journal article·2021-09

Humidity mediated performance and material properties of orb weaving spider adhesive droplets

Brent D. Opell, Hannah Mae Elmore, Mary L. Hendricks

Acta Biomaterialia· Volume 131
Publisher page

Abstract

Capture thread glue droplets retain insects that strike an orb web and are key to the success of over 4,600 described spider species. Each droplet is a self-assembling adhesive system whose emergent biomechanical properties are centered on its viscoelastic, protein core. This bioadhesive is dependent on its surrounding hygroscopic aqueous layer for hydration and chemical conditioning. Consequently, a droplet's water content and adhesive performance track environmental humidity. We tested the hypothesis that natural selection has tuned a droplet's adhesive performance and material properties to a species' foraging humidity. At 55% relative humidity (RH) the adhesive properties of 12 species ranged from that of PEG-based hydrogels to that of silicone rubber, exhibiting a 1088-fold inter-specific difference in stiffness (0.02-21.76 MPa) and a 147-fold difference in toughness (0.14-20.51 MJ/m3). When tested over a 70% RH range, droplet extension lengths per protein core volume peaked at lower humidities in species from exposed, low humidity habitats, and at higher humidities in nocturnal species and those found in humid habitats. However, at the RH's where these species' maximum extension per protein volume indices were observed, the stiffness of most species' adhesive did not differ, documenting that selection has tuned elastic modulus by adjusting droplet hygroscopicity. This inverse relationship between droplet hygroscopicity and a species' foraging humidity ensures optimal adhesive stiffness. By characterizing the humidity responsiveness and properties of orb spider glue droplets, our study also profiles the range of its biomimetic potential. STATEMENT OF SIGNIFICANCE: Over 4,600 described species of orb weaving spider rely on tiny glue droplets in their webs to retain insect that the web intercepts. The aqueous layer that covers each droplet's core allows this adhesive to remain pliable and to stretch as an insect struggles to escape. The aqueous solution also attracts water from the air, causing the glue droplet's performance to change with humidity. By characterizing the droplet extensions and adhesive material properties of twelve species at relative humidities between of 20 and 90%, this study examined how this unique adhesive system responds to its environment and how it is tuned to the humidity of a species' habitat.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Silk-based biomaterials and applications · Adhesion, Friction, and Surface Interactions · Insect and Arachnid Ecology and Behavior

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (54)

