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Biotechnology Advances xxx (2014) xxx–xxx
JBA-06846; No of Pages 12
Contents lists available at ScienceDirect
Biotechnology Advances
j ourna l homepage: www.e lsev ie r .com/ locate /b iotechadv
Research review paper
Product and technology innovation: What can biomimicry inspire?
F
Elena Lurie-Luke ⁎P&G Life Sciences C + D (Open Innovation), UK
⁎ Procter & Gamble, Whitehall Lane, Egham, Surrey TWE-mail address: [email protected].
http://dx.doi.org/10.1016/j.biotechadv.2014.10.0020734-9750/© 2014 Elsevier Inc. All rights reserved.
Please cite this article as: Lurie-Luke E, Prodx.doi.org/10.1016/j.biotechadv.2014.10.002
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Article history:Received 23 July 2014Received in revised form 3 October 2014Accepted 6 October 2014Available online xxxx
Keywords:BiomimicryInnovationSmart materialsSurface modificationMovementSensorsRoboticsEnvironmental technologiesBiodiversity
PROBiomimicry (bio- meaning life in Greek, and -mimesis, meaning to copy) is a growing field that seeks to interpo-
late natural biological mechanisms and structures into a wide range of applications. The rise of interest inbiomimicry in recent years has provided a fertile ground for innovation. This review provides an eco-systembased analysis of biomimicry inspired technology and product innovation. A multi-disciplinary framework hasbeen developed to accomplish this analysis and the findings focus on the areas that have been most strikinglyaffected by the application of biomimicry and also highlight the emerging trends and opportunity areas.
© 2014 Elsevier Inc. All rights reserved.
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Contents
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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Data collection methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Diversity of species inspiring the biomimicry based innovation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0What are the most successful areas of biomimicry applications? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
Material development inspired by biomimicry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Smart materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Materials based on surface modification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Material architectures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Materials with targeted applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
Locomotion inspired by biomimicry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Movement kinetics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Release motion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Shapes enhancing movement performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
What are the emerging trends in biomimicry applications? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Smart material . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
Self-assembled materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Dynamic optical materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
Sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Acoustic sensing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Chemical sensing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Temperature sensing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
What are the untapped areas in biomimicry applications? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Process inspired biomimicry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
Environmentally friendly process and anti-pollution technologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Energy production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
20 9NW, UK. Tel.: +44 1784 474518.
duct and technology innovation: What can biomimicry inspire?, Biotechnol Adv (2014), http://
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Behaviour & cognition applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Software development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Computer and robotics development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
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Introduction
Biological systems are the result of 3.8 billion years of evolution.Humans have long relied on lessons derived from the organisms aroundthem. One of the earliest of Greek legends centres on the attempt byDaedalus and his son, Icarus, to mimic the flight of birds to escapetheir island prison (Ovid, 2004). In the Renaissance, one of Leonardoda Vinci's most famous inventions was a flying machine which mim-icked his observations of the movements of birds and bats (Taylor,2009). More recently, in the 20th century, George de Mestral, a Swissengineer was walking in the Alps and was intrigued by the mechanismby which burrs attached to his dog's fur. After studying their mode ofattachment, he was inspired to create Velcro which closely imitatedthis property (Benyus, 2002).
Inmodern science, the search for biomimetic applications has devel-oped into a scientific discipline and biomimicry based innovations arenow the subject of systematic study (Ball, 2001; Benyus, 2002; CBID,n.d.; Swiegers, 2012; Vogel and Davis, 1998; Wyss, n.d.) Learning fromthese concepts may drive a significant shift in modern science(Aizenberg et al., 2004; Grinthal et al., 2012; Smith, 2006; Vogel,2013). The underlying methodology of biomimicry is to gain an under-standing of the fundamental principles of a biological process or adapta-tion and to subsequently adapt these concepts for bio-inspired productapplications or to solve specific technical challenges (Agnarssonet al., 2009; Assous et al., 2008; Bar-Cohen, 2006; Epstein, 2010;Holten-Anderson, 2011; Gattiker, 2005; Schmitz et al, 2012). Therise of interest in biomimicry in recent years has provided a fertileground for a number of product innovations (Biolytix, n.d.; Eaton,2009; FastSkinz, n.d.; Gymnobot, 2009; Karr, 2009; NanoSphere, n.d.).This review provides an eco-system based analysis of biomimicryinspired technology and product innovation (initial base size 222 refer-ences). A multi-disciplinary framework has been developed to accom-plish this analysis and the findings focus on the areas that have beenmost strikingly affected by the application of biomimicry and also high-light the emerging trends and opportunity areas. For the purposes ofthis review, references dealing with synthetic biology and industrialbiotechnology have been excluded from the discussion.
An analysis of bioinspired innovations can be approached from avariety of angles, focusing on organism groupings, the stage of develop-ment or the properties of the innovation. Innovations can be alsocategorised based on the nature of the source of inspiration: how thingsare created in nature (materials), how organisms sense their environ-ment (sensors), how they move in their environment (biomechanicsand kinetics) and how they behave and function (processes). The find-ings of this analysis focus on the areas that have been most strikinglyaffected by the application of biomimicry and also highlight the emerg-ing trends and opportunity areas.
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Data collection methodology
A simple search using ‘biomimicry’ as a search string has resulted inmore than a million hits on Google and few hundred publications indifferent scientific publications ranging from Nature to Journal of Trans-portation. Therefore, it was essential to develop amethodology to collectthe relevant data references and create a meaningful data set of refer-ences to accomplish the aim of this review — biomimicry inspired
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innovation, i.e. a translation of the research into a product application.It was also important to look at different stages of the biomimicry rele-vant developments — from an idea stage to a marketed product. Theabove points could be addressed only by collecting data from multiplesources to create a holistic view of the biomimicry space (eco-system).
The data collection was done in partnership with a companyspecialising in mapping business, technologies, and products environ-ments using its unique proprietary platform for data collection and anintuitive visualisation tool (the Visual Insights interface). It also madeit possible to access different data sources that was not possible to dousing a single search engine or/and databases.
The references databasewas created using a set of specifically devel-oped search strings and involved the following steps:
1. Assessment of different web-based sources: magazines, websites,databases, blogs;
2. Text analysis algorithms using the company's proprietary smartsemanticweb crawling, scrapers to access any kind of freely availabledatabase on the web and application programming interfaces toaccess both free and paid databases, web applications and socialnetworks;
3. Development of a visual representation of the biomimicryeco-systemdifferent levels of thedata break downs, i.e. fromcategorysub segments to individual companies/technologies.
Subsequent to the development of this eco-system, a substantialeffort wasmade to complimentmachine intelligence with human intel-ligence and further refine the data set of references to select the appro-priate references for the analysis. This included an in-depth profiling ofthe eco-system and development of the taxonomy to address specificobjectives of the review. The 101 references selected for this review(including theweb references in the text) aim to provide an overall per-spective on biomimicry inspired innovationwith 71% beingpublicationsin peer-review journals including books and patents and 29% beingwebbased references where 15% corresponds to the product web sites and14% refers to different research activities related to biomimicry.
Diversity of species inspiring the biomimicry based innovation
The data analysis illustrates the diversity of species that haveinspired the biomimicry approach (Fig. 1). Due to the diversity of lifeforms (species) ranging from the basic structural, functional and biolog-ical unit (cells) to humans, it was difficult to derive to the same taxono-my principles across the full data set. To give a representation ofdifferent species, a further break down was done for the animal king-dom: the phylum of the species (Fig. 1a) and their taxonomic groupings(Fig. 1b). Examining the data set reveals the most inspiring species interms of variety of applications and a number of references are plantsand insects (Fig. 1). The large numbers and variety of innovationsinspired by these groupsmay be a consequence of two factors, diversityand survival capacity. While it is difficult to make a correlation betweennumbers of species in each class and a number of biomimicry refer-ences, it is worthwhile to note that these groups are relatively large,have a global distribution and consequently possess a high degree ofdiversity, thereby providing a greater resource for researchers. Forexample, there are estimated to be ~1,000,000 species of insects andaround ~300,000 plant species (Chapman, 2009). In addition, these
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Fig. 1. Diversity of organisms that have inspired the biomimicry approach ranging from the basic structural, functional and biological unit (cells) to humans (base size: 218 references).a: Diversity of different life forms that have inspired the biomimicry (* cells are included for a completeness of representations of the biomimicry inspiration). b: Diversity of classes in theanimal kingdom that have inspired the biomimicry approach.
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Fig. 2. Biomimicry applications per different areas and their developmental stage. Successof biomimicry applications has been assessed based on a variety of biomimicry applica-tions and ability to translate biomimicry application into products and technologies(base size: 218 references).
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Rorganisms exhibit remarkable survivalmethods for their environments,for example, the high reproductive capacity of insects also promotesdiversity and adaptation and as for plants, they are unable to moveeven in response to changes in their environment and have to adaptin situ in order to survive (Attenborough, 1995).
