Subdivision of the neotropical Prisopodinae Brunner von Wattenwyl, 1893 based on features of tarsal attachment pads (Insecta, Phasmatodea)

The euplantulae of species from all five genera of the Prisopodinae Brunner von Wattenwyl, 1893 were examined using scanning electron microscopy with the aim to reveal the significance of attachment pads regarding their phylogenetic relationships. The split into the conventional two sister groups is supported by the two-lobed structure of the euplantulae with a smooth surface in the Prisopodini and a nubby surface microstructure in the Paraprisopodini. The two lineages are well distinguishable by this feature, as well as by the shape of the euplantulae themselves. The functional importance of the attachment pad surface features is discussed

The exceptional attachment ability of the ectoparasitic bee louse Braula coeca (Diptera, Braulidae) on the honeybee

Bee lice (Braulidae) are small parasitic flies, which are adapted to live on their bee host. As such, the wingless Braula coeca is a parasite of the common honey bee Apis mellifera and it is well adapted to attach to its hairy surface. The attachment system of B. coeca provides a secure grip on the fine setae of the bee. This is crucial for the parasite survival, as detachment from the host is fatal for the bee louse. The feet morphology of B. coeca is well adapted to the challenging bee surface, notably by strongly broadened claws, which are split into a high number of comb-like teeth, perfectly matching the diameter of the bee hairs. Based on microscopy observations, both the morphology and material composition of the tarsi of B. coeca are characterized in detail. Using high-speed video analysis, we combine the morphology data on the attachment system with a behavioural context. Furthermore, we directly measured the attachment forces generated by the bee lice in contact with the host. In particular, the claws are involved in attachment to the host, as the interstices between the teeth-like spines allow for the collection of several hairs and generate strong friction, when the hairs slip to the narrow gap between the spines. The overall morphology of the tarsus produces strong attachment, with average safety factors (force per body weight) around 1130, and stabilizes the tarsal chain with lateral stoppers against overflexion, but also allows for the fast detachment by the tarsal chain torsion.Deutsche Forschungsgemeinschaft; Human Frontier Science Program and the National Research Foundation.https://onlinelibrary.wiley.com/journal/13653032hj2021Zoology and Entomolog

Convergent Evolution of Adhesive Properties in Leaf Insect Eggs and Plant Seeds: Cross-Kingdom Bioinspiration

Plants and animals are often used as a source for inspiration in biomimetic engineering. However, stronger engagement of biologists is often required in the field of biomimetics. The actual strength of using biological systems as a source of inspiration for human problem solving does not lie in a perfect copy of a single system but in the extraction of core principles from similarly functioning systems that have convergently solved the same problem in their evolution. Adhesive systems are an example of such convergent traits that independently evolved in different organisms. We herein compare two analogous adhesive systems, one from plants seeds and one from insect eggs, to test their properties and functional principles for differences and similarities in order to evaluate the input that can be potentially used for biomimetics. Although strikingly similar, the eggs of the leaf insect Phyllium philippinicum and the seeds of the ivy gourd Coccinia grandis make use of different surface structures for the generation of adhesion. Both employ a water-soluble glue that is spread on the surface via reinforcing fibrous surface structures, but the morphology of these structures is different. In addition to microscopic analysis of the two adhesive systems, we mechanically measured the actual adhesion generated by both systems to quantitatively compare their functional differences on various standardized substrates. We found that seeds can generate much stronger adhesion in some cases but overall provided less reliable adherence in comparison to eggs. Furthermore, eggs performed better regarding repetitive attachment. The similarities of these systems, and their differences resulting from their different purposes and different structural/chemical features, can be informative for engineers working on technical adhesive systems

Attachment Performance of Stick Insects (Phasmatodea) on Plant Leaves with Different Surface Characteristics

Herbivorous insects and plants exemplify a longstanding antagonistic coevolution, resulting in the development of a variety of adaptations on both sides. Some plant surfaces evolved features that negatively influence the performance of the attachment systems of insects, which adapted accordingly as a response. Stick insects (Phasmatodea) have a well-adapted attachment system with paired claws, pretarsal arolium and tarsal euplantulae. We measured the attachment ability of Medauroidea extradentata with smooth surface on the euplantulae and Sungaya inexpectata with nubby microstructures of the euplantulae on different plant substrates, and their pull-off and traction forces were determined. These species represent the two most common euplantulae microstructures, which are also the main difference between their respective attachment systems. The measurements were performed on selected plant leaves with different properties (smooth, trichome-covered, hydrophilic and covered with crystalline waxes) representing different types among the high diversity of plant surfaces. Wax-crystal-covered substrates with fine roughness revealed the lowest, whereas strongly structured substrates showed the highest attachment ability of the Phasmatodea species studied. Removal of the claws caused lower attachment due to loss of mechanical interlocking. Interestingly, the two species showed significant differences without claws on wax-crystal-covered leaves, where the individuals with nubby euplantulae revealed stronger attachment. Long-lasting effects of the leaves on the attachment ability were briefly investigated, but not confirmed

Characterization of Morphologically Distinct Components in the Tarsal Secretion of <i>Medauroidea extradentata</i> (Phasmatodea) Using Cryo-Scanning Electron Microscopy

