Bioprospecting finds the toughest biological material: extraordinary silk from a giant riverine orb spider

Abstract

Background: Combining high strength and elasticity, spider silks are exceptionally tough, i.e., able to absorb massive kinetic energy before breaking. Spider silk is therefore a model polymer for development of high performance biomimetic fibers. There are over 41,000 described species of spiders, most spinning multiple types of silk. Thus we have available some 200,000+ unique silks that may cover an amazing breadth of material properties. To date, however, silks from only a few tens of species have been characterized, most chosen haphazardly as model organisms (Nephila) or simply from researchers' backyards. Are we limited to 'blindly fishing' in efforts to discover extraordinary silks? Or, could scientists use ecology to predict which species are likely to spin silks exhibiting exceptional performance properties?

Methodology: We examined the biomechanical properties of silk produced by the remarkable Malagasy 'Darwin's bark spider' (Caerostris darwini), which we predicted would produce exceptional silk based upon its amazing web. The spider constructs its giant orb web (up to 2.8 m(2)) suspended above streams, rivers, and lakes. It attaches the web to substrates on each riverbank by anchor threads as long as 25 meters. Dragline silk from both Caerostris webs and forcibly pulled silk, exhibits an extraordinary combination of high tensile strength and elasticity previously unknown for spider silk. The toughness of forcibly silked fibers averages 350 MJ/m(3), with some samples reaching 520 MJ/m(3). Thus, C. darwini silk is more than twice tougher than any previously described silk, and over 10 times better than Kevlar®. Caerostris capture spiral silk is similarly exceptionally tough.

Conclusions: Caerostris darwini produces the toughest known biomaterial. We hypothesize that this extraordinary toughness coevolved with the unusual ecology and web architecture of these spiders, decreasing the likelihood of bridgelines breaking and collapsing the web into the river. This hypothesis predicts that rapid change in material properties of silk co-occurred with ecological shifts within the genus, and can thus be tested by combining material science, behavioral observations, and phylogenetics. Our findings highlight the potential benefits of natural history-informed bioprospecting to discover silks, as well as other materials, with novel and exceptional properties to serve as models in biomimicry.

Figure 1. Webs of C. darwini spanning streams and rivers.

A, several C. darwini webs over river in Ranomafana. Individual web area (the extent of the sticky spiral) was about 0.5–1 m², the longest bridgelines exceeded 10 m. B, a web across a small stream in Andasibe-Mantadia NP illustrating architecture. Web width (outermost spirals)  = 105 cm.

Figure 2. Digital photographs of radial MAP (A) and spiral Flag silk and aggregate silk glue droplets (B).

Diameters and volumes of threads and glue are readily measured from these photographs. Scale bars are 10 µm.

Figure 3. Tensile performance of C. darwini dragline silk compared to other spiders.

A) the strength of Caerostris silk is high but unexceptional while stiffness is slightly below average. B) In contrast extensibility and toughness of C. darwini forcibly pulled silk both far surpass that found in the broad taxonomic sample by Swanson et al. (2007). Red lines show the range of Caerostris silks with dots indicating average values. Note that Caerostris was not included in the phylogeny of Swanson et al. (2007), red dots are placed arbitrarily among other orbweavers. Vertical grey lines show average values across the spiders examined by Swanson et al. (2007).

Figure 4. Comparison of C. darwini silk tensile tests to other orb spiders.

Each line represents a single silk sample, with strength measured as stress on the y axis and stretchiness on the x axis. The tensile strength and total stretchiness of a silk are represented by the end of the lines, where the fibers break. The curves for Argiope are typical for orb weaving spiders, while the bars represent the total variation in pulled dragline silk strength and stretchiness across spiders (from Swanson et al 2006). Caerostris darwini silk is far stretchier than typical major ampullate silk. This allows Caerostris silk to absorb massive amounts of kinetic energy without breaking, making it the toughest biological material ever discovered. Across all spiders, Swanson et al (2006) found that silk toughness ranged from 50–230 MJ/m3. These values are already exceptional when compared to synthetic materials like Kevlar (33 MJ/m3). However, silk from C. darwini exhibited an average toughness of 350 MJ/m3 across 10 spiders, with some individuals ranging up to 500 MJ/m3.