What are the most successful areas of biomimicry applications?
For the purpose of this review, the most successful areas ofbiomimicry applications have been defined as the areas that have alarge variety of biomimicry applications and the best track record oftranslating biomimicry application into products and technologies.These areas relate to material design and locomotion (movement)(Fig. 2).
Material development inspired by biomimicry
Material development seems to be the largest area of biomimicryresearch, accounting for approximately 50% of all reviewed references.Biomimicry based material design can be broadly categorised into fourgroups: (i) smart materials inspired by nature's ability to react andchange in response to external stimuli; (ii) surface modificationswhich include novel surface topographies with improved functions;
Please cite this article as: Lurie-Luke E, Product and technology innovation: What can biomimicry inspire?, Biotechnol Adv (2014), http://dx.doi.org/10.1016/j.biotechadv.2014.10.002
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(iii) material architectures which feature novel shapes and structuralarrangements and (iv) technologies which are based on enhancingexisting systems using specific parameters of an adaptation (ratherthan developing an entirely new technological platform). This hasbeen successfully translated into new opportunities for material devel-opment across a range of fields, including optical materials, medicine,agriculture, textiles and coating materials (Fig. 3).
Smart materialsThe ability of an organism to change certain parameters and charac-
teristics in response to a range of chemical, mechanical and environ-mental conditions provides endless opportunities for the developmentof smart materials, a class of materials with dynamic parameters thatare capable of responding reversibly to changes within their surround-ing environment. The biomimicry inspired smart material innovationswere grouped based on a type (nature) of the stimuli that promptsthe changes and split into two groups — chemical stimuli and physicalstimuli.
Chemical stimuli are detected by specific receptors and can inducehighly specific responses within an organism. Mimicry of the responseof species to various chemical stimuli may lead to the development ofvarious technologies associated with pollution detection and materialdesign. The most common chemical stimuli which have inspiredbiomimicry applications are pH changes and metal ions.
Natural cells can extract signals from the surfaces that they come incontact with. This could be the mechanical, chemical, spatial, and eventemporal information from the surface that they can process on andreact to. Gaining an understanding of how this information is processedcould enable the development of “smart surfaces” which encodeinstructions for specific cell behaviour. To unravel this mechanism, theAizenberg lab has utilised a technique that allows the construction ofdifferent nanostructured surfaces with a variety of chemical and struc-tural combinations. Sensing mechanisms of cilia on fish and amphibianskin inspired a development of hydrogel-actuated integrated respon-sive systems (HAIRS). HAIRS can change from contraction to swellingwith a change of pH: the contraction of the hydrogel and the bending
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Fig. 3. Examples of variety of biomimicry applications formaterial development. Biomimicry basnature's ability to react and change in response to external stimuli; surface modifications whicfeature novel shapes and structural arrangements and biomimetic technologies which are base
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of microstructures in acidic conditions, and swelling and straighteningunder alkaline conditions (Zarzar et al., 2011).
Another example of pH responsive materials is a development ofnew adhesive agents inspired by mussel species to form strong, revers-ible bonds to their substrates. Mussels utilise an iron ligand whichmeans the resulting bonds exhibit both strength and reversibility.Scientists at the University of Chicago have used this to create a newsynthetic mussel-inspired material that exhibits both strength andreversibility (Holten-Anderson et al., 2011). One of the central compo-nents of the synthetic version is a polymer that, when combined withmetal salts at a lowpH isfluid in its nature.When, however, the solutionismixedwith sodiumhydroxide to raise the pH, the solution transformsinto a gel. This technology would be able to address limitation of manyexisting synthetic coatings that rely on permanent covalent bonds.Potential applications of this technology include an adhesive or coatingfor underwater machinery, or in a biomedical setting as a surgical adhe-sive or bonding agent for implants.
Metal ions present another example of chemical stimuli used in thedevelopment of biomimicry inspired smart materials. In fish, colourchange can be regulated by motor proteins that disperse skin pigmentcrystals along the microtubule cytoskeleton and are regulated by acomplex signalling network. Experiments have demonstrated that it ispossible to reengineer this protein structure to generate a switch ableto turn nanofluidic devices on and off using zinc ions (Greene et al.,2008). In addition to zinc ions, calcium ions can be also exploited inthe regulation of biomimetic materials. The forisome, a protein struc-ture found in a variety of plants, responds to injury by swelling inresponse to increases in cytosolic calcium. This swelling prevents theplant from losing nutrients. The development of a chemically stableartificial forisome could lead to a system that can integrate sensingwith actions and further advancements in the design of smart materials(Shen et al., 2006).
Physical stimuli can range from light to heat and water content.Examples presented in this section focus mainly on temperature andhydrophobicity and the visible light induced changes are discussed inthe section dealing the emerging trends in biomimicry applications.
edmaterial design can be broadly categorised into four groups: smartmaterials inspired byh includes novel surface topographies with improved functions; structural designs whichd on enhancing existing systems using specific parameters of an adaptation.
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Organisms have developed various systems to detect temperaturechanges that range from simple temperature fluctuations to infrared(IR) waves. These systems can provide an interesting source of inspira-tion for the development of a variety of technologies that can enhancetextile design and improve energy efficiency. Unique ability to focusand direct IR radiation by the lobster eye has inspired IRLens™ technol-ogy that mimics this system to direct and focus IR radiation. It is alreadybeing exploited in the development of energy-efficient gas and electricheaters (Radiant Optics, n.d.).
A change in hydrophobicity canmodify properties of someof naturalfibres. For example, spider silk contracts in response to humidity chang-es. A series of powerful cyclic contractions, in response to changes inhumidity, generate a performance 50 times greater than the equivalenthuman muscle tissue. This performance capability is observed across arange of spatial scales which is a significant advantage over currentvoltage-driven polymer muscles and could provide opportunities fornovel artificial muscle developments (Agnarsson et al., 2009). Cellulosefibres can also alter their properties in response to the changes in hydro-phobicity. Mimicking tunicate cellulose found in sessile sea squirts ledto a development of advanced brain electrodes. These electrodes usecellulose nanofibres and are stiff and inflexible when initially implantedbut subsequently soften in contact with water (Capadona et al., 2008).In addition to properties' alterations, hydrophobicity changes couldalso result into specific actions like the “pine cone effect”. The “pinecone effect” is the mechanism by which, in response to changes inhumidity, pine cones are able to “open” and “close” allowing thedispersal of seeds. Fabrics have been developed that are able to respondin a similar manner to micro-climate changes, with the textile structureitself opening when damp and closing when dry (Inotec, n.d.). Plantsphysiological response to physical changes, in this case osmotic pres-sure, provided an insight for another smart textile development.Stomatex® textile consists of a pattern of dome-shaped chamberseach with a small pore that mimics behaviour of certain plant coolingbehaviour and may have the potential to overcome over-heatingand perspiration problems associated with a range of textiles(Stomatex, n.d.).
Materials based on surface modificationNatural topographies and their inherent functionality provide a
source of inspiration for designing novel surface modification materials(Wong et al., 2011). Nature offers a variety of solutions to achieve differ-ent surfaces properties including repellent, drag reduction, anti-bacterial and anti-reflective properties.
A large number of biomimicry efforts are in the area of repellentsurfaces, in particular, water repellence. The majority of plants possessa waxy cuticle over the epidermis of leaves, rendering them highlyhydrophobic and thereby allowing water to easily run-off. The Lotusleaf effect has already been utilised to develop a number of water repel-lent technologies (Lin et al., 2011) and products, Lotusan® (StolitLotusan, n.d.), NanoSphere® (NanoSphere, n.d.) and Greenshield®(Greenshield, n.d.). Bacterial biofilms are, perhaps, an unexpectedsource of inspiration. Bacterial biofilms are found in a diverse array ofenvironments, from teeth to water pipes, and are all too often highlyimpervious to anti-microbial treatments. Investigations of bacterialcommunities have shown a multiscale slime-like matrix that is able torepel water, in addition to a variety of other liquids, including ethanoland acetone (Epstein et al., 2010, 2012). Further development of tech-nologies based on biofilm topography may yield a new generation ofwater and chemical resistant materials.
Similarly to plants, butterfly and cicadawings are able to direct rain-drops away from the insect's body through tiny ratchet-like surfacestructures. Structures of moth eyes and cicada wings have inspired adevelopment of self-cleaning coatings (Sun et al., 2008). In addition topossessing a self-cleaning function, the nanostructure of the moth eyehas an anti-reflective surface that reduces glare and thus enhancestheir ability to hide from predators. A group of researchers in Japan
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has created a new synthetic film to cover solar cells which can reducethe amount of reflected light and thus enhance efficiency. It is estimatedthat this innovation can improve the efficiency of solar cells by up to 6%(Yamada et al., 2011).
