Extreme suction attachment performance from specialised insects living in mountain streams (Diptera: Blephariceridae)
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Abstract
Suction is widely used by animals for strong controllable underwater adhesion but is less well understood than adhesion of terrestrial climbing animals. Here we investigate the attachment of aquatic insect larvae (Blephariceridae), which cling to rocks in torrential streams using the only known muscle-actuated suction organs in insects. We measured their attachment forces on well-defined rough substrates and found that their adhesion was less reduced by micro-roughness than that of terrestrial climbing insects. In vivo visualisation of the suction organs in contact with microstructured substrates revealed that they can mould around large asperities to form a seal. We have shown that the ventral surface of the suction disc is covered by dense arrays of microtrichia, which are stiff spine-like cuticular structures that only make tip contact. Our results demonstrate the impressive performance and versatility of blepharicerid suction organs and highlight their potential as a study system to explore biological suction mechanisms.
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This manuscript is in revision at eLife
The decision letter after peer review, sent to the authors on November 19 2020, follows.
Summary
Kang et al. eloquently describe the active suction organ that the larvae of aquatic insects of the Dipterian family Blephariceridae use to adhere robustly to complex surfaces. While the morphology of the mechanism has been reported previously, it's biomechanical adhesion function and performance across different substrates is unknown. The authors present three advances. First, they quantify the adhesion performance on rough, micro-rough, and smooth surfaces using an effective centrifugal setup. The ultimate adhesion tests show the larvae can resist shear forces up to 1100 times their body weight on smooth surfaces. Second, they visualize the suction function in vivo using interference reflection …
This manuscript is in revision at eLife
The decision letter after peer review, sent to the authors on November 19 2020, follows.
Summary
Kang et al. eloquently describe the active suction organ that the larvae of aquatic insects of the Dipterian family Blephariceridae use to adhere robustly to complex surfaces. While the morphology of the mechanism has been reported previously, it's biomechanical adhesion function and performance across different substrates is unknown. The authors present three advances. First, they quantify the adhesion performance on rough, micro-rough, and smooth surfaces using an effective centrifugal setup. The ultimate adhesion tests show the larvae can resist shear forces up to 1100 times their body weight on smooth surfaces. Second, they visualize the suction function in vivo using interference reflection microscopy. This reveals that small hair like microtrichia can enter gaps in the surface. Because the microtrichia are angled inward, the authors surmise that the microtrichia's angle and small size helps increase adhesion contact area on rough surfaces. Finally, they compare the adhesion performance of the Blephariceridae larvae to other species, showing it is 3-10 times greater than found in stick insects. The finding that the larvae have such high attachment forces is impressive and the study offers new biological insights that may inspire engineers to invent new underwater suction mechanisms.
Essential Revisions
Although the reviewers were generally appreciative of the well-written manuscript and the remarkable performance reported for the active suction mechanism, the consensus is that the mechanism itself is not described in sufficient detail for the reader to fully appreciate the advance. Hence the main critiques focus on helping the authors to further flesh out the mechanism and report it in more mechanistic detail like how other adhesion mechanism are described functionally across the biomechanical literature. Further the presentation of the figures does not meet graphic design clarity standards essential to inform eLife's broad readership. To provide guidance, we list the following essential revisions.
The introduction states that the suction organs have been observed, however, the manuscript does not communicate the observed mechanism as one would expect in the biomechanical adhesion literature. Instead it reports the measurements of the force and a suggestion that the microtrichia may be involved. We were hoping to find a quantitative report of the mechanism integrating the force data and microscopy images into biomechanical diagrams and to the extent possible, equations, that capture and communicate the mechanism as quantitatively as possible. Whereas we are not requesting further measurements, because the performance of the mechanism is well documented, we do ask a more in-depth biomechanical analysis that spells out the mechanism in a way it can be compared to the other classic mechanisms that the authors compare to. If this requires some additional measurements to inform the model, those efforts would be well worth it. In case the authors can use a mechanistic analysis lead, we recommend reviewing a couple of papers. E.g. Jeffries, Lindsie, and David Lentink. "Design Principles and Function of Mechanical Fasteners in Nature and Technology." Applied Mechanics Reviews 72.5 (2020). Or any other review or research paper that the authors find more useful.
