The importance of biological materials has long been recognized from the molecular level to higher levels of organization. Whereas, in traditional engineering, hardness and stiffness are considered desirable properties in a material, biology makes considerable and advantageous use of softer, more pliable resources. The development, structure and mechanics of these materials are well documented and will not be covered here. The purpose of this paper is, however, to demonstrate the importance of such materials and, in particular, the functional structures they form. Using only a few simple building blocks, nature is able to develop a plethora of diverse materials, each with a very different set of mechanical properties and from which a seemingly impossibly large number of assorted structures are formed. There is little doubt that this is made possible by the fact that the majority of biological ‘materials’ or ‘structures’ are based on fibres and that these fibres provide opportunities for functional hierarchies. We show how these structures have inspired a new generation of innovative technologies in the science and engineering community. Particular attention is given to the use of insects as models for biomimetically inspired innovations.
It is important to understand the difference between a material and a structure. A material is homogeneous, right down to the atomic level. A structure, on the other hand, is inhomogeneous and may even be anisotropic. The mechanical properties of a structure depend as much on the shape of the structure as on the properties of the material(s) from which it is made (Vincent 1992). Wood, muscle and cuticle are all natural examples of how simple materials, proteins and polysaccharides are formed in a hierarchical manner to create higher organization structures with added functionality (Jeronimidis 1980; Vincent & Wegst 2004).
Nature makes good use of shape. Many biomimetic designs such as Velcro, lotus-effect surfaces and sharkskin-inspired riblets owe their success simply to the clever morphology and scale of biological materials (Dickinson 1999). However, in a biomimetic context, there is no benefit simply in copying nature's designs since we would gain nothing more than limited versions of the biological counterparts; an artificial wood, for example, is unlikely to be as cost-effective as real wood. Bio-inspiration should aim at extracting nature's good designs and implementing them in a way that adds value and functionality to our mechanical designs.
Although there are not always natural analogies to our design and engineering solutions, the vast range of materials and structures that are available in nature provides us with a seemingly limitless source of inspiration. Insects are, evolutionarily very old and make up around three-quarters of all animal species. As well as demonstrating their evolutionary prowess, often inhabiting environmental extremes, they provide us with a vast catalogue of natural examples from which to study and learn. We present a number of such examples of how clever morphology plays a significant role in insect behaviour and, in particular, in mechanosensory systems, flight and sight.
2. Mechanosensory systems
Animals, vertebrates and invertebrates alike live in often complex environments about which they must obtain qualitative and quantitative information in order to apply the behaviours necessary for survival and reproduction. The possession of multiple sensors increases stimulus detection probability and sensitivity, permits compensation for localized damage and enables the formation of specialized central processing centres. Sensor diversity enhances stimulus discrimination (Derby & Steullet 2001). Sensors and sensing systems are, therefore, essential components to the existence of life. Plants and animals have developed and devised a plethora of sensory systems that capture information from their physical and chemical environment, ultimately ensuring their survival through communication, orientation and locomotion, adaptation, defence against predators and the capture of prey.
The sensory systems of insects are simple in their design, efficient in their function and robust in many an environment. They are also remarkably sensitive, making them ideal paradigms for engineering and design applications. Proper sensing function occurs on a cellular level but hierarchical organization of the materials and structures provides additional functionality such as the amplification and filtering of incoming signals. Filiform and campaniform sensilla are two such examples, providing airflow and strain sensing, respectively.
(a) Airflow sensing
Crickets and other insects are able to detect the approach of predators with the use of highly sensitive mechanoreceptive sensory hairs. These filiform, or ‘thread-like’, hairs respond to faint air currents, low-frequency sound and medium vibration (Keil 1997). Filiform hairs are, in particular, abundant in crickets, located at the rear of the abdomen on appendices known as cerci. Filiform mechanosensors vary greatly in length and number in relation to ontogeny (Dangles et al. 2006) and phylogeny. The reasons for this variation in length and number are plentiful, but the primary advantage of having multi-sensor arrays is that they are better suited to the extraction of meaning from noise than single sensors, something the cricket is particularly adept at.
Filiform sensilla are shaped as extremely elongated paraboloids where the diameter of the hairs varies with the square root of the distance from the tip of the hair, a square-root cone (Kumagai et al. 1998). Each hair is housed within a socket and secured at the base by a flexible membrane. The morphology of the hair and its associated features are such that each hair has a preferential plane of oscillation. This is characterized by an elliptically shaped hair base that fits neatly into an elliptical hole at the base of the socket (figure 1). The distribution of this preferred directionality according to hair socket orientation can be divided into two main subclasses and mapped according to their location on the cercus (Palka et al. 1977).
