Nguyen Vienny Ug Thesis Signed.Pdf (2.436Mb)

ABSTRACT

Insect exoskeleton is an interesting and complex system that plays both structural and functional roles. It is a composite that consists of many different types of materials and shapes that vary based on its local function. This review of exoskeleton micro- and macro-structure addresses the performance of exoskeleton based on these two factors.

Exoskeleton is a composite whose material properties are dependent on its constituents and fiber orientation. At the macro-structural level, exoskeleton’s shape can play many roles in local structural and motional functions. The lessons from this review are examined and considered for potential applications in the fields of material fabrication and development and in microrobotics.

ACKNOWLEDGEMENTS

I give thanks to my family and friends for getting me to where I am today – for believing

when they shouldn’t have.

I am grateful for Dr. Lilly, my advisor, for his support and guidance.

I am thankful for David, my fiancé, for his love.

TABLE OF CONTENTS

ABSTRACT ...... i

ACKNOWLEDGEMENTS ...... ii

TABLE OF CONTENTS ...... iii

LIST OF FIGURES ...... v

LIST OF TABLES ...... vii

Section 1: Introduction ...... 1

1.1 Introduction ...... 1

1.2 Motivation ...... 1

1.3 Objectives ...... 2

Section 2: Background ...... 3

2.1 Arthropods ...... 3

2.2 Chitin ...... 6

2.3 Resilin ...... 9

2.4 The Arthropod Exoskeleton: A Composite ...... 11

Section 3: Examples in Nature ...... 16

3.1 Examples of Microstructures in Exoskeleton ...... 16

3.1.1 A Study of Material at a Beetle Neck Joint ...... 16

3.1.2 The Comparative Study of Hardened and Membrane-Like Cuticle ...... 20

3.2 Examples of Macrostructures in Exoskeleton ...... 24

3.2.1 The Folded Cuticle of a Dragonfly Neck ...... 24

3.2.2 The Macrosculpture of Fly Cuticle Armor ...... 26

iii

3.2.3 The Head Manipulation System of a Dragonfly ...... 33

Section 4: Current and Future Applications ...... 36

4.1 Recent Work ...... 36

4.1.1 Resilin Production ...... 36

4.1.2 Micro-Robots ...... 37

4.2 Potential Applications...... 39

4.2.1 The Exoskeleton Composite ...... 40

4.2.2 The Multi-functionality of Fly Cuticle ...... 40

4.2.3 The Dragonfly Attachment Methods ...... 41

Section 5: Summary ...... 42

Works Cited ...... 44

Appendix 1: Glossary ...... 47

LIST OF FIGURES

Figure 1: Arthropod Classification ...... 4

Figure 2: Three polymorphic configurations of chitin...... 9

Figure 3: A material property chart for natural materials ...... 12

Figure 4: Transition in shear modulus with change in water content of a sample of

untanned maggot ...... 13

Figure 5: Parallel and series limit models of platey or fibrous composite materials...... 14

Figure 6: SEM show chitin fiber orientation within the cuticle ...... 15

Figure 7: Diagram of the location of the gula surface in the beetle body...... 17

Figure 8: SEM images of dry gula...... 18

Figure 9: Hardness (A) and elastic modulus (B) values from indentation tests ploted

versus displacement for fresh, dry, and chemically treated samples...... 19

Figure 10: Locust in the Oviposition ...... 20

Figure 11: SEM of neck area in damselflies...... 25

Figure 12: Three orders of the neck membrane profile in adult Odanata ...... 26

Figure 13: Membraneous cuticle in Brachycera, suborder of Diptera...... 28

Figure 14: Different types of macrostructure of membraneous cuticle in various Diptera

species...... 29

Figure 15: Possible functions of macrostructure on membraneous cuticle of various

Diptera species ...... 32

Figure 16: SEM images shows the microtrichia fields on the neck and head sclerites. ... 34

Figure 17: Illustrations of corresponding frictional surfaces occuring in the dragonfly

head manipulation system...... 35

Figure 18: Bio-synthesised resilin molded into a flexible rod by drawing pro-resilin into a

glass tube...... 36

Figure 19: Stress-strain plots for a strip of synthesized resilin ...... 37

Figure 20: Examples of micro-air vehicles...... 38

Figure 21: The flexible wings designed to flex under small loads ...... 39

Figure 22: Layers of Cuticle ...... 47

LIST OF TABLES

Table 1: Summary of chitin fiber sizes ...... 8

Table 2: Elastic efficiencies of various rubber-like cuticle ...... 10

Table 3: Tensile properties of arthrodial membrane cuticle and chitin ...... 21

Table 4: Tensile properties of solid sclerite cuticle and chitin ...... 23

Table 5: Quantitative comparison of the macrostructure of the armored membranes in the

head-body joints of various Diptera species ...... 30

Table 6: Quantitative comparison of the macrostructure of the membranes in the body-leg

joints of various Diptera species...... 31

vii

Section 1: Introduction

1.1 Introduction

The purpose of this project is to perform a literature review of what has been studied regarding the material and functional properties of arthropod exoskeleton. The exoskeletons, or outer shells, play a vital role in the form and function of these creatures.