Please clarify if the experiments are done in air or underwater. We consider underwater as most appropriate; at minimum the surface should be wetted. The authors mention that the Stefan adhesion forces underwater would be higher than in air, but it's not clear if that statement pertains to the experiment. Please provide a full clarification, and in case the experiments were performed in air we would prefer to see them performed in water. If this is not possible, the manuscript should be entirely transparent on this matter so the reader can evaluate the precise merit of this study and its limitations fully.
We found the images confusing at times. To resolve this we would like to see clear schematics (avatars) that ground the reader's perspective in all figures.
Considering eLife's broad multidisciplinary readership and the appeal of this study for bioinspired designers and engineers, Fig 1d,e has to provide better anatomical readability. Please assume a Biology and Engineering undergrad level for the first figure, ensuring all definitions and anatomical names can be fully comprehended without reference to other literature. Please provide clear connections to the different views and perspectives presented in the panels leveraging graphic design to the benefit of the interested reader not familiar with insect morphology.
Likewise, Fig 2 is also confusing. A schematic is in order to show the reader what they are looking at, how the images relate, and why they matter (significance) for understanding the main findings reported in this manuscript.
Fig 3 clearly shows that course-rough surfaces provide far less adhesion force. We wonder, are there any images similar to Fig 6 showing that the microtrichia cannot enter the gaps? To comprehend what causes the differences, we would like to see a report of the length scale of the microtrichia compared to that of the gap's dimensions, both for the rough and micro rough surfaces. To clarify this in a universal fashion, please consider reporting gap size non-dimensionally based on the relevant microtrichia length scale. More discussion of the relevant length scales would help bring the force measurements and the observations of the microtrichia together.
Fig 6 is an important figure, so it would help the reader to more easily grasp the viewing perspective using diagrams and avatars. I panel a, a schematic should clearly define the suction disc fringe and the perspective shown. What part is the suction disc and what is the length scale of this image compared to the suction disc? Also, it would be useful if the columns of the microstructure could all be aligned for clarity.
Currently, the authors provide an estimate of the shear stress. It would be helpful to also include the normal stress based on the normal force data on smooth surfaces for lugubris. It would be informative for the reader to know if it exceeds 1 atm. If so, that is a very interesting finding. Please report and discuss what you find in the revised manuscript.
Discussion: Please include a comparison of the magnitude of shear and normal stress that this suction mechanism creates with that of other organisms. Currently the comparison is done with force per body weight, which is biologically relevant. However, reporting stress provides an objective bio-mechanistic perspective on adhesion performance.
Discussion, Ln 300: The suggestion that the inward-facing microtrichia may function to prevent inward slipping of the suction cup is interesting. Please discuss the tradeoff between smooth and micro-rough surfaces: is it possible that on micro-rough surfaces the microtrichia are better able to resist slip, but on smooth surfaces, the seal is better? And if so, this would suggest the effect of a better seal is more important than preventing slip, since performance is better on smooth surfaces? In-vivo visualization during failure would be very informative (in future work).
Please discuss why there may be an intricate branching of the fan-fibres into the microtrichia. E.g. in the gecko, the branched tendons insert into the lamella, supporting the large tensile loads applied to the adhesive. However, here it is less clear if large tensile loads would be applied to the microtrichia. It seems logical that applying large normal loads to the suction cup should be done at its centre, resulting in decreased pressure if no slip occurs (as opposed to applying the normal force to the rim, which would not decrease pressure). So, this would not explain the intricate network of fan-fibres. However, for shear loads, it could make more sense: pulling in shear would engage the microtrichia on the far side of the cup, and the fan-fibres could help transmit this tension. It might be worth thinking this through and discussing the outcome in the paper to strengthen the mechanistic analysis.
We would be excited to learn if the authors have thoughts on the slight curvature of the microtrichia and how it may be involved in the adhesion mechanism. In case this is purely speculative, this could go into the last paragraph of the paper, alternatively it could go into the biomechanical model of the mechanism.
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