A filiform mechanosensor behaves as an inverted pendulum with the hair acting as a rigid shaft anchored to a spring. The system is very highly damped with hair resonance frequencies in the range of 85–500 Hz. Owing to the low Reynolds number of the airflow around the cercus, the hairs are affected by significant boundary-layer effects and are deflected by drag forces acting on the hair shaft. Their high moment of inertia makes them irresponsive to high frequency air motion (Shimozawa et al. 1998).
The mechanics of single mechanosensors, as well as the neurophysiological aspects of the sensory system, have been studied extensively through both experimental and analytical modelling. Analysis of the canopy response of the cercal mechanosensor array, however, is less comprehensive. Modelling of a hair-based mechanosensor array has revealed viscous-mediated coupling effects to be non-negligible in crickets (Cummins et al. 2007) and spiders (Barthellier et al. 2005). This implies that, although the study of single hair mechanics is warranted in its own right, it cannot tell us the whole story.
Using a high-speed video camera capable of recording at up to 650 000 frames s−1, the authors have observed the response of the cricket cercal hair canopy to an oscillatory input. Figure 2 is a single image captured from the high-speed camera, showing the hair canopy of a single adult cercus. Two hairs of different lengths are highlighted.
At 60 Hz (identified as the cercal best frequency for the hair canopy; Magal et al. 2006), evidence of a wave effect as a result of the energy supplied by the source was observed as the stimulus induced by the oscillation travelled down the length of the cercus.
The angular amplitude of individual hairs in relation to their length and their distance from the oscillatory source was also measured (figure 3).
Where one might have expected the shorter hairs to move at lower amplitudes owing to the increased inertia required for their movement, this is not observed here. The shorter hairs are located primarily at the cercus tip, closest to the source, so receive the highest amount of energy available. The response of the filiform hairs is, therefore, likely to be affected by both hair length and source attenuation. Using the same technique, evidence of possible viscous coupling in filiform hairs has also been observed. Scanning laser vibrometry has also been used to measure hair response to an oscillatory flow and of significant note is that, regardless of length and distance from the source, filiform hairs move at the same frequency as the input stimulus, although phase differences have been observed.
Significant interest has developed in the mechanosensory system of crickets due to their extreme sensitivity, with filiform hairs responding to air velocities as low as 0.03 mm s−1 (Shimozawa et al. 2003). This astounding level of sensitivity is bordering the thermal noise range, implying that these mechanosensors can detect changes due to Brownian motion. Owing partly to this level of sensitivity, the flow-sensitive hairs found on the cerci of crickets have inspired the development of MEMS-fabricated flow sensors (Humphrey et al. 2003). Dijkstra et al. (2005) developed arrays of long SU-8-based structures mounted atop suspended membranes with capacitance readouts. The hairs were capable of normal translational and rotational degrees of freedom and demonstrated a level of preferred directionality. A need to increase the sensitivity of the array was identified and, subsequently, Krijnen et al. (2006) showed that, by using DC biasing, the effective spring stiffness of the structures could be lowered, hence permitting adaptation of the resonant frequency and sensitivity of the hairs. It was also suggested that, by lengthening the artificial hairs, they could be brought out of the boundary layer permitting higher torques.
With the progress currently being made in fabrication techniques, microelectromechanical systems are paving the way to the development of small, lightweight, highly sensitive array devices, providing solutions to the rapid advancement of technology towards smart, adaptive intelligent and integrated systems.
(b) Strain sensing
Campaniform sensilla are singly innervated proprioreceptors, unique to insects, which respond to strains in the arthropod exoskeleton (Pringle 1938). The term ‘sensilla campaniformia’, meaning bell-shaped, was first adopted by Berlese in 1909. The sensilla are homologous to filiform hair sensilla, corresponding in structure and origin but providing an entirely different function (McIver 1975).
Campaniform sensilla are generally constructed of a ‘cap and collar’ arrangement, a small oval-shaped cuticular dome surrounded by a ring of raised cuticle (Grünert & Gnatzy 1987). The cap contains a pore, the ecdysial canal, at its centre, which extends through the cuticle and undergoes a shape change in response to loading. The cap acts to rotate the displacement mechanism through 90°, converting in-plane movement of the cuticle into out-of-plane motion detected by a single cell. The oval shape of a campaniform sensillum means that it can be deformed more readily in one direction than the other, providing a level of directional sensitivity to the strain. The length of the long axis typically ranges from 5 to 25 μm. Variations in sensillum size and morphology are common according to the specific characteristics of the stimulus perceived at the sensillum location (McIver 1985).
