The function of the pad secretion in insects

Lead Research Organisation: Imperial College London
Department Name: Dept of Bioengineering

Abstract

The sticky pads on the feet of arthropods outperform man-made adhesives in several aspects: they can be controlled on short time-scales, survive thousands of usage cycles without a decline in performance, work on rough and wet surfaces, and regain functionality after contamination. Understanding the structure-function relationship of these pads hence promises to reveal effective strategies for the design of technical adhesives with novel properties. A hallmark of arthropod adhesives is that they are "wet" - the contact between the soft footpads and a surface is mediated by nano-metre thin films of an oily secretion. Despite its discovery almost 200 years ago, the function of this fluid is still unclear, and recent experiments have suggested that the adhesive performance of the pads may be dominated by the properties of the solid footpad itself, reigniting the debate about the fluid's function - why do insects secrete this fluid? Does it serve as a protective layer against wear, or does it prevent dehydration of the pad itself, which would result in an increased pad stiffness, and hence reduced adaptability to rough surfaces? Others have argued that the fluid is crucial for the control of attachment forces: it may serve as a "release layer" which ensures that fast voluntary detachment can be performed with ease, but that strong attachment occurs when the fluid is depleted from the contact zone during the fast sliding events that accompany forced detachment. In this project, we address these hypotheses by quantifying the relevant physical properties of both the footpads and the adhesive secretion in separate experiments: the viscoelastic properties of the attachment pads will be quantified using indentation and state-of-the-art viscoelastic modelling, while the viscosity and surface tension of the pad secretion will be measured with a combination of dewetting experiments and contact angle measurements. The obtained information will then be used to construct and inform mathematical models which will allow us to predict the pads' adhesive performance. By comparing these theoretical predictions to experimental data on the rate-dependence of the adhesion of the biological adhesive pads in the absence and presence of the pad secretion, we will be able to separate the contribution of both the fluid and the pad viscoelasticity to the observed adhesive performance, and thereby increase our understanding of the functional significance of the pad secretion. Our study will hence not only help to solve a centuries-old puzzle, provide new fundamental insights into the mechanical coupling between soft solids and thin liquid films, but importantly yield results relevant for the design of novel man-made adhesives which successfully replicate some of the most outstanding performance characteristics of dynamic biological adhesives.

Technical Summary

Dynamic biological adhesives, such as the footpads of insects, promise to provide inspiration for the design of novel synthetic adhesives. However, despite several ingenious attempts to produce powerful bio-inspired adhesives, the performance of the biological "originals" has not been remotely matched. One reason for this discrepancy is a lack of understanding of the key structure-function relationships, arising from the small number of studies investigating the fundamental properties of the biological adhesives themselves. In this project, we will address one of the hallmarks of insect adhesives - the presence of a contact-mediating fluid. The function of this fluid is still unclear, and will be investigated by quantifying (i) the rate-dependence of adhesion of single attachment pads in the presence and absence of the pad secretion, (ii) the viscoelastic properties of the pad cuticle via indentation and state-of-the-art viscoelastic modelling and (iii) the surface tension and viscosity of the secretion itself, using a combination of contact angle measurements and dewetting experiments on surfaces with varying surface energy. These results will be combined with analytical modelling of the rate-dependence of these "wet" and soft adhesives, in order to quantify the relative contributions of the secretion and the soft footpads to the adhesive performance, and to clarify the functional significance of the pad secretion in insects.

Planned Impact

The potential economic impact of powerful and effective bio-inspired adhesives is significant, and includes diverse applications in small-scale assembly processes, medical applications and climbing robots. As a consequence, many groups worldwide are currently attempting to mimic animal adhesive organs, but these efforts are often limited by a lack of understanding of the basic functional principles of the structures to be reconstructed. Insects are arguably the most diverse potential source of inspiration, but the presence of a secretion, allegedly crucial for adhesive performance, has held some researchers back, as technical adhesives which leave residues are undesirable. By clarifying the function of this pad secretion we seek to provide new insights into the functional design of insect adhesives, which will be relevant for the improvement of technical adhesives through novel, bio-inspired approaches. The insights gained from this project may not only help to design bio-inspired adhesives, but also reveal novel strategies for the development of insect-repellent coatings for pest control. Previous work has indicated that selective absorption of the pad secretion can reduce the attachment performance of insects, suggesting that non-toxic insect-repellent coatings are feasible. Understanding the functional significance of the secretion will allow a more targeted design of such coatings, and the basic research conducted in this project will push this important field through Technology Readiness Level 1. It is anticipated that following the success of this project, translational grant funding such as from the BBSRC Follow-on Fund or Innovate UK will be sought to develop bio-inspired adhesives either directly through this group or in conjunction with industry partners. To this end, the communication channels of industry bodies relevant to the area will be targeted, for example the Advanced Materials Leadership Council and the Society for Adhesion and Adhesives (part of IOM3).