Anti-fouling skin properties of shark skin has led to the developmentof Sharklet® technology platform (Sharklet, n.d.) and other technolo-gies (A⁎STAR, 2010) with anti-bacterial properties where surface mod-ification properties prevent bacteria to adhere to the surface. While theabovementioned approaches aim to prevent the adhesion of unwantedspecies, there are a number of cases when it is desirable to create sur-faces with increased adhesive properties, for instance, the developmentof climbing robots, attaching everyday objects such as lights to walls,and in the development of new gloves for climbers. Geckos have longbeen of interest to researchers due to their ability to stick to a range ofsurfaces and easily break free to move. The footpad of the geckocontains microscale and nanoscale filamentous structures that canmodulate the surface area in contact with any given substrate. Asynthetic polymer stamp has been developed which mimics thisprocess. On the underside are four pyramidal-shaped rubber tipswhich, when pressed firmly against a surface, expand and thus increasethe area of contact (Kim et al., 2010; Soto et al., 2010).
Aerodynamic and hydrodynamic structures in nature aim to mini-mise the effect of drag, which can significantly reduce the efficiency ofmovement. Mimicry of nature's solutions to develop surfaces withdrag reduction properties could significantly increase fuel efficiencyfor transport vehicles operating in different physical environments(Stenzel et al., 2011). Shark skin, in addition to possessing innate anti-bacterial properties, has also low drag, enabling it to swim moresmoothly through water. An experimental film has been developedwhich is able to coat the blades of wind turbines and thus enhancetheir efficiency (Shaffer, 2011). The same idea is also been applied toMPG-Plus™, a drag-reducing technology, that is applied to vehicles(Eaton, 2009; FastSkinz, n.d.; Salaverry, 2012).
Material architecturesWithin nature there are amyriad of designswhichprovide optimisa-
tion for their function. The mimicry of these designs may have thepotential to give rise to a variety of new material architectures withapplications across a range of industries. Natural endo- and exoskele-tons are a good starting point for the development of strong materials.The skeletons of birds are lightweight andmany bones are pneumatisedand feature criss-crossing internal structures to increase their strength.The evolution of bone shapes and material properties played an impor-tant role in flight evolution and are helping to lead to new lightweightstructures for aeroplanes (Dumont, 2010).
Another example of natural structural adaptations enabling flying isbeetle elytra. Beetle elytra (hardened modified forewings) consist oftwo layers which maintain their integrity through a series ofinterconnecting attachments. The structure and ability of the elytra toresist high pressures may inspire new materials for the constructionindustry. It could lead to the development of stronger materials thatwould be better able to resist sharing force (Fan et al., 2005). The struc-tural adaptions to the high pressure are also exhibited by the humanteeth. Human teeth are able to resist high stresses exerted throughouta lifetime's worth of eating. The exteriors of human teeth featurenetworks of microcracks, which can gradually repair themselves overtime. The outer layers of the tooth consist of layers offibres andmatriceswhich optimise integrity, with the microcracks absorbing pressure andthus preventing major cracking. This ability may eventually be replicat-ed in new synthetic material design to develop lighter aircraft wingsthat could better able to resist mechanical stresses (Lawn et al., 2010).
A lot may be gained through replicating the natural photonic struc-tures and development of novel nanoscale structures (Kolle et al.,2013). For example, multiple layers of guanine crystals in fish are akey component in the coloured and silver reflections seen in manyspecies. The optical properties of brittlestars have nanoscale microlense
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structures. Analogous synthetic structures based on these designs,known as inverse opals, may be of use in the development of newoptic materials (Swiegers, 2012).
Materials with targeted applicationsIn certain instances, biomimicry approaches have been used for
specific (targeted) applications, compared to the technology platformsdiscussed above. The difference lies in the development of new innova-tions for the enhancement of existing technologies. A range of thesedevelopment is very diverse: new anti-cancer drugs based on allicin, anaturally occurring defence compound found in plants including garlicand onions where it functions to kill soil fungi, bacteria and parasites(Rabinkov et al., 2008); new bioadhesives based on bivalve mollusks(Stevens et al., 2007); novel anti-microbial technologies (Bauer andMathesius, 2004; Todd et al., 2007); formulation of stabilisation agentsinspired by seeds that can be kept in hot and dry conditions for extend-ed periods (Stabilitech, n.d.); ceramic designs based on seashell struc-tures (Launey et al., 2010); a highly effective insect repellingbiopesticide that utilises an ingredient isolated from catmint (Karr,2009).
Locomotion inspired by biomimicry
Animal locomotion models provide the second biggest area forbiomimicry applications. Insights into the general principles that under-lie movement, the mechanisms and structures of muscular and skeletalsystems provide insights that can be applied to increase the efficiency ofmoving vehicles, especially in robotics, or help to inspire entirely newmodes of transport. The biomimicry applications of movement arediscussed based on a type of improved ‘mobility’ performance:(1) improvement based on movement kinetics, (2) improvementbased releasemechanisms (means of dispersal across an environment),and (3) improvements based on structural configuration (energyefficient shapes).
Movement kineticsThe ability to move is one of themost obvious features of the animal
kingdom and it can be achieved through a variety of mechanismsand across all three physical environments: in water, in the air, andon/through the ground. Humans are perhaps unique as an individualspecies in seeking to operate across all of these environments but arenot ideally adapted for any. A better understanding of movement adap-tations in specific physical environment could lead to increase the effi-ciency of man-made moving vehicles operating in air, water and onthe ground.
A range of aquatic organisms have inspired improvements in watertransport systems, especially swimming robots, e.g. Gymnobot, a robotwhich models the mode of swimming of the knifefish (Collins et al.,2008; Gymnobot, 2009). Gymnobot possesses a single undulating finalong the length of its body. This design is thought to be more energyefficient than conventional propellers and allows the small robot tonavigate very shallow water. The robot may have applications, in addi-tion to being a model for an alternative transport mechanism, in thestudy of biodiversity in shallows, and as a pollution monitor.
The challenges of movement in air are, in many ways, similarto those faced by aquatic organisms. Streamlined design is vital toreduce drag and thus save energy. But in the air, birds must also gener-ate lift, whereas in water, this is provided by the media itself. There areseveral different mechanisms of flight utilised by animals in the naturalworld, including powered flight, gliding and hovering, as well asanimals that move in both air and water. The common swift hasinspired the RoboSwift, a micro aeroplane with moveable wings. TheRoboSwift is able to fold its feathers back, altering its wing area andcamber in a manner that mimic the swift's efficient flight model(RoboSwift, n.d.).
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On-the-ground movement equally has a range of mechanisms thatcan employ different muscle architectures to achieve a range of gaits.Cockroaches have six small legs which move approximately sixteentimes a second. Studying their movement has led to the design anddevelopment of iSprawl, small hexapedal robots, which are an idealmodel to test concepts about robotic and natural locomotion dynamicsand the optimal arrangement of legs iSprawl (iSprawl, n.d.).
Many animals are capable of using their limbs to strongly grip arange of surfaces and these abilities are of interest to researchers fortheir potential applications in robotics and prosthetics that can beadaptable and flexible in order to achieve a range of different grips.Cockroaches have inspired a robotic hand design due to their ability towalk on uneven surfaces (Dollar and Howe, 2010). Themarine environ-ment has also inspired advances in robotic limb design. One novelconcept is a prosthesis that looks and functions in a similar manner toa tentacle, by being highly flexible and adjustable and possessing anadaptive grip (Trivedi et al., 2008).
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Release motionAnimals and plants employ a range of release and delivery (dispers-
al) mechanisms. They can range from the generation of liquid jets forpropulsion or a defence mechanism to the needle like structuresfound in stinging insects. Modelling these mechanisms and structurescan have applications in medicine, e.g. NanoCyte, a new drug deliverytechnology based on microinjectors found in sea anemones(NanoCyte, n.d.); mosquito-inspired new needle designs (Chakrabortyand Tsuchiya, 2008; Gattiker et al., 2005; Izumi et al., 2011); agriculture,e.g. irrigation devices based on plant dispersal mechanism (Vogel,2003) and platform technologies with multiple application areas, e.g.the μMist® spray technology with a valve controlled delivery systemwhich copies the bombardier beetle's defence mechanism (Mcintoshand Beheshti, 2008).
Shapes enhancing movement performanceIn addition to understanding the mechanisms and structures of
muscular and skeletal systems, organisms have developed specificfeatures that help them to move in their environment or enhance themechanisms by which this is achieved. Understanding these propertiesmight give rise to innovations ranging from new building designs(Vázquez, 2014), and improved transport technologies (Lee, n.d.).Classic examples include curved shapes of aerofoils and hydrofoilswhich mimic the structure of bird wings (State, 2004). Spinning seedsby plants inspired single-bladed helicopters (Aron, 2011).