These functions include providing:

1. A protective barrier against outside forces, fluids, etc.

2. Structural support that give the creature its form

3. Functional support for muscle attachment

Because of the multi-functionality of exoskeletons, this project seeks to review their known material characteristics and properties in order to provide a foundation for the possible application of similar materials in the field of micro-robotics.

1.2 Motivation

Arthropod exoskeletons can be considered to have been optimized, through evolution, for specific tasks at very small scales. The study of exoskeleton material properties and functional structure is important for the development of biomimetic materials and devices. Insect exoskeleton, in particular, can be studied for applications in millimeter and sub-millimeter mechanisms as well as micro-air-vehicles (MAV) in which materials play an important role in the design of flexible wings and light, structural materials [1]. Finally, studying the micro- and macrostructure of insect exoskeleton can provide insight and solutions to the problems of small scale design that many researchers

are being faced with [2]. This review was performed in anticipation of a graduate research project that will focus on applying what is known about insect cuticle structure and composition to develop micro-robotic mechanisms.

1.3 Objectives

The goal of this review is to gain basic knowledge of insect exoskeleton. This

includes the compilation of information related to material properties, structures, and

mechanisms that are associated with the exoskeleton. The results of this review can be

used as a starting point for potential research and implementation in engineering.

Section 2: Background

2.1 Arthropods

An arthropod is a creature that has the following characteristics [3]:

1. Bilateral (left/right) symmetry

2. Segmented body

3. Exoskeleton

4. Jointed Legs

5. Many pairs of limbs

Examples of arthropods are crabs, spiders, millipedes, and grasshoppers. Figure 1 below shows a graphical taxonomy of arthropods.

Animalia

Arthropoda

Myriapods Crustaceans Hexapods Chelicerates Trilobites

Malacostraca Arachnida

Decapoda Insecta Araneae

Hymenoptera Hemiptera

Coleoptera Odonata

Diptera Siphonaptera Orthoptera

Figure 1: Arthropod Classification The following is a listing of the arthropods that will be discussed and their descriptions [4]:

Ant: Of the order Hymenoptera, which also includes wasps and bees, and family

Formicidae. The adults can range in size from minute to medium and have a

wide and varied morphology depending on species and caste status, which

corresponds to their function in the colony. For example, body, head, and

mandible size can vary depending on the ants’ function.

Beetle: Of the order Coleoptera, which is the largest order of insects. The adults range in

size from small to large and are heavily sclerotized, or even armored. The larvae

are typically characterized by a large, sclerotized head.

Cicada: Of the order Hemiptera. The adults range in size from small to large and have

membraneous forewings. The immature form of the cicada is a nymph that

moults its exoskeleton to emerge as the adult insect.

Dragonfly: Of the order Odonata. Adults are medium to large in size with a mobile head

and a long, slender abdomen. The immature form of the dragonfly is a nymph

that is aquatic

Flea: Of the order Siphonaptera. The adults are small, highly modified and laterally

compressed parasites. Their bodies consist of many backward-directed plates

with spiney features. The larvae are legless.

Fly: Of the order Diptera. The adults are small to medium. The larvae have unjointed

legs and a sclerotized head.

Locust: Of the order Orthoptera. The adults range in size from medium to large and are

usually winged. They can be easily charactized by large hind legs for jumping.

The immature form of the locust is a nymph that resembles a small adult.

In addition to learning about each arthropod, it is important to understand the

multifunctionality of exoskeleton. Many studies regarding different parts of different

arthropods are described in this review. The Glossary in Appendix 1 can be referenced

for anatomical terms that refer to exoskeleton features.

The next two sections address the main contents of exoskeleton individually to

provide more information and detail related to the general properties of exoskeleton.

2.2 Chitin

Chitin is a fibrous polymeric sugar and is the most commonly used tensile material in animals [5]. In exoskeleton, chitin exists as the fibrous phase within a protein matrix, whose increased content can also serve to increase the strength of the cuticle. Chitin fibers are typically the same size and length with diameters of about 2.8 nm [6] and about 0.4 µm long [7].