In addition to reports targeted at academic and industrial partners, this work will be shared with the general public via internet, social and print media (blog posts, tweets, etc), as well as via dedicated outreach efforts in schools; the PI has considerable experience with outreach, as indicated by the high average altmetric score of the majority of the previous publications (within 5% of the top scores), coverage of his work by major news outlets (BBC, The Daily Mail), interviews with high-profile podcasts such as "The Naked Scientist" and consulting work for an upcoming BBC documentary on the importance of body size.

Publications

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Federle W (2019) Dynamic biological adhesion: mechanisms for controlling attachment during locomotion. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

 
Description Collaboration with Daniele Liprandi from the University of Trento 
Organisation European Cooperation in Science and Technology (COST)
Country Belgium 
Sector Public 
PI Contribution The collaboration was first discussed while attending the COST Workshop on Advances in Numerical Modelling of Adhesion (18-19/11/2019). The project was suggested by Dr David Labonte and it was decided for our group to host Daniele in April 2020. During his stay, we will revise the data we have already collected on a wide range of biological adhesive systems and assess which experiments could be reproduced in simulations. Daniele will then perform some preliminary simulations and further discussions will follow on how to pair our fields of expertise for a multi-technique analysis.
Collaborator Contribution In the past 15 years, biological adhesives have been widely studied as promising role models for the improvement of man-made adhesives. The term "smart adhesion" has been introduced to describe the amazing adhesive properties common to different species of animals and plants. Despite this phylogenetic diversity, there are some unifying principles shared by all biological adhesive pads used for locomotion. For example, controllability of attachment is achieved via direction-dependence of adhesive performance. Independently of pad size, pad morphology and the alleged adhesive mechanisms, the adhesive force appears to depend approximately linearly on the applied shear force. However, the detailed underlying mechanisms, e.g. how sliding and pre-straining are exploited by the animals, remain largely unclear and requires the development of new contact/tribology models. A key limitation of the models available in the literature is that they are only valid for one- or two-dimensional adhesion problems, solved using a variety of techniques which are mostly based on fundamental contact mechanics, i.e. the JKR, DMT, Kendall models and their extensions. While a number of articles address the interaction between adhesion and friction theoretically, few articles analysed three-dimensional problems. However, real adhesive contacts are 3-dimensional, and 3D modelling of adhesives is therefore highly relevant for uncovering the biomechanics of shear-sensitive adhesion. In order to fill these gaps and contribute to the understanding of the behaviour of biological adhesive structures, a comprehensive mechanical analysis is to be performed: phenomena like sliding and pre-straining must be included in a new three-dimensional adhesive model, which should be validated by experimental results. Daniele Liprandi from the University of Trento (supervised by Prof Nicola Pugno and Dr Federico Bosia) will visit our lab in April 2020 and with our help he will improve the three-dimensional model that he has previously developed by implementing the new required physical features. We will also study the geometrical properties of biological "membranes", focusing on how hierarchy and shape of the structures influence the controllability of adhesion.
Impact No outputs have resulted as of yet.
Start Year 2019
 
Description Collaboration with Daniele Liprandi from the University of Trento 
Organisation University of Trento
Country Italy 
Sector Academic/University 
PI Contribution The collaboration was first discussed while attending the COST Workshop on Advances in Numerical Modelling of Adhesion (18-19/11/2019). The project was suggested by Dr David Labonte and it was decided for our group to host Daniele in April 2020. During his stay, we will revise the data we have already collected on a wide range of biological adhesive systems and assess which experiments could be reproduced in simulations. Daniele will then perform some preliminary simulations and further discussions will follow on how to pair our fields of expertise for a multi-technique analysis.
Collaborator Contribution In the past 15 years, biological adhesives have been widely studied as promising role models for the improvement of man-made adhesives. The term "smart adhesion" has been introduced to describe the amazing adhesive properties common to different species of animals and plants. Despite this phylogenetic diversity, there are some unifying principles shared by all biological adhesive pads used for locomotion. For example, controllability of attachment is achieved via direction-dependence of adhesive performance. Independently of pad size, pad morphology and the alleged adhesive mechanisms, the adhesive force appears to depend approximately linearly on the applied shear force. However, the detailed underlying mechanisms, e.g. how sliding and pre-straining are exploited by the animals, remain largely unclear and requires the development of new contact/tribology models. A key limitation of the models available in the literature is that they are only valid for one- or two-dimensional adhesion problems, solved using a variety of techniques which are mostly based on fundamental contact mechanics, i.e. the JKR, DMT, Kendall models and their extensions. While a number of articles address the interaction between adhesion and friction theoretically, few articles analysed three-dimensional problems. However, real adhesive contacts are 3-dimensional, and 3D modelling of adhesives is therefore highly relevant for uncovering the biomechanics of shear-sensitive adhesion. In order to fill these gaps and contribute to the understanding of the behaviour of biological adhesive structures, a comprehensive mechanical analysis is to be performed: phenomena like sliding and pre-straining must be included in a new three-dimensional adhesive model, which should be validated by experimental results. Daniele Liprandi from the University of Trento (supervised by Prof Nicola Pugno and Dr Federico Bosia) will visit our lab in April 2020 and with our help he will improve the three-dimensional model that he has previously developed by implementing the new required physical features. We will also study the geometrical properties of biological "membranes", focusing on how hierarchy and shape of the structures influence the controllability of adhesion.
Impact No outputs have resulted as of yet.
Start Year 2019
 