Natural shapes have been also applied in developing alternativeenergy technologies. For example, a novel blade structure, modelledon the shape of humpback whale flippers can enhance the efficiencyof tidal energy generation (Choi et al., 2012). The Phillips Head Protec-tion system was modelled based on a human scalp where the skin onthe outside of the thick skull bone provides additional protection eachtime when the head receives an impact. The Philips Head Protectionsystem provides protection to motorcycle riders from impact traumaby helping to reduce cranial trauma in a variety of circumstances(Phillips Head, n.d.).
What are the emerging trends in biomimicry applications?
Emerging trends in biomimicry application refer to the areas thatalready have a number of interesting biomimicry developments andwould benefit from further translation to industrial applications.(Fig. 2) These areas largely focus on the exploitation of the ability oforganisms to sense and react to their environment that could be appliedin the development of smart materials, in particular self-assembly andoptical materials, and also sensors design.
tion: What can biomimicry inspire?, Biotechnol Adv (2014), http://
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Smart material
Self-assembled materialsMaterial development presents the largest area for biomimicry
applications and not surprisingly it has both already successful applica-tions as well as emerging ones. As discussed in the previous sectionsmart materials have been developed based on the ability of many ofthe biological processes to demonstrate significant responses to certainkey stimuli, whether chemical, physical or environmental. Other func-tions of biological systems, such as cellular signalling or the self-assembly of complexmolecular and tissue level structures, may providemodels and concepts for further biomimetic innovations. The self-assembly of biological structures is an interesting phenomena in natureand is defined as the ability of a system to adopt a specific structuralarrangement, or pattern, without external influences.
Self-assembly of cellulose microfibrils in plants provides a goodexample of self-assembly in nature and could lead to useful insightsfor fibre design. Cellulose is one of the most profuse polysaccharidesin nature and has a high commercial importance. However, relativelylittle is known about its polymerisation and self-assembly at the plasmamembrane. Better understanding of the molecular mechanisms ofdifferent processes associated with the cellulose microfibrils includingits self-assembly could provide inspiration to design novel fibre mate-rials (The Swedish Center for Biomimetic Fiber Engineering, n.d.).Beetles' tarsi present another example of self-assembly where theirtarsi consist of hair-like structures that exhibit highly controlled self-organisation. Research into these structures has helped scientists todevelop novel synthetic nanofibres capable of mimicking this property(Grinthal et al., 2012).
Cellular communication can be one of the forces responsible for self-assembly. The principles of cellular communication were used to devel-op biomimetic microcapsules. The communication between microcap-sules happen through the chemical mechanism: in simulations,agonist particles are released by microcapsules and can be tracked andfollowed by a second set of microcapsules. The collective dynamics ofthese microcapsules is achieved via hydrodynamic interactions andthe feedback mechanism provided by the dissolved particles(Kolmakov et al., 2010).
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Another emerging area of smart material design is the developmentof novel dynamic optical materials. In addition to the optical materialdesign based on surface modification, the other areas include colourchanges induced by visible light used as camouflage for survival, abilityto selectively diffuse light as a communication tool and different irides-cent properties.
Camouflage-capable organisms are able to change their colour usingadaptive colouration induced by visible light (Hanlon, 2007). The colourchange in cuttlefish can happen either by colourant transportationwhere a colour change is achieved by compacting or spreading pigment(the chromatophores function) or/and by producing structural colourwhere a colour change is a result of optical interference (the iridophoresand leucophores function) (Cloney and Brocco, 1983 and Sutherlandet al., 2008). The latter mechanism has inspired the development of anelectronic ink for a new generation of television screens that is capableof producing images using very low voltages. At rest, in the absence ofan electrical charge, the screen is clear; as the electrical charge increases,the poly-2-vinyl expands, becoming increasingly thick and thusreflecting longer wavelengths of light. This type of screens can reflectnon-visible wavelengths, including parts of the infrared and ultravioletspectra, dependent on voltage. Thewhole screen is capable of producingimages using very low voltages, primarily because it reflects light, ratherthan emitting it (Walish et al, 2009). Developments in this area maylead to the creation of new dynamic optical materials, such as energy-saving window coatings that can alter their transparency in response
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to various environmental stimuli (Chan et al., 2013 and Vasquez et al.,2014).
Some living organisms are able to produce visible light for intra- andinter-specific communication. The marine snail, Hinea brasiliana, is onesuch bioluminescent organism, which is capable of producing a lumi-nous display when it is mechanically stimulated by interactions withother motile marine organisms. The mechanisms by which this processoccurs are yet to be fully characterised but it has been suggested that theability may be linked to layers of deposited calcium, rather than thepresence of overlaying pigment cells. This ability to selectively diffuselightmay have applications in developing new light fittings and sensorsthat are able to diffuse light without requiring energy (Deheyn andWilson, 2011).
β-Keratin nanofibres on the feather tips of blue penguins produce anon-iridescent colour by scattering light. Biophotonic nanostructuresmodelled on this may be of use as a colouring agent in a range of prod-ucts for the textile and automotive industry (D'Alba et al., 2011; Prumet al., 2009). The opposite effect, iridescent, is also of interest to thebiomimicry applications. Iridescent blue-leaved plants can be found inthe understory of rainforests where the property of iridescence mayprovide a photoprotective function. These photoprotective propertiescan be further explored in the development of coating materials forhighly sensitive light sensors and photosensitive surfaces (Thomaset al., 2010).
Sensors
The ability of an organism to efficiently gather information about itssurrounding environment from a variety of sources is an integral part oftheir existence (living) and plays an important role in their ability tosurvive. Organisms are able to sense a range of physical, chemical andtactile signals in their environment. Interpreting these signals is ofvital importance to the organisms for their communication, behaviouralresponses, hunting for food and avoiding predators. Frequently, organ-isms can possess detection systems with unique structural adaptationsthat may be able to enhance current technologies (Ayers et al., 2005).Mimicking the visual system of the bumblebee, the Nissan MotorCompanydeveloped a laser range finder to improve the crash avoidancesystem (Nissan, 2008). The current sensor developments are based onthe understanding of different sensing mechanisms in the areas ofacoustics, chemical, temperature and electric waves sensing.
Acoustic sensingAcoustic sensing is based upon the use of sound for the identification
of objects in an organism's path. This adaptation is frequently associatedwith a range of bat species flying at nightwhen flight vision is not useful(Gao et al., 2011). A number of technology developments could benefitfrom the re-application of the bat's sensing technique in particular inthe areas of novel navigation system (Moore, 2008) and improvingthe ability of autonomous vehicles to avoid collisions (Assous et al.,2008).
Chemical sensingAll organisms possess, to some degree, a mechanism to sense
chemicals and odours in their surrounding environments. Thechemosensory abilities of plankton species enable communication intheir aquatic ecosystem (Larsoon and Dobson, 1993). Lobsters are capa-ble of detecting trace odours in their surroundings, despite the strongcurrents to which they are frequently exposed (Reidenbach and Koehl,2011). Seabirds possess a highly developed olfactory system that assiststhem in navigation (Wallgraff and Andreae, 2000). Improving ourunderstanding of how certain organisms achieve this so efficiently orso accurately might lead to the development of novel new chemo-based sensors. For example, many species are able to readily detectlow level changes in CO2 and gaining a thorough understanding of themechanism by which this is achieved may be of use in developing
tion: What can biomimicry inspire?, Biotechnol Adv (2014), http://
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new chemical sensors for atmospheric pollutants or toxic compounds inthe environment.
Temperature sensingOrganisms can respond to changes in temperature and some of the
mechanisms bywhich changes are detectedmay be of use in the devel-opment of novel synthetic sensors that might be in homes to activatefans or heating. Snakes possess a unique sensory system for the detec-tion of IR. Infrared signals are detected by a specialised facial structure(the pit organ) which can activate a temperature sensitive ion channel(Gracheva et al., 2010). The jewel beetle also demonstrates an innateability to detect infrared light to locate burnt wood in which to lay itseggs. Their sense organs include pits which contain large numbers ofmodified mechanosensors. Researchers at the University of Bonn haveengineered its biomimicry application using a series a polyethyleneplate instead of a cuticle layer. This innovation may be produced morecheaply than commercially available IR sensors, although the newsystem is not as sensitive as current sensors (Schmitz et al., 2012).
What are the untapped areas in biomimicry applications?
The untapped areas of biomimicry applicationswere classified as theareaswith a relatively small number of publications andwhere the largeproportions of references refer to an idea stage. These areas refer tobiomimicry applications dealing with organisms' ability to utilise theirenvironment and studies of animal behaviour and cognition (Fig. 2).
Process inspired biomimicry
Environmentally friendly process and anti-pollution technologiesA range of organisms create compounds from materials in their im-
mediate environment (Ball, 2001). The processes by which this isachieved can provide inspiration for a series ofmanufacturing processesin industry. For example, corals are able to incorporate carbon dioxidepresent in their immediate surroundings into layers of stable minerals.Over time, significant amounts of carbon dioxide are naturally absorbedby the oceans and converted in such a manner. Now, a new technologyhas been developed that can enhance these processes. Key to this is theformation of novel, metastable calcium and magnesium carbonate andbicarbonates similar to those found in corals and the skeletons ofother marine organisms. This technology may mean that it is possibleto produce new building materials in an environmentally sustainablemanner (Calera, n.d.).
