Wednesday, December 01, 2010

Not slippery when wet

Ever wondered how a fly effortlessly lands and runs on your window without falling off? Judging by the natural curiosity of most Physics World readers, it is probably the sort of thing you thought about when you first started exploring the world around you as a child. However, as you might have noticed back then if you tried to get a better look, it is really hard to see those little insect feet in action without any form of magnification.

As the childlike curiosity of scientists never ends, it is somehow no big surprise that this apparently simple question – of how a fly sticks to a surface instead of just sliding off – was addressed in the 17th century by some of the pioneers of optical microscopy, including Robert Hooke. Better optical lenses suddenly allowed researchers to explore the world beyond the resolution of their eyes for the very first time.

Even back then, scientists knew that there is more to insects than meets the eye. While the most basic system of mechanical interlocking found in arthropods is the claw, insects do not merely have a miniature version of this. Many surfaces in the natural world are simply not soft enough to allow claws to be inserted, or are too smooth to provide a safe grip. The question of how insects stick, crawl and run on vertical surfaces and even upside down remains as hotly debated between scientists now as it was in the 17th century.

One of the first books on microscopy was Experimental Philosophy, written by Henry Power in 1664. Along with detailed observations of various organisms, Power described and discussed the adhesive organs of the fly. He suggested that the fly's feet can hold the creature upside down using a "whitish viscous liquor" secreted via tiny sponges on its feet.

However, just one year later, Hooke (best known to physicists for his eponymous law of elasticity) sparked a heated debate by challenging Power's wet-adhesion theory. In his respected book Micrographia, Hooke speculated that on the length scale of a fly's foot, surfaces are rough enough that the feet can interlock and adhere using fine hairs (figure 1): "without the access or need of any such Sponges fill'd with an imaginary gluten, as many have, for want of good Glasses, perhaps, or a troublesome and diligent examination, suppos'd".

After this rather personal dispute, many researchers proposed and tested the mechanisms of insect adhesion over the subsequent 200 years. Even Jonathan Swift, the passionate Irish natural scientist, mentions how insects stick in his well-known 1726 novel Gulliver's Travels. Gulliver, exploring a land of giants during his second journey, is attacked by wasps one morning and complains that "these odious insects would sometimes alight upon my victuals, and leave their loathsome excrement, or spawn behind...which, our naturalists tell us, enables those creatures to walk with their feet upwards upon a ceiling".

By the mid-19th century, most scientists had written off insect adhesion as fully understood, as Power's theory of glue-based adhesion had been mostly accepted within the scientific community. Yet confusingly, in 1832 a different idea was introduced that, despite being proven wrong the following year, is still among the most popular "cocktail party" explanations. The idea came from German zoologist Herman Burmeister, who postulated that insects stick using "muscular suction cups". To check this theory, in 1833 the British naturalist John Blackwall placed insects in sealed cylinders, out of which he then pumped the air. He found that the insects' ability to adhere to the smooth inner surface was unaffected by the air pressure, and so dismissed Burmeister's theory. However, despite the evidence, many scientists continued to pursue the suction-cup idea, and only a few investigated fluid adhesion in the years that followed.

Meanwhile, in further studies Blackwall noticed that placing small quantities of water vapour, oil, wheat, pulverized chalk or gypsum onto clean glass surfaces prevented insects and spiders from sticking to them. "These facts, far from corroborating the mechanical theory," he concluded, "appeared quite inexplicable, except on the supposition that an adhesive secretion is emitted by the instruments employed in climbing."

After this flurry of activity in the early to mid-1800s, scientists soon turned their attention and their microscopes towards other wonders of nature's micro-cosmos, and insect adhesion became a largely forgotten quest – a backwater in the broader sweep of science.

Fast-forward to the present day, however, and the study of insects has come back into fashion. Elaborate instruments such as the scanning electron microscope and the atomic force microscope have allowed us to glimpse a new realm – the nano-cosmos. Scientists can now unmask even more of nature's mysteries, and engineers have realized that taking inspiration from the natural world can be a neat route to developing innovative products. For example, the adhesive organs of insects, spiders and geckos are better than many artificial adhesives, at least in terms of their versatility (see "Stewed and digested"), and the fact that they are reusable and work in dynamic situations.

