Sorting out the Science of Stickiness

For many animals, to stick is to survive. Nature's varied adhesive structures and substances enable animals to stick to inert substrates, to each other, and even to parts of themselves. An octopus uses its suckers to grab food, a gecko coordinates its highly specialized feet to ascend a wall, and a mussel emits strings of proteinaceous goo to hold fast to a rock in times of turbulence. Insects coordinate their jumping motions by choreographing contact of leg parts. Some species can even multitask. The tube feet of echinoderms, for example, can specialize for attachment and locomotion, or feeding and burrowing. A symposium at the Society for Integrative and Comparative Biology's annual meeting in Anaheim, Calif., Jan. 2-6, celebrated the natural engineering wonders of adhesion. Explained Ciprien Gay, a polymer scientist at the National Center for Scientific Research in Bordeaux, France, "Adhesion is what happens at the interfaces between solids." His talk was called, simply, "stickiness." Other talks delved into the specifics of organisms' strategies for attachment. Adhesion biology is eclectic yet integrated, attracting chemists, physicists, engineers, and materials scientists, cell and molecular biologists, as well as those interested in ecology, ethology, or evolution. Reflecting this variety is the funding—support comes from the Office of Naval Research, the Defense Advanced Research Projects Agency (DARPA), the US Department of Agriculture, and private industry. Applications range from building a better bandage to cleaning ship hulls of crusty, clingy life. Experimental tools reflect the creativity of the field. To scrutinize stickiness, researchers dislodge ants spinning in centrifuges with strobe lights; run 18-inch-long lizards along all sorts of surfaces to test their tenacity; measure forces with pressure gauges; and take footprints using dental wax and epoxy resin. Yet the research also uses such higher-tech tools as mass spectrometry and atomic force microscopy. Macroscopic Adhesion Reflects Microscopic Events Adhesion research dissects the steps that underlie the ability to stick. Consider "leukocyte trafficking," the molecular interactions that deliver white blood cells to an injury site, felt on the whole-body level as inflammation. Adhesion proteins called selectins on certain white blood cells grab specific carbohydrates on blood vessel interiors, like a person shooting down a water slide grabbing at the walls. Daniel Hammer, chair and professor of bioengineering at the University of Pennsylvania, wondered whether the reigned-in cell slides—like Michael Jackson doing a moonwalk—or rolls. He set up an in vitro system to re-create the tango between selectin and carbohydrate interactions using budding yeast as a model for the blood cells.1 "We send carbohydrate-coated polystyrene microspheres over a surface dotted with selectins to re-create the dynamics of leukocyte rolling. As yeast buds, the rolling movement changes. And they roll, not slide," he reported. A gecko's remarkable movements also reflect smaller scale events. "These animals have turned their hind feet back into hands, which facilitates locomotion in a variety of directions," said Anthony Russell, a professor of biological sciences at the University of Calgary. Each gecko digit sports thousands of hair-like setae that branch into thousands more, ending in spatula-like tips. After many experiments that pulled and pushed the extensions, Kellar Autumn, a professor of biology at Lewis and Clark College in Portland, Ore., discovered that the setae of these "stubborn creatures" wouldn't stick without a small and increasing push, which boosts the adhesive force as more spatula tips form.2 "The animal needs only to attach 10% of its setae to generate maximal observed foot force. A gecko's worth of setae is very adhesive," Autumn said. The lizard's highly symmetrical stance also contributes to its agility, said Russell. "Gecko digits are more similar in size and spread more than those of other lizards. The trend toward symmetry of pads came about before adhesion was invented," he added. Gecko locomotion may therefore be an "exaptation," a new use for an existing capability. Autumn and Russell also observed that sticking setae pop off when displaced from the surface by more than a 30-degree angle. Geckos attach using van der Waals forces, the weak attraction that occurs as two materials approach one another. If the surfaces are large, the forces add up. "Geckos stick due to geometry, and not the chemistry of the surface," Autumn concluded. Sticking Chemically and Mechanically Organisms stick using chemical adhesives or mechanical interactions—or both. The tropical weaver ant of Southeast Asia is a master of both approaches. Up in the canopy, a single ant can straddle adjacent leaves and bind them with larval silk to form a nest the size of a football. "The tarsus [terminal leg segment] has claws that attach to rough surfaces and an adhesive pad that attaches to smooth surfaces," said Walter Federle, a visiting scholar at the University of California, Berkeley. The pad secretes a two-phase adhesive that acts like a surfactant, sealing leg to substrate, whether a leaf or a sheet of glass in the lab. Limpets also stick in two ways. "It's hard to rip a limpet off a rock. They live in a wave-swept environment, attached to rocks with nothing more than a thin layer of slime. They alternate between suction adhesion, when they are hunting algae, and being glued down," explained Andrew Smith, an assistant professor of biology at Ithaca