Description Collaboration with Dr. Aurélie Levillain 
Organisation Imperial College London
Department Department of Bioengineering
Country United Kingdom 
Sector Academic/University 
PI Contribution Dr Levillain, a postdoctoral researcher at the Nowlan group, was researching the effect of mechanical stimuli in vertebral development in mice. As part of this research, nanomechanical characterisation of the spine tissue was required, an experimental need that matched the capabilities of the Chiaro nanoindenter purchased with the funds of this grant. D-M. Kaimaki actively contributed to the experimental design and collection of data to mechanically characterise the spine tissue and together with Dr. Labonte, they contributed to the data analysis and the preparation of the resulting manuscript.
Collaborator Contribution Dr. Levillain and Dr. Nowlan conceived of the study, with Dr. Levillain performing the majority of the experimental work involving techniques such as cryosectioning, histology and immunofluorescence. Dr. Levillain also wrote the manuscript and presented the work in a scientific conference.
Impact Publication 1. A. Levillain, S. Ahmed, D-M. Kaimaki, S. Schuler, S. Barros, D. Labonte, J.C. Iatridis, N.C. Nowlan, Prenatal muscle forces are necessary for vertebral segmentation and disc structure, but not for notochord involution in mice (accepted for publication in eCells & Materials journal on 28/02/2021) Conference presentation 1. Orthopedic Research Society, February 2021
Start Year 2019
 
Description Collaboration with the Polymer Science group at the University of Groningen 
Organisation European Cooperation in Science and Technology (COST)
Country Belgium 
Sector Public 
PI Contribution Dr. Domna-Maria Kaimaki completed two research stays at the Zernike Institute of Advanced Materials of the University of Groningen (March 2019, September 2019). During her first visit she devised a protocol to functionalise glass coverslips with silanes so that they remain transparent and smooth while their wettability is varied. The expertise and equipment of the Polymer Group were utilised by Domna-Maria to produce and characterise 10 surfaces for each of 5 silanes covering a range of water contact angles from 10-110 degrees. The produced surfaces were brought back to Imperial College London and were used to extract the surface tension of the insect secretion. During her second stay, Domna-Maria further optimised the research protocol and performed similar experiments to functionalise ITO-coated glass coverslips since the control of the surface temperature via Joule heating was desired to quantify the effect of temperature of the viscosity of the insect secretion. Apart from performing experiments at the University of Groningen, Domna-Maria also used her expertise in nanoindentation to attempt mechanical characterisation of complex coacervate samples brought by Prof Marleen Kamperman and her student, Larissa van Westervelt during a research stay at Imperial College London (April 2019).
Collaborator Contribution Prof Marleen Kamperman hosted Dr Domna-Maria Kaimaki at the Zernike Institute of Advanced Materials in Groningen. Her contribution as a host comprised: 1. Advice on the selection of silanes for the chemical functionalisation of surfaces to create smooth substrates of varying wettability. 2. Access to equipment (Schlenk line for Chemical Vapour Deposition, and goniometer and an AFM for surface characterisation). 3. Purchasing of the chemicals required and the 3D printing materials as well as general support from a Polymer Science group technician (Dr Peter Dijkstra).
Impact Output - Poster presented at the Gordon Conference on the Science of Adhesion (July 2019). - Posters presented at the Society of Integrative and Comparative Biology (SICB) Conference (January 2020, posters by Dr Domna-Maria Kaimaki & Andrea Attipoe). The collaboration is at the interface of chemistry and engineering.
Start Year 2019
 
