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Limits of piriform silk adhesion—similar effects of substrate surface polarity on silk anchor performance in two spider species with disparate microhabitat use

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Abstract

It has been suggested that physical interactions between biological and environmental surfaces may constrain ecological niche spaces. However, the mechanistic understanding of niche formation is frequently limited by the lack of information on the function and variation of these interactions. Here, we hypothesised that two closely related species of orb-web spiders have evolved different adhesion performance of web attachment (i.e. piriform silk) facilitating the occupation of contrasting microhabitats: plants versus rocks. Contrary to our prediction, we found that piriform silk adhesion was equally affected by surface chemistry in both species, with maximal adhesion on surfaces with high surface polarity and an average adhesion loss of 70–75% on low polar surfaces. Spiders did not respond to adhesion losses by increasing the anchor size, despite the repeated failure to attach their web to low polar surfaces. In a natural setting, poor adhesion on low polar surfaces may be mitigated by behavioural means, like the preference to place anchors on corrugated surface features such as leaf edges, or the spinning of multiple anchorages and formation of a bundled anchor line. Thus, microhabitat choice for web-building spiders may be governed by structural properties rather than surface chemistry. These results suggest that the repeatedly demonstrated effects of surface chemistry on bio-adhesion may be ecologically less important than assumed and that the role of behaviour in the evolution of bio-adhesion performance has been underestimated.

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References

  • Afferrante L, Carbone G (2016) The ultratough peeling of elastic tapes from viscoelastic substrates. J Mech Phys Solids 96:223–234

    Article  Google Scholar 

  • Amarpuri G, Zhang C, Diaz C, Opell BD, Blackledge TA, Dhinojwala A (2015) Spiders tune glue viscosity to maximize adhesion. ACS Nano 9:11472–11478

    Article  PubMed  CAS  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Berglin M, Gatenholm P (1999) The nature of bioadhesive bonding between barnacles and fouling-release silicone coatings. J Adhes Sci Technol 13:713–727

    Article  CAS  Google Scholar 

  • Betz O, Kölsch G (2004) The role of adhesion in prey capture and predator defence in arthropods. Arthropod Struct Dev 33:3–30

    Article  PubMed  Google Scholar 

  • Bhushan B, Wyant JC, Koliopoulos CL (1985) Measurement of surface topography of magnetic tapes by Mirau interferometry. Appl Opt 24:1489–1497

    Article  PubMed  CAS  Google Scholar 

  • Brau F, Lanterbecq D, Zghikh L-N, Bels V, Damman P (2016) Dynamics of prey prehension by chameleons through viscous adhesion. Nat Phys 12:931–935

    Article  CAS  Google Scholar 

  • Callow ME, Fletcher RL (1994) The influence of low surface energy materials on bioadhesion—a review. Int Biodeterior Biodegrad 34:333–348

    Article  CAS  Google Scholar 

  • Crawford N, Endlein T, Pham JT, Riehle M, Barnes WJP (2016) When the going gets rough–studying the effect of surface roughness on the adhesive abilities of tree frogs. Beilstein J Nanotechnol 7:2116–2131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Crisp D, Walker G, Young G, Yule A (1985) Adhesion and substrate choice in mussels and barnacles. J Colloid Interface Sci 104:40–50

    Article  Google Scholar 

  • De Groot PJ (1995) Derivation of algorithms for phase-shifting interferometry using the concept of a data-sampling window. Appl Opt 34:4723–4730

    Article  PubMed  CAS  Google Scholar 

  • Eisner T, Aneshansley DJ (2000) Defense by foot adhesion in a beetle (Hemisphaerota cyanea). Proc Natl Acad Sci 97:6568–6573

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • England MW, Sato T, Yagihashi M, Hozumi A, Gorb SN, Gorb EV (2016) Surface roughness rather than surface chemistry essentially affects insect adhesion. Beilstein J Nanotechnol 7:1471–1479

