Elastic modulus and toughness of orb spider glycoprotein glue

Abstract

An orb web’s prey capture thread features tiny glue droplets, each formed of an adhesive glycoprotein core surrounded by an aqueous layer. Small molecules in the aqueous layer confer droplet hygroscopicity and maintain glycoprotein viscoelasticity, causing droplet volume and glycoprotein performance to track changes in environmental humidity. Droplet extension combines with that of a thread’s supporting flagelliform fibers to sum the adhesive forces of multiple droplets, creating an effective adhesive system. We combined measurements of the force on an extending droplet, as gauged by the deflection of its support line, with measurements of glycoprotein volume and droplet extension to determine the Young’s modulus (E) and toughness of three species’ glycoproteins. We did this at five relative humidities between 20–90% to assess the effect of humidity on these properties. When droplets of a thread span extend, their extensions are constrained and their glycoprotein filaments remain covered by aqueous material. This was also the case during the first extension phase of the individual droplets that we examined. However, as extension progressed, the aqueous layer was progresses disrupted, exposing the glycoprotein. During the first extension phase E ranged from 0.00003 GPa, a value similar to that of fibronectin, a glycoprotein that anchors cells in the extracellular matrix, to 0.00292 GPa, a value similar to that of resilin in insect ligaments. Second phase E increased 4.7–19.4-fold. When compared at the same humidity the E of each species’ glycoprotein was less than 5% of the value reported for its flagelliform fibers. This difference may facilitate the coordinated extension of these two capture thread components that is responsible for summing the thread’s adhesive forces.

Linking properties of an orb‐weaving spider's capture thread glycoprotein adhesive and flagelliform fiber components to prey retention time

“…A growing number of studies on the properties and performance of orb‐weaver prey capture thread have revealed details about this natural adhesive system and how it responds to environmental humidity (Figure d), temperature, ultraviolet light, and insect surface texture (Opell Clouse & Andrews, ; Opell, Jain, et al, ; Opell & Schwend, ; Stellwagen, Opell, & Clouse, , ; Stellwagen, Opell, & Short, ). Humidity has a pronounced effect on glue droplet adhesion, and interspecific differences in this response have been attributed to natural selection that optimizes thread performance to the humidity of each species' habitat (Amarpuri, Zhang, et al, ).…”

“…Capture thread adhesion has been characterized in two ways: (a) the force required to pull a thread or one of its glue droplets from a surface (Opell & Hendricks, ; Opell, Karinshak, & Sigler, ) and (b) the work done in pulling a thread or glue droplet from a surface (Opell, Clouse, & Andrews, ; Piorkowski & Blackledge, ; Sahni, Blackledge, & Dhinojwala, ). The latter approach probably best characterizes a thread's ability to overcome the work of an ensnared insect as it struggles to escape from a web.…”

“…To better understand this highly integrated and compliant adhesive system, our study attempted to model the contributions glycoprotein adhesive and flagelliform fibers in the capture threads of A. aurantia , A. trifasciata , and A. marmoreus . Although the material properties of these three species' axial lines are reported in the literature (Sensenig, Agnarsson, & Blackledge, ), this required us to characterize the properties of their glycoproteins at each of the three experimental RH's (37%, 50%, and 72%) using recently developed techniques (Opell, Clouse, & Andrews ().…”

“…The LMMCs serve several important functions. Along with glycoproteins, they confer hygroscopicity, causing the droplets' size and performance to change over the course of a day as they track environmental humidity (Figure d; Jain et al, ; Opell, Clouse, & Andrews, ; Opell, Jain, et al, ), they maintain glycoprotein structure and solvate glycoprotein, enhancing its surface interaction (Sahni et al, ), and they remove interfacial water from a droplet's contact footprint, enhancing adhesion (Singla, Amarpuri, Dhopatkar, Blackledge, & Dhinojwala, ). Optimal adhesion of an araneoid glue droplet is achieved when the viscosity of the droplet's glycoprotein is low enough to spread on a surface to establish sufficient adhesive contact, but high enough to ensure that the glycoprotein will cohere as it extends, thereby transferring adhesive force to the thread's axial lines (Figure c; Amarpuri, Zhang, Blackledge, & Dhinojwala, ; Amarpuri, Zhang, et al, ).…”

“…Optimal adhesion of an araneoid glue droplet is achieved when the viscosity of the droplet's glycoprotein is low enough to spread on a surface to establish sufficient adhesive contact, but high enough to ensure that the glycoprotein will cohere as it extends, thereby transferring adhesive force to the thread's axial lines (Figure c; Amarpuri, Zhang, Blackledge, & Dhinojwala, ; Amarpuri, Zhang, et al, ). Glycoprotein viscosity is determined primarily by the LMMCs in the droplets aqueous layer (Jain et al, ; Opell, Clouse, & Andrews, ; Opell, Jain, et al, ) and tuned to the humidity of an orb‐weaving species' habitat during a spider's foraging time (Amarpuri, Zhang, et al, ).…”