Andrew Sensenig

Behavioural and biomaterial coevolution in spider orb webs

Mechanical performance of biological structures, such as tendons, byssal threads, muscles, and spider webs, is determined by a complex interplay between material quality (intrinsic material properties, larger scale morphology) and proximate behaviour. Spider orb webs are a system in which fibrous biomaterials—silks—are arranged in a complex design resulting from stereotypical behavioural patterns, to produce effective energy absorbing traps for flying prey. Orb webs show an impressive range of designs, some effective at capturing tiny insects such as midges, others that can occasionally stop even small birds. Here, we test whether material quality and behaviour (web design) co‐evolve to fine‐tune web function. We quantify the intrinsic material properties of the sticky capture silk and radial support threads, as well as their architectural arrangement in webs, across diverse species of orb‐weaving spiders to estimate the maximum potential performance of orb webs as energy absorbing traps. We find a dominant pattern of material and behavioural coevolution where evolutionary shifts to larger body sizes, a common result of fecundity selection in spiders, is repeatedly accompanied by improved web performance because of changes in both silk material and web spinning behaviours. Large spiders produce silk with improved material properties, and also use more silk, to make webs with superior stopping potential. After controlling for spider size, spiders spinning higher quality silk used it more sparsely in webs. This implies that improvements in silk quality enable ‘sparser’ architectural designs, or alternatively that spiders spinning lower quality silk compensate architecturally for the inferior material quality of their silk. In summary, spider silk material properties are fine‐tuned to the architectures of webs across millions of years of diversification, a coevolutionary pattern not yet clearly demonstrated for other important biomaterials such as tendon, mollusc byssal threads, and keratin.

Spider orb webs rely on radial threads to absorb prey kinetic energy

The kinetic energy of flying insect prey is a formidable challenge for orb-weaving spiders. These spiders construct two-dimensional, round webs from a combination of stiff, strong radial silk and highly elastic, glue-coated capture spirals. Orb webs must first stop the flight of insect prey and then retain those insects long enough to be subdued by the spiders. Consequently, spider silks rank among the toughest known biomaterials. The large number of silk threads composing a web suggests that aerodynamic dissipation may also play an important role in stopping prey. Here, we quantify energy dissipation in orb webs spun by diverse species of spiders using data derived from high-speed videos of web deformation under prey impact. By integrating video data with material testing of silks, we compare the relative contributions of radial silk, the capture spiral and aerodynamic dissipation. Radial silk dominated energy absorption in all webs, with the potential to account for approximately 100 per cent of the work of stopping prey in larger webs. The most generous estimates for the roles of capture spirals and aerodynamic dissipation show that they rarely contribute more than 30 per cent and 10 per cent of the total work of stopping prey, respectively, and then only for smaller orb webs. The reliance of spider orb webs upon internal energy absorption by radial threads for prey capture suggests that the material properties of the capture spirals are largely unconstrained by the selective pressures of stopping prey and can instead evolve freely in response to alternative functional constraints such as adhering to prey.

MECHANICAL ENERGY OSCILLATIONS DURING LOCOMOTION IN THE HARVESTMAN LEIOBUNUM VITTATUM (OPILIONES)

Abstract The long legs, compact body and hanging posture of many harvestmen are unique among terrestrial animals, but no quantitative analyses of locomotion have been conducted to determine if this extreme morphology is associated with novel mechanisms of locomotion. Here we have undertaken a three-dimensional kinematic analysis of running Leiobunum vittatum (Say 1821) using field-by-field analysis of high-speed video. The center of mass of harvestmen was found to undergo vertical and transverse displacements of unprecedented magnitude, but the pattern of displacements was consistent with those predicted by general models of energetic efficiency and dynamic stability of pedestrian locomotion. Because these models assume substantial roles for elastic energy storage in leg elements, elasticity is probably an important component of the locomotor mechanism in harvestmen, and we identify two skeletomuscular elements as possible springs.

Mechanical performance of spider orb webs is tuned for high-speed prey.