Table 1 below shows the results from a study that quantified the size of chitin fibers within various arthropods.

Table 1: Summary of chitin fiber sizes [6].

The extreme values of fiber diameter that were recorded from this experiment ranged from 2.3 to 3.5 nm.

Chitin has been reported to have a Young’s modulus of 150 GPa and a density of about 1.6 kg/m3 [5], though it is believed that the Young’s modulus could be significantly higher [7].

The strength of chitin can be attributed to its crystalline structure. Three polymorphic forms have been differentiated based on their structure. These are represented in Figure 2 below.

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Figure 2: Three polymorphic configurations of chitin. (A) α-chitin (B) β-chitin (C) γ-chitin [8] α-chitin is arranged in an opposing parallel configuration, β-chitin is arranged in a parallel configuration, and γ-chitin is a combination of the α- and β- chitin. α-chitin is the most abundant form found in nature and its configuration gives it a highly ordered crystalline structure with strong hydrogen bonds. These strong bonds lead to its rigidity and strength [8].

2.3 Resilin

Resilin is a rubber-like protein whose name comes from the term resilience. This is because it is considered to return the largest amount of work that is imposed on it after

the removal of the acting stress. In pure forms, it is used at the base of the legs of

jumping insects and at wing hinges for flying insects for the storage of energy [5].

The first published description of resilin provided an in depth discussion

regarding various tests that were performed on insect tendon. These tests showed that

resilin showed characteristics of perfect elasticity and that it was capable of experiencing

millions of cycles of elastic deformation. For example, the wings of a locust can deform

20 million times within its lifetime; the sound producing tymbal of a cicada can deform a

total of 400 million times in its lifetime [9]. Another test on the tendon of a dragonfly

was performed in which the tendon was deformed over the period of two weeks. At the

end of the experiment, the forces that were applied for deformation were removed and the

tendon returned to its original form. The elastic effiency of the tendon was reported to be

97% [10]. Table 2 below tabulates the efficiencies of other rubber-like cuticle that was

tested.

Table 2: Elastic efficiencies of various rubber-like cuticle [10]

The general results of mechanically tested dragonfly tendon are a Young’s modulus of about 1.96 MPa and a shear modulus of about 64 kPa and is considered to be isotropic

[9].

Water content plays a large role in the performance of resilin. The removal of water from samples of resilin cause the material to plasticize and eventually become 10 glassy and brittle. However, the reintroduction of water have returned samples to their original shape [9].

2.4 The Arthropod Exoskeleton: A Composite

Arthropod exoskeleton is a composite that consists primarily of chitin fibers in a matrix of protein – typically resilin [5] – and may also include a ceramic phase for added stiffness (7) as well as some metals such as zinc, manganese and iron [11]. With variations in the content of the material, the exoskeleton is able to meet a wide range of mechanical properties. This is best shown by Figure 3 below.

Figure 3: A material property chart for natural materials, plotting Young's Modulus against density. Guide lines identify structurally efficient materials which are light and stiff [11]. This figure shows that the Young’s modulus of cuticle ranges from about 1x10-6 GPA to about 50 GPA that represent cuticle from the soft membrane between joints and plates to stiff wings.

The main method of increasing cuticle stiffness is through a method called tanning, or sclerotization. Sclerotization is a process in which water content is decreased, resulting in the cross-linking of protein. Though sclerotization refers to a specific process, it has been shown that simply varying the water content greatly affects the

12 stiffness of exoskeleton and that some insects are able to control this voluntarily. For example, increasing the water content in a blood-sucking bug, Rhodnius, from 26% to

31% dropped the stiffness from 250 MPa to 10 MPa [7]. Figure 4 below is a plot that shows the relationship between water content and shear stiffness in un-sclerotized cuticle, with the stiffness decreasing significantly with increasing amounts of water.

Figure 4: Transition in shear modulus with change in water content of a sample of untanned maggot (Calliphora sp.) cuticle [11]. In addition to water content playing a major role in exoskeleton stiffness, chitin and protein content also play a significant role. Most soft cuticles tend to have an equal amount of chitin and protein and about 40-75% water, while stiffer cuticles have about

15-30% chitin and only 12% water [11]. Finally, exoskeleton can be locally hardened on the surface, for example: mouthparts, by the addition of up to 10% of manganese or zinc.

In addition to changing the material content of exoskeleton, its strength can also be greatly affected by the direction of its chitin fibers. For example, an area of

exoskeleton in which the forces applied are parallel to the direction of the fibers will

depend mainly on the characteristics of the fibers. Alternately, an area in which the

forces are perpendicular to or in series with the fibers will depend on the characteristics

of the protein matrix [11]. These cases are shown below in Figure 5.