Attachment to the substrate is an important phenomenon that determines the survival of many organisms. Most insects utilize wet adhesion to support attachment, which is characterized by fluids that are secreted into the interface between the tarsus and the substrates. Previous research has investigated the composition and function of tarsal secretions of different insect groups, showing that the secretions are likely viscous emulsions that contribute to attachment by generating capillary and viscous adhesion, leveling surface roughness and providing self-cleaning of the adhesive systems. Details of the structural organization of these secretions are, however, largely unknown. Here, we analyzed footprints originating from the arolium and euplantulae of the stick insect Medauroidea extradentata using cryo-scanning electron microscopy (cryo-SEM) and white light interferometry (WLI). The secretion was investigated with cryo-SEM, revealing four morphologically distinguishable components. The 3D WLI measurements of the droplet shapes and volumes over time revealed distinctly different evaporation rates for different types of droplets. Our results indicate that the subfunctionalization of the tarsal secretion is facilitated by morphologically distinct components, which are likely a result of different proportions of components within the emulsion. Understanding these components and their functions may aid in gaining insights for developing adaptive and multifunctional biomimetic adhesive systems

Leaves that walk and eggs that stick: comparative functional morphology and evolution of the adhesive system of leaf insect eggs (Phasmatodea: Phylliidae)

Abstract Phylliidae are herbivorous insects exhibiting impressive cryptic masquerade and are colloquially called “walking leaves”. They imitate angiosperm leaves and their eggs often resemble plant seeds structurally and in some cases functionally. Despite overall morphological similarity of adult Phylliidae, their eggs reveal a significant diversity in overall shape and exochorionic surface features. Previous studies have shown that the eggs of most Phylliidae possess a specialised attachment mechanism with hierarchical exochorionic fan-like structures (pinnae), which are mantled by a film of an adhesive secretion (glue). The folded pinnae and glue respond to water contact, with the fibrous pinnae expanding and the glue being capable of reversible liquefaction. In general, the eggs of phylliids appear to exhibit varying structures that were suggested to represent specific adaptations to the different environments the eggs are deposited in. Here, we investigated the diversity of phylliid eggs and the functional morphology of their exochorionic structure. Based on the examination of all phylliid taxa for which the eggs are known, we were able to characterise eleven different morphological types. We explored the adhesiveness of these different egg morphotypes and experimentally compared the attachment performance on a broad range of substrates with different surface roughness, surface chemistry and tested whether the adhesion is replicable after detachment in multiple cycles. Furthermore, we used molecular phylogenetic methods to reconstruct the evolutionary history of different egg types and their adhesive systems within this lineage, based on 53 phylliid taxa. Our results suggest that the egg morphology is congruent with the phylogenetic relationships within Phylliidae. The morphological differences are likely caused by adaptations to the specific environmental requirements for the particular clades, as the egg morphology has an influence on the performance regarding the surface roughness. Furthermore, we show that different pinnae and the adhesive glue evolved convergently in different species. While the evolution of the Phylliidae in general appears to be non-adaptive judging on the strong similarity of the adults and nymphs of most species, the eggs represent a stage with complex and rather diverse functional adaptations including mechanisms for both fixation and dispersal of the eggs

Description of the observed types of attachment microstructures from Versatility of Turing patterns potentiates rapid evolution in tarsal attachment microstructures of stick and leaf insects (Phasmatodea)

In its evolution, the diverse group of stick and leaf insects (Phasmatodea) has undergone a rapid radiation. These insects evolved specialized structures to adhere to different surfaces typical for their specific ecological environments. The cuticle of their tarsal attachment pads (euplantulae) is known to possess a high diversity of attachment microstructures (AMS) which are suggested to reflect ecological specializations of different groups within phasmids. However, the origin of these microstructures and their developmental background remain largely unknown. Here, based on the detailed scanning electron microscopy study of pad surfaces, we present a theoretical approach to mathematically model an outstanding diversity of phasmid AMS using the reaction–diffusion model by Alan Turing. In general, this model explains pattern formation in nature. For the first time, we were able to identify eight principal patterns and simulate the transitions among these. In addition, intermediate transitional patterns were predicted by the model. The ease of transformation suggests a high adaptability of the microstructures that might explain the rapid evolution of pad characters. We additionally discuss the functional morphology of the different microstructures and their assumed advantages in the context of the ecological background of species

Taxon list from Versatility of Turing patterns potentiates rapid evolution in tarsal attachment microstructures of stick and leaf insects (Phasmatodea)

Table S3. List of phasmatodean species examined in this study. The distribution and the current taxonomical placement are stated, as well as the pattern type of attachment microstructures on the euplantulae determined by the modelling

Data_Sheet1_The Evolution of Tarsal Adhesive Microstructures in Stick and Leaf Insects (Phasmatodea).ZIP

<p>Insects have developed specialized structures on their feet for adhering to surfaces, with stick and leaf insects or Phasmatodea exhibiting an unexpectedly high diversity of these structures. In Phasmatodea, attachment on different substrates is achieved by two types of pads on the legs: the euplantulae on the tarsomeres and the arolium on the pretarsus. The euplantulae are adhesive structures capable of adaptability to the substrate profile and generation of the required attachment strength. The diversity of euplantular microstructures of 56 species that represent all major lineages recognized within Phasmatodea and the whole biogeographical distribution of the group are examined using scanning electron microscopy (SEM). Nine different types of attachment structures can be distinguished whereby one, the nubby type, can be further divided into three different distinct types based on the specific ratio of each conical outgrowth. We mapped the morphological data from the SEM onto a phylogenetic tree we reconstructed based on molecular data. Previously, the evolution of different adhesive microstructures (AMs) on these pads has been suggested to reflect phylogenetic groups. However, different types of AMs are found within monophyletic groups, and our ancestral character state reconstruction suggests smooth euplantulae in the ground pattern of Euphasmatodea and multiple independent origins of other forms. The type of AM appears to be strongly associated with ecomorphs, e.g., smooth euplantular surfaces are more frequently found in tree-dwellers than in ground-dwellers, whilst the attachment pads of ground-dwelling species primarily bear conical cuticular outgrowths (nubby euplantulae).</p