Orb weavers produce webs that trap prey using a capture spiral formed of regularly spaced glue droplets supported by protein fibers. Each droplet consists of an outer aqueous layer and an adhesive, viscoelastic glycoprotein core. Organic and inorganic compounds in the aqueous layer make droplets hygroscopic and cause droplet features to change with environmental humidity. When droplets contact a surface, they adhere and extend as an insect struggles. Thus, a droplet’s extensibility is as important for prey capture as its adhesion. Cursory observations show that droplets can adhere, extend, and pull off from a surface several times, a process called cycling. Our study cycled individual droplets of four species—Argiope aurantia, Neoscona crucifera, Verrucosa arenata, and Larinioides cornutus. Droplets were subjected to 40 cycles at two humidities to determine how humidity affected droplet performance. We hypothesized that droplets would continue to perform, but that performance would decrease. Droplet performance was characterized by filament length and force on droplets at pull-off, aqueous volume, and glycoprotein volume. As hypothesized, cycling decreased performance, notably extensibility and aqueous volume. However, humidity did not impact the response to cycling. In a natural context, droplets are not subjected to extensive cycling, but reusability is advantageous for orb-weaving spiders. Moreover, the ability to cycle, combined with their environmental responsiveness, allows us to characterize orb weaver droplets as smart materials for the first time.
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Adhesive contact and protein elastic modulus tune orb weaving spider glue droplet biomechanics to habitat humidity
Tiny glue droplets along the viscous capture threads of spider orb webs prevent insects from escaping. Each droplet is formed of a protein core surrounded by a hygroscopic aqueous layer, which cause
the droplet’s adhesion to change with humidity. As an insect struggles to escape the web, a thread’s
viscoelastic core proteins extend, transferring adhesive forces to the thread’s support fibers. Maximum
adhesive force is achieved when absorbed atmospheric moisture allows a flattened droplet to establish
sufficient adhesive contact while maintaining the core protein cohesion necessary for force transfer. We
examined the relationship between these droplet properties and adhesive force and the work of extending droplets at five relative humidities in twelve species that occupy habitats which have different humidities. A regression analysis that included both flattened droplet area and core protein elastic modulus
described droplet adhesion, but the model was degraded when core protein area was substituted for
droplet. Species from low humidity habitats expressed greater adhesion at lower humidities, whereas
species from high humidity habitats expressed greater adhesion at high humidities. Our results suggest a
general model of droplet adhesion with two adhesion peaks, one for low humidity species, which occurs
when increasing droplet area and decreasing protein cohesion intersect, and another for high humidity
species, which occurs when area and cohesion have diverged maximally. These dual peaks in adhesive
force explain why some species from intermediate and high humidity habitats express high adhesion at
several humidities.
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- Award ID(s):
- 1755028
- NSF-PAR ID:
- 10473506
- Publisher / Repository:
- Acta Biomaterialia
- Date Published:
- Journal Name:
- Acta Biomaterialia
- Volume:
- 151
- Issue:
- C
- ISSN:
- 1742-7061
- Page Range / eLocation ID:
- 468 to 479
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1016/j.actbio.2022.08.018
