Distinct spinning patterns gain differentiated loading tolerance of silk thread anchorages in spiders with different ecology

Building behaviour in animals extends biological functions beyond bodies. Many studies have emphasized the role of behavioural programmes, physiology and extrinsic factors for the structure and function of buildings. Structure attachments associated with animal constructions offer yet unrealized research opportunities. Spiders build a variety of one- to three-dimensional structures from silk fibres. The evolution of economic web shapes as a key for ecological success in spiders has been related to the emergence of high performance silks and thread coating glues. However, the role of thread anchorages has been widely neglected in those models. Here, we show that orb-web (Araneidae) and hunting spiders (Sparassidae) use different silk application patterns that determine the structure and robustness of the joint in silk thread anchorages. Silk anchorages of orb-web spiders show a greater robustness against different loading situations, whereas the silk anchorages of hunting spiders have their highest pull-off resistance when loaded parallel to the substrate along the direction of dragline spinning. This suggests that the behavioural ‘printing' of silk into attachment discs along with spinneret morphology was a prerequisite for the evolution of extended silk use in a three-dimensional space. This highlights the ecological role of attachments in the evolution of animal architectures.

[1]  Erik Meijering,et al.  Methods for cell and particle tracking. , 2012, Methods in enzymology.

[2]  Ali Dhinojwala,et al.  Cobweb-weaving spiders produce different attachment discs for locomotion and prey capture , 2012, Nature Communications.

[3]  Jonathan A Coddington,et al.  Reconstructing web evolution and spider diversification in the molecular era , 2009, Proceedings of the National Academy of Sciences.

[4]  Jonas O. Wolff Structural effects of glue application in spiders-what can we learn from silk anchors? , 2017 .

[5]  Wolfgang Nentwig,et al.  The Great Silk Alternative: Multiple Co-Evolution of Web Loss and Sticky Hairs in Spiders , 2013, PloS one.

[6]  F. Rohlf,et al.  Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks , 1990 .

[7]  Ingi Agnarsson,et al.  Biomaterial evolution parallels behavioral innovation in the origin of orb-like spider webs , 2012, Scientific Reports.

[8]  M. Elgar,et al.  Foraging strategies of Eriophora transmarina and Nephila plumipes (Araneae: Araneoidea): Nocturnal and diurnal orb‐weaving spiders , 1994 .

[9]  F. Vollrath,et al.  The Role of Behavior in the Evolution of Spiders, Silks, and Webs , 2007 .

[10]  Jonas O. Wolff,et al.  Three-dimensional printing spiders: back-and-forth glue application yields silk anchorages with high pull-off resistance under varying loading situations , 2017, Journal of The Royal Society Interface.

[11]  B. J. Kaston THE EVOLUTION OF SPIDER WEBS , 1964 .

[12]  R. Foelix,et al.  The biology of spiders. , 1987 .

[13]  J. Deneubourg,et al.  Dragline Attachment Pattern in the Neotropical Social Spider Anelosimus eximius (Araneae: Theridiidae) , 1999, Journal of Insect Behavior.

[14]  B. Swanson,et al.  The evolution of complex biomaterial performance: The case of spider silk. , 2009, Integrative and comparative biology.

[15]  Joshua S Madin,et al.  High-performance spider webs: integrating biomechanics, ecology and behaviour , 2011, Journal of The Royal Society Interface.

[16]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[17]  J. Kovoor,et al.  Comparative Structure and Histochemistry of Silk-Producing Organs in Arachnids , 1987 .

[18]  Todd A Blackledge,et al.  Silken toolkits: biomechanics of silk fibers spun by the orb web spider Argiope argentata (Fabricius 1775) , 2006, Journal of Experimental Biology.

[19]  J. Coddington Spinneret Silk Spigot Morphology: Evidence for the Monophyly of Orbweaving Spiders, Cyrtophorinae (Araneidae), and the Group Theridiidae Plus Nesticidae , 1989 .

[20]  Stanislav N. Gorb,et al.  Composition and substrate-dependent strength of the silken attachment discs in spiders , 2014, Journal of The Royal Society Interface.

[21]  Fritz Vollrath,et al.  Liquid crystalline spinning of spider silk , 2001, Nature.

[22]  Kerstin Pingel,et al.  50 Years of Image Analysis , 2012 .

[23]  W. Eberhard Possible functional significance of spigot placement on the spinnerets of spiders , 2010 .

[24]  J. Coddington Phylogeny and Classification of Spiders , 2005 .

[25]  Jonas O. Wolff,et al.  Surface roughness effects on attachment ability of the spider Philodromus dispar (Araneae, Philodromidae) , 2012, Journal of Experimental Biology.

[26]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[27]  Stanislav N Gorb,et al.  Adhesive foot pads: an adaptation to climbing? An ecological survey in hunting spiders. , 2015, Zoology.

[28]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[29]  Jonas O. Wolff,et al.  Spider's super-glue: thread anchors are composite adhesives with synergistic hierarchical organization. , 2015, Soft matter.

[30]  Jonas O. Wolff,et al.  Hunting Without a Web: How Lycosoid Spiders Subdue their Prey , 2015 .