During their lifetime insects need to attach and detach their feet many millions of times. Each of these steps risks damaging or contaminating the insect's feet, which would reduce their ability to stick. (Ever tried to reuse a Post-it note?) Insects get around this problem by using self-cleaning mechanisms, which rid the feet of any dirt to allow optimal stickiness, regardless of the number of steps taken. Such mechanisms have also been found in geckos.

While some insects remain stuck to a single surface for almost their entire lifetime, others run quickly carrying heavy loads or jump between surfaces. This requires their feet to be dynamic – to stick one moment and release the next. An outstanding example of this is the weaver ant Oecophylla smaragdina, whose feet can support a theoretical maximum of 100 times its body weight, according to Walter Federle and Thomas Endlein from the Insect Biomechanics Workgroup at Cambridge University in the UK (figure 2). However, the ant can still almost immediately detach its feet to place its next step.

Endlein has also shown that some insects can mechanically unfold their feet passively – without neuronal signals – in fractions of a second. This overrides any possible delay and is useful in unexpected events of mechanical disturbance, such as raindrops or a gust of wind. However, the details of how insects control their feet so quickly are still not fully understood. In particular, the adhesion control during jumping, which can be a change from firm adhesion to complete detachment within a fraction of a second, is the focus of ongoing research.

All insect feet have foot pads that can be classed as one of two functional designs: "hairy" or "smooth". In general, both types let the insect attach itself more strongly to a surface by conforming to substrates with roughness at different length scales. This explains why insects can stick to so many different surface types: from hard to soft; rough to smooth; on stone, glass, plastic and even Teflon.

Smooth adhesive pads can be found in many groups of insects – ants, bees, stick insects, grasshoppers, bugs and cockroaches. These insects possess a specialized organ, the arolium, which is located at the tip of the feet and consists of a very soft, cushion-like sac.

As already described by Hooke more than 300 years ago, the pads on the feet of flies, beetles and other insect groups are densely covered with flexible hairs arranged in arrays. Today, we know that similar structures can be found in many other creatures, such as geckos and spiders, indicating a general favourable design for adhesive structures. Although it is believed that hairy pads have several advantages over smooth ones, there is still an ongoing discussion in the biomechanics community about which is the better system (see, for example, J Bullock, P Drechsler and W Federle 2008 J. Exp. Biol. 211 3333).

Whether they are smooth or hairy, all insect feet have one thing in common: they use a nanometre-thin layer of fluid to help them stick to surfaces. Power already suggested that this is secreted using a "fuzzy kinde of substance like little sponges", which the fly can squeeze liquid out of "at pleasure". However, it was only recently that Federle and I were able to show that this 300-year-old idea is actually true for the smooth pads of insects. Using a motorized-stage to repeatedly (and carefully!) press the feet of insects onto smooth glass plates to simulate footsteps, we found that the amount of residue actually decreases with each step. Insects, in other words, have a limited volume of adhesive fluid in their feet. We also repeated the experiment using different walking speeds and it turns out that the sponges always refill at the same rate, no matter how fast the insects run. Nevertheless, it is still not known where the adhesive fluid is actually produced within the insect's body.

As for the nature of this fluid, it is often thought to be a kind of sticky glue. But if this were the case, how would insects that place their sticky feet down ever lift them up again? The wet-adhesive mechanism is thought to result from three physical principles of fluid mechanics: the forces of surface tension; the pressure difference between the fluid and the surrounding air (Laplace pressure); and the viscosity of the fluid. But as you may know from walking with wet feet beside a swimming pool, a layer of fluid can reduce adhesion and friction forces. So why, then, do insects use fluid-based adhesion at all, if the additional fluid layer bears the danger of reducing their ability to walk on smooth surfaces?