Figure 5: Parallel and series limit models of platey or fibrous composite materials [11]. Outside of both of the cases mentioned above, cuticle can achieve vary degrees in strength in different directions through lamination. Unlike the lamination that is shown

in Figure 5, and that is typical of man-made composites, exoskeleton layers have a

gradual change in direction by utilizing helicoidal fiber orientations [11]. Figure 6 below

is an SEM micrograph that shows the fiber orientations in different layers.

Figure 6: SEM show chitin fiber orientation within the cuticle. (A) show a unidirectional layer while (B)shows a helicoidal transition layer [8]. The gradual change in direction of fiber orientations afforded by the helicoidal layers increases the continuity and thus the strength of the exoskeleton. It also decreases the potential for stress concentration between layers. 15

Section 3: Examples in Nature

Though it is tempting to lump material characteristics and make universal

assumptions, a study of insect exoskeleton will have more meaning if it looks at the various implementations individually. The purpose of this section is to present information on the individual studies of various arthropods and their functions. Material microstructure and composition will first be addressed followed by examples of some of the structures of exoskeleton.

3.1 Examples of Microstructures in Exoskeleton

The microstructure of the exoskeleton layers and composition have strong correlations with the local function that it performs. This section will describe the results of studies of exoskeleton that focus on the microstructure of the cuticle and the functions that are afforded by their design.

3.1.1 A Study of Material at a Beetle Neck Joint

Though it is generally well known that insects derive their physical structure from an external skeleton , it still may come as a great surprise to learn that there is typically no internal mechanism or structure at each joint. The joints of insects have adapted through evolutionary pressures to their specialized functions. This section reviews the results of a particular study on a portion of the neck joint of a beetle, Coleoptera

Scarabaeidae.

The gula, in particular, is a plate on the head which interfaces with the pro-thorax, or forward-most section of the thorax. As a result, the gula seems to have been adapted

16 to have friction reducing and wear-resistance properties. Figure 7 below shows the location of the gula with respect to the head and thorax.

Figure 7: Diagram of the location of the gula surface in the beetle body. Parasagittal (A) and frontal (B) virtual sections through the head-neck articulartion a, anterior direction; l, lateral direction; md, midline [12]. The structure of the gula was observed using a scanning electron microscope

(SEM). Some images are shown below in Figure 8.

Figure 8: SEM images of dry gula. (A, C, D) Surface of the gula. (B) Cross fracture of the gula cuticle showing the epicuticle (epi), exocuticle (exo) and endocuticle (endo). Pores (pr), dried organic substances (se) and cracks (cr) can be seen on the cuticle surface. c, d rectangles indicate parts of the sample magnified in C and D, respectively [12]. The SEM images show that the gula has a smooth surface and that the chitin fibers are oriented perpendicular to the surface in the exocuticle and parallel to the surface in the deeper layers. Finally, the images also show the existence of pores and dried substances on the surface that could have been delivered by the pores.

The mechanical properties were also tested using nano-indentation. During testing, water content was monitored in order to study the effects of dessication on

18 mechanical performance. Figure 9 below shows the results from nanoindentation on fresh, dry, and chemically treated gula specimens.

Figure 9: Hardness (A) and elastic modulus (B) values from indentation tests ploted versus displacement for fresh, dry, and chemically treated samples [12]. The results show that both hardness and Young’s modulus increases significantly between hydrated specimens and dehydrated specimens. The indentation results also show that as the indentation depth increases, both the elastic modulus and hardness decrease. This is the opposite of what would be expected of a crystalline material such as steel. This response could indicate that the the gula is characterized by a softer material

that is coated with a hard film. The hard outer surface can be considered to improve the wear resistance of the gula, and the softer inner material can provide the pliance

necessary for head articulation [12].

3.1.2 The Comparative Study of Hardened and Membrane-Like Cuticle

In addition to the harder forms of cuticle, softer, membrane-like cuticle also

perform essential functions as part of the exoskeleton. While the harder cuticles provide

rigidity, protection, and wear-resistance, the softer cuticles allow for large deformations

and stretching to accommodate motion and growth due to maturation and even abdominal

expansion during eating or reproduction. Figure 10 below is a picture of a female locust

in the position of laying eggs. Locusts are capable of laying their eggs up to 8 cm

underground in order to allow the eggs to reach water [5].

Figure 10: Locust in the Oviposition [13] A study was conducted by Hepburn and Chandler in order to identify the

differences in mechanical properties between harder cuticles and membrane-like cuticles.