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Federle W, Rohrseitz K, Holldobler B (2000) Attachment forces of ants measured with a centrifuge: better ‘wax-runners’ have a poorer attachment to a smooth surface. J Exp Biol 203:505–512

    Article  PubMed  CAS  Google Scholar 

  • Gorb S (2001) Attachment devices of insect cuticle. Springer Science & Business Media, Dordrecht

    Google Scholar 

  • Grawe I, Wolff JO, Gorb SN (2014) Composition and substrate-dependent strength of the silken attachment discs in spiders. J R Soc Interface 11:1742–5662

    Article  Google Scholar 

  • Grohmann C, Blankenstein A, Koops S, Gorb SN (2014) Attachment of Galerucella nymphaeae (Coleoptera, Chrysomelidae) to surfaces with different surface energy. J Exp Biol 217:4213–4220

    PubMed  Google Scholar 

  • Hansell MH (2005) Animal architecture. Oxford University Press, New York

    Book  Google Scholar 

  • Heepe L, Petersen DS, Tölle L, Wolff JO, Gorb SN (2017) Sexual dimorphism in the attachment ability of the ladybird beetle Coccinella septempunctata on soft substrates. Appl Phys A Mater Sci Process 123:34

    Article  CAS  Google Scholar 

  • Heepe L, Wolff JO, Gorb SN (2016) Influence of ambient humidity on the attachment ability of ladybird beetles (Coccinella septempunctata). Beilstein J Nanotechnol 7:1322–1329

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Herberstein ME (2000) Foraging behaviour in orb-web spiders (Araneidae): do web decorations increase prey capture success in Argiope keyserlingi Karsch, 1878? Aust J Zool 48:217–223

    Article  Google Scholar 

  • Hesselberg T (2013) Web-building flexibility differs in two spatially constrained orb spiders. J Insect Behav 26:283–303

    Article  Google Scholar 

  • Huber G, Mantz H, Spolenak R, Mecke K, Jacobs K, Gorb SN, Arzt E (2005) Evidence for capillarity contributions to gecko adhesion from single spatula nanomechanical measurements. Proc Natl Acad Sci 102:16293–16296

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kendall K (1975) Thin-film peeling—elastic term. J Phys D Appl Phys 8:1449–1452

    Article  Google Scholar 

  • Lenth R, Singmann H, Love J, Buerkner P, Herve M (2018) Emmeans: estimated marginal means, aka least-squares means, R package version 1.1. https://cran.r-project.org/package=emmeans

  • Niewiarowski PH, Lopez S, Ge L, Hagan E, Dhinojwala A (2008) Sticky gecko feet: the role of temperature and humidity. PLoS One 3:e2192

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Opell B (1998) Economics of spider orb-webs: the benefits of producing adhesive capture thread and of recycling silk. Funct Ecol 12:613–624

    Article  Google Scholar 

  • Piorkowski D, Blackledge T, Liao CP, Doran N, Wu CL, Blamires S, Tso IM (2018) Humidity-dependent mechanical and adhesive properties of Arachnocampa tasmaniensis capture threads. J Zool 305:256–266

    Article  Google Scholar 

  • Pugno NM (2011) The theory of multiple peeling. Int J Fract 171:185–193

    Article  Google Scholar 

  • Pugno NM, Cranford S, Buehler MJ (2013) Synergetic material and structural optimization yields robust spider web anchorages. Small 9:2747–2756

    Article  PubMed  CAS  Google Scholar 

  • Puthoff JB, Prowse MS, Wilkinson M, Autumn K (2010) Changes in materials properties explain the effects of humidity on gecko adhesion. J Exp Biol 213:3699–3704

    Article  PubMed  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/

  • Rao D, Cheng K, Herberstein ME (2007) A natural history of web decorations in the St. Andrew’s Cross spider (Argiope keyserlingi). Aust J Zool 55:9–14

