Vertical asymmetries in orb webs

Journal of Experimental Biology

Jain

Dhinojwala

et al. 2018

Orb-weaving spiders use adhesive threads to delay the escape of insects from their webs until the spiders can locate and subdue the insects. These viscous threads are spun as paired flagelliform axial fibers coated by a cylinder of solution derived from the aggregate glands. As low molecular mass compounds (LMMCs) in the aggregate solution attract atmospheric moisture, the enlarging cylinder becomes unstable and divides into droplets. Within each droplet an adhesive glycoprotein core condenses. The plasticity and axial line extensibility of the glycoproteins are maintained by hygroscopic LMMCs. These compounds cause droplet volume to track changes in humidity and glycoprotein viscosity to vary approximately 1000-fold over the course of a day. Natural selection has tuned the performance of glycoprotein cores to the humidity of a species' foraging environment by altering the composition of its LMMCs. Thus, species from low-humidity habits have more hygroscopic threads than those from humid forests. However, at their respective foraging humidities, these species' glycoproteins have remarkably similar viscosities, ensuring optimal droplet adhesion by balancing glycoprotein adhesion and cohesion. Optimal viscosity is also essential for integrating the adhesion force of multiple droplets. As force is transferred to a thread's support line, extending droplets draw it into a parabolic configuration, implementing a suspension bridge mechanism that sums the adhesive force generated over the thread span. Thus, viscous capture threads extend an orb spider's phenotype as a highly integrated complex of large proteins and small molecules that function as a self-assembling, highly tuned, environmentally responsive, adhesive biomaterial. Understanding the synergistic role of chemistry and design in spider adhesives, particularly the ability to stick in wet conditions, provides insight in designing synthetic adhesives for biomedical applications.

Section: Physiological and Ecological Impact Of Humiditymentioning

confidence: 99%

Tuning orb spider glycoprotein glue performance to habitat humidity

Journal of Experimental Biology

Jain

Dhinojwala

et al. 2018

“…These include: (1) the mass of an insect and its impact velocity, (2) the number of capture threads that it strikes, (3) the region of the web a prey strikes, and (4) whether, after struggling free from these threads, the insect tumbles into other capture threads (Blackledge and Zevenbergen, 2006;Zschokke and Nakata, 2015). Moreover, insects often exhibit bouts of escape behavior with intervals of inactivity.…”

Section: Introductionmentioning

confidence: 99%

Humidity-mediated changes in an orb spider's glycoprotein adhesive impact prey retention time

Journal of Experimental Biology

Buccella

Godwin

et al. 2017

Properties of the viscous prey capture threads of araneoid orb spiders change in response to their environment. Relative humidity (RH) affects the performance of the thread's hygroscopic droplets by altering the viscoelasticity of each droplet's adhesive glycoprotein core. Studies that have characterized this performance used smooth glass and steel surfaces and uniform forces. In this study, we tested the hypothesis that these changes in performance translate into differences in prey retention times. We first characterized the glycoprotein contact surface areas and maximum extension lengths of Araneus marmoreus droplets at 20%, 37%, 55%, 72% and 90% RH and then modeled the relative work required to initiate pull-off of a 4 mm thread span, concluding that this species' droplets and threads performed optimally at 72% RH. Next, we evaluated the ability of three equally spaced capture thread strands to retain a house fly at 37%, 55% and 72% RH. Each fly's struggle was captured in a video and bouts of active escape behavior were summed. House flies were retained 11 s longer at 72% RH than at 37% and 55% RH. This difference is ecologically significant because the short time after an insect strikes a web and before a spider begins wrapping it is an insect's only opportunity to escape from the web. Moreover, these results validate the mechanism by which natural selection can tune the performance of an orb spider's capture threads to the humidity of its habitat.

“…Translating these humidity‐mediated material properties of orb spider glycoprotein glue into prey retention performance is challenging because many factors other than capture thread adhesion affect prey retention by orb webs. These include web orientation (horizontal vs. vertical), velocity of insect impact, the number of capture spirals contacted, the surface texture of the insect body regions that contact capture threads, the insect's struggle behavior, and whether or not an insect readheres to capture threads after pulling free of one set of threads and tumbling into lower capture thread spirals of a vertical orb web (Blackledge & Zevenbergen, ; Opell & Schwend, ; Zschokke & Nakata, ). As in the previous study of A. marmoreus (Opell et al, ), we attempted to control for as many of these variables as possible by preparing three horizontally oriented capture thread arrays from each spider's web sample and by placing an anesthetized adult Musca domestica Linnaeus, 1758 housefly wings downward on the center of each array.…”

Section: Methodsmentioning

confidence: 99%

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

Burba

Deva

et al. 2019

Ecology and Evolution

An orb web's adhesive capture spiral is responsible for prey retention. This thread is formed of regularly spaced glue droplets supported by two flagelliform axial lines. Each glue droplet features a glycoprotein adhesive core covered by a hygroscopic aqueous layer, which also covers axial lines between the droplets, making the entire thread responsive to environmental humidity. We characterized the effect of relative humidity (RH) on ability of Argiope aurantia and Argiope trifasciata thread arrays to retain houseflies and characterize the effect of humidity on their droplet properties. Using these data and those of Araneus marmoreus from a previous study, we then develop a regression model that correlated glycoprotein and flagelliform fiber properties with prey retention time. The model selection process included newly determined, humidity‐specific Young's modulus and toughness values for the three species' glycoproteins. Argiope aurantia droplets are more hygroscopic than A. trifasciata droplets, causing the glycoprotein within A. aurantia droplets to become oversaturated at RH greater than 55% RH and their extension to decrease, whereas A. trifasciata droplet performance increases to 72% RH. This difference is reflected in species' prey retention times, with that of A. aurantia peaking at 55% RH and that of A. trifasciata at 72% RH. Fly retention time was explained by a regression model of five variables: glue droplet distribution, flagelliform fiber work of extension, glycoprotein volume, glycoprotein thickness, and glycoprotein Young's modulus. The material properties of both glycoprotein and flagelliform fibers appear to be phylogenetically constrained, whereas natural selection can more freely act on the amount of each material invested in a thread and on components of the thread's aqueous layer. Thus, it becomes easier to understand how natural selection can tune the performance of viscous capture threads by directing small changes in these components.