IMPLEMENTING BIOMIMICRY THINKING FROM FUNDAMENTAL R&D TO CREATING

NATURE-ALIGNED ORGANIZATIONS

A Dissertation

Presented to

The Graduate Faculty of The University of Akron

In Partial Fulfillment

of the Requirements for the Degree

Doctor of Philosophy

Daphne Fecheyr-Lippens

August, 2017

i IMPLEMENTING BIOMIMICRY THINKING FROM FUNDAMENTAL R&D TO CREATING

NATURE-ALIGNED ORGANIZATIONS

Daphne Fecheyr-Lippens

Dissertation

Approved: Accepted:

______Advisor Program Director, Integrated Bioscience Dr. Peter H. Niewiarowski Dr. Hazel Barton

______Co-Advisor/Committee Member Interim Dean of Arts and Sciences Dr. Matthew D. Shawkey Dr. John Green

______Committee Member Dean of the Graduate School Dr. Ali Dhinojwala Dr. Chand Midha

______Committee Member Date Dr. Karim Alamgir

______Committee Member Dr. Dayna Baumeister

______Committee Member Dr. Pravin Bhiwapurkar

ii DEDICATION

This work is dedicated to my grandfather Opapie, who sadly past away on Oct,

4th 2014. He was our family’s nutty professor and injected his children and grandchildren with the exploration bugs. His curiosity and strong will resulted in several new verbs and words that were so often used in our family that I didn’t even realize they were invented by him. His enthusiasm and life vision encouraged me to dream about things that seem unreachable.

iii ABSTRACT

The appreciation for nature as inspiration for design has happened throughout human history. However, it wasn’t until the late 1990s that biomimicry was put forward as a discipline providing a framework to more actively and consciously use nature’s time-tested and refined strategies to inform innovative products, services and systems.

The implementation of biomimicry as a design tool to solve real-life, time-sensitive challenges inherently requires an interdisciplinary and collaborative approach. Biological knowledge needs to be made available, either by new research or by extracting it from existing literature. This then needs to be abstracted into design principles to be used to inform the creation of new designs. Ultimately this design needs to be commercialized by organizations that remain successful under rapidly changing conditions.

In this PhD work I explored the implications of implementing biomimicry thinking throughout this entire process, which included the scientific, engineering, design and business world. It is through experiential and observational learning that people are trained to design, support, and lead biomimicry endeavors. By sharing my experiences, challenges, concerns and research results I am hoping to boost the further development of biomimicry as a tool for technological and social innovation, as well as promote the potential of biomimicry to facilitate a sustainability transition and therefore increase its prominent implementation for solving real-life, time-sensitive challenges. The growing

iv interest and successful application of biomimicry can ultimately result not only in more environmentally conscious technologies, but also make organizations themselves nature-aligned.

v ACKNOWLEDGEMENTS

Everyone who knows me has most likely been exposed to my emotional side, so no need to hide that writing this section comes to me with lots of emotions. Relief, proudness, excitement, but also a little nostalgia. This PhD was not only an opportunity to develop my professional skills; it has also been a beautiful personal chapter in my life.

My passion for biomimicry motivated me to move from my oh so comfortable house in which I had been living my entire life. Although really motivated to explore the

(biomimicry) world, the immature girl I was then had no idea how challenging it would be to leave her hometown in Belgium together with her supportive and loving family and friends. Little she knew the amazing people she would meet along her journey in

‘Meurica.

Peter Niewiarowski, not only have you been the father of this groundbreaking

Biomimicry PhD program, you were also my surrogate father who kindly obligated me to wear a helmet when biking to campus or give me advice on difficult life decisions, from which car insurance to take to whether I should continue my PhD. Your support, advice, patience, encouragement and professionalism have been key for my PhD work.

Although your feedback on my research proposals and articles was always very critical, and at times hard to deal with, it assured me to go find my boundaries, which is

vi necessary for growth. You kept asking provocative questions that pushed forward my research endeavors, all with the motivation to further advance the development of biomimicry. Even better, you were always great at bringing in humor as balancing ingredient.

Matthew Shawkey, from the beginning you have given me tremendous trust and support, have been extremely patient, and were always at first hand for giving advice, guidance and constructive feedback. Not only were you pivotal in shaping me as an independent researcher, you have played an important role in welcoming me into the

USA. I’ve had the pleasure to play never-ending board games while sipping a coffee, eating a delicious home-cooked meal from Liliana or watching the Super Bowl. It came as great surprise to welcome you, Liliana, Tristan, Keira, and now little Sophia to

Belgium. I’m still surprised when seeing you run around in the streets of Gent.

I’m very honored to have had Karim Alamgir, Pravin Bhiwapurkar, Dayna

Baumeister, and Ali Dhinojwala as my PhD committee members. There is much to say about them besides the amount of difficult to spell and pronouncing last names. Thanks to their broad areas of expertise I gained interdisciplinary insights and a broadening perspective on my research goals. Whatever type of research challenge, I was peppered to overcome it thanks to them (this is quite bluntly translated from Dutch so I hope this is also an expression in English). The collaborative project with Pravin Bhiwapurkar has given me valuable exposure to the architectural design world, which appeared to be a hidden fascination of mine. Dayna Baumeister was actually one of my main firing ingredients that cultivated my passion for Biomimicry, so when she accepted my

vii invitation to be on my committee I was thrilled. She has given me the opportunity to deepen my knowledge in biomimicry thanks to our inspiring conversations, her thought- provoking questions and her insights as one of the foundational members of the field.

I would like to thank everyone from GLBio, and especially Tom Tyrell and Don

Knechtges, as it wasn’t thanks to their endless efforts that this biomimicry PhD program was made possible. This PhD was also not able without the financial support given by

Parker Hannifin, who gave GLBio the trust in finding a suitable doctoral student who would in return be active in their organization to bring biomimicry as a new tool for innovation and problem solving. Although I was not as deeply embedded in my sponsor company as my fellows, my exposure to the industrial world was truly fascinating. Never would I have imagined how complex the production of a simple hose could be. Also the accessibility of their research equipment has been crucial for the progress of my PhD work. Thank you Pete Buca for the inspiring conversations, the learning opportunities and sharing your expertise from the industrial world. Thank you Jonathan Markley and

Joseph Horinger for the many hours in assisting me with my experimental PhD work.

Emily Kennedy and Bill Hsiung, we were the guinea pigs of this new PhD program. I’m not exaggerating when I say I would have not survived the test without you. Being able to share difficulties, frustrations and panic attics made me feel like I could handle it (most of the times at least). I will never forget our champagne moment when our paper finally got accepted. And besides our professional achievements we have endless good memories to remember as our friendship continues, however far away we are.

viii We were so excited to see our program grow over time. It is truly impressive which talented people UAkron was able to attract. Thank you to all those bright, motivated minds that I was able to meet, although my time with some of you unfortunately was much too short (yes the blame is on me).

Besides our biomimicry hub, I also had the pleasure to be part of the colorful

Shawkey lab. Each one of you inspired me how fascinated and determined you were in your research interests. Sometimes some of you were so deeply fascinated by your results that I had no clue what you were talking about during our lab meetings.

However, it pushed me to show more dedication to my own research.

Thank you to everyone from the entire IB department for making this PhD possible. I have enjoyed the interesting lectures and the social encounters. A special thank you to Hazel Barton, whose enthusiasm, continuous support and administrative skills gave me the courage to get this PhD done.

This journey would have been incomplete with the new friends I made during my time in Akron. Gaya, you were my sunshine not only when walking by my lab, but your laugh and friendship gave me strength, warmth and happiness. Brani, I’m still debating if

I found your scientific advice in the lab or your sushi-making and Halloween-custom making advice more valuable. Stefanie, Lauren, Katie, Sara(h), Spencer, Matt, Jake, Mar,

Ricardo, our lovely neighbors, Michael, Candy dough, Mimi, Ceth, …Who would have thought that the city of “nice lawns in the middle of nowhere” had too many amazing people to name them all in my acknowledgements.

ix Off course my friends at home also deserve a thank you, as even from far away they supported me and with many of you we shared (although often virtually) our PhD frustrations.

How in the world can I ever find the words that would honor my incredible family? I’m sorry to everyone who reads this, but I think I’m one of the luckiest persons with the family I have. Sometimes it’s easy to take their endless support, love and trust for granted, but never have I had to miss it, even though we were suddenly a huge ocean apart. The distance made me appreciate even more the incredible special family I have. It is often when not in reach, that you realize the value of it. Daddy the pilot and mom the USA-lover luckily took every occasion they found to come visit and plan a trip together to explore the most beautiful parts of the US. I don’t think many grad students have been dropped off to campus in a mobile home on their first day. Alicja, it was hard for me to become an independent woman without the loving care and advice from you.

I guess it is appropriate to thank Steve Jobs for the creation of FaceTime. My two intelligent, successful big brothers and their lovely wives are a great example to me. For a couple of months we were nicely distributed over the US: two on the East coast, two in the middle, and two on the West coast. Not being there for the birth of their first child was extremely hard, Emily and Darwin are the cutest little creatures on earth. I will never have enough of their smile, cuddles and funny phrases. Thank you to my grandparents, uncles and aunts and my many wonderful cousins, who perhaps all together have all the pieces to understand what it was exactly what I was doing over there. Each one of you has always been truly interested in hearing our stories.

x And as if I’m not already enough spoiled with such a lovely family, I could have not been more fortunate with my family in law. Thank you to always have an open door and being there when we need a talk while giving enough freedom for personal growth and exploration. Line, I have always wanted a sister and now I have one who is always joyfully smiling, singing or dancing. You are a true star. Sam, perhaps I would still not know about biomimicry if I hadn’t seen the TED talk by Janine Benyus you sent to me many years ago.

Although I personally rarely take the advice “save the best for the last” I decided for once to not be different and follow the conventional outline of a dissertation acknowledgement section. Mathias, although it sounds lame, but I really would have never done this PhD without your support. It was not an evident decision for you to move with me to the USA, especially because that would not be our reason to get married. Your determination, positive mindset and “you can do it” attitude makes you the inspirational person I’m deeply in love with. Over the years you have given me confidence to dream about things that I thought I would never been able to achieve. Yet there I am climbing on a 30ft high rock in Arkansas with acrophobia, proudly calling myself co-founder of two startups while never realizing my passion for entrepreneurship before, and having explored desolate places in the world staying close to you to not freeze in our little tent or being eaten by bears we never even encountered. The difficulties we already have overcome together make it easy for me to see that you are my best partner in life and in business. I’m childishly excited and curious to what adventures are still to come for us.

xi TABLE OF CONTENTS Page

LIST OF TABLES ...... xv

LIST OF FIGURES ...... xvi

CHAPTER

I. INTRODUCTION ...... 1

II. THE CUTICLE MODULATES ULTRAVIOLET REFLECTANCE OF AVIAN EGGSHELLS ...... 8

Summary ...... 8

Introduction ...... 9

Materials and Methods ...... 12

Results ...... 16

Discussion ...... 22

Acknowledgements ...... 25

III. EXPLORING THE USE OF UNPROCESSED WASTE CHICKEN EGGSHELLS FOR UV- PROTECTIVE APPLICATIONS ...... 26

Summary ...... 26

Introduction ...... 27

Materials and Methods ...... 29

Results and Discussion ...... 34

xii Conclusion ...... 41

Acknowledgements ...... 44

IV. BIOMIMICRY: A PATH TO SUSTAINABLE INNOVATION ...... 45

Introduction ...... 45

What is Biomimicry? ...... 46

Biomimetic design practice ...... 48

Biomimicry and Sustainability ...... 49

Conclusion ...... 56

Acknowledgements ...... 58

V. APPLYING BIOMIMICRY TO DESIGN BUILDING ENVELOPES THAT LOWER ENERGY CONSUMPTION IN A HOT-HUMID CLIMATE ...... 59

Summary ...... 59

Introduction ...... 60

Methods ...... 64

Biological Domain ...... 65

Transfer phase ...... 69

Technological domain: Designing the biomimetic building envelope ...... 75

Evaluating energy saving potential of our biomimetic building envelope ... 77

Discussion ...... 84

Conclusion ...... 90

Acknowledgements ...... 90

VI. CONCLUSION ...... 91

LITERATURE CITED ...... 97

xiii APPENDICES ...... 107

APPENDIX A SUPPLEMENTAL MATERIAL FOR “THE CUTICLE MODULATES ULTRAVIOLET REFLECTANCE OF AVIAN EGGSHELLS” ...... 108

APPENDIX B SUPPLEMENTARY MATERIAL FOR “EXPLORING THE USE OF UNPROCESSED WASTE CHICKEN EGGSHELLS FOR UV- PROTECTIVE APPLICATIONS” ...... 111

APPENDIX C VARIATION OF UV-COLORATION OF WHITE, IMMACULATE AVIAN EGGS ...... 115

APPENDIX D EXPLORATION OF CAUSAL CHARACTERSTICS OF UV- COLORATION ...... 117

APPENDIX E VISUALIZATION OF LAYERING WITH NANO-CT ...... 120

APPENDIX F HEDGEHOG-INSPIRED HELMET LINER ...... 123

xiv LIST OF TABLES Table Page

2.1 Thickness measurements of untreated and EDTA-treated eggshells and their cuticle if present. The EDTA treatment was 90 min for chicken, brushturkey and pigeon, and 30 min for budgerigar. Results are given as mean ± s.e.m., with n = 10 ...... 18

2.2 The effects of sequential EDTA treatment on UV-chroma (mean ± s.e.m., n = 3)...... 20

2.3 Chemical composition (atom percentages, %) before and after EDTA treatment determined by XPS. Values indicating ND (=not detectable) are below detection limit. EDTA treatment was 90 min for chicken, brushturkey and pigeon, but only 30 min for budgerigar...... 22

5.1 Solution-based Biomimicry methodology following Badarnah & Kadri...... 65

5.2 Comparison of the baseline prototypical small-office building envelope with the proposed variations of the biomimetic building envelope system...... 78

A.1 Summary output for linear models comparing the change in UV chroma in relation to EDTA treatment...... 111

A.2 One-way ANOVA and Tukey multiple comparison tests (α = 0.05) for UV degradation of polystyrene (n=3)...... 112

A.3 One-way ANOVA and Tukey multiple comparison tests (α = 0.05) for UV degradation of nylon (n=6)...... 112

xv LIST OF FIGURES

Figure Page

2.1 SEM images showing the different eggshell morphologies for untreated and EDTA treated eggs. The EDTA treatment durations are 90 min for chicken, brushturkey, pigeon, and 30 min for budgerigar. First and third column are cross-sections, second and fourth column are topview images. C=Cuticle layer. Scale bars are 10 μm ...... 17

2.2 The effect of EDTA treatment on diffuse reflectance of white-coloured eggshells from chicken, brushturkey, pigeon and budgerigar. Durations for EDTA treatment were different for budgerigar, as the eggshells were very fragile. Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error. Grey area represents the UV-region, highlighting differences in reflectance...... 19

2.3 UV-chroma as a function of the duration of EDTA treatment. The data are presented as means ± s.e.m. Note that the x-axis scales are different for each species...... 20

2.4 XPS survey spectra showing the chemical composition of eggshells before and after EDTA treatment. The EDTA treatment duration are 90 min for chicken, brushturkey, pigeon, and 30 min for budgerigar. The sodium peak results from the residual presence of EDTA, and was not taken into account to calculate the atomic percentages...... 21

3.1 Schematic showing the UV aging experimental setup to test the UV protectiveness of white and brown eggshells (replicates n=3) (a), and compared to a commonly used UV-protective additive (n=6) (b)...... 32

3.2 SEM images of polystyrene (a) and nylon (b) before and after UV exposure. Scale bars = 200 μm. Arrows highlight cracks formed in the polymer...... 35

3.3 Diffuse reflectance spectra show changes in optical properties of polystyrene after UV exposure in the control but not when covered by eggshells (a). Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error. The yellowing of polystyrene is visible to the human eye (b)...... 36

xvi 3.4 FTIR spectra of polystyrene before and after 800h of UV exposure (a). The inset shows the degree of photo-oxidation (b), which is the calculated by integrating the area underneath the peak in the 1750 – 1600 cm-1 region. Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error...... 38

3.5 FTIR spectra of nylon before and after 800h of UV exposure (a). The inset shows the degree of photo-oxidation (b), which is the calculated by integrating the area underneath the peak in the 1750 – 1600 cm-1 region. The FTIR spectra show that the sample with the UV-additive has an extra peak around 3700 cm-1 (c), which disappeared after 100h of UV exposure (d). Plotted lines are group mean spectra (n=6) with shaded areas representing the standard error...... 39

3.6 Boxplots showing the degree of UV degradation of nylon after 800h of UV exposure. Box = 25th and 75th percentiles, with median shown as a thick line; bars are minimum and maximum values. Means with different letters (A,B,C) are significantly different (Tukey’s HSD, p <0.01, n= 6)...... 39

3.7 The suspension films of TiO2, white, and brown eggshell particles trap most of the UV light. The three films show comparable transmittance values that are well below 10%. Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error...... 41

4.1 Life’s Principles is a systems-thinking tool that contains common principles embodied by most species on Earth. Its purpose is to help practitioners create designs that fit seamlessly within the larger natural system. Permission to reprint image granted by Biomimicry 3.8...... 54

5.1 Comparison of the skin of the African reed frog during wet and dry season. The skin contains three types of chromatophores: iridophores (blue), xanthophores (orange), and melanophores (black). The number of iridophores increases significantly during transitioning to the dry season, while the xanthophores and melanophores are shifted to the bottom...... 67

5.2 Colour changing mechanism in the Hercules beetle. A spongy layer of filamentary strings of chitin arranged in layers parallel to the epicuticle, creates open pores filled with air (dry environment) or water (humid environment). Depending on the contrast between the refractive indices, this results in a greenish (dry) or black (humid) colour...... 68

5.3 Thermal zoning: Plan and axonometric view. Each floor has four perimeter zones and one core zone...... 70

5.4 Heat extraction rate from thermal zones of the middle floor on the hottest day of the year (July 26)...... 72

xvii 5.5 Graphic showing the main components of the biomimetic building envelope. Hot humid outside air (1) gets dehumidified in the hydrogel chambers (2) and is cooled by heat exchangers (Bio-PCM encapsulated wall) (3). The preconditioned air is used for natural ventilation or circulated via an integrated HVAC system (4)...... 76

5.6 Comparative HVAC-related EUI (a) of different building envelopes where phase change material (PCM), mixed-mode (MM) and natural ventilation (NV) are used with adaptive thermal comfort conditions extending cooling set-points from 23.8°C to 31.7°C. Comparative heat extraction rate (b) of different building envelopes on the south zone of the middle floor during hottest weekdays of the year (Monday, July 15 to Friday, July 19)...... 82

A.1 Mass spectra of chicken and brushturkey eggshell extracts are shown as example of eggs that lack a detectable amount of protoporphyrin (upper three) and biliverdin (lower three)...... 109

A.2 Cross-sectional SEM image of one particular pigeon egg showing a structure resembling a very thin cuticle (C). Scale bar is 10 μm...... 110

A.3 Effect of 30 min EDTA treatment on the surface morphologies of chicken, brushturkey and pigeon...... 110

