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The tymbal organ of Bena bicolorana. (A) Caudal view of a cross section of the male abdomen at the level of the tymbal organ (stained with Heidenhain's Azan). The tymbal muscles insert dorso-medially on the tymbal frame and extend dorsolaterally . A circular region in the middle of both membranes stains weakly blue. The dark (and weakly blue-stained) structure (arrow) on the dorso-lateral part of the tymbal frame corresponds to the resilin-containing cylinder-like structure in Pseudoips prasinana. Scale bar, 1.4 mm. (B) At greater magnification, the striae on the medial ventral part of the tymbals can be clearly seen. Scale bar, 0.4 mm. (C) Scanning electron micrograph of the area of the left tymbal membrane containing the striae. Seven striae are visible in this preparation. Scale bar, 0.1 mm.
Source publication
Male moths of the chloephorine species Pseudoips prasinana and Bena bicolorana produce clicks (approximately 100 dB peSPL at 10 cm) using ventral tymbal organs located in a cleft in the second abdominal sternite. Large muscles insert on the dorsal part of the tymbal frame and rhythmically flex a thin sheet of cuticle. Normally, each sound-productio...
Contexts in source publication
Context 1
... B. bicolorana, both in the three specimens we caught and in some dried museum specimens from the Zoological Museum at the University of Copenhagen. The overall structure of the tymbal organ is the same as in male P. prasinana, but B. bicolorana has striae on the ventro-medial part of the tymbals, whereas the same area in P. prasinana is smooth (Fig. 3). Seven or eight striae were clearly visible in all the B. bicolorana males we examined (Fig. ...
Context 2
... the Zoological Museum at the University of Copenhagen. The overall structure of the tymbal organ is the same as in male P. prasinana, but B. bicolorana has striae on the ventro-medial part of the tymbals, whereas the same area in P. prasinana is smooth (Fig. 3). Seven or eight striae were clearly visible in all the B. bicolorana males we examined (Fig. ...
Context 3
... also has a pronounced structure containing resilin lateral to the tymbal but, compared with P. prasinana, this structure is considerably smaller and placed more dorsally. The large dorsal tymbal muscles in B. bicolorana attach to a smaller, more lateral area of the tergum compared with those of P. prasinana, and they appear less fan-shaped (Fig. 3A). The ventral longitudinal muscles are very similar in both species. Furthermore, B. bicolorana has two minor muscles attached to the dorsal medial part of the tymbal frame extending caudad. Corresponding muscles are seen in P. ...
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... common to the large clicks of both species. The fact that B. bicolorana emits series of small clicks that may or may not coincide with the large clicks indicates that these are produced by an independent mechanism which may be controlled by another set of muscles, causing sequential buckling of the small striae on the medial part of the tymbals (Fig. 3B,C), which then directly or indirectly emit the small clicks. We recorded up to 14 small clicks in one buckling phase. Since there are only seven or eight striae on each side, this indicates that both the left and right tymbals are also active simultaneously in B. bicolorana. Tymbal organs with striae have been found in other ...
Citations
... Flexion lines are stripes of flexible cuticle that can act as hinges or joints and are crucial for camber shape adaptation (19). Resilin, a rubber-like material that can be found as an additional constituent in cuticle materials, is typically detected along wing folding and flexion lines, for instance, on the wings of honeybees and earwigs (20,21), and it has been reported to be present in the abdominal tymbals of Noctuoidea (22). Resilin is characterized by its low energy loss under dynamic loading (23) and can be observed in cuticle materials using laser scanning confocal microscopy (LSCM) (24,25). ...