Show source-provided references
1. Grand challenges in soft matter physics10.3389/fphy.2018.00087 ↗
2. Viscoelastic solids explain spider web stickiness
3. Glycoprotein glue beneath a spider web's aqueous coat10.1007/BF01134447 ↗
4. Untangling spider silk evolution with spidroin terminal domains10.1186/1471-2148-10-243 ↗
5. Evidence from multiple species that spider silk glue component ASG2 is a spidroin10.1038/srep21589 ↗
6. Spider orb webs rely on radial threads to absorb prey energy
7. Damping capacity is evolutionarily conserved in the radial silk of orb-weaving spiders10.1016/j.zool.2011.02.001 ↗
8. Function and phylogeny of spider webs10.1146/annurev.es.21.110190.002013 ↗
9. Spinneret silk spigot morphology: Evidence for the monophyly of orb-weaving spiders, Cyrtophorinae (Araneidae), and the group Theridiidae plus Nesticidae
10. On a new spinning gland found in geometric spiders and its function
11. Über den spinnapparat von Nephila madagascariensis10.1515/znb-1955-0708 ↗
12. The contribution of atmospheric water vapour to the formation and efficiency of a spider's web10.1098/rspb.1992.0055 ↗
13. Compounds in the droplets of the orb spider's viscid spiral10.1038/345526a0 ↗
14. Protein composition and associated material properties of cobweb spiders’ gumfoot glue droplets10.1093/icb/icab086 ↗
15. Ubiquitous distribution of salts and proteins in spider glue enhances spider silk adhesion
16. Role of hygroscopic low molecular mass compounds in responsive adhesion of spiders capture silk10.1021/acs.biomac.8b00602 ↗
17. Aggregate Silk Gland Secretions of Araneoid Spiders
18. Adhesion modulation using glue droplet spreading in spider capture silk10.1098/rsif.2017.0228 ↗
19. Composition and function of spider glues maintained during the evolution of cobwebs10.1021/acs.biomac.5b01040 ↗
20. Guinea · Biomacromolecules · 2010 · 11 · 117410.1021/bm901285c ↗
21. Direct solvation of glycoproteins by salts in spider silk glues enhances adhesion and helps to explain the evolution of modern spider orb webs10.1021/bm401800y ↗
22. Comparative study of orb web hygroscopicity and adhesive spiral composition in three araneid spiders10.1002/jez.1402590203 ↗
23. Spiders tune glue viscosity to maximize adhesion10.1021/acsnano.5b05658 ↗
24. Orb weaver glycoprotein is a smart biological material, capable of repeated adhesion cycles10.1007/s00114-019-1607-z ↗
25. Tuning orb spider glycoprotein glue performance to habitat humidity10.1242/jeb.161539 ↗
26. The adhesive delivery system of viscous prey capture threads spin by orb-weaving spiders10.1242/jeb.030064 ↗
27. Synergistic adhesion mechanisms of spider capture silk
28. On the robustness of spider capture silk's adhesion10.1016/j.eml.2019.100477 ↗
29. Changes in the adhesive properties of spider aggregate glue during the evolution of cobwebs
30. Natural underwater adhesives10.1002/polb.22256 ↗
31. World Spider Catalog, World Spider Catalog v21.5. 2020 (accessed August 26, 2020).
32. Testing adaptive radiation and key innovation hypotheses in spiders10.1111/j.1558-5646.1998.tb01641.x ↗
33. Web forms and phylogeny of theridiid spiders (Araneae: Theridiidae)10.1017/S1477200008002855 ↗
34. Homology behaviour and spider webs: web construction behaviour of Linyphia hortensis and L. triangularis (Araneae: Linyphiidae) and its evolutionary significance10.1046/j.1420-9101.2004.00667.x ↗
35. Eberhard · 2020
36. The silk-producing system of Linyphia triangularis (Araneae, Linyphiidae) and some comparisons with Araneidae. Structure, histochemistry and function10.1007/BF01632706 ↗
37. Environmental response and adaptation of glycoprotein glue within the droplets of viscous prey capture threads from araneoid spider orb-webs
38. Linking properties of an orb weaving spider's capture thread glycoprotein adhesive and flagelliform fiber components to prey retention time
39. Rounding up the usual suspects: a standard target-gene approach for resolving the interfamilial phylogenetic relationships of ecribellate orb-weaving spiders with a new family-rank classification (Araneae, Araneoidea)10.1111/cla.12165 ↗
40. Elastic modulus and toughness of orb spider glycoprotein glue10.1371/journal.pone.0196972 ↗
41. Properties of orb weaving spider glycoprotein glue change during Argiope trifasciata web construction10.1038/s41598-019-56707-1 ↗
42. Image_J, Image J. http://www.uhnresearch.ca/facilities/wcif/imagej/, Bethesda, Maryland, U.S.A., 2006.
43. A re-evaluation of the formula to estimate the volume of orb web glue droplets10.1636/M14-50.1 ↗
44. Behavioral and biomaterial coevolution in spider orb webs10.1111/j.1420-9101.2010.02048.x ↗
45. In-drop capillary spooling of spider capture thread inspires hybrid fibers with mixed solid–liquid mechanical properties
46. In-drop capillary spooling of spider capture thread inspires hybrid fibers with mixed solid–liquid mechanical properties10.1073/pnas.1602451113 ↗
47. Silken toolkits: biomechanics of silk fibers spun by the orb web spider Argiope argentata (Fabricius 1775)10.1242/jeb.02275 ↗
48. Unraveling the mechanical properties of composite silk threads spun by cribellate orbweaving spiders10.1242/jeb.02327 ↗
49. Variation in the material properties of spider dragline silk across species10.1007/s00339-005-3427-6 ↗
50. Guinea · Biomacromolecules · 2010 · 11 · 117410.1021/bm901285c ↗
51. Mechanical performance of spider orb webs is tuned for high-speed prey10.1242/jeb.085571 ↗
52. Spider silk inspired functional microthreads10.1021/la203275x ↗
53. The complexity of silk under the spotlight of synthetic biology10.1042/BST20160058 ↗
54. Spider silk as a model biomaterial10.1007/s00339-005-3437-4 ↗