A.4 Diffuse reflectance of a thin, flat layer of pure calcite powder (Sigma Aldrich, St. Louis, MO, USA), compared to those of untreated (solid lines) and EDTA-treated (dashed lines) eggshells...... 111

A.5 Temperature measured underneath a white and a brown chicken eggshell, and the quartz coverslips...... 113

A.6 Diffuse reflectance spectra showing no changes of optical properties of nylon after 800h UV exposure. Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error...... 113

A.7 Full FTIR spectra of polystyrene before and after 800h of UV exposure. Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error...... 114

A.8 Full FTIR spectra of nylon before and after 800h of UV exposure. Plotted lines are group mean spectra (n=6) with shaded areas representing the standard error...... 115

A.9 Optical (a) and SEM (b) images of suspension films of TiO2 particles, brown eggshell particles and white eggshell particles. Scale bars of optical images are 500 μm and SEM images are 100 μm...... 115

xviii A.10 Diffuse reflectance spectra of white-coloured eggshells from Australian brushturkey, budgerigar, ring-necked dove, King pigeon, chicken, zebra finch and flamingo and of a thin, flat layer of pure calcite powder (Sigma Aldrich, St. Louis, MO, USA). Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error...... 117

A.11 Thermogravimetric analysis and experimental modifications of the structure indicate the importance of structural integrity and the presence of proteins for UV reflectivity. Untreated (black) eggshell has high UV reflectivity, which is lost when organic matter is removed (TGA 100°C and 800°C, red line), and the nanostructure is destroyed (powderized, pink dotted line)...... 119

A.12 Decalcified eggshells reveal the lamellar organization (arrows) of the organic matrix. Figure taken from Chien et al (2008)...... 120

A.13 Scanning electron microscopy (SEM) images show the layering of the calcium carbonate crystals of eggshells. The inset is a higher magnification of the middle part. Both scale bars are 10 μm...... 120

A.14 The area that was chosen for the nano-ct scan, which is in the crystallized part of the eggshell. The eggshell cross section is seen horizontally, with the right side being the internal membrane side...... 122

A.15 A 3D volume rendering of the reconstructed image...... 123

A.16 Focused Ion Beam ablation resulted in melting of the structures of the eggshell due to its high energy. The left image shows a part that was melted after FIB, while the right image shows a more preserved part of the eggshell. Scalebars are 2 μm...... 123

A.17 (a) Photograph of a hedgehog spine, with the bulbed end on the left that is attached to the animal (scale bar 2 mm); (b) SEM of a spine’s lateral cross-section (scale bar 100 µm); (c) CT scan of a spine’s longitudinal cross-section (scale bar 100 µm). Figure taken from Swift et al. 2016...... 125

xix CHAPTER I

INTRODUCTION

Biology has inspired human design ever since prehistoric man fashioned spears from the teeth of animals and mimicked the effective sneak-and-pounce hunting technique of large predators, but the development of a methodological framework for translating biological strategies into design innovations is a recent one. American inventor, Otto Schmitt, coined the term “biomimetics” in the 1960s to describe the transfer of ideas from biology to technology (Schmitt, 1938). Three decades later, biomimicry was popularized by Janine Benyus who broadcast its enormous potential to inform a new era of design in her critically acclaimed book, Biomimicry: Innovation

Inspired by Nature (Benyus, 1997). Biomimicry, as defined today, involves learning from and emulating biological forms, processes, and ecosystems tested by the environment and refined through evolution (Baumeister, 2014).

Biomimicry is a burgeoning field of study, as evidenced by a growing demand for training in biomimicry theory and practice (Lepora et al., 2013) and a fivefold increase in biomimicry patents, scholarly articles, and research grants since 2000 (Fermanian

Business & Economic Institute, 2013). Biomimicry examples arise in different fields, including medicine, architecture, robotics, fashion, and even the banking world. For example, MIT engineers recently fabricated a fur-like, rubbery pelt inspired by hairy,

1 semiaquatic mammals such as beavers and sea otters, which can be used for wetsuits to hold surfers warm and dry (Nasto et al., 2016). Fashion designer Marieka Ratsma and architect Kostika Spaho took a bird’s skull to design a hollow high-heeled 3D-printed shoe, resulting in a lightweight, strong, elegant and material efficient design (Chalcraft,

2012). Katherine Collins explores in her book The Nature of Investing principles learned from the natural world to transform the mechanized investment framework from the roots up (Collins, 2014).

These examples show the importance of an interdisciplinary approach, since generally wetsuit manufacturers, shoe designers, architects and investors are not trained to study and understand the biological strategies found in nature. On the other hand, if it wasn’t for the MIT engineering students who wanted to understand the mechanical principles of how semiaquatic mammals trap air in their fur, that biological observation might have never resulted into a real-life application. However, since all these disciplines have their distinct language, methodologies and expertise, effective collaboration resulting in commercial outputs is not straightforward. The development of Biomimicry as a methodological framework has the potential to increase the collaboration between scientists, engineers, designers and business people.

In this light, formal biomimicry education should assist in training people who are comfortable with working in highly interdisciplinary and applied environments, and who aim at connecting real-life human challenges with fundamental biological knowledge. If we want biomimicry to be a feasible design and innovation tool to be commonly used in real-life, time-sensitive challenges, we need people that are trained

2 to be critical connectors, abstractors and translators over different fields, rather than experts in one field.

Therefor I have chosen to take an integrative approach for my PhD work rather than focusing on one specific fundamental research project. Through observational and experiential learning I gained knowledge about the implications of introducing biomimicry thinking into the scientific, engineering, design and business world. I wanted to get exposed to those different fields to attain a better understanding of their specific challenges, languages and methodologies. This way necessary skills that will be helpful in designing, supporting and leading interdisciplinary biomimicry projects can be identified. In particular, these skills include finding and understanding appropriate natural models, abstracting nature’s lessons into contextual design principles, rephrasing scientific research questions and real-life design problems, creating opportunities by linking seemingly unrelated fields, and ultimately support effective collaboration.

I started my PhD with the intention to take on one biomimicry project from start to finish, so that I would get exposed to the scientific world (i.e. finding and understanding an interesting biological observation, followed by the abstraction of the biological strategies into more general design principles), the design and engineering world (i.e. brainstorming and designing a biomimetic product), and the business world

(turning it into a commercial product). But it ended up quite differently; instead each step of a biomimicry process has been done on a different project.

3 First I designed and performed fundamental science experiments, which were driven by the interesting observation that white-colored eggshells, although looking the same for our human eyes, differ in their UV-coloration (Appendix C). In Chapter II we investigated if the cuticle, a non-crystalized layer that can vary in thickness and covers the external surface of most but not all avian eggs (Mikhailov, 1997), contributes to differences in UV-coloration. The cuticle differs both in composition and structure from the underlying crystalized eggshell (Baker and Balch, 1962; Kusuda et al., 2011) and therefore may differentially affect light modulation. Despite the absence of known eggshell pigments (biliverdin and protoporphyrin), we showed that removal of the outer layers of avian eggshells that contain a cuticle increased UV-chroma while this was not the case for eggshell without a cuticle. Our results suggest that the cuticle modulates

UV-reflectance, which is likely achieved by selective absorption of UV-wavelengths by the organic compounds in the cuticle.

However, this does not explain the color variation between eggshells of which cuticles were removed (revealing the crystalized part of the eggshell that is made 96% from calcite), eggshells without a cuticle, and that of pure calcite. Several experiments were undertaken to further investigate the causal differences in UV-coloration because that would contribute to a better understanding of the underlying mechanism that produces UV-colors in avian eggshells. Unfortunately these efforts did not result in strong evidence. Our initial experiments (Appendix D) suggested that UV-coloration was dependent on chemical and structural preservation. We hypothesize that UV-coloration is likely the result of a nanostructural layering of the crystallized calcite and organic

4 matrix sheets (Appendix D). Unfortunately the nano-computed tomography (nano-ct) scan did not identify nano-scale ordering that could result in structural coloration, although this might have been due to inadequate resolution (Appendix E). Further research is thus necessary to identify the mechanistic principles of UV-coloration in avian eggshells.

The reason why UV-coloration captured my interest is the outlook that eggshells could inspire the creation of novel UV-additives. Titanium dioxide (TiO2) is currently the most commonly used UV-additive, but besides its great optical properties it also has undesired environmental properties. In chapter III we found that unprocessed pieces of eggshells provide a durable and effective UV protection to two commonly used synthetic polymers: nylon and polystyrene. Films made from grinded eggshell had similar UV-transmittance properties than TiO2-films, setting the stage for future research to find a practical way to use the large amounts of unprocessed chicken eggshell waste as novel, economically appealing and environmentally friendly UV- protective additives.

The next focus of my work was to support a sustainability transition in the design world by showing the potential of biomimicry for creating more environmentally friendly designs. In chapter IV we raise the awareness that biomimicry can be used by designers to proactively support and guide the creation of sustainable designs, when practiced in a deep, thoughtful way. For retrieving the best potential to use biomimicry as a sustainability and innovation tool, designers should strive to emulate biological

5 lessons on three levels: form, process, and ecosystem (Baumeister, 2014) and adopt a biomimicry approach at the onset of a design project.

This reasoning is then put to practice in chapter V, in which I explored how biomimicry can be applied in the design world to create outcomes with a desirable ecological output. During a design class for architecture students given by Prof. Pravin

Bhiwapurkar, one of my PhD committee members, at the College of Architecture and

Environmental Design at Kent State University (OH) I had the opportunity to introduce biomimicry. We used the Hercules beetle and the African reed frog as inspiration for designing a biomimetic building envelope. Computer simulations showed the potential to decrease the HVAC-related energy use intensity (EUI) with 66%, especially during hot summer days.

Although each chapter has their own specific results, my eclectic PhD research can be summarized in the following eight general lessons, which are discussed throughout the chapters of this dissertation.

1. Interesting biological functions are not always evolutionary beneficial adaptations,

but can be the result of emergent properties. For example, the inside of abalone

shells is iridescent due to the arrangement of the aragonite tiles, and not because it

gives them a competitive advantage.

2. Biomimicry is based on the principle that nature optimizes rather than maximizes.

However, nature’s adaptations are not always global optimizations, but can also be

local optimization because of other, usually competing, functional needs.

6 3. Although biomimetic designs should be as true as possible to the biological

strategies used as inspiration, a too literal translation can limit biomimicry’s

application. Therefore, a conscious decision should be made to consider a more

metaphorical versus super literal translation.

4. While biomimicry can be the aim of a project, in some cases bio-inspiration and/or

bio-utilization can be considered as a preferred outcome.

5. The further development of a methodological framework for biomimicry should

also include social innovation besides technological innovation.

6. While biomimicry is the aim of a project, sometimes a shift in the focus of your

manuscript might be needed for finding appropriate journals. I’ve had multiple

reviewers stating that my manuscript “was not the focus of their journal.” It was

either too technical for a biology-focused journal or not technical enough for a

more specialized journal.

7. Be realistic about the time frame of a biomimicry project. Both the fundamental

research of UV-coloration in avian eggshell and the one based on social learning to

improve communication were much more research intensive than expected.

Fundamental R&D is tedious and time-consuming in order to obtain replicable

results and strong evidence.

8. It is not unlikely to encounter logistical challenges, which will be due to limitations

in technological advancements (e.g. appropriate research or manufacturing

techniques) or social advancements (e.g. finding suitable collaborators and

maintaining collaboration over long distances).

7 CHAPTER II

THE CUTICLE MODULATES ULTRAVIOLET REFLECTANCE OF AVIAN EGGSHELLS

Published in Biology One:

Fecheyr-Lippens, D., Igic, B., D'Alba, L., Hanley, D., Verdes, A., Holford, M., Waterhouse

G., Grim T., Hauber M. & Shawkey, M. 2015. The cuticle modulates ultraviolet

reflectance of avian eggshells. Biology open 4(7), 753-759.

Summary

Avian eggshells are variedly coloured, yet only two pigments, biliverdin and protoporphyrin IX, are known to contribute to the dramatic diversity of their colours. By contrast, the contributions of structural or other chemical components of the eggshell are poorly understood. For example, unpigmented eggshells, which appear white to the human eye, vary in their ultraviolet (UV) reflectance, which may be detectable by birds.

We investigated the proximate mechanisms for the variation in UV-reflectance of unpigmented bird eggshells using spectrophotometry, electron microscopy, chemical analyses, and experimental manipulations. We specifically tested how UV-reflectance is affected by the eggshell cuticle, the outermost layer of most avian eggshells. The chemical dissolution of the outer eggshell layers, including the cuticle, increased UV- reflectance for only eggshells that contained a cuticle. Our findings demonstrate that

8 the outer eggshell layers, including the cuticle, absorb UV-light, probably because they contain higher levels of organic components and other chemicals, such as calcium phosphates, compared to the predominantly calcite-based eggshell matrix. These data highlight the need to examine factors other than the known pigments in studies of avian eggshell colour.

Introduction

Understanding the proximate causes of variation in morphological traits like colour is critical to understanding their functions and evolution (Hill and McGraw, 2006).

Eggshell coloration may serve several roles, including camouflage (Merilaita and Lind,

2005), sexual selection (Moreno and Osorno, 2003), or host-parasite egg mimicry and rejection (Yang et al., 2013). A recent study further suggested that colour produced by pigments modulates the amount of beneficial vs. harmful UV-light reaching the embryo by acting as an absorbing barrier (Maurer et al., 2015). However, many eggshells lack pigmentation (Hauber, 2014) and the mechanism by which they attenuate ultraviolet light is unknown (Kilner, 2006). Studying the proximate basis of egg coloration may also help provide inspiration for applied systems, including the development of biomimetic materials by identifying important factors that contribute to light modulation (Li et al.,

2010; Yoo et al., 2009). Colours in nature can be produced by pigments, nanostructured architectures (generating structural colour), or a combination of both (Parker, 2000; Sun et al., 2013). Whereas pigments produce colour through the absorbance of light at specific wavelengths, structural colours are produced by selective reflectance, scattering

9 or diffraction of light by nanostructured biological materials (Kinoshita et al., 2008;

Srinivasarao, 1999).

Little is known about the mechanisms that generate eggshell coloration.

Currently, only two classes of tetrapyrrole pigments (biliverdin and protoporphyrin IX) are considered to influence eggshell coloration of most bird species (Kennedy and

Vevers, 1976). However, recent studies have shown that eggshell coloration of a number of different species cannot be explained solely by variation in biliverdin and protoporphyrin concentrations (Cassey et al., 2012a; Igic et al., 2012), suggesting that other mechanisms may contribute to the appearance of eggshells. Indeed, in addition to the two tetrapyrrole pigments avian eggshells consist of numerous other compounds that may selectively absorb light or modify the absorption properties of the two pigments.

In addition to pigments, eggshell proteins or nanostructures could contribute to eggshell coloration by either selectively absorbing certain wavelengths or enhancing light reflectance, respectively. Eggshells consists of about 4% organic and 96% inorganic material, the latter of which 98% is calcium carbonate, and the remainder includes calcium phosphates and metal ions (Hamilton, 1986). Furthermore, the external eggshell surface of most avian species is covered by a cuticle, a non-crystalized layer that can vary in thickness and consist of proteins, polysaccharides, lipids, calcium carbonate, and calcium phosphates (Kusuda et al., 2011; Mikhailov, 1997; Wedral et al., 1974). Aromatic amino acids of proteins (Holiday, 1936) and calcium phosphates (Bogrekci and Lee,

10 2004; Holzmann et al., 2009) also have distinctive absorption spectra compared to calcite and the two tetrapyrrole pigments. Both groups of molecules absorb maximally in the (near) UV-range, and are common constituents of eggshells (Hincke et al., 1992;

Sparks, 1994). Moreover, the nanostructural organisation of calcium carbonate can produce structural colour [e.g. nacre (Alexander Finnemore, 2012; Bonderer et al., 2008;

Grégoire, 1957)]. Critically, the eggshell cuticle differs both in composition and structure from the underlying crystalized eggshell (Baker and Balch, 1962; Kusuda et al., 2011) and therefore may differentially affect light modulation. Indeed, it has been shown that an extremely smooth cuticle produces glossiness and iridescence in tinamou eggs (Igic et al., 2015).

Here, we investigated mechanisms underlying colour variation of immaculate, white avian eggshells. We specifically examined how the eggshell cuticle contributes to coloration. To do this, we experimentally removed the outer layers of immaculate, white eggshells of four species: chicken (Gallus gallus), Australian brushturkey (Alectura lathami), king pigeon (Columba livia domestica), and budgerigar (Melopsittacus undulatus). If the cuticle contributes to eggshell coloration, we predicted that its removal would cause a larger colour change in eggshells with cuticles compared to those without. We then used scanning electron microscopy, X-ray photoelectron spectroscopy, and chemical extractions to investigate if nanostructural features or chemical composition explain the observed patterns of coloration and its change following experimental manipulation.

11 Materials and Methods

Samples

We sourced three unincubated, untreated and non-pasteurized eggs of four species: chicken (Gallus gallus) eggs from a commercial farm in Akron, Ohio; Australian brushturkey (Alectura lathami) eggs from Brisbane, Australia; king pigeon (Columba livia domestica) eggs from a breeder in Dallas, TX; and budgerigar (Melopsittacus undulatus) eggs from a captive research colony in Las Cruces, NM. Eggshells were fragmented into

1 cm2 pieces using soft pressure and washed using 100% ethanol. We measured pigment concentration to verify the absence of biliverdin and protoporphyrin. We compared diffuse reflectance and conducted scanning electron microscopy (SEM) and X- ray photoelectron spectroscopy (XPS) on eggshells before and after chemical dissolution of the outer shell layers.

Pigment extraction

We followed a modified pigment extraction protocol of (Gorchein et al., 2009).

We used the solvent alone as negative control, a brown chicken egg for protoporphyrin positive control and a blue chicken egg (Araucana strain) as biliverdin positive control.

Briefly, shell samples were broken into small fragments (surface area ∼1 cm2 and/or weight ∼400 mg), rinsed with distilled water, 70% ethanol and homogenized by grinding; then 1 ml of aqueous solution of disodium ethylenediaminetetraacetic acid (EDTA) pH

7.2 (100mg/ml) was added, and the tubes were vortex-mixed for 1 min and centrifuged at 15,000 g for 30 s in an Eppendorf 5430R Centrifuge, discarding the supernatants. This

12 procedure was repeated three times and then 1 ml of acetonitrile-acetic acid (4:1 v/v) was added. The tubes were vortex-mixed for 2 min in 30 s bursts (and opened to allow the escape of CO2), and subsequently centrifuged for 2 min at 15,000 g. The supernatants were then transferred to clean tubes and stored at 4°C in the dark until further analysis within 24 h. An aliquot was measured in a NanoDrop 2000c spectrophotometer for its UV-Vis absorbance spectrum from 250–700 nm versus acetonitrile-acetic acid as a blank. Pigment presence or absence was indicated from these spectra and confirmed and quantified by Ultra High Performance Liquid

Chromatography (UHPLC) and Mass Spectrophotometry (MS). All shell extracts (whether or not pigment was detected by methods above) were further analysed through MS ion detection at specific masses (563 m/z for protoporphyrin and 583 m/z for biliverdin) to detect presence of pigments below the detection threshold of standard MS analysis. All observed pigments were also compared to commercially obtained standards of the free acids of biliverdin and protoporphyrin from Frontier Scientific Inc. (UT, USA) dissolved in acetonitrile-acetic acid.