Metabolism processes of a number of microorganisms could alsoprovide an inspiration for a development of different environmentaltechnologies. These technologies may enhance our ability to offset theconsequences of climate change, pollution and loss of fresh water.Heavy metal contamination of water is a common problem associatedwith industrial pollution. Researchers at the University of Californiahave noted a novel natural process by which such contaminants maysuccessfully be removed. This process is based on the understandingof the processes of how sulphate-reducing bacteria release sulphidewhich can bind and sequester zinc (Moreau et al., 2007). Using bacteriafor metal extraction has been used already in the mining industry asthey can break up metal oxides to release copper, cobalt, nickel andother metals from old mining sites (Dicks, 2004).
Toxic aromatic compounds such as benzene and toluene can alsosignificantly pollute bodies of water. Bacteria again may play a role intheir removal by using a multicomponent dioxygenase enzyme system(Nishino and Spain, 2002). In nature, the majority of decompositionoccurs in oxygen rich humus on dry land and less frequently in water.Biolytix water treatment technology models this by separating solidorganic waste from liquid. The solid waste is subsequently convertedrapidly into humus by the action of a range of microorganisms. Thehumus then acts to oxygenate and clean the water (Biolytix, n.d.).
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Microorganisms may also be key to the development of newtechnologies for the removal of harmful radiation. The black fungushas been collected from the Chernobyl nuclear site and was found topossess unusually high levels of melanin. Melanin (a pigment alsofound in human skin) apparently served to capture energy from radia-tion and convert it to metabolic energy in a similar manner to chloro-phyll capturing sunlight in plants (O'Connell, 2007).
Energy productionBioenergy, often used interchangeably with green energy produc-
tion, is one of several key areas of research in the quest for sustainableand efficient power generation. In nature, photosynthesis is able to ulti-mately generate energy for plants and underlies the survival of commu-nities. Similarly, micro-organisms are often able to generate theirenergy from other sources, such as sulphur-fixing bacteria and thosespecies found in hydrothermal vents. A number of approaches havebeen taken to mimic some of these abilities and to generate newadvanced microbial fuel cells (EcoVolt, n.d.; Oh et al., 2010; Rabaeyand Verstraete, 2005).
Rising levels of carbon dioxide in the atmosphere are now widelyaccepted as one of the principal causes of climatic forcing. However, asynthetic foam based on a semi-tropical frog species has now beendeveloped that captures energy and may help to reduce excess carbondioxide in the atmosphere. Researchers have developed a new artificialphotosynthetic material which utilises enzymes from a range of organ-isms, trapped within foam, to produce sugars from sunlight and carbondioxide. The design of the foamnests is based on the Tungara frogwhichcreates long-lived foams to protect its developing tadpoles. The foamsystem possesses many advantages over creating similar systems withnatural organisms which must use much of the energy they produceto maintain life. The foam can be used in a range of environments andmay be a viable manner to economically produce energy and reduceatmospheric carbon dioxide (Wendell et al., 2010).
Plants have also directly inspired solar cell design, potentially gener-ating cheaper alternatives to silicon-based photovoltaics. Conventionalsolar panels capture and utilise light energy in a highly purifiedmaterialwhose creation requires large energy inputs and a range of toxicsolvents. In the future, however, dye-sensitive solar cells based onplant photosynthetic compounds may be used which can be highlyflexible and more readily incorporated into existing buildings and intowindow panes, building paints and textiles (Service, 2011).
Behaviour & cognition applications
TransportAnimals frequently display a range of altruistic and cooperative
behaviours which may be adapted for human systems. Army ants, forexample, may provide inspiration for improved transportation strate-gies by setting rules for behaviour and self-organisation. Ants' armycan include up to 200,000 ants often moving in opposite directions.Key to their regulation is the behavioural difference between antswith and without food. Ants returning successfully with food from ahunting expedition are less likely to deviate in their path following thepheromone trail of ants in front of them. Ants travelling away withoutfood are more likely to move aside. The result of this is a middle laneof ants carrying food back, and two outer lanes of unburdened antsmoving in the opposite direction. Computer modelling has demonstrat-ed that as behavioural differences between burdened and unburdenedants decrease, the efficiency of the three-lane system declines (Couzinand Franks, 2003).
Software developmentAnts also provide the inspiration for new software design and are
used in a model to prevent computer infection by viruses. Ants rapidlyrespond to threats and then quickly resume their original behaviouronce the threat has subsided. The same behaviour has been applied to
tion: What can biomimicry inspire?, Biotechnol Adv (2014), http://
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a computer system featuring digital ants looking for threats. As theymove about the network, they leave digital trails similar to ant phero-mone trails. Stronger trails, which attract more attention, are left byants that identify evidence of infection (Haack et al., 2011).
Biological mechanisms can be also applied to better organise wire-less networks. For example, the fruit fly nervous system may help inthe development of new computer algorithms. For several decades,computer scientists have been faced with the problem of how proces-sors are able to best select a maximal independent set. The standardselection processes entails complicated communication across thenetwork and requires all processors to know in advance their methodof connection. This can be a problem for wireless sensor networks, assensors may be distributed randomly and may not easily communicatedirectly with one another. In the fruit fly, there is a similar arrangementwherebymultiple tiny bristles are used to sense the outsideworld. Eachsensory bristle develops from a sensory organ precursorwhich connectsto adjoining nerve cells but not directly to other precursor cells. A smallnumber of cells in the developing nervous system act as leaders andprovide direct communication with every other cell, a much simplerand more robust methodology than standard human conceptions.An algorithm has been developed which mimics this approach(Navlakha and Bar-Joseph, 2011).
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Computer and robotics developmentBiomimicry approaches are being used for computer hardware
design (Smith, 2006). There are processes which, as yet, computersare less efficient compared to mammal brains including plasticity andthe ability to perform many operations simultaneously. A computerdesign approach has been suggested that mimics synopses inneuromorphic circuits using memristors (Jo et al., 2010). Memristorsare dynamical devices with resistances that change their parameterswhen the voltages and/or electric current applied across them andthat remember their history when the electric power supply is turnedoff (Borghetti et al., 2010). It has been shown that this new system iscapable of amemory and learningprocess (Jo et al., 2010) and its furtherdevelopments could provide an opportunity to build a computer thatwill operate in a similar way to mammal brains.
The behaviours of ants and cells are the source of inspiration forimproved efficiencies in robotics. Individual ants or cells have a limitednumber of functions and abilities but collectively can carry out a range
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Fig. 4. Examples of variety of biomimicry applications inspired by plants: Plants are one of threferences. The large numbers and variety of innovations inspired by this group may be a conare unable to move even in response to changes in their environment, they endure and adapt
Please cite this article as: Lurie-Luke E, Product and technology innovadx.doi.org/10.1016/j.biotechadv.2014.10.002
of behaviours. These are being modelled in engineering modules, eachlimited to its own particular task, which can then be assembled to createlarger systems which can adapt to particular environments. Robotic“swarms” are also being designed to perform group tasks (Werfelet al., 2014).
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Conclusions
A product development starts with an initial concept defining thekey performance benefits, and biomimicry offers the experiences ofbillions of years of evolution as a source of inspiration. Since earlyhuman civilisation has developed, mankind has adopted and adaptedideas seen in nature. For example, Fig. 4 illustrates a variety ofbiomimicry applications inspired by plants. Eventually this search forinspiration and the subsequent development of new technologies hasbecome systematised and is now an effective pathway for new productdevelopment. Collectively, these results indicate that there is stillconsiderable further work required in order to bring more products tomarket but that significant new developments are being made. Largenumbers of prototypes are in development in various fields, especiallyin robotics.
In addition to improved technology efficiency, biomimicry approachcan also provide a source of inspiration for the diversity of technologydevelopment. The latter could be driven by a vast range of naturaldesigns, mechanical features, materials as well as different ways ofhow nature and humans invent things, e.g. examples listed by Vogeland Davis (Vogel and Davis, 1998) include few right angles in naturewhile they are almost everywhere in human constructions, naturemostly creates wet and flexible structures while humans' one are dryand stiff.
Biomimicry research is focused not only on the materials utilised byorganisms but also on their sensing, movement, behaviour and process-es. A large number of innovations are currently being developed whichrely on novel surface structures. Many of these function on a similarprinciple between different industries. For example, the topographicalstructures with repelling properties can be used in textiles and implantdevices and create surfaces that are capable of preventing microbialgrowth and biofilm formation. Work on biological sensors is primarilyfocused on the development of new navigation equipment which willsignificantly benefit the shipping, motor and airline industries. In the
e most biomimicry inspiring species in terms of variety of applications and a number ofsequence of two factors, diversity (~300,000 plant species) and survival capacity (plantsin situ in order to survive).