To answer this question, a more detailed knowledge of insect-feet forces is required. Federle, and Patrick Drechsler from the University of Würzburg in Germany, were among the first to actually measure the forces generated by placing single insect feet on well-defined substrates. Using a custom-made force transducer on a 3D motor stage, they gently pushed and pulled insects' feet along various smooth and rough surfaces. By comparing the forces generated on these substrates the researchers were able to show that an important function of the fluid appears to be filling in the gaps between the pad and the surface. This maximizes the contact area of the adhesive pad and increases adhesion to rough substrates.

Interestingly, Drechsler and Federle found that the sliding friction forces generated by insects' wet feet were substantially greater than expected. The experiments also revealed a significant static-friction component, which prevents a resting insect from sliding on smooth surfaces. Unfortunately, neither of these friction forces can be explained by assuming a continuous "simple" fluid layer between the feet and the substrates. Chemical analyses of footprint droplets also revealed nothing that might help to explain the high friction observed in fluid layers where one would expect slippage. The fluids appear simply to contain long-chained hydrocarbons, fatty acids, carbohydrates and amino acids.

It was only when the fluid was observed in situ, in the moment it is secreted into the contact zone, that its secret was revealed. In 2002 Federle and collaborators from the universities of Würzburg, Glasgow and Berkeley used interference reflection microscopy to discover that the adhesive fluid of ants and stick-insects is not a simple fluid but consists of two components that together form an emulsion. The experiments demonstrated that the bulk component of this emulsion is an oily substance, which is stable even over several days at room temperature. (This is probably what was discovered in insects' footprints about 300 years ago.) The second, smaller component is a highly volatile water-like substance that evaporates within fractions of a second when in contact with air, which explains why it had never been found in residues before. Federle and co-workers suggested that this two-phase structure might play an important role in the generation of friction forces.

To test this idea my colleagues and I again measured the forces generated by a single adhesive pad, but this time using a special polymeric surface. This smooth coating works like a selective sponge by only absorbing the short-lived watery phase of the emulsion and leaving the oily part behind. By making thick and thin polymer layers with different absorbing capacities, we were able to compare the forces generated with both fluids present with those with only the oily part present. Our results showed that the friction forces of smooth pads were significantly reduced without the watery phase present: the insects were slipping on their own oil. (We later put this finding to good use – see figure 3.)

It turns out that both phases are vital, and together they form a non-Newtonian Bingham fluid. This means that the fluid behaves like a solid when at rest, but with a viscosity that decreases when it is sheared. It is this property that provides resistance to sliding, complementing the simple capillary adhesion.

• Watch the cockroaches slide like firefighters down a pole with the patented "Insectislide" technology, in this video.

From what we know today, Henry Power was surprisingly accurate with his first observations about the adhesive mechanisms of insects in 1664. Two centuries later, in 1884, the German scientist Hermann Dewitz paid late tribute to Power's pioneering work by writing "Many different ideas [about insect adhesion] have been expressed so far; oddly enough, the correct one seems to be the oldest of them."

Insects have been sticking around for the last couple of million years and, although their adhesive organs have been studied for about the last 300 years, their tricks have still not lost any of their fascination. To the attentive observer, and imaginative research-grant applicant, even such a "simple" thing as a fly running across the office window still demonstrates a great selection from nature's box of tricks.

When an insect journeys thorough the world, it has to cope with a variety of different substrates with changing and unpredictable orientation, contamination, roughness and wettability. In fact, there are only a few known natural surface structures that insects cannot stick to – mostly carnivorous plants! One such plant is the carnivorous pitcher – so-named because it looks like a jug. Many varieties of the plant have a hydrophilic rim. When the rim is dry, ants are able to climb in to the pitcher to collect nectar from just under the rim's mouth and then climb back out again. But as Holger Bohn and Ulrike Bauer from the University of Cambridge showed during their PhD work in the last few years, air humidity or rain can easily form a very thin water layer on the plant's surface. This layer somehow foils the insect's usually reliable feet and makes them aquaplane into the bottom of the pitcher, where they are destined to stew in the plant's digestive juices. But surprisingly, some ants can walk on the plants when they are wet and do not slip at all. They can climb in and out of the pitcher with ease, and even swim within the digestive fluid.

• Watch some unlucky ants meet their fate, while others manage to avoid the deadly trap, in this video.

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