The study also took an additional step to correlate the difference in properties to varying

contents of chitin and protein. Table 3 below tabulates the result from testing membrane-

20 like cuticle. Under each arthropod named are a series of angles that refer to the tensile direction where zero degrees refers to a direction longitudinal to the body (from head to tail) and ninety degrees refers to a direction transverse to the body (from side to side).

Also, some of the series also include an additional note indicating that tensile tests were performed on the cuticle after the protein was removed and only chitin remained.

Table 3: Tensile properties of arthrodial membrane cuticle and chitin [14].

The results first show that exoskeleton is not an isotropic material based on its performance when tested in different directions. The results also show a variability in its

ability to elongate, with the cuticle of the female locust, shown above as Locusta, having

the most elongation of about 2000%; while the next “stretchiest” is the cuticle found at

the joints of crabs, shown as Scylla, with elongation between 278 and 304%. Finally,

when comparing between the whole cuticle and cuticle with the protein removed, the

hardness increases in all directions and percent elongation generally decreases when

looking at the results for shrimp cuticle, shown as Panaeus.

Table 4 below shows a tabulation of results from mechanical testing of hardened

cuticle. Similar to Table 3, a series of angles are listed under each arthropod that refer to

the tensile direction where zero degrees refers to a direction longitudinal to the body

(from head to tail) and ninety degrees refers to a direction transverse to the body (from

side to side), as well as a note indicating if protein was chemically removed from the

cuticle.

Table 4: Tensile properties of solid sclerite cuticle and chitin [14].

The results show that the hardened cuticles typically have higher moduli of elasticity, relative stiffness coefficients, and much lower breaking strains. When

comparing between whole cuticle and cuticle with protein removed, both stiffness and the

modulus of elasticity increase for membranous cuticle while there is a decrease of both

properties for hardened cuticle.

From these results, it can be concluded that the mechanical properties of un-

sclerotized, membrane-like cuticle depends heavily on the chitin fibers, while the

sclerotized cuticle depends on the protein matrix. In the case of sclerotized cuticle, it is

possible that the chitin fibers play a stronger role in structural stability and fracture

resistance [14].

3.2 Examples of Macrostructures in Exoskeleton

Beyond the material content and mechanical properties of exoskeleton, its structure plays a major role in the function that it performs. In the previous section, it was shown that the strength and flexibility of cuticle could be determined by material content and microstructure. This section will describe the results of studies of exoskeleton that focus on the macrostructure of the cuticle and describe the possible functions these structures perform.

3.2.1 The Folded Cuticle of a Dragonfly Neck

The membrane that is found between hard plates and body sections in arthropods can be either highly extensible, as shown in Section 3.1, or folded and laminated to provide a lower degree of extensibility but higher degree of strength. To understand the shape and function of folding cuticle, a study was done where the neck of various species of dragonflies, Odanata, was examined. Figure 11 below shows sample images that were taken using SEM.

Figure 11: SEM of neck area in damselflies. (A) Dorsal aspect with head removed of Ischnura elegans; (B) Semi-thin cross section of the neck region of I. elegans; (C) Dorsal aspect with head removed of Coenagrion puella; (D) Semi-thin cross section of the neck region of C. puella. a, anterior direction; d, dorsal direction; m, medial direction; EC, epidermal cells; ML, midline; NM, neck membrane; PN, pronotum; SP, postcervical sclerite; TRD, dorsal trachea; TRV, ventral trachea; TS, trichoid sensilla. Scale bars: 380 nm (A & B); 75 µm (C); 86µ (D) [15]. The results of the study showed that there were several orders of folds present in the neck membrane. Figure 12 below shows a visual representation of the three orders.

Figure 12: Three orders of the neck membrane profile in adult Odanata [15]. Having this hierarchy and structure of folds allow the necks of Odanata to pitch,

roll, and yaw. This set of structures also allows the cuticle itself to be stiffer and have

higher elastic moduli because the folds allow it to deform beyond that of its smoother

counter part. In addition to these formations, the cuticle is also laminar which allow the

layers to slide over each other during motion.

3.2.2 The Macrosculpture of Fly Cuticle Armor

The exoskeleton of many insects include various types of membranous cuticle

designed to stretch between hardened plates. In order to understand the structure of this type of membrane, a study was done in order to correlate the surface structure of the membrane with function. In this study, various types of flies, Diptera, were used and two different areas were examined using SEM. The first area focuses on the head-body joint,

26 while the second focuses on the body-leg joints. Figure 13 below shows examples of the structures that were observed for each joint type.