The loss of elastic stability (buckling) can lead to catastrophic failure in the context of traditional engineering structures. Conversely, in nature, buckling often serves a desirable function, such as in the prey-trapping mechanism of the Venus fly trap ( Dionaea muscipula ). This paper investigates the buckling-enabled sound production in the wingbeat-powered (aeroelastic) tymbals of Yponomeuta moths. The hindwings of Yponomeuta possess a striated band of ridges that snap through sequentially during the up- and downstroke of the wingbeat cycle—a process reminiscent of cellular buckling in compressed slender shells. As a result, bursts of ultrasonic clicks are produced that deter predators (i.e. bats). Using various biological and mechanical characterization techniques, we show that wing camber changes during the wingbeat cycle act as the single actuation mechanism that causes buckling to propagate sequentially through each stria on the tymbal. The snap-through of each stria excites a bald patch of the wing’s membrane, thereby amplifying sound pressure levels and radiating sound at the resonant frequencies of the patch. In addition, the interaction of phased tymbal clicks from the two wings enhances the directivity of the acoustic signal strength, suggesting an improvement in acoustic protection. These findings unveil the acousto-mechanics of Yponomeuta tymbals and uncover their buckling-driven evolutionary origin. We anticipate that through bioinspiration, aeroelastic tymbals will encourage novel developments in the context of multi-stable morphing structures, acoustic structural monitoring, and soft robotics.
... Males of the nocturnal Nolidae (Chloephorinae) moths Bena bicolorana and Pseudoips prasinana produce loud ultrasonic clicks with ventral tymbal organs located on the second abdominal sternite. The positive correlation between microtymbal structure and the number of clicks in these two species is similar to that in tiger moths: B. bicolorana, which has corrugated tymbals with striae on the medial part, produces a series of clicks for each buckling of the tymbal, whereas P. prasinana, which has smooth tymbals, produces a single click for each buckling of the tymbal (Skals and Surlykke 1999;Dowdy and Conner 2019). It is suggested that male ultrasonic clicks in the two nolid species are used as calling songs to attract female moths although no direct observations or experiments have been conducted. ...
This chapter first touches on the taxonomic groups of insects that have been observed to tonic immobility. Although I have used the word “death feigning” in many of my previous papers, I used “tonic immobility (TI)” here as the same meaning as death feigning. Next, the two modes of insects the author discovered in our experiments with beetles, stationary and activity, are described. Individuals in the active mode do not TI, while individuals in the stationary mode TI. In other words, TI is a behavior with phenotypic plasticity. Eight factors are outlined as to what conditions cause this plasticity. Finally, I outline the results of direct and correlated responses in artificial selection for duration of TI on beetles as model materials. Using the selected strains, I will also present the results of experiments approaching a group of genes that control duration of TI and the stimuli that arouse from TI.
... Males of the nocturnal Nolidae (Chloephorinae) moths Bena bicolorana and Pseudoips prasinana produce loud ultrasonic clicks with ventral tymbal organs located on the second abdominal sternite. The positive correlation between microtymbal structure and the number of clicks in these two species is similar to that in tiger moths: B. bicolorana, which has corrugated tymbals with striae on the medial part, produces a series of clicks for each buckling of the tymbal, whereas P. prasinana, which has smooth tymbals, produces a single click for each buckling of the tymbal (Skals and Surlykke 1999;Dowdy and Conner 2019). It is suggested that male ultrasonic clicks in the two nolid species are used as calling songs to attract female moths although no direct observations or experiments have been conducted. ...
Coevolutionary adaptation leads to modifications of sensory physiology and behavioral responses of predators and prey. From the ecological point of view, insect hearing and acoustic behavior are an attractive study area for researchers in entomology, animal behavior, and neuroethology. Recent technical advances in sound-recording equipment and molecular techniques have contributed to understanding the evolution of acoustic communication, including sexual dialogue, intraspecific competition, and the interspecific arms race between predators (e.g., bats) and prey (e.g., moths). Singing male moths exploit ultrasound-induced freezing responses of potential female mates or unwelcome rival males to enhance mating success. Freezing responses to ultrasound by moths are originally an antipredator reaction to echolocating insectivorous bats. The aim of Chap. 5 is to provide a sensory-behavioral explanation of the freezing response of insects during predator–prey interaction.