Experimental removal of outer layers

To experimentally investigate the contribution of the cuticle to the optical properties of the eggshells, we sequentially removed the outer eggshell layers (including the cuticle if present) over a course of treatments. For each treatment, we floated eggshells (with their surface down) on a weak alkaline solution (pH 8.1) of 0.37M EDTA and then gently brushed the surface using soft tissue paper (Baker and Balch, 1962; Igic

13 et al., 2015). We repeated this over a course of treatment times depending on the thickness of the eggshells: successive increments of 10 min for budgerigar and increments of 30 min for chicken, brushturkey, and pigeon. We repeated treatments until the eggshells became too thin and fragile to handle (30 min for budgerigar, 90 min for pigeon, 120 min for chicken and 180 min for brushturkey). The removal of the outer layers was visualised by SEM after 30 and 90 min of EDTA treatment (or only after 30 min for the budgerigar).

Scanning electron microscopy (SEM)

We mounted untreated and EDTA-treated eggshell fragments onto aluminium stubs, allowing the visualisation of both the shell surface and cross-section, which we then sputter-coated with gold/palladium for 3 min. SEM (JSM7401F, JEOL Japan) images were taken at a working distance of 8 mm with an accelerating voltage of 5 kV.

Spectrophotometry

We measured diffuse reflectance on eggshell fragments between 300 and 700 nm. To minimize geometric variation associated with shell curvature and rough surfaces, we measured reflectance from the flattest part of fragments taken from the equatorial region of eggs. We used an integrating sphere (AvaSphere-50-REFL) with a black gloss trap to exclude specular reflectance, an AvaSpec-2048 spectrometer, and an AvaLight-

XE pulsed xenon light source (Avantes Inc., Broomfield, CO, USA). All reflectance measurements were taken relative to a diffuse white standard (WS-2, Avantes Inc.).

14 We quantified UV-reflectance because this region showed the greatest level of

variation for our samples. To evaluate changes in UV-reflectance, we calculated UV-

chroma as a proportion of UV-reflectance from total reflectance (R300-400/R300-700) using the summary function of the R package PAVO (Maia et al., 2013). UV-chroma accounts for differences in total reflectance and thereby eliminates the confounding effect of eggshell thickness on our results. We then compared UV-chroma of eggshells across sequential EDTA treatments.

We used linear models to test if UV-chroma changed following sequential removal of the outer layers. For each species separately, we constructed models with

UV-chroma as responses, egg ID as discrete predictor and EDTA treatment as continuous predictor. We constructed models using normal error distributions and identity link functions (Table A.1). We analysed each species separately because: (i) EDTA treatment durations were not quantitatively the same for the four species because of their differences in eggshell thickness and (ii) it was unclear whether EDTA treatment had the same effects for all other species’ eggs. P-values were adjusted following Holm’s method (Aickin and Gensler, 1996). All statistical tests were implemented in R v.3.0.1 (R

Development Core Team, 2013).

X-ray photoelectron spectroscopy (XPS)

The survey spectra of untreated and EDTA-treated eggshells (90 min for chicken, brushturkey, and pigeon eggs; and 30 min for budgerigar eggs) were collected using a

VersaProbe II Scanning XPS Microprobe from Physical Electronics (PHI), under ultrahigh

15 vacuum conditions with a pressure of 2×10−6 Pa. Automated dual beam charge neutralization was used during the analysis of the samples to provide accurate data. The analyser pass energy was 117.4 eV and each spectrum was collected using a monochromatic Al Kα X-rays (hν=1486 eV) over a 200 μm diameter analysis area. The survey scans were used to evaluate the near surface region elemental composition of the eggshells. Peak areas were measured for the C 1s, O 1s, Ca 2p, N 1s, P 2p and S 2p regions and elements were quantified using instrument-modified Schofield cross sections (PHI MultiPak software). The sodium peak results from the residual presence of

EDTA, and was not taken into account to calculate the atomic percentages. Under ideal conditions, this technique allows the detection of elements that have near surface region concentrations higher than ∼1% by weight at an analysis depth of approximately

10 nm. However, surface roughness can affect quantification accuracy.

Results

Ultra High Performance Liquid Chromatography (UHPLC) and Mass

Spectrophotometry (MS) confirmed that none of the eggshells of the four species

(chicken, brushturkey, pigeon, and budgerigar) contained any detectable concentrations of protoporphyrin or biliverdin, whereas these pigments were detected in our positive controls (Fig. A.1).

Untreated eggs of the four species differed in overall structure, thickness and presence of cuticle (Fig. 2.1; Table 2.1). Chicken eggs were covered by a thin smooth

16 cuticle that contained nanospheres with a mean diameter of 151.4±5.2 nm (n=40, s.e.m.). Brushturkey eggshells had a distinct cuticle composed of nanospheres with a mean diameter of 307.8±13.1 nm (n=40, s.e.m.). Pigeon eggshells had a smooth surface with some pores, and cross-section images for one of the eggs showed a structure resembling a very thin cuticle (Fig. A.2). Budgerigar eggshells lacked a cuticle, and the vesicles of the organic matrix were visible on the surface as pores with a diameter varying between 1–2 μm in diameter (Fig. 2.1).

Chicken Brushturkey

C C Untreated EDTA

Pigeon Budgerigar Untreated EDTA

Figure 2.1. SEM images showing the different eggshell morphologies for untreated and EDTA treated eggs. The EDTA treatment durations are 90 min for chicken, brushturkey, pigeon, and 30 min for budgerigar. First and third column are cross-sections, second and fourth column are topview images. C=Cuticle layer. Scale bars are 10 μm.

17 Table 2.1. Thickness measurements of untreated and EDTA-treated eggshells and their cuticle if present. The EDTA treatment was 90 min for chicken, brushturkey and pigeon, and 30 min for budgerigar. Results are given as mean ± s.e.m., with n = 10.

Species Thickness Thickness cuticle Thickness Proportional untreated untreated eggs EDTA-treated decrease in eggshell (µm) (µm) eggshell (µm) thickness (%) Chicken 275.49 ± 3.90 2.74 ± 0.36 220.70 ± 3.00 20.2 Brushturkey 327.58 ± 2.91 15.21 ± 1.04 307.97 ± 8.41 6.0 Pigeon 132.90 ± 1.57 <1.00* 118.47 ± 2.12 11.3 Budgerigar 60.31 ± 0.43 No cuticle 56.03 ± 0.32 7.1 * We found evidence of a very thin cuticle (approx. 130 nm) on one particular pigeon egg.

Sequential treatment with ethylenediaminetetraacetic acid (EDTA) gradually

removed the outer layers of all four species’ eggshells, but had differential effects on

their structure (Fig. 2.1; Fig. A.3) and decrease in thickness (Table 2.1). After 30 min of

EDTA treatment, the nanospheres of chicken eggshell cuticle were removed (Fig. A.3),

whereas after 90 min of EDTA treatment, the cuticle was fully removed along with a

portion of the underlying palisade layer (Fig. 2.1). After 30 min of EDTA treatment, only a few nanospheres were still present on the brushturkey eggshell (Fig. A.3), and after 90 min of EDTA treatment, parts of the underlying palisade layer became visible and removal of the cuticle was confirmed in the cross-section image (Fig. 2.1). After

sequential EDTA treatment, the vesicles of the pigeon eggshell became gradually more

distinct as deeper pores according to the time of the treatment (Fig. 2.1; Fig. A.3). After

30 min of EDTA treatment, the holes on the budgerigar eggshell were still visible,

however, the surface became much rougher and pockmarked (Fig. 2.1).

18 Gradual removal of the outer layers (including the cuticle if present) resulted in a significant increase in UV-chroma for chicken and brushturkey eggs. With increasing chemical etching of the outer layers, UV-chroma increased for chicken (F1,11=103.7,

P<0.001), brushturkey (F1,17=62.0, P<0.001), and pigeon (F1,8=11.6, P<0.01), but not for budgerigar (F1,8=1.8, P=0.22) (Figs 2.2,2.3; Table 2.2).

Figure 2.2. The effect of EDTA treatment on diffuse reflectance of white-coloured eggshells from chicken, brushturkey, pigeon and budgerigar. Durations for EDTA treatment were different for budgerigar, as the eggshells were very fragile. Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error. Grey area represents the UV-region, highlighting differences in reflectance.

19 Chicken Brushturkey 26 26

25 25

24 24

23 23

22 22

21 21 0 40 80 120 0 40 80 120 160 200

26 Pigeon 26 Budgerigar

UV Chroma (%) 25 25

24 24

23 23

22 22

21 21 0 20 40 60 80 100 0 10 20 30 40 EDTA treatment (min)

Figure 2.3. UV-chroma as a function of the duration of EDTA treatment. The data are presented as means±s.e.m. Note that the x-axis scales are different for each species.

Table 2.2. The effects of sequential EDTA treatment on UV-chroma (mean ± s.e.m., n = 3).

Difference in UV-chroma EDTA (%) Brushturkey Pigeon treatment (min) Chicken Budgerigar 10 n/a n/a n/a −0.17 ± 0.11 20 n/a n/a n/a 0.01 ± 0.11 30 1.40 ± 0.95 1.69 ± 1.13 0.16 ± 0.39 0.15 ± 0.28 60 2.30 ± 0.86 1.27 ± 1.06 0.32 ± 0.40 n/a 90 3.73 ± 1.46 1.87 ± 0.58 0.66 ± 0.16 n/a 120 4.46 ± 1.59 2.58 ± 0.33 n/a n/a 150 n/a 2.97 ± 0.74 n/a n/a 180 n/a 3.55 ± 0.65 n/a n/a

20 X-ray photoelectron spectroscopy (XPS) revealed the presence of phosphorus on the surface of chicken and brushturkey eggs, which completely disappeared following 90 min of EDTA treatment (Fig. 2.4; Table 2.3).

Chicken Brushturkey 1s 1s

O Chicken + EDTA O Brushturkey + EDTA 1s C 2p (KLL) Ca (KLL) 1s 1s Na C N Na 2s 2p 1s Ca 2s N Ca Ca 3p 2p 2s 2s 3p 3s P 2s Ca P Ca Na Ca Na 0 10000 20000 30000 40000 0 10000 20000 30000

600 500 400 300 200 100 0 600 500 400 300 200 100 0

Budgerigar

Pigeon 1s 1s O O Pigeon + EDTA Budgerigar + EDTA 1s C 1s C (KLL) (KLL) Counts per second (c/s) Na Na 1s 1s N N 2p 2p 2s 2s Ca Ca Ca Ca 2s 2s 3p 3p 2p Na Na Ca S Ca 0 10000 20000 30000 0 10000 20000 25000

600 500 400 300 200 100 0 600 500 400 300 200 100 0 Binding energy (eV)

Figure 2.4. XPS survey spectra showing the chemical composition of eggshells before and after EDTA treatment. The EDTA treatment duration are 90 min for chicken, brushturkey, pigeon, and 30 min for budgerigar. The sodium peak results from the residual presence of EDTA, and was not taken into account to calculate the atomic percentages.

21 Table 2.3. Chemical composition (atom percentages, %) before and after EDTA treatment determined by XPS. Values indicating ND (=not detectable) are below detection limit. EDTA treatment was 90 min for chicken, brushturkey and pigeon, but only 30 min for budgerigar.

Chicken Brushturkey Pigeon Budgerigar Untreated EDTA Untreated EDTA Untreated EDTA Untreated EDTA C 64.7 59.6 39.4 60.0 67.3 64.4 69.4 62.2 O 23.3 27.2 40.5 28.0 24.8 27.6 23.2 29.5 N 10.0 11.1 7.1 10.5 6.7 7.0 6.6 6.7 Ca 1.4 2.1 8.6 1.5 0.8 0.6 0.7 1.5 P 0.7 ND 4.4 ND ND ND ND ND S ND ND ND ND 0.5 0.4 ND ND

Discussion

Despite the absence of known eggshell pigments (biliverdin and protoporphyrin), we found differences in the UV-reflectance of the four species’ eggshells. We showed that removal of the outer layers of avian eggshells that contain a cuticle increases UV- chroma, suggesting that the cuticle modulates UV-reflectance of white eggshells. This is likely achieved by selective absorption of UV-wavelengths by the compounds in the cuticle. The effects of the cuticle on eggshell coloration are particularly important, because the composition, thickness and extent of coverage of the cuticle (and thus potentially colour of the shell) can vary according to female age and egg freshness

(Rodriguez-Navarro et al., 2013). These results highlight the importance of factors other than biliverdin and protoporphyrin in influencing avian eggshell coloration.

Eggshell colour varied across these unpigmented eggshells, and differed from that of pure calcite, even after their cuticles were removed (Fig. A.4). Although avian eggshells consist of approximately 96% calcite overall (Hamilton, 1986), the underlying structure

22 of calcite crystals, or the composition of the organic matrix, can differ among species

(Panheleux et al., 1999). These differences may cause variation in UV-chroma among the different species’ eggs studied here and highlight a role of non-pigmentary chemical or structural differences in influencing avian eggshell coloration. The chicken eggshell is particularly interesting as its UV-chroma drastically increased following removal of its outer layers. This finding suggests that some characteristic of the chicken eggshell increases the inherent UV-reflectance of calcite (Fig. A.4), possibly through nanostructuring as no identified pigment absorbs light across all wavelengths except UV

(Andersson, 1999); however, the exact mechanism requires further investigation.

The increase in UV-chroma associated with removal of the outer eggshell layers was highest for eggshells with a clearly defined cuticle. EDTA treatment had the largest effect on chicken eggs, likely because it caused the greatest proportional decrease in eggshell thickness (Table 2.1), meaning that additional material other than the cuticle was removed. It is therefore possible that the drastic increase in UV-chroma is caused by interaction of light with structures or compounds inside the underlying palisade layer. By contrast, UV- chroma of budgerigar eggshells, which lack a cuticle (Mikhailov,

1997), did not increase after treatment. Despite the previously reported absence of cuticles on pigeon eggshells (Board, 1974), we found evidence of a very thin cuticle on one of the three pigeon eggshells (Fig. A.2), and it is likely that its removal caused the low (<1%), but significant, increase in UV- chroma. Indeed, it has been suggested that cuticles may be present on some freshly laid, open-nesting pigeon’s eggs (Mikhailov,

1997). Our data thus suggest that the cuticle absorbs UV-light.

23 The composition of the cuticle varied between chicken and brushturkey, and

EDTA treatment resulted in differential effects on eggshell thickness, making it difficult

to identify the precise cause of the increase in UV-chroma. Unlike the mostly calcareous

eggshell layer underneath, the XPS data showed the presence of phosphorous in the

cuticles of chicken and brushturkey eggs (Table 2.3). This is likely coming from inorganic calcium phosphates, probably in the form of hydroxyapatite (Board et al., 1984; D’Alba et al., 2014; Dennis et al., 1996). Chicken cuticles mainly consists of proteins (85–90%), polysaccharides (4–5%), and lipids (2.5–3.5%) (Baker and Balch, 1962; Hamilton, 1986;

Rodriguez-Navarro et al., 2013; Wedral et al., 1974). Therefore, these organic components may selectively absorb wavelengths in the UV-range (Albalasmeh et al.,

2013; Edelhoch, 1967; Holiday, 1936; Itagaki, 1994). The small amount of inorganic phosphates may also selectively absorb UV- wavelengths (Holzmann et al., 2009;

Piccirillo et al., 2014). The cuticle of brushturkey eggshells is composed predominantly of calcium phosphates (Board et al., 1984; D’Alba et al., 2014) and may have a similar effect on UV-absorbance.

The function of UV-reflectance by eggshells is unclear and needs more focal functional studies (Lahti, 2008) and broad comparative studies on eggshell composition and colour in relation to ecology (Cassey et al., 2012b). Substantial variation in ultraviolet coloration could alter the effectiveness of egg camouflage or UV protection, or impact mate choice. Whether variation in cuticle thickness or composition is sufficient to affect such changes are excellent topics for future research.

24 Avian eggshells are a good model system for inspiring biomimetic materials (Yoo et al., 2009). The modulation of UV-radiation is of prime importance for the design of many materials, including textiles, polymer coatings and paints (Andrady et al., 1998), because it can reduce detrimental effects of sun-exposure. UV-coloration produced through structural colour is likely less costly over the long-term than that produced using pigments because they are more durable (Sun et al., 2013), and thus more efficient for UV-protective coatings. Understanding the non-pigmentary mechanisms behind UV- modulation of avian eggshells could reveal potential new insights for the development of innovative UV-protective materials. In particular, unpigmented chicken eggshells are a prime candidate for further biomimetic study because their UV- reflectance characteristics are above that of calcite alone.

Acknowledgements

We thank B. Hsiung, J. Peteya, and M. Xiao for comments on the manuscript, Z.

Nikolov for help with the XPS analysis, and D. Jones and T. Wright for egg samples

(brushturkey and budgerigar, respectively).

25 CHAPTER III

EXPLORING THE USE OF UNPROCESSED WASTE CHICKEN EGGSHELLS FOR UV-

PROTECTIVE APPLICATIONS

Published in Sustainability:

Fecheyr-Lippens, D., Nallapaneni, A. & Shawkey, M. 2017 Exploring the use of

unprocessed waste chicken eggshells for UV-protective applications. Sustainability 9(2),

232

Summary

Photodegradation causes a steady loss of the useful physical, mechanical and optical properties of materials, necessitating their replacement over time. Because

UV light is most harmful in this regard, many materials now contain UV-protective additives. However, these additives are not always effective and durable, can be expensive, and their natural extraction or synthetic production can be harmful to the environment. Here we investigated the use of unprocessed chicken eggshells in providing UV protection to two commonly used synthetic polymers: polystyrene and nylon. We show that unprocessed chicken eggshells provide a durable and effective UV protection. Our data sets the stage for future research to find a practical way to use the

26 large amounts of unprocessed chicken eggshell waste as novel, economically appealing and environmentally friendly UV-protective additives.

Introduction

Although sunlight is essential for life, it also has harmful effects. Most incident solar radiation that reaches Earth’s surface is infrared (43%) and visible light (53%), and only a small portion is ultraviolet (4%) (Brooks, 2012). However, the UV portion is most harmful due to its shorter wavelengths and higher energies (Rabek, 1995). The incident terrestrial solar UV consists of light with wavelengths between 290–400 nm, because the stratospheric ozone absorbs UV-C (100–280 nm) and some UV-B (280–315 nm)

(Madronich and Flocke, 1997). UV light has deleterious effects on many materials, including synthetic polymers and naturally-occurring biopolymers such as skin, hair, and wood (Andrady et al., 1998). These materials absorb UV, triggering photolytic and photo-oxidative reactions, resulting in photodegradation and therefore a steady loss of useful physical, mechanical, and optical properties.