Figure 13: Membraneous cuticle in Brachycera, suborder of Diptera. MB, flexible membrane; PT, microplates; Arrowheads indicate point of contact between microtrichia. (A) Microplates of Statriomys chamaeleon legs (B) Membrane showing curved, parallel microtrichia of Lucilia caesar legs; (C) Short papillae on the prothorax-neck membrane of Tabanus bovinus; (D) membrane of the hip-leg joint with single microtrichia of Eristalis tenax; (E) multiple microtrichia on each micro-plate joined by flexible membrane Eristalis tenax on head-trunk membrane; (F) mixture of papillae-like and elongated microtrichia on neck-head membrane of Myathropa florea; (G) parallel microtrichia on microplates of side hip joint of Eristalis tenax [16]. The macrostructure of the membranes can be generalized into the following categories: 28

- Microplates without microtrichia

- Single, short papillae-like microtrichia directly connected to membrane

- Single, elongated microtrichia directly connected to membrane

- Single, elongated microtrichia on microplates

- Microplates that containing groupings of microtrichia

These categories are shown below in Figure 14.

Figure 14: Different types of macrostructure of membraneous cuticle in various Diptera species. (A) single, short microtrichia directly connected to membrane; (B) single, elongated microtrichia directly connected to membrane; (C) single, elongated microtrichia on microplates; (D) groupings of microtrichia on microplates; (E) microplates without microtrichia [16] The results from analyzing the joints between the head and body were quantified by the number of microtrichia occuring on a microplate, microplate size, and spacing between microplates. These results are tabulated below in Table 5.

Table 5: Quantitative comparison of the macrostructure of the armored membranes in the head- body joints of various Diptera species [16].

The results from analyzing the joints between the body and legs were quantified similarly to the results from the body and head joints above. The results are tabulated below in Table 6.

Table 6: Quantitative comparison of the macrostructure of the membranes in the body-leg joints of various Diptera species [16].

From the results shown above, the membrane found in the body to head transition tends

to have only single formations of microtrichia per microplate and their lengths are

sometimes longer than the distance between the microplates. Also, the transition from

body to neck tends to have shorter microtrichia than in the transition from the neck to the

head. In the transition from the body to the legs, there is a higher number of microtrichia and their lengths tend to be longer than the distance between the microplates.

These formations are suggested to help provide structural stability of flexible membranes as well as vary the frictional forces in contact areas. Depending on the direction of deformation and shape of the macrostructures, these can increase the frictional forces, providing stability of motion. Examples of the functions these frictional forces are shown below in Figure 15.

Figure 15: Possible functions of macrostructure on membraneous cuticle of various Diptera species. (A-D) Fixation function; (E-F) String function; (G) Folding function [16]. These functions are grouped into three categories. The first is fixation in which the microtrichia are longer than the spacings between microplates and can interact in order to provide holding stability. The second is the string function where the microtrichia are angled parallel to the surface of the cuticle in order to provide another degree of resilience to deformations in the membrane. The final function is folding in which pattern of the microtrichia provide a specific direction for the membrane to fold.

It is suggested that microtrichia exists to perform at least two of these functions in a particular area [16].

3.2.3 The Head Manipulation System of a Dragonfly

An example of a system that utilizes the two macrostructures described in the previous section is the head manipulation system of a dragonfly, Odanata. Like many insects, dragonflies have wide ranges of motion that are afforded by the structural design of the cuticle and a system of muscles and tendons. In particular, and study by Stanislav

Gorb reported that the head manipulation system of the dragonfly consists of three parts:

- Abductor muscles that allow the head to manipulated away from its normal

position, and adductor tendons that act as tension springs to passively pull the

head into the normal position when the abductor muscles are relaxed.

- Neck membrane that consists of folds that allow flexibility and locally

increase the strength of the cuticle (please see Section 3.2.1).

- Sclerites on the neck, thorax-side, that interface with the neck membrane and

contain fields of specialized microtrichia.

The interaction between the neck membrane and the fields of microtrichia play

the role of the fixation function that was discussed in Section 3.2.2. Figure 16

below shows SEM images of these fields.

Figure 16: SEM images shows the microtrichia fields on the neck and head sclerites. (A) A sclerite from Anisoptera, Libellulidae. (B) A field of microtrichia on the head. (C) An enlarged view of the box C in image A. (D) An enlarged view of the box D in image A. (E) An enlarged view of the field in image B [17]. The sets of interfacing fields can be categorized into four sets of correlating microtrichia types. These are represented in Figure 17 below.

