When Rainer Foelix read a 2006 Nature paper from Stanislav Gorb’s lab (Gorb et al., 2006, Nature443, 407) and Claire Rind’s 2010 JEB paper (Rind et al., 2011, J. Exp. Biol.214, 1874-1879) reporting that tarantulas secrete silk from their feet to steady themselves during falls, Foelix was sceptical. In 1968, he had discovered chemosensitive (taste) hairs on the legs of spiders, and when he saw the electron microscopy images of the hair structures that were proposed to produce the tarantula’s stabilising foot silk, Foelix was perplexed. They looked very similar to the taste hairs that he had identified 40 years before, but the hairs produced some kind of secretion when the animals slipped, which could be silk. Intrigued by the puzzle, Foelix decided to take a closer look at the hairs to find out whether they are silk-producing spigots or chemosensors (p. 1084).
As he was familiar with the structure of arachnid chemosensory hairs, Foelix knew that he would have to look inside the hair structures to find out whether they had any of the telltale features that he would expect to find. Collecting specimens from five species of tarantula, Foelix scrutinised their shed skins with light microscopy and scanning electron microscopy. He found the long ridged hair shafts that the other researchers had described protruding above the spider’s brush-like adhesive hairs. The ridged hairs were also sparsely distributed amongst the adhesive hairs. Zooming in on the hairs, Foelix found a narrow pore at the tip of each hair, which was often covered by a blob of fluid. Foelix says, ‘A distal pore opening is a must for any contact chemoreceptor. This is where the nerve endings (dendrites) are exposed to the environment. They also have to be bathed in a fluid (receptor lymph), otherwise they would dry out quickly.’ And when Foelix looked through the hair shaft using light microscopy, the pore continued into a central canal. Also, instead of extending to a silk canal at the base of the hairs, the canal terminated much earlier; just like the fluid-filled canal in other arachnid chemosensors.
Having convinced himself that the hairs had all of the characteristics of chemoreceptors and not silk spigots, Foelix was still left with the puzzle about the secretions produced by the hairs. Were they silk or some other substance? Teaming up with Bastian Rast and Anne Peattie, Foelix compared the tarantula foot hairs with the spigots on the spiders’ spinnerets. Pressing the spiders’ feet and spinnerets against clean glass slides, the team found that the spinnerets produced masses of silk thread. However, the footprints appeared to produce only a few silk threads, which Foelix suspects had been picked up previously from the tarantula’s spinnerets.
Next, Peattie caused the feet of a Chilean rose tarantula to slip on a glass slide. This time they successfully produced the same silk-like trails from the hairs that other researchers had found. However, instead of continuing to pay out after losing contact with the glass, the threads always snapped. And when Foelix took a closer look at the secretions, he realised that the trails could not be threads, as some of them were composed of droplets rather than a continuous strand. Foelix suspects that instead of exuding silk, the hairs ooze lymph as they are dragged along a surface during a slip.
So Foelix and his colleagues are convinced that the hairs are chemosensors instead of spigots and that tarantulas do not exude silk from their feet to break a fall, and he keenly anticipates the next instalment in this heated debate.