the choreography of wing folding

    Generally speaking, insects have two sets of wings. Front wings and hind wings. As different insect groups evolved there have been many modifications to this configuration. From a bioinspiration perspective, it is interesting to consider how many possibilities have been explored through the process of evolution. For example, dragonfly wings are kept in a constant position perpendicular to the body at all times. 

Dragonfly - Image credit: Luc Viatour

     

    Other insects, such as cockroaches, position the wings flat over the back of their body when not in use. Ants, bees, and wasps have hook-like structures (called hamuli) on the front side of the hind wing that fit in a groove on the back side of the front wing linking the two wings during flight. 

Wasp and close up of the junction between the front and hind wings showing the hook-like hamuli (Image credit)

    Beetles have evolved a different wing configuration. The front wings have evolved to be wing covers for the hind wings – they are not used for flight at all. The front wings of beetles, also known as elytra (singular = elytron), are hardened structures that lift up and out of the way when the beetle takes flight. The hind wings are tucked up and out of the way underneath the elytra, like a neatly folded shirt packed in your suit case. The wings, however, are spring loaded so they are ready for action when the elytra are lifted up.

June beetle (Phyllophaga sp.) getting ready for flight - elytra lifted up with hind wings unfolding (Image credit: Bev Wigney)

    Now there is a useful mechanism. Compact structures that can go from being neatly folded, out of the way under a protective covering, to springing into position to propel an insect in flight. Imagine flying down the street for coffee with wings that self-deployed from your backpack. Okay, probably not the current goal for beetle wing bioinspiration - but think of the possibilities. A group of Japanese scientists has already started. Using microcomputed tomography in combination with synthetically made translucent elytra, Saito et al. (2017) studied how ladybird beetles fold their wings up under their elytra. I could go through the play-by-play but I highly recommend you watch the video. The folding action is aided by movements of the abdomen in combination with supporting structures that create friction. The idea is that different aspects of the wing, such as the wing veins, are shaped in a particular way that allows the wing to fold while also spring loading it for deployment. Maybe some of you saw this segment on 60 minutes – one of many ways engineers can draw inspiration from insect folding and deployment mechanisms.

    Of course, Saito and colleagues were not the first to notice the incredible wing folding mechanisms of beetles. One of the earliest pioneers of wing folding in beetles was William Trowbridge Merrifield Forbes (1885 – 1968). W.T.M. Forbes published many papers on beetles and butterflies. In 1924, he published a paper titled “How a beetle folds its wings” where he provided detailed descriptions of wing folding mechanisms based on dried specimens he started collecting as a child. In 1926, Forbes followed up with “The wing folding patterns of the Coleoptera” (Coleoptera = the scientific name for beetles), which was a more extensive treatise using specimens from the Cornell University Insect Collection. In this paper, he described a ‘fundamental plan’ such that “The folding patterns of practically all beetles prove to be derivable by relatively simple modifications from a single fundamental plan…” (p. 42). Inferring this plan from the specimens available reveals the flexible and ingenious mind of an evolutionary morphologist. He went on to describe this plan, and then remarked on the deviations exhibited by all the different beetle groups, of which there are many. The paper was 27 pages long and the last three words were: (To be continued).

Figure 1 from Forbes (1926) - Journal of the New York Entomological Society 34, pgs. 42-68). PDF courtesy of the Biodiversity Heritage Library.

    Forbes’ publications also included a bit of scientific sleuthing. Unlike my scientific sleuthing, which typically goes back to the early 1900’s (although last time it went back to the early 1700’s), Forbes took an investigation of a silkworm moth back to Pliny the Elder (AD 77) and Aristotle (BC 384 – 322). One comment I found particularly interesting was: “Pliny is of course beyond saving by any mere definition”.

    I would love nothing more than to trade in my car for a pair of self-deployable, beetle inspired wings to meet up with Pliny the Elder.

adhesion anniversary

    I have been working on this post for over two months. The existence of a piece of writing that I don’t love has caused writer’s block, procrastination, and a long hiatus in my blog posting activity. The options were to 1) trash it or, 2) make it work. This is my attempt to make it work. I don’t give up easily. We’ll see if it pays off.

    For the 1+ year anniversary of this blog (which was in January), I have chosen my favorite subject. Adhesion. I seem to have a thing for adhesion. Or maybe adhesion has a thing for me. It may just be that adhesion has been a hard problem for humans to solve, and evolution has a time advantage we must necessarily draw inspiration from. I had never really thought about adhesion much before. But once you do, it is clear there are a lot of different organisms living in diverse habitats that have evolved attachment mechanisms. We have talked about adhesive adaptations in plant seeds that allow them to stick to passersby and mobilize away from the mother plant (dispersal). We also discussed adhesion in parasitic tapeworms that allows the worm to anchor itself to and extract nutrients from the intestinal lining of its host (feeding). Today we are going to talk about adhesion from the perspective of mussels. The mussel attachment mechanism is like the tapeworm in that it uses adhesion as an anchoring system in a fluid environment, the difference is it anchors itself to an impenetrable substrate in a desirable real estate location.