Figure 17: Illustrations of corresponding frictional surfaces occuring in the dragonfly head manipulation system. (A) Hook-like or cone-shaped and mushroom-like microtrichia. (B) Hook-like or cone-shaped and thin seta-like microtrichia. (C) Mushroom-like microtrichia on both sides. (D) Smooth, compressed microtrichia on both sides [17]. These sets are:

- Hook-like or cone-shaped and mushroom-like microtrichia - Hook-like or cone-shaped and thin seta-like microtrichia - Mushroom-like microtrichia on both sides - Smooth, compressed surface microtrichia on both sides

The study concluded that purpose of having multiple types of interfaces allows the surface area of the microtrichia fields to remain approximately the same size. As a result, the attachment stability of the head in various positions is afforded by the different interface types rather than by area of contact.

Section 4: Current and Future Applications

4.1 Recent Work

More researchers are looking to insects as a source of inspiration. Biomimicry as a design virtue has become prevalent in the fields of materials and engineering in particular. This section will briefly describe examples from both of these fields and their relation to insect exoskeleton.

4.1.1 Resilin Production

Based on the behaviors of pure resilin that have been identified as energy storage devices in arthropods, many researchers have worked to learn more about this material as well as devise methods of producing resilin in higher quantities. Some progress has been made such that it may be cast into rod-like shapes, shown below Figure 18, and mechanically tested for performance.

Figure 18: Bio-synthesised resilin molded into a flexible rod by drawing pro-resilin into a glass tube. Left, the rod illuminated by white light. Right, the same rod illuminated by UV light at 315 nm showing its florescence at 409 nm [18]. The results of the mechanical testing showed that the experimental stress-strain curve of the systhesized resilin deviated from the theoretical curve at 20% strain as opposed to

50% in another study of insect resilin. Figure 19 below shows the stress strain curves

that were obtained through experimentation.

Figure 19: Stress-strain plots for a strip of synthesized resilin. The pink curve shows the cycling of 225% strain with a resilience of 97%. The blue curve shows the testing to failure with an extension of 313% at break. The green curve shows the theoretical curve [19]. Based on the pink curve that is shown above, the bio-synthesized resilin has a resilience

of 97% when cycled to 225% strain [19]. This characteristic holds many possibilities for

resilin as a future biological implant material, micro-actuators, and nanosprings [18].

4.1.2 Micro-Robots

When addressing the issue of micro-robotic design, insects can be seen as the

example to learn from and follow. The adaptations of their exoskeleton material,

structure, and mechanisms have been optimized for performance on a micro-scale and

many designers are looking towards insects for study and inspiration.

The field of flying micro-robots faces many challenges with respect to balancing weight, strength, and resilience, let alone energy storage and actuation [20]. Some

examples of some micro-air vehicles (MAV) are shown below in Figure 20.

Figure 20: Examples of micro-air vehicles. (A) Aerovironment’s Black Widow, 56 g. (B) David Liu’s triplane, 10 g. (C) Martin Newell’s Shark, 0.495 g [20]. In the development of MAV’s, particularly their wings, designers have begun to mimic the structure and material found in insect wings. An example of a wing design of an

MAV that was inspired by the structure and material of insect wings is shown below in

Figure 21.

Figure 21: The flexible wings designed to flex under small loads [21]. In the design of the wings shown above, carbon fiber tape is layered onto a carbon fiber

frame. The carbon fiber frame is constructed using tape layers which are increased in

areas in which high strength is required. After the frame is constructed, a sheet of latex

rubber is applied in order to provide flexibility. This method of construction is analogous

to layers that are found in insect cuticle as well as the cuticle formations that provide

increased strength and stability in specific areas.

4.2 Potential Applications

Based on the results of the studies that were reviewed many lessons can be

learned for the application of new material processes and products. Material properties of

composites can be modified locally through composition and fiber orientation. Gradual changes in fiber orientation, rather than abrupt laminations can better distribute stresses

and increase the structural strength. Finally, material properties can be modified locally

through the use of microsculptures that can be designed to perform specific functions.

This section presents potential applications in which these ideas can be implemented.

4.2.1 The Exoskeleton Composite

Insect cuticle provides insight into many improvements that can be made towards

to fabrication of composites. For example, the use of transition layers between changes in fiber direction with the use of helicoidal patterns would help to strengthen material.

This could also help to distribute stress through the material in a continuous manner. The process would require the control of fiber orientation within a matrix that selectively bonds to the fibers as well as to itself. Controlling the fiber direction would also lend itself to the local customization of material properties. Being able to do so would allow for the control of wear resistance, material resilience, and crack propagation.

Finally, the concept of changing the matrix properties simply through the removal or addition of water presents an interesting possibility. The development of a material in which water could be easily added or removed would provide many new opportunities

for products that are “self-adaptive” to its environment or local function. A very specific example would be a material that could be used in the wetsuits used by Navy Seals.