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field ofmovement, themajority ofwork is in the development of roboticprototypes. These prototypesmay eventually be developed into devicesthat can be used in a variety of industries including dealingwith hazard-ous waste, new transport technologies and improved production lineefficiency. Ability to translate our understanding of how organismsinteract with their environment provide a prolific ground for the devel-opment of environmental technologies, both focussing onmore sustain-ablemanufacturing processes and anti-pollution technologies. Researchin behaviour and cognition stimulates innovations in the digital space.
It is also interesting to look at the type of species that have inspiredinnovation across different areas. Furthermore, this may serve to betterhighlight species uponwhich it is best to focus for further developmentsin specific fields. For example, in material design arthropod and plantspecies have led to the greatest number of ideas, research and proto-types. Frequently this is due to their surface structures which areadapted to specific functions in line with a given environment, forexample, water repellence. Within sensing, however, the most inspira-tional species are principallymammalian (primarily in thedevelopmentof acoustic sensors) and also to a lesser extent, crustaceans. In behav-iour, microorganisms are the most inspirational species with insectsalso generating significant areas for new research. Insects have alsoinspired the most innovations in movement, often in the design ofnew robotic prototypes.
The development of biomimicry applications can be a long andfailure-prone path but the rewards are tantalising due to the ability totranslate biomimicry inspired designs into new products or technologyplatforms that can significantly enhance existing knowledge. The num-ber of ideas is likely to frequently increase as our understanding of thenatural world improves.There are a range of technology platformswhich are yet to be fully adopted but may eventually achieve the ubiq-uity of Velcro, one of the earliest of the biomimicry based innovations.Many ideas are still subject to on-going research, but innovations devel-oped by this approach are now beginning to be brought to market andapplied in existing systems. IRLenses™, inspired by the unique proper-ties of the lobster's eye, is one such success story, and is being appliedin new energy-efficient heating systems (Radiant Optics, n.d.).Sharklet®, modelled on shark denticles may prove to be an effectiveantibacterial surface with wide applications (Sharklet, n.d.). MPG-Plus™, a novel surface design also based on shark skin,may significantlyenhance the fuel efficiencies of new vehicles (Eaton, 2009; FastSkinz,n.d.; Salaverry, 2012). Biomimicry application led to the developmentof a new generation of textile designs, e.g. Stomatex® (Stomatex,n.d.), Inotek ™ (Inotek, n.d.).
Biomimicry has revealed new opportunities for material develop-ment across a range of fields, including optics, medicine, agriculture,energy generation, textiles, transport aids and construction. Fullyexploiting the range of structures on offer in nature presents theunique opportunity to utilise our environment in a new, safe andenvironmentally-sustainable manner.
Acknowledgement
I would like to thank Prof. Keith Lindsey (Durham University),Prof Nigel Robinson (Durham University), Dr. Bob Leboeuf (P&G) andDr. Bob Isfort (P&G) for their support in my work on this article.
References
A*STAR. Singapore consortium learns from nature to produce new chemical-free,anti-bacteria plastic ‘skins’ [press-release]. Retrieved from http://bit.ly/WmkNAj,2010. [Dec 06, Last accessed 6th July 2014].
Agnarsson I, Dhinojwala A, Sahni V, Blackledge TA. Spider silk as a novel high perfor-mance biomimetic muscle driven by humidity. J Exp Biol 2009;212:1990–4.
Aizenberg J, Livage J, Mann S. New developments in bio-related materials. J Mater Chem2004;14:E5–6.
Aron J. Spinning seeds inspire single-bladed helicopters [NewScientist on-line]. Retrievedfrom http://www.newscientist.com/article/dn20045-spinning-seeds-inspire-singlebladed-helicopters.html, 2011. [Jan 28, Last accessed 6th July 2014].
Please cite this article as: Lurie-Luke E, Product and technology innovadx.doi.org/10.1016/j.biotechadv.2014.10.002
ED P
RO
OF
Assous S, Jackson P, Hopper C, Gunn D, Rees J, Lovell M. Bat-inspired distance measure-ments using phase information. J Acoust Soc Am 2008;124:596–2598.
Attenborough D. The private life of plants: a natural history of plant behaviour. 1st ed.Princeton: Princeton University Press; 1995.
Ayers J, Witting J, Ryder S, Olcott C. Process and architecture of robotic system to mimicanimal behavior in the natural environment. US Patent 8 494 676; Mar 24, 2005.
Ball P. Life's lessons in design. Nature 2001;409:413–6.Bar-Cohen Y. Biomimetics: biologically inspired technologies. 1st ed. Boca Raton: Taylor &
Francis; 2006.Bauer WD, Mathesius U. Plant responses to bacterial quorum sensing signals. Curr Opin
Plant Biol 2004;7(4):429–33.Benyus JM. Biomimicry: innovation inspired by nature. 1st ed. NewYork: Perennial; 2002.Biolytix. Biolytix incorporated nature's time-tested strategies into its patented biopod
[information on page]. Retrieved from http://www.biolytix.com/. [(n.d.), Lastaccessed 6th July 2014].
Borghetti J, Snider GS, Kuekes PJ, Yang JJ, Stewart DR, Williams RS. ‘Memristive’ switchesenable ‘stateful’ logic operations via material implication. Nature 2010;464:873–6.
Calera. The special form of calcium carbonate that Calera makes in its process alsomimics or copies the form of calcium carbonate that marine organisms use tomake their shells and other structures [Information on a page]. Retrieved fromhttp://www.calera.com/site/beneficial-reuse-of-co2/science.html. [(n.d.), Lastaccessed 6th July 2014].
Capadona JR, Shanmuganathan K, Tyler DJ, Rowan SJ, Weder C. Stimuli-responsivepolymer nanocomposites inspired by the sea cucumber dermis. Science 2008;319:1370–4.
CBID: Center for Biologically Inspired Design. Examining biomaterials provides insightsinto how to design materials that are differentially sensitive to forces along certaindirections, which can reduce weight and material usage in structures [informationon a page]. Retrieved from http://www.cbid.gatech.edu/biomimetic.html. [(n.d.),Last accessed 6th July 2014].
Chakraborty S, Tsuchiya K. Development and fluidic simulation of microneedlesfor painless pathological interfacing with living systems. J Appl Phys 2008;103:114701.
Chan EP, Walish JJ, Urbas AM, Thomas EL. Mechanochromic photonic gels. Adv Mater2013;25(29):3934–47.
Chapman AD. Number of living species in Australia and the world. 2nd ed. Toowoomb:Australia Biodiversity Information Service; 2009.
Choi H, Park H, Sagong W, Lee S. Biomimetic flow control based on morphologicalfeatures of living creatures. Phys Fluids 2012;24:121302.
Cloney RA, Brocco SL. Chromatophore organs, reflector cells, iridocytes and leucophoresin cephalopods. Am Zool 1983;23(3):581–92.
Collins K, Foerster F, Dolan S, Bowyer A, Megill W. Kinematics and force characterisationof a knifefish-inspired mechanical propulsor. Proceedings Biological Approaches forEngineering. University of Southampton: Institute of Sound and Vibration Research;2008. p. 30–3. [Retrieved from http://opus.bath.ac.uk/30129/1/BAEC.pdf. Lastaccessed 6th July 2014].
Couzin I, Franks N. Self-organized lane formation and optimized traffic flow in army ants.Proc R Soc 2003;B 270:139–46.
D'Alba L, Saranathan V, Clarke JA, Vinther JA, Prum RO, Shawkey MD. Colour-producingβ-keratin nanofibres in blue penguin (Eudyptula minor) feathers. Biol Lett 2011;7(4):543–6.
Deheyn DD, Wilson NG. Bioluminescent signals spatially amplified by wavelength-specific diffusion through the shell of a marine snail. Proc Biol Sci 2011;278(1715):2112–21.
Dicks L. Marine bugs have a flair for deep-sea mining. New Sci 2004;182:23.Dollar AM, Howe RD. The highly adaptive SDM hand: design and performance evaluation.
Int J Robot Res 2010;29(5):585–97.Dumont ER. Bone density and the lightweight skeletons of birds. Proc R Soc 2010;B 277:
2193–8.Eaton K. Shark-skin inspired car cover improves gas mileage [Information on a page].
Retrieved from http://www.fastcompany.com/1142983/shark-skin-inspired-car-cover-improves-gas-mileage, 2009. [Jan 20, Last accessed 6th July 2014].
EcoVolt Technology. EcoVolt is a wastewater treatment system that leverages electricallyactive microbes to create clean water [information on a page]. Retrieved from http://cambrianinnovation.com/resources/cambrian-technology/. [(n.d.), Last accessed 6thJuly 2014].