    Article  Google Scholar 

  • Sahni V, Harris J, Blackledge TA, Dhinojwala A (2012) Cobweb-weaving spiders produce different attachment discs for locomotion and prey capture. Nat Commun 3:1–7

    Article  CAS  Google Scholar 

  • Schnee L, Sampalla B, Müller JK, Betz O (2019) A comparison of tarsal morphology and traction force in the two burying beetles Nicrophorus nepalensis and Nicrophorus vespilloides (Coleoptera, Silphidae). Beilstein J Nanotechnol 10:47–61

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Searle SR, Speed FM, Milliken GA (1980) Population marginal means in the linear model: an alternative to least squares means. Am Stat 34:216–221

    Google Scholar 

  • Shin D, Choi WT, Lin H, Qu Z, Breedveld V, Meredith JC (2019) Humidity-tolerant rate-dependent capillary viscous adhesion of bee-collected pollen fluids. Nat Commun 10:1379

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stalder AF, Kulik G, Sage D, Barbieri L, Hoffmann P (2006) A snake-based approach to accurate determination of both contact points and contact angles. Colloids Surf A Physicochem Eng Asp 286:92–103

    Article  CAS  Google Scholar 

  • Voigt D, de Souza E, Kovalev A, Gorb S (2019) Inter-and intraspecific differences in leaf beetle attachment on rigid and compliant substrates. J Zool 307:1–8

    Article  Google Scholar 

  • von Byern J et al (2019) Biomechanical properties of fishing lines of the glowworm Arachnocampa luminosa (Diptera; Keroplatidae). Sci Rep 9:1–14

    Google Scholar 

  • von Byern J, Grunwald I (2010) Biological adhesive systems: from nature to technical and medical application. Springer, Vienna

    Book  Google Scholar 

  • Walter A, Elgar MA (2016) Signal polymorphism under a constant environment: the odd cross in a web decorating spider. Sci Nat 103:93

    Article  CAS  Google Scholar 

  • Whitney HM, Federle W (2013) Biomechanics of plant-insect interactions. Curr Opin Plant Biol 16:105–111

    Article  PubMed  Google Scholar 

  • Wirth M, Wolff JO, Appel E, Gorb SN (2019) Ultrastructure of spider thread anchorages. J Morphol 280:534–543

    Article  PubMed  Google Scholar 

  • Wolff JO (2017) Structural effects of glue application in spiders—what can we learn from silk anchors? In: Xue L, Heepe L, Gorb SN (eds) Bio-inspired structured adhesives. NanoScience and Technology. Springer Science+Business Media, Dordrecht, pp 63–80

    Chapter  Google Scholar 

  • Wolff JO, García-Hernández S, Gorb SN (2016) Adhesive secretions in harvestmen (Arachnida: Opiliones). In: Smith AM, Callows JA (eds) Biological adhesives. Springer, Cham, pp 281–301

    Chapter  Google Scholar 

  • Wolff JO, Gorb SN (2011) The influence of humidity on the attachment ability of the spider Philodromus dispar (Araneae, Philodromidae). Proc R Soc B 279:139–143

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolff JO, Gorb SN (2012) Surface roughness effects on attachment ability of the spider Philodromus dispar (Araneae, Philodromidae). J Exp Biol 215:179–184

    Article  PubMed  Google Scholar 

  • Wolff JO, Gorb SN (2016) Attachment structures and adhesive secretions in arachnids. Biologically-inspired systems. Springer, Cham

    Book  Google Scholar 

  • Wolff JO, Grawe I, Wirth M, Karstedt A, Gorb SN (2015a) Spider's super-glue: thread anchors are composite adhesives with synergistic hierarchical organization. Soft Matter 11:2394–2403

    Article  PubMed  CAS  Google Scholar 

  • Wolff JO, Herberstein ME (2017) 3D-printing spiders: back-and-forth glue application yields silk anchorages with high pull-off resistance under varying loading situations. J R Soc Interface 14:20160783