While submerged in water, the material would be pliant to provide for appropriate

dexterity while moving within the water. Once out of the water, the material would harden and act as protective armor on the suit.

4.2.2 The Multi-functionality of Fly Cuticle

The passive functions of the macrostructures found in fly cuticle could provide

inspiration for new fabrics or other flexible material. These materials could take

advantage of microsculptures to either temporarily hold positions or preferentially fold

and snap back into position. This can have applications in robotics for the design of multi-jointed, flexible manipulators. Specifically, manipulators used in surgery strive for

more organic control and a minimally invasive device. Future manipulator designs can

integrate the use of external or internal microstructures to provide motion stability and

decrease device size. The passive control afforded by the microsculptures would reduce the number of actuators and internal components required for a manipulator.

4.2.3 The Dragonfly Attachment Methods

The devices that are used in the head manipulation system of the dragonfly presents interesting design constraints and methods. Instead of having two full sets of muscles for abduction and adduction, the system is simplified by using a passive set of elastic tendons that act as tension springs for the adduction motions. So, the active abduction muscles work with the passive attachment devices formed by the microsculptures on the cuticle. This design method can be implemented in many mechanisms in which there is a normal position to which it always returns. It can help decrease complexity or even reduce the amount of energy that is used during operation.

In addition to the overall system design, the various attachment devices formed by the microsculptures on the cuticle could be used to improve many products. For example, repositionable tapes that don’t use an adhesive coating can be designed to adhere to specific surfaces and used on bicycle handle-bar grips, tennis racket-grips, tool grips, etc.

Gloves and shoes that use microsculptured surfaces can improve grip for climbers.

Section 5: Summary

This review focused on the mechanical performance of insect exoskeleton based

on microstructure and macrostructure properties. The exoskeleton material is a

composite that consists of a soft protein matrix, typically resilin, and harder fiber

reinforcements such as chitin. First, examples of material microstructure were presented.

Based on the studies reviewed, a wide range of mechanical performance can be achieved

by varying the material content. It was found that water plays an important role in the

strength of exoskeleton material and that membrane-like materials derive their strength

from chitin fibers, while harder, sclerotized materials depend more on the protein

structure. This suggested that chitin plays a greater role in the structural stability and

fracture resistance of harder exoskeletons. In addition to the material content, mechanical

performance is also dependent on the fiber orientations of chitin. When applied forces

act in parallel to laminations or fiber orientations, the material performance is dominated

by the strength of the stiffer laminations or fibers. Finally, when applied forces act in

series with laminations or fiber orientations, the performance is dominated by the softer

laminations or matrix.

The effects of macrostructure of exoskeleton was also presented and showed that

there are many types of microscupltures on the surfaces of exoskeleton that can perform

multiple functions. At the joints, in particular, there are three main functions that the microsculptures can perform: fixation, string, and folding. These functions are passive and can be integrated into a motion system in order to decrease size and complexity.

Based on these studies, multiple fields could benefit from the examples found in nature. Improvements in material fabrication and design can help to improve both structural and motional performance of materials. The integration of adaptive, passive funtion materials into the field of micro-robotics can decrease size and the complexity of internal components. Finally, using insect exoskeleton as an example for systems and material design can provide a stepping stone towards the development of new-age devices that are better optimized for size, weight, and function.

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Appendix 1: Glossary

The following listing of terms are used to describe the exoskeleton and its features

(4)(5):

Abdomen: The third, tail-end section of insects.

Arthrodial Membrane: Soft, stretchable cuticle found in larvae and between segments.

Cuticle: The external skeletal structure, secreted by the epidermis, composed of chitin

and protein. The cuticle consists of several layers: the epicuticle, exocuticle, and

endocuticle.

Figure 22: Layers of Cuticle (22) Dessication:The process of removing water.

Epidermis: The unicellular layer of extodermally derived integument that secretes the

cuticle.

Gula:A sclerotized plate on the head of insects that interfaces with the body (12).

Larva: An immature insect after emerging from the egg.

Mandible: The jaws that can be jaw-like in shape for biting and chewing, or as stylets for

piercing and sucking.

Microplate:A small hardened plate found on insect cuticle, typically on membranous

cuticle [23].

Microtrichia: Subcellular cuticular hairs with several to many extensions per cell.

Sclerite: A plate on the body wall surrounded by membrane [4].

Sclerotization: Stiffening of the cuticle by cross linkage of proteins. An irreversible

process that visibly darkens the exocuticle.

Thorax: The mid-section of insects.