Epstein A, Pokroya B, Seminarab A, Aizenberg J. Bacterial biofilm shows persistentresistance to liquid wetting and gas penetration. Proc Natl Acad Sci U S A 2010;108(3):995–1000.
Epstein AK, Wong T-S, Belisle RA, Boggs EM, Aizenberg J. Liquid-infused structuredsurfaces with exceptional anti-biofouling performance. Proc Natl Acad Sci U S A2012;109(33):13182–7.
Fan J, Chen B, Gao Z, Xiang CJ. Mechanisms in failure prevention of bio-materials andbio-structures. Mech Adv Mater Struct 2005;12:229–37.
FastSkinz Inc. FastSkinz Inc. has invented and patented a line of drag-reducing filmsspecifically engineered to noticeably reduce a vehicle's pressure drag [informationon line]. Retrieved from http://fastskinz.com/wordpress. [(n.d.), Last accessed 6thJuly 2014].
Gao L, Balakrishnan S, He W, Yan Z, Muller R. Ear deformations give bats a physicalmechanism for fast adaptation of ultrasonic beam patterns. Phys Rev Lett 2011;107:214301.
Gattiker G, Kaler KVIS, Mintchev MP. Electronic mosquito: designing a semi-invasivemicrosystem for blood sampling, analysis and drug delivery applications. J MicrosystTechnol 2005;12:44–51.
Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G, Chesler AT, et al.Molecular basis of infrared detection by snakes. Nature 2010;464:1006–11.
tion: What can biomimicry inspire?, Biotechnol Adv (2014), http://
T
98798898999099199299399499599699799899910001001100210031004Q1310051006100710081009101010111012101310141015101610171018101910201021102210231024102510261027102810291030103110321033103410351036103710381039104010411042104310441045104610471048104910501051105210531054105510561057105810591060106110621063106410651066106710681069107010711072
10731074107510761077107810791080108110821083108410851086108710881089109010911092109310941095109610971098109911001101110211031104110511061107110811091110111111121113111411151116111711181119112011211122112311241125112611271128112911301131113211331134113511361137113811391140114111421143114411451146114711481149115011511152115311541155115611571158
11E. Lurie-Luke / Biotechnology Advances xxx (2014) xxx–xxx
UNCO
RREC
Greene AC, Trent AM, Bachand GD. Controlling kinesinmotor proteins in nanoengineeredsystems through a metal-binding on/off switch. Biotechnol Bioeng 2008;101:478–86.
GreenShield. Microscopic roughness is the technology behind GreenShield which lever-ages the enormous surface area of each nanoparticle enabling the particles to effi-ciently deliver the appropriate chemistry to the fabric [information on a page].Retrieved from http://www.greenshieldfinish.com/. [(n.d), Last accessed 6th July2014].
Grinthal A, Kang SH, Epstein AK, Aizenberg M, Khan M, Aizenberg J. Steering nanofibers:an integrative approach to bio-inspired fiber fabrication and assembly. Nano Today2012;7(1):35–52.
Gymnobot. Researchers at the University of Bath have used nature for inspiration indesigning a new type of swimming robot which could bring a breakthrough insubmersible technology [information on a page]. Retrieved from http://www.bath.ac.uk/news/2009/09/21/robot-fish/, 2009. [Sep 21, Last accessed 6th July 2014].
Haack JN, Fink GA, Maiden WM, McKinnon AD, Templeton SJ, Fulp EW. Ant-based cybersecurity. In: Latifi S, et al, editors. 8th International Conference on InformationTechnology:NewGenerations. Los Alamitos: IEEE Computer Society; 2011. p. 918–26.
Hanlon RT. Cephalopod dynamic camouflage. Curr Biol 2007;17:R400–4.Holten-Anderson N, Harrington MJ, Birkedal H, Lee BP, Messersmith PB, Lee KYC, et al.
pH-induced metal–ligand cross-links inspired by mussel yield self-healing polymernetworks with near-covalent elastic moduli. Proc Natl Acad Sci U S A 2011;108:2651–5.
Inotek. Inotek™ bi-component fibres are designed to react when exposed to elevatedlevels of relative humidity in a micro-climate [information on a page]. Retrievedfrom http://www.inotektextiles.com/company-news/. [(n.d.), Last accessed 6th July2014].
iSprawl (Independent Sprawl robot). Sprawl robots are designed by inspiration based onstudy of cockroaches. [information on a page]. Retrieved from http://www-cdr.stanford.edu/~sangbae/iSprawl.htm. [(n.d.), Last accessed 6th July 2014].
Izumi H, Suzukia M, Aoyagia S, Kanzakibet T. Realistic imitation of mosquito's proboscis:electrochemically etched sharp and jagged needles and the cooperative insertingmotion. Sensors Actuators A Phys 2011;100:115–23.
Jo SH, Chang T, Ebong I, Bhadviya BB, Mazumder P, Lu W. Nanoscale memristor device assynapse in neuromorphic systems. Nano Lett 2010;10:1297–301.
Karr DA. New innovative use for catmint: DuPont develops new natural insect repellent[Information on a page]. Retrieved from http://bit.ly/1wMlSfK, 2009. [Apr 27, Lastaccessed 6th July 2014].
Kim S,Wub J, Carlsona A, Jina SH, Kovalskya A, Glassc P, et al. Microstructured elastomericsurfaces with reversible adhesion and examples of their use in deterministicassembly by transfer printing. Proc Natl Acad Sci U S A 2010;107(40):17095–100.
Kolle M, Lethbridge A, Kreysing M, Baumberg JJ, Aizenberg J, Vukusic P. Bio-inspiredband-gap tunable elastic optical multilayer fibers. Adv Mater 2013;25(15):2239–45.
Kolmakov G, Yashin VV, Levitan SP, Balazs AC. Designing communicating colonies ofbiomimetic microcapsules. Proc Natl Acad Sci U S A 2010;107:12417–22.
Larsoon P, Dobson S. Chemical communication in planktonic animals. Arch Hydrobiol1993;129(2):129–55.
Launey ME, Munch E, Alsem DH, Saiz E, Tomsia AP, Ritchie RO. A novel biomimeticapproach to the design of high-performance ceramic–metal composites. J R SocInterface 2010;7(46):741–53.
Lawn BR, Lee JJ-W, Chai H. Teeth: among nature's most durable biocomposites. Annu RevMater Res 2010;40:55–75.
Lee B. A. N.T. — Aid Necessities Transporter: the name itself describes that this vehicleadopts styling cues from the aesthetics of ants being a 6-wheeled vehicle with anabdomen-like supply unit [information on a page]. Retrieved from http://bit.ly/1mtgHf5. [(n.d.), Last accessed 6th July 2014].
Lin J, Cai Y, Wang X, Ding B, Yu J, Wang M. Fabrication of biomimetic superhydrophobicsurfaces inspired by lotus leaf and silver ragwort leaf. Nanoscale 2011;3:1258–62.
Mcintosh A, Beheshti N. Drug Deliver. European Patent 193733A1; Jul 2, 2008.Moore NC. Sensors for bat-inspired spy plane under development [information on a
page]. Retrieved from http://bit.ly/1jNVfGJ, 2008. [Mar 13, Last accessed 6th July2014].
Moreau JW, Weber PK, Martin M, Gilbert B, Hutcheon ID, Banfield JF. Extracellularproteins limit the dispersal of biogenic nanoparticles. Science 2007;316(5831):1600–3.
NanoCyte. NanoCyte is leveraging a sophisticated natural injection system that evolvedin sea life over the last 700 million years [information on a page]. Retrieved frohttp://www.nano-cyte.com/technology.html. [(n.d.), Last accessed 6th July 2014].
NanoSphere. NanoSphere is a textile finish based on nanotechnology. It shows high levelof self cleaning, oil and water repellence as well as high abrasion resistance and washpermanence [Information on a page]. Retrieved from http://bit.ly/Uk5Qx5. [(n.d.),Last accessed 6th July 2014].
Navlakha S, Bar-Joseph Z. Algorithms in nature: the convergence of systems biology andcomputational thinking. Mol Syst Biol 2011;7:546.
Nishino SF, Spain JC. Biodegradation, transformation and bioremediation of nitroaromaticcompounds. In: Hurst CH, Knudsen GR, McInerney MJ, Stetzenbach LD, Walter MV,editors. Manual of environmental microbiology. 2nd ed. Washington DC: ASMPress; 2002.
Nissan. Crash avoidance robotic car inspired by flight of the bumblebee [information on apage]. Retrieved from http://www.nissan-global.com/EN/NEWS/2008/_STORY/080926-01-e.html, 2008. [Sep 26, Last accessed 6th July 2014].