Substantial efforts have gone into reduction of photodamage and improvement of durability of photodegradable materials upon exposure to UV light using both organic and inorganic additives (Andrady et al., 1998). Organic additives generally absorb UV and are considered sacrificial components that only provide temporary protection. They usually require the addition of hindered amine light stabilizers (HALS) that react with free radicals formed by UV absorption and interfere with photo-oxidation reactions

(Berdahl et al., 2008). Inorganic additives are usually semiconductor oxides like TiO2,

ZnO, SiO2, and Al2O3, and whether they protect materials by reflecting or absorbing UV

27 is unclear (Yang et al., 2004). The most common inorganic additive is titanium dioxide

(TiO2), with a global consumption of more than 4 million tons in 2005 (Völz et al., 2000)

of which about 60% is used as whitening and UV-protective additives in coatings

(Gázquez et al., 2014). The high refractive indices of rutile and anatase (the most

common forms of TiO2: 2.70 and 2.55, respectively) enable them to efficiently scatter

light when formed into particles of the appropriate size (~200 nm) (Buxbaum, 2008) and

to absorb light regardless of particle size (Yang et al., 2004). These optical properties

make TiO2 an excellent UV-protectant. However, pigment chalking of paints and coatings containing TiO2 occurs under UV exposure (Buxbaum, 2008). Moreover, the natural extraction and synthetic production of TiO2 is environmentally harmful, quickly depletes

finite resources, and is energy-intensive and costly (Chen and Mao, 2007). TiO2 is also

potentially carcinogenic to animals (Costa et al., 2012). Thus, alternatives to TiO2 are needed for both environmental and economic reasons.

Here we investigated the avian eggshell’s potential as a UV-protectant. In a previous study we found that white-colored chicken eggshells (Gallus gallus) reflect large amounts of UV light (Fecheyr-Lippens et al., 2015). Moreover, chicken eggshell waste from manufacturing plants and food processing is currently generated at enormous amounts of several tons per day (Kamkum et al., 2015). Most eggshell waste is discarded because further processing is too expensive and cumbersome, and unprocessed (i.e. still having the calcium carbonate eggshell and protein-rich membrane together) eggshells are considered useless (Wei et al., 2009). Sending unprocessed eggshell waste to landfill is associated with a cost of more than $40 a ton depending on

28 the location of the landfill (Yoo et al., 2009). The main objective of our study is to find an environmentally and economically appealing use of waste chicken eggshells by turning them into valuable UV-additives, which can be used to protect against photodegradation.

Materials and Methods

We examined if chicken eggshells protect synthetic polymers (polystyrene and nylon) from UV degradation and compared their effectiveness with that of a commonly used UV-protective additive, which we identified as TiO2. We exposed the two polymers

(covered by eggshells) to UV light for 800h in a controlled UV-aging chamber. We then used scanning electron microscopy, spectrophotometry, and Fourier-transform infrared spectroscopy to determine if the polymers showed signs of UV degradation. We further took a first step to determine if eggshells in a more practical form (i.e. ground into a powder) would also provide protection against photodegradation by measuring the transmittance of UV light.

Samples for the UV aging experiments

Polymers

We analyzed photo-degradation of two different synthetic polymers: polyamide

11 (PA-11, or nylon) and polystyrene (PS). We chose PS because it is a common UV weathering reference material that changes color (becomes yellow) quickly with UV exposure (Fedor and Brennan, 1996), and nylon because it is a common thermoplastic used for many industrial applications and has better sunlight resistance (Kohan, 1995).

29 Styrene sheets (purchased from Plastics 2000, Modesto, CA, USA) were 1 mm

thick, and 30 x 30 cm in size. Two types of nylon were extruded from polymer pellets

(only polymer: RILSAN BESNO; and polymer + UV-protective additives: RILSAN BESNO

TL), into strips of 0.8 mm thick and 2.5 cm wide. The manufacturer of RILSAN BESNO TL

did not specify the chemical identity of the UV-protective additives. The three different

polymer specimens were cut into pieces of 2.5 x 7 cm.

Eggshells

We sourced white and brown unincubated and non-pasteurized chicken eggs

(Gallus gallus domesticus) from a commercial farm in Akron, OH. The egg white and

yolk were carefully removed and the eggshells were washed with DI water and 100%

ethanol. The eggshells were fragmented into 1 cm2 pieces using soft pressure and stored in the dark at room temperature.

Quartz Coverslip

As control we covered the polymers with UV-transparent 25 x 25 x 0.2 mm quartz coverslips (EMS, Hatfield, PA, USA). We stacked two coverslips to achieve a thickness similar to the chicken eggshells (~ 450 µm). This control allowed us to determine if the UV protectiveness of the eggshells is the result of its chemical and/or physical properties rather than the effect of simply representing a physical barrier thick enough to block or filter the passage of light. We used quartz as it does not interfere with UV wavelengths (Kopitkovas et al., 2004) and the exclusive effect of the material thickness can be tested.

30 UV Aging Chamber

To assess the effect of UV exposure on photo-degradation of the polymers we

mounted the specimens in a QUV Accelerated Weathering Tester (Q-Lab, Westlake, OH,

USA). Accelerated weathering testers are commonly used as they provide results more

quickly (i.e. UV degradation is accelerated compared to natural conditions) and are more economically viable than extensive outdoor exposure experiments (Jelle, 2012).

However, the data are relative, because it is theoretically impossible to have a single conversion number to calculate the years of outdoor hours from the UV-exposed hours in the UV chamber (Grossman, 1984). The experiments were performed with fluorescent UVA-340 lamps, because they simulate sunlight in the region of the spectrum that causes most polymer damage (295-365 nm) (Jelle, 2012). The UVA-340 lamps were operated at 0.85 W/m2/nm. A single exposure temperature of 45°C was

chosen according to SAE Standard J844.

Specimen Installation

The polymer strips were cut into pieces of 2.5 x 7 cm, and wrapped in aluminum

foil to protect them from UV degradation. Pieces of 1 cm2 were cut in the aluminum foil

to expose the polymer, and were then covered either by a piece of eggshell, or by the

quartz coverslips as control (Fig. 3.1). The specimens were mounted on standard

specimen holders (Q-Lab, Westlake, OH, USA).

Experimental Setup

To test for differences in UV protectiveness between the white and brown

colored eggshells, we covered polystyrene with a piece of eggshell of each color (Fig.

31 3.1(a)). In the second replicate we compared the UV protectiveness of eggshells with

that of a commonly used UV-protective additive (Fig. 3.1(b)). Here we compared

specimens of nylon (RILSAN BESNO) covered with eggshells to a specimen of nylon that

includes UV-protective additives (RILSAN BESNO TL; which we identified as TiO2).

Figure 3.1. Schematic showing the UV aging experimental setup to test the UV protectiveness of white and brown eggshells (replicates n=3) (a), and compared to a commonly used UV-protective additive (n=6) (b).

Temperature Measurement

To control for any possible thermal degradation effects we measured the

temperature beneath one brown- and one white-colored eggshell and one set of quartz

coverslips. We mounted small temperature TK-4023 monitors (Gemini Data Loggers Ltd,

UK) beneath the samples and the Tinytag Talk Thermistor Probes registered the

temperature each hour during the entire 800h of continuous UV exposure.

Fourier-Transform Infrared Spectroscopy (FTIR)

We used FTIR to measure the amount of photodegradation. FTIR spectra were

collected on a Nicolet 6700 FTIR spectrometer (Thermo Scientific, Waltham, MA, USA),

and analyzed using the software Essential FTIR. The spectra were produced from 32

scans at a 4 cm-1 resolution. We quantified photo-oxidation by calculating the area

underneath the peak in the 1750 – 1600 cm-1 region (Wen et al., 1988), which corresponds to the carbonyl group.

32 Statistical Analysis

We performed a one-way ANOVA and Tukey multiple comparison tests (α = 0.05)

to compare the different specimens with respect to the amount of UV degradation to

the material underneath. All statistical tests were implemented in R v.3.0.1 (The R

Foundation, Vienna, Austria) (R Development Core Team, n.d.).

UV transmittance through eggshell and TiO2 particles suspension films

We purchased white and brown chicken eggs from a grocery store. The egg white and yolk were carefully removed and were washed with DI water and 100% ethanol. White and brown egg shells were separately ground using a pestle and mortar into fine particles. Titanium dioxide (TiO2) nanoparticles of size less than 100 nm were purchased from Sigma Aldrich. We made three suspensions using 50 mg eggshell particles (white and brown) and TiO2 particles in 500 µl DI water resulting in 100 mg/ml suspensions. However, the particles settled down and did not form uniform suspensions. Hence, the suspensions were mixed thoroughly before casting films. We made films by drop casting 100 µl of the suspension on a glass slide and letting them dry overnight.

Scanning Electron Microscopy (SEM)

We used spectrophotometry to test for color changes of the polymers indicating photodegradation. We also used SEM to determine the morphology of the films of the eggshell and TiO2 particles. We mounted the samples onto aluminum stubs using double-sided tape, which we sputter-coated with gold/palladium for 3 min. SEM

33 (JSM7401F, JEOL Japan) images were taken at a working distance around 8 mm with an

accelerating voltage of 5 kV.

UV-Vis Spectrophotometry

We used spectrophotometry to test for color changes of the polymers indicating

UV damage. We measured diffuse reflectance of the polymer samples between 300 and

700 nm. We used an integrating sphere (AvaSphere-50-REFL) with a black gloss trap to

exclude specular reflectance, an AvaSpec-2048 spectrometer, and an AvaLight-XE pulsed

xenon light source (Avantes Inc., Broomfield, CO, USA). All reflectance measurements

were taken relative to a diffuse white standard (WS-2, Avantes Inc.).

We also used spectrophotometry to measure the transmittance of UV light

through the eggshell and TiO2 films. The spectrophotometer was equipped with two fibres that rotate independently from one another. One fibre was connected to a light source (AvaLight-XE pulsed xenon light) and the other fibre to a spectrophotometer

(AvaSpec-2048, Avantes Inc., Broomfield, CO, USA). Transmittance measurements were normalized using a glass slide as standard. Light was incident normal to the suspended film.

Results and Discussion

UV Aging of two synthetic polymers

Temperature Measurement

Although we set the temperature of the UV aging chamber to 45°C, we measured the temperature underneath the eggshells and quartz coverslips (Fig. A.5) to investigate if the eggshells affected the temperature underneath the surface. The

34 highest temperature measured was 46°C, and there was no noticeable difference in temperature between the eggshells and the quartz coverslips. Pigmentation of eggshells has been hypothesized to increase the temperature inside the eggs (Lahti et al., 2016), but UV-radiation alone did not cause an increase in temperature beneath the eggshell surfaces (Fig. A.5). Thermal oxidative degradation of the polymers only occurs on temperatures above 120°C (Thanki and Singh, 1998), thus any degradation of the polymers detected is not due to thermal oxidative degradation and thus can be attributed to photo-oxidation caused by UV-radiation.

Scanning Electron Microscopy

Scanning electron microscopy (SEM) images showed that 800h of UV exposure caused cracking of both synthetic polymers in the control specimens, but when they were covered with eggshells their physical integrity was maintained (Fig. 3.2). The eggshells thus provided a protective covering to the polymers against the high energies of UV-radiation that caused physical damage in controls.

Figure 3.2. SEM images of polystyrene (a) and nylon (b) before and after UV exposure. Scale bars = 200 µm. Arrows highlight cracks formed in the polymer.

35 Spectrophotometry

We measured diffuse reflectance of the polymers before and after UV exposure

to measure if it caused alteration of optical properties (Fig. 3.3). Polystyrene showed

yellowing after UV exposure, which was clearly visible to human eyes (Fig. 3.3(b)) and

detectable with spectrophotometry (Fig. 3.3(a)). There was a clear difference in the

degree of yellowing between the control specimen and the eggshell specimens.

However, there was no distinguishable difference between the white and brown

eggshells. UV exposure did not change the color of the nylon specimens (Fig. A.6).

Figure 3.3. Diffuse reflectance spectra show changes in optical properties of polystyrene after UV exposure in the control but not when covered by eggshells (a). Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error. The yellowing of polystyrene is visible to the human eye (b).

36 Fourier-Transform Infrared Spectroscopy

We used Fourier-Transform Infrared Spectroscopy (FTIR) to investigate if UV- radiation caused decomposition and formation of chemical bonds in the synthetic polymers (Fig. 3.4 & 3.5). The FTIR spectra showed that UV degradation caused a significant increase of the peak in the 1750 – 1600 cm-1 region for both polymers compared to the controls (full spectra see Fig. A.7 & A.8). This region corresponds to the carbonyl group and may increase due to photo-oxidation (Wen et al., 1988). UV degradation was greater for polystyrene (Fig. 3.4) than nylon (Fig. 3.5(a,b)). Covering the polymers with eggshells provided a significantly greater protection against UV degradation than controls (Fig. 3.4 & 3.5; statistics see table A.2 & A.3). Covering nylon with eggshells provided a significantly greater protection against UV degradation than the nylon with embedded UV-protective additives (brown eggshell vs. UV-protective additive 57.1% higher; white eggshell vs. UV-protective additive 43.5% higher UV protection; Fig. 3.6). FTIR analysis showed that the sample with the UV-protective

-1 additive had an extra peak around 3700 cm , which corresponds to that of TiO2 (Hirose

et al., 2008). Surprisingly, the TiO2 peak was no longer detected after 100h of UV

exposure (Fig. 3.5(d)). A possible explanation is that the TiO2 particles are still present deeper in the polymer, but are not detected by FTIR, which is limited to detection of the surface (Yang et al., 2004). Interestingly, nylon photo-oxidized at the highest rate for the first 100h, but the rapid photo-oxidation rate slowed down for the remainder of the treatment period (Fig. 3.5(b)). Zan et al. (2004) showed that TiO2 particles enhanced

photo-oxidative degradation of polystyrene by generating reactive oxygen species under

37 UV-illumination (Zan et al., 2004). The hydroxyl radicals and active oxygen species formed attack the C–H bond in the polymer chain to form the carbonyl group (Zan et al.,

2004). Chen et al. (2007) showed that the crystal structure also plays an important role as anatase TiO2 nanoparticles were intrinsically more photo-catalytically active than rutile TiO2 nanoparticles in photo-oxidative degradation of polyurethane (Chen et al.,

2007). A possible explanation for our results is that during the first 100h TiO2 particles led to an increase of the efficiency of the photo-oxidative degradation of nylon, which slowed down after the loss of TiO2.

Figure 3.4. FTIR spectra of polystyrene before and after 800h of UV exposure (a). The inset shows the degree of photo-oxidation (b), which is the calculated by integrating the area underneath the peak in the 1750 – 1600 cm-1 region. Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error.

38 Figure 3.5. FTIR spectra of nylon before and after 800h of UV exposure (a). The inset shows the degree of photo-oxidation (b), which is the calculated by integrating the area underneath the peak in the 1750 – 1600 cm-1 region. The FTIR spectra show that the sample with the UV-additive has an extra peak around 3700 cm-1 (c), which disappeared after 100h of UV exposure (d). Plotted lines are group mean spectra (n=6) with shaded areas representing the standard error. 4.5 4.0

3.5 B 3.0 2.5 UV degradation A 2.0

C

1.5 C

UV-additive Quartz control Brown eggshell White eggshell

Figure 3.6. Boxplots showing the degree of UV degradation of nylon after 800h of UV exposure. Box = 25th and 75th percentiles, with median shown as a thick line; bars are minimum and maximum values. Means with different letters (A,B,C) are significantly different (Tukey’s HSD, p <0.01, n= 6).

39 UV transmittance through eggshell and TiO2 particles suspension films

The suspension films of the eggshells show that the particles had irregular sizes and geometries (Fig. A.9), while the suspension film of TiO2 particles is more

homogenous. Some particles of the ground eggshells were too large, making

measurement of the size-range of the particles by Dynamic Light Scattering impossible.

However, SEM images (Fig. A.9(b)) showed that some particles were larger than 100

microns, an order of magnitude larger than the TiO2 particles, which are approximately

100 nm. Nevertheless, we were able to make films of the eggshell particles and measure

UV transmittance using a UV-Vis spectrophotometer (Fig. 3.7). For all three films, the UV

transmittance was low (under 10%) and not significantly different. This promising result

suggests that unprocessed waste chicken eggshell in a more useful format (i.e. ground

into a powder) likely will provide UV protection, as UV-radiation does not pass through.

However, we do not know why UV is not transmitted through the films (i.e. UV

reflection, absorption or scattering), so further experiments should be performed to test

the applicability of eggshell particles as UV-protective additives for industrial

applications.

40 Figure 3.7. The suspension films of TiO2, white, and brown eggshell particles trap most of the UV light. The three films show comparable transmittance values that are well below 10%. Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error.

Conclusion

Chicken eggshell waste is becoming an environmental concern due to its rapidly

increasing amount and high costs to dispose it. In particular unprocessed eggshells are

considered a problem, as the protein-rich membrane attracts rats to landfills (Walton et

al., 1973). Moreover, the processing of eggshells is cumbersome and expensive, thus

further increasing the likelihood that chicken eggshells will be classified as waste (Than

et al., 2012). It is thus of increasing interest to find valuable applications for

unprocessed eggshells. In our study we showed promising results for the use of

41 unprocessed eggshells in providing protection against photo-oxidative degradation of

polymers. The placement of eggshell pieces provided effective and durable protection

to nylon and polystyrene during 800h of high UV-illumination. The nylon protected with

eggshells showed slower photo-oxidative rates compared to nylon that was protected

with embedded TiO2 particles. The UV protection was 57.1% higher for brown eggshell and 43.5% higher for white eggshells than that of nylon with TiO2 particles. Surprisingly,

the photo-oxidative rate was high during the first 100h of UV exposure for nylon with

embedded TiO2 particles, but after loss of TiO2 it slowed down. It is likely that the presence of TiO2 actually increased the efficiency of photodegradation due to the formation of active radicals rather than providing photoprotection.

It is unlikely that pieces of eggshells would be used in this form for practical applications. We took one step to determine if eggshells would also be useful in a more practical format. Our results showed that a thin film of grinded eggshell particles had the same capacity as a thin film of TiO2 particles to omit UV radiation to pass through. A next step will be to compare the UV-resistance of a nylon strip with embedded chicken eggshell particles with that of a nylon strip with embedded TiO2 particles.

Synthetic CaCO3 particles have been widely used as inorganic filler for many

industrial applications, including construction, healthcare, polymer industry and

coatings (Tegethoff et al., 2001), but the use of chicken eggshells might provide

significant differences. Although chicken eggshells are also predominantly made from

CaCO3, they also contain organic component. Biominerals in many cases show superior

42 properties to synthetic equivalents (Mann, 2001) and their nanostructural organization

is often organized in hierarchical levels, making them distinct from traditional

engineered composites (Gower, 2008). For example, different or even new crystal faces

that cannot be expressed in synthetic CaCO3 are preferred in biominerals, leading to stronger materials that are more resistant to fracturing (Okumura et al., 2013).