... 222,223 Owing to its low stiffness, high resilience, and efficient energy storage, resilin plays an important role in the flight of fruit flies, jumping ability of fleas, and sound-producing organs of cicadas and moths. 222,[224][225][226][227][228][229][230][231][232][233][234] Resilins from various species of insects contain repeated sequence motif with high contents of hydrophobic side chains such as glycine, alanine, and proline, and especially with tyrosine residues. [235][236][237] Natural resilin from insect joints and tendons has been indicated to allow for the outstanding physical activities of insects and this type of resilin has been found to be composed of randomly orientated coiled polypeptide chains covalently crosslinked by the reactions between their tyrosine residues, with the resulting di-and trityrosine bonds contributing to the formation of a highly stable and flexible resilin network. ...
Proteins are fundamentally the most important macromolecules for biochemical, mechanical, and structural functions in living organisms. Therefore, they provide us with diverse structural building blocks for constructing various types of biomaterials, including an important class of such materials, hydrogels. Since natural peptides and proteins are biocompatible and biodegradable, they perform features advantageous for their use as the building blocks of hydrogels for biomedical applications. They display constitutional and mechanical similarities with the native extracellular matrix (ECM), and can be easily bio-functionalized via genetic and chemical engineering with features such as bio-recognition, specific stimulus-reactivity, and controlled degradation. This review aims to give an overview of hydrogels made up of recombinant proteins or synthetic peptides as the structural elements building the polymer network. A wide variety of hydrogels composed of protein or peptide building blocks with different origins and compositions—including β-hairpin peptides, α-helical coiled coil peptides, elastin-like peptides, silk fibroin, and resilin—have been designed up to date. In this review, the structures and characteristics of these natural proteins and peptides, with each of their gelation mechanisms, and the physical, chemical, and mechanical properties as well as biocompatibility of the resulting hydrogels are described. In addition, this review discusses the potential of using protein- or peptide-based hydrogels in the field of biomedical sciences, especially tissue engineering.
... The first mechanism is based on sound production. Moths not only perceive sounds, but some moths can also actively produce them by using parts of their abdomen [43], legs [44] or tegula and wings [45] to emit chirps and bursts of sound. In the family of Erebidae and Arctiidae, it is quite common that in the very last second of an attack those sounds are emitted by the moth. ...
... Among Lepidoptera, the Arctiinae are not alone in utilizing tymbals for sound production. A number of major lepidopteran lineages have convergently evolved tymbal or tymbal-like organs in order to produce sounds for courtship or defense (e.g., Geometridae [33]; Nolidae [34]; Lymantriinae [35]; Noctuidae [36]; Pyralidae [37]; Crambidae [38]; for an overview, see [39]). Similar structures can also be found in other insect lineages, including cicadas and other subgroups of Hemipterans [28][29][30][31]40]. ...
Background:
Acoustic signals are used by many animals to transmit information. Variation in the acoustic characteristics of these signals often covaries with morphology and can relay information about an individual's fitness, sex, species, and/or other characteristics important for both mating and defense. Tiger moths (Lepidoptera: Erebidae: Arctiinae) use modified cuticular plates called "tymbal organs" to produce ultrasonic clicks which can aposematically signal their toxicity, mimic the signals of other species, or, in some cases, disrupt bat echolocation. The morphology of the tymbal organs and the sounds they produce vary greatly between species, but it is unclear how the variation in morphology gives rise to the variation in acoustic characteristics. This is the first study to determine how the morphological features of tymbals can predict the acoustic characteristics of the signals they produce.
Results:
We show that the number of striations on the tymbal surface (historically known as "microtymbals") and, to a lesser extent, the ratio of the projected surface area of the tymbal to that of the thorax have a strong, positive correlation with the number of clicks a moth produces per unit time. We also found that some clades have significantly different regression coefficients, and thus the relationship between microtymbals and click rate is also dependent on the shared ancestry of different species.
Conclusions:
Our predictive model allows the click rates of moths to be estimated using preserved material (e.g., from museums) in cases where live specimens are unavailable. This has the potential to greatly accelerate our understanding of the distribution of sound production and acoustic anti-bat strategies employed by tiger moths. Such knowledge will generate new insights into the evolutionary history of tiger moth anti-predator defenses on a global scale.