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolff JO, Huber SJ, Gorb SN (2015b) How to stay on mummy's back: morphological and functional changes of the pretarsus in arachnid postembryonic stages. Arthropod Struct Dev 44:301–312

    Article  PubMed  Google Scholar 

  • Wolff JO, Jones B, Herberstein ME (2018) Plastic material investment in load-bearing silk attachments in spiders. Zoology 131:45–47

    Article  PubMed  Google Scholar 

  • Wolff JO, Lovtsova J, Gorb E, Dai Z, Ji A, Zhao Z, Jiang N, Gorb SN (2017a) Strength of silk attachment to Ilex chinensis leaves in the tea bagworm Eumeta minuscula (Lepidoptera, Psychidae). J R Soc Interface 14:20170007

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolff JO, Paterno GB, Liprandi D, Ramírez MJ, Bosia F, Meijden A, Michalik P, Smith HM, Jones BR, Ravelo AM, Pugno N, Herberstein ME (2019) Evolution of aerial spider webs coincided with repeated structural optimization of silk anchorages. Evolution 73:2122–2134

    Article  PubMed  Google Scholar 

  • Wolff JO, Řezáč M, Krejčí T, Gorb SN (2017b) Hunting with sticky tape: functional shift in silk glands of araneophagous ground spiders (Gnaphosidae). J Exp Biol 220:2250–2259

    Article  PubMed  Google Scholar 

  • Wolff JO, Schönhofer AL, Schaber CF, Gorb SN (2014) Gluing the ‘unwettable’: soil-dwelling harvestmen use viscoelastic fluids for capturing springtails. J Exp Biol 217:3535–3544

    Article  PubMed  Google Scholar 

  • Wolff JO, van der Meijden A, Herberstein ME (2017c) Distinct spinning patterns gain differentiated loading tolerance of silk thread anchorages in spiders with different ecology. Proc R Soc B 284:20171124

    Article  PubMed  PubMed Central  Google Scholar 

  • Zschokke S, Herberstein ME (2005) Laboratory methods for maintaining and studying web-building spiders. J Arachnol 33:205–213

    Article  Google Scholar 

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Acknowledgements

Thanks to Alan Henderson (Minibeasts Wildlife, Kuranda, QLD) for providing A. mascordi individuals and to André Walter (Aarhus University) for providing habitat photos and observational details of A. mascordi.

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Raw data are deposited in the electronic supplemental material.

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Funding

This study was supported by a Macquarie Research Fellowship of Macquarie University and a Discovery Early Career Researcher Award of the Australian Research Council (DE190101338) to JOW.

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Authors and Affiliations

  1. Department of Biological Sciences, Macquarie University, Sydney, NSW, 2109, Australia

    Jonas O. Wolff & Marie E. Herberstein

  2. MQ Photonics Research Centre, Department of Physics and Astronomy, Macquarie University, Sydney, NSW, 2109, Australia

    Douglas Little

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  1. Jonas O. Wolff
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Contributions

JOW and MEH conceived and designed the study. JOW performed the experiments and analysed the data. DL performed the profilometric measurements of substrate surfaces. JOW wrote the paper and all other authors equally contributed in revision.

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Correspondence to Jonas O. Wolff.

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The authors declare that they have no competing interests.

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All applicable international and national guidelines for the care and use of animals were followed.

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Communicated by: Matjaž Gregorič

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ESM 1

Individual pull-off force data (CSV 3 kb)

ESM 2

Individual anchor measurements (CSV 8 kb)

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Wolff, J.O., Little, D. & Herberstein, M.E. Limits of piriform silk adhesion—similar effects of substrate surface polarity on silk anchor performance in two spider species with disparate microhabitat use. Sci Nat 107, 31 (2020). https://doi.org/10.1007/s00114-020-01687-w

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  • DOI: https://doi.org/10.1007/s00114-020-01687-w

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