While campaniform sensilla are located widely over the bodies of insects, they are particularly concentrated in regions of the exoskeleton where deformations of the cuticle are likely to occur, for example at the base of wings (Gnatzy et al. 1987), the halteres of flies (Fraenkel & Pringle 1938) and on the leg joints of locusts (Newland & Emptage 1996) and cockroaches (Moran et al. 1971; Chapman et al. 1973; Seelinger & Tobin 1981). As well as the location of these sensilla being of utmost importance, their arrangement plays a significant part of their functionality. Campaniform sensilla can occur as single entities, grouped in small numbers or arranged in fields (Gnatzy et al. 1987). They are at their highest organization at the base of the halteres in flies where the deformation is measured in a graded manner (Keil 1997). Previously thought to exist only in adult insects, the authors have observed campaniform sensilla in cricket hatchlings (figure 1).
Biomimetic strain sensors, based on the morphology and mechanics of the campaniform sensilla of Calliphora vicina, were suggested by Skordos et al. (2002), who modelled a hole in a fibrous composite plate. Vincent et al. (2007) applied this concept by considering the use of integrated strain sensors for a range of space-related applications such as health monitoring of spacecraft and as feedback devices in active control systems. A wide variety of methods for measuring deformation in structures are employed by the space industry. Vincent et al. (2007) discuss the advantages and disadvantages of some of these methods, concluding that these existing systems do not take advantage of the signal amplifications induced by mechanical modification of the structure. The model presents the use of holes as an integral part of the structure, allowing the holes to interact with the structure and feed back information about its condition.
In traditional engineering, the presence of holes in a material is usually considered a disadvantage to the strength and integrity of a structure as the holes behave as stress concentrators and crack initiators. If applied correctly, however, the presence of such holes can be used to amplify mechanical deformation in the material and convert this deformation into an electrical signal. The micro-holes formed in nature have been used to demonstrate the measurement of strain amplification, even in a stiff material. The holes present in campaniform sensilla, for example, serve to increase the compliance of the dome-shaped cap structure and, in fact, form an essential mechanistic component of the sensor without diminishing the integrity of the material. The key to the success of a hole is the arrangement of the material surrounding it. In biology, chitin, the fibrous component of the cuticle, is arranged around the hole in such a way that it carries the loads around it (Vincent & Wegst 2004). Two- and three-dimensional finite-element modelling was used by Skordos et al. (2002) to measure the strain energy density associated with different hole and fibre configurations and to subsequently assess the expected strength reduction effect of the holes. Oval holes drilled into a sheet of uniaxially orientated fibres interrupt the line of the fibres creating high stress concentrations on either side of the hole, orthogonally to the direction of the strain. A formed hole, with the fibres oriented round the hole, carried the strain much more evenly with smaller stress concentrations found in line to the applied strain. Additionally, it was hypothesized that the elastic properties of the campaniform sensillum collar can be modified by changing the thickness of the tanned cuticle of which it is constituted (Skordos et al. 2002). This idea can also be applied to engineered holes as the sensitivity of a hole-based strain sensor can be altered by adjusting the properties of the surrounding material.
(c) Sensillum coupling
In many insects, for example crickets, cockroaches and mosquitoes, campaniform and hair sensilla are often closely associated as a functional unit. On the legs of cockroaches, a single campaniform sensillum can be found in the wall of the tactile spine at the junction with the articular membrane. Although the spine is not innervated, the sensillum is stimulated by movement of the hair (Chapman 1965). In crickets, campaniform sensilla are found in close proximity to the filiform hair sensilla of the cerci (figure 1; Edwards & Palka 1974). The role of these campaniform sensilla is still unclear, although functional coupling between the campaniform and hair sensilla is becoming more apparent (Dumpert & Gnatzy 1977; Heusslein & Gnazty 1987).
3. Insect flight and sight
Motivated largely by the need for aerial reconnaissance robots inside buildings and confined spaces, MEMS technology is also being used in the development of wings for use in micro-air vehicles (MAVs; Pornsin-sirirak et al. 2001). By definition, in accordance with the Defence Advanced Research Projects Agency (DARPA), a MAV must have a wingspan of not more than 15 cm and must be capable of staying aloft for 20–60 min while carrying a payload of 20 g or less to a distance of 10 km (McMichael & Francis 1997). These constraints are driven largely by the physical conditions experienced by a vehicle of this size. MAVs must be small and agile and, at the scales proposed, operate at the same Reynolds numbers as for large insects (100–10 000). Additionally, fixed wing flight is not as suitable at these Reynolds numbers and flapping is, by far, the most advantageous mechanism for enabling the insect to generate enough lift to overcome its own weight. Insects, therefore, make ideal models for MAV design. Insect wings are described as ‘elegant essays in small-scale engineering. They are deformable aerofoils whose shape is actively controlled by the wing base articulation while the wing area is subject to inertial, elastic and aerodynamic forces’ (Ellington 1999). Norberg (2002) reviewed the structure and function of natural flight in relation to MAV development and, in particular, highlighted the importance of morphology in flight kinematics.