Therefore, the use of waste chicken eggshells as organic-inorganic composites as alternative to engineered composites can be attractive for various applications. Even more, chicken eggshells are being used as food additive and as a source of calcium in animal and human nutrition (Than et al., 2012), thus providing evidence that is not harmful. Possible applications where eggshell particles could be used as UV-additives include synthetic polymers such as polystyrene and sunscreens. Polystyrene is widely used in building and packaging as expanded foam, but undergoes light-induced yellowing (Yousif and Haddad, 2013). As previously noticed (Zan et al., 2004), and confirmed in our study, TiO2 particles can actually speed up its photo-oxidative

degradation rather than providing photoprotection. Sunscreens often includes TiO2

particles as inert light scatters and are suppose to provide improved protection in the

UVA region (Ricci et al., 2003). However, it is shown that the presence of TiO2 can

actually increase the loss of UV protection due to photodegradation of the organic fillers

(Dondi et al., 2006; Ricci et al., 2003). Thus, also here the non-harmful eggshell particles

might provide a valuable alternative for TiO2 particles.

43 Acknowledgements

This works is supported by Parker Hannifin and by a Human Frontiers Science

Program grant (RGY-0083). We thank Jonathan Markley and Joseph Horinger for extruding the nylon strips, providing the UV chamber, and assisting with the FTIR measurements. We thank my colleagues of the Shawkey lab for comments on the manuscript and specifically Branislav Igic for helping with the statistics.

44 CHAPTER IV

BIOMIMICRY: A PATH TO SUSTAINABLE INNOVATION

Published in Design Issues:

Kennedy*, E., Fecheyr-Lippens*, D., Hsiung, B. K., Niewiarowski, P. H., & Kolodziej, M.

2015. Biomimicry: A Path to Sustainable Innovation. Design Issues 31(3), 66-73.

* Co-first authors

Introduction

In his 1998 article “Design for a sustainable world,” Victor Margolin argues that our ecological plight is beckoning designers to broaden their purpose beyond shaping commodities for clients (Margolin, 1998). Designers are poised to become agents of change that guide a sustainability transition. To do so, they must proactively mold the future profile of their profession by strategically adopting new forms of practice (Findeli,

2001). Biomimicry is an emerging paradigm that can help launch designers into their new role as sustainability interventionists. However, biomimicry does not necessarily render sustainable outcomes. To increase the likelihood of sustainable outcomes,

45 practitioners must consider the form, process, and ecosystem levels of biomimetic design.

The purpose of this paper is to introduce scholars, students, and professionals in all fields of design to biomimicry and its potential to yield sustainable outcomes when practiced in a deep, thoughtful way. The design community is an important leverage point for fueling dialogue about biomimicry because designers work “at the nexus of values, attitudes, needs, and actions,” and, therefore, are uniquely positioned to act as transdisciplinary integrators and facilitators (Wahl and Baxter, 2008).

What is Biomimicry?

Biomimicry involves learning from and emulating biological forms, processes, and ecosystems tested by the environment and refined through evolution (Baumeister,

2014). Biomimicry can be applied to solve technical and social challenges of any scale

(Benyus, 1997). Biology has inspired design since prehistoric man fashioned spears from the teeth of animals and mimicked the effective sneak-and-pounce hunting technique of large predators, but the development of a methodological framework for translating biological strategies into design innovations is a recent one. American inventor, Otto

Schmitt, coined the term “biomimetics” in the 1960s to describe the transfer of ideas from biology to technology1 (Harkness, 2002). Three decades later, biomimicry was popularized by Janine Benyus who broadcast its enormous potential to inform a new era

1 Schmitt transferred knowledge of the transmission of electrical signals across squid nerves to develop a positive feedback electrical circuit called a thermionic trigger (Schmitt, 1938).

46 of design in her critically acclaimed book, Biomimicry: Innovation Inspired by Nature

(Benyus, 1997).

Biomimicry is a burgeoning field of study, as evidenced by a growing demand for training in biomimicry theory and practice (Lepora et al., 2013) and a fivefold increase in biomimicry patents, scholarly articles, and research grants since 2000 (Fermanian

Business & Economic Institute, 2013). According to a report by the Fermanian Business

& Economic Institute, biomimicry could account for $425 billion of U.S. GDP and $1.6 trillion of global output by 2030 (Fermanian Business & Economic Institute, 2013). The popularization of biomimicry is exciting not just because of its economic prospects, but because of its tremendous potential to inspire eco-friendly designs at this critical juncture in human history. Biomimicry forces a new set of questions that can be applied to the design process as well as the outcome. Biological designs are, for instance, resilient, adaptable, multifunctional, regenerative, and generally zero-waste. When deeply informed by biology, design thinking shifts away from an anthropocentric model and considers product life cycles and earth system limitations.

Some argue that the sustainability criterion is too limiting (Rawlings et al., 2012) but “smart companies now treat sustainability as innovation’s new frontier” (Nidumolu et al., 2009). When tackled appropriately it offers opportunities for lowering costs and generating additional revenues, and enables companies to create new businesses to achieve competitive advantage. However, "imitation of the living world is not by default environmentally superior” (O’Rourke, 2013; Reap et al., 2005). Therefore, it is important

47 to inform designers, among others, about the circumstances under which biomimicry is most likely to lead to sustainable solutions, in order to enable them to engage with the future in a more direct way (Margolin, 2007). At its best, biomimicry is an elegant merger of sustainability and innovation that allows designers to continue earning a living within a system of consumer culture (Margolin, 1998), while working alongside biologists to co-create a human civilization able to flourish within the ecological limits of our planetary support system (Margolin, 1998; Wahl and Baxter, 2008).

Biomimetic design practice

Biologists are key players in the biomimicry design process, as it relies heavily on biological knowledge; however, the role of the designer remains central. This is particularly true when it comes to abstracting biological strategies into more broadly- applicable design principles, and implementing them to solve human challenges

(Baumeister, 2014). The aim of biomimicry is not to create an exact replica of a natural form, process, or ecosystem; it is to derive design principles from biology and use those principles as stimulus for ideation. That said, a final biomimetic solution should clearly evidence a transfer of functional or organizational principle from biology. After all, the whole purpose of biomimicry is to tap the knowledge embodied by nature’s 3.8 billion years of research and development (Benyus, 1997) and that is not possible if the functional analogy between the natural model and the final design is lost in translation.

48 Biomimicry and Sustainability

The direct connection

Humans are currently using energy and resources unsustainably. Through

biomimicry, designers can guide development of technologies that have net zero or net

positive environmental consequences, because biological solutions have been time-

tested by billions of years of evolution and embody successful strategies for thriving on

earth (Baumeister, 2014). To demonstrate how biomimicry – repurposing nature’s best

ideas to solve human challenges – can help inform sustainable design, consider the

following. TRIZ, a widely-used engineering problem-solving tool was adapted to create

BioTRIZ (Vincent and Mann, 2002). The original TRIZ, developed by Soviet inventor

Genrich Altshuller and his colleagues in 1946, is a matrix where intersections represent engineering tradeoffs; for instance, to make a vehicle go faster, you need more power, which consumes more fuel (Domb, 2012). At each intersection there is a cell containing

numbers which reference technological design principles for resolving a trade-off

(Domb, 2012). For example, if the vehicle’s body is made more aerodynamic, you can make the vehicle go faster with the same amount of power and fuel. To create BioTRIZ, researchers analyzed 2500 trade-offs and resolutions in biology, and populated a matrix

with biological, instead of technological design principles (Sartori et al., 2010). Analysts

found there is only 12% overlap between trade-off resolutions recommended by BioTRIZ

versus TRIZ, which shows biology solves problems differently than technology. In

technology, the manipulation of energy may account for up to 70% of the solution,

whereas in biology, energy never figures into more than 5% of the solution. Instead of

49 manipulating energy, biological solutions tend to leverage information transfer and structure (Bogatyrev and Bogatyreva, 2009; McKeag, 2013).

Biomimicry marks a divergence from the unsustainable Industrial Revolution, which was “an era based on what we can extract from nature” (Benyus, 1997).

Emulating biology is different from harvesting or domesticating organisms to accomplish a desired function. This may seem obvious, however newcomers to biomimicry commonly seek “to use an organism to ‘do what it does’ instead of leveraging the design principles embodied by the organism. This is the equivalent of using fireflies themselves to produce light, rather than understanding and applying the complex chemistry involved in bioluminescence” (Helms et al., 2009).

The deeper connection

Beyond the direct connection between biomimicry and sustainability – the simple fact that in emulating biological systems we are emulating strategies time-tested by evolution – there is a much deeper connection. Biomimicry does not necessarily render sustainable outcomes, and that fact cannot be overlooked (Reap et al., 2005). A biomimetic solution could get high marks in functional performance but fail miserably in a sustainable life cycle analysis (Reap et al., 2005). Designers who want to use biomimicry to create more sustainable designs must strive to emulate biological lessons on three levels - form, process, and ecosystem (Baumeister, 2014). This multilevel approach is most effective for achieving solutions that awe in terms of sustainable performance.

50 1. Form

The first level is emulating form. The shape and support ribs of the giant leaves

of the Amazon water lily can inform a new innovation of lightweight but structurally

strong building panels (Attenborough, 1995). However, this innovation may or may not

be sustainable. For example, if these panels are made of toxic materials that pollute the

environment, the costs outweigh the benefits.

2. Process

The second level of biomimicry focuses on emulating biological processes; more

specifically, how nature manufactures. Nature assembles structures at ambient

temperature and pressure using non-toxic chemistry2 (Faludi, 2005). By contrast, most

factories form product by carving, bending, melting, casting, or otherwise manipulating

large blocks of raw material at high temperatures and pressures. Compared to biological

manufacturing, the factory approach shows tremendous room for improvement. It is

much more energy-intensive, polluting and wasteful (Faludi, 2005).

It will be difficult to encourage a large-scale shift from traditional to biomimetic

manufacturing given the markedly different infrastructure required. A team might

envision a biomimetic solution that is environmentally sustainable, in theory, but if no

2 There are always exceptions to a general rule. For instance, bombardier beetles defend themselves against predators by ejecting a steaming hot spray of noxious chemicals. The spray is generated internally when two chemicals, hydroquinone and hydrogen peroxide, stored in separate reservoirs in the beetle's abdomen, are mixed in a third chamber with water and catalytic enzymes (Beheshti and Mcintosh, 2007). This brings the water to a boil. Despite this being a case of a biological organism using extreme heat to manufacture, it is worth noting that bombardier beetles generate this heat by way of a simple chemical reaction, as opposed to using large amounts of electricity or other external energy sources.

51 appropriate manufacturing techniques are at hand it might be impossible to realize. The development of infrastructure required to manufacture environmentally-friendly, cost- effective biomimetic products is lagging behind (Bruck et al., 2007). One major challenge is that nature builds using a very small palette of materials, constructed from a small subset of chemical elements, each of which is abundantly available on earth (namely carbon, hydrogen, oxygen, nitrogen, phosphorous, and sulfur). Nature arranges basic building blocks to enable high performing, multifunctional design. A beetle’s shell provides strength, breathability, color, and waterproofing, but is only made from one polymer – chitin – that in turn is made from only four chemical elements – carbon, hydrogen, nitrogen and oxygen (Hepburn and Ball, 1973). In contrast, a chip bag is made of several different materials that each fulfills a separate function. The beetle’s shell is biodegradable, but the chip bag ends up in a landfill. In order to produce our own multifunctional materials from a small chemical palette we still have much to learn about biological construction. Additionally, biological manufacturing has a higher fault tolerance. Even with minor defects, natural systems are usually still fully functional. The tolerance for a discernable degree of variation would allow for fabrication noise, offering ways to create successful designs with lower production cost (Starkey and

Vukusic, 2013).

One example of a promising approach to improve manufacturing is 3D printing, which involves forming a solid object from a digital model by laying down successive layers of material. This mimics nature’s additive, material-efficient manufacturing processes. Advances in 3D printing are unbelievably exciting, but 3D printing processes

52 urgently need tweaking before this technology can be considered eco-friendly. There are opportunities to enhance the technology by looking at other aspects of biological manufacturing. Right now, 3D printing uses toxic resins, ceramics, and powdered metal as feedstock (Howard, 2013), but research is currently being conducted to investigate the viability of using benign locally-sourced feedstocks such as waste woodchips, used paper, plastic scrap, clay, or carbon dioxide (Baechler et al., 2013; Henke and Treml,

2013). At the end of the 3D-printed product’s lifecycle, it could be disassociated using naturally occurring enzymes, returning it to printing feedstock for 100% recycling

(Howard, 2013). We can also improve 3D printing if we stick material layers together using attractive forces like hydrogen or ionic bonds, because there would no longer be a need for toxic glue between the additive layers of a 3D-printed object. Another pressing problem is the amount of energy the printing process consumes. Currently, 3D printers consume an estimated 50 to 100 times more electrical energy than injection molding to create a product of the same weight (Lipson and Kurman, 2013).

3. Ecosystem

Even emulating both form and process does not guarantee development of a product with net zero or net positive environmental impact (O’Rourke, 2013). The design might still be lacking in terms of how it fits within the larger ecosystem. All organisms are part of a biome that is part of the biosphere. As such, every organism’s continued prosperity is dependent on the health of the biosphere (Braungart and McDonough, W., 2008; McDonough, W., 2005). The highest level of biomimicry, emulating the ecosystem, is most difficult because it requires skilled systems thinking to make sure the design fits seamlessly within the biosphere. Biomimicry 3.8 (the 3.8 stands for 3.8 billion years of evolution) developed a creative commons tool called Life’s

53 Principles that helps evaluate a biomimetic design’s ecosystem-level sustainability. Life’s Principles summarizes repeated patterns and principles embodied by organisms and ecosystems on earth. These patterns and principles are thought to support a sustaining biosphere (Baumeister, 2014). In total, the tool outlines six major principles and 20 sub- principles (Fig. 4.1). Inconsistencies with Life’s Principles are indicators of a potentially unsustainable innovation and identify opportunities to further optimize your design. These inconsistencies are easier to detect and resolve when the tool is used as a benchmark throughout the entire design process, and the team makes an effort to integrate Life’s Principles along the way.

Figure 4.1. Life’s Principles is a systems-thinking tool that contains common principles embodied by most species on Earth. Its purpose is to help practitioners create designs that fit seamlessly within the larger natural system. Permission to reprint image granted by Biomimicry 3.8.

54 Biomimetic designs, like all designs, can be used in a variety of ways, including those that are potentially dangerous and counterproductive. Another aspect of ecosystem-level biomimicry focuses on ensuring biomimetic designs are used in ways that are socially beneficial. It is not always possible to regulate how innovations are used, but it is still important that designers do what they can to encourage solutions are deployed to do “what is possible and useful” rather than “what is possible, but harmful”

(Gebeshuber et al., 2009). The Defense Advanced Research Projects Agency (DARPA), has been the biggest financial supporter of biomimicry research as well as development of biomimetic concepts (Johnson, 2010). DARPA recognizes that if understood properly, biological strategies could inform new defense capabilities. DARPA’s Defense Sciences

Office (DSO) focuses on “understanding and emulating the unique locomotion and chemical, visual, and aural sensing capabilities of animals” (DARPA, 2008). DARPA’s DSO funded the development of BigDog, a dynamically stable quadruped robot that can run over rough-terrains and carry heavy loads. BigDog mimics quadruped mammal leg articulation, with compliant elements that absorb shock and recycle energy from one step to the next (Boston Dynamics, 2013). DARPA appreciates BigDog as a robotic mule to accompany soldiers in terrains too rough for conventional vehicles. Biomimetic robotic technologies like BigDog can be used in both productive and destructive ways3.

They can venture into remote or dangerous areas, preventing possible human injury or

3 Our focus here is on the technology itself. We do not provide comment on the essentiality of a military as that would reach far beyond the scope of this paper. We also assume in this discussion that the robot was made in an environmentally sustainable way, which in many cases has not yet been accomplished.

55 death. They can dismantle mines or locate survivors after a chemical disaster. On the other hand, robots can be used to illegally surveil or kill innocent civilians.

Design affects how we interface with the world, so we should balance the profound innovation possible through biomimicry with a lens of environmental and social scrutiny. This requires effort on the part of the designer to selectively transfer desirable aspects of the natural model to the final design and advocate for it being used for positive ends. That said, the lofty ideal of net social and environmental contribution should not dissuade designers from using the biomimicry approach. A biomimetic design that does not achieve net positive impact but does improve environmental or social performance by any increment versus the status quo is worth pursuit. Every biomimetic design is at least one pace in the marathon towards a better relationship with each other and our natural environment.

Conclusion

Given our ecological plight, now is the time for designers to broaden their purpose beyond just shaping commodities according to client specifications (Margolin

1998). Designers have a unique opportunity to act as sustainability interventionists. To do so, designers must adopt new forms of practice that yield sustainable solutions. One such emerging practice is biomimicry, which involves repurposing biology’s best ideas to solve human challenges.

Biomimicry has generated designs that are environmentally and socially sustainable. Consider the success of Stabilitech, a UK company that has created a biomimetic technology that allows storage and handling of biological samples without

56 refrigeration. Traditionally, biological materials such as vaccines have to be kept refrigerated until delivery to the patient to prevent them from degradation. Healthcare facilities in developing countries lacking reliable refrigeration infrastructure were forced to discard half of supplied vaccines due to problems with temperature control (Jennings and Wcislo, 2012). Some organisms like spikemoss, tardigrades and brine shrimp are able to temporarily halt their metabolism in response to adverse environmental conditions such as extreme dryness and cold temperatures (Clegg, 2001; Crowe et al.,

1992; The Biomimicry 3.8 Institute, n.d., n.d.). By mimicking the principles of biological mechanism, Stabilitech successfully developed non-toxic and inexpensive chemical excipients that stabilizes biological materials in ambient temperatures (Drew, 2007;

Ritter, 2012). Now viable vaccines be made available to a greater number of people in developing countries for a lower cost. And, the technology is sustainable. According to a

Stanford University pilot project, shifting the storage of biological samples from frozen storage to room temperature could result in 200,000 million BTUs refrigeration energy savings and more than 18,000 tons of associated reduced carbon dioxide emissions per decade over the next ten years (Jensen, 2009).

Design practitioners can set an example for others by practicing a deep form of biomimicry, which considers emulation of form, process, and ecosystem. This multilevel approach should not be limiting – it is not an all or nothing – but is most likely to lead to solutions that awe in terms of sustainability. There is still much to be investigated and learned about biomimicry in order for the paradigm to mature. The more design practitioners adopt biomimicry, the quicker this can happen. Through trial-and-error,

57 biomimetic design practitioners will evolve best practices. Similar to nature’s way, mal- adapted strategies should rapidly disappear or transition into better-adapted ones.

Every attempt at biomimicry provides value in the form of lessons learned and regular practice will encourage a sense of responsibility to care for nature, as mentor and source of inspiration for innovative solutions (Yen et al., 2010).

Acknowledgments

We thank D. Page, A. Iouguina, C. Hastrich, M. Shawkey, L. D'Alba, R. Maia, C. Eliason,

A. Stark and S. Engelhardt for reviewing this manuscript and offering insightful feedback prior to submission.

58 CHAPTER V

APPLYING BIOMIMICRY TO DESIGN BUILDING ENVELOPES THAT LOWER ENERGY

CONSUMPTION IN A HOT-HUMID CLIMATE

Fecheyr-Lippens*, D., Bhiwapurkar*, P. 2017 Applying biomimicry to design building envelopes that lower energy consumption in a hot-humid climate. Architectural Science

Review, 1(11), 360

* Co-first authors: DFL contributed to the biomimicry part, whereas PB contributed to the architectural engineering and simulations. Both authors contributed towards synergy of biomimicry and design applications.