SUMMARY Spiders in the Orbiculariae spin orb webs that dissipate the mechanical energy of their flying prey, bringing the insects to rest and retaining them long enough for the spider to attack and subdue their meals. Small prey are easily stopped by webs but provide little energetic gain. While larger prey offer substantial nourishment, they are also challenging to capture and can damage the web if they escape. We therefore hypothesized that spider orb webs exhibit properties that improve their probability of stopping larger insects while minimizing damage when the mechanical energy of those prey exceeds the webs capacity. Large insects are typically both heavier and faster flying than smaller prey, but speed plays a disproportionate role in determining total kinetic energy, so we predicted that orb webs may dissipate energy more effectively under faster impacts, independent of kinetic energy per se. We used high-speed video to visualize the impact of wooden pellets fired into orb webs to simulate prey strikes and tested how capture probability varied as a function of pellet size and speed. Capture probability was virtually nil above speeds of ~3 m s−1. However, successful captures do not directly measure the maximum possible energy dissipation by orb webs because these events include lower-energy impacts that may not significantly challenge orb web performance. Therefore, we also compared the total kinetic energy removed from projectiles that escaped orb webs by breaking through the silk, asking whether more energy was removed at faster speeds. Over a range of speeds relevant to insect flight, the amount of energy absorbed by orb webs increases with the speed of prey (i.e. the rates at which webs are stretched). Orb webs therefore respond to faster – and hence higher kinetic energy – prey with better performance, suggesting adaptation to capture larger and faster flying insect prey. This speed-dependent toughness of a complex structure suggests the utility of the intrinsic toughness of spider silk and/or features of the macro-design of webs for high-velocity industrial or military applications, such as ballistic energy absorption.

Webs in vitro and in vivo: spiders alter their orb-web spinning behavior in the laboratory

Abstract Many studies of the elegant architectures of orb webs are conducted in controlled laboratory environments that remove environmental variability. The degree to which spider behavior in these circumstances resembles that of spiders in the wild is largely unknown. We compared web architecture and silk investment of furrowed orb weavers Larinioides cornutus (Clerck 1757) building webs in laboratory cages and spinning webs on fences in the field and found significant differences. The volume of major ampullate silk in radii was 53% lower in cage webs, primarily because the silk was 50% thinner, but also because spiders tended to spin 14% fewer radii than in fence webs. Cage spiders also invested about 40% less flagelliform silk and aggregate glue in the capture spiral, although the difference was not statistically significant, a trend primarily driven by a decrease in the length of the glue-coated capture spiral. These patterns were consistent with spiders reducing silk investment when building at new web sites while they assessed insect abundance. Differences in the type of substrate for web attachment, amount of available space, and condition may also have influenced web architecture. Cage webs were more symmetrical than fence webs, which displayed an unusual horizontal asymmetry that may have maximized their capture areas within the constraints of the available fence-railing attachment sites. Our findings suggest using caution when generalizing the properties of laboratory-spun webs to more natural conditions. More importantly, they demonstrate that orb spiders actively modify their behaviors when spinning webs under different conditions.

Hydrodynamic pumping by serial gill arrays in the mayfly nymph Centroptilum triangulifer

SUMMARY Aquatic nymphs of the mayfly Centroptilum triangulifer produce ventilatory flow using a serial array of seven abdominal gill pairs that operates across a Reynolds numbers (Re) range from 2 to 22 during ontogeny. Net flow in small animals is directed ventrally and essentially parallel to the stroke plane (i.e. rowing), but net flow in large animals is directed dorsally and essentially transverse to the stroke plane (i.e. flapping). Detailed flow measurements based on Particle Image Velocimetry (PIV) ensemble-correlation analysis revealed that the phasing of the gills produces a time-dependent array of vortices associated with a net ventilatory current, a fluid kinematic pattern, here termed a ‘phased vortex pump’. Absolute size of vortices does not change with increasing animal size or Re, and thus the vortex radius (Rv) decreases relative to inter-gill distance (Lis) during mayfly growth. Given that effective flapping in appendage-array animals requires organized flow between adjacent appendages, we hypothesize that rowing should be favored when Lis/Rv<1 and flapping should be favored when Lis/Rv>1. Significantly, the rowing-to-flapping transition in Centroptilum occurs at Re∼5, when the mean dynamic inter-gill distance equals the vortex radius. This result suggests that the Re-based rowing–flapping demarcation observed in appendage-array aquatic organisms may be determined by the relative size of the propulsive mechanism and its self-generated vortices.