Description Collaboration with the Polymer Science group at the University of Groningen 
Organisation University of Groningen
Country Netherlands 
Sector Academic/University 
PI Contribution Dr. Domna-Maria Kaimaki completed two research stays at the Zernike Institute of Advanced Materials of the University of Groningen (March 2019, September 2019). During her first visit she devised a protocol to functionalise glass coverslips with silanes so that they remain transparent and smooth while their wettability is varied. The expertise and equipment of the Polymer Group were utilised by Domna-Maria to produce and characterise 10 surfaces for each of 5 silanes covering a range of water contact angles from 10-110 degrees. The produced surfaces were brought back to Imperial College London and were used to extract the surface tension of the insect secretion. During her second stay, Domna-Maria further optimised the research protocol and performed similar experiments to functionalise ITO-coated glass coverslips since the control of the surface temperature via Joule heating was desired to quantify the effect of temperature of the viscosity of the insect secretion. Apart from performing experiments at the University of Groningen, Domna-Maria also used her expertise in nanoindentation to attempt mechanical characterisation of complex coacervate samples brought by Prof Marleen Kamperman and her student, Larissa van Westervelt during a research stay at Imperial College London (April 2019).
Collaborator Contribution Prof Marleen Kamperman hosted Dr Domna-Maria Kaimaki at the Zernike Institute of Advanced Materials in Groningen. Her contribution as a host comprised: 1. Advice on the selection of silanes for the chemical functionalisation of surfaces to create smooth substrates of varying wettability. 2. Access to equipment (Schlenk line for Chemical Vapour Deposition, and goniometer and an AFM for surface characterisation). 3. Purchasing of the chemicals required and the 3D printing materials as well as general support from a Polymer Science group technician (Dr Peter Dijkstra).
Impact Output - Poster presented at the Gordon Conference on the Science of Adhesion (July 2019). - Posters presented at the Society of Integrative and Comparative Biology (SICB) Conference (January 2020, posters by Dr Domna-Maria Kaimaki & Andrea Attipoe). The collaboration is at the interface of chemistry and engineering.
Start Year 2019
 
Description "A day in the life of" instagram story focused around the research work and experience of Andrea Attipoe 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact Andrea Attipoe was invited by Imperial's Bioengineering society to take part in their series "A day in the life of". The outreach event consisted in an Instagram takeover, during which Andrea took the students through a typical day as a PhD student in the Bioengineering department, showcasing teaching, the lab facilities and atmosphere and the subject of his research. The series of stories (still available in the highlights of the @icl_bgsoc Instagram page) received extremely positive feedback from the page's 400 followers.
Year(s) Of Engagement Activity 2021
URL https://instagram.com/icl_bgsoc?igshid=53nllk3ejzxe
 
Description Laboratory visit by bachelor students from the Aperture Maastricht Science Program in the Netherlands 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact 60 bachelor students from the Faculty of Engineering of Maastricht University visited the Department of Bioengineering on 06/06/2019 and were guided through the research performed in our lab as well as the Neuromechanics & Bioinspired Technologies Lab (PI:Dr Huai-Ti Lin). Our lab showcased work on: 1. the adhesion of insects and more specifically on the determination of the insect secretion's surface tension using Interference Reflection Microscopy and 2. the conduction of bite force measurements using a custom-built sensor so as to quantify the peak force leaf-cutter ants can apply to cut leaves. The bachelor students were very engaged during the activity requesting further information on our current and future work. In addition, one of the participating students later got in touch with us asking for opportunities to conduct research in our group.
Year(s) Of Engagement Activity 2019
 
Description Year 9 Girls Engineering Summer School 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact 60 girls from year 9 visited Imperial on 29/08/2019 to participate in an engineering summer school intended to inspire the next generation of women in STEM. The day was coordinated by the outreach office of the Department of Bioengineering and the girls were split in four groups to attend different activities. Our group organised an outreach activity similar to an escape room called "Outsmarting the insects". The 15 students that we hosted at each session were split into 4 groups and allocated to 4 stations. Each stations introduced a scientific problem and they were given 10 mins to complete a related activity and gather points. Once all teams had attended all stations, a short discussion on how bioengineering research can address such questions followed and the team with the highest score was presented with a laser-cut trophy. The stations included tasks such as: 1. Match the body parts of insects with their function, 2. Can you estimate weight better than a computer?, 3. Can you build the strongest glue? and 4. Can you cut faster than a leaf-cutter ant?, covering the whole range of the research performed at our lab. The activities were mostly performed by the group's PhD students and they were received with a lot of enthusiasm by the year 9 girls and praise from the department's outreach office. Given its reception and limited materials required, the outreach activity is currently adapted to be taken to schools.
Year(s) Of Engagement Activity 2019