High-performance spider webs: integrating biomechanics, ecology and behaviour

Abstract

Spider silks exhibit remarkable properties, surpassing most natural and synthetic materials in both strength and toughness. Orb-web spider dragline silk is the focus of intense research by material scientists attempting to mimic these naturally produced fibres. However, biomechanical research on spider silks is often removed from the context of web ecology and spider foraging behaviour. Similarly, evolutionary and ecological research on spiders rarely considers the significance of silk properties. Here, we highlight the critical need to integrate biomechanical and ecological perspectives on spider silks to generate a better understanding of (i) how silk biomechanics and web architectures interacted to influence spider web evolution along different structural pathways, and (ii) how silks function in an ecological context, which may identify novel silk applications. An integrative, mechanistic approach to understanding silk and web function, as well as the selective pressures driving their evolution, will help uncover the potential impacts of environmental change and species invasions (of both spiders and prey) on spider success. Integrating these fields will also allow us to take advantage of the remarkable properties of spider silks, expanding the range of possible silk applications from single threads to two- and three-dimensional thread networks.

Figure 1.

Representative stress–strain curve of Argiope keyserlingi radial silk showing the key measures of biomechanical properties in spider silks (A. M. T. Harmer, 2010 unpublished data). The biomechanical properties of spider silks (and materials in general) are defined by several key parameters. These include: stress, calculated as force divided by the cross-sectional area of the fibre (engineering stress). For silks, this is usually converted to true stress by multiplying engineering stress by L/L₀ (length of stretched fibre/original length; e.g. [79]). This approximates the instantaneous cross-sectional area of the fibre that is important for elastic materials [78]. Strain measures the change in the length of a fibre relative to its original length (engineering strain). It is usually converted to true strain by taking the natural log of L/L₀ [146]. Tensile strength is the stress at the breaking point of a material under uniaxial loading [78]. Extensibility describes the stretchiness of a fibre, for example the percentage increase in a fibre's length at breaking when compared with its original length. Stiffness is defined by Young's modulus and is calculated from the slope of the initial elastic region of the stress–strain curve. It is a measure of the ability of a fibre to resist deformation [95]. Yield is the point where a fibre transitions from elastic (and reversible) deformation to plastic deformation. Higher yield values make fibres more resistant to permanent deformation [33]. Toughness is the energy required to break a thread. It is calculated as the area under the stress–strain curve [95]. Hysteresis (not shown on figure) is the proportion of energy lost during a loading–unloading cycle [78]. The energy required to stretch a silk thread is greater than that required to return it to its natural state as some energy is lost as heat.

Figure 2.

Hierarchical structure of two common web types, an orb-web and cobweb. (a) Microhabitat in which each web type is generally found. Orb-webs usually span open spaces in and between vegetation. Cobwebs tend to enclose three-dimensional spaces between two substrates. (b) Representative orb-web showing the main structural elements. An orb-web is suspended in space, potentially metres from the nearest vegetation, by three or more anchor threads (dragline silk). The anchor threads attach to frame threads (dragline silk), which form the periphery of the web. The radial threads (dragline silk) attach to the frame and converge on the centre of the web known as the hub [62]. During web construction, the radials are overlaid with a widely spaced, non-viscid temporary spiral. This is then replaced (with the exception of nephilids [18]) by the final, closely spaced, viscid capture spiral, creating a more or less evenly spaced mesh (redrawn and modified from Jocqué & Dippenaar-Schoeman [147]). (c) Representative cobweb showing the main structural elements. Cobwebs are usually built between two substrates and consist of a supporting network of scaffolding threads with the capture (gumfoot) threads spanning the space between the scaffolding and the substrate. Both scaffolding and gumfoot threads are composed of dragline silk, but the gumfoot lines have glue droplets deposited on their lower portions (redrawn and modified from Jocqué & Dippenaar-Schoeman [147]). (d) Distribution of forces during orb-web function. During prey impacts, the relatively strong and stiff radial threads (bold line) probably perform most of the work of dissipating prey energy, acting much like shock absorbers [78]. The much more compliant capture spiral (dotted lines) may contribute to energy dissipation via thread displacement and aerodynamic damping [64]. F = prey force, rF = restoring force of pre-tensioned threads. (e) Distribution of forces during cobweb function. Cobwebs are more likely to encounter ambulatory prey that stumble against a gumfoot thread, which then breaks and restrains or lifts the prey towards the scaffolding and waiting spider. Pre-tensioning of the gumfoot threads and scaffolding helps catapult small prey up into the web (redrawn and modified from Boutry & Blackledge [33]). F = prey force, rF = restoring force of pre-tensioned threads. (f) Orb-web viscid silk (left) and simplified molecular structure of relaxed (top right) and stretched (bottom right) fibre. Note the glue droplets distributed along the viscid silk fibre. Viscid silk is composed largely of β-spirals that act as nanosprings (redrawn from Becker et al. [81]). D = direction of fibre elongation. (g) Dragline silk (left) and simplified molecular structure of relaxed (top right) and stretched (bottom right) fibre. β-sheet crystals are embedded in a semi-amorphous network of β-turns and helices. When a fibre is stretched, there is a transition from β-turns to β-sheets in the amorphous regions (schematic adapted from Keten & Buehler [45]). D = direction of fibre elongation. (h) Representative stress–strain curves for dragline silk and viscid silk in the web of A. keyserlingi (Harmer, unpublished data). The high tensile strength and stiffness of dragline silk [35] allow it to absorb the energy of prey impacts [4]. The extreme compliance of viscid silk, on the other hand, results in lower tensile strength but much greater extensibility (and lower stiffness) than dragline silk [35]. This allows viscid silk to dissipate energy via thread displacement and stretching and prevents insects from ricocheting out of webs [4]. Stress–strain curves for dragline silks typically show an initial phase of high stiffness before the fibre yields. The fibre then shows plastic deformation until rupture. Viscid silks do not show an initial elastic phase, but instead exhibit high extensibility (more than 200–300%) before an exponential increase in stiffness just prior to failure. Such ‘j-shaped’ stress–strain curves are indicative of natural biomaterials that need to be stretchy for performance but also have high safety factors.

Figure 3.

Evolutionary and environmental influences on spider web function. Silk biomechanics are influenced by both evolutionary effects (such as gene/protein diversification and spider morphology) and by the environmental conditions under which silks are produced. In the same way, overall web architecture can be influenced by genetically determined web-building behaviours and the evolution of novel web elements, as well as by environmental factors (such as prey, microhabitat and flexibility in spider behaviour). Both silk biomechanics and web architecture interact to determine how a web functions to catch prey.