Mytilus edilus in a tide pool (Photo credit: Andreas Trepte, www.photo-natur.net)

     
    Mussels in the genus Mytilus have a special morphological character for attachment. The byssus. The byssus is generated after the larval stage in a process called byssogenesis. Byssogenesis. Throw that one out there when you want to sound smart. Or crazy. The structure itself is not composed of living cells, but is secreted by the living portion of the mussel. Research on the byssus has focused on two species of mussel, the common mussel and the California mussel. The common (or blue) mussel (Mytilus edulis) was described by our friend Linneaus in 1758, and can be found along coastlines in the northern Atlantic Ocean. The California mussel (Mytilus californianus) was described by Timothy Abbot Conrad in 1837. Conrad was a geologist that described many species of mussel on the east and west coasts of the United States.

    Mussels have an aquatic larval stage that is mobile and swims through the water. The adult stage becomes stationary after attaching to rocks, or other mussels, in intertidal zones. This is where the byssus enters. The intertidal zone is a dynamic environment where waves provide nearly constant aeration and an influx of nutrients, with a corresponding efflux of waste products. This energetic habitat requires an advanced adhesion mechanism that withstands both water intrusion as well as the force of the waves.

    As I started researching the mussel byssus, it became clear to me that this rabbit hole was deeper than most I have gone down in the past. Usually when I start the process of following references back from the bioinspiration of the day (or month(s)), I find morphological and taxonomic studies conducted with no eye on future application. In this case, however, some of the early papers on mussel attachment were not conducted by organismal biologists, but by bioprospecting scientists. In a 1971 report by Engel, Hillman, Neat, and Quinby, published by the National Institutes of Dental Research at the National Institutes of Health (accessed through UCSD libraries), the citations for the original papers describing mussel attachment were very old. The first one was from 1711 – Histoire de l’ Academie Royale des Sciences by R.A.F. Reaumer. !. 1711. I don’t think we have ever traced a paper back that far. The mussel attachment study by Reaumer piqued the interest of dentists in the early 1970’s for potential applications as a glue in dental surgery. Mussels continue to captivate interest today and are inspiring the development of mussel mimetic polymers.

    The generation and application of mussel inspired polymers was reviewed in a paper by Bruce Lee (different than this Bruce Lee) and colleagues (Lee et al., 2011). Lee et al. simplify the problem for us at the beginning of the paper:

“Water, particularly saline water, limits what can bind and where. At a simplistic molecular level, Coulomb’s law for electrostatic interactions predicts that the interaction energy for two point charges QaQb is −QaQb/4πεr, where ε is the dielectric constant and r is the interionic distance. An electrostatic interaction between opposite charges will be only 1/80 as strong in water (ε = 80) as it is under vacuum (ε = 1). Actually, the interaction is often further diminished because r will also be increased due to strong solvation of ions such as Mg2+ and Li+ by H₂O (2).”

    In other words, adhesion in salt water is difficult. Mussels already knew this. One of the crazy things scientists discovered through continued study of the byssus is that the attachment mechanism is more like the webbing that comes out of Spider-Man’s hands (is that morphology right? I am not a superhero expert) than the head of the tapeworm embedding itself into its host intestinal lining. The byssus is not made up of living cells, it is a matrix of proteinaceous threads that are controlled by muscles inside the mussel. 

Figure 4 from Lee et. al (2011) illustrating the ultrastructure of byssus attachment.

    
    Current applications of mussel inspired adhesion technology have since expanded beyond surgical applications. The plan of attack thus far has been to mimic the structure of the proteins using synthetic polymers. In the process of doing this engineers have hybridized two bioinspired technologies, gecko feet and the mussel byssus. The pads of gecko feet deserve their own post but suffice it to say that they are sticky when dry, but not when wet. If gecko inspired technology (terrestrially based) is combined with mussel inspired technology (aquatically based) the result is an adhesive mechanism that overcomes the simple difficulties of adhesion in water elegantly explained above. 

  

    Even more recently, Bruce Lee was awarded a grant by the Office of Naval Research to develop an underwater adhesive that could be controlled by electricity. The Naval applications for such technology are many and include a mechanism to attach devices to ships, or provide an additional level of control to aquatic robots exploring the sea floor or rocky intertidal zones.

Appendix I – For the chemically inspired.

Figure 5 from Lee et al. 2011. Figure legend: “Chemical structure of a Dopa-rich mussel foot protein (mfp). Shown is mfp-3 (variant f) sequence from Mytilus edulis. The protein functions at the interface between the plaque and the substratum. Dopa residues are highlighted in red; the sequence contains nearly as many guanidinium groups (4-hydroxyarginines; purple) as Dopa residues. Results from Papov et al. (26).”