Since DARPA published its requirements for MAVs, a considerable amount of research has been undertaken, by many a research group, into the development of MAVs, which can now exist at under 1 g in mass (Karpelson et al. 2008). Although considerable research continues in this area, the focus of this research has now turned to the development of flexible and foldable wings based on those of the bat (Bunget & Seelecke 2008).
As relatively simple creatures, insects make particularly useful models for the study of sensory systems as their neuronal connections are considerably fewer in number than those of higher animals. Neural processing of the visual environment, for example, typically occurs using approximately 1 million neurons, approximately 40 000 times less than a human eye. Despite a relatively poor spatial resolution, insects possess an impressively high temporal resolution. The fly retina can follow the flickering of a monitor at up to 133 flashes s−1 and that of a bee can resolve over 200 flashes s−1. The locust has a slower temporal resolution of 60 flashes s−1 but is still capable of avoiding collisions with objects by extracting information in relation to depth of motion. This has inspired the development of robot collision detectors, with success rates of 91 per cent at velocities of 2.5 cm s−1 (Rind et al. 2003).
A thorough understanding of insect vision and other sensory motor abilities has provided an abundant source of knowledge and considerable development in the field of self-guided vehicles and robots. The multifaceted compound eye of flying insects has inspired many an engineering application, from the very large, such as the biomes at the Eden Project, UK, to the very small. The eye of the microscopic fly Xenos peckii, for example, became the ideal candidate for the development of a revolutionary new optical imaging system for the defence and aerospace industry (Laycock & Handerek 2007). The multi-lens camera can provide missile tracking systems with a very wide field of view while being much smaller and lighter than existing systems. Flies are also inspiring a generation of fly-by-sight micro-robots (Franceschini et al. 2007). Using an array of elementary motion detectors, visually guided terrestrial and aerial robots have been developed (Franceschini 2003), which can successfully avoid obstacles while moving at relatively high velocities (50 cm s−1 in the terrestrial robot and 1–3 m s−1 in the flying model). Flight and sight capabilities are also being combined in the development of biomimetic insects weighing less than 100 g (Deng et al. 2006).
4. The future of biomimetic innovation and sensors
Biomimetic principles are being used as a source of innovation across a broad range of industries. The contributions of biomimetics are found not only in technology but also in the social sciences (Wahl 2006) and business (Richardson 2007). Biomimetics continues, however, to primarily instigate technological innovation (Vincent & Mann 2002; Lu 2004) and a useful measure of such advancements is through the number of patent publications. Bonser (2006) reported a sixfold increase in the number of biologically inspired patented technologies, identified by searches of the US Patent and Trademark Office datasets, over a 20-year period (1985–2005). By applying a logistic regression analysis of these data, a sigmoid model of patent growth was generated and implied that we are currently half way through an innovation cycle with a peak of patents expected around the year 2015. Subsequent exploration of patenting activity in China indicates similar trends (Bonser & Vincent 2007) and also sustained growth in membership of networks promoting biomimetics as a source of innovation for industry. Clearly, interest in biomimetics, as a path to innovation, is growing rapidly and sensing is one area with immense potential for future growth.
In this review, we have described recent advances in biomimetic sensing technologies. Such technologies, when mature, will have the potential to impact on diverse areas of business and industry. Obvious application areas include autonomous vehicles, aerospace, security, defence and biomedicine. There are intriguing opportunities for other industries, for example sensing in ‘intelligent buildings’ and embedded sensors in composite structures for condition monitoring.
There are several advantages to the use of arthropods as models for new biomimetic sensors. First, given their high levels of redundancy, their sensory systems are very robust. An example of this, as shown in this review, is that of the multifaceted compound eye where functional loss of a single facet does little to impair the performance of the whole organ. Second, arthropods are hugely successful, so their sensor ‘technology’ has been tried and tested over many millions of years. They have also successfully colonized a vast range of habitats, requiring robust and adaptable sensory functions. Finally, many sensory systems are embedded within the cuticle, making them ideal candidates for incorporation in composite materials, for example. Although in its infancy, the use of arthropods as models for biomimetic sensors is showing much promise. The key challenge now is to successfully transfer these mechanisms into engineered technologies for a wide range of industries.
One contribution of 9 to a Theme Issue ‘Biomimetics I: functional biosurfaces’.
- © 2009 The Royal Society