Summary

Design thinking in architecture has shifted due to an increasing concern in climate change, and the role it plays in energy consumption. The majority of energy usage of buildings can be attributed to maintaining comfortable indoor temperatures.

The building envelope is a key design element, as it separates indoor and outdoor conditions. Our study uses the solution-based approach for generating biomimetic

59 architectural concepts described by (Badarnah and Kadri, 2014). Our proposed biomimetic design was inspired by the adaptive strategies of the African reed frog and the Hercules beetle. It incorporates a hydrogel chamber, embedded phase changing material, and the use of adaptive thermal comfort, and can be integrated into a common curtain wall. We calculated potential energy savings using

DesignBuilder/EnergyPlus, based on the thermal behaviour of a small-sized office building in Chicago. Our results show a potential of up to 66% reduction of the HVAC- related energy use intensity, thanks to a decrease of cooling energy needs.

Introduction

Scientific evidence and greater awareness about climate change and environmental pollution has influenced architectural design in the 21st century.

Architecture plays a crucial role; buildings worldwide use 20-40% of total consumed energy, largely through heating and cooling building interiors. HVAC systems account for

48% to 57% of total energy consumption depending upon geography (U.S. Energy

Information Administration (eia), 2013) and when lighting is also considered this number rises above 65% (CBECS, 2012). Warming urban climates and increasing frequency of extreme heat events are expected to have a significant impact on future energy consumption (Huang and Gurney, 2016). The building envelope is the most important structural subsystem affecting the energy balance of the building (Schittich et

60 al., 2006), and is therefore an ideal element to optimize for improved thermal behaviour.

The building envelope is usually a static barrier between exterior environmental variables and dynamic inside activities. A new architectural trend is to make an adaptive envelope that is responsive to both exterior and interior variable environments

(Armstrong, 2012). The ability to adapt to conditions is relatively new to the field of architecture, whereas it's a phenomenon as old as life itself. Living organisms are able to adapt to changing weather conditions while maintaining their body temperature in very narrow ranges, because they implement physiological, morphological, and/or behavioural means for thermoregulation (Badarnah, 2015). In this context, biomimicry

(i.e. the emulation of biological strategies) has a huge potential as a design tool to improve the sustainable performance of buildings.

In 1997 Janine Benyus popularized biomimicry as an emerging discipline that mimics nature’s forms, functions, processes, and systems to create a healthier, more sustainable planet (Benyus, 1997). The use of biomimicry as a design approach to specifically redesign building envelopes has recently become more prevalent (Badarnah

Kadri, 2012; Gosztonyi et al., 2013; López et al., 2017; Mazzoleni, 2013). For example, studying the mechanism of how plant stomata function in relation to gas exchange resulted in building envelopes adaptive to varying environmental conditions (López et al., 2015). The banana slug inspired the design of a greenhouse with an adaptive envelope that adjusts and changes according to weather conditions, and collects rain

61 water to irrigate the plants, with overflow stored for further irrigation (Mazzoleni,

2013).

However, copying nature doesn’t necessarily result in more sustainable solutions

(Reap et al., 2005). It is therefore important to consider different levels of emulation: form, process and ecosystem (Benyus, 1997). Mimicking natural strategies in buildings can occur at many levels. For example, you could simply create a building that only mimics form for aesthetics (e.g. Tirau’s iconic dog building in New Zealand) or one that mimics a natural form to provide additional functionality (e.g. the glass panels of the

Waterloo International Terminal mimic the flexible scale arrangement of pangolin, which allows the building to respond to changes in air pressure when trains are entering and departing from the terminal) (Zari, 2010). In addition to mimicking form, it is also important to consider the manufacturing process—nature often uses self-assembly and readily available materials (Benyus, 1997; Whitesides and Grzybowski, 2002). For increasing the likelihood of sustainable outcomes the ecosystem level should also be taken into account by considering how a building will function in a particular habitat and integrate with the already existing urban system (Weissburg, 2016; Zari and Maibritt,

2017). Using biomimicry for creating more sustainable designs requires a thoughtful practice and an interdisciplinary approach from the onset (Kennedy et al., 2015). The development of methodological tools to support a biomimicry approach for energy- efficient building design provides a framework for biomimicry’s successful implementation (Badarnah and Kadri, 2014; Chayaamor-Heil and Hannachi-Belkadi,

2017). Badarnah and Kadri (2014) provide a systemic review on different biomimicry

62 methodologies. Currently two different approaches have been recognized: either starting from a design challenge (i.e. top-down (Speck and Speck, 2008), challenge-to- biology (Baumeister, 2014), biomimetics by analogy (Gebeshuber and Drack, 2008), problem-based (Vattam et al., 2009)) or starting from an inspiring biological observation

(i.e. bottom-up (Speck and Speck, 2008), biology-to-design (Baumeister, 2014), biomimetics by induction (Gebeshuber and Drack, 2008), solution-based (Vattam et al.,

2009)).

This paper focuses on how energy needs of a building can be reduced using biomimicry principles. We investigated if the solution-based approach described in

Badarnah and Kadri (2014) can be used to redesign a building envelope that effectively lowers energy consumption while meeting thermoregulatory needs. We will describe our design process in detail, but practically we examined the Hercules beetle (Dynastes hercules) and the African reed frog (Hyperolius viridiflavus nitidulus) as natural models and mimicked their unique biological mechanisms to design a biomimetic building envelope that lowers energy consumption while minimizing energy needs for thermoregulation. Although a biomimetic architectural design is supposedly more responsive to the external and interior environment by design, we introduced a simulation tool that allows the evaluation of its energy performance in a chosen climatic context (Cadenas et al., 2015). Moreover, this allowed us to investigate the importance of each of the different biomimetic design components.

63 Methods

The biomimicry methodology used in this paper (table 5.1) is based on the solution-based approach for generating biomimetic architectural concepts described in

Badarnah and Kadri (2014), which has been adapted from the fundamental work on

Biomimicry Thinking by Baumeister (2014) and the top-down approach developed by the Plants Biomechanics Group led by Thomas Speck (Speck and Speck, 2008). The reason we chose to follow this approach is because we wanted to ground ourselves quickly into the solution space and did not want to restrict our design process to one specific problem. We started with inspiring observations from nature, and focused on the challenges of heat and humidity prevailing in hot-humid conditions to help us identify adaptive biological systems in nature. The two most inspiring examples were the African reed frog and the Hercules beetle because of their adaptive responses to extreme heat and humidity, respectively. It was important to obtain a proper understanding of the biological strategies before we could use them as inspiration in the next phases. To further understand their unique adaptive mechanisms we used the

AskNature.org database and Google Scholar’s search engine to find scientific research papers. Then we explored how these biological strategies could be applied to design an innovative building envelope that lowers energy consumption. We first investigated the thermal behaviour of a prototypical building found in the U.S. to obtain a better understanding of the context of the biomimetic design and this assisted us to abstract the biological strategies into more suitable and applicable design principles. We focused on Chicago because it is considered to have a hot and humid climate, and thus

64 accompanied with intensive HVAC usage. To evaluate our biomimetic design we performed comparative energy simulations to determine if the biomimetic building envelope indeed saved energy and which of the different biomimetic design components is most important for achieving this.

Table 5.1. Solution-based Biomimicry methodology following Badarnah & Kadri.

Strategies African reed frog Hercules beetle Biological domain - Identify biological - African reed frog - Hercules beetle system - Analyse biological - Behavioural & - Cuticle, porous system morphological changes photonic crystal - Understand -Light reflection and - Humidity-based biological principles thermal adaptation colour change

Transfer phase - Understand thermal - High-albedo surface - Passive behaviour of building - Adaptive thermal (de)humidification - Abstract & comfort model - Superabsorbent brainstorm - Delay internal heat polymers gain Technological Implement technology Design and evaluate energy savings of domain through prototyping biomimetic envelope system using performative and testing simulation

Biological domain

The African reed frog

The first biological example which inspired us was Hyperolius viridiflavus nitidulus, a species of the African reed frog that lives in the savannahs of western Africa

(Lampert, 2001). While most savannah frogs hide themselves under sand to escape high temperatures and low air humidity, immature individuals of African reed frog survive the very hot, dry season while fully exposed to the sun and harsh conditions clinging to

65 vegetation. They are highly dependent on water and staying above ground permits

them to catch even the smallest amount of rain or condensation of water (Lampert and

Linsenmair 2002; Geise and Linsenmair 1986). They hold a special sitting position to

minimize water loss, minimize solar exposure, and move only when seriously disturbed.

The African reed frog can survive in harsh dry and hot conditions thanks to its

spectacular physiological adaptations triggered when temperatures reach 36-38°C. Their

unique aestivation behaviour lowers their metabolic rate at high temperatures and arid

conditions. Their body colour changes from beige or grey to a highly reflective white

(Kobelt and Linsenmair, 1986). During aestivation the frog does not urinate or defecate,

holding all nitrogenous waste stored in its body. Yet, high concentrations of urea in body

fluids can be dangerous due to osmotic problems; the frog solves this by converting its

nitrogenous waste into purine crystals which it stores in specialized cells called

iridophores (Schmuck et al., 1988). The number of iridophores increases four to six

times during the dry season forming a layer on the upper part of the skin (figure 5.1).

Because these purine crystals create a high refractive index contrast to the surrounding cytoplasm, the iridophores become light-reflecting cells (Levy-Lior et al., 2010, 2008).

Their position during the dry season is almost parallel to the skin surface, causing them to act as a light reflector similar to a mirror (Kobelt and Linsenmair, 1992). Interestingly, the frog has two other types of specialized cells, chromatophores, which contain certain pigments (Kobelt and Linsenmair, 1986). During the wet season the upper part of the skin will consist mainly of xanthophores (creating yellowish colours) and melanophores

(creating brown/black) resulting in a beige or grey colour (figure 5.1). The number of

66 xanthophores and melanophores does not increase during transitioning to the dry skin.

However, they are shifted to the bottom of the skin and are replaced by layers of iridophores, which results in a highly reflective white coloration.

Brown/Beige (Wet season) White (Dry season)

Epidermis Epidermis Xanthophores Xanthophores

Melanophores Melanophores

Iridophores Iridophores

Figure 5.1. Comparison of the skin of the African reed frog during wet and dry season. The skin contains three types of chromatophores: iridophores (blue), xanthophores (orange), and melanophores (black). The number of iridophores increases significantly during transitioning to the dry season, while the xanthophores and melanophores are shifted to the bottom.

The Hercules beetle

A second organism we have chosen for this study is the Hercules beetle

(Dynastes hercules). Hercules beetles can be found in the rainforest of South and Central

America (Rassart et al., 2008). They are one of the largest beetles in the world and can grow up to 17 cm in length. Being primarily nocturnal makes them particularly vulnerable to predators. Consequently, they have found a way to adapt their body colour to match that of its environment and be less conspicuous. The beetle’s body changes from black on a dark, rainy day or night to an olive-greenish colour during sunny days (figure 5.2). This colour change is reversible, doesn’t need external energy, and happens within mere minutes.

67 The greenish coloration under dry conditions originates from a spongy layer

underneath the transparent epicuticle that has a 3D photonic crystal structure (figure

5.2). Specifically, a network of filamentary strings of chitin are arranged in layers parallel

to the cuticle surface, creating open pores that are filled with air (Rassart et al., 2008).

Because the photonic crystal structure (refractive index n = 1.36) and air (n= 1.00) have

a high refractive index contrast, this causes multi-layer interference (Sun et al., 2013)

resulting in a greenish colour. On humid days, the spongy layer absorbs ambient

moisture. Water (n = 1.33) has a very similar refractive index from the surrounding

chitin so there is no light reflection, which makes the body appear black.

Green (Dry) Black (Humid)

Ambient moisture Epicuticle Chitin filament Chitin filament

Figure 5.2. Colour changing mechanism in the Hercules beetle. A spongy layer of filamentary strings of chitin arranged in layers parallel to the epicuticle, creates open pores filled with air (dry environment) or water (humid environment). Depending on the contrast between the refractive indices, this results in a greenish (dry) or black (humid) colour.

68 Transfer phase

Having an understanding of the biological systems allows for applicable abstraction into design principles that can be used for brainstorming and solution thinking to design biomimetic building envelopes. To realize transferability of relevant design principles to buildings, we first needed to understand how a building behaves as that ultimately determines the context of a successful biomimetic design. We investigated the thermal behaviour of a small office building as a test case using a whole building simulation program, DesignBuilder4.5/EnergyPlus 8.1 (DesignBuilder Software

Ltd, n.d.). This building type was selected because it accounts for significant building efforts in the U.S. and consumes significant amounts of energy (Thornton et al., 2010).

Simulation parameters

A representative 3-storied, small-sized office building of 1366 m² (CBECS, 2012) was modelled per ASHRAE Standard 90.1 Climatic Zone:5A (ASHRAE, 2013) and

Appendix G requirements (standard 90.1 requirements for energy efficient buildings).

This building type represents a majority of the built–up area in the U.S. and therefore it is selected for this investigation. Chicago (IL) was chosen as a suitable test location because it poses heat and humidity related challenges (ASHRAE, 2013) during summer months, thus being a good case study model to demonstrate energy saving potential of our selected biological inspirations.

69 The square shaped building footprint of 21.3 x 21.3 m was chosen for orientation neutrality and based on the existing building stock in the U.S. (Thornton et al., 2010).

The perimeter and core-zoning pattern was adopted for understanding thermal behaviour of the building because it accounts for heat exchanges on differently oriented building facades. Each floor has four thermal zones along the perimeter (depth is 3.65 m, adopted from Thornton et al. 2010) and one core zone (figure 5.3). The summertime temperatures of the cross section of the baseline envelope were taken from a previous study (Bhiwapurkar and Moschandreas, 2010). The floor to floor glazing of 30% is equally distributed on exteriors walls and its thermal properties (i.e. solar heat gain coefficient, U-value, and visible transparency) are kept constant at 30% throughout this study.

Figure 5.3. Thermal zoning: Plan and axonometric view. Each floor has four perimeter zones and one core zone.

The selected envelope construction is based on common practices adopted for small-sized office buildings in the U.S. (CBECS, 2012; Richman et al., 2008) and the interior space is air-conditioned by a packaged single zone DX system with furnace

70 (System3: PSZ-AC). The HVAC system maintains a 23.8°C cooling set-point and 21.1°C heating set-point during occupied hours. During off hours, thermostat set-points are

27.7°C for cooling and 17.7°C for heating. The economizer is set to a maximum dry bulb temperature of 21.1°C. The operating schedule is from 8:00 am to 5:00 pm. Additional details on simulation parameters are published elsewhere (Bhiwapurkar, 2015).

Thermal behaviour of building

The building’s thermal behaviour is determined by an addition or extraction of heat from various thermal zones to maintain the temperature set-point range 21.1-

23.8°C. The building envelope is in constant flux with outside and inside environmental conditions, which influences the building’s thermal behaviour. Solar heat, the primary source of external heat, is transferred inside the building via the envelope—through glazing, walls, and the roof. Thermal properties of these elements determine the heat flow, thus making material choices and its organization in the construction assembly important. Buildings also gain heat from internal sources: electric lighting, equipment, and people, affected by the building’s operating schedule for lighting, equipment, and

HVAC, based on occupancy.

Figure 5.4 presents the thermal behaviour of the middle floor of a 3-storied building based on the amount of heat extracted to maintain the desired thermal comfort range (i.e. heat extraction rate). We chose the middle floor because it is less affected by the roof and ground, which allows us to focus on the building envelope.

Time of day, solar position, and the intensity of radiation play a significant role in the

71 thermal behaviour of the building. The core zone receives heat primarily generated by internal sources while the perimeter zones have a significant external heat load. For example, the East zone receives early solar radiation, warms up quickly, and the heat extraction rate peaks as early as at 11:00 am, reaching 2350W. In contrast, the West zone starts receiving solar radiation after noon and its heat extraction rate peaks at 4:00 pm, reaching 2587W. The Core zone is not exposed to outside conditions and is surrounded by adiabatic internal walls (does not allow heat exchange between zones), keeping the heat extraction rate peak to approximately 600W.

3000

2500

2000

1500

1000

500 Heat extraction rate (W) 0 15 10 15 2024

Time (Hrs)

North Zone South Zone East Zone West Zone Core Zone

Figure 5.4. Heat extraction rate from thermal zones of the middle floor on the hottest day of the year (July

26).

Further investigation of the building envelope shows that when the heat extraction rate peaks, the external wall surface temperature can be up to 27.7°C higher

72 than the outdoor air temperature. In contrast, the internal wall temperature is closer to the room temperature because of indoor thermal conditions. The difference between external and internal wall temperature (ΔT) determines the amount as well as the direction of heat transfer (i.e. from higher to lower temperature).

Abstracted design principles

Our investigation of the thermal behaviour of the building showed that the high heat extraction rate due to the transfer of heat from outside to inside is a key factor contributing to high cooling energy needs. Therefore this became the challenge area for which to focus our biomimetic solutions (as well as the design principles abstracted from the biology). Having a better problem definition and design focus allowed us to abstract the biological principles in a more suitable and applicable fashion.

For the African reed frog, we found the trigger of physiological adaptations according to body temperature to become highly reflective particularly interesting as a strategy to survive the very hot conditions. This inspired us to use a high albedo material to reflect solar radiation and use the indoor temperature to trigger adaptive thermal comfort (ASHRAE, 2004) to minimize cooling energy needs (Dear and Brager, 2001). The adaptive thermal comfort model goes beyond fundamental physics and physiology to determine the range of comfortable inside temperatures, by also including contextual effects such as the physiological responses of building occupants (Brager et al., 2015;

Dear and Brager, 2001). There is empirical evidence of increasing occupants’ satisfaction at the work place with wider temperature ranges (Brager, Zhang, and Arens 2015).

73 Using an adaptive thermal comfort model, the comfort temperature range in this study

has been extended from a narrow 21.1-23.8°C based on the conventional thermal

comfort zone to a wider 21.1-31.7°C by allowing ventilation when it is comfortable

outside (Bhiwapurkar, 2016).

The physiological adaptations in response to high body temperature of the

African reed frog inspired us to think about internal heat gain. An additional design

component that we used for delaying the internal heat build-up is embedding phase

change materials (PCM). These materials melt and solidify at a certain temperature and

therefore are capable of storing and releasing large amounts of energy. They have been

recently introduced for architectural purposes because they can be used for latent heat

storage and delay the peak thermal load (Kośny et al., 2013; Sharma et al., 2009). In this

study, we chose commercially available Bio-PCM made from rapidly renewable and

sustainably harvested non-food natural materials like palm oil by-products, coconut or soy (Phase Change Energy Solutions, 2005).

In summary, the African reed frog inspired us to develop a biomimetic building envelope that minimize the heat extraction rate by reflecting solar radiation, using adaptive thermal comfort, and increasing thermal delay.

