Changes in the adhesive properties of spider aggregate glue during the evolution of cobwebs

Abstract

We compare the prey capture glues produced by orb-weaving spiders (viscid glue) and their evolutionary descendents, the cobweb-weaving spiders (gumfoot glue). These glues are produced in homologous glands but exhibit contrasting structure, properties and response to changing humidity. Individual glue droplet stretching measurements indicate that the gumfoot glue behaves like a viscoelastic liquid in contrast to the viscid glue, which behaves like a viscoelastic solid. Moreover, the gumfoot glue is largely humidity-resistant - elasticity and adhesion are constant across variation in humidity and there is weak volume-dependence. Viscid glue, however, is highly humidity-sensitive. The glue expands an order of magnitude and demonstrates a monotonous reduction in elasticity under increased humidity, while glue adhesion optimizes at intermediate levels of humidity. We suggest that observed differences are due to different 'tackifiers' used in these systems. These results shall inspire future efforts in fabricating stimuli-resistant and stimuli-sensitive materials.

Figure 1. Gumfoot silk glue vs. viscid silk glue (a) and (b) show individual viscid silk thread and gumfoot silk thread spun by Larinioides cornutus and Latrodectus hesperus, respectively.

Capture threads were laid on clean cover slips for both the cases. The difference in the wetting kinetics of the coating peptides and the high-molecular-weight adhesive polymers (probably glycoproteins) gives the appearance of a ‘diffuse core' in the gumfoot silk glue droplets. The glue droplets homogenize with time which disperses the core. Also, this core is not observed in pictures of suspended gumfoot silk threads. Scale bar is 20 µm for both the cases. (c) and (d) show a gumfoot silk thread at 0% R.H. and 90% R.H., respectively. It was observed that when a gumfoot silk thread is humidified, the glue droplets flow and coalesce to form bigger droplets.

Figure 2. Water uptake of the glues.

Change in volume of the viscid silk glue (squares) and gumfoot silk glue (circles) as the silk threads are exposed to a high-humidity environment. Insets a and b show gumfoot silk glue while c and d show viscid silk glue at 0% R.H. and 100% R.H., respectively. Similar to figure 1c and d, inset b shows fewer but bigger glue drops than inset a. Scale bar is 100 µm for all the figures. The uptake of water in viscid silk glue drops is due to the presence of low molecular weight hygroscopic compounds present in the glue. It was experimentally determined that there is no hysteresis in water uptake with humidity cycling (data not shown). In the case of the gumfoot silk glue, however, the order of changing humidity plays a role. While going up in humidity for the first time, the glue drops on gumfoot silk coalesce to form bigger drops and a slight change in total glue volume is observed (circles). Reducing the humidity subsequently restores the original glue volume but obviously not the original number of glue drops. Subsequent humidity cycles are completely reversible in terms of both glue volume and number of glue drops.

Figure 3. Effect of humidity on the stretching behavior of the glues.

Force-displacement behavior when glue drops of viscid silk (gumfoot silk), equilibrated at 15% R.H. a(b), 40% R.H. c (d), and 90 % R.H. e (f), were stretched at 1 µm/s (inverted triangles), 10 µm/s(upright triangles), 50 µm/s(squares), and 100 µm/s (circles).

Figure 4. Comparison between viscid silk glue and gumfoot silk glue.

(a) and (b) Force-displacement behavior when individual glue drops of viscid silk and gumfoot silk, equilibrated at 15% R.H. (circles), 40% R.H. (squares), and 90 % R.H. (upright triangles), are stretched at 50 µm/s, respectively (data from Figure 2). (c) Comparison of the pull-off force obtained from Figure 4a and b with the capillary forces exerted by unentangled PDMS (γ ∼ 20 mN/m) and an aqueous solution of composition similar to the viscous coat used by modern orb-weaving spiders to coat their capture threads (γ ∼ 40 mN/m). VSS glue denotes viscid spiral silk glue whereas GFS glue denotes gumfoot silk glue. GFS glue is represented by box and whiskers outlined by red (15% R.H.), blue (40% R.H.), and green (90% R.H.), whereas, for VSS glue, boxes and whiskers are outlined with black and boxes are filled with the color. PDMS is represented by box filled with purple whereas aqueous solution is represented by box and whiskers outlined with purple. d) Comparison of energy of adhesion between viscid silk glue, gumfoot silk glue, and the U_glue values obtained using the energy model (supplementary information). Values are obtained by multiplying the area under the force-displacement curve obtained from individual glue drop stretching measurements by 42 (number of glue drops in contact with a 2 mm glass substrate used for the peeling experiments). Even though gumfoot silk does not have 42 droplets per 2 mm length, and thread peeling measurements were not performed with it, values plotted are obtained by multiplying the area under the force-displacement curve by 42, to compare it with viscid silk glue and the U_glue values obtained using the energy model. Values are plotted as box and whiskers from 5 measurements each. VSS glue is represented by box and whiskers outlined with black and filled with red (1µm/s), blue (10µm/s), green (50 µm/s), and purple (100 µm/s). GFS glue, depending on the rate of stretching, is outlined by one of the above colors. U_glue values are represented by blank boxes outlined with black.

Figure 5. Effect of humidity on crosslinkers.

Load-relaxation behavior of individual glue drops of viscid silk (gumfoot silk) equilibrated at 15% R.H. a (b), 40% R.H. c (d), and 90% R.H. e (f) stretched by a constant length at rates of 1 µm/s (inverted triangles), 10 µm/s (upright triangles), 50 µm/s (squares) and 100 µm/s (circles). Values are plotted as mean ± s.d. from 5 measurements each. When viscid silk glue is stretched at 100 µm/s at 15% R.H., it releases contact with the tip before stretching 100 µm (Figure 3a), hence load relaxation measurements could not be performed at these conditions. (Figure 5a)

Figure 6. Effect on glue elasticity.

Plateau values, indicative of the amount of elasticity in the glue, reduce with increasing humidity in the case of viscid silk glue (a) but remain constant for gumfoot silk glue (b). Plateau values for gumfoot silk glue are plotted using a fitting function since the values were lower than the resolution of the equipment (1µN).

Figure 7. Polymer model to understand the humidity effect.

(a) Pull-off energy plotted as a function of concentration of the PEO/water solution at a pull-off rate of 1mm/sec. (b) Energy calculated as area under the load-displacement curve during pull-off plotted as a function of the pull-off rate for concentrations of 13.7% (circle), 17.7% (upright triangles), 35.5% (squares), and 52.2 % (inverted triangles) of the PEO/Water solutions. (c) A schematic of the state of the glue drops at different values of R.H. Chemical crosslinking (red) remains unaffected with changes in humidity while the viscosity and elasticity reduce with increasing humidity. Lubricating action becomes predominant at higher values of humidity.