College in New York.3 Limpet mucus, which is quite different from the familiar mammalian mucus, comprises 5% of the glue and is a tangle of proteins that entraps the other 95%, which is water. The animal secretes a stickier glue when it wants to stay put, thinning it when it needs to wander, leaving a trail. Chemical Sealing—of Mussels and Algae When a marine mussel senses increasing turbulence, it knits itself a holdfast organ and a water-resistant foam adhesive to cling to the substratum. The organ consists of byssal threads, each made in minutes from a specialized, foamy form of collagen. J. Herb Waite, a professor of molecular, cellular, and developmental biology at the University of California, Santa Barbara, explained this dramatic adaptation. "Mussels are very insecure organisms. When water flow increases, the mussel explores by extending a foot that is seven to eight times its length. It looks like it is tiptoeing around. Then the mussel becomes less mobile, and makes what looks like a cleaning motion. Then the foot becomes still as it assembles fibers. This is a fleeting and vulnerable state—predators can nip the foot off as the threads are made. Then the animal disengages." The primary forces that attach marine mussels are van der Waals. The secret to the "opportunistic stickiness" of mussel foam adhesive, said Waite, is addition of hydroxyl (OH) groups to certain tyrosine residues in the collagen, easing crosslinking. To a mussel, adhesion is an adaptation. To a ship hull, it is a form of biofouling. Another culprit is the spore adhesive of Enteromorpha, a green alga found in intertidal zones. Like mussel attachment, Enteromorpha follows a distinct choreography. "Over 10 to 15 minutes, a spore settles with a temporary and reversible adhesion. It then commits to irreversible, primary adhesion, which takes about a minute, when it secretes a preformed space-filling adhesive glycoprotein. Finally, in the consolidation phase, the adhesive cures. Sticky becomes stiff, in two to three minutes," explained James Callow, Mason Professor of Botany at the University of Birmingham, UK.5 Like mussels, algal stickiness may increase the odds of survival in the wake of turbulence. "Fluorescence micrographs of chlorophyll reveal small groups and singles before flow, and only big clumps of cells after flow. This settlement behavior may be adaptive, enabling groups to survive turbulence better," he added. Mechanical Sealing—of Octopuses and Insects Arrangement of antagonistic muscles powers the octopus sucker. William Kier, a professor of biology at the University of North Carolina at Chapel Hill, effectively demonstrated roughly how an octopus sucker sticks—he slammed a toilet bowl plunger against the podium. An octopus uses what physiologists call a "muscular hydrostat," a device that requires little energy to exert a powerful adhesive force, and is related to trunks and tongues. "Suction adhesion provides an amazing variety of functions: anchoring to surfaces, holding prey, chemotactile recognition, clinging. The octopus can grip a remarkable range of objects. It prefers flat surfaces, and can attach to objects smaller than the sucker. The sucker is the last thing a crab sees when it meets an octopus," said Kier of his "irascible grumpy animals." An octopus sucker is mostly muscle with some connective tissue, attached by muscle to the arm. The sucker is a spherical cavity, the acetabulum, that opens to form the infundibulum. Suction arises because the volume of the infundibulum must remain near-constant. So when the infundibulum adheres, a radial muscle contracts, thinning its wall. To maintain the wall's volume, the cavity expands, subambiant pressure is generated, and the arm sticks. Since the force originates in the sucker, researchers can study isolated octopus arms. Kier monitors whole-octopus action by forcing the animal to grab dental wax, then studies the imprints with scanning electron microscopy.6 Studying biological adhesion systems sheds light on evolution past and ecology present. It also provides what Autumn calls "biological inspiration" for a range of products that transcend simply brave new adhesives. Understanding the topographies of plant waxes and how they affect pest adhesion can be used to develop new herbicide strategies, suggests Stanislav Gorb, from the Max-Planck Institute of Developmental Biology in Tubingen, Germany. Autumn envisions geckotape, a RoboGecko on the next Mars mission, geckogloves for rockclimbing, setae as microscopic surgical tools, and last but not least, a counterpart to Spiderman. Geckoman, anyone? Ricki Lewis (rickilewis@nasw.org) is a contributing editor. References 1. K.-C. Chang et al., "The state diagram for cell adhesion under flow: leukocyte rolling and firm adhesion," Proceedings of the National Academy of Sciences, 97:11262-7, 2000. 2. K. Autumn et al., "Adhesive force of a single gecko foot-hair," Nature, 405:681-5, 2000. 3. A.M. Smith et al., "Differences in the composition of adhesive and non-adhesive mucus from the limpet Lottia limatula," Biological Bulletin, 196:34-44, 1999. 4. R.Y. Floriolli et al., "Marine surfaces and the expression of specific byssal adhesive protein variants in Mytilus," Marine Biotechnolology, 2:352-63, 2000. 5. J.A. Callow, "Cellular and molecular approaches to understanding primary adhesion in Enteromorpha: an overview." Biofouling, 16:141-50, 2000. 6. W.M. Kier, A.M. Smith, "The morphology and mechanics of octopus suckers," Biological Bulletin, 178:126-36, 1990

Sorting out the Science of Stickiness

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