, H.-Y. Fang, X.-H. Wang, S.-H. Yu, Hierarchical assembly of micro-/nano-building blocks: bio-inspired rigid structural functional materials, Chemical Society Reviews 40 (7) (2011) 3764e3785. [77] J. Zhang, W. Feng, H. Zhang, Z. Wang, H.A. Calcaterra, B. Yeom, P.A. Hu, N.A. Kotov, Multiscale deformations lead to high toughness and circularly polarized emission in helical nacre-like fibres, Nature Communications 7 (2016) 10701. [78] D. Zhao, V. Gimenez-Pinto, A.M. Jimenez, L. Zhao, J. Jestin, S.K. Kumar, B. Kuei, E.D. Gomez, A.S. Prasad, L.S. Schadler, M.M. Khani, B.C. Benicewicz, Tunable multiscale nanoparticle ordering by polymer crystallization, ACS Central Science 3 (7) (2017) 751e758. [79] H. Zhao, L. Guo, Nacre-Inspired structural composites: performance-enhancement strategy and perspective, Advanced Materials 29 (45) (2017) 1702903. [80] H. Zhao, Z. Yang, L. Guo, Nacre-inspired composites with different macroscopic dimensions: strategies for improved mechanical performance and applications, NPG Asia Materials 10 (4) (2018) 1e22. ´ lvarez, E. Arzt, Patterned surfaces with pillars with controlled 3d tip geometry mimicking bioattachment [81] A. del Campo, C. Greiner, I. A devices, Advanced Materials 19 (15) (2007) 1973e1977. [82] C. Greiner, E. Arzt, A. del Campo, Hierarchical gecko-like adhesives, Advanced Materials 21 (4) (2009) 479e482. [83] A. Mahdavi, L. Ferreira, C. Sundback, J.W. Nichol, E.P. Chan, D.J.D. Carter, C.J. Bettinger, S. Patanavanich, L. Chignozha, E. Ben-Joseph, A. Galakatos, H. Pryor, I. Pomerantseva, P.T. Masiakos, W. Faquin, A. Zumbuehl, S. Hong, J. Borenstein, J. Vacanti, R. Langer, J.M. Karp, A biodegradable and biocompatible gecko-inspired tissue adhesive, Proceedings of the National Academy of Sciences 105 (7) (2008) 2307e2312. [84] S. Sethi, L. Ge, L. Ci, P.M. Ajayan, A. Dhinojwala, Gecko-Inspired carbon nanotube-based self-cleaning adhesives, Nano Letters 8 (3) (2008) 822e825. [85] R. Cutkosky Mark, Climbing with adhesion: from bioinspiration to biounderstanding, Interface Focus 5 (4) (2015) 20150015. [86] L. Ripley Renee, B. Bhushan, Bioarchitecture: bioinspired art and architectureda perspective, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences 374 (2073) (2016) 20160192. [87] C. Audibert, J. Chaves-Jacob, J.-M. Linares, Q.-A. Lopez, Bio-inspired method based on bone architecture to optimize the structure of mechanical workspieces, Materials & Design 160 (2018) 708e717. [88] A. Cannavale, F. Fiorito, M. Manca, G. Tortorici, R. Cingolani, G. Gigli, Multifunctional bioinspired sol-gel coatings for architectural glasses, Building and Environment 45 (5) (2010) 1233e1243. [89] A. Gamage, R. Hyde, A model based on Biomimicry to enhance ecologically sustainable design, Architectural Science Review 55 (3) (2012) 224e235. [90] B. Han, L. Zhang, J. Ou, Future developments and challenges of smart and multifunctional concrete, in: Smart and Multifunctional Concrete toward Sustainable Infrastructures, Springer Singapore, Singapore, 2017, pp. 391e400. [91] G. John, D. Clements-Croome, G. Jeronimidis, Sustainable building solutions: a review of lessons from the natural world, Building and Environment 40 (3) (2005) 319e328. [92] K. Klang, G. Bauer, N. Toader, C. Lauer, K. Termin, S. Schmier, D. Kovaleva, W. Haase, C. Berthold, K.G. Nickel, T. Speck, W. Sobek, Plants and animals as source of inspiration for energy dissipation in load bearing systems and facades, in: J. Knippers, K.G. Nickel, T. Speck (Eds.), Biomimetic Research for Architecture and Building Construction: Biological Design and Integrative Structures, Springer International Publishing, Cham, 2016, pp. 109e133. [93] M. Mirkhalaf, A.K. Dastjerdi, F. Barthelat, Overcoming the brittleness of glass through bio-inspiration and micro-architecture, Nature Communications 5 (2014) 3166.

REFERENCES

31

[94] F. Natalio, T.P. Corrales, M. Pantho¨fer, D. Schollmeyer, I. Lieberwirth, W.E.G. Mu¨ller, M. Kappl, H.-J. Butt, W. Tremel, Flexible minerals: selfassembled calcite spicules with extreme bending strength, Science 339 (6125) (2013) 1298e1302. [95] M. Seifan, A.K. Samani, A. Berenjian, Bioconcrete: next generation of self-healing concrete, Applied Microbiology and Biotechnology 100 (6) (2016) 2591e2602. [96] P. Vukusic, J.R. Sambles, Photonic structures in biology, Nature 424 (2003) 852. [97] Y. Xing, P. Jones, M. Bosch, I. Donnison, M. Spear, G. Ormondroyd, Exploring design principles of biological and living building envelopes: what can we learn from plant cell walls? Intelligent Buildings International 10 (2) (2018) 78e102. [98] M.P. Zari, Biomimetic design for climate change adaptation and mitigation, Architectural Science Review 53 (2) (2010) 172e183.