The biological principle of the Hercules beetle was abstracted into: “leverage ambient humidity to passively and reversibly absorb water”. Inspired by this strategy, we used a passive reversible dehumidification process that helps support the adaptive thermal comfort in the building. During hot, humid summer conditions, dehumidification improves thermal comfort by removing latent heat via evaporative

74 process (Badarnah, 2015). We chose to use superabsorbent polymers (i.e. hydrogels) for

this application as they mimic the mechanism of the Hercules beetle. Superabsorbent

polymers can absorb and retain extremely large amounts of liquid relative to their own

mass without becoming soft or disintegrating (Zohuriaan-Mehr and Kabiri, 2008).

Hydrogels are superabsorbent polymers that absorb water via hydrogen bonding.

Technological domain: Designing the biomimetic building envelope

The proposed biomimetic building envelope composed of an adaptive thermal comfort approach, a high albedo surface, and an integrated hydrogel and Bio-PCM system, is illustrated in figure 5.5. The biomimetic envelope has three main components and is designed to fit into a common curtain wall system. The first component is a standard glazing and high albedo solid panel system that covers the majority of the façade. The second component is a series of hydrogel dehumidification chambers. The third is a wall integrated with a Bio-PCM layer to remove undesired heat from the air.

The integration with an HVAC system is useful in case additional cooling or humidification is required before circulating the air in the building.

75 HVAC intake

Glazing panel

Curtain wall system Solid panel

4

3 Natural ventillation

Hydrogel chamber

2

Bio-PCM heat exchanger Outside air intake vent

1

Figure 5.5. Graphic showing the main components of the biomimetic building envelope. Hot humid outside air (1) gets dehumidified in the hydrogel chambers (2) and is cooled by heat exchangers (Bio-PCM encapsulated wall) (3). The preconditioned air is used for natural ventilation or circulated via an integrated HVAC system (4).

The biomimetic building envelope is designed to save energy by preconditioning outside air in a four-step process (figure 5.5) while achieving adaptive thermal comfort conditions inside. First, outside air (1) is drawn through a filter and into the hydrogel chambers. As the air passes over the hydrogel (2), the moisture is absorbed, which will

76 increase the temperature of the dried air. Next, the dehumidified and relatively hot, dry air (3) moves over the encapsulated Bio-PCM, which absorbs sensible heat. The air is cooled and the absorbed heat can be used to preheat water entering a domestic hot water boiler (note, this design aspect goes beyond the scope of this paper, and was therefore not included in the study). The pre-conditioned air can be used for natural ventilation or if needed, conditioned further by the HVAC system (4). Based on the air movement through the building envelope system, it is possible to create a mixed-mode and natural ventilation scenario in the building (Brager et al., 2015; de Dear and Brager,

2002). Such variations are explained in the following section. By reducing the dehumidification and cooling loads of the HVAC system, the overall energy use of the building can be greatly reduced.

Evaluating energy saving potential of our biomimetic building envelope

Four variations of the biomimetic building envelope system were investigated for energy saving potential in comparison to the baseline envelope system (table 5.2).

These variations included modification in the existing building envelope system to achieve adaptive thermal comfort using mixed-mode ventilation and natural ventilation, and its combination with the integrated Bio-PCM layer.

77 Table 5.2. Comparison of the baseline prototypical small-office building envelope with the proposed variations of the biomimetic building envelope system.

Biomimetic Baseline* Mixed-mode Natural PCM with mixed- envelope ventilation ventilation mode & natural Component ventilation (Fig. 5.5) 1 Outside air is Outside air (21.1°C Outside air Outside air conditioned – 23.8°C) passes (21.1°C – 31.7°C) (temperature crf. by the roof through the passes through respective top unit and dehumidification the scenario) passes circulated via zone dehumidification through the central duct zone dehumidification system. zone

Dehumidification Dehumidification Dehumidification 2 zone (moisture is zone (moisture is zone (moisture is absorbed by the absorbed by the absorbed by the hydrogel) hydrogel) hydrogel)

3 Heat exchanger (sensible heat stored by Bio-PCM)

4 Fan Coil Unit (FCU) Air is circulated Air is circulated to treat and naturally in naturally in indoor circulate air per indoor spaces, fan spaces, fan indoor thermal assistance is assistance is comfort conditions available to available to achieve (21.1°C – 23.8°C, achieve minimum minimum air 0.3 ac/h) air changes, FCU changes, FCU to to treat and treat and circulate circulate air per air per outside indoor thermal indoor thermal comfort comfort conditions conditions (21.1°C (21.1°C – 31.7°C, – 31.7°C, 0.3 0.3 ac/h) ac/h) * Does not incorporate any of the biomimetic building envelope components presented in figure 5.5.

78 Baseline building envelope

The baseline building envelope (table 5.2) is represented by a dry wall with stucco and board insulation on exterior side (R13+R10ci) whereas the metal deck roof has insulation above (R30ci) that meets the code requirements (see section 2.2.1). The thermal properties of glazing include a solar heat gain coefficient (SHGC) of 0.4, a U- value of 2.38 W/m2K, and a visible transparency of 1. The baseline building with HVAC system maintains 21.1-23.8°C and it is mechanically ventilated using constant air volume during the occupied period. The mechanical ventilation indicates that the outside air and/or re-circulated air is delivered to the thermal zone. In this study, the mechanical ventilation delivers air through a centrally ducted air conditioning system. Simulations were performed using “room ventilation” where mechanical ventilation is modelled using EnergyPlusZoneVentilation:DesignFlowRate data separate from the main HVAC system.

Biomimetic building envelope using mixed-mode ventilation (MM)

The biomimetic building envelope using mixed-mode ventilation uses mechanical ventilation and allows natural ventilation when it is desirable outside while keeping heating and cooling set-points similar to the baseline i.e. 21.1-23.8°C (see Bhiwapurkar

2016). Natural ventilation is made possible with mechanically controlled windows.

Outside air requirement data is set at the zone level and is a sum of mechanical ventilation, natural ventilation, and infiltration in air changes per hour (ac/h). This data can be used for checking occupant discomfort when used together with other

79 environmental elements like air temperature and humidity. The required air changes

per hour (0.3 ac/h) at minimum velocity (0.001524 m/s) in a mixed-mode cooling allow

occupants to adapt to the relatively higher temperatures and humidity in the office

building because the provision of operable (manual or mechanical) windows and the

perception of fresh air improves perceived comfort (Brager and Baker, 2009).

Biomimetic building envelope using natural ventilation (NV)

The biomimetic building envelope using natural ventilation is made possible by

extending the set-points, particularly for cooling, i.e. from 21.1-23.8°C to 21.1-31.7°C.

Adjusting the cooling set-point to 31.7°C, allows the adaptable thermal comfort to be

maintained by natural ventilation only. The mechanical system will only be activated to

heat and cool if temperatures do not fall between the set-points. Maximum natural

ventilation rate is defined using “minimum fresh air requirements per person” and it is

calculated as m3/s = MinFreshAir x NumberPeople /1000.

Biomimetic building envelope with phase change material (PCM)

In this scenario the biomimetic building envelope has a 1 cm Bio-PCM layer integrated in the wall and roof assembly. Both mixed-mode and natural ventilation scenarios described above are simulated with an integrated Bio-PCM layer (i.e. MM-

PCM and NV-PCM respectively).

80 Comparative simulation results

Figure 5.6 shows the comparison of the HVAC-related energy use intensity (EUI)

in the small-sized office building using the variations of the biomimetic building

envelopes over the baseline envelope (table 5.2). The HVAC-related EUI includes

heating, cooling, and fan energy. For our small office building, the summertime HVAC-

related EUI is 59.4% of the total EUI of the building (297.88 MJ/m2), which includes interior lighting, equipment, and HVAC. The HVAC-related EUI presented in this paper is for summer months (April-September) only, where cooling energy need is very high

(88.9%) compared to the heating and fan energy needs (see figure 5.6(a)). The HVAC- related EUI is estimated by dividing the total HVAC-related energy (MJ) by the built-up area (m2).

The baseline HVAC-related EUI is 177.0 MJ/m2. The biomimetic envelope with a mixed-mode ventilation (MM(23.8)) saves 13% of HVAC-related EUI over the baseline scenario. This reduction over the baseline scenario is made possible by a reduction from

177.0 to 154.4 MJ/m2 (figure 5.6(a)). The majority of this saving is attributed to a reduction in cooling energy needs because it reduced conditioning needs when outside conditions were in a comfort range. The mixed-mode ventilation scenario with the Bio-

PCM layer (MM-PCM (23.8)) reduced HVAC-related EUI by 14%. Because the role of

PCM (absorbing sensible heat and delaying thermal lag) is quite limited when the thermal comfort range is limited to 21.1-23.8°C there is almost no difference in energy savings. When we simulated the natural ventilation scenario (NV(31.7)), HVAC-related

EUI is reduced by 48% compared to the baseline scenario and 35% over the mixed-mode

81 (MM(23.8)) scenario. This reduction is made possible by 50% reduction in cooling energy need, although a slight increase in the fan energy is observed (figure 5.6(a)). The natural ventilation scenario with the Bio-PCM layer (NV-PCM(31.7)) further increased cooling energy savings, leading to a reduction of HVAC-related EUI by 66%. The HVAC- related EUI is reduced to 59.4 MJ/m2, which is the lowest among all scenarios. Thus for our best-case scenario the total EUI of the building can be reduced by 39% (i.e. 59.4% of the HVAC-related EUI).

200

160

120

80

Energy use 40

intensity (MJ/sq.m) 0 Baseline MM(23.8) MM-PCM(23.8) NV(31.7) NV-PCM(31.7)

(a) Heating Fan Cooling

4000

3000

2000

1000

0 Heat extraction rate (W) 1193143556779 91 103 115

Monday July 15 - Friday July 19 (Hrs)

Baseline MM(23.8) MM-PCM(23.8) (b) NV(31.7) NV-PCM(31.7)

Figure 5.6. Comparative HVAC-related EUI (a) of different building envelopes where phase change material (PCM), mixed-mode (MM) and natural ventilation (NV) are used with adaptive thermal comfort conditions extending cooling set-points from 23.8°C to 31.7°C. Comparative heat extraction rate (b) of different building envelopes on the south zone of the middle floor during hottest weekdays of the year (Monday, July 15 to Friday, July 19).

82 The energy reduction potential of each envelope is further analysed in figure

5.6(b), which shows changes in the heat extraction associated with the cooling energy during the hottest week of the year, i.e. July 15-21. Only the working days of the week are shown because cooling is turned off during weekdays. We chose to evaluate the south zone of the middle floor of the building because south wall presents maximum opportunity to save energy than other orientations through the year. Figure 5.6(b)) helps understand how the performance of the proposed envelopes varies on a daily basis. For example, cooling needs on Monday July 15 are higher than Friday July 19, where the energy saving potential of the natural ventilation scenario NV(31.7) is highest. The peak heat extraction rate in the baseline scenario (figure 5.6(b), Baseline) is 4286W and occurs at 3:00 pm. In comparison, the peak heat extraction in NV(31.7) at

3:00 pm is only 546W. This is a reduction of 85%. The NV-PCM(31.7) scenario at 3:00 pm reduced heat extraction rate by 75%. The heat extraction rate of each envelope varies during the week changing its energy saving potential. For example, NV(31.7) reduced heat extraction rate by 87%, 81%, 76%, 77%, and 76% during Monday through Friday, respectively. In comparison, NV-PCM(31.7) saves 75%, 59%, 53%, 52%, and 53% during the week. The NV(31.7) scenario is showing maximum savings during the hottest week of the summer while the NV-PCM(31.7) scenario saves maximum energy across summer months. In this study, the envelope integrated Bio-PCM absorbs sensible heat and delays internal heat gain by the walls during occupied hours while natural ventilation provides comfort conditions in adaptable range. This strategy is best demonstrated when the ambient temperature is high and the use of mechanical system is minimal, like

83 in NV-PCM(31.7). Therefore, highest savings are observed when the Bio-PCM and extended set-point at 31.7°C are combined.

Discussion

We adopted the solution-based approach presented by Badarnah and Kadri

(2014) for developing a feasible biomimetic building envelope that reduces energy needs of a small-sized office building in hot-humid conditions. This approach provided a systematic biomimicry design process that helped us reach our goal: to emulate a practical and easily implementable design. However, we added one step to the described approach. Rather than directly abstracting biological strategies into design principles, we first investigated the thermal behaviour of the building in order to obtain a better understanding of the context of the biomimetic design. This allowed us to abstract the biological strategies into more suitable and applicable design principles.

Based on the building thermoregulation investigation, the African reed frog’s ability to manipulate heat build-up and the Hercules beetle’s ability to manage humidity were most inspiring for designs in hot-humid conditions. The African reed frog’s physiological adaption strategies inspired us to use a high albedo surface, phase change materials for delaying heat build-up, and explore adaptive thermal comfort strategies using mixed-mode and natural ventilation. The Hercules beetle’s camouflage strategy of using ambient humidity for passive colour change inspired us to precondition outside air through dehumidification of incoming air (i.e. using hydrogels).

84 The strength of using a computational approach at the onset of the design process lies in the prospect of conducting a comparative analysis of different design components and thus better informed decision-making on the basis of the building’s expected energy performance (Loonen et al., 2014). Moreover, the biomimetic design can be hypothesized to save energy, but computational calculations provide more insight under which environmental conditions and in which geographical locations energy savings are indeed achieved. The comparative energy simulations were important to show the energy saving contribution of each design component.

The energy comparisons showed the possibility of a 66% decrease in the HVAC- related energy use intensity (EUI) or 39% of the overall EUI, primarily for cooling during hot-humid summer months. This was achieved for the natural ventilation scenario with the Bio-PCM layer (NV-PCM(31.7)), whereas other scenarios had lower energy savings.

This result shows that it was interesting to mimic both the African reed frog and the

Hercules beetle, and that their strategies complimented each other to gain additional energy savings.

85 The biomimetic envelope system using mixed-mode and natural ventilation saved 13% and 48% energy, respectively, over the baseline code compliant air- conditioned small office building. The use of an adaptive thermal comfort model by extending set-points for an expanded thermal comfort range were particularly evident in improving energy savings by the biomimetic envelope systems using natural ventilation. The integration of a Bio-PCM layer was especially useful in saving additional energy during occupied hours when outside temperature was high and the use of mechanical system was minimal. While we choose a square building based on the most prevalent building form in the U.S., Olgyay (1963) recommended a rectangular building for hot-humid climates. It is thus possible that energy savings can be further improved when building forms and shape are adapted according to climate zone (Olgyay, 1963).

Indeed, the surface area of the south façade, which has the most heat gain, can be smaller in a square building than in a rectangular building, and thus more energy savings are possible.

Although living organisms and architectural buildings are very different in many ways, there are benefits from studying organisms’ adaptation strategies, including physiological, morphological, and behavioural strategies (Badarnah, 2015). Especially when designing more responsive building envelopes, nature has shown to be one of the most prominent inspiration sources, as biological systems are inherently responsive to their environment (Loonen et al., 2013; Han et al., 2015; López et al., 2017). Biomimicry is a recently developed design methodology that assists in borrowing biological information to inspire new designs (Baumeister, 2014; Benyus, 1997). This fundamental

86 work was adapted by Badarnah and Kadri who focused on biomimicry for creating architectural designs (Badarnah and Kadri, 2014). We based our study on their proposed solution-based approach. Our study had the objective to design a feasible biomimetic building envelope, which is why we designed it to be compatible with an existing curtain wall system. Although our decision perhaps limited the innovativeness of our design, the value lays in creating a biomimetic design that is feasible and practical to implement.

We did not want to reinvent the entire building envelope, but rather explored the value of incremental improvements rather than radical innovation (Dewar and Dutton, 1986).

Similarly, we looked for building materials that can be used for architectural purposes. Current manufacturing techniques do not yet yield building materials with the same functionality as nature, and especially not at affordable prices (Gruber and

Jeronimidis, 2012; Kennedy et al., 2015). For example, while the Hercules beetle uses an intricate multi-layer photonic structure, we chose to use more cost effective hydrogels as they also reversibly and passively absorb moisture. Hydrogels have been recently suggested as a new architectural building material to improve thermoregulation (Ima

Lab, 2015), so our study encourages further development for such materials by providing additional evidence for their potential in creating energy-efficient building envelopes.

87 Each effort in applying biomimicry principles for designing innovative building envelopes identifies interesting biological strategies, provides insights in practical expectations and realizations, and contributes to building a more practical framework for facilitating the abstraction from biology into design principles. One important realization and exercise we had to go through was the abstraction level of the biological strategies, which can range from very literal to more metaphorical. To give an example, the most literal abstraction of the Hercules beetle’s camouflage strategy would be: “a hygroscopic nano-photonic material that leverages ambient humidity for adaptive colour changing.” Although this is the most accurate interpretation of the biological strategy, and thus likely to be an evolutionary beneficial strategy (Baumeister, 2014), in this case, using this abstracted design principle would have limited the applicability and feasibility of a proposed biomimetic design. While it is important to maintain biological integrity, it is important to have enough creative freedom to develop a feasible biomimetic design for a desired context. In our study, we translated the “hygroscopic nano-photonic material” simply into a hydrogel, because our desired outcome was not colour changing (which requires nanostructuring) but rather a (de)humidification function.

88 Our computational calculations show that our proposed biomimetic building envelope could result in up to 66% savings of HVAC-related EUI during summer months in Chicago. However, further empirical research is required to validate, test, and enhance the application of our biomimetic building envelope. To further improve the sustainable outcome of the biomimetic building, ideally we would also include an ecosystem-level focus. Indeed, it is best to look at different emulation levels: form, process and ecosystem (Reap et al., 2005; Baumeister, 2014; Kennedy et al., 2015).

Once a geographical location is chosen, the building should be designed to fit within the urban microclimatic and the city context and explore which ecosystem services it can provide (Bhiwapurkar, 2016; Costanza et al., 1997; Zari and Maibritt, 2017). For example, we could investigate how recuperated water and heat from preconditioning the incoming air could be used not only within the building, but also among buildings within the city. A systems approach would recognize that using high albedo surfaces and phase change materials could also influence the thermal behaviour of the surrounding buildings (Santamouris et al., 2011).

89 Conclusion

The adoption of the solution-based approach described by Badarnah and Kadri

(2014) assisted us in the development of a biomimetic building envelope that lowers energy consumption while minimizing energy needs for thermoregulation in a hot- humid climate. We used an energy simulation tool to first investigate the thermal behaviour of a building, providing us a better understanding of the design context, and to evaluate the potential energy savings of the biomimetic design. A comparative analysis indicated that the highest energy savings were obtained when the biomimetic design components of both the African reed frog and the Hercules beetle were combined. Our maximum calculated energy saving resulted in a 66% decrease in the

HVAC-related EUI (or 39% of the total energy use of the building). Importantly, this could further be enhanced when also taking into account the form and shape of the building (Olgyay, 1963).

Acknowledgements

We would like to acknowledge the valuable architectural design input by S.

Bennet and J.A. Ury, who also created figures 5.2 and 5.5. We thank M. Shawkey and P.