O'Connell D. Fungal physiology: radiation junkies. Nat Rev Microbiol 2007;5(7):475.Ovid. Methamorphoses: a new verse translation. 1st ed. London: Penguin Classics; 2004.Phillips Helmets. The Phillips Head Protection System (PHPS) is a revolutionary
advance in head protection inspired by nature [information on a page]. Retrievedfrom http://www.phillipshelmets.com/ABOUT_PHPS.htm. [(n.d.), Last accessed6th July 2014].
Please cite this article as: Lurie-Luke E, Product and technology innovadx.doi.org/10.1016/j.biotechadv.2014.10.002
ED P
RO
OF
Prum RO, Dufresne ER, Quinn T, Waters K. Development of colour-producing β-keratinnanostructures in avian feather barbs. J R Soc Interface 2009;6(2):S253–65.
Rabaey K, Verstraete W. Microbial fuel cells: novel biotechnology for energy generation.Trends Biotechnol 2005;23(6):291–8.
Rabinkov A, Miron T, Mirelma D, Wilchek M. Site-specific in situ generation of allicinusing a targeted alliinase delivery system for the treatment of cancers, tumors, infec-tious diseases and other allicin-sensitive diseases. US Patent 7 445 802B2; Nov 4,2008.
Radiant Optics Inc. Radiant Optics was founded by inventor/entrepreneur Roger Johnsonto capitalize on his lobster-eye inspired compound reflective lens that uniquelyfocuses and directs infrared energy [information on a page]. Retrieved from http://bit.ly/1u5A7jY. [(n.d.), Last accessed 6th July 2014].
Reidenbach MA, Koehl MAR. The spatial and temporal patterns of odors sampled bylobsters and crabs in a turbulent plume. J Exp Biol 2011;214:3138–53.
RoboSwift. RoboSwift is a micro airplane fitted with movable wings, inspired by thecommon swift, one of nature's most efficient flyers. [Information on a page].Retrieved from http://www.roboswift.nl/. [(n.d.), Last accessed 6th July 2014].
Salaverry PC. Vehicle with drag-reducing outer surface (Fastskinz). US Patent 8 141 936B2; Mar 27, 2012.
Schmitz H, Soltner H, Bousack H. Biomimetic infrared sensors based on photomechanicinfrared receptors in pyrophilous (“fire-loving”) insects. IEEE Sensors J 2012;12(2):281–8.
Service RF. Artificial leaf turns sunlight into a cheap energy source. Science 2011;332(6025):25.
Shaffer D. A life-size lab chases the wind [StarTribune: Business on-line]. Retrieved fromhttp://www.startribune.com/business/133262228.html, 2011. [Nov 5, Last accessed6th July 2014].
Sharklet Technologies. The patented, microscopic pattern manufactured by SharkletTechnologies creates a surface upon which bacteria do not like to grow [informationon a page]. Retrieved from http://sharklet.com/technology/. [(n.d.), Last accessed 6thJuly 2014].
Shen AQ, Hamlington BD, Knoblauch M, Peters WS, Pickard WF. Forisome based biomi-metic smart materials. Smart Struct Syst 2006;2:225–36.
Smith LS. Handbook of nature-inspired and innovative computing: integrating classicalmodels with emerging technologies. New York: Springer; 2006.
Soto D, Hill G, Parness A, Esparza N, Cutkosky M, Kenny T. Effect of fibril shape onadhesive properties. Appl Phys Lett 2010;97:53701–4.
Stabilitech. Stabilitech's technology mimics natural phenomena well defined non-toxicand inexpensive chemical excipients [information on a page]. Retrieved from www.stabilitech.com. [(n.d.), Last accessed 6th July 2014].
State P. Airplanewings that change shape like a bird's have scales like a fish [Science Dailyon-line]. Retrieved from http://www.sciencedaily.com/releases/2004/04/040422000037.htm, 2004. [Apr 22, Last accessed 6th July 2014].
Stenzel V,Wilke Y, HageW. Drag-reducing paints for the reduction of fuel consumption inaviation and shipping. Prog Org Coat 2011;70(4):224–9.
Stevens MJ, Steren RE, Hlady V, Stewart RJ. Multiscale structure of the underwateradhesive of californica: a nanostructured latex with a steep microporosity gradient.Langmuir 2007;23:5045–9.
Stolit Lotusan. The exterior textured finish with pronounced self-cleaning properties[technical report]. Retrieved from http://bit.ly/Uj3krk. [(n.d.), Last accessed 6th July2014].
Stomatex. Stomatex is the patented physics that replicates the way that the leaves ofplants transpire [Information on a page]. Retrieved from http://www.stomatex.com/faqs.htm. [(n.d.), Last accessed 6th July 2014].
Sun C-H, Gonzalez A, Linn NC, Jiang P, Jiang B. Templated biomimetic multifunctionalcoatings. Appl Phys Lett 2008;92:51107–10.
Sutherland RL, Mäthger LM, Hanlon RT, Urbas AM, Stone MO. Cephalopod colorationmodel. I. Squid chromatophores and iridophores. J Opt Soc Am 2008;A 25:588–99.
Swiegers GF, editor. Bioinspiration and biomimicry: reverse-engineering nature. 1st ed.New Jersey: John Wiley & Sons Inc.; 2012.
Taylor R. Reflecting the impossible. Nature 2009;460:462.The Swedish Center for Biomimetic Fiber Engineering. Mimicry of the natural self-
assembly of cell wall macromolecules has a high potential to contribute to the futuredevelopment of intelligent nanomaterials[information on a page]. Retrieved fromhttp://www.biomime.org/. [(n.d.), Last accessed 6th July 2014].
Thomas RT, Kolle M, Whitney HM, Glover BJ, Steiner U. Function of blue iridescence intropical understorey plants. J R Soc Interface 2010;7(53):1699–707.
Todd SM, Sonenshine DE, Hynes WL. Tissue and life-stage distribution of a defensin genein the Lone Star tick, Amblyomma americanum. Med Vet Entomol 2007;21:141–7.
Trivedi D, Rahn CD, Kier WM, Walker ID. Soft robotics: biological inspiration, state of theart, and future research. Appl Bionics Biomech 2008;5:99–117.
Vasquez Y, Kolle M, Mishchenko L, Hatton BD, Aizenberg J. Three-phase co-assembly: insitu incorporation of nanoparticles intotunable, highly ordered, porous silica films.ACS Photonics 2014;1:53–60.
Vázquez WM. Metatectonica: further the understanding on biomimicry as one of themost important emergent theories for the future of design and architecture [Blogpost]. Retrieved from http://metatectonica.blogspot.co.uk/, 2014. [Jun 17, Lastaccessed 6th July 2014].
Vogel S. Comparative biomechanics: life's physical world. 2nd ed. Princeton: PrincetonUniversity Press; 2013.
Vogel S, Davis KK. Cats' paws and catapults: mechanical worlds of nature and people. 1sted. New York: W. W. Norton & Company Inc.; 1998.
Walish JJ, Kang Y, Mickiewicz RA, Thomas EL. Bioinspired electrochemically tunable blockcopolymer full color pixels. Adv Mater 2009;21(3):3078–81.
Wallgraff HG, Andreae MO. Spatial gradients in ratios of atmospheric trace gases: a studystimulated by experiments on bird navigation. Tellus Ser B 2000;52:1138–57.
tion: What can biomimicry inspire?, Biotechnol Adv (2014), http://
1159Q1411601161116211631164116511661167
116811691170117111721173117411751176
12 E. Lurie-Luke / Biotechnology Advances xxx (2014) xxx–xxx
Wendell D, Todd J, Montemagno C. Artificial photosynthesis in ranaspumin-2 based foam.Nano Lett 2010;10:3231–6.
Werfel J, Kirstin Petersen K, Nagpal R. Designing collective behavior in a termite-inspiredrobot construction team. Science 2014;343(6172):754–8.
Wong T-S, Kang SH, Tang SKY, Smythe EJ, Hatton BD, Grinthal A, Aizenberg J. Bioinspiredself-repairing slippery surfaces with pressure-stable omniphobicity. Nature 2011;477:443–7.
Wyss Institute For Biologicall Inspired Engineering. Development of p biologicallyinspired materials and devices that will solve critical medical and environmental
UNCO
RRECT
Please cite this article as: Lurie-Luke E, Product and technology innovadx.doi.org/10.1016/j.biotechadv.2014.10.002
problems and translations of these transformative technologies into products thathave an impact on society and the world [information on a page]. Retrieved fromhttp://wyss.harvard.edu/viewpage/264. [(n.d.), Last accessed 6th July 2014].
Yamada N, Ijiro T, Okamoto E, Hayashi K, Masuda H. Characterization of antireflectionmoth-eye film on crystalline silicon photovoltaic module. Opt Express 2011;19:118–25.
Zarzar LD, Kim P, Aizenberg J. Bio-inspired design of submerged hydrogel-actuatedpolymer microstructures operating in response to pH. Adv Mater 2011;23(12):1442–6.
ED P
RO
OF
tion: What can biomimicry inspire?, Biotechnol Adv (2014), http://