... Resilin is a well-known elastomeric, structural protein normally present in the specialized regions of most insects' cuticle compartments to provide efficient energy storage and release in order to support mechanical function during jumping, flight, and sound production. [1][2][3][4] Naturally crosslinked resilin exhibits unique rubber-like features, including high resilience, reversible extensibility at large strains, and high-efficiency energy transfer. Although mechanically similar to other elastomeric proteins, compositionally, resilin is substantially more hydrophilic than natural elastins, collagens or silks. ...
Detailed understanding of the local structure–property relationships in soft biopolymeric hydrogels can be instrumental for applications in regenerative tissue engineering. Resilin-like polypeptide (RLP) hydrogels have been previously demonstrated as useful biomaterials with a unique combination of low elastic moduli, excellent resilience, and cell-adhesive properties. However, comprehensive mechanical characterization of RLP hydrogels under both low-strain and high-strain conditions has not yet been conducted, despite the unique information such measurements can provide about the local structure and macromolecular behavior underpinning mechanical properties. In this study, mechanical properties (elastic modulus, resilience, and fracture initiation toughness) of equilibrium swollen resilin-based hydrogels were characterized via oscillatory shear rheology, small-strain microindentation, and large-strain puncture tests as a function of polypeptide concentration. These methods allowed characterization, for the first time, of the resilience and failure in hydrogels with low polypeptide concentrations (<20 wt%), as the employed methods obviate the handling difficulties inherent in the characterization of such soft materials via standard mechanical techniques, allowing characterization without any special sample preparation and requiring minimal volumes (as low as 50 μL). Elastic moduli measured from small-strain microindentation showed good correlation with elastic storage moduli obtained from oscillatory shear rheology at a comparable applied strain rate, and evaluation of multiple loading-unloading cycles revealed decreased resilience values at lower hydrogel concentrations. In addition, large-strain indentation-to-failure (or puncture) tests were performed to measure large-strain mechanical response and fracture toughness on length scales similar to biological cells (∼10–50 μm) at various polypeptide concentrations, indicating very high fracture initiation toughness for high-concentration hydrogels. Our results establish the utility of employing microscale mechanical methods for the characterization of the local mechanical properties of biopolymeric hydrogels of low concentrations (<20 wt%), and show how the combination of small and large-strain measurements can provide unique insight into structure–property relationships for biopolymeric elastomers. Overall, this study provides new insight into the effects on local mechanical properties of polypeptide concentration near the overlap polymer concentration c* for resilin-based hydrogels, confirming their unique elastomeric features for applications in regenerative medicine.
... For example, resilin plays an important role in fl ight systems of insects, in particular in insects that use a wing beat with a low frequency (10-50 Hz) (see below). Resilin-containing exoskeleton structures have been described for various mechanical systems including leg joints (Gorb 1996 ;Neff et al. 2000 ), vein joints and membranous areas of insect wings (Gorb 1999 ;Haas et al. 2000a , b ), the foodpump of reduviid bugs (Edwards 1983 ), tymbal sound production organs of cicadas (Young and Bennet-Clark 1995 ;Bennet-Clark 1997 ) and moths (Skals and Surlykke 1999 ), abdominal cuticle of honey ant workers (Raghu Varman 1981 ) and termite queens (Raghu Varman 1980 ), the fulcral arms of the poison apparatus of ants (Raghu Varman and Hermann 1982 ) and the tendons of dragonfl y fl ight muscles and basal wing joints of locusts (as already mentioned above) (Andersen and Weis-Fogh 1964 ). In the following, some selected representative structures and systems with large proportions of resilin are highlighted, and their functions are described. ...