Niewiarowski for reviewing this manuscript and offering insightful feedback prior to submission.

90 CHAPTER VI

CONCLUSION

Biomimicry is an emergent discipline that motivates scientists, engineers, designers and business people to appreciate nature as a source of successful strategies and solutions to problems we are trying to solve. Because humans are a very young species compared to the millions of other organisms currently existing on our planet, we have not had the same amount of refinement of our solutions through the test of evolution. Currently some of our most revolutionary designs are also causing the greatest amount of pollution and are depleting earth’s finite resources. Thanks to the growing field of biomimicry there is evidence that looking at nature for inspiring new technologies, services and even entire systems like cities and organizations can result in more economical and ecological sustainable solutions (Terrapin Bright Green, 2015).

Throughout this dissertation I have explored the implications of implementing biomimicry thinking into the scientific, engineering, design and business world. Although biomimicry has great potential to result in technological and social innovations, there are still challenges that limit it from effectively being used as a design tool to solve time- sensitive, real-life problems. Moreover, only since the late 1990s a framework for biomimicry is being developed, thus more practice will lead to further improvements and realizations of this emergent discipline. By sharing my experiences, concerns,

91 challenges and research results I hope to further promote the development of biomimicry as a discipline and its application as an innovation tool that facilitates a systemic sustainability transition.

Implementing Biomimicry thinking into the scientific world asks for a very practical and applied approach. Fundamental research easily takes up several years, so for new knowledge to result in tangible biomimicry outcomes the type of research questions should be more focused to understanding how rather than why. My research started with the exploration of which eggshells all had high UV reflectivity because I thought that finding an ecological pattern would make it easier to identify commonalities and thus provide information to what contributes to UV reflection. But because eggshells have so many different characteristics it was difficult to identify the contributing characteristic. It was then that I focused on one easily distinguishable aspect: the cuticle. This speeded up the research, and enabled to identify at least one more characteristic that contributes to UV-coloration (Chapter II). A future step of this research is to further optimize the application of nano-ct to resolve smaller structural features within the crystalized part of the eggshell. Another route to possibly explain

UV-coloration, which I have not started yet, is to investigate if the biomineralization of the CaCO3 crystals contribute to UV-coloration.

We also showed that avian eggshells provide effective and durable UV protection (Chapter III). However, future research is needed to investigate if eggshells in a more industrial format (e.g. grounded particles embedded in a polymer) also provide high photo-protection. It’s important to note that turning a waste product (we create

92 tons of eggshell waste per day) into a useful product is considered bio-utilization and

not biomimicry. Not that one is necessarily better than the other, yet, making that

distinction is important for identifying when one should consider pursuing the

development of a mimic rather than using a natural product. In this case, since waste

eggshells are readily available and are causing environmental issues (i.e. eggshell waste

attracts rats to landfills), it makes sense to use it rather than a mimic.

During a next part of my PhD work I collaboratively explored how biomimicry

thinking can stimulate designers to create a biomimetic building envelope that is more

energy-efficient while optimizing thermoregulation (Chapter V). Once natural models

were chosen we had to deepen our understanding of the functional biological

strategies. The Hercules beetle has previously been used to inspire a humidity sensor

without electronics, making it easier to find relevant information. On the other hand,

the only research articles available about the aestivation mechanism used by the African

reed frog were published in the 1980-1990s. Thus, the more frequently natural models

are used for biomimetic applications, the better the biology will become available in

more practical ways. Consequently, the African reed frog was more used as bio-

inspiration, while the Hercules beetle’s strategies resulted in moderately literal

biomimicry. We consciously decided not to translate the Hercules beetle super literally,

because color changing based on nanostructures is currently not feasible for

architectural purposes. To illustrate, a super literal translation of the Hercules’s beetle

would have been using photonic nano-crystals that leverage ambient humidity for

adaptive color changing. A level bellow would be: using photonic-crystals that leverage

93 ambient humidity for another function. The abstraction level we used was: using hygroscopic materials to leverage ambient humidity for another function (i.e. thermoregulation). The strategies of the African reed frog were more freely translated: the highly reflective body based on light reflection inspired us to use a high-albedo surface; the metabolic and physiological adaptations that were trigged when its body reached a certain temperature inspired us to use an adaptive thermal comfort model and delaying heat build up, which we achieved using natural ventilation and phase change materials.

Throughout my PhD I was involved in many discussions about biomimicry: how can life’s principles be interpreted and best used, what are the implications of developing a methodological framework for biomimicry, how important is it that a biomimetic design is based on accurate biological knowledge,... This lead to the publication of one theoretical paper in which we discussed the importance to mimic nature not only on a form-level, but additionally to look at natural processes (especially manufacturing) and system-level strategies. Moreover, how can we motivate designers to create outcomes that go beyond shaping commodities for their clients and that would increase the likelihood of a design to be used in a socially beneficial way.

There are two important discussion points that I want to bring up here, because they do not belong to one specific project but they raise interesting questions on the implication for biomimicry. The first one is that inspiring biological functions are not always evolutionary beneficial adaptations. They can be the result of emergent properties, or remnants of evolutionary baggage. Natural selection is not a perfect

94 process, and some of these traits can actually be slightly disadvantageous. Take our wisdom teeth, they once were useful, but due to changes in our diet and the introduction of tools they aren’t anymore. On the contrary, wisdom teeth are considered susceptible areas for caries, infection and inflammation, which is why their prophylactic removal is a common surgical procedure (Song et al., 2000). The occurrence of UV reflection in avian eggshells might provide a relevant biological function, such as protection from sunlight, but might just be an emergent property resulting from the structural layering of calcite crystals. How do we now if a biological function is actually an evolutionary beneficial adaptation or just an emergent property or useless remnant? How does that influence biomimicry: is there still value in mimicking these biologically irrelevant strategies?

Another one is that biomimicry is based on the principle that nature optimizes rather than maximizes. However, nature’s adaptations are not always global optimizations, but can also be local optimizations because of other, usually competing, functional needs. Moreover, is it always clear what nature optimizes for (i.e. which function)? For example, we believe that the photonic nano-crystal layer of the Hercules beetle is optimized for adaptive and reversible color changing (Rassart et al., 2008), but perhaps it might be for thermoregulation. It might take up ambient humidity because it provides cooling through evaporation. In any case, it uses a hygroscopic material to leverage humidity, and it results in a visible color change. This point is for me an argument why we should not focus discussions on “is this literal biomimicry or not (i.e. is it based on accurate biological knowledge)”, but rather focus the discussion on how to

95 correctly evaluate the environmental and social impact of biomimetic designs in order to optimize their positive impact and sustainable implementation.

In conclusion, my dissertation work has exposed me to many challenges that arise when using biomimicry as an innovation tool. I believe in the value that formal education plays to facilitate the development and practical use of biomimicry by training students to be critical abstractors, translators and connectors and to develop skills necessary to design, support and lead biomimicry projects.

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106 APPENDICES

107 APPENDIX A

SUPPLEMENTAL MATERIAL FOR “THE CUTICLE MODULATES ULTRAVIOLET REFLECTANCE

OF AVIAN EGGSHELLS”

Commercial protoporphyrin IX acid (+ control)

Chicken

Brushturkey

Brown-headed cowbird (+ control)

Chicken

Brushturkey

Figure A.1. Mass spectra of chicken and brushturkey eggshell extracts are shown as example of eggs that lack a detectable amount of protoporphyrin (upper three) and biliverdin (lower three).

108 Figure A.2. Cross-sectional SEM image of one particular pigeon egg showing a structure resembling a very thin cuticle (C). Scale bar is 10 μm.

Figure A.3. Effect of 30 min EDTA treatment on the surface morphologies of chicken, brushturkey and pigeon.

109 Figure A.4. Diffuse reflectance of a thin, flat layer of pure calcite powder (Sigma Aldrich, St. Louis, MO, USA), compared to those of untreated (solid lines) and EDTA-treated (dashed lines) eggshells.

Table A.1. Summary output for linear models comparing the change in UV chroma in relation to EDTA treatment.

Species UV chromai 95 % C.I. Termii F dfs Piii Chicken 3.92e-02 ± 0.38e-02 [3.07e-04, 4.77e-04] Egg ID 3.33 2, 11 0.074 EDTA 103.66 1, 11 < 0.001 Brushturkey 1.73e-02 ± 0.22e-02 [1.27e-04, 2.19e-04] Egg ID 5.93 2, 17 0.011 EDTA 61.95 1, 17 < 0.001 Pigeon 0.71e-02 ± 0.21-02 [0.23e-04, 1.20e-04] Egg ID 5.43 2, 8 0.032 EDTA 11.62 1, 8 0.009 Budgerigar 0.62e-02 ± 0.47-02 [-0.45e-04, 1.70e-04] Egg ID 1.09 2, 8 0.380 EDTA 1.78 1, 8 0.219 iChange in UV chroma (%) per min of EDTA treatment ± SE iiEgg ID: number of egg; EDTA: time of EDTA treatment iiiP-values for EDTA were adjusted following Holm’s method

110 APPENDIX B

SUPPLEMENTARY MATERIAL FOR “EXPLORING THE USE OF UNPROCESSED

WASTE CHICKEN EGGSHELLS FOR UV-PROTECTIVE APPLICATIONS”

Table A.2. One-way ANOVA and Tukey multiple comparison tests (α = 0.05) for UV degradation of polystyrene (n=3).

Samples UV degradation1 95 % C.I. P2 Control-Brown 11.42 [8.99, 13.84] < 0.001 Quartz-Brown 2.71 [0.28, 5.13] 0.03 White-Brown 0.19 [-2.23, 2.61] 1.00 Quartz-Control -8.71 [-11.13, -6.29] < 0.001 White-Control -11.23 [-13.65, -8.80] < 0.001 White-Quartz -2.52 [-4.94, -0.09] 0.04 1 Difference in degree of UV degradation. 2 P-values were adjusted following Thukey HSD’s method.

Table A.3. One-way ANOVA and Tukey multiple comparison tests (α = 0.05) for UV degradation of nylon (n=6).

Samples UV degradation1 95 % C.I. P2 Quartz-Brown 2.75 [2.49, 3.02] < 0.001

TiO2-Brown 0.69 [0.43, 0.95] < 0.001 White-Brown 0.11 [-0.15, 0.73] 0.62

TiO2-Quartz -2.06 [-2.32, -1.80] < 0.001 White-Quartz -2.64 [-2.90, -2.38] < 0.001

White- TiO2 -0.58 [-0.84, -0.32] < 0.001 1 Difference in degree of UV degradation. 2 P-values were adjusted following Thukey HSD’s method.

111 Figure A.5. Temperature measured underneath a white and a brown chicken eggshell, and the quartz coverslips.

Figure A.6. Diffuse reflectance spectra showing no changes of optical properties of nylon after 800h UV exposure. Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error.

112 Figure A.7. Full FTIR spectra of polystyrene before and after 800h of UV exposure. Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error.

113 Figure A.8. Full FTIR spectra of nylon before and after 800h of UV exposure. Plotted lines are group mean spectra (n=6) with shaded areas representing the standard error.

Figure A.9. Optical (a) and SEM (b) images of suspension films of TiO2 particles, brown eggshell particles and white eggshell particles. Scale bars of optical images are 500 µm and SEM images are 100 µm.

114 APPENDIX C

VARIATION OF UV-COLORATION OF WHITE, IMMACULATE AVIAN EGGS

Although white, immaculate avian eggshells all have the same color to us, when their reflectance is measured using a UV-Vis spectrophotometer there are significant differences measured, especially in their UV range (below 400 nm) (figure A.10). Even though avian eggshells are approximately 96% made of calcite, their reflectance also significantly differs from that of pure calcite.

115 Figure A.10. Diffuse reflectance spectra of white-coloured eggshells from Australian brushturkey, budgerigar, ring-necked dove, King pigeon, chicken, zebra finch and flamingo and of a thin, flat layer of pure calcite powder (Sigma Aldrich, St. Louis, MO, USA). Plotted lines are group mean spectra (n=3) with shaded areas representing the standard error.

116 APPENDIX D

EXPLORATION OF CAUSAL CHARACTERSTICS OF UV-COLORATION

The color variations (figure A.10) of avian eggshells go beyond what can be explained by the differences in the presence of the two known pigments (biliverdin and protoporphyrin), but the possible contributions of structural colors or other chemical components are poorly understood. If and how crystalline patterns of CaCO3 produce structural coloration in avian eggshell is unknown. Yet, UV colors are expected to be structural, because until now no pigment has been identified to absorb light throughout the whole visible spectrum, but not in the UV. We have performed experimental modifications to the eggshells to advance our understanding in the possible proximate causes of UV-coloration.

Thermogravimetric analysis (TGA) was used to remove the organic components from the eggshells. After TGA the diffuse reflectance flattened and UV-coloration was lost (figure A.11). Grinding the eggshell with pestle and mortar also resulted in loss of

UV-coloration. This indicates the importance of structural integrity and the presence of proteins or other organic material for UV reflectivity (figure A.11).

117 Figure A.11. Thermogravimetric analysis and experimental modifications of the structure indicate the importance of structural integrity and the presence of proteins for UV reflectivity. Untreated (black) eggshell has high UV reflectivity, which is lost when organic matter is removed (TGA 100°C and 800°C, red line), and the nanostructure is destroyed (powderized, pink dotted line).

According to Chien et al (2008) the organic matrix forms a network with “variable,

region-specific organization including lamellar sheets of matrix, interconnected fine

filamentous threads, thin film-like surface coatings of proteins, granules, vesicles, and

isolated proteins residing preferentially on internal {104} crystallographic faces of

fractured eggshell calcite” (figure A.12 taken from Chien et al., 2008).

118 Figure A.12. Decalcified eggshells reveal the lamellar organization (arrows) of the organic matrix. Figure taken from Chien et al (2008).

Structural layering at the crystalized eggshell part was indeed visible with SEM

(figure A.13), however, the organic matrix is not visible. That is why we decided to further investigate the presence of nanostructures layers using nano-computed tomography (nano-ct), because it is supposed to provide a more in depth, accurate 3D visualization.

Figure A.13. Scanning electron microscopy (SEM) images show the layering of the calcium carbonate crystals of eggshells. The inset is a higher magnification of the middle part. Both scale bars are 10 µm.

119 APPENDIX E

VISUALIZATION OF LAYERING WITH NANO-CT

Although the power of X-ray computed tomography has been greatly appreciated in several fields of study, it has only recently been used to study “hidden” structures of biominerals (Li et al., 2009, 2015; Riley et al., 2014). The non-destructive character and high penetrating depth make nano-ct an ideal investigation method to retrieve high spatial information at a nano-scale resolution of structurally colored materials. We expected to see an interesting network of organic matrix (including protein sheets and air vesicles) interwoven into layers of CaCO3 crystals. The nanostructural ordering for UV colors is of a size-scale around 50-100 nm, as it has to be around 1/4th of the wavelengths of the electromagnetic waves (for UV this is 100-

400 nm).

The nano-ct scan was performed at Carnegie Melon. The scan was taken at an area from the crystalized part of the eggshell (figure A.14). The nano-ct scan took 26 hours, because the exposure time for each projection had to be 90 seconds due to high attenuation of the sample. The sample needed to be around the same size of the field of view (around 65 µm for Large Field of View (LFOV) and 16 µm for high resolution

(HRES)) but the sample preparation caused difficulties. The laser ablation used to cut the samples was able to cut through the cuticle and membrane but the inner layers

120 were resistant to all the tested laser energies (i.e. UV, Green and Infrared). That is why we first took a scan with a large field of view (LFOV) mode.

Unfortunately the nano-ct scan did not resolve any protein layering (figure A.15).

The LFOV mode should be able to resolve layers that are separated by ≥ 120 nm. To resolve layers with a smaller separation HRES mode was needed. Because the laser ablation was not able to make sample sizes small enough for HRES mode, we tried to use Focused Ion Beam (FIB) lithography. However, the large energies used in this technique caused deformation of the structures (figure A. 16). We decided to not further investigate other possibilities for sample preparation or to optimize the FIB technique. However, the initial experiments showed promising results and we believe that with more expertise, the availability of the required equipment and adequate financial resources the visualization of the organic matrix – CaCO3 layering would be possible with HRES mode nano-ct.

Figure A.14. The area that was chosen for the nano-ct scan, which is in the crystallized part of the eggshell. The eggshell cross section is seen horizontally, with the right side being the internal membrane side.

121 Figure A.15. A 3D volume rendering of the reconstructed image.

Figure A.16. Focused Ion Beam ablation resulted in melting of the structures of the eggshell due to its high energy. The left image shows a part that was melted after FIB, while the right image shows a more preserved part of the eggshell. Scalebars are 2 µm.

122 APPENDIX F

HEDGEHOG-INSPIRED HELMET LINER

In 2015 I co-founded Hedgemon, a startup focused on research and development of hedgehog-inspired impact protection technologies with initial focus on sports safety industry applications. Hedgehogs forage in trees for insects and their fastest escape from predators is to roll into a ball and fall. The impact of the fall is significant, yet they walk away uninjured. On the contrary, 1 in 10 American footballers experiences severe concussions, even when wearing high-performance helmets.

Although I’m currently no longer involved with Hedgemon, I was a part of the team during the initial startup development phase and helped designing fundamental R&D projects. I’m sharing the steps I was involved with, as it provides relevant experience for the execution of a Biomimicry-focused entrepreneurship endeavor.

The idea of using hedgehog’s intricate spine system to inspire an impact protection technology that can be used as a helmet liner resulted from a design course co-taught by an industrial design professor from the Cleveland Institute of Art and a biology professor from the University of Akron. The following semester some of us took a course in entrepreneurship, in which we developed a business plan on this idea. We were selected to partake in an NSF Innovation Corps, a program that coaches innovators through critical market and commercialization evaluations. To enable us to perform fundamental R&D we looked for financial support by pitching our idea in front of investors. We were also advised to protect our idea, and the University of Akron Research Foundation assisted us in applying for a provisional patent.

123 Besides the business-related sides of this endeavor, we also had to design and execute fundamental research experiments to gain more understanding in the spines of hedgehogs. We investigated the internal architecture of the spines using light microscopy, scanning electron microscopy (SEM), and nano-computed tomography (nano-ct).

Figure A.17. (a) Photograph of a hedgehog spine, with the bulbed end on the left that is attached to the animal (scale bar 2 mm); (b) SEM of a spine’s lateral cross-section (scale bar 100 µm); (c) nano-ct scan of a spine’s longitudinal cross-section (scale bar 100 µm). Figure taken from Swift et al. 2016.

We further analyzed the hedgehog’s spine layout: the hedgehog has about 7,000 spines and they are overlapping and interacting with each other. According to our

124 findings we 3D printed prototypes, although we had to scale up the dimensions due to limitations of current additive printing technologies at nano-scale.

The Hedgemon team, albeit without me, is continuing their investigation in the intricate spine system to support the development of a hedgehog-inspired impact absorption material. This resulted in a scientific publication, in which prototypes were used for dynamic impact tests to determine the influence of humidity, impact energy, and substrate hardness (Swift et al., 2016).

The utility patent “Impact protection and shock absorbing device” with application number PCT/US16/52760 has been filed but is not yet been published.

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