Resilin is an elastomeric protein typically occurring in exoskeletons of arthropods. It is composed of randomly orientated coiled polypeptide chains that are covalently cross-linked together at regular intervals by the two unusual amino acids dityrosine and trityrosine forming a stable network with a high degree of flexibility and mobility. As a result of its molecular prerequisites, resilin features exceptional rubber-like properties including a relatively low stiffness, a rather pronounced long-range deformability and a nearly perfect elastic recovery. Within the exoskeleton structures, resilin commonly forms composites together with other proteins and/or chitin fibres. In the last decades, numerous exoskeleton structures with large proportions of resilin have been described. In these structures, resilin has various functions. Today, resilin is known to be responsible for the generation of deformability and flexibility in membrane and joint systems, the storage of elastic energy in jumping and catapulting systems, the enhancement of adaptability to uneven surfaces in attachment and prey catching systems, the reduction of fatigue and damage in reproductive, folding and feeding systems and the sealing of wounds in a traumatic reproductive system. In addition, resilin is present in many compound eye lenses and is suggested to be a very suitable material for optical elements because of its transparency and amorphousness. The evolution of this remarkable functional diversity can be assumed to have only been possible because resilin exhibits a unique combination of different outstanding properties. In order to benefit from these properties in industrial and medical applications such as biosensor techniques and tissue engineering, various recombinant resilin-like polypeptides (RLPs) have been synthesised in the past few years. Due to their unusual multi-responsiveness and low toxicity and the possibility to tune their mechanical properties and to produce modular, chimeric RLPs with desired biological properties, RLPs have a wide field of potential applications and might replace many synthetic polymers in the future.
... For example , resilin plays an important role in flight systems of insects, in particular in insects that use a wing beat with a low frequency (10?50 Hz) (see below). Resilin-containing exoskeleton structures have been described for various mechanical systems including leg joints [40,50] , vein joints and membranous areas of insect wings [21,22,24], the food-pump of reduviid bugs [51], tymbal sound production organs of cicadas [52,53] and moths [54], abdominal cuticle of honey ant workers [55] and termite queens [56], the fulcral arms of the poison apparatus of ants [57] and the tendons of dragonfly flight muscles and basal wing joints of locusts (as already mentioned above) [5] . In the following, some selected representative structures and systems with large proportions of resilin are highlighted , and their functions are described. ...
Resilin is an elastomeric protein typically occurring in exoskeletons of arthropods. It is composed of randomly orientated coiled polypeptide chains that are covalently cross-linked together at regular intervals by the two unusual amino acids dityrosine and trityrosine forming a stable network with a high degree of flexibility and mobility. As a result of its molecular prerequisites, resilin features exceptional rubber-like properties including a relatively low stiffness, a rather pronounced long-range deformability and a nearly perfect elastic recovery. Within the exoskeleton structures, resilin commonly forms composites together with other proteins and/or chitin fibres. In the last decades, numerous exoskeleton structures with large proportions of resilin and various resilin functions have been described. Today, resilin is known to be responsible for the generation of deformability and flexibility in membrane and joint systems, the storage of elastic energy in jumping and catapulting systems, the enhancement of adaptability to uneven surfaces in attachment and prey catching systems, the reduction of fatigue and damage in reproductive, folding and feeding systems and the sealing of wounds in a traumatic reproductive system. In addition, resilin is present in many compound eye lenses and is suggested to be a very suitable material for optical elements because of its transparency and amorphousness. The evolution of this remarkable functional diversity can be assumed to have only been possible because resilin exhibits a unique combination of different outstanding properties.
... The elasticity of resilin is directly proportional to the level of hydration [39]. Resilin is stable when heated up to 125 8C and can withstand vibrations with the frequency of 4 kHz [3,32,40]. It is insoluble in water and nonpolar solvents [32]. ...
The elastomeric proteins elastin and resilin have been used extensively in the fabrication of biomaterials for tissue engineering applications due to their unique mechanical and biological properties. Tropoelastin is the soluble monomer component of elastin. Tropoelastin and resilin are both highly elastic with high resilience, substantial extensibility, high durability and low energy loss, which makes them excellent candidates for the fabrication of elastic tissues that demand regular and repetitive movement like the skin, lung, blood vessels, muscles and vocal folds. Combinations of these proteins with silk fibroin further enhance their biomechanical and biological properties leading to a new class of protein alloy materials with versatile properties. In this review, the properties of tropoelastin-based and resilin-based biomaterials with and without silk are described in concert with